Skip to main content
SpringerLink
Log in

NFκB signaling regulates embryonic and adult neurogenesis

  • Review
  • Published:
Frontiers in Biology

Abstract

Both embryonic and adult neurogenesis involves the self-renewal/proliferation, survival, migration and lineage differentiation of neural stem/progenitor cells. Such dynamic process is tightly regulated by intrinsic and extrinsic factors and complex signaling pathways. Misregulated neurogenesis contributes much to a large range of neurodevelopmental defects and neurodegenerative diseases. The signaling of NFκB regulates many genes important in inflammation, immunity, cell survival and neural plasticity. During neurogenesis, NFκB signaling mediates the effect of numerous niche factors such as cytokines, chemokines, growth factors, extracellular matrix molecules, but also crosstalks with other signaling pathways such as Notch, Shh, Wnt/β-catenin. This review summarizes current progress on the NFκB signaling in all aspects of neurogenesis, focusing on the novel role of NFκB signaling in initiating early neural differentiation of neural stem cells and embryonic stem cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alcamo E, Mizgerd J P, Horwitz B H, Bronson R, Beg A A, Scott M, Doerschuk C M, Hynes R O, Baltimore D (2001). Targeted mutation of TNF receptor I rescues the RelA-deficient mouse and reveals a critical role for NF-κB in leukocyte recruitment. J Immunol, 167(3): 1592–1600

    PubMed  CAS  Google Scholar 

  • Andres-Mach M, Fike J R, Łuszczki J J (2011). Neurogenesis in the epileptic brain: a brief overview from temporal lobe epilepsy. Pharmacol Rep, 63(6): 1316–1323

    PubMed  CAS  Google Scholar 

  • Andreu-Agulló C, Morante-Redolat JM, Delgado A C, Fariñas I (2009). Vascular niche factor PEDF modulates Notch-dependent stemness in the adult subependymal zone. Nat Neurosci, 12(12): 1514–1523

    PubMed  Google Scholar 

  • Ang H L, Tergaonkar V (2007). Notch and NFκB signaling pathways: Do they collaborate in normal vertebrate brain development and function? Bioessays, 29(10): 1039–1047

    PubMed  CAS  Google Scholar 

  • Angibaud J, Louveau A, Baudouin S J, Nerrière-Daguin V, Evain S, Bonnamain V, Hulin P, Csaba Z, Dournaud P, Thinard R, Naveilhan P, Noraz N, Pellier-Monnin V, Boudin H (2011). The immune molecule CD3zeta and its downstream effectors ZAP-70/Syk mediate ephrin signaling in neurons to regulate early neuritogenesis. J Neurochem, 119(4): 708–722

    PubMed  CAS  Google Scholar 

  • Artegiani B, Calegari F (2012). Age-related cognitive decline: Can neural stem cells help us? Aging (Albany NY), 4(3): 176–186

    Google Scholar 

  • Ayyar S, Pistillo D, Calleja M, Brookfield A, Gittins K, Goldstone C, Simpson P (2007). NF-κB/Rel-mediated regulation of the neural fate in Drosophila. PLoS ONE, 2(11): e1178

    PubMed  Google Scholar 

  • Azoitei N, Wirth T, Baumann B (2005). Activation of the IκB kinase complex is sufficient for neuronal differentiation of PC12 cells. J Neurochem, 93(6): 1487–1501

    PubMed  CAS  Google Scholar 

  • Beg A A, Sha W C, Bronson R T, Ghosh S, Baltimore D (1995). Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-κB. Nature, 376(6536): 167–170

    PubMed  CAS  Google Scholar 

  • Ben-Hur T, Ben-Menachem O, Furer V, Einstein O, Mizrachi-Kol R, Grigoriadis N (2003). Effects of proinflammatory cytokines on the growth, fate, and motility of multipotential neural precursor cells. Mol Cell Neurosci, 24(3): 623–631

    PubMed  CAS  Google Scholar 

  • Ben Menachem-Zidon O, Goshen I, Kreisel T, Ben Menahem Y, Reinhartz E, Ben Hur T, Yirmiya R (2008). Intrahippocampal transplantation of transgenic neural precursor cells overexpressing interleukin-1 receptor antagonist blocks chronic isolation-induced impairment in memory and neurogenesis. Neuropsychopharmacology, 33(9): 2251–2262

    PubMed  CAS  Google Scholar 

  • Bernardino L, Agasse F, Silva B, Ferreira R, Grade S, Malva J O (2008). Tumor necrosis factor-alpha modulates survival, proliferation, and neuronal differentiation in neonatal subventricular zone cell cultures. Stem Cells, 26(9): 2361–2371

    PubMed  CAS  Google Scholar 

  • Boersma M C, Dresselhaus E C, De Biase L M, Mihalas A B, Bergles D E, Meffert M K (2011). A requirement for nuclear factor-κB in developmental and plasticity-associated synaptogenesis. J Neurosci, 31(14): 5414–5425

    PubMed  CAS  Google Scholar 

  • Bonaguidi MA, Wheeler MA, Shapiro J S, Stadel R P, Sun G J, Ming G L, Song H (2011). In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell, 145(7): 1142–1155

    PubMed  CAS  Google Scholar 

  • Bonini S A, Ferrari-Toninelli G, Uberti D, Montinaro M, Buizza L, Lanni C, Grilli M, Memo M (2011). Nuclear factor κB-dependent neurite remodeling is mediated by Notch pathway. J Neurosci, 31(32): 11697–11705

    PubMed  CAS  Google Scholar 

  • Boyce B F, Yao Z, Xing L (2010). Functions of nuclear factor κB in bone. Ann N Y Acad Sci, 1192(1): 367–375

    PubMed  CAS  Google Scholar 

  • Cai C, Thorne J, Grabel L (2008). Hedgehog serves as a mitogen and survival factor during embryonic stem cell neurogenesis. Stem Cells, 26(5): 1097–1108

    PubMed  CAS  Google Scholar 

  • Callan M A, Zarnescu D C (2011). Heads-up: new roles for the fragile X mental retardation protein in neural stem and progenitor cells. Genesis, 49(6): 424–440

    PubMed  CAS  Google Scholar 

  • Camandola S, Mattson M P (2007). NF-κB as a therapeutic target in neurodegenerative diseases. Expert Opin Ther Targets, 11(2): 123–132

    PubMed  CAS  Google Scholar 

  • Cao Q, Kaur C, Wu C Y, Lu J, Ling E A (2011). Nuclear factor-κβ regulates notch signaling in production of proinflammatory cytokines and nitric oxide in murine BV-2 microglial cells. Neuroscience, 192: 140–154

    PubMed  CAS  Google Scholar 

  • Cau E, Gradwohl G, Casarosa S, Kageyama R, Guillemot F (2000). Hes genes regulate sequential stages of neurogenesis in the olfactory epithelium. Development, 127(11): 2323–2332

    PubMed  CAS  Google Scholar 

  • Chen G, Handel K, Roth S (2000). The maternal NF-κB/dorsal gradient of Tribolium castaneum: dynamics of early dorsoventral patterning in a short-germ beetle. Development, 127(23): 5145–5156

    PubMed  CAS  Google Scholar 

  • Chen L F, Greene WC (2004). Shaping the nuclear action of NF-κB. Nat Rev Mol Cell Biol, 5(5): 392–401

