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Published in: Molecular Cancer 1/2017

Open Access 01-12-2017 | Review

Factors involved in cancer metastasis: a better understanding to “seed and soil” hypothesis

Authors: Qiang Liu, Hongfei Zhang, Xiaoli Jiang, Caiyun Qian, Zhuoqi Liu, Daya Luo

Published in: Molecular Cancer | Issue 1/2017

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Abstract

Metastasis has intrigued researchers for more than 100 years. Despite the development of technologies and therapeutic strategies, metastasis is still the major cause of cancer-related death until today. The famous “seed and soil” hypothesis is widely cited and accepted, and it still provides significant instructions in cancer research until today. To our knowledge, there are few reviews that comprehensively and correlatively focus on both the seed and soil factors involved in cancer metastasis; moreover, despite the fact that increasingly underlying mechanisms and concepts have been defined recently, previous perspectives are appealing but may be limited. Hence, we reviewed factors involved in cancer metastasis, including both seed and soil factors. By integrating new concepts with the classic hypothesis, we aim to provide a comprehensive understanding of the “seed and soil” hypothesis and to conceptualize the framework for understanding factors involved in cancer metastasis. Based on a dynamic overview of this field, we also discuss potential implications for future research and clinical therapeutic strategies.
Literature
1.
go back to reference Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA: a cancer journal for clinicians. 2016;66(1):7–30. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA: a cancer journal for clinicians. 2016;66(1):7–30.
4.
go back to reference Paget S. The distribution of secondary growths in cancer of the breast. The Lancet. 1889;133(3421):571–3.CrossRef Paget S. The distribution of secondary growths in cancer of the breast. The Lancet. 1889;133(3421):571–3.CrossRef
5.
go back to reference Fidler IJ, Poste G. The “seed and soil” hypothesis revisited. The Lancet Oncology. 2008;9(8):808.PubMedCrossRef Fidler IJ, Poste G. The “seed and soil” hypothesis revisited. The Lancet Oncology. 2008;9(8):808.PubMedCrossRef
6.
go back to reference Ewing J. Metastasis, neoplastic disease: a treatise on tumors. London: Philadelphia and London; 1928. Ewing J. Metastasis, neoplastic disease: a treatise on tumors. London: Philadelphia and London; 1928.
7.
go back to reference Kim MY, Oskarsson T, Acharyya S, Nguyen DX, Zhang XH, Norton L, Massague J. Tumor self-seeding by circulating cancer cells. Cell. 2009;139(7):1315–26.PubMedPubMedCentralCrossRef Kim MY, Oskarsson T, Acharyya S, Nguyen DX, Zhang XH, Norton L, Massague J. Tumor self-seeding by circulating cancer cells. Cell. 2009;139(7):1315–26.PubMedPubMedCentralCrossRef
8.
go back to reference Comen E, Norton L, Massague J. Clinical implications of cancer self-seeding. Nat Rev. Clin Oncol. 2011;8(6):369–77.PubMed Comen E, Norton L, Massague J. Clinical implications of cancer self-seeding. Nat Rev. Clin Oncol. 2011;8(6):369–77.PubMed
10.
go back to reference Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004;117(7):927–39.PubMedCrossRef Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004;117(7):927–39.PubMedCrossRef
11.
go back to reference Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, Isakoff SJ, Ciciliano JC, Wells MN, Shah AM, et al. Circulating Breast Tumor Cells Exhibit Dynamic Changes in Epithelial and Mesenchymal Composition. Science. 2013;339(6119):580–4.PubMedPubMedCentralCrossRef Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, Isakoff SJ, Ciciliano JC, Wells MN, Shah AM, et al. Circulating Breast Tumor Cells Exhibit Dynamic Changes in Epithelial and Mesenchymal Composition. Science. 2013;339(6119):580–4.PubMedPubMedCentralCrossRef
12.
go back to reference Chaffer CL, Thompson EW, Williams ED. Mesenchymal to epithelial transition in development and disease. Cells Tissues Organs. 2007;185(1–3):7–19.PubMedCrossRef Chaffer CL, Thompson EW, Williams ED. Mesenchymal to epithelial transition in development and disease. Cells Tissues Organs. 2007;185(1–3):7–19.PubMedCrossRef
13.
go back to reference Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer. 2002;2(6):442–54.PubMedCrossRef Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer. 2002;2(6):442–54.PubMedCrossRef
14.
go back to reference Chaffer CL, Brennan JP, Slavin JL, Blick T, Thompson EW, Williams ED. Mesenchymal-to-epithelial transition facilitates bladder cancer metastasis: role of fibroblast growth factor receptor-2. Cancer Res. 2006;66(23):11,271–8.CrossRef Chaffer CL, Brennan JP, Slavin JL, Blick T, Thompson EW, Williams ED. Mesenchymal-to-epithelial transition facilitates bladder cancer metastasis: role of fibroblast growth factor receptor-2. Cancer Res. 2006;66(23):11,271–8.CrossRef
15.
go back to reference Tsai JH, Donaher JL, Murphy DA, Chau S, Yang J. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer cell. 2012;22(6):725–36.PubMedPubMedCentralCrossRef Tsai JH, Donaher JL, Murphy DA, Chau S, Yang J. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer cell. 2012;22(6):725–36.PubMedPubMedCentralCrossRef
16.
go back to reference Ocana OH, Corcoles R, Fabra A, Moreno-Bueno G, Acloque H, Vega S, Barrallo-Gimeno A, Cano A, Nieto MA. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer cell. 2012;22(6):709–24.PubMedCrossRef Ocana OH, Corcoles R, Fabra A, Moreno-Bueno G, Acloque H, Vega S, Barrallo-Gimeno A, Cano A, Nieto MA. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer cell. 2012;22(6):709–24.PubMedCrossRef
17.
go back to reference Zheng X, Carstens JL, Kim J, Scheible M, Kaye J, Sugimoto H, Wu CC, LeBleu VS, Kalluri R. Epithelial-to-mesenchymal transition is dispensable for metastasis but induces chemoresistance in pancreatic cancer. Nature. 2015;527(7579):525–30.PubMedPubMedCentralCrossRef Zheng X, Carstens JL, Kim J, Scheible M, Kaye J, Sugimoto H, Wu CC, LeBleu VS, Kalluri R. Epithelial-to-mesenchymal transition is dispensable for metastasis but induces chemoresistance in pancreatic cancer. Nature. 2015;527(7579):525–30.PubMedPubMedCentralCrossRef
18.
go back to reference Fischer KR, Durrans A, Lee S, Sheng J, Li F, Wong ST, Choi H, El Rayes T, Ryu S, Troeger J, et al. Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance. Nature. 2015;527(7579):472–6.PubMedPubMedCentralCrossRef Fischer KR, Durrans A, Lee S, Sheng J, Li F, Wong ST, Choi H, El Rayes T, Ryu S, Troeger J, et al. Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance. Nature. 2015;527(7579):472–6.PubMedPubMedCentralCrossRef
20.
go back to reference Ye X, Brabletz T, Kang Y, Longmore GD, Nieto MA, Stanger BZ, Yang J, Weinberg RA. Upholding a role for EMT in breast cancer metastasis. Nature. 2017;547(7661):E1–3.PubMedCrossRef Ye X, Brabletz T, Kang Y, Longmore GD, Nieto MA, Stanger BZ, Yang J, Weinberg RA. Upholding a role for EMT in breast cancer metastasis. Nature. 2017;547(7661):E1–3.PubMedCrossRef
21.
go back to reference Aiello NM, Brabletz T, Kang Y, Nieto MA, Weinberg RA, Stanger BZ. Upholding a role for EMT in pancreatic cancer metastasis. Nature. 2017;547(7661):E7–8.PubMedCrossRef Aiello NM, Brabletz T, Kang Y, Nieto MA, Weinberg RA, Stanger BZ. Upholding a role for EMT in pancreatic cancer metastasis. Nature. 2017;547(7661):E7–8.PubMedCrossRef
22.
go back to reference Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer. 2008;8(10):755–68.PubMedCrossRef Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer. 2008;8(10):755–68.PubMedCrossRef
23.
go back to reference Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, Visvader J, Weissman IL, Wahl GM. Cancer stem cells--perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 2006;66(19):9339–44.PubMedCrossRef Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, Visvader J, Weissman IL, Wahl GM. Cancer stem cells--perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 2006;66(19):9339–44.PubMedCrossRef
24.
go back to reference Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M, Danenberg E, Clarke AR, Sansom OJ, Clevers H. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature. 2009;457(7229):608–11.PubMedCrossRef Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M, Danenberg E, Clarke AR, Sansom OJ, Clevers H. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature. 2009;457(7229):608–11.PubMedCrossRef
25.
go back to reference Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003;100(7):3983–8.PubMedPubMedCentralCrossRef Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003;100(7):3983–8.PubMedPubMedCentralCrossRef
26.
go back to reference Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA, Dick JE. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367(6464):645.PubMedCrossRef Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA, Dick JE. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367(6464):645.PubMedCrossRef
27.
go back to reference Malanchi I, Santamaria-Martinez A, Susanto E, Peng H, Lehr HA, Delaloye JF, Huelsken J. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature. 2012;481(7379):85–9.CrossRef Malanchi I, Santamaria-Martinez A, Susanto E, Peng H, Lehr HA, Delaloye JF, Huelsken J. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature. 2012;481(7379):85–9.CrossRef
28.
go back to reference Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Migrating cancer stem cells—an integrated concept of malignant tumour progression. Nat Rev Cancer. 2005;5(9):744–9.PubMedCrossRef Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Migrating cancer stem cells—an integrated concept of malignant tumour progression. Nat Rev Cancer. 2005;5(9):744–9.PubMedCrossRef
29.
go back to reference Wilson RJ, Thomas CD, Fox R, Roy DB, Kunin WE. Spatial patterns in species distributions reveal biodiversity change. Nature. 2004;432(7015):393–6.PubMedCrossRef Wilson RJ, Thomas CD, Fox R, Roy DB, Kunin WE. Spatial patterns in species distributions reveal biodiversity change. Nature. 2004;432(7015):393–6.PubMedCrossRef
30.
go back to reference Okuda H, Kobayashi A, Xia B, Watabe M, Pai SK, Hirota S, Xing F, Liu W, Pandey PR, Fukuda K, et al. Hyaluronan synthase HAS2 promotes tumor progression in bone by stimulating the interaction of breast cancer stem-like cells with macrophages and stromal cells. Cancer Res. 2012;72(2):537–47.PubMedCrossRef Okuda H, Kobayashi A, Xia B, Watabe M, Pai SK, Hirota S, Xing F, Liu W, Pandey PR, Fukuda K, et al. Hyaluronan synthase HAS2 promotes tumor progression in bone by stimulating the interaction of breast cancer stem-like cells with macrophages and stromal cells. Cancer Res. 2012;72(2):537–47.PubMedCrossRef
31.
go back to reference Morel AP, Lievre M, Thomas C, Hinkal G, Ansieau S, Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PloS one. 2008;3(8):e2888.PubMedPubMedCentralCrossRef Morel AP, Lievre M, Thomas C, Hinkal G, Ansieau S, Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PloS one. 2008;3(8):e2888.PubMedPubMedCentralCrossRef
32.
