Skip to main content
Top
Published in: Molecular Cancer 1/2018

Open Access 01-12-2018 | Review

The hepatic pre-metastatic niche in pancreatic ductal adenocarcinoma

Authors: Demi S. Houg, Maarten F. Bijlsma

Published in: Molecular Cancer | Issue 1/2018

Login to get access

Abstract

Pancreatic ductal adenocarcinoma (PDAC) remains one of the most aggressive malignancies to date, largely because it is associated with high metastatic risk. Pancreatic tumors have a characteristic tendency to metastasize preferentially to the liver. Over the past two decades, it has become evident that the otherwise hostile milieu of the liver is selectively preconditioned at an early stage to render it more conducive to the engraftment and growth of disseminated cancer cells, a concept defined as pre-metastatic niche (PMN) formation. Pancreatic cancer cells exploit components of the tumor microenvironment to facilitate their migration out of the primary tumor, which often involves conversion of pancreatic cancer cells from an epithelial to a mesenchymal phenotype via the epithelial-to-mesenchymal transition. Pancreatic stellate cells and matrix stiffness have been put forward as major drivers of invasiveness in PDAC. Even before the onset of pancreatic cancer cell dissemination, soluble factors and extracellular vesicles secreted by the primary tumor, and possibly even premalignant lesions, help shape a supportive niche in the liver by providing vascular docking sites for circulating tumor cells, enhancing vascular permeability, remodeling the extracellular matrix and recruiting immunosuppressive inflammatory cells. Emerging evidence suggests that some of these tumor-derived factors may represent powerful diagnostic or prognostic biomarkers. Though our understanding of the mechanisms driving PMN formation in PDAC has expanded considerably, many outstanding questions and challenges remain. Further studies dissecting the molecular and cellular events involved in hepatic PMN formation in PDAC will likely improve diagnosis and open new avenues from a therapeutic standpoint.
Literature
2.
go back to reference Åkerberg D, Ansari D, Andersson R, Tingstedt B. The effects of surgical exploration on survival of unresectable pancreatic carcinoma: a retrospective case-control study. J Biomed Sci Eng. 2017;10:1–9.CrossRef Åkerberg D, Ansari D, Andersson R, Tingstedt B. The effects of surgical exploration on survival of unresectable pancreatic carcinoma: a retrospective case-control study. J Biomed Sci Eng. 2017;10:1–9.CrossRef
3.
go back to reference Paulson AS, Tran Cao HS, Tempero MA, Lowy AM. Therapeutic advances in pancreatic cancer. Gastroenterology. 2013;144:1316–26.PubMedCrossRef Paulson AS, Tran Cao HS, Tempero MA, Lowy AM. Therapeutic advances in pancreatic cancer. Gastroenterology. 2013;144:1316–26.PubMedCrossRef
4.
go back to reference Garrido-Laguna I, Hidalgo M. Pancreatic cancer: from state-of-the-art treatments to promising novel therapies. Nat Rev Clin Oncol. 2015;12:319–34.PubMedCrossRef Garrido-Laguna I, Hidalgo M. Pancreatic cancer: from state-of-the-art treatments to promising novel therapies. Nat Rev Clin Oncol. 2015;12:319–34.PubMedCrossRef
5.
go back to reference Almoguera C, Shibata D, Forrester K, Martin J, Arnheim N, Perucho M. Most human carcinomas of the exocrine pancreas contain mutant c-K-ras genes. Cell. 1988;53:549–54.PubMedCrossRef Almoguera C, Shibata D, Forrester K, Martin J, Arnheim N, Perucho M. Most human carcinomas of the exocrine pancreas contain mutant c-K-ras genes. Cell. 1988;53:549–54.PubMedCrossRef
6.
go back to reference Schutte M, Hruban RH, Geradts J, Maynard R, Hilgers W, Rabindran SK, Moskaluk CA, Hahn SA, Schwarte-Waldhoff I, Schmiegel W, et al. Abrogation of the Rb/p16 tumor-suppressive pathway in virtually all pancreatic carcinomas. Cancer Res. 1997;57:15. Schutte M, Hruban RH, Geradts J, Maynard R, Hilgers W, Rabindran SK, Moskaluk CA, Hahn SA, Schwarte-Waldhoff I, Schmiegel W, et al. Abrogation of the Rb/p16 tumor-suppressive pathway in virtually all pancreatic carcinomas. Cancer Res. 1997;57:15.
7.
go back to reference Hruban RH, Goggins M, Parsons J, Kern SE. Progression model for pancreatic cancer. Clin Cancer Res. 2000;6:8. Hruban RH, Goggins M, Parsons J, Kern SE. Progression model for pancreatic cancer. Clin Cancer Res. 2000;6:8.
8.
go back to reference Hingorani SR, Wang L, Multani AS, Combs C, Deramaudt TB, Hruban RH, Rustgi AK, Chang S, Tuveson DA. Trp53R127H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell. 2005;7:469–83.PubMedCrossRef Hingorani SR, Wang L, Multani AS, Combs C, Deramaudt TB, Hruban RH, Rustgi AK, Chang S, Tuveson DA. Trp53R127H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell. 2005;7:469–83.PubMedCrossRef
9.
go back to reference Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Wicha M, Clarke MF, Simeone DM. Identification of pancreatic cancer stem cells. Cancer Res. 2007;67:1030–7.PubMedCrossRef Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Wicha M, Clarke MF, Simeone DM. Identification of pancreatic cancer stem cells. Cancer Res. 2007;67:1030–7.PubMedCrossRef
10.
go back to reference Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science. 2008;321:1801–6.PubMedPubMedCentralCrossRef Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science. 2008;321:1801–6.PubMedPubMedCentralCrossRef
11.
go back to reference Burris HA 3rd, Moore MJ, Andersen J, Green MR, Rothenberg ML, Modiano MR, Cripps MC, Portenoy RK, Storniolo AM, Tarassoff P, et al. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J Clin Oncol. 1997;15:2403–13.PubMedCrossRef Burris HA 3rd, Moore MJ, Andersen J, Green MR, Rothenberg ML, Modiano MR, Cripps MC, Portenoy RK, Storniolo AM, Tarassoff P, et al. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J Clin Oncol. 1997;15:2403–13.PubMedCrossRef
12.
go back to reference Von Hoff DD, Ervin T, Arena FP, Chiorean G, Infante J, Moore M, Seay T, Tjulandin SA, Ma WW, Saleh MN, et al. Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N Engl J Med. 2013;369:1691–703.PubMedPubMedCentralCrossRef Von Hoff DD, Ervin T, Arena FP, Chiorean G, Infante J, Moore M, Seay T, Tjulandin SA, Ma WW, Saleh MN, et al. Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N Engl J Med. 2013;369:1691–703.PubMedPubMedCentralCrossRef
13.
go back to reference Neoptolemos JP, Palmer DH, Ghaneh P, Psarelli EE, Valle J, Halloran CM, Faluyi O, O'Reilly DA, Cunningham D, Wadsley J, et al. Comparison of adjuvant gemcitabine and capecitabine with gemcitabine monotherapy in patients with resected pancreatic cancer (ESPAC-4): a multicentre, open-label, randomised, phase 3 trial. Lancet. 2017;389:1011–24.PubMedCrossRef Neoptolemos JP, Palmer DH, Ghaneh P, Psarelli EE, Valle J, Halloran CM, Faluyi O, O'Reilly DA, Cunningham D, Wadsley J, et al. Comparison of adjuvant gemcitabine and capecitabine with gemcitabine monotherapy in patients with resected pancreatic cancer (ESPAC-4): a multicentre, open-label, randomised, phase 3 trial. Lancet. 2017;389:1011–24.PubMedCrossRef
14.
go back to reference Paget S. The distribution of secondary growths in cancer of the breast. Lancet. 1889;133:571–3.CrossRef Paget S. The distribution of secondary growths in cancer of the breast. Lancet. 1889;133:571–3.CrossRef
15.
go back to reference Iacobuzio-Donahue CA, Fu B, Yachida S, Luo M, Abe H, Henderson CM, Vilardell F, Wang Z, Keller JW, Banerjee P, et al. DCP4 gene status of the primary carcinoma correlates with patterns of failure in patients with pancreatic cancer. J Clin Oncol. 2009;27:1806–13.PubMedPubMedCentralCrossRef Iacobuzio-Donahue CA, Fu B, Yachida S, Luo M, Abe H, Henderson CM, Vilardell F, Wang Z, Keller JW, Banerjee P, et al. DCP4 gene status of the primary carcinoma correlates with patterns of failure in patients with pancreatic cancer. J Clin Oncol. 2009;27:1806–13.PubMedPubMedCentralCrossRef
16.
go back to reference Yachida S, White CM, Naito Y, Zhong Y, Brosnan JA, Macgregor-Das AM, Morgan RA, Saunders T, Laheru DA, Herman JM, et al. Clinical significance of the genetic landscape of pancreatic cancer and implications for identification of potential long-term survivors. Clin Cancer Res. 2012;18:6339–47.PubMedPubMedCentralCrossRef Yachida S, White CM, Naito Y, Zhong Y, Brosnan JA, Macgregor-Das AM, Morgan RA, Saunders T, Laheru DA, Herman JM, et al. Clinical significance of the genetic landscape of pancreatic cancer and implications for identification of potential long-term survivors. Clin Cancer Res. 2012;18:6339–47.PubMedPubMedCentralCrossRef
17.
go back to reference Lyden D, Welch DR, Psaila B, editors. Cancer metastasis: biologic basis and therapeutics. Cambridge and New York: Cambridge University Press; 2011. Lyden D, Welch DR, Psaila B, editors. Cancer metastasis: biologic basis and therapeutics. Cambridge and New York: Cambridge University Press; 2011.
18.
go back to reference Peinado H, Zhang H, Matei IR, Costa-Silva B, Hoshino A, Rodrigues G, Psaila B, Kaplan RN, Bromberg JF, Kang Y, et al. Pre-metastatic niches: organ-specific homes for metastases. Nat Rev. 2017;17:302–17.CrossRef Peinado H, Zhang H, Matei IR, Costa-Silva B, Hoshino A, Rodrigues G, Psaila B, Kaplan RN, Bromberg JF, Kang Y, et al. Pre-metastatic niches: organ-specific homes for metastases. Nat Rev. 2017;17:302–17.CrossRef
19.
go back to reference Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 2005;438:820–7.PubMedPubMedCentralCrossRef Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 2005;438:820–7.PubMedPubMedCentralCrossRef
20.
go back to reference Hiratsuka S, Watanabe A, Aburatani H, Maru Y. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat Cell Biol. 2006;8:1369–75.PubMedCrossRef Hiratsuka S, Watanabe A, Aburatani H, Maru Y. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat Cell Biol. 2006;8:1369–75.PubMedCrossRef
21.
go back to reference Hiratsuka S, Watanabe A, Sakurai Y, Akashi-Takamura S, Ishibashi S, Miyake K, Shibuya M, Akira S, Aburatani H, Maru Y. The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat Cell Biol. 2008;10:1349–55.PubMedCrossRef Hiratsuka S, Watanabe A, Sakurai Y, Akashi-Takamura S, Ishibashi S, Miyake K, Shibuya M, Akira S, Aburatani H, Maru Y. The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat Cell Biol. 2008;10:1349–55.PubMedCrossRef
22.
go back to reference Steeg PS. Tumor metastasis: mechanistic insights and clinical challenges. Nat Med. 2006;12:895–904.PubMedCrossRef Steeg PS. Tumor metastasis: mechanistic insights and clinical challenges. Nat Med. 2006;12:895–904.PubMedCrossRef
23.
go back to reference Beuran M, Negoi I, Paun S, Ion AD, Bleotu C, Negoi RI, Hostiuc S. The epithelial to mesenchymal transition in pancreatic cancer: a systematic review. Pancreatology. 2015;15:217–25.PubMedCrossRef Beuran M, Negoi I, Paun S, Ion AD, Bleotu C, Negoi RI, Hostiuc S. The epithelial to mesenchymal transition in pancreatic cancer: a systematic review. Pancreatology. 2015;15:217–25.PubMedCrossRef
24.
25.
go back to reference Maier HJ, Wirth T, Beug H. Epithelial-mesenchymal transition in pancreatic carcinoma. Cancers (Basel). 2010;2:2058–83.CrossRef Maier HJ, Wirth T, Beug H. Epithelial-mesenchymal transition in pancreatic carcinoma. Cancers (Basel). 2010;2:2058–83.CrossRef
27.
go back to reference Zheng X, Carstens JL, Kim J, Scheible M, Kaye J, Sugimoto H, Wu C, LeBleu VS, Kalluri R. EMT program is dispensable for metastasis but induces chemoresistance in pancreatic cancer. Nature. 2015;527:525–30.PubMedPubMedCentralCrossRef Zheng X, Carstens JL, Kim J, Scheible M, Kaye J, Sugimoto H, Wu C, LeBleu VS, Kalluri R. EMT program is dispensable for metastasis but induces chemoresistance in pancreatic cancer. Nature. 2015;527:525–30.PubMedPubMedCentralCrossRef
28.
