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Published in: Journal of Experimental & Clinical Cancer Research 1/2019

Open Access 01-12-2019 | Biomarkers | Review

Collagens and Cancer associated fibroblasts in the reactive stroma and its relation to Cancer biology

Authors: Neel I. Nissen, Morten Karsdal, Nicholas Willumsen

Published in: Journal of Experimental & Clinical Cancer Research | Issue 1/2019

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Abstract

The extracellular matrix (ECM) plays an important role in cancer progression. It can be divided into the basement membrane (BM) that supports epithelial/endothelial cell behavior and the interstitial matrix (IM) that supports the underlying stromal compartment. The major components of the ECM are the collagens. While breaching of the BM and turnover of e.g. type IV collagen, is a well described part of tumorigenesis, less is known regarding the impact on tumorigenesis from the collagens residing in the stroma. Here we give an introduction and overview to the link between tumorigenesis and stromal collagens, with focus on the fibrillar collagens type I, II, III, V, XI, XXIV and XXVII as well as type VI collagen. Moreover, we discuss the impact of the cells responsible for this altered stromal collagen remodeling, the cancer associated fibroblasts (CAFs), and how these cells are key players in orchestrating the tumor microenvironment composition and tissue microarchitecture, hence also driving tumorigenesis and affecting response to treatment. Lastly, we discuss how specific collagen-derived biomarkers reflecting the turnover of stromal collagens and CAF activity may be used as tools to non-invasively interrogate stromal reactivity in the tumor microenvironment and predict response to treatment.
Literature
3.
go back to reference Ricard-blum S. The collagen family. Cold Spring Harb Perspect Biol. 2011;3(1):1–19. Ricard-blum S. The collagen family. Cold Spring Harb Perspect Biol. 2011;3(1):1–19.
4.
go back to reference Ivarsson M, McWhirter a, Borg TK, Rubin K. Type I collagen synthesis in cultured human fibroblasts: regulation by cell spreading, platelet-derived growth factor and interactions with collagen fibers. Matrix Biol. 1998; Ivarsson M, McWhirter a, Borg TK, Rubin K. Type I collagen synthesis in cultured human fibroblasts: regulation by cell spreading, platelet-derived growth factor and interactions with collagen fibers. Matrix Biol. 1998;
7.
go back to reference Zou Y, Zhang RZ, Sabatelli P, Chu ML, Bönnemann CG. Muscle interstitial fibroblasts are the main source of collagen VI synthesis in skeletal muscle: implications for congenital muscular dystrophy types Ullrich and Bethlem. J Neuropathol Exp Neurol. 2008. Zou Y, Zhang RZ, Sabatelli P, Chu ML, Bönnemann CG. Muscle interstitial fibroblasts are the main source of collagen VI synthesis in skeletal muscle: implications for congenital muscular dystrophy types Ullrich and Bethlem. J Neuropathol Exp Neurol. 2008.
8.
go back to reference Oxford JT, Doege KJ, Horton WE, Morris NP. Characterization of type II and type XI collagen synthesis by an immortalized rat chondrocyte cell line (IRC) having a low level of type II collagen mRNA expression. Exp Cell Res. 1994. Oxford JT, Doege KJ, Horton WE, Morris NP. Characterization of type II and type XI collagen synthesis by an immortalized rat chondrocyte cell line (IRC) having a low level of type II collagen mRNA expression. Exp Cell Res. 1994.
9.
go back to reference Bonnans C, Chou J, Werb Z. Remodelling the extracellular matrix in development and disease. Nat rev mol cell biol. 2014;15(12):786–801.PubMedPubMedCentral Bonnans C, Chou J, Werb Z. Remodelling the extracellular matrix in development and disease. Nat rev mol cell biol. 2014;15(12):786–801.PubMedPubMedCentral
10.
go back to reference Mason SD, Joyce J. a. Proteolytic networks in Cancer. Trends Cell Biol. 2011;21(4):1–18. Mason SD, Joyce J. a. Proteolytic networks in Cancer. Trends Cell Biol. 2011;21(4):1–18.
11.
go back to reference Kalluri R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nat Rev Cancer. 2003;3(6):422–33.PubMed Kalluri R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nat Rev Cancer. 2003;3(6):422–33.PubMed
12.
go back to reference Tanjore H, Kalluri R. The role of type IV collagen and basement membranes in cancer progression and metastasis. Am J Pathol. 2006;168(3):715–7.PubMedPubMedCentral Tanjore H, Kalluri R. The role of type IV collagen and basement membranes in cancer progression and metastasis. Am J Pathol. 2006;168(3):715–7.PubMedPubMedCentral
13.
go back to reference Xu J, Rodriguez D, Petitclerc E, Kim JJ, Hangai M, Moon Yuen S, et al. Proteolytic exposure of a cryptic site within collagen type IV is required for angiogenesis and tumor growth in vivo. J Cell Biol. 2001;154(5):1069–79.PubMedPubMedCentral Xu J, Rodriguez D, Petitclerc E, Kim JJ, Hangai M, Moon Yuen S, et al. Proteolytic exposure of a cryptic site within collagen type IV is required for angiogenesis and tumor growth in vivo. J Cell Biol. 2001;154(5):1069–79.PubMedPubMedCentral
14.
go back to reference Xu J, Rodriguez D, Kim JJ, Brooks PC. Generation of monoclonal antibodies to cryptic collagen sites by using subtractive immunization. Hybridoma. 2000;19(5):375–85.PubMed Xu J, Rodriguez D, Kim JJ, Brooks PC. Generation of monoclonal antibodies to cryptic collagen sites by using subtractive immunization. Hybridoma. 2000;19(5):375–85.PubMed
15.
go back to reference O’Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, et al. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell. 1997;88(2):277–85.PubMed O’Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, et al. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell. 1997;88(2):277–85.PubMed
17.
go back to reference Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006;6(5):392–401.PubMed Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006;6(5):392–401.PubMed
20.
go back to reference Pickup MW, Mouw JK, Weaver VM. The extracellular matrix modulates the hallmarks of cancer. EMBO Rep. 2014 Dec;15(12):1243–53.PubMedPubMedCentral Pickup MW, Mouw JK, Weaver VM. The extracellular matrix modulates the hallmarks of cancer. EMBO Rep. 2014 Dec;15(12):1243–53.PubMedPubMedCentral
21.
