The recombinant Lactococcus lactis oral vaccine induces protection against C. difficile spore challenge in a mouse model

Vaccine

Volumn 33, Issue 13, 2015, Pages 1586-1595

  Guo, Shanguang ^a,b   Yan, Weiwei ^a   McDonough, Sean P ^a   Lin, Nengfeng ^a   Wu, Katherine J ^a   He, Hongxuan ^a,c   Xiang, Hua ^a,d   Yang, Maosheng ^a,e   Moreira, Maira Aparecida S ^a,f   Chang, Yung Fu ^a  

^a Animal Health Diagnostic Center   (United States)

^b SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^c INSTITUTE OF ZOOLOGY   (China)

^d INSTITUTE OF ANIMAL SCIENCE   (China)

^e Guizhou Academy of Agricultural Sciences   (China)

^f FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

Author keywords

Clostridium difficile; Lactococus lactis; TcbB; TcdA; Vaccine trial

Indexed keywords

CLOSTRIDIUM DIFFICILE TOXIN A; CLOSTRIDIUM DIFFICILE TOXIN B; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; LACTOCOCCUS LACTIS VACCINE; NEUTRALIZING ANTIBODY; RECOMBINANT VACCINE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; BACTERIAL PROTEIN; BACTERIAL TOXIN; BACTERIAL VACCINE; BACTERIUM ANTIBODY; ENTEROTOXIN; IMMUNOGLOBULIN G; RECOMBINANT PROTEIN; SECRETORY IMMUNOGLOBULIN; TCDA PROTEIN, CLOSTRIDIUM DIFFICILE; TOXB PROTEIN, CLOSTRIDIUM DIFFICILE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BACTERIAL SPORE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BODY WEIGHT; CARBOXY TERMINAL SEQUENCE; CLOSTRIDIUM DIFFICILE INFECTION; CONTROLLED STUDY; DIARRHEA; DISEASE SEVERITY; DRUG DELIVERY SYSTEM; ESCHERICHIA COLI; FEMALE; HISTOPATHOLOGY; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGENICITY; IN VITRO STUDY; INFECTION; INFECTION PREVENTION; LACTIC ACID BACTERIUM; LACTOCOCCUS LACTIS; MORTALITY; MOUSE; MOUSE MODEL; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURVIVAL; SURVIVAL RATE; TRANSGENIC ORGANISM; VACCINATION; WEIGHT REDUCTION; ANIMAL; C57BL MOUSE; CHLOROCEBUS AETHIOPS; CLOSTRIDIUM INFECTIONS; COLON; DISEASE MODEL; GENE VECTOR; GENETIC ENGINEERING; GENETICS; IMMUNOLOGY; MOUTH; PATHOLOGY; PEPTOCLOSTRIDIUM DIFFICILE; PHYSIOLOGY; VERO CELL LINE;

ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL PROTEINS; BACTERIAL TOXINS; BACTERIAL VACCINES; CERCOPITHECUS AETHIOPS; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM INFECTIONS; COLON; DISEASE MODELS, ANIMAL; ENTEROTOXINS; ESCHERICHIA COLI; GENETIC ENGINEERING; GENETIC VECTORS; IMMUNOGLOBULIN A, SECRETORY; IMMUNOGLOBULIN G; LACTOCOCCUS LACTIS; MICE; MICE, INBRED C57BL; MOUTH; RECOMBINANT PROTEINS; SPORES, BACTERIAL; VACCINES, SYNTHETIC; VERO CELLS;

EID: 84924872871     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2015.02.006     Document Type: Article

References (63)

