Secretion of hedgehog-related peptides and WNT during Caenorhabditis elegans development

Traffic

Volumn 10, Issue 7, 2009, Pages 803-810

  Kolotuev, Irina ^a   Apaydin, Ahmet ^a   Labouesse, Michel ^a  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Caenorhabditis elegans; Cuticle; Dispatched; Epithelial; Exosome; Hedgehog; Polarized secretion; Retromer; V ATPase; WNT

Indexed keywords

ADENOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; PROTEIN DISPATCHED; PROTEIN EGL 20; PROTEIN MIG 14; PROTEIN PATCHED; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; V0 COMPLEX; VACUOLAR ADENOSINE TRIPHOSPHATASE; WNT PROTEIN;

CAENORHABDITIS ELEGANS; CELL COMMUNICATION; CELL INTERACTION; CELL MEMBRANE TRANSPORT; CELL VACUOLE; DEVELOPMENT; ENDOCYTOSIS; EPITHELIUM CELL; EXOSOME; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; ENDOCYTOSIS; EXOSOMES; HEDGEHOG PROTEINS; LIGANDS; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 67249115310     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2009.00871.x     Document Type: Review

References (54)

1. Bartscherer K, Boutros M. Regulation of Wnt protein secretion and its role in gradient formation. EMBO Rep 2008;9:977-982.
2. Eaton S. Multiple roles for lipids in the Hedgehog signalling pathway. Nat Rev Mol Cell Biol 2008;9:437-445.
3. Rohatgi R, Scott MP. Patching the gaps in Hedgehog signalling. Nat Cell Biol 2007;9:1005-1009.
4. Burglin TR, Kuwabara PE. Homologs of the Hh signalling network in C. elegans. WormBook 2006;1-14.
5. Gallet A, Rodriguez R, Ruel L, Therond PP. Cholesterol modification of hedgehog is required for trafficking and movement, revealing an asymmetric cellular response to hedgehog. Dev Cell 2003;4:191-204.
6. Burke R, Nellen D, Bellotto M, Hafen E, Senti KA, Dickson BJ, Basler K. Dispatched, a novel sterol-sensing domain protein dedicated to the release of cholesterol-modified hedgehog from signaling cells. Cell 1999;99:803-815.
7. Beckett K, Franch-Marro X, Vincent JP. Glypican-mediated endocytosis of Hedgehog has opposite effects in flies and mice. Trends Cell Biol 2008;18:360-363.
8. Kuwabara PE, Labouesse M. The sterol-sensing domain: Multiple families, a unique role? Trends Genet 2002;18:193-201.
9. Davies JP, Chen FW, Ioannou YA. Transmembrane molecular pump activity of Niemann-Pick C1 protein. Science 2000;290:2295-2298.
10. Aspock G, Kagoshima H, Niklaus G, Burglin TR. Caenorhabditis elegans has scores of hedgehog-related genes: Sequence and expression analysis. Genome Res 1999;9:909-923.
11. Burglin TR. Evolution of hedgehog and hedgehog-related genes, their origin from Hog proteins in ancestral eukaryotes and discovery of a novel Hint motif. BMC Genomics 2008;9:127.
12. Burglin TR. The Hedgehog protein family. Genome Biol 2008; 9:241.
13. Hao L, Aspock G, Burglin TR. The hedgehog-related gene wrt-5 is essential for hypodermal development in Caenorhabditis elegans. Dev Biol 2006;290:323-336.
14. Hao L, Johnsen R, Lauter G, Baillie D, Burglin TR. Comprehensive analysis of gene expression patterns of hedgehog-related genes. BMC Genomics 2006;7:280.
15. Hao L, Mukherjee K, Liegeois S, Baillie D, Labouesse M, Burglin TR. The hedgehog -related gene qua-1 is required for molting in Caenorhabditis elegans. Dev Dyn 2006;235:1469-1481.
16. Zugasti O, Rajan J, Kuwabara PE. The function and expansion of the Patched- and Hedgehog-related homologs in C. elegans. Genome Res 2005;15:1402-1410.