    PubMed  CAS  Google Scholar 

  • Cho H H, Shin K K, Kim Y J, Song J S, Kim J M, Bae Y C, Kim C D, Jung J S (2010). NF-κB activation stimulates osteogenic differentiation of mesenchymal stem cells derived from human adipose tissue by increasing TAZ expression. J Cell Physiol, 223(1): 168–177

    PubMed  CAS  Google Scholar 

  • Conti L, Cattaneo E (2010). Neural stem cell systems: physiological players or in vitro entities? Nat Rev Neurosci, 11(3): 176–187

    PubMed  CAS  Google Scholar 

  • Cox R, Chen S H, Yoo E, Segev N (2007). Conservation of the TRAPPII-specific subunits of a Ypt/Rab exchanger complex. BMC Evol Biol, 7(1): 12

    PubMed  Google Scholar 

  • Curtis MA, Low VF, Faull RL (2012). Neurogenesis and progenitor cells in the adult human brain: a comparison between hippocampal and subventricular progenitor proliferation. Dev Neurobiol, Online Available April 27, 2012

    Google Scholar 

  • Das S, Basu A (2008). Inflammation: a new candidate in modulating adult neurogenesis. J Neurosci Res, 86(6): 1199–1208

    PubMed  CAS  Google Scholar 

  • Dave R K, Ellis T, Toumpas M C, Robson J P, Julian E, Adolphe C, Bartlett P F, Cooper H M, Reynolds B A, Wainwright B J (2011). Sonic hedgehog and notch signaling can cooperate to regulate neurogenic divisions of neocortical progenitors. PLoS ONE, 6(2): e14680

    PubMed  CAS  Google Scholar 

  • DeLotto R, DeLotto Y, Steward R, Lippincott-Schwartz J (2007). Nucleocytoplasmic shuttling mediates the dynamic maintenance of nuclear Dorsal levels during Drosophila embryogenesis. Development, 134(23): 4233–4241

    PubMed  CAS  Google Scholar 

  • Denham M, Parish C L, Leaw B, Wright J, Reid C A, Petrou S, Dottori M, Thompson L H (2012). Neurons derived from human embryonic stem cells extend long-distance axonal projections through growth along host white matter tracts after intra-cerebral transplantation. Front Cell Neurosci, 6: 11

    PubMed  CAS  Google Scholar 

  • Denis-Donini S, Caprini A, Frassoni C, Grilli M (2005). Members of the NF-κB family expressed in zones of active neurogenesis in the postnatal and adult mouse brain. Brain Res Dev Brain Res, 154(1): 81–89

    PubMed  CAS  Google Scholar 

  • Denis-Donini S, Dellarole A, Crociara P, Francese M T, Bortolotto V, Quadrato G, Canonico P L, Orsetti M, Ghi P, Memo M, Bonini S A, Ferrari-Toninelli G, Grilli M (2008). Impaired adult neurogenesis associated with short-term memory defects in NF-κB p50-deficient mice. J Neurosci, 28(15): 3911–3919

    PubMed  CAS  Google Scholar 

  • Dominguez I, Sanz L, Arenzana-Seisdedos F, Diaz-Meco MT, Virelizier J L, Moscat J (1993). Inhibition of protein kinase C zeta subspecies blocks the activation of an NF-κB-like activity in Xenopus laevis oocytes. Mol Cell Biol, 13(2): 1290–1295

    PubMed  CAS  Google Scholar 

  • Dong J, Liu B, Song L, Lu L, Xu H, Gu Y (2011). Neural stem cells in the ischemic and injured brain: endogenous and transplanted. Cell Tissue Bank Online Available Dec 21, 2011

  • Encinas J M, Sierra A (2012). Neural stem cell deforestation as the main force driving the age-related decline in adult hippocampal neurogenesis. Behav Brain Res, 227(2): 433–439

    PubMed  Google Scholar 

  • Encinas J M, Vazquez M E, Switzer R C, Chamberland D W, Nick H, Levine H G, Scarpa P J, Enikolopov G, Steindler D A (2008). Quiescent adult neural stem cells are exceptionally sensitive to cosmic radiation. Exp Neurol, 210(1): 274–279

    PubMed  Google Scholar 

  • Feng Z, Porter A G (1999). NF-κB/Rel proteins are required for neuronal differentiation of SH-SY5Y neuroblastoma cells. J Biol Chem, 274(43): 30341–30344

    PubMed  CAS  Google Scholar 

  • Fior R, Henrique D (2005). A novel hes5/hes6 circuitry of negative regulation controls Notch activity during neurogenesis. Dev Biol, 281(2): 318–333

    PubMed  CAS  Google Scholar 

  • Foehr E D, Bohuslav J, Chen L F, DeNoronha C, Geleziunas R, Lin X, O’Mahony A, Greene W C (2000). The NF-κB-inducing kinase induces PC12 cell differentiation and prevents apoptosis. J Biol Chem, 275(44): 34021–34024

    PubMed  CAS  Google Scholar 

  • Fridmacher V, Kaltschmidt B, Goudeau B, Ndiaye D, Rossi F M, Pfeiffer J, Kaltschmidt C, Israël A, Mémet S (2003). Forebrainspecific neuronal inhibition of nuclear factor-κB activity leads to loss of neuroprotection. J Neurosci, 23(28): 9403–9408

    PubMed  CAS  Google Scholar 

  • Fujita K, Yasui S, Shinohara T, Ito K (2011). Interaction between NF-κB signaling and Notch signaling in gliogenesis of mouse mesencephalic neural crest cells. Mech Dev, 128(7–10): 496–509

    PubMed  CAS  Google Scholar 

  • Gallagher D, Gutierrez H, Gavalda N, O’Keeffe G, Hay R, Davies A M (2007). Nuclear factor-κB activation via tyrosine phosphorylation of inhibitor κB-alpha is crucial for ciliary neurotrophic factor-promoted neurite growth from developing neurons. J Neurosci, 27(36): 9664–9669

    PubMed  CAS  Google Scholar 

  • Gavaldà N, Gutierrez H, Davies A M (2009). Developmental regulation of sensory neurite growth by the tumor necrosis factor superfamily member LIGHT. J Neurosci, 29(6): 1599–1607

    PubMed  Google Scholar 

  • Gavert N, Vivanti A, Hazin J, Brabletz T, Ben-Ze’ev A (2011). L1-mediated colon cancer cell metastasis does not require changes in EMT and cancer stem cell markers. Mol Cancer Res, 9(1): 14–24

    PubMed  CAS  Google Scholar 

  • Ghosh A, Roy A, Liu X, Kordower J H, Mufson E J, Hartley D M, Ghosh S, Mosley R L, Gendelman H E, Pahan K (2007). Selective inhibition of NF-κB activation prevents dopaminergic neuronal loss in a mouse model of Parkinson’s disease. Proc Natl Acad Sci USA, 104(47): 18754–18759

    PubMed  CAS  Google Scholar 

  • Gloire G, Legrand-Poels S, Piette J (2006). NF-κB activation by reactive oxygen species: fifteen years later. Biochem Pharmacol, 72(11): 1493–1505

    PubMed  CAS  Google Scholar 

  • Gloire G, Piette J (2009). Redox regulation of nuclear post-translational modifications during NF-κB activation. Antioxid Redox Signal, 11(9): 2209–2222

    PubMed  CAS  Google Scholar 

  • Goshen I, Kreisel T, Ben-Menachem-Zidon O, Licht T, Weidenfeld J, Ben-Hur T, Yirmiya R (2008). Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol Psychiatry, 13(7): 717–728

