Vascular effects of aerobic exercise training in rat adult offspring exposed to hypoxia-induced intrauterine growth restriction

Journal of Physiology

Volumn 593, Issue 8, 2015, Pages 1913-1929

  Reyes, Laura M ^a   Morton, Jude S ^a   Kirschenman, Raven ^a   Delorey, Darren S ^a   Davidge, Sandra T ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

1 [(2 CHLOROPHENYL)DIPHENYLMETHYL] 1H PYRAZOLE; APAMIN; CORTICOSTERONE; INDOMETACIN; METHACHOLINE; N(G) NITROARGININE METHYL ESTER; PHENYLEPHRINE; POTASSIUM; SCAVENGER; CHOLINE; METHYLCHOLINE; VASOCONSTRICTOR AGENT; VASODILATOR AGENT;

ADULT; AEROBIC EXERCISE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY COMPOSITION; BODY WEIGHT; CONCENTRATION RESPONSE; CONTROLLED STUDY; ECHOGRAPHY; ENDOTHELIAL DYSFUNCTION; EXERCISE TOLERANCE; EXPOSURE; FEMALE; FOOD INTAKE; GASTROCNEMIUS MUSCLE; GESTATION PERIOD; HYPERPOLARIZATION; HYPOXIA; INTRAUTERINE GROWTH RETARDATION; MALE; MESENTERIC ARTERY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PREGNANCY; PRIORITY JOURNAL; PROGENY; RAT; SPRAGUE DAWLEY RAT; TREADMILL; VASOCONSTRICTION; VASODILATATION; ANALOGS AND DERIVATIVES; ANIMAL; COMPLICATION; DRUG EFFECTS; FETAL GROWTH RETARDATION; PATHOPHYSIOLOGY; PHYSIOLOGY; PRENATAL EXPOSURE; SEX DIFFERENCE; VASCULAR ENDOTHELIUM;

ANIMALS; CHOLINE; ENDOTHELIUM, VASCULAR; FEMALE; FETAL GROWTH RETARDATION; HYPOXIA; MALE; MESENTERIC ARTERIES; PHENYLEPHRINE; PHYSICAL CONDITIONING, ANIMAL; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; SEX FACTORS; VASOCONSTRICTION; VASOCONSTRICTOR AGENTS; VASODILATION; VASODILATOR AGENTS;

EID: 84927696557     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.288449     Document Type: Article

References (60)

