Middle domain of human Hsp90 isoforms differentially binds Aha1 in human cells and alters Hsp90 activity in yeast

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1853, Issue 2, 2015, Pages 445-452

  Synoradzki, Kamil ^a   Bieganowski, Pawel ^a  

^a MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

Author keywords

Aha1; CIAP1; Hsp90; Human; Isoform; Yeast

Indexed keywords

AMINO ACID; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 ALPHA; HEAT SHOCK PROTEIN 90 BETA; INHIBITOR OF APOPTOSIS PROTEIN 1; PROTEIN; PROTEIN AHA1; TANESPIMYCIN; UNCLASSIFIED DRUG; AHSA1 PROTEIN, HUMAN; CHAPERONE; HCH1 PROTEIN, S CEREVISIAE; INHIBITOR OF APOPTOSIS PROTEIN; ISOPROTEIN; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CONTROLLED STUDY; GENE INTERACTION; HEK293 CELL LINE; HUMAN; HUMAN CELL; PHENOTYPE; POINT MUTATION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; YEAST CELL; CHEMISTRY; GENETICS; METABOLISM; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE; STRUCTURE ACTIVITY RELATION;

EUKARYOTA;

HEK293 CELLS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MOLECULAR CHAPERONES; MUTATION; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84916886859     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.11.026     Document Type: Article

References (58)

