Circadian clock function is disrupted by environmental tobacco/cigarette smoke, leading to lung inflammation and injury via a SIRT1-BMAL1 pathway

FASEB Journal

Volumn 28, Issue 1, 2014, Pages 176-194

  Hwang, Jae Woong ^a   Sundar, Isaac K ^a   Yao, Hongwei ^a   Sellix, Michael T ^a   Rahman, Irfan ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Chronic obstructive pulmonary disease; Cytokines; Emphysema; Locomotor activity; Mouse; Oxidative stress

Indexed keywords

ANTIINFLAMMATORY AGENT; CIGARETTE SMOKE; CRYPTOCHROME 1; CRYPTOCHROME 2; NUCLEAR RECEPTOR NR1D1; PER1 PROTEIN; PER2 PROTEIN; PROTEIN BMAL1; SIRTUIN 1; SRT 1720; TOBACCO SMOKE; TRANSCRIPTION FACTOR CLOCK; UNCLASSIFIED DRUG; ARNTL PROTEIN, MOUSE; CYTOKINE; SIRT1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR ARNTL;

ACETYLATION; ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CIRCADIAN RHYTHM; CONTROLLED STUDY; CYTOKINE RELEASE; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVATION; GENE DELETION; GENE EXPRESSION; HUMAN; HUMAN TISSUE; LOCOMOTION; LONG TERM EXPOSURE; LUNG ALVEOLUS EPITHELIUM; LUNG EMPHYSEMA; LUNG FUNCTION; LUNG INJURY; LUNG LAVAGE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PNEUMONIA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; SURVIVAL RATE; ANIMAL; BRAIN; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; EMPHYSEMA; IN VITRO STUDY; LUNG; METABOLISM; MOTOR ACTIVITY; PASSIVE SMOKING;

CHRONIC OBSTRUCTIVE PULMONARY DISEASE; CYTOKINES; EMPHYSEMA; LOCOMOTOR ACTIVITY; MOUSE; OXIDATIVE STRESS;

ANIMALS; ARNTL TRANSCRIPTION FACTORS; BRAIN; HUMANS; LUNG; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; SIRTUIN 1; TOBACCO SMOKE POLLUTION;

EID: 84894521804     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-232629     Document Type: Article

References (70)

