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5 - Bacterial immunoglobulin-evading mechanisms: Ig-degrading and Ig-binding proteins

from Part II - Evasion of humoral immunity

Published online by Cambridge University Press:  13 August 2009

By
Mogens Kilian
Edited by
Brian Henderson  and
Petra C. F. Oyston
Mogens Kilian
Affiliation:
Department of Medical Microbiology and Immunology, University of Aarhus, The Bartholin Building, DK-800, Aarhus C, Denmark
Brian Henderson
Affiliation:
University College London
Petra C. F. Oyston
Affiliation:
Defence Science and Technology Laboratory, Salisbury
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Summary

INTRODUCTION

The mucosae are the largest surface areas of the body directly exposed to the environment and, in consequence, throughout life these surfaces are constantly challenged by microbes. Indeed, most infectious diseases take place or are initiated on these surfaces. The approximately 400 m2 of the mucosae in the respiratory, gastrointestinal, and genito-urinary tract of humans are protected by a multitude of innate and adaptive immune mechanisms (Ogra et al., 1999). To successfully colonise, all microorganisms, whether they are pathogens or commensals, must be able to evade local defence mechanisms. The dominant adaptive immune factor in the mucosal surfaces is secretory IgA (S-IgA), which is actively transported to the surface by a receptor-mediated mechanism. This chapter reviews the bacterial strategies to evade the functions of immunoglobulins (Ig), that involve proteolytic/glycolytic degradation or Ig-binding proteins, with a particular focus on IgA

IgA PROTEASE-PRODUCING BACTERIA

IgA proteases constitute a diverse group of bacterial proteinases that share several unique enzymatic properties including the ability to cleave human IgA in the hinge region. They are post-proline endopeptidases and, in most cases, attack the target polypeptide immediately adjacent to a carbohydrate side chain. With a single exception, the IgA proteases cleave only IgA1. The first examples of IgA1 proteases were demonstrated in Streptococcus sanguis, Neisseria meningitidis, and Neisseria gonorrhoeae by Plaut and coworkers in the mid-1970s (Plaut et al., 1974; Plaut et al., 1975).

Type
Chapter
Information
Bacterial Evasion of Host Immune Responses , pp. 81 - 102
Publisher: Cambridge University Press
Print publication year: 2003

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References

Ahl, T. and Reinholdt, J. (1991). Detection of immunoglobulin A1 protease-induced Fabα fragments on dental plaque bacteria. Infection and Immunity 59, 563–569Google Scholar
Beck, S. C. and Meyer, T. F. (2000). IgA1 protease from Neisseria gonorrhoeae inhibits TNFα-mediated apoptosis of human monocytic cells. FEBSLetters 472, 287–292Google Scholar
Berge, A., Kihlberg, B.-M., Sjöholm, A. G., and Björck, L. (1997). Streptococcal protein H forms soluble complement-activating complexes with IgG, but inhibits complement activation by IgG-coated targets. Journal of Biological Chemistry 272, 20,774–20,781CrossRefGoogle ScholarPubMed
Biesbrock, A. R., Reddy, M. S., and Levine, M. J. (1991). Interaction of a salivary mucinsecretory immunoglobulin A complex with mucosal pathogens. Infection and Immunity 59, 3492–3497Google ScholarPubMed
