Epigenetic regulation of muscle phenotype and adaptation: A potential role in COPD muscle dysfunction

Journal of Applied Physiology

Volumn 114, Issue 9, 2013, Pages 1263-1272

  Barreiro, Esther ^a,b   Sznajder, Jacob I ^c  

^a HOSPITAL DEL MAR   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Chronic obstructive pulmonary disease; Epigenetics; Muscle adaptation; Muscle dysfunction; Myogenesis

Indexed keywords

MICRORNA;

ADAPTATION; CHRONIC OBSTRUCTIVE LUNG DISEASE; EPIGENETICS; GENETIC EPIGENESIS; GENETICS; HUMAN; MUSCLE ADAPTATION; MUSCLE DEVELOPMENT; MUSCLE DYSFUNCTION; PATHOPHYSIOLOGY; PHENOTYPE; QUADRICEPS FEMORIS MUSCLE; REVIEW;

CHRONIC OBSTRUCTIVE PULMONARY DISEASE; EPIGENETICS; MUSCLE ADAPTATION; MUSCLE DYSFUNCTION; MYOGENESIS;

ADAPTATION, PHYSIOLOGICAL; EPIGENESIS, GENETIC; HUMANS; MICRORNAS; MUSCLE DEVELOPMENT; PHENOTYPE; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; QUADRICEPS MUSCLE;

EID: 84878550243     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01027.2012     Document Type: Review

References (101)

