Intermittent hypoxia causes NOX2-dependent remodeling of atrial connexins

BMC Cell Biology

Volumn 18, Issue , 2017, Pages

  Gemel, Joanna ^a   Su, Zihan ^b   Gileles Hillel, Alex ^c   Khalyfa, Abdelnaby ^a   Gozal, David ^a   Beyer, Eric C ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b WILLIAMS COLLEGE   (United States)

^c HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

Atrial fibrillation; Connexin; Gap junctions; Intermittent hypoxia; Obstructive sleep apnea

Indexed keywords

CONNEXIN 40; CONNEXIN 43; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; CADHERIN; CYBB PROTEIN, MOUSE; GAP JUNCTION PROTEIN; MEMBRANE PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATRIAL FIBRILLATION; CONTROLLED STUDY; CX40 GENE; CX43 GENE; GAP JUNCTION; HEART ATRIUM REMODELING; HEART VENTRICLE REMODELING; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; INTERMITTENT HYPOXIA; MALE; MOUSE; NONHUMAN; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SLEEP DISORDERED BREATHING; ANIMAL; C57BL MOUSE; HEART ATRIUM; HYPOXIA; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; CADHERINS; CONNEXIN 43; CONNEXINS; HEART ATRIA; HYPOXIA; MALE; MEMBRANE GLYCOPROTEINS; MICE, INBRED C57BL; MICE, KNOCKOUT; NADPH OXIDASE 2; NADPH OXIDASES;

EID: 85009957894     PISSN: None     EISSN: 14712121     Source Type: Journal    
DOI: 10.1186/s12860-016-0117-5     Document Type: Article

References (40)

