Mesenchymal stem cell transplantation in multiple sclerosis

Prockop, 1997, Marrow stromal cells as stem cells for nonhematopoietic tissues, Science, 276, 71, 10.1126/science.276.5309.71 Pittenger, 1999, Multilineage potential of adult human mesenchymal stem cells, Science, 284, 143, 10.1126/science.284.5411.143 Da Silva Meirelles, 2008, In search of the in vivo identity of mesenchymal stem cells, Stem Cells, 26, 2287, 10.1634/stemcells.2007-1122 Crisan, 2008, A perivascular origin for mesenchymal stem cells in multiple human organs, Cell Stem Cell, 3, 301, 10.1016/j.stem.2008.07.003 Dominici, 2006, Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society For Cellular Therapy position statement, Cytotherapy, 8, 315, 10.1080/14653240600855905 Mahad, 2011, Mesenchymal stem cell transplantation to treat multiple sclerosis, 520 Sadan, 2009, Bone-marrow-derived mesenchymal stem cell therapy for neurodegenerative diseases, Expert Opin Biol Ther, 9, 1487, 10.1517/14712590903321439 Siatskas, 2009, Stem cell and gene therapeutic strategies for the treatment of multiple sclerosis, Curr Mol Med, 9, 992, 10.2174/156652409789712774 Freedman, 2010, The therapeutic potential of mesenchymal stem cell transplantation as a treatment for multiple sclerosis: consensus report of the International MSCT Study Group, Mult Scler, 16, 503, 10.1177/1352458509359727 Maltman, 2011, Role of mesenchymal stem cells in neurogenesis and nervous system repair, Neurochem Int, 59, 347 Zappia, 2005, Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy, Blood, 106, 1755, 10.1182/blood-2005-04-1496 Karussis, 2005, Mesenchymal bone marrow stem cells migrate in CNS lesions in experimental autoimmune encephalomyelitis, differentiate into neuronal and glial line and downregulate EAE (abstract), Neurology, 64, A407 Karussis, 2007, Use of stem cells for the treatment of multiple sclerosis, Expert Rev Neurother, 7, 1189, 10.1586/14737175.7.9.1189 Zhang, 2005, Human bone marrow stromal cell treatment improves neurological functional recovery in EAE mice, Exp Neurol, 195, 16, 10.1016/j.expneurol.2005.03.018 Gerdoni, 2007, Mesenchymal stem cells effectively modulate pathogenic immune response in experimental autoimmune encephalomyelitis, Ann Neurol, 61, 219, 10.1002/ana.21076 Le Blanc, 2005, Immunobiology of human mesenchymal stem cells and future use in hematopoietic stem cell transplantation, Biol Blood Marrow Transplant, 11, 321, 10.1016/j.bbmt.2005.01.005 Uccelli, 2006, Immunoregulatory function of mesenchymal stem cells, Eur J Immunol, 36, 2566, 10.1002/eji.200636416 Newman, 2009, Treatment of inflammatory diseases with mesenchymal stem cells, Inflamm Allergy Drug Targets, 8, 110, 10.2174/187152809788462635 Bartholomew, 2002, Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo, Exp Hematol, 30, 42, 10.1016/S0301-472X(01)00769-X Le Blanc, 2003, Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatability complex, Scand J Immunol, 57, 11, 10.1046/j.1365-3083.2003.01176.x Darlington, 2010, Reciprocal Th1 and Th17 regulation by mesenchymal stem cells: implications for MS, Ann Neurol, 68, 540, 10.1002/ana.22065 Djouad, 2003, Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals, Blood, 102, 3837, 10.1182/blood-2003-04-1193 Krampera, 2003, Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide, Blood, 101, 3722, 10.1182/blood-2002-07-2104 Beyth, 2005, Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness, Blood, 105, 2214, 10.1182/blood-2004-07-2921 Di Nicola, 2002, Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli, Blood, 99, 3838, 10.1182/blood.V99.10.3838 Rasmusson, 2003, Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells, Transplantation, 76, 1208, 10.1097/01.TP.0000082540.43730.80 Tse, 2003, Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation, Transplantation, 75, 389, 10.1097/01.TP.0000045055.63901.A9 Le Blanc, 2004, Mesenchymal stem cells inhibit the expression of CD25 (interleukin-2 receptor) and CD38 on phytohaemagglutinin-activated lymphocytes, Scand J Immunol, 60, 307, 