Identification of an Agrin Mutation that Causes Congenital Myasthenia and Affects Synapse Function

American Journal of Human Genetics

Volumn 85, Issue 2, 2009, Pages 155-167

  Huzé, Caroline ^a   Bauché, Stéphanie ^b,c,d   Richard, Pascale ^e   Chevessier, Frédéric ^b,f   Goillot, Evelyne ^a   Gaudon, Karen ^e   Ben Ammar, Asma ^b,c,g   Chaboud, Annie ^h   Grosjean, Isabelle ^h   Lecuyer, Heba Aude ^a   Bernard, Véronique ⁱ   Rouche, Andrée ^b   Alexandri, Nektaria ^b   Kuntzer, Thierry ^j   Fardeau, Michel ^k   Fournier, Emmanuel ^e   Brancaccio, Andrea ^l   Rüegg, Markus A ^m   Koenig, Jeanine ^b,c,n   Eymard, Bruno ^b,c,k   Schaeffer, Laurent ^a   Hantaï, Daniel ^b,c,k   more..

^a UNIVERSITÉ DE LYON   (France)

^b INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d PSL RESEARCH UNIVERSITY   (France)

^e PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^f MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^g Institut National de Neurologie Tunisia   (Tunisia)

^h Institut Fédératif de Recherche 128   (France)

ⁱ INSERM   (France)

^j LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^k ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^l CATHOLIC UNIVERSITY   (Italy)

^m UNIVERSITY OF BASEL   (Switzerland)

ⁿ UNIVERSITÉ DE BORDEAUX   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; ARGININE; CHOLINERGIC RECEPTOR; DYSTROGLYCAN; DYSTROGLYCAN ALPHA; GENOMIC DNA; GLYCINE; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 4; PROTEIN MUSK; PROTEIN TYROSINE KINASE; RECEPTOR PROTEIN; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

ADULT; AGRIN GENE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CASE REPORT; CLINICAL FEATURE; CONGENITAL MYASTHENIC SYNDROME; CONTROLLED STUDY; FEMALE; GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; MISSENSE MUTATION; MUSCLE BIOPSY; MUTATIONAL ANALYSIS; MYOTUBE; NEUROMUSCULAR SYNAPSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PEDIGREE ANALYSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT;

RATTUS;

EID: 68349151039     PISSN: 00029297     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ajhg.2009.06.015     Document Type: Article

References (41)

