Brain damage in preterm newborns: Might enhancement of developmentally regulated endogenous protection open a door for prevention?

Pediatrics

Volumn 104, Issue 3 I, 1999, Pages 541-550

  Dammann, Olaf ^a   Leviton, Alan ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Brain development; Cell protection; Infant; Oligodendrocytes; Premature

Indexed keywords

CYTOKINE; GROWTH FACTOR;

ARTICLE; BRAIN DEVELOPMENT; BRAIN INJURY; BRAIN PROTECTION; CELL PROTECTION; HUMAN; OLIGODENDROGLIA; PREMATURITY; PRIORITY JOURNAL; WHITE MATTER;

BRAIN DAMAGE, CHRONIC; CYTOKINES; GROWTH SUBSTANCES; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; INFANT, PREMATURE, DISEASES; MODELS, BIOLOGICAL; OLIGODENDROGLIA;

EID: 0032881633     PISSN: 00314005     EISSN: None     Source Type: Journal    
DOI: 10.1542/peds.104.3.541     Document Type: Article

References (187)

1. Claris O, Besnier S, Lapillonne A, Picaud JC, Salle BL. Incidence of ischemic-hemorrhagic cerebral lesions in premature infants of gestational age ≤28 weeks: a prospective ultrasound study. Biol Neonate. 1996;70:29-34
2. Berkowitz GS, Papiernik E. Epidemiology of preterm birth. Epidemiol Rev. 1993;15:414-443
3. Hagberg B, Hagberg G, Glow I, van Wendt L. The changing panorama of cerebral palsy in Sweden. VII. Prevalence and origin in the birth year period 1987-90. Acta Paediatr. 1996;85:954-960
4. Goldenberg RL, Rouse DJ. Prevention of premature birth. N Engl J Med. 1998;339:313-320
5. Kuban KC, Leviton A. Cerebral palsy. N Engl J Med. 1994;330:188-195
6. Leviton A, Paneth N. White matter damage in preterm newborns - an epidemiologic perspective. Early Hum Dev. 1990;24:1-22
7. Govaert P, DeVries LS. An atlas of neonatal brain sonography. In: Clinics in Developmental Medicine, Volume 141/142. London, United Kingdom: Mac Keith; 1997
8. Paneth N, Rudelli R, Kazam E, Monte W. Brain damage in the preterm infant. In: Clinics in Developmental Medicine, Volume 131. London, United Kingdom: Mac Keith; 1994
9. Kuban KC. White-matter disease of prematurity, periventricular leukomalacia, and ischemic lesions. Dev Med Child Neurol. 1998;40:571-573
10. Banker BQ, Larroche JC. Periventricular leukomalacia of infancy. Arch Neurol. 1962;7:386-410
11. Crawford CL, Hobbs MJ. Anatomy of diplegia: an hypothesis. Dev Med Child Neurol. 1994;36:513-517
12. Gilles FH, Murphy SF. Perinatal telencephalic leucoencephalopathy. J Neurol Neurosurg Psychiatry. 1969;32:404-413
13. O'Shea TM, Klinepeter KL, Dillard RG. Prenatal events and the risk of cerebral palsy in very low birth weight infants. Am J Epidemiol. 1998; 147:362-369
14. Pinto-Martin JA, Riolo S, Cnaan A, Holzman C, Susser MW, Paneth N. Cranial ultrasound prediction of disabling and nondisabling cerebral palsy at age two in a low birth weight population. Pediatrics. 1995;95: 249-254
15. Holling EE, Leviton A. Characteristics of cranial ultrasound white matter echolucencies that predict disability: a review. Dev Med Child Neurol. 1999;41:136-139
16. Allan WC, Vohr B, Makuch RW, Katz KH, Ment LR. Antecedents of cerebral palsy in a multicenter trial of indomethacin for intraventricular hemorrhage. Arch Pediatr Adolesc Med. 1997;151:580-585
17. Aziz K, Vickar DB, Sauve RS, Etches PC, Pain KS, Robertson CM. Province-based study of neurologic disability of children weighing 500 through 1249 grams at birth in relation to neonatal cerebral ultrasound findings. Pediatrics. 1995;95:837-844
18. Leviton A, Gilles F. Ventriculomegaly, delayed myelination, white matter hypoplasia, and "periventricular" leukomalacia: how are they related? Pediatr Neurol. 1996;15:127-136
19. Leviton A, Gilles FH. Morphologic abnormalities in human infant cerebral white matter related to gestational and postnatal age. Pediatr Res. 1974;8:718-720
20. Adinolfi M. The development of the human blood-CSF-brain barrier. Dev Med Child Neurol. 1985;27:532-537
21. Davison AN, Dobbing J. Myelination as a vulnerable period in brain development. Br Med Bull. 1966;22:40-44
22. Goldman JE. Regulation of oligodendrocyte differentiation. Trends Neurosci. 1992;15:359-362
23. Gilles FH, Shankle W, Dooling EC. Myelinated tracts: growth patterns. In: Gilles FH, Leviton A, Dooling EC, eds. The Developing Human Brain. Growth and Epidemiologic Neuropathology. Boston, MA: John Wright; 1983:117-183
