A Functional Role for Antibodies in Tuberculosis

Cell - Tập 167 - Trang 433-443.e14 - 2016
Lenette L. Lu1,2, Amy W. Chung1,3, Tracy R. Rosebrock2, Musie Ghebremichael1, Wen Han Yu1,4, Patricia S. Grace1, Matthew K. Schoen1, Fikadu Tafesse1, Constance Martin2, Vivian Leung2, Alison E. Mahan1, Magdalena Sips1,5, Manu P. Kumar4, Jacquelynne Tedesco1, Hannah Robinson1, Elizabeth Tkachenko1, Monia Draghi1, Katherine J. Freedberg1, Hendrik Streeck6, Todd J. Suscovich1
1Ragon Institute of MGH, MIT, and Harvard, Cambridge, MA 02139, USA
2Department of Immunology and Infectious Diseases, Harvard School of Public Health, Boston, MA 02115, USA
3Department of Microbiology and Immunology, Doherty Institute for Infection and Immunity, University of Melbourne, Melbourne, VIC 3000, Australia
4Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA 02142, USA
5Department of Biomedical Molecular Biology, Ghent University, Ghent 9000, Belgium
6Institute for Medical Biology, University Hospital Essen, University of Duisburg-Essen, 45141 Essen, Germany

Tài liệu tham khảo

Achkar, 2015, B cells and antibodies in the defense against Mycobacterium tuberculosis infection, Immunol. Rev., 264, 167, 10.1111/imr.12276 Ackerman, 2013, Opportunities to exploit non-neutralizing HIV-specific antibody activity, Curr. HIV Res., 11, 365, 10.2174/1570162X113116660058 Ackerman, 2011, A robust, high-throughput assay to determine the phagocytic activity of clinical antibody samples, J. Immunol. Methods, 366, 8, 10.1016/j.jim.2010.12.016 Ackerman, 2013, Natural variation in Fc glycosylation of HIV-specific antibodies impacts antiviral activity, J. Clin. Invest., 123, 2183, 10.1172/JCI65708 Anthony, 2011, Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway, Nature, 475, 110, 10.1038/nature10134 Arnold, 2007, The impact of glycosylation on the biological function and structure of human immunoglobulins, Annu. Rev. Immunol., 25, 21, 10.1146/annurev.immunol.25.022106.141702 Bakema, 2014, Fc receptor-dependent mechanisms of monoclonal antibody therapy of cancer, Curr. Top. Microbiol. Immunol., 382, 373 Balu, 2011, A novel human IgA monoclonal antibody protects against tuberculosis, J. Immunol., 186, 3113, 10.4049/jimmunol.1003189 Barry, 2009, The spectrum of latent tuberculosis: rethinking the biology and intervention strategies, Nat. Rev. Microbiol., 7, 845, 10.1038/nrmicro2236 Beatty, 2001, Mycobacterial surface moieties are released from infected macrophages by a constitutive exocytic event, Eur. J. Cell Biol., 80, 31, 10.1078/0171-9335-00131 Bergmann-Leitner, 2006, Critical evaluation of different methods for measuring the functional activity of antibodies against malaria blood stage antigens, Am. J. Trop. Med. Hyg., 75, 437, 10.4269/ajtmh.2006.75.437 Berry, 2010, An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis, Nature, 466, 973, 10.1038/nature09247 Böhm, 2014, Sweet and sour: the role of glycosylation for the anti-inflammatory activity of immunoglobulin G, Curr. Top. Microbiol. Immunol., 382, 393 Bournazos, 2014, Broadly neutralizing anti-HIV-1 antibodies require Fc effector functions for in vivo activity, Cell, 158, 1243, 10.1016/j.cell.2014.08.023 Briken, 2013, Mycobacterium tuberculosis and the host cell inflammasome: a complex relationship, Front. Cell. Infect. Microbiol., 3, 