Synemin acts as a regulator of signalling molecules during skeletal muscle hypertrophy

Journal of Cell Science

Volumn 127, Issue 21, 2014, Pages 4589-4601

  Li, Zhenlin ^a   Parlakian, Ara ^a   Coletti, Dario ^a   Alonso Martin, Sonia ^a   Hourdé, Christophe ^a   Joanne, Pierre ^a   Gao Li, Jacqueline ^a   Blanc, Jocelyne ^a   Ferry, Arnaud ^a   Paulin, Denise ^a   Xue, Zhigang ^a   Agbulut, Onnik ^a  

^a SORBONNE UNIVERSITÉ   (France)

Author keywords

Desmin; Intermediate filament; Muscle hypertrophy; Skeletal muscle

Indexed keywords

ATROGIN 1; CYTOSKELETON PROTEIN; FOLLISTATIN; MYOSTATIN; SYNEMIN; UNCLASSIFIED DRUG; DESMIN; INTERMEDIATE FILAMENT PROTEIN; SYNEMIN PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL RENEWAL; CONTROLLED STUDY; FEMALE; MALE; MOUSE; MUSCLE FATIGUE; MUSCLE HYPERTROPHY; MUSCLE MASS; MUSCLE STRENGTH; NONHUMAN; SARCOLEMMA; SATELLITE CELL; SIGNAL TRANSDUCTION; ANIMAL; GENETICS; HYPERTROPHY; KNOCKOUT MOUSE; METABOLISM; MUSCLE DISEASE; PATHOLOGY; PHYSIOLOGY; SKELETAL MUSCLE; ULTRASTRUCTURE;

ANIMALS; CELL DIFFERENTIATION; DESMIN; HYPERTROPHY; INTERMEDIATE FILAMENT PROTEINS; MALE; MICE; MICE, KNOCKOUT; MUSCLE, SKELETAL; MUSCULAR DISEASES;

EID: 84913586182     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.143164     Document Type: Article

References (51)

