Human neural stem cell replacement therapy for amyotrophic lateral sclerosis by spinal transplantation

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Hefferan, Michael P ^a   Galik, Jan ^b,c   Kakinohana, Osamu ^a   Sekerkova, Gabriela ^d   Santucci, Camila ^a   Marsala, Silvia ^a   Navarro, Roman ^a   Hruska Plochan, Marian ^a,h,i   Johe, Karl ^e   Feldman, Eva ^f   Cleveland, Don W ^g   Marsala, Martin ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

^c P J AFÁRIK UNIVERSITY   (Slovakia)

^d NORTHWESTERN UNIVERSITY   (United States)

^e Neuralstem Inc   (United States)

^f UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h INSTITUTE OF ANIMAL PHYSIOLOGY AND GENETICS   (Czech Republic)

ⁱ CHARLES UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE;

ALPHA NERVE FIBER; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; ELECTROSTIMULATION; EVOKED MUSCLE RESPONSE; FEMALE; FETUS; HUMAN; HUMAN CELL; LIFESPAN; LUMBAR SPINAL CORD; MALE; MOTOR CORTEX; MOTOR SYSTEM; NERVE FIBER; NEURAL STEM CELL TRANSPLANTATION; NEUROPROTECTION; NONHUMAN; PYRAMIDAL TRACT; RAT; RUBROSPINAL TRACT; SPINAL CORD VENTRAL HORN; SPINAL TRANSPLANTATION; THORACIC SPINAL CORD; TREATMENT RESPONSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ELECTRIC STIMULATION; EVOKED POTENTIALS, MOTOR; HUMANS; MUTATION; NEURAL STEM CELLS; RATS; RATS, TRANSGENIC; SPINAL CORD; STEM CELL TRANSPLANTATION; SUPEROXIDE DISMUTASE; SYNAPSES;

EID: 84865171632     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042614     Document Type: Article

References (56)

