Overexpression of mini-agrin in skeletal muscle increases muscle integrity and regenerative capacity in laminin-α2-deficient mice

FASEB Journal

Volumn 19, Issue 8, 2005, Pages 934-942

  Bentzinger, C Florian ^a   Barzaghi, Patrizia ^a   Lin, Shuo ^a   Ruegg, Markus A ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Laminin 2 deficiency; Muscle regeneration; Muscular dystrophy

Indexed keywords

AGRIN; LAMININ ALPHA2;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CONTROLLED STUDY; GENE OVEREXPRESSION; GENETIC LINKAGE; MOUSE; MUSCLE ATROPHY; MUSCLE FIBER MEMBRANE; MUSCLE FUNCTION; MUSCLE INJURY; MUSCLE REGENERATION; MUSCULAR DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SARCOLEMMA; SKELETAL MUSCLE; TRANSCRIPTION REGULATION; WILD TYPE;

AGRIN; ANIMALS; BASEMENT MEMBRANE; DYSTROGLYCANS; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; LAMININ; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MOTOR ACTIVITY; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; REGENERATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SARCOLEMMA;

EID: 20444434366     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.04-3376com     Document Type: Article

References (35)

1. Tome, F. M., Evangelista, T., Leclerc, A., Sunada, Y., Manole, E., Estournet, B., Barois, A., Campbell, K. P., and Fardeau, M. (1994) Congenital muscular dystrophy with merosin deficiency. C. R. Acad. Sci. III 317, 351-357
2. Ruegg, M. A. (2005) Commonalities and differences in muscular dystrophies: mechanisms and molecules involved in merosin-deficient congenital muscular dystrophy. In Molecular mechanisms of muscular dystrophies (Winder, S., ed) Landes Bioscience, In press
3. Michelson, A. M., Russell, E. S., and Harman, P. J. (1955) Dystrophia muscularis: a hereditary primary myopathy in the house mouse. Proc. Natl. Acad. Sci. USA 41, 1079-1084
4. Meier, H., and Southard, J. L. (1970) Muscular dystrophy in the mouse caused by an allele at the dy-locus. Life Sci. 9, 137-144
5. Kuang, W., Xu, H., Vachon, P. H., Liu, L., Loechel, F., Wewer, U. M., and Engvall, E. (1998) Merosin-deficient congenital muscular dystrophy. Partial genetic correction in two mouse models. J. Clin. Invest. 102, 844-852
6. Miyagoe, Y., Hanaoka, K., Nonaka, I., Hayasaka, M., Nabeshima, Y., Arahata, K., and Takeda, S. (1997) Laminin alpha2 chain-null mutant mice by targeted disruption of the Lama2 gene: a new model of merosin (laminin 2)-deficient congenital muscular dystrophy. FEBS Lett. 415, 33-39
7. Guo, L. T., Zhang, X. U., Kuang, W., Xu, H., Liu, L. A., Vilquin, J. T., Miyagoe-Suzuki, Y., Takeda, S., Ruegg, M. A., Wewer, U. M., et al. (2003) Laminin alpha2 deficiency and muscular dystrophy; genotype-phenotype correlation in mutant mice. Neuromusc. Disord. 13, 207-215
8. Jones, K. J., Morgan, G., Johnston, H., Tobias, V., Ouvrier, R. A., Wilkinson, I., and North, K. N. (2001) The expanding phenotype of laminin alpha2 chain (merosin) abnormalities: case series and review. J. Med. Genet. 38, 649-657
9. Colognato, H., and Yurchenco, P. D. (2000) Form and function: the laminin family of heterotrimers. Dev. Dyn. 218, 213-234
10. Li, S., Edgar, D., Fassler, R., Wadsworth, W., and Yurchenco, P. D. (2003) The role of laminin in embryonic cell polarization and tissue organization. Dev. Cell, 613-624
11. Patton, B. L., Miner, J. H., Chiu, A. Y., and Sanes, J. R. (1997) Distribution and function of laminins in the neuromuscular system of developing, adult, and mutant mice. J. Cell Biol. 139, 1507-1521
12. Ringelmann, B., Roder, C., Hallmann, R., Maley, M., Davies, M., Grounds, M., and Sorokin, L. (1999) Expression of laminin alpha1, alpha2, alpha4, and alpha5 chains, fibronectin, and tenascin-C in skeletal muscle of dystrophic 129ReJ dy/dy mice. Exp. Cell Res. 246, 165-182
13. Moll, J., Barzaghi, P., Lin, S., Bezakova, G., Lochmuller, H., Engvall, E., Muller, U., and Ruegg, M. A. (2001) An agrin minigene rescues dystrophic symptoms in a mouse model for congenital muscular dystrophy. Nature (London) 413, 302-307
14. Talts, J. F., Sasaki, T., Miosge, N., Gohring, W., Mann, K., Mayne, R., and Timpl, R. (2000) Structural and functional analysis of the recombinant G domain of the laminin alpha 4 chain and its proteolytic processing in tissues. J. Biol. Chem. 275, 35192-35199
