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Quantity and Activation of Myofiber-Associated Satellite Cells in a Mouse Model of Amyotrophic Lateral Sclerosis

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References

  1. Gros-Louis, F., Gaspar, C., & Rouleau, G. A. (2006). Genetics of familial and sporadic amyotrophic lateral sclerosis. Biochimica et Biophysica Acta, 1762(11–12), 956–972.

    PubMed  CAS  Google Scholar 

  2. Julien, J. P., & Kriz, J. (2006). Transgenic mouse models of amyotrophic lateral sclerosis. Biochimica et Biophysica Acta, 1762(11–12), 1013–1024.

    PubMed  CAS  Google Scholar 

  3. Kato, S. (2008). Amyotrophic lateral sclerosis models and human neuropathology: similarities and differences. Acta Neuropathologica, 115(1), 97–114.

    Article  PubMed  Google Scholar 

  4. Shibata, N. (2001). Transgenic mouse model for familial amyotrophic lateral sclerosis with superoxide dismutase-1 mutation. Neuropathology, 21(1), 82–92.

    Article  PubMed  CAS  Google Scholar 

  5. Gurney, M. E. (1994). Transgenic-mouse model of amyotrophic lateral sclerosis. The New England Journal of Medicine, 331(25), 1721–1722.

    Article  PubMed  CAS  Google Scholar 

  6. Gurney, M. E. (1997). Transgenic animal models of familial amyotrophic lateral sclerosis. Journal of Neurology, 244(Suppl 2), S15–S20.

    Article  PubMed  Google Scholar 

  7. Miana-Mena, F. J., Munoz, M. J., Yague, G., et al. (2005). Optimal methods to characterize the G93A mouse model of ALS. Amyotrophic Lateral Sclerosis and Other Motor Neuron Disorders, 6(1), 55–62.

    Article  PubMed  CAS  Google Scholar 

  8. Lino, M. M., Schneider, C., & Caroni, P. (2002). Accumulation of SOD1 mutants in postnatal motoneurons does not cause motoneuron pathology or motoneuron disease. The Journal of Neuroscience, 22(12), 4825–4832.

    PubMed  CAS  Google Scholar 

  9. Pramatarova, A., Laganiere, J., Roussel, J., Brisebois, K., & Rouleau, G. A. (2001). Neuron-specific expression of mutant superoxide dismutase 1 in transgenic mice does not lead to motor impairment. The Journal of Neuroscience, 21(10), 3369–3374.

    PubMed  CAS  Google Scholar 

  10. Gong, Y. H., Parsadanian, A. S., Andreeva, A., Snider, W. D., & Elliott, J. L. (2000). Restricted expression of G86R Cu/Zn superoxide dismutase in astrocytes results in astrocytosis but does not cause motoneuron degeneration. The Journal of Neuroscience, 20(2), 660–665.

    PubMed  CAS  Google Scholar 

  11. Beers, D. R., Henkel, J. S., Xiao, Q., et al. (2006). Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proceedings of the National Academy of Sciences of the United States of America, 103(43), 16021–16026.

    Article  PubMed  CAS  Google Scholar 

  12. Nagai, M., Re, D. B., Nagata, T., et al. (2007). Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nature Neuroscience, 10(5), 615–622.

    Article  PubMed  CAS  Google Scholar 

  13. Yamanaka, K., Chun, S. J., Boillee, S., et al. (2008). Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nature Neuroscience, 11(3), 251–253.

    Article  PubMed  CAS  Google Scholar 

  14. Boillee, S., Vande Velde, C., & Cleveland, D. W. (2006). ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron, 52(1), 39–59.

    Article  PubMed  CAS  Google Scholar 

  15. Martin, L. J., & Liu, Z. (2007). 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. Journal of Neuropathology and Experimental Neurology, 66(11), 1002–1018.

    Article  PubMed  CAS  Google Scholar 

  16. Clement, A. M., Nguyen, M. D., Roberts, E. A., et al. (2003). Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science, 302(5642), 113–117.

