Immunological regulation of neurogenic niches in the adult brain

Neuroscience

Volumn 226, Issue , 2012, Pages 270-281

  Gonzalez Perez, O ^a,b   Gutierrez Fernandez, F ^a   Lopez Virgen, V ^a   Collas Aguilar, J ^a   Quinones Hinojosa, A ^c   Garcia Verdugo, J M ^d  

^a UNIVERSIDAD DE COLIMA   (Mexico)

^b UNIVERSITY OF GUADALAJARA   (Mexico)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

Author keywords

Cytokine; Inflammation; Interleukin; Microglia; Neural stem cells; Subventricular zone

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CILIARY NEUROTROPHIC FACTOR; G PROTEIN COUPLED RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 1; INTERLEUKIN 15; INTERLEUKIN 18; INTERLEUKIN 6; LEUKEMIA INHIBITORY FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; SOMATOMEDIN C; STROMAL CELL DERIVED FACTOR 1; TUMOR NECROSIS FACTOR ALPHA;

ASTROCYTE; BRAIN; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TYPE; CONTROLLED STUDY; CYTOARCHITECTURE; DEGENERATIVE DISEASE; GRANULAR CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; MICROGLIA; NEURAL STEM CELL; NEUROGENIC NICHE; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SPATIAL MEMORY; SUBVENTRICULAR ZONE;

ANIMALS; BRAIN; CHEMOKINES; CYTOKINES; HUMANS; NEURAL STEM CELLS; NEURODEGENERATIVE DISEASES; NEUROGENESIS;

EID: 84867287224     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.08.053     Document Type: Review

References (144)

1. Aguirre A., Dupree J.L., Mangin J.M., Gallo V. A functional role for EGFR signaling in myelination and remyelination. Nat Neurosci 2007, 10:990-1002.
2. Aimone J.B., Deng W., Gage F.H. Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 2011, 70:589-596.
3. Ajmone-Cat M.A., Cacci E., Ragazzoni Y., Minghetti L., Biagioni S. Pro-gliogenic effect of IL-1alpha in the differentiation of embryonic neural precursor cells in vitro. J Neurochem 2010, 113:1060-1072.
4. Akiyama S., Yonezawa T., Kudo T.A., Li M.G., Wang H., Ito M., Yoshioka K., Ninomiya-Tsuji J., Matsumoto K., Kanamaru R., Tamura S., Kobayashi T. Activation mechanism of c-Jun amino-terminal kinase in the course of neural differentiation of P19 embryonic carcinoma cells. J Biol Chem 2004, 279:36616-36620.
5. Alboni S., Cervia D., Sugama S., Conti B. Interleukin 18 in the CNS. J Neuroinflamm 2010, 7:9-20.
6. Alvarez-Buylla A., Garcia-Verdugo J.M., Tramontin A.D. A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2001, 2(2):287-293.
7. Amura C.R., Marek L., Winn R.A., Heasley L.E. Inhibited neurogenesis in JNK1-deficient embryonic stem cells. Mol Cell Biol 2005, 25:10791-10802.
8. Battista D., Ferrari C.C., Gage F.H., Pitossi F.J. Neurogenic niche modulation by activated microglia: transforming growth factor beta increases neurogenesis in the adult dentate gyrus. Eur J Neurosci 2006, 23:83-93.
9. Bauer S. Cytokine control of adult neural stem cells. Ann N Y Acad Sci 2009, 1153:48-56.
10. Bauer S., Patterson P.H. Leukemia inhibitory factor promotes neural stem cell self-renewal in the adult brain. J Neurosci 2006, 26:12089-12099.
11. Ben-Hur T., Ben-Menachem O., Furer V., Einstein O., Mizrachi-Kol R., Grigoriadis N. Effects of proinflammatory cytokines on the growth, fate, and motility of multipotential neural precursor cells. Mol Cell Neurosci 2003, 24:623-631.
12. Bonecchi R., Galliera E., Borroni E.M., Corsi M.M., Locati M., Mantovani A. Chemokines and chemokine receptors: an overview. Front Biosci 2009, 14:540-551.
