Stem cells and spinal cord regeneration

Current Opinion in Biotechnology

Volumn 20, Issue 5, 2009, Pages 552-562

  Rossi, Sharyn L ^a   Keirstead, Hans S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL-BASED; COMBINATION THERAPY; EXPRESSION PROFILE; GROWTH FACTOR; HIGH PURITY; INJURED SPINAL CORDS; MICROENVIRONMENTS; NEUROPROTECTION; NEUROTROPHIC; SPINAL CORDS; STEM CELL; TRANSPLANTED CELLS;

CELLS;

DOSIMETRY;

BONE MARROW TRANSPLANTATION; CELL DIFFERENTIATION; CELL LINEAGE; CELL MANIPULATION; CELL SURVIVAL; EMBRYONIC STEM CELL; HUMAN; MESENCHYMAL STEM CELL TRANSPLANTATION; NERVE CELL PLASTICITY; NEURAL STEM CELL; NEUROPROTECTION; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REMYELINIZATION; REVIEW; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; STEM CELL TRANSPLANTATION; TISSUE REGENERATION; TISSUE REPAIR;

ANIMALS; HUMANS; NERVE REGENERATION; SPINAL CORD; SPINAL CORD INJURIES; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 70449807650     PISSN: 09581669     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.copbio.2009.09.008     Document Type: Review

References (66)

