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Mesenchymal Stem Cell Therapy for the Treatment of Amyotrophic Lateral Sclerosis: Signals for Hope?

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Pages 637-647 | Published online: 05 Nov 2014

References

  • Janson CG , RameshTM , DuringMJ , LeoneP , HeywoodJ . Human intrathecal transplantation of peripheral blood stem cells in amyotrophic lateral sclerosis . J. Hematother. Stem Cell Res.10 ( 6 ), 913 – 915 ( 2001 ).
  • NINDS Amyotrophic Lateral Sclerosis (ALS) Fact Sheet . www.ninds.nih.gov/disorders/amyotrophiclateralsclerosis/detail_ALS.htm#244954842
  • Robberecht W , PhilipsT . The changing scene of amyotrophic lateral sclerosis . Nat. Rev. Neurosci.14 ( 4 ), 248 – 264 ( 2013 ).
  • Nishitoh H , KadowakiH , NagaiAet al. ALS-linked mutant SOD1 induces ER stress- and ASK1-dependent motor neuron death by targeting Derlin-1 . Genes Dev.22 ( 11 ), 1451 – 1464 ( 2008 ).
  • Seetharaman SV , PrudencioM , KarchC , HollowaySP , BorcheltDR , HartPJ . Immature copper-zinc superoxide dismutase and familial amyotrophic lateral sclerosis . Exp. Biol. Med. (Maywood)234 ( 10 ), 1140 – 1154 ( 2009 ).
  • Fujisawa T , HommaK , YamaguchiNet al. A novel monoclonal antibody reveals a conformational alteration shared by amyotrophic lateral sclerosis-linked SOD1 mutants . Ann. Neurol.72 ( 5 ), 739 – 749 ( 2012 ).
  • Da Cruz S , ClevelandDW . Understanding the role of TDP-43 and FUS/TLS in ALS and beyond . Curr. Opin. Neurobiol.21 ( 6 ), 904 – 919 ( 2011 ).
  • Xu ZS . Does a loss of TDP-43 function cause neurodegeneration?Mol. Neurodegener.7 , 27 ( 2012 ).
  • Wang Q , ZhangX , ChenS , ZhangS , YoudiumM , LeW . Prevention of motor neuron degeneration by novel iron chelators in SOD1(G93A) transgenic mice of amyotrophic lateral sclerosis . Neurodegener. Dis.8 ( 5 ), 310 – 321 ( 2011 ).
  • Del Aguila MA , LongstrethWTJr , McguireV , KoepsellTD , Van BelleG . Prognosis in amyotrophic lateral sclerosis: a population-based study . Neurology60 ( 5 ), 813 – 819 ( 2003 ).
  • Traynor BJ , ZhangH , ShefnerJM , SchoenfeldD , CudkowiczME . Functional outcome measures as clinical trial endpoints in ALS . Neurology63 ( 10 ), 1933 – 1935 ( 2004 ).
  • Millul A , BeghiE , LogroscinoG , MicheliA , VitelliE , ZardiA . Survival of patients with amyotrophic lateral sclerosis in a population-based registry . Neuroepidemiology25 ( 3 ), 114 – 119 ( 2005 ).
  • Corcia P , GordonPH . Amyotrophic lateral sclerosis and the clinical potential of dexpramipexole . Ther. Clin. Risk Manag.8 , 359 – 366 ( 2012 ).
  • Miller RG , MitchellJD , MooreDH . Riluzole for amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND) . Cochrane Database Syst Rev.3 , CD001447 ( 2012 ).
  • Bova MP , KinneyGG . Emerging drug targets in amyotrophic lateral sclerosis . Expert Opin. Orphan Drugs1 ( 1 ), 5 – 20 ( 2013 ).
  • Orrell RW , LaneRJ , RossM . A systematic review of antioxidant treatment for amyotrophic lateral sclerosis/motor neuron disease . Amyotroph. Lateral Scler.9 ( 4 ), 195 – 211 ( 2008 ).