13. Bonfanti L. From hydra regeneration to human brain structural plasticity: a long trip through narrowing roads. ScientificWorldJournal 2011, 11:1270-1299.
14. Boutin C., Hardt O., de Chevigny A., Core N., Goebbels S., Seidenfaden R., Bosio A., Cremer H. NeuroD1 induces terminal neuronal differentiation in olfactory neurogenesis. Proc Natl Acad Sci U S A 2010, 107:1201-1206.
15. Burdon T., Smith A., Savatier P. Signalling, cell cycle and pluripotency in embryonic stem cells. Trends Cell Biol 2002, 12:432-438.
16. Butovsky O., Ziv Y., Schwartz A., Landa G., Talpalar A.E., Pluchino S., Martino G., Schwartz M. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 2006, 31:149-160.
17. Campbell I.L., Abraham C.R., Masliah E., Kemper P., Inglis J.D., Oldstone M.B., Mucke L. Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc Natl Acad Sci U S A 1993, 90:10061-10065.
18. Choi Y.S., Cho H.Y., Hoyt K.R., Naegele J.R., Obrietan K. IGF-1 receptor-mediated ERK/MAPK signaling couples status epilepticus to progenitor cell proliferation in the subgranular layer of the dentate gyrus. Glia 2008, 56:791-800.
19. Cooper O., Isacson O. Intrastriatal transforming growth factor alpha delivery to a model of Parkinson's disease induces proliferation and migration of endogenous adult neural progenitor cells without differentiation into dopaminergic neurons. J Neurosci 2004, 24:8924-8931.
20. Cordiglieri C., Farina C. Astrocytes Exert and Control Immune Responses in the Brain. Curr Immunol Rev 2010, 6:150-159.
21. Costa R.A., Ruiz-de-Souza V., Azevedo G.M., Gava E., Kitten G.T., Vaz N.M., Carvalho C.R. Indirect effects of oral tolerance improve wound healing in skin. Wound Repair Regen 2011, 19:487-497.
22. Covey M.V., Levison S.W. Leukemia inhibitory factor participates in the expansion of neural stem/progenitors after perinatal hypoxia/ischemia. Neuroscience 2007, 148:501-509.
23. Craig C.G., Tropepe V., Morshead C.M., Reynolds B.A., Weiss S., Van der Kooy D. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 1996, 16:2649-2658.
24. Curtis M.A., Penney E.B., Pearson A.G., van Roon-Mom W.M., Butterworth N.J., Dragunow M., Connor B., Faull R.L. Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc Natl Acad Sci U S A 2003, 100:9023-9027.
25. Curtis M.A., Faull R.L., Eriksson P.S. The effect of neurodegenerative diseases on the subventricular zone. Nat Rev Neurosci 2007, 8:712-723.
26. Das S., Basu A. Inflammation: a new candidate in modulating adult neurogenesis. J Neurosci Res 2008, 86:1199-1208.
27. Deng W., Aimone J.B., Gage F.H. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nat Rev Neurosci 2010, 11:339-350.
28. Dominguez E., Rivat C., Pommier B., Mauborgne A., Pohl M. JAK/STAT3 pathway is activated in spinal cord microglia after peripheral nerve injury and contributes to neuropathic pain development in rat. J Neurochem 2008, 107:50-60.
29. Ekdahl C.T., Claasen J.H., Bonde S., Kokaia Z., Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci U S A 2003, 100:13632-13637.
30. Eugenin E.A., D'Aversa T.G., Lopez L., Calderon T.M., Berman J.W. MCP-1 (CCL2) protects human neurons and astrocytes from NMDA or HIV-tat-induced apoptosis. J Neurochem 2003, 85:1299-1311.
31. Fahmy G.H., Sicard R.E. A role for effectors of cellular immunity in epimorphic regeneration of amphibian limbs. In Vivo 2002, 16:179-184.
32. Feng R., Rampon C., Tang Y.P., Shrom D., Jin J., Kyin M., Sopher B., Miller M.W., Ware C.B., Martin G.M., Kim S.H., Langdon R.B., Sisodia S.S., Tsien J.Z. Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron 2001, 32:911-926.