24. Allen MC, Donohue PK, Dusman AE. The limit of viability - neonatal outcome of infants born at 22 to 25 weeks' gestation. N Engl J Med. 1993;329:1597-1601
25. McMorris FA, McKinnon RD. Regulation of oligodendrocyte development and CNS myelination by growth factors: prospects for therapy of demyelinating disease. Brain Pathol 1996;6:313-329
26. Reuss ML, Paneth N, Susser M. Does the loss of placental hormones contribute to neurodevelopmental disabilities in preterm infants? Dev Med Child Neurol. 1994;36:743-747
27. Raff MC, Barres BA, Burne JF, Coles HS, Ishizaki Y, Jacobson MD. Programmed cell death and the control of cell survival: lessons from the nervous system. Science. 1993;262:695-700
28. Kitagawa H, Hayashi T, Mitsumoto Y, Koga N, Itoyama Y, Abe K. Reduction of ischemic brain injury by topical application of glial cell line-derived neurotrophic factor after permanent middle cerebral artery occlusion in rats. Stroke. 1998;29:1417-1422
29. Martin LJ, Al-Abdulla NA, Brambrink AM, Kirsch JR, Sieber FE, Portera-Cailliau C. Neurodegeneration in excitotoxicity, global cerebral ischemia, and target deprivation: a perspective on the contributions of apoptosis and necrosis. Brain Res Bull. 1998;46:281-309
30. Matsushita K, Matsuyama T, Kitagawa K, Matsumoto M, Yanagihara T, Sugita M. Alterations of Bcl-2 family proteins precede cytoskeletal proteolysis in the penumbra, but not in infarct centres following focal cerebral ischemia in mice. Neuroscience. 1998;83:439-448
31. Johnson J, Oppenheim R. Neurotrophins. Keeping track of changing neurotrophic theory. Curr Biol. 1994;4:662-665
32. Raff MC. Social controls on cell survival and cell death. Nature. 1992; 356:397-400
33. Finklestein SP. The potential use of neurotrophic growth factors in the treatment of cerebral ischemia. Adv Neurol. 1996;71:413-417
34. Gard AL, Burrell MR, Pfeiffer SE, Rudge JS, Williams WC II. Astroglial control of oligodendrocyte survival mediated by PDGF and leukemia inhibitory factor-like protein. Development. 1995;121:2187-2197
35. Cohen RI, Marmur R, Norton WT, Mehler MF, Kessler JA. Nerve growth factor and neurotrophin-3 differentially regulate the proliferation and survival of developing rat brain oligodendrocytes. J. Neurosci. 1996;16:6433-6442
36. Holtzman DM, Sheldon RA, Jaffe W, Cheng Y, Ferriero DM. Nerve growth factor protects the neonatal brain against hypoxic-ischemic injury. Ann Neurol. 1996;39:114-122
37. Barres BA, Schmid R, Sendtner M, Raff MC. Multiple extracellular signals are required for long-term oligodendrocyte survival. Development. 1993;118:283-295
38. Leviton A, Paneth N, Reuss ML, et al. Hypothyroxinemia of prematurity and the risk of cerebral white matter damage. J Pediatr. 1999;134: 706-711
39. Reuss ML, Paneth N, Pinto-Martin JA, Lorenz JM, Susser M. The relation of transient hypothyroxinemia in preterm infants to neurologic development at two years of age. N Engl J Med. 1996;334:821-827
40. Salokorpi T, Sajaniemi N, Hällback H, Kari A, Rita H, von Wendt L. Randomized study of the effect of antenatal dexamethasone on growth and development of premature children at the corrected age of 2 years. Acta Paediatr. 1997;86:294-298
41. Pasquini JM, Adamo AM. Thyroid hormones and the central nervous system. Dev Neurosci. 1994;16:1-8
42. Barres BA, Lazar MA, Raff MC. A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development. 1994;120:1097-1108
43. Tosic M, Torch S, Comte V, Dolivo M, Honegger P, Mathieu JM. Triiodothyronine has diverse and multiple stimulating effects on expression of the major myelin protein genes. J Neurochem. 1992;59: 1770-1777
44. Walter IB. Triiodothyronine exerts a tropic action on rat sensory neuron survival and neurite outgrowth through different pathways. Eur J Neurosci. 1996;8:455-466
45. Heisenberg CP, Thoenen H, Lindholm D. Tri-iodothyronine regulates survival and differentiation of rat cerebellar granule neurons. Neuroreport. 1992;3:685-688
46. Filipcik P, Saito H, Katsuki H. 3,5,3′-L-triiodothyronine promotes survival and axon elongation of embryonic rat septal neurons. Brain Res. 1994;647:148-152
47. Benigni F, Villa P, Demitri MT, et al. Ciliary neurotrophic factor inhibits brain and peripheral tumor necrosis factor production and, when coadministered with its soluble receptor, protects mice from lipopolysaccharide toxicity. Mol Med. 1995;1:568-575
