Dichotomous effects of chronic intermittent hypoxia on focal cerebral ischemic injury

Stroke

Volumn 45, Issue 5, 2014, Pages 1460-1467

  Jackman, Katherine A ^a   Zhou, Ping ^a   Faraco, Giuseppe ^a   Peixoto, Pablo M ^a,c   Coleman, Christal ^a   Voss, Henning U ^b   Pickel, Virginia ^a   Manfredi, Giovanni ^a   Iadecola, Costantino ^a  

^a FEIL FAMILY BRAIN AND MIND RESEARCH INSTITUTE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Free radicals; Mitochondria; Sleep apnea syndromes; Stroke

Indexed keywords

CALCIUM ION; ERYTHROPOIETIN; GLUCOSE TRANSPORTER 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; REACTIVE OXYGEN METABOLITE; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN BLOOD FLOW; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN MITOCHONDRION; CHRONIC INTERMITTENT HYPOXIA; CONTROLLED STUDY; ENCEPHALE ISOLE; GENE EXPRESSION; LASER DOPPLER FLOWMETRY; MALE; MEMBRANE DEPOLARIZATION; MIDDLE CEREBRAL ARTERY OCCLUSION; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NEUROPROTECTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SPIN LABELING; TISSUE INJURY;

FREE RADICALS; MITOCHONDRIA; SLEEP APNEA SYNDROMES; STROKE;

ANIMALS; ANOXIA; CEREBROVASCULAR CIRCULATION; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; INFARCTION, MIDDLE CEREBRAL ARTERY; LASER-DOPPLER FLOWMETRY; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; REACTIVE OXYGEN SPECIES;

EID: 84899920062     PISSN: 00392499     EISSN: 15244628     Source Type: Journal    
DOI: 10.1161/STROKEAHA.114.004816     Document Type: Article

References (47)

