Recombinant IgG1 Fc hexamers block cytotoxicity and pathological changes in experimental in vitro and rat models of neuromyelitis optica

Neuropharmacology

Volumn 133, Issue , 2018, Pages 345-353

  Tradtrantip, Lukmanee ^a   Felix, Christian M ^a   Spirig, Rolf ^b   Morelli, Adriana Baz ^c   Verkman, A S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CSL Behring AG   (Switzerland)

^c CSL LIMITED   (Australia)

Author keywords

AQP4; Astrocyte; Complement; Fc multimer; Immunoglobulin; Neuroinflammation; NMO

Indexed keywords

AQUAPORIN 4; AUTOANTIBODY; COMPLEMENT; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; RECOMBINANT PROTEIN; 5-(3-FERROCENECARBOXAMIDOPROPENYL-1) 2'-DEOXYURIDINE 5'-TRIPHOSPHATE; AQP4 PROTEIN, HUMAN; COMPLEMENT COMPONENT C1Q; DEOXYURIDINE PHOSPHATE; GLIAL FIBRILLARY ACIDIC PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; ASTROCYTE; CELL CULTURE; CELL DAMAGE; COMPLEMENT ACTIVATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEMYELINATION; DRUG POTENCY; FEMALE; INFLAMMATION; MYELOOPTIC NEUROPATHY; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RAT MODEL; SINGLE DRUG DOSE; SLICE CULTURE; SPINAL CORD SLICE; ANIMAL; CHEMISTRY; CHO CELL LINE; CRICETULUS; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECT; GENETIC TRANSFECTION; GENETICS; HUMAN; IMMUNOLOGY; IN VITRO STUDY; INTRAVENOUS DRUG ADMINISTRATION; METABOLISM; MUTATION; NONPARAMETRIC TEST; PATHOLOGY; SPINAL CORD; SPRAGUE DAWLEY RAT; TIME FACTOR;

ADMINISTRATION, INTRAVENOUS; ANIMALS; AQUAPORIN 4; ASTROCYTES; AUTOANTIBODIES; CHO CELLS; COMPLEMENT C1Q; CRICETULUS; DEOXYURACIL NUCLEOTIDES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; IN VITRO TECHNIQUES; MUTATION; NEUROMYELITIS OPTICA; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; SPINAL CORD; STATISTICS, NONPARAMETRIC; TIME FACTORS; TRANSFECTION;

EID: 85042124542     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2018.02.002     Document Type: Article

References (64)

