SNX3 controls Wingless/Wnt secretion through regulating retromer-dependent recycling of Wntless

Cell Research

Volumn 21, Issue 12, 2011, Pages 1677-1690

  Zhang, Peng ^a   Wu, Yihui ^a   Belenkaya, Tatyana Y ^b   Lin, Xinhua ^a,b  

^a INSTITUTE OF ZOOLOGY   (China)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Drosophila SNX3 (DSNX3); retromer; signaling; Wingless (Wg); Wnt; Wntless (Wls)

Indexed keywords

DROSOPHILA PROTEIN; SIGNAL PEPTIDE; SORTING NEXIN; VESICULAR TRANSPORT PROTEIN; VPS35 PROTEIN, DROSOPHILA; WG PROTEIN, DROSOPHILA; WNT PROTEIN; WNT1 PROTEIN; WNTLESS PROTEIN, DROSOPHILA;

ANIMAL; ARTICLE; CELL LINE; DROSOPHILA; ENDOSOME; GENETICS; METABOLISM; MUTATION; SECRETION; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; DROSOPHILA; DROSOPHILA PROTEINS; ENDOSOMES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MUTATION; SIGNAL TRANSDUCTION; SORTING NEXINS; VESICULAR TRANSPORT PROTEINS; WNT PROTEINS; WNT1 PROTEIN;

EID: 82655178026     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2011.167     Document Type: Article

References (58)

