Role of histone deacetylase 2 in epigenetics and cellular senescence: Implications in lung inflammaging and COPD

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 303, Issue 7, 2012, Pages

  Yao, Hongwei ^a   Rahman, Irfan ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Cigarette smoke; DNA damage and repair; Inflammation; Oxidants; Polyphenols; Premature lung aging

Indexed keywords

BAICALIN; CIGARETTE SMOKE; CORTICOSTEROID; CURCUMIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ERYTHROMYCIN; FORMOTEROL; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; NORTRIPTYLINE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEASOME; PROTEIN KINASE C; SALMETEROL; SULFORAPHANE; THEOPHYLLINE;

ACETYLATION; ARTICLE; CARBONYLATION; CELL AGING; CELL STRESS; CHRONIC OBSTRUCTIVE LUNG DISEASE; DNA DAMAGE; DNA END JOINING REPAIR; DNA MODIFICATION; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME MODIFICATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; EPIGENETICS; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; LUNG EMPHYSEMA; NITRATION; NITROSYLATION; NONHUMAN; OXIDATIVE STRESS; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN PROCESSING; RESPIRATORY TRACT INFLAMMATION; SMOKING; TRANSLATIONAL RESEARCH; UBIQUITINATION;

ADRENAL CORTEX HORMONES; ANIMALS; CELL AGING; DNA DAMAGE; DNA REPAIR; EPIGENESIS, GENETIC; HISTONE DEACETYLASE 2; HISTONES; HUMANS; MICE; OXIDATIVE STRESS; PNEUMONIA; PROTEIN PROCESSING, POST-TRANSLATIONAL; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RATS; SMOKING;

EID: 84867162444     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00175.2012     Document Type: Article

References (147)

1. Acosta JC, O'Loghlen A, Banito A, Guijarro MV, Augert A, Raguz S, Fumagalli M, Da Costa M, Brown C, Popov N, Takatsu Y, Melamed J, Adda di Fagagna F, Bernard D, Hernando, E., Gil, J. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 133: 1006-1018, 2008.
2. Adenuga D, Caito S, Yao H, Sundar IK, Hwang JW, Chung S, Rahman I. Nrf2 deficiency influences susceptibility to steroid resistance via HDAC2 reduction. Biochem Biophys Res Commun 403: 452-456, 2010.
3. Adenuga D, Rahman I. Protein kinase CK2-mediated phosphorylation of HDAC2 regulates co-repressor formation, deacetylase activity and acetylation of HDAC2 by cigarette smoke and aldehydes. Arch Biochem Biophys 498: 62-73, 2010.
4. Adenuga D, Yao H, March TH, Seagrave J, Rahman I. Histone deacetylase 2 is phosphorylated, ubiquitinated, and degraded by cigarette smoke. Am J Respir Cell Mol Biol 40: 464-473, 2009.
5. Adimoolam S, Sirisawad M, Chen J, Thiemann P, Ford JM, Buggy JJ. HDAC inhibitor PCI-24781 decreases RAD51 expression and inhibits homologous recombination. Proc Natl Acad Sci USA 104: 19482-19487, 2007.
6. Alder JK, Guo N, Kembou F, Parry EM, Anderson CJ, Gorgy AI, Walsh MF, Sussan T, Biswal S, Mitzner W, Tuder RM, Armanios M. Telomere length is a determinant of emphysema susceptibility. Am J Respir Crit Care Med 184: 904-912, 2011.
7. Aoshiba K, Nagai A. Senescence hypothesis for the pathogenetic mechanism of chronic obstructive pulmonary disease. Proc Am Thorac Soc 6: 596-601, 2009.
8. Aoshiba K, Zhou F, Tsuji T, Nagai A. Dna damage as a molecular link in the pathogensis of copd in smokers. Eur Respir J 39: 1368-1376, 2012.
9. Baker DJ, Wijshake T, Tchkonia T, LeBrasseur NK, Childs BG, van de Sluis B, Kirkland JL, van Deursen JM. Clearance of p16Ink4apositive senescent cells delays ageing-associated disorders. Nature 479: 232-236, 2011.
10. Baltus GA, Kowalski MP, Tutter AV, Kadam S. A positive regulatory role for the mSin3A-HDAC complex in pluripotency through Nanog and Sox2. J Biol Chem 284: 6998-7006, 2009.
11. Bernhard D, Moser C, Backovic A, Wick G. Cigarette smoke-an aging accelerator? Exp Gerontol 42: 160-165, 2007.
12. Botuyan MV, Lee J, Ward IM, Kim JE, Thompson JR, Chen J, Mer G. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127: 1361-1373, 2006.
13. Braig M, Lee S, Loddenkemper C, Rudolph C, Peters AH, Schlegelberger B, Stein H, Dorken B, Jenuwein T, Schmitt CA. Oncogeneinduced senescence as an initial barrier in lymphoma development. Nature 436: 660-665, 2005.
14. Cannizzo ES, Clement CC, Sahu R, Follo C, Santambrogio L. Oxidative stress, inflamm-aging and immunosenescence. J Proteomics 74: 2313-2323, 2011.
