Skip to main content

Ontogeny of Antioxidant Systems

  • Chapter
  • First Online:
Perinatal and Prenatal Disorders

Abstract

Changes in the redox conditions of the biosphere have shaped the evolution of biological adaptations that permit successful energy capture and transfer by life forms. These include the systems that can scavenge molecular oxygen and nitrogen oxides. Mammalian development partly recapitulates this sequence as the zygote implants and undergoes early development in a low oxygen environment, ultimately developing a vascular supply that supports gas exchange and metabolism, as well as the enzymatic antioxidant/antinitrosant systems required to handle the burden. These systems differ among the organ systems, and their function and expression are dependent on the stage of development and the particular metabolic demands, as well as the exposure to redox stress.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Van Der Giezen M, Lenton TM. The rise of oxygen and complex life. J Eukaryot Microbiol. 2012;59(2):111–3.

    Article  Google Scholar 

  2. Dennery PA. Role of redox in fetal development and neonatal diseases. Antioxid Redox Signal. 2004;6(1):147–53.

    Article  CAS  PubMed  Google Scholar 

  3. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev. 2007;87(1):315–424.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Derakhshan B, Hao G, Gross SS. Balancing reactivity against selectivity: the evolution of protein S-nitrosylation as an effector of cell signaling by nitric oxide. Cardiovasc Res. 2007;75(2):210–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Angelo M, et al. Interactions of NO with hemoglobin: from microbes to man. Methods Enzymol. 2008;436:131–68.

    Article  CAS  PubMed  Google Scholar 

  6. Forrester MT, Foster MW. Protection from nitrosative stress: a central role for microbial flavohemoglobin. Free Radic Biol Med. 2012;52(9):1620–33.

    Article  CAS  PubMed  Google Scholar 

  7. Burton GJ, Hempstock J, Jauniaux E. Oxygen, early embryonic metabolism and free radical-mediated embryopathies. Reprod Biomed Online. 2003;6(1):84–96.

    Article  PubMed  Google Scholar 

  8. Frank L, Groseclose EE. Preparation for birth into an O2-rich environment: the antioxidant enzymes in the developing rabbit lung. Pediatr Res. 1984;18(3):240–4.

    Article  CAS  PubMed  Google Scholar 

  9. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol. 1996;271(5 Pt 1):C1424–37.

    CAS  PubMed  Google Scholar 

  10. Bonaventura J, Gow A. NO and superoxide: opposite ends of the seesaw in cardiac contractility. Proc Natl Acad Sci U S A. 2004;101(47):16403–4.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Foster MW, Hess DT, Stamler JS. Protein S-nitrosylation in health and disease: a current perspective. Trends Mol Med. 2009;15(9):391–404.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Benhar M, Forrester MT, Stamler JS. Protein denitrosylation: enzymatic mechanisms and cellular functions. Nat Rev Mol Cell Biol. 2009;10(10):721–32.

    CAS  PubMed  Google Scholar 

  13. Anand P, Stamler JS. Enzymatic mechanisms regulating protein S-nitrosylation: implications in health and disease. J Mol Med (Berl). 2012;90(3):233–44.

    Article  CAS  Google Scholar 

  14. Wu C, et al. Redox regulatory mechanism of transnitrosylation by thioredoxin. Mol Cell Proteomics. 2010;9(10):2262–75.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Bendix I, et al. Hyperoxia changes the balance of the thioredoxin/peroxiredoxin system in the neonatal rat brain. Brain Res. 2012;1484:68–75.

    Article  CAS  PubMed  Google Scholar 

  16. Perez-Jimenez R, et al. Diversity of chemical mechanisms in thioredoxin catalysis revealed by single-molecule force spectroscopy. Nat Struct Mol Biol. 2009;16(8):890–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Sengupta R, Holmgren A. Thioredoxin and thioredoxin reductase in relation to reversible S-Nitrosylation. Antioxid Redox Signal. 2013;18(3):259–69.

    Article  CAS  PubMed  Google Scholar 

  18. Carter AM. Animal models of human placentation – a review. Placenta. 2007;28(Suppl A):S41–7.

    Article  PubMed  Google Scholar 

  19. Cox B, et al. Comparative systems biology of human and mouse as a tool to guide the modeling of human placental pathology. Mol Syst Biol. 2009;5:279.

