Maternal melatonin administration mitigates coronary stiffness and endothelial dysfunction, and improves heart resilience to insult in growth restricted lambs

Journal of Physiology

Volumn 592, Issue 12, 2014, Pages 2695-2709

  Tare, Marianne ^a   Parkington, Helena C ^a   Wallace, Euan M ^a,b   Sutherland, Amy E ^b   Lim, Rebecca ^a,b   Yawno, Tamara ^b   Coleman, Harold A ^a   Jenkin, Graham ^a,b   Miller, Suzanne L ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MELATONIN; NITRIC OXIDE; CARDIOTONIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTINUOUS INFUSION; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; CORONARY ARTERY DISEASE; DISEASE ASSOCIATION; DRUG MECHANISM; ENDOTHELIAL DYSFUNCTION; FEMALE; FETUS; GROWTH RETARDATION; HEART LEFT VENTRICLE CONTRACTION; HEART PROTECTION; IN VIVO STUDY; LAMB; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; OXYGEN CONSUMPTION; OXYGENATION; PLACENTA DISORDER; PRIORITY JOURNAL; REPERFUSION INJURY; TREATMENT OUTCOME; TWIN PREGNANCY; ANIMAL; ARTERIAL STIFFNESS; DRUG EFFECTS; FETAL GROWTH RETARDATION; FETOMATERNAL TRANSFUSION; FETUS HEART; HEART CONTRACTION; MYOCARDIAL REPERFUSION INJURY; PATHOPHYSIOLOGY; PREGNANCY; SHEEP; VASCULAR ENDOTHELIUM;

ANIMALS; CARDIOTONIC AGENTS; CORONARY CIRCULATION; ENDOTHELIUM, VASCULAR; FEMALE; FETAL GROWTH RETARDATION; FETAL HEART; MATERNAL-FETAL EXCHANGE; MELATONIN; MYOCARDIAL CONTRACTION; MYOCARDIAL REPERFUSION INJURY; PREGNANCY; SHEEP; VASCULAR STIFFNESS;

EID: 84902328874     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.270934     Document Type: Article

References (56)

