Growth factor-expressing human neural progenitor cell grafts protect motor neurons but do not ameliorate motor performance and survival in ALS mice

Experimental and Molecular Medicine

Volumn 41, Issue 7, 2009, Pages 487-500

  Park, Sungju ^a   Kim, Hyoung Tae ^a   Yun, Seokhwan ^a   Kim, Il Sun ^a   Lee, Jiyoon ^a   Lee, Il Shin ^a   Kook, In Park ^a  

^a Yonsei University College of Medicine   (South Korea)

Author keywords

Amyotrophic lateral sclerosis; Cell differentiation; Glial cell line derived neurotrophic factor; Nerve growth factors; Stem cell transplantation; Stem cells

Indexed keywords

ADENOVIRUS VECTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; COPPER ZINC SUPEROXIDE DISMUTASE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GROWTH FACTOR; LENTIVIRUS VECTOR; NEUROTROPHIN 3; SOMATOMEDIN C; VASCULOTROPIN; VESICULAR GLUTAMATE TRANSPORTER 1;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; GENETIC ENGINEERING; HUMAN; HUMAN TISSUE; LIFESPAN; MALE; MOTONEURON; MOTOR PERFORMANCE; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE GRAFT; NONHUMAN; OLIGODENDROGLIA; SEX DIFFERENCE; STEM CELL TRANSPLANTATION; SURVIVAL; TRANSGENIC MOUSE;

ANIMALIA; MUS; MUS MUSCULUS;

EID: 68049110630     PISSN: 12263613     EISSN: 20926413     Source Type: Journal    
DOI: 10.3858/emm.2009.41.7.054     Document Type: Article

References (61)