33.
go back to reference Kenific CM, Thorburn A, Debnath J. Autophagy and metastasis: another double-edged sword. Curr Opin Cell Biol. 2010;22(2):241–5.PubMedCrossRef Kenific CM, Thorburn A, Debnath J. Autophagy and metastasis: another double-edged sword. Curr Opin Cell Biol. 2010;22(2):241–5.PubMedCrossRef
34.
go back to reference Chen S, Han Q, Wang X, Yang M, Zhang Z, Li P, Chen A, Hu C, Li S. IBP-mediated suppression of autophagy promotes growth and metastasis of breast cancer cells via activating mTORC2/Akt/FOXO3a signaling pathway. Cell Death Dis. 2013;4:e842.PubMedPubMedCentralCrossRef Chen S, Han Q, Wang X, Yang M, Zhang Z, Li P, Chen A, Hu C, Li S. IBP-mediated suppression of autophagy promotes growth and metastasis of breast cancer cells via activating mTORC2/Akt/FOXO3a signaling pathway. Cell Death Dis. 2013;4:e842.PubMedPubMedCentralCrossRef
35.
go back to reference Singh BN, Kumar D, Shankar S, Srivastava RK. Rottlerin induces autophagy which leads to apoptotic cell death through inhibition of PI3K/Akt/mTOR pathway in human pancreatic cancer stem cells. Biochem Pharmacol. 2012;84(9):1154–63.PubMedCrossRef Singh BN, Kumar D, Shankar S, Srivastava RK. Rottlerin induces autophagy which leads to apoptotic cell death through inhibition of PI3K/Akt/mTOR pathway in human pancreatic cancer stem cells. Biochem Pharmacol. 2012;84(9):1154–63.PubMedCrossRef
36.
go back to reference Saiki S, Sasazawa Y, Imamichi Y, Kawajiri S, Fujimaki T, Tanida I, Kobayashi H, Sato F, Sato S, Ishikawa K-I, et al. Caffeine induces apoptosis by enhancement of autophagy via PI3K/Akt/mTOR/p70S6K inhibition. Autophagy. 2014;7(2):176–87.CrossRef Saiki S, Sasazawa Y, Imamichi Y, Kawajiri S, Fujimaki T, Tanida I, Kobayashi H, Sato F, Sato S, Ishikawa K-I, et al. Caffeine induces apoptosis by enhancement of autophagy via PI3K/Akt/mTOR/p70S6K inhibition. Autophagy. 2014;7(2):176–87.CrossRef
37.
go back to reference Lock R, Kenific CM, Leidal AM, Salas E, Debnath J. Autophagy-Dependent Production of Secreted Factors Facilitates Oncogenic RAS-Driven Invasion. Cancer Discov. 2014;4(4):466–79.PubMedPubMedCentralCrossRef Lock R, Kenific CM, Leidal AM, Salas E, Debnath J. Autophagy-Dependent Production of Secreted Factors Facilitates Oncogenic RAS-Driven Invasion. Cancer Discov. 2014;4(4):466–79.PubMedPubMedCentralCrossRef
38.
go back to reference Peng Y-F, Shi Y-H, Ding Z-B, Ke A-W, Gu C-Y, Hui B, Zhou J, Qiu S-J, Dai Z, Fan J. Autophagy inhibition suppresses pulmonary metastasis of HCC in mice via impairing anoikis resistance and colonization of HCC cells. Autophagy. 2014;9(12):2056–68.CrossRef Peng Y-F, Shi Y-H, Ding Z-B, Ke A-W, Gu C-Y, Hui B, Zhou J, Qiu S-J, Dai Z, Fan J. Autophagy inhibition suppresses pulmonary metastasis of HCC in mice via impairing anoikis resistance and colonization of HCC cells. Autophagy. 2014;9(12):2056–68.CrossRef
39.
go back to reference Gong C, Bauvy C, Tonelli G, Yue W, Delomenie C, Nicolas V, Zhu Y, Domergue V, Marin-Esteban V, Tharinger H, et al. Beclin 1 and autophagy are required for the tumorigenicity of breast cancer stem-like/progenitor cells. Oncogene. 2013;32(18):2261–72. 2272e 2261–2211PubMedCrossRef Gong C, Bauvy C, Tonelli G, Yue W, Delomenie C, Nicolas V, Zhu Y, Domergue V, Marin-Esteban V, Tharinger H, et al. Beclin 1 and autophagy are required for the tumorigenicity of breast cancer stem-like/progenitor cells. Oncogene. 2013;32(18):2261–72. 2272e 2261–2211PubMedCrossRef
40.
go back to reference Bellodi C, Lidonnici MR, Hamilton A, Helgason GV, Soliera AR, Ronchetti M, Galavotti S, Young KW, Selmi T, Yacobi R, et al. Targeting autophagy potentiates tyrosine kinase inhibitor-induced cell death in Philadelphia chromosome-positive cells, including primary CML stem cells. J Clin Invest. 2009;119(5):1109–23.PubMedPubMedCentralCrossRef Bellodi C, Lidonnici MR, Hamilton A, Helgason GV, Soliera AR, Ronchetti M, Galavotti S, Young KW, Selmi T, Yacobi R, et al. Targeting autophagy potentiates tyrosine kinase inhibitor-induced cell death in Philadelphia chromosome-positive cells, including primary CML stem cells. J Clin Invest. 2009;119(5):1109–23.PubMedPubMedCentralCrossRef
41.
go back to reference Zhu H, Wang D, Liu Y, Su Z, Zhang L, Chen F, Zhou Y, Wu Y, Yu M, Zhang Z. Role of the Hypoxia-inducible factor-1 alpha induced autophagy in the conversion of non-stem pancreatic cancer cells into CD133+ pancreatic cancer stem-like cells. Cancer Cell Int. 2013;13(1):119.PubMedPubMedCentralCrossRef Zhu H, Wang D, Liu Y, Su Z, Zhang L, Chen F, Zhou Y, Wu Y, Yu M, Zhang Z. Role of the Hypoxia-inducible factor-1 alpha induced autophagy in the conversion of non-stem pancreatic cancer cells into CD133+ pancreatic cancer stem-like cells. Cancer Cell Int. 2013;13(1):119.PubMedPubMedCentralCrossRef
42.
go back to reference Li J, Yang B, Zhou Q, Wu Y, Shang D, Guo Y, Song Z, Zheng Q, Xiong J. Autophagy promotes hepatocellular carcinoma cell invasion through activation of epithelial-mesenchymal transition. Carcinogenesis. 2013;34(6):1343–51.PubMedCrossRef Li J, Yang B, Zhou Q, Wu Y, Shang D, Guo Y, Song Z, Zheng Q, Xiong J. Autophagy promotes hepatocellular carcinoma cell invasion through activation of epithelial-mesenchymal transition. Carcinogenesis. 2013;34(6):1343–51.PubMedCrossRef
43.
go back to reference Zhu H, Wang D, Zhang L, Xie X, Wu Y, Liu Y, Shao G, Su Z. Upregulation of autophagy by hypoxia-inducible factor-1alpha promotes EMT and metastatic ability of CD133+ pancreatic cancer stem-like cells during intermittent hypoxia. Oncol Rep. 2014;32(3):935–42.PubMedCrossRef Zhu H, Wang D, Zhang L, Xie X, Wu Y, Liu Y, Shao G, Su Z. Upregulation of autophagy by hypoxia-inducible factor-1alpha promotes EMT and metastatic ability of CD133+ pancreatic cancer stem-like cells during intermittent hypoxia. Oncol Rep. 2014;32(3):935–42.PubMedCrossRef
44.
go back to reference Peng YF, Shi YH, Shen YH, Ding ZB, Ke AW, Zhou J, Qiu SJ, Fan J. Promoting colonization in metastatic HCC cells by modulation of autophagy. PloS one. 2013;8(9):e74407.PubMedPubMedCentralCrossRef Peng YF, Shi YH, Shen YH, Ding ZB, Ke AW, Zhou J, Qiu SJ, Fan J. Promoting colonization in metastatic HCC cells by modulation of autophagy. PloS one. 2013;8(9):e74407.PubMedPubMedCentralCrossRef
45.
go back to reference Wolpin BM, Rubinson DA, Wang X, Chan JA, Cleary JM, Enzinger PC, Fuchs CS, McCleary NJ, Meyerhardt JA, Ng K, et al. Phase II and pharmacodynamic study of autophagy inhibition using hydroxychloroquine in patients with metastatic pancreatic adenocarcinoma. Oncologist. 2014;19(6):637–8.PubMedPubMedCentralCrossRef Wolpin BM, Rubinson DA, Wang X, Chan JA, Cleary JM, Enzinger PC, Fuchs CS, McCleary NJ, Meyerhardt JA, Ng K, et al. Phase II and pharmacodynamic study of autophagy inhibition using hydroxychloroquine in patients with metastatic pancreatic adenocarcinoma. Oncologist. 2014;19(6):637–8.PubMedPubMedCentralCrossRef
46.
go back to reference Husemann Y, Geigl JB, Schubert F, Musiani P, Meyer M, Burghart E, Forni G, Eils R, Fehm T, Riethmuller G, et al. Systemic spread is an early step in breast cancer. Cancer cell. 2008;13(1):58–68.PubMedCrossRef Husemann Y, Geigl JB, Schubert F, Musiani P, Meyer M, Burghart E, Forni G, Eils R, Fehm T, Riethmuller G, et al. Systemic spread is an early step in breast cancer. Cancer cell. 2008;13(1):58–68.PubMedCrossRef
47.
go back to reference Suzuki M, Mose ES, Montel V, Tarin D. Dormant cancer cells retrieved from metastasis-free organs regain tumorigenic and metastatic potency. Am J Pathol. 2006;169(2):673–81.PubMedPubMedCentralCrossRef Suzuki M, Mose ES, Montel V, Tarin D. Dormant cancer cells retrieved from metastasis-free organs regain tumorigenic and metastatic potency. Am J Pathol. 2006;169(2):673–81.PubMedPubMedCentralCrossRef
48.
go back to reference Chen H, Ko JM, Wong VC, Hyytiainen M, Keski-Oja J, Chua D, Nicholls JM, Cheung FM, Lee AW, Kwong DL, et al. LTBP-2 confers pleiotropic suppression and promotes dormancy in a growth factor permissive microenvironment in nasopharyngeal carcinoma. Cancer Lett. 2012;325(1):89–98.PubMedCrossRef Chen H, Ko JM, Wong VC, Hyytiainen M, Keski-Oja J, Chua D, Nicholls JM, Cheung FM, Lee AW, Kwong DL, et al. LTBP-2 confers pleiotropic suppression and promotes dormancy in a growth factor permissive microenvironment in nasopharyngeal carcinoma. Cancer Lett. 2012;325(1):89–98.PubMedCrossRef
49.
go back to reference Straume O, Shimamura T, Lampa MJG, Carretero J, Oyan AM, Jia D, Borgman CL, Soucheray M, Downing SR, Short SM, et al. Suppression of heat shock protein 27 induces long-term dormancy in human breast cancer. Proc Natl Acad Sci U S A. 2012;109(22):8699–704.PubMedPubMedCentralCrossRef Straume O, Shimamura T, Lampa MJG, Carretero J, Oyan AM, Jia D, Borgman CL, Soucheray M, Downing SR, Short SM, et al. Suppression of heat shock protein 27 induces long-term dormancy in human breast cancer. Proc Natl Acad Sci U S A. 2012;109(22):8699–704.PubMedPubMedCentralCrossRef
50.
go back to reference Lu X, Mu E, Wei Y, Riethdorf S, Yang Q, Yuan M, Yan J, Hua Y, Tiede BJ, Lu X, et al. VCAM-1 promotes osteolytic expansion of indolent bone micrometastasis of breast cancer by engaging alpha4beta1-positive osteoclast progenitors. Cancer cell. 2011;20(6):701–14.PubMedPubMedCentralCrossRef Lu X, Mu E, Wei Y, Riethdorf S, Yang Q, Yuan M, Yan J, Hua Y, Tiede BJ, Lu X, et al. VCAM-1 promotes osteolytic expansion of indolent bone micrometastasis of breast cancer by engaging alpha4beta1-positive osteoclast progenitors. Cancer cell. 2011;20(6):701–14.PubMedPubMedCentralCrossRef
51.
go back to reference Kobayashi A, Okuda H, Xing F, Pandey PR, Watabe M, Hirota S, Pai SK, Liu W, Fukuda K, Chambers C, et al. Bone morphogenetic protein 7 in dormancy and metastasis of prostate cancer stem-like cells in bone. J Exp Med. 2011;208(13):2641–55.PubMedPubMedCentralCrossRef Kobayashi A, Okuda H, Xing F, Pandey PR, Watabe M, Hirota S, Pai SK, Liu W, Fukuda K, Chambers C, et al. Bone morphogenetic protein 7 in dormancy and metastasis of prostate cancer stem-like cells in bone. J Exp Med. 2011;208(13):2641–55.PubMedPubMedCentralCrossRef
52.