62, 10.3389/fcimb.2013.00062 Brown, 2012, High-throughput, multiplexed IgG subclassing of antigen-specific antibodies from clinical samples, J. Immunol. Methods, 386, 117, 10.1016/j.jim.2012.09.007 Bruhns, 2012, Properties of mouse and human IgG receptors and their contribution to disease models, Blood, 119, 5640, 10.1182/blood-2012-01-380121 Carlsson, 2010, Host-detrimental role of Esx-1-mediated inflammasome activation in mycobacterial infection, PLoS Pathog., 6, e1000895, 10.1371/journal.ppat.1000895 Carpenter, 2006, CellProfiler: image analysis software for identifying and quantifying cell phenotypes, Genome Biol., 7, R100, 10.1186/gb-2006-7-10-r100 Casadevall, 2006, A reappraisal of humoral immunity based on mechanisms of antibody-mediated protection against intracellular pathogens, Adv. Immunol., 91, 1, 10.1016/S0065-2776(06)91001-3 Chatterji, 2006, Reference based annotation with GeneMapper, Genome Biol., 7, R29, 10.1186/gb-2006-7-4-r29 Chen, 2014, The neutrophil NLRC4 inflammasome selectively promotes IL-1β maturation without pyroptosis during acute Salmonella challenge, Cell Rep., 8, 570, 10.1016/j.celrep.2014.06.028 Chen, 2016, Association of human antibodies to arabinomannan with enhanced mycobacterial opsonophagocytosis and intracellular growth reduction, J. Infect. Dis., 214, 300, 10.1093/infdis/jiw141 Chung, 2014, Identification of antibody glycosylation structures that predict monoclonal antibody Fc-effector function, AIDS, 28, 2523, 10.1097/QAD.0000000000000444 Chung, 2014, Polyfunctional Fc-effector profiles mediated by IgG subclass selection distinguish RV144 and VAX003 vaccines, Sci. Transl. Med., 6, 228ra38, 10.1126/scitranslmed.3007736 Chung, 2015, Dissecting polyclonal vaccine-induced humoral immunity against HIV using systems serology, Cell, 163, 988, 10.1016/j.cell.2015.10.027 Darrah, 2007, Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major, Nat. Med., 13, 843, 10.1038/nm1592 Day, 2011, Functional capacity of Mycobacterium tuberculosis-specific T cell responses in humans is associated with mycobacterial load, J. Immunol., 187, 2222, 10.4049/jimmunol.1101122 de Vallière, 2005, Enhancement of innate and cell-mediated immunity by antimycobacterial antibodies, Infect. Immun., 73, 6711, 10.1128/IAI.73.10.6711-6720.2005 DiLillo, 2014, Broadly neutralizing hemagglutinin stalk-specific antibodies require FcγR interactions for protection against influenza virus in vivo, Nat. Med., 20, 143, 10.1038/nm.3443 Doherty, 2009, Biomarkers for tuberculosis disease status and diagnosis, Curr. Opin. Pulm. Med., 15, 181, 10.1097/MCP.0b013e328326f42c Eklund, 2014, Human gene variants linked to enhanced NLRP3 activity limit intramacrophage growth of Mycobacterium tuberculosis, J. Infect. Dis., 209, 749, 10.1093/infdis/jit572 Ferrara, 2011, Unique carbohydrate-carbohydrate interactions are required for high affinity binding between FcgammaRIII and antibodies lacking core fucose, Proc. Natl. Acad. Sci. USA, 108, 12669, 10.1073/pnas.1108455108 Fletcher, 2016, T-cell activation is an immune correlate of risk in BCG vaccinated infants, Nat. Commun., 7, 11633, 10.1038/ncomms11633 Gardinassi, 2014, Clinical severity of visceral leishmaniasis is associated with changes in immunoglobulin g fc N-glycosylation, MBio, 5, e01844, 10.1128/mBio.01844-14 