Specialized membrane-localized chaperones prevent aggregation of polytopic proteins in the ER

Journal of Cell Biology

Volumn 168, Issue 1, 2005, Pages 79-88

  Kota, Jhansi ^a   Ljungdahl, Per O ^a  

^a LUDWIG INSTITUTE FOR CANCER RESEARCH   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CHAPERONE; CHITIN SYNTHASE; GLUCOSE TRANSPORTER; PHOSPHATE TRANSPORTER; PROTEIN AMINO ACID PERMEASE; PROTEIN CHS7P; PROTEIN GSF2P; PROTEIN PHO86P; PROTEIN SHR3P; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; INTRACELLULAR TRANSPORT; LIPID BILAYER; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

AMINO ACID TRANSPORT SYSTEMS; AMINO ACIDS; CARRIER PROTEINS; ENDOPLASMIC RETICULUM; INTRACELLULAR MEMBRANES; MEMBRANE PROTEINS; MOLECULAR CHAPERONES; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 12144251018     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200408106     Document Type: Article

References (47)

1. Abramson, J., I. Smirnova, V. Kasho, G. Verner, H.R. Kaback, and S. Iwata. 2003. Structure and mechanism of the lactose permease of Escherichia coli. Science. 301:610-615.
2. Alder, N.N., and A.E. Johnson. 2004. Cotranslational membrane protein biogenesis at the endoplasmic reticulum. J. Biol. Chem. 279:22787-22790.
3. Andréasson, C., and P.O. Ljungdahl. 2002. Receptor-mediated endoproteolytic activation of two transcription factors in yeast. Genes Dev. 16:3158-3172.
4. Antonny, B., and R. Schekman. 2001. ER export: public transportation by the COPII coach. Curr. Opin. Cell Biol. 13:438-443.
5. Barlowe, C. 2003. Molecular recognition of cargo by the COPII complex: a most accommodating coat. Cell. 114:395-399.
6. Bermak, J.C., M. Li, C. Bullock, and Q.Y. Zhou. 2001. Regulation of transport of the dopamine D1 receptor by a new membrane-associated ER protein. Nat. Cell Biol. 3:492-498.
7. Bickford, L.C., E. Mossessova, and J. Goldberg. 2004. A structural view of the COPII vesicle coat. Curr. Opin. Struct. Biol. 14:147-153.
8. Burke, D., D. Dawson, and T. Stearns. 2000. Methods in Yeast Genetics: A Cold Spring Harbor Laboratory Course Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 171-182.
9. Dalbey, R.E., and A. Kuhn. 2004. YidC family members are involved in the membrane insertion, lateral integration, folding, and assembly of membrane proteins. J. Cell Biol. 166:769-774.
10. Dwyer, N.D., E.R. Troemel, P. Sengupta, and C.I. Bargmann. 1998. Odorant receptor localization to olfactory cilia is mediated by ODR-4, a novel membrane-associated protein. Cell. 93:455-466.
11. Egner, R., Y. Mahé, R. Pandjaitan, and K. Kuchler. 1995. Endocytosis and vacuolar degradation of the plasma membrane-localized Pdr5 ATP-binding cassette multidrug transporter in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:5879-5887.
12. Forsberg, H., and P.O. Ljungdahl. 2001. Sensors of extracellular nutrients in Saccharomyces cerevisiae. Curr. Genet. 40:91-109.
13. Gilstring, C.F., M. Melin-Larsson, and P.O. Ljungdahl. 1999. Shr3p mediates specific COPII coatomer-cargo interactions required for the packaging of amino acid permeases into ER-derived transport vesicles. Mol. Biol. Cell. 10:3549-3565.
14. Gilstring, C.F., and P.O. Ljungdahl. 2000. A method for determining the in vivo topology of yeast polytopic membrane proteins demonstrates that Gap1p fully integrates into the membrane independently of Shr3p. J. Biol. Chem. 275:31488-31495.
15. Heinrich, S.U., and T.A. Rapoport. 2003. Cooperation of transmembrane segments during the integration of a double-spanning protein into the ER membrane. EMBO J. 22:3654-3663.
16. Heinrich, S.U., W. Mothes, J. Brunner, and T.A. Rapoport. 2000. The Sec61 complex mediates the integration of a membrane protein by allowing lipid partitioning of the transmembrane domain. Cell. 102:233-244.
17. Herrmann, J.M., P. Malkus, and R. Schekman. 1999. Out of the ER-outfitters, escorts and guides. Trends Cell Biol. 9:5-7.
18. Huang, Y., M.J. Lemieux, J. Song, M. Auer, and D.N. Wang. 2003. Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science. 301:616-620.
19. Iraqui, I., S. Vissers, F. Bernard, J.O. de Craene, E. Boles, A. Urrestarazu, and B. André. 1999. Amino acid signaling in Saccharomyces cerevisiae: a permease-like sensor of external amino acids and F-Box protein Grr1p are required for transcriptional induction of the AGP1 gene, which encodes a broad-specificity amino acid permease. Mol. Cell. Biol. 19:989-1001.
20. Kaneko, Y., A. Toh-e, and Y. Oshima. 1982. Identification of the genetic locus for the structural gene and a new regulatory gene for the synthesis of repressible alkaline phosphatase in Saccharomyces cerevisiae. Mol. Cell. Biol. 2:127-137.
21. Kuehn, M.J., R. Schekman, and P.O. Ljungdahl. 1996. Amino acid permeases require COPII components and the ER resident membrane protein Shr3p for packaging into transport vesicles in vitro. J. Cell Biol. 135:585-595.