48. Leviton A. Preterm birth and cerebral palsy: is tumor necrosis factor the missing link? Dev Med Child Neural. 1993;35:553-558
49. Mocchetti I, Spiga G, Hayes VY, Isackson PJ, Colangelo A. Glucocorticoids differentially increase nerve growth factor and basic fibroblast growth factor expression in the rat brain. J Neurosci. 1996;16:2141-2148
50. Crossin KL, Tai MH, Krushel LA, Mauro VP, Edelman GM. Glucocorticoid receptor pathways are involved in the inhibition of astrocyte proliferation. Proc Natl Acad Sci U S A. 1997;94:2687-2692
51. McRae A, Bona E, Hagberg H. Microglia-astrocyte interactions after cortisone treatment in a neonatal hypoxia-ischemia model. Brain Res Dev Brain Res. 1996;94:44-51
52. Chao CC, Hu S, Sheng WS, Bu D, Bukrinsky MI, Peterson PK. Cytokine-stimulated astrocytes damage human neurons via a nitric oxide mechanism. Glia. 1996;16:276-284
53. Cheung PT, Wu J, Banach W, Chernausek SD. Glucocorticoid regulation of an insulin-like growth factor-binding protein-4 protease produced by a rat neuronal cell line. Endocrinology. 1994;135:1328-1335
54. Lee WH, Wang GM, Seaman LB, Vannucci SJ. Coordinate IGF-I and IGFBP5 gene expression in perinatal rat brain after hypoxia-ischemia. J Cereb Blood Flow Metab. 1996;16:227-236
55. McMorris FA, Mozell RL, Carson MJ, Shinar Y, Meyer RD, Marchetti N. Regulation of oligodendrocyte development and central nervous system myelination by insulin-like growth factors. Ann N Y Acad Sci. 1993;692:321-334
56. Miller RH. Oligodendrocyte origins. Trends Neurosci. 1996;19:92-96
57. Sternberg EM. Neural-immune interactions in health and disease. J Clin Invest. 1997;100:2641-2647
58. Mayer M, Bhakoo K, Noble M. Ciliary neurotrophic factor and leukemia inhibitory factor promote the generation, maturation and survival of oligodendrocytes in vitro. Development. 1994;120:143-153
59. Bertollini L, Ciotti MT, Cherubini E, Cattaneo A. Neurotrophin-3 promotes the survival of oligodendrocyte precursors in embryonic hippocampal cultures under chemically defined conditions. Brain Res. 1997;746:19-24
60. Barres BA, Burne JF, Holtmann B, Thoenen H, Sendtner M, Raff MC. Ciliary neurotrophic factor enhances the rate of oligodendrocyte generation. Mol Cell Neurosci. 1996;8:146-156
61. Raff MC, Lillien LE, Richardson WD, Burne JF, Noble MD. Platelet-derived growth factor from astrocytes drives the clock that times oligodendrocyte development in culture. Nature. 1988;333:562-565
62. Noble M, Murray K, Stroobant P, Waterfield MD, Riddle P. Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature. 1988;333:560-562
63. Richardson WD, Pringle N, Mosley MJ, Westermark B, Dubois-Dalcq M. A role for platelet-derived growth factor in normal gliogenesis in the central nervous system. Cell. 1988;53:309-319
64. Bögler O, Wren D, Barnett SC, Land H, Noble M. Cooperation between two growth factors promotes extended self-renewal and inhibits differentiation of oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells. Proc Natl Acad Sci U S A. 1990;87:6368-6372
65. Milner R, Anderson HJ, Rippon RF, et al. Contrasting effects of mitogenic growth factors on oligodendrocyte precursor cell migration. Glia. 1997;19:85-90
66. Barres BA, Hart IK, Coles HSR, et al. Cell death and control of cell survival in the oligodendrocyte lineage. Cell. 1992;70:31-64
67. McKinnon RD, Matsui T, Dubois-Dalcq M, Aaronson SA. FGF modulates the PDGF-driven pathway of oligodendrocyte development. Neuron. 1990;5:603-614
68. Mayer M, Bögler O, Noble M. The inhibition of oligodendrocytic differentiation of O-2A progenitors caused by basic fibroblast growth factor is overridden by astrocytes. Glia. 1993;8:12-19
69. Mito T, Konomi H, Houdou S, Takashima S. Immunohistochemical study of the vasculature in the developing brain. Pediatr Neurol. 1991; 7:18-22
70. Gillespie GY. Cytokines as modulators of malignant glioma progression. In: Ransohoff RM, Benveniste EN, eds. Cytokines and the CNS. Boca Raton, FL: CRC Press; 1996
71. Volpe JJ. Neurology of the Newborn. Philadelphia, PA: Saunders; 1995
72. Painter MJ. Animal models of perinatal asphyxia: contributions, contradictions, clinical relevance. Semin Pediatr Neurol. 1995;2:37-56
