Nuclear factor-κB regulates seizure threshold and gene transcription following convulsant stimulation

Journal of Neurochemistry

Volumn 103, Issue 4, 2007, Pages 1381-1395

  Lubin, Farah D ^a,b   Ren, Yajun ^a   Xu, Xianghua ^a,c   Anderson, Anne E ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama ^*  (United States)

Author keywords

Hippocampus; Kainate; Seizures; Status epilepticus; Transcriptional regulation

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DNA; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; PROTEIN P50; TRANSCRIPTION FACTOR RELA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CONVULSION; DISEASE PREDISPOSITION; DNA BINDING; EPILEPTIC STATE; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HIPPOCAMPUS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SEIZURE; SIGNAL PROCESSING; UPREGULATION;

ANIMALS; CONVULSANTS; KAINIC ACID; MALE; NF-KAPPA B; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

ANIMALIA;

EID: 35448940367     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04863.x     Document Type: Article

References (78)

1. Aid T., Kazantseva A., Piirsoo M., Palm K. Timmusk T. (2007) Mouse and rat BDNF gene structure and expression revisited. J. Neurosci. Res. 85, 525 535.
2. Albensi B. C. (2001) Potential roles for tumor necrosis factor and nuclear factor-kappa B in seizure activity. J. Neurosci. Res. 66, 151 154.
3. Albensi B. C. Mattson M. P. (2000) Evidence for the involvement of TNF and NF-kappa B in hippocampal synaptic plasticity. Synapse 35, 151 159.
4. Angelov D., Lenouvel F., Hans F., Muller C. W., Bouvet P., Bednar J., Moudrianakis E. N., Cadet J. Dimitrov S. (2004) The histone octamer is invisible when NF-kappa B binds to the nucleosome. J. Biol. Chem. 279, 42374 42382.
5. Baldwin Jr. A. S. (1996) The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu. Rev. Immunol. 14, 649 683.
6. Bazan N. G. Serou M. J. (1999) Second messengers, long-term potentiation, gene expression and epileptogenesis. Adv. Neurol. 79, 659 664.
7. Becker A. J., Chen J., Zien A., Sochivko D., Normann S., Schramm J., Elger C. E., Wiestler O. D. Blumcke I. (2003) Correlated stage- and subfield-associated hippocampal gene expression patterns in experimental and human temporal lobe epilepsy. Eur. J. Neurosci. 18, 2792 2802.
8. Bernard C., Anderson A., Becker A., Poolos N. P., Beck H. Johnston D. (2004) Acquired dendritic channelopathy in temporal lobe epilepsy. Science 305, 532 535.
9. Binder D. K. (2004) The role of BDNF in epilepsy and other diseases of the mature nervous system. Adv. Exp. Med. Biol. 548, 34 56.
10. Binder D. K., Routbort M. J., Ryan T. E., Yancopoulos G. D. McNamara J. O. (1999) Selective inhibition of kindling development by intraventricular administration of TrkB receptor body. J. Neurosci. 19, 1424 1436.
11. Binder D. K., Croll S. D., Gall C. M. Scharfman H. E. (2001) BDNF and epilepsy: too much of a good thing? Trends Neurosci. 24, 47 53.
12. Blondeau N., Widmann C., Lazdunski M. Heurteaux C. (2001) Activation of the nuclear factor-kappa B is a key event in brain tolerance. J. Neurosci. 21, 4668 4677.
13. Bonizzi G., Bebien M., Otero D. C. et al. (2004) Activation of IKK alpha target genes depends on recognition of specific kappa B binding sites by RelB:p52 dimers. EMBO J. 23, 4202 4210.
14. Chen Y. Q., Ghosh S. Ghosh G. (1998) A novel DNA recognition mode by the NF-kappa B p65 homodimer. Nat. Struct. Biol. 5, 67 73.
15. Chen Z., Gardi J., Kushikata T., Fang J. Krueger J. M. (1999) Nuclear factor-kappa B-like activity increases in murine cerebral cortex after sleep deprivation. Am. J. Physiol. 276, R1812 R1818.
16. Chen J., Sochivko D., Beck H., Marechal D., Wiestler O. D. Becker A. J. (2001) Activity-induced expression of common reference genes in individual CNS neurons. Lab. Invest. 81, 913 916.
17. Denk A., Wirth T. Baumann B. (2000) NF-kappa B transcription factors: critical regulators of hematopoiesis and neuronal survival. Cytokine Growth Factor Rev. 11, 303 320.
