Overexpression of miR-29 Leads to Myopathy that Resemble Pathology of Ullrich Congenital Muscular Dystrophy
Abstract
:1. Introduction
2. Materials and Methods
2.1. Ethics Statement
2.2. Mice
2.3. Micro-Computed Tomography Experiment
2.4. Exercise
2.5. Histology, Immunochemistry, and Immunofluorescence
2.6. Cell Culture
2.7. Luciferase Reporter Assay
2.8. Q-PCR
2.9. Western Blotting
2.10. Statistical Analysis
3. Results
3.1. Overexpression of the miR-29ab1 Cluster Leads to Skeletal Muscle Dysplasia
3.2. Overexpression of the miR-29ab1 Cluster in Juvenile Mice Induces Skeletal Muscle Injury
3.3. Col4a1 and Col4a2 Are the Direct Target Genes of miR-29
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Lampe, A.K.; Bushby, K.M.D. Collagen VI related muscle disorders. J. Med. Genet. 2005, 42, 673–685. [Google Scholar] [CrossRef] [PubMed]
- Briñas, L.; Richard, P.; Quijano-Roy, S.; Gartioux, C.; Ledeuil, C.; Lacène, E.; Makri, S.; Ferreiro, A.; Maugenre, S.; Topaloglu, H.; et al. Early onset collagen VI myopathies: Genetic and clinical correlations. Ann. Neurol. 2010, 68, 511–520. [Google Scholar] [PubMed]
- Bushby, K.M.D.; Gardner-Medwin, D. The clinical, genetic and dystrophin characteristics of Becker muscular dystrophy. J. Neurol. 1993, 240, 98–104. [Google Scholar] [CrossRef] [PubMed]
- Nadeau, A.; Kinali, M.; Main, M.; Jimenez-Mallebrera, C.; Aloysius, A.; Clément, E.; North, B.; Manzur, A.Y.; Robb, S.A.; Mercuri, E.; et al. Natural history of Ullrich congenital muscular dystrophy. Neurology 2009, 73, 25–31. [Google Scholar] [PubMed]
- Schessl, J.; Goemans, N.M.; Magold, A.I.; Zou, Y.; Hu, Y.; Kirschner, J.; Sciot, R.; Bönnemann, C.G. Predominant fiber atrophy and fiber type disproportion in early ullrich disease. Muslce Nerve 2008, 38, 1184–1191. [Google Scholar] [CrossRef] [PubMed]
- Lamandé, S.R.; Bateman, J.F. Collagen VI disorders: Insights on form and function in the extracellular matrix and beyond. Matrix Biol. 2018, 71–72, 348–367. [Google Scholar] [CrossRef]
- Yonekawa, T.; Nishino, I. Ullrich congenital muscular dystrophy: Clinicopathological features, natural history and pathomechanism(s). J. Neurol. Neurosurg. Psychiatr. 2015, 86, 280–287. [Google Scholar] [CrossRef]
- Bonaldo, P.; Braghetta, P.; Zanetti, M.; Piccolo, S.; Volpin, D.; Bressan, G.M. Collagen VI deficiency induces early onset myopathy in the mouse: An animal model for Bethlem myopathy. Hum. Mol. Genet. 1998, 7, 2135–2140. [Google Scholar] [CrossRef]
- Meehan, T.F.; The International Mouse Phenotyping Consortium; Conte, N.; West, D.B.; O Jacobsen, J.; Mason, J.; Warren, J.; Chen, C.-K.; Tudose, I.; Relac, M.; et al. Disease model discovery from 3,328 gene knockouts by The International Mouse Phenotyping Consortium. Nat. Genet. 2017, 49, 1231–1238. [Google Scholar] [CrossRef] [PubMed]
- Cescon, M.; Gattazzo, F.; Chen, P.; Bonaldo, P. Collagen VI at a glance. J. Cell Sci. 2015, 128, 3525–3531. [Google Scholar] [CrossRef]
