Harnessing the therapeutic potential of mesenchymal stem cells in multiple sclerosis

References

• Bar-Or A, Darlington PJ. The immunology of MS. In: MS Therapeutics (4th Edition). Cohen JA, Rudick RA (Eds). Cambridge University Press, Cambridge, UK (2011).
   Google Scholar
• Mendez-Ferrer S, Michurina TV, Ferraro F et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature466(7308), 829–834 (2010).
   PubMed Web of Science ®Google Scholar
• Horwitz EM, Le Blanc K, Dominici M et al. Clarification of the nomenclature for MSC: the International Society for Cellular Therapy position statement. Cytotherapy7(5), 393–395 (2005).
   PubMed Web of Science ®Google Scholar
• Devine SM, Bartholomew AM, Mahmud N et al. Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. Exp. Hematol.29(2), 244–255 (2001).
   PubMed Web of Science ®Google Scholar
• Flynn A, O’Brien T. Stem cell therapy for cardiac disease. Expert Opin. Biol. Ther.11(2), 177–187 (2011).
   PubMed Web of Science ®Google Scholar
• Kebriaei P, Robinson S. Treatment of graft-versus-host-disease with mesenchymal stromal cells. Cytotherapy13(3), 262–268 (2011).
   PubMed Web of Science ®Google Scholar
• Bartholomew A, Sturgeon C, Siatskas M et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp. Hematol.30(1), 42–48 (2002).
   PubMed Web of Science ®Google Scholar
• Krampera M, Glennie S, Dyson J et al. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood101(9), 3722–3729 (2003).
   PubMed Web of Science ®Google Scholar
• Potian JA, Aviv H, Ponzio NM, Harrison JS, Rameshwar P. Veto-like activity of mesenchymal stem cells: functional discrimination between cellular responses to alloantigens and recall antigens. J. Immunol.171(7), 3426–3434 (2003).
   PubMed Web of Science ®Google Scholar
• Uccelli A, Laroni A, Freedman MS. Mesenchymal stem cells for the treatment of multiple sclerosis and other neurological diseases. Lancet Neurol.10(7), 649–656 (2011).
   PubMed Web of Science ®Google Scholar
• Dazzi F, Krampera M. Mesenchymal stem cells and autoimmune diseases. Best Pract Res. Clin. Haematol.24(1), 49–57 (2011).
   Google Scholar
• Abreu SC, Antunes MA,Pelosi P, Morales MM, Rocco PR. Mechanisms of cellular therapy in respiratory diseases. Intensive Care Med. DOI: 10.1007/s00134-011-2268-3 (2011) (Epub ahead of print).
   Google Scholar
• Shi Y, Hu G, Su J et al. Mesenchymal stem cells: a new strategy for immunosuppression and tissue repair. Cell Res.20(5), 510–518 (2010).
   PubMed Web of Science ®Google Scholar
• Zappia E, Casazza S, Pedemonte E et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood106(5), 1755–1761 (2005).
   PubMed Web of Science ®Google Scholar
• Zhang J, Li Y, Chen J et al. Human bone marrow stromal cell treatment improves neurological functional recovery in EAE mice. Exp. Neurol.195(1), 16–26 (2005).
   PubMed Web of Science ®Google Scholar
• Gerdoni E, Gallo B, Casazza S et al. Mesenchymal stem cells effectively modulate pathogenic immune response in experimental autoimmune encephalomyelitis. Ann. Neurol.61(3), 219–227 (2007).
   PubMed Web of Science ®Google Scholar
• Pedemonte E, Benvenuto F, Casazza S et al. The molecular signature of therapeutic mesenchymal stem cells exposes the architecture of the hematopoietic stem cell niche synapse. BMC Genomics8, 65 (2007).
   PubMedGoogle Scholar
• Kassis I, Grigoriadis N, Gowda-Kurkalli B et al. Neuroprotection and immunomodulation with mesenchymal stem cells in chronic experimental autoimmune encephalomyelitis. Arch. Neurol.65(6), 753–761 (2008).
