Influenza A virus-dependent remodeling of pulmonary clock function in a mouse model of COPD

Scientific Reports

Volumn 4, Issue , 2015, Pages

  Sundar, Isaac K ^a   Ahmad, Tanveer ^a   Yao, Hongwei ^a   Hwang, Jae Woong ^a   Gerloff, Janice ^a   Lawrence, B Paige ^a   Sellix, Michael T ^a   Rahman, Irfan ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARNTL PROTEIN, MOUSE; CLOCK PROTEIN, MOUSE; SMOKE; TRANSCRIPTION FACTOR ARNTL; TRANSCRIPTION FACTOR CLOCK;

ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; CIRCADIAN RHYTHM; DEFICIENCY; DISEASE MODEL; EMPHYSEMA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; INFLUENZA A VIRUS; KNOCKOUT MOUSE; LUNG; LUNG FUNCTION TEST; MALE; METABOLISM; MORTALITY; MOUSE; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; PULMONARY FIBROSIS; SMOKE; SURVIVAL ANALYSIS; TOBACCO; VIROLOGY;

ANIMALS; ARNTL TRANSCRIPTION FACTORS; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; CLOCK PROTEINS; DISEASE MODELS, ANIMAL; EMPHYSEMA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; INFLUENZA A VIRUS; LUNG; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; PULMONARY FIBROSIS; RESPIRATORY FUNCTION TESTS; SMOKE; SURVIVAL ANALYSIS; TOBACCO;

EID: 84928958335     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep09927     Document Type: Article

References (82)

1. Traves, S. L., Proud, D. Viral-associated exacerbations of asthma andCOPD. Curr. Opin. Pharmacol. 7, 252-258 (2007).
2. Vestbo, J., et al. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am. J. Respir. Crit. Care Med. 187, 347-365 (2013).
3. De Serres, G., et al. Importance of viral and bacterial infections in chronic obstructive pulmonary disease exacerbations. Journal of clinical virology : the official publication of the Pan. American Society for Clinical Virology 46, 129-133 (2009).
4. Dimopoulos, G., et al. Viral epidemiology of acute exacerbations of chronic obstructive pulmonary disease. Pulm. Pharmacol. Ther. 25, 12-18 (2012).
5. Mallia, P., Johnston, S. L. How viral infections cause exacerbation of airway diseases. Chest 130, 1203-1210 (2006).
6. Papi, A., et al. Infections and airway inflammation in chronic obstructive pulmonary disease severe exacerbations. Am. J. Respir. Crit. Care. Med. 173, 1114-1121 (2006).
7. Mohawk, J. A., Green, C. B., Takahashi, J. S. Central and peripheral circadian clocks in mammals. Annu. Rev. Neurosci. 35, 445-462 (2012).
8. Albrecht, U. Timing to perfection: the biology of central and peripheral circadian clocks. Neuron 74, 246-260 (2012).
9. Dibner, C., Schibler, U., Albrecht, U. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 72, 517-549 (2010).
10. Lamia, K. A., Storch, K. F., Weitz, C. J. Physiological significance of a peripheral tissue circadian clock. Proc. Natl. Acad. Sci. U. S. A. 105, 15172-15177 (2008).
11. Pezuk, P., Mohawk, J. A., Wang, L. A., Menaker, M. Glucocorticoids as entraining signals for peripheral circadian oscillators. Endocrinology 153, 4775-4783 (2012).
12. Korencic, A., et al. Timing of circadian genes in mammalian tissues. Sci. Rep. 4, 5782 (2014).
13. Calverley, P. M., et al. Effect of tiotropium bromide on circadian variation in airflow limitation in chronic obstructive pulmonary disease. Thorax. 58, 855-860 (2003).
14. Spengler, C. M., Shea, S. A. Endogenous circadian rhythm of pulmonary function in healthy humans. Am. J. Respir. Crit. Care Med. 162, 1038-1046 (2000).
15. Connolly, C. K. Diurnal rhythms in airway obstruction. Br. J. Dis. Chest 73, 357-366 (1979).
16. Scheiermann, C., Kunisaki, Y., Frenette, P. S. Circadian control of the immune system. Nat. Rev. Immunol. 13, 190-198 (2013).
17. Scheiermann, C., et al. Adrenergic nerves govern circadian leukocyte recruitment to tissues. Immunity 37, 290-301 (2012).
18. Keller, M., et al. Acircadian clock in macrophages controls inflammatory immune responses. Proc. Natl. Acad. Sci. U. S. A. 106, 21407-21412 (2009).
19. Gibbs, J. E., et al. 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 (2012).
20. Cermakian, N., et al. Crosstalk between the circadian clock circuitry and the immune system. Chronobiol. Int. 30, 870-888 (2013).
21. Curtis, A. M., Bellet, M. M., Sassone-Corsi, P., O'Neill, L. A. Circadian clock proteins and immunity. Immunity 40, 178-186 (2014).
22. Bechtold, D. A., Gibbs, J. E., Loudon, A. S. Circadian dysfunction in disease. Trends Pharmacol. Sci 31, 191-198 (2010).
23. Borsboom, G. J., et al. Diurnal variation in lung function in subgroups from two Dutch populations: consequences for longitudinal analysis. American journal of respiratory and critical care medicine 159, 1163-1171 (1999).
24. Casale, R., Pasqualetti, P. 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; international review of thoracic diseases 64, 251-256 (1997).
25. Petty, T. L. Circadian variations in chronic asthma and chronic obstructive pulmonary disease. Am. J. Med. 85, 21-23 (1988).
26. Tsai, C. L., Brenner, B. E., Camargo, C. A., Jr. Circadian-rhythm differences among emergency department patients with chronic obstructive pulmonary disease exacerbation. Chronobiol. Int. 24, 699-713 (2007).
27. Thomas, A., Petro, W., Konietzko N. The circadian rhythm of ciliary beat frequency of human nasal cilia in probands with healthy lungs and in patients with chronic obstructive lung disease. Includes adrenergic stimulation by terbutaline. Pneumologie 47, 526-530 (1993).
28. Lewis, D. A. Sleep in patients with asthma and chronic obstructive pulmonary disease. Curr. Opin. Pulm. Med. 7, 105-112 (2001).
29. Traylor, Z. P., Aeffner, F., Davis, I. C. Influenza A H1N1 induces declines in alveolar gas exchange in mice consistent with rapid post-infection progression from acute lung injury to ARDS. Influenza and other respiratory viruses 7, 472-479 (2013).
30. Hwang, J. W., Sundar, I. K., Yao, H., Sellix, M. T., Rahman, I. Circadian clock function is disrupted by environmental tobacco/cigarette smoke, leading to lung inflammation and injury via a SIRT1-BMAL1 pathway. FASEB. J 28, 176-194 (2014).
31. Sukumaran, S., Jusko, W. J., Dubois, D. C., Almon, R. R. Light-dark oscillations in the lung transcriptome: implications for lung homeostasis, repair, metabolism, disease, and drug action. Journal of applied physiology 110, 1732-1747 (2011).
32. O'Reilly, M. A., Marr, S. H., Yee, M., McGrath-Morrow, S. A., Lawrence BP. Neonatal hyperoxia enhances the inflammatory response in adult mice infected with influenza A virus. Am. J. Respir. Crit. Care Med. 177, 1103-1110 (2008).
33. Chakravorty, I., Chahal, K., Austin, G. A pilot study of the impact of highfrequency chest wall oscillation in chronic obstructive pulmonary disease patients with mucus hypersecretion. Int. J. Chron. Obstruct. Pulmon. Dis. 6, 693-699 (2011).
34. Marrone, O., Salvaggio, A., Insalaco, G. Respiratory disorders during sleep in chronic obstructive pulmonary disease. Int. J. Chron. Obstruct. Pulmon. Dis. 1, 363-372 (2006).
35. Owens, R. L., Malhotra, A. Sleep-disordered breathing and COPD: the overlap syndrome. Respiratory care 55, 1333-1344 (2010).
36. Parish, J. M. Sleep-related problems in common medical conditions. Chest 135, 563-572 (2009).
37. Sundar, I. K., et al. Serotonin and corticosterone rhythms in mice exposed to cigarette smoke and in patients with COPD: implication for COPD-associated neuropathogenesis. PLoS. One 9, e87999 (2014).
38. Toth, L. A., Hughes, L. F. Macrophage participation in influenza-induced sleep enhancement in C57BL/6J mice. Brain Behav. Immun. 18, 375-389 (2004).
39. Toth, L. A., Verhulst, S. J. Strain differences in sleep patterns of healthy and influenza-infected inbred mice. Behavior genetics 33, 325-336 (2003).
40. Beraki, S., Aronsson, F., Karlsson, H., Ogren, S. O., Kristensson, K. Influenza A virus infection causes alterations in expression of synaptic regulatory genes combined with changes in cognitive and emotional behaviors in mice. Mol. Psychiatry. 10, 299-308 (2005).
41. Marin, J. M., Soriano, J. B., Carrizo, S. J., Boldova, A., Celli BR. Outcomes in patients with chronic obstructive pulmonary disease and obstructive sleep apnea: the overlap syndrome. Am. J. Respir. Crit. Care Med. 182, 325-331 (2010).
42. Ding, M., Toth, L. A. mRNA expression in mouse hypothalamus and basal forebrain during influenza infection: a novel model for sleep regulation. Physiol. Genomics 24, 225-234 (2006).
43. Castanon-Cervantes, O., et al. Dysregulation of inflammatory responses by chronic circadian disruption. J. Immunol. 185, 5796-5805 (2010).
44. Hadden, H., Soldin, S. J., Massaro, D. Circadian disruption alters mouse lung clock gene expression and lung mechanics. Journal of applied physiology 113, 385-392 (2012).
45. Thompson, A. A., Walmsley, S. R., Whyte, M. K. A local circadian clock calls time on lung inflammation. Nat. Med. 20, 809-811 (2014).
46. Silver, A. C., Arjona, A., Walker, W. E., Fikrig, E. The circadian clock controls tolllike receptor 9-mediated innate and adaptive immunity. Immunity 36, 251-261 (2012).
47. Sato, S., et al. ACircadian Clock Gene, Rev-erbalpha, Modulates the Inflammatory Function of Macrophages through the Negative Regulation of Ccl2 Expression. J. Immunol. 192, 407-417 (2014).
48. Spengler, M. L., et al. Core circadian protein CLOCK is a positive regulator of NFkappaB-mediated transcription. Proc. Natl. Acad. Sci. U. S. A. 109, E2457-2465 (2012).
49. Yang, G., et al. Oxidative stress and inflammation modulate Rev-erbalpha signaling in the neonatal lung and affect circadian rhythmicity. Antioxid Redox Signal 21, 17-32 (2014).
50. Bunger, M. K., et al. Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103, 1009-1017 (2000).
51. Kondratov, R. V., Kondratova, A. A., Gorbacheva, V. Y., Vykhovanets, O. V., Antoch, M. P. Early aging and age-related pathologies in mice deficient in BMAL1, the core componentof the circadian clock. Genes. Dev. 20, 1868-1873 (2006).
52. Kondratov, R. V., Vykhovanets, O., Kondratova, A. A., Antoch MP. Antioxidant N-acetyl-L-cysteine ameliorates symptoms of premature aging associated with the deficiency of the circadian protein BMAL1. Aging (Albany NY) 1, 979-987 (2009).
53. Nguyen, K. D., et al. Circadian gene Bmal1 regulates diurnal oscillations of Ly6C(hi) inflammatory monocytes. Science 341, 1483-1488 (2013).
54. Pekovic-Vaughan, V., et al. The circadian clock regulates rhythmic activation of the NRF2/glutathione-mediated antioxidant defense pathway to modulate pulmonary fibrosis. Genes. Dev. 28, 548-560 (2014).
55. Thatcher, T. H., et al. Aryl hydrocarbon receptor-deficient mice develop heightened inflammatory responses to cigarette smoke and endotoxin associated with rapid loss of the nuclear factor-kappaB component RelB. Am. J. Pathol. 170, 855-864 (2007).
56. Yao, H., et al. Cigarette smoke-mediated inflammatory and oxidative responses are strain dependent in mice. Am. J. Physiol. Lung. Cell Mol. Physiol. 294, L1174-L1186 (2008).
57. Han, Y., et al. Influenza virus-induced lung inflammation was modulated by cigarette smoke exposure in mice. PLoS. One 9, e86166 (2014).
58. Gualano, R. C., et al. Cigarette smoke worsens lung inflammation and impairs resolution of influenza infection in mice. Respir. Res. 9, 53 (2008).
59. Yageta, Y., et al. Carbocisteine reduces virus-induced pulmonary inflammation in mice exposed to cigarette smoke. Am J. Respir. Cell Mol. Biol. 50, 963-973 (2014).
60. Yageta, Y., et al. Role of Nrf2 in host defense against influenza virus in cigarette smoke-exposed mice. Journal of virology 85, 4679-4690 (2011).
61. Yao, H., et al. Genetic ablation of NADPH oxidase enhances susceptibility to cigarette smoke-induced lung inflammation and emphysema in mice. Am. J. Pathol. 172, 1222-1237 (2008).
62. Gibbs, J., et al. An epithelial circadian clock controls pulmonary inflammation and glucocorticoid action. Nat. Med. 20, 919-926 (2014).
63. Ferraz, E., Borges, M. C., Terra-Filho, J., Martinez, J. A., Vianna, E. O. Comparison of 4 AMand 4 PMbronchial responsiveness to hypertonic saline in asthma. Lung. 184, 341-346 (2006).
64. Burioka, N., et al. Circadian rhythms in the CNS and peripheral clock disorders: function of clock genes: influence of medication for bronchial asthma on circadian gene. Journal of pharmacological sciences 103, 144-149 (2007).
65. Durrington, H. J, Farrow, S. N., Loudon, A. S., Ray, D. W. The circadian clock and asthma. Thorax 69, 90-92 (2014).
66. Kang, M. J., et al. Cigarette smoke selectively enhances viral PAMP-and virus-induced pulmonary innate immune and remodeling responses in mice. J. Clin. Invest. 118, 2771-2784 (2008).
67. Beckett, E. L., et al. A new short-term mouse model of chronic obstructive pulmonary disease identifies a role for mast cell tryptase in pathogenesis. J. Allergy Clin. Immunol. 131, 752-762 (2013).
68. Zhou, Y., et al. Role of ribonuclease L in viral pathogen-associated molecular pattern/influenza virus and cigarette smoke-induced inflammation and remodeling. J. Immunol. 191, 2637-2646 (2013).
69. Kimura, G., et al. Toll-like receptor 3 stimulation causes corticosteroid-refractory airway neutrophilia and hyperresponsiveness in mice. Chest 144, 99-105 (2013).
70. Robbins, C. S., et al. Cigarette smoke impacts immune inflammatory responses to influenza in mice. Am. J. Respir. Crit. Care Med. 174, 1342-1351 (2006).
71. Wortham, B. W., et al. NKG2D mediates NK cell hyperresponsiveness and influenza-induced pathologies in a mouse model of chronic obstructive pulmonary disease. J. Immunol. 188, 4468-4475 (2012).
72. Haspel, J. A., et al. Circadian rhythm reprogramming during lung inflammation. Nat. Commun. 5, 4753 (2014).
73. Sujino, M., et al. Differential entrainment of peripheral clocks in the rat by glucocorticoid and feeding. Endocrinology 153, 2277-2286 (2012).
74. Yao, H., et al. SIRT1 protects against emphysema via FOXO3-mediated reduction of premature senescence in mice. J. Clin. Invest. 122, 2032-2045 (2012).
75. Yao, H., et al. Extracellular superoxide dismutase protects against pulmonary emphysema by attenuating oxidative fragmentation of ECM. Proc. Natl. Acad. Sci. U. S. A. 107, 15571-15576 (2010).
76. Buczynski, B. W., Yee, M., Martin, K. C., Lawrence, B. P., O'Reilly, M. A. Neonatal hyperoxia alters the host response to influenza A virus infection in adult mice throughmultiple pathways. Am J. Physiol. Lung. Cell Mol. Physiol. 305, L282-290 (2013).
77. Yoo, S. H., et al. 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 (2004).
78. Mortola, J. P., Seifert EL. Circadian patterns of breathing. Respir. Physiol. Neurobiol. 131, 91-100 (2002).
79. Sundar, I. K., Hwang, J. W., Wu, S., Sun, J., Rahman, I. Deletion of vitamin D receptor leads to premature emphysema/COPD by increased matrix met alloproteinases and lymphoid aggregates formation. Biochem. Biophys. Res. Commun. 406, 127-133 (2011).
80. Ashcroft, T., Simpson, J. M., Timbrell, V. Simple method of estimating severity of pulmonary fibrosis on a numerical scale. Journal of clinical pathology 41, 467-470 (1988).
81. Foronjy, R. F., et al. Structural emphysema does not correlate with lung compliance: lessons from the mouse smoking model. Exp. Lung. Res. 31, 547-562 (2005).
82. Oster, H., Damerow, S., Hut, R. A., Eichele, G. Transcriptional profiling in the adrenal gland reveals circadian regulation of hormone biosynthesis genes and nucleosome assembly genes. J. Biol. Rhythms 21, 350-361 (2006).