Sequential duplications of an ancient member of the DnaJ-family expanded the functional chaperone network in the eukaryotic cytosol

Molecular Biology and Evolution

Volumn 30, Issue 5, 2013, Pages 985-998

  Sahi, Chandan ^a,c   Kominek, Jacek ^b   Ziegelhoffer, Thomas ^a   Yu, Hyun Young ^a   Baranowski, MacIej ^b   Marszalek, Jaroslaw ^a,b   Craig, Elizabeth A ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF GDA SK   (Poland)

^c INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH BHOPAL   (India)

Author keywords

divergent evolution; gene duplication; Hsp40; Hsp70; J protein; yeast

Indexed keywords

APJ1 PROTEIN; PROTEIN DNAJ; UNCLASSIFIED DRUG; XDJ1 PROTEIN;

ARTICLE; ASCOMYCETES; CYTOSOL; EUKARYOTIC CELL; GENE DUPLICATION; GENE SEQUENCE; MOLECULAR MODEL; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE;

CYTOSOL; EVOLUTION, MOLECULAR; GENE DUPLICATION; HEAT-SHOCK PROTEINS; HSP40 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

ASCOMYCOTA; EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84876573356     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mst008     Document Type: Article

References (63)

1. Abascal F, Zardoya R, Posada D. 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105. (Pubitemid 40668057)
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215: 403-410.
3. Becker J, Walter W, Yan W, Craig EA. 1996. Functional interaction of cytosolic hsp70 and a DnaJ-related protein, Ydj1p, in protein translocation in vivo. Mol Cell Biol. 16: 4378-4386. (Pubitemid 26251239)
4. Bhangoo MK, Tzankov S, Fan AC, Dejgaard K, Thomas DY, Young JC. 2007. Multiple 40-kDa heat-shock protein chaperones function in Tom70-dependent mitochondrial import. Mol Biol Cell. 18: 3414-3428. (Pubitemid 47378681)
5. Bukau B, Weissman J, Horwich A. 2006. Molecular chaperones and protein quality control. Cell 125: 443-451.
6. Burri L, Vascotto K, Gentle IE, Chan NC, Beilharz T, Stapleton DI, Ramage L, Lithgow T. 2006. Integral membrane proteins in the mitochondrial outer membrane of Saccharomyces cerevisiae. FEBS J. 273: 1507-1515. (Pubitemid 44029113)
7. Caplan AJ, Douglas MG. 1991. Characterization of YDJ1: a yeast homologue of the bacterial dnaJ protein. J Cell Biol. 114: 609-621. (Pubitemid 21909828)
8. 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.
9. Cheetham ME, Caplan AJ. 1998. Structure, function and evolution of DnaJ: conservation and adaptation of chaperone function. Cell Stress Chaperones 3: 28-36. (Pubitemid 28159676)
10. Costanzo M, Baryshnikova A, Bellay J, et al. (53 co-authors). 2010. The genetic landscape of a cell. Science 327: 425-431.
11. Craig EA, Huang P, Aron R, Andrew A. 2006. The diverse roles of J-proteins, the obligate Hsp70 co-chaperone. Rev Physiol Biochem Pharmacol. 156: 1-21.
12. Demoinet E, Jacquier A, Lutfalla G, Fromont-Racine M. 2007. The Hsp40 chaperone Jjj1 is required for the nucleo-cytoplasmic recycling of preribosomal factors in Saccharomyces cerevisiae. RNA 13: 1570-1581. (Pubitemid 47347427)
13. Dragovic Z, Broadley SA, Shomura Y, Bracher A, Hartl FU. 2006. Molecular chaperones of the Hsp110 family act as nucleotide exchange factors of Hsp70s. EMBO J. 25: 2519-2528. (Pubitemid 44012234)
14. Drummond DA, Bloom JD, Adami C, Wilke CO, Arnold FH. 2005. Why highly expressed proteins evolve slowly. Proc Natl Acad Sci USA. 102: 14338-14343. (Pubitemid 41429699)
15. Drummond DA, Wilke CO. 2009. The evolutionary consequences of erroneous protein synthesis. Nat Rev Genet. 10: 715-724.
