Neuroinflammation and cell therapy for Parkinson's disease

Frontiers in Bioscience - Scholar

Volumn 3 S, Issue 4, 2011, Pages 1407-1420

  Zhu, Shugan ^a   Li, Feng ^a   Zhu, Shaowei ^a   Wu, Chengyuan ^a   Yan, Chuanzhu ^a   Liu, Yuguang ^a  

^a SHANDONG UNIVERSITY   (China)

Author keywords

Anti inflammatory; Cell therapy; Microglia; Neuroinflammation; Parkinson's disease; Review; Stem cells

Indexed keywords

ALPHA SYNUCLEIN; BONE MORPHOGENETIC PROTEIN 4; CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR5; GELATINASE A; HLA ANTIGEN; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 6; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 3; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SONIC HEDGEHOG PROTEIN; STROMAL CELL DERIVED FACTOR 1; TENASCIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ASTROCYTE; BASAL GANGLION; BLOOD BRAIN BARRIER; CELL ADHESION; CELL CONTACT; CELL DEATH; CELL DIFFERENTIATION; CELL DIVISION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELL THERAPY; CINGULATE GYRUS; CYTOKINE PRODUCTION; CYTOTOXICITY; DEGENERATIVE DISEASE; DOPAMINERGIC NERVE CELL; GENETIC ASSOCIATION; GLIOSIS; HIPPOCAMPUS; HUMAN; HUMORAL IMMUNITY; IMMUNOMODULATION; INTERNALIZATION; MACROPHAGE ACTIVATION; MICROGLIA; MYELOID DENDRITIC CELL; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PHAGOCYTE; PHAGOCYTOSIS; PROTEIN EXPRESSION; REMYELINIZATION; REVIEW; STEM CELL; STEM CELL TRANSPLANTATION; SUBSTANTIA NIGRA; SUBSTANTIA NIGRA PARS COMPACTA; TELENCEPHALON; CELL MOTION; CYTOLOGY; GRAFT REJECTION; IMMUNOLOGY; INFLAMMATION; METHODOLOGY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; XENOGRAFT;

CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; GRAFT REJECTION; HUMANS; IMMUNOMODULATION; INFLAMMATION; MICROGLIA; PARKINSON DISEASE; STEM CELL TRANSPLANTATION; STEM CELLS; TRANSPLANTATION, HETEROLOGOUS;

EID: 80053128823     PISSN: 19450516     EISSN: 19450524     Source Type: Journal    
DOI: 10.2741/s232     Document Type: Review

References (156)

1. Bennett D.A., Beckett L.A., Murray A.M., Shannon K.M., Goetz C.G., Pilgrim D.M., and Evans D.A.: Prevalence of parkinsonian signs and associated mortality in a community population of older people. N Engl J Med 334, 71-76 (1996)
2. Lang A.E., and Lozano A.M.: Parkinson' s disease. First of two parts. N Engl J Med 339, 1044-1053 (1998)
3. Deumens R., Blokland A., and Prickaerts J.: Modelling Parkinson's disease in rats: an evualtion of 6-OHDA lesions of the nigrastraital pathway. Exp Neurol 175, 303-317 (2002)
4. Björklund A., and Lindvall O.: Cell replacement therapies for central nervous system disorders. Nat Neurosci 3, 537-44 (2000)
5. Palmer M.R., Granholm A.C., van Horne C.G., Giardina K.E., Freund R.K., Moorhead J.W., and Gerhardt GA.: Intranigral transplantation of solid tissue ventral mesencephalon or striatal grafts induces behavioral recovery in 6-OHDA-lesioned rats. Brain Res 890,86-99 (2001)
6. Bjugstad K.B., Teng Y.D., Redmond D.E. Jr., Elsworth J.D., Roth R.H., Cornelius S.K., Snyder E.Y., and Sladek J.R. Jr.: Human neural stem cells migrate along the nigrostriatal pathway in a primate model of Parkinson's disease. Exp Neurol 211,362-9 (2008)
7. Zou Z., Jiang X., Zhang W., Zhou Y., Ke Y., Zhang S., and Xu R.: Efficacy of Tyrosine Hydroxylase gene modified neural stem cells derived from bone marrow on Parkinson's disease-a rat model study. Brain Res 30, 279-86 (2010)
8. Yang J.R., Liao C.H., Pang C.Y., Huang L.L., Lin Y.T., Chen Y.L., Shiue Y.L., and Chen L.R.: Directed differentiation into neural lineages and therapeutic potential of porcine embryonic stem cells in rat Parkinson's disease model. Cell Reprogram 12,447-61 (2010)
9. Toriumi H., Yoshikawa M., Matsuda R., Nishimura F., Yamada S., Hirabayashi H., Nakase H., Nonaka J., Ouji Y., Ishizaka S., and Sakaki T.: Treatment of Parkinson's disease model mice with allogeneic embryonic stem cells: necessity of immunosuppressive treatment for sustained improvement. Neurol Res 31,220-7 (2009)