33. Gage F.H. Neurogenesis in the adult brain. J Neurosci 2002, 22:612-613.
34. Galileo D.S., Gray G.E., Owens G.C., Majors J., Sanes J.R. Neurons and glia arise from a common progenitor in chicken optic tectum: demonstration with two retroviruses and cell type-specific antibodies. Proc Natl Acad Sci U S A 1990, 87:458-462.
35. Galvao R.P., Garcia-Verdugo J.M., Alvarez-Buylla A. Brain-derived neurotrophic factor signaling does not stimulate subventricular zone neurogenesis in adult mice and rats. J Neurosci 2008, 28:13368-13383.
36. Galvez-Contreras A.Y., Gonzalez-Castaneda R.E., Luquin S., Gonzalez-Perez O. Role of fibroblast growth factor receptors in astrocytic stem cells. Curr Signal Transduct Ther 2012, 7:81-86.
37. Giunta B., Obregon D., Velisetty R., Sanberg P.R., Borlongan C.V., Tan J. The immunology of traumatic brain injury: a prime target for Alzheimer inverted question marks disease prevention. J Neuroinflamm 2012, 9:185-192.
38. Gomez-Nicola D., Valle-Argos B., Pallas-Bazarra N., Nieto-Sampedro M. Interleukin-15 regulates proliferation and self-renewal of adult neural stem cells. Mol Biol Cell 2011, 22:1960-1970.
39. Gong X., He X., Qi L., Zuo H., Xie Z. Stromal cell derived factor-1 acutely promotes neural progenitor cell proliferation in vitro by a mechanism involving the ERK1/2 and PI-3K signal pathways. Cell Biol Int 2006, 30:466-471.
40. Gonzalez-Castaneda R.E., Galvez-Contreras A.Y., Luquin S., Gonzalez-Perez O. Neurogenesis in Alzheimer's disease: a realistic alternative to neuronal degeneration?. Curr Signal Transduct Ther 2011, 6:314-319.
41. Gonzalez-Perez O., Alvarez-Buylla A. Oligodendrogenesis in the subventricular zone and the role of epidermal growth factor. Brain Res Rev 2011, 67:147-156.
42. Gonzalez-Perez O., Quinones-Hinojosa A. Dose-dependent effect of EGF on migration and differentiation of adult subventricular zone astrocytes. Glia 2010, 58:975-983.
43. Gonzalez-Perez O., Ramos-Remus C., Garcia-Estrada J., Luquin S. Prednisone induces anxiety and glial cerebral changes in rats. J Rheumatol 2001, 28:2529-2534.
44. Gonzalez-Perez O., Romero-Rodriguez R., Soriano-Navarro M., Garcia-Verdugo J.M., Alvarez-Buylla A. Epidermal growth factor induces the progeny of subventricular zone type B cells to migrate and differentiate into oligodendrocytes. Stem Cells 2009, 27:2032-2043.
45. Gonzalez-Perez O., Chavez-Casillas O., Jauregui-Huerta F., Lopez-Virgen V., Guzman-Muniz J., Moy-Lopez N., Gonzalez-Castaneda R.E., Luquin S. Stress by noise produces differential effects on the proliferation rate of radial astrocytes and survival of neuroblasts in the adult subgranular zone. Neurosci Res 2011, 70:243-250.
46. Gordon R.J., McGregor A.L., Connor B. Chemokines direct neural progenitor cell migration following striatal cell loss. Mol Cell Neurosci 2009, 41:219-232.
47. Gordon R.J., Mehrabi N.F., Maucksch C., Connor B. Chemokines influence the migration and fate of neural precursor cells from the young adult and middle-aged rat subventricular zone. Exp Neurol 2011, 233:587-594.
48. Gordon R.J., Mehrabi N.F., Maucksch C., Connor B. Chemokines influence the migration and fate of neural precursor cells from the young adult and middle-aged rat subventricular zone. Exp Neurol 2012, 233:587-594.