    Article  PubMed  CAS  Google Scholar 

  17. Aguirre, T., Van Den Bosch, L., Goetschalckx, K., et al. (1998). Increased sensitivity of fibroblasts from amyotrophic lateral sclerosis patients to oxidative stress. Annals of Neurology, 43(4), 452–457.

    Article  PubMed  CAS  Google Scholar 

  18. McEachern, G., Kassovska-Bratinova, S., Raha, S., et al. (2000). Manganese superoxide dismutase levels are elevated in a proportion of amyotrophic lateral sclerosis patient cell lines. Biochemical and Biophysical Research Communications, 273(1), 359–363.

    Article  PubMed  CAS  Google Scholar 

  19. Cova, E., Cereda, C., Galli, A., et al. (2006). Modified expression of Bcl-2 and SOD1 proteins in lymphocytes from sporadic ALS patients. Neuroscience Letters, 399(3), 186–190.

    Article  PubMed  CAS  Google Scholar 

  20. Dupuis, L., Gonzalez de Aguilar, J. L., Echaniz-Laguna, A., & Loeffler, J. P. (2006). Mitochondrial dysfunction in amyotrophic lateral sclerosis also affects skeletal muscle. Muscle & Nerve, 34(2), 253–254.

    Article  Google Scholar 

  21. Wiedemann, F. R., Winkler, K., Kuznetsov, A. V., et al. (1998). Impairment of mitochondrial function in skeletal muscle of patients with amyotrophic lateral sclerosis. Journal of the Neurological Sciences, 156(1), 65–72.

    Article  PubMed  CAS  Google Scholar 

  22. Brooks, K. J., Hill, M. D., Hockings, P. D., & Reid, D. G. (2004). MRI detects early hindlimb muscle atrophy in Gly93Ala superoxide dismutase-1 (G93A SOD1) transgenic mice, an animal model of familial amyotrophic lateral sclerosis. NMR in Biomedicine, 17(1), 28–32.

    Article  PubMed  Google Scholar 

  23. Fischer, L. R., Culver, D. G., Tennant, P., et al. (2004). Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Experimental Neurology, 185(2), 232–240.

    Article  PubMed  Google Scholar 

  24. Chiu, A. Y., Zhai, P., Dal Canto, M. C., et al. (1995). Age-dependent penetrance of disease in a transgenic mouse model of familial amyotrophic lateral sclerosis. Molecular and Cellular Neurosciences, 6(4), 349–362.

    Article  PubMed  CAS  Google Scholar 

  25. Dupuis, L., & Loeffler, J. P. (2009). Neuromuscular junction destruction during amyotrophic lateral sclerosis: insights from transgenic models. Current Opinion in Pharmacology, 9(3), 341–346.

    Article  PubMed  CAS  Google Scholar 

  26. Krasnianski, A., Deschauer, M., Neudecker, S., et al. (2005). Mitochondrial changes in skeletal muscle in amyotrophic lateral sclerosis and other neurogenic atrophies. Brain, 128(Pt 8), 1870–1876.

    Article  PubMed  Google Scholar 

  27. Vielhaber, S., Winkler, K., Kirches, E., et al. (1999). Visualization of defective mitochondrial function in skeletal muscle fibers of patients with sporadic amyotrophic lateral sclerosis. Journal of the Neurological Sciences, 169(1–2), 133–139.

    Article  PubMed  CAS  Google Scholar 

  28. Comi, G. P., Bordoni, A., Salani, S., et al. (1998). Cytochrome c oxidase subunit I microdeletion in a patient with motor neuron disease. Annals of Neurology, 43(1), 110–116.

    Article  PubMed  CAS  Google Scholar 

  29. Echaniz-Laguna, A., Zoll, J., Ponsot, E., et al. (2006). Muscular mitochondrial function in amyotrophic lateral sclerosis is progressively altered as the disease develops: a temporal study in man. Experimental Neurology, 198(1), 25–30.

    Article  PubMed  CAS  Google Scholar 

  30. Corti, S., Donadoni, C., Ronchi, D., et al. (2009). Amyotrophic lateral sclerosis linked to a novel SOD1 mutation with muscle mitochondrial dysfunction. Journal of the Neurological Sciences, 276(1–2), 170–174.

