Pharmacological neuroprotection after perinatal hypoxic-ischemic brain injury

Current Neuropharmacology

Volumn 8, Issue 4, 2010, Pages 324-334

  Fan, Xiyong ^a,b   Kavelaars, Annemieke ^a   Heijnen, Cobi J ^a   Groenendaal, Floris ^a   van Bel, Frank ^a  

^a PEKING UNIVERSITY FIRST HOSPITAL   (China)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Brain; Hypoxia; Ischemia; Neonate; Neuroprotection; Pharmacology

Indexed keywords

EID: 84863177175     PISSN: 1570159X     EISSN: 18756190     Source Type: Journal    
DOI: 10.2174/157015910793358150     Document Type: Article

References (131)

1. [1] Glass, H.C.; Ferriero, D.M. Treatment of hypoxic-ischemic encephalopathy in newborns. Curr. Treat Options Neurol., 2007, 9(6), 414-423.
2. [2] Gonzalez, F.F.; Ferriero, D.M. Therapeutics for neonatal brain injury. Pharmacol. Ther., 2008, 120(1), 43-53.
3. [3] Scafidi, J.; Gallo, V. New concepts in perinatal hypoxia ischemia encephalopathy. Curr. Neurol. Neurosci. Rep., 2008, 8(2), 130-138.
4. [4] Azzopardi, D.V.; Strohm, B.; Edwards, A.D.; Dyet, L.; Halliday, H.L.; Juszczak, E.; Kapellou, O.; Levene, M.; Marlow, N.; Porter, E.; Thoresen, M.; Whitelaw, A.; Brocklehurst, P. Moderate hypothermia to treat perinatal asphyxial encephalopathy. N. Engl. J. Med., 2009, 361(14), 1349-1358.
5. [5] Hoeger, H.; Engidawork, E.; Stolzlechner, D.; Bubna-Littitz, H.; Lubec, B. Long-term effect of moderate and profound hypothermia on morphology, neurological, cognitive and behavioural functions in a rat model of perinatal asphyxia. Amino Acids, 2006, 31(4), 385-396.
6. [6] Ohmura, A.; Nakajima, W.; Ishida, A.; Yasuoka, N.; Kawamura, M.; Miura, S.; Takada, G. Prolonged hypothermia protects neonatal rat brain against hypoxic-ischemia by reducing both apoptosis and necrosis. Brain Dev., 2005, 27(7), 517-526.
7. [7] Robertson, N.J.; Nakakeeto, M.; Hagmann, C.; Cowan, F.M.; Acolet, D.; Iwata, O.; Allen, E.; Elbourne, D.; Costello, A.; Jacobs, I. Therapeutic hypothermia for birth asphyxia in low-resource settings: a pilot randomised controlled trial. Lancet, 2008, 372(9641), 801-803.
8. [8] Hoehn, T.; Hansmann, G.; Bührer, C.; Simbruner, G.; Gunn, A.J.; Yager, J.; Levene, M.; Hamrick, S.E.; Shankaran, S.; Thoresen, M. Therapeutic hypothermia in neonates. Review of current clinical data, ILCOR recommendations and suggestions for implementation in neonatal intensive care units. Resuscitation, 2008, 78(1), 7-12.
9. [9] Badr Zahr, L.K.; Purdy, I. Brain injury in the infant: the old, the new, and the uncertain. J. Perinat. Neonatal. Nurs., 2006, 20(2), 163-175.
10. [10] Girard, S.; Kadhim, H.; Larouche, A.; Roy, M.; Gobeil, F.; Sébire, G. Pro-inflammatory disequilibrium of the IL-1 beta/IL-1ra ratio in an experimental model of perinatal brain damages induced by lipopolysaccharide and hypoxia-ischemia. Cytokine, 2008, 43(1), 54-62.
11. [11] Hilton, G.D.; Nunez, J.L.; Bambrick, L.; Thompson, S.M.; McCarthy, M.M. Glutamate-mediated excitotoxicity in neonatal hippocampal neurons is mediated by mGluR-induced release of Ca++ from intracellular stores and is prevented by estradiol. Eur. J. Neurosci., 2006, 24(11), 3008-3016.
12. [12] Kumar, A.; Mittal, R.; Khanna, H.D.; Basu, S. Free radical injury and blood-brain barrier permeability in hypoxic-ischemic encephalopathy. Pediatrics, 2008, 122(3), e722-e727.
13. [13] Ferriero, D.M. Oxidant mechanisms in neonatal hypoxia-ischemia. Dev. Neurosci., 2001, 23(3), 198-202.
14. [14] Papazisis, G.; Pourzitaki, C.; Sardeli, C.; Lallas, A.; Amaniti, E.; Kouvelas, D. Deferoxamine decreases the excitatory amino acid levels and improves the histological outcome in the hippocampus of neonatal rats after hypoxia-ischemia. Pharmacol. Res., 2008, 57(1), 73-78.
15. [15] Ogihara, T.; Hirano, K.; Ogihara, H.; Misaki, K.; Hiroi, M.; Morinobu, T.; Kim, H.S.; Ogawa, S.; Ban, R.; Hasegawa, M.; Tamai, H. Non-protein-bound transition metals and hydroxyl radical generation in cerebrospinal fluid of newborn infants with hypoxic ischemic encephalopathy. Pediatr. Res., 2003, 53(4), 594-599.
