Nitric oxide deficit in chronic intermittent hypoxia impairs large conductance calcium-activated potassium channel activity in rat hippocampal neurons

Free Radical Biology and Medicine

Volumn 44, Issue 4, 2008, Pages 547-557

  Tjong, Yung Wui ^a   Li, Meifang ^a   Hung, Ming Wai ^a   Wang, Kun ^a   Fung, Man Lung ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Hippocampus; Intermittent hypoxia; Nitric oxide; Potassium channel; S Nitrosylation; Sleep apnea

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 8 BROMO CYCLIC GMP; CALCIUM; CALCIUM ACTIVATED POTASSIUM CHANNEL; CYCLIC GMP; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRIC OXIDE DONOR; NITROPRUSSIDE SODIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DYSFUNCTION; BRAIN INJURY; BRAIN NERVE CELL; BRAIN REGION; BRAIN SLICE; CALCIUM CELL LEVEL; CHRONIC INTERMITTENT HYPOXIA; CONTROLLED STUDY; DISSOCIATION; DOWN REGULATION; ELECTROCHEMISTRY; HIPPOCAMPUS; HYPOXIA; NITROSYLATION; NONHUMAN; PATCH CLAMP; POTASSIUM CONDUCTANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSOR; SLEEP APNEA SYNDROME; SPECTROFLUOROMETRY;

ANIMALS; ANOXIA; CALCIUM; CHRONIC DISEASE; COENZYMES; HIPPOCAMPUS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE TYPE I; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; UBIQUINONE;

RATTUS;

EID: 38749113411     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2007.10.033     Document Type: Article

References (40)