1. ACSM (2013). ACSM's Guidelines for Exercise Testing and Prescription, 9th edn. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Allen JD, Stabler T, Kenjale AA, Ham KL, Robbins JL, Duscha BD, Kraus WE & Annex BH (2014). Diabetes status differentiates endothelial function and plasma nitrite response to exercise stress in peripheral arterial disease following supervised training. J Diabetes Complications 28, 219-225.
3. Arida RM, Scorza CA, da Silva AV, Scorza FA & Cavalheiro EA (2004). Differential effects of spontaneous versus forced exercise in rats on the staining of parvalbumin-positive neurons in the hippocampal formation. Neurosci Lett 364, 135-138.
4. Barker DJ, Winter PD, Osmond C, Margetts B & Simmonds SJ (1989). Weight in infancy and death from ischaemic heart disease. Lancet 2, 577-580.
5. Batinić-Haberle I, Cuzzocrea S, Rebouças JS, Ferrer-Sueta G, Mazzon E, Di Paola R, Radi R, Spasojević I, Benov L & Salvemini D (2009). Pure MnTBAP selectively scavenges peroxynitrite over superoxide: comparison of pure and commercial MnTBAP samples to MnTE-2-PyP in two models of oxidative stress injury, an SOD-specific Escherichia coli model and carrageenan-induced pleurisy. Free Radic Biol Med 46, 192-201.
6. Beckman JS & Koppenol WH (1996). Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol Cell Physiol 271, C1424-C1437.
7. Bourque SL, Gragasin FS, Quon AL, Mansour Y, Morton JS & Davidge ST (2013). Prenatal hypoxia causes long-term alterations in vascular endothelin-1 function in aged male, but not female, offspring. Hypertension 62, 753-758.
8. 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.
9. Campos JC, Gomes KM & Ferreira JC (2013). Impact of exercise training on redox signaling in cardiovascular diseases. Food Chem Toxicol 62, 107-119.
10. Class QA, Rickert ME, Lichtenstein P & D'Onofrio BM (2014). Birth weight, physical morbidity, and mortality: A population-based sibling-comparison study. Am J Epidemiol 179, 550-558.
11. Desai M, Gayle D, Han G & Ross MG (2007). Programmed hyperphagia due to reduced anorexigenic mechanisms in intrauterine growth-restricted offspring. Reprod Sci 14, 329-337.
12. Fukami T, Sun X, Li T, Desai M & Ross MG (2012). Mechanism of programmed obesity in intrauterine fetal growth restricted offspring: paradoxically enhanced appetite stimulation in fed and fasting states. Reprod Sci 19, 423-430.
13. Garg M, Thamotharan M, Oak SA, Pan G, Maclaren DC, Lee PW & Devaskar SU (2009). Early exercise regimen improves insulin sensitivity in the intrauterine growth-restricted adult female rat offspring. Am J Physiol Endocrinol Metab 296, E272-E281.
14. 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.
15. Giussani DA & Davidge ST (2013). Developmental programming of cardiovascular disease by prenatal hypoxia. J Dev Orig Health Dis 4, 328-337.
16. Green DJ, Maiorana A, O'Driscoll G & Taylor R (2004). Effect of exercise training on endothelium-derived nitric oxide function in humans. J Physiol 561, 1-25.
17. Green DJ, Spence A, Halliwill JR, Cable NT & Thijssen DH (2011). Exercise and vascular adaptation in asymptomatic humans. Exp Physiol 96, 57-70.
18. Gündüz F, Koçer G, Ulker S, Meiselman HJ, Başkurt OK & Sentürk UK (2011). Exercise training enhances flow-mediated dilation in spontaneously hypertensive rats. Physiol Res 60, 589-597.
19. Hanson M, Godfrey KM, Lillycrop KA, Burdge GC & Gluckman PD (2011). Developmental plasticity and developmental origins of non-communicable disease: theoretical considerations and epigenetic mechanisms. Prog Biophys Mol Biol 106, 272-280.
20. Hemmings DG, Williams SJ & Davidge ST (2005). Increased myogenic tone in 7-month-old adult male but not female offspring from rat dams exposed to hypoxia during pregnancy. Am J Physiol Heart Circ Physiol 289, H674-H682.
21. Herrera EA, Kane AD, Hansell JA, Thakor AS, Allison BJ, Niu Y & Giussani DA (2012). A role for xanthine oxidase in the control of fetal cardiovascular function in late gestation sheep. J Physiol 590, 1825-1837.
22. 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.
23. Jendzjowsky NG & DeLorey DS (2011). A prospective evaluation of non-interval- and interval-based exercise training progressions in rodents. Appl Physiol Nutr Metab 36, 723-729.
24. Jendzjowsky NG & DeLorey DS (2013). Short-term exercise training augments 2-adrenoreceptor-mediated sympathetic vasoconstriction in resting and contracting skeletal muscle. J Physiol 591, 5221-5233.
25. Kane AD, Herrera EA, Hansell JA & Giussani DA (2012). Statin treatment depresses the fetal defence to acute hypoxia via increasing nitric oxide bioavailability. J Physiol 590, 323-334.
26. Kingdom JC & Kaufmann P (1997). Oxygen and placental villous development: origins of fetal hypoxia. Placenta 18, 613-621; discussion 623-626.
27. Laker RC, Gallo LA, Wlodek ME, Siebel AL, Wadley GD & McConell GK (2011). Short-term exercise training early in life restores deficits in pancreatic β-cell mass associated with growth restriction in adult male rats. Am J Physiol Endocrinol Metab 301, E931-E940.
28. Lawn JE, Cousens S & Zupan J; Lancet Neonatal Survival Steering Team (2005). 4 million neonatal deaths: When? Where? Why? Lancet 365, 891-900.
29. Leasure JL & Jones M (2008). Forced and voluntary exercise differentially affect brain and behavior. Neuroscience 156, 456-465.
30. Lesage J, Dufourny L, Laborie C, Bernet F, Blondeau B, Avril I, Breant B & Dupouy JP (2002). Perinatal malnutrition programs sympathoadrenal and hypothalamic-pituitary-adrenal axis responsiveness to restraint stress in adult male rats. J Neuroendocrinol 14, 135-143.
