NF-κB proteins in adult neurogenesis: Relevance for learning and memory in physiology and pathology

Transcription Factors CREB and NF-kB: Involvement in Synaptic Plasticity and Memory Formation

Volumn , Issue , 2012, Pages 79-96

  Grilli, Mariagrazia ^a   Meneghini, Vasco ^a  

^a UNIVERSITY OF EASTERN PIEDMONT   (Italy)

Author keywords

Hippocampus; Learning; Memory; Neural progenitor cells; Neural stem cells; Neurodegeneration; Neurogenesis; Neuroplasticity; Neuropsychiatric disorders; NF B; Subgranular zone

Indexed keywords

EID: 84882708354     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.2174/978160805257811201010079     Document Type: Chapter

References (155)

1. Sen R, Baltimore D. Inducibility of kappa immunoglobulin enhancer-binding protein NF-kappa B by a post translational mechanism. Cell 1986; 47: 921-8.
2. Krakauer T. Nuclear factor-kappaB: fine-tuning a central integrator of diverse biologic stimuli. Int Rev Immunol 2008; 27: 286-92.
3. Gerondakis S, Grumont R, Gugasyna R, et al. Unravelling the complexities of the NF-kappaB signaling pathway using mouse knockout and transgenic models. Oncogene 2006; 25: 6781-99.
4. Grilli M, Chiu JJ-S, Lenardo MJ. NF-κB and Rel: participants in a multiform transcriptional regulatory system. Int Rev Cytol 1993; 143: 01-62.
5. Pizzi M, Spano PF. Distinct roles of diverse nuclear factor-kappaB complexes in neuropathological mechanisms. Eur J Pharmacol 2006; 545: 22-8.
6. Leung TH, Hoffmann A, Baltimore D. One nucleotide in a kappaB site can determine cofactor specificity for NF-kappaB dimmers. Cell 2004; 118: 453-64.
7. Bates PW, Miyamoto S. Expanded nuclear roles for IκBs. Sci STKE 2004; 254: 01-2.
8. Van Loo G, De Lorenzi R, Schmidt H, et al. Inhibition of transcription factor NF-kappaB in the central nervous system ameliorates autoimmune encephalomyelitis in mice. Nat Immunol 2006; 7: 954-61.
9. Huang TT, Wuerzberger-Davis SM, Wu ZH, Miyamoto S. Sequential modification of NEMO/IKKgamma by SUMO-1 and ubiquitin mediates NF-kappaB activation by genotoxic stress. Cell 2003; 115: 565-76.
10. Saccani S, Marazzi I, Beg AA, Natoli G. Degradation of promoter-bound p65/RelA is essential for the prompt termination of the nuclear factor kappa B response. J Exp Med 2004; 200: 107-13.
11. Chen LF, Williams SA, Mu Y, et al. NF-kappaB RelA phosphorylation regulates RelA acetylation. Mol Cell Biol 2005; 25: 7966-75.
12. Franzoso G, Bours V, Park S, Tomita-Yamaguchi M, Kelly K, Siebenlist U. The candidate oncoprotein Bcl3 is an antagonist of p50/NFkappaB-mediated inhibition. Nature 1992; 359: 339-42.
13. Bours V, Franzoso G, Azarenko V, et al. The oncoprotein BCL-3 directly transactivates through kappa B motifs via association with DNA-binding p50 homodimers. Cell 1993; 72: 729-39.
14. Kaltschmidt C, Kaltschmidt B, Neumann H, Wekerle H, Baeuerle PA. Constitutive NF-kappaB activity in neurons. Mol Cell Biol 1994; 14: 3981-92.
15. Guerrini L, Blasi F, Denis-Donini S. Synaptic activation of NF-kappaB by glutamate in cerebellar granule neurons in vitro. Proc Natl Acad Sci USA 1995; 92: 9077-81.
