Dependency of Colorectal Cancer on a TGF-β-Driven Program in Stromal Cells for Metastasis Initiation

Cancer Cell

Volumn 22, Issue 5, 2012, Pages 571-584

  Calon, Alexandre ^a   Espinet, Elisa ^a   Palomo Ponce, Sergio ^a   Tauriello, Daniele V F ^a   Iglesias, Mar ^b   Céspedes, María Virtudes ^c   Sevillano, Marta ^a   Nadal, Cristina ^d   Jung, Peter ^a   Zhang, Xiang H F ^e   Byrom, Daniel ^a   Riera, Antoni ^a,f   Rossell, David ^a   Mangues, Ramón ^c   Massagué, Joan ^e,g   Sancho, Elena ^a   Batlle, Eduard ^a,h  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^b INST MUNIC D INVESTIGACIO MEDICA   (Spain)

^c HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

^d HOSPITAL CLÍNIC   (Spain)

^e MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^f UNIVERSITY OF BARCELONA   (Spain)

^g HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^h INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; INTERLEUKIN 1; STAT3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER RISK; CELL SURVIVAL; COLORECTAL CANCER; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; METASTASIS POTENTIAL; MICROENVIRONMENT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RELAPSE; STROMA;

EID: 84869021181     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2012.08.013     Document Type: Article

References (51)

