Distinct Embryonic and Adult Fates of Multipotent Myogenic Progenitors Isolated from Skeletal Muscle and Bone Marrow
Cell Biology
Volume 3, Issue 4, November 2015, Pages: 58-73
Received: Dec. 30, 2015; Published: Dec. 30, 2015
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Authors
Zhuqing Qu-Petersen, The Copenhagen Muscle Research Center, National University Hospital, Copenhagen, Denmark
Jesper L. Andersen, Institute of Sports Medicine and Center for Healthy Aging, University of Copenhagen, Bispebjerg Hospital, Copenhagen, Denmark
Shi Zhou, School of Health and Human Sciences, Southern Cross University, Lismore, Australia
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Abstract
Identification of multipotent progenitors has been difficult due to their rarity in adults. Here, we report a novel type of neuroepithelial myogenic progenitor that can be isolated from adult murine skeletal muscle. In culture, these progenitors generated radial glia-like cells that initiated mosaic myotubes, and subsequently developed into embryonic/fetal-like myoblasts capable of robust myofiber formation. These cells could also differentiate into neuronal lineage. By contrast, progenitors from bone marrow produced progenies more uniformly of an adult myoblast lineage. When grafted into dystrophic muscles of mdx mice, the muscle- and marrow-derived cells restored dystrophin expression; however, fetal-like myogenesis towards a defective adult fate was demonstrated in the muscle-derived cells. This impaired regenerative capacity resembled Duchenne muscular dystrophy patients, suggesting a potential connection between the neuroepithelial myogenic progenitor and the etiology of this myopathy. The distinct fates of the two types of progenitors imply their different roles in muscle regeneration and pathogenesis.
Keywords
Neuroepithelial Myogenic Progenitors, Bone Marrow Myogenic Cells, Neural Differentiation, Myogenesis, Cell Transplantation, Muscular Dystrophy
To cite this article
Zhuqing Qu-Petersen, Jesper L. Andersen, Shi Zhou, Distinct Embryonic and Adult Fates of Multipotent Myogenic Progenitors Isolated from Skeletal Muscle and Bone Marrow, Cell Biology. Vol. 3, No. 4, 2015, pp. 58-73. doi: 10.11648/j.cb.20150304.12
References
[1]
Weissman, I. L. (2000). Stem cells: units of development, units of regeneration, and units in evolution. Cell 100, 157–168.
[2]
Fuchs, E., and Segre, J. A. (2000). Stem cells: a new lease on life. Cell 100, 143–155.
[3]
Sell, S. (2004). Stem cell handbook. (Humana Press, Totowa).
[4]
Salero, E., Blenkinsop, T. A., Corneo, B., Harris, A., Rabin, D., Stern, J. H., and Temple, S. (2012). Adult human RPE can be activated into a multipotent stem cell that produces mesenchymal derivatives. Cell Stem Cell 10, 88–95.
[5]
Gussoni, E., Soneoka, Y., Strickland, C. D., Buzney, E. A., Khan, M. K., Flint, A. F., Kunkel, L. M., and Mulligan, R. C. (1999). Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401, 390–394.
[6]
Qu-Petersen, Z., Deasy, B., Jankowski, R., Ikezawa, M., Cummins, J., Pruchnic, R., Mytinger, J., Cao, B., Gates, C., Wernig, A., et al. (2002). Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J. Cell Biol. 157, 851–864.
[7]
Corbel, S. Y., Lee, A., Yi, L., Duenas, J., Brazelton, T. R., Blau, H. M., and Rossi, F. M. (2003). Contribution of hematopoietic stem cells to skeletal muscle. Nat. Med. 9, 1528–1532.
[8]
Dezawa, M., Ishikawa, H., Itokazu, Y., Yoshihara, T., Hoshino, M., Takeda, S., Ide, C., and Nabeshima, Y. (2005). Bone marrow stromal cells generate muscle cells and repair muscle degeneration. Science 309, 314–317.
