Abstract
Unique proteins on the surface of certain bacteria bind selectively and with high affinity to the Fc region of various species of IgG. The interaction of bacterial Fc receptors with constant region determinants on the heavy chain of the IgG molecule does not influence the ability of the antibody to recognize its antigen. This property makes these receptors valuable tracers for quantitation of antigen–antibody complexes. The majority of studies to date have focused on the type I Fc receptor from Staphylococcus aureus more frequently designated as protein A. In this report we discuss the limitations of protein A and describe the properties of a second generation of bacterial Fc receptors that should find broad applications in immunochemistry, immuno–histology, and immuno–electronmicroscopy.
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References
Langone, J.J. 1982. Protein A from Staphylococcus aureus and related immunoglobulin receptors produced by streptococci and pneumococci. Adv. Immunol. 32: 157–252.
Porter, R.R. 1959. The hydrolysis of rabbit γ-globulin and antibody with crystalline papain. J. Biochem. 73: 119–126.
Forsgren, A., Ghetie, V., Lindmark, R. and Sjöquist, H. 1983. Protein A and its exploitation, p. 429–480. In: Staphylococci and Staphylococcal Infections, Vol. 2. C. S. F. Easmon and C. Adlam (eds.). Academic Press Inc., London.
Langone, J.J., Boyle, M.D.P. and Borsos, T. 1977. 125I Protein A: Applications to the quantitative determination of fluid phase and cell-bound IgG. J. Immunol. Meth. 18: 281–293.
Langone, J.J. 1978. 125I Protein A: A tracer for immunoassay. J. Immunol. Method. 24: 269–285.
Boyle, M.D.P. 1984. Applications of bacterial Fc receptors in immunotechnology. Biotechniques. 2: 334–340.
Langone, J.J., Boyle, M.D.P. and Borsos, T. 1979. A solid phase immunoassay for human immunoglobulin E. Use of 125I protein A as the tracer. Analyt. Biochem. 93: 207–215.
J.J., Langone . 1982. Use of labeled protein A in quantitative immuno-chemical analysis of antigens and antibodies. J. Immunol. Meth. 51: 3–22.
Gee, A.P. and Langone, J.J. 1981. Immunoassay using 125I- or enzyme-labeled protein A and antigen-coated tubes. Anal. Biochem. 116: 524–530.
Richman, D.D. 1983. The use of staphylococcal protein A in diagnostic virology. Curr. Top. Microbiol. Immunol. 104: 159–576.
Duboid-Dalcq, M., McFarland, H. and McFarlin, D. 1977. Protein A-peroxidase: a valuable tool for the localization of antigens. J. Histochem. Cytochem. 25: 1201–1206.
Chang, H.C., Takashima, I., Arikawa, J. and Hashimoto, N. 1984. Biotin-labeled protein A enzyme-linked immunosorbent assay for the detection of Japanese encephalitis antibody in sera from humans, swine, and several animal species. J. Virol. Methods. 9: 143–51.
Jensen, K. 1958. A normally occurring Staphylococcus antibody in human serum. Acta Path. Microbiol. 44: 421–428.
Forsgren, A. and Sjöquist, J. 1966. Protein A from S. aureus. I. Pseudoimmune reaction with human γ-globulin. J. Immunol. 97: 822–827.
Kronvall, G. 1973. A surface component of group A, C, and G streptococci with non-immune reactivity for immunoglobulin G. J. Immunol. 111: 1401–1406.
Myhre, E.B. and Kronvall, G. 1981. Immunoglobulin specificities of defined types of streptococcal Ig receptors, p. 209–210. In: Basic Concepts of Streptococci and Streptococcal Diseases. S. E. Holm and P. Christensen (eds). Redbook, Ltd. Chertsey, Surrey.
Reis, K.J., Ayoub, E.M. and Boyle, M.D.P. 1983. Detection of receptors for Fc region of IgG on streptococci. J. Immunol. Methods. 59: 83–94.
Reis, K.J., Ayoub, E.M. and Boyle, M.D.P. 1984. Streptococcl Fc receptors: I. Isolation and partial characterization of the receptors from a group C streptococcus. J. Immunol. 132: 3091–3097.
Van der Merwe, J.P. and Stegeman, J.H. 1985. Binding of Coprococcus comes to the Fc portion of IgG. A possible role in the pathogenesis of Crohn's disease? Eur. J. Immunol. 15: 860–863.
Widders, P.R., Stoke, C.R., Newby, T.J. and Bourne, F.J. 1985. Nonimmune binding of equine immunoglobulin by the causative organism of contagious equine metritis, Taylorella equigenitalis Infect. Immunity 48: 417–421.