1. Borkovich K.A., Farrelly F.W., Finkelstein D.B., Taulien J., Lindquist S. hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol. Cell. Biol. 1989, 9:3919-3930.
2. Meyer P., Prodromou C., Hu B., Vaughan C., Roe S.M., Panaretou B., Piper P.W., Pearl L.H. Structural and functional analysis of the middle segment of hsp90: implications for ATP hydrolysis and client protein and cochaperone interactions. Mol. Cell 2003, 11:647-658.
3. Harris S.F., Shiau A.K., Agard D.A. The crystal structure of the carboxy-terminal dimerization domain of htpG, the Escherichia coli Hsp90, reveals a potential substrate binding site. Structure 2004, 12:1087-1097.
4. Stebbins C.E., Russo A.A., Schneider C., Rosen N., Hartl F.U., Pavletich N.P. Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 1997, 89:239-250.
5. Prodromou C., Roe S.M., O'Brien R., Ladbury J.E., Piper P.W., Pearl L.H. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 1997, 90:65-75.
6. Lai B.T., Chin N.W., Stanek A.E., Keh W., Lanks K.W. Quantitation and intracellular localization of the 85K heat shock protein by using monoclonal and polyclonal antibodies. Mol. Cell. Biol. 1984, 4:2802-2810.
7. McDowell C.L., Bryan Sutton R., Obermann W.M. Expression of Hsp90 chaperone [corrected] proteins in human tumor tissue. Int. J. Biol. Macromol. 2009, 45:310-314.
8. Nollen E.A., Morimoto R.I. Chaperoning signaling pathways: molecular chaperones as stress-sensing 'heat shock' proteins. J. Cell Sci. 2002, 115:2809-2816.
9. Garnier C., Lafitte D., Jorgensen T.J., Jensen O.N., Briand C., Peyrot V. Phosphorylation and oligomerization states of native pig brain HSP90 studied by mass spectrometry. Eur. J. Biochem. 2001, 268:2402-2407.
10. Metchat A., Akerfelt M., Bierkamp C., Delsinne V., Sistonen L., Alexandre H., Christians E.S. Mammalian heat shock factor 1 is essential for oocyte meiosis and directly regulates Hsp90alpha expression. J. Biol. Chem. 2009, 284:9521-9528.
11. Barnier J.V., Bensaude O., Morange M., Babinet C. Mouse 89 kD heat shock protein. Two polypeptides with distinct developmental regulation. Exp. Cell Res. 1987, 170:186-194.
12. Krone P.H., Sass J.B. HSP 90 alpha and HSP 90 beta genes are present in the zebrafish and are differentially regulated in developing embryos. Biochem. Biophys. Res. Commun. 1994, 204:746-752.
13. Somji S., Ann Sens M., Garrett S.H., Gurel V., Todd J.H., Sens D.A. Expression of hsp 90 in the human kidney and in proximal tubule cells exposed to heat, sodium arsenite and cadmium chloride. Toxicol. Lett. 2002, 133:241-254.
14. Minami Y., Kawasaki H., Miyata Y., Suzuki K., Yahara I. Analysis of native forms and isoform compositions of the mouse 90-kDa heat shock protein, HSP90. J. Biol. Chem. 1991, 266:10099-10103.
15. Nemoto T., Ohara-Nemoto Y., Ota M., Takagi T., Yokoyama K. Mechanism of dimer formation of the 90-kDa heat-shock protein. Eur. J. Biochem. 1995, 233:1-8.
16. Moullintraffort L., Bruneaux M., Nazabal A., Allegro D., Giudice E., Zal F., Peyrot V., Barbier P., Thomas D., Garnier C. Biochemical and biophysical characterization of the Mg2+-induced 90-kDa heat shock protein oligomers. J. Biol. Chem. 2010, 285:15100-15110.
17. Hartson S.D., Matts R.L. Approaches for defining the Hsp90-dependent proteome. Biochim. Biophys. Acta 2012, 1823:656-667.
18. Echeverria P.C., Bernthaler A., Dupuis P., Mayer B., Picard D. An interaction network predicted from public data as a discovery tool: application to the Hsp90 molecular chaperone machine. PLoS One 2011, 6:e26044.
19. Kunisawa J., Shastri N. Hsp90alpha chaperones large C-terminally extended proteolytic intermediates in the MHC class I antigen processing pathway. Immunity 2006, 24:523-534.
20. Peterson L.B., Eskew J.D., Vielhauer G.A., Blagg B.S. The hERG channel is dependent upon the Hsp90alpha isoform for maturation and trafficking. Mol. Pharm. 2012, 9:1841-1846.
21. Grad I., Cederroth C.R., Walicki J., Grey C., Barluenga S., Winssinger N., De Massy B., Nef S., Picard D. The molecular chaperone Hsp90alpha is required for meiotic progression of spermatocytes beyond pachytene in the mouse. PLoS One 2010, 5:e15770.