49. Greco S.J., Rameshwar P. Enhancing effect of IL-1alpha on neurogenesis from adult human mesenchymal stem cells: implication for inflammatory mediators in regenerative medicine. J Immunol 2007, 179:3342-3350.
50. Grunblatt E., Mandel S., Youdim M.B. Neuroprotective strategies in Parkinson's disease using the models of 6-hydroxydopamine and MPTP. Ann N Y Acad Sci 2000, 899:262-273.
51. Hama T., Kushima Y., Miyamoto M., Kubota M., Takei N., Hatanaka H. Interleukin-6 improves the survival of mesencephalic catecholaminergic and septal cholinergic neurons from postnatal, two-week-old rats in cultures. Neuroscience 1991, 40:445-452.
52. Harty M., Neff A.W., King M.W., Mescher A.L. Regeneration or scarring: an immunologic perspective. Dev Dyn 2003, 226:268-279.
53. Hickey W.F. Leukocyte traffic in the central nervous system: the participants and their roles. Semin Immunol 1999, 11:125-137.
54. Huang Y.S., Cheng S.N., Chueh S.H., Tsai Y.L., Liou N.H., Guo Y.W., Liao M.H., Shen L.H., Chen C.C., Liu J.C., Ma K.H. Effects of interleukin-15 on neuronal differentiation of neural stem cells. Brain Res 2009, 1304:38-48.
55. Iosif R.E., Ekdahl C.T., Ahlenius H., Pronk C.J., Bonde S., Kokaia Z., Jacobsen S.E., Lindvall O. Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J Neurosci 2006, 26:9703-9712.
56. Islam O., Gong X., Rose-John S., Heese K. Interleukin-6 and neural stem cells: more than gliogenesis. Mol Biol Cell 2009, 20:188-199.
57. Jackson E.L., Garcia-Verdugo J.M., Gil-Perotin S., Roy M., Quinones-Hinojosa A., VandenBerg S., Alvarez-Buylla A. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 2006, 51:187-199.
58. Jauregui-Huerta F., Ruvalcaba-Delgadillo Y., Gonzalez-Castaneda R., Garcia-Estrada J., Gonzalez-Perez O., Luquin S. Responses of glial cells to stress and glucocorticoids. Curr Immunol Rev 2010, 6:195-204.
59. Jin K., Peel A.L., Mao X.O., Xie L., Cottrell B.A., Henshall D.C., Greenberg D.A. Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci U S A 2004, 101:343-347.
60. Jin K., Galvan V., Xie L., Mao X.O., Gorostiza O.F., Bredesen D.E., Greenberg D.A. Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSw, Ind) mice. Proc Natl Acad Sci U S A 2004, 101:13363-13367.
61. Johansson S., Price J., Modo M. Effect of inflammatory cytokines on major histocompatibility complex expression and differentiation of human neural stem/progenitor cells. Stem Cells 2008, 26:2444-2454.
62. Kabatas S., Cansever T., Civelek E., Yilmaz E.C. The therapeutic potential of neural stem cells in traumatic brain injuries. Curr Signal Transduct Ther 2011, 6:327-336.
63. Kasahara Y., Nakagomi T., Nakano-Doi A., Matsuyama T., Taguchi A. The therapeutic potential of neural stem cells in cerebral ischemia. Curr Signal Transduct Ther 2011, 6:347-352.
64. Keohane A., Ryan S., Maloney E., Sullivan A.M., Nolan Y.M. Tumour necrosis factor-alpha impairs neuronal differentiation but not proliferation of hippocampal neural precursor cells: role of Hes1. Mol Cell Neurosci 2009, 43:127-135.
65. Kim S.J., Son T.G., Kim K., Park H.R., Mattson M.P., Lee J. Interferon-gamma promotes differentiation of neural progenitor cells via the JNK pathway. Neurochem Res 2007, 32:1399-1406.
66. Kokaia Z., Martino G., Schwartz M., Lindvall O. Cross-talk between neural stem cells and immune cells: the key to better brain repair?. Nat Neurosci 2012, 15:1078-1087.
67. Kokovay E., Goderie S., Wang Y., Lotz S., Lin G., Sun Y., Roysam B., Shen Q., Temple S. Adult SVZ lineage cells home to and leave the vascular niche via differential responses to SDF1/CXCR4 signaling. Cell Stem Cell 2010, 7:163-173.