go back to reference Bager CL, Willumsen N, Leeming DJ, Smith V, Karsdal MA, Dornan D, et al. Collagen degradation products measured in serum can separate ovarian and breast cancer patients from healthy controls: a preliminary study. Cancer Biomarkers. 2015;15(6):783–8.PubMed Bager CL, Willumsen N, Leeming DJ, Smith V, Karsdal MA, Dornan D, et al. Collagen degradation products measured in serum can separate ovarian and breast cancer patients from healthy controls: a preliminary study. Cancer Biomarkers. 2015;15(6):783–8.PubMed
22.
go back to reference Willumsen N, Bager CL, Leeming DJ, Smith V, Karsdal M a, Dornan D, et al. Extracellular matrix specific protein fingerprints measured in serum can seperate pancreatic cancer patients from healthy controls. BMC Cancer [Internet]. 2013;13:554. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4222497&tool=pmcentrez&rendertype=abstract%5Cnhttp://www.ncbi.nlm.nih.gov/pubmed/24261855 Willumsen N, Bager CL, Leeming DJ, Smith V, Karsdal M a, Dornan D, et al. Extracellular matrix specific protein fingerprints measured in serum can seperate pancreatic cancer patients from healthy controls. BMC Cancer [Internet]. 2013;13:554. Available from: http://​www.​pubmedcentral.​nih.​gov/​articlerender.​fcgi?​artid=​4222497&​tool=​pmcentrez&​rendertype=​abstract%5Cnhttp://www.ncbi.nlm.nih.gov/pubmed/24261855
23.
go back to reference Willumsen N, Bager CL, Leeming DJ, Smith V, Christiansen C, Karsdal MA, et al. Serum biomarkers reflecting specific tumor tissue remodeling processes are valuable diagnostic tools for lung cancer. Cancer Med. 2014;3(5):1136–45.PubMedPubMedCentral Willumsen N, Bager CL, Leeming DJ, Smith V, Christiansen C, Karsdal MA, et al. Serum biomarkers reflecting specific tumor tissue remodeling processes are valuable diagnostic tools for lung cancer. Cancer Med. 2014;3(5):1136–45.PubMedPubMedCentral
24.
go back to reference Kehlet SN, Sanz-Pamplona R, Brix S, Leeming DJ, Karsdal MA, Moreno V. Excessive collagen turnover products are released during colorectal cancer progression and elevated in serum from metastatic colorectal cancer patients. Sci Rep [Internet] 2016;6(July):1–7. Available from: https://doi.org/10.1038/srep30599 Kehlet SN, Sanz-Pamplona R, Brix S, Leeming DJ, Karsdal MA, Moreno V. Excessive collagen turnover products are released during colorectal cancer progression and elevated in serum from metastatic colorectal cancer patients. Sci Rep [Internet] 2016;6(July):1–7. Available from: https://​doi.​org/​10.​1038/​srep30599
25.
go back to reference Leeming DJ, Koizumi M, Qvist P, Barkholt V, Zhang C, Henriksen K, et al. Serum N-Terminal Propeptide of Collagen Type I is Associated with the Number of Bone Metastases in Breast and Prostate Cancer and Correlates to Other Bone Related Markers. Biomark Cancer [Internet]. 2011;3:15–23. Available from: https://www.ncbi.nlm.nih.gov/pubmed/24179387 Leeming DJ, Koizumi M, Qvist P, Barkholt V, Zhang C, Henriksen K, et al. Serum N-Terminal Propeptide of Collagen Type I is Associated with the Number of Bone Metastases in Breast and Prostate Cancer and Correlates to Other Bone Related Markers. Biomark Cancer [Internet]. 2011;3:15–23. Available from: https://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​24179387
28.
go back to reference Meng X, Nikolic-Patersen D, Lan H. TGF-β the master regulator of fibrosis.Pdf. Nat Rev Nephrol. 2016;12(6):325–38.PubMed Meng X, Nikolic-Patersen D, Lan H. TGF-β the master regulator of fibrosis.Pdf. Nat Rev Nephrol. 2016;12(6):325–38.PubMed
29.
go back to reference Mertens JC, Fingas CD, Christensen JD, Smoot RL, Bronk SF, Werneburg NW, et al. Therapeutic effects of deleting cancer-associated fibroblasts in cholangiocarcinoma. Cancer Res. 2013. Mertens JC, Fingas CD, Christensen JD, Smoot RL, Bronk SF, Werneburg NW, et al. Therapeutic effects of deleting cancer-associated fibroblasts in cholangiocarcinoma. Cancer Res. 2013.
31.
go back to reference Radisky DC, Kenny PA, Bissel MJ. Fibrosis and Cancer: do Myofibroblasts come also from epithelial cells via EMT. NIH Public Access. 2007;101(4):830–9. Radisky DC, Kenny PA, Bissel MJ. Fibrosis and Cancer: do Myofibroblasts come also from epithelial cells via EMT. NIH Public Access. 2007;101(4):830–9.
32.
go back to reference Zeisberg EM, Potenta S, Xie L, Zeisberg M, Kalluri R. Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts. Cancer Res. 2007;67(21):10123–8.PubMed Zeisberg EM, Potenta S, Xie L, Zeisberg M, Kalluri R. Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts. Cancer Res. 2007;67(21):10123–8.PubMed
33.
go back to reference Gascard P, Tlsty TD. Carcinoma-associated fibroblasts: orchestrating the composition of malignancy. Genes Dev. 2016;30(9):1002–19.PubMedPubMedCentral Gascard P, Tlsty TD. Carcinoma-associated fibroblasts: orchestrating the composition of malignancy. Genes Dev. 2016;30(9):1002–19.PubMedPubMedCentral
34.
go back to reference Kauppila S, Stenback F, Risteli J, Jukkola A, Risteli L. Aberrant type I and type III collagen gene expression in human breast cancer in vivo. J Pathol. 1998;268(July):262–8. Kauppila S, Stenback F, Risteli J, Jukkola A, Risteli L. Aberrant type I and type III collagen gene expression in human breast cancer in vivo. J Pathol. 1998;268(July):262–8.
35.
go back to reference Hanley CJ, Noble F, Ward M, Bullock M, Drifka C, Mellone M, et al. A subset of myofibroblastic cancer-associated fibroblasts regulate collagen fiber elongation, which is prognostic in multiple cancers. Oncotarget [Internet] 2016;7(5):6159–6174. Available from: https://www.ncbi.nlm.nih.gov/pubmed/26716418 Hanley CJ, Noble F, Ward M, Bullock M, Drifka C, Mellone M, et al. A subset of myofibroblastic cancer-associated fibroblasts regulate collagen fiber elongation, which is prognostic in multiple cancers. Oncotarget [Internet] 2016;7(5):6159–6174. Available from: https://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​26716418
36.
go back to reference Öhlund D, Handly-Santana A, Biffi G, Elyada E, Almeida AS, Ponz-Sarvise M, et al. Distinct populations of inflammatory fibroblasts and myofibroblasts in pancreatic cancer. J Exp Med. 2017. Öhlund D, Handly-Santana A, Biffi G, Elyada E, Almeida AS, Ponz-Sarvise M, et al. Distinct populations of inflammatory fibroblasts and myofibroblasts in pancreatic cancer. J Exp Med. 2017.