    PubMed  CAS  Google Scholar 

  • Goshen I, Yirmiya R (2009). Interleukin-1 (IL-1): a central regulator of stress responses. Front Neuroendocrinol, 30(1): 30–45

    PubMed  CAS  Google Scholar 

  • Granic I, Dolga A M, Nijholt I M, van Dijk G, Eisel U L (2009). Inflammation and NF-κB in Alzheimer’s disease and diabetes. J Alzheimers Dis, 16(4): 809–821

    PubMed  Google Scholar 

  • Green H F, Treacy E, Keohane A K, Sullivan A M, O’Keeffe G W, Nolan Y M (2012). A role for interleukin-1β in determining the lineage fate of embryonic rat hippocampal neural precursor cells. Mol Cell Neurosci, 49(3): 311–321

    PubMed  CAS  Google Scholar 

  • Grossmann M, Metcalf D, Merryfull J, Beg A, Baltimore D, Gerondakis S (1999). The combined absence of the transcription factors Rel and RelA leads to multiple hemopoietic cell defects. Proc Natl Acad Sci USA, 96(21): 11848–11853

    PubMed  CAS  Google Scholar 

  • Gutierrez H, Davies A M (2011). Regulation of neural process growth, elaboration and structural plasticity by NF-κB. Trends Neurosci, 34(6): 316–325

    PubMed  CAS  Google Scholar 

  • Häcker H, Karin M (2006). Regulation and function of IKK and IKKrelated kinases. Sci STKE, 2006(357): re13

    PubMed  Google Scholar 

  • Hanson N D, Owens M J, Nemeroff C B (2011). Depression, antidepressants, and neurogenesis: a critical reappraisal. Neuropsychopharmacology, 36(13): 2589–2602

    PubMed  Google Scholar 

  • Hashimoto R, Ohi K, Yasuda Y, Fukumoto M, Yamamori H, Takahashi H, Iwase M, Okochi T, Kazui H, Saitoh O, Tatsumi M, Iwata N, Ozaki N, Kamijima K, Kunugi H, Takeda M (2011). Variants of the RELA gene are associated with schizophrenia and their startle responses. Neuropsychopharmacology, 36(9): 1921–1931

    PubMed  CAS  Google Scholar 

  • Heanue T A, Pachnis V (2007). Enteric nervous system development and Hirschsprung’s disease: advances in genetic and stem cell studies. Nat Rev Neurosci, 8(6): 466–479

    PubMed  CAS  Google Scholar 

  • Hess K, Ushmorov A, Fiedler J, Brenner R E, Wirth T (2009). TNFalpha promotes osteogenic differentiation of human mesenchymal stem cells by triggering the NF-κB signaling pathway. Bone, 45(2): 367–376

    PubMed  CAS  Google Scholar 

  • Hodge R D, Hevner R F (2011). Expression and actions of transcription factors in adult hippocampal neurogenesis. Dev Neurobiol, 71(8): 680–689

    PubMed  CAS  Google Scholar 

  • Hu WH, Pendergast J S, Mo X M, Brambilla R, Bracchi-Ricard V, Li F, Walters W M, Blits B, He L, Schaal S M, Bethea J R (2005). NIBP, a novel NIK and IKK(beta)-binding protein that enhances NF-(κ)B activation. J Biol Chem, 280(32): 29233–29241

    PubMed  CAS  Google Scholar 

  • Huehnchen P, Prozorovski T, Klaissle P, Lesemann A, Ingwersen J, Wolf S A, Kupsch A, Aktas O, Steiner B (2011). Modulation of adult hippocampal neurogenesis during myelin-directed autoimmune neuroinflammation. Glia, 59(1): 132–142

    PubMed  Google Scholar 

  • Huillard E, Ziercher L, Blond O, Wong M, Deloulme J C, Souchelnytskyi S, Baudier J, Cochet C, Buchou T (2010). Disruption of CK2beta in embryonic neural stem cells compromises proliferation and oligodendrogenesis in the mouse telencephalon. Mol Cell Biol, 30(11): 2737–2749

    PubMed  CAS  Google Scholar 

  • Hyun Hwa C, Hye Joon J, Ji Sun S, Yong Chan B, Jin Sup J (2008). Crossregulation of beta-catenin/Tcf pathway by NF-κB is mediated by lzts2 in human adipose tissue-derived mesenchymal stem cells. Biochim Biophys Acta, (3): 419–428

  • Ideguchi M, Shinoyama M, Gomi M, Hayashi H, Hashimoto N, Takahashi J (2008). Immune or inflammatory response by the host brain suppresses neuronal differentiation of transplanted ES cellderived neural precursor cells. J Neurosci Res, 86(9): 1936–1943

    PubMed  CAS  Google Scholar 

  • Imielski Y, Schwamborn J C, Lüningschrör P, Heimann P, Holzberg M, Werner H, Leske O, Püschel A W, Memet S, Heumann R, Israel A, Kaltschmidt C, Kaltschmidt B (2012). Regrowing the adult brain: NF-κB controls functional circuit formation and tissue homeostasis in the dentate gyrus. PLoS ONE, 7(2): e30838

    PubMed  CAS  Google Scholar 

  • Inta D, Meyer-Lindenberg A, Gass P (2011). Alterations in postnatal neurogenesis and dopamine dysregulation in schizophrenia: a hypothesis. Schizophr Bull, 37(4): 674–680

    PubMed  Google Scholar 

  • Islam O, Gong X, Rose-John S, Heese K (2009). Interleukin-6 and neural stem cells: more than gliogenesis. Mol Biol Cell, 20(1): 188–199

    PubMed  CAS  Google Scholar 

  • Johansson S, Price J, Modo M (2008). Effect of inflammatory cytokines on major histocompatibility complex expression and differentiation of human neural stem/progenitor cells. Stem Cells, 26(9): 2444–2454

    PubMed  CAS  Google Scholar 

  • Kageyama R, Ohtsuka T, Kobayashi T (2008). Roles of Hes genes in neural development. Dev Growth Differ, 50(Suppl 1): S97–S103

    PubMed  CAS  Google Scholar 

  • Kajiwara K, Ogata S, Tanihara M (2005). Promotion of neurite outgrowth from fetal hippocampal cells by TNF-alpha receptor 1-derived peptide. Cell Transplant, 14(9): 665–672

    PubMed  Google Scholar 

  • Kaltschmidt B, Kaltschmidt C (2009). NF-κB in the nervous system. Cold Spring Harb Perspect Biol, 1(3): a001271

    PubMed  Google Scholar 

  • Kang H B, Kim Y E, Kwon H J, Sok D E, Lee Y (2007). Enhancement of NF-κB expression and activity upon differentiation of human embryonic stem cell line SNUhES3. Stem Cells Dev, 16(4): 615–624

    PubMed  CAS  Google Scholar 

  • Kasperczyk H, Baumann B, Debatin K M, Fulda S (2009). Characterization of sonic hedgehog as a novel NF-κB target gene that promotes NF-κB-mediated apoptosis resistance and tumor growth in vivo. FASEB J, 23(1): 21–33

    PubMed  CAS  Google Scholar 

  • Kato T Jr, Delhase M, Hoffmann A, Karin M (2003). CK2 Is a CTerminal IκB Kinase Responsible for NF-κB Activation during the UV Response. Mol Cell, 12(4): 829–839

    PubMed  CAS  Google Scholar 

  • Kaul M (2008). HIV’s double strike at the brain: neuronal toxicity and compromised neurogenesis. Front Biosci, 13(13): 2484–2494