    Article  PubMed  CAS  Google Scholar 

  31. Vielhaber, S., Kornblum, C., Heinze, H. J., Elger, C. E., & Kunz, W. S. (2005). Mitochondrial changes in skeletal muscle in amyotrophic lateral sclerosis and other neurogenic atrophies–a comment. Brain, 128(Pt 12), E38.

    Article  PubMed  Google Scholar 

  32. Derave, W., Van Den Bosch, L., Lemmens, G., Eijnde, B. O., Robberecht, W., & Hespel, P. (2003). Skeletal muscle properties in a transgenic mouse model for amyotrophic lateral sclerosis: effects of creatine treatment. Neurobiology of Disease, 13(3), 264–272.

    Article  PubMed  CAS  Google Scholar 

  33. Dupuis, L., Oudart, H., Rene, F., Gonzalez de Aguilar, J. L., & Loeffler, J. P. (2004). Evidence for defective energy homeostasis in amyotrophic lateral sclerosis: benefit of a high-energy diet in a transgenic mouse model. Proceedings of the National Academy of Sciences of the United States of America, 101(30), 11159–11164.

    Article  PubMed  CAS  Google Scholar 

  34. Mahoney, D. J., Kaczor, J. J., Bourgeois, J., Yasuda, N., & Tarnopolsky, M. A. (2006). Oxidative stress and antioxidant enzyme upregulation in SOD1-G93A mouse skeletal muscle. Muscle & Nerve, 33(6), 809–816.

    Article  CAS  Google Scholar 

  35. Dobrowolny, G., Aucello, M., Rizzuto, E., et al. (2008). Skeletal muscle is a primary target of SOD1G93A-mediated toxicity. Cell Metabolism, 8(5), 425–436.

    Article  PubMed  CAS  Google Scholar 

  36. Wong, M., & Martin, L. J. Skeletal muscle-restricted expression of human SOD1 causes motor neuron degeneration in transgenic mice. Human Molecular Genetics, 19(11), 2284–2302.

  37. Dobrowolny, G., Aucello, M., Molinaro, M., & Musaro, A. (2008). Local expression of mIgf-1 modulates ubiquitin, caspase and CDK5 expression in skeletal muscle of an ALS mouse model. Neurological Research, 30(2), 131–136.

    Article  PubMed  CAS  Google Scholar 

  38. Dobrowolny, G., Giacinti, C., Pelosi, L., et al. (2005). Muscle expression of a local Igf-1 isoform protects motor neurons in an ALS mouse model. The Journal of Cell Biology, 168(2), 193–199.

    Article  PubMed  CAS  Google Scholar 

  39. Jokic, N., Gonzalez de Aguilar, J. L., Dimou, L., et al. (2006). The neurite outgrowth inhibitor Nogo-A promotes denervation in an amyotrophic lateral sclerosis model. EMBO Reports, 7(11), 1162–1167.

    Article  PubMed  CAS  Google Scholar 

  40. Kaspar, B. K., Llado, J., Sherkat, N., Rothstein, J. D., & Gage, F. H. (2003). Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science, 301(5634), 839–842.

    Article  PubMed  CAS  Google Scholar 

  41. Ates, K., Yang, S. Y., Orrell, R. W., et al. (2007). The IGF-I splice variant MGF increases progenitor cells in ALS, dystrophic, and normal muscle. FEBS Letters, 581(14), 2727–2732.

    Article  PubMed  CAS  Google Scholar 

  42. Musaro, A., Giacinti, C., Borsellino, G., et al. (2004). Stem cell-mediated muscle regeneration is enhanced by local isoform of insulin-like growth factor 1. Proceedings of the National Academy of Sciences of the United States of America, 101(5), 1206–1210.

    Article  PubMed  CAS  Google Scholar 

  43. Seale, P., & Rudnicki, M. A. (2000). A new look at the origin, function, and “stem-cell” status of muscle satellite cells. Developmental Biology, 218(2), 115–124.