Borén, T., Falk, P., Roth, K. A., Larson, G., and Normark, S. (1993). Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science 262, 1892–1895CrossRefGoogle ScholarPubMed
Boyle, M. D. P. (1990). ed. Bacterial Immunoglobulin-Binding Proteins: Microbiology, Chemistry, Biology. San Diego: Academic Press
Bronson, R. A., Cooper, G. W., Rosenfeld, D. L., Gilbert, J. V., and Plaut, A. G. (1987). The effect of an IgA1 protease on immunoglobulins bound to the sperm surface and sperm cervical mucus penetrating ability. Fertility and Sterility 47, 985–991CrossRefGoogle ScholarPubMed
Brooks, G. F., Lammel, C. J., Blake, M. S., Kusecek, B., and Achtman, M. (1992). Antibodies against IgA1 protease are stimulated both by clinical disease and asymptomatic carriage of serogroup A Neisseria meningitidis. Journal of Infectious Diseases 166, 1316–1321CrossRefGoogle ScholarPubMed
Chuang, P. D. and Morrison, S. L. (1997). Elimination of N-linked glycosylation sites from the human IgA1 constant region: effects on structure and function. Journal of Immunology 158, 724–732Google ScholarPubMed
Cole, M. F., Evans, M., Fitzsimmons, S., Johnson, J., Pearce, C., Sheridan, M. J., Wientzen, R., and Bowden, G. (1994). Pioneer oral streptococci produce immunoglobulin A1 protease. Infection and Immunity 62, 2165–2168Google ScholarPubMed
Collin, M. and Olsén, A. (2001). EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. The European Molecular Biology Organisation Journal 20, 3046–3055CrossRefGoogle ScholarPubMed
Cooper, M. D., McGhee, Z. A., Mulks, M. H., Koomey, J. M., and Hindman, T. L. (1984). Attachment to and invasion of human fallopian tube mucosa by an IgA1 protease-deficient mutant of Nesseria gonorrhoeae and its wild-type parent. Journal of Infectious Diseases 150, 737–744CrossRefGoogle Scholar
Falk, P., Roth, K. A., Boren, T., Westblom, T. U., Gordon, J. I., and Normark, S. (1993). An in vitro adherence assay reveals that Helicobacter pylori exhibits cell lineage-specific tropism in the human gastric epithelium. Proceedings of the National Academy of Sciences USA 90, 2035–2039CrossRefGoogle Scholar
Farley, M. M., Stephens, D. S., Mulks, M. H., Cooper, M. D., Bricker, J. V., Mirra, S. S., and Wright, A. (1986). Pathogenesis of IgA1 protease-producing and -nonproducing Haemophilus influenzae in human nasopharyngeal organ cultures. Journal of Infectious Diseases 154, 752–759CrossRefGoogle ScholarPubMed
Forsgren, A., Brant, M., Möllenkvist, A., Muyombwe, A., Janson, H., Woin, N., and Riesbeck, K. (2001). Isolation and characterization of a novel IgD-binding protein from Moraxella catarrhalis. Journal of Immunology 167, 2112–2120CrossRefGoogle ScholarPubMed
Frandsen, E. V. G. (1994). Carbohydrate depletion of immunoglobulin A1 by oral species of Gram-positive rods. Oral Microbiology and Immunology 9, 352–358CrossRefGoogle ScholarPubMed
Frandsen, E. V. G., Reinholdt, J., and Kilian, M. (1995). In vivo cleavage of immunoglobulin A1 by immunoglobulin A1 proteases from Prevotella and Capnocytophaga species. Oral Microbiology and Immunology 10, 291–296CrossRefGoogle ScholarPubMed
Friman, V., Adlerberth, I., Connell, H., Svanborg, C., Hanson, L.-A., and Wold, A. E. (1996). Decreased expression of mannose-specific adhesins by Escherichia coli in the colonic microflora of immunoglobulin A-deficient individuals. Infection and Immunity 64, 2794–2798Google ScholarPubMed
Frithz, E., Hedén, L.-O., and Lindahl, G. (1989). Extensive sequence homology between IgA receptor and M proteins in Streptococcus pyogenes. Molecular Microbiology 3, 1111–1119CrossRefGoogle Scholar
Fujiyama, Y., Iwaki, M., Hodohara, K., Hosoda, S., and Kobayashi, K. (1986). The site of cleavage in human alpha chains of IgA1 and IgA2:A2m(1) allotype paraproteins by the clostridial IgA protease. Molecular Immunology 23, 147–150Google ScholarPubMed
Gilbert, J. V., Plaut, A. G., Longmaid, B., and Lamm, M. E. (1983). Inhibition of microbial IgA proteases by human secretory IgA and serum. Molecular Immunology 20, 1039–1049CrossRefGoogle ScholarPubMed
Hajishengallis, G., Nikolova, E., and Russell, M. W. (1992). Inhibition of Streptococcus mutans adherence to saliva-coated hydroxyapatite by human secretory immunoglobulin A (S-IgA) antibodies to cell surface protein antigen I/II: reversal by IgA1 protease cleavage. Infection and Immunity 60, 5057–5064Google ScholarPubMed
Halter, R., Pohlner, J., and Meyer, T. F. (1989). Mosaic-like organization of IgA protease genes in Neisseria gonorrhoeae generated by horizontal genetic exchange in vivo. The European Molecular Biology Organisation Journal 8, 2737–2744Google ScholarPubMed
Hammerschmidt, S., Talay, S. R., Brandtzaeg, P., and Chatwal, G. S. (1997). SpsA, a novel pneumococcal surface protein with specific binding to secretory immunoglobulin A and secretory component. Molecular Microbiology 25, 1113–1124CrossRefGoogle ScholarPubMed
Hauck, C. R. and Meyer, T. F. (1997). The lysosomal/phagosomal membrane protein h-lamp-1 is a target of the IgA1 protease of Neisseria gonorrhoeae. FEBSLetters 405, 86–90Google Scholar
Hedges, S. R., Mayo, M. S., Kallman, L., Mestecky, J., Hook, E. W. III, and Russell, M. W. (1998). Evaluation of immunoglobulin A1 (IgA1) protease and IgA1 protease-inhibitory activity in human female genital infection with Neisseria gonorrhoeae. Infection and Immunity 66, 5826–5832Google ScholarPubMed
Henderson, I. R., Navarro-Garcia, F., and Nataro, J. P. (1998). The great escape: structure and function of the autotransporter proteins. Trends in Microbiology 6, 370–378CrossRefGoogle ScholarPubMed
Hohwy, J., Reinholdt, J., and Kilian, M. (2001). Population kinetics of Streptococcus mitis in its natural habitat. Infection and Immunity 69, 6055–6063CrossRefGoogle Scholar
Hopper, S., Vasquez, B., Merz, A., Clary, S., Wilbur, J. S., and So, M. (2000). Effects of the IgA1 protease on Neisseria gonorrhoeae trafficking across polarized T84 epithelial monolayers. Infection and Immunity 68, 906–911CrossRefGoogle ScholarPubMed
Jarvis, G. A. and Griffiss, J. M. (1991). Human IgA1 blockade of IgG-initiated lysis of Neisseria meningitidis is a function of antigen-binding fragment binding to the polysaccharide capsule. Journal of Immunology 147, 1962–1967Google ScholarPubMed
Jerlström, P. G., Chhatwal, G. S., and Timmis, K. N. (1991). The IgA-binding beta antigen of the c protein complex of group B streptococci: sequence determination of its gene and detection of two binding regions. Molecular Microbiology 5, 843–849CrossRefGoogle Scholar
Johannsen, D. B., Johnston, D. M., Koymen, H. O., Cohen, M. S., and Cannon, J. G. (1999). A Neisseria gonorrhoeae immunoglobulin A1 protease mutant is infectious in the human challenge model of urethral infection. Infection and Immunity 67, 3009–3013Google ScholarPubMed
