Human microglia transplanted in rat focal ischemia brain induce neuroprotection and behavioral improvement

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Narantuya, Dashdemberel ^a   Nagai, Atsushi ^a   Abdullah, Md ^a   Masuda, Junichi ^a   Kobayashi, Shotai ^b   Yamaguchi, Shuhei ^a   Kim, Seung U ^c,d  

^a SHIMANE UNIVERSITY FACULTY OF MEDICINE   (Japan)

^b SHIMANE UNIVERSITY HOSPITAL   (Japan)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d Chung Ang University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CHEMOKINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; INTERLEUKIN 4; INTERLEUKIN 5; OSTEOGENIC PROTEIN 1; VASCULOTROPIN; CYTOKINE; NERVE GROWTH FACTOR; TETRAZOLIUM; TRIPHENYLTETRAZOLIUM;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL COUNT; CELL MIGRATION; CELL SURVIVAL; CELL TRANSPLANTATION; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LASER CAPTURE MICRODISSECTION; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; RAT; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; CELL LINE; CYTOLOGY; METABOLISM; MICRODISSECTION; PATHOLOGY; POLYMERASE CHAIN REACTION; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ANIMALIA; RATTUS;

ANIMALS; BRAIN ISCHEMIA; CELL LINE; CYTOKINES; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICRODISSECTION; MICROGLIA; NERVE GROWTH FACTORS; POLYMERASE CHAIN REACTION; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; TETRAZOLIUM SALTS;

EID: 77955363785     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011746     Document Type: Article

References (49)

