MuSK autoantibodies in myasthenia gravis detected by cell based assay - A multinational study

Journal of Neuroimmunology

Volumn 284, Issue , 2015, Pages 10-17

  Tsonis, A I ^a,b   Zisimopoulou, P ^a   Lazaridis, K ^a   Tzartos, J ^a   Matsigkou, E ^a   Zouvelou, V ^c   Mantegazza, R ^d   Antozzi, C ^d   Andreetta, F ^d   Evoli, A ^e   Deymeer, F ^f   Saruhan Direskeneli, G ^f   Durmus, H ^f   Brenner, T ^g   Vaknin, A ^g   Berrih Aknin, S ^h   Behin, A ^h   Sharshar, T ⁱ   De Baets, M ^j   Losen, M ^j   Martinez Martinez, P ^j   Kleopa, K A ^k   Zamba Papanicolaou, E ^k   Kyriakides, T ^k   Kostera Pruszczyk, A ^l   Szczudlik, P ^l   Szyluk, B ^l   Lavrnic, D ^m   Basta, I ^m   Peric, S ^m   Tallaksen, C ^n,o   Maniaol, A ⁿ   Casasnovas Pons, C ^p   Pitha, J ^q   Jakubikova M ^q   Hanisch, F ^r   Tzartos, S J ^a,b,s   more..

^a HELLENIC PASTEUR INSTITUTE   (Greece)

^b UNIVERSITY OF PATRAS   (Greece)

^c NATIONAL AND KAPODISTRIAN UNIVERSITY OF ATHENS   (Greece)

^d DEPARTMENT OF NEUROSURGERY   (Italy)

^e CATHOLIC UNIVERSITY   (Italy)

^f ISTANBUL UNIVERSITY   (Turkey)

^g HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^h SORBONNE UNIVERSITÉ   (France)

ⁱ RAYMOND POINCARÉ HOSPITAL   (France)

^j MAASTRICHT UNIVERSITY   (Netherlands)

^k CYPRUS INSTITUTE OF NEUROLOGY AND GENETICS   (Cyprus)

^l MEDICAL UNIVERSITY OF WARSAW   (Poland)

^m UNIVERSITY OF BELGRADE   (Serbia)

ⁿ ULLEVÅL UNIVERSITY HOSPITAL   (Norway)

^o UNIVERSITY OF OSLO   (Norway)

^p HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^q CHARLES UNIVERSITY   (Czech Republic)

^r MARTIN LUTHER UNIVERSITÄT HALLE WITTENBERG   (Germany)

^s Tzartos NeuroDiagnostics   (Greece)

more..

Author keywords

Autoantibodies; Cell based assay; Diagnosis; MuSK; Myasthenia gravis

Indexed keywords

AUTOANTIBODY; AZATHIOPRINE; IMMUNOGLOBULIN; MUSK AUTOANTIBODY; PREDNISONE; PYRIDOSTIGMINE; UNCLASSIFIED DRUG; CHOLINERGIC RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; LRP4 PROTEIN, HUMAN; PROTEIN TYROSINE KINASE;

ADULT; ANTIBODY DETECTION; ARTICLE; CELL ASSAY; CELL BASED ASSAY; CLINICAL FEATURE; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; FEMALE; GOLD STANDARD; HUMAN; HUMAN CELL; IMMUNOPATHOLOGY; MAJOR CLINICAL STUDY; MALE; MULTIPLE SCLEROSIS; MYASTHENIA GRAVIS; MYELOOPTIC NEUROPATHY; NEUROIMMUNE DISEASE; NEUROLOGIC DISEASE; PRIORITY JOURNAL; RETROSPECTIVE STUDY; THYMUS HYPERPLASIA; TREATMENT RESPONSE; AGED; BLOOD; FLOW CYTOMETRY; IMMUNOLOGY; INTERNATIONAL COOPERATION; MIDDLE AGED; NEUROMYELITIS OPTICA; PATHOLOGY; RADIOIMMUNOASSAY; THYMUS;