1. Acuna-Castroviejo D, Escames G, Rodriguez MI & Lopez LC (2007). Melatonin role in the mitochondrial function. Front Biosci 12, 947-963.
2. Alers NO, Jenkin G, Miller SL & Wallace EM (2013). Antenatal melatonin as an antioxidant in human pregnancies complicated by fetal growth restriction-a phase I pilot clinical trial: study protocol. BMJ Open 3, e004141.
3. Bahtiyar MO & Copel JA (2008). Cardiac changes in the intrauterine growth-restricted fetus. Semin Perinatol 32, 190-193.
4. Bubb KJ, Cock ML, Black MJ, Dodic M, Boon W-M, Parkington HC, Harding R & Tare M (2007). Intrauterine growth restriction delays cardiomyocyte maturation and alters coronary artery function in the fetal sheep. J Physiol 578, 871-881.
5. Burrell JH, Boyn AM, Kumarasamy V, Hsieh A, Head SI & Lumbers ER (2003). Growth and maturation of cardiac myocytes in fetal sheep in the second half of gestation. Anat Rec A Discov Mol Cell Evol Biol 274, 952-961.
6. Cardinali DP & Ritta MN (1983). The role of prostaglandins in neuroendocrine junctions: studies in the pineal gland and the hypothalamus. Neuroendocrinology 36, 152-160.
7. Chan PY, Morris JM, Leslie GI, Kelly PJ & Gallery ED (2010). The long-term effects of prematurity and intrauterine growth restriction on cardiovascular, renal, and metabolic function. Int J Pediatr 2010, 280402.
8. Crispi F, Bijnens B, Figueras F, Bartrons J, Eixarch E, Le Noble F, Ahmed A & Gratacos E (2010). Fetal growth restriction results in remodeled and less efficient hearts in children. Circulation 121, 2427-2436.
9. 2 melatonin receptors in mammals. Endocrine 27, 101-110.
10. 2 is present in the human cardiovascular system. J Pineal Res 35, 40-44.
11. Giles TD, Sander GE, Nossaman BD & Kadowitz PJ (2012). Impaired vasodilation in the pathogenesis of hypertension: focus on nitric oxide, endothelial-derived hyperpolarizing factors, and prostaglandins. J Clin Hypertens 14, 198-205.
12. Grossini E, Molinari C, Uberti F, Mary DA, Vacca G & Caimmi PP (2011). Intracoronary melatonin increases coronary blood flow and cardiac function through β-adrenoreceptors, MT1/MT2 receptors, and nitric oxide in anaesthetized pigs. J Pineal Res 51, 246-257.
13. Hallows SE, Regnault TR & Betts DH (2012). The long and short of it: the role of telomeres in fetal origins of adult disease. J Pregnancy 2012, 638476.
14. 1-acetyl-5-methoxykynuramine. J Pineal Res 43, 382-388.
15. Hardeland R, Cardinali DP, Srinivasan V, Spence DW, Brown GM & Pandi-Perumal SR (2011). Melatonin-a pleiotropic, orchestrating regulator molecule. Prog Neurobiol 93, 350-384.
16. Hardeland R, Poeggeler B, Niebergall R & Zelosko V (2003). Oxidation of melatonin by carbonate radicals and chemiluminescence emitted during pyrrole ring cleavage. J Pineal Res 34, 17-25.
17. Herrera EA, Verkerk MM, Derks JB & Giussani DA (2010). Antioxidant treatment alters peripheral vascular dysfunction induced by postnatal glucocorticoid therapy in rats. PLoS One 5, e9250.
18. Hink U, Li H, Mollnau H, Oelze M, Matheis E, Hartmann M, Skatchkov M, Thaiss F, Stahl RA, Warnholtz A, Meinertz T, Griendling K, Harrison DG, Forstermann U & Munzel T (2001). Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circ Res 88, E14-22.
19. Izzard AS, Horton S, Heerkens EH, Shaw L & Heagerty AM (2006). Middle cerebral artery structure and distensibility during developing and established phases of hypertension in the spontaneously hypertensive rat. J Hypertens 24, 875-880.
20. Kim SF (2011). The role of nitric oxide in prostaglandin biology; update. Nitric Oxide 25, 255-264.
21. Laurent S, Boutouyrie P, Asmar R, Gautier I, Laloux B, Guize L, Ducimetiere P & Benetos A (2001). Aortic stiffness is an independent predictor of all-cause and cardiovascular mortality in hypertensive patients. Hypertension 37, 1236-1241.