16. [16] van den Tweel, E.R.; Nijboer, C.; Kavelaars, A.; Heijnen, C.J.; Groenendaal, F.; van Bel, F. Expression of nitric oxide synthase isoforms and nitrotyrosine formation after hypoxia-ischemia in the neonatal rat brain. J. Neuroimmunol., 2005, 167(1-2), 64-71.
17. [17] Cimino, M.; Balduini, W.; Carloni, S.; Gelosa, P.; Guerrini, U.; Tremoli, E.; Sironi, L. Neuroprotective effect of simvastatin in stroke: a comparison between adult and neonatal rat models of cerebral ischemia. Neurotoxicology, 2005, 26(5), 929-933.
18. [18] Chang, Y.; Hsieh, C.Y.; Peng, Z.A.; Yen, T.L.; Hsiao, G.; Chou, D.S.; Chen, C.M.; Sheu, J.R. Neuroprotective mechanisms of puerarin in middle cerebral artery occlusion-induced brain infarction in rats. J. Biomed. Sci., 2009, 16, 9.
19. [19] Fabian, R.H.; Perez-Polo, J.R.; Kent, T.A. Perivascular nitric oxide and superoxide in neonatal cerebral hypoxia-ischemia. Am. J. Physiol. Heart. Circ. Physiol., 2008, 295(4), H1809-H1814.
20. [20] Suzuki, M.; Tabuchi, M.; Ikeda, M.; Tomita, T. Concurrent formation of peroxynitrite with the expression of inducible nitric oxide synthase in the brain during middle cerebral artery occlusion and reperfusion in rats. Brain. Res., 2002, 951(1), 113-120.
21. [21] Yang, L.; Sameshima, H.; Yamaguchi, M.; Ikenoue, T. Expression of inducible nitric oxide synthase and cyclooxygenase-2 mRNA in brain damage induced by lipopolysaccharide and intermittent hypoxia-ischemia in neonatal rats. J. Obstet. Gynaecol. Res., 2005, 31(2), 185-191.
22. [22] Leonardo, C.C.; Pennypacker, K.R. Neuroinflammation and MMPs: potential therapeutic targets in neonatal hypoxic-ischemic injury. J. Neuroinflamm., 2009, 6, 13.
23. [23] Nijboer, C.H.; Heijnen, C.J.; Groenendaal, F.; May, M.J.; van Bel, F.; Kavelaars, A. Strong neuroprotection by inhibition of NFkappaB after neonatal hypoxia-ischemia involves apoptotic mechanisms but is independent of cytokines. Stroke, 2008, 39(7), 2129-2137.
24. [24] Nijboer, C.H.; Heijnen, C.J.; Groenendaal, F.; May, M.J.; van Bel, F.; Kavelaars, A. A dual role of the NF-kappaB pathway in neonatal hypoxic-ischemic brain damage. Stroke, 2008, 39(9), 2578-2586.
25. [25] Waetzig, V.; Czeloth, K.; Hidding, U.; Mielke, K.; Kanzow, M.; Brecht, S.; Goetz, M.; Lucius, R.; Herdegen, T.; Hanisch, U.K. c-Jun N-terminal kinases (JNKs) mediate pro-inflammatory actions of microglia. Glia, 2005, 50(3), 235-246.
26. [26] Northington, F.J.; Ferriero, D.M.; Graham, E.M.; Traystman, R.J.; Martin, L.J. Early neurodegeneration after hypoxia-ischemia in neonatal rat is necrosis while delayed neuronal death is apoptosis. Neurobiol. Dis., 2001, 8(2), 207-219.
27. [27] Blomgren, K.; Leist, M.; Groc, L. Pathological apoptosis in the developing brain. Apoptosis, 2007, 12(5), 993-1010.
28. [28] Wang, X.; Karlsson, J.O.; Zhu, C.; Bahr, B.A.; Hagberg, H.; Blomgren, K. Caspase-3 activation after neonatal rat cerebral hypoxia-ischemia. Biol. Neonate, 2001, 79(3-4), 172-179.
29. [29] Gill, R.; Soriano, M.; Blomgren, K.; Hagberg, H.; Wybrecht, R.; Miss, M.T.; Hoefer, S.; Adam, G.; Niederhauser, O.; Kemp, J.A.; Loetscher, H. Role of caspase-3 activation in cerebral ischemiainduced neurodegeneration in adult and neonatal brain. J. Cereb. Blood Flow Metab., 2002, 22(4), 420-430.
30. [30] Scheepens, A.; Wassink, G.; Blanco, C.E. The effect of a global birth asphyxia on the ontogeny of BDNF and NGF protein expression in the juvenile brain. Brain Res. Dev. Brain Res., 2003, 140(2), 215-221.
31. [31] van Velthoven, C.T.; Kavelaars, A.; van Bel, F.; Heijnen, C.J. Mesenchymal stem cell treatment after neonatal hypoxic-ischemic brain injury improves behavioral outcome and induces neuronal and oligodendrocyte regeneration. Brain Behav. Immun., 2010, 24(3), 387-393.