37.
go back to reference Madar S, Goldstein I, Rotter V. “Cancer associated fibroblasts” - more than meets the eye. Trends in Molecular Medicine. 2013. Madar S, Goldstein I, Rotter V. “Cancer associated fibroblasts” - more than meets the eye. Trends in Molecular Medicine. 2013.
38.
go back to reference Wagner EF. Cancer: fibroblasts for all seasons. Nature. 2016. Wagner EF. Cancer: fibroblasts for all seasons. Nature. 2016.
39.
go back to reference Glentis A, Oertle P, Mariani P, Chikina A, El Marjou F, Attieh Y, et al. Cancer-associated fibroblasts induce metalloprotease-independent cancer cell invasion of the basement membrane. Nat Commun [Internet]. 2017;8(1):1–13. Available from: https://doi.org/10.1038/s41467-017-00985-8 Glentis A, Oertle P, Mariani P, Chikina A, El Marjou F, Attieh Y, et al. Cancer-associated fibroblasts induce metalloprotease-independent cancer cell invasion of the basement membrane. Nat Commun [Internet]. 2017;8(1):1–13. Available from: https://​doi.​org/​10.​1038/​s41467-017-00985-8
40.
go back to reference Alkasalias T, Moyano-Galceran L, Arsenian-Henriksson M, Lehti K. Fibroblasts in the tumor microenvironment: shield or spear? International journal of molecular sciences; 2018. Alkasalias T, Moyano-Galceran L, Arsenian-Henriksson M, Lehti K. Fibroblasts in the tumor microenvironment: shield or spear? International journal of molecular sciences; 2018.
41.
go back to reference Shekhar MP, Werdell J, Santner SJ, Pauley RJ, Tait L. Breast stroma plays a dominant regulatory role in breast epithelial growth and differentiation: implications for tumor development and progression. Cancer res [internet]. 2001;61(4):1320–1326. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11245428. Shekhar MP, Werdell J, Santner SJ, Pauley RJ, Tait L. Breast stroma plays a dominant regulatory role in breast epithelial growth and differentiation: implications for tumor development and progression. Cancer res [internet]. 2001;61(4):1320–1326. Available from: http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​11245428.
43.
go back to reference Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, Cunha GR. Carcinoma-associated Fibroblasts Direct Tumor Progression of Initiated HumanProstatic Epithelium.pdf. Ep Prostatic. 1999;5002–5011. Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, Cunha GR. Carcinoma-associated Fibroblasts Direct Tumor Progression of Initiated HumanProstatic Epithelium.pdf. Ep Prostatic. 1999;5002–5011.
44.
go back to reference Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell. 2005;121(3):335–48.PubMed Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell. 2005;121(3):335–48.PubMed
45.
go back to reference Wang L, Cao L, Wang H, Liu B, Zhang Q, Meng Z, et al. Cancer-associated fibroblasts enhance metastatic potential of lung cancer cells through IL-6/STAT3 signaling pathway. Oncotarget [Internet]. 2017;8(44):76116–76128. Available from: http://www.oncotarget.com/fulltext/18814 Wang L, Cao L, Wang H, Liu B, Zhang Q, Meng Z, et al. Cancer-associated fibroblasts enhance metastatic potential of lung cancer cells through IL-6/STAT3 signaling pathway. Oncotarget [Internet]. 2017;8(44):76116–76128. Available from: http://​www.​oncotarget.​com/​fulltext/​18814
47.
go back to reference Kashima H, Noma K, Ohara T, Kato T, Katsura Y, Komoto S, et al. Cancer-associated fibroblasts (CAFs) promote the lymph node metastasis of esophageal squamous cell carcinoma. Int J Cancer. 2018. Kashima H, Noma K, Ohara T, Kato T, Katsura Y, Komoto S, et al. Cancer-associated fibroblasts (CAFs) promote the lymph node metastasis of esophageal squamous cell carcinoma. Int J Cancer. 2018.
48.
go back to reference Cohen N, Shani O, Raz Y, Sharon Y, Hoffman D, Abramovitz L, et al. Fibroblasts drive an immunosuppressive and growth-promoting microenvironment in breast cancer via secretion of Chitinase 3-like 1. Oncogene. 2017. Cohen N, Shani O, Raz Y, Sharon Y, Hoffman D, Abramovitz L, et al. Fibroblasts drive an immunosuppressive and growth-promoting microenvironment in breast cancer via secretion of Chitinase 3-like 1. Oncogene. 2017.
49.
go back to reference Erez N, Glanz S, Raz Y, Avivi C, Barshack I. Cancer Associated Fibroblasts express pro-inflammatory factors in human breast and ovarian tumors. Biochem Biophys Res Commun. 2013. Erez N, Glanz S, Raz Y, Avivi C, Barshack I. Cancer Associated Fibroblasts express pro-inflammatory factors in human breast and ovarian tumors. Biochem Biophys Res Commun. 2013.
50.
go back to reference Balachander GM, Talukdar PM, Debnath M, Rangarajan A, Chatterjee K. Inflammatory Role of Cancer-Associated Fibroblasts in Invasive Breast Tumors Revealed Using a Fibrous Polymer Scaffold. ACS Appl Mater Interfaces. 2018; Balachander GM, Talukdar PM, Debnath M, Rangarajan A, Chatterjee K. Inflammatory Role of Cancer-Associated Fibroblasts in Invasive Breast Tumors Revealed Using a Fibrous Polymer Scaffold. ACS Appl Mater Interfaces. 2018;
51.
go back to reference Lim H, Moon A. Inflammatory fibroblasts in cancer. Arch Pharm Res. 2016. Lim H, Moon A. Inflammatory fibroblasts in cancer. Arch Pharm Res. 2016.
52.
go back to reference Attieh Y, Clark AG, Grass C, Richon S, Pocard M, Mariani P, et al. Cancer-associated fibroblasts lead tumor invasion through integrin-beta3-dependent fibronectin assembly. J Cell Biol. 2017;216(11):1–12. Attieh Y, Clark AG, Grass C, Richon S, Pocard M, Mariani P, et al. Cancer-associated fibroblasts lead tumor invasion through integrin-beta3-dependent fibronectin assembly. J Cell Biol. 2017;216(11):1–12.
