Secreted antagonists of the Wnt signalling pathway

Journal of Cell Science

Volumn 116, Issue 13, 2003, Pages 2627-2634

  Kawano, Yoshiaki ^a   Kypta, Robert ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Cerberus; Dickkopf; Frizzled; Wnt

Indexed keywords

CELL PROTEIN; PROTEIN SFRP; RECEPTOR SUBUNIT; UNCLASSIFIED DRUG; WNT PROTEIN;

HUMAN; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FAMILY; PROTEIN INTERACTION; RECEPTOR BINDING; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CARRIER PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; PROTEINS; PROTO-ONCOGENE PROTEINS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; WNT PROTEINS; XENOPUS PROTEINS; ZEBRAFISH PROTEINS;

CERBERUS;

EID: 0038783316     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00623     Document Type: Review

References (81)

1. Abu-Jawdeh, G., Comella, N., Tomita, Y., Brown, L. F., Tognazzi, K., Sokol, S. Y. and Kocher, O. (1999). Differential expression of frpHE: a novel human stromal protein of the secreted frizzled gene family, during the endometrial cycle and malignancy. Lab. Invest. 79, 439-447.
2. Aravind, L. and Koolin, E. V. (1998). A colipase fold in the carboxy-terminal domain of the Wnt antagonists - the Dickkopfs. Curr. Biol. 8, R477-R478.
3. Bafico, A., Gazit, A., Pramila, T., Finch, P. W., Yaniv, A. and Aaronson, S. A. (1999). Interaction of frizzled related protein (FRP) with Wnt ligands and the frizzled receptor suggests alternative mechanisms for FRP inhibition of Wnt signaling. J. Biol. Chem. 274, 16180-16187.
4. Bafico, A., Liu, G., Yaniv, A., Gazit, A. and Aaronson, S. A. (2001). Novel mechanism of Wnt signalling inhibition mediated by Dickkopf-1 interaction with LRP6/Arrow. Nat. Cell Biol. 3, 683-686.
5. Banyai, L. and Patthy, L. (1999). The NTR module: domains of netrins, secreted frizzled related proteins, and type I procollagen C-proteinase enhancer protein are homologous with tissue inhibitors of metalloproteases. Protein Sci. 8, 1636-1642.
6. Bell, E., Munoz-Sanjuan, I., Altmann, C. R., Vonica, A. and Brivanlou, A.H. (2003). Cell fate specification and competence by Coco, a maternal BMP, TGFbeta and Wnt inhibitor. Development 130, 1381-1389.
7. Belo, J. A., Bachiller, D., Agius, E., Kemp, C., Borges, A. C., Marques, S., Piccolo, S. and de Robertis, E. M. (2000). Cerberus-like is a secreted BMP and nodal antagonist not essential for mouse development. Genesis 26, 265-270.
8. Biben, C., Stanley, E., Fabri, L., Kotecha, S., Rhinn, M., Drinkwater, C., Lah, M., Wang, C. C., Nash, A., Hilton, D. et al. (1998). Murine cerberus homologue mCer-1: a candidate anterior patterning molecule. Dev. Biol. 194, 135-151.
9. Bouwmeester, T., Kim, S., Sasai, Y., Lu, B. and de Robertis, E. M. (1996). Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer. Nature 382, 595-601.
10. Boyden, L. M., Mao, J., Belsky, J., Mitzner, L., Farhi, A., Mitnick, M. A., Wu, D., Insogna, K. and Lifton, R. P. (2002). High bone density due to a mutation in LDL-receptor-related protein 5. N. Engl. J. Med. 346, 1513-1521.
11. Bradley, L., Sun, B., Collins-Racie, L., La Vallie, E., McCoy, J. and Sive, H. (2000). Different activities of the frizzled-related proteins frzb2 and sizzled2 during Xenopus anteroposterior patterning. Dev. Biol. 227, 118-132.
12. Brott, B. K. and Sokol, S. Y. (2002). Regulation of Wnt/LRP signaling by distinct domains of Dickkopf proteins. Mol. Cell. Biol. 22, 6100-6110.
13. Collavin, L. and Kirschner, M. W. (2003). The secreted Frizzled-related protein Sizzled functions as a negative feedback regulator of extreme ventral mesoderm. Development 130, 805-816.
