Developmental Febrile Seizures Modulate Hippocampal Gene Expression of Hyperpolarization-Activated Channels in an Isoform- and Cell-Specific Manner

Journal of Neuroscience

Volumn 22, Issue 11, 2002, Pages 4591-4599

  Brewster, Amy ^a   Bender, Roland A ^a   Chen, Yuncai ^a   Dube, Celine ^a   Eghbal Ahmadi, Mariam ^a   Baram, Tallie Z ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Channels; Development; Epilepsy; Febrile seizures; HCN; Hippocampus; Hyperpolarization; Neuroplasticity

Indexed keywords

BRAIN PROTEIN; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL PROTEIN; ION CHANNEL; MESSENGER RNA; UNCLASSIFIED DRUG; HCN2 POTASSIUM CHANNEL; HCN4 PROTEIN, HUMAN; HYPERPOLARIZATION ACTIVATED CATION CHANNEL; HYPERPOLARIZATION-ACTIVATED CATION CHANNEL; ISOPROTEIN; MUSCLE PROTEIN;

AGE DISTRIBUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL ACTIVITY; CELL KINETICS; CELL SPECIFICITY; CONTROLLED STUDY; CORRELATION ANALYSIS; DEVELOPMENTAL DISORDER; FEBRILE CONVULSION; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HYPERPOLARIZATION; HYPERTHERMIA; INTERNEURON; MEMBRANE CURRENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEIZURE SUSCEPTIBILITY; TRANSCRIPTION REGULATION; AGING; ANIMAL; ANTIBODY SPECIFICITY; CYTOLOGY; DISEASE MODEL; GENETICS; HYPERTHERMIC THERAPY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; NERVE CELL; PATHOPHYSIOLOGY; PYRAMIDAL NERVE CELL; SPRAGUE DAWLEY RAT;

AGING; ANIMALS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; HYPERTHERMIA, INDUCED; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERNEURONS; ION CHANNELS; MUSCLE PROTEINS; NEURONS; ORGAN SPECIFICITY; PHENOTYPE; PROTEIN ISOFORMS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SEIZURES, FEBRILE;

EID: 0036616875     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-11-04591.2002     Document Type: Article

References (57)