    PubMed  CAS  Google Scholar 

  • Kennedy K A, Ostrakhovitch E A, Sandiford S D, Dayarathna T, Xie X, Waese E Y, Chang W Y, Feng Q, Skerjanc I S, Stanford W L, Li S S (2010). Mammalian numb-interacting protein 1/dual oxidase maturation factor 1 directs neuronal fate in stem cells. J Biol Chem, 285(23): 17974–17985

    PubMed  CAS  Google Scholar 

  • Kennedy K A, Sandiford S D, Skerjanc I S, Li S S (2012). Reactive oxygen species and the neuronal fate. Cell Mol Life Sci, 69(2): 215–221

    PubMed  CAS  Google Scholar 

  • Keohane A, Ryan S, Maloney E, Sullivan A M, Nolan Y M (2010). Tumour necrosis factor-alpha impairs neuronal differentiation but not proliferation of hippocampal neural precursor cells: Role of Hes1. Mol Cell Neurosci, 43(1): 127–135

    PubMed  CAS  Google Scholar 

  • Kim J, Wong P K (2009). Loss of ATM impairs proliferation of neural stem cells through oxidative stress-mediated p38 MAPK signaling. Stem Cells, 27(8): 1987–1998

    PubMed  CAS  Google Scholar 

  • Kim J H, Park S H, Park S G, Choi J S, Xia Y, Sung J H (2011a). The pivotal role of reactive oxygen species generation in the hypoxiainduced stimulation of adipose-derived stem cells. Stem Cells Dev, 20(10): 1753–1761

    PubMed  CAS  Google Scholar 

  • Kim J M, Song J S, Cho H H, Shin K K, Bae Y C, Lee B J, Jung J S (2011b). Effect of the modulation of leucine zipper tumor suppressor 2 expression on proliferation of various cancer cells functions as a tumor suppressor. Mol Cell Biochem, 346(1–2): 125–136

    PubMed  CAS  Google Scholar 

  • Kim Y E, Kang H B, Park J A, Nam K H, Kwon H J, Lee Y (2008). Upregulation of NF-κB upon differentiation of mouse embryonic stem cells. BMB Rep, 41(10): 705–709

    PubMed  Google Scholar 

  • Kishi N, Macklis J D (2010). MeCP2 functions largely cellautonomously, but also non-cell-autonomously, in neuronal maturation and dendritic arborization of cortical pyramidal neurons. Exp Neurol, 222(1): 51–58

    PubMed  CAS  Google Scholar 

  • Kondo T, Matsuoka A J, Shimomura A, Koehler K R, Chan R J, Miller J M, Srour E F, Hashino E (2011). Wnt signaling promotes neuronal differentiation from mesenchymal stem cells through activation of Tlx3. Stem Cells, 29(5): 836–846

    PubMed  CAS  Google Scholar 

  • Köntgen F, Grumont R J, Strasser A, Metcalf D, Li R, Tarlinton D, Gerondakis S (1995). Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev, 9(16): 1965–1977

    PubMed  Google Scholar 

  • Koo J W, Duman R S (2008). IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc Natl Acad Sci USA, 105(2): 751–756

    PubMed  CAS  Google Scholar 

  • Koo J W, Duman R S (2009). Evidence for IL-1 receptor blockade as a therapeutic strategy for the treatment of depression. Curr Opin Investig Drugs, 10(7): 664–671

    PubMed  CAS  Google Scholar 

  • Koo J W, Russo S J, Ferguson D, Nestler E J, Duman R S (2010). Nuclear factor-κB is a critical mediator of stress-impaired neurogenesis and depressive behavior. Proc Natl Acad Sci USA, 107(6): 2669–2674

    PubMed  CAS  Google Scholar 

  • Kümmel D, Oeckinghaus A, Wang C, Krappmann D, Heinemann U (2008). Distinct isocomplexes of the TRAPP trafficking factor coexist inside human cells. FEBS Lett, 582(27): 3729–3733

    PubMed  Google Scholar 

  • Lake B B, Ford R, Kao K R (2001). Xrel3 is required for head development in Xenopus laevis. Development, 128(2): 263–273

    PubMed  CAS  Google Scholar 

  • Le Belle J E, Orozco N M, Paucar A A, Saxe J P, Mottahedeh J, Pyle A D, Wu H, Kornblum H I (2011). Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell, 8(1): 59–71

    PubMed  Google Scholar 

  • Le Douarin N M, Calloni G W, Dupin E (2008). The stem cells of the neural crest. Cell Cycle, 7(8): 1013–1019

    PubMed  Google Scholar 

  • Li Q, Estepa G, Memet S, Israel A, Verma I M (2000). Complete lack of NF-κB activity in IKK1 and IKK2 double-deficient mice: additional defect in neurulation. Genes Dev, 14(14): 1729–1733

    PubMed  CAS  Google Scholar 

  • Li Q, Spencer N Y, Oakley F D, Buettner G R, Engelhardt J F (2009). Endosomal Nox2 facilitates redox-dependent induction of NF-κB by TNF-alpha. Antioxid Redox Signal, 11(6): 1249–1263

    PubMed  CAS  Google Scholar 

  • Lilienbaum A, Sage J, Mémet S, Rassoulzadegan M, Cuzin F, Israël A (2000). NF-κB is developmentally regulated during spermatogenesis in mice. Dev Dyn, 219(3): 333–340

    PubMed  CAS  Google Scholar 

  • Lin Y, Bai L, Chen W, Xu S (2010). The NF-κB activation pathways, emerging molecular targets for cancer prevention and therapy. Expert Opin Ther Targets, 14(1): 45–55

    PubMed  CAS  Google Scholar 

  • Lou S J, Gu P, Xu H, Xu X H, Wang M W, He C, Lu C L (2003). Effect of tumor necrosis factor-alpha on differentiation of mesencephalic neural stem cells and proliferation of oligodendrocytes in the rat. Sheng Li Xue Bao, 55(2): 183–186

    PubMed  CAS  Google Scholar 

  • Lum M, Croze E, Wagner C, McLenachan S, Mitrovic B, Turnley A M (2008). Inhibition of neurosphere proliferation by IFNgamma but not IFNbeta is coupled to neuronal differentiation. J Neuroimmunol, 206(1–2):32–38

    PubMed  Google Scholar 

  • Lüningschrör P, Stöcker B, Kaltschmidt B, Kaltschmidt C (2012). miR-290 cluster modulates pluripotency by repressing canonical NF-κB signaling. Stem Cells, 30(4): 655–664

    PubMed  Google Scholar 

  • Ma D K, Bonaguidi M A, Ming G L, Song H (2009). Adult neural stem cells in the mammalian central nervous system. Cell Res, 19(6): 672–682

    PubMed  CAS  Google Scholar 

  • Mancino A, Lawrence T (2010). Nuclear factor-κB and tumor-associated macrophages. Clin Cancer Res, 16(3): 784–789

    PubMed  CAS  Google Scholar 

  • Maniati E, Bossard M, Cook N, Candido J B, Emami-Shahri N, Nedospasov S A, Balkwill F R, Tuveson D A, Hagemann T (2011). Crosstalk between the canonical NF-κB and Notch signaling pathways inhibits Pparγ expression and promotes pancreatic cancer progression in mice. J Clin Invest, 121(12): 4685–4699

    PubMed  CAS  Google Scholar 

  • Marcora E, Kennedy M B (2010). The Huntington’s disease mutation impairs Huntingtin’s role in the transport of NF-κB from the synapse to the nucleus. Hum Mol Genet, 19(22): 4373–4384