  • Zhang X , HongYL , XuDSet al. A review of experimental research on herbal compounds in amyotrophic lateral sclerosis . Phytother. Res.28 ( 1 ), 9 – 21 ( 2013 ).
  • Hoffmann M . Linking respiratory chain uncoupling to amyotrophic lateral sclerosis implies potential treatment with herbal extracts containing genipin . Med. Hypotheses80 ( 3 ), 327 ( 2013 ).
  • Silani V , CovaL , CorboM , CiammolaA , PolliE . Stem-cell therapy for amyotrophic lateral sclerosis . Lancet364 ( 9429 ), 200 – 202 ( 2004 ).
  • Thonhoff JR , OjedaL , WuP . Stem cell-derived motor neurons: applications and challenges in amyotrophic lateral sclerosis . Curr. Stem Cell Res. Ther.4 ( 3 ), 178 – 199 ( 2009 ).
  • Lepore AC , O’DonnellJ , KimASet al. Human glial-restricted progenitor transplantation into cervical spinal cord of the SOD1 mouse model of ALS . PLoS ONE6 ( 10 ), e25968 ( 2011 ).
  • Hefferan MP , GalikJ , KakinohanaOet al. Human neural stem cell replacement therapy for amyotrophic lateral sclerosis by spinal transplantation . PLoS ONE7 ( 8 ), e42614 ( 2012 ).
  • Hass R , KasperC , BohmS , JacobsR . Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC . Cell Commun. Signal.9 , 12 ( 2011 ).
  • Conget PA , AllersC , MinguellJJ . Identification of a discrete population of human bone marrow-derived mesenchymal cells exhibiting properties of uncommitted progenitors . J. Hematother. Stem Cell Res.10 ( 6 ), 749 – 758 ( 2001 ).
  • Delorme B , RingeJ , PontikoglouCet al. Specific lineage-priming of bone marrow mesenchymal stem cells provides the molecular framework for their plasticity . Stem Cells27 ( 5 ), 1142 – 1151 ( 2009 ).
  • Pontikoglou C , DelormeB , CharbordP . Human bone marrow native mesenchymal stem cells . Regen. Med.3 ( 5 ), 731 – 741 ( 2008 ).
  • Minguell JJ , AllersC , LasalaGP . Mesenchymal stem cells and the treatment of conditions and diseases: the less glittering side of a conspicuous stem cell for basic research . Stem Cells Dev.22 ( 2 ), 193 – 203 ( 2013 ).
  • Murphy MB , MoncivaisK , CaplanAI . Mesenchymal stem cells: environmentally responsive therapeutics for regenerative medicine . Exp. Mol. Med.45 , e54 ( 2013 ).
  • Dominici M , Le BlancK , MuellerIet al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement . Cytotherapy8 ( 4 ), 315 – 317 ( 2006 ).
  • Minguell JJ , FierroFA , EpunanMJ , EricesAA , SierraltaWD . Nonstimulated human uncommitted mesenchymal stem cells express cell markers of mesenchymal and neural lineages . Stem Cells Dev.14 ( 4 ), 408 – 414 ( 2005 ).
  • Rivera FJ , SierraltaWD , MinguellJJ , AignerL . Adult hippocampus derived soluble factors induce a neuronal-like phenotype in mesenchymal stem cells . Neurosci. Lett.406 ( 1–2 ), 49 – 54 ( 2006 ).
  • Nagai A , KimWK , LeeHJet al. Multilineage potential of stable human mesenchymal stem cell line derived from fetal marrow . PLoS ONE2 ( 12 ), e1272 ( 2007 ).
  • Fu L , ZhuL , HuangY , LeeTD , FormanSJ , ShihCC . Derivation of neural stem cells from mesenchymal stem cells: evidence for a bipotential stem cell population . Stem Cells Dev.17 ( 6 ), 1109 – 1121 ( 2008 ).
  • Park HE , KimD , KohHS , ChoS , SungJS , KimJY . Real-time monitoring of neural differentiation of human mesenchymal stem cells by electric cell-substrate impedance sensing . J. Biomed. Biotechnol. 2011 , 485173 ( 2011 ).
