In vitro characterization of an acetylcholine receptor–transferrin fusion protein for the treatment of myasthenia gravis

References

• Conti-Fine BM, Milani M, Kaminski HJ. Myasthenia gravis: Past, present, and future. J Clin Invest. 2006; 116:2843–2854.
   PubMed Web of Science ®Google Scholar
• Sahashi K, Engel AG, Lambert EH, Howard FMJr. Ultrastructural localization of the terminal and lytic ninth complement component (C9) at the motor end-plate in myasthenia gravis. J Neuropathol Exp Neurol. 1980; 39:160–172.
   PubMed Web of Science ®Google Scholar
• Lennon VA, Seybold ME, Lindstrom JM, Cochrane C, Ulevitch R. Role of complement in the pathogenesis of experimental autoimmune myasthenia gravis. J Exp Med. 1978; 147:973–983.
   PubMedGoogle Scholar
• Biesecker G, Gomez CM. Inhibition of acute passive transfer experimental autoimmune myasthenia gravis with Fab antibody to complement C6. J Immunol. 1989; 142:2654–2659.
   PubMed Web of Science ®Google Scholar
• Vincent A, Leite MI. Neuromuscular junction autoimmune disease: Muscle specific kinase antibodies and treatments for myasthenia gravis. Curr Opin Neurol. 2005; 18:519–525.
   PubMed Web of Science ®Google Scholar
• Vincent A, McConville J, Farrugia ME, Newsom-Davis J. Seronegative myasthenia gravis. Semin Neurol. 2004; 24:125–133.
   PubMed Web of Science ®Google Scholar
• Abramsky O, Brenner T, Lisak RP, Zeidman A, Beyth Y. Significance in neonatal myasthenia gravis of inhibitory effect of amniotic fluid on binding of antibodies to acetylcholine receptor. Lancet. 1979; 2:1333–1335.
   PubMedGoogle Scholar
• Donaldson JO, Penn AS, Lisak RP, Abramsky O, Brenner T, Schotland DL. Antiacetylcholine receptor antibody in neonatal myasthenia gravis. Am J Dis Child. 1981; 135:222–226.
   PubMedGoogle Scholar
• Newsom-Davis J, Pinching AJ, Vincent A, Wilson SG. Function of circulating antibody to acetylcholine receptor in myasthenia gravis: Investigation by plasma exchange. Neurology. 1978; 28:266–272.
   PubMed Web of Science ®Google Scholar
• Christadoss P, Poussin M, Deng C. Animal models of myasthenia gravis. Clin Immunol. 2000; 94:75–87.
   PubMed Web of Science ®Google Scholar
• Garcia-Carrasco M, Escarcega RO, Fuentes-Alexandro S, Riebeling C, Cervera R. Therapeutic options in autoimmune myasthenia gravis. Autoimmun Rev. 2007; 6:373–378.
   PubMed Web of Science ®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; 274:3799–3845.
   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; 190:44–52.
   PubMedGoogle Scholar
• Loutrari H, Kokla A, Trakas N, Tzartos SJ. Expression of human-Torpedo hybrid acetylcholine receptor (AChR) for analysing the subunit specificity of antibodies in sera from patients with myasthenia gravis (MG). Clin Exp Immunol. 1997; 109:538–546.
   PubMed Web of Science ®Google Scholar
• Sideris S, Lagoumintzis G, Kordas G, Kostelidou K, Sotiriadis A, Poulas K, Tzartos SJ. Isolation and functional characterization of anti-acetylcholine receptor subunit-specific autoantibodies from myasthenic patients: Receptor loss in cell culture. J Neuroimmunol. 2007; 189:111–117.
   PubMedGoogle 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 NY Acad Sci. 2008; 1132:291–299.
   PubMed Web of Science ®Google Scholar
• Barchan D, Asher O, Tzartos SJ, Fuchs S, Souroujon MC. Modulation of the anti-acetylcholine receptor response and experimental autoimmune myasthenia gravis by recombinant fragments of the acetylcholine receptor. Eur J Immunol. 1998; 28:616–624.