29.
go back to reference Krebs AM, Mitschke J, Losada ML, Schmalhofer O, Boerries M, Busch H, Boettcher M, Mougiakakos D, Reichardt W, Bronsert P, et al. The EMT-activator Zeb1 is a key factor for cell plasticity and promotes metastasis in pancreatic cancer. Nat Cell Biol. 2017;19:518–42.PubMedCrossRef Krebs AM, Mitschke J, Losada ML, Schmalhofer O, Boerries M, Busch H, Boettcher M, Mougiakakos D, Reichardt W, Bronsert P, et al. The EMT-activator Zeb1 is a key factor for cell plasticity and promotes metastasis in pancreatic cancer. Nat Cell Biol. 2017;19:518–42.PubMedCrossRef
30.
go back to reference Arumugam T, Ramachandran V, Fournier KF, Wang H, Marquis L, Abbruzzese JL, Gallick GE, Logsdon CD, McConkey DJ, Choi W. Epithelial to mesenchymal transition contributes to drug resistance in pancreatic cancer. Cancer Res. 2009;69:5820–8.PubMedPubMedCentralCrossRef Arumugam T, Ramachandran V, Fournier KF, Wang H, Marquis L, Abbruzzese JL, Gallick GE, Logsdon CD, McConkey DJ, Choi W. Epithelial to mesenchymal transition contributes to drug resistance in pancreatic cancer. Cancer Res. 2009;69:5820–8.PubMedPubMedCentralCrossRef
31.
32.
go back to reference Erkan M, Michalski CW, Rieder S, Reiser-Erkan C, Abiatari I, Kolb A, Giese NA, Esposito I, Friess H, Kleeff J. The activated stroma index is a novel and independent prognostic marker in pancreatic ductal adenocarcinoma. Clin Gastroenterol Hepatol. 2008;6:1155–61.PubMedCrossRef Erkan M, Michalski CW, Rieder S, Reiser-Erkan C, Abiatari I, Kolb A, Giese NA, Esposito I, Friess H, Kleeff J. The activated stroma index is a novel and independent prognostic marker in pancreatic ductal adenocarcinoma. Clin Gastroenterol Hepatol. 2008;6:1155–61.PubMedCrossRef
33.
go back to reference Wilson JS, Pirola RC, Apte MV. Stars and stripes in pancreatic cancer: role of stellate cells and stroma in cancer progression. Front Physiol. 2014;5:52.PubMedPubMedCentralCrossRef Wilson JS, Pirola RC, Apte MV. Stars and stripes in pancreatic cancer: role of stellate cells and stroma in cancer progression. Front Physiol. 2014;5:52.PubMedPubMedCentralCrossRef
34.
go back to reference Hwang RF, Moore T, Arumugam T, Ramachandran V, Amos KD, Rivera A, Ji B, Evans DB, Logsdon CD. Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res. 2008;68:918–26.PubMedPubMedCentralCrossRef Hwang RF, Moore T, Arumugam T, Ramachandran V, Amos KD, Rivera A, Ji B, Evans DB, Logsdon CD. Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res. 2008;68:918–26.PubMedPubMedCentralCrossRef
35.
go back to reference Mantoni TS, Lunardi S, Al-Assar O, Masamune A, Brunner TB. Pancreatic stellate cells radioprotect pancreatic cancer cells through β1-integrin signaling. Cancer Res. 2011;71:3453–8.PubMedPubMedCentralCrossRef Mantoni TS, Lunardi S, Al-Assar O, Masamune A, Brunner TB. Pancreatic stellate cells radioprotect pancreatic cancer cells through β1-integrin signaling. Cancer Res. 2011;71:3453–8.PubMedPubMedCentralCrossRef
36.
go back to reference Gao Z, Wang X, Wu K, Zhao Y, Hu G. Pancreatic stellate cells increase the invasion of human pancreatic cancer cells through the stromal cell-derived factor-1/CXCR4 axis. Pancreatology. 2010;10:186–93.PubMedCrossRef Gao Z, Wang X, Wu K, Zhao Y, Hu G. Pancreatic stellate cells increase the invasion of human pancreatic cancer cells through the stromal cell-derived factor-1/CXCR4 axis. Pancreatology. 2010;10:186–93.PubMedCrossRef
37.
go back to reference Cheng X, Kohi S, Koga A, Hirata K, Sato N. Hyaluronan stimulates pancreatic cancer cell motility. Oncotarget. 2016;7:4829–40.PubMed Cheng X, Kohi S, Koga A, Hirata K, Sato N. Hyaluronan stimulates pancreatic cancer cell motility. Oncotarget. 2016;7:4829–40.PubMed
38.
go back to reference Phillips P. Pancreatic stellate cells and fibrosis. In: Grippo PJ, Munshi HG, editors. Pancreatic Cancer and tumor microenvironment. Trivandrum: Transworld Research Network; 2012. Phillips P. Pancreatic stellate cells and fibrosis. In: Grippo PJ, Munshi HG, editors. Pancreatic Cancer and tumor microenvironment. Trivandrum: Transworld Research Network; 2012.
39.
go back to reference Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, Honess D, Madhu B, Goldgraben MA, Caldwell ME, Allard D. Inhibition of hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science. 2009;324:1457–61.PubMedPubMedCentralCrossRef Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, Honess D, Madhu B, Goldgraben MA, Caldwell ME, Allard D. Inhibition of hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science. 2009;324:1457–61.PubMedPubMedCentralCrossRef
40.
go back to reference Jacobetz MA, Chan DS, Neesse A, Bapiro TE, Cook N, Frese KK, Feig C, Nakagawa T, Caldwell ME, Zecchini HI. Hyaluronan impairs vascular function and drug delivery in an mouse model of pancreatic cancer. Gut. 2013;62:112–20.PubMedCrossRef Jacobetz MA, Chan DS, Neesse A, Bapiro TE, Cook N, Frese KK, Feig C, Nakagawa T, Caldwell ME, Zecchini HI. Hyaluronan impairs vascular function and drug delivery in an mouse model of pancreatic cancer. Gut. 2013;62:112–20.PubMedCrossRef
41.
go back to reference Al-Assar O, Demiciorglu F, Lunardi S, Gaspar-Carvalho MM, McKenna WG, Muschel RM, Brunner TB. Contextual regulation of pancreatic cancer stem cell phenotype and radioresistance by pancreatic stellate cells. Radiother Oncol. 2014;11:243–51.CrossRef Al-Assar O, Demiciorglu F, Lunardi S, Gaspar-Carvalho MM, McKenna WG, Muschel RM, Brunner TB. Contextual regulation of pancreatic cancer stem cell phenotype and radioresistance by pancreatic stellate cells. Radiother Oncol. 2014;11:243–51.CrossRef
42.
go back to reference Apte MV, Park S, Phillips PA, Santucci N, Goldstein D, Kumar RK, Ramm GA, Buchler M, Friess H, McCarroll JA. Desmoplastic reaction in pancreatic cancer: role of pancreatic stellate cells. Pancreas. 2004;29:179–87.PubMedCrossRef Apte MV, Park S, Phillips PA, Santucci N, Goldstein D, Kumar RK, Ramm GA, Buchler M, Friess H, McCarroll JA. Desmoplastic reaction in pancreatic cancer: role of pancreatic stellate cells. Pancreas. 2004;29:179–87.PubMedCrossRef
43.
go back to reference Vonlaufen A, Joshi S, Qu C, Phillips PA, Xu Z, Parker NR, Toi CS, Pirola RC, Wilson JS, Goldstein D, Apte MV. Pancreatic stellate cells: partners in crime with pancreatic cancer cells. Cancer Res. 2008;68:2085–93.PubMedCrossRef Vonlaufen A, Joshi S, Qu C, Phillips PA, Xu Z, Parker NR, Toi CS, Pirola RC, Wilson JS, Goldstein D, Apte MV. Pancreatic stellate cells: partners in crime with pancreatic cancer cells. Cancer Res. 2008;68:2085–93.PubMedCrossRef
44.
go back to reference Phillips PA, Wu MJ, Kumar RK, Doherty E, McCarroll JA, Park S, Pirola RC, Wilson JS, Apte MV. Cell migration: a novel aspect of pancreatic stellate cell biology. Gut. 2003;52:677–82.PubMedPubMedCentralCrossRef Phillips PA, Wu MJ, Kumar RK, Doherty E, McCarroll JA, Park S, Pirola RC, Wilson JS, Apte MV. Cell migration: a novel aspect of pancreatic stellate cell biology. Gut. 2003;52:677–82.PubMedPubMedCentralCrossRef
45.
go back to reference Bachem MG, Schünemann M, Ramadani M, Siech M, Beger H, Buck A, Zhou S, Schmid-Kotsas A, Adler G. Pancreatic carcinoma cells induce fibrosis by stimulating proliferation and matrix synthesis of stellate cells. Gastroenterology. 2005;128:907–21.PubMedCrossRef Bachem MG, Schünemann M, Ramadani M, Siech M, Beger H, Buck A, Zhou S, Schmid-Kotsas A, Adler G. Pancreatic carcinoma cells induce fibrosis by stimulating proliferation and matrix synthesis of stellate cells. Gastroenterology. 2005;128:907–21.PubMedCrossRef
46.
go back to reference Hessmann E, Patzak MS, Klein L, Chen N, Kari V, Ramu I, Bapiro TE, Frese KK, Gopinathan A, Richards FM, et al. Fibroblast drug scavenging increases intratumoural gemcitabine accumulation in murine pancreas cancer. Gut. 2018;67:497–507.PubMedCrossRef Hessmann E, Patzak MS, Klein L, Chen N, Kari V, Ramu I, Bapiro TE, Frese KK, Gopinathan A, Richards FM, et al. Fibroblast drug scavenging increases intratumoural gemcitabine accumulation in murine pancreas cancer. Gut. 2018;67:497–507.PubMedCrossRef
47.
go back to reference Kikuta K, Masamune A, Watanabe T, Ariga H, Itoh H, Hamada S, Satoh K, Egawa S, Unno M, Shimosegawa T. Pancreatic stellate cells promote epithelial-mesenchymal transition in pancreatic cancer cells. Biochem Biophys Res Commun. 2010;403:380–4.PubMedCrossRef Kikuta K, Masamune A, Watanabe T, Ariga H, Itoh H, Hamada S, Satoh K, Egawa S, Unno M, Shimosegawa T. Pancreatic stellate cells promote epithelial-mesenchymal transition in pancreatic cancer cells. Biochem Biophys Res Commun. 2010;403:380–4.PubMedCrossRef
48.
go back to reference Qian D, Lu Z, Xu Q, Wu P, Tian L, Zhao L, Cai B, Yin J, Wu Y, Staveley-O’Carroll KF. Galectin-1-driven upregulation of SDF-1 in pancreatic stellate cells promotes pancreatic cancer metastasis. Cancer Lett. 2017;397:43–51.PubMedCrossRef Qian D, Lu Z, Xu Q, Wu P, Tian L, Zhao L, Cai B, Yin J, Wu Y, Staveley-O’Carroll KF. Galectin-1-driven upregulation of SDF-1 in pancreatic stellate cells promotes pancreatic cancer metastasis. Cancer Lett. 2017;397:43–51.PubMedCrossRef
49.
go back to reference Li X, Ma Q, Xu Q, Liu H, Lei J, Duan W, Bhat K, Wang F, Wu E, Wang Z. SDF-1/CXCR4 signaling induces pancreatic cancer cell invasion and epithelial–mesenchymal transition in vitro through noncanonical activation of hedgehog pathway. Cancer Lett. 2012;322:169–76.PubMedPubMedCentralCrossRef Li X, Ma Q, Xu Q, Liu H, Lei J, Duan W, Bhat K, Wang F, Wu E, Wang Z. SDF-1/CXCR4 signaling induces pancreatic cancer cell invasion and epithelial–mesenchymal transition in vitro through noncanonical activation of hedgehog pathway. Cancer Lett. 2012;322:169–76.PubMedPubMedCentralCrossRef
50.
go back to reference Sato N, Maehara N, Goggins M. Gene expression profiling of tumor-stromal interactions between pancreatic cancer cells and stromal fibroblasts. Cancer Res. 2004;64:6950–6.PubMedCrossRef Sato N, Maehara N, Goggins M. Gene expression profiling of tumor-stromal interactions between pancreatic cancer cells and stromal fibroblasts. Cancer Res. 2004;64:6950–6.PubMedCrossRef
51.
go back to reference Tsujii M, Kawano S, DuBois RN. Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. P Natl Acad Sci USA. 1997;94:3336–40.CrossRef Tsujii M, Kawano S, DuBois RN. Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. P Natl Acad Sci USA. 1997;94:3336–40.CrossRef
52.
go back to reference Gialeli C, Theocharis AD, Karamanos NK. Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J. 2010;278:16–27.PubMedCrossRef Gialeli C, Theocharis AD, Karamanos NK. Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J. 2010;278:16–27.PubMedCrossRef
53.