  • Neirinckx V , CosteC , RogisterB , Wislet-GendebienS . Neural fate of mesenchymal stem cells and neural crest stem cells: which ways to get neurons for cell therapy purpose? In:Trends in Cell Signaling Pathways in Neuronal Fate Decision.Wislet-GendebienS (Ed.) ., InTech, Europe, Croatia , 327 – 358 ( 2013 ).
  • Faca VM . Human mesenchymal stromal cell proteomics: contribution for identification of new markers and targets for medicine intervention . Expert Rev. Proteomics9 ( 2 ), 217 – 230 ( 2012 ).
  • Mindaye ST , RaM , Lo SurdoJ , BauerSR , AltermanMA . Improved proteomic profiling of the cell surface of culture-expanded human bone marrow multipotent stromal cells . J. Proteomics78 , 1 – 14 ( 2013 ).
  • Wislet-Gendebien S , HansG , LeprinceP , RigoJM , MoonenG , RogisterB . Plasticity of cultured mesenchymal stem cells: switch from nestin-positive to excitable neuron-like phenotype . Stem Cells23 ( 3 ), 392 – 402 ( 2005 ).
  • Montzka K , LassonczykN , TschokeBet al. Neural differentiation potential of human bone marrow-derived mesenchymal stromal cells: misleading marker gene expression . BMC Neurosci.10 , 16 ( 2009 ).
  • Hermann A , ListC , HabischHJet al. Age-dependent neuroectodermal differentiation capacity of human mesenchymal stromal cells: limitations for autologous cell replacement strategies . Cytotherapy12 ( 1 ), 17 – 30 ( 2010 ).
  • Niehage C , SteenblockC , PurscheT , BornhauserM , CorbeilD , HoflackB . The cell surface proteome of human mesenchymal stromal cells . PLoS ONE6 ( 5 ), e20399 ( 2011 ).
  • Peng J , WangY , ZhangLet al. Human umbilical cord Wharton’s jelly-derived mesenchymal stem cells differentiate into a Schwann-cell phenotype and promote neurite outgrowth in vitro . Brain Res. Bull.84 ( 3 ), 235 – 243 ( 2011 ).
  • Gu W , ZhangF , XueQ , MaZ , LuP , YuB . Bone mesenchymal stromal cells stimulate neurite outgrowth of spinal neurons by secreting nuero-trophic factors . Neurol. Res.34 ( 2 ), 172 – 180 ( 2012 ).
  • Osathanon T , ManokawinchokeJ , NowwaroteN , AguilarP , PalagaT , PavasantP . Notch signaling is involved in neurogenic commitment of human periodontal ligament-derived mesenchymal stem cells . Stem Cells Dev.22 ( 8 ), 1220 – 1231 ( 2013 ).
  • Kang SK , LeeDH , BaeYC , KimHK , BaikSY , JungJS . Improvement of neurological deficits by intracerebral transplantation of human adipose tissue-derived stromal cells after cerebral ischemia in rats . Exp. Neuol.183 ( 2 ), 355 – 366 ( 2003 ).
  • Ding DC , ShyuWC , ChiangMFet al. Enhancement of neuroplasticity through upregulation of beta1-integrin in human umbilical cord-derived stromal cell implanted stroke model . Neurobiol. Dis.27 ( 3 ), 339 – 353 ( 2007 ).
  • Koh SH , KimKS , ChoiMRet al. Implantation of human umbilical cord-derived mesenchymal stem cells as a neuroprotective therapy for ischemic stroke in rats . Brain Res.1229 , 233 – 248 ( 2008 ).
  • Knippenberg S , ThauN , DenglerR , BrinkerT , PetriS . Intracerebroventricular injection of encapsulated human mesenchymal cells producing glucagon-like peptide 1 prolongs survival in a mouse model of ALS . PLoS ONE7 ( 6 ), e36857 ( 2012 ).
  • Uccelli A , MilaneseM , PrincipatoMCet al. Intravenous mesenchymal stem cells improve survival and motor function in experimental amyotrophic lateral sclerosis . Mol. Med.18 , 794 – 804 ( 2012 ).