1. Mulder DW, Kurland LT, Offord KP, Beard CM, ((1986)) Familial adult motor neuron disease: amyotrophic lateral sclerosis. Neurology 36:: 511--517.
2. Cudkowicz ME, McKenna-Yasek D, Sapp PE, Chin W, Geller B, et al. ((1997)) Epidemiology of mutations in superoxide dismutase in amyotrophic lateral sclerosis. Ann Neurol 41:: 210--221.
3. Rothstein JD, Martin LJ, Kuncl RW, ((1992)) Decreased glutamate transport by the brain and spinal cord in amyotrophic lateral sclerosis. N Engl J Med 326:: 1464--1468.
4. Bruijn LI, Becher MW, Lee MK, Anderson KL, Jenkins NA, et al. ((1997)) ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 18:: 327--338.
5. Howland DS, Liu J, She Y, Goad B, Maragakis NJ, et al. ((2002)) Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc Natl Acad Sci U S A 99:: 1604--1609.
6. Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillee S, et al. ((2003)) Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 302:: 113--117.
7. Yamanaka K, Boillee S, Roberts EA, Garcia ML, McAlonis-Downes M, et al. ((2008)) Mutant SOD1 in cell types other than motor neurons and oligodendrocytes accelerates onset of disease in ALS mice. Proc Natl Acad Sci U S A 105:: 7594--7599.
8. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, et al. ((2007)) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10:: 615--622.
9. Marchetto MC, Muotri AR, Mu Y, Smith AM, Cezar GG, et al. ((2008)) Non-cell-autonomous effect of human SOD1 G37R astrocytes on motor neurons derived from human embryonic stem cells. Cell Stem Cell 3:: 649--657.
10. Di Giorgio FP, Carrasco MA, Siao MC, Maniatis T, Eggan K, ((2007)) Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat Neurosci 10:: 608--614.
11. Di Giorgio FP, Boulting GL, Bobrowicz S, Eggan KC, ((2008)) Human embryonic stem cell-derived motor neurons are sensitive to the toxic effect of glial cells carrying an ALS-causing mutation. Cell Stem Cell 3:: 637--648.
12. Lepore AC, Rauck B, Dejea C, Pardo AC, Rao MS, et al. ((2008)) Focal transplantation-based astrocyte replacement is neuroprotective in a model of motor neuron disease. Nat Neurosci 11:: 1294--1301.
13. Boillee S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, et al. ((2006)) Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312:: 1389--1392.
14. Ralph GS, Radcliffe PA, Day DM, Carthy JM, Leroux MA, et al. ((2005)) Silencing mutant SOD1 using RNAi protects against neurodegeneration and extends survival in an ALS model. Nat Med 11:: 429--433.
15. Miller TM, Kaspar BK, Kops GJ, Yamanaka K, Christian LJ, et al. ((2005)) Virus-delivered small RNA silencing sustains strength in amyotrophic lateral sclerosis. Ann Neurol 57:: 773--776.
16. Xu L, Yan J, Chen D, Welsh AM, Hazel T, et al. ((2006)) Human neural stem cell grafts ameliorate motor neuron disease in SOD-1 transgenic rats. Transplantation 82:: 865--875.
17. Xu L, Ryugo DK, Pongstaporn T, Johe K, Koliatsos VE, ((2009)) Human neural stem cell grafts in the spinal cord of SOD1 transgenic rats: differentiation and structural integration into the segmental motor circuitry. J Comp Neurol 514:: 297--309.
18. Lee MK, Tuttle JB, Rebhun LI, Cleveland DW, Frankfurter A, ((1990)) The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil Cytoskeleton 17:: 118--132.
19. Fehlings MG, Tator CH, Linden RD, Piper IR, ((1987)) Motor evoked potentials recorded from normal and spinal cord-injured rats. Neurosurgery 20:: 125--130.
20. Fehlings MG, Tator CH, Linden RD, Piper IR, ((1988)) Motor and somatosensory evoked potentials recorded from the rat. Electroencephalogr Clin Neurophysiol 69:: 65--78.
21. Zappulla RA, Hollis P, Ryder J, Moore FM, Adamson J, et al. ((1988)) Noncortical origins of the spinal motor evoked potential in rats. Neurosurgery 22:: 846--852.
22. Braak H, Braak E, Ohm T, Bohl J, ((1988)) Silver impregnation of Alzheimer's neurofibrillary changes counterstained for basophilic material and lipofuscin pigment. Stain Technol 63:: 197--200.
23. de Olmos JS, Beltramino CA, de Olmos de Lorenzo S, ((1994)) Use of an amino-cupric-silver technique for the detection of early and semiacute neuronal degeneration caused by neurotoxicants, hypoxia, and physical trauma. Neurotoxicol Teratol 16:: 545--561.
24. Hall ED, Sullivan PG, Gibson TR, Pavel KM, Thompson BM, et al. ((2005)) Spatial and temporal characteristics of neurodegeneration after controlled cortical impact in mice: more than a focal brain injury. J Neurotrauma 22:: 252--265.
25. Switzer RC 3rd, ((2000)) Application of silver degeneration stains for neurotoxicity testing. Toxicol Pathol 28:: 70--83.
26. Suzuki M, McHugh J, Tork C, Shelley B, Klein SM, et al. ((2007)) GDNF secreting human neural progenitor cells protect dying motor neurons, but not their projection to muscle, in a rat model of familial ALS. PLoS One 2:: e689.
27. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, et al. ((1994)) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264:: 1772--1775.
28. Ozdinler PH, Benn S, Yamamoto TH, Guzel M, Brown RH Jr, et al. ((2011)) Corticospinal motor neurons and related subcerebral projection neurons undergo early and specific neurodegeneration in hSOD1G(9)(3)A transgenic ALS mice. J Neurosci 31:: 4166--4177.
29. Cosottini M, Giannelli M, Siciliano G, Lazzarotti G, Michelassi MC, et al. ((2005)) Diffusion-tensor MR imaging of corticospinal tract in amyotrophic lateral sclerosis and progressive muscular atrophy. Radiology 237:: 258--264.
