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BioMed Research International
Volume 2014 (2014), Article ID 610474, 10 pages
http://dx.doi.org/10.1155/2014/610474
Research Article

Nitric Oxide and Superoxide Anion Balance in Rats Exposed to Chronic and Long Term Intermittent Hypoxia

1Instituto de Estudios de la Salud, Universidad Arturo Prat, Avenida Arturo Prat 2120, 11100939 Iquique, Chile
2Departamento de Fisiología, Facultad de Medicina, Universidad Autónoma de Madrid, 28029 Madrid, Spain
3Instituto de Investigación Hospital Universitario Gregorio Marañón, 28007 Madrid, Spain
4Departamento de Ciencias Biológicas y Fisiológicas, Facultad de Ciencias y Filosofía/IIA, Universidad Peruana Cayetano Heredia, Lima 31, Lima, Peru
5Departamento de Medicina Preventiva, Salud Pública y Microbiología, Facultad de Medicina, Universidad Autónoma de Madrid, 28029 Madrid, Spain

Received 5 December 2013; Accepted 15 January 2014; Published 26 February 2014

Academic Editor: Iveta Bernatova

Copyright © 2014 Patricia Siques 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. F. León-Velarde, M. Maggiorini, J. T. Reeves, et al., “Consensus statement on chronic and subacute high altitude diseases,” High Altitude Medicine and Biology, vol. 6, no. 2, pp. 147–157, 2005.
  2. R. Dumitrascu, J. Heitmann, W. Seeger, N. Weissmann, and R. Schulz, “Obstructive sleep apnea, oxidative stress and cardiovascular disease: lessons from animal studies,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 234631, 7 pages, 2013. View at Publisher · View at Google Scholar
  3. J.-P. Richalet, M. V. Donoso, D. Jiménez et al., “Chilean miners commuting from sea level to 4500 m: a prospective study,” High Altitude Medicine and Biology, vol. 3, no. 2, pp. 159–166, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. G. E. Foster, J. V. Brugniaux, V. Pialoux et al., “Cardiovascular and cerebrovascular responses to acute hypoxia following exposure to intermittent hypoxia in healthy humans,” Journal of Physiology, vol. 587, no. 13, pp. 3287–3299, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Siqués Lee, J. Brito, F. León-Velarde et al., “Time course of cardiovascular and hematological responses in rats exposed to chronic intermittent hypobaric hypoxia (4600 m),” High Altitude Medicine and Biology, vol. 7, no. 1, pp. 72–80, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. A. F. Corno, G. Milano, S. Morel et al., “Hypoxia: unique myocardial morphology?” Journal of Thoracic and Cardiovascular Surgery, vol. 127, no. 5, pp. 1301–1308, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. M. McGuire and A. Bradford, “Chronic intermittent hypoxia increases haematocrit and causes right ventricular hypertrophy in the rat,” Respiration Physiology, vol. 117, no. 1, pp. 53–58, 1999. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Brito, P. Siqués, F. León-Velarde et al., “Varying exposure regimes to long term chronic intermittent hypoxia exert different outcomes and morphological effects on Wistar rats at 4600 m,” Toxicological and Environmental Chemistry, vol. 90, no. 1, pp. 169–179, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. A. G. Durmowicz and K. R. Stenmark, “Mechanisms of structural remodeling in chronic pulmonary hypertension,” Pediatrics in Review, vol. 20, no. 11, pp. e91–e102, 1999. View at Scopus
  10. N. Sommer, A. Dietrich, R. T. Schermuly et al., “Regulation of hypoxic pulmonary vasoconstriction: basic mechanisms,” European Respiratory Journal, vol. 32, no. 6, pp. 1639–1651, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. M. S. Wolin, S. A. Gupte, C. J. Mingone, B. H. Neo, Q. Gao, and M. Ahmad, “Redox regulation of responses to hypoxia and NO-cGMP signaling in pulmonary vascular pathophysiology,” Annals of the New York Academy of Sciences, vol. 1203, pp. 126–132, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. W. Steudel, M. Scherrer-Crosbie, K. D. Bloch et al., “Sustained pulmonary hypertension and right ventricular hypertrophy after chronic hypoxia in mice with congenital deficiency of nitric oxide synthase,” Journal of Clinical Investigation, vol. 101, no. 11, pp. 2468–2477, 1998. View at Scopus
  13. G. Frazziano, H. C. Champion, and P. J. Pagano, “NADPH oxidase-derived ROS and the regulation of pulmonary vessel tone,” The American Journal of Physiology, vol. 302, no. 11, pp. H2166–H2177, 2012.
