Autologous bone marrow stromal cell transplantation for central nervous system disorders - recent progress and perspective for clinical application

Journal of Stem Cells and Regenerative Medicine

Volumn 7, Issue 1, 2011, Pages 2-13

  Kuroda, Satoshi ^a   Shichinohe, Hideo ^a   Houkin, Kiyohiro ^a   Iwasaki, Yoshinobu ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Bone marrow stromal cell; Cerebral stroke; Spinal cord injury; Translational study; Transplantation

Indexed keywords

DISUFENTON SODIUM; NEUROPROTECTIVE AGENT; NEUROTROPHIC FACTOR;

AMYOTROPHIC LATERAL SCLEROSIS; AUTOLOGOUS BONE MARROW STROMAL CELL TRANSPLANTATION; BONE MARROW CELL; BONE MARROW STROMAL CELL; BRAIN ISCHEMIA; CELL EXPANSION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CELL TRACKING; CELL TRANSPLANTATION; CENTRAL NERVOUS SYSTEM DISEASE; CULTURE MEDIUM; CYTOLOGY; GENE EXPRESSION; HUMAN; IMAGING; NEUROPROTECTION; NONHUMAN; OPTICAL IMAGING; PHENOTYPE; REVIEW; SPINAL CORD INJURY; TRAUMATIC BRAIN INJURY;

ANIMALIA;

EID: 80052059773     PISSN: 09737154     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (75)