22. Lemley CO, Meyer AM, Camacho LE, Neville TL, Newman DJ, Caton JS & Vonnahme KA (2012). Melatonin supplementation alters uteroplacental hemodynamics and fetal development in an ovine model of intrauterine growth restriction. Am J Physiol Regul Integr Comp Physiol 302, R454-R467.
23. Li G, Xiao Y, Estrella JL, Ducsay CA, Gilbert RD & Zhang L (2003). Effect of fetal hypoxia on heart susceptibility to ischemia and reperfusion injury in the adult rat. J Soc Gynecol Invest 10, 265-274.
24. Lian IA, Loset M, Mundal SB, Fenstad MH, Johnson MP, Eide IP, Bjorge L, Freed KA, Moses EK & Austgulen R (2011). Increased endoplasmic reticulum stress in decidual tissue from pregnancies complicated by fetal growth restriction with and without pre-eclampsia. Placenta 32, 823-829.
25. Longo S, Bollani L, Decembrino L, Comite AD, Angelini M & Stronati M (2012). Short-term and long-term sequelae in intrauterine growth retardation (IUGR). J Matern Fetal Neonatal Med 26, 222-225.
26. López LC, Escames G, Tapias V, Utrilla P, León J & Acuña-Castroviejo D (2006). Identification of an inducible nitric oxide synthase in diaphragm mitochondria from septic mice: its relation with mitochondrial dysfunction and prevention by melatonin. Int J Biochem Cell Biol 38, 267-278.
27. Mayhew TM, Pharaoh A, Austin A & Fagan DG (1997). Stereological estimates of nuclear number in human ventricular cardiomyocytes before and after birth obtained using physical disectors. J Anat 191, 107-115.
28. Mazzuca MQ, Wlodek ME, Dragomir NM, Parkington HC & Tare M (2010). Uteroplacental insufficiency programs regional vascular dysfunction and alters arterial stiffness in female offspring. J Physiol 588, 1997-2010.
29. Mert I, Oruc AS, Yuksel S, Cakar ES, Buyukkagnici U, Karaer A & Danisman N (2012). Role of oxidative stress in preeclampsia and intrauterine growth restriction. J Obstet Gynaecol Res 38, 658-664.
30. Miller SL, Chai M, Loose J, Castillo-Melendez M, Walker DW, Jenkin G & Wallace EM (2007). The effects of maternal betamethasone administration on the intrauterine growth-restricted fetus. Endocrinology 148, 1288-1295.
31. Miller SL, Supramaniam VG, Jenkin G, Walker DW & Wallace EM (2009). Cardiovascular responses to maternal betamethasone administration in the intrauterine growth-restricted ovine fetus. Am J Obstet Gynecol 201, 613 e611-618.
32. Miller SL, Yawno T, Alers NO, Castillo-Melendez M, Supramaniam VG, Vanzyl N, Sabaretnam T, Loose JM, Drummond GR, Walker DW, Jenkin G & Wallace EM (2014). Antenatal antioxidant treatment with melatonin to decrease newborn neurodevelopmental deficits and brain injury caused by fetal growth restriction. J Pineal Res 56, 283-294.
33. Norman M (2008). Low birth weight and the developing vascular tree: a systematic review. Acta Paediatrica 97, 1165-1172.
34. Paulis L, Pechanova O, Zicha J, Barta A, Gardlik R, Celec P, Kunes J & Simko F (2010). Melatonin interactions with blood pressure and vascular function during l-NAME-induced hypertension. J Pineal Res 48, 102-108.
35. Paulis L, Simko F & Laudon M (2012). Cardiovascular effects of melatonin receptor agonists. Expert Opin Investig Drugs 21, 1661-1678.
36. Petrosillo G, Di Venosa N, Pistolese M, Casanova G, Tiravanti E, Colantuono G, Federici A, Paradies G & Ruggiero FM (2006). Protective effect of melatonin against mitochondrial dysfunction associated with cardiac ischemia-reperfusion: role of cardiolipin. FASEB J 20, 269-276.
37. Pisaneschi S, Strigini FA, Sanchez AM, Begliuomini S, Casarosa E, Ripoli A, Ghirri P, Boldrini A, Fink B, Genazzani AR, Coceani F & Simoncini T (2012). Compensatory feto-placental upregulation of the nitric oxide system during fetal growth restriction. PLoS One 7, e45294.
38. Poeggeler B, Reiter RJ, Tan DX, Chen LD & Manchester LC (1993). Melatonin, hydroxyl radical-mediated oxidative damage, and aging: a hypothesis. J Pineal Res 14, 151-168.