16. Meberg PJ, Kinney WR, Valcourt EG, Routtenberg A. Gene expression of the transcription factor NF-kappaB in hippocampus: regulation by synaptic activity. Brain Res Mol Brain Res 1996; 38: 179-90.
17. Wellmann H, Kaltschmidt B, Kaltschmidt C. Retrograde transport of transcription factor NF-kappaB in living neurons. J Biol Chem 2001; 276: 11821-9.
18. Meffert MK, Chang JM, Wiltgen BJ, Fanselow MS, Baltimore D. NF-kappaB functions in synaptic signaling and behavior. Nat Neurosci 2003; 6: 1072-8.
19. Schölzke MN, Potrovita I, Subramaniam S, Prinz S, Schwaninger M. Glutamate activates NF-kappaB through calpain in neurons. Eur J Neurosci 2003; 8: 3305-10.
20. Suzuki T, Mitake S, Okumura-Noji K, Yang JP, Fujii T, Okamoto T. Presence of NF-kappaB-like and IkappaB-like immunoreactivities in postsynaptic densities. Neuroreport 1997; 8: 2931-5.
21. Albensi BC, Mattson MP. Evidence for the involvement of TNF and NF-kappaB in hippocampal synaptic plasticity. Synapse 2000; 35: 151-9.
22. Mattson MP, Culmsee C, Yu Z, Camandola S. Roles of nuclear factor kappa B in neuronal survival and plasticity. J Neurochem 2000; 74: 443-56.
23. Burr PB, Morris BJ. Involvement of NMDA receptors and a p21Ras-like guanosine triphosphatase in the constitutive activation of nuclear factor-kappaB in cortical neurons. Exp Brain Res 2002; 147: 273-9.
24. Lilienbaum A, Israël A. From calcium to NF-kappaB signaling pathways in neurons. Mol Cell Biol 2003; 23: 2680-98.
25. Freudenthal R, Romano A, Routtenberg A. Transcription factor NF-kappaB activation after in vivo perforant path LTP in mouse hippocampus. Hippocampus 2004; 14: 677-83.
26. Yeh SH, Lin CH, Lee CF, Gean PW. A requirement of nuclear factor-kappaB activation in fear-potentiated startle. J Biol Chem 2002; 277: 46720-9.
27. Meffert MK, Baltimore D. Physiological functions for brain NF-κB. TINS 2004; 28: 37-43.
28. Mattson MP. NF-kappaB in the survival and plasticity of neurons. Neurochem Res 2005; 30: 883-93.
29. Memet S. NF-κB functions in the nervous system: from development to disease. Biochem Pharmacol 2006; 72: 1180-95.
30. Romano A, Freudenthal R, Merlo E, Routtenberg A. Evolutionary conserved role of the NF-κB transcription factor in neural plasticity and memory. Eur J Neurosci 2006; 24: 1507-16.
31. Beg AA, Sha WC, Bronson RT, Ghosh S, Baltimore D. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappaB. Nature 1995; 376: 167-70.
32. Alcamo E, Mizgerd JP, Horwitz BH, et al. Targeted mutation of TNF receptor I rescues the RelA-deficient mouse and reveals a critical role for NF-kappaB in leukocyte recruitment. J Immunol 2001; 167: 1592-00.
33. Levenson JM, Choi S, Lee SY, et al. A bioinformatics analysis of memory consolidation reveals involvement of the transcription factor c-rel. J Neurosci 2004; 24: 3933-43.
34. Ahn HJ, Hernandez CM, Levenson JM, Lubinm FD, Liou HC, Sweatt JD. c-Rel, an NF-kappaB family transcription factor, is required for hippocampal long-term synaptic plasticity and memory formation. Learn Mem 2008; 15: 539-49.
35. Kaltschmidt B, Ndiaye D, Korte M, et al. NF-kappaB regulates spatial memory formation and synaptic plasticity through protein kinase A/CREB signaling. Mol Cell Biol 2006; 26: 2936-46.
