Melatonin ameliorates endothelial dysfunction, vascular inflammation, and systemic hypertension in rats with chronic intermittent hypoxia

Journal of Pineal Research

Volumn 55, Issue 3, 2013, Pages 247-256

  Hung, Ming Wai ^a   Kravtsov, Gennadi M ^a   Lau, Chi Fai ^a   Poon, Angela Ming See ^a   Tipoe, George L ^a,b   Fung, Man Lung ^a,b  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

adhesion molecules; antioxidant enzymes; hypertension; inflammation; intermittent hypoxia; melatonin; sleep apnea

Indexed keywords

ANTIOXIDANT; CELL ADHESION MOLECULE; COPPER ZINC SUPEROXIDE DISMUTASE; CYCLOOXYGENASE 2; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; GLUTATHIONE PEROXIDASE; INTERCELLULAR ADHESION MOLECULE 1; MALONALDEHYDE; MELATONIN; NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC INTERMITTENT HYPOXIA; CONTROLLED STUDY; DRUG SUBSTITUTION; ENDOTHELIAL DYSFUNCTION; HYPERTENSION; INTERMITTENT HYPOXIA; NONHUMAN; OXIDATIVE STRESS; RAT; SLEEP DISORDERED BREATHING; SPRAGUE DAWLEY RAT; SYSTOLIC BLOOD PRESSURE; THORACIC AORTA; VASCULITIS;

ADHESION MOLECULES; ANTIOXIDANT ENZYMES; HYPERTENSION; INFLAMMATION; INTERMITTENT HYPOXIA; MELATONIN; SLEEP APNEA;

ANIMALS; ANOXIA; ANTIOXIDANTS; AORTA, THORACIC; CELL ADHESION MOLECULES; CHRONIC DISEASE; ENDOTHELIUM, VASCULAR; HYPERTENSION; INFLAMMATION MEDIATORS; MALONDIALDEHYDE; MELATONIN; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; OXIDOREDUCTASES; RATS, SPRAGUE-DAWLEY; TUMOR NECROSIS FACTOR-ALPHA; VASCULITIS;

EID: 84883744044     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/jpi.12067     Document Type: Article

References (62)

