Specific regulation of noncanonical p38α activation by Hsp90-Cdc37 chaperone complex in cardiomyocyte

Circulation Research

Volumn 106, Issue 8, 2010, Pages 1404-1412

  Ota, Asuka ^a   Zhang, Jun ^a   Ping, Peipei ^a   Han, Jiahuai ^b   Wang, Yibin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b XIAMEN UNIVERSITY   (China)

Author keywords

Autophosphorylation; Cdc37; Hsp90; Noncanonical pathway; P38 mitogen activated protein kinase

Indexed keywords

CELL CYCLE PROTEIN 37; MITOGEN ACTIVATED PROTEIN KINASE 14; MITOGEN ACTIVATED PROTEIN KINASE KINASE 3; 17-(ALLYLAMINO)-17-DEMETHOXYGELDANAMYCIN; BENZOQUINONE DERIVATIVE; CDC37 PROTEIN, HUMAN; CDC37 PROTEIN, MOUSE; CELL CYCLE PROTEIN; CHAPERONE; CHAPERONIN; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; HSPCA PROTEIN, MOUSE; MACROCYCLIC LACTAM; MULTIPROTEIN COMPLEX; RECOMBINANT PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TANESPIMYCIN;

APOPTOSIS; ARTICLE; AUTOPHOSPHORYLATION; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CLINICAL ASSESSMENT; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; GENE CONTROL; HEART MUSCLE CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; ANIMAL; CELL STRAIN COS1; CELL SURVIVAL; CERCOPITHECUS; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; HELA CELL; HUMAN; METABOLISM; MOUSE; MUTATION; PHOSPHORYLATION; PROTEIN BINDING; RAT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME; TRANSGENIC MOUSE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; BENZOQUINONES; CELL CYCLE PROTEINS; CELL SURVIVAL; CERCOPITHECUS AETHIOPS; CHAPERONINS; COS CELLS; ENZYME ACTIVATION; HELA CELLS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC; MAP KINASE KINASE 3; MICE; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE 14; MOLECULAR CHAPERONES; MULTIPROTEIN COMPLEXES; MUTATION; MYOCYTES, CARDIAC; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN BINDING; RATS; RECOMBINANT PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

EID: 77952480068     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.109.213769     Document Type: Article

References (59)