22. Eustace B.K., Sakurai T., Stewart J.K., Yimlamai D., Unger C., Zehetmeier C., Lain B., Torella C., Henning S.W., Beste G., Scroggins B.T., Neckers L., Ilag L.L., Jay D.G. Functional proteomic screens reveal an essential extracellular role for hsp90 alpha in cancer cell invasiveness. Nat. Cell Biol. 2004, 6:507-514.
23. Voss A.K., Thomas T., Gruss P. Mice lacking HSP90beta fail to develop a placental labyrinth. Development 2000, 127:1-11.
24. Didelot C., Lanneau D., Brunet M., Bouchot A., Cartier J., Jacquel A., Ducoroy P., Cathelin S., Decologne N., Chiosis G., Dubrez-Daloz L., Solary E., Garrido C. Interaction of heat-shock protein 90 beta isoform (HSP90 beta) with cellular inhibitor of apoptosis 1 (c-IAP1) is required for cell differentiation. Cell Death Differ. 2008, 15:859-866.
25. Angelo G., Lamon-Fava S., Sonna L.A., Lindauer M.L., Wood R.J. Heat shock protein 90beta: a novel mediator of vitamin D action. Biochem. Biophys. Res. Commun. 2008, 367:578-583.
26. Kuo C.C., Liang C.M., Lai C.Y., Liang S.M. Involvement of heat shock protein (Hsp)90 beta but not Hsp90 alpha in antiapoptotic effect of CpG-B oligodeoxynucleotide. J. Immunol. 2007, 178:6100-6108.
27. Cortes-Gonzalez C., Barrera-Chimal J., Ibarra-Sanchez M., Gilbert M., Gamba G., Zentella A., Flores M.E., Bobadilla N.A. Opposite effect of Hsp90alpha and Hsp90beta on eNOS ability to produce nitric oxide or superoxide anion in human embryonic kidney cells. Cell. Physiol. Biochem. 2010, 26:657-668.
28. Gao Y., Yechikov S., Vazquez A.E., Chen D., Nie L. Distinct roles of molecular chaperones HSP90alpha and HSP90beta in the biogenesis of KCNQ4 channels. PLoS One 2013, 8:e57282.
29. Wandinger S.K., Richter K., Buchner J. The Hsp90 chaperone machinery. J. Biol. Chem. 2008, 283:18473-18477.
30. Chadli A., Felts S.J., Toft D.O. GCUNC45 is the first Hsp90 co-chaperone to show alpha/beta isoform specificity. J. Biol. Chem. 2008, 283:9509-9512.
31. Zurawska A., Urbanski J., Matuliene J., Baraniak J., Klejman M.P., Filipek S., Matulis D., Bieganowski P. Mutations that increase both Hsp90 ATPase activity in vitro and Hsp90 drug resistance in vivo. Biochim. Biophys. Acta 2010, 1803:575-583.
32. Ho S.N., Hunt H.D., Horton R.M., Pullen J.K., Pease L.R. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 1989, 77:51-59.
33. Li M.Z., Elledge S.J. Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC. Nat. Methods 2007, 4:251-256.
34. Boeke J.D., Trueheart J., Natsoulis G., Fink G.R. 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol. 1987, 154:164-175.
35. Scroggins B.T., Robzyk K., Wang D., Marcu M.G., Tsutsumi S., Beebe K., Cotter R.J., Felts S., Toft D., Karnitz L., Rosen N., Neckers L. An acetylation site in the middle domain of Hsp90 regulates chaperone function. Mol. Cell 2007, 25:151-159.
36. Kobayakawa T., Yamada S., Mizuno A., Nemoto T.K. Substitution of only two residues of human Hsp90alpha causes impeded dimerization of Hsp90beta. Cell Stress Chaperones 2008, 13:97-104.
37. Richter K., Reinstein J., Buchner J. N-terminal residues regulate the catalytic efficiency of the Hsp90 ATPase cycle. J. Biol. Chem. 2002, 277:44905-44910.
38. Millson S.H., Prodromou C., Piper P.W. A simple yeast-based system for analyzing inhibitor resistance in the human cancer drug targets Hsp90alpha/beta. Biochem. Pharmacol. 2010, 79:1581-1588.
39. Meyer P., Prodromou C., Liao C., Hu B., Mark Roe S., Vaughan C.K., Vlasic I., Panaretou B., Piper P.W., Pearl L.H. Structural basis for recruitment of the ATPase activator Aha1 to the Hsp90 chaperone machinery. EMBO J. 2004, 23:511-519.
40. Nathan D.F., Vos M.H., Lindquist S. Identification of SSF1, CNS1, and HCH1 as multicopy suppressors of a Saccharomyces cerevisiae Hsp90 loss-of-function mutation. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:1409-1414.
41. Lotz G.P., Lin H., Harst A., Obermann W.M. Aha1 binds to the middle domain of Hsp90, contributes to client protein activation, and stimulates the ATPase activity of the molecular chaperone. J. Biol. Chem. 2003, 278:17228-17235.
42. Richter K., Soroka J., Skalniak L., Leskovar A., Hessling M., Reinstein J., Buchner J. Conserved conformational changes in the ATPase cycle of human Hsp90. J. Biol. Chem. 2008, 283:17757-17765.
43. Mollapour M., Neckers L. Post-translational modifications of Hsp90 and their contributions to chaperone regulation. Biochim. Biophys. Acta 2012, 1823:648-655.
44. Mollapour M., Tsutsumi S., Donnelly A.C., Beebe K., Tokita M.J., Lee M.J., Lee S., Morra G., Bourboulia D., Scroggins B.T., Colombo G., Blagg B.S., Panaretou B., Stetler-Stevenson W.G., Trepel J.B., Piper P.W., Prodromou C., Pearl L.H., Neckers L. Swe1Wee1-dependent tyrosine phosphorylation of Hsp90 regulates distinct facets of chaperone function. Mol. Cell 2010, 37:333-343.
45. Mollapour M., Bourboulia D., Beebe K., Woodford M.R., Polier S., Hoang A., Chelluri R., Li Y., Guo A., Lee M.J., Fotooh-Abadi E., Khan S., Prince T., Miyajima N., Yoshida S., Tsutsumi S., Xu W., Panaretou B., Stetler-Stevenson W.G., Bratslavsky G., Trepel J.B., Prodromou C., Neckers L. Asymmetric Hsp90 N domain SUMOylation recruits Aha1 and ATP-competitive inhibitors. Mol. Cell 2014, 53:317-329.
46. Solier S., Kohn K.W., Scroggins B., Xu W., Trepel J., Neckers L., Pommier Y. Heat shock protein 90alpha (HSP90alpha), a substrate and chaperone of DNA-PK necessary for the apoptotic response. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:12866-12872.
47. Lees-Miller S.P., Anderson C.W. The human double-stranded DNA-activated protein kinase phosphorylates the 90-kDa heat-shock protein, hsp90 alpha at two NH2-terminal threonine residues. J. Biol. Chem. 1989, 264:17275-17280.
48. Chen B., Zhong D., Monteiro A. Comparative genomics and evolution of the HSP90 family of genes across all kingdoms of organisms. BMC Genomics 2006, 7:156.
49. Panaretou B., Siligardi G., Meyer P., Maloney A., Sullivan J.K., Singh S., Millson S.H., Clarke P.A., Naaby-Hansen S., Stein R., Cramer R., Mollapour M., Workman P., Piper P.W., Pearl L.H., Prodromou C. Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1. Mol. Cell 2002, 10:1307-1318.
50. Retzlaff M., Hagn F., Mitschke L., Hessling M., Gugel F., Kessler H., Richter K., Buchner J. Asymmetric activation of the hsp90 dimer by its cochaperone aha1. Mol. Cell 2010, 37:344-354.
51. Okayama S., Kopelovich L., Balmus G., Weiss R.S., Herbert B.S., Dannenberg A.J., Subbaramaiah K. p53 protein regulates Hsp90 ATPase activity and thereby Wnt signaling by modulating Aha1 expression. J. Biol. Chem. 2014, 289:6513-6525.
52. Ratzke C., Mickler M., Hellenkamp B., Buchner J., Hugel T. Dynamics of heat shock protein 90 C-terminal dimerization is an important part of its conformational cycle. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:16101-16106.
53. Zurawska A., Urbanski J., Bieganowski P. Hsp90n-an accidental product of a fortuitous chromosomal translocation rather than a regular Hsp90 family member of human proteome. Biochim. Biophys. Acta 2008, 1784:1844-1846.
54. Roe S.M., Ali M.M., Meyer P., Vaughan C.K., Panaretou B., Piper P.W., Prodromou C., Pearl L.H. The Mechanism of Hsp90 regulation by the protein kinase-specific cochaperone p50(cdc37). Cell 2004, 116:87-98.
55. Ghaemmaghami S., Huh W.K., Bower K., Howson R.W., Belle A., Dephoure N., O'Shea E.K., Weissman J.S. Global analysis of protein expression in yeast. Nature 2003, 425:737-741.
56. Armstrong H., Wolmarans A., Mercier R., Mai B., LaPointe P. The co-chaperone Hch1 regulates Hsp90 function differently than its homologue Aha1 and confers sensitivity to yeast to the Hsp90 inhibitor NVP-AUY922. PLoS One 2012, 7:e49322.
57. Hawle P., Siepmann M., Harst A., Siderius M., Reusch H.P., Obermann W.M. The middle domain of Hsp90 acts as a discriminator between different types of client proteins. Mol. Cell. Biol. 2006, 26:8385-8395.
58. Vaughan C.K., Gohlke U., Sobott F., Good V.M., Ali M.M., Prodromou C., Robinson C.V., Saibil H.R., Pearl L.H. Structure of an Hsp90-Cdc37-Cdk4 complex. Mol. Cell 2006, 23:697-707.