14. Davidson, G., Mao, B., del Barco Barrantes, I. and Niehrs, C. (2002). Kremen proteins interact with Dickkopf1 to regulate anteroposterior CNS patterning. Development 129, 5587-5596.
15. Dufourcq, P., Couffinhal, T., Ezan, J., Barandon, L., Moreau, C., Daret, D. and Duplaa, C. (2002). FrzA, a secreted frizzled related protein, induced angiogenic response. Circulation 106, 3097-3103.
16. Duplaa, C., Jaspard, B., Moreau, C. and D'Amore, P. A. (1999). Identification and cloning of a secreted protein related to the cysteine-rich domain of frizzled. Evidence for a role in endothelial cell growth control. Circ. Res. 84, 1433-1445.
17. Fedi, P., Bafico, A., Nieto Soria, A., Burgess, W. H., Miki, T., Bottaro, D. P., Kraus, M. H. and Aaronson, S. A. (1999). Isolation and biochemical characterization of the human Dkk-1 homologue, a novel inhibitor of mammalian Wnt signaling. J. Biol. Chem. 274, 19465-19472.
18. Finch, P. W., He, X., Kelley, M. J., Uren, A., Schaudies, R. P., Popescu, N. C., Rudikoff, S., Aaronson, S. A., Varmus, H. E. and Rubin, J. S. (1997). Purification and molecular cloning of a secreted, Frizzled-related antagonist of Wnt action. Proc. Natl. Acad. Sci. USA 94, 6770-6775.
19. Glinka, A., Wu, W., Delius, H., Monaghan, A. P., Blumenstock, C. and Niehrs, C. (1998). Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 391, 357-362.
20. Grotewold, L. and Ruther, U. (2002). Bmp, Fgf and Wnt signalling in programmed cell death and chondrogenesis during vertebrate limb development: the role of Dickkopf-1. Int. J. Dev. Biol. 46, 943-947.
21. He, X., Saint-Jeannet, J. P., Wang, Y., Nathans, J., Dawid, I. and Varmus, H. (1997). A member of the Frizzled protein family mediating axis induction by Wnt-5A. Science 275, 1652-1654.
22. Heisenberg, C. P., Tada, M., Rauch, G. J., Saude, L., Concha, M. L., Geisler, R., Stemple, D. L., Smith, J. C. and Wilson, S. W. (2000). Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405, 76-81.
23. Hoang, B., Moos, M., Jr., Vukicevic, S. and Luyten, F. P. (1996). Primary structure and tissue distribution of FRZB, a novel protein related to Drosophila frizzled, suggest a role in skeletal morphogenesis. J. Biol. Chem. 271, 26131-26137.
24. Hsieh, J. C., Kodjabachian, L., Rebbert, M. L., Rattner, A., Smallwood, P. M., Samos, C. H., Nusse, R., Dawid, I. B. and Nathans, J. (1999). A new secreted protein that binds to Wnt proteins and inhibits their activities. Nature 398, 431-436.
25. Illies, M. R., Peeler, M. T., Dechtiaruk, A. and Ettensohn, C. A. (2002). Cloning and developmental expression of a novel, secreted frizzled-related protein from the sea urchin, Strongylocentrotus purpuratus. Mech. Dev. 113, 61-64.
26. Ishitani, T., Kishida, S., Hyodo-Miura, J., Ueno, N., Yasuda, J., Waterman, M., Shibuya, H., Moon, R. T., Ninomiya-Tsuji, J. and Matsumoto, K. (2003). The TAK1-NLK mitogen-activated protein kinase cascade functions in the Wnt-5a/Ca(2+) pathway to antagonize Wnt/beta-catenin signaling. Mol. Cell. Biol. 23, 131-139.
27. Jones, S. E. and Jomary, C. (2002). Secreted Frizzled-related proteins: searching for relationships and patterns. Bioessays 24, 811-820.
28. Jones, S. E., Jomary, C., Grist, J., Stewart, H. J. and Neal, M. J. (2000). Modulated expression of secreted frizzled-related proteins in human retinal degeneration. Neuroreport 11, 3963-3967.
29. Kaneko, K. J. and DePamphilis, M. L. (2000). Soggy, a spermatocyte-specific gene, lies 3.8 kb upstream of and antipodal to TEAD-2, a transcription factor expressed at the beginning of mouse development. Nucleic Acids Res. 28, 3982-3990.