Glatman-Freedman, 1998, Serum therapy for tuberculosis revisited: reappraisal of the role of antibody-mediated immunity against Mycobacterium tuberculosis, Clin. Microbiol. Rev., 11, 514, 10.1128/CMR.11.3.514 Gómez-Román, 2006, A simplified method for the rapid fluorometric assessment of antibody-dependent cell-mediated cytotoxicity, J. Immunol. Methods, 308, 53, 10.1016/j.jim.2005.09.018 Gunn, 2016, Enhanced binding of antibodies generated during chronic HIV infection to mucus component MUC16, Mucosal Immunol., 10.1038/mi.2016.8 Hamasur, 2004, A mycobacterial lipoarabinomannan specific monoclonal antibody and its F(ab’) fragment prolong survival of mice infected with Mycobacterium tuberculosis, Clin. Exp. Immunol., 138, 30, 10.1111/j.1365-2249.2004.02593.x Herter, 2014, Glycoengineering of therapeutic antibodies enhances monocyte/macrophage-mediated phagocytosis and cytotoxicity, J. Immunol., 192, 2252, 10.4049/jimmunol.1301249 Hessell, 2007, Fc receptor but not complement binding is important in antibody protection against HIV, Nature, 449, 101, 10.1038/nature06106 Hirako, 2015, DNA-containing immunocomplexes promote inflammasome assembly and release of pyrogenic cytokines by CD14+ CD16+ CD64high CD32low inflammatory monocytes from malaria patients, MBio, 6, e01605, 10.1128/mBio.01605-15 Ho, 2014, Association of serum IgG N-glycome and transforming growth factor-β1 with hepatitis B virus e antigen seroconversion during entecavir therapy, Antiviral Res., 111, 121, 10.1016/j.antiviral.2014.09.011 Holm, 1979, A simple sequentially rejective multiple test procedure, Scand. J. Stat., 6, 65 Jefferis, 2009, Glycosylation as a strategy to improve antibody-based therapeutics, Nat. Rev. Drug Discov., 8, 226, 10.1038/nrd2804 Jegaskanda, 2013, Antibody-dependent cellular cytotoxicity is associated with control of pandemic H1N1 influenza virus infection of macaques, J. Virol., 87, 5512, 10.1128/JVI.03030-12 Jolliffe, 1986 Kahnert, 2007, Mycobacterium tuberculosis triggers formation of lymphoid structure in murine lungs, J. Infect. Dis., 195, 46, 10.1086/508894 Kozakiewicz, 2013, The role of B cells and humoral immunity in Mycobacterium tuberculosis infection, Adv. Exp. Med. Biol., 783, 225, 10.1007/978-1-4614-6111-1_12 Machado, 2013, Copy number variation of Fc gamma receptor genes in HIV-infected and HIV-tuberculosis co-infected individuals in sub-Saharan Africa, PLoS ONE, 8, e78165, 10.1371/journal.pone.0078165 Maglione, 2007, B cells moderate inflammatory progression and enhance bacterial containment upon pulmonary challenge with Mycobacterium tuberculosis, J. Immunol., 178, 7222, 10.4049/jimmunol.178.11.7222 Maglione, 2008, Fc gamma receptors regulate immune activation and susceptibility during Mycobacterium tuberculosis infection, J. Immunol., 180, 3329, 10.4049/jimmunol.180.5.3329 Mahan, 2015, A method for high-throughput, sensitive analysis of IgG Fc and Fab glycosylation by capillary electrophoresis, J. Immunol. Methods, 417, 34, 10.1016/j.jim.2014.12.004 Mahan, 2016, Antigen-specific antibody glycosylation is regulated via vaccination, PLoS Pathog., 12, e1005456, 10.1371/journal.ppat.1005456 Malhotra, 1995, Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein, Nat. Med., 1, 237, 10.1038/nm0395-237 Martin, 2012, Efferocytosis is an innate antibacterial