Chronic neonatal hypoxia leads to long term decreases in the volume and cell number of the rat cerebral cortex

Seminars in Perinatology

Volumn 28, Issue 6, 2004, Pages 379-388

  Schwartz, Michael L ^a   Vaccarino, Flora ^a,b   Chacon, Monica ^a   Li Yan, Wei ^a   Ment, Laura R ^a   Stewart, William B ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

apoptosis; cell death; cerebral cortex; corticogenesis; development; hypoxia

Indexed keywords

PROTEIN BAX; PROTEIN BCL 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN HYPOXIA; BRAIN OXYGEN TENSION; CELL COUNT; CELL SIZE; CELL TYPE; CELL VOLUME; CONTROLLED STUDY; GLIA CELL; LONG TERM EXPOSURE; MEDICAL ASSESSMENT; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NEWBORN; NONHUMAN; PERINATAL PERIOD; PREMATURE LABOR; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; REARING; ROOM TEMPERATURE; SPECIES COMPARISON; WESTERN BLOTTING;

EID: 11144349071     PISSN: 01460005     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.semperi.2004.10.009     Document Type: Review

References (84)

1. N.S. Wood, N. Marlow, K. Costeloe Neurologic and developmental disability after extremely preterm birth N Engl J Med 343 2000 378 384
2. M.B. Hack, D.J. Flannery, M. Schluchter Outcomes in young adulthood for very-low-birth-weight infants N Engl J Med 346 2002 149 157
3. M.C. Allen Developmental outcome of neonatal intensive care What questions are we asking? Curr Opin Pediatr 12 2000 116 122
4. NIH Consensus Development Panel on the Effect of Corticosteroids for Fetal Maturation on Perinatal Outcomes Effect of corticosteroids for fetal maturation on perinatal outcomes Obstet Gynecol 50 1995 505 507
5. B. Guyer, M.F. MacDorman, J.A. Martin Annual summary of vital statistics, 1997 Pediatrics 102 1998 1333 1349
6. B. Guyer, D.L. Hoyert, J.A. Martin Annual summary of vital statistics, 1998 Pediatrics 104 1999 1229 1246
7. J.L. Hutton, A.F. Colver, P.C. Mackie Effect of severity of disability on survival in north east England cerebral palsy cohort Arch Dis Child 83 2000 468 474
8. J.A. Pinto-Martin, A.H. Whitaker, J. Feldman Relation of cranial ultrasound abnormalities in low-birthweight infants to motor or cognitive performance at ages 2, 6 and 9 years Dev Med Child Neurol 41 1999 826 833
9. A.H. Whitaker, R. van Rossem, J.F. Feldman Psychiatric outcomes in low-birth-weight children at age 6 years Relation to neonatal cranial ultrasound abnormalities Arch Gen Psychiatry 54 1997 847 856
10. T. Salokorpi, T. Rautio, N. Sajaniemi Neurological development up to the age of four years of extremely low birthweight infants born in Southern Finland in 1991-94 Acta Paediatr 90 2001 218 221
11. L. Stigson, I. Kjellmer Serum levels of magnesium at birth related to complications of immaturity Acta Paediatr 86 1997 991 994
12. C. McCarton, J. Brooks-Gunn, I. Wallace Results at age 8 years of early intervention for low-birth-weight premature infants J Am Med Assoc 277 1997 126 132
13. M. McCormick, K. Workman-Daniels, J. Brooks-Gunn The behavioral and emotional well-being of school-age children with different birth weights Pediatrics 97 1996 18 25
14. K. Maxwell, J.A. Berliner, P.A. Cancilla Stimulation of glucoses analogue uptake by cerebral microvessel endothelial cells by a product released by astrocytes J Neuropathol 48 1989 69 80
15. P.S. Huppi, S.E.P. Maier, G.P. Zientara Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging Pediatr Res 44 1998 584 590