ADULT; AGED; AUTOANTIBODIES; FEMALE; FLOW CYTOMETRY; HUMANS; INTERNATIONAL COOPERATION; LDL-RECEPTOR RELATED PROTEINS; MALE; MIDDLE AGED; MYASTHENIA GRAVIS; NEUROMYELITIS OPTICA; RADIOIMMUNOASSAY; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, CHOLINERGIC; THYMUS GLAND; THYMUS HYPERPLASIA;

EID: 84929849327     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2015.04.015     Document Type: Article

References (52)

1. Baggi F., Andreetta F., Maggi L., Confalonieri P., Morandi L., Salerno F., et al. Complete stable remission and autoantibody specificity in myasthenia gravis. Neurology 2013, 80:188-195.
2. Bartoccioni E., Scuderi F., Minicuci G.M., Marino M., Ciaraffa F., Evoli A. Anti-MuSK antibodies: correlation with myasthenia gravis severity. Neurology 2006, 67:505-507.
3. Bau V., Hanisch F., Hain B., Zierz S. Ocular involvement in MuSK antibody-positive myasthenia gravis. Klin. Monatsbl. Augenheilkd. 2006, 223:81-83.
4. Boneva N., Hamra-Amitay Y., Wirguin I., Brenner T. Stimulated-single fiber electromyography monitoring of anti-sense induced changes in experimental autoimmune myasthenia gravis. Neurosci. Res. 2006, 55:40-44.
5. Caress J.B., Hunt C.H., Batish S.D. Anti-MuSK myasthenia gravis presenting with purely ocular findings. Arch. Neurol. 2005, 62:1002-1003.
6. Chan J.W., Orrison W.W. Ocular myasthenia: a rare presentation with MuSK antibody and bilateral extraocular muscle atrophy. Br. J. Ophthalmol. 2007, 91:842-843.
7. Chang T., Leite M.I., Senanayake S., Gunaratne P.S., Gamage R., Riffsy M.T., et al. Clinical and serological study of myasthenia gravis using both radioimmunoprecipitation and cell-based assays in a South Asian population. J. Neurol. Sci. 2014, 343:82-87.
8. Devic P., Petiot P., Simonet T., Stojkovic T., Delmont E., Franques J., et al. Antibodies to clustered acetylcholine receptor: expanding the phenotype. Eur. J. Neurol. 2014, 21:130-134.
9. Evoli A., Padua L. Diagnosis and therapy of myasthenia gravis with antibodies to muscle-specific kinase. Autoimmun. Rev. 2013, 12:931-935.
10. Evoli A., Tonali P.A., Padua L., Monaco M.L., Scuderi F., Batocchi A.P., et al. Clinical correlates with anti-MuSK antibodies in generalized seronegative myasthenia gravis. Brain 2003, 126:2304-2311.
11. Evoli A., Bianchi M.R., Riso R., Minicuci G.M., Batocchi A.P., Servidei S., et al. Response to therapy in myasthenia gravis with anti-MuSK antibodies. Ann. N. Y. Acad. Sci. 2008, 1132:76-83.
12. Guptill J.T., Sanders D.B., Evoli A. Anti-MuSK antibody myasthenia gravis: clinical findings and response to treatment in two large cohorts. Muscle Nerve 2011, 44:36-40.
13. Hatanaka Y., Hemmi S., Morgan M.B., Scheufele M.L., Claussen G.C., Wolfe G.I., et al. Nonresponsiveness to anticholinesterase agents in patients with MuSK-antibody-positive MG. Neurology 2005, 65:1508-1509.
14. 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.
15. 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.
16. Huijbers M.G., Zhang W., Klooster R., Niks E.H., Friese M.B., Straasheijm K.R., et al. MuSK IgG4 autoantibodies cause myasthenia gravis by inhibiting binding between MuSK and Lrp4. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:20783-20788.
17. Jacob S., Viegas S., Leite M.I., Webster R., Cossins J., Kennett R., et al. Presence and pathogenic relevance of antibodies to clustered acetylcholine receptor in ocular and generalized myasthenia gravis. Arch. Neurol. 2012, 69:994-1001.