68. Koo J.W., Duman R.S. IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc Natl Acad Sci U S A 2008, 105:751-756.
69. Koo J.W., Duman R.S. Evidence for IL-1 receptor blockade as a therapeutic strategy for the treatment of depression. Curr Opin Investig Drugs 2009, 10:664-671.
70. Krathwohl M.D., Kaiser J.L. HIV-1 promotes quiescence in human neural progenitor cells. J Infect Dis 2004, 190:216-226.
71. Kriegstein A., Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 2009, 32:149-184.
72. Kuhn H.G., Winkler J., Kempermann G., Thal L.J., Gage F.H. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 1997, 17:5820-5829.
73. Lai K., Kaspar B.K., Gage F.H., Schaffer D.V. Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat Neurosci 2003, 6:21-27.
74. Leipzig N.D., Xu C., Zahir T., Shoichet M.S. Functional immobilization of interferon-gamma induces neuronal differentiation of neural stem cells. J Biomed Mater Res A 2010, 93:625-633.
75. Leonard B.E. The concept of depression as a dysfunction of the immune system. Curr Immunol Rev 2010, 6:205-212.
76. Leong S.Y., Turnley A.M. Regulation of adult neural precursor cell migration. Neurochem Int 2011, 59:382-393.
77. Lindvall O., Kokaia Z. Stem cells in human neurodegenerative disorders - time for clinical translation?. J Clin Invest 2010, 120:29-40.
78. Liu Y.P., Lin H.I., Tzeng S.F. Tumor necrosis factor-alpha and interleukin-18 modulate neuronal cell fate in embryonic neural progenitor culture. Brain Res 2005, 1054:152-158.
79. Liu X.S., Zhang Z.G., Zhang R.L., Gregg S.R., Wang L., Yier T., Chopp M. Chemokine ligand 2 (CCL2) induces migration and differentiation of subventricular zone cells after stroke. J Neurosci Res 2007, 85:2120-2125.
80. Lois C., Alvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci U S A 1993, 90:2074-2077.
81. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994, 264:1145-1148.
82. Machold R., Hayashi S., Rutlin M., Muzumdar M.D., Nery S., Corbin J.G., Gritli-Linde A., Dellovade T., Porter J.A., Rubin L.L., Dudek H., McMahon A.P., Fishell G. Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 2003, 39:937-950.
83. Makela J., Koivuniemi R., Korhonen L., Lindholm D. Interferon-gamma produced by microglia and the neuropeptide PACAP have opposite effects on the viability of neural progenitor cells. PLoS One 2010, 5:e11091.
84. Martino G., Pluchino S., Bonfanti L., Schwartz M. Brain regeneration in physiology and pathology: the immune signature driving therapeutic plasticity of neural stem cells. Physiol Rev 2011, 91:1281-1304.
85. Mathieu P., Battista D., Depino A., Roca V., Graciarena M., Pitossi F. The more you have, the less you get: the functional role of inflammation on neuronal differentiation of endogenous and transplanted neural stem cells in the adult brain. J Neurochem 2010, 112:1368-1385.
86. Matsumoto A., Onoyama I., Sunabori T., Kageyama R., Okano H., Nakayama K.I. Fbxw7-dependent degradation of Notch is required for control of "stemness" and neuronal-glial differentiation in neural stem cells. J Biol Chem 2011, 286:13754-13764.
87. McPherson C.A., Aoyama M., Harry G.J. Interleukin (IL)-1 and IL-6 regulation of neural progenitor cell proliferation with hippocampal injury: differential regulatory pathways in the subgranular zone (SGZ) of the adolescent and mature mouse brain. Brain Behav Immun 2011, 25:850-862.
88. Menn B., Garcia-Verdugo J.M., Yaschine C., Gonzalez-Perez O., Rowitch D., Alvarez-Buylla A. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 2006, 26:7907-7918.
