Immune Influence on Adult Neural Stem Cell Regulation and Function

Neuron

Volumn 64, Issue 1, 2009, Pages 79-92

  Carpentier, Pamela A ^a   Palmer, Theo D ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ADULT STEM CELL; ALZHEIMER DISEASE; BRAIN CANCER; CELL FUNCTION; CEREBROVASCULAR ACCIDENT; DEPRESSION; EPILEPSY; GRAFT REJECTION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOREGULATION; INTRAUTERINE INFECTION; MENTAL STRESS; MICROGLIA; MULTIPLE SCLEROSIS; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INFLAMMATION; NEURAL STEM CELL; NEURAL STEM CELL TRANSPLANTATION; NEUROLOGIC DISEASE; NONHUMAN; OLIGODENDROGLIA; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN FUNCTION; RADIATION INJURY; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ADULT STEM CELLS; ANIMALS; BRAIN; HUMANS; NEUROIMMUNOMODULATION; NEURONS;

EID: 70349813944     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2009.08.038     Document Type: Review

References (149)

1. Aarum J., Sandberg K., Haeberlein S.L., and Persson M.A. Migration and differentiation of neural precursor cells can be directed by microglia. Proc. Natl. Acad. Sci. USA 100 (2003) 15983-15988
2. Agresti C., D'Urso D., and Levi G. Reversible inhibitory effects of interferon-gamma and tumour necrosis factor-alpha on oligodendroglial lineage cell proliferation and differentiation in vitro. Eur. J. Neurosci. 8 (1996) 1106-1116
3. Aharonowiz M., Einstein O., Fainstein N., Lassmann H., Reubinoff B., and Ben-Hur T. Neuroprotective effect of transplanted human embryonic stem cell-derived neural precursors in an animal model of multiple sclerosis. PLoS ONE 3 (2008) e3145
4. Andrews T., Zhang P., and Bhat N.R. TNFalpha potentiates IFNgamma-induced cell death in oligodendrocyte progenitors. J. Neurosci. Res. 54 (1998) 574-583
5. Arnett H.A., Mason J., Marino M., Suzuki K., Matsushima G.K., and Ting J.P. TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat. Neurosci. 4 (2001) 1116-1122
6. Arvidsson A., Collin T., Kirik D., Kokaia Z., and Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8 (2002) 963-970
7. Bailey S.L., Carpentier P.A., McMahon E.J., Begolka W.S., and Miller S.D. Innate and adaptive immune responses of the central nervous system. Crit. Rev. Immunol. 26 (2006) 149-188
8. Baker S.A., Baker K.A., and Hagg T. Dopaminergic nigrostriatal projections regulate neural precursor proliferation in the adult mouse subventricular zone. Eur. J. Neurosci. 20 (2004) 575-579
9. Bastos G.N., Moriya T., Inui F., Katura T., and Nakahata N. Involvement of cyclooxygenase-2 in lipopolysaccharide-induced impairment of the newborn cell survival in the adult mouse dentate gyrus. Neuroscience 155 (2008) 454-462
10. Ben-Hur T., Ben-Menachem O., Furer V., Einstein O., Mizrachi-Kol R., and Grigoriadis N. Effects of proinflammatory cytokines on the growth, fate, and motility of multipotential neural precursor cells. Mol. Cell. Neurosci. 24 (2003) 623-631
11. Bernardino L., Agasse F., Silva B., Ferreira R., Grade S., and Malva J.O. Tumor necrosis factor-alpha modulates survival, proliferation, and neuronal differentiation in neonatal subventricular zone cell cultures. Stem Cells 26 (2008) 2361-2371
12. Beversdorf D.Q., Manning S.E., Hillier A., Anderson S.L., Nordgren R.E., Walters S.E., Nagaraja H.N., Cooley W.C., Gaelic S.E., and Bauman M.L. Timing of prenatal stressors and autism. J. Autism Dev. Disord. 35 (2005) 471-478
13. Bhat R., and Steinman L. Innate and adaptive autoimmunity directed to the central nervous system. Neuron 64 (2009) 123-132 this issue