1. Aebischer P, Schluep M, Déglon N, Joseph JM, Hirt L, Heyd B, Goddard M, Hammang JP, Zurn AD, Kato AC, Regli F, Baetge EE. Intrathecal delivery of CNTF using encapsulated genetically modified xenogeneic cells in amyotrophic lateral sclerosis patients. Nat Med 1996;2:696-699 (Pubitemid 26191960)
2. Azzouz M, Ralph GS, Storkebaum E, Walmsley LE, Mitrophanous KA, Kingsman SM, Carmeliet P, Mazarakis ND. VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature 2004;429:413-417 (Pubitemid 38715132)
3. Beers DR, Henkel JS, Xiao Q, Zhao W, Wang J, Yen AA, Siklos L, McKercher SR, Appel SH. Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 2006;103:16021-16026 (Pubitemid 44657585)
4. Boillee S, Vande Velde C, Cleveland DW. ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 2006;52:39-59 (Pubitemid 44466358)
5. Boillée S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G, Kollias G, Cleveland DW. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 2006;312:1389-1392 (Pubitemid 43839552)
6. Bruijn LI, Miller TM, Cleveland DW. Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu Rev Neurosci 2004;27:723-749
7. Choi CI, Lee YD, Gwag BJ, Cho SI, Kim SS, Suh-Kim H. Effects of estrogen on lifespan and motor functions in female hSOD1 G93A transgenic mice. J Neurol Sci 2008;268:40-47
8. Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillée S, Rule M, McMahon AP, Doucette W, Siwek D, Ferrante RJ, Brown RH Jr, Julien JP, Goldstein LS, Cleveland DW. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 2003;302:113-117 (Pubitemid 37210700)
9. Corti S, Locatelli F, Donadoni C, Guglieri M, Papadimitriou D, Strazzer S, Del Bo R, Comi GP. Wild-type bone marrow cells ameliorate the phenotype of SOD1-G93A ALS mice and contribute to CNS, heart and skeletal muscle tissues. Brain 2004;127:2518-2532 (Pubitemid 39472980)
10. Corti S, Locatelli F, Papadimitriou D, Del Bo R, Nizzardo M, Nardini M, Donadoni C, Salani S, Fortunato F, Strazzer S, Bresolin N, Comi GP. Neural stem cells LewisX+ CXCR4+ modify disease progression in an amyotrophic lateral sclerosis model. Brain 2007;130:1289-1305 (Pubitemid 47355948)
11. Deshpande DM, Kim YS, Martinez T, Carmen J, Dike S, Shats I, Rubin LL, Drummond J, Krishnan C, Hoke A, Maragakis N, Shefner J, Rothstein JD, Kerr DA. Recovery from paralysis in adult rats using embryonic stem cells. Ann Neurol 2006;60:32-44
12. Di Giorgio FP, Carrasco MA, Siao MC, Maniatis T, Eggan K. Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat Neurosci 2007;10:608-614 (Pubitemid 46652442)
13. Di Giorgio FP, Boulting GL, Bobrowicz S, Eggan KC. Human embryonic stem cell-derived motor neurons are sensitive to the toxic effects of glial cells carrying an ALS-causing mutation. Cell Stem Cell 2008;3:637-648
14. Federici T, Boulis NM. Gene-based treatment of motor neuron diseases. Muscle Nerve 2006;33:302-323 (Pubitemid 43305907)
15. Fischer LR, Culver DG, Tennant P, Davis AA, Wang M, Castellano-Sanchez A, Khan J, Polak MA, Glass JD. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol 2004;185:232-240 (Pubitemid 38084849)
16. Flax JD, Aurora S, Yang C, Simonin C, Wills AM, Billinghurst LL, Jendoubi M, Sidman RL, Wolfe JH, Kim SU, Snyder EY. Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat Biotechnol 1998;16:1033-1039 (Pubitemid 28515895)
17. Garbuzova-Davis S, Willing AE, Milliken M, Saporta S, Zigova T, Cahill DW, Sanberg PR. Positive effect of transplantation of hNT neurons (NTera 2/D1cell line) in a model of familial amyotrophic lateral sclerosis. Exp Neurol 2002;174:169-180 (Pubitemid 34293447)
18. Garbuzova-Davis S, Willing AE, Zigova T, Saporta S, Justen EB, Lane JC, Hudson JE, Chen N, Davis CD, Sanberg PR. Intravenous administration of human umbilical cord blood cells in a mouse model of amyotrophic lateral sclerosis: distribution, migration, and differentiation. J Hematother Stem Cell Res 2003;12:255-270 (Pubitemid 36736737)
19. Garbuzova-Davis S, Saporta S, Haller E, Kolomey I, Bennett SP, Potter H, Sanberg PR. Evidence of compromised blood-spinal cord barrier in early and late symptomatic SOD1 mice modeling ALS. PLoS ONE 2007;2:e1205
20. Gurney ME. Transgenic-mouse model of amyotrophic lateral sclerosis. N Engl J Med 1994;331:1721-1722 (Pubitemid 24373633)
21. Habisch HJ, Janowski M, Binder D, Kuzma-Kozakiewicz M, Widmann A, Habich A, Schwalenstöcker B, Hermann A, Brenner R, Lukomska B, Domanska-Janik K, Ludolph AC, Storch A. Intrathecal application of neuroectodermally converted stem cells into a mouse model of ALS: limited intraparenchymal migration and survival narrows therapeutic effects. J Neural Transm 2007;114:1395-1406 (Pubitemid 350112275)
