Identification of chemoattractive factors involved in the migration of bone marrow-derived mesenchymal stem cells to brain lesions caused by prions

Journal of Virology

Volumn 85, Issue 21, 2011, Pages 11069-11078

  Song, Chang Hyun ^a,d   Honmou, Osamu ^b   Furuoka, Hidefumi ^c   Horiuchi, Motohiro ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b SAPPORO MEDICAL UNIVERSITY   (Japan)

^c OBIHIRO UNIVERSITY OF AGRICULTURE AND VETERINARY MEDICINE   (Japan)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOATTRACTANT; CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR3; CHEMOKINE RECEPTOR CCR3 ANTIBODY; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR5 ANTIBODY; CHEMOKINE RECEPTOR CX3CR1; CHEMOKINE RECEPTOR CXCR3; CHEMOKINE RECEPTOR CXCR3 ANTIBODY; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR4 ANTIBODY; LIGAND; PROTEIN ANTIBODY; UNCLASSIFIED DRUG; VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BRAIN DAMAGE; CELL ASSAY; CELL FUNCTION; CELL MIGRATION; CHEMOTAXIS; CONTROLLED STUDY; CORPUS CALLOSUM; DISEASE COURSE; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMOBILIZED CELL; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PRION; PRION DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BRAIN; CELL MIGRATION ASSAYS; CELL MOVEMENT; CYTOKINES; MESENCHYMAL STEM CELLS; MICE; PRION DISEASES; PRIONS; RECEPTORS, CYTOKINE;

MUS;

EID: 80055121059     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05318-11     Document Type: Article

References (66)

