White matter injury following systemic endotoxemia or asphyxia in the fetal sheep

Neurochemical Research

Volumn 28, Issue 2, 2003, Pages 215-223

  Mallard, Carina ^a   Welin, Anna Karin ^b   Peebles, Donald ^c   Hagberg, Henrik ^b   Kjellmer, Ingemar ^d  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d QUEEN SILVIA CHILDREN'S HOSPITAL   (Sweden)

Author keywords

Asphyxia; Endotoxemia; Infection; Oligodendrocyte; Periventricular leukomalacia

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASPHYXIA; ASTROCYTE; BRAIN DEVELOPMENT; BRAIN INJURY; BRAIN PERFUSION; BRAIN REGION; CELL ACTIVATION; CELL DAMAGE; CELL LOSS; CELL SPECIFICITY; CONTROLLED STUDY; CORPUS STRIATUM; ENDOTOXEMIA; ESCHERICHIA COLI; FEMALE; FETUS; GRAY MATTER; HIPPOCAMPUS; INFLAMMATORY INFILTRATE; INTRAUTERINE INFECTION; MICROGLIA; NERVE CELL LESION; NERVE CELL NECROSIS; NONHUMAN; OLIGODENDROGLIA; PREGNANCY; PREMATURITY; PRIORITY JOURNAL; SHEEP; UMBILICAL CORD; WHITE MATTER;

ANIMALS; ASPHYXIA; ENDOTOXEMIA; FEMALE; HUMANS; INFANT, NEWBORN; LEUKOMALACIA, PERIVENTRICULAR; PREGNANCY; SHEEP;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; OVIS ARIES;

EID: 0037321714     PISSN: 03643190     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1022368915400     Document Type: Article

References (46)

