Fetal undernutrition is associated with perinatal sex-dependent alterations in oxidative status

Journal of Nutritional Biochemistry

Volumn 26, Issue 12, 2015, Pages 1650-1659

  Rodríguez Rodríguez, Pilar ^a   de Pablo, Angel Luis López ^a   Condezo Hoyos, Luis ^a   Martín Cabrejas, María Angeles ^a   Aguilera, Yolanda ^a   Ruiz Hurtado, Gema ^b,c   Gutierrez Arzapalo, Perla Y ^a   Ramiro Cortijo, David ^a   Fernández Alfonso, María Soledad ^b   González, María del Carmen ^a   Arribas, Silvia M ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c HOSPITAL UNIVERSITARIO 12 DE OCTUBRE   (Spain)

Author keywords

Experimental models; Fetal programming; Hypertension; Melatonin; Oxidative stress; Plasma; Sex

Indexed keywords

CARBONYL DERIVATIVE; CATALASE; ESTRADIOL; GLUTATHIONE; MELATONIN; SUPEROXIDE; THIOL DERIVATIVE; ANTIOXIDANT; BIOLOGICAL MARKER; ESTROGEN; OXYGEN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; FETAL MALNUTRITION; FETUS; GENDER; HYPERTENSION; IN VIVO STUDY; MALE; MALNUTRITION; MATERNAL UNDERNUTRITION; NONHUMAN; OXIDATIVE STRESS; RAT; SEX DIFFERENCE; SUPEROXIDE ANION SCAVENGING ACTIVITY; TOTAL ANTIOXIDANT CAPACITY; ANIMAL; BLOOD; BODY WEIGHT; DISEASE MODEL; INTRAUTERINE GROWTH RETARDATION; METABOLISM; NEWBORN; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; ANTIOXIDANTS; BIOMARKERS; BLOOD PRESSURE; BODY WEIGHT; CATALASE; DISEASE MODELS, ANIMAL; ESTRADIOL; ESTROGENS; FEMALE; FETAL GROWTH RETARDATION; FETAL NUTRITION DISORDERS; GLUTATHIONE; MALE; MELATONIN; OXIDATIVE STRESS; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; SEX FACTORS; SULFHYDRYL COMPOUNDS;

EID: 84983171459     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2015.08.004     Document Type: Article

References (65)