1. Somers VK, White DP, Amin R, Abraham WT, Costa F, Culebras A, Daniels S, Floras JS, Hunt CE, Olson LJ, Pickering TG, Russell R, Woo M, Young T. leep apnea and cardiovascular disease: an American Heart Association/American College of Cardiology Foundation Scientific Statement from the American Heart Association Council for High Blood Pressure Research Professional Education Committee, Council on Clinical Cardiology, Stroke Council, and Council on Cardiovascular Nursing. J Am Coll Cardiol. 2008;52:686-717.
2. Bradley TD, Floras JS. Obstructive sleep apnoea and its cardiovascular consequences. Lancet. 2009;373:82-93.
3. Malhotra A, Loscalzo J. Sleep and cardiovascular disease: an overview. Prog Cardiovasc Dis. 2009;51:279-84.
4. Linz D, Linz B, Hohl M, Bohm M. Atrial arrhythmogenesis in obstructive sleep apnea: Therapeutic implications. Sleep Med Rev. 2015;26:87-94.
5. Gami AS, Pressman G, Caples SM, Kanagala R, Gard JJ, Davison DE, Malouf JF, Ammash NM, Friedman PA, Somers VK. Association of atrial fibrillation and obstructive sleep apnea. Circulation. 2004;110:364-7.
6. Gami AS, Hodge DO, Herges RM, Olson EJ, Nykodym J, Kara T, Somers VK. Obstructive sleep apnea, obesity, and the risk of incident atrial fibrillation. J Am Coll Cardiol. 2007;49:565-71.
7. Braga B, Poyares D, Cintra F, Guilleminault C, Cirenza C, Horbach S, Macedo D, Silva R, Tufik S, De Paola AA. Sleep-disordered breathing and chronic atrial fibrillation. Sleep Med. 2009;10:212-6.
8. Cadby G, McArdle N, Briffa T, Hillman DR, Simpson L, Knuiman M, Hung J. Severity of OSA Is an Independent Predictor of Incident Atrial Fibrillation Hospitalization in a Large Sleep-Clinic Cohort. Chest. 2015;148:945-52.
9. Holmqvist F, Guan N, Zhu Z, Kowey PR, Allen LA, Fonarow GC, Hylek EM, Mahaffey KW, Freeman JV, Chang P, Holmes DN, Peterson ED, Piccini JP, Gersh BJ. Impact of obstructive sleep apnea and continuous positive airway pressure therapy on outcomes in patients with atrial fibrillation-Results from the Outcomes Registry for Better Informed Treatment of Atrial Fibrillation (ORBIT-AF). Am Heart J. 2015;169:647-54.
10. Kwon Y, Gharib SA, Biggs ML, Jacobs Jr DR, Alonso A, Duprez D, Lima J, Lin GM, Soliman EZ, Mehra R, Redline S, Heckbert SR. Association of sleep characteristics with atrial fibrillation: the multi-ethnic study of atherosclerosis. Thorax. 2015;70:873-9.
11. Lin GM, Colangelo LA, Lloyd-Jones DM, Redline S, Yeboah J, Heckbert SR, Nazarian S, Alonso A, Bluemke DA, Punjabi NM, Szklo M, Liu K. Association of sleep apnea and snoring with incident atrial fibrillation in the multi-ethnic study of atherosclerosis. Am J Epidemiol. 2015;182:49-57.
12. Matassini MV, Brambatti M, Guerra F, Scappini L, Capucci A. Sleep-disordered breathing and atrial fibrillation: review of the evidence. Cardiol Rev. 2015;23:79-86.
13. Allessie MA, Boyden PA, Camm AJ, Kleber AG, Lab MJ, Legato MJ, Rosen MR, Schwartz PJ, Spooner PM, Van Wagoner DR, Waldo AL. Pathophysiology and prevention of atrial fibrillation. Circulation. 2001;103:769-77.
14. Iwasaki YK, Nishida K, Kato T, Nattel S. Atrial fibrillation pathophysiology: implications for management. Circulation. 2011;124:2264-74.
15. Spach MS, Starmer CF. Altering the topology of gap junctions a major therapeutic target for atrial fibrillation. Cardiovasc Res. 1995;30:337-44.
16. Nattel S. Age, gender, and supraventricular arrhythmias: roles of ion channels, connexins, and tissue architecture? Heart Rhythm. 2004;1:397-8.
17. Severs NJ. Gap junction remodeling and cardiac arrhythmogenesis: cause or coincidence? J Cell Molec Med. 2001;5:355-66.
18. Lin X, Gemel J, Glass A, Zemlin CW, Beyer EC, Veenstra RD. Connexin40 and connexin43 determine gating properties of atrial gap junction channels. J Mol Cell Cardiol. 2010;48:238-45.
19. Gileles-Hillel A, Almendros I, Khalyfa A, Zhang SX, Wang Y, Gozal D. Early intermittent hypoxia induces proatherogenic changes in aortic wall macrophages in a murine model of obstructive sleep apnea. Am J Respir Crit Care Med. 2014;190:958-61.