  • Chen J , LiY , WangL , LuM , ZhangX , ChoppM . Therapeutic benefit of intracerebral transplantation of bone marrow stromal cells after cerebral ischemia in rats . J. Neurol. Sci.189 ( 1–2 ), 49 – 57 ( 2001 ).
  • Shibata N . Transgenic mouse model for familial amyotrophic lateral sclerosis with superoxide dismutase-1 mutation . Neuropathology21 ( 1 ), 82 – 92 ( 2001 ).
  • Zhao CP , ZhangC , ZhouSNet al. Human mesenchymal stromal cells ameliorate the phenotype of SOD1-G93A ALS mice . Cytotherapy9 ( 5 ), 414 – 426 ( 2007 ).
  • Satake K , LouJ , LenkeLG . Migration of mesenchymal stem cells through cerebrospinal fluid into injured spinal cord tissue . Spine29 ( 18 ), 1971 – 1979 ( 2004 ).
  • Bakshi A , BarshingerAL , SwangerSAet al. Lumbar puncture delivery of bone marrow stromal cells in spinal cord contusion: a novel method for minimally invasive cell transplantation . J. Neurotrauma23 ( 1 ), 55 – 65 ( 2006 ).
  • Himes BT , NeuhuberB , ColemanCet al. Recovery of function following grafting of human bone marrow-derived stromal cells into the injured spinal cord . Neurorehabil. Neural Repair20 ( 2 ), 278 – 296 ( 2006 ).
  • Nishida K , TanakaN , NakanishiKet al. Magnetic targeting of bone marrow stromal cells into spinal cord: through cerebrospinal fluid . Neuroreport17 ( 12 ), 1269 – 1272 ( 2006 ).
  • Vaquero J , ZuritaM , OyaS , SantosM . Cell therapy using bone marrow stromal cells in chronic paraplegic rats: systemic or local administration?Neurosci. Lett.398 ( 1–2 ), 129 – 134 ( 2006 ).
  • Shi E , KazuiT , JiangXet al. Intrathecal injection of bone marrow stromal cells attenuates neurologic injury after spinal cord ischemia . Ann. Thorac Surg.81 ( 6 ), 2227 – 2233 ; discussion 2233–2224 ( 2006 ).
  • Lee PH , LeeJE , KimHSet al. A randomized trial of mesenchymal stem cells in multiple system atrophy . Ann. Neurol.72 ( 1 ), 32 – 40 ( 2012 ).
  • Forostyak S , JendelovaP , KapcalovaM , ArboledaD , SykovaE . Mesenchymal stromal cells prolong the lifespan in a rat model of amyotrophic lateral sclerosis . Cytotherapy13 ( 9 ), 1036 – 1046 ( 2011 ).
  • Knippenberg S , ThauN , DenglerR , BrinkerT , PetriS . Intracerebroventricular injection of encapsulated human mesenchymal cells producing glucagon-like peptide 1 prolongs survival in a mouse model of ALS . PLoS ONE7 ( 6 ), e36857 ( 2012 ).
  • Pastor D , Viso-LeonMC , JonesJet al. Comparative effects between bone marrow and mesenchymal stem cell transplantation in GDNF expression and motor function recovery in a motorneuron degenerative mouse model . Stem Cell Rev.8 ( 2 ), 445 – 458 ( 2012 ).
  • Marconi S , BonaconsaM , ScambiIet al. Systemic treatment with adipose-derived mesenchymal stem cells ameliorates clinical and pathological features in the amyotrophic lateral sclerosis murine model . Neuroscience248C , 333 – 343 ( 2013 ).
  • Sun H , BenardaisK , StanslowskyNet al. Therapeutic potential of mesenchymal stromal cells and MSC conditioned medium in amyotrophic lateral sclerosis (ALS) – in vitro evidence from primary motor neuron cultures, NSC-34 cells, astrocytes and microglia . PLoS ONE8 ( 9 ), e72926 ( 2013 ).
