Cripto binds transforming growth factor β (TGF-β) and inhibits TGF-β signaling

Molecular and Cellular Biology

Volumn 26, Issue 24, 2006, Pages 9268-9278

  Gray, Peter C ^a   Shani, Gidi ^a   Aung, Kevin ^a   Kelber, Jonathan ^a   Vale, Wylie ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CANCER GROWTH FACTOR; CRYPTIC PROTEIN; EPIDERMAL GROWTH FACTOR; GROWTH DIFFERENTIATION FACTOR 1; GROWTH DIFFERENTIATION FACTOR 3; GROWTH DIFFERENTIATION FACTOR 5; LIGAND; MEMBRANE PROTEIN; ONCOPROTEIN; PROTEIN CRIPTO; PROTEIN FRL 1; PROTEIN NODAL; RECEPTOR PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1;

ARTICLE; BREAST EPITHELIUM; CARCINOGENESIS; CONTROLLED STUDY; CYTOSTASIS; EMBRYO DEVELOPMENT; HUMAN; HUMAN CELL; LIGAND BINDING; ONCOGENE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS REGULATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TUMOR PROMOTION;

ANIMALS; CELL LINE; CELL LINE, TUMOR; EPIDERMAL GROWTH FACTOR; HELA CELLS; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; NEOPLASM PROTEINS; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 33845465701     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01168-06     Document Type: Article

References (60)

