Effect of resveratrol on metabolic and cardiovascular function in male and female adult offspring exposed to prenatal hypoxia and a high-fat diet

Journal of Physiology

Volumn 594, Issue 5, 2016, Pages 1465-1482

  Shah, Amin ^a   Reyes, Laura M ^a   Morton, Jude S ^a   Fung, David ^a   Schneider, Jillian ^a   Davidge, Sandra T ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ADENYLATE KINASE; RESVERATROL; SUPEROXIDE; CARDIOTONIC AGENT; STILBENE DERIVATIVE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; CARDIOVASCULAR FUNCTION; CONTROLLED STUDY; DIET SUPPLEMENTATION; FEMALE; HEART FUNCTION; HYPOXIA; IN VIVO STUDY; LIPID DIET; MALE; NONHUMAN; OXIDATIVE STRESS; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; REPERFUSION; SIGNAL TRANSDUCTION; ADVERSE EFFECTS; ANIMAL; CARDIAC MUSCLE; CARDIOVASCULAR DISEASES; COMPLICATION; DRUG EFFECTS; FETUS HYPOXIA; HEART; HEART CONTRACTION; HEART VENTRICLE FUNCTION; METABOLISM; PATHOLOGY; PREGNANCY; SPRAGUE DAWLEY RAT;

ANIMALS; CARDIOTONIC AGENTS; CARDIOVASCULAR DISEASES; DIET, HIGH-FAT; FEMALE; FETAL HYPOXIA; HEART; MALE; MYOCARDIAL CONTRACTION; MYOCARDIUM; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; STILBENES; SUPEROXIDES; VENTRICULAR FUNCTION;

EID: 84959271583     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP271133     Document Type: Article

References (57)

