Bone marrow stromal cell transplantation for ischemic stroke - its multi-functional feature

• Autorzy: Kuroda S.
• Języki publikacji: EN

Abstrakty

EN

In this article, the author reviews recent advancements of basic research on bone marrow stromal cell (BMSC) transplantation for ischemic stroke. The BMSCs are easily isolated from the patients themselves and transplanted into them without any ethical and immunological problem. Animal experiments have shown that BMSC transplantation significantly enhance the recovery of motor and/or cognitive function in various types of neurological disorders such as ischemic stroke. The transplanted BMSCs aggressively migrate toward the damaged tissue and proliferate in the host brain. The BMSCs significantly improve the neuronal receptor function and local glucose metabolism in the peri-infarct area when transplanted into the infarct brain. Recent studies strongly suggest that the BMSCs contain heterogeneous subpopulations and contribute to functional recovery through multiple mechanisms, including neuroprotection, inflammatory modulation, cell fusion, and neural differentiation. The author describes the importance to establish BMSC transplantation as a therapeutic entity that is scientifically proven.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2013
• Tom: 73
• Numer: 1
• Opis fizyczny: p.57-65,fig.,ref.

Twórcy

autor

Kuroda S.

• Department of Neurosurgery, Graduate School of Medicine and Pharmaceutical Science, University of Toyama, Toyama, Japan
• Department of Neurosurgery, Hokkaido University Graduate School of Medicine, Sapporo, Japan

