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

Journal of Neuroimmunology

Volumn 216, Issue 1-2, 2009, Pages 39-50

  Chao, Yin Xia ^a   He, Bei Ping ^a   Tay, Samuel Sam Wah ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Blood brain barrier; Mesenchymal stem cells; MPTP; Neuroinflammation; Parkinson's disease

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; CLAUDIN 1; CLAUDIN 5; MANNOSE BINDING LECTIN; OCCLUDIN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CELL ACTIVATION; CELL MIGRATION; CONTROLLED STUDY; CYTOTOXICITY; DOPAMINERGIC NERVE CELL; IMMUNOMODULATION; LIVER PARENCHYMA; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MICROGLIA; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; SUBSTANTIA NIGRA; THERAPY EFFECT;

ANIMALS; BLOOD-BRAIN BARRIER; CELL DEATH; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOPAMINE; ENCEPHALITIS; GLIOSIS; INFUSIONS, INTRAVENOUS; LIVER; MALE; MANNOSE-BINDING LECTINS; MEMBRANE PROTEINS; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; MICE, INBRED C57BL; NERVE DEGENERATION; NEURONS; PARKINSONIAN DISORDERS; SUBSTANTIA NIGRA; TREATMENT OUTCOME;

EID: 71749083461     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2009.09.003     Document Type: Article

References (61)

