258
Views
3
CrossRef citations to date
0
Altmetric
Research Article

Physiological and oxidative stress responses to intermittent hypoxia training in Sprague Dawley rats

, ORCID Icon, , &
Pages 376-392 | Received 09 Jun 2020, Accepted 05 Sep 2020, Published online: 15 Sep 2020

References

  • Hackett PH, Roach RC. High-altitude illness. N Engl J Med. 2001;345(2):107–114. doi:10.1056/NEJM200107123450206.
  • Muza SR. Military applications of hypoxic training for high-altitude operations. Med Sci Sports Exercise. ;39(9):1625-1631. doi:10.1249/mss.0b013e3180de49fe.
  • Nafstad P, Stigum H, Wu T, Haldorsen OD, Ommundsen K, Bjertness E. Acute mountain sickness among tourists visiting the high-altitude city of Lhasa at 3658 m above sea level: a cross-sectional study. Arch Public Health. 2016;74(1):23. doi:10.1186/s13690-016-0134-z.
  • Maggiorini M, Bühler B, Walter M, Oelz O. Prevalence of acute mountain sickness in the Swiss Alps. BMJ. 1990;301(6756):853–855. doi:10.1136/bmj.301.6756.853.
  • Roach RC, Loeppky JA, Icenogle MV. Acute mountain sickness: increased severity during simulated altitude compared with normobaric hypoxia. J Appl Physiol. 1996;81(5):1908–1910. doi:10.1152/jappl.1996.81.5.1908.
  • Gallagher SA, Hackett PH. High-altitude illness. Emerg Med Clin North Am. 2004;22(2):329–355. doi:10.1016/j.emc.2004.02.001.
  • Dean A, Yip R, Hoffmann R. High incidence of mild acute mountain sickness in conference attendees at 10,000 foot altitude. J Wilderness Med. 1990;1(2):86–92. doi:10.1580/0953-9859-1.2.86.
  • Montgomery AB, Mills J, Luce JM. Incidence of acute mountain sickness at intermediate altitude. JAMA. 1989;261(5):732–734. doi: 10.1001/jama.1989.03420050082044.
  • Schneider M, Bernasch D, Weymann J, Holle R, Bartsch P. Acute mountain sickness: influence of susceptibility, preexposure, and ascent rate. Med Sci Sports Exerc. 2002;34(12):1886–1891. doi:10.1097/00005768-200212000-00005.
  • Beidleman BA, Muza SR, Fulco CS, et al. Intermittent altitude exposures improve muscular performance at 4,300 m. J Appl Physiol. 2003;95(5):1824–1832. doi:10.1152/japplphysiol.01160.2002.
  • Moraga FA, López I, Morales A, Soza D, Noack J. The effect of oxygen enrichment on cardiorespiratory and neuropsychological responses in workers with chronic intermittent exposure to high altitude (ALMA, 5,050 m). Front Physiol. 2018; 9:187. doi:10.3389/fphys.2018.00187.
  • Marzatico F, Curti D, Dagani F, Tagliti M, Benzi G. Brain enzyme adaptation to mild normobaric intermittent hypoxia. J Neurosci Res. 1986; 16(2):419–428. doi:10.1002/jnr.490160209.
  • Fulco CS, Rock PB, Cymerman A. Improving athletic performance: is altitude residence or altitude training helpful?. Aviat Space Environ Med. 2000;71(2):162–171.
  • Meerson F, Ustinova E, Manukhina E. Prevention of cardiac arrhythmias by adaptation to hypoxia: regulatory mechanisms and cardiotropic effect. Biomed Biochim Acta. 1989;48(2-3):S83–S88.
  • Kitaev M, Aĭtbaev K, Liamtsev V. Effect of hypoxic hypoxia on development of atherosclerosis in rabbits. Aviakosmicheskaiaiekologicheskaiameditsina = Aerospace Environ Med. 1999;33(5):54–57. doi:10.1016/0021-9150(83)90070-9.
