The BAG homology domain of Snl1 cures yeast prion [URE3] through regulation of Hsp70 chaperones

G3: Genes, Genomes, Genetics

Volumn 4, Issue 3, 2014, Pages 461-470

  Kumar, Navinder ^a   Gaur, Deepika ^a   Masison, Daniel C ^b   Sharma, Deepak ^a  

^a INSTITUTE OF MICROBIAL TECHNOLOGY   (India)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

BAG domain; Exchange factor; Hsp70; Nucleotide; snl1; Yeast prion

Indexed keywords

ALANINE; BAG PROTEIN; FUNGAL PROTEIN; HEAT SHOCK PROTEIN 70; LYSINE; PRION PROTEIN; SNL1 PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; NONHUMAN; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; YEAST;

BAG DOMAIN; HSP70; NUCLEOTIDE EXCHANGE FACTOR; SNL1; YEAST PRION;

ENDOPLASMIC RETICULUM; GENOTYPE; GLUTATHIONE PEROXIDASE; HSP70 HEAT-SHOCK PROTEINS; MEMBRANE PROTEINS; MOLECULAR CHAPERONES; MUTAGENESIS; NUCLEAR ENVELOPE; PRIONS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84896951249     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.113.009993     Document Type: Article

References (43)

1. Alberti, S., Esser C., and J. Hohfeld, 2003 BAG-1-a nucleotide exchange factor of Hsc70 with multiple cellular functions. Cell Stress Chaperones 8: 225-231.
2. Baxa, U., Wickner R.B., Steven A.C., Anderson D.E., Marekov L.N. et al., 2007 Characterization of beta-sheet structure in Ure2p1-89 yeast prion fibrils by solid-state nuclear magnetic resonance. Biochemistry 46: 13149- 13162.
3. Brachmann, A., Baxa U., and R. B. Wickner, 2005 Prion generation in vitro: amyloid of Ure2p is infectious. EMBO J. 24: 3082-3092.
4. Chernoff Y.O., Lindquist S.L., Ono B., Inge S.G.-Vechtomov, and S. W. Liebman, 1995 Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi+]. Science 268: 880-884.
5. Cyr D.M., Lu X., and M. G. Douglas, 1992 Regulation of Hsp70 function by a eukaryotic DnaJ homolog. J. Biol. Chem. 267: 20927-20931.
6. Du, Z., Park K.W., Yu H., Q. Fan, and L. Li, 2008 Newly identified prion linked to the chromatin-remodeling factor Swi1 in Saccharomyces cerevisiae. Nat. Genet. 40: 460-465.
7. Fan, Q., Park K.W., Du Z., Morano K.A., and L. Li, 2007 The role of Sse1 in the de novo formation and variant determination of the [PSI+] prion. Genetics 177: 1583-1593.
8. Gassler C.S., Wiederkehr T., Brehmer D., Bukau B., and M. P. Mayer, 2001 Bag-1M accelerates nucleotide release for human Hsc70 and Hsp70 and can act concentration-dependent as positive and negative cofactor. J. Biol. Chem. 276: 32538-32544.
9. Ho A.K., Raczniak G.A., Ives E.B., and S. R. Wente, 1998 The integral membrane protein snl1p is genetically linked to yeast nuclear pore complex function. Mol. Biol. Cell 9: 355-373.
10. Hohfeld, J., and S. Jentsch, 1997 GrpE-like regulation of the hsc70 chaperone by the anti-apoptotic protein BAG-1. EMBO J. 16: 6209-6216.
11. Hung G.C., and D. C. Masison, 2006 N-terminal domain of yeast Hsp104 chaperone is dispensable for thermotolerance and prion propagation but necessary for curing prions by Hsp104 overexpression. Genetics 173: 611-620.
12. Jung, G., Jones G., Wegrzyn R.D., and D. C. Masison, 2000 A role for cytosolic hsp70 in yeast [PSI(+)] prion propagation and [PSI(+)] as a cellular stress. Genetics 156: 559-570.
13. Kabbage, M., and M. B. Dickman, 2008 The BAG proteins: a ubiquitous family of chaperone regulators. Cell. Mol. Life Sci. 65: 1390-1402.
14. Knapp R.T., Steiner A., Schmidt U., Hafner K., F. Holsboer et al., 2012 BAG-1 diversely affects steroid receptor activity. Biochem. J. 441: 297-303.
15. Kryndushkin, D., and R. B. Wickner, 2007 Nucleotide exchange factors for Hsp70s are required for [URE3] prion propagation in Saccharomyces cerevisiae. Mol. Biol. Cell 18: 2149-2154.
16. Liberek, K., Marszalek J., Ang D., Georgopoulos C., and M. Zylicz, 1991 Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc. Natl. Acad. Sci. USA 88: 2874-2878.
17. Liu, R., Takayama S., Zheng Y., Froesch B., Chen G.Q. et al., 1998 Interaction of BAG-1 with retinoic acid receptor and its inhibition of retinoic acid-induced apoptosis in cancer cells. J. Biol. Chem. 273: 16985-16992.
18. Moriyama, H., Edskes H.K., and R. B. Wickner, 2000 [URE3] prion propagation in Saccharomyces cerevisiae: requirement for chaperone Hsp104 and curing by overexpressed chaperone Ydj1p. Mol. Cell. Biol. 20: 8916-8922.