1. Aloisi F. Immune function of microglia. Glia 36 (2001) 165-179
2. Bertani N., Malatesta P., Volpi G., Sonego P., and Perris R. Neurogenic potential of human mesenchymal stem cells revisited: analysis by immunostaining, time-lapse video and microarray. J. Cell Sci. 118 (2005) 3925-3936
3. Boche D., Cunningham C., Docagne F., Scott H., and Perry V.H. TGFbeta1 regulates the inflammatory response during chronic neurodegeneration. Neurobiol. Dis. 22 (2006) 638-650
4. Bonifati D.M., and Kishore U. Role of complement in neurodegeneration and neuroinflammation. Mol. Immunol. 44 (2007) 999-1010
5. Chao Y.X., He B.P., Cao Q., and Tay S.S. Protein aggregate-containing neuron-like cells are differentiated from bone marrow mesenchymal stem cells from mice with neurofilament light subunit gene deficiency. Neurosci. Lett. 417 (2007) 240-245
6. Chen Y., Teng F.Y., and Tang B.L. Coaxing bone marrow stromal mesenchymal stem cells towards neuronal differentiation: progress and uncertainties. Cell. Mol. Life Sci. 63 (2006) 1649-1657
7. Choi C.B., Cho Y.K., Prakash K.V., Jee B.K., Han C.W., Paik Y.K., Kim H.Y., Lee K.H., Chung N., and Rha H.K. Analysis of neuron-like differentiation of human bone marrow mesenchymal stem cells. Biochem. Biophys. Res. Commun. 350 (2006) 138-146
8. Corcione A., Benvenuto F., Ferretti E., Giunti D., Cappiello V., Cazzanti F., Risso M., Gualandi F., Mancardi G.L., Pistoia V., and Uccelli A. Human mesenchymal stem cells modulate B-cell functions. Blood 107 (2006) 367-372
9. Dezawa M., Hoshino M., Nabeshima Y., and Ide C. Marrow stromal cells: implications in health and disease in the nervous system. Curr. Mol. Med. 5 (2005) 723-732
10. Di Nicola M., Carlo-Stella C., Magni M., Milanesi M., Longoni P.D., Matteucci P., Grisanti S., and Gianni A.M. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99 (2002) 3838-3843
11. Dohgu S., Yamauchi A., Takata F., Naito M., Tsuruo T., Higuchi S., Sawada Y., and Kataoka Y. Transforming growth factor-beta1 upregulates the tight junction and P-glycoprotein of brain microvascular endothelial cells. Cell. Mol. Neurobiol. 24 (2004) 491-497
12. El-Badri N.S., Maheshwari A., and Sanberg P.R. Mesenchymal stem cells in autoimmune disease. Stem Cells Dev. 13 (2004) 463-472
13. Gao H.M., Liu B., Zhang W., and Hong J.S. Novel anti-inflammatory therapy for Parkinson's disease. Trends Pharmacol. Sci. 24 (2003) 395-401
14. Hajela K., Kojima M., Ambrus G., Wong K.H., Moffatt B.E., Ferluga J., Hajela S., Gál P., and Sim R.B. The biological functions of MBL-associated serine proteases (MASPs). Immunobiology 205 (2002) 467-475
15. Hart M.L., Walsh M.C., and Stahl G.L. Initiation of complement activation following oxidative stress. In vitro and in vivo observations. Mol. Immunol. 41 (2004) 165-171
16. Herrera A.J., Tomas-Camardiel M., Venero J.L., Cano J., and Machado A. Inflammatory process as a determinant factor for the degeneration of substantia nigra dopaminergic neurons. J. Neural Transm. 112 (2005) 111-119
17. Holmskov U., Thiel S., and Jensenius J.C. Collections and ficolins: humoral lectins of the innate immune defense. Ann. Rev. Immunol. 21 (2003) 547-578
18. Iravani M.M., Leung C.C., Sadeghian M., Haddon C.O., Rose S., and Jenner P. The acute and the long-term effects of nigral lipopolysaccharide administration on dopaminergic dysfunction and glial cell activation. Eur. J. NeuroSci. 22 (2005) 317-330
19. Jackson-Lewis V., and Przedborski S. Protocol for the MPTP mouse model of Parkinson's disease. Natl. Protoc. 2 (2007) 141-151
20. Ji J.F., He B.P., Dheen S.T., and Tay S.S. Interactions of chemokines and chemokine receptors mediate the migration of mesenchymal stem cells to the impaired site in the brain after hypoglossal nerve injury. Stem Cells 22 (2004) 415-427
21. Jiang X.X., Zhang Y., Liu B., Zhang S.X., Wu Y., Yu X.D., and Mao N. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 105 (2005) 4120-4126
22. Keshet G.I., Tolwani R.J., Trejo A., Kraft P., Doyonnas R., Clayberger C., Weimann J.M., and Blau H.M. Increased host neuronal survival and motor function in BMT Parkinsonian mice: involvement of immunosuppression. J. Comp. Neurol. 504 (2007) 690-701
23. 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 (2006) 333-347
24. 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 (2009) 13-23
25. Kokovay E., and Cunningham L.A. Bone marrow-derived microglia contribute to the neuroinflammatory response and express iNOS in the MPTP mouse model of Parkinson's disease. Neurobiol. Dis. 19 (2005) 471-478
26. Kortekaas R., Leenders K.L., Van Oostrom J.C., Vaalburg W., Bart J., Willemsen A.T., and Hendrikse N.H. Blood brain barrier dysfunction in Parkinsonian midbrain in vivo. Ann. Neurol. 57 (2005) 176-179
27. Kurkowska-Jastrzebska I., Wronska A., Kohutnicka M., Czlonkowski A., and Czlonkowska A. The inflammatory reaction following 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine intoxication in mouse. Exp. Neurol. 156 (1999) 50-61
28. Le Blanc K., Tammik L., Sundberg B., Haynesworth S.E., and Ringden O. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand. J. Immunol. 57 (2003) 11-20
29. Li Y., Chen J., Wang L., Zhang L., Lu M., and Chopp M. Intracerebral transplantation of bone marrow stromal cells in a 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine mouse model of Parkinson's disease. Neurosci. Lett. 316 (2001) 67-70
30. Liu H., Jensen L., Hansen S., Petersen S.V., Takahashi K., Ezekowitz A.B., Hansen F.D., Jensenius J.C., and Thiel S. Characterization and quantification of mouse mannan-binding lectins (MBL-A and MBL-C) and study of acute phase responses. Scand. J. Immunol. 53 (2001) 489-497
