Isotype switching increases efficacy of antibody protection against staphylococcal enterotoxin B-induced lethal shock and Staphylococcus aureus sepsis in mice

mBio

Volumn 5, Issue 3, 2014, Pages

  Varshney, Avanish K ^a   Wang, Xiaobo ^a   Aguilar, Jorge L ^a   Scharff, Matthew D ^a   Fries, Bettina C ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; IMMUNOGLOBULIN CLASS; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY IGG2B; STAPHYLOCOCCUS ENTEROTOXIN B; UNCLASSIFIED DRUG; BACTERIUM ANTIBODY; ENTEROTOXIN; ENTEROTOXIN B, STAPHYLOCOCCAL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; BINDING AFFINITY; CELLULAR IMMUNITY; DRUG DESIGN; DRUG EFFICACY; DRUG PROTEIN BINDING; FEMALE; GENE REARRANGEMENT; IC 50; IMMUNE RESPONSE; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; LETHALITY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SHOCK; STAPHYLOCOCCAL BACTEREMIA; ANIMAL; BACTEREMIA; BAGG ALBINO MOUSE; GENETICS; HUMAN; IMMUNOLOGY; MICROBIOLOGY; SEPSIS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TOXICITY;

ANIMALS; ANTIBODIES, BACTERIAL; BACTEREMIA; ENTEROTOXINS; FEMALE; HUMANS; IMMUNOGLOBULIN CLASS SWITCHING; MICE; MICE, INBRED BALB C; SEPSIS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84903956909     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01007-14     Document Type: Article

References (49)

1. Hamad AR, Herman A, Marrack P, Kappler JW. 1994. Monoclonal antibodies defining functional sites on the toxin superantigen staphylococcal enterotoxin B. J. Exp. Med. 180: 615-621. http://dx. doi. org/10. 1084/jem. 180. 2. 615.
2. Varshney AK, Wang X, Cook E, Dutta K, Scharff MD, Goger MJ, Fries BC. 2011. Generation, characterization, and epitope mapping of neutralizing and protective monoclonal antibodies against staphylococcal enterotoxin B-induced lethal shock. J. Biol. Chem. 286: 9737-9747. http://dx. doi. org/10. 1074/jbc. M110. 212407.
3. LeClaire RD, Hunt RE, Bavari S. 2002. Protection against bacterial superantigen staphylococcal enterotoxin B by passive vaccination. Infect. Immun. 70: 2278-2281. http://dx. doi. org/10. 1128/IAI. 70. 5. 2278-2281. 2002.
4. Tilahun ME, Rajagopalan G, Shah-Mahoney N, Lawlor RG, Tilahun AY, Xie C, Natarajan K, Margulies DH, Ratner DI, Osborne BA, Goldsby RA. 2010. Potent neutralization of staphylococcal enterotoxin B by synergistic action of chimeric antibodies. Infect. Immun. 78: 2801-2811. http://dx. doi. org/10. 1128/IAI. 01121-09.
5. Larkin EA, Stiles BG, Ulrich RG. 2010. Inhibition of toxic shock by human monoclonal antibodies against staphylococcal enterotoxin B. PLoS One 5: e13253. http://dx. doi. org/10. 1371/journal. pone. 0013253.
6. Drozdowski B, Zhou Y, Kline B, Spidel J, Chan YY, Albone E, Turchin H, Chao Q, Henry M, Balogach J, Routhier E, Bavari S, Nicolaides NC, Sass PM, Grasso L. 2010. Generation and characterization of high affinity human monoclonal antibodies that neutralize staphylococcal enterotoxin B. J. Immune Based Ther. Vaccines 8: 9. http://dx. doi. org/10. 1186/1476-8518-8-9.
