Recent approaches to the development of antigen-specific immunotherapies for myasthenia gravis

References

• Vincent A. Unravelling the pathogenesis of myasthenia gravis. Nat Rev Immunol. 2002; 2:797–804.
   PubMed Web of Science ®Google Scholar
• 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 3: 365–368.
   PubMed Web of Science ®Google Scholar
• Lindstrom JM, Seybold ME, Lennon VA, Whittingham S, Duane DD. Antibody to acetylcholine receptor in myasthenia gravis. Prevalence, clinical correlates, and diagnostic value. Neurology. 1976; 26:1054–1059.
   PubMed Web of Science ®Google Scholar
• Lang B, Newsom-Davis J, Prior C, Wray D. Antibodies to motor nerve terminals: An electrophysiological study of a human myasthenic syndrome transferred to mouse. J Physiol. 1983; 344:335–345.
   PubMed Web of Science ®Google Scholar
• Mossman S, Vincent A, Newsom-Davis J. Passive transfer of myasthenia gravis by immunoglobulins: Lack of correlation between AChR with antibody bound, acetylcholine receptor loss and transmission defect. J Neurol Sci. 1988; 84:15–28.
   Google Scholar
• Engel AG, Sahashi K, Fumagalli G. The immunopathology of acquired myasthenia gravis. Ann N Y Acad Sci. 1981; 377:158–174.
   Google Scholar
• Pinching AJ, Peters DK, Newsom-Davis J. Remission of myasthenia gravis following plasma-exchange. Lancet. 1976; 2:1373–1376.
   PubMed Web of Science ®Google Scholar
• Patrick J, Lindstrom J. Autoimmune response to acetylcholine receptor. Science. 1973; 180:871–872.
   PubMed Web of Science ®Google Scholar
• 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 1–2: 107–117.
   Google Scholar
• Tzartos S, Hochschwender S, Vasquez P, Lindstrom J. Passive transfer of experimental autoimmune myasthenia gravis by monoclonal antibodies to the main immunogenic region of the acetylcholine receptor. J Neuroimmunol. 1987; 15:185–194.
   PubMed Web of Science ®Google Scholar
• Tzartos SJ, Bitzopoulou K, Gavra I, Kordas G, Jacobson L, Kostelidou K, Lagoumintzis G, Lazos O, Poulas K, Sideris S, Sotiriadis A, Trakas N, Zisimopoulou P. Antigen-specific apheresis of pathogenic autoantibodies from myasthenia gravis sera. Ann N Y Acad Sci. 2008; 1132:291–299.
   PubMed Web of Science ®Google Scholar
• Kaminski HJ. Treatment of myasthenia gravisIn: Current Clinical Neurology: Myasthenia gravis and Related Disorders. New York: Humana Press; 2003. 197–221.
   Google Scholar
• Fostieri E, Kostelidou K, Poulas K, Tzartos SJ. Recent advances in the understanding and therapy of myasthenia gravis. Future Neurol. 2006; 1:799–801.
   Google Scholar
• Chiu HC, Chen WH, Yeh JH. The six year experience of plasmapheresis in patients with myasthenia gravis. Ther Apher. 2000; 4:291–295.
   Google Scholar
• Yeh JH, Chiu HC. Comparison between double-filtration plasmapheresis and immunoadsorption plasmapheresis in the treatment of patients with myasthenia gravis. J Neurol. 2000; 247 7: 510–513.
   PubMed Web of Science ®Google Scholar
• Gajdos P, Outin HD, Morel E, Raphael JC, Goulon M. High-dose intravenous gamma globulin for myasthenia gravis: Analternative to plasmaexchange. Ann N Y Acad Sci. 1987; 505:842–844.
   Google Scholar
• Ferrero B, Durelli L, Cavallo R, Dutto A, Aimo G, Pecchio F, Bergamasco B. Therapies for exacerbation of myasthenia gravis. The mechanism of action of intravenous high-dose immunoglobulin G. Ann N Y Acad Sci. 1993; 681:563–566.
   Google Scholar
• Dalakas MC. Intravenous immunoglobulin in autoimmune neuromuscular diseases. JAMA. 2004; 291:2367–2375.
   PubMed Web of Science ®Google Scholar
• Brannagan THIII, Nagle KJ, Lange DJ, Rowland LP. Complications of intravenous immune globulin treatment in neurologic disease. Neurology. 1996; 47 3: 674–677.
   Google Scholar
• Kazatchkine MD, Kaveri SV. Immunomodulation of autoimmune and inflammatory diseases with intravenous immuneglobulin. N Engl J Med. 2001; 345:747–755.