1. Popovich P.G., Horner P.J., Mullin B.B., and Stokes B.T. A quantitative spatial analysis of the blood-spinal cord barrier. I. Permeability changes after experimental spinal contusion injury. Exp Neurol 142 (1996) 258-275
2. Loy D.N., Crawford C.H., Darnall J.B., Burke D.A., Onifer S.M., and Whittemore S.R. Temporal progression of angiogenesis and basal lamina deposition after contusive spinal cord injury in the adult rat. J Comp Neurol 445 (2002) 308-324
3. Goolsby J., Marty M.C., Heletz D., Chiappelli J., Tashko G., Yarnell D., Fishman P.S., Dhib-Jalbut S., Bever Jr. C.T., Pessac B., et al. Hematopoietic progenitors express neural genes. Proc Natl Acad Sci U S A 100 (2003) 14926-14931
4. Andrews E.M., Tsai S.Y., Johnson S.C., Farrer J.R., Wagner J.P., Kopen G.C., and Kartje G.L. Human adult bone marrow-derived somatic cell therapy results in functional recovery and axonal plasticity following stroke in the rat. Exp Neurol 211 (2008) 588-592
5. Chopp M., Zhang X.H., Li Y., Wang L., Chen J., Lu D., Lu M., and Rosenblum M. Spinal cord injury in rat: treatment with bone marrow stromal cell transplantation. Neuroreport 11 (2000) 3001-3005
6. Cizkova D., Rosocha J., Vanicky I., Jergova S., and Cizek M. Transplants of human mesenchymal stem cells improve functional recovery after spinal cord injury in the rat. Cell Mol Neurobiol 26 (2006) 1165-1178
7. Himes B.T., Neuhuber B., Coleman C., Kushner R., Swanger S.A., Kopen G.C., Wagner J., Shumsky J.S., and Fischer I. Recovery of function following grafting of human bone marrow-derived stromal cells into the injured spinal cord. Neurorehabil Neural Repair 20 (2006) 278-296
8. Hofstetter C.P., Schwarz E.J., Hess D., Widenfalk J., El Manira A., Prockop D.J., and Olson L. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci U S A 99 (2002) 2199-2204
9. Sykova E., and Jendelova P. Magnetic resonance tracking of implanted adult and embryonic stem cells in injured brain and spinal cord. Ann N Y Acad Sci 1049 (2005) 146-160
10. Yoon S.H., Shim Y.S., Park Y.H., Chung J.K., Nam J.H., Kim M.O., Park H.C., Park S.R., Min B.H., Kim E.Y., et al. Complete spinal cord injury treatment using autologous bone marrow cell transplantation and bone marrow stimulation with granulocyte macrophage-colony stimulating factor: phase I/II clinical trial. Stem Cells 25 (2007) 2066-2073
11. Callera F., and do Nascimento R.X. Delivery of autologous bone marrow precursor cells into the spinal cord via lumbar puncture technique in patients with spinal cord injury: a preliminary safety study. Exp Hematol 34 (2006) 130-131
12. Chen Q., Long Y., Yuan X., Zou L., Sun J., Chen S., Perez-Polo J.R., and Yang K. Protective effects of bone marrow stromal cell transplantation in injured rodent brain: synthesis of neurotrophic factors. J Neurosci Res 80 (2005) 611-619
13. Yaghoobi M.M., and Mowla S.J. Differential gene expression pattern of neurotrophins and their receptors during neuronal differentiation of rat bone marrow stromal cells. Neurosci Lett 397 (2006) 149-154
14. Neuhuber B., Timothy Himes B., Shumsky J.S., Gallo G., and Fischer I. Axon growth and recovery of function supported by human bone marrow stromal cells in the injured spinal cord exhibit donor variations. Brain Res 1035 (2005) 73-85
15. Chen X., Li Y., Wang L., Katakowski M., Zhang L., Chen J., Xu Y., Gautam S.C., and Chopp M. Ischemic rat brain extracts induce human marrow stromal cell growth factor production. Neuropathology 22 (2002) 275-279
16. Zhou C., Zhang C., Chi S., Xu Y., Teng J., Wang H., Song Y., and Zhao R. Effects of human marrow stromal cells on activation of microglial cells and production of inflammatory factors induced by lipopolysaccharide. Brain Res 1269 (2009) 23-30
17. Schinkothe T., Bloch W., and Schmidt A. In vitro secreting profile of human mesenchymal stem cells. Stem Cells Dev 17 (2008) 199-206
18. Ankeny D.P., McTigue D.M., and Jakeman L.B. Bone marrow transplants provide tissue protection and directional guidance for axons after contusive spinal cord injury in rats. Exp Neurol 190 (2004) 17-31
19. Wu S., Suzuki Y., Ejiri Y., Noda T., Bai H., Kitada M., Kataoka K., Ohta M., Chou H., and Ide C. Bone marrow stromal cells enhance differentiation of cocultured neurosphere cells and promote regeneration of injured spinal cord. J Neurosci Res 72 (2003) 343-351
20. Opatz J., Kury P., Schiwy N., Jarve A., Estrada V., Brazda N., Bosse F., and Muller H.W. SDF-1 stimulates neurite growth on inhibitory CNS myelin. Mol Cell Neurosci 40 (2009) 293-300
21. Wright K.T., El Masri W., Osman A., Roberts S., Chamberlain G., Ashton B.A., and Johnson W.E.B. Bone marrow stromal cells stimulate neurite outgrowth over neural proteoglycans (CSPG), myelin associated glycoprotein and Nogo-A. Biochem Biophys Res Commun 354 (2007) 559-566
22. Gerdoni E., Gallo B., Casazza S., Musio S., Bonanni I., Pedemonte E., Mantegazza R., Frassoni F., Mancardi G., Pedotti R., et al. Mesenchymal stem cells effectively modulate pathogenic immune response in experimental autoimmune encephalomyelitis. Ann Neurol 61 (2007) 219-227
