Abstract
The muscular dystrophies are an heterogeneous group of inherited myopathies characterised by the progressive wasting of skeletal muscle tissue. Pericytes have been shown to make muscle in vitro and to contribute to skeletal muscle regeneration in several animal models, although recent data has shown this to be controversial. In fact, some pericyte subpopulations have been shown to contribute to fibrosis and adipose deposition in muscle. In this chapter, we explore the identity and the multifaceted role of pericytes in dystrophic muscle, potential therapeutic applications and the current need to overcome the hurdles of characterisation (both to identify pericyte subpopulations and track cell fate), to prevent deleterious differentiation towards myogenic-inhibiting subpopulations, and to improve cell proliferation and engraftment efficacy.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Al Ahmad, A., Taboada, C. B., Gassmann, M., & Ogunshola, O. O. (2011). Astrocytes and pericytes differentially modulate blood-brain barrier characteristics during development and hypoxic insult. Journal of Cerebral Blood Flow and Metabolism, 31, 693–705.
Armulik, A., Genove, G., & Betsholtz, C. (2011). Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Developmental Cell, 21, 193–215.
Armulik, A., Genove, G., Mae, M., Nisancioglu, M. H., Wallgard, E., Niaudet, C., He, L., Norlin, J., Lindblom, P., Strittmatter, K., et al. (2010). Pericytes regulate the blood-brain barrier. Nature, 468, 557–561.
Arpke, R. W., Darabi, R., Mader, T. L., Zhang, Y., Toyama, A., Lonetree, C. L., Nash, N., Lowe, D. A., Perlingeiro, R. C., & Kyba, M. (2013). A new immuno-, dystrophin-deficient model, the NSG-mdx(4Cv) mouse, provides evidence for functional improvement following allogeneic satellite cell transplantation. Stem Cells, 31, 1611–1620.
Balabanov, R., Beaumont, T., & Dore-Duffy, P. (1999). Role of central nervous system microvascular pericytes in activation of antigen-primed splenic T-lymphocytes. Journal of Neuroscience Research, 55, 578–587.
Bartoccioni, E., Gallucci, S., Scuderi, F., Ricci, E., Servidei, S., Broccolini, A., & Tonali, P. (1994). MHC class I, MHC class II and intercellular adhesion molecule-1 (ICAM-1) expression in inflammatory myopathies. Clinical and Experimental Immunology, 95, 166–172.
Benedetti, S., Hoshiya, H., & Tedesco, F. S. (2013). Repair or replace? Exploiting novel gene and cell therapy strategies for muscular dystrophies. The FEBS Journal, 280, 4263–4280.
Benedetti, S., Uno, N., Hoshiya, H., Ragazzi, M., Ferrari, G., Kazuki, Y., Moyle, L. A., Tonlorenzi, R., Lombardo, A., Chaouch, S., et al. (2018). Reversible immortalisation enables genetic correction of human muscle progenitors and engineering of next-generation human artificial chromosomes for Duchenne muscular dystrophy. EMBO Molecular Medicine, 10, 254–275.
Bengtsson, N. E., Seto, J. T., Hall, J. K., Chamberlain, J. S., & Odom, G. L. (2016). Progress and prospects of gene therapy clinical trials for the muscular dystrophies. Human Molecular Genetics, 25, R9–R17.
Bentzinger, C. F., Wang, Y. X., & Rudnicki, M. A. (2012). Building muscle: Molecular regulation of myogenesis. Cold Spring Harbor Perspectives in Biology, 4.
Berry, S. E., Liu, J., Chaney, E. J., & Kaufman, S. J. (2007). Multipotential mesoangioblast stem cell therapy in the mdx/utrn−/− mouse model for Duchenne muscular dystrophy. Regenerative Medicine, 2, 275–288.
Bianco, P., & Cossu, G. (1999). Uno, nessuno e centomila: Searching for the identity of mesodermal progenitors. Experimental Cell Research, 251, 257–263.
Birbrair, A., Borges, I. D. T., Gilson Sena, I. F., Almeida, G. G., da Silva Meirelles, L., Goncalves, R., Mintz, A., & Delbono, O. (2017). How plastic are pericytes? Stem Cells and Development, 26, 1013–1019.
Birbrair, A., Wang, Z. M., Messi, M. L., Enikolopov, G. N., & Delbono, O. (2011). Nestin-GFP transgene reveals neural precursor cells in adult skeletal muscle. PLoS One, 6, e16816.
Birbrair, A., Zhang, T., Files, D. C., Mannava, S., Smith, T., Wang, Z. M., Messi, M. L., Mintz, A., & Delbono, O. (2014). Type-1 pericytes accumulate after tissue injury and produce collagen in an organ-dependent manner. Stem Cell Research & Therapy, 5, 122.
Birbrair, A., Zhang, T., Wang, Z. M., Messi, M. L., Enikolopov, G. N., Mintz, A., & Delbono, O. (2013a). Role of pericytes in skeletal muscle regeneration and fat accumulation. Stem Cells and Development, 22, 2298–2314.
Birbrair, A., Zhang, T., Wang, Z. M., Messi, M. L., Enikolopov, G. N., Mintz, A., & Delbono, O. (2013b). Skeletal muscle pericyte subtypes differ in their differentiation potential. Stem Cell Research, 10, 67–84.
Birbrair, A., Zhang, T., Wang, Z. M., Messi, M. L., Mintz, A., & Delbono, O. (2013c). Type-1 pericytes participate in fibrous tissue deposition in aged skeletal muscle. American Journal of Physiology. Cell Physiology, 305, C1098–C1113.
Birbrair, A., Zhang, T., Wang, Z. M., Messi, M. L., Mintz, A., & Delbono, O. (2015). Pericytes at the intersection between tissue regeneration and pathology. Clinical Science (London, England), 128, 81–93.
Blau, H. M., Webster, C., & Pavlath, G. K. (1983). Defective myoblasts identified in Duchenne muscular dystrophy. Proceedings of the National Academy of Sciences of the United States of America, 80, 4856–4860.
Boldrin, L., Muntoni, F., & Morgan, J. E. (2010). Are human and mouse satellite cells really the same? The Journal of Histochemistry and Cytochemistry, 58, 941–955.
Boldrin, L., Neal, A., Zammit, P. S., Muntoni, F., & Morgan, J. E. (2012). Donor satellite cell engraftment is significantly augmented when the host niche is preserved and endogenous satellite cells are incapacitated. Stem Cells, 30, 1971–1984.