1. Fujimoto, S., Yamaguchi, N., Togari, H., Wada, Y., and Yokochi, K. 1994. Cerebral palsy of cystic periventricular leukomalacia in low-birth-weight infants. Acta Paediatr. 83:397-401.
2. Volpe, J. J. 1998. Brain injury in the premature infant: Overview of clinical aspects, neuropathology, and pathogenesis. Semin. Pediatr. Neurol. 5:135-151.
3. Banker, B. Q. and Larroche, J.-C. 1962. Periventricular leukomalacia of infancy: A form of neonatal anoxic encephalopathy. Arch. Neurol. 7:386-410.
4. Takashima, S. and Tanaka, K. 1978. Development of cerebrovascular architecture and its relationship to periventricular leukomalacia. Arch. Neurol. 35:11-16.
5. De Reuck, J. L. 1984. Cerebral angioarchitecture and perinatal brain lesions in premature and full-term infants. Acta Neurol. Scand. 70:391-395.
6. Back, S. A., Luo, N. L., Borenstein, N. S., Levine, J. M., Volpe, J. J., and Kinney, H. C. 2001. Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J. Neurosci. 21:1302-1312.
7. Dammann, O. and Leviton, A. 1998. Infection remote from the brain, neonatal white matter damage, and cerebral palsy in the preterm infant. Semin. Pediatr. Neurol. 5:190-201.
8. Leviton, A. 1993. Preterm birth and cerebral palsy: Is tumor necrosis factor the missing link? Dev. Med. Child Neurol. 35:553-558.
9. Deguchi, K., Oguchi, K., and Takashima, S. 1997. Characteristic neuropathology of leukomalacia in extremely low birth weight infants. Pediatr. Neurol. 16:296-300.
10. Nelson, K. B., Dambrosia, J. M., Grether, J. K., and Phillips, T. M. 1998. Neonatal cytokines and coagulation factors in children with cerebral palsy. Ann. Neurol. 44:665-675.
11. Reddy, K., Mallard, C., Guan, J., Marks, K., Bennet, L., Gunning, M., Gunn, A., Gluckman, P., and Williams, C. 1998. Maturational change in the cortical response to hypoperfusion injury in the fetal sheep. Pediatr. Res. 43:674-682.
12. Gilles, F. H., Averill, D. R., Jr., and Kerr, C. S. 1977. Neonatal endotoxin encephalopathy. Ann. Neurol. 2:49-56.
13. Young, R. S., Yagel, S. K., and Towfighi, J. 1983. Systemic and neuropathologic effects of E. coli endotoxin in neonatal dogs. Pediatr. Res. 17:349-353.
14. Yoon, B. H., Kim, C. J., Romero, R., Jun, J. K., Park, K. H., Choi, S. T., and Chi, J. G. 1997. Experimentally induced intrauterine infection causes fetal brain white matter lesions in rabbits. Am. J. Obstet. Gynecol. 177:797-802.
15. Debillon, T., Gras-Leguen, C., Verielle, V., Winer, N., Caillon, J., Roze, J. C., and Gressens, P. 2000. Intrauterine infection induces programmed cell death in rabbit periventricular white matter. Pediatr. Res. 47:736-742.
16. Mallard, E. C., Gunn, A. J., Williams, C. E., Johnston, B. M., and Gluckman, P. D. 1992. Transient umbilical cord occlusion causes hippocampal damage in the fetal sheep. Am. J. Obstet. Gynecol. 167:1423-1430.
17. Mallard, E. C., Williams, C. E., Gunn, A. J., Gunning, M. I., and Gluckman, P. D. 1993. Frequent episodes of brief ischemia sensitize the fetal sheep brain to neuronal loss and induce striatal injury. Pediatr. Res. 33:61-65.
18. Gilland, E., Bona, E., and Hagberg, H. 1998. Temporal changes of regional glucose use, blood flow, and microtubule-associated protein 2 immunostaining after hypoxia-ischemia in the immature rat brain. J. Cereb. Blood Flow Metab. 18:222-228.
19. Braun, P. E., Sandillon, F., Edwards, A., Matthieu, J. M., and Privat, A. 1988. Immunocytochemical localization by electron microscopy of 2′3′-cyclic nucleotide 3′-phosphodiesterase in developing oligodendrocytes of normal and mutant brain. J. Neurosci. 8:3057-3066.
20. Paneth, N., Rudelli, R., Monte, W., Rodriguez, E., Pinto, J., Kairam, R., and Kazam, E. 1990. White matter necrosis in very low birth weight infants: Neuropathologic and ultrasonographic findings in infants surviving six days or longer. J. Pediatr. 116:975-984.
21. Duggan, P. J., Maalouf, E. F., Watts, T. L., Sullivan, M. H., Counsell, S. J., Allsop, J., Al-Nakib, L., Rutherford, M. A., Battin, M., Roberts, I., and Edwards, A. D. 2001. Intrauterine T-cell activation and increased proinflammatory cytokine concentrations in preterm infants with cerebral lesions. Lancet 358:1699-1700.
22. Chamnanvanakij, S., Margraf, L. R., Burns, D., and Perlman, J. M. 2002. Apoptosis and white matter injury in preterm infants. Pediatr. Dev. Pathol. 5:184-189.
23. Volpe, J. J. 2001. Neurobiology of periventricular leukomalacia in the premature infant. Pediatr. Res. 50:553-562.