   PubMed Web of Science ®Google Scholar
• Bai L, Lennon DP, Eaton V et al. Human bone marrow-derived mesenchymal stem cells induce Th2-polarized immune response and promote endogenous repair in animal models of multiple sclerosis. Glia57(11), 1192–1203 (2009).
   PubMed Web of Science ®Google Scholar
• Constantin G, Marconi S, Rossi B et al. Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells27(10), 2624–2635 (2009).
   PubMed Web of Science ®Google Scholar
• Rafei M, Campeau PM, Aguilar-Mahecha A 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(10), 5994–6002 (2009).
   PubMed Web of Science ®Google Scholar
• Barhum Y, Gai-Castro S, Bahat-Stromza M, Barzilay R, Melamed E, Offen D. Intracerebroventricular transplantation of human mesenchymal stem cells induced to secrete neurotrophic factors attenuates clinical symptoms in a mouse model of multiple sclerosis. J. Mol. Neurosci.41(1), 129–137 (2010).
   Google Scholar
• Gordon D, Pavlovska G, Uney JB, Wraith DC, Scolding NJ. Human mesenchymal stem cells infiltrate the spinal cord, reduce demyelination, and localize to white matter lesions in experimental autoimmune encephalomyelitis. J. Neuropathol. Exp. Neurol.69(11), 1087–1095 (2010).
   PubMedGoogle Scholar
• Yamaza T, Kentaro A, Chen C et al. Immunomodulatory properties of stem cells from human exfoliated deciduous teeth. Stem Cell Res. Ther.1(1), 5 (2010).
   PubMed Web of Science ®Google Scholar
• Grigoriadis N, Lourbopoulos A, Lagoudaki R et al. Variable behavior and complications of autologous bone marrow mesenchymal stem cells transplanted in experimental autoimmune encephalomyelitis. Exp. Neurol.230(1), 78–89 (2011).
   Google Scholar
• Rafei M, Birman E, Forner K, Galipeau J. Allogeneic mesenchymal stem cells for treatment of experimental autoimmune encephalomyelitis. Mol. Ther.17(10), 1799–1803 (2009).
   PubMedGoogle Scholar
• Di Nicola M, Carlo-Stella C, Magni M et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood99(10), 3838–3843 (2002).
   PubMed Web of Science ®Google Scholar
• Tse WT, Pendleton JD, Beyer WM, Egalka MC, Guinan EC. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation75(3), 389–397 (2003).
   PubMed Web of Science ®Google Scholar
• Glennie S, Soeiro I, Dyson PJ, Lam EW, Dazzi F. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood105(7), 2821–2827 (2005).
   PubMed Web of Science ®Google Scholar
• Kang HS, Habib M, Chan J et al. A paradoxical role for IFN-γ in the immune properties of mesenchymal stem cells during viral challenge. Exp. Hematol.33(7), 796–803 (2005).
   PubMed Web of Science ®Google Scholar
• Liu XJ, Zhang JF, Sun B et al. Reciprocal effect of mesenchymal stem cell on experimental autoimmune encephalomyelitis is mediated by transforming growth factor-β and interleukin-6. Clin. Exp. Immunol.158(1), 37–44 (2009).
   Google Scholar
• Lanz TV, Opitz CA, Ho PP et al. Mouse mesenchymal stem cells suppress antigen-specific TH cell immunity independent of indoleamine 2,3-dioxygenase 1 (IDO1). Stem Cells Dev.19(5), 657–668 (2010).
   PubMedGoogle Scholar
• Ren G, Zhao X, Zhang L et al. Inflammatory cytokine-induced intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in mesenchymal stem cells are critical for immunosuppression. J. Immunol.184(5), 2321–2328 (2010).
   PubMed Web of Science ®Google Scholar
• Sato K, Ozaki K, Oh I et al. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood109(1), 228–234 (2007).
   PubMed Web of Science ®Google Scholar
• Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood105(4), 1815–1822 (2005).
