MuSK levels differ between adult skeletal muscles and influence postsynaptic plasticity

European Journal of Neuroscience

Volumn 33, Issue 5, 2011, Pages 890-898

  Punga, Anna R ^a,b   Maj, Marcin ^b   Lin, Shuo ^a   Meinen, Sarina ^a   Rüegg, Markus A ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UPPSALA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Acetylcholine receptors; Agrin; Mice; Muscle; MuSK; Neuromuscular junction

Indexed keywords

AGRIN; CHOLINERGIC RECEPTOR; CHOLINERGIC RECEPTOR ALPHA; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MUSCLE PROTEIN; MUSCLE SPECIFIC TYROSINE KINASE; PROTEIN DOK 7; PROTEIN LRP4; PROTEIN TYROSINE KINASE; RAPSYN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXTENSOR DIGITORUM LONGUS MUSCLE; FEMALE; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OMOHYOID MUSCLE; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SKELETAL MUSCLE; SOLEUS MUSCLE; STERNOCLEIDOMASTOID MUSCLE; TRANSGENIC MOUSE; WILD TYPE;

AGRIN; ANIMALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE PROTEINS; MUSCLE, SKELETAL; NEURONAL PLASTICITY; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, CHOLINERGIC; SYNAPSES; SYNAPTIC POTENTIALS;

EID: 79952440857     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07569.x     Document Type: Article

References (43)

