Recombinant Salmonella vaccination technology and its application to Human Bacterial Pathogens

Current Pharmaceutical Biotechnology

Volumn 14, Issue 2, 2013, Pages 209-219

  Zhang, Song ^a   Walters, Nancy ^b   Cao, Ling ^b   Robison, Amanda ^b   Yang, Xinghong ^b  

^a Taishan Sanatorium of Shandong Province ^*  (China)

^b MONTANA STATE UNIVERSITY   (United States)

Author keywords

Escherichia coli; Helicobacter pylori; Mycobacterium tuberculosis; Passenger antigen; Recombinant vaccine; Salmonella vaccine vector; Shigella dysenteriae; Yersinia pestis

Indexed keywords

ENTEROTOXIGENIC ESCHERICHIA COLI VACCINE; IMMUNOGLOBULIN G; RECOMBINANT VACCINE; SALMONELLOSIS VACCINE; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 6; UNCLASSIFIED DRUG; VACCINE; VXM01;

ADAPTIVE IMMUNITY; ARTICLE; BACTERIAL INFECTION; BACTERIAL STRAIN; BLOODY DIARRHEA; CELL PROLIFERATION; COST EFFECTIVENESS ANALYSIS; DRUG DEVELOPMENT; DRUG STABILITY; ENTEROTOXIGENIC ESCHERICHIA COLI; ESCHERICHIA COLI; GASTRITIS; GENE EXPRESSION; HELICOBACTER PYLORI; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; INFLAMMATION; INNATE IMMUNITY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PLAGUE; RISK FACTOR; SALMONELLA; SALMONELLOSIS; SHIGELLA DYSENTERIAE; VACCINATION; YERSINIA PESTIS;

EID: 84875331580     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/1389201011314020011     Document Type: Article

References (150)

1. Spellberg, B.; Guidos, R.; Gilbert, D.; Bradley, J.; Boucher, H.W.; Scheld, W.M.; Bartlett, J.G.; Edwards, J. Jr. The epidemic of antibiotic-resistant infections: a call to action for the medical community from the Infectious Diseases Society of America. Clin. Infect. Dis., 2008, 46, 155-164.
2. Boucher, H.W.; Talbot, G.H.; Bradley, J.S.; Edwards, J.E.; Gilbert, D.; Rice, L.B.; Scheld, M.; Spellberg, B.; Bartlett, J. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin. Infect. Dis., 2009, 48, 1-12.
3. Gilbert, D.N.; Guidos, R.J.; Boucher, H.W.; Talbot, G.H.; Spellberg, B.; Edwards, J.E.; Scheld, W.M.; Bradley, J.S.; Bartlett, J.G. The 10 x '20 Initiative: Pursuing a global commitment to develop 10 new antibacterial drugs by 2020. Clin. Infect. Dis., 2010, 50, 1081-1083.
4. Zaki, S.A.; Karande, S. Multidrug-resistant typhoid fever: a review. J. Infect. Dev. Ctries., 2011, 5, 324-337.
5. Platell, J.L.; Johnson, J.R.; Cobbold, R.N.; Trott, D.J. Multidrugresistant extraintestinal pathogenic. Escherichia coli of sequence type ST131 in animals and foods. Vet. Microbiol., 2011, 153, 99-108.
6. Michetti, P. Vaccine against Helicobacter pylori: fact or fiction? Gut, 1997, 41, 728-730.
7. Muytjens, H.L., Eggink, C.A., Dijkman, F.C.; Bakkers, J.M.; Melchers, W.J. Keratitis due to Shigella flexneri. J. Clin. Microbiol., 2006, 44, 2291-2294.
8. Galimand, M.; Carniel, E.; Courvalin, P. Resistance of Yersinia pestis to antimicrobial agents. Antimicrob. Agents Chemother., 2006, 50, 3233-3236.
9. Basile, J.I.; Geffner, L.J.; Romero, M.M.; Balboa, L.; Sabio, Y.G.C.; Ritacco, V.; Garcia, A.; Cuffre, M.; Abbate, E.; Lopez, B.; Barrera, L.; Ambroggi, M.; Aleman, M.; Sasiain, M.C.; de la Barrera, S.S. Outbreaks of Mycobacterium tuberculosis MDR strains induce high IL-17 T-cell response in patients with MDR tuberculosis that is closely associated with high antigen load. J. Infect. Dis., 2011, 204, 1054-1064.
10. Yang, X.; Hinnebusch, B.J.; Trunkle, T.; Bosio, C.M.; Suo, Z.; Tighe, M.; Harmsen, A.; Becker, T.; Crist, K.; Walters, N.; Avci, R.; Pascual, D.W. Oral vaccination with Salmonella simultaneously expressing Yersinia pestis F1 and V antigens protects against bubonic and pneumonic plague. J. Immunol., 2007, 178, 1059-1067.
11. Yang, X.; Thornburg, T.; Holderness, K.; Suo, Z.; Cao, L.; Lim, T.; Avci, R.; Pascual, D.W. Serum antibodies protect against intraperitoneal challenge with enterotoxigenic Escherichia coli. J. Biomed. Biotechnol., 2011, 6323-6396.
12. Gnazzo, V.; Cebrian, I.; Langellotti, C.; Chabalgoity, J.; Mongini, C.; Quattrocchi, V.; Zamorano, P. Immunogenicity of a bovine herpes virus I peptide expressed in tandem copies in attenuated Salmonella. Viral Immunol., 2012, 25, 63-72.
13. Jiao, H.; Pