Human glial-restricted progenitors survive, proliferate, and preserve electrophysiological function in rats with focal inflammatory spinal cord demyelination

GLIA

Volumn 59, Issue 3, 2011, Pages 499-510

  Walczak, Piotr ^a   All, Angelo H ^a   Rumpal, Nidhi ^a   Gorelik, Michael ^a   Kim, Heechul ^a   Maybhate, Anil ^a   Agrawal, Gracee ^a   Campanelli, James T ^b   Gilad, Assaf A ^a   Kerr, Douglas A ^a   Bulte, Jeff W M ^a  

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

^b Q Therapeutics Inc   (United States)

Author keywords

Electrophysiology; Glial precursors; Myelination; Spinal cord; Transplantation

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; CELL FATE; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSPLANTATION; DEMYELINATION; ELECTROPHYSIOLOGY; GLIA CELL; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; MOUSE; NONHUMAN; PHENOTYPE; PHYSIOLOGY; PRIORITY JOURNAL; RAT; REMYELINIZATION; SPINAL CORD; SPINAL CORD LESION; STEM CELL;

ANIMALS; ANIMALS, NEWBORN; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DEMYELINATING DISEASES; FEMALE; GRAFT SURVIVAL; HUMANS; INFLAMMATION MEDIATORS; MICE; MICE, KNOCKOUT; MICE, NEUROLOGIC MUTANTS; MYELITIS; NEUROGLIA; RATS; RATS, INBRED LEW; RECOVERY OF FUNCTION; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 78751683373     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21119     Document Type: Article

References (34)

