A monoclonal immunoglobulin G antibody directed against an immunodominant linear epitope on the ricin A chain confers systemic and mucosal immunity to ricin

Infection and Immunity

Volumn 78, Issue 1, 2010, Pages 552-561

  Neal, Lori M ^a   O'Hara, Joanne ^b   Brey III, Robert N ^c   Mantis, Nicholas J ^a,b  

^a WADSWORTH CENTER   (United States)

^b UNIVERSITY AT ALBANY   (United States)

^c Soligenix   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOTOXIN; NEUTRALIZING ANTIBODY; RECOMBINANT ENZYME; RICIN A;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY BLOOD LEVEL; ANTIBODY PRODUCTION; ANTIGEN BINDING; ARTICLE; ASSAY; BAGG ALBINO MOUSE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; DISSOCIATION CONSTANT; FEMALE; IMMUNITY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PASSIVE IMMUNIZATION; PRIORITY JOURNAL; PURIFICATION; VERO CELL;

ANIMALS; ANTIBODIES, MONOCLONAL; CERCOPITHECUS AETHIOPS; FEMALE; IMMUNITY, MUCOSAL; IMMUNODOMINANT EPITOPES; IMMUNOGLOBULIN G; MICE; MODELS, MOLECULAR; OPEN READING FRAMES; RICIN; VERO CELLS;

EID: 73449123743     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00796-09     Document Type: Article

References (53)