23. Zappia E., Casazza S., Pedemonte E., Benvenuto F., Bonanni I., Gerdoni E., Giunti D., Ceravolo A., Cazzanti F., Frassoni F., et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 106 (2005) 1755-1761
24. Rafei M., Hsieh J., Fortier S., Li M., Yuan S., Birman E., Forner K., Boivin M.N., Doody K., Tremblay M., et al. Mesenchymal stromal cell-derived CCL2 suppresses plasma cell immunoglobulin production via STAT3 inactivation and PAX5 induction. Blood 112 (2008) 4991-4998
25. Rafei M., Campeau P.M., Aguilar-Mahecha A., Buchanan M., Williams P., Birman E., Yuan S., Young Y.K., Boivin M.-N., Forner K., et al. Mesenchymal Stromal Cells Ameliorate Experimental Autoimmune Encephalomyelitis by Inhibiting CD4 Th17 T Cells in a CC Chemokine Ligand 2-Dependent Manner. J Immunol 182 (2009) 5994-6002
26. Matysiak M., Stasiolek M., Orlowski W., Jurewicz A., Janczar S., Raine C.S., and Selmaj K. Stem cells ameliorate EAE via an indoleamine 2,3-dioxygenase (IDO) mechanism. J Neuroimmunol 193 (2008) 12-23
27. Zhang J., Brodie C., Li Y., Zheng X., Roberts C., Lu M., Gao Q., Borneman J., Savant-Bhonsale S., Elias S.B., et al. Bone marrow stromal cell therapy reduces proNGF and p75 expression in mice with experimental autoimmune encephalomyelitis. J Neurol Sci 279 (2009) 30-38
28. Vercelli A., Mereuta O.M., Garbossa D., Muraca G., Mareschi K., Rustichelli D., Ferrero I., Mazzini L., Madon E., and Fagioli F. Human mesenchymal stem cell transplantation extends survival, improves motor performance and decreases neuroinflammation in mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 31 (2008) 395-405
29. Zhang C., Zhou C., Teng J.J., Zhao R.L., and Song Y.Q. Multiple administrations of human marrow stromal cells through cerebrospinal fluid prolong survival in a transgenic mouse model of amyotrophic lateral sclerosis. Cytotherapy 11 (2009) 299-306
30. Webber D.J., Bradbury E.J., McMahon S.B., and Minger S.L. Transplanted neural progenitor cells survive and differentiate but achieve limited functional recovery in the lesioned adult rat spinal cord. Regen Med 2 (2007) 929-945
31. Cummings B.J., Uchida N., Tamaki S.J., Salazar D.L., Hooshmand M., Summers R., Gage F.H., and Anderson A.J. Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc Natl Acad Sci U S A 102 (2005) 14069-14074
32. Vroemen M., Aigner L., Winkler J., and Weidner N. Adult neural progenitor cell grafts survive after acute spinal cord injury and integrate along axonal pathways. Eur J Neurosci 18 (2003) 743-751
33. Cao Q.L., Howard R.M., Dennison J.B., and Whittemore S.R. Differentiation of engrafted neuronal-restricted precursor cells is inhibited in the traumatically injured spinal cord. Exp Neurol 177 (2002) 349-359
34. Cao Q.L., Zhang Y.P., Howard R.M., Walters W.M., Tsoulfas P., and Whittemore S.R. Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. Exp Neurol 167 (2001) 48-58
35. Hofstetter C.P., Holmstrom N.A., Lilja J.A., Schweinhardt P., Hao J., Spenger C., Wiesenfeld-Hallin Z., Kurpad S.N., Frisen J., and Olson L. Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat Neurosci 8 (2005) 346-353
36. Yan J., Welsh A.M., Bora S.H., Snyder E.Y., and Koliatsos V.E. Differentiation and tropic/trophic effects of exogenous neural precursors in the adult spinal cord. J Comp Neurol 480 (2004) 101-114
37. Lu P., Jones L.L., Snyder E.Y., and Tuszynski M.H. Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp Neurol 181 (2003) 115-129
38. Llado J., Haenggeli C., Maragakis N.J., Snyder E.Y., and Rothstein J.D. Neural stem cells protect against glutamate-induced excitotoxicity and promote survival of injured motor neurons through the secretion of neurotrophic factors. Mol Cell Neurosci 27 (2004) 322-331
39. Ziv Y., Avidan H., Pluchino S., Martino G., and Schwartz M. Synergy between immune cells and adult neural stem/progenitor cells promotes functional recovery from spinal cord injury. Proc Natl Acad Sci U S A 103 (2006) 13174-13179
40. Xu L., Yan J., Chen D., Welsh A.M., Hazel T., Johe K., Hatfield G., and Koliatsos V.E. Human neural stem cell grafts ameliorate motor neuron disease in SOD-1 transgenic rats. Transplantation 82 (2006) 865-875
41. Corti S., Locatelli F., Papadimitriou D., Del Bo R., Nizzardo M., Nardini M., Donadoni C., Salani S., Fortunato F., Strazzer S., et al. Neural stem cells LewisX+ CXCR4+ modify disease progression in an amyotrophic lateral sclerosis model. Brain 130 (2007) 1289-1305
42. Kerr D.A., Llado J., Shamblott M.J., Maragakis N.J., Irani D.N., Crawford T.O., Krishnan C., Dike S., Gearhart J.D., and Rothstein J.D. Human embryonic germ cell derivatives facilitate motor recovery of rats with diffuse motor neuron injury. J Neurosci 23 (2003) 5131-5140
43. Corti S., Nizzardo M., Nardini M., Chiara D., Sabrina S., Dario R., Francesca S., Andreina B., Francesco F., Roberto D.B., et al. Neural stem cell transplantation can ameliorate the phenotype of a mouse model of spinal muscular atrophy. J Clin Invest 118 (2008) 3316-3330
