SIRT1 protects against emphysema via FOXO3-mediated reduction of premature senescence in mice

Journal of Clinical Investigation

Volumn 122, Issue 6, 2012, Pages 2032-2045

  Yao, Hongwei ^a   Chung, Sangwoon ^a   Hwang, Jae Woong ^a   Rajendrasozhan, Saravanan ^a   Sundar, Isaac K ^a   Dean, David A ^a   McBurney, Michael W ^b   Guarente, Leonard ^c   Gu, Wei ^d   Rönty, Mikko ^e   Kinnula, Vuokko L ^e   Rahman, Irfan ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d Och Spine at New York Presbyterian Hospitals   (United States)

^e UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

CIGARETTE SMOKE; ELASTASE; I KAPPA B KINASE INHIBITOR; SIRTUIN 1; TRANSCRIPTION FACTOR FKHRL1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CHRONIC OBSTRUCTIVE LUNG DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; DEACETYLATION; EXERCISE TOLERANCE; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; LUNG EMPHYSEMA; LUNG FUNCTION; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; SENESCENCE;

ACETYLATION; ANIMALS; CELL AGING; ENZYME ACTIVATORS; FORKHEAD TRANSCRIPTION FACTORS; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HUMANS; INFLAMMATION; MICE; MICE, KNOCKOUT; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; PULMONARY EMPHYSEMA; RESPIRATORY MUCOSA; SIRTUIN 1;

EID: 84861831957     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI60132     Document Type: Article

References (89)

