Journal of Pediatric Biochemistry 2016; 06(02): 96-102
DOI: 10.1055/s-0036-1593811
Review Article
Georg Thieme Verlag KG Stuttgart · New York

Fetal Programming, Maternal Nutrition, and Oxidative Stress Hypothesis

Serafina Perrone
1   Department of Molecular and Developmental Medicine, General Hospital “Santa Maria alle Scotte,” University of Siena, Siena, Italy
,
Maria Luisa Tataranno
2   Department of Neonatology, Wilhelmina Children's Hospital, University Medical Centre Utrecht, Utrecht, The Netherlands
,
Antonino Santacroce
1   Department of Molecular and Developmental Medicine, General Hospital “Santa Maria alle Scotte,” University of Siena, Siena, Italy
,
Carlotta Bracciali
1   Department of Molecular and Developmental Medicine, General Hospital “Santa Maria alle Scotte,” University of Siena, Siena, Italy
,
Marina Riccitelli
1   Department of Molecular and Developmental Medicine, General Hospital “Santa Maria alle Scotte,” University of Siena, Siena, Italy
,
Maria Gabriella Alagna
1   Department of Molecular and Developmental Medicine, General Hospital “Santa Maria alle Scotte,” University of Siena, Siena, Italy
,
Mariangela Longini
1   Department of Molecular and Developmental Medicine, General Hospital “Santa Maria alle Scotte,” University of Siena, Siena, Italy
3   Clinical Pathology, AOUS Siena, Italy
,
Elisa Belvisi
1   Department of Molecular and Developmental Medicine, General Hospital “Santa Maria alle Scotte,” University of Siena, Siena, Italy
,
Francesco Bazzini
1   Department of Molecular and Developmental Medicine, General Hospital “Santa Maria alle Scotte,” University of Siena, Siena, Italy
,
Giuseppe Buonocore
1   Department of Molecular and Developmental Medicine, General Hospital “Santa Maria alle Scotte,” University of Siena, Siena, Italy
,
on behalf of the “Gruppo di Studio di Biochimica Clinica Neonatale della Società Italiana di Neonatologia” › Institutsangaben
Weitere Informationen

Publikationsverlauf

25. Juli 2016

17. August 2016

Publikationsdatum:
25. Oktober 2016 (online)

Abstract

Fetal programming occurs when the normal pattern of fetal development is disrupted by an abnormal stimulus or an “insult” during intrauterine life, which leads to adaptations by the fetus to allow its survival but could finally result in permanent structural and physiological changes with long-term consequences in adulthood. The availability of nutrients, hormones, and respiratory gases is the principal determinant of fetal growth and offspring's subsequent health. Fetal nutrient and oxygen availability depend on the rate of transfer across the “placental barrier.” Nutritional status of the mother is also important: both maternal undernutrition and/or overnutrition during early gestation may increase the incidence of cardiovascular and metabolic disorders in the offspring in later life. Oxidative stress has been supposed to be the link between adverse intrauterine environment and later elevated risks of chronic diseases. It is an important initiating mechanism underlying the programming process due to suboptimal nutrition. Antioxidant vitamins, proteins, and trace elements can be compromised under condition of poor maternal nutrition leading to oxidant/antioxidant imbalance during pregnancy. On the other hand, maternal overnutrition is associated to chronic inflammatory states that increase free radicals' production. Developing dietary strategies to optimize maternal nutrition is necessary to supply the fetus with appropriate substrates and to avoid fetal redox status disruption.