1. Nieto FJ, Young TB, Lind BK, et al. Association of sleep-disordered breathing, sleep apnea, and hypertension in a large community-based study. Sleep Heart Health Study. JAMA 2000; 283: 1829-1836.
2. Shahar E, Whitney CW, Redline S, et al. Sleep-disordered breathing and cardiovascular disease: cross-sectional results of the Sleep Heart Health Study. Am J Respir Crit Care Med 2001; 163: 19-25.
3. Patil SP, Schneider H, Schwartz AR, et al. Adult obstructive sleep apnea: pathophysiology and diagnosis. Chest 2007; 132: 325-337.
4. 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.
5. Hernandez C, Abreu J, Abreu P, et al. Effects of nasal positive airway pressure treatment on oxidative stress in patients with sleep apnea-hypopnea syndrome. Arch Bronconeumol 2006; 42: 125-129.
6. Ciftci TU, Kokturk O, Bukan N, et al. The relationship between serum cytokine levels with obesity and obstructive sleep apnea syndrome. Cytokine 2004; 28: 87-91.
7. Ohga E, Tomita T, Wada H, et al. Effects of obstructive sleep apnea on circulating ICAM-1, IL-8, and MCP-1. J Appl Physiol 2003; 94: 179-184.
8. Lavie L, Hefetz A, Luboshitzky R, et al. Plasma levels of nitric oxide and L-arginine in sleep apnea patients: effects of nCPAP treatment. J Mol Neurosci 2003; 21: 57-63.
9. Carlson JT, Rangemark C, Hedner JA,. Attenuated endothelium-dependent vascular relaxation in patients with sleep apnoea. J Hypertens 1996; 14: 577-584.
10. Kato M, Roberts-Thomson P, Phillips BG, et al. Impairment of endothelium-dependent vasodilation of resistance vessels in patients with obstructive sleep apnea. Circulation 2000; 102: 2607-2610.
11. Phillips SA, Olson EB, Morgan BJ, et al. 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.
12. Kumar GK, Rai V, Sharma SD, et al. Chronic intermittent hypoxia induces hypoxia-evoked catecholamine efflux in adult rat adrenal medulla via oxidative stress. J Physiol 2006; 575: 229-239.
13. Troncoso Brindeiro CM, Da Silva AQ, Allahdadi KJ, et al. Reactive oxygen species contribute to sleep apnea-induced hypertension in rats. Am J Physiol Heart Circ Physiol 2007; 293: H2971-H2976.
14. Reiter RJ, Tan DX, Maldonado MD,. Melatonin as an antioxidant: physiology versus pharmacology. J Pineal Res 2005; 39: 215-216.
15. Galano A, Tan DX, Reiter RJ,. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 2011; 51: 1-16.
16. 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.
17. Mayo JC, Sainz RM, Tan DX, et al. Anti-inflammatory actions of melatonin and its metabolites, N1-acetyl-N2-formyl-5-methoxykynuramine (AFMK) and N1-acetyl-5-methoxykynuramine (AMK), in macrophages. J Neuroimmunol 2005; 165: 139-149.
18. Rodriguez C, Mayo JC, Sainz RM, et al. Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 2004; 36: 1-9.
19. Mauriz JL, Collado PS, Veneroso C, et al. A review of the molecular aspects of melatonin's anti-inflammatory actions: recent insights and new perspectives. J Pineal Res 2013; 54: 1-14.
20. Xia MZ, Liang YL, Wang H, et al. Melatonin modulates TLR4-mediated inflammatory genes through MyD88- and TRIF-dependent signaling pathways in lipopolysaccharide-stimulated RAW264.7 cells. J Pineal Res 2012; 53: 325-334.
21. Simko F, Paulis L,. Melatonin as a potential antihypertensive treatment. J Pineal Res 2007; 42: 319-322.
22. Reiter RJ, Tan DX, Korkmaz A,. The circadian melatonin rhythm and its modulation: possible impact on hypertension. J Hypertens Suppl 2009; 27: S17-S20.
23. Hernandez C, Abreu J, Abreu P, et al. Nocturnal melatonin plasma levels in patients with OSAS: the effect of CPAP. Eur Respir J 2007; 30: 496-500.
24. Fletcher EC, Lesske J, Qian W, et al. Repetitive, episodic hypoxia causes diurnal elevation of blood pressure in rats. Hypertension 1992; 19: 555-561.
25. 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.
26. Cheung RT, Tipoe GL, Tam S, et al. Preclinical evaluation of pharmacokinetics and safety of melatonin in propylene glycol for intravenous administration. J Pineal Res 2006; 41: 337-343.
27. Kaur C, Sivakumar V, Lu J, et al. Increased vascular permeability and nitric oxide production in response to hypoxia in the pineal gland. J Pineal Res 2007; 42: 338-349.
28. Prabhakar NR, Kumar GK, Nanduri J, et al. ROS signaling in systemic and cellular responses to chronic intermittent hypoxia. Antioxid Redox Signal 2007; 9: 1397-1403.
29. Schulz R, Mahmoudi S, Hattar K, et al. Enhanced release of superoxide from polymorphonuclear neutrophils in obstructive sleep apnea. Impact of continuous positive airway pressure therapy. Am J Respir Crit Care Med 2000; 162: 566-570.
30. Lavie L,. Obstructive sleep apnoea syndrome-an oxidative stress disorder. Sleep Med Rev 2003; 7: 35-51.
31. Peng YJ, Overholt JL, Kline D, et al. Induction of sensory long-term facilitation in the carotid body by intermittent hypoxia: implications for recurrent apneas. Proc Natl Acad Sci USA 2003; 100: 10073-10078.
32. Zhan G, Serrano F, Fenik P, et al. NADPH oxidase mediates hypersomnolence and brain oxidative injury in a murine model of sleep apnea. Am J Respir Crit Care Med 2005; 172: 921-929.