15. Caramori G, Adcock IM, Casolari P, Ito K, Jazrawi E, Tsaprouni L, Villetti G, Civelli M, Carnini C, Chung KF, Barnes PJ, Papi A. Unbalanced oxidant-induced DNA damage and repair in COPD: a link towards lung cancer. Thorax 66: 521-527, 2011.
16. Ceylan E, Kocyigit A, Gencer M, Aksoy N, Selek S. Increased DNA damage in patients with chronic obstructive pulmonary disease who had once smoked or been exposed to biomass. Respir Med 100: 1270-1276, 2006.
17. Chapman RW, Phillips JE, Hipkin RW, Curran AK, Lundell D, Fine JS. CXCR2 antagonists for the treatment of pulmonary disease. Pharmacol Ther 121: 55-68, 2009.
18. Charron CE, Chou PC, Coutts DJ, Kumar V, To M, Akashi K, Pinhu L, Griffiths M, Adcock IM, Barnes PJ, Ito K. Hypoxia-inducible factor 1alpha induces corticosteroid-insensitive inflammation via reduction of histone deacetylase-2 transcription. J Biol Chem 284: 36047-36054, 2009.
19. Chen CS, Wang YC, Yang HC, Huang PH, Kulp SK, Yang CC, Lu YS, Matsuyama S, Chen CY. Histone deacetylase inhibitors sensitize prostate cancer cells to agents that produce DNA double-strand breaks by targeting Ku70 acetylation. Cancer Res 67: 5318-5327, 2007.
20. Chen Y, Huang P, Ai W, Li X, Guo W, Zhang J, Yang J. Histone deacetylase activity is decreased in peripheral blood monocytes in patients with COPD. J Inflamm 9: 10, 2012.
21. Chen Y, Wang H, Yoon SO, Xu X, Hottiger MO, Svaren J, Nave KA, Kim HA, Olson EN, Lu QR. HDAC-mediated deacetylation of NFkappaB is critical for Schwann cell myelination. Nat Neurosci 14: 437-441, 2011.
22. Colussi C, Mozzetta C, Gurtner A, Illi B, Rosati J, Straino S, Ragone G, Pescatori M, Zaccagnini G, Antonini A, Minetti G, Martelli F, Piaggio G, Gallinari P, Steinkuhler C, Clementi E, Dell'Aversana C, Altucci L, Mai A, Capogrossi MC, Puri PL, Gaetano C. HDAC2 blockade by nitric oxide and histone deacetylase inhibitors reveals a common target in Duchenne muscular dystrophy treatment. Proc Natl Acad Sci USA 105: 19183-19187, 2008.
23. Cosio BG, Tsaprouni L, Ito K, Jazrawi E, Adcock IM, Barnes PJ. Theophylline restores histone deacetylase activity and steroid responses in COPD macrophages. J Exp Med 200: 689-695, 2004.
24. Dannenberg JH, David G, Zhong S, van der Torre J, Wong WH, Depinho RA. mSin3A corepressor regulates diverse transcriptional networks governing normal and neoplastic growth and survival. Genes Dev 19: 1581-1595, 2005.
25. de Ruijter AJ, van Gennip AH, Caron HN, Kemp S, van Kuilenburg AB. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 370: 737-749, 2003.
26. De Santa F, Totaro MG, Prosperini E, Notarbartolo S, Testa G, Natoli G. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130: 1083-1094, 2007.
27. Deslee G, Adair-Kirk TL, Betsuyaku T, Woods JC, Moore CH, Gierada DS, Conradi SH, Atkinson JJ, Toennies HM, Battaile JT, Kobayashi DK, Patterson GA, Holtzman MJ, Pierce RA. Cigarette smoke induces nucleic-acid oxidation in lung fibroblasts. Am J Respir Cell Mol Biol 43: 576-584, 2010.
28. Deslee G, Woods JC, Moore C, Conradi SH, Gierada DS, Atkinson JJ, Battaile JT, Liu L, Patterson GA, Adair-Kirk TL, Holtzman MJ, Pierce RA. Oxidative damage to nucleic acids in severe emphysema. Chest 135: 965-974, 2009.
29. El Gazzar M, Yoza BK, Hu JY, Cousart SL, McCall CE. Epigenetic silencing of tumor necrosis factor alpha during endotoxin tolerance. J Biol Chem 282: 26857-26864, 2007.
30. Faucher D, Wellinger RJ. Methylated H3K4, a transcription-associated histone modification, is involved in the DNA damage response pathway. PLoS Genet 6: e1001082, 2010.
31. Fnu S, Williamson EA, De Haro LP, Brenneman M, Wray J, Shaheen M, Radhakrishnan K, Lee SH, Nickoloff JA, Hromas R. Methylation of histone H3 lysine 36 enhances DNA repair by nonhomologous end-joining. Proc Natl Acad Sci USA 108: 540-545, 2011.
32. Ford PA, Durham AL, Russell RE, Gordon F, Adcock IM, Barnes PJ. Treatment effects of low-dose theophylline combined with an inhaled corticosteroid in COPD. Chest 137: 1338-1344, 2010.