32. [32] van Velthoven, C.T.; Kavelaars, A.; van Bel, F.; Heijnen, C.J. Regeneration of the ischemic brain by engineered stem cells: fuelling endogenous repair processes. Brain Res. Rev., 2009, 61(1), 1-13.
33. [33] Peeters, C.; Hoelen, D.; Groenendaal, F.; van Bel, F.; Bär, D. Deferoxamine, allopurinol and oxypurinol are not neuroprotective after oxygen/glucose deprivation in an organotypic hippocampal model, lacking functional endothelial cells. Brain Res., 2003, 963(1-2), 72-80.
34. [34] Berger, R.; Lehmann, T.; Karcher, J.; Garnier, Y.; Jensen, A. Low dose flunarizine protects the fetal brain from ischemic injury in sheep. Pediatr. Res., 1998, 44(3), 277-282.
35. [35] Kittaka, M.; Giannotta, S.L.; Zelman, V.; Correale, J.D.; DeGiorgio, C.M.; Weiss, M.H.; Zlokovic, B.V. Attenuation of brain injury and reduction of neuron-specific enolase by nicardipine in systemic circulation following focal ischemia and reperfusion in a rat model. J. Neurosurg., 1997, 87(5), 731-737.
36. [36] Levene, M.I.; Gibson, N.A.; Fenton, A.C.; Papathoma, E.; Barnett, D. The use of a calcium-channel blocker, nicardipine, for severely asphyxiated newborn infants. Dev. Med. Child. Neurol., 1990, 32(7), 567-574.
37. [37] Maroszyńska, I.; Sobolewska, B.; Gulczyńska, E.; Zylińska, L.; Lerch, E.; Kicińska, M.; Rudecka, M. Can magnesium sulfate reduce the risk of cerebral injury after perinatal asphyxia? Acta Pol. Pharm., 1999, 56(6), 469-473.
38. [38] Groenendaal, F.; Rademaker, C.M.; Toet, M.C.; de Vries, L.S. Effects of magnesium sulphate on amplitude-integrated continuous EEG in asphyxiated term neonates. Acta Paediatr., 2002, 91(10), 1073-1077.
39. [39] Whitelaw, A.; Thoresen, M. Clinical trials of treatments after perinatal asphyxia. Curr. Opin. Pediatr., 2002, 14(6), 664-668.
40. [40] Dingley, J.; Tooley, J.; Porter, H.; Thoresen, M. Xenon provides short-term neuroprotection in neonatal rats when administered after hypoxia-ischemia. Stroke, 2006, 37(2), 501-506.
41. [41] Hobbs, C.; Thoresen, M.; Tucker, A.; Aquilina, K.; Chakkarapani, E.; Dingley, J. Xenon and hypothermia combine additively, offering long-term functional and histopathologic neuroprotection after neonatal hypoxia/ischemia. Stroke, 2008, 39(4), 1307-1313.
42. [42] Mink, R.; Johnston, J. The effect of infusing hypoxanthine or xanthine on hypoxic-ischemic brain injury in rabbits. Brain. Res., 2007, 1147, 256-264.
43. [43] Shouman, B.O.; Mesbah, A.; Aly, H. Iron metabolism and lipid peroxidation products in infants with hypoxic ischemic encephalopathy. J. Perinatol., 2008, 28(7), 487-491.
44. [44] Windelborn, J.A.; Lipton, P. Lysosomal release of cathepsins causes ischemic damage in the rat hippocampal slice and depends on NMDA-mediated calcium influx, arachidonic acid metabolism, and free radical production. J. Neurochem., 2008, 106(1), 56-69.
45. [45] Saugstad, O.D. Role of xanthine oxidase and its inhibitor in hypoxia: reoxygenation injury. Pediatrics, 1996, 98(1), 103-107.
46. [46] Moorhouse, P.C.; Grootveld, M.; Halliwell, B.; Quilan, J.G.; Gutteridge, J.M. Allopurinol and oxypurinol are hydroxyl radical scavengers. FEBS Lett., 1987, 213(1), 23-28.
47. [47] Palmer, C.; Towfighi, J.; Roberts, R.L.; Heitjan, D.F. Allopurinol administered after inducing hypoxia-ischemia reduces brain injury in 7-day-old rats. Pediatr. Res., 1993, 33(4 Pt 1), 405-411.
48. [48] Benders, M.J.; Bos, A.F.; Rademaker, C.M.; Rijken, M.; Torrance, H.L.; Groenendaal, F.; van Bel, F. Early postnatal allopurinol does not improve short term outcome after severe birth asphyxia. Arch. Dis. Child Fetal Neonatal. Ed., 2006, 91(3), F163-F165.
49. [49] Gunes, T.; Ozturk, M.A.; Koklu, E.; Kose, K.; Gunes, I. Effect of allopurinol supplementation on nitric oxide levels in asphyxiated newborns. Pediatr. Neurol., 2007, 36(1), 17-24.