18. Koneczny I., Cossins J., Waters P., Beeson D., Vincent A. MuSK myasthenia gravis IgG4 disrupts the interaction of LRP4 with MuSK but both IgG4 and IgG1-3 can disperse preformed agrin-independent AChR clusters. PLoS One 2013, 8:e80695.
19. Kostera-Pruszczyk A., Kaminska A., Dutkiewicz M., Emeryk-Szajewska B., Strugalska-Cynowska M.H., Vincent A., et al. MuSK-positive myasthenia gravis is rare in the Polish population. Eur. J. Neurol. 2008, 15:720-724.
20. Lauriola L., Ranelletti F., Maggiano N., Guerriero M., Punzi C., Marsili F., et al. Thymus changes in anti-MuSK-positive and -negative myasthenia gravis. Neurology 2005, 64:536-538.
21. Lefvert A.K., Cuenoud S., Fulpius B.W. Binding properties and subclass distribution of anti-acetylcholine receptor antibodies in myasthenia gravis. J. Neuroimmunol. 1981, 1:125-135.
22. Leite M.I., Strobel P., Jones M., Micklem K., Moritz R., Gold R., et al. Fewer thymic changes in MuSK antibody-positive than in MuSK antibody-negative MG. Ann. Neurol. 2005, 57:444-448.
23. Leite M.I., Jacob S., Viegas S., Cossins J., Clover L., Morgan B.P., et al. IgG1 antibodies to acetylcholine receptors in 'seronegative' myasthenia gravis. Brain 2008, 131:1940-1952.
24. Leite M.I., Waters P., Vincent A. Diagnostic use of autoantibodies in myasthenia gravis. Autoimmunity 2010, 43:371-379.
25. Marx A., Pfister F., Schalke B., Saruhan-Direskeneli G., Melms A., Strobel P. The different roles of the thymus in the pathogenesis of the various myasthenia gravis subtypes. Autoimmun. Rev. 2013, 12:875-884.
26. McConville J., Farrugia M.E., Beeson D., Kishore U., Metcalfe R., Newsom-Davis J., et al. Detection and characterization of MuSK antibodies in seronegative myasthenia gravis. Ann. Neurol. 2004, 55:580-584.
27. Meriggioli M.N., Sanders D.B. Autoimmune myasthenia gravis: emerging clinical and biological heterogeneity. Lancet Neurol. 2009, 8:475-490.
28. Meriggioli M.N., Sanders D.B. Muscle autoantibodies in myasthenia gravis: beyond diagnosis?. Expert. Rev. Clin. Immunol. 2012, 8:427-438.
29. Niks E.H., Kuks J.B., Verschuuren J.J. Epidemiology of myasthenia gravis with anti-muscle specific kinase antibodies in The Netherlands. J. Neurol. Neurosurg. Psychiatry 2007, 78:417-418.
30. Niks E.H., van Leeuwen Y., Leite M.I., Dekker F.W., Wintzen A.R., Wirtz P.W., et al. Clinical fluctuations in MuSK myasthenia gravis are related to antigen-specific IgG4 instead of IgG1. J. Neuroimmunol. 2008, 195:151-156.
31. Oh S.J. Muscle-specific receptor tyrosine kinase antibody positive myasthenia gravis current status. J. Clin. Neurol. 2009, 5:53-64.
32. Ohta K., Shigemoto K., Kubo S., Maruyama N., Abe Y., Ueda N., et al. MuSK antibodies in AChR Ab-seropositive MG vs AChR Ab-seronegative MG. Neurology 2004, 62:2132-2133.
33. Pevzner A., Schoser B., Peters K., Cosma N.C., Karakatsani A., Schalke B., et al. Anti-LRP4 autoantibodies in AChR- and MuSK-antibody-negative myasthenia gravis. J. Neurol. 2012, 259:427-435.
34. Plested C.P., Tang T., Spreadbury I., Littleton E.T., Kishore U., Vincent A. AChR phosphorylation and indirect inhibition of AChR function in seronegative MG. Neurology 2002, 59:1682-1688.