go back to reference Bragado P, Estrada Y, Parikh F, Krause S, Capobianco C, Farina HG, Schewe DM, Aguirre-Ghiso JA. TGF-beta2 dictates disseminated tumour cell fate in target organs through TGF-beta-RIII and p38alpha/beta signalling. Nat Cell Biol. 2013;15(11):1351–61.PubMedPubMedCentralCrossRef Bragado P, Estrada Y, Parikh F, Krause S, Capobianco C, Farina HG, Schewe DM, Aguirre-Ghiso JA. TGF-beta2 dictates disseminated tumour cell fate in target organs through TGF-beta-RIII and p38alpha/beta signalling. Nat Cell Biol. 2013;15(11):1351–61.PubMedPubMedCentralCrossRef
53.
go back to reference Gao H, Chakraborty G, Lee-Lim AP, Mo Q, Decker M, Vonica A, Shen R, Brogi E, Brivanlou AH, Giancotti FG. The BMP inhibitor Coco reactivates breast cancer cells at lung metastatic sites. Cell. 2012;150(4):764–79.PubMedPubMedCentralCrossRef Gao H, Chakraborty G, Lee-Lim AP, Mo Q, Decker M, Vonica A, Shen R, Brogi E, Brivanlou AH, Giancotti FG. The BMP inhibitor Coco reactivates breast cancer cells at lung metastatic sites. Cell. 2012;150(4):764–79.PubMedPubMedCentralCrossRef
54.
go back to reference Lu Z, Luo RZ, Lu Y, Zhang X, Yu Q, Khare S, Kondo S, Kondo Y, Yu Y, Mills GB, et al. The tumor suppressor gene ARHI regulates autophagy and tumor dormancy in human ovarian cancer cells. J Clin Invest. 2008;118(12):3917–29.PubMedPubMedCentral Lu Z, Luo RZ, Lu Y, Zhang X, Yu Q, Khare S, Kondo S, Kondo Y, Yu Y, Mills GB, et al. The tumor suppressor gene ARHI regulates autophagy and tumor dormancy in human ovarian cancer cells. J Clin Invest. 2008;118(12):3917–29.PubMedPubMedCentral
55.
go back to reference Minciacchi VR, Freeman MR, Di Vizio D. Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes. Semin Cell Dev Biol. 2015;40:41–51.PubMedPubMedCentralCrossRef Minciacchi VR, Freeman MR, Di Vizio D. Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes. Semin Cell Dev Biol. 2015;40:41–51.PubMedPubMedCentralCrossRef
56.
go back to reference Becker A, Thakur BK, Weiss JM, Kim HS, Peinado H, Lyden D. Extracellular Vesicles in Cancer: Cell-to-Cell Mediators of Metastasis. Cancer cell. 2016;30(6):836–48.PubMedCrossRef Becker A, Thakur BK, Weiss JM, Kim HS, Peinado H, Lyden D. Extracellular Vesicles in Cancer: Cell-to-Cell Mediators of Metastasis. Cancer cell. 2016;30(6):836–48.PubMedCrossRef
57.
go back to reference Ghasemi R, Grassadonia A, Tinari N, Piccolo E, Natoli C, Tomao F, Iacobelli S. Tumor-derived microvesicles: the metastasomes. Med Hypotheses. 2013;80(1):75–82.PubMedCrossRef Ghasemi R, Grassadonia A, Tinari N, Piccolo E, Natoli C, Tomao F, Iacobelli S. Tumor-derived microvesicles: the metastasomes. Med Hypotheses. 2013;80(1):75–82.PubMedCrossRef
58.
go back to reference Lee TH, D’Asti E, Magnus N, Al-Nedawi K, Meehan B, Rak J: Microvesicles as mediators of intercellular communication in cancer--the emerging science of cellular ‘debris’. Semin Immunopathol 2011, 33(5):455–467. Lee TH, D’Asti E, Magnus N, Al-Nedawi K, Meehan B, Rak J: Microvesicles as mediators of intercellular communication in cancer--the emerging science of cellular ‘debris’. Semin Immunopathol 2011, 33(5):455–467.
59.
go back to reference Harris DA, Patel SH, Gucek M, Hendrix A, Westbroek W, Taraska JW. Exosomes released from breast cancer carcinomas stimulate cell movement. PloS one. 2015;10(3):e0117495.PubMedPubMedCentralCrossRef Harris DA, Patel SH, Gucek M, Hendrix A, Westbroek W, Taraska JW. Exosomes released from breast cancer carcinomas stimulate cell movement. PloS one. 2015;10(3):e0117495.PubMedPubMedCentralCrossRef
60.
go back to reference Cho JA, Park H, Lim EH, Lee KW. Exosomes from breast cancer cells can convert adipose tissue-derived mesenchymal stem cells into myofibroblast-like cells. Int J Oncol. 2012;40(1):130–8.PubMed Cho JA, Park H, Lim EH, Lee KW. Exosomes from breast cancer cells can convert adipose tissue-derived mesenchymal stem cells into myofibroblast-like cells. Int J Oncol. 2012;40(1):130–8.PubMed
61.
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. Nature cell biology. 2015;17(6):816–26.PubMedCrossRef 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. Nature cell biology. 2015;17(6):816–26.PubMedCrossRef
62.
go back to reference Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M, Molina H, Kohsaka S, Di Giannatale A, Ceder S, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015;527(7578):329–35.PubMedPubMedCentralCrossRef Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M, Molina H, Kohsaka S, Di Giannatale A, Ceder S, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015;527(7578):329–35.PubMedPubMedCentralCrossRef
63.
go back to reference Liu Y, Gu Y, Han Y, Zhang Q, Jiang Z, Zhang X, Huang B, Xu X, Zheng J, Cao X. Tumor Exosomal RNAs Promote Lung Pre-metastatic Niche Formation by Activating Alveolar Epithelial TLR3 to Recruit Neutrophils. Cancer cell. 2016;30(2):243–56.PubMedCrossRef Liu Y, Gu Y, Han Y, Zhang Q, Jiang Z, Zhang X, Huang B, Xu X, Zheng J, Cao X. Tumor Exosomal RNAs Promote Lung Pre-metastatic Niche Formation by Activating Alveolar Epithelial TLR3 to Recruit Neutrophils. Cancer cell. 2016;30(2):243–56.PubMedCrossRef
64.
go back to reference Zhang H, Deng T, Liu R, Bai M, Zhou L, Wang X, Li S, Wang X, Yang H, Li J, et al. Exosome-delivered EGFR regulates liver microenvironment to promote gastric cancer liver metastasis. Nature communications. 2017;8:15,016.CrossRef Zhang H, Deng T, Liu R, Bai M, Zhou L, Wang X, Li S, Wang X, Yang H, Li J, et al. Exosome-delivered EGFR regulates liver microenvironment to promote gastric cancer liver metastasis. Nature communications. 2017;8:15,016.CrossRef
65.
go back to reference Fremder E, Munster M, Aharon A, Miller V, Gingis-Velitski S, Voloshin T, Alishekevitz D, Bril R, Scherer SJ, Loven D, et al. Tumor-derived microparticles induce bone marrow-derived cell mobilization and tumor homing: a process regulated by osteopontin. Int J Cancer. 2014;135(2):270–81.PubMedCrossRef Fremder E, Munster M, Aharon A, Miller V, Gingis-Velitski S, Voloshin T, Alishekevitz D, Bril R, Scherer SJ, Loven D, et al. Tumor-derived microparticles induce bone marrow-derived cell mobilization and tumor homing: a process regulated by osteopontin. Int J Cancer. 2014;135(2):270–81.PubMedCrossRef
66.
go back to reference Peinado H, Lavotshkin S, Lyden D. The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin Cancer Biol. 2011;21(2):139–46.PubMedCrossRef Peinado H, Lavotshkin S, Lyden D. The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin Cancer Biol. 2011;21(2):139–46.PubMedCrossRef
67.
go back to reference Janowska-Wieczorek A, Wysoczynski M, Kijowski J, Marquez-Curtis L, Machalinski B, Ratajczak J, Ratajczak MZ. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer. 2005;113(5):752–60.PubMedCrossRef Janowska-Wieczorek A, Wysoczynski M, Kijowski J, Marquez-Curtis L, Machalinski B, Ratajczak J, Ratajczak MZ. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer. 2005;113(5):752–60.PubMedCrossRef
68.
go back to reference Di Vizio D, Morello M, Dudley AC, Schow PW, Adam RM, Morley S, Mulholland D, Rotinen M, Hager MH, Insabato L, et al. Large oncosomes in human prostate cancer tissues and in the circulation of mice with metastatic disease. Am J Pathol. 2012;181(5):1573–84.PubMedPubMedCentralCrossRef Di Vizio D, Morello M, Dudley AC, Schow PW, Adam RM, Morley S, Mulholland D, Rotinen M, Hager MH, Insabato L, et al. Large oncosomes in human prostate cancer tissues and in the circulation of mice with metastatic disease. Am J Pathol. 2012;181(5):1573–84.PubMedPubMedCentralCrossRef
69.
go back to reference Kim S, Takahashi H, Lin WW, Descargues P, Grivennikov S, Kim Y, Luo JL, Karin M. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature. 2009;457(7225):102–6.PubMedPubMedCentralCrossRef Kim S, Takahashi H, Lin WW, Descargues P, Grivennikov S, Kim Y, Luo JL, Karin M. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature. 2009;457(7225):102–6.PubMedPubMedCentralCrossRef
70.
go back to reference Lu X, Kang Y. Chemokine (C-C motif) ligand 2 engages CCR2+ stromal cells of monocytic origin to promote breast cancer metastasis to lung and bone. J Biol Chem. 2009;284(42):29,087–96.CrossRef Lu X, Kang Y. Chemokine (C-C motif) ligand 2 engages CCR2+ stromal cells of monocytic origin to promote breast cancer metastasis to lung and bone. J Biol Chem. 2009;284(42):29,087–96.CrossRef
71.
go back to reference Lee E, Fertig EJ, Jin K, Sukumar S, Pandey NB, Popel AS. Breast cancer cells condition lymphatic endothelial cells within pre-metastatic niches to promote metastasis. Nat Commun. 2014;5:4715.PubMedPubMedCentralCrossRef Lee E, Fertig EJ, Jin K, Sukumar S, Pandey NB, Popel AS. Breast cancer cells condition lymphatic endothelial cells within pre-metastatic niches to promote metastasis. Nat Commun. 2014;5:4715.PubMedPubMedCentralCrossRef
72.
go back to reference Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, Kaiser EA, Snyder LA, Pollard JW. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 2011;475(7355):222–5.PubMedPubMedCentralCrossRef Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, Kaiser EA, Snyder LA, Pollard JW. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 2011;475(7355):222–5.PubMedPubMedCentralCrossRef
73.
go back to reference Bonapace L, Coissieux MM, Wyckoff J, Mertz KD, Varga Z, Junt T, Bentires-Alj M. Cessation of CCL2 inhibition accelerates breast cancer metastasis by promoting angiogenesis. Nature. 2014;515(7525):130–3.PubMedCrossRef Bonapace L, Coissieux MM, Wyckoff J, Mertz KD, Varga Z, Junt T, Bentires-Alj M. Cessation of CCL2 inhibition accelerates breast cancer metastasis by promoting angiogenesis. Nature. 2014;515(7525):130–3.PubMedCrossRef
74.
go back to reference Mi Z, Bhattacharya SD, Kim VM, Guo H, Talbot LJ, Kuo PC. Osteopontin promotes CCL5-mesenchymal stromal cell-mediated breast cancer metastasis. Carcinogenesis. 2011;32(4):477–87.PubMedPubMedCentralCrossRef Mi Z, Bhattacharya SD, Kim VM, Guo H, Talbot LJ, Kuo PC. Osteopontin promotes CCL5-mesenchymal stromal cell-mediated breast cancer metastasis. Carcinogenesis. 2011;32(4):477–87.PubMedPubMedCentralCrossRef
75.
go back to reference Oskarsson T, Acharyya S, Zhang XH, Vanharanta S, Tavazoie SF, Morris PG, Downey RJ, Manova-Todorova K, Brogi E, Massague J. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med. 2011;17(7):867–74.PubMedPubMedCentralCrossRef Oskarsson T, Acharyya S, Zhang XH, Vanharanta S, Tavazoie SF, Morris PG, Downey RJ, Manova-Todorova K, Brogi E, Massague J. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med. 2011;17(7):867–74.PubMedPubMedCentralCrossRef
76.
go back to reference Wang C, Jiang K, Kang X, Gao D, Sun C, Li Y, Sun L, Zhang S, Liu X, Wu W, et al. Tumor-derived secretory clusterin induces epithelial-mesenchymal transition and facilitates hepatocellular carcinoma metastasis. Int J Biochem Cell Biol. 2012;44(12):2308–20.PubMedCrossRef Wang C, Jiang K, Kang X, Gao D, Sun C, Li Y, Sun L, Zhang S, Liu X, Wu W, et al. Tumor-derived secretory clusterin induces epithelial-mesenchymal transition and facilitates hepatocellular carcinoma metastasis. Int J Biochem Cell Biol. 2012;44(12):2308–20.PubMedCrossRef
77.
go back to reference Joo YN, Jin H, Eun SY, Park SW, Chang KC, Kim HJ. P2Y2R activation by nucleotides released from the highly metastatic breast cancer cell contributes to pre-metastatic niche formation by mediating lysyl oxidase secretion, collagen crosslinking, and monocyte recruitment. Oncotarget. 2014;5(19):9322.PubMedPubMedCentralCrossRef Joo YN, Jin H, Eun SY, Park SW, Chang KC, Kim HJ. P2Y2R activation by nucleotides released from the highly metastatic breast cancer cell contributes to pre-metastatic niche formation by mediating lysyl oxidase secretion, collagen crosslinking, and monocyte recruitment. Oncotarget. 2014;5(19):9322.PubMedPubMedCentralCrossRef
78.