1. Kuehne S.A., Cartman S.T., Heap J.T., Kelly M.L., Cockayne A., Minton N.P. The role of toxin A and toxin B in Clostridium difficile infection. Nature 2010, 467(7316):711-713.
2. Rupnik M., Wilcox M.H., Gerding D.N. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat Rev Microbiol 2009, 7(7):526-536.
3. Hunt J.J., Ballard J.D. Variations in virulence and molecular biology among emerging strains of Clostridium difficile. Microbiol Mol Biol Rev 2013, 77(4):567-581.
4. Scaria J., Mao C., Chen J.W., McDonough S.P., Sobral B., Chang Y.F. Differential stress transcriptome landscape of historic and recently emerged hypervirulent strains of Clostridium difficile strains determined using RNA-seq. PLoS ONE 2013, 8(11):e78489.
5. Chen J.W., Scaria J., Mao C., Sobral B., Zhang S., Lawley T., et al. Proteomic comparison of historic and recently emerged hypervirulent Clostridium difficile strains. J Proteome Res 2013, 12(3):1151-1161.
6. Stabler R.A., He M., Dawson L., Martin M., Valiente E., Corton C., et al. Comparative genome and phenotypic analysis of Clostridium difficile 027 strains provides insight into the evolution of a hypervirulent bacterium. Genome Biol 2009, 10(9):R102.
7. Loo V.G., Poirier L., Miller M.A., Oughton M., Libman M.D., Michaud S., et al. A predominantly clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. N Engl J Med 2005, 353(23):2442-2449.
8. McDonald L.C., Killgore G.E., Thompson A., Owens R.C., Kazakova S.V., Sambol S.P., et al. An epidemic, toxin gene-variant strain of Clostridium difficile. N Engl J Med 2005, 353(23):2433-2441.
9. Kuijper E.J., Coignard B., Tull P. Emergence of Clostridium difficile-associated disease in North America and Europe. Clin Microbiol Infect 2006, 12(Suppl 6):2-18.
10. O'Brien J.A., Lahue B.J., Caro J.J., Davidson D.M. The emerging infectious challenge of Clostridium difficile-associated disease in Massachusetts hospitals: clinical and economic consequences. Infect Control Hosp Epidemiol 2007, 28(11):1219-1227.
11. McFarland L.V., Elmer G.W., Surawicz C.M. Breaking the cycle: treatment strategies for 163 cases of recurrent Clostridium difficile disease. Am J Gastroenterol 2002, 97(7):1769-1775.
12. Zar F.A., Bakkanagari S.R., Moorthi K.M., Davis M.B. A comparison of vancomycin and metronidazole for the treatment of Clostridium difficile-associated diarrhea, stratified by disease severity. Clin Infect Dis 2007, 45(3):302-307.
13. Aslam S., Hamill R.J., Musher D.M. Treatment of Clostridium difficile-associated disease: old therapies and new strategies. Lancet Infect Dis 2005, 5(9):549-557.
14. Ritter A.S., Petri W.A. New developments in chemotherapeutic options for Clostridium difficile colitis. Curr Opin Infect Dis 2013, 26(5):461-470.
15. Zilberberg M.D., Shorr A.F., Micek S.T., Doherty J.A., Kollef M.H. Clostridium difficile-associated disease and mortality among the elderly critically ill. Crit Care Med 2009, 37(9):2583-2589.
16. von Eichel-Streiber C., Warfolomeow I., Knautz D., Sauerborn M., Hadding U. Morphological changes in adherent cells induced by Clostridium difficile toxins. Biochem Soc Trans 1991, 19(4):1154-1160.
17. Permpoonpattana P., Hong H.A., Phetcharaburanin J., Huang J.M., Cook J., Fairweather N.F., et al. Immunization with Bacillus spores expressing toxin A peptide repeats protects against infection with Clostridium difficile strains producing toxins A and B. Infect Immun 2011, 79(6):2295-2302.
18. Lowy I., Molrine D.C., Leav B.A., Blair B.M., Baxter R., Gerding D.N., et al. Treatment with monoclonal antibodies against Clostridium difficile toxins. N Engl J Med 2010, 362(3):197-205.
19. Giannasca P.J., Warny M. Active and passive immunization against Clostridium difficile diarrhea and colitis. Vaccine 2004, 22(7):848-856.
20. Mohamadzadeh M., Duong T., Sandwick S.J., Hoover T., Klaenhammer T.R. Dendritic cell targeting of Bacillus anthracis protective antigen expressed by Lactobacillus acidophilus protects mice from lethal challenge. Proc Natl Acad Sci U S A 2009, 106(11):4331-4336.
21. Bermudez-Humaran L.G., Kharrat P., Chatel J.M., Langella P. Lactococci and lactobacilli as mucosal delivery vectors for therapeutic proteins and DNA vaccines. Microb Cell Fact 2011, 10(Suppl 1):S4.
