A ribosome-anchored chaperone network that facilitates eukaryotic ribosome biogenesis

Journal of Cell Biology

Volumn 189, Issue 1, 2010, Pages 69-81

  Albanèse, Véronique ^a   Reissmann, Stefanie ^a,b   Frydman, Judith ^a  

^a STANFORD UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CHAPERONES LINKED TO PROTEIN SYNTHESIS; HEAT SHOCK PROTEIN 70; JJJ1 PROTEIN; PROTEIN; RIBOSOME RNA; RNA 25S; RNA 35S; STRESS 70 B RIBOSOME ASSOCIATED COMPLEX; UNCLASSIFIED DRUG; ZUO1 PROTEIN;

ARTICLE; BIOGENESIS; EUKARYOTE; GENE INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RIBOSOME; RNA PROCESSING;

CYTOSOL; EUKARYOTA; HSP40 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; MOLECULAR CHAPERONES; PROTEIN FOLDING; RIBOSOMES; RNA, RIBOSOMAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA;

EID: 77950573146     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201001054     Document Type: Article

References (52)

1. Agashe, V.R., S. Guha, H.C. Chang, P. Genevaux, M. Hayer-Hartl, M. Stemp, C. Georgopoulos, F.U. Hartl, and J.M. Barrai. 2004. Function of trigger factor and. DnaK in multidomain protein folding: increase in yield at the expense of folding speed. Cell. 117:199-209. doi:10.1016/ S0092-8674(04)00299-305
2. Albanèse, V., A.Y. Yam, J. Baughman, C. Parnot, and J. Frydman. 2006. Systems analyses reveal two chaperone networks with distinct functions in eukaryotic cells. Cell. 124:75-88. doi: 10.1016/j.ccll.2005.11.039 (Pubitemid 43069311)
3. Balch, W.E., R.I. Morimoto, A. Dillin, and J.W. Kelly. 2008. Adapting proteostasis for disease intervention. Science. 319:916-919. doi:10.1126/ science.1141448
4. Bobula, J., K. Tomala, E. Jez, D.M. W'loch, R.H. Borts, and R. Korona. 2006. Why molecular chaperones buffer mutational damage: a case study with ayeast Hsp40/70 system. Genetics. 174:937-944. doi:10.1534/ genetics.106.061564
5. Bukau, B., J. Weissman, and A. Horwich. 2006. Molecular chaperones and protein quality control. Cell. 125:443-451. doi:10.1016/j.cell.2006.04.014
6. Caplan, A.J., D.M. Cyr, and M.G. Douglas. 1992. YDJ 1p facilitates polypeptide translocation across different intracellular membranes by a conserved mechanism. Cell. 71:1143-1155. doi:10.1016/S0092-8674(05)80063-7
7. Cyr, D.M., T. Langer, and M.G. Douglas. 1994. DnaJ-like proteins: molecular chaperones and specific regulators of Hsp70. Trends Biochem. Sci. 19:176-181. doi:10.1016/0968-0004(94)90281-X
8. De Marchis, M.L., A. Giorgi, ME. Schininà, I. Bozzoni, and A. Fatica. 2005. Rrp15p, a novel component of pre-ribosomal particles required for 60S ribosome submit maturation. RNA. 11:495-502. doi:10.1261/rna.7200205
9. Demoinet, E., A. Jacquier, G. Lutfalla, and M. Fromont-Racine. 2007. The Hsp40 chaperone Jjj 1 is required for the nucleo-cytoplasmic recycling of preribosomal factors in Sacchammyces cerevisiae. RNA. 13: 1570-1581.
10. El Hage, A., and J.H. Alix. 2004. Authentic precursors to ribosomal subunits accumulate in Escherichia coli in the absence of functional DnaK chaperone. Mol. Micmbiol. 51:189-201. doi:10.1046/j.1365-2958 .2003.03813.x (Pubitemid 38031081)
11. El Hage, A., M. Sbaï, and J.H. Alix. 2001. The chaperonin Groel and other heat-shock proteins, besides DnaK, participate in ribosome biogenesis in Escherichia, coli. Mol. Gen. Genet. 264:796-808. doi:10.1007/ S004380000369
12. Fatica, A., and D. Tollervey. 2002. Making ribosomes. Curr. Opin. Cell Biol. 14:313-318. doi:10.1.016/S0955-0674(02)00336-8
13. Forsburg, S.L. 2001. The art and design of genetic screens: yeast. Nat. Rev. Genet. 2:659-668. doi:10.1038/35088500 (Pubitemid 33674788)
14. Fromont-Racine, M., B. Senger, C. Saveanu, and F. Fasiolo. 2003. Ribosome assembly in eukaryotes. Gene. 313:17-42. doi:10.1016/S0378-1119(03) 00629-2
15. Frydman, J. 2001. Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu. Rev. Biochem. 70:603-647. doi.:10.1146/annurev .biochem.70.1.603 (Pubitemid 32662220)