14. Blumcke I., Schewe J.C., Normann S., Brustle O., Schramm J., Elger C.E., and Wiestler O.D. Increase of nestin-immunoreactive neural precursor cells in the dentate gyrus of pediatric patients with early-onset temporal lobe epilepsy. Hippocampus 11 (2001) 311-321
15. Bonde S., Ekdahl C.T., and Lindvall O. Long-term neuronal replacement in adult rat hippocampus after status epilepticus despite chronic inflammation. Eur. J. Neurosci. 23 (2006) 965-974
16. Borges K., Gearing M., McDermott D.L., Smith A.B., Almonte A.G., Wainer B.H., and Dingledine R. Neuronal and glial pathological changes during epileptogenesis in the mouse pilocarpine model. Exp. Neurol. 182 (2003) 21-34
17. Borta A., and Hoglinger G.U. Dopamine and adult neurogenesis. J. Neurochem. 100 (2007) 587-595
18. Boulanger L.M. Immune proteins in brain development and synaptic plasticity. Neuron 64 (2009) 93-109 this issue
19. Brown A.S., Schaefer C.A., Wyatt R.J., Goetz R., Begg M.D., Gorman J.M., and Susser E.S. Maternal exposure to respiratory infections and adult schizophrenia spectrum disorders: a prospective birth cohort study. Schizophr. Bull. 26 (2000) 287-295
20. Bruck A., Kurki T., Kaasinen V., Vahlberg T., and Rinne J.O. Hippocampal and prefrontal atrophy in patients with early non-demented Parkinson's disease is related to cognitive impairment. J. Neurol. Neurosurg. Psychiatry 75 (2004) 1467-1469
21. Bsibsi M., Ravid R., Gveric D., and van Noort J.M. Broad expression of Toll-like receptors in the human central nervous system. J. Neuropathol. Exp. Neurol. 61 (2002) 1013-1021
22. Buckwalter M.S., Yamane M., Coleman B.S., Ormerod B.K., Chin J.T., Palmer T., and Wyss-Coray T. Chronically increased transforming growth factor-beta1 strongly inhibits hippocampal neurogenesis in aged mice. Am. J. Pathol. 169 (2006) 154-164
23. Butovsky O., Ziv Y., Schwartz A., Landa G., Talpalar A.E., Pluchino S., Martino G., and Schwartz M. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol. Cell. Neurosci. 31 (2006) 149-160
24. Cacci E., Claasen J.H., and Kokaia Z. Microglia-derived tumor necrosis factor-alpha exaggerates death of newborn hippocampal progenitor cells in vitro. J. Neurosci. Res. 80 (2005) 789-797
25. Cai Z., Pan Z.L., Pang Y., Evans O.B., and Rhodes P.G. Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration. Pediatr. Res. 47 (2000) 64-72
26. Cameron H.A., and Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61 (1994) 203-209
27. Carmichael S.T. Themes and strategies for studying the biology of stroke recovery in the poststroke epoch. Stroke 39 (2008) 1380-1388
28. Chen Z., and Palmer T.D. Cellular repair of CNS disorders: an immunological perspective. Hum. Mol. Genet. 17 (2008) R84-R92
29. Chu K., Kim M., Chae S.H., Jeong S.W., Kang K.S., Jung K.H., Kim J., Kim Y.J., Kang L., Kim S.U., and Yoon B.W. Distribution and in situ proliferation patterns of intravenously injected immortalized human neural stem-like cells in rats with focal cerebral ischemia. Neurosci. Res. 50 (2004) 459-465
30. Corriveau R.A., Huh G.S., and Shatz C.J. Regulation of class I MHC gene expression in the developing and mature CNS by neural activity. Neuron 21 (1998) 505-520
31. Covacu R., Arvidsson L., Andersson A., Khademi M., Erlandsson-Harris H., Harris R.A., Svensson M.A., Olsson T., and Brundin L. TLR activation induces TNF-alpha production from adult neural stem/progenitor cells. J. Immunol. 182 (2009) 6889-6895
32. Dayer A.G., Cleaver K.M., Abouantoun T., and Cameron H.A. New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J. Cell Biol. 168 (2005) 415-427
33. Deisseroth K., Singla S., Toda H., Monje M., Palmer T.D., and Malenka R.C. Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42 (2004) 535-552