33. Foster SL, Hargreaves DC, Medzhitov R. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 447: 972-978, 2007.
34. Franceschi C, Bonafe M, Valensin S, Olivieri F, De Luca M, Ottaviani E, De Benedictis Inflamm-aging G. An evolutionary perspective on immunosenescence. Ann NY Acad Sci 908: 244-254, 2000.
35. Freund A, Orjalo AV, Desprez PY, Campisi J. Inflammatory networks during cellular senescence: causes and consequences. Trends Mol Med 16: 238-246, 2010.
36. Frye M, Fisher AG, Watt FM. Epidermal stem cells are defined by global histone modifications that are altered by Myc-induced differentiation. PLoS One 2: e763, 2007.
37. Fukuchi Y. The aging lung and chronic obstructive pulmonary disease: similarity and difference. Proc Am Thorac Soc 6: 570-572, 2009.
38. Gilmour PS, Rahman I, Donaldson K, MacNee W. Histone acetylation regulates epithelial IL-8 release mediated by oxidative stress from environmental particles. Am J Physiol Lung Cell Mol Physiol 284: L533-L540, 2003.
39. Gontan C, de Munck A, Vermeij M, Grosveld F, Tibboel D, Rottier R. Sox2 is important for two crucial processes in lung development: branching morphogenesis and epithelial cell differentiation. Dev Biol 317: 296-309, 2008.
40. Grandinetti KB, Jelinic P, DiMauro T, Pellegrino J, Fernandez Rodriguez R, Finnerty PM, Ruoff R, Bardeesy N, Logan SK, David G. Sin3B expression is required for cellular senescence and is upregulated upon oncogenic stress. Cancer Res 69: 6430-6437, 2009.
41. Guan JS, Haggarty SJ, Giacometti E, Dannenberg JH, Joseph N, Gao J, Nieland TJ, Zhou Y, Wang X, Mazitschek R, Bradner JE, DePinho RA, Jaenisch R, Tsai LH. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459: 55-60, 2009.
42. Guillemette B, Drogaris P, Lin HH, Armstrong H, Hiragami-Hamada K, Imhof A, Bonneil E, Thibault P, Verreault A, Festenstein RJ. H3 lysine 4 is acetylated at active gene promoters and is regulated by H3 lysine 4 methylation. PLoS Genet 7: e1001354, 2011.
43. Hashimoto S, Chen H, Que J, Brockway BL, Drake JA, Snyder JC, Randell SH, Stripp BR. beta-Catenin-SOX2 signaling regulates the fate of developing airway epithelium. J Cell Sci 125: 932-942, 2012.
44. Hassa PO, Haenni SS, Buerki C, Meier NI, Lane WS, Owen H, Gersbach M, Imhof R, Hottiger MO. Acetylation of poly(ADP-ribose) polymerase-1 by p300/CREB-binding protein regulates coactivation of NF-kappaB-dependent transcription. J Biol Chem 280: 40450-40464, 2005.
45. Huang PH, Chen CH, Chou CC, Sargeant AM, Kulp SK, Teng CM, Byrd JC, Chen CS. Histone deacetylase inhibitors stimulate histone H3 lysine 4 methylation in part via transcriptional repression of histone H3 lysine 4 demethylases. Mol Pharmacol 79: 197-206, 2011.
46. Huyen Y, Zgheib O, Ditullio RA Jr, Gorgoulis VG, Zacharatos P, Petty TJ, Sheston EA, Mellert HS, Stavridi ES, Halazonetis TD. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432: 406-411, 2004.
47. Ito K, Ito M, Elliott WM, Cosio B, Caramori G, Kon OM, Barczyk A, Hayashi S, Adcock IM, Hogg JC, Barnes PJ. Decreased histone deacetylase activity in chronic obstructive pulmonary disease. N Engl J Med 352: 1967-1976, 2005.
48. Ito K, Yamamura S, Essilfie-Quaye S, Cosio B, Ito M, Barnes PJ, Adcock IM. Histone deacetylase 2-mediated deacetylation of the glucocorticoid receptor enables NF-kappaB suppression. J Exp Med 203: 7-13, 2006.
49. Jung KH, Noh JH, Kim JK, Eun JW, Bae HJ, Xie HJ, Chang YG, Kim MG, Park H, Lee JY, Nam SW. HDAC2 overexpression confers oncogenic potential to human lung cancer cells by deregulating expression of apoptosis and cell cycle proteins. J Cell Biochem 113: 2167-2177, 2012.
50. Kageyama S, Liu H, Kaneko N, Ooga M, Nagata M, Aoki F. Alterations in epigenetic modifications during oocyte growth in mice. Reproduction 133: 85-94, 2007.
51. Kajstura J, Rota M, Hall SR, Hosoda T, D'Amario D, Sanada F, Zheng H, Ogorek B, Rondon-Clavo C, Ferreira-Martins J, Matsuda A, Arranto C, Goichberg P, Giordano G, Haley KJ, Bardelli S, Rayatzadeh H, Liu X, Quaini F, Liao R, Leri A, Perrella MA, Loscalzo J, Anversa P. Evidence for human lung stem cells. N Engl J Med 364: 1795-1806, 2011.
