Tumour-stroma interactions in colorectal cancer: Converging on β-catenin activation and cancer stemness

British Journal of Cancer

Volumn 98, Issue 12, 2008, Pages 1886-1893

  Le, N H ^a   Franken, P ^a   Fodde, R ^a  

^a JOSEPHINE NEFKENS INSTITUTE   (Netherlands)

Author keywords

catenin; Cancer stem cells; Colorectal cancer; Fibroblast; Stroma

Indexed keywords

ANDROGEN RECEPTOR; BETA CATENIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; ESTROGEN RECEPTOR ALPHA; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NUCLEAR PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN C FOS; PROTEIN C JUN; PROTEIN GRIPI; PROTEIN KINASE B; PROTEIN P68; PROTEIN TYROSINE PHOSPHATASE SHP 1; REPTIN 52; RETINOIC ACID RECEPTOR; RETINOID X RECEPTOR; SMAD1 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; SMAD7 PROTEIN; STRATIFIN; TRANSCRIPTION FACTOR FOXO; TRANSCRIPTION FACTOR PITX2; TRANSCRIPTION FACTOR SOX17; TRANSCRIPTION FACTOR SOX4; TRANSCRIPTION FACTOR SOX9; UNINDEXED DRUG; VITAMIN D RECEPTOR; WNT PROTEIN;

CANCER INVASION; CELL TYPE; COLORECTAL CANCER; GENE MUTATION; HUMAN; METASTASIS; MICROENVIRONMENT; NONHUMAN; PARACRINE SIGNALING; PARENCHYMA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STABILITY; REGULATORY MECHANISM; SHORT SURVEY; STROMA CELL;

ADIPOCYTES; BETA CATENIN; COLORECTAL NEOPLASMS; HUMANS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASTIC STEM CELLS; STROMAL CELLS;

EID: 44949226873     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6604401     Document Type: Short Survey

References (66)