16. P.S. Huppi, S. Warfield, R. Kikinis Quantitative magnetic resonance imaging of brain development in premature and mature newborns Ann Neurol 43 1998 224 235
17. P.S. Huppi, F. Lazeyras Proton magnetic resonance spectroscopy (1H-MRS) in neonatal brain injury Pediatr Res 49 2001 317 319
18. P.S. Huppi, B. Murphy, S.E. Jaier Microstructural brain development after perinatal cerebral white matter injury assed by diffusion tensor magnetic resonance imaging Pediatrics 107 2001 455 460
19. J.J. Volpe Neurologic outcome of prematurity Arch Neurol 55 1998 297 300
20. J.J. Volpe Perinatal brain injury From pathogenesis to neuroprotection Ment Retard Dev Disabil Res Rev 7 2001 56 64
21. N. Paneth Classifying brain damage in preterm infants J Pediatr 134 1999 527 529
22. J.M. Perlman White matter injury in the preterm infant An important determination of abnormal neurodevelopmental outcome Early Hum Dev 53 1998 99 120
23. B. Vohr, L.R. Ment Intraventricular hemorrhage in the preterm infant Early Hum Dev 44 1996 1 16
24. M. Hack, L.L. Wright, S. Shankaran Very-low-birth-weight outcomes of the National Institute of Child Health and Human Development Neonatal Network, November 1989 to October 1990 Am J Obstet Gynecol 172 1995 457 464
25. B.R. Vohr, M.E. Msall Neuropsychological and functional outcomes of very low birth weight infants Semin Perinatol 21 1997 202 220
26. J.J. Volpe, P. Herscovitch, J.M. Perlman Positron emission tomography in the newborn Extensive impairment of regional cerebral blood flow with intraventricular hemorrhage and hemorrhagic intracerebral involvement Pediatrics 72 1983 589 601
27. J.M. Perlman, J.J. Volpe Cerebral blood flow velocity in relation to intraventricular hemorrhage in the premature newborn infant J Pediatr 100 1982 956 959
28. L.R. Ment, C.C. Duncan, R.A. Ehrenkranz Intraventricular hemorrhage of the preterm neonate Timing and cerebral blood flow changes J Pediatr 104 1984 419 425
29. M. Hack, A.A. Fanaroff Outcomes of children of extremely low birth-weight and gestational age in the 1990's Early Hum Dev 53 1999 193 218
30. A.L. Stewart, L. Rifkin, P.N. Amess Brain structure and neurocognitive and behavioural function in adolescents who were born very preterm Lancet 353 1999 1653 1657
31. L.R. Ment, B. Vohr, W. Allan The etiology and outcome of cerebral ventriculomegaly at term in very low birth weight preterm infants Pediatrics 104 1999 210 215
32. B.S. Peterson, G. Vohr, C.J. Cannistraci Regional brain volume abnormalities and long-term cognitive outcome in preterm infants J Am Med Assoc 284 2000 1939 1947
33. P.R. Huttenlocher, C. de Courten, L.J. Garey Synaptogenesis in human visual cortex-evidence for synapse elimination during normal development Neurosci Lett 33 1982 247 252
34. I. Kostovic, P. Rakic Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain J Comp Neurol 297 1990 441 470
35. J. Dobbing Undernutrition and the developing brain The use of animal models to elucidate the human problem Psychiatr Neurol Neurochir 74 1971 433-422
36. L.A. Rothblat, L.L. Hayes Age-related changes in the distribution of visual callosal neurons following monocular enucleation in the rat Brain Res 246 1982 146 149
37. J. Olavarria, R.C. Van Sluyters Organization and postnatal development of callosal connections in the visual cortex of the rat J Comp Neurol 239 1985 1 26
38. I. Ferrer, E. Soriano, J.A. DelRio Cell death and removal in the cerebral cortex during development Prog Neurobiol 39 1992 1 43
