A Mutation Causes MuSK Reduced Sensitivity to Agrin and Congenital Myasthenia

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Ben Ammar, Asma ^a,b   Soltanzadeh, Payam ^a   Bauché, Stéphanie ^a,c   Richard, Pascale ^a   Goillot, Evelyne ^d   Herbst, Ruth ^e   Gaudon, Karen ^a   Huzé, Caroline ^d   Schaeffer, Laurent ^d   Yamanashi, Yuji ^f   Higuchi, Osamu ^f   Taly, Antoine ^g   Koenig, Jeanine ^a   Leroy, Jean Paul ^a   Hentati, Fayçal ^b   Najmabadi, Hossein ^h   Kahrizi, Kimia ^h   Ilkhani, Manouchehr ⁱ   Fardeau, Michel ^a   Eymard, Bruno ^a   Hantaï, Daniel ^a   more..

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b Institut National de Neurologie Tunisia   (Tunisia)

^c PSL RESEARCH UNIVERSITY   (France)

^d UNIVERSITÉ DE LYON   (France)

^e Medical University of Vienna   (Austria)

^f UNIVERSITY OF TOKYO   (Japan)

^g Faculté de Pharmacie   (France)

^h UNIVERSITY OF SOCIAL WELFARE AND REHABILITATION SCIENCES   (Iran)

ⁱ SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; MUSCLE SPECIFIC TYROSINE KINASE; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CASE REPORT; CHILD; CONGENITAL MYASTHENIC SYNDROME; CONSANGUINITY; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTROPORATION; ENZYME ACTIVATION; GAZE PARALYSIS; GENE; GENE MUTATION; GENETIC ANALYSIS; HETEROZYGOSITY; HUMAN; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MISSENSE MUTATION; MOLECULAR PATHOLOGY; MOUSE; MUSCLE BIOPSY; MUSCLE SPECIFIC TYROSINE KINASE GENE; MUSCLE WEAKNESS; NERVE GROWTH; NERVE SPROUTING; NEUROMUSCULAR SYNAPSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN AGGREGATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PTOSIS; SCHOOL CHILD; SYNAPTIC TRANSMISSION; WALKING DIFFICULTY;

AGRIN; ANIMALS; CHILD; HEK293 CELLS; HUMANS; MALE; MICE; MUSCLE PROTEINS; MUSCLE WEAKNESS; MUSCLE, SKELETAL; MUTATION, MISSENSE; MYASTHENIC SYNDROMES, CONGENITAL; NEUROMUSCULAR JUNCTION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, CHOLINERGIC; RECEPTORS, GROWTH FACTOR; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

EID: 84872246996     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053826     Document Type: Article

References (48)

