Antioxidant therapies: A potential role in perinatal medicine

Neuroendocrinology

Volumn 96, Issue 1, 2012, Pages 13-23

  Miller, S L ^a,b   Wallace, E M ^a,b   Walker, D W ^a,b  

^a HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Lipoic acid; Allopurinol; Antioxidant; Fetus; Melatonin; Neonate; Neuroprotection; Vitamin C; Vitamin E

Indexed keywords

ALLOPURINOL; ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; FREE RADICAL; HYDROGEN PEROXIDE; HYDROXYL RADICAL; MELATONIN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; THIOCTIC ACID;

ANTIOXIDANT ACTIVITY; BIOSYNTHESIS; BRAIN DAMAGE; BRAIN PROTECTION; DRUG EFFICACY; DRUG MECHANISM; DRUG SAFETY; FETUS DEVELOPMENT; FETUS HYPOXIA; HUMAN; INFLAMMATION; LIPID PEROXIDATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PERINATAL ASPHYXIA; PERINATAL PERIOD; PREECLAMPSIA; PREGNANCY; PRIORITY JOURNAL; REVIEW; TREATMENT OUTCOME; UNSPECIFIED SIDE EFFECT;

ANIMALS; ANTIOXIDANTS; BRAIN; FEMALE; FREE RADICALS; HUMANS; INFLAMMATION; OXIDATIVE STRESS; PREGNANCY; PREGNANCY COMPLICATIONS;

EID: 84864886698     PISSN: 00283835     EISSN: 14230194     Source Type: Journal    
DOI: 10.1159/000336378     Document Type: Review

References (94)

