The effect of prenatal hypoxia on brain development: Short- and long-term consequences demonstrated in rodent models

Developmental Science

Volumn 9, Issue 4, 2006, Pages 338-349

  Golan, Hava ^a   Huleihel, Mahmoud ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ANOXIA; ARTICLE; BIOLOGICAL MODEL; BRAIN; BRAIN MAPPING; CELL DEATH; DISEASE MODEL; FEMALE; HUMAN; ISCHEMIA; LEARNING; MEMORY; PATHOLOGY; PREGNANCY; PRENATAL DEVELOPMENT; RAT;

ANIMALS; ANOXIA; BEHAVIOR, ANIMAL; BRAIN; BRAIN MAPPING; CELL DEATH; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; ISCHEMIA; LEARNING; MEMORY; MODELS, BIOLOGICAL; PREGNANCY; RATS;

EID: 33744957605     PISSN: 1363755X     EISSN: 14677687     Source Type: Journal    
DOI: 10.1111/j.1467-7687.2006.00498.x     Document Type: Article

References (72)

1. Ådén, U., Dahlberg, V., Fredholm, B.B., Lai, L.J., Chen, Z., & Bjelke, B. (2002). MRI evaluation and functional assessment of brain injury after hypoxic ischemia in neonatal mice. Stroke, 33, 1405-1410.
2. Almli, C.R., Levy, T.J., Han, B.H., Shah, A.R., Gidday, J.M., & Holtzman, D.M. (2000). BDNF protects against spatial memory deficits following neonatal hypoxia-ischemia. Experimental Neurology, 166, 99-114.
3. Back, S.A., Han, B.H., Luo, N.L., Chricton, C.A., Xanthoudakis, S., Tam, J., Arvin, K.L., & Holtzman, D.M. (2002). Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. Journal of Neuroscience, 22, 455-463.
4. Bayer, S.A., Altman, J., Russo, R.J., & Zhang, X. (1993) Time-tables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology, 14, 83-144.
5. Blomgren, K., Zhu, C., Wang, X., Karlsson, J.O., Leverin, A.L., Bahr, B.A., Mallard, C., & Hagberg, H. (2001). Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia: a mechanism of 'pathological apoptosis'? Journal of Biological Chemistry, 276, 10191-10198.
6. Boksa, P. (2004). Animal models of obstetric complications in relation to schizophrenia. Brain Research Reviews, 45, 1-17.
7. Bona, E., Johansson, B.B., & Hagberg, H. (1997). Sensorimotor function and neuropathology five to six weeks after hypoxiaischemia in seven-day-old rats. Pediatric Research, 42, 678-683.
8. Cai, Z., Hutchins, J.B., & Rhodes, P.G. (1998). Intrauterine hypoxia-ischemia alters nitric oxide synthase expression and activity in fetal and neonatal rat brains. Developmental Brain Research, 109, 265-269.
9. Cai, Z., Xiao, F., Lee, B., Paul, I., & Rhodes P.G. (1999). Prenatal hypoxia-ischemia alters expression and activity of nitric oxide synthase in the young rat brain and causes learning deficits. Brain Research Bulletin, 49, 359-365.
10. Chou, I.-C., Trakht, T., Signori, C., Smith, J., Felt, B.T., Vazquez, D.M., & Barks, J.D.E. (2001). Behavioral/environmental intervention improves learning after cerebral hypoxiaischemia in rats. Stroke, 32, 2192-2197.
11. Crawley, J.N. (1999). What's wrong with my mouse? Behavioral phenotyping of transgenic and knockout mice. New York: Wiley-Liss.
12. Curristin, S.M., Cao, A., Stewart, M.B., Zhang, H., Madri, J.A., Morrow, J.S., & Ment, L.R. (2002). Disrupted synaptic development in the hypoxic newborn brain. Proceedings of the National Academy of Science, USA, 99, 15729-15734.