go back to reference Okami J, Nakamori S, Hiraoka N, Tsujie M, Hayashi N, Yamamoto H, Fujiwara Y, Nagano H, Dono K, Umeshita K, et al. Suppression of pancreatic cancer cell invasion by a cyclooxygenase-2-specific inhibitor. Clin Exp Metastas. 2003;20:577–84.CrossRef Okami J, Nakamori S, Hiraoka N, Tsujie M, Hayashi N, Yamamoto H, Fujiwara Y, Nagano H, Dono K, Umeshita K, et al. Suppression of pancreatic cancer cell invasion by a cyclooxygenase-2-specific inhibitor. Clin Exp Metastas. 2003;20:577–84.CrossRef
54.
go back to reference Wei D, Wang L, He Y, Xiong HQ, Abbruzzese JL, Xie K. Celecoxib inhibits vascular endothelial growth factor expression in and reduces angiogenesis and metastasis of human pancreatic cancer via suppression of Sp1 transcription factor activity. Cancer Res. 2004;64:2030–8.PubMedCrossRef Wei D, Wang L, He Y, Xiong HQ, Abbruzzese JL, Xie K. Celecoxib inhibits vascular endothelial growth factor expression in and reduces angiogenesis and metastasis of human pancreatic cancer via suppression of Sp1 transcription factor activity. Cancer Res. 2004;64:2030–8.PubMedCrossRef
55.
go back to reference Theocharis AD, Tsara ME, Papageorgacopoulou N, Karavias DD, Theocharis DA. Pancreatic carcinoma is characterized by elevated content of hyaluronan and chondroitin sulfate with altered disaccharide composition. Biochim Biophys Act. 2000;1502:201–6.CrossRef Theocharis AD, Tsara ME, Papageorgacopoulou N, Karavias DD, Theocharis DA. Pancreatic carcinoma is characterized by elevated content of hyaluronan and chondroitin sulfate with altered disaccharide composition. Biochim Biophys Act. 2000;1502:201–6.CrossRef
56.
go back to reference Itano N, Atsumi F, Sawai T, Yamada Y, Miyaishi O, Senga T, Hamaguchi M, Kimata K. Abnormal accumulation of hyaluronan matrix diminishes contact inhibition of cell growth and promotes cell migration. P Natl Acad Sci USA. 2002;99:3609–14.CrossRef Itano N, Atsumi F, Sawai T, Yamada Y, Miyaishi O, Senga T, Hamaguchi M, Kimata K. Abnormal accumulation of hyaluronan matrix diminishes contact inhibition of cell growth and promotes cell migration. P Natl Acad Sci USA. 2002;99:3609–14.CrossRef
57.
go back to reference Kim HR, Wheeler MA, Wilson CM, Iida J, Eng D. Hyaluronan facilitates invasion of colon carcinoma cells in vitro via interaction with CD44. Cancer Res. 2004;64:4569–76.PubMedCrossRef Kim HR, Wheeler MA, Wilson CM, Iida J, Eng D. Hyaluronan facilitates invasion of colon carcinoma cells in vitro via interaction with CD44. Cancer Res. 2004;64:4569–76.PubMedCrossRef
58.
go back to reference Liu N, Gao F, Han Z, Xu X, Underhill CB, Zhang L. Hyaluronan synthase 3 overexpression promotes the growth of TSU prostate cancer cells. Cancer Res. 2001;61:5207–17.PubMed Liu N, Gao F, Han Z, Xu X, Underhill CB, Zhang L. Hyaluronan synthase 3 overexpression promotes the growth of TSU prostate cancer cells. Cancer Res. 2001;61:5207–17.PubMed
59.
go back to reference Scaife CL, Shea JE, Dai Q, Firpo MA, Prestwich GD, Mulvihill SJ. Synthetic extracellular matrix enhances tumor growth and metastasis in an orthotopic mouse model of pancreatic adenocarcinoma. J Gastrointest Surg. 2008;12:1074–80.PubMedCrossRef Scaife CL, Shea JE, Dai Q, Firpo MA, Prestwich GD, Mulvihill SJ. Synthetic extracellular matrix enhances tumor growth and metastasis in an orthotopic mouse model of pancreatic adenocarcinoma. J Gastrointest Surg. 2008;12:1074–80.PubMedCrossRef
60.
go back to reference Camenisch TD, Spicer AP, Brehm-Gibson T, Biesterfeldt J, Augustine ML, Calabro A Jr, Kubalak S, Klewer SE, McDonald JA. Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. J Clin Invest. 2000;106:349–60.PubMedPubMedCentralCrossRef Camenisch TD, Spicer AP, Brehm-Gibson T, Biesterfeldt J, Augustine ML, Calabro A Jr, Kubalak S, Klewer SE, McDonald JA. Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. J Clin Invest. 2000;106:349–60.PubMedPubMedCentralCrossRef
61.
go back to reference Zoltan-Jones A, Huang L, Ghatak S, Toole BP. Elevated hyaluronan production induces mesenchymal and transformed properties in epithelial cells. J Biol Chem. 2003;278:45801–10.PubMedCrossRef Zoltan-Jones A, Huang L, Ghatak S, Toole BP. Elevated hyaluronan production induces mesenchymal and transformed properties in epithelial cells. J Biol Chem. 2003;278:45801–10.PubMedCrossRef
62.
go back to reference Kultti A, Zhoa C, Singha NC, Zimmerman S, Osgood RJ, Symons R, Jiang P, Li X, Thompson CB, Infante JR, et al. Accumulation of extracellular hyaluronan by hyaluronan synthase 3 promotes tumor growth and modulates the pancreatic cancer microenvironment. Biomed Res Int. 2014;2014:817613.PubMedPubMedCentralCrossRef Kultti A, Zhoa C, Singha NC, Zimmerman S, Osgood RJ, Symons R, Jiang P, Li X, Thompson CB, Infante JR, et al. Accumulation of extracellular hyaluronan by hyaluronan synthase 3 promotes tumor growth and modulates the pancreatic cancer microenvironment. Biomed Res Int. 2014;2014:817613.PubMedPubMedCentralCrossRef
63.
go back to reference Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2010;144:646–74.CrossRef Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2010;144:646–74.CrossRef
64.
go back to reference Vonlaufen A, Phillips PA, Xu Z, Goldstein D, Pirola RC, Wilson JS, Apte MV. Pancreatic stellate cells and pancreatic cancer cells: an unholy alliance. Cancer Res. 2008;68:7707–10.PubMedCrossRef Vonlaufen A, Phillips PA, Xu Z, Goldstein D, Pirola RC, Wilson JS, Apte MV. Pancreatic stellate cells and pancreatic cancer cells: an unholy alliance. Cancer Res. 2008;68:7707–10.PubMedCrossRef
65.
go back to reference Masamune A, Kikuta K, Watanabe T, Satoh K, Shimosegawa T. Pancreatic stellate cells induce angiogenesis. Pancreas. 2009;38:483.CrossRef Masamune A, Kikuta K, Watanabe T, Satoh K, Shimosegawa T. Pancreatic stellate cells induce angiogenesis. Pancreas. 2009;38:483.CrossRef
66.
go back to reference Xu Z, Vonlaufen A, Phillips PA, Fiala-Beer E, Zhang X, Yang L, Biankin AV, Goldstein D, Pirola RC, Wilson JS, et al. Role of pancreatic stellate cells in pancreatic cancer metastasis. Am J Pathol. 2010;177:2585–96.PubMedPubMedCentralCrossRef Xu Z, Vonlaufen A, Phillips PA, Fiala-Beer E, Zhang X, Yang L, Biankin AV, Goldstein D, Pirola RC, Wilson JS, et al. Role of pancreatic stellate cells in pancreatic cancer metastasis. Am J Pathol. 2010;177:2585–96.PubMedPubMedCentralCrossRef
67.
go back to reference Masamune A, Kikuta K, Watanabe T, Satoh K, Hirota M, Shimosegawa T. Hypoxia stimulates pancreatic stellate cells to induce fibrosis and angiogenesis in pancreatic cancer. Am J Phys. 2008;295:G709–17. Masamune A, Kikuta K, Watanabe T, Satoh K, Hirota M, Shimosegawa T. Hypoxia stimulates pancreatic stellate cells to induce fibrosis and angiogenesis in pancreatic cancer. Am J Phys. 2008;295:G709–17.
68.
go back to reference Erkan M, Reiser-Erkan C, Michalski CW, Deucker S, Sauliunaite D, Streit S, Esposito I, Friess H, Kleeff J. Cancer-stellate cell interactions perpetuate the hypoxia-fibrosis cycle in pancreatic ductal adenocarcinoma. Neoplasia. 2009;11:497–508.PubMedPubMedCentralCrossRef Erkan M, Reiser-Erkan C, Michalski CW, Deucker S, Sauliunaite D, Streit S, Esposito I, Friess H, Kleeff J. Cancer-stellate cell interactions perpetuate the hypoxia-fibrosis cycle in pancreatic ductal adenocarcinoma. Neoplasia. 2009;11:497–508.PubMedPubMedCentralCrossRef
69.
go back to reference Suetsugu A, Snyder CS, Moriwaki H, Saji S, Bouvet M, Hoffman RM. Imaging the interaction of pancreatic cancer and stellate cells in the tumor microenvironment during metastasis. Anticancer Res. 2015;35:2545–51.PubMed Suetsugu A, Snyder CS, Moriwaki H, Saji S, Bouvet M, Hoffman RM. Imaging the interaction of pancreatic cancer and stellate cells in the tumor microenvironment during metastasis. Anticancer Res. 2015;35:2545–51.PubMed
70.
go back to reference Coleman SJ, Chioni AM, Ghallab M, Anderson RK, Lemoine NR, Kocher HM, Grose RP. Nuclear translocation of FGFR1 and FGF2 in pancreatic stellate cells facilitates pancreatic cancer cell invasion. EMBO Mol Med. 2014;6:467–81.PubMedPubMedCentralCrossRef Coleman SJ, Chioni AM, Ghallab M, Anderson RK, Lemoine NR, Kocher HM, Grose RP. Nuclear translocation of FGFR1 and FGF2 in pancreatic stellate cells facilitates pancreatic cancer cell invasion. EMBO Mol Med. 2014;6:467–81.PubMedPubMedCentralCrossRef
71.
go back to reference Fang M, Yuan J, Peng C, Li Y. Collagen as a double-edged sword in tumor progression. Tumour Biol. 2014;5:2871–82.CrossRef Fang M, Yuan J, Peng C, Li Y. Collagen as a double-edged sword in tumor progression. Tumour Biol. 2014;5:2871–82.CrossRef
72.
go back to reference Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, et al. Tensional homeostasis and the malignant phenotype. Cancer Cell. 2005;8:241–54.PubMedCrossRef Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, et al. Tensional homeostasis and the malignant phenotype. Cancer Cell. 2005;8:241–54.PubMedCrossRef
73.
go back to reference Wei SC, Fattet L, Tsai JH, Guo Y, Pai VH, Majeski HE, Chen AC, Sah RL, Taylor SS, Engler AJ, et al. Matrix stiffness drives epithelial-mesenchymal transition and tumour metastasis through a TWIST1-G3BP2 mechanotransduction pathway. Nat Cell Biol. 2015;17:678–88.PubMedPubMedCentralCrossRef Wei SC, Fattet L, Tsai JH, Guo Y, Pai VH, Majeski HE, Chen AC, Sah RL, Taylor SS, Engler AJ, et al. Matrix stiffness drives epithelial-mesenchymal transition and tumour metastasis through a TWIST1-G3BP2 mechanotransduction pathway. Nat Cell Biol. 2015;17:678–88.PubMedPubMedCentralCrossRef
74.
go back to reference Rice AJ, Cortes E, Lachowski D, Cheung BCH, Karim SA, Morton JP, Del Río Hernández A. Matrix stiffness induces epithelial-mesenchymal transition and promotes chemoresistance in pancreatic cancer cells. Oncogene. 2017;6:e352.CrossRef Rice AJ, Cortes E, Lachowski D, Cheung BCH, Karim SA, Morton JP, Del Río Hernández A. Matrix stiffness induces epithelial-mesenchymal transition and promotes chemoresistance in pancreatic cancer cells. Oncogene. 2017;6:e352.CrossRef
75.
go back to reference Haage A, Schneider IC. Cellular contractility and extracellular matrix stiffness regulate matrix metalloproteinase activity in pancreatic cancer cells. FASEB J. 2014;28:3589–99.PubMedCrossRef Haage A, Schneider IC. Cellular contractility and extracellular matrix stiffness regulate matrix metalloproteinase activity in pancreatic cancer cells. FASEB J. 2014;28:3589–99.PubMedCrossRef
76.
go back to reference Koenig A, Mueller C, Hasel C, Adler G, Menke A. Collagen type I induces disruption of E-cadherin-mediated cell-cell contacts and promotes proliferation of pancreatic carcinoma cells. Cancer Res. 2006;66:4662–71.PubMedCrossRef Koenig A, Mueller C, Hasel C, Adler G, Menke A. Collagen type I induces disruption of E-cadherin-mediated cell-cell contacts and promotes proliferation of pancreatic carcinoma cells. Cancer Res. 2006;66:4662–71.PubMedCrossRef
77.
