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AMPK-HDAC5 pathway facilitates nuclear accumulation of HIF-1α and functional activation of HIF-1 by deacetylating Hsp70 in the cytosol

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Pages 2520-2536 | Received 24 Apr 2015, Accepted 15 May 2015, Published online: 17 Jul 2015

References

  • Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003; 3:721-32; PMID:13130303; http://dx.doi.org/10.1038/nrc1187
  • Semenza GL. Hypoxia-inducible factors in physiology and medicine. Cell 2012; 148:399-408; PMID:22304911; http://dx.doi.org/10.1016/j.cell.2012.01.021
  • Kaelin WG Jr, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 2008; 30:393-402; PMID:18498744; http://dx.doi.org/10.1016/j.molcel.2008.04.009
  • Semenza GL. Hypoxia-inducible factor 1 and cardiovascular disease. Ann Rev Physiol 2014; 76:39-56; PMID:23988176; http://dx.doi.org/10.1146/annurev-physiol-021113-170322
  • Takubo K, Goda N, Yamada W, Iriuchishima H, Ikeda E, Kubota Y, Shima H, Johnson RS, Hirao A, Suematsu M, et al. Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 2010; 7:391-402; PMID:20804974; http://dx.doi.org/10.1016/j.stem.2010.06.020
  • Doedens AL, Phan AT, Stradner MH, Fujimoto JK, Nguyen JV, Yang E, Johnson RS, Goldrath AW. Hypoxia-inducible factors enhance the effector responses of CD8(+) T cells to persistent antigen. Nat Immunol 2013; 14:1173-82; PMID:24076634; http://dx.doi.org/10.1038/ni.2714
  • Keith B, Simon MC. Hypoxia-inducible factors, stem cells, and cancer. Cell 2007; 129:465-72; PMID:17482542; http://dx.doi.org/10.1016/j.cell.2007.04.019
  • Zhang Z, Yan J, Chang Y, ShiDu Yan S, Shi H. Hypoxia inducible factor-1 as a target for neurodegenerative diseases. Cur Med Chem 2011; 18:4335-43; PMID:21861815; http://dx.doi.org/10.2174/092986711797200426
  • Hardie DG, Ross FA, Hawley SA. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 2012; 13:251-62; PMID:22436748; http://dx.doi.org/10.1038/nrm3311
  • Mihaylova MM, Shaw RJ. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol 2011; 13:1016-23; PMID:21892142; http://dx.doi.org/10.1038/ncb2329
  • Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 2011; 13:132-41; PMID:21258367; http://dx.doi.org/10.1038/ncb2152
  • Mungai PT, Waypa GB, Jairaman A, Prakriya M, Dokic D, Ball MK, Schumacker PT. Hypoxia triggers AMPK activation through reactive oxygen species-mediated activation of calcium release-activated calcium channels. Mol Cell Biol 2011; 31:3531-45; PMID:21670147; http://dx.doi.org/10.1128/MCB.05124-11
  • Laderoute KR, Amin K, Calaoagan JM, Knapp M, Le T, Orduna J, Foretz M, Viollet B. 5′-AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments. Mol Cell Biol 2006; 26:5336-47; PMID:16809770; http://dx.doi.org/10.1128/MCB.00166-06
  • Jibb LA, Richards JG. AMP-activated protein kinase activity during metabolic rate depression in the hypoxic goldfish, Carassius auratus. J Exp Biol 2008; 211:3111-22; PMID:18805810; http://dx.doi.org/10.1242/jeb.019117
  • Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. P Natl Acad Sci USA 1995; 92:5510-4; PMID:7539918; http://dx.doi.org/10.1073/pnas.92.12.5510
  • Kaelin WG Jr. The von Hippel-Lindau protein, HIF hydroxylation, and oxygen sensing. Biochem Biophys Res Commun 2005; 338:627-38; PMID:16153592; http://dx.doi.org/10.1016/j.bbrc.2005.08.165
  • Lando D, Gorman JJ, Whitelaw ML, Peet DJ. Oxygen-dependent regulation of hypoxia-inducible factors by prolyl and asparaginyl hydroxylation. Eur J Biochem 2003; 270:781-90; PMID:12603311; http://dx.doi.org/10.1046/j.1432-1033.2003.03445.x