1. Agbulut, O., Li, Z., Périé, S., Ludosky, M. A., Paulin, D., Cartaud, J. and Butler-Browne, G. (2001). Lack of desmin results in abortive muscle regeneration and modifications in synaptic structure. Cell Motil. Cytoskeleton 49, 51-66.
2. Agbulut, O., Vignaud, A., Hourde, C., Mouisel, E., Fougerousse, F., Butler-Browne, G. S. and Ferry, A. (2009). Slow myosin heavy chain expression in the absence of muscle activity. Am. J. Physiol. 296, C205-C214.
3. Bellin, R. M., Sernett, S. W., Becker, B., Ip, W., Huiatt, T. W. and Robson, R. M. (1999). Molecular characteristics and interactions of the intermediate filament protein synemin. Interactions with alpha-actinin may anchor synemin-containing heterofilaments. J. Biol. Chem. 274, 29493-29499.
4. Berdeaux, R. and Stewart, R. (2012). cAMP signaling in skeletal muscle adaptation: hypertrophy, metabolism, and regeneration. Am. J. Physiol. 303, E1-E17.
5. Bhosle, R. C., Michele, D. E., Campbell, K. P., Li, Z. and Robson, R. M. (2006). Interactions of intermediate filament protein synemin with dystrophin and utrophin. Biochem. Biophys. Res. Commun. 346, 768-777.
6. Carlsson, L., Li, Z. L., Paulin, D., Price, M. G., Breckler, J., Robson, R. M., Wiche, G. and Thornell, L. E. (2000). Differences in the distribution of synemin, paranemin, and plectin in skeletal muscles of wild-type and desmin knock-out mice. Histochem. Cell Biol. 114, 39-47.
7. Chen, A. E., Ginty, D. D. and Fan, C.-M. (2005). Protein kinase A signalling via CREB controls myogenesis induced by Wnt proteins. Nature 433, 317-322.
8. Chourbagi, O., Bruston, F., Carinci, M., Xue, Z., Vicart, P., Paulin, D. and Agbulut, O. (2011). Desmin mutations in the terminal consensus motif prevent synemin-desmin heteropolymer filament assembly. Exp. Cell Res. 317, 886-897.
9. Colucci-Guyon, E., Portier, M. M., Dunia, I., Paulin, D., Pournin, S. and Babinet, C. (1994). Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell 79, 679-694.
10. de Souza Martins, S. C., Agbulut, O., Diguet, N., Larcher, J.-C., Paulsen, B. S., Rehen, S. K., Moura-Neto, V., Paulin, D., Li, Z. and Xue, Z. (2011). Dynamic expression of synemin isoforms in mouse embryonic stem cells and neural derivatives. BMC Cell Biol. 12, 51.
11. Dessauer, C. W. (2009). Adenylyl cyclase-A-kinase anchoring protein complexes: the next dimension in cAMP signaling. Mol. Pharmacol. 76, 935-941.
12. Gary-Bobo, G., Parlakian, A., Escoubet, B., Franco, C. A., Clément, S., Bruneval, P., Tuil, D., Daegelen, D., Paulin, D., Li, Z. et al. (2008). Mosaic inactivation of the serum response factor gene in the myocardium induces focal lesions and heart failure. Eur. J. Heart Fail. 10, 635-645.
13. Goodman, C. A., Frey, J. W., Mabrey, D. M., Jacobs, B. L., Lincoln, H. C., You, J.-S. and Hornberger, T. A. (2011). The role of skeletal muscle mTOR in the regulation of mechanical load-induced growth. J. Physiol. 589, 5485-5501.
14. Granger, B. L. and Lazarides, E. (1980). Synemin: a new high molecular weight protein associated with desmin and vimentin filaments in muscle. Cell 22, 727-738.
15. Hijikata, T., Nakamura, A., Isokawa, K., Imamura, M., Yuasa, K., Ishikawa, R., Kohama, K., Takeda, S. and Yorifuji, H. (2008). Plectin 1 links intermediate filaments to costameric sarcolemma through beta-synemin, alpha-dystrobrevin and actin. J. Cell Sci. 121, 2062-2074.
16. Hirako, Y., Yamakawa, H., Tsujimura, Y., Nishizawa, Y., Okumura, M., Usukura, J., Matsumoto, H., Jackson, K. W., Owaribe, K. and Ohara, O. (2003). Characterization of mammalian synemin, an intermediate filament protein present in all four classes of muscle cells and some neuroglial cells: colocalization and interaction with type III intermediate filament proteins and keratins. Cell Tissue Res. 313, 195-207.
