Cover Image

Protein Acetylation as an Integral Part of Metabolism in Cancer Development and Progression

Miroslava Cuperlovic-Culf, Adrian Culf

Abstract


Acetylation of lysine is one of the major post-translational modifications of histone and non-histone proteins of eukaryotic cells. Acetylation has been indicated as an avenue for cellular response to environmental, nutritional and behavioral factors. At the same time, aberrant protein acetylation has been related to cancer as well as many other diseases. Abnormal expression of some classes of histone deacetylases and histone acetyl transferases has been documented for the majority of cancers. These observations have led to extensive efforts in the development of inhibitors for these enzymes for the treatment of cancer as well as other diseases as well as pathogen control.

Regulation of protein activities and gene expression by acetylation influences many processes relevant for cancer development, including metabolism. At the same time acetylation depends on a number of metabolic co-factors and a variety of metabolites act as inhibitors of acetylation proteins making acetylation enzymes an integral part of metabolism. Cancer metabolic phenotype is generally understood as one of the major hallmarks of cancer and thus the interplay between acetylation, anabolism and catabolism provides a very interesting forum for exploration of cancer development and for novel treatments. An ever increasing pool of publications shows relationships between the acetylation process and related enzymes with metabolites in cancerous and non-cancerous systems. In this review we are presenting previously established relationships between acetylation/deacetylation, metabolites and enzyme regulation particularly in relation to cancer development, progression and treatment.


Keywords


Epigenetics; metabolism; cancer; acetylation; deacetylation; metaboloepigenetics; Warburg effect

Full Text:

PDF

References


Sassone-Corsi P. When metabolism and epigenetics converge. Science. 2013, 339:148-150

Katada S, Imhof A, Sassone-Corsi P. Connecting threads: epigenetics and metabolism. Cell. 2012, 148: 24-28

Lu C, Thompson C B. Metabolic regulation of epigenetics. Cell metabolism. 2012, 16:9-17

Kaelin WG. McKnight SL. Influence of Metabolism on Epigenetics and Disease. Cell. 2013, 153: 56-69

Allfrey VG, Faulkner R, Mirsky AE. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci. 1964, 51: 786-794

Warburg, Uber den Stoffwechsel der Carcinomzelle. Klin Wochenschr Berl. 1925, 4:534-536

Barneda-Zahonero B, Parra M. Histone deacetylases and cancer. Molecular oncology. 2012, 6:579-89

Bannister AJ, Kouzarides T. Regulation of chromatin by histone modification. Cell Res. 2011, 21:381-395

Imai S, Armstrong CM, Kaeberlein M, Guarente L. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature. 2000, 403:795- 800

Landry J, Sutton A, Tafrov ST, Heller RC, Stebbins J, Pillus L, Sternglanz R. The silencing protein SIR2 and its homologs are NAD-dependent protein deacetylases. Proc Natl Acad Sci. 2000, 97:5807-5811

Haberland M, Montgomery RL, Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nature Rev Genetics. 2009, 10:32-42

Foglietti C, Filocamo G, Cundari E, De Rinaldis E, Lahm A, Cortese R, Steinkühler C. Dissecting the biological functions of histone deacetylases by RNA interference and transcriptional profiling. J Biol Chem. 2006, 281:17968-17976

Villagra A, Sotomayor EM, Seto E. Histone deacetylases and the immunological network: implications in cancer and inflammation. Oncogene. 2010, 29:157-173

Waterborg JH. Dynamics of histone acetylation in vivo. A function for acetylation turnover? Biochem Cell Biol. 2002, 80:363-378

Kouzarides T. Acetylation: a regulatory modification to rival phosphorylation? EMBO J. 2000, 19:1176-1179

Choudhary C, Mann M. Decoding signalling networks by mass spectrometry-based proteomics. Nat Rev Mol Cell Biol. 2010, 11: 427-439

Guan KL, Xiong Y. Regulation of intermediary metabolism by protein acetylation. Trends Biochem Sci. 2011, 36:108-116