50. [50] Torrance, H.L.; Benders, M.J.; Derks, J.B.; Rademaker, C.M.; Bos, A.F.; Van Den Berg, P.; Longini, M.; Buonocore, G.; Venegas, M.; Baquero, H.; Visser, G.H.; Van Bel, F. Maternal allopurinol during fetal hypoxia lowers cord blood levels of the brain injury marker S-100B. Pediatrics, 2009, 124(1), 350-357.
51. [51] Sävman, K.; Nilsson, U.A.; Thoresen, M.; Kjellmer, I. Nonprotein-bound iron in brain interstitium of newborn pigs after hypoxia. Dev. Neurosci., 2005, 27(2-4), 176-184.
52. [52] Dawson, V.L.; Dawson, T.M.; Bartley, D.A.; Uhl, G.R.; Snyder, S.H. Mechanisms of nitric oxide mediated neurotoxicity in primary brain cultures. J. Neurosci., 1993, 13(6), 2651-2661.
53. [53] Hamada, Y.; Hayakawa, T.; Hattor, H.; Mikawa, H. Inhibitor of nitric oxide synthesis reduces hypoxicischemic brain damage in the neonatal rat. Pediatr. Res., 1994, 35(1), 10-14.
54. [54] Ashwal, S.; Cole, D.J.; Osborne, T.N.; Pearce, W.J. Dual effects of L-NAME during transient focal cerebral ischemia in spontaneously hypertensive rats. Am. J. Physiol., 1994, 267(1 Pt2), H276-H284.
55. [55] Groenendaal, F.; de Graaf, R.A.; van Vliet, G.; Nicolay, K. Effects of hypoxia-ischemia and inhibition of nitric oxide synthase on cerebral energy metabolism in newborn piglets. Pediatr. Res., 1999, 45(6), 827-833.
56. [56] Marks, K.A.; Mallard, C.E.; Roberts, I.; Williams, C.E.; Gluckman, P.D.; Edwards, A.D. Nitric oxide synthase inhibition and delayed cerebral injury after severe cerebral ischemia in fetal sheep. Pediatr. Res., 1999, 46(1), 8-12.
57. [57] Ishida, A.; Trescher, W.H.; Lange, M.S.; Johnston, M.V. Prolonged suppression of brain nitric oxide synthase activity by 7-nitroindazole protects against cerebral hypoxic-ischemic injury in neonatal rat. Brain Dev., 2001, 23(5), 349-354.
58. [58] Tsuji, M.; Higuchi, Y.; Shiraishi, K.; Kume, T.; Akaike, A.; Hattori, H. Protective effect of aminoguanidine on hypoxicischemic brain damage and temporal profile of brain nitric oxide in neonatal rat. Pediatr. Res., 2000, 47(1), 79-83.
59. [59] van den Tweel, E.R.; Peeters-Scholte, C.M.; van Bel, F.; Heijnen, C.J.; Groenendaal, F. Inhibition of nNOS and iNOS following hypoxia-ischaemia improves long-term outcome but does not influence the inflammatory response in the neonatal rat brain. Dev. Neurosci., 2002, 24(5), 389-395.
60. [60] Nijboer, C.H.; Groenendaal, F.; Kavelaars, A.; Hagberg, H.H.; van Bel, F.; Heijnen, C.J. Gender-specific neuroprotection by 2-iminobiotin after hypoxia-ischemia in the neonatal rat via a nitric oxide independent pathway. J. Cereb. Blood. Flow Metab., 2007, 27(2), 282-292.
61. [61] Nijboer, C.H.; Kavelaars, A.; van Bel, F.; Heijnen, C.J.; Groenendaal, F. Gender-dependent pathways of hypoxia-ischemiainduced cell death and neuroprotection in the immature P3 rat. Dev. Neurosci., 2007, 29(4-5), 385-392.
62. [62] van den Tweel, E.R.; van Bel, F.; Kavelaars, A.; Peeters-Scholte, C.M.; Haumann, J.; Nijboer, C.H.; Heijnen, C.J.; Groenendaal, F. Long-term neuroprotection with 2-iminobiotin, an inhibitor of neuronal and inducible nitric oxide synthase, after cerebral hypoxia-ischemia in neonatal rats. J. Cereb. Blood. Flow. Metab., 2005, 25(1), 67-74.
63. [63] Taskin, E.; Ozcan, K.; Canacankatan, N.; Satar, M.; Yapicioglu, H.Y.; Erdogan, S. The effects of indomethacin on caspases, glutathione level and lipid peroxidation in the newborn rats with hypoxic-ischemic cerebral injury. Brain Res., 2009, 1289, 118-123.
64. [64] Kumar Nair, P.A.; Pai, M.G.; Gazal, H.A.; Da Costa, D.E.; Al Khusaiby, S.M. Indomethacin prophylaxis for intraventricular hemorrhage in very low birth weight babies. Indian. Pediatr., 2004, 41(6), 551-558.
65. [65] Ment, L.R.; Vohr, B.R.; Makuch, R.W.; Westerveld, M.; Katz, K.H.; Schneider, K.C.; Duncan, C.C.; Ehrenkranz, R.; Oh, W.; Philip, A.G.; Scott, D.T.; Allan, W.C. Prevention of intraventricular hemorrhage by indomethacin in male preterm infants. J. Pediatr., 2004, 145(6), 832-834.