52. Karrasch S, Holz O, Jorres RA. Aging and induced senescence as factors in the pathogenesis of lung emphysema. Respir Med 102: 1215-1230, 2008.
53. Kim DW, Lassar AB. Smad-dependent recruitment of a histone deacetylase/ Sin3A complex modulates the bone morphogenetic protein-dependent transcriptional repressor activity of Nkx3.2. Mol Cell Biol 23: 8704-8717, 2003.
54. Kirkham PA, Caramori G, Casolari P, Papi AA, Edwards M, Shamji B, Triantaphyllopoulos K, Hussain F, Pinart M, Khan Y, Heinemann L, Stevens L, Yeadon M, Barnes PJ, Chung KF, Adcock IM. Oxidative stress-induced antibodies to carbonyl-modified protein correlate with severity of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 184: 796-802, 2011.
55. Koike K, Kondo Y, Sekiya M, Sato Y, Tobino K, Iwakami SI, Goto S, Takahashi K, Maruyama N, Seyama K, Ishigami A. Complete lack of vitamin C intake generates pulmonary emphysema in senescence marker protein-30 knockout mice. Am J Physiol Lung Cell Mol Physiol 298: L784-L792, 2010.
56. Koprinarova M, Botev P, Russev G. Histone deacetylase inhibitor sodium butyrate enhances cellular radiosensitivity by inhibiting both DNA nonhomologous end joining and homologous recombination. DNA Repair (Amst) 10: 970-977, 2011.
57. Kramer OH. HDAC2: a critical factor in health and disease. Trends Pharmacol Sci 30: 647-655, 2009.
58. Krishnamurthy J, Torrice C, Ramsey MR, Kovalev GI, Al-Regaiey K, Su L, Sharpless NE. Ink4a/Arf expression is a biomarker of aging. J Clin Invest 114: 1299-1307, 2004.
59. Krishnan V, Chow MZ, Wang Z, Zhang L, Liu B, Liu X, Zhou Z. Histone H4 lysine 16 hypoacetylation is associated with defective DNA repair and premature senescence in Zmpste24-deficient mice. Proc Natl Acad Sci USA 108: 12325-12330, 2011.
60. Kuilman T, Michaloglou C, Vredeveld LC, Douma S, van Doorn R, Desmet CJ, Aarden LA, Mooi WJ, Peeper DS. Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 133: 1019-1031, 2008.
61. Laberge RM, Zhou L, Sarantos MR, Rodier F, Freund A, de Keizer PL, Liu S, Demaria M, Cong YS, Kapahi P, Desprez PY, Hughes RE, Campisi J. Glucocorticoids suppress selected components of the senescenceassociated secretory phenotype. Aging Cell 11: 569-578, 2012.
62. Lambers C, Hacker S, Posch M, Hoetzenecker K, Pollreisz A, Lichtenauer M, Klepetko W, Ankersmit HJ. T cell senescence and contraction of T cell repertoire diversity in patients with chronic obstructive pulmonary disease. Clin Exp Immunol 155: 466-475, 2009.
63. Latham JA, Dent SY. Cross-regulation of histone modifications. Nat Struct Mol Biol 14: 1017-1024, 2007.
64. Lee J, Reddy R, Barsky L, Scholes J, Chen H, Shi W, Driscoll B. Lung alveolar integrity is compromised by telomere shortening in telomerasenull mice. Am J Physiol Lung Cell Mol Physiol 296: L57-L70, 2009.
65. Lee J, Sandford A, Man P, Sin DD. Is the aging process accelerated in chronic obstructive pulmonary disease? Curr Opin Pulm Med 17: 90-97, 2011.
66. Lee MG, Wynder C, Bochar DA, Hakimi MA, Cooch N, Shiekhattar R. Functional interplay between histone demethylase and deacetylase enzymes. Mol Cell Biol 26: 6395-6402, 2006.
67. Li L, Wu J, Liu B, Sun J, Gong W, Lv Y, Zhang H, Luo Q, Wu X, Dong J. Baicalin is anti-inflammatory in cigarette smoke-induced inflammatory models in vivo and in vitro: A possible role for HDAC2 activity. Int Immunopharmacol 13: 15-22, 2012.
68. Li M, Zhong X, He Z, Wen M, Li J, Peng X, Liu G, Deng J, Zhang J, Bai J. Effect of erythromycin on cigarette-induced histone deacetylase protein expression and nuclear factor-kappaB activity in human macrophages in vitro. Int Immunopharmacol 12: 643-650, 2012.
69. Li XN, Shu Q, Su JM, Perlaky L, Blaney SM, Lau CC. Valproic acid induces growth arrest, apoptosis, and senescence in medulloblastomas by increasing histone hyperacetylation and regulating expression of p21Cip1, CDK4, and CMYC. Mol Cancer Ther 4: 1912-1922, 2005.
70. Liu F, Killian JK, Yang M, Walker RL, Hong JA, Zhang M, Davis S, Zhang Y, Hussain M, Xi S, Rao M, Meltzer PA, Schrump DS. Epigenomic alterations and gene expression profiles in respiratory epithelia exposed to cigarette smoke condensate. Oncogene 29: 3650-3664, 2010.