22. Pontes D.S., de Azevedo M.S., Chatel J.M., Langella P., Azevedo V., Miyoshi A. Lactococcus lactis as a live vector: heterologous protein production and DNA delivery systems. Protein Expr Purif 2011, 79(2):165-175.
23. Martin J., Mawer D., Wilcox M.H. Clostridium difficile: biological therapies. Curr Opin Infect Dis 2013, 26(5):454-460.
24. Wells J.M., Mercenier A. Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria. Nat Rev Microbiol 2008, 6(5):349-362.
25. Sorg J.A., Dineen S.S. Laboratory maintenance of Clostridium difficile. Curr Protoc Microbiol 2009, (February). Chapter 9:Unit9A 1.
26. Yan W., Shin K.S., Wang S.J., Xiang H., Divers T., McDonough S., et al. Equine hyperimmune serum protects mice against Clostridium difficile spore challenge. J Vet Sci 2014, 15(2):249-258.
27. Yan W., Faisal S.M., McDonough S.P., Divers T.J., Barr S.C., Chang C-F., et al. Immunogenicity and protective efficacy of recombinant Leptospira immunoglobulin-like protein B (rLigB) in a hamster challenge model. Microbes Infect 2009, 11(2):230-237.
28. Holo H., Nes I.F. High-frequency transformation, by electroporation, of Lactococcus lactis subsp. cremoris grown with glycine in osmotically stabilized media. Appl Environ Microbiol 1989, 55(12):3119-3123.
29. Ehrich M., Van Tassell R.L., Libby J.M., Wilkins T.D. Production of Clostridium difficile antitoxin. Infect Immun 1980, 28(3):1041-1043.
30. 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(6):1984-1992.
31. McDonald L.C. Virulence and clinical outcomes in Clostridium difficile infection: a complex business. Clin Infect Dis 2013, 56(6):906-907.
32. Louie T.J., Miller M.A., Mullane K.M., Weiss K., Lentnek A., Golan Y., et al. Fidaxomicin versus Vancomycin for Clostridium difficile infection. N Engl J Med 2011.
33. Salcedo J., Keates S., Pothoulakis C., Warny M., Castagliuolo I., LaMont J.T., et al. Intravenous immunoglobulin therapy for severe Clostridium difficile colitis. Gut 1997, 41(3):366-370.
34. 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(3):764-770.
35. Ward S.J., Douce G., Dougan G., Wren B.W. Local and systemic neutralizing antibody responses induced by intranasal immunization with the nontoxic binding domain of toxin A from Clostridium difficile. Infect Immun 1999, 67(10):5124-5132.
36. 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(5):2145-2152.
37. 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(27):3598-3604.
38. Ghose C., Verhagen J.M., Chen X., Yu J., Huang Y., Chenesseau O., et al. Toll-like receptor 5-dependent immunogenicity and protective efficacy of a recombinant fusion protein vaccine containing the nontoxic domains of Clostridium difficile toxins A and B and Salmonella enterica serovar Typhimurium flagellin in a mouse model of Clostridium difficile disease. Infect Immun 2013, 81(6):2190-2196.
39. Maynard-Smith M., Ahern H., McGlashan J., Nugent P., Ling R., Denton H., et al. Recombinant antigens based on toxins A and B of Clostridium difficile that evoke a potent toxin-neutralising immune response. Vaccine 2014, 32(6):700-705.
40. Wang H., Sun X., Zhang Y., Li S., Chen K., Shi L., et al. A chimeric toxin vaccine protects against primary and recurrent Clostridium difficile infection. Infect Immun 2012, 80(8):2678-2688.
41. Martin C.E., Broecker F., Eller S., Oberli M.A., Anish C., Pereira C.L., et al. Glycan arrays containing synthetic Clostridium difficile lipoteichoic acid oligomers as tools toward a carbohydrate vaccine. Chem Commun 2013, 49(64):7159-7161.
42. Martin C.E., Broecker F., Oberli M.A., Komor J., Mattner J., Anish C., et al. Immunological evaluation of a synthetic Clostridium difficile oligosaccharide conjugate vaccine candidate and identification of a minimal epitope. J Am Chem Soc 2013, 135(26):9713-9722.
43. Martin C.E., Weishaupt M.W., Seeberger P.H. Progress toward developing a carbohydrate-conjugate vaccine against Clostridium difficile ribotype 027: synthesis of the cell-surface polysaccharide PS-I repeating unit. Chem Commun 2011, 47(37):10260-10262.
44. Ryan E.T., Butterton J.R., Smith R.N., Carroll P.A., Crean T.I., Calderwood S.B. Protective immunity against Clostridium difficile toxin A induced by oral immunization with a live, attenuated Vibrio cholerae vector strain. Infect Immun 1997, 65(7):2941-2949.