1. Savitz SI, Fisher M. Future of neuroprotection for acute stroke: In the aftermath of the SAINT trials. Ann Neurol. 2007;61:396-402
2. Bliss T, Guzman R, Daadi M, Steinberg GK. Cell transplantation therapy for stroke. Stroke. 2007;38:817-826
3. Parr AM, Tator CH, Keating A. Bone marrow-derived mesenchymal stromal cells for the repair of central nervous system injury. Bone Marrow Transplant. 2007;40:609-619
4. Hokari M, Kuroda S, Shichinohe H, Yano S, Hida K, Iwasaki Y. Bone marrow stromal cells protect and repair damaged neurons through multiple mechanisms. J Neurosci Res. 2008;86:1024-1035
5. Prockop DJ, Gregory CA, Spees JL. One strategy for cell and gene therapy: Harnessing the power of adult stem cells to repair tissues. Proc Natl Acad Sci U S A. 2003;100 Suppl 1:11917-11923
6. Chiba Y, Kuroda S, Maruichi K, Osanai T, Hokari M, Yano S, Shichinohe H, Hida K, Iwasaki Y. Transplanted bone marrow stromal cells promote axonal regeneration and improve motor function in a rat spinal cord injury model. Neurosurgery. 2009;64:991-999; discussion 999-1000
7. Itosaka H, Kuroda S, Shichinohe H, Yasuda H, Yano S, Kamei S, Kawamura R, Hida K, Iwasaki Y. Fibrin matrix provides a suitable scaffold for bone marrow stromal cells transplanted into injured spinal cord: A novel material for cns tissue engineering. Neuropathology. 2009;29:248-257
8. Lee JB, Kuroda S, Shichinohe H, Ikeda J, Seki T, Hida K, Tada M, Sawada K, Iwasaki Y. Migration and differentiation of nuclear fluorescence-labeled bone marrow stromal cells after transplantation into cerebral infarct and spinal cord injury in mice. Neuropathology. 2003;23:169-180
9. Lee JB, Kuroda S, Shichinohe H, Yano S, Kobayashi H, Hida K, Iwasaki Y. A pre-clinical assessment model of rat autogeneic bone marrow stromal cell transplantation into the central nervous system. Brain Res Brain Res Protoc. 2004;14:37-44
10. Shichinohe H, Kuroda S, Lee JB, Nishimura G, Yano S, Seki T, Ikeda J, Tamura M, Iwasaki Y. In vivo tracking of bone marrow stromal cells transplanted into mice cerebral infarct by fluorescence optical imaging. Brain Res Brain Res Protoc. 2004;13:166-175
11. Shichinohe H, Kuroda S, Tsuji S, Yamaguchi S, Yano S, Lee JB, Kobayashi H, Kikuchi S, Hida K, Iwasaki Y. Bone marrow stromal cells promote neurite extension in organotypic spinal cord slice: Significance for cell transplantation therapy. Neurorehabil Neural Repair. 2008;22:447-457
12. Shichinohe H, Kuroda S, Yano S, Hida K, Iwasaki Y. Role of SDF-1/CXCR4 system in survival and migration of bone marrow stromal cells after transplantation into mice cerebral infarct. Brain Res. 2007;1183:138-147
13. Shichinohe H, Kuroda S, Yano S, Ohnishi T, Tamagami H, Hida K, Iwasaki Y. Improved expression of gamma-aminobutyric acid receptor in mice with cerebral infarct and transplanted bone marrow stromal cells: An autoradiographic and histologic analysis. J Nucl Med. 2006;47:486-491
14. Yamaguchi S, Kuroda S, Kobayashi H, Shichinohe H, Yano S, Hida K, Shinpo K, Kikuchi S, Iwasaki Y. The effects of neuronal induction on gene expression profile in bone marrow stromal cells (BMSC)-a preliminary study using microarray analysis. Brain Res. 2006;1087:15-27
15. Yano S, Kuroda S, Lee JB, Shichinohe H, Seki T, Ikeda J, Nishimura G, Hida K, Tamura M, Iwasaki Y. In vivo fluorescence tracking of bone marrow stromal cells transplanted into a pneumatic injury model of rat spinal cord. J Neurotrauma. 2005;22:907-918
16. Yano S, Kuroda S, Shichinohe H, Hida K, Iwasaki Y. Do bone marrow stromal cells proliferate after transplantation into mice cerebral infarct?--a double labeling study. Brain Res. 2005;1065:60-67
17. Yano S, Kuroda S, Shichinohe H, Seki T, Ohnishi T, Tamagami H, Hida K, Iwasaki Y. Bone marrow stromal cell transplantation preserves gammaaminobutyric acid receptor function in the injured spinal cord. J Neurotrauma. 2006;23:1682-1692
18. Maruichi K, Kuroda S, Chiba Y, Hokari M, Shichinohe H, Hida K, Iwasaki Y. Graded model of diffuse axonal injury for studying head injury-induced cognitive dysfunction in rats. Neuropathology. 2009;29:132-139
