Human mesenchymal stem cell-derived Schwann cell-like cells exhibit neurotrophic effects, via distinct growth factor production, in a model of spinal cord injury

GLIA

Volumn 58, Issue 9, 2010, Pages 1118-1132

  Park, Hwan Woo ^a   Lim, Mi Jin ^a   Jung, Heekyung ^a   Lee, Seung Pyo ^a   Paik, Ki Suk ^a   Chang, Mi Sook ^a  

^a Seoul National University   (South Korea)

Author keywords

Adult stem cells; Nerve regeneration; Nervous system; Neurotrophic factors; Transplantation

Indexed keywords

DNA; GROWTH FACTOR; NEUROTROPHIN RECEPTOR P75; SCATTER FACTOR; VASCULOTROPIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CYCLE; CELL DEATH; CELL PROLIFERATION; CELL STRUCTURE; CELL THERAPY; CONTROLLED STUDY; DNA MODIFICATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; RAT; SCHWANN CELL; SPINAL CORD INJURY;

ANIMALS; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CELL LINE; COCULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; NERVE REGENERATION; RATS; RATS, SPRAGUE-DAWLEY; SCHWANN CELLS; SPINAL CORD INJURIES;

EID: 77954413328     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20992     Document Type: Article

References (58)

1. Bianco P, Riminucci M, Gronthos S, Robey PG. 2001. Bone marrow stromal stem cells: Nature, biology, and potential applications. Stem Cells 19:180-192. (Pubitemid 32524539)
2. Biernaskie J, Sparling JS, Liu J, Shannon CP, Plemel JR, Xie Y, Miller FD, Tetzlaff W. 2007. Skin-derived precursors generate myelinating Schwann cells that promote remyelination and functional recovery after contusion spinal cord injury. J Neurosci 27:9545-9559.
3. Brohlin M, Mahay D, Novikov LN, Terenghi G, Wiberg M, Shawcross SG, Novikova LN. 2009. Characterisation of human mesenchymal stem cells following differentiation into Schwann cell-like cells. Neurosci Res 64:41-49.
4. Bunge MB. 2002. Bridging the transected or contused adult rat spinal cord with Schwann cell and olfactory ensheathing glia transplants. Prog Brain Res 137:275-282.
5. Bunge RP. 1994. The role of the Schwann cell in trophic support and regeneration. J Neurol 242:S19-S21. (Pubitemid 24367035)
6. Caddick J, Kingham PJ, Gardiner NJ, Wiberg M, Terenghi G. 2006. Phenotypic and functional characteristics of mesenchymal stem cells differentiated along a Schwann cell lineage. Glia 54:840-849.
7. Cho JS, Park HW, Park SK, Roh S, Kang SK, Paik KS, Chang MS. 2009. Transplantation of mesenchymal stem cells enhances axonal outgrowth and cell survival in an organotypic spinal cord slice culture. Neurosci Lett 454:43-48.
8. Crigler L, Robey RC, Asawachaicharn A, Gaupp D, Phinney DG. 2006. Human mesenchymal stem cell subpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. Exp Neurol 198:54-64.
9. Delfino-Machin M, Chipperfield TR, Rodrigues FS, Kelsh RN. 2007. The proliferating field of neural crest stem cells. Dev Dyn 236:3242-3254.
10. Dezawa M, Takahashi I, Esaki M, Takano M, Sawada H. 2001. Sciatic nerve regeneration in rats induced by transplantation of in vitro differentiated bone-marrow stromal cells. Eur J Neurosci 14:1771-1776.
11. Ebens A, Brose K, Leonardo ED, Hanson MG, Jr., Bladt F, Birchmeier C, Barres BA, Tessier-Lavigne M. 1996. Hepatocyte growth factor/ scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron 17:1157-1172.
12. Ferrara N, Gerber HP, LeCouter J. 2003. The biology of VEGF and its receptors. Nat Med 9:669-676.
13. Frostick SP, Yin Q, Kemp GJ. 1998. Schwann cells, neurotrophic factors, and peripheral nerve regeneration. Microsurgery 18:397-405. (Pubitemid 29014397)
14. Isakova IA, Baker K, DuTreil M, Dufour J, Gaupp D, Phinney DG. 2007. Age- and dose-related effects on MSC engraftment levels and anatomical distribution in the central nervous systems of nonhuman primates: Identification of novel MSC subpopulations that respond to guidance cues in brain. Stem Cells 25:3261-3270.