Bonfanti, C., Rossi, G., Tedesco, F. S., Giannotta, M., Benedetti, S., Tonlorenzi, R., Antonini, S., Marazzi, G., Dejana, E., Sassoon, D., et al. (2015). PW1/Peg3 expression regulates key properties that determine mesoangioblast stem cell competence. Nature Communications, 6, 6364.
Brunelli, S., Sciorati, C., D’Antona, G., Innocenzi, A., Covarello, D., Galvez, B. G., Perrotta, C., Monopoli, A., Sanvito, F., Bottinelli, R., et al. (2007). Nitric oxide release combined with nonsteroidal antiinflammatory activity prevents muscular dystrophy pathology and enhances stem cell therapy. Proceedings of the National Academy of Sciences of the United States of America, 104, 264–269.
Buckingham, M. (2006). Myogenic progenitor cells and skeletal myogenesis in vertebrates. Current Opinion in Genetics & Development, 16, 525–532.
Campagnolo, P., Cesselli, D., Al Haj Zen, A., Beltrami, A. P., Krankel, N., Katare, R., Angelini, G., Emanueli, C., & Madeddu, P. (2010). Human adult vena saphena contains perivascular progenitor cells endowed with clonogenic and proangiogenic potential. Circulation, 121, 1735–1745.
Cano, E., Gebala, V., & Gerhardt, H. (2017). Pericytes or mesenchymal stem cells: Is that the question? Cell Stem Cell, 20, 296–297.
Cappellari, O., Benedetti, S., Innocenzi, A., Tedesco, F. S., Moreno-Fortuny, A., Ugarte, G., Lampugnani, M. G., Messina, G., & Cossu, G. (2013). Dll4 and PDGF-BB convert committed skeletal myoblasts to pericytes without erasing their myogenic memory. Developmental Cell, 24, 586–599.
Cappellari, O., & Cossu, G. (2013). Pericytes in development and pathology of skeletal muscle. Circulation Research, 113, 341–347.
Carss, K. J., Stevens, E., Foley, A. R., Cirak, S., Riemersma, M., Torelli, S., Hoischen, A., Willer, T., van Scherpenzeel, M., Moore, S. A., et al. (2013). Mutations in GDP-mannose pyrophosphorylase B cause congenital and limb-girdle muscular dystrophies associated with hypoglycosylation of alpha-dystroglycan. American Journal of Human Genetics, 93, 29–41.
Cassano, M., Dellavalle, A., Tedesco, F. S., Quattrocelli, M., Crippa, S., Ronzoni, F., Salvade, A., Berardi, E., Torrente, Y., Cossu, G., et al. (2011). Alpha sarcoglycan is required for FGF-dependent myogenic progenitor cell proliferation in vitro and in vivo. Development, 138, 4523–4533.
Cerletti, M., Jurga, S., Witczak, C. A., Hirshman, M. F., Shadrach, J. L., Goodyear, L. J., & Wagers, A. J. (2008). Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell, 134, 37–47.
Cheung, C., Bernardo, A. S., Trotter, M. W., Pedersen, R. A., & Sinha, S. (2012). Generation of human vascular smooth muscle subtypes provides insight into embryological origin-dependent disease susceptibility. Nature Biotechnology, 30, 165–173.
Chin, C. J., Li, S., Corselli, M., Casero, D., Zhu, Y., He, C. B., Hardy, R., Peault, B., & Crooks, G. M. (2018). Transcriptionally and functionally distinct mesenchymal subpopulations are generated from human pluripotent stem cells. Stem Cell Reports, 10, 436–446.
Christov, C., Chretien, F., Abou-Khalil, R., Bassez, G., Vallet, G., Authier, F. J., Bassaglia, Y., Shinin, V., Tajbakhsh, S., Chazaud, B., et al. (2007). Muscle satellite cells and endothelial cells: Close neighbors and privileged partners. Molecular Biology of the Cell, 18, 1397–1409.
Cochrane, A., Albers, H. J., Passier, R., Mummery, C. L., van den Berg, A., Orlova, V. V., & van der Meer, A. D. (2018). Advanced in vitro models of vascular biology: Human induced pluripotent stem cells and organ-on-chip technology. Advanced Drug Delivery Reviews.
Collett, G. D., & Canfield, A. E. (2005). Angiogenesis and pericytes in the initiation of ectopic calcification. Circulation Research, 96, 930–938.
Collins, C. A., Olsen, I., Zammit, P. S., Heslop, L., Petrie, A., Partridge, T. A., & Morgan, J. E. (2005). Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell, 122, 289–301.
Comai, G., & Tajbakhsh, S. (2014). Molecular and cellular regulation of skeletal myogenesis. Current Topics in Developmental Biology, 110, 1–73.
Cordova, G., Negroni, E., Cabello-Verrugio, C., Mouly, V., & Trollet, C. (2018). Combined therapies for Duchenne muscular dystrophy to optimize treatment efficacy. Frontiers in Genetics, 9, 114.
Cossu, G., Previtali, S. C., Napolitano, S., Cicalese, M. P., Tedesco, F. S., Nicastro, F., Noviello, M., Roostalu, U., Natali Sora, M. G., Scarlato, M., et al. (2015). Intra-arterial transplantation of HLA-matched donor mesoangioblasts in Duchenne muscular dystrophy. EMBO Molecular Medicine, 7, 1513–1528.
Crisan, M., Deasy, B., Gavina, M., Zheng, B., Huard, J., Lazzari, L., & Peault, B. (2008a). Purification and long-term culture of multipotent progenitor cells affiliated with the walls of human blood vessels: Myoendothelial cells and pericytes. Methods in Cell Biology, 86, 295–309.
Crisan, M., Yap, S., Casteilla, L., Chen, C. W., Corselli, M., Park, T. S., Andriolo, G., Sun, B., Zheng, B., Zhang, L., et al. (2008b). A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell, 3, 301–313.
Daneman, R., Zhou, L., Kebede, A. A., & Barres, B. A. (2010). Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature, 468, 562–566.
Dar, A., Domev, H., Ben-Yosef, O., Tzukerman, M., Zeevi-Levin, N., Novak, A., Germanguz, I., Amit, M., & Itskovitz-Eldor, J. (2012). Multipotent vasculogenic pericytes from human pluripotent stem cells promote recovery of murine ischemic limb. Circulation, 125, 87–99.
