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PMID: 12783416 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Mitochondrial uncoupling protein-2 protects the immature brain from excitotoxic neuronal death.

Annals of neurology ·Vol. 53 ·No. 6 ·2003-06-00 ·Pages 711-7

Sullivan PG, Dubé C, Dorenbos K, Steward O, Baram TZ

Abstract

Excitotoxic cell death is the fundamental process responsible for many human neurodegenerative disorders, yet the basic mechanisms involved are not fully understood. Here, we exploited the fact that the immature brain is remarkably resistant to seizure-induced excitotoxic cell death and examined the underlying protective mechanisms. We found that, unlike in the adult, seizures do not increase the formation of reactive oxygen species or result in mitochondrial dysfunction in neonatal brain, because of high levels of the mitochondrial uncoupling protein (UCP2). UCP2 expression and function were basally increased in neonatal brain by the fat-rich diet of maternal milk, and substituting a low-fat diet reduced UCP2, restored mitochondrial coupling, and permitted seizure-induced neuronal injury. Thus, modulation of UCP2 expression and function by dietary fat protects neonatal neurons from excitotoxicity by preventing mitochondrial dysfunction. This mechanism offers novel neuroprotective strategies for individuals, greater than 1% of the world's population, who are affected by seizures.

MeSH Terms
Age Factors Animals Animals, Newborn Antibodies/immunology Carrier Proteins/immunology,metabolism Cell Death/drug effects Hippocampus/drug effects,metabolism,pathology Immunohistochemistry Ion Channels Kainic Acid/adverse effects,antagonists & inhibitors Limbic System/drug effects,metabolism,pathology Membrane Proteins/immunology,metabolism Membrane Transport Proteins Mitochondrial Proteins Neurons/drug effects,metabolism,pathology Neurotoxins/adverse effects,antagonists & inhibitors Proteins/immunology,metabolism Rats Rats, Sprague-Dawley Reactive Oxygen Species/metabolism Seizures/chemically induced Uncoupling Protein 1 Uncoupling Protein 2
Chemicals
Antibodies Carrier Proteins Ion Channels Membrane Proteins Membrane Transport Proteins Mitochondrial Proteins Neurotoxins Proteins Reactive Oxygen Species UCP2 protein, human Ucp2 protein, rat Uncoupling Protein 1 Uncoupling Protein 2 Kainic Acid
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Sullivan Patrick G
Department of Neurobiology and Behavior, University of California at Irvine, Irvine, CA 92697-4475, USA.
Dubé Celine
Dorenbos Kristina
Steward Oswald
Baram Tallie Z
References (58)
58 references, click to expand
  1. Maturation of kainic acid seizure-brain damage syndrome in the rat. II. Histopathological sequelae.
    Neuroscience. 1984 Dec;13(4):1073-94 PMID: 6527790
  2. Excitotoxic mechanisms of epileptic brain damage.
    Adv Neurol. 1986;44:857-77 PMID: 3706027
  3. Hippocampal neuron loss in temporal lobe epilepsy: correlation with early childhood convulsions.
    Ann Neurol. 1987 Sep;22(3):334-40 PMID: 3674798
  4. Autoradiographic measurement of local cerebral beta-hydroxybutyrate uptake in the rat during postnatal development.
    Neuroscience. 1991;40(3):871-8 PMID: 2062444
  5. The prevalence and incidence of convulsive disorders in children.
    Epilepsia. 1994;35 Suppl 2:S1-6 PMID: 8275976
  6. Quinolinate-induced injury is enhanced in developing rat brain.
    Brain Res Dev Brain Res. 1994 Dec 16;83(2):224-32 PMID: 7697883
  7. Involvement of free radicals in excitotoxicity in vivo.
    J Neurochem. 1995 May;64(5):2239-47 PMID: 7536809
  8. Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation.
    J Neurosci. 1995 May;15(5 Pt 1):3318-27 PMID: 7751912
  9. Unprovoked seizures and developmental disabilities: clinical characteristics of children referred to a child development center.
    Pediatr Neurol. 1995 Oct;13(3):235-41 PMID: 8554661
  10. Requirement for superoxide in excitotoxic cell death.
    Neuron. 1996 Feb;16(2):345-55 PMID: 8789949
