The Type II Hsp40 Sis1 Cooperates with Hsp70 and the E3 Ligase Ubr1 to Promote Degradation of Terminally Misfolded Cytosolic Protein

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Summers, Daniel W ^a,b   Wolfe, Katie J ^a   Ren, Hong Yu ^a   Cyr, Douglas M ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; UBIQUITIN PROTEIN LIGASE E3;

ARTICLE; NONHUMAN; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; QUALITY CONTROL; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; CYCLOHEXIMIDE; CYTOSOL; GREEN FLUORESCENT PROTEINS; HSP40 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; MOLECULAR SEQUENCE DATA; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; PROTEIN STABILITY; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 84872482670     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052099     Document Type: Article

References (48)

1. Hartl FU, Hayer-Hartl M, (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295: 1852-1858.
2. Mayer MP, Bukau B, (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62: 670-684.
3. Cyr DM, Hohfeld J, Patterson C, (2002) Protein quality control: U-box-containing E3 ubiquitin ligases join the fold. Trends Biochem Sci 27: 368-375.
4. Meacham GC, Patterson C, Zhang W, Younger JM, Cyr DM, (2001) The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat Cell Biol 3: 100-105.
5. Bukau B, Weissman J, Horwich A, (2006) Molecular chaperones and protein quality control. Cell 125: 443-451.
6. Douglas PM, Summers DW, Cyr DM, (2009) Molecular chaperones antagonize proteotoxicity by differentially modulating protein aggregation pathways. Prion 3.
7. Douglas PM, Treusch S, Ren HY, Halfmann R, Duennwald ML, et al. (2008) Chaperone-dependent amyloid assembly protects cells from prion toxicity. Proc Natl Acad Sci U S A.
8. Kaganovich D, Kopito R, Frydman J, (2008) Misfolded proteins partition between two distinct quality control compartments. Nature 454: 1088-1095.
9. Specht S, Miller SB, Mogk A, Bukau B, (2011) Hsp42 is required for sequestration of protein aggregates into deposition sites in Saccharomyces cerevisiae. J Cell Biol 195: 617-629.
10. Douglas PM, Summers DW, Ren HY, Cyr DM, (2009) Reciprocal efficiency of RNQ1 and polyglutamine detoxification in the cytosol and nucleus. Mol Biol Cell 20: 4162-4173.
11. Cyr DM, Langer T, Douglas MG, (1994) DnaJ-like proteins: molecular chaperones and specific regulators of Hsp70. Trends Biochem Sci 19: 176-181.
12. Langer T, Lu C, Echols H, Flanagan J, Hayer MK, et al. (1992) Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding. Nature 356: 683-689.
13. Kampinga HH, Craig EA, (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11: 579-592.
14. Walsh P, Bursac D, Law YC, Cyr D, Lithgow T, (2004) The J-protein family: modulating protein assembly, disassembly and translocation. EMBO Rep 5: 567-571.
15. Qiu XB, Shao YM, Miao S, Wang L, (2006) The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell Mol Life Sci 63: 2560-2570.
16. Meacham GC, Lu Z, King S, Sorscher E, Tousson A, et al. (1999) The Hdj-2/Hsc70 chaperone pair facilitates early steps in CFTR biogenesis. Embo J 18: 1492-1505.
17. Metzger MB, Maurer MJ, Dancy BM, Michaelis S, (2008) Degradation of a cytosolic protein requires endoplasmic reticulum-associated degradation machinery. J Biol Chem 283: 32302-32316.
18. McClellan AJ, Scott MD, Frydman J, (2005) Folding and quality control of the VHL tumor suppressor proceed through distinct chaperone pathways. Cell 121: 739-748.
19. Youker RT, Walsh P, Beilharz T, Lithgow T, Brodsky JL, (2004) Distinct roles for the Hsp40 and Hsp90 molecular chaperones during cystic fibrosis transmembrane conductance regulator degradation in yeast. Mol Biol Cell 15: 4787-4797.
20. Grove DE, Fan CY, Ren HY, Cyr DM, (2010) The endoplasmic reticulum-associated Hsp40 DNAJB12 and Hsc70 cooperate to facilitate RMA1 E3-dependent degradation of nascent CFTRDeltaF508. Mol Biol Cell 22: 301-314.
21. Yan W, Schilke B, Pfund C, Walter W, Kim S, et al. (1998) Zuotin, a ribosome-associated DnaJ molecular chaperone. Embo J 17: 4809-4817.
22. Caplan AJ, Cyr DM, Douglas MG, (1992) YDJ1p facilitates polypeptide translocation across different intracellular membranes by a conserved mechanism. Cell 71: 1143-1155.
23. Douglas PM, Treusch S, Ren HY, Halfmann R, Duennwald ML, et al. (2008) Chaperone-dependent amyloid assembly protects cells from prion toxicity. Proc Natl Acad Sci U S A 105: 7206-7211.