36. Grilli M, Memo M. Nuclear factor-kappaB/Rel proteins: a point of convergence of signalling pathways relevant in neuronal function and dysfunction. Biochem Pharmacol 1999; 57: 01-7.
37. Bracchi-Ricard V, Brambilla R, Levenson J, et al. Astroglial nuclear factor-kappaB regulates learning and memory and synaptic plasticity in female mice. J Neurochem 2008; 104: 611-23.
38. Sha WC, Liou HC, Tuomanen EI, Baltimore D. Targeted disruption of the p50 subunit of NF-kappa B leads to multifocal defects in immune responses. Cell 1995; 80: 321-30.
39. Kassed CA, Willing AE, Garbuzova-Davis S, Sanberg PR, Pennypacker KR. Lack of NF-kappaB p50 exacerbates degeneration of hippocampal neurons after chemical exposure and impairs learning. Exp Neurol 2002; 176: 277-88.
40. Kassed CA, Herkenham M. NF-kappaB p50-deficient mice show reduced anxiety-like behaviors in tests of exploratory drive and anxiety. Behav Brain Res 2004; 154: 577-84.
41. Ashburner BP, Westerheide SD, Baldwin AS Jr. The p65 (RelA) subunit of NF-kappaB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol Cell Biol 2001; 21: 7065-77.
42. Viatour P, Legrand-Poels S, van Lint C, et al. Cytoplasmic IkappaBalpha increases NF-kappaB-independent transcription through binding to histone deacetylase (HDAC) 1 and HDAC3. J Biol Chem 2003; 278: 46541-8.
43. Anest V, Cogswell PC, Baldwin AS Jr. IkappaB kinase alpha and p65/RelA contribute to optimal epidermal growth factor-induced c-fos gene expression independent of IkappaBalpha degradation. J Biol Chem 2004; 279: 31183-9.
44. Colvis CM, Pollock JD, Goodman RH, et al. Epigenetic mechanisms and gene networks in the nervous system. J Neurosci 2005; 25: 10379-89.
45. Levenson JM, Sweatt JD. Epigenetic mechanisms in memory formation. Nat Rev Neurosci 2005; 6: 108-18.
46. Lubin FD, Sweatt JD. The IkappaB kinase regulates chromatin structure during reconsolidation of conditioned fear memories. Neuron 2007; 55: 942-57.
47. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001; 21: 7153-60.
48. Kempermann G, Jessberger S, Steiner B, Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004; 27: 447-52.
49. Seri B, Garcia-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 2004; 478: 359-78.
50. Ming GL, Song H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 2005; 28: 223-50.
51. Biebl M, Cooper CM, Winkler J, Kuhn HG. Analysis of neurogenesis and programmed cell death reveals a self renewing capacity in the adult rat brain. Neurosci Lett 2000; 291: 17-20.
52. Lehmann K, Butz M, Teuchert-Noodt G. Offer and demand: proliferation and survival of neurons in the dentate gyrus. Eur J Neurosci 2005; 21: 3205-16.
53. Gould E, Tanapat P, Hastings NB, Shors TJ. Neurogenesis in adulthood: a possible role in learning. Trends Cogn Sci 1999; 3: 186-92.
54. van Praag H, Christie BR, Sejnowski TJ, Gage FH. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 1999; 96: 13427-31.
55. Shors TJ, Miesagaes G, Beylin A, Zhao M, Rydel T, Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 2001; 410: 372-76.
56. Kempermann G, Gage FH. Genetic determinants of adult hippocampal neurogenesis correlate with acquisition, but not probe trial performance, in the water maze task. Eur J Neurosci 2002; 16: 129-36.
57. Aimone JB, Wiles J, Gage FH. Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci 2006; 9: 723-27.
58. Leuner B, Gould E, Shors TJ. Is there a link between adult neurogenesis and learning? Hippocampus 2006; 16: 216-24.
59. Kee N, Teixairan CM, Wang AH, Frankland PW. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 2007; 10: 355-62.
60. Saxe MD, Malleret G, Vronskaya S, et al. Paradoxical influence of hippocampal neurogenesis on working memory. Proc Natl Acad Sci USA 2007; 10: 4642-6.