34. Deverman B.E., and Patterson P.H. Cytokines and CNS development. Neuron 64 (2009) 61-78 this issue
35. Dimos J.T., Rodolfa K.T., Niakan K.K., Weisenthal L.M., Mitsumoto H., Chung W., Croft G.F., Saphier G., Leibel R., Goland R., et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 321 (2008) 1218-1221
36. Duan X., Kang E., Liu C.Y., Ming G.L., and Song H. Development of neural stem cell in the adult brain. Curr. Opin. Neurobiol. 18 (2008) 108-115
37. Ebert A.D., Yu J., Rose Jr. F.F., Mattis V.B., Lorson C.L., Thomson J.A., and Svendsen C.N. Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 457 (2009) 277-280
38. Einstein O., Fainstein N., Vaknin I., Mizrachi-Kol R., Reihartz E., Grigoriadis N., Lavon I., Baniyash M., Lassmann H., and Ben-Hur T. Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression. Ann. Neurol. 61 (2007) 209-218
39. Ekdahl C.T., Claasen J.H., Bonde S., Kokaia Z., and Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. USA 100 (2003) 13632-13637
40. Elenkov I.J., and Chrousos G.P. Stress hormones, proinflammatory and antiinflammatory cytokines, and autoimmunity. Ann. N Y Acad. Sci. 966 (2002) 290-303
41. Ellman L., and Susser E. The promise of epidemiologic studies: neuroimmune mechanisms in the etiologies of brain disorders. Neuron 64 (2009) 25-27 this issue
42. Emsley J.G., Mitchell B.D., Kempermann G., and Macklis J.D. Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog. Neurobiol. 75 (2005) 321-341
43. Foote A.K., and Blakemore W.F. Inflammation stimulates remyelination in areas of chronic demyelination. Brain 128 (2005) 528-539
44. Franklin R.J., and Ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat. Rev. Neurosci. 9 (2008) 839-855
45. Fujiwara Y., Tanaka N., Ishida O., Fujimoto Y., Murakami T., Kajihara H., Yasunaga Y., and Ochi M. Intravenously injected neural progenitor cells of transgenic rats can migrate to the injured spinal cord and differentiate into neurons, astrocytes and oligodendrocytes. Neurosci. Lett. 366 (2004) 287-291
46. Gabryelewicz T., Styczynska M., Luczywek E., Barczak A., Pfeffer A., Androsiuk W., Chodakowska-Zebrowska M., Wasiak B., Peplonska B., and Barcikowska M. The rate of conversion of mild cognitive impairment to dementia: predictive role of depression. Int. J. Geriatr. Psychiatry 22 (2007) 563-567
47. Glezer I., Lapointe A., and Rivest S. Innate immunity triggers oligodendrocyte progenitor reactivity and confines damages to brain injuries. FASEB J. 20 (2006) 750-752
48. Goshen I., Kreisel T., Ounallah-Saad H., Renbaum P., Zalzstein Y., Ben-Hur T., Levy-Lahad E., and Yirmiya R. A dual role for interleukin-1 in hippocampal-dependent memory processes. Psychoneuroendocrinology 32 (2007) 1106-1115
49. Goshen I., Kreisel T., Ben-Menachem-Zidon O., Licht T., Weidenfeld J., Ben-Hur T., and Yirmiya R. Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol. Psychiatry 13 (2008) 717-728
50. Hanna J., Wernig M., Markoulaki S., Sun C.W., Meissner A., Cassady J.P., Beard C., Brambrink T., Wu L.C., Townes T.M., and Jaenisch R. Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science 318 (2007) 1920-1923
51. Hattiangady B., and Shetty A.K. Implications of decreased hippocampal neurogenesis in chronic temporal lobe epilepsy. Epilepsia 49 Suppl 5 (2008) 26-41
52. Hattiangady B., Rao M.S., and Shetty A.K. Chronic temporal lobe epilepsy is associated with severely declined dentate neurogenesis in the adult hippocampus. Neurobiol. Dis. 17 (2004) 473-490
53. Hawkes C. Olfaction in neurodegenerative disorder. Adv. Otorhinolaryngol. 63 (2006) 133-151