10. Redmond D.E. Jr., Vinuela A., Kordower J.H., and Isacson O.: Influence of cell preparation and target location on the behavioral recovery after striatal transplantation of fetal dopaminergic neurons in a primate model of Parkinson's disease. Neurobiol Dis 29,103-16 (2008)
11. Yasuhara T., Matsukawa N., Hara K., Yu G., Xu L., Maki M., Kim S.U., and Borlongan C.V.: Transplantation of human neural stem cells exerts neuroprotection in a rat model of Parkinson's disease. J Neurosci 26, 12497-511 (2006)
12. Olanow C.W., Kordower J.H., and Freeman T.B.: Fetal nigral transplantation as a therapy for Parkinson's disease. Trends Neurosci 19, 102-109 (1996)
13. Lindvall O.: Cerebral implantation in movement disorders: State of the art. Mov Disord 14, 201-205 (1999)
14. Kordower J.H., Freeman T.B., Snow B.J., Vingerhoets F.J., Mufson E.J., Sanberg P.R., Hauser R.A., Smith D.A., Nauert G.M., and Perl D.P.: Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson' s disease. N Engl J Med 332, 1118-1124 (1995)
15. Kordower J. H., Freeman T.B., Chen E.Y., Mufson E.J., Sanberg P.R., Hauser R.A., Snow B., and Olanow C.W.: Fetal nigral grafts survive and mediate clinical benefit in a patient with Parkinson' s disease. Mov Disord 13, 383-393 (2004)
16. Zawada W.M., Zastrow D.J., Clarkson E.D., Adams F.S., Bell K.P., and Freed C.R.:Growth factors improve immediate survival of embryonic dopamine neurons after transplantation into rats. Brain Res 786,96-103 (1998)
17. Nakao N., Frodl E.M., Duan W.M., Widner H., and Brundin P.: Lazaroids improve the survival of grafted rat embryonic dopamine neurons. Proc Natl Acad Sci U S A 91,12408-12 (1994)
18. Li J.Y., Englund E., Holton J.L., Soulet D., Hagell P., Lees A.J., Lashley T., Quinn N.P., Rehncrona S., Björklund A., Widner H., Revesz T., Lindvall O., and Brundin P.: Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat Med 14,501-503 (2008)
19. Lee P.H., and Park H.J.:Bone marrow-derived mesenchymal stem cell therapy as a candidate diseasemodifying strategy in Parkinson's disease and multiple system atrophy. J Clin Neurol 5,1-10 (2009)
20. Bing G. L. X., Zheng N. A., Jin L., Qi Y., and Kim H.C.: Microglia mediated dopaminergic cell death in the substantia nigra: a new animal model for Parkinson's disease. Neurosci Abstr 24, 44 (1998)
21. Liu B., Jiang J. W., Wilson B.C., Du L., Yang S.N., Wang J. Y., Wu G.C., Cao X.D., and Hong J.S.: Systemic infusion of naloxone reduces degeneration of rat substantia nigral dopaminergic neurons induced by intranigral injection of lipopolysaccharide. J Pharmacol Exp Ther 295, 125-132 (2000)
22. Lu X., Bing G., and Hagg T.: Naloxone prevents microglia-induced degeneration of dopaminergic substantia nigra neurons in adult rats. Neuroscience 97, 285-291 (2000)
23. Iravani M.M., Kashefi K., Mander P., Rose S., and Jenner P.: Involvement of inducible nitric oxide synthase in inflammationinduced dopaminergic neurodegeneration. Neuroscience 110, 49-58 (2002)
24. Arimoto T., Choi D. Y., Lu X., Liu M., Nguyen X.V., Zheng N., Stewart C.A., Kim H. C., and Bing G.: Interleukin-10 protects against inflammation-mediated degeneration of dopaminergic neurons in substantia nigra. Neurobiol Aging 28, 894-906 (2007)
25. Arimoto T., and Bing G.: Up-regulation of inducible nitric oxide synthase in the substantia nigra by lipopolysaccharide causes microglial activation and neurodegeneration. Neurobiol Dis 12, 35-45 (2003)
26. Zhang J., Stanton D.M., Nguyen X.V., Liu M., Zhang Z., Gash D., and Bing G.: Intrapallidal lipopolysaccharide injection increases iron and ferritin levels in glia of the rat substantia nigra and induces locomotor deficits. Neuroscience 135, 829-838 (2005)
27. Banati R.B., Gehrmann J., Schubert P., and Kreutzberg G.W.: Cytotoxicity of microglia. Glia 7, 111-118 (1993)
28. Minghetti L., and Levi G.: Microglia as effector cells in brain damage and repair: focus on prostanoids and nitric oxide. Prog Neurobiol 54, 99-125 (1998)
29. Kim S.S., Kong P.J., Kim B.S., Sheen D.H., Nam S.Y., and Chun W.: Inhibitory action of minocycline on lipopolysaccharide-induced release of nitric oxide and prostaglandin E2 in BV2 microglial cells. Arch Pharm Res 27, 314-318 (2004)
30. 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 U S A, 100 13632-7 (2003)
31. Monje M.L., Toda H., and Palmer T.D.: Inflammatory blockade restores adult hippocampal neurogenesis. Science 302,1760-5 (2003)
32. Tansey M.G., Frank-Cannon T.C., McCoy M.K., Lee J.K., Martinez T.N., McAlpine F.E., Ruhn K.A., and Tran T.A.:Neuroinflammation in Parkinson's disease: is there sufficient evidence for mechanism-based interventional therapy? Front Biosci 13,709-17 (2008)
33. Polazzi E., and Contestabile A.: Reciprocal interactions between microglia and neurons: from survival to neuropathology. Rev Neurosci 13,221-242 (2002)
34. Andersson, P.B., Perry, V.H., and Gordon, S.: The CNS acute inflammatory response to excitotoxic neuronal cell death. Immunol Lett 30,177-181 (1991)
35. Andersson P.B., Perry V.H., and Gordon S.: The kinetics and morphological characteristics of the macrophage-microglial response to kainic acid-induced neuronal degeneration. Neuroscience 42,201-214 (1991)
36. Block M.L., Zecca L., and Hong J.S.: Microgliamediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev, Neurosci 8,57-69 (2007)
37. McGeer P.L., Itagaki S., Boyes B.E., and McGeer E.G.: Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 8,1285-91 (1988)
38. McGeer P.L., Schwab C., Parent A., and Doudet D.: Presence of reactive microglia in monkey substantia nigra years after 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine administration. Ann Neurol 54,599-604 (2003)
39. Gao H.M., Hong J.S., Zhang W., and Liu B.: Distinct role for microglia in rotenone-induced degeneration of dopaminergic neurons. J Neurosci 22, 782-790 (2002)
40. Cicchetti F., Brownell A.L., Williams K., Chen Y.I., Livni E., and Isacson O.: Neuroinflammation of the nigrostriatal pathway during progressive 6-OHDA dopamine degeneration in rats monitored by immunohistochemistry and PET imaging. Eur J Neurosci 15, 991-998 (2002)
41. Mogi M., Harada M., Narabayashi H., Inogaki H., Minami M., and Nagatsu T.: Interleukin (IL)-1 beta, IL-2, IL-4, IL-6 and transforming growth factor-alpha levels are elevated in ventricular cerebrospinal fluid in juvenile parkinsonism and Parkinson' s disease. Neurosci Lett 211,13-16 (1996)
42. Hirsch E.C., Hunot S., Damier P., Brugg B., Faucheux B.A., Michel P.P., Ruberg M., Muriel M.P., Mouatt-Prigent A., and Agid Y.: Glia cells and inflammation in Parkinson's disease: a role in neurodegeneration. Ann Neurol 44, S115-S120 (1998)
43. Mogi M., Harada M., Riederer P., Narabayashi H., Fujita K., and Nagatsu T.: Tumor necrosis factor-α (TNF- α) increases both in the brain and in the cerebrospinal fluid from parkinsonian patients. Neurosci Lett 165,208-210 (1994)
44. Le W.D., Rowe D.B., Jankovic J., Xie W.J., and Appel S.H.: Effects of cerebrospinal fluid from patients with Parkinson disease on dopaminergic cells. Arch Neurol 56,194-200 (1999)
45. Hunot S., Boissière F., Faucheux B., Brugg B., Mouatt- Prigent A., Agid Y., and Hirsch EC.: Nitric oxide synthase and neuronal vulnerability in Parkinson's disease. Neuroscience 72,355-63 (1996)
46. Hamza T.H., Zabetian C.P., Tenesa A., Laederach A., Montimurro J., Yearout D., Kay D.M., Doheny K.F., Paschall J., Pugh E., Kusel V.I., Collura R., Roberts J., Griffith A., Samii A., Scott W.K., Nutt J., Factor S.A., and Payami H.:Common genetic variation in the HLA region is associated with late-onset sporadic Parkinson's disease. Nat Genet 42,781-5 (2010)
47. Ben-Shlomo Y.: The epidemiology of Parkinson's disease. Baillieres Clin Neurol 6,55-68 (1997)
48. Factor S.A., Sanchez-Ramos J., and Weiner W.J.: Trauma as an etiology of parkinsonism: a historical review of the concept. Mov Disord 3,30-36 (1988)