[9]
Sampaolesi, M., Blot, S., D’Antona, G., Granger, N., Tonlorenzi, R., Innocenzi, A., Mognol, P., Thibaud, J. L., Galvez, B. G., Barthelemy, I., et al. (2006). Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444, 574–579.
[10]
Zhang, Y., Zhu, Y., Li, Y., Cao, J., Zhang, H., Chen, M., Wang, L., and Zhang, C. (2015). Long-term engraftment of myogenic progenitors from adipose-derived stem cells and muscle regeneration in dystrophic mice. Hum. Mol. Genet. 24, 6029–6040.
[11]
Fujita, R., Tamai, K., Aikawa, E., Nimura, K., Ishino, S., Kikuchi, Y., and Kaneda, Y. (2015). Endogenous mesenchymal stromal cells in bone marrow are required to preserve muscle function in mdx mice. Stem Cells 33, 962–975.
[12]
Hoffman, E. P., Brown, R. H., and Kunkel, L. M. (1987). Dystrophin: the protein product of the Duchenne Muscular Dystrophy locus. Cell 51, 919–928.
[13]
Briggs, D., and Morgan, J. E. (2013). Recent progress in satellite cell/myoblast engraftment: relevance for therapy. FEBS J. 280, 4281–4293.
[14]
Negroni, E., Gidaro, T., Bigot, A., Butler-Browne, G. S., Mouly, V., and Trollet, C. (2015). Invited review: Stem cells and muscle diseases: advances in cell therapy strategies. Neuropathol. Appl. Neurobiol. 41, 270–287.
[15]
Lapidos, K. A., Chen, Y. E., Earley, J. U., Heydemann, A., Huber, J. M., Chien, M., Ma, A., and McNally, E. M. (2004). Transplanted hematopoietic stem cells demonstrate impaired sarcoglycan expression after engraftment into cardiac and skeletal muscle. J. Clin. Invest. 114, 1577–1585.
[16]
Montarras, D., Morgan, J., Collins, C., Relaix, F., Zaffran, S., Cumano, A., Partridge, T., and Buckingham, M. (2005). Direct isolation of satellite cells for skeletal muscle regeneration. Science 309, 2064–2067.
[17]
Cerletti, M., Jurga, S., Witczak, C. A., Hirshman, M. F., Shadrach, J. L., Goodyear, L. J., and Wagers, A. J. (2008). Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell 134, 37–47.
[18]
Tanaka, K. K., Hall, J. K., Troy, A. A., Cornelison, D. D., Majka, S. M., and Olwin, B. B. (2009). Syndecan-4-expressing muscle progenitor cells in the SP engraft as satellite cells during muscle regeneration. Cell Stem Cell 4, 217–225.
[19]
Gang, E. J., Darabi, R., Bosnakovski, D., Xu, Z., Kamm, K. E., Kyba, M., and Perlingeiro, R. C. (2009). Engraftment of mesenchymal stem cells into dystrophin-deficient mice is not accompanied by functional recovery. Exp. Cell Res. 315, 2624–2636.
[20]
Darabi, R., Gehlbach, K., Bachoo, R. M., Kamath, S., Osawa, M., Kamm, K. E., Kyba, M., and Perlingeiro, R. C. (2008). Functional skeletal muscle regeneration from differentiating embryonic stem cells. Nat. Med. 14, 134–143.
[21]
Davies, K. E., and Grounds, M. D. (2006). Treating muscular dystrophy with stem cells? Cell 127, 1304–1306.
[22]
Partridge, T. (2008) Denominator problems in a muscle stem cell study? Cell 135, 997–998.
[23]
Weiss, S. W., and Goldblum, J. R. (2001). Enzinger and Weiss’s soft tissue tumors. (Mosby, London).