79.
go back to reference Chambers AF, Groom AC, MacDonald IC. Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer. 2002;2(8):563–72.PubMedCrossRef Chambers AF, Groom AC, MacDonald IC. Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer. 2002;2(8):563–72.PubMedCrossRef
80.
go back to reference Wirtz D, Konstantopoulos K, Searson PC. The physics of cancer: the role of physical interactions and mechanical forces in metastasis. Nat Rev Cancer. 2011;11(7):512–22.PubMedPubMedCentralCrossRef Wirtz D, Konstantopoulos K, Searson PC. The physics of cancer: the role of physical interactions and mechanical forces in metastasis. Nat Rev Cancer. 2011;11(7):512–22.PubMedPubMedCentralCrossRef
81.
go back to reference Evani SJ, Prabhu RG, Gnanaruban V, Finol EA, Ramasubramanian AK. Monocytes mediate metastatic breast tumor cell adhesion to endothelium under flow. FASEB J. 2013;27(8):3017–29.PubMedPubMedCentralCrossRef Evani SJ, Prabhu RG, Gnanaruban V, Finol EA, Ramasubramanian AK. Monocytes mediate metastatic breast tumor cell adhesion to endothelium under flow. FASEB J. 2013;27(8):3017–29.PubMedPubMedCentralCrossRef
82.
go back to reference Uppal A, Wightman SC, Ganai S, Weichselbaum RR, An G. Investigation of the essential role of platelet-tumor cell interactions in metastasis progression using an agent-based model. Theor Biol Med Model. 2014;11(1):17.PubMedPubMedCentralCrossRef Uppal A, Wightman SC, Ganai S, Weichselbaum RR, An G. Investigation of the essential role of platelet-tumor cell interactions in metastasis progression using an agent-based model. Theor Biol Med Model. 2014;11(1):17.PubMedPubMedCentralCrossRef
83.
go back to reference Aceto N, Bardia A, Miyamoto DT, Donaldson MC, Wittner BS, Spencer JA, Yu M, Pely A, Engstrom A, Zhu H, et al. Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell. 2014;158(5):1110–22.PubMedPubMedCentralCrossRef Aceto N, Bardia A, Miyamoto DT, Donaldson MC, Wittner BS, Spencer JA, Yu M, Pely A, Engstrom A, Zhu H, et al. Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell. 2014;158(5):1110–22.PubMedPubMedCentralCrossRef
84.
go back to reference Guo P, Cai B, Lei M, Liu Y, Fu BM. Differential arrest and adhesion of tumor cells and microbeads in the microvasculature. Biomech Model Mechanobiol. 2014;13(3):537–50.PubMedCrossRef Guo P, Cai B, Lei M, Liu Y, Fu BM. Differential arrest and adhesion of tumor cells and microbeads in the microvasculature. Biomech Model Mechanobiol. 2014;13(3):537–50.PubMedCrossRef
85.
go back to reference Kienast Y, von Baumgarten L, Fuhrmann M, Klinkert WE, Goldbrunner R, Herms J, Winkler F. Real-time imaging reveals the single steps of brain metastasis formation. Nat Med. 2010;16(1):116–22.PubMedCrossRef Kienast Y, von Baumgarten L, Fuhrmann M, Klinkert WE, Goldbrunner R, Herms J, Winkler F. Real-time imaging reveals the single steps of brain metastasis formation. Nat Med. 2010;16(1):116–22.PubMedCrossRef
86.
go back to reference Reymond N, d’Agua BB, Ridley AJ. Crossing the endothelial barrier during metastasis. Nat Rev Cancer. 2013;13(12):858–70.PubMedCrossRef Reymond N, d’Agua BB, Ridley AJ. Crossing the endothelial barrier during metastasis. Nat Rev Cancer. 2013;13(12):858–70.PubMedCrossRef
87.
go back to reference Azevedo AS, Follain G, Patthabhiraman S, Harlepp S, Goetz JG. Metastasis of circulating tumor cells: favorable soil or suitable biomechanics, or both? Cell Adh Migr. 2015;9(5):345–56.PubMedPubMedCentralCrossRef Azevedo AS, Follain G, Patthabhiraman S, Harlepp S, Goetz JG. Metastasis of circulating tumor cells: favorable soil or suitable biomechanics, or both? Cell Adh Migr. 2015;9(5):345–56.PubMedPubMedCentralCrossRef
88.
go back to reference Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer. 2009;9(4):239–52.PubMedCrossRef Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer. 2009;9(4):239–52.PubMedCrossRef
89.
go back to reference Yang M, Chen J, Su F, Yu B, Su F, Lin L, Liu Y, Huang J-D, Song E. Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer. 2011;10(1):117.PubMedPubMedCentralCrossRef Yang M, Chen J, Su F, Yu B, Su F, Lin L, Liu Y, Huang J-D, Song E. Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer. 2011;10(1):117.PubMedPubMedCentralCrossRef
90.
go back to reference Chen J, Yao Y, Gong C, Yu F, Su S, Chen J, Liu B, Deng H, Wang F, Lin L, et al. CCL18 from tumor-associated macrophages promotes breast cancer metastasis via PITPNM3. Cancer cell. 2011;19(4):541–55.PubMedPubMedCentralCrossRef Chen J, Yao Y, Gong C, Yu F, Su S, Chen J, Liu B, Deng H, Wang F, Lin L, et al. CCL18 from tumor-associated macrophages promotes breast cancer metastasis via PITPNM3. Cancer cell. 2011;19(4):541–55.PubMedPubMedCentralCrossRef
91.
go back to reference Liu B, Jia Y, Ma J, Wu S, Jiang H, Cao Y, Sun X, Yin X, Yan S, Shang M, et al. Tumor-associated macrophage-derived CCL20 enhances the growth and metastasis of pancreatic cancer. Acta Biochim Biophys Sin (Shanghai). 2016;48(12):1067–74.CrossRef Liu B, Jia Y, Ma J, Wu S, Jiang H, Cao Y, Sun X, Yin X, Yan S, Shang M, et al. Tumor-associated macrophage-derived CCL20 enhances the growth and metastasis of pancreatic cancer. Acta Biochim Biophys Sin (Shanghai). 2016;48(12):1067–74.CrossRef
92.
go back to reference Oren B, Urosevic J, Mertens C, Mora J, Guiu M, Gomis RR, Weigert A, Schmid T, Grein S, Brune B, et al. Tumour stroma-derived lipocalin-2 promotes breast cancer metastasis. J Pathol. 2016;239(3):274–85.PubMedCrossRef Oren B, Urosevic J, Mertens C, Mora J, Guiu M, Gomis RR, Weigert A, Schmid T, Grein S, Brune B, et al. Tumour stroma-derived lipocalin-2 promotes breast cancer metastasis. J Pathol. 2016;239(3):274–85.PubMedCrossRef
93.
go back to reference Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, Richardson AL, Polyak K, Tubo R, Weinberg RA. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature. 2007;449(7162):557–63.PubMedCrossRef Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, Richardson AL, Polyak K, Tubo R, Weinberg RA. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature. 2007;449(7162):557–63.PubMedCrossRef
94.
go back to reference Swamydas M, Ricci K, Rego SL, Dreau D. Mesenchymal stem cell-derived CCL-9 and CCL-5 promote mammary tumor cell invasion and the activation of matrix metalloproteinases. Cell Adh Migr. 2013;7(3):315–24.PubMedPubMedCentralCrossRef Swamydas M, Ricci K, Rego SL, Dreau D. Mesenchymal stem cell-derived CCL-9 and CCL-5 promote mammary tumor cell invasion and the activation of matrix metalloproteinases. Cell Adh Migr. 2013;7(3):315–24.PubMedPubMedCentralCrossRef
95.
go back to reference Gonzalez ME, Martin EE, Anwar T, Arellano-Garcia C, Medhora N, Lama A, Chen YC, Tanager KS, Yoon E, Kidwell KM, et al. Mesenchymal Stem Cell-Induced DDR2 Mediates Stromal-Breast Cancer Interactions and Metastasis Growth. Cell Rep. 2017;18(5):1215–28.PubMedPubMedCentralCrossRef Gonzalez ME, Martin EE, Anwar T, Arellano-Garcia C, Medhora N, Lama A, Chen YC, Tanager KS, Yoon E, Kidwell KM, et al. Mesenchymal Stem Cell-Induced DDR2 Mediates Stromal-Breast Cancer Interactions and Metastasis Growth. Cell Rep. 2017;18(5):1215–28.PubMedPubMedCentralCrossRef
96.
go back to reference Mazzone M, Dettori D, Leite de Oliveira R, Loges S, Schmidt T, Jonckx B, Tian YM, Lanahan AA, Pollard P, Ruiz de Almodovar C, et al. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell. 2009;136(5):839–51.PubMedPubMedCentralCrossRef Mazzone M, Dettori D, Leite de Oliveira R, Loges S, Schmidt T, Jonckx B, Tian YM, Lanahan AA, Pollard P, Ruiz de Almodovar C, et al. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell. 2009;136(5):839–51.PubMedPubMedCentralCrossRef
97.
go back to reference Wang X, Lee SO, Xia S, Jiang Q, Luo J, Li L, Yeh S, Chang C. Endothelial cells enhance prostate cancer metastasis via IL-6-- > androgen receptor-- > TGF-beta-- > MMP-9 signals. Mol Cancer Ther. 2013;12(6):1026–37.PubMedPubMedCentralCrossRef Wang X, Lee SO, Xia S, Jiang Q, Luo J, Li L, Yeh S, Chang C. Endothelial cells enhance prostate cancer metastasis via IL-6-- > androgen receptor-- > TGF-beta-- > MMP-9 signals. Mol Cancer Ther. 2013;12(6):1026–37.PubMedPubMedCentralCrossRef
98.
go back to reference Yadav A, Kumar B, Yu JG, Old M, Teknos TN, Kumar P. Tumor-Associated Endothelial Cells Promote Tumor Metastasis by Chaperoning Circulating Tumor Cells and Protecting Them from Anoikis. PloS one. 2015;10(10):e0141602.PubMedPubMedCentralCrossRef Yadav A, Kumar B, Yu JG, Old M, Teknos TN, Kumar P. Tumor-Associated Endothelial Cells Promote Tumor Metastasis by Chaperoning Circulating Tumor Cells and Protecting Them from Anoikis. PloS one. 2015;10(10):e0141602.PubMedPubMedCentralCrossRef
99.