39. Qin W, Lu W, Li H, Yuan X, Li B, Zhang Q & Xiu R (2012). Melatonin inhibits IL1β-induced MMP9 expression and activity in human umbilical vein endothelial cells by suppressing NF-κB activation. J Endocrinol 214, 145-153.
40. Rezzani R, Porteri E, De Ciuceis C, Bonomini F, Rodella LF, Paiardi S, Boari GE, Platto C, Pilu A, Avanzi D, Rizzoni D & Agabiti Rosei E (2010). Effects of melatonin and Pycnogenol on small artery structure and function in spontaneously hypertensive rats. Hypertension 55, 1373-1380.
41. Rossi P, Tauzin L, Marchand E, Boussuges A, Gaudart J & Frances Y (2011). Respective roles of preterm birth and fetal growth restriction in blood pressure and arterial stiffness in adolescence. J Adolesc Health 48, 520-522.
42. Rueda-Clausen CF, Morton JS, Lopaschuk GD & Davidge ST (2011). Long-term effects of intrauterine growth restriction on cardiac metabolism and susceptibility to ischaemia/reperfusion. Cardiovasc Res 90, 285-294.
43. 2 and elevates the ANP level in the rat left ventricle. J Pineal Res 45, 61-69.
44. Sandow SL & Tare M (2007). C-type natriuretic peptide: a new endothelium-derived hyperpolarizing factor? Trends Pharmacol Sci 28, 61-67.
45. 1-acetyl-5-methoxykynuramine prevent mitochondrial nitric oxide synthase induction in parkinsonian mice. J Neurosci Res 87, 3002-3010.
46. Tare M, Miller SL, Wallace EM, Sutherland AE, Yawno T, Coleman HA, Jenkin G & Parkington HC (2012a). Glucocorticoid treatment does not alter early cardiac adaptations to growth restriction in preterm sheep fetuses. BJOG 119, 906-914.
47. Tare M, Parkington HC, Bubb KJ & Wlodek ME (2012b). Uteroplacental insufficiency and lactational environment separately influence arterial stiffness and vascular function in adult male rats. Hypertension 60, 378-386.
48. Thakor AS, Herrera EA, Seron-Ferre M & Giussani DA (2010). Melatonin and vitamin C increase umbilical blood flow via nitric oxide-dependent mechanisms. J Pineal Res 49, 399-406.
49. Thompson JA, Gros R, Richardson BS, Piorkowska K & Regnault TR (2011a). Central stiffening in adulthood linked to aberrant aortic remodeling under suboptimal intrauterine conditions. Am J Physiol Regul Integr Comp Physiol 301, R1731-R1737.
50. Thompson JA, Richardson BS, Gagnon R & Regnault TR (2011b). Chronic intrauterine hypoxia interferes with aortic development in the late gestation ovine fetus. J Physiol 589, 3319-3332.
51. Torres-Farfan C, Valenzuela FJ, Mondaca M, Valenzuela GJ, Krause B, Herrera EA, Riquelme R, Llanos AJ & Seron-Ferre M (2008). Evidence of a role for melatonin in fetal sheep physiology: direct actions of melatonin on fetal cerebral artery, brown adipose tissue and adrenal gland. J Physiol 586, 4017-4027.
52. Voges I, Jerosch-Herold M, Hedderich J, Pardun E, Hart C, Gabbert DD, Hansen JH, Petko C, Kramer HH & Rickers C (2012). Normal values of aortic dimensions, distensibility, and pulse wave velocity in children and young adults: a cross-sectional study. J Cardiovasc Magn Reson 14, 77.
53. Wigg SJ, Tare M, Forbes J, Cooper ME, Thomas MC, Coleman HA, Parkington HC & O'Brien RC (2004). Early vitamin E supplementation attenuates diabetes-associated vascular dysfunction and the rise in protein kinase C-β in mesenteric artery and ameliorates wall stiffness in femoral artery in rats. Diabetologia 47, 1038-1046.
54. Xu J & Zou MH (2009). Molecular insights and therapeutic targets for diabetic endothelial dysfunction. Circulation 120, 1266-1286.
55. Yeung HM, Hung MW & Fung ML (2008). Melatonin ameliorates calcium homeostasis in myocardial and ischemia-reperfusion injury in chronically hypoxic rats. J Pineal Res 45, 373-382.
56. Zieman SJ, Melenovsky V & Kass DA (2005). Mechanisms, pathophysiology, and therapy of arterial stiffness. Arterioscler Thromb Vasc Biol 25, 932-943.