54. Heldmann U., Thored P., Claasen J.H., Arvidsson A., Kokaia Z., and Lindvall O. TNF-alpha antibody infusion impairs survival of stroke-generated neuroblasts in adult rat brain. Exp. Neurol. 196 (2005) 204-208
55. Hoehn B.D., Palmer T.D., and Steinberg G.K. Neurogenesis in rats after focal cerebral ischemia is enhanced by indomethacin. Stroke 36 (2005) 2718-2724
56. Hoglinger G.U., Rizk P., Muriel M.P., Duyckaerts C., Oertel W.H., Caille I., and Hirsch E.C. Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat. Neurosci. 7 (2004) 726-735
57. Hori J., Ng T.F., Shatos M., Klassen H., Streilein J.W., and Young M.J. Neural progenitor cells lack immunogenicity and resist destruction as allografts. Stem Cells 21 (2003) 405-416
58. Hou S.W., Wang Y.Q., Xu M., Shen D.H., Wang J.J., Huang F., Yu Z., and Sun F.Y. Functional integration of newly generated neurons into striatum after cerebral ischemia in the adult rat brain. Stroke 39 (2008) 2837-2844
59. Huh G.S., Boulanger L.M., Du H., Riquelme P.A., Brotz T.M., and Shatz C.J. Functional requirement for class I MHC in CNS development and plasticity. Science 290 (2000) 2155-2159
60. Ideguchi M., Shinoyama M., Gomi M., Hayashi H., Hashimoto N., and Takahashi J. Immune or inflammatory response by the host brain suppresses neuronal differentiation of transplanted ES cell-derived neural precursor cells. J. Neurosci. Res. 86 (2008) 1936-1943
61. Imitola J., Raddassi K., Park K.I., Mueller F.J., Nieto M., Teng Y.D., Frenkel D., Li J., Sidman R.L., Walsh C.A., et al. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc. Natl. Acad. Sci. USA 101 (2004) 18117-18122
62. Iosif R.E., Ekdahl C.T., Ahlenius H., Pronk C.J., Bonde S., Kokaia Z., Jacobsen S.E., and Lindvall O. Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J. Neurosci. 26 (2006) 9703-9712
63. Iosif R.E., Ahlenius H., Ekdahl C.T., Darsalia V., Thored P., Jovinge S., Kokaia Z., and Lindvall O. Suppression of stroke-induced progenitor proliferation in adult subventricular zone by tumor necrosis factor receptor 1. J. Cereb. Blood Flow Metab. 28 (2008) 1574-1587
64. Jakubs K., Bonde S., Iosif R.E., Ekdahl C.T., Kokaia Z., Kokaia M., and Lindvall O. Inflammation regulates functional integration of neurons born in adult brain. J. Neurosci. 28 (2008) 12477-12488
65. Jin K., Wang X., Xie L., Mao X.O., Zhu W., Wang Y., Shen J., Mao Y., Banwait S., and Greenberg D.A. Evidence for stroke-induced neurogenesis in the human brain. Proc. Natl. Acad. Sci. USA 103 (2006) 13198-13202
66. Johansson S., Price J., and Modo M. Effect of inflammatory cytokines on major histocompatibility complex expression and differentiation of human neural stem/progenitor cells. Stem Cells 26 (2008) 2444-2454
67. Jung K.H., Chu K., Lee S.T., Kim J., Sinn D.I., Kim J.M., Park D.K., Lee J.J., Kim S.U., Kim M., et al. Cyclooxygenase-2 inhibitor, celecoxib, inhibits the altered hippocampal neurogenesis with attenuation of spontaneous recurrent seizures following pilocarpine-induced status epilepticus. Neurobiol. Dis. 23 (2006) 237-246
68. Kauppinen T.M., Suh S.W., Berman A.E., Hamby A.M., and Swanson R.A. Inhibition of poly(ADP-ribose) polymerase suppresses inflammation and promotes recovery after ischemic injury. J. Cereb. Blood Flow Metab. 29 (2009) 820-829
69. Keene C.D., Chang R., Stephen C., Nivison M., Nutt S.E., Look A., Breyer R.M., Horner P.J., Hevner R., and Montine T.J. Protection of hippocampal neurogenesis from toll-like receptor 4-dependent innate immune activation by ablation of prostaglandin E2 receptor subtype EP1 or EP2. Am. J. Pathol. 174 (2009) 2300-2309
70. Kim H.S., and Suh Y.H. Minocycline and neurodegenerative diseases. Behav. Brain Res. 196 (2009) 168-179