45. Torres J.F., Lyerly D.M., Hill J.E., Monath T.P. Evaluation of formalin-inactivated Clostridium difficile vaccines administered by parenteral and mucosal routes of immunization in hamsters. Infect Immun 1995, 63(12):4619-4627.
46. Monteiro M.A., Ma Z., Bertolo L., Jiao Y., Arroyo L., Hodgins D., et al. Carbohydrate-based Clostridium difficile vaccines. Expert Rev. Vaccines 2013, 12(4):421-431.
47. Pechine S., Deneve C., Le Monnier A., Hoys S., Janoir C., Collignon A. Immunization of hamsters against Clostridium difficile infection using the Cwp84 protease as an antigen. FEMS Immunol Med Microbiol 2011, 63(1):73-81.
48. Pechine S., Hennequin C., Boursier C., Hoys S., Collignon A. Immunization using GroEL decreases Clostridium difficile intestinal colonization. PLoS One 2013, 8(11):e81112.
49. Donald R.G., Flint M., Kalyan N., Johnson E., Witko S.E., Kotash C., et al. A novel approach to generate a recombinant toxoid vaccine against Clostridium difficile. Microbiology 2013, 159(Pt 7):1254-1266.
50. Foglia G., Shah S., Luxemburger C., Pietrobon P.J. Clostridium difficile: development of a novel candidate vaccine. Vaccine 2012, 30(29):4307-4309.
51. Greenberg R.N., Marbury T.C., Foglia G., Warny M. Phase I dose finding studies of an adjuvanted Clostridium difficile toxoid vaccine. Vaccine 2012, 30(13):2245-2249.
52. Tian J.H., Fuhrmann S.R., Kluepfel-Stahl S., Carman R.J., Ellingsworth L., Flyer D.C. A novel fusion protein containing the receptor binding domains of C. difficile toxin A and toxin B elicits protective immunity against lethal toxin and spore challenge in preclinical efficacy models. Vaccine 2012, 30(28):4249-4258.
53. Leuzzi R., Spencer J., Buckley A., Brettoni C., Martinelli M., Tulli L., et al. Protective efficacy induced by recombinant Clostridium difficile toxin fragments. Infect Immun 2013, 81(8):2851-2860.
54. Anosova N.G., Brown A.M., Li L., Liu N., Cole L.E., Zhang J., et al. Systemic antibody responses induced by a two-component Clostridium difficile toxoid vaccine protect against C. difficile-associated disease in hamsters. J Med Microbiol 2013, 62(Pt 9):1394-1404.
55. Bertolo L., Boncheff A.G., Ma Z., Chen Y.H., Wakeford T., Friendship R.M., et al. Clostridium difficile carbohydrates: glucan in spores PSII common antigen in cells, immunogenicity of PSII in swine and synthesis of a dual C. difficile-ETEC conjugate vaccine. Carbohydr Res 2012.
56. Seregin S.S., Aldhamen Y.A., Rastall D.P., Godbehere S., Amalfitano A. Adenovirus-based vaccination against Clostridium difficile toxin A allows for rapid humoral immunity and complete protection from toxin A lethal challenge in mice. Vaccine 2012, 30(8):1492-1501.
57. Jiao Y., Ma Z., Hodgins D., Pequegnat B., Bertolo L., Arroyo L., et al. Clostridium difficile PSI polysaccharide: synthesis of pentasaccharide repeating block, conjugation to exotoxin B subunit, and detection of natural anti-PSI IgG antibodies in horse serum. Carbohydr Res 2013, 378:15-25.
58. Oberli M.A., Hecht M.L., Bindschadler P., Adibekian A., Adam T., Seeberger P.H. A possible oligosaccharide-conjugate vaccine candidate for Clostridium difficile is antigenic and immunogenic. Chem Biol 2011, 18(5):580-588.
59. del Rio B., Fuente J.L., Neves V., Dattwyler R., Seegers J.F., Gomes-Solecki M. Platform technology to deliver prophylactic molecules orally: an example using the Class A select agent Yersinia pestis. Vaccine 2010, 28(41):6714-6722.
60. Yang X.Q., Zhao Y.G., Chen X.Q., Jiang B., Sun D.Y. The protective effect of recombinant Lactococcus lactis oral vaccine on a Clostridium difficile-infected animal model. BMC Gastroenterol 2013, 13:117.
61. Vaerman J.P., Langendries A. Hepatobiliary transport of IgA in the golden Syrian hamster (Mesocricetus auratus). Immunol Lett 1997, 55(1):19-26.
62. Belyi I.F., Varfolomeeva N.A. Construction of a fusion protein carrying antigenic determinants of enteric clostridial toxins. FEMS Microbiol Lett 2003, 225(2):325-329.
63. Suebwongsa N., Panya M., Namwat W., Sookprasert S., Redruello B., Mayo B., et al. Cloning and expression of a codon-optimized gene encoding the influenza A virus nucleocapsid protein in Lactobacillus casei. Int Microbiol 2013, 16(2):93-101.