1. Morris JM, Gopaul NK, Endresen MJ, Knight M, Linton EA, Dhir S, Anggard EE, Redman CW: Circulating markers of oxida-tive stress are raised in normal pregnancy and pre-eclampsia. Br J Obstet Gynaecol 1998; 105:1195-1199.
2. Little RE, Gladen BC: Levels of lipid peroxides in uncomplicated pregnancy: a review of the literature. Reprod Toxicol 1999; 13:347-352.
3. Myatt L, Cui X: Oxidative stress in the placenta. Histochem Cell Biol 2004; 122:369-382.
4. Walsh SW, Wang Y: Secretion of lipid peroxides by the human placenta. Am J Obstet Gy-necol 1993; 169:1462-1576.
5. Buonocore G, Perrone S, Tataranno ML: Oxygen toxicity: chemistry and biology of reactive oxygen species. Semin Fetal Neonatal Med 2010; 15: 186-190.
6. Lewen A, Matz P, Chan PH: Free radical pathways in CNS injury. J Neurotrauma 2000; 17:871-890.
7. Hensley K, Robinson KA, Gabbita SP, Sals-man S, Floyd RA: Reactive oxygen species, cell signaling, and cell injury. Free Radic Biol Med 2000; 28:1456-1462.
8. Redman CW, Sargent IL: Pre-eclampsia, the placenta and the maternal systemic inflammatory respons-a review. Placenta 2003; 24(suppl A):S21-S27.
9. Floyd RA: Role of oxygen free radicals in car-cinogenesis and brain ischemia. Faseb J 1990; 4: 2587-2597.
10. Buonocore G, Perrone S, Tataranno ML: Oxygen toxicity: chemistry and biology of reactive oxygen species. Semin Fetal Neonatal Med 2010;15: 186-190.
11. Delivoria-Papadopoulos M, Mishra OP: Mechanisms of cerebral injury in perinatal asphyxia and strategies for prevention. J Pe-diatr 1998; 132:S30-S34.
12. Rodrigo J, Fernandez AP, Serrano J, Peinado MA, Martinez A: The role of free radicals in cerebral hypoxia and ischemia. Free Radic Biol Med 2005; 39: 26-50.
13. Abramov AY, Scorziello A, Duchen MR: Three distinct mechanisms generate oxygen free radicals in neurons and contribute to cell death during anoxia and reoxygenation. J Neurosci 2007; 27:1129-1138.
14. Traystman RJ, Kirsch JR, Koehler RC: Oxygen radical mechanisms of brain injury following ischemia and reperfusion. J Appl Physiol 1991; 71: 1185-1195.
15. Sugawara T, Chan PH: Reactive oxygen radicals and pathogenesis of neuronal death after cerebral ischemia. Antioxid Redox Signal 2003; 5: 597-607.
16. Blomgren K, Hagberg H: Free radicals, mitochondria, and hypoxia-ischemia in the developing brain. Free Radic Biol Med 2006; 40: 388-397.
17. Vannucci RC, Perlman JM: Interventions for perinatal hypoxic-ischemic encephalopathy. Pediatrics 1997; 100:1004-1014.
18. Myatt L: Placental adaptive responses and feta l programming. J Physiol 2006; 572: 25-30.
19. Mishra OP, Delivoria-Papadopoulos M: Cellular mechanisms of hypoxic brain injury in the developing brain. Brain Res Bull 1999; 48: 233-238.
20. Back SA: Perinatal white matter injury: the changing spectrum of pathology and emerging insights into pathogenetic mechanisms. Ment Retard Dev Disabil Res Rev 2006; 12: 129-140.
21. Gitto E, Pellegrino S, Gitto P, Barberi I, Re-iter RJ: Oxidative stress of the newborn in the pre-and postnatal period and the clinical utility of melatonin. J Pineal Res 2009; 46: 128-139.
22. Saugstad OD: Mechanisms of tissue injury by oxygen radicals: implications for neonatal disease. Acta Paediatr 1996; 85:1-4.
23. Volpe JJ: Perinatal brain injury: from patho-genesis to neuroprotection. Ment Retard Dev Disabil Res Rev 2001; 7: 56-64.
24. Miller SL, Yan EB, Castillo-Melendez M, Jenkin G, Walker DW: Melatonin provides neuroprotection in the late-gestation fetal sheep brain in response to umbilical cord occlusion. Dev Neurosci 2005; 27:200-210.
