Bilirubin exerts additional toxic effects in hypoxic cultured neurons from the developing rat brain by the recruitment of glutamate neurotoxicity

Pediatric Research

Volumn 49, Issue 4, 2001, Pages 507-513

  Grojean, Stéphanie ^a   ÉRie Lievre, Val ^a   Koziel, Violette ^a   Vert, Paul ^a   Daval, Jean Luc ^a  

^a UNIVERSITÉ DE LORRAINE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BILIRUBIN; CYCLOHEXIMIDE; DEOXYGLUCOSE; DIZOCILPINE; FREE RADICAL; GLUTAMATE RECEPTOR ANTAGONIST; GLUTAMIC ACID; LEUCINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SCAVENGER;

ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN HYPOXIA; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; ENERGY METABOLISM; FETUS; NERVE CELL CULTURE; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; RISK FACTOR;

EID: 0035066363     PISSN: 00313998     EISSN: 15300447     Source Type: Journal    
DOI: 10.1203/00006450-200104000-00012     Document Type: Article

References (59)

1. Mutch L, Alberman E, Hagberg B, Kodoma K, Perat MV 1992 Cerebral palsy epidemiology: where are we and where are we going? Dev Med Child Neurol 34: 547-551
2. Patel J, Edwards AD 1997 Prediction of outcome after perinatal asphyxia. Curr Opin Pediatr 9: 128-132
3. + o. J Neurosci 13: 63-72
4. Taniguchi T, Fukunaga R, Matsuoka Y, Terai K, Tooyama I, Kimura H 1994 Delayed expression of c-fos protein in rat hippocampus and cerebral cortex following transient in vivo exposure to hypoxia. Brain Res 640: 119-125
5. Rothman SM 1983 Synaptic activity mediates cell death of hypoxic neurons. Science 220: 536-537
6. Banasiak KJ, Haddad GG 1998 Hypoxia-induced apoptosis: effect of hypoxic severity and role of p53 in neuronal cell death. Brain Res 797: 295-304
7. Dichter MA 1978 Rat cortical neurons in cell culture: culture methods, cell morphology, electrophysiology and synapse formation. Brain Res 149: 279-293
8. Laerum OD, Steinsvag S, Bjerkvig R 1985 Cell and tissue culture of the central nervous system: recent developments and current applications. Acta Neurol Scand 72: 529-549
9. Bossenmeyer C, Chihab R, Muller S, Schroeder H, Daval JL 1998 Hypoxia/reoxygenation induces apoptosis through biphasic induction of protein synthesis in central neurons. Brain Res 787: 107-116
10. Chihab R, Ferry C, Koziel V, Monin P, Daval JL 1998 sequential activation of activator protein-1-related transcription factors and JNK protein kinases may contribute to apoptotic death induced by transient hypoxia in developing brain neurons. Mol Brain Res 63: 105-120
11. Tamatani M, Mitsuda N, Matsuzaki H, Okado H, Miyake S, Vitek MP, Yamaguchi A, Tohyama M 2000 A pathway of neuronal apoptosis induced by hypoxia/reoxygenation: roles of nuclear factor-kappa B and Bcl-2. J Neurochem 75: 683-693
12. Maisels MJ 1994 Bilirubin. In: Avery GB, Fletcher MA, MacDonald MG (eds) Neonatology: Pathophysiology and Management of the Newborn, 4th ed. JB Lippincott, Philadelphia, pp 630-725
13. Volpe JJ 1995 Bilirubin and brain injury. In: Volpe JJ (ed) Neurology of the Newborn. Saunders, Philadelphia, pp 490-514
14. Ahdab-Barmada M, Moossy J 1982 The neuropathology of kernicterus in the premature infant: diagnostic problems. J Neuropathol Exp Neurol 43: 45-56
15. Grojean S, Koziel V, Vert P, Daval JL 2000 Bilirubin induces apoptosis via activation of NMDA receptors in developing rat brain neurons. Exp Neurol 166: 334-341
16. Lucey JF, Hibbard E, Behrman RE, Esquivel de Gallardo FO, Windle WF 1964 Kernicterus in asphyxiated newborn Rhesus monkey. Exp Neurol 9: 43-49