1. Alarcón C., Zaromytidou A.I., Xi Q., Gao S., Yu J., Fujisawa S., Barlas A., Miller A.N., Manova-Todorova K., Macias M.J., et al. Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-beta pathways. Cell 2009, 139:757-769.
2. Becker C., Fantini M.C., Schramm C., Lehr H.A., Wirtz S., Nikolaev A., Burg J., Strand S., Kiesslich R., Huber S., et al. TGF-beta suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling. Immunity 2004, 21:491-501.
3. Bhatia M., Davenport V., Cairo M.S. The role of interleukin-11 to prevent chemotherapy-induced thrombocytopenia in patients with solid tumors, lymphoma, acute myeloid leukemia and bone marrow failure syndromes. Leuk. Lymphoma 2007, 48:9-15.
4. Bos P.D., Zhang X.H., Nadal C., Shu W., Gomis R.R., Nguyen D.X., Minn A.J., van de Vijver M.J., Gerald W.L., Foekens J.A., Massagué J. Genes that mediate breast cancer metastasis to the brain. Nature 2009, 459:1005-1009.
5. Bueno L., de Alwis D.P., Pitou C., Yingling J., Lahn M., Glatt S., Trocóniz I.F. Semi-mechanistic modelling of the tumour growth inhibitory effects of LY2157299, a new type I receptor TGF-beta kinase antagonist, in mice. Eur. J. Cancer 2008, 44:142-150.
6. Céspedes M.V., Espina C., García-Cabezas M.A., Trias M., Boluda A., Gómez del Pulgar M.T., Sancho F.J., Nistal M., Lacal J.C., Mangues R. Orthotopic microinjection of human colon cancer cells in nude mice induces tumor foci in all clinically relevant metastatic sites. Am. J. Pathol. 2007, 170:1077-1085.
7. Flavell R.A., Sanjabi S., Wrzesinski S.H., Licona-Limón P. The polarization of immune cells in the tumour environment by TGFbeta. Nat. Rev. Immunol. 2010, 10:554-567.
8. Gay L.J., Felding-Habermann B. Contribution of platelets to tumour metastasis. Nat. Rev. Cancer 2011, 11:123-134.
9. Grady W.M., Markowitz S.D. Genetic and epigenetic alterations in colon cancer. Annu. Rev. Genomics Hum. Genet. 2002, 3:101-128.
10. Hahn J.N., Falck V.G., Jirik F.R. Smad4 deficiency in T cells leads to the Th17-associated development of premalignant gastroduodenal lesions in mice. J. Clin. Invest. 2011, 121:4030-4042.
11. Ikeda M., Furukawa H., Imamura H., Shimizu J., Ishida H., Masutani S., Tatsuta M., Satomi T. Poor prognosis associated with thrombocytosis in patients with gastric cancer. Ann. Surg. Oncol. 2002, 9:287-291.
12. Jones S., Chen W.D., Parmigiani G., Diehl F., Beerenwinkel N., Antal T., Traulsen A., Nowak M.A., Siegel C., Velculescu V.E., et al. Comparative lesion sequencing provides insights into tumor evolution. Proc. Natl. Acad. Sci. USA 2008, 105:4283-4288.
13. Jorissen R.N., Gibbs P., Christie M., Prakash S., Lipton L., Desai J., Kerr D., Aaltonen L.A., Arango D., Kruhøffer M., et al. Metastasis-associated gene expression changes predict poor outcomes in patients with Dukes stage B and C colorectal cancer. Clin. Cancer Res. 2009, 15:7642-7651.
14. Jung P., Sato T., Merlos-Suárez A., Barriga F.M., Iglesias M., Rossell D., Auer H., Gallardo M., Blasco M.A., Sancho E., et al. Isolation and in vitro expansion of human colonic stem cells. Nat. Med. 2011, 17:1225-1227.
15. Kang Y., Siegel P.M., Shu W., Drobnjak M., Kakonen S.M., Cordón-Cardo C., Guise T.A., Massagué J. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 2003, 3:537-549.
16. Kang Y., He W., Tulley S., Gupta G.P., Serganova I., Chen C.R., Manova-Todorova K., Blasberg R., Gerald W.L., Massagué J. Breast cancer bone metastasis mediated by the Smad tumor suppressor pathway. Proc. Natl. Acad. Sci. USA 2005, 102:13909-13914.
17. Kim B.G., Li C., Qiao W., Mamura M., Kasprzak B., Anver M., Wolfraim L., Hong S., Mushinski E., Potter M., et al. Smad4 signalling in T cells is required for suppression of gastrointestinal cancer. Nature 2006, 441:1015-1019.
18. Kitamura T., Biyajima K., Aoki M., Oshima M., Taketo M.M. Matrix metalloproteinase 7 is required for tumor formation, but dispensable for invasion and fibrosis in SMAD4-deficient intestinal adenocarcinomas. Lab. Invest. 2009, 89:98-105.
19. Kusaba T., Nakayama T., Yamazumi K., Yakata Y., Yoshizaki A., Inoue K., Nagayasu T., Sekine I. Activation of STAT3 is a marker of poor prognosis in human colorectal cancer. Oncol. Rep. 2006, 15:1445-1451.
20. Labelle M., Begum S., Hynes R.O. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell 2011, 20:576-590.
21. Liu F., Pouponnot C., Massagué J. Dual role of the Smad4/DPC4 tumor suppressor in TGFbeta-inducible transcriptional complexes. Genes Dev. 1997, 11:3157-3167.
22. Luzzi K.J., MacDonald I.C., Schmidt E.E., Kerkvliet N., Morris V.L., Chambers A.F., Groom A.C. Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am. J. Pathol. 1998, 153:865-873.
23. Markowitz S.D., Bertagnolli M.M. Molecular origins of cancer: molecular basis of colorectal cancer. N. Engl. J. Med. 2009, 361:2449-2460.
24. Markowitz S., Wang J., Myeroff L., Parsons R., Sun L., Lutterbaugh J., Fan R.S., Zborowska E., Kinzler K.W., Vogelstein B., et al. Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability. Science 1995, 268:1336-1338.
25. Massagué J. TGFbeta in Cancer. Cell 2008, 134:215-230.
26. Merlos-Suárez A., Barriga F.M., Jung P., Iglesias M., Céspedes M.V., Rossell D., Sevillano M., Hernando-Momblona X., da Silva-Diz V., Muñoz P., et al. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell 2011, 8:511-524.