13. Decker, M.J., Hue, G.E., Caudle, W.M. Miller, G.W., Keating, G.L., & Rye, D.B. (2003). Episodic neonatal hypoxia evokes executive dysfunction and regionally specific alterations in markers of dopamine signaling. Neuroscience, 117, 417-425.
14. Dell'Anna, E., Geloso, M.C., Magarelli, M., & Molinari, M. (1996). Development of GABA and calcium binding proteins immunoreactivity in the rat hippocampus following neonatal anoxia. Neuroscience Letters, 211, 93-96.
15. Dicni, S., & Rees, S. (2003). Dendritic morphology is altered in hippocampal neurons following prenatal compromise. Journal of Neurobiology, 55, 41-52.
16. Du Plessis, A.J., & Volpe, J.J. (2002). Perinatal brain injury in the preterm and term newborn. Current Opinion in Neurology, 15, 151-157.
17. Farber, N.B., & Olney, J.W. (2003). Drugs of abuse that cause developing neurons to commit suicide. Developmental Brain Research, 147, 37-45.
18. Ferriero, D.M. (2005). Protecting neurons. Epilepsia, 46 Suppl. 7, 45-51.
19. Galvin, K.A., & Oorschot, D.E. (2003). 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, 118, 1023-1032.
20. Gerstein, M., Huleihel, M., Mane, R., Stilman, M., Kashtuzki, I., Hallak, M., & Golan, H. (2005). Remodeling of hippocampal gabaergic system in adult offspring after maternal hypoxia and magnesium sulfate load: immuno-histo-chernical study. Experimental Neurology, 196, 18-29.
21. Glass, T.F., Reeves, B., & Sharp, F.R. (2004). The impact of cxcitotoxic blockade on the evolution of injury following combined mechanical and hypoxic insults in primary rat neuronal culture. Neurobiology of Disease, 17, 378-384.
22. Golan, H., Kashtuzki, I., Hallak, M., Sorokin, Y., & Huleihel, M. (2004a). Maternal hypoxia during pregnancy induces fetal neurodevelopmental brain damage: partial protection by magnesium sulfate. Journal of Neuroscience Research, 78, 430-441.
23. Golan, H., Kashtutsky, I., Hallak, M., Sorokin, Y., & Huleihel, M. (2004b). Maternal hypoxia during pregnancy delays the development of motor reflexes in newborn mice. Developmental Neuroscience, 26, 24-29.
24. Graham, E.M., Sheldon, R.A., Flock, D.L., Ferriero, D.M., Martin, L.J., O'Riordan, D.P., & Northington, K.J. (2004). Neonatal mice lacking functional Fas death receptors are resistant to hypoxic-ischemic brain injury. Neurobiology of Disease, 17, 89-98.
25. Grojean, S., Pourié, G., Vert, P., & Daval, J.-L. (2003a). Differential neuronal fates in the Cal hippocampus after hypoxia in newborn and 7-day-old rats: effects of pre-treatment with MK-801. Hippocampus, 13, 970-977.
26. Grojean, S., Schroeder, H., Pourié, G., Charriaut-Marlangue, C., Koziel, V., Desor, D., Vert, P., & Davala, J.-L. (2003b). Histopathological alterations and functional brain deficits after transient hypoxia in the newborn rat pup: a long term follow-up. Neurobiology of Disease, 14, 265-278.
27. Han, B.H., D'Costa, A., Back, S.A., Parsadanian, M., Patel, S., Shah, AR., Gidday, J.M., Srinivasan, A., Deshmukh, M., & Holtzman, D.M. (2000). BDNF blocks caspase-3 activation in neonatal hypoxia-ischemia. Neurobiology of Disease, 7, 38-53.
28. Han, B.H., & Holtzman, D.M. (2000). BDNF protects the neonatal brain from hypoxic-ischemic injury in vivo via the ERK pathway. Journal of Neuroscience, 20, 5775-5781.
29. Herlenius, E., & Lagercrantz, H. (2004). Development of neurotransmitter systems during critical periods. Experimental Neurology, 190, S8-S21.