    Article  PubMed Central  PubMed  Google Scholar 

  20. Davis JM, Auten RL. Maturation of the antioxidant system and the effects on preterm birth. Semin Fetal Neonatal Med. 2010;15(4):191–5.

    Article  PubMed  Google Scholar 

  21. Qanungo S, Mukherjea M. Ontogenic profile of some antioxidants and lipid peroxidation in human placental and fetal tissues. Mol Cell Biochem. 2000;215(1–2):11–9.

    Article  CAS  PubMed  Google Scholar 

  22. Boggess KA, et al. Differential localization of placental extracellular superoxide dismutase as pregnancy progresses. Am J Obstet Gynecol. 2000;183(1):199–205.

    CAS  PubMed  Google Scholar 

  23. Kim MR, et al. Expression profiles of extracellular superoxide dismutase during mouse organogenesis. Gene Expr Patterns. 2011;11(3–4):207–15.

    Article  CAS  PubMed  Google Scholar 

  24. Garrel C, Fowler PA, Al-Gubory KH. Developmental changes in antioxidant enzymatic defences against oxidative stress in sheep placentomes. J Endocrinol. 2010;205(1):107–16.

    Article  CAS  PubMed  Google Scholar 

  25. Carter AM. Evolution of factors affecting placental oxygen transfer. Placenta. 2009;30(Suppl A):S19–25.

    Article  PubMed  Google Scholar 

  26. Myatt L. Review: Reactive oxygen and nitrogen species and functional adaptation of the placenta. Placenta. 2010;31(Suppl):S66–9.

    Article  PubMed Central  PubMed  Google Scholar 

  27. Al-Sabbagh M, et al. NADPH oxidase-derived reactive oxygen species mediate decidualization of human endometrial stromal cells in response to cyclic AMP signaling. Endocrinology. 2011;152(2):730–40.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Bevilacqua E, et al. NADPH oxidase as an important source of reactive oxygen species at the mouse maternal-fetal interface: putative biological roles. Reprod Biomed Online. 2012;25(1):31–43.

    Article  CAS  PubMed  Google Scholar 

  29. Vieira-Filho LD, et al. Placental oxidative stress in malnourished rats and changes in kidney proximal tubule sodium ATPases in offspring. Clin Exp Pharmacol Physiol. 2009;36(12):1157–63.

    Article  CAS  PubMed  Google Scholar 

  30. Ayling LJ, et al. Dimethylarginine dimethylaminohydrolase (DDAH) regulates trophoblast invasion and motility through effects on nitric oxide. Hum Reprod. 2006;21(10):2530–7.

    Article  CAS  PubMed  Google Scholar 

  31. Teichert AM, et al. Endothelial nitric oxide synthase gene expression during murine embryogenesis: commencement of expression in the embryo occurs with the establishment of a unidirectional circulatory system. Circ Res. 2008;103(1):24–33.

    Article  CAS  PubMed  Google Scholar 

  32. Krause BJ, Hanson MA, Casanello P. Role of nitric oxide in placental vascular development and function. Placenta. 2011;32(11):797–805.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Kossenjans W, et al. Role of peroxynitrite in altered fetal-placental vascular reactivity in diabetes or preeclampsia. Am J Physiol Heart Circ Physiol. 2000;278(4):H1311–9.

    CAS  PubMed  Google Scholar 

  34. Webster RP, Roberts VH, Myatt L. Protein nitration in placenta – functional significance. Placenta. 2008;29(12):985–94.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Zhang HH, Wang YP, Chen DB. Analysis of nitroso-proteomes in normotensive and severe preeclamptic human placentas. Biol Reprod. 2011;84(5):966–75.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Song J, et al. The expression of thioredoxin-1 in preterm delivery placenta. Redox Rep. 2012;17(5):187–93.

    Article  CAS  PubMed  Google Scholar 

  37. Umekawa T, et al. Overexpression of thioredoxin-1 reduces oxidative stress in the placenta of transgenic mice and promotes fetal growth via glucose metabolism. Endocrinology. 2008;149(8):3980–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Raunig JM, et al. Placental inflammation and oxidative stress in the mouse model of assisted reproduction. Placenta. 2011;32(11):852–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Nelson KB, et al. Neonatal cytokines and coagulation factors in children with cerebral palsy. Ann Neurol. 1998;44(4):665–75.

    Article  CAS  PubMed  Google Scholar 

  40. Buonocore G, Perrone S, Tataranno ML. Oxygen toxicity: chemistry and biology of reactive oxygen species. Semin Fetal Neonatal Med. 2010;15(4):186–90.

    Article  PubMed  Google Scholar 

  41. Mishra OP, Delivoria-Papadopoulos M. Cellular mechanisms of hypoxic injury in the developing brain. Brain Res Bull. 1999;48(3):233–8.

    Article  CAS  PubMed  Google Scholar 

  42. Volpe JJ, et al. The developing oligodendrocyte: key cellular target in brain injury in the premature infant. Int J Dev Neurosci. 2011;29(4):423–40.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Folkerth RD, et al. Developmental lag in superoxide dismutases relative to other antioxidant enzymes in premyelinated human telencephalic white matter. J Neuropathol Exp Neurol. 2004;63(9):990–9.

    CAS  PubMed  Google Scholar 

  44. Baud O, et al. Developmental up-regulation of MnSOD in rat oligodendrocytes confers protection against oxidative injury. Eur J Neurosci. 2004;20(1):29–40.

    Article  PubMed  Google Scholar 

  45. Khan JY, Black SM. Developmental changes in murine brain antioxidant enzymes. Pediatr Res. 2003;54(1):77–82.

    Article  CAS  PubMed  Google Scholar 

  46. Xu L, Sapolsky RM, Giffard RG. Differential sensitivity of murine astrocytes and neurons from different brain regions to injury. Exp Neurol. 2001;169(2):416–24.

    Article  CAS  PubMed  Google Scholar 

  47. Takikawa M, et al. Temporospatial relationship between the expressions of superoxide dismutase and nitric oxide synthase in the developing human brain: immunohistochemical and immunoblotting analyses. Acta Neuropathol. 2001;102(6):572–80.

    Article  CAS  PubMed  Google Scholar 

  48. Lipton AJ, et al. S-nitrosothiols signal the ventilatory response to hypoxia. Nature. 2001;413(6852):171–4.

    Article  CAS  PubMed  Google Scholar 

  49. Marshall HE, Stamler JS. Inhibition of NF-kappa B by S-nitrosylation. Biochemistry. 2001;40(6):1688–93.

    Article  CAS  PubMed  Google Scholar 

  50. Sheng H, et al. Pharmacologically augmented S-nitrosylated hemoglobin improves recovery from murine subarachnoid hemorrhage. Stroke. 2011;42(2):471–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Joksovic PM, et al. Functional regulation of T-type calcium channels by s-nitrosothiols in the rat thalamus. J Neurophysiol. 2007;97(4):2712–21.

    Article  CAS  PubMed  Google Scholar 

  52. Mannick JB, et al. Fas-induced caspase denitrosylation. Science. 1999;284(5414):651–4.

    Article  CAS  PubMed  Google Scholar 

  53. Forrester MT, et al. Thioredoxin-interacting protein (Txnip) is a feedback regulator of S-nitrosylation. J Biol Chem. 2009;284(52):36160–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Foster MW, McMahon TJ, Stamler JS. S-nitrosylation in health and disease. Trends Mol Med. 2003;9(4):160–8.

    Article  CAS  PubMed  Google Scholar 

  55. Khan M, et al. The inhibitory effect of S-nitrosoglutathione on blood-brain barrier disruption and peroxynitrite formation in a rat model of experimental stroke. J Neurochem. 2012;123 Suppl 2:86–97.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  56. Palmer LA, et al. Ventilatory responses during and following exposure to a hypoxic challenge in conscious mice deficient or null in S-nitrosoglutathione reductase. Respir Physiol Neurobiol. 2013;185(3):571–81.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Westerlund M, et al. Tissue- and species-specific expression patterns of class I, III, and IV Adh and Aldh 1 mRNAs in rodent embryos. Cell Tissue Res. 2005;322(2):227–36.

    Article  CAS  PubMed  Google Scholar 

  58. Castillo-Melendez M, Chow JA, Walker DW. Lipid peroxidation, caspase-3 immunoreactivity, and pyknosis in late-gestation fetal sheep brain after umbilical cord occlusion. Pediatr Res. 2004;55(5):864–71.