1. Hantaï D., Richard P., Koenig J., and Eymard B. Congenital myasthenic syndromes. Curr. Opin. Neurol. 17 (2004) 539-551
2. Engel A.G., and Sine S.M. Current understanding of congenital myasthenic syndromes. Curr. Opin. Pharmacol. 5 (2005) 308-321
3. Müller J.S., Mihaylova V., Abicht A., and Lochmüller H. Congenital myasthenic syndromes: Spotlight on genetic defects of neuromuscular transmission. Expert Rev. Mol. Med. 9 (2007) 1-20
4. Maselli R.A., Ng J.J., Anderson J.A., Cagney O., Arredondo J., Williams C., Wessel H.B., Abdel-Hamid H., and Wollmann R.L. Mutations in LAMB2 causing a severe form of synaptic congenital myasthenic syndrome. J. Med. Genet. 46 (2009) 203-208
5. Chevessier F., Faraut B., Ravel-Chapuis A., Richard P., Gaudon K., Bauché S., Prioleau C., Herbst R., Goillot E., Ioos C., et al. MUSK, a new target for mutations causing congenital myasthenic syndrome. Hum. Mol. Genet. 13 (2004) 3229-3240
6. Beeson D., Higuchi O., Palace J., Cossins J., Spearman H., Maxwell S., Newsom-Davis J., Burke G., Fawcett P., Motomura M., et al. Dok-7 mutations underlie a neuromuscular junction synaptopathy. Science 313 (2006) 1975-1978
7. Kim N., Stiegler A.L., Cameron T.O., Hallock P.T., Gomez A.M., Huang J.H., Hubbard S.R., Dustin M.L., and Burden S.J. Lrp4 is a receptor for Agrin and forms a complex with MuSK. Cell 135 (2008) 334-342
8. Zhang B., Luo S., Wang Q., Suzuki T., Xiong W.C., and Mei L. LRP4 serves as a coreceptor of agrin. Neuron 60 (2008) 285-297
9. Sobel A., Heidmann T., Hofler J., and Changeux J.P. Distinct protein components from Torpedo marmorata membranes carry the acetylcholine receptor site and the binding site for local anesthetics and histrionicotoxin. Proc. Natl. Acad. Sci. USA 75 (1978) 510-514
10. Brockhausen J., Cole R.N., Gervásio O.L., Ngo S.T., Noakes P.G., and Phillips W.D. Neural agrin increases postsynaptic ACh receptor packing by elevating rapsyn protein at the mouse neuromuscular synapse. Dev. Neurobiol. 68 (2008) 1153-1169
11. Misgeld T., Kummer T.T., Lichtman J.W., and Sanes J.R. Agrin promotes synaptic differentiation by counteracting an inhibitory effect of neurotransmitter. Proc. Natl. Acad. Sci. USA 102 (2005) 11088-11093
12. Lin S., Maj M., Bezakova G., Magyar J.P., Brenner H.R., and Rüegg M.A. Muscle wide secretion of a miniaturized form of neural agrin rescues focal neuromuscular innervation in agrin mutant mice. Proc. Natl. Acad. Sci. USA 105 (2008) 11406-11411
13. Gautam M., Noakes P.G., Moscoso L., Rupp F., Scheller R.H., Merlie J.P., and Sanes J.R. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85 (1996) 525-535
14. Denzer A.J., Brandenberger R., Gesemann M., Chiquet M., and Rüegg M.A. Agrin binds to the nerve-muscle basal lamina via laminin. J. Cell Biol. 137 (1997) 671-683
15. Gee S.H., Montanaro F., Lindenbaum M.H., and Carbonetto S. Dystroglycan-alpha, a dystrophin-associated glycoprotein, is a functional agrin receptor. Cell 77 (1994) 675-686
16. Scotton P., Bleckmann D., Stebler M., Sciandra F., Brancaccio A., Meier T., Stetefeld J., and Rüegg M.A. Activation of muscle-specific receptor tyrosine kinase and binding to dystroglycan are regulated by alternative mRNA splicing of agrin. J. Biol. Chem. 281 (2006) 36835-36845
17. Tsim K.W., Rüegg M.A., Escher G., Kröger S., and McMahan U.J. cDNA that encodes active agrin. Neuron 8 (1992) 677-689
18. Rupp F., Ozçelik T., Linial M., Peterson K., Francke U., and Scheller R. Structure and chromosomal localization of the mammalian agrin gene. J. Neurosci. 12 (1992) 3535-3544
19. Bezakova G., and Rüegg M.A. New insights into the roles of agrin. Nat. Rev. Mol. Cell Biol. 4 (2003) 295-308
20. Gesemann M., Denzer A.J., and Rüegg M.A. Acetylcholine receptor-aggregating activity of agrin isoforms and mapping of the active site. J. Cell Biol. 128 (1995) 625-636
21. Koelle G.B., and Friedenwald J.A. A histochemical method for localizing cholinesterase activity. Proc. Soc. Exp. Biol. Med. 70 (1949) 617-622
22. Brooke M.H., and Kaiser K.K. Some comments on the histochemical characterization of muscle adenosine-triphosphatase. J. Histochem. Cytochem. 17 (1969) 431-432