1. Gonzalez-Scarano F, Baltuch G (1999) Microglia as mediators of inflammatory and degenerative diseases. Annu Rev Neurosci 22: 219-240.
2. Kim SU, de Vellis J (2005) Microglia in health and disease. J Neurosci Res 81: 302-313.
3. Lee YB, Nagai A, Kim SU (2002) Cytokines, chemokines, and cytokine receptors in human microglia. J Neurosci Res 69: 94-103.
4. McGeer PL, McGeer EG (1995) The inflammatory response system of brain: implications for therapy of Alzheimer and other neurodegenerative diseases. Brain Res Rev 21: 195-218.
5. Block F, Peters M, Nolden-Koch M (2000) Expression of IL-6 in the ischemic penumbra. Neuroreport 11: 963-967.
6. Buttini M, Appel K, Sauter A, Gebicke-Haerter PJ, Boddeke HW (1996) Expression of tumor necrosis factor alpha after focal cerebral ischaemia in the rat. Neuroscience 71: 1-16.
7. Clausen BH, Lambertsen KL, Meldgaard M, Finsen B (2005) A quantitative in situ hybridization and polymerase chain reaction study of microglial-macro-phage expression of interleukin-1beta mRNA following permanent middle cerebral artery occlusion in mice. Neuroscience 132: 879-892.
8. Tomimoto H, Akiguchi I, Wakita H, Kinoshita A, Ikemoto A, et al. (1996) Glial expression of cytokines in the brains of cerebrovascular disease patients. Acta Neuropathol 92: 281-287.
9. Minami M, Satoh M (2003) Chemokines and their receptors in the brain: pathophysiological roles in ischemic brain injury. Life Sci 74: 321-327.
10. Miyamoto Y, Kim SU (1999) Cytokine-induced production of macrophage inflammatory protein-1alpha (MIP-1alpha) in cultured human astrocytes. J Neurosci Res 55: 245-251.
11. Takami S, Nishikawa H, Minami M, Nishiyori A, Sato M, et al. (1997) Induction of macrophage inflammatory protein MIP-1alpha mRNA on glial cells after focal cerebral ischemia in the rat. Neurosci Lett 227: 173-176.
12. Elkabes S, DiCicco-Bloom EM, Black IB (1996) Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J Neurosci 16: 2508-2521.
13. Miwa T, Furukawa S, Nakajima K, Furukawa Y, Kohsaka S (1997) Lipopolysaccharide enhances synthesis of brain-derived neurotrophic factor in cultured rat microglia. J Neurosci Res 50: 1023-1029.
14. Nakajima K, Kohsaka S (1993) Functional roles of microglia in the brain. Neurosci Res 17: 187-203.
15. Kim SU, de Vellis J (2009) Stem cell-based cell therapy in neurological diseases: a review. J Neurosci Res 87: 2183-2200.
16. Chen J, Li Y, Wang L, Zhang Z, Lu D, et al. (2001) Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 32: 1005-1011.
17. Lee HJ, Kim KS, Kim EJ, Choi HB, Lee KH, et al. (2007) Brain transplantation of immortalized human neural stem cells promotes functional recovery in mouse intracerebral hemorrhage stroke model. Stem Cells 25: 1204-1212.
18. Nagai A, Mishima S, Ishida Y, Ishikura H, Harada T, et al. (2005) Immortalized human microglial cell line: phenotypic expression. J Neurosci Res 81: 342-348.
19. Nagai A, Nakagawa E, Hatori K, Choi HB, McLarnon JG, et al. (2001) Generation and characterization of immortalized human microglial cell lines: expression of cytokines and chemokines. Neurobiol Dis 8: 1057-1068.
20. Chen H, Chopp M, Zhang ZG, Garcia JH (1992) The effect of hypothermia on transient middle cerebral artery occlusion in the rat. J Cereb Blood Flow Metab 12: 621-628.
21. Chen J, Sanberg PR, Li Y, Wang L, Lu M, et al. (2001) Intravenous administration of human umbilical cord blood reduces behavioral deficits after stroke in rats. Stroke 32: 2682-2688.
22. Nagai A, Kim WK, Lee HJ, Jeong HS, Kim KS, et al. (2007) Multilineage potential of stable human mesenchymal stem cell line derived from fetal marrow. PLoS One 2: e1272.
23. Li Y, Chopp M, Chen J, Wang L, Gautam SC, et al. (2000) Intrastriatal transplantation of bone marrow nonhematopoietic cells improves functional recovery after stroke in adult mice. J Cereb Blood Flow Metab 20: 1311-1319.
24. Jin K, Sun Y, Xie L, Mao XO, Childs J, et al. (2005) Comparison of ischemia-directed migration of neural precursor cells after intrastriatal, intraventricular, or intravenous transplantation in the rat. Neurobiol Dis 18: 366-374.
25. Chen B, Gao XQ, Yang CX, Tan SK, Sun ZL, et al. (2009) Neuroprotective effect of grafting GDNF gene-modified neural stem cells on cerebral ischemia in rats. Brain Res 1284: 1-11.