1. Adegboyega PA, Mifflin RC, DiMari JF, Saada JI, Powell DW (2002) Immunohistochemical study of myofibroblasts in normal colonic mucosa, hyperplastic polyps, and adenomatous colorectal polyps. Arch Pathol Lab Med 126: 829-836
2. Amemori S, Ootani A, Aoki S, Fujise T, Shimoda R, Kakimoto T, Shiraishi R, Sakata Y, Tsunada S, Iwakiri R, Fujimoto K (2007) Adipocytes and preadipocytes promote the proliferation of colon cancer cells in vitro. Am J Physiol Gastrointest Liver Physiol 292(3): G923-G929
3. Auguste P, Fallavollita L, Wang N, Burnier J, Bikfalvi A, Brodt P (2007) The host inflammatory response promotes liver metastasis by increasing tumor cell arrest and extravasation. Am J Pathol 170: 1781-1792
4. Bacman D, Merkel S, Croner R, Papadopoulos T, Brueckl W, Dimmler A (2007) TGF-beta receptor 2 downregulation in tumour-associated stroma worsens prognosis and high-grade tumours show more tumour-associated macrophages and lower TGF-beta1 expression in colon carcinoma: a retrospective study. BMC Cancer 7: 156
5. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, Clevers H (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449: 1003-1007
6. Bhowmick NA, Chytil A, Plieth D, Gorska AE, Dumont N, Shappell S, Washington MK, Neilson EG, Moses HL (2004) TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303: 848-851
7. Brabletz T, Hlubek F, Spaderna S, Schmalhofer O, Hiendlmeyer E, Jung A, Kirchner T (2005b) Invasion and metastasis in colorectal cancer: epithelial-mesenchymal transition, mesenchymal - epithelial transition, stem cells and beta-catenin. Cells Tissues Organs 179: 56-65
8. Brabletz T, Jung A, Hermann K, Gunther K, Hohenberger W, Kirchner T (1998) Nuclear overexpression of the oncoprotein beta-catenin in colorectal cancer is localized predominantly at the invasion front. Pathol Res Pract 194: 701-704
9. Brabletz T, Jung A, Reu S, Porzner M, Hlubek F, Kunz-Schughart LA, Knuechel R, Kirchner T (2001) Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc Natl Acad Sci USA 98: 10356-10361
10. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T (2005a) Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat Rev Cancer 5: 744-749
11. Chakladar A, Dubeykovskiy A, Wojtukiewicz LJ, Pratap J, Lei S, Wang TC (2005) Synergistic activation of the murine gastrin promoter by oncogenic Ras and beta-catenin involves SMAD recruitment. Biochem Biophys Res Commun 336: 190-196
12. Clarke SL, Betts GJ, Plant A, Wright KL, El-Shanawany TM, Harrop R, Torkington J, Rees BI, Williams GT, Gallimore AM, Godkin AJ (2006) CD4+CD25+FOXP3+ regulatory T cells suppress anti-tumor immune responses in patients with colorectal cancer. PLoS ONE 1: e129
13. Cleven AH, van Engeland M, Wouters BG, de Bruine AP (2007) Stromal expression of hypoxia regulated proteins is an adverse prognostic factor in colorectal carcinomas. Cell Oncol 29: 229-240
14. Coluccia AM, Vacca A, Dunach M, Mologni L, Redaelli S, Bustos VH, Benati D, Pinna LA, Gambacorti-Passerini C (2007) Bcr-Abl stabilizes beta-catenin in chronic myeloid leukemia through its tyrosine phosphorylation. EMBO J 26(5): 1456-1466
15. Crosnier C, Stamataki D, Lewis J (2006) Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet 7: 349-359
16. de Visser KE, Eichten A, Coussens LM (2006) Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 6: 24-37
17. De Wever O, Mareel M (2003) Role of tissue stroma in cancer cell invasion. J Pathol 200: 429-447
18. Desmouliere A, Guyot C, Gabbiani G (2004) The stroma reaction myofibroblast: a key player in the control of tumor cell behavior. Int J Dev Biol 48: 509-517
19. Dvorak HF (1986) Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 315: 1650-1659
20. Edlund S, Lee SY, Grimsby S, Zhang S, Aspenstrom P, Heldin CH, Landstrom M (2005) Interaction between Smad7 and beta-catenin: importance for transforming growth factor beta-induced apoptosis. Mol Cell Biol 25: 1475-1488
21. Essers MA, de Vries-Smits LM, Barker N, Polderman PE, Burgering BM, Korswagen HC (2005) Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science 308: 1181-1184
22. Fischer AN, Fuchs E, Mikula M, Huber H, Beug H, Mikulits W (2007) PDGF essentially links TGF-beta signaling to nuclear beta-catenin accumulation in hepatocellular carcinoma progression. Oncogene 26(23): 3395-3405
