Topical application of human-derived Ig isotypes for the control of acute respiratory infection evaluated in a human CD89-expressing mouse model.


Journal

Mucosal immunology
ISSN: 1935-3456
Titre abrégé: Mucosal Immunol
Pays: United States
ID NLM: 101299742

Informations de publication

Date de publication:
07 2019
Historique:
received: 26 11 2018
accepted: 27 03 2019
revised: 11 03 2019
pubmed: 21 5 2019
medline: 11 4 2020
entrez: 21 5 2019
Statut: ppublish

Résumé

Recurrent and persistent airway infections remain prevalent in patients with primary immunodeficiency (PID), despite restoration of serum immunoglobulin levels by intravenous or subcutaneous plasma-derived IgG. We investigated the effectiveness of different human Ig isotype preparations to protect mice against influenza when delivered directly to the respiratory mucosa. Four polyvalent Ig preparations from pooled plasma were compared: IgG, monomeric IgA (mIgA), polymeric IgA-containing IgM (IgAM) and IgAM associated with the secretory component (SIgAM). To evaluate these preparations, a transgenic mouse expressing human FcαRI/CD89 within the myeloid lineage was created. CD89 was expressed on all myeloid cells in the lung and blood except eosinophils, reflecting human CD89 expression. Intranasal administration of IgA-containing preparations was less effective than IgG in reducing pulmonary viral titres after infection of mice with A/California/7/09 (Cal7) or the antigenically distant A/Puerto Rico/8/34 (PR8) viruses. However, IgA reduced weight loss and inflammatory mediator expression. Both IgG and IgA protected mice from a lethal dose of PR8 virus and for mIgA, this effect was partially CD89 dependent. Our data support the beneficial effect of topically applied Ig purified from pooled human plasma for controlling circulating and non-circulating influenza virus infections. This may be important for reducing morbidity in PID patients.

Identifiants

pubmed: 31105268
doi: 10.1038/s41385-019-0167-z
pii: S1933-0219(22)00279-3
pmc: PMC7746524
doi:

Substances chimiques

Antibodies, Neutralizing 0
Antigens, CD 0
Cytokines 0
Fc(alpha) receptor 0
Immunoglobulin A 0
Immunoglobulin Isotypes 0
Receptors, Fc 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1013-1024