Zhao SM, Xu W, Jiang WQ, Yu W, Lin Y, Zhang TF, Yao J, Zhou L, Zeng YX, Li H, Li YX, Shi J, An WL, Hancock SM, He FC, Qin LX, Chin J, Yang PY, Chen X, Lei QY, Xiong Y, Guan KL. Regulation of cellular metabolism by protein lysine acetylation. Science. 2010, 327:1000-1004

Thangaraju M, Gopal E, Martin PM, Ananth S, Smith SB, Prasad PD, Sterneck E, Ganapathy V. Slc5a8 triggers tumor cell apoptosis through pyruvate-dependent inhibition of histone deacetylases. Cancer Research. 2006, 66:11560-11564

Huang H, Liu N, Guo H, Liao S, Li X, Yang C, Liu S, Guan L, Li B, Xu L, Zhang C, Wang X, Dou QP, Liu J. L-Carnitine Is an Endogenous HDAC Inhibitor Selectively Inhibiting Cancer Cell Growth In Vivo and In Vitro. PloS one. 2012, 7:e49062

Nakahata Y, Sahar S, Astarita G, Kaluzova M, Sassone-Corsi P. Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science. 2009, 324:654-657

Phang JM, Liu W, Hancock C. Bridging epigenetics and metabolism. Epigenetics. 2013, 8:231-236

Wellen KE, Hatzivassiliou G, Sachdeva UM, Bui TV, Cross JR, Thompson CB. ATP-citrate lyase links cellular metabolism to histone acetylation. Science. 2009, 324: 1076-1080

Zaidi N, Swinnen JV, Smans K. ATP-citrate lyase: a key player in cancer metabolism. Cancer Res. 2012, 7:3709-3714

Donohoe D R, Collins LB, Wali A, Bigler R, Sun W, Bultman SJ. The Warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. Mol Cell. 2012, 48:612-626

McBrian MA, Behbahan IS, Ferrari R, Su T, Huang T-W, Li K, Hong CS, Christofk HR, Vogelauer M, Seligson DB, Kurdistani SK. Histone acetylation regulates intracellular ph. Molecular Cell. 2013, 49:310-321

Elsheikh SE, Green AR, Rakha EA, Powe DG, Ahmed RA, Collins HM, Soria D, Garibaldi JM, Paish CE, Ammar AA, Grainge MJ, Ball GR, Abdelghany MK, Martinez-Pomares L, Heery DM, Ellis IO. Global histone modifications in breast cancer correlate with tumor phenotypes, prognostic factors, and patient outcome. Cancer Research. 2009, 69:3802-3809

Manuyakorn A, Paulus R, Farrell J, Dawson NA, Tze S, Cheung-Lau G, Hines OJ, Reber H, Seligson DB, Horvath S, Kurdistani SK, Guha C, Dawson DW. Cellular histone modification patterns predict prognosis and treatment response in resectable pancreatic adenocarcinoma: Results from rtog 9704. Journal of Clinical Oncology. 2010, 28:1358-1365

Robey IF, Baggett BK, Kirkpatrick ND, Roe DJ, Dosescu J, Sloane BF, Hashim AI, Morse DL, Raghunand N, Gatenby RA, Gillies RJ. Bicarbonate increases tumor pH and inhibits spontaneous metastases. Cancer Research. 2009, 69:2260-2268

Cuperlovic-Culf M, Culf A, Touaibia M, Lefort N. Targeting the last hallmark of cancer: another attempt at a “magic bullet” drug targeting cancers’ metabolic phenotype. Future Oncology. 2012, 8:1315-1330

Gregoretti IV, Lee YM, Goodson HV. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. Journal of molecular biology. 2004, 338:17-31

Bernstein BE, Tong JK, Schreiber SL. Genome-wide studies of histone deacetylase function in yeast. Proc Natl Acad Sci. 2000, 97:13708-13713

Wang AH, Kruhlak MJ, Wu J, Bertos NR, Vezmar M, Posner BI, Bazett-Jones DP, Yang X-J. Regulation of histone deacetylase 4 by binding of 14-3-3 proteins. Molecular and Cellular Biology. 2000, 20:6904-6912

Grozinger CM, Schreiber SL. Regulation of histone deacetylase 4 and 5 and transcriptional activity by 14-3-3-dependent cellular localization. Proc Natl Acad Sci. 2000, 97: 7835-7840