30. da Rocha AJ, Oliveira AS, Fonseca RB, Maia AC Jr, Buainain RP, et al. ((2004)) Detection of corticospinal tract compromise in amyotrophic lateral sclerosis with brain MR imaging: relevance of the T1-weighted spin-echo magnetization transfer contrast sequence. AJNR Am J Neuroradiol 25:: 1509--1515.
31. Davidson CD, ((1941)) Amyotrophic lateral sclerosis: origin and extent ofthe upper motor neuron lesion. Arch Neurol 46:: 1039--1056.
32. Brownell B, Oppenheimer DR, Hughes JT, ((1970)) The central nervous system in motor neurone disease. J Neurol Neurosurg Psychiatry 33:: 338--357.
33. Castro AJ, ((1972)) Motor performance in rats. The effects of pyramidal tract section. Brain Res 44:: 313--323.
34. Xu L, Shen P, Hazel T, Johe K, Koliatsos VE, ((2011)) Dual transplantation of human neural stem cells into cervical and lumbar cord ameliorates motor neuron disease in SOD1 transgenic rats. Neurosci Lett 494:: 222--226.
35. Scott S, Kranz JE, Cole J, Lincecum JM, Thompson K, et al. ((2008)) Design, power, and interpretation of studies in the standard murine model of ALS. Amyotroph Lateral Scler 9:: 4--15.
36. Dal Canto MC, Gurney ME, ((1997)) A low expressor line of transgenic mice carrying a mutant human Cu,Zn superoxide dismutase (SOD1) gene develops pathological changes that most closely resemble those in human amyotrophic lateral sclerosis. Acta Neuropathol 93:: 537--550.
37. Dal Canto MC, Gurney ME, ((1995)) Neuropathological changes in two lines of mice carrying a transgene for mutant human Cu,Zn SOD, and in mice overexpressing wild type human SOD: a model of familial amyotrophic lateral sclerosis (FALS). Brain Res 676:: 25--40.
38. Smith RA, Miller TM, Yamanaka K, Monia BP, Condon TP, et al. ((2006)) Antisense oligonucleotide therapy for neurodegenerative disease. J Clin Invest 116:: 2290--2296.
39. Yamanaka K, Chun SJ, Boillee S, Fujimori-Tonou N, Yamashita H, et al. ((2008)) Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat Neurosci 11:: 251--253.
40. Horner PJ, Power AE, Kempermann G, Kuhn HG, Palmer TD, et al. ((2000)) Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 20:: 2218--2228.
41. Zai LJ, Wrathall JR, ((2005)) Cell proliferation and replacement following contusive spinal cord injury. Glia 50:: 247--257.
42. Takasawa K, Kitagawa K, Yagita Y, Sasaki T, Tanaka S, et al. ((2002)) Increased proliferation of neural progenitor cells but reduced survival of newborn cells in the contralateral hippocampus after focal cerebral ischemia in rats. J Cereb Blood Flow Metab 22:: 299--307.
43. Kang SH, Fukaya M, Yang JK, Rothstein JD, Bergles DE, ((2010)) NG2+ CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 68:: 668--681.
44. Magnus T, Carmen J, Deleon J, Xue H, Pardo AC, et al. ((2008)) Adult glial precursor proliferation in mutant SOD1G93A mice. Glia 56:: 200--208.
45. Mothe AJ, Tator CH, ((2005)) Proliferation, migration, and differentiation of endogenous ependymal region stem/progenitor cells following minimal spinal cord injury in the adult rat. Neuroscience 131:: 177--187.
46. Johe KK, Hazel TG, Muller T, Dugich-Djordjevic MM, McKay RD, ((1996)) Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev 10:: 3129--3140.
47. Kakinohana O, Cizkova D, Tomori Z, Hedlund E, Marsala S, et al. ((2004)) Region-specific cell grafting into cervical and lumbar spinal cord in rat: a qualitative and quantitative stereological study. Exp Neurol 190:: 122--132.
48. Basso DM, Beattie MS, Bresnahan JC, Anderson DK, Faden AI, et al. ((1996)) MASCIS evaluation of open field locomotor scores: effects of experience and teamwork on reliability. Multicenter Animal Spinal Cord Injury Study. J Neurotrauma 13:: 343--359.
49. Schwarz M, Block F, Pergande G, ((1994)) N-methyl-D-aspartate (NMDA)-mediated muscle relaxant action of flupirtine in rats. Neuroreport 5:: 1981--1984.
50. Kakinohana O, Hefferan MP, Nakamura S, Kakinohana M, Galik J, et al. ((2006)) Development of GABA-sensitive spasticity and rigidity in rats after transient spinal cord ischemia: a qualitative and quantitative electrophysiological and histopathological study. Neuroscience 141:: 1569--1583.
51. Mackie M, Hughes DI, Maxwell DJ, Tillakaratne NJ, Todd AJ, ((2003)) Distribution and colocalisation of glutamate decarboxylase isoforms in the rat spinal cord. Neuroscience 119:: 461--472.
52. Todd AJ, Hughes DI, Polgar E, Nagy GG, Mackie M, et al. ((2003)) The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci 17:: 13--27.
53. Hughes DI, Mackie M, Nagy GG, Riddell JS, Maxwell DJ, et al. ((2005)) P boutons in lamina IX of the rodent spinal cord express high levels of glutamic acid decarboxylase-65 and originate from cells in deep medial dorsal horn. PNAS 102:: 9038--9043.
54. Kakinohana O, Hefferan MP, Miyanohara A, Nejime T, Marsala S, et al. ((2012)) Combinational Spinal GAD65 Gene Delivery and Systemic GABA-Mimetic Treatment for Modulation of Spasticity. PLoS One 7:: e30561.
55. Suzuki M, McHugh J, Tork C, Shelley B, Klein SM, et al. ((2007)) GDNF secreting human neural progenitor cells protect dying motor neurons, but not their projection to muscle, in a rat model of familial ALS. PLoS One 2:: e689.
56. Suzuki M, McHugh J, Tork C, Shelley B, Hayes A, et al. ((2008)) Direct muscle delivery of GDNF with human mesenchymal stem cells improves motor neuron survival and function in a rat model of familial ALS. Mol Ther 16:: 2002--2010.