1. Alamdari N, Aversa Z, Castillero E, Hasselgren PO. Acetylation and deacetylation-novel factors in muscle wasting. Metabolism 62:1-11, 2013.
2. Alamdari N, Smith IJ, Aversa Z, Hasselgren PO. Sepsis and glucocorticoids upregulate p300 and downregulate HDAC6 expression and activity in skeletal muscle. Am J Physiol Regul Integr Comp Physiol 299:R509-R520, 2010.
3. Allen DL, Bandstra ER, Harrison BC, Thorng S, Stodieck LS, Kostenuik PJ, Morony S, Lacey DL, Hammond TG, Leinwand LL, Argraves WS, Bateman TA, Barth JL. Effects of spaceflight on murine skeletal muscle gene expression. J Appl Physiol 106:582-595, 2009.
4. Allen DL, Weber JN, Sycuro LK, Leinwand LA. Myocyte enhancer factor-2 and serum response factor binding elements regulate fast myosin heavy chain transcription in vivo. J Biol Chem 280:17126-17134, 2005. (Pubitemid 41389177)
5. Anderson C, Catoe H, Werner R. MIR-206 regulates connexin43 expression during skeletal muscle development. Nucleic Acids Res 34:5863-5871, 2006. (Pubitemid 44941165)
6. Angulo M, Lecuona E, Sznajder JI. Role of microRNAs in lung disease. Arch Bronconeumol 48:325-330, 2012.
7. Aoi W, Naito Y, Mizushima K, Takanami Y, Kawai Y, Ichikawa H, Yoshikawa T. The microRNA miR-696 regulates PGC-1α in mouse skeletal muscle in response to physical activity. Am J Physiol Endocrinol Metab 298:E799-E806, 2010.
8. Baar K. Epigenetic control of skeletal muscle fibre type. Acta Physiol (Oxf) 199:477-487, 2010.
9. Baldwin KM, Cheadle WG, Martinez OM, Cooke DA. Effect of functional overload on enzyme levels in different types of skeletal muscle. J Appl Physiol 42:312-317, 1977. (Pubitemid 8038608)
10. 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 for antileukemia activity of histone deacetylase inhibitors. J Biol Chem 280:26729-26734, 2005. (Pubitemid 41040705)
11. Barreiro E, De La PB, Minguella J, Corominas JM, Serrano S, Hussain SN, Gea J. Oxidative stress and respiratory muscle dysfunction in severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med 171:1116-1124, 2005. (Pubitemid 40663723)
12. Barreiro E, Del Puerto-Nevado L, Puig-Vilanova E, Perez-Rial S, Sanchez F, Martinez-Galan L, Rivera S, Gea J, Gonzalez-Mangado N, and Peces-Barba G. Cigarette smoke-induced oxidative stress in skeletal muscles of mice. Respir Physiol Neurobiol 182:9-17, 2012.
13. Barreiro E, Ferrer D, Sanchez F, Minguella J, Marin-Corral J, Martinez-Llorens J, Lloreta J, Gea J. Inflammatory cells and apoptosis in respiratory and limb muscles of patients with COPD. J Appl Physiol 111:808-817, 2011.
14. Barreiro E, Galdiz JB, Marinan M, Alvarez FJ, Hussain SN, Gea J. Respiratory loading intensity and diaphragm oxidative stress: N-acetylcysteine effects. J Appl Physiol 100:555-563, 2006. (Pubitemid 43671608)
15. Barreiro E, Gea J, Matar G, Hussain SN. Expression and carbonylation of creatine kinase in the quadriceps femoris muscles of patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 33:636-642, 2005. (Pubitemid 41753140)
16. Barreiro E, Peinado VI, Galdiz JB, Ferrer E, Marin-Corral J, Sanchez F, Gea J, Barbera JA. Cigarette smoke-induced oxidative stress: a role in chronic obstructive pulmonary disease skeletal muscle dysfunction. Am J Respir Crit Care Med 182:477-488, 2010.
17. Barreiro E, Rabinovich R, Marin-Corral J, Barbera JA, Gea J, Roca J. Chronic endurance exercise induces quadriceps nitrosative stress in patients with severe COPD. Thorax 64:13-19, 2009.
18. Barreiro E, Schols AM, Polkey MI, Galdiz JB, Gosker HR, Swallow EB, Coronell C, Gea J. Cytokine profile in quadriceps muscles of patients with severe COPD. Thorax 63:100-107, 2008. (Pubitemid 351236469)
19. Bentzinger CF, Wang YX, Rudnicki MA. Building muscle: molecular regulation of myogenesis. Cold Spring Harb Perspect Biol 4:2012.
20. Braun T, Bober E, Winter B, Rosenthal N, Arnold HH. Myf-6, a new member of the human gene family of myogenic determination factors: evidence for a gene cluster on chromosome 12. EMBO J 9:821-831, 1990.