  • Semenza GL. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiol (Bethesda) 2004; 19:176-82; PMID:15304631; http://dx.doi.org/10.1152/physiol.00001.2004
  • Yu F, White SB, Zhao Q, Lee FS. HIF-1alpha binding to VHL is regulated by stimulus-sensitive proline hydroxylation. P Natl Acad Sci USA 2001; 98:9630-5; PMID:11504942; http://dx.doi.org/10.1073/pnas.181341498
  • Epstein ACR, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, Mole DR, Mukherji M, Metzen E, Wilson MI, Dhanda A, et al. C-elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001; 107:43-54; PMID:11595184; http://dx.doi.org/10.1016/S0092-8674(01)00507-4
  • Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, Salic A, Asara JM, Lane WS, Kaelin WG Jr. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 2001; 292:464-8; PMID:11292862; http://dx.doi.org/10.1126/science.1059817
  • Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, Gaskell SJ, Kriegsheim A, Hebestreit HF, Mukherji M, Schofield CJ, et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001; 292:468-72; PMID:11292861; http://dx.doi.org/10.1126/science.1059796
  • Koh MY, Spivak-Kroizman TR, Powis G. HIF-1 regulation: not so easy come, easy go. Trends Biochem Sci 2008; 33:526-34; PMID:18809331; http://dx.doi.org/10.1016/j.tibs.2008.08.002
  • Huang LE, Gu J, Schau M, Bunn HF. Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. P Natl Acad Sci U S A 1998; 95:7987-92; PMID:NOT_FOUND; http://dx.doi.org/10.1073/pnas.95.14.7987
  • Salceda S, Caro J. Hypoxia-inducible factor 1alpha (HIF-1alpha) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J Biol Chem 1997; 272:22642-7; PMID:9278421; http://dx.doi.org/10.1074/jbc.272.36.22642
  • Mahon PC, Hirota K, Semenza GL. FIH-1: a novel protein that interacts with HIF-1alpha and VHL to mediate repression of HIF-1 transcriptional activity. Genes Dev 2001; 15:2675-86; PMID:11641274; http://dx.doi.org/10.1101/gad.924501
  • Lando D, Peet DJ, Whelan DA, Gorman JJ, Whitelaw ML. Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science 2002; 295:858-61; PMID:11823643; http://dx.doi.org/10.1126/science.1068592
  • Sang N, Fang J, Srinivas V, Leshchinsky I, Caro J. Carboxyl-terminal transactivation activity of hypoxia-inducible factor 1 alpha is governed by a von Hippel-Lindau protein-independent, hydroxylation-regulated association with p300/CBP. Mol Cell Biol 2002; 22:2984-92; PMID:11940656; http://dx.doi.org/10.1128/MCB.22.9.2984-2992.2002
  • Fath DM, Kong X, Liang D, Lin Z, Chou A, Jiang Y, Fang J, Caro J, Sang N. Histone deacetylase inhibitors repress the transactivation potential of hypoxia-inducible factors independently of direct acetylation of HIF-alpha. J Biol Chem 2006; 281:13612-9; PMID:16543236; http://dx.doi.org/10.1074/jbc.M600456200
  • Qian DZ, Kachhap SK, Collis SJ, Verheul HM, Carducci MA, Atadja P, Pili R. Class II histone deacetylases are associated with VHL-independent regulation of hypoxia-inducible factor 1 alpha. Cancer Res 2006; 66:8814-21; PMID:16951198; http://dx.doi.org/10.1158/0008-5472.CAN-05-4598
  • Liang D, Kong X, Sang N. Effects of histone deacetylase inhibitors on HIF-1. Cell Cycle 2006; 5:2430-5; PMID:17102633; http://dx.doi.org/10.4161/cc.5.21.3409
  • Isaacs JS JY, Mimnaugh EG, Martinez A, Cuttitta F, Neckers LM. Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1 alpha-degradative pathway. J Biol Chem 2002; 277:29936-44; PMID:12052835; http://dx.doi.org/10.1074/jbc.M204733200