  • Prabhakar NR. Invited Review: Oxygen sensing during intermittent hypoxia: cellular and molecular mechanisms. J Appl Physiol. 2001;90(5):1986–1994. doi: 10.1152/jappl.2001.90.5.1986
  • Lin H, Wang C, Niu K, et al. Hypobaric hypoxia preconditioning attenuates acute lung injury during high-altitude exposure in rats via up-regulating heat-shock protein. Clin Sci. 2011;121(5):223–231. ). 70. 231, doi:10.1042/CS20100596.
  • Bhaumik G, Dass D, Ghosh D, et al. Effect of intermittent normobaric hypoxia exposures on acute mountain sickness during acute ascent to 3500 m in Indian Army Personnel. Defence Life Sci J. 2018;3:209–215. doi:10.14429/dlsj.3.12906.
  • Gangwar A, Sharma M, Singh K, et al. Intermittent normobaric hypoxia facilitates high altitude acclimatization by curtailing hypoxia-induced inflammation and dyslipidemia. PflügersArchiv-Eur J Physiol. 2019;471(7):949–959. doi:10.1007/s00424-019-02273-4.
  • Burtscher M, Brandstätter E, Gatterer H. Preacclimatization in simulated altitudes. Sleep Breath. 2008;12(2):109–114. doi:10.1007/s11325-007-0127-9.
  • Levine B, Stray-Gundersen J. A practical approach to altitude training. Int J Sports Med. 1992;13(S 1):S209–S212. doi:10.1055/s-2007-1024642.
  • Ventura M, Jordi I, Ferran A. Intermittent hypobaric hypoxia induces altitude acclimation and improves the lactate threshold. Aviat Space Environ Med. 2000;71(2):125–130.
  • Lipman GS, Kanaan NC, Phillips C, et al. Study looking at end expiratory pressure for altitude illness decrease (SLEEP-AID). High Altitude Med Biol. 2015;16(2):154–161. doi:10.1089/ham.2014.1110.
  • Beidleman BA, Muza SR, Fulco CS, et al. Intermittent altitude exposures reduce acute mountain sickness at 4300 m. Clin Sci. 2004;106(3):321–328. doi:10.1042/CS20030161.
  • Muza SR, Beidleman BA, Fulco CS. Altitude preexposure recommendations for inducing acclimatization. High Altitude Med Biol. 2010;11(2):87–92. doi:10.1089/ham.2010.1006.
  • Sarada S, Himadri P, Mishra C, Geetali P, Ram MS, Ilavazhagan G. Role of oxidative stress and NFkB in hypoxia-induced pulmonary edema. Exp Biol Med (Maywood). 2008;233(9):1088–1098. doi:10.3181/0712-RM-337.
  • Strohl K, Baekey D, Dase S, Hete B. Validation of the MouseOx arterial oxygen saturation measurements. Oakmont, PA: Starr Life Sciences Corp. 2007.
  • LeBel CP, Ischiropoulos H, Bondy SC. Evaluation of the probe 2',7'-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress . Chem Res Toxicol. 1992;5(2):227–231. doi:10.1021/tx00026a012.
  • Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95(2):351–358. doi:10.1016/0003-2697(79)90738-3.
  • Beytut E, Sözmen M, Ergínsoy S. Immunohistochemical detection of pulmonary surfactant proteins and retroviral antigens in the lungs of sheep with pulmonary adenomatosis. J Comp Pathol. 2009;140(1):43–53. doi:10.1016/j.jcpa.2008.10.003.
  • Morgan BJ, Adrian R, Bates ML, Dopp JM, Dempsey JA. Quantifying hypoxia-induced chemoreceptor sensitivity in the awake rodent. J Appl Physiol. 2014;117(7):816–‐824. doi:10.1152/japplphysiol.00484.2014.
  • Semenza GL. Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol. 1999;15(1):551–578. doi:10.1146/annurev.cellbio.15.1.551.
  • DE Daly MB, Scott MJ. The effects of stimulation of the carotid body chemoreceptors on heart rate in the dog. J Physiol (Lond). 1958;144(1):148–166. doi: 10.1113/jphysiol.1958.sp006092.
  • Semenza GL. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology (Bethesda). 2004;19(4):176–182. doi:10.1152/physiol.00001.2004.