21. Bustamante V, Casanova J, Lopez De SE, Mas S, Sellares J, Gea J, Galdiz JB, Barreiro E. Redox balance following magnetic stimulation training in the quadriceps of patients with severe COPD. Free Radic Res 42:939-948, 2008.
22. Caron C, Boyault C, Khochbin S. Regulatory cross-talk between lysine acetylation and ubiquitination: role in the control of protein stability. Bioessays 27:408-415, 2005. (Pubitemid 40592597)
23. Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL, Wang DZ. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 38:228-233, 2006. (Pubitemid 43177239)
24. Chen LF, Greene WC. Regulation of distinct biological activities of the NF-kappaB transcription factor complex by acetylation. J Mol Med (Berl) 81:549-557, 2003. (Pubitemid 37214993)
25. Cohen TJ, Waddell DS, Barrientos T, Lu Z, Feng G, Cox GA, Bodine SC, Yao TP. The histone deacetylase HDAC4 connects neural activity to muscle transcriptional reprogramming. J Biol Chem 282:33752-33759, 2007. (Pubitemid 350159508)
26. Cote J, Richard S. Tudor domains bind symmetrical dimethylated arginines. J Biol Chem 280:28476-28483, 2005. (Pubitemid 41105747)
27. Crist CG, Montarras D, Pallafacchina G, Rocancourt D, Cumano A, Conway SJ, Buckingham M. Muscle stem cell behavior is modified by microRNA-27 regulation of Pax3 expression. Proc Natl Acad Sci USA 106:13383-13387, 2009.
28. Davidsen PK, Gallagher IJ, Hartman JW, Tarnopolsky MA, Dela F, Helge JW, Timmons JA, Phillips SM. High responders to resistance exercise training demonstrate differential regulation of skeletal muscle microRNA expression. J Appl Physiol 110:309-317, 2011.
29. Davis RL, Weintraub H, Lassar AB. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51:987-1000, 1987.
30. Deato MD, Marr MT, Sottero T, Inouye C, Hu P, Tjian R. MyoD targets TAF3/TRF3 to activate myogenin transcription. Mol Cell 32:96-105, 2008.
31. Drummond MJ, McCarthy JJ, Fry CS, Esser KA, Rasmussen BB. Aging differentially affects human skeletal muscle microRNA expression at rest and after an anabolic stimulus of resistance exercise and essential amino acids. Am J Physiol Endocrinol Metab 295:E1333-E1340, 2008.
32. Edmondson DG, Olson EN. A gene with homology to the myc similarity region of MyoD1 is expressed during myogenesis and is sufficient to activate the muscle differentiation program. Genes Dev 3:628-640, 1989.
33. Elia L, Contu R, Quintavalle M, Varrone F, Chimenti C, Russo MA, Cimino V, De ML, Frustaci A, Catalucci D, Condorelli G. Reciprocal regulation of microRNA-1 and insulin-like growth factor-1 signal transduction cascade in cardiac and skeletal muscle in physiological and pathological conditions. Circulation 120:2377-2385, 2009.
34. Ellis PD, Martin KM, Rickman C, Metcalfe JC, Kemp PR. Increased actin polymerization reduces the inhibition of serum response factor activity by Yin Yang 1. Biochem J 364:547-554, 2002. (Pubitemid 34620815)
35. Fermoselle C, Rabinovich R, Ausin P, Puig-Vilanova E, Coronell C, Sanchez F, Roca J, Gea J, Barreiro E. Does oxidative stress modulate limb muscle atrophy in severe COPD patients? Eur Respir J 40:851-862, 2012.
36. Fredriksson K, Tjader I, Keller P, Petrovic N, Ahlman B, Scheele C, Wernerman J, Timmons JA, Rooyackers O. Dysregulation of mitochondrial dynamics and the muscle transcriptome in ICU patients suffering from sepsis induced multiple organ failure. PLoS One 3:e3686, 2008.
37. Gallagher IJ, Scheele C, Keller P, Nielsen AR, Remenyi J, Fischer CP, Roder K, Babraj J, Wahlestedt C, Hutvagner G, Pedersen BK, Timmons JA. Integration of microRNA changes in vivo identifies novel molecular features of muscle insulin resistance in type 2 diabetes. Genome Med 2:9, 2010.
38. Gosselink R, Troosters T, Decramer M. Peripheral muscle weakness contributes to exercise limitation in COPD. Am J Respir Crit Care Med 153:976-980, 1996. (Pubitemid 26081648)
39. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130:77-88, 2007. (Pubitemid 47031323)
40. Huang Y, Fang J, Bedford MT, Zhang Y, Xu RM. Recognition of histone H3 lysine-4 methylation by the double tudor domain of JMJD2A. Science 312:748-751, 2006.