49. Casals J., Elizan T.S., and Yahr M.D.: Postencephalitic parkinsonism-a review. J Neural Transm 105,645-676 (1998)
50. Ling Z., Gayle D.A., Ma S.Y., Lipton J.W., Tong C.W., Hong J.S., and Carvey P.M.: In utero bacterial endotoxin exposure causes loss of tyrosine hydroxylase neurons in the postnatal rat midbrain. Mov Disord 17,116-124 (2002)
51. Kim W.G., Mohney R.P., Wilson B., Jeohn G.H., Liu B., and Hong J.S.: Regional difference in susceptibility to lipopolysacchride-induced neurotoxicity in the rat brain: role of microglia. J Neurosci 20,6309-6316 (2000)
52. Ling Z., Zhu Y., Tong C.W., Snyder J.A., Lipoton J.W., and Carvey P.M.: Progressive dopamine neuron loss following supra-nigral lipopolysaccharide (LPS) infusion into rats exposed to LPS prenatally. Exp Neurol 199,499-512 (2006)
53. Whitton P.S.: Inflammation as a causative factor in the aetiology of Parkinson's disease. Br J Pharmacol 150,963-76 (2007)
54. Gao H.M., Jiang J., Wilson B., Zhang W.Q., Hong J.S., and Liu B.: Microglial activation-mediated delayed and progressive degeneration of rat nigral dopaminergic neurons: relevance to Parkinson's disease. J Neurochem 81,1285-1297 (2002)
55. Hererra A.J., Castano A., Venero J.L., Cano J., and Machado A.: The single intranigral injection of LPS as a new model for studying the selective effects of inflammatory reactions on dopaminergic system. Neuorobiol Dis 7,429-44 (2000)
56. Saijo K., Winner B., Carson C.T., Collier J.G. , Boyer L., Rosenfeld M.G.,Gage F.H., and Glass C.K.: A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 137, 47-59 (2009)
57. Glass C.K., Saijo K., Winner B., Marchetto M.C., and Gage F.H.: Mechanisms underlying inflammation in neurodegeneration. Cell 140,918-34 (2010)
58. Lawson L.J., Perry V.H., Dri P., and Gordon S.: Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39,151-70 (1990)
59. Kim Y.S., and Joh T.H.: Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson's disease. Exp Mol Med 38,333-47 (2006)
60. Nagatsu T., and Sawada M.: Cellular and molecular mechanisms of Parkinson's disease: neurotoxins, causative genes, and inflammatory cytokines. Cell Mol Neurobiol 26,781-802 (2006)
61. Penkowa M., Camats J., Hadberg H., Quintana A., Rojas S., Giralt M., Molinero A., Campbell I.L., and Hidalgo J.: Astrocyte-targeted expression of interleukin-6 protects the central nervous system during neuroglial degeneration induced by 6-aminonicotinamide. J Neurosci Res 73,481-496 (2003)
62. Penkowa M., Giralt M., Lago N., Camats J., Carrasco J., Hernández J., Molinero A., Campbell I.L., and Hidalgo J.: Astrocyte-targeted expression of IL-6 protects the CNS against a focal brain injury. Exp Neurol 181,130-148 (2003)
63. 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 22,486-492 (2002)
64. Sedgwick J.D., Riminton D.S., Cyster J.G., and Korner H.: Tumor necrosis factor: a master-regulator of leukocyte movement. Immunol Today 21,110-3 (2000)
65. Gayle D.A., Ling Z., Tong C., Landers T., Lipton J.W., and Carvey P.M.: Lipopolysacchride (LPS)-induced dopamine cell loss in culture: roles of tumor necrosis factor-alpha, interleukin-1beta, and nitric oxide. Brain Res Dev 133, 27-35 (2002)
66. Hunot S., Hartmann A., and Hirsh E.C.: The inflammatory response in the Parkinson brain. Clin Neurosci Res 1, 434-443 (2001)
67. Nagatsu T., and Sawada M.:Inflammatory process in Parkinson's disease: role for cytokines. Curr Pharm Des 11,999-1016 (2005)
68. Wu D.C., Teismann P., Tieu K., Vila M., Jackson-Lewis V., Ischiropoulos H., and Przedborski S.: NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine model of Parkinson's disease. Proc Natl Acad Sci U S A 100,6145-50 (2003)
69. Qin L., Liu Y., Wang T., Wei S.J., Block M.L., Wilson B., Liu B., and Hong J.S.: NADPH oxidase mediates lipopolysaccharide induced neurotoxicity and proinflammatory gene expression in activated microglia. J Biol Chem 279, 1415-1421 (2004)