Kapatais-Zoumbos, K., Chandler, D. K., and Barile, M. F. (1985). Survey of immunoglobulin A protease activity among selected species of Ureaplasma and Mycoplasma specificity for host immunoglobulin A. Infection and Immunity 47, 704–709Google ScholarPubMed
Kett, K., Brandtzaeg, P., Radl, J., and Haaijman, J. T. (1986). Different subclass distribution of IgA-producing cells in human lymphoid organs and various secretory tissues. Journal of Immunology 136, 3631–3635Google ScholarPubMed
Kilian, M., Husby, S., Høst, A., and Halken, S. (1995). Increased proportions of bacteria capable of cleaving IgA1 in the pharynx of infants with atopic disease. Pediatric Research 38, 182–186CrossRefGoogle ScholarPubMed
Kilian, M., Mestecky, J., Kulhavy, R., Tomana, M., and Butler, W. T. (1980). IgA1 proteases from Haemophilus influenzae, Streptococcus pneumoniae, Neisseria meningitidis, and Streptococcus sanguis: comparative immunochemical studies. Journal of Immunology 124, 2596–2600Google ScholarPubMed
Kilian, M., Mestecky, J., and Schrohenloher, R. E. (1979). Pathogenic species of Haemophilus and Streptococcus pneumoniae produce immunoglobulin A1 protease. Infection and Immunity 26, 143–149Google ScholarPubMed
Kilian, M. and Reinholdt, J. (1987). A hypothetical model for the development of invasive infection due to IgA1 protease-producing bacteria. Advances in Experimental Medicine and Biology 216B, 1261–1269Google ScholarPubMed
Kilian, M., Roland, K., and Mestecky, J. (1981). Interference of secretory immunoglobulin A with sorption of oral bacteria to hydroxyapatite. Infection and Immunity 31, 942–951Google ScholarPubMed
Kilian, M. and Russell, M. W. (1999). Microbial evasion of IgA functions. In Handbook of Mucosal Immunology, 2nd edn, ed. P. L. Ogra, J. Mestecky, M. E. Lamm, W. Strober, J. B. Bienenstock and J. R. McGhee, pp. 241–251. San Diego: Academic Press
Kilian, M. and Thomsen, B. (1983). Antigenic heterogeneity of immunoglobulin A1 proteases from encapsulated and non-encapsulated Haemophilus influenzae. Infection and Immunity 42, 126–132Google ScholarPubMed
Kirkeby, L., Rasmussen, T. T., Reinholdt, J., and Kilian, M. (2000). Immunoglobulins in nasal secretions of healthy humans: Structural integrity of secretory immunoglobulin A1 (IgA1) and occurrence of neutralizing antibodies to IgA1 proteases of nasal bacteria. Clinical and Diagostic Laboratory Immunology 7, 31–39Google ScholarPubMed
Kobayashi, K., Fujiyama, Y., Hagiwara, K., and Kondoh, H. (1987). Resistance of normal serum IgA and secretory IgA to bacterial IgA proteases: evidence for the presence of enzyme-neutralizing antibodies in both serum and secretory IgA, and also in serum IgG. Microbiology and Immunology 31, 1097–1106CrossRefGoogle ScholarPubMed
Liljemark, W. F., Bloomquist, C. G., and Ofstehage, J. C. (1979). Aggregation and adherence of Streptococcus sanguis: role of human salivary immunglobulin A. Infection and Immunity 26, 1104–1110Google Scholar
Lin, L., Ayala, P., Larson, J., Mulks, M., Fukuda, M., Carlsson, S. R., Enns, C., and So, M. (1997). The Neisseria type 2 IgA1 protease cleaves LAMP1 and promotes survival of bacteria within epithelial cells. Molecular Microbiology 24, 1083–1094CrossRefGoogle ScholarPubMed
Lomholt, H. (1995). Evidence of recombination and an antigenically diverse immunoglobulin A1 protease among strains of Streptococcus pneumoniae. Infection and Immunity 63, 4238–4243Google ScholarPubMed
Lomholt, H., Poulsen, K., and Kilian, M. (1995). Comparative characterization of the iga gene encoding IgA1 protease in Neisseria meningitidis, Neisseria gonorrhoeae and Haemophilus influenzae. Molecular Microbiology 15, 495–506CrossRefGoogle ScholarPubMed
Lomholt, H., van-Alphen, L., and Kilian, M. (1993). Antigenic variation of immunoglobulin A1 proteases among sequential isolates of Haemophilus influenzae from healthy children and patients with chronic obstructive pulmonary disease. Infection and Immunity 61, 4575–4581Google ScholarPubMed
Lorenzen, D. R., Düx, F., Wölk, U., Tsirpouchtsidis, A., Hass, G., and Meyer, T. F. (1999). Immunogloubulin A1 protease, an exoenzyme of pathogenic Neisseriae, is a potent inducer of proinflammatory cytokines. Journal of Experimental Medicine 190, 1049–1058CrossRefGoogle Scholar
Male, C. (1979). Immunoglobulin A1 protease production by Haemophilus influenzae and Streptococcus pneumoniae. Infection and Immunity 26, 254–261Google ScholarPubMed
Mattu, T. S., Pleass, R. J., Willis, A. C., Kilian, M., Wormald, M. R., Lellouch, A. C., Rudd, P. M., Woof, J. M., and Dwek, R. A. (1998). The glycosylation and structure of human serum IgA1, Fab and Fc regions and the role of N-glycosylation on FcαR interactions. Journal Biological Chemistry 273, 2260–2272CrossRefGoogle Scholar
Mestecky, J. and Russell, M. W. (1986). IgA subclasses. Monographs in Allergy 19, 277–301Google ScholarPubMed
Meyer, T. F., Pohlner, J., and Putten, J. P. (1994). Biology of the pathogenic Neisseriae. Current Topics in Microbiology and Immunology 192, 283–317Google ScholarPubMed
Morelli, G., del Valle, J., Lammel, C. J., Pohlner, J., Muller, K., Blake, M., Brooks, G. F., Meyer, T. F., Koumare, B., Brieske, N., et al. (1994). Immunogenicity and evolutionary variability of epitopes within IgA1 protease from serogroup A Neisseria meningitidis. Molecular Microbiology 11, 175–187CrossRefGoogle ScholarPubMed
Mulks, M. H., Plaut, A. G., and Lamm, M. (1980). Gonococcal IgA protease reduces inhibition of bacterial adherence by human secretory IgA. In Genetics and Immunobiology of Pathogenic Neisseria, ed. S. Normark and D. Danielsson, pp. 217–220. University of Umeå: Umeå, Sweden
Novak, R., Charpentier, E., Braun, J. S., Park, E., Murti, S., Tuomanen, E., and Masure, R. (2000). Extracellular targeting of choline-binding proteins in Streptococcus pneumoniae by a zinc metalloprotease. Molecular Microbiology 36, 366–376CrossRefGoogle ScholarPubMed
Ogra, P. L., Mestecky, J., Lamm, M. E., Strober, W., Bienenstock, J., and McGhee, J. R. (1999). Mucosal Immunology, 2nd edn. San Diego: Academic Press
Plaut, A. G., Genco, R. J., and Tomasi, T. B. Jr. (1974). Isolation of an enzyme from Streptococcus sanguis which specifically cleaves IgA. Journal of Immunology 113, 289–291Google ScholarPubMed
Plaut, A. G., Gilbert, J. V., Artenstein, M. S., and Capra, J. D. (1975). Neisseria gonorrhoeae and Neisseria meningitidis: extracellular enzyme cleaves human immunoglobulin A. Science 193, 1103–1105CrossRefGoogle Scholar
Plaut, A. G., Qiu, J., Grundy, F., and Wright, A. (1992). Growth of Haemophilus influenzae in human milk: synthesis, distribution and activity of IgA protease as determined by study of iga+ and mutant iga-cells. Journal of Infectious Diseases 166, 43–52CrossRefGoogle ScholarPubMed