 
  • References

  • 1 Gluckman PD, Hanson MA, Low FM. The role of developmental plasticity and epigenetics in human health. Birth Defects Res C Embryo Today 2011; 93 (1) 12-18
  • 2 Barker DJ. Fetal programming of coronary heart disease. Trends Endocrinol Metab 2002; 13 (9) 364-368
  • 3 Barker DJ. The origins of the developmental origins theory. J Intern Med 2007; 261 (5) 412-417
  • 4 Barker DJ, Gluckman PD, Robinson JS. Conference report: fetal origins of adult disease – report of the First International Study Group, Sydney, 29–30 October 1994. Placenta 1995; 16 (3) 317-320
  • 5 Burton GJ, Fowden AL. Review: the placenta and developmental programming: balancing fetal nutrient demands with maternal resource allocation. Placenta 2012; 33 (Suppl): S23-S27
  • 6 Myatt L. Placental adaptive responses and fetal programming. J Physiol 2006; 572 (Pt 1) 25-30
  • 7 Bazer FW, Wu G, Spencer TE, Johnson GA, Burghardt RC, Bayless K. Novel pathways for implantation and establishment and maintenance of pregnancy in mammals. Mol Hum Reprod 2010; 16 (3) 135-152
  • 8 Spencer TE, Bazer FW. Conceptus signals for establishment and maintenance of pregnancy. Reprod Biol Endocrinol 2004; 2: 49
  • 9 Bazer FW, Wu G, Johnson GA, Kim J, Song G. Uterine histotroph and conceptus development: select nutrients and secreted phosphoprotein 1 affect mechanistic target of rapamycin cell signaling in ewes. Biol Reprod 2011; 85 (6) 1094-1107
  • 10 Burton GJ, Charnock-Jones DS, Jauniaux E. Regulation of vascular growth and function in the human placenta. Reproduction 2009; 138 (6) 895-902
  • 11 Burton GJ, Fowden AL. The placenta: a multifaceted, transient organ. Philos Trans R Soc Lond B Biol Sci 2015; 370 (1663) 20140066
  • 12 Bloomfield FH, Spiroski AM, Harding JE. Fetal growth factors and fetal nutrition. Semin Fetal Neonatal Med 2013; S1744-165X(13)00022-X
  • 13 Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 2008; 359 (1) 61-73
  • 14 Sugden MC, Holness MJ. Gender-specific programming of insulin secretion and action. J Endocrinol 2002; 175 (3) 757-767
  • 15 Bernal AJ, Jirtle RL. Epigenomic disruption: the effects of early developmental exposures. Birth Defects Res A Clin Mol Teratol 2010; 88 (10) 938-944
  • 16 Wang J, Wu Z, Li D , et al. Nutrition, epigenetics, and metabolic syndrome. Antioxid Redox Signal 2012; 17 (2) 282-301
  • 17 Lumey LH. Reproductive outcomes in women prenatally exposed to undernutrition: a review of findings from the Dutch famine birth cohort. Proc Nutr Soc 1998; 57 (1) 129-135
  • 18 Roseboom T, de Rooij S, Painter R. The Dutch famine and its long-term consequences for adult health. Early Hum Dev 2006; 82 (8) 485-491
  • 19 Painter RC, Roseboom TJ, Bleker OP. Prenatal exposure to the Dutch famine and disease in later life: an overview. Reprod Toxicol 2005; 20 (3) 345-352
  • 20 Bleker LS, de Rooij SR, Painter RC, van der Velde N, Roseboom TJ. Prenatal undernutrition and physical function and frailty at the age of 68 years: the Dutch famine birth cohort study. J Gerontol A Biol Sci Med Sci 2016; 71 (10) 1306-1314
  • 21 Fernandez-Twinn DS, Ozanne SE. Early life nutrition and metabolic programming. Ann N Y Acad Sci 2010; 1212: 78-96
  • 22 Li M, Sloboda DM, Vickers MH. Maternal obesity and developmental programming of metabolic disorders in offspring: evidence from animal models. Exp Diabetes Res 2011; 2011: 592408
