Muscle specific kinase autoantibodies cause synaptic failure through progressive wastage of postsynaptic acetylcholine receptors

Experimental Neurology

Volumn 237, Issue 2, 2012, Pages 286-295

  Morsch, Marco ^a   Reddel, Stephen W ^b   Ghazanfari, Nazanin ^a   Toyka, Klaus V ^c   Phillips, William D ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b Department of Geriatric Medicine   (Australia)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Acetylcholine receptors; Diaphragm; Endplate potentials; Muscle weakness; MuSK; Myasthenia gravis

Indexed keywords

AUTOANTIBODY; CHOLINERGIC RECEPTOR; IMMUNOGLOBULIN G ANTIBODY; MUSCLE SPECIFIC KINASE; MUSCLE SPECIFIC KINASE AUTOANTIBODY; PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DIAPHRAGM MUSCLE; ELECTROMYOGRAM; ENDPLATE POTENTIAL; FEMALE; GASTROCNEMIUS MUSCLE; MINIATURE ENDPLATE POTENTIAL; MOUSE; MUSCLE ACTION POTENTIAL; MUSCLE WEAKNESS; MYASTHENIA GRAVIS; NEUROMUSCULAR SYNAPSE; NEUROMUSCULAR TRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DENSITY; SYNAPSE; SYNAPTIC FAILURE; WEIGHT REDUCTION;

ACTION POTENTIALS; ANIMALS; AUTOANTIBODIES; AUTOANTIGENS; ELECTROMYOGRAPHY; FEMALE; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MYASTHENIA GRAVIS; NEUROMUSCULAR JUNCTION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, CHOLINERGIC; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84864818526     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.06.034     Document Type: Article

References (50)