71. Kim B.J., Kim M.J., Park J.M., Lee S.H., Kim Y.J., Ryu S., Kim Y.H., and Yoon B.W. Reduced neurogenesis after suppressed inflammation by minocycline in transient cerebral ischemia in rat. J. Neurol. Sci. 279 (2009) 70-75
72. Klein M.A., Moller J.C., Jones L.L., Bluethmann H., Kreutzberg G.W., and Raivich G. Impaired neuroglial activation in interleukin-6 deficient mice. Glia 19 (1997) 227-233
73. Koo J.W., and Duman R.S. IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc. Natl. Acad. Sci. USA 105 (2008) 751-756
74. Kordower J.H., Styren S., Clarke M., DeKosky S.T., Olanow C.W., and Freeman T.B. Fetal grafting for Parkinson's disease: expression of immune markers in two patients with functional fetal nigral implants. Cell Transplant. 6 (1997) 213-219
75. Kuhlmann T., Miron V., Cuo Q., Wegner C., Antel J., and Bruck W. Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 131 (2008) 1749-1758
76. Kuhn H.G., Cooper-Kuhn C.M., Boekhoorn K., and Lucassen P.J. Changes in neurogenesis in dementia and Alzheimer mouse models: are they functionally relevant?. Eur. Arch. Psychiatry Clin. Neurosci. 257 (2007) 281-289
77. Lee S.T., Chu K., Park J.E., Lee K., Kang L., Kim S.U., and Kim M. Intravenous administration of human neural stem cells induces functional recovery in Huntington's disease rat model. Neurosci. Res. 52 (2005) 243-249
78. Lee S.T., Chu K., Jung K.H., Kim S.J., Kim D.H., Kang K.M., Hong N.H., Kim J.H., Ban J.J., Park H.K., et al. Anti-inflammatory mechanism of intravascular neural stem cell transplantation in haemorrhagic stroke. Brain 131 (2008) 616-629
79. Liu Y.P., Lin H.I., and Tzeng S.F. Tumor necrosis factor-alpha and interleukin-18 modulate neuronal cell fate in embryonic neural progenitor culture. Brain Res. 1054 (2005) 152-158
80. Liu Z., Fan Y., Won S.J., Neumann M., Hu D., Zhou L., Weinstein P.R., and Liu J. Chronic treatment with minocycline preserves adult new neurons and reduces functional impairment after focal cerebral ischemia. Stroke 38 (2007) 146-152
81. Lucin K.M., and Wyss-Coray T. Immune pathways in brain aging and neurodegeneration: too much or too little?. Neuron 64 (2009) 110-122 this issue
82. Ma Q., Jones D., Borghesani P.R., Segal R.A., Nagasawa T., Kishimoto T., Bronson R.T., and Springer T.A. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in C. Proc. Natl. Acad. Sci. USA 95 (1998) 9448-9453
83. Ma D.K., Jang M.H., Guo J.U., Kitabatake Y., Chang M.L., Pow-Anpongkul N., Flavell R.A., Lu B., Ming G.L., and Song H. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323 (2009) 1074-1077
84. Magavi S.S., Leavitt B.R., and Macklis J.D. Induction of neurogenesis in the neocortex of adult mice. Nature 405 (2000) 951-955
85. Magavi S.S., Mitchell B.D., Szentirmai O., Carter B.S., and Macklis J.D. Adult-born and preexisting olfactory granule neurons undergo distinct experience-dependent modifications of their olfactory responses in vivo. J. Neurosci. 25 (2005) 10729-10739
86. Malberg J.E., Eisch A.J., Nestler E.J., and Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20 (2000) 9104-9110
87. Mammolenti M., Gajavelli S., Tsoulfas P., and Levy R. Absence of major histocompatibility complex class I on neural stem cells does not permit natural killer cell killing and prevents recognition by alloreactive cytotoxic T lymphocytes in vitro. Stem Cells 22 (2004) 1101-1110
88. Matsuda H. The role of neuroimaging in mild cognitive impairment. Neuropathology 27 (2007) 570-577
89. McAfoose J., and Baune B.T. Evidence for a cytokine model of cognitive function. Neurosci. Biobehav. Rev. 33 (2009) 355-366
90. McCoy M.K., and Tansey M.G. TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. J. Neuroinflammation 5 (2008) 45
