Transplanted Modified Muscle Progenitor Cells Expressing a Mixture of Neurotrophic Factors Delay Disease Onset and Enhance Survival in the SOD1 Mouse Model of ALS

Journal of Molecular Neuroscience

Volumn 55, Issue 3, 2015, Pages 788-797

  Dadon Nachum, M ^a   Ben Yaacov, K ^a   Ben Zur, T ^a   Barhum, Y ^a   Yaffe, D ^b   Perlson, E ^a   Offen, D ^a,c  

^a TEL AVIV UNIVERSITY   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c RABIN MEDICAL CENTER   (Israel)

Author keywords

Amyotrophic lateral sclerosis (ALS); BDNF; GDNF; IGF 1; Muscle progenitor cell (MPC); Neurotrophic factors; SOD1 mice; VEGF

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NEURITE PROMOTING FACTOR; NEUROTROPHIC FACTOR; PROTEIN BAD; PROTEIN KINASE B; SOMATOMEDIN C; VASCULOTROPIN; COPPER ZINC SUPEROXIDE DISMUTASE; NERVE GROWTH FACTOR; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HINDLIMB; IMMUNOCYTOCHEMISTRY; MALE; MOTONEURON; MOTOR PERFORMANCE; MOUSE; MUSCLE STEM CELL; NONHUMAN; STEM CELL TRANSPLANTATION; SURVIVAL; SYMPTOM; TRANSGENIC MOUSE; ANIMAL; GENETICS; METABOLISM; MYOBLAST; NEUROMUSCULAR SYNAPSE; PATHOLOGY; TRANSPLANTATION;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; FEMALE; MALE; MICE; MYOBLASTS; NERVE GROWTH FACTORS; NEUROMUSCULAR JUNCTION; SUPEROXIDE DISMUTASE;

EID: 84925461075     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-014-0426-0     Document Type: Article

References (37)