71. Londhe VA, Sundar IK, Lopez B, Maisonet TM, Yu Y, Aghai ZH, Rahman I. Hyperoxia impairs alveolar formation and induces senescence through decreased histone deacetylase activity and up-regulation of p21 in neonatal mouse lung. Pediatr Res 69: 371-377, 2011.
72. Ma P, Pan H, Montgomery RL, Olson EN, Schultz RM. Compensatory functions of histone deacetylase 1 (HDAC1) and HDAC2 regulate transcription and apoptosis during mouse oocyte development. Proc Natl Acad Sci USA 109: E481-E489, 2012.
73. MacNee W. Accelerated lung aging: a novel pathogenic mechanism of chronic obstructive pulmonary disease (COPD). Biochem Soc Trans 37: 819-823, 2009.
74. MacNee W. Aging, inflammation, emphysema. Am J Respir Crit Care Med 184: 1327-1329, 2011.
75. Malhotra D, Thimmulappa RK, Mercado N, Ito K, Kombairaju P, Kumar S, Ma J, Feller-Kopman D, Wise R, Barnes P, Biswal S. Denitrosylation of HDAC2 by targeting Nrf2 restores glucocorticosteroid sensitivity in macrophages from COPD patients. J Clin Invest 121: 4289-4302, 2011.
76. Marchion DC, Bicaku E, Turner JG, Schmitt ML, Morelli DR, Munster PN. HDAC2 regulates chromatin plasticity and enhances DNA vulnerability. Mol Cancer Ther 8: 794-801, 2009.
77. Marinova Z, Leng Y, Leeds P, Chuang DM. Histone deacetylase inhibition alters histone methylation associated with heat shock protein 70 promoter modifications in astrocytes and neurons. Neuropharmacology 60: 1109-1115, 2011.
78. Marwick JA, Caramori G, Stevenson CS, Casolari P, Jazrawi E, Barnes PJ, Ito K, Adcock IM, Kirkham PA, Papi A. Inhibition of PI3Kdelta restores glucocorticoid function in smoking-induced airway inflammation in mice. Am J Respir Crit Care Med 179: 542-548, 2009.
79. Marwick JA, Kirkham PA, Stevenson CS, Danahay H, Giddings J, Butler K, Donaldson K, Macnee W, Rahman I. Cigarette smoke alters chromatin remodeling and induces proinflammatory genes in rat lungs. Am J Respir Cell Mol Biol 31: 633-642, 2004.
80. Meja KK, Rajendrasozhan S, Adenuga D, Biswas SK, Sundar IK, Spooner G, Marwick JA, Chakravarty P, Fletcher D, Whittaker P, Megson IL, Kirkham PA, Rahman I. Curcumin restores corticosteroid function in monocytes exposed to oxidants by maintaining HDAC2. Am J Respir Cell Mol Biol 39: 312-323, 2008.
81. Mercado N, To Y, Ito K, Barnes PJ. Nortriptyline reverses corticosteroid insensitivity by inhibition of phosphoinositide-3-kinase-delta. J Pharmacol Exp Ther 337: 465-470, 2011.
82. Miller KM, Tjeertes JV, Coates J, Legube G, Polo SE, Britton S, Jackson SP. Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat Struct Mol Biol 17: 1144-1151, 2010.
83. Mizuno S, Yasuo M, Bogaard HJ, Kraskauskas D, Natarajan R, Voelkel NF. Inhibition of histone deacetylase causes emphysema. Am J Physiol Lung Cell Mol Physiol 300: L402-L413, 2011.
84. Moodie FM, Marwick JA, Anderson CS, Szulakowski P, Biswas SK, Bauter MR, Kilty I, Rahman I. Oxidative stress and cigarette smoke alter chromatin remodeling but differentially regulate NF-_B activation and proinflammatory cytokine release in alveolar epithelial cells. FASEB J 18: 1897-1899, 2004.
85. Morrisey EE, Hogan BL. Preparing for the first breath: genetic and cellular mechanisms in lung development. Dev Cell 18: 8-23, 2010.
86. Muller KC, Welker L, Paasch K, Feindt B, Erpenbeck VJ, Hohlfeld JM, Krug N, Nakashima M, Branscheid D, Magnussen H, Jorres RA, Holz O. Lung fibroblasts from patients with emphysema show markers of senescence in vitro. Respir Res 7: 32, 2006.
87. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292: 110-113, 2001.
88. Nott A, Watson PM, Robinson JD, Crepaldi L, Riccio A. S-Nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature 455: 411-415, 2008.
89. Nottke A, Colaiacovo MP, Shi Y. Developmental roles of the histone lysine demethylases. Development 136: 879-889, 2009.
90. Nunez B, Sauleda J, Anto JM, Julia MR, Orozco M, Monso E, Noguera A, Gomez FP, Garcia-Aymerich J, Agusti A. Anti-tissue antibodies are related to lung function in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 183: 1025-1031, 2011.