61. Denis-Donini S, Dellarole A, Crociara P, et al. Impaired adult neurogenesis associated with short-term memory defects in NF-kappaB p50-deficient mice. J Neurosci 2008; 28: 3911-9.
62. Tashiro A, Makino H, Gage FH. Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J Neurosci 2007; 27: 3252-9.
63. Dupret D, Fabre A, Dobrossy MD, et al. Spatial learning depends on both the addition and removal of new hippocampal neurons. PLOS Biol 2007; 5: 1683-94.
64. Snyder JS, Radik R, Wojtowicz JM, Cameron HA. Anatomical gradients of adult neurogenesis and activity: young neurons in the ventral dentate gyrus are activated by water maze training. Hippocampus 2009; 19: 360-70.
65. Brown J, Cooper-Kuhn CM, Kempermann G, et al. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 2003; 17: 2042-6.
66. Bruel-Jungerman E, Laroche S, Rampon C. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci 2005; 21: 513-21.
67. Ueda S, Sakakibara S, Yoshimoto K. Effect of long-lasting serotonin depletion on environmental enrichment-induced neurogenesis in adult rat hippocampus and spatial learning. Neuroscience 2005; 135: 395-02.
68. Leal-Galicia P, Castañeda-Bueno M, Quiroz-Baez R, Arias C. Long-term exposure to environmental enrichment since youth prevents recognition memory decline and increases synaptic plasticity markers in aging. Neurobiol Learn Mem 2008; 90: 511-8.
69. Gould E, McEwen BS, Tanapat P, Galea LA, Fuchs E. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 1997; 17: 2492-8.
70. Lemaire V, Koehl M, Le Moal M, Abrous DN. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 2000; 97: 11032-7.
71. Coe CL, Kramer M, Czéh B, et al. Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry 2003; 54: 1025-34.
72. Simon M, Czéh B, Fuchs E. Age-dependent susceptibility of adult hippocampal cell proliferation to chronic psychosocial stress. Brain Res 2005; 1049: 244-8.
73. Thomas RM, Hotsenpiller G, Peterson DA. Acute psychosocial stress reduces cell survival in adult hippocampal neurogenesis without altering proliferation. J Neurosci 2007; 27: 2734-43.
74. Klempin F, Kempermann G. Adult hippocampal neurogenesis and aging. Eur Arch Psychiatry Clin Neurosci 2007; 257: 271-80.
75. Jin K, Peel AL, Mao XO, et al. Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci USA 2004; 6: 343-7.
76. Boekhoorn K, Joels M, Lucassen PJ. Increased proliferation reflects glial and vascular-associated changes, but not neurogenesis in the presenile Alzheimer hippocampus. Neurobiol Dis 2006; 24: 01-14.
77. Haughey NJ, Liu D, Nath A, Borchard AC, Mattson MP. Disruption of neurogenesis in the subventricular zone of adult mice, and in human cortical neuronal precursor cells in culture, by amyloid beta-peptide: implications for the pathogenesis of Alzheimer's disease. Neuromolecular Med 2002; 1: 125-35.
78. Haughey NJ, Nath A, Chan SL, Borchard AC, Rao MS, Mattson MP. Disruption of neurogenesis by amyloid beta-peptide, and perturbed neural progenitor cell homeostasis, in models of Alzheimer's disease. J Neurochem 2002; 83: 1509-24.
79. Kaneko N, Okano H, Sawamoto K. Role of the cholinergic system in regulating survival of newborn neurons in the adult mouse dentate gyrus and olfactory bulb. Genes Cells 2006; 1: 1145-59.
80. Jankowsky JL, Melnikova T, Fadale DJ, et al. Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer's disease. J Neurosci 2005; 25: 5217-24.