    PubMed  CAS  Google Scholar 

  • Massa P T, Aleyasin H, Park D S, Mao X, Barger S W (2006). NFκB in neurons? The uncertainty principle in neurobiology. J Neurochem, 97(3): 607–618

    PubMed  CAS  Google Scholar 

  • Mattson M P, Culmsee C, Yu Z, Camandola S (2000). Roles of nuclear factor κB in neuronal survival and plasticity. J Neurochem, 74(2): 443–456

    PubMed  CAS  Google Scholar 

  • Mattson M P, Meffert M K (2006). Roles for NF-κB in nerve cell survival, plasticity, and disease. Cell Death Differ, 13(5): 852–860

    PubMed  CAS  Google Scholar 

  • Meneghini V, Francese MT, Carraro L, Grilli M (2010). A novel role for the receptor for advanced glycation end-products in neural progenitor cells derived from adult SubVentricular Zone. Mol Cell Neurosci, 45(2): 139–150

    PubMed  CAS  Google Scholar 

  • Metzger M (2010). Neurogenesis in the enteric nervous system. Arch Ital Biol, 148(2): 73–83

    PubMed  Google Scholar 

  • Ming G L, Song H (2011). Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron, 70(4): 687–702

    PubMed  CAS  Google Scholar 

  • Mir A, Kaufman L, Noor A, Motazacker M M, Jamil T, Azam M, Kahrizi K, Rafiq M A, Weksberg R, Nasr T, Naeem F, Tzschach A, Kuss A W, Ishak G E, Doherty D, Ropers H H, Barkovich A J, Najmabadi H, Ayub M, Vincent J B (2009). Identification of mutations in TRAPPC9, which encodes the NIK- and IKK-betabinding protein, in nonsyndromic autosomal-recessive mental retardation. Am J Hum Genet, 85(6): 909–915

    PubMed  CAS  Google Scholar 

  • Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S (2003). The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell, 113(5): 631–642

    PubMed  CAS  Google Scholar 

  • Mochida G H, Mahajnah M, Hill A D, Basel-Vanagaite L, Gleason D, Hill R S, Bodell A, Crosier M, Straussberg R, Walsh C A (2009). A truncating mutation of TRAPPC9 is associated with autosomalrecessive intellectual disability and postnatal microcephaly. Am J Hum Genet, 85(6): 897–902

    PubMed  CAS  Google Scholar 

  • Montano-Almendras C P, Essaghir A, Schoemans H, Varis I, Noel LA, Velghe AI, Latinne D, Knoops L, Demoulin J B (2012). ETV6-PDGFRB and FIP1L1-PDGFRA stimulate human hematopoietic progenitor proliferation and differentiation into eosinophils: role of NF-κB. Haematologica, Online Available Jan 22, 2012

    Google Scholar 

  • Morgan M J, Liu Z G (2011). Crosstalk of reactive oxygen species and NF-κB signaling. Cell Res, 21(1): 103–115

    PubMed  CAS  Google Scholar 

  • Mu Y, Gage F H (2011). Adult hippocampal neurogenesis and its role in Alzheimer’s disease. Mol Neurodegener, 6(1): 85

    PubMed  Google Scholar 

  • Mu Y, Lee SW, Gage F H (2010). Signaling in adult neurogenesis. Curr Opin Neurobiol, 20(4): 416–423

    PubMed  CAS  Google Scholar 

  • Mukaino M, Nakamura M, Okada S, Toyama Y, Liu M, Okano H (2008). [Role of IL-6 in regulation of inflammation and stem cell differentiation in CNS trauma]. Nihon Rinsho Meneki Gakkai Kaishi, 31(2): 93–98 (Role of IL-6 in regulation of inflammation and stem cell differentiation in CNS trauma)

    PubMed  CAS  Google Scholar 

  • Nakanishi M, Niidome T, Matsuda S, Akaike A, Kihara T, Sugimoto H (2007). Microglia-derived interleukin-6 and leukaemia inhibitory factor promote astrocytic differentiation of neural stem/progenitor cells. Eur J Neurosci, 25(3): 649–658

    PubMed  Google Scholar 

  • Nishikimi A, Mukai J, Yamada M (1999). Nuclear translocation of nuclear factor κB in early 1-cell mouse embryos. Biol Reprod, 60(6): 1536–1541

    PubMed  CAS  Google Scholar 

  • Nogueira L, Ruiz-Ontañon P, Vazquez-Barquero A, Lafarga M, Berciano M T, Aldaz B, Grande L, Casafont I, Segura V, Robles E F, Suarez D, Garcia L F, Martinez-Climent J A, Fernandez-Luna J L (2011). Blockade of the NFκB pathway drives differentiating glioblastoma-initiating cells into senescence both in vitro and in vivo. Oncogene, 30(32): 3537–3548

    PubMed  CAS  Google Scholar 

  • Noor A, Windpassinger C, Patel M, Stachowiak B, Mikhailov A, Azam M, Irfan M, Siddiqui Z K, Naeem F, Paterson A D, Lutfullah M, Vincent J B, Ayub M (2008). CC2D2A, encoding a coiled-coil and C2 domain protein, causes autosomal-recessive mental retardation with retinitis pigmentosa. Am J Hum Genet, 82(4): 1011–1018

    PubMed  CAS  Google Scholar 

  • Okamoto S, Kang Y J, Brechtel C W, Siviglia E, Russo R, Clemente A, Harrop A, McKercher S, Kaul M, Lipton S A (2007). HIV/gp120 decreases adult neural progenitor cell proliferation via checkpoint kinase-mediated cell-cycle withdrawal and G1 arrest. Cell Stem Cell, 1(2): 230–236

    PubMed  CAS  Google Scholar 

  • Okano H (2006). Adult neural stem cells and central nervous system repair. Ernst Schering Res Found Workshop, 60: 215–228

    PubMed  CAS  Google Scholar 

  • Osakada F, Takahashi M (2011). Neural induction and patterning in Mammalian pluripotent stem cells. CNS Neurol Disord Drug Targets, 10(4): 419–432

    PubMed  CAS  Google Scholar 

  • Paciolla M, Boni R, Fusco F, Pescatore A, Poeta L, Ursini M V, Lioi M B, Miano M G (2011). Nuclear factor-κ-B-inhibitor alpha (NFKBIA) is a developmental marker of NF-κB/p65 activation during in vitro oocyte maturation and early embryogenesis. Hum Reprod, 26(5): 1191–1201

    PubMed  CAS  Google Scholar 

  • Pan J X, Ding K, Wang C Y (2012). Niclosamide, an old antihelminthic agent, demonstrates antitumor activity by blocking multiple signaling pathways of cancer stem cells. Chin J Cancer, Online Available Jan 9, 2012

    Google Scholar 

  • Pardal R, Ortega-Sáenz P, Durán R, Platero-Luengo A, López-Barneo J (2010). The carotid body, a neurogenic niche in the adult peripheral nervous system. Arch Ital Biol, 148(2): 95–105

    PubMed  CAS  Google Scholar 

  • Pathania M, Yan L D, Bordey A (2010). A symphony of signals conducts early and late stages of adult neurogenesis. Neuropharmacology, 58(6): 865–876

    PubMed  CAS  Google Scholar 

  • Pei Y, Brun S N, Markant S L, Lento W, Gibson P, Taketo M M, Giovannini M, Gilbertson R J, Wechsler-Reya R J (2012). WNT signaling increases proliferation and impairs differentiation of stem cells in the developing cerebellum. Development, 139(10): 1724–1733