1. Kim N, Stiegler AL, Cameron TO, Hallock PT, Gomez AM, et al. (2008) Lrp4 is a receptor for Agrin and forms a complex with MuSK. Cell 135: 334-342.
2. Zhang B, Luo S, Wang Q, Suzuki T, Xiong WC, et al. (2008) LRP4 serves as a coreceptor of agrin. Neuron 60: 285-297.
3. Zhang W, Coldefy AS, Hubbard SR, Burden SJ, (2010) Agrin binds to the N-terminal region of Lrp4 protein and stimulates association between Lrp4 and the first immunoglobulin-like domain in muscle-specific kinase (MuSK). J Biol Chem 286: 40624-40630.
4. Sobel A, Heidmann T, Hofler J, Changeux JP, (1978) 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: 510-504.
5. Brockhausen J, Cole RN, Gervásio OL, Ngo ST, Noakes PG, et al. (2008) Neural agrin increases postsynaptic ACh receptor packing by elevating rapsyn protein at the mouse neuromuscular synapse. Dev Neurobiol 68: 1153-1169.
6. Zong Y, Zhang B, Gu S, Lee K, Zhou J, et al. (2012) Structural basis of agrin-LRP4-MuSK signaling. Genes Dev 26: 247-258.
7. Jennings CG, Dyer SM, Burden SJ, (1993) Muscle-specific trk-related receptor with a kringle domain defines a distinct class of receptor kinases. Proc Natl Acad Sci USA 90: 2895-2899.
8. Masiakowski P, Yancopoulos GD, (1998) The Wnt receptor CRD domain is also found in MuSK and related orphan receptor tyrosine kinases. Curr Biol 8: R407.
9. Stiegler AL, Burden SJ, Hubbard SR, (2009) Crystal structure of the Frizzled-like cysteine-rich domain of the receptor tyrosine kinase MuSK. J Mol Biol 393: 1-9.
10. Herbst R, Burden SJ, (2000) The juxtamembrane region of MuSK has a critical role in agrin-mediated signaling. EMBO J 19: 67-77.
11. Till JH, Becerra M, Watty A, Lu Y, Ma Y, et al. (2002) Crystal structure of the MuSK tyrosine kinase: insights into receptor autoregulation. Structure 10: 1187-1196.
12. Wiesner A, Fuhrer C, (2006) Regulation of nicotinic acetylcholine receptors by tyrosine kinases in the peripheral and central nervous system: same players, different roles. Cell Mol Life Sci 63: 2818-2828.
13. Strochlic L, Cartaud A, Cartaud J, (2005) The synaptic muscle-specific kinase (MuSK) complex: new partners, new functions. Bioessays 27: 1129-1135.
14. Okada K, Inoue A, Okada M, Murata Y, Kakuta S, et al. (2006) The muscle protein Dok-7 is essential for neuromuscular synaptogenesis. Science 312: 1802-1805.
15. Inoue A, Setoguchi K, Matsubara Y, Okada K, Sato N, et al. (2009) Dok-7 activates the muscle receptor kinase MuSK and shapes synapse formation. Sci Signal 2(59): ra7.
16. Gautam M, Noakes PG, Moscoso L, Rupp F, Scheller RH, et al. (1996) Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 17: 525-535.
17. Weatherbee SD, Anderson KV, Niswander LA, (2006) LDL-receptor-related protein 4 is crucial for formation of the neuromuscular junction. Development 133: 4993-5000.
18. Kong XC, Barzaghi P, Rüegg MA, (2004) Inhibition of synapse assembly in mammalian muscle in vivo by RNA interference. EMBO Rep 5: 183-188.
19. Hesser BA, 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.
20. Engel AG, Sine SM, (2005) Current understanding of congenital myasthenic syndromes. Curr Opin Pharmacol 5: 308-321.
21. Engel AG, Shen XM, Selcen D, Sine SM, (2008) Further observations in congenital myasthenic syndromes. Ann NY Acad Sci 1132: 104-113.
22. Beeson D, Webster R, Cossins J, Lashley D, Spearman H, et al. (2008) Congenital myasthenic syndromes and the formation of the neuromuscular junction. Ann NY Acad Sci 1132: 99-103.
23. Chevessier F, Faraut B, Ravel-Chapuis A, Richard P, Gaudon K, et al. (2004) MuSK, a new target for mutations causing congenital myasthenic syndrome. Hum Mol Genet 13: 3229-3240.
24. Beeson D, Higuchi O, Palace J, Spearman H, Maxwell S, et al. (2006) Dok-7 mutations underlie a neuromuscular junction synaptopathy. Science 313: 1975-1978.
25. Huzé C, Bauché S, Richard P, Chevessier F, Goillot E, et al. (2009) Identification of an agrin mutation that causes congenital myasthenia and affects synapse function. Am J Hum Genet 85: 155-167.
26. Mihaylova V, Salih MA, Mukhtar MM, Abuzeid HA, El-Sadig SM, et al. (2009) Refinement of the clinical phenotype in MuSK-related congenital myasthenic syndromes. Neurology 73: 1926-1928.