7. Varshney AK, Wang X, Scharff MD, Macintyre J, Zollner RS, Kovalenko OV, Martinez LR, Byrne FR, Fries BC. 2013. Staphylococcal enterotoxin B-specific monoclonal antibody 20B1 successfully treats diverse Staphylococcus aureus infections. J. Infect. Dis. 208: 2058-2066. http://dx. doi. org/10. 1093/infdis/jit421.
8. Leavy O. 2010. Therapeutic antibodies: past, present and future. Nat. Rev. Immunol. 10: 297. http://dx. doi. org/10. 1038/nri2763.
9. The IMpact-RSV Study Group. 1998. Palivizumab, a humanized respiratory syncytial virus monoclonal antibody, reduces hospitalization from respiratory syncytial virus infection in high-risk infants. Pediatrics 102: 531-537.
10. Goldenberg MM. 2013. Pharmaceutical approval update. PT 38: 86-95.
11. Ravetch JV, Kinet JP. 1991. Fc receptors. Annu. Rev. Immunol. 9: 457-492. http://dx. doi. org/10. 1146/annurev. iy. 09. 040191. 002325.
12. Neuberger MS, Rajewsky K. 1981. Activation of mouse complement by monoclonal mouse antibodies. Eur. J. Immunol. 11: 1012-1016. http://dx. doi. org/10. 1002/eji. 1830111212.
13. Gessner JE, Heiken H, Tamm A, Schmidt RE. 1998. The IgG Fc receptor family. Ann. Hematol. 76: 231-248. http://dx. doi. org/10. 1007/s002770050396.
14. Nimmerjahn F, Bruhns P, Horiuchi K, Ravetch JV. 2005. FcgammaRIV: a novel FcR with distinct IgG subclass specificity. Immunity 23: 41-51. http://dx. doi. org/10. 1016/j. immuni. 2005. 05. 010.
15. Nimmerjahn F, Ravetch JV. 2005. Divergent immunoglobulin G subclass activity through selective Fc receptor binding. Science 310: 1510-1512. http://dx. doi. org/10. 1126/science. 1118948.
16. Pirofski LA, Casadevall A. 2008. The damage-response framework of microbial pathogenesis and infectious diseases. Adv. Exp. Med. Biol. 635: 135-146. http://dx. doi. org/10. 1007/978-0-387-09550-9_11.
17. Nimmerjahn F, Ravetch JV. 2007. Fc-receptors as regulators of immunity. Adv. Immunol. 96: 179-204. http://dx. doi. org/10. 1016/S0065-2776(07)96005-8.
18. Cook E, Wang X, Robiou N, Fries BC. 2007. Measurement of staphylococcal enterotoxin B in serum and culture supernatant with a capture enzyme-linked immunosorbent assay. Clin. Vaccine Immunol. 14: 1094-1101. http://dx. doi. org/10. 1128/CVI. 00183-07.
19. Rapoport MI, Hodoval LF, Grogan EW, McGann V, Beisel WR. 1966. The influence of specific antibody on the disappearance of staphylococcal enterotoxin B from blood. J. Clin. Invest. 45: 1365-1372. http://dx. doi. org/10. 1172/JCI105444.
20. Vabulas R, Bittlingmaier R, Heeg K, Wagner H, Miethke T. 1996. Rapid clearance of the bacterial superantigen staphylococcal enterotoxin B in vivo. Infect. Immun. 64: 4567-4573.
21. Langley R, Patel D, Jackson N, Clow F, Fraser JD. 2010. Staphylococcal superantigen super-domains in immune evasion. Crit. Rev. Immunol. 30: 149-165. http://dx. doi. org/10. 1615/CritRevImmunol. v30. i2. 40.
22. Otto M. 2012. MRSA virulence and spread. Cell. Microbiol. 14: 1513-1521. http://dx. doi. org/10. 1111/j. 1462-5822. 2012. 01832. x.
23. Foster TJ. 2005. Immune evasion by staphylococci. Nat. Rev. Microbiol. 3: 948-958. http://dx. doi. org/10. 1038/nrmicro1289.