Harboe, M. and Fölliny, I. 1974. Recognition of two distinct groups of human IgM and IgA based on different binding to Staphylococci. Scand. J. Immunol. 3: 471–482.
Inganäs, M. 1981. Comparison of mechanisms of interaction between protein A from Staphylococcus aureus and human monoclonal IgG, IgA and IgM in relation to the classical Fcγ and the alternative F(ab′)2ε protein A interactions. Scand. J. Immunol. 13: 343–352.
Erntell, M., Myhre, E.B., and Kronvall, G. 1983. Alternative non-immune F(ab′)2-mediated immunoglobulin binding to group C and G streptococci. Scand. J. Immunol. 17: 201–209.
Christensen, P. and Oxelius, V.-A. 1975. A reaction between some streptococci and IgA myeloma proteins. Acta Path. Microbiol. Scand. Sect. C 83: 184–188.
Havlicek, J. 1978. Occurrence of Fc-reacting factor in acid extracts of Streptococcus pyogenes and its relationship to M protein. Expl. Cell. Biol. 46: 146–151.
Reis, K.J., Yarnall, M., Ayoub, E.M. and Boyle, M.D.P. 1984. Effect of mouse passage on Fc receptor expression by group A streptococci. Scand. J. Immunol. 20: 433–439.
Burova, L.A. and Christensen, P., Grubb, R., Jonsson, A., Samuelsson, G., Schalén, C. and Svensson, M.-L. 1980. Changes in virulence, M-protein and IgG Fc receptor activity in a type 12 group A streptococcal strain during mouse passages. Acta P. path. Microbiol. Scand. Sect. B 98: 199–205.
Burova, L.A., Christensen, P., Grubb, R., Krasilnikov, I.A., Samuelsson, G., Schalén, C., Svensson, M.-L., and Zätterström, U. 1981. IgG Fc-receptors in T-type 12 group A streptococci from clinical specimens: absence from M:type 12 and presence in M-type 22. Acta Path. Microbiol. Scand. Sect. B 89: 433–435.
Schwan, W.R. and Hartman, P.A. 1986. Binding of chicken, bovine, and rabbit immunoglobulins by avian, bovine, and human strains of Staphylococcus aureus. Poultry Science 65: 696–703.
Freimer, E.H., Raeder, R., Feinstein, A., Herbert, J., Gurner, B.W. and Coombs, R.R.A. 1979. Detection of protein A-like substances on hemolytic streptococci prior to use in mixed reverse passive antiglobu-lin hemagglutination (MRPHH). J. Immunol. Method. 31: 219–230.
Yarnall, M., Reis, K.J., Ayoub, E.M. and Boyle, M.D.P. 1984. An immunoblotting technique for the detection of bound and secreted bacterial Fc receptors. J. Microbiol. Methods 3: 83–93.
Sjöquist, J., Meloun, B. and Hjelm, H. 1972. Protein A isolated from Staphylococcus aureus after disgestion with lysostaphin. Eur. J. Biochem. 29: 572–578.
Sjödahl, J. 1977. Repetitive sequences in protein A from Staphylococcus aureus: Arrangement of five regions within the protein, four of them highly homologous and Fc-binding. Eur. J. Biochem. 73: 343–351.
Sjödahl, J. 1977. Structural studies on the four repetitive Fc-binding regions in protein A from Staphylococcus aureus. Eur. J. Biochem. 78: 471–490.
Deisenhofer, J. 1981. Crystallographic refinement and atomic models of a human Fc fragment and its complex with fragments B of protein A from Staphylococcus aureus at 2.9Å and 2.8Å resolution. Biochemistry 20: 2361–2370.
Deisenhofer, J., Jones, T.A., Huber, R., Sjödahl, J. and Sjöquist, J. 1978. Crystallization, crystal structure analysis and atomic model of the complex formed by a human Fc fragment and fragment B of protein A from Staphylococcus aureus . Hoppe-Seyler's Z. Physiol. Chem. 395: 975–985.
Lofdahl, S., Guss, B., Uhlén, M., Philipson, L. and Lindberg, M. 1983. Gene for staphylococcal protein A. Proc. Natl. Acad. Sci. 80: 697–701.
Uhlén, M., Guss, B., Nilsson, B., Gatenbeck, S., Philipson, L. and Lindberg, M. 1984. Complete sequence of the Staphylococcal gene encoding protein A. J. Biol. Chem. 259: 1695–1702.