Yuan H, Marmorstein R. Histone acetyltransferases: Rising ancient counterparts to protein kinases. Biopolymers. 2013, 99:98-111

Marmorstein R, Trievel RC. Histone modifying enzymes: Structures, mechanisms, and specificities. Biochimica et Biophysica Acta. 2009,1789:58-68

Wallace D, Fan W. Energetics, epigenetics, mitochondrial genetics. Mitochondrion. 2010, 10:12-31

Rokudai S, Laptenko O, Arnal SM, Taya Y, Kitabayashi I, Prives C. MOZ increases p53 acetylation and premature senescence through its complex formation with PML. Proc Natl Acad Sci. 2013, 110:3895-900

Love IM, Sekaric P, Shi D, Grossman SR, Androphy EJ. The histone acetyltransferase PCAF regulates p21 transcription through stress-induced acetylation of histone H3. Cell Cycle. 2012, 11:2458-2466

Spiegel S, Milstien S, Grant S. Endogenous modulators and pharmacological inhibitors of histone deacetylases in cancer therapy. Oncogene. 2012, 31:537-551

Lin Y-Y, Kiihl S, Suhail Y, Liu SY, Chou YH, Kuang Z, Lu JY, Khor CN, Lin CL, Bader JS, Irizarry R, Boeke JD. Functional dissection of lysine deacetylases reveals that HDAC1 and p300 regulate AMPK. Nature. 2012, 482: 251-255

Mihaylova MM, Shaw RJ. Metabolic reprogramming by class I and II histone deacetylases. Trends in endocrinology and metabolism: TEM. 2013, 24:48-57

Faubert B, Boily G, Izreig S, Griss T, Samborska B, Dong Z, Dupuy F, Chambers C, Fuerth BJ, Viollet B, Mamer OA, Avizonis D, DeBerardinis RJ, Siegel PM, Jones RG. Ampk is a negative regulator of the warburg effect and suppresses tumor growth in vivo. Cell Metabolism. 2013, 17:113-124

Geng H, Harvey CT, Pittsenbarger J, Liu Q, Beer TM, Xue C, Qian DZ. HDAC4 protein regulates HIF1α protein lysine acetylation and cancer cell response to hypoxia. J Biol Chem. 2011, 286:38095-102

Geng H, Liu Q, Xue C, David LL, Beer TM, Thomas GV, Dai MS, Qian DZ. HIF1α protein stability is increased by acetylation at lysine 709. J Biol Chem. 2012, 287:35496-34505

Marcu MG, Jung YJ, Lee S, Chung EJ, Lee MJ, Trepel J, Neckers L. Curcumin is an inhibitor of p300 histone acetylatransferase. Med Chem. 2006, 2:169-174

Lee SJ, Krauthauser C, Maduskuie V, Fawcett PT, Olson JM, Rajasekaran S.,Curcumin-induced HDAC inhibition and attenuation of medulloblastoma growth in vitro and in vivo. BMC Cancer. 2011, 11:144

Luo Y, Jian W, Stavreva D, Fu X, Hager G, Bungert J, Huang S, Qiu Y. Trans-regulation of histone deacetylase activities through acetylation. J Biol Chem. 2009, 284:34901-34910

Wagner JM, Hackanson B, Lübbert M, Jung M. Histone deacetylase (HDAC) inhibitors in recent clinical trials for cancer therapy. Clinical Epigenetics. 2010, 1: 117-136

Lahm A, Paolini C, Pallaoro M, Nardi MC, Jones P, Neddermann P, Sambucini S, Bottomley MJ, Lo Surdo P, Carfi A, Koch U, De Francesco R, Steinkuehler C, Gallinari P. Unraveling the hidden catalytic activity of vertebrate class ila histone deacetylases. Proc Natl Acad Sci. 2007, 104:17335-17340

Fischle W, Dequiedt F, Fillion M, Hendzel MJ, Voelter W, Verdin E. Human HDAC7 histone deacetylase activity is associated with HDAC3 in vivo. J Biol Chem. 2001, 276:35826-35835

Fischle W, Dequiedt F, Fillion M, Hendzel MJ, 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

