68
Views
18
CrossRef citations to date
0
Altmetric
Review

Use of stem cells for the treatment of multiple sclerosis

&
Pages 1189-1201 | Published online: 10 Jan 2014

References

  • Steinman L. Multiple sclerosis: a two-stage disease. Nat. Immunol.2(9), 762–764 (2001).
  • Einstein O, Grigoriadis N, Mizrachi-Kol R et al. Transplanted neural precursor cells reduce brain inflammation to attenuate chronic experimental autoimmune encephalomyelitis. Exp. Neurol.198(2), 275–284 (2006).
  • Einstein O, Ben-Menachem-Tzidon O, Mizrachi-Kol R et al. Survival of neural precursor cells in growth factor-poor environment: implications for transplantation in chronic disease. Glia53(4), 449–455 (2006).
  • Gehrmann J, Banati RB, Cuzner ML, Kreutzberg GW, Newcombe J. Amyloid precursor protein (APP) expression in multiple sclerosis lesions. Glia15(2), 141–151 (1995).
  • Foong J, Rozewicz L, Davie CA et al. Correlates of executive function in multiple sclerosis: the use of magnetic resonance spectroscopy as an index of focal pathology. J. Neuropsychiatry Clin. Neurosci.11(1), 45–50 (1999).
  • Trapp BD, Peterson J, Ransohoff RM et al. Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med.338(5), 278–285 (1998).
  • Vladimirova O, O’Connor J, Cahill A et al. Oxidative damage to DNA in plaques of MS brains. Mult. Scler.4(5), 413–418 (1998).
  • Lovas G, Szilagyi N, Majtenyi K, Palkovits M, Komoly S. Axonal changes in chronic demyelinated cervical spinal cord plaques. Brain123(Pt 2), 308–317 (2000).
  • Evangelou N, Esiri MM, Smith S, Palace J, Matthews PM. Quantitative pathological evidence for axonal loss in normal appearing white matter in multiple sclerosis. Ann. Neurol.47(3), 391–395 (2000).
  • Heins N, Englund MC, Sjoblom C et al. Derivation, characterization, and differentiation of human embryonic stem cells. Stem Cells22(3), 367–376 (2004).
  • Conley BJ, Young JC, Trounson AO, Mollard R. Derivation, propagation and differentiation of human embryonic stem cells. Int. J. Biochem. Cell Biol.36(4), 555–567 (2004).
  • Alessandri G, Pagano S, Bez A et al. Isolation and culture of human muscle-derived stem cells able to differentiate into myogenic and neurogenic cell lineages. Lancet364(9448), 1872–1883 (2004).
  • Gimble J, Guilak F. Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy5(5), 362–369 (2003).
  • Burnstein RM, Foltynie T, He X et al. Differentiation and migration of long term expanded human neural progenitors in a partial lesion model of Parkinson’s disease. Int. J. Biochem. Cell Biol.36(4), 702–713 (2004).
  • Bottai D, Fiocco R, Gelain F et al. Neural stem cells in the adult nervous system. J. Hematother. Stem Cell Res.12(6), 655–670 (2003).
  • Lennon DP, Caplan AI. Isolation of human marrow-derived mesenchymal stem cells. Exp. Hematol.34(11), 1604–1605 (2006).
  • Bernstein ID, Andrews RG, Rowley S. Isolation of human hematopoietic stem cells. Blood Cells20(1), 15–23; discussion 24 (1994).
  • Jiang Y, Vaessen B, Lenvik T et al. Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp. Hematol.30(8), 896–904 (2002).
  • Bain G, Kitchens D, Yao M, Huettner JE, Gottlieb DI. Embryonic stem cells express neuronal properties in vitro.Dev. Biol.168(2), 342–357 (1995).
  • Strubing C, Ahnert-Hilger G, Shan J et al. Differentiation of pluripotent embryonic stem cells into the neuronal lineage in vitro gives rise to mature inhibitory and excitatory neurons. Mech. Dev.53(2), 275–287 (1995).
  • Fraichard A, Chassande O, Bilbaut G et al.In vitro differentiation of embryonic stem cells into glial cells and functional neurons. J. Cell Sci.108(Pt 10), 3181–3188 (1995).