19. Maruichi K, Kuroda S, Chiba Y, Hokari M, Shichinohe H, Hida K, Iwasaki Y. Transplanted bone marrow stromal cells improves cognitive dysfunction due to diffuse axonal injury in rats. Neuropathology. 2009;29:422-432
20. 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. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol. 2000;164:247-256
21. Woodbury D, Schwarz EJ, Prockop DJ, Black IB. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res. 2000;61:364-370
22. Azizi SA, Stokes D, Augelli BJ, DiGirolamo C, Prockop DJ. Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats--similarities to astrocyte grafts. Proc Natl Acad Sci U S A. 1998;95:3908-3913
23. Kopen GC, Prockop DJ, Phinney DG. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc Natl Acad Sci U S A. 1999;96:10711-10716
24. 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
25. Neuhuber B, Gallo G, Howard L, Kostura L, Mackay A, Fischer I. 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. 2004;77:192-204
26. Terada N, Hamazaki T, Oka M, Hoki M, Mastalerz DM, Nakano Y, Meyer EM, Morel L, Petersen BE, Scott EW. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature. 2002;416:542-545
27. Zhong C, Qin Z, Zhong CJ, Wang Y, Shen XY. Neuroprotective effects of bone marrow stromal cells on rat organotypic hippocampal slice culture model of cerebral ischemia. Neurosci Lett. 2003;342:93-96
28. Kortesidis A, Zannettino A, Isenmann S, Shi S, Lapidot T, Gronthos S. Stromal-derived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells. Blood. 2005;105:3793-3801
29. Neuhuber B, Timothy Himes B, Shumsky JS, Gallo G, 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. 2005;1035:73-85
30. Chen Q, Long Y, Yuan X, Zou L, Sun J, Chen S, Perez-Polo JR, Yang K. Protective effects of bone marrow stromal cell transplantation in injured rodent brain: Synthesis of neurotrophic factors. J Neurosci Res. 2005;80:611-619
31. Garcia R, Aguiar J, Alberti E, de la Cuetara K, Pavon N. Bone marrow stromal cells produce nerve growth factor and glial cell line-derived neurotrophic factors. Biochem Biophys Res Commun. 2004;316:753-754
32. Gu Y, Wang J, Ding F, Hu N, Wang Y, Gu X. Neurotrophic actions of bone marrow stromal cells on primary culture of dorsal root ganglion tissues and neurons. J Mol Neurosci. 2009
33. Kamei N, Tanaka N, Oishi Y, Ishikawa M, Hamasaki T, Nishida K, Nakanishi K, Sakai N, Ochi M. Bone marrow stromal cells promoting corticospinal axon growth through the release of humoral factors in organotypic cocultures in neonatal rats. J Neurosurg Spine. 2007;6:412-419
34. He XY, Chen ZZ, Cai YQ, Xu G, Shang JH, Kou SB, Li M, Zhang HT, Duan CZ, Zhang SZ, Ke YQ, Zeng YJ, Xu RX, Jiang XD. Expression of cytokines in rat brain with focal cerebral ischemia after grafting with bone marrow stromal cells and endothelial progenitor cells. Cytotherapy. 2011;13:46-53
35. Wang L, Li Y, Chen J, Gautam SC, Zhang Z, Lu M, Chopp M. Ischemic cerebral tissue and MCP-1 enhance rat bone marrow stromal cell migration in interface culture. Exp Hematol. 2002;30:831-836
36. Askari AT, Unzek S, Popovic ZB, Goldman CK, Forudi F, Kiedrowski M, Rovner A, Ellis SG, Thomas JD, DiCorleto PE, Topol EJ, Penn MS. Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet. 2003;362:697-703
37. Son BR, Marquez-Curtis LA, Kucia M, Wysoczynski M, Turner AR, Ratajczak J, Ratajczak MZ, Janowska-Wieczorek A. Migration of bone marrow and cord blood mesenchymal stem cells in vitro is regulated by stromal-derived factor-1-CXCR4 and hepatocyte growth factor-c-met axes and involves matrix metalloproteinases. Stem Cells. 2006;24:1254-1264
38. Hokari M, Kuroda S, Chiba Y, Maruichi K, Iwasaki Y. Synergistic effects of granulocyte-colony stimulating factor on bone marrow stromal cell transplantation for mice cerebral infarct. Cytokine. 2009;46:260-266
39. Sugiyama T, Kuroda S, Osanai T, Shichinohe H, Kuge Y, Ito M, Kawabori M, Iwasaki Y. Near infrared fluorescence labeling allows non-invasive tracking of bone marrow stromal cells transplanted into rat infarct brain. Neurosurgery. in press
