Stem Cell Reviews and Reports

, Volume 8, Issue 1, pp 279–287 | Cite as

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

  • Raquel Manzano
  • Janne M. Toivonen
  • Ana Cristina Calvo
  • Sara Oliván
  • Pilar Zaragoza
  • Maria Jesús Muñoz
  • Didier Montarras
  • Rosario Osta
Article

Supplementary material

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12015_2011_9268_MOESM2_ESM.wmv (25.2 mb)
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References

  1. 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.PubMedGoogle Scholar
  2. 2.
    Julien, J. P., & Kriz, J. (2006). Transgenic mouse models of amyotrophic lateral sclerosis. Biochimica et Biophysica Acta, 1762(11–12), 1013–1024.PubMedGoogle Scholar
  3. 3.
    Kato, S. (2008). Amyotrophic lateral sclerosis models and human neuropathology: similarities and differences. Acta Neuropathologica, 115(1), 97–114.PubMedCrossRefGoogle Scholar
  4. 4.
    Shibata, N. (2001). Transgenic mouse model for familial amyotrophic lateral sclerosis with superoxide dismutase-1 mutation. Neuropathology, 21(1), 82–92.PubMedCrossRefGoogle Scholar
  5. 5.
    Gurney, M. E. (1994). Transgenic-mouse model of amyotrophic lateral sclerosis. The New England Journal of Medicine, 331(25), 1721–1722.PubMedCrossRefGoogle Scholar
  6. 6.
    Gurney, M. E. (1997). Transgenic animal models of familial amyotrophic lateral sclerosis. Journal of Neurology, 244(Suppl 2), S15–S20.PubMedCrossRefGoogle Scholar
  7. 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.PubMedCrossRefGoogle Scholar
  8. 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.PubMedGoogle Scholar
  9. 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.PubMedGoogle Scholar
  10. 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.PubMedGoogle Scholar
  11. 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.PubMedCrossRefGoogle Scholar
  12. 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.PubMedCrossRefGoogle Scholar
  13. 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.PubMedCrossRefGoogle Scholar
  14. 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.PubMedCrossRefGoogle Scholar
  15. 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.PubMedCrossRefGoogle Scholar
  16. 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.PubMedCrossRefGoogle Scholar
  17. 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.PubMedCrossRefGoogle Scholar
  18. 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.PubMedCrossRefGoogle Scholar
  19. 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.PubMedCrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. 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.PubMedCrossRefGoogle Scholar
  22. 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.PubMedCrossRefGoogle Scholar
  23. 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.PubMedCrossRefGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. 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.PubMedCrossRefGoogle Scholar
  26. 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.PubMedCrossRefGoogle Scholar
  27. 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.PubMedCrossRefGoogle Scholar
  28. 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.PubMedCrossRefGoogle Scholar
  29. 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.PubMedCrossRefGoogle Scholar
  30. 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.PubMedCrossRefGoogle Scholar
  31. 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.PubMedCrossRefGoogle Scholar
  32. 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.PubMedCrossRefGoogle Scholar
  33. 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.PubMedCrossRefGoogle Scholar
  34. 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.CrossRefGoogle Scholar
  35. 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.PubMedCrossRefGoogle Scholar
  36. 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.Google Scholar
  37. 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.PubMedCrossRefGoogle Scholar
  38. 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.PubMedCrossRefGoogle Scholar
  39. 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.PubMedCrossRefGoogle Scholar
  40. 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.PubMedCrossRefGoogle Scholar
  41. 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.PubMedCrossRefGoogle Scholar
  42. 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.PubMedCrossRefGoogle Scholar
  43. 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.PubMedCrossRefGoogle Scholar
  44. 44.
    Buckingham, M. (2007). Skeletal muscle progenitor cells and the role of Pax genes. Comptes Rendus Biologies, 330(6–7), 530–533.PubMedCrossRefGoogle Scholar
  45. 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.PubMedCrossRefGoogle Scholar
  46. 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.PubMedCrossRefGoogle Scholar
  47. 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.PubMedCrossRefGoogle Scholar
  48. 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.PubMedGoogle Scholar
  49. 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.PubMedGoogle Scholar
  50. 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.PubMedCrossRefGoogle Scholar
  51. 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.PubMedCrossRefGoogle Scholar
  52. 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.PubMedCrossRefGoogle Scholar
  53. 53.
    Collins, C. A., & Partridge, T. A. (2005). Self-renewal of the adult skeletal muscle satellite cell. Cell Cycle, 4(10), 1338–1341.PubMedCrossRefGoogle Scholar
  54. 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.PubMedCrossRefGoogle Scholar
  55. 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.PubMedCrossRefGoogle Scholar
  56. 56.
    Hawke, T. J., & Garry, D. J. (2001). Myogenic satellite cells: physiology to molecular biology. Journal of Applied Physiology, 91(2), 534–551.PubMedGoogle Scholar
  57. 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.PubMedCrossRefGoogle Scholar
  58. 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.PubMedCrossRefGoogle Scholar
  59. 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.PubMedCrossRefGoogle Scholar
  60. 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.PubMedGoogle Scholar
  61. 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.PubMedCrossRefGoogle Scholar
  62. 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.PubMedCrossRefGoogle Scholar
  63. 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.Google Scholar
  64. 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.PubMedCrossRefGoogle Scholar
  65. 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.PubMedGoogle Scholar
  66. 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.PubMedCrossRefGoogle Scholar
  67. 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.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Raquel Manzano
    • 1
  • Janne M. Toivonen
    • 1
  • Ana Cristina Calvo
    • 1
  • Sara Oliván
    • 1
  • Pilar Zaragoza
    • 1
  • Maria Jesús Muñoz
    • 1
  • Didier Montarras
    • 2
  • Rosario Osta
    • 1
    • 3
  1. 1.LAGENBIO-I3A, Instituto Aragonés de Ciencias de la Salud (IACS)Universidad de ZaragozaZaragozaSpain
  2. 2.Unité de Génétique Moléculaire du Développement, Centre National de la Recherche Scientifique URA 2578, Département de Biologie du Développement, Institut PasteurParis Cedex 15France
  3. 3.LAGENBIO-I3A, Instituto Aragonés de Ciencias de la Salud (IACS)University of ZaragozaZaragozaSpain

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