   PubMed Web of Science ®Google Scholar
• Nasef A, Mathieu N, Chapel A et al. Immunosuppressive effects of mesenchymal stem cells: involvement of HLA-G. Transplantation84(2), 231–237 (2007).
   PubMed Web of Science ®Google Scholar
• Lepelletier Y, Lecourt S, Renand A et al. Galectin-1 and semaphorin-3A are two soluble factors conferring T-cell immunosuppression to bone marrow mesenchymal stem cell. Stem Cells Dev.19(7), 1075–1079 (2010).
   Web of Science ®Google Scholar
• Krampera M, Cosmi L, Angeli R et al. Role for interferon-γ in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells24(2), 386–398 (2006).
   PubMed Web of Science ®Google Scholar
• Skalnikova H, Motlik J, Gadher SJ, Kovarova H. Mapping of the secretome of primary isolates of mammalian cells, stem cells and derived cell lines. Proteomics11(4), 691–708 (2011).
   PubMed Web of Science ®Google Scholar
• Guo Z, Zheng C, Chen Z et al. Fetal BM-derived mesenchymal stem cells promote the expansion of human Th17 cells, but inhibit the production of Th1 cells. Eur. J. Immunol.39(10), 2840–2849 (2009).
   Google Scholar
• Darlington PJ, Boivin MN, Renoux C et al. Reciprocal Th1 and Th17 regulation by mesenchymal stem cells: implication for multiple sclerosis. Ann. Neurol.68(4), 540–545 (2010).
   PubMed Web of Science ®Google Scholar
• Corcione A, Benvenuto F, Ferretti E et al. Human mesenchymal stem cells modulate B-cell functions. Blood107(1), 367–372 (2006).
   PubMed Web of Science ®Google Scholar
• Tabera S, Perez-Simon JA, Diez-Campelo M et al. The effect of mesenchymal stem cells on the viability, proliferation and differentiation of B-lymphocytes. Haematologica93(9), 1301–1309 (2008).
   PubMed Web of Science ®Google Scholar
• Asari S, Itakura S, Ferreri K et al. Mesenchymal stem cells suppress B-cell terminal differentiation. Exp. Hematol.37(5), 604–615 (2009).
   PubMed Web of Science ®Google Scholar
• Aldinucci A, Rizzetto L, Pieri L et al. Inhibition of immune synapse by altered dendritic cell actin distribution: a new pathway of mesenchymal stem cell immune regulation. J. Immunol.185(9), 5102–5110 (2010).
   Google Scholar
• Zhang W, Ge W, Li C et al. Effects of mesenchymal stem cells on differentiation, maturation, and function of human monocyte-derived dendritic cells. Stem Cells Dev.13(3), 263–271 (2004).
   PubMed Web of Science ®Google Scholar
• Jiang XX, Zhang Y, Liu B et al. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood105(10), 4120–4126 (2005).
   PubMed Web of Science ®Google Scholar
• Wang Q, Sun B, Wang D et al. Murine bone marrow mesenchymal stem cells cause mature dendritic cells to promote T-cell tolerance. Scand. J. Immunol.68(6), 607–615 (2008).
   PubMed Web of Science ®Google Scholar
• Beyth S, Borovsky Z, Mevorach D et al. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood105(5), 2214–2219 (2005).
   PubMed Web of Science ®Google Scholar
• Maggini J, Mirkin G, Bognanni I et al. Mouse bone marrow-derived mesenchymal stromal cells turn activated macrophages into a regulatory-like profile. PLoS One5(2), e9252 (2010).
   PubMed Web of Science ®Google Scholar
• Prigione I, Benvenuto F, Bocca P, Battistini L, Uccelli A, Pistoia V. Reciprocal interactions between human mesenchymal stem cells and γδ T cells or invariant natural killer T cells. Stem Cells27(3), 693–702 (2009).