26. Rupalla K, Allegrini PR, Sauer D, Wiessner C (1998) Time course of microglia activation and apoptosis in various brain regions after permanent focal cerebral ischemia in mice. Acta Neuropathol 96: 172-178.
27. Wakabayashi K, Nagai A, Sheikh AM, Shiota Y, Narantuya D, et al. (2010) Transplantation of human mesenchymal stem cells promotes functional improvement and increased expression of neurotrophic factors in rat focal cerebral ischemia model. J Neurosci Res 88: 1017-1025.
28. Xu XH, Zhang SM, Yan WM, Li XR, Zhang HY, et al. (2006) Development of cerebral infarction, apoptotic cell death and expression of X-chromosome-linked inhibitor of apoptosis protein following focal cerebral ischemia in rats. Life Sci 78: 704-712.
29. Chen J, Li Y, Katakowski M, Chen X, Wang L, et al. (2003) Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J Neurosci Res 73: 778-786.
30. Okazaki T, Magaki T, Takeda M, Kajiwara Y, Hanaya R, et al. (2008) Intravenous administration of bone marrow stromal cells increases survivin and Bcl-2 protein expression and improves sensorimotor function following ischemia in rats. Neurosci Lett 430: 109-114.
31. Dirnagl U, Iadecola C, Moskowitz MA (1999) Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22: 391-397.
32. Panickar KS, Norenberg MD (2005) Astrocytes in cerebral ischemic injury: morphological and general considerations. Glia 50: 287-298.
33. Pekny M, Nilsson M (2005) Astrocyte activation and reactive gliosis. Glia 50: 427-434.
34. Zhang Z, Chopp M, Powers C (1997) Temporal profile of microglial response following transient (2 h) middle cerebral artery occlusion. Brain Res 744: 189-198.
35. Bruce-Keller AJ (1999) Microglial-neuronal interactions in synaptic damage and recovery. J Neurosci Res 58: 191-201.
36. Danton GH, Dietrich WD (2003) Inflammatory mechanisms after ischemia and stroke. J Neuropathol Exp Neurol 62: 127-136.
37. Zawadzka M, Kaminska B (2005) A novel mechanism of FK506-mediated neuroprotection: downregulation of cytokine expression in glial cells. Glia 49: 36-51.
38. Wang W, Redecker C, Yu ZY, Xie MJ, Tian DS, et al. (2008) Rat focal cerebral ischemia induced astrocyte proliferation and delayed neuronal death are attenuated by cyclin-dependent kinase inhibition. J Clin Neurosci 15: 278-285.
39. Zhu Z, Zhang Q, Yu Z, Zhang L, Tian D, et al. (2007) Inhibiting cell cycle progression reduces reactive astrogliosis initiated by scratch injury in vitro and by cerebral ischemia in vivo. Glia 55: 546-558.
40. Horita Y, Honmou O, Harada K, Houkin K, Hamada H, et al. (2006) Intravenous administration of glial cell line-derived neurotrophic factor gene-modified human mesenchymal stem cells protects against injury in a cerebral ischemia model in the adult rat. J Neurosci Res 84: 1495-1504.
41. Kurozumi K, Nakamura K, Tamiya T, Kawano Y, Kobune M, et al. (2004) BDNF gene-modified mesenchymal stem cells promote functional recovery and reduce infarct size in the rat middle cerebral artery occlusion model. Mol Ther 9: 189-197.
42. Toyama K, Honmou O, Harada K, Suzuki J, Houkin K, et al. (2009) Therapeutic benefits of angiogenetic gene-modified human mesenchymal stem cells after cerebral ischemia. Exp Neurol 216: 47-55.
43. Chen HL, Lein PJ, Wang JY, Gash D, Hoffer BJ, et al. (2003) Expression of bone morphogenetic proteins in the brain during normal aging and in 6-hydroxydopamine-lesioned animals. Brain Res 994: 81-90.
44. Chou J, Harvey BK, Chang CF, Shen H, Morales M, et al. (2006) Neuroregenerative effects of BMP7 after stroke in rats. J Neurol Sci 240: 21-29.
45. Lee HJ, Kim KS, Park IH, Kim SU (2007) Human neural stem cells over-expressing VEGF provide neuroprotection, angiogenesis and functional recovery in mouse stroke model. PLoS One 2: e156.
46. Lee HJ, Park IH, Kim HJ, Kim SU (2009) Human neural stem cells overexpressing glial cell line-derived neurotrophic factor in experimental cerebral hemorrhage. Gene Ther 16: 1066-1076.
47. Chen J, Zhang ZG, Li Y, Wang L, Xu YX, et al. (2003) Intravenous administration of human bone marrow stromal cells induces angiogenesis in the ischemic boundary zone after stroke in rats. Circ Res 92: 692-699.
48. Kilic U, Kilic E, Dietz GP, Bahr M (2003) Intravenous TAT-GDNF is protective after focal cerebral ischemia in mice. Stroke 34: 1304-1310.
49. Sun Y, Jin K, Xie L, Childs J, Mao XO, et al. (2003) VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J Clin Invest 111: 1843-1851.