  • 23 Patti ME. Intergenerational programming of metabolic disease: evidence from human populations and experimental animal models. Cell Mol Life Sci 2013; 70 (9) 1597-1608
  • 24 Ozanne SE. Metabolic programming in animals. Br Med Bull 2001; 60: 143-152
  • 25 Langley-Evans SC, Gardner DS, Jackson AA. Maternal protein restriction influences the programming of the rat hypothalamic–pituitary–adrenal axis. J Nutr 1996; 126 (6) 1578-1585
  • 26 Nwagwu MO, Cook A, Langley-Evans SC. Evidence of progressive deterioration of renal function in rats exposed to a maternal low-protein diet in utero. Br J Nutr 2000; 83 (1) 79-85
  • 27 Hales CN, Barker DJ. The thrifty phenotype hypothesis. Br Med Bull 2001; 60: 5-20
  • 28 Desai M, Beall M, Ross MG. Developmental origins of obesity: programmed adipogenesis. Curr Diab Rep 2013; 13 (1) 27-33
  • 29 Shepherd PR, Crowther NJ, Desai M, Hales CN, Ozanne SE. Altered adipocyte properties in the offspring of protein malnourished rats. Br J Nutr 1997; 78 (1) 121-129
  • 30 Bieswal F, Ahn MT, Reusens B , et al. The importance of catch-up growth after early malnutrition for the programming of obesity in male rat. Obesity (Silver Spring) 2006; 14 (8) 1330-1343
  • 31 Guan H, Arany E, van Beek JP , et al. Adipose tissue gene expression profiling reveals distinct molecular pathways that define visceral adiposity in offspring of maternal protein-restricted rats. Am J Physiol Endocrinol Metab 2005; 288 (4) E663-E673
  • 32 Palmer AC. Nutritionally mediated programming of the developing immune system. Adv Nutr 2011; 2 (5) 377-395
  • 33 Triunfo S, Lanzone A. Impact of overweight and obesity on obstetric outcomes. J Endocrinol Invest 2014; 37 (4) 323-329
  • 34 Chen M, McNiff C, Madan J, Goodman E, Davis JM, Dammann O. Maternal obesity and neonatal Apgar scores. J Matern Fetal Neonatal Med 2010; 23 (1) 89-95
  • 35 Boney CM, Verma A, Tucker R, Vohr BR. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics 2005; 115 (3) e290-e296
  • 36 Gluckman PD, Hanson MA, Morton SM, Pinal CS. Life-long echoes – a critical analysis of the developmental origins of adult disease model. Biol Neonate 2005; 87 (2) 127-139
  • 37 Harding JE. The nutritional basis of the fetal origins of adult disease. Int J Epidemiol 2001; 30 (1) 15-23
  • 38 Oken E, Rifas-Shiman SL, Field AE, Frazier AL, Gillman MW. Maternal gestational weight gain and offspring weight in adolescence. Obstet Gynecol 2008; 112 (5) 999-1006
  • 39 Djelantik AA, Kunst AE, van der Wal MF, Smit HA, Vrijkotte TG. Contribution of overweight and obesity to the occurrence of adverse pregnancy outcomes in a multi-ethnic cohort: population attributive fractions for Amsterdam. BJOG 2012; 119 (3) 283-290
  • 40 Surkan PJ, Hsieh CC, Johansson AL, Dickman PW, Cnattingius S. Reasons for increasing trends in large for gestational age births. Obstet Gynecol 2004; 104 (4) 720-726
  • 41 Simmons R. Epigenetics and maternal nutrition: nature v. nurture. Proc Nutr Soc 2011; 70 (1) 73-81
  • 42 Oken E. Maternal and child obesity: the causal link. Obstet Gynecol Clin North Am 2009; 36 (2) 361-377 , ix–x ix–x.
  • 43 Chu SY, Callaghan WM, Kim SY , et al. Maternal obesity and risk of gestational diabetes mellitus. Diabetes Care 2007; 30 (8) 2070-2076