   PubMed Web of Science ®Google Scholar
• Bleil JD, Bretscher MS. Transferrin receptor and its recycling in HeLa cells. EMBO J. 1982; 1:351–355.
   PubMed Web of Science ®Google Scholar
• Lamb JE, Ray F, Ward JH, Kushner JP, Kaplan J. Internalization and subcellular localization of transferrin and transferrin receptors in HeLa cells. J Biol Chem. 1983; 258:8751–8758.
   PubMed Web of Science ®Google Scholar
• Sager PR, Brown PA, Berlin RD. Analysis of transferrin recycling in mitotic and interphase HeLa cells by quantitative fluorescence microscopy. Cell. 1984; 39:275–282.
   PubMed Web of Science ®Google Scholar
• Chan C, Sandhu J, Guha A, Scollard DA, Wang J, Chen P, Bai K, Lee L, Reilly RM. A human transferrin–vascular endothelial growth factor (hnTf-VEGF) fusion protein containing an integrated binding site for (111)In for imaging tumor angiogenesis. J Nucl Med. 2005; 46:1745–1752.
   PubMedGoogle Scholar
• Hall WA. Targeted toxin therapy for malignant astrocytoma. Neurosurgery. 2000; 46:544–551 discussion 552.
   PubMed Web of Science ®Google Scholar
• Debinski W. Local treatment of brain tumors with targeted chimera cytotoxic proteins. Cancer Invest. 2002; 20:801–809.
   PubMed Web of Science ®Google Scholar
• Razzini G, Parise F, Calebiro D, Battini R, Bagni B, Corazzari T, Tarugi P, Angelelli C, Molinari S, Falqui L, Ferrari S. Low-density lipoprotein (LDL) receptor/transferrin fusion protein: In vivo production and functional evaluation as a potential therapeutic tool for lowering plasma LDL cholesterol. Hum Gene Ther. 2004; 15:533–541.
   PubMedGoogle Scholar
• Bai Y, Ann DK, Shen WC. Recombinant granulocyte colony-stimulating factor-transferrin fusion protein as an oral myelopoietic agent. Proc Natl Acad Sci USA. 2005; 102:7292–7296.
   PubMed Web of Science ®Google Scholar
• Lim CJ, Shen WC. Comparison of monomeric and oligomeric transferrin as potential carrier in oral delivery of protein drugs. J Control Rel. 2005; 106:273–286.
   PubMed Web of Science ®Google Scholar
• Shin SU, Friden P, Moran M, Olson T, Kang YS, Pardridge WM, Morrison SL. Transferrin-antibody fusion proteins are effective in brain targeting. Proc Natl Acad Sci USA. 1995; 92:2820–2824.
   PubMed Web of Science ®Google Scholar
• Rainov NG, Soling A. Clinical studies with targeted toxins in malignant glioma. Rev Rec Clin Trials. 2006; 1:119–131.
   PubMedGoogle Scholar
• Park E, Starzyk RM, McGrath JP, Lee T, George J, Schutz AJ, Lynch P, Putney SD. Production and characterization of fusion proteins containing transferrin and nerve growth factor. J Drug Target. 1998; 6:53–64.
   PubMed Web of Science ®Google Scholar
• Osborn MJ, McElmurry RT, Peacock B, Tolar J, Blazar BR. Targeting of the CNS in MPS-IH using a nonviral transferrin-alpha-l-iduronidase fusion gene product. Mol Ther. 2008; 16:1459–1466.
   PubMed Web of Science ®Google Scholar
• Beeson D, Jacobson L, Newsom-Davis J, Vincent A. A transfected human muscle cell line expressing the adult subtype of the human muscle acetylcholine receptor for diagnostic assays in myasthenia gravis. Neurology. 1996; 47:1552–1555.
   PubMed Web of Science ®Google Scholar
• Lindstrom J, Einarson B, Tzartos S. Production and assay of antibodies to acetylcholine receptors. Meth Enzymol. 1981; 74 Pt C: 432–460.
