Melatonin ameliorates hippocampal nitric oxide production and large conductance calcium-activated potassium channel activity in chronic intermittent hypoxia

Journal of Pineal Research

Volumn 44, Issue 3, 2008, Pages 234-243

  Tjong, Y W ^a   Li, M F ^a   Hung, M W ^a   Fung, M L ^a,b  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

BK channel; Hippocampus; Nitric oxide synthase; Oxidative stress; Sleep apnea

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; MALONALDEHYDE; MELATONIN; N(G) METHYLARGININE; NITRIC OXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; ELECTROCHEMICAL ANALYSIS; ELECTROPHYSIOLOGY; HIPPOCAMPUS; HYPOXIA; MALE; NONHUMAN; PATCH CLAMP; PROBABILITY; RAT;

ANIMALS; ANOXIA; HIPPOCAMPUS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MALE; MELATONIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; OMEGA-N-METHYLARGININE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 40849088098     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2007.00515.x     Document Type: Article

References (65)

1. Ryan CM, Bradley TD. Pathogenesis of obstructive sleep apnea. J Appl Physiol 2005 99 : 2440 2450.
2. Chiang AA. Obstructive sleep apnea and chronic intermittent hypoxia: a review. Chin J Physiol 2006 49 : 234 243.
3. Gozal D, Daniel JM, Dohanich GP. Behavioral and anatomical correlates of chronic episodic hypoxia during sleep in the rat. J Neurosci 2001 21 : 2442 2450.
4. O'Brien LM, Gozal D. Behavioural and neurocognitive implications of snoring and obstructive sleep apnoea in children: facts and theory. Paediatr Respir Rev 2002 3 : 3 9.
5. Halbower AC, Degaonkar M, Barker PB et al. Childhood obstructive sleep apnea associates with neuropsychological deficits and neuronal brain injury. PLoS Med 2006 3 : e301.
6. Macey PM, Henderson LA, Macey KE et al. Brain morphology associated with obstructive sleep apnea. Am J Respir Crit Care Med 2002 166 : 1382 1387.
7. Morrell MJ, McRobbie DW, Quest RA et al. Changes in brain morphology associated with obstructive sleep apnea. Sleep Med 2003 4 : 451 454.
8. Xu W, Chi L, Row BW et al. Increased oxidative stress is associated with chronic intermittent hypoxia-mediated brain cortical neuronal cell apoptosis in a mouse model of sleep apnea. Neuroscience 2004 126 : 313 323.
9. Row BW, Liu R, Xu W et al. Intermittent hypoxia is associated with oxidative stress and spatial learning deficits in the rat. Am J Respir Crit Care Med 2003 167 : 1548 1553.
10. Bartlett DJ, Rae C, Thompson CH et al. Hippocampal area metabolites relate to severity and cognitive function in obstructive sleep apnea. Sleep Med 2004 5 : 593 596.
11. Suzuki YJ, Jain V, Park AM et al. Oxidative stress and oxidant signaling in obstructive sleep apnea and associated cardiovascular diseases. Free Radic Biol Med 2006 40 : 1683 1692.
12. Tjong YW, Jian K, Li M et al. Elevated endogenous nitric oxide increases Ca2+ flux via L-type Ca2+ channels by S-nitrosylation in rat hippocampal neurons during severe hypoxia and in vitro ischemia. Free Radic Biol Med 2007 42 : 52 63.
13. Tjong YW, Li M, Gao TM et al. Involvement of nitric oxide in reduced large conductance calcium-activated potassium channel activity in rat hippocampal CA1 pyramidal neurons in intermittent hypoxia. Asian Pacific Society for Neurochemistry J Neurochem 2006 98 (Suppl. 1 66 67.
14. Liu H, Moczydlowski E, Haddad GG. O(2) deprivation inhibits Ca(2+)-activated K(+) channels via cytosolic factors in mice neocortical neurons. J Clin Invest 1999 104 : 577 588.
15. Gao TM, Fung ML. Decreased large conductance Ca(2+)-activated K(+) channel activity in dissociated CA1 hippocampal neurons in rats exposed to perinatal and postnatal hypoxia. Neurosci Lett 2002 332 : 163 166.
16. Ahern GP, Hsu SF, Jackson MB. Direct actions of nitric oxide on rat neurohypophysial K+ channels. J Physiol 1999 520 (Pt 1) : 165 176.
17. Jeong SY, Ha TS, Park CS et al. Nitric oxide directly activates large conductance Ca2+-activated K+ channels (rSlo). Mol Cells 2001 12 : 97 102.
18. Lee JE, Kwak J, Suh CK et al. Dual effects of nitric oxide on the large conductance calcium-activated potassium channels of rat brain. J Biochem Mol Biol 2006 39 : 91 96.