  • 44 Deierlein AL, Siega-Riz AM, Chantala K, Herring AH. The association between maternal glucose concentration and child BMI at age 3 years. Diabetes Care 2011; 34 (2) 480-484
  • 45 Lawlor DA, Lichtenstein P, Långström N. Association of maternal diabetes mellitus in pregnancy with offspring adiposity into early adulthood: sibling study in a prospective cohort of 280,866 men from 248,293 families. Circulation 2011; 123 (3) 258-265
  • 46 Buonocore G, Groenendaal F. Anti-oxidant strategies. Semin Fetal Neonatal Med 2007; 12 (4) 287-295
  • 47 Leal CA, Schetinger MR, Leal DB , et al. Oxidative stress and antioxidant defenses in pregnant women. Redox Rep 2011; 16 (6) 230-236
  • 48 Mueller A, Koebnick C, Binder H , et al. Placental defence is considered sufficient to control lipid peroxidation in pregnancy. Med Hypotheses 2005; 64 (3) 553-557
  • 49 Burton GJ, Jauniaux E. Placental oxidative stress: from miscarriage to preeclampsia. J Soc Gynecol Investig 2004; 11 (6) 342-352
  • 50 Lee J, Giordano S, Zhang J. Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem J 2012; 441 (2) 523-540
  • 51 Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009; 417 (1) 1-13
  • 52 Ferreira DJ, da Silva Pedroza AA, Braz GR , et al. Mitochondrial bioenergetics and oxidative status disruption in brainstem of weaned rats: immediate response to maternal protein restriction. Brain Res 2016; 1642: 553-561
  • 53 Mikhed Y, Daiber A, Steven S. Mitochondrial oxidative stress, mitochondrial DNA damage and their role in age-related vascular dysfunction. Int J Mol Sci 2015; 16 (7) 15918-15953
  • 54 Callinan PA, Feinberg AP. The emerging science of epigenomics. Hum Mol Genet 2006; 15 (Spec No 1) R95-R101
  • 55 Reddy PH. Amyloid β, mitochondrial structural and functional dynamics in Alzheimer's disease. Exp Neurol 2009; 218 (2) 286-292
  • 56 Canugovi C, Shamanna RA, Croteau DL, Bohr VA. Base excision DNA repair levels in mitochondrial lysates of Alzheimer's disease. Neurobiol Aging 2014; 35 (6) 1293-1300
  • 57 Dikalov SI, Nazarewicz RR, Bikineyeva A , et al. Nox2-induced production of mitochondrial superoxide in angiotensin II-mediated endothelial oxidative stress and hypertension. Antioxid Redox Signal 2014; 20 (2) 281-294
  • 58 Doughan AK, Harrison DG, Dikalov SI. Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ Res 2008; 102 (4) 488-496
  • 59 Nazarewicz RR, Dikalova AE, Bikineyeva A, Dikalov SI. Nox2 as a potential target of mitochondrial superoxide and its role in endothelial oxidative stress. Am J Physiol Heart Circ Physiol 2013; 305 (8) H1131-H1140
  • 60 Souza-Pinto NC, Croteau DL, Hudson EK, Hansford RG, Bohr VA. Age-associated increase in 8-oxo-deoxyguanosine glycosylase/AP lyase activity in rat mitochondria. Nucleic Acids Res 1999; 27 (8) 1935-1942
  • 61 Sevini F, Giuliani C, Vianello D , et al. mtDNA mutations in human aging and longevity: controversies and new perspectives opened by high-throughput technologies. Exp Gerontol 2014; 56: 234-244
  • 62 Iorio MV, Piovan C, Croce CM. Interplay between microRNAs and the epigenetic machinery: an intricate network. Biochim Biophys Acta 2010; 1799 (10–12) 694-701
  • 63 Agarwal A, Gupta S, Sekhon L, Shah R. Redox considerations in female reproductive function and assisted reproduction: from molecular mechanisms to health implications. Antioxid Redox Signal 2008; 10 (8) 1375-1403