go back to reference Shintani Y, Hollingsworth MA, Wheelock MJ, Johnson KR. Collagen I promotes metastasis in pancreatic cancer by activating c-Jun NH(2)-terminal kinase 1 and up-regulating N-cadherin expression. Cancer Res. 2006;66:11745–53.PubMedCrossRef Shintani Y, Hollingsworth MA, Wheelock MJ, Johnson KR. Collagen I promotes metastasis in pancreatic cancer by activating c-Jun NH(2)-terminal kinase 1 and up-regulating N-cadherin expression. Cancer Res. 2006;66:11745–53.PubMedCrossRef
78.
go back to reference Imamichi Y, König A, Gress T, Menke A. Collagen type I-induced Smad-interacting protein 1 expression downregulates E-cadherin in pancreatic cancer. Oncogene. 2007;25:2381–5.CrossRef Imamichi Y, König A, Gress T, Menke A. Collagen type I-induced Smad-interacting protein 1 expression downregulates E-cadherin in pancreatic cancer. Oncogene. 2007;25:2381–5.CrossRef
79.
go back to reference Wang W, Wyckoff JB, Centonze Frohlich V, Oleynikov Y, Hüttelmaier S, Zavadil J, Cermak L, Bottinger EP, Singer RH, White JG, et al. Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling. Cancer Res. 2002;62:6278–88.PubMed Wang W, Wyckoff JB, Centonze Frohlich V, Oleynikov Y, Hüttelmaier S, Zavadil J, Cermak L, Bottinger EP, Singer RH, White JG, et al. Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling. Cancer Res. 2002;62:6278–88.PubMed
80.
go back to reference Lu J, Zhou S, Siech M, Habisch H, Seufferlein T, Bachem MG. Pancreatic stellate cells promote hapto-migration of cancer cells through collagen I-mediated signalling pathway. Brit J Cancer. 2014;110:409–20.PubMedCrossRef Lu J, Zhou S, Siech M, Habisch H, Seufferlein T, Bachem MG. Pancreatic stellate cells promote hapto-migration of cancer cells through collagen I-mediated signalling pathway. Brit J Cancer. 2014;110:409–20.PubMedCrossRef
81.
go back to reference Drifka CR, Tod J, Loeffler AG, Liu Y, Thomas GJ, Eliceiri KW, Kao WJ. Periductal stromal collagen topology of pancreatic ductal adenocarcinoma differs from that of normal and chronic pancreatitis. Modern Pathol. 2015;28:1470–80.CrossRef Drifka CR, Tod J, Loeffler AG, Liu Y, Thomas GJ, Eliceiri KW, Kao WJ. Periductal stromal collagen topology of pancreatic ductal adenocarcinoma differs from that of normal and chronic pancreatitis. Modern Pathol. 2015;28:1470–80.CrossRef
82.
go back to reference Beerling E, Oosterom I, Voest E, Lolkema M, Van Rheenen J. Intravital characterization of tumor cell migration in pancreatic cancer. Intravital. 2016;5:e1261773.PubMedPubMedCentralCrossRef Beerling E, Oosterom I, Voest E, Lolkema M, Van Rheenen J. Intravital characterization of tumor cell migration in pancreatic cancer. Intravital. 2016;5:e1261773.PubMedPubMedCentralCrossRef
83.
go back to reference Rhim AD, Mirek ET, Aiello NM, Maitra A, Bailey JM, McAllister F, Reichert M, Beatty GL, Rustgi AK, Vonderheide RH, et al. EMT and dissemination precede pancreatic tumor formation. Cell. 2012;148:349–61.PubMedPubMedCentralCrossRef Rhim AD, Mirek ET, Aiello NM, Maitra A, Bailey JM, McAllister F, Reichert M, Beatty GL, Rustgi AK, Vonderheide RH, et al. EMT and dissemination precede pancreatic tumor formation. Cell. 2012;148:349–61.PubMedPubMedCentralCrossRef
84.
go back to reference Chambers AF, Naumov GN, Varghese HJ, Nadkarni KV, Mac Donald IC, Groom AC. Critical steps in hematogenous metastasis: an overview. Surg Oncol Clin N Am. 2001;10:243–55.PubMedCrossRef Chambers AF, Naumov GN, Varghese HJ, Nadkarni KV, Mac Donald IC, Groom AC. Critical steps in hematogenous metastasis: an overview. Surg Oncol Clin N Am. 2001;10:243–55.PubMedCrossRef
85.
86.
go back to reference Tzanakakis GN, Agarwal KC, Veronikis DK, Vezeridis MP. Effects of antiplatelet agents alone or in combinations on platelet aggregation and on liver metastases from a human pancreatic adenocarcinoma in the nude mouse. J Surg Oncol. 1991;48:45–50.PubMedCrossRef Tzanakakis GN, Agarwal KC, Veronikis DK, Vezeridis MP. Effects of antiplatelet agents alone or in combinations on platelet aggregation and on liver metastases from a human pancreatic adenocarcinoma in the nude mouse. J Surg Oncol. 1991;48:45–50.PubMedCrossRef
87.
go back to reference Brown KM, Domin C, Aranha GV, Yong S, Shoup M. Increased preoperative platelet count is associated with decreased survival after resection for adenocarcinoma of the pancreas. Am J Surg. 2005;189:278–82.PubMedCrossRef Brown KM, Domin C, Aranha GV, Yong S, Shoup M. Increased preoperative platelet count is associated with decreased survival after resection for adenocarcinoma of the pancreas. Am J Surg. 2005;189:278–82.PubMedCrossRef
88.
go back to reference Wang H, Gao J, Bai M, Liu R, Li H, Deng T, Zhou L, Han R, Ge S, Huang D, et al. The pretreatment platelet and plasma fibrinogen level correlate with tumor progression and metastasis in patients with pancreatic cancer. Platelets. 2014;25:382–7.PubMedCrossRef Wang H, Gao J, Bai M, Liu R, Li H, Deng T, Zhou L, Han R, Ge S, Huang D, et al. The pretreatment platelet and plasma fibrinogen level correlate with tumor progression and metastasis in patients with pancreatic cancer. Platelets. 2014;25:382–7.PubMedCrossRef
89.
go back to reference Mezouar S, Darbousset R, Dignat-George F, Panicot-Dubois L, Dubois C. Inhibition of platelet activation prevents the P-selectin and integrin-dependent accumulation of cancer cell microparticles and reduces tumor growth and metastasis in vivo. Int J Cancer. 2015;136:462–75.PubMedCrossRef Mezouar S, Darbousset R, Dignat-George F, Panicot-Dubois L, Dubois C. Inhibition of platelet activation prevents the P-selectin and integrin-dependent accumulation of cancer cell microparticles and reduces tumor growth and metastasis in vivo. Int J Cancer. 2015;136:462–75.PubMedCrossRef
90.
go back to reference Shirai Y, Shiba H, Sakamoto T, Horiuchi T, Haruki K, Fujiwara Y, Futagawa Y, Ohashi T, Yanaga K. Preoperative platelet to lymphocyte ratio predicts outcome of patients with pancreatic ductal adenocarcinoma after pancreatic resection. Surgery. 2015;158:360–5.PubMedCrossRef Shirai Y, Shiba H, Sakamoto T, Horiuchi T, Haruki K, Fujiwara Y, Futagawa Y, Ohashi T, Yanaga K. Preoperative platelet to lymphocyte ratio predicts outcome of patients with pancreatic ductal adenocarcinoma after pancreatic resection. Surgery. 2015;158:360–5.PubMedCrossRef
91.
go back to reference Chadha AS, Kocak-Uzel E, Das P, Minsky BD, Delclos ME, Mahmood U, Guha S, Ahmad M, Varadhachary GR, Javle M, et al. Paraneoplastic thrombocytosis independently predicts poor prognosis in patients with locally advanced pancreatic cancer. Act Oncol. 2015;54:971–8.CrossRef Chadha AS, Kocak-Uzel E, Das P, Minsky BD, Delclos ME, Mahmood U, Guha S, Ahmad M, Varadhachary GR, Javle M, et al. Paraneoplastic thrombocytosis independently predicts poor prognosis in patients with locally advanced pancreatic cancer. Act Oncol. 2015;54:971–8.CrossRef
92.
go back to reference Thomas GM, Panicot-Dubois L, Lacroix R, Dignat-George F, Lombardo D, Dubois C. Cancer cell–derived microparticles bearing P-selectin glycoprotein ligand 1 accelerate thrombus formation in vivo. J Exp Med. 2009;206:1913–27.PubMedPubMedCentralCrossRef Thomas GM, Panicot-Dubois L, Lacroix R, Dignat-George F, Lombardo D, Dubois C. Cancer cell–derived microparticles bearing P-selectin glycoprotein ligand 1 accelerate thrombus formation in vivo. J Exp Med. 2009;206:1913–27.PubMedPubMedCentralCrossRef
93.
go back to reference Wang JG, Geddings JE, Aleman MM, Cardenas JC, Chantrathammachart P, Williams JC, Kirchhofer D, Bogdanov VY, Bach RR, Rak J, et al. Tumor-derived tissue factor activates coagulation and enhances thrombosis in a mouse xenograft model of human pancreatic cancer. Blood. 2012;119:5543–52.PubMedPubMedCentralCrossRef Wang JG, Geddings JE, Aleman MM, Cardenas JC, Chantrathammachart P, Williams JC, Kirchhofer D, Bogdanov VY, Bach RR, Rak J, et al. Tumor-derived tissue factor activates coagulation and enhances thrombosis in a mouse xenograft model of human pancreatic cancer. Blood. 2012;119:5543–52.PubMedPubMedCentralCrossRef
94.
go back to reference Thaler J, Koder S, Kornek G, Pabinger I, Ay C. Microparticle-associated tissue factor activity in patients with metastatic pancreatic cancer and its effect on fibrin clot formation. Transl Res. 2014;163:145–50.PubMedCrossRef Thaler J, Koder S, Kornek G, Pabinger I, Ay C. Microparticle-associated tissue factor activity in patients with metastatic pancreatic cancer and its effect on fibrin clot formation. Transl Res. 2014;163:145–50.PubMedCrossRef
95.
go back to reference Woei-A-Jin FJSH, Tesselaar MET, Garcia Rodriguez P, Romijn FPHTM, Bertina RM, Osanto S. Tissue factor-bearing microparticles and CA19.9: two players in pancreatic cancer-associated thrombosis? Brit J Cancer. 2016;115:332–8.PubMedPubMedCentralCrossRef Woei-A-Jin FJSH, Tesselaar MET, Garcia Rodriguez P, Romijn FPHTM, Bertina RM, Osanto S. Tissue factor-bearing microparticles and CA19.9: two players in pancreatic cancer-associated thrombosis? Brit J Cancer. 2016;115:332–8.PubMedPubMedCentralCrossRef
96.
go back to reference Geddings JE, Hisada Y, Boulaftali Y, Getz TM, Whelihan M, Fuentes R, Dee R, Cooley BC, Key NS, Wolberg AS, et al. Tissue factor-positive tumor microvesicles activate platelets and enhance thrombosis in mice. J Thromb Haemost. 2016;4:153–66.CrossRef Geddings JE, Hisada Y, Boulaftali Y, Getz TM, Whelihan M, Fuentes R, Dee R, Cooley BC, Key NS, Wolberg AS, et al. Tissue factor-positive tumor microvesicles activate platelets and enhance thrombosis in mice. J Thromb Haemost. 2016;4:153–66.CrossRef
98.
go back to reference Gil-Bernabé AM, Ferjančič S, Tlalka M, Zhao L, Allen PD, Im JH, Watson K, Hill SA, Amirkhosravi A, Francis JL, et al. Recruitment of monocytes/macrophages by tissue factor-mediated coagulation is essential for metastatic cell survival and premetastatic niche establishment in mice. Blood. 2012;119:3164–75.PubMedCrossRef Gil-Bernabé AM, Ferjančič S, Tlalka M, Zhao L, Allen PD, Im JH, Watson K, Hill SA, Amirkhosravi A, Francis JL, et al. Recruitment of monocytes/macrophages by tissue factor-mediated coagulation is essential for metastatic cell survival and premetastatic niche establishment in mice. Blood. 2012;119:3164–75.PubMedCrossRef
99.
go back to reference Labelle M, Begum S, Hynes RO. Platelets guide the formation of early metastatic niches. P Natl Acad Sci USA. 2014;111:E3053–61.CrossRef Labelle M, Begum S, Hynes RO. Platelets guide the formation of early metastatic niches. P Natl Acad Sci USA. 2014;111:E3053–61.CrossRef
100.