35. Poulas K., Tsibri E., Kokla A., Papanastasiou D., Tsouloufis T., Marinou M., et al. Epidemiology of seropositive myasthenia gravis in Greece. J. Neurol. Neurosurg. Psychiatry 2001, 71:352-356.
36. Poulas K., Koutsouraki E., Kordas G., Kokla A., Tzartos S.J. Anti-MuSK- and anti-AChR-positive myasthenia gravis induced by d-penicillamine. J. Neuroimmunol. 2012, 250:94-98.
37. 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.
38. Rodriguez Cruz P.M., Huda S., Lopez-Ruiz P., Vincent A. Use of cell-based assays in myasthenia gravis and other antibody-mediated diseases. Exp. Neurol. 2015, 10.1016/j.expneurol.2015.01.011.
39. Sanders D.B., El-Salem K., Massey J.M., McConville J., Vincent A. Clinical aspects of MuSK antibody positive seronegative MG. Neurology 2003, 60:1978-1980.
40. Scuderi F., Marino M., Colonna L., Mannella F., Evoli A., Provenzano C., et al. Anti-p110 autoantibodies identify a subtype of "seronegative" myasthenia gravis with prominent oculobulbar involvement. Lab. Investig. 2002, 82:1139-1146.
41. Suzuki S., Utsugisawa K., Nagane Y., Satoh T., Kuwana M., Suzuki N. Clinical and immunological differences between early and late-onset myasthenia gravis in Japan. J. Neuroimmunol. 2011, 230:148-152.
42. Trakas N., Zisimopoulou P., Tzartos S.J. Development of a highly sensitive diagnostic assay for muscle-specific tyrosine kinase (MuSK) autoantibodies in myasthenia gravis. J. Neuroimmunol. 2011, 240-241:79-86.
43. Tsiamalos P., Kordas G., Kokla A., Poulas K., Tzartos S.J. Epidemiological and immunological profile of muscle-specific kinase myasthenia gravis in Greece. Eur. J. Neurol. 2009, 16:925-930.
44. Vincent A., Drachman D.B. Myasthenia gravis. Adv. Neurol. 2002, 88:159-188.
45. Vincent A., Bowen J., Newsom-Davis J., McConville J. Seronegative generalised myasthenia gravis: clinical features, antibodies, and their targets. Lancet Neurol. 2003, 2:99-106.
46. Vincent A., Leite M.I., Farrugia M.E., Jacob S., Viegas S., Shiraishi H., et al. Myasthenia gravis seronegative for acetylcholine receptor antibodies. Ann. N. Y. Acad. Sci. 2008, 1132:84-92.
47. Vincent A., Waters P., Leite M.I., Jacobson L., Koneczny I., Cossins J., et al. Antibodies identified by cell-based assays in myasthenia gravis and associated diseases. Ann. N. Y. Acad. Sci. 2012, 1274:92-98.
48. Yamamoto T., Vincent A., Ciulla T.A., Lang B., Johnston I., Newsom-Davis J. Seronegative myasthenia gravis: a plasma factor inhibiting agonist-induced acetylcholine receptor function copurifies with IgM. Ann. Neurol. 1991, 30:550-557.
49. Yang L., Maxwell S., Leite M.I., Waters P., Clover L., Fan X., et al. Non-radioactive serological diagnosis of myasthenia gravis and clinical features of patients from Tianjin, China. J. Neurol. Sci. 2011, 301:71-76.
50. Zhang B., Tzartos J.S., Belimezi M., Ragheb S., Bealmear B., Lewis R.A., et al. Autoantibodies to lipoprotein-related protein 4 in patients with double-seronegative myasthenia gravis. Arch. Neurol. 2012, 69:445-451.
51. Zisimopoulou P., Evangelakou P., Tzartos J., Lazaridis K., Zouvelou V., Mantegazza R., et al. A comprehensive analysis of the epidemiology and clinical characteristics of anti-LRP4 in myasthenia gravis. J. Autoimmun. 2013, 52:139-145.
52. Zouvelou V., Kyriazi S., Rentzos M., Belimezi M., Micheli M.A., Tzartos S.J., et al. Double-seropositive myasthenia gravis. Muscle Nerve 2013, 47:465-466.