1. Absoud, M., Brex, P., Ciccarelli, O., Diribe, O., Giovannoni, G., Hellier, J., Howe, R., Holland, R., Kelly, J., McCrone, P., Murphy, C., Palace, J., Pickles, A., Pike, M., Robertson, N., Jacob, A., Lim, M., A multicentre randomiSed controlled TRial of IntraVEnous immunoglobulin compared with standard therapy for the treatment of transverse myelitis in adults and children (STRIVE). Health Technol. Assess. 21 (2017), 1–50.
2. Adrichem, M.E., Starink, M.V., van leeuwen, E.M., Kramer, C., van Schaik, I.N., Eftimou, F., Drug-induced cutaneous lupus erythematosus after immunoglobulin treatment in chronic inflammatory demyelinating polyneuropathy: a case series. J. Peripher. Nerv. Syst. 22 (2017), 213–218.
3. Anthony, R.M., Nimmerjahn, F., Ashline, D.J., Reinhold, V.N., Paulson, J.C., Ravetch, J.V., Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc. Science 320 (2008), 373–376.
4. Araki, M., Matsuoka, T., Miyamoto, K., Kusunoki, S., Okamoto, T., Murata, M., Miyake, S., Aranami, T., Yamamura, T., Efficacy of the anti-IL-6 receptor antibody tocilizumab in neuromyelitis optica: a pilot study. Neurology 82 (2014), 1302–1306.
5. Asavapanumas, N., Ratelade, J., Verkman, A.S., Unique neuromyelitis optica pathology produced in naive rats by intracerebral administration of NMO-IgG. Acta Neuropathol. 127 (2014), 539–551.
6. Asgari, N., Khorooshi, R., Lillevang, S.T., Owens, T., Complement-dependent pathogenicity of brain-specific antibodies in cerebrospinal fluid. J. Neuroimmunol. 254 (2013), 76–82.
7. Bakker, J., Metz, L., Devic's neuromyelitis optica treated with intravenous gamma globulin (IVIG). Can. J. Neurol. Sci. 31 (2004), 265–267.
8. Bennett, J.L., Lam, C., Kalluri, S.R., Saikali, P., Bautista, K., Dupree, C., Glogowska, M., Case, D., Antel, J.P., Owens, G.P., Gilden, D., Nessler, S., Stradelmann, C., Hemmer, B., Intrathecal pathogenic anti-aquaporin-4 antibodies in early neuromyelitis optica. Ann. Neurol. 66 (2009), 617–629.
9. Berger, M., McCallus, D.E., Lin, C.S., Rapid and reversible responses to IVIG in autoimmune neuromuscular diseases suggest mechanisms of action involving competition with functionally important autoantibodies. J. Peripher. Nerv. Syst. 18 (2013), 275–296.
10. Botto, M., c1q knock-out mice for the study of complement deficiency in autoimmune disease. Exp. Clin. Immunogent 15 (1998), 231–234.
11. Chaigne, B., Mouthon, L., Mechanisms of action of intravenous immunoglobulin. Transfus. Apher. Sci. 56 (2017), 45–49.
12. Crane, J.M., Lam, C., Rossi, A., Gupta, T., Bennett, J.L., Verkman, A.S., Binding affinity and specificity of neuromyelitis optica autoantibodies to aquaporin-4 M1/M23 isoforms and orthogonal arrays. J. Biol. Chem. 286 (2011), 16516–16524.
13. Cree, B.A., Lamb, S., Morgan, K., Chen, A., Waubant, E., Genain, C., An open label study of the effects of rituximab in neuromyelitis optica. Neurology 64 (2005), 1270–1272.
14. Czajkowsky, D.M., Anderson, J.T., Fuchs, A., Wilson, T.J., Mekhaiel, D., Colonna, M., He, J., Shao, Z., Mitchell, D.A., Wu, G., Dell, A., Haslam, S., Lloy, K.A., Moore, S.C., Sandlie, I., Blundell, P.A., Pleass, R.J., Developing the IVIG biomimetic, Hexa-Fc, for drug and vaccine applications. Sci. Rep., 5, 2015, 9526.
15. Dalakas, M.C., The use of intravenous immunoglobulin in the treatment of autoimmune neuromuscular diseases: evidence-based indications and safety profile. Pharmacol. Ther. 102 (2004), 177–193.