17. Hourdé, C., Joanne, P., Medja, F., Mougenot, N., Jacquet, A., Mouisel, E., Pannerec, A., Hatem, S., Butler-Browne, G., Agbulut, O. et al. (2013a). Voluntary physical activity protects from susceptibility to skeletal muscle contraction-induced injury but worsens heart function in mdx mice. Am. J. Pathol. 182, 1509-1518.
18. Hourdé, C., Joanne, P., Noirez, P., Agbulut, O., Butler-Browne, G. and Ferry, A. (2013b). Protective effect of female gender-related factors on muscle force-generating capacity and fragility in the dystrophic mdx mouse. Muscle Nerve 48, 68-75.
19. Izmiryan, A., Cheraud, Y., Khanamiryan, L., Leterrier, J. F., Federici, T., Peltekian, E., Moura-Neto, V., Paulin, D., Li, Z. and Xue, Z. G. (2006). Different expression of synemin isoforms in glia and neurons during nervous system development. Glia 54, 204-213.
20. Izmiryan, A., Franco, C. A., Paulin, D., Li, Z. and Xue, Z. (2009). Synemin isoforms during mouse development: multiplicity of partners in vascular and neuronal systems. Exp. Cell Res. 315, 769-783.
21. Izmiryan, A., Peltekian, E., Federici, T., Paulin, D., Li, Z. L. and Xue, Z. G. (2010). Synemin isoforms in astroglial and neuronal cells from human central nervous system. Neurochem. Res. 35, 881-887.
22. Jing, R., Pizzolato, G., Robson, R. M., Gabbiani, G. and Skalli, O. (2005). Intermediate filament protein synemin is present in human reactive and malignant astrocytes and associates with ruffled membranes in astrocytoma cells. Glia 50, 107-120.
23. Jing, R., Wilhelmsson, U., Goodwill, W., Li, L., Pan, Y., Pekny, M. and Skalli, O. (2007). Synemin is expressed in reactive astrocytes in neurotrauma and interacts differentially with vimentin and GFAP intermediate filament networks. J. Cell Sci. 120, 1267-1277.
24. Joanne, P., Hourdé, C., Ochala, J., Caudéran, Y., Medja, F., Vignaud, A., Mouisel, E., Hadj-Said, W., Arandel, L., Garcia, L. et al. (2012). Impaired adaptive response to mechanical overloading in dystrophic skeletal muscle. PLoS ONE 7, e35346.
25. Joanne, P., Chourbagi, O., Hourdé, C., Ferry, A., Butler-Browne, G., Vicart, P., Dumonceaux, J. and Agbulut, O. (2013). Viral-mediated expression of desmin mutants to create mouse models of myofibrillar myopathy. Skelet. Muscle 3, 4.
26. Khanamiryan, L., Li, Z., Paulin, D. and Xue, Z. (2008). Self-assembly incompetence of synemin is related to the property of its head and rod domains. Biochemistry 47, 9531-9539.
27. Launay, T., Noirez, P., Butler-Browne, G. and Agbulut, O. (2006). Expression of slow myosin heavy chain during muscle regeneration is not always dependent on muscle innervation and calcineurin phosphatase activity. Am. J. Physiol. 290, R1508-R1514.
28. Lazarides, E. (1980). Intermediate filaments as mechanical integrators of cellular space. Nature 283, 249-255.
29. Le Grand, F., Jones, A. E., Seale, V., Scimè, A. and Rudnicki, M. A. (2009). Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell 4, 535-547.
30. Li, Z., Colucci-Guyon, E., Pinçon-Raymond, M., Mericskay, M., Pournin, S., Paulin, D. and Babinet, C. (1996). Cardiovascular lesions and skeletal myopathy in mice lacking desmin. Dev. Biol. 175, 362-366.
31. Li, Z., Mericskay, M., Agbulut, O., Butler-Browne, G., Carlsson, L., Thornell, L. E., Babinet, C. and Paulin, D. (1997). Desmin is essential for the tensile strength and integrity of myofibrils but not for myogenic commitment, differentiation, and fusion of skeletal muscle. J. Cell Biol. 139, 129-144.
32. Lund, L. M., Kerr, J. P., Lupinetti, J., Zhang, Y., Russell, M. A., Bloch, R. J. and Bond, M. (2012). Synemin isoforms differentially organize cell junctions and desmin filaments in neonatal cardiomyocytes. FASEB J. 26, 137-148.
33. Milner, D. J., Weitzer, G., Tran, D., Bradley, A. and Capetanaki, Y. (1996). Disruption of muscle architecture and myocardial degeneration in mice lacking desmin. J. Cell Biol. 134, 1255-1270.