   PubMed Web of Science ®Google Scholar
• Dalakas MC. Immunotherapies in the treatment of neuromuscular disorders. Neuromuscular disorders in clinical practice. Boston: Butterworth Heinemann; 2002. 364–383.
   Google Scholar
• Verschuuren JJ, Graus YM, Tzartos JS, van Breda Vriesman PJ, De Baets MH. Paratope- and framework-related cross-reactive idiotopes on anti-acetylcholine receptor antibodies. J Immunol. 1991; 146 3: 941–948.
   Google Scholar
• Souroujon MC, Pachner AR, Fuchs S. The treatment of passively transferred experimental myasthenia with anti-idiotypic antibodies. Neurology. 1986; 36 5: 622–625.
   PubMed Web of Science ®Google Scholar
• Wang ZY, Qiao J, Link H. Suppression of experimental autoimmune myasthenia gravis by oral administration of acetylcholine receptor. J Neuroimmunol. 1993; 44 2: 209–214.
   PubMed Web of Science ®Google Scholar
• Im SH, Barchan D, Maiti PK, Raveh L, Souroujon MC, Fuchs S. Suppression of experimental myasthenia gravis, a B cell-mediated autoimmune disease, by blockade of IL-18. FASEB J. 2001; 15 12: 2140–2148.
   PubMed Web of Science ®Google Scholar
• Wu JM, Wu B, Miagkov A, Adams RN, Drachman DB. Specific immunotherapy of experimental myasthenia gravis in vitro: The “guided missile” strategy. Cell Immunol. 2001; 208 2: 137–147.
   Google Scholar
• Psaridi-Linardaki L, Trakas N, Mamalaki A, Tzartos SJ. Specific immunoadsorption of the autoantibodies from myasthenic patients using the extracellular domain of the human muscle acetylcholine receptor alpha-subunit. Development of an antigen-specific therapeutic strategy. J Neuroimmunol. 2005; 159:183–191.
   PubMed Web of Science ®Google Scholar
• Kostelidou K, Trakas N, Tzartos SJ. Extracellular domains of the beta, gamma and epsilon subunits of the human acetylcholine receptor as immunoadsorbents for myasthenic autoantibodies: A combination of immunoadsorbents results in increased efficiency. J Neuroimmunol. 2007; 190 1–2: 44–52.
   Google Scholar
• Zisimopoulou P, Lagoumintzis G, Poulas K, Tzartos S. Antigen-specific apheresis of human anti-acetylcholine receptor autoantibodies from myasthenia gravis patients' sera using Escherichia coli-expressed receptor domains. J Neuroimmunol. 2008; 200 1–2: 133–141.
   PubMed Web of Science ®Google Scholar
• Fostieri E, Tzartos SJ, Berrih-Aknin S, Beeson D, Mamalaki A. Isolation of potent human Fab fragments against a novel highly immunogenic region on human muscle acetylcholine receptor which protect the receptor from myasthenic autoantibodies. Eur J Immunol. 2005; 35 2: 632–643.
   Google Scholar
• Mamalaki A, Trakas N, Tzartos SJ. Bacterial expression of a single-chain Fv fragment which efficiently protects the acetylcholine receptor against antigenic modulation caused by myasthenic antibodies. Eur J Immunol. 1993; 23 8: 1839–1845.
   Google Scholar
• Papanastasiou D, Mamalaki A, Eliopoulos E, Poulas K, Liolitsas C, Tzartos SJ. Construction and characterization of a humanized single chain Fv antibody fragment against the main immunogenic region of the acetylcholine receptor. J Neuroimmunol. 1999; 94 1–2: 182–195.
   PubMed Web of Science ®Google Scholar
• Tsantili P, Tzartos SJ, Mamalaki A. High affinity single-chain Fv antibody fragments protecting the human nicotinic acetylcholine receptor. J Neuroimmunol. 1999; 94 1–2: 15–27.
   Google Scholar
• Sophianos D, Tzartos SJ. Fab fragments of monoclonal antibodies protect the human acetylcholine receptor against antigenic modulation caused by myasthenic sera. J Autoimmun. 1989; 2 6: 777–789.
   Google Scholar
• Papanastasiou D, Poulas K, Kokla A, Tzartos SJ. Prevention of passively transferred experimental autoimmune myasthenia gravis by Fab fragments of monoclonal antibodies directed against the main immunogenic region of the acetylcholine receptor. J Neuroimmunol. 2000; 104 2: 124–132.
