An inducible chaperone adapts proteasome assembly to stress

Molecular Cell

Volumn 55, Issue 4, 2014, Pages 566-577

  Hanssum, Ariane ^a,b   Zhong, Zhen ^a   Rousseau, Adrien ^a   Krzyzosiak, Agnieszka ^a   Sigurdardottir, Anna ^a   Bertolotti, Anne ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b MERCK KGAA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADC17 PROTEIN; ADENOSINE TRIPHOSPHATASE; CHAPERONE; MUTANT PROTEIN; PROTEASOME; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOGENESIS; CELL MUTANT; CELL STRESS; CONTROLLED STUDY; ENZYME ANALYSIS; GENE INTERACTION; IMMUNOPRECIPITATION; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; NONHUMAN; PHENOTYPE; PROTEIN ASSEMBLY; YEAST;

ADENOSINE TRIPHOSPHATASES; CIRCULAR DICHROISM; FUNGAL PROTEINS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; PROTEASOME ENDOPEPTIDASE COMPLEX; SEQUENCE ALIGNMENT; STRESS, PHYSIOLOGICAL; YEASTS;

EID: 84906791334     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.06.017     Document Type: Article

References (42)

1. Beck F., Unverdorben P., Bohn S., Schweitzer A., Pfeifer G., Sakata E., Nickell S., Plitzko J.M., Villa E., Baumeister W., Förster F. Near-atomic resolution structural model of the yeast 26S proteasome. Proc. Natl. Acad. Sci. USA 2012, 109:14870-14875.
2. Beckwith R., Estrin E., Worden E.J., Martin A. Reconstitution of the 26S proteasome reveals functional asymmetries in its AAA+ unfoldase. Nat. Struct. Mol. Biol. 2013, 20:1164-1172.
3. Brandman O., Stewart-Ornstein J., Wong D., Larson A., Williams C.C., Li G.-W., Zhou S., King D., Shen P.S., Weibezahn J., et al. A ribosome-bound quality control complex triggers degradation of nascent peptides and signals translation stress. Cell 2012, 151:1042-1054.
4. Cuanalo-Contreras K., Mukherjee A., Soto C. Role of protein misfolding and proteostasis deficiency in protein misfolding diseases and aging. Int. J. Cell Biol. 2013, 2013:638083.
5. da Fonseca P.C., He J., Morris E.P. Molecular model of the human 26S proteasome. Mol. Cell 2012, 46:54-66.
6. Elsasser S., Schmidt M., Finley D.D. Characterization of the proteasome using native gel electrophoresis. Methods Enzymol. 2005, 398:353-363.
7. Finley D.D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 2009, 78:477-513.
8. Fleischer T.C., Weaver C.M., McAfee K.J., Jennings J.L., Link A.J. Systematic identification and functional screens of uncharacterized proteins associated with eukaryotic ribosomal complexes. Genes Dev. 2006, 20:1294-1307.
9. Foiani M., Cigan A.M., Paddon C.J., Harashima S., Hinnebusch A.G. GCD2, a translational repressor of the GCN4 gene, has a general function in the initiation of protein synthesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 1991, 11:3203-3216.
10. Förster F., Lasker K., Beck F., Nickell S., Sali A., Baumeister W. An atomic model AAA-ATPase/20S core particle sub-complex of the 26S proteasome. Biochem. Biophys. Res. Commun. 2009, 388:228-233.
11. Funakoshi M., Tomko R.J., Kobayashi H., Hochstrasser M. Multiple assembly chaperones govern biogenesis of the proteasome regulatory particle base. Cell 2009, 137:887-899.
12. Ghislain M., Udvardy A., Mann C. S.cerevisiae 26S protease mutants arrest cell division in G2/metaphase. Nature 1993, 366:358-362.
13. Gietz R.D., Woods R.A. Yeast transformation by the LiAc/SS Carrier DNA/PEG method. Methods Mol. Biol. 2006, 313:107-120.
14. Goldberg A.L. Functions of the proteasome: from protein degradation and immune surveillance to cancer therapy. Biochem. Soc. Trans. 2007, 35:12-17.
15. Hanna J., Finley D.D. A proteasome for all occasions. FEBS Lett. 2007, 581:2854-2861.
16. Heinemeyer W., Kleinschmidt J.A., Saidowsky J., Escher C., Wolf D.H. Proteinase yscE, the yeast proteasome/multicatalytic-multifunctional proteinase: mutants unravel its function in stress induced proteolysis and uncover its necessity for cell survival. EMBO J. 1991, 10:555-562.
17. Hershko A., Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 1998, 67:425-479.
