The making of Wnt: New insights into Wnt maturation, sorting and secretion

Development

Volumn 134, Issue 1, 2007, Pages 3-12

  Coudreuse, Damien ^a   Korswagen, Hendrik C ^a  

^a HUBRECHT INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPROTEIN; MEMBRANE PROTEIN; RECEPTOR PROTEIN; REGULATOR PROTEIN; WNT PROTEIN; WNT1 PROTEIN; WNT11 PROTEIN; WNT2 PROTEIN; WNT3 PROTEIN; WNT3A PROTEIN; WNT4 PROTEIN; WNT5A PROTEIN;

CELL COMPARTMENTALIZATION; COMPLEX FORMATION; CULTURE MEDIUM; DOWNSTREAM PROCESSING; EMBRYO DEVELOPMENT; ENDOPLASMIC RETICULUM; INTRACELLULAR TRANSPORT; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; TRANSCYTOSIS;

ANIMALS; CYSTEINE; ENDOPLASMIC RETICULUM; ENDOSOMES; GLYCOPROTEINS; MODELS, BIOLOGICAL; MOLECULAR WEIGHT; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 33846468965     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02699     Document Type: Review

References (60)

1. Arighi, C. N., Hartnell, L. M., Aguilar, R. C., Haft, C. R. and Bonifacino, J. S. (2004). Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell Biol. 165, 123-133.
2. Baeg, G. H., Lin, X., Khare, N., Baumgartner, S. and Perrimon, N. (2001). Heparan sulfate proteoglycans are critical for the organization of the extracellular distribution of Wingless. Development 128, 87-94.
3. Banziger, C., Soldini, D., Schutt, C., Zipperlen, P., Hausmann, G. and Basler, K. (2006). Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell 125, 509-522.
4. Bartscherer, K., Pelte, N., Ingelfinger, D. and Boutros, M. (2006). Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell 125, 523-533.
5. Bienz, M. and Clevers, H. (2000). Linking colorectal cancer to Wnt signaling. Cell 103, 311-320.
6. Bijlmakers, M. J. and Marsh, M. (2003). The on-off story of protein palmitoylation. Trends Cell. Biol. 13, 32-42.
7. Burrus, L. W. and McMahon, A. P. (1995). Biochemical analysis of murine Wnt proteins reveals both shared and distinct properties. Exp. Cell Res. 220, 363-373.
8. Cadigan, K. M. (2002). Regulating morphogen gradients in the Drosophila wing. Semin. Cell Dev Biol. 13, 83-90.
9. Cadigan, K. M. and Nusse, R. (1997). Wnt signaling: a common theme in animal development. Genes Dev 11, 3286-3305.
10. Cadigan, K. M. and Liu, Y. I. (2006). Wnt signaling: complexity at the surface. J. Cell Sci. 119, 395-402.
11. Coudreuse, D. Y., Roel, G., Betist, M. C., Destree, O. and Korswagen, H. C. (2006). Wnt gradient formation requires retromer function in Wnt-producing cells. Science 312, 921-924.
12. Dhanvantari, S. and Loh, Y. P. (2000). Lipid raft association of carboxypeptidase E is necessary for its function as a regulated secretory pathway sorting receptor. J. Biol. Chem. 275, 29887-29893.
13. Eaton, S. (2006). Release and trafficking of lipid-linked morphogens. Curr Opin. Genet. Dev 16, 17-22.
14. Eisenmann, D. M. and Kim, S. K. (2000). Protruding vulva mutants identify novel loci and Wnt signaling factors that function during Caenorhabditis elegans vulva development. Genetics 156, 1097-1116.
15. Gallet, A., Rodriguez, R., Ruel, L. and Therond, P. P. (2003). Cholesterol modification of hedgehog is required for trafficking and movement, revealing an asymmetric cellular response to hedgehog. Dev Cell 4, 191-204.
16. Gething, M. J. and Sambrook, J. (1990). Transport and assembly processes in the endoplasmic reticulum. Semin. Cell Biol. 1, 65-72.
17. Giraldez, A. J., Copley, R. R. and Cohen, S. M. (2002). HSPG modification by the secreted enzyme Notum shapes the Wingless morphogen gradient. Dev Cell 2, 667-676.
18. Gonzalez, F., Swales, L., Bejsovec, A., Skaer, H. and Martinez Arias, A. (1991). Secretion and movement of wingless protein in the epidermis of the Drosophila embryo. Mech. Dev 35, 43-54.
