Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2018, Article ID 9649608, 12 pages
https://doi.org/10.1155/2018/9649608
Research Article

Nocturnal Hypoxia Improves Glucose Disposal, Decreases Mitochondrial Efficiency, and Increases Reactive Oxygen Species in the Muscle and Liver of C57BL/6J Mice Independent of Weight Change

1Division of Endocrinology and Metabolism, University of Pittsburgh Medical Center, University of Pittsburgh, 3459 Fifth Avenue, 628 NW, Pittsburgh, PA 15213, USA
2Division of Pulmonary, Allergy and Critical Care Medicine, Department of Medicine, University of Pittsburgh Medical Center, University of Pittsburgh, 3459 Fifth Avenue, 628 NW Pittsburgh, PA 15213, USA
3Department of Pharmacology and Chemical Biology, University of Pittsburgh Medical Center, University of Pittsburgh, 3459 Fifth Avenue, 628 NW Pittsburgh, PA 15213, USA

Correspondence should be addressed to Christopher P. O’Donnell; ude.cmpu@pcllennodo

Received 10 July 2017; Revised 14 November 2017; Accepted 29 November 2017; Published 4 February 2018

Academic Editor: Lena Lavie

Copyright © 2018 Simona Ioja 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. D. Z. Levett, E. J. Radford, D. A. Menassa et al., “Acclimatization of skeletal muscle mitochondria to high-altitude hypoxia during an ascent of Everest,” The FASEB Journal, vol. 26, no. 4, pp. 1431–1441, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. J. L. Fan, A. W. Subudhi, O. Evero et al., “AltitudeOmics: enhanced cerebrovascular reactivity and ventilatory response to CO2 with high-altitude acclimatization and reexposure,” Journal of Applied Physiology, vol. 116, no. 7, pp. 911–918, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. C. Reinke, S. Bevans-Fonti, L. F. Drager, M. K. Shin, and V. Y. Polotsky, “Effects of different acute hypoxic regimens on tissue oxygen profiles and metabolic outcomes,” Journal of Applied Physiology, vol. 111, no. 3, pp. 881–890, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. C. E. Murry, R. B. Jennings, and K. A. Reimer, “Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium,” Circulation, vol. 74, no. 5, pp. 1124–1136, 1986. View at Publisher · View at Google Scholar
  5. R. J. Schott, S. Rohmann, E. R. Braun, and W. Schaper, “Ischemic preconditioning reduces infarct size in swine myocardium,” Circulation Research, vol. 66, no. 4, pp. 1133–1142, 1990. View at Publisher · View at Google Scholar
  6. J. M. Marin, S. J. Carrizo, E. Vicente, and A. G. Agusti, “Long-term cardiovascular outcomes in men with obstructive sleep apnoea-hypopnoea with or without treatment with continuous positive airway pressure: an observational study,” The Lancet, vol. 365, no. 9464, pp. 1046–1053, 2005. View at Publisher · View at Google Scholar
  7. T. Young, L. Finn, P. E. Peppard et al., “Sleep disordered breathing and mortality: eighteen-year follow-up of the Wisconsin sleep cohort,” Sleep, vol. 31, no. 8, pp. 1071–1078, 2008. View at Google Scholar
  8. H. K. Yaggi, J. Concato, W. N. Kernan, J. H. Lichtman, L. M. Brass, and V. Mohsenin, “Obstructive sleep apnea as a risk factor for stroke and death,” The New England Journal of Medicine, vol. 353, no. 19, pp. 2034–2041, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. B. D. Kent, L. Grote, S. Ryan et al., “Diabetes mellitus prevalence and control in sleep-disordered breathing: the European Sleep Apnea Cohort (ESADA) study,” Chest, vol. 146, no. 4, pp. 982–990, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. N. M. Punjabi, E. Shahar, S. Redline et al., “Sleep-disordered breathing, glucose intolerance, and insulin resistance: the sleep heart health study,” American Journal of Epidemiology, vol. 160, no. 6, pp. 521–530, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. C. Imray, A. Wright, A. Subudhi, and R. Roach, “Acute mountain sickness: pathophysiology, prevention, and treatment,” Progress in Cardiovascular Diseases, vol. 52, no. 6, pp. 467–484, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. H. Chiodi, “Respiratory adaptations to chronic high altitude hypoxia,” Journal of Applied Physiology, vol. 10, no. 1, pp. 81–87, 1957. View at Publisher · View at Google Scholar