1. Murray C.J., Vos T., Lozano R., Naghavi M., Flaxman A.D., Michaud C., et al. Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2013, 380:2197-2223.
2. Ebrahim S., Pearce N., Smeeth L., Casas J.P., Jaffar S., Piot P. Tackling non-communicable diseases in low-and middle-income countries: is the evidence from high-income countries all we need?. PLoS Med 2013, 10:e1001377.
3. Barker D.J., Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1986, 327:1077-1081.
4. Hanson M.A., Gluckman P.D. Developmental origins of health and disease: new insights. Basic Clin Pharmacol Toxicol 2008, 102:90-93.
5. Nuyt A.M., Alexander B.T. Developmental programming and hypertension. Curr Opin Nephrol Hypertens 2009, 18:144-152.
6. Camps J., García-Heredia A. Introduction: oxidation and inflammation, a molecular link between non-communicable diseases. Anonymous Oxidative Stress and Inflammation in Non-Communicable Diseases-Molecular Mechanisms and Perspectives in Therapeutics 2014, 1-4. Springer.
7. Thompson L.P., Al-Hasan Y. Impact of oxidative stress in fetal programming. J Pregnancy 2012, 2012. 10.1155/2012/582748.
8. Tarry-Adkins J.L., Martin-Gronert M.S., Fernandez-Twinn D.S., Hargreaves I., Alfaradhi M.Z., Land J.M., et al. Poor maternal nutrition followed by accelerated postnatal growth leads to alterations in DNA damage and repair, oxidative and nitrosative stress, and oxidative defense capacity in rat heart. FASEB J 2013, 27:379-390.
9. Paixao A.D., Alexander B.T. How the kidney is impacted by the perinatal maternal environment to develop hypertension. Biol Reprod 2013, 89:144.
10. Bi J., Contag S.A., Chen K., Su Y., Figueroa J.P., Chappell M.C., et al. Sex-specific effect of antenatal betamethasone exposure on renal oxidative stress induced by angiotensins in adult sheep. Am J Physiol Renal Physiol 2014, 307:F1013-F1022.
11. Franco M.C., Akamine E.H., Rebouças N., Carvalho M.H.C., Tostes R.C., Nigro D., et al. Long-term effects of intrauterine malnutrition on vascular function in female offspring: implications of oxidative stress. Life Sci 2007, 80:709-715.
12. Halliwell B. Free radicals and other reactive species in disease 2005, Wiley Online Library.
13. Condezo-Hoyos L., Rubio M., Arribas S.M., España-Caparrós G., Rodríguez-Rodríguez P., Mujica-Pacheco E., et al. A plasma oxidative stress global index in early stages of chronic venous insufficiency. J Vasc Surg 2013, 57:205-213.
14. Ruiz-Hurtado G., Condezo-Hoyos L., Pulido-Olmo H., Aranguez I., del Carmen Gónzalez M., Arribas S., et al. Development of albuminuria and enhancement of oxidative stress during chronic renin-angiotensin system suppression. J Hypertens 2014, 32:2082-2091.
15. Veglia F., Cavalca V., Tremoli E. OXY-SCORE: a global index to improve evaluation of oxidative stress by combining pro-and antioxidant markers. Anonymous Advanced Protocols in Oxidative Stress II 2010, 197-213. Springer.
16. Grigore D., Ojeda N.B., Alexander B.T. Sex differences in the fetal programming of hypertension. Gend Med 2008, 5:S121-S132.
17. Ozaki T., Nishina H., Hanson M.A., Poston L. Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring. J Physiol 2001, 530:141-152.
18. Holemans K., Gerber R., Meurrens K., Clerck F.D., Poston L., Van Assche F.A. Maternal food restriction in the second half of pregnancy affects vascular function but not blood pressure of rat female offspring. Br J Nutr 1999, 81:73-80.
19. Ojeda N., Intapad S., Alexander B. Sex differences in the developmental programming of hypertension. Acta Physiol 2014, 210:307-316.
20. Miller V.M., Reckelhoff J.F., Sieck G.C. Physiology's impact: stop ignoring the obvious-sex matters!. Physiology (Bethesda) 2014, 29:4-5.
21. Khorram O., Momeni M., Desai M., Ross M.G. Nutrient restriction in utero induces remodeling of the vascular extracellular matrix in rat offspring. Reprod Sci 2007, 14:73-80.
22. Khorram O., Keen-Rinehart E., Chuang T., Ross M.G., Desai M. Maternal undernutrition induces premature reproductive senescence in adult female rat offspring. Fertil Steril 2015, 103:291-298.