go back to reference Che SPY, Park JY, Stokol T. Tissue factor-expressing tumor-derived extracellular vesicles activate quiescent endothelial cells via protease-activated receptor-1. Front Oncol. 2017;7:261.PubMedPubMedCentralCrossRef Che SPY, Park JY, Stokol T. Tissue factor-expressing tumor-derived extracellular vesicles activate quiescent endothelial cells via protease-activated receptor-1. Front Oncol. 2017;7:261.PubMedPubMedCentralCrossRef
101.
go back to reference Schumacher D, Strilic B, Sivaraj KK, Wettschureck N, Offermanns S. Platelet-derived nucleotides promote tumor-cell transendothelial migration and metastasis via P2Y2 receptor. Cancer Cell. 2013;24:130–7.PubMedCrossRef Schumacher D, Strilic B, Sivaraj KK, Wettschureck N, Offermanns S. Platelet-derived nucleotides promote tumor-cell transendothelial migration and metastasis via P2Y2 receptor. Cancer Cell. 2013;24:130–7.PubMedCrossRef
102.
go back to reference Nieswandt B, Hafner M, Echtenacher B, Männel DN. Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Res. 1999;59:1295–300.PubMed Nieswandt B, Hafner M, Echtenacher B, Männel DN. Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Res. 1999;59:1295–300.PubMed
103.
go back to reference Palumbo JS, Talmage KE, Massari JV, La Jeunesse CM, Flick MJ, Kombrinck KW, Jirousková M, Degen JL. Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell–mediated elimination of tumor cells. Blood. 2005;105:178–85.PubMedCrossRef Palumbo JS, Talmage KE, Massari JV, La Jeunesse CM, Flick MJ, Kombrinck KW, Jirousková M, Degen JL. Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell–mediated elimination of tumor cells. Blood. 2005;105:178–85.PubMedCrossRef
104.
go back to reference Palumbo JS, Talmage KE, Massari JV, La Jeunesse CM, Flick MJ, Kombrinck KW, Hu Z, Barney KA, Degen JL. Tumor cell–associated tissue factor and circulating hemostatic factors cooperate to increase metastatic potential through natural killer cell–dependent and–independent mechanisms. Blood. 2007;110:133–41.PubMedPubMedCentralCrossRef Palumbo JS, Talmage KE, Massari JV, La Jeunesse CM, Flick MJ, Kombrinck KW, Hu Z, Barney KA, Degen JL. Tumor cell–associated tissue factor and circulating hemostatic factors cooperate to increase metastatic potential through natural killer cell–dependent and–independent mechanisms. Blood. 2007;110:133–41.PubMedPubMedCentralCrossRef
105.
go back to reference Martin MD, Matrisian LM. The other side of MMPs: protective roles in tumor progression. Cancer Metastas Rev. 2007;26:717–24.CrossRef Martin MD, Matrisian LM. The other side of MMPs: protective roles in tumor progression. Cancer Metastas Rev. 2007;26:717–24.CrossRef
106.
go back to reference Kopitz C, Gerg M, Bandapalli OR, Ister D, Pennington CJ, Hauser S, Flechsig C, Krell HW, Antolovic D, Brew K, et al. Tissue inhibitors of metalloproteinases-1 promotes liver metastasis by induction of hepatocyte growth factor signaling. Cancer Res. 2007;67:8615–23.PubMedCrossRef Kopitz C, Gerg M, Bandapalli OR, Ister D, Pennington CJ, Hauser S, Flechsig C, Krell HW, Antolovic D, Brew K, et al. Tissue inhibitors of metalloproteinases-1 promotes liver metastasis by induction of hepatocyte growth factor signaling. Cancer Res. 2007;67:8615–23.PubMedCrossRef
107.
go back to reference Schelter F, Grandl M, Seubert B, Schaten S, Hauser S, Gerg M, Boccaccio C, Comoglio P, Krüger A. Tumor cell-derived Timp-1 is necessary for maintaining metastasis-promoting met-signaling via inhibition of Adam-10. Clin Exp Metastas. 2011;28:793–802.CrossRef Schelter F, Grandl M, Seubert B, Schaten S, Hauser S, Gerg M, Boccaccio C, Comoglio P, Krüger A. Tumor cell-derived Timp-1 is necessary for maintaining metastasis-promoting met-signaling via inhibition of Adam-10. Clin Exp Metastas. 2011;28:793–802.CrossRef
108.
go back to reference Gress TM, Müller-Pillasch F, Lerch MM, Friess H, Büchler M, Adler G. Expression and in-situ localization of genes coding for extracellular matrix proteins and extracellular matrix degrading proteases in pancreatic cancer. Int J Cancer. 1995;62:407–13.PubMedCrossRef Gress TM, Müller-Pillasch F, Lerch MM, Friess H, Büchler M, Adler G. Expression and in-situ localization of genes coding for extracellular matrix proteins and extracellular matrix degrading proteases in pancreatic cancer. Int J Cancer. 1995;62:407–13.PubMedCrossRef
109.
go back to reference Bramhall SR, Stamp GWH, Dunn J, Lemoine NR, Neoptolemos JP. Expression of collagenase (MMP2), stromelysin (MMP3) and tissue inhibitor of the metalloproteinases (TIMP1) in pancreatic and ampullary disease. Brit J Cancer. 1996;73:972–8.PubMedPubMedCentralCrossRef Bramhall SR, Stamp GWH, Dunn J, Lemoine NR, Neoptolemos JP. Expression of collagenase (MMP2), stromelysin (MMP3) and tissue inhibitor of the metalloproteinases (TIMP1) in pancreatic and ampullary disease. Brit J Cancer. 1996;73:972–8.PubMedPubMedCentralCrossRef
110.
go back to reference Bramhall SR, Neoptolemos JP, Stamp GWH, Lemoine NR. Imbalance of expression of matrix metalloproteinases (MMPs) and tissue inhibitors of the matrix metalloproteinases (TIMPs) in human pancreatic carcinoma. J Pathol. 1997;182:347–55.PubMedCrossRef Bramhall SR, Neoptolemos JP, Stamp GWH, Lemoine NR. Imbalance of expression of matrix metalloproteinases (MMPs) and tissue inhibitors of the matrix metalloproteinases (TIMPs) in human pancreatic carcinoma. J Pathol. 1997;182:347–55.PubMedCrossRef
111.
go back to reference Crnogorac-Jurcevic T, Efthimiou E, Capelli P, Blaveri E, Baron A, Terris B, Jones M, Tyson K, Bassi C, Scarpa A, et al. Gene expression profiles of pancreatic cancer and stromal desmoplasia. Oncogene. 2001;20:7437–46.PubMedCrossRef Crnogorac-Jurcevic T, Efthimiou E, Capelli P, Blaveri E, Baron A, Terris B, Jones M, Tyson K, Bassi C, Scarpa A, et al. Gene expression profiles of pancreatic cancer and stromal desmoplasia. Oncogene. 2001;20:7437–46.PubMedCrossRef
112.
go back to reference Crnogorac-Jurcevic T, Efthimiou E, Nielsen T, Loader J, Terris B, Stamp G, Baron A, Scarpa A, Lemoine NR. Expression profiling of microdissected pancreatic adenocarcinomas. Oncogene. 2002;21:4587–94.PubMedCrossRef Crnogorac-Jurcevic T, Efthimiou E, Nielsen T, Loader J, Terris B, Stamp G, Baron A, Scarpa A, Lemoine NR. Expression profiling of microdissected pancreatic adenocarcinomas. Oncogene. 2002;21:4587–94.PubMedCrossRef
113.
go back to reference Schrötzlmair F, Kopitz C, Halbgewachs B, Lu F, Algül H, Brünner N, Gänsbacher B, Krüger A. Tissue inhibitor of metalloproteinases-1-induced scattered liver metastasis is mediated by host-derived urokinase-type plasminogen activator. J Cell Mol Med. 2010;14:2760–70.PubMedCrossRef Schrötzlmair F, Kopitz C, Halbgewachs B, Lu F, Algül H, Brünner N, Gänsbacher B, Krüger A. Tissue inhibitor of metalloproteinases-1-induced scattered liver metastasis is mediated by host-derived urokinase-type plasminogen activator. J Cell Mol Med. 2010;14:2760–70.PubMedCrossRef
114.
go back to reference Grünwald B, Harant V, Schaten S, Frühschütz M, Spallek R, Höchst B, Stutzer K, Berchtold S, Erkan M, Prokopchuk O, et al. Pancreatic premalignant lesions secrete tissue inhibitor of metalloproteinases-1, which activates hepatic stellate cells via CD63 signaling to create a premetastatic niche in the liver. Gastroenterology. 2016;151:1011–1024.e7.PubMedCrossRef Grünwald B, Harant V, Schaten S, Frühschütz M, Spallek R, Höchst B, Stutzer K, Berchtold S, Erkan M, Prokopchuk O, et al. Pancreatic premalignant lesions secrete tissue inhibitor of metalloproteinases-1, which activates hepatic stellate cells via CD63 signaling to create a premetastatic niche in the liver. Gastroenterology. 2016;151:1011–1024.e7.PubMedCrossRef
115.
go back to reference Kobuch J, Cui H, Grünwald B, Saftig P, Knolle PA, Krüger A. TIMP-1 signaling via CD63 triggers granulopoiesis and neutrophilia in mice. Haematologica. 2015;100:1005–13.PubMedPubMedCentral Kobuch J, Cui H, Grünwald B, Saftig P, Knolle PA, Krüger A. TIMP-1 signaling via CD63 triggers granulopoiesis and neutrophilia in mice. Haematologica. 2015;100:1005–13.PubMedPubMedCentral
116.
go back to reference Matsusue R, Kubo H, Hisamori S, Okoshi K, Takagi H, Hida K, Nakano K, Itami A, Kawada K, Nagayama S, et al. Hepatic stellate cells promote liver metastasis of colon cancer cells by the action of SDF-1/CXCR4 axis. Ann Surg Oncol. 2009;16:2645–53.PubMedCrossRef Matsusue R, Kubo H, Hisamori S, Okoshi K, Takagi H, Hida K, Nakano K, Itami A, Kawada K, Nagayama S, et al. Hepatic stellate cells promote liver metastasis of colon cancer cells by the action of SDF-1/CXCR4 axis. Ann Surg Oncol. 2009;16:2645–53.PubMedCrossRef
117.
go back to reference Saur D, Seidler B, Schneider G, Algül H, Beck R, Senekowitsch-Schmidtke R, Schwaiger M, Schmid RM. CXCR4 expression increases liver and lung metastasis in a mouse model of pancreatic cancer. Gastroenterology. 2005;129:1237–50.PubMedCrossRef Saur D, Seidler B, Schneider G, Algül H, Beck R, Senekowitsch-Schmidtke R, Schwaiger M, Schmid RM. CXCR4 expression increases liver and lung metastasis in a mouse model of pancreatic cancer. Gastroenterology. 2005;129:1237–50.PubMedCrossRef
118.
go back to reference D’Costa Z, Jones K, Azad A, Van Stiphout R, Lim SY, Gomes AL, Kinchesh P, Smart SC, Gillies McKenna W, Buffa FM, et al. Gemcitabine-induced TIMP1 attenuates therapy response and promotes tumor growth and liver metastasis in pancreatic cancer. Cancer Res. 2017;77:5952–62.PubMedCrossRef D’Costa Z, Jones K, Azad A, Van Stiphout R, Lim SY, Gomes AL, Kinchesh P, Smart SC, Gillies McKenna W, Buffa FM, et al. Gemcitabine-induced TIMP1 attenuates therapy response and promotes tumor growth and liver metastasis in pancreatic cancer. Cancer Res. 2017;77:5952–62.PubMedCrossRef
119.
go back to reference Poruk KE, Firpo MA, Scaife CL, Adler DG, Emerson LL, Boucher KM, Mulvihill SJ. Serum osteopontin and TIMP-1 as diagnostic and prognostic biomarkers for pancreatic adenocarcinoma. Pancreas. 2013;42:193–7.PubMedPubMedCentralCrossRef Poruk KE, Firpo MA, Scaife CL, Adler DG, Emerson LL, Boucher KM, Mulvihill SJ. Serum osteopontin and TIMP-1 as diagnostic and prognostic biomarkers for pancreatic adenocarcinoma. Pancreas. 2013;42:193–7.PubMedPubMedCentralCrossRef
120.
go back to reference Malka D, Hammel P, Maire F, Rufat P, Madeira I, Pessione F, Lévy P, Ruszniewski P. Risk of pancreatic adenocarcinoma in chronic pancreatitis. Gut. 2002;51:849–52.PubMedPubMedCentralCrossRef Malka D, Hammel P, Maire F, Rufat P, Madeira I, Pessione F, Lévy P, Ruszniewski P. Risk of pancreatic adenocarcinoma in chronic pancreatitis. Gut. 2002;51:849–52.PubMedPubMedCentralCrossRef
121.
go back to reference Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur BK, Becker A, Hoshino A, Mark MT, Molina H, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 2015;17:816–26.PubMedPubMedCentralCrossRef Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur BK, Becker A, Hoshino A, Mark MT, Molina H, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 2015;17:816–26.PubMedPubMedCentralCrossRef
122.
go back to reference Robinson SM, Fan L, White SA, Charnley RM, Mann J. The role of exosomes in the pathogenesis of pancreatic ductal adenocarcinoma. International J Biochem Cell B. 2016;7:131–9.CrossRef Robinson SM, Fan L, White SA, Charnley RM, Mann J. The role of exosomes in the pathogenesis of pancreatic ductal adenocarcinoma. International J Biochem Cell B. 2016;7:131–9.CrossRef
123.
go back to reference Hoshino A, Costa-Silva B, Shen T, Rodrigues G, Hashimoto A. Tumor exosome integrins determine organotropic metastasis. Nature. 2016;27:329–35. Hoshino A, Costa-Silva B, Shen T, Rodrigues G, Hashimoto A. Tumor exosome integrins determine organotropic metastasis. Nature. 2016;27:329–35.