  • Reubinoff BE, Itsykson P, Turetsky T et al. Neural progenitors from human embryonic stem cells. Nat. Biotechnol.19(12), 1134–1140 (2001).
  • Benzing C, Segschneider M, Leinhaas A, Itskovitz-Eldor J, Brustle O. Neural conversion of human embryonic stem cell colonies in the presence of fibroblast growth factor-2. Neuroreport17(16), 1675–1681 (2006).
  • Kang SM, Cho MS, Seo H et al. Efficient induction of oligodendrocytes from human embryonic stem cells. Stem Cells25(2), 419–424 (2007).
  • Billon N, Jolicoeur C, Raff M. Generation and characterization of oligodendrocytes from lineage-selectable embryonic stem cells in vitro.Methods Mol. Biol.330, 15–32 (2006).
  • Mueller D, Shamblott MJ, Fox HE, Gearhart JD, Martin LJ. Transplanted human embryonic germ cell-derived neural stem cells replace neurons and oligodendrocytes in the forebrain of neonatal mice with excitotoxic brain damage. J. Neurosci. Res.82(5), 592–608 (2005).
  • Nistor GI, Totoiu MO, Haque N, Carpenter MK, Keirstead HS. Human embryonic stem cells differentiate into oligodendrocytes in high purity and myelinate after spinal cord transplantation. Glia49(3), 385–396 (2005).
  • Liu S, Qu Y, Stewart TJ et al. Embryonic stem cells differentiate into oligodendrocytes and myelinate in culture and after spinal cord transplantation. Proc. Natl Acad. Sci. USA97(11), 6126–6131 (2000).
  • Srivastava AS, Shenouda S, Mishra R, Carrier E. Transplanted embryonic stem cells successfully survive, proliferate, and migrate to damaged regions of the mouse brain. Stem Cells24(7), 1689–1694 (2006).
  • McDonald JW, Liu XZ, Qu Y et al. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat. Med.5(12), 1410–1412 (1999).
  • Brustle O, Jones KN, Learish RD et al. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science285(5428), 754–756 (1999).
  • Zeng L, Rahrmann E, Hu Q et al. Multipotent adult progenitor cells from swine bone marrow. Stem Cells24(11), 2355–2366 (2006).
  • Zhang SC, Wernig M, Duncan ID, Brustle O, Thomson JA. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol.19(12), 1129–1133 (2001).
  • Zhang PL, Izrael M, Ainbinder E et al. Increased myelinating capacity of embryonic stem cell derived oligodendrocyte precursors after treatment by interleukin-6/soluble interleukin-6 receptor fusion protein. Mol. Cell. Neurosci.31(3), 387–398 (2006).
  • Takagi Y, Takahashi J, Saiki H et al. Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J. Clin. Invest.115(1), 102–109 (2005).
  • Buhnemann C, Scholz A, Bernreuther C et al. Neuronal differentiation of transplanted embryonic stem cell-derived precursors in stroke lesions of adult rats. Brain129(Pt 12), 3238–3248 (2006).
  • Bhagavati S, Xu W. Generation of skeletal muscle from transplanted embryonic stem cells in dystrophic mice. Biochem. Biophys. Res. Commun.333(2), 644–649 (2005).
  • Kuai XL, Cong XQ, Du ZW, Bian YH, Xiao SD. Treatment of surgically induced acute liver failure by transplantation of HNF4-overexpressing embryonic stem cells. Chin. J. Dig. Dis.7(2), 109–116 (2006).
  • Min JY, Yang Y, Sullivan MF et al. Long-term improvement of cardiac function in rats after infarction by transplantation of embryonic stem cells. J. Thorac. Cardiovasc. Surg.125(2), 361–369 (2003).
  • Kim JH, Auerbach JM, Rodriguez-Gomez JA et al. Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson’s disease. Nature418(6893), 50–56 (2002).
  • Carpenter M, Rao MS, Freed W, Zeng X. Derivation and characterization of neuronal precursors and dopaminergic neurons from human embryonic stem cells in vitro.Methods Mol. Biol.331, 153–167 (2006).