16. Dujon B. 2010. Yeast evolutionary genomics. Nat Rev Genet. 11: 512-524.
17. Fan AC, Young JC. 2011. Function of cytosolic chaperones in Tom70-mediated mitochondrial import. Protein Pept Lett. 18: 122-131.
18. Fan CY, Ren HY, Lee P, Caplan AJ, Cyr DM. 2005. The type I Hsp40 zinc finger-like region is required for Hsp70 to capture non-native polypeptides from Ydj1. J Biol Chem. 280: 695-702. (Pubitemid 40165037)
19. Fitzpatrick DA, Logue ME, Stajich JE, Butler G. 2006. A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol Biol. 6: 99.
20. Glover JR, Lindquist S. 1998. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94: 73-82. (Pubitemid 28347471)
21. Gu X. 1999. Statistical methods for testing functional divergence after gene duplication. Mol Biol Evol. 16: 1664-1674.
22. Gu X. 2001. Maximum-likelihood approach for gene family evolution under functional divergence. Mol Biol Evol. 18: 453-464. (Pubitemid 32267997)
23. Gu X, Vander Velden K. 2002. DIVERGE: phylogeny-based analysis for functional-structural divergence of a protein family. Bioinformatics 18: 500-501. (Pubitemid 34284959)
24. Hartl FU, Bracher A, Hayer-Hartl M. 2011. Molecular chaperones in protein folding and proteostasis. Nature 475: 324-332.
25. Kampinga HH, Craig EA. 2010. The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol. 11: 579-592.
26. Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30: 3059-3066. (Pubitemid 34851225)
27. Kiefer F, Arnold K, Kunzli M, Bordoli L, Schwede T. 2009. The SWISS-MODEL repository and associated resources. Nucleic Acids Res. 37: D387-D392.
28. Le SQ, Gascuel O. 2008. An improved general amino acid replacement matrix. Mol Biol Evol. 25: 1307-1320. (Pubitemid 351882003)
29. Li J, Qian X, Sha B. 2003. The crystal structure of the yeast Hsp40 Ydj1 complexed with its peptide substrate. Structure 11: 1475-1483. (Pubitemid 37510348)
30. Li J, Sha B. 2005. Structure-based mutagenesis studies of the peptide substrate binding fragment of type I heat-shock protein 40. Biochem J. 386: 453-460. (Pubitemid 40445869)
31. Linke K,Wolfram T, Bussemer J, Jakob U. 2003. The roles of the two zinc binding sites in DnaJ. J Biol Chem. 278: 44457-44466. (Pubitemid 37377197)
32. Lopez-Buesa P, Pfund C, Craig EA. 1998. The biochemical properties of the ATPase activity of a 70-kDa heat shock protein (Hsp70) are governed by the C-terminal domains. Proc Natl Acad Sci USA. 95: 15253-15258. (Pubitemid 29018685)
33. Loytynoja A, Goldman N. 2005. An algorithm for progressive multiple alignment of sequences with insertions. Proc Natl Acad Sci USA. 102: 10557-10562. (Pubitemid 41061593)
34. Lynch M, Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155.
35. Malakhov MP, Mattern MR, Malakhova OA, Drinker M, Weeks SD, Butt TR. 2004. SUMO fusions and SUMO-specific protease for efficient expression and purification of proteins. J Struct Funct Genomics. 5: 75-86. (Pubitemid 39030623)
36. Mayer MP. 2010. Gymnastics of molecular chaperones. Mol Cell. 39: 321-331.
37. Meyer AE, Hung NJ, Yang P, Johnson AW, Craig EA. 2007. The specialized cytosolic J-protein, Jjj1, functions in 60S ribosomal subunit biogenesis. Proc Natl Acad Sci USA. 104: 1558-1563. (Pubitemid 46214629)
38. Mullen JR, Brill SJ. 2008. Activation of the Slx5-Slx8 ubiquitin ligase by poly-small ubiquitin-like modifier conjugates. J Biol Chem. 283: 19912-19921.
39. Ohno S. 1970. Evolution by gene duplication. New York: Springer.