1. Akaaboune M., Culican S.M., Turney S.G., Lichtman J.W. Rapid and reversible effects of activity on acetylcholine receptor density at the neuromuscular junction in vivo. Science 1999, 286:503-507.
2. Benveniste O., Jacobson L., Farrugia M.E., Clover L., Vincent A. MuSK antibody positive myasthenia gravis plasma modifies MURF-1 expression in C2C12 cultures and mouse muscle in vivo. J. Neuroimmunol. 2005, 170:41-48.
3. 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.
4. Cole R.N., Reddel S.W., Gervasio O.L., Phillips W.D. Anti-MuSK patient antibodies disrupt the mouse neuromuscular junction. Ann. Neurol. 2008, 63:782-789.
5. Cole R.N., Ghazanfari N., Ngo S.T., Gervasio O.L., Reddel S.W., Phillips W.D. Patient autoantibodies deplete postsynaptic muscle-specific kinase leading to disassembly of the ACh receptor scaffold and myasthenia gravis in mice. J. Physiol. 2010, 588:3217-3229.
6. Conti-Fine B.M., Milani M., Kaminski H.J. Myasthenia gravis: past, present, and future. J. Clin. Invest. 2006, 116:2843-2854.
7. 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. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 1996, 85:501-512.
8. Evoli A., Tonali P.A., Padua L., Monaco M.L., Scuderi F., Batocchi A.P., Marino M., Bartoccioni E. Clinical correlates with anti-MuSK antibodies in generalized seronegative myasthenia gravis. Brain 2003, 126:2304-2311.
9. Ghazanfari N., Fernandez K.J., Murata Y., Morsch M., Ngo S.T., Reddel S.W., Noakes P.G., Phillips W.D. Muscle specific kinase: organiser of synaptic membrane domains. Int. J. Biochem. Cell Biol. 2011, 43:295-298.
10. Harris J.B., Ribchester R.R. The relationship between end-plate size and transmitter release in normal and dystrophic muscles of the mouse. J. Physiol. 1979, 296:245-265.
11. Hesser B.A., 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.
12. Higuchi O., Hamuro J., Motomura M., Yamanashi Y. Autoantibodies to low-density lipoprotein receptor-related protein 4 in myasthenia gravis. Ann. Neurol. 2011, 69:418-422.
13. Hoch W., McConville J., Helms S., Newsom-Davis J., Melms A., Vincent A. Auto-antibodies to the receptor tyrosine kinase MuSK in patients with myasthenia gravis without acetylcholine receptor antibodies. Nat. Med. 2001, 7:365-368.
14. Jha S., Xu K., Maruta T., Oshima M., Mosier D.R., Atassi M.Z., 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.
15. Kao I., Drachman D.B. Myasthenic immunoglobulin accelerates acetylcholine receptor degradation. Science 1977, 196:527-529.
16. Kawakami Y., Ito M., Hirayama M., Sahashi K., Ohkawara B., Masuda A., Nishida H., Mabuchi N., Engel A.G., Ohno K. Anti-MuSK autoantibodies block binding of collagen Q to MuSK. Neurology 2011, 77:1819-1826.
17. Klooster R., Plomp J.J., Huijbers M.G., Niks E.H., Straasheijm K.R., Detmers F.J., Hermans P.W., Sleijpen K., Verrips A., Losen M., Martinez-Martinez P., De Baets M.H., van der Maarel S.R.M., Verschuuren J.J. Muscle-specific kinase myasthenia gravis IgG4 autoantibodies cause severe neuromuscular junction dysfunction in mice. Brain 2012, 135:1081-1101.
18. Kong X.C., Barzaghi P., Ruegg M.A. Inhibition of synapse assembly in mammalian muscle in vivo by RNA interference. EMBO Rep. 2004, 5:183-188.
19. Land B.R., Salpeter E.E., Salpeter M.M. Kinetic parameters for acetylcholine interaction in intact neuromuscular junction. Proc. Natl. Acad. Sci. U. S. A. 1981, 78:7200-7204.
20. Martignago S., Fanin M., Albertini E., Pegoraro E., Angelini C. Muscle histopathology in myasthenia gravis with antibodies against MuSK and AChR. Neuropathol. Appl. Neurobiol. 2009, 35:103-110.
21. Martin A.R. The effect of membrane capacitance on non-linear summation of synaptic potentials. J. Theor. Biol. 1976, 59:179-187.
22. McConville J., Farrugia M.E., Beeson D., Kishore U., Metcalfe R., Newsom-Davis J., Vincent A. Detection and characterization of MuSK antibodies in seronegative myasthenia gravis. Ann. Neurol. 2004, 55:580-584.
23. McLachlan E.M., Martin A.R. Non-linear summation of end-plate potentials in the frog and mouse. J. Physiol. 1981, 311:307-324.
24. Mori S., Kubo S., Akiyoshi T., Yamada S., Miyazaki T., Hotta H., Desaki J., Kishi M., Konishi T., Nishino Y., Miyazawa A., Maruyama N., Shigemoto K. Antibodies against muscle-specific kinase impair both presynaptic and postsynaptic functions in a murine model of myasthenia gravis. Am. J. Pathol. 2012, 180:798-810.
25. Niks E.H., van Leeuwen Y., Leite M.I., Dekker F.W., Wintzen A.R., Wirtz P.W., Vincent A., van Tol M.J., Jol-van der Zijde C.M., Verschuuren J.J. Clinical fluctuations in MuSK myasthenia gravis are related to antigen-specific IgG4 instead of IgG1. J. Neuroimmunol. 2008, 195:151-156.