go back to reference Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, Carey VJ, Richardson AL, Weinberg RA. 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.PubMedCrossRef Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, Carey VJ, Richardson AL, Weinberg RA. 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.PubMedCrossRef
100.
go back to reference Goetz JG, Minguet S, Navarro-Lerida I, Lazcano JJ, Samaniego R, Calvo E, Tello M, Osteso-Ibanez T, Pellinen T, Echarri A, et al. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell. 2011;146(1):148–63.PubMedPubMedCentralCrossRef Goetz JG, Minguet S, Navarro-Lerida I, Lazcano JJ, Samaniego R, Calvo E, Tello M, Osteso-Ibanez T, Pellinen T, Echarri A, et al. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell. 2011;146(1):148–63.PubMedPubMedCentralCrossRef
101.
go back to reference Luga V, Zhang L, Viloria-Petit AM, Ogunjimi AA, Inanlou MR, Chiu E, Buchanan M, Hosein AN, Basik M, Wrana JL. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell. 2012;151(7):1542–56.PubMedCrossRef Luga V, Zhang L, Viloria-Petit AM, Ogunjimi AA, Inanlou MR, Chiu E, Buchanan M, Hosein AN, Basik M, Wrana JL. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell. 2012;151(7):1542–56.PubMedCrossRef
102.
go back to reference Dirat B, Bochet L, Dabek M, Daviaud D, Dauvillier S, Majed B, Wang YY, Meulle A, Salles B, Le Gonidec S, et al. Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion. Cancer Res. 2011;71(7):2455–65.PubMedCrossRef Dirat B, Bochet L, Dabek M, Daviaud D, Dauvillier S, Majed B, Wang YY, Meulle A, Salles B, Le Gonidec S, et al. Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion. Cancer Res. 2011;71(7):2455–65.PubMedCrossRef
103.
go back to reference Park J, Euhus DM, Scherer PE. Paracrine and endocrine effects of adipose tissue on cancer development and progression. Endocr Rev. 2011;32(4):550–70.PubMedPubMedCentralCrossRef Park J, Euhus DM, Scherer PE. Paracrine and endocrine effects of adipose tissue on cancer development and progression. Endocr Rev. 2011;32(4):550–70.PubMedPubMedCentralCrossRef
104.
go back to reference Carter JC, Church FC. Mature breast adipocytes promote breast cancer cell motility. Exp Mol Pathol. 2012;92(3):312–7.PubMedCrossRef Carter JC, Church FC. Mature breast adipocytes promote breast cancer cell motility. Exp Mol Pathol. 2012;92(3):312–7.PubMedCrossRef
105.
go back to reference Kushiro K, Chu RA, Verma A, Nunez NP. Adipocytes Promote B16BL6 Melanoma Cell Invasion and the Epithelial-to-Mesenchymal Transition. Cancer Microenviron. 2012;5(1):73–82.PubMedCrossRef Kushiro K, Chu RA, Verma A, Nunez NP. Adipocytes Promote B16BL6 Melanoma Cell Invasion and the Epithelial-to-Mesenchymal Transition. Cancer Microenviron. 2012;5(1):73–82.PubMedCrossRef
106.
go back to reference Xie H, Li L, Zhu G, Dang Q, Ma Z, He D, Chang L, Song W, Chang HC, Krolewski JJ, et al. Infiltrated pre-adipocytes increase prostate cancer metastasis via modulation of the miR-301a/androgen receptor (AR)/TGF-beta1/Smad/MMP9 signals. Oncotarget. 2015;6(14):12,326–39.CrossRef Xie H, Li L, Zhu G, Dang Q, Ma Z, He D, Chang L, Song W, Chang HC, Krolewski JJ, et al. Infiltrated pre-adipocytes increase prostate cancer metastasis via modulation of the miR-301a/androgen receptor (AR)/TGF-beta1/Smad/MMP9 signals. Oncotarget. 2015;6(14):12,326–39.CrossRef
107.
go back to reference Wang C, Gao C, Meng K, Qiao H, Wang Y. Human adipocytes stimulate invasion of breast cancer MCF-7 cells by secreting IGFBP-2. PloS one. 2015;10(3):e0119348.PubMedPubMedCentralCrossRef Wang C, Gao C, Meng K, Qiao H, Wang Y. Human adipocytes stimulate invasion of breast cancer MCF-7 cells by secreting IGFBP-2. PloS one. 2015;10(3):e0119348.PubMedPubMedCentralCrossRef
108.
go back to reference Padua D, Zhang XH, Wang Q, Nadal C, Gerald WL, Gomis RR, Massague J. TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell. 2008;133(1):66–77.PubMedPubMedCentralCrossRef Padua D, Zhang XH, Wang Q, Nadal C, Gerald WL, Gomis RR, Massague J. TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell. 2008;133(1):66–77.PubMedPubMedCentralCrossRef
109.
go back to reference Cao Y, Slaney CY, Bidwell BN, Parker BS, Johnstone CN, Rautela J, Eckhardt BL, Anderson RL. BMP4 inhibits breast cancer metastasis by blocking myeloid-derived suppressor cell activity. Cancer Res. 2014;74(18):5091–102.PubMedCrossRef Cao Y, Slaney CY, Bidwell BN, Parker BS, Johnstone CN, Rautela J, Eckhardt BL, Anderson RL. BMP4 inhibits breast cancer metastasis by blocking myeloid-derived suppressor cell activity. Cancer Res. 2014;74(18):5091–102.PubMedCrossRef
110.
go back to reference Gay LJ, Felding-Habermann B. Contribution of platelets to tumour metastasis. Nat Rev Cancer. 2011;11(2):123–34.PubMedCrossRef Gay LJ, Felding-Habermann B. Contribution of platelets to tumour metastasis. Nat Rev Cancer. 2011;11(2):123–34.PubMedCrossRef
111.
go back to reference Labelle M, Begum S, Hynes RO. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer cell. 2011;20(5):576–90.PubMedPubMedCentralCrossRef Labelle M, Begum S, Hynes RO. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer cell. 2011;20(5):576–90.PubMedPubMedCentralCrossRef
112.
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(1):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(1):130–7.PubMedCrossRef
113.
go back to reference Cooke VG, LeBleu VS, Keskin D, Khan Z, O’Connell JT, Teng Y, Duncan MB, Xie L, Maeda G, Vong S et al.: Pericyte depletion results in hypoxia-associated epithelial-to-mesenchymal transition and metastasis mediated by met signaling pathway. Cancer cell 2012, 21(1):66–81. Cooke VG, LeBleu VS, Keskin D, Khan Z, O’Connell JT, Teng Y, Duncan MB, Xie L, Maeda G, Vong S et al.: Pericyte depletion results in hypoxia-associated epithelial-to-mesenchymal transition and metastasis mediated by met signaling pathway. Cancer cell 2012, 21(1):66–81.
114.
go back to reference Hu S, Li L, Yeh S, Cui Y, Li X, Chang HC, Jin J, Chang C. Infiltrating T cells promote prostate cancer metastasis via modulation of FGF11-- > miRNA-541-- > androgen receptor (AR)-- > MMP9 signaling. Mol Oncol. 2015;9(1):44–57.PubMedCrossRef Hu S, Li L, Yeh S, Cui Y, Li X, Chang HC, Jin J, Chang C. Infiltrating T cells promote prostate cancer metastasis via modulation of FGF11-- > miRNA-541-- > androgen receptor (AR)-- > MMP9 signaling. Mol Oncol. 2015;9(1):44–57.PubMedCrossRef
115.
go back to reference Xing F, Okuda H, Watabe M, Kobayashi A, Pai SK, Liu W, Pandey PR, Fukuda K, Hirota S, Sugai T, et al. Hypoxia-induced Jagged2 promotes breast cancer metastasis and self-renewal of cancer stem-like cells. Oncogene. 2011;30(39):4075–86.PubMedPubMedCentralCrossRef Xing F, Okuda H, Watabe M, Kobayashi A, Pai SK, Liu W, Pandey PR, Fukuda K, Hirota S, Sugai T, et al. Hypoxia-induced Jagged2 promotes breast cancer metastasis and self-renewal of cancer stem-like cells. Oncogene. 2011;30(39):4075–86.PubMedPubMedCentralCrossRef
116.
go back to reference Chaturvedi P, Gilkes DM, Wong CC. Kshitiz, Luo W, Zhang H, Wei H, Takano N, Schito L, Levchenko A et al.: Hypoxia-inducible factor-dependent breast cancer-mesenchymal stem cell bidirectional signaling promotes metastasis. J Clin Invest. 2013;123(1):189–205.PubMed Chaturvedi P, Gilkes DM, Wong CC. Kshitiz, Luo W, Zhang H, Wei H, Takano N, Schito L, Levchenko A et al.: Hypoxia-inducible factor-dependent breast cancer-mesenchymal stem cell bidirectional signaling promotes metastasis. J Clin Invest. 2013;123(1):189–205.PubMed
117.
go back to reference Ye LY, Chen W, Bai XL, Xu XY, Zhang Q, Xia XF, Sun X, Li GG, Hu QD, Fu QH, et al. Hypoxia-Induced Epithelial-to-Mesenchymal Transition in Hepatocellular Carcinoma Induces an Immunosuppressive Tumor Microenvironment to Promote Metastasis. Cancer Res. 2016;76(4):818–30.PubMedCrossRef Ye LY, Chen W, Bai XL, Xu XY, Zhang Q, Xia XF, Sun X, Li GG, Hu QD, Fu QH, et al. Hypoxia-Induced Epithelial-to-Mesenchymal Transition in Hepatocellular Carcinoma Induces an Immunosuppressive Tumor Microenvironment to Promote Metastasis. Cancer Res. 2016;76(4):818–30.PubMedCrossRef
118.
go back to reference Sceneay J, Chow MT, Chen A, Halse HM, Wong CS, Andrews DM, Sloan EK, Parker BS, Bowtell DD, Smyth MJ, et al. Primary tumor hypoxia recruits CD11b+/Ly6Cmed/Ly6G+ immune suppressor cells and compromises NK cell cytotoxicity in the premetastatic niche. Cancer Res. 2012;72(16):3906–11.PubMedCrossRef Sceneay J, Chow MT, Chen A, Halse HM, Wong CS, Andrews DM, Sloan EK, Parker BS, Bowtell DD, Smyth MJ, et al. Primary tumor hypoxia recruits CD11b+/Ly6Cmed/Ly6G+ immune suppressor cells and compromises NK cell cytotoxicity in the premetastatic niche. Cancer Res. 2012;72(16):3906–11.PubMedCrossRef
119.
go back to reference Hiratsuka S, Nakamura K, Iwai S, Murakami M, Itoh T, Kijima H, Shipley JM, Senior RM, Shibuya M. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer cell. 2002;2(4):289–300.PubMedCrossRef Hiratsuka S, Nakamura K, Iwai S, Murakami M, Itoh T, Kijima H, Shipley JM, Senior RM, Shibuya M. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer cell. 2002;2(4):289–300.PubMedCrossRef
120.
go back to reference Chen Q, Zhang XH, Massague J. Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Cancer cell. 2011;20(4):538–49.PubMedPubMedCentralCrossRef Chen Q, Zhang XH, Massague J. Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Cancer cell. 2011;20(4):538–49.PubMedPubMedCentralCrossRef
121.
go back to reference Laubli H, Spanaus KS, Borsig L. Selectin-mediated activation of endothelial cells induces expression of CCL5 and promotes metastasis through recruitment of monocytes. Blood. 2009;114(20):4583–91.PubMedCrossRef Laubli H, Spanaus KS, Borsig L. Selectin-mediated activation of endothelial cells induces expression of CCL5 and promotes metastasis through recruitment of monocytes. Blood. 2009;114(20):4583–91.PubMedCrossRef
122.