17. Porter JA, Ekker SC, Park WJ, von Kessler DP, Young KE, Chen CH, Ma Y, Woods AS, Cotter RJ, Koonin EV, Beachy PA. Hedgehog patterning activity: role of a lipophilic modification mediated by the carboxy-terminal autoprocessing domain. Cell 1996;86:21-34.
18. Kuwabara PE, Lee MH, Schedl T, Jefferis GS. A C. elegans patched gene, ptc-1, functions in germ-line cytokinesis. Genes Dev 2000;14:1933-1944.
19. Michaux G, Gansmuller A, Hindelang C, Labouesse M. CHE-14, a protein with a sterol-sensing domain, is required for apical sorting in C. elegans ectodermal epithelial cells. Curr Biol 2000;10:1098-1107.
20. Perkins LA, Hedgecock EM, Thomson JN, Culotti JG. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol 1986;117:456-487.
21. Perens EA, Shaham S. C. elegans daf-6 encodes a patched-related protein required for lumen formation. Dev Cell 2005;8:893-906.
22. Incardona JP, Lee JH, Robertson CP, Enga K, Kapur RP, Roelink H. Receptor-mediated endocytosis of soluble and membrane-tethered Sonic hedgehog by Patched-1. Proc Natl Acad Sci U S A 2000;97:12044-12049.
23. Balklava Z, Pant S, Fares H, Grant BD. Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat Cell Biol 2007;9:1066-1073.
24. Yochem J, Tuck S, Greenwald I, Han M. A gp330/megalin-related protein is required in the major epidermis of Caenorhabditis elegans for completion of molting. Development 1999;126:597-606.
25. Liegeois S, Benedetto A, Garnier JM, Schwab Y, Labouesse M. The V0-ATPase mediates apical secretion of exosomes containing Hedgehog-related proteins in Caenorhabditis elegans. J Cell Biol 2006;173:949-961.
26. Lakkaraju A, Rodriguez-Boulan E. Itinerant exosomes: Emerging roles in cell and tissue polarity. Trends Cell Biol 2008;18:199-209.
27. Liegeois S, Benedetto A, Michaux G, Belliard G, Labouesse M. Genes required for osmoregulation and apical secretion in Caenorhabditis elegans. Genetics 2007;175:709-724.
28. Hiesinger PR, Fayyazuddin A, Mehta SQ, Rosenmund T, Schulze KL, Zhai RG, Verstreken P, Cao Y, Zhou Y, Kunz J, Bellen HJ. The v-ATPase V0 subunit a1 is required for a late step in synaptic vesicle exocytosis in Drosophila. Cell 2005;121:607-620.
29. Peri F, Nusslein-Volhard C. Live imaging of neuronal degradation by microglia reveals a role for v0-ATPase a1 in phagosomal fusion in vivo. Cell 2008;133: 916-927.
30. Peters C, Bayer MJ, Buhler S, Andersen JS, Mann M, Mayer A. Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion. Nature 2001;409:581-588.
31. Sun-Wada GH, Toyomura T, Murata Y, Yamamoto A, Futai M, Wada Y. The a3 isoform of V-ATPase regulates insulin secretion from pancreatic beta-cells. J Cell Sci 2006;119:4531-4540.
32. Lee J, Willer JR, Willer GB, Smith K, Gregg RG, Gross JM. Zebrafish blowout provides genetic evidence for Patched1-mediated negative regulation of Hedgehog signaling within the proximal optic vesicle of the vertebrate eye. Dev Biol 2008;319:10-22.
33. Couillault C, Pujol N, Reboul J, Sabatier L, Guichou J-F, Kohara Y, Ewbank JJ. TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat Immunol 2004;5:488-494.
34. Coudreuse D, Korswagen HC. The making of Wnt: New insights into Wnt maturation, sorting and secretion. Development 2007;134:3-12.
35. Hausmann G, Banziger C, Basler K. Helping Wingless take flight: How WNT proteins are secreted. Nat Rev Mol Cell Biol 2007;8:331-336.