1. Bogoyevitch MA. Signalling via stress-activated mitogen-activated protein kinases in the cardiovascular system. Cardiovasc Res. 2000;45:826-842.
2. New L, Han J. The p38 MAP kinase pathway and its biological function. Trends Cardiovasc Med. 1998;8:220-228.
3. Obata T, Brown GE, Yaffe MB. Map kinase pathways activated by stress: The p38 MAPK pathway. Crit Care Med. 2000;28: N67-77.
4. Widmann C, Gibson S, Jarpe MB, Johnson GL. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev. 1999;79:143-180.
5. Raman M, Chen W, Cobb MH. Differential regulation and properties of MAPKs. Oncogene. 2007;26:3100-3112.
6. Ichijo H, Nishida E, Irie K, ten Dijke P, Saitoh M, Moriguchi T, Takagi M, Matsumoto K, Miyazono K, Gotoh Y. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science. 1997;275:90-94.
7. Ono K, Han J. The p38 signal transduction pathway: activation and function. Cell Signal. 2000;12:1-13.
8. Avitzour M, Diskin R, Raboy B, Askari N, Engelberg D, Livnah O. Intrinsically active variants of all human p38 isoforms. FEBS J. 2007;274:963-975.
9. Levin-Salomon V, Maayan I, Avrahami-Moyal L, Marbach I, Livnah O, Engelberg D. When expressed in yeast, mammalian mitogen-activated protein kinases lose proper regulation and become spontaneously phosphorylated. Biochem J. 2009;417:331-340.
10. Nguyen AN, Shiozaki K. Heat-shock-induced activation of stress map kinase is regulated by threonine-and tyrosine-specific phosphatases. Genes Dev. 1999;13:1653-1663.
11. Takekawa M, Maeda T, Saito H. Protein phosphatase 2calpha inhibits the human stress-responsive p38 and JNK MAPK pathways. EMBO J. 1998;17:4744-4752.
12. Meskiene I, Baudouin E, Schweighofer A, Liwosz A, Jonak C, Rodriguez PL, Jelinek H, Hirt H. Stress-induced protein phosphatase 2c is a negative regulator of a mitogen-activated protein kinase. J Biol Chem. 2003;278:18945-18952.
13. Ge B, Gram H, Di Padova F, Huang B, New L, Ulevitch RJ, Luo Y, Han J. MAPKK-independent activation of p38alpha mediated by TAB1-dependent autophosphorylation of p38alpha. Science. 2002;295:1291-1294.
14. Tanno M, Bassi R, Gorog DA, Saurin AT, Jiang J, Heads RJ, Martin JL, Davis RJ, Flavell RA, Marber MS. Diverse mechanisms of myocardial p38 mitogen-activated protein kinase activation: evidence for MKK-independent activation by a TAB1-associated mechanism contributing to injury during myocardial ischemia. Circ Res. 2003;93:254-261.
15. Lu G, Kang YJ, Han J, Herschman HR, Stefani E, Wang Y. TAB-1 modulates intracellular localization of p38 MAP kinase and downstream signaling. J Biol Chem. 2006;281:6087-6095.
16. Salvador JM, Mittelstadt PR, Guszczynski T, Copeland TD, Yamaguchi H, Appella E, Fornace AJ Jr, Ashwell JD. Alternative p38 activation pathway mediated by t cell receptor-proximal tyrosine kinases. Nat Immunol. 2005;6:390-395.
17. Riggs DL, Cox MB, Cheung-Flynn J, Prapapanich V, Carrigan PE, Smith DF. Functional specificity of co-chaperone interactions with hsp90 client proteins. Crit Rev Biochem Mol Biol. 2004;39:279-295.
18. Sreedhar AS, Soti C, Csermely P. Inhibition of hsp90: a new strategy for inhibiting protein kinases. Biochim Biophys Acta. 2004;1697:233-242.
19. Prince T, Sun L, Matts RL. Cdk2: A genuine protein kinase client of hsp90 and cdc37. Biochemistry. 2005;44:15287-15295.
20. MacLean M, Picard D. Cdc37 goes beyond hsp90 and kinases. Cell Stress Chaperones. 2003;8:114-119.
21. Sato S, Fujita N, Tsuruo T. Modulation of akt kinase activity by binding to hsp90. Proc Natl Acad Sci U S A. 2000;97:10832-10837.
22. Pearl LH. Hsp90 and cdc37 - a chaperone cancer conspiracy. Curr Opin Genet Dev. 2005;15:55-61.
23. Terasawa K, Yoshimatsu K, Iemura S, Natsume T, Tanaka K, Minami Y. Cdc37 interacts with the glycine-rich loop of hsp90 client kinases. Mol Cell Biol. 2006;26:3378-3389.
24. Citri A, Harari D, Shohat G, Ramakrishnan P, Gan J, Lavi S, Eisenstein M, Kimchi A, Wallach D, Pietrokovski S, Yarden Y. Hsp90 recognizes a common surface on client kinases. J Biol Chem. 2006;281:14361-14369.
25. Zhang H, Wu W, Du Y, Santos SJ, Conrad SE, Watson JT, Grammatikakis N, Gallo KA. Hsp90/p50cdc37 is required for mixed-lineage kinase (MLK) 3 signaling. J Biol Chem. 2004;279:19457-19463.
26. Miyata Y, Ikawa Y, Shibuya M, Nishida E. Specific association of a set of molecular chaperones including hsp90 and cdc37 with MOK, a member of the mitogen-activated protein kinase superfamily. J Biol Chem. 2001;276:21841-21848.
27. Mackay K, Mochly-Rosen D. An inhibitor of p38 mitogen-activated protein kinase protects neonatal cardiac myocytes from ischemia. J Biol Chem. 1999;274:6272-6279.
28. Wang Y, Huang S, Sah VP, Ross J Jr, Brown JH, Han J, Chien KR. Cardiac muscle cell hypertrophy and apoptosis induced by distinct members of the p38 mitogen-activated protein kinase family. J Biol Chem. 1998;273:2161-2168.
29. Ren J, Zhang S, Kovacs A, Wang Y, Muslin AJ. Role of p38alpha MAPK in cardiac apoptosis and remodeling after myocardial infarction. J Mol Cell Cardiol. 2005;38:617-623.
30. Rajapandi T, Greene LE, Eisenberg E. The molecular chaperones hsp90 and hsc70 are both necessary and sufficient to activate hormone binding by glucocorticoid receptor. J Biol Chem. 2000;275:22597-22604.