70. Block M.L., and Hong J.S. Microglia and inflammationmediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol 76,77-98 (2005)
71. Dheen S.T., Kaur C., and Ling E.A.:Microglial activation and its implications in the brain diseases. Curr Med Chem 14,1189-97 (2007)
72. Kreutzberg G.W.: Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19,312-8 (1996)
73. Raivich G., Bohatschek M., Kloss U.A., Werner A., Jones L.L., and Kreutzberg G.W.: Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Res Rev 30,77-105 (1999)
74. Braak H., Del Tredici K., Rub U., de Vos R.A., Jansen Steur E.N., and Braak E.: Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 24, 197-211 (2003)
75. Roodveldt C., Christodoulou J., and Dobson C.M.: Immunological features of alpha-synuclein in Parkinson' s disease. J Cell Mol Med 12,1820-1829 (2008)
76. Reynolds A.D., Kadiu I., Garg S.K., Glanzer J.G., Nordgren T., Ciborowski P., Banerjee R., and Gendelman H.E.: Nitrated alpha-synuclein and microglial neuroregulatory activities. J Neuroimmune Pharmacol 3, 59-74 (2008)
77. Zhang W., Wang T., Pei Z., Miller D.S., Wu X., Block M.L., Wilson, B. Zhang W., Zhou Y., Hong J.S., and Zhang J.: Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson's disease. FASEB J 19, 533-542 (2005)
78. Chang R.C., Hudson P., Wilson B., Haddon L., and Hong J.S.: Influence of neurons on lipopolysaccharidestimulated production of nitric oxide and tumor necrosis factor-alpha by cultured glia. Brain Res 853,236-344 (2000)
79. Chang R.C., Hudson P., Wilson B., Liu B., Abel H., Hemperly J., and Hong J.S.: Immune modulatory effects of neural cell adhesion molecules on lipopolysaccharideinduced nitric oxide production by cultured glia. Brain Res Mol Brain Res 81,197-201 (2000)
80. Brundin P., Karlsson J., Emgård M., Schierle G.S., Hansson O., Petersén A., and Castilho R.F.:Improving the survival of grafted dopaminergic neurons: a review over current approaches. Cell Transplant 9,179-95 (2000)
81. Barker R.A., Dunnett S.B., Faissner A., and Fawcett J.W.:The time course of loss of dopaminergic neurons and the gliotic reaction surrounding grafts of embryonic mesencephalon to the striatum. Exp Neurol 141,79-93 (1996)
82. Kelly S., Bliss T.M., Shah A.K., Sun G.H., Ma M., Foo W.C., Masel J., Yenari M.A., Weissman I.L. Uchida N., Palmer T., and Steinberg G.K.:Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc Natl Acad Sci U S A 101,11839-44 (2004)
83. 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 24,623-31 (2003)
84. 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 78,1233-41 (2005)
85. 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 26,2361-71 (2008)
86. Sasaki T., Kitagawa K., Sugiura S., Omura-Matsuoka E., Tanaka S., Yagita Y., Okano H., Matsumoto M., and Hori M.: Implication of cyclooxygenase-2 on enhanced proliferation of neural progenitor cells in the adult mouse hippocampus after ischemia. J Neurosci Res 72,461-471 (2003)
87. 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;454-62 (2008)
88. Tamm C., Zhivotovsky B., and Ceccatelli S.: Caspase-2 activation in neural stem cells undergoing oxidative stressinduced apoptosis. Apoptosis 13,354-63 (2008)
89. Lin H.J., Wang X., Shaffer K.M., Sasaki C.Y., and Ma W.:Characterization of H2O2-induced acute apoptosis in cultured neural stem/progenitor cells. FEBS Lett 570,102-6 (2004)
90. Moreno-López B., Romero-Grimaldi C., Noval J.A., Murillo-Carretero M., Matarredona E.R., and Estrada C.:Nitric oxide is a physiological inhibitor of neurogenesis in the adult mouse subventricular zone and olfactory bulb. J Neurosci 24,85-95 (2004)
91. Day R.M., and Suzuki Y.J.: Cell proliferation, reactive oxygen and cellular glutathione. D ose Response 3, 425-442 (2006)
92. Halliwell B.: Oxidative stress in cell culture: an underappreciated problem? FEBS Lett 540, 3-6 (2003)
93. Yoneyama M., Kawada K., Gotoh Y., Shiba T., and Ogita K.:Endogenous reactive oxygen species are essential for proliferation of neural stem/progenitor cells. Neurochem Int 56,740-6 (2010)