  • Nishimura F, Toriumi H, Ishizaka S, Sakaki T, Yoshikawa M. Use of differentiating embryonic stem cells in the Parkinsonian mouse model. Methods Mol. Biol.329, 485–493 (2006).
  • Brederlau A, Correia AS, Anisimov SV et al. Transplantation of human embryonic stem cell-derived cells to a rat model of Parkinson’s disease: effect of in vitro differentiation on graft survival and teratoma formation. Stem Cells24(6), 1433–1440 (2006).
  • Cho YH, Kim DS, Kim PG et al. Dopamine neurons derived from embryonic stem cells efficiently induce behavioral recovery in a Parkinsonian rat model. Biochem. Biophys. Res. Commun.341(1), 6–12 (2006).
  • Yoshizaki T, Inaji M, Kouike H et al. Isolation and transplantation of dopaminergic neurons generated from mouse embryonic stem cells. Neurosci. Lett.363(1), 33–37 (2004).
  • Bjorklund LM, Sanchez-Pernaute R, Chung S et al. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc. Natl Acad. Sci. USA99(4), 2344–2349 (2002).
  • Nakao N, Yokote H, Nakai K, Itakura T. Promotion of survival and regeneration of nigral dopamine neurons in a rat model of Parkinson’s disease after implantation of embryonal carcinoma-derived neurons genetically engineered to produce glial cell line-derived neurotrophic factor. J. Neurosurg.92(4), 659–670 (2000).
  • Zhang SC. Embryonic stem cells for neural replacement therapy: prospects and challenges. J. Hematother. Stem Cell Res.12(6), 625–634 (2003).
  • Senior K. Embryonic stem cells used to remyelinate injured rat spinal cord neurons. Lancet355(9218), 1890 (2000).
  • Hendricks WA, Pak ES, Owensby JP et al. Predifferentiated embryonic stem cells prevent chronic pain behaviors and restore sensory function following spinal cord injury in mice. Mol. Med.12(1–3), 34–46 (2006).
  • Lerou PH, Daley GQ. Therapeutic potential of embryonic stem cells. Blood Rev.19(6), 321–331 (2005).
  • Kimura H, Yoshikawa M, Matsuda R et al. Transplantation of embryonic stem cell-derived neural stem cells for spinal cord injury in adult mice. Neurol. Res.27(8), 812–819 (2005).
  • Grabowski M, Brundin P, Johansson BB. Fetal neocortical grafts implanted in adult hypertensive rats with cortical infarcts following a middle cerebral artery occlusion: ingrowth of afferent fibers from the host brain. Exp. Neurol.116(2), 105–121 (1992).
  • Grabowski M, Christofferson RH, Brundin P, Johansson BB. Vascularization of fetal neocortical grafts implanted in brain infarcts in spontaneously hypertensive rats. Neuroscience51(3), 673–682 (1992).
  • Chopko BW, Voneida TJ. Fetal rat cerebellar fragment transplantation into adult rat forebrain lesion cavities. J. Neural Transplant. Plast.3(1), 63–69 (1992).
  • Fiandaca MS, Gash DM. New insights and technologies in brain grafting. Clin. Neurosurg.39, 482–508 (1992).
  • Jiao S, Wolff JA. Long-term survival of autologous muscle grafts in rat brain. Neurosci. Lett.137(2), 207–210 (1992).
  • Wirth ED 3rd, Theele DP, Mareci TH et al.In vivo magnetic resonance imaging of fetal cat neural tissue transplants in the adult cat spinal cord. J. Neurosurg.76(2), 261–274 (1992).
  • Deacon T, Dinsmore J, Costantini LC, Ratliff J, Isacson O. Blastula-stage stem cells can differentiate into dopaminergic and serotonergic neurons after transplantation. Exp. Neurol.149(1), 28–41 (1998).
  • Yanai J, Doetchman T, Laufer N et al. Embryonic cultures but not embryos transplanted to the mouse’s brain grow rapidly without immunosuppression. Int. J. Neurosci.81(1–2), 21–26 (1995).
  • Drukker M, Katchman H, Katz G et al. Human embryonic stem cells and their differentiated derivatives are less susceptible to immune rejection than adult cells. Stem Cells24(2), 221–229 (2006).