25. Castillo-Melendez M, Chow JA, Walker DW: Lipid peroxidation, caspase-3 immunoreac-tivity, and pyknosis in late-gestation fetal sheep brain after umbilical cord occlusion. Pediatr Res 2004; 55:864-871.
26. Bagenholm R, Nilsson UA, Kjellmer I: Formation of free radicals in hypoxic ischemic brain damage in the neonata l rat, assessed by an endogenous spin trap and lipid peroxida-tion. Brain Res 1997; 773: 132-138.
27. Torres L, Anderson C, Marro P, Mishra OP, Delivoria-Papadopoulos M: Cyclooxygen-ase-mediated generation of free radica ls during hypoxia in the cerebral cortex of newborn pig lets. Neurochem Res 2004; 29: 1825-1830.
28. Welin AK, Svedin P, Lapatto R, Sultan B, Hagberg H, Gressens P, Kjellmer I, Mallard C: Melatonin reduces inflammation and cell death in white matter in the mid-gestation fetal sheep following umbilical cord occlusion. Pediatr Res 2007; 61:153-158.
29. Miller SL, Chai M, Loose J, Castillo-Melen-dez M, Walker DW, Jenkin G, Wallace EM: The effects of maternal betamethasone administration on the intrauterine growth-restricted fetus. Endocrinology 2007; 148: 1288-1295.
30. Back SA, Gan X, Li Y, Rosenberg PA, Volpe JJ: Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J Neurosci 1998; 18: 6241-6253.
31. Volpe JJ, Kinney HC, Jensen FE, Rosenberg PA: The developing oligodendrocyte: key cellular target in brain injury in the premature infa nt. Int J Dev Neurosci 2011; 29: 423-440.
32. Volpe JJ: Neurobiology of periventricular leukomalacia in the premature infant. Pedi-atr Res 2001; 50:553-562.
33. Dringen R: Metabolism and functions of glu-tathione in brain. Prog Neurobiol 2000; 62: 649-671.
34. Fatemi A, Wilson MA, Johnston MV: Hy-poxic-ischemic encephalopathy in the term infant. Clin Perinatol 2009; 36:835-858, vii.
35. Perlman JM: Intervention strategies for neonatal hypoxic-ischemic cerebral injury. Clin Ther 2006; 28: 1353-1365.
36. van Bel F, Groenendaal F: Long-term phar-macologic neuroprotection after birth asphyxia: where do we stand? Neonatology 2008; 94: 203-210.
37. Li N, Karin M: Is NF-kappaB the sensor of oxidative stress? Faseb J 1999; 13: 1137-1143.
38. Hutton LC, Castillo-Melendez M, Smythe GA, Walker DW: Microglial activation, mac-rophage infiltration, and evidence of cell death in the fetal brain after uteroplacent-al administration of lipopolysaccharide in sheep in late gestation. Am J Obstet Gynecol 2008; 198: 117, e1-e11.
39. Hutton LC, Castillo-Melendez M, Walker DW: Uteroplacental inflammation results in blood brain barrier breakdown, increased activated caspase 3 and lipid peroxidation in the late gestation ovine fetal cerebellum. Dev Neurosci 2007; 29:341-354.
40. Peebles DM, Miller S, Newman JP, Scott R, Hanson MA: The effect of systemic administration of lipopolysaccharide on cerebral haemodynamics and oxygenation in the 0.65 gestation ovine fetus in utero. Bjog 2003; 110: 735-743.
41. Manuelpillai U, Ligam P, Smythe G, Wallace EM, Hirst J, Walker DW: Identification of kynurenine pathway enzyme mRNAs and metabolites in human placenta: up-regula-tion by inflammatory stimuli and with clinical infection. Am J Obstet Gynecol 2005; 192: 280-288.
42. Cindrova-Davies T, Spasic-Boskovic O, Jau-niaux E, Charnock-Jones DS, Burton GJ: Nuclear factor-kappa B, p38, and stress-activated protein kinase mitogen-activated protein kinase signaling pathways regulate proin-flammatory cytokines and apoptosis in human placental explants in response to oxida-tive stress: effects of antioxidant vitamins. Am J Pathol 2007; 170:1511-1520.
43. Dharane Nee Ligam P, Manuelpillai U, Wallace E, Walker DW: NFkappaB-dependent increase of kynurenine pathway activity in human placenta: inhibition by sulfasalazine. Placenta 2010; 31: 997-1002.
