Prevention of vascular dysfunction and arterial hypertension in mice generated by assisted reproductive technologies by addition of melatonin to culture media

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 309, Issue 7, 2015, Pages H1151-H1156

  Rexhaj, Emrush ^a   Pireva, Agim ^a   Paoloni Giacobino, Ariane ^b   Allemann, Yves ^a   Cerny, David ^a   Dessen, Pierre ^c   Sartori, Claudio ^a,c   Scherrer, Urs ^a,d   Rimoldi, Stefano F ^a  

^a BERN UNIVERSITY HOSPITAL   (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^d UNIVERSIDAD DE TARAPACÁ   (Chile)

Author keywords

Arterial hypertension; Endothelial dysfunction; Epigenetic; In vitro fertilization; Melatonin; Nitric oxide

Indexed keywords

ACETYLCHOLINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MELATONIN; NITRATE; NITRIC OXIDE; NITRITE; ANTIOXIDANT; CULTURE MEDIUM; NOS3 PROTEIN, MOUSE; VASODILATOR AGENT;

ADD ON THERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL PRESSURE; ARTICLE; CONTROLLED STUDY; CULTURE MEDIUM; DNA METHYLATION; EMBRYO; EPIGENETICS; FEMALE; FERTILIZATION; HYPERTENSION; INFERTILITY THERAPY; MEAN ARTERIAL PRESSURE; MESENTERIC ARTERY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; VASCULAR DISEASE; VASCULAR DYSFUNCTION; VASCULAR TISSUE; VASODILATATION; ANIMAL; BLOOD PRESSURE; DRUG EFFECTS; EMBRYO CULTURE; GENETIC EPIGENESIS; GENETICS; METABOLISM;

ACETYLCHOLINE; ANIMALS; ANTIOXIDANTS; BLOOD PRESSURE; CULTURE MEDIA; DNA METHYLATION; EMBRYO CULTURE TECHNIQUES; EPIGENESIS, GENETIC; HYPERTENSION; MELATONIN; MESENTERIC ARTERIES; MICE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PROMOTER REGIONS, GENETIC; REPRODUCTIVE TECHNIQUES, ASSISTED; VASODILATOR AGENTS;

EID: 84943173616     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00621.2014     Document Type: Article

References (36)