66. [66] Miller, S.P.; Mayer, E.E.; Clyman, R.I.; Glidden, D.V.; Hamrick, S.E.; Barkovich, A.J. Prolonged indomethacin exposure is associated with decreased white matter injury detected with magnetic resonance imaging in premature newborns at 24 to 28 weeks' gestation at birth. Pediatrics, 2006, 117(5), 1626-1631.
67. [67] Torres, L.; Anderson, C.; Marro, P.; Mishra, O.P.; Delivoria-Papadopoulos, M. Cyclooxygenase-mediated generation of free radicals during hypoxia in the cerebral cortex of newborn piglets. Neurochem. Res., 2004, 29(10), 1825-1830.
68. [68] van der Kooij, M.A.; Groenendaal, F.; Kavelaars, A.; Heijnen, C.J.; van Bel, F. Neuroprotective properties and mechanisms of erythropoietin in in vitro and in vivo experimental models for hypoxia/ischemia. Brain Res. Rev., 2008, 59(1), 22-33.
69. [69] Gonzalez, F.F.; Abel, R.; Almli, C.R.; Mu, D.; Wendland, M.; Ferriero, D.M. Erythropoietin sustains cognitive function and brain volume after neonatal stroke. Dev. Neurosci., 2009, 31(5), 403-411.
70. [70] Iwai, M.; Cao, G.; Yin, W.; Stetler, R.A.; Liu, J.; Chen, J. Erythropoietin promotes neuronal replacement through revascularization and neurogenesis after neonatal hypoxia/ischemia in rats. Stroke, 2007, 38(10), 2795-2803.
71. [71] Juul, S.E.; Beyer, R.P.; Bammler, T.K.; McPherson, R.J.; Wilkerson, J.; Farin, F.M. Microarray analysis of high-dose recombinant erythropoietin treatment of unilateral brain injury in neonatal mouse hippocampus. Pediatr. Res., 2009, 65(5), 485-492.
72. [72] Zhu, C.; Kang, W.; Xu, F.; Cheng, X.; Zhang, Z.; Jia, L.; Ji, L.; Guo, X.; Xiong, H.; Simbruner, G.; Blomgren, K.; Wang, X. Erythropoietin improved neurologic outcomes in newborns with hypoxic-ischemic encephalopathy. Pediatrics, 2009, 124(2), e218-e226.
73. [73] Nagai, A.; Nakagawa, E.; Choi, H.B.; Hatori, K.; Kobayashi, S.; Kim, S.U. Erythropoietin and erythropoietin receptors in human CNS neurons, astrocytes, microglia, and oligodendrocytes grown in culture. J. Neuropathol. Exp. Neurol., 2001, 60(4), 386-392.
74. [74] Sun, Y.; Calvert, J.W.; Zhang, J.H. Neonatal hypoxia/ischemia is associated with decreased inflammatory mediators after erythropoietin administration. Stroke, 2005, 36(8), 1672-1678.
75. [75] Demers, E.J.; McPherson, R.J.; Juul, S.E. Erythropoietin protects dopaminergic neurons and improves neurobehavioral outcomes in juvenile rats after neonatal hypoxia-ischemia. Pediatr. Res., 2005, 58(2), 297-301.
76. [76] Kumral, A.; Uysal, N.; Tugyan, K.; Sonmez, A.; Yilmaz, O.; Gokmen, N.; Kiray, M.; Genc, S.; Duman, N.; Koroglu, T.F.; Ozkan, H.; Genc, K. Erythropoietin improves long-term spatial memory deficits and brain injury following neonatal hypoxiaischemia in rats. Behav. Brain. Res., 2004, 153(1), 77-86.
77. [77] Ehrenreich, H.; Weissenborn, K.; Prange, H.; Schneider, D.; Weimar, C.; Wartenberg, K.; Schellinger, P.D.; Bohn, M.; Becker, H.; Wegrzyn, M.; Jähnig, P.; Herrmann, M.; Knauth, M.; Bähr, M.; Heide, W.; Wagner, A.; Schwab, S.; Reichmann, H.; Schwendemann, G.; Dengler, R.; Kastrup, A.; Bartels, C. Recombinant human erythropoietin in the treatment of acute ischemic stroke. Stroke, 2009, 40(12), e647-e656.
78. [78] van der Kooij, M.A.; Groenendaal, F.; Kavelaars, A.; Heijnen, C.J.; van Bel, F. Combination of deferoxamine and erythropoietin: therapy for hypoxia-ischemia-induced brain injury in the neonatal rat? Neurosci. Lett., 2009, 451(2), 109-113.
79. [79] Wen, T.C.; Rogido, M.; Peng, H.; Genetta, T.; Moore, J.; Sola, A. Gender differences in long-term beneficial effects of erythropoietin given after neonatal stroke in postnatal day-7 rats. Neuroscience, 2006, 139(3), 803-811.
80. [80] Claustrat, B.; Brun, J.; Chazot, G. The basic physiology and pathophysiology of melatonin. Sleep Med. Rev., 2005, 9(1), 11-24.
81. [81] Welin, A.K.; 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(2), 153-158.