  • Minet E, Mottet D, Michel G, Roland I, Raes M, Remacle J, Michiels C. Hypoxia-induced activation of HIF-1: role of HIF-1alpha-Hsp90 interaction. FEBS Lett 1999; 460:251-6; PMID:10544245; http://dx.doi.org/10.1016/S0014-5793(99)01359-9
  • Taipale M, Jarosz DF, Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 2010; 11:515-28; PMID:20531426; http://dx.doi.org/10.1038/nrm2918
  • Chen S, Sang N. Histone deacetylase inhibitors: the epigenetic therapeutics that repress hypoxia-inducible factors. J Biomed Biotech 2011; 2011:197946
  • Yang XJ, Seto E. HATs and HDACs: from structure, function and regulation to novel strategies for therapy and prevention. Oncogene 2007; 26:5310-8; PMID:17694074; http://dx.doi.org/10.1038/sj.onc.1210599
  • Fischle W, Dequiedt F, Hendzel MJ, Guenther MG, Lazar MA, Voelter W, Verdin E. Enzymatic activity associated with class II HDACs is dependent on a multiprotein complex containing HDAC3 and SMRT/N-CoR. Mol Cell 2002; 9:45-57; PMID:11804585; http://dx.doi.org/10.1016/S1097-2765(01)00429-4
  • Yang XJ, Seto E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol 2008; 9:206-18; PMID:18292778; http://dx.doi.org/10.1038/nrm2346
  • Yang XJ, Gregoire S. Class II histone deacetylases: from sequence to function, regulation, and clinical implication. Mol Cell Biol 2005; 25:2873-84; PMID:15798178; http://dx.doi.org/10.1128/MCB.25.8.2873-2884.2005
  • McKinsey TA, Zhang CL, Olson EN. Identification of a signal-responsive nuclear export sequence in class II histone deacetylases. Mol Cell Biol 2001; 21:6312-21; PMID:11509672; http://dx.doi.org/10.1128/MCB.21.18.6312-6321.2001
  • Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, Nixon A, Yoshida M, Wang XF, Yao TP. HDAC6 is a microtubule-associated deacetylase. Nature 2002; 417:455-8; PMID:12024216; http://dx.doi.org/10.1038/417455a
  • Kovacs JJ, Murphy PJ, Gaillard S, Zhao X, Wu JT, Nicchitta CV, Yoshida M, Toft DO, Pratt WB, Yao TP. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol Cell 2005; 18:601-7; PMID:15916966; http://dx.doi.org/10.1016/j.molcel.2005.04.021
  • Marek L, Hamacher A, Hansen FK, Kuna K, Gohlke H, Kassack MU, Kurz T. Histone deacetylase (HDAC) inhibitors with a novel connecting unit linker region reveal a selectivity profile for HDAC4 and HDAC5 with improved activity against chemoresistant cancer cells. J Med Chem 2013; 56:427-36; PMID:23252603; http://dx.doi.org/10.1021/jm301254q
  • Lao T, Chen S, Sang N. Two mutations impair the stability and function of ubiquitin-activating enzyme (E1). J Cell Physiol 2012; 227:1561-8; PMID:21678405; http://dx.doi.org/10.1002/jcp.22870
  • Lahm A, Paolini C, Pallaoro M, Nardi MC, Jones P, Neddermann P, Sambucini S, Bottomley MJ, Lo Surdo P, Carfi A, et al. Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases. P Natl Acad Sci USA 2007; 104:17335-40; PMID:17956988; http://dx.doi.org/10.1073/pnas.0706487104
  • Bottomley MJ, Lo Surdo P, Di Giovine P, Cirillo A, Scarpelli R, Ferrigno F, Jones P, Neddermann P, De Francesco R, Steinkuhler C, et al. Structural and functional analysis of the human HDAC4 catalytic domain reveals a regulatory structural zinc-binding domain. J Biol Chem 2008; 283:26694-704; PMID:18614528; http://dx.doi.org/10.1074/jbc.M803514200
  • Greco TM, Yu F, Guise AJ, Cristea IM. Nuclear import of histone deacetylase 5 by requisite nuclear localization signal phosphorylation. Mol Cell Proteomics 2011; 10:M110 004317; PMID:21081666; http://dx.doi.org/10.1074/mcp.M110.004317