89. Mertens B., Vanderheyden P., Michotte Y., Sarre S. The role of the central renin-angiotensin system in Parkinson's disease. J Renin Angiotensin Aldosterone Syst 2010, 11:49-56.
90. Mescher A.L., Neff A.W. Limb regeneration in amphibians: immunological considerations. ScientificWorldJournal 2006, 6(Suppl. 1):1-11.
91. Miller R.J., Rostene W., Apartis E., Banisadr G., Biber K., Milligan E.D., White F.A., Zhang J. Chemokine action in the nervous system. J Neurosci 2008, 28:11792-11795.
92. Ming G.L., Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 2011, 70:687-702.
93. Mirzadeh Z., Merkle F.T., Soriano-Navarro M., Garcia-Verdugo J.M., Alvarez-Buylla A. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 2008, 3:265-278.
94. Mitrecic D., Nicaise C., Gajovic S., Pochet R. The therapeutic potential of stem cells in amyotrophic lateral sclerosis. Curr Signal Transduct Ther 2011, 6:341-346.
95. Molyneaux K.A., Zinszner H., Kunwar P.S., Schaible K., Stebler J., Sunshine M.J., O'Brien W., Raz E., Littman D., Wylie C., Lehmann R. The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival. Development 2003, 130:4279-4286.
96. Mongiat L.A., Schinder A.F. Adult neurogenesis and the plasticity of the dentate gyrus network. Eur J Neurosci 2011, 33:1055-1061.
97. Monje M.L., Toda H., Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003, 302:1760-1765.
98. Morgan S.C., Taylor D.L., Pocock J.M. Microglia release activators of neuronal proliferation mediated by activation of mitogen-activated protein kinase, phosphatidylinositol-3-kinase/Akt and delta-Notch signalling cascades. J Neurochem 2004, 90:89-101.
99. Muller N., Schwarz M.J. Immune system and schizophrenia. Curr Immunol Rev 2010, 6:213-220.
100. Nakagomi N., Nakagomi T., Kubo S., Nakano-Doi A., Saino O., Takata M., Yoshikawa H., Stern D.M., Matsuyama T., Taguchi A. Endothelial cells support survival, proliferation, and neuronal differentiation of transplanted adult ischemia-induced neural stem/progenitor cells after cerebral infarction. Stem Cells 2009, 27:2185-2195.
101. Northrop N.A., Yamamoto B.K. Neuroimmune pharmacology from a neuroscience perspective. J Neuroimmune Pharmacol 2011, 6:10-19.
102. Oshima K., Teo D.T., Senn P., Starlinger V., Heller S. LIF promotes neurogenesis and maintains neural precursors in cell populations derived from spiral ganglion stem cells. BMC Dev Biol 2007, 7:112.
103. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 1997, 17:3727-3738.
104. Pechnick R.N., Zonis S., Wawrowsky K., Cosgayon R., Farrokhi C., Lacayo L., Chesnokova V. Antidepressants stimulate hippocampal neurogenesis by inhibiting p21 expression in the subgranular zone of the hipppocampus. PLoS One 2012, 6:e27290.
105. Peng H., Huang Y., Rose J., Erichsen D., Herek S., Fujii N., Tamamura H., Zheng J. Stromal cell-derived factor 1-mediated CXCR4 signaling in rat and human cortical neural progenitor cells. J Neurosci Res 2004, 76:35-50.
106. Philips T., Robberecht W. Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease. Lancet Neurol 2011, 10:253-263.
107. Piatti V.C., Davies-Sala M.G., Esposito M.S., Mongiat L.A., Trinchero M.F., Schinder A.F. The timing for neuronal maturation in the adult hippocampus is modulated by local network activity. J Neurosci 2011, 31:7715-7728.
108. Pluchino S., Zanotti L., Rossi B., Brambilla E., Ottoboni L., Salani G., Martinello M., Cattalini A., Bergami A., Furlan R., Comi G., Constantin G., Martino G. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 2005, 436:266-271.
109. Ramos-Remus C., Duran-Barragan S. Neurological involvement in rheumatoid arthritis. Curr Immunol Rev 2010, 6:174-184.