  13. J. J. Larsen, J. M. Hansen, N. V. Olsen, H. Galbo, and F. Dela, “The effect of altitude hypoxia on glucose homeostasis in men,” The Journal of Physiology, vol. 504, no. 1, pp. 241–249, 1997. View at Publisher · View at Google Scholar · View at Scopus
  14. E. J. Lee, L. C. Alonso, D. Stefanovski et al., “Time-dependent changes in glucose and insulin regulation during intermittent hypoxia and continuous hypoxia,” European Journal of Applied Physiology, vol. 113, no. 2, pp. 467–478, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. O. Castillo, O. O. Woolcott, E. Gonzales et al., “Residents at high altitude show a lower glucose profile than sea-level residents throughout 12-hour blood continuous monitoring,” High Altitude Medicine & Biology, vol. 8, no. 4, pp. 307–311, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. J. L. Santos, F. Perez-Bravo, E. Carrasco, M. Calvillan, and C. Albala, “Low prevalence of type 2 diabetes despite a high average body mass index in the Aymara natives from Chile,” Nutrition, vol. 17, no. 4, pp. 305–309, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. V. Lecoultre, C. M. Peterson, J. D. Covington et al., “Ten nights of moderate hypoxia improves insulin sensitivity in obese humans,” Diabetes Care, vol. 36, no. 12, pp. e197–e198, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. L. A. Sena and N. S. Chandel, “Physiological roles of mitochondrial reactive oxygen species,” Molecular Cell, vol. 48, no. 2, pp. 158–167, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. V. L. Kinnula and I. Hassinen, “Effect of chronic hypoxia on hepatic triacylglycerol concentration and mitochondrial fatty acid oxidizing capacity in liver and heart,” Acta Physiologica Scandinavica, vol. 102, no. 1, pp. 64–73, 1978. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Chen, Y. Gao, W. Liao, J. Huang, and W. Gao, “Hypoxia affects mitochondrial protein expression in rat skeletal muscle,” OMICS, vol. 16, no. 3, pp. 98–104, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. J. L. Gamboa and F. H. Andrade, “Muscle endurance and mitochondrial function after chronic normobaric hypoxia: contrast of respiratory and limb muscles,” Pflügers Archiv - European Journal of Physiology, vol. 463, no. 2, pp. 327–338, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. K. M. Oltmanns, H. Gehring, S. Rudolf et al., “Hypoxia causes glucose intolerance in humans,” American Journal of Respiratory and Critical Care Medicine, vol. 169, no. 11, pp. 1231–1237, 2004. View at Publisher · View at Google Scholar
  23. J. L. Gamboa, M. L. Garcia-Cazarin, and F. H. Andrade, “Chronic hypoxia increases insulin-stimulated glucose uptake in mouse soleus muscle,” American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, vol. 300, no. 1, pp. R85–R91, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. L. M. Sparks, H. Xie, R. A. Koza et al., “A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle,” Diabetes, vol. 54, no. 7, pp. 1926–1933, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. S. S. Ali, M. Hsiao, H. W. Zhao, L. L. Dugan, G. G. Haddad, and D. Zhou, “Hypoxia-adaptation involves mitochondrial metabolic depression and decreased ROS leakage,” PLoS One, vol. 7, no. 5, article e36801, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. G. Solaini, A. Baracca, G. Lenaz, and G. Sgarbi, “Hypoxia and mitochondrial oxidative metabolism,” Biochimica et Biophysica Acta (BBA) - Bioenergetics, vol. 