IgG Subclass and Heavy Chain Domains Contribute to Binding and Protection by mAbs to the Poly γ-D-glutamic Acid Capsular Antigen of Bacillus anthracis

PLoS Pathogens

Volumn 9, Issue 4, 2013, Pages

  Hovenden, Maria ^a   Hubbard, Mark A ^a   AuCoin, David P ^a   Thorkildson, Peter ^a   Reed, Dana E ^a   Welch, William H ^a   Lyons, C Rick ^b,c   Lovchik, Julie A ^b   Kozel, Thomas R ^a  

^a UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

^c Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G3; MONOCLONAL ANTIBODY; POLYGLUTAMIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTHRAX; ARTICLE; BACILLUS ANTHRACIS; BACILLUS LICHENIFORMIS; BEHAVIOR; BINDING AFFINITY; CONTROLLED STUDY; CORRELATION ANALYSIS; DISSOCIATION CONSTANT; ELECTRIC POTENTIAL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE; GEL PERMEATION CHROMATOGRAPHY; HEAVY CHAIN; IMMUNOCHEMISTRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; SURFACE PLASMON RESONANCE;

ANIMALS; ANTHRAX; ANTIBODIES, MONOCLONAL; ANTIBODY AFFINITY; ANTIGEN-ANTIBODY REACTIONS; BACILLUS ANTHRACIS; BACTERIAL CAPSULES; GLUTAMIC ACID; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN CONSTANT REGIONS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAINS; MICE; MICE, INBRED BALB C; PROTEIN STRUCTURE, TERTIARY;

BACILLUS ANTHRACIS; BACTERIA (MICROORGANISMS); MURINAE;

EID: 84876834017     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003306     Document Type: Article

References (53)