  • 64 Moore VM, Davies MJ. Diet during pregnancy, neonatal outcomes and later health. Reprod Fertil Dev 2005; 17 (3) 341-348
  • 65 Hawk SN, Lanoue L, Keen CL, Kwik-Uribe CL, Rucker RB, Uriu-Adams JY. Copper-deficient rat embryos are characterized by low superoxide dismutase activity and elevated superoxide anions. Biol Reprod 2003; 68 (3) 896-903
  • 66 Lenzen S. Oxidative stress: the vulnerable beta-cell. Biochem Soc Trans 2008; 36 (Pt 3) 343-347
  • 67 Baydas G, Karatas F, Gursu MF , et al. Antioxidant vitamin levels in term and preterm infants and their relation to maternal vitamin status. Arch Med Res 2002; 33 (3) 276-280
  • 68 Jenkins C, Wilson R, Roberts J, Miller H, McKillop JH, Walker JJ. Antioxidants: their role in pregnancy and miscarriage. Antioxid Redox Signal 2000; 2 (3) 623-628
  • 69 Saben J, Lindsey F, Zhong Y , et al. Maternal obesity is associated with a lipotoxic placental environment. Placenta 2014; 35 (3) 171-177
  • 70 Lesseur C, Armstrong DA, Paquette AG, Koestler DC, Padbury JF, Marsit CJ. Tissue-specific Leptin promoter DNA methylation is associated with maternal and infant perinatal factors. Mol Cell Endocrinol 2013; 381 (1–2) 160-167
  • 71 Malti N, Merzouk H, Merzouk SA , et al. Oxidative stress and maternal obesity: feto-placental unit interaction. Placenta 2014; 35 (6) 411-416
  • 72 Ferretti G, Cester AM, Bacchetti T , et al. Leptin and paraoxonase activity in cord blood from obese mothers. J Matern Fetal Neonatal Med 2014; 27 (13) 1353-1356
  • 73 Perrone S, Negro S, Tataranno ML, Buonocore G. Oxidative stress and antioxidant strategies in newborns. J Matern Fetal Neonatal Med 2010; 23 (Suppl. 03) 63-65
  • 74 Zhang X, Strakovsky R, Zhou D, Zhang Y, Pan YX. A maternal high-fat diet represses the expression of antioxidant defense genes and induces the cellular senescence pathway in the liver of male offspring rats. J Nutr 2011; 141 (7) 1254-1259
  • 75 Kinalski M, Sledziewski A, Telejko B , et al. Lipid peroxidation, antioxidant defence and acid–base status in cord blood at birth: the influence of diabetes. Horm Metab Res 2001; 33 (4) 227-231
  • 76 Ornoy A, Zaken V, Kohen R. Role of reactive oxygen species (ROS) in the diabetes-induced anomalies in rat embryos in vitro: reduction in antioxidant enzymes and low-molecular-weight antioxidants (LMWA) may be the causative factor for increased anomalies. Teratology 1999; 60 (6) 376-386
  • 77 Kharb S. Lipid peroxidation in pregnancy with preeclampsia and diabetes. Gynecol Obstet Invest 2000; 50 (2) 113-116
  • 78 Kamath U, Rao G, Raghothama C, Rai L, Rao P. Erythrocyte indicators of oxidative stress in gestational diabetes. Acta Paediatr 1998; 87 (6) 676-679
  • 79 Coughlan MT, Vervaart PP, Permezel M, Georgiou HM, Rice GE. Altered placental oxidative stress status in gestational diabetes mellitus. Placenta 2004; 25 (1) 78-84
  • 80 Baynes JW. Role of oxidative stress in development of complications in diabetes. Diabetes 1991; 40 (4) 405-412
  • 81 West IC. Radicals and oxidative stress in diabetes. Diabet Med 2000; 17 (3) 171-180
  • 82 Hauguel-de Mouzon S, Shafrir E. Carbohydrate and fat metabolism and related hormonal regulation in normal and diabetic placenta. Placenta 2001; 22 (7) 619-627
  • 83 Barker DJ. In utero programming of chronic disease. Clin Sci (Lond) 1998; 95 (2) 115-128