Effects of chronic placental insufficiency on brain development in fetal sheep

Pediatric Research

Volumn 43, Issue 2, 1998, Pages 262-270

  Mallard, E Carina ^a   Rees, Sandra ^a   Stringer, Michelle ^a   Cock, Megan L ^b   Harding, Richard ^b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; MYELIN BASIC PROTEIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN HYPOXIA; CEREBELLUM; CONTROLLED STUDY; FETUS; FETUS DEVELOPMENT; GESTATIONAL AGE; IMMUNOHISTOCHEMISTRY; MYELINATION; NERVOUS SYSTEM DEVELOPMENT; NEUROLOGICAL COMPLICATION; NONHUMAN; PLACENTA CIRCULATION; PLACENTA INSUFFICIENCY; PRIORITY JOURNAL; SHEEP; WHITE MATTER;

EID: 0031933376     PISSN: 00313998     EISSN: None     Source Type: Journal    
DOI: 10.1203/00006450-199802000-00018     Document Type: Article

References (55)

1. Gagnon R, Challis J, Johnston L, Fraher L 1994 Fetal endocrine responses to chronic placental embolization in the late-gestation ovine fetus. Am J Obstet Gynecol 170:929-938
2. Marsal K, Ley D 1992 Intrauterine blood flow and postnatal neurological development in growth-retarded fetuses. Biol Neonate 62:258-264
3. Gunn AJ, Parer JT, Mallard EC, Williams CE, Gluckman PD 1992 Cerebral histologic and electrocorticographic changes after asphyxia in fetal sheep. Pediatr Res 31:486-491
4. Mallard EC, Gunn AJ, Williams CE, Johnston BM, Gluckman PD 1992 Transient umbilical cord occlusion causes hippocampal damage in the fetal sheep. Am J Obstet Gynecol 167:1423-1430
5. Williams C, Gunn AJ, Mallard C, Gluckman P 1992 Outcome after ischaemia in the developing sheep brain: an electroencephalographic and histological study. Ann Neurol 31:14-21
6. Mallard EC, Williams CE, Gunn AJ, Gunning MI, Gluckman PD 1993 Frequent episodes of brief ischemia sensitize the fetal sheep brain to neuronal loss and induce striatal injury. Pediatr Res 33:61-65
7. Penning DH, Grafe MD, Hammond R, Matsuda Y, Patrick J, Richardson B 1994 Neuropathology of the near-term and midgestation ovine fetal brain after sustained in utero hypoxemia. Am J Obstet Gynecol 170:1425-1432
8. Rees S, Harding R 1995 The effects of experimentally induced placental insufficiency on prenatal brain development. Dev Brain Dysfunct 8:152-166
9. Robinson JS, Kingston EJ, Jones CT, Thorburn GD 1979 Studies on experimental growth retardation in sheep. The effect of removal of endometrial caruncles on fetal size and metabolism. J Dev Physiol 1:379-398
10. Rees S, Bocking AD, Harding R 1988 Structure of the fetal sheep brain in experimental growth retardation. J Dev Physiol 10:211-225
11. Nitsos I, Rees S 1990 The effects of intrauterine growth retardation on the development of neuroglia in fetal guinea pigs. An immunohistochemical and an ultrastructural study. Int J Dev Neurosci 8:233-244
12. Cock ML, Harding R 1997 Renal and amniotic fluid responses to umbilicoplacental embolization for 20 days in fetal sheep. Am J Physiol 273:R1094-R1102
13. Murotsuki J, Gagnon R, Matthews SG, Challis JR 1996 Effects of long-term hypoxemia on pituitary-adrenal function in fetal sheep. Am J Physiol 271:E678-E685
14. Rees S, Harding R 1988 The effects of intrauterine growth retardation on the development of the Purkinje cell dendritic tree in the cerebellar cortex of fetal sheep: a note on the ontogeny of the Purkinje cell. Int J Dev Neurosci 6:461-469
15. Reynolds ML, Mollgard K 1985 The distribution of plasma protein in the neocortex and early allocortex of the developing sheep brain. Anat Embryol 171:41-60
16. Tomimoto H, Nishimura M, Suenaga T, Nakamura S, Akiguchi I, Wakita H, Kimura J, Mayer B 1994 Distribution of nitric oxide synthase in the human cerebral blood vessels and brain tissues. J Cereb Blood Flow Metab 14:930-938