81. Kaltschmidt B, Uherek M, Volk B, Baeuerle PA, Kaltschmidt C. Transcription factor NF-kappaB 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 1997; 94: 2642-7.
82. Terai K, Matsuo A, McGeer PL. Enhancement of immunoreactivity for NF-kappa B in the hippocampal formation and cerebral cortex of Alzheimer's disease. Brain Res 1996; 735: 159-68.
83. Boissière F, Hunot S, Faucheux B, et al. Nuclear translocation of NF-kappaB in cholinergic neurons of patients with Alzheimer's disease. Neuroreport 1997; 8: 2849-52.
84. Kaltschmidt B, Uherek M, Wellmann H, Volk B, Kaltschmidt C. Inhibition of NF-kappaB potentiates amyloid beta-mediated neuronal apoptosis. Proc Natl Acad Sci USA 1999; 96: 9409-14.
85. Behl C, Davis JB, Lesley R, Schubert D. Hydrogen peroxide mediates amyloid beta protein toxicity. Cell 1994; 77: 817-27.
86. Du Yan S, Zhu H, Fu J, et al. Amyloid-beta peptide-receptor for advanced glycation endproduct interaction elicits neuronal expression of macrophage-colony stimulating factor: a proinflammatory pathway in Alzheimer disease. Proc Natl Acad Sci USA 1997; 94: 5296-01.
87. Valerio A, Boroni F, Benarese M, et al. NF-kappaB pathway: a target for preventing beta-amyloid (Abeta)-induced neuronal damage and Abeta42 production. Eur J Neurosci 2006; 23: 1711-20.
88. Barger SW, Horster D, Furukawa K, Goodman Y, Krieglstein J, Mattson MP. Tumor necrosis factors alpha and beta protect neurons against amyloid beta-peptide toxicity: evidence for involvement of a kB-binding factor and attenuation of peroxide and Ca2+ accumulation. Proc Natl Acad Sci USA 1995; 92: 9328-32.
89. Pizzi M, Sarnico I, Boroni F, et al. NF-kappaB factor c-Rel mediates neuroprotection elicited by mGlu5 receptor agonists against amyloid beta-peptide toxicity. Cell Death Differ 2005; 12: 761-72.
90. Guo Q, Robinson N, Mattson MP. Secreted beta-amyloid precursor protein counteracts the pro-apoptotic action of mutant presenilin-1 by activation of NF-kB and stabilization of calcium homeostasis. J Biol Chem 1998; 273: 12341-5.
91. Walker DG, Lue LF, Beach TG. Gene expression profiling of amyloid beta peptide-stimulated human post-mortem brain microglia. Neurobiol Aging 2001; 22: 957-66.
92. Chen J, Zhou Y, Mueller-Steiner S, et al. SIRT1 protects against microglia-dependent amyloid-beta toxicity through inhibiting NFkappaB signaling. J Biol Chem 2005; 280: 40364-74.
93. Curtis MA, Penney EB, Pearson AG, et al. Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc Natl Acad Sci USA 2003; 100: 9023-7.
94. Curtis MA, Penney EB, Pearson J, Dragunow M, Connor B, Faull RL. The distribution of progenitor cells in the subependymal layer of the lateral ventricle in the normal and Huntington's disease human brain. Neuroscience 2005; 132: 777-88.
95. Batista CM, Kippin TE, Willaime-Morawek S, Shimabukuro MK, Akamatsu W, van der Kooy D. A progressive and cell nonautonomous increase in striatal neural stem cells in the Huntington's disease R6/2 mouse. J Neurosci 2006; 26: 10452-60.
96. Jin K, LaFevre-Bernt M, Sun Y, et al. FGF-2 promotes neurogenesis and neuroprotection and prolongs survival in a transgenic mouse model of Huntington's disease. Proc Natl Acad Sci USA 2005; 102: 18189-94.