17. Ackerman BD, Dyer GI, Leydorf MM 1970 Hyperbilirubinemia and kernicterus in small premature infants. Pediatrics 45: 918-925
18. Cashore WJ, Oh W 1982 Unbound bilirubin and kernicterus in low-birth-weight infants. Pediatrics 69: 481-485
19. Graziani LJ, Mitchell DG, Kornhauser M, Pidcock FS, Merton DA, Stanley C, McKee LE 1992 Neurodevelopment of preterm infants: neonatal neurosonographic and serum bilirubin studies. Pediatrics 89: 229-234.
20. Cowger ML 1973 Bilirubin encephalopathy. In: Gaull GE (ed) Brain Dysfunction. Plenum Press, New York, pp 265-293
21. Myers RE 1979 A unitary theory of causation of anoxia and hypoxia brain pathology. In: Fahn C, Davis JN, Rowland LP (eds) Cerebral Hypoxia and Its Consequences. Advances in Neurology, Vol 26. Raven Press New York, pp 195-213
22. Odell GB 1981 Neonatal Hyperbilirubinemia. Grune and Stratton, New York
23. Mayor F Jr, Pagés M, Diez-Guerra J, Valdivieso F, Mayor F 1985 Effect of postnatal anoxia on bilirubin levels in rat brain. Pediatr Res 19: 231-236
24. Vannucci RC, Plum F 1975 Pathophysiology of perinatal hypoxic-ischemic brain damage. In: Gaull GE (ed) Biology of Brain Dysfunction. Plenum Press, New York, pp 1-45
25. Kim MH, Yoon JJ, Sher J, Brown AK 1980 Lack of predictive indices in kernicterus: a comparison of clinical and pathologic factors in infants with or without kernicterus. Pediatrics 66: 852-858
26. Sastry PS, Rao KS 2000 Apoptosis and the nervous system. J Neurochem 74: 1-20
27. Bossenmeyer-Pourié C, Koziel V, Daval JL 2000 Effects of hypothermia on hypoxia-induced apoptosis in cultured neurons from developing rat forebrain: comparison with preconditioning. Pediatr Res 47: 385-391
28. Hansen MB, Nielsen SE, Berg K 1989 Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J Immunol Meth 119: 203-210
29. Gschwind M, Huber G 1997 Detection of apoptotic or necrotic death in neuronal cells by morphological, biochemical, and molecular analysis. In: Poirier J (ed) Apoptosis Techniques and Protocols, Neuromethods, Vol 29. Humana Press, Totowa, pp 13-31
30. Park DS, Morris EJ, Greene LA, Geller HM 1997 G1/S cell cycle blockers and inhibitors of cyclin-dependent kinases suppress camptothecin-induced neuronal apoptosis. J Neurosci 17: 1256-1270
31. Wolvetang EJ, Johnson KL Krauer K, Ralph SJ, Linnane AW 1994 Mitochondrial respiratory chain inhibitors induce apoptosis. FEBS Lett 339: 40-44
32. Bradford MM 1976 A rapid and sensitive method for the quantitation of microgram quantities of proteins utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
33. Oillet J, Koziel V, Vert P, Daval JL 1996 Influence of post-hypoxia reoxygenation conditions on energy metabolism and superoxide production in cultured neurons from the rat forebrain. Pediatr Res 39: 598-603
34. Rothe G, Emmendorffer A, Oser A, Roesler J, Valet G 1991 Flow cytometric measurement of the respiratory burst activity of phagocytes using dihydrorhodamine 123. J Immunol Meth 138: 133-135
35. 2 production in human macrophages. Biochim Biophys Acta 1244: 79-84
36. Shigeno T, Yamasaki Y, Kato G, Kusaka K, Mima T, Takakura K, Graham DI, Furukawa S 1990 Reduction of delayed neuronal death by inhibition of protein synthesis. Neurosci Lett 120: 117-119
37. Johnson EM, Deckwerth TL 1993 Molecular mechanisms of developmental neuronal death. Annu Rev Neurosci 16: 31-46
38. Pittman RN, Wang S, DiBenedetto AJ, Mills JC 1993 A system for characterizing cellular and molecular events in programmed neuronal cell death. J Neurosci 13: 3669-3680
39. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN 1987 Bilirubin is an antioxidant of possible physiological importance. Science 235: 1043-1046