Bibliografia

• Abe K, Yamashita T, Takizawa S, Kuroda S, Kinouchi H, Kawahara N (2012) Stem cell therapy for cerebral isch¬emia: from basic science to clinical applications. J Cereb Blood Flow Metab 32: 1317-1331.
• Alvarez-Dolado M, Pardal R, Garcia-Verdugo JM, Fike JR, Lee HO, Pfeffer K, Lois C, Morrison SJ, Alvarez-Buylla A (2003) Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425: 968-973.
• Askari AT, Unzek S, Popovic ZB, Goldman CK, Forudi F, Kiedrowski M, Rovner A, Ellis SG, Thomas JD, DiCorleto PE, Topol EJ, Penn MS (2003) Effect of stromal-cell-de- rived factor 1 on stem-cell homing and tissue regenera¬tion in ischaemic cardiomyopathy. Lancet 362: 697-703.
• Auletta JJ, Deans RJ, Bartholomew AM (2012) Emerging roles for multipotent, bone marrow-derived stromal cells in host defense. Blood 119: 1801-1809.
• Azizi SA, Stokes D, Augelli BJ, DiGirolamo C, Prockop DJ (1998) Engraftment and migration of human bone mar¬row stromal cells implanted in the brains of albino rats-¬similarities to astrocyte grafts. Proc Natl Acad Sci U S A 95: 3908-3913.
• Bang OY, Lee JS, Lee PH, Lee G (2005) Autologous mesen- chymal stem cell transplantation in stroke patients. Ann Neurol 57: 874-882. Barone FC, Feuerstein GZ (1999) Inflammatory mediators and stroke: new opportunities for novel therapeutics. J Cereb Blood Flow Metab 19: 819-834.
• Bianco P, Gehron Robey P (2000) Marrow stromal stem cells. J Clin Invest 105: 1663-1668.
• Bliss T, Guzman R, Daadi M, Steinberg GK (2007) Cell transplantation therapy for stroke. Stroke 38: 817-826.
• Bossolasco P, Cova L, Calzarossa C, Rimoldi SG, Borsotti C, Deliliers GL, Silani V, Soligo D, Polli E (2005) Neuro¬glial differentiation of human bone marrow stem cells in vitro. Exp Neurol 193: 312-325.
• Chiba Y, Kuroda S, Maruichi K, Osanai T, Hokari M, Yano S, Shichinohe H, Hida K, Iwasaki Y (2009) Transplanted bone marrow stromal cells promote axonal regeneration and improve motor function in a rat spinal cord injury model. Neurosurgery 64: 991-999; discussion 999¬1000.
• Curril IM, Koide M, Yang CH, Segal A, Wellman GC, Spees JL (2010) Incomplete reprogramming after fusion of human multipotent stromal cells and bronchial epithelial cells. FASEB J 24: 4856-4864.
• Friedenstein AJ, Gorskaja JF, Kulagina NN (1976) Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 4: 267-274.
• Gornicka-Pawlak E, Janowski M, Habich A, Jablonska A, Drela K, Kozlowska H, Lukomska B, Sypecka J, Domanska-Janik K (2011) Systemic treatment of focal brain injury in the rat by human umbilical cord blood cells being at different level of neural commitment. Acta Neurobiol Exp (Wars) 71: 46-64.
• Gu Y, Wang J, Ding F, Hu N, Wang Y, Gu X (2009) Neurotrophic actions of bone marrow stromal cells on primary culture of dorsal root ganglion tissues and neu¬rons. J Mol Neurosci 40: 332-341
• 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 (2011) Expression of cytokines in rat brain with focal cerebral ischemia after grafting with bone mar¬row stromal cells and endothelial progenitor cells. Cytotherapy 13: 46-53.
• Hermann A, Liebau S, Gastl R, Fickert S, Habisch HJ, Fiedler J, Schwarz J, Brenner R, Storch A (2006) Comparative analysis of neuroectodermal differentiation capacity of human bone marrow stromal cells using vari¬ous conversion protocols. J Neurosci Res 83: 1502¬1514.
• Hoffmann J, Glassford AJ, Doyle TC, Robbins RC, Schrepfer S, Pelletier MP (2010) Angiogenic effects despite limited cell survival of bone marrow-derived mesenchymal stem cells under ischemia. Thorac Cardiovasc Surg 58: 136¬142.
• Hofstetter CP, Schwarz EJ, Hess D, Widenfalk J, El Manira A, Prockop DJ, Olson L (2002) Marrow stromal cells form guiding strands in the injured spinal cord and pro¬mote recovery. Proc Natl Acad Sci U S A 99: 2199¬2204.