1. MacDonald BT, Tamai K, He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 2009;17:9-26.
2. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006;127:469-480.
3. Klaus A, Birchmeier W. Wnt signalling and its impact on development and cancer. Nat Rev Cancer 2008;8:387-398. (Pubitemid 351589714)
4. Moon RT, Bowerman B, Boutros M, Perrimon N. The promise and perils of Wnt signaling through beta-catenin. Science 2002;296:1644-1646. (Pubitemid 34579151)
5. Wodarz A, Nusse R. Mechanisms of Wnt signaling in development. Annu Rev Cell Dev Biol 1998;14:59-88. (Pubitemid 29001449)
6. Tabata T, Takei Y. Morphogens, their identification and regulation. Development 2004;131:703-712. (Pubitemid 38263187)
7. Vincent J P, Dubois L. Morphogen transport along epithelia, an integrated trafficking problem. Dev Cell 2002;3:615-623. (Pubitemid 35339480)
8. Port F, Basler K. Wnt trafficking: new insights into Wnt maturation, secretion and spreading. Traffic 2010;11:1265-1271.
9. 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.
10. Bartscherer K, Pelte N, Ingelfinger D, Boutros M. Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell 2006;125:523-533.
11. Goodman RM, Thombre S, Firtina Z, et al. Sprinter: a novel transmembrane protein required for Wg secretion and signaling. Development 2006;133:4901-4911. (Pubitemid 46085056)
12. Belenkaya TY, Wu Y, Tang X, et al. The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev Cell 2008;14:120-131.
13. Franch-Marro X, Wendler F, Guidato S, et al. Wingless secretion requires endosome-to-Golgi retrieval of Wntless/Evi/Sprinter by the retromer complex. Nat Cell Biol 2008;10:170-177. (Pubitemid 351194046)
14. Port F, Kuster M, Herr P, et al. Wingless secretion promotes and requires retromer-dependent cycling of Wntless. Nat Cell Biol 2008;10:178-185. (Pubitemid 351194047)
15. Fu J, Ivy Yu HM, Maruyama T, Mirando AJ, Hsu W. Gpr177/mouse Wntless is essential for Wnt-mediated craniofacial and brain development. Dev Dyn 2011;240:365-371.
16. Fu J, Jiang M, Mirando AJ, Yu HM, Hsu W. Reciprocal regulation of Wnt and Gpr177/mouse Wntless is required for embryonic axis formation. Proc Natl Acad Sci USA 2009;106:18598-18603.
17. 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.
18. Yang PT, Lorenowicz MJ, Silhankova M, Coudreuse D Y, Betist MC, Korswagen HC. Wnt signaling requires retromerdependent recycling of MIG-14/Wntless in Wnt-producing cells. Dev Cell 2008;14:140-147.
19. 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. (Pubitemid 43727326)
20. Prasad BC, Clark SG. Wnt signaling establishes anteroposterior neuronal polarity and requires retromer in C. elegans. Development 2006;133:1757-1766. (Pubitemid 43810982)
21. Bonifacino JS, Hurley JH. Retromer. Curr Opin Cell Biol 2008;20:427-436.
22. Seaman MN. Recycle your receptors with retromer. Trends Cell Biol 2005;15:68-75. (Pubitemid 40188216)
23. McGough IJ, Cullen PJ. Recent advances in retromer biology. Traffic 2011;12:963-971.
24. Cullen PJ. Endosomal sorting and signalling: an emerging role for sorting nexins. Nat Rev Mol Cell Biol 2008;9:574-582. (Pubitemid 351881840)
25. Seet LF, Hong W. The Phox (PX) domain proteins and membrane traffic. Biochim Biophys Acta 2006;1761:878-896. (Pubitemid 44348964)
26. Teasdale RD, Loci D, Houghton F, Karlsson L, Gleeson PA. A large family of endosome-localized proteins related to sorting nexin 1. Biochem J 2001;358:7-16. (Pubitemid 32778092)
27. Rojas R, Kametaka S, Haft CR, Bonifacino JS. Interchangeable but essential functions of SNX1 and SNX2 in the association of retromer with endosomes and the trafficking of mannose 6-phosphate receptors. Mol Cell Biol 2007;27:1112-1124. (Pubitemid 46174571)
28. Griffin CT, Trejo J, Magnuson T. Genetic evidence for a mammalian retromer complex containing sorting nexins 1 and 2. Proc Natl Acad Sci USA 2005;102:15173-15177. (Pubitemid 41513354)
29. Wassmer T, Attar N, Bujny MV, Oakley J, Traer CJ, Cullen PJ. A loss-of-function screen reveals SNX5 and SNX6 as potential components of the mammalian retromer. J Cell Sci 2007;120:45-54. (Pubitemid 46206648)
30. Chen D, Xiao H, Zhang K, et al. Retromer is required for apoptotic cell clearance by phagocytic receptor recycling. Science 2010;327:1261-1264.
31. Seaman MN. Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval. J Cell Sci 2007;120:2378-2389. (Pubitemid 47225941)
32. Seaman MN. Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J Cell Biol 2004;165:111-122. (Pubitemid 38649181)
