Unconjugated bilirubin exposure impairs hippocampal long-term synaptic plasticity

PLoS ONE

Volumn 4, Issue 6, 2009, Pages

  Chang, Fang Yu ^a   Lee, Cheng Che ^a   Huang, Chiung Chun ^a   Hsu, Kuei Sen ^a,b  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

BILIRUBIN; CALPAIN; CALPASTATIN; CYTOKINE; INTERLEUKIN 1BETA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; PROPIDIUM IODIDE; RECEPTOR SUBUNIT; TUMOR NECROSIS FACTOR ALPHA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG TARGETING; ELECTROPHYSIOLOGY; HIPPOCAMPUS; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN DEGRADATION; RAT; ANIMAL; DRUG EFFECT; HUMAN; JAUNDICE; METABOLISM; METHODOLOGY; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT; SYNAPTIC TRANSMISSION;

RATTUS;

ANIMALS; BILIRUBIN; CALPAIN; ELECTROPHYSIOLOGY; HIPPOCAMPUS; HUMANS; JAUNDICE; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MALE; NEURONAL PLASTICITY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION;

EID: 67649946332     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005876     Document Type: Article

References (62)

1. Berk PD, Noyer C (1994) Bilirubin metabolism and the hereditary hyperbilirubinemias. Semin Liver Dis 14: 325-345.
2. Gourley GR (1997) Bilirubin metabolism and kernicterus. Adv Pediatr 44: 173-229.
3. Doré S, Takahashi M, Ferris CD, Zakhary R, Hester LD, et al. (1999) Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc Natl Acad Sci USA 96: 2445-2450.
4. Ahdab-Barmada M, Moossy J (1984) The neuropathology of kernicterus in the premature neonate: diagnostic problems. J Neuropathol Exp Neurol 43: 45-56.
5. Shapiro SM (2003) Bilirubin toxicity in the developing nervous system. Pediatr Neurol 29: 410-421.
6. Johnson L, Boggs TR (1974) Bilirubin-dependent brain damage: Incidence and indications for treatment. In: Odell GB, Schaffer R, Sionpoulous AP, eds. Phototherapy in the newborn: An overview. Washington: National Academy of Sciences. pp 122-149.
7. Rubin RA, Balow B, Fisch RO (1979) Neonatal serum bilirubin levels related to cognitive development at ages 4 through 7 years. J Pediatr 94: 601-604.
8. Oktay R, Satar M, Atici A (1996) The risk of bilirubin encephalopathy in neonatal hyperbilirubinemia. Turk J Pediatr 38: 199-204.
9. Newman TB, Liljestrand P, Jeremy RJ, Ferriero DM, Wu YW, et al. (2006) Outcomes among newborns with total serum bilirubin levels of 25 mg per deciliter or more. N Engl J Med 354: 1889-1900.
10. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274: 1133-1138.
11. Zhang LI, Poo MM (2001) Electrical activity and development of neural circuits. Nat Neurosci 4 Suppl: 1207-1214.
12. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39.
13. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23: 649-711.
14. Mulkey RM, Malenka RC (1992) Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9: 967-975.
15. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232: 331-356.
16. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44: 5-21.
17. Squire LR (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99: 195-231.
18. Malenka RC, Nicoll RA (1999) Long-term potentiation-a decade of progress? Science 285: 1870-1874.
19. Zhang L, Liu W, Tanswell AK, Luo X (2003) The effects of bilirubin on evoked potentials and long-term potentiation in rat hippocampus in vivo. Pediatr Res 53: 939-944.
20. A receptor subunit expression in organotypic hippocampal slice cultures. Neuroscience 118: 967-974.