Duggleby, Clive, J. and Susan, A. 1983. Cloning and expression of the Staphylococcus aureus protein A gene in Escherichia coli. Nucleic Acids Research. 11: 3065–3076.
Uhlén, M., Lindberg, M. and Philipson, L. 1984. The gene for staphylococcal protein A. Immunol Today 5: 244–248.
Sjöquist, J. and Stålenheim, G. 1969. Protein A from Staphylococcus aureus. IX. Complement-fixing activity of protein A-IgG complexes. J. Immunol. 103: 467–473.
Stålenheim, G. and Sjöquist, J. 1970. Protein A from Staphylococcus aureus. X. Complement fixing activity of complexes between protein A and myeloma IgG or papain fragments of IgG. J. Immunol. 105: 944–948.
Kronvall, G. and Gewurz, H. 1970. Activation and inhibition of IgG mediated complement fixation by staphylococcal protein A. Clin. Exp. Immunol. 7: 211–220.
Ståhlenheim, G., Gotze, O., Cooper, N.R., Sjöquist, J. and Muller-Eberhard, H.J. 1973. Consumption of human complement components by complexes of IgG with protein A of Staphylococcus aureus. Immunochemistry 10: 501–507.
Langone, J.J., Boyle, M.D.P. and Borsos, T. 1978. Studies on the interaction between protein A and immunoglobulin G: Effect of protein A on the functional activity of IgG. J. Immunol. 121: 327–332.
Langone, J.J., Boyle, M.D.P. and Borsos, I. 1978. Studies on the interaction between protein A and immunoglobulin G: Composition and activity of complexes formed between protein A and IgG. J. Immunol. 121: 333–338.
Martin, R.R., Crowder, J.G. and White, A. 1967. Human reactions to Staphylococcus antigens. A possible role of leukocyte lysosomal enzymes. J. Immunol. 99: 269–275.
Gustafson, G.T., Stålenheim, G., Forsgren, A. and Sjöquist, J. 1968. “Protein A” from Staphylococcus aureus. IV. Production of anaphylaxis-like cutaneous and systemic reactions in non-immunized guinea-pigs. J. Immunol. 100: 530–534.
Lawman, M.J.P., Boyle, M.D.P., Gee, A.P. and Young, M. 1984. A rapid technique for measuring leukocyte chemotaxis in vivo. J. Immunol. Methods 69: 197–206.
Forsgren, A., Svedjelund, A. and Wigzell, H. 1976. Lymphocyte stimulation by protein A of Staphylococcus aureus. Eur. J. Immunol. 6: 207–213.
Romangnani, S., Amadori, A., Giudizi, M.G., Biagiotti, R., Maggi, E. and Ricci, M. 1978. Different mitogenic activity of soluble and insoluble staphylococcal protein A (SPA). Immunology 35: 471–470.
Smith, E., Johnson, H.M. and Blalock, J.E. 1983. Staphylococcus aureus protein A induces the production of interferon-α in human lymphocytes and interferon-α/β in mouse spleen cells. J. Immunol. 130: 773–776.
Pryjma, J., Munoz, J., Galbraith, R.M., Fudenberg, H.H. and Virella, G. 1980. Induction and suppression of immunoglobulin synthesis in cultures of human lymphocytes: effects of pokeweek mitogen and Staphylococcus aureus Cowan I. J. Immunol. 124: 56–661.
Ringden, O. 1985. Induction of immunoglobulin secretion by protein A from Staphylococcus aureus in human blood and bone marrow B cells. Scand. J. Immunol. 22: 7–26.
Pryjma, J., Munoz, J., Virella, G. and Fudenberg, H.H. 1980. Evaluation of IgM, IgG, IgA, IgD and IgE. Secretion by human peripheral blood lymphocytes in cultures stimulated with pokeweed mitogen and Staphylococcus aureus Cowan I. Cell Immunol. 50: 115–125.
Bansal, S.C., Bansal, B.R., Thomas, H.E., Siegel, P.D., Rhoads, J.E., Cooper, D.R., Terman, D.S. and Mark, R. 1978. Ex vivo removal of serum IgG in a patient with colon carcinoma. Cancer 42: 1–18.
Bansal, S.C., Bansal, B.R., Rhoads, J.E., Cooper, D.R., Boland, J.P. and Mark, R. 1978. Ex-vivo removal of mammalian immunoglobulin G: Methods and Immunological Alterations. Int. J. Artif. Organs 1: 94–103.
