Lack of NF-κB p50 exacerbates degeneration of hippocampal neurons after chemical exposure and impairs learning

Experimental Neurology

Volumn 176, Issue 2, 2002, Pages 277-288

  Kassed, C A ^a   Willing, A E ^a   Garbuzova Davis, S ^a   Sanberg, P R ^a   Pennypacker, K R ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Hippocampus; Knockout mice; Learning and memory; Neurodegeneration; Neuroplasticity; Neuroprotection; NF B; Signal transduction; Transcription factors; Trimethyltin

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P50; PROTEIN SUBUNIT; TRIMETHYLTIN; FLUORESCENT DYE; FLUORO JADE; ORGANIC COMPOUND;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CELL COUNT; CONTROLLED STUDY; DENTATE GYRUS; GRANULE CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LEARNING DISORDER; LIMBIC CORTEX; MEMORY; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SURVIVAL; TASK PERFORMANCE; WILD TYPE; ANIMAL; ANIMAL BEHAVIOR; BIOSYNTHESIS; CELL DEATH; CHEMICALLY INDUCED DISORDER; DEGENERATIVE DISEASE; DISEASE MODEL; DRUG EFFECT; GENETICS; LONG TERM MEMORY; METABOLISM; MOUSE MUTANT; NERVE CELL; NERVE CELL PLASTICITY; PATHOLOGY; SURVIVAL RATE;

ANIMALS; BEHAVIOR, ANIMAL; CELL DEATH; DISEASE MODELS, ANIMAL; FLUORESCENT DYES; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LEARNING DISORDERS; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; NEURODEGENERATIVE DISEASES; NEURONAL PLASTICITY; NEURONS; NF-KAPPA B; NF-KAPPA B P50 SUBUNIT; ORGANIC CHEMICALS; RETENTION (PSYCHOLOGY); SURVIVAL RATE; TRIMETHYLTIN COMPOUNDS;

EID: 0036025433     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.2002.7967     Document Type: Article

References (81)

1. Albensi, B., and M. Mattson. 2000. Evidence for involvement of TNF and NF-kappaB in hippocampal and synaptic plasticity. Synapse 35: 151-159.
2. Albensi, B., P. Sullivan, M. Thompson, S. Scheff, and M. Mattson. 2000. Cyclosporin ameliorates traumatic brain-injury-induced alterations of hippocampal synaptic plasticity. Exp. Neurol. 162: 385-389.
3. Arenzana-Seisdedos, F., J. Thompson, M. Rodriguez, F. Bachelerie, D. Thomas, and R. Hay. 1995. Inducible nuclear expression of newly synthesized IκBα negatively regulates DNA-binding and transcriptional activities of NF-kappa B. Mol. Cell. Biol. 15: 2689-2696.
4. Arenzana-Seisdedos, F., P. Turpin, M. Rodriguez, D. Thomas, R. Hay, J.-L. Virelizier, and C. Dargemont. 1997. Nuclear localization of IκBα promotes active transport of NF-κB from the nucleus to the cytoplasm. J. Cell Sci. 110: 369-378.
5. Baeuerle, P., and D. Baltimore. 1989. A specific inhibitor of the NFκB. Science 242: 540-546.
6. Baeuerle, P., and T. Henkel. 1994. Function and activation of NF-κB in the immune system. Annu. Rev. Immunol. 12: 141-179.
7. Balaban, C., J. O'Callaghan, and M. Billingsley. 1988. Trimethyltin-induced neuronal damage in the rat brain: Comparative studies using silver degeneration stains, immunocytochemistry and immunoassay for neuronotypic and gliotypic proteins. Neuroscience 26: 337-361.
8. Baldwin, A.. 1996. The NF-kappaB and I kappa B proteins: New discoveries and insights. Annu. Rev. Immunol. 14: 649-683.
9. Blackwood, E., B. Lüscher, and B. Eisenmann. 1992. Myc and Max associate in vivo. Genes Dev. 6: 71-80.
10. Butler, T. L., C. A. Kassed, and K. R. Pennypacker. 2002. Neurodegeneration in the rat hippocampus and striatum after middle cerebral artery occlusion. Brain Res 929: 252-260.