- Pan, T.-C.; Zhang, R.-Z.; Markova, D.; Arita, M.; Zhang, Y.; Bogdanovich, S.; Khurana, T.S.; Bönnemann, C.G.; Birk, D.E.; Chu, M.-L. COL6A3 Protein Deficiency in Mice Leads to Muscle and Tendon Defects Similar to Human Collagen VI Congenital Muscular Dystrophy. J. Biol. Chem. 2013, 288, 14320–14331. [Google Scholar] [CrossRef]
- Pan, T.-C.; Zhang, R.-Z.; Arita, M.; Bogdanovich, S.; Adams, S.M.; Gara, S.K.; Wagener, R.; Khurana, T.S.; Birk, D.E.; Chu, M.-L. A mouse model for dominant collagen VI disorders: Heterozygous deletion of Col6a3 Exon 16. J. Biol. Chem. 2014, 289, 10293–10307. [Google Scholar] [CrossRef] [PubMed]
- Kriegel, A.J.; Liu, Y.; Fang, Y.; Ding, X.; Liang, M. The miR-29 family: Genomics, cell biology, and relevance to renal and cardiovascular injury. Physiol. Genom. 2012, 44, 237–244. [Google Scholar] [CrossRef]
- Wang, Y.; Zhang, X.; Li, H.; Yu, J.; Ren, X. The role of miRNA-29 family in cancer. Eur. J. Cell Biol. 2013, 92, 123–128. [Google Scholar] [CrossRef]
- Liu, C.; Wang, M.; Chen, M.; Zhang, K.; Gu, L.; Li, Q.; Yu, Z.; Li, N.; Meng, Q. miR-18a induces myotubes atrophy by down-regulating IgfI. Int. J. Biochem. Cell Biol. 2017, 90, 145–154. [Google Scholar] [CrossRef]
- Hamer, P.W.; McGeachie, J.M.; Davies, M.J.; Grounds, M.D. Evans Blue Dye as an in vivo marker of myofibre damage: Optimising parameters for detecting initial myofibre membrane permeability. J. Anat. 2002, 200, 69–79. [Google Scholar] [CrossRef]
- Zhang, Y.; Li, X.; Grailer, J.J.; Wang, N.; Wang, M.; Yao, J.; Zhong, R.; Gao, G.F.; Ward, P.A.; Tan, D.-X.; et al. Melatonin alleviates acute lung injury through inhibiting the NLRP3 inflammasome. J. Pineal Res. 2016, 60, 405–414. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Li, Y.; Zhang, D.; Liu, J.; Gou, K.; Cui, S. Mitogen-Activated Protein Kinase 8 (MAP3K8) Mediates the Signaling Pathway of Estradiol Stimulating Progesterone Production Through G Protein-Coupled Receptor 30 (GPR30) in Mouse Corpus Luteum. Mol. Endocrinol. 2015, 29, 703–715. [Google Scholar] [CrossRef] [PubMed]
- Wei, W.; He, H.-B.; Zhang, W.-Y.; Zhang, H.-X.; Bai, J.-B.; Liu, H.-Z.; Cao, J.-H.; Chang, K.-C.; Li, X.-Y.; Zhao, S.-H. miR-29 targets Akt3 to reduce proliferation and facilitate differentiation of myoblasts in skeletal muscle development. Cell Death 2013, 4, e668. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Garzon, R.; Sun, H.; Ladner, K. J.; Singh, R.; Dahlman, J.; Cheng, A.; Hall, B.M.; Qualman, S.J.; Chandler, D.S.; et al. NF-kappaB-YY1-miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma. Cancer Cell 2008, 14, 369–381. [Google Scholar] [CrossRef]
- Mayer, U.; Saher, G.; Fassler, R.; Bornemann, A.; Echtermeyer, F.; von der Mark, H.; Miosge, N.; Poschl, E.; von der Mark, K. Absence of integrin alpha 7 causes a novel form of muscular dystrophy. Nat. Genet. 1997, 17, 318–323. [Google Scholar] [CrossRef]
- Gabellini, D.; D’Antona, G.; Moggio, M.; Prelle, A.; Zecca, C.; Adami, R.; Angeletti, B.; Ciscato, P.; Pellegrino, M.A.; Bottinelli, R.; et al. Facioscapulohumeral muscular dystrophy in mice overexpressing FRG1. Nature 2006, 439, 973–977. [Google Scholar] [CrossRef] [PubMed]
- Bönnemann, C.G. The collagen VI-related myopathies: Muscle meets its matrix. Nat. Rev. Neurol. 2011, 7, 379–390. [Google Scholar] [CrossRef] [PubMed]
- Wooddell, C.I.; Zhang, G.; Griffin, J.B.; Hegge, J.O.; Huss, T.; Wolff, J.A. Use of Evans blue dye to compare limb muscles in exercised young and old mdx mice. Muscle Nerve 2010, 41, 487–499. [Google Scholar] [CrossRef] [PubMed]
- Thomas, M.M.; Wang, D.C.; D’Souza, D.M.; Krause, M.P.; Layne, A.S.; Criswell, D.S.; O’Neill, H.M.; Connor, M.K.; Anderson, J.E.; Kemp, B.E.; et al. Muscle-specific AMPK beta1beta2-null mice display a myopathy due to loss of capillary density in nonpostural muscles. FASEB J. 2014, 28, 2098–2107. [Google Scholar] [CrossRef]
- Relaix, F.; Zammit, P.S. Satellite cells are essential for skeletal muscle regeneration: The cell on the edge returns centre stage. Development 2012, 139, 2845–2856. [Google Scholar] [CrossRef]
- Rigamonti, E.; Zordan, P.; Sciorati, C.; Rovere-Querini, P.; Brunelli, S. Macrophage Plasticity in Skeletal Muscle Repair. BioMed Int. 2014, 2014, 1–9. [Google Scholar] [CrossRef]
- Lund, D.K.; Cornelison, D.D.W. Enter the Matrix: Shape, Signal, and Superhighway. FEBS J. 2013, 280, 4089–4099. [Google Scholar] [CrossRef]
- Sabatelli, P.; Bonaldo, P.; Lattanzi, G.; Braghetta, P.; Bergamin, N.; Capanni, C.; Mattioli, E.; Columbaro, M.; Ognibene, A.; Pepe, G.; et al. Collagen VI deficiency affects the organization of fibronectin in the extracellular matrix of cultured fibroblasts. Matrix Biol. 2001, 20, 475–486. [Google Scholar] [CrossRef]
- Kuo, H.-J.; Maslen, C.L.; Keene, D.R.; Glanville, R.W. Type VI Collagen Anchors Endothelial Basement Membranes by Interacting with Type IV Collagen. J. Biol. Chem. 1997, 272, 26522–26529. [Google Scholar] [CrossRef] [PubMed]
- Gould, D.B.; Phalan, F.C.; Breedveld, G.J.; Van Mil, S.E.; Smith, R.S.; Schimenti, J.C.; Aguglia, U.; Van Der Knaap, M.S.; Heutink, P.; John, S.W.M. Mutations in Col4a1 Cause Perinatal Cerebral Hemorrhage and Porencephaly. Science 2005, 308, 1167–1171. [Google Scholar] [CrossRef] [PubMed]
- Plaisier, E.; Gribouval, O.; Alamowitch, S.; Mougenot, B.; Prost, C.; Verpont, M.C.; Marro, B.; Desmettre, T.; Cohen, S.Y.; Roullet, E.; et al. COL4A1Mutations and Hereditary Angiopathy, Nephropathy, Aneurysms, and Muscle Cramps. N. Engl. J. Med. 2007, 357, 2687–2695. [Google Scholar] [CrossRef] [PubMed]
- Labelle-Dumais, C.; Dilworth, D.J.; Harrington, E.P.; De Leau, M.; Lyons, D.; Kabaeva, Z.; Manzini, M.C.; Dobyns, W.B.; Walsh, C.A.; Michele, D.E.; et al. COL4A1 Mutations Cause Ocular Dysgenesis, Neuronal Localization Defects, and Myopathy in Mice and Walker-Warburg Syndrome in Humans. PLoS Genet. 2011, 7, 1002062. [Google Scholar] [CrossRef] [PubMed]
- Steffen, F.; Bilzer, T.; Brands, J.; Golini, L.; Jagannathan, V.; Wiedmer, M.; Drögemüller, M.; Drögemüller, C.; Leeb, T. A Nonsense Variant in COL6A1 in Landseer Dogs with Muscular Dystrophy. G3 Genes Genomes Genet. 2015, 5, 2611–2617. [Google Scholar] [CrossRef] [PubMed]