19. Li RC, Row BW, Kheirandish L et al. Nitric oxide synthase and intermittent hypoxia-induced spatial learning deficits in the rat. Neurobiol Dis 2004 17 : 44 53.
20. Zhan G, Fenik P, Pratico D et al. Inducible nitric oxide synthase in long-term intermittent hypoxia: hypersomnolence and brain injury. Am J Respir Crit Care Med 2005 171 : 1414 1420.
21. Reiter RJ. Melatonin: lowering the high price of free radicals. News Physiol Sci 2000 15 : 246 250.
22. Okatani Y, Wakatsuki A, Kaneda C. Melatonin increases activities of glutathione peroxidase and superoxide dismutase in fetal rat brain. J Pineal Res 2000 28 : 89 96.
23. Pei Z, Pang SF, Cheung RT. Pretreatment with melatonin reduces volume of cerebral infarction in a rat middle cerebral artery occlusion stroke model. J Pineal Res 2002 32 : 168 172.
24. Reiter RJ, Sainz RM, Lopez-Burillo S et al. Melatonin ameliorates neurologic damage and neurophysiologic deficits in experimental models of stroke. Ann N Y Acad Sci 2003 993 : 35 47.
25. Uchida K, Samejima M, Okabe A et al. Neuroprotective effects of melatonin against anoxia/aglycemia stress, as assessed by synaptic potentials and superoxide production in rat hippocampal slices. J Pineal Res 2004 37 : 215 222.
26. Lee EJ, Lee MY, Chen HY et al. Melatonin attenuates gray and white matter damage in a mouse model of transient focal cerebral ischemia. J Pineal Res 2005 38 : 42 52.
27. Tutunculer F, Eskiocak S, Basaran UN et al. The protective role of melatonin in experimental hypoxic brain damage. Pediatr Int 2005 47 : 434 439.
28. Chen HY, Chen TY, Lee MY et al. Melatonin decreases neurovascular oxidative/nitrosative damage and protects against early increases in the blood-brain barrier permeability after transient focal cerebral ischemia in mice. J Pineal Res 2006 41 : 175 182.
29. Lee MY, Kuan YH, Chen HY et al. Intravenous administration of melatonin reduces the intracerebral cellular inflammatory response following transient focal cerebral ischemia in rats. J Pineal Res 2007 42 : 297 309.
30. Hung HW, Tipoe GL, Poon AMS et al. Protective effect of melatonin against hippocampal injury of rats with intermittent hypoxia. J Pineal Res 2007 doi:.
31. Li XM, Li JG, Yang JM et al. An improved method for acute isolation of neurons from the hippocampus of adult rats suitable for patch-clamping study. Sheng Li Xue Bao 2004 56 : 112 117.
32. Fung ML, Ye JS, Fung PC. Acute hypoxia elevates nitric oxide generation in rat carotid body in vitro. Pflugers Arch 2001 442 : 903 909.
33. Ye JS, Tipoe GL, Fung PC et al. 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 2002 444 : 178 185.
34. Ling S, Sheng JZ, Braun JE et al. Syntaxin 1A co-associates with native rat brain and cloned large conductance, calcium-activated potassium channels in situ. J Physiol 2003 553 : 65 81.
35. Liu P, Smith PF, Appleton I et al. Regional variations and age-related changes in nitric oxide synthase and arginase in the sub-regions of the hippocampus. Neuroscience 2003 119 : 679 687.
36. Kadekaro M, Su G, Chu R et al. Effects of nitric oxide on expressions of nitrosocysteine and calcium-activated potassium channels in the supraoptic nuclei and neural lobe of dehydrated rats. Neurosci Lett 2007 411 : 117 122.
37. Tan DX, Chen LD, Poeggeler B et al. Melatonin: a potent endogenous hydroxyl radical scavenger. Endocr J 1993 1 : 57 60.
38. Tan DX, Manchester LC, Terron MP et al. One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species? J Pineal Res 2007 42 : 28 42.
39. Jordan W, Cohrs S, Degner D et al. Evaluation of oxidative stress measurements in obstructive sleep apnea syndrome. J Neural Transm 2006 113 : 239 254.
40. Warner DS, Sheng H, Batinic-Haberle I. Oxidants, antioxidants and the ischemic brain. J Exp Biol 2004 207 : 3221 3231.
41. Lewen A, Matz P, Chan PH. Free radical pathways in CNS injury. J Neurotrauma 2000 17 : 871 890.
42. Sopova IY, Zamorskii II. Effect of melatonin on the relationship between lipid peroxidation and proteolytic activity in basal nuclei of rat brain during acute hypoxia. Bull Exp Biol Med 2006 142 : 83 85.