19. Mumberg, D., Muller R., and M. Funk, 1995 Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156: 119-122.
20. Newnam G.P., Birchmore J.L., and Y. O. Chernoff, 2011 Destabilization and recovery of a yeast prion after mild heat shock. J. Mol. Biol. 408: 432-448.
21. Ngo, S., Gu L., and Z. Guo, 2011 Hierarchical organization in the amyloid core of yeast prion protein Ure2. J. Biol. Chem. 286: 29691-29699.
22. Patel B.K., and S. W. Liebman, 2007 "Prion-proof" for [PIN+]: infection with in vitro-made amyloid aggregates of Rnq1p-(132-405) induces [PIN+]. J. Mol. Biol. 365: 773-782.
23. Reidy, M., and D. C. Masison, 2011 Modulation and elimination of yeast prions by protein chaperones and co-chaperones. Prion 5: 245-249.
24. Rose M.D., and G. R. Fink, 1987 KAR1, a gene required for function of both intranuclear and extranuclear microtubules in yeast. Cell 48: 1047- 1060.
25. Sadlish, H., Rampelt H., Shorter J., Wegrzyn R.D., C. Andreasson et al., 2008 Hsp110 chaperones regulate prion formation and propagation in S. cerevisiae by two discrete activities. PLoS One 3: e1763.
26. Schwimmer, C., and D. C. Masison, 2002 Antagonistic interactions between yeast [PSI(+)] and [URE3] prions and curing of [URE3] by Hsp70 protein chaperone Ssa1p but not by Ssa2p. Mol. Cell. Biol. 22: 3590-3598.
27. Sharma, D., and D. C. Masison, 2008 Functionally redundant isoforms of a yeast Hsp70 chaperone subfamily have different antiprion effects. Genetics 179: 1301-1311.
28. Sharma, D., and D. C. Masison, 2011 Single methyl group determines prion propagation and protein degradation activities of yeast heat shock protein (Hsp)-70 chaperones Ssa1p and Ssa2p. Proc. Natl. Acad. Sci. USA 108: 13665-13670.
29. Sharma, D., Martineau C.N., Le M.T. Dall, Reidy M., Masison D.C. et al., 2009a Function of SSA subfamily of Hsp70 within and across species varies widely in complementing Saccharomyces cerevisiae cell growth and prion propagation. PLoS One 4: e6644.
30. Sharma, D., Stanley R.F., and D. C. Masison, 2009b Curing of yeast [URE3] prion by the Hsp40 cochaperone Ydj1p is mediated by Hsp70. Genetics 181: 129-137.
31. Shewmaker, F., Wickner R.B., and R. Tycko, 2006 Amyloid of the prion domain of Sup35p has an in-register parallel beta-sheet structure. Proc. Natl. Acad. Sci. USA 103: 19754-19759.
32. Shi, Y., and J. O. Thomas, 1992 The transport of proteins into the nucleus requires the 70-kilodalton heat shock protein or its cytosolic cognate. Mol. Cell. Biol. 12: 2186-2192.
33. Sondermann, H., Scheufler C., Schneider C., Hohfeld J., Hartl F.U. et al., 2001 Structure of a Bag/Hsc70 complex: convergent functional evolution of Hsp70 nucleotide exchange factors. Science 291: 1553-1557.
34. Sondermann, H., Ho A.K., Listenberger L.L., Siegers K., I. Moarefi et al., 2002 Prediction of novel Bag-1 homologs based on structure/function analysis identifies Snl1p as an Hsp70 co-chaperone in Saccharomyces cerevisiae. J. Biol. Chem. 277: 33220-33227.
35. Sondheimer, N., and S. Lindquist, 2000 Rnq1: an epigenetic modifier of protein function in yeast. Mol. Cell 5: 163-172.
36. Song, J., Takeda M., and R. I. Morimoto, 2001 Bag1-Hsp70 mediates a physiological stress signalling pathway that regulates Raf-1/ERK and cell growth. Nat. Cell Biol. 3: 276-282.
37. Su P.H., and H. M. Li, 2010 Stromal Hsp70 is important for protein translocation into pea and Arabidopsis chloroplasts. Plant Cell 22: 1516- 1531.
38. Suzuki, G., Shimazu N., and M. Tanaka, 2012 A yeast prion, Mod5, promotes acquired drug resistance and cell survival under environmental stress. Science 336: 355-359.
39. Suzuki, G., and M. Tanaka, 2013 Expanding the yeast prion world: Active prion conversion of non-glutamine/asparagine-rich Mod5 for cell survival. Prion 7: 109-113.
40. Tanaka, M., Chien P., Naber N., Cooke R., and J. S. Weissman, 2004 Conformational variations in an infectious protein determine prion strain differences. Nature 428: 323-328.
41. Verghese, J., and K. A. Morano, 2012 A lysine-rich region within fungal BAG domain-containing proteins mediates a novel association with ribosomes. Eukaryot. Cell 11: 1003-1011.
42. Wickner R.B., 1994 [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264: 566-569.
43. Xu, Z., Page R.C., Gomes M.M., Kohli E., Nix J.C. et al., 2008 Structural basis of nucleotide exchange and client binding by the Hsp70 cochaperone Bag2. Nat. Struct. Mol. Biol. 15: 1309-1317.