BMP signaling promotes the growth of primary human colon carcinomas in vivo

Journal of Molecular Cell Biology

Volumn 2, Issue 6, 2010, Pages 318-332

  Lorente Trigos, Aiala ^a   Varnat, Frédéric ^a   Melotti, Alice ^a   Altaba, Ariel Ruiz I ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

BMP; Colon cancer; GLI1; Human

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; GLI PROTEIN; ONCOPROTEIN; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANSACTIVATOR PROTEIN;

ANIMAL; APOPTOSIS; ARTICLE; CARCINOMA; CELL CULTURE; CELL PROLIFERATION; CELL SURVIVAL; COLON TUMOR; HUMAN; METABOLISM; MOUSE; NUDE MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION; XENOGRAFT;

ANIMALS; APOPTOSIS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEINS; CARCINOMA; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; COLONIC NEOPLASMS; HUMANS; MICE; MICE, NUDE; ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANS-ACTIVATORS; TRANSPLANTATION, HETEROLOGOUS;

EID: 79951483059     PISSN: 16742788     EISSN: 17594685     Source Type: Journal    
DOI: 10.1093/jmcb/mjq035     Document Type: Article

References (54)

1. American Cancer Society. (2010). Colorectal cancer facts and figures 2008-2010. http://www.cancer.org/downloads/STT/F861708-finalforweb.pdf.
2. Arimura, S., Matsunaga, A., Kitamura, T., Aoki, K., Aoki, M., and Taketo, M. M. (2009). Reduced level of smoothened suppresses intestinal tumorigenesis by down-regulation of Wnt signaling. Gastroenterology 137, 629-638.
3. Ashique, A. M., Fu, K., and Richman, J. M. (2002). Signalling via type IA and type IB bone morphogenetic protein receptors (BMPR) regulates intramembranous bone formation, chondrogenesis and feather formation in the chicken embryo. Int. J. Dev. Biol. 46, 243-253. (Pubitemid 34288707)
4. Beck, S. E., and Carethers, J. M. (2007). BMP suppresses PTEN expression via RAS/ERK signaling. Cancer Biol. Ther. 6, 1313-1317. (Pubitemid 351590388)
5. Beck, S. E., Jung, B. H., Fiorino, A., Gomez, J., Rosario, E. D., Cabrera, B. L., Huang, S. C., Chow, J. Y., and Carethers, J. M. (2006). Bone morphogenetic protein signaling and growth suppression in colon cancer. Am. J. Physiol. Gastrointest. Liver Physiol. 291, G135-G145. (Pubitemid 44024671)
6. Blobe, G. C., Schiemann, W. P., and Lodish, H. F. (2000). Role of transforming growth factor beta in human disease. N. Engl. J. Med. 342, 1350-1358. (Pubitemid 30408720)
7. Clement, V., Sanchez, P., de Tribolet, N., Radovanovic, I., and Ruiz i Altaba, A. (2007). HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr. Biol. 17, 165-172. (Pubitemid 46107823)
8. Cho, K. R., and Vogelstein, B. (1992). Suppressor gene alterations in the colorectal adenoma-carcinoma sequence. J. Cell Biochem. Suppl. 16 G, 137-141.
9. Deng, H., Makizumi, R., Ravikumar, T. S., Dong, H., Yang, W., and Yang, W. L. (2007). Bone morphogenetic protein-4 is overexpressed in colonic adenocarcinomas and promotes migration and invasion of HCT116 cells. Exp. Cell Res. 313, 1033-1044. (Pubitemid 46273448)
10. Deng, H., Ravikumar, T. S., and Yang, W. L. (2009). Overexpression of bone morphogenetic protein 4 enhances the invasiveness of Smad4-deficient human colorectal cancer cells. Cancer Lett. 281, 220-231.
11. Dennler, S., Andre, J., Alexaki, I., Li, A., Magnaldo, T., ten Dijke, P., Wang, X. J., Verrecchia, F., and Mauviel, A. (2007). Induction of sonic hedgehog mediators by transforming growth factor-beta: Smad3-dependent activation of Gli2 and Gli1 expression in vitro and in vivo. Cancer Res. 67, 6981-6986. (Pubitemid 47105546)