21. Noraberg J, Poulsen FR, Blaabjerg M, Kristensen BW, Bonde C, et al. (2005) Organotypic hippocampal slice cultures for studies of brain damage, neuroprotection and neurorepair. Curr Drug Targets CNS Neurol Disord 4: 435-452.
22. Zucker RS (1989) Short-term synaptic plasticity. Annu Rev Neurosci 12: 13-31.
23. Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2: 32-48.
24. Silva RF, Mata LM, Gulbenkian S, Brites D (2001) Endocytosis in rat cultured astrocytes is inhibited by unconjugated bilirubin. Neurochem Res 26: 793-800.
25. Silva RF, Rodrigues CM, Brites D (2002) Rat cultured neuronal and glial cells respond differently to toxicity of unconjugated bilirubin. Pediatr Res 51: 535-541.
26. Falcão AS, Fernandes A, Brito MA, Silva RF, Brites D (2005) Bilirubin-induced inflammatory response, glutamate release, and cell death in rat cortical astrocytes are enhanced in younger cells. Neurobiol Dis 20: 199-206.
27. Fernandes A, Falcão AS, Silva RF, Gordo AC, Gama MJ, et al. (2006) Inflammatory signalling pathways involved in astroglial activation by unconjugated bilirubin. J Neurochem 96: 1667-1679.
28. Bellinger FP, Madamba S, Siggins GR (1993) Interleukin-1β inhibits synaptic strength and long-term potentiation in the rat CA1 hippocampus. Brain Res 628: 227-234.
29. Lynch MA (1998) Analysis of the mechanisms underlying the age-related impairment in long-term potentiation in the rat. Rev Neurosci 9: 169-201.
30. Albensi BC, Mattson MP (2000) Evidence for the involvement of TNF and NF-κB in hippocampal synaptic plasticity. Synapse 35: 151-159.
31. 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.
32. 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.
33. Hankø E, Hansen TW, Almaas R, Paulsen R, Rootwelt T (2006) Synergistic protection of a general caspase inhibitor and MK-801 in bilirubin-induced cell death in human NT2-N neurons. Pediatr Res 59: 72-77.
34. Bi R, Bi X, Baudry M (1998) Phosphorylation regulates calpain-mediated truncation of glutamate ionotropic receptors. Brain Res 797: 154-158.
35. Guttmann RP, Sokol S, Baker DL, Simpkins KL, Dong Y, et al. (2002) Proteolysis of the N-methyl-D-aspartate receptor by calpain in situ. J Pharmacol Exp Ther 302: 1023-1030.
36. Simpkins KL, Guttmann RP, Dong Y, Chen Z, Sokol S, et al. (2003) Selective activation induced cleavage of the NR2B subunit by calpain. J Neurosci 23: 11322-11331.
37. Guttmann RP, Baker DL, Seifert KM, Cohen AS, Coulter DA, et al. (2001) Specific proteolysis of the NR2 subunit at multiple sites by calpain. J Neurochem 78: 1083-1093.
38. Guttmann RP, Johnson GV (1998) Oxidative stress inhibits calpain activity in situ. J Biol Chem 273: 13331-13338.
39. Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, et al. (2004) Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304: 1021-1024.
40. Massey PV, Johnson BE, Moult PR, Auberson YP, Brown MW, et al. (2004) Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J Neurosci 24: 7821-7828.
41. Hansen TW, Paulsen O, Gjerstad L, Bratlid D (1988) Short-term exposure to bilirubin reduces synaptic activation in rat transverse hippocampal slices. Pediatr Res 23: 453-456.
42. Zhang L, Liu W, Tanswell AK, Luo X (2003) The effects of bilirubin on evoked potentials and long-term potentiation in rat hippocampus in vivo. Pediatr Res 53: 939-944.
43. Hansen TW, Bratlid D, Walaas SI (1988) Bilirubin decreases phosphorylation of synapsin I, a synaptic vesicle-associated neuronal phosphoprotein, in intact synaptosomes from rat cerebral cortex. Pediatr Res 23: 219-223.