82. [82] Carloni, S.; Perrone, S.; Buonocore, G.; Longini, M.; Proietti, F.; Balduini, W. Melatonin protects from the long-term consequences of a neonatal hypoxic-ischemic brain injury in rats. J. Pineal. Res., 2008, 44(2), 157-164.
83. [83] Reiter, R.J.; Calvo, J.R.; Karbownik, M.; Qi, W.; Tan, D.X. Melatonin and its relation to the immune system and inflammation. Ann. N. Y. Acad. Sci., 2000, 917, 376-386.
84. [84] Nijboer, C.H.; Heijnen, C.J.; Groenendaal, F.; van Bel, F.; Kavelaars, A. Alternate pathways preserve tumor necrosis factoralpha production after nuclear factor-kappaB inhibition in neonatal cerebral hypoxia-ischemia. Stroke, 2009, 40(10), 3362-3368.
85. [85] Nijboer, C.H.; van der Kooij, M.A.; van Bel, F.; Ohl, F.; Heijnen, C.J.; Kavelaars, A. Inhibition of the JNK/AP-1 pathway reduces neuronal death and improves behavioral outcome after neonatal hypoxic-ischemic brain injury. Brain. Behav. Immun., 2009, doi:10.1016/j.bbi.2009.09.008.
86. [86] Ginet, V.; Puyal, J.; Magnin, G.; Clarke, P.G.; Truttmann, A.C. Limited role of the c-Jun N-terminal kinase pathway in a neonatal rat model of cerebral hypoxia-ischemia. J. Neurochem., 2009, 108(3), 552-562.
87. [87] van den Tweel, E.R.; Kavelaars, A.; Lombardi, M.S.; Groenendaal, F.; May, M.; Heijnen, C.J.; van Bel, F. Selective inhibition of nuclear factor-kappaB activation after hypoxia/ischemia in neonatal rats is not neuroprotective. Pediatr. Res., 2006, 59(2), 232-236.
88. [88] Strauss, M.B.; Hargens, A.R.; Gershuni, D.H.; Greenberg, D.A.; Crenshaw, A.G.; Hart, G.B.; Akeson, W.H. Reduction of skeletal muscle necrosis using intermittent hyperbaric oxygen in a model compartment syndrome. J. Bone Joint Surg. Am., 1983, 65(5), 656-662.
89. [89] Zhang, J.H.; Lo, T.; Mychaskiw, G.; Colohan, A. Mechanisms of hyperbaric oxygen and neuroprotection in stroke. Pathophysiology, 2005, 12(1), 63-77.
90. [90] Matchett, G.A.; Martin, R.D.; Zhang, J.H. Hyperbaric oxygen therapy and cerebral ischemia: neuroprotective mechanisms. Neurol. Res., 2009, 31(2), 114-121.
91. [91] Calvert, J.W.; Yin, W.; Patel, M.; Badr, A.; Mychaskiw, G.; Parent, A.D.; Zhang, J.H. Hyperbaric oxygenation prevented brain injury induced by hypoxia-ischemia in a neonatal rat model. Brain Res., 2002, 951(1), 1-8.
92. [92] Zamboni, W.A.; Roth, A.C.; Russell, R.C.; Graham, B.; Suchy, H.; Kucan, J.O. Morphologic analysis of the microcirculation during reperfusion of ischemic skeletal muscle and the effect of hyperbaric oxygen. Plast. Reconstr. Surg., 1993, 91(6), 1110-1123.
93. [93] Buras, J.A.; Stahl, G.L.; Svoboda, K.S.; Reenstra, W.R. Hyperbaric oxygen down-regulates ICAM-1 expression induced by hypoxia and hypoglycemia: the role of eNOS. Am. J. Physiol., 2000, 278(2), C292-C302.
94. [94] Kurata, S.; Yamashita, U.; Nakajima, H. Hyperbaric oxygenation reduces the cytostatic activity and transcription of nitric oxide synthetase gene of mouse peritoneal macrophages. Biochim. Biophys. Acta, 1995, 1263(1), 35-38.
95. [95] Li, J.; Liu, W.; Ding, S.; Xu, W.; Guan, Y.; Zhang, J.H.; Sun, X. Hyperbaric oxygen preconditioning induces tolerance against brain ischemia-reperfusion injury by upregulation of antioxidant enzymes in rats. Brain Res., 2008, 1210, 223-229.
96. [96] Chen, M.F.; Chen, H.M.; Ueng, S.W.; Shyr, M.H. Hyperbaric oxygen pre-treatment attenuates hepatic reperfusion injury. Liver, 1998, 18(2), 110-116.
97. [97] Li, J.S.; Zhang, W.; Kang, Z.M.; Ding, S.J.; Liu, W.W.; Zhang, J.H.; Guan, Y.T.; Sun, X.J. Hyperbaric oxygen preconditioning reduces ischemia-reperfusion injury by inhibition of apoptosis via mitochondrial pathway in rat brain. Neuroscience, 2009, 159(4), 1309-1315.
98. [98] Yang, Y.J.; Wang, X.L.; Yu, X.H.; Wang, X.; Xie, M.; Liu, C.T. Hyperbaric oxygen induces endogenous neural stem cells to proliferate and differentiate in hypoxic-ischemic brain damage in neonatal rats. Undersea. Hyperb. Med., 2008, 35(2), 113-129.