36. Takada R, Satomi Y, Kurata T, Ueno N, Norioka S, Kondoh H, Takao T, Takada S. Monounsaturated fatty acid modification of Wnt protein: Its role in Wnt secretion. Dev Cell 2006;11:791-801.
37. Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, Reya T, Yates JR III, Nusse R. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 2003;423:448-452.
38. Tanaka K, Kitagawa Y, Kadowaki T. Drosophila segment polarity gene product porcupine stimulates the posttranslational N-glycosylation of wingless in the endoplasmic reticulum. J Biol Chem 2002;277:12816-12823.
39. Rocheleau CE, Downs WD, Lin R, Wittmann C, Bei Y, Cha YH, Ali M, Priess JR, Mello CC. Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos. Cell 1997;90:707-716.
40. Banziger C, Soldini D, Schutt C, Zipperlen P, Hausmann G, Basler K. Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell 2006;125:509-522.
41. Bartscherer K, Pelte N, Ingelfinger D, Boutros M. Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell 2006;125:523-533.
42. Goodman RM, Thombre S, Firtina Z, Gray D, Betts D, Roebuck J, Spana EP, Selva EM. Sprinter: A novel transmembrane protein required for Wg secretion and signaling. Development 2006;133:4901-4911.
43. Belenkaya TY, Wu Y, Tang X, Zhou B, Cheng L, Sharma YV, Yan D, Selva EM, Lin X. The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev Cell 2008;14:120-131.
44. Franch-Marro X, Wendler F, Guidato S, Griffith J, Baena-Lopez A, Itasaki N, Maurice MM, Vincent JP. Wingless secretion requires endosome-to-Golgi retrieval of Wntless/Evi/Sprinter by the retromer complex. Nat Cell Biol 2008;10:170-177.
45. Pan CL, Baum PD, Gu M, Jorgensen EM, Clark SG, Garriga G. C. elegans AP-2 and retromer control Wnt signaling by regulating mig-14/Wntless. Dev Cell 2008;14:132-139.
46. Yang PT, Lorenowicz MJ, Silhankova M, Coudreuse DY, Betist MC, Korswagen HC. Wnt signaling requires retromer-dependent recycling of MIG-14/ Wntless in Wnt-producing cells. Dev Cell 2008;14:140-147.
47. Seaman MN. Recycle your receptors with retromer. Trends Cell Biol 2005;15:68-75.
48. Coudreuse DY, Roel G, Betist MC, Destree O, Korswagen HC. Wnt gradient formation requires retromer function in Wnt-producing cells. Science 2006;312:921-924.
49. Prasad BC, Clark SG. Wnt signaling establishes anteroposterior neuronal polarity and requires retromer in C. elegans. Development 2006;133:1757-1766.
50. Port F, Kuster M, Herr P, Furger E, Banziger C, Hausmann G, Basler K. Wingless secretion promotes and requires retromer-dependent cycling of Wntless. Nat Cell Biol 2008;10:178-185.
51. Paladino S, Sarnataro D, Tivodar S, Zurzolo C. Oligomerization is a specific requirement for apical sorting of glycosyl-phosphatidylinositol-anchored proteins but not for non-raft-associated apical proteins. Traffic 2007;8:251-258.
52. Delacour D, Cramm-Behrens CI, Drobecq H, Le Bivic A, Naim HY, Jacob R. Requirement for galectin-3 in apical protein sorting. Curr Biol 2006;16:408-414.
53. Delacour D, Gouyer V, Zanetta JP, Drobecq H, Leteurtre E, Grard G, Moreau-Hannedouche O, Maes E, Pons A, Andre S, Le Bivic A, Gabius HJ, Manninen A, Simons K, Huet G. Galectin-4 and sulfatides in apical membrane trafficking in enterocyte-like cells. J Cell Biol 2005;169:491-501.
54. Mellman I, Nelson WJ. Coordinated protein sorting, targeting and distribution in polarized cells. Nat Rev Mol Cell Biol 2008;9:833-845.