11. Chang, L., and R. Dyer. 1983. A time-course study of trimethyltin induced neuropathology in rats. Neurobehav. Toxicol. Teratol. 5: 443-459.
12. Chang, L., T. Tiemeyer, G. Wenger, and D. McMillian. 1982. Neuropathology of mouse hippocampus in acute trimethyltin intoxication. Neurobehav. Toxicol. Teratol. 4: 149-156.
13. Clemens, J., D. Stephenson, E. Smalstig, E. Dixon, and S. Little. 1997. Global ischemia activates nuclear factor-kappaB in forebrain neurons of rats. Stroke 28: 1013-1081.
14. Clemens, J., D. Stephenson, T. Yin, E. Smalstig, J. Panetta, and S. Little. 1998. Drug-induced neuroprotection from global ischemia is associated with prevention of persistent but not transient activation of NF-κB in rats. Stroke 29: 677-682.
15. Cohen, N. J., and H. Eichenbaum. 1994. Memory, Amnesia, and the Hippocampal System, 2nd ed. MIT Press, Cambridge, MA.
16. Cruise, L., L. Ho, K. Veitch, G. Fuller, and B. Morris. 2000. Kainate receptors activate NF-kappaB via MAP kinase in striatal neurones. NeuroReport 11: 395-398.
17. Desimone, R. 1992. The physiology of memory: Recordings of things past. Science 258: 245-246.
18. DiDonato, J., M. Hayakawa, D. Rothwarf, E. Zandi, and M. Karin. 1997. A cytokine-responsive IκB kinase that activates transcription factor NF-κB. Nature 388: 548-554.
19. Duan, W., V. Rangnekar, and M. Mattson. 1999. Prostate apoptosis response-4 production in synaptic compartments following apoptotic and excitotoxic insults: Evidence for a pivotal role in mitochondrial dysfunction and neuronal degeneration. J. Neurochem. 72: 2312-2322.
20. Duménil, J. 1999. International programme on chemical safety, group poisons, Vol. 2001.http://inchem.org/documents/pims/chemmical/pimg019.htm.
21. Eisch, A., L. Schmued, and J. Marshall. 1998. Characterizing cortical neuron injury with Fluoro-Jade labeling after a neurotoxic regimen of methamphetamine. Synapse 30: 329-333.
22. Fiedorowicz, A., I. Figiel, B. Kaminska, M. Zaremba, S. Wilk, and B. Oderfeld-Nowak. 2001. Dentate granule neuron apoptosis and glia activation in murine hippocampus induced by trimethyltin exposure. Brain Res. 912: 116-127.
23. Finco, T., A. Beg, and A. Baldwin. 1994. Inducible phosphorylation of IκBα is not sufficient for its dissociation from NF-κB and is inhibited by protease inhibitors. Proc. Natl. Acad. Sci. USA 91: 11884-11888.
24. Freudenthal, R., and A. Romano. 2000. Participation of Rel/NF-kappaB transcription factors in long-term memory in the crab Chasmagnathus. Brain Res. 855: 274-281.
25. Frey, S., J. Bergado-Rosado, T. Seidenbecher, H. C. Pape, and J. U. Frey. 2001. Reinforcement of early long-term potentiation (early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: Heterosynaptic induction mechanisms of late-LTP. J. Neurosci. 21: 3697-3703.
26. Ghosh, S., M. May, and E. Kopp. 1998. NF-κB and Rel proteins: Evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16: 225-260.
27. Grilli, M., M. Pizzi, M. Memo, and P. Spano. 1996. Neuroprotection by aspirin and sodium salicylate through blockade of NF-κB activation. Science 274: 1383-1385.
28. Grimm, S., and P. A. Baeuerle. 1993. The inducible transcription factor NF-kappa B: Structure-function relationship of its protein subunits. Biochem. J. 290: 297-308.