1797, no. 6-7, pp. 1171–1177, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. M. J. Campen, L. A. Shimoda, and C. P. O'Donnell, “Acute and chronic cardiovascular effects of intermittent hypoxia in C57BL/6J mice,” Journal of Applied Physiology, vol. 99, no. 5, pp. 2028–2035, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Singamsetty, Y. Watanabe, L. Guo et al., “Inorganic nitrite improves components of the metabolic syndrome independent of weight change in a murine model of obesity and insulin resistance,” The Journal of Physiology, vol. 593, no. 14, pp. 3135–3145, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. B. Kautza, H. Gomez, D. Escobar et al., “Inhaled, nebulized sodium nitrite protects in murine and porcine experimental models of hemorrhagic shock and resuscitation by limiting mitochondrial injury,” Nitric Oxide, vol. 51, pp. 7–18, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Mu, J. T. Brozinick Jr, O. Valladares, M. Bucan, and M. J. A. Birnbaum, “Role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle,” Molecular Cell, vol. 7, no. 5, pp. 1085–1094, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. G. D. Cartee, A. G. Douen, T. Ramlal, A. Klip, and J. O. Holloszy, “Stimulation of glucose transport in skeletal muscle by hypoxia,” Journal of Applied Physiology, vol. 70, no. 4, pp. 1593–1600, 1991. View at Publisher · View at Google Scholar
  32. J. L. Azevedo Jr, J. O. Carey, W. J. Pories, P. G. Morris, and G. L. Dohm, “Hypoxia stimulates glucose transport in insulin-resistant human skeletal muscle,” Diabetes, vol. 44, no. 6, pp. 695–698, 1995. View at Publisher · View at Google Scholar
  33. T. Costa Leite, D. Da Silva, R. Guimaraes Coelho, P. Zancan, and M. Sola-Penna, “Lactate favours the dissociation of skeletal muscle 6-phosphofructo-1-kinase tetramers down-regulating the enzyme and muscle glycolysis,” The Biochemical Journal, vol. 408, no. 1, pp. 123–130, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. J. A. Pospisilik, C. Knauf, N. Joza et al., “Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes,” Cell, vol. 131, no. 3, pp. 476–491, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. T. R. Koves, J. R. Ussher, R. C. Noland et al., “Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance,” Cell Metabolism, vol. 7, no. 1, pp. 45–56, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. R. S. Surwit, C. M. Kuhn, C. Cochrane, J. A. McCubbin, and M. N. Feinglos, “Diet-induced type II diabetes in C57BL/6J mice,” Diabetes, vol. 37, no. 9, pp. 1163–1167, 1988. View at Publisher · View at Google Scholar
  37. J. D. MacDougall, H. J. Green, J. R. Sutton et al., “Structural adaptations in skeletal muscle in response to extreme simulated altitude,” Acta Physiologica Scandinavica, vol. 142, no. 3, pp. 421–427, 1991. View at Publisher · View at Google Scholar
  38. H. Hoppeler, E. Kleinert, C. Schlegel et al., “Morphological adaptations of human skeletal muscle to chronic hypoxia,” International Journal of Sports Medicine, vol. 11, no. S 1, pp. S3–S9, 1990. View at Publisher · View at Google Scholar
  39. M. Kinoshita, G. Tomonaga, T. Hoshino, K. Kin, and R. Kusukawa, “Proceedings: clinical studies of mitral valve insufficiency due to ruptured chordae tendineae,” Japanese Circulation Journal, vol. 39, p. 840, 1975. View at Google Scholar
  40. P. Jakobsson, L. Jorfeldt, and J. Henriksson, “Metabolic enzyme activity in the quadriceps femoris muscle in patients with severe chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 151, no. 2, pp. 374–377, 1995. View at Publisher · View at Google Scholar
  41. A. Hjalmarsen, U. Aasebo, K. Birkeland, G. Sager, and R. Jorde, “Impaired glucose tolerance in patients with chronic hypoxic pulmonary disease,” Diabetes & Metabolism, vol. 22, no. 1, pp. 37–42, 1996. View at Google Scholar