24. Rees, S., Stringer, M., Just, Y., Hooper, S. B., and Harding, R. 1997. The vulnerability of the fetal sheep brain to hypoxemia at mid-gestation. Brain Res. Dev. Brain Res. 103:103-118.
25. Matsuda, T., Okuyama, K., Cho, K., Hoshi, N., Matsumoto, Y., Kobayashi, Y., and Fujimoto, S. 1999. Induction of antenatal periventricular leukomalacia by hemorrhagic hypotension in the chronically instrumented fetal sheep. Am. J. Obstet. Gynecol. 181:725-730.
26. Mallard, E. C., Waldvogel, H. J., Williams, C. E., Faull, R. L., and Gluckman, P. D. 1995. Repeated asphyxia causes loss of striatal projection neurons in the fetal sheep brain. Neuroscience 65:827-836.
27. De Haan, H. H., Gunn, A. J., Williams, C. E., and Gluckman, P. D. 1997. Brief repeated umbilical cord occlusions cause sustained cytotoxic cerebral edema and focal infarcts in near-term fetal lambs. Pediatr. Res. 41:96-104.
28. Mayhan, W. G. 1998. Effect of lipopolysaccharide on the permeability and reactivity of the cerebral microcirculation: Role of inducible nitric oxide synthase. Brain Res. 792:353-357.
29. Chao, C. C., Hu, S., and Peterson, P. K. 1995. Glia, cytokines, and neurotoxicity. Crit. Rev. Neurobiol. 9:189-205.
30. Hagberg, H., Gilland, E., Bona, E., Hanson, L. A., Hahin-Zoric, M., Blennow, M., Holst, M., McRae, A., and Soder, O. 1996. Enhanced expression of interleukin (IL)-1 and IL-6 messenger RNA and bioactive protein after hypoxia-ischemia in neonatal rats. Pediatr. Res. 40:603-609.
31. Kim, W. G., Mohney, R. P., Wilson, B., Jeohn, G. H., Liu, B., and Hong, J. S. 2000. Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: Role of microglia. J. Neurosci. 20:6309-6316.
32. Anthony, D. C., Bolton, S. J., Feam, S., and Perry, V. H. 1997. Age-related effects of interleukin-1 beta on polymorphonuclear neutrophil-dependent increases in blood-brain barrier permeability in rats. Brain 120:435-444.
33. Inage, Y. W., Itoh, M., and Takashima, S. 2000. Correlation between cerebrovascular maturity and periventricular leukomalacia. Pediatr. Neurol. 22:204-208.
34. Hardy, R. J. and Friedrich, V. L., Jr. 1996. Progressive remodeling of the oligodendrocyte process arbor during myelinogenesis. Dev. Neurosci. 18:243-254.
35. Fern, R. and Moller, T. 2000. Rapid ischemic cell death in immature oligodendrocytes: A fatal glutamate release feedback loop. J. Neurosci. 20:34-42.
36. Selmaj, K. W. and Raine, C. S. 1988. Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann. Neurol. 23:339-346.
37. Yonezawa, M., Back, S. A., Gan, X., Rosenberg, P. A., and Volpe, J. J. 1996. Cystine deprivation induces oligodendroglial death: Rescue by free radical scavengers and by a diffusible glial factor. J. Neurochem. 67:566-573.
38. Follett, P. L., Rosenberg, P. A., Volpe, J. J., and Jensen, F. E. 2000. NBQX attenuates excitotoxic injury in developing white matter. J. Neurosci. 20:9235-9241.
39. Bennet, L., Rossenrode, S., Gunning, M. I., Gluckman, P. D., and Gunn, A. J. 1999. The cardiovascular and cerebrovascular responses of the immature fetal sheep to acute umbilical cord occlusion. J. Physiol. 517:247-257.
40. Young, R. S., Hernandez, M. J., and Yagel, S. K. 1982. Selective reduction of blood flow to white matter during hypotension in newborn dogs: A possible mechanism of periventricular leukomalacia. Ann. Neurol. 12:445-448.
41. Ando, M., Takashima, S., and Mito, T. 1988. Endotoxin, cerebral blood flow, amino acids and brain damage in young rabbits. Brain Dev. 10:365-370.
42. Quan, N., Whiteside, M., and Herkenham, M. 1998. Time course and localization patterns of interleukin-1 beta messenger RNA expression in brain and pituitary after peripheral administration of lipopolysaccharide. Neuroscience 83:281-293.
43. van Dam, A. M., Poole, S., Schultzberg, M., Zavala, F., and Tilders, F. J. 1998. Effects of peripheral administration of LPS on the expression of immunoreactive interleukin-1 alpha, beta, and receptor antagonist in rat brain. Ann. N Y Acad. Sci. 840:128-138.
44. Lacroix, S., Feinstein, D., and Rivest, S. 1998. The bacterial endotoxin lipopolysaccharide has the ability to target the brain in upregulating its membrane CD14 receptor within specific cellular populations. Brain Pathol. 8:625-640.
45. Nadeau, S. and Rivest, S. 2000. Role of microglial-derived tumor necrosis factor in mediating CD14 transcription and nuclear factor kappa B activity in the brain during endotoxemia. J. Neurosci. 20:3456-3468.
46. Eklind, S., Mallard, C., Leverin, A. L., Gilland, E., Blomgren, K., Mattsby-Baltzer, I., and Hagberg, H. 2001. Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur. J. Neurosci. 13:1101-1106.