   PubMed Web of Science ®Google Scholar
• Mazzanti B, Aldinucci A, Biagioli T et al. Differences in mesenchymal stem cell cytokine profiles between MS patients and healthy donors: implication for assessment of disease activity and treatment. J. Neuroimmunol.199(1–2), 142–150 (2008).
   PubMed Web of Science ®Google Scholar
• Ferrari D, Gulinelli S, Salvestrini V et al. Purinergic stimulation of human mesenchymal stem cells potentiates their chemotactic response to CXCL12 and increases the homing capacity and production of proinflammatory cytokines. Exp. Hematol.39(3), 360–374 e1–5 (2011).
   Google Scholar
• Liotta F, Angeli R, Cosmi L et al. Toll-like receptors 3 and 4 are expressed by human bone marrow-derived mesenchymal stem cells and can inhibit their T-cell modulatory activity by impairing Notch signaling. Stem Cells26(1), 279–289 (2008).
   PubMed Web of Science ®Google Scholar
• Fruscione F, Scarfi S, Ferraris C et al. Regulation of human mesenchymal stem cell functions by an autocrine loop involving NAD+ release and P2Y11-mediated signaling. Stem Cells Dev.20(7), 1183–1198 (2010).
   Google Scholar
• Greco SJ, Rameshwar P. Microenvironmental considerations in the application of human mesenchymal stem cells in regenerative therapies. Biologics2(4), 699–705 (2008).
   PubMedGoogle Scholar
• Karussis D, Kassis I. The potential use of stem cells in multiple sclerosis: an overview of the preclinical experience. Clin. Neurol. Neurosurg.110(9), 889–896 (2008).
   Google Scholar
• Karussis D, Kassis I, Kurkalli BG, Slavin S. Immunomodulation and neuroprotection with mesenchymal bone marrow stem cells (MSCs): a proposed treatment for multiple sclerosis and other neuroimmunological/neurodegenerative diseases. J. Neurol. Sci.265(1–2), 131–135 (2008).
   PubMed Web of Science ®Google Scholar
• Freedman MS, Bar-Or A, Atkins HL et al. 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(4), 503–510 (2010).
   PubMed Web of Science ®Google Scholar
• Uccelli A, Benvenuto F, Laroni A, Giunti D. Neuroprotective features of mesenchymal stem cells. Best Pract. Res. Clin. Haematol.24(1), 59–64 (2011).
   PubMed Web of Science ®Google Scholar
• Uccelli A, Morando S, Bonanno S, Bonanni I, Leonardi A, Mancardi G. Mesenchymal stem cells for multiple sclerosis: does neural differentiation really matter? Curr. Stem Cell Res. Ther.6(1), 69–72 (2011).
   Google Scholar
• Gao J, Dennis JE, Muzic RF, Lundberg M, Caplan AI. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues Organs169(1), 12–20 (2001).
   PubMed Web of Science ®Google Scholar
• Devine SM, Cobbs C, Jennings M, Bartholomew A, Hoffman R. Mesenchymal stem cells distribute to a wide range of tissues following systemic infusion into nonhuman primates. Blood101(8), 2999–3001 (2003).
   PubMed Web of Science ®Google Scholar
• Barbash IM, Chouraqui P, Baron J et al. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: feasibility, cell migration, and body distribution. Circulation108(7), 863–868 (2003).
   PubMed Web of Science ®Google Scholar
• Sykova E, Jendelova P. Migration, fate and in vivo imaging of adult stem cells in the CNS. Cell Death Differ.14(7), 1336–1342 (2007).
   PubMed Web of Science ®Google Scholar
• Karussis D, Karageorgiou C, Vaknin-Dembinsky A et al. Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch. Neurol.67(10), 1187–1194 (2010).
   PubMed Web of Science ®Google Scholar
• Ji JF, He BP, Dheen ST, Tay SS. Interactions of chemokines and chemokine receptors mediate the migration of mesenchymal stem cells to the impaired site in the brain after hypoglossal nerve injury. Stem Cells22(3), 415–427 (2004).
