ICV-transplanted human glial precursor cells are short-lived yet exert immunomodulatory effects in mice with EAE

GLIA

Volumn 60, Issue 7, 2012, Pages 1117-1129

  Kim, Heechul ^a   Walczak, Piotr ^a   Muja, Naser ^a   Campanelli, James T ^b   Bulte, Jeff W M ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Q Therapeutics Inc   (United States)

Author keywords

Bioluminescence imaging; EAE; Glial precursor cells; MR imaging; Multiple sclerosis

Indexed keywords

ANTIGEN; CONTRAST MEDIUM; FIREFLY LUCIFERASE; PHOSPHATE BUFFERED SALINE; SUPERPARAMAGNETIC IRON OXIDE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN DETECTION; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; ASTROCYTOSIS; BIOLUMINESCENCE; BRAIN FUNCTION; CELL DEATH; CELL FATE; CELL INFILTRATION; CELL MIGRATION; CELL SURVIVAL; CERVICAL SPINAL CORD; CONTROLLED STUDY; DISEASE SEVERITY; EX VIVO STUDY; FEMALE; GLIA CELL; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INFLAMMATORY CELL; LATERAL BRAIN VENTRICLE; LYMPHOCYTE PROLIFERATION; MACROPHAGE ACTIVATION; MICROGLIA; MOUSE; NERVE CELL DIFFERENTIATION; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOGENESIS; PHAGOCYTE; PRIORITY JOURNAL; REMYELINIZATION; SPLEEN WEIGHT; STEM CELL TRANSPLANTATION; T LYMPHOCYTE; WHITE MATTER;

ANIMALS; CELL PROLIFERATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; IMMUNOLOGIC FACTORS; INJECTIONS, INTRAVENTRICULAR; MICE; NEURAL STEM CELLS; NEUROGLIA; STEM CELL TRANSPLANTATION; T-LYMPHOCYTES;

EID: 84860669067     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22339     Document Type: Article

References (50)