22. Harper JM, Krishnan C, Darman JS, Deshpande DM, Peck S, Shats I, Backovic S, Rothstein JD, Kerr DA. Axonal growth of embryonic stem cell-derived motoneurons in vitro and in motoneuron-injured adult rats. Proc Natl Acad Sci USA 2004;101:7123-7128 (Pubitemid 38596453)
23. Howland DS, Liu J, She Y, Goad B, Maragakis NJ, Kim B, Erickson J, Kulik J, DeVito L, Psaltis G, DeGennaro LJ, Cleveland DW, Rothstein JD. Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc Natl Acad Sci USA 2002;99:1604-1609 (Pubitemid 34136539)
24. Imitola J, Raddassi K, Park KI, Mueller FJ, Nieto M, Teng YD, Frenkel D, Li J, Sidman RL, Walsh CA, Snyder EY, Khoury SJ. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci USA 2004;101:18117-18122 (Pubitemid 40054083)
25. Ivanova T, Karolczak M, Beyer C. Estradiol stimulates GDNF expression in developing hypothalamic neurons. Endocrinology 2002;143:3175-3178 (Pubitemid 34809891)
26. Kaspar BK, Llado J, Sherkat N, Rothstein JD, Gage FH. Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science 2008;301:839-842 (Pubitemid 36962626)
27. Kerr DA, Lladó J, Shamblott MJ, Maragakis NJ, Irani DN, Crawford TO, Krishnan C, Dike S, Gearhart JD, Rothstein JD. Human embryonic germ cell derivatives facilitate motor recovery of rats with diffuse motor neuron injury. J Neurosci 2003;23:5131-5140 (Pubitemid 36793241)
28. Kim HT, Kim IS, Lee IS, Lee JP, Snyder EY, Park KI. Human neurospheres derived from the fetal central nervous system are regionally and temporally specified but are not committed. Exp Neurol 2006;199:222-235
29. Klein SM, Behrstock S, McHugh J, Hoffmann K, Wallace K, Suzuki M, Aebischer P, Svendsen CN. GDNF delivery using human neural progenitor cells in a rat model of ALS. Hum Gene Ther 2005;16:509-521 (Pubitemid 40647148)
30. Kordower JH, Palfi S, Chen EY, Ma SY, Sendera T, Cochran EJ, Cochran EJ, Mufson EJ, Penn R, Goetz CG, Comella CD. Clinicopathological findings following intraventricular glial-derived neurotrophic factor treatment in a patient with Parkinson's disease. Ann Neurol 1999;46:419-424 (Pubitemid 29416283)
31. Lee JP, Jeyakumar M, Gonzalez R, Takahashi H, Lee PJ, Baek RC, Clark D, Rose H, Fu G, Clarke J, McKercher S, Meerloo J, Muller FJ, Park KI, Butters TD, Dwek RA, Schwartz P, Tong G, Wenger D, Lipton SA, Seyfried TN, Platt FM, Snyder EY. Stem cells act through multiple mechanisms to benefit mice with neurodegenerative metabolic disease. Nat Med 2007;13:439-447 (Pubitemid 46559825)
32. Lepore AC, Maragakis NJ. Targeted stem cell transplantaiton strategies in ALS. Neurochem Int 2007;50:966-975 (Pubitemid 46962803)
33. Lepore AC, Rauck B, Dejea C, Pardo AC, Rao MS, Rothstein JD, Maragakis NJ. Focal transplantation-based astrocyte replacement is neuroprotective in a model of motor neuron disease. Nat Neurosci 2008;11:1294-1301
34. Llado J, Haenggeli C, Maragakis NJ, Snyder EY, Rothstein JD. Neural stem cells protect against glutamate-induced excitotoxicity and promote survival of injured motor neurons through the secretion of neurotrophic factors. Mol Cell Neurosci 2004;27:322-331 (Pubitemid 39433844)
35. Marchetto MCN, Muotri AR, Mu Y, Smith AM, Cezar GG, Gage FH. Non-cell-autonomous effect of human SOD1G37R astrocytes on motor neurons derived from human embryonic stem cells. Cell Stem Cell 2008;3:649-657
36. Martin LJ, Liu Z. Adult olfactory bulb neural precursor cell grafts provide temporary protection from motor neuron degeneration, improve motor function and extend survival in amyotrophic lateral sclerosis mice. J Neuropathol Exp Neurol 2007;66:1002-1018 (Pubitemid 350060368)
37. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, Przedborski S. Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 2007;10:615-622 (Pubitemid 46652435)
38. Nagano I, Ilieva H, Shiote M, Murakami T, Yokoyama M, Shoji M, Abe K. Therapeutic benefit of intrathecal injection of insulin-like growth factor-1 in a mouse model of amyotrophic lateral sclerosis. J Neurol Sci 2005a;235:61-68 (Pubitemid 41039094)
39. Nagano I, Shiote M, Murakami T, Kamada H, Hamakawa Y, Matsubara E, Yokoyama M, Moritaz K, Shoji M, Abe K. Beneficial effects of intrathecal IGF-1 administration in patients with amyotrophic lateral sclerosis. Neurol Res 2005b;27:768-772 (Pubitemid 41513087)
40. Nutt JG, Burchiel KJ, Comella CL, Jankovic J, Lang AE, Laws ER Jr, Lozano AM, Penn RD, Simpson RK Jr, Stacy M, Wooten GF; ICV GDNF Study Group. Implanted intracerebroventricular. Glial cell line-derived neurotrophic factor. Randomized, double-blind trial of glial cell line-derived neurotrophic factor (GDNF) in PD. Neurology 2003;60:69-73
41. Park KI, Teng YD, Snyder EY. The injured brain interacts reciprocally with neural stem cells supported by scaffolds to reconstitute lost tissue. Nat Biotechnol 2002;20:1111-1117