1. Baram TZ, Hatalski CG (1998) Neuropeptide-mediated excitability: a key triggering mechanism for seizure generation in the developing brain. Trends Neurosci 21:471-476.
2. Bender RA, Baram TZ (2002) Do prolonged febrile seizures injure hippocampal neurons? Insights from animal models. In: Febrile seizures (Baram TZ, Shinnar S, eds), pp 127-137. San Diego: Academic.
3. Bender RA, Dubé C, Baram TZ (2000) Mossy fiber sprouting into the inner molecular layer of the dentate gyrus follows prolonged febrile seizures in the immature rat model. Epilepsia 41 [Suppl 7]:76.
4. Bender RA, Brewster A, Santoro B, Ludwig A, Hofmann F, Biel M, Baram TZ (2001) Differential and age-dependent expression of hyperpolarization-activated, cyclic nucleotide-gated cation channel isoforms 1-4 suggests evolving roles in the developing rat hippocampus. Neuroscience 106:689-698.
5. Biervert C, Schroeder BC, Kubisch C, Berkovic SF, Propping P, Jentsch TJ, Steinlein OK (1998) A potassium channel mutation in neonatal human epilepsy. Science 279:403-406.
6. Brauer AU, Savaskan NE, Kole MH, Plaschke M, Monteggia LM, Nestler EJ, Simburger E, Deisz RA, Ninneman O, Nitsch R (2001) Molecular and functional analysis of hyperpolarization-activated pacemaker channels in the hippocampus after entorhinal cortex lesion. FASEB J 15:2689-2701.
7. Brunson KL, Schultz L, Baram TZ (1998) 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 111:119-128.
8. Brunson KL, Eghbal-Ahmadi M, Bender RA, Chen Y, Baram TZ (2001) Long-term, progressive hippocampal cell loss and dysfunction induced by early-life administration of corticotropin-releasing hormone reproduce the effects of early-life stress. Proc Natl Acad Sci USA 98:8856-8861.
9. Burgess DL, Noebels JL (1999) Voltage-dependent calcium channel mutations in neurological disease. Ann NY Acad Sci 868:199-212.
10. Cendes F, Andermann F (2002) Do febrile seizures promote temporal lobe epilepsy? Retrospective studies. In: Febrile seizures (Baram TZ, Shinnar S, eds), pp 77-86. San Diego: Academic.
11. Charlier C, Singh NA, Ryan SG, Lewis TB, Reus BE, Leach RJ, Leppert M (1998) A pore mutation in a novel KQT-like potassium channel gene in an idiopathic epilepsy family. Nat Genet 18:53-55.
12. Chen K, Baram TZ, Soltesz I (1999) Febrile seizures in the developing brain result in persistent modification of neuronal excitability in limbic circuits. Nat Med 5:888-894.
13. Chen K, Aradi I, Thon N, Eghbal-Ahmadi M, Baram TZ, Soltesz I (2001) Persistently modified h-channels after complex febrile seizures convert the seizure-induced enhancement of inhibition to hyperexcitability. Nat Med 7:331-337.
14. Chen S, Wang J, Siegelbaum SA (2001) Properties of hyperpolarization-activated pacemaker current defined by coassembly of HCN1 and HCN2 subunits and basal modulation by cyclic nucleotide. J Gen Physiol 117:491-503.
15. Chen Y, Bender RA, Frotscher M, Baram TZ (2001) Novel and transient populations of corticotropin-releasing hormone-expressing neurons in developing hippocampus suggest unique functional roles: a quantitative spatiotemporal analysis. J Neurosci 21:7171-7181.
16. DiFrancesco D (1993) Pacemaker mechanisms in cardiac tissue. Annu Rev Physiol 55:455-472.
17. DiFrancesco D, Tortora P (1991) Direct activation of cardiac pacemaker channels by intracellular cyclic AMP. Nature 351:145-147.
18. Dubé C (2002) Do prolonged febrile seizures in an immature rat model cause epilepsy? In: Febrile seizures (Baram TZ, Shinnar S, eds), pp 215-229. San Diego: Academic.
19. Dubé C, Chen K, Eghbal-Ahmadi M, Brunson K, Soltesz I, Baram TZ (2000) Prolonged febrile seizures in the immature rat model enhance hippocampal excitability long term. Ann Neurol 47:336-344.
20. 2) in hypothalamus and amygdala of the immature rat by sensory input and food intake. J Neurosci 19:3982-3991.
21. Eghbal-Ahmadi M, Yin H, Stafstrom CE, Tran K, Weiss JH, Baram TZ (2001) Altered expression of specific AMPA type glutamate receptor subunits after prolonged experimental febrile seizures in CA3 of immature rat hippocampus. Soc Neurosci Abstr 31:684.6.
22. Escayg A, MacDonald BT, Meisler MH, Baulac S, Huberfeld G, AnGourfinkel I, Brice A, LeGuern E, Moulard B, Chaigne D, Buresi C, Malafosse A (2000) Mutations of SCN1A, encoding a neuronal sodium channel, in two families with GEFS+2. Nat Genet 24:343-345.
23. Franz O, Liss B, Neu A, Roeper J (2000) Single-cell mRNA expression of HCN1 correlates with a fast gating phenotype of hyperpolarization-activated cyclic nucleotide-gated ion channels (Ih) in central neurons. Eur J Neurosci 12:2685-2693.
24. Friedman LK, Sperber EF, Moshe SL, Bennett MV, Zukin RS (1997) Developmental regulation of glutamate and GABA(A) receptor gene expression in rat hippocampus following kainate-induced status epilepticus. Dev Neurosci 19:529-542.
25. Gauss R, Seifert R, Kaupp UB (1998) Molecular identification of a hyperpolarization-activated channel in sea urchin sperm. Nature 393:583-587.
26. Gottlieb A, Keydar I, Epstein HT (1977) Rodent brain growth stages: an analytical review. Biol Neonate 32:166-176.
27. Hatalski CG, Brunson KL, Tantayanubutr B, Chen Y, Baram TZ (2000) Neuronal activity and stress differently regulate hippocampal and hypothalamic corticotropin-releasing hormone expression in the immature rat. Neuroscience 101:571-580.
