The GET Complex Mediates Insertion of Tail-Anchored Proteins into the ER Membrane

Cell

Volumn 134, Issue 4, 2008, Pages 634-645

  Schuldiner, Maya ^a   Metz, Jutta ^b   Schmid, Volker ^b   Denic, Vladimir ^a   Rakwalska, Magdalena ^b   Schmitt, Hans Dieter ^c   Schwappach, Blanche ^b   Weissman, Jonathan S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

CELLBIO; PROTEINS

Indexed keywords

ASPARAGINE; GET3 PROTEIN; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CELL AGGREGATION; CYTOSOL; ENDOPLASMIC RETICULUM; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRION; MOLECULAR RECOGNITION; PRIORITY JOURNAL; YEAST;

EID: 49549086224     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2008.06.025     Document Type: Article

References (55)

1. Abell B.M., Pool M.R., Schlenker O., Sinning I., and High S. Signal recognition particle mediates post-translational targeting in eukaryotes. EMBO J. 23 (2004) 2755-2764
2. Abell B.M., Rabu C., Leznicki P., Young J.C., and High S. Post-translational integration of tail-anchored proteins is facilitated by defined molecular chaperones. J. Cell Sci. 120 (2007) 1743-1751
3. Auld K.L., Hitchcock A.L., Doherty H.K., Frietze S., Huang L.S., and Silver P.A. The conserved ATPase Get3/Arr4 modulates the activity of membrane-associated proteins in Saccharomyces cerevisiae. Genetics 174 (2006) 215-227
4. Banfield D.K., Lewis M.J., Rabouille C., Warren G., and Pelham H.R. Localization of Sed5, a putative vesicle targeting molecule, to the cis-Golgi network involves both its transmembrane and cytoplasmic domains. J. Cell Biol. 127 (1994) 357-371
5. Beilharz T., Egan B., Silver P.A., Hofmann K., and Lithgow T. Bipartite signals mediate subcellular targeting of tail-anchored membrane proteins in Saccharomyces cerevisiae. J. Biol. Chem. 278 (2003) 8219-8223
6. Borgese N., Gazzoni I., Barberi M., Colombo S., and Pedrazzini E. Targeting of a tail-anchored protein to endoplasmic reticulum and mitochondrial outer membrane by independent but competing pathways. Mol. Biol. Cell 12 (2001) 2482-2496
7. Borgese N., Brambillasca S., and Colombo S. How tails guide tail-anchored proteins to their destinations. Curr. Opin. Cell Biol. 19 (2007) 368-375
8. Brambillasca S., Yabal M., Makarow M., and Borgese N. Unassisted translocation of large polypeptide domains across phospholipid bilayers. J. Cell Biol. 175 (2006) 767-777
9. Brodsky J.L. An in vitro assay for the selective endoplasmic reticulum associated degradation of an unglycosylated secreted protein. Methods 35 (2005) 354-359
10. Bulbarelli A., Sprocati T., Barberi M., Pedrazzini E., and Borgese N. Trafficking of tail-anchored proteins: transport from the endoplasmic reticulum to the plasma membrane and sorting between surface domains in polarised epithelial cells. J. Cell Sci. 115 (2002) 1689-1702
11. Campbell R.E., Tour O., Palmer A.E., Steinbach P.A., Baird G.S., Zacharias D.A., and Tsien R.Y. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 99 (2002) 7877-7882
12. Denic V., and Weissman J.S. A molecular caliper mechanism for determining very long-chain fatty acid length. Cell 130 (2007) 663-677
13. Dimmer K.S., Fritz S., Fuchs F., Messerschmitt M., Weinbach N., Neupert W., and Westermann B. Genetic basis of mitochondrial function and morphology in Saccharomyces cerevisiae. Mol. Biol. Cell 13 (2002) 847-853
14. Egan B., Beilharz T., George R., Isenmann S., Gratzer S., Wattenberg B., and Lithgow T. Targeting of tail-anchored proteins to yeast mitochondria in vivo. FEBS Lett. 451 (1999) 243-248
15. Egea P.F., Stroud R.M., and Walter P. Targeting proteins to membranes: structure of the signal recognition particle. Curr. Opin. Struct. Biol. 15 (2005) 213-220