    Article  CAS  PubMed  Google Scholar 

  59. Miller SL, et al. Melatonin provides neuroprotection in the late-gestation fetal sheep brain in response to umbilical cord occlusion. Dev Neurosci. 2005;27(2–4):200–10.

    Article  CAS  PubMed  Google Scholar 

  60. Mishra OP, Delivoria-Papadopoulos M. Mechanism of tyrosine phosphorylation of procaspase-9 and Apaf-1 in cytosolic fractions of the cerebral cortex of newborn piglets during hypoxia. Neurosci Lett. 2010;480(1):35–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  61. Drever N, et al. The expression of antioxidant enzymes in a mouse model of fetal alcohol syndrome. Am J Obstet Gynecol. 2012;206(4):358.e19-22.

    Article  PubMed  Google Scholar 

  62. Patten AR, Brocardo PS, Christie BR. Omega-3 supplementation can restore glutathione levels and prevent oxidative damage caused by prenatal ethanol exposure. J Nutr Biochem. 2013;24(5):760–9.

    Article  CAS  PubMed  Google Scholar 

  63. Frank L, Sosenko IR. Prenatal development of lung antioxidant enzymes in four species. J Pediatr. 1987;110(1):106–10.

    Article  CAS  PubMed  Google Scholar 

  64. Frank L, Sosenko IR. Development of lung antioxidant enzyme system in late gestation: possible implications for the prematurely born infant. J Pediatr. 1987;110(1):9–14.

    Article  CAS  PubMed  Google Scholar 

  65. Sosenko IR, Frank L. Guinea pig lung development: antioxidant enzymes and premature survival in high O2. Am J Physiol. 1987;252(4 Pt 2):R693–8.

    CAS  PubMed  Google Scholar 

  66. Yuan HT, Bingle CD, Kelly FJ. Differential patterns of antioxidant enzyme mRNA expression in guinea pig lung and liver during development. Biochim Biophys Acta. 1996;1305(3):163–71.

    Article  PubMed  Google Scholar 

  67. Asayama K, et al. Immunohistochemical study on perinatal development of rat superoxide dismutases in lungs and kidneys. Pediatr Res. 1991;29(5):487–91.

    Article  CAS  PubMed  Google Scholar 

  68. Sharma S, et al. Lung antioxidant enzymes are regulated by development and increased pulmonary blood flow. Am J Physiol Lung Cell Mol Physiol. 2007;293(4):L960–71.

    Article  CAS  PubMed  Google Scholar 

  69. Nozik-Grayck E, et al. Secretion of extracellular superoxide dismutase in neonatal lungs. Am J Physiol Lung Cell Mol Physiol. 2000;279(5):L977–84.

    CAS  PubMed  Google Scholar 

  70. Mamo LB, et al. Discordant extracellular superoxide dismutase expression and activity in neonatal hyperoxic lung. Am J Respir Crit Care Med. 2004;170(3):313–8.

    Article  PubMed  Google Scholar 

  71. Auten RL, White CW. Oxidative and nitrosative stress and bronchopulmonary dysplasia. In: Abman SH, editor. Bronchopulmonary dysplasia. Philadelphia: Informa Health Care; 2009. p. 499.

    Google Scholar 

  72. Chen Y, Whitney PL, Frank L. Negative regulation of antioxidant enzyme gene expression in the developing fetal rat lung by prenatal hormonal treatments. Pediatr Res. 1993;33(2):171–6.

    Article  CAS  PubMed  Google Scholar 

  73. Buckley BJ, Li S, Whorton AR. Keap1 modification and nuclear accumulation in response to S-nitrosocysteine. Free Radic Biol Med. 2008;44(4):692–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  74. Cho HY, Reddy SP, Kleeberger SR. Nrf2 defends the lung from oxidative stress. Antioxid Redox Signal. 2006;8(1–2):76–87.

    Article  CAS  PubMed  Google Scholar 

  75. Cho HY, et al. Role of NRF2 in protection against hyperoxic lung injury in mice. Am J Respir Cell Mol Biol. 2002;26(2):175–82.

    Article  CAS  PubMed  Google Scholar 

  76. McGrath-Morrow S, et al. Nrf2 increases survival and attenuates alveolar growth inhibition in neonatal mice exposed to hyperoxia. Am J Physiol Lung Cell Mol Physiol. 2009;296(4):L565–73.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  77. Kadkodayan, R., et al. Developmental expression and interaction of Nrf2 with ECSOD in developing lung. In: American Thoracic Society International Conference. San Diego: American Thoracic Society; 2009.