94. Jeong S.W., Chu K., Jung K.H., Kim S.U., Kim M., and Roh J.K.:Human neural stem cell transplantation promotes functional recovery in rats with experimental intracerebral hemorrhage. Stroke 34,2258-63 (2003)
95. Li F., Liu Y., Zhu S., Wang X., Yang H., Liu C., Zhang Y., and Zhang Z.:Therapeutic time window and effect of intracarotid neural stem cells transplantation for intracerebral hemorrhage. Neuroreport 18,1019-23 (2007)
96. Honma T., Honmou O., Iihoshi S., Harada K., Houkin K., Hamada H., and Kocsis J.D.:Intravenous infusion of immortalized human mesenchymal stem cells protects against injury in a cerebral ischemia model in adult rat. Exp Neurol 199,56-66 (2006)
97. Veizovic T., Beech J.S., Stroemer R.P., Watson W.P., and Hodges H.:Resolution of stroke deficits following contralateral grafts of conditionally immortal neuroepithelial stem cells. Stroke 32,1012-9 (2001)
98. Kim D., Chun B.-g., Kim Y.-K., Lee Y.H., Park C.-S., Jeon I., Hwang T.S., Chung H., Gwag B.J., Hong K.S., and Song J.: In vivo tracking of human mesenchymal stem cells in experimental stroke. Cell Transplant 16,1007-1012 (2008)
99. 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 U S A 100,15983-8 (2003)
100. Belmadani A., Tran P.B., Ren D., and Miller R.J .:Chemokines regulate the migration of neural progenitors to sites of neuroinflammation. J Neurosci 26,3182-91 (2006)
101. Pluchino S., Zanotti L., Rossi B., Brambilla E., Ottoboni L., Salani G., Martinello M., Cattalini A., Bergami A., Furlan R., Comi G., Constantin G., and Martino G.:Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 436,266-71 (2005)
102. Mathieu P., Battista D., Depino A., Roca V., Graciarena M., and 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 112,1368-85 (2010)
103. Cayre M., Canoll P., and Goldman J.E.:Cell migration in the normal and pathological postnatal mammalian brain. Prog Neurobiol 88,41-63 (2009)
104. Chamberlain G., Fox J., Ashton B., and Middleton J.:mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25,2739-49 (2007)
105. Karp J.M., and Leng Teo G.S.:Mesenchymal stem cell homing: the devil is in the details. Cell S tem Cell 4,206-16 (2009)
106. Hall P.E., Lathia J.D., Miller N.G., Caldwell M.A., and ffrench-Constant C.: Integrins are markers of human neural stem cells. Stem Cells 24,2078-2084 (2006)
107. Rampon C., Weiss N., Deboux C., Chaverot N., Miller F., Buchet D., Tricoire-Leignel H., Cazaubon S., Baron- Van Evercooren A., and Couraud P.O.: Molecular mechanism of systemic delivery of neural precursor cells to the brain: assembly of brain endothelial apical cups and control of transmigration by CD44. Stem Cells 26,1673-1682 (2008)
108. Yagi H., Soto-Gutierrez A., Parekkadan B., Kitagawa Y., Tompkins R.G., Kobayashi N., and Yarmush M.L.:Mesenchymal Stem Cells: Mechanisms of Immunomodulation and Homing. Cell Transplant 19,667- 79 (2010)
109. De Becker A., Van Hummelen P., Bakkus M., Vande Broek I., De Wever J., De Waele M., and Van Riet I.: Migration of culture-expanded human mesenchymal stem cells through bone marrow endothelium is regulated by matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-3. Haematologica 92, 440-449 (200 7)
110. McCoy M.K., and Tansey M.G.: TNF signaling inhibition in the CNS: Implications for normal brain function and neurodegenerative disease. J Neuroinflammation 5,45 (2008)
111. Tuttolomondo A., Di Raimondo D., di Sciacca R., Pinto A., and Licata G.: Inflammatory cytokines in acute ischemic stroke. Curr Pharm Des 14,3574-3589 (2008)
112. Garzón-Muvdi T., and Quiñones-Hinojosa A.:Neural stem cell niches and homing: recruitment and integration into functional tissues. ILAR J 51,3-23 (2010)
113. Lundberg C., Martinez-Serrano A., Cattaneo E. , McKay R.D., and Bjorklund A.: Survival, integration, and differentiation of neural stem cell lines after transplantation to the adult rat striatum. Exp Neurol 145, 342-360 (1997)