24. Goldman DL, Casadevall A. 2008. Anthrax-associated shock. Front. Biosci. 13: 4009-4014.
25. Pinchuk IV, Beswick EJ, Reyes VE. 2010. Staphylococcal enterotoxins. Toxins 2: 2177-2197. http://dx. doi. org/10. 3390/toxins2082177.
26. Fraser JD. 2011. Clarifying the mechanism of superantigen toxicity. PLoS Biol. 9: e1001145. http://dx. doi. org/10. 1371/journal. pbio. 1001145.
27. Buonpane RA, Churchill HR, Moza B, Sundberg EJ, Peterson ML, Schlievert PM, Kranz DM. 2007. Neutralization of staphylococcal enterotoxin B by soluble, high-affinity receptor antagonists. Nat. Med. 13: 725-729. http://dx. doi. org/10. 1038/nm1584.
28. Xia T, Liang S, Wang H, Hu S, Sun Y, Yu X, Han J, Li J, Guo S, Dai J, Lou Z, Guo Y. 2014. Structural basis for the neutralization and specificity of staphylococcal enterotoxin B against its MHC class II binding site. MAbs 6: 119-129. http://dx. doi. org/10. 4161/mabs. 27106.
29. Karauzum H, Chen G, Abaandou L, Mahmoudieh M, Boroun AR, Shulenin S, Devi VS, Stavale E, Warfield KL, Zeitlin L, Roy CJ, Sidhu SS, Aman MJ. 2012. Synthetic human monoclonal antibodies toward staphylococcal enterotoxin B (SEB) protective against toxic shock syndrome. J. Biol. Chem. 287: 25203-25215. http://dx. doi. org/10. 1074/jbc. M112. 364075.
30. Whitmore AC, Prowse DM, Haughton G, Arnold LW. 1991. Ig isotype switching in B lymphocytes. The effect of T cell-derived interleukins, cytokines, cholera toxin, and antigen on isotype switch frequency of a cloned B cell lymphoma. Int. Immunol. 3: 95-103. http://dx. doi. org/10. 1093/intimm/3. 1. 95.
31. Correia IR. 2010. Stability of IgG isotypes in serum. MAbs 2:-221-232. http://dx. doi. org/10. 4161/mabs. 2. 3. 11788.
32. Bernstein ID, Tam MR, Nowinski RC. 1980. Mouse leukemia: therapy with monoclonal antibodies against a thymus differentiation antigen. Science 207: 68-71. http://dx. doi. org/10. 1126/science. 6965328.
33. Herlyn D, Koprowski H. 1982. IgG2a monoclonal antibodies inhibit human tumor growth through interaction with effector cells. Proc. Natl. Acad. Sci. U. S. A. 79: 4761-4765. http://dx. doi. org/10. 1073/pnas. 79. 15. 4761.
34. Seto M, Takahashi T, Nakamura S, Matsudaira Y, Nishizuka Y. 1983. In vivo antitumor effects of monoclonal antibodies with different immunoglobulin classes. Cancer Res. 43: 4768-4773.
35. Wahl RL, Wissing JR, Kaminski MS. 1989. Isotype switch variant antiidiotype monoclonal antibodies: comparative radiolabeling and in vitro binding. J. Nucl. Med. 30: 227-232.
36. Baldridge JR, Buchmeier MJ. 1992. Mechanisms of antibody-mediated protection against lymphocytic choriomeningitis virus infection: motherto-baby transfer of humoral protection. J. Virol. 66: 4252-4257.
37. Markine-Goriaynoff D, Coutelier JP. 2002. Increased efficacy of the immunoglobulin G2a subclass in antibody-mediated protection against lactate dehydrogenase-elevating virus-induced polioencephalomyelitis revealed with switch mutants. J. Virol. 76: 432-435. http://dx. doi. org/10. 1128/JVI. 76. 1. 432-435. 2002.