[24]
Hendrix, M. J., Seftor, E. A., Seftor, R. E., Kasemeier-Kulesa, J., Kulesa, P. M., and Postovit, L. M. (2007). Reprogramming metastatic tumour cells with embryonic microenvironments. Nat. Rev. Cancer 7, 246–255.
[25]
Richler, C., and Yaffe, D. (1970). The in vitro cultivation and differentiation capacities of myogenic cell lines. Dev. Biol. 23, 1–22.
[26]
Rando, T. A., and Blau, H. M. (1994). Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J. Cell Biol. 125, 1275–1287.
[27]
Delaporte, C., Dautreaux, B., and Fardeau, M. (1986). Human myotube differentiation in vitro in different culture conditions. Biol. Cell 57, 17–22.
[28]
Lendahl, U., Zimmerman, L. B., and McKay, R. D. (1990). CNS stem cells express a new class of intermediate filament protein. Cell 60, 585–595.
[29]
Goulding, M., Lumsden, A., and Paquette, A. J. (1994). Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 120, 957–971.
[30]
Murphy, M., and Kardon, G. (2011). Origin of vertebrate limb muscle: the role of progenitor and myoblast populations. Curr. Top Dev. Biol. 96, 1–32.
[31]
Buckingham, M., and Relaix, F. (2015). PAX3 and PAX7 as upstream regulators of myogenesis. 44, 115–125.
[32]
Plaks, V., Kong, N., and Werb, Z. (2015). The cancer stem cell niche: how essential is the niche in regulating stemness of tumor cells? Cell Stem Cell 16, 225–238.
[33]
Bonner, P. H., and Hauschka, S. D. (1974). Clonal analysis of vertebrate myogenesis: I. Early developmental events in the chick limb. Dev. Biol. 37, 317–328.
[34]
Stockdale, F. E. (1992). Myogenic cell lineages. Del. Biol. 154, 284–298.
[35]
Cho, M., Webster, S. G., and Blau, H. M. (1993). Evidence for myoblast-extrinsic regulation of slow myosin heavy chain expression during muscle fiber formation in embryonic development. J. Cell Biol. 121, 795–810.
[36]
Maximow, A. A., and Bloom, W. (1948). A text book of histology. (W.B. Saunders Company, Philadelphia), pp.167–171.
[37]
Schmalbruch, H. (1976). The morphology of regeneration of skeletal muscles in the rat. Tissue Cell 8, 673–692.
[38]
Morgan, J. E., Pagel, C. N., Sherratt, T., and Partridge, T. A. (1993). Long-term persistence and migration of myogenic cells injected into pre-irradiated muscles of mdx mice. J. Neurol. Sci. 115, 191–200.
[39]
Pin, C. L., and Merrifield, P. A. (1997). Developmental potential of rat L6 myoblasts in vivo following injection into regenerating muscles. Dev. Biol. 188, 147–166.
[40]
Cornelison, D. D., and Wold, B. J. (1997). Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev. Boil. 191, 270–283.
[41]
Zhao, P., and Hoffman, E. P. (2004). Embryonic myogenesis pathways in muscle regerenation. Dev. Dyn. 229, 380–392.
[42]
Coulton, G. R., Morgan, J. E., Partridge, T. A., and Sloper, J. C. (1988). The mdx mouse skeletal muscle myopathy: I. A histological, morphometric and biochemical investigation. Neuropathol. Appl. Neurobiol. 14, 53–70.
[43]
Xu, X., Wilschut, K. J., Kouklis, G., Tian, H., Hesse, R., Garland, C., Sbitany, H., Seth, R., Knott, P. D., Hoffman, W. Y., et al. (2015). Human satellite cell transplantation and regeneration from diverse skeletal muscles. Stem Cell Reports 5, 419–434.
[44]
Dellavalle, A., Sampaolesi, M., Tonlorenzi, R., Tagliafico, E., Sacchetti, B., Perani, L., Innocenzi, A., Galvez, B. G., Messina, G., Morosetti, R., et al. (2007). Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat. Cell Biol. 9, 255–267.