91. Merkle F.T., and Alvarez-Buylla A. Neural stem cells in mammalian development. Curr. Opin. Cell Biol. 18 (2006) 704-709
92. Meyer U., Nyffeler M., Engler A., Urwyler A., Schedlowski M., Knuesel I., Yee B.K., and Feldon J. The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J. Neurosci. 26 (2006) 4752-4762
93. Meyer U., Yee B.K., and Feldon J. The neurodevelopmental impact of prenatal infections at different times of pregnancy: the earlier the worse?. Neuroscientist 13 (2007) 241-256
94. Ming G.L., and Song H. Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 28 (2005) 223-250
95. Mirza B., Krook H., Andersson P., Larsson L.C., Korsgren O., and Widner H. Intracerebral cytokine profiles in adult rats grafted with neural tissue of different immunological disparity. Brain Res. Bull. 63 (2004) 105-118
96. Monje M.L., and Palmer T. Radiation injury and neurogenesis. Curr. Opin. Neurol. 16 (2003) 129-134
97. Monje M.L., Mizumatsu S., Fike J.R., and Palmer T.D. Irradiation induces neural precursor-cell dysfunction. Nat. Med. 8 (2002) 955-962
98. Monje M.L., Toda H., and Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302 (2003) 1760-1765
99. Muraoka K., Shingo T., Yasuhara T., Kameda M., Yuan W., Hayase H., Matsui T., Miyoshi Y., and Date I. The high integration and differentiation potential of autologous neural stem cell transplantation compared with allogeneic transplantation in adult rat hippocampus. Exp. Neurol. 199 (2006) 311-327
100. Nakanishi M., Niidome T., Matsuda S., Akaike A., Kihara T., and Sugimoto H. Microglia-derived interleukin-6 and leukaemia inhibitory factor promote astrocytic differentiation of neural stem/progenitor cells. Eur. J. Neurosci. 25 (2007) 649-658
101. Niederkorn J.Y. See no evil, hear no evil, do no evil: the lessons of immune privilege. Nat. Immunol. 7 (2006) 354-359
102. Ormerod B.K., Palmer T.D., and Caldwell M.A. Neurodegeneration and cell replacement. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363 (2008) 153-170
103. Palmer T.D., Markakis E.A., Willhoite A.R., Safar F., and Gage F.H. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J. Neurosci. 19 (1999) 8487-8497
104. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., and Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 17 (1997) 3727-3738
105. Parent J.M., Vexler Z.S., Gong C., Derugin N., and Ferriero D.M. Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann. Neurol. 52 (2002) 802-813
106. Pluchino S., Quattrini A., Brambilla E., Gritti A., Salani G., Dina G., Galli R., Del C.U., Amadio S., Bergami A., et al. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422 (2003) 688-694
107. Pluchino S., Zanotti L., Rossi B., Brambilla E., Ottoboni L., Salani G., Martinello M., Cattalini A., Bergami A., Furlan R., et al. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 436 (2005) 266-271
108. Poewe W. Non-motor symptoms in Parkinson's disease. Eur. J. Neurol. 15 Suppl 1 (2008) 14-20
109. Preynat-Seauve O., de Rham C., Tirefort D., Ferrari-Lacraz S., Krause K.H., and Villard J. Neural progenitors derived from human embryonic stem cells are targeted by allogeneic T and natural killer cells. J. Cell Mol. Med. (2009) 10.1111/j.1582-4934.2009.00746.x in press. Published online March 13, 2009
110. Rolls A., Shechter R., London A., Ziv Y., Ronen A., Levy R., and Schwartz M. Toll-like receptors modulate adult hippocampal neurogenesis. Nat. Cell Biol. 9 (2007) 1081-1088
111. Rolls A., Shechter R., and Schwartz M. The bright side of the glial scar in CNS repair. Nat. Rev. Neurosci. 10 (2009) 235-241