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, 246–259.
De Angelis, L., Berghella, L., Coletta, M., Lattanzi, L., Zanchi, M., Cusella-De Angelis, M. G., Ponzetto, C., & Cossu, G. (1999). Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration. The Journal of Cell Biology, 147, 869–878.
Dellavalle, A., Maroli, G., Covarello, D., Azzoni, E., Innocenzi, A., Perani, L., Antonini, S., Sambasivan, R., Brunelli, S., Tajbakhsh, S., et al. (2011). Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nature Communications, 2, 499.
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. Nature Cell Biology, 9, 255–267.
Dias Moura Prazeres, P. H., Sena, I. F. G., Borges, I. D. T., de Azevedo, P. O., Andreotti, J. P., de Paiva, A. E., de Almeida, V. M., de Paula Guerra, D. A., Pinheiro Dos Santos, G. S., Mintz, A., et al. (2017). Pericytes are heterogeneous in their origin within the same tissue. Developmental Biology, 427, 6–11.
Diaz-Manera, J., Gallardo, E., de Luna, N., Navas, M., Soria, L., Garibaldi, M., Rojas-Garcia, R., Tonlorenzi, R., Cossu, G., & Illa, I. (2012). The increase of pericyte population in human neuromuscular disorders supports their role in muscle regeneration in vivo. The Journal of Pathology, 228, 544–553.
Diaz-Manera, J., Touvier, T., Dellavalle, A., Tonlorenzi, R., Tedesco, F. S., Messina, G., Meregalli, M., Navarro, C., Perani, L., Bonfanti, C., et al. (2010). Partial dysferlin reconstitution by adult murine mesoangioblasts is sufficient for full functional recovery in a murine model of dysferlinopathy. Cell Death & Disease, 1, e61.
Dohgu, S., Takata, F., Yamauchi, A., Nakagawa, S., Egawa, T., Naito, M., Tsuruo, T., Sawada, Y., Niwa, M., & Kataoka, Y. (2005). Brain pericytes contribute to the induction and up-regulation of blood-brain barrier functions through transforming growth factor-beta production. Brain Research, 1038, 208–215.
Domi, T., Porrello, E., Velardo, D., Capotondo, A., Biffi, A., Tonlorenzi, R., Amadio, S., Ambrosi, A., Miyagoe-Suzuki, Y., Takeda, S., et al. (2015). Mesoangioblast delivery of miniagrin ameliorates murine model of merosin-deficient congenital muscular dystrophy type 1A. Skeletal Muscle, 5, 30.
Duffield, J. S., Lupher, M., Thannickal, V. J., & Wynn, T. A. (2013). Host responses in tissue repair and fibrosis. Annual Review of Pathology, 8, 241–276.
Dulauroy, S., Di Carlo, S. E., Langa, F., Eberl, G., & Peduto, L. (2012). Lineage tracing and genetic ablation of ADAM12(+) perivascular cells identify a major source of profibrotic cells during acute tissue injury. Nature Medicine, 18, 1262–1270.
Dumont, N. A., Bentzinger, C. F., Sincennes, M. C., & Rudnicki, M. A. (2015). Satellite cells and skeletal muscle regeneration. Comprehensive Physiology, 5, 1027–1059.
Eberth, C.J. (1871). Handbuch der Lehre von der Gewegen des Menschen und der Tiere. 1.
Emery, A. E. (2002). The muscular dystrophies. Lancet, 359, 687–695.
Enge, M., Bjarnegard, M., Gerhardt, H., Gustafsson, E., Kalen, M., Asker, N., Hammes, H. P., Shani, M., Fassler, R., & Betsholtz, C. (2002). Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. The EMBO Journal, 21, 4307–4316.
Engel, W. K. (1967). Muscle biopsies in neuromuscular diseases. Pediatric Clinics of North America, 14, 963–995.
Ervasti, J. M., & Campbell, K. P. (1991). Membrane organization of the dystrophin-glycoprotein complex. Cell, 66, 1121–1131.
Esner, M., Meilhac, S. M., Relaix, F., Nicolas, J. F., Cossu, G., & Buckingham, M. E. (2006). Smooth muscle of the dorsal aorta shares a common clonal origin with skeletal muscle of the myotome. Development, 133, 737–749.
Etchevers, H. C., Vincent, C., Le Douarin, N. M., & Couly, G. F. (2001). The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development, 128, 1059–1068.
Fabry, Z., Fitzsimmons, K. M., Herlein, J. A., Moninger, T. O., Dobbs, M. B., & Hart, M. N. (1993). Production of the cytokines interleukin 1 and 6 by murine brain microvessel endothelium and smooth muscle pericytes. Journal of Neuroimmunology, 47, 23–34.
Fan, Y., Maley, M., Beilharz, M., & Grounds, M. (1996). Rapid death of injected myoblasts in myoblast transfer therapy. Muscle & Nerve, 19, 853–860.
Farrington-Rock, C., Crofts, N. J., Doherty, M. J., Ashton, B. A., Griffin-Jones, C., & Canfield, A. E. (2004). Chondrogenic and adipogenic potential of microvascular pericytes. Circulation, 110, 2226–2232.
Frontera, W. R., & Ochala, J. (2015). Skeletal muscle: A brief review of structure and function. Calcified Tissue International, 96, 183–195.
Galvez, B. G., Sampaolesi, M., Brunelli, S., Covarello, D., Gavina, M., Rossi, B., Constantin, G., Torrente, Y., & Cossu, G. (2006). Complete repair of dystrophic skeletal muscle by mesoangioblasts with enhanced migration ability. The Journal of Cell Biology, 174, 231–243.
Gargioli, C., Coletta, M., De Grandis, F., Cannata, S. M., & Cossu, G. (2008). PlGF-MMP-9-expressing cells restore microcirculation and efficacy of cell therapy in aged dystrophic muscle. Nature Medicine, 14, 973–978.
Gaudio, E., Pannarale, L., & Marinozzi, G. (1985). An S.E.M. corrosion cast study on pericyte localization and role in microcirculation of skeletal muscle. Angiology, 36, 458–464.
Gautam, J., Nirwane, A., & Yao, Y. (2017). Laminin differentially regulates the stemness of type I and type II pericytes. Stem Cell Research & Therapy, 8, 28.