23. Fodde R, Brabletz T (2007) Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol 19(2): 150-158
24. Fodde R, Smits R, Clevers H (2001) APC, signal transduction and genetic instability in colorectal cancer. Nat Rev Cancer 1: 55-67
25. Gabbiani G (2003) The myofibroblast in wound healing and fibrocontractive diseases. J Pathol 200: 500-503
26. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, Tosolini M, Camus M, Berger A, Wind P, Zinzindohoue F, Bruneval P, Cugnenc PH, Trajanoski Z, Fridman WH, Pages F (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313: 1960-1964
27. Gaspar C, Fodde R (2004) APC dosage effects in tumorigenesis and stem cell differentiation. Int J Dev Biol 48: 377-386
28. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, Egan LJ, Kagnoff MF, Karin M (2004) IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118: 285-296
29. Han G, Li AG, Liang YY, Owens P, He W, Lu S, Yoshimatsu Y, Wang D, Ten Dijke P, Lin X, Wang XJ (2006) Smad7-induced beta-catenin degradation alters epidermal appendage development. Dev Cell 11: 301-312
30. Hill R, Song Y, Cardiff RD, Van Dyke T (2005) Selective evolution of stromal mesenchyme with p53 loss in response to epithelial tumorigenesis. Cell 123: 1001-1011
31. Hoschuetzky H, Aberle H, Kemler R (1994) Beta-catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor. J Cell Biol 127: 1375-1380
32. Hu MC, Rosenblum ND (2005) Smad1, beta-catenin and Tcf4 associate in a molecular complex with the Myc promoter in dysplastic renal tissue and cooperate to control Myc transcription. Development 132: 215-225
33. Hussein SM, Duff EK, Sirard C (2003) Smad4 and beta-catenin co-activators functionally interact with lymphoid-enhancing factor to regulate graded expression of Msx2. J Biol Chem 278: 48805-48814
34. Kaidi A, Williams AC, Paraskeva C (2007) Interaction between beta-catenin and HIF-1 promotes cellular adaptation to hypoxia. Nat Cell Biol 9(2): 210-217
35. Kajiguchi T, Lee S, Lee MJ, Trepel JB, Neckers L (2008) KIT regulates tyrosine phosphorylation and nuclear localization of beta-catenin in mast cell leukemia. Leuk Res 32(5): 761-770
36. Kalluri R, Zeisberg M (2006) Fibroblasts in cancer. Nat Rev Cancer 6: 392-401
37. Kaplan CD, Kruger JA, Zhou H, Luo Y, Xiang R, Reisfeld RA (2006) A novel DNA vaccine encoding PDGFRbeta suppresses growth and dissemination of murine colon, lung and breast carcinoma. Vaccine 24: 6994-7002
38. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA, Zhu Z, Hicklin D, Wu Y, Port JL, Altorki N, Port ER, Ruggero D, Shmelkov SV, Jensen KK, Rafii S, Lyden D (2005) VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438: 820-827
39. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, Richardson AL, Polyak K, Tubo R, Weinberg RA (2007) Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449: 557-563
40. Kim BG, Li C, Qiao W, Mamura M, Kasprzak B, Anver M, Wolfraim L, Hong S, Mushinski E, Potter M, Kim SJ, Fu XY, Deng C, Letterio JJ (2006) Smad4 signalling in T cells is required for suppression of gastrointestinal cancer. Nature 441: 1015-1019
41. Kitadai Y, Sasaki T, Kuwai T, Nakamura T, Bucana CD, Fidler IJ (2006b) Targeting the expression of platelet-derived growth factor receptor by reactive stroma inhibits growth and metastasis of human colon carcinoma. Am J Pathol 169: 2054-2065
42. Kitadai Y, Sasaki T, Kuwai T, Nakamura T, Bucana CD, Hamilton SR, Fidler IJ (2006a) Expression of activated platelet-derived growth factor receptor in stromal cells of human colon carcinomas is associated with metastatic potential. Int J Cancer 119: 2567-2574
43. Kitamura T, Kometani K, Hashida H, Matsunaga A, Miyoshi H, Hosogi H, Aoki M, Oshima M, Hattori M, Takabayashi A, Minato N, Taketo MM (2007) SMAD4-deficient intestinal tumors recruit CCR1+ myeloid cells that promote invasion. Nat Genet 39: 467-475
44. Kosinski C, Li VS, Chan AS, Zhang J, Ho C, Tsui WY, Chan TL, Mifflin RC, Powell DW, Yuen ST, Leung SY, Chen X (2007) Gene expression patterns of human colon tops and basal crypts and BMP antagonists as intestinal stem cell niche factors. Proc Natl Acad Sci USA 104: 15418-15423
45. Koukourakis MI, Giatromanolaki A, Harris AL, Sivridis E (2006) Comparison of metabolic pathways between cancer cells and stromal cells in colorectal carcinomas: a metabolic survival role for tumor-associated stroma. Cancer Res 66: 632-637