1. Mock M, Fouet A, (2001) Anthrax. Annu Rev Microbiol 55: 647-671.
2. Mikesell P, Ivins BE, Ristroph JD, Dreier TM, (1983) Evidence for plasmid-mediated toxin production in Bacillus anthracis. Infect Immun 39: 371-376.
3. Green BD, Battisti L, Koehler TM, Thorne CB, Ivins BE, (1985) Demonstration of a capsule plasmid in Bacillus anthracis. Infect Immun 49: 291-297.
4. Beall FA, Taylor MJ, Thorne CB, (1962) Rapid lethal effects in rats of a third component found upon fractionating the toxin of Bacillus anthracis. J Bacteriol 83: 1274-1280.
5. Stanley JL, Smith H, (1961) Purification of factor I and recognition of a third factor of the anthrax toxin. J Gen Microbiol 26: 49-66.
6. Zwartouw HT, Smith H, (1956) Polyglutamic acid from Bacillus anthracis grown in vivo: structure and agressin activity. Biochem J 63: 437-442.
7. Goodman JW, Nitecki DE, (1967) Studies on the relation of a prior immune response to immunogenicity. Immunology 13: 577-583.
8. Wang TT, Lucas AH, (2004) The capsule of Bacillus anthracis behaves as a thymus-independent type 2 antigen. Infect Immun 72: 5460-5463.
9. Makino S, Uchida I, Terakado N, Sasakawa C, Yoshikawa M, (1989) Molecular characterization and protein analysis of the cap region, which is essential for encapsulation in Bacillus anthracis. J Bacteriol 171: 722-730.
10. Puziss M, Manning LC, Lynch JW, Barclay E, Abelow I, et al. (1963) Large-scale production of protective antigen of Bacillus anthracis in anaerobic cultures. Appl Microbiol 11: 330-334.
11. Schneerson R, Kubler-Kielb J, Liu T-Y, Dai Z, Leppla SH, et al. (2003) Poly(γ-D-glutamic acid) protein conjugates induce IgG antibodies in mice to the capsule of Bacillus anthracis: a potential addition to the anthrax vaccine. Proc Natl Acad Sci U S A 100: 8945-8950.
12. Rhie GE, Roehrl MH, Mourez M, Collier RJ, Mekalanos JJ, et al. (2003) A dually active anthrax vaccine that confers protection against both bacilli and toxins. Proc Natl Acad Sci U S A 100: 10925-10930.
13. Kozel TR, Murphy WJ, Brandt S, Blazar BR, Lovchik JA, et al. (2004) mAbs to Bacillus anthracis capsular antigen for immunoprotection in anthrax and detection of antigenemia. Proc Natl Acad Sci U S A 101: 5042-5047.
14. Kozel TR, Thorkildson P, Brandt S, Welch WH, Lovchik JA, et al. (2007) Protective and immunochemical activities of monoclonal antibodies reactive with the Bacillus anthracis polypeptide capsule. Infect Immun 75: 152-163.
15. Chabot DJ, Scorpio A, Tobery SA, Little SF, Norris SL, et al. (2004) Anthrax capsule vaccine protects against experimental infection. Vaccine 23: 43-47.
16. Joyce J, Cook J, Chabot DJ, Hepler R, Shoop W, et al. (2006) Immunogenicity and protective efficacy of Bacillus anthracis poly-γ-D-glutamic acid capsule covalently coupled to a protein carrier using a novel triazine-based conjugation strategy. J Biol Chem 281: 4831-4843.
17. Wang TT, Fellows PF, Leighton TJ, Lucas AH, (2004) Induction of opsonic antibodies to the gamma-D-glutamic acid capsule of Bacillus anthracis by immunization with a synthetic peptide-carrier protein conjugate. FEMS Immunol Med Microbiol 40: 231-237.
18. Spira G, Bargellesi A, Teillaud JL, Scharff MD, (1984) The identification of monoclonal class switch variants by sib selection and an ELISA assay. J Immunol Methods 74: 307-315.
19. Akahori Y, Kurosawa Y, (1997) Nucleotide sequences of all the gamma gene loci of murine immunoglobulin heavy chains. Genomics 41: 100-104.
20. Neufeld F, (1902) Ueber die agglutination der pneumokokken und uber die theorie der agglutination. Zeit f Hyg u Infektionskr 40: 54-72.
21. MacGill TC, MacGill RS, Casadevall A, Kozel TR, (2000) Biological correlates of capsular (quellung) reactions of Cryptococcus neoformans. J Immunol 164: 4835-4842.
22. Torres M, Casadevall A, (2007) The immunoglobulin constant region contributes to affinity and specificity. Trends Immunol 29: 91-97.
23. Karush F, (1976) Multivalent binding and functional affinity. Contemp Top Mol Immunol 5: 217-228.
24. Greenspan NS, (2001) Affinity, complementarity, cooperativity, and specificity in antibody recognition. Curr Top Microbiol Immunol 260: 65-85.
25. Chen Z, Schneerson R, Lovchik J, Lyons CR, Zhao H, et al. (2011) Pre- and postexposure protection against virulent anthrax infection in mice by humanized monoclonal antibodies to Bacillus anthracis capsule. Proc Natl Acad Sci U S A 108: 739-744.
26. Robbins JB, Schneerson R, Szu SC, Fattom A, Yang Y, et al. (1989) Prevention of invasive bacterial diseases by immunization with polysaccharide-protein conjugates. Curr Top Microbiol Immunol 146: 169-180.
27. Perlmutter RM, Hansburd D, Briles DE, Nicolotti RA, Davie JM, (1978) Subclass restriction of murine anti-carbohydrate antibodies. J Immunol 121: 566-577.
28. Slack J, DerBalian GP, Nahm M, Davie JM, (1980) Subclass restriction of murine antibodies: II. The IgG plaque forming cell response to thymus-independent type 1 and type 2 antigens in normal mice and mice expressing an X-linked immunodeficiency. J Exp Med 151: 853-862.
