The Saccharomyces cerevisiae YFR041C/ERJ5 gene encoding a type I membrane protein with a J domain is required to preserve the folding capacity of the endoplasmic reticulum

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1773, Issue 2, 2007, Pages 232-242

  Carla Fama M ^a   Raden, David ^b   Zacchi, Nicolás ^a   Lemos, Darío R ^a   Robinson, Anne S ^b   Silberstein, Susana ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b University of Delaware   (United States)

Author keywords

Chaperone; DnaJ; Endoplasmic reticulum; Protein folding; Saccharomyces cerevisiae; Unfolded protein response

Indexed keywords

HEAT SHOCK PROTEIN 70; MEMBRANE PROTEIN; MESSENGER RNA; PROTEIN DNAJ; PROTEIN ERJ5P; PROTEIN KAR2P; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ERJ5 GENE; FUNGAL GENE; FUNGAL GENETICS; GENE CONTROL; GENE IDENTIFICATION; GENE INTERACTION; GENE MUTATION; GENETIC REGULATION; IRE1 GENE; JEM1 GENE; KAR2 GENE; KNOCKOUT GENE; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN LOCALIZATION; REGULATORY MECHANISM; RNA GENE; SACCHAROMYCES CEREVISIAE; SCJ1 GENE;

ALLELES; AMINO ACID SEQUENCE; BLOTTING, NORTHERN; ENDOPLASMIC RETICULUM; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; HSP40 HEAT-SHOCK PROTEINS; MEMBRANE PROTEINS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT;

SACCHAROMYCES CEREVISIAE;

EID: 33846268455     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2006.10.011     Document Type: Article

References (51)