40. Chiba Y, Kuroda S, Shichinohe H, Hokari M, Osanai T, Maruichi K, Yano S, Hida K, Iwasaki Y. Synergistic effects of bone marrow stromal cells and a rho kinase (ROCK) inhibitor, fasudil on axon regeneration in rat spinal cord injury. Neuropathology. 2010;30:241-250
41. Wu QY, Li J, Feng ZT, Wang TH. Bone marrow stromal cells of transgenic mice can improve the cognitive ability of an alzheimer's disease rat model. Neurosci Lett. 2007;417:281-285
42. Shichinohe H, Kuroda S, Sugiyama T, Ito M, Kawabori M. Bone marrow stromal cell transplantation attenuates cognitive dysfunction due to chronic cerebral ischemia in rats. Dement Geriatr Cogn Disord. 2010;30:293-301
43. Hofstetter CP, Schwarz EJ, Hess D, Widenfalk J, El Manira A, Prockop DJ, Olson L. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci U S A. 2002;99:2199-2204
44. Mori K, Iwata J, Miyazaki M, Nakao Y, Maeda M. Functional recovery of neuronal activity in rat whisker-barrel cortex sensory pathway from freezing injury after transplantation of adult bone marrow stromal cells. J Cereb Blood Flow Metab. 2005;25:887-898
45. Bang OY, Lee JS, Lee PH, Lee G. Autologous mesenchymal stem cell transplantation in stroke patients. Ann Neurol. 2005;57:874-882
46. Lee PH, Kim JW, Bang OY, Ahn YH, Joo IS, Huh K. Autologous mesenchymal stem cell therapy delays the progression of neurological deficits in patients with multiple system atrophy. Clin Pharmacol Ther. 2008;83:723-730
47. Mazzini L, Ferrero I, Luparello V, Rustichelli D, Gunetti M, Mareschi K, Testa L, Stecco A, Tarletti R, Miglioretti M, Fava E, Nasuelli N, Cisari C, Massara M, Vercelli R, Oggioni GD, Carriero A, Cantello R, Monaco F, Fagioli F. Mesenchymal stem cell transplantation in amyotrophic lateral sclerosis: A phase i clinical trial. Exp Neurol. 2010;223:229-237
48. Pal R, Venkataramana NK, Bansal A, Balaraju S, Jan M, Chandra R, Dixit A, Rauthan A, Murgod U, Totey S. Ex vivo-expanded autologous bone marrow-derived mesenchymal stromal cells in human spinal cord injury/paraplegia: A pilot clinical study. Cytotherapy. 2009;11:897-911
49. Zhang ZX, Guan LX, Zhang K, Zhang Q, Dai LJ. A combined procedure to deliver autologous mesenchymal stromal cells to patients with traumatic brain injury. Cytotherapy. 2008;10:134-139
50. Saito F, Nakatani T, Iwase M, Maeda Y, Hirakawa A, Murao Y, Suzuki Y, Onodera R, Fukushima M, Ide C. Spinal cord injury treatment with intrathecal autologous bone marrow stromal cell transplantation: The first clinical trial case report. J Trauma. 2008;64:53-59
51. Bakay RA. Neural transplantation. J Neurosurg. 2005;103:6-8; discussion 8
52. Quinn N, Barker RA, Wenning GK. Are trials of intravascular infusions of autologous mesenchymal stem cells in patients with multiple system atrophy currently justified, and are they effective? Clin Pharmacol Ther. 2008;83:663-665
53. Roundtable STAI. Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke. 1999;30:2752-2758
54. Kuroda S, Tsuchidate R, Smith M-L, Maples KR, Siesjo BK. Neuroprotective effects of a novel nitrone, NXY-059, after transient focal cerebral ischemia in the rat. J Cereb Blood Flow Metab. 1999;19:778-787
55. Marshall JWB, Duffin KJ, Green AR, Ridley RM. Nxy-059, a free radical-trapping agent, substantially lessons the functional disability resulting from cerebral ischemia in a primate species. Stroke. 2001;32:190-198
56. Lees KR, Zivin JA, Ashwood T, Davalos A, Davis SM, Diener HC, Grotta J, Lyden P, Shuaib A, Hardemark HG, Wasiewski WW. Nxy-059 for acute ischemic stroke. N Engl J Med. 2006;354:588-600
57. Shuaib A, Lees KR, Lyden P, Grotta J, Davalos A, Davis SM, Diener HC, Ashwood T, Wasiewski WW, Emeribe U. NXY-059 for the treatment of acute ischemic stroke. N Engl J Med. 2007;357:562-571
58. Feuerstein GZ, Zaleska MM, Krams M, Wang X, Day M, Rutkowski JL, Finklestein SP, Pangalos MN, Poole M, Stiles GL, Ruffolo RR, Walsh FL. Missing steps in the stair case: A translational medicine perspective on the development of NXY-059 for treatment of acute ischemic stroke. J Cereb Blood Flow Metab. 2008;28:217-219