30. Kato, M., Patel, M. S., Levasseur, R., Lobov, I., Chang, B. H., Glass, D. A. 2nd, Hartmann, C., Li, L., Hwang, T. H., Brayton, C. F. et al. (2002). Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J. Cell Biol. 157, 303-314.
31. Kim, A. S., Lowenstein, D. H. and Pleasure, S. J. (2001). Wnt receptors and Wnt inhibitors are expressed in gradients in the developing telencephalon. Mech. Dev. 103, 167-172.
32. Ko, J., Ryu, K. S., Lee, Y. H., Na, D. S., Kim, Y. S., Oh, Y. M., Kim, I. S. and Kim, J. W. (2002). Human secreted frizzled-related protein is downregulated and induces apoptosis in human cervical cancer. Exp. Cell Res. 280, 280-287.
33. Krupnik, V. E., Sharp, J. D., Jiang, C., Robison, K., Chickering, T. W., Amaravadi, L., Brown, D. E., Guyot, D., Mays, G., Leiby, K. et al. (1999). Functional and structural diversity of the human Dickkopf gene family. Gene 238, 301-313.
34. 2+ pathway: a new vertebrate Wnt signaling pathway takes shape. Trends Genet. 16, 279-283.
35. 2+ signaling. Mech. Dev. 106, 61-76.
36. Ladher, R. K., Church, V. L., Allen, S., Robson, L., Abdelfattah, A., Brown, N. A., Hattersley, G., Rosen, V., Luyten, F. P., Dale, L. and Francis-West, P. H. (2000). Cloning and expression of the Wnt antagonists Sfrp-2 and Frzb during chick development. Dev. Biol. 218, 183-198.
37. Lescher, B., Haenig, B. and Kispert, A. (1998), sFRP-2 is a target of the Wnt-4 signaling pathway in the developing metanephric kidney. Dev. Dyn. 213, 440-451.
38. Leyns, L., Bouwmeester, T., Kim, S. H., Piccolo, S. and de Robertis, E. M. (1997). Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. Cell 88, 747-756.
39. Li, L., Mao, J., Sun, L., Liu, W. and Wu, D. (2002). Second cysteine-rich domain of Dickkopf-2 activates canonical Wnt signaling pathway via LRP-6 independently of dishevelled. J. Biol. Chem. 277, 5977-5981.
40. Lin, K., Wang, S., Julius, M. A., Kitajewski, J., Moos, M., Jr and Luyten, F. P. (1997). The cysteine-rich frizzled domain of Frzb-1 is required and sufficient for modulation of Wnt signaling. Proc. Natl. Acad. Sci. USA 94, 11196-11200.
41. Little, R. D., Carulli, J. P., del Mastro, R. G., Dupuis, J., Osborne, M., Folz, C., Manning, S. P., Swain, P. M., Zhao, S. C., Eustace, B. et al. (2002). A mutation in the LDL receptor-related protein 5 gene results in the autosomal dominant high-bone-mass trait. Am. J. Hum. Genet. 70, 11-19.
42. Mao, B. and Niehrs, C. (2003). Kremen2 modulates Dickkopf2 activity during Wnt/1RP6 signaling. Gene 302, 179-183.
43. Mao, B., Wu, W., Li, Y., Hoppe, D., Stannek, P., Glinka, A. and Niehrs, C. (2001). LDL-receptor-related protein 6 is a receptor for Dickkopf proteins. Nature 411, 321-325.
44. Mao, B., Wu, W., Davidson, G., Marhold, J., Li, M., Mechler, B. M., Delius, H., Hoppe, D., Stannek, P., Walter, C. et al. (2002). Kremen proteins are Dickkopf receptors that regulate Wnt/beta-catenin signalling. Nature 417, 664-667.
45. Mao, J., Wang, J., Liu, B., Pan, W., Farr, G. H., 3rd, Flynn, C., Yuan, H., Takada, S., Kimelman, D., Li, L. and Wu, D. (2001). Low-density lipoprotein receptor-related protein-5 binds to Axin and regulates the canonical Wnt signaling pathway. Mol. Cell 7, 801-809.
46. Mayr, T., Deutsch, U., Kuhl, M., Drexler, H. C., Lottspeich, F., Deutzmann, R., Wedlich, D. and Risau, W. (1997). Fritz: a secreted frizzled-related protein that inhibits Wnt activity. Mech. Dev. 63, 109-125.