44. Lappas M, Permezel M, Georgiou HM, Rice GE: Nuclear factor kappa B regulation of proinf lammatory cytokines in human gesta-tional tissues in vitro. Biol Reprod 2002; 67: 668-673.
45. Higgins RD, Raju T, Edwards AD, Azzopardi DV, Bose CL, Clark RH, Ferriero DM, Guillet R, Gunn AJ, Hagberg H, Hirtz D, Inder TE, Jacobs SE, Jenkins D, Juul S, Laptook AR, Lucey JF, Maze M, Palmer C, Papile L, Pfister RH, Robertson NJ, Rutherford M, Shankaran S, Silverstein FS, Soll RF, Thoresen M, Walsh WF: Hypothermia and other treatment options for neonatal encephalopathy: an executive summary of the Eunice Kennedy Shriver NICHD workshop. J Pediatr 2011; 159:851-858, e1.
46. Moorhouse PC, Grootveld M, Halliwell B, Quinlan JG, Gutteridge JM: Allopurinol and oxypurinol are hydroxyl radical scavengers. FEBS Lett 1987; 213: 23-28.
47. Saugstad OD: Role of xanthine oxidase and its inhibitor in hypoxia: reoxygenation injury. Pediatrics 1996; 98:103-107.
48. Boda D, Nemeth I, Hencz P, Denes K: Effect of allopurinol treatment in premature infants with idiopathic respiratory distress syndrome. Dev Pharmacol Ther 1984; 7:357-367.
49. Russell GA, Cooke RW: Randomised controlled trial of allopurinol prophylaxis in very preterm infants. Arch Dis Child Fetal Neonatal Ed 1995; 73:F27-F31.
50. Palmer C, Towfighi J, Roberts RL, Heitjan DF: Allopurinol administered after inducing hypoxia-ischemia reduces brain injury in 7-day-old rats. Pediatr Res 1993; 33:405-411.
51. Palmer C, Vannucci RC, Towfighi J: Reduction of perinatal hypoxic-ischemic brain damage with allopurinol. Pediatr Res 1990; 27:332-336.
52. Marro PJ, Mishra OP, Delivoria-Papadopou-los M: Effect of allopurinol on brain adenosine levels during hypoxia in newborn piglets. Brain Res 2006; 1073-1074:444-450.
53. Marro PJ, Hoffman D, Schneiderman R, Mishra OP, Delivoria-Papadopoulos M: Effect of allopurinol on NMDA receptor modification following recurrent asphyxia in newborn piglets. Bra in Res 1998; 787: 71-77.
54. Rivkees SA, Wendler CC: Adverse and protective influences of adenosine on the newborn and embryo: implications for preterm white matter injury and embryo protection. Pediatr Res 2011; 69:271-278.
55. Derks JB, Oudijk MA, Torrance HL, Rade-maker CM, Benders MJ, Rosen KG, Cindro-va-Davies T, Thakor AS, Visser GH, Burton GJ, van Bel F, Giussani DA: Allopurinol reduces oxidative stress in the ovine fetal cardiovascular system after repeated episodes of ischemia-reperfusion. Pediatr Res 2010; 68: 374-380.
56. Van Bel F, Shadid M, Moison RM, Dorrepaal CA, Fontijn J, Monteiro L, Van De Bor M, Berger HM: Effect of allopurinol on postas-phyxial free radical formation, cerebral he-modynamics, and electrical brain activity. Pediat rics 1998; 101: 185-193.
57. Gunes T, Ozturk MA, Koklu E, Kose K, Gunes I: Effect of allopurinol supplementation on nitric oxide levels in asphyxiated newborns. Pediatr Neurol 2007; 36:17-24.
58. Kaandorp JJ, van Bel F, Veen S, Derks JB, Groenendaal F, Rijken M, Roze E, Venema MM, Rademaker CM, Bos AF, Benders MJ: Long-term neuroprotective effects of allopu-rinol after moderate perinatal asphyxia: follow-up of two randomised controlled trials. Arch Dis Child Fetal Neonatal Ed 2011, E-pub ahead of print.
59. Kaandorp JJ, Benders MJ, Rademaker CM, Torrance HL, Oudijk MA, de Haan TR, Bloemenkamp KW, Rijken M, van Pampus MG, Bos AF, Porath MM, Oetomo SB, Willekes C, Gavilanes AW, Wouters MG, van Elburg RM, Huisjes AJ, Bakker SC, van Meir CA, von Lindern J, Boon J, de Boer IP, Rijnders RJ, Jacobs CJ, Uiterwaal CS, Mol BW, Visser GH, van Bel F, Derks JB: Antenatal allopurinol for reduction of birth asphyxia induced brain damage (ALLO-Tri-al); a randomized double blind placebo controlled multicenter study. BMC Pregnancy Childbirth 2010; 10:8.