mechanism, Cell Host Microbe, 12, 289, 10.1016/j.chom.2012.06.010 Martinon, 2002, The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta, Mol. Cell, 10, 417, 10.1016/S1097-2765(02)00599-3 McElvania Tekippe, 2010, Granuloma formation and host defense in chronic Mycobacterium tuberculosis infection requires PYCARD/ASC but not NLRP3 or caspase-1, PLoS ONE, 5, e12320, 10.1371/journal.pone.0012320 McEwan, 2013, Intracellular antibody-bound pathogens stimulate immune signaling via the Fc receptor TRIM21, Nat. Immunol., 14, 327, 10.1038/ni.2548 Mishra, 2010, Mycobacterium tuberculosis protein ESAT-6 is a potent activator of the NLRP3/ASC inflammasome, Cell. Microbiol., 12, 1046, 10.1111/j.1462-5822.2010.01450.x Müller-Calleja, 2015, Cofactor-independent antiphospholipid antibodies activate the NLRP3-inflammasome via endosomal NADPH-oxidase: implications for the antiphospholipid syndrome, Thromb. Haemost., 113, 1071, 10.1160/TH14-07-0628 Nimmerjahn, 2008, Fcgamma receptors as regulators of immune responses, Nat. Rev. Immunol., 8, 34, 10.1038/nri2206 Niwa, 2005, IgG subclass-independent improvement of antibody-dependent cellular cytotoxicity by fucose removal from Asn297-linked oligosaccharides, J. Immunol. Methods, 306, 151, 10.1016/j.jim.2005.08.009 Nunes-Alves, 2014, In search of a new paradigm for protective immunity to TB, Nat. Rev. Microbiol., 12, 289, 10.1038/nrmicro3230 O’Garra, 2013, The immune response in tuberculosis, Annu. Rev. Immunol., 31, 475, 10.1146/annurev-immunol-032712-095939 Olinger, 2012, Delayed treatment of Ebola virus infection with plant-derived monoclonal antibodies provides protection in rhesus macaques, Proc. Natl. Acad. Sci. USA, 109, 18030, 10.1073/pnas.1213709109 Olivares, 2013, The protective effect of immunoglobulin in murine tuberculosis is dependent on IgG glycosylation, Pathog. Dis., 69, 176, 10.1111/2049-632X.12069 Parekh, 1989, A comparative analysis of disease-associated changes in the galactosylation of serum IgG, J. Autoimmun., 2, 101, 10.1016/0896-8411(89)90148-0 Phuah, 2012, Activated B cells in the granulomas of nonhuman primates infected with Mycobacterium tuberculosis, Am. J. Pathol., 181, 508, 10.1016/j.ajpath.2012.05.009 Phuah, 2016, Effects of B cell depletion on early Mycobacterium tuberculosis infection in cynomolgus macaques, Infect. Immun., 84, 1301, 10.1128/IAI.00083-16 Pincetic, 2014, Type I and type II Fc receptors regulate innate and adaptive immunity, Nat. Immunol., 15, 707, 10.1038/ni.2939 Pleass, 2009, Fc-receptors and immunity to malaria: from models to vaccines, Parasite Immunol., 31, 529, 10.1111/j.1365-3024.2009.01101.x Pontillo, 2013, Susceptibility to Mycobacterium tuberculosis infection in HIV-positive patients is associated with CARD8 genetic variant, J. Acquir. Immune Defic. Syndr., 63, 147, 10.1097/QAI.0b013e31828f93bb Prinz, 2011, Antiphospholipid antibodies induce translocation of TLR7 and TLR8 to the endosome in human monocytes and plasmacytoid dendritic cells, Blood, 118, 2322, 10.1182/blood-2011-01-330639 Raju, 2008, Terminal sugars of Fc glycans influence antibody effector functions of IgGs, Curr. Opin. Immunol., 20, 471, 10.1016/j.coi.2008.06.007 Ravetch, 1989, Alternative membrane forms of Fc gamma RIII(CD16) on human natural killer cells and neutrophils. Cell type-specific expression