26. Niks E.H., Kuks J.B., Wokke J.H., Veldman H., Bakker E., Verschuuren J.J., Plomp J.J. Pre- and postsynaptic neuromuscular junction abnormalities in MuSK myasthenia. Muscle Nerve 2010, 42:283-288.
27. Otterness I.G., Chang Y.H. Comparative study of cyclophosphamide, 6-mercaptopurine, azathiopurine and methotrexate. Relative effects on the humoral and the cellular immune response in the mouse. Clin. Exp. Immunol. 1976, 26:346-354.
28. Pevzner A., Schoser B., Peters K., Cosma N.-C., Karakatsani A., Schalke B., Melms A., Kröger S. Anti-LRP4 autoantibodies in AChR- and MuSK-antibody-negative myasthenia gravis. J. Neurol. 2011, 259:427-435.
29. Plomp J.J., van Kempen G.T., Molenaar P.C. Adaptation of quantal content to decreased postsynaptic sensitivity at single endplates in alpha-bungarotoxin-treated rats. J. Physiol. 1992, 458:487-499.
30. Plomp J.J., van Kempen G.T., Molenaar P.C. The upregulation of acetylcholine release at endplates of alpha-bungarotoxin-treated rats: its dependency on calcium. J. Physiol. 1994, 478:125-136.
31. Plomp J.J., Van Kempen G.T., De Baets M.B., Graus Y.M., Kuks J.B., Molenaar P.C. Acetylcholine release in Myasthenia gravis: regulation at single end-plate level. Ann. Neurol. 1995, 37:627-636.
32. Punga A.R., Lin S., Oliveri F., Meinen S., Ruegg M.A. Muscle-selective synaptic disassembly and reorganization in MuSK antibody positive MG mice. Exp. Neurol. 2011, 230:207-217.
33. Richman D.P., Nishi K., Morell S.W., Chang J.M., Ferns M.J., Wollmann R.L., Maselli R.A., Schnier J., Agius M.A. Acute severe animal model of anti-muscle-specific kinase myasthenia: combined postsynaptic and presynaptic changes. Arch. Neurol. 2012, 69:453-460.
34. Rodgaard A., Nielsen F.C., Djurup R., Somnier F., Gammeltoft S. Acetylcholine receptor antibody in Myasthenia gravis: predominance of IgG subclasses 1 and 3. Clin. Exp. Immunol. 1987, 67:82-88.
35. Ruff R.L., Lennon V.A. How Myasthenia gravis alters the safety factor for neuromuscular transmission. J. Neuroimmunol. 2008, 201-202:13-20.
36. Selcen D., Fukuda T., Shen X.M., Engel A.G. Are MuSK antibodies the primary cause of myasthenic symptoms?. Neurology 2004, 62:1945-1950.
37. 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.
38. Shiraishi H., Motomura M., Yoshimura T., Fukudome T., Fukuda T., Nakao Y., Tsujihata M., Vincent A., Eguchi K. Acetylcholine receptors loss and postsynaptic damage in MuSK antibody-positive myasthenia gravis. Ann. Neurol. 2005, 57:289-293.
39. Stacy S., Gelb B.E., Koop B.A., Windle J.J., Wall K.A., Krolick K.A., Infante A.J., Kraig E. Split tolerance in a novel transgenic model of autoimmune myasthenia gravis. J. Immunol. 2002, 169:6570-6579.
40. Stevens C.F. A comment on Martin's relation. Biophys. J. 1976, 16:891-895.
41. ter Beek W.P., Martinez-Martinez P., Losen M., de Baets M.H., Wintzen A.R., Verschuuren J.J., Niks E.H., van Duinen S.G., Vincent A., Molenaar P.C. The effect of plasma from muscle-specific tyrosine kinase myasthenia patients on regenerating endplates. Am. J. Pathol. 2009, 175:1536-1544.
42. Toyka K.V., Brachman D.B., Pestronk A., Kao I. Myasthenia gravis: passive transfer from man to mouse. Science 1975, 190:397-399.
43. Toyka K.V., Drachman D.B., Griffin D.E., Pestronk A., Winkelstein J.A., Fishbeck K.H., Kao I. Myasthenia gravis. Study of humoral immune mechanisms by passive transfer to mice. N. Engl. J. Med. 1977, 296:125-131.
44. Tsujimoto T., Umemiya M., Kuno M. Terminal sprouting is not responsible for enhanced transmitter release at disused neuromuscular junctions of the rat. J. Neurosci. 1990, 10:2059-2065.
45. Viegas S., Jacobson L., Waters P., Cossins J., Jacob S., Leite M.I., Webster R., Vincent A. Passive and active immunization models of MuSK-Ab positive myasthenia: electrophysiological evidence for pre and postsynaptic defects. Exp. Neurol. 2012, 234:506-512.
46. Vincent A., Newsom-Davis J. Acetylcholine receptor antibody characteristics in myasthenia gravis. I. Patients with generalized myasthenia or disease restricted to ocular muscles. Clin. Exp. Immunol. 1982, 49:257-265.
47. Wang X., Wang Q., Engisch K.L., Rich M.M. Activity-dependent regulation of the binomial parameters p and n at the mouse neuromuscular junction in vivo. J. Neurophysiol. 2010, 104:2352-2358.
48. Wood S.J., Slater C.R. Safety factor at the neuromuscular junction. Prog. Neurobiol. 2001, 64:393-429.
49. Wu H., Xiong W.C., Mei L. To build a synapse: signaling pathways in neuromuscular junction assembly. Development 2010, 137:1017-1033.
50. Xu K., Jha S., Hoch W., Dryer S.E. Delayed synapsing muscles are more severely affected in an experimental model of MuSK-induced myasthenia gravis. Neuroscience 2006, 143:655-659.