Retinoic acid-related orphan receptor-α is induced in the setting of DNA damage and promotes pulmonary emphysema

American Journal of Respiratory and Critical Care Medicine

Volumn 186, Issue 5, 2012, Pages 412-419

  Shi, Ying ^a   Cao, Jiaofei ^a   Gao, Jane ^a   Zheng, Liang ^b   Goodwin, Andrew ^a   An, Chang Hyoek ^a   Patel, Avignat ^a   Lee, Janet S ^b   Duncan, Steven R ^b   Kaminski, Naftali ^b   Pandit, Kusum V ^b   Rosas, Ivan O ^a   Choi, Augustine M K ^a,b   Morse, Danielle ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Chronic obstructive pulmonary disease; p53; Retinoic acid related orphan receptor ; Senescence

Indexed keywords

CIGARETTE SMOKE; ELASTASE; RETINOIC ACID RECEPTOR ALPHA; RETINOIC ACID RELATED ORPHAN RECEPTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATAXIA TELANGIECTASIA; CELL CULTURE; CELL DEATH; CELL NUCLEUS; CELL STRESS; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; GENE; GENE EXPRESSION PROFILING; GENE SILENCING; GENE TRANSLOCATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LUNG EMPHYSEMA; LUNG PARENCHYMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BIOLOGICAL MARKERS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION PROFILING; HUMANS; LUNG; MICE; MICE, INBRED C57BL; MICE, NEUROLOGIC MUTANTS; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 1; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; PULMONARY EMPHYSEMA; TOBACCO SMOKE POLLUTION;

EID: 84865825957     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201111-2023OC     Document Type: Article

References (54)

1. Stapleton CM, Jaradat M, Dixon D, Kang HS, Kim SC, Liao G, Carey MA, Cristiano J, Moorman MP, Jetten AM. Enhanced susceptibility of staggerer (roralphasg/sg) mice to lipopolysaccharide-induced lung inflammation. Am J Physiol Lung Cell Mol Physiol 2005;289: L144-L152. (Pubitemid 40863564)
2. Jaradat M, Stapleton C, Tilley SL, Dixon D, Erikson CJ, McCaskill JG, Kang HS, Angers M, Liao G, Collins J, et al. Modulatory role for retinoid-related orphan receptor alpha in allergen-induced lung inflammation. Am J Respir Crit Care Med 2006;174:1299-1309. (Pubitemid 44913031)
3. Meyer T, Kneissel M, Mariani J, Fournier B. In vitro and in vivo evidence for orphan nuclear receptor roralpha function in bone metabolism. Proc Natl Acad Sci U S A 2000;97:9197-9202. (Pubitemid 30626697)
4. Ueda HR, Chen W, Adachi A, Wakamatsu H, Hayashi S, Takasugi T, Nagano M, Nakahama K, Suzuki Y, Sugano S, et al. A transcription factor response element for gene expression during circadian night. Nature 2002;418:534-539. (Pubitemid 34851399)
5. Coste H, Rodriguez JC. Orphan nuclear hormone receptor rev-erbalpha regulates the human apolipoprotein CIII promoter. J Biol Chem 2002; 277:27120-27129. (Pubitemid 34951726)
6. Serra HG, Duvick L, Zu T, Carlson K, Stevens S, Jorgensen N, Lysholm A, Burright E, Zoghbi HY, Clark HB, et al. Roralpha-mediated Purkinje cell development determines disease severity in adult sca1 mice. Cell 2006;127:697-708. (Pubitemid 44716252)
7. Hoeijmakers JH. DNA damage, aging, and cancer. N Engl J Med 2009; 361:1475-1485.
8. Davis T, Kipling D. Werner syndrome as an example of inflamm-aging: possible therapeutic opportunities for a progeroid syndrome? Rejuvenation Res 2006;9:402-407. (Pubitemid 44168875)
9. McGrath-Morrow SA, Collaco JM, Crawford TO, Carson KA, Lefton-Greif MA, Zeitlin P, Lederman HM. Elevated serum IL-8 levels in ataxia telangiectasia. J Pediatr 2010;156:682-684.e1.
10. Patel BD, Loo WJ, Tasker AD, Screaton NJ, Burrows NP, Silverman EK, Lomas DA. Smoking related COPD and facial wrinkling: Is there a common susceptibility? Thorax 2006;61:568-571. (Pubitemid 44035135)
11. Ohara T, Hirai T, Muro S, Haruna A, Terada K, Kinose D, Marumo S, Ogawa E, Hoshino Y, Niimi A, et al. Relationship between pulmonary emphysema and osteoporosis assessed by CT in patients with COPD. Chest 2008;134:1244-1249.
12. Schmidt MI, Duncan BB, Sharrett AR, Lindberg G, Savage PJ, Offenbacher S, Azambuja MI, Tracy RP, Heiss G. Markers of inflammation and prediction of diabetes mellitus in adults (atherosclerosis risk in communities study): a cohort study. Lancet 1999;353:1649-1652. (Pubitemid 29224520)
13. Curkendall SM, DeLuise C, Jones JK, Lanes S, Stang MR, Goehring E Jr, She D. Cardiovascular disease in patients with chronic obstructive pulmonary disease: Saskatchewan Canada cardiovascular disease in COPD patients. Ann Epidemiol 2006;16:63-70. (Pubitemid 41783891)
14. Sin DD, Man SF. Why are patients with chronic obstructive pulmonary disease at increased risk of cardiovascular diseases? The potential role of systemic inflammation in chronic obstructive pulmonary disease. Circulation 2003;107:1514-1519. (Pubitemid 36378490)
15. Wilson DO, Weissfeld JL, Balkan A, Schragin JG, Fuhrman CR, Fisher SN, Wilson J, Leader JK, Siegfried JM, Shapiro SD, et al. Association of radiographic emphysema and airflow obstruction with lung cancer. Am J Respir Crit Care Med 2008;178:738-744.
16. Schwartz AG, Cote ML, Wenzlaff AS, Van Dyke A, Chen W, Ruckdeschel JC, Gadgeel S, Soubani AO. Chronic obstructive lung diseases and risk of non-small cell lung cancer in women. J Thorac Oncol 2009;4:291-299.
