ATPase activity and ATP-dependent conformational change in the Co-chaperone HSP70/HSP90-organizing protein (HOP)

Journal of Biological Chemistry

Volumn 289, Issue 14, 2014, Pages 9880-9886

  Yamamoto, Soh ^a,b   Subedi, Ganesh Prasad ^c   Hanashima, Shinya ^c   Satoh, Tadashi ^c   Otaka, Michiro ^d   Wakui, Hideki ^a,e   Sawada, Ken Ichi ^e   Yokota, Shin Ichi ^b   Yamaguchi, Yoshiki ^c   Kubota, Hiroshi ^a   Itoh, Hideaki ^a  

^a AKITA UNIVERSITY   (Japan)

^b SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c RIKEN   (Japan)

^d JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e AKITA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

ATP-ASE ACTIVITY; ATP-BINDING; ATPASE DOMAIN; CELLULAR HOMEOSTASIS; CONFORMATIONAL CHANGE; DELETION MUTANTS; MOLECULAR CHAPERONES; PROTEIN QUALITY CONTROL;

PROTEINS;

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; AMINO ACID; CHAPERONE; HEAT SHOCK PROTEIN 90; HSP70 HSP90 ORGANIZING PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; HYDROLYSIS; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION;

HEAT SHOCK PROTEIN; HSP90; MOLECULAR CHAPERONE; PROTEIN COMPLEXES; PROTEIN STRUCTURE;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYDROLYSIS; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE DELETION;

EID: 84898064231     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.553255     Document Type: Article

References (42)