19. Han, C., Yan, D., Belenkaya, T. Y. and Lin, X. (2005). Drosophila glypicans Dally and Dally-like shape the extracellular Wingless morphogen gradient in the wing disc. Development 132, 667-679.
20. Harris, J., Honigberg, L., Robinson, N. and Kenyon, C. (1996). Neuronal cell migration in C. elegans: regulation of Hox gene expression and cell position. Development 122, 3117-3131.
21. He, X., Semenov, M., Tamai, K. and Zeng, X. (2004). LDL receptor-related proteins 5 and 6 in Wntβ-catenin signaling: arrows point the way. Development 131, 1663-1677.
22. Hurtley, S. M., Bole, D. G., Hoover-Litty, H., Helenius, A. and Copeland, C. S. (1989). Interactions of misfolded influenza virus hemagglutinin with binding protein (BiP). J. Cell Biol. 108, 2117-2126.
23. Ikonen, E. (2001). Roles of lipid rafts in membrane transport. Curr. Opin. Cell Biol. 13, 470-477.
24. Kadowaki, I., Wilder, E., Klingensmith, J., Zachary, K. and Perrimon, N. (1996). The segment polarity gene porcupine encodes a putative multitransmembrane protein involved in Wingless processing. Genes Dev 10, 3116-3128.
25. Kassenbrock, C. K., Garcia, P. D., Walter, P. and Kelly, R. B. (1988). Heavy-chain binding protein recognizes aberrant polypeptides translocated in vitro. Nature 333, 90-93.
26. Kiecker, C. and Niehrs, C. (2001). A morphogen gradient of Wnt/ β-catenin signalling regulates anteroposterior neural patterning in Xenopus. Development 128, 4189-4201.
27. Kirkpatrick, C. A., Dimitroff, B. D., Rawson, J. M. and Selleck, S. B. (2004). Spatial regulation of Wingless morphogen distribution and signaling by Dally-like protein. Dev Cell 7, 513-523.
28. Kitajewski, J., Mason, J. O. and Varmus, H. E. (1992). Interaction of Wnt-1 proteins with the binding protein BiP. Mol. Cell. Biol. 12, 784-790.
29. Kreuger, J., Perez, L., Giraldez, A. J. and Cohen, S. M. (2004). Opposing activities of Dally-like glypican at high and low levels of Wingless morphogen activity. Dev Cell 7, 503-512.
30. Kusserow, A., Pang, K., Sturm, C., Hrouda, M., Lentfer, J., Schmidt, H. A., Technau, U., von Haeseler, A., Hobmayer, B., Martindale, M. Q. et al. (2005). Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433, 156-160.
31. Lander, A. D., Nie, Q. and Wan, F. Y. (2002). Do morphogen gradients arise by diffusion? Dev Cell 2, 785-796.
32. Logan, C. Y. and Nusse, R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev Cell Dev. Biol. 20, 781-810.
33. Mason, J. O., Kitajewski, J. and Varmus, H. E. (1992). Mutational analysis of mouse Wnt-1 identifies two temperature-sensitive alleles and attributes of Wnt-1 protein essential for transformation of a mammary cell line. Mol. Biol. Cell 3, 521-533.
34. McMahon, A. P. and Moon, R. T. (1989). int-1, a proto-oncogene involved in cell signalling. Development 107 Suppl, 161-167.
35. Miller, J. R. (2002). The Wnts. Genome Biol. 3, REVIEWS3001.
36. Moon, R. T., Bowerman, B., Boutros, M. and Perrimon, N. (2002). The promise and perils of Wnt signaling through β-catenin. Science 296, 1644-1646.
37. Neumann, C. J. and Cohen, S. M. (1997). Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing. Development 124, 871-880.
38. Nothwehr, S. F., Ha, S. A. and Bruinsma, R (2000). Sorting of yeast membrane proteins into an endosome-to-Golgi pathway involves direct interaction of their cytosolic domains with Vps35p. J. Cell Biol. 151, 297-310.
39. Nusse, R. (2003). Wnts and Hedgehogs: lipid-modified proteins and similarities in signaling mechanisms at the cell surface. Development 130, 5297-5305.
40. Panakova, D., Sprong, H., Marois, E., Thiele, C. and Eaton, S. (2005). Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature 435, 58-65.