17. Young RP, Hopkins RJ, Christmas T, Black PN, Metcalf P, Gamble GD. COPD prevalence is increased in lung cancer, independent of age, sex and smoking history. Eur Respir J 2009;34:380-386.
18. DeMarini DM. Genotoxicity of tobacco smoke and tobacco smoke condensate: a review. Mutat Res 2004;567:447-474. (Pubitemid 39574548)
19. Hersh CP, Pillai SG, Zhu G, Lomas DA, Bakke P, Gulsvik A, Demeo DL, Klanderman BJ, Lazarus R, Litonjua AA, et al. Multi-study fine mapping of chromosome 2q identifies xrcc5 as a COPD susceptibility gene. Am J Respir Crit Care Med 2010;182:605-613.
20. Wang Y, Ghosh G, Hendrickson EA. Ku86 represses lethal telomere deletion events in human somatic cells. Proc Natl Acad Sci U S A 2009;106:12430-12435.
21. Chen Z, Trotman LC, Shaffer D, Lin HK, Dotan ZA, Niki M, Koutcher JA, Scher HI, Ludwig T, Gerald W, et al. Crucial role of p53-dependent cellular senescence in suppression of PTEN-deficient tumorigenesis. Nature 2005;436:725-730. (Pubitemid 41117277)
22. Caramori G, Adcock IM, Casolari P, Ito K, Jazrawi E, Tsaprouni L, Villetti G, Civelli M, Carnini C, Chung KF, et al. Unbalanced oxidant-induced DNA damage and repair in COPD: a link towards lung cancer. Thorax 2011;66:521-527.
23. Siganaki M, Koutsopoulos AV, Neofytou E, Vlachaki E, Psarrou M, Soulitzis N, Pentilas N, Schiza S, Siafakas NM, Tzortzaki EG. Deregulation of apoptosis mediators' p53 and bcl2 in lung tissue of COPD patients. Respir Res 2010;11:46.
24. Savale L, Chaouat A, Bastuji-Garin S, Marcos E, Boyer L, Maitre B, Sarni M, Housset B, Weitzenblum E, Matrat M, et al. Shortened telomeres in circulating leukocytes of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2009;179:566-571.
25. Xue J, Duncan SR. Are telomere lengths of leukocytes from patients with pulmonary fibrosis really genetically determined? Am J Respir Crit Care Med 2009;179:852, author reply 852-853.
26. Boulton SJ, Jackson SP. Components of the ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J 1998;17:1819-1828. (Pubitemid 28119135)
27. Tsuji T, Aoshiba K, Nagai A. Alveolar cell senescence in patients with pulmonary emphysema. Am J Respir Crit Care Med 2006;174:886-893. (Pubitemid 44564788)
28. Deslee G, Woods JC, Moore C, Conradi SH, Gierada DS, Atkinson JJ, Battaile JT, Liu L, Patterson GA, Adair-Kirk TL, et al. Oxidative damage to nucleic acids in severe emphysema. Chest 2009;135:965-974.
29. Deslee G, Adair-Kirk TL, Betsuyaku T, Woods JC, Moore CH, Gierada DS, Conradi SH, Atkinson JJ, Toennies HM, Battaile JT, et al. Cigarette smoke induces nucleic-acid oxidation in lung fibroblasts. Am J Respir Cell Mol Biol 2010;43:576-584.
30. Alder JK, Guo N, Kembou F, Parry EM, Anderson CJ, Gorgy AI, Walsh MF, Sussan T, Biswal S, Mitzner W, et al. Telomere length is a determinant of emphysema susceptibility. Am J Respir Crit Care Med 2011; 184:904-912.
31. 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 2011;6:209-217.
32. Tuder RM, Kern JA, Miller YE. Senescence in chronic obstructive pulmonary disease. Proc Am Thorac Soc 2012;9:62-63.
33. Cress WD. E2f1: a new role in the DNA damage response. Cell Cycle 2011;10:1718.
34. Chen ZH, Kim HP, Sciurba FC, Lee SJ, Feghali-Bostwick C, Stolz DB, Dhir R, Landreneau RJ, Schuchert MJ, Yousem SA, et al. Egr-1 regulates autophagy in cigarette smoke-induced chronic obstructive pulmonary disease. PLoS ONE 2008;3:e3316.
35. Chen ZH, Lam HC, Jin Y, Kim HP, Cao J, Lee SJ, Ifedigbo E, Parameswaran H, Ryter SW, Choi AM. Autophagy protein microtubule-associated protein 1 light chain-3b (lc3b) activates extrinsic apoptosis during cigarette smoke-induced emphysema. Proc Natl Acad Sci USA 2010;107:18880-18885.