30. Hu, B.R., Liu, C.L., Ouyang, Y., Blomgren, K., & Siesjo, B.K. (2000). Involvement of caspasc-3 in cell death after hypoxiaischemia declines during brain maturation. Journal of Cerebral Blood Flow & Metabolism, 20, 1294-1300.
31. Hu, X., Nesic-Taylor, O., Qiu, J., Rea, H.C., Fabian, R., Rassin D.K., & Perez-Polo, J.R. (2005). Activation of nuclear factor-jB signaling pathway by interleukin-1 after hypoxia/ischemia in neonatal rat hippocampus and cortex. Journal of Neurochemistry, 93, 26-37.
32. Hu, X., Qiu, J., Grate, M.R., Rea, H.C., Rassin, D.K., & Perez-Polo, J.R. (2003). Bcl-2 family members make different contributions to cell death in hypoxia and/or hyperoxia in rat cerebral cortex. International Journal of Developmental Neuroscience, 21, 371-377.
33. Ishimaru, M.J., Ikonomidou, C., Tenkova, T.I., Der, T.C., Dikranian, K., Sesma, M.A., & Olney, J.W. (1999). Distinguishing excitotoxic from apoptotic neurodegeneration in the developing rat brain. Journal of Comparative Neurology, 408, 461-476.
34. Johnston, M.V. (1995). Neurotransmitters and vulnerability of the developing brain. Brain and Development, 17, 301-306.
35. Joseph, V., Mamet, J., Lee, F., Dalmaz, Y., & Van Reeth, O. (2002). Prenatal hypoxia impairs circadian synchronisation and response of the biological clock to light in adult rats. Journal of Physiology, 543 (1), 387-395.
36. Katsuragi, S., Ikeda, T., Date, I., Shingo, T., Yasuhara, T., Mishima, K., Aoo, N., Harada, K., Egashira, N., Iwasaki, K., Fujiwara, M., & Ikenoue, T. (2005). Implantation of encapsulated glial cell line-derived neurotrophic factor-secreting cells prevents long-lasting learning impairment following neonatal hypoxic-ischernic brain insult in rats. American Journal of Obstetrics and Gynecology, 192, 1028-1037.
37. Kawamura, M., Nakajima, W., Ishida, A., Ohmura, A., Miura, S., & Takada, G. (2005) Calpain inhibitor MDL 28170 protects hypoxic-ischemic brain injury in neonatal rats by inhibition of both apoptosis and necrosis. Brain Research, 1037, 59-69.
38. Kerr, J.F., Wyllie, A.H., & Currie, A.R. (1972). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. British Journal of Cancer, 26, 239-257.
39. Lee, H.T., Chang, Y.C., Wang, L.Y., Wang, S.T., Huang, C.C., & Ho, C.J. (2004). cAMP response element-binding protein activation in ligation preconditioning in neonatal brain. Annals of Neurology, 56, 611-623.
40. Liu, C.L., Siesjö, B.K., & Hu, B.R. (2004). Pathogenesis of hippocampal neuronal death after hypoxia-ischcmia changes during brain development. Neuroscience, 127, 113-123.
41. Lo, E.H, Steinberg, G.K., Panahian, N., Maidment, N.T., & Newcomb, R. (1993). Profiles of extracellular amino acid changes in focal cerebral ischacmia: effects of mild hypothermia. Neurology Research, 15, 281-287.
42. Loeliger, M., Watson, C.S., Reynolds, J.D., Penning, D.H., Harding, R., Bocking, A.D., & Rees, S.M. (2003). Extracellular glutamate levels and neuropathology in cerebral white matter following repeated umbilical cord occlusion in the near term fetal sheep. Neuroscience, 116, 705-714.
43. Lubics, A., Reglödi, D., Tamás, A., Kiss, P., Szalai, M., Szalontay, L., & Lengvári, I. (2005). Neurological reflexes and early motor behavior in rats subjected to neonatal hypoxic-ischemic injury. Behavioural Brain Research, 157, 157-165.