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(12):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(12):1369–75.PubMedCrossRef
123.
go back to reference Yan HH, Pickup M, Pang Y, Gorska AE, Li Z, Chytil A, Geng Y, Gray JW, Moses HL, Yang L. Gr-1 + CD11b + myeloid cells tip the balance of immune protection to tumor promotion in the premetastatic lung. Cancer Res. 2010;70(15):6139–49.PubMedPubMedCentralCrossRef Yan HH, Pickup M, Pang Y, Gorska AE, Li Z, Chytil A, Geng Y, Gray JW, Moses HL, Yang L. Gr-1 + CD11b + myeloid cells tip the balance of immune protection to tumor promotion in the premetastatic lung. Cancer Res. 2010;70(15):6139–49.PubMedPubMedCentralCrossRef
124.
go back to reference Gao D, Joshi N, Choi H, Ryu S, Hahn M, Catena R, Sadik H, Argani P, Wagner P, Vahdat LT, et al. Myeloid progenitor cells in the premetastatic lung promote metastases by inducing mesenchymal to epithelial transition. Cancer Res. 2012;72(6):1384–94.PubMedCrossRef Gao D, Joshi N, Choi H, Ryu S, Hahn M, Catena R, Sadik H, Argani P, Wagner P, Vahdat LT, et al. Myeloid progenitor cells in the premetastatic lung promote metastases by inducing mesenchymal to epithelial transition. Cancer Res. 2012;72(6):1384–94.PubMedCrossRef
125.
126.
go back to reference Clever D, Roychoudhuri R, Constantinides MG, Askenase MH, Sukumar M, Klebanoff CA, Eil RL, Hickman HD, Yu Z, Pan JH, et al. Oxygen Sensing by T Cells Establishes an Immunologically Tolerant Metastatic Niche. Cell. 2016;166(5):1117–31. e1114PubMedPubMedCentralCrossRef Clever D, Roychoudhuri R, Constantinides MG, Askenase MH, Sukumar M, Klebanoff CA, Eil RL, Hickman HD, Yu Z, Pan JH, et al. Oxygen Sensing by T Cells Establishes an Immunologically Tolerant Metastatic Niche. Cell. 2016;166(5):1117–31. e1114PubMedPubMedCentralCrossRef
127.
go back to reference Eveno C, Hainaud P, Rampanou A, Bonnin P, Bakhouche S, Dupuy E, Contreres JO, Pocard M. Proof of prometastatic niche induction by hepatic stellate cells. J Surg Res. 2015;194(2):496–504.PubMedCrossRef Eveno C, Hainaud P, Rampanou A, Bonnin P, Bakhouche S, Dupuy E, Contreres JO, Pocard M. Proof of prometastatic niche induction by hepatic stellate cells. J Surg Res. 2015;194(2):496–504.PubMedCrossRef
128.
go back to reference Nielsen SR, Quaranta V, Linford A, Emeagi P, Rainer C, Santos A, Ireland L, Sakai T, Sakai K, Kim YS, et al. Macrophage-secreted granulin supports pancreatic cancer metastasis by inducing liver fibrosis. Nature Cell biol. 2016;18(5):549–60.PubMedPubMedCentralCrossRef Nielsen SR, Quaranta V, Linford A, Emeagi P, Rainer C, Santos A, Ireland L, Sakai T, Sakai K, Kim YS, et al. Macrophage-secreted granulin supports pancreatic cancer metastasis by inducing liver fibrosis. Nature Cell biol. 2016;18(5):549–60.PubMedPubMedCentralCrossRef
129.
go back to reference Hu C-T, Guo L-L, Feng N, Zhang L, Zhou N, Ma L-L, Shen L, Tong G-H, Yan Q-W, Zhu S-J. MIF, secreted by human hepatic sinusoidal endothelial cells, promotes chemotaxis and outgrowth of colorectal cancer in liver prometastasis. Oncotarget. 2015;6(26):22,410.CrossRef Hu C-T, Guo L-L, Feng N, Zhang L, Zhou N, Ma L-L, Shen L, Tong G-H, Yan Q-W, Zhu S-J. MIF, secreted by human hepatic sinusoidal endothelial cells, promotes chemotaxis and outgrowth of colorectal cancer in liver prometastasis. Oncotarget. 2015;6(26):22,410.CrossRef
130.
go back to reference Marchio S, Soster M, Cardaci S, Muratore A, Bartolini A, Barone V, Ribero D, Monti M, Bovino P, Sun J, et al. A complex of alpha6 integrin and E-cadherin drives liver metastasis of colorectal cancer cells through hepatic angiopoietin-like 6. EMBO Mol Med. 2012;4(11):1156–75.PubMedPubMedCentralCrossRef Marchio S, Soster M, Cardaci S, Muratore A, Bartolini A, Barone V, Ribero D, Monti M, Bovino P, Sun J, et al. A complex of alpha6 integrin and E-cadherin drives liver metastasis of colorectal cancer cells through hepatic angiopoietin-like 6. EMBO Mol Med. 2012;4(11):1156–75.PubMedPubMedCentralCrossRef
131.
go back to reference Zuo Y, Ren S, Wang M, Liu B, Yang J, Kuai X, Lin C, Zhao D, Tang L, He F. Novel roles of liver sinusoidal endothelial cell lectin in colon carcinoma cell adhesion, migration and in-vivo metastasis to the liver. Gut. 2013;62(8):1169–78.PubMedCrossRef Zuo Y, Ren S, Wang M, Liu B, Yang J, Kuai X, Lin C, Zhao D, Tang L, He F. Novel roles of liver sinusoidal endothelial cell lectin in colon carcinoma cell adhesion, migration and in-vivo metastasis to the liver. Gut. 2013;62(8):1169–78.PubMedCrossRef
132.
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(7069):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(7069):820–7.PubMedPubMedCentralCrossRef
133.
go back to reference Wang H, Yu C, Gao X, Welte T, Muscarella AM, Tian L, Zhao H, Zhao Z, Du S, Tao J, et al. The osteogenic niche promotes early-stage bone colonization of disseminated breast cancer cells. Cancer cell. 2015;27(2):193–210.PubMedPubMedCentralCrossRef Wang H, Yu C, Gao X, Welte T, Muscarella AM, Tian L, Zhao H, Zhao Z, Du S, Tao J, et al. The osteogenic niche promotes early-stage bone colonization of disseminated breast cancer cells. Cancer cell. 2015;27(2):193–210.PubMedPubMedCentralCrossRef
134.
go back to reference Sottnik JL, Dai J, Zhang H, Campbell B, Keller ET. Tumor-induced pressure in the bone microenvironment causes osteocytes to promote the growth of prostate cancer bone metastases. Cancer Res. 2015;75(11):2151–8.PubMedPubMedCentralCrossRef Sottnik JL, Dai J, Zhang H, Campbell B, Keller ET. Tumor-induced pressure in the bone microenvironment causes osteocytes to promote the growth of prostate cancer bone metastases. Cancer Res. 2015;75(11):2151–8.PubMedPubMedCentralCrossRef
135.
go back to reference Zhou JZ, Riquelme MA, Gao X, Ellies LG, Sun LZ, Jiang JX. Differential impact of adenosine nucleotides released by osteocytes on breast cancer growth and bone metastasis. Oncogene. 2015;34(14):1831–42.PubMedCrossRef Zhou JZ, Riquelme MA, Gao X, Ellies LG, Sun LZ, Jiang JX. Differential impact of adenosine nucleotides released by osteocytes on breast cancer growth and bone metastasis. Oncogene. 2015;34(14):1831–42.PubMedCrossRef
136.
go back to reference de Oliveira Barros EG, Palumbo A Jr, Mello PLP, de Mattos RM, da Silva JH, Pontes B, Viana NB, do Amaral RF, FRS L, da Costa NM, et al. Clin Exp Metastasis. 2014;31(4):461–74.PubMedCrossRef de Oliveira Barros EG, Palumbo A Jr, Mello PLP, de Mattos RM, da Silva JH, Pontes B, Viana NB, do Amaral RF, FRS L, da Costa NM, et al. Clin Exp Metastasis. 2014;31(4):461–74.PubMedCrossRef
137.
go back to reference Klein A, Schwartz H, Sagi-Assif O, Meshel T, Izraely S, Ben Menachem S, Bengaiev R, Ben-Shmuel A, Nahmias C, Couraud PO, et al. Astrocytes facilitate melanoma brain metastasis via secretion of IL-23. J Pathol. 2015;236(1):116–27.PubMedCrossRef Klein A, Schwartz H, Sagi-Assif O, Meshel T, Izraely S, Ben Menachem S, Bengaiev R, Ben-Shmuel A, Nahmias C, Couraud PO, et al. Astrocytes facilitate melanoma brain metastasis via secretion of IL-23. J Pathol. 2015;236(1):116–27.PubMedCrossRef
138.
go back to reference Zhang L, Zhang S, Yao J, Lowery FJ, Zhang Q, Huang WC, Li P, Li M, Wang X, Zhang C, et al. Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth. Nature. 2015;527(7576):100–4.PubMedPubMedCentralCrossRef Zhang L, Zhang S, Yao J, Lowery FJ, Zhang Q, Huang WC, Li P, Li M, Wang X, Zhang C, et al. Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth. Nature. 2015;527(7576):100–4.PubMedPubMedCentralCrossRef
140.
go back to reference Raggi C, Mousa HS, Correnti M, Sica A, Invernizzi P. Cancer stem cells and tumor-associated macrophages: a roadmap for multitargeting strategies. Oncogene. 2016;35(6):671–82.PubMedCrossRef Raggi C, Mousa HS, Correnti M, Sica A, Invernizzi P. Cancer stem cells and tumor-associated macrophages: a roadmap for multitargeting strategies. Oncogene. 2016;35(6):671–82.PubMedCrossRef
141.
go back to reference Movahedi K, Laoui D, Gysemans C, Baeten M, Stange G, Van den Bossche J, Mack M, Pipeleers D, In’t Veld P, De Baetselier P, et al. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res. 2010;70(14):5728–39.PubMedCrossRef Movahedi K, Laoui D, Gysemans C, Baeten M, Stange G, Van den Bossche J, Mack M, Pipeleers D, In’t Veld P, De Baetselier P, et al. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res. 2010;70(14):5728–39.PubMedCrossRef
142.
go back to reference Lewis CE, Pollard JW. Distinct role of macrophages in different tumor microenvironments. Cancer Res. 2006;66(2):605–12.PubMedCrossRef Lewis CE, Pollard JW. Distinct role of macrophages in different tumor microenvironments. Cancer Res. 2006;66(2):605–12.PubMedCrossRef
143.
go back to reference Allavena P, Sica A, Solinas G, Porta C, Mantovani A. The inflammatory micro-environment in tumor progression: the role of tumor-associated macrophages. Crit Rev. Oncol Hematol. 2008;66(1):1–9.PubMedCrossRef Allavena P, Sica A, Solinas G, Porta C, Mantovani A. The inflammatory micro-environment in tumor progression: the role of tumor-associated macrophages. Crit Rev. Oncol Hematol. 2008;66(1):1–9.PubMedCrossRef
144.
go back to reference Margol AS, Robison NJ, Gnanachandran J, Hung LT, Kennedy RJ, Vali M, Dhall G, Finlay JL, Erdreich-Epstein A, Krieger MD, et al. Tumor-associated macrophages in SHH subgroup of medulloblastomas. Clin Cancer Res. 2015;21(6):1457–65.PubMedCrossRef Margol AS, Robison NJ, Gnanachandran J, Hung LT, Kennedy RJ, Vali M, Dhall G, Finlay JL, Erdreich-Epstein A, Krieger MD, et al. Tumor-associated macrophages in SHH subgroup of medulloblastomas. Clin Cancer Res. 2015;21(6):1457–65.PubMedCrossRef
145.
go back to reference Sarkar S, Doring A, Zemp FJ, Silva C, Lun X, Wang X, Kelly J, Hader W, Hamilton M, Mercier P, et al. Therapeutic activation of macrophages and microglia to suppress brain tumor-initiating cells. Nature neuroscience. 2014;17(1):46–55.PubMedCrossRef Sarkar S, Doring A, Zemp FJ, Silva C, Lun X, Wang X, Kelly J, Hader W, Hamilton M, Mercier P, et al. Therapeutic activation of macrophages and microglia to suppress brain tumor-initiating cells. Nature neuroscience. 2014;17(1):46–55.PubMedCrossRef
146.