  • Jaramillo-Merchan J , JonesJ , IvorraJLet al. Mesenchymal stromal-cell transplants induce oligodendrocyte progenitor migration and remyelination in a chronic demyelination model . Cell Death Dis.4 , e779 ( 2013 ).
  • Joyce N , AnnettG , WirthlinL , OlsonS , BauerG , NoltaJA . Mesenchymal stem cells for the treatment of neurodegenerative disease . Regen. Med.5 ( 6 ), 933 – 946 ( 2010 ).
  • Mazzini L , FagioliF , BoccalettiRet al. Stem cell therapy in amyotrophic lateral sclerosis: a methodological approach in humans . Amyotroph. Lateral Scler. Other Motor Neuron Disord.4 ( 3 ), 158 – 161 ( 2003 ).
  • Karussis D , KarageorgiouC , Vaknin-DembinskyAet 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 ).
  • Mazzini L , FerreroI , LuparelloVet al. Mesenchymal stem cell transplantation in amyotrophic lateral sclerosis: a Phase I clinical trial . Exp. Neuol.223 ( 1 ), 229 – 237 ( 2010 ).
  • Mazzini L , MareschiK , FerreroIet al. Mesenchymal stromal cell transplantation in amyotrophic lateral sclerosis: a long-term safety study . Cytotherapy14 ( 1 ), 56 – 60 ( 2012 ).
  • Prabhakar S , MarwahaN , LalV , SharmaRR , RajanR , KhandelwalN . Autologous bone marrow-derived stem cells in amyotrophic lateral sclerosis: a pilot study . Neurology India60 ( 5 ), 465 – 469 ( 2012 ).
  • Minguell JJ , AllersC , Jones , GanjiSS . Allogeneic mesenchymal stem cells infusion to an ALS patient proved to be safe and capable to initiate clinical recuperation . CellR41 ( 3 ), e530 ( 2013 ).
  • ClincalTrials.gov . www.ClinicalTrials.gov .
  • Parr AM , TatorCH , KeatingA . Bone marrow-derived mesenchymal stromal cells for the repair of central nervous system injury . Bone Marrow Transplant.40 ( 7 ), 609 – 619 ( 2007 ).
  • Phinney DG , ProckopDJ . Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair – current views . Stem Cells25 ( 11 ), 2896 – 2902 ( 2007 ).
  • Soler B , FadicR , Von BernhardiR . [Stem cells therapy in amyotrophic lateral sclerosis treatment. A critical view] . Rev. Neurol.52 ( 7 ), 426 – 434 ( 2011 ).
  • Ferrero I , MazziniL , RustichelliDet al. Bone marrow mesenchymal stem cells from healthy donors and sporadic amyotrophic lateral sclerosis patients . Cell Transplant.17 ( 3 ), 255 – 266 ( 2008 ).
  • Tichon A , GowdaBK , SlavinS , GazitA , PrielE . Telomerase activity and expression in adult human mesenchymal stem cells derived from amyotrophic lateral sclerosis individuals . Cytotherapy11 ( 7 ), 837 – 848 ( 2009 ).
  • Bossolasco P , CovaL , CalzarossaCet al. Metalloproteinase alterations in the bone marrow of ALS patients . J. Mol. Med. (Berl.)88 ( 6 ), 553 – 564 ( 2010 ).
  • Cho GW , NohMY , KimHY , KohSH , KimKS , KimSH . Bone marrow-derived stromal cells from amyotrophic lateral sclerosis patients have diminished stem cell capacity . Stem Cells Dev.19 ( 7 ), 1035 – 1042 ( 2010 ).
  • Nachmany H , WaldS , AbekasisM , BulvikS , WeilM . Two potential biomarkers identified in mesenchymal stem cells and leukocytes of patients with sporadic amyotrophic lateral sclerosis . Dis. Markers32 ( 4 ), 211 – 220 ( 2012 ).
  • Koh SH , BaikW , NohMYet al. The functional deficiency of bone marrow mesenchymal stromal cells in ALS patients is proportional to disease progression rate . Exp. Neuol.233 ( 1 ), 472 – 480 ( 2012 ).