28. Hauser WA (1994) The prevalence and incidence of convulsive disorders in children. Epilepsia 35 [Suppl 2]:S1-S6.
29. Herschkowitz N, Kagan J, Zilles K (1997) Neurobiological bases of behavioral development in the first year. Neuropediatrics 28:296-306.
30. Holmes GL, Thompson JL, Marchi T, Feldman DS (1988) Behavioral effects of kainic acid administration on the immature brain. Epilepsia 29:721-730.
31. Hunyady B, Krempels K, Harta G, Mezey É (1996) Immunohistochemical signal amplification by catalyzed reporter deposition and its application in double immunostaining. J Histochem Cytochem 44:1353-1362.
32. Ishii TM, Takano M, Xie LH, Noma A, Ohmori H (1999) Molecular characterization of the hyperpolarization-activated cation channel in rabbit heart sinoatrial node. J Biol Chem 274:12835-12839.
33. Ludwig A, Zong X, Jeglitsch M, Hofmann F, Biel M (1998) A familv of hyperpolarization-activated mammalian cation channels. Nature 393:587-591.
34. Lupica CR, Bell JA, Hoffman AF, Watson PL (2001) Contribution of the hyperpolarization-activated current (Ih) to membrane potential and GABA release in hippocampal interneurons. J Neurophysiol 86:261-268.
35. Lynch M, Sayin Ü, Bownds J, Janumpalli S, Sutula T (2000) Long-term consequences of early postnatal seizures on hippocampal learning and plasticity. Eur J Neurosci 12:2252-2264.
36. h) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurons. J Physiol (Lond) 497:119-130.
37. Monteggia LM, Eisch AJ, Tang MD, Kaczmarek LK, Nestler EJ (2000) Cloning and localization of the hyperpolarization-activated cyclic nucleotide-gated channel family in rat brain. Brain Res Mol Brain Res 81:129-139.
38. Moosmang S, Biel M, Hofmann F, Ludwig A (1999) Differential distribution of four hyperpolarization-activated cation channels in mouse brains. Biol Chem 380:975-980.
39. Pachucki J, Burmeister LA, Larsen PR (1999) Thyroid hormone regulates hyperpolarization-activated cyclic nucleotide-gated channel (HCN2) mRNA in the rat heart. Circ Res 85:498-503.
40. Pape HC (1996) Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Annu Rev Physiol 58:299-327.
41. H. Soc Neurosci Abstr 31:605.2.
42. Sanchez RM, Koh S, Rio C, Wang C, Lamperti ED, Sharma D, Corfas G, Jensen FE (2001) Decreased glutamate receptor 2 expression and enhanced epileptogenesis in immature rat hippocampus after perinatal hypoxia-induced seizures. J Neurosci 21:8154-8163.
43. Santoro B, Tibbs GR (1999) The HCN gene family: molecular basis of the hyperpolarization-activated pacemaker channels. Ann NY Acad Sci 868:741-764.
44. Santoro B, Grant SGN, Bartsch D, Kandel ER (1997) Interactive cloning with the SH3 domain of N-src identifies a new brain specific ion channel protein, with homology to Eag and cyclic nucleotide-gated channels. Proc Natl Acad Sci USA 94:14815-14820.
45. Santoro B, Liu D, Yao H, Bartsch D, Kandel ER, Siegelbaum SA, Tibbs GR (1998) Identification of a gene encoding a hyperpolarization-activated pacemaker channel of brain. Cell 93:717-729.
46. Santoro B, Chen S, Lüthi A, Pavlidis P, Shumyatsky GP, Tibbs GR, Siegelbaum SA (2000) Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J Neurosci 20:5264-5275.
47. Sarkisian MR, Tandon P, Liu Z, Yang Y, Hori A, Holmes GL, Stafstrom CE (1997) Multiple kainic acid seizures in the immature and adult brain: ictal manifestations and long-term effects on learning and memory. Epilepsia 38:1157-1166.
48. Schroeder BC, Kubisch C, Stein V, Jentsch TJ (1998) Moderate loss of function of cyclic-AMP-modulated KCNQ2/KCNQ3 K+ channels causes epilepsy. Nature 396:687-690.
49. Shinnar S (1998) Prolonged febrile seizures and mesial temporal sclerosis. Ann Neurol 43:411-412.
50. Stafstrom CE, Chronopoulos A, Thurber S, Thompson JL, Holmes GL (1993) Age-dependent cognitive and behavioral deficits after kainic acid seizures. Epilepsia 34:420-432.
51. Toth Z, Yan XX, Haftoglou S, Ribak CE, Baram TZ (1998) Seizure-induced neuronal injury: vulnerability to febrile seizures in an immature rat model. J Neurosci 18:4285-4294.
52. Tremblay E, Nitecka L, Berger ML, Ben-Ari Y (1984) Maturation of kainic acid seizure-brain damage syndrome in the rat. I. Clinical, electrographic and metabolic observations. Neuroscience 13:1051-1072.
53. Ulens C, Tytgat J (2001) Functional heteromerization of HCN1 and HCN2 pacemaker channels. J Biol Chem 276:6069-6072.
54. Waigner BJ, DeGennaro M, Santoro B, Siegelbaum SA, Tibbs GR (2001) Molecular mechanism of cAMP modulation of HCN pacemaker channels. Nature 411:805-809.
55. Walker MC, Kullmann DM (1999) Febrile convulsions: a "benign" condition? Nat Med 5:871-872.
56. Wallace RH, Wang DW, Singh R, Scheffer IE, George Jr AL, Phillips HA, Saar K, Reis A, Johnson EW, Sutherland GR, Berkovic SF, Mulley JC (1998) Febrile seizures and generalized epilepsy associated with a mutation in the Na+-channel β1 subunit gene SCN1B. Nat Genet 19:366-370.
57. Zuberi SM, Eunson LH, Spauschus A, De Silva R, Tolmie J, Wood NW, McWilliam RC, Stephenson JP, Kullmann DM, Hanna MG (1999) A novel mutation in the human voltage-gated potassium channel gene (Kv1.1) associates with episodic ataxia type 1 and sometimes with partial epilepsy. Brain 122:817-825.