18. Kaneko T., Hamazaki J., Iemura S., Sasaki K., Furuyama K., Natsume T., Tanaka K., Murata S. Assembly pathway of the Mammalian proteasome base subcomplex is mediated by multiple specific chaperones. Cell 2009, 137:914-925.
19. Kim Y.E., Hipp M.S., Bracher A., Hayer-Hartl M., Hartl F.U. Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem. 2013, 82:323-355.
20. Kisselev A.F., Goldberg A.L. Proteasome inhibitors: from research tools to drug candidates. Chem. Biol. 2001, 8:739-758.
21. Kisselev A.F., Goldberg A.L. Monitoring activity and inhibition of 26S proteasomes with fluorogenic peptide substrates. Methods Enzymol. 2005, 398:364-378.
22. Lander G.C., Estrin E., Matyskiela M.E., Bashore C., Nogales E., Martin A. Complete subunit architecture of the proteasome regulatory particle. Nature 2012, 482:186-191.
23. Le Tallec B., Barrault M.B., Guérois R., Carré T., Peyroche A. Hsm3/S5b participates in the assembly pathway of the 19S regulatory particle of the proteasome. Mol. Cell 2009, 33:389-399.
24. Lee C.-S., Tee L.Y., Warmke T., Vinjamoori A., Cai A., Fagan A.M., Snider B.J. A proteasomal stress response: pre-treatment with proteasome inhibitors increases proteasome activity and reduces neuronal vulnerability to oxidative injury. J.Neurochem. 2004, 91:996-1006.
25. Morimoto R.I. The heat shock response: systems biology of proteotoxic stress in aging and disease. Cold Spring Harb. Symp. Quant. Biol. 2011, 76:91-99.
26. Murata S., Yashiroda H., Tanaka K. Molecular mechanisms of proteasome assembly. Nat. Rev. Mol. Cell Biol. 2009, 10:104-115.
27. Navon A., Ciechanover A. The 26S proteasome: from basic mechanisms to drug targeting. J.Biol. Chem. 2009, 284:33713-33718.
28. Park S., Li X., Kim H.M., Singh C.R., Tian G., Hoyt M.A., Lovell S., Battaile K.P., Zolkiewski M., Coffino P., et al. Reconfiguration of the proteasome during chaperone-mediated assembly. Nature 2013, 497:512-516.
29. Roelofs J., Park S., Haas W., Tian G., McAllister F.E., Huo Y., Lee B.H., Zhang F., Shi Y., Gygi S.P., Finley D. Chaperone-mediated pathway of proteasome regulatory particle assembly. Nature 2009, 459:861-865.
30. Rubin D.M., Glickman M.H., Larsen C.N., Dhruvakumar S., Finley D.D. Active site mutants in the six regulatory particle ATPases reveal multiple roles for ATP in the proteasome. EMBO J. 1998, 17:4909-4919.
31. Saeki Y., Tanaka K. Assembly and function of the proteasome. Methods Mol. Biol. 2012, 832:315-337.
32. Saeki Y., Toh-E A., Kudo T., Kawamura H., Tanaka K. Multiple proteasome-interacting proteins assist the assembly of the yeast 19S regulatory particle. Cell 2009, 137:900-913.
33. Schwartz A.L., Ciechanover A. Targeting proteins for destruction by the ubiquitin system: implications for human pathobiology. Annu. Rev. Pharmacol. Toxicol. 2009, 49:73-96.
34. Sherman M.Y., Goldberg A.L. Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron 2001, 29:15-32.
35. Soto C. Unfolding the role of protein misfolding in neurodegenerative diseases. Nat. Rev. Neurosci. 2003, 4:49-60.
36. Suraweera A., Münch C., Hanssum A., Bertolotti A. Failure of amino acid homeostasis causes cell death following proteasome inhibition. Mol. Cell 2012, 48:242-253.
37. Tan S. A modular polycistronic expression system for overexpressing protein complexes in Escherichia coli. Protein Expr. Purif. 2001, 21:224-234.
38. Tanaka K., Mizushima T., Saeki Y. The proteasome: molecular machinery and pathophysiological roles. Biol. Chem. 2012, 393:217-234.
39. Tomko R.J.J., Hochstrasser M. Molecular architecture and assembly of the eukaryotic proteasome. Annu. Rev. Biochem. 2013, 82:415-445.
40. Tomko R.J., Funakoshi M., Schneider K., Wang J., Hochstrasser M. Heterohexameric ring arrangement of the eukaryotic proteasomal ATPases: implications for proteasome structure and assembly. Mol. Cell 2010, 38:393-403.
41. Walter P., Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011, 334:1081-1086.
42. Xie Y., Varshavsky A. RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: a negative feedback circuit. Proc. Natl. Acad. Sci. USA 2001, 98:3056-3061.