Transplanted neurally modified bone marrow-derived mesenchymal stem cells promote tissue protection and locomotor recovery in spinal cord injured rats

Neurorehabilitation and Neural Repair

Volumn 25, Issue 9, 2011, Pages 873-880

  Alexanian, Arshak R ^a   Fehlings, Michael G ^b   Zhang, Zhiying ^a   Maiman, Dennis J ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

epigenetics; mesenchymal stem cells; neural transplantation; regeneration; spinal cord injury

Indexed keywords

CYCLIC AMP; ENROFLOXACIN; PHOSPHATE BUFFERED SALINE; TACROLIMUS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; DEACETYLATION; DNA METHYLATION; FEMALE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; RAT; SINGLE DRUG DOSE; SPINAL CORD INJURY; SPRAGUE DAWLEY RAT; STEREOLOGY; TISSUE REPAIR;

ANIMALS; BONE MARROW TRANSPLANTATION; FEMALE; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; NEUROGENESIS; PARALYSIS; PRIMARY CELL CULTURE; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD INJURIES; TRANSPLANTATION, HETEROLOGOUS; TREATMENT OUTCOME;

EID: 80054030150     PISSN: 15459683     EISSN: 15526844     Source Type: Journal    
DOI: 10.1177/1545968311416823     Document Type: Article

References (43)

1. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997 ; 276: 71-74 (Pubitemid 27161245)
2. Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng.. 2001 ; 7: 211-28 (Pubitemid 32295155)
3. Lee OK, Kuo TK, Chen WM, Lee KD, Hsieh SL, Chen TH. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood. 2004 ; 10: 1669-1675 (Pubitemid 38268958)
4. Moloney TC, Dockery P, Windebank AJ, Barry FP, Howard L, Dowd E. Survival and immunogenicity of mesenchymal stem cells from the green fluorescent protein transgenic rat in the adult rat brain. Neurorehabil Neural Repair. 2010 ; 24: 645-656
5. Pereira RF, O'Hara MD, Laptev AV, et al. Marrow stromal cells as a source of progenitor cells for nonhematopoietic tissues in transgenic mice with a phenotype of osteogenesis imperfecta. Proc Natl Acad Sci U S A. 1998 ; 95: 1142-1147 (Pubitemid 28124926)
6. Umezawa A, Tachibana K, Harigaya K, et al. Colony-stimulating factor 1 expression is down-regulated during the adipocyte differentiation of H-1/A marrow stromal cells and induced by cachectin/tumor necrosis factor. Mol Cell Biol.. 1991 ; 11: 920-927 (Pubitemid 21895441)
7. Ferrari G, Cusella-De Angelis G, Coletta M, et al. Muscle regeneration by bone marrow-derived myogenic progenitors. Science. 1998 ; 279: 1528-1530 (Pubitemid 28217075)
8. Dobrossy M, Bussee M, Piroth T, Rosser A, Dunnett S, Nikkhah G. Neurorehabilitation with neural transplantation. Neurorehabil Neural Repair. 2010 ; 24: 692-701
9. Kohyama J, Abe H, Shimazaki T, et al. Brain from bone: efficient "meta-differentiation" of marrow stroma-derived mature osteoblasts to neurons with Noggin or a demethylating agent. Differentiation. 2001 ; 68: 235-244 (Pubitemid 33754996)
10. Jiang Y, Henderson D, Blackstad M, Chen A, Miller RF, Verfaillie CM. Neuroectodermal differentiation from mouse multipotent adult progenitor cells. Proc Natl Acad Sci U S A. 2003 ; 100 (suppl 1). 11854-11860 (Pubitemid 37205895)
11. Bonilla S, Silva A, Valdes L, Geijo E, Garcia-Verdugo JM, Martinez S. Functional neural stem cells derived from adult bone marrow. Neuroscience. 2005 ; 133: 85-95 (Pubitemid 40694160)
12. Kim SS, Yoo SW, Park TS, et al. Neural induction with neurogenin1 increases the therapeutic effects of mesenchymal stem cells in the ischemic brain. Stem Cells. 2008 ; 26: 2217-2228
13. Trzaska KA, King CC, Li KY, et al. Brain-derived neurotrophic factor facilitates maturation of mesenchymal stem cell-derived dopamine progenitors to functional neurons. J Neurochem. 2009 ; 110: 1058-1069
14. Alexanian AR, Maiman DJ, Kurpad SN, Gennarelli TA. In vitro and in vivo characterization of neurally modified mesenchymal stem cells induced by epigenetic modifiers and neural stem cell environment. Stem Cells Dev.. 2008 ; 17: 1123-1130
15. Wislet-Gendebien S, Hans G, Leprince P, Rigo JM, Moonen G, Rogister B. Plasticity of cultured mesenchymal stem cells: switch from nestin-positive to excitable neuron-like phenotype. Stem Cells. 2005 ; 23: 392-402 (Pubitemid 40404458)
16. Hermann A, Gastl R, Liebau S, et al. Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J Cell Sci.. 2004 ; 117 (pt 19). 4411-4422 (Pubitemid 39360068)
17. Chen J, Li Y, Wang L, et al. Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke. 2001 ; 32: 1005-1011 (Pubitemid 32285175)
18. Chopp M, Zhang XH, Li Y, et al. Spinal cord injury in rat: treatment with bone marrow stromal cell transplantation. Neuro-report. 2000 ; 11: 3001-3005
19. Kishk NA, Gabr H, Hamdy S, et al. Case control series of intrathecal autologous bone marrow mesenchymal stem cell therapy for chronic spinal cord injury. Neurorehabil Neural Repair. 2101 ; 24: 702-708
20. Sasaki M, Honmou O, Akiyama Y, Uede T, Hashi K, Kocsis JD. Transplantation of an acutely isolated bone marrow fraction repairs demyelinated adult rat spinal cord axons. Glia. 2001 ; 35: 26-34 (Pubitemid 32656750)
21. Alexanian AR. An efficient method for generation of neural-like cells from adult human bone marrow-derived mesenchymal stem cells. Regen Med.. 2010 ; 5: 891-900
22. Basso DM, Beattie MS, Bresnahan JC. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neuro-trauma. 1995 ; 12: 1-21
23. Bennett AD, Chastain KM, Hulsebosch CE. Alleviation of mechanical and thermal allodynia by CGRP(8-37) in a rodent model of chronic central pain. Pain. 2000 ; 86: 163-175 (Pubitemid 30211715)
24. Hains BC, Johnson KM, Eaton MJ, Willis WD, Hulsebosch CE. Serotonergic neural precursor cell grafts attenuate bilateral hyperexcitability of dorsal horn neurons after spinal hemisection in rat. Neuroscience. 2003 ; 116: 1097-1110 (Pubitemid 36262968)
25. Page KM. A stain for myelin using solochrome cyanin. J Med Lab Technol. 1965 ; 22: 224-225
26. Ankeny DP, McTigue DM, Jakeman LB. Bone marrow transplants provide tissue protection and directional guidance for axons after contusive spinal cord injury in rats. Exp Neurol.. 2004 ; 190: 17-31 (Pubitemid 39335703)
27. Stroemer P, Patel S, Hope A, Oliveira C, Pollock K, Sinden J. The neural stem cell line CTX0E03 promotes behavioral recovery and endogenous neurogenesis after experimental stroke in a dose-dependent fashion. Neurorehabil Neural Repair. 2009 ; 23: 895-909
28. Tetzlaff W, Okon E, Karimi-Abolrezaee S, et al. A systematic review of cellular transplantation therapies for spinal cord injury. J Neurotrauma. 2011 ; 28: 1611-1682
29. Lima C, Escada P, Pratas-Vital J, et al. Olfactory mucosal autografts and rehabilitation for chronic traumatic spinal cord injury. Neurorehabil Neural Repair. 2010 ; 24: 10-22
30. Kim SS, Choi JM, Kim JW, et al. cAMP induces neuronal differentiation of mesenchymal stem cells via activation of extracellular signal-regulated kinase/MAPK. Neuroreport. 2005 ; 16: 1357-1361
31. Sanchez-Ramos J, Song S, Cardozo-Pelaez F, et al. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol.. 2000 ; 164: 247-256 (Pubitemid 32008970)
32. Kim BJ, Seo JH, Bubien JK, Oh YS. Differentiation of adult bone marrow stem cells into neuroprogenitor cells in vitro. Neuroreport. 2002 ; 13: 1185-1188 (Pubitemid 34722050)
33. Kondo T, Johnson SA, Yoder MC, Romand R, Hashino E. Sonic hedgehog and retinoic acid synergistically promote sensory fate specification from bone marrow-derived pluripotent stem cells. Proc Natl Acad Sci U S A. 2005 ; 102: 4789-4794 (Pubitemid 40471532)
34. Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM. Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron. 2005 ; 45: 675-688 (Pubitemid 40320703)
35. Long X, Olszewski M, Huang W, Kletzel M. Neural cell differentiation in vitro from adult human bone marrow mesenchymal stem cells. Stem Cells Dev.. 2005 ; 14: 65-69 (Pubitemid 40328249)
36. Lu P, Blesch A, Tuszynski MH. Induction of bone marrow stromal cells to neurons: differentiation, transdifferentiation, or artifact?. J Neurosci Res.. 2004 ; 77: 174-191 (Pubitemid 38859403)
37. Yang XS, Wu HX, Xiao B. Human mesenchymal stem cells differentiate into neuron-like cells and show SMN protein expression [in Chinese]. Zhonghua Yi Xue Za Zhi. 2005 ; 85: 1125-1128 (Pubitemid 40867356)
38. Munoz-Elias G, Woodbury D, Black IB. Marrow stromal cells, mitosis, and neuronal differentiation: stem cell and precursor functions. Stem Cells. 2003 ; 21: 437-448 (Pubitemid 36793486)
39. Deng W, Obrocka M, Fischer I, Prockop DJ. In vitro differentiation of human marrow stromal cells into early progenitors of neural cells by conditions that increase intracellular cyclic AMP. Biochem Biophys Res Commun.. 2001 ; 282: 148-152 (Pubitemid 32924357)
40. Qian L, Saltzman WM. Improving the expansion and neuronal differentiation of mesenchymal stem cells through culture surface modification. Biomaterials. 2004 ; 25: 1331-1337 (Pubitemid 37476209)
41. Alexanian AR. Neural stem cells induce bone-marrow-derived mesenchymal stem cells to generate neural stem-like cells via juxtacrine and paracrine interactions. Exp Cell Res.. 2005 ; 310: 383-391 (Pubitemid 41457341)
42. Qu TY, Dong XJ, Sugaya I, Vaghani A, Pulido J, Sugaya K. Bromodeoxyuridine increases multipotency of human bone marrow-derived stem cells. Restor Neurol Neurosci. 2004 ; 22: 459-468 (Pubitemid 40529081)
43. Dezawa M, Kanno H, Hoshino M, et al. Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation. J Clin Invest.. 2004 ; 113: 1701-1710 (Pubitemid 39071662)