10.1111/j.0300-9475.2004.01483.x Chabannes, 2007, A role for heme oxygenase-1 in the immunosuppressive effect of adult rat and human mesenchymal stem cells, Blood, 110, 3691, 10.1182/blood-2007-02-075481 Nasef, 2007, Immunosuppressive effects of mesenchymal stem cells: involvement of HLA-G, Transplantation, 84, 231, 10.1097/01.tp.0000267918.07906.08 Corcione, 2006, Human mesenchymal stem cells modulate B-cell functions, Blood, 107, 367, 10.1182/blood-2005-07-2657 Bai, 2009, Human bone marrow-derived mesenchymal stem cells induce Th2-polarized immune response and promote endogenous repair in animal models of multiple sclerosis, Glia, 57, 1192, 10.1002/glia.20841 Zepp, 2011, IL-17 receptor signaling and T helper 17-mediated autoimmune demyelinating disease, Trends Immunol, 32, 232, 10.1016/j.it.2011.02.007 Einstein, 2007, Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression, Ann Neurol, 61, 209, 10.1002/ana.21033 Jiang, 2002, Pluripotency of mesenchymal stem cells derived from adult marrow, Nature, 418, 41, 10.1038/nature00870 Rutenberg, 2004, Stem cell plasticity, beyond alchemy, Int J Hematol, 79, 15, 10.1007/BF02983528 Rivera, 2006, Mesenchymal stem cells instruct oligodrogenic fate decision on adult neural stem cells, Stem Cells, 24, 2209, 10.1634/stemcells.2005-0614 Fuller, 2007, Bone morphogenetic proteins promote gliosis in demyelinating spinal cord lesions, Ann Neurol, 62, 288, 10.1002/ana.21179 Bai, 2012, Hepatocyte growth factor mediates mesenchymal stem cell-induced recovery in multiple sclerosis models, Nat Neurosci, 15, 862, 10.1038/nn.3109 Brass, 2006, Bone marrow for the brain?, Exp Neurol, 199, 16, 10.1016/j.expneurol.2006.03.009 Bliss, 2007, Cell transplantation therapy for stroke, Stroke, 38, 817, 10.1161/01.STR.0000247888.25985.62 Phinney, 2005, Plasticity and therapeutic potential of mesenchymal stem cells in the nervous system, Curr Pharm Des, 11, 1255, 10.2174/1381612053507495 English, 2006, Elusive mechanisms of “stem-cell”-mediated repair of cerebral damage, Exp Neurol, 199, 10, 10.1016/j.expneurol.2006.03.005 Phinney, 2007, Mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair—current views, Stem Cells, 25, 2896, 10.1634/stemcells.2007-0637 Chopp, 2008, Plasticity and remodeling of brain, J Neurol Sci, 265, 97, 10.1016/j.jns.2007.06.013 Dharmasaroja, 2009, Bone marrow-derived mesenchymal stem cells for the treatment of ischemic stroke, J Clin Neurosci, 16, 12, 10.1016/j.jocn.2008.05.006 Akiyama, 2002, Remyelination of the spinal cord following intravenous delivery of bone marrow cells, Glia, 39, 229, 10.1002/glia.10102 Dezawa, 2001, Sciatic nerve regeneration in rats induced by transplantation of in vitro differentiated bone-marrow stromal cells, Eur J Neurosci, 14, 1771, 10.1046/j.0953-816x.2001.01814.x Zhao, 2007, Human mesenchymal stromal cells ameliorate the phenotype of SOD1-G93A ALS mice, Cytotherapy, 9, 414, 10.1080/14653240701376413 Zhang, 2009, Multiple administrations of human marrow stromal cells through cerebrospinal fluid prolong survival in a transgenic mouse model of amyotrophic lateral sclerosis, Cytotherapy, 11, 299, 10.1080/14653240902806986 Li, 2001, Intracerebral transplantation of bone marrow stromal cells in a 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson's disease, Neurosci Lett, 315, 67, 10.1016/S0304-3940(01)02384-9 Sadan, 2008, Migration of neurotrophic factor-secreting mesenchymal stem cells toward a quinolinic acid lesion as viewed by magnetic resonance imaging, Stem Cells, 26, 2542, 10.1634/stemcells.2008-0240 Mahmood, 2001, Treatment of traumatic brain injury in female rats with intravenous administration of bone marrow stromal cells, Neurosurgery, 49, 1196 Lu, 2005, Can bone marrow-derived stem cells differentiate into functional neurons?, Exp Neurol, 193, 273, 10.1016/j.expneurol.2005.01.031 Chopp, 2000, Spinal cord injury in rat: treatment with bone marrow stromal cell transplantation, NeuroReport, 11, 3001, 10.1097/00001756-200009110-00035 Hofstetter, 2002, Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery, Proc