33. Bonnefont-Rousselot D, Collin F, Jore D, et al. Reaction mechanism of melatonin oxidation by reactive oxygen species in vitro. J Pineal Res 2011; 50: 328-335.
34. Lavie L,. Sleep-disordered breathing and cerebrovascular disease: a mechanistic approach. Neurol Clin 2005; 23: 1059-1075.
35. Vgontzas AN, Papanicolaou DA, Bixler EO, et al. Elevation of plasma cytokines in disorders of excessive daytime sleepiness: role of sleep disturbance and obesity. J Clin Endocrinol Metab 1997; 82: 1313-1316.
36. Alzoghaibi MA, Bahammam AS,. Lipid peroxides, superoxide dismutase and circulating IL-8 and GCP-2 in patients with severe obstructive sleep apnea: a pilot study. Sleep Breath 2005; 9: 119-126.
37. Chaves FJ, Mansego ML, Blesa S, et al. Inadequate cytoplasmic antioxidant enzymes response contributes to the oxidative stress in human hypertension. Am J Hypertens 2007; 20: 62-69.
38. Laliena A, San Miguel B, Crespo I, et al. Melatonin attenuates inflammation and promotes regeneration in rabbits with fulminant hepatitis of viral origin. J Pineal Res 2012; 53: 270-278.
39. Ryan S, Taylor CT, McNicholas WT,. Selective activation of inflammatory pathways by intermittent hypoxia in obstructive sleep apnea syndrome. Circulation 2005; 112: 2660-2667.
40. Williams A, Scharf SM,. Obstructive sleep apnea, cardiovascular disease, and inflammation-is NF-kappaB the key? Sleep Breath 2007; 11: 69-76.
41. Greenberg H, Ye X, Wilson D, et al. Chronic intermittent hypoxia activates nuclear factor-kappaB in cardiovascular tissues in vivo. Biochem Biophys Res Commun 2006; 343: 591-596.
42. Alonso M, Collado PS, Gonzalez-Gallego J,. Melatonin inhibits the expression of the inducible isoform of nitric oxide synthase and nuclear factor kappa B activation in rat skeletal muscle. J Pineal Res 2006; 41: 8-14.
43. Mohan N, Sadeghi K, Reiter RJ, et al. The neurohormone melatonin inhibits cytokine, mitogen and ionizing radiation induced NF-kappa B. Biochem Mol Biol Int 1995; 37: 1063-1070.
44. Chuang JI, Mohan N, Meltz ML, et al. Effect of melatonin on NF-kappa-B DNA-binding activity in the rat spleen. Cell Biol Int 1996; 20: 687-692.
45. Pechanova O, Zicha J, Paulis L, et al. The effect of N-acetylcysteine and melatonin in adult spontaneously hypertensive rats with established hypertension. Eur J Pharmacol 2007; 561: 129-136.
46. Kojsova S, Jendekova L, Zicha J, et al. The effect of different antioxidants on nitric oxide production in hypertensive rats. Physiol Res 2006; 55 (Suppl 1): S3-S16.
47. Beni SM, Kohen R, Reiter RJ, et al. Melatonin-induced neuroprotection after closed head injury is associated with increased brain antioxidants and attenuated late-phase activation of NF-kappaB and AP-1. FASEB J 2004; 18: 149-151.
48. Carlberg C,. Gene regulation by melatonin. Ann N Y Acad Sci 2000; 917: 387-396.
49. Ram PT, Dai J, Yuan L, et al. Involvement of the mt1 melatonin receptor in human breast cancer. Cancer Lett 2002; 179: 141-150.
50. Masana MI, Doolen S, Ersahin C, et al. MT(2) melatonin receptors are present and functional in rat caudal artery. J Pharmacol Exp Ther 2002; 302: 1295-1302.
51. Doolen S, Krause DN, Dubocovich ML, et al. Melatonin mediates two distinct responses in vascular smooth muscle. Eur J Pharmacol 1998; 345: 67-69.
52. Deniz E, Sahna E, Aksulu HE,. Nitric oxide synthase inhibition in rats: melatonin reduces blood pressure and ischemia/reperfusion-induced infarct size. Scand Cardiovasc J 2006; 40: 248-252.
53. Pogan L, Bissonnette P, Parent L, et al. The effects of melatonin on Ca(2 +) homeostasis in endothelial cells. J Pineal Res 2002; 33: 37-47.
54. Maxwell AJ,. Mechanisms of dysfunction of the nitric oxide pathway in vascular diseases. Nitric Oxide 2002; 6: 101-124.
55. Mutoh T, Shibata S, Korf HW, et al. Melatonin modulates the light-induced sympathoexcitation and vagal suppression with participation of the suprachiasmatic nucleus in mice. J Physiol 2003; 547: 317-332.
56. Leuenberger UA, Brubaker D, Quraishi S, et al. Effects of intermittent hypoxia on sympathetic activity and blood pressure in humans. Auton Neurosci 2005; 121: 87-93.
57. Holmes SW, Sugden D,. Proceedings: the effect of melatonin on pinealectomy-induced hypertension in the rat. Br J Pharmacol 1976; 56: 360P-361P.
58. Zanoboni A, Forni A, Zanoboni-Muciaccia W, et al. Effect of pinealectomy on arterial blood pressure and food and water intake in the rat. J Endocrinol Invest 1978; 1: 125-130.
59. Cunnane SC, Manku MS, Oka M, et al. Enhanced vascular reactivity to various vasoconstrictor agents following pinealectomy in the rat: role of melatonin. Can J Physiol Pharmacol 1980; 58: 287-293.
60. Scheer FA, van Montfrans GA, van Someren EJ, et al. Daily nighttime melatonin reduces blood pressure in male patients with essential hypertension. Hypertension 2004; 43: 192-197.
61. Grossman E, Laudon M, Yalcin R, et al. Melatonin reduces night blood pressure in patients with nocturnal hypertension. Am J Med 2006; 119: 898-902.
62. Forman JP, Curhan GC, Schernhammer ES,. Urinary melatonin and risk of incident hypertension among young women. J Hypertens 2010; 28: 446-451.