1. Apter, F. M., W. I. Lencer, R. A. Finkelstein, J. J. Mekalanos, and M. R. Neutra. 1993. Monoclonal immunoglobulin A antibodies directed against cholera toxin prevent the toxin-induced chloride secretory response and block toxin binding to intestinal epithelial cells in vitro. Infect. Immun. 61:5271-5278.
2. Atlas, R. M. 2002. Bioterrorism: from threat to reality. Annu. Rev. Microbiol. 56:167-185.
3. Audi, J., M. Belson, M. Patel, J. Schier, and J. Osterloh. 2005. Ricin poisoning: a comprehensive review. JAMA 294:2342-2351.
4. Baenziger, J. U., and D. Fiete. 1979. Structural determinants of Ricinus communis agglutinin and toxin specificity for oligosaccharides. J. Biol. Chem. 254:9795-9799.
5. Burns, J. W., M. Siadat-Pajouh, A. A. Krishnaney, and H. B. Greenberg. 1996. Protective effects of rotavirus VP6-specific IgA monoclonal antibodies that lack neutralizing activity. Science 272:104-107.
6. Carra, J. H., R. W. Wannemacher, R. F. Tammariello, C. Y. Lindsey, R. E. Dinterman, R. D. Schokman, and L. A. Smith. 2007. Improved formulation of a recombinant ricin A-chain vaccine increases its stability and effective antigenicity. Vaccine 25:4149-4158.
7. Castelletti, D., G. Fracasso, S. Righetti, G. Tridente, R. Schnell, A. Engert, and M. Colombatti. 2004. A dominant linear B-cell epitope of ricin A-chain is the target of a neutralizing antibody response in Hodgkin's lymphoma patients treated with an anti-CD25 immunotoxin. Clin. Exp. Immunol. 136: 365-372.
8. Crawford, L. M. 2002. New drug and biological drug products; evidence needed to demonstrate effectiveness of new drugs when human efficacy studies are not ethical or feasible. Fed. Regist. 67:37988-37998.
9. Endo, Y., K. Mitsui, M. Motizuki, and K. Tsurugi. 1987. The mechanism of action of ricin and related toxins on eukaryotic ribosomes. J. Biol. Chem. 262:5908-5912.
10. Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
11. Hewetson, J. F., V. R. Rivera, D. A. Creasia, P. V. Lemley, M. K. Rippy, and M. A. Poli. 1993. Protection of mice from inhaled ricin by vaccination with ricin or by passive treatment with heterologous antibody. Vaccine 11:743-746.
12. Hulse, C. 3 February 2004. Tests indicate poison in Senate mail room of majority leader, p. A12. New York Times, New York, NY.
13. Hutchings, A. B., A. Helander, K. J. Silvey, K. Chandran, W. T. Lucas, M. L. Nibert, and M. R. Neutra. 2004. Secretory immunoglobulin A antibodies against the sigma1 outer capsid protein of reovirus type 1 Lang prevent infection of mouse Peyer's patches. J. Virol. 78:947-957.
14. Katzin, B. J., E. J. Collins, and J. D. Robertus. 1991. Structure of ricin A-chain at 2.5 Å. Proteins 10:251-259.
15. Kelly-Cirino, C. D., and N. J. Mantis. 2009. Neutralizing monoclonal antibodies directed against defined linear epitopes on domain 4 of anthrax protective antigen. Infect. Immun. 77:4859-4867.
16. Kende, M., G. Del Giudice, N. Rivera, and J. Hewetson. 2006. Enhancement of intranasal vaccination in mice with deglycosylated chain A ricin by LTR72, a novel mucosal adjuvant. Vaccine 24:2213-2221.
17. Kim, Y., and J. D. Robertus. 1992. Analysis of several key active site residues of ricin A chain by mutagenesis and X-ray crystallography. Protein Eng. 5:775-779.
18. Krautz-Peterson, G., S. Chapman-Bonofiglio, K. Boisvert, H. Feng, I. M. Herman, S. Tzipori, and A. S. Sheoran. 2008. Intracellular neutralization of Shiga toxin 2 by an a subunit-specific human monoclonal antibody. Infect. Immun. 76:1931-1939.
19. Lebeda, F. J., and M. A. Olson. 1999. Prediction of a conserved, neutralizing epitope in ribosome-inactivating proteins. Int. J. Biol. Macromol. 24:19-26.
20. Lemley, P. V., P. Amanatides, and D. C. Wright. 1994. Identification and characterization of a monoclonal antibody that neutralizes ricin toxicity in vitro and in vivo. Hybridoma 13:417-421.
21. Lord, J. M., E. Deeks, C. J. Marsden, K. Moore, C. Pateman, D. C. Smith, R. A. Spooner, P. Watson, and L. M. Roberts. 2003. Retrograde transport of toxins across the endoplasmic reticulum membrane. Biochem. Soc. Trans. 31:1260-1262.
22. Lycke, N., L. Erlandsson, L. Ekman, K. Schon, and T. Leanderson. 1999. Lack of J chain inhibits the transport of gut IgA and abrogates the development of intestinal antitoxic protection. J. Immunol. 163:913-919.
23. Maddaloni, M., C. Cooke, R. Wilkinson, A. V. Stout, L. Eng, and S. H. Pincus. 2004. Immunological characteristics associated with the protective efficacy of antibodies to ricin. J. Immunol. 172:6221-6228.
24. Maman, M., and Y. Yehezkelli. 2005. Ricin: a possible, non-infectious biological weapon, p. 205-216. In I. W. Fong and K. Alibek (ed.), Bioterrorism and infectious agents. Springer Science and Business Media, New York, NY.
25. Mantis, N. J. 2005. Vaccines against the category B toxins: staphylococcal enterotoxin B, epsilon toxin and ricin. Adv. Drug Deliv. Rev. 57:1424-1439.
26. Mantis, N. J., C. R. McGuinness, O. Sonuyi, G. Edwards, and S. A. Farrant. 2006. Immunoglobulin A antibodies against ricin A and B subunits protect epithelial cells from ricin intoxication. Infect. Immun. 74:3455-3462.
27. McGuinness, C. R., and N. J. Mantis. 2006. Characterization of a novel high-affinity monoclonal immunoglobulin G antibody against the ricin B subunit. Infect. Immun. 74:3463-3470.