Terman, D.S., Yamamoto, T., Tillquist, R.L., Henry, J.F., Cook, G.L., Silver, A. and Shearer, W.T. 1980. Tumoricidal response induced by cytosine arabinoside after plasma perfusion over protein A. Science 209: 1257–1259.
Terman, D.S., Yamamoto, T., Mattioli, M., Cook, G.L., Tillquist, R., Henry, J.F., Poser, R. and Daskal, Y. 1980. Extensive necrosis of spontaneous canine mammary adenocarcinoma after extracorporeal perfusion over Staphylococcus aureus Cowan I: Description of acute tumoricidal response: Morphologic, histologic, immunohistochemical, immunologic and serologic findings. J. Immunol. 124: 795–805.
Brown, J.P., Tamerius, J.D. and Hellström, I. 1979. Indirect 125I labeled protein A assay for monoclonal antibodies to cell surface antigens. J. Immunol. Methods. 31: 201–209.
Suter, L., Brüggen, J. and Sorg, C. 1980. Use of an enzyme-linked immunosorbent assay (ELISA) for screening of hybridoma antibodies against cell surface antigens. J. Immunol. Methods. 39: 407–411.
Goding, J.W. 1983. Monoclonal Antibodies: Principles and Practice, 113–116. Academic Press. Inc. London and New York.
Christensen, P. and Oxelius, V.-A. 1974. Quantitation of the uptake of human IgG by some streptococci of groups A, B, C, and G. Acta Path. Microbiol. Scans. Sect. C. 82: 475–483.
Yarnall, M. and Boyle, M.D.P. 1986. Isolation and partial characterization of a type II Fc receptor from a group A streptococcus. Mol. Cell. Biochem. 70: 57–66.
Yarnall, M. and Boyle, M.D.P. 1986. Identification of a unique receptor on a group A streptococcus for the Fc region of human IgG3 . J. Immunol. 136: 2670–2673.
Yarnall, M. and Boyle, M.D.P. 1986. Isolation and characterization of Type IIa and Type IIb Fc receptors from a group A streptococcus. Scand. J. Immunol. 24: 549–557.
Yarnall, M. and Boyle, M.D.P. 1986. Influence of dipeptides on the interaction of immunoglobulins with bacterial Fc receptors. Biochemical and Biophysical Research Communications. 135: 1105–1111.
Christensen, P., Grubb, A., Grubb, R., Samuelsson, G., Schalén, C. and Svensson, M.-L. 1979. Demonstration of the non-identity between the Fc receptor for human IgG from group A streptococci type 15 and M protein, peptidoglycan and the group specific carbohydrate. Acta Path. Microbiol. Scand. Sect. C. 87: 257–261.
Schalén, C., Christensen, P., Grubb, A., Samuelsson, G. and Svensson, M.-L. 1980. Demonstration of separate receptors for human IgA and IgG in group A streptococci type 4. Acta Path. Microbiol. Scand. Sect. C. 88: 77–82.
Grubb, A., Grubb, R., Christensen, P. and Schalén, C. 1982. Isolation and some properties of an IgG Fc binding protein from group A streptococci type 15. Int. Archs. Allergy Appl. Immun. 67: 369–376.
Wagner, B., Wagner, M. and Ryc, M. 1983. Morphological evidence for different types of IgG-Fc receptors in group A streptococci. Zbl. Bakt. Hyg. A. 256: 61–71.
Burova, L., Ravdonikas, L.E., Christensen, P., Schalén, C. and Totolian, A.A. 1983. The genetic control of virulence in group A streptococci. II. Trigger effect by plasmids on anti-phagocytic activity, opacity factor and IgG and IgA Fc-receptors. Acta Path. Microbiol. Immunol. Scand. Sect. B. 91: 61–67.
Ravdonikas, L.E., Christensen, P., Burova, L.A., Grabovskaya, Björck, L., Schalén, C., Svensson, M.-L., and Totolian, A.A. 1984. The genetic control of virulence in group A streptococci. III. Plasmid-Induced. “switch-off”-effect on some pathogenic properties. Acta Path. Microbiol. Immunol. Scand. Sect. B. 92: 65–69.
Schalén, C., Truedsson, L., Christensen, K. and Christensen, P. 1985. Blocking of antibody complement-dependent effector functions by streptococcal IgG Fc-receptor and staphylococcal protein A. Acta Path. Microbiol. Immunol. Scand. Sect. B. 93: 395–400.
Björck, L. and Kronvall, G. 1984. Purification and some properties of streptococcal protein G, a novel IgG-binding reagent. J. Immunol. 133: 964–974.