15. Jessen KR, Mirsky R. 1999. Schwann cells and their precursors emerge as major regulators of nerve development. Trends Neurosci 22:402-410.
16. Jessen KR, Mirsky R. 2005. The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 6:671-682.
17. Keck PJ, Hauser SD, Krivi G, Sanzo K, Warren T, Feder J, Connolly DT. 1989. Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science 246:1309-1312. (Pubitemid 20066717)
18. Keilhoff G, Goihl A, Langnase K, Fansa H, Wolf G. 2006. Transdifferentiation of mesenchymal stem cells into Schwann cell-like myelinating cells. Eur J Cell Biol 85:11-24. (Pubitemid 43055554)
19. Keirstead HS, Morgan SV, Wilby MJ, Fawcett JW. 1999. Enhanced axonal regeneration following combined demyelination plus schwann cell transplantation therapy in the injured adult spinal cord. Exp Neurol 159:225-236.
20. Kitamura K, Iwanami A, Nakamura M, Yamane J, Watanabe K, Suzuki Y, Miyazawa D, Shibata S, Funakoshi H, Miyatake S, Coffin RS, Nakamura T, Toyama Y, Okano H. 2007. Hepatocyte growth factor promotes endogenous repair and functional recovery after spinal cord injury. J Neurosci Res 85:2332-2342.
21. Krasnoselsky A, Massay MJ, DeFrances MC, Michalopoulos G, Zarnegar R, Ratner N. 1994. Hepatocyte growth factor is a mitogen for Schwann cells and is present in neurofibromas. J Neurosci 14:7284-7290.
22. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. 1989. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246:1306-1309. (Pubitemid 20066716)
23. Lipinski MM, Jacks T. 1999. The retinoblastoma gene family in differentiation and development. Oncogene 18:7873-7882.
24. Mahato RI, Henry J, Narang AS, Sabek O, Fraga D, Kotb M, Gaber AO. 2003. Cationic lipid and polymer-based gene delivery to human pancreatic islets. Mol Ther 7:89-100.
25. Mahay D, Terenghi G, Shawcross SG. 2008. Schwann cell mediated trophic effects by differentiated mesenchymal stem cells. Exp Cell Res 314:2692-2701.
26. Maina F, Hilton MC, Ponzetto C, Davies AM, Klein R. 1997. Met receptor signaling is required for sensory nerve development and HGF promotes axonal growth and survival of sensory neurons. Genes Dev 11:3341-3350.
27. Maina F, Klein R. 1999. Hepatocyte growth factor, a versatile signal for developing neurons. Nat Neurosci 2:213-217.
28. McKenzie IA, Biernaskie J, Toma JG, Midha R, Miller FD. 2006. Skinderived precursors generate myelinating Schwann cells for the injured and dysmyelinated nervous system. J Neurosci 26:6651-6660.
29. Miller FD. 2007. Riding the waves: Neural and nonneural origins for mesenchymal stem cells. Cell Stem Cell 1:129-130. (Pubitemid 47215593)
30. Munoz-Elias G, Woodbury D, Black IB. 2003. Marrow stromal cells, mitosis, and neuronal differentiation: Stem cell and precursor functions. Stem Cells 21:437-448. (Pubitemid 36793486)
31. Nagoshi N, Shibata S, Kubota Y, Nakamura M, Nagai Y, Satoh E, Morikawa S, Okada Y, Mabuchi Y, Katoh H, Okada S, Fukuda K, Suda T, Matsuzaki Y, Toyama Y, Okano H. 2008. Ontogeny and multipotency of neural crest-derived stem cells in mouse bone marrow, dorsal root ganglia, and whisker pad. Cell Stem Cell 2:392-403.
32. Neuhuber B, Gallo G, Howard L, Kostura L, Mackay A, Fischer I. 2004. Reevaluation of in vitro differentiation protocols for bone marrow stromal cells: Disruption of actin cytoskeleton induces rapid morphological changes and mimics neuronal phenotype. J Neurosci Res 77:192-204.
33. Pearse DD, Pereira FC, Marcillo AE, Bates ML, Berrocal YA, Filbin MT, Bunge MB. 2004. cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat Med 10:610-616.
34. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. 1999. Multi-lineage potential of adult human mesenchymal stem cells. Science 284:143-147.
35. Prockop DJ. 1997. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71-74.
36. Prockop DJ. 2007. "Stemness" does not explain the repair of many tissues by mesenchymal stem/multipotent stromal cells (MSCs). Clin Pharmacol Ther 82:241-243.