Références

Bonilla, F. A. et al. Practice parameter for the diagnosis and management of primary immunodeficiency. J. Allergy Clin. Immunol. 136, 1186–1205–e1181-1178 (2015).
doi: 10.1016/j.jaci.2015.04.049
Picard, C. et al. Primary immunodeficiency diseases: an update on the classification from the International Union of Immunological Societies Expert Committee for primary immunodeficiency 2015. J. Clin. Immunol. 35, 696–726 (2015).
doi: 10.1007/s10875-015-0201-1
Jolles, S. Subclinical infection and dosing in primary immunodeficiencies. Clin. Exp. Immunol. 178(Suppl. 1), 67–69 (2014).
doi: 10.1111/cei.12516
Kainulainen, L., Vuorinen, T., Rantakokko-Jalava, K., Osterback, R. & Ruuskanen, O. Recurrent and persistent respiratory tract viral infections in patients with primary hypogammaglobulinemia. J. Allergy Clin. Immunol. 126, 120–126 (2010).
doi: 10.1016/j.jaci.2010.04.016
Peltola, V., Waris, M., Kainulainen, L., Kero, J. & Ruuskanen, O. Virus shedding after human rhinovirus infection in children, adults and patients with hypogammaglobulinaemia. Clin. Microbiol Infect. 19, E322–E327 (2013).
doi: 10.1111/1469-0691.12193
Hart, T. K. et al. Preclinical efficacy and safety of mepolizumab (SB-240563), a humanized monoclonal antibody to IL-5, in cynomolgus monkeys. J. Allergy Clin. Immunol. 108, 250–257 (2001).
doi: 10.1067/mai.2001.116576
Dall’Acqua, W. F., Kiener, P. A. & Wu, H. Properties of human IgG1s engineered for enhanced binding to the neonatal Fc receptor (FcRn). J. Biol. Chem. 281, 23514–23524 (2006).
doi: 10.1074/jbc.M604292200
Ramisse, F. et al. Effective prophylaxis of influenza A virus pneumonia in mice by topical passive immunotherapy with polyvalent human immunoglobulins or F(ab’)2 fragments. Clin. Exp. Immunol. 111, 583–587 (1998).
doi: 10.1046/j.1365-2249.1998.00538.x
Gonzalez-Quintela, A. et al. Serum levels of immunoglobulins (IgG, IgA, IgM) in a general adult population and their relationship with alcohol consumption, smoking and common metabolic abnormalities. Clin. Exp. Immunol. 151, 42–50 (2008).
doi: 10.1111/j.1365-2249.2007.03545.x
Longet, S. et al. Human plasma-derived polymeric IgA and IgM antibodies associate with secretory component to yield biologically active secretory-like antibodies. J. Biol. Chem. 288, 4085–4094 (2013).
doi: 10.1074/jbc.M112.410811
Longet, S. et al. Reconstituted human polyclonal plasma-derived secretory-like IgM and IgA maintain the barrier function of epithelial cells infected with an enteropathogen. J. Biol. Chem. 289, 21617–21626 (2014).
doi: 10.1074/jbc.M114.549139
Hong, D. K., Tremoulet, A. H., Burns, J. C. & Lewis, D. B. Cross-reactive neutralizing antibody against pandemic 2009 H1N1 influenza a virus in intravenous immunoglobulin preparations. Pediatr. Infect. Dis. J. 30, 67–69 (2011).
doi: 10.1097/INF.0b013e3181f127be
Rockman, S. et al. Intravenous immunoglobulin protects against severe pandemic influenza infection. EBioMedicine 19, 119–127 (2017).
doi: 10.1016/j.ebiom.2017.04.010
Jegaskanda, S. et al. Cross-reactive influenza-specific antibody-dependent cellular cytotoxicity in intravenous immunoglobulin as a potential therapeutic against emerging influenza viruses. J. Infect. Dis. 210, 1811–1822 (2014).
doi: 10.1093/infdis/jiu334
Monteiro, R. C. & Van De Winkel, J. G. IgA Fc receptors. Annu. Rev. Immunol. 21, 177–204 (2003).
doi: 10.1146/annurev.immunol.21.120601.141011
Wilson, T. J., Fuchs, A. & Colonna, M. Cutting edge: human FcRL4 and FcRL5 are receptors for IgA and IgG. J. Immunol. 188, 4741–4745 (2012).
doi: 10.4049/jimmunol.1102651
Bidgood, S. R., Tam, J. C., McEwan, W. A., Mallery, D. L. & James, L. C. Translocalized IgA mediates neutralization and stimulates innate immunity inside infected cells. Proc. Natl Acad. Sci. USA 111, 13463–13468 (2014).
doi: 10.1073/pnas.1410980111
van Egmond, M. et al. Human immunoglobulin A receptor (FcalphaRI, CD89) function in transgenic mice requires both FcR gamma chain and CR3 (CD11b/CD18). Blood 93, 4387–4394 (1999).
doi: 10.1182/blood.V93.12.4387
van Egmond, M. et al. FcalphaRI-positive liver Kupffer cells: reappraisal of the function of immunoglobulin A in immunity. Nat. Med. 6, 680–685 (2000).
doi: 10.1038/76261
Stewart, W. W. & Kerr, M. A. The specificity of the human neutrophil IgA receptor (Fc alpha R) determined by measurement of chemiluminescence induced by serum or secretory IgA1 or IgA2. Immunology 71, 328–334 (1990).
pubmed: 2269470 pmcid: 1384427
Bakema, J. E. & van Egmond, M. The human immunoglobulin A Fc receptor FcalphaRI: a multifaceted regulator of mucosal immunity. Mucosal Immunol. 4, 612–624 (2011).
doi: 10.1038/mi.2011.36
Monteiro, R. C. Immunoglobulin A as an anti-inflammatory agent. Clin. Exp. Immunol. 178, 108–110 (2014).
doi: 10.1111/cei.12531
Wu, J. et al. Fc RI (CD89) alleles determine the proinflammatory potential of serum IgA. J. Immunol. 178, 3973–3982 (2007).
doi: 10.4049/jimmunol.178.6.3973
Maillet, A. et al. The airways, a novel route for delivering monoclonal antibodies to treat lung tumors. Pharm. Res. 28, 2147–2156 (2011).
doi: 10.1007/s11095-011-0442-5
Bioley, G. et al. Plasma-derived polyreactive secretory-like IgA and IgM opsonizing Salmonella enterica typhimurium reduces invasion and gut tissue inflammation through agglutination. Front. Immunol. 8, 1043 (2017).
doi: 10.3389/fimmu.2017.01043
Launay, P. et al. Fcalpha receptor (CD89) mediates the development of immunoglobulin A (IgA) nephropathy (Berger’s disease). Evidence for pathogenic soluble receptor-Iga complexes in patients and CD89 transgenic mice. J. Exp. Med. 191, 1999–2009 (2000).
doi: 10.1084/jem.191.11.1999
Xu, L. et al. Critical role of Kupffer cell CD89 expression in experimental IgA nephropathy. PloS ONE 11, e0159426 (2016).
doi: 10.1371/journal.pone.0159426
Pasquier, B. et al. Identification of FcalphaRI as an inhibitory receptor that controls inflammation: dual role of FcRgamma ITAM. Immunity 22, 31–42 (2005).
pubmed: 15664157
Jackson, R. J. The current status of vertebrate cellular mRNA IRESs. Cold Spring Harb. Perspect. Biol. 5, a011569 (2013).
doi: 10.1101/cshperspect.a011569
Pommerenke, C. et al. Global transcriptome analysis in influenza-infected mouse lungs reveals the kinetics of innate and adaptive host immune responses. PloS ONE 7, e41169 (2012).
doi: 10.1371/journal.pone.0041169
Kanamaru, Y. et al. Inhibitory ITAM signaling by Fc RI-FcR chain controls multiple activating responses and prevents renal inflammation. J. Immunol. 180, 2669–2678 (2008).
doi: 10.4049/jimmunol.180.4.2669
Kelton, W. et al. IgGA: a “cross-isotype” engineered human Fc antibody domain that displays both IgG-like and IgA-like effector functions. Chem. Biol. 21, 1603–1609 (2014).
doi: 10.1016/j.chembiol.2014.10.017
He, W. et al. Alveolar macrophages are critical for broadly-reactive antibody-mediated protection against influenza A virus in mice. Nat. Commun. 8, 846 (2017).
doi: 10.1038/s41467-017-00928-3
Shaykhiev, R. et al. Smoking-dependent reprogramming of alveolar macrophage polarization: implication for pathogenesis of chronic obstructive pulmonary disease. J. Immunol. 183, 2867–2883 (2009).
doi: 10.4049/jimmunol.0900473
Lindh, E. Increased risistance of immunoglobulin A dimers to proteolytic degradation after binding of secretory component. J. Immunol. 114, 284–286 (1975).
pubmed: 1090649
Renegar, K. B., Jackson, G. D. & Mestecky, J. In vitro comparison of the biologic activities of monoclonal monomeric IgA, polymeric IgA, and secretory IgA. J. Immunol. 160, 1219–1223 (1998).
pubmed: 9570537
Ye, J. et al. Intranasal delivery of an IgA monoclonal antibody effective against sublethal H5N1 influenza virus infection in mice. Clin. Vaccin Immunol. 17, 1363–1370 (2010).
doi: 10.1128/CVI.00002-10
Rossato, E. et al. Reversal of arthritis by human monomeric IgA through the receptor-mediated SH2 domain-containing phosphatase 1 inhibitory pathway. Arthritis Rheum. 67, 1766–1777 (2015).
doi: 10.1002/art.39142
Misharin, A. V., Morales-Nebreda, L., Mutlu, G. M., Budinger, G. R. & Perlman, H. Flow cytometric analysis of macrophages and dendritic cell subsets in the mouse lung. Am. J. Respir. Cell Mol. Biol. 49, 503–510 (2013).
doi: 10.1165/rcmb.2013-0086MA