39. C. Malinak, F.S. Silverstein Hypoxic-ischemic injury acutely disrupts microtubule-associated protein 2 immunostaining in neonatal rat brain Biol Neonate 69 1996 257 267
40. L.R. Ment, M. Schwartz, R.W. Makuch Association of chronic sublethal hypoxia with ventriculomegaly in the developing rat brain Dev Brain Res 111 1998 197 203
41. P.S. Huppi, B. Schuknecht, C. Boesch Structural and neurobehavioral delay in postnatal brain development of preterm infants Pediatr Res 39 1996 895 901
42. B.P. Murphy, T.E. Inder, P.S. Huppi Impaired cerebral cortical gray matter growth after treatment with dexamethasone for neonatal chronic lung disease Pediatrics 107 2001 217 221
43. H.J.G. Gundersen, P. Bagger, T.F. Bendtse The new stereological tools Dissector, fractionator, nucleator and point sampled intercepts and their uses in pathological research and diagnosis APMIS 96 1988 857 881
44. H.J. Gundersen, T.F. Bendtsen, L. Korbo Some new, simple and efficient stereological methods and their use in pathological research and diagnosis [Review] APMIS 96 1988 379 394
45. M.J. West, L. Slomianka, H.J. Gundersen Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator Anat Rec 231 1991 482 497
46. F.M. Vaccarino, M.L. Schwartz, R. Raballo Changes in the size of the cerebral cortex are governed by fibroblast growth factor during embryogenesis Nat Neurosci 2 1999 246 253
47. L.R. Ment, M.L. Schwartz, R.W. Makuch Association of chronic sublethal hypoxia with ventriculomegaly in the developing rat brain Dev Brain Res 760 1998 197 203
48. L.R. Ment, G.G. Haddad, J.A. Madri Adaptive mechanisms in developing brain. I. Neuropathology Ann Neurol 38 1995 521
49. D.M. Holtzman, R.A. Sheldon, W. Jaffe Nerve growth factor protects the neonatal brain against hypoxic-ischemic injury Ann Neurol 39 1996 114 122
50. K. Muramatsu, R.A. Sheldon, S.M. Black Nitric oxide synthase activity and inhibition after neonatal hypoxia ischemia in the mouse brain Brain Res Dev Brain Res 123 2000 119 127
51. R.A. Sheldon, C. Sedik, D.M. Ferriero Strain-related brain injury in neonatal mice subjected to hypoxia-ischemia Brain Res 810 1998 114 122
52. K. Hasegawa, H. Yoshioka, T. Sawada Lipid peroxidation in neonatal mouse brain subjected to two different types of hypoxia Brain Dev 13 1991 101 103
53. J. Uematsu, K. Ono, T. Yamano Development of corticospinal tract fibers and their plasticity. I. Quantitative analysis of the developing corticospinal tract in mice Brain Dev 18 1996 29 34
54. J. Uematsu, K. Ono, T. Yamano Development of corticospinal tract fibers and their plasticity. II. Neonatal unilateral cortical damage and subsequent development of the corticospinal tract in mice Brain Dev 18 1996 173 178
55. I. Ferrer, E. Soriano, J.A. Delrio Cell death and removal in the cerebral cortex during development Prog Neurobiol 39 1992 1 43
56. P. Rakic, J.-P. Bourgeois, M.F. Eckenhoff Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex Science 232 1986 232 235
57. N. Zecevic, J.-P. Bourgeois, P. Rakic Changes in synaptic density in motor cortex of rhesus monkey during fetal and postnatal life Dev Brain Res 50 1989 11 32
58. M.E. Blue, J.G. Parnavelas The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis J Neurocytol 12 1983 697 712
59. G.M. Innocenti Growth and reshaping of axons in the establishment of visual callosal connections Science 218 1981 824 827
60. D.J. Price, C. Blakemore Regressive events in the postnatal development of association projections in the visual cortex Nature 316 1985 721 724