29. Henkel, T., T. Machleidt, I. Alkalay, M. Kronke, Y. Ben-Neriah, and P. A. Baeuerle. 1993. Rapid proteolysis of I kappa B-alpha is necessary for activation of transcription factor NF-kappa B. Nature 365: 182-185.
30. Henkel, T., U. Zabel, K. van Zee, J. Muller, E. Fanning, and P. Baeuerle. 1992. Intramolecular masking of the nuclear location signal and dimerization domain in the precursor for the p50 NF-κB subunit. Cell 68: 1121-1133.
31. Herdegen, T., P. Skene, and M. Bahr. 1997. The c-Jun transcription factor-bipotential mediator of neuronal death, survival and regeneration. Trends Neurosci. 20: 227-231.
32. Huxford, T., D.-B. Huang, S. Malek, and G. Ghosh. 1998. The crystal structure of the IκBα/NF-κB complex reveals mechanisms of NF-κB inactivation. Cell 95: 759-770.
33. Isaacson, R. L. 1982. The Limbic System, Plenum Press, New York.
34. Israël, A. 2000. The IKK complex: An integrator of all signals that activate NF-κB? Trends Cell. Biol. 10: 129-133.
35. Jacobs, M., and S. Harrison. 1998. Structure of an IκBα/NF-κB complex. Cell 95: 749-758.
36. Kaltschmidt, C., B. Kaltschmidt, and P. A. Baeuerle. 1993. Brain synapses contain inducible forms of the transcription factor NF-kappa B. Mech. Dev. 43: 135-147.
37. Kaltschmidt, C., B. Kaltschmidt, and P. A. Baeuerle. 1995. Stimulation of inotropic glutamate receptors activates transcription factor NF-kappa B in primary neurons. Proc. Natl. Acad. Sci. USA 92: 9618-9622.
38. Kaltschmidt, C., B. Kaltschmidt, H. Neumann, H. Wekerle, and P. A. Baeuerle. 1994. Constitutive NF-kappa B activity in neurons. Mol. Cell. Biol. 14: 3981-3992.
39. Krady, J., G. Oyler, C. Balaban, and M. Billingsley. 1990. Use of avidin-biotin subtractive hybridization to characterize mRNA common to neurons destroyed by the selective neurotoxicant trimethyltin. Mol. Brain Res. 7: 287-297.
40. Lahiri, D., and C. Nall. 1995. Promoter activity of the gene encoding the beta-amyloid precursor protein is up-regulated by growth factors, phorbol ester, retinoic acid and interleukin-1. Brain Res. Mol. Brain Res. 32: 233-240.
41. Lalonde, R. 2002. The neurobiological basis of spontaneous alternation. Neurosci. Biobehav. Rev. 26: 91-104.
42. Li, M., D. Carpio, Y. Zheng, P. Bruzzo, V. Singh, F. Ouaaz, R. Medzhitov, and A. Beg. 2001. An essential role of the NF-κB/Toll-like receptor pathway in induction of inflammatory and tissue-repair gene expression by necrotic cells. J. Immunol. 166: 7128-7135.
43. Little, A., and J. O'Callaghan. 1999. TNF-alpha, IL-1alpha, and IL-1beta gene expression is not altered in response to trimethyltin-induced neuronal damage in the adult rat hippocampus. Soc. Neurosci. Abs. 25: 1535.
44. Mattson, M., and S. Camandola. 2001. NF-κB in neuronal plasticity and neurodegenerative disorders. J. Clin. Invest. 107: 247-254.
45. Mattson, M. P., W. Duan, W. A. Pedersen, and C. Culmsee. 2001. Neurodegenerative disorders and ischemic brain diseases. Apoptosis 6: 69-81.
46. Meberg, P., W. Kinney, E. Valcourt, and A. Routtenberg. 1996. Gene expression of the transcription factor NF-κB in hippocampus: Regulation by synaptic activity. Mol. Brain Res. 38: 179-190.
47. Mercurio, F., H. Zhu, B. Murray, A. Shevchenko, B. Benett, J. Li, D. Young, M. Barbosa, M. Mann, A. Manning, and A. Rao. 1997. IKK-1 and IKK-2: Cytokine-activated IκB kinases essential for NF-κB activation. Science 278: 860-866.