110. Rivera F.J., Kraus J., Steffenhagen C., Kury P., Weidner N., Aigner L. Remyelination in multiple sclerosis: the therapeutic potential of neural and mesenchymal stem/progenitor cells. Curr Signal Transduct Ther 2011, 6:293-313.
111. Saino O., Taguchi A., Nakagomi T., Nakano-Doi A., Kashiwamura S., Doe N., Nakagomi N., Soma T., Yoshikawa H., Stern D.M., Okamura H., Matsuyama T. Immunodeficiency reduces neural stem/progenitor cell apoptosis and enhances neurogenesis in the cerebral cortex after stroke. J Neurosci Res 2010, 88:2385-2397.
112. Sanai N., Tramontin A.D., Quinones-Hinojosa A., Barbaro N.M., Gupta N., Kunwar S., Lawton M.T., McDermott M.W., Parsa A.T., Manuel-Garcia Verdugo J., Berger M.S., Alvarez-Buylla A. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004, 427:740-744.
113. Sawamoto K., Wichterle H., Gonzalez-Perez O., Cholfin J.A., Yamada M., Spassky N., Murcia N.S., Garcia-Verdugo J.M., Marin O., Rubenstein J.L., Tessier-Lavigne M., Okano H., Alvarez-Buylla A. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 2006, 311:629-632.
114. Schwamborn J., Lindecke A., Elvers M., Horejschi V., Kerick M., Rafigh M., Pfeiffer J., Prullage M., Kaltschmidt B., Kaltschmidt C. Microarray analysis of tumor necrosis factor alpha induced gene expression in U373 human glioblastoma cells. BMC Genomics 2003, 4:46.
115. Seri B., Garcia-Verdugo J.M., McEwen B.S., Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001, 21:7153-7160.
116. Seri B., Garcia-Verdugo J.M., Collado-Morente L., McEwen B.S., Alvarez-Buylla A. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 2004, 478:359-378.
117. Shen Q., Wang Y., Kokovay E., Lin G., Chuang S.M., Goderie S.K., Roysam B., Temple S. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008, 3:289-300.
118. Sicard R.E. Blood cells and their role in regeneration. I. Changes in circulating blood cell counts during forelimb regeneration. Exp Cell Biol 1983, 51:51-59.
119. Skihar V., Silva C., Chojnacki A., Doring A., Stallcup W.B., Weiss S., Yong V.W. Promoting oligodendrogenesis and myelin repair using the multiple sclerosis medication glatiramer acetate. Proc Natl Acad Sci U S A 2009, 106:17992-17997.
120. So K., Moriya T., Nishitani S., Takahashi H., Shinohara K. The olfactory conditioning in the early postnatal period stimulated neural stem/progenitor cells in the subventricular zone and increased neurogenesis in the olfactory bulb of rats. Neuroscience 2008, 151:120-128.
121. Song J.H., Wang C.X., Song D.K., Wang P., Shuaib A., Hao C. Interferon gamma induces neurite outgrowth by up-regulation of p35 neuron-specific cyclin-dependent kinase 5 activator via activation of ERK1/2 pathway. J Biol Chem 2005, 280:12896-12901.
122. Soulet D., Cicchetti F. The role of immunity in Huntington's disease. Mol Psychiatry 2011, 16:889-902.
123. Spooren A., Kolmus K., Laureys G., Clinckers R., De Keyser J., Haegeman G., Gerlo S. Interleukin-6, a mental cytokine. Brain Res Rev 2011, 67:157-183.
124. Tassava R.A., Olsen C.L. Higher vertebrates do not regenerate digits and legs because the wound epidermis is not functional. A hypothesis. Differentiation 1982, 22:151-155.
125. Tavazoie M., Van der Veken L., Silva-Vargas V., Louissaint M., Colonna L., Zaidi B., Garcia-Verdugo J.M., Doetsch F. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 2008, 3:279-288.
126. Temple S. The development of neural stem cells. Nature 2001, 414:112-117.
127. Tepavcevic V., Lazarini F., Alfaro-Cervello C., Kerninon C., Yoshikawa K., Garcia-Verdugo J.M., Lledo P.M., Nait-Oumesmar B., Baron-Van Evercooren A. Inflammation-induced subventricular zone dysfunction leads to olfactory deficits in a targeted mouse model of multiple sclerosis. J Clin Invest 2011, 121:4722-4734.