Natl Acad Sci U S A, 99, 2199, 10.1073/pnas.042678299 Wu, 2003, Bone marrow stromal cells enhance differentiation of cocultured neurosphere cells and promote regeneration of injured spinal cord, J Neurosci Res, 72, 343, 10.1002/jnr.10587 Lalu, 2012, Safety of cell therapy with mesenchymal stromal cells (SafeCell): a systematic review and meta-analysis of clinical trials, PLoS One, 7, e47559, 10.1371/journal.pone.0047559 Koc, 2002, Mesenchymal stem cells. Allogeneic mesenchymal stem cell infusion for treatment of metachromatic leukodystrophy (MLD) and Hurler syndrome (MPS-IH), Bone Marrow Transplant, 30, 215, 10.1038/sj.bmt.1703650 Horwitz, 2002, Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone, Proc Natl Acad Sci U S A, 99, 8932, 10.1073/pnas.132252399 Chen-Plotkin, 2007, Encephalopathy, stroke and myocardial infarction with DMSO use in stem cell transplantation, Neurology, 68, 859, 10.1212/01.wnl.0000256716.04218.5b Moll, 2012, Are therapeutic human mesenchymal stromal cells compatible with human blood?, Stem Cells, 30, 1565, 10.1002/stem.1111 Breitbach, 2007, Potential risks of bone marrow cell transplantation into infarcted hearts, Blood, 110, 1362, 10.1182/blood-2006-12-063412 Kassis, 2008, Neuoprotection and immunomodulation with mesenchymal stem cells in chronic experimental autoimmune encephalomyelitis, Arch Neurol, 65, 753, 10.1001/archneur.65.6.753 Grigoriadis, 2011, Variable behavior and complications of autologous bone marrow mesenchymal stem cells transplanted in experimental autoimmune encephalomyelitis, Exp Neurol, 230, 78, 10.1016/j.expneurol.2011.02.021 von Bahr, 2012, Analysis of tissues following mesenchymal stromal cell therapy in humans indicate limited long-term engraftment and no ectopic tissue formation, Stem Cells, 30, 557, 10.1002/stem.1118 DelaRosa, 2010, Modulation of adult mesenchymal stem cells activity by toll-like receptors: implications on therapeutic potential, Mediators Inflamm, 2010, 865601, 10.1155/2010/865601 Waterman, 2010, A new mesenchymal stem cell (MSC) paradigm: polarization into a pro-inflammatory MSC1 or an immunosuppressive MSC2 phenotype, PLoS One, 5, e10088, 10.1371/journal.pone.0010088 Coles, 2008, Alemtuzumab vs. interferon beta-1a in early multiple sclerosis, N Engl J Med, 359, 1786, 10.1056/NEJMoa0802670 1999, The University of British Columbia MS/MRI Analysis Group. TNF neutralization in MS. Results of a randomized, placebo-controlled multicenter study, Neurology, 53, 457, 10.1212/WNL.53.3.457 Kishk, 2013, Possible induction of acute disseminated encephalomyelitis (ADEM)-like demyelinating illness by intrathecal mesenchymal stem cell injection, J Clin Neurosci, 20, 310, 10.1016/j.jocn.2012.04.013 Moyeddin Bonab, 2007, Does mesenchymal stem cell therapy help multiple sclerosis patients?, Iran J Immunol, 4, 50 Scolding, 2008, Autologous mesenchymal bone marrow stem cells: practical considerations, J Neurol Sci, 265, 111, 10.1016/j.jns.2007.08.009 Riordan, 2009, Non-expanded adipose stromal vascular fraction cell therapy for multiple sclerosis, J Transl Med, 7, 29, 10.1186/1479-5876-7-29 Yamout, 2010, Bone marrow mesenchymal stem cell transplantation in patients with multiple sclerosis: a pilot study, J Neuroimmunol, 227, 185, 10.1016/j.jneuroim.2010.07.013 Karussis, 2010, Safety and immunologic effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis, Arch Neurol, 67, 1187, 10.1001/archneurol.2010.248 Connick, 2012, Autologous mesenchymal stem cells for the treatment of secondary progressive multiple sclerosis: an open-label phase 2a proof-of-concept study, Lancet Neurol, 11, 150, 10.1016/S1474-4422(11)70305-2 Barkhof, 2003, Validation of diagnostic magnetic resonance imaging criteria for multiple sclerosis and response to interferon β1a, Ann Neurol, 53, 718, 10.1002/ana.10551 Tintore, 2003, New diagnostic criteria for multiple sclerosis. Application in first demyelinating episode, Neurology, 60, 27, 10.1212/WNL.60.1.27 Neuhuber, 2008, Effect of plating density and