The role of tumour stroma in colorectal cancer invasion and metastasis

Cancers

Volumn 3, Issue 2, 2011, Pages 2160-2168

  Conti, John ^a   Thomas, Gareth ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Colorectal cancer; Myofibroblasts; Stroma; Tumour microenvironment

Indexed keywords

ARTICLE; CANCER ADJUVANT THERAPY; CANCER GROWTH; CANCER INVASION; CANCER MORTALITY; CANCER RECURRENCE; CANCER SURVIVAL; CARCINOGENESIS; COLORECTAL CANCER; HUMAN; IMMUNE RESPONSE; LIVER METASTASIS; LUNG METASTASIS; MOLECULAR MECHANICS; MYOFIBROBLAST; PROGNOSIS; STROMA; TUMOR MICROENVIRONMENT;

EID: 79959739151     PISSN: None     EISSN: 20726694     Source Type: Journal    
DOI: 10.3390/cancers3022160     Document Type: Article

References (54)

1. Office for National Statistics. Cancer Statistics Registrations: Registrations of Cancer Diagnosed in 2007; Series MB1 No. 38; England, 2010.
2. Coussens, L.M.; Werb, Z. Inflammation and cancer. Nature 2002, 420, 860-867.
3. Tlsty, T.D.; Hein, P.W. Know thy neighbour: Stromal cells can contribute oncogenic signals. Curr. Opin. Genet. Dev. 2001, 11, 54-59.
4. Liotta, L.A.; Kohn, E.C. The microenvironment of the tumour-host interface. Nature 2001, 411, 375-379.
5. De Wever, O.; Demetter, P.; Mareel, M.; Bracke, M. Stromal myofibroblasts are drivers of invasive cancer growth. Int. J. Cancer 2008, 123, 2229-2238.
6. Tsujino, T.; Seshimo, I.; Yamamoto, H.; Ngan, C.Y.; Ezumi, K.; Takemasa, I.; Ikeda, M.; Sekimoto, M.; Matsuura, N.; Monden, M. Stromal myofibroblasts predict disease recurrence for colorectal cancer. Clin. Cancer Res. 2007, 13, 2082-2090.
7. Kellermann, M.G.; Sobral, L.M.; da Silva, S.D.; Zecchin, K.G.; Graner, E.; Lopes, M.A.; Nishimoto, I.; Kowalski, L.P.; Coletta, R.D. Myofibroblasts in the stroma of oral squamous cell carcinoma are associated with poor prognosis. Histopathology 2007, 51, 849-853.
8. Surowiak, P.; Murawa, D.; Materna, V.; Maciejczyk, A.; Pudelko, M.; Ciesla, S.; Breborowicz, J.; Murawa, P.; Zabel, M.; Dietel, M.; et al. Occurence of stromal myofibroblasts in the invasive ductal breast cancer tissue is an unfavourable prognostic factor. Anticancer Res. 2007, 27, 2917-2924.
9. Moutasim, K.A.; Jenei, V.; Sapienza, K.; Marsh, D.; Weinreb, P.H.; Violette, S.M.; Lewis, M.P.; Marshall, J.F.; Fortune, F.; Tilakaratne, W.M.; et al. Betel-derived alkaloid up-regulates keratinocyte alphavbeta6 integrin expression and promotes oral submucous fibrosis. J. Pathol. 2011, 223, 366-377.
10. De Wever, O.; Nguyen, Q.D.; Van Hoorde, L.; Bracke, M.; Bruyneel, E.; Gespach, C.; Mareel, M. Tenascin-C and SF/HGF produced by myofibroblasts in vitro provide convergent pro-invasive signals to human colon cancer cells through RhoA and Rac. FASEB J. 2004, 18, 1016-1018.
11. Andersson-Sjöland, A.; de Alba, C.G.; Nihlberg, K.; Becerril, C.; Ramírez, R.; Pardo, A.; Westergren-Thorsson, G.; Selman, M. Fibrocytes are a potential source of lung fibroblasts in idiopathic pulmonary fibrosis. Int. J. Biochem. Cell Biol. 2008, 40, 2129-2140.