1. Alvarez-Dolado, M., et al. 2003. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes, and hepatocytes. Nature 425:968-973.
2. Annabi, B., et al. 2003. Hypoxia promotes murine bone-marrow-derived stromal cell migration and tube formation. Stem Cells 21:337-347.
3. Azizi, S. A., D. Stokes, B. J. Augelli, C. DiGirolamo, and D. J. Prockop. 1998. Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats: similarities to astrocyte grafts. Proc. Natl. Acad. Sci. U. S. A. 95:3908-3913.
4. Bang, O. Y., J. S. Lee, P. H. Lee, and G. Lee. 2005. Autologous mesenchymal stem cell transplantation in stroke patients. Ann. Neurol. 57:874-882.
5. Campbell, I. L., M. Eddleston, P. Kemper, M. B. Oldstone, and M. V. Hobbs. [1994] Activation of cerebral cytokine gene expression and its correlation with onset of reactive astrocyte and acute-phase response gene expression in scrapie. J. Virol. 68:2383-2387.
6. Carbonell, W. S., S. Murase, A. F. Horwitz, and J. W. Mandell. 2005. Migration of perilesional microglia after focal brain injury and modulation by CC chemokine receptor 5: an in situ time-lapse confocal imaging study. J. Neurosci. 25:7040-7047.
7. Cardona, A. E., et al. 2006. Control of microglial neurotoxicity by the fractalkine receptor. Nat. Neurosci. 9:917-924.
8. Chamberlain, G., J. Fox, B. Ashton, and J. Middleton. 2007. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells. 25:2739-2749.
9. Charo, I. F., and R. M. Ransohoff. 2006. The many roles of chemokines and chemokine receptors in inflammation. N. Engl. J. Med. 354:610-621.
10. Chen, J., et al. 2001. Therapeutic benefit of intracerebral transplantation of bone marrow stromal cells after cerebral ischemia in rats. J. Neurol. Sci. 189:49-57.
11. Chien, L. Y., et al. 2011. In vivo magnetic resonance imaging of cell tropism, trafficking mechanism, and therapeutic impact of human mesenchymal stem cells in a murine glioma model. Biomaterials 32:3275-3284.
12. Chopp, M., and Y. Li. 2002. Treatment of neural injury with marrow stromal cells. Lancet Neurol. 1:92-100.
13. Demaimay, R., et al. 1997. Late treatment with polyene antibiotics can prolong the survival time of scrapie-infected animals. J. Virol. 71:9685-9689.
14. Doh-ura, K., et al. 2004. Treatment of transmissible spongiform encephalopathy by intraventricular drug infusion in animal models. J. Virol. 78:4999-5006.
15. Dwyer, R. M., et al. 2007. Monocyte chemotactic protein-1 secreted by primary breast tumors stimulates migration of mesenchymal stem cells. Clin. Cancer Res. 13:5020-5027.
16. Forte, G., et al. 2006. Hepatocyte growth factor effects on mesenchymal stem cells: proliferation, migration, and differentiation. Stem Cells 24:23-33.
17. Fox, J. M., G. Chamberlain, B. A. Ashton, and J. Middleton. 2007. Recent advances into the understanding of mesenchymal stem cell trafficking. Br. J. Haematol. 137:491-502.
18. Haynes, S. E., et al. 2006. The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat. Neurosci. 9:1512-1519.
19. Hellmann, M. A., H. Panet, Y. Barhum, E. Melamed, and D. Offen. 2006. Increased survival and migration of engrafted mesenchymal bone marrow stem cells in 6-hydroxydopamine-lesioned rodents. Neurosci. Lett. 395:124-128.
20. Hofstetter, C. P., et al. 2002. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc. Natl. Acad. Sci. U. S. A. 99:2199-2204.
21. Huang, D., et al. 2006. The neuronal chemokine CX3CL1/fractalkine selectively recruits NK cells that modify experimental autoimmune encephalomyelitis within the central nervous system. FASEB J. 20:896-905.
22. Hung, S. C., et al. 2007. Short-term exposure of multipotent stromal cells to low oxygen increases their expression of CX3CR1 and CXCR4 and their engraftment in vivo. PLoS One 2:e416.
23. Ip, J. E., et al. 2007. Mesenchymal stem cells use integrin beta1 not CXC chemokine receptor 4 for myocardial migration and engraftment. Mol. Biol. Cell 18:2873-2882.
24. Ji, J. F., B. P. He, S. T. Dheen, and S. S. Tay. 2004. 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 22:415-427.
25. Kawasaki, Y., et al. 2007. Orally administered amyloidophilic compound is effective in prolonging the incubation periods of animals cerebrally infected with prion diseases in a prion strain-dependent manner. J. Virol. 81:12889-12898.
26. Kobune, M., et al. 2003. Telomerized human multipotent mesenchymal cells can differentiate into hematopoietic and cobblestone area-supporting cells. Exp. Hematol. 31:715-722.
27. Kocisko, D. A., et al. 2006. A porphyrin increases survival time of mice after intracerebral prion infection. Antimicrob. Agents Chemother. 50:759-761.
28. Koizumi, S., et al. 2007. UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 446:1091-1095.
29. Kopen, G. C., D. J. Prockop, and D. G. Phinney. 1999. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc. Natl. Acad. Sci. U. S. A. 96:10711-10716.
30. Lapidot, T. 2001. Mechanism of human stem cell migration and repopulation of NOD/SCID and B2mnull NOD/SCID mice: the role of SDF-1/CXCR4 interactions. Ann. N. Y. Acad. Sci. 938:83-95.
31. Lauro, C., et al. 2008. Activity of adenosine receptors type 1 Is required for CX3CL1-mediated neuroprotection and neuromodulation in hippocampal neurons. J. Immunol. 180:7590-7596.
32. Lee, P. H., et al. 2008. Autologous mesenchymal stem cell therapy delays the progression of neurological deficits in patients with multiple system atrophy. Clin. Pharmacol. Ther. 83:723-730.