   PubMedGoogle Scholar
• Tsouloufis T, Mamalaki A, Remoundos M, Tzartos SJ. Reconstitution of conformationally dependent epitopes on the N-terminal extracellular domain of the human muscle acetylcholine receptor alpha subunit expressed in Escherichia coli: Implications for myasthenia gravis therapeutic approaches. Int Immunol. 2000; 12:1255–1265.
   PubMedGoogle Scholar
• Hradilek A, Neuwirt J. Iron uptake by MOLT 3 cells from transferrin/monoclonal antitransferrin antibody complexes. Br J Haematol. 1986; 62:21–30.
   PubMedGoogle Scholar
• Tzartos SJ, Kokla A, Walgrave SL, Conti-Tronconi BM. Localization of the main immunogenic region of human muscle acetylcholine receptor to residues 67–76 of the alpha subunit. Proc Natl Acad Sci USA. 1988; 85:2899–2903.
   PubMed Web of Science ®Google Scholar
• Venkatesh N, Im SH, Balass M, Fuchs S, Katchalski-Katzir E. Prevention of passively transferred experimental autoimmune myasthenia gravis by a phage library-derived cyclic peptide. Proc Natl Acad Sci USA. 2000; 97:761–766.
   PubMedGoogle Scholar
• Chen W, Feng Y, Chen D, Wandinger-Ness A. Rab11 is required for trans-golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor. Mol Biol Cell. 1998; 9:3241–3257.
   PubMedGoogle Scholar
• Ren M, Xu G, Zeng J, De Lemos-Chiarandini C, Adesnik M, Sabatini DD. Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc Natl Acad Sci USA. 1998; 95:6187–6192.
   PubMed Web of Science ®Google Scholar
• Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG. Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol. 1996; 135:913–924.
   PubMed Web of Science ®Google Scholar
• Rohrer J, Schweizer A, Russell D, Kornfeld S. The targeting of Lamp1 to lysosomes is dependent on the spacing of its cytoplasmic tail tyrosine sorting motif relative to the membrane. J Cell Biol. 1996; 132:565–576.
   PubMed Web of Science ®Google Scholar
• Jones KL, Stewart RM, Fowler M, Fukuda M, Holcombe RF. Chediak–Higashi lymphoblastoid cell lines: Granule characteristics and expression of lysosome-associated membrane proteins. Clin Immunol Immunopathol. 1992; 65:219–226.
   PubMedGoogle Scholar
• Keefe D, Hess D, Bosco J, Tzartos S, Powell J, Lamsa J, Josiah S. A rapid, fluorescence-based assay for detecting antigenic modulation of the acetylcholine receptor on human cell lines. Cytom B Clin Cytom. 2008; 76 3: 206–212.
   Google Scholar
• Beroukhim R, Unwin N. Three-dimensional location of the main immunogenic region of the acetylcholine receptor. Neuron. 1995; 15:323–331.
   PubMedGoogle 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; 134:2343–2349.
   PubMed Web of Science ®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
• Sophianos D, Tzartos SJ. Fab fragments of monoclonal antibodies protect the human acetylcholine receptor against antigenic modulation caused by myasthenic sera. J Autoimmun. 1989; 2:777–789.
   PubMed Web of Science ®Google Scholar
• Kumari S, Borroni V, Chaudhry A, Chanda B, Massol R, Mayor S, Barrantes FJ. Nicotinic acetylcholine receptor is internalized via a Rac-dependent, dynamin-independent endocytic pathway. J Cell Biol. 2008; 181:1179–1193.
   PubMedGoogle Scholar
• Bruneau E, Sutter D, Hume RI, Akaaboune M. Identification of nicotinic acetylcholine receptor recycling and its role in maintaining receptor density at the neuromuscular junction in vivo. J Neurosci. 2005; 25:9949–9959.
   PubMedGoogle Scholar
• Bruneau EG, Akaaboune M. The dynamics of recycled acetylcholine receptors at the neuromuscular junction in vivo. Development. 2006; 133:4485–4493.
   PubMedGoogle Scholar