47. Melkonyan, H. S., Chang, W. C., Shapiro, J. P., Mahadevappa, M., Fitzpatrick, P. A., Kiefer, M. C., Tomei, L. D. and Umansky, S. R. (1997). SARPs: a family of secreted apoptosis-related proteins. Proc. Natl. Acad. Sci. USA 94, 13636-13641.
48. Miller, J. R. (2001). The Wnts. Genome Biol. 3, reviews3001.1-3001.15.
49. Mukhopadhyay, M., Shtrom, S., Rodriguez-Esteban, C., Chen, L., Tsukui, T., Gomer, L., Dorward, D. W., Glinka, A., Grinberg, A., Huang, S. P. et al. (2001). Dickkopf1 is required for embryonic head induction and limb morphogenesis in the mouse. Dev. Cell 1, 423-434.
50. Niehrs, C., Kazanskaya, O., Wu, W. and Glinka, A. (2001). Dickkopf1 and the Spemann-Mangold head organizer. Int. J. Dev. Biol. 45, 237-240.
51. Pandur, P., Lasche, M., Eisenberg, L. M. and Kuhl, M. (2002). Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis. Nature 418, 636-641.
52. Patthy, L. (2000). The WIF module. Trends Biochem. Sci. 25, 12-13.
53. Pera, E. M. and de Robertis, E. M. (2000). A direct screen for secreted proteins in Xenopus embryos identifies distinct activities for the Wnt antagonists Crescent and Frzb-1. Mech. Dev. 96, 183-195.
54. Pfeffer, P. L., de Robertis, E. M. and Izpisua-Belmonte, J. C. (1997). Crescent, a novel chick gene encoding a Frizzled-like cysteine-rich domain, is expressed in anterior regions during early embryogenesis. Int. J. Dev. Biol. 41, 449-458.
55. Piccolo, S., Agius, E., Leyns, L., Bhattacharyya, S., Grunz, H., Bouwmeester, T. and de Robertis, E. M. (1999). The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals. Nature 397, 707-710.
56. Pinson, K. I., Brennan, J., Monkley, S., Avery, B. J. and Skarnes, W. C. (2000). An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 407, 535-538.
57. Rattner, A., Hsieh, J. C., Smallwood, P. M., Gilbert, D. J., Copeland, N. G., Jenkins, N. A. and Nathans, J. (1997). A family of secreted proteins contains homology to the cysteine-rich ligand-binding domain of frizzled receptors. Proc. Natl. Acad. Sci. USA 94, 2859-2863.
58. Roth, W., Wild-Bode, C., Platten, M., Grimmel, C., Melkonyan, H. S., Dichgans, J. and Weller, M. (2000). Secreted Frizzled-related proteins inhibit motility and promote growth of human malignant glioma cells. Oncogene 19, 4210-4220.
59. Salic, A. N., Kroll, K. L., Evans, L. M. and Kirschner, M. W. (1997). Sizzled: a secreted Xwnt8 antagonist expressed in the ventral marginal zone of Xenopus embryos. Development 124, 4739-4748.
60. Semenov, M. V., Tamai, K., Brott, B. K., Kuhl, M., Sokol, S. and He, X. (2001). Head inducer Dickkopf-1 is a ligand for Wnt coreceptor LRP6. Curr. Biol. 11, 951-961.
61. Shou, J., Ali-Osman, F., Multani, A. S., Pathak, S., Fedi, P. and Srivenugopal, K. S. (2002). Human Dkk-1, a gene encoding a Wnt antagonist, responds to DNA damage and its overexpression sensitizes brain tumor cells to apoptosis following alkylation damage of DNA. Oncogene 21, 878-889.
62. Suzuki, H., Gabrielson, E., Chen, W., Anbazhagan, R., van Engeland, M., Weijenberg, M. P., Herman, J. G. and Baylin, S. B. (2002). A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nat. Genet. 31, 141-149.
63. Tamai, K., Semenov, M., Kato, Y., Spokony, R., Liu, C., Katsuyama, Y., Hess, F., Saint-Jeannet, J. P. and He, X. (2000). LDL-receptor-related proteins in Wnt signal transduction. Nature 407, 530-535.
64. Torres, M. A., Yang-Snyder, J. A., Purcell, S. M., DeMarais, A. A., McGrew, L. L. and Moon, R. T. (1996). Activities of the Wnt-1 class of secreted signaling factors are antagonized by the Wnt-5A class and by a dominant negative cadherin in early Xenopus development. J. Cell Biol. 133, 1123-1137.
65. Tsuji, T., Miyazaki, M., Sakaguchi, M., Inoue, Y. and Namba, M. (2000). A REIC gene shows down-regulation in human immortalized cells and human tumor-derived cell lines. Biochem. Biophys. Res. Commun. 268, 20-24.
66. Tsuji, T., Nozaki, I., Miyazaki, M., Sakaguchi, M., Pu, H., Hamazaki, Y., Iijima, O. and Namba, M. (2001). Antiproliferative activity of REIC/Dkk-3 and its significant down-regulation in non-small-cell lung carcinomas. Biochem. Biophys. Res. Commun. 289, 257-263.
67. Ugolini, F., Charafe-Jauffret, E., Bardou, V. J., Geneix, J., Adelaide, J., Labat-Moleur, F., Penault-Llorca, F., Longy, M., Jacquemier, J., Birnbaum, D. and Pebusque, M. J. (2001). WNT pathway and mammary carcinogenesis: loss of expression of candidate tumor suppressor gene SFRP1 in most invasive carcinomas except of the medullary type. Oncogene 20, 5810-5817.
68. Uren, A., Reichsman, F., Anest, V., Taylor, W. G., Muraiso, K., Bottaro, D. P., Cumberledge, S. and Rubin, J. S. (2000). Secreted frizzled-related protein-1 binds directly to Wingless and is a biphasic modulator of Wnt signaling. J. Biol. Chem. 275, 4374-4382.
69. van Tilbeurgh, H., Bezzine, S., Cambillau, C., Verger, R. and Carriere, F. (1999). Colipase: structure and interaction with pancreatic lipase. Biochim. Biophys. Acta 1441, 173-184.
70. Wang, S., Krinks, M., Lin, K., Luyten, F. P. and Moos, M., Jr. (1997a). Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8. Cell 88, 757-766.
71. Wang, S., Krinks, M. and Moos, M., Jr. (1997b). Frzb-1, an antagonist of Wnt-1 and Wnt-8, does not block signaling by Wnts -3A, -5A, or -11. Biochem. Biophys. Res. Commun. 236, 502-504.
72. Wang, J., Shou, J. and Chen, X. (2000). Dickkopf-1, an inhibitor of the Wnt signaling pathway, is induced by p53. Oncogene 19, 1843-1848.
73. Wehrli, M., Dougan, S. T., Caldwell, K., O'Keefe, L., Schwartz, S., Vaizel-Ohayon, D., Schejter, E., Tomlinson, A. and DiNardo, S. (2000). arrow encodes an LDL-receptor-related protein essential for Wingless signalling. Nature 407, 527-530.
74. Willert, K., Brown, J. D., Danenberg, E., Duncan, A. W., Weissman, I. L., Reya, T., Yates, J. R. and Nusse, R. (2003). Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature Apr. 27 [epub ahead of print].
75. Wright, K., Wilson, P. J., Kerr, J., Do, K., Hurst, T., Khoo, S. K., Ward, B. and Chenevix-Trench, G. (1998). Frequent loss of heterozygosity and three critical regions on the short arm of chromosome 8 in ovarian adenocarcinomas. Oncogene 17, 1185-1188.
76. Wu, W., Glinka, A., Delius, H. and Niehrs, C. (2000). Mutual antagonism between dickkopf1 and dickkopf2 regulates Wnt/beta-catenin signalling. Curr. Biol. 10, 1611-1614.
77. Xu, Q., D'Amore, P. A. and Sokol, S. Y. (1998). Functional and biochemical interactions of Wnts with FrzA, a secreted Wnt antagonist. Development 125, 4767-4776.
78. Yamaguchi, T. P. (2001). Heads or tails: Wnts and anterior-posterior patterning. Curr. Biol. 11, R713-R724.
79. Yoshikawa, S., McKinnon, R. D., Kokel, M. and Thomas, J. B. (2003). Wnt-mediated axon guidance via the Drosophila Derailed receptor. Nature 422, 583-588.
80. Yoshino, K., Rubin, J. S., Higinbotham, K. G., Uren, A., Anest, V., Plisov, S. Y. and Perantoni, A. O. (2001). Secreted Frizzled-related proteins can regulate metanephric development. Mech. Dev. 102, 45-55.
81. Zhou, Z., Wang, J., Han, X., Zhou, J. and Linder, S. (1998). Up-regulation of human secreted frizzled homolog in apoptosis and its down-regulation in breast tumors. Int. J. Cancer 78, 95-99.