    PubMed  CAS  Google Scholar 

  • Peng H, Whitney N, Wu Y, Tian C, Dou H, Zhou Y, Zheng J (2008). HIV-1-infected and/or immune-activated macrophage-secreted TNFalpha affects human fetal cortical neural progenitor cell proliferation and differentiation. Glia, 56(8): 903–916

    PubMed  Google Scholar 

  • Perkins N D (2007). Integrating cell-signalling pathways with NF-κB and IKK function. Nat Rev Mol Cell Biol, 8(1): 49–62

    PubMed  CAS  Google Scholar 

  • Philippe O, Rio M, Carioux A, Plaza J M, Guigue P, Molinari F, Boddaert N, Bole-Feysot C, Nitschke P, Smahi A, Munnich A, Colleaux L (2009). Combination of linkage mapping and microarrayexpression analysis identifies NF-κB signaling defect as a cause of autosomal-recessive mental retardation. Am J Hum Genet, 85(6): 903–908

    PubMed  CAS  Google Scholar 

  • Piao Y J, Seo Y H, Hong F, Kim J H, Kim Y J, Kang MH, Kim B S, Jo S A, Jo I, Jue D M, Kang I, Ha J, Kim S S (2005). Nox 2 stimulates muscle differentiation via NF-κB/iNOS pathway. Free Radic Biol Med, 38(8): 989–1001

    PubMed  CAS  Google Scholar 

  • Politi C, Del Turco D, Sie JM, Golinski P A, Tegeder I, Deller T, Schultz C (2008). Accumulation of phosphorylated IκB alpha and activated IKK in nodes of Ranvier. Neuropathol Appl Neurobiol, 34(3): 357–365

    PubMed  CAS  Google Scholar 

  • Qin L, Crews F T (2012). NADPH oxidase and reactive oxygen species contribute to alcohol-induced microglial activation and neurodegeneration. J Neuroinflammation, 9(1): 5

    PubMed  CAS  Google Scholar 

  • Quirling M, Page S, Jilg N, Plenagl K, Peus D, Grubmüller C, Weingärtner M, Fischer C, Neumeier D, Brand K (2004). Detection of IKKbeta-IKKgamma subcomplexes in monocytic cells and characterization of associated signaling. J Biol Chem, 279(36): 37452–37460

    PubMed  CAS  Google Scholar 

  • Razani B, Reichardt A D, Cheng G (2011). Non-canonical NF-κB signaling activation and regulation: principles and perspectives. Immunol Rev, 244(1): 44–54

    PubMed  CAS  Google Scholar 

  • Reeves G T, Stathopoulos A (2009). Graded dorsal and differential gene regulation in the Drosophila embryo. Cold Spring Harb Perspect Biol, 1(4): a000836

    PubMed  Google Scholar 

  • Reikvam H, Olsnes A M, Gjertsen B T, Ersvar E, Bruserud O (2009). Nuclear factor-κB signaling: a contributor in leukemogenesis and a target for pharmacological intervention in human acute myelogenous leukemia. Crit Rev Oncog, 15(1–2): 1–41

    Google Scholar 

  • Ricci-Vitiani L, Casalbore P, Petrucci G, Lauretti L, Montano N, Larocca L M, Falchetti M L, Lombardi D G, Gerevini V D, Cenciarelli C, D’Alessandris Q G, Fernandez E, De Maria R, Maira G, Peschle C, Parati E, Pallini R (2006). Influence of local environment on the differentiation of neural stem cells engrafted onto the injured spinal cord. Neurol Res, 28(5): 488–492

    PubMed  Google Scholar 

  • Richards G R, Smith A J, Cuddon P, Ma Q P, Leveridge M, Kerby J, Roderick H L, Bootman M D, Simpson P B (2006). The JAK3 inhibitor WHI-P154 prevents PDGF-evoked process outgrowth in human neural precursor cells. J Neurochem, 97(1): 201–210

    PubMed  CAS  Google Scholar 

  • Richardson J C, Garcia Estrabot A M, Woodland H R (1994). XrelA, a Xenopus maternal and zygotic homologue of the p65 subunit of NF-κ B. Characterisation of transcriptional properties in the developing embryo and identification of a negative interference mutant. Mech Dev, 45(2): 173–189

    CAS  Google Scholar 

  • Rolls A, Shechter R, London A, Ziv Y, Ronen A, Levy R, Schwartz M (2007). Toll-like receptors modulate adult hippocampal neurogenesis. Nat Cell Biol, 9(9): 1081–1088

    PubMed  CAS  Google Scholar 

  • Rubio-Araiz A, Arévalo-Martín A, Gómez-Torres O, Navarro-Galve B, García-Ovejero D, Suetterlin P, Sánchez-Heras E, Molina-Holgado E, Molina-Holgado F (2008). The endocannabinoid system modulates a transient TNF pathway that induces neural stem cell proliferation. Mol Cell Neurosci, 38(3): 374–380

    PubMed  CAS  Google Scholar 

  • Saldanha-Araujo F, Haddad R, Malmegrim de Farias K C, Alves Souza AD, Palma P V, Araujo A G, Orellana M D, Voltarelli J C, Covas D T, Zago M A, Panepucci R A (2011). Mesenchymal stem cells promote the sustained expression of CD69 on activated Tlymphocytes: roles of canonical and non-canonical NF-κB signaling. J Cell Mol Med, Online Available July 21, 2011

    Google Scholar 

  • Sanchez-Ponce D, Tapia M, Muñoz A, Garrido J J (2008). New role of IKK alpha/beta phosphorylated I κB alpha in axon outgrowth and axon initial segment development. Mol Cell Neurosci, 37(4): 832–844

    PubMed  CAS  Google Scholar 

  • Sauvageot C M, Stiles C D (2002). Molecular mechanisms controlling cortical gliogenesis. Curr Opin Neurobiol, 12(3): 244–249

    PubMed  CAS  Google Scholar 

  • Schäfer K H, Micci M A, Pasricha P J (2009). Neural stem cell transplantation in the enteric nervous system: roadmaps and roadblocks. Neurogastroenterol Motil, 21(2): 103–112

    PubMed  Google Scholar 

  • Schmidt-Ullrich R, Mémet S, Lilienbaum A, Feuillard J, Raphaël M, Israel A (1996). NF-κB activity in transgenic mice: developmental regulation and tissue specificity. Development, 122(7): 2117–2128

    PubMed  CAS  Google Scholar 

  • Schölzke M N, Röttinger A, Murikinati S, Gehrig N, Leib C, Schwaninger M (2011). TWEAK regulates proliferation and differentiation of adult neural progenitor cells. Mol Cell Neurosci, 46(1): 325–332

    PubMed  Google Scholar 

  • Schölzke M N, Schwaninger M (2007). Transcriptional regulation of neurogenesis: potential mechanisms in cerebral ischemia. J Mol Med (Berl), 85(6): 577–588

    Google Scholar 

  • Schultz C, König H G, Del Turco D, Politi C, Eckert G P, Ghebremedhin E, Prehn J H, Kögel D, Deller T (2006). Coincident enrichment of phosphorylated IκBalpha, activated IKK, and phosphorylated p65 in the axon initial segment of neurons. Mol Cell Neurosci, 33(1): 68–80

    PubMed  CAS  Google Scholar 

  • Schwarz T J, Ebert B, Lie D C (2012). Stem cell maintenance in the adult mammalian hippocampus: A matter of signal integration? Dev Neurobiol, Online Available April 5, 2012