44. Einstein O., Fainstein N., Vaknin I., Mizrachi-Kol R., Reihartz E., Grigoriadis N., Lavon I., Baniyash M., Lassmann H., and Ben-Hur T. Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression. Ann Neurol 61 (2007) 209-218
45. Zhang Y.W., Denham J., and Thies R.S. Oligodendrocyte Progenitor Cells Derived from Human Embryonic Stem Cells Express Neurotrophic Factors. Stem Cells Dev 15 (2006) 943-952
46. Keirstead H.S., Nistor G., Bernal G., Totoiu M., Cloutier F., Sharp K., and Steward O. Human Embryonic Stem Cell-Derived Oligodendrocyte Progenitor Cell Transplants Remyelinate and Restore Locomotion after Spinal Cord Injury. J Neurosci 25 (2005) 4694-4705
47. Chiba S., Iwasaki Y., Sekino H., and Suzuki N. Transplantation of motoneuron-enriched neural cells derived from mouse embryonic stem cells improves motor function of hemiplegic mice. Cell Transplant 12 (2003) 457-468
48. Glazova M., Pak E.S., Moretto J., Hollis S., Brewer K.L., and Murashov A.K. Pre-differentiated Embryonic Stem Cells Promote Neuronal Regeneration by Cross-coupling of BDNF and IL-6 Signaling Pathways in the Host Tissue. J Neurotrauma (2009) Epub Ahead of Print
49. Aharonowiz M., Einstein O., Fainstein N., Lassmann H., Reubinoff B., and Ben-Hur T. Neuroprotective effect of transplanted human embryonic stem cell-derived neural precursors in an animal model of multiple sclerosis. PLoS ONE 3 (2008) e3145
50. Cummings B.J., Uchida N., Tamaki S.J., and Anderson A.J. Human neural stem cell differentiation following transplantation into spinal cord injured mice: association with recovery of locomotor function. Neurol Res 28 (2006) 474-481
51. Tarasenko Y.I., Gao J., Nie L., Johnson K.M., Grady J.J., Hulsebosch C.E., McAdoo D.J., and Wu P. Human fetal neural stem cells grafted into contusion-injured rat spinal cords improve behavior. J Neurosc Res 85 (2007) 47-57
52. Gao J., Coggeshall R.E., Chung J.M., Wang J., and Wu P. Functional motoneurons develop from human neural stem cell transplants in adult rats. Neuroreport 18 (2007) 565-569
53. Gao J., Coggeshall R.E., Tarasenko Y.I., and Wu P. Human neural stem cell-derived cholinergic neurons innervate muscle in motoneuron deficient adult rats. Neuroscience 131 (2005) 257-262
54. Yan J., Xu L., Welsh A.M., Hatfield G., Hazel T., Johe K., and Koliatsos V.E. Extensive neuronal differentiation of human neural stem cell grafts in adult rat spinal cord. PLoS Med 4 (2007) e39
55. Xu L., Ryugo D.K., Pongstaporn T., Johe K., and Koliatsos V.E. Human neural stem cell grafts in the spinal cord of SOD1 transgenic rats: differentiation and structural integration into the segmental motor circuitry. J Comp Neurol 514 (2009) 297-309
56. Guest J.D., Hiester E.D., and Bunge R.P. Demyelination and Schwann cell responses adjacent to injury epicenter cavities following chronic human spinal cord injury. Exp Neurol 192 (2005) 384-393
57. Totoiu M.O., and Keirstead H.S. Spinal cord injury is accompanied by chronic progressive demyelination. J Comp Neurol 486 (2005) 373-383
58. Nistor G.I., Totoiu M.O., Haque N., Carpenter M.K., and Keirstead H.S. Human embryonic stem cells differentiate into oligodendrocytes in high purity and myelinate after spinal cord transplantation. Glia 49 (2005) 385-396
59. Izrael M., Zhang P., Kaufman R., Shinder V., Ella R., Amit M., Itskovitz-Eldor J., Chebath J., and Revel M. Human oligodendrocytes derived from embryonic stem cells: Effect of noggin on phenotypic differentiation in vitro and on myelination in vivo. Mol Cell Neurosci 34 (2007) 310-323
60. Totoiu M.O., Nistor G.I., Lane T.E., and Keirstead H.S. Remyelination, axonal sparing, and locomotor recovery following transplantation of glial-committed progenitor cells into the MHV model of multiple sclerosis. Exp Neurol 187 (2004) 254-265
61. Kohama I., Lankford K.L., Preiningerova J., White F.A., Vollmer T.L., and Kocsis J.D. Transplantation of cryopreserved adult human Schwann cells enhances axonal conduction in demyelinated spinal cord. J Neurosci 21 (2001) 944-950
62. Imaizumi T., Lankford K.L., Waxman S.G., Greer C.A., and Kocsis J.D. Transplanted olfactory ensheathing cells remyelinate and enhance axonal conduction in the demyelinated dorsal columns of the rat spinal cord. J Neurosci 18 (1998) 6176-6185
63. Brustle O., Jones K.N., Learish R.D., Karram K., Choudhary K., Wiestler O.D., Duncan I.D., and McKay R.D. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science 285 (1999) 754-756
64. Horky L.L., Galimi F., Gage F.H., and Horner P.J. Fate of endogenous stem/progenitor cells following spinal cord injury. J Comp Neurol 498 (2006) 525-538
65. Wu P., Tarasenko Y.I., Gu Y., Huang L.Y., Coggeshall R.E., and Yu Y. Region-specific generation of cholinergic neurons from fetal human neural stem cells grafted in adult rat. Nat Neurosci 5 (2002) 1271-1278
66. Deshpande D.M., Kim Y.S., Martinez T., Carmen J., Dike S., Shats I., Rubin L.L., Drummond J., Krishnan C., Hoke A., et al. Recovery from paralysis in adult rats using embryonic stem cells. Ann Neurol 60 (2006) 32-44