   PubMed Web of Science ®Google Scholar
• Protopapadakis E, Kokla A, Tzartos SJ, Mamalaki A. Isolation and characterization of human anti-acetylcholine receptor monoclonal antibodies from transgenic mice expressing human immunoglobulin loci. Eur J Immunol. 2005; 35 6: 1960–1968.
   PubMed Web of Science ®Google Scholar
• Meng F, Stassen MH, Schillberg S, Fischer R, De Baets MH. Construction and characterization of a single-chain antibody fragment derived from thymus of a patient with myasthenia gravis. Autoimmunity. 2002; 35:125–133.
   Web of Science ®Google Scholar
• Graus YF, de Baets MH, van Breda Vriesman PJ, Burton DR. Anti-acetylcholine receptor Fab fragments isolated from thymus-derived phage display libraries from myasthenia gravis patients reflect predominant specificities in serum and block the action of pathogenic serum antibodies. Immunol Lett. 1997; 57 1–3: 59–62.
   Google Scholar
• van der Neut Kolfschoten M, Schuurman J, Losen M, Bleeker WK, Martínez-Martínez P, Vermeulen E, den Bleker TH, Wiegman L, Vink T, Aarden LA, De Baets MH, van de Winkel JG, Aalberse RC, Parren PW. Anti-inflammatory activity of human IgG4 antibodies by dynamic Fab arm exchange. Science. 2007; 317 5844: 1554–1557.
   PubMed Web of Science ®Google Scholar
• Karlin A. Emerging structure of the nicotinic acetylcholine receptors. Nat Rev Neurosci. 2002; 3:102–114.
   PubMed Web of Science ®Google Scholar
• Psaridi-Linardaki L, Mamalaki A, Remoundos M, Tzartos SJ. Expression of soluble ligand and antibody-binding extracellular domain of human muscle acetylcholine receptor alpha subunit in yeast Pichia pastoris. Role of glycosylation in alpha-bungarotoxin binding. J Biol Chem. 2002; 277:26980–26986.
   Google Scholar
• Kostelidou K, Trakas N, Zouridakis M, Bitzopoulou K, Sotiriadis A, Gavra I, Tzartos SJ. Expression and characterization of soluble forms of the extracellular domains of the beta, gamma and epsilon subunits of the human muscle acetylcholine receptor. FEBS J. 2006; 273:3557–3568.
   Google Scholar
• Bitzopoulou K, Kostelidou K, Poulas K, Tzartos SJ. Mutant forms of the extracellular domain of the human acetylcholine receptor-subunit with improved solubility and enhanced antigenicity. The importance of the Cys-loop. Biochim Biophys Acta. 2008; 1784 9: 1226–1233.
   Google Scholar
• Zouridakis M, Kostelidou K, Sotiriadis A, Stergiou C, Eliopoulos E, Poulas K, Tzartos SJ. Circular dichroism studies of extracellular domains of human nicotinic acetylcholine receptors provide an insight into their structure. Int J Biol Macromol. 2007; 41:423–429.
   Google Scholar
• Brejc K, van Dijk WJ, Klaassen RV, Schuurmans M, van Der Oost J, Smit AB, Sixma TK. Crystal structure of an ACh-binding protein reveals the ligand binding domain of nicotinic receptors. Nature. 2001; 411:269–276.
   PubMed Web of Science ®Google Scholar
• Unwin N. Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J Mol Biol. 2005; 346:967–989.
   PubMed Web of Science ®Google Scholar
• Yamazaki Z, Fujimori Y, Takahama T, Inoue N, Wada T, Kazama M, Morioka M, Abe T, Yamawaki N, Inagaki K. Efficiency and biocompatibility of a new immunosorbent. Trans Am Soc Artif Intern Organs. 1982; 28:318–323.
   PubMedGoogle Scholar
• Matic G, Winkler RE, Tiess M, Ramlow W. Selective apheresis- time for a change. Int J Artif Organs. 2001; 24:4–7.
   Google Scholar
• Ptak J. Changes of plasma proteins after immunoadsorption using Ig-Adsopak columns in patients with myasthenia gravis. Transfus Apher Sci. 2004; 30 2: 125–129.
   Google Scholar
• Takamori M, Maruta T. Immunoadsorption in myasthenia gravis based on specific ligands mimicking the immunogenic sites of the acetylcholine receptor. Therap Apher. 2001; 5:340–350.
   PubMedGoogle Scholar
• Guo CY, Li ZY, Xu MQ, Yuan JM. Preparation of an immunoadsorbent coupled with a recombinant antigen to remove anti-acetylcholine receptor antibodies in abnormal serum. J Immunol Meth. 2005; 303:142–147.