1. Belmadani A, Tran PB, Ren D, Miller RJ. 2006. Chemokines regulate the migration of neural progenitors to sites of neuroinflammation. J Neurosci 26: 3182-3191.
2. Ben-Hur T, van Heeswijk RB, Einstein O, Aharonowiz M, Xue R, Frost EE, Mori S, Reubinoff BE, Bulte JW. 2007. Serial in vivo MR tracking of magnetically labeled neural spheres transplanted in chronic EAE mice. Magn Reson Med 57: 164-171.
3. Berman SC, Galpoththawela C, Gilad AA, Bulte JW, Walczak P. 2011. Long-term MR cell tracking of neural stem cells grafted in immunocompetent versus immunodeficient mice reveals distinct differences in contrast between live and dead cells. Magn Reson Med 65: 564-574.
4. Black JA, Liu S, Hains BC, Saab CY, Waxman SG. 2006. Long-term protection of central axons with phenytoin in monophasic and chronic-relapsing EAE. Brain 129: 3196-3208.
5. Buddensiek J, Dressel A, Kowalski M, Storch A, Sabolek M. 2009. Adult cerebrospinal fluid inhibits neurogenesis but facilitates gliogenesis from fetal rat neural stem cells. J Neurosci Res 87: 3054-3066.
6. Bulte JW, Arbab AS, Douglas T, Frank JA. 2004. Preparation of magnetically labeled cells for cell tracking by magnetic resonance imaging. Methods Enzymol 386: 275-299.
7. Bulte JW, Ben-Hur T, Miller BR, Mizrachi-Kol R, Einstein O, Reinhartz E, Zywicke HA, Douglas T, Frank JA. 2003. MR microscopy of magnetically labeled neurospheres transplanted into the Lewis EAE rat brain. Magn Reson Med 50: 201-205.
8. Bulte JW, Zhang S, van Gelderen P, Herynek V, Jordan EK, Duncan ID, Frank JA. 1999. Neurotransplantation of magnetically labeled oligodendrocyte progenitors: Magnetic resonance tracking of cell migration and myelination. Proc Natl Acad Sci USA 96: 15256-15261.
9. Campanelli JT, Sandrock RW, Wheatley W, Xue H, Zheng J, Liang F, Chesnut JD, Zhan M, Rao MS, Liu Y. 2008. Expression profiling of human glial precursors. BMC Dev Biol 8: 102.
10. Cheng P, Gao ZQ, Liu YH, Xue YX. 2009. Platelet-derived growth factor BB promotes the migration of bone marrow-derived mesenchymal stem cells towards C6 glioma and up-regulates the expression of intracellular adhesion molecule-1. Neurosci Lett 451: 52-56.
11. Cohen ME, Muja N, Fainstein N, Bulte JW, Ben-Hur T. 2010. Conserved fate and function of ferumoxides-labeled neural precursor cells in vitro and in vivo. J Neurosci Res 88: 936-944.
12. Compston A, Coles A. 2008. Multiple sclerosis. Lancet 372: 1502-1517.
13. Edinger M, Sweeney TJ, Tucker AA, Olomu AB, Negrin RS, Contag CH. 1999. Noninvasive assessment of tumor cell proliferation in animal models. Neoplasia 1: 303-310.
14. Einstein O, Fainstein N, Vaknin I, Mizrachi-Kol R, Reihartz E, Grigoriadis N, Lavon I, Baniyash M, Lassmann H, Ben-Hur T. 2007. Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression. Ann Neurol 61: 209-218.
15. Engelhardt B. 2008. Immune cell entry into the central nervous system: Involvement of adhesion molecules and chemokines. J Neurol Sci 274: 23-26.
16. Engelhardt B, Wolburg-Buchholz K, Wolburg H. 2001. Involvement of the choroid plexus in central nervous system inflammation. Microsc Res Tech 52: 112-129.
17. Franklin RJ, Ffrench-Constant C. 2008. Remyelination in the CNS: From biology to therapy. Nat Rev Neurosci 9: 839-855.
18. Frohman EM, Racke MK, Raine CS. 2006. Multiple sclerosis-The plaque and its pathogenesis. N Engl J Med 354: 942-955.
19. Hardison JL, Nistor G, Gonzalez R, Keirstead HS, Lane TE. 2006. Transplantation of glial-committed progenitor cells into a viral model of multiple sclerosis induces remyelination in the absence of an attenuated inflammatory response. Exp Neurol 197: 420-429.
20. Hatch MN, Schaumburg CS, Lane TE, Keirstead HS. 2009. Endogenous remyelination is induced by transplant rejection in a viral model of multiple sclerosis. J Neuroimmunol 212: 74-81.
21. Hatterer E, Touret M, Belin MF, Honnorat J, Nataf S. 2008. Cerebrospinal fluid dendritic cells infiltrate the brain parenchyma and target the cervical lymph nodes under neuroinflammatory conditions. PLoS One 3: e3321.
22. Hemmer B, Archelos JJ, Hartung HP. 2002. New concepts in the immunopathogenesis of multiple sclerosis. Nat Rev Neurosci 3: 291-301.
23. Hinks GL, Franklin RJ. 1999. Distinctive patterns of PDGF-A, FGF-2, IGF-I, and TGF-beta1 gene expression during remyelination of experimentally-induced spinal cord demyelination. Mol Cell Neurosci 14: 153-168.
24. Jin Y, Neuhuber B, Singh A, Bouyer J, Lepore A, Bonner J, Himes T, Campanelli JT, Fischer I. 2011. Transplantation of human glial restricted progenitors and derived astrocytes into a contusion model of spinal cord injury. J Neurotrauma 28: 579-594.
25. Jones MV, Nguyen TT, Deboy CA, Griffin JW, Whartenby KA, Kerr DA, Calabresi PA. 2008. Behavioral and pathological outcomes in MOG 35-55 experimental autoimmune encephalomyelitis. J Neuroimmunol 199: 83-93.
26. Karussis D, Karageorgiou C, Vaknin-Dembinsky A, Gowda-Kurkalli B, Gomori JM, Kassis I, Bulte JW, Petrou P, Ben-Hur T, Abramsky O, Slavin S. 2010. Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch Neurol 67: 1187-1194.
27. Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, Sharp K, Steward O. 2005. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 25: 4694-4705.