44. McQuillen, P.S., Sheldon, R.A., Shatz, C.J., & Ferriero, D.M. (2003). Selective vulnerability of subplate neurons after early neonatal hypoxia-ischemia. Journal of Neuroscience, 23, 3308-3315.
45. Mishima, K., Ikeda, T., Yoshikawa, T., Aooa, N., Egashira, N., Xia, Y.X., Ikenoue, T., Iwasaki, K., & Fujiwara, M. (2004). Effects of hypothermia and hyperthermia on attentional and spatial learning deficits following neonatal hypoxia-ischemic insult in rats. Behavioural Brain Research, 151, 209-217.
46. Nakajima, W., Ishida, A., Lange, M.S., Gabrielson, K.L., Wilson M.A., Martin, L.J., Blue, M.E., & Johnston, M.V. (2000). Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat. Journal of Neuroscience, 20, 7994-8004.
47. Northington, E.J., Ferriero, D.M., Flock, D.L., & Martin, L.J. (2001 a). Delayed neurodegeneration in neonatal rat thalamus after hypoxia-ischemia is apoptosis. Journal of Neuroscience, 21, 1931-1938.
48. Northington, F.J, Ferriero, D.M., & Martin L.J. (2001b). Neurodegeneration in the thalamus following neonatal hypoxia-ischemia is programmed cell death. Developmental Neuroscience, 23, 186-191.
49. Nyakas, C., Buwalda, B., & Luiten, P.G. (1996). Hypoxia and brain development. Progress in Neurobiology, 49, 1-51.
50. Nyakas, C., Buwalda, B., Markel, E., Korte, S.M., & Luiten, P.G. (1994). Life-spanning behavioural and adrenal dysfunction induced by prenatal hypoxia in the rat is prevented by the calcium antagonist nimodipine. European Journal of Neuroscience, 6, 746-753.
51. Perrin, D., Mamet, J., Scarna, H.L.N., Roux, J.C., Be'Rod, A., & Dalmaz, Y. (2004). Long-term prenatal hypoxia alters maturation of brain catecholaminergic systems and motor behavior in rats. Synapse, 54, 92-101.
52. Puka-Sundvall, M., Wallin, C., Gilland, H., Hallin, U., Wang, X., Sandberg, M., Karlsson, J.O., Blomgren, K., & Hagberg, H. (2000). Impairment of mitochondrial respiration after cerebral hypoxia-ischemia in immature rats: relationship to activation of caspase-3 and neuronal injury. Developmental Brain Research, 125, 43-50.
53. Qiu, J., Hu, X., Nesic, O., Grafe, M.R., Rassin, D.K., Wood, T.G., & Perez-Polo, J.R. (2004). Effects of NF-B oligonucleotide 'decoys' on gene expression in p7 rat hippocampus after hypoxia/ischemia. Journal of Neuroscience Research, 77, 108-118.
54. Ran, R., Xu, H., Lu A., Bernaudin, M., & Sharp, F.R. (2005). Hypoxia preconditioning in the brain. Developmental Neuroscience, 27, 87-92.
55. Ravishankar, S., Ashraf, Q.M., Fritz, K., Mishra, O.P., & Delivoria-Papadopoulos, M. (2001). Expression of Bax and Bcl-2 proteins during hypoxia in cerebral cortical neuronal nuclei of newborn piglets: effect of administration of magnesium sulfate. Brain Research, 901, 23-29.
56. Rice, J.E., Vannucci, R.C., & Brierley, J.B. (1981). The influence of immaturity on hypoxic-ischemic brain damage in the rat. Annals of Neurology, 9, 131-141.
57. Robinson, S., Petelenz, K., Li, Q., Cohen, M.L., DeChant, A., Tabrizi, N., Bucek, M., Lust, D., & Miller, R.H. (2005). Developmental changes induced by graded prenatal systemic hypoxic-ischemic insults in rats. Neurobiology of Disease, 18, 568-581.