12. Saigusa, S.; Toiyama, Y.; Tanaka, K.; Yokoe, T.; Okugawa, Y.; Kawamoto, A.; Yasuda, H.; Inoue, Y.; Miki, C.; Kusunoki, M. Stromal CXCR4 and CXCL12 expression is associated with distant recurrence and poor prognosis in rectal cancer after chemoradiotherapy. Ann. Surg. Oncol. 2010, 17, 2051-2058.
13. Radisky, D.C.; Kenny, P.A.; Bissell, M.J. Fibrosis and cancer: Do myofibroblasts come also from epithelial cells via EMT? J. Cell. Biochem. 2007, 101, 830-839.
14. Xu, J.; Lamouille, S.; Derynck, R. TGF-beta-induced epithelial to mesenchymal transition. Cell Res. 2009.19, 156-172.
15. Van Zijl, F.; Mair, M.; Csiszar, A.; Schneller, D.; Zulehner, G.; Huber, H.; Eferl, R.; Beug, H.; Dolznig, H.; Mikulits, W. Hepatic tumor-stroma cross-talk guides epithelial to mesenchymal transition at the tumour edge. Oncogene 2009, 28, 4022-4033.
16. Wakefield, L.M.; Roberts, A.B. TGF-beta signaling: Positive and negative effects on tumorigenesis. Curr. Opin. Genet. Dev. 2002, 12, 22-29.
17. Sheppard, D. Transforming growth factor beta: A central modulator of pulmonary and airway inflammation and fibrosis. Proc. Am. Thorac. Soc. 2006, 3, 413-417.
18. Safina, A.F.; Varga, A.E.; Bianchi, A.; Zheng, Q.; Kunnev, D.; Liang, P.; Bakin, A.V. Ras alters epithelial-mesenchymal transition in response to TGFbeta by reducing actin fibers and cell-matrix adhesion. Cell Cycle 2009, 8, 284-298.
19. Pohl, M.; Radacz, Y.; Pawlik, N.; Schoeneck, A.; Baldus, S.E.; Munding, J.; Schmiegel, W.; Schwarte-Waldhoff, I.; Reinacher-Schick, A. SMAD4 mediates mesenchymal-epithelial reversion in SW480 colon carcinoma cells. Anticancer Res. 2010, 30, 2603-2613.
20. Pino, M.S.; Kikuchi, H.; Zeng, M.; Herraiz, M.T.; Sperduti, I.; Berger, D.; Park, D.Y.; Iafrate, A.J.; Zukerberg, L.R.; Chung, D.C. Epithelial to mesenchymal transition is impaired in colon cancer cells with microsatellite instability. Gastroenterology 2010, 138, 1406-1417.
21. Kirkland, S.C. Type I collagen inhibits differentiation and promotes a stem cell-like phenotype in human colorectal carcinoma cells. Br. J. Cancer 2010, 101, 320-326.
22. Bates, R.C.; Bellovin, D.I.; Brown, C.; Maynard, E.; Wu, B.; Kawakatsu, H.; Sheppard, D.; Oettgen, P.; Mercurio, A.M. Transcriptional activation of integrin beta6 during the epithelial-mesenchymal transition defines a novel prognostic indicator of aggressive colon carcinoma. J. Clin. Invest. 2005, 115, 339-347.
23. Serini, G.; Bochaton-Piallat, M.L.; Ropraz, P.; Geinoz, A.; Borsi, L.; Zardi, L.; Gabbiani, G. The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-beta1. J. Cell. Biol. 1998, 10, 873-881.
24. Lenga, Y.; Koh, A.; Perera, A.S.; McCulloch, C.A.; Sodek, J.; Zohar, R. Osteopontin expression is required for myofibroblast differentiation. Circ. Res. 2008, 102, 319-327.
25. Valcz, G.; Sipos, F.; Krenács, T.; Molnár, J.; Patai, A.V.; Leiszter, K.; Tóth, K.; Solymosi, N.; Galamb, O.; Molnár, B, et al. Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-alpha. Science 2010, 330, 827-830.
26. Imano, M.; Okuno, K.; Itoh, T.; Ishimaru, E.; Satou, T.; Shiozaki, H. Increased osteopontin positive macrophage expression in colorectal cancer stroma with synchronous liver metastasis. World J. Surg. 2010, 34, 1930-1936.