  • Prabhakar NR, Semenza GL. Gaseous messengers in oxygen sensing. J Mol Med. 2012;90(3):265–272. doi:10.1007/s00109-012-0876-1.
  • Rowell LB, Johnson DG, Chase PB, Comess KA, Seals DR. Hypoxemia raises muscle sympathetic activity but not norepinephrine in resting humans. J Appl Physiol. 1989;66(4):1736–1743. doi:10.1152/jappl.1989.66.4.1736.
  • Heinonen IH, Boushel R, Kalliokoski KK. The circulatory and metabolic responses to hypoxia in Humans - With Special Reference to Adipose Tissue Physiology and Obesity. Front Endocrinol (Lausanne). 2016;7:116doi:10.3389/fendo.2016.00116.
  • Floras JS. Clinical aspects of sympathetic activation and parasympathetic withdrawal in heart failure. J Am Coll Cardiol . 1993;22(4):A72–A84. doi:10.1016/0735-1097(93)90466-E.
  • Halliwill JR, Morgan BJ, Charkoudian N. Peripheral chemoreflex and baroreflex interactions in cardiovascular regulation in humans. J Physiol. 2003;552(1):295–302. doi:10.1113/jphysiol.2003.050708.
  • West JB. Human responses to extreme altitudes. Integr Comp Biol. 2006;46(1):25–34. doi:10.1093/icb/icj005.
  • Bernardi L, Passino C, Wilmerding V, et al. Breathing patterns and cardiovascular autonomic modulation during hypoxia induced by simulated altitude. J Hypertens. 2001;19(5):947–958. doi:10.1097/00004872-200105000-00016.
  • Weir EK, López-Barneo J, Buckler KJ, Archer SL. Acute oxygen-sensing mechanisms. N Engl J Med. 2005;353(19):2042–2055. doi:10.1056/NEJMra050002.
  • Bakonyi T, Radak Z. High altitude and free radicals. J Sports Sci Med. 2004;3(2):64–69.
  • Prabhakar NR. Sleep apneas: an oxidative stress?. Am J Respir Crit Care Med. 2002;165(7):859–860. doi:10.1164/ajrccm.165.7.2202030c.
  • da Rosa DP, Forgiarini LF, Baronio D, Feijó CA, Martinez D, Marroni NP. Simulating sleep apnea by exposure to intermittent hypoxia induces inflammation in the lung and liver. Mediators Inflamm. 2012;2012:879419–879418. doi:10.1155/2012/79419.
  • Yasunari K, Maeda K, Nakamura M, Yoshikawa J. Oxidative stress in leukocytes is a possible link between blood pressure, blood glucose, and C-reacting protein. Hypertension. 2002;39(3):777–780. doi:10.1161/hy0302.104670.
  • Abramson JL, Hooper WC, Jones DP, et al. Association between novel oxidative stress markers and C-reactive protein among adults without clinical coronary heart disease. Atherosclerosis. 2005;178(1):115–121. doi:10.1016/j.atherosclerosis.2004.08.007.
  • Lee D-H, Jacobs DR. Association between serum gamma-glutamyltransferase and C-reactive protein. Atherosclerosis. 2005;178(2):327–330. doi:10.1016/j.atherosclerosis.2004.08.027.
  • Sasaki R, Ikura K, Sugimoto E, Chiba H. Purification of bisphosphoglyceromutase, 2,3-bisphosphoglycerate phosphatase and phosphoglyceromutase from human erthrocytes. Three enzyme activities in one protein . Eur J Biochem. 1975;50(3):581–593. doi:10.1111/j.1432-1033.1975.tb09899.x.
  • Moore LG, Brewer GJ. Biochemical mechanisms of red blood cell 2,3-diphosphoglycerate increase at high altitude . Am J Phys Anthropol. 1980;53(1):11–18. doi:10.1002/ajpa.1330530104.
  • Himadri P, Tirpude RJ, Singh SB, Singh SN, Salhan AK, Kumar B. Erythroxylum Coca In High Altitude Acclimatization And Endurance Performance. Br J Pharmaceut Med Res. ;4:1748–1763. doi:10.24942/bjpmr.2019.451.