44. Hilfiker S, Pieribone VA, Czernik AJ, Kao HT, Augustine GJ, et al. (1999) Synapsins as regulators of neurotransmitter release. Philos Trans R Soc Lond B Biol Sci 354: 269-279.
45. Silva R, Mata LR, Gulbenkian S, Brito MA, Tiribelli C, et al. (1999) Inhibition of glutamate uptake by unconjugated bilirubin in cultured cortical rat astrocytes: role of concentration and pH. Biochem Biophys Res Commun 265: 67-72.
46. 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.
47. Bernardino L, Xapelli S, Silva AP, Jakobsen B, Poulsen FR, et al. (2005) Modulator effects of interleukin-1β and tumor necrosis factor-α on AMPA-induced excitotoxicity in mouse organotypic hippocampal slice cultures. J Neurosci 25: 6734-6744.
48. Huuskonen J, Suuronen T, Miettinen R, van Groen T, Salminen A (2006) A refined in vitro model to study inflammatory responses in organotypic membrane culture of postnatal rat hippocampal slices. J Neuroinflammation 2: 25.
49. Dennery PA, Seidman DS, Stevenson DK (2001) Neonatal hyperbilirubinemia. N Engl J Med 344: 581-590.
50. Ostrow JD, Pascolo L, Tiribelli C (2003) Reassessment of the unbound concentrations of unconjugated bilirubin in relation to neurotoxicity in vitro. Pediatr Res 54: 98-104.
51. Shapiro SM (2003) Bilirubin toxicity in the developing nervous system. Pediatr Neurol 29: 410-421.
52. Ip S, Chung M, Kulig J, O'Brien R, Sege R, et al. (2004) An evidence-based review of important issues concerning neonatal hyperbilirubinemia. Pediatrics 114: e130-153.
53. Rodrigues CM, Solá S, Castro RE, Laires PA, Brites D, et al. (2002) Perturbation of membrane dynamics in nerve cells as an early event during bilirubin-induced apoptosis. J Lipid Res 43: 885-894.
54. Hahm JS, Ostrow JD, Mukerjee P, Celic L (1992) Ionization and self-association of unconjugated bilirubin, determined by rapid solvent partition from chloroform, with further studies of bilirubin solubility. J Lipid Res 33: 1123-3117.
55. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37: 173-182.
56. Chen SF, Huang CC, Wu HM, Chen SH, Liang YC, et al. (2004) Seizure, neuron loss, and mossy fiber sprouting in herpes simplex virus type 1-infected organotypic hippocampal cultures. Epilepsia 45: 322-332.
57. Dobbing J (1981) The later development of the brain and its vulnerability. In: Davis JA, ed. Scientific Foundations of Paediatrics. London: Heinemann. pp 744-759.
58. McDonagh AF (1979) Bile pigment: bilatrienes and 5,15 biladienes. In: Dolphin D, ed. The porphyrins. New Work: Academic Press. pp 294-491.
59. Weisiger RA, Ostrow JD, Koehler RK, Webster CC, Mukerjee P, et al. (2001) Affinity of human serum albumin for bilirubin varies with albumin concentration and buffer composition: results of a novel ultrafiltration method. J Biol Chem 276: 29953-29960.
60. Huang CC, Liang YC, Hsu KS (1999) A role for extracellular adenosine in time-dependent reversal of long-term potentiation by low-frequency stimulation at hippocampal CA1 synapses. J Neurosci 19: 9728-9738.
61. Pickering C, Gustafsson L, Cebere A, Nylander I, Liljequist S (2006) Repeated maternal separation of male Wistar rats alters glutamate receptor expression in the hippocampus but not the prefrontal cortex. Brain Res 1099: 101-108.
62. Ku HY, Huang YF, Chao PH, Huang CC, Hsu KS (2008) Neonatal isolation delays the developmental decline of long-term depression in the CA1 region of rat hippocampus. Neuropsychopharmacology 33: 2847-2859.