1. Adkins, H. B., C. Bianco, S. G. Schiffer, P. Rayhorn, M. Zafari, A. E. Cheung, O. Orozco, D. Olson, A. De Luca, L. L. Chen, K. Miatkowski, C. Benjamin, N. Normanno, K. P. Williams, M. Jarpe, D. LePage, D. Salomon, and M. Sanicola. 2003. Antibody blockade of the Cripto CFC domain suppresses tumor cell growth in vivo. J. Clin. Investig. 112:575-587.
2. Akhurst, R. J., and R. Derynck. 2001. TGF-beta signaling in cancer - a double-edged sword. Trends Cell Biol. 11:S44-S51.
3. Bianco, C., L. Strirri, N. Normanno, N. Khan, and D. S. Salomon. 2005. Cripto-1: an oncofetal gene with many faces. Curr. Top. Dev. Biol. 67:85-133.
4. Branford, W. W., and H. J. Yost. 2004. Nodal signaling: CrypticLefty mechanism of antagonism decoded. Curr. Biol. 14:R341-R343.
5. Brivanlou, A. H., F. H. Gage, R. Jaenisch, T. Jessell, D. Melton, and J. Rossant. 2003. Stem cells. Setting standards for human embryonic stem cells. Science 300:913-916.
6. Brown, C. W., D. E. Houston-Hawkins, T. K. Woodruff, and M. M. Matzuk. 2000. Insertion of Inhbb into the Inhba locus rescues the Inhba-null phenotype and reveals new activin functions. Nat. Genet. 25:453-457.
7. Chen, C., S. M. Ware, A. Sato, D. E. Houston-Hawkins, R. Habas, M. M. Matzuk, M. M. Shen, and C. W. Brown. 2006. The Vg1-related protein Gdf3 acts in a Nodal signaling pathway in the pre-gastrulation mouse embryo. Development 133:319-329.
8. Cheng, S. K., F. Olale, J. T. Bennett, A. H. Brivanlou, and A. F. Schier. 2003. EGF-CFC proteins are essential coreceptors for the TGF-beta signals Vg1 and GDF1. Genes Dev. 17:31-36.
9. Ciardiello, F., R. Dono, N. Kim, M. G. Persico, and D. S. Salomon. 1991. Expression of cripto, a novel gene of the epidermal growth factor gene family, leads to in vitro transformation of a normal mouse mammary epithelial cell line. Cancer Res. 51:1051-1054.
10. Ciardiello, F., G. Tortora, C. Bianco, M. P. Selvam, F. Basolo, G. Fontanini, F. Pacifico, N. Normanno, R. Brandt, M. G. Persico, et al. 1994. Inhibition of CRIPTO expression and tumorigenicity in human colon cancer cells by antisense RNA and oligodeoxynucleotides. Oncogene 9:291-298.
11. Derynck, R., R. J. Akhurst, and A. Balmain. 2001. TGF-beta signaling in tumor suppression and cancer progression. Nat. Genet. 29:117-129.
12. Ding, J., L. Yang, Y. T. Yan, A. Chen, N. Desai, A. Wynshaw-Boris, and M. M. Shen. 1998. Cripto is required for correct orientation of the anterior-posterior axis in the mouse embryo. Nature 395:702-707.
13. Ebert, A. D., C. Wechselberger, S. Frank, B. Wallace-Jones, M. Seno, I. Martinez-Lacaci, C. Bianco, M. De Santis, H. K. Weitzel, and D. S. Salomon. 1999. Cripto-1 induces phosphatidylinositol 3′-kinase-dependent phosphorylation of AKT and glycogen synthase kinase 3beta in human cervical carcinoma cells. Cancer Res. 59:4502-4505.
14. Gray, P. C., J. Greenwald, A. L. Blount, K. S. Kunitake, C. J. Donaldson, S. Choe, and W. Vale. 2000. Identification of a binding site on the type II activin receptor for activin and inhibin. J. Biol. Chem. 275:3206-3212.
15. Gray, P. C., C. A. Harrison, and W. Vale. 2003. Cripto forms a complex with activin and type II activin receptors and can block activin signaling. Proc. Natl. Acad. Sci. USA 100:5193-5198.
16. Hanahan, D., and R. A. Weinberg. 2000. The hallmarks of cancer. Cell 100:57-70.
17. Harms, P. W., and C. Chang. 2003. Tomoregulin-1 (TMEFF1) inhibits nodal signaling through direct binding to the nodal coreceptor Cripto. Genes Dev. 17:2624-2629.
18. Harrison, C. A., P. C. Gray, S. C. Koerber, W. Fischer, and W. Vale. 2003. Identification of a functional binding site for activin on the type I receptor ALK4. J. Biol. Chem. 278:21129-21135.
19. Harrison, C. A., P. C. Gray, W. W. Vale, and D. M. Robertson. 2005. Antagonists of activin signaling: mechanisms and potential biological applications. Trends Endocrinol. Metab. 16:73-78.
20. Hogan, B. L. 1996. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10:1580-1594.