Pleass, R. J., Areschoug, T., Lindahl, G., and Woof, J. M. (2001). Streptococcal IgA-binding proteins bind in the C2-C3 interdomain region and inhibit binding of IgA to human CD89. Journal of Biological Chemistry 276, 8197–8204CrossRefGoogle Scholar
Pleass, R. J., Kusel, J. R., and Woof, J. M. (2000). Cleavage of human IgE mediated by Schistosoma mansoni. International Archives of Allergy and Immunology 121, 194–204CrossRefGoogle ScholarPubMed
Polissi, A., Pontiggia, A., Feger, G., Altieri, M., Mottl, H., Ferrari, L., and Simon, D. (1998). Large-scale identification of virulence genes from Streptococcus pneumoniae. Infection and Immunity 66, 5620–5629Google ScholarPubMed
Pohlner, J., Halter, R., Beyreuther, K., and Meyer, T. F. (1987). Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325, 458–462CrossRefGoogle ScholarPubMed
Poulsen, K., Reinholdt, J., and Kilian, M. (1992). A comparative genetic study of serologically distinct Haemophilus influenzae type 1 immunoglobulin A1 proteases. Journal of Bacteriology 174, 2913–2921CrossRefGoogle ScholarPubMed
Poulsen, K., Reinholdt, J., Jespersgaard, C., Boye, K., Brown, T. A., Hauge, M., and Kilian, M. (1997). A comprehensive genetic study of streptococcal IgA1 protease: Evidence for recombination within and between species. Infection and Immunity 66, 181–190Google Scholar
Prokesová, L., Potuzniková, B., Potempa, J., Zikán, J., Radl, J., Hachova, L., Baran, K., Porwit-Bobr, Z., and John, C. (1992). Cleavage of human immunoglobulins by serine proteinase from Staphylococcus aureus. Immunology Letters 31, 259–266CrossRefGoogle ScholarPubMed
Qiu, J., Brackee, G. P., and Plaut, A. G. (1996). Analysis of the specificity of bacterial immunoglobulin A (IgA) protease by a comparative study of ape serum IgAs as substrates. Infection and Immunity 64, 933–937Google ScholarPubMed
Qiu, J., Hendrixson, D. R., Baker, E. N., Murphy, T. F., St. Geme, J. W. III, and Plaut, A. G. (1998). Human milk lactoferrin inactivates two putative colonization factors expressed by Haemophilus influenzae. Proceedings of the National Academy of Sciences USA 95, 12,641–12,646CrossRefGoogle ScholarPubMed
Radaev, S. and Sun, P. D. (2001). Recognition of IgG by Fcγ receptor. Journal of Immunology 276, 16,478–16,483Google ScholarPubMed
Reinholdt, J. and Kilian, M. (1987). Interference of IgA protease with the effect of secretory IgA on adherence of oral streptococci to saliva-coated hydroxyapatite. Journal of Dental Research 66, 492–497CrossRefGoogle ScholarPubMed
Reinholdt, J. and Kilian, M. (1997). Comparative analysis of immunoglobulin A1 protease activity among bacteria representing different genera, species, and strains. Infection and Immunity 65, 4452–4459Google ScholarPubMed
Reinholdt, J., Friman, V., and Kilian, M. (1993). Similar proportions of immunoglobulin A1 (IgA1) protease-producing streptococci in initial dental plaque of selectively IgA-deficient and normal individuals. Infection and Immunity 61, 3998–4000Google ScholarPubMed
Reinholdt, J., Tomana, M., Mortensen, S. B., and Kilian, M. (1990). Molecular aspects of immunoglobulin A1 degradation by oral streptococci. Infection and Immunity 58, 1186–1194Google ScholarPubMed