1. Barker DJ. In utero programming of cardiovascular disease. Theriogenology 53: 555-574, 2000.
2. Barker DJ. Maternal and fetal origins of coronary heart disease. J R Coll Physicians Lond 28: 544-551, 1994.
3. Chan Y, Fish JE, D=Abreo C, Lin S, Robb GB, Teichert AM, Karantzoulis-Fegaras F, Keightley A, Steer BM, Marsden PA. The cellspecific expression of endothelial nitric-oxide synthase: a role for DNA methylation. J Biol Chem 279: 35087-35100, 2004.
4. Chataigneau T, Feletou M, Huang PL, Fishman MC, Duhault J, Vanhoutte PM. Acetylcholine-induced relaxation in blood vessels from endothelial nitric oxide synthase knockout mice. Br J Pharmacol 126: 219-226, 1999.
5. Cook S, Hugli O, Egli M, Menard B, Thalmann S, Sartori C, Perrin C, Nicod P, Thorens B, Vollenweider P, Scherrer U, Burcelin R. Partial gene deletion of endothelial nitric oxide synthase predisposes to exaggerated high-fat diet-induced insulin resistance and arterial hypertension. Diabetes 53: 2067-2072, 2004.
6. Doherty AS, Mann MR, Tremblay KD, Bartolomei MS, Schultz RM. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol Reprod 62: 1526-1535, 2000.
7. Duplain H, Burcelin R, Sartori C, Cook S, Egli M, Lepori M, Vollenweider P, Pedrazzini T, Nicod P, Thorens B, Scherrer U. Insulin resistance, hyperlipidemia, and hypertension in mice lacking endothelial nitric oxide synthase. Circulation 104: 342-345, 2001.
8. Fish JE, Matouk CC, Rachlis A, Lin S, Tai SC, D'Abreo C, Marsden PA. The expression of endothelial nitric-oxide synthase is controlled by a cell-specific histone code. J Biol Chem 280: 24824-24838, 2005.
9. Ishizuka B, Kuribayashi Y, Murai K, Amemiya A, Itoh MT. The effect of melatonin on in vitro fertilization and embryo development in mice. J Pineal Res 28: 48-51, 2000.
10. Jayet PY, Rimoldi SF, Stuber T, Salmon CS, Hutter D, Rexhaj E, Thalmann S, Schwab M, Turini P, Sartori-Cucchia C, Nicod P, Villena M, Allemann Y, Scherrer U, Sartori C. Pulmonary and systemic vascular dysfunction in young offspring of mothers with preeclampsia. Circulation 122: 488-494, 2010.
11. Kang JT, Koo OJ, Kwon DK, Park HJ, Jang G, Kang SK, Lee BC. Effects of melatonin on in vitro maturation of porcine oocyte and expression of melatonin receptor RNA in cumulus and granulosa cells. J Pineal Res 46: 22-28, 2009.
12. Khosla S, Dean W, Brown D, Reik W, Feil R. Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes. Biol Reprod 64: 918-926, 2001.
13. Korkmaz A. Epigenetic actions of melatonin. J Pineal Res 46: 117-118, 2009.
14. Maganhin CC, Fuchs LF, Simoes RS, Oliveira-Filho RM, de Jesus Simoes M, Baracat EC, Soares JM Jr. Effects of melatonin on ovarian follicles. Eur J Obstet Gynecol Reprod Biol 166: 178-184, 2013.
15. Market-Velker BA, Fernandes AD, Mann MR. Side-by-side comparison of five commercial media systems in a mouse model: suboptimal in vitro culture interferes with imprint maintenance. Biol Reprod 83: 938-950, 2010.
16. Mulvany MJ, Halpern W. Contractile properties of small arterial resistance vessels in spontaneously hypertensive and normotensive rats. Circ Res 41: 19-26, 1977.
17. Niles LP, Pan Y, Kang S, Lacoul A. Melatonin induces histone hyperacetylation in the rat brain. Neurosci Lett 541: 49-53, 2013.
18. Peyter AC, Muehlethaler V, Liaudet L, Marino M, Di Bernardo S, Diaceri G, Tolsa JF. Muscarinic receptor M1 and phosphodiesterase 1 are key determinants in pulmonary vascular dysfunction following perinatal hypoxia in mice. Am J Physiol Lung Cell Mol Physiol 295: L201-L213, 2008.
19. Rexhaj E, Bloch J, Jayet PY, Rimoldi SF, Dessen P, Mathieu C, Tolsa JF, Nicod P, Scherrer U, Sartori C. Fetal programming of pulmonary vascular dysfunction in mice: role of epigenetic mechanisms. Am J Physiol Heart Circ Physiol 301: H247-H252, 2011.