20. Kheirandish L, Row BW, Li RC, Brittian KR, Gozal D. Apolipoprotein E-deficient mice exhibit increased vulnerability to intermittent hypoxia-induced spatial learning deficits. Sleep. 2005;28:1412-7.
21. Lin M, Liu R, Gozal D, Wead WB, Chapleau MW, Wurster R, Cheng ZJ. Chronic intermittent hypoxia impairs baroreflex control of heart rate but enhances heart rate responses to vagal efferent stimulation in anesthetized mice. Am J Physiol Heart Circ Physiol. 2007;293:H997-1006.
22. Soukhova-O'Hare GK, Shah ZA, Lei Z, Nozdrachev AD, Rao CV, Gozal D. Erectile dysfunction in a murine model of sleep apnea. Am J Respir Crit Care Med. 2008;178:644-50.
23. Xu J, Long YS, Gozal D, Epstein PN. Beta-cell death and proliferation after intermittent hypoxia: role of oxidative stress. Free Radic Biol Med. 2009;46:783-90.
24. Wang Y, Guo SZ, Bonen A, Li RC, Kheirandish-Gozal L, Zhang SX, Brittian KR, Gozal D. Monocarboxylate transporter 2 and stroke severity in a rodent model of sleep apnea. J Neurosci. 2011;31:10241-8.
25. Zhan G, Serrano F, Fenik P, Hsu R, Kong L, Pratico D, Klann E, Veasey SC. NADPH oxidase mediates hypersomnolence and brain oxidative injury in a murine model of sleep apnea. Am J Respir Crit Care Med. 2005;172:921-9.
26. Nair D, Dayyat EA, Zhang SX, Wang Y, Gozal D. Intermittent hypoxia-induced cognitive deficits are mediated by NADPH oxidase activity in a murine model of sleep apnea. PLoS ONE. 2011;6:e19847.
27. Zhang SX, Khalyfa A, Wang Y, Carreras A, Hakim F, Neel BA, Brady MJ, Qiao Z, Hirotsu C, Gozal D. Sleep fragmentation promotes NADPH oxidase 2-mediated adipose tissue inflammation leading to insulin resistance in mice. Int J Obes (Lond). 2014;38:619-24.
28. Gemel J, Levy AE, Simon AR, Bennett KB, Ai X, Akhter S, Beyer EC. Connexin40 abnormalities and atrial fibrillation in the human heart. J Mol Cell Cardiol. 2014;76:159-68.
29. Pandya K, Kim HS, Smithies O. Fibrosis, not cell size, delineates beta-myosin heavy chain reexpression during cardiac hypertrophy and normal aging in vivo. Proc Natl Acad Sci U S A. 2006;103:16864-9.
30. Iwasaki YK, Kato T, Xiong F, Shi YF, Naud P, Maguy A, Mizuno K, Tardif JC, Comtois P, Nattel S. Atrial fibrillation promotion with long-term repetitive obstructive sleep apnea in a rat model. J Am Coll Cardiol. 2014;64:2013-23.
31. Kato T, Iwasaki YK, Nattel S. Connexins and atrial fibrillation: filling in the gaps. Circulation. 2012;125:203-6.
32. Kanmanthareddy A, Emert MP, Pimentel RC, Reddy YM, Bommana S, Atkins D, Tadakamalla R, Lakkireddy T, Lakkireddy D. Lone atrial fibrillation: electrophysiology, risk factors, catheter ablation and other non-pharmacologic treatments. Curr Pharm Des. 2015;21:580-90.
33. Kim YM, Guzik TJ, Zhang YH, Zhang MH, Kattach H, Ratnatunga C, Pillai R, Channon KM, Casadei B. A myocardial Nox2 containing NAD(P)H oxidase contributes to oxidative stress in human atrial fibrillation. Circ Res. 2005;97:629-36.
34. Adam O, Frost G, Custodis F, Sussman MA, Schafers HJ, Bohm M, Laufs U. Role of Rac1 GTPase activation in atrial fibrillation. J Am Coll Cardiol. 2007;50:359-67.
35. Zhang M, Perino A, Ghigo A, Hirsch E, Shah AM. NADPH oxidases in heart failure: poachers or gamekeepers? Antioxid Redox Signal. 2013;18:1024-41.
36. Dolber PC, Beyer EC, Junker JL, Spach MS. Distribution of gap junctions in dog and rat ventricle studied with a double-label technique. J Mol Cell Cardiol. 1992;24:1443-57.
37. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein-dye binding. Anal Biochem. 1976;72:248-54.
38. Bolte S, Cordelieres FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc. 2006;224:213-32.
39. Kanagaratnam P, Rothery S, Patel P, Severs NJ, Peters NS. Relative expression of immunolocalized connexins 40 and 43 correlates with human atrial conduction properties. J Am Coll Cardiol. 2002;39:116-23.
40. Wilhelm M, Kirste W, Kuly S, Amann K, Neuhuber W, Weyand M, Daniel WG, Garlichs C. Atrial distribution of connexin 40 and 43 in patients with intermittent, persistent, and postoperative atrial fibrillation. Heart Lung Circ. 2006;15:30-7.