33. Li, Y., et al. 2001. 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. 316:67-70.
34. Marella, M., and J. Chabry. 2004. Neurons and astrocytes respond to prion infection by inducing microglia recruitment. J. Neurosci. 24:620-627.
35. Mazzini, L., et al. 2008. Stem cell treatment in amyotrophic lateral sclerosis. J. Neurol. Sci. 265:78-83.
36. Miyasaka, M., and T. Tanaka. 2004. Lymphocyte trafficking across high endothelial venules: dogmas and enigmas. Nat. Rev. Immunol. 4:360-370.
37. Mukherjee, A., et al. 2010. Calcineurin inhibition at the clinical phase of prion disease reduces neurodegeneration, improves behavioral alterations and increases animal survival. PLoS Pathog. 6:e1001138.
38. Munoz, J. R., B. R. Stoutenger, A. P. Robinson, J. L. Spees, and D. J. Prockop. 2005. Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc. Natl. Acad. Sci. U. S. A. 102:18171-18176.
39. Nakamura, K., et al. 2004. Antitumor effect of genetically engineered mesenchymal stem cells in a rat glioma model. Gene Ther. 11:1155-1164.
40. Peled, A., et al. 1999. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 283:845-848.
41. Pittenger, M. F., et al. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
42. Ponte, A. L., et al. 2007. The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells 25:1737-1745.
43. Prockop, D. J. 1997. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71-74.
44. Prusiner, S. B., M. R. Scott, S. J. DeArmond, and F. E. Cohen. 1998. Prion protein biology. Cell 93:337-348.
45. Rappert, A., et al. 2004. CXCR3-dependent microglial recruitment is essential for dendrite loss after brain lesion. J. Neurosci. 24:8500-8509.
46. Riemer, C., et al. 2004. Gene expression profiling of scrapie-infected brain tissue. Biochem. Biophys. Res. Commun. 323:556-564.
47. Riemer, C., et al. 2008. Accelerated prion replication in, but prolonged survival times of, prion-infected CXCR3_/_ mice. J. Virol. 82:12464-12471.
48. Ringe, J., et al. 2007. Towards in situ tissue repair: human mesenchymal stem cells express chemokine receptors CXCR1, CXCR2, and CCR2 and migrate upon stimulation with CXCL8 but not CCL2. J. Cell Biochem. 101:135-146.
49. Son, B. R., et al. 2006. Migration of bone marrow and cord blood mesenchymal stem cells in vitro is regulated by stromal-derived factor-1-CXCR4 and hepatocyte growth factor-c-met axes and involves matrix metalloproteinases. Stem Cells 24:1254-1264.
50. Song, C. H., et al. 2008. Effect of intraventricular infusion of anti-prion protein monoclonal antibodies on disease progression in prion-infected mice. J. Gen. Virol. 89:1533-1544.
51. Song, C. H., et al. 2009. Effect of transplantation of bone marrow-derived mesenchymal stem cells on mice infected with prions. J. Virol. 83:5918-5927.
52. Spaeth, E., A. Klopp, J. Dembinski, M. Andreeff, and F. Marini. 2008. Inflammation and tumor microenvironments: defining the migratory itinerary of mesenchymal stem cells. Gene Ther. 15:730-738.
53. Springer, T. A. 1994. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76:301-314.
54. Sykova, E., and P. Jendelova. 2007. Migration, fate and in vivo imaging of adult stem cells in the CNS. Cell Death Differ. 14:1336-1342.
55. Tamguney, G., et al. 2008. Genes contributing to prion pathogenesis. J. Gen. Virol. 89:1777-1788.
56. Trevitt, C. R., and J. Collinge. 2006. A systematic review of prion therapeutics in experimental models. Brain 129:2241-2265.
57. Tribouillard-Tanvier, D., J. F. Striebel, K. E. Peterson, and B. Chesebro. [2009] Analysis of protein levels of 24 cytokines in scrapie agent-infected brain and glial cell cultures from mice differing in prion protein expression levels. J. Virol. 83:11244-11253.
58. Uryu, M., A. Karino, Y. Kamihara, and M. Horiuchi. 2007. Characterization of prion susceptibility in Neuro2a mouse neuroblastoma cell subclones. Microbiol. Immunol. 51:661-669.
59. Vercelli, A., et al. 2008. Human mesenchymal stem cell transplantation extends survival, improves motor performance and decreases neuroinflammation in mouse model of amyotrophic lateral sclerosis. Neurobiol. Dis. 31:395-405.
60. Von Luttichau, I., et al. 2005. Human adult CD34_ progenitor cells functionally express the chemokine receptors CCR1, CCR4, CCR7, CXCR5, and CCR10 but not CXCR4. Stem Cells Dev. 14:329-336.
61. Wang, L., et al. 2002. Ischemic cerebral tissue and MCP-1 enhance rat bone marrow stromal cell migration in interface culture. Exp. Hematol. 30:831-836.
62. Wang, L., et al. 2002. MCP-1, MIP-1, IL-8 and ischemic cerebral tissue enhance human bone marrow stromal cell migration in interface culture. Hematology 7:113-117.
63. Wang, Y., Y. Deng, and G. Q. Zhou. 2008. SDF-1alpha/CXCR4-mediated migration of systemically transplanted bone marrow stromal cells toward ischemic brain lesion in a rat model. Brain Res. 1195:104-112.
64. Wilson, E. H., W. Weninger, and C. A. Hunter. 2010. Trafficking of immune cells in the central nervous system. J. Clin. Invest. 120:1368-1379.
65. Xiang, W., et al. 2004. Identification of differentially expressed genes in scrapie-infected mouse brains by using global gene expression technology. J. Virol. 78:11051-11060.
66. Zhang, F., et al. 2009. Transforming growth factor-beta promotes recruitment of bone marrow cells and bone marrow-derived mesenchymal stem cells through stimulation of MCP-1 production in vascular smooth muscle cells. J. Biol. Chem. 284:17564-17574.