54.
go back to reference Zanconato F, Cordenonsi M, Piccolo S. YAP/TAZ at the Roots of Cancer. Cancer Cell. 2016. Zanconato F, Cordenonsi M, Piccolo S. YAP/TAZ at the Roots of Cancer. Cancer Cell. 2016.
55.
go back to reference Calvo F, Ege N, Grande-Garcia A, Hooper S, Jenkins RP, Chaudhry SI, et al. Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer-associated fibroblasts. Nat Cell Biol. 2013. Calvo F, Ege N, Grande-Garcia A, Hooper S, Jenkins RP, Chaudhry SI, et al. Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer-associated fibroblasts. Nat Cell Biol. 2013.
56.
go back to reference Cadamuro M, Nardo G, Indraccolo S, Dall’Olmo L, Sambado L, Moserle L, et al. Platelet-derived growth factor-D and Rho GTPases regulate recruitment of cancer-associated fibroblasts in cholangiocarcinoma. Hepatology. 2013. Cadamuro M, Nardo G, Indraccolo S, Dall’Olmo L, Sambado L, Moserle L, et al. Platelet-derived growth factor-D and Rho GTPases regulate recruitment of cancer-associated fibroblasts in cholangiocarcinoma. Hepatology. 2013.
57.
go back to reference Ge J, Burnier L, Adamopoulou M, Kwa MQ, Schaks M, Rottner K, et al. RhoA, Rac1, and Cdc42 differentially regulate SMA and collagen i expression in mesenchymal stem cells. J Biol Chem. 2018. Ge J, Burnier L, Adamopoulou M, Kwa MQ, Schaks M, Rottner K, et al. RhoA, Rac1, and Cdc42 differentially regulate SMA and collagen i expression in mesenchymal stem cells. J Biol Chem. 2018.
59.
go back to reference Shiga K, Hara M, Nagasaki T, Sato T, Takahashi H, Takeyama H. Cancer-associated fibroblasts: their characteristics and their roles in tumor growth. Cancers (Basel) 2015;7(4):2443–2458. Shiga K, Hara M, Nagasaki T, Sato T, Takahashi H, Takeyama H. Cancer-associated fibroblasts: their characteristics and their roles in tumor growth. Cancers (Basel) 2015;7(4):2443–2458.
60.
go back to reference Heldin CH, Rubin K, Pietras K, Östman A. High interstitial fluid pressure - an obstacle in cancer therapy. Nat Rev Cancer. 2004;4(10):806–13.PubMed Heldin CH, Rubin K, Pietras K, Östman A. High interstitial fluid pressure - an obstacle in cancer therapy. Nat Rev Cancer. 2004;4(10):806–13.PubMed
61.
go back to reference Fang M, Yuan J, Peng C, Li Y. Collagen as a double-edged sword in tumor progression. Tumor Biol. 2014;35(4):2871–82. Fang M, Yuan J, Peng C, Li Y. Collagen as a double-edged sword in tumor progression. Tumor Biol. 2014;35(4):2871–82.
62.
go back to reference Rhim AD, Oberstein PE, Thomas DH, Mirek ET, Palermo CF, Sastra SA, et al. Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell. 2014;25(6):735–47.PubMedPubMedCentral Rhim AD, Oberstein PE, Thomas DH, Mirek ET, Palermo CF, Sastra SA, et al. Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell. 2014;25(6):735–47.PubMedPubMedCentral
63.
go back to reference Özdemir BC, Pentcheva-Hoang T, Carstens JL, Zheng X, Wu CC, Simpson TR, et al. Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell. 2014;25(6):719–34.PubMedPubMedCentral Özdemir BC, Pentcheva-Hoang T, Carstens JL, Zheng X, Wu CC, Simpson TR, et al. Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell. 2014;25(6):719–34.PubMedPubMedCentral
64.
go back to reference Froeling FEM, Kocher HM. Homeostatic restoration of desmoplastic stroma rather than its ablation slows pancreatic cancer progression. Gastroenterology. 2015 Apr;148(4):849–50.PubMed Froeling FEM, Kocher HM. Homeostatic restoration of desmoplastic stroma rather than its ablation slows pancreatic cancer progression. Gastroenterology. 2015 Apr;148(4):849–50.PubMed
65.
go back to reference Lo A, Wang L-CS, Scholler J, Monslow J, Avery D, Newick K, et al. Tumor-promoting Desmoplasia is disrupted by depleting FAP-expressing stromal cells. Cancer Res. 2018;75(14):2800–10. Lo A, Wang L-CS, Scholler J, Monslow J, Avery D, Newick K, et al. Tumor-promoting Desmoplasia is disrupted by depleting FAP-expressing stromal cells. Cancer Res. 2018;75(14):2800–10.
66.
go back to reference Surowiak P, Murawa D, Materna V, Maciejczyk A, Pudelko M, Ciesla S, et al. Occurence of stromal myofibroblasts in the invasive ductal breast cancer tissue is an unfavourable prognostic factor. Anticancer Res. 2007;27(4 C):2917–24.PubMed Surowiak P, Murawa D, Materna V, Maciejczyk A, Pudelko M, Ciesla S, et al. Occurence of stromal myofibroblasts in the invasive ductal breast cancer tissue is an unfavourable prognostic factor. Anticancer Res. 2007;27(4 C):2917–24.PubMed
67.
go back to reference Marsh D, Suchak K, Moutasim KA, Vallath S, Hopper C, Jerjes W, et al. Stromal features are predictive of disease mortality in oral cancer patients. J Pathol. 2011;223(4):470–81.PubMed Marsh D, Suchak K, Moutasim KA, Vallath S, Hopper C, Jerjes W, et al. Stromal features are predictive of disease mortality in oral cancer patients. J Pathol. 2011;223(4):470–81.PubMed
69.
go back to reference Tsujino T, Seshimo I, Yamamoto H, Chew YN, Ezumi K, Takemasa I, et al. Stromal myofibroblasts predict disease recurrence for colorectal cancer. Clin Cancer Res. 2007;13(7):2082–90.PubMed Tsujino T, Seshimo I, Yamamoto H, Chew YN, Ezumi K, Takemasa I, et al. Stromal myofibroblasts predict disease recurrence for colorectal cancer. Clin Cancer Res. 2007;13(7):2082–90.PubMed
70.