23. Suzuki M., Shibanuma M., Kimura S. Effect of severe maternal dietary restriction on growth and intra-abdominal adipose tissue weights in offspring rats. J Nutr Sci Vitaminol 2010, 56:293-298.
24. Howie G., Sloboda D., Vickers M. Maternal undernutrition during critical windows of development results in differential and sex-specific effects on postnatal adiposity and related metabolic profiles in adult rat offspring. Br J Nutr 2012, 108:298-307.
25. Munoz-Valverde D., Rodriguez-Rodriguez P., Gutierrez-Arzapalo P.Y., de Pablo A.L., Gonzalez M.C., Lopez-Gimenez R., et al. Effect of fetal undernutrition and postnatal overfeeding on rat adipose tissue and organ growth at early stages of postnatal development. Physiol Res 2015, 64:547-559.
26. Reiter R.J., Manchester L., Tan D. Melatonin in walnuts: influence on levels of melatonin and total antioxidant capacity of blood. Nutrition 2005, 21:920-924.
27. Condezo-Hoyos L., Arribas S.M., Abderrahim F., Somoza B., Gil-Ortega M., Diaz-Gil J.J., et al. Liver growth factor treatment reverses vascular and plasmatic oxidative stress in spontaneously hypertensive rats. J Hypertens 2012, 30:1185-1194.
28. Hawkins C.L., Morgan P.E., Davies M.J. Quantification of protein modification by oxidants. Free Radic Biol Med 2009, 46:965-988.
29. Saleh L., Plieth C. A coelenterazine-based luminescence assay to quantify high-molecular-weight superoxide anion scavenger activities. Nat Protoc 2010, 5:1635-1641.
30. Blackmore H., Ozanne S. Maternal diet-induced obesity and offspring cardiovascular health. J Dev Orig Health Dis 2013, 4:338-347.
31. Norman A.M., Miles-Chan J.L., Thompson N.M., Breier B.H., Huber K. Postnatal development of metabolic flexibility and enhanced oxidative capacity after prenatal undernutrition. Reprod Sci 2012, 19:607-614.
32. Kerkhof G.F., Willemsen R.H., Leunissen R.W., Breukhoven P.E., Hokken-Koelega A.C. Health profile of young adults born preterm: negative effects of rapid weight gain in early life. J Clin Endocrinol Metab 2012, 97:4498-4506.
33. Corpeleijn W.E., Kouwenhoven S.M., van Goudoever J.B. Optimal growth of preterm infants. World Rev Nutr Diet 2013, 106:149-155.
34. Singhal A., Lucas A. Early origins of cardiovascular disease: is there a unifying hypothesis?. Lancet 2004, 363:1642-1645.
35. Keen-Rhinehart E., Desai M., Ross M.G. Central insulin sensitivity in male and female juvenile rats. Horm Behav 2009, 56:275-280.
36. Woods L.L., Ingelfinger J.R., Nyengaard J.R., Rasch R. Maternal protein restriction suppresses the newborn renin-angiotensin system and programs adult hypertension in rats. Pediatr Res 2001, 49:460-467.
37. Touyz R.M., Briones A.M. Reactive oxygen species and vascular biology: implications in human hypertension. Hypertens Res 2010, 34:5-14.
38. González J., Valls N., Brito R., Rodrigo R. Essential hypertension and oxidative stress: new insights. World J Cardiol 2014, 6:353.
39. Conde M.V., Gonzalez M.C., Quintana-Villamandos B., Abderrahim F., Briones A.M., Condezo-Hoyos L., et al. Liver growth factor treatment restores cell-extracellular matrix balance in resistance arteries and improves left ventricular hypertrophy in SHR. Am J Physiol Heart Circ Physiol 2011, 301:H1153-H1165.
40. Poston L. Influence of maternal nutritional status on vascular function in the offspring. Microcirculation 2011, 18:256-262.
41. Ingelfinger J.R., Nuyt A. Impact of fetal programming, birth weight, and infant feeding on later hypertension. J Clin Hypertens 2012, 14:365-371.
42. Cambonie G., Comte B., Yzydorczyk C., Ntimbane T., Germain N., Le N.L., et al. Antenatal antioxidant prevents adult hypertension, vascular dysfunction, and microvascular rarefaction associated with in utero exposure to a low-protein diet. Am J Physiol Regul Integr Comp Physiol 2007, 292:R1236-R1245.
43. Nuyt A. Mechanisms underlying developmental programming of elevated blood pressure and vascular dysfunction: evidence from human studies and experimental animal models. Clin Sci 2008, 114:1-17.