97. Lazic SE, Grote H, Armstrong RJ, et al. Decreased hippocampal cell proliferation in R6/1 Huntington's mice. Neuroreport 2004; 15: 811-3.
98. Gil JM, Mohapel P, Araújo IM, Popovic N, Li JY, Brundin P, Petersén A. Reduced hippocampal neurogenesis in R6/2 transgenic Huntington's disease mice. Neurobiol Dis 2005; 20: 744-51.
99. van Dellen A, Cordery PM, Spires TL, Blakemore C, Hannan AJ. Wheel running from a juvenile age delays onset of specific motor deficits but does not alter protein aggregate density in a mouse model of Huntington's disease. BMC Neurosci 2008; 01: 34.
100. Khoshnan A, Ko J, Watkin EE, Paige LA, Reinhart PH, Patterson PH. Activation of the IkappaB kinase complex and nuclear factorkappaB contributes to mutant huntingtin neurotoxicity. J Neurosci 2004; 24: 7999-08.
101. Qin ZH, Chen RW, Wang Y, Nakai M, Chuang DM, Chase TN. Nuclear factor kappaB nuclear translocation upregulates c-Myc and p53 expression during NMDA receptor-mediated apoptosis in rat striatum. J Neurosci 1999; 19: 4023-33.
102. Yu Z, Zhou D, Cheng G, Mattson MP. Neuroprotective role for the p50 subunit of NF-kappaB in an experimental model of Huntington's disease. J Mol Neurosci 2000; 15: 31-44.
103. Höglinger GU, Rizk P, Muriel MP, et al. Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci 2004; 7: 726-35.
104. Hunot S, Brugg B, Ricard D, et al. Nuclear translocation of NF-κB is increased in dopaminergic neurons of patients with parkinson disease. Proc Natl Acad Sci USA 1997; 94: 7531-6.
105. Blum D, Torch, S, Nissou MF, Verna JM. 6-Hydroxydopamine-induced nuclear factor-kappa B activation in PC12 cells. Biochem Pharmacol 2001; 62: 473-81.
106. Panet H, Barzilai A, Daily D, Melamed E, Offen D. Activation of nuclear transcription factor kappa B (NFkappaB) is essential for dopamine-induced apoptosis in PC12 cells. J Neurochem 2001; 77: 391-8.
107. Lee HJ, Kim SH, Kim KW, et al. Anti-apoptotic role of NF-kappaB in the auto-oxidized dopamine-induced apoptosis of PC12 cells. J Neurochem 2001; 76: 602-9.
108. Levites Y, Youdim MB, Maor G, Mandel S. Attenuation of 6-hydroxydopamine (6-OHDA)-induced nuclear factor-kappaB (NFkappaB) activation and cell death by tea extracts in neuronal cultures. Biochem Pharmacol 2002; 63: 21-29.
109. Park SH, Choi WS, Yoon SY, Ahn YS, Oh YJ. Activation of NF-kappaB is involved in 6-hydroxydopamine-but not MPP+-induced dopaminergic neuronal cell death: its potential role as a survival determinant. Biochem Biophys Res Commun 2004; 322: 727-33.
110. Teismann P, Schwaninger M, Weih F, Ferger B. Nuclear factor-kappaB activation is not involved in a MPTP model of Parkinson's disease. Neuroreport 2001; 12: 1049-53.
111. Jin K, Wang X, Xie L, et al. Evidence for stroke-induced neurogenesis in the human brain. Proc Natl Acad Sci USA 2006; 103: 13198-02.
112. Liu J, Solway K, Messing RO, Sharp FR. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci 1998; 18: 7768-78.
113. Nakatomi H, Kuriu T, Okabe S, et al. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 2002; 110: 429-41.
114. Arvidsson A, Kokaia Z, Lindvall O. N-methyl-D-aspartate receptor-mediated increase of neurogenesis in adult rat dentate gyrus following stroke. Eur J Neurosci 2001; 14: 10-8.