40. Pais JE, Schilke B, Craig EA. 2011. Reevaluation of the role of the Pam18: Pam16 interaction in translocation of proteins by the mitochondrial Hsp70-based import motor. Mol Biol Cell. 22: 4740-4749.
41. Pan X, Ye P, Yuan DS, Wang X, Bader JS, Boeke JD. 2006. A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 124: 1069-1081. (Pubitemid 43344244)
42. Peden JF. 1999. Analysis of codon usage [PhD thesis]. [Nottingham (UK)]: University of Nottingham.
43. R Development Core Team. R: a language and environment for statistical computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2012. R version 2.15.1 (2012-06-22). ISBN 3-900051-07-0. Available from: http://www.R-project.org.
44. Raviol H, Sadlish H, Rodriguez F, Mayer MP, Bukau B. 2006. Chaperone network in the yeast cytosol: Hsp110 is revealed as an Hsp70 nucleotide exchange factor. EMBO J. 25: 2510-2518. (Pubitemid 44012233)
45. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. (Pubitemid 37038874)
46. Sahi C, Craig EA. 2007. Network of general and specialty J protein chaperones of the yeast cytosol. Proc Natl Acad Sci USA. 104: 7163-7168. (Pubitemid 47186026)
47. Sahi C, Lee T, Inada M, Pleiss JA, Craig EA. 2010. Cwc23, an essential J protein critical for pre-mRNA splicing with a dispensable J domain. Mol Cell Biol. 30: 33-42.
48. Schiller D. 2009. Pam17 and Tim44 act sequentially in protein import into the mitochondrial matrix. Int J Biochem Cell Biol. 41: 2343-2349.
49. Shaner L, Sousa R, Morano KA. 2006. Characterization of Hsp70 binding and nucleotide exchange by the yeast Hsp110 chaperone Sse1. Biochemistry 45: 15075-15084. (Pubitemid 44937020)
50. Sharp PM, Cowe E. 1991. Synonymous codon usage in Saccharomyces cerevisiae. Yeast 7: 657-678.
51. Stajich JE, Block D, Boulez K, et al. (21 co-authors). 2002. The Bioperl toolkit: Perl modules for the life sciences. Genome Res. 12: 1611-1618. (Pubitemid 35175100)
52. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690. (Pubitemid 44642609)
53. 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.
54. Terada K, Kanazawa M, Bukau B, Mori M. 1997. The human DnaJ homologue dj2 facilitates mitochondrial protein import and luciferase refolding. J Cell Biol. 139: 1089-1095. (Pubitemid 27523199)
55. van der Laan M, Chacinska A, Lind M, Perschil I, Sickmann A, Meyer HE, Guiard B, Meisinger C, Pfanner N, Rehling P. 2005. Pam17 is required for architecture and translocation activity of the mitochondrial protein import motor. Mol Cell Biol. 25: 7449-7458. (Pubitemid 41170109)
56. Vos MJ, Hageman J, Carra S, Kampinga HH. 2008. Structural and functional diversities between members of the human HSPB, HSPH, HSPA, and DNAJ chaperone families. Biochemistry 47: 7001-7011. (Pubitemid 351956349)
57. 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. (Pubitemid 39136416)
58. Whelan S, Goldman N. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol. 18: 691-699. (Pubitemid 32372940)
59. Wolfe KH, Shields DC. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387: 708-713. (Pubitemid 27270611)
60. Wright F. 1990. The "effective number of codons" used in a gene. Gene 87: 23-29. (Pubitemid 20139850)
61. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24: 1586-1591. (Pubitemid 47236688)
62. 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. (Pubitemid 39392196)
63. Zhao R, Davey M, Hsu YC, Kaplanek P, Tong A, Parsons AB, Krogan N, Cagney G, Mai D, Greenblatt J, Boone C, Emili A, Houry WA. 2005. Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 120: 715-727. (Pubitemid 40343082)