42. Park KI, Hack MA, Ourednik J, Yandava B, Flax JD, Stieg PE, Gullans S, Jensen FE, Sidman RL, Ourednik V, Snyder EY. Acute injury directs the migration, proliferation, & differentiation of solid organ stem cells: Evidence from the effect of hypoxia-ischemia in the CNS on clonal "reporter" neural stem cells. Exp Neurol 2006a;199:156-178
43. Park KI, Himes BT, Stieg PE, Tessler A, Fischer I, Snyder EY. Neural stem cells may be uniquely suited for combined gene therapy & cell replacement: Evidence from engraftment of Neurotrophin-3-expressing stem cells in hypoxic-ischemic brain injury. Exp Neurol 2006b;199:179-190 (Pubitemid 43913761)
44. Pasinelli P, Brown RH. Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat Rev Neurosci 2006;7:710-723 (Pubitemid 44267495)
45. Pun S, Santos AF, Saxena S, Xu L, Caroni P. Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat Neurosci 2006;9:408-419 (Pubitemid 43290971)
46. Rothstein JD, Van Kammen M, Levey AI, Martin LJ, Kuncl RW. Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann Neurol 1995;38:73-84
47. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, Welty DF. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 1996;16:675-686 (Pubitemid 26103145)
48. Snyder EY, Taylor RM, Wolfe JH. Neural progenitor cell engraftment corrects lysosomal storage throughout the MPS VII mouse brain. Nature 1995;374:367-370
49. Storkebaum E, Lambrechts D, Dewerchin M, Moreno-Murciano MP, Appelmans S, Oh H, Van Damme P, Rutten B, Man WY, De Mol M, Wyns S, Manka D, Vermeulen K, Van Den Bosch L, Mertens N, Schmitz C, Robberecht W, Conway EM, Collen D, Moons L, Carmeliet P. Treatment of motoneuron degeneration by intracerebroventricular delivery of VEGF in a rat model of ALS. Nat Neurosci 2005;8:85-92 (Pubitemid 41236736)
50. Svendsen CN, Caldwell MA, Shen J, ter Borg MG, Rosser AE, Tyers P, Karmiol S, Dunnett SB. Long-term survival of human central nervous system progenitor cells transplanted into a rat model of Parkinson's disease. Exp Neurol 1997;148:135-146
51. Suzuki M, McHugh J, Tork C, Shelley B, Klein SM, Aebischer P, Svendsen CN. 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 2007a;2:e689 (Pubitemid 351325410)
52. Suzuki M, Tork C, Shelley B, McHugh J, Wallace K, Klein SM, Lindstrom MJ, Svendsen CN. Sexual dimorphism in disease onset and progression of a rat model of ALS. Amyotroph Lateral Scler 2007b;8:20-25 (Pubitemid 46322935)
53. Van Damme P, Bogaert E, Dewil M, Hersmus N, Kiraly D, Scheveneels W, Bockx I, Braeken D, Verpoorten N, Verhoeven K, Timmerman V, Herijgers P, Callewaert G, Carmeliet P, Van Den Bosch L, Robberecht W. Astrocytes regulate GluR2 expression in motor neurons and their vulnerability to excitotoxicity. Proc Natl Acad Sci USA 2007;1 04:14825-14830 (Pubitemid 350003227)
54. Williamson TL, Cleveland DW. Slowing of axonal transport is a very early event in the toxicity of ALS-linked SOD1 mutants to motor neurons. Nat Neurosci 1999;2:50-56
55. Woodhall E, West AK, Chuah MI. Cultured olfactory ensheathing cells express nerve growth factor, brain-derived neurotrophic factor, glia cell line-derived neurotrophic factor and their receptors. Brain Res Mol Brain Res 2001;88:203-213 (Pubitemid 32274278)
56. Wu P, Tarasenko YI, Gu Y, Huang LY, Coggeshall RE, Yu Y. Region-specific generation of cholinergic neurons from fetal human neural stem cells grafted in adult rats. Nat Neurosci 2002;5:1271-1278 (Pubitemid 35417761)
57. Xu L, Yan J, Chen D, Welsh AM, Hazel T, Johe K, Hatfield G, Koliatsos VE. Human neural stem cell grafts ameliorate motor neuron disease in SOD-1 transgenic rats. Transplantation 2006;82:865-875 (Pubitemid 44564030)
58. Yasuhara T, Shingo T, Muraoka K, wen Ji Y, Kameda M, Takeuchi A, Yano A, Nishio S, Matsui T, Miyoshi Y, Hamada H, Date I. The differences between high and low-dose administration of VEGF to dopaminergic neurons of in vitro and in vivo Parkinson's disease model. Brain Res 2005;1038:1-10
59. Yamanaka K, Chun SJ, Boillee S, Fujimori-Tonou N, Yamashita H, Gutmann DH, Takahashi R, Misawa H, Cleveland DW. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat Neurosci 2008a;11:251-253 (Pubitemid 351311795)
60. Yamanaka K, Boillee S, Roberts EA, Garcia ML, McAlonis- Downes M, Mikse OR, Cleveland DW, Goldstein LS. Mutant SOD1 in cell types other than motor neurons and oligodendrocytes accelerates onset of disease in ALS mice. Proc Natl Acad Sci USA 2008b;105:7594-7599 (Pubitemid 351830063)
61. Yan J, Xu L, Welsh AM, Chen D, Hazel T, Johe K, Koliatsos VE. Combined immunosuppressive agents or CD4 antibodies prolong survival of human neural stem cell grafts and improve disease outcomes in amyotrophic lateral sclerosis transgenic mice. Stem Cells 2006;24:1976-1985 (Pubitemid 44474174)