1. MacNee W, Tuder RM. New paradigms in the pathogenesis of chronic obstructive pulmonary disease I. Proc Am Thorac Soc. 2009;6(6):527-531.
2. Karrasch S, Holz O, Jorres RA. Aging and induced senescence as factors in the pathogenesis of lung emphysema. Respir Med. 2008;102(9):1215-1230.
3. Tsuji T, Aoshiba K, Nagai A. Alveolar cell senescence in patients with pulmonary emphysema. Am J Respir Crit Care Med. 2006;174(8):886-893. (Pubitemid 44564788)
4. Han MK, et al. Chronic obstructive pulmonary disease phenotypes: the future of COPD. Am J Respir Crit Care Med. 2010;182(5):598-604.
5. Yao H, Rahman I. Current concepts on oxidative/carbonyl stress, inflammation and epigenetics in pathogenesis of chronic obstructive pulmonary disease. Toxicol Appl Pharmacol. 2011;254(2):72-85.
6. Leibiger IB, Berggren PO. Sirt1: a metabolic master switch that modulates lifespan. Nat Med. 2006; 12(1):34-36. (Pubitemid 43050055)
7. Chung S, Yao H, Caito S, Hwang JW, Arunachalam G, Rahman I. Regulation of SIRT1 in cellular functions: role of polyphenols. Arch Biochem Biophys. 2010;501(1):79-90.
8. Donmez G, Guarente L. Aging and disease: connections to sirtuins. Aging Cell. 2010;9(2):285-290.
9. Zhang J, et al. The type III histone deacetylase Sirt1 is essential for maintenance of T cell tolerance in mice. J Clin Invest. 2009;119(10):3048-3058.
10. Yuan J, Pu M, Zhang Z, Lou Z. Histone H3-K56 acetylation is important for genomic stability in mammals. Cell Cycle. 2009;8(11):1747-1753.
11. Brunet A, et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science. 2004;303(5666):2011-2015. (Pubitemid 38393275)
12. Dang W, et al. Histone H4 lysine 16 acetylation regulates cellular lifespan. Nature. 2009; 459(7248):802-807.
13. Willcox BJ, et al. FOXO3A genotype is strongly associated with human longevity. Proc Natl Acad Sci U S A. 2008;105(37):13987-13992.
14. Kyoung Kim H, et al. Down-regulation of a forkhead transcription factor, FOXO3a, accelerates cellular senescence in human dermal fibroblasts. J Gerontol A Biol Sci Med Sci. 2005;60(1):4-9.
15. Dentice M, et al. The FoxO3/type 2 deiodinase pathway is required for normal mouse myogenesis and muscle regeneration. J Clin Invest. 2010; 120(11):4021-4030.
16. Sengupta A, Molkentin JD, Paik JH, DePinho RA, Yutzey KE. FoxO transcription factors promote cardiomyocyte survival upon induction of oxidative stress. J Biol Chem. 2011;286(9):7468-7478.
17. Nakamaru Y, et al. A protein deacetylase SIRT1 is a negative regulator of metalloproteinase-9. FASEB J. 2009;23(9):2810-2819.
18. Rajendrasozhan S, Yang SR, Kinnula VL, Rahman I. SIRT1, an antiinflammatory and antiaging protein, is decreased in lungs of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2008;177(8):861-870. (Pubitemid 351600664)
19. Savale L, et al. Shortened telomeres in circulating leukocytes of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2009; 179(7):566-571.
20. Mui TS, et al. Telomere length and chronic obstructive pulmonary disease: evidence of accelerated aging. J Am Geriatr Soc. 2009;57(12):2372-2374.
21. Lambers C, et al. T cell senescence and contraction of T cell repertoire diversity in patients with chronic obstructive pulmonary disease. Clin Exp Immunol. 2009;155(3):466-475.
22. Nyunoya T, Monick MM, Klingelhutz A, Yarovinsky TO, Cagley JR, Hunninghake GW. Cigarette smoke induces cellular senescence. Am J Respir Cell Mol Biol. 2006;35(6):681-688. (Pubitemid 44901857)
23. Muller KC, et al. Lung fibroblasts from patients with emphysema show markers of senescence in vitro. Respir Res. 2006;7:32.
24. Tsuji T, Aoshiba K, Nagai A. Cigarette smoke induces senescence in alveolar epithelial cells. Am J Respir Cell Mol Biol. 2004;31(6):643-649. (Pubitemid 39587494)
25. Hara H, et al. Involvement of creatine kinase B in cigarette smoke-induced bronchial epithelial cell senescence. Am J Respir Cell Mol Biol. 2012;46(3):306-312.
26. McBurney MW, et al. The mammalian SIR2alpha protein has a role in embryogenesis and gametogenesis. Mol Cell Biol. 2003;23(1):38-54. (Pubitemid 36008499)
27. Bordone L, et al. SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell. 2007;6(6):759-767. (Pubitemid 350131044)
28. Oga T, Nishimura K, Tsukino M, Sato S, Hajiro T, Mishima M. Exercise capacity deterioration in patients with COPD: longitudinal evaluation over 5 years. Chest. 2005;128(1):62-69. (Pubitemid 40994455)
29. Li H, Rajendran GK, Liu N, Ware C, Rubin BP, Gu Y. SirT1 modulates the estrogen-insulin-like growth factor-1 signaling for postnatal development of mammary gland in mice. Breast Cancer Res. 2007;9(1):R1.
30. Simon DM, et al. Epithelial cell PPAR[gamma] contributes to normal lung maturation. FASEB J. 2006;20(9):1507-1509.
31. Schug TT, et al. Myeloid deletion of SIRT1 induces inflammatory signaling in response to environmental stress. Mol Cell Biol. 2010;30(19):4712-4721.