Gavina, M., Belicchi, M., Rossi, B., Ottoboni, L., Colombo, F., Meregalli, M., Battistelli, M., Forzenigo, L., Biondetti, P., Pisati, F., et al. (2006). VCAM-1 expression on dystrophic muscle vessels has a critical role in the recruitment of human blood-derived CD133+ stem cells after intra-arterial transplantation. Blood, 108, 2857–2866.
Geissinger, H. D., Rao, P. V., & McDonald-Taylor, C. K. (1990). “mdx” mouse myopathy: Histopathological, morphometric and histochemical observations on young mice. Journal of Comparative Pathology, 102, 249–263.
Gerli, M. F., Maffioletti, S. M., Millet, Q., & Tedesco, F. S. (2014). Transplantation of induced pluripotent stem cell-derived mesoangioblast-like myogenic progenitors in mouse models of muscle regeneration. Journal of Visualized Experiments, e50532.
Gerli, M. F. M., Moyle, L. A., Benedetti, S., Ferrari, G., Ucuncu, E., Ragazzi, M., Constantinou, C., Lousa, I., Sakai, H., Ala, P., De Coppi, P., Tajbakhsh, S., et al. (2019). Combined notch and PDGF signalling enhances expression of stem cell markers while inducing perivascular cell features in muscle satellite cells. Stem Cell Reports, 12(3), 461–473.
Giannotta, M., Benedetti, S., Tedesco, F. S., Corada, M., Trani, M., D’Antuono, R., Millet, Q., Orsenigo, F., Galvez, B. G., Cossu, G., et al. (2014). Targeting endothelial junctional adhesion molecule-A/EPAC/Rap-1 axis as a novel strategy to increase stem cell engraftment in dystrophic muscles. EMBO Molecular Medicine, 6, 239–258.
Gilbert, P. M., Havenstrite, K. L., Magnusson, K. E., Sacco, A., Leonardi, N. A., Kraft, P., Nguyen, N. K., Thrun, S., Lutolf, M. P., & Blau, H. M. (2010). Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science, 329, 1078–1081.
Giovannelli, G., Giacomazzi, G., Grosemans, H., & Sampaolesi, M. (2018). Morphological and functional analyses of skeletal muscles from an immunodeficient animal model of limb-girdle muscular dystrophy type 2E. Muscle & Nerve.
Guerette, B., Skuk, D., Celestin, F., Huard, C., Tardif, F., Asselin, I., Roy, B., Goulet, M., Roy, R., Entman, M., et al. (1997). Prevention by anti-LFA-1 of acute myoblast death following transplantation. Journal of Immunology, 159, 2522–2531.
Guimaraes-Camboa, N., Cattaneo, P., Sun, Y., Moore-Morris, T., Gu, Y., Dalton, N. D., Rockenstein, E., Masliah, E., Peterson, K. L., Stallcup, W. B., et al. (2017). Pericytes of multiple organs do not behave as mesenchymal stem cells in vivo. Cell Stem Cell, 20, 345–359 e345.
Hall, C. N., Reynell, C., Gesslein, B., Hamilton, N. B., Mishra, A., Sutherland, B. A., O’Farrell, F. M., Buchan, A. M., Lauritzen, M., & Attwell, D. (2014). Capillary pericytes regulate cerebral blood flow in health and disease. Nature, 508, 55–60.
Hara, Y., Balci-Hayta, B., Yoshida-Moriguchi, T., Kanagawa, M., Beltran-Valero de Bernabe, D., Gundesli, H., Willer, T., Satz, J. S., Crawford, R. W., Burden, S. J., et al. (2011). A dystroglycan mutation associated with limb-girdle muscular dystrophy. The New England Journal of Medicine, 364, 939–946.
Hegyi, L., Gannon, F. H., Glaser, D. L., Shore, E. M., Kaplan, F. S., & Shanahan, C. M. (2003). Stromal cells of fibrodysplasia ossificans progressiva lesions express smooth muscle lineage markers and the osteogenic transcription factor Runx2/Cbfa-1: Clues to a vascular origin of heterotopic ossification? The Journal of Pathology, 201, 141–148.
Hellstrom, M., Gerhardt, H., Kalen, M., Li, X., Eriksson, U., Wolburg, H., & Betsholtz, C. (2001). Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. The Journal of Cell Biology, 153, 543–553.
Hellstrom, M., Kalen, M., Lindahl, P., Abramsson, A., & Betsholtz, C. (1999). Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development, 126, 3047–3055.
Hirschi, K. K., & D’Amore, P. A. (1996). Pericytes in the microvasculature. Cardiovascular Research, 32, 687–698.
Holm, A., Heumann, T., & Augustin, H. G. (2018). Microvascular mural cell organotypic heterogeneity and functional plasticity. Trends in Cell Biology, 28, 302–316.
Huard, J., Roy, R., Bouchard, J. P., Malouin, F., Richards, C. L., & Tremblay, J. P. (1992). Human myoblast transplantation between immunohistocompatible donors and recipients produces immune reactions. Transplantation Proceedings, 24, 3049–3051.
Humphreys, B. D., Lin, S. L., Kobayashi, A., Hudson, T. E., Nowlin, B. T., Bonventre, J. V., Valerius, M. T., McMahon, A. P., & Duffield, J. S. (2010). Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. The American Journal of Pathology, 176, 85–97.
Iyer, P. S., Mavoungou, L. O., Ronzoni, F., Zemla, J., Schmid-Siegert, E., Antonini, S., Neff, L. A., Dorchies, O. M., Jaconi, M., Lekka, M., et al. (2018). Autologous cell therapy approach for duchenne muscular dystrophy using piggybac transposons and mesoangioblasts. Molecular Therapy, 26, 1093–1108.
James, A. W., Zara, J. N., Zhang, X., Askarinam, A., Goyal, R., Chiang, M., Yuan, W., Chang, L., Corselli, M., Shen, J., et al. (2012). Perivascular stem cells: A prospectively purified mesenchymal stem cell population for bone tissue engineering. Stem Cells Translational Medicine, 1, 510–519.
Janssen, I., Heymsfield, S. B., Wang, Z. M., & Ross, R. (2000). Skeletal muscle mass and distribution in 468 men and women aged 18–88 year. Journal of Applied Physiology (Bethesda, MD: 1985), 89, 81–88.
Joe, A. W., Yi, L., Natarajan, A., Le Grand, F., So, L., Wang, J., Rudnicki, M. A., & Rossi, F. M. (2010). Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nature Cell Biology, 12, 153–163.