17. Richardson BS, Carmichael L, Homan J, Patrick JE 1993 Cerebral oxidative metabolism in fetal sheep with prolonged and graded hypoxemia. J Dev Physiol 19:77-83
18. Anderson CR, Furness JB, Woodman HL, Edwards SL, Crack PJ, Smith AI 1995 Characterisation of neurons with nitric oxide synthase immunoreactivity that project to prevertebral ganglia. J Auton Nerv Syst 52:107-116
19. Altman J 1969 Autoradiographic and histological studies of postnatal neurogenesis. II. Dating the time of the production and onset of differentiation of cerebellar microneurons in rats. J Comp Neurol 136:269-294
20. Vincent SR, Kimura H 1992 Histochemical mapping of nitric oxide synthase in the rat brain. Neurosciences 46:755-784
21. Mizukawa K, Vincent SR, McGeer PL, McGeer EG 1989 Distribution of reduced-nicotinamide-adenine-dinucleotide-phosphate diaphorase-positive cells and fibers in the cat central nervous system. J Comp Neurol 279:281-311
22. Soothill PW, Nicolaides KH, Campbell S 1987 Prenatal asphyxia, hyperlacticaemia, hypoglycaemia, and erythroblastosis in growth retarded fetuses. Br Med J Clin Res Ed 294:1051-1053
23. Mallard EC, Waldvogel HJ, Williams CE, Faull RL, Gluckman PD 1995 Repeated asphyxia causes loss of striatal projection neurons in the fetal sheep brain. Neurosciences 65:827-836
24. Mallard EC, Williams CE, Johnston BM, Gunning MI, Davis S, Gluckman PD 1995 Repeated episodes of umbilical cord occlusion in fetal sheep lead to preferential damage to the striatum and sensitize the heart to further insults. Pediatr Res 37:707-713
25. Stys PK, Steffensen I 1996 Na(+)-Ca2+ exchange in anoxic/ischemic injury of CNS myelinated axons. Ann NY Acad Sci 779:366-378
26. Gaffney G, Squier MV, Johnson A, Flavell V, Sellers S 1994 Clinical associations of prenatal ischaemic white matter injury. Arch Dis Child Fetal Neonatal Ed 70:F101-106
27. Squier M, Keeling JW 1991 The incidence of prenatal brain injury. Neuropathol Appl Neurobiol 17:29-38
28. 14C]thymidine metabolism in different regions of the rat brain: Histological and biochemical correlations. Brain Res Dev Brain Res 21:283-292
29. Qi Y, Dawson G 1993 Effects of hypoxia on oligodendrocyte signal transduction. J Neurochem 61:1097-1104
30. Husain J, Juurlink BH 1995 Oligodendroglial precursor cell susceptibility to hypoxia is related to poor ability to cope with reactive oxygen species. Brain Res 698:86-94
31. Oka A, Belliveau MJ, Rosenberg PA, Volpe JJ 1993 Vulnerability of oligodendroglia to glutamate: pharmacology, mechanisms, and prevention. J Neurosci 13:1441-1453
32. McMorris FA, Smith TM, DeSalvo S, Furlanetto R 1986 Insulin like growth factor I/somatomedin C: A potent inducer of oligodendrocyte development. Proc Natl Acad Sci USA 83:822-826
33. Jones CT, Gu W, Harding JE, Price DA, Parer JY 1988 Studies on the growth of fetal sheep. Effect of surgical reduction in placental size or experimental manipulation of uterine blood flow on plasma sulphation promoting activity on the concentration of insulin like growth factors I and II. J Dev Physiol 10:179-189
34. Blennow M, Hagberg H, Rosengren L 1995 Glial fibrillary acidic protein in the cerebrospinal fluid: a possible indicator of prognosis in full-term asphyxiated new-born infants? Pediatr Res 37:260-264
35. Burtrum D, Silverstein FS 1994 Hypoxic-ischemic brain injury stimulates glial fibrillary acidic protein mRNA and protein expression in neonatal rats. Exp Neurol 126:112-118
36. Kindy MS, Bhat AN, Bhat NR 1992 Transient ischemia stimulates glial fibrillary acid protein and vimentin gene expression in the gerbil neocortex, striatum and hippocampus. Brain Res Mol Brain Res 13:199-206