  • Senftleben U, Cao Y, Xiao G, Greten F R, Krähn G, Bonizzi G, Chen Y, Hu Y, Fong A, Sun S C, Karin M (2001). Activation by IKKalpha of a second, evolutionary conserved, NF-κ B signaling pathway. Science, 293(5534): 1495–1499

    PubMed  CAS  Google Scholar 

  • Sha D, Chin L S, Li L (2010). Phosphorylation of parkin by Parkinson disease-linked kinase PINK1 activates parkin E3 ligase function and NF-κB signaling. Hum Mol Genet, 19(2): 352–363

    PubMed  CAS  Google Scholar 

  • Sha W C, Liou H C, Tuomanen E I, Baltimore D (1995). Targeted disruption of the p50 subunit of NF-κB leads to multifocal defects in immune responses. Cell, 80(2): 321–330

    PubMed  CAS  Google Scholar 

  • Shi Y, Sun G, Zhao C, Stewart R (2008). Neural stem cell self-renewal. Crit Rev Oncol Hematol, 65(1): 43–53

    PubMed  Google Scholar 

  • Shingo T, Sorokan S T, Shimazaki T, Weiss S (2001). Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J Neurosci, 21(24): 9733–9743

    PubMed  CAS  Google Scholar 

  • Siebzehnrubl F A, Vedam-Mai V, Azari H, Reynolds B A, Deleyrolle L P (2011). Isolation and characterization of adult neural stem cells. Methods Mol Biol, 750: 61–77

    PubMed  Google Scholar 

  • Song X Q, Lv L X, Li W Q, Hao Y H, Zhao J P (2009). The interaction of nuclear factor-κB and cytokines is associated with schizophrenia. Biol Psychiatry, 65(6): 481–488

    PubMed  CAS  Google Scholar 

  • Sun S C (2012). The noncanonical NF-κB pathway. Immunol Rev, 246(1): 125–140

    PubMed  Google Scholar 

  • Taupin P (2008). Adult neurogenesis, neuroinflammation and therapeutic potential of adult neural stem cells. Int J Med Sci, 5(3): 127–132

    PubMed  CAS  Google Scholar 

  • Teng F Y, Tang B L (2010). NF-κB signaling in neurite growth and neuronal survival. Rev Neurosci, 21(4): 299–314

    PubMed  CAS  Google Scholar 

  • Tepavčević V, Lazarini F, Alfaro-Cervello C, Kerninon C, Yoshikawa K, Garcia-Verdugo J M, Lledo P M, Nait-Oumesmar B, Baron-Van Evercooren A (2011). Inflammation-induced subventricular zone dysfunction leads to olfactory deficits in a targeted mouse model of multiple sclerosis. J Clin Invest, 121(12): 4722–4734

    PubMed  Google Scholar 

  • Torchinsky A, Toder V (2004). To die or not to die: the function of the transcription factor NF-κB in embryos exposed to stress. Am J Reprod Immunol, 51(2): 138–143

    PubMed  CAS  Google Scholar 

  • Torres J, Watt F M (2008). Nanog maintains pluripotency of mouse embryonic stem cells by inhibiting NFκB and cooperating with Stat3. Nat Cell Biol, 10(2): 194–201

    PubMed  CAS  Google Scholar 

  • Vaillend C, Poirier R, Laroche S (2008). Genes, plasticity and mental retardation. Behav Brain Res, 192(1): 88–105

    PubMed  CAS  Google Scholar 

  • Vaira S, Johnson T, Hirbe A C, Alhawagri M, Anwisye I, Sammut B, O’Neal J, Zou W, Weilbaecher K N, Faccio R, Novack D V (2008). RelB is the NF-κB subunit downstream of NIK responsible for osteoclast differentiation. Proc Natl Acad Sci USA, 105(10): 3897–3902

    PubMed  CAS  Google Scholar 

  • van den Berge S A, van Strien M E, Korecka J A, Dijkstra A A, Sluijs J A, Kooijman L, Eggers R, De Filippis L, Vescovi A L, Verhaagen J, van de Berg W D, Hol E M (2011). The proliferative capacity of the subventricular zone is maintained in the parkinsonian brain. Brain, 134(Pt 11): 3249–3263

    PubMed  Google Scholar 

  • Viatour P, Merville M P, Bours V, Chariot A (2005). Phosphorylation of NF-κB and IκB proteins: implications in cancer and inflammation. Trends Biochem Sci, 30(1): 43–52

    PubMed  CAS  Google Scholar 

  • Vieira H L, Alves P M, Vercelli A (2011). Modulation of neuronal stem cell differentiation by hypoxia and reactive oxygen species. Prog Neurobiol, 93(3): 444–455

    PubMed  CAS  Google Scholar 

  • Vilas-Boas F, Henrique D (2010). HES6-1 and HES6-2 function through different mechanisms during neuronal differentiation. PLoS ONE, 5(12): e15459

    PubMed  CAS  Google Scholar 

  • Villeda S A, Luo J, Mosher K I, Zou B, Britschgi M, Bieri G, Stan T M, Fainberg N, Ding Z, Eggel A, Lucin K M, Czirr E, Park J S, Couillard-Després S, Aigner L, Li G, Peskind E R, Kaye J A, Quinn J F, Galasko D R, Xie X S, Rando T A, Wyss-Coray T (2011). The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature, 477(7362): 90–94

    PubMed  CAS  Google Scholar 

  • Wang D D, Bordey A (2008). The astrocyte odyssey. Prog Neurobiol, 86(4): 342–367

    PubMed  CAS  Google Scholar 

  • Weih F, Durham S K, Barton D S, Sha W C, Baltimore D, Bravo R (1997). p50-NF-κB complexes partially compensate for the absence of RelB: severely increased pathology in p50-/-relB-/-doubleknockout mice. J Exp Med, 185(7): 1359–1370

    PubMed  CAS  Google Scholar 

  • Westlake C J, Baye L M, Nachury M V, Wright K J, Ervin K E, Phu L, Chalouni C, Beck J S, Kirkpatrick D S, Slusarski D C, Sheffield V C, Scheller R H, Jackson P K (2011). Primary cilia membrane assembly is initiated by Rab11 and transport protein particle II (TRAPPII) complex-dependent trafficking of Rabin8 to the centrosome. Proc Natl Acad Sci USA, 108(7): 2759–2764

    PubMed  CAS  Google Scholar 

  • Whitney N P, Eidem T M, Peng H, Huang Y, Zheng J C (2009). Inflammation mediates varying effects in neurogenesis: relevance to the pathogenesis of brain injury and neurodegenerative disorders. J Neurochem, 108(6): 1343–1359

    PubMed  CAS  Google Scholar 

  • Widera D, Kaus A, Kaltschmidt C, Kaltschmidt B (2008). Neural stem cells, inflammation and NF-κB: basic principle of maintenance and repair or origin of brain tumours? J Cell Mol Med, 12(2): 459–470

    PubMed  CAS  Google Scholar 

  • Widera D, Mikenberg I, Elvers M, Kaltschmidt C, Kaltschmidt B (2006a). Tumor necrosis factor alpha triggers proliferation of adult neural stem cells via IKK/NF-κB signaling. BMC Neurosci, 7(1): 64

    PubMed  Google Scholar 

  • Widera D, Mikenberg I, Kaltschmidt B, Kaltschmidt C (2006b). Potential role of NF-κB in adult neural stem cells: the underrated steersman? Int J Dev Neurosci, 24(2–3): 91–102