114. Zhu P., Hata R., Cao F., Gu F., Hanakawa Y., Hashimoto K., and Sakanaka M.:Ramified microglial cells promote astrogliogenesis and maintenance of neural stem cells through activation of Stat3 function. FASEB J 22,3866-77 (2008)
115. 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 25,649-58 (2007)
116. Monje M.L., Toda H., and Palmer T.D.:Inflammatory blockade restores adult hippocampal neurogenesis. Science 302,1760-5 (2003)
117. Keohane A., Ryan S., Maloney E., Sullivan A.M., and Nolan Y.M.:Tumour necrosis factor-alpha impairs neuronal differentiation but not proliferation of hippocampal neural precursor cells: Role of Hes1. Mol Cell Neurosci 43,127-35 (2010)
118. Liu Y.P., Lin H.I., and Tzeng S.F.:Tumor necrosis factoralpha and interleukin-18 modulate neuronal cell fate in embryonic neural progenitor culture. Brain Res 1054,152-8 (2005)
119. 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 26,2361-71 (2008)
120. Ziv Y., Ron N., Butovsky O., Landa G., Sudai E., Greenberg N., Cohen H., Kipnis J., and Schwartz M.:Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 9,268-75 (2006)
121. Walton N.M., Sutter B.M., Laywell E.D., Levkoff L.H., Kearns S.M., Marshall G.P., 2nd, Scheffler B., and Steindler D.A.:Microglia instruct subventricular zone neurogenesis. Glia 54, 815-825 (2006)
122. 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, 149-160 (2006)
123. Ziv Y., and Schwartz M.:Immune-based regulation of adult neurogenesis: implications for learning and memory. Brain Behav Immun 22,167-76 (2008)
124. Cicchetti F., Saporta S., Hauser R.A., Parent M., Saint-Pierre M., Sanberg P.R., Li X.J., Parker J.R., Chu,Y., Mufson E.J., Kordower J.H., and Freeman T.B.: Neural transplants in patients with Huntington's disease undergo disease-like neuronal degeneration. Proc Natl Acad Sci U S A 106 12483-8 (2009)
125. Modo M., Mellodew K., and Rezaie P.: In vitro expression of major histocompatibility class I and class II antigens by conditionally immortalized murine neural stem cells. Neurosci Lett 337, 85-88 (2003)
126. McLaren F.H., Svendsen C.N., Van der Meide P., and Joly E.: Analysis of neural stem cells by flow cytometry: cellular differentiation modifies patterns of MHC expression. J Neuroimmunol 112, 35-46 (2001)
127. Imitola J., Comabella M., Chandraker A.K., Dangond F., Sayegh M.H., Snyder E.Y., and Khoury S.J.: Neural stem/progenitor cells express costimulatory molecules that are differentially regulated by inflammatory and apoptotic stimuli. Am J Pathol 164, 1615-1625 (2004)
128. 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, 2444-2454 (2008)
129. 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 13, 3556-69 (2009)
130. 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, 128-143 (1996)
131. 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, 213-219 (1997)
132. 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, 311-327 (2006)
133. Carpentier P.A., and Palmer T.D.: Immune influence on adult neural stem cell regulation and function. Neuron 64,79-92 (2009)
134. Drukker M., Katz G., Urbach A., Schuldiner M., Markel G., Itskovitz-Eldor J., Reubinoff B., Mandelboim O., and Benvenisty N.: Characterization of the expression of MHC proteins in human embryonic stem cells. Proc Natl Acad Sci U S A 99, 9864-9869 (2002)
135. Swijnenburg R.J., Tanaka M., Vogel H., Baker J., Kofidis T., Gunawan F., Lebl D.R., Caffarelli A.D., de Bruin J.L., Fedoseyeva E.V., and Robbins R.C.: Embryonic stem cell immunogenicity increases upon differentiation after transplantation into ischemic myocardium. Circulation 112, I166-I172 (2005)
136. Le Blanc K., Tammik C., Rosendahl K., Zetterberg E., and Ringdén O.: HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 31, 890-896 (2003)
137. Le Blanc K.: Immunomodulatory effects of fetal and adult mesenchymal stem cells. Cytotherapy 5, 485-489 (2003)
138. Nasef A., Mathieu N., Chapel A., Frick J., François S., Mazurier C., Boutarfa A., Bouchet S., Gorin N.C., Thierry D., and Fouillard L.: Immunosuppressive effects of mesenchymal stem cells: involvement of HLA-G. Transplantation 84,231-237 (2007)