21. Iavarone, A., and J. Massague. 1997. Repression of the CDK activator Cdc25A and cell-cycle arrest by cytokine TGF-beta in cells lacking the CDK inhibitor p15. Nature 387:417-422.
22. Kannan, S., M. De Santis, M. Lohmeyer, D. J. Riese II, G. H. Smith, N. Hynes, M. Seno, R. Brandt, C. Bianco, G. Persico, N. Kenney, N. Normanno, I. Martinez-Lacaci, F. Ciardiello, D. F. Stern, W. J. Gullick, and D. S. Salomon. 1997. Cripto enhances the tyrosine phosphorylation of She and activates mitogen-activated protein kinase (MAPK) in mammary epithelial cells. J. Biol. Chem. 272:3330-3335.
23. Kirkbride, K. C., B. N. Ray, and G. C. Blobe. 2005. Cell-surface co-receptors: emerging roles in signaling and human disease. Trends Biochem. Sci. 30:611-621.
24. Lebrin, F., M. J. Goumans, L. Jonker, R. L. Carvalho, G. Valdimarsdottir, M. Thorikay, C. Mummery, H. M. Arthur, and P. ten Dijke. 2004. Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction. EMBO J. 23:4018-4028.
25. Lewis, K. A., P. C. Gray, A. L. Blount, L. A. MacConell, E. Wiater, L. M. Bilezikjian, and W. Vale. 2000. Betaglycan binds inhibin and can mediate functional antagonism of activin signalling. Nature 404:411-414.
26. Lohmeyer, M., P. M. Harrison, S. Kannan, M. DeSantis, N. J. O'Reilly, M. J. Sternberg, D. S. Salomon, and W. J. Gullick. 1997. Chemical synthesis, structural modeling, and biological activity of the epidermal growth factor-like domain of human cripto. Biochemistry 36:3837-3845.
27. López-Casillas, F., S. Cheifetz, J. Doody, J. L. Andres, W. S. Lane, and J. Massagué. 1991. Structure and expression of the membrane proteoglycan betaglycan, a component of the TGF-β receptor system. Cell 67:785-795.
28. López-Casillas, F., J. L. Wrana, and J. Massague. 1993. Betaglycan presents ligand to the TGF beta signaling receptor. Cell 73:1435-1444.
29. Massague, J. 1998. TGF-beta signal transduction. Annu. Rev. Biochem. 67:753-791.
30. Minchiotti, G., G. Manco, S. Parisi, C. T. Lago, F. Rosa, and M. G. Persico. 2001. Structure-function analysis of the EGF-CFC family member Cripto identifies residues essential for nodal signalling. Development 128:4501-4510.
31. Miyoshi, H., U. Blomer, M. Takahashi, F. H. Gage, and I. M. Verma. 1998. Development of a self-inactivating lentivirus vector. J. Virol. 72:8150-8157.
32. Niemeyer, C. C., M. G. Persico, and E. D. Adamson. 1998. Cripto: roles in mammary cell growth, survival, differentiation and transformation. Cell Death Differ. 5:440-449.
33. Normanne, N., A. De Luca, C. Bianco, M. R. Maiello, M. V. Carriero, A. Rehman, C. Wechselberger, C. Arra, L. Strizzi, M. Sanicola, and D. S. Salomon. 2004. Cripto-1 overexpression leads to enhanced invasiveness and resistance to anoikis in human MCF-7 breast cancer cells. J. Cell. Physiol. 198:31-39.
34. Onichtchouk, D., Y. G. Chen, R. Dosch, V. Gawantka, H. Delius, J. Massague, and C. Niehrs. 1999. Silencing of TGF-beta signalling by the pseudoreceptor BAMBI. Nature 401:480-485.
35. Pece-Barbara, N., S. Vera, K. Kathirkamathamby, S. Liebner, G. M. Di Guglielmo, E. Dejana, J. L. Wrana, and M. Letarte. 2005. Endoglin null endothelial cells proliferate faster and are more responsive to transforming growth factor beta 1 with higher affinity receptors and an activated Alk1 pathway. J. Biol. Chem. 280:27800-27808.
36. Rasmussen, S. B., E. Kordon, R. Callahan, and G. H. Smith. 2001. Evidence for the transforming activity of a truncated Int6 gene, in vitro. Oncogene 20:5291-5301.
37. Roberts, A. B., and L. M. Wakefield. 2003. The two faces of transforming growth factor beta in carcinogenesis. Proc. Natl. Acad. Sci. USA 100:8621-8623.
38. Schier, A. F. 2003. Nodal signaling in vertebrate development. Annu. Rev. Cell Dev. Biol. 19:589-621.
39. Seton-Rogers, S. E., and J. S. Brugge. 2004. ErbB2 and TGF-beta: a cooperative role in mammary tumor progression? Cell Cycle 3:597-600.