12. Dennler, S., Andre, J., Verrecchia, F., and Mauviel, A. (2009). Cloning of the human GLI2 Promoter: transcriptional activation by transforming growth factor-beta via SMAD3/beta-catenin cooperation. J. Biol. Chem. 284, 31523-31531.
13. Derynck, R., and Zhang, Y. E. (2003). Smad-dependent and Smad independent pathways in TGF-beta family signalling. Nature 425, 577-584. (Pubitemid 37280136)
14. Fre, S., Pallavi, S. K., Huyghe, M., Lae, M., Janssen, K. P., Robine, S., Artavanis-Tsakonas, S., and Louvard, D. (2009). Notch and Wnt signals cooperatively control cell proliferation and tumorigenesis in the intestine. Proc. Natl. Acad. Sci. USA 106, 6309-6314.
15. Grady, W. M., Myeroff, L. L., Swinler, S. E., Rajput, A., Thiagalingam, S., Lutterbaugh, J. D., Neumann, A., Brattain, M. G., Chang, J., Kim, S. J., et al. (1999). Mutational inactivation of transforming growth factor beta receptor type II in microsatellite stable colon cancers. Cancer Res. 59, 320-324. (Pubitemid 29048861)
16. Grijelmo, C., Rodrigue, C., Svrcek, M., Bruyneel, E., Hendrix, A., de Wever, O., and Gespach, C. (2007). Proinvasive activity of BMP-7 through SMAD4/src-independent and ERK/Rac/JNK-dependent signaling pathways in colon cancer cells. Cell Signal. 19, 1722-1732. (Pubitemid 46935428)
17. Gulacsi, A., and Lillien, L. (2003). Sonic hedgehog and bone morphogenetic protein regulate interneuron development from dorsal telencephalic progenitors in vitro. J. Neurosci. 23, 9862-9872. (Pubitemid 37371600)
18. Haramis, A. P., Begthel, H., van den Born, M., van Es, J., Jonkheer, S., Offerhaus, G. J., and Clevers, H. (2004). De novo crypt formation and juvenile polyposis on BMP inhibition in mouse intestine. Science 303, 1684-1686. (Pubitemid 38338329)
19. Hardwick, J. C., Kodach, L. L., Offerhaus, G. J., and van den Brink, G. R. (2008). Bone morphogenetic protein signalling in colorectal cancer. Nat. Rev. Cancer 8, 806-812.
20. Howe, J. R., Roth, S., Ringold, J. C., Summers, R. W., Jarvinen, H. J., Sistonen, P., Tomlinson, I. P., Houlston, R. S., Bevan, S., Mitros, F. A., et al. (1998). Mutations in the SMAD4/DPC4 gene in juvenile polyposis. Science 280, 1086-1088. (Pubitemid 28234951)
21. Jemal, A., Siegel, R., Ward, E., Hao, Y., Xu, J., and Thun, M. J. (2009). Cancer statistics, 2009. CA Cancer J. Clin. 59, 225-249.
22. Kang, M. H., Kang, H. N., Kim, J. L., Kim, J. S., Oh, S. C., and Yoo, Y. A. (2009). Inhibition of PI3 kinase/Akt pathway is required for BMP2-induced EMT and invasion. Oncol. Rep. 22, 525-534.
23. Kawai, S., and Sugiura, T. (2001). Characterization of human bone morphogenetic protein (BMP)-4 and-7 gene promoters: activation of BMP promoters by Gli, a sonic hedgehog mediator. Bone 29, 54-61. (Pubitemid 32707923)
24. Kim, J. S., Crooks, H., Dracheva, T., Nishanian, T. G., Singh, B., Jen, J., and Waldman, T. (2002). Oncogenic beta-catenin is required for bone morphogenetic protein 4 expression in human cancer cells. Cancer Res. 62, 2744-2748. (Pubitemid 34525754)
25. Kodach, L. L., Bleuming, S. A., Peppelenbosch, M. P., Hommes, D. W., van den Brink, G. R., and Hardwick, J. C. (2007). The effect of statins in colorectal cancer is mediated through the bone morphogenetic protein pathway. Gastroenterology 133, 1272-1281. (Pubitemid 47494465)