61. S.A. Bayer, J. Altman Neocortical Development 1991 Raven New York
62. D. Heumann, G. Leuba Neuronal death in the developing and aging of the cerebral cortex of the mouse Neuropathol Appl Neurobiol 9 1982 297 311
63. I. Ferrer, E. Bernet, E. Soriano Naturally occurring cell death in the cerebral cortex of the rat and removal of dead cells by transitory phagocytes Neuroscience 39 1990 451 458
64. E. Castren, Y. Ohga, M.P. Berzaghi bcl-2 messenger RNA is localized in neurons of the developing and adult rat brain Neuroscience 61 1994 165 177
65. S. Jaw, D. Su, D. Truong Expression of Bcl-2 and Bax in the frontoparietal cortex of the rat following cardiac arrest Brain Res Bull 38 1995 577 580
66. H. Frankowski, M. Missotten, P.A. Fernandez Function and expression of the Bcl-x gene in the developing and adult nervous system Neuroreport 6 1995 1917 1921
67. T.P. Yamaguchi, K. Harpal, M. Henkemeyer fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation Genes Dev 8 1994 3032 3044
68. F. Gillardon, H. Wickert, M. Zimmermann Up-regulation of bax and down-regulation of bcl-2 is associated with kainate-induced apoptosis in mouse brain Neurosci Lett 192 1995 85 88
69. M.D. Jacobsen, M.C. Raff Programmed cell death and Bcl-2 protection in very low oxygen Nature 374 1995 814 816
70. S. Shimizu, Y. Eguchi, H. Kosaka Prevention of hypoxia-induced cell death by Bcl-2 and bcl-xL Nature 374 1995 811 813
71. T.G. Graeber, C. Osmanian, T. Jacks Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumors Nature 379 1996 88 91
72. H. Okazawa, J. Shimuzi, M. Kamei Bcl-2 inhibits retinoic acid-induced apoptosis during the neural differentiation of embryonal stem cells J Cell Biol 132 1996 955 968
73. G. Nunez, L. London, D. Hockenberry Deregulated bcl-2 gene expression selectively prolongs survival of growth factor-deprived hemopoietic cell lines J Immunol 144 1990 3602 3610
74. A. Hara, T. Iwai, M. Niwa Immunohistochemical detection of bax and bcl-2 proteins in gerbil hippocampus following transient forebrain ischemia Brain Res 711 1996 249 253
75. S. Krajewski, J. Mai, M. Krajewska Upregulation of bax protein levels in neurons following cerebral ischemia J Neurosci 15 1995 6364 6376
76. K. Herrup, J.C. Busser The induction of multiple cell cycle events precedes target-related neuronal death Development 121 1995 2385 2395
77. D. Thomaidou, M.C. Mione, J.F. Cavanagh Apoptosis and its relation to the cell cycle in the developing cerebral cortex J Neurosci 17 1997 1075 1085
78. A. Copani, D. Uberti, A.M. Sortino Activation of cell-cycle-associated proteins in neuronal death A mandatory or dispensable path? Trends Neurosci 21 2001 25 31
79. J. Busser, D.S. Geldmacher, K. Herrup Ectopic cell cycle proteins predict the sites of neuronal cell death in alzheimer's disease brain J Neurosci 18 1998 2801 2807
80. S.A. Back, B.H. Han, N.L. Luo Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia J Neurosci 22 2002 455 463
81. S.A. Back, N.L. Luo, N.S. Borenstein Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury J Neurosci 21 2001 1302 1312
82. S.A. Back, X.-D. Gan, Y. Li Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion J Neurosci 18 1998 6241 6253
83. W. Nakajima, A. Ishida, M.S. Lange Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat J Neurosci 20 2000 7994 8004
84. F. Doetsch, I. Caille, D.A. Lim Subventricular zone astrocytes are neural stem cells in the adult mammalian brain Cell 97 1999 703 716