46. Ling KL, Pratap SE, Bates GJ, Singh B, Mortensen NJ, George BD, Warren BF, Piris J, Roncador G, Fox SB, Banham AH, Cerundolo V (2007) Increased frequency of regulatory T cells in peripheral blood and tumour infiltrating lymphocytes in colorectal cancer patients. Cancer Immunol 7: 7
47. Lizee G, Radvanyi LG, Overwijk WW, Hwu P (2006) Improving antitumor immune responses by circumventing immunoregulatory cells and mechanisms. Clin Cancer Res 12: 4794-4803
48. Mishra L, Shetty K, Tang Y, Stuart A, Byers SW (2005) The role of TGF-beta and Wnt signaling in gastrointestinal stem cells and cancer. Oncogene 24: 5775-5789
49. Monga SP, Mars WM, Pediaditakis P, Bell A, Mule K, Bowen WC, Wang X, Zarnegar R, Michalopoulos GK (2002) Hepatocyte growth factor induces Wnt-independent nuclear translocation of beta-catenin after Met-beta-catenin dissociation in hepatocytes. Cancer Res 62: 2064-2071
50. Mukaratirwa S, Koninkx JF, Gruys E, Nederbragt H (2005) Mutual paracrine effects of colorectal tumour cells and stromal cells: modulation of tumour and stromal cell differentiation and extracellular matrix component production in culture. Int J Exp Pathol 86: 219-229
51. Nateri AS, Spencer-Dene B, Behrens A (2005) Interaction of phosphorylated c-Jun with TCF4 regulates intestinal cancer development. Nature 437: 281-285
52. Nishita M, Hashimoto MK, Ogata S, Laurent MN, Ueno N, Shibuya H, Cho KW (2000) Interaction between Wnt and TGF-beta signalling pathways during formation of Spemann's organizer. Nature 403: 781-785
53. Orimo A, Weinberg RA (2006) Stromal fibroblasts in cancer: a novel tumor-promoting cell type. Cell Cycle 5: 1597-1601
54. Pages F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R, Mlecnik B, Kirilovsky A, Nilsson M, Damotte D, Meatchi T, Bruneval P, Cugnenc PH, Trajanoski Z, Fridman WH, Galon J (2005) Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 353: 2654-2666
55. Potten CS, Loeffler M (1990) Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110: 1001-1020
56. Powrie F (2004) Immune regulation in the intestine: a balancing act between effector and regulatory T cell responses. Ann NY Acad Sci 1029: 132-141
57. Rakoff-Nahoum S, Medzhitov R (2007) Regulation of spontaneous intestinal tumorigenesis through the adaptor protein MyD88. Science 317: 124-127
58. Rasola A, Fassetta M, De Bacco F, D'Alessandro L, Gramaglia D, Di Renzo MF, Comoglio PM (2007) A positive feedback loop between hepatocyte growth factor receptor and beta-catenin sustains colorectal cancer cell invasive growth. Oncogene 26: 1078-1087
59. Sakamoto K, Tominaga Y, Yamauchi K, Nakatsu Y, Sakumi K, Yoshiyama K, Egashira A, Kura S, Yao T, Tsuneyoshi M, Maki H, Nakabeppu Y, Tsuzuki T (2007) MUTYH-null mice are susceptible to spontaneous and oxidative stress induced intestinal tumorigenesis. Cancer Res 67: 6599-6604
60. Sivridis E, Giatromanolaki A, Koukourakis MI (2005) Proliferating fibroblasts at the invading tumour edge of colorectal adenocarcinomas are associated with endogenous markers of hypoxia, acidity, and oxidative stress. J Clin Pathol 58: 1033-1038
61. Stein U, Arlt F, Walther W, Smith J, Waldman T, Harris ED, Mertins SD, Heizmann CW, Allard D, Birchmeier W, Schlag PM, Shoemaker RH (2006) The metastasis-associated gene S100A4 is a novel target of beta-catenin/T-cell factor signaling in colon cancer. Gastroenterology 131: 1486-1500
62. Sullivan R, Graham CH (2007) Hypoxia-driven selection of the metastatic phenotype. Cancer Metastasis Rev 26: 319-331
63. Tian YC, Phillips AO (2002) Interaction between the transforming growth factor-beta type II receptor/Smad pathway and beta-catenin during transforming growth factor-beta1-mediated adherens junction disassembly. Am J Pathol 160: 1619-1628
64. Toualbi K, Guller MC, Mauriz JL, Labalette C, Buendia MA, Mauviel A, Bernuau D (2007) Physical and functional cooperation between AP-1 and beta-catenin for the regulation of TCF-dependent genes. Oncogene 26: 3492-3502
65. van Es JH, Jay P, Gregorieff A, van Gijn ME, Jonkheer S, Hatzis P, Thiele A, van den Born M, Begthel H, Brabletz T, Taketo MM, Clevers H (2005) Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol 7: 381-386
66. Yang L, Lin C, Liu ZR (2006) P68 RNA helicase mediates PDGF-induced epithelial mesenchymal transition by displacing Axin from beta-catenin. Cell 127: 139-155