73. Gunn AJ, de Haan HH, Gluckman PD. Experimental models of perinatal brain injury. In: Stevenson DK, Sunshine P, eds. Fetal and Neonatal Brain Injury. Mechanisms, Management, and the Risk of Practice. Oxford, United Kingdom: Oxford University Press; 1997
74. Hagberg H, Bona E, Gilland E, Puka-Sundvall M. Hypoxia-ischaemia model in the 7-day-old rat: possibilities and shortcomings. Acta Paediatr Suppl. 1997;422:85-88
75. Yoshioka H, Goma H, Nioka S, et al. Bilateral carotid artery occlusion causes periventricular leukomalacia in neonatal dogs. Brain Res Dev Brain Res. 1994;78:273-278
76. Palmer C. Hypoxic-ischemic encephalopathy. Therapeutic approaches against microvascular injury, and role of neutrophils, PAF, and free radicals. Clin Perinatol. 1995;22:481-517
77. Dammann O, Leviton A. Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr Res. 1997;42:1-8
78. Dammann O, Leviton A. Infection remote from the brain, neonatal white matter damage, and cerebral palsy in the preterm infant. Semin Pediatr Neurol. 1998;5:190-201
79. Leviton A, Gilles FH. An epidemiologic study of perinatal telencephalic leucoencephalopathy in an autopsy population. J Neurol Sci. 1973;18:53-66
80. Leviton A, Gilles F, Neff R, Yaney P. Multivariate analysis of risk of perinatal telencephalic leucoencephalopathy. Am J Epidemiol. 1976;104: 621-626
81. Gilles FH, Leviton A, Kerr CS. Endotoxin leucoencephalopathy in the telencephalon of the newborn kitten. J Neurol Sci. 1976;27:183-191
82. Gilles FH, Averill DR Jr, Kerr CS. Neonatal endotoxin encephalopathy. Ann Neurol. 1977;2:49-56
83. Young RSK, Hernandez MJ, Yagel SK. Selective reduction of blood flow to white matter during hypotension in newborn dogs: a possible mechanism of periventricular leukomalacia. Ann Neurol. 1982;12: 445-448
84. Young RS, Yagel SK, Towfighi J. Systemic and neuropathologic effects of E coli endotoxin in neonatal dogs. Pediatr Res. 1983;17:349-353
85. Ornoy A, Altshuler G. Maternal endotoxemia, fetal anomalies, and central nervous system damage: a rat model of a human problem. Am J Obstet Gynecol. 1976;124:196-204
86. Yoon BH, Kim CJ, Romero R, et al. Experimentally induced intrauterine infection causes fetal brain white matter lesions in rabbits. Am J Obstet Gynecol. 1997;177:797-802
87. Anderson CA, Higgins RJ, Smith ME, Osburn BI. Border disease. Virus-induced decrease in thyroid hormone levels with associated hypomyelination. Lab Invest. 1987;57:168-175
88. Anderson CA, Sawyer M, Higgins RJ, East N, Osburn BI. Experimentally induced ovine border disease: extensive hypomyelination with minimal viral antigen in neonatal spinal cord. Am J Vet Res. 1987;48: 499-503
89. Hewicker-Trautwein M, Trautwein G. Porencephaly, hydranencephaly and leukoencephalopathy in ovine fetuses following transplacental infection with bovine virus diarrhoea virus: distribution of viral antigen and characterization of cellular response. Acta Neuropathol (Berl). 1994;87:385-397
90. Silverstein FS, Barks JDE, Hagan P, Liu XH, Ivacko J, Szaflarski J. Cytokines and perinatal brain injury. Neurochem Int. 1997;30:375-383
91. Romero R, Manogue KR, Mitchell MD, et al. Infection and labor. IV. Cachectin-tumor necrosis factor in the amniotic fluid of women with intraamniotic infection and preterm labor. Am J Obstet Gynecol. 1989; 161:336-341
92. Yoon BH, Jun JK, Romero R, et al. Amniotic fluid inflammatory cytokines (interleukin-6, interleukin-1β, and tumor necrosis factor-α), neonatal brain white matter lesions, and cerebral palsy. Am J Obstet Gynecol. 1997;177:19-26
93. Yoon BH, Romero R, Yang SH, et al. Interleukin-6 concentrations in umbilical cord plasma are elevated in neonates with white matter lesions associated with periventricular leukomalacia. Am J Obstet Gynecol. 1996;174:1433-1440
94. Deguchi K, Mizuguchi M, Takashima S. Immunohistochemical expression of tumor necrosis factor alpha in neonatal leukomalacia. Pediatr Neurol. 1996;14:13-16
95. Deguchi K, Oguchi K, Takashima S. Characteristic neuropathology of leukomalacia in extremely low birth weight infants. Pediatr Neurol. 1997;16:296-300
96. Yoon BH, Romero R, Kim CJ, et al. High expression of tumor necrosis factor-alpha and interleukin-6 in periventricular leukomalacia. Am J Obstet Gynecol. 1997;177:406-411
97. Gomez R, Romero R, Ghezzi F, Yoon BH, Mazor M, Berry SM. The fetal inflammatory response syndrome. Am J Obstet Gynecol. 1998;179: 194-202