  14. K. K. Griendling and M. Ushio-Fukai, “Reactive oxygen species as mediators of angiotensin II signaling,” Regulatory Peptides, vol. 91, no. 1–3, pp. 21–27, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. M. C. González, “Confocal Microscopy as New Tool for the Study of Pulmonary Artery Remodelling at a Cellular Level in Rats Exposed to Chronic Hypobaric Hypoxia,” vol. 11, pp. 262, 2010.
  16. P. Siques, “Structural changes in pulmonary artery of exposed rats to chronic intermittent hypobaric hypoxia,” High Altitude Medicine and Biology, vol. 11, article 290, 2010.
  17. R. Germack, F. Leon-Velarde, R. Valdes De La Barra, J. Farias, G. Soto, and J. P. Richalet, “Effect of intermittent hypoxia on cardiovascular function, adrenoceptors and muscarinic receptors in Wistar rats,” Experimental Physiology, vol. 87, no. 4, pp. 453–460, 2002. View at Scopus
  18. J. Brito, P. Siqués, F. León-Velarde, J. J. De La Cruz, V. López, and R. Herruzo, “Chronic intermittent hypoxia at high altitude exposure for over 12 years: assessment of hematological, cardiovascular, and renal effects,” High Altitude Medicine and Biology, vol. 8, no. 3, pp. 236–244, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. J. M. González, B. Somoza, M. V. Conde, M. S. Fernández-Alfonso, M. C. González, and S. M. Arribas, “Hypertension increases middle cerebral artery resting tone in spontaneously hypertensive rats: role of tonic vasoactive factor availability,” Clinical Science, vol. 114, no. 9-10, pp. 651–659, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. Z. Wang, A. Y. Li, Q. H. Guo et al., “Effects of cyclic intermittent hypoxia on ET-1 responsiveness and endothelial dysfunction of pulmonary arteries in rats,” PLoS ONE, vol. 8, no. 3, Article ID e58078, 2013.
  21. Z. Tahawi, N. Orolinova, I. G. Joshua, M. Bader, and E. C. Fletcher, “Altered vascular reactivity in arterioles of chronic intermittent hypoxic rats,” Journal of Applied Physiology, vol. 90, no. 5, pp. 2007–2000, 2001. View at Scopus
  22. 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,” The American Journal of Physiology, vol. 286, no. 1, pp. H388–H393, 2004. View at Scopus
  23. D. C. Irwin, J. M. McCord, E. Nozik-Grayck et al., “A potential role for reactive oxygen species and the HIF-1α-VEGF pathway in hypoxia-induced pulmonary vascular leak,” Free Radical Biology and Medicine, vol. 47, no. 1, pp. 55–61, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. N. Weissmann, R. T. Schermuly, H. A. Ghofrani et al., “Hypoxic pulmonary vasoconstriction: triggered by an increase in reactive oxygen species?” Novartis Foundation Symposium, vol. 272, pp. 196–208, 2006. View at Scopus
  25. N. Weissmann, S. Zeller, R. U. Schäfer et al., “Impact of mitochondria and NADPH oxidases on acute and sustained hypoxic pulmonary vasoconstriction,” The American Journal of Respiratory Cell and Molecular Biology, vol. 34, no. 4, pp. 505–513, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Kojima, N. Nakatsubo, K. Kikuchi et al., “Direct evidence of NO production in rat hippocampus and cortex using a new fluorescent indicator: DAF-2 DA,” NeuroReport, vol. 9, no. 15, pp. 3345–3348, 1998. View at Scopus
  27. F.-X. Yi, A. Y. Zhang, W. B. Campbell, A.-P. Zou, C. Van Breemen, and P.-L. Li, “Simultaneous in situ monitoring of intracellular Ca2+ and NO in endothelium of coronary arteries,” The American Journal of Physiology, vol. 283, no. 6, pp. H2725–H2732, 2002. View at Scopus
  28. S. M. Arribas, C. J. Daly, M. C. González, and J. C. Mcgrath, “Imaging the vascular wall using confocal microscopy,” Journal of Physiology, vol. 584, no. 1, pp. 5–9, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. B. Somoza, F. Abderrahim, J. M. González et al., “Short-term treatment of spontaneously hypertensive rats with liver growth factor reduces carotid artery fibrosis, improves vascular function, and lowers blood pressure,” Cardiovascular Research, vol. 69, no. 3, pp. 764–771, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. F. L. Powell and N. Garcia, “Physiological effects of intermittent hypoxia,” High Altitude Medicine and Biology, vol. 1, no. 2, pp. 125–136, 2000. View at Scopus