go back to reference Saadi A, Shannon NB, Lao-Sirieix P, O’Donovan M, Walker E, Clemons NJ, et al. Stromal genes discriminate preinvasive from invasive disease, predict outcome, and highlight inflammatory pathways in digestive cancers. Proc Natl Acad Sci [Internet] 2010;107(5):2177–2182. Available from: https://doi.org/10.1073/pnas.0909797107 Saadi A, Shannon NB, Lao-Sirieix P, O’Donovan M, Walker E, Clemons NJ, et al. Stromal genes discriminate preinvasive from invasive disease, predict outcome, and highlight inflammatory pathways in digestive cancers. Proc Natl Acad Sci [Internet] 2010;107(5):2177–2182. Available from: https://​doi.​org/​10.​1073/​pnas.​0909797107
71.
go back to reference Karsdal MA, Nielsen SH, Leeming DJ, Langholm LL, Nielsen MJ, Manon-Jensen T, et al. The good and the bad collagens of fibrosis – their role in signaling and organ function. Adv Drug Deliv Rev. 2017;121:43–56.PubMed Karsdal MA, Nielsen SH, Leeming DJ, Langholm LL, Nielsen MJ, Manon-Jensen T, et al. The good and the bad collagens of fibrosis – their role in signaling and organ function. Adv Drug Deliv Rev. 2017;121:43–56.PubMed
73.
go back to reference Chintala S, Sawaya R, Gokaslan Z, Rao J. The effect of type III collagen on migration and invasion of human. Cancer Lett. 1996;102:57–63.PubMed Chintala S, Sawaya R, Gokaslan Z, Rao J. The effect of type III collagen on migration and invasion of human. Cancer Lett. 1996;102:57–63.PubMed
74.
go back to reference Hirai K, Shimada H, Ogawa T, Taji S. The spread of human lung cancer cells on collagens and its inhibition by type III collagen. Clin Exp Metastasis. 1991;9:517–27.PubMed Hirai K, Shimada H, Ogawa T, Taji S. The spread of human lung cancer cells on collagens and its inhibition by type III collagen. Clin Exp Metastasis. 1991;9:517–27.PubMed
75.
go back to reference Kanematsu A, Marui A, Yamamoto S, Ozeki M, Hirano Y, Yamamoto M, et al. Type I collagen can function as a reservoir of basic fibroblast growth factor. J Control Release. 2004;99(2):281–92.PubMed Kanematsu A, Marui A, Yamamoto S, Ozeki M, Hirano Y, Yamamoto M, et al. Type I collagen can function as a reservoir of basic fibroblast growth factor. J Control Release. 2004;99(2):281–92.PubMed
76.
go back to reference Zhao H, Han K-LL, Wang Z-YY, Chen Y, Li H-TT, Zeng J-LL, et al. Value of C-telopeptide-cross-linked type I collagen, osteocalcin, bone-specific alkaline phosphatase and procollagen type I N-terminal propeptide in the diagnosis and prognosis of bone metastasis in patients with malignant tumors. Med Sci Monit [internet]. 2011;17(11):CR626-CR633. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22037741. Zhao H, Han K-LL, Wang Z-YY, Chen Y, Li H-TT, Zeng J-LL, et al. Value of C-telopeptide-cross-linked type I collagen, osteocalcin, bone-specific alkaline phosphatase and procollagen type I N-terminal propeptide in the diagnosis and prognosis of bone metastasis in patients with malignant tumors. Med Sci Monit [internet]. 2011;17(11):CR626-CR633. Available from: http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​22037741.
77.
go back to reference Cloos PAC, Fledelius C, Christgau S, Christiansen C, Engsig M. Delmas P, et al. Calcif Tissue Int: Investigation of bone disease using isomerized and racemized fragments of type I collagen; 2003. Cloos PAC, Fledelius C, Christgau S, Christiansen C, Engsig M. Delmas P, et al. Calcif Tissue Int: Investigation of bone disease using isomerized and racemized fragments of type I collagen; 2003.
78.
go back to reference Hall CL, Dai J, van Golen KL, Keller ET, Long MW. Type I collagen receptor (alpha 2 beta 1) signaling promotes the growth of human prostate cancer cells within the bone. Cancer Res. 2006. Hall CL, Dai J, van Golen KL, Keller ET, Long MW. Type I collagen receptor (alpha 2 beta 1) signaling promotes the growth of human prostate cancer cells within the bone. Cancer Res. 2006.
79.
go back to reference Ferreira AR, Alho I, Shan N, Matias M, Faria M, Casimiro S, et al. N-Telopeptide of type I collagen Long-term dynamics in breast Cancer patients with bone metastases: clinical outcomes and influence of Extraskeletal metastases. Oncologist [Internet] 2016;21(12):1418–1426. Available from: https://doi.org/10.1634/theoncologist.2015-0527 Ferreira AR, Alho I, Shan N, Matias M, Faria M, Casimiro S, et al. N-Telopeptide of type I collagen Long-term dynamics in breast Cancer patients with bone metastases: clinical outcomes and influence of Extraskeletal metastases. Oncologist [Internet] 2016;21(12):1418–1426. Available from: https://​doi.​org/​10.​1634/​theoncologist.​2015-0527
82.
go back to reference Menke A, Philippi C, Vogelmann R, Seidel B, Lutz MP, Adler G, et al. Down-regulation of E-cadherin gene expression by collagen type I and type III in pancreatic Cancer cell lines 1. Biochemistry. 2001:3508–17. Menke A, Philippi C, Vogelmann R, Seidel B, Lutz MP, Adler G, et al. Down-regulation of E-cadherin gene expression by collagen type I and type III in pancreatic Cancer cell lines 1. Biochemistry. 2001:3508–17.
83.
go back to reference Cheng JC, Leung PCK. Type I collagen down-regulates E-cadherin expression by increasing PI3KCA in cancer cells. Cancer Lett. 2011. Cheng JC, Leung PCK. Type I collagen down-regulates E-cadherin expression by increasing PI3KCA in cancer cells. Cancer Lett. 2011.
85.
go back to reference Barcus CE, O’Leary KA, Brockman JL, Rugowski DE, Liu Y, Garcia N, et al. Elevated collagen-I augments tumor progressive signals, intravasation and metastasis of prolactin-induced estrogen receptor alpha positive mammary tumor cells. Breast Cancer Res [Internet] 2017;19(1):1–13. Available from: https://doi.org/10.1186/s13058-017-0801-1 Barcus CE, O’Leary KA, Brockman JL, Rugowski DE, Liu Y, Garcia N, et al. Elevated collagen-I augments tumor progressive signals, intravasation and metastasis of prolactin-induced estrogen receptor alpha positive mammary tumor cells. Breast Cancer Res [Internet] 2017;19(1):1–13. Available from: https://​doi.​org/​10.​1186/​s13058-017-0801-1
86.
go back to reference Gelse K, Pöschl E, Aigner T. Collagens - structure, function, and biosynthesis. Adv Drug Deliv Rev. 2003. Gelse K, Pöschl E, Aigner T. Collagens - structure, function, and biosynthesis. Adv Drug Deliv Rev. 2003.
