Adenovirus-based vaccination against Clostridium difficile toxin A allows for rapid humoral immunity and complete protection from toxin A lethal challenge in mice

Vaccine

Volumn 30, Issue 8, 2012, Pages 1492-1501

  Seregin, Sergey S ^a   Aldhamen, Yasser A ^a   Rastall, David P W ^a   Godbehere, Sarah ^a   Amalfitano, Andrea ^a,b  

^a Michigan State University ^*  (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Antibody responses; Challenge model; Clostridium difficile; Recombinant Adenovirus; T cell responses; Vaccine

Indexed keywords

ADENOVIRUS VECTOR; BACTERIAL VACCINE; CLOSTRIDIUM DIFFICILE TOXIN A; EPITOPE; IMMUNOGLOBULIN G; RECOMBINANT ADENOVIRUS VECTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR IMMUNITY; CLOSTRIDIUM DIFFICILE INFECTION; CONTROLLED STUDY; DRUG FORMULATION; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNIZATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ADENOVIRIDAE; ANIMALS; ANTITOXINS; BACTERIAL TOXINS; BACTERIAL VACCINES; CLOSTRIDIUM INFECTIONS; DISEASE MODELS, ANIMAL; DRUG CARRIERS; ENTEROTOXINS; EPITOPES, T-LYMPHOCYTE; IMMUNITY, CELLULAR; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; POISONING; SURVIVAL ANALYSIS; VACCINATION;

EID: 84856570281     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.12.064     Document Type: Article

References (56)