of two genes that differ in single nucleotide substitutions, J. Exp. Med., 170, 481, 10.1084/jem.170.2.481 Restrepo, 2011, Cross-sectional assessment reveals high diabetes prevalence among newly-diagnosed tuberculosis cases, Bull. World Health Organ., 89, 352, 10.2471/BLT.10.085738 Schmaljohn, 2016, Cell-targeting antibodies in immunity to Ebola, Pathog. Dis., 74, ftw021, 10.1093/femspd/ftw021 Selman, 2012, Changes in antigen-specific IgG1 Fc N-glycosylation upon influenza and tetanus vaccination, Mol. Cell. Proteomics, 11, 10.1074/mcp.M111.014563 Steingart, 2011, Commercial serological tests for the diagnosis of active pulmonary and extrapulmonary tuberculosis: an updated systematic review and meta-analysis, PLoS Med., 8, e1001062, 10.1371/journal.pmed.1001062 Suter, 1953, Multiplication of tubercle bacilli within mononuclear phagocytes in tissue cultures derived from normal animals and animals vaccinated with BCG, J. Exp. Med., 97, 235, 10.1084/jem.97.2.235 Sutherland, 2014, Differential gene expression of activating Fcgamma receptor classifies active tuberculosis regardless of human immunodeficiency virus status or ethnicity, Clin. Microbiol. Infect., 20, O230, 10.1111/1469-0691.12383 Teitelbaum, 1998, A mAb recognizing a surface antigen of Mycobacterium tuberculosis enhances host survival, Proc. Natl. Acad. Sci. USA, 95, 15688, 10.1073/pnas.95.26.15688 Tibshirani, 1997, The lasso method for variable selection in the Cox model, Stat. Med., 16, 385, 10.1002/(SICI)1097-0258(19970228)16:4<385::AID-SIM380>3.0.CO;2-3 Torrado, 2013, Differential and site specific impact of B cells in the protective immune response to Mycobacterium tuberculosis in the mouse, PLoS ONE, 8, e61681, 10.1371/journal.pone.0061681 Tsai, 2006, Characterization of the tuberculous granuloma in murine and human lungs: cellular composition and relative tissue oxygen tension, Cell. Microbiol., 8, 218, 10.1111/j.1462-5822.2005.00612.x Ulrichs, 2004, Human tuberculous granulomas induce peripheral lymphoid follicle-like structures to orchestrate local host defence in the lung, J. Pathol., 204, 217, 10.1002/path.1628 Vestrheim, 2014, A pilot study showing differences in glycosylation patterns of IgG subclasses induced by pneumococcal, meningococcal, and two types of influenza vaccines, Immun. Inflamm. Dis., 2, 76, 10.1002/iid3.22 Vidarsson, 2014, IgG subclasses and allotypes: from structure to effector functions, Front. Immunol., 5, 520, 10.3389/fimmu.2014.00520 Vordermeier, 1996, Increase of tuberculous infection in the organs of B cell-deficient mice, Clin. Exp. Immunol., 106, 312, 10.1046/j.1365-2249.1996.d01-845.x Zak, 2016, A blood RNA signature for tuberculosis disease risk: a prospective cohort study, Lancet, 387, 2312, 10.1016/S0140-6736(15)01316-1 Zimmerli, 1996, Selective receptor blockade during phagocytosis does not alter the survival and growth of Mycobacterium tuberculosis in human macrophages, Am. J. Respir. Cell Mol. Biol., 15, 760, 10.1165/ajrcmb.15.6.8969271 Zou, 2011, Chemoenzymatic synthesis and Fcγ receptor binding of homogeneous glycoforms of antibody Fc domain. Presence of a bisecting sugar moiety enhances the affinity of Fc to FcγIIIa receptor, J. Am. Chem. Soc., 133, 18975, 10.1021/ja208390n Zumla, 2013, Tuberculosis, N. Engl. J. Med., 368, 745, 10.1056/NEJMra1200894