88.
go back to reference Hayashi S, Zhepeng W, Bryan J, Kobayashi C, Faccio R, Sandell L. The type II collagen N-propeptide, PIIBNP, inhibits cell survival and bone resorption of osteoclasts via integrin-mediated signaling. Bone. 2011;49(4):644–52.PubMedPubMedCentral Hayashi S, Zhepeng W, Bryan J, Kobayashi C, Faccio R, Sandell L. The type II collagen N-propeptide, PIIBNP, inhibits cell survival and bone resorption of osteoclasts via integrin-mediated signaling. Bone. 2011;49(4):644–52.PubMedPubMedCentral
89.
go back to reference Sipilä K, Haag S, Denessiouk K, Kap̈ylä J, Peters EC, Denesyuk A, et al. Citrullination of collagen II affects integrin-mediated cell adhesion in a receptor-specific manner. FASEB J. 2014; Sipilä K, Haag S, Denessiouk K, Kap̈ylä J, Peters EC, Denesyuk A, et al. Citrullination of collagen II affects integrin-mediated cell adhesion in a receptor-specific manner. FASEB J. 2014;
90.
go back to reference Wang Z, Bryan J, Franz C, Havlioglu N, Sandell LJ. Type IIB procollagen NH2-propeptide induces death of tumor cells via interaction with integrins αvβ3and αvβ5. J Biol Chem. 2010;285(27):20806–17.PubMedPubMedCentral Wang Z, Bryan J, Franz C, Havlioglu N, Sandell LJ. Type IIB procollagen NH2-propeptide induces death of tumor cells via interaction with integrins αvβ3and αvβ5. J Biol Chem. 2010;285(27):20806–17.PubMedPubMedCentral
91.
go back to reference Hilska M, Peltonen J, Gullichsen R, Paajanen H, Laato M. The Distribution of Collagen Types I , III , and IV in Normal and Malignant Colorectal Mucosa. 1998; Hilska M, Peltonen J, Gullichsen R, Paajanen H, Laato M. The Distribution of Collagen Types I , III , and IV in Normal and Malignant Colorectal Mucosa. 1998;
93.
go back to reference Basso D, Belluco C, Mazza S, Greco E. Colorectal cancer metastatic phenotype stimulates production by fibroblasts of N-terminal peptide of type III collagen : clinical implications for prognosis. 2001; Basso D, Belluco C, Mazza S, Greco E. Colorectal cancer metastatic phenotype stimulates production by fibroblasts of N-terminal peptide of type III collagen : clinical implications for prognosis. 2001;
94.
go back to reference Jensen C, Madsen D, Hansen M, Schmidt H, Svane I, Karsdal M, et al. Altered type III collagen turnover measured in pre-treatment serum predicts outcome in metastatic melanoma patients treated with Ipilimumab. Eur J Cancer. 2018;92. Jensen C, Madsen D, Hansen M, Schmidt H, Svane I, Karsdal M, et al. Altered type III collagen turnover measured in pre-treatment serum predicts outcome in metastatic melanoma patients treated with Ipilimumab. Eur J Cancer. 2018;92.
95.
go back to reference Fichard A, Kleman JP, Ruggiero F. Another look at collagen V and XI molecules. Matrix Biology. 1995. Fichard A, Kleman JP, Ruggiero F. Another look at collagen V and XI molecules. Matrix Biology. 1995.
100.
go back to reference Schnoor M, Cullen P, Lorkowski J, Stolle K, Robenek H, Troyer D, et al. Production of type VI collagen by human macrophages: a new dimension in macrophage functional heterogeneity. J Immunol. 2008. Schnoor M, Cullen P, Lorkowski J, Stolle K, Robenek H, Troyer D, et al. Production of type VI collagen by human macrophages: a new dimension in macrophage functional heterogeneity. J Immunol. 2008.
101.
go back to reference Wright A, Li Y-H, Zhu C, Woodruff W, Coulter H. The differential effect of endothelial cell factors on in vitro motility of malignant and non-malignant cells. Ann Biomed Eng. 2008;36(6):958–69.PubMedPubMedCentral Wright A, Li Y-H, Zhu C, Woodruff W, Coulter H. The differential effect of endothelial cell factors on in vitro motility of malignant and non-malignant cells. Ann Biomed Eng. 2008;36(6):958–69.PubMedPubMedCentral
102.
go back to reference Han J. Daniel JC. Connect Tissue Res: Biosynthesis of type VI collagen by glioblastoma cells and possible function in cell invasion of three-dimensional matrices; 1995. Han J. Daniel JC. Connect Tissue Res: Biosynthesis of type VI collagen by glioblastoma cells and possible function in cell invasion of three-dimensional matrices; 1995.
103.
go back to reference Sherman-Baust CA, Weeraratna AT, Rangel LBA, Pizer ES, Cho KR, Schwartz DR, et al. Remodeling of the extracellular matrix through overexpression of collagen VI contributes to cisplatin resistance in ovarian cancer cells. Cancer Cell. 2003;3(4):377–86. Sherman-Baust CA, Weeraratna AT, Rangel LBA, Pizer ES, Cho KR, Schwartz DR, et al. Remodeling of the extracellular matrix through overexpression of collagen VI contributes to cisplatin resistance in ovarian cancer cells. Cancer Cell. 2003;3(4):377–86.
104.
go back to reference Varma RR, Hector SM, Clark K, Greco WR, Hawthorn L, Pendyala L. Gene expression profiling of a clonal isolate of oxaliplatin-resistant ovarian carcinoma cell line A2780/C10. Oncol Rep. 2005. Varma RR, Hector SM, Clark K, Greco WR, Hawthorn L, Pendyala L. Gene expression profiling of a clonal isolate of oxaliplatin-resistant ovarian carcinoma cell line A2780/C10. Oncol Rep. 2005.
