Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 2354870, 9 pages
http://dx.doi.org/10.1155/2016/2354870
Research Article

Uncoupling of Vascular Nitric Oxide Synthase Caused by Intermittent Hypoxia

1Department of Anesthesiology, Pharmacology and Therapeutics, University of British Columbia, Vancouver, BC, Canada
2Divisions of Critical Care and Respiratory Medicine, Department of Medicine, University of British Columbia, Vancouver, BC, Canada
3Sleep Disorders Program, UBC Hospital, Vancouver, BC, Canada
4Division of Critical Care Medicine, Providence Healthcare, Vancouver, BC, Canada

Received 3 August 2016; Accepted 3 October 2016

Academic Editor: Giuseppe Cirillo

Copyright © 2016 Mohammad Badran et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Badran, N. Ayas, and I. Laher, “Insights into obstructive sleep apnea research,” Sleep Medicine, vol. 15, no. 5, pp. 485–495, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. W. T. McNicholas and M. R. Bonsigore, “Sleep apnoea as an independent risk factor for cardiovascular disease: current evidence, basic mechanisms and research priorities,” The European Respiratory Journal, vol. 29, no. 1, pp. 156–178, 2007. View at Google Scholar
  3. L. F. Drager, S. M. Togeiro, V. Y. Polotsky, and G. Lorenzi-Filho, “Obstructive sleep apnea: a cardiometabolic risk in obesity and the metabolic syndrome,” Journal of the American College of Cardiology, vol. 62, no. 7, pp. 569–576, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. D. Koren, J. A. Chirinos, L. E. L. Katz et al., “Interrelationships between obesity, obstructive sleep apnea syndrome and cardiovascular risk in obese adolescents,” International Journal of Obesity, vol. 39, no. 7, pp. 1086–1093, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. R. N. Aurora and N. M. Punjabi, “Obstructive sleep apnoea and type 2 diabetes mellitus: a bidirectional association,” The Lancet Respiratory Medicine, vol. 1, no. 4, pp. 329–338, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. P. Rajan and H. Greenberg, “Obstructive sleep apnea as a risk factor for type 2 diabetes mellitus,” Nature and Science of Sleep, vol. 7, pp. 113–125, 2015. View at Publisher · View at Google Scholar · View at Scopus
  7. J. M. Marin, A. Agusti, I. Villar et al., “Association between treated and untreated obstructive sleep apnea and risk of hypertension,” The Journal of the American Medical Association, vol. 307, no. 20, pp. 2169–2176, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. H. Vrints, B. Shivalkar, H. Hilde et al., “Cardiovascular mechanisms and consequences of obstructive sleep apnoea,” Acta Clinica Belgica, vol. 68, no. 3, pp. 169–178, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. D. J. Eckert and A. Malhotra, “Pathophysiology of adult obstructive sleep apnea,” Proceedings of the American Thoracic Society, vol. 5, no. 2, pp. 144–153, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Feng, D. Zhang, and B. Chen, “Endothelial mechanisms of endothelial dysfunction in patients with obstructive sleep apnea,” Sleep and Breathing, vol. 16, no. 2, pp. 283–294, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Badran, S. Golbidi, A. Devlin, N. Ayas, and I. Laher, “Chronic intermittent hypoxia causes endothelial dysfunction in a mouse model of diet-induced obesity,” Sleep Medicine, vol. 15, no. 5, pp. 596–602, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. C.-Y. Chen, C.-L. Chen, and C.-C. Yu, “Obstructive sleep apnea is independently associated with arterial stiffness in ischemic stroke patients,” Journal of Neurology, vol. 262, no. 5, pp. 1247–1254, 2015. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Kohler, S. Craig, J. C. T. Pepperell et al., “CPAP improves endothelial function in patients with minimally symptomatic OSA: results from a subset study of the MOSAIC trial,” Chest, vol. 144, no. 3, pp. 896–902, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. S. A. Phillips, E. B. Olson, B. J. Morgan, and J. H. Lombard, “Chronic intermittent hypoxia impairs endothelium-dependent dilation in rat cerebral and skeletal muscle resistance arteries,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 286, no. 1, pp. H388–H393, 2004. View at Google Scholar · View at Scopus