  • Jeong JW, Bae MK, Ahn MY, Kim SH, Sohn TK, Bae MH, Yoo MA, Song EJ, Lee KJ, Kim KW. Regulation and destabilization of HIF-1alpha by ARD1-mediated acetylation. Cell 2002; 111:709-20; PMID:12464182; http://dx.doi.org/10.1016/S0092-8674(02)01085-1
  • Yang Y, Fiskus W, Yong B, Atadja P, Takahashi Y, Pandita TK, Wang HG, Bhalla KN. Acetylated hsp70 and KAP1-mediated Vps34 SUMOylation is required for autophagosome creation in autophagy. P Natl Acad Sci USA 2013; 110:6841-6; PMID:23569248; http://dx.doi.org/10.1073/pnas.1217692110
  • Wang Y, Wang SY, Zhang XH, Zhao M, Hou CM, Xu YJ, Du ZY, Yu XD. FK228 inhibits Hsp90 chaperone function in K562 cells via hyperacetylation of Hsp70. Biochem Biophys Res Commun 2007; 356:998-1003; PMID:17397803; http://dx.doi.org/10.1016/j.bbrc.2007.03.076
  • To KK, Robey R, Zhan Z, Bangiolo L, Bates SE. Upregulation of ABCG2 by romidepsin via the aryl hydrocarbon receptor pathway. Mol Cancer Res 2011; 9:516-27; PMID:21357443; http://dx.doi.org/10.1158/1541-7786.MCR-10-0270
  • Towler MC, Hardie DG. AMP-activated protein kinase in metabolic control and insulin signaling. Cir Res 2007; 100:328-41; PMID:17307971; http://dx.doi.org/10.1161/01.RES.0000256090.42690.05
  • McGee SL, van Denderen BJ, Howlett KF, Mollica J, Schertzer JD, Kemp BE, Hargreaves M. AMP-activated protein kinase regulates GLUT4 transcription by phosphorylating histone deacetylase 5. Diabetes 2008; 57:860-7; PMID:18184930; http://dx.doi.org/10.2337/db07-0843
  • Chang SR, McKinsey TA, Zhang CL, Richardson JA, Hill JA, Olson EN. Histone deacetylases 5 and 9 govern responsiveness of the heart to a subset of stress signals and play redundant roles in heart development. Mol Cell Biol 2004; 24:8467-76; PMID:15367668; http://dx.doi.org/10.1128/MCB.24.19.8467-8476.2004
  • Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, et al. Multiplex genome engineering using CRISPR/Cas systems. Science 2013; 339:819-23; PMID:23287718; http://dx.doi.org/10.1126/science.1231143
  • Shi P, Scott MA, Ghosh B, Wan D, Wissner-Gross Z, Mazitschek R, Haggarty SJ, Yanik MF. Synapse microarray identification of small molecules that enhance synaptogenesis. Nat Comm 2011; 2:510; PMID:22027590; http://dx.doi.org/10.1038/ncomms1518
  • McGee SL, Sparling D, Olson AL, Hargreaves M. Exercise increases MEF2- and GEF DNA-binding activity in human skeletal muscle. FASEB J 2006; 20:348-9; PMID:16368714
  • Zhao JX, Yue WF, Zhu MJ, Du M. AMP-activated protein kinase regulates beta-catenin transcription via histone deacetylase 5. J Biol Chem 2011; 286:16426-34; PMID:21454484; http://dx.doi.org/10.1074/jbc.M110.199372
  • McKinsey TA, Zhang CL, Olson EN. Activation of the myocyte enhancer factor-2 transcription factor by calcium/calmodulin-dependent protein kinase-stimulated binding of 14-3-3 to histone deacetylase 5. P Natl Acad Sci USA 2000; 97:14400-5; PMID:11114197; http://dx.doi.org/10.1073/pnas.260501497
  • Cho Y, Cavalli V. HDAC5 is a novel injury-regulated tubulin deacetylase controlling axon regeneration. EMBO J 2012; 31:3063-78; PMID:22692128; http://dx.doi.org/10.1038/emboj.2012.160
  • McGee SL, Hargreaves M. Histone modifications and skeletal muscle metabolic gene expression. Clin Exp Pharm Physiol 2010; 37:392-6; PMID:19793100; http://dx.doi.org/10.1111/j.1440-1681.2009.05311.x
  • Shackelford DB, Shaw RJ. The LKB1-AMPK pathway: metabolism and growth control in tumour suppression. Nat Rev Cancer 2009; 9:563-75; PMID:19629071; http://dx.doi.org/10.1038/nrc2676
  • Arnesen T, Kong X, Evjenth R, Gromyko D, Varhaug JE, Lin Z, Sang N, Caro J, Lillehaug JR. Interaction between HIF-1α (ODD) and hARD1 does not induce acetylation and destabilization of HIF-1α. FEBS Lett 2005; 579:6428-32; PMID:16288748; http://dx.doi.org/10.1016/j.febslet.2005.10.036