Auteurs

Sandra Koernig (S)

CSL Limited, Bio21 Institute, 30 Flemington Rd, Parkville, VIC, 3010, Australia. sandra.koernig@csl.com.au.

Ian K Campbell (IK)

CSL Limited, Bio21 Institute, 30 Flemington Rd, Parkville, VIC, 3010, Australia.

Charley Mackenzie-Kludas (C)

Department of Microbiology and Immunology The Peter Doherty Institute for Infection and Immunity, The University of Melbourne, 792 Elizabeth St, Melbourne, VIC, 3000, Australia.

Alexander Schaub (A)

CSL Behring AG, Wankdorfstrasse 10, 3010, Bern, Switzerland.

Marius Loetscher (M)

CSL Behring AG, Wankdorfstrasse 10, 3010, Bern, Switzerland.

Wy Ching Ng (W)

Department of Microbiology and Immunology The Peter Doherty Institute for Infection and Immunity, The University of Melbourne, 792 Elizabeth St, Melbourne, VIC, 3000, Australia.

Roland Zehnder (R)

CSL Behring AG, Wankdorfstrasse 10, 3010, Bern, Switzerland.

Pawel Pelczar (P)

Center for Transgenic Models, Mattenstrasse 22, 4002, Basel, Switzerland.

Ildem Sanli (I)

Center for Transgenic Models, Mattenstrasse 22, 4002, Basel, Switzerland.

Monther Alhamdoosh (M)

CSL Limited, Bio21 Institute, 30 Flemington Rd, Parkville, VIC, 3010, Australia.

Milica Ng (M)

CSL Limited, Bio21 Institute, 30 Flemington Rd, Parkville, VIC, 3010, Australia.

Lorena E Brown (LE)

Department of Microbiology and Immunology The Peter Doherty Institute for Infection and Immunity, The University of Melbourne, 792 Elizabeth St, Melbourne, VIC, 3000, Australia.

Fabian Käsermann (F)

CSL Behring AG, Wankdorfstrasse 10, 3010, Bern, Switzerland.

Cédric Vonarburg (C)

CSL Behring AG, Wankdorfstrasse 10, 3010, Bern, Switzerland.

Adrian W Zuercher (AW)

CSL Behring AG, Wankdorfstrasse 10, 3010, Bern, Switzerland. adrian.zuercher@cslbehring.com.

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