1. Bukau B., and Horwich A.L. The Hsp70 and Hsp60 chaperone machines. Cell 92 (1998) 351-366
2. Corsi A.K., and Schekman R. The lumenal domain of Sec63p stimulates the ATPase activity of BiP and mediates BiP recruitment to the translocon in Saccharomyces cerevisiae. J. Cell Biol. 137 (1997) 1483-1493
3. Rudiger S., Schneider-Mergener J., and Bukau B. Its substrate specificity characterizes the DnaJ co-chaperone as a scanning factor for the DnaK chaperone. EMBO J. 20 (2001) 1042-1050
4. Ng D.T., Spear E.D., and Walter P. The unfolded protein response regulates multiple aspects of secretory and membrane protein biogenesis and endoplasmic reticulum quality control. J. Cell Biol. 150 (2000) 77-88
5. Rutkowski D.T., and Kaufman R.J. A trip to the ER: coping with stress. Trends Cell Biol. 14 (2004) 20-28
6. Casagrande R., Stern P., Diehn M., Shamu C., Osario M., Zuniga M., Brown P.O., and Ploegh H. Degradation of proteins from the ER of S. cerevisiae requires an intact unfolded protein response pathway. Mol. Cell 5 (2000) 729-735
7. Rose M.D., Misra L.M., and Vogel J.P. KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell 57 (1989) 1211-1221
8. Vogel J.P., Misra L.M., and Rose M.D. Loss of BiP/GRP78 function blocks translocation of secretory proteins in yeast. J. Cell Biol. 110 (1990) 1885-1895
9. te Heesen S., and Aebi M. The genetic interaction of kar2 and wbp1 mutations. Distinct functions of binding protein BiP and N-linked glycosylation in the processing pathway of secreted proteins in Saccharomyces cerevisiae. Eur. J. Biochem. 222 (1994) 631-637
10. Simons J.F., Ferro-Novick S., Rose M.D., and Helenius A. BiP/Kar2p serves as a molecular chaperone during carboxypeptidase Y folding in yeast. J. Cell Biol. 130 (1995) 41-49
11. Silberstein S., Schlenstedt G., Silver P.A., and Gilmore R. A role for the DnaJ homologue Scj1p in protein folding in the yeast endoplasmic reticulum. J. Cell Biol. 143 (1998) 921-933
12. Nishikawa S.I., Fewell S.W., Kato Y., Brodsky J.L., and Endo T. Molecular chaperones in the yeast endoplasmic reticulum maintain the solubility of proteins for retrotranslocation and degradation. J. Cell Biol. 153 (2001) 1061-1070
13. Latterich M., and Schekman R. The karyogamy gene KAR2 and novel proteins are required for ER-membrane fusion. Cell 78 (1994) 87-98
14. Holkeri H., Paunola E., Jamsa E., and Makarow M. Dissection of the translocation and chaperoning functions of yeast BiP/Kar2p in vivo. J. Cell Sci. 111 Pt. 6 (1998) 749-757
15. Nishikawa S., and Endo T. The yeast JEM1p is a DnaJ-like protein of the endoplasmic reticulum membrane required for nuclear fusion. J. Biol. Chem. 272 (1997) 12889-12892
16. Brizzio V., Khalfan W., Huddler D., Beh C.T., Andersen S.S., Latterich M., and Rose M.D. Genetic interactions between KAR7/SEC71, KAR8/JEM1, KAR5, and KAR2 during nuclear fusion in Saccharomyces cerevisiae. Mol. Biol. Cell. 10 (1999) 609-626
17. Craven R.A., Egerton M., and Stirling C.J. A novel Hsp70 of the yeast ER lumen is required for the efficient translocation of a number of protein precursors. EMBO J. 15 (1996) 2640-2650
18. Hamilton T.G., Norris T.B., Tsuruda P.R., and Flynn G.C. Cer1p functions as a molecular chaperone in the endoplasmic reticulum of Saccharomyces cerevisiae. Mol. Cell. Biol. 19 (1999) 5298-5307
19. Baxter B.K., James P., Evans T., and Craig E.A. SSI1 encodes a novel Hsp70 of the Saccharomyces cerevisiae endoplasmic reticulum. Mol. Cell. Biol. 16 (1996) 6444-6456
20. Steel G.J., Fullerton D.M., Tyson J.R., and Stirling C.J. Coordinated activation of Hsp70 chaperones. Science 303 (2004) 98-101
21. 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
22. Walsh P., Bursac D., Law Y.C., Cyr D., and Lithgow T. The J-protein family: modulating protein assembly, disassembly and translocation. EMBO Rep. 5 (2004) 567-571
23. Rothblatt J.A., Deshaies R.J., Sanders S.L., Daum G., and Schekman R. Multiple genes are required for proper insertion of secretory proteins into the endoplasmic reticulum in yeast. J. Cell Biol. 109 (1989) 2641-2652
24. Schlenstedt G., Harris S., Risse B., Lill R., and Silver P.A. A yeast DnaJ homologue, Scj1p, can function in the endoplasmic reticulum with BiP/Kar2p via a conserved domain that specifies interactions with Hsp70s. J. Cell Biol. 129 (1995) 979-988
25. 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
26. Kuo C.L., and Campbell J.L. Cloning of Saccharomyces cerevisiae DNA replication genes: isolation of the CDC8 gene and two genes that compensate for the cdc8-1 mutation. Mol. Cell. Biol. 3 (1983) 1730-1737