16. Elsone, L., Panicker, J., Mutch, K., Boggild, M., Appleton, R., Jacob, A., Role of intravenous immunoglobulin in the treatment of acute relapses of neuromyelitis optica: experience in 10 patients. Mult. Scler. 20 (2014), 501–504.
17. Ephrem, A., Chamat, S., Miquel, C., Fisson, S., Mouthon, L., Caligiuri, G., Delignat, S., Elluru, S., Bayry, J., Lacroix-Desmazes, S., Cohen, J.L., Salomon, B.L., Kazatchkine, M.D., Kaveri, S.V., Misra, N., Expansion of CD4+CD25+ regulatory T cells by intravenous immunoglobulin: a critical factor in controlling experimental autoimmune encephalomyelitis. Blood 111 (2008), 715–722.
18. Esen, F., Senturk, E., Ozcan, P.E., Ahishali, B., Arican, N., Orhan, N., Ekizoglu, O., Kucuk, M., Kaya, M., Intravenous immunoglobulins prevent the breakdown of the blood-brain barrier in experimentally induced sepsis. Crit. Care Med. 40 (2012), 1214–1220.
19. Galeotti, C., Bayry, J., Kone-Paut, I., Kaveri, S.V., Kawasaki disease: aetiopathogenesis and therapeutic utility of intravenous immunoglobulin. Autoimmun. Rev. 9 (2010), 441–448.
20. Gelfand, E.W., Intravenous immune globulin in autoimmune and inflammatory diseases. N. Engl. J. Med. 367 (2012), 2015–2025.
21. Graber, D.J., Levy, M., Kerr, D., Wade, W.F., Neuromyelitis optica pathogenesis and aquaporin 4. J. Neuroinflam, 5, 2008, 22.
22. Greenberg, B.M., Graves, D., Remington, G., Hardeman, P., Mann, M., Karendikar, N., Stuve, O., Monson, N., Frohman, E., Rituximab dosing and monitoring strategies in neuromyelitis optica patients: creating strategies for therapeutic success. Mult. Scler. 18 (2012), 1022–1026.
23. Grünewald, B., Bennett, J.L., Toyka, K.V., Sommer, C., Geis, C., Efficacy of polyvalent Human immunoglobulins in an animal model of neuromyelitis optica evoked by intrathecal anti-aquaporin 4 antibodies. Int. J. Mol. Sci., 2016 https://doi.org/10.3390/ijms17091407.
24. Hengstman, G.J., Wesseling, P., Frenken, C.W., Jongen, P.J., Neuromyelitis optica with clinical and histopathological involvement of the brain. Mult. Scler. 13 (2007), 679–682.
25. Imbach, P., Barandun, S., d'Apuzzo, V., Baumgartner, C., Hirt, A., Morell, A., Rossi, E., Schöni, M., Vest, M., Wagner, H.P., High-dose intravenous gammaglobulin for idiopathic thrombocytopenic purpura in childhood. Lancet 1 (1981), 1228–1231.
26. Jacob, S., Rajabally, Y.A., Current proposed mechanisms of action of intravenous immunoglobulins in inflammatory neuropathies. Curr. Neuropharmacol. 7 (2009), 337–342.
27. Jain, A., Olsen, H.S., Vyzasatya, R., Burch, E., Sakoda, Y., Mérigeon, E.Y., Cai, L., Lu, C., Tan, M., Tamada, K., Schulze, D., Block, D.S., Strome, S.E., Fully recombinant IgG2a Fc multimers (stradomers) effectively treat collagen-induced arthritis and prevent idiopathic thrombocytopenic purpura in mice. Arthritis Res., 14, 2012, R192.
28. Jarius, S., Wildemann, B., AQP4 antibodies in neuromyelitis optica: diagnostic and pathogenetic relevance. Nat. Rev. Neurol. 6 (2010), 383–392.
29. Jarius, S., Wildemann, B., Paul, F., Neuromyelitis optica: clinical features, immunopathogenesis and treatment. Clin. Exp. Immunol. 176 (2014), 149–164.
30. Kageyama, T., Komori, M., Miyamoto, K., Ozaki, A., Suenaga, T., Takahashi, R., Matsumoto, S., Kondo, T., Combination of cyclosporin A with corticosteroids is effective for the treatment of neuromyelitis optica. J. Neurol. 260 (2013), 627–634.
31. Katz-Agranov, N., Khattri, S., Zandman-Goddard, G., The role of intravenous immunoglobulin in the treatment of rheumatoid arthritis. Autoimmun. Rev. 14 (2015), 651–658.