115. Yamashita T, Ninomiya M, Hernández Acosta P, et al. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J Neurosci 2006; 26: 6627-36.
116. Ridder DA, Schwaninger M. NF-kappaB signaling in cerebral ischemia. Neuroscience 2009; 158: 995-06.
117. Steiner B, Wolf S, Kempermann G. Adult neurogenesis and neurodegenerative disease. Regen Med 2006; 1: 15-28.
118. Galvan V, Bredesen DE. Neurogenesis in the adult brain: implications for Alzheimer's disease. CNS Neurol Disord Drug Targets 2007; 6: 303-10.
119. Kempermann G, Krebs J, Fabel K. The contribution of failing adult hippocampal neurogenesis to psychiatric disorders. Curr Opin Psychiatry 2008; 21: 290-5.
120. Abdipranoto A, Wu S, Stayte S, Vissel B. The role of neurogenesis in neurodegenerative diseases and its implications for therapeutic development. CNS Neurol Disord Drug Targets 2008; 7: 187-10.
121. Denis-Donini S, Caprini A, Frassoni C, Grilli M. Members of the NF-kappaB family expressed in zone of active neurogenesis in the postnatal and adult mouse brain. Brain Res Dev Brain Res 2005; 154: 81-9.
122. Young KM, Bartlett PF, Coulson EJ. Neural progenitor number is regulated by nuclear factor-kappaB p65 and p50 subunit-dependent proliferation rather than cell survival. J Neurosci Res 2006; 83: 39-49.
123. Zhu C, Liu Z, Gui L, Yao W, Qian W, Zhang C. Mutated IkappaBalpha represses proliferation of immortalized neural progenitor cells and prevents their apoptosis after oxygen-glucose deprivation. Brain Res 2008; 1244: 24-31.
124. Widera D, Mikenberg I, Elvers M, Kaltschmidt C, Kaltschmidt B. Tumor necrosis factor alpha triggers proliferation of adult neural stem cells via IKK/NF-kappaB signaling. BMC Neurosci 2006; 7: 64.
125. Geissler D, Konwalinka G, Peschel C, Braunsteiner H. The role of erythropoietin, megakaryocyte colony-stimulating factor, and T-cellderived factors on human megakaryocyte colony formation: evidence for T-cell-mediated and T-cell-independent stem cell proliferation. Exp Hematol 1987; 15: 845-53.
126. Shingo T, Sorokan ST, Shimazaki T, Weiss S. Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J Neurosci 2001; 21: 9733-43.
127. Wada T, Haigh JJ, Ema M, et al. Vascular endothelial growth factor directly inhibits primitive neural stem cell survival but promotes definitive neural stem cell survival. J Neurosci 2006; 26: 6803-12.
128. Brazel CY, Nuñez JL, Yang Z, Levison SW. Glutamate enhances survival and proliferation of neural progenitors derived from the subventricular zone. Neuroscience 2005; 131: 55-65.
129. Rolls A, Shechter R, London A, et al. Toll-like receptors modulate adult hippocampal neurogenesis. Nat Cell Biol 2007; 9: 1081-8.
130. Koo JW, Duman RS. IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc Natl Acad Sci USA 2008; 105: 751-6.
131. Widera D, Holtkamp W, Entschladen F, et al. MCP-1 induces migration of adult neural stem cells. Eur J Cell Biol 2004; 83: 381-7.
132. Sironi L, Banfi C, Brioschi M, et al. Activation of NF-κB and ERK1/2 after permanent focal ischemia is abolished by simvastatin treatment. Neurobiol Dis 2006; 22: 445-51.
133. Ninkovic J, Mori T, Götz M. Distinct modes of neuron addition in adult mouse neurogenesis. J Neurosci 2007; 27: 10906-11.
134. Mattson MP, Camandola S. NF-kappaB in neuronal plasticity and neurodegenerative disorders. J Clin Invest 2001; 107: 247-54.