  15. S. Pamidi and E. Tasali, “Obstructive sleep apnea and type 2 diabetes: Is there a link?” Frontiers in Neurology, vol. 3, article 126, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Kendzerska, A. S. Gershon, G. Hawker, G. Tomlinson, and R. S. Leung, “Obstructive sleep apnea and incident diabetes. A historical cohort study,” American Journal of Respiratory and Critical Care Medicine, vol. 190, no. 2, pp. 218–225, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. Promotion, N. C. f. C. D. P. a. H. National Diabetes Statistics Report, 2014
  18. N. Sallam, A. Fisher, S. Golbidi, and I. Laher, “Weight and inflammation are the major determinants of vascular dysfunction in the aortae of db/db mice,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 383, no. 5, pp. 483–492, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Ghosh, M. Khazaei, F. Moien-Afshari et al., “Moderate exercise attenuates caspase-3 activity, oxidative stress, and inhibits progression of diabetic renal disease in db/db mice,” American Journal of Physiology—Renal Physiology, vol. 296, no. 4, pp. F700–F708, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Khazaei, F. Moien-Afshari, T. J. Kieffer, and I. Laher, “Effect of exercise on augmented aortic vasoconstriction in the db/db mouse model of type-II diabetes,” Physiological Research, vol. 57, no. 6, pp. 847–856, 2008. View at Google Scholar · View at Scopus
  21. A. Daiber, M. Oelze, S. Daub et al., “Vascular redox signaling, redox switches in endothelial nitric oxide synthase (eNOS Uncoupling), and endothelial dysfunction,” in Systems Biology of Free Radicals and Antioxidants, pp. 1177–1211, Springer, Berlin, Germany, 2014. View at Publisher · View at Google Scholar
  22. T. Anothaisintawee, S. Reutrakul, E. Van Cauter, and A. Thakkinstian, “Sleep disturbances compared to traditional risk factors for diabetes development: systematic review and meta-analysis,” Sleep Medicine Reviews, vol. 30, pp. 11–24, 2016. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Doumit and B. Prasad, “Sleep Apnea in type 2 diabetes,” Diabetes Spectrum, vol. 29, no. 1, pp. 14–19, 2016. View at Publisher · View at Google Scholar
  24. R. Yang, G. Sikka, J. Larson et al., “Restoring leptin signaling reduces hyperlipidemia and improves vascular stiffness induced by chronic intermittent hypoxia,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 300, no. 4, pp. H1467–H1476, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. M.-W. Hung, G. M. Kravtsov, C.-F. Lau, A. M.-S. Poon, G. L. Tipoe, and M.-L. Fung, “Melatonin ameliorates endothelial dysfunction, vascular inflammation, and systemic hypertension in rats with chronic intermittent hypoxia,” Journal of Pineal Research, vol. 55, no. 3, pp. 247–256, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Hernández-Guerra, Z. A. de Ganzo, Y. González-Méndez et al., “Chronic intermittent hypoxia aggravates intrahepatic endothelial dysfunction in cirrhotic rats,” Hepatology, vol. 57, no. 4, pp. 1564–1574, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. V. Savransky, A. Nanayakkara, J. Li et al., “Chronic intermittent hypoxia induces atherosclerosis,” American Journal of Respiratory and Critical Care Medicine, vol. 175, no. 12, pp. 1290–1297, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Dematteis, C. Julien, C. Guillermet et al., “Intermittent hypoxia induces early functional cardiovascular remodeling in mice,” American Journal of Respiratory and Critical Care Medicine, vol. 177, no. 2, pp. 227–235, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Badran, N. Ayas, and I. Laher, “Cardiovascular complications of sleep apnea: role of oxidative stress,” Oxidative Medicine and Cellular Longevity, vol. 2014, Article ID 985258, 10 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. D. Pitocco, M. Tesauro, R. Alessandro, G. Ghirlanda, and C. Cardillo, “Oxidative stress in diabetes: implications for vascular and other complications,” International Journal of Molecular Sciences, vol. 14, no. 11, pp. 21525–21550, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. S. W. Schaffer, C. J. Jong, and M. Mozaffari, “Role of oxidative stress in diabetes-mediated vascular dysfunction: unifying hypothesis of diabetes revisited,” Vascular Pharmacology, vol. 57, no. 5-6, pp. 139–149, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Lavie, “Oxidative stress in obstructive sleep apnea and intermittent hypoxia—revisited—the bad ugly and good: implications to the heart and brain,” Sleep Medicine Reviews, vol. 20, pp. 27–45, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. S.