40. Dennery PA, McDonagh AF, Spitz DR, Rodgers PA, Stevenson DK 1995 Hyperbilirubinemia results in reduced oxidative injury in neonatal gunn rats exposed to hyperoxia. Free Rad Biol Med 19: 395-404
41. Hoffman DJ, Zanelli SA, Kubin J, Mishra OP, Delivoria-Papadopoulos M 1996 The in vivo effect of bilirubin on the N-methyl- d -aspartate receptor/ion channel complex in the brains of newborn piglets. Pediatr Res 40: 804-808
42. McDonald JW, Shapiro SM, Silverstein FS, Johnston MV 1998 Role of glutamate receptor mediated excitotoxicity in bilirubin-induced brain injury in the Gunn rat model. Exp Neurol 150: 21-29
43. Brodersen R 1979 Bilirubin: solubility and interaction with albumin and phospholipid. J Biol Chem 254: 2364-2369
44. Notter MFD, Kendig JW 1986 Differential sensitivity of neural cells to bilirubin toxicity. Exp Neurol 94: 670-682
45. Bossenmeyer-Pourié C, Koziel V, Daval JL 1999 CPP32/caspase-3-like proteases in hypoxia-induced apoptosis in developing brain neurons. Mol Brain Res 71: 225-237
46. Bossenmeyer-Pourié C, Koziel V, Daval JL 2000 Involvement of caspase-1 proteases in hypoxic brain injury. Effects of their inhibitors in developing neurons. Neuroscience 95: 1157-1165
47. Jones MD, Burd LI, Makowski EI, Meschia G, Battaglia FC 1975 Cerebral metabolism in sheep: a comparative study in the adult, the lamb, and the fetus. Am J Physiol 229: 235-239
48. Settergren G, Lindblad BS, Persson B 1980 Cerebral blood flow and exchange of oxygen, glucose, ketone bodies, lactate, pyruvate and amino acids in anesthetized children. Acta Pediatr Scand 69: 457-465
49. Bômont L, Bilger A, Boyet S, Vert P, Nehlig A 1992 Acute hypoxia induces specific changes in local cerebral glucose utilization at different postnatal ages in the rat. Dev Brain Res 66: 33-45
50. 31 P nuclear magnetic resonance spectroscopy. Pediatr Res 23: 569-573
51. Roger C, Koziel V, Vert P, Nehlig A 1995 Regional cerebral metabolic consequences of bilirubin in rat depend upon post-gestational age at the time of hyperbilirubinemia. Dev Brain Res 87: 194-202
52. Roger C, Koziel V, Vert P, Nehlig A 1993 Effects of bilirubin infusion on local cerebral glucose utilization in the immature rat. Dev Brain Res 76: 115-130
53. Durkin JP, Tremblay R, Chakravarthy B, Mealing G, Morley P, Song D 1997 Evidence that the early loss of membrane protein kinase C is a necessary step in the excitatory amino acid-induced death of primary cortical neurons. J Neurochem 68: 1400-1412
54. Chihab R, Bossenmeyer C, Oillet J, Daval JL 1998 Lack of correlation between the effects of transient exposure to glutamate and those of hypoxia/reoxygenation in immature neurons in vitro. J Neurochem 71: 1177-1186
55. Oillet J, Nicolas F, Koziel V, Daval JL 1995 Analysis of glutamate receptors in primary cultured neurons from fetal rat forebrain. Neurochem Res 20: 761-768
56. Chihab R, Oillet J, Bossenmeyer C, Daval JL 1998 Glutamate triggers cell death specifically in mature central neurons through a necrotic process. Mol Gen Metab 63: 142-147
57. Durkin JP, Tremblay R, Buchan A, Blosser J, Chakravarthy B, Mealing G, Morley P, Song D 1996 An early loss in membrane protein kinase C activity precedes the excitatory amino acid-induced death of primary cortical neurons. J Neurochem 66: 951-962
58. Sano K, Nakamura H, Matsuo T 1985 Mode of inhibitory action of bilirubin on protein kinase C. Pediatr Res 19: 587-590
59. Amit Y, Boneh A 1993 Bilirubin inhibits protein kinase C activity and protein kinase C-mediated phosphorylation of endogenous substrates in human skin fibroblasts. Clin Chim Acta 223: 103-111