60. Torrance HL, Benders MJ, Derks JB, Rade-maker CM, Bos AF, Van Den Berg P, Longini M, Buonocore G, Venegas M, Baquero H, Visser GH, Van Bel F: Maternal allopurinol during fetal hypoxia lowers cord blood levels of the brain injury marker S-100B. Pediatrics 2009; 124:350-357.
61. Reiter RJ, Tan DX: Melatonin: a novel protective agent against oxidative injury of the ischemic/reperfused heart. Cardiovasc Res 2003; 58: 10-19.
62. Reiter RJ, Tan DX, Osuna C, Gitto E: Actions of melatonin in the reduction of oxidative stress. A review. J Biomed Sci 2000; 7:444-458.
63. Fulia F, Gitto E, Cuzzocrea S, Reiter RJ, Dugo L, Gitto P, Barberi S, Cordaro S, Barberi I: Increased levels of malondialdehyde and nitrite/nitrate in the blood of asphyxiated new-borns: reduction by melatonin. J Pineal Res 2001; 31:343-349.
64. Watanabe K, Wakatsuki A, Shinohara K, Ikenoue N, Yokota K, Fukaya T: Maternally administered melatonin protects against ischemia and reperfusion-induced oxidative mitochondrial damage in premature fetal rat brain. J Pineal Res 2004; 37: 276-280.
65. Okatani Y, Wakatsuki A, Kaneda C: Melato-nin increases activities of glutathione perox-idase and superoxide dismutase in fetal rat brain. J Pineal Res 2000; 28:89-96.
66. Torres-Farfan C, Valenzuela FJ, Mondaca M, Valenzuela GJ, Krause B, Herrera EA, Riquelme R, Llanos AJ, Seron-Ferre M: Evidence of a role for melatonin in fetal sheep physiology: direct actions of melatonin on fetal cerebral artery, brown adipose tissue and adrenal gland. J Physiol 2008; 586:4017-4027.
67. Kaur C, Sivakumar V, Ling EA: Melatonin protects periventricular white matter from damage due to hypoxia. J Pineal Res 2010; 48: 185-193.
68. Thakor AS, Herrera EA, Seron-Ferre M, Giussani DA: Melatonin and vitamin C increase umbilical blood flow via nitric oxide-dependent mechanisms. J Pineal Res 2010; 49: 399-406.
69. Radogna F, Diederich M, Ghibelli L: Melato-nin: a pleiotropic molecule regulating inflammation. Biochem Pharmacol 2010; 80: 1844-1852.
70. Sadowsky DW, Yellon S, Mitchell MD, Na-thanielsz PW: Lack of effect of melatonin on myometrial electromyographic activity in the pregnant sheep at 138-142 days gestation (term = 147 days gestation). Endocrinology 1991; 128: 1812-1818.
71. Torres-Farfan C, Richter HG, Germain AM, Valenzuela GJ, Campino C, Rojas-Garcia P, Forcelledo ML, Torrealba F, Seron-Ferre M: Maternal melatonin selectively inhibits cor-tisol production in the primate fetal adrenal gland. J Physiol 2004; 554:841-856.
72. Holmquist L, Stuchbury G, Berbaum K, Muscat S, Young S, Hager K, Engel J, Munch G: Lipoic acid as a novel treatment for Alzheimer's disease and related dementias. Pharmacol Ther 2007; 113:154-164.
73. Packer L, Tritschler HJ, Wessel K: Neuropro-tection by the metabolic antioxidant alpha-lipoic acid. Free Radic Biol Med 1997; 22:359-378.
74. Toklu HZ, Hakan T, Celik H, Biber N, Erzik C, Ogunc AV, Akakin D, Cikler E, Cetinel S, Ersahin M, Sener G: Neuroprotective effects of alpha-lipoic acid in experimental spinal cord injury in rats. J Spinal Cord Med 2010; 33:401-409.
75. Ersahin M, Toklu HZ, Cetinel S, Yuksel M, Erzik C, Berkman MZ, Yegen BC, Sener G: Alpha lipoic acid alleviates oxidative stress and preserves blood brain permeability in rats with subarachnoid hemorrhage. Neuro-chem Res 2010; 35: 418-428.
76. Panigrahi M, Sadguna Y, Shivakumar BR, Kolluri SV, Roy S, Packer L, Ravindranath V: alpha-Lipoic acid protects against reperfu-sion injury following cerebral ischemia in rats. Brain Res 1996; 717: 184-188.