• Hokari M, Kuroda S, Shichinohe H, Yano S, Hida K, Iwasaki Y (2008) Bone marrow stromal cells protect and repair damaged neurons through multiple mechanisms. J Neurosci Res 86: 1024-1035.
• Islam MN, Das SR, Emin MT, Wei M, Sun L, Westphalen K, Rowlands DJ, Quadri SK, Bhattacharya S, Bhattacharya J (2012) Mitochondrial transfer from bone-marrow-de¬rived stromal cells to pulmonary alveoli protects against acute lung injury. Nat Med 18: 759-765.
• Ito M, Kuroda S, Sugiyama T, Maruichi K, Kawabori M, Nakayama N, Houkin K, Iwasaki Y (2012) Transplanted bone marrow stromal cells protect neurovascular units and ameliorate brain damage in stroke-prone spontane¬ously hypertensive rats. Neuropathology 32: 522-533.
• Jablonska A, Lukomska B (2011) Stroke induced brain changes: Implications for stem cell transplantation. Acta Neurobiol Exp (Wars) 71: 74-85.
• Jiang Y, Henderson D, Blackstad M, Chen A, Miller RF, Verfaillie CM (2003) Neuroectodermal differentiation from mouse multipotent adult progenitor cells. Proc Natl Acad Sci U S A 100 (Suppl 1): 11854-11860.
• Jin K, Mao XO, Batteur S, Sun Y, Greenberg DA (2003) Induction of neuronal markers in bone marrow cells: dif¬ferential effects of growth factors and patterns of intracel¬lular expression. Exp Neurol 184: 78-89.
• Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J (1999) Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96: 25-34.
• Kamei N, Tanaka N, Oishi Y, Ishikawa M, Hamasaki T, Nishida K, Nakanishi K, Sakai N, Ochi M (2007) Bone marrow stromal cells promoting corticospinal axon growth through the release of humoral factors in organo- typic cocultures in neonatal rats. J Neurosurg Spine 6: 412-419.
• Kawabori M, Kuroda S, Sugiyama T, Ito M, Shichinohe H, Houkin K, Kuge Y, Tamaki N (2012) Intracerebral, but not intravenous, transplantation of bone marrow stromal cells enhances functional recovery in rat cerebral infarct: An optical imaging study. Neuropathology 32: 217-226.
• Kohyama J, Abe H, Shimazaki T, Koizumi A, Nakashima K, Gojo S, Taga T, Okano H, Hata J, Umezawa A (2001) Brain from bone: efficient "meta-differentiation" of mar¬row stroma-derived mature osteoblasts to neurons with Noggin or a demethylating agent. Differentiation 68: 235-244.
• Kopen GC, Prockop DJ, Phinney DG (1999) Marrow strom¬al cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neo¬natal mouse brains. Proc Natl Acad Sci U S A 96: 10711¬10716.
• Kortesidis A, Zannettino A, Isenmann S, Shi S, Lapidot T, Gronthos S (2005) Stromal-derived factor-1 promotes the growth, survival, and development of human bone mar¬row stromal stem cells. Blood 105: 3793-3801.
• Kuroda Y, Kitada M, Wakao S, Nishikawa K, Tanimura Y, Makinoshima H, Goda M, Akashi H, Inutsuka A, Niwa A, Shigemoto T, Nabeshima Y, Nakahata T, Fujiyoshi Y, Dezawa M (2010) Unique multipotent cells in adult human mesenchymal cell populations. Proc Natl Acad Sci U S A 107: 8639-8643.
• Lee JB, Kuroda S, Shichinohe H, Ikeda J, Seki T, Hida K, Tada M, Sawada K, Iwasaki Y (2003) Migration and dif¬ferentiation of nuclear fluorescence-labeled bone marrow stromal cells after transplantation into cerebral infarct and spinal cord injury in mice. Neuropathology 23: 169-180.
• Lee JB, Kuroda S, Shichinohe H, Yano S, Kobayashi H, Hida K, Iwasaki Y (2004) A pre-clinical assessment model of rat autogeneic bone marrow stromal cell trans¬plantation into the central nervous system. Brain Res Brain Res Protoc 14: 37-44.
• Lee JS, Hong JM, Moon GJ, Lee PH, Ahn YH, Bang OY (2010) A long-term follow-up study of intravenous autol¬ogous mesenchymal stem cell transplantation in patients with ischemic stroke. Stem Cells 28: 1099-1106.