40. Shen, M. M. 2003. Decrypting the role of Cripto in tumorigenesis. J. Clin. Investig. 112:500-502.
41. Shen, M. M., and A. F. Schier. 2000. The EGF-CFC gene family in vertebrate development. Trends Genet. 16:303-309.
42. Shi, Y., and J. Massague. 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113:685-700.
43. Siegel, P. M., and J. Massague. 2003. Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat. Rev. Cancer 3:807-821.
44. Singer, O., R. A. Marr, E. Rockenstein, L. Crews, N. G. Coufal, F. H. Gage, I. M. Verma, and E. Masliah. 2005. Targeting BACE1 with siRNAs ameliorates Alzheimer disease neuropathology in a transgenic model. Nat. Neurosci. 8:1343-1349.
45. Soule, H. D., T. M. Maloney, S. R. Wolman, W. D. Peterson, Jr., R. Brenz, C. M. McGrath, J. Russo, R. J. Pauley, R. F. Jones, and S. C. Brooks. 1990. Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res. 50:6075-6086.
46. Strizzi, L., C. Bianco, N. Normanno, and D. Salomon. 2005. Cripto-1: a multifunctional modulator during embryogenesis and oncogenesis. Oncogene 24:5731-5741.
47. Tian, F., S. D. Byfield, W. T. Parks, C. H. Stuelten, D. Nemani, Y. E. Zhang, and A. B. Roberts. 2004. Smad-binding defective mutant of transforming growth factor beta type I receptor enhances tumorigenesis but suppresses metastasis of breast cancer cell lines. Cancer Res. 64:4523-4530.
48. Tian, F., S. DaCosta Byfield, W. T. Parks, S. Yoo, A. Felici, B. Tang, E. Piek, L. M. Wakefield, and A. B. Roberts. 2003. Reduction in Smad2/3 signaling enhances tumorigenesis but suppresses metastasis of breast cancer cell lines. Cancer Res. 63:8284-8292.
49. Wakefield, L. M., and A. B. Roberts. 2002. TGF-beta signaling: positive and negative effects on tumorigenesis. Curr. Opin. Genet. Dev. 12:22-29.
50. Wang, X. F., H. Y. Lin, E. E. Ng, J. Downward, H. F. Lodish, and R. A. Weinberg. 1991. Expression cloning and characterization of the TGF-beta type III receptor. Cell 67:797-805.
51. Wechselberger, C., A. D. Ebert, C. Bianco, N. I. Khan, Y. Sun, B. Wallace-Jones, R. Montesano, and D. S. Salomon, 2001. Cripto-1 enhances migration and branching morphogenesis of mouse mammary epithelial cells. Exp. Cell Res. 266:95-105.
52. Wechselberger, C., L. Strizzi, N. Kenney, M. Hirota, Y. Sun, A. Ebert, O. Orozco, C. Bianco, N. I. Khan, B. Wallace-Jones, N. Normanno, H. Adkins, M. Sanicola, and D. S. Salomon. 2005. Human Cripto-1 overexpression in the mouse mammary gland results in the development of hyperplasia and adenocarcinoma. Oncogene 24:4094-4105.
53. Welt, C., Y. Sidis, H. Keutmann, and A. Schneyer. 2002. Activins, inhibins, and follistatins: from endocrinology to signaling. A paradigm for the new millennium. Exp. Biol. Med. (Maywood) 227:724-752.
54. Wiater, E., and W. Vale. 2003. Inhibin is an antagonist of bone morphogenetic protein signaling. J. Biol. Chem. 278:7934-7941.
55. Wrana, J. L., L. Attisano, J. Carcamo, A. Zentella, J. Doody, M. Laiho, X. F. Wang, and J. Massague. 1992. TGF beta signals through a heteromeric protein kinase receptor complex. Cell 71:1003-1014.
56. Wrana, J. L., L. Attisano, R. Wieser, F. Ventura, and J. Massague. 1994. Mechanism of activation of the TGF-beta receptor. Nature 370:341-347.
57. Xing, P. X., X. F. Hu, G. A. Pietersz, H. L. Hosick, and I. F. McKenzie. 2004. Cripto: a novel target for antibody-based cancer immunotherapy. Cancer Res. 64:4018-4023.
58. Xu, C., G. Liguori, M. G. Persico, and E. D. Adamson. 1999. Abrogation of the Cripto gene in mouse leads to failure of postgastrulation morphogenesis and lack of differentiation of cardiomyocytes. Development 126:483-494.
59. Yan, Y.-T., J.-J. Liu, Y. Luo, E. Chaosu, R. S. Haltiwanger, C. Abate-Shen, and M. M. Shen. 2002. Dual roles of Cripto as a ligand and coreceptor in the nodal signaling pathway. Mol. Cell. Biol. 22:4439-4449.
60. Yeo, C., and M. Whitman. 2001. Nodal signals to Smads through Cripto-dependent and Cripto-independent mechanisms. Mol. Cell 7:949-957.