   PubMed Web of Science ®Google Scholar
• Lindstrom J, Campbell M, Nave B. Specificities of antibodies to acetylcholine receptors. Muscle Nerve. 1978; 1:140–145.
   PubMed Web of Science ®Google Scholar
• Loutrari H, Tzartos SJ, Claudio T. Use of Torpedo-mouse hybrid acetylcholine receptors reveals immunodominance of the alpha subunit in myasthenia gravis antisera. Eur J Immunol. 1992; 22:2949–2956.
   Google Scholar
• Psaridi-Linardaki L, Mamalaki A, Tzartos SJ. Future therapeutic strategies in autoimmune myasthenia gravis. Ann N Y Acad Sci. 2003; 998:539–548.
   Google Scholar
• Burnouf T, Eber M, Kientz D, Cazenave JP, Burkhardt T. Assessment of complement activation during membrane-based plasmapheresis procedures. J Clin Apher. 2004; 19 3: 142–147.
   Google Scholar
• Kalamida D, Poulas K, Avramopoulou V, Fostieri E, Lagoumintzis G, Lazaridis K, Sideri A, Zouridakis M, Tzartos SJ. Muscle and neuronal nicotinic acetylcholine receptors. Structure, function and pathogenicity. FEBS J. 2007; 274 15: 3799–3845.
   PubMed Web of Science ®Google Scholar
• Loutrari H, Kokla A, Tzartos SJ. Passive transfer of experimental myasthenia gravis via antigenic modulation of acetylcholine receptor. Eur J Immunol. 1992; 22 9: 2449–2452.
   PubMed Web of Science ®Google Scholar
• Vincent A. Aetiological factors in development of myasthenia gravis. Adv Neuroimmunol. 1994; 4 4: 355–371.
   Google Scholar
• Tzartos SJ, Sophianos D, Efthimiadis A. Role of the main immunogenic region of acetylcholine receptor in myasthenia gravis. An Fab monoclonal antibody protects against antigenic modulation by human sera. J Immunol. 1985; 134 4: 2343–2349.
   Google Scholar
• Tzartos SJ, Barkas T, Cung MT, Mamalaki A, Marraud M, Orlewski P, Papanastasiou D, Sakarellos C, Sakarellos-Daitsiotis M, Tsantili P, Tsikaris V. Anatomy of the antigenic structure of a large membrane autoantigen, the muscle-type nicotinic acetylcholine receptor. Immunol Rev. 1998; 163:89–120.
   PubMed Web of Science ®Google Scholar
• Tzartos SJ, Lindstrom JM. Monoclonal antibodies used to probe acetylcholine receptor structure: Localization of the main immunogenic region and detection of similarities between subunits. Proc Natl Acad Sci USA. 1980; 77 2: 755–759.
   Google Scholar
• Tzartos SJ, Seybold ME, Lindstrom JM. Specificities of antibodies to acetylcholine receptors in sera from myasthenia gravis patients measured by monoclonal antibodies. Proc Natl Acad Sci. 1982; 79 1: 188–192.
   Google Scholar
• Heidenreich F, Vincent A, Willcox N, Newsom-Davis J. Anti-acetylcholine receptor antibody specificities in serum and in thymic cell culture supernatants from myasthenia gravis patients. Neurology. 1988; 38 11: 1784–1788.
   Google Scholar
• Lennon VA, Griesmann GE. Evidence against acetylcholine receptor having a main immunogenic region as target for autoantibodies in myasthenia gravis. Neurology. 1989; 39 8: 1069–1076.
   Google Scholar
• Trakas N, Tzartos SJ. Conjugation of acetylcholine receptor-protecting Fab fragments with polyethylene glycol results in a prolonged half-life in the circulation and reduced immunogenicity. J Neuroimmunol. 2001; 120 1–2: 42–49.
   Google Scholar
• Farrar J, Portolano S, Willcox N, Vincent A, Jacobson L, Newsom-Davis J, Rapoport B, McLachlan SM. Diverse Fab specific for acetylcholine receptor epitopes from a myasthenia gravis thymus combinatorial library. Int Immunol. 1997; 9 9: 1311–1318.
   Google Scholar
• Schuurman J, Van Ree R, Perdok GJ, Van Doorn HR, Tan KY, Aalberse RC. Normal human immunoglobulin G4 is bispecific: It has two different antigen-combining sites. Immunology. 1999; 97 4: 693–698.
   Google Scholar
• Aalberse RC, Schuurman J. IgG4 breaking the rules. Immunology. 2002; 105 1: 9–19.
   PubMed Web of Science ®Google Scholar