44. He Z.X., Sun Z.H., Tan Z.L., Tang S.X., Zhou C.S., Han X.F., et al. Effects of maternal protein or energy restriction during late gestation on antioxidant status of plasma and immune tissues in postnatal goats. J Anim Sci 2012, 90:4319-4326.
45. Fetoui H., Garoui M., Zeghal N. Protein restriction in pregnant-and lactating rats-induced oxidative stress and hypohomocysteinaemia in their offspring. J Anim Physiol Anim Nutr 2009, 93:263-270.
46. Veskoukis A.S., Nikolaidis M.G., Kyparos A., Kouretas D. Blood reflects tissue oxidative stress depending on biomarker and tissue studied. Free Radic Biol Med 2009, 47:1371-1374.
47. Jones J.E., Jurgens J.A., Evans S.A., Ennis R.C., Villar V.A.M., Jose P.A. Mechanisms of fetal programming in hypertension. Int J Pediatr 2012, 2012. 10.1155/2012/584831.
48. Ojeda N.B., Grigore D., Yanes L.L., Iliescu R., Robertson E.B., Zhang H. Testosterone contributes to marked elevations in mean arterial pressure in adult male intrauterine growth restricted offspring. Am J Physiol Regul Integr Comp Physiol 2007, 292:R758-R763.
49. Reyes M.R., Sifuentes-Alvarez A., Lazalde B. Estrogens are potentially the only steroids with an antioxidant role in pregnancy: in vitro evidence. Acta Obstet Gynecol Scand 2006, 85:1090-1093.
50. Gabory A., Attig L., Junien C. Sexual dimorphism in environmental epigenetic programming. Mol Cell Endocrinol 2009, 304:8-18.
51. Tarrade A., Panchenko P., Junien C., Gabory A. Placental contribution to nutritional programming of health and diseases: epigenetics and sexual dimorphism. J Exp Biol 2015, 218:50-58.
52. Jansson T., Scholtbach V., Powell T.L. Placental transport of leucine and lysine is reduced in intrauterine growth restriction. Pediatr Res 1998, 44:532-537.
53. Vickers M.H. Early life nutrition, epigenetics and programming of later life disease. Nutrients 2014, 6:2165-2178.
54. Bermejo-Alvarez P., Rizos D., Rath D., Lonergan P., Gutierrez-Adan A. Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc Natl Acad Sci U S A 2010, 107:3394-3399.
55. Chen Y., Sheen J., Tiao M., Tain Y., Huang L. Roles of melatonin in fetal programming in compromised pregnancies. Int J Mol Sci 2013, 14:5380-5401.
56. Rodriguez C., Mayo J.C., Sainz R.M., Antolin I., Herrera F., Martin V. Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 2004, 36:1-9.
57. Reiter R.J., Tan D., Osuna C., Gitto E. Actions of melatonin in the reduction of oxidative stress. J Biomed Sci 2000, 7:444-458.
58. Okatani Y., Wakatsuki A., Reiter R.J., Miyahara Y. Melatonin reduces oxidative damage of neural lipids and proteins in senescence-accelerated mouse. Neurobiol Aging 2002, 23:639-644.
59. Maggioni C., Cornelissen G., Antinozzi R., Ferrario M., Grafe A., Halberg F. A half-yearly aspect of circulating melatonin in pregnancies complicated by intrauterine growth retardation. Neuroendocrinol Lett 1999, 20:55-68.
60. Lemley C., Camacho L., Meyer A., Kapphahn M., Caton J., Vonnahme K. Dietary melatonin supplementation alters uteroplacental amino acid flux during intrauterine growth restriction in ewes. Animal 2013, 7:1500-1507.
61. Nagai R., Watanabe K., Wakatsuki A., Hamada F., Shinohara K., Hayashi Y., et al. Melatonin preserves fetal growth in rats by protecting against ischemia/reperfusion-induced oxidative/nitrosative mitochondrial damage in the placenta. J Pineal Res 2008, 45:271-276.
62. Richter H.G., Hansell J.A., Raut S., Giussani D.A. Melatonin improves placental efficiency and birth weight and increases the placental expression of antioxidant enzymes in undernourished pregnancy. J Pineal Res 2009, 46:357-364.
63. Georgeson G.D., Szony B.J., Streitman K., Varga I.S., Kovács A., Kovács L., et al. Antioxidant enzyme activities are decreased in preterm infants and in neonates born via caesarean section. Eur J Obstet Gynecol Reprod Biol 2002, 103:136-139.
64. Lee Y., Chou Y. Antioxidant profiles in full term and preterm neonates. Chang Gung Med J 2005, 28:846.
65. Gitto E., Marseglia L., Manti S., D'Angelo G., Barberi I., Salpietro C., et al. Protective role of melatonin in neonatal diseases. Oxidative Med Cell Longev 2013, 2013. 10.1155/2013/980374.