28. Michetti, P., M. J. Mahan, J. M. Slauch, J. J. Mekalanos, and M. R. Neutra. 1992. Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium. Infect. Immun. 60:1786-1792.
29. Neuman de Vegvar, H. E., R. R. Amara, L. Steinman, P. J. Utz, H. L. Robinson, and W. H. Robinson. 2003. Microarray profiling of antibody responses against simian-human immunodeficiency virus: postchallenge convergence of reactivities independent of host histocompatibility type and vaccine regimen. J. Virol. 77:11125-11138.
30. Neuman de Vegvar, H. E., and W. H. Robinson. 2004. Microarray profiling of antiviral antibodies for the development of diagnostics, vaccines, and therapeutics. Clin. Immunol. 111:196-201.
31. Olsnes, S., A. M. Pappenheimer, Jr., and R. Meren. 1974. Lectins from Abrus precatorius and Ricinus communis. II. Hybrid toxins and their interaction with chain-specific antibodies. J. Immunol. 113:842-847.
32. Olson, M. A. 1997. Ricin A-chain structural determinant for binding substrate analogues: a molecular dynamics simulation analysis. Proteins 27:80-95.
33. Peterson, D. A., N. P. McNulty, J. L. Guruge, and J. I. Gordon. 2007. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2:328-339.
34. Pincus, S. H., L. Eng, C. L. Cooke, and M. Maddaloni. 2002. Identification of hypoglycemia in mice as a surrogate marker of ricin toxicosis. Comp. Med. 52:530-533.
35. Plotkin, S. A. 2008. Vaccines: correlates of vaccine-induced immunity. Clin. Infect. Dis. 47:401-409.
36. Rapak, A., P. O. Falnes, and S. Olsnes. 1997. Retrograde transport of mutant ricin to the endoplasmic reticulum with subsequent translocation to cytosol. Proc. Natl. Acad. Sci. U. S. A. 94:3783-3788.
37. Roche, J. K., M. K. Stone, L. K. Gross, M. Lindner, R. Seaner, S. H. Pincus, and T. G. Obrig. 2008. Post-exposure targeting of specific epitopes on ricin toxin abrogates toxin-induced hypoglycemia, hepatic injury, and lethality in a mouse model. Lab. Invest. 88:1178-1191.
38. Sandvig, K., S. Grimmer, S. U. Lauvrak, M. L. Torgersen, G. Skretting, B. van Deurs, and T. G. Iversen. 2002. Pathways followed by ricin and Shiga toxin into cells. Histochem. Cell Biol. 117:131-141.
39. Sandvig, K., and B. van Deurs. 2005. Delivery into cells: lessons learned from plant and bacterial toxins. Gene Ther. 12:865-872.
40. Schier, J. G., M. M. Patel, M. G. Belson, A. Patel, M. Schwartz, N. Fitzpatrick, D. Drociuk, S. Deitchman, R. Meyer, T. Litovitz, W. A. Watson, C. H. Rubin, and M. Kiefer. 2007. Public health investigation after the discovery of ricin in a South Carolina postal facility. Am. J. Public Health 97(Suppl. 1):S152-S157.
41. Silvey, K. J., A. B. Hutchings, M. Vajdy, M. M. Petzke, and M. R. Neutra. 2001. Role of immunoglobulin A in protection against reovirus entry into murine Peyer's patches. J. Virol. 75:10870-10879.
42. Smallshaw, J. E., A. Firan, J. R. Fulmer, S. L. Ruback, V. Ghetie, and E. S. Vitetta. 2002. A novel recombinant vaccine which protects mice against ricin intoxication. Vaccine 20:3422-3427.
43. Smallshaw, J. E., V. Ghetie, J. Rizo, J. R. Fulmer, L. L. Trahan, M. A. Ghetie, and E. S. Vitetta. 2003. Genetic engineering of an immunotoxin to eliminate pulmonary vascular leak in mice. Nat. Biotechnol. 21:387-391.
44. Smallshaw, J. E., J. A. Richardson, S. Pincus, J. Schindler, and E. S. Vitetta. 2005. Preclinical toxicity and efficacy testing of RiVax, a recombinant protein vaccine against ricin. Vaccine 23:4775-4784.
45. Smallshaw, J. E., J. A. Richardson, and E. S. Vitetta. 2007. RiVax, a recombinant ricin subunit vaccine, protects mice against ricin delivered by gavage or aerosol. Vaccine 25:7459-7469.
46. Smith, M. J., A. R. Melton-Celsa, J. F. Sinclair, H. M. Carvalho, C. M. Robinson, and A. D. O'Brien. 2009. Monoclonal antibody 11E10, which neutralizes Shiga toxin type 2 (Stx2), recognizes three regions on the Stx2 A subunit, blocks the enzymatic action of the toxin in vitro, and alters the overall cellular distribution of the toxin. Infect. Immun. 77:2730-2740.
47. Stirpe, F. 2004. Ribosome-inactivating proteins. Toxicon 44:371-383.
48. Stone, R. 2002. Biodefense. Peering into the shadows: Iraq's bioweapons program. Science 297:1110-1112.
49. Sullivan, N. J., J. E. Martin, B. S. Graham, and G. J. Nabel. 2009. Correlates of protective immunity for Ebola vaccines: implications for regulatory approval by the animal rule. Nat. Rev. Microbiol. 7:393-400.
50. Tommasi, M., D. Castelletti, M. Pasti, G. Fracasso, I. Lorenzetti, S. Sartoris, C. Pera, G. B. Ferrara, G. Tridente, and M. Colombatti. 2001. Identification of ricin A-chain HLA class II-restricted epitopes by human T-cell clones. Clin. Exp. Immunol. 125:391-400.
51. Uren, T. K., O. L. Wijburg, C. Simmons, F. E. Johansen, P. Brandtzaeg, and R. A. Strugnell. 2005. Vaccine-induced protection against gastrointestinal bacterial infections in the absence of secretory antibodies. Eur. J. Immunol. 35:180-188.
52. Vitetta, E. S., J. E. Smallshaw, E. Coleman, H. Jafri, C. Foster, R. Munford, and J. Schindler. 2006. A pilot clinical trial of a recombinant ricin vaccine in normal humans. Proc. Natl. Acad. Sci. U. S. A. 103:2268-2273.
53. Yoder, J. M., R. U. Aslam, and N. J. Mantis. 2007. Evidence for widespread epithelial damage and coincident production of monocyte chemotactic protein 1 in a murine model of intestinal ricin intoxication. Infect. Immun. 75:1745-1750.