124.
go back to reference Sceneay J, Smyth MJ, Möller A. The pre-metastatic niche: finding common ground. Cancer Metastasis Rev. 2013;32(3–4):449–64.PubMedCrossRef Sceneay J, Smyth MJ, Möller A. The pre-metastatic niche: finding common ground. Cancer Metastasis Rev. 2013;32(3–4):449–64.PubMedCrossRef
125.
go back to reference Funamizu N, Hu C, Lacy C, Schetter A, Zhang G, He P, Gaedcke J, Ghadimi BM, Ried T, Yfantis HG, et al. Macrophage migration inhibitory factor induces epithelial to mesenchymal transition, enhances tumor aggressiveness and predicts clinical outcome in resected pancreatic ductal adenocarcinoma. Carcinogenesis. 2012;132:785–94. Funamizu N, Hu C, Lacy C, Schetter A, Zhang G, He P, Gaedcke J, Ghadimi BM, Ried T, Yfantis HG, et al. Macrophage migration inhibitory factor induces epithelial to mesenchymal transition, enhances tumor aggressiveness and predicts clinical outcome in resected pancreatic ductal adenocarcinoma. Carcinogenesis. 2012;132:785–94.
126.
go back to reference Datta J, Vollmer CM Jr. Investigational biomarkers for pancreatic adenocarcinoma: where do we stand? South Med J. 2014;107:256–63.PubMedCrossRef Datta J, Vollmer CM Jr. Investigational biomarkers for pancreatic adenocarcinoma: where do we stand? South Med J. 2014;107:256–63.PubMedCrossRef
127.
go back to reference Pavai S, Yap SF. The clinical significance of elevated levels of serum CA 19-9. Med J Malaysia. 2003;58:667–72.PubMed Pavai S, Yap SF. The clinical significance of elevated levels of serum CA 19-9. Med J Malaysia. 2003;58:667–72.PubMed
128.
go back to reference Goonetilleke KS, Siriwardena AK. Systematic review of carbohydrate antigen (CA 19-9) as a biochemical marker in the diagnosis of pancreatic cancer. Eur J Surg Oncol. 2007;33:266–70.PubMedCrossRef Goonetilleke KS, Siriwardena AK. Systematic review of carbohydrate antigen (CA 19-9) as a biochemical marker in the diagnosis of pancreatic cancer. Eur J Surg Oncol. 2007;33:266–70.PubMedCrossRef
129.
go back to reference Duffy MJ, Sturgeon C, Lamerz R, Haglund C, Holubec VL, Klapdor R, Nicolini A, Topolcan O, Heinemann V. Tumor markers in pancreatic cancer: a European group on tumor markers (EGTM) status report. Ann Oncol. 2010;21:441–7.PubMedCrossRef Duffy MJ, Sturgeon C, Lamerz R, Haglund C, Holubec VL, Klapdor R, Nicolini A, Topolcan O, Heinemann V. Tumor markers in pancreatic cancer: a European group on tumor markers (EGTM) status report. Ann Oncol. 2010;21:441–7.PubMedCrossRef
130.
go back to reference Melo SA, Luecke LB, Kahlert C, Fernandez AF, Gammon ST, Kaye J, LeBleu VS, Mittendorf EA, Weitz J, Rahbari N, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 2015;523:177–82.PubMedPubMedCentralCrossRef Melo SA, Luecke LB, Kahlert C, Fernandez AF, Gammon ST, Kaye J, LeBleu VS, Mittendorf EA, Weitz J, Rahbari N, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 2015;523:177–82.PubMedPubMedCentralCrossRef
133.
go back to reference Nielsen SR, Quaranta V, Linford A, Emeagi P, Rainer C, Santos A, Santos A, Ireland L, Sakai T, Sakai K, Kim YS, et al. Macrophage-secreted granulin supports pancreatic cancer metastasis by inducing liver fibrosis. Nat Cell Biol. 2016;18:549–60.PubMedPubMedCentralCrossRef Nielsen SR, Quaranta V, Linford A, Emeagi P, Rainer C, Santos A, Santos A, Ireland L, Sakai T, Sakai K, Kim YS, et al. Macrophage-secreted granulin supports pancreatic cancer metastasis by inducing liver fibrosis. Nat Cell Biol. 2016;18:549–60.PubMedPubMedCentralCrossRef
134.
go back to reference Sanford DE, Belt BA, Panni RZ, Mayer A, Deshpande AD, Carpenter D, Mitchem JB, Plambeck-Suess SM, Worley LA, Goetz BD, et al. Inflammatory monocyte mobilization decreases patient survival in pancreatic cancer: a role for targeting the CCL2/CCR2 axis. Clin Cancer Res. 2013;19:3404–15.PubMedPubMedCentralCrossRef Sanford DE, Belt BA, Panni RZ, Mayer A, Deshpande AD, Carpenter D, Mitchem JB, Plambeck-Suess SM, Worley LA, Goetz BD, et al. Inflammatory monocyte mobilization decreases patient survival in pancreatic cancer: a role for targeting the CCL2/CCR2 axis. Clin Cancer Res. 2013;19:3404–15.PubMedPubMedCentralCrossRef
135.
go back to reference Schmid MC, Avraamides CJ, Foubert P, Shaked Y, Kang SW, Kerbel RS, Varner JA. Combined blockade of integrin-α4β1 plus cytokines SDF-1α or IL-1β potently inhibits tumor inflammation and growth. Cancer Res. 2011;71:6965–75.PubMedPubMedCentralCrossRef Schmid MC, Avraamides CJ, Foubert P, Shaked Y, Kang SW, Kerbel RS, Varner JA. Combined blockade of integrin-α4β1 plus cytokines SDF-1α or IL-1β potently inhibits tumor inflammation and growth. Cancer Res. 2011;71:6965–75.PubMedPubMedCentralCrossRef
136.
go back to reference Quaranta V, Rainer C, Nielsen SR, Raymant M, Ahmed MS, Engle D, Taylor A, Murray T, Campbell F, Palmer D, et al. Macrophage-derived granulin drives resistance to immune checkpoint inhibition in metastatic pancreatic cancer. BioRxiv. 2017; https://doi.org/10.1101/234906. Quaranta V, Rainer C, Nielsen SR, Raymant M, Ahmed MS, Engle D, Taylor A, Murray T, Campbell F, Palmer D, et al. Macrophage-derived granulin drives resistance to immune checkpoint inhibition in metastatic pancreatic cancer. BioRxiv. 2017; https://​doi.​org/​10.​1101/​234906.
137.
go back to reference He Z, Ong CH, Halper J, Bateman A. Progranulin is a mediator of the wound response. Nat Med. 2003;9:225–9.PubMedCrossRef He Z, Ong CH, Halper J, Bateman A. Progranulin is a mediator of the wound response. Nat Med. 2003;9:225–9.PubMedCrossRef
138.
go back to reference Elkabets M, Gifford AM, Scheel C, Nilsson B, Reinhardt F, Bray MA, Carpenter AE, Jirström K, Magnusson K, Ebert BL, et al. Human tumors instigate granulin-expressing hematopoietic cells that promote malignancy by activating stromal fibroblasts in mice. J Clin Invest. 2011;121:784–99.PubMedPubMedCentralCrossRef Elkabets M, Gifford AM, Scheel C, Nilsson B, Reinhardt F, Bray MA, Carpenter AE, Jirström K, Magnusson K, Ebert BL, et al. Human tumors instigate granulin-expressing hematopoietic cells that promote malignancy by activating stromal fibroblasts in mice. J Clin Invest. 2011;121:784–99.PubMedPubMedCentralCrossRef
139.
go back to reference Bao S, Ouyang G, Bai X, Huang Z, Ma C, Liu M, Shao R, Anderson RM, Rich JN, Wang XF. Periostin potently promotes metastastic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell. 2004;5:329–39.PubMedCrossRef Bao S, Ouyang G, Bai X, Huang Z, Ma C, Liu M, Shao R, Anderson RM, Rich JN, Wang XF. Periostin potently promotes metastastic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell. 2004;5:329–39.PubMedCrossRef
140.
go back to reference Malanchi I, Santamaria-Martínez A, Susanto E, Peng H, Lehr HA, Delaloye JF, Huelsken J. Interactions between cancer stem cells and their niche governs metastatic colonization. Nature. 2011;481:85–9.PubMedCrossRef Malanchi I, Santamaria-Martínez A, Susanto E, Peng H, Lehr HA, Delaloye JF, Huelsken J. Interactions between cancer stem cells and their niche governs metastatic colonization. Nature. 2011;481:85–9.PubMedCrossRef
141.
go back to reference Erez N. Fibroblasts form a hospitable metastatic niche in the liver. Nat Cell Biol. 2016;18:465–6.PubMedCrossRef Erez N. Fibroblasts form a hospitable metastatic niche in the liver. Nat Cell Biol. 2016;18:465–6.PubMedCrossRef
142.
go back to reference Goedegebuure P, Mitchem JB, Porembka MR, Tan MCB, Belt BA, Wang-Gillam A, Gillanders WE, Hawkins WG, Linehan DC. Myeloid-derived suppressor cells: general characteristics and relevance to clinical management of pancreatic cancer. Curr Cancer Drug Tar. 2011;11:734–51.CrossRef Goedegebuure P, Mitchem JB, Porembka MR, Tan MCB, Belt BA, Wang-Gillam A, Gillanders WE, Hawkins WG, Linehan DC. Myeloid-derived suppressor cells: general characteristics and relevance to clinical management of pancreatic cancer. Curr Cancer Drug Tar. 2011;11:734–51.CrossRef
144.
go back to reference Almand B, Clark JI, Nikitina E, Van Beynen J, English NR, Knight SC, Carbone DP, Gabrilovich DI. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J Immunol. 2001;166:678–89.PubMedCrossRef Almand B, Clark JI, Nikitina E, Van Beynen J, English NR, Knight SC, Carbone DP, Gabrilovich DI. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J Immunol. 2001;166:678–89.PubMedCrossRef
145.
go back to reference Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, Montero AJ. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin–cyclophosphamide chemotherapy. Cancer Immunol. 2009;58:49–59.CrossRef Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, Montero AJ. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin–cyclophosphamide chemotherapy. Cancer Immunol. 2009;58:49–59.CrossRef
146.
go back to reference Zhang B, Wang Z, Wu L, Zhang M, Li W, Ding J, Zhu J, Wei H, Zhao K. Circulating and tumor-infiltrating myeloid-derived suppressor cells in patients with colorectal carcinoma. PLoS One. 2013;8:e57114.PubMedPubMedCentralCrossRef Zhang B, Wang Z, Wu L, Zhang M, Li W, Ding J, Zhu J, Wei H, Zhao K. Circulating and tumor-infiltrating myeloid-derived suppressor cells in patients with colorectal carcinoma. PLoS One. 2013;8:e57114.PubMedPubMedCentralCrossRef
147.
go back to reference OuYang L, Wu X, Ye S, Zhang R, Li Z, Liao W, Pan ZZ, Zheng LM, Zhang XS, Wang Z, et al. Tumor-induced myeloid-derived suppressor cells promote tumor progression through oxidative metabolism in human colorectal cancer. J Transl Med. 2015;13:47.PubMedPubMedCentralCrossRef OuYang L, Wu X, Ye S, Zhang R, Li Z, Liao W, Pan ZZ, Zheng LM, Zhang XS, Wang Z, et al. Tumor-induced myeloid-derived suppressor cells promote tumor progression through oxidative metabolism in human colorectal cancer. J Transl Med. 2015;13:47.PubMedPubMedCentralCrossRef
148.
go back to reference Zea AH, Rodriguez PC, Atkins MB, Hernandez C, Signoretti S, Zabaleta J, McDermott D, Quiceno D, Youmans A, O’Neill A, et al. Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res. 2005;65:3044–8.PubMedCrossRef Zea AH, Rodriguez PC, Atkins MB, Hernandez C, Signoretti S, Zabaleta J, McDermott D, Quiceno D, Youmans A, O’Neill A, et al. Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res. 2005;65:3044–8.PubMedCrossRef
149.