16. Gautschi, M, H. Lilie, U. Fünfschilling, A. Mun, S. Ross, T. Lithgow, P. Rücknagel, and S. Rospert. 2001. RAC, a stable ribosome-associated complex in yeast formed by the DnaK-DnaJ homologs Ssz1p and zuotin. Proc. Natl. Acad. Sci. USA. 98:3762-3767. doi:10.1073/pnas .071057198 (Pubitemid 32249845)
17. Gautschi, M., A. Mun, S. Ross, and. S. Rospert. 2002. A functional. chaperone triad on the yeast ribosome. Pmc. Natl. Acad. Sci. USA. 99:4209-4214. doi:10.1073/pnas.062048599
18. Hartl, F.U., M. Hayer-Hartl, M. Hayer-Hartl, and M. Hayer-Hartl. 2009. Converging concepts of protein folding in vitro and in vivo. Nat. Struct. Mol. Biol. 16:574-581. doi:10.1038/nsmb.1591
19. Hogan, D.J., D.P. Riordan, A.P. Gerber, D. Herschlag, and P.O. Brown. 2008. Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol. 6:e255. doi:10.1371/journal.pbio.0060255
20. Horsey, E.W., J. Jakovljevic, T.D. Miles, P. Harnpicharnchai, and J.L. Woolford Jr. 2004. Role of the yeast Rrp1 protein in the dynamics of pre-ribosome maturation. RNA. 10:813-827. doi:10.1261/rna.5255804
21. Huang, P., M. Gautschi, W. Walter, S. Rospert, and E.A. Craig. 2005. The Hsp70 Ssz1 modulates the function of the ribosome-associated J-protein Zuo1. Nat. Struct. Mol. Biol, 12:497-504. doi:10.1038/nsmb942 (Pubitemid 43085879)
22. Huh, W.K., J.V. Falvo, L.C. Gerke, A.S. Carroll, R.W. Howson, J.S. Weissman, and E.K. O'Shea. 2003. Global analysis of protein localization in budding yeast. Nature. 425:686-691. doi:10.1038/nature02026 (Pubitemid 37314307)
23. Hurt, E., S. Hannus, B. Schmelzl, D. Lau, D. Tollervcy, and G. Simos. 1999. A novel in vivo assay reveals inhibition of ribosomal nuclear export in ran-cycle and nueleoporin mutants. J. Cell Biol. 144:389-401. doi:10 .1083/jcb.144.3.389
24. Kramer, G., D. Boehringer, N. Ban, and B. Bukau. 2009. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 16:589-597. doi: 10.1038/ nsmb.1614
25. la Cour, T., L. Kiemer, A. Mølgaard, R. Gupta, K. Skriver, and S. Brunak. 2004. Analysis and prediction of leucine-rich nuclear export signals. Protein Eng. Des. Sel. 17:527-536. doi:10.1093/protein/gzh062
26. Labbé, S., and DJ. Thiele. 1999. Copper ion inducible and rcpressible promoter systems in yeast. Methods Enzymol. 306:145-153. doi:10.1016/ S0076-6879(99)06010-6013 (Pubitemid 29356829)
27. Lebreton, A., C. Saveanu, L. Decourty, J.C. Rain, A. Jacquier, and M. Fromont-Racine. 2006. A functional network involved in the recycling of nucleocytoplasmic pre-60S factors. J. Cell Biol. 173:349-360. doi:10 .1083/jcb.200510080
28. Maki, J.A., DJ. Schnobrich, and G.M. Culver. 2002. The DnaK chaperone system facilitates 30S ribosomal subunit assembly. Mol. Cell. 10:129-138. doi:10.1016/S1097-2765(02)00562-2
29. Mayer, M.P., and B. Bukau. 2005. Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 62:670-684. doi:10.1007/ s0018-004-4464-4466
30. McClellan, A.J., and J.L. Brodsky. 2000. Mutation of the ATP-binding pocket of SSA1 indicates that a functional interaction between Ssa1p and Ydj 1p is required for post-translational translocation into the yeast endoplasmic reticulum. Genetics. 156:501-512.
31. McClellan, A.J., S. Tarn, D. Kaganovich, and J. Frydman. 2005. Protein quality control: chaperones culling corrupt conformations. Nat. Cell Biol. 7:736-741.doi:10.1038/ncb0805-736
32. McClellan, A.J., Y. Xia, A.M. Deutschbauer, R.W. Davis, M. Gerstein, and J. Frydman. 2007. Diverse cellular functions of the Hsp90 molecular chaperone uncovered using systems approaches. Cell. 131:121-135. doi: 10.1016/j.cell.2007. 07.036
33. Meyer, A.E., N.J. Hung, P. Yang, A.W. Johnson, and E.A. Craig. 2007. The specialized cytosolic J-protein, Jjj1., functions in 60S ribosomal subunit biogenesis. Proc. Natl. Acad. Sci. USA. 104:1558-1563. doi:10.1073/ pnas.0610704104
34. Meyer, A.E., L.A. Hoover, and E.A. Craig. 2010. The cytosolic J-protein, Jjj1, and Reil function in the removal of the pre-60 S subunit factor Aral. J. Biol. Chem. 285:961-968. doi:10.1074/jbc.M109.038349