1. Pechine S., Janoir C., Collignon A. Variability of Clostridium difficile surface proteins and specific serum antibody response in patients with Clostridium difficile-associated disease. J Clin Microbiol 2005, 43(October (10)):5018-5025.
2. Ghose C., Kalsy A., Sheikh A., Rollenhagen J., John M., Young J., et al. Transcutaneous immunization with Clostridium difficile toxoid A induces systemic and mucosal immune responses and toxin A-neutralizing antibodies in mice. Infect Immun 2007, 75(June (6)):2826-2832.
3. Pechine S., Janoir C., Boureau H., Gleizes A., Tsapis N., Hoys S., et al. Diminished intestinal colonization by Clostridium difficile and immune response in mice after mucosal immunization with surface proteins of Clostridium difficile. Vaccine 2007, 25(May (20)):3946-3954.
4. Aslam S., Hamill R.J., Musher D.M. Treatment of Clostridium difficile-associated disease: old therapies and new strategies. Lancet Infect Dis 2005, 5(September (9)):549-557.
5. Hookman P., Barkin J.S. Clostridium difficile associated infection, diarrhea and colitis. World J Gastroenterol 2009, 15(April (13)):1554-1580.
6. Gerding D.N., Muto C.A., Owens R.C. Treatment of Clostridium difficile infection. Clin Infect Dis 2008, 46(January (Suppl. 1)):S32-S42.
7. Giannasca P.J., Warny M. Active and passive immunization against Clostridium difficile diarrhea and colitis. Vaccine 2004, 22(February (7)):848-856.
8. Wright A., Drudy D., Kyne L., Brown K., Fairweather N.F. Immunoreactive cell wall proteins of Clostridium difficile identified by human sera. J Med Microbiol 2008, 57(June (Pt 6)):750-756.
9. Savidge T.C., Pan W.H., Newman P., O'Brien M., Anton P.M., Pothoulakis C. Clostridium difficile toxin B is an inflammatory enterotoxin in human intestine. Gastroenterology 2003, 125(August (2)):413-420.
10. Hamm E.E., Voth D.E., Ballard J.D. Identification of Clostridium difficile toxin B cardiotoxicity using a zebrafish embryo model of intoxication. Proc Natl Acad Sci USA 2006, 103(September (38)):14176-14181.
11. Johnson S., Kent S.A., O'Leary K.J., Merrigan M.M., Sambol S.P., Peterson L.R., et al. Fatal pseudomembranous colitis associated with a variant clostridium difficile strain not detected by toxin A immunoassay. Ann Intern Med 2001, 135(September (6)):434-438.
12. Jacob S.S., Sebastian J.C., Hiorns D., Jacob S., Mukerjee P.K. Clostridium difficile and acute respiratory distress syndrome. Heart Lung 2004, 33(July-August (4)):265-268.
13. Sougioultzis S., Kyne L., Drudy D., Keates S., Maroo S., Pothoulakis C., et al. Clostridium difficile toxoid vaccine in recurrent C. difficile-associated diarrhea. Gastroenterology 2005, 128(March (3)):764-770.
14. Gardiner D.F., Rosenberg T., Zaharatos J., Franco D., Ho D.D. A DNA vaccine targeting the receptor-binding domain of Clostridium difficile toxin A. Vaccine 2009, 27(June (27)):3598-3604.
15. Castagliuolo I., Sardina M., Brun P., DeRos C., Mastrotto C., Lovato L., et al. Clostridium difficile toxin A carboxyl-terminus peptide lacking ADP-ribosyltransferase activity acts as a mucosal adjuvant. Infect Immun 2004, 72(May (5)):2827-2836.
16. Brun P., Scarpa M., Grillo A., Palu G., Mengoli C., Zecconi A., et al. Clostridium difficile TxAC314 and SLP-36kDa enhance the immune response toward a co-administered antigen. J Med Microbiol 2008, 57(June (Pt 6)):725-731.
17. Kotloff K.L., Wasserman S.S., Losonsky G.A., Thomas W., Nichols R., Edelman R., et al. Safety and immunogenicity of increasing doses of a Clostridium difficile toxoid vaccine administered to healthy adults. Infect Immun 2001, 69(February (2)):988-995.
18. Seregin S.S., Aldhamen Y.A., Appledorn D.M., Hartman Z.C., Schuldt N.J., Scott J., et al. Adenovirus capsid-display of the retro-oriented human complement inhibitor DAF reduces Ad vector-triggered immune responses in vitro and in vivo. Blood 2010, 116(September (10)):1669-1677.
19. Kink J.A., Williams J.A. Antibodies to recombinant Clostridium difficile toxins A and B are an effective treatment and prevent relapse of C. difficile-associated disease in a hamster model of infection. Infect Immun 1998, 66(May (5)):2018-2025.