- Marioni-Henry, K.; Haworth, P.; Scott, H.; Witte, P.; Guo, L.T.; Shelton, G.D. Sarcolemmal specific collagen VI deficient myopathy in a Labrador Retriever. J. Vet. Intern. Med. 2014, 28, 243–249. [Google Scholar] [CrossRef]
- Telfer, W.R.; Busta, A.S.; Bönnemann, C.G.; Feldman, E.L.; Dowling, J.J. Zebrafish models of collagen VI-related myopathies. Hum. Mol. Genet. 2010, 19, 2433–2444. [Google Scholar] [CrossRef] [PubMed]
- Irwin, W.A.; Bergamin, N.; Sabatelli, P.; Reggiani, C.; Megighian, A.; Merlini, L.; Braghetta, P.; Columbaro, M.; Volpin, D.; Bressan, G.M.; et al. Mitochondrial dysfunction and apoptosis in myopathic mice with collagen VI deficiency. Nat. Genet. 2003, 35, 367–371. [Google Scholar] [CrossRef] [PubMed]
- Gattazzo, F.; Molon, S.; Morbidoni, V.; Braghetta, P.; Blaauw, B.; Urciuolo, A.; Bonaldo, P. Cyclosporin A Promotes in vivo Myogenic Response in Collagen VI-Deficient Myopathic Mice. Front. Aging Neurosci. 2014, 6, 244. [Google Scholar] [CrossRef] [PubMed]
- Palma, E.; Tiepolo, T.; Angelin, A.; Sabatelli, P.; Maraldi, N.M.; Basso, E.; Forte, M.A.; Bernardi, P.; Bonaldo, P. Genetic ablation of cyclophilin D rescues mitochondrial defects and prevents muscle apoptosis in collagen VI myopathic mice. Hum. Mol. Genet. 2009, 18, 2024–2031. [Google Scholar] [CrossRef] [PubMed]
- Menazza, S.; Blaauw, B.; Tiepolo, T.; Toniolo, L.; Braghetta, P.; Spolaore, B.; Reggiani, C.; Di Lisa, F.; Bonaldo, P.; Canton, M. Oxidative stress by monoamine oxidases is causally involved in myofiber damage in muscular dystrophy. Hum. Mol. Genet. 2010, 19, 4207–4215. [Google Scholar] [CrossRef] [PubMed]
- Grumati, P.; Coletto, L.; Sabatelli, P.; Cescon, M.; Angelin, A.; Bertaggia, E.; Blaauw, B.; Urciuolo, A.; Tiepolo, T.; Merlini, L.; et al. Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat. Med. 2010, 16, 1313–1320. [Google Scholar] [CrossRef] [PubMed]
- Chrisam, M.; Pirozzi, M.; Castagnaro, S.; Blaauw, B.; Polishchuck, R.; Cecconi, F.; Grumati, P.; Bonaldo, P. Reactivation of autophagy by spermidine ameliorates the myopathic defects of collagen VI-null mice. Autophagy 2015, 11, 2142–2152. [Google Scholar] [CrossRef] [PubMed]
- Urciuolo, A.; Quarta, M.; Morbidoni, V.; Gattazzo, F.; Molon, S.; Grumati, P.; Montemurro, F.; Tedesco, F.S.; Blaauw, B.; Cossu, G.; et al. Collagen VI regulates satellite cell self-renewal and muscle regeneration. Nat. Commun. 2013, 4, 1964. [Google Scholar] [CrossRef] [PubMed]
- Wiberg, C.; Klatt, A.R.; Mörgelin, M.; Wagener, R.; Paulsson, M.; Bateman, J.F.; Heinegãrd, D. Complexes of Matrilin-1 and Biglycan or Decorin Connect Collagen VI Microfibrils to Both Collagen II and Aggrecan. J. Boil. Chem. 2003, 278, 37698–37704. [Google Scholar] [CrossRef] [PubMed]
- Purslow, P.P. The structure and functional significance of variations in the connective tissue within muscle. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2002, 133, 947–966. [Google Scholar] [CrossRef]
