Patient autoantibodies deplete postsynaptic muscle-specific kinase leading to disassembly of the ACh receptor scaffold and myasthenia gravis in mice

Journal of Physiology

Volumn 588, Issue 17, 2010, Pages 3217-3229

  Cole, R N ^a   Ghazanfari, N ^a   Ngo, S T ^a   Gervasio O L ^a   Reddel, S W ^b   Phillips, W D ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b Department of Geriatric Medicine   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; CHOLINERGIC RECEPTOR; IMMUNOGLOBULIN G; PHOSPHOTRANSFERASE; PROTEIN SUBUNIT; TYROSINE; MESSENGER RNA; POSTSYNAPTIC MUSCLE SPECIFIC KINASE; PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; MOUSE; MUSCLE CELL; MUSCLE WEAKNESS; MYASTHENIA GRAVIS; NEUROMUSCULAR SYNAPSE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ADULT; ENZYME PHOSPHORYLATION; HUMAN; IMMUNOFLUORESCENCE; INTERNALIZATION; MYOTUBE; PROTEIN DEPLETION; STAINING;

ANIMALS; AUTOANTIBODIES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; IMMUNOGLOBULIN G; MATRIX ATTACHMENT REGIONS; MICE; MICE, INBRED C57BL; MYASTHENIA GRAVIS; NEUROMUSCULAR JUNCTION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, CHOLINERGIC; SYNAPSES;

EID: 77956275172     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.190298     Document Type: Article

References (51)