128. Tian L., Rauvala H. Immune functions of glia and neurons in the central nervous system. Curr Immunol Rev 2010, 6:160-166.
129. Tournefier A., Laurens V., Chapusot C., Ducoroy P., Padros M.R., Salvadori F., Sammut B. Structure of MHC class I and class II cDNAs and possible immunodeficiency linked to class II expression in the Mexican axolotl. Immunol Rev 1998, 166:259-277.
130. Tran P.B., Banisadr G., Ren D., Chenn A., Miller R.J. Chemokine receptor expression by neural progenitor cells in neurogenic regions of mouse brain. J Comp Neurol 2007, 500:1007-1033.
131. Turbic A., Leong S.Y., Turnley A.M. Chemokines and inflammatory mediators interact to regulate adult murine neural precursor cell proliferation, survival and differentiation. PLoS One 2011, 6:e25406.
132. Vezzani A., French J., Bartfai T., Baram T.Z. The role of inflammation in epilepsy. Nat Rev Neurol 2011, 7:31-40.
133. von Zahn J., Moller T., Kettenmann H., Nolte C. Microglial phagocytosis is modulated by pro- and anti-inflammatory cytokines. Neuroreport 1997, 8:3851-3856.
134. Wang H., Ikeda S., Kanno S., Guang L.M., Ohnishi M., Sasaki M., Kobayashi T., Tamura S. Activation of c-Jun amino-terminal kinase is required for retinoic acid-induced neural differentiation of P19 embryonal carcinoma cells. FEBS Lett 2001, 503:91-96.
135. Wen P.H., Shao X., Shao Z., Hof P.R., Wisniewski T., Kelley K., Friedrich V.L., Ho L., Pasinetti G.M., Shioi J., Robakis N.K., Elder G.A. Overexpression of wild type but not an FAD mutant presenilin-1 promotes neurogenesis in the hippocampus of adult mice. Neurobiol Dis 2002, 10:8-19.
136. Whitney N.P., Eidem T.M., Peng H., Huang Y., Zheng J.C. Inflammation mediates varying effects in neurogenesis: relevance to the pathogenesis of brain injury and neurodegenerative disorders. J Neurochem 2009, 108:1343-1359.
137. Widera D., Holtkamp W., Entschladen F., Niggemann B., Zanker K., Kaltschmidt B., Kaltschmidt C. MCP-1 induces migration of adult neural stem cells. Eur J Cell Biol 2004, 83:381-387.
138. 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.
139. Wong G., Goldshmit Y., Turnley A.M. Interferon-gamma but not TNF alpha promotes neuronal differentiation and neurite outgrowth of murine adult neural stem cells. Exp Neurol 2004, 187:171-177.
140. Wuwongse S., Chang R.C., Law A.C. The putative neurodegenerative links between depression and Alzheimer's disease. Prog Neurobiol 2010, 91:362-375.
141. Yamashita T., Ninomiya M., Hernandez Acosta P., Garcia-Verdugo J.M., Sunabori T., Sakaguchi M., Adachi K., Kojima T., Hirota Y., Kawase T., Araki N., Abe K., Okano H., Sawamoto K. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J Neurosci 2006, 26:6627-6636.
142. Yang J., Jiang Z., Fitzgerald D.C., Ma C., Yu S., Li H., Zhao Z., Li Y., Ciric B., Curtis M., Rostami A., Zhang G.X. Adult neural stem cells expressing IL-10 confer potent immunomodulation and remyelination in experimental autoimmune encephalitis. J Clin Invest 2009, 119:3678-3691.
143. Zentrich E., Han S.Y., Pessoa-Brandao L., Butterfield L., Heasley L.E. Collaboration of JNKs and ERKs in nerve growth factor regulation of the neurofilament light chain promoter in PC12 cells. J Biol Chem 2002, 277:4110-4118.
144. Zhao C., Deng W., Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 2008, 132:645-660.