35. Muldoon-Jacobs, K.L., and J.D. Dinman. 2006. Specific effects of ribosometethcred molecular chaperones on programmed -1 ribosomal frameshifting. Eukaryot, Cell. 5:762-770. doi:10.1128/EC.5.4.762-770.2006
36. Peng, W.T., M.D. Robinson, S. Mnaimneh, N.J. Krogan, G. Cagney, Q. Marris, A.P. Davierwala, J. Grigull, X. Yang, W. Zhang, et al. 2003. A panoramic view of yeast noncoding RNA processing. Cell. 113:919-933. doi: 10.1016/S0092-8674(03)00466-5
37. Pfund, C., N. Lopez-Hoyo, T. Ziegelhoffer, B.A. Schilke, P. Lopez-Buesa, W.A. Walter, M. Wiedmann, and E.A. Craig. 1998. The molecular chaperone Ssb from. Sacchammyces cerevisiae is a component of the ribosomenascent chain complex. EMBO J. 17:3981-3989. doi:10.1093/emboj/ 17.14.3981 (Pubitemid 28333983)
38. Puig, O., F. Caspary, G. Rigaut, B. Rutz, E. Bouvcret, E. Bragado-Nilsson, M. Wilm, and B. Séraphin. 2001. The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods. 24:2.18-229. doi:10.1006/meth.2001.1183 (Pubitemid 32846428)
39. Qiu, H., J. Eifert, L. Wacheul, M. Thiry, A.C. Berger, J. Jakovljevic, J.L. Woolford. Jr., A.H. Corbett, D.L. Lafontaine, R.M. Terns, and M.P. Terns. 2008. Identification of genes that function in the biogenesis and localization of small nucleolar RNAs in Sacchammyces cerevisiae. Mol. Celt. Biol. 28:3686-3699. doi:10.1128/MCB.01115-07
40. Raue, U., S. Ocllerer, and S. Rospert. 2007. Association of protein biogenesis factors at the yeast ribosomal tunnel exit is affected by the translational status and nascent polypeptide sequence. J. Biol. Chem. 282:7809-7816. (Pubitemid 47093553)
41. Reissmann, S., C. Parnot, C.R. Booth, W. Chiu, and J. Frydman. 2007. Essential function of the built-in lid in the allosteric regulation of eukaryotic and archaeal chaperonins. Nat. Struct. Mol. Biol. 14:432-440. doi:10.1038/nsmb1236 (Pubitemid 46685886)
42. Russell, R. 2008. RNA misfolding and the action of chaperones. Front. Biosei. 13:1-20. doi:10.2741/2557
43. Shulga, N., P. James, E.A. Craig, and D.S. Goldfarb. 1999. A nuclear export signal prevents Sacchammyces cerevisiae Hsp70 Ssb1p from stimulating nuclear localization signal-directed nuclear transport. J. Biol. Chem. 274:16501-16507. doi:10.1074/jbc.274.23.16501 (Pubitemid 129526407)
44. Strunk, B.S., and K. Karbstein. 2009. Powering through ribosome assembly. RNA. 15:2083-2104. doi:10.1261/rna.1792109
45. Sun, C., and J.L. Woolford Jr. 1994. The yeast NOP4 gene product is an essential nucleolar protein required for pre-rRNA processing and accumulation of 60S ribosomal subunits. EMBO J. 13:3127-3135. (Pubitemid 24213464)
46. Sung, M.K., and W.K. Huh. 2007. Bimolecular fluorescence complementation analysis system for in vivo detection of protein-protein interaction in Sacchammyces cerevisiae. Yeast. 24:767-775. doi:10.1002/yea.1504 (Pubitemid 47412457)
47. Tschochner, H., and E. Hurt. 2003. Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol. 13:255-263. doi:10.1016/ S0962-8924(03)00054-60
48. Wegrzyn, R.D., and E. Deuerling. 2005. Molecular guardians for newborn proteins: ribosome-associated chaperones and their role in protein folding. Cell. Mot. Life Sci. 62:2727-2738. doi:10.1007/s00018-005-5292-z
49. Winzeler, E. A., D.D. Shoemaker, A. Astromoff, H. Liang, K. Anderson, B. Andre, R. Bangham, R. Benito, J.D. Boeke, H. Bussey, et al. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science. 285:901-906. doi: 10.11267science.285.5429.901 (Pubitemid 29381993)
50. Yam, A.Y., V. Albanèse, H.T. Lin, and J. Frydman. 2005. Hsp 110 cooperates with different cytosolic HSP70 systems in a pathway for de novo folding. J. Biol. Chem. 280:41252-41261. doi:10.1074/jbc.M503615200
51. Yan, W., B. Schilke, C. Pfund, W. Walter, S. Kim. and E.A. Craig. 1998. Zuotin, a ribosome-associated DnaJ molecular chaperone. EMBO J. 17:4809-4817. do:i:10.1093/cmboj/17.16.4809 (Pubitemid 28377181)
52. Young, J.C., V.R. Agashe, K. Siegers, and F.U. Hartl. 2004. Pathways of chaperone-mediated protein folding in the cytosol. Nat. Rev. Mol. Celt Biol. 5:781-791. doi:10.1038/nrm1492