go back to reference Porembka MR, Mitchem JB, Belt BA, Hsieh C, Lee H, Herndon J, Gillanders WE, Linehan DC, Goedegebuure P. Pancreatic adenocarcinoma induces bone marrow mobilization of myeloid-derived suppressor cells which promote primary tumor growth. Cancer Immunol. 2012;61:1373–85.CrossRef Porembka MR, Mitchem JB, Belt BA, Hsieh C, Lee H, Herndon J, Gillanders WE, Linehan DC, Goedegebuure P. Pancreatic adenocarcinoma induces bone marrow mobilization of myeloid-derived suppressor cells which promote primary tumor growth. Cancer Immunol. 2012;61:1373–85.CrossRef
150.
go back to reference Xu X, Hu J, Wang M, Peng F, Tian R, Guo XJ, Xie Y, Qin RY. Circulating myeloid-derived suppressor cells in patients with pancreatic cancer. Hepatob Pancreat Dis. 2016;15:99–105.CrossRef Xu X, Hu J, Wang M, Peng F, Tian R, Guo XJ, Xie Y, Qin RY. Circulating myeloid-derived suppressor cells in patients with pancreatic cancer. Hepatob Pancreat Dis. 2016;15:99–105.CrossRef
151.
go back to reference Khaled YS, Ammori BJ, Elkord E. Increased levels of granulocytic myeloid-derived suppressor cells in peripheral blood and tumor tissue of pancreatic cancer patients. J Immunol Res. 2014;2014:879897.PubMedPubMedCentralCrossRef Khaled YS, Ammori BJ, Elkord E. Increased levels of granulocytic myeloid-derived suppressor cells in peripheral blood and tumor tissue of pancreatic cancer patients. J Immunol Res. 2014;2014:879897.PubMedPubMedCentralCrossRef
152.
go back to reference Panni RZ, Sanford DE, Belt BA, Mitchem JB, Worley LA, Goetz BD, Mukherjee P, Wang-Gillam A, Link DC, Denardo DG, et al. Tumor-induced STAT3 activation in monocytic myeloid-derived suppressor cells enhances stemness and mesenchymal properties in human pancreatic cancer. Cancer Immunol. 2014;63:513–28.CrossRef Panni RZ, Sanford DE, Belt BA, Mitchem JB, Worley LA, Goetz BD, Mukherjee P, Wang-Gillam A, Link DC, Denardo DG, et al. Tumor-induced STAT3 activation in monocytic myeloid-derived suppressor cells enhances stemness and mesenchymal properties in human pancreatic cancer. Cancer Immunol. 2014;63:513–28.CrossRef
153.
go back to reference Javeed N, Gustafson MP, Dutta SK, Lin Y, Bamlet WR, et al. Immunosuppressive CD14+HLA-DRlo/neg monocytes are elevated in pancreatic cancer and “primed” by tumor-derived exosomes. Oncoimmunology. 2017;6:e1252013.PubMedCrossRef Javeed N, Gustafson MP, Dutta SK, Lin Y, Bamlet WR, et al. Immunosuppressive CD14+HLA-DRlo/neg monocytes are elevated in pancreatic cancer and “primed” by tumor-derived exosomes. Oncoimmunology. 2017;6:e1252013.PubMedCrossRef
154.
go back to reference Rodriguez PC, Ernstoff MS, Hernandez C, Atkins M, Zabaleta J, Sierra R, Ochoa AC. Arginase I-producing myeloid-derived suppressor cells in renal cell carcinoma are a subpopulation of activated granulocytes. Cancer Res. 2009;69:1553–60.PubMedPubMedCentralCrossRef Rodriguez PC, Ernstoff MS, Hernandez C, Atkins M, Zabaleta J, Sierra R, Ochoa AC. Arginase I-producing myeloid-derived suppressor cells in renal cell carcinoma are a subpopulation of activated granulocytes. Cancer Res. 2009;69:1553–60.PubMedPubMedCentralCrossRef
155.
go back to reference Serafini P, Borrello I, Bronte V. Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin Cancer Biol. 2006;16:53–65.PubMedCrossRef Serafini P, Borrello I, Bronte V. Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin Cancer Biol. 2006;16:53–65.PubMedCrossRef
156.
go back to reference Gerner EW, Meyskens FL Jr. Polyamines and cancer: old molecules, new understanding. Nat Rev Cancer. 2004;4:781–92.PubMedCrossRef Gerner EW, Meyskens FL Jr. Polyamines and cancer: old molecules, new understanding. Nat Rev Cancer. 2004;4:781–92.PubMedCrossRef
157.
go back to reference Schmielau J, Finn OJ. Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of T-cell function in advanced cancer patients. Cancer Res. 2001;61:4756–60.PubMed Schmielau J, Finn OJ. Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of T-cell function in advanced cancer patients. Cancer Res. 2001;61:4756–60.PubMed
158.
go back to reference Nagaraj S, Gupta K, Pisarev V, Kinarsky L, Sherman S, Kang L, Herber D, Schneck J, Gabrilovich ID. Altered recognition of antigen is a novel mechanism of CD8+ T cell tolerance in cancer. Nat Med. 2007;13:828–35.PubMedPubMedCentralCrossRef Nagaraj S, Gupta K, Pisarev V, Kinarsky L, Sherman S, Kang L, Herber D, Schneck J, Gabrilovich ID. Altered recognition of antigen is a novel mechanism of CD8+ T cell tolerance in cancer. Nat Med. 2007;13:828–35.PubMedPubMedCentralCrossRef
159.
go back to reference Nagaraj S, Schrum AG, Cho H, Celis E, Gabrilovich DI. Mechanism of T-cell tolerance induced by myeloid-derived suppressor cells. J Immunol. 2010;184:3106–16.PubMedPubMedCentralCrossRef Nagaraj S, Schrum AG, Cho H, Celis E, Gabrilovich DI. Mechanism of T-cell tolerance induced by myeloid-derived suppressor cells. J Immunol. 2010;184:3106–16.PubMedPubMedCentralCrossRef
160.
go back to reference Clark CE, Hingorani SR, Mick R, Combs C, Tuveson DA, Vonderheide RH. Dynamics of the immune reaction to pancreatic cancer from inception to invasion. Cancer Res. 2007;67:9518–27.PubMedCrossRef Clark CE, Hingorani SR, Mick R, Combs C, Tuveson DA, Vonderheide RH. Dynamics of the immune reaction to pancreatic cancer from inception to invasion. Cancer Res. 2007;67:9518–27.PubMedCrossRef
161.
go back to reference Stromnes IM, Brockenbrough S, Izeradjene K, Carlson MA, Cuevas C, Simmons RM, Greenberg PD, Hingorani SR. Targeted depletion of a MDSC subset unmasks pancreatic ductal adenocarcinoma to adaptive immunity. Gut. 2014;63:1769–81.PubMedPubMedCentralCrossRef Stromnes IM, Brockenbrough S, Izeradjene K, Carlson MA, Cuevas C, Simmons RM, Greenberg PD, Hingorani SR. Targeted depletion of a MDSC subset unmasks pancreatic ductal adenocarcinoma to adaptive immunity. Gut. 2014;63:1769–81.PubMedPubMedCentralCrossRef
162.
go back to reference Liu C, Yu S, Kappes J, Wang J, Grizzle WE, Zinn KR, Zhang HG. Expansion of spleen myeloid suppressor cells represses NK cell cytotoxicity in tumor-bearing host. Blood. 2007;109:4336–42.PubMedPubMedCentralCrossRef Liu C, Yu S, Kappes J, Wang J, Grizzle WE, Zinn KR, Zhang HG. Expansion of spleen myeloid suppressor cells represses NK cell cytotoxicity in tumor-bearing host. Blood. 2007;109:4336–42.PubMedPubMedCentralCrossRef
163.
go back to reference Li H, Han Y, Guo Q, Zhang M, Cao X. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-β1. J Immunol. 2009;182:240–9.PubMedCrossRef Li H, Han Y, Guo Q, Zhang M, Cao X. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-β1. J Immunol. 2009;182:240–9.PubMedCrossRef
164.
go back to reference Huang B, Pan PY, Li Q, Sato AI, Levy DE, Bromberg J, Divino CM, Chen SH. Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res. 2006;66:1123–31.PubMedCrossRef Huang B, Pan PY, Li Q, Sato AI, Levy DE, Bromberg J, Divino CM, Chen SH. Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res. 2006;66:1123–31.PubMedCrossRef
165.
go back to reference Liyanage UK, Moore TT, Joo HG, Tanaka Y, Herrmann V, Doherty G, Drebin JA, Strasberg SM, Eberlein TJ, Goedegebuure PS, et al. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J Immunol. 2002;169:2756–61.PubMedCrossRef Liyanage UK, Moore TT, Joo HG, Tanaka Y, Herrmann V, Doherty G, Drebin JA, Strasberg SM, Eberlein TJ, Goedegebuure PS, et al. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J Immunol. 2002;169:2756–61.PubMedCrossRef
166.
go back to reference Qu X, Zhuang G, Yu L, Meng G, Ferrara N. Induction of Bv8 expression by granulocyte colony-stimulating factor in CD11b+Gr1+ cells: key role of Stat3 signaling. J Biol Chem. 2012;287:19574–84.PubMedPubMedCentralCrossRef Qu X, Zhuang G, Yu L, Meng G, Ferrara N. Induction of Bv8 expression by granulocyte colony-stimulating factor in CD11b+Gr1+ cells: key role of Stat3 signaling. J Biol Chem. 2012;287:19574–84.PubMedPubMedCentralCrossRef
167.
go back to reference Kujawski M, Kortylewski M, Lee H, Herrmann A, Kay H, Yu H. Stat3 mediates myeloid cell-dependent tumor angiogenesis in mice. J Clin Invest. 2008;118:3367–77.PubMedPubMedCentralCrossRef Kujawski M, Kortylewski M, Lee H, Herrmann A, Kay H, Yu H. Stat3 mediates myeloid cell-dependent tumor angiogenesis in mice. J Clin Invest. 2008;118:3367–77.PubMedPubMedCentralCrossRef
168.
go back to reference Yang L, DeBusk LM, Fukuda K, Fingleton B, Green-Jarvis B, Shyr Y, Matrisian LM, Carbone DP, Lin PC. Expansion of myeloid immune suppressor gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell. 2004;6:409–21.PubMedCrossRef Yang L, DeBusk LM, Fukuda K, Fingleton B, Green-Jarvis B, Shyr Y, Matrisian LM, Carbone DP, Lin PC. Expansion of myeloid immune suppressor gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell. 2004;6:409–21.PubMedCrossRef
169.
go back to reference Melani C, Sangaletti S, Barazzetta FM, Werb Z, Colombo MP. Amino-biphosphonate-mediated MMP-9 inhibition breaks the tumor-bone marrow axis responsible for myeloid-derived suppressor cell expansion and macrophage infiltration in tumor stroma. Cancer Res. 2007;67:11438–46.PubMedPubMedCentralCrossRef Melani C, Sangaletti S, Barazzetta FM, Werb Z, Colombo MP. Amino-biphosphonate-mediated MMP-9 inhibition breaks the tumor-bone marrow axis responsible for myeloid-derived suppressor cell expansion and macrophage infiltration in tumor stroma. Cancer Res. 2007;67:11438–46.PubMedPubMedCentralCrossRef
170.
go back to reference Steele CW, Karim SA, Leach JDG, Bailey P, Upstill-Goddard R, Rishi L, Foth M, Bryson S, McDaid K, Wilson Z, et al. CXCR2 inhibition profoundly suppresses metastases and augments immunotherapy in pancreatic ductal adenocarcinoma. Cancer Cell. 2016;29:832–45.PubMedPubMedCentralCrossRef Steele CW, Karim SA, Leach JDG, Bailey P, Upstill-Goddard R, Rishi L, Foth M, Bryson S, McDaid K, Wilson Z, et al. CXCR2 inhibition profoundly suppresses metastases and augments immunotherapy in pancreatic ductal adenocarcinoma. Cancer Cell. 2016;29:832–45.PubMedPubMedCentralCrossRef
171.
go back to reference Ilkovitch D, Lopez DM. The liver is a site for tumor-induced myeloid-derived suppressor cell accumulation and immunosuppression. Cancer Res. 2009;69:5514–21.PubMedPubMedCentralCrossRef Ilkovitch D, Lopez DM. The liver is a site for tumor-induced myeloid-derived suppressor cell accumulation and immunosuppression. Cancer Res. 2009;69:5514–21.PubMedPubMedCentralCrossRef
172.
go back to reference Connolly MK, Mallen-St Clair J, Bedroian AS, Malhotra A, Vera V, Ibrahim J, Henning J, Pachter HL, Bar-Sagi D, Frey AB, et al. Distinct populations of metastases-enabling myeloid cells expand in the liver of mice harboring invasive and preinvasive intra-abdominal tumor. J Leukoc Biol. 2010;87:713–25.PubMedCrossRef Connolly MK, Mallen-St Clair J, Bedroian AS, Malhotra A, Vera V, Ibrahim J, Henning J, Pachter HL, Bar-Sagi D, Frey AB, et al. Distinct populations of metastases-enabling myeloid cells expand in the liver of mice harboring invasive and preinvasive intra-abdominal tumor. J Leukoc Biol. 2010;87:713–25.PubMedCrossRef
173.