33. Arighi CN, Hartnell LM, Aguilar RC, Haft CR, Bonifacino JS. Role of the mammalian retromer in sorting of the cationindependent mannose 6-phosphate receptor. J Cell Biol 2004;165:123-133. (Pubitemid 38649182)
34. Hong Z, Yang Y, Zhang C, et al. The retromer component SNX6 interacts with dynactin p150 (Glued) and mediates endosome-to-TGN transport. Cell Res 2009;19:1334-1349.
35. Wassmer T, Attar N, Harterink M, et al. The retromer coat complex coordinates endosomal sorting and dynein-mediated transport, with carrier recognition by the trans-Golgi network. Dev Cell 2009;17:110-122.
36. Strochlic TI, Setty TG, Sitaram A, Burd CG. Grd19/Snx3p functions as a cargo-specific adapter for retromer-dependent endocytic recycling. J Cell Biol 2007;177:115-125. (Pubitemid 46588406)
37. Zhou CZ, Li de La Sierra-Gallay I, Quevillon-Cheruel S, et al. Crystal structure of the yeast Phox homology (PX) domain protein Grd19p complexed to phosphatidylinositol-3-phosphate. J Biol Chem 2003;278:50371-50376. (Pubitemid 37548880)
38. Voos W, Stevens TH. Retrieval of resident late-Golgi membrane proteins from the prevacuolar compartment of Saccharomyces cerevisiae is dependent on the function of Grd19p. J Cell Biol 1998;140:577-590. (Pubitemid 28134061)
39. Temkin P, Lauffer B, Jager S, Cimermancic P, Krogan NJ, von Zastrow M. SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat Cell Biol 2011;13:717-723.
40. Gong WJ, Golic KG. Ends-out, or replacement, gene targeting in Drosophila. Proc Natl Acad Sci USA 2003;100:2556-2561. (Pubitemid 36297537)
41. Belenkaya TY, Han C, Standley HJ, Lin X, Houston DW, Heasman J. pygopus Encodes a nuclear protein essential for wingless/Wnt signaling. Development 2002;129:4089-4101. (Pubitemid 35012494)
42. Couso JP, Bishop SA, Martinez Arias A. The wingless signalling pathway and the patterning of the wing margin in Drosophila. Development 1994;120:621-636. (Pubitemid 24071204)
43. Neumann CJ, Cohen SM. Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing. Development 1997;124:871-880. (Pubitemid 27107435)
44. Nolo R, Abbott LA, Bellen HJ. Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell 2000;102:349-362.
45. Zecca M, Basler K, Struhl G. Direct and long-range action of a wingless morphogen gradient. Cell 1996;87:833-844. (Pubitemid 26404283)
46. Xu T, Rubin GM. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 1993;117:1223-1237. (Pubitemid 23154489)
47. Strigini M, Cohen SM. Wingless gradient formation in the Drosophila wing. Curr Biol 2000;10:293-300. (Pubitemid 30186132)
48. Rulifson EJ, Blair SS. Notch regulates wingless expression and is not required for reception of the paracrine wingless signal during wing margin neurogenesis in Drosophila. Development 1995;121:2813-2824.
49. Gaullier JM, Simonsen A, D'Arrigo A, Bremnes B, Stenmark H, Aasland R. FYVE fingers bind PtdIns (3) P. Nature 1998;394:432-433.
50. Christoforidis S, McBride HM, Burgoyne RD, Zerial M. The Rab5 effector EEA1 is a core component of endosome docking. Nature 1999;397:621-625. (Pubitemid 29091948)
51. Xu Y, Seet LF, Hanson B, Hong W. The Phox homology (PX) domain, a new player in phosphoinositide signalling. Biochem J 2001;360:513-530. (Pubitemid 34020256)
52. Xu Y, Hortsman H, Seet L, Wong SH, Hong W. SNX3 regulates endosomal function through its PX-domain-mediated interaction with PtdIns (3) P. Nat Cell Biol 2001;3:658-666. (Pubitemid 32624422)
53. Seaman MN, McCaffery JM, Emr SD. A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J Cell Biol 1998;142:665-681. (Pubitemid 28381486)
54. Korolchuk VI, Schutz MM, Gomez-Llorente C, et al. Drosophila Vps35 function is necessary for normal endocytic trafficking and actin cytoskeleton organisation. J Cell Sci 2007;120:4367-4376.
55. Gallop JL, McMahon HT. BAR domains and membrane curvature: bringing your curves to the BAR. Biochem Soc Symp 2005;72:223-231. (Pubitemid 44804748)
56. Harterink M, Port F, Lorenowicz MJ, et al. A SNX3-dependent retromer pathway mediates retrograde transport of the Wnt sorting receptor Wntless and is required for Wnt secretion. Nat Cell Biol 2011;13:914-923.
57. Bellen HJ, Levis RW, Liao G, et al. The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 2004;167:761-781. (Pubitemid 38931863)
58. Taylor AM, Nakano Y, Mohler J, Ingham PW. Contrasting distributions of patched and hedgehog proteins in the Drosophila embryo. Mech Dev 1993;42:89-96. (Pubitemid 23235182)