    Article  PubMed  CAS  Google Scholar 

  44. Buckingham, M. (2007). Skeletal muscle progenitor cells and the role of Pax genes. Comptes Rendus Biologies, 330(6–7), 530–533.

    Article  PubMed  CAS  Google Scholar 

  45. Zammit, P. S., Golding, J. P., Nagata, Y., Hudon, V., Partridge, T. A., & Beauchamp, J. R. (2004). Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? The Journal of Cell Biology, 166(3), 347–357.

    Article  PubMed  CAS  Google Scholar 

  46. Collins, C. A., Olsen, I., Zammit, P. S., et al. (2005). Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell, 122(2), 289–301.

    Article  PubMed  CAS  Google Scholar 

  47. Seale, P., Sabourin, L. A., Girgis-Gabardo, A., Mansouri, A., Gruss, P., & Rudnicki, M. A. (2000). Pax7 is required for the specification of myogenic satellite cells. Cell, 102(6), 777–786.

    Article  PubMed  CAS  Google Scholar 

  48. Shefer, G., & Yablonka-Reuveni, Z. (2005). Isolation and culture of skeletal muscle myofibers as a means to analyze satellite cells. Methods in Molecular Biology, 290, 281–304.

    PubMed  Google Scholar 

  49. Cooper, R. N., Tajbakhsh, S., Mouly, V., Cossu, G., Buckingham, M., & Butler-Browne, G. S. (1999). In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. Journal of Cell Science, 112(Pt 17), 2895–2901.

    PubMed  CAS  Google Scholar 

  50. Smith, C. K., 2nd, Janney, M. J., & Allen, R. E. (1994). Temporal expression of myogenic regulatory genes during activation, proliferation, and differentiation of rat skeletal muscle satellite cells. Journal of Cellular Physiology, 159(2), 379–385.

    Article  PubMed  CAS  Google Scholar 

  51. Yablonka-Reuveni, Z., & Rivera, A. J. (1994). Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Developmental Biology, 164(2), 588–603.

    Article  PubMed  CAS  Google Scholar 

  52. Asakura, A., Komaki, M., & Rudnicki, M. (2001). Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation, 68(4–5), 245–253.

    Article  PubMed  CAS  Google Scholar 

  53. Collins, C. A., & Partridge, T. A. (2005). Self-renewal of the adult skeletal muscle satellite cell. Cell Cycle, 4(10), 1338–1341.

    Article  PubMed  CAS  Google Scholar 

  54. Shefer, G., Van de Mark, D. P., Richardson, J. B., & Yablonka-Reuveni, Z. (2006). Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Developmental Biology, 294(1), 50–66.

    Article  PubMed  CAS  Google Scholar 

  55. Halevy, O., Piestun, Y., Allouh, M. Z., et al. (2004). Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Developmental Dynamics, 231(3), 489–502.

    Article  PubMed  CAS  Google Scholar 

  56. Hawke, T. J., & Garry, D. J. (2001). Myogenic satellite cells: physiology to molecular biology. Journal of Applied Physiology, 91(2), 534–551.

    PubMed  CAS  Google Scholar 

  57. Turner, B. J., Lopes, E. C., & Cheema, S. S. (2003). Neuromuscular accumulation of mutant superoxide dismutase 1 aggregates in a transgenic mouse model of familial amyotrophic lateral sclerosis. Neuroscience Letters, 350(2), 132–136.

    Article  PubMed  CAS  Google Scholar 

  58. Hegedus, J., Putman, C. T., & Gordon, T. (2007). Time course of preferential motor unit loss in the SOD1 G93A mouse model of amyotrophic lateral sclerosis. Neurobiology of Disease, 28(2), 154–164.

    Article  PubMed  CAS  Google Scholar 

  59. Pun, S., Santos, A. F., Saxena, S., Xu, L., & Caroni, P. (2006). Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nature Neuroscience, 9(3), 408–419.

    Article  PubMed  CAS  Google Scholar 

  60. Frey, D., Schneider, C., Xu, L., Borg, J., Spooren, W., & Caroni, P. (2000). Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. The Journal of Neuroscience, 20(7), 2534–2542.