    PubMed  CAS  Google Scholar 

  • Widera D, Mikenberg I, Kaus A, Kaltschmidt C, Kaltschmidt B (2006c). Nuclear factor-κB controls the reaggregation of 3D neurosphere cultures in vitro. Eur Cell Mater, 11: 76–84, discussion 85

    PubMed  CAS  Google Scholar 

  • Winner B, Kohl Z, Gage F H (2011). Neurodegenerative disease and adult neurogenesis. Eur J Neurosci, 33(6): 1139–1151

    PubMed  Google Scholar 

  • Wong E T, Tergaonkar V (2009). Roles of NF-κB in health and disease: mechanisms and therapeutic potential. Clin Sci (Lond), 116(6): 451–465

    CAS  Google Scholar 

  • Wong G, Goldshmit Y, Turnley A M (2004). Interferon-gamma but not TNF alpha promotes neuronal differentiation and neurite outgrowth of murine adult neural stem cells. Exp Neurol, 187(1): 171–177

    PubMed  CAS  Google Scholar 

  • Wooten M W, Seibenhener M L, Neidigh K B, Vandenplas M L (2000). Mapping of atypical protein kinase C within the nerve growth factor signaling cascade: relationship to differentiation and survival of PC12 cells. Mol Cell Biol, 20(13): 4494–4504

    PubMed  CAS  Google Scholar 

  • Woronicz J D, Gao X, Cao Z, Rothe M, Goeddel D V (1997). IκB kinase-beta: NF-κB activation and complex formation with IκB kinase-alpha and NIK. Science, 278(5339): 866–869

    PubMed  CAS  Google Scholar 

  • Wu J P, Kuo J S, Liu Y L, Tzeng S F (2000). Tumor necrosis factor-alpha modulates the proliferation of neural progenitors in the subventricular/ ventricular zone of adult rat brain. Neurosci Lett, 292(3): 203–206

    PubMed  CAS  Google Scholar 

  • Xiao M, Inal C E, Parekh V I, Li X H, Whitnall M H (2009). Role of NF-κB in hematopoietic niche function of osteoblasts after radiation injury. Exp Hematol, 37(1): 52–64

    PubMed  CAS  Google Scholar 

  • Yaddanapudi K, De Miranda J, Hornig M, Lipkin W I (2011). Toll-like receptor 3 regulates neural stem cell proliferation by modulating the Sonic Hedgehog pathway. PLoS ONE, 6(10): e26766

    PubMed  CAS  Google Scholar 

  • Yang C, Atkinson S P, Vilella F, Lloret M, Armstrong L, Mann D A, Lako M (2010). Opposing putative roles for canonical and noncanonical NFκB signaling on the survival, proliferation, and differentiation potential of human embryonic stem cells. Stem Cells, 28(11): 1970–1980

    PubMed  CAS  Google Scholar 

  • Yang L, Tao L Y, Chen X P (2007). Roles of NF-κB in central nervous system damage and repair. Neurosci Bull, 23(5): 307–313

    PubMed  CAS  Google Scholar 

  • Yeo J E, Kang S K 2007. Selenium effectively inhibits ROS-mediated apoptotic neural precursor cell death in vitro and in vivo in traumatic brain injury. Biochim Biophys Acta, (11–12): 1199–1210

  • Yirmiya R, Goshen I (2011). Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav Immun, 25(2): 181–213

    PubMed  CAS  Google Scholar 

  • Yoneyama M, Kawada K, Gotoh Y, Shiba T, Ogita K (2010). Endogenous reactive oxygen species are essential for proliferation of neural stem/progenitor cells. Neurochem Int, 56(6–7): 740–746

    PubMed  CAS  Google Scholar 

  • Young K M, Bartlett P F, Coulson E J (2006). Neural progenitor number is regulated by nuclear factor-κB p65 and p50 subunit-dependent proliferation rather than cell survival. J Neurosci Res, 83(1): 39–49

    PubMed  CAS  Google Scholar 

  • Zhang C, Wu H, Zhu X, Wang Y, Guo J (2011). Role of transcription factors in neurogenesis after cerebral ischemia. Rev Neurosci, 22(4): 457–465

    PubMed  Google Scholar 

  • Zhang Q, Wang C, Liu Z, Liu X, Han C, Cao X, Li N (2012a). Notch signal suppresses Toll-like receptor-triggered inflammatory responses in macrophages by inhibiting extracellular signal-regulated kinase 1/2-mediated nuclear factor κB activation. J Biol Chem, 287(9): 6208–6217

    PubMed  CAS  Google Scholar 

  • Zhang Y, Liu J, Yao S, Li F, Xin L, Lai M, Bracchi-Ricard V, Xu H, Yen W, Meng W, Liu S, Yang L, Karmally S, Liu J, Zhu H, Gordon J, Khalili K, Srinivasan S, Bethea J R, Mo X, Hu W (2012b). Nuclear factor κB signaling initiates early differentiation of neural stem cells. Stem Cells, 30(3): 510–524

    PubMed  CAS  Google Scholar 

  • Zhao C, Deng W, Gage F H (2008). Mechanisms and functional implications of adult neurogenesis. Cell, 132(4): 645–660

    PubMed  CAS  Google Scholar 

  • Zhao C, Xiu Y, Ashton J, Xing L, Morita Y, Jordan C T, Boyce B F (2012). Noncanonical NF-κB signaling regulates hematopoietic stem cell self-renewal and microenvironment interactions. Stem Cells, 30(4): 709–718

    PubMed  CAS  Google Scholar 

  • Zhao M, Li X D, Chen Z (2010). CC2D1A, a DM14 and C2 domain protein, activates NF-κB through the canonical pathway. J Biol Chem, 285(32): 24372–24380

    PubMed  CAS  Google Scholar 

  • Zhu C, Liu Z, Gui L, Yao W, Qian W, Zhang C (2008). Mutated IκBalpha represses proliferation of immortalized neural progenitor cells and prevents their apoptosis after oxygen-glucose deprivation. Brain Res, 1244: 24–31

    PubMed  CAS  Google Scholar 

  • Ziercher L, Filhol O, Laudet B, Prudent R, Cochet C, Buchou T (2011). Structure-function analysis of the beta regulatory subunit of protein kinase CK2 by targeting embryonic stem cell. Mol Cell Biochem, 356(1–2): 75–81

    PubMed  CAS  Google Scholar 

  • Zong M, Satoh A, Yu M K, Siu K Y, Ng W Y, Chan H C, Tanner J A, Yu S (2012). TRAPPC9 mediates the interaction between p150 and COPII vesicles at the target membrane. PLoS ONE, 7(1): e29995

    PubMed  CAS  Google Scholar 

  • Zong M, Wu X G, Chan C W, Choi M Y, Chan H C, Tanner J A, Yu S (2011). The adaptor function of TRAPPC2 in mammalian TRAPPs explains TRAPPC2-associated SEDT and TRAPPC9-associated congenital intellectual disability. PLoS ONE, 6(8): e23350

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neuroscience, Temple University School of Medicine, Philadelphia, PA, 19140, USA

    Yonggang Zhang & Wenhui Hu

Authors
  1. Yonggang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wenhui Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wenhui Hu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, Y., Hu, W. NFκB signaling regulates embryonic and adult neurogenesis. Front. Biol. 7, 277–291 (2012). https://doi.org/10.1007/s11515-012-1233-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11515-012-1233-z

Keywords

Search

Navigation