Kobayashi, Y. M., Rader, E. P., Crawford, R. W., Iyengar, N. K., Thedens, D. R., Faulkner, J. A., Parikh, S. V., Weiss, R. M., Chamberlain, J. S., Moore, S. A., et al. (2008). Sarcolemma-localized nNOS is required to maintain activity after mild exercise. Nature, 456, 511–515.
Kostallari, E., Baba-Amer, Y., Alonso-Martin, S., Ngoh, P., Relaix, F., Lafuste, P., & Gherardi, R. K. (2015). Pericytes in the myovascular niche promote post-natal myofiber growth and satellite cell quiescence. Development, 142, 1242–1253.
Kragstrup, T. W., Kjaer, M., & Mackey, A. L. (2011). Structural, biochemical, cellular, and functional changes in skeletal muscle extracellular matrix with aging. Scandinavian Journal of Medicine & Science in Sports, 21, 749–757.
Kudryashova, E., Kramerova, I., & Spencer, M. J. (2012). Satellite cell senescence underlies myopathy in a mouse model of limb-girdle muscular dystrophy 2H. The Journal of Clinical Investigation, 122, 1764–1776.
Kumar, A., D’Souza, S. S., Moskvin, O. V., Toh, H., Wang, B., Zhang, J., Swanson, S., Guo, L. W., Thomson, J. A., & Slukvin, I. I. (2017). Specification and diversification of pericytes and smooth muscle cells from mesenchymoangioblasts. Cell Reports, 19, 1902–1916.
Kume, T. (2012). Ligand-dependent notch signaling in vascular formation. Advances in Experimental Medicine and Biology, 727, 210–222.
Lees-Shepard, J. B., Yamamoto, M., Biswas, A. A., Stoessel, S. J., Nicholas, S. E., Cogswell, C. A., Devarakonda, P. M., Schneider, M. J., Jr., Cummins, S. M., Legendre, N. P., et al. (2018). Activin-dependent signaling in fibro/adipogenic progenitors causes fibrodysplasia ossificans progressiva. Nature Communications, 9, 471.
Leveen, P., Pekny, M., Gebre-Medhin, S., Swolin, B., Larsson, E., & Betsholtz, C. (1994). Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes & Development, 8, 1875–1887.
Levy, M. M., Joyner, C. J., Virdi, A. S., Reed, A., Triffitt, J. T., Simpson, A. H., Kenwright, J., Stein, H., & Francis, M. J. (2001). Osteoprogenitor cells of mature human skeletal muscle tissue: an in vitro study. Bone, 29, 317–322.
Lin, A. Y., & Wang, L. H. (2018). Molecular therapies for muscular dystrophies. Current Treatment Options in Neurology, 20, 27.
Lin, S. L., Kisseleva, T., Brenner, D. A., & Duffield, J. S. (2008). Pericytes and perivascular fibroblasts are the primary source of collagen-producing cells in obstructive fibrosis of the kidney. The American Journal of Pathology, 173, 1617–1627.
Lindahl, P., Johansson, B. R., Leveen, P., & Betsholtz, C. (1997). Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science, 277, 242–245.
Loperfido, M., Steele-Stallard, H. B., Tedesco, F. S., & VandenDriessche, T. (2015). Pluripotent stem cells for gene therapy of degenerative muscle diseases. Current Gene Therapy, 15, 364–380.
Lukjanenko, L., Brachat, S., Pierrel, E., Lach-Trifilieff, E., & Feige, J. N. (2013). Genomic profiling reveals that transient adipogenic activation is a hallmark of mouse models of skeletal muscle regeneration. PLoS One, 8, e71084.
Maffioletti, S. M., Gerli, M. F., Ragazzi, M., Dastidar, S., Benedetti, S., Loperfido, M., VandenDriessche, T., Chuah, M. K., & Tedesco, F. S. (2015). Efficient derivation and inducible differentiation of expandable skeletal myogenic cells from human ES and patient-specific iPS cells. Nature Protocols, 10, 941–958.
Maffioletti, S. M., Noviello, M., English, K., & Tedesco, F. S. (2014). Stem cell transplantation for muscular dystrophy: The challenge of immune response. BioMed Research International, 2014, 964010.
Majesky, M. W. (2007). Developmental basis of vascular smooth muscle diversity. Arteriosclerosis, Thrombosis, and Vascular Biology, 27, 1248–1258.
Majesky, M. W., Dong, X. R., Regan, J. N., & Hoglund, V. J. (2011). Vascular smooth muscle progenitor cells: Building and repairing blood vessels. Circulation Research, 108, 365–377.
Mankodi, A., Bishop, C. A., Auh, S., Newbould, R. D., Fischbeck, K. H., & Janiczek, R. L. (2016). Quantifying disease activity in fatty-infiltrated skeletal muscle by IDEAL-CPMG in Duchenne muscular dystrophy. Neuromuscular Disorders, 26, 650–658.
Mann, C. J., Perdiguero, E., Kharraz, Y., Aguilar, S., Pessina, P., Serrano, A. L., & Munoz-Canoves, P. (2011). Aberrant repair and fibrosis development in skeletal muscle. Skeletal Muscle, 1, 21.
Manzur, A. Y., & Muntoni, F. (2009). Diagnosis and new treatments in muscular dystrophies. Postgraduate Medical Journal, 85, 622–630.
Matsumura, K., & Campbell, K. P. (1994). Dystrophin-glycoprotein complex: Its role in the molecular pathogenesis of muscular dystrophies. Muscle & Nerve, 17, 2–15.
Mauro, A. (1961). Satellite cell of skeletal muscle fibers. The Journal of Biophysical and Biochemical Cytology, 9, 493–495.
Meng, J., Adkin, C. F., Xu, S. W., Muntoni, F., & Morgan, J. E. (2011). Contribution of human muscle-derived cells to skeletal muscle regeneration in dystrophic host mice. PLoS One, 6, e17454.
Mercuri, E., & Muntoni, F. (2013). Muscular dystrophies. Lancet, 381, 845–860.
Michalak, M., & Opas, M. (1997). Functions of dystrophin and dystrophin associated proteins. Current Opinion in Neurology, 10, 436–442.
Minasi, M. G., Riminucci, M., De Angelis, L., Borello, U., Berarducci, B., Innocenzi, A., Caprioli, A., Sirabella, D., Baiocchi, M., De Maria, R., et al. (2002). The meso-angioblast: A multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development, 129, 2773–2783.