98. Romero R, Gomez R, Ghezzi F, et al. A fetal systemic inflammatory response is followed by the spontaneous onset of preterm parturition. Am J Obstet Gynecol. 1998;179:186-193
99. Berner R, Niemeyer CM, Leititis JU, et al. Plasma levels and gene expression of granulocyte colony-stimulating factor, tumor necrosis factor-alpha, interleukin (IL)-1beta, IL-6, IL-8, and soluble intercellular adhesion molecule-1 in neonatal early onset sepsis. Pediatr Res. 1998; 44:469-477
100. Selmaj KW, Raine CS. Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann Neurol. 1988;23:339-346
101. Zajicek JP, Wing M, Scolding NJ, Compston DA. Interactions between oligodendrocytes and microglia. A major role for complement and tumour necrosis factor in oligodendrocyte adherence and killing. Brain. 1992;115:1611-1631
102. Louis JC, Magal E, Takayama S, Varon S. CNTF protection of oligodendrocytes against natural and tumor necrosis factor-induced death. Science. 1993;259:689-692
103. D'Souza SD, Alinauskas KA, Antel JP. Ciliary neurotrophic factor selectively protects human oligodendrocytes from tumor necrosis factor-mediated injury. J Neurosci Res. 1996;43:289-298
104. Kahn MA, de Vellis J. Growth factors in the CNS and their effects on oligodendroglia. Prog Brain Res. 1995;105:145-169
105. Kahn MA, de Vellis J. Regulation of an oligodendrocyte progenitor cell line by the interleukin-6 family of cytokines. Glia. 1994;12:87-98
106. Jones CA, Cayabyab RG, Kwong KY, et al. Undetectable interleukin (IL)-10 and persistent IL-8 expression early in hyaline membrane disease: a possible developmental basis for the predisposition to chronic lung inflammation in preterm newborns. Pediatr Res. 1996;39: 966-975
107. Küster H, Weiss M, Willeitner AE, et al. Interleukin-1 receptor antagonist and interleukin-6 for early diagnosis of neonatal sepsis 2 days before clinical manifestation. Lancet. 1998;352:1271-1277
108. Romero R, Tartakovsky B. The natural interleukin-1 receptor antagonist prevents interleukin-1-induced preterm delivery in mice. Am J Obstet Gynecol. 1992;167:1041-1045
109. Hagberg H, Gilland E, Bona E, et al. Enhanced expression of interleukin (IL)-1 and IL-6 messenger RNA and bioactive protein after hypoxia-ischemia in neonatal rats. Pediatr Res. 1996;40:603-609
110. Loddick SA, Rothwell NJ. Neuroprotective effects of human recombinant interleukin-1 receptor antagonist in focal cerebral ischaemia in the rat. J Cereb Blood Flow Metab. 1996;16:932-940
111. Shi Y, Li HQ, Shen CK, et al. Association between protective efficacy of antibodies to tumor necrosis factor and suppression of nitric oxide production in neonatal rats with fatal infection. Pediatr Res. 1993;34: 345-348
112. Fisher CJJ Jr, Agosti JM, Opal SM, et al. Treatment of septic shock with the tumor necrosis factor receptor:fc fusion protein. N Engl J Med. 1996;334:1697-1702
113. Grau GE, Maennel DN. TNF inhibition and sepsis - sounding a cautionary note. Nat Med. 1997;3:1193-1195
114. Pringle AK, Sundstrom LE, Wilde GJ, Williams LR, Iannotti F. Brain-derived neurotrophic factor, but not neurotrophin-3, prevents ischaemia-induced neuronal cell death in organotypic rat hippocampal slice cultures. Neurosci Lett. 1996;211:203-206
115. Cheng Y, Gidday JM, Yan Q, Shah AR, Holtzman DM. Marked age-dependent neuroprotection by brain-derived neurotrophic factor against neonatal hypoxic-ischemic brain injury. Ann Neurol. 1997;41: 521-529
116. Bejar R, Wozniak P, Allard M, et al. Antenatal origin of neurologic damage in newborn infants. I. Preterm infants. Am J Obstet Gynecol. 1988;159:357-363
117. de Vries LS, Eken P, Groenendaal F, Rademaker KJ, Hoogervorst B, Bruinse HW. Antenatal onset of haemorrhagic and/or ischaemic lesions in preterm infants: prevalence and associated obstetric variables. Arch Dis Child Fetal Neonatal Ed. 1998;78:F51-F56
118. van Wassenaer AG, Kok JH, de Vijlder JJ, et al. Effects of thyroxine supplementation on neurologic development in infants born at less than 30 weeks' gestation. N Engl J Med. 1997;336:21-26
119. Crowther CA, Hiller JE, Haslam RR, Robinson JS, and the ACTOBAT Study Group. Australian Collaborative Trial of Antenatal Thyrotropin-Releasing Hormone: adverse effects at 12-month follow-up. Pediatrics. 1997;99:311-317