38. Yuan RR, Spira G, Oh J, Paizi M, Casadevall A, Scharff MD. 1998. Isotype switching increases efficacy of antibody protection against Cryptococcus neoformans infection in mice. Infect. Immun. 66: 1057-1062.
39. Liu F, Bergami PL, Duval M, Kuhrt D, Posner M, Cavacini L. 2003. Expression and functional activity of isotype and subclass switched human monoclonal antibody reactive with the base of the V3 loop of HIV-1 gp120. AIDS Res. Hum. Retroviruses 19: 597-607. http://dx. doi. org/10. 1089/088922203322230969.
40. Cavacini LA, Kuhrt D, Duval M, Mayer K, Posner MR. 2003. Binding and neutralization activity of human IgG1 and IgG3 from serum of HIVinfected individuals. AIDS Res. Hum. Retroviruses 19: 785-792. http://dx. doi. org/10. 1089/088922203769232584.
41. Abboud N, Chow SK, Saylor C, Janda A, Ravetch JV, Scharff MD, Casadevall A. 2010. A requirement for Fc_R in antibody-mediated bacterial toxin neutralization. J. Exp. Med. 207: 2395-2405. http://dx. doi. org/10. 1084/jem. 20100995.
42. Varshney AK, Wang X, Macintyre J, Zollner RS, Kelleher K, Kovalenko OV, Pechuan X, Byrne FR, Fries BC. 5 May 2014. Humanized staphylococcal enterotoxin B (SEB)-specific monoclonal antibodies protect from SEB intoxication and Staphylococcus aureus infections alone or as adjunctive therapy with vancomycin. J. Infect. Dis. http://dx. doi. org/10. 1093/infdis/jiu198.
43. Hovenden M, Hubbard MA, Aucoin DP, Thorkildson P, Reed DE, Welch WH, Lyons CR, Lovchik JA, Kozel TR. 2013. IgG subclass and heavy chain domains contribute to binding and protection by MAbs to the poly gamma-D-glutamic acid capsular antigen of Bacillus anthracis. PLoS Pathog. 9: e1003306. doi: http://dx. doi. org/10. 1371/journal. ppat. 1003306.
44. Hubbard MA, Thorkildson P, Kozel TR, AuCoin DP. 2013. Constant domains influence binding of mouse-human chimeric antibodies to the capsular polypeptide of Bacillus anthracis. Virulence 4:-483-488. http://dx. doi. org/10. 4161/viru. 25711.
45. Bournazos S, Chow SK, Abboud N, Casadevall A, Ravetch JV. 2014. Human IgG Fc domain engineering enhances antitoxin neutralizing antibody activity. J. Clin. Invest. 124:-725-729. http://dx. doi. org/10. 1172/JCI72676.
46. Varshney AK, Mediavilla JR, Robiou N, Guh A, Wang X, Gialanella P, Levi MH, Kreiswirth BN, Fries BC. 2009. Diverse enterotoxin gene profiles among clonal complexes of Staphylococcus aureus isolates from the Bronx, New York. Appl. Environ. Microbiol. 75: 6839-6849. http://dx. doi. org/10. 1128/AEM. 00272-09.
47. Greene G, Hodous J, Dintzis RZ, Dintzis HM. 1990. Modification, optimization and simplification of the spot ELISA technique for the enumeration of cells secreting anti-hapten antibodies. J. Immunol. Methods 129: 187-197. http://dx. doi. org/10. 1016/0022-1759(90)90438-2.
48. Spira G, Scharff MD. 1992. Identification of rare immunoglobulin switch variants using the ELISA spot assay. J. Immunol. Methods 148: 121-129. http://dx. doi. org/10. 1016/0022-1759(92)90165-P.
49. Zhang W, Bardwell PD, Woo CJ, Poltoratsky V, Scharff MD, Martin A. 2001. Clonal instability of V region hypermutation in the Ramos Burkitt's lymphoma cell line. Int. Immunol. 13: 1175-1184. http://dx. doi. org/10. 1093/intimm/13. 9. 1175.