27. El Kahi, C.G.; Atiyeh, B.S.; Abdallah, H.; Hussein, I.; Jurjus, R.; Dibo, S.A.; Jurjus, A.; Jurjus, A. Modulation of wound contracture alpha-smooth muscle actin and multispecific vitronectin receptor integrin alphavbeta3 in the rabbit's experimental model. Int. Wound J. 2009, 6, 214-224.
28. Ding, Q.; Gladson, C.L.; Wu, H.; Hayasaka, H.; Olman, M.A. Focal adhesion kinase (FAK)-related non-kinase inhibits myofibroblast differentiation through differential MAPK activation in a FAK-dependent manner. J. Biol. Chem. 2008, 283, 26839-26849.
29. Lygoe, K.A.; Wall, I.; Stephens, P.; Lewis, M.P. Role of vitronectin and fibronectin receptors in oral mucosal and dermal myofibroblast differentiation. Biol. Cell 2007, 99, 601-614.
30. Yamasaki, M.; Kang, H.R.; Homer, R.J.; Chapoval, S.P.; Cho, S.J.; Lee, B.J.; Elias, J.A.; Lee, C.G. P21 regulates TGF-beta1-induced pulmonary responses via a TNF-alpha-signaling pathway. Am. J. Respir. Cell Mol. Biol. 2008, 38, 346-353.
31. Webber, J.; Jenkins, R.H.; Meran, S.; Phillips, A.; Steadman, R. Modulation of TGFbeta1-dependent myofibroblast differentiation by hyaluronan. Am. J. Pathol. 2009, 175, 148-160.
32. Bharadwaj, A.G.; Kovar, J.L.; Loughman, E.; Elowsky, C.; Oakley, G.G.; Simpson, M.A. Spontaneous metastasis of prostate cancer is promoted by excess hyaluornan synthesis and processing. Am. J. Path. 2009, 174, 1027-1036.
33. Lugli, A.; Zlobec, I.; Günthert, U.; Minoo, P.; Baker, K.; Tornillo, L.; Terracciano, L.; Jass, J.R. Overexpression of the receptor for hyaluronic acid mediated motility is an independent adverse prognostic factor in colorectal cancer. Modern Pathol. 2006, 19, 1302-1309.
34. Surowiak, P.; Murawa, D.; Materna, V.; Maciejczyk, A.; Pudelko, M.; Ciesla, S.; Breborowicz, J.; Murawa, P.; Zabel, M.; Dietel, M.; et al. Occurence of stromal myofibroblasts in the invasive ductal breast cancer tissue is an unfavourable prognostic factor. Anticancer Res. 2007, 27, 2917-2924.
35. Marsh, D.; Suchak, K.; Moutasim, K.A.; Vallath, S.; Hopper, C.; Jerjes, W.; Upile, T.; Kalavrezos, N.; Violette, S.M.; Weinreb, P.H.; et al. Stromal features are predictive of disease mortality in oral cancer patients. J. Pathol. 2011, 223, 470-481.
36. Li, F.Y.; Lai, M.D. Colorectal cancer, one entity or three. J. Zhejiang Univ. Sci. B 2009, 10, 219-229.
37. Ueno, H.; Jones, A.M.; Wilkinson, K.H.; Jass, J.R.; Talbot, I.C. Histological categoristaion of fibrotic cancer stroma in advanced rectal cancer. Gut 2004, 53, 581-586.
38. Cui, G.; Yuan, A.; Vonen, B.; Florholmen, J. Progressive cellular response in the lamina propria of the colorectal adenoma-Carcinoma sequence. Histopathology 2009, 54, 550-560.
39. Marsh, D.; Dickinson, S.; Neill, G.W.; Marshall, J.F.; Hart, I.R.; Thomas, G.J. αvβ6 integrin promotes the invasion of morphoeic basal cell carcinoma through stromal modulation. Cancer Res. 2008, 68, 3295-3303.
40. Svagzyds, S.; Lesauskaite, V.; Pangonyte, D.; Saladzinskas, Z.; Tamelis, A.; Pavalkis, D. Matrix metalloproteinase-9 is a prognostic marker to predict survival of patients who underwent surgery due to rectal carcinoma. Tohoku J. Exp. Med. 2011, 223, 67-73.
41. Gaggioli, C.; Hooper, S.; Hidalgo-Carcedo, C.; Grosse, R.; Marshall, J.F.; Harrington, K.; Sahai, E. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat. Cell. Biol. 2007, 9, 1392-1400.