23. Moll J., Barzaghi P., Lin S., Bezakova G., Lochmüller H., Engvall E., Müller U., and Rüegg M.A. An agrin minigene rescues dystrophic symptoms in a mouse model for congenital muscular dystrophy. Nature 413 (2001) 302-307
24. Fuhrer C., Sugiyama J.E., Taylor R.G., and Hall Z.W. Association of muscle-specific kinase MuSK with the acetylcholine receptor in mammalian muscle. EMBO J. 16 (1997) 4951-4960
25. Gesemann M., Cavalli V., Denzer A.J., Brancaccio A., Schumacher B., and Rüegg M.A. Alternative splicing of agrin alters its binding to heparin, dystroglycan, and the putative agrin receptor. Neuron 16 (1996) 755-767
26. Ishigaki K., Nicolle D., Krejci E., Leroy J.P., Koenig J., Fardeau M., Eymard B., and Hantaï D. Two novel mutations in the COLQ gene cause endplate acetylcholinesterase deficiency. Neuromuscul. Disord. 13 (2003) 236-244
27. Meier T., Marangi P.A., Moll J., Hauser D.M., Brenner H.R., and Rüegg M.A. A minigene of neural agrin encoding the laminin-binding and acetylcholine receptor-aggregating domains is sufficient to induce postsynaptic differentiation in muscle fibres. Eur. J. Neurosci. 10 (1998) 3141-3152
28. Pun S., Ng Y.P., Yang J.F., Ip N.Y., and Tsim K.W. Agrin-deficient myotube retains its acetylcholine receptor aggregation ability when challenged with agrin. J. Neurochem. 69 (1997) 2555-2563
29. Meinen S., Barzaghi P., Lin S., Lochmüller H., and Rüegg M.A. Linker molecules between laminins and dystroglycan ameliorate laminin-alpha2-deficient muscular dystrophy at all disease stages. J. Cell Biol. 176 (2007) 979-993
30. Hashemolhosseini S., Moore C., Landmann L., Sander A., Schwarz H., Witzemann V., Sakmann B., and Brenner H.R. Electrical activity and postsynapse formation in adult muscle: gamma-AChRs are not required. Mol. Cell. Neurosci. 16 (2000) 697-707
31. Bezakova G., Helm J.P., Francolini M., and Lømo T. Effects of purified recombinant neural and muscle agrin on skeletal muscle fibers in vivo. J. Cell Biol. 153 (2001) 1441-1452
32. Bezakova G., and Lømo T. Muscle activity and muscle agrin regulate the organization of cytoskeletal proteins and attached acetylcholine receptor (AChR) aggregates in skeletal muscle fibers. J. Cell Biol. 153 (2001) 1453-1463
33. Bezakova G., Rabben I., Sefland I., Fumagalli G., and Lømo T. Neural agrin controls acetylcholine receptor stability in skeletal muscle fibers. Proc. Natl. Acad. Sci. USA 98 (2001) 9924-9929
34. Nishimune H., Valdez G., Jarad G., Moulson C.L., Müller U., Miner J.H., and Sanes J.R. Laminins promote postsynaptic maturation by an autocrine mechanism at the neuromuscular junction. J. Cell Biol. 182 (2008) 1201-1215
35. Grady R.M., Zhou H., Cunningham J.M., Henry M.D., Campbell K.P., and Sanes J.R. Maturation and maintenance of the neuromuscular synapse: Genetic evidence for roles of the dystrophin-glycoprotein complex. Neuron 25 (2000) 279-293
36. Adams M.E., Kramarcy N., Krall S.P., Rossi S.G., Rotundo R.L., Sealock R., and Froehner S.C. Absence of alpha-syntrophin leads to structurally aberrant neuromuscular synapses deficient in utrophin. J. Cell Biol. 150 (2000) 1385-1398
37. Cairns N.J., Lee V.M., and Trojanowski J.Q. The cytoskeleton in neurodegenerative diseases. J. Pathol. 204 (2004) 438-449
38. Hilgenberg L.G., Ho K.D., Lee D., O'Dowd D.K., and Smith M.A. Alpha3Na+/K+-ATPase is a neuronal receptor for agrin. Cell 125 (2006) 359-369
39. Zahler R., Sun W., Ardito T., Zhang Z.T., Kocsis J.D., and Kashgarian M. The alpha3 isoform protein of the Na+, K(+)-ATPase is associated with the sites of cardiac and neuromuscular impulse transmission. Circ. Res. 78 (1996) 870-879
40. Blaustein M.P. Physiological effects of endogenous ouabain: Control of intracellular Ca2+ stores and cell responsiveness. Am. J. Physiol. 264 (1993) C1367-C1387
41. Denzer A.J., Hauser D.M., Gesemann M., and Rüegg M.A. Synaptic differentiation: The role of agrin in the formation and maintenance of the neuromuscular junction. Cell Tissue Res. 290 (1997) 357-365