29. Scott MG, Shackelford PG, Briles DE, Nahm MH, (1988) Human IgG subclasses and their relation to carbohydrate antigen immunocompetence. Diagn Clin Immunol 5: 241-245.
30. Greenspan NS, Cooper LJN, (1992) Intermolecular cooperativity: a clue to why mice have IgG3. Immunol Today 13: 164-168.
31. Tudor D, Yu H, Maupetit J, Drillet A-S, Bouceba T, et al. (2012) Isotype modulates epitope specificity, affinity, and antiviral activities of anti-HIV-1 human broadly neutralizing 2F5 antibody. Proc Natl Acad Sci U S A 109: 12680-12685.
32. Yuan R, Casadevall A, Spira G, Scharff MD, (1995) Isotype switching from IgG3 to IgG1 converts a nonprotective murine antibody to Cryptococcus neoformans into a protective antibody. J Immunol 154: 1810-1816.
33. Yuan RR, Spira G, Oh J, Paizi M, Casadevall A, et al. (1998) Isotype switching increases efficacy of antibody protection against Cryptococcus neoformans infection in mice. Infect Immun 66: 1057-1062.
34. Torres M, Fernandez-Fuentes N, Fiser A, Casadevall A, (2007) The immunoglobulin heavy chain constant region affects kinetic and thermodynamic parameters of antibody variable region interactions with antigen. J Biol Chem 282: 13917-13927.
35. Cooper LJN, Schimenti JC, Glass DD, Greenspan NS, (1991) H chain C domains influence the strength of binding of IgG for streptococcal group A carbohydrate. J Immunol 146: 2659-2663.
36. Schreiber JR, Cooper LJ, Diehn S, Dahlhauser PA, Tosi MF, et al. (1993) Variable region-identical monoclonal antibodies of different IgG subclass directed to Pseudomonas aeruginosa lipopolysaccharide O-specific side chain function differently. J Infect Dis 167: 221-226.
37. Cooper LJ, Robertson D, Granzow R, Greenspan NS, (1994) Variable domain-identical antibodies exhibit IgG subclass-related differences in affinity and kinetic constants as determined by surface plasmon resonance. Mol Immunol 31: 577-584.
38. Morelock MM, Rothlein R, Bright S, Robinson MK, Graham ET, et al. (1994) Isotype choice for chimeric antibodies affects binding properties. J Biol Chem 269: 13048-13055.
39. Dangl JL, Wensel TG, Morrison SL, Stryer L, Herzenberg LA, et al. (1988) Segmental flexibility and complement fixation of genetically engineered chimeric human, rabbit and mouse antibodies. EMBO J 7: 1989-1994.
40. Cooper LJN, Robertson D, Granzow R, Greenspan NS, (1994) Variable domain-identical antibodies exhibit IgG subclass-related differences in affinity and kinetic constants as determined by surface plasmon resonance. Mol Immunol 31: 577-584.
41. Cooper LJN, Shikhman AR, Glass DD, Kangisser D, Cunningham MW, et al. (1993) Role of heavy chain constant domains in antibody-antigen interaction. Apparent specificity differences among streptococcal IgG antibodies expressing identical variable regions. J Immunol 150: 2231-2242.
42. Greenspan NS, Cooper LJN, (1993) Cooperative binding by mouse IgG3 antibodies: implications for functional affinity, effector function, and isotype restriction. Springer Semin Immunopathol 15: 275-291.
43. Huang C-M, Huang H-JS, Lee S-C, (1984) Detection of immunoglobulin heavy chain IgG3 polymorphism in wild mice with xenogenic monoclonal antibodies. Immunogenetics 20: 565-575.
44. Amor M, Bonhomme F, Guenet J-L, Petter F, Cazenave P-A, (1984) Polymorphism of heavy chain immunoglobulin isotypes in the mus gubgenus I. Limited γ3 polymorphism revealed by antibodies raised in SPE wild-derived strain. Immunogenetics 20: 577-581.
45. Casadevall A, Janda A, (2012) Immunoglobulin isotype influences affinity and specificity. Proc Natl Acad Sci U S A 109: 12272-12273.
46. Janda A, Eryilmaz E, Nakouzi A, Cowburn D, Casadevall A, (2012) Variable region identical immunoglobulins differing in isotype express different paratopes. J Biol Chem 287: 35409-35417.
47. Neuberger MS, Rajewsky K, (1981) Activation of mouse complement by monoclonal mouse antibodies. Eur J Immunol 11: 1012-1016.
48. Nimmerjahn F, Bruhns P, Horiuchi K, Ravetch JV, (2005) FcγRIV: A novel FcR with distinct IgG subclass specificity. Immunity 23: 41-51.
49. Gavin AL, Barnes HM, Dijstelbloem HM, Hogarth PM, (1998) Identification of the mouse IgG3 receptor: implications for antibody effector function at the interface between innate and adaptive immunity. J Immunol 160: 20-23.
50. Bruhns P, (2012) Properties of mouse and human IgG receptors and their contribution to disease models. Blood 119: 5640-5649.
51. Torres M, May R, Scharff MD, Casadevall A, (2005) Variable-region-identical antibodies differing in isotype demonstrate differences in fine specificity and idiotype. J Immunol 174: 2132-2142.
52. Leonard CG, Housewright RD, Thorne CB, (1958) Effects of some metallic ions on glutamyl polypeptide synthesis by Bacillus subtilis. J Bacteriol 76: 499-503.
53. MacKenzie CR, Hirama T, Deng SJ, Bundle DR, Narang SA, et al. (1996) Analysis by surface plasmon resonance of the influence of valence on the ligand binding affinity and kinetics of an anti-carbohydrate antibody. J Biol Chem 271: 1527-1533.