  • Benesch R, Benesch RE. Oxygenation and ion transport in red cells. Science. 1968;160(3823):83doi:10.1126/science.160.3823.83.
  • Lenfant C, Torrance J, English E, et al. Effect of altitude on oxygen binding by hemoglobin and on organic phosphate levels. J Clin Invest. 1968;47(12):2652–2656. doi:10.1172/jci105948.
  • Bunn HF, Poyton RO. Oxygen sensing and molecular adaptation to hypoxia. Physiol Rev. 1996;76(3):839–885. doi:10.1152/physrev.1996.76.3.839.
  • Cavadas MA, Mesnieres M, Crifo B, Manresa MC, et al. REST mediates resolution of HIF-dependent gene expression in prolonged hypoxia. Sci Rep. 2015;5:17851doi:10.1038/srep17851.
  • Eltzschig HK, Carmeliet P. Hypoxia and inflammation. N Engl J Med. 2011;364(7):656–665. doi:10.1056/NEJMra0910283.
  • Haddad JJ, Harb HL. Cytokines and the regulation of hypoxia-inducible factor (HIF)-1alpha. Int Immunopharmacol. 2005;5(3):461–483. doi:10.1016/j.intimp.2004.11.009.
  • Mojsilovic-Petrovic J, Callaghan D, Cui H, Dean C, Stanimirovic DB, Zhang W. Hypoxia-inducible factor-1 (HIF-1) is involved in the regulation of hypoxia-stimulated expression of monocyte chemoattractant protein-1 (MCP-1/CCL2) and MCP-5 (Ccl12) in astrocytes. J Neuroinflamm. 2007;4(1):12. doi:10.1186/1742-2094-4-12.
  • Eckardt K-U, Boutellier U, Kurtz A, Schopen M, Koller EA, Bauer C. Rate of erythropoietin formation in humans in response to acute hypobaric hypoxia. J Appl Physiol. 1989;66(4):1785–1788. doi:10.1152/jappl.1989.66.4.1785.
  • Semenza GL, Wang GL. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol. 1992;12(12):5447–5454. doi:10.1128/mcb.12.12.5447.
  • Rankin EB, Biju MP, Liu Q, et al. Hypoxia-inducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo . J Clin Invest. 2007;117(4):1068–1077. doi:10.1172/JCI30117.
  • Kapitsinou PP, Liu Q, Unger TL, et al. Hepatic HIF-2 regulates erythropoietic responses to hypoxia in renal anemia. J Amer Soc Hematol. 2010;116(16):3039–3048. doi:10.1182/blood-2010-02-270322.
  • Manalo DJ, Rowan A, Lavoie T, et al. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood. 2005;105(2):659–669. doi:10.1182/blood-2004-07-2958.
  • Lukiw WJ, Ottlecz A, Lambrou G, et al. Coordinate activation of HIF-1 and NF-kappaB DNA binding and COX-2 and VEGF expression in retinal cells by hypoxia . Invest Ophthalmol Vis Sci. 2003;44(10):4163–4170. doi:10.1167/iovs.02-0655.
  • Schoch HJ, Fischer S, Marti HH. Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain . Brain. 2002;125(Pt 11):2549–2557. doi:10.1093/brain/awf257.
  • Purushothaman J, Suryakumar G, Shukla D, et al. Modulatory effects of seabuckthorn (Hippophae rhamnoides L.) in hypobaric hypoxia induced cerebral vascular injury. Brain Res Bull. 2008;77(5):246–252. doi:10.1016/j.brainresbull.2008.08.026.
  • Kaner RJ, Ladetto JV, Singh R, Fukuda N, Matthay MA, Crystal RG. Lung overexpression of the vascular endothelial growth factor gene induces pulmonary edema. Am J Respir Cell Mol Biol. 2000;22(6):657–664. doi:10.1165/ajrcmb.22.6.3779.
  • Sagi S, Mathew T, Patir H. Prophylactic administration of curcumin abates the incidence of hypobaric hypoxia induced pulmonary edema in rats: a molecular approach. J Pulm Respir Med. 2014;4:1000164. doi:10.4172/2161-105X.1000164.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.