28. Li Z, Suzuki Y, Huang M, Cao F, Xie X, Connolly AJ, Yang PC, Wu JC. 2008. Comparison of reporter gene and iron particle labeling for tracking fate of human embryonic stem cells and differentiated endothelial cells in living subjects. Stem Cells 26: 864-873.
29. Matsumoto Y, Abe S, Tsuchida M, Hirahara H, Abo T, Shin T, Tanuma N, Kojima T, Ishihara Y. 1996. Characterization of CD4-CD8- T cell receptor alpha beta + T cells appearing in the subarachnoid space of rats with autoimmune encephalomyelitis. Eur J Immunol 26: 1328-1334.
30. McMenamin PG, Wealthall RJ, Deverall M, Cooper SJ, Griffin B. 2003. Macrophages and dendritic cells in the rat meninges and choroid plexus: Three-dimensional localisation by environmental scanning electron microscopy and confocal microscopy. Cell Tissue Res 313: 259-269.
31. Muja N, Bulte JWM. 2009. Magnetic resonance imaging of cells in experimental disease models. Prog Nucl Magn Reson Spectrosc 55: 61-77.
32. Muja N, Cohen ME, Zhang JY, Kim H, Gilad AA, Walczak P, Ben-Hur T, Bulte JWM. 2011. Neural precursors exhibit distinctly different patterns of cell migration upon transplantation during either the acute or chronic phase of EAE: A serial MR imaging study. Magn Reson Med 65: 1738-1749.
33. Neri M, Maderna C, Cavazzin C, Deidda-Vigoriti V, Politi LS, Scotti G, Marzola P, Sbarbati A, Vescovi AL, Gritti A. 2008. Efficient in vitro labeling of human neural precursor cells with superparamagnetic iron oxide particles: Relevance for in vivo cell tracking. Stem Cells 26: 505-516.
34. Ourednik V, Ourednik J, Xu YF, Zhang Y, Lynch WP, Snyder EY, Schachner M. 2009. Cross-talk between stem cells and the dysfunctional brain is facilitated by manipulating the niche: Evidence from an adhesion molecule. Stem Cells 27: 2846-2856.
35. Payne N, Siatskas C, Bernard CCA. 2008. The promise of stem cell and regenerative therapies for multiple sclerosis. J Autoimmun 31: 288-294.
36. Pluchino S, Quattrini A, Brambilla E, Gritti A, Salani G, Dina G, Galli R, Del Carro U, Amadio S, Bergami A, Furlan R, Comi Gy, Vescovi AL, Martino G. 2003. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422: 688-694.
37. 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 JM, Comi G, Manfredi AA, Martino G. 2009. Immune regulatory neural stem/precursor cells protect from central nervous system autoimmunity by restraining dendritic cell function. PLoS One 4: e5959.
38. Polfliet MMJ, van de Veerdonk F, Dopp EA, van Kesteren-Hendrikx EML, van Rooijen N, Dijkstra CD, van den Berg TK. 2002. The role of perivascular and meningeal macrophages in experimental allergic encephalomyelitis. J Neuroimmunol 122: 1-8.
39. Politi LS, Bacigaluppi M, Brambilla E, Cadioli M, Falini A, Comi G, Scotti G, Martino G, Pluchino S. 2007. Magnetic-resonance-based tracking and quantification of intravenously injected neural stem cell accumulation in the brains of mice with experimental multiple sclerosis. Stem Cells 25: 2583-2592.
40. Rampon C, Weiss N, Deboux C, Chaverot N, Miller F, Buchet D, Tricoire-Leignel H, Cazaubon S, Evercooren ABV, Couraud PO. 2008. 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.
41. Ransohoff RM, Kivisakk P, Kidd G. 2003. Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol 3: 569-581.
42. Redzic ZB, Preston JE, Duncan JA, Chodobski A, Szmydynger-Chodobska J. 2005. The choroid plexus-cerebrospinal fluid system: From development to aging. Curr Top Dev Biol 71: 1-52.
43. Sandrock RW, Wheatley W, Levinthal C, Lawson J, Hashimoto B, Rao M, Campanelli JT. 2010. Isolation, characterization and preclinical development of human glial-restricted progenitor cells for treatment of neurological disorders. Regen Med 5: 381-394.
44. Steinman L. 2001. Multiple sclerosis: A two-stage disease. Nat Immunol 2: 762-764.
45. Sweeney TJ, Mailander V, Tucker AA, Olomu AB, Zhang W, Cao Y, Negrin RS, Contag CH. 1999. Visualizing the kinetics of tumor-cell clearance in living animals. Proc Natl Acad Sci USA 96: 12044- 12049.
46. Takahashi K, Prinz M, Stagi M, Chechneva O, Neumann H. 2007. TREM2-transduced myeloid precursors mediate nervous tissue debris clearance and facilitate recovery in an animal model of multiple sclerosis. PLoS Med 4: e124.
47. Walczak P, All AH, Rumpal N, Gorelik M, Kim H, Maybhate A, Agrawal G, Campanelli JT, Gilad AA, Kerr DA, Bulte JW. 2011. Human glial-restricted progenitors survive, proliferate, and preserve electrophysiological function in rats with focal inflammatory spinal cord demyelination. Glia 59: 499-510.
48. Windrem MS, Nunes MC, Rashbaum WK, Schwartz TH, Goodman RA, McKhann GII, Roy NS, Goldman SA. 2004. Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dysmyelinated brain. Nat Med 10: 93-97.
49. Windrem MS, Schanz SJ, Guo M, Tian GF, Washco V, Stanwood N, Rasband M, Roy NS, Nedergaard M, Havton LA, Wang S, Goldman SA. 2008. Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2: 553-565.
50. Zhang Y, Huang P, Du G, Kanaho Y, Frohman MA, Tsirka SE. 2004. Increased expression of two phospholipase D isoforms during experimentally induced hippocampal mossy fiber outgrowth. Glia 46: 74-83.