1. Hartl, F. U., Bracher, A., and Hayer-Hartl, M. (2011) Molecular chaper-ones in protein folding and proteostasis. Nature 475, 324-332
2. Itoh, H., and Tashima, Y. (1991) The stress (heat shock) proteins. Int. J. Biochem. 23, 1185-1191
3. Kubota, H. (2009) Quality control against misfolded proteins in the cyto-sol: a network for cell survival. J. Biochem. 146, 609-616
4. Mayer, M. P., and Bukau, B. (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol. Life Sci. 62, 670-684
5. Flaherty, K. M., DeLuca-Flaherty, C., and McKay, D. B. (1990) Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature 346, 623-628
6. Morshauser, R. C., Hu, W., Wang, H., Pang, Y., Flynn, G. C., and Zuider-weg, E. R. (1999) High-resolution solution structure of the 18 kDa substrate-binding domain of the mammalian chaperone protein Hsc70. J. Mol. Biol. 289, 1387-1403
7. Ali, M. M., Roe, S. M., Vaughan, C. K., Meyer, P., Panaretou, B., Piper, P. W., Prodromou, C., and Pearl, L. H. (2006) Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 440, 1013-1017
8. Mayer, M. P. (2010) Gymnastics of molecular chaperones. Mol. Cell 39, 321-331
9. Li, J., Richter, K., and Buchner, J. (2011) Mixed Hsp90-cochaperone complexes are important for the progression of the reaction cycle. Nat. Struct. Mol. Biol. 18, 61-66
10. Kubota, H., Yamamoto, S., Itoh, E., Abe, Y., Nakamura, A., Izumi, Y., Okada, H., Iida, M., Nanjo, H., Itoh, H., and Yamamoto, Y. (2010) Increased expression of co-chaperone HOP with HSP90 and HSC70 and complex formation in human colonic carcinoma. Cell Stress Chaperones 15, 1003-1011
11. Smith, D. F., and Toft, D. O. (2008) Minireview: the intersection of steroid receptors with molecular chaperones: observations and questions. Mol. Endocrinol. 22, 2229-2240
12. Wegele, H., Müller, L., and Buchner, J. (2004) Hsp70 and Hsp90-a relay team for protein folding. Rev. Physiol. Biochem. Pharmacol. 151, 1-44
13. Richter, K., Muschler, P., Hainzl, O., Reinstein, J., and Buchner, J. (2003) Sti1 is a non-competitive inhibitor of the Hsp90 ATPase. Binding prevents the N-terminal dimerization reaction during the ATPase cycle. J. Biol. Chem. 278, 10328-10333
14. Wegele, H., Haslbeck, M., Reinstein, J., and Buchner, J. (2003) Sti1 is a novel activator of the Ssa proteins. J. Biol. Chem. 278, 25970-25976
15. Wegele, H., Wandinger, S. K., Schmid, A. B., Reinstein, J., and Buchner, J. (2006) Substrate transfer from the chaperone Hsp70 to Hsp90. J. Mol. Biol. 356, 802-811
16. Odunuga, O. O., Longshaw, V. M., and Blatch, G. L. (2004) Hop: more than an Hsp70/Hsp90 adaptor protein. Bioessays 26, 1058-1068
17. Yi, F., Doudevski, I., and Regan, L. (2010) HOP is a monomer: investigation of the oligomeric state of the co-chaperone HOP. Protein Sci. 19, 19-25
18. Blatch, G. L., and Lassle, M. (1999) The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21, 932-939
19. Scheufler, C., Brinker, A., Bourenkov, G., Pegoraro, S., Moroder, L., Bar-tunik, H., Hartl, F. U., and Moarefi, I. (2000) Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101, 199-210
20. Kajander, T., Sachs, J. N., Goldman, A., and Regan, L. (2009) Electrostatic interactions of Hsp-organizing protein tetratricopeptide domains with Hsp70 andHsp90: computational analysis and protein engineering. J. Biol. Chem. 284, 25364-25374
21. Schmid, A. B., Lagleder, S., Grawert, M. A., Rohl, A., Hagn, F., Wandinger, S. K., Cox, M. B., Demmer, O., Richter, K., Groll, M., Kessler, H., and Buchner, J. (2012) The architecture of functional modules in the Hsp90 co-chaperone Sti1/Hop. EMBOJ.
22. Flom, G., Weekes, J., Williams, J. J., and Johnson, J. L. (2006) Effect of mutation of the tetratricopeptide repeat and asparatate-proline 2 domains of Sti1 on Hsp90 signaling and interaction in Saccharomyces cerevisiae. Genetics 172, 41-51
23. Ishida, R., Takaoka, Y., Yamamoto, S., Miyazaki, T., Otaka, M., Watanabe, S., Komatsuda, A., Wakui, H., Sawada, K., Kubota, H., and Itoh, H. (2008) Cisplatin differently affects amino terminal and carboxyl terminal domains of HSP90. FEBSLett. 582, 3879-3883
24. Yamamoto, S., Nakano, S., Owari, K., Fuziwara, K., Ogawa, N., Otaka, M., Tamaki, K., Watanabe, S., Komatsuda, A., Wakui, H, Sawada, K., Kubota, H, and Itoh, H. (2010) Gentamicin inhibits HSP70-assisted protein folding by interfering with substrate recognition. FEBS Lett. 584, 645-651