  • Wognum AW, Eaves AC, Thomas TE. Identification and isolation of hematopoietic stem cells. Arch. Med. Res.34(6), 461–475 (2003).
  • Huss R. Isolation of primary and immortalized CD34-hematopoietic and mesenchymal stem cells from various sources. Stem Cells18(1), 1–9 (2000).
  • Pittenger MF, Mackay AM, Beck SC et al. Multilineage potential of adult human mesenchymal stem cells. Science284(5411), 143–147 (1999).
  • Lennon DP, Caplan AI. Isolation of rat marrow-derived mesenchymal stem cells. Exp. Hematol.34(11), 1606–1607 (2006).
  • Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science276(5309), 71–74 (1997).
  • Verfaillie CM. Multipotent adult progenitor cells: an update. Novartis Found. Symp.265, 55–61; discussion 61–55, 92–57 (2005).
  • Raedt R, Pinxteren J, Van Dycke A et al. Differentiation assays of bone marrow-derived multipotent adult progenitor cell (MAPC)-like cells towards neural cells cannot depend on morphology and a limited set of neural markers. Exp. Neurol.203(2), 542–554 (2007).
  • Woodward WA, Chen MS, Behbod F, Rosen JM. On mammary stem cells. J. Cell Sci.118(Pt 16), 3585–3594 (2005).
  • Clarke RB. Isolation and characterization of human mammary stem cells. Cell Prolif.38(6), 375–386 (2005).
  • Capuco AV, Ellis S. Bovine mammary progenitor cells: current concepts and future directions. J. Mammary Gland Biol. Neoplasia10(1), 5–15 (2005).
  • Roisen FJ, Klueber KM, Lu CL et al. Adult human olfactory stem cells. Brain Res.890(1), 11–22 (2001).
  • Frank MH, Sayegh MH. Immunomodulatory functions of mesenchymal stem cells. Lancet363(9419), 1411–1412 (2004).
  • Yu JJ, Sun X, Yuan X et al. Immunomodulatory neural stem cells for brain tumour therapy. Expert Opin. Biol. Ther.6(12), 1255–1262 (2006).
  • Krampera M, Pasini A, Pizzolo G et al. Regenerative and immunomodulatory potential of mesenchymal stem cells. Curr. Opin. Pharmacol.6(4), 435–441 (2006).
  • Puissant B, Barreau C, Bourin P et al. Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br. J. Haematol.129(1), 118–129 (2005).
  • Hsu YC, Lee DC, Chiu IM. Neural stem cells, neural progenitors, and neurotrophic factors. Cell Transplant.16(2), 133–150 (2007).
  • Campos LS. Neurospheres: insights into neural stem cell biology. J. Neurosci. Res.78(6), 761–769 (2004).
  • Cameron HA, Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience61(2), 203–209 (1994).
  • Eriksson PS, Perfilieva E, Bjork-Eriksson T et al. Neurogenesis in the adult human hippocampus. Nat. Med.4(11), 1313–1317 (1998).
  • Gould E, Reeves AJ, Fallah M et al. Hippocampal neurogenesis in adult Old World primates. Proc. Natl Acad. Sci. USA96(9), 5263–5267 (1999).
  • Kornack DR, Rakic P. Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc. Natl Acad. Sci. USA96(10), 5768–5773 (1999).
  • Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell97(6), 703–716 (1999).
  • Alvarez-Buylla A, Herrera DG, Wichterle H. The subventricular zone: source of neuronal precursors for brain repair. Prog. Brain Res.127, 1–11 (2000).
  • Pluchino S, Quattrini A, Brambilla E et al. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature422(6933), 688–694 (2003).
  • Ben-Hur T, Einstein O, Mizrachi-Kol R et al. Transplanted multipotential neural precursor cells migrate into the inflamed white matter in response to experimental autoimmune encephalomyelitis. Glia41(1), 73–80 (2003).
  • Einstein O, Fainstein N, Vaknin I et al. Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression. Ann. Neurol.61(3), 209–218 (2007).