18. DiDonato J. A., Hayakawa M., Rothwarf D. M., Zandi E. Karin M. (1997) A cytokine-responsive I kappa B kinase that activates the transcription factor NF-kappa B. Nature 388, 548 554.
19. Dugich-Djordjevic M. M., Tocco G., Willoughby D. A., Najm I., Pasinetti G., Thompson R. F., Baudry M., Lapchak P. A. Hefti F. (1992) BDNF mRNA expression in the developing rat brain following kainic acid-induced seizure activity. Neuron 8, 1127 1138.
20. Elliott R. C. Lowenstein D. H. (2004) Gene expression profiling of seizure disorders. Neurochem. Res. 29, 1083 1092.
21. Freudenthal R., Romano A. Routtenberg A. (2004) Transcription factor NF-kappa B activation after in vivo perforant path LTP in mouse hippocampus. Hippocampus 14, 677 683.
22. Freudenthal R., Boccia M. M., Acosta G. B., Blake M. G., Merlo E., Baratti C. M. Romano A. (2005) NF-kappa B transcription factor is required for inhibitory avoidance long-term memory in mice. Eur. J. Neurosci. 21, 2845 2852.
23. Ghosh G., van Duyne G., Ghosh S. Sigler P. B. (1995) Structure of NF-kappa B p50 homodimer bound to a kappa B site. Nature 373, 303 310.
24. Ghosh S., May M. J. Kopp E. B. (1998) NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16, 225 260.
25. Hill W. D., Hess D. C., Carroll J. E., Wakade C. G., Howard E. F., Chen Q., Cheng C., Martin-Studdard A., Waller J. L. Beswick R. A. (2001) The NF-kappa B inhibitor diethyldithiocarbamate (DDTC) increases brain cell death in a transient middle cerebral artery occlusion model of ischemia. Brain Res. Bull. 55, 375 386.
26. Hoffmann A., Leung T. H. Baltimore D. (2003) Genetic analysis of NF-kappa B/Rel transcription factors defines functional specificities. EMBO J. 22, 5530 5539.
27. Huang Y., Myers S. J. Dingledine R. (1999) Transcriptional repression by REST: recruitment of Sin3A and histone deacetylase to neuronal genes. Nat. Neurosci. 2, 867 872.
28. Huang Y., Doherty J. J. Dingledine R. (2002) Altered histone acetylation at glutamate receptor 2 and brain-derived neurotrophic factor genes is an early event triggered by status epilepticus. J. Neurosci. 22, 8422 8428.
29. Humpel C., Wetmore C. Olson L. (1993) Regulation of brain- derived neurotrophic factor messenger RNA and protein at the cellular level in pentylenetetrazol-induced epileptic seizures. Neuroscience 53, 909 918.
30. Hunsberger J. G., Bennett A. H., Selvanayagam E., Duman R. S. Newton S. S. (2005) Gene profiling the response to kainic acid induced seizures. Brain Res. Mol. Brain Res. 141, 95 112.
31. Kaltschmidt B., Uherek M., Volk B., Baeuerle P. A. Kaltschmidt C. (1997) Transcription factor NF-kappa B is activated in primary neurons by amyloid beta peptides and in neurons surrounding early plaques from patients with Alzheimer disease. Proc. Natl Acad. Sci. USA 94, 2642 2647.
32. Kent W. J. (2002) BLAT - the BLAST-like alignment tool. Genome Res. 12, 656 664.
33. Kornblum H. I., Sankar R., Shin D. H., Wasterlain C. G. Gall C. M. (1997) Induction of brain derived neurotrophic factor mRNA by seizures in neonatal and juvenile rat brain. Brain Res. Mol. Brain Res. 44, 219 228.
34. Koyama R. Ikegaya Y. (2005) To BDNF or not to BDNF: that is the epileptic hippocampus. Neuroscientist 11, 282 287.
35. Kubota T., Kushikata T., Fang J. Krueger J. M. (2000) Nuclear factor-kappa B inhibitor peptide inhibits spontaneous and interleukin-1beta- induced sleep. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279, R404 R413.
36. Kunsch C., Ruben S. M. Rosen C. A. (1992) Selection of optimal kappa B/Rel DNA-binding motifs: interaction of both subunits of NF-kappa B with DNA is required for transcriptional activation. Mol. Cell. Biol. 12, 4412 4421.
37. Larmet Y., Reibel S., Carnahan J., Nawa H., Marescaux C. Depaulis A. (1995) Protective effects of brain-derived neurotrophic factor on the development of hippocampal kindling in the rat. Neuroreport 6, 1937 1941.