36. Gupta D, Harvey SA, Kaminski N, Swamynathan SK. Mouse conjunctival forniceal gene expression during postnatal development and its regulation by Kruppel-like factor 4. Invest Ophthalmol Vis Sci 2011; 52:4951-4962.
37. Feghali-Bostwick CA, Tsai CG, Valentine VG, Kantrow S, Stoner MW, Pilewski JM, Gadgil A, George MP, Gibson KF, Choi AM, et al. Cellular and humoral autoreactivity in idiopathic pulmonary fibrosis. J Immunol 2007;179:2592-2599.
38. Ning W, Lee J, Kaminski N, Feghali-Bostwick CA, Watkins SC, Pilewski JM, Peters DG, Hogg JC, Choi AM. Comprehensive analysis of gene expression on gold-2 versus gold-0 smokers reveals novel genes important in the pathogenesis of COPD. Proc Am Thorac Soc 2006;3:466. (Pubitemid 44285513)
39. Delerive P, Chin WW, Suen CS. Identification of reverb(alpha) as a novel ror(alpha) target gene. J Biol Chem 2002;277:35013-35018.
40. Lau P, Nixon SJ, Parton RG, Muscat GE. Roralpha regulates the expression of genes involved in lipid homeostasis in skeletal muscle cells: caveolin-3 and CPT-1 are direct targets of ror. J Biol Chem 2004; 279:36828-36840. (Pubitemid 39129032)
41. Dussault I, Fawcett D, Matthyssen A, Bader JA, Giguere V. Orphan nuclear receptor ror alpha-deficient mice display the cerebellar defects of staggerer. Mech Dev 1998;70:147-153. (Pubitemid 28116489)
42. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001;98:5116-5121. (Pubitemid 32397092)
43. Essers J, van Steeg H, de Wit J, Swagemakers SM, Vermeij M, Hoeijmakers JH, Kanaar R. Homologous and non-homologous recombination differentially affect DNA damage repair in mice. EMBO J 2000;19:1703-1710. (Pubitemid 30182176)
44. Hickson I, Zhao Y, Richardson CJ, Green SJ, Martin NM, Orr AI, Reaper PM, Jackson SP, Curtin NJ, Smith GC. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res 2004;64:9152-9159. (Pubitemid 39665530)
45. Kasahara Y, Tuder RM, Taraseviciene-Stewart L, Le Cras TD, Abman S, Hirth PK, Waltenberger J, Voelkel NF. Inhibition of VEGF receptors causes lung cell apoptosis and emphysema. J Clin Invest 2000;106:1311-1319.
46. Vousden KH. Functions of p53 in metabolism and invasion. Biochem Soc Trans 2009;37:511-517.
47. Yan X, Polo Carbayo JJ, Weibel ER, Hsia CC. Variation of lung volume after fixation when measured by immersion or cavalieri method. Am J Physiol Lung Cell Mol Physiol 2003;284:L242-L245. (Pubitemid 35471277)
48. Mandavilli BS, Ali SF, Van Houten B. DNA damage in brain mitochondria caused by aging and MPTP treatment. Brain Res 2000;885:45-52.
49. Haugen AC, Di Prospero NA, Parker JS, Fannin RD, Chou J, Meyer JN, Halweg C, Collins JB, Durr A, Fischbeck K, et al. Altered gene expression and DNA damage in peripheral blood cells from Friedreich's ataxia patients: cellular model of pathology. PLoS Genet 2010;6:e1000812.
50. Morissette MC, Vachon-Beaudoin G, Parent J, Chakir J, Milot J. Increased p53 level, bax/bcl-x(l) ratio, and trail receptor expression in human emphysema. Am J Respir Crit Care Med 2008;178:240-247.
51. Tyner SD, Venkatachalam S, Choi J, Jones S, Ghebranious N, Igelmann H, Lu X, Soron G, Cooper B, Brayton C, et al. P53 mutant mice that display early ageing-associated phenotypes. Nature 2002;415:45-53. (Pubitemid 34062443)
52. Rass U, Ahel I, West SC. Defective DNA repair and neurodegenerative disease. Cell 2007;130:991-1004. (Pubitemid 47410275)
53. Lee JM, Kim IS, Kim H, Lee JS, Kim K, Yim HY, Jeong J, Kim JH, Kim JY, Lee H, et al. Roralpha attenuates wnt/beta-catenin signaling by pkcalpha-dependent phosphorylation in colon cancer. Mol Cell 2010; 37:183-195.
54. Zhu Y, McAvoy S, Kuhn R, Smith DI. Rora, a large common fragile site gene, is involved in cellular stress response. Oncogene 2006;25:2901-2908. (Pubitemid 43739240)