Mitsuhashi, S., & Kang, P. B. (2012). Update on the genetics of limb girdle muscular dystrophy. Seminars in Pediatric Neurology, 19, 211–218.
Montarras, D., Morgan, J., Collins, C., Relaix, F., Zaffran, S., Cumano, A., Partridge, T., & Buckingham, M. (2005). Direct isolation of satellite cells for skeletal muscle regeneration. Science, 309, 2064–2067.
Morales, M. G., Gutierrez, J., Cabello-Verrugio, C., Cabrera, D., Lipson, K. E., Goldschmeding, R., & Brandan, E. (2013). Reducing CTGF/CCN2 slows down mdx muscle dystrophy and improves cell therapy. Human Molecular Genetics, 22, 4938–4951.
Morosetti, R., Gidaro, T., Broccolini, A., Gliubizzi, C., Sancricca, C., Tonali, P. A., Ricci, E., & Mirabella, M. (2011). Mesoangioblasts from facioscapulohumeral muscular dystrophy display in vivo a variable myogenic ability predictable by their in vitro behavior. Cell Transplantation, 20, 1299–1313.
Murray, I. R., Baily, J. E., Chen, W. C. W., Dar, A., Gonzalez, Z. N., Jensen, A. R., Petrigliano, F. A., Deb, A., & Henderson, N. C. (2017). Skeletal and cardiac muscle pericytes: Functions and therapeutic potential. Pharmacology & Therapeutics, 171, 65–74.
Nakagawa, S., Deli, M. A., Nakao, S., Honda, M., Hayashi, K., Nakaoke, R., Kataoka, Y., & Niwa, M. (2007). Pericytes from brain microvessels strengthen the barrier integrity in primary cultures of rat brain endothelial cells. Cellular and Molecular Neurobiology, 27, 687–694.
Negroni, E., Bigot, A., Butler-Browne, G. S., Trollet, C., & Mouly, V. (2016). Cellular therapies for muscular dystrophies: Frustrations and clinical successes. Human Gene Therapy, 27, 117–126.
Nguyen, F., Cherel, Y., Guigand, L., Goubault-Leroux, I., & Wyers, M. (2002). Muscle lesions associated with dystrophin deficiency in neonatal golden retriever puppies. Journal of Comparative Pathology, 126, 100–108.
Norrmen, C., Tammela, T., Petrova, T. V., & Alitalo, K. (2011). Biological basis of therapeutic lymphangiogenesis. Circulation, 123, 1335–1351.
Noviello, M., Tedesco, F. S., Bondanza, A., Tonlorenzi, R., Rosaria Carbone, M., Gerli, M. F. M., Marktel, S., Napolitano, S., Cicalese, M. P., Ciceri, F., et al. (2014). Inflammation converts human mesoangioblasts into targets of alloreactive immune responses: Implications for allogeneic cell therapy of DMD. Molecular Therapy, 22, 1342–1352.
Orlova, V. V., van den Hil, F. E., Petrus-Reurer, S., Drabsch, Y., Ten Dijke, P., & Mummery, C. L. (2014). Generation, expansion and functional analysis of endothelial cells and pericytes derived from human pluripotent stem cells. Nature Protocols, 9, 1514–1531.
Pallone, T. L., & Silldorff, E. P. (2001). Pericyte regulation of renal medullary blood flow. Experimental Nephrology, 9, 165–170.
Pallone, T. L., Silldorff, E. P., & Turner, M. R. (1998). Intrarenal blood flow: Microvascular anatomy and the regulation of medullary perfusion. Clinical and Experimental Pharmacology & Physiology, 25, 383–392.
Palmieri, B., Tremblay, J. P., & Daniele, L. (2010). Past, present and future of myoblast transplantation in the treatment of Duchenne muscular dystrophy. Pediatric Transplantation, 14, 813–819.
Palumbo, R., Sampaolesi, M., De Marchis, F., Tonlorenzi, R., Colombetti, S., Mondino, A., Cossu, G., & Bianchi, M. E. (2004). Extracellular HMGB1, a signal of tissue damage, induces mesoangioblast migration and proliferation. The Journal of Cell Biology, 164, 441–449.
Partridge, T. (2000). The current status of myoblast transfer. Neurological Sciences, 21, S939–S942.
Partridge, T. A., Morgan, J. E., Coulton, G. R., Hoffman, E. P., & Kunkel, L. M. (1989). Conversion of mdx myofibres from dystrophin-negative to -positive by injection of normal myoblasts. Nature, 337, 176–179.
Peppiatt, C. M., Howarth, C., Mobbs, P., & Attwell, D. (2006). Bidirectional control of CNS capillary diameter by pericytes. Nature, 443, 700–704.
Pessina, P., Conti, V., Tonlorenzi, R., Touvier, T., Meneveri, R., Cossu, G., & Brunelli, S. (2012). Necdin enhances muscle reconstitution of dystrophic muscle by vessel-associated progenitors, by promoting cell survival and myogenic differentiation. Cell Death and Differentiation, 19, 827–838.
Pini, V., Morgan, J. E., Muntoni, F., & O’Neill, H. C. (2017). Genome editing and muscle stem cells as a therapeutic tool for muscular dystrophies. Current Stem Cell Reports, 3, 137–148.
Prazeres, P., Almeida, V. M., Lousado, L., Andreotti, J. P., Paiva, A. E., Santos, G. S. P., Azevedo, P. O., Souto, L., Almeida, G. G., Filev, R., et al. (2018). Macrophages generate pericytes in the developing brain. Cellular and Molecular Neurobiology, 38, 777–782.
Quan, T. E., Cowper, S. E., & Bucala, R. (2006). The role of circulating fibrocytes in fibrosis. Current Rheumatology Reports, 8, 145–150.
Quattrocelli, M., Costamagna, D., Giacomazzi, G., Camps, J., & Sampaolesi, M. (2014). Notch signaling regulates myogenic regenerative capacity of murine and human mesoangioblasts. Cell Death & Disease, 5, e1448.
Relaix, F., & Zammit, P. S. (2012). Satellite cells are essential for skeletal muscle regeneration: The cell on the edge returns centre stage. Development, 139, 2845–2856.
Rocheteau, P., Gayraud-Morel, B., Siegl-Cachedenier, I., Blasco, M. A., & Tajbakhsh, S. (2012). A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell, 148, 112–125.