- Gao, Y.; Kostrominova, T.Y.; Faulkner, J.A.; Wineman, A.S. Age-related changes in the mechanical properties of the epimysium in skeletal muscles of rats. J. Biomech. 2008, 41, 465–469. [Google Scholar] [CrossRef] [PubMed]
- Gao, Y.; Waas, A.M.; Faulkner, J.A.; Kostrominova, T.Y.; Wineman, A.S. Micromechanical modeling of the epimysium of the skeletal muscles. J. Biomech. 2008, 41, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Ghazwani, M.; Li, J.; Sun, M.; Stolz, D.B.; He, F.; Fan, J.; Xie, W.; Li, S. MiR-29b inhibits collagen maturation in hepatic stellate cells through down-regulating the expression of HSP47 and lysyl oxidase. Biochem. Biophys. Res. Commun. 2014, 446, 940–944. [Google Scholar] [CrossRef] [PubMed]
- Roderburg, C.; Luedde, T. Circulating microRNAs as markers of liver inflammation, fibrosis and cancer. J. Hepatol. 2014, 61, 1434–1437. [Google Scholar] [CrossRef]
- Roderburg, C.; Urban, G.W.; Bettermann, K.; Vucur, M.; Zimmermann, H.; Schmidt, S.; Janssen, J.; Koppe, C.; Knolle, P.; Castoldi, M.; et al. Micro-RNA profiling reveals a role for miR-29 in human and murine liver fibrosis. Hepatology 2011, 53, 209–218. [Google Scholar] [CrossRef]
- Cushing, L.; Kuang, P.P.; Qian, J.; Shao, F.; Wu, J.; Little, F.; Thannickal, V.J.; Cardoso, W.V.; Lu, J. miR-29 is a major regulator of genes associated with pulmonary fibrosis. Am. J. Respir. Cell Mol. Biol. 2011, 45, 287–294. [Google Scholar] [CrossRef] [PubMed]
- Cushing, L.; Kuang, P.; Lü, J. The role of miR-29 in pulmonary fibrosis. Biochem. Cell Boil. 2015, 93, 109–118. [Google Scholar] [CrossRef]
- Yang, T.; Liang, Y.; Lin, Q.; Liu, J.; Luo, F.; Li, X.; Zhou, H.; Zhuang, S.; Zhang, H. miR-29 mediates TGFbeta1-induced extracellular matrix synthesis through activation of PI3K-AKT pathway in human lung fibroblasts. J. Cell Biochem. 2013, 114, 1336–1342. [Google Scholar] [CrossRef] [PubMed]
- Maegdefessel, L.; Azuma, J.; Tsao, P.S. MicroRNA-29b regulation of abdominal aortic aneurysm development. Trends Cardiovasc. Med. 2014, 24, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Van Rooij, E.; Sutherland, L.B.; Thatcher, J.E.; DiMaio, J.M.; Naseem, R.H.; Marshall, W.S.; Hill, J.A.; Olson, E.N. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc. Natl. Acad. Sci. USA 2008, 105, 13027–13032. [Google Scholar] [CrossRef] [PubMed]
- Wang, G.; Kwan, B.C.-H.; Lai, F.M.-M.; Chow, K.-M.; Li, P.K.-T.; Szeto, C.-C. Urinary miR-21, miR-29, and miR-93: Novel Biomarkers of Fibrosis. Am. J. Nephrol. 2012, 36, 412–418. [Google Scholar] [CrossRef]
- Maurer, B.; Stanczyk, J.; Jüngel, A.; Akhmetshina, A.; Trenkmann, M.; Brock, M.; Kowal-Bielecka, O.; Gay, R.E.; Michel, B.A.; Distler, J.H.W.; et al. MicroRNA-29, a key regulator of collagen expression in systemic sclerosis. Arthritis Rheum. 2010, 62, 1733–1743. [Google Scholar] [CrossRef]
- O’Reilly, S. miRNA-29a in systemic sclerosis: A valid target. Autoimmunity 2015, 48, 511–512. [Google Scholar] [CrossRef] [PubMed]