  • Belmadani A, Tran PB, Ren D, Miller RJ. Chemokines regulate the migration of neural progenitors to sites of neuroinflammation. J. Neurosci.26(12), 3182–3191 (2006).
  • Yasuhara T, Matsukawa N, Hara K et al. Transplantation of human neural stem cells exerts neuroprotection in a rat model of Parkinson’s disease. J. Neurosci.26(48), 12497–12511 (2006).
  • Harrower TP, Tyers P, Hooks Y, Barker RA. Long-term survival and integration of porcine expanded neural precursor cell grafts in a rat model of Parkinson’s disease. Exp. Neurol.197(1), 56–69 (2006).
  • Ben-Hur T, Idelson M, Khaner H et al. Transplantation of human embryonic stem cell-derived neural progenitors improves behavioral deficit in Parkinsonian rats. Stem Cells22(7), 1246–1255 (2004).
  • Snyder BJ, Olanow CW. Stem cell treatment for Parkinson’s disease: an update for 2005. Curr. Opin. Neurol.18(4), 376–385 (2005).
  • Lindvall O. Parkinson disease. Stem cell transplantation. Lancet358(Suppl.), S48 (2001).
  • Teng YD, Lavik EB, Qu X et al. Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proc. Natl Acad. Sci. USA99(5), 3024–3029 (2002).
  • Iwanami A, Kaneko S, Nakamura M et al. Transplantation of human neural stem cells for spinal cord injury in primates. J. Neurosci. Res.80(2), 182–190 (2005).
  • Okano H, Ogawa Y, Nakamura M et al. Transplantation of neural stem cells into the spinal cord after injury. Semin. Cell Dev. Biol.14(3), 191–198 (2003).
  • Pallini R, Vitiani LR, Bez A et al. Homologous transplantation of neural stem cells to the injured spinal cord of mice. Neurosurgery57(5), 1014–1025; discussion 1014–1025 (2005).
  • Ogawa Y, Sawamoto K, Miyata T et al. Transplantation of in vitro expanded fetal neural progenitor cells results in neurogenesis and functional recovery after spinal cord contusion injury in adult rats. J. Neurosci. Res.69(6), 925–933 (2002).
  • Cummings BJ, Uchida N, Tamaki SJ, Anderson AJ. Human neural stem cell differentiation following transplantation into spinal cord injured mice: association with recovery of locomotor function. Neurol. Res.28(5), 474–481 (2006).
  • Shihabuddin LS, Horner PJ, Ray J, Gage FH. Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J. Neurosci.20(23), 8727–8735 (2000).
  • Doetsch F, Verdugo JM, Caille I et al. Lack of the cell-cycle inhibitor p27Kip1 results in selective increase of transit-amplifying cells for adult neurogenesis. J. Neurosci.22(6), 2255–2264 (2002).
  • Marshall GP 2nd, Laywell ED, Zheng T, Steindler DA, Scott EW. In vitro-derived “neural stem cells” function as neural progenitors without the capacity for self-renewal. Stem Cells24(3), 731–738 (2006).
  • Gallacher L, Murdoch B, Wu DM et al. Isolation and characterization of human CD34-Lin- and CD34+Lin- hematopoietic stem cells using cell surface markers AC133 and CD7. Blood95(9), 2813–2820 (2000).
  • Brazelton TR, Rossi FM, Keshet GI, Blau HM. From marrow to brain: expression of neuronal phenotypes in adult mice. Science290(5497), 1775–1779 (2000).
  • Eglitis MA, Mezey E. Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc. Natl Acad. Sci. USA94(8), 4080–4085 (1997).
  • Locatelli F, Corti S, Donadoni C et al. Neuronal differentiation of murine bone marrow Thy-1- and Sca-1-positive cells. J. Hematother. Stem Cell Res.12(6), 727–734 (2003).
  • Mezey E, Chandross KJ, Harta G, Maki RA, McKercher SR. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science290(5497), 1779–1782 (2000).
  • Karussis DM, Vourka-Karussis U, Mizrachi-Koll R, Abramsky O. Acute/relapsing experimental autoimmune encephalomyelitis: induction of long lasting, antigen-specific tolerance by syngeneic bone marrow transplantation. Mult. Scler.5(1), 17–21 (1999).