Boyault C, Sadoul K, Pabion M, Khochbin S. HDAC6, at the crossroads between cytoskeleton and cell signaling by acetylation and ubiquitination. Oncogene. 2007, 26:5468-5476

Valenzuela-Fernandez A, Cabrero JR, Serrador JM, Sanchez-Madrid F. Hdac6: A key regulator of cytoskeleton, cell migration and cell-cell interactions. Trends in Cell Biology. 2008, 18:291-297

Kamemura K, Ogawa M, Ohkubo S, Y. Ohtsuka, Shitara Y, Komiya T, Maeda S, Ito A, Yoshida M. Depression of mitochondrial metabolism by downregulation of cytoplasmic deacetylase, HDAC6. FEBS Lett. 2012, 586 :, 1379-1383

Matsuyama A, Shimazu T, Sumida Y, Saito A, Yoshimatsu Y, Seigneurin-Berny D, Osada H, Komatsu Y, Nishino N, Khochbin S, Horinouchi S, Yoshida M. In vivo destabilization of dynamic microtubules by hdac6-mediated deacetylation. Embo Journal. 2002, 21:6820-6831

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, 417:455-458

Haggarty SJ, Koeller KM, Wong JC, Grozinger CM, Schreiber SL. Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc Natl Acad Sci. 2003, 100:4389- 4394.

Zhang X, Yuan Z, Zhang Y, Yong S, Salas-Burgos A, Koomen J, Olashaw N, Parsons JT, Yang X-J, Dent SR, Yao T-P, Lane WS, Seto E. Hdac6 modulates cell motility by altering the acetylation level of cortactin. Molecular Cell. 2007, 27:197-213

Li Y, Zhang X, Polakiewicz RD, Yao TP, Comb MJ. HDAC6 is required for epidermal growth factor-induced -catenin nuclear localization. J Biol Chem. 2008, 283:12686-12690

Parmigiani RB, Xu WS, Venta-Perez G, Erdjument-Bromage H, Yaneva M, Tempst P, Marks PA. HDAC6 is a specific deacetylase of peroxiredoxins and is involved in redox regulation. Proc Natl Acad Sci. 2008, 105:9633-9638

Subramanian C, Jarzembowski JA, Opipari AW, Jr., Castle VP, Kwok RPS. Hdac6 deacetylates ku70 and regulates ku70-bax binding in neuroblastoma. Neoplasia. 2011, 13:726-734

Winkler R, Benz V, Clemenz M, Bloch M, Foryst-Ludwig A, Wardat S, Witte N, Trappiel M, Namsolleck P, Mai K, Spranger J, Matthias G, Roloff T, Truee O, Kappert K, Schupp M, Matthias P, Kintscher U. Histone deacetylase 6 (hdac6) is an essential modifier of glucocorticoid-induced hepatic gluconeogenesis. Diabetes. 2012, 61:513-523

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, 417:455-458

Cabrero JR, Serrador JM, Barreiro O, Mittelbrunn M, Naranjo-Suarez S, Martin-Cofreces N, Vicente-Manzanares M, Mazitschek R, Bradner JE, Avila J, Valenzuela-Fernandez A, Sanchez-Madrid F. Lymphocyte chemotaxis is regulated by histone deacetylase 6, independently of its deacetylase activity. Molecular Biology of the Cell. 2006, 17:3435-3445

Fischer DD, Cai R, Bhatia U, Asselbergs FAM, Song CZ, Terry R, Trogani N, Widmer R, Atadja P, Cohen D. Isolation and characterization of a novel class ii histone deacetylase, hdac10. Journal of Biological Chemistry. 2002, 277:6656-6666

Matthias P, Yoshida M, Khochbin S. HDAC6 a new cellular stress surveillance factor. Cell Cycle. 2008, 7:7-10

Chalkiadaki A, Guarente L. Sirtuins mediate mammalian metabolic responses to nutrient availability. Nature Reviews Endocrinology. 2012, 8:287-296

Chiarugi A, Dolle C, Felici R, Ziegler M. The nad metabolome - a key determinant of cancer cell biology. Nature Reviews Cancer. 2012, 12:741-752