38. Latimer M., Ernst M. K., Dunn L. L., Drutskaya M. Rice N. R. (1998) The N-terminal domain of I kappa B alpha masks the nuclear localization signal(s) of p50 and c-Rel homodimers. Mol. Cell. Biol. 18, 2640 2649.
39. Lauterborn J. C., Rivera S., Stinis C. T., Hayes V. Y., Isackson P. J. Gall C. M. (1996) Differential effects of protein synthesis inhibition on the activity-dependent expression of BDNF transcripts: evidence for immediate-early gene responses from specific promoters. J. Neurosci. 16, 7428 7436.
40. Le Bail O., Schmidt-Ullrich R. Israel A. (1993) Promoter analysis of the gene encoding the I kappa B-alpha/MAD3 inhibitor of NF-kappa B: positive regulation by members of the rel/NF-kappa B family. EMBO J. 12, 5043 5049.
41. Lee S. Rivier C. (2005) Role played by hypothalamic nuclear factor-κB in alcohol-mediated activation of the rat hypothalamic- pituitary-adrenal axis. Endocrinology 146, 2006 2014.
42. Lipsky R. H., Xu K., Zhu D., Kelly C., Terhakopian A., Novelli A. Marini A. M. (2001) Nuclear factor kappa B is a critical determinant in N-methyl-D-aspartate receptor-mediated neuroprotection. J. Neurochem. 78, 254 264.
43. Liu Q. R., Lu L., Zhu X. G., Gong J. P., Shaham Y. Uhl G. R. (2006) Rodent BDNF genes, novel promoters, novel splice variants, and regulation by cocaine. Brain Res. 1067, 1 12.
44. Lubin F. D., Johnston L. D., Sweatt J. D. Anderson A. E. (2005) Kainate mediates nuclear factor-kappa B activation in hippocampus via phosphatidylinositol-3 kinase and extracellular signal- regulated protein kinase. Neuroscience 133, 969 981.
45. Lukasiuk K. Pitkanen A. (2004) Large-scale analysis of gene expression in epilepsy research: is synthesis already possible? Neurochem. Res. 29, 1169 1178.
46. Maisonpierre P. C., Le Beau M. M., Espinosa R. III., Ip N. Y., Belluscio L., de la Monte S. M., Squinto S., Furth M. E. Yancopoulos G. D. (1991) Human and rat brain-derived neurotrophic factor and neurotrophin-3: gene structures, distributions, and chromosomal localizations. Genomics 10, 558 568.
47. Mattson M. P. (2005) NF-kappa B in the survival and plasticity of neurons. Neurochem. Res. 30, 883 893.
48. Mattson M. P. Camandola S. (2001) NF-kappa B in neuronal plasticity and neurodegenerative disorders. J. Clin. Invest. 107, 247 254.
49. Mattson M. P. Meffert M. K. (2006) Roles for NF-kappa B in nerve cell survival, plasticity, and disease. Cell Death Differ. 13, 852 860.
50. Metsis M., Timmusk T., Arenas E. Persson H. (1993) Differential usage of multiple brain-derived neurotrophic factor promoters in the rat brain following neuronal activation. Proc. Natl Acad. Sci. USA 90, 8802 8806.
51. Muller C. W., Rey F. A., Sodeoka M., Verdine G. L. Harrison S. C. (1995) Structure of the NF-kappa B p50 homodimer bound to DNA. Nature 373, 311 317.
52. Nanda S. Mack K. J. (1998) Multiple promoters direct stimulus and temporal specific expression of brain-derived neurotrophic factor in the somatosensory cortex. Brain Res. Mol. Brain Res. 62, 216 219.
53. O'Mahony A., Raber J., Montano M., Foehr E., Han V., Lu S. M., Kwon H., LeFevour A., Chakraborty-Sett S. Greene W. C. (2006) NF-kappa B/Rel regulates inhibitory and excitatory neuronal function and synaptic plasticity. Mol. Cell. Biol. 26, 7283 7298.
54. O'Riordan K. J., Huang I. C., Pizzi M. et al. (2006) Regulation of nuclear factor kappa B in the hippocampus by group I metabotropic glutamate receptors. J. Neurosci. 26, 4870 4879.
55. Parent J. M., Yu T. W., Leibowitz R. T., Geschwind D. H., Sloviter R. S. Lowenstein D. H. (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 17, 3727 3738.
56. Parent J. M., Elliott R. C., Pleasure S. J., Barbaro N. M. Lowenstein D. H. (2006) Aberrant seizure-induced neurogenesis in experimental temporal lobe epilepsy. Ann. Neurol. 59, 81 91.
57. Paxinos G. Watson C. (1998) The rat brain in stereotoxic coordinates. Academic Press, San Diego.