16. Elgersma Y., Kwast L., van den Berg M., Snyder W.B., Distel B., Subramani S., and Tabak H.F. Overexpression of Pex15p, a phosphorylated peroxisomal integral membrane protein required for peroxisome assembly in S. cerevisiae, causes proliferation of the endoplasmic reticulum membrane. EMBO J. 16 (1997) 7326-7341
17. Enyenihi A.H., and Saunders W.S. Large-scale functional genomic analysis of sporulation and meiosis in Saccharomyces cerevisiae. Genetics 163 (2003) 47-54
18. Favaloro V., Spasic M., Schwappach B., and Dobberstein B. Distinct targeting pathways for the membrane insertion of tail-anchored (TA) proteins. J. Cell Sci. 121 (2008) 1832-1840
19. Garcia P.D., Hansen W., and Walter P. In vitro protein translocation across microsomal membranes of Saccharomyces cerevisiae. Methods Enzymol. 194 (1991) 675-682
20. Giaever G., Chu A.M., Ni L., Connelly C., Riles L., Veronneau S., Dow S., Lucau-Danila A., Anderson K., Andre B., et al. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418 (2002) 387-391
21. Hardwick K.G., and Pelham H.R. SED5 encodes a 39-kD integral membrane protein required for vesicular transport between the ER and the Golgi complex. J. Cell Biol. 119 (1992) 513-521
22. High S., and Abell B.M. Tail-anchored protein biosynthesis at the endoplasmic reticulum: the same but different. Biochem. Soc. Trans. 32 (2004) 659-662
23. Ho Y., Gruhler A., Heilbut A., Bader G.D., Moore L., Adams S.L., Millar A., Taylor P., Bennett K., Boutilier K., et al. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415 (2002) 180-183
24. Hoepfner D., Schildknegt D., Braakman I., Philippsen P., and Tabak H.F. Contribution of the endoplasmic reticulum to peroxisome formation. Cell 122 (2005) 85-95
25. Huh W.K., Falvo J.V., Gerke L.C., Carroll A.S., Howson R.W., Weissman J.S., and O'Shea E.K. Global analysis of protein localization in budding yeast. Nature 425 (2003) 686-691
26. James P., Halladay J., and Craig E.A. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144 (1996) 1425-1436
27. Kao G., Nordenson C., Still M., Ronnlund A., Tuck S., and Naredi P. ASNA-1 positively regulates insulin secretion in C. elegans and mammalian cells. Cell 128 (2007) 577-587
28. Kitada K., Yamaguchi E., and Arisawa M. Cloning of the Candida glabrata TRP1 and HIS3 genes, and construction of their disruptant strains by sequential integrative transformation. Gene 165 (1995) 203-206
29. Krajewski S., Tanaka S., Takayama S., Schibler M.J., Fenton W., and Reed J.C. Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res. 53 (1993) 4701-4714
30. Labbe S., and Thiele D.J. Pipes and wiring: the regulation of copper uptake and distribution in yeast. Trends Microbiol. 7 (1999) 500-505
31. Lithgow T., van Driel R., Bertram J.F., and Strasser A. The protein product of the oncogene bcl-2 is a component of the nuclear envelope, the endoplasmic reticulum, and the outer mitochondrial membrane. Cell Growth Differ. 5 (1994) 411-417
32. Longtine M.S., McKenzie III A., Demarini D.J., Shah N.G., Wach A., Brachat A., Philippsen P., and Pringle J.R. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14 (1998) 953-961
33. Metz J., Wachter A., Schmidt B., Bujnicki J.M., and Schwappach B. The yeast Arr4p ATPase binds the chloride transporter Gef1p when copper is available in the cytosol. J. Biol. Chem. 281 (2006) 410-417
34. Mnaimneh S., Davierwala A.P., Haynes J., Moffat J., Peng W.T., Zhang W., Yang X., Pootoolal J., Chua G., Lopez A., et al. Exploration of essential gene functions via titratable promoter alleles. Cell 118 (2004) 31-44