24. Caplan AJ, Tsai J, Casey PJ, Douglas MG, (1992) Farnesylation of YDJ1p is required for function at elevated growth temperatures in Saccharomyces cerevisiae. J Biol Chem 267: 18890-18895.
25. Lu Z, Cyr DM, (1998) The conserved carboxyl terminus and zinc finger-like domain of the co-chaperone Ydj1 assist Hsp70 in protein folding. J Biol Chem 273: 5970-5978.
26. Lu Z, Cyr DM, (1998) Protein folding activity of Hsp70 is modified differentially by the hsp40 co-chaperones Sis1 and Ydj1. J Biol Chem 273: 27824-27830.
27. Fan CY, Lee S, Ren HY, Cyr DM, (2004) Exchangeable chaperone modules contribute to specification of type I and type II Hsp40 cellular function. Mol Biol Cell 15: 761-773.
28. Ramos CH, Oliveira CL, Fan CY, Torriani IL, Cyr DM, (2008) Conserved central domains control the quaternary structure of type I and type II Hsp40 molecular chaperones. J Mol Biol 383: 155-166.
29. Summers DW, Douglas PM, Ren HY, Cyr DM, (2009) The type I Hsp40 Ydj1 utilizes a farnesyl moiety and zinc finger-like region to suppress prion toxicity. J Biol Chem 284: 3628-3639.
30. Kushnirov VV, (2000) Rapid and reliable protein extraction from yeast. Yeast 16: 857-860.
31. Rudiger S, Schneider-Mergener J, Bukau B, (2001) Its substrate specificity characterizes the DnaJ co-chaperone as a scanning factor for the DnaK chaperone. Embo J 20: 1042-1050.
32. Kota P, Summers DW, Ren HY, Cyr DM, Dokholyan NV, (2009) Identification of a consensus motif in substrates bound by a Type I Hsp40. Proc Natl Acad Sci U S A 106: 11073-11078.
33. Stade K, Ford CS, Guthrie C, Weis K, (1997) Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 90: 1041-1050.
34. Eisele F, Wolf DH, (2008) Degradation of misfolded protein in the cytoplasm is mediated by the ubiquitin ligase Ubr1. FEBS Lett 582: 4143-4146.
35. Nillegoda NB, Theodoraki MA, Mandal AK, Mayo KJ, Ren HY, et al. (2010) Ubr1 and Ubr2 function in a quality control pathway for degradation of unfolded cytosolic proteins. Mol Biol Cell 21: 2102-2116.
36. Prasad R, Kawaguchi S, Ng DT, (2010) A nucleus-based quality control mechanism for cytosolic proteins. Mol Biol Cell 21: 2117-2127.
37. Lewis MJ, Pelham HR, (2009) Inefficient quality control of thermosensitive proteins on the plasma membrane. PLoS One 4: e5038.
38. Heck JW, Cheung SK, Hampton RY, (2010) Cytoplasmic protein quality control degradation mediated by parallel actions of the E3 ubiquitin ligases Ubr1 and San1. Proc Natl Acad Sci U S A 107: 1106-1111.
39. Feldman DE, Thulasiraman V, Ferreyra RG, Frydman J, (1999) Formation of the VHL-elongin BC tumor suppressor complex is mediated by the chaperonin TRiC. Mol Cell 4: 1051-1061.
40. Melville MW, McClellan AJ, Meyer AS, Darveau A, Frydman J, (2003) The Hsp70 and TRiC/CCT chaperone systems cooperate in vivo to assemble the von Hippel-Lindau tumor suppressor complex. Mol Cell Biol 23: 3141-3151.
41. Schoenfeld AR, Davidowitz EJ, Burk RD, (2000) Elongin BC complex prevents degradation of von Hippel-Lindau tumor suppressor gene products. Proc Natl Acad Sci U S A 97: 8507-8512.
42. Rosenbaum JC, Fredrickson EK, Oeser ML, Garrett-Engele CM, Locke MN, et al. (2011) Disorder targets misorder in nuclear quality control degradation: a disordered ubiquitin ligase directly recognizes its misfolded substrates. Mol Cell 41: 93-106.
43. Tipton KA, Verges KJ, Weissman JS, (2008) In vivo monitoring of the prion replication cycle reveals a critical role for Sis1 in delivering substrates to Hsp104. Mol Cell 32: 584-591.
44. Winkler J, Tyedmers J, Bukau B, Mogk A, (2012) Hsp70 targets Hsp100 chaperones to substrates for protein disaggregation and prion fragmentation. J Cell Biol 198: 387-404.
45. Sondheimer N, Lopez N, Craig EA, Lindquist S, (2001) The role of Sis1 in the maintenance of the [RNQ+] prion. Embo J 20: 2435-2442.
46. Higurashi T, Hines JK, Sahi C, Aron R, Craig EA, (2008) Specificity of the J-protein Sis1 in the propagation of 3 yeast prions. Proc Natl Acad Sci U S A 105: 16596-16601.
47. Shorter J, Lindquist S, (2008) Hsp104, Hsp70 and Hsp40 interplay regulates formation, growth and elimination of Sup35 prions. Embo J 27: 2712-2724.
48. Weisberg SJ, Lyakhovetsky R, Werdiger AC, Gitler AD, Soen Y, et al. (2012) Compartmentalization of superoxide dismutase 1 (SOD1G93A) aggregates determines their toxicity. Proc Natl Acad Sci U S A 109: 15811-15816.