99. [99] Wang, X.L.; Zhao, Y.S.; Yang, Y.J.; Xie, M.; Yu, X.H. Therapeutic window of hyperbaric oxygen therapy for hypoxicischemic brain damage in newborn rats. Brain Res., 2008, 1222, 87-94.
100. [100] Binder, D.K. Neurotrophins in the dentate gyrus. Prog. Brain. Res., 2007, 163, 371-397.
101. [101] Alagappan, D.; Lazzarino, D.A.; Felling, R.J.; Balan, M.; Kotenko, S.V.; Levison, S.W. Brain injury expands the numbers of neural stem cells and progenitors in the SVZ by enhancing their responsiveness to EGF. ASN Neuro., 2009, 1(2), e00009.
102. [102] Kanagawa, T.; Fukuda, H.; Tsubouchi, H.; Komoto, Y.; Hayashi, S.; Fukui, O.; Shimoya, K.; Murata, Y. A decrease of cell proliferation by hypothermia in the hippocampus of the neonatal rat. Brain Res., 2006, 1111(1), 36-40.
103. [103] Sifringer, M.; Brait, D.; Weichelt, U.; Zimmerman, G.; Endesfelder, S.; Brehmer, F.; von Haefen, C.; Friedman, A.; Soreq, H.; Bendix, I.; Gerstner, B.; Felderhoff-Mueser, U. Erythropoietin attenuates hyperoxia-induced oxidative stress in the developing rat brain. Brain Behav. Immun., 2009, doi:10.1016/j.bbi.2009.08.010.
104. [104] Campana, W.M.; Misasi, R.; O'Brien, J.S. Identification of a neurotrophic sequence in erythropoietin. Int. J. Mol. Med., 1998, 1(1), 235-241.
105. [105] Chen, Z.Y.; Asavaritikrai, P.; Prchal, J.T.; Noguchi, C.T. Endogenous erythropoietin signaling is required for normal neural progenitor cell proliferation. J. Biol. Chem., 2007, 282(35), 25875-25883.
106. [106] Wang, L.; Zhang, Z.; Wang, Y.; Zhang, R.; Chopp, M. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke, 2004, 35(7), 1732-1737.
107. [107] Shingo, T.; Sorokan, S.T.; Shimazaki, T.; Weiss, S. Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J. Neurosci., 2001, 21(24), 9733-9743.
108. [108] Gonzalez, F.F.; McQuillen, P.; Mu, D.; Chang, Y.; Wendland, M.; Vexler, Z.; Ferriero, D.M. Erythropoietin enhances long-term neuroprotection and neurogenesis in neonatal stroke. Dev. Neurosci., 2007, 29(4-5), 321-330.
109. [109] Peeters, C.; van Bel, F. Pharmacotherapeutical reduction of posthypoxic-ischemic brain injury in the newborn. Biol. Neonate, 2001, 79(3-4), 274-280.
110. [110] Satar, M.; Ozcan, K.; Yapiciońlu, H.; Narli, N. Serum insulin-like growth factor 1 and growth hormone levels of hypoxic-ischemic newborns. Biol. Neonate., 2004, 85(1), 15-20.
111. [111] Lin, S.; Fan, L.W.; Rhodes, P.G.; Cai, Z. Intranasal administration of IGF-1 attenuates hypoxic-ischemic brain injury in neonatal rats. Exp. Neurol., 2009, 217(2), 361-370.
112. [112] Kirschner, P.B.; Henshaw, R.; Weise, J.; Trubetskoy, V.; Finklestein, S.; Schulz, J.B.; Beal, M.F. Basic fibroblast growth factor protects against excitotoxicity and chemical hypoxia in both neonatal and adult rats. J. Cereb. Blood Flow Metab., 1995, 15(4), 619-623.
113. [113] Galvin, K.A.; Oorschot, D.E. Continuous low-dose treatment with brain-derived neurotrophic factor or neurotrophin-3 protects striatal medium spiny neurons from mild neonatal hypoxia/ischemia: a stereological study. Neuroscience, 2003, 118(4), 1023-1032.
114. [114] Fan, X.; Heijnen, C.J.; van der Kooij, M.A.; Groenendaal, F.; van Bel, F. The role and regulation of hypoxia-inducible factor-1alpha expression in brain development and neonatal hypoxic-ischemic brain injury. Brain Res. Rev., 2009, 62(1), 99-108.
115. [115] Weidemann, A.; Kerdiles, Y.M.; Knaup, K.X.; Rafie, C.A.; Boutin, A.T.; Stockmann, C.; Takeda, N.; Scadeng, M.; Shih, A.Y.; Haase, V.H.; Simon, M.C.; Kleinfeld, D.; Johnson, R.S. The glial cell response is an essential component of hypoxia-induced erythropoiesis in mice. J. Clin. Invest., 2009, 119(11), 3373-3383.
116. [116] Zhang, L.; Qu, Y.; Yang, C.; Tang, J.; Zhang, X.; Mao, M.; Mu, D.; Ferriero, D. Signaling pathway involved in hypoxia-inducible factor-1alpha regulation in hypoxic-ischemic cortical neurons in vitro. Neurosci. Lett., 2009, 461(1), 1-6.