41. Paravicini, G., Horazdovsky, B. F. and Emr, S. D. (1992). Alternative pathways for the sorting of soluble vacuolar proteins in yeast: a vps35 null mutant missorts and secretes only a subset of vacuolar hydrolases. Mol. Biol. Cell 3, 415-427.
42. Pfeiffer, S., Ricardo, S., Manneville, J. B., Alexandre, C. and Vincent, J. P. (2002). Producing cells retain and recycle Wingless in Drosophila embryos. Curr. Biol. 12, 957-962.
43. Prasad, B. C. and Clark, S. G. (2006). Wnt signaling establishes anteroposterior neuronal polarity and requires retromer in C elegans. Development 133, 1757-1766.
44. Riggleman, B., Schedl, P. and Wieschaus, E. (1990). Spatial expression of the Drosophila segment polarity gene armadillo is posttranscriptionally regulated by wingless. Cell 63, 549-560.
45. Schmidt, K., Schrader, M., Kern, H. F. and Kleene, R. (2001). Regulated apical secretion of zymogens in rat pancreas. Involvement of the glycosylphosphatidylinositol-anchored glycoprotein GP-2, the lectin ZG16p, and cholesterol-glycosphingolipid-enriched microdomains. J. Biol. Chem. 276, 14315-14323.
46. Seaman, M. N., Marcusson, E. G., Cereghino, J. L. and Emr, S. D. (1997). Endosome to Golgi retrieval of the vacuolar protein sorting receptor, Vps10p, requires the function of the VPS29, VPS30, and VPS35 gene products. J. Cell Biol. 137, 79-92.
47. Seaman, M. N., McCaffery, J. M. and Emr, S. D. (1998). A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J. Cell Biol. 142, 665-681.
48. St-Arnaud, R., Craig, J., McBurney, M. W. and Papkoff, J. (1989). The int-1 proto-oncogene is transcriptionally activated during neuroectodermal differentiation of P19 mouse embryonal carcinoma cells. Oncogene 4, 1077-1080.
49. Strigini, M. and Cohen, S. M. (2000). Wingless gradient formation in the Drosophila wing. Curr. Biol.10, 293-300.
50. Tanaka, K., Kitagawa, Y. and Kadowaki, T. (2002). Drosophila segment polarity gene product porcupine stimulates the posttranslational N-glycosylation of wingless in the endoplasmic reticulum. J. Biol. Chem. 277, 12816-12823.
51. Thorpe, C. J., Schlesinger, A., Carter, J. C. and Bowerman, B. (1997). Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell 90, 695-705.
52. van den Heuvel, M., Nusse, R., Johnston, R and Lawrence, R A. (1989). Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication. Cell 59, 739-749.
53. van den Heuvel, M., Harryman-Samos, C., Klingensmith, J., Perrimon, N. and Nusse, R. (1993). Mutations in the segment polarity genes wingless and porcupine impair secretion of the wingless protein. EMBO J. 12, 5293-5302.
54. van Es, J. H., Barker, N. and Clevers, H. (2003). You Wnt some, you lose some: oncogenes in the Wnt signaling pathway Curr. Opin. Genet Dev 13, 28-33.
55. Verges, M., Luton, F., Gruber, C., Tiemann, E, Reinders, L. G., Huang, L., Burlingame, A. L., Haft, C. R. and Mostov, K. E. (2004). The mammalian retromer regulates transcytosis of the polymeric immunoglobulin receptor. Nat. Cell. BioL 6, 763-769.
56. Vincent, J. P. and Dubois, L. (2002). Morphogen transport along epithelia, an integrated trafficking problem. Dev Cell 3, 615-623.
57. Willert, K., Brown, J. D., Danenberg, E., Duncan, A. W., Weissman, I. L., Reya, T., Yates, J. R., 3rd and Nusse, R. (2003). Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423, 448-452.
58. Wodarz, A. and Nusse, R. (1998). Mechanisms of Wnt signaling in development. Annu. Rev Cell Dev Biol. 14, 59-88.
59. Zecca, M., Basler, K. and Struhl, G. (1996). Direct and long-range action of a wingless morphogen gradient. Cell 87, 833-844.
60. Zhai, L., Chaturvedi, D. and Cumberledge, S. (2004). Drosophila wnt-1 undergoes a hydrophobic modification and is targeted to lipid rafts, a process that requires porcupine. J. Biol. Chem. 279, 33220-33227.