Reis, K.J., Ayoub, E.M. and Boyle, M.D.P. 1985. A rapid method for the isolation and characterization of a homogeneous population of streptotoccal Fc receptors. J. Microbiol. Methods. 4: 45–58.
Reis, K.J., Ayoub, E.M. and Boyle, M.D.P. 1984. Streptococcal Fc receptors:II. Comparison of the reactivity of a receptor from a group C streptococcus with staphylococcal protein A. J. Immunol. 132: 3098–3102.
Åkerström, B., Brodin, T., Reis, K.J. and Björck, L. 1985. Protein G: A powerful tool for binding and detection of monoclonal and polyclonal antibodies. J. Immunol. 135: 2589–2592.
Müller, H.-P. and Blobel, H. 1983. Purification and properties of a receptor for the Fc-component of immunoglobulin G from Streptotoccus dysgalactiae. Zbl. Bact. Hyg., I. Abt. Orig. A 254: 352–360.
von Mering, G. and Boyle, M.D.P. 1986. Comparison of type III Fc receptors associated with group C and group G streptococci. Mol. Immunol. 23: 811–821.
Åkerström, B. and Björck, L. 1986. A physicochemical study of protein G, a molecule with unique immunoglobulin G-binding properties. J. Biol. Chem. 261: 10240–10247.
Reis, K.J., Hansen, H.F. and Björck, L. 1986. Extraction and characterization of streptococcal IgG Fc receptors from group C and group G streptococci. Mol. Immunol. 23: 425–431.
Boyle, M.D.P., Wallner, W.A., von Mering, G.O., Reis, K.J., and Lawman, M.J.P. 1985. Interaction of bacterial Fc receptors with goat immunoglobulins. Mol. Immunol. 220: 1115–1121.
Fahnestock, S.R., Alexander, P., Nagle, J. and Filpula, D. 1986. Gene for an immunoglobulin-binding protein from a group G streptococcus. J. Bacteriol. 167: 870–880.
Guss, B., Eliasson, M., Olsson, A., Uhlén, M., Frej, A.-K., Jörnvall, H., Flock, J.-I. and Lindberg, M. 1986. Structure of the IgG-binding regions of streptococcal protein G. EMBO Journal 5: 1567–1575.
Myhre, E.B., Holmberg, O. and Kronvall, G. 1979. Immunolgobulin-binding structures on bovine group G streptococci different from type III Fc receptors on human group G streptococci. Infect. Immun. 23: 1–7.
Myhre, E.B. and Kronvall, G. 1980. Immunochemical aspects of Fc-mediated binding of human IgG subclasses to group A, C and G streptococci. Mol. Immunol. 17: 1563–1573.
Myhre, E.B. and Kronvall, G. 1981. Specific binding of bovine, ovine, caprine and equine IgG subclasses to defined types of immunoglobulin receptors in Gram-positive cocci. Comp. Immun. Microbiol. Infect. Dis. 4: 317–28.
Myhre, E.B. and Kronvall, G. 1980. Demonstration of a new type of immunoglobulin G receptor in Streptococcus zooepidemicus strains. Infect. Immun. 27: 808–816.
Fahnestock, S.R. and Fisher, K.E. 1986. Expression of the staphylococcal protein A gene in Bacillus subtilis by gene fusions utilizing the promoter from a Bacillus amyloliquefaciens α-amylase gene. J. Bacteriol. 165: 796–804.
Nilsson, B., Holmgren, E., Josephson, S., Gatenbeck, S., Philipson, L. and Uhlén, M. 1985. Efficient secretion and purification of human insulin-like growth factor I with a gene fusion vector in Staphylococci. Nucleic Acids. Res. 13: 1151–1162.
Nilsson, B., Abrahmsén and Uhlén, M. 1985. Immunobilization and purification of enzymes with staphylococcal protein A gene fusion vectors. EMBO J. 4: 1075–1080.
Reis, K.J., Boyle, M.D.P. and Ayoub, E.M. 1984. Identification of distinct Fc-receptor molecules on streptococci and Staphylococci. J. Clin. Lab. Immunol. 13: 75–80.
Yarnall, M., Ayoub, E.M. and Boyle, M.D.P. 1986. Analysis of surface receptor expression on bacteria isolated from patients with endocarditis. J. Gen. Microbiol. 132: 2049–2052.
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Boyle, M., Reis, K. Bacterial Fc Receptors. Nat Biotechnol 5, 697–703 (1987). https://doi.org/10.1038/nbt0787-697
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DOI: https://doi.org/10.1038/nbt0787-697
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