• Lee PH, Kim JW, Bang OY, Ahn YH, Joo IS, Huh K (2008) Autologous mesenchymal stem cell therapy delays the progression of neurological deficits in patients with mul¬tiple system atrophy. Clin Pharmacol Ther 83: 723-730.
• Lu P, Blesch A, Tuszynski MH (2004) Induction of bone marrow stromal cells to neurons: differentiation, transdif-ferentiation, or artifact? J Neurosci Res 77: 174-191.
• Maruichi K, Kuroda S, Chiba Y, Hokari M, Shichinohe H, Hida K, Iwasaki Y (2009) Transplanted bone marrow stromal cells improves cognitive dysfunction due to dif¬fuse axonal injury in rats. Neuropathology 29: 422-432.
• 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 (2010) Mesenchymal stem cell transplantation in amyo- trophic lateral sclerosis: A Phase I clinical trial. Exp Neurol 223: 229-237.
• Miyamoto M, Kuroda S, Zhao S, Magota K, Shichinohe H, Houkin K, Kuge Y, Tamaki N (2012) Bone marrow stromal cell transplantation enhances recovery of local glucose metabolism after cerebral infarction in rats: A serial 18F-FDG PET study. J Nucl Med 54:145-150
• Mori K, Iwata J, Miyazaki M, Nakao Y, Maeda M (2005) 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 25: 887-898.
• Mundra V, Gerling IC, Mahato RI (2012) Mesenchymal stem cell-based therapy. Mol Pharm 10: 77-89.
• 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.
• Neuhuber B, Timothy Himes B, Shumsky JS, Gallo G, Fischer I (2005) Axon growth and recovery of function supported by human bone marrow stromal cells in the injured spinal cord exhibit donor variations. Brain Res 1035: 73-85.
• Pal R, Venkataramana NK, Bansal A, Balaraju S, Jan M, Chandra R, Dixit A, Rauthan A, Murgod U, Totey S (2009) Ex vivo-expanded autologous bone marrow-de¬rived mesenchymal stromal cells in human spinal cord injury/paraplegia: a pilot clinical study. Cytotherapy 11: 897-911.
• Parr AM, Tator CH, Keating A (2007) Bone marrow-derived mesenchymal stromal cells for the repair of central nervous system injury. Bone Marrow Transplant 40: 609-619.
• Prockop DJ, Gregory CA, Spees JL (2003) One strategy for cell and gene therapy: harnessing the power of adult stem cells to repair tissues. Proc Natl Acad Sci U S A 100 (Suppl 1): 11917-11923.
• Raffaghello L, Bianchi G, Bertolotto M, Montecucco F, Busca A, Dallegri F, Ottonello L, Pistoia V (2008) Human mesenchymal stem cells inhibit neutrophil apoptosis: a model for neutrophil preservation in the bone marrow niche. Stem cells 26: 151-162.
• Saito F, Nakatani T, Iwase M, Maeda Y, Murao Y, Suzuki Y, Fukushima M, Ide C (2012) Administration of cultured autologous bone marrow stromal cells into cerebrospinal fluid in spinal injury patients: a pilot study. Restor Neurol Neurosci 30: 127-136.
• 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.
• Savitz SI, Fisher M (2007) Future of neuroprotection for acute stroke: in the aftermath of the SAINT trials. Ann Neurol 61: 396-402.
• Scheibe F, Klein O, Klose J, Priller J (2012) Mesenchymal stromal cells rescue cortical neurons from apoptotic cell death in an in vitro model of cerebral ischemia. Cellular and molecular neurobiology 32: 567-576.
• Shichinohe H, Kuroda S, Yano S, Ohnishi T, Tamagami H, Hida K, Iwasaki Y (2006) Improved expression of gam- ma-aminobutyric acid receptor in mice with cerebral infarct and transplanted bone marrow stromal cells: an autoradiographic and histologic analysis. J Nucl Med 47: 486-491.
• Shichinohe H, Kuroda S, Yano S, Hida K, Iwasaki Y (2007) Role of SDF-1/CXCR4 system in survival and migration of bone marrow stromal cells after transplantation into mice cerebral infarct. Brain Res 1183: 138-147.