1. Al-Hasan YM, Pinkas GA & Thompson LP (2014). Prenatal hypoxia reduces mitochondrial protein levels and cytochrome c oxidase activity in offspring guinea pig hearts. Reprod Sci 21, 883-891.
2. Alexander BT, Henry Dasinger J & Intapad S (2014). Effect of low birth weight on women's health. Clin Ther 36, 1913-1923.
3. Barker DJ (1993). Fetal origins of coronary heart disease. Br Heart J 69, 195-196.
4. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K & Clark PM (1993). Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36, 62-67.
5. Berenson GS (2002). Childhood risk factors predict adult risk associated with subclinical cardiovascular disease. The Bogalusa Heart Study. Am J Cardiol 90, 3l-7l.
6. Bjarnegard N, Morsing E, Cinthio M, Lanne T & Brodszki J (2013). Cardiovascular function in adulthood following intrauterine growth restriction with abnormal fetal blood flow. Ultrasound Obstet Gynecol 41, 177-184.
7. Camm EJ, Hansell JA, Kane AD, Herrera EA, Lewis C, Wong S, Morrell NW & Giussani DA (2010). Partial contributions of developmental hypoxia and undernutrition to prenatal alterations in somatic growth and cardiovascular structure and function. Am J Obstet Gynecol 203, 495.e424-495.e434.
8. Camm EJ, Martin-Gronert MS, Wright NL, Hansell JA, Ozanne SE & Giussani DA (2011). Prenatal hypoxia independent of undernutrition promotes molecular markers of insulin resistance in adult offspring. FASEB J 25, 420-427.
9. Comas M, Crispi F, Cruz-Martinez R, Martinez JM, Figueras F & Gratacos E (2010). Usefulness of myocardial tissue Doppler vs. conventional echocardiography in the evaluation of cardiac dysfunction in early-onset intrauterine growth restriction. Am J Obstet Gynecol 203, 45.e41-45.e47.
10. Crispi F, Hernandez-Andrade E, Pelsers MM, Plasencia W, Benavides-Serralde JA, Eixarch E, Le Noble F, Ahmed A, Glatz JF, Nicolaides KH & Gratacos E (2008). Cardiac dysfunction and cell damage across clinical stages of severity in growth-restricted fetuses. Am J Obstet Gynecol 199, 254.e251-254.e258.
11. Demicheva E & Crispi F (2014). Long-term follow-up of intrauterine growth restriction: cardiovascular disorders. Fetal Diagn Ther 36, 143-153.
12. Dernek S, Ikizler M, Erkasap N, Ergun B, Koken T, Yilmaz K, Sevin B, Kaygisiz Z & Kural T (2004). Cardioprotection with resveratrol pretreatment: improved beneficial effects over standard treatment in rat hearts after global ischemia. Scand Cardiovasc J 38, 245-254.
13. Deschamps AM, Murphy E & Sun J (2010). Estrogen receptor activation and cardioprotection in ischemia reperfusion injury. Trends Cardiovasc Med 20, 73-78.
14. Dessi A, Ottonello G & Fanos V (2012). Physiopathology of intrauterine growth retardation: from classic data to metabolomics. J Matern Fetal Neonatal Med 25, 13-18.
15. Dolinsky VW, Rueda-Clausen CF, Morton JS, Davidge ST & Dyck JR (2011). Continued postnatal administration of resveratrol prevents diet-induced metabolic syndrome in rat offspring born growth restricted. Diabetes 60, 2274-2284.
16. Evans LC, Liu H, Pinkas GA & Thompson LP (2012). Chronic hypoxia increases peroxynitrite, MMP9 expression, and collagen accumulation in fetal guinea pig hearts. Pediatr Res 71, 25-31.
17. Fouzas S, Karatza AA, Davlouros PA, Chrysis D, Alexopoulos D, Mantagos S & Dimitriou G (2014). Neonatal cardiac dysfunction in intrauterine growth restriction. Pediatr Res 75, 651-657.
18. Fullerton MD & Steinberg GR (2010). SIRT1 takes a backseat to AMPK in the regulation of insulin sensitivity by resveratrol. Diabetes 59, 551-553.
19. Gabel SA, Walker VR, London RE, Steenbergen C, Korach KS & Murphy E (2005). Estrogen receptor beta mediates gender differences in ischemia/reperfusion injury. J Mol Cell Cardiol 38, 289-297.
20. Giordano FJ (2005). Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest 115, 500-508.
21. Giussani DA, Camm EJ, Niu Y, Richter HG, Blanco CE, Gottschalk R, Blake EZ, Horder KA, Thakor AS, Hansell JA, Kane AD, Wooding FB, Cross CM & Herrera EA (2012). Developmental programming of cardiovascular dysfunction by prenatal hypoxia and oxidative stress. PLoS One 7, e31017.
22. Giussani DA & Davidge ST (2013). Developmental programming of cardiovascular disease by prenatal hypoxia. J Dev Orig Health Dis 4, 328-337.
23. Gupta P, Narang M, Banerjee BD & Basu S (2004). Oxidative stress in term small for gestational age neonates born to undernourished mothers: a case control study. BMC Pediatr 4, 14.
24. Hecher K, Campbell S, Doyle P, Harrington K & Nicolaides K (1995). Assessment of fetal compromise by Doppler ultrasound investigation of the fetal circulation. Arterial, intracardiac, and venous blood flow velocity studies. Circulation 91, 129-138.
25. Intapad S, Ojeda NB, Dasinger JH & Alexander BT (2014). Sex differences in the developmental origins of cardiovascular disease. Physiology (Bethesda) 29, 122-132.
26. Jansson T & Lambert GW (1999). Effect of intrauterine growth restriction on blood pressure, glucose tolerance and sympathetic nervous system activity in the rat at 3-4 months of age. J Hypertens 17, 1239-1248.
27. Jaquet D, Gaboriau A, Czernichow P & Levy-Marchal C (2000). Insulin resistance early in adulthood in subjects born with intrauterine growth retardation. J Clin Endocrinol Metab 85, 1401-1406.
28. Jeon BT, Jeong EA, Shin HJ, Lee Y, Lee DH, Kim HJ, Kang SS, Cho GJ, Choi WS & Roh GS (2012). Resveratrol attenuates obesity-associated peripheral and central inflammation and improves memory deficit in mice fed a high-fat diet. Diabetes 61, 1444-1454.
29. Juan ME, Vinardell MP & Planas JM (2002). The daily oral administration of high doses of trans-resveratrol to rats for 28 days is not harmful. J Nutr 132, 257-260.
30. Kane AD, Herrera EA, Camm EJ & Giussani DA (2013). Vitamin C prevents intrauterine programming of in vivo cardiovascular dysfunction in the rat. Circ J 77, 2604-2611.
31. Khatri JJ, Johnson C, Magid R, Lessner SM, Laude KM, Dikalov SI, Harrison DG, Sung HJ, Rong Y & Galis ZS (2004). Vascular oxidant stress enhances progression and angiogenesis of experimental atheroma. Circulation 109, 520-525.
32. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P, Geny B, Laakso M, Puigserver P & Auwerx J (2006). Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1α. Cell 127, 1109-1122.
33. 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 Investig 10, 265-274.
34. Ma N & Hardy DB (2012). The fetal origins of the metabolic syndrome: can we intervene? J Pregnancy 2012, 482690.
35. Patterson AJ, Xiao D, Xiong F, Dixon B & Zhang L (2012). Hypoxia-derived oxidative stress mediates epigenetic repression of PKCε gene in foetal rat hearts. Cardiovasc Res 93, 302-310.
36. Pennathur S, Wagner JD, Leeuwenburgh C, Litwak KN & Heinecke JW (2001). A hydroxyl radical-like species oxidizes cynomolgus monkey artery wall proteins in early diabetic vascular disease. J Clin Invest 107, 853-860.
37. Ram R, Mickelsen DM, Theodoropoulos C & Blaxall BC (2011). New approaches in small animal echocardiography: imaging the sounds of silence. Am J Physiol Heart Circ Physiol 301, H1765-1780.
38. Ray PS, Maulik G, Cordis GA, Bertelli AA, Bertelli A & Das DK (1999). The red wine antioxidant resveratrol protects isolated rat hearts from ischemia reperfusion injury. Free Radic Biol Med 27, 160-169.
39. Rinaudo P & Wang E (2012). Fetal programming and metabolic syndrome. Annu Rev Physiol 74, 107-130.
40. Rueda-Clausen CF, Dolinsky VW, Morton JS, Proctor SD, Dyck JR & Davidge ST (2011a). Hypoxia-induced intrauterine growth restriction increases the susceptibility of rats to high-fat diet-induced metabolic syndrome. Diabetes 60, 507-516.
41. Rueda-Clausen CF, Morton JS & Davidge ST (2009). Effects of hypoxia-induced intrauterine growth restriction on cardiopulmonary structure and function during adulthood. Cardiovasc Res 81, 713-722.
42. Rueda-Clausen CF, Morton JS, Dolinsky VW, Dyck JR & Davidge ST (2012a). Synergistic effects of prenatal hypoxia and postnatal high-fat diet in the development of cardiovascular pathology in young rats. Am J Physiol Regul Integr Comp Physiol 303, R418-426.
43. Rueda-Clausen CF, Morton JS, Lopaschuk GD & Davidge ST (2011b). Long-term effects of intrauterine growth restriction on cardiac metabolism and susceptibility to ischaemia/reperfusion. Cardiovasc Res 90, 285-294.
44. Rueda-Clausen CF, Morton JS, Oudit GY, Kassiri Z, Jiang Y & Davidge ST (2012b). Effects of hypoxia-induced intrauterine growth restriction on cardiac siderosis and oxidative stress. J Dev Orig Health Dis 3, 350-357.
45. Sahn DJ, DeMaria A, Kisslo J & Weyman A (1978). Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 58, 1072-1083.
46. Shiomi T, Tsutsui H, Matsusaka H, Murakami K, Hayashidani S, Ikeuchi M, Wen J, Kubota T, Utsumi H & Takeshita A (2004). Overexpression of glutathione peroxidase prevents left ventricular remodeling and failure after myocardial infarction in mice. Circulation 109, 544-549.
47. Sinha N & Dabla PK (2015). Oxidative stress and antioxidants in hypertension-A current review. Curr Hypertens Rev 11, 132-142.
48. Skeffington KL, Higgins JS, Mahmoud AD, Evans AM, Sferruzzi-Perri AN, Fowden AL, Yung HW, Burton GJ, Giussani DA & Moore LG (2016). Hypoxia, AMPK activation and uterine artery vasoreactivity. J Physiol 594, 1357-1369.
49. Sugden PH & Clerk A (1998). Cellular mechanisms of cardiac hypertrophy. J Mol Med (Berl) 76, 725-746.
50. Turrens JF, Lariccia J & Nair MG (1997). Resveratrol has no effect on lipoprotein profile and does not prevent peroxidation of serum lipids in normal rats. Free Radic Res 27, 557-562.
51. Wang M, Crisostomo P, Wairiuko GM & Meldrum DR (2006). Estrogen receptor-alpha mediates acute myocardial protection in females. Am J Physiol Heart Circ Physiol 290, H2204-2209.
52. Williams SJ, Campbell ME, McMillen IC & Davidge ST (2005). Differential effects of maternal hypoxia or nutrient restriction on carotid and femoral vascular function in neonatal rats. Am J Physiol Regul Integr Comp Physiol 288, R360-367.
53. Xiao X, Zhang ZX, Li WH, Feng K, Sun Q, Cohen HJ, Xu T, Wang H, Liu AM, Gong XM, Shen Y & Yi Z (2010). Low birth weight is associated with components of the metabolic syndrome. Metabolism 59, 1282-1286.
54. Xue Q & Zhang L (2009). Prenatal hypoxia causes a sex-dependent increase in heart susceptibility to ischemia and reperfusion injury in adult male offspring: role of protein kinase C epsilon. J Pharmacol Exp Ther 330, 624-632.
55. Yoshino J, Conte C, Fontana L, Mittendorfer B, Imai S, Schechtman KB, Gu C, Kunz I, Rossi Fanelli F, Patterson BW & Klein S (2012). Resveratrol supplementation does not improve metabolic function in nonobese women with normal glucose tolerance. Cell Metab 16, 658-664.
56. Zanetti M, d'Uscio LV, Peterson TE, Katusic ZS & O'Brien T (2005). Analysis of superoxide anion production in tissue. Methods Mol Med 108, 65-72.
57. Zordoky BN, Robertson IM & Dyck JR (2015). Preclinical and clinical evidence for the role of resveratrol in the treatment of cardiovascular diseases. Biochim Biophys Acta 1852, 1155-1177.