120. Den Ouden AL, Kok JH, Verkerk PH, Brand R, Verloove-Vanhorick SP. The relation between neonatal thyroxine levels and neurodevelopmental outcome at age 5 and 9 years in a national cohort of very preterm and/or very low birth weight infants. Pediatr Res. 1996;39: 142-145
121. Warringa RAJ, Hoeben RC, Koper JW, Sykes JEC, van Golde LMG, Lopes-Cardozo M. Hydrocortisone stimulates the development of oligodendrocytes in primary glial cultures and affects glucose metabolism and lipid synthesis in these cultures. Dev Brain Res. 1987;34:79-86
122. Triarhou LC, Herndon RM. The effect of dexamethasone on L-alpha-lysophosphatidyl choline (lysolecithin)-induced demyelination of the rat spinal cord. Arch Neurol. 1986;43:121-125
123. Kim YS, Tauber MG. Neurotoxicity of glia activated by gram-positive bacterial products depends on nitric oxide production. Infect Immunol. 1996;64:3148-3153
124. Marz P, Gadient RA, Otten U. Expression of interleukin-6 receptor (IL-6R) and gp130 mRNA in PC12 cells and sympathetic neurons: modulation by tumor necrosis factor alpha (TNF-alpha). Brain Res. 1996;706:71-79
125. Zysk G, Bruck W, Gerber J, Bruck Y, Prange HW, Nau R. Antiinflammatory treatment influences neuronal apoptotic cell death in the dentate gyrus in experimental pneumococcal meningitis. J Neuropathol Exp Neurol 1996;55:722-728
126. Baas D, Bourbeau D, Sarlieve LL, Ittel ME, Dussault JH, Puymirat J. Oligodendrocyte maturation and progenitor cell proliferation are independently regulated by thyroid hormone. Glia. 1997;19:324-332
127. Eccleston P, A., Silberberg DH. The differentiation of oligodendrocytes in a serum-free hormone-supplemented medium. Brain Res. 1984;318: 1-9
128. Walters S, Morell P. Effects of altered thyroid states on myelinogenesis. J Neurochem. 1981;36:1792-1801
129. Adamo AM, Aloise PA, Soto EF, Pasquini JM. Neonatal hyperthyroidism in the rat produce an increase in the activity of microperoxismal marker enzymes coincident with biochemical signs of accelerated myelination. J Neurosci Res. 1990;25:353-359
130. Lindholm D, Dechant G, Heisenberg CP, Thoenen H. Brain-derived neurotrophic factor is a survival factor for cultured rat cerebellar granule neurons and protects them against glutamate-induced neurotoxicity. Eur J Neurosci. 1993;5:1455-1464
131. Akaneya Y, Takahashi M, Hatanaka H. Selective acid vulnerability of dopaminergic neurons and its recovery by brain-derived neurotrophic factor. Brain Res. 1995;704:175-183
132. Nakao N, Kokaia Z, Odin P, Lindvall O. Protective effects of BDNF and NT-3 but not PDGF against hypoglycemic injury to cultured striatal neurons. Exp Neurol. 1995;131:1-10
133. Yu O, Chuang DM. Neurotrophin protection against toxicity induced by low potassium and nitroprusside in cultured cerebellar granule neurons. J Neurochem. 1997;68:68-77
134. Wang W, Salvaterra PM, Loera S, Chiu AY. Brain-derived neurotrophic factor spares choline acetyltransferase mRNA following axotomy of motor neurons in vivo. J Neurosci Res. 1997;47:134-143
135. Casaccia-Bonnefil P, Carter BD, Dobrowsky RT, Chao MV. Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature. 1996;383:716-719
136. Frim DM, Uhler TA, Short MP, et al. Effects of biologically delivered NGF, BDNF and bFGF on striatal excitotoxic lesions. Neuroreport. 1993;4:367-370
137. Semkova I, Schilling M, Henrich-Noack P, Rami A, Krieglstein J. Clenbuterol protects mouse cerebral cortex and rat hippocampus from ischemic damage and attenuates glutamate neurotoxicity in cultured hippocampal neurons by induction of NGF. Brain Res. 1996;717:44-54
138. Wilcox BJ, Applegate MD, Portera-Cailliau C, Koliatsos VE. Nerve growth factor prevents apoptotic cell death in injured central cholinergic neurons. J Comp Neurol. 1995;359:573-585
139. Perez-Navarro E, Alberch J. Protective role of nerve growth factor against excitatory amino acid injury during neostriatal cholinergic neurons postnatal development. Exp Neurol. 1995;135:146-152
140. Pechan PA, Yoshida T, Panahian N, Moskowitz MA, Breakefield XO. Genetically modified fibroblasts producing NGF protect hippocampal neurons after ischemia in the rat. Neuroreport. 1995;6:669-672
141. Ernfors P, Duan ML, ElShamy WM, Canlon B. Protection of auditory neurons from aminoglycoside toxicity by neurotrophin-3. Nat Med. 1996;2:463-467