58. Rodricksa, C.L., Rosea, I.A., Camma, E.J., Jenkina, G., Millera, S.L., & Gibbs, M.E. (2004). The effect of prenatal hypoxia and malnutrition on memory consolidation in the chick. Developmental Brain Research, 148, 113-119.
59. Roland, E.H., Poskitt, K., Rodriguez, E., Lupton, B.A., & Hill, A. (1998). Perinatal hypoxic-ischemic thalamic injury: clinical features and neuroimaging. Annals of Neurology, 44, 161-166.
60. Sheldona, R.A., Halla, J.J., Nobleb, L.J., & Ferriero D.M. (2001). Delayed cell death in neonatal mouse hippocampus from hypoxia-ischemia is neither apoptotic nor necrotic. Neuroscience Letters, 304, 165-168.
61. Sofroniew, M., Howe, C., & Mobley, W. (2001). Nerve growth factor signaling, neuroprotection, and neural repair. Annual Review of Neuroscience, 24, 677-736.
62. Tashima, L., Nakata, M., Anno, K., Sugino, N., & Kato, H. (2001). Prenatal influence of ischemia-hypoxia-induced intrauterine growth retardation on brain development and behavioral activity in rats. Biology Neonate, 80, 81-87.
63. Ten, V.S., Bradley-Moore, M., Gingrich, J.A., Stark, R.I., & Pinsky, D.J. (2003). Brain injury and neurofunctional deficit in neonatal mice with hypoxic-ischemic encephalopathy. Behavioural Brain Research, 145, 209-219.
64. Terrie, E.I., & Volpe, J.J. (2000). Mechanisms of perinatal brain injury. Seminars in Neonatology, 5, 3-16.
65. Tuor, U.I., Del Bigio, M.R., & Chumas, P.D. (1996). Brain damage due to cerebral hypoxia/ischemia in the neonate: pathology and pharmacological modification. Cerebrovascular & Brain Metabolism Review, 8, 159-193.
66. Van de Berg, W.D.J., Schmitz, C., Steinbusch, H.W.M., & Blanco, C.E. (2002). Perinatal asphyxia induced neuronal loss by apoptosis in the neonatal rat striatum: a combined TUNEL and stereological study. Experimental Neurology, 174, 29-36.
67. Van de Berg, W.D.J., Kwaijtaal, M., De Louw, A.J.A., Lissone, N.P.A., Schmitz, C., Faull, R.L.M., Blokland, A., Blanco, C.E., & Steinbusch, H.W.M. (2003). Impact of perinatal asphyxia on the GABAergic and locomotor system. Neuroscience, 117, 83-96.
68. Wagner, B.P., Nedelcu, J., & Martin, E. (2002). Delayed postischemic hypothermia improves long-term behavioral outcome after cerebral hypoxia-ischemia in neonatal rats. Pediatric Research, 51, 354-360.
69. Wei, X., Zhao, L., Ma, Z., Holtzman, D.M., Yan, C., Dodel, R.C., Hampel, H., Oertel, W., Farlow, M.R., & Du, Y. (2004). Caffeic acid phenethyl ester prevents neonatal hypoxic-ischaemic brain injury. Brain, 127, 2629-2635.
70. Wyllie, A.H. (1997). Apoptosis: an overview. British Medical Bulletin, 53, 451-465.
71. Zhuravin, I.A., Dubrovskaya, N.M., & Tumanova, N.L. (2004). Neuroscience and postnatal physiological development of rats after acute prenatal hypoxia. Behavioral Physiology, 34, 809-816.
72. Zornberg, G.L., Buka, S.L., & Tsuang, M.T. (2000). Hypoxic-ischemia-related fetal/neonatal complications and risk of schizophrenia and other nonaffective psychoses: a 19-year longitudinal study. American Journal of Psychiatry, 157, 196-202.