43. Tan DX, Manchester LC, Reiter RJ et al. Melatonin suppresses autoxidation and hydrogen peroxide-induced lipid peroxidation in monkey brain homogenate. Neuroendocrinol Lett 2000 21 : 361 365.
44. Reiter RJ, Acuna-Castroviejo D, Tan DX et al. Free radical-mediated molecular damage. Mechanisms for the protective actions of melatonin in the central nervous system. Ann N Y Acad Sci 2001 939 : 200 215.
45. Lu T, He T, Katusic ZS et al. Molecular mechanisms mediating inhibition of human large conductance Ca2+-activated K+ channels by high glucose. Circ Res 2006 99 : 607 616.
46. Hepp S, Gerich FJ, Muller M. Sulfhydryl oxidation reduces hippocampal susceptibility to hypoxia-induced spreading depression by activating BK channels. J Neurophysiol 2005 94 : 1091 1103.
47. Gong L, Gao TM, Huang H et al. Redox modulation of large conductance calcium-activated potassium channels in CA1 pyramidal neurons from adult rat hippocampus. Neurosci Lett 2000 286 : 191 194.
48. Zhang G, Xu R, Heinemann SH et al. Cysteine oxidation and rundown of large-conductance Ca2+-dependent K+ channels. Biochem Biophys Res Commun 2006 342 : 1389 1395.
49. Tang XD, Garcia ML, Heinemann SH et al. Reactive oxygen species impair Slo1 BK channel function by altering cysteine-mediated calcium sensing. Nat Struct Mol Biol 2004 11 : 171 178.
50. McCartney CE, McClafferty H, Huibant JM et al. 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 2005 102 : 17870 17876.
51. Santarelli LC, Wassef R, Heinemann SH et al. Three methionine residues located within the regulator of conductance for K+ (RCK) domains confer oxidative sensitivity to large-conductance Ca2+-activated K+ channels. J Physiol 2006 571 : 329 348.
52. Musshoff U, Riewenherm D, Berger E et al. Melatonin receptors in rat hippocampus: molecular and functional investigations. Hippocampus 2002 12 : 165 173.
53. Hogan MV, El-Sherif Y, Wieraszko A. The modulation of neuronal activity by melatonin: in vitro studies on mouse hippocampal slices. J Pineal Res 2001 30 : 87 96.
54. Larson J, Jessen RE, Uz T et al. Impaired hippocampal long-term potentiation in melatonin MT2 receptor-deficient mice. Neurosci Lett 2006 393 : 23 26.
55. Wang LM, Suthana NA, Chaudhury D et al. Melatonin inhibits hippocampal long-term potentiation. Eur J Neurosci 2005 22 : 2231 2237.
56. Chang HM, Ling EA, Chen CF et al. Melatonin attenuates the neuronal NADPH-d/NOS expression in the nodose ganglion of acute hypoxic rats. J Pineal Res 2002 32 : 65 73.
57. Ananth C, Gopalakrishnakone P, Kaur C. Protective role of melatonin in domoic acid-induced neuronal damage in the hippocampus of adult rats. Hippocampus 2003 13 : 375 387.
58. Aydogan S, Yerer MB, Goktas A. Melatonin and nitric oxide. J Endocrinol Invest 2006 29 : 281 287.
59. Pei Z, Fung PC, Cheung RT. Melatonin reduces nitric oxide level during ischemia but not blood-brain barrier breakdown during reperfusion in a rat middle cerebral artery occlusion stroke model. J Pineal Res 2003 34 : 110 118.
60. Michel T, Feron O. Nitric oxide synthases: which, where, how, and why? J Clin Invest 1997 100 : 2146 2152.
61. Kaster MP, Ferreira PK, Santos AR et al. Effects of potassium channel inhibitors in the forced swimming test: possible involvement of L-arginine-nitric oxide-soluble guanylate cyclase pathway. Behav Brain Res 2005 165 : 204 209.
62. Lang RJ, Harvey JR, Mulholland EL. Sodium (2-sulfonatoethyl) methanethiosulfonate prevents S-nitroso-L-cysteine activation of Ca2+-activated K+ (BKCa) channels in myocytes of the guinea-pig taenia caeca. Br J Pharmacol 2003 139 : 1153 1163.
63. Calderone V. Large-conductance, Ca(2+)-activated K(+) channels: function, pharmacology and drugs. Curr Med Chem 2002 9 : 1385 1395.
64. Gong L, Gao TM, Li X et al. Enhancement in activities of large conductance calcium-activated potassium channels in CA1 pyramidal neurons of rat hippocampus after transient forebrain ischemia. Brain Res 2000 884 : 147 154.
65. Runden-Pran E, Haug FM, Storm JF et al. BK channel activity determines the extent of cell degeneration after oxygen and glucose deprivation: a study in organotypical hippocampal slice cultures. Neuroscience 2002 112 : 277 288.