    Google Scholar 

  78. Saugstad OD, Rognum TO. High postmortem levels of hypoxanthine in the vitreous humor of premature babies with respiratory distress syndrome. Pediatrics. 1988;81(3):395–8.

    CAS  PubMed  Google Scholar 

  79. Jain A, et al. Glutathione metabolism in newborns: evidence for glutathione deficiency in plasma, bronchoalveolar lavage fluid, and lymphocytes in prematures. Pediatr Pulmonol. 1995;20(3):160–6.

    Article  CAS  PubMed  Google Scholar 

  80. Dobashi K, et al. Immunohistochemical study of copper-zinc and manganese superoxide dismutases in the lungs of human fetuses and newborn infants: developmental profile and alterations in hyaline membrane disease and bronchopulmonary dysplasia. Virchows Arch A Pathol Anat Histopathol. 1993;423(3):177–84.

    Article  CAS  PubMed  Google Scholar 

  81. Asikainen TM, et al. Expression and developmental profile of antioxidant enzymes in human lung and liver. Am J Respir Cell Mol Biol. 1998;19(6):942–9.

    Article  CAS  PubMed  Google Scholar 

  82. Kaarteenaho-Wiik R, Kinnula VL. Distribution of antioxidant enzymes in developing human lung, respiratory distress syndrome, and bronchopulmonary dysplasia. J Histochem Cytochem. 2004;52(9):1231–40.

    Article  CAS  PubMed  Google Scholar 

  83. Meng X, et al. Genetic and epigenetic down-regulation of microRNA-212 promotes colorectal tumor metastasis via dysregulation of MnSOD. Gastroenterology. 2013;145(2):426–36.e1-6.

    Article  CAS  PubMed  Google Scholar 

  84. Zhong Q, Kowluru RA. Epigenetic modification of Sod2 in the development of diabetic retinopathy and in the metabolic memory: role of histone methylation. Invest Ophthalmol Vis Sci. 2013;54(1):244–50.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  85. Bryan HK, et al. The Nrf2 cell defence pathway: Keap1-dependent and -independent mechanisms of regulation. Biochem Pharmacol. 2013;85(6):705–17.

    Article  CAS  PubMed  Google Scholar 

  86. Waly MI, et al. Prenatal and postnatal epigenetic programming: implications for GI, immune, and neuronal function in autism. Autism Res Treat. 2012;2012:190930.

    PubMed Central  PubMed  Google Scholar 

  87. Rahman I, Biswas SK, Kirkham PA. Regulation of inflammation and redox signaling by dietary polyphenols. Biochem Pharmacol. 2006;72(11):1439–52.

    Article  CAS  PubMed  Google Scholar 

  88. Kim HS, et al. Rat lung peroxiredoxins I and II are differentially regulated during development and by hyperoxia. Am J Physiol Lung Cell Mol Physiol. 2001;280(6):L1212–7.

    CAS  PubMed  Google Scholar 

  89. Das KC, et al. Induction of peroxiredoxin gene expression by oxygen in lungs of newborn primates. Am J Respir Cell Mol Biol. 2001;25(2):226–32.

    Article  CAS  PubMed  Google Scholar 

  90. Chen Y, et al. Thioredoxin protects fetal type II epithelial cells from hyperoxia-induced injury. Pediatr Pulmonol. 2010;45(12):1192–200.

    Article  PubMed  Google Scholar 

  91. Que LG, et al. Protection from experimental asthma by an endogenous bronchodilator. Science. 2005;308(5728):1618–21.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  92. Westerlund M, et al. High and complementary expression patterns of alcohol and aldehyde dehydrogenases in the gastrointestinal tract: implications for Parkinson’s disease. FEBS J. 2007;274(5):1212–23.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard L. Auten Jr. M.D. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Auten, R.L. (2014). Ontogeny of Antioxidant Systems. In: Dennery, P., Buonocore, G., Saugstad, O. (eds) Perinatal and Prenatal Disorders. Oxidative Stress in Applied Basic Research and Clinical Practice. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-1405-0_17

Download citation

Publish with us

Policies and ethics