- Villarreal, G.; Oh, D.-J.; Kang, M.H.; Rhee, D.J. Coordinated Regulation of Extracellular Matrix Synthesis by the MicroRNA-29 Family in the Trabecular Meshwork. Investig. Opthalmol. Sci. 2011, 52, 3391–3397. [Google Scholar] [CrossRef]
- Kapinas, K.; Kessler, C.; Ricks, T.; Gronowicz, G.; Delany, A.M. miR-29 Modulates Wnt Signaling in Human Osteoblasts through a Positive Feedback Loop. J. Biol. Chem. 2010, 285, 25221–25231. [Google Scholar] [CrossRef]
- Kapinas, K.; Kessler, C.B.; Delany, A.M. miR-29 Suppression of Osteonectin in Osteoblasts: Regulation During Differentiation and by Canonical Wnt Signaling. J. Cell. Biochem. 2009, 108, 216–224. [Google Scholar] [CrossRef] [PubMed]
- Zanotti, S.; Gibertini, S.; Curcio, M.; Savadori, P.; Pasanisi, B.; Morandi, L.; Cornelio, F.; Mantegazza, R.; Mora, M. Opposing roles of miR-21 and miR-29 in the progression of fibrosis in Duchenne muscular dystrophy. Biochim. Biophys. Acta 2015, 1852, 1451–1464. [Google Scholar] [CrossRef] [PubMed]
- Wein, N.; Alfano, L.; Flanigan, K.M. Genetics and Emerging Treatments for Duchenne and Becker Muscular Dystrophy. Pediatr. Clin. N. Am. 2015, 62, 723–742. [Google Scholar] [CrossRef] [PubMed]
- Durbeej, M. Laminin-alpha2 Chain-Deficient Congenital Muscular Dystrophy: Pathophysiology and Development of Treatment. Curr. Top. Membr. 2015, 76, 31–60. [Google Scholar]
- Holmberg, J.; Durbeej, M. Laminin-211 in skeletal muscle function. Cell Adh. Migr. 2013, 7, 111–121. [Google Scholar] [CrossRef]
- Van Agtmael, T.; Schlötzer-Schrehardt, U.; McKie, L.; Brownstein, D.G.; Lee, A.W.; Cross, S.H.; Sado, Y.; Mullins, J.J.; Pöschl, E.; Jackson, I.J. Dominant mutations of Col4a1 result in basement membrane defects which lead to anterior segment dysgenesis and glomerulopathy. Hum. Mol. Genet. 2005, 14, 3161–3168. [Google Scholar] [CrossRef] [PubMed]
- Kjaer, M. Role of Extracellular Matrix in Adaptation of Tendon and Skeletal Muscle to Mechanical Loading. Physiol. Rev. 2004, 84, 649–698. [Google Scholar] [CrossRef] [PubMed]
- Mao, M.; Kiss, M.; Ou, Y.; Gould, D.B. Genetic dissection of anterior segment dysgenesis caused by a Col4a1 mutation in mouse. Model. Mech. 2017, 10, 475–485. [Google Scholar] [CrossRef] [PubMed]
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Liu, C.; Li, L.; Ge, M.; Gu, L.; Wang, M.; Zhang, K.; Su, Y.; Zhang, Y.; Liu, C.; Lan, M.; et al. Overexpression of miR-29 Leads to Myopathy that Resemble Pathology of Ullrich Congenital Muscular Dystrophy. Cells 2019, 8, 459. https://doi.org/10.3390/cells8050459
Liu C, Li L, Ge M, Gu L, Wang M, Zhang K, Su Y, Zhang Y, Liu C, Lan M, et al. Overexpression of miR-29 Leads to Myopathy that Resemble Pathology of Ullrich Congenital Muscular Dystrophy. Cells. 2019; 8(5):459. https://doi.org/10.3390/cells8050459
Chicago/Turabian StyleLiu, Chuncheng, Lei Li, Mengxu Ge, Lijie Gu, Meng Wang, Kuo Zhang, Yang Su, Yuying Zhang, Chang Liu, Miaomiao Lan, and et al. 2019. "Overexpression of miR-29 Leads to Myopathy that Resemble Pathology of Ullrich Congenital Muscular Dystrophy" Cells 8, no. 5: 459. https://doi.org/10.3390/cells8050459