147.
go back to reference Mestres JA, iMolins AB, Martinez LC, Lopez-Muniz JI, Gil EC, de Juan Ferre A, Del Barco Berron S, Perez YF, Mata JG, Palomo AG et al.: Defining the optimal sequence for the systemic treatment of metastatic breast cancer. Clin Transl Oncol 2017, 19(2):149–161. Mestres JA, iMolins AB, Martinez LC, Lopez-Muniz JI, Gil EC, de Juan Ferre A, Del Barco Berron S, Perez YF, Mata JG, Palomo AG et al.: Defining the optimal sequence for the systemic treatment of metastatic breast cancer. Clin Transl Oncol 2017, 19(2):149–161.
148.
go back to reference Weyden LV, Arends MJ, Campbell AD, Bald T, Wardle-Jones H, Griggs N, Velasco-Herrera MD, Tuting T, Sansom OJ, Karp NA, et al. Genome-wide in vivo screen identifies novel host regulators of metastatic colonization. Nature. 2017;541(7636):233–6.PubMedCrossRef Weyden LV, Arends MJ, Campbell AD, Bald T, Wardle-Jones H, Griggs N, Velasco-Herrera MD, Tuting T, Sansom OJ, Karp NA, et al. Genome-wide in vivo screen identifies novel host regulators of metastatic colonization. Nature. 2017;541(7636):233–6.PubMedCrossRef
150.
go back to reference Mowers E. Sharifi M, Macleod K. Autophagy in cancer metastasis. Oncogene. 2017;36:1619-1630. Mowers E. Sharifi M, Macleod K. Autophagy in cancer metastasis. Oncogene. 2017;36:1619-1630.
151.
152.
go back to reference Liu Z, Zhang B, Liu K, Ding Z, Hu X. Schisandrin B attenuates cancer invasion and metastasis via inhibiting epithelial-mesenchymal transition. PloS one. 2012;7(7):e40480.PubMedPubMedCentralCrossRef Liu Z, Zhang B, Liu K, Ding Z, Hu X. Schisandrin B attenuates cancer invasion and metastasis via inhibiting epithelial-mesenchymal transition. PloS one. 2012;7(7):e40480.PubMedPubMedCentralCrossRef
153.
go back to reference Pascual G, Avgustinova A, Mejetta S, Martin M, Castellanos A, Attolini CS, Berenguer A, Prats N, Toll A, Hueto JA, et al. Targeting metastasis-initiating cells through the fatty acid receptor CD36. Nature. 2017;541(7635):41–5.PubMedCrossRef Pascual G, Avgustinova A, Mejetta S, Martin M, Castellanos A, Attolini CS, Berenguer A, Prats N, Toll A, Hueto JA, et al. Targeting metastasis-initiating cells through the fatty acid receptor CD36. Nature. 2017;541(7635):41–5.PubMedCrossRef
154.
go back to reference Wirth M, Heidenreich A, Gschwend JE, Gil T, Zastrow S, Laniado M, Gerloff J, Zuhlsdorf M, Mordenti G, Uhl W, et al. A multicenter phase 1 study of EMD 525797 (DI17E6), a novel humanized monoclonal antibody targeting alphav integrins, in progressive castration-resistant prostate cancer with bone metastases after chemotherapy. Eur Urol. 2014;65(5):897–904.PubMedCrossRef Wirth M, Heidenreich A, Gschwend JE, Gil T, Zastrow S, Laniado M, Gerloff J, Zuhlsdorf M, Mordenti G, Uhl W, et al. A multicenter phase 1 study of EMD 525797 (DI17E6), a novel humanized monoclonal antibody targeting alphav integrins, in progressive castration-resistant prostate cancer with bone metastases after chemotherapy. Eur Urol. 2014;65(5):897–904.PubMedCrossRef
155.
go back to reference Rosenberg JE, Bambury RM, Van Allen EM, Drabkin HA, Lara PN Jr, Harzstark AL, Wagle N, Figlin RA, Smith GW, Garraway LA, et al. A phase II trial of AS1411 (a novel nucleolin-targeted DNA aptamer) in metastatic renal cell carcinoma. Invest New Drugs. 2014;32(1):178–87.PubMedCrossRef Rosenberg JE, Bambury RM, Van Allen EM, Drabkin HA, Lara PN Jr, Harzstark AL, Wagle N, Figlin RA, Smith GW, Garraway LA, et al. A phase II trial of AS1411 (a novel nucleolin-targeted DNA aptamer) in metastatic renal cell carcinoma. Invest New Drugs. 2014;32(1):178–87.PubMedCrossRef
156.
go back to reference Forero-Torres A, Infante JR, Waterhouse D, Wong L, Vickers S, Arrowsmith E, He AR, Hart L, Trent D, Wade J, et al. Phase 2, multicenter, open-label study of tigatuzumab (CS-1008), a humanized monoclonal antibody targeting death receptor 5, in combination with gemcitabine in chemotherapy-naive patients with unresectable or metastatic pancreatic cancer. Cancer Med. 2013;2(6):925–32.PubMedPubMedCentralCrossRef Forero-Torres A, Infante JR, Waterhouse D, Wong L, Vickers S, Arrowsmith E, He AR, Hart L, Trent D, Wade J, et al. Phase 2, multicenter, open-label study of tigatuzumab (CS-1008), a humanized monoclonal antibody targeting death receptor 5, in combination with gemcitabine in chemotherapy-naive patients with unresectable or metastatic pancreatic cancer. Cancer Med. 2013;2(6):925–32.PubMedPubMedCentralCrossRef
157.
go back to reference Andersson Y, Engebraaten O, Juell S, Aamdal S, Brunsvig P, Fodstad O, Dueland S. Phase I trial of EpCAM-targeting immunotoxin MOC31PE, alone and in combination with cyclosporin. Br J Cancer. 2015;113(11):1548–55.PubMedPubMedCentralCrossRef Andersson Y, Engebraaten O, Juell S, Aamdal S, Brunsvig P, Fodstad O, Dueland S. Phase I trial of EpCAM-targeting immunotoxin MOC31PE, alone and in combination with cyclosporin. Br J Cancer. 2015;113(11):1548–55.PubMedPubMedCentralCrossRef
158.
go back to reference Starodub AN, Ocean AJ, Shah MA, Guarino MJ, Picozzi VJ Jr, Vahdat LT, Thomas SS, Govindan SV, Maliakal PP, Wegener WA, et al. First-in-Human Trial of a Novel Anti-Trop-2 Antibody-SN-38 Conjugate, Sacituzumab Govitecan, for the Treatment of Diverse Metastatic Solid Tumors. Clin Cancer Res. 2015;21(17):3870–8.PubMedPubMedCentralCrossRef Starodub AN, Ocean AJ, Shah MA, Guarino MJ, Picozzi VJ Jr, Vahdat LT, Thomas SS, Govindan SV, Maliakal PP, Wegener WA, et al. First-in-Human Trial of a Novel Anti-Trop-2 Antibody-SN-38 Conjugate, Sacituzumab Govitecan, for the Treatment of Diverse Metastatic Solid Tumors. Clin Cancer Res. 2015;21(17):3870–8.PubMedPubMedCentralCrossRef
160.
go back to reference Hosseini H, Obradovic MM, Hoffmann M, Harper KL, Sosa MS, Werner-Klein M, Nanduri LK, Werno C, Ehrl C, Maneck M, et al. Early dissemination seeds metastasis in breast cancer. Nature. 2016; Hosseini H, Obradovic MM, Hoffmann M, Harper KL, Sosa MS, Werner-Klein M, Nanduri LK, Werno C, Ehrl C, Maneck M, et al. Early dissemination seeds metastasis in breast cancer. Nature. 2016;
161.
go back to reference Harper KL, Sosa MS, Entenberg D, Hosseini H, Cheung JF, Nobre R, Avivar-Valderas A, Nagi C, Girnius N, Davis RJ, et al. Mechanism of early dissemination and metastasis in Her2+ mammary cancer. Nature. 2016; Harper KL, Sosa MS, Entenberg D, Hosseini H, Cheung JF, Nobre R, Avivar-Valderas A, Nagi C, Girnius N, Davis RJ, et al. Mechanism of early dissemination and metastasis in Her2+ mammary cancer. Nature. 2016;
162.
go back to reference Welt S, Divgi CR, Scott AM, Garin-Chesa P, Finn RD, Graham M, Carswell EA, Cohen A, Larson SM, Old LJ. Antibody targeting in metastatic colon cancer: a phase I study of monoclonal antibody F19 against a cell-surface protein of reactive tumor stromal fibroblasts. J Clinical Oncol. 1994;12(6):1193–203.CrossRef Welt S, Divgi CR, Scott AM, Garin-Chesa P, Finn RD, Graham M, Carswell EA, Cohen A, Larson SM, Old LJ. Antibody targeting in metastatic colon cancer: a phase I study of monoclonal antibody F19 against a cell-surface protein of reactive tumor stromal fibroblasts. J Clinical Oncol. 1994;12(6):1193–203.CrossRef
163.
go back to reference Grothey A, Cutsem EV, Sobrero A, Siena S, Falcone A, Ychou M, Humblet Y, Bouché O, Mineur L, Barone C, et al. Regorafenib monotherapy for previously treated metastatic colorectal cancer (CORRECT): an international, multicentre, randomised, placebo-controlled, phase 3 trial. The Lancet. 2013;381(9863):303–12.CrossRef Grothey A, Cutsem EV, Sobrero A, Siena S, Falcone A, Ychou M, Humblet Y, Bouché O, Mineur L, Barone C, et al. Regorafenib monotherapy for previously treated metastatic colorectal cancer (CORRECT): an international, multicentre, randomised, placebo-controlled, phase 3 trial. The Lancet. 2013;381(9863):303–12.CrossRef
164.
go back to reference Borsig L, Wolf MJ, Roblek M, Lorentzen A, Heikenwalder M. Inflammatory chemokines and metastasis—tracing the accessory. Oncogene. 2014;33(25):3217–24.PubMedCrossRef Borsig L, Wolf MJ, Roblek M, Lorentzen A, Heikenwalder M. Inflammatory chemokines and metastasis—tracing the accessory. Oncogene. 2014;33(25):3217–24.PubMedCrossRef
165.
166.
go back to reference Plaks V, Kong N, Werb Z. The cancer stem cell niche: how essential is the niche in regulating stemness of tumor cells? Cell stem cell. 2015;16(3):225–38.PubMedPubMedCentralCrossRef Plaks V, Kong N, Werb Z. The cancer stem cell niche: how essential is the niche in regulating stemness of tumor cells? Cell stem cell. 2015;16(3):225–38.PubMedPubMedCentralCrossRef
167.
go back to reference Liu Y, Cao X. Characteristics and Significance of the Pre-metastatic Niche. Cancer cell. 2016;30(5):668–81.PubMedCrossRef Liu Y, Cao X. Characteristics and Significance of the Pre-metastatic Niche. Cancer cell. 2016;30(5):668–81.PubMedCrossRef
168.
go back to reference Qian BZ, Zhang H, Li J, He T, Yeo EJ, Soong DY, Carragher NO, Munro A, Chang A, Bresnick AR, et al. FLT1 signaling in metastasis-associated macrophages activates an inflammatory signature that promotes breast cancer metastasis. J Exp Med. 2015;212(9):1433–48.PubMedPubMedCentralCrossRef Qian BZ, Zhang H, Li J, He T, Yeo EJ, Soong DY, Carragher NO, Munro A, Chang A, Bresnick AR, et al. FLT1 signaling in metastasis-associated macrophages activates an inflammatory signature that promotes breast cancer metastasis. J Exp Med. 2015;212(9):1433–48.PubMedPubMedCentralCrossRef
169.
go back to reference Lee JW, Shahzad MM, Lin YG, Armaiz-Pena G, Mangala LS, Han HD, Kim HS, Nam EJ, Jennings NB, Halder J et al.: Surgical stress promotes tumor growth in ovarian carcinoma. Clin Cancer Res 2009, 15(8):Clin Cancer Res–2702. Lee JW, Shahzad MM, Lin YG, Armaiz-Pena G, Mangala LS, Han HD, Kim HS, Nam EJ, Jennings NB, Halder J et al.: Surgical stress promotes tumor growth in ovarian carcinoma. Clin Cancer Res 2009, 15(8):Clin Cancer Res–2702.