41. Hupkes M, Jonsson MK, Scheenen WJ, Van RW, Sotoca AM, Van Someren EP, Van Der Heyden MA, Van Veen TA, Van Ravestein-van Os RI, Bauerschmidt S, Piek E, Ypey DL, Van Zoelen EJ, Dechering KJ. Epigenetics: DNA demethylation promotes skeletal myotube maturation. FASEB J 25:3861-3872, 2011.
42. Hutcheson DA, Zhao J, Merrell A, Haldar M, Kardon G. Embryonic and fetal limb myogenic cells are derived from developmentally distinct progenitors and have different requirements for beta-catenin. Genes Dev 23:997-1013, 2009.
43. Hutvagner G. Small RNA asymmetry in RNAi: function in RISC assembly and gene regulation. FEBS Lett 579:5850-5857, 2005. (Pubitemid 41487105)
44. Ianuzzo CD, Chen V. Metabolic character of hypertrophied rat muscle. J Appl Physiol 46:738-742, 1979. (Pubitemid 9172224)
45. Ianuzzo CD, Gollnick PD, Armstrong RB. Compensatory adaptations of skeletal muscle fiber types to a long-term functional overload. Life Sci 19:1517-1523, 1976.
46. Ikeda S, He A, Kong SW, Lu J, Bejar R, Bodyak N, Lee KH, Ma Q, Kang PM, Golub TR, Pu WT. MicroRNA-1 negatively regulates expression of the hypertrophy-associated calmodulin and Mef2a genes. Mol Cell Biol 29:2193-2204, 2009.
47. Ito A, Kawaguchi Y, Lai CH, Kovacs JJ, Higashimoto Y, Appella E, Yao TP. MDM2-HDAC1-mediated deacetylation of p53 is required for its degradation. EMBO J 21:6236-6245, 2002. (Pubitemid 35415340)
48. Jacobs SA, Khorasanizadeh S. Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295:2080-2083, 2002. (Pubitemid 34229471)
49. Jin YH, Jeon EJ, Li QL, Lee YH, Choi JK, Kim WJ, Lee KY, Bae SC. Transforming growth factor-beta stimulates p300-dependent RUNX3 acetylation, which inhibits ubiquitination-mediated degradation. J Biol Chem 279:29409-29417, 2004. (Pubitemid 38915820)
50. Keller P, Vollaard NB, Gustafsson T, Gallagher IJ, Sundberg CJ, Rankinen T, Britton SL, Bouchard C, Koch LG, Timmons JA. A transcriptional map of the impact of endurance exercise training on skeletal muscle phenotype. J Appl Physiol 110:46-59, 2011.
51. Kraft CS, Le Moine CM, Lyons CN, Michaud D, Mueller CR, Moyes CD. Control of mitochondrial biogenesis during myogenesis. Am J Physiol Cell Physiol 290:C1119-C1127, 2006.
52. Kuang S, Kuroda K, Le GF, Rudnicki MA. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129:999-1010, 2007. (Pubitemid 46802699)
53. Kurihara Y, Watanabe Y. Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101:12753-12758, 2004. (Pubitemid 39122095)
54. Lawless MW, O'Byrne KJ, Gray SG. Targeting oxidative stress in cancer. Expert Opin Ther Targets 14:1225-1245, 2010.
55. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23:4051-4060, 2004. (Pubitemid 39472426)
56. Lewis A, Riddoch-Contreras J, Natanek SA, Donaldson A, Man WD, Moxham J, Hopkinson NS, Polkey MI, Kemp PR. Downregulation of the serum response factor/miR-1 axis in the quadriceps of patients with COPD. Thorax 67:26-34, 2012.
57. Lucarelli M, Fuso A, Strom R, Scarpa S. The dynamics of myogenin site-specific demethylation is strongly correlated with its expression and with muscle differentiation. J Biol Chem 276:7500-7506, 2001.
58. Maltais F, Le Blanc P, Jobin J, Berube C, Bruneau J, Carrier L, Breton MJ, Falardeau G, Belleau R. Intensity of training and physiologic adaptation in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 155:555-561, 1997. (Pubitemid 27085801)
59. Marin-Corral J, Minguella J, Ramirez-Sarmiento AL, Hussain SN, Gea J, Barreiro E. Oxidised proteins and superoxide anion production in the diaphragm of severe COPD patients. Eur Respir J 33:1309-1319, 2009.
60. Marquis K, Debigare R, Lacasse Y, Le Blanc P, Jobin J, Carrier G, Maltais F. Midthigh muscle cross-sectional area is a better predictor of mortality than body mass index in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 166:809-813, 2002.
61. McCarthy JJ, Esser KA. MicroRNA-1 and microRNA-133a expression are decreased during skeletal muscle hypertrophy. J Appl Physiol 102:306-313, 2007. (Pubitemid 46089780)