Huang J-Y, Hirschey MD, Shimazu T, Ho L, Verdin E. Mitochondrial sirtuins. Biochimica Et Biophysica Acta-Proteins and Proteomics. 2010, 1804:1645-1651

Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin YX, Tran H, Ross SE, Mostoslavsky R, Cohen HY, Hu LS, Cheng HL, Jedrychowski MP, Gygi SP, Sinclair DA, Alt FW, Greenberg ME. Stress-dependent regulation of foxo transcription factors by the sirt1 deacetylase. Science. 2004, 303:2011-2015

Luo J, Nikolaev AY, Imai S-i, Chen D, Su F, Shiloh A, Guarente L, Gu W. Negative control of p53 by sir2alpha promotes cell survival under stress. Cell. 2001, 107:137-148

Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR, Frye RA, Mayo MW. Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 2004, 23:2369-2380

North BJ, Marshall BL, Borra MT, Denu JM, Verdin E. The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol Cell. 2003, 11:437-444

Michishita E, McCord RA, Berber E, Kioi M, Padilla-Nash H, Damian M, Cheung P, Kusumoto R, Kawahara TL, Barrett JC, Chang HY, Bohr VA, Ried T, Gozani O, Chua KF. SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin, Nature. 2008, 452:492-496

Ford E, Voit R, Liszt G, Magin C, Grummt I, Guarente L. Mammalian Sir2 homolog SIRT7 is an activator of RNA polymerase I transcription. Genes Dev. 2006, 20:1075-1080

Nakahata Y, Sahar S, Astarita G, Kaluzova M, P. Sassone-Corsi. Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science. 2009, 324:654-657

Ramsey KM, Yoshino J, Brace CS, Abrassart D, Kobayashi Y, Marcheva B, Hong H-K, Chong JL, Buhr ED, Lee C, Takahashi JS, Imai S-i, Bass J. Circadian clock feedback cycle through nampt-mediated nad(+) biosynthesis. Science. 2009, 324:651-654

Imai S, Guarente L. Ten years of NAD-dependent SIR2 family deacetylases: implications for metabolic diseases. Trends Pharmacol Sci. 2010, 31:212

Sassone-Corsi P. Physiology. When metabolism and epigenetics converge. Science. 2013, 339:148-150.

Yang H, Yang T, Baur JA, Perez E, Matsui T, Carmona JJ, Lamming DW, Souza-Pinto NC, Bohr VA, Rosenzweig A, de Cabo R, Sauve AA, Sinclair DA. Nutrient-sensitive mitochondrial nad(+) levels dictate cell survival. Cell. 2007, 130:1095-1107

Nakagawa T, Lomb DJ, Haigis MC, Guarente L. SIRT5 Deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle. Cell. 2009, 137:560-570

Hsieh Y-L, Kuo H-Y, Chang C-C, Naik MT, Liao P-H, Ho C-C, Huang T-C, Jeng J-C, Hsu P-H, Tsai M-D, Huang T-H, Shih H-M. Ubc9 acetylation modulates distinct sumo target modification and hypoxia response. Embo Journal. 2013, 32:791-804

Kim H-S, Patel K, Muldoon-Jacobs K, Bisht KS, Aykin-Burns N, Pennington JD, van der Meer R, Nguyen P, Savage J, Owens KM, Vassilopoulos A, Ozden O, Park S-H, Singh KK, Abdulkadir SA, Spitz DR, Deng C-X, Gius D. Sirt3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress. Cancer Cell. 2010, 17:41-52

Sebastian C, Zwaans BMM, Silberman DM, Gymrek M, Goren A, Zhong L, Ram O, Truelove J, Guimaraes AR, Toiber D, Cosentino C, Greenson JK, MacDonald AI, McGlynn L, Maxwell F, Edwards J, Giacosa S, Guccione E, Weissleder R, Bernstein BE, Regev A, Shiels PG, Lombard DB, Mostoslavsky R. The histone deacetylase sirt6 is a tumor suppressor that controls cancer metabolism. Cell. 2012, 151:1185-1199

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, 42:426-437.