91. Nyunoya T, Monick MM, Klingelhutz A, Yarovinsky TO, Cagley JR, Hunninghake GW. Cigarette smoke induces cellular senescence. Am J Respir Cell Mol Biol 35: 681-688, 2006.
92. Nyunoya T, Monick MM, Klingelhutz AL, Glaser H, Cagley JR, Brown CO, Matsumoto E, Aykin-Burns N, Spitz DR, Oshima J, Hunninghake GW. Cigarette smoke induces cellular senescence via Werner's syndrome protein down-regulation. Am J Respir Crit Care Med 179: 279-287, 2009.
93. Ogiwara H, Ui A, Otsuka A, Satoh H, Yokomi I, Nakajima S, Yasui A, Yokota J, Kohno T. Histone acetylation by CBP and p300 at double-strand break sites facilitates SWI/SNF chromatin remodeling and the recruitment of non-homologous end joining factors. Oncogene 30: 2135-2146, 2011.
94. Ohanna M, Giuliano S, Bonet C, Imbert V, Hofman V, Zangari J, Bille K, Robert C, Bressac-Depaillerets B, Hofman P, Rocchi S, Peyron JF, Lacour JP, Ballotti R, Bertolotto C. Senescent cells develop a PARP-1 and nuclear factor-kappaB-associated secretome (PNAS). Genes Dev 25: 1245-1261, 2011.
95. Osoata GO, Yamamura S, Ito M, Vuppusetty C, Adcock IM, Barnes PJ, Ito K. Nitration of distinct tyrosine residues causes inactivation of histone deacetylase 2. Biochem Biophys Res Commun 384: 366-371, 2009.
96. Palomera-Sanchez Z, Zurita M. Open, repair and close again: chromatin dynamics and the response to UV-induced DNA damage. DNA Repair (Amst) 10: 119-125, 2011.
97. Pastukh VM, Zhang L, Ruchko MV, Gorodnya O, Bardwell GC, Tuder RM, Gillespie MN. Oxidative DNA damage in lung tissue from patients with COPD is clustered in functionally significant sequences. Int J Chron Obstruct Pulmon Dis 6: 209-217, 2011.
98. Pegoraro G, Kubben N, Wickert U, Gohler H, Hoffmann K, Misteli T. Ageing-related chromatin defects through loss of the NURD complex. Nat Cell Biol 11: 1261-1267, 2009.
99. Perng DW, Su KC, Chou KT, Wu YC, Chen CS, Hsiao YH, Tseng CM, Chen YH, Hsueh TY, Lee YC. Long-acting beta(2) agonists and corticosteroids restore the reduction of histone deacetylase activity and inhibit H(2)O(2)-induced mediator release from alveolar macrophages. Pulm Pharmacol Ther 25: 312-318, 2012.
100. Que J, Luo X, Schwartz RJ, Hogan BL. Multiple roles for Sox2 in the developing and adult mouse trachea. Development 136: 1899-1907, 2009.
101. Rahman I, van Schadewijk AA, Crowther AJ, Hiemstra PS, Stolk J, MacNee W, De Boer WI. 4-Hydroxy-2-nonenal, a specific lipid peroxidation product, is elevated in lungs of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 166: 490-495, 2002.
102. Rea S, Eisenhaber F, O'Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, Jenuwein T. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406: 593-599, 2000.
103. Rodier F, Coppe JP, Patil CK, Hoeijmakers WA, Munoz DP, Raza SR, Freund A, Campeau E, Davalos AR, Campisi J. Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat Cell Biol 11: 973-979, 2009.
104. Rodier F, Munoz DP, Teachenor R, Chu V, Le O, Bhaumik D, Coppe JP, Campeau E, Beausejour CM, Kim SH, Davalos AR, Campisi J. DNA-SCARS: distinct nuclear structures that sustain damage-induced senescence growth arrest and inflammatory cytokine secretion. J Cell Sci 124: 68-81, 2011.
105. Rossetto D, Truman AW, Kron SJ, Cote J. Epigenetic modifications in double-strand break DNA damage signaling and repair. Clin Cancer Res 16: 4543-4552, 2010.
106. Sanders SL, Portoso M, Mata J, Bahler J, Allshire RC, Kouzarides T. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119: 603-614, 2004.
107. Sarg B, Koutzamani E, Helliger W, Rundquist I, Lindner HH. Postsynthetic trimethylation of histone H4 at lysine 20 in mammalian tissues is associated with aging. J Biol Chem 277: 39195-39201, 2002.
108. Sato T, Seyama K, Sato Y, Mori H, Souma S, Akiyoshi T, Kodama Y, Mori T, Goto S, Takahashi K, Fukuchi Y, Maruyama N, Ishigami A. Senescence marker protein-30 protects mice lungs from oxidative stress, aging, and smoking. Am J Respir Crit Care Med 174: 530-537, 2006.
109. Savale L, Chaouat A, Bastuji-Garin S, Marcos E, Boyer L, Maitre B, Sarni M, Housset B, Weitzenblum E, Matrat M, Le Corvoisier P, Rideau D, Boczkowski J, Dubois-Rande JL, Chouaid C, Adnot S. Shortened telomeres in circulating leukocytes of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 179: 566-571, 2009.