1. Acsadi G, Anguelov RA, Yang H, Toth G, Thomas R, Jani A, Wang Y, Ianakova E, Mohammad S, Lewis RA et al (2002) Increased survival and function of SOD1 mice after glial cell-derived neurotrophic factor gene therapy. Hum Gene Ther 13:1047–1059
2. Arce V, Garces A, de Bovis B, Filippi P, Henderson C, Pettmann B, deLapeyriere O (1999) Cardiotrophin-1 requires LIFRbeta to promote survival of mouse motoneurons purified by a novel technique. J Neurosci Res 55:119–126
3. Azzouz M, Ralph GS, Storkebaum E, Walmsley LE, Mitrophanous KA, Kingsman SM, Carmeliet P, Mazarakis ND (2004) VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature 429:413–417
4. BDNF study group (1999) A controlled trial of recombinant methionyl human BDNF in ALS: the BDNF study group (Phase III). Neurology 52:1427–1433
5. Beauverd M, Mitchell JD, Wokke JH, Borasio GD (2012) Recombinant human insulin-like growth factor I (rhIGF-I) for the treatment of amyotrophic lateral sclerosis/motor neuron disease. Cochrane Database Syst Rev 11, CD002064
6. Benkler C, Offen D, Melamed E, Kupershmidt L, Amit T, Mandel S, Youdim MB, Weinreb O (2010) Recent advances in amyotrophic lateral sclerosis research: perspectives for personalized clinical application. EPMA J 1:343–361
7. Bosco DA, Morfini G, Karabacak NM, Song Y, Gros-Louis F, Pasinelli P, Goolsby H, Fontaine BA, Lemay N, McKenna-Yasek D et al (2010) Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nat Neurosci 13:1396–1403
8. Brown RH Jr, Robberecht W (2001) Amyotrophic lateral sclerosis: pathogenesis. Semin Neurol 21:131–139
9. Carilho R, de Carvalho M, Swash M, Pinto S, Pinto A, Costa J (2013) Vascular endothelial growth factor and amyotrophic lateral sclerosis: the interplay with exercise and non-invasive ventilation. Muscle Nerve 49(4):545–550. doi:10.1002/mus.23955
10. Chen S, Sayana P, Zhang X, Le W (2013) Genetics of amyotrophic lateral sclerosis: an update. Mol Neurodegener 8:28
11. Dadon- Nachum M, Ben-Zur T, Srugo I, Shamir HM, Melamed E, Yaffe D, Offen D (2012) Therapeutic effect of genetically modified muscle progenitor cells in a rat model of sciatic nerve injury. J Stem Cells Regen Med (JSRM) 1:21–27
12. Dadon-Nachum M, Melamed E, Offen D (2011) The “dying-back” phenomenon of motor neurons in ALS. J Mol Neurosci 43:470–477
13. deLapeyriere O, Henderson CE (1997) Motoneuron differentiation, survival and synaptogenesis. Curr Opin Genet Dev 7:642–650
14. Fischer LR, Culver DG, Tennant P, Davis AA, Wang M, Castellano-Sanchez A, Khan J, Polak MA, Glass JD (2004) Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol 185:232–240
15. Guillot S, Azzouz M, Deglon N, Zurn A, Aebischer P (2004) Local GDNF expression mediated by lentiviral vector protects facial nerve motoneurons but not spinal motoneurons in SOD1(G93A) transgenic mice. Neurobiol Dis 16:139–149
16. Hedlund E, Hefferan MP, Marsala M, Isacson O (2007) Cell therapy and stem cells in animal models of motor neuron disorders. Eur J Neurosci 26:1721–1737
17. Krakora D, Macrander C, Suzuki M (2012) Neuromuscular junction protection for the potential treatment of amyotrophic lateral sclerosis. Neurol Res Int 2012:379657
18. Krakora D, Mulcrone P, Meyer M, Lewis C, Bernau K, Gowing G, Zimprich C, Aebischer P, Svendsen CN, Suzuki M (2013) Synergistic effects of GDNF and VEGF on lifespan and disease progression in a familial ALS rat model. Mol Ther 21:1602–1610
19. Li W, Brakefield D, Pan Y, Hunter D, Myckatyn TM, Parsadanian A (2007) Muscle-derived but not centrally derived transgene GDNF is neuroprotective in G93A-SOD1 mouse model of ALS. Exp Neurol 203:457–471
20. Marcuzzo S, Zucca I, Mastropietro A, de Rosbo NK, Cavalcante P, Tartari S, Bonanno S, Preite L, Mantegazza R, Bernasconi P (2011) Hind limb muscle atrophy precedes cerebral neuronal degeneration in G93A-SOD1 mouse model of amyotrophic lateral sclerosis: a longitudinal MRI study. Exp Neurol 231:30–37
21. Mazzini L, Ferrero I, Luparello V, Rustichelli D, Gunetti M, Mareschi K, Testa L, Stecco A, Tarletti R, Miglioretti M et al (2010) Mesenchymal stem cell transplantation in amyotrophic lateral sclerosis: a phase I clinical trial. Exp Neurol 223:229–237
22. Mograbi B, Bocciardi R, Bourget I, Busca R, Rochet N, Farahi-Far D, Juhel T, Rossi B (2001) Glial cell line-derived neurotrophic factor-stimulated phosphatidylinositol 3-kinase and Akt activities exert opposing effects on the ERK pathway: importance for the rescue of neuroectodermic cells. J Biol Chem 276:45307–45319
23. Mohajeri MH, Figlewicz DA, Bohn MC (1999) Intramuscular grafts of myoblasts genetically modified to secrete glial cell line-derived neurotrophic factor prevent motoneuron loss and disease progression in a mouse model of familial amyotrophic lateral sclerosis. Hum Gene Ther 10:1853–1866
24. Moreno-Igoa M, Calvo AC, Ciriza J, Munoz MJ, Zaragoza P, Osta R (2012) Non-viral gene delivery of the GDNF, either alone or fused to the C-fragment of tetanus toxin protein, prolongs survival in a mouse ALS model. Restor Neurol Neurosci 30:69–80
25. Morren JA, Galvez-Jimenez N (2012) Current and prospective disease-modifying therapies for amyotrophic lateral sclerosis. Expert Opin Investig Drugs 21:297–320
26. Ozdinler PH, Macklis JD (2006) IGF-I specifically enhances axon outgrowth of corticospinal motor neurons. Nat Neurosci 9:1371–1381
27. Pasinelli P, Brown RH (2006) Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat Rev Neurosci 7:710–723
28. Perlson E, Jeong GB, Ross JL, Dixit R, Wallace KE, Kalb RG, Holzbaur EL (2009) A switch in retrograde signaling from survival to stress in rapid-onset neurodegeneration. J Neurosci 29:9903–9917
29. Rocha MC, Pousinha PA, Correia AM, Sebastiao AM, Ribeiro JA (2013) Early changes of neuromuscular transmission in the SOD1(G93A) mice model of ALS start long before motor symptoms onset. PLoS One 8:e73846
30. Saenger S, Holtmann B, Nilges MR, Schroeder S, Hoeflich A, Kletzl H, Spooren W, Ostrowitzki S, Hanania T, Sendtner M et al (2012) Functional improvement in mouse models of familial amyotrophic lateral sclerosis by PEGylated insulin-like growth factor I treatment depends on disease severity. Amyotroph Lateral Scler 13:418–429
31. Sagot Y, Rosse T, Vejsada R, Perrelet D, Kato AC (1998) Differential effects of neurotrophic factors on motoneuron retrograde labeling in a murine model of motoneuron disease. J Neurosci 18:1132–1141
32. Sarig R, Baruchi Z, Fuchs O, Nudel U, Yaffe D (2006) Regeneration and transdifferentiation potential of muscle-derived stem cells propagated as myospheres. Stem Cells 24:1769–1778
33. Suzuki M, McHugh J, Tork C, Shelley B, Hayes A, Bellantuono I, Aebischer P, Svendsen CN (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
34. Wang LJ, Lu YY, Muramatsu S, Ikeguchi K, Fujimoto K, Okada T, Mizukami H, Matsushita T, Hanazono Y, Kume A et al (2002) Neuroprotective effects of glial cell line-derived neurotrophic factor mediated by an adeno-associated virus vector in a transgenic animal model of amyotrophic lateral sclerosis. J Neurosci 22:6920–6928
35. Yaffe D (1968) Retention of differentiation potentialities during prolonged cultivation of myogenic cells. Proc Natl Acad Sci U S A 61:477–483
36. Yaffe D (1969) Cellular aspects of muscle differentiation in vitro. Curr Top Dev Biol 4:37–77
37. Zurn AD, Henry H, Schluep M, Aubert V, Winkel L, Eilers B, Bachmann C, Aebischer P (2000) Evaluation of an intrathecal immune response in amyotrophic lateral sclerosis patients implanted with encapsulated genetically engineered xenogeneic cells. Cell Transplant 9:471–484