Rudd, P. M., Elliott, T., Cresswell, P., Wilson, I. A., and Dwek, R. A. (2001). Glycosylation and the immune system. Science 291, 2370–2376CrossRefGoogle ScholarPubMed
Ruhl, S., Sandberg, A. L., Cole, M. F., and Cisar, J. O. (1996). Recognition of immunoglobulin A1 by oral actinomyces and streptococcal lectins. Infection and Immunity 64, 5421–5424Google ScholarPubMed
Russell, M. W., Kilian, M., and Lamm, M. E. (1999). Biological activities of IgA. In Mucosal Immunology, 2nd edn., ed. P. L. Ogra, J. Mestecky, M. E. Lamm, W. Strober, J. B. Bienenstock, and J. R. McGhee, pp. 225–240. San Diego: Academic Press
Russell, M. W., Reinholdt, J., and Kilian, M. (1989). Anti-inflammatory activity of human IgA antibodies and their Faba fragments: inhibition of IgG-mediated complement activation. European Journal of Immunology 19, 2243–2249CrossRefGoogle Scholar
Saltzman, W. M., Radomsky, M. L., Whaley, K. J., and Cone, R. A. (1994). Antibody diffusion in human cervical mucus. Biophysical Journal 66, 508–515CrossRefGoogle ScholarPubMed
Sasso, E. H., Silverman, G. J., and Mannik, M. (1991). Human IgA and IgG F(ab′2 that bind to staphylococcal protein A belong to the VHIII subgroup. Journal of Immunology 147, 1877–1883Google Scholar
Senda, S., Fujiyama, Y., Ushijima, T., Hodohara, K., Bamba, T., Hosoda, S., Kobayashi, K. (1985). Clostridium ramosum, an IgA protease-producing species and its ecology in the human intestinal tract. Microbiology and Immunology 29, 203–207CrossRefGoogle ScholarPubMed
Shin, M. H., Kita, H., Park, H. Y., and Seoh, J. Y. (2001). Cysteine protease secreted by Paragonimus westermani attenuates effector functions of human eosinophils stimulated with immunoglobulin G. Infection and Immunity 69, 1599–1604CrossRefGoogle ScholarPubMed
Sørensen, C. H. and Kilian, M. (1984). Bacterium-induced cleavage of IgA in nasopharyngeal secretions from atopic children. Acta Pathologica, Microbiologica, and Immunologica Scandinavica, Section C 92, 85–87Google ScholarPubMed
Stenberg, L., O'Toole, P. W., Mestecky, J., and Lindahl, G. (1994). Molecular characterization of protein Sir, a streptococcal cell surface protein that binds both IgA and IgG. Journal of Biological Chemistry 269, 13,458–13,464Google Scholar
Thern, A., Stenberg, L., Dahlbäck, B., and Lindahl, G. (1995). Ig-binding surface proteins of Streptococcus pyogenes also bind human C4b-binding protein (C4BP), a regulatory component of the complement system. Journal of Immunology 154, 375–386Google Scholar
Egmond, M., Damen, C. A., Spriel, A. B., Vidarsson, G., Garderen, E., and Winkel, J. G. J. (2001). IgA and the IgA Fc receptor. Trends in Immunology 22, 205–211CrossRefGoogle ScholarPubMed
Vitovski, S., Read, R. C., and Sayers, J. R. (1999). Invasive isolates of Nesseria meningitidis possess enhanced immunoglobulin A1 protease activity compared to colonizing strains. FASEBJournal 13, 331–337Google Scholar
Wold, A. E., Motas, C., Svanborg, C., and Mestecky, J. (1994). Lectin receptors on IgA isotypes. Scandinavian Journal of Immunology 39, 195–201CrossRefGoogle ScholarPubMed
Wold, A., Mestecky, J., Tomana, M., Kobata, A., Ohbayashi, H., Endo, T., and Svanborg Edén, C. (1990). Secretory immunoglobulin A carries oligosaccharide receptors for Escherichia coli type 1 fimbrial lectin. Infection and Immunity 58, 3073–3077Google ScholarPubMed

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