Michishita E, McCord RA, Boxer LD, Barber MF, Hong T, Gozani O, Chua KF. Cell cycle-dependent deacetylation of telomeric histone H3 lysine K56 by human SIRT6. Cell Cycle. 2009, 8:2664-2666

Bauer I, Grozio A, Lasiglie D, Basile G, Sturla L, Magnone M, Sociali G, Soncini D, Caffa I, Poggi A, Zoppoli G, Cea M, Feldmann G, Mostoslavsky R, Ballestrero A, Patrone F, Bruzzone S, Nencioni A. The nad(+)-dependent histone deacetylase sirt6 promotes cytokine production and migration in pancreatic cancer cells by regulating ca2+ responses. Journal of Biological Chemistry. 2012, 287:40924-40937

Kokkonen P, Rahnasto-Rilla M, Kiviranta PH, Huhtiniemi T, Laitinen T, Poso A, Jarho E, Lahtela-Kakkonen M. Peptides and Pseudopeptides as SIRT6 Deacetylation Inhibitors. ACS Medicinal Chemistry Letters. 2012, 3:969-974

Deubzer HE, Schier MC, Oehme I, Lodrini M, Haendler B, Sommer A, Witt O. HDAC11 is a novel drug target in carcinomas. Int J Cancer. 2013, 132:2200-8.

Soliman ML, Rosenberger T. Acetate supplementation increases brain histone acetylation and inhibits histone deacetylase activity and expression. Mol Cell Biochem. 2011, 352:173-80.

Vogelauer M, Krall AS, McBrian M, Li JY, Kurdistani SK. Stimulation of histone deacetylase activity by metabolites of intermediary metabolism. J Biol Chem. 2012, 287:32006-32016

Candido EP, Reeves R, Davie JR. Sodium butyrate inhibits histone deacetylation in cultured cells. Cell. 1978, 14:105-113

Shimazu T, Hirschey MD, Newman J, He W, Shirakawa K, Le Moan N, Grueter CA, Lim H, L.R. Saunders, R.D. Stevens, C.B. Newgard, Farese Jr RV, de Cabo R, Ulrich S, Akassoglou K, Verdin E. Suppression of oxidative stress by -hydroxybutyrate, an endogenous histone deacetylase inhibitor. Science. 2013, 339:211-214.

Thangaraju M, Gopal E, Martin PM, Ananth S, Smith SB, Prasad PD, Sterneck E, Ganapathy V. SLC5A8 triggers tumor cell apoptosis through pyruvate-dependent inhibition of histone deacetylases. Cancer Res. 2006, 66:11560-11564

Latham T, Mackay L, Sproul D, Karim M, Culley J, Harrison DJ, Hayward L, Langridge-Smith P, Gilbert N, Ramsahoye BH. Lactate, a product of glycolytic metabolism, inhibits histone deacetylase activity and promotes changes in gene expression. Nucleic Acids Res. 2012, 40:4794-4803

Nunes MJ, Moutinho M, Gama MJ, Rodrigues CM, Rodrigues E. Histone deacetylase inhibition decreases cholesterol levels in neuronal cells by modulating key genes in cholesterol synthesis, uptake and efflux. PloS One. 2013, 8: e53394

Villagra, N. Ulloa, X. Zhang, Z. Yuan, E. Sotomayor, E. Seto, Histone deacetylase 3 down-regulates cholesterol synthesis through repression of lanosterol synthase gene expression. J Biol Chem. 2007, 282:35457-35470

Hait NC, Allegood J, Maceyka M, Strub GM, Harikumar KB, Singh SK, Luo C, Marmorstein R, Kordula T, Milstien S, Spiegel S. Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science. 2009, 325:1254-1257

Choudhary, C. Kumar, F. Gnad, M.L. Nielsen, M. Rehman, T.C. Walther, J.V. Olsen, M. Mann Lysine Acetylation Targets Protein Complexes and Co-Regulates Major Cellular Functions. Science. 2009, 325:834-840

Schwer B, Eckersdorff M, Li Y, Silva JC, Fermin D, Kurtev MV, Giallourakis C, Comb MJ, Alt FW, Lombard DB. Calorie restriction alters mitochondrial protein acetylation. Aging Cell. 2009, 8:604-606