  • Karussis DM, Slavin S, Ben-Nun A et al. Chronic-relapsing experimental autoimmune encephalomyelitis (CR-EAE): treatment and induction of tolerance, with high dose cyclophosphamide followed by syngeneic bone marrow transplantation. J. Neuroimmunol.39(3), 201–210 (1992).
  • Karussis DM, Slavin S, Lehmann D et al. Prevention of experimental autoimmune encephalomyelitis and induction of tolerance with acute immunosuppression followed by syngeneic bone marrow transplantation. J. Immunol.148(6), 1693–1698 (1992).
  • Karussis DM, Vourka-Karussis U, Lehmann D et al. Immunomodulation of autoimmunity in MRL/lpr mice with syngeneic bone marrow transplantation (SBMT). Clin. Exp. Immunol.100(1), 111–117 (1995).
  • Karussis DM, Vourka-Karussis U, Lehmann D et al. Prevention and reversal of adoptively transferred, chronic relapsing experimental autoimmune encephalomyelitis with a single high dose cytoreductive treatment followed by syngeneic bone marrow transplantation. J. Clin. Invest.92(2), 765–772 (1993).
  • van Gelder M, van Bekkum DW. Effective treatment of relapsing experimental autoimmune encephalomyelitis with pseudoautologous bone marrow transplantation. Bone Marrow Transplant.18(6), 1029–1034 (1996).
  • van Gelder M, van Bekkum DW. Treatment of relapsing experimental autoimmune encephalomyelitis in rats with allogeneic bone marrow transplantation from a resistant strain. Bone Marrow Transplant.16(3), 343–351 (1995).
  • Nash RA, Bowen JD, McSweeney PA et al. High-dose immunosuppressive therapy and autologous peripheral blood stem cell transplantation for severe multiple sclerosis. Blood102(7), 2364–2372 (2003).
  • Saccardi R, Kozak T, Bocelli-Tyndall C et al. Autologous stem cell transplantation for progressive multiple sclerosis: update of the European Group for Blood and Marrow Transplantation autoimmune diseases working party database. Mult. Scler.12(6), 814–823 (2006).
  • Mancardi GL, Saccardi R, Filippi M et al. Autologous hematopoietic stem cell transplantation suppresses Gd-enhanced MRI activity in MS. Neurology57(1), 62–68 (2001).
  • Fassas A, Passweg JR, Anagnostopoulos A et al. Hematopoietic stem cell transplantation for multiple sclerosis. A retrospective multicenter study. J. Neurol.249(8), 1088–1097 (2002).
  • Muraro PA, Douek DC. Renewing the T cell repertoire to arrest autoimmune aggression. Trends Immunol.27(2), 61–67 (2006).
  • Muraro PA, Douek DC, Packer A et al. Thymic output generates a new and diverse TCR repertoire after autologous stem cell transplantation in multiple sclerosis patients. J. Exp. Med.201(5), 805–816 (2005).
  • Minagawa H, Takenaka A, Itoyama Y, Mori R. Experimental allergic encephalomyelitis in the Lewis rat. A model of predictable relapse by cyclophosphamide. J. Neurol. Sci.78(2), 225–235 (1987).
  • Miyazaki C, Nakamura T, Kaneko K, Mori R, Shibasaki H. Reinduction of experimental allergic encephalomyelitis in convalescent Lewis rats with cyclophosphamide. J. Neurol. Sci.67(3), 277–284 (1985).
  • Polman CH, Matthaei I, de Groot CJ et al. Low-dose cyclosporin A induces relapsing remitting experimental allergic encephalomyelitis in the Lewis rat. J. Neuroimmunol.17(3), 209–216 (1988).
  • Chen JT, Collins DL, Atkins HL et al. Brain atrophy after immunoablation and stem cell transplantation in multiple sclerosis. Neurology66(12), 1935–1937 (2006).
  • Inglese M, Mancardi GL, Pagani E et al. Brain tissue loss occurs after suppression of enhancement in patients with multiple sclerosis treated with autologous haematopoietic stem cell transplantation. J. Neurol. Neurosurg. Psychiatry75(4), 643–644 (2004).