• Shichinohe H, Kuroda S, Tsuji S, Yamaguchi S, Yano S, Lee JB, Kobayashi H, Kikuchi S, Hida K, Iwasaki Y (2008) Bone marrow stromal cells promote neurite extension in organotypic spinal cord slice: significance for cell transplan¬tation therapy. Neurorehabil Neural Repair 22: 447-457.
• Shichinohe H, Kuroda S, Sugiyama T, Ito M, Kawabori M (2010) Bone marrow stromal cell transplantation attenu¬ates cognitive dysfunction due to chronic cerebral isch¬emia in rats. Dement Geriatr Cogn Disord 30: 293-301.
• Shihabuddin LS, Horner PJ, Ray J, Gage FH (2000) Adult spinal cord stem cells generate neurons after transplanta¬tion in the adult dentate gyrus. J Neurosci 20: 8727-8735.
• Son BR, Marquez-Curtis LA, Kucia M, Wysoczynski M, Turner AR, Ratajczak J, Ratajczak MZ, Janowska- Wieczorek A (2006) 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 24: 1254-1264.
• Spees JL, Olson SD, Ylostalo J, Lynch PJ, Smith J, Perry A, Peister A, Wang MY, Prockop DJ (2003) Differentiation, cell fusion, and nuclear fusion during ex vivo repair of epithelium by human adult stem cells from bone marrow stroma. Proc Natl Acad Sci U S A 100: 2397-2402.
• Terada N, Hamazaki T, Oka M, Hoki M, Mastalerz DM, Nakano Y, Meyer EM, Morel L, Petersen BE, Scott EW (2002) Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 416: 542-545.
• van den Akker F, Deddens JC, Doevendans PA, Sluijter JP (2013) Cardiac stem cell therapy to modulate inflamma¬tion upon myocardial infarction. Biochim Biophys Acta 1830: 2449-2458.
• Vassilopoulos G, Wang PR, Russell DW (2003) Transplanted bone marrow regenerates liver by cell fusion. Nature 422: 901-904.
• Wakao S, Kitada M, Kuroda Y, Shigemoto T, Matsuse D, Akashi H, Tanimura Y, Tsuchiyama K, Kikuchi T, Goda M, Nakahata T, Fujiyoshi Y, Dezawa M (2011) Multilineage-differentiating stress-enduring (Muse) cells are a primary source of induced pluripotent stem cells in human fibroblasts. Proc Natl Acad Sci U S A 108: 9875¬9880.
• Wang L, Li Y, Chen J, Gautam SC, Zhang Z, Lu M, Chopp M (2002) Ischemic cerebral tissue and MCP-1 enhance rat bone marrow stromal cell migration in interface cul¬ture. Exp Hematol 30: 831-836.
• Wislet-Gendebien S, Hans G, Leprince P, Rigo JM, Moonen G, Rogister B (2005) Plasticity of cultured mesenchymal stem cells: switch from nestin-positive to excitable neu¬ron-like phenotype. Stem Cells 23: 392-402.
• Woodbury D, Schwarz EJ, Prockop DJ, Black IB (2000) Adult rat and human bone marrow stromal cells differen¬tiate into neurons. J Neurosci Res 61: 364-370.
• Wu QY, Li J, Feng ZT, Wang TH (2007) Bone marrow stromal cells of transgenic mice can improve the cogni¬tive ability of an Alzheimer's disease rat model. Neurosci Lett 417: 281-285.
• Yamaguchi S, Kuroda S, Kobayashi H, Shichinohe H, Yano S, Hida K, Shinpo K, Kikuchi S, Iwasaki Y (2006) The effects of neuronal induction on gene expression profile in bone marrow stromal cells (BMSC)-a preliminary study using microarray analysis. Brain Res 1087: 15-27.
• Yang WJ, Li SH, Weisel RD, Liu SM, Li RK (2012) Cell fusion contributes to the rescue of apoptotic cardiomyo- cytes by bone marrow cells. J Cell Mol Med 16: 3085¬3095.
• Yano S, Kuroda S, Shichinohe H, Hida K, Iwasaki Y (2005) Do bone marrow stromal cells proliferate after transplan¬tation into mice cerebral infarct? - a double labeling study. Brain Res 1065: 60-67.
• Zhang ZX, Guan LX, Zhang K, Zhang Q, Dai LJ (2008) A combined procedure to deliver autologous mesenchymal stromal cells to patients with traumatic brain injury. Cytotherapy 10: 134-139.
• Zhong C, Qin Z, Zhong CJ, Wang Y, Shen XY (2003) Neuroprotective effects of bone marrow stromal cells on rat organotypic hippocampal slice culture model of cere¬bral ischemia. Neurosci Lett 342: 93-96.

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