1. Beeson, D., Webster, R., Cossins, J., Lashley, D., Spearman, H., Maxwell, S., Slater, C.R., Newsom-Davis, J., Palace, J. & Vincent, A. (2008) Congenital myasthenic syndromes and the formation of the neuromuscular junction. Ann. NY Acad. Sci., 1132, 99-103.
2. Bowen, D.C., Park, J.S., Bodine, S., Stark, J.L., Valenzuela, D.M., Stitt, T.N., Yancopoulos, G.D., Lindsay, R.M., Glass, D.J. & DiStefano, P.S. (1998) Localization and regulation of MuSK at the neuromuscular junction. Dev. Biol., 199, 309-319.
3. Chevessier, F., Faraut, B., Ravel-Chapuis, A., Richard, P., Gaudon, K., Bauche, S., Prioleau, C., Herbst, R., Goillot, E., Ioos, C., Azulay, J.P., Attarian, S., Leroy, J.P., Fournier, E., Legay, C., Schaeffer, L., Koenig, J., Fardeau, M., Eymard, B., Pouget, J. & Hantai, D. (2004) MUSK, a new target for mutations causing congenital myasthenic syndrome. Hum. Mol. Genet., 13, 3229-3240.
4. Chevessier, F., Girard, E., Molgo, J., Bartling, S., Koenig, J., Hantai, D. & Witzemann, V. (2008) A mouse model for congenital myasthenic syndrome due to MuSK mutations reveals defects in structure and function of neuromuscular junctions. Hum. Mol. Genet., 17, 3577-3595.
5. DeChiara, T.M., Bowen, D.C., Valenzuela, D.M., Simmons, M.V., Poueymirou, W.T., Thomas, S., Kinetz, E., Compton, D.L., Rojas, E., Park, J.S., Smith, C., DiStefano, P.S., Glass, D.J., Burden, S.J. & Yancopoulos, G.D. (1996) The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell, 85, 501-512.
6. Dulhunty, A.F. & Dlutowski, M. (1979) Fiber types in red and white segments of rat sternomastoid muscle. Am J Anat, 156, 51-61.
7. Engel, A.G. & Sine, S.M. (2005) Current understanding of congenital myasthenic syndromes. Curr Opin Pharmacol., 5, 308-321.
8. Evoli, A., Tonali, P.A., Padua, L., Monaco, M.L., Scuderi, F., Batocchi, A.P., Marino, M. & Bartoccioni, E. (2003) Clinical correlates with anti-MuSK antibodies in generalized seronegative myasthenia gravis. Brain, 126, 2304-2311.
9. Feng, G., Mellor, R.H., Bernstein, M., Keller-Peck, C., Nguyen, Q.T., Wallace, M., Nerbonne, J.M., Lichtman, J.W. & Sanes, J.R. (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron, 28, 41-51.
10. Gautam, M., Noakes, P.G., Mudd, J., Nichol, M., Chu, G.C., Sanes, J.R. & Merlie, J.P. (1995) Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature, 377, 232-236.
11. Goldman, D. & Staple, J. (1989) Spatial and temporal expression of acetylcholine receptor RNAs in innervated and denervated rat soleus muscle. Neuron, 3, 219-228.
12. Herbst, R., Avetisova, E. & Burden, S.J. (2002) Restoration of synapse formation in Musk mutant mice expressing a Musk/Trk chimeric receptor. Development, 129, 5449-5460.
13. Hesser, B.A., Henschel, O. & Witzemann, V. (2006) Synapse disassembly and formation of new synapses in postnatal muscle upon conditional inactivation of MuSK. Mol. Cell. Neurosci., 31, 470-480.
14. Hoch, W., McConville, J., Helms, S., Newsom-Davis, J., Melms, A. & Vincent, A. (2001) Auto-antibodies to the receptor tyrosine kinase MuSK in patients with myasthenia gravis without acetylcholine receptor antibodies. Nat. Med., 7, 365-368.
15. Inoue, A., Setoguchi, K., Matsubara, Y., Okada, K., Sato, N., Iwakura, Y., Higuchi, O. & Yamanashi, Y. (2009) Dok-7 activates the muscle receptor kinase MuSK and shapes synapse formation. Sci Signal., 2, ra7.
16. Jha, S., Xu, K., Maruta, T., Oshima, M., Mosier, D.R., Atassi, M.Z. & Hoch, W. (2006) Myasthenia gravis induced in mice by immunization with the recombinant extracellular domain of rat muscle-specific kinase (MuSK). J. Neuroimmunol., 175, 107-117.
17. Jones, G., Meier, T., Lichtsteiner, M., Witzemann, V., Sakmann, B. & Brenner, H.R. (1997) Induction by agrin of ectopic and functional postsynaptic-like membrane in innervated muscle. Proc. Natl Acad. Sci. USA, 94, 2654-2659.
18. Jones, G., Moore, C., Hashemolhosseini, S. & 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.
19. Kim, N., Stiegler, A.L., Cameron, T.O., Hallock, P.T., Gomez, A.M., Huang, J.H., Hubbard, S.R., Dustin, M.L. & Burden, S.J. (2008) Lrp4 is a receptor for Agrin and forms a complex with MuSK. Cell, 135, 334-342.
20. Kong, X.C., Barzaghi, P. & Ruegg, M.A. (2004) Inhibition of synapse assembly in mammalian muscle in vivo by RNA interference. EMBO Rep., 5, 183-188.
21. Krejci, E., Legay, C., Thomine, S., Sketelj, J. & Massoulie, J. (1999) Differences in expression of acetylcholinesterase and collagen Q control the distribution and oligomerization of the collagen-tailed forms in fast and slow muscles. J. Neurosci., 19, 10672-10679.