1. Mohawk, J. A., Green, C. B., and Takahashi, J. S. (2012) Central and peripheral circadian clocks in mammals. Annu. Rev. Neurosci. 35, 445-462
2. Dibner, C., Schibler, U., and Albrecht, U. (2010) The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 72, 517-549
3. Bechtold, D. A., Gibbs, J. E., and Loudon, A. S. (2010) Circadian dysfunction in disease. Trends Pharmacol. Sci. 31, 191-198
4. Mortola, J. P., and Seifert, E. L. (2002) Circadian patterns of breathing. Respir. Physiol. Neurobiol. 131, 91-100
5. Hadden, H., Soldin, S. J., and Massaro, D. (2012) Circadian disruption alters mouse lung clock gene expression and lung mechanics. J. Appl. Physiol. 113, 385-392
6. Boysen, P. G., Block, A. J., Wynne, J. W., Hunt, L. A., and Flick, M. R. (1979) Nocturnal pulmonary hypertension in patients with chronic obstructive pulmonary disease. Chest 76, 536-542
7. Spengler, C. M., and Shea, S. A. (2000) Endogenous circadian rhythm of pulmonary function in healthy humans. Am. J. Respir. Crit. Care Med. 162, 1038-1046
8. Sukumaran, S., Jusko, W. J., Dubois, D. C., and Almon, R. R. (2011) Light-dark oscillations in the lung transcriptome: implications for lung homeostasis, repair, metabolism, disease, and drug action. J. Appl. Physiol. 110, 1732-1747
9. Fu, L., Pelicano, H., Liu, J., Huang, P., and Lee, C. (2002) The circadian gene Period2 plays an important role in tumor suppression and DNA damage response in vivo. Cell 111, 41-50
10. Zheng, X., Yang, Z., Yue, Z., Alvarez, J. D., and Sehgal, A. (2007) FOXO and insulin signaling regulate sensitivity of the circadian clock to oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 104, 15899-15904
11. Khapre, R. V., Kondratova, A. A., Susova, O., and Kondratov, R. V. (2011) Circadian clock protein BMAL1 regulates cellular senescence in vivo. Cell Cycle 10, 4162-4169
12. Yao, H., and Rahman, I. (2011) Current concepts on oxidative/ carbonyl stress, inflammation and epigenetics in pathogenesis of chronic obstructive pulmonary disease. Toxicol. Appl. Pharmacol. 254, 72-85
13. Hoegh, S. V., Sorensen, G. L., Tornoe, I., Lottenburger, T., Ytting, H., Nielsen, H. J., Junker, P., and Holmskov, U. (2010) Long-term stability and circadian variation in circulating levels of surfactant protein D. Immunobiology 215, 314-320
14. Thomas, A., Petro, W., and Konietzko, N. (1993) [The circadian rhythm of ciliary beat frequency of human nasal cilia in pro- bands with healthy lungs and in patients with chronic obstructive lung disease: includes adrenergic stimulation by terbutaline]. Pneumologie 47, 526-530; German
15. Gebel, S., Gerstmayer, B., Kuhl, P., Borlak, J., Meurrens, K., and Muller, T. (2006) The kinetics of transcriptomic changes induced by cigarette smoke in rat lungs reveals a specific program of defense, inflammation, and circadian clock gene expression. Toxicol. Sci. 93, 422-431
16. Gibbs, J. E., Beesley, S., Plumb, J., Singh, D., Farrow, S., Ray, D. W., and Loudon, A. S. (2009) Circadian timing in the lung: a specific role for bronchiolar epithelial cells. Endocrinology 150, 268-276
17. Casale, R., and Pasqualetti, P. (1997) Cosinor analysis of circadian peak expiratory flow variability in normal subjects, passive smokers, heavy smokers, patients with chronic obstructive pulmonary disease and patients with interstitial lung disease. Respiration 64, 251-256
18. Petty, T. L. (1988) Circadian variations in chronic asthma and chronic obstructive pulmonary disease. Am. J. Med. 85, 21-23
19. Tsai, C. L., Brenner, B. E., and Camargo, C. A., Jr. (2007) Circadian-rhythm differences among emergency department patients with chronic obstructive pulmonary disease exacerbation. Chronobiol. Int. 24, 699-713
20. Agusti, A., Hedner, J., Marin, J. M., Barbe, F., Cazzola, M., and Rennard, S. (2011) Night-time symptoms: a forgotten dimension of COPD. Eur. Respir. Rev. 20, 183-194
21. Belden, W. J., and Dunlap, J. C. (2008) SIRT1 is a circadian deacetylase for core clock components. Cell 134, 212-214
22. Imai, S., Armstrong, C. M., Kaeberlein, M., and Guarente, L. (2000) Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403, 795-800
23. Grimaldi, B., Nakahata, Y., Kaluzova, M., Masubuchi, S., and Sassone-Corsi, P. (2009) Chromatin remodeling, metabolism and circadian clocks: the interplay of CLOCK and SIRT1. Int. J. Biochem. Cell Biol. 41, 81-86
24. Asher, G., Gatfield, D., Stratmann, M., Reinke, H., Dibner, C., Kreppel, F., Mostoslavsky, R., Alt, F. W., and Schibler, U. (2008) SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134, 317-328
25. Nakahata, Y., Kaluzova, M., Grimaldi, B., Sahar, S., Hirayama, J., Chen, D., Guarente, L. P., and Sassone-Corsi, P. (2008) The NAD-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell 134, 329-340
26. Rajendrasozhan, S., Yang, S. R., Kinnula, V. L., and Rahman, I. (2008) SIRT1, an antiinflammatory and antiaging protein, is decreased in lungs of patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 177, 861-870
27. Yao, H., Chung, S., Hwang, J. W., Rajendrasozhan, S., Sundar, I. K., Dean, D. A., McBurney, M. W., Guarente, L., Gu, W., Ronty, M., and Rahman, I. (2012) SIRT1 protects against emphysema via FOXO3-mediated reduction of premature senescence in mice. J. Clin. Invest. 122, 2032-2045
28. Yang, S. R., Wright, J., Bauter, M., Seweryniak, K., Kode, A., and Rahman, I. (2007) 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. 292, L567-L576
29. Simon, D. M., Arikan, M. C., Srisuma, S., Bhattacharya, S., Tsai, L. W., Ingenito, E. P., Gonzalez, F., Shapiro, S. D., and Mariani, T. J. (2006) Epithelial cell PPAR contributes to normal lung maturation. FASEB J. 20, 1507-1509
30. McBurney, M. W., Yang, X., Jardine, K., Hixon, M., Boekelheide, K., Webb, J. R., Lansdorp, P. M., and Lemieux, M. (2003) The mammalian SIR2alpha protein has a role in embryogenesis and gametogenesis. Mol. Cell. Biol. 23, 38-54
31. Bordone, L., Cohen, D., Robinson, A., Motta, M. C., van Veen, E., Czopik, A., Steele, A. D., Crowe, H., Marmor, S., Luo, J., Gu, W., and Guarente, L. (2007) SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell 6, 759-767
32. Yao, H., Arunachalam, G., Hwang, J. W., Chung, S., Sundar, I. K., Kinnula, V. L., Crapo, J. D., and Rahman, I. (2010) Extracellular superoxide dismutase protects against pulmonary emphysema by attenuating oxidative fragmentation of ECM. Proc. Natl. Acad. Sci. U. S. A. 107, 15571-15576
33. Yao, H., Edirisinghe, I., Rajendrasozhan, S., Yang, S. R., Caito, S., Adenuga, D., and Rahman, I. (2008) Cigarette smokemediated inflammatory and oxidative responses are straindependent in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 294, L1174-L1186
34. Hwang, J. W., Rajendrasozhan, S., Yao, H., Chung, S., Sundar, I. K., Huyck, H. L., Pryhuber, G. S., Kinnula, V. L., and Rahman, I. (2011) FOXO3 deficiency leads to increased susceptibility to cigarette smoke-induced inflammation, airspace enlargement, and chronic obstructive pulmonary disease. J. Immunol. 187, 987-998
35. Yoon, J. A., Han, D. H., Noh, J. Y., Kim, M. H., Son, G. H., Kim, K., Kim, C. J., Pak, Y. K., and Cho, S. (2012) Meal time shift disturbs circadian rhythmicity along with metabolic and behavioral alterations in mice. PLoS One 7, e44053
36. Yoo, S. H., Yamazaki, S., Lowrey, P. L., Shimomura, K., Ko, C. H., Buhr, E. D., Siepka, S. M., Hong, H. K., Oh, W. J., Yoo, O. J., Menaker, M., and Takahashi, J. S. (2004) Period2: Luciferase real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc. Natl. Acad. Sci. U. S. A. 101, 5339-5346
37. Foronjy, R. F., Mercer, B. A., Maxfield, M. W., Powell, C. A., D'Armiento, J., and Okada, Y. (2005) Structural emphysema does not correlate with lung compliance: lessons from the mouse smoking model. Exp. Lung Res. 31, 547-562
38. Guerassimov, A., Hoshino, Y., Takubo, Y., Turcotte, A., Yamamoto, M., Ghezzo, H., Triantafillopoulos, A., Whittaker, K., Hoidal, J. R., and Cosio, M. G. (2004) The development of emphysema in cigarette smoke-exposed mice is strain dependent. Am. J. Respir. Crit. Care Med. 170, 974-980
39. Oster, H., Damerow, S., Hut, R. A., and Eichele, G. (2006) Transcriptional profiling in the adrenal gland reveals circadian regulation of hormone biosynthesis genes and nucleosome assembly genes. J. Biol. Rhythms 21, 350-361
40. Milne, J. C., Lambert, P. D., Schenk, S., Carney, D. P., Smith, J. J., Gagne, D. J., Jin, L., Boss, O., Perni, R. B., Vu, C. B., Bemis, J. E., Xie, R., Disch, J. S., Ng, P. Y., Nunes, J. J., Lynch, A. V., Yang, H., Galonek, H., Israelian, K., Choy, W., Iffland, A., Lavu, S., Medvedik, O., Sinclair, D. A., Olefsky, J. M., Jirousek, M. R., Elliott, P. J., and Westphal, C. H. (2007) Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 450, 712-716
41. Keller, M., Mazuch, J., Abraham, U., Eom, G. D., Herzog, E. D., Volk, H. D., Kramer, A., and Maier, B. (2009) A circadian clock in macrophages controls inflammatory immune responses. Proc. Natl. Acad. Sci. U. S. A. 106, 21407-21412
42. Logan, R. W., and Sarkar, D. K. (2012) Circadian nature of immune function. Mol. Cell. Endocrinol. 349, 82-90
43. Narasimamurthy, R., Hatori, M., Nayak, S. K., Liu, F., Panda, S., and Verma, I. M. (2012) Circadian clock protein cryptochrome regulates the expression of proinflammatory cytokines. Proc. Natl. Acad. Sci. U. S. A. 109, 12662-12667
44. Castanon-Cervantes, O., Wu, M., Ehlen, J. C., Paul, K., Gamble, K. L., Johnson, R. L., Besing, R. C., Menaker, M., Gewirtz, A. T., and Davidson, A. J. (2010) Dysregulation of inflammatory responses by chronic circadian disruption. J. Immunol. 185, 5796-5805
45. Chen, C. Y., Chow, D., Chiamvimonvat, N., Glatter, K. A., Li, N., He, Y., Pinkerton, K. E., and Bonham, A. C. (2008) Short-term secondhand smoke exposure decreases heart rate variability and increases arrhythmia susceptibility in mice. Am. J. Physiol. Heart Circ. Physiol. 295, H632-H639
46. Gentner, N. J., and Weber, L. P. (2012) Secondhand tobacco smoke, arterial stiffness, and altered circadian blood pressure patterns are associated with lung inflammation and oxidative stress in rats. Am. J. Physiol. Heart Circ. Physiol. 302, H818-H825
47. Vasu, V. T., Cross, C. E., and Gohil, K. (2009) Nr1d1, an important circadian pathway regulatory gene, is suppressed by cigarette smoke in murine lungs. Integr. Cancer Ther. 8, 321-328
48. Silver, A. C., Arjona, A., Walker, W. E., and Fikrig, E. (2012) The circadian clock controls toll-like receptor 9-mediated innate and adaptive immunity. Immunity 36, 251-261
49. Leone, M. J., Marpegan, L., Duhart, J. M., and Golombek, D. A. (2012) Role of proinflammatory cytokines on lipopolysaccharide- induced phase shifts in locomotor activity circadian rhythm. Chronobiol. Int. 29, 715-723
50. Spengler, C. M., and Shea, S. A. (2012) Core circadian protein CLOCK is a positive regulator of NF-kappaB-mediated transcription. Proc. Natl. Acad. Sci. U. S. A. 109, E2457-E2465
51. Yao, H., Edirisinghe, I., Yang, S. R., Rajendrasozhan, S., Kode, A., Caito, S., Adenuga, D., and Rahman, I. (2008) Genetic ablation of NADPH oxidase enhances susceptibility to cigarette smoke-induced lung inflammation and emphysema in mice. Am. J. Pathol. 172, 1222-1237
52. Gibbs, J. E., Blaikley, J., Beesley, S., Matthews, L., Simpson, K. D., Boyce, S. H., Farrow, S. N., Else, K. J., Singh, D., Ray, D. W., and Loudon, A. S. (2012) The nuclear receptor REV-ERBalpha mediates circadian regulation of innate immunity through selective regulation of inflammatory cytokines. Proc. Natl. Acad. Sci. U. S. A. 109, 582-587
53. Murphy, J. M., Horton, N. J., Monson, R. R., Laird, N. M., Sobol, A. M., and Leighton, A. H. (2003) Cigarette smoking in relation to depression: historical trends from the Stirling County Study. Am. J. Psychiatry 160, 1663-1669
54. Mykletun, A., Overland, S., Aaro, L. E., Liabo, H. M., and Stewart, R. (2008) Smoking in relation to anxiety and depression: evidence from a large population survey: the HUNT study. Eur. Psychiatry 23, 77-84
55. Hida, A., Kitamura, S., and Mishima, K. (2012) Pathophysiology and pathogenesis of circadian rhythm sleep disorders. J. Physiol. Anthropol. 31, 7
56. Lewis, D. A. (2001) Sleep in patients with asthma and chronic obstructive pulmonary disease. Curr. Opin. Pulm. Med. 7, 105-112
57. Gierisch, J. M., Bastian, L. A., Calhoun, P. S., McDuffie, J. R., and Williams, J. W., Jr. (2012) Smoking cessation interventions for patients with depression: a systematic review and meta-analysis. J. Gen. Intern. Med. 27, 351-360
58. Antoniu, S. A. (2011) Predictors of depression in chronic obstructive pulmonary disease patients. Expert Rev. Respir. Med. 5, 333-335
59. Divo, M., Cote, C., de Torres, J. P., Casanova, C., Marin, J. M., Pinto-Plata, V., Zulueta, J., Cabrera, C., Zagaceta, J., Hunninghake, G., and Celli, B. (2012) Comorbidities and risk of mortality in patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 186, 155-161
60. Hanania, N. A., Mullerova, H., Locantore, N. W., Vestbo, J., Watkins, M. L., Wouters, E. F., Rennard, S. I., and Sharafkhaneh, A. (2011) Determinants of depression in the ECLIPSE chronic obstructive pulmonary disease cohort. Am. J. Respir. Crit. Care Med. 183, 604-611
61. Laurin, C., Moullec, G., Bacon, S. L., and Lavoie, K. L. (2012) Impact of anxiety and depression on chronic obstructive pulmonary disease exacerbation risk. Am. J. Respir. Crit. Care Med. 185, 918-923
62. Caito, S., Rajendrasozhan, S., Cook, S., Chung, S., Yao, H., Friedman, A. E., Brookes, P. S., and Rahman, I. (2010) SIRT1 is a redox-sensitive deacetylase that is post-translationally modified by oxidants and carbonyl stress. FASEB J. 24, 3145-3159
63. Nakahata, Y., Sahar, S., Astarita, G., Kaluzova, M., and Sassone-Corsi, P. (2009) Circadian control of the NAD salvage pathway by CLOCK-SIRT1. Science 324, 654-657
64. Chang, H. C., and Guarente, L. (2013) SIRT1 mediates central circadian control in the SCN by a mechanism that decays with aging. Cell 153, 1448-1460
65. Cavadini, G., Petrzilka, S., Kohler, P., Jud, C., Tobler, I., Birchler, T., and Fontana, A. (2007) TNF-alpha suppresses the expression of clock genes by interfering with E-box-mediated transcription. Proc. Natl. Acad. Sci. U. S. A. 104, 12843-12848
66. Okada, K., Yano, M., Doki, Y., Azama, T., Iwanaga, H., Miki, H., Nakayama, M., Miyata, H., Takiguchi, S., Fujiwara, Y., Yasuda, T., Ishida, N., and Monden, M. (2008) Injection of LPS causes transient suppression of biological clock genes in rats. J. Surg. Res. 145, 5-12
67. Kwon, I., Lee, J., Chang, S. H., Jung, N. C., Lee, B. J., Son, G. H., Kim, K., and Lee, K. H. (2006) BMAL1 shuttling controls transactivation and degradation of the CLOCK/BMAL1 heterodimer. Mol. Cell. Biol. 26, 7318-7330
68. Tamaru, T., Isojima, Y., van der Horst, G. T., Takei, K., Nagai, K., and Takamatsu, K. (2003) Nucleocytoplasmic shuttling and phosphorylation of BMAL1 are regulated by circadian clock in cultured fibroblasts. Genes Cells 8, 973-983
69. Kondratov, R. V., Kondratova, A. A., Gorbacheva, V. Y., Vykhovanets, O. V., and Antoch, M. P. (2006) Early aging and agerelated pathologies in mice deficient in BMAL1, the core component of the circadian clock. Genes Dev. 20, 1868-1873
70. Bellet, M. M., Nakahata, Y., Boudjelal, M., Watts, E., Mossakowska, D. E., Edwards, K. A., Cervantes, M., Astarita, G., Loh, C., Ellis, J. L., Vlasuk, G. P., and Sassone-Corsi, P. (2013) Pharmacological modulation of circadian rhythms by synthetic activators of the deacetylase SIRT1. Proc. Natl. Acad. Sci. U. S. A. 110, 3333-3338