117. [117] Yasuhara, T.; Hara, K.; Maki, M.; Mays, R.W.; Deans, R.J.; Hess, D.C.; Carroll, J.E.; Borlongan, C.V. Intravenous grafts recapitulate the neurorestoration afforded by intracerebrally delivered multipotent adult progenitor cells in neonatal hypoxic-ischemic rats. J. Cereb. Blood. Flow. Metab., 2008, 28(11), 1804-1810.
118. [118] Yasuhara, T.; Matsukawa, N.; Yu, G.; Xu, L.; Mays, R.W.; Kovach, J.; Deans, R.J.; Hess, D.C.; Carroll, J.E.; Borlongan, C.V. Behavioral and histological characterization of intrahippocampal grafts of human bone marrow-derived multipotent progenitor cells in neonatal rats with hypoxic-ischemic injury. Cell Transplant., 2006, 15(3), 231-238.
119. [119] Schmidt, N.O.; Koeder, D.; Messing, M.; Mueller, F.J.; Aboody, K.S.; Kim, S.U.; Black, P.M.; Carroll, R.S.; Westphal, M.; Lamszus, K. Vascular endothelial growth factor-stimulated cerebral microvascular endothelial cells mediate the recruitment of neural stem cells to the neurovascular niche. Brain Res., 2009, 1268, 24-37.
120. [120] Toyama, K.; Honmou, O.; Harada, K.; Suzuki, J.; Houkin, K.; Hamada, H.; Kocsis, J.D. Therapeutic benefits of angiogenetic gene-modified human mesenchymal stem cells after cerebral ischemia. Exp. Neurol., 2009, 216(1), 47-55.
121. [121] Wei, X.; Du, Z.; Zhao, L.; Feng, D.; Wei, G.; He, Y.; Tan, J.; Lee, W.H.; Hampel, H.; Dodel, R.; Johnstone, B.H.; March, K.L.; Farlow, M.R.; Du, Y. IFATS collection: The conditioned media of adipose stromal cells protect against hypoxia-ischemia-induced brain damage in neonatal rats. Stem Cells, 2009, 27(2), 478-488.
122. [122] Chen, J.; Li, Y.; Wang, L.; Lu, M.; Zhang, X.; Chopp, M. Therapeutic benefit of intracerebral transplantation of bone marrow stromal cells after cerebral ischemia in rats. J. Neurol. Sci., 2001, 189(1-2), 49-57.
123. [123] Shen, L.H.; Li, Y.; Chen, J.; Cui, Y.; Zhang, C.; Kapke, A.; Lu, M.; Savant-Bhonsale, S.; Chopp, M. One-year follow-up after bone marrow stromal cell treatment in middle-aged female rats with stroke. Stroke, 2007, 38(7), 2150-2156.
124. [124] Li, Y.; Chen, J.; Chen, X.G.; Wang, L.; Gautam, S.C.; Xu, Y.X.; Katakowski, M.; Zhang, L.J.; Lu, M.; Janakiraman, N.; Chopp, M. Human marrow stromal cell therapy for stroke in rat: neurotrophins and functional recovery. Neurology, 2002, 59(4), 514-523.
125. [125] Rivera, F.J.; Sierralta, W.D.; Minguell, J.J.; Aigner, L. Adult hippocampus derived soluble factors induce a neuronal-like phenotype in mesenchymal stem cells. Neurosci. Lett., 2006, 406(1-2), 49-54.
126. [126] Barks, J.D. Current controversies in hypothermic neuroprotection. Semin. Fetal Neonatal. Med., 2008, 13(1), 30-34.
127. [127] Guan, J.; Gunn, A.J.; Sirimanne, E.S.; Tuffin, J.; Gunning, M.I.; Clark, R.; Gluckman, P.D. The window of opportunity for neuronal rescue with insulin-like growth factor-1 after hypoxia-ischemia in rats is critically modulated by cerebral temperature during recovery. J. Cereb. Blood Flow Metab., 2000, 20(3), 513-519.
128. [128] Thoresen, M.; Hobbs, C.E.; Wood, T.; Chakkarapani, E.; Dingley, J. Cooling combined with immediate or delayed xenon inhalation provides equivalent long-term neuroprotection after neonatal hypoxia-ischemia. J. Cereb. Blood Flow Metab., 2009, 29(4), 707-714.
129. [129] Cariou, A.; Claessens, Y.E.; Pène, F.; Marx, J.S.; Spaulding, C.; Hababou, C.; Casadevall, N.; Mira, J.P.; Carli, P.; Hermine, O. Early high-dose erythropoietin therapy and hypothermia after outof-hospital cardiac arrest: a matched control study. Resuscitation, 2008, 76(3), 397-404.
130. [130] Hlutkin, S.; Zinchuk, V. Effect of melatonin on the blood oxygen transport during hypothermia and rewarming in rats. Adv. Med. Sci., 2008, 53(2), 234-239.
131. [131] Hurn, P.D.; Vannucci, S.J.; Hagberg, H. Adult or perinatal brain injury: does sex matter? Stroke, 2005, 36(2), 193-195.