1. Bass J.L., Corwin M., Gozal D., Moore C., Nishida H., Parker S., Schonwald A., Wilker R.E., Stehle S., and Kinane T.B. The effect of chronic or intermittent hypoxia on cognition in childhood: a review of the evidence. Pediatrics 114 (2004) 805-816
2. Gozal D., and Kheirandish L. Sleepiness and neurodegeneration in sleep-disordered breathing: convergence of signaling cascades. Am. J. Respir. Crit. Care Med. 171 (2005) 1325-1327
3. O'Brien L.M., and Gozal D. Neurocognitive dysfunction and sleep in children: from human to rodent. Pediatr. Clin. North Am. 51 (2004) 187-202
4. Ray R.M., and Bower C.M. Pediatric obstructive sleep apnea: the year in review. Curr. Opin. Otolaryngol. Head Neck Surg. 13 (2005) 360-365
5. Li R.C., Row B.W., Kheirandish L., Brittian K.R., Gozal E., Guo S.Z., Sachleben Jr. L.R., and Gozal D. Nitric oxide synthase and intermittent hypoxia-induced spatial learning deficits in the rat. Neurobiol. Dis. 17 (2004) 44-53
6. Payne R.S., Goldbart A., Gozal D., and Schurr A. Effect of intermittent hypoxia on long-term potentiation in rat hippocampal slices. Brain Res. 1029 (2004) 195-199
7. Row B.W., Liu R., Xu W., Kheirandish L., and Gozal D. Intermittent hypoxia is associated with oxidative stress and spatial learning deficits in the rat. Am. J. Respir. Crit. Care Med. 167 (2003) 1548-1553
8. Liu H., Moczydlowski E., and Haddad G.G. O(2) deprivation inhibits Ca(2+)-activated K(+) channels via cytosolic factors in mice neocortical neurons. J. Clin. Invest. 104 (1999) 577-588
9. McCartney C.E., McClafferty H., Huibant J.M., Rowan E.G., Shipston M.J., and Rowe I.C. A cysteine-rich motif confers hypoxia sensitivity to mammalian large conductance voltage- and Ca-activated K (BK) channel alpha-subunits. Proc. Natl. Acad. Sci U. S. A. 102 (2005) 17870-17876
10. Jaffrey S.R., Erdjument-Bromage H., Ferris C.D., Tempst P., and Snyder S.H. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat. Cell Biol. 3 (2001) 193-197
11. Wang G., Moniri N.H., Ozawa K., Stamler J.S., and Daaka Y. Nitric oxide regulates endocytosis by S-nitrosylation of dynamin. Proc. Natl. Acad. Sci U. S. A. 103 (2006) 1295-1300
12. Hess D.T., Matsumoto A., Kim S.O., Marshall H.E., and Stamler J.S. Protein S-nitrosylation: purview and parameters. Nat. Rev., Mol. Cell Biol. 6 (2005) 150-166
13. 2+ channels by S-nitrosylation in rat hippocampal neurons during severe hypoxia and in vitro ischemia. Free Radic. Biol. Med. 42 (2007) 52-63
14. Kato M., Roberts-Thomson P., Phillips B.G., Haynes W.G., Winnicki M., Accurso V., and Somers V.K. Impairment of endothelium-dependent vasodilation of resistance vessels in patients with obstructive sleep apnea. Circulation 102 (2000) 2607-2610
15. Suzuki Y.J., Jain V., Park A.M., and Day R.M. Oxidative stress and oxidant signaling in obstructive sleep apnea and associated cardiovascular diseases. Free Radic. Biol. Med. 40 (2006) 1683-1692
16. Lavie L., Hefetz A., Luboshitzky R., and Lavie P. Plasma levels of nitric oxide and L-arginine in sleep apnea patients: effects of nCPAP treatment. J. Mol. Neurosci. 21 (2003) 57-63
17. Lattimore J.L., Wilcox I., Skilton M., Langenfeld M., and Celermajer D.S. Treatment of obstructive sleep apnoea leads to improved microvascular endothelial function in the systemic circulation. Thorax 61 (2006) 491-495
18. Zhan G., Fenik P., Pratico D., and Veasey S.C. Inducible nitric oxide synthase in long-term intermittent hypoxia: hypersomnolence and brain injury. Am. J. Respir. Crit. Care Med. 171 (2005) 1414-1420
19. Gao T.M., and Fung M.L. Decreased large conductance Ca(2+)-activated K(+) channel activity in dissociated CA1 hippocampal neurons in rats exposed to perinatal and postnatal hypoxia. Neurosci. Lett. 332 (2002) 163-166
20. Gu X.Q., and Haddad G.G. Maturation of neuronal excitability in hippocampal neurons of mice chronically exposed to cyclic hypoxia. Am. J. Physiol., Cell Physiol. 284 (2003) C1156-C1163
21. Ye J.S., Tipoe G.L., Fung P.C., and Fung M.L. Augmentation of hypoxia-induced nitric oxide generation in the rat carotid body adapted to chronic hypoxia: an involvement of constitutive and inducible nitric oxide synthases. Pflugers Arch. 444 (2002) 178-185
22. Liu P., Smith P.F., Appleton I., Darlington C.L., and Bilkey D.K. Regional variations and age-related changes in nitric oxide synthase and arginase in the sub-regions of the hippocampus. Neuroscience 119 (2003) 679-687
23. Ghatta S., Nimmagadda D., Xu X., and O'Rourke S.T. Large-conductance, calcium-activated potassium channels: structural and functional implications. Pharmacol. Ther. 110 (2006) 103-116
24. Lu R., Alioua A., Kumar Y., Eghbali M., Stefani E., and Toro L. MaxiK channel partners: physiological impact. J. Physiol. 570 (2006) 65-72
25. Calderone V. Potassium channels. Curr. Top. Med. Chem. 6 (2006) 997
26. Ahern G.P., Hsu S.F., and Jackson M.B. Direct actions of nitric oxide on rat neurohypophysial K+ channels. J. Physiol. 520 Pt 1 (1999) 165-176
27. Lee J.E., Kwak J., Suh C.K., and Shin J.H. Dual effects of nitric oxide on the large conductance calcium-activated potassium channels of rat brain. J. Biochem. Mol. Biol. 39 (2006) 91-96
28. Gragasin F.S., Michelakis E.D., Hogan A., Moudgil R., Hashimoto K., Wu X., Bonnet S., Haromy A., and Archer S.L. The neurovascular mechanism of clitoral erection: nitric oxide and cGMP-stimulated activation of BKCa channels. FASEB J. 18 (2004) 1382-1391
29. Tanaka Y., Koike K., and Toro L. MaxiK channel roles in blood vessel relaxations induced by endothelium-derived relaxing factors and their molecular mechanisms. J. Smooth Muscle Res. 40 (2004) 125-153
30. 2+-activated K+ (BKCa) channels in myocytes of the guinea-pig taenia caeca. Br. J. Pharmacol. 139 (2003) 1153-1163
31. Guix F.X., Uribesalgo I., Coma M., and Munoz F.J. The physiology and pathophysiology of nitric oxide in the brain. Prog. Neurobiol. 76 (2005) 126-152
32. Michel T., and Feron O. Nitric oxide synthases: which, where, how, and why?. J. Clin. Invest. 100 (1997) 2146-2152
33. 2+-dependent K+ channels in spike broadening during repetitive firing in rat hippocampal pyramidal cells. J. Physiol. 521 Pt 1 (1999) 135-146
34. Gong L., Gao T.M., Li X., Huang H., and Tong Z. Enhancement in activities of large conductance calcium-activated potassium channels in CA1 pyramidal neurons of rat hippocampus after transient forebrain ischemia. Brain Res. 884 (2000) 147-154
35. Gong L., Gao T.M., Huang H., and Tong Z. Redox modulation of large conductance calcium-activated potassium channels in CA1 pyramidal neurons from adult rat hippocampus. Neurosci. Lett. 286 (2000) 191-194
36. Tang X.D., Garcia M.L., Heinemann S.H., and Hoshi T. Reactive oxygen species impair Slo1 BK channel function by altering cysteine-mediated calcium sensing. Nat. Struct. Mol. Biol. 11 (2004) 171-178
37. Tang X.D., Daggett H., Hanner M., Garcia M.L., McManus O.B., Brot N., Weissbach H., Heinemann S.H., and Hoshi T. Oxidative regulation of large conductance calcium-activated potassium channels. J. Gen. Physiol. 117 (2001) 253-274
38. 2+-dependent K+ channels. Biochem. Biophys. Res. Commun. 342 (2006) 1389-1395
39. 2+-activated K+ channels. J. Physiol. 571 (2006) 329-348
40. Xu W., Chi L., Row B.W., Xu R., Ke Y., Xu B., Luo C., Kheirandish L., Gozal D., and Liu R. Increased oxidative stress is associated with chronic intermittent hypoxia-mediated brain cortical neuronal cell apoptosis in a mouse model of sleep apnea. Neuroscience 126 (2004) 313-323