1. Young T, Palta M, Dempsey J, Skatrud J, Weber S, Badr S. The occurrence of sleep-disordered breathing among middle-aged adults. N Engl J Med. 1993;328:1230-1235.
2. Dempsey JA, Veasey SC, Morgan BJ, O'Donnell CP. Pathophysiology of sleep apnea. Physiol Rev. 2010;90:47-112.
3. Durgan DJ, Bryan RM Jr. Cerebrovascular consequences of obstructive sleep apnea. J Am Heart Assoc. 2012;1:e000091.
4. Yaggi HK, Concato J, Kernan WN, Lichtman JH, Brass LM, Mohsenin V. Obstructive sleep apnea as a risk factor for stroke and death. N Engl J Med. 2005;353:2034-2041.
5. Redline S, Yenokyan G, Gottlieb DJ, Shahar E, O'Connor GT, Resnick HE, et al. Obstructive sleep apnea-hypopnea and incident stroke: the sleep heart health study. Am J Respir Crit Care Med. 2010;182:269-277.
6. Veasey S. Insight from animal models into the cognitive consequences of adult sleep-disordered breathing. ILAR J. 2009;50:307-311.
7. Capone C, Faraco G, Coleman C, Young CN, Pickel VM, Anrather J, et al. Endothelin 1-dependent neurovascular dysfunction in chronic intermittent hypoxia. Hypertension. 2012;60:106-113.
8. Culebras A. Sleep and stroke. Semin Neurol. 2009;29:438-445.
9. Phillips SA, Olson EB, Morgan BJ, Lombard JH. Chronic intermittent hypoxia impairs endothelium-dependent dilation in rat cerebral and skeletal muscle resistance arteries. Am J Physiol Heart Circ Physiol. 2004;286:H388-H393.
10. Crossland RF, Durgan DJ, Lloyd EE, Phillips SC, Reddy AK, Marrelli SP, et al. A new rodent model for obstructive sleep apnea: effects on ATP- mediated dilations in cerebral arteries. Am J Physiol Regul Integr Comp Physiol. 2013;305:R334-R342.
11. Stowe AM, Altay T, Freie AB, Gidday JM. Repetitive hypoxia extends endogenous neurovascular protection for stroke. Ann Neurol. 2011;69:975-985.
12. Lavie P, Lavie L, Herer P. All-cause mortality in males with sleep apnoea syndrome: declining mortality rates with age. Eur Respir J. 2005;25:514-520.
13. Lavie L, Lavie P. Ischemic preconditioning as a possible explanation for the age decline relative mortality in sleep apnea. Med Hypotheses. 2006;66:1069-1073.
14. Park AM, Suzuki YJ. Effects of intermittent hypoxia on oxidative stress-induced myocardial damage in mice. J Appl Physiol (1985). 2007;102:1806-1814.
15. Joyeux-Faure M, Stanke-Labesque F, Lefebvre B, Béguin P, Godin- Ribuot D, Ribuot C, et al. Chronic intermittent hypoxia increases infarction in the isolated rat heart. J Appl Physiol (1985). 2005;98:1691-1696.
16. Milano G, Abruzzo PM, Bolotta A, Marini M, Terraneo L, Ravara B, et al. Impact of the phosphatidylinositide 3-kinase signaling pathway on the cardioprotection induced by intermittent hypoxia. PLoS One. 2013;8:e76659.
17. Wang ZH, Cai XL, Wu L, Yu Z, Liu JL, Zhou ZN, et al. Mitochondrial energy metabolism plays a critical role in the cardioprotection afforded by intermittent hypobaric hypoxia. Exp Physiol. 2012;97:1105-1118.
18. Kolár F, Neckár J, Ostádal B. MCC-134, a blocker of mitochondrial and opener of sarcolemmal ATP-sensitive K+ channels, abrogates cardioprotective effects of chronic hypoxia. Physiol Res. 2005;54:467-471.
19. Davis EM, O'Donnell CP. Rodent models of sleep apnea. Respir Physiol Neurobiol. 2013;188:355-361.
20. Coleman CG, Wang G, Park L, Anrather J, Delagrammatikas GJ, Chan J, et al. Chronic intermittent hypoxia induces NMDA receptor-dependent plasticity and suppresses nitric oxide signaling in the mouse hypothalamic paraventricular nucleus. J Neurosci. 2010;30:12103-12112.
21. Boland LL, Shahar E, Iber C, Knopman DS, Kuo TF, Nieto FJ; Sleep Heart Health Study (SHHS) Investigators. Measures of cognitive function in persons with varying degrees of sleep-disordered breathing: the Sleep Heart Health Study. J Sleep Res. 2002;11:265-272.
22. Jackman K, Kunz A, Iadecola C. Modeling focal cerebral ischemia in vivo. Methods Mol Biol. 2011;793:195-209.
23. Jackman K, Kahles T, Lane D, Garcia-Bonilla L, Abe T, Capone C, et al. Progranulin deficiency promotes post-ischemic blood-brain barrier disruption. J Neurosci. 2013;33:19579-19589.
24. Hochrainer K, Jackman K, Anrather J, Iadecola C. Reperfusion rather than ischemia drives the formation of ubiquitin aggregates after middle cerebral artery occlusion. Stroke. 2012;43:2229-2235.