48. Nakao, K., Y. Ikegaya, M. K. Yamada, N. Nishiyama, and N. Matsuki. 2001. Spatial performance correlates with long-term potentiation of the dentate gyrus but not of the CA1 region in rats with fimbria-fornix lesions. Neurosci. Lett. 307: 159-162.
49. O'Callaghan, J. 1988. Neurotypic and gliotypic markers of neurotoxicity. Neurotoxicol. Teratol. 10: 445-452.
50. O'Callaghan, J., and D. Miller. 1984. Neuron-specific proteins and biochemical indicators of neurotoxicity: Effects of acute administration of trimethyltin to the adult rat. J. Pharmacol. Exp. Ther. 231: 736-743.
51. O'Connell, C., H. C. Gallagher, A. O'Malley, M. Bourke, and C. M. Regan. 2000. CREB phosphorylation coincides with transient synapse formation in the rat hippocampal dentate gyrus following avoidance learning. Neural Plast. 7: 279-289.
52. O'Neill, L., and C. Kaltschmidt. 1997. NF-κB: A crucial transcription factor for glial and neuronal cell function. Trends Neurosci. 20: 252-258.
53. Okazaki, M., D. Evenson, and J. Nadler. 1995. Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: Visualization after retrograde transport of biocytin. J. Comp. Neurol. 352: 515-534.
54. Penkowa, M., M. Giralt, P. Thomsen, J. Carrasco, and J. Hidalgo. 2001. Zinc or copper deficiency-induced impaired inflammatory response to brain trauma may be caused by the concomitant metallothionein changes. J. Neurotrauma 18: 447-463.
55. Pennypacker, K. R., S. Eidizadeh, C. A. Kassed, J. P. O'Callaghan, P. R. Sanberg, and A. E. Willing. 2000. Expression of fos-related antigen-2 in rat hippocampus after middle cerebral arterial occlusion. Neurosci. Lett. 289: 1-4.
56. Pennypacker, K. R., C. A. Kassed, S. Eidizadeh, and J. P. O'Callaghan. 2000. Brain injury: Prolonged induction of transcription factors. Acta Neurobiol. Exp. 60: 515-528.
57. Pennypacker, K. R., C. A. Kassed, S. Eidizadeh, S. Saporta, P. Sanberg, and A. Willing. 2001. NF-κB p50 is increased in neurons surviving hippocampal injury. Exp. Neurol. 172: 307-319.
58. Philbert, M. A., M. L. Billingsley, and K. R. Reuhl. 2000. Mechanisms of injury in the central nervous system. Toxicol. Pathol. 28: 43-53.
59. Qin, Z., Y. Wang, M. Nakai, and T. Chase. 1998. Nuclear factor-kappa B contributes to excitotoxin-induced apoptosis in rat striatum. Mol. Pharmacol. 53: 33-42.
60. Raghavendra, V., K. Chopra, and S. Kulkarni. 1998. Involvement of cholinergic system in losartan-induced facilitation of spatial and short-term working memory. Neuropeptides 32: 417-421.
61. Raghavendra, V., K. Chopra, and S. Kulkarni. 2001. Comparative studies on the memory-enhancing actions of captopril and losartan in mice using inhibitory shock avoidance paradigm. Neuropeptides 35: 65-69.
62. Regnier, C., H. Song, X. Gao, D. Goeddel, Z. Cao, and M. Rothe. 1997. Identification and characterization of an IκB kinase. Cell 90: 373-383.
63. Rivas-Arancibia, S., A. Willing, T. Zigova, A. Rodriguez, D. Cahill, and P. Sanberg. 2000. The effects of taurine on hNT neurons transplanted in adult rat striatum. Cell Transplant. 9: 751-758.
64. Rostasy, K., L. Monti, C. Yiannoutsos, J. Wu, J. Bell, J. Hedreen, and B. Navia. 2000. NF-kappaB activation, TNF-alpha expression, and apoptosis in the AIDS-Dementia-Complex. J. Neurovirol. 6: 537-543.