1. Antolik C, Catino DH, Resneck WG, Bloch RJ. The tetratricopeptide repeat domains of rapsyn bind directly to cytoplasmic sequences of the muscle-specific kinase. Neuroscience 2007, 145:56-65.
2. Banks GB, Fuhrer C, Adams ME, Froehner SC. The postsynaptic submembrane machinery at the neuromuscular junction: requirement for rapsyn and the utrophin/dystrophin-associated complex. J Neurocytol 2003, 32:709-726.
3. Bezakova G, Rabben I, Sefland I, Fumagalli G, Lomo T. Neural agrin controls acetylcholine receptor stability in skeletal muscle fibers. Proc Natl Acad Sci U S A 2001, 98:9924-9929.
4. Boneva N, Frenkian-Cuvelier M, Bidault J, Brenner T, Berrih-Aknin S. Major pathogenic effects of anti-MuSK antibodies in myasthenia gravis. J Neuroimmunol 2006, 177:119-131.
5. Borges L, Yechikov S, Lee YI, Rudell JB, Friese MB, Burden SJ, Ferns M. Identification of a motif in the acetylcholine receptor β-subunit whose phosphorylation regulates rapsyn association and postsynaptic receptor localization. J Neurosci 2008, 28:11468-11476.
6. Bowen DC, Park JS, Bodine S, Stark JL, Valenzuela DM, Stitt TN, Yancopoulos GD, Lindsay RM, Glass DJ, DiStefano PS. Localisation and regulation of MuSK at the neuromuscular junction. Dev Biol 1998, 199:309-319.
7. Brockhausen J, Cole RN, Gervásio OL, Ngo ST, Noakes PG, Phillips WD. Neural agrin increases postsynaptic ACh receptor packing by elevating rapsyn protein at the mouse neuromuscular synapse. Dev Neurobiol 2008, 68:1153-1169.
8. Burges J, Vincent A, Molenaar PC, Newsom-Davis J, Peers C, Wray D. Passive transfer of seronegative myasthenia gravis to mice. Muscle Nerve 1994, 17:1393-1400.
9. Cole RN, Reddel SW, Gervásio OL, Phillips WD. Anti-MuSK patient antibodies disrupt the mouse neuromuscular junction. Ann Neurol 2008, 63:782-789.
10. Conti-Fine BM, Milani M, Kaminski HJ. Myasthenia gravis: past, present, and future. J Clin Invest 2006, 116:2843-2854.
11. Drummond GB. Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 2009, 587:713-719.
12. Evoli A, Tonali PA, Padua L, Monaco ML, Scuderi F, Batocchi AP, Marino M, Bartoccioni E. Clinical correlates with anti-MuSK antibodies in generalized seronegative myasthenia gravis. Brain 2003, 126:2304-2311.
13. Farrugia ME, Bonifatia DM, Clovera L, Cossinsa J, Beesona D, Vincent A. Effect of sera from AChR-antibody negative myasthenia gravis patients on AChR and MuSK in cell cultures. J Neuroimmunol 2007, 185:136-144.
14. Fuhrer C, Gautam M, Sugiyama JE, Hall ZW. Roles of rapsyn and agrin in interaction of postsynaptic proteins with acetylcholine receptors. J Neurosci 1999, 19:6405-6416.
15. Gervásio OL, Armson PF, Phillips WD. Developmental increase in the amount of rapsyn per acetylcholine receptor promotes postsynaptic receptor packing and stability. Dev Biol 2007, 305:262-275.
16. Gervásio OL, Phillips WD. Increased ratio of rapsyn to ACh receptor stabilizes postsynaptic receptors at the mouse neuromuscular synapse. J Physiol 2005, 562:673-685.
17. Glass DJ, Bowen DC, Stitt TN, Radiejewski C, Brunno J, Ryan TE, Gies DR, Shah S, Mattsson K, Burden SJ, DiStefano PS, Valenzuela DM, DeChiara TM, Yancopoulos GD. Agrin acts via a MuSK receptor complex. Cell 1996, 85:513-523.
18. Hesser BA, Henschel O, Witzemann V. Synapse disassembly and formation of new synapses in postnatal muscle upon conditional inactivation of MuSK. Mol Cell Neurosci 2006, 31:470-480.
19. Hoch W, McConville J, Helms S, Newsom-Davis J, Melms A, Vincent A. Autoantibodies to the receptor tyrosine kinase MuSK in patients with myasthenia gravis without acetylcholine receptor antibodies. Nat Med 2001, 7:365-368.
20. Hopf C, Hoch W. Dimerization of the muscle-specific kinase induces tyrosine phosphorylation of acetylcholine receptors and their aggregation on the surface of myotubes. J Biol Chem 1998, 273:6467-6473.
21. Inoue A, Setoguchi K, Matsubara Y, Okada K, Sato N, Iwakura Y, Higuchi O, Yamanashi Y. Dok-7 activates the muscle receptor kinase MuSK and shapes synapse formation. Sci Signal 2009, 2:ra7.
22. Jha S, Xu K, Maruta T, Oshima M, Mosier DR, Atassi MZ, Hoch W. Myasthenia gravis induced in mice by immunization with the recombinant extracellular domain of rat muscle-specific kinase (MuSK). J Neuroimmunol 2006, 175:107-117.
23. Kim N, Stiegler AL, Cameron TO, Hallock PT, Gomez AM, Huang JH, Hubbard SR, Dustin ML, Burden SJ. Lrp4 is a receptor for agrin and forms a complex with MuSK. Cell 2008, 135:334-342.
24. Kong XC, Barzaghi P, Ruegg MA. Inhibition of synapse assembly in mammalian muscle in vivo by RNA interference. EMBO Rep 2004, 5:183-188.
25. Lacazette E, Le Calvez S, Gajendran N, Brenner HR. A novel pathway for MuSK to induce key genes in neuromuscular synapse formation. J Cell Biol 2003, 161:727-736.