31. Karnitz LM, Felts SJ Cdc37 regulation of the kinome: When to hold 'em and when to fold 'em. Sci STKE. 2007;2007: pe22.
32. Hemmer W, McGlone M, Tsigelny I, Taylor SS. Role of the glycine triad in the ATP-binding site of camp-dependent protein kinase. J Biol Chem. 1997;272:16946-16954.
33. Terasawa K, Minami Y. A client-binding site of cdc37. FEBS J. 2005;272:4684-4690.
34. Jiang Y, Li Z, Schwarz EM, Lin A, Guan K, Ulevitch RJ, Han J. Structure-function studies of p38 mitogen-activated protein kinase. Loop 12 influences substrate specificity and autophosphorylation, but not upstream kinase selection. J Biol Chem. 1997;272:11096-11102.
35. Diskin R, Lebendiker M, Engelberg D, Livnah O. Structures of p38alpha active mutants reveal conformational changes in l16 loop that induce autophosphorylation and activation. J Mol Biol. 2007;365:66-76.
36. Csermely P, Kajtar J, Hollosi M, Jalsovszky G, Holly S, Kahn CR, Gergely P Jr, Soti C, Mihaly K, Somogyi J. ATP induces a conformational change of the 90-kda heat shock protein (hsp90). J Biol Chem. 1993;268:1901-1907.
37. Prodromou C, Panaretou B, Chohan S, Siligardi G, O'Brien R, Ladbury JE, Roe SM, Piper PW, Pearl LH. The ATPase cycle of hsp90 drives a molecular 'clamp' via transient dimerization of the n-terminal domains. EMBO J. 2000;19:4383-4392.
38. Picard D. Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life Sci. 2002;59:1640-1648.
39. Nemoto T, Sato N. Oligomeric forms of the 90-kda heat shock protein. Biochem J. 1998;330(Pt 2):989-995.
40. Gray CC, Amrani M, Yacoub MH. Heat stress proteins and myocardial protection: experimental model or potential clinical tool? Int J Biochem Cell Biol. 1999;31:559-573.
41. Nishizawa J, Nakai A, Matsuda K, Komeda M, Ban T, Nagata K. Reactive oxygen species play an important role in the activation of heat shock factor 1 in ischemic-reperfused heart. Circulation. 1999;99:934-941.
42. Proctor CJ, Soti C, Boys RJ, Gillespie CS, Shanley DP, Wilkinson DJ, Kirkwood TB. Modelling the actions of chaperones and their role in ageing. Mech Ageing Dev. 2005;126:119-131.
43. Wandinger SK, Richter K, Buchner J. The hsp90 chaperone machinery. J Biol Chem. 2008;283:18473-18477.
44. Dezwaan DC, Freeman BC. Hsp90: the rosetta stone for cellular protein dynamics? Cell Cycle. 2008;7:1006-1012.
45. Dey A, Cederbaum AI. Geldanamycin, an inhibitor of hsp90 increases cytochrome p450 2e1 mediated toxicity in hepg2 cells through sustained activation of the p38mapk pathway. Arch Biochem Biophys. 2007;461:275-286.
46. Lochhead PA, Kinstrie R, Sibbet G, Rawjee T, Morrice N, Cleghon V. A chaperone-dependent gsk3beta transitional intermediate mediates activation-loop autophosphorylation. Mol Cell. 2006;24:627-633.
47. Tatebe H, Shiozaki K. Identification of cdc37 as a novel regulator of the stress-responsive mitogen-activated protein kinase. Mol Cell Biol. 2003;23:5132-5142.
48. Lee P, Rao J, Fliss A, Yang E, Garrett S, Caplan AJ. The cdc37 protein kinase-binding domain is sufficient for protein kinase activity and cell viability. J Cell Biol. 2002;159:1051-1059.
49. Garcia-Echeverria C, Sellers WR. Drug discovery approaches targeting the pi3k/akt pathway in cancer. Oncogene. 2008;27:5511-5526.
50. Messaoudi S, Peyrat JF, Brion JD, Alami M. Recent advances in hsp90 inhibitors as antitumor agents. Anticancer Agents Med Chem. 2008;8:761-782.
51. Li J, Miller EJ, Ninomiya-Tsuji J, Russell RR III, Young LH. AMP-activated protein kinase activates p38 mitogen-activated protein kinase by increasing recruitment of p38 MAPK to TAB1 in the ischemic heart. Circ Res. 2005;97:872-879.
52. Fiedler B, Feil R, Hofmann F, Willenbockel C, Drexler H, Smolenski A, Lohmann SM, Wollert KC. cGMP-dependent protein kinase type I inhibits TAB1-p38 mitogen-activated protein kinase apoptosis signaling in cardiac myocytes. J Biol Chem. 2006;281:32831-32840.
53. Gabrielson K, Bedja D, Pin S, Tsao A, Gama L, Yuan B, Muratore N. Heat shock protein 90 and erbb2 in the cardiac response to doxorubicin injury. Cancer Res. 2007;67:1436-1441.
54. Kupatt C, Dessy C, Hinkel R, Raake P, Daneau G, Bouzin C, Boekstegers P, Feron O. Heat shock protein 90 transfection reduces ischemiareperfusion-induced myocardial dysfunction via reciprocal endothelial no synthase serine 1177 phosphorylation and threonine 495 dephosphorylation. Arterioscler Thromb Vasc Biol. 2004;24:1435-1441.
55. Richter K, Hendershot LM, Freeman BC. The cellular world according to hsp90. Nat Struct Mol Biol. 2007;14:90-94.
56. Engel FB. Cardiomyocyte proliferation: a platform for mammalian cardiac repair. Cell Cycle. 2005;4:1360-1363.
57. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. Opposing effects of ERK and JNK-p38 map kinases on apoptosis. Science. 1995;270:1326-1331.
58. Liao P, Wang SQ, Wang S, Zheng M, Zhang SJ, Cheng H, Wang Y, Xiao RP. p38 mitogen-activated protein kinase mediates a negative inotropic effect in cardiac myocytes. Circ Res. 2002;90:190-196.
59. Vahebi S, Ota A, Li M, Warren CM, de Tombe PP, Wang Y, Solaro RJ. p38-MAPK induced dephosphorylation of alpha-tropomyosin is associated with depression of myocardial sarcomeric tension and ATPase activity. Circ Res. 2007;100:408-415.