  • Cramer C , FreisingerE , JonesRKet al. Persistent high glucose concentrations alter the regenerative potential of mesenchymal stem cells . Stem Cells Dev.19 ( 12 ), 1875 – 1884 ( 2010 ).
  • Allers C , LasalaGP , MinguellJJ . Presence of osteoclast precursor cells during ex vivo expansion of bone marrow-derived mesenchymal stem cells for autologous use in cell therapy . Cytotherapy16 ( 4 ), 454 – 459 ( 2013 ).
  • Liu L , EckertMA , RiazifarH , KangDK , AgalliuD , ZhaoW . From blood to the brain: can systemically transplanted mesenchymal stem cells cross the blood–brain barrier?Stem Cells Int.435093 ( 2013 ) ( 2013 ).
  • Izadpanah R , KaushalD , KriedtCet al. Long-term in vitro expansion alters the biology of adult mesenchymal stem cells . Cancer Res.68 ( 11 ), 4229 – 4238 ( 2008 ).
  • Sethe S , ScuttA , StolzingA . Aging of mesenchymal stem cells . Ageing Res. Rev.5 ( 1 ), 91 – 116 ( 2006 ).
  • Wagner W , HornP , CastoldiMet al. Replicative senescence of mesenchymal stem cells: a continuous and organized process . PLoS ONE3 ( 5 ), e2213 ( 2008 ).
  • Madeira A , Da SilvaCL , Dos SantosF , CamafeitaE , CabralJM , Sa-CorreiaI . Human mesenchymal stem cell expression program upon extended ex-vivo cultivation, as revealed by 2-DE-based quantitative proteomics . PLoS ONE7 ( 8 ), e43523 ( 2012 ).
  • Garbuzova-Davis S , RodriguesMC , MirtylSet al. Multiple intravenous administrations of human umbilical cord blood cells benefit in a mouse model of ALS . PLoS ONE7 ( 2 ), e31254 ( 2012 ).
  • Lin P , CorreaD , KeanTJ , AwadallahA , DennisJE , CaplanAI . Serial transplantation and long-term engraftment of intra-arterially delivered clonally derived mesenchymal stem cells to injured bone marrow . Mol. Ther.22 ( 1 ), 160 – 168 ( 2013 ).
  • Riley J , GlassJ , FeldmanELet al. Intraspinal stem cell transplantation in ALS: a Phase I trial, cervical microinjection and final surgical safety outcomes . Neurosurgery74 ( 1 ), 77 – 87 ( 2014 ).
  • Moviglia GA , Moviglia-BrandolinoMT , VarelaGSet al. Feasibility, safety, and preliminary proof of principles of autologous neural stem cell treatment combined with T-cell vaccination for ALS patients . Cell Transplant.21 ( Suppl. 1 ), S57 – S63 ( 2012 ).
  • Glass JD , BoulisNM , JoheKet al. Lumbar intraspinal injection of neural stem cells in patients with amyotrophic lateral sclerosis: results of a Phase I trial in 12 patients . Stem Cells30 ( 6 ), 1144 – 1151 ( 2012 ).
  • Martinez HR , Gonzalez-GarzaMT , Moreno-CuevasJE , CaroE , Gutierrez-JimenezE , SeguraJJ . Stem-cell transplantation into the frontal motor cortex in amyotrophic lateral sclerosis patients . Cytotherapy11 ( 1 ), 26 – 34 ( 2009 ).
  • Deda H , InciMC , KurekciAEet al. Treatment of amyotrophic lateral sclerosis patients by autologous bone marrow-derived hematopoietic stem cell transplantation: a 1-year follow-up . Cytotherapy11 ( 1 ), 18 – 25 ( 2009 ).
  • Blanquer M , MoraledaJM , IniestaFet al. Nuero-trophic bone marrow cellular nests prevent spinal motoneuron degeneration in amyotrophic lateral sclerosis patients: a pilot safety study . Stem Cells30 ( 6 ), 1277 – 1285 ( 2012 ).

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