37. Robinson CJ, Stringer SE. 2001. The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J Cell Sci 114:853-865. (Pubitemid 32273121)
38. Rosenstein JM, Mani N, Khaibullina A, Krum JM. 2003. Neurotrophic effects of vascular endothelial growth factor on organotypic cortical explants and primary cortical neurons. J Neurosci 23:11036-11044.
39. Sanchez-Ramos J, Song S, Cardozo-Pelaez F, Hazzi C, Stedeford T, Willing A, Freeman TB, Saporta S, Janssen W, Patel N, Cooper DR, Sanberg PR. 2000. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol 164:247-256.
40. Schwab JM, Brechtel K, Mueller CA, Failli V, Kaps HP, Tuli SK, Schluesener HJ. 2006. Experimental strategies to promote spinal cord regeneration-an integrative perspective. Prog Neurobiol 78:91-116.
41. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF. 1983. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219:983-985.
42. Shimizu S, Kitada M, Ishikawa H, Itokazu Y, Wakao S, Dezawa M. 2007. Peripheral nerve regeneration by the in vitro differentiatedhuman bone marrow stromal cells with Schwann cell property. Biochem Biophys Res Commun 359:915-920.
43. Sondell M, Lundborg G, Kanje M. 1999a. Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J Neurosci 19:5731-5740. (Pubitemid 29327910)
44. Sondell M, Lundborg G, Kanje M. 1999b. Vascular endothelial growth factor stimulates Schwann cell invasion and neovascularization of acellular nerve grafts. Brain Res 846:219-228.
45. Takami T, Oudega M, Bates ML, Wood PM, Kleitman N, Bunge MB. 2002. Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J Neurosci 22:6670-6681.
46. Takashima Y, Era T, Nakao K, Kondo S, Kasuga M, Smith AG, Nishikawa S. 2007. Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell 129:1377-1388.
47. Tei K, Matsumoto T, Mifune Y, Ishida K, Sasaki K, Shoji T, Kubo S, Kawamoto A, Asahara T, Kurosaka M, Kuroda R. 2008. Administrations of peripheral blood CD34-positive cells contribute to medial collateral ligament healing via vasculogenesis. Stem Cells 26:819-830.
48. Thuret S, Moon LD, Gage FH. 2006. Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 7:628-643.
49. Tohill M, Mantovani C, Wiberg M, Terenghi G. 2004. Rat bone marrow mesenchymal stem cells express glial markers and stimulate nerve regeneration. Neurosci Lett 362:200-203.
50. Trzaska KA, Kuzhikandathil EV, Rameshwar P. 2007. Specification of a dopaminergic phenotype from adult human mesenchymal stem cells. Stem Cells 25:2797-2808. (Pubitemid 350127864)
51. Uchijima M, Nagata T, Aoshi T, Koide Y. 2005. IFN-g overcomes low responsiveness of myeloid dendritic cells to CpG DNA. Immunol Cell Biol 83:92-95.
52. Widenfalk J, Lipson A, Jubran M, Hofstetter C, Ebendal T, Cao Y, Olson L. 2003. Vascular endothelial growth factor improves functional outcome and decreases secondary degeneration in experimental spinal cord contusion injury. Neuroscience 120:951-960.
53. Wong V, Glass DJ, Arriaga R, Yancopoulos GD, Lindsay RM, Conn G. 1997. Hepatocyte growth factor promotes motor neuron survival and synergizes with ciliary neurotrophic factor. J Biol Chem 272:5187-5191.
54. Woodbury D, Schwarz EJ, Prockop DJ, Black IB. 2000. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 61:364-370.
55. Woodhoo A, Sommer L. 2008. Development of the Schwann cell lineage: From the neural crest to the myelinated nerve. Glia 56:1481-1490.
56. Xu XM, Guenard V, Kleitman N, Bunge MB. 1995. Axonal regeneration into Schwann cell-seeded guidance channels grafted into transected adult rat spinal cord. J Comp Neurol 351:145-160.
57. Yang XM, Toma JG, Bamji SX, Belliveau DJ, Kohn J, Park M, Miller FD. 1998. Autocrine hepatocyte growth factor provides a local mechanism for promoting axonal growth. J Neurosci 18:8369-8381. (Pubitemid 28465012)
58. Zachary I. 2005. Neuroprotective role of vascular endothelial growth factor: Signalling mechanisms, biological function, and therapeutic potential. Neurosignals 14:207-221.