22. Kuehn, M.J., J.M. Herrmann, and R. Schekman. 1998. COPII-cargo interactions direct protein sorting into ER-derived transport vesicles. Nature. 391:187-190.
23. Kuhn, A., R. Stuart, R. Henry, and R.E. Dalbey. 2003. The Alb3/Oxa1/YidC protein family: membrane-localized chaperones facilitating membrane protein insertion? Trends Cell Biol. 13:510-516.
24. Lagerstedt, J.O., R. Zvyagilskaya, J.R. Pratt, J. Pattison-Granberg, A.L. Kruckeberg, J.A. Berden, and B.L. Persson. 2002. Mutagenic and functional analysis of the C-terminus of Saccharomyces cerevisiae Pho84 phosphate transporter. FEBS Lett. 526:31-37.
25. Lau, W.T., R.W. Howson, P. Malkus, R. Schekman, and E.K. O'Shea. 2000. Pho86p, an endoplasmic reticulum (ER) resident protein in Saccharomyces cerevisiae, is required for ER exit of the high-affinity phosphate transporter Pho84p. Proc. Natl. Acad. Sci. USA. 97:1107-1112.
26. Lecomte, F.J., N. Ismail, and S. High. 2003. Making membrane proteins at the mammalian endoplasmic reticulum. Biochem. Soc. Trans. 31:1248-1252.
27. Lee, M.C., E.A. Miller, J. Goldberg, L. Orci, and R. Schekman. 2004. Bi-directional protein transport between the ER and Golgi. Annu. Rev. Cell Dev. Biol. 20:87-123.
28. Levine, T.P., C.A. Wiggins, and S. Munro. 2000. Inositol phosphorylceramide synthase is located in the Golgi apparatus of Saccharomyces cerevisiae. Mol. Biol. Cell. 11:2267-2281.
29. Ljungdahl, P.O., C.J. Gimeno, C.A. Styles, and G.R. Fink. 1992. SHR3: A novel component of the secretory pathway specifically required for the localization of amino acid permeases in yeast. Cell. 71:463-478.
30. Malkus, P., F. Jiang, and R. Schekman. 2002. Concentrative sorting of secretory cargo proteins into COPII-coated vesicles. J. Cell Biol. 159:915-921.
31. Martínez, P., and P.O. Ljungdahl. 2000. The SHR3 homologue from S. pombe demonstrates a conserved function of ER packaging chaperones. J. Cell Sci. 113:4351-4362.
32. Martínez, P., and P.O. Ljungdahl. 2004. An ER packaging chaperone determines the amino acid uptake capacity and virulence of Candida albicans. Mol. Microbiol. 51:371-384.
33. McClintock, T.S., and N. Sammeta. 2003. Trafficking prerogatives of olfactory receptors. Neuroreport. 14:1547-1552.
34. McLatchie, L.M., N.J. Fraser, M.J. Main, A. Wise, J. Brown, N. Thompson, R. Solari, M.G. Lee, and S.M. Foord. 1998. RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature. 393:333-339.
35. Miller, E.A., T.H. Beilharz, P.N. Malkus, M.C. Lee, S. Hamamoto, L. Orci, and R. Schekman. 2003. Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell. 114:497-509.
36. Nagamori, S., I.N. Smirnova, and H.R. Kaback. 2004. Role of YidC in folding of polytopic membrane proteins. J. Cell Biol. 165:53-62.
37. Nakano, A., D. Brada, and R. Schekman. 1988. A membrane glycoprotein, Sec12p, required for protein transport from the endoplasmic reticulum to the Golgi apparatus in yeast. J. Cell Biol. 107:851-863.
38. Nyman, T., J. Kota, and P.O. Ljungdahl. 2004. Ancillary proteins in membrane targeting of transporters. In Topics in Current Genetics - Molecular Mechanisms Controlling Transmembrane Transport. E. Boles and R. Krämer, editors. Springer-Verlag, Heidelberg. 207-234.
39. Rapoport, T.A., V. Goder, S.U. Heinrich, and K.E.S. Matlack. 2004. Membrane-protein integration and the role of the translocation channel. Trends Cell Biol. 14:568-575.
40. Rutkowski, D.T., and R.J. Kaufman. 2004. A trip to the ER: coping with stress. Trends Cell Biol. 14:20-28.
41. Saier, M.H., Jr. 2000. Families of transmembrane transporters selective for amino acids and their derivatives. Microbiol. 146:1775-1795.
42. Schägger, H., W.A. Cramer, and G. von Jagow. 1994. Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal. Biochem. 217:220-230.
43. Schamel, W.W.A., S. Kuppig, B. Becker, K. Gimborn, H.P. Hauri, and M. Reth. 2003. A high-molecular-weight complex of membrane proteins BAP29/BAP31 is involved in the retention of membrane-bound IgD in the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA. 100:9861-9866.
44. Sherwood, P.W., and M. Carlson. 1999. Efficient export of the glucose transporter Hxt1p from the endoplasmic reticulum requires Gsf2p. Proc. Natl. Acad. Sci. USA. 96:7415-7420.
45. Trilla, J.A., A. Duran, and C. Roncero. 1999. Chs7p, a new protein involved in the control of protein export from the endoplasmic reticulum that is specifically engaged in the regulation of chitin synthesis in Saccharomyces cerevisiae. J. Cell Biol. 145:1153-1163.
46. Turner, R.J. 2003. Understanding the biogenesis of polytopic integral membrane proteins. J. Membr. Biol. 192:149-157.
47. van den Berg, B., W.M. Clemons Jr., I. Collinson, Y. Modis, E. Hartmann, S.C. Harrison, and T. A. Rapoport. 2004. X-ray structure of a protein-conducting channel. Nature. 427:36-44.