31. Maeda S, Sugawara J, Yoshizawa M, Otsuki T, Shimojo N, Jesmin S, Ajisaka R, Miyauchi T & Tanaka H (2009). Involvement of endothelin-1 in habitual exercise-induced increase in arterial compliance. Acta Physiol (Oxf) 196, 223-229.
32. Matsumoto T, Kakami M, Noguchi E, Kobayashi T & Kamata K (2007). Imbalance between endothelium-derived relaxing and contracting factors in mesenteric arteries from aged OLETF rats, a model of Type 2 diabetes. Am J Physiol Heart Circ Physiol 293, H1480-H1490.
33. Mazzuca MQ, Tare M, Parkington HC, Dragomir NM, Parry LJ & Wlodek ME (2012). Uteroplacental insufficiency programmes vascular dysfunction in non-pregnant rats: compensatory adaptations in pregnancy. J Physiol 590, 3375-3388.
34. 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.
35. + channel SK3 and connexin40 in arteriolar dilations during skeletal muscle contraction. FASEB J 24, 3572-3579.
36. Minami A, Ishimura N, Harada N, Sakamoto S, Niwa Y & Nakaya Y (2002). Exercise training improves acetylcholine-induced endothelium-dependent hyperpolarization in type 2 diabetic rats, Otsuka Long-Evans Tokushima fatty rats. Atherosclerosis 162, 85-92.
37. + channels in diabetic dyslipidemic pigs is prevented by exercise. J Appl Physiol (1985) 95, 1179-1193.
38. Morton JS, Rueda-Clausen CF & Davidge ST (2010). Mechanisms of endothelium-dependent vasodilation in male and female, young and aged offspring born growth restricted. Am J Physiol Regul Integr Comp Physiol 298, R930-R938.
39. Morton JS, Rueda-Clausen CF & Davidge ST (2011). Flow-mediated vasodilation is impaired in adult rat offspring exposed to prenatal hypoxia. J Appl Physiol (1985) 110, 1073-1082.
40. Olusanya BO(2010). Intrauterine growth restriction in a low-income country: Risk factors, adverse perinatal outcomes and correlation with current WHO Multicenter Growth Reference. Early Hum Dev 86, 439-444.
41. Ozaki T, Nishina H, Hanson MA & Poston L (2001). Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring. J Physiol 530, 141-152.
42. Payne JA, Alexander BT & Khalil RA (2003). Reduced endothelial vascular relaxation in growth-restricted offspring of pregnant rats with reduced uterine perfusion. Hypertension 42, 768-774.
43. Powers SK, Quindry JC & Kavazis AN (2008). Exercise-induced cardioprotection against myocardial ischemia-reperfusion injury. Free Radic Biol Med 44, 193-201.
44. Rueda-Clausen CF, Dolinsky VW, Morton JS, Proctor SD, Dyck JR & Davidge ST (2011). Hypoxia-induced intrauterine growth restriction increases the susceptibility of rats to high-fat diet-induced metabolic syndrome. Diabetes 60, 507-516.
45. 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.
46. Rush JW, Turk JR & Laughlin MH (2003). Exercise training regulates SOD-1 and oxidative stress in porcine aortic endothelium. Am J Physiol Heart Circ Physiol 284, H1378-H1387.
47. Santos MS & Joles JA (2012). Early determinants of cardiovascular disease. Best Pract Res Clin Endocrinol Metab 26, 581-597.
48. Sessa WC, Pritchard K, Seyedi N, Wang J & Hintze TH (1994). Chronic exercise in dogs increases coronary vascular nitric oxide production and endothelial cell nitric oxide synthase gene expression. Circ Res 74, 349-353.
49. Stewart KG, Zhang Y & Davidge ST (2000). Aging increases PGHS-2-dependent vasoconstriction in rat mesenteric arteries. Hypertension 35, 1242-1247.
50. Thakor AS, Herrera EA, Serón-Ferré M & Giussani DA (2010). Melatonin and vitamin C increase umbilical blood flow via nitric oxide-dependent mechanisms. J Pineal Res 49, 399-406.
51. Vanhoutte PM, Feletou M & Taddei S (2005). Endothelium-dependent contractions in hypertension. Br J Pharmacol 144, 449-458.
52. Vega CC, Reyes-Castro LA, Bautista CJ, Larrea F, Nathanielsz PW & Zambrano E (2013). Exercise in obese female rats has beneficial effects on maternal and male and female offspring metabolism. Int J Obes (Lond) (in press; DOI: 10.1038/ijo.2013.150).
53. Wang J, Wolin MS & Hintze TH (1993). Chronic exercise enhances endothelium-mediated dilation of epicardial coronary artery in conscious dogs. Circ Res 73, 829-838.
54. Wang X, Lin G, Liu C, Feng C, Zhou H, Wang T, Li D, Wu G & Wang J (2014). Temporal proteomic analysis reveals defects in small-intestinal development of porcine fetuses with intrauterine growth restriction. J Nutr Biochem 25, 785-795.
55. Williams SJ, Campbell ME, McMillen IC & Davidge ST (2005a). 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-R367.
56. Williams SJ, Hemmings DG, Mitchell JM, McMillen IC & Davidge ST (2005b). Effects of maternal hypoxia or nutrient restriction during pregnancy on endothelial function in adult male rat offspring. J Physiol 565, 125-135.
57. Wu G, Imhoff-Kunsch B & Girard AW (2012). Biological mechanisms for nutritional regulation of maternal health and fetal development. Paediatr Perinat Epidemiol 26 (Suppl. 1), 4-26.
58. Xu Y, Williams SJ, O'Brien D & Davidge ST (2006). Hypoxia or nutrient restriction during pregnancy in rats leads to progressive cardiac remodeling and impairs postischemic recovery in adult male offspring. FASEB J 20, 1251-1253.
59. Yen MH, Yang JH, Sheu JR, Lee YM & Ding YA (1995). Chronic exercise enhances endothelium-mediated dilation in spontaneously hypertensive rats. Life Sci 57, 2205-2213.
60. Zguira MS, Vincent S, LeDouairon Lahaye S, Malarde L, Tabka Z & Saïag B (2013). Intense exercise training is not effective to restore the endothelial NO-dependent relaxation in STZ-diabetic rat aorta. Cardiovasc Diabetol 12, 32.