[45]
Mitchell, K. J., Pannerec, A., Cadot, B., Parlakian, A., Besson, V., Gomes, E. R., Marazzi, G., and Sassoon, D. A. (2010). Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat. Cell Biol. 12, 257–266.
[46]
Kostallari, E., Baba-Amer, Y., Alonso-Martin, S., Ngoh, P., Relaix, F., Lafuste, P., and Gherardi, R. K. (2015). Pericytes in the myovascular niche promote post-natal myofiber growth and satellite cell quiescence. Development 124, 1242–1253.
[47]
Lepper, C., Conway, S. J., and Fan, C. M. (2009). Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 460, 627–631.
[48]
Neal, A., Boldrin, L., and Morgan, J. E. (2012). The satellite cell in male and female, developing and adult mouse muscle: distinct stem cells for growth and regeneration. PLoS One 7, e37950.
[49]
Seale, P., Sabourin, L. A., Girgis-Gabardo, A., Mansouri, A., Gruss, P., and Rudnicki, M. A. (2000). Pax7 is required for the specification of myogenic satellite cells. Cell 102, 777–786.
[50]
Romero-Ramos, M., Vourc'h, P., Young, H. E., Lucas, P. A., Wu, Y., Chivatakarn, O., Zaman, R., Dunkelman, N., el-Kalay, M. A., and Chesselet, M. F. (2002). Neuronal differentiation of stem cells isolated from adult muscle. J. Neurosci. Res. 69, 894–907.
[51]
Arsic, N., Mamaeva, D., Lamb, N. J., and Fernandez, A. (2008). Muscle-derived stem cells isolated as non-adherent population give rise to cardiac, skeletal muscle and neural lineages. Exp. Cell Res. 314, 1266–1280.
[52]
Chanas-Sacre, G., Rogister, B., Moonen, G., and Leprince, P. (2000). Radial glia phenotype: origin, regulation, and transdifferentiation. J. Neurosci. Res. 61, 357–363.
[53]
Boldrin, L., Zammit, P. S., and Morgan, J. E. (2014). Satellite cells from dystrophic muscle retain regenerative capacity. Stem Cell Res. 14, 20–29.
[54]
Dubowitz, V. (1985). Muscle biopsy: A practical approach. (Bailliere Tindall, London), pp. 294.
[55]
Karpati, G., Carpenter, S., and Prescott, S. (1988). Small-caliber skeletal muscle fibers do not suffer necrosis in mdx mouse dystrophy. Muscle Nerve 11, 795–803.
[56]
Blau, H. M., Webster, C., and Pavlath, G. K. (1983). Defective myoblasts identified in Duchenne muscular dystrophy. Proc. Natl. Acad. Sci. USA 80, 4856–4860.
[57]
Delaporte, C., Dehaupas, M., Fardeau, M. (1984). Comparison between the growth pattern of cell cultures from normal and Duchenne dystrophy muscle. J. Neurol. Sci. 64, 149–160.
[58]
Maier, F., and Bornemann, A. (1999). Comparison of the muscle fiber diameter and satellite cell frequency in human muscle biopsies. Muscle Nerve 22, 578–583.
[59]
Yokota, T., Lu, Q. L., Morgan, J. E., Davies, K. E., Fisher, R., Takeda, S., and Partridge, T. A. (2006). Expansion of revertant fibers in dystrophic mdx muscles reflects activity of muscle precursor cells and serves as an index of muscle regeneration. J. Cell Sci. 119, 2679–2687.
[60]
Schiaffino, S., Gorza, L., Pitton, G., Saggin, L., Ausoni, S., Sartore, S., and Lømo, T. (1988). Embryonic and neonatal myosin heavy chain in denervated and paralyzed rat skeletal muscle. Dev. Biol. 127, 1–11.
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