1. Abbott NJ, Ronnback L, Hansson E. 2006. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7: 41-53.
2. All AH, Walczak P, Agrawal G, Gorelik M, Lee C, Thakor NV, Bulte JW, Kerr DA. 2009. Effect of MOG sensitization on somatosensory evoked potential in Lewis rats. J Neurol Sci 284: 81-89.
3. Baumann N, Pham-Dinh D. 2001. Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81: 871-927.
4. Beattie MS, Harrington AW, Lee R, Kim JY, Boyce SL, Longo FM, Bresnahan JC, Hempstead BL, Yoon SO. 2002. ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 36: 375-386.
5. Chang A, Nishiyama A, Peterson J, Prineas J, Trapp BD. 2000. NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci 20: 6404-6412.
6. 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.
7. Goldman S. 2005. Stem and progenitor cell-based therapy of the human central nervous system. Nat Biotechnol 23: 862-871.
8. Gregori N, Proschel C, Noble M, Mayer-Proschel M. 2002. The tripotential glial-restricted precursor (GRP) cell and glial development in the spinal cord: Generation of bipotential oligodendrocyte-type-2 astrocyte progenitor cells and dorsal-ventral differences in GRP cell function. J Neurosci 22: 248-256.
9. Gumpel M, Lachapelle F, Gansmuller A, Baulac M, Baron van Evercooren A, Baumann N. 1987. Transplantation of human embryonic oligodendrocytes into shiverer brain. Ann N Y Acad Sci 495: 71-85.
10. Han SS, Liu Y, Tyler-Polsz C, Rao MS, Fischer I. 2004. Transplantation of glial-restricted precursor cells into the adult spinal cord: Survival, glial-specific differentiation, and preferential migration in white matter. Glia 45: 1-16.
11. Iannotti C, Li H, Yan P, Lu X, Wirthlin L, Xu XM. 2003. Glial cell line-derived neurotrophic factor-enriched bridging transplants promote propriospinal axonal regeneration and enhance myelination after spinal cord injury. Exp Neurol 183: 379-393.
12. Jacobs LD, Cookfair DL, Rudick RA, Herndon RM, Richert JR, Salazar AM, Fischer JS, Goodkin DE, Granger CV, Simon JH, Alam JJ, Bartoszak DM, Bourdette DN, Braiman J, Brownscheidle CM, Coats ME, Cohan SL, Dougherty DS, Kinkel RP, Mass MK, Munschauer FE, 3rd, Priore RL, Pullicino PM, Scherokman BJ, Whitham RH. 1996. Intramuscular interferon beta-1a for disease progression in relapsing multiple sclerosis. The Multiple Sclerosis Collaborative Research Group (MSCRG). Ann Neurol 39: 285-294.
13. Janowski M, Walczak P, Date I. 2010. Intravenous route of cell delivery for treatment of neurological disorders. A meta-analysis of preclinical results. Stem Cells Dev 19: 5-16.
14. Kazatchkine MD, Kaveri SV. 2001. Immunomodulation of autoimmune and inflammatory diseases with intravenous immune globulin. N Engl J Med 345: 747-755.
15. 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(19): 4694-705.
16. Kerr DA, Ayetey H. 2002. Immunopathogenesis of acute transverse myelitis. Curr Opin Neurol 15: 339-347.
17. Kerschensteiner M, Stadelmann C, Buddeberg BS, Merkler D, Bareyre FM, Anthony DC, Linington C, Bruck W, Schwab ME. 2004. Targeting experimental autoimmune encephalomyelitis lesions to a predetermined axonal tract system allows for refined behavioral testing in an animal model of multiple sclerosis. Am J Pathol 164: 1455-1469.
18. Krishnan C, Kaplin AI, Pardo CA, Kerr DA, Keswani SC. 2006. Demyelinating disorders: Update on transverse myelitis. Curr Neurol Neurosci Rep 6: 236-243.
19. Lucchinetti CF, Brueck W, Rodriguez M, Lassmann H. 1998. Multiple sclerosis: Lessons from neuropathology. Semin Neurol 18: 337-349.
20. Maragakis NJ, Rao MS, Llado J, Wong V, Xue H, Pardo A, Herring J, Kerr D, Coccia C, Rothstein JD. 2005. Glial restricted precursors protect against chronic glutamate neurotoxicity of motor neurons in vitro. Glia 50: 145-159.
21. Mothe AJ, Tator CH. 2008. Transplanted neural stem/progenitor cells generate myelinating oligodendrocytes and Schwann cells in spinal cord demyelination and dysmyelination. Exp Neurol 213: 176-190.
22. Murray JA, Blakemore WF. 1980. The relationship between internodal length and fibre diameter in the spinal cord of the cat. J Neurol Sci 45: 29-41.
23. Narayanan SP, Flores AI, Wang F, Macklin WB. 2009. Akt signals through the mammalian target of rapamycin pathway to regulate CNS myelination. J Neurosci 29: 6860-6870.
24. Raine CS. 1997. The Norton Lecture: A review of the oligodendrocyte in the multiple sclerosis lesion. J Neuroimmunol 77: 135-152.
25. Rao MS, Noble M, Mayer-Proschel M. 1998. A tripotential glial precursor cell is present in the developing spinal cord. Proc Natl Acad Sci USA 95: 3996-4001.
26. Saito M, Kitamura H, Sugiyama K. 2001. The specificity of monoclonal antibody A2B5 to c-series gangliosides. J Neurochem 78: 64-74.
27. 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.
28. Setzu A, Lathia JD, Zhao C, Wells K, Rao MS, Ffrench-Constant C, Franklin RJ. 2006. Inflammation stimulates myelination by transplanted oligodendrocyte precursor cells. Glia 54: 297-303.
29. Talbott JF, Cao Q, Enzmann GU, Benton RL, Achim V, Cheng XX, Mills MD, Rao MS, Whittemore SR. 2006. Schwann cell-like differentiation by adult oligodendrocyte precursor cells following engraftment into the demyelinated spinal cord is BMP-dependent. Glia 54: 147-159.
30. Talbott JF, Loy DN, Liu Y, Qiu MS, Bunge MB, Rao MS, Whittemore SR. 2005. Endogenous Nkx2.2+/Olig2+ oligodendrocyte precursor cells fail to remyelinate the demyelinated adult rat spinal cord in the absence of astrocytes. Exp Neurol 192: 11-24.
31. Tyler WA, Gangoli N, Gokina P, Kim HA, Covey M, Levison SW, Wood TL. 2009. Activation of the mammalian target of rapamycin (mTOR) is essential for oligodendrocyte differentiation. J Neurosci 29: 6367-6378.
32. Walczak P, Kedziorek DA, Gilad AA, Barnett BP, Bulte JW. 2007. Applicability and limitations of MR tracking of neural stem cells with asymmetric cell division and rapid turnover: The case of the shiverer dysmyelinated mouse brain. Magn Reson Med 58: 261-269.
33. Walczak P, Zhang J, Gilad AA, Kedziorek DA, Ruiz-Cabello J, Young RG, Pittenger MF, van Zijl PC, Huang J, Bulte JW. 2008. Dual-modality monitoring of targeted intraarterial delivery of mesenchymal stem cells after transient ischemia. Stroke 39: 1569-1574.
34. 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.