32. Lennon, V.A., Kryzer, T.J., Pittock, S.J., Verkman, A.S., Hinson, S.R., IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J. Exp. Med. 202 (2005), 473–477.
33. Li, N., Zhao, M., Hilario-Vargas, J., Prisayanh, P., Warren, S., Diaz, L.A., Roopenian, D.C., Liu, Z., Complete FcRn dependence for intravenous Ig therapy in autoimmune skin blistering diseases. J. Clin. Invest. 115 (2005), 3440–3450.
34. Lin, H.H., Wang, M.X., Spies, J.M., Pollard, J.D., Effective treatment of experimental autoimmune neuritis with Fc fragment of human immunoglobulin. J. Neuroimmunol. 186 (2007), 133–140.
35. Lucchinetti, C.F., Mandler, R.N., McGavern, D., Bruck, W., Gleich, G., Ransohoff, R.M., Trebst, C., Weinshenker, B.G., Wingerchuk, D.M., Parisi, J.E., Lassmann, H., A role for humoral mechanisms in the pathogenesis of Devic's neuromyelitis optica. Brain 125 (2002), 1450–1461.
36. Lünemann, J.D., Nimmerjahn, F., Dalakas, M.C., Intravenous immunoglobulin in neurology-mode of action and clinical efficacy. Nat. Rev. Neurol. 11 (2015), 80–89.
37. Magraner, M.J., Coret, F., Casanova, B., The effect of intravenous immunoglobulin on neuromyelitis optica. Neurologia 28 (2013), 65–72.
38. Misu, T., Fujihara, K., Kakita, A., Konno, H., Nakamura, M., Watanabe, S., Takahashi, T., Nakashima, I., Takahashi, H., Itoyama, Y., Loss of aquaporin 4 in lesions of neuromyelitis optica: distinction from multiple sclerosis. Brain 130 (2007), 1224–1234.
39. Nguyen, D.H., Cho, N., Satkunendrarajah, K., Austin, J.W., Wang, J., Fehlings, M.G., Immunoglobulin G (IgG) attenuates neuroinflammation and improves neurobehavioral recovery after cervical spinal cord injury. J. Neuroinflam, 9, 2012, 224.
40. Niknami, M., Wang, M.X., Nguyen, T., Pollard, J.D., Beneficial effect of a multimerized immunoglobulin Fc in an animal model of inflammatory neuropathy (experimental autoimmune neuritis). J. Peripher. Nerv. Syst. 18 (2013), 141–152.
41. Okada, K., Tsuji, S., Tanaka, K., Intermittent intravenous immunoglobulin successfully prevents relapses of neuromyelitis optica. Intern. Med 46 (2007), 1671–1672.
42. Ortiz, D.R., Lansing, J.C., Rutitzky, L., Kurtegic, E., Prod'homme, T., Choudhury, A., Elucidating the interplay between IgG-Fc valency and FcγR activation for the design of immune complex inhibitors. Sci. Transl. Med., 8, 2016 365ra158.
43. Papadopoulos, M.C., Bennett, J.L., Verkman, A.S., Treatment of neuromyelitis optica: state-of-the-art and emerging therapies. Nat. Rev. Neurol. 10 (2014), 493–506.
44. Papadopoulos, M.C., Verkman, A.S., Aquaporin 4 and neuromyelitis optica. Lancet Neurol. 11 (2012), 535–544.
45. Parratt, J.D., Prineas, J.W., Neuromyelitis optica: a demyelinating disease characterized by acute destruction and regeneration of a perivascular astrocytes. Mult. Scler. 16 (2010), 1156–1172.
46. Phuan, P.W., Zhang, H., Asavapanumas, N., Leviten, M., Rosenthal, A., Tradtrantip, L., Verkman, A.S., C1q-targeted monoclonal antibody prevents complement-dependent cytotoxicity and neuropathology in in vitro and mouse models of neuromyelitis optica. Acta Neuropathol. 125 (2013), 829–840.
47. Piepers, S., Jansen, M.D., Cats, E.A., van Sorge, N.M., van den Berg, L.H., van der Pol, W.L., IVIg inhibits classical pathway activity and anti-GM1 IgM-mediated complement deposition in MMN. J. Neuroimmunol. 229 (2010), 256–262.