  31. C. E. Norton, N. L. Jernigan, N. L. Kanagy, B. R. Walker, and T. C. Resta, “Intermittent hypoxia augments pulmonary vascular smooth muscle reactivity to NO: regulation by reactive oxygen species,” Journal of Applied Physiology, vol. 111, no. 4, pp. 980–988, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. B. Fuchs, N. Sommer, A. Dietrich et al., “Redox signaling and reactive oxygen species in hypoxic pulmonary vasoconstriction,” Respiratory Physiology and Neurobiology, vol. 174, no. 3, pp. 282–291, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. R. E. Nisbet, A. S. Graves, D. J. Kleinhenz et al., “The role of NADPH oxidase in chronic intermittent hypoxia-induced pulmonary hypertension in mice,” The American Journal of Respiratory Cell and Molecular Biology, vol. 40, no. 5, pp. 601–609, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. J. M. Dopp, N. R. Philippi, N. J. Marcus et al., “Xanthine oxidase inhibition attenuates endothelial dysfunction caused by chronic intermittent hypoxia in rats,” Respiration, vol. 82, no. 5, pp. 458–467, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. A. A. El Solh, R. Saliba, T. Bosinski, B. J. B. Grant, E. Berbary, and N. Miller, “Allopurinol improves endothelial function in sleep apnoea: a randomised controlled study,” European Respiratory Journal, vol. 27, no. 5, pp. 997–1002, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. I. Al Ghouleh, N. K. H. Khoo, U. G. Knaus et al., “Oxidases and peroxidases in cardiovascular and lung disease: new concepts in reactive oxygen species signaling,” Free Radical Biology and Medicine, vol. 51, no. 7, pp. 1271–1288, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. U. Förstermann, “Nitric oxide and oxidative stress in vascular disease,” Pflügers Archiv, vol. 459, no. 6, pp. 923–939, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Aggarwal, C. M. Gross, S. Sharma, J. R. Fineman, and S. M. Black, “Reactive oxygen species in pulmonary vascular remodeling,” Comprehensive Physiology, vol. 3, no. 3, pp. 1011–1034.
  39. E. Panzhinskiy, W. M. Zawada, K. R. Stenmark, and M. Das, “Hypoxia induces unique proliferative response in adventitial fibroblasts by activating PDGFbeta receptor-JNK1 signalling,” Cardiovascular Research, vol. 95, no. 3, pp. 356–365, 2012.
  40. S. Li, S. S. Tabar, V. Malec et al., “NOX4 regulates ROS levels under normoxic and hypoxic conditions, triggers proliferation, and inhibits apoptosis in pulmonary artery adventitial fibroblasts,” Antioxidants and Redox Signaling, vol. 10, no. 10, pp. 1687–1697, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Berry, C. A. Hamilton, M. J. Brosnan et al., “Investigation into the sources of superoxide in human blood vessels: angiotensin II increases superoxide production in human internal mammary arteries,” Circulation, vol. 101, no. 18, pp. 2206–2212, 2000. View at Scopus
  42. P. J. Pagano, Y. Ito, K. Tornheim, P. M. Gallop, A. I. Tauber, and R. A. Cohen, “An NADPH oxidase superoxide-generating system in the rabbit aorta,” The American Journal of Physiology, vol. 268, no. 6, pp. H2274–H2280, 1995. View at Scopus
  43. H. D. Wang, P. J. Pagano, Y. Du et al., “Superoxide anion from the adventitia of the rat thoracic aorta inactivates nitric oxide,” Circulation Research, vol. 82, no. 7, pp. 810–818, 1998. View at Scopus
  44. B. Somoza, M. C. González, J. M. González, F. Abderrahim, S. M. Arribas, and M. S. Fernández-Alfonso, “Modulatory role of the adventitia on noradrenaline and angiotensin II responses: role of endothelium and AT2 receptors,” Cardiovascular Research, vol. 65, no. 2, pp. 478–486, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Chao, J. G. Wood, V. G. Blanco, and N. C. Gonzalez, “The systemic inflammation of alveolar hypoxia is initiated by alveolar macrophage-borne mediator(s),” The American Journal of Respiratory Cell and Molecular Biology, vol. 41, no. 5, pp. 573–582, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. D. L. Burke, M. G. Frid, C. L. Kunrath et al., “Sustained hypoxia promotes the development of a pulmonary artery-specific chronic inflammatory microenvironment,” The American Journal of Physiology, vol. 297, no. 2, pp. L238–L250, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Zhang, J. M. Patel, Y. D. Li, and E. R. Block, “Proinflammatory cytokines downregulate gene expression and activity of constitutive nitric oxide synthase in porcine pulmonary artery endothelial cells,” Research Communications in Molecular Pathology and Pharmacology, vol. 96, no. 1, pp. 71–88, 1997. View at Scopus
  48. 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