27. Maselli RA, Arredondo J, Cagney Ó, Ng JJ, Anderson JA, et al. (2010) Mutations in MUSK causing congenital myasthenic syndrome impair MuSK-Dok-7 interaction. Hum Mol Genet 19: 2370-2379.
28. Koelle GB, Friedenwald JS, (1949) A histological method for localization of cholinesterase activity. Proc Soc Exp Biol Med 70: 617-622.
29. Glass DJ, Apel ED, Shah S, Bowen DC, DeChiara TM, et al. (1997) Kinase domain of the muscle-specific receptor tyrosine kinase (MuSK) is sufficient for phosphorylation but not clustering of acetylcholine receptors: required role for the MuSK ectodomain? Proc Natl Acad Sci USA 94: 8848-8853.
30. Mir LM, Bureau MF, Gehl J, Rangara R, Rouy D, et al. (1999) High-efficiency gene transfer into skeletal muscle mediated by electric pulses. Proc Natl Acad Sci USA 96: 4262-4267.
31. Duclert A, Savatier N, Changeux JP, (1993) A 83-nucleotide promoter of the acetylcholine receptor epsilon-subunit gene confers preferential synaptic expression in mouse muscle. Proc Natl Acad Sci USA 90: 3043-3047.
32. Jat PS, Noble MD, Ataliotis P, Tanaka Y, Yannoutsos N, et al. (1991) Direct derivation of conditionally immortal cell lines from an H-2Kb-tsA58 transgenic mouse. Proc Natl Acad Sci USA 88: 5096-5100.
33. Bedlack RS, Simel DL, Bosworth H, Samsa G, Tucker-Lipscomb B, et al. (2005) Quantitative myasthenia gravis score: assessment of responsiveness and longitudinal validity. Neurology 64: 1968-1970.
34. Bergamin E, Hallock PT, Burden SJ, Hubbard SR, (2010) The cytoplasmic adapter-protein Dok7 activates the receptor tyrosine kinase MuSK via dimerization.,Mol Cell. 39: 100-109.
35. Do Thi NA, Bourre JM, Koenig HL, Trouillet V, Dumont O, et al. (1990) Alteration of ethanolamine glycerophospholipid turnover in Trembler dysmyelinating mutant: an analysis of the sciatic nerve by biochemistry and radioautography. Neurochem Int 17: 573-585.
36. Vincent A, Bowen J, Newsom-Davis J, McConville J, (2003) Seronegative generalised myasthenia gravis: clinical features, antibodies, and their targets. Lancet Neurol 2: 99-106.
37. Müller JS, Herczegfalvi A, Vilchez JJ, Colomer J, Bachinski LL, et al. (2007) Phenotypical spectrum of DOK7 mutations in congenital myasthenic syndromes. Brain 130: 1497-1506.
38. Apel PJ, Ma J, Callahan M, Northam CN, Alton TB, et al. (2010) Effect of locally delivered IGF-1 on nerve regeneration during aging: an experimental study in rats. Muscle Nerve 41: 335-341.
39. Caroni P, Schneider C, Kiefer MC, Zapf J, (1994) Role of muscle insulin-like growth factors in nerve sprouting: suppression of terminal sprouting in paralyzed muscle by IGF-binding protein 4. J Cell Biol 125: 893-902.
40. Tam SL, Gordon T, (2003) Mechanisms controlling axonal sprouting at the neuromuscular junction. J Neurocytol 32: 961-974.
41. Feng Z, Koirala S, Ko CP, (2005) Synapse-glia interactions at the vertebrate neuromuscular junction. Neuroscientist 11: 503-513.
42. Richard S, Brion JP, Couck AM, Flament-Durand J, (1989) Accumulation of smooth endoplasmic reticulum in Alzheimer's disease: new morphological evidence of axoplasmic flow disturbances. J Submicrosc Cytol Pathol 21: 461-467.
43. Hopf C, Hoch W, (1998) Dimerization of the muscle-specific kinase induces tyrosine phosphorylation of acetylcholine receptors and their aggregation on the surface of myotubes. J Biol Chem 273: 6467-6473.
44. Jones G, Moore C, Hashemolhosseini S, Brenner HR, (1999) Constitutively active MuSK is clustered in the absence of agrin and induces ectopic post-synaptic-like membranes in skeletal muscle fibers. J Neurosci 19: 3376-3383.
45. Yamanashi Y, Tezuka T, Yokohama K, (2012) Activation of receptor protein-tyrosine kinases from the cytoplasmic compartment. J Biol Chem 151: 353-359.
46. Hamuro J, Higuchi O, Okada K, Ueno M, Iemura S, et al. (2008) Mutations causing DOK7 congenital myasthenia ablate functional motifs in Dok-7. J Biol,Chem 283: 5518-5524.
47. Taly A, Corringer PJ, Grutter T, Prado de Carvalho L, Karplus M, et al. (2006) Implications of the quaternary twist allosteric model for the physiology and pathology of nicotinic acetylcholine receptors. Proc Natl Acad Sci USA 103: 16965-16970.
48. Taly A, Changeux JP, (2008) Functional organization and conformational dynamics of the nicotinic receptor: a plausible structural interpretation of myasthenic mutations. Ann NY Acad Sci 1132: 42-52.