37. Zimmer C, Sampaolo S, Sharma HS, Cervos Navarro J 1991 Altered glial fibrillary acidic protein immunoreactivity in rat brain following chronic hypoxia. Neurosciences 40:353-361
38. Romijn HJ, Janszen AW, Van den Bogert C 1994 Permanent increase of immunocytochemical reactivity for γ-aminobutyric acid (GABA), glutamic acid decarboxylase, mitochondrial enzymes, and glial fibrillary acidic protein in rat cerebral cortex damaged by early postnatal hypoxia-ischemia. Acta Neuropathol 87:612-627
39. Eddleston M, Mucke L 1993 Molecular profile of reactive astrocytes-implications for their role in neurologic disease. Neurosciences 54:15-36
40. Li Y, Chopp M, Zhang ZG, Zhang RL 1995 Expression of glial fibrillary acidic protein in areas of focal cerebral ischemia accompanies neuronal expression of 72-kDa heat shock protein. J Neurol Sci 128:134-142
41. Kato H, Kogure K, Araki T, Itoyama Y 1994 Astroglial and microglial reactions in the gerbil hippocampus with induced ischemic tolerance. Brain Res 664:69-76
42. Gluckman P, Klempt N, Guan J, Mallard C, Sirimanne E, Dragunow M, Klempt M, Singh K, Williams C, Nikolics K 1992 A role for IGF-1 in the rescue of CNS neurons following hypoxic-ischemic injury. Biochem Biophysiol Res Commun 182:593-599
43. Guan J, Williams C, Gunning M, Mallard C, Gluckman P 1993 The effects of IGF-1 treatment after hypoxic-ischemic brain injury in adult rats. J Cereb Blood Flow Metab 13:609-616
44. Johnston BM, Mallard EC, Williams CE, Gluckman PD 1996 Insulin-like growth factor-1 is a potent neuronal rescue agent after hypoxic-ischemic injury in fetal lambs. J Clin Invest 97:300-308
45. Takami K, Iwane M, Kiyota Y, Miyamoto M, Tsukuda R, Shiosaka S 1992 Increase of basic fibroblast growth factor immunoreactivity and its mRNA level in rat brain following transient forebrain ischemia. Exp Brain Res 90:1-10
46. Reier PJ, Stensaas LJ, Guth L 1983 The astrocytic scar as an impediment to regeneration in the central nervous system. In: Kao CC, Bunge RP, Reier PJ (eds) Spinal Cord Reconstruction. Raven Press, New York, pp 163-195
47. Endoh M, Maiese K, Pulsinelli WA, Wagner JA 1993 Reactive astrocytes express NADPH diaphorase in vivo after transient ischemia. Neurosci Lett 154:125-128
48. Roufail E, Stringer M, Rees S 1995 Nitric oxide synthase immunoreactivity and NADPH diaphorase staining are co-localised in neurons closely associated with the vasculature in rat and human retina. Brain Res 684:36-46
49. Iadecola C, Beitz AJ, Renno W, Xu X, Mayer B, Zhang F 1993 Nitric oxide synthase-containing neural processes on large cerebral arteries and cerebral microvessels. Brain Res 606:148-155
50. Minami Y, Kimura H, Aimi Y, Vincent SR 1994 Projections of nitric oxide synthase-containing fibers from the sphenopalatine ganglion to cerebral arteries in the rat. Neurosciences 60:745-759
51. Kobari M, Fukuuchi Y, Tomita M, Tanahashi N, Konno S, Takeda H 1994 Dilatation of cerebral microvessels mediated by endothelin ETB receptor and nitric oxide in cats. Neurosci Lett 176:157-160
52. Marks KA, Mallard EC, Roberts I, Williams CE, Gluckman PD, Edwards AD 1996 Nitric oxide synthase inhibition attenuates delayed vasodilation and increases injury after cerebral ischemia in fetal sheep. Pediatr Res 40:185-191
53. McCrabb GJ, Harding R 1996 Role of nitric oxide in the regulation of cerebral blood flow in the ovine foetus. Clin Exp Pharmacol Physiol 23:855-860
54. Shweiki D, Itin A, Soffer D, Keshet E 1992 Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359:843-845
55. Rakic P 1969 Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study in Macacus Rhesus. J Comp Neurol 141:283-312