112. Sahay A., and Hen R. Adult hippocampal neurogenesis in depression. Nat. Neurosci. 10 (2007) 1110-1115
113. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., Weisstaub N., Lee J., Duman R., Arancio O., et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301 (2003) 805-809
114. Schmidt H.D., and Duman R.S. The role of neurotrophic factors in adult hippocampal neurogenesis, antidepressant treatments and animal models of depressive-like behavior. Behav. Pharmacol. 18 (2007) 391-418
115. Schwartz M. Beneficial autoimmune T cells and posttraumatic neuroprotection. Ann. N Y Acad. Sci. 917 (2000) 341-347
116. Segi-Nishida E., Warner-Schmidt J.L., and Duman R.S. Electroconvulsive seizure and VEGF increase the proliferation of neural stem-like cells in rat hippocampus. Proc. Natl. Acad. Sci. USA 105 (2008) 11352-11357
117. Setzu A., Lathia J.D., Zhao C., Wells K., Rao M.S., Ffrench-Constant C., and Franklin R.J. Inflammation stimulates myelination by transplanted oligodendrocyte precursor cells. Glia 54 (2006) 297-303
118. Sheng W.S., Hu S., Ni H.T., Rowen T.N., Lokensgard J.R., and Peterson P.K. TNF-alpha-induced chemokine production and apoptosis in human neural precursor cells. J. Leukoc. Biol. 78 (2005) 1233-1241
119. Shi L., Fatemi S.H., Sidwell R.W., and Patterson P.H. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J. Neurosci. 23 (2003) 297-302
120. Shi L., Smith S.E., Malkova N., Tse D., Su Y., and Patterson P.H. Activation of the maternal immune system alters cerebellar development in the offspring. Brain Behav. Immun. 23 (2009) 116-123
121. Shimazaki T., Shingo T., and Weiss S. The ciliary neurotrophic factor/leukemia inhibitory factor/gp130 receptor complex operates in the maintenance of mammalian forebrain neural stem cells. J. Neurosci. 21 (2001) 7642-7653
122. Smith S.E., Li J., Garbett K., Mirnics K., and Patterson P.H. Maternal immune activation alters fetal brain development through interleukin-6. J. Neurosci. 27 (2007) 10695-10702
123. So K., Moriya T., Nishitani S., Takahashi H., and 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 151 (2008) 120-128
124. Soldner F., Hockemeyer D., Beard C., Gao Q., Bell G.W., Cook E.G., Hargus G., Blak A., Cooper O., Mitalipova M., et al. Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 136 (2009) 964-977
125. Spulber S., Oprica M., Bartfai T., Winblad B., and Schultzberg M. Blunted neurogenesis and gliosis due to transgenic overexpression of human soluble IL-1ra in the mouse. Eur. J. Neurosci. 27 (2008) 549-558
126. Stevens B., Allen N.J., Vazquez L.E., Howell G.R., Christopherson K.S., Nouri N., Micheva K.D., Mehalow A.K., Huberman A.D., Stafford B., et al. The classical complement cascade mediates CNS synapse elimination. Cell 131 (2007) 1164-1178
127. Taga T., and Fukuda S. Role of IL-6 in the neural stem cell differentiation. Clin. Rev. Allergy Immunol. 28 (2005) 249-256
128. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., and Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131 (2007) 861-872
129. Tamura Y., Kataoka Y., Cui Y., Takamori Y., Watanabe Y., and Yamada H. Multi-directional differentiation of doublecortin- and NG2-immunopositive progenitor cells in the adult rat neocortex in vivo. Eur. J. Neurosci. 25 (2007) 3489-3498
130. Tanapat P., Galea L.A., and Gould E. Stress inhibits the proliferation of granule cell precursors in the developing dentate gyrus. Int. J. Dev. Neurosci. 16 (1998) 235-239
131. Tang Y., Shah K., Messerli S.M., Snyder E., Breakefield X., and Weissleder R. In vivo tracking of neural progenitor cell migration to glioblastomas. Hum. Gene Ther. 14 (2003) 1247-1254