-Y. Lam, Y. Liu, K.-M. Ng et al., “Chronic intermittent hypoxia induces local inflammation of the rat carotid body via functional upregulation of proinflammatory cytokine pathways,” Histochemistry and Cell Biology, vol. 137, no. 3, pp. 303–317, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. N. R. Philippi, C. E. Bird, N. J. Marcus, E. B. Olson, N. C. Chesler, and B. J. Morgan, “Time course of intermittent hypoxia-induced impairments in resistance artery structure and function,” Respiratory Physiology and Neurobiology, vol. 170, no. 2, pp. 157–163, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Jun, V. Savransky, A. Nanayakkara et al., “Intermittent hypoxia has organ-specific effects on oxidative stress,” American Journal of Physiology—Regulatory, Integrative and Comparative Physiology, vol. 295, no. 4, pp. R1274–R1281, 2008. View at Google Scholar
  36. J. Li, V. Savransky, A. Nanayakkara, P. L. Smith, C. P. O'Donnell, and V. Y. Polotsky, “Hyperlipidemia and lipid peroxidation are dependent on the severity of chronic intermittent hypoxia,” Journal of Applied Physiology, vol. 102, no. 2, pp. 557–563, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. A. K. Htoo, H. Greenberg, S. Tongia et al., “Activation of nuclear factor κB in obstructive sleep apnea: a pathway leading to systemic inflammation,” Sleep and Breathing, vol. 10, no. 1, pp. 43–50, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. T. Yokoe, K. Minoguchi, H. Matsuo et al., “Elevated levels of C-reactive protein and interleukin-6 in patients with obstructive sleep apnea syndrome are decreased by nasal continuous positive airway pressure,” Circulation, vol. 107, no. 8, pp. 1129–1134, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Zhang, L. Zheng, J. Cao, B. Chen, and D. Jin, “Inflammation induced by increased frequency of intermittent hypoxia is attenuated by tempol administration,” Brazilian Journal of Medical and Biological Research, vol. 48, no. 12, pp. 1115–1121, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. N. Sallam and I. Laher, “Exercise modulates oxidative stress and inflammation in aging and cardiovascular diseases,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 7239639, 32 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  41. U. Förstermann and T. Münzel, “Endothelial nitric oxide synthase in vascular disease: from marvel to menace,” Circulation, vol. 113, no. 13, pp. 1708–1714, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. Y.-M. Yang, A. Huang, G. Kaley, and D. Sun, “eNOS uncoupling and endothelial dysfunction in aged vessels,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 297, no. 5, pp. H1829–H1836, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Varadharaj, K. Porter, A. Pleister et al., “Endothelial nitric oxide synthase uncoupling: a novel pathway in OSA induced vascular endothelial dysfunction,” Respiratory Physiology and Neurobiology, vol. 207, pp. 40–47, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Oelze, S. Kröller-Schön, P. Welschof et al., “The sodium-glucose co-transporter 2 inhibitor empagliflozin improves diabetes-induced vascular dysfunction in the streptozotocin diabetes rat model by interfering with oxidative stress and glucotoxicity,” PLoS ONE, vol. 9, no. 11, Article ID e112394, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Luo, H. Lei, H. Qin, and Y. Xia, “Molecular mechanisms of endothelial no synthase uncoupling,” Current Pharmaceutical Design, vol. 20, no. 22, pp. 3548–3553, 2014. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Badran, S. Golbidi, N. Ayas, and I. Laher, “Nitric oxide bioavailability in obstructive sleep apnea: interplay of asymmetric dimethylarginine and free radicals,” Sleep Disorders, vol. 2015, Article ID 387801, 10 pages, 2015. View at Publisher · View at Google Scholar
  47. M. B. P. Landim, A. Casella Filho, and A. C. P. Chagas, “Asymmetric dimethylarginine (ADMA) and endothelial dysfunction: implications for atherogenesis,” Clinics, vol. 64, no. 5, pp. 471–478, 2009. View at Publisher · View at Google Scholar · View at Scopus