  • Bilton R, Mazure N, Trottier E, Hattab M, Déry M-A, Richard DE, Pouysségur J, Brahimi-Horn MC. Arrest-defective-1 protein, an acetyltransferase, does not alter stability of hypoxia-inducible factor (HIF)-1α and is not induced by hypoxia or HIF. J Biol Chem 2005; 280:31132-40; PMID:15994306; http://dx.doi.org/10.1074/jbc.M504482200
  • Kong X, Lin Z, Liang D, Fath D, Sang N, Caro J. Histone deacetylase inhibitors induce VHL and ubiquitin-independent proteasomal degradation of hypoxia-inducible factor 1alpha. Mol Cell Biol 2006; 26:2019-28; PMID:16507982; http://dx.doi.org/10.1128/MCB.26.6.2019-2028.2006
  • Yoo YG, Kong, G, Lee M-O. Metastasis-associated protein 1 enhances stability of hypoxia-inducible factor-1a protein by recruiting histone deacetylase 1. EMBO J 2006; 25:1231-41; PMID:16511565; http://dx.doi.org/10.1038/sj.emboj.7601025
  • Geng H, Harvey CT, Pittsenbarger J, Liu Q, Beer TM, Xue C, Qian DZ. HDAC4 protein regulates HIF1alpha protein lysine acetylation and cancer cell response to hypoxia. J Biol Chem 2011; 286:38095-102; PMID:21917920; http://dx.doi.org/10.1074/jbc.M111.257055
  • Xue W, Cai L, Tan Y, Thistlethwaite P, Kang YJ, Li X, Feng W. Cardiac-specific overexpression of HIF-1{alpha} prevents deterioration of glycolytic pathway and cardiac remodeling in streptozotocin-induced diabetic mice. Am J Pathol 2010; 177:97-105; PMID:20566749; http://dx.doi.org/10.2353/ajpath.2010.091091
  • Cai L, Sutter BM, Li B, Tu BP. Acetyl-CoA induces cell growth and proliferation by promoting the acetylation of histones at growth genes. Mol Cell 2011; 42:426-37; PMID:21596309; http://dx.doi.org/10.1016/j.molcel.2011.05.004
  • Jiang W, Wang S, Xiao M, Lin Y, Zhou L, Lei Q, Xiong Y, Guan KL, Zhao S. Acetylation regulates gluconeogenesis by promoting PEPCK1 degradation via recruiting the UBR5 ubiquitin ligase. Mol Cell 2011; 43:33-44; PMID:21726808; http://dx.doi.org/10.1016/j.molcel.2011.04.028
  • Lv L, Li D, Zhao D, Lin R, Chu Y, Zhang H, Zha Z, Liu Y, Li Z, Xu Y, et al. Acetylation targets the M2 isoform of pyruvate kinase for degradation through chaperone-mediated autophagy and promotes tumor growth. Mol Cell 2011; 42:719-30; PMID:21700219; http://dx.doi.org/10.1016/j.molcel.2011.04.025
  • Wang Q, Zhang Y, Yang C, Xiong H, Lin Y, Yao J, Li H, Xie L, Zhao W, Yao Y, et al. Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science 2010; 327:1004-7; PMID:20167787; http://dx.doi.org/10.1126/science.1179687
  • Zhang T, Wang S, Lin Y, Xu W, Ye D, Xiong Y, Zhao S, Guan KL. Acetylation negatively regulates glycogen phosphorylase by recruiting protein phosphatase 1. Cell Metab 2012; 15:75-87; PMID:22225877; http://dx.doi.org/10.1016/j.cmet.2011.12.005
  • Zhao S, Xu W, Jiang W, Yu W, Lin Y, Zhang T, Yao J, Zhou L, Zeng Y, Li H, et al. Regulation of cellular metabolism by protein lysine acetylation. Science 2010; 327:1000-4; PMID:20167786; http://dx.doi.org/10.1126/science.1179689
  • Fischle W, Emiliani S, Hendzel MJ, Nagase T, Nomura N, Voelter W, Verdin E. A new family of human histone deacetylases related to Saccharomyces cerevisiae HDA1p. J Biol Chem 1999; 274:11713-20; PMID:10206986; http://dx.doi.org/10.1074/jbc.274.17.11713
  • Stiehl DP, Fath DM, Liang D, Jiang Y, Sang N. Histone deacetylase inhibitors synergize p300 autoacetylation that regulates its transactivation activity and complex formation. Cancer Res 2007; 67:2256-64; PMID:17332356