20. Rexhaj E, Paoloni-Giacobino A, Rimoldi SF, Fuster DG, Anderegg M, Somm E, Bouillet E, Allemann Y, Sartori C, Scherrer U. Mice generated by in vitro fertilization exhibit vascular dysfunction and shortened life span. J Clin Invest 123: 5052-5060, 2013.
21. Richard V, Solans V, Favre J, Henry JP, Lallemand F, Thuillez C, Marie I. Role of endogenous endothelin in endothelial dysfunction in murine model of systemic sclerosis: tight skin mice 1. Fundam Clin Pharmacol 22: 649-655, 2008.
22. Rimoldi SF, Sartori C, Rexhaj E, Bailey DM, Marchi SF, McEneny J, Arx RV, Cerny D, Duplain H, Germond M, Allemann Y, Scherrer U. Antioxidants improve vascular function in children conceived by assisted reproductive technologies: a randomized double-blind placebo-controlled trial. Eur J Prev Cardiol. 2014 May 9. [Epub ahead of print].
23. Rimoldi SF, Sartori C, Rexhaj E, Cerny D, Von Arx R, Soria R, Germond M, Allemann Y, Scherrer U. Vascular dysfunction in children conceived by assisted reproductive technologies: underlying mechanisms and future implications. Swiss Med Wkly 144: w13973, 2014.
24. Sartori C, Allemann Y, Trueb L, Delabays A, Nicod P, Scherrer U. Augmented vasoreactivity in adult life associated with perinatal vascular insult. Lancet 353: 2205-2207, 1999.
25. Scherrer U, Rexhaj E, Allemann Y, Sartori C, Rimoldi SF. Cardiovascular dysfunction in children conceived by assisted reproductive technologies. Eur Heart J 36: 1583-1589, 2015.
26. Scherrer U, Rimoldi SF, Rexhaj E, Stuber T, Duplain H, Garcin S, de Marchi SF, Nicod P, Germond M, Allemann Y, Sartori C. Systemic and pulmonary vascular dysfunction in children conceived by assisted reproductive technologies. Circulation 125: 1890-1896, 2012.
27. Scherrer U, Sartori C. Insulin as a vascular and sympathoexcitatory hormone: implications for blood pressure regulation, insulin sensitivity, and cardiovascular morbidity. Circulation 96: 4104-4113, 1997.
28. Sharma R, Ottenhof T, Rzeczkowska PA, Niles LP. Epigenetic targets for melatonin: induction of histone H3 hyperacetylation and gene expression in C17.2 neural stem cells. J Pineal Res 45: 277-284, 2008.
29. Shi W, Haaf T. Aberrant methylation patterns at the two-cell stage as an indicator of early developmental failure. Mol Reprod Dev 63: 329-334, 2002.
30. Tamura H, Nakamura Y, Korkmaz A, Manchester LC, Tan DX, Sugino N, Reiter RJ. Melatonin and the ovary: physiological and pathophysiological implications. Fertil Steril 92: 328-343, 2009.
31. Tamura H, Takasaki A, Miwa I, Taniguchi K, Maekawa R, Asada H, Taketani T, Matsuoka A, Yamagata Y, Shimamura K, Morioka H, Ishikawa H, Reiter RJ, Sugino N. Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J Pineal Res 44: 280-287, 2008.
32. Unfer V, Raffone E, Rizzo P, Buffo S. Effect of a supplementation with myo-inositol plus melatonin on oocyte quality in women who failed to conceive in previous in vitro fertilization cycles for poor oocyte quality: a prospective, longitudinal, cohort study. Gynecol Endocrinol 27: 857-861, 2011.
33. Valenzuela-Alcaraz B, Crispi F, Bijnens B, Cruz-Lemini M, Creus M, Sitges M, Bartrons J, Civico S, Balasch J, Gratacos E. Assisted reproductive technologies are associated with cardiovascular remodeling in utero that persists postnatally. Circulation 128: 1442-1450, 2013.
34. von Arx R, Allemann Y, Sartori C, Rexhaj E, Cerny D, de Marchi SF, Soria R, Germond M, Scherrer U, Rimoldi SF. Right ventricular dysfunction in children and adolescents conceived by assisted reproductive technologies. J Appl Physiol (1985) 118: 1200-1206, 2015.
35. Yang YM, Huang A, Kaley G, Sun D. eNOS uncoupling and endothelial dysfunction in aged vessels. Am J Physiol Heart Circ Physiol 297: H1829-H1836, 2009.
36. Zhang DX, Mendoza SA, Bubolz AH, Mizuno A, Ge ZD, Li R, Warltier DC, Suzuki M, Gutterman DD. Transient receptor potential vanilloid type 4-deficient mice exhibit impaired endothelium-dependent relaxation induced by acetylcholine in vitro and in vivo. Hypertension 53: 532-538, 2009.