Rodeheffer, M. S. (2010). Tipping the scale: Muscle versus fat. Nature Cell Biology, 12, 102–104.
Rouget, C. (1873). Mémoire sur le développement, la structure et les proprietés physiologiques des capillaires sanguins et lymphatiques. Archives Physical, 5, 603–610.
Ryall, J. G., Schertzer, J. D., & Lynch, G. S. (2008). Cellular and molecular mechanisms underlying age-related skeletal muscle wasting and weakness. Biogerontology, 9, 213–228.
Sacchetti, B., Funari, A., Remoli, C., Giannicola, G., Kogler, G., Liedtke, S., Cossu, G., Serafini, M., Sampaolesi, M., Tagliafico, E., et al. (2016). No identical “mesenchymal stem cells” at different times and sites: Human committed progenitors of distinct origin and differentiation potential are incorporated as adventitial cells in microvessels. Stem Cell Reports, 6, 897–913.
Sacco, A., Doyonnas, R., Kraft, P., Vitorovic, S., & Blau, H. M. (2008). Self-renewal and expansion of single transplanted muscle stem cells. Nature, 456, 502–506.
Sacco, A., Mourkioti, F., Tran, R., Choi, J., Llewellyn, M., Kraft, P., Shkreli, M., Delp, S., Pomerantz, J. H., Artandi, S. E., et al. (2010). Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell, 143, 1059–1071.
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.
Sampaolesi, M., Torrente, Y., Innocenzi, A., Tonlorenzi, R., D’Antona, G., Pellegrino, M. A., Barresi, R., Bresolin, N., De Angelis, M. G., Campbell, K. P., et al. (2003). Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science, 301, 487–492.
Sciorati, C., Galvez, B. G., Brunelli, S., Tagliafico, E., Ferrari, S., Cossu, G., & Clementi, E. (2006). Ex vivo treatment with nitric oxide increases mesoangioblast therapeutic efficacy in muscular dystrophy. Journal of Cell Science, 119, 5114–5123.
Scoto, M., Finkel, R., Mercuri, E., & Muntoni, F. (2018). Genetic therapies for inherited neuromuscular disorders. Lancet Child Adolescent Health, 2, 600–609.
Sims, D. E. (1986). The pericyte—a review. Tissue & Cell, 18, 153–174.
Skuk, D., Goulet, M., Roy, B., Chapdelaine, P., Bouchard, J. P., Roy, R., Dugre, F. J., Sylvain, M., Lachance, J. G., Deschenes, L., et al. (2006). Dystrophin expression in muscles of duchenne muscular dystrophy patients after high-density injections of normal myogenic cells. Journal of Neuropathology and Experimental Neurology, 65, 371–386.
Skuk, D., Goulet, M., Roy, B., Piette, V., Cote, C. H., Chapdelaine, P., Hogrel, J. Y., Paradis, M., Bouchard, J. P., Sylvain, M., et al. (2007). First test of a “high-density injection” protocol for myogenic cell transplantation throughout large volumes of muscles in a Duchenne muscular dystrophy patient: Eighteen months follow-up. Neuromuscular Disorders, 17, 38–46.
Skuk, D., Roy, B., Goulet, M., Chapdelaine, P., Bouchard, J. P., Roy, R., Dugre, F. J., Lachance, J. G., Deschenes, L., Helene, S., et al. (2004). Dystrophin expression in myofibers of Duchenne muscular dystrophy patients following intramuscular injections of normal myogenic cells. Molecular Therapy, 9, 475–482.
Skuk, D., & Tremblay, J. P. (2011). Intramuscular cell transplantation as a potential treatment of myopathies: Clinical and preclinical relevant data. Expert Opinion on Biological Therapy, 11, 359–374.
Smythe, G. M., Fan, Y., & Grounds, M. D. (2000). Enhanced migration and fusion of donor myoblasts in dystrophic and normal host muscle. Muscle & Nerve, 23, 560–574.
Soriano, P. (1994). Abnormal kidney development and hematological disorders in PDGF beta-receptor mutant mice. Genes & Development, 8, 1888–1896.
Straub, V., Bittner, R. E., Leger, J. J., & Voit, T. (1992). Direct visualization of the dystrophin network on skeletal muscle fiber membrane. The Journal of Cell Biology, 119, 1183–1191.
Straub, V., & Campbell, K. P. (1997). Muscular dystrophies and the dystrophin-glycoprotein complex. Current Opinion in Neurology, 10, 168–175.
Tagliafico, E., Brunelli, S., Bergamaschi, A., De Angelis, L., Scardigli, R., Galli, D., Battini, R., Bianco, P., Ferrari, S., Cossu, G., et al. (2004). TGFbeta/BMP activate the smooth muscle/bone differentiation programs in mesoangioblasts. Journal of Cell Science, 117, 4377–4388.
Tanaka, K. K., Hall, J. K., Troy, A. A., Cornelison, D. D., Majka, S. M., & 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.
Tedesco, F. S., Dellavalle, A., Diaz-Manera, J., Messina, G., & Cossu, G. (2010). Repairing skeletal muscle: Regenerative potential of skeletal muscle stem cells. The Journal of Clinical Investigation, 120, 11–19.
Tedesco, F. S., Gerli, M. F., Perani, L., Benedetti, S., Ungaro, F., Cassano, M., Antonini, S., Tagliafico, E., Artusi, V., Longa, E., et al. (2012). Transplantation of genetically corrected human iPSC-derived progenitors in mice with limb-girdle muscular dystrophy. Science Translational Medicine, 4, 140ra189.
Tedesco, F. S., Hoshiya, H., D’Antona, G., Gerli, M. F., Messina, G., Antonini, S., Tonlorenzi, R., Benedetti, S., Berghella, L., Torrente, Y., et al. (2011). Stem cell-mediated transfer of a human artificial chromosome ameliorates muscular dystrophy. Science Translational Medicine, 3, 96ra78.
Tedesco, F. S., Moyle, L. A., & Perdiguero, E. (2017). Muscle interstitial cells: A brief field guide to non-satellite cell populations in skeletal muscle. Methods in Molecular Biology, 1556, 129–147.
Tews, D. S., & Goebel, H. H. (1995). Expression of cell adhesion molecules in inflammatory myopathies. Journal of Neuroimmunology, 59, 185–194.
Thomas, G. D. (2013). Functional muscle ischemia in Duchenne and Becker muscular dystrophy. Frontiers in Physiology, 4, 381.