105.
go back to reference Park J, Morley TS, Scherer PE. Inhibition of endotrophin, a cleavage product of collagen VI, confers cisplatin sensitivity to tumours. EMBO Mol Med. 2013;5(6):935–48.PubMedPubMedCentral Park J, Morley TS, Scherer PE. Inhibition of endotrophin, a cleavage product of collagen VI, confers cisplatin sensitivity to tumours. EMBO Mol Med. 2013;5(6):935–48.PubMedPubMedCentral
106.
go back to reference Iyengar P, Espina V, Williams TW, Lin Y, Berry D, Jelicks LA, et al. Adipocyte-derived collagen VI affects early mammary tumor progression in vivo, demonstrating a critical interaction in the tumor/stroma microenvironment. J Clin Invest. 2005;115(5):1163–76.PubMedPubMedCentral Iyengar P, Espina V, Williams TW, Lin Y, Berry D, Jelicks LA, et al. Adipocyte-derived collagen VI affects early mammary tumor progression in vivo, demonstrating a critical interaction in the tumor/stroma microenvironment. J Clin Invest. 2005;115(5):1163–76.PubMedPubMedCentral
107.
108.
go back to reference Ellsworth RE, Seebach J, Field L a, Heckman C, Kane J, Hooke J a, et al. A gene expression signature that defines breast cancer metastases. Clin Exp Metastasis. 2009; Ellsworth RE, Seebach J, Field L a, Heckman C, Kane J, Hooke J a, et al. A gene expression signature that defines breast cancer metastases. Clin Exp Metastasis. 2009;
109.
go back to reference Zhao Y, Zhou T, Li A, Yao H, He F, Wang L, et al. A potential role of collagens expression in distinguishing between premalignant and malignant lesions in stomach. Anat Rec. 2009. Zhao Y, Zhou T, Li A, Yao H, He F, Wang L, et al. A potential role of collagens expression in distinguishing between premalignant and malignant lesions in stomach. Anat Rec. 2009.
110.
go back to reference García-Pravia C, Galván JA, Gutiérrez-Corral N, Solar-García L, García-Pérez E, García-Ocaña M, et al. Overexpression of COL11A1 by Cancer-associated fibroblasts: clinical relevance of a stromal marker in pancreatic Cancer. PLoS One. 2013;8(10):1–13. García-Pravia C, Galván JA, Gutiérrez-Corral N, Solar-García L, García-Pérez E, García-Ocaña M, et al. Overexpression of COL11A1 by Cancer-associated fibroblasts: clinical relevance of a stromal marker in pancreatic Cancer. PLoS One. 2013;8(10):1–13.
111.
go back to reference Chong IW, Chang MY, Chang HC, Yu YP, Sheu CC, Tsai JR, et al. Great potential of a panel of multiple hMTH1, SPD, ITGA11 and COL11A1 markers for diagnosis of patients with non-small cell lung cancer. Oncol Rep. 2006. Chong IW, Chang MY, Chang HC, Yu YP, Sheu CC, Tsai JR, et al. Great potential of a panel of multiple hMTH1, SPD, ITGA11 and COL11A1 markers for diagnosis of patients with non-small cell lung cancer. Oncol Rep. 2006.
112.
go back to reference Fischer H. Colorectal carcinogenesis is associated with stromal expression of COL11A1 and COL5A2. Carcinogenesis. 2001. Fischer H. Colorectal carcinogenesis is associated with stromal expression of COL11A1 and COL5A2. Carcinogenesis. 2001.
113.
go back to reference Vecchi M, Nuciforo P, Romagnoli S, Confalonieri S, Pellegrini C, Serio G, et al. Gene expression analysis of early and advanced gastric cancers. Oncogene. 2007. Vecchi M, Nuciforo P, Romagnoli S, Confalonieri S, Pellegrini C, Serio G, et al. Gene expression analysis of early and advanced gastric cancers. Oncogene. 2007.
114.
go back to reference Badea L, Herlea V, Dima SO, Dumitrascu T, Popescu I. Combined gene expression analysis of whole-tissue and microdissected pancreatic ductal adenocarcinoma identifies genes specifically overexpressed in tumor epithelia. Hepatogastroenterology. 2008. Badea L, Herlea V, Dima SO, Dumitrascu T, Popescu I. Combined gene expression analysis of whole-tissue and microdissected pancreatic ductal adenocarcinoma identifies genes specifically overexpressed in tumor epithelia. Hepatogastroenterology. 2008.
115.
go back to reference Wu Y-H, Chang T-H, Huang Y-F, Huang H-D, Chou C-Y. COL11A1 promotes tumor progression and predicts poor clinical outcome in ovarian cancer. Oncogene. 2013. Wu Y-H, Chang T-H, Huang Y-F, Huang H-D, Chou C-Y. COL11A1 promotes tumor progression and predicts poor clinical outcome in ovarian cancer. Oncogene. 2013.
116.
go back to reference Kim H, Watkinson J, Varadan V, Anastassiou D. Multi-cancer computational analysis reveals invasion-associated variant of desmoplastic reaction involving INHBA, THBS2 and COL11A1. BMC Med Genet. 2010. Kim H, Watkinson J, Varadan V, Anastassiou D. Multi-cancer computational analysis reveals invasion-associated variant of desmoplastic reaction involving INHBA, THBS2 and COL11A1. BMC Med Genet. 2010.
117.
go back to reference Teng PN, Wang G, Hood BL, Conrads KA, Hamilton CA, Maxwell GL, et al. Identification of candidate circulating cisplatin-resistant biomarkers from epithelial ovarian carcinoma cell secretomes. Br J Cancer. 2014. Teng PN, Wang G, Hood BL, Conrads KA, Hamilton CA, Maxwell GL, et al. Identification of candidate circulating cisplatin-resistant biomarkers from epithelial ovarian carcinoma cell secretomes. Br J Cancer. 2014.
118.
go back to reference Navab R, Strumpf D, Bandarchi B, Zhu C, Pintilie M, Rohan V. Prognostic gene-expression signature of carcinoma- associated fi broblasts in non-small cell lung cancer. Proc Natl Acad Sci U S A. 2011;108(april 26th):7160–5. Navab R, Strumpf D, Bandarchi B, Zhu C, Pintilie M, Rohan V. Prognostic gene-expression signature of carcinoma- associated fi broblasts in non-small cell lung cancer. Proc Natl Acad Sci U S A. 2011;108(april 26th):7160–5.
119.
go back to reference Cheon DJ, Tong Y, Sim MS, Dering J, Berel D, Cui X, et al. A collagen-remodeling gene signature regulated by TGF-β signaling is associated with metastasis and poor survival in serous ovarian cancer. Clin Cancer Res. 2014. Cheon DJ, Tong Y, Sim MS, Dering J, Berel D, Cui X, et al. A collagen-remodeling gene signature regulated by TGF-β signaling is associated with metastasis and poor survival in serous ovarian cancer. Clin Cancer Res. 2014.