135. Wang S, Scott BW, Wojtowicz JM. Heterogenous properties of dentate granule neurons in the adult rat. J Neurobiol 2000; 42: 248-57.
136. Schmidt-Hieber C, Jonas P, Bischofberger J. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 2004; 429: 184-7.
137. Song H, Kempermann G, Overstreet Wadiche L, Zhao C, Schinder AF, Bischofberger J. New neurons in the adult mammalian brain: synaptogenesis and functional integration. J Neurosci 2005; 25: 10366-8.
138. Barco A, Alarcon JM, Kandel ER. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 2002; 108: 689-03.
139. Pittenger C, Huang YY, Paletzki RF, et al. Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory. Neuron 2002; 34: 447-62.
140. Duffy SN, Nguyen PV. Postsynaptic application of a peptide inhibitor of cAMP-dependent protein kinase blocks expression of longlasting synaptic potentiation in hippocampal neurons. J Neurosci 2003; 23: 1142-50.
141. Jia Z, Lu YM, Agopyan N, Roder J. Gene targeting reveals a role for the glutamate receptors mGluR5 and GluR2 in learning and memory. Physiol Behav 2001; 73: 793-02.
142. O'Riordan KJ, Huang IC, Pizzi M, et al. Regulation of nuclear factor kappaB in the hippocampus by group I metabotropic glutamate receptors. J Neurosci 2006; 26: 4870-9.
143. Di Giorgi Gerevini VD, Caruso A, et al. The mGlu5 metabotropic glutamate receptor is expressed in zones of active neurogenesis of the embryonic and postnatal brain. Brain Res Dev Brain Res 2004; 150: 17-22.
144. De Smaele E, Zazzeroni F, Papa S, et al. Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling. Nature 2001; 414: 308-13.
145. Ma DK, Jang MH, Guo JU, et al. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 2009; 323: 1074-7.
146. Ma QH, Futagawa T, Yang WL, et al. A TAG1-APP signalling pathway through Fe65 negatively modulates neurogenesis. Nat Cell Biol 2008; 10: 283-94.
147. Cao X, Südhof TC. Dissection of amyloid-beta precursor protein-dependent transcriptional transactivation. J Biol Chem 2004; 279: 24601-11.
148. von Rotz RC, Kohli BM, Bosset J, et al. The APP intracellular domain forms nuclear multiprotein complexes and regulates the transcription of its own precursor. J Cell Sci 2004; 117: 4435-48.
149. Zhao Q, Lee FS. The transcriptional activity of the APP intracellular domain-Fe65 complex is inhibited by activation of the NF-kappaB pathway. Biochemistry 2003; 42: 3627-34.
150. Baek SH, Ohgi KA, Rose DW, Koo EH, Glass CK, Rosenfeld MG. Exchange of N-CoR corepressor and Tip60 coactivator complexes links gene expression by NF-kappaB and beta-amyloid precursor protein. Cell 2002; 110: 55-67.
151. Caillé I, Allinquant B, Dupont E, et al. Soluble form of amyloid precursor protein regulates proliferation of progenitors in the adult subventricular zone. Development 2004; 131: 2173-81.
152. Grilli M, Goffi F, Memo M, Spano PF. Interleukin-1beta and glutamate activate the NF-kappaB/Rel binding site from the regulatory region of the amyloid precursor protein gene in primary neuronal cultures. J Biol Chem 1996; 27: 15002-7.
153. Mattson MP, Meffert MK. Roles for NF-kappaB in nerve cell survival, plasticity, and disease. Cell Death Diff 2006; 13: 852-60.
154. Toliver-Kinsky T, Papaconstantinou J, Perez-Polo JR. Age-associated alterations in hippocampal and basal forebrain nuclear factor kappa B activity. J Neurosci Res 1997; 48: 580-7.
155. Greenberg DA. Neurogenesis and stroke. CNS Neurol Disord Drug Targets 2007; 6: 321-5.