  11. Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants.
    Q Rev Biophys. 1996 May;29(2):169-202 PMID: 8870073
  12. Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration.
    Brain Res. 1997 Mar 14;751(1):37-46 PMID: 9098566
  13. Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches.
    Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):4103-8 PMID: 9108112
  14. Status epilepticus.
    N Engl J Med. 1998 Apr 2;338(14):970-6 PMID: 9521986
  15. Recurrent seizures may cause hippocampal damage in temporal lobe epilepsy.
    Neurology. 1998 May;50(5):1377-82 PMID: 9595990
  16. Seizure-induced neuronal injury: vulnerability to febrile seizures in an immature rat model.
    J Neurosci. 1998 Jun 1;18(11):4285-94 PMID: 9592105
  17. Distribution of the uncoupling protein 2 mRNA in the mouse brain.
    J Comp Neurol. 1998 Aug 10;397(4):549-60 PMID: 9699915
  18. Patterns of status epilepticus-induced neuronal injury during development and long-term consequences.
    J Neurosci. 1998 Oct 15;18(20):8382-93 PMID: 9763481
  19. The in vivo proconvulsant effects of corticotropin releasing hormone in the developing rat are independent of ionotropic glutamate receptor activation.
    Brain Res Dev Brain Res. 1998 Nov 1;111(1):119-28 PMID: 9804917
  20. Neuropeptide-mediated excitability: a key triggering mechanism for seizure generation in the developing brain.
    Trends Neurosci. 1998 Nov;21(11):471-6 PMID: 9829688
  21. Seizures in the developing brain: perhaps not so benign after all.
    Neuron. 1998 Dec;21(6):1231-4 PMID: 9883716
  22. Mitochondrial disease in superoxide dismutase 2 mutant mice.
    Proc Natl Acad Sci U S A. 1999 Feb 2;96(3):846-51 PMID: 9927656
  23. Correlation between hypermetabolism and neuronal damage during status epilepticus induced by lithium and pilocarpine in immature and adult rats.
    J Cereb Blood Flow Metab. 1999 Feb;19(2):195-209 PMID: 10027775
  24. Glutamate-induced neuron death requires mitochondrial calcium uptake.
    Nat Neurosci. 1998 Sep;1(5):366-73 PMID: 10196525
  25. Progression in mesial temporal lobe epilepsy.
    Ann Neurol. 1999 May;45(5):553-6 PMID: 10319875
  26. Differential regulation of the expression of corticotropin-releasing factor receptor type 2 (CRF2) in hypothalamus and amygdala of the immature rat by sensory input and food intake.
    J Neurosci. 1999 May 15;19(10):3982-91 PMID: 10234028
  27. EUK-134, a synthetic superoxide dismutase and catalase mimetic, prevents oxidative stress and attenuates kainate-induced neuropathology.
    Proc Natl Acad Sci U S A. 1999 Aug 17;96(17):9897-902 PMID: 10449791
  28. Basic mechanisms of status epilepticus.
    Adv Neurol. 1999;79:725-33 PMID: 10514858
  29. Brain uncoupling protein 2: uncoupled neuronal mitochondria predict thermal synapses in homeostatic centers.
    J Neurosci. 1999 Dec 1;19(23):10417-27 PMID: 10575039
  30. Animal models of the ketogenic diet: what have we learned, what can we learn?
    Epilepsy Res. 1999 Dec;37(3):241-59 PMID: 10584974
  31. Prolonged febrile seizures in the immature rat model enhance hippocampal excitability long term.
    Ann Neurol. 2000 Mar;47(3):336-44 PMID: 10716253
  32. Mitochondrial membrane potential and neuronal glutamate excitotoxicity: mortality and millivolts.
    Trends Neurosci. 2000 Apr;23(4):166-74 PMID: 10717676
  33. Energy metabolism in uncoupling protein 3 gene knockout mice.
    J Biol Chem. 2000 May 26;275(21):16258-66 PMID: 10748196
  34. Energetics in the pathogenesis of neurodegenerative diseases.
    Trends Neurosci. 2000 Jul;23(7):298-304 PMID: 10856939
  35. Dietary supplement creatine protects against traumatic brain injury.
    Ann Neurol. 2000 Nov;48(5):723-9 PMID: 11079535
  36. Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production.
    Nat Genet. 2000 Dec;26(4):435-9 PMID: 11101840
  37. Mitochondrial superoxide production in kainate-induced hippocampal damage.
    Neuroscience. 2000;101(3):563-70 PMID: 11113305
  38. Brain development and generation of brain pathologies.
