Neutralization and clearance of GM-CSF by autoantibodies in pulmonary alveolar proteinosis

Nature Communications

Volumn 6, Issue , 2015, Pages

  Piccoli, Luca ^a,b   Campo, Ilaria ^c   Fregni, Chiara Silacci ^a   Rodriguez, Blanca Maria Fernandez ^a   Minola, Andrea ^a   Sallusto, Federica ^a   Luisetti, Maurizio ^c   Corti, Davide ^a,d   Lanzavecchia, Antonio ^a,b  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

^d Humabs Biomed SA ^*  (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; EPITOPE; FC RECEPTOR; NEUTRALIZING ANTIBODY;

ANTIBODY; ANTIGEN; BIOASSAY; BIOAVAILABILITY; DEGRADATION; MUTATION; NEUTRALIZATION; PHENOTYPE; PROTEIN; RODENT;

ANIMAL EXPERIMENT; ANTIGEN ANTIBODY COMPLEX; ANTIGEN SPECIFICITY; ARTICLE; BIOASSAY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG ALVEOLUS PROTEINOSIS; MOUSE; NONHUMAN; PROTEIN DEGRADATION; SOMATIC MUTATION; ADULT; AGED; ANIMAL; AUTOIMMUNE DISEASE; BAGG ALBINO MOUSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOLOGY; MALE; MIDDLE AGED; TUMOR CELL LINE;

MUS;

ADULT; AGED; ANIMALS; ANTIBODIES, NEUTRALIZING; AUTOANTIBODIES; AUTOIMMUNE DISEASES; CELL LINE, TUMOR; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPES; FEMALE; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; IN VITRO TECHNIQUES; MALE; MICE; MICE, INBRED BALB C; MIDDLE AGED; PULMONARY ALVEOLAR PROTEINOSIS; RECEPTORS, IGG;

EID: 84935857724     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8375     Document Type: Article

References (38)