170.
go back to reference Gul N, Bogels M, Grewal S, van der Meer AJ, Rojas LB, Fluitsma DM, van den Tol MP, Hoeben KA, van Marle J, de Vries HE, et al. Surgery-induced reactive oxygen species enhance colon carcinoma cell binding by disrupting the liver endothelial cell lining. Gut. 2011;60(8):1076–86.PubMedCrossRef Gul N, Bogels M, Grewal S, van der Meer AJ, Rojas LB, Fluitsma DM, van den Tol MP, Hoeben KA, van Marle J, de Vries HE, et al. Surgery-induced reactive oxygen species enhance colon carcinoma cell binding by disrupting the liver endothelial cell lining. Gut. 2011;60(8):1076–86.PubMedCrossRef
171.
go back to reference Peeters CF, de Waal RM, Wobbes T, Westphal JR, Ruers TJ. Outgrowth of human liver metastases after resection of the primary colorectal tumor: a shift in the balance between apoptosis and proliferation. Int J Cancer. 2006;119(6):1249–53.PubMedCrossRef Peeters CF, de Waal RM, Wobbes T, Westphal JR, Ruers TJ. Outgrowth of human liver metastases after resection of the primary colorectal tumor: a shift in the balance between apoptosis and proliferation. Int J Cancer. 2006;119(6):1249–53.PubMedCrossRef
172.
173.
go back to reference Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, Molina DA, Salcedo R, Back T, Cramer S. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science. 2013;342(6161):967–70.PubMedCrossRef Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, Molina DA, Salcedo R, Back T, Cramer S. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science. 2013;342(6161):967–70.PubMedCrossRef
174.
go back to reference Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CP. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015;350(6264):1079–84.PubMedPubMedCentralCrossRef Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CP. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015;350(6264):1079–84.PubMedPubMedCentralCrossRef
175.
go back to reference Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, Benyamin FW, Lei YM, Jabri B, Alegre M-L. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti–PD-L1 efficacy. Science. 2015;350(6264):1084–9.PubMedPubMedCentralCrossRef Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, Benyamin FW, Lei YM, Jabri B, Alegre M-L. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti–PD-L1 efficacy. Science. 2015;350(6264):1084–9.PubMedPubMedCentralCrossRef
176.
go back to reference Weng CJ, Yen GC. Chemopreventive effects of dietary phytochemicals against cancer invasion and metastasis: phenolic acids, monophenol, polyphenol, and their derivatives. Cancer Treat Rev. 2012;38(1):76–87.PubMedCrossRef Weng CJ, Yen GC. Chemopreventive effects of dietary phytochemicals against cancer invasion and metastasis: phenolic acids, monophenol, polyphenol, and their derivatives. Cancer Treat Rev. 2012;38(1):76–87.PubMedCrossRef
177.
go back to reference Ho VW, Hamilton MJ, Dang NH, Hsu BE, Adomat HH, Guns ES, Weljie A, Samudio I, Bennewith KL, Krystal G. A low carbohydrate, high protein diet combined with celecoxib markedly reduces metastasis. Carcinogenesis. 2014;35(10):2291–9.PubMedPubMedCentralCrossRef Ho VW, Hamilton MJ, Dang NH, Hsu BE, Adomat HH, Guns ES, Weljie A, Samudio I, Bennewith KL, Krystal G. A low carbohydrate, high protein diet combined with celecoxib markedly reduces metastasis. Carcinogenesis. 2014;35(10):2291–9.PubMedPubMedCentralCrossRef
178.
go back to reference Matsuoka T, Adair JE, Lih FB, Hsi LC, Rubino M, Eling TE, Tomer KB, Yashiro M, Hirakawa K, Olden K, et al. Elevated dietary linoleic acid increases gastric carcinoma cell invasion and metastasis in mice. Br J Cancer. 2010;103(8):1182–91.PubMedPubMedCentralCrossRef Matsuoka T, Adair JE, Lih FB, Hsi LC, Rubino M, Eling TE, Tomer KB, Yashiro M, Hirakawa K, Olden K, et al. Elevated dietary linoleic acid increases gastric carcinoma cell invasion and metastasis in mice. Br J Cancer. 2010;103(8):1182–91.PubMedPubMedCentralCrossRef
179.
go back to reference Casey SC, Vaccari M, Al-Mulla F, Al-Temaimi R, Amedei A, Barcellos-Hoff MH, Brown DG, Chapellier M, Christopher J, Curran CS, et al. The effect of environmental chemicals on the tumor microenvironment. Carcinogenesis. 2015;36(Suppl 1):S160–83.PubMedPubMedCentralCrossRef Casey SC, Vaccari M, Al-Mulla F, Al-Temaimi R, Amedei A, Barcellos-Hoff MH, Brown DG, Chapellier M, Christopher J, Curran CS, et al. The effect of environmental chemicals on the tumor microenvironment. Carcinogenesis. 2015;36(Suppl 1):S160–83.PubMedPubMedCentralCrossRef
180.
go back to reference Weigelt B, Peterse JL, van ‘t Veer LJ: Breast cancer metastasis: markers and models. Nat Rev Cancer 2005, 5(8):591–602. Weigelt B, Peterse JL, van ‘t Veer LJ: Breast cancer metastasis: markers and models. Nat Rev Cancer 2005, 5(8):591–602.
181.
go back to reference Strilic B, Yang L, Albarran-Juarez J, Wachsmuth L, Han K, Muller UC, Pasparakis M, Offermanns S. Tumour-cell-induced endothelial cell necroptosis via death receptor 6 promotes metastasis. Nature. 2016;536(7615):215–8.PubMedCrossRef Strilic B, Yang L, Albarran-Juarez J, Wachsmuth L, Han K, Muller UC, Pasparakis M, Offermanns S. Tumour-cell-induced endothelial cell necroptosis via death receptor 6 promotes metastasis. Nature. 2016;536(7615):215–8.PubMedCrossRef
182.
go back to reference Bentolila LA, Prakash R, Mihic-Probst D, Wadehra M, Kleinman HK, Carmichael TS, Peault B, Barnhill RL, Lugassy C. Imaging of Angiotropism/Vascular Co-Option in a Murine Model of Brain Melanoma: Implications for Melanoma Progression along Extravascular Pathways. Sci Rep. 2016;6:23,834.CrossRef Bentolila LA, Prakash R, Mihic-Probst D, Wadehra M, Kleinman HK, Carmichael TS, Peault B, Barnhill RL, Lugassy C. Imaging of Angiotropism/Vascular Co-Option in a Murine Model of Brain Melanoma: Implications for Melanoma Progression along Extravascular Pathways. Sci Rep. 2016;6:23,834.CrossRef
183.
go back to reference Edlund M, Sung SY, Chung LW. Modulation of prostate cancer growth in bone microenvironments. J Cell Biochem. 2004;91(4):686–705.PubMedCrossRef Edlund M, Sung SY, Chung LW. Modulation of prostate cancer growth in bone microenvironments. J Cell Biochem. 2004;91(4):686–705.PubMedCrossRef
184.
go back to reference Smith MR, Saad F, Coleman R, Shore N, Fizazi K, Tombal B, Miller K, Sieber P, Karsh L, Damião R, et al. Denosumab and bone-metastasis-free survival in men with castration-resistant prostate cancer: results of a phase 3, randomised, placebo-controlled trial. The Lancet. 2012;379(9810):39–46.CrossRef Smith MR, Saad F, Coleman R, Shore N, Fizazi K, Tombal B, Miller K, Sieber P, Karsh L, Damião R, et al. Denosumab and bone-metastasis-free survival in men with castration-resistant prostate cancer: results of a phase 3, randomised, placebo-controlled trial. The Lancet. 2012;379(9810):39–46.CrossRef
186.
go back to reference Tirosh I, Izar B, Prakadan SM, Wadsworth MH, Treacy D, Trombetta JJ, Rotem A, Rodman C, Lian C, Murphy G. Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq. Science. 2016;352(6282):189–96.PubMedPubMedCentralCrossRef Tirosh I, Izar B, Prakadan SM, Wadsworth MH, Treacy D, Trombetta JJ, Rotem A, Rodman C, Lian C, Murphy G. Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq. Science. 2016;352(6282):189–96.PubMedPubMedCentralCrossRef
187.
go back to reference Ritsma L, Steller EJ, Beerling E, Loomans CJ, Zomer A, Gerlach C, Vrisekoop N, Seinstra D, van Gurp L, Schafer R, et al. Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis. Sci Transl Med. 2012;4(158):158ra145.PubMedCrossRef Ritsma L, Steller EJ, Beerling E, Loomans CJ, Zomer A, Gerlach C, Vrisekoop N, Seinstra D, van Gurp L, Schafer R, et al. Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis. Sci Transl Med. 2012;4(158):158ra145.PubMedCrossRef
189.
go back to reference Guo S, Diep D, Plongthongkum N, Fung HL, Zhang K, Zhang K. Identification of methylation haplotype blocks aids in deconvolution of heterogeneous tissue samples and tumor tissue-of-origin mapping from plasma DNA. Nat Genet. 2017;49(4):635–42.PubMedPubMedCentralCrossRef Guo S, Diep D, Plongthongkum N, Fung HL, Zhang K, Zhang K. Identification of methylation haplotype blocks aids in deconvolution of heterogeneous tissue samples and tumor tissue-of-origin mapping from plasma DNA. Nat Genet. 2017;49(4):635–42.PubMedPubMedCentralCrossRef
190.
go back to reference Huh D, Matthews BD, Mammoto A, Montoya-Zavala M, Hsin HY, Ingber DE. Reconstituting organ-level lung functions on a chip. Science. 2010;328(5986):1662–8.PubMedCrossRef Huh D, Matthews BD, Mammoto A, Montoya-Zavala M, Hsin HY, Ingber DE. Reconstituting organ-level lung functions on a chip. Science. 2010;328(5986):1662–8.PubMedCrossRef
191.
go back to reference Xu Z, Li E, Guo Z, Yu R, Hao H, Xu Y, Sun Z, Li X, Lyu J, Wang Q. Design and Construction of a Multi-Organ Microfluidic Chip Mimicking the in vivo Microenvironment of Lung Cancer Metastasis. ACS Appl Mater Interfaces. 2016;8(39):25,840–7.CrossRef Xu Z, Li E, Guo Z, Yu R, Hao H, Xu Y, Sun Z, Li X, Lyu J, Wang Q. Design and Construction of a Multi-Organ Microfluidic Chip Mimicking the in vivo Microenvironment of Lung Cancer Metastasis. ACS Appl Mater Interfaces. 2016;8(39):25,840–7.CrossRef
192.
go back to reference Ebrahimkhani MR, Neiman JA, Raredon MS, Hughes DJ, Griffith LG. Bioreactor technologies to support liver function in vitro. Adv Drug Deliv Rev. 2014;69–70:132–57.PubMedCrossRef Ebrahimkhani MR, Neiman JA, Raredon MS, Hughes DJ, Griffith LG. Bioreactor technologies to support liver function in vitro. Adv Drug Deliv Rev. 2014;69–70:132–57.PubMedCrossRef
193.
go back to reference Lancaster MA, Renner M, Martin CA, Wenzel D, Bicknell LS, Hurles ME, Homfray T, Penninger JM, Jackson AP, Knoblich JA. Cerebral organoids model human brain development and microcephaly. Nature. 2013;501(7467):373–9.PubMedCrossRef Lancaster MA, Renner M, Martin CA, Wenzel D, Bicknell LS, Hurles ME, Homfray T, Penninger JM, Jackson AP, Knoblich JA. Cerebral organoids model human brain development and microcephaly. Nature. 2013;501(7467):373–9.PubMedCrossRef
Metadata
Title
Factors involved in cancer metastasis: a better understanding to “seed and soil” hypothesis
Authors
Qiang Liu
Hongfei Zhang
Xiaoli Jiang
Caiyun Qian
Zhuoqi Liu
Daya Luo
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Molecular Cancer / Issue 1/2017
Electronic ISSN: 1476-4598
DOI
https://doi.org/10.1186/s12943-017-0742-4

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