go back to reference Zhao F, Obermann S, Von Wasielewski R, Haile L, Manns MP, Korangy F, Greten TF. Increase in frequency of myeloid-derived suppressor cells in mice with spontaneous pancreatic carcinoma. Immunology. 2009;128:141–9.PubMedPubMedCentralCrossRef Zhao F, Obermann S, Von Wasielewski R, Haile L, Manns MP, Korangy F, Greten TF. Increase in frequency of myeloid-derived suppressor cells in mice with spontaneous pancreatic carcinoma. Immunology. 2009;128:141–9.PubMedPubMedCentralCrossRef
174.
go back to reference Bayne LJ, Beatty GL, Jhala N, Clark CE, Rhim AD, Stanger BZ, Vonderheide RH. Tumor-derived granulocyte-macrophage colony-stimulating factor regulates myeloid inflammation and T cell immunity in pancreatic cancer. Cancer Cell. 2012;21:822–35.PubMedPubMedCentralCrossRef Bayne LJ, Beatty GL, Jhala N, Clark CE, Rhim AD, Stanger BZ, Vonderheide RH. Tumor-derived granulocyte-macrophage colony-stimulating factor regulates myeloid inflammation and T cell immunity in pancreatic cancer. Cancer Cell. 2012;21:822–35.PubMedPubMedCentralCrossRef
175.
go back to reference Song J, Lee J, Kim J, Jo S, Kim YJ, Baek JE, Kwon ES, Lee KP, Yang S, Kwon KS, et al. Pancreatic adenocarcinoma up-regulated factor (PAUF) enhances the accumulation and functional activity of myeloid-derived suppressor cells (MDSCs) in pancreatic cancer. Oncotarget. 2016;7:51840–53.PubMedPubMedCentral Song J, Lee J, Kim J, Jo S, Kim YJ, Baek JE, Kwon ES, Lee KP, Yang S, Kwon KS, et al. Pancreatic adenocarcinoma up-regulated factor (PAUF) enhances the accumulation and functional activity of myeloid-derived suppressor cells (MDSCs) in pancreatic cancer. Oncotarget. 2016;7:51840–53.PubMedPubMedCentral
176.
go back to reference Mace TA, Ameen Z, Collins A, Wojcik S, Mair M, Young GS, Fuchs JR, Eubank TD, Frankel WL, Bekaii-Saab T, et al. Pancreatic cancer-associated stellate cells promote differentiation of myeloid-derived suppressor cells in a STAT3-dependent manner. Cancer Res. 2013;73:3007–18.PubMedPubMedCentralCrossRef Mace TA, Ameen Z, Collins A, Wojcik S, Mair M, Young GS, Fuchs JR, Eubank TD, Frankel WL, Bekaii-Saab T, et al. Pancreatic cancer-associated stellate cells promote differentiation of myeloid-derived suppressor cells in a STAT3-dependent manner. Cancer Res. 2013;73:3007–18.PubMedPubMedCentralCrossRef
177.
go back to reference Basso D, Gnatta E, Padoan A, Fogar P, Furlanello S, Aita A, Bozzato D, Zambon F, Arrigoni G, Frasson C, et al. PDAC-derived exosomes enrich the microenvironment in MDSCs in a SMAD4-dependent manner through a new calcium related axis. Oncotarget. 2017;8:84928–44.PubMedPubMedCentralCrossRef Basso D, Gnatta E, Padoan A, Fogar P, Furlanello S, Aita A, Bozzato D, Zambon F, Arrigoni G, Frasson C, et al. PDAC-derived exosomes enrich the microenvironment in MDSCs in a SMAD4-dependent manner through a new calcium related axis. Oncotarget. 2017;8:84928–44.PubMedPubMedCentralCrossRef
178.
go back to reference Yachida S, Jones S, Bozic I, Antal T, Leary R, Fu B, Kamiyama M, Hruban RH, Eshleman JR, Nowak MA, et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature. 2010;467:1114–7.PubMedPubMedCentralCrossRef Yachida S, Jones S, Bozic I, Antal T, Leary R, Fu B, Kamiyama M, Hruban RH, Eshleman JR, Nowak MA, et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature. 2010;467:1114–7.PubMedPubMedCentralCrossRef
180.
go back to reference Kakkar AK, Lemoine NR, Scully MF, Tebbutt S, Williamson RC. Tissue factor expression correlates with histological grade in human pancreatic cancer. Brit J Surg. 1995;82:1101–4.PubMedCrossRef Kakkar AK, Lemoine NR, Scully MF, Tebbutt S, Williamson RC. Tissue factor expression correlates with histological grade in human pancreatic cancer. Brit J Surg. 1995;82:1101–4.PubMedCrossRef
181.
go back to reference Nitori N, Ino Y, Nakanishi Y, Yamada T, Honda K, Yanagihara K, Kosuge T, Kanai Y, Kitajima M, Hirohashi S. Prognostic significance of tissue factor in pancreatic ductal adenocarcinoma. Clin Cancer Res. 2005;11:2531–9.PubMedCrossRef Nitori N, Ino Y, Nakanishi Y, Yamada T, Honda K, Yanagihara K, Kosuge T, Kanai Y, Kitajima M, Hirohashi S. Prognostic significance of tissue factor in pancreatic ductal adenocarcinoma. Clin Cancer Res. 2005;11:2531–9.PubMedCrossRef
182.
go back to reference Saito Y, Hashimoto Y, Kuroda J, Yasunaga M, Koga Y, Takahashi A, Matsumura Y. The inhibition of pancreatic cancer invasion-metastasis cascade in both cellular signal and blood coagulation cascade of tissue factor by its neutralisation antibody. Eur J Cancer. 2011;47:2230–9.PubMedCrossRef Saito Y, Hashimoto Y, Kuroda J, Yasunaga M, Koga Y, Takahashi A, Matsumura Y. The inhibition of pancreatic cancer invasion-metastasis cascade in both cellular signal and blood coagulation cascade of tissue factor by its neutralisation antibody. Eur J Cancer. 2011;47:2230–9.PubMedCrossRef
183.
go back to reference Krüger A, Soeltl R, Sopov I, Kopitz C, Arlt M, Magdolen V, Harbeck N, Gänsbacher B, Schmitt M. Hydroxamate-type matrix metalloproteinase inhibitor batimastat promotes liver metastasis. Cancer Res. 2001;61:1272–5.PubMed Krüger A, Soeltl R, Sopov I, Kopitz C, Arlt M, Magdolen V, Harbeck N, Gänsbacher B, Schmitt M. Hydroxamate-type matrix metalloproteinase inhibitor batimastat promotes liver metastasis. Cancer Res. 2001;61:1272–5.PubMed
184.
go back to reference Tester AM, Waltham M, Oh SJ, Bae SN, Bills MM, Walker EC, Kern FG, Stetler-Stevenson WG, Lippman ME, Thompson EW. Pro-matrix metalloproteinase-2 transfection increases orthotopic primary growth and experimental metastasis of MDA-MB-231 human breast cancer cells in nude mice. Cancer Res. 2004;64:652–8.PubMedCrossRef Tester AM, Waltham M, Oh SJ, Bae SN, Bills MM, Walker EC, Kern FG, Stetler-Stevenson WG, Lippman ME, Thompson EW. Pro-matrix metalloproteinase-2 transfection increases orthotopic primary growth and experimental metastasis of MDA-MB-231 human breast cancer cells in nude mice. Cancer Res. 2004;64:652–8.PubMedCrossRef
185.
go back to reference Kopitz C, Anton M, Gansbacher B, Krüger A. Reduction of experimental human fibrosarcoma lung metastasis in mice by adenovirus-mediated cystatin C overexpression in the host. Cancer Res. 2005;65:8608–12.PubMedCrossRef Kopitz C, Anton M, Gansbacher B, Krüger A. Reduction of experimental human fibrosarcoma lung metastasis in mice by adenovirus-mediated cystatin C overexpression in the host. Cancer Res. 2005;65:8608–12.PubMedCrossRef
186.
go back to reference Yu Z, Zhao S, Ren L, Wang L, Chen Z, Hoffman RM, Zhou J. Pancreatic cancer-derived exosomes promote tumor metastasis and liver pre-metastatic niche formation. Oncotarget. 2017;8:63461–83.PubMedPubMedCentral Yu Z, Zhao S, Ren L, Wang L, Chen Z, Hoffman RM, Zhou J. Pancreatic cancer-derived exosomes promote tumor metastasis and liver pre-metastatic niche formation. Oncotarget. 2017;8:63461–83.PubMedPubMedCentral
187.
go back to reference Nuzhat Z, Kinhal V, Sharma S, Rice GE, Joshi V, Salomon C. Tumour-derived exosomes as a signature of pancreatic cancer – liquid biopsies as indicators of tumour progression. Oncotarget. 2017;8:17279–91.PubMedCrossRef Nuzhat Z, Kinhal V, Sharma S, Rice GE, Joshi V, Salomon C. Tumour-derived exosomes as a signature of pancreatic cancer – liquid biopsies as indicators of tumour progression. Oncotarget. 2017;8:17279–91.PubMedCrossRef
188.
go back to reference Babic A, Wolpin BM. Circulating exosomes in pancreatic cancer: will they succeed on the long, littered road to early detection marker? Clin Chem. 2016;62:307–9.PubMedCrossRef Babic A, Wolpin BM. Circulating exosomes in pancreatic cancer: will they succeed on the long, littered road to early detection marker? Clin Chem. 2016;62:307–9.PubMedCrossRef
190.
go back to reference Krüger A. Premetastatic niche formation in the liver: emerging mechanisms and mouse models. J Mol Med. 2015;93:1193–201.PubMedCrossRef Krüger A. Premetastatic niche formation in the liver: emerging mechanisms and mouse models. J Mol Med. 2015;93:1193–201.PubMedCrossRef
191.
go back to reference Lai X, Wang M, McElyea SD, Sherman S, House M, Korc MA. microRNA signature in circulating exosomes is superior to exosomal glypican-1 levels for diagnosing pancreatic cancer. Cancer Lett. 2017;393:86–93.PubMedPubMedCentralCrossRef Lai X, Wang M, McElyea SD, Sherman S, House M, Korc MA. microRNA signature in circulating exosomes is superior to exosomal glypican-1 levels for diagnosing pancreatic cancer. Cancer Lett. 2017;393:86–93.PubMedPubMedCentralCrossRef
192.
go back to reference Madhavan B, Yue S, Galli U, Rana S, Gross W, Müller M, Giese NA, Kalthoff H, Becker T, Büchler MW, et al. Combined evaluation of a panel of protein and miRNA serum-exosome biomarkers for pancreatic cancer diagnosis increases sensitivity and specificity. Int J Cancer. 2015;136:2616–27.PubMedCrossRef Madhavan B, Yue S, Galli U, Rana S, Gross W, Müller M, Giese NA, Kalthoff H, Becker T, Büchler MW, et al. Combined evaluation of a panel of protein and miRNA serum-exosome biomarkers for pancreatic cancer diagnosis increases sensitivity and specificity. Int J Cancer. 2015;136:2616–27.PubMedCrossRef
193.
go back to reference Que R, Ding G, Chen J, Cao L. Analysis of serum exosomal microRNAs and clinicopathologic features of patients with pancreatic adenocarcinoma. World J Surg Oncol. 2013;11:219.PubMedPubMedCentralCrossRef Que R, Ding G, Chen J, Cao L. Analysis of serum exosomal microRNAs and clinicopathologic features of patients with pancreatic adenocarcinoma. World J Surg Oncol. 2013;11:219.PubMedPubMedCentralCrossRef
194.
go back to reference Kahlert C, Melo SA, Protopopov A, Tang J, Seth S, Koch M, Zhang J, Weitz J, Chin L, Futreal A, et al. Identification of double-stranded genomic DNA spanning all chromosomes with mutated KRAS and p53 DNA in the serum exosomes of patients with pancreatic cancer. J Biol Chem. 2014;289:3869–75.PubMedPubMedCentralCrossRef Kahlert C, Melo SA, Protopopov A, Tang J, Seth S, Koch M, Zhang J, Weitz J, Chin L, Futreal A, et al. Identification of double-stranded genomic DNA spanning all chromosomes with mutated KRAS and p53 DNA in the serum exosomes of patients with pancreatic cancer. J Biol Chem. 2014;289:3869–75.PubMedPubMedCentralCrossRef
Metadata
Title
The hepatic pre-metastatic niche in pancreatic ductal adenocarcinoma
Authors
Demi S. Houg
Maarten F. Bijlsma
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Molecular Cancer / Issue 1/2018
Electronic ISSN: 1476-4598
DOI
https://doi.org/10.1186/s12943-018-0842-9

Other articles of this Issue 1/2018

Molecular Cancer 1/2018 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine