Oxidative stress and inflammation modulate Rev-erbα signaling in the neonatal lung and affect circadian rhythmicity

Antioxidants and Redox Signaling

Volumn 21, Issue 1, 2014, Pages 17-32

  Yang, Guang ^a   Wright, Clyde J ^b   Hinson, Maurice D ^a   Fernando, Amal P ^a   Sengupta, Shaon ^a   Biswas, Chhanda ^a,c   La, Ping ^a   Dennery, Phyllis A ^a,c  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b University of Colorado Denver and Children s Hospital Colorado   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NUCLEAR RECEPTOR NR1D1; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR NRF2; HYDROGEN PEROXIDE; MESSENGER RNA; NR1D1 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL FUNCTION; CELL METABOLISM; CIRCADIAN RHYTHM; CONSENSUS SEQUENCE; CONTROLLED STUDY; GENE; HYPEROXIA; IN VITRO STUDY; INFLAMMATION; LUNG; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; STIMULUS; ANIMAL; BINDING SITE; C57BL MOUSE; CELL SURVIVAL; COMET ASSAY; DNA DAMAGE; DRUG EFFECTS; GENETICS; METABOLISM; NEWBORN; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; BINDING SITES; CELL SURVIVAL; CELLS, CULTURED; CIRCADIAN RHYTHM; COMET ASSAY; DNA DAMAGE; HYDROGEN PEROXIDE; LUNG; MICE; MICE, INBRED C57BL; NF-KAPPA B; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP D, MEMBER 1; OXIDATIVE STRESS; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84902123997     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5539     Document Type: Article

References (75)

1. Adelmant G, Begue A, Stehelin D, and Laudet V. A functional Rev-erb alpha responsive element located in the human Rev-erb alpha promoter mediates a repressing activity. Proc Natl Acad Sci U S A 93: 3553-3558, 1996.
2. Angelov D, Lenouvel F, Hans F, Muller CW, Bouvet P, Bednar J, Moudrianakis EN, Cadet J, and Dimitrov S. The histone octamer is invisible when NF-kappaB binds to the nucleosome. J Biol Chem 279: 42374-42382, 2004.
3. Auten RL, Mason SN, Auten KM, and Brahmajothi M. Hyperoxia impairs postnatal alveolar epithelial development via NADPH oxidase in newborn mice. Am J Physiol Lung Cell Mol Physiol 297: L134-L142, 2009.
4. Balsalobre A, Damiola F, and Schibler U. A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93: 929-937, 1998.
5. Barker GF, Manzo ND, Cotich KL, Shone RK, and Waxman AB. DNA damage induced by hyperoxia: quantitation and correlation with lung injury. Am J Respir Cell Mol Biol 35: 277-288, 2006.
6. Bhandari V. Molecular mechanisms of hyperoxia-induced acute lung injury. Front Biosci 13: 6653-6661, 2008.
7. Bilodeau JF, Faure R, Piedboeuf B, and Mirault ME. Hyperoxia induces S-phase cell-cycle arrest and p21(Cip1/ Waf1)-independent Cdk2 inhibition in human carcinoma T47D-H3 cells. Exp Cell Res 256: 347-357, 2000.
8. Bookout AL, Jeong Y, Downes M, Yu RT, Evans RM, and Mangelsdorf DJ. Anatomical profiling of nuclear receptor expression reveals a hierarchical transcriptional network. Cell 126: 789-799, 2006.
9. Bozek K, Relogio A, Kielbasa SM, Heine M, Dame C, Kramer A, and Herzel H. Regulation of clock-controlled genes in mammals. PLoS One 4: e4882, 2009.
10. Bugge A, Feng D, Everett LJ, Briggs ER, Mullican SE, Wang F, Jager J, and Lazar MA. Rev-erbalpha and Rev-erbbeta coordinately protect the circadian clock and normal metabolic function. Genes Dev 26: 657-667, 2012.
11. Carmody RJ, Ruan Q, Palmer S, Hilliard B, and Chen YH. Negative regulation of toll-like receptor signaling by NFkappaB p50 ubiquitination blockade. Science 317: 675-678, 2007.
12. Carnesecchi S, Deffert C, Pagano A, Garrido-Urbani S, Metrailler-Ruchonnet I, Schappi M, Donati Y, Matthay MA, Krause KH, and Barazzone Argiroffo C. NADPH oxidase-1 plays a crucial role in hyperoxia-induced acute lung injury in mice. Am J Respir Crit Care Med 180: 972-981, 2009.
13. Chawla A and Lazar MA. Induction of Rev-ErbA alpha, an orphan receptor encoded on the opposite strand of the alpha- thyroid hormone receptor gene, during adipocyte differentiation. J Biol Chem 268: 16265-16269, 1993.
14. Cho H, Zhao X, Hatori M, Yu RT, Barish GD, Lam MT, Chong LW, DiTacchio L, Atkins AR, Glass CK, Liddle C, Auwerx J, Downes M, Panda S, and Evans RM. Regulation of circadian behaviour and metabolism by REV-ERB-alpha and REV-ERB-beta. Nature 485: 123-127, 2012.
15. Clement A, Edeas M, Chadelat K, and Brody JS. Inhibition of lung epithelial cell proliferation by hyperoxia. Posttranscriptional regulation of proliferation-related genes. J Clin Invest 90: 1812-1818, 1992.
16. Cramer P, Larson CJ, Verdine GL, and Muller CW. Structure of the human NF-kappaB p52 homodimer-DNA complex at 2.1A resolution. EMBO J 16: 7078-7090, 1997.
17. Crumbley C, Wang Y, Kojetin DJ, and Burris TP. Characterization of the core mammalian clock component, NPAS2, as a REV-ERBalpha/RORalpha target gene. J Biol Chem 285: 35386-35392, 2010.
18. Dinkova-Kostova AT, Holtzclaw WD, Cole RN, Itoh K, Wakabayashi N, Katoh Y, Yamamoto M, and Talalay P. Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc Natl Acad Sci U S A 99: 11908-11913, 2002.
19. Downes M, Carozzi AJ, and Muscat GE. Constitutive expression of the orphan receptor, Rev-erbA alpha, inhibits muscle differentiation and abrogates the expression of the myoD gene family. Mol Endocrinol 9: 1666-1678, 1995.
20. Duffield GE, Best JD, Meurers BH, Bittner A, Loros JJ, and Dunlap JC. Circadian programs of transcriptional activation, signaling, and protein turnover revealed by microarray analysis of mammalian cells. Curr Biol 12: 551-557, 2002.
21. Edgar RS, Green EW, Zhao Y, van Ooijen G, Olmedo M, Qin X, Xu Y, Pan M, Valekunja UK, Feeney KA, Maywood ES, Hastings MH, Baliga NS, Merrow M, Millar AJ, Johnson CH, Kyriacou CP, O'Neill JS, and Reddy AB. Peroxiredoxins are conserved markers of circadian rhythms. Nature 485: 459-464, 2012.
22. Elsharkawy AM, Oakley F, Lin F, Packham G, Mann DA, and Mann J. The NF-kappaB p50:p50:HDAC-1 repressor complex orchestrates transcriptional inhibition of multiple pro-inflammatory genes. J Hepatol 53: 519-527, 2010.
23. Erickson AM, Nevarea Z, Gipp JJ, and Mulcahy RT. Identification of a variant antioxidant response element in the promoter of the human glutamate-cysteine ligase modifier subunit gene. Revision of the ARE consensus sequence. J Biol Chem 277: 30730-30737, 2002.
24. Fourquet S, Guerois R, Biard D, and Toledano MB. Activation of NRF2 by nitrosative agents and H2O2 involves KEAP1 disulfide formation. J Biol Chem 285: 8463-8471, 2010.
25. Frank L. Developmental aspects of experimental pulmonary oxygen toxicity. Free Radic Biol Med 11: 463-494, 1991.
26. Froy O and Miskin R. Effect of feeding regimens on circadian rhythms: implications for aging and longevity. Aging (Albany NY) 2: 7-27, 2010.
27. Gao Z, He Q, Peng B, Chiao PJ, and Ye J. Regulation of nuclear translocation of HDAC3 by IkappaBalpha is required for tumor necrosis factor inhibition of peroxisome proliferator-activated receptor gamma function. J Biol Chem 281: 4540-4547, 2006.
28. Ghosh G, van Duyne G, Ghosh S, and Sigler PB. Structure of NF-kappa B p50 homodimer bound to a kappa B site. Nature 373: 303-310, 1995.
29. Gibbs JE, Blaikley J, Beesley S, Matthews L, Simpson KD, Boyce SH, Farrow SN, Else KJ, Singh D, Ray DW, and Loudon AS. 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.
30. Guillaumond F, Dardente H, Giguere V, and Cermakian N. Differential control of Bmal1 circadian transcription by REV-ERB and ROR nuclear receptors. J Biol Rhythms 20: 391-403, 2005.
31. Harding HP and Lazar MA. The orphan receptor Rev-ErbA alpha activates transcription via a novel response element. Mol Cell Biol 13: 3113-3121, 1993.
32. Hayden MS and Ghosh S. Shared principles in NF-kappaB signaling. Cell 132: 344-362, 2008.
33. Hayden MS and Ghosh S. NF-kappaB, the first quartercentury: remarkable progress and outstanding questions. Genes Dev 26: 203-234, 2012.
34. Itoh K, Mimura J, and Yamamoto M. Discovery of the negative regulator of Nrf2, Keap1: a historical overview. Antioxid Redox Signal 13: 1665-1678, 2010.
35. Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, Field Y, LeProust EM, Hughes TR, Lieb JD, Widom J, and Segal E. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458: 362-366, 2009.
36. King DP and Takahashi JS. Molecular genetics of circadian rhythms in mammals. Annu Rev Neurosci 23: 713-742, 2000.
37. Kobayashi A, Kang MI, Okawa H, Ohtsuji M, Zenke Y, Chiba T, Igarashi K, and Yamamoto M. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol Cell Biol 24: 7130-7139, 2004.
38. Kondratov RV, Kondratova AA, Gorbacheva VY, Vykhovanets OV, and Antoch MP. Early aging and age-related pathologies in mice deficient in BMAL1, the core componentof the circadian clock. Genes Dev 20: 1868-1873, 2006.
39. Krishnan N, Davis AJ, and Giebultowicz JM. Circadian regulation of response to oxidative stress in Drosophila melanogaster. Biochem Biophys Res Commun 374: 299-303, 2008.
40. Lee J, Reddy R, Barsky L, Weinberg K, and Driscoll B. Contribution of proliferation and DNA damage repair to alveolar epithelial type 2 cell recovery from hyperoxia. Am J Physiol Lung Cell Mol Physiol 290: L685-L694, 2006.
41. Lee YJ and Lee SH. Sulforaphane induces antioxidative and antiproliferative responses by generating reactive ox-ygen species in human bronchial epithelial BEAS-2B cells. J Korean Med Sci 26: 1474-1482, 2011.
42. Lin Q, Weis S, Yang G, Weng YH, Helston R, Rish K, Smith A, Bordner J, Polte T, Gaunitz F, and Dennery PA. Heme oxygenase-1 protein localizes to the nucleus and activates transcription factors important in oxidative stress. J Biol Chem 282: 20621-20633, 2007.
43. Lin QS, Weis S, Yang G, Zhuang T, Abate A, and Dennery PA. Catalytic inactive heme oxygenase-1 protein regulates its own expression in oxidative stress. Free Radic Biol Med 44: 847-855, 2008.
44. Martin RJ. Nocturnal asthma: circadian rhythms and therapeutic interventions. Am Rev Respir Dis 147: S25-S28, 1993.
45. Muller CW, Rey FA, and Harrison SC. Comparison of two different DNA-binding modes of the NF-kappa B p50 homodimer. Nat Struct Biol 3: 224-227, 1996.
46. Muller CW, Rey FA, Sodeoka M, Verdine GL, and Harrison SC. Structure of the NF-kappa B p50 homodimer bound to DNA. Nature 373: 311-317, 1995.
47. Muller JE, Stone PH, Turi ZG, Rutherford JD, Czeisler CA, Parker C, Poole WK, Passamani E, Roberts R, Robertson T, et al. Circadian variation in the frequency of onset of acute myocardial infarction. N Engl J Med 313: 1315-1322, 1985.
48. Mund SI, Stampanoni M, and Schittny JC. Developmental alveolarization of the mouse lung. Dev Dyn 237: 2108-2116, 2008.
49. Naamane N, van Helden J, and Eizirik DL. In silico identification of NF-kappaB-regulated genes in pancreatic betacells. BMC Bioinformatics 8: 55, 2007.
50. Natoli G, Saccani S, Bosisio D, and Marazzi I. Interactions of NF-kappaB with chromatin: the art of being at the right place at the right time. Nat Immunol 6: 439-445, 2005.
51. Nolan GP, Fujita T, Bhatia K, Huppi C, Liou HC, Scott ML, and Baltimore D. The bcl-3 proto-oncogene encodes a nuclear I kappa B-like molecule that preferentially interacts with NF-kappa B p50 and p52 in a phosphorylation- dependent manner. Mol Cell Biol 13: 3557-3566, 1993.
52. O'Neill JS and Reddy AB. Circadian clocks in human red blood cells. Nature 469: 498-503, 2011.
53. O'Neill JS, van Ooijen G, Dixon LE, Troein C, Corellou F, Bouget FY, Reddy AB, and Millar AJ. Circadian rhythms persist without transcription in a eukaryote. Nature 469: 554-558, 2011.
54. O'Reilly MA, Staversky RJ, Finkelstein JN, and Keng PC. Activation of the G2 cell cycle checkpoint enhances survival of epithelial cells exposed to hyperoxia. Am J Physiol Lung Cell Mol Physiol 284: L368-L375, 2003.
55. Oakley F, Mann J, Nailard S, Smart DE, Mungalsingh N, Constandinou C, Ali S, Wilson SJ, Millward-Sadler H, Iredale JP, and Mann DA. Nuclear factor-kappaB1 (p50) limits the inflammatory and fibrogenic responses to chronic injury. Am J Pathol 166: 695-708, 2005.
56. Olmedo M, O'Neill JS, Edgar RS, Valekunja UK, Reddy AB, and Merrow M. Circadian regulation of olfaction and an evolutionarily conserved, nontranscriptional marker in Caenorhabditis elegans. Proc Natl Acad Sci U S A 109: 20479-20484, 2012.
57. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, and Hogenesch JB. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109: 307-320, 2002.
58. Ramirez-Carrozzi VR, Braas D, Bhatt DM, Cheng CS, Hong C, Doty KR, Black JC, Hoffmann A, Carey M, and Smale ST. A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell 138: 114-128, 2009.
59. Savinova OV, Hoffmann A, and Ghosh G. The Nfkb1 and Nfkb2 proteins p105 and p100 function as the core of highmolecular- weight heterogeneous complexes. Mol Cell 34: 591-602, 2009.
60. Scheff JD, Mavroudis PD, Calvano SE, and Androulakis IP. Translational applications of evaluating physiologic variability in human endotoxemia. J Clin Monit Comput 27: 405-415, 2013.
61. Stangherlin A and Reddy AB. Regulation of circadian clocks by redox homeostasis. J Biol Chem 288: 26505-26511, 2013.
62. Storch KF, Lipan O, Leykin I, Viswanathan N, Davis FC, Wong WH, and Weitz CJ. Extensive and divergent circadian gene expression in liver and heart. Nature 417: 78-83, 2002.
63. Tong KI, Kobayashi A, Katsuoka F, and Yamamoto M. Two-site substrate recognition model for the Keap1-Nrf2 system: a hinge and latch mechanism. Biol Chem 387: 1311-1320, 2006.
64. Torra IP, Tsibulsky V, Delaunay F, Saladin R, Laudet V, Fruchart JC, Kosykh V, and Staels B. Circadian and glucocorticoid regulation of Rev-erbalpha expression in liver. Endocrinology 141: 3799-3806, 2000.
65. Triqueneaux G, Thenot S, Kakizawa T, Antoch MP, Safi R, Takahashi JS, Delaunay F, and Laudet V. The orphan receptor Rev-erbalpha gene is a target of the circadian clock pacemaker. J Mol Endocrinol 33: 585-608, 2004.
66. Vasu VT, Cross CE, and Gohil K. Nr1d1, an important circadian pathway regulatory gene, is suppressed by cigarette smoke in murine lungs. Integr Cancer Ther 8: 321-328, 2009.
67. Warner BB, Stuart LA, Papes RA, and Wispe JR. Functional and pathological effects of prolonged hyperoxia in neonatal mice. Am J Physiol 275: L110-L117, 1998.
68. Welsh DK, Logothetis DE, Meister M, and Reppert SM. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14: 697-706, 1995.
69. Westerheide SD, Mayo MW, Anest V, Hanson JL, and Baldwin AS Jr. The putative oncoprotein Bcl-3 induces cyclin D1 to stimulate G(1) transition. Mol Cell Biol 21: 8428-8436, 2001.
70. Xu YQ, Zhang D, Jin T, Cai DJ, Wu Q, Lu Y, Liu J, and Klaassen CD. Diurnal variation of hepatic antioxidant gene expression in mice. PLoS One 7: e44237, 2012.
71. Yang G, Abate A, George AG, Weng YH, and Dennery PA. Maturational differences in lung NF-kappaB activation and their role in tolerance to hyperoxia. J Clin Invest 114: 669-678, 2004.
72. Yang G, Hinson MD, Bordner JE, Lin QS, Fernando AP, La P, Wright CJ, and Dennery PA. Silencing hyperoxiainduced C/EBPalpha in neonatal mice improves lung architecture via enhanced proliferation of alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 301: L187-L196, 2011.
73. Yang G, Madan A, and Dennery PA. Maturational differences in hyperoxic AP-1 activation in rat lung. Am J Physiol Lung Cell Mol Physiol 278: L393-L398, 2000.
74. Yang HT, Papoutsopoulou S, Belich M, Brender C, Janzen J, Gantke T, Handley M, and Ley SC. Coordinate regulation of TPL-2 and NF-kappaB signaling in macrophages by NF-kappaB1 p105. Mol Cell Biol 32: 3438-3451, 2012.
75. Yin L, Wu N, and Lazar MA. Nuclear receptor Reverbalpha: a heme receptor that coordinates circadian rhythm and metabolism. Nucl Recept Signal 8: e001, 2010.