142. Cui Q, Harvey AR. At least two mechanisms are involved in the death of retinal ganglion cells following target ablation in neonatal rats. J Neurosci. 1995;15:8143-8155
143. Hagg T, Quon D, Higaki J, Varon S. Ciliary neurotrophic factor prevents neuronal degeneration and promotes low affinity NGF receptor expression in the adult rat CNS. Neuron. 1992;8:145-158
144. Dale SM, Kuang RZ, Wei X, Varon S. Corticospinal motor neurons in the adult rat: degeneration after intracortical axotomy and protection by ciliary neurotrophic factor (CNTF). Exp Neurol. 1995;135:67-73
145. Ogata N, Ogata K, Imhof HG, Yonekawa Y. Effect of CNTF on ischaemic cell damage in rat hippocampus. Acta Neurochir (Wien). 1996; 138:580-583
146. Kovacs Z, Ikezaki K, Samoto K, Inamura T, Fukui M. VEGF and flt. Expression time kinetics in rat brain infarct. Stroke. 1996;27:1865-1872
147. Hata Y, Nakagawa K, Ishibashi T, Inomata H, Ueno H, Sueishi K. Hypoxia-induced expression of vascular endothelial growth factor by retinal glial cells promotes in vitro angiogenesis. Virchows Arch. 1995; 426:479-486
148. Stone J, Itin A, Alon T, et al. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci. 1995;15:4738-4747
149. Yasuda T, Grinspan J, Stern J, Franceschini B, Bannerman P, Pleasure D. Apoptosis occurs in the oligodendroglial lineage, and is prevented by basic fibroblast growth factor. J Neurosci Res. 1995;40:307-317
150. Gard AL, Pfeiffer SE. Glial cell mitogens bFGF and PDGF differentially regulate development of O4+GalC- oligodendrocyte progenitors. Dev Biol. 1993;159:618-630
151. Grinspan JB, Reeves MF, Coulaloglou MJ, Nathanson D, Pleasure D. Re-entry into the cell cycle is required for bFGF-induced oligodendroglial dedifferentiation and survival. J Neurosci Res. 1996;46:456-464
152. Fressinaud C, Laeng P, Labourdette G, Durand J, Vallat JM. The proliferation of mature oligodendrocytes in vitro is stimulated by basic fibroblast growth factor and inhibited by oligodendrocyte-type 2 astrocyte precursors. Dev Biol. 1993;158:317-329
153. Fressinaud C, Vallat JM. Basic fibroblast growth factor improves recovery after chemically induced breakdown of myelin-like membranes in pure oligodendrocyte cultures. J Neurosci Res. 1994;38:202-213
154. Fernandez-Sanchez MT, Novelli A. Basic fibroblast growth factor protects cerebellar neurons in primary culture from NMDA and non-NMDA receptor mediated neurotoxicity. FEBS Lett. 1993;335:124-131
155. Park TH, Mytilineou C. Protection from 1-methyl-4-phenylpyridinium (MPP+) toxicity and stimulation of regrowth of MPP(+)-damaged dopaminergic fibers by treatment of mesencephalic cultures with EGF and basic FGF. Brain Res. 1992;599:83-97
156. Maiese K, Boniece I, DeMeo D, Wagner JA. Peptide growth factors protect against ischemia in culture by preventing nitric oxide toxicity. J Neurosci. 1993;13:3034-3040
157. Casper D, Blum M. Epidermal growth factor and basic fibroblast growth factor protect dopaminergic neurons from glutamate toxicity in culture. J Neurochem. 1995;65:1016-1026
158. Shen HZ, Turnley A, Murphy M, Bernard CCA, Bartlett PF. Epidermal growth factor inhibits the expression of myelin basic protein in oligodendrocytes. J Neurosci Res. 1989;23:425-432
159. Matthieu JM, Comte V, Tosic M, Honegger P. Myelin gene expression during demyelination and remyelination in aggregating brain cell cultures. J Neuroimmunol. 1992;40:231-234
160. Pauwels PJ, van Assouw HP, Leysen JE. Attenuation of neurotoxicity following anoxia or glutamate receptor activation in EGF- and hippocampal extract-treated neuronal cultures. Cell Signal. 1989;1:45-54
161. Abe K, Saito H. Protective effect of epidermal growth factor on glutamate neurotoxicity in cultured cerebellar neurons. Neurosci Res. 1992; 14:117-123
162. Yamada M, Enokido Y, Ikeuchi T, Hatanaka H. Epidermal growth factor prevents oxygen-triggered apoptosis and induces sustained signaling in cultured rat cerebral cortical neurons. Eur J Neurosci. 1995;7: 2130-2138
163. Mozell RL, McMorris FA. Insulin-like growth factor I stimulates oligodendrocyte development and myelination in rat brain aggregate cultures. J Neurosci Res. 1991;30:382-390
164. Masters BA, Werner H, Roberts CTJ, LeRoith D, Raizada MK. Insulin-like growth factor (IGF-1) receptors and IGF-1 action in oligodendrocytes from rat brains. Regul Pept. 1991;33:117-131