35. Mukhopadhyay R., Ho Y.S., Swiatek P.J., Rosen B.P., and Bhattacharjee H. Targeted disruption of the mouse Asna1 gene results in embryonic lethality. FEBS Lett. 580 (2006) 3889-3894
36. Neupert W. Protein import into mitochondria. Annu. Rev. Biochem. 66 (1997) 863-917
37. Ogg S.C., Poritz M.A., and Walter P. Signal recognition particle receptor is important for cell growth and protein secretion in Saccharomyces cerevisiae. Mol. Biol. Cell 3 (1992) 895-911
38. Pfanner N., and Meijer M. The Tom and Tim machine. Curr. Biol. 7 (1997) R100-R103
39. Rabu C., and High S. Membrane protein chaperones: a new twist in the tail?. Curr. Biol. 17 (2007) R472-R474
40. Rachubinski R.A., Verma D.P., and Bergeron J.J. Synthesis of rat liver microsomal cytochrome b5 by free ribosomes. J. Cell Biol. 84 (1980) 705-716
41. Rapoport T.A., Matlack K.E., Plath K., Misselwitz B., and Staeck O. Posttranslational protein translocation across the membrane of the endoplasmic reticulum. Biol. Chem. 380 (1999) 1143-1150
42. Roth A.F., Wan J., Bailey A.O., Sun B., Kuchar J.A., Green W.N., Phinney B.S., Yates III J.R., and Davis N.G. Global analysis of protein palmitoylation in yeast. Cell 125 (2006) 1003-1013
43. Sambade M., Alba M., Smardon A.M., West R.W., and Kane P.M. A genomic screen for yeast vacuolar membrane ATPase mutants. Genetics 170 (2005) 1539-1551
44. Schuldiner M., Collins S.R., Thompson N.J., Denic V., Bhamidipati A., Punna T., Ihmels J., Andrews B., Boone C., Greenblatt J.F., et al. Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 123 (2005) 507-519
45. Shen J., Hsu C.M., Kang B.K., Rosen B.P., and Bhattacharjee H. The Saccharomyces cerevisiae Arr4p is involved in metal and heat tolerance. Biometals 16 (2003) 369-378
46. Stefanovic S., and Hegde R.S. Identification of a targeting factor for posttranslational membrane protein insertion into the ER. Cell 128 (2007) 1147-1159
47. Tam Y.Y., Fagarasanu A., Fagarasanu M., and Rachubinski R.A. Pex3p initiates the formation of a preperoxisomal compartment from a subdomain of the endoplasmic reticulum in Saccharomyces cerevisiae. J. Biol. Chem. 280 (2005) 34933-34939
48. Travers K.J., Patil C.K., Wodicka L., Lockhart D.J., Weissman J.S., and Walter P. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101 (2000) 249-258
49. Wattenberg B., and Lithgow T. Targeting of C-terminal (tail)-anchored proteins: understanding how cytoplasmic activities are anchored to intracellular membranes. Traffic 2 (2001) 66-71
50. Weinberger A., Kamena F., Kama R., Spang A., and Gerst J.E. Control of Golgi morphology and function by Sed5 t-SNARE phosphorylation. Mol. Biol. Cell 16 (2005) 4918-4930
51. Wickner W., and Schekman R. Protein translocation across biological membranes. Science 310 (2005) 1452-1456
52. Wuestehube L.J., and Schekman R.W. Reconstitution of transport from endoplasmic reticulum to Golgi complex using endoplasmic reticulum-enriched membrane fraction from yeast. Methods Enzymol. 219 (1992) 124-136
53. Yabal M., Brambillasca S., Soffientini P., Pedrazzini E., Borgese N., and Makarow M. Translocation of the C terminus of a tail-anchored protein across the endoplasmic reticulum membrane in yeast mutants defective in signal peptide-driven translocation. J. Biol. Chem. 278 (2003) 3489-3496
54. Yamaguchi T., Dulubova I., Min S.W., Chen X., Rizo J., and Sudhof T.C. Sly1 binds to Golgi and ER syntaxins via a conserved N-terminal peptide motif. Dev. Cell 2 (2002) 295-305
55. Zewail A., Xie M.W., Xing Y., Lin L., Zhang P.F., Zou W., Saxe J.P., and Huang J. Novel functions of the phosphatidylinositol metabolic pathway discovered by a chemical genomics screen with wortmannin. Proc. Natl. Acad. Sci. USA 100 (2003) 3345-3350