20. Ward S.J., Douce G., Figueiredo D., Dougan G., Wren B.W. Immunogenicity of a Salmonella typhimurium aroA aroD vaccine expressing a nontoxic domain of Clostridium difficile toxin A. Infect Immun 1999, 67(May (5)):2145-2152.
21. Ahearn J.M., Fischer M.B., Croix D., Goerg S., Ma M., Xia J., et al. Disruption of the Cr2 locus results in a reduction in B-1a cells and in an impaired B cell response to T-dependent antigen. Immunity 1996, 4(March (3)):251-262.
22. Aboudola S., Kotloff K.L., Kyne L., Warny M., Kelly E.C., Sougioultzis S., et al. Clostridium difficile vaccine and serum immunoglobulin G antibody response to toxin A. Infect Immun 2003, 71(March (3)):1608-1610.
23. Ng P., Graham F.L. Construction of first-generation adenoviral vectors. Methods Mol Med 2002, 69:389-414.
24. Seregin S.S., Aldhamen Y.A., Appledorn D.M., Schuldt N.J., McBride A.J., Bujold M., et al. CR1/2 is an important suppressor of Adenovirus-induced innate immune responses and is required for induction of neutralizing antibodies. Gene Ther 2009, 16(October (10)):1245-1259.
25. Seregin S.S., Appledorn D.M., McBride A.J., Schuldt N.J., Aldhamen Y.A., Voss T., et al. Transient pretreatment with glucocorticoid ablates innate toxicity of systemically delivered adenoviral vectors without reducing efficacy. Mol Ther 2009, 17(April (4)):685-696.
26. Hensley S.E., Cun A.S., Giles-Davis W., Li Y., Xiang Z., Lasaro M.O., et al. Type I interferon inhibits antibody responses induced by a chimpanzee adenovirus vector. Mol Ther 2007, 15(February (2)):393-403.
27. Weaver E.A., Barry M.A. Effects of shielding adenoviral vectors with polyethylene glycol (PEG) on vector-specific and vaccine-mediated immune responses. Hum Gene Ther 2008, 19(12):1369-1382.
28. Aldhamen Y.A., Appledorn D.M., Seregin S.S., Liu C.J., Schuldt N.J., Godbehere S., et al. Expression of the SLAM family of receptors adapter EAT-2 as a novel strategy for enhancing beneficial immune responses to vaccine antigens. J Immunol 2011, 186(January (2)):722-732.
29. Hu H., Serra D., Amalfitano A. Persistence of an [E1-, polymerase-] adenovirus vector despite transduction of a neoantigen into immune-competent mice. Hum Gene Ther 1999, 10(February (3)):355-364.
30. Kyne L., Warny M., Qamar A., Kelly C.P. Asymptomatic carriage of Clostridium difficile and serum levels of IgG antibody against toxin A. N Engl J Med 2000, 342(February (6)):390-397.
31. Appledorn D.M., Aldhamen Y.A., Depas W., Seregin S.S., Liu C.J., Schuldt N., et al. A new adenovirus based vaccine vector expressing an Eimeria tenella derived TLR agonist improves cellular immune responses to an antigenic target. PLoS One 2010, 5(3):e9579.
32. Seregin S.S., Aldhamen Y.A., Appledorn D.M., Zehnder J., Voss T., Godbehere S., et al. Use of DAF-displaying adenovirus vectors reduces induction of transgene- and vector-specific adaptive immune responses in mice. Hum Gene Ther 2011, 22(9):1083-1094.
33. Chen X., Katchar K., Goldsmith J.D., Nanthakumar N., Cheknis A., Gerding D.N., et al. A mouse model of Clostridium difficile-associated disease. Gastroenterology 2008, 135(December (6)):1984-1992.
34. Taylor C.P., Tummala S., Molrine D., Davidson L., Farrell R.J., Lembo A., et al. Open-label, dose escalation phase I study in healthy volunteers to evaluate the safety and pharmacokinetics of a human monoclonal antibody to Clostridium difficile toxin A. Vaccine 2008, 26(June (27-28)):3404-3409.
35. Seregin S.S., Amalfitano A. Gene therapy for lysosomal storage diseases: progress, challenges and future prospects. Curr Pharm Des 2011, 17(24):2558-2574.
36. Wang R., Doolan D.L., Le T.P., Hedstrom R.C., Coonan K.M., Charoenvit Y., et al. Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine. Science 1998, 282(October (5388)):476-480.
37. Asmuth D.M., Brown E.L., Dinubile M.J., Sun X., Del Rio C., Harro C., et al. Comparative cell-mediated immunogenicity of DNA/DNA, DNA/Adenovirus type 5 (Ad5), or Ad5/Ad5 HIV-1 Clade B gag vaccine prime-boost regimens. J Infect Dis 2010, 201(January (1)):132-141.