15. Xu, H., Wu, X. R., Wewer, U. M., and Engvall, E. (1994) Murine muscular dystrophy caused by a mutation in the laminin alpha 2 (Lama2) gene. Nat. Genet. 8, 297-302
16. Colognato, H., and Yurchenco, P. D. (1999) The laminin a2 expressed by dystrophic dy(2J) mice is defective in its ability to form polymers. Curr. Biol. 9, 1327-1330
17. Kuang, W., Xu, H., Vilquin, J. T., and Engvall, E. (1999) Activation of the lama2 gene in muscle regeneration: abortive regeneration in laminin alpha2-deficiency. Lab. Invest. 79, 1601-1613
18. Gawlik, K., Miyagoe-Suzuki, Y, Ekblom, P., Takeda, S., and Durbeej, M. (2004) Laminin a1 chain reduces muscular dystrophy in laminin a2 chain deficient mice. Hum. Mol. Genet. 13, 1775-1784
19. Kammerer, R. A., Schulthess, T., Landwehr, R., Schumacher, B., Lustig, A., Yurchenco, P. D., Ruegg, M. A., Engel, J., and Denzer, A. J. (1999) Interaction of agrin with laminin requires a coiled-coil conformation of the agrin-binding site within the laminin gl chain. EMBO J. 18, 6762-6770
20. Gesemann, M., Brancaccio, A., Schumacher, B., and Ruegg, M. A. (1998) Agrin is a high-affinity binding protein of dystroglycan in non-muscle tissue. J. Biol. Chem. 273, 600-605
21. Aufderheide, E., Chiquet-Ehrismann, R., and Ekblom, P. (1987) Epithelial-mesenchymal interactions in the developing kidney lead to expression of tenascin in the mesenchyme. J. Cell Biol. 105, 599-608
22. Gesemann, M., Denzer, A. J., and Ruegg, M. A. (1995) Acetylcholine receptor-aggregating activity of agrin isoforms and mapping of the active site. J. Cell Biol. 128, 625-636
23. Jones, G., Moore, C., Hashemolhosseini, S., and Brenner, H. R. (1999) Constitutively active MuSK is clustered in the absence of agrin and induces ectopic postsynaptic-like membranes in skeletal muscle fibers. J. Neurosci. 19, 3376-3383
24. Moore, C., Leu, M., Muller, U., and Brenner, H. R. (2001) Induction of multiple signaling loops by MuSK during neuromuscular synapse formation. Proc. Natl. Acad. Sci. USA 98, 14655-14660
25. Briguet, A., Courdier-Fruh, I., Foster, M., Meier, T., and Magyar, J. P. (2004) Histological parameters for the quantitative assessment of muscular dystrophy in the mdx-mouse. Neuromusc. Disord. 14, 675-682
26. Covault, J., Merlie, J. P., Goridis, C., and Sanes, J. R. (1986) Molecular forms of N-CAM and its RNA in developing and denervated skeletal muscle. J. Cell Biol. 102, 731-739
27. Harris, J. B., and Johnson, M. A. (1978) Further observations on the pathological responses of rat skeletal muscle to toxins isolated from the venom of the Australian tiger snake, Notechis scutatus scutatus. Clin. Exp. Pharmacol. Physiol 5, 587-600
28. Harris, J. B., and Cullen, M. J. (1990) Muscle necrosis caused by snake venoms and toxins. Electron Microsc. Rev. 3, 183-211
29. Mayer, U., Saher, G., Fassler, R., Bornemann, A., Echtermeyer, F., Von der Mark, H., Miosge, N., Poschl, E., and Von der Mark, K. (1997) Absence of integrin alpha7 causes a novel form of muscular dystrophy. Nat. Genet. 17, 318-323
30. Burkin, D. J., Wallace, G. Q., Nicol, K. J., Kaufman, D. J., and Kaufman, S. J. (2001) Enhanced expression of the alpha 7 beta 1 integrin reduces muscular dystrophy and restores viability in dystrophic mice. J. Cell Biol. 152, 1207-1218
31. Schwander, M., Leu, M., Stumm, M., Dorchies, O. M., Ruegg, U. T., Schittny, J., and Muller, U. (2003) Beta1 integrins regulate myoblast fusion and sarcomere assembly. Dev. Cell 4, 673-685
32. Cohn, R. D., Henry, M. D., Michele, D. E., Barresi, R., Saito, F., Moore, S. A., Flanagan, J. D., Skwarchuk, M. W., Robbins, M. E., Mendell, J. R., et al. (2002) Disruption of DAG1 in differentiated skeletal muscle reveals a role for dystroglycan in muscle regeneration. Cell 110, 639-648
33. Langenbach, K. J., and Rando, T. A. (2002) Inhibition of dystroglycan binding to laminin disrupts the PI3K/AKT pathway and survival signaling in muscle cells. Muscle Nerve 26, 644-653
34. Spence, H.J., Dhillon, A. S., James, M., and Winder, S. J. (2004) Dystroglycan, a scaffold for the ERK-MAP kinase cascade. EMBO Rep. 5, 484-489
35. Yu, H., and Talts, J. F. (2003) Beta1 integrin and alpha-dystroglycan binding sites are localized to different laminin-G-domain-like (LG) modules within the laminin alphas chain G domain. Biochem. J. 371, 289-299