Regulation of Endosomal Clathrin and Retromer-mediated Endosome to Golgi Retrograde Transport by the J-domain Protein RME-8

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 2009 Sep 19

PMID 19763082

Citations 94

Authors

Anbing Shi

Lin Sun

Riju Banerjee

Michael Tobin

Yinhua Zhang

Barth D Grant

Affiliations

Soon will be listed here.

Abstract

After endocytosis, most cargo enters the pleiomorphic early endosomes in which sorting occurs. As endosomes mature, transmembrane cargo can be sequestered into inwardly budding vesicles for degradation, or can exit the endosome in membrane tubules for recycling to the plasma membrane, the recycling endosome, or the Golgi apparatus. Endosome to Golgi transport requires the retromer complex. Without retromer, recycling cargo such as the MIG-14/Wntless protein aberrantly enters the degradative pathway and is depleted from the Golgi. Endosome-associated clathrin also affects the recycling of retrograde cargo and has been shown to function in the formation of endosomal subdomains. Here, we find that the Caemorhabditis elegans endosomal J-domain protein RME-8 associates with the retromer component SNX-1. Loss of SNX-1, RME-8, or the clathrin chaperone Hsc70/HSP-1 leads to over-accumulation of endosomal clathrin, reduced clathrin dynamics, and missorting of MIG-14 to the lysosome. Our results indicate a mechanism, whereby retromer can regulate endosomal clathrin dynamics through RME-8 and Hsc70, promoting the sorting of recycling cargo into the retrograde pathway.

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References

Sato M, Grant B, Harada A, Sato K . Rab11 is required for synchronous secretion of chondroitin proteoglycans after fertilization in Caenorhabditis elegans. J Cell Sci. 2008; 121(Pt 19):3177-86. DOI: 10.1242/jcs.034678. View

Hermann G, Schroeder L, Hieb C, Kershner A, Rabbitts B, Fonarev P . Genetic analysis of lysosomal trafficking in Caenorhabditis elegans. Mol Biol Cell. 2005; 16(7):3273-88. PMC: 1165410. DOI: 10.1091/mbc.e05-01-0060. View

Raiborg C, Bremnes B, Mehlum A, Gillooly D, DArrigo A, Stang E . FYVE and coiled-coil domains determine the specific localisation of Hrs to early endosomes. J Cell Sci. 2001; 114(Pt 12):2255-63. DOI: 10.1242/jcs.114.12.2255. View

Greener T, Grant B, Zhang Y, Wu X, Greene L, Hirsh D . Caenorhabditis elegans auxilin: a J-domain protein essential for clathrin-mediated endocytosis in vivo. Nat Cell Biol. 2001; 3(2):215-9. DOI: 10.1038/35055137. View

Port F, Kuster M, Herr P, Furger E, Banziger C, Hausmann G . Wingless secretion promotes and requires retromer-dependent cycling of Wntless. Nat Cell Biol. 2008; 10(2):178-85. DOI: 10.1038/ncb1687. View

Timmons L, Fire A . Specific interference by ingested dsRNA. Nature. 1998; 395(6705):854. DOI: 10.1038/27579. View

Pan C, Baum P, Gu M, Jorgensen E, Clark S, Garriga G . C. elegans AP-2 and retromer control Wnt signaling by regulating mig-14/Wntless. Dev Cell. 2007; 14(1):132-9. PMC: 2709403. DOI: 10.1016/j.devcel.2007.12.001. View

Bonifacino J, Hurley J . Retromer. Curr Opin Cell Biol. 2008; 20(4):427-36. PMC: 2833274. DOI: 10.1016/j.ceb.2008.03.009. View

Rojas R, Kametaka S, Haft C, Bonifacino J . 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. 2006; 27(3):1112-24. PMC: 1800681. DOI: 10.1128/MCB.00156-06. View

10.

Belenkaya T, Wu Y, Tang X, Zhou B, Cheng L, Sharma Y . The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev Cell. 2007; 14(1):120-31. DOI: 10.1016/j.devcel.2007.12.003. View

11.

Ungewickell E, Ungewickell H, Holstein S, Lindner R, Prasad K, Barouch W . Role of auxilin in uncoating clathrin-coated vesicles. Nature. 1995; 378(6557):632-5. DOI: 10.1038/378632a0. View

12.

Chang H, Newmyer S, Hull M, Ebersold M, Schmid S, Mellman I . Hsc70 is required for endocytosis and clathrin function in Drosophila. J Cell Biol. 2002; 159(3):477-87. PMC: 2173062. DOI: 10.1083/jcb.200205086. View

13.

Shi A, Pant S, Balklava Z, Chen C, Figueroa V, Grant B . A novel requirement for C. elegans Alix/ALX-1 in RME-1-mediated membrane transport. Curr Biol. 2007; 17(22):1913-24. PMC: 2175126. DOI: 10.1016/j.cub.2007.10.045. View

14.

Praitis V, Casey E, Collar D, Austin J . Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics. 2001; 157(3):1217-26. PMC: 1461581. DOI: 10.1093/genetics/157.3.1217. View

15.

Kamath R, Ahringer J . Genome-wide RNAi screening in Caenorhabditis elegans. Methods. 2003; 30(4):313-21. DOI: 10.1016/s1046-2023(03)00050-1. View

16.

Treusch S, Knuth S, Slaugenhaupt S, Goldin E, Grant B, Fares H . Caenorhabditis elegans functional orthologue of human protein h-mucolipin-1 is required for lysosome biogenesis. Proc Natl Acad Sci U S A. 2004; 101(13):4483-8. PMC: 384773. DOI: 10.1073/pnas.0400709101. View

17.

Lee D, Zhao X, Zhang F, Eisenberg E, Greene L . Depletion of GAK/auxilin 2 inhibits receptor-mediated endocytosis and recruitment of both clathrin and clathrin adaptors. J Cell Sci. 2005; 118(Pt 18):4311-21. DOI: 10.1242/jcs.02548. View

18.

Prasad B, Clark S . Wnt signaling establishes anteroposterior neuronal polarity and requires retromer in C. elegans. Development. 2006; 133(9):1757-66. DOI: 10.1242/dev.02357. View

19.

Fujibayashi A, Taguchi T, Misaki R, Ohtani M, Dohmae N, Takio K . Human RME-8 is involved in membrane trafficking through early endosomes. Cell Struct Funct. 2008; 33(1):35-50. DOI: 10.1247/csf.07045. View

20.

Lin S, Mallet W, Huang A, Maxfield F . Endocytosed cation-independent mannose 6-phosphate receptor traffics via the endocytic recycling compartment en route to the trans-Golgi network and a subpopulation of late endosomes. Mol Biol Cell. 2003; 15(2):721-33. PMC: 329388. DOI: 10.1091/mbc.e03-07-0497. View