27. Morikawa K., Walker S.M., Nakajima M., Pathak S., Jessup J.M., Fidler I.J. Influence of organ environment on the growth, selection, and metastasis of human colon carcinoma cells in nude mice. Cancer Res. 1988, 48:6863-6871.
28. Morikawa T., Baba Y., Yamauchi M., Kuchiba A., Nosho K., Shima K., Tanaka N., Huttenhower C., Frank D.A., Fuchs C.S., Ogino S. STAT3 expression, molecular features, inflammation patterns, and prognosis in a database of 724 colorectal cancers. Clin. Cancer Res. 2011, 17:1452-1462.
29. Muñoz N.M., Upton M., Rojas A., Washington M.K., Lin L., Chytil A., Sozmen E.G., Madison B.B., Pozzi A., Moon R.T., et al. Transforming growth factor beta receptor type II inactivation induces the malignant transformation of intestinal neoplasms initiated by Apc mutation. Cancer Res. 2006, 66:9837-9844.
30. Musashi M., Yang Y.C., Paul S.R., Clark S.C., Sudo T., Ogawa M. Direct and synergistic effects of interleukin 11 on murine hemopoiesis in culture. Proc. Natl. Acad. Sci. USA 1991, 88:765-769.
31. Nouso K., Ito Y., Kuwaki K., Kobayashi Y., Nakamura S., Ohashi Y., Yamamoto K. Prognostic factors and treatment effects for hepatocellular carcinoma in Child C cirrhosis. Br. J. Cancer 2008, 98:1161-1165.
32. Oskarsson T., Acharyya S., Zhang X.H., Vanharanta S., Tavazoie S.F., Morris P.G., Downey R.J., Manova-Todorova K., Brogi E., Massagué J. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat. Med. 2011, 17:867-874.
33. Padua D., Zhang X.H., Wang Q., Nadal C., Gerald W.L., Gomis R.R., Massagué J. TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 2008, 133:66-77.
34. Sabates-Bellver J., Van der Flier L.G., de Palo M., Cattaneo E., Maake C., Rehrauer H., Laczko E., Kurowski M.A., Bujnicki J.M., Menigatti M., et al. Transcriptome profile of human colorectal adenomas. Mol. Cancer Res. 2007, 5:1263-1275.
35. Sato T., Stange D.E., Ferrante M., Vries R.G., Van Es J.H., Van den Brink S., Van Houdt W.J., Pronk A., Van Gorp J., Siersema P.D., Clevers H. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 2011, 141:1762-1772.
36. Sethi N., Dai X., Winter C.G., Kang Y. Tumor-derived JAGGED1 promotes osteolytic bone metastasis of breast cancer by engaging notch signaling in bone cells. Cancer Cell 2011, 19:192-205.
37. Shultz L.D., Ishikawa F., Greiner D.L. Humanized mice in translational biomedical research. Nat. Rev. Immunol. 2007, 7:118-130.
38. Smith J.J., Deane N.G., Wu F., Merchant N.B., Zhang B., Jiang A., Lu P., Johnson J.C., Schmidt C., Bailey C.E., et al. Experimentally derived metastasis gene expression profile predicts recurrence and death in patients with colon cancer. Gastroenterology 2010, 138:958-968.
39. Sonoshita M., Aoki M., Fuwa H., Aoki K., Hosogi H., Sakai Y., Hashida H., Takabayashi A., Sasaki M., Robine S., et al. Suppression of colon cancer metastasis by Aes through inhibition of Notch signaling. Cancer Cell 2011, 19:125-137.
40. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 2005, 102:15545-15550.
41. Takaku K., Oshima M., Miyoshi H., Matsui M., Seldin M.F., Taketo M.M. Intestinal tumorigenesis in compound mutant mice of both Dpc4 (Smad4) and Apc genes. Cell 1998, 92:645-656.
42. Tan A.R., Alexe G., Reiss M. Transforming growth factor-beta signaling: emerging stem cell target in metastatic breast cancer?. Breast Cancer Res. Treat. 2009, 115:453-495.
43. Teramura M., Kobayashi S., Hoshino S., Oshimi K., Mizoguchi H. Interleukin-11 enhances human megakaryocytopoiesis in vitro. Blood 1992, 79:327-331.
44. Tsushima H., Ito N., Tamura S., Matsuda Y., Inada M., Yabuuchi I., Imai Y., Nagashima R., Misawa H., Takeda H., et al. Circulating transforming growth factor beta 1 as a predictor of liver metastasis after resection in colorectal cancer. Clin. Cancer Res. 2001, 7:1258-1262.
45. Valastyan S., Weinberg R.A. Tumor metastasis: molecular insights and evolving paradigms. Cell 2011, 147:275-292.
46. Van der Flier L.G., Sabates-Bellver J., Oving I., Haegebarth A., De Palo M., Anti M., Van Gijn M.E., Suijkerbuijk S., Van de Wetering M., Marra G., Clevers H. The intestinal Wnt/TCF signature. Gastroenterology 2007, 132:628-632.
47. Walther A., Johnstone E., Swanton C., Midgley R., Tomlinson I., Kerr D. Genetic prognostic and predictive markers in colorectal cancer. Nat. Rev. Cancer 2009, 9:489-499.
48. Wang J., Sun L., Myeroff L., Wang X., Gentry L.E., Yang J., Liang J., Zborowska E., Markowitz S., Willson J.K., et al. Demonstration that mutation of the type II transforming growth factor beta receptor inactivates its tumor suppressor activity in replication error-positive colon carcinoma cells. J. Biol. Chem. 1995, 270:22044-22049.
49. Warren R.S., Yuan H., Matli M.R., Gillett N.A., Ferrara N. Regulation by vascular endothelial growth factor of human colon cancer tumorigenesis in a mouse model of experimental liver metastasis. J. Clin. Invest. 1995, 95:1789-1797.
50. Yin J.J., Selander K., Chirgwin J.M., Dallas M., Grubbs B.G., Wieser R., Massagué J., Mundy G.R., Guise T.A. TGF-beta signaling blockade inhibits PTHrP secretion by breast cancer cells and bone metastases development. J. Clin. Invest. 1999, 103:197-206.
51. Yingling J.M., Blanchard K.L., Sawyer J.S. Development of TGF-beta signalling inhibitors for cancer therapy. Nat. Rev. Drug Discov. 2004, 3:1011-1022.