25. Abe T, Zhou P, Jackman K, Capone C, Casolla B, Hochrainer K, et al. Lipoprotein receptor-related protein-6 protects the brain from ischemic injury. Stroke. 2013;44:2284-2291.
26. Kunz A, Park L, Abe T, Gallo EF, Anrather J, Zhou P, et al. Neurovascular protection by ischemic tolerance: role of nitric oxide and reactive oxygen species. J Neurosci. 2007;27:7083-7093.
27. Abe T, Kunz A, Shimamura M, Zhou P, Anrather J, Iadecola C. The neuroprotective effect of prostaglandin E2 EP1 receptor inhibition has a wide therapeutic window, is sustained in time and is not sexually dimorphic. J Cereb Blood Flow Metab. 2009;29:66-72.
28. Kunz A, Abe T, Hochrainer K, Shimamura M, Anrather J, Racchumi G, et al. Nuclear factor-kappaB activation and postischemic inflammation are suppressed in CD36-null mice after middle cerebral artery occlusion. J Neurosci. 2008;28:1649-1658.
29. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402-408.
30. Zhou P, Qian L, Zhou T, Iadecola C. Mitochondria are involved in the neurogenic neuroprotection conferred by stimulation of cerebellar fastigial nucleus. J Neurochem. 2005;95:221-229.
31. Murphy AN, Bredesen DE, Cortopassi G, Wang E, Fiskum G. Bcl-2 potentiates the maximal calcium uptake capacity of neural cell mitochondria. Proc Natl Acad Sci U S A. 1996;93:9893-9898.
32. Starkov AA. Measurement of mitochondrial ROS production. Methods Mol Biol. 2010;648:245-255.
33. Prabhakar NR, Semenza GL. Adaptive and maladaptive cardiorespiratory responses to continuous and intermittent hypoxia mediated by hypoxia-inducible factors 1 and 2. Physiol Rev. 2012;92:967-1003.
34. Sims NR, Muyderman H. Mitochondria, oxidative metabolism and cell death in stroke. Biochim Biophys Acta. 2010;1802:80-91.
35. Douglas RM, Ryu J, Kanaan A, Del Carmen Rivero M, Dugan LL, Haddad GG, et al. Neuronal death during combined intermittent hypoxia/hypercapnia is due to mitochondrial dysfunction. Am J Physiol Cell Physiol. 2010;298:C1594-C1602.
36. Lin AM, Dung SW, Chen CF, Chen WH, Ho LT. Hypoxic preconditioning prevents cortical infarction by transient focal ischemia-reperfusion. Ann N Y Acad Sci. 2003;993:168-78, discussion 195.
37. Bernaudin M, Nedelec AS, Divoux D, MacKenzie ET, Petit E, Schumann-Bard P. Normobaric hypoxia induces tolerance to focal permanent cerebral ischemia in association with an increased expression of hypoxia-inducible factor-1 and its target genes, erythropoietin and VEGF, in the adult mouse brain. J Cereb Blood Flow Metab. 2002;22:393-403.
38. Gong SJ, Chen LY, Zhang M, Gong JX, Ma YX, Zhang JM, et al. Intermittent hypobaric hypoxia preconditioning induced brain ischemic tolerance by up-regulating glial glutamate transporter-1 in rats. Neurochem Res. 2012;37:527-537.
39. Miller BA, Perez RS, Shah AR, Gonzales ER, Park TS, Gidday JM. Cerebral protection by hypoxic preconditioning in a murine model of focal ischemia-reperfusion. Neuroreport. 2001;12:1663-1669.
40. Jackman K, Iadecola C. Neurovascular regulation in the ischemic brain [published online ahead of print March 4, 2014]. Antioxid Redox Signal. doi: 10.1089/ars.2013.5669.
41. Zhang F, Eckman C, Younkin S, Hsiao KK, Iadecola C. Increased susceptibility to ischemic brain damage in transgenic mice overexpressing the amyloid precursor protein. J Neurosci. 1997; 17: 7655-7661.
42. Iadecola C, Sugimoto K, Niwa K, Kazama K, Ross ME. Increased susceptibility to ischemic brain injury in cyclooxygenase-1-deficient mice. J Cereb Blood Flow Metab. 2001;21:1436-1441.
43. Huang Z, Huang PL, Ma J, Meng W, Ayata C, Fishman MC, et al. Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro-L-arginine. J Cereb Blood Flow Metab. 1996;16:981-987.
44. Aviles-Reyes RX, Angelo MF, Villarreal A, Rios H, Lazarowski A, Ramos AJ. Intermittent hypoxia during sleep induces reactive gliosis and limited neuronal death in rats: implications for sleep apnea. J Neurochem. 2010;112:854-869.
45. Ohga E, Tomita T, Wada H, Yamamoto H, Nagase T, Ouchi Y. Effects of obstructive sleep apnea on circulating ICAM-1, IL-8, and MCP-1. J Appl Physiol (1985). 2003;94:179-184.
46. Yokoe T, Minoguchi K, Matsuo H, Oda N, Minoguchi H, Yoshino G, 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. 2003;107:1129-1134.
47. Lemasters JJ, Theruvath TP, Zhong Z, Nieminen AL. Mitochondrial calcium and the permeability transition in cell death. Biochim Biophys Acta. 2009;1787:1395-1401.