culture time on bone marrow stromal cell characteristics, Exp Hematol, 36, 1176, 10.1016/j.exphem.2008.03.019 Samuelsson, 2009, Optimizing in vitro conditions for immunomodulation and expansion of mesenchymal stromal cells, Cytotherapy, 11, 129, 10.1080/14653240802684194 Sundin, 2007, No alloantibodies against mesenchymal stromal cells, but presence of anti-fetal calf serum antibodies, after transplantation in allogeneic hematopoietic stem cell recipients, Haematologia (Budap), 92, 1208 Wagner, 2009, Optimizing mesenchymal stem cell-based theraputics, Curr Opin Biotechnol, 20, 1, 10.1016/j.copbio.2009.08.009 Lu, 2008, Overexpression of CNTF in mesenchymal stem cells reduces demyelination and induces clinical recovery in experimental autoimmune encephalomyelitis mice, J Neuroimmunol, 206, 58, 10.1016/j.jneuroim.2008.10.014 Pereira, 1995, Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice, Proc Natl Acad Sci U S A, 92, 4857, 10.1073/pnas.92.11.4857 Pereira, 1998, 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, 95, 1142, 10.1073/pnas.95.3.1142 Li, 2000, Evidence for migration of donor bone marrow stromal cells into recipient thymus after bone marrow transplantation plus bone grafts: a role of stromal cells in positive selection, Exp Hematol, 28, 950, 10.1016/S0301-472X(00)00483-5 Chen, 2001, Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats, Stroke, 32, 1005, 10.1161/01.STR.32.4.1005 Devine, 2001, Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion, Exp Hematol, 29, 244, 10.1016/S0301-472X(00)00635-4 Gao, 2001, The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion, Cells Tissues Organs, 169, 12, 10.1159/000047856 Wu, 2003, Migration of mesenchymal stem cells to heart allografts during chronic rejection, Transplantation, 75, 679, 10.1097/01.TP.0000048488.35010.95 Allers, 2004, Dynamic of distribution of human bone marrow-derived mesenchymal stem cells after transplantation into adult unconditioned mice, Transplantation, 78, 503, 10.1097/01.TP.0000128334.93343.B3 Niemeyer, 2008, Survival of human mesenchymal stromal cells from bone marrow and adipose tissue after xenogenic transplantation in immunocompetent mice, Cytotherapy, 10, 784, 10.1080/14653240802419302 Sokolova, 2007, Distribution of mesenchymal stem cells in the area of tissue inflammation after transplantation of the cell material via different routes, Bull Exp Biol Med, 143, 143, 10.1007/s10517-007-0036-8 Inoue, 2003, Comparative analysis of remyelinating potential of focal and intravenous administration of autologous bone marrow cells into the rat demyelinated spinal cord, Glia, 44, 111, 10.1002/glia.10285 Nakamizo, 2005, Human bone marrow-derived mesenchymal stem cells in the treatment of gliomas, Cancer Res, 65, 3307, 10.1158/0008-5472.CAN-04-1874 Chapel, 2003, Mesenchymal stem cells home to injured tissues when co-infused with hematopoietic cells to treat a radiation-induced multi-organ failure syndrome, J Gene Med, 5, 1028, 10.1002/jgm.452 Li, 2001, Treatment of stroke in rat with intracarotid administration of marrow stromal cells, Neurology, 56, 1666, 10.1212/WNL.56.12.1666 Lee, 2012, A randomized trial of mesenchymal stem cells in multiple system atrophy, Ann Neurol, 72, 32, 10.1002/ana.23612 Danielyan, 2009, Intranasal delivery of cells to the brain, Eur J Cell Biol, 88, 315, 10.1016/j.ejcb.2009.02.001 Danielyan, 2011, Therapeutic efficacy of intranasally delivered mesenchymal stem cells in a rat model of Parkinson disease, Rejuvenation Res, 14, 3, 10.1089/rej.2010.1130 Mohyeddin Bonab, 2007, Does mesenchymal stem cell therapy help multiple sclerosis patients? Report of a pilot study, Iran J Immunol, 4, 50 Liang, 2009, Allogeneic mesenchymal stem cells transplantation in treatment of multiple sclerosis, Mult Scler, 15, 644, 10.1177/1352458509104590 Rice, 2010, Safety and feasibility of autologous bone marrow cellular therapy in relapsing-progressive multiple sclerosis, Clin Pharmacol Ther, 87, 679, 10.1038/clpt.2010.44 Koc, 1999, Bone marrow-derived mesenchymal stem cells