Ponchaut S, van Hoof F, Veitch K. Cytochrome aa3 depletion is the cause of the deficient mitochondrial respiration induced by chronic valproate administration. Biochem Pharmacol. 1992, 43:644-647

Silva MF, Ruiter JP, Li IJ, Jakobs C, Duran M, de Almeida IT, Wanders RJ. Differential effect of valproate and its Delta2- and Delta4-unsaturated metabolites, on the betaoxidation rate of long-chain and medium-chain fatty acids. Chem Biol Interact. 2001, 137:203-212

Turnbull DM, Bone AJ, Bartlett K, Koundakjian PP, Sherratt HS. The effects of valproate on intermediary metabolism in isolated rat hepatocytes and intact rats. Biochem Pharmacol. 1983, 32:1887-1892

Alcarraz-Vizan G, Boren J, Lee WN, Cascante M. Histone deacetylase inhibition results in a common metabolic profile associated with HT29 differentiation. Metabolomics. 2010, 6:229-237

Boren J, Lee WN, Bassilian S, Centelles JJ, Lim S, Cascante M. The stable isotope-based dynamic metabolic profile of butyrate-induced HT29 cell differentiation. J Biol Chem. 2003, 278: 28395-28402

Wardell SE, Ilkayeva OR, Wieman HL, Frigo DE, Rathmell JC. Glucose metabolism as a target of histone deacetylase inhibitors. Mol Endocrinol. 2009, 23:388-401

Amoêdo ND, Rodrigues MF, Pezzuto P, Galina A, Da Costa RM, De Almeida FCL, El-Bacha T, Rumjanek FD. Energy metabolism in H460 lung cancer cells: effects of histone deacetylase inhibitors. PloS One. 2011, 6 :, e22264

Zhao D, Zou S-W, Liu Y, Zhou X, Mo Y, Wang P, Xu Y-H, Dong B, Xiong Y, Lei Q-Y, Guan K-L. Lysine-5 acetylation negatively regulates lactate dehydrogenase a and is decreased in pancreatic cancer. Cancer Cell. 2013, 23:464-476

Zheng Y, Thompson PR, Cebrat M, Wang L, Devlin MK, Alani R, Cole P. Selective HAT inhibitors as mechanistic tools for protein acetylation. Methods in enzymology. 2004, 376 :, 188-199

Rekowski MVW, Giannis A. Histone acetylation modulation by small molecules: a chemical approach. Biochim Biophys Acta. 2010, 1799:760-767

Mahlknecht U, Hoelzer D. Histone acetylation modifiers in the pathogenesis of malignant disease. Molecular Med. 2000, 6:623-644

Kovacs JJ, Murphy PJM, 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, 18:601-607

Bali P, Pranpat M, Bradner J, Balasis M, Fiskus W, Guo F, Rocha K, Kumaraswamy S, Boyapalle S, Atadja P, Seto E, Bhalla K. Inhibition of histone deacetylase 6 acetylates and disrupts the chaperone function of heat shock protein 90: a novel basis of antileukemia activity of histone deacetylase inhibitors. J Biol Chem. 2005, 280:26729-26734

Kim SC, Sprung R, Chen Y, Xu Y, Ball H, Pei J, Cheng T, Kho Y, Xiao H, Xiao L, Grishin NV, White M, Yang XJ, Zhao Y. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol Cell. 2006, 23:607-618

Lee JH, Jeong EG, Choi MC, Kim SH, Park JH, Song SH, Park J, Bang YJ, Kim TY. Inhibition of histone deacetylase 10 induces thioredoxin-interacting protein and causes accumulation of reactive oxygen species in SNU-620 human gastric cancer cells. Mol Cell. 2010, 30:107-112

Kim SH, Jeong JW, Park JA, Lee JW, Seo JH, Jung BK, Bae MK, Kim KW. Regulation of the HIF-1alpha stability by histone deacetylases. Oncol Rep. 2007, 17:647-51


Refbacks

  • There are currently no refbacks.


AJCR(ISSN 2572-5769) Copyright © 2012-2021. All rights reserved. Published by Ivy Union Publishing, 3204 Valley Rush Dr, Apex, North Carolina 27502, United States