139. Kordower J.H., Freeman T.B., Snow B.J., Vingerhoets F.J.G., Mufson E.J., Sanberg P.R., Hauser R.A., Smith D.A., Nauert G.M., Perl D.P., and Olanow C.W.: Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson's disease. N Engl J Med 332,1118-1124 (1995)
140. Olanow C.W., G oetz C.G., Kordower J.H., Stoessl A.J., Sossi V., Brin M.F., Shannon K.M., Nauert G.M., Perl D.P., Godbold J., and Freeman T.B.: A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson' s disease. Ann Neurol 54, 403-414 (2003)
141. Fändrich F., Lin X., Chai G.X., Schulze M., Ganten D., Bader M., Holle J., Huang D.S., Parwaresch R., Zavazava N., and Binas B.: Preimplantation-stage stem cells induce longterm allogeneic graft acceptance without supplementary host conditioning. Nat Med 8,171-8 (2002)
142. Zappia E., Casazza S., Pedemonte E., Benvenuto F., Bonanni I., Gerdoni E., Giunti D., Ceravolo A., Cazzanti F., Frassoni F., Mancardi G., and Uccelli A.: Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 106,1755-61 (2005)
143. Minghetti L.: Role of inflammation in neurodegenerative diseases. Curr Opin Neurol 18,315-21 (2005)
144. Owens T., Wekerle H., and Antel J.: Genetic models for CNS inflammation. Nat Med 7,161-6 (2001)
145. Pluchino S., Quattrini A., Brambilla E., Gritti A., Salani G., Dina G., Galli R., Del Carro U., Amadio S., Bergami A., Furlan R., Comi G., Vescovi A.L., and Martino G.: Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422,688-94 (2003)
146. 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 61,209-18 (2007)
147. Ben-Hur T.:Immunomodulation by neural stem cells. J Neurol Sci 265,102-4 (2008)
148. Pluchino S., Zanotti L., Brambilla E., Rovere-Querini P., Capobianco A., Alfaro-Cervello C., Salani G., Cossetti C., Borsellino G., Battistini L., Ponzoni M., Doglioni C., Garcia- Verdugo J.M., Comi G., and Manfredi A.A., Martino G.:Immune regulatory neural stem/precursor cells protect from central nervous system autoimmunity by restraining dendritic cell function. PLoS One 4,e5959 (2009)
149. Yang J., Jiang Z., Fitzgerald D.C., Ma C., Yu S., Li H., Zhao Z., Li Y., Ciric B., Curtis M., Rostami A., and Zhang G.X.:Adult neural stem cells expressing IL-10 confer potent immunomodulation and remyelination in experimental autoimmune encephalitis. J Clin Invest 119,3678-91 (2009)
150. 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., Kim S.U., Park C.G., Lee S.K., Kim M., and Roh J.K.:Anti-inflammatory mechanism of intravascular neural stem cell transplantation in haemorrhagic stroke. Brain 131,616-29 (2008)
151. Nauta A.J., and Fibbe W.E.:Immunomodulatory properties of mesenchymal stromal cells. Blood 110,3499-506 (2007)
152. Müller I., Lymperi S., and Dazzi F.:Mesenchymal stem cell therapy for degenerative inflammatory disorders. Curr Opin Organ Transplant 13, 639-44 (2008)
153. Gerdoni E., Gallo B., Casazza S., Musi, S., Bonanni I., Pedemonte E., Mantegazza R., Frassoni F., Mancardi G., Pedotti R., and Uccelli A.:Mesenchymal stem cells effectively modulate pathogenic immune response in experimental autoimmune encephalomyelitis. Ann Neurol 61,219-27 (2007)
154. Kassis I., Grigoriadis N., Gowda-Kurkalli B., Mizrachi-Kol R., Ben-Hur T., Slavin S., Abramsky O., and Karussis D.: Neuroprotection and immunomodulation with mesenchymal stem cells in chronic experimental autoimmune
155. Kim Y.J., Park H.J., Lee G., Bang O.Y., Ahn Y.H., Joe E., Kim H.O., and Lee P.H.:Neuroprotective effects of human mesenchymal stem cells on dopaminergic neurons through anti-inflammatory action. Glia 57,13-23 (2009)
156. Chao Y.X., He B.P., and Tay S.S.:Mesenchymal stem cell transplantation attenuates blood brain barrier damage and neuroinflammation and protects dopaminergic neurons against MPTP toxicity in the substantia nigra in a model of Parkinson's disease. J Neuroimmunol 216,39-50 (2009)