32. Giannakou ME, Partridge L. The interaction between FOXO and SIRT1: tipping the balance towards survival. Trends Cell Biol. 2004;14(8):408-412. (Pubitemid 39092697)
33. Tsuji T, Aoshiba K, Nagai A. Alveolar cell senescence exacerbates pulmonary inflammation in patients with chronic obstructive pulmonary disease. Respiration. 2010;80(1):59-70.
34. Yao H, et al. Disruption of p21 attenuates lung inflammation induced by cigarette smoke, LPS, and fMLP in mice. Am J Respir Cell Mol Biol. 2008; 39(1):7-18. (Pubitemid 351883953)
35. Yeung F, et al. Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 2004;23(12):2369-2380. (Pubitemid 38954844)
36. Di Stefano A, et al. Increased expression of nuclear factor-kappaB in bronchial biopsies from smokers and patients with COPD. Eur Respir J. 2002; 20(3):556-563.
37. Yang SR, Wright J, Bauter M, Seweryniak K, Kode A, Rahman I. Sirtuin regulates cigarette smoke-induced proinflammatory mediator release via RelA/p65 NF-kappaB in macrophages in vitro and in rat lungs in vivo: implications for chronic inflammation and aging. Am J Physiol Lung Cell Mol Physiol. 2007;292(2):L567-L576.
38. Caito S, et al. SIRT1 is a redox-sensitive deacetylase that is post-translationally modified by oxidants and carbonyl stress. FASEB J. 2010;24(9):3145-3159.
39. Braidy N, Guillemin GJ, Mansour H, Chan-Ling T, Poljak A, Grant R. Age related changes in NAD+ metabolism oxidative stress and Sirt1 activity in wistar rats. PLoS One. 2011;6(4):e19194.
40. Yao H, et al. Extracellular superoxide dismutase protects against pulmonary emphysema by attenuating oxidative fragmentation of ECM. Proc Natl Acad Sci U S A. 2010;107(35):15571-15576.
41. Vanoirbeek JA, et al. Noninvasive and invasive pulmonary function in mouse models of obstructive and restrictive respiratory diseases. Am J Respir Cell Mol Biol. 2010;42(1):96-104.
42. McDonough JE, et al. Small-airway obstruction and emphysema in chronic obstructive pulmonary disease. N Engl J Med. 2011;365(17):1567-1575.
43. Irvin CG, Bates JH. Measuring the lung function in the mouse: the challenge of size. Respir Res. 2003;4:4.
44. Rangasamy T, et al. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest. 2004;114(9):1248-1259. (Pubitemid 40385296)
45. Guerassimov A, et al. The development of emphysema in cigarette smoke-exposed mice is strain dependent. Am J Respir Crit Care Med. 2004;170(9):974-980. (Pubitemid 39425693)
46. Han W, Dong Z, Dimitropoulou C, Su Y. Hydrogen sulfide ameliorates tobacco smoke-induced oxidative stress and emphysema in mice. Antioxid Redox Signal. 2011;15(8):2121-2134.
47. Yoshida T, et al. Rtp801, a suppressor of mTOR signaling, is an essential mediator of cigarette smoke-induced pulmonary injury and emphysema. Nat Med. 2010;16(7):767-773.
48. Clauss M, et al. Lung endothelial monocyte-activating protein 2 is a mediator of cigarette smoke-induced emphysema in mice. J Clin Invest. 2011; 121(6):2470-2479.
49. Hegab AE, et al. Intranasal HGF administration ameliorates the physiologic and morphologic changes in lung emphysema. Mol Ther. 2008;16(8):1417-1426.
50. Iizuka T, et al. Nrf2-deficient mice are highly susceptible to cigarette smoke-induced emphysema. Genes Cells. 2005;10(12):1113-1125. (Pubitemid 41830071)
51. Hwang JW, et al. FOXO3 deficiency leads to increased susceptibility to cigarette smoke-induced inflammation, airspace enlargement, and chronic obstructive pulmonary disease. J Immunol. 2011;187(2):987-998.
52. Aoshiba K, Nagai A. Senescence hypothesis for the pathogenetic mechanism of chronic obstructive pulmonary disease. Proc Am Thorac Soc. 2009; 6(7):596-601.
53. Palacios JA, Herranz D, De Bonis ML, Velasco S, Serrano M, Blasco MA. SIRT1 contributes to telomere maintenance and augments global homologous recombination. J Cell Biol. 2010;191(7):1299-1313.
54. Alder JK, et al. Telomere length is a determinant of emphysema susceptibility. Am J Respir Crit Care Med. 2011;184(8):904-912.
55. Koike K, et al. Complete lack of vitamin C intake generates pulmonary emphysema in senescence marker protein-30 knockout mice. Am J Physiol Lung Cell Mol Physiol. 2010;298(6):L784-L792.
56. Afanas'ev I. Reactive oxygen species and age-related genes p66shc, Sirtuin, FOX03, and Klotho in senescence. Oxid Med Cell Longev. 2010;3(2):77-85.
57. Holloway KR, et al. SIRT1 regulates Dishevelled proteins and promotes transient and constitutive Wnt signaling. Proc Natl Acad Sci U S A. 2010; 107(20):9216-9221.
58. Guarani V, et al. Acetylation-dependent regulation of endothelial Notch signalling by the SIRT1 deacetylase. Nature. 2011;473(7346):234-238.
59. Sato T, et al. Senescence marker protein-30 protects mice lungs from oxidative stress, aging, and smoking. Am J Respir Crit Care Med. 2006;174(5):530-537. (Pubitemid 44330545)
60. Suga T, et al. 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. 2000;22(1):26-33. (Pubitemid 30342956)
61. Alcendor RR, et al. Sirt1 regulates aging and resistance to oxidative stress in the heart. Circ Res. 2007; 100(10):1512-1521. (Pubitemid 46834764)
62. Tanno M, et al. Induction of manganese superoxide dismutase by nuclear translocation and activation of SIRT1 promotes cell survival in chronic heart failure. J Biol Chem. 2010;285(11):8375-8382.
63. Kops GJ, et al. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature. 2002;419(6904):316-321.
64. He W, et al. Sirt1 activation protects the mouse renal medulla from oxidative injury. J Clin Invest. 2010; 120(4):1056-1068.
65. You H, Yamamoto K, Mak TW. Regulation of transactivation-independent proapoptotic activity of p53 by FOXO3a. Proc Natl Acad Sci U S A. 2006; 103(24):9051-9056. (Pubitemid 43902531)
66. You H, et al. p53-dependent inhibition of FKHRL1 in response to DNA damage through protein kinase SGK1. Proc Natl Acad Sci U S A. 2004; 101(39):14057-14062. (Pubitemid 39305029)
67. Petrache I, et al. Ceramide upregulation causes pulmonary cell apoptosis and emphysema-like disease in mice. Nat Med. 2005;11(5):491-498. (Pubitemid 40685971)
68. Arunachalam G, Yao H, Sundar IK, Caito S, Rahman I. SIRT1 regulates oxidant- and cigarette smoke-induced eNOS acetylation in endothelial cells: Role of resveratrol. Biochem Biophys Res Commun. 2010;393(1):66-72.
69. Hwang JW, et al. Cigarette smoke-induced autophagy is regulated by SIRT1-PARP-1-dependent mechanism: implication in pathogenesis of COPD. Arch Biochem Biophys. 2010;500(2):203-209.
70. Sequeira J, et al. sirt1-null mice develop an autoimmune-like condition. Exp Cell Res. 2008; 314(16):3069-3074.
71. Rahman I, Kinnula VL, Gorbunova V, Yao H. SIRT1 as a therapeutic target in inflammaging of the pulmonary disease [published online ahead of print December 8, 2011]. Prev Med. doi:10.1016/j.ypmed.2011.11.014.
72. Freund A, Orjalo AV, Desprez PY, Campisi J. Inflammatory networks during cellular senescence: causes and consequences. Trends Mol Med. 2010; 16(5):238-246.
73. Acosta JC, et al. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell. 2008; 133(6):1006-1018. (Pubitemid 351795610)
74. Xue W, et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature. 2007;445(7128):656-660. (Pubitemid 46232886)
75. Foronjy R, et al. Transgenic expression of matrix metalloproteinase-9 causes adult-onset emphysema in mice associated with the loss of alveolar elastin. Am J Physiol Lung Cell Mol Physiol. 2008; 294(6):L1149-L1157.
76. Lanone S, et al. Overlapping and enzyme-specific contributions of matrix metalloproteinases-9 and -12 in IL-13-induced inflammation and remodeling. J Clin Invest. 2002;110(4):463-474. (Pubitemid 34919700)
77. Westphal CH, Dipp MA, Guarente L. A therapeutic role for sirtuins in diseases of aging? Trends Biochem Sci. 2007;32(12):555-560. (Pubitemid 350123051)
78. Castrillon DH, Miao L, Kollipara R, Horner JW, DePinho RA. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science. 2003;301(5630):215-218. (Pubitemid 36858475)
79. Yao H, et al. Cigarette smoke-mediated inflammatory and oxidative responses are strain-dependent in mice. Am J Physiol Lung Cell Mol Physiol. 2008;294(6):L1174-L1186.
80. Foronjy RF, et al. Superoxide dismutase expression attenuates cigarette smoke- or elastase-generated emphysema in mice. Am J Respir Crit Care Med. 2006; 173(6):623-631. (Pubitemid 43363803)
81. Kim SR, et al. Involvement of sirtuin 1 in airway inflammation and hyperresponsiveness of allergic airway disease. J Allergy Clin Immunol. 2010; 125(2):449-460.
82. Milne JC, et al. Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature. 2007;450(7170):712-716. (Pubitemid 350207685)
83. Ota H, et al. Sirt1 inhibitor, Sirtinol, induces senescence-like growth arrest with attenuated Ras-MAPK signaling in human cancer cells. Oncogene. 2006; 25(2):176-185. (Pubitemid 43083679)
84. Rajendrasozhan S, Hwang JW, Yao H, Kishore N, Rahman I. Anti-inflammatory effect of a selective IkappaB kinase-beta inhibitor in rat lung in response to LPS and cigarette smoke. Pulm Pharmacol Ther. 2010;23(3):172-181.
85. Massett MP, Berk BC. Strain-dependent differences in responses to exercise training in inbred and hybrid mice. Am J Physiol Regul Integr Comp Physiol. 2005; 288(4):R1006-R1013. (Pubitemid 40404177)
86. Verhoeven D, Teijaro JR, Farber DL. Pulse-oximetry accurately predicts lung pathology and the immune response during influenza infection. Virology. 2009;390(2):151-156.
87. Yao H, et al. Protein kinase C zeta mediates cigarette smoke/aldehyde- and lipopolysaccharide-induced lung inflammation and histone modifications. J Biol Chem. 2010;285(8):5405-5416.
88. Gary RK, Kindell SM. Quantitative assay of senescence-associated beta-galactosidase activity in mammalian cell extracts. Anal Biochem. 2005;343(2):329-334. (Pubitemid 41074047)
89. Atkinson JJ, Adair-Kirk TL, Kelley DG, Demello D, Senior RM. Clara cell adhesion and migration to extracellular matrix. Respir Res. 2008;9:1.