22. Kues, W.A., Sakmann, B. & Witzemann, V. (1995) Differential expression patterns of five acetylcholine receptor subunit genes in rat muscle during development. Eur. J. Neurosci., 7, 1376-1385.
23. Lin, S., Maj, M., Bezakova, G., Magyar, J.P., Brenner, H.R. & Ruegg, M.A. (2008) Muscle-wide secretion of a miniaturized form of neural agrin rescues focal neuromuscular innervation in agrin mutant mice. Proc. Natl Acad. Sci. USA, 105, 11406-11411.
24. Meier, T., Hauser, D.M., Chiquet, M., Landmann, L., Ruegg, M.A. & Brenner, H.R. (1997) Neural agrin induces ectopic postsynaptic specializations in innervated muscle fibers. J. Neurosci., 17, 6534-6544.
25. Meinen, S., Barzaghi, P., Lin, S., Lochmuller, H. & Ruegg, M.A. (2007) Linker molecules between laminins and dystroglycan ameliorate laminin-alpha2-deficient muscular dystrophy at all disease stages. J. Cell Biol., 176, 979-993.
26. Meriggioli, M.N. & Sanders, D.B. (2009) Autoimmune myasthenia gravis: emerging clinical and biological heterogeneity. Lancet Neurol., 8, 475-490.
27. Moll, J., Barzaghi, P., Lin, S., Bezakova, G., Lochmuller, H., Engvall, E., Muller, U. & Ruegg, M.A. (2001) An agrin minigene rescues dystrophic symptoms in a mouse model for congenital muscular dystrophy. Nature, 413, 302-307.
28. Muntener, M., Gottschall, J., Neuhuber, W., Mysicka, A. & Zenker, W. (1980) The ansa cervicalis and the infrahyoid muscles of the rat I. Anatomy; distribution, number and diameter of fiber types; motor units. Anat Embryol (Berl)., 159, 49-57.
29. Murphy, R.M., Watt, K.K., Cameron-Smith, D., Gibbons, C.J. & Snow, R.J. (2003) Effects of creatine supplementation on housekeeping genes in human skeletal muscle using real-time RT-PCR. Physiol. Genomics, 12, 163-174.
30. Okada, K., Inoue, A., Okada, M., Murata, Y., Kakuta, S., Jigami, T., Kubo, S., Shiraishi, H., Eguchi, K., Motomura, M., Akiyama, T., Iwakura, Y., Higuchi, O. & Yamanashi, Y. (2006) The muscle protein Dok-7 is essential for neuromuscular synaptogenesis. Science, 312, 1802-1805.
31. Pun, S., Sigrist, M., Santos, A.F., Ruegg, M.A., Sanes, J.R., Jessell, T.M., Arber, S. & Caroni, P. (2002) An intrinsic distinction in neuromuscular junction assembly and maintenance in different skeletal muscles. Neuron, 34, 357-370.
32. Rostedt Punga, A., Ahlqvist, K., Bartoccioni, E., Scuderi, F., Marino, M., Suomalainen, A., Kalimo, H. & Stalberg, E.V. (2006) Neurophysiological and mitochondrial abnormalities in MuSK antibody seropositive myasthenia gravis compared to other immunological subtypes. Clin. Neurophysiol., 117, 1434-1443.
33. Sanes, J.R. & Lichtman, J.W. (2001) Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci., 2, 791-805.
34. Schaeffer, L., de Kerchove d'Exaerde, A. & Changeux, J.P. (2001) Targeting transcription to the neuromuscular synapse. Neuron, 31, 15-22.
35. Schmittgen, T.D. & Livak, K.J. (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc., 3, 1101-1108.
36. Scotton, P., Bleckmann, D., Stebler, M., Sciandra, F., Brancaccio, A., Meier, T., Stetefeld, J. & Ruegg, M.A. (2006) Activation of muscle-specific receptor tyrosine kinase and binding to dystroglycan are regulated by alternative mRNA splicing of agrin. J. Biol. Chem., 281, 36835-36845.
37. Slater, C.R. (2008) Structural factors influencing the efficacy of neuromuscular transmission. Ann. NY Acad. Sci., 1132, 1-12.
38. Till, J.H., Becerra, M., Watty, A., Lu, Y., Ma, Y., Neubert, T.A., Burden, S.J. & Hubbard, S.R. (2002) Crystal structure of the MuSK tyrosine kinase: insights into receptor autoregulation. Structure, 10, 1187-1196.
39. Valenzuela, D.M., Stitt, T.N., DiStefano, P.S., Rojas, E., Mattsson, K., Compton, D.L., Nunez, L., Park, J.S., Stark, J.L., Gies, D.R., Thomas, S., Le Beau, M.M., Fernald, A.A., Copeland, N.G., Jenkins, N.A., Burden, S.J., Glass, D.J., & Yancopoulos, G.D. (1995) Receptor tyrosine kinase specific for the skeletal muscle lineage: expression in embryonic muscle, at the neuromuscular junction, and after injury. Neuron, 15, 573-584.
40. Wang, Q., Zhang, B., Xiong, W.C. & Mei, L. (2006) MuSK signaling at the neuromuscular junction. J. Mol. Neurosci., 30, 223-226.
41. Witzemann, V., Barg, B., Criado, M., Stein, E. & Sakmann, B. (1989) Developmental regulation of five subunit specific mRNAs encoding acetylcholine receptor subtypes in rat muscle. FEBS Lett., 242, 419-424.
42. Yuzbasioglu, A., Onbasilar, I., Kocaefe, C. & Ozguc, M. (2010) Assessment of housekeeping genes for use in normalization of real time PCR in skeletal muscle with chronic degenerative changes. Exp. Mol. Pathol., 88, 326-329.
43. Zhang, B., Luo, S., Wang, Q., Suzuki, T., Xiong, W.C. & Mei, L. (2008) LRP4 serves as a coreceptor of agrin. Neuron, 60, 285-297.