59. Borlongan CV, Chopp M, Steinberg GK, Bliss TM, Li Y, Lu M, Hess DC, Kondziolka D. Potential of stem/progenitor cells in treating stroke: The missing steps in translating cell therapy from laboratory to clinic. Regen Med. 2008;3:249-250
60. Sugiyama T, Kuroda S, Takeda Y, Nishio M, Ito M, Shichinohe H, Koike T. Therapeutic impact of human bone marrow stromal cells (HBMSC) expanded by animal serum-free medium for cerebral infarct in rats. Neurosurgery. in press
61. Bakshi A, Barshinger AL, Swanger SA, Madhavani V, Shumsky JS, Neuhuber B, Fischer I. Lumbar puncture delivery of bone marrow stromal cells in spinal cord contusion: A novel method for minimally invasive cell transplantation. J Neurotrauma. 2006;23:55-65
62. Vaquero J, Zurita M, Oya S, Santos M. Cell therapy using bone marrow stromal cells in chronic paraplegic rats: Systemic or local administration? Neurosci Lett. 2006;398:129-134
63. Zurita M, Vaquero J. Functional recovery in chronic paraplegia after bone marrow stromal cells transplantation. Neuroreport. 2004;15:1105-1108
64. Zurita M, Vaquero J. Bone marrow stromal cells can achieve cure of chronic paraplegic rats: Functional and morphological outcome one year after transplantation. Neurosci Lett. 2006;402:51-56
65. Sykova E, Homola A, Mazanec R, Lachmann H, Konradova SL, Kobylka P, Padr R, Neuwirth J, Komrska V, Vavra V, Stulik J, Bojar M. Autologous bone marrow transplantation in patients with subacute and chronic spinal cord injury. Cell Transplant. 2006;15:675-687
66. Yoon SH, Shim YS, Park YH, Chung JK, Nam JH, Kim MO, Park HC, Park SR, Min BH, Kim EY, Choi BH, Park H, Ha Y. 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. 2007;25:2066-2073
67. Lu D, Mahmood A, Wang L, Li Y, Lu M, Chopp M. Adult bone marrow stromal cells administered intravenously to rats after traumatic brain injury migrate into brain and improve neurological outcome. Neuroreport. 2001;12:559-563
68. Shen LH, Li Y, Chen J, Zhang J, Vanguri P, Borneman J, Chopp M. Intracarotid transplantation of bone marrow stromal cells increases axon-myelin remodeling after stroke. Neuroscience. 2006;137:393-399
69. Lu D, Mahmood A, Qu C, Hong X, Kaplan D, Chopp M. Collagen scaffolds populated with human marrow stromal cells reduce lesion volume and improve functional outcome after traumatic brain injury. Neurosurgery. 2007;61:596-602; discussion 602-593
70. Yasuda H, Kuroda S, Shichinohe H, Kamei S, Kawamura R, Iwasaki Y. Effect of biodegradable fibrin scaffold on survival, migration, and differentiation of transplanted bone marrow stromal cells after cortical injury in rats. J Neurosurg. 2009
71. Osanai T, Kuroda S, Yasuda H, Chiba Y, Maruichi K, Hokari M, Sugiyama T, Shichinohe H, Iwasaki Y. Noninvasive transplantation of bone marrow stromal cells for ischemic stroke: Preliminary study with a thermoreversible gelation polymer hydrogel. Neurosurgery. 2010;66:1140-1147; discussion 1147
72. Hoehn M, Kustermann E, Blunk J, Wiedermann D, Trapp T, Wecker S, Focking M, Arnold H, Hescheler J, Fleischmann BK, Schwindt W, Buhrle C. Monitoring of implanted stem cell migration in vivo: A highly resolved in vivo magnetic resonance imaging investigation of experimental stroke in rat. Proc Natl Acad Sci U S A. 2002;99:16267-16272
73. Jendelova P, Herynek V, DeCroos J, Glogarova K, Andersson B, Hajek M, Sykova E. Imaging the fate of implanted bone marrow stromal cells labeled with superparamagnetic nanoparticles. Magn Reson Med. 2003;50:767-776
74. Modo M, Mellodew K, Cash D, Fraser SE, Meade TJ, Price J, Williams SC. Mapping transplanted stem cell migration after a stroke: A serial, in vivo magnetic resonance imaging study. Neuroimage. 2004;21:311-317
75. Correa PL, Mesquita CT, Felix RM, Azevedo JC, Barbirato GB, Falcao CH, Gonzalez C, Mendonca ML, Manfrim A, de Freitas G, Oliveira CC, Silva D, Avila D, Borojevic R, Alves S, Oliveira AC, Jr., Dohmann HF. Assessment of intra-arterial injected autologous bone marrow mononuclear cell distribution by radioactive labeling in acute ischemic stroke. Clin Nucl Med. 2007;32:839-841