26. Kodach, L. L., Bleuming, S. A., Musler, A. R., Peppelenbosch, M. P., Hommes, D. W., van den Brink, G. R., van Noesel, C. J., Offerhaus, G. J., and Hardwick, J. C. (2008a). The bone morphogenetic protein pathway is active in human colon adenomas and inactivated in colorectal cancer. Cancer 112, 300-306.
27. Kodach, L. L., Wiercinska, E., de Miranda, N. F., Bleuming, S. A., Musler, A. R., Peppelenbosch, M. P., Dekker, E., van den Brink, G. R., van Noesel, C. J., Morreau, H., et al. (2008b). The bone morphogenetic protein pathway is inactivated in the majority of sporadic colorectal cancers. Gastroenterology 134, 1332-1341.
28. Kretzschmar, M., Liu, F., Hata, A., Doody, J., and Massague, J. (1997). The TGF-beta family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev. 11, 984-995. (Pubitemid 27199878)
29. Lagna, G., Hata, A., Hemmati-Brivanlou, A., and Massague, J. (1996). Partnership between DPC4 and SMAD proteins in TGF-beta signalling pathways. Nature 383, 832-836. (Pubitemid 26372668)
30. Lee, C. W., Ito, K., and Ito, Y. (2010). Role of RUNX3 in bone morphogenetic protein signaling in colorectal cancer. Cancer Res. 70, 4243-4252.
31. Loh, K., Chia, J. A., Greco, S., Cozzi, S. J., Buttenshaw, R. L., Bond, C. E., Simms, L. A., Pike, T., Young, J. P., Jass, J. R., et al. (2008). Bone morphogenic protein 3 inactivation is an early and frequent event in colorectal cancer development. Genes Chromosomes Cancer 47, 449-460. (Pubitemid 351657180)
32. Lopez-Rovira, T., Chalaux, E., Massague, J., Rosa, J. L., and Ventura, F. (2002). Direct binding of Smad1 and Smad4 to two distinct motifs mediates bone morphogenetic protein-specific transcriptional activation of Id1 gene. J. Biol. Chem. 277, 3176-3185. (Pubitemid 34953179)
33. Massague, J. (1996). TGFbeta signaling: receptors, transducers, and Mad proteins. Cell 85, 947-950.
34. Morin, P. J., Sparks, A. B., Korinek, V., Barker, N., Clevers, H., Vogelstein, B., and Kinzler, K. W. (1997). Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275, 1787-1790. (Pubitemid 27136715)
35. Nishanian, T. G., Kim, J. S., Foxworth, A., and Waldman, T. (2004). Suppression of tumorigenesis and activation of Wnt signaling by bone morphogenetic protein 4 in human cancer cells. Cancer Biol. Ther. 3, 667-675. (Pubitemid 41351107)
36. Piccirillo, S. G., Reynolds, B. A., Zanetti, N., Lamorte, G., Binda, E., Broggi, G., Brem, H., Olivi, A., Dimeco, F., and Vescovi, A. L. (2006). Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 444, 761-765. (Pubitemid 44949605)
37. Powell, S. M., Zilz, N., Beazer-Barclay, Y., Bryan, T. M., Hamilton, S. R., Thibodeau, S. N., Vogelstein, B., and Kinzler, K. W. (1992). APC mutations occur early during colorectal tumorigenesis. Nature 359, 235-237.
38. Sahni, V., Mukhopadhyay, A., Tysseling, V., Hebert, A., Birch, D., McGuire, T. L., Stupp, S. I., and Kessler, J. A. (2010). BMPR1a and BMPR1b signaling exert opposing effects on gliosis after spinal cord injury. J. Neurosci. 30, 1839-1855.
39. Sirard, C., de la Pompa, J. L., Elia, A., Itie, A., Mirtsos, C., Cheung, A., Hahn, S., Wakeham, A., Schwartz, L., Kern, S. E., et al. (1998). The tumor suppressor gene Smad4/Dpc4 is required for gastrulation and later for anterior development of the mouse embryo. Genes Dev. 12, 107-119. (Pubitemid 28083662)