27. Wach A., Brachat A., Pohlmann R., and Philippsen P. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10 (1994) 1793-1808
28. Knop M., Siegers K., Pereira G., Zachariae W., Winsor B., Nasmyth K., and Schiebel E. Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 15 (1999) 963-972
29. Hann B.C., and Walter P. The signal recognition particle in S. cerevisiae. Cell 67 (1991) 131-144
30. Silberstein S., Collins P.G., Kelleher D.J., and Gilmore R. The essential OST2 gene encodes the 16-kD subunit of the yeast oligosaccharyltransferase, a highly conserved protein expressed in diverse eukaryotic organisms. J. Cell Biol. 131 (1995) 371-383
31. Sikorski R.S., and Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122 (1989) 19-27
32. Pringle J.R., Adams A.E., Drubin D.G., and Haarer B.K. Immunofluorescence methods for yeast. Methods Enzymol. 194 (1991) 565-602
33. Kohrer K., and Domdey H. Preparation of high molecular weight RNA. Methods Enzymol. 194 (1991) 398-405
34. Sambrook J., Fritsch E.F., and Maniatis T. Molecular cloning: a laboratory manual. 2nd ed. (1989), Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
35. Xu P., Raden D., Doyle III F.J., and Robinson A.S. Analysis of unfolded protein response during single-chain antibody expression in Saccaromyces cerevisiae reveals different roles for BiP and PDI in folding. Metab. Eng. 7 (2005) 269-279
36. 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
37. Szyperski T., Pellecchia M., Wall D., Georgopoulos C., and Wuthrich K. NMR structure determination of the Escherichia coli DnaJ molecular chaperone: secondary structure and backbone fold of the N-terminal region (residues 2-108) containing the highly conserved J domain. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 11343-11347
38. Genevaux P., Schwager F., Georgopoulos C., and Kelley W.L. Scanning mutagenesis identifies amino acid residues essential for the in vivo activity of the Escherichia coli DnaJ (Hsp40) J-domain. Genetics 162 (2002) 1045-1053
39. Hamilton T.G., and Flynn G.C. Cer1p, a novel Hsp70-related protein required for posttranslational endoplasmic reticulum translocation in yeast. J. Biol. Chem. 271 (1996) 30610-30613
40. Kimata Y., Kimata Y.I., Shimizu Y., Abe H., Farcasanu I.C., Takeuchi M., Rose M.D., and Kohno K. Genetic evidence for a role of BiP/Kar2 that regulates Ire1 in response to accumulation of unfolded proteins. Mol. Biol. Cell 14 (2003) 2559-2569
41. Cox J.S., Shamu C.E., and Walter P. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73 (1993) 1197-1206
42. Normington K., Kohno K., Kozutsumi Y., Gething M.J., and Sambrook J. S. cerevisiae encodes an essential protein homologous in sequence and function to mammalian BiP. Cell 57 (1989) 1223-1236
43. Mori K., Sant A., Kohno K., Normington K., Gething M.J., and Sambrook J.F. A 22 bp cis-acting element is necessary and sufficient for the induction of the yeast KAR2 (BiP) gene by unfolded proteins. EMBO J. 11 (1992) 2583-2593
44. Cheetham M.E., and Caplan A.J. Structure, function and evolution of DnaJ: conservation and adaptation of chaperone function. Cell Stress Chaperones 3 (1998) 28-36
45. Deshaies R.J., Sanders S.L., Feldheim D.A., and Schekman R. Assembly of yeast Sec proteins involved in translocation into the endoplasmic reticulum into a membrane-bound multisubunit complex. Nature 349 (1991) 806-808
46. Silberstein S., and Gilmore R. Biochemistry, molecular biology, and genetics of the oligosaccharyltransferase. FASEB J. 10 (1996) 849-858
47. Caldwell S.R., Hill K.J., and Cooper A.A. Degradation of endoplasmic reticulum (ER) quality control substrates requires transport between the ER and Golgi. J. Biol. Chem. 276 (2001) 23296-23303
48. Taxis C., Hitt R., Park S.H., Deak P.M., Kostova Z., and Wolf D.H. Use of modular substrates demonstrates mechanistic diversity and reveals differences in chaperone requirement of ERAD. J. Biol. Chem. 278 (2003) 35903-35913
49. Palmer E.A., Kruse K.B., Fewell S.W., Buchanan S.M., Brodsky J.L., and McCracken A.A. Differential requirements of novel A1PiZ degradation deficient (ADD) genes in ER-associated protein degradation. J. Cell Sci. 116 (2003) 2361-2373
50. Ellgaard L., Molinari M., and Helenius A. Setting the standards: quality control in the secretory pathway. Science 286 (1999) 1882-1888
51. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882