26. Land BR, Salpeter EE, Salpeter MM. Acetylcholine receptor site density affects the rising phase of miniature endplate currents. Proc Natl Acad Sci U S A 1980, 77:3736-3740.
27. Linnoila J, Wang Y, Yao Y, Wang ZZ. A mammalian homologue of Drosophila tumorous imaginal discs, TID1, mediates agrin signaling at the neuromuscular junction. Neuron 2008, 60:625-641.
28. Lu Z, Je H-S, Young P, Gross J, Lu B, Feng G. Regulation of synaptic growth and maturation by a synapse-associated E3 ubiquitin ligase at the neuromuscular junction. J Cell Biol 2007, 177:1077-1089.
29. Luo ZG, Wang Q, Zhou JZ, Wang J, Luo Z, Liu M, He X, Wynshaw-Boris A, Xiong WC, Lu B, Mei L. Regulation of AChR clustering by dishevelled interacting with MuSK and PAK1. Neuron 2002, 35:489-505.
30. McConville J, Farrugia ME, Beeson D, Kishore U, Metcalf R, Newsom-Davis J, Vincent A. Detection and characterization of MuSK antibodies in seronegative myasthenia gravis. Ann Neurol 2004, 55:580-584.
31. Madhavan R, Peng HB. Molecular regulation of postsynaptic differentiation at the neuromuscular junction. IUBMB Life 2005, 57:719-730.
32. Moransard M, Borges LS, Willmann R, Marangi PA, Brenner HR, Ferns MJ, Fuhrer C. Agrin regulates rapsyn interaction with surface AChRs which underlies cytoskeletal anchoring and clustering. J Biol Chem 2003, 278:7350-7359.
33. Ngo ST, Balke C, Phillips WD, Noakes PG. Neuregulin potentiates agrin-induced acetylcholine receptor clustering in myotubes. Neuroreport 2004, 15:2501-2505.
34. Peng HB, Froehner SC. Association of the postsynaptic 43K protein with newly formed acetylcholine receptor clusters in cultured muscle cells. J Cell Biol 1985, 100:1698-1705.
35. Qian YK, Chan AWS, Madhavan R, Peng HB. The function of Shp2 tyrosine phosphatase in the dispersal of acetylcholine receptor clusters. BMC Neurosci 2008, 9:70.
36. Rupp F, Ozçelik T, Linial M, Peterson K, Francke U, Scheller R. Structure and chromosomal localization of the mammalian agrin gene. J Neurosci 1992, 12:3535-3544.
37. Salpeter MM, Harris R. Distribution and turnover rate of acetylcholine receptors throughout the junction folds at a vertebrate neuromuscular junction. J Cell Biol 1983, 96:1781-1785.
38. Sanes JR, Lichtman JW. Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2001, 2:791-805.
39. Shigemoto K, Kubo S, Maruyama N, Hato N, Yamada H, Jie C, Kobayashi N, Mominoki K, Abe Y, Ueda N, Matsuda S. Induction of myasthenia by immunization against muscle-specific kinase. J Clin Invest 2006, 116:1016-1024.
40. Stacy S, Gelb BE, Koop BA, Windle JJ, Wall KA, Krolick KA, Infante AJ, Kraig E. Split tolerance in a novel transgenic model of autoimmune myasthenia gravis. J Immunol 2002, 169:6570-6579.
41. Strochlic L, Cartaud A, Cartaud J. The synaptic muscle-specific kinase (MuSK) complex: new partners, new functions. Bioessays 2005, 27:1129-1135.
42. Strochlic L, Cartaud A, Mejat A, Grailhe R, Schaeffer L, Changeux JP, Cartaud J. 14-3-3 γ associates with muscle specific kinase and regulates synaptic gene transcription at vertebrate neuromuscular synapse. Proc Natl Acad Sci U S A 2004, 101:18189-18194.
43. ter Beek PW, Martínez-Martínez P, Losen M, de Baets MH, Wintzen AR, Verschuuren JJ, Niks EH, Duinen SGV, Vincent A, Molenaar PC. The effect of plasma from muscle-specific tyrosine kinase myasthenia gravis patients on regenerating endplates. Am J Path 2009, 175:1536-1544.
44. Toyka KV, Drachman DB, Griffin DE, Pestronk A, Winkelstein JA, Fishbeck KH, Kao I. Myasthenia gravis. Study of humoral immune mechanisms by passive transfer to mice. N Engl J Med 1977, 296:125-131.
45. Weston C, Yee B, Hod E, Prives JM. Agrin-induced acetylcholine receptor clustering is mediated by the small guanosine triphosphatases Rac and Cdc42. J Cell Biol 2000, 150:205-212.
46. Witzemann V, Brenner HR, Sakmann B. Neural factors regulate AChR subunit mRNAs at rat neuromuscular junctions. J Cell Biol 1991, 114:125-141.
47. Wood SJ, Slater CR. Safety factor at the neuromuscular junction. Prog Neurobiol 2001, 64:393-429.
48. Xu K, Jha S, Hoch W, Dryer SE. Delayed synapsing muscle are more severely affected in an experimental model of MuSK-induced myasthenia gravis. Neuroscience 2006, 143:655-659.
49. Zhang B, Luo S, Wang Q, Suzuki T, Xiong WC, Mei L. LRP4 serves as a coreceptor of agrin. Neuron 2008, 60:285-297.
50. Zhou H, Glass DJ, Yancopoulos GD, Sanes JR. Distinct domains of MuSK mediate its abilities to induce and to associate with postsynaptic specializations. J Cell Biol 1999, 146:1133-1146.
51. Zhu D, Yang Z, Luo Z, Luo S, Xiong WC, Mei L. Muscle-specific receptor tyrosine kinase endocytosis in acetylcholine receptor clustering in response to agrin. J Neurosci 2008, 28:1688-1696.