1. Watanabe, M., Uchida, K., Nakagaki, K., Trapnell, B. C. & Nakata, K. High avidity cytokine autoantibodies in health and disease: pathogenesis and mechanisms. Cytokine Growth Factor Rev. 21, 263-273 (2010).
2. Puel, A. et al. Autoantibodies against IL-17A, IL-17F, and IL-22 in patients with chronic mucocutaneous candidiasis and autoimmune polyendocrine syndrome type I. J. Exp. Med. 207, 291-297 (2010).
3. Madariaga, L. et al. Detection of anti-interferon-gamma autoantibodies in subjects infected by Mycobacterium tuberculosis. Int. J. Tuberc. Lung Dis. 2, 62-68 (1998).
4. Patel, S. Y. et al. Anti-IFN-gamma autoantibodies in disseminated nontuberculous mycobacterial infections. J. Immunol. 175, 4769-4776 (2005).
5. Trapnell, B. C., Carey, B. C., Uchida, K. & Suzuki, T. Pulmonary alveolar proteinosis, a primary immunodeficiency of impaired GM-CSF stimulation of macrophages. Curr. Opin. Immunol. 21, 514-521 (2009).
6. Casadevall, N. et al. Pure red-cell aplasia and antierythropoietin antibodies in patients treated with recombinant erythropoietin. New Engl. J. Med. 346, 469-475 (2002).
7. Sergeeva, A., Ono, Y., Rios, R. & Molldrem, J. J. High titer autoantibodies to GM-CSF in patients with AML, CML and MDS are associated with active disease. Leukemia 22, 783-790 (2008).
8. Sethu, S. et al. Immunoglobulin G1 and immunoglobulin G4 antibodies in multiple sclerosis patients treated with IFNbeta interact with the endogenous cytokine and activate complement. Clin. Immunol. 148, 177-185 (2013).
9. Pohl, M. A., Rivera, J., Nakouzi, A., Chow, S. K. & Casadevall, A. Combinations of monoclonal antibodies to anthrax toxin manifest new properties in neutralization assays. Infect. Immun. 81, 1880-1888 (2013).
10. Chen, C. et al. Potent neutralization of botulinum neurotoxin/B by synergistic action of antibodies recognizing protein and ganglioside receptor binding domain. PLoS ONE 7, e43845 (2012).
11. Nowakowski, A. et al. Potent neutralization of botulinum neurotoxin by recombinant oligoclonal antibody. Proc. Natl Acad. Sci. USA 99, 11346-11350 (2002).
12. Montero-Julian, F. A., Gautherot, E., Wijdenes, J., Klein, B. & Brailly, H. Pharmacokinetics of interleukin-6 during therapy with anti-interleukin-6 monoclonal antibodies: enhanced clearance of interleukin-6 by a combination of three anti-interleukin-6 antibodies. J. Interferon Res. 14, 301-302 (1994).
13. Boyman, O., Kovar, M., Rubinstein, M. P., Surh, C. D. & Sprent, J. Selective stimulation of T cell subsets with antibody-cytokine immune complexes. Science 311, 1924-1927 (2006).
14. Shibata, Y. et al. GM-CSF regulates alveolar macrophage differentiation and innate immunity in the lung through PU.1. Immunity 15, 557-567 (2001).
15. Uchida, K. et al. GM-CSF autoantibodies and neutrophil dysfunction in pulmonary alveolar proteinosis. New Engl. J. Med. 356, 567-579 (2007).
16. Sakagami, T. et al. Human GM-CSF autoantibodies and reproduction of pulmonary alveolar proteinosis. New Engl. J. Med. 361, 2679-2681 (2009).
17. Uchida, K. et al. High-affinity autoantibodies specifically eliminate granulocytemacrophage colony-stimulating factor activity in the lungs of patients with idiopathic pulmonary alveolar proteinosis. Blood 103, 1089-1098 (2004).
18. Wang, Y. et al. Characterization of pathogenic human monoclonal autoantibodies against GM-CSF. Proc. Natl Acad. Sci. USA 110, 7832-7837 (2013).
19. Traggiai, E. et al. An efficient method to make human monoclonal antibodies from memory B cells: potent neutralization of SARS coronavirus. Nat. Med. 10, 871-875 (2004).
20. Lefranc, M. P. et al. IMGT, the international ImMunoGeneTics information system. Nucleic Acids Res. 37, D1006-D1012 (2009).
21. Uchida, K. et al. Granulocyte/macrophage-colony-stimulating factor autoantibodies and myeloid cell immune functions in healthy subjects. Blood 113, 2547-2556 (2009).
22. Krinner, E. M. et al. A human monoclonal IgG1 potently neutralizing the pro-inflammatory cytokine GM-CSF. Mol. Immunol. 44, 916-925 (2007).
23. Steidl, S., Ratsch, O., Brocks, B., Durr, M. & Thomassen-Wolf, E. In vitro affinity maturation of human GM-CSF antibodies by targeted CDR-diversification. Mol. Immunol. 46, 135-144 (2008).
24. Niu, L., Heaney, M. L., Vera, J. C. & Golde, D. W. High-affinity binding to the GM-CSF receptor requires intact N-glycosylation sites in the extracellular domain of the beta subunit. Blood 95, 3357-3362 (2000).
25. Hansen, G. et al. The structure of the GM-CSF receptor complex reveals a distinct mode of cytokine receptor activation. Cell 134, 496-507 (2008).
26. Behrens, F. et al. MOR103, a human monoclonal antibody to granulocytemacrophage colony-stimulating factor, in the treatment of patients with moderate rheumatoid arthritis: results of a phase Ib/IIa randomised, double-blind, placebo-controlled, dose-escalation trial. Ann. Rheum. Dis. 74, 1058-1064 (2014).
27. Respaud, R., Vecellio, L., Diot, P. & Heuze-Vourc'h, N. Nebulization as a delivery method for mAbs in respiratory diseases. Expert Opin. Drug Deliv. 12, 1027-1039 (2015).
28. Tabrizi, M., Bornstein, G. G. & Suria, H. Biodistribution mechanisms of therapeutic monoclonal antibodies in health and disease. AAPS J. 12, 33-43 (2010).
29. Di Zenzo, G. et al. Pemphigus autoantibodies generated through somatic mutations target the desmoglein-3 cis-interface. J. Clin. Invest. 122, 3781-3790 (2012).
30. Mietzner, B. et al. Autoreactive IgG memory antibodies in patients with systemic lupus erythematosus arise from nonreactive and polyreactive precursors. Proc. Natl Acad. Sci. USA 105, 9727-9732 (2008).
31. Schroeder, K., Herrmann, M. & Winkler, T. H. The role of somatic hypermutation in the generation of pathogenic antibodies in SLE. Autoimmunity 46, 121-127 (2013).
32. Corti, D. et al. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333, 850-856 (2011).
33. Corti, D. et al. Cross-neutralization of four paramyxoviruses by a human monoclonal antibody. Nature 501, 439-443 (2013).
34. Pappas, L. et al. Rapid development of broadly influenza neutralizing antibodies through redundant mutations. Nature 516, 418-422 (2014).
35. Lin, R. H., Mamula, M. J., Hardin, J. A. & Janeway, Jr. C. A. Induction of autoreactive B cells allows priming of autoreactive T cells. J. Exp. Med. 173, 1433-1439 (1991).
36. Dabritz, J. et al. Granulocyte macrophage colony-stimulating factor autoantibodies and disease relapse in inflammatory bowel disease. Am. J. Gastroenterol. 108, 1901-1910 (2013).
37. Kitamura, T. et al. Serological diagnosis of idiopathic pulmonary alveolar proteinosis. Am. J. Respir. Crit. Care Med. 162, 658-662 (2000).
38. Inoue, Y. et al. Characteristics of a large cohort of patients with autoimmune pulmonary alveolar proteinosis in Japan. Am. J. Respir. Crit. Care Med. 177, 752-762 (2008).