165. Saneto RP, de Vellis J. Characterization of cultured rat oligodendrocytes proliferating in serum-free, chemically defined medium. Proc Natl Acad Sci USA, 1985;82:3509-3513
166. Yao DL, West NR, Bondy CA, et al. Cryogenic spinal cord injury induces astrocytic gene expression of insulin-like growth factor I and insulin-like growth factor binding protein 2 during myelin regeneration. J Neurosci Res. 1995;40:647-659
167. Armstrong RC, Harvath L, Dubois-Dalcq ME. Type 1 astrocytes and oligodendrocyte-type 2 astrocyte glial progenitors migrate toward distinct molecules. J Neurosci Res. 1990;27:400-407
168. Dore S, Kar S, Quirion R. Insulin-like growth factor I protects and rescues hippocampal neurons against beta-amyloid- and human amylin-induced toxicity. Proc Natl Acad Sci U S A. 1997;94:4772-4777
169. Sortino MA, Canonico PL. Neuroprotective effect of insulin-like growth factor I in immortalized hypothalamic cells. Endocrinology. 1996;137:1418-1422
170. Guan J, Williams CE, Skinner SJ, Mallard EC, Gluckman PD. The effects of insulin-like growth factor (IGF)-1, IGF-2, and des-IGF-1 on neuronal loss after hypoxic-ischemic brain injury in adult rats: evidence for a role for IGF binding proteins. Endocrinology. 1996;137: 893-898
171. Matthews CC, Feldman EL. Insulin-like growth factor I rescues SH-SY5Y human neuroblastoma cells from hyperosmotic induced programmed cell death. J Cell Physiol. 1996;166:323-331
172. Mattson MP, Cheng B. Growth factors protect neurons against excitotoxic/ischemic damage by stabilizing calcium homeostasis. Stroke. 1993;24:1136-1140; discussion 1144-1145
173. Fressinaud C, Vallat JM, Pouplard-Barthelaix A. Platelet-derived growth factor partly prevents chemically induced oligodendrocyte death and improves myelin-like membranes repair in vitro. Glia. 1996; 16:40-50
174. Pietz K, Odin P, Funa K, Lindvall O. Protective effect of platelet-derived growth factor against 6- hydroxydopamine-induced lesion of rat dopaminergic neurons in culture. Neurosci Lett. 1996;204:101-104
175. Cheng B, Mattson MP. PDGFs protect hippocampal neurons against energy deprivation and oxidative injury: evidence for induction of antioxidant pathways. J Neurosci. 1995;15:7095-7104
176. McKinnon RD, Piras G, Ida JA, Dubois-Dalcq M. A role for TGF-beta in oligodendrocyte development. J Cell Biol. 1993;121:1397-1407
177. Merrill JE, Zimmermann RP. Natural and induced cytotoxicity by microglia is inhibitable by TGF-beta. Glia. 1991;4:327-331
178. Prehn JH, Miller RJ. Opposite effects of TGF-beta 1 on rapidly- and slowly-triggered excitotoxic injury. Neuropharmacology. 1996;35:249-56
179. Ren RF, Flanders KC. Transforming growth factors-beta protect primary rat hippocampal neuronal cultures from degeneration induced by beta-amyloid peptide. Brain Res. 1996;732:16-24
180. Meucci O, Miller RJ. gp120-induced neurotoxicity in hippocampal pyramidal neuron cultures: protective action of TGF-betal. J Neurosci. 1996;16:4080-4088
181. Henrich-Noack P, Prehn JH, Krieglstein J. TGF-beta 1 protects hippocampal neurons against degeneration caused by transient global ischemia. Dose-response relationship and potential neuroprotective mechanisms. Stroke. 199627:1609-1615
182. Chao CC, Hu S, Kravitz FH, Tsang M, Anderson WR, Peterson PK. Transforming growth factor-beta protects human neurons against beta-amyloid-induced injury. Mol Chem Neuropathol. 1994;23:159-178
183. Canoll PD, Musacchio JM, Hardy R, Reynolds R, Marchionni MA, Salzer JL. GGF/Neuregulin promotes the proliferation and survival and inhibits the differentiation of cells in the oligodendrocyte lineage. Neuron. 1996;17:229-243
184. Merrill JE. Macroglia: neural cells responsive to lymphokines and growth factors. Immunol Today. 1987;8:146-150
185. Merrill JE. Effect of Lymphokines and Monotones on Glial Cells In Vitro and In Vivo. Neuroimmune Networks: Physiology and Disease. New York, NY: Liss; 1989:89-97
186. Benveniste EN, Merrill JE. Stimulation of oligodendroglia proliferation and maturation by interleukin-2. Nature. 1986;321:610-613
187. Benveniste EN, Herman PV, Whitaker JN. Myelin basic protein-specific RNA levels in interleukin 2-stimulated oligodendrocytes. J Neurochem. 1987;49:1274-1279