38. Liu J., O'Brien K.L., Lynch D.M., Simmons N.L., La Porte A., Riggs A.M., et al. Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys. Nature 2009, 457(January (7225)):87-91.
39. Shott J.P., McGrath S.M., Pau M.G., Custers J.H., Ophorst O., Demoitie M.A., et al. Adenovirus 5 and 35 vectors expressing Plasmodium falciparum circumsporozoite surface protein elicit potent antigen-specific cellular IFN-gamma and antibody responses in mice. Vaccine 2008, 26(June (23)):2818-2823.
40. Abbink P., Lemckert A.A., Ewald B.A., Lynch D.M., Denholtz M., Smits S., et al. Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from subgroups B and D. J Virol 2007, 81(May (9)):4654-4663.
41. Barouch D.H., Pau M.G., Custers J.H., Koudstaal W., Kostense S., Havenga M.J., et al. Immunogenicity of recombinant adenovirus serotype 35 vaccine in the presence of pre-existing anti-Ad5 immunity. J Immunol 2004, 172(May (10)):6290-6297.
42. Allaker R.P. Host defence peptides-a bridge between the innate and adaptive immune responses. Trans R Soc Trop Med Hygiene 2008, 102(January (1)):3-4.
43. Iwasaki A., Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol 2004, 5(October (10)):987-995.
44. Kemper C., Atkinson J.P. T-cell regulation: with complements from innate immunity. Nat Rev Immunol 2007, 7(January (1)):9-18.
45. Morgan B.P., Marchbank K.J., Longhi M.P., Harris C.L., Gallimore A.M. Complement: central to innate immunity and bridging to adaptive responses. Immunol Lett 2005, 97(March (2)):171-179.
46. Catanzaro A.T., Koup R.A., Roederer M., Bailer R.T., Enama M.E., Moodie Z., et al. Phase 1 safety and immunogenicity evaluation of a multiclade HIV-1 candidate vaccine delivered by a replication-defective recombinant adenovirus vector. J Infect Dis 2006, 194(December (12)):1638-1649.
47. Gao W., Soloff A.C., Lu X., Montecalvo A., Nguyen D.C., Matsuoka Y., et al. Protection of mice and poultry from lethal H5N1 avian influenza virus through adenovirus-based immunization. J Virol 2006, 80(February (4)):1959-1964.
48. Sullivan N.J., Sanchez A., Rollin P.E., Yang Z.Y., Nabel G.J. Development of a preventive vaccine for Ebola virus infection in primates. Nature 2000, 408(November (6812)):605-609.
49. Pinto A.R., Fitzgerald J.C., Giles-Davis W., Gao G.P., Wilson J.M., Ertl H.C. Induction of CD8+ T cells to an HIV-1 antigen through a prime boost regimen with heterologous E1-deleted adenoviral vaccine carriers. J Immunol 2003, 171(December (12)):6774-6779.
50. Reyes-Sandoval A., Sridhar S., Berthoud T., Moore A.C., Harty J.T., Gilbert S.C., et al. Single-dose immunogenicity and protective efficacy of simian adenoviral vectors against Plasmodium berghei. Eur J Immunol 2008, 38(March (3)):732-741.
51. Shiver J.W., Fu T.M., Chen L., Casimiro D.R., Davies M.E., Evans R.K., et al. Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature 2002, 415(January (6869)):331-335.
52. Schirmbeck R., Reimann J., Kochanek S., Kreppel F. The immunogenicity of adenovirus vectors limits the multispecificity of CD8 T-cell responses to vector-encoded transgenic antigens. Mol Ther 2008, 16(September (9)):1609-1616.
53. Buchbinder S.P., Mehrotra D.V., Duerr A., Fitzgerald D.W., Mogg R., Li D., et al. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 2008, 372(November (9653)):1881-1893.
54. Weaver E.A., Nehete P.N., Buchl S.S., Senac J.S., Palmer D., Ng P., et al. Comparison of replication-competent, first generation, and helper-dependent adenoviral vaccines. PLoS One 2009, 4(3):e5059.
55. Gabitzsch E.S., Xu Y., Yoshida L.H., Balint J., Amalfitano A., Jones F.R. Novel Adenovirus type 5 vaccine platform induces cellular immunity against HIV-1 Gag, Pol, Nef despite the presence of Ad5 immunity. Vaccine 2009, 27(46):6394-6398.
56. Pichla-Gollon S.L., Lin S.W., Hensley S.E., Lasaro M.O., Herkenhoff-Haut L., Drinker M., et al. Effect of preexisting immunity on an adenovirus vaccine vector: in vitro neutralization assays fail to predict inhibition by antiviral antibody in vivo. J Virol 2009, 83(June (11)):5567-5573.