Thompson, L. V. (2009). Age-related muscle dysfunction. Experimental Gerontology, 44, 106–111.
Tu, Z., Li, Y., Smith, D. S., Sheibani, N., Huang, S., Kern, T., & Lin, F. (2011). Retinal pericytes inhibit activated T cell proliferation. Investigative Ophthalmology & Visual Science, 52, 9005–9010.
Uezumi, A., Fukada, S., Yamamoto, N., Takeda, S., & Tsuchida, K. (2010). Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nature Cell Biology, 12, 143–152.
Ugarte, G., Cappellari, O., Perani, L., Pistocchi, A., & Cossu, G. (2012). Noggin recruits mesoderm progenitors from the dorsal aorta to a skeletal myogenic fate. Developmental Biology, 365, 91–100.
Valadares, M. C., Gomes, J. P., Castello, G., Assoni, A., Pellati, M., Bueno, C., Corselli, M., Silva, H., Bartolini, P., Vainzof, M., et al. (2014). Human adipose tissue derived pericytes increase life span in Utrn (tm1Ked) Dmd (mdx)/J mice. Stem Cell Reviews, 10, 830–840.
Valero, M. C., Huntsman, H. D., Liu, J., Zou, K., & Boppart, M. D. (2012). Eccentric exercise facilitates mesenchymal stem cell appearance in skeletal muscle. PLoS One, 7, e29760.
Verbeek, M. M., Westphal, J. R., Ruiter, D. J., & de Waal, R. M. (1995). T lymphocyte adhesion to human brain pericytes is mediated via very late antigen-4/vascular cell adhesion molecule-1 interactions. Journal of Immunology, 154, 5876–5884.
Verdijk, L. B., Snijders, T., Drost, M., Delhaas, T., Kadi, F., & van Loon, L. J. (2014). Satellite cells in human skeletal muscle; from birth to old age. Age (Dordrecht, Netherlands), 36, 545–547.
Walston, J. D. (2012). Sarcopenia in older adults. Current Opinion in Rheumatology, 24, 623–627.
Willis, B. C., duBois, R. M., & Borok, Z. (2006). Epithelial origin of myofibroblasts during fibrosis in the lung. Proceedings of the American Thoracic Society, 3, 377–382.
Worton, R. (1995). Muscular dystrophies: Diseases of the dystrophin-glycoprotein complex. Science, 270, 755–756.
Wren, T. A., Bluml, S., Tseng-Ong, L., & Gilsanz, V. (2008). Three-point technique of fat quantification of muscle tissue as a marker of disease progression in Duchenne muscular dystrophy: Preliminary study. AJR. American Journal of Roentgenology, 190, W8–W12.
Wynn, T. A. (2008). Cellular and molecular mechanisms of fibrosis. The Journal of Pathology, 214, 199–210.
Yablonka-Reuveni, Z. (2011). The skeletal muscle satellite cell: Still young and fascinating at 50. The Journal of Histochemistry and Cytochemistry, 59, 1041–1059.
Yamazaki, T., Nalbandian, A., Uchida, Y., Li, W., Arnold, T. D., Kubota, Y., Yamamoto, S., Ema, M., & Mukouyama, Y. S. (2017). Tissue myeloid progenitors differentiate into pericytes through TGF-beta signaling in developing skin vasculature. Cell Reports, 18, 2991–3004.
Yao, Y., Norris, E. H., Mason, C. E., & Strickland, S. (2016). Laminin regulates PDGFRbeta(+) cell stemness and muscle development. Nature Communications, 7, 11415.
Yin, H., Price, F., & Rudnicki, M. A. (2013). Satellite cells and the muscle stem cell niche. Physiological Reviews, 93, 23–67.
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, 347–357.
Zammit, P. S., Partridge, T. A., & Yablonka-Reuveni, Z. (2006). The skeletal muscle satellite cell: The stem cell that came in from the cold. The Journal of Histochemistry and Cytochemistry, 54, 1177–1191.
Zeisberg, E. M., Tarnavski, O., Zeisberg, M., Dorfman, A. L., McMullen, J. R., Gustafsson, E., Chandraker, A., Yuan, X., Pu, W. T., Roberts, A. B., et al. (2007). Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nature Medicine, 13, 952–961.
Zhang, X., Peault, B., Chen, W., Li, W., Corselli, M., James, A. W., Lee, M., Siu, R. K., Shen, P., Zheng, Z., et al. (2011). The Nell-1 growth factor stimulates bone formation by purified human perivascular cells. Tissue Engineering. Part A, 17, 2497–2509.
Zimmermann, K. W. (1923). Der feinere Bau der Blutkapillaren. Zeitschrift für Anatomie und Entwicklungsgeschichte, 68, 29–109.
Acknowledgements
We thank Giulio Cossu for the critical reading of this manuscript. This research was supported by the National Institute for Health Research (NIHR) Great Ormond Street Hospital Biomedical Research Centre. F.S.T. is also funded by NIHR (Clinical Lectureship in Paediatrics). The views expressed are those of the authors and not necessarily those of the National Health Service (NHS), the NIHR or the Department of Health. Work in the Benedetti laboratory is supported by Great Ormond Street Children’s Charity, Sparks and Krabbe UK. Work in the Tedesco laboratory is funded by the European Research Council (7591108—HISTOID), Muscular Dystrophy UK, the UK MRC and BBSRC and the AFM-Telethon. F.S.T. is also grateful to previous funding from the European Union’s 7th Framework Programme for research, technological development and demonstration under grant agreement no. 602423 (PluriMes), Fundació La Marató de TV3, IMI joint undertaking n° 115582 EBiSC (EU FP7 and EFPIA companies), Duchenne Parent Project Onlus, Takeda New Frontier Science and the NIHR (Academic Clinical Fellowship in Paediatrics). L.A.M. is supported by the Human Frontiers Science Program.
Author information
Authors and Affiliations
Corresponding authors
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Moyle, L.A., Tedesco, F.S., Benedetti, S. (2019). Pericytes in Muscular Dystrophies. In: Birbrair, A. (eds) Pericyte Biology in Disease. Advances in Experimental Medicine and Biology, vol 1147. Springer, Cham. https://doi.org/10.1007/978-3-030-16908-4_15
Download citation
DOI: https://doi.org/10.1007/978-3-030-16908-4_15
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-16907-7
Online ISBN: 978-3-030-16908-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)