   PubMed Web of Science ®Google Scholar
• Kassis I, Vaknin-Dembinsky A, Karussis D. Bone marrow mesenchymal stem cells: agents of immunomodulation and neuroprotection. Curr. Stem Cell Res. Ther.6(1), 63–68 (2011).
   PubMed Web of Science ®Google Scholar
• Rivera FJ, Siebzehnrubl FA, Kandasamy M et al. Mesenchymal stem cells promote oligodendroglial differentiation in hippocampal slice cultures. Cell Physiol. Biochem.24(3–4), 317–324 (2009).
   Google Scholar
• Cho JS, Park HW, Park SK et al. Transplantation of mesenchymal stem cells enhances axonal outgrowth and cell survival in an organotypic spinal cord slice culture. Neurosci. Lett.454(1), 43–48 (2009).
   PubMed Web of Science ®Google Scholar
• Cristofanilli M, Harris VK, Zigelbaum A et al. Mesenchymal stem cells enhance the engraftment and myelinating ability of allogeneic oligodendrocyte progenitors in dysmyelinated mice. Stem Cells Dev. DOI: 10.1089/scd.2010.0547 (2011) (Epub ahead of print).
   Google Scholar
• Matysiak M, Orlowski W, Fortak-Michalska M, Jurewicz A, Selmaj K. Immunoregulatory function of bone marrow mesenchymal stem cells in EAE depends on their differentiation state and secretion of PGE2. J. Neuroimmunol.233(1–2), 106–111 (2011).
   Google Scholar
• Wright KT, El Masri W, Osman A, Chowdhury J, Johnson WE. Bone marrow for the treatment of spinal cord injury: mechanisms and clinical application. Stem Cells29(2), 169–178 (2011).
   PubMed Web of Science ®Google Scholar
• Kemp K, Gordon D, Wraith DC et al. Fusion between human mesenchymal stem cells and rodent cerebellar Purkinje cells. Neuropathol. Appl. Neurobiol.37(2), 166–178 (2011).
   Google Scholar
• Liang J, Zhang H, Hua B et al. Allogeneic mesenchymal stem cells transplantation in treatment of multiple sclerosis. Mult. Scler.15(5), 644–646 (2009).
   PubMed Web of Science ®Google Scholar
• Mohyeddin Bonab M, Yazdanbakhsh S, Lotfi J et al. Does mesenchymal stem cell therapy help multiple sclerosis patients? Report of a pilot study. Iran J. Immunol.4(1), 50–57 (2007).
   PubMedGoogle Scholar
• Siatskas C, Payne NL, Short MA, Bernard CC. A consensus statement addressing mesenchymal stem cell transplantation for multiple sclerosis: it’s time! Stem Cell Rev.6(4), 500–506 (2010).
   Google Scholar
• Scolding N. Adult stem cells and multiple sclerosis. Cell Prolif.44(Suppl. 1), 35–38 (2011).
   Google Scholar
• Riordan NH, Ichim TE, Min WP et al. Non-expanded adipose stromal vascular fraction cell therapy for multiple sclerosis. J. Transl. Med.7, 29 (2009).
   PubMed Web of Science ®Google Scholar
• Yamout B, Hourani R, Salti H et al. Bone marrow mesenchymal stem cell transplantation in patients with multiple sclerosis: a pilot study. J. Neuroimmunol.227(1–2), 185–189 (2010).
   PubMed Web of Science ®Google Scholar
• Mahad DP, Cohen JA. Mesenchymal stem cell transplantation to treat multiple sclerosis. In: Multiple Sclerosis Therapeutics (4th Edition). Cohen JA, Rudick RA (Eds). Cambridge University Press, Cambridge, UK (2011).
   Google Scholar
• Connick P, Kolappan M, Patani R et al. The mesenchymal stem cells in multiple sclerosis (MSCIMS) trial protocol and baseline cohort characteristics: an open-label pre-test: post-test study with blinded outcome assessments. Trials12, 62 (2011).
   PubMed Web of Science ®Google Scholar