40. Sneddon, J. B., Zhen, H. H., Montgomery, K., van de Rijn, M., Tward, A. D., West, R., Gladstone, H., Chang, H. Y., Morganroth, G. S., Oro, A. E., et al. (2006). Bone morphogenetic protein antagonist gremlin 1 is widely expressed by cancer-associated stromal cells and can promote tumor cell proliferation. Proc. Natl. Acad. Sci. USA 103, 14842-14847. (Pubitemid 44527816)
41. Sparks, A. B., Morin, P. J., Vogelstein, B., and Kinzler, K. W. (1998). Mutational analysis of the APC/beta-catenin/Tcf pathway in colorectal cancer. Cancer Res. 58, 1130-1134. (Pubitemid 28183198)
42. Stecca, B., and Ruiz i Altaba, A. (2010). Context-dependent regulation of the GLI code in cancer by HEDGEHOG and non-HEDGEHOG signals. J. Mol. Cell Biol. 2, 84-95.
43. Stecca, B., Mas, C., Clement, V., Zbinden, M., Correa, R., Piguet, V., Beermann, F., and Ruiz i Altaba, A. (2007). Melanomas require HEDGEHOG-GLI signaling regulated by interactions between GLI1 and the RAS-MEK/AKT pathways. Proc. Natl. Acad. Sci. USA 104, 5895-5900. (Pubitemid 47175630)
44. Thawani, J. P., Wang, A. C., Than, K. D., Lin, C. Y., La Marca, F., and Park, P. (2010). Bone morphogenetic proteins and cancer: review of the literature. Neurosurgery 66, 233-246; discussion 246.
45. van Es, J. H., van Gijn, M. E., Riccio, O., van den Born, M., Vooijs, M., Begthel, H., Cozijnsen, M., Robine, S., Winton, D. J., Radtke, F., et al. (2005). Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435, 959-963. (Pubitemid 40896322)
46. Varnat, F., Duquet, A., Malerba, M., Zbinden, M., Mas, C., Gervaz, P., and Ruiz i Altaba, A. (2009). Human colon cancer epithelial cells harbour active HEDGEHOG-GLI signalling that is essential for tumour growth, recurrence, metastasis and stem cell survival and expansion. EMBO Mol. Med. 1, 338-351.
47. Varnat, F., Zacchetti, G., and Ruiz i Altaba, A. (2010a). Hedgehog pathway activity is required for the lethality and intestinal phenotypes of mice with hyperactive Wnt signaling. Mech. Dev. 127, 73-81.
48. Varnat, F., Siegl-Cachedenier, I., Malerba, M., Gervaz, P., and Ruiz i Altaba, A. (2010b). Loss of WNT-TCF addiction and enhancement of HH-GLI1 define the metastatic transition of human colon cancers. EMBO Mol. Med. Doi:10.1002/emmm.201000098
49. Walsh, D. W., Godson, C., Brazil, D. P., and Martin, F. (2010). Extracellular BMP-antagonist regulation in development and disease: tied up in knots. Trends Cell Biol. 20, 244-256.
50. Xu, Y., and Pasche, B. (2007). TGF-beta signaling alterations and susceptibility to colorectal cancer. Hum. Mol. Genet. 16, R14-R20. (Pubitemid 47241839)
51. Zbinden, M., Duquet, A., Lorente-Trigos, A., Ngwabyt, S. N., Borges, I., and Ruiz i Altaba, A. (2010). NANOG regulates glioma stem cells and is essential in vivo acting in a cross-functional network with GLI1 and p53. EMBO J. 29, 2659-2674.
52. Zhang, Y., Feng, X., We, R., and Derynck, R. (1996). Receptor-associated Mad homologues synergize as effectors of the TGF-beta response. Nature 383, 168-172. (Pubitemid 26303979)
53. Zhou, X. P., Woodford-Richens, K., Lehtonen, R., Kurose, K., Aldred, M., Hampel, H., Launonen, V., Virta, S., Pilarski, R., Salovaara, R., et al. (2001). Germline mutations in BMPR1A/ALK3 cause a subset of cases of juvenile polyposis syndrome and of Cowden and Bannayan-Riley-Ruvalcaba syndromes. Am. J. Hum. Genet. 69, 704-711. (Pubitemid 32868516)
54. Zou, H., Wieser, R., Massague, J., and Niswander, L. (1997). Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev. 11, 2191-2203. (Pubitemid 27387970)