remain host-derived despite successful hematopoietic engraftment after allogeneic transplantation in patients with lysosomal and peroxisomal storage diseases, Exp Hematol, 27, 1675, 10.1016/S0301-472X(99)00101-0 Horwitz, 1999, Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta, Nat Med, 5, 309, 10.1038/6529 Ringden, 2006, Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease, Transplantation, 81, 1390, 10.1097/01.tp.0000214462.63943.14 Dominici, 2008, Donor cell-specific osteopoiesis originates from a self-renewing stem cell with a limited regenerative contribution after transplantation, Blood, 111, 4386, 10.1182/blood-2007-10-115725 Le Blanc, 2008, Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study, Lancet, 371, 1579, 10.1016/S0140-6736(08)60690-X Klyushnenkova, 2005, T cell responses to allogeneic human mesenchymal stem cells: immunogenicity, tolerance, and suppression, J Biomed Sci, 12, 47, 10.1007/s11373-004-8183-7 Rasmusson, 2007, Mesenchymal stem cells fail to trigger effector functions of cytotoxic T lymphocytes, J Leukoc Biol, 82, 887, 10.1189/jlb.0307140 Kebriaei, 2009, Adult human mesenchymal stem cells added to corticosteroid therapy for the treatment of acute graft-versus-host disease, Biol Blood Marrow Transplant, 15, 804, 10.1016/j.bbmt.2008.03.012 Hare, 2009, A randomized, double-blind, placebo-controlled, dose-escalation study of entravenous adult human mesenchymal stem cells (Prohymal) after acute myocardial infarction, J Am Coll Cardiol, 54, 2277, 10.1016/j.jacc.2009.06.055 Liang, 2010, Allogenic mesenchymal stem cell transplantation in refractory systemic lupus erythematosus: a pilot clinical study, Ann Rheum Dis, 69, 1423, 10.1136/ard.2009.123463 Horwitz, 2001, Clinical responses to bone marrow transplantation in children with severe osteogenesis perfecta, Blood, 97, 1227, 10.1182/blood.V97.5.1227 Cahill, 2004, Replacement of recipient stromal/mesenchymal cells after bone marrow transplantation using bone fragments and cultured osteoblast-like cells, Biol Blood Marrow Transplant, 10, 709, 10.1016/j.bbmt.2004.06.001 Zangi, 2009, Direct imaging of immune rejection and memory induction by allogeneic mesenchymal stromal cells, Stem Cells, 27, 2865, 10.1002/stem.217 Bacigalupo, 2005, T-cell suppression mediated by mesenchymal stem cells is deficient in patients with severe aplastic anemia, Exp Hematol, 33, 819, 10.1016/j.exphem.2005.05.006 Murphy, 2002, Reduced chondrogenic and adipogenic activity of mesenchymal stem cells from patients with advanced osteoarthritis, Arthritis Rheum, 46, 704, 10.1002/art.10118 Del Papa, 2006, Bone marrow endothelial progenitors are defective in systemic sclerosis, Arthritis Rheum, 54, 2605, 10.1002/art.22035 Kastrinaki, 2008, Functional, molecular and proteomic characterisation of bone marrow mesenchymal stem cells in rheumatoid arthritis, Ann Rheum Dis, 67, 741, 10.1136/ard.2007.076174 Bocelli-Tyndall, 2007, Bone marrow mesenchymal stromal cells (BM-MSCs) from healthy donors and auto-immune disease patients reduce the proliferation of autologous- and allogeneic-stimulated lymphocytes in vitro, Rheumatology (Oxford), 46, 403, 10.1093/rheumatology/kel267 Larghero, 2008, Phenotypical and functional characteristics of in vitro expanded bone marrow mesenchymal stem cells from patients with systemic sclerosis, Ann Rheum Dis, 67, 443, 10.1136/ard.2007.071233 Papadaki, 2005, Normal bone marrow hematopoietic stem cell reserves and normal stromal cell function support the use of autologous stem cell transplantation in patients with multiple sclerosis, Bone Marrow Transplant, 36, 1053, 10.1038/sj.bmt.1705179 Mallam, 2010, Characterization of in vitro expanded bone marrow-derived mesenchymal stem cells from patients with multiple sclerosis, Mult Scler, 16, 909, 10.1177/1352458510371959 Mazzanti, 2008, Differences in mesenchymal stem cell cytokine profiles between MS patients and healthy donors: implications for assessment of disease activity and treatment, J Neuroimmunol, 199, 142, 10.1016/j.jneuroim.2008.05.006