  • Bossolasco P, Cova L, Calzarossa C et al. Neuro-glial differentiation of human bone marrow stem cells in vitro.Exp. Neurol.193(2), 312–325 (2005).
  • Oswald J, Boxberger S, Jorgensen B et al. Mesenchymal stem cells can be differentiated into endothelial cells in vitro.Stem Cells22(3), 377–384 (2004).
  • Talens-Visconti R, Bonora A, Jover R et al. Hepatogenic differentiation of human mesenchymal stem cells from adipose tissue in comparison with bone marrow mesenchymal stem cells. World J. Gastroenterol.12(36), 5834–5845 (2006).
  • Sanchez-Ramos J, Song S, Cardozo-Pelaez F et al. Adult bone marrow stromal cells differentiate into neural cells in vitro.Exp. Neurol.164(2), 247–256 (2000).
  • Woodbury D, Schwarz EJ, Prockop DJ, Black IB. Adult rat and human bone marrow stromal cells differentiate into neurons. J. Neurosci. Res.61(4), 364–370 (2000).
  • 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).
  • Uccelli A, Moretta L, Pistoia V. Immunoregulatory function of mesenchymal stem cells. Eur. J. Immunol.36(10), 2566–2573 (2006).
  • Crigler L, Robey RC, Asawachaicharn A, Gaupp D, Phinney DG. Human mesenchymal stem cell subpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. Exp. Neurol.198(1), 54–64 (2006).
  • Spaggiari GM, Capobianco A, Becchetti S, Mingari MC, Moretta L. Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation. Blood107(4), 1484–1490 (2006).
  • Sotiropoulou PA, Perez SA, Gritzapis AD, Baxevanis CN, Papamichail M. Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells24(1), 74–85 (2006).
  • Le Blanc K, Tammik L, Sundberg B, Haynesworth SE, Ringden O. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand. J. Immunol.57(1), 11–20 (2003).
  • Deng W, Han Q, Liao L et al. Effects of allogeneic bone marrow-derived mesenchymal stem cells on T and B lymphocytes from BXSB mice. DNA Cell Biol.24(7), 458–463 (2005).
  • 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).
  • Augello A, Tasso R, Negrini SM et al. Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur. J. Immunol.35(5), 1482–1490 (2005).
  • Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood105(4), 1815–1822 (2005).
  • 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).
  • Corcione A, Benvenuto F, Ferretti E et al. Human mesenchymal stem cells modulate B-cell functions. Blood107(1), 367–372 (2006).
  • 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).
  • 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).
  • 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).
  • Meisel R, Zibert A, Laryea M et al. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood103(12), 4619–4621 (2004).
  • Rasmusson I, Ringden O, Sundberg B, Le Blanc K. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation76(8), 1208–1213 (2003).
  • 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).
  • 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).
  • Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp. Hematol.31(10), 890–896 (2003).
  • 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).
  • Zappia E, Casazza S, Pedemonte E et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood106(5), 1755–1761 (2005).
  • 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).
  • 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).
  • Inoue M, Honmou O, Oka S et al. Comparative analysis of remyelinating potential of focal and intravenous administration of autologous bone marrow cells into the rat demyelinated spinal cord. Glia44(2), 111–118 (2003).
  • Karussis DM, Grigoriadis N, Ben-Hur T et al. Mesenchymal bone marrow stem cells, migrate into CNS lesions in experimental autoimmune encephalomyelitis, differentiate into neuronal and glial line and downregulate chronic EAE. Neurology64(6), A407 (2005).
  • Giordano A, Galderisi U, Marino IR. From the laboratory bench to the patient’s bedside: an update on clinical trials with mesenchymal stem cells. J. Cell. Physiol.211(1), 27–35 (2007).
  • Chen SL, Fang WW, Ye F et al. Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am. J. Cardiol.94(1), 92–95 (2004).
  • Wollert KC, Meyer GP, Lotz J et al. Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet364(9429), 141–148 (2004).
  • Katritsis DG, Sotiropoulou PA, Karvouni E et al. Transcoronary transplantation of autologous mesenchymal stem cells and endothelial progenitors into infarcted human myocardium. Catheter Cardiovasc. Interv.65(3), 321–329 (2005).