110. Seimetz M, Parajuli N, Pichl A, Veit F, Kwapiszewska G, Weisel FC, Milger K, Egemnazarov B, Turowska A, Fuchs B, Nikam S, Roth M, Sydykov A, Medebach T, Klepetko W, Jaksch P, Dumitrascu R, Garn H, Voswinckel R, Kostin S, Seeger W, Schermuly RT, Grimminger F, Ghofrani HA, Weissmann N. Inducible NOS inhibition reverses tobacco-smoke-induced emphysema and pulmonary hypertension in mice. Cell 147: 293-305, 2011.
111. Sengupta N, Seto E. Regulation of histone deacetylase activities. J Cell Biochem 93: 57-67, 2004.
112. Suga T, Kurabayashi M, Sando Y, Ohyama Y, Maeno T, Maeno Y, Aizawa H, Matsumura Y, Kuwaki T, Kuro OM, Nabeshima Y, Nagai R. Disruption of the klotho gene causes pulmonary emphysema in mice. Defect in maintenance of pulmonary integrity during postnatal life. Am J Respir Cell Mol Biol 22: 26-33, 2000.
113. Sugiura H, Kawabata H, Ichikawa T, Koarai A, Yanagisawa S, Kikuchi T, Minakata Y, Matsunaga K, Nakanishi M, Hirano T, Akamatsu K, Furukawa K, Ichinose M. Inhibitory effects of theophylline on the peroxynitrite-augmented release of matrix metalloproteinases by lung fibroblasts. Am J Physiol Lung Cell Mol Physiol 302: L764-L774, 2012.
114. Sun X, Li Q, Gong Y, Ren L, Wan H, Deng W. Low-dose theophylline restores corticosteroid responsiveness in rats with smoke-induced airway inflammation. Can J Physiol Pharmacol 90: 895-902, 2012.
115. Sundar IK, Hwang JW, Yao H, Rahman I. Profiling of epigenetic chromatin modification genes and susceptibility to chronic lung disease by cigarette smoke. Am J Respir Crit Care Med 185: A3480, 2012.
116. Szulakowski P, Crowther AJ, Jimenez LA, Donaldson K, Mayer R, Leonard TB, MacNee W, Drost EM. The effect of smoking on the transcriptional regulation of lung inflammation in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 174: 41-50, 2006.
117. Thatcher TH, McHugh NA, Egan RW, Chapman RW, Hey JA, Turner CK, Redonnet MR, Seweryniak KE, Sime PJ, Phipps RP. Role of CXCR2 in cigarette smoke-induced lung inflammation. Am J Physiol Lung Cell Mol Physiol 289: L322-L328, 2005.
118. Tilstra JS, Robinson AR, Wang J, Gregg SQ, Clauson CL, Reay DP, Nasto LA, St Croix CM, Usas A, Vo N, Huard J, Clemens PR, Stolz DB, Guttridge DC, Watkins SC, Garinis GA, Wang Y, Niedernhofer LJ, Robbins PD. NF-kappaB inhibition delays DNA damage-induced senescence and aging in mice. J Clin Invest 122: 2601-2612, 2012.
119. Tompkins DH, Besnard V, Lange AW, Wert SE, Keiser AR, Smith AN, Lang R, Whitsett JA. Sox2 is required for maintenance and differentiation of bronchiolar Clara, ciliated, and goblet cells. PLoS One 4: e8248, 2009.
120. Tsai SC, Seto E. Regulation of histone deacetylase 2 by protein kinase CK2. J Biol Chem 277: 31826-31833, 2002.
121. Tsuji T, Aoshiba K, Nagai A. Alveolar cell senescence exacerbates pulmonary inflammation in patients with chronic obstructive pulmonary disease. Respiration 80: 59-70, 2010.
122. Tsuji T, Aoshiba K, Nagai A. Alveolar cell senescence in patients with pulmonary emphysema. Am J Respir Crit Care Med 174: 886-893, 2006.
123. Tsuji T, Aoshiba K, Nagai A. Cigarette smoke induces senescence in alveolar epithelial cells. Am J Respir Cell Mol Biol 31: 643-649, 2004.
124. Tuder RM, Kern JA, Miller YE. Senescence in chronic obstructive pulmonary disease. Proc Am Thorac Soc 9: 62-63, 2012.
125. Vashisht Gopal YN, Arora TS, Van Dyke MW. Tumour necrosis factor-alpha depletes histone deacetylase 1 protein through IKK2. EMBO Rep 7: 291-296, 2006.
126. Vaute O, Nicolas E, Vandel L, Trouche D. Functional and physical interaction between the histone methyl transferase Suv39H1 and histone deacetylases. Nucleic Acids Res 30: 475-481, 2002.
127. Vempati RK, Jayani RS, Notani D, Sengupta A, Galande S, Haldar D. p300-mediated acetylation of histone H3 lysine 56 functions in DNA damage response in mammals. J Biol Chem 285: 28553-28564, 2010.
128. Wagner EJ, Carpenter PB. Understanding the language of Lys36 methylation at histone H3. Nat Rev Mol Cell Biol 13: 115-126, 2012.