58. 2+ entry. Neuroscience 126, 665 676.
59. Qin Z. H., Wang Y., Nakai M. Chase T. N. (1998) Nuclear factor-kappa B contributes to excitotoxin-induced apoptosis in rat striatum. Mol. Pharmacol. 53, 33 42.
60. Racine R. J. (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32, 281 294.
61. Reibel S., Larmet Y., Le B. T., Carnahan J., Marescaux C. Depaulis A. (2000) Brain-derived neurotrophic factor delays hippocampal kindling in the rat. Neuroscience 100, 777 788.
62. Roberts D. S., Raol Y. H., Bandyopadhyay S., Lund I. V., Budreck E. C., Passini M. A., Wolfe J. H., Brooks-Kayal A. R. Russek S. J. (2005) Egr3 stimulation of GABRA4 promoter activity as a mechanism for seizure-induced up-regulation of GABA(A) receptor alpha4 subunit expression. Proc. Natl Acad. Sci. USA 102, 11894 11899.
63. Rong Y. Baudry M. (1996) Seizure activity results in a rapid induction of nuclear factor-kappa B in adult but not juvenile rat limbic structures. J. Neurochem. 67, 662 668.
64. Sakai R. R., Ma L. Y., He P. F. Fluharty S. J. (1995) Intracerebroventricular administration of angiotensin type 1 (AT1) receptor antisense oligonucleotides attenuate thirst in the rat. Regul. Pept. 59, 183 192.
65. Sanjabi S., Williams K. J., Saccani S., Zhou L., Hoffmann A., Ghosh G., Gerondakis S., Natoli G. Smale S. T. (2005) A c-Rel subdomain responsible for enhanced DNA-binding affinity and selective gene activation. Genes Dev. 19, 2138 2151.
66. Scharfman H., Goodman J., Macleod A., Phani S., Antonelli C. Croll S. (2005) Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol. 192, 348 356.
67. Siebenlist U., Franzoso G. Brown K. (1994) Structure, regulation and function of NF-kappa B. Annu. Rev. Cell Biol. 10, 405 455.
68. Sloviter R. S. (1999) Status epilepticus-induced neuronal injury and network reorganization. Epilepsia 40 (Suppl. 1 S34 S39.
69. Swartz B. E., Houser C. R., Tomiyasu U., Walsh G. O., DeSalles A., Rich J. R. Delgado-Escueta A. (2006) Hippocampal cell loss in posttraumatic human epilepsy. Epilepsia 47, 1373 1382.
70. Timmusk T., Palm K., Metsis M., Reintam T., Paalme V., Saarma M. Persson H. (1993) Multiple promoters direct tissue-specific expression of the rat BDNF gene. Neuron 10, 475 489.
71. Tongiorgi E., Armellin M., Giulianini P. G., Bregola G., Zucchini S., Paradiso B., Steward O., Cattaneo A. Simonato M. (2004) Brain-derived neurotrophic factor mRNA and protein are targeted to discrete dendritic laminas by events that trigger epileptogenesis. J. Neurosci. 24, 6842 6852.
72. Tsankova N. M., Kumar A. Nestler E. J. (2004) Histone modifications at gene promoter regions in rat hippocampus after acute and chronic electroconvulsive seizures. J. Neurosci. 24, 5603 5610.
73. Vezzani A., Ravizza T., Moneta D., Conti M., Borroni A., Rizzi M., Samanin R. Maj R. (1999) Brain-derived neurotrophic factor immunoreactivity in the limbic system of rats after acute seizures and during spontaneous convulsions: temporal evolution of changes as compared to neuropeptide Y. Neuroscience 90, 1445 1461.
74. Weinberger D. R. (1999) Cell biology of the hippocampal formation in schizophrenia. Biol. Psychiatry 45, 395 402.
75. Yeh S. H., Lin C. H., Lee C. F. Gean P. W. (2002) A requirement of nuclear factor-kappa B activation in fear-potentiated startle. J. Biol. Chem. 277, 46720 46729.
76. Yu Z., Zhou D., Bruce-Keller A. J., Kindy M. S. Mattson M. P. (1999) Lack of the p50 subunit of nuclear factor-kappa B increases the vulnerability of hippocampal neurons to excitotoxic injury. J. Neurosci. 19, 8856 8865.
77. Yu Z., Zhou D., Cheng G. Mattson M. P. (2000) Neuroprotective role for the p50 subunit of NF-kappa B in an experimental model of Huntington's disease. J. Mol. Neurosci. 15, 31 44.
78. Zandi E., Chen Y. Karin M. (1998) Direct phosphorylation of I kappa B by IKK alpha and IKK beta: discrimination between free and NF-kappa B-bound substrate. Science 281, 1360 1363.