65. Rothwarf, D., E. Zandi, G. Natoli, and M. Karin. 1998. IKKγ is an essential regulatory subunit of the IkappaB kinase complex. Nature 395: 297-300.
66. Sachdev, S., and M. Hannink. 1998. Loss of IκBα-mediated control over nuclear import and DNA binding enables oncogenic activation of c-Rel. Mol. Cell. Biol. 18: 5445-5456.
67. Sachdev, S., A. Hoffman, and M. Hannik. 1998. Nuclear localization of IκBα is mediated by the second ankyrin repeat; the IκBα ankyrin repeats define a novel class of cis-acting nuclear import sequences. Mol. Cell. Biol. 18: 2524-2534.
68. Schmidt-Ullrich, R., S. Memet, A. Lillienbaum, J. Feullard, M. Raphael, and A. Israël. 1996. NF-κB activity in transgenic mice: Developmental regulation and tissue specificity. Development 122: 2117-2128.
69. Schmued, L., C. Albertson, and W. Slikker. 1997. Fluoro-Jade: A novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res. 751: 37-46.
70. Schneider, A., A. Martin-Villaba, F. Weih, J. Vogel, T. Wirth, and M. Schwaninger. 1999. NF-kappaB is activated and promotes cell death in focal cerebral ischemia. Nat. Med. 5: 554-559.
71. Schütze, S., K. Potthoff, T. Machleidt, D. Benkovic, K. Wiegmann, and M. Krönke. 1992. TNF activates NF-κB by phosphatidylcholine-specific phospholipase C-induced "acidic" sphingomyelin breakdown. Cell 71: 765-766.
72. Sha, W., H.-C. Liou, E. Tuomanen, and D. Baltimore. 1995. Targeted disruption of the p50 subunit of NFκ-B leads to multifocal defects in immune responses. Cell 80: 321-330.
73. Smith-Swintosky, V., L. Pettigrew, S. Craddock, A. Culwell, R. Rydel, and M. Mattson. 1994. Secreted forms of beta-amyloid precursor protein protect against ischemic brain injury. J. Neurochem. 63: 781-784.
74. Tam, W., L. Lee, L. Davis, and R. Sen. 2000. Cytoplasmic sequestration of Rel proteins by IκBα requires CRM1-dependent nuclear export. Mol. Cell. Biol. 20: 2269-2284.
75. Thompson, R. F., and D. J. Krupa. 1994. Organization of memory traces in the mammalian brain. Annu. Rev. Neurosci. 17: 519-549.
76. Toggas, S., J. Krady, and M. Billingsley. 1992. Molecular neurotoxicity of trimethyltin: Identification of stannin, a novel protein expressed in trimethyltin-sensitive cells. Mol. Pharmacol. 42: 44-56.
77. Traenckner, E. B., and P. A. Baeuerle. 1995. Appearance of apparently ubiquitin-conjugated I kappa B-alpha during its phosphorylation-induced degradation in intact cells. J. Cell Sci. Suppl. 19: 79-84.
78. Yan, S., X. Chen, J. Fu, M. Chen, H. Zhu, A. Roher, T. Slattery, L. Zhao, M. Nagashima, J. Morser, A. Migheli, P. Nawroth, D. Stern, and A. Schmidt. 1996. RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 382: 685-691.
79. Yu, Z., D. Zhou, A. Bruce-Keller, M. Kindy, and M. Mattson. 1999. Lack of p50 subunit of nuclear factor-κB increases the vulnerability of hippocampal neurons to excitotoxic injury. J. Neurosci. 19: 8856-8865.
80. Zabel, U., T. Henkel, M. S. Silva, and P. A. Baeuerle. 1993. Nuclear uptake control of NF-kappa B by MAD-3, an I kappa B protein present in the nucleus. EMBO J. 12: 201-211.
81. Zandi, E., D. Rothwarf, M. Delhases, M. Hayakawa, and M. Karin. 1997. The I kappaB kinase complex (IKK) contains two kinase subunits, IKKα and IKKβ, necessary for IκB phosphorylation and NF-κB activation. Cell 91: 243-252.