25. Vetter, I. R., and Wittinghofer, A. (1999) Nucleoside triphosphate-binding proteins: different scaffolds to achieve phosphoryl transfer. Q. Rev. Bio-phys. 32, 1-56
26. Traut, T. W. (1994) The functions and consensus motifs of nine types of peptide segments that form different types of nucleotide-binding sites. Eur. J. Biochem. 222, 9-19
27. Ghosh, J.G., Houck, S. A., Doneanu, C.E., and Clark, J.I. (2006) The/34-/38 groove is an ATP-interactive site in the a crystallin core domain of the small heat shock protein, human aB crystallin. J. Mol. Biol. 364, 364-375
28. Prodromou, C, Roe, S. M., O'Brien, R., Ladbury, J. E., Piper, P. W., and Pearl, L. H. (1997) Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell90, 65-75
29. Boisvert, D. C, Wang, J., Otwinowski, Z., Horwich, A. L., and Sigler, P. B. (1996) The 2.4 A crystal structure of the bacterial chaperonin GroEL com-plexed with ATP7S. Nat. Struct. Biol. 3, 170-177
30. Meyer, A. S., Gillespie, J. R., Walther, D., Millet, I. S., Doniach, S., and Frydman, J. (2003) Closing the folding chamber of the eukaryotic chaper-onin requires the transition state of ATP hydrolysis. Cell 113, 369-381
31. Hessling, M., Richter, K., and Buchner, J. (2009) Dissection of the ATP-induced conformational cycle of the molecular chaperone Hsp90. Nat. Struct. Mol. Biol. 16, 287-293
32. Flom, G., Behal, R. H., Rosen, L., Cole, D. G., and Johnson, J. L. (2007) Definition of the minimal fragments of Sti1 required for dimerization, interaction with Hsp70 and Hsp90 and in vivo functions. Biochem. J. 404, 159-167
33. Gaiser, A. M., Brandt, F., and Richter, K. (2009) The non-canonical Hop protein from Caenorhabditis elegans exerts essential functions and forms binary complexes with either Hsc70 or Hsp90. J. Mol. Biol. 391, 621-634
34. Carrigan, P. E., Riggs, D. L., Chinkers, M., and Smith, D. F. (2005) Functional comparison of human and Drosophila Hop reveals novel role in steroid receptor maturation. J. Biol. Chem. 280, 8906-8911
35. Onuoha, S.C., Coulstock, E. T., Grossmann, J. G., and Jackson, S. E. (2008) Structural studies on the co-chaperone Hop and its complexes with Hsp90. J. Mol. Biol. 379, 732-744
36. Song, H. O., Lee, W., An, K., Lee, H. S., Cho, J. H., Park, Z. Y., and Ahnn, J. (2009) C. elegans STI-1, the homolog of Sti1/Hop, is involved in aging and stress response. J. Mol. Biol. 390, 604-617.
37. Marozkina, N. V., Yemen, S., Borowitz, M., Liu, L., Plapp, M., Sun, F., Islam, R., Erdmann-Gilmore, P., Townsend, R. R., Lichti, C. F., Mantri, S., Clapp, P. W., Randell, S. H., Gaston, B., and Zaman, K. (2010) Hsp 70/Hsp 90 organizing protein as a nitrosylation target in cystic fibrosis therapy. Proc. Natl. Acad. Sci. U.S.A. 107, 11393-11398
38. Gangaraju, V. K., Yin, H., Weiner, M. M., Wang, J., Huang, X. A., and Lin, H. (2011) Drosophila Piwi functions in Hsp90-mediated suppression of phenotypic variation. Nat. Genet. 43, 153-158
39. Chen, L., Hamada, S., Fujiwara, M., Zhu, T., Thao, N. P., Wong, H. L., Krishna, P., Ueda, T., Kaku, H., Shibuya, N., Kawasaki, T., and Shimamoto, K. (2010) The Hop/Sti1-Hsp90 chaperone complex facilitates the maturation and transport of a PAMP receptor in rice innate immunity. Cell Host Microbe 7, 185-196
40. Zanata, S. M., Lopes, M. H., Mercadante, A. F., Hajj, G. N., Chiarini, L. B., Nomizo, R., Freitas, A. R., Cabral, A. L., Lee, K. S., Juliano, M. A., de Oliveira, E., Jachieri, S. G., Burlingame, A., Huang, L., Linden, R., Brentani, R. R., and Martins, V. R. (2002) Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection. EMBO J. 21, 3307-3316
41. Longshaw, V. M., Chapple, J. P., Balda, M. S., Cheetham, M. E., and Blatch, G. L.(2004) Nuclear translocation of the Hsp70/Hsp90 organizing protein mSTI1 is regulated by cell cycle kinases. J. Cell Sci. 117, 701-710
42. Lopes, M. H., Hajj, G. N., Muras, A. G., Mancini, G. L., Castro, R. M., Ribeiro, K. C., Brentani, R. R., Linden, R., and Martins, V. R. (2005) Interaction of cellular prion and stress-inducible protein 1 promotes neurito-genesis and neuroprotection by distinct signaling pathways. J. Neurosci. 25, 11330-11339