31. Liu H., Kemeny D.M., Heng B.C., Ouyang H.W., Melendez A.J., and Cao T. The immunogenicity and immunomodulatory function of osteogenic cells differentiated from mesenchymal stem cells. J. Immunol. 176 (2006) 2864-2871
32. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) Method. Methods 25 (2001) 402-408
33. Lu J., Moochhala S., Moore X.L., Ng K.C., Tan M.H., Lee L.K.H., He B.P., Wong M.C., and Ling E.A. Adult bone marrow cells differentiate into neural phenotypes and improve functional recovery in rats following traumatic brain injury. Neurosci. Lett. 398 (2006) 12-17
34. Matter K., and Balda M.S. Holey barrier: claudins and the regulation of brain endothelial permeability. J. Cell Biol. 161 (2003) 459-460
35. 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 38 (1988) 1285-1291
36. 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 (2003) 599-604
37. Nag S., Venugopalan R., and Stewart D.J. Increased caveolin-1 expression precedes decreased expression of occludin and claudin-5 during blood-brain barrier breakdown. Acta Neuropathol. 114 (2007) 459-469
38. Orr C.F., Rowe D.B., Mizuno Y., Mori H., and Halliday G.M. A possible role for humoral immunity in the pathogenesis of Parkinson's disease. Brain 128 (2005) 2665-2674
39. Papadopoulos M.C., Saadoun S., Binder D.K., Manley G.T., Krishna S., and Verkman A.S. Molecular mechanisms of brain tumor edema. Neuroscience 129 (2004) 1011-1020
40. Park H.J., Lee P.H., Bang O.Y., Lee G., and Ahn Y.H. Mesenchymal stem cells therapy exerts neuroprotection in a progressive animal model of Parkinson's disease. J. Neurochem. 107 (2008) 141-151
41. Piccini P., and Brooks D.J. Etiology of Parkinson's disease: contributions from 18F-DOPA positron emission tomography. Adv. Neurol. 80 (1999) 227-231
42. Prat A., Bienacki K., Wosik K., and Antel J.P. Glial cell influence on the human blood-brain barrier. Glia 36 (2001) 145-155
43. Qin L., Wu X., Block M.L., Liu Y., Breese G.R., Hong J.S., Knapp D.J., and Crews F.T. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55 (2007) 453-462
44. Ren G., Zhang L., Zhao X., Xu G., Zhang Y., Roberts A.I., Zhao R.C., and Shi Y. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2 (2008) 141-150
45. Smeyne M., Jiao Y., Shepherd K.R., and Smeyne R.J. Glia cell number modulates sensitivity to MPTP in mice. Glia 52 (2005) 144-152
46. Sørensen C.M., Hansen T.K., Steffensen R., Jensenius J.C., and Thiel S. Hormonal regulation of mannan-binding lectin synthesis in hepatocytes. Clin. Exp. Immunol. 145 (2006) 173-182
47. Tan X.W., Liao H., Sun L., Okabe M., Xiao Z.C., and Dawe G.S. Fetal microchimerism in the maternal mouse brain: a novel population of fetal progenitor or stem cells able to cross the blood-brain barrier?. Stem Cells 23 (2005) 1443-1452
48. Tropel P., Platet N., Platel J.C., Noel D., Albrieux M., Benabid A.L., and Berger F. Functional neuronal differentiation of bone marrow-derived mesenchymal stem cells. Stem Cells 24 (2006) 2868-2876
49. Trzaska K.A., Kuzhikandathil E.V., and Rameshwar P. Specification of a dopaminergic phenotype from adult human mesenchymal stem cells. Stem Cells 25 (2007) 2797-2808
50. Uccelli A., Moretta L., and Pistoia V. Immunoregulatory function of mesenchymal stem cells. Eur. J. Immunol. 36 (2006) 2566-2573
51. Vorup-Jensen T., Petersen S.V., Hansen A.G., Poulsen K., Schwaeble W., Sim R.B., Reid K.B., Davis S.J., Thiel S., and Jensenius J.C. Distinct pathways of mannan-binding lectin (MBL)- and C1-complex autoactivation revealed by reconstitution of MBL with recombinant MBL-associated serine protease-2. J. Immunol. 165 (2000) 2093-2100
52. Webster S.D., Galvan M.D., Ferran E., Garzon-Rodriguez W., Glabe C.G., and Tenner A.J. Antibody-mediated phagocytosis of the amyloid beta-peptide in microglia is differentially modulated by C1q. J. Immunol. 166 (2001) 7496-7503
53. Whitton P.S. Inflammation as a causative factor in the aetiology of Parkinson's disease. Br. J. Pharmacol. 150 (2007) 963-976
54. Wislet-Gendebien S., Hans G., Leprince P., Rigo J.M., Moonen G., and Rogister B. Plasticity of cultured mesenchymal stem cells: switch from nestin-positive to excitable neuron-like phenotype. Stem Cells 23 (2005) 392-402
55. Wu D.C., Jackson-Lewis V., Vila M., Tieu K., Teismann P., Vadseth C., Choi D.K., Ischiropoulos H., and Przedborski S. Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine mouse model of Parkinson disease. J. Neurosci. 22 (2002) 1763-1771
56. Yamada T., McGeer P.L., and McGeer E.G. Lewy bodies in Parkinson's disease are recognized by antibodies to complement proteins. Acta Neuropathol. 84 (1992) 100-104
57. Yamada T., McGeer P.L., and McGeer E.G. Histological and biochemical pathology in a family with autosomal dominant Parkinsonism and dementia. Neurol. Psychiatry Brain Res. 2 (1993) 26-35
58. Yasuda Y., Shinagawa R., Yamada M., Mori T., Tateishi N., and Fujita S. Long-lasting reactive changes observed in microglia in the striatal and substantia nigral of mice after 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine. Brain Res. 1138 (2007) 196-202
59. 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 (2006) 12497-12511
60. Zhao C., Ling Z., Newman M.B., Bhatia A., and Carvey P.M. TNF-alpha knockout and minocycline treatment attenuates blood-brain barrier leakage in MPTP-treated mice. Neurobiol. Dis. 26 (2007) 36-46
61. Zhou Y., Wang Y., Kovacs M., Jin J., and Zhang J. Microglial activation induced by neurodegeneration: a proteomic analysis. Mol. Cell. Proteomics 4 (2005) 1471-1479