120.
go back to reference Ricard-Blum S, Ruggiero F. The collagen superfamily: from the extracellular matrix to the cell membrane. Pathol Biol. 2005;53(7):430–42.PubMed Ricard-Blum S, Ruggiero F. The collagen superfamily: from the extracellular matrix to the cell membrane. Pathol Biol. 2005;53(7):430–42.PubMed
121.
go back to reference Koch M, Laub F, Zhou P, Hahn RA, Tanaka S, Burgeson RE, et al. Collagen XXIV , a Vertebrate Fibrillar Collagen with Structural Features of Invertebrate Collagens. J Biol Chem 2003;278(44):43236–44. Koch M, Laub F, Zhou P, Hahn RA, Tanaka S, Burgeson RE, et al. Collagen XXIV , a Vertebrate Fibrillar Collagen with Structural Features of Invertebrate Collagens. J Biol Chem 2003;278(44):43236–44.
122.
go back to reference Wang W, Olson D, Liang G, Franceschi RT, Li C, Wang B, et al. Collagen XXIV (Col24α1) promotes osteoblastic differentiation and mineralization.Pdf. Int J Biol Sci. 2012;8(10):1310–22.PubMedPubMedCentral Wang W, Olson D, Liang G, Franceschi RT, Li C, Wang B, et al. Collagen XXIV (Col24α1) promotes osteoblastic differentiation and mineralization.Pdf. Int J Biol Sci. 2012;8(10):1310–22.PubMedPubMedCentral
123.
go back to reference Misawa K, Kabazawa T, Imai A, Endo S, Mochizuki D. Fukushima Hi, et al. Mol Clin Oncol: Prognostic value of type XXII and XXIV collagen mRNA expression in head and neck cancer patients; 2014. Misawa K, Kabazawa T, Imai A, Endo S, Mochizuki D. Fukushima Hi, et al. Mol Clin Oncol: Prognostic value of type XXII and XXIV collagen mRNA expression in head and neck cancer patients; 2014.
124.
go back to reference Pace JM, Corrado M, Missero C, Byers PH. Identification, characterization and expression analysis of a new fibrillar collagen gene, COL27A1. Matrix Biol. 2003. Pace JM, Corrado M, Missero C, Byers PH. Identification, characterization and expression analysis of a new fibrillar collagen gene, COL27A1. Matrix Biol. 2003.
125.
go back to reference Plumb DA, Dhir V, Mironov A, Ferrara L, Poulsom R, Kadler KE, et al. Collagen XXVII is developmentally regulated and forms thin fibrillar structures distinct from those of classical vertebrate fibrillar collagens. J Biol Chem. 2007. Plumb DA, Dhir V, Mironov A, Ferrara L, Poulsom R, Kadler KE, et al. Collagen XXVII is developmentally regulated and forms thin fibrillar structures distinct from those of classical vertebrate fibrillar collagens. J Biol Chem. 2007.
126.
go back to reference Hjorten R, Hansen U, Underwood RA, Telfer HE, Fernandes RJ, Krakow D, et al. Type XXVII collagen at the transition of cartilage to bone during skeletogenesis. Bone. 2007. Hjorten R, Hansen U, Underwood RA, Telfer HE, Fernandes RJ, Krakow D, et al. Type XXVII collagen at the transition of cartilage to bone during skeletogenesis. Bone. 2007.
131.
go back to reference Wang S, Willumsen N, Cecilie B, Karsdal M, Chondros D, Taverna D. Extracellular matrix (ECM) circulating peptide biomarkers as potential predictors of survival in patients (pts) with untreated metastatic pancreatic ductal adenocarcinoma (mPDA) receiving pegvorhyaluronidase alfa (PEGPH20), nab-paclitaxel (a), and gemcita. J Clin Oncol. 2018;36(15):–12030. Wang S, Willumsen N, Cecilie B, Karsdal M, Chondros D, Taverna D. Extracellular matrix (ECM) circulating peptide biomarkers as potential predictors of survival in patients (pts) with untreated metastatic pancreatic ductal adenocarcinoma (mPDA) receiving pegvorhyaluronidase alfa (PEGPH20), nab-paclitaxel (a), and gemcita. J Clin Oncol. 2018;36(15):–12030.
132.
go back to reference Burchardt ER, Hein R, Bosserhoff AK. Laminin, hyaluronan, tenascin-C and type VI collagen levels in sera from patients with malignant melanoma. Clin Exp Dermatol. 2003. Burchardt ER, Hein R, Bosserhoff AK. Laminin, hyaluronan, tenascin-C and type VI collagen levels in sera from patients with malignant melanoma. Clin Exp Dermatol. 2003.
133.
go back to reference Kang CY, Wang J, Axell-House D, Soni P, Chu M-L, Chipitsyna G, et al. Clinical significance of serum COL6A3 in pancreatic ductal adenocarcinoma. J Gastrointest Surg. 2014. Kang CY, Wang J, Axell-House D, Soni P, Chu M-L, Chipitsyna G, et al. Clinical significance of serum COL6A3 in pancreatic ductal adenocarcinoma. J Gastrointest Surg. 2014.
134.
go back to reference Bierie B, Moses HL. TGFβ the molecular Jekyll and Hyde.Pdf. Nat Rev Cancer. 2006;6. Bierie B, Moses HL. TGFβ the molecular Jekyll and Hyde.Pdf. Nat Rev Cancer. 2006;6.
135.
go back to reference Borthwicka LA, Wynnb TA, Fishera AJ. Cytokine mediated tissue fibrosis. Biochim Biophys Acta. 2013;1832(7):1049–60. Borthwicka LA, Wynnb TA, Fishera AJ. Cytokine mediated tissue fibrosis. Biochim Biophys Acta. 2013;1832(7):1049–60.
136.
go back to reference Mariathasan S, Turley S, Nickles D, Castiglioni A, Yuen K, Wang Y, et al. TGFβ attenuates tumour response to PD-L1 blockade by contributing to exclusion of T cells. Nature. 2018;22(554):544–8. Mariathasan S, Turley S, Nickles D, Castiglioni A, Yuen K, Wang Y, et al. TGFβ attenuates tumour response to PD-L1 blockade by contributing to exclusion of T cells. Nature. 2018;22(554):544–8.
Metadata
Title
Collagens and Cancer associated fibroblasts in the reactive stroma and its relation to Cancer biology
Authors
Neel I. Nissen
Morten Karsdal
Nicholas Willumsen
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Biomarkers
Published in
Journal of Experimental & Clinical Cancer Research / Issue 1/2019
Electronic ISSN: 1756-9966
DOI
https://doi.org/10.1186/s13046-019-1110-6

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