  • Perin EC, Dohmann HF, Borojevic R et al. Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation107(18), 2294–2302 (2003).
  • Perin EC, Dohmann HF, Borojevic R et al. Improved exercise capacity and ischemia 6 and 12 months after transendocardial injection of autologous bone marrow mononuclear cells for ischemic cardiomyopathy. Circulation110(11 Suppl. 1), II213–II218 (2004).
  • Janssens S, Dubois C, Bogaert J et al. Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind, randomised controlled trial. Lancet367(9505), 113–121 (2006).
  • Lunde K, Solheim S, Aakhus S et al. Autologous stem cell transplantation in acute myocardial infarction: The ASTAMI randomized controlled trial. Intracoronary transplantation of autologous mononuclear bone marrow cells, study design and safety aspects. Scand. Cardiovasc. J.39(3), 150–158 (2005).
  • Meyer GP, Wollert KC, Lotz J et al. Intracoronary bone marrow cell transfer after myocardial infarction: eighteen months’ follow-up data from the randomized, controlled BOOST (BOne marrOw transfer to enhance ST-elevation infarct regeneration) trial. Circulation113(10), 1287–1294 (2006).
  • Rosenzweig A. Cardiac cell therapy – mixed results from mixed cells. N. Engl. J. Med.355(12), 1274–1277 (2006).
  • Welt FG, Losordo DW. Cell therapy for acute myocardial infarction: curb your enthusiasm? Circulation113(10), 1272–1274 (2006).
  • Ferrari G, Cusella-De Angelis G, Coletta M et al. Muscle regeneration by bone marrow-derived myogenic progenitors. Science279(5356), 1528–1530 (1998).
  • Horwitz EM, Prockop DJ, Fitzpatrick LA et al. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat. Med.5(3), 309–313 (1999).
  • Horwitz EM, Prockop DJ, Gordon PL et al. Clinical responses to bone marrow transplantation in children with severe osteogenesis imperfecta. Blood97(5), 1227–1231 (2001).
  • Koc ON, Day J, Nieder M et al. Allogeneic mesenchymal stem cell infusion for treatment of metachromatic leukodystrophy (MLD) and Hurler syndrome (MPS-IH). Bone Marrow Transplant.30(4), 215–222 (2002).
  • Koc ON, Gerson SL, Cooper BW et al. Rapid hematopoietic recovery after coinfusion of autologous-blood stem cells and culture-expanded marrow mesenchymal stem cells in advanced breast cancer patients receiving high-dose chemotherapy. J. Clin. Oncol.18(2), 307–316 (2000).
  • Lazarus HM. Bone marrow transplantation in low-grade non-Hodgkin’s lymphoma. Leuk. Lymphoma17(3–4), 199–210 (1995).
  • Lazarus HM, Haynesworth SE, Gerson SL, Rosenthal NS, Caplan AI. Ex vivo expansion and subsequent infusion of human bone marrow-derived stromal progenitor cells (mesenchymal progenitor cells): implications for therapeutic use. Bone Marrow Transplant.16(4), 557–564 (1995).
  • Lazarus HM, Koc ON, Devine SM et al. Cotransplantation of HLA-identical sibling culture-expanded mesenchymal stem cells and hematopoietic stem cells in hematologic malignancy patients. Biol. Blood Marrow Transplant.11(5), 389–398 (2005).
  • Lazarus HM, Winton EF, Williams SF et al. Phase I multicenter trial of interleukin 6 therapy after autologous bone marrow transplantation in advanced breast cancer. Bone Marrow Transplant.15(6), 935–942 (1995).
  • Mazzini L, Mareschi K, Ferrero I et al. Autologous mesenchymal stem cells: clinical applications in amyotrophic lateral sclerosis. Neurol. Res.28(5), 523–526 (2006).
  • Karussis D, Kassis I, Basan GS, Slavin S. Immunomodulation and neuroprotection with mesenchymal bone marrow stem cells (MSCs): a porposed treatment for multiple sclerosis and other neuroimmunological/neurodegenerative diseases. J. Neurol. Sci. (2007) (Epub ahead of print).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.