42. Sis, B.; Sarioglu, S.; Sokmen, S.; Sakar, M.; Kupelioglu, A.; Fuzun, M. Desmoplasia measured by computer assisted image analysis: an independent prognostic marker in colorectal carcinoma. J. Clin. Path. 2005, 58, 32-38.
43. Crispino, P.; De Toma, G.; Ciardi, A.; Bella, A.; Rivera, M.; Cavallaro, G.; Polistena, A; Fornari, F.; Unim, H.; Pica, R.; et al. Role of desmoplasia in recurrence of stage II colorectal cancer within 5 years after surgery and therapeutic implication. Cancer Invest. 2008, 26, 419-425.
44. Yoong, K.F.; Afford, S.C.; Randhawa, S.; Hubscher, S.G.; Adams, D.H. Fas/Fas ligand interaction in human colorectal hepatic metastases: A mechanism of hepatocyte destruction to facilitate local tumor invasion. Am. J. Pathol. 1999, 154, 693-703.
45. Conti, J.A.; Kendall, T.J.; Bateman, A.; Armstrong, T.A.; Papa-Adams, A.; Xu, Q.; Packham, G.; Primrose, J.N.; Benyon, R.C.; Iredale, J.P. The desmoplastic reaction surrounding hepatic colorectal adenocarcinoma metastases aids tumor growth and survival via alphav integrin ligation. Clin. Cancer Res. 2008, 14, 6405-6413.
46. Monnier, Y.; Farmer, P.; Bieler, G.; Imaizumi, N.; Sengstag, T.; Alghisi, G.C.; Stehle, J.C.; Ciarloni, L.; Andrejevic-Blant, S.; Moeckli, R.; et al. CYR61 and alphaVbeta5 integrin cooperate to promote invasion and metastasis of tumors growing in pre-irradiated stroma. Cancer Res. 2008, 68, 7323-7331.
47. Yang, G.Y.; Xu, K.S.; Pan, Z.Q.; Zhang, Z.Y.; Mi, Y.T.; Wang, J.S.; Chen, R.; Niu, J. Integrin alphavbeta 6 mediates the potential for colon cancer cells to colonize in and metastasize to the liver. Cancer Sci. 2008, 99, 879-887.
48. He, J.M.; Wang, F.C.; Qi, H.B.; Li, Y.; Liang, H.J. Down-regulation of alphav integrin by retroviral delivery of small interfering RNA reduces multicellular resistance of HT29. Cancer Lett. 2009, 284, 182-188.
49. Vermeulen, L.; De Sousa, E.; Melo, F.; van der Heijden, M.; Cameron, K.; de Jong, J.H.; Borovski, T.; Tuynman, J.B.; Todaro, M.; Merz, C.; et al. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat. Cell. Biol. 2010, 12, 468-476.
50. Cui, G.; Goll, R.; Olsen, T.; Steigen, S.E.; Husebekk, A.; Vonen, B.; Florholmen, J. Reduced expression of microenvironment Th1 cytokines accompanies adenomas-carcinomas sequence of colorectum. Cancer Immunol. Immunother. 2007, 56, 985-995.
51. Galon, J.; Costes, A.; Sanchez-Cabo, F.; Kirilovsky, A.; Mlecnik, B.; Lagorce-Pagès, C.; Tosolini, M.; Camus, M.; Berger, A.; Wind, P.; et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006, 313, 1960-1964.
52. Rosenberg, S.A.; Yang, J.C.; Restifo, N.P. Cancer immunotherapy: moving beyond current vaccines. Nat. Med. 2004, 10, 909-915.
53. Kraman, M.; Bambrough, P.J.; Arnold, J.N.; Roberts, E.W.; Magiera, L.; Jones, J.O.; Gopinathan, A.; Tuveson, D.A.; Fearon, D.T. Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-alpha. Science 2010, 330, 827-830.
54. Santos, A.M.; Jung, J.; Aziz, N.; Kissil, J.L.; Puré, E. Targeting fibroblast activation protein inhibits tumor stromagenesis and growth in mice. J. Clin. Invest. 2009, 119, 3613-3625.