62. McCarthy JJ, Esser KA, Peterson CA, Dupont-Versteegden EE. Evidence of MyomiR network regulation of beta-myosin heavy chain gene expression during skeletal muscle atrophy. Physiol Genomics 39:219-226, 2009.
63. McGee SL. Exercise and HDAC interactions. Appl Physiol Nutr Metab 32:852-856, 2007.
64. McGee SL, Fairlie E, Garnham AP, Hargreaves M. Exercise-induced histone modifications in human skeletal muscle. J Physiol 587:5951-5958, 2009.
65. 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 57:860-867, 2008.
66. McKinnell IW, Ishibashi J, Le GF, Punch VG, Addicks GC, Greenblatt JF, Dilworth FJ, Rudnicki MA. Pax7 activates myogenic genes by recruitment of a histone methyltransferase complex. Nat Cell Biol 10:77-84, 2008.
67. McKinsey TA, Zhang CL, Olson EN. Control of muscle development by dueling HATs and HDACs. Curr Opin Genet Dev 11:497-504, 2001. (Pubitemid 32800722)
68. Mercken EM, Hageman GJ, Schols AM, Akkermans MA, Bast A, Wouters EF. Rehabilitation decreases exercise-induced oxidative stress in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 172:994-1001, 2005. (Pubitemid 41476536)
69. Moresi V, Williams AH, Meadows E, Flynn JM, Potthoff MJ, McAnally J, Shelton JM, Backs J, Klein WH, Richardson JA, Bassel-Duby R, Olson EN. Myogenin and class II HDACs control neurogenic muscle atrophy by inducing E3 ubiquitin ligases. Cell 143:35-45, 2010.
70. Naguibneva I, Ameyar-Zazoua M, Polesskaya A, Ait-Si-Ali S, Groisman R, Souidi M, Cuvellier S, Harel-Bellan A. The microRNA miR-181 targets the homeobox protein Hox-A11 during mammalian myoblast differentiation. Nat Cell Biol 8:278-284, 2006. (Pubitemid 43336070)
71. Nakajima N, Takahashi T, Kitamura R, Isodono K, Asada S, Ueyama T, Matsubara H, Oh H. MicroRNA-1 facilitates skeletal myogenic differentiation without affecting osteoblastic and adipogenic differentiation. Biochem Biophys Res Commun 350:1006-1012, 2006. (Pubitemid 44584193)
72. Natanek SA, Riddoch-Contreras J, Marsh GS, Hopkinson NS, Man WD, Moxham J, Polkey MI, Kemp PR. Yin Yang 1 expression and localisation in quadriceps muscle in COPD. Arch Bronconeumol 47:296-302, 2011.
73. Nielsen S, Scheele C, Yfanti C, Akerstrom T, Nielsen AR, Pedersen BK, Laye MJ. Muscle specific microRNAs are regulated by endurance exercise in human skeletal muscle. J Physiol 588:4029-4037, 2010.
74. O'Rourke JR, Georges SA, Seay HR, Tapscott SJ, McManus MT, Goldhamer DJ, Swanson MS, Harfe BD. Essential role for Dicer during skeletal muscle development. Dev Biol 311:359-368, 2007. (Pubitemid 350046531)
75. Palacios D, Puri PL. The epigenetic network regulating muscle development and regeneration. J Cell Physiol 207:1-11, 2006.
76. Pandorf CE, Haddad F, Wright C, Bodell PW, Baldwin KM. Differential epigenetic modifications of histones at the myosin heavy chain genes in fast and slow skeletal muscle fibers and in response to muscle unloading. Am J Physiol Cell Physiol 297:C6-C16, 2009.
77. Perdiguero E, Sousa-Victor P, Ballestar E, Munoz-Canoves P. Epigenetic regulation of myogenesis. Epigenetics 4:541-550, 2009.
78. Potthoff MJ, Wu H, Arnold MA, Shelton JM, Backs J, McAnally J, Richardson JA, Bassel-Duby R, Olson EN. Histone deacetylase degradation and MEF2 activation promote the formation of slow-twitch myofibers. J Clin Invest 117:2459-2467, 2007. (Pubitemid 47494347)
79. Rao PK, Kumar RM, Farkhondeh M, Baskerville S, Lodish HF. Myogenic factors that regulate expression of muscle-specific microRNAs. Proc Natl Acad Sci USA 103:8721-8726, 2006. (Pubitemid 43878086)
80. Rodriguez DA, Kalko S, Puig-Vilanova E, Perez-Olabarria M, Falciani F, Gea J, Cascante M, Barreiro E, Roca J. Muscle and blood redox status after exercise training in severe COPD patients. Free Radic Biol Med 52:88-94, 2012.
81. Sadoul K, Boyault C, Pabion M, Khochbin S. Regulation of protein turnover by acetyltransferases and deacetylases. Biochimie 90:306-312, 2008. (Pubitemid 351172566)
82. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA. Pax7 is required for the specification of myogenic satellite cells. Cell 102:777-786, 2000.
83. Seymour JM, Spruit MA, Hopkinson NS, Natanek SA, Man WD, Jackson A, Gosker HR, Schols AM, Moxham J, Polkey MI, Wouters EF. The prevalence of quadriceps weakness in COPD and the relationship with disease severity. Eur Respir J 36:81-88, 2010.
84. Sharma S, Kelly TK, Jones PA. Epigenetics in cancer. Carcinogenesis 31:27-36, 2010.
85. Simonsson M, Heldin CH, Ericsson J, Gronroos E. The balance between acetylation and deacetylation controls Smad7 stability. J Biol Chem 280:21797-21803, 2005. (Pubitemid 40827829)
86. Sun Y, Ge Y, Drnevich J, Zhao Y, Band M, Chen J. Mammalian target of rapamycin regulates miRNA-1 and follistatin in skeletal myogenesis. J Cell Biol 189:1157-1169, 2010.
87. Swallow EB, Reyes D, Hopkinson NS, Man WD, Porcher R, Cetti EJ, Moore AJ, Moxham J, Polkey MI. Quadriceps strength predicts mortality in patients with moderate to severe chronic obstructive pulmonary disease. Thorax 62:115-120, 2007.
88. Tajbakhsh S. Skeletal muscle stem cells in developmental versus regenerative myogenesis. J Intern Med 266:372-389, 2009.
89. Taverna SD, Ilin S, Rogers RS, Tanny JC, Lavender H, Li H, Baker L, Boyle J, Blair LP, Chait BT, Patel DJ, Aitchison JD, Tackett AJ, Allis CD. Yng1 PHD finger binding to H3 trimethylated at K4 promotes NuA3 HAT activity at K14 of H3 and transcription at a subset of targeted ORFs. Mol Cell 24:785-796, 2006. (Pubitemid 44839214)
90. Taylor SM, Jones PA. Multiple new phenotypes induced in 10T1/2 and 3T3 cells treated with 5-azacytidine. Cell 17:771-779, 1979. (Pubitemid 9252286)
91. Walsh B, Hooks RB, Hornyak JE, Koch LG, Britton SL, Hogan MC. Enhanced mitochondrial sensitivity to creatine in rats bred for high aerobic capacity. J Appl Physiol 100:1765-1769, 2006. (Pubitemid 43845848)
92. Wang H, Garzon R, Sun H, Ladner KJ, Singh R, Dahlman J, Cheng A, Hall BM, Qualman SJ, Chandler DS, Croce CM, Guttridge DC. NF-kappaB-YY1-miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma. Cancer Cell 14:369-381, 2008.
93. Wang H, Hertlein E, Bakkar N, Sun H, Acharyya S, Wang J, Carathers M, Davuluri R, Guttridge DC. NF-kappaB regulation of YY1 inhibits skeletal myogenesis through transcriptional silencing of myofibrillar genes. Mol Cell Biol 27:4374-4387, 2007. (Pubitemid 46906562)
94. Wang L, Tang Y, Cole PA, Marmorstein R. Structure and chemistry of the p300/CBP and Rtt109 histone acetyltransferases: implications for histone acetyltransferase evolution and function. Curr Opin Struct Biol 18:741-747, 2008.
95. Weintraub H, Tapscott SJ, Davis RL, Thayer MJ, Adam MA, Lassar AB, Miller AD. Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. Proc Natl Acad Sci USA 86:5434-5438, 1989. (Pubitemid 19185563)
96. Wisloff U, Najjar SM, Ellingsen O, Haram PM, Swoap S, Al-Share Q, Fernstrom M, Rezaei K, Lee SJ, Koch LG, Britton SL. Cardiovascular risk factors emerge after artificial selection for low aerobic capacity. Science 307:418-420, 2005. (Pubitemid 40139985)
97. Wu H, Rothermel B, Kanatous S, Rosenberg P, Naya FJ, Shelton JM, Hutcheson KA, Di Maio JM, Olson EN, Bassel-Duby R, Williams RS. Activation of MEF2 by muscle activity is mediated through a calcineurin-dependent pathway. EMBO J 20:6414-6423, 2001. (Pubitemid 33078714)
98. Yang H, Menconi MJ, Wei W, Petkova V, Hasselgren PO. Dexamethasone upregulates the expression of the nuclear cofactor p300 and its interaction with C/EBPbeta in cultured myotubes. J Cell Biochem 94:1058-1067, 2005. (Pubitemid 41420264)
99. Yang H, Wei W, Menconi M, Hasselgren PO. Dexamethasone-induced protein degradation in cultured myotubes is p300/HAT dependent. Am J Physiol Regul Integr Comp Physiol 292:R337-R344, 2007. (Pubitemid 46089846)
100. Yang XJ, Seto E. Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol Cell 31:449-461, 2008.
101. Zhao Y, Samal E, Srivastava D. Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 436:214-220, 2005. (Pubitemid 41021266)