132. Theele D.P., Schrimsher G.W., and Reier P.J. Comparison of the growth and fate of fetal spinal iso- and allografts in the adult rat injured spinal cord. Exp. Neurol. 142 (1996) 128-143
133. Tran P.B., Banisadr G., Ren D., Chenn A., and Miller R.J. Chemokine receptor expression by neural progenitor cells in neurogenic regions of mouse brain. J. Comp. Neurol. 500 (2007) 1007-1033
134. Uematsu S., and Akira S. Toll-like receptors and innate immunity. J. Mol. Med. 84 (2006) 712-725
135. Vallieres L., Campbell I.L., Gage F.H., and Sawchenko P.E. Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J. Neurosci. 22 (2002) 486-492
136. Vela J.M., Molina-Holgado E., Arevalo-Martin A., Almazan G., and Guaza C. Interleukin-1 regulates proliferation and differentiation of oligodendrocyte progenitor cells. Mol. Cell. Neurosci. 20 (2002) 489-502
137. Wang H., Yu M., Ochani M., Amella C.A., Tanovic M., Susarla S., Li J.H., Wang H., Yang H., Ulloa L., et al. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421 (2003) 384-388
138. Wang L., Shi J., van Ginkel F.W., Lan L., Niemeyer G., Martin D.R., Snyder E.Y., and Cox N.R. Neural stem/progenitor cells modulate immune responses by suppressing T lymphocytes with nitric oxide and prostaglandin E2. Exp. Neurol. 216 (2009) 177-183
139. Ware C.B., Horowitz M.C., Renshaw B.R., Hunt J.S., Liggitt D., Koblar S.A., Gliniak B.C., McKenna H.J., Papayannopoulou T., and Thoma B. Targeted disruption of the low-affinity leukemia inhibitory factor receptor gene causes placental, skeletal, neural and metabolic defects and results in perinatal death. Development 121 (1995) 1283-1299
140. Wernig M., Zhao J.P., Pruszak J., Hedlund E., Fu D., Soldner F., Broccoli V., Constantine-Paton M., Isacson O., and Jaenisch R. Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease. Proc. Natl. Acad. Sci. USA 105 (2008) 5856-5861
141. Widera D., Mikenberg I., Elvers M., Kaltschmidt C., and Kaltschmidt B. Tumor necrosis factor alpha triggers proliferation of adult neural stem cells via IKK/NF-kappaB signaling. BMC Neurosci. 7 (2006) 64
142. Winner B., Lie D.C., Rockenstein E., Aigner R., Aigner L., Masliah E., Kuhn H.G., and Winkler J. Human wild-type alpha-synuclein impairs neurogenesis. J. Neuropathol. Exp. Neurol. 63 (2004) 1155-1166
143. Wolswijk G. Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. J. Neurosci. 18 (1998) 601-609
144. Wu J.P., Kuo J.S., Liu Y.L., and Tzeng S.F. Tumor necrosis factor-alpha modulates the proliferation of neural progenitors in the subventricular/ventricular zone of adult rat brain. Neurosci. Lett. 292 (2000) 203-206
145. Yan Y.P., Sailor K.A., Lang B.T., Park S.W., Vemuganti R., and Dempsey R.J. Monocyte chemoattractant protein-1 plays a critical role in neuroblast migration after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 27 (2007) 1213-1224
146. Zhang R.L., Zhang Z.G., Zhang L., and Chopp M. Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia. Neuroscience 105 (2001) 33-41
147. Zhang R., Zhang Z., Zhang C., Zhang L., Robin A., Wang Y., Lu M., and Chopp M. Stroke transiently increases subventricular zone cell division from asymmetric to symmetric and increases neuronal differentiation in the adult rat. J. Neurosci. 24 (2004) 5810-5815
148. Zou Y.R., Kottmann A.H., Kuroda M., Taniuchi I., and Littman D.R. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393 (1998) 595-599
149. Zuckerman L., Rehavi M., Nachman R., and Weiner I. Immune activation during pregnancy in rats leads to a postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limbic morphology in the offspring: a novel neurodevelopmental model of schizophrenia. Neuropsychopharmacology 28 (2003) 1778-1789