    PubMed  CAS  Google Scholar 

  61. Burkholder, T. J., Fingado, B., Baron, S., & Lieber, R. L. (1994). Relationship between muscle fiber types and sizes and muscle architectural properties in the mouse hindlimb. Journal of Morphology, 221(2), 177–190.

    Article  PubMed  CAS  Google Scholar 

  62. Day, K., Shefer, G., Richardson, J. B., Enikolopov, G., & Yablonka-Reuveni, Z. (2007). Nestin-GFP reporter expression defines the quiescent state of skeletal muscle satellite cells. Developmental Biology, 304(1), 246–259.

    Article  PubMed  CAS  Google Scholar 

  63. Day, K., Shefer, G., Shearer, A., & Yablonka-Reuveni, Z. The depletion of skeletal muscle satellite cells with age is concomitant with reduced capacity of single progenitors to produce reserve progeny. Developmental Biology , 340(2), 330–343.

  64. Bradley, L. J., Taanman, J. W., Kallis, C., & Orrell, R. W. (2009). Increased sensitivity of myoblasts to oxidative stress in amyotrophic lateral sclerosis peripheral tissues. Experimental Neurology, 218(1), 92–97.

    Article  PubMed  CAS  Google Scholar 

  65. Manzano, R., Toivonen, J. M., Oliván, S., et al. (2011). Altered expression of myogenic regulatory factors in the mouse model of amyotrophic lateral sclerosis. Neurodegenerative Diseases. doi:10.1159/000324159.

    PubMed  Google Scholar 

  66. Kuschel, R., Yablonka-Reuveni, Z., & Bornemann, A. (1999). Satellite cells on isolated myofibers from normal and denervated adult rat muscle. The Journal of Histochemistry and Cytochemistry, 47(11), 1375–1384.

    Article  PubMed  CAS  Google Scholar 

  67. Halter, B., Gonzalez de Aguilar, J. L., Rene, F., et al. Oxidative stress in skeletal muscle stimulates early expression of Rad in a mouse model of amyotrophic lateral sclerosis. Free Radical Biology & Medicine, 48(7):915–923.

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Acknowledgements

The authors thank María Royo and Mamen Carreras (Microscopy and Image Service) for excellent technical assistance and help with confocal microscope, and the I+ CS/IIS Aragon (Instituto Aragonés de Ciencias de la Salud) for access to the microscope and Barbara Gayraud Morel from the Department of Developmental Biology of the Institut Pasteur for her technical and methodological assistance . This study was supported by the grant of CAJA NAVARRA: “Tú eliges, tu decides”; PI071133 and PI10/01787 from the Fondo de Investigación Sanitaria of Spain and PAMER from the Instituto Aragonés de Ciencias de la Salud (PIPAMER 09/09).

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The authors declare they have no conflict of interest.

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Authors and Affiliations

  1. LAGENBIO-I3A, Instituto Aragonés de Ciencias de la Salud (IACS), Universidad de Zaragoza, Miguel Servet 177, 50013, Zaragoza, Spain

    Raquel Manzano, Janne M. Toivonen, Ana Cristina Calvo, Sara Oliván, Pilar Zaragoza, Maria Jesús Muñoz & Rosario Osta

  2. Unité de Génétique Moléculaire du Développement, Centre National de la Recherche Scientifique URA 2578, Département de Biologie du Développement, Institut Pasteur, 75724, Paris Cedex 15, France

    Didier Montarras

  3. LAGENBIO-I3A, Instituto Aragonés de Ciencias de la Salud (IACS), University of Zaragoza, C/Miguel Servet 177, 50013, Zaragoza, Spain

    Rosario Osta

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  1. Raquel Manzano
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Correspondence to Rosario Osta.

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Manzano, R., Toivonen, J.M., Calvo, A.C. et al. Quantity and Activation of Myofiber-Associated Satellite Cells in a Mouse Model of Amyotrophic Lateral Sclerosis. Stem Cell Rev and Rep 8, 279–287 (2012). https://doi.org/10.1007/s12015-011-9268-0

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