34. Mitchell, K. J., Pannérec, 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.
35. Mizuno, Y., Thompson, T. G., Guyon, J. R., Lidov, H. G., Brosius, M., Imamura, M., Ozawa, E., Watkins, S. C. and Kunkel, L. M. (2001). Desmuslin, an intermediate filament protein that interacts with alpha-dystrobrevin and desmin. Proc. Natl. Acad. Sci. USA 98, 6156-6161.
36. Musarò, A., McCullagh, K., Paul, A., Houghton, L., Dobrowolny, G., Molinaro, M., Barton, E. R., Sweeney, H. L. and Rosenthal, N. (2001). Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat. Genet. 27, 195-200.
37. Noetzel, E., Rose, M., Sevinc, E., Hilgers, R.-D., Hartmann, A., Naami, A., Knüchel, R. and Dahl, E. (2010). Intermediate filament dynamics and breast cancer: aberrant promoter methylation of the Synemin gene is associated with early tumor relapse. Oncogene 29, 4814-4825.
38. Pekny, T., Faiz, M., Wilhelmsson, U., Curtis, M. A., Matej, R., Skalli, O. and Pekny, M. (2014). Synemin is expressed in reactive astrocytes and Rosenthal fibers in Alexander disease. APMIS 122, 76-80.
39. Pitre, A., Davis, N., Paul, M., Orr, A. W. and Skalli, O. (2012). Synemin promotes AKT-dependent glioblastoma cell proliferation by antagonizing PP2A. Mol. Biol. Cell 23, 1243-1253.
40. Russell, M. A., Lund, L. M., Haber, R., McKeegan, K., Cianciola, N. and Bond, M. (2006). The intermediate filament protein, synemin, is an AKAP in the heart. Arch. Biochem. Biophys. 456, 204-215.
41. Schmitt-Graeff, A., Jing, R., Nitschke, R., Desmoulière, A. and Skalli, O. (2006). Synemin expression is widespread in liver fibrosis and is induced in proliferating and malignant biliary epithelial cells. Hum. Pathol. 37, 1200-1210.
42. Stewart, R., Flechner, L., Montminy, M. and Berdeaux, R. (2011). CREB is activated by muscle injury and promotes muscle regeneration. PLoS ONE 6, e24714.
43. Sun, N., Critchley, D. R., Paulin, D., Li, Z. and Robson, R. M. (2008a). Human alpha-synemin interacts directly with vinculin and metavinculin. Biochem. J. 409, 657-667.
44. Sun, N., Critchley, D. R., Paulin, D., Li, Z. and Robson, R. M. (2008b). Identification of a repeated domain within mammalian alpha-synemin that interacts directly with talin. Exp. Cell Res. 314, 1839-1849.
45. Sun, N., Huiatt, T. W., Paulin, D., Li, Z. and Robson, R. M. (2010a). Synemin interacts with the LIM domain protein zyxin and is essential for cell adhesion and migration. Exp. Cell Res. 316, 491-505.
46. Sun, Y., Ge, Y., Drnevich, J., Zhao, Y., Band, M. and Chen, J. (2010b). Mammalian target of rapamycin regulates miRNA-1 and follistatin in skeletal myogenesis. J. Cell Biol. 189, 1157-1169.
47. Tawk, M., Titeux, M., Fallet, C., Li, Z., Daumas-Duport, C., Cavalcante, L. A., Paulin, D. and Moura-Neto, V. (2003). Synemin expression in developing normal and pathological human retina and lens. Exp. Neurol. 183, 499-507.
48. Titeux, M., Brocheriou, V., Xue, Z., Gao, J., Pellissier, J. F., Guicheney, P., Paulin, D. and Li, Z. (2001). Human synemin gene generates splice variants encoding two distinct intermediate filament proteins. Eur. J. Biochem. 268, 6435-6449.
49. Uyama, N., Zhao, L., Van Rossen, E., Hirako, Y., Reynaert, H., Adams, D. H., Xue, Z., Li, Z., Robson, R., Pekny, M. et al. (2006). Hepatic stellate cells express synemin, a protein bridging intermediate filaments to focal adhesions. Gut 55, 1276-1289.
50. Xue, Z. G., Cheraud, Y., Brocheriou, V., Izmiryan, A., Titeux, M., Paulin, D. and Li, Z. (2004). The mouse synemin gene encodes three intermediate filament proteins generated by alternative exon usage and different open reading frames. Exp. Cell Res. 298, 431-444.
51. Zammit, P. S., Golding, J. P., Nagata, Y., Hudon, V., Partridge, T. A. and Beauchamp, J. R. (2004). Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J. Cell Biol. 166, 347-357.