77. Cao X, Phillis JW: The free radical scavenger, alpha-lipoic acid, protects against cerebral ischemia-reperfusion injury in gerbils. Free Radic Res 1995; 23: 365-370.
78. Singh U, Jialal I: Alpha-lipoic acid supplementation and diabetes. Nutr Rev 2008; 66: 646-657.
79. Sugimura Y, Murase T, Kobayashi K, Oyama K, Hayasaka S, Kanou Y, Oiso Y, Murata Y: Alpha-lipoic acid reduces congenital malformations in the offspring of diabetic mice. Diabetes Metab Res Rev 2009; 25:287-294.
80. Wolz P, Krieglstein J: Neuroprotective effects of alpha-lipoic acid and its enantiomers demonstrated in rodent models of focal cerebral ischemia. Neuropharmacolog y 1996; 35: 369-375.
81. Sheldon RA, Christen S, Ferriero DM: Genetic and pharmacologic manipulation of oxidative stress after neonatal hypoxia-isch-emia. Int J Dev Neurosci 2008; 26: 87-92.
82. Packer L, Weber SU, Rimbach G: Molecular aspects of alpha-tocotrienol antioxidant action and cell signalling. J Nutr 2001; 131: 369S-373S.
83. Halks-Miller M, Henderson M, Eng LF: Alpha tocopherol decreases lipid peroxidation, neuronal necrosis, and reactive gliosis in re-aggregate cultures of fetal rat brain. J Neuro-pathol Exp Neurol 1986; 45:471-484.
84. Osakada F, Hashino A, Kume T, Katsuki H, Kaneko S, Akaike A: Neuroprotective effects of alpha-tocopherol on oxidative stress in rat striatal cultures. Eur J Pharmacol 2003; 465: 15-22.
85. Miura S, Ishida-Nakajima W, Ishida A, Kawamura M, Ohmura A, Oguma R, Sato Y, Takahashi T: Ascorbic acid protects the newborn rat brain from hypoxic-ischemia. Brain Dev 2009; 31: 307-417.
86. Then SM, Mazlan M, Mat Top G, Wan Ngah WZ: Is vitamin E toxic to neuron cells? Cell Mol Neurobiol 2009; 29:485-496.
87. van Tits LJ, Demacker PN, de Graaf J, Hak-Lemmers HL, Stalenhoef AF: alpha-tocoph-erol supplementation decreases production of superoxide and cytokines by leukocytes ex vivo in both normolipidemic and hypertri-glyceridemic individuals. Am J Clin Nutr 2000; 71: 458-464.
88. Flanary BE, Streit WJ: Alpha-tocopherol (vitamin E) induces rapid, nonsustained proliferation in cultured rat microglia. Glia 2006; 53: 669-674.
89. Beyer RE: The role of ascorbate in antioxi-dant protection of biomembranes: interaction with vitamin E and coenzyme Q. J Bio-energ Biomembr 1994; 26: 349-358.
90. Nakai A, Shibazaki Y, Taniuchi Y, Oya A, Asakura H, Koshino T, Araki T: Vitamins ameliorate secondary mitochondrial failure in neonatal rat brain. Pediatr Neurol 2002; 27: 30-35.
91. Chappell LC, Seed PT, Kelly FJ, Briley A, Hunt BJ, Charnock-Jones DS, Mallet A, Poston L: Vitamin C and E supplementation in women at risk of preeclampsia is associated with changes in indices of oxidative stress and placental function. Am J Obstet Gynecol 2002; 187:777-784.
92. Chappell LC, Seed PT, Briley AL, Kelly FJ, Lee R, Hunt BJ, Parmar K, Bewley SJ, Shen-nan AH, Steer PJ, Poston L: Effect of anti-oxidants on the occurrence of pre-eclampsia in women at increased risk: a randomised trial. Lancet 1999; 354: 810-816.
93. Roberts JM, Myatt L, Spong CY, Thom EA, Hauth JC, Leveno KJ, Pearson GD, Wapner RJ, Varner MW, Thorp JM, Jr, Mercer BM, Peaceman AM, Ramin SM, Carpenter MW, Samuels P, Sciscione A, Harper M, Smith WJ, Saade G, Sorokin Y, Anderson GB: Vitamins C and E to prevent complications of pregnancy-associated hypertension. N Engl J Med 2010; 362:1282-1291.
94. Conde-Agudelo A, Romero R, Kusanovic JP, Hassan SS: Supplementation with vitamins C and E during pregnancy for the prevention of preeclampsia and other adverse maternal and perinatal outcomes: a systematic review and metaanalysis. Am J Obstet Gynecol 2011; 204:503, e1-e12.