129. Wagner M, Brosch G, Zwerschke W, Seto E, Loidl P, Jansen-Durr P. Histone deacetylases in replicative senescence: evidence for a senescencespecific form of HDAC-2. FEBS Lett 499: 101-106, 2001.
130. Wakeman TP, Wang Q, Feng J, Wang XF. Bat3 facilitates H3K79 dimethylation by DOT1L and promotes DNA damage-induced 53BP1 foci at G1/G2 cell-cycle phases. EMBO J 31: 2169-2181, 2012.
131. Whyte WA, Bilodeau S, Orlando DA, Hoke HA, Frampton GM, Foster CT, Cowley SM, Young RA. Enhancer decommissioning by LSD1 during embryonic stem cell differentiation. Nature 482: 221-225, 2012.
132. Wilting RH, Yanover E, Heideman MR, Jacobs H, Horner J, van der Torre J, DePinho RA, Dannenberg JH. Overlapping functions of Hdac1 and Hdac2 in cell cycle regulation and haematopoiesis. EMBO J 29: 2586-2597, 2010.
133. Winkler AR, Nocka KN, Williams CM. Smoke exposure of human macrophages reduces HDAC3 activity, resulting in enhanced inflammatory cytokine production. Pulm Pharmacol Ther 25: 286-292, 2012.
134. Woodhouse BC, Dianov GL. Poly ADP-ribose polymerase-1: an international molecule of mystery. DNA Repair (Amst) 7: 1077-1086, 2008.
135. Yang L, Mei Q, Zielinska-Kwiatkowska A, Matsui Y, Blackburn ML, Benedetti D, Krumm AA, Taborsky GJ Jr, Chansky HA. An ERG (ets-related gene)-associated histone methyltransferase interacts with histone deacetylases 1/2 and transcription co-repressors mSin3A/B. Biochem J 369: 651-657, 2003.
136. Yang SR, Chida AS, Bauter MR, Shafiq N, Seweryniak K, Maggirwar SB, Kilty I, Rahman I. Cigarette smoke induces proinflammatory cytokine release by activation of NF-_B and posttranslational modifications of histone deacetylase in macrophages. Am J Physiol Lung Cell Mol Physiol 291: L46-L57, 2006.
137. Yang WM, Inouye C, Zeng Y, Bearss D, Seto E. Transcriptional repression by YY1 is mediated by interaction with a mammalian homolog of the yeast global regulator RPD3. Proc Natl Acad Sci USA 93: 12845-12850, 1996.
138. Yao H, Chung S, Hwang JW, Rajendrasozhan S, Sundar IK, Dean DA, McBurney MW, Guarente L, Gu W, Ronty M, Kinnula VL, Rahman I. SIRT1 protects against emphysema via FOXO3-mediated reduction of premature senescence in mice. J Clin Invest 122: 2032-2045, 2012.
139. Yao H, Chung S, Sundar IK, Rahman I. Cigarette smoke extract treatment caused a residue-specific histone methylation and its cross-talk with histone acetylation in human lung epithelial cells. Am J Respir Crit Care Med 185: A3474, 2012.
140. Yao H, Edirisinghe I, Rajendrasozhan S, Yang SR, Caito S, Adenuga D, Rahman I. Cigarette smoke-mediated inflammatory and oxidative responses are strain-dependent in mice. Am J Physiol Lung Cell Mol Physiol 294: L1174-L1186, 2008.
141. Yao H, Hwang JW, Moscat J, Diaz-Meco MT, Leitges M, Kishore N, Li X, Rahman I. Protein kinase C zeta mediates cigarette smoke/ aldehydeand lipopolysaccharide-induced lung inflammation and histone modifications. J Biol Chem 285: 5405-5416, 2010.
142. Yao H, Rahman I. Current concepts on the role of inflammation in COPD and lung cancer. Curr Opin Pharmacol 9: 375-383, 2009.
143. Yuan J, Pu M, Zhang Z, Lou Z. Histone H3-K56 acetylation is important for genomic stability in mammals. Cell Cycle 8: 1747-1753, 2009.
144. Zhou BO, Wang SS, Zhang Y, Fu XH, Dang W, Lenzmeier BA, Zhou JQ. Histone H4 lysine 12 acetylation regulates telomeric heterochromatin plasticity in Saccharomyces cerevisiae. PLoS Genet 7: e1001272, 2011.
145. Zhou Q, Wang Y, Yang L, Chen P, Dong X, Xie L. Histone deacetylase inhibitors blocked activation and caused senescence of corneal stromal cells. Mol Vis 14: 2556-2565, 2008.
146. Zhou R, Han L, Li G, Tong T. Senescence delay and repression of p16INK4a by Lsh via recruitment of histone deacetylases in human diploid fibroblasts. Nucleic Acids Res 37: 5183-5196, 2009.
147. Zhu L, Li H, Tang J, Zhu J, Zhang Y. Hyperoxia arrests alveolar development through suppression of histone deacetylases in neonatal rats. Pediatr Pulmonol 47: 264-274, 2012.