    Int Rev Neurobiol. 2001;45:17-41 PMID: 11130898
  39. Status epilepticus causes necrotic damage in the mediodorsal nucleus of the thalamus in immature rats.
    J Neurosci. 2001 May 15;21(10):3593-9 PMID: 11331388
  40. More evidence for seizure-induced neuron loss: is hippocampal sclerosis both cause and effect of epilepsy?
    Neurology. 2001 Jul 24;57(2):169-70 PMID: 11468296
  41. Novel and transient populations of corticotropin-releasing hormone-expressing neurons in developing hippocampus suggest unique functional roles: a quantitative spatiotemporal analysis.
    J Neurosci. 2001 Sep 15;21(18):7171-81 PMID: 11549728
  42. DeltaPsi(m)-Dependent and -independent production of reactive oxygen species by rat brain mitochondria.
    J Neurochem. 2001 Oct;79(2):266-77 PMID: 11677254
  43. Mechanism of uncoupling protein action.
    Biochem Soc Trans. 2001 Nov;29(Pt 6):803-6 PMID: 11709078
  44. Uncoupling protein 2 in the brain: distribution and function.
    Biochem Soc Trans. 2001 Nov;29(Pt 6):812-7 PMID: 11709080
  45. Superoxide activates mitochondrial uncoupling proteins.
    Nature. 2002 Jan 3;415(6867):96-9 PMID: 11780125
  46. Resistance of immature hippocampus to morphologic and physiologic alterations following status epilepticus or kindling.
    Hippocampus. 2001;11(6):615-25 PMID: 11811655
  47. Induction of uncoupling protein 2 mRNA in beta-cells is stimulated by oxidation of fatty acids but not by nutrient oversupply.
    Endocrinology. 2002 Apr;143(4):1371-7 PMID: 11897694
  48. Calcium-induced cytochrome c release from CNS mitochondria is associated with the permeability transition and rupture of the outer membrane.
    J Neurochem. 2002 Jan;80(2):207-18 PMID: 11902111
  49. Mitochondrial dysfunction associated with neuronal death following status epilepticus in rat.
    Epilepsy Res. 2002 Feb;48(3):157-68 PMID: 11904234
  50. Cognitive outcomes and predictive factors in epilepsy.
    Neurology. 2002 Apr 23;58(8 Suppl 5):S21-6 PMID: 11971129
  51. Developmental febrile seizures modulate hippocampal gene expression of hyperpolarization-activated channels in an isoform- and cell-specific manner.
    J Neurosci. 2002 Jun 1;22(11):4591-9 PMID: 12040066
  52. Progression of neuronal damage after status epilepticus and during spontaneous seizures in a rat model of temporal lobe epilepsy.
    Prog Brain Res. 2002;135:67-83 PMID: 12143371
  53. Repeated brief seizures induce progressive hippocampal neuron loss and memory deficits.
    Prog Brain Res. 2002;135:95-110 PMID: 12143373
  54. Hippocampal neuron damage in human epilepsy: Meyer's hypothesis revisited.
    Prog Brain Res. 2002;135:237-51 PMID: 12143344
  55. Is neuronal death required for seizure-induced epileptogenesis in the immature brain?
    Prog Brain Res. 2002;135:365-75 PMID: 12143355
  56. Brain mitochondrial uncoupling protein 2 (UCP2): a protective stress signal in neuronal injury.
    Biochem Pharmacol. 2002 Aug 1;64(3):363-7 PMID: 12147286
  57. Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: a histological study.
    Neuroscience. 1980;5(6):991-1014 PMID: 7402461
  58. Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy.
    Neuroscience. 1981;6(7):1361-91 PMID: 7266871
Article Info
Journal
Annals of neurology
Abbr.
Ann Neurol
ISSN
0364-5134
Published
2003-06-00
Pages
711-7
Language
English
Region
United States
NLM ID
7707449
PMCID
PMC2930774
Subset
IM
Grants
NINDS NIH HHS · R01 NS035439-06 · United States
NINDS NIH HHS · R01 NS028912-08 · United States
NINDS NIH HHS · R01 NS035439 · United States
NINDS NIH HHS · T32 NS007444 · United States
NINDS NIH HHS · R01 NS028912-09 · United States
NINDS NIH HHS · NS35439 · United States
NINDS NIH HHS · R37 NS035439 · United States
NINDS NIH HHS · NS07444 · United States
NINDS NIH HHS · NS28912 · United States
NINDS NIH HHS · R01 NS035439-05 · United States
NINDS NIH HHS · R01 NS028912 · United States
NINDS NIH HHS · NS32280 · United States
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