48. Pittock, S.J., Lennon, V.A., McKeon, A., Mandrekar, J., Weinshenker, B.G., Lucchinetti, C.F., O'Toole, O., Wingerchuk, D.M., Eculizumab in AQP4-IgG-positive relapsing neuromyelitis optica spectrum disorders: an open-label pilot study. Lancet Neurol. 12 (2013), 554–562.
49. Ratelade, J., Smith, A.J., Verkman, A.S., Human immunoglobulin G reduces the pathogenicity of aquaporin-4 autoantibodies in neuromyelitis optica. Exp. Neurol. 225 (2014), 145–153.
50. Ratelade, J., Verkman, A.S., Inhibitor(s) of the classical complement pathway in mouse serum limit the utility of mice as experimental models of neuromyelitis optica. Mol. Immunol. 62 (2014), 103–114.
51. Schwab, I., Nimmerjahn, F., Intravenous immunoglobulin therapy: how does IgG modulate the immune system?. Nat. Rev. Immunol. 13 (2013), 176–189.
52. Sorensen, V., Sundvold, V., Michaelsen, T.E., Sandlie, I., Polymerization of IgA and IgM: role of Cys309/Cys414 and the secretory tailpiece. J. Immunol. 162 (1999), 3448–3455.
53. Spirig, R., Campbell, I.K., Koernig, S., Chen, C.G., Lewis, B.J.B., Butcher, R., Muir, I., Taylor, S., Chia, J., Leong, D., Simmonds, J., Scotney, P., Schmidt, P., Fabri, L., Hofmann, A., Jordi, M., Spycher, M.O., Cattepoel, S., Brasseit, J., Panousis, C., Rowe, T., Branch, D.R., Morelli, A.B., Käsermann, F., Zuercher, A.W., Unique rIgG1 Fc hexamers inhibit antibody-mediated disease via complement and FcgRs. [Submitted].
54. Thiruppathi, M., Sheng, J.R., Li, L., Prabhakar, B.S., Meriggioli, M.N., Recombinant IgG2a Fc (M045) multimers effectively suppress experimental autoimmune myasthenia gravis. J. Autoimmun. 52 (2014), 64–73.
55. Tradtrantip, L., Zhang, H., Saadoun, S., Phuan, P.W., Lam, C., Papadopoulos, M.C., Bennett, J.L., Verkman, A.S., Anti-aquaporin-4 monoclonal antibody blocker therapy for neuromyelitis optica. Ann. Neurol. 71 (2012), 314–322.
56. Verkman, A.S., Phuan, P.W., Asavapanumas, N., Tradtrantip, L., Biology of AQP4 and anti-AQP4 antibody: therapeutic implications for NMO. Brain Pathol. 23 (2013), 84–695.
57. Viswanathan, S., Wong, A.H., Quek, A.M., Yuki, N., Intravenous immunoglobulin may reduce relapse frequency in neuromyelitis optica. J. Neuroimmunol. 282 (2015), 92–96.
58. Weishaupt, A., Kuhlmann, T., Schonrock, L.M., Toyka, K.V., Bruck, W., Gold, R., Effects of intravenous immunoglobulins on T cell and oligodendrocyte apoptosis in high-dose antigen therapy in experimental autoimmune encephalomyelitis. Acta Neuropathol. 104 (2002), 385–390.
59. Wingerchuk, D.M., Neuromyelitis optica: potential roles for intravenous immunoglobulin. J. Clin. Immunol. 33:Suppl. 1 (2013), S33–S37.
60. Winkelmann, A., Zettl, U.K., Use of intravenous immunoglobulin in the treatment of immune-mediated demyelinating diseases of the nervous system. Curr. Pharm. Des 18 (2012), 4570–4582.
61. Yao, X., Verkman, A.S., Marked central nervous system pathology in CD59 knockout rats following passive transfer of neuromyelitis optica immunoglobulin G. Acta Neurolpathol. Commun, 5, 2017, 15.
62. Yuki, N., Watanabe, H., Nakajima, T., Spath, P.J., IVIG blocks complement deposition mediated by anti-GM1 antibodies in multifocal motor neuropathy. J. Neurol. Neurosurg. Psychiatry 82 (2011), 87–91.
63. Yusa, S., Catina, T.L., Campbell, K.S., SHP-1- and phosphotyrosine-independent inhibitory signaling by a killer cell Ig-like receptor cytoplasmic domain in human NK cells. J. Immunol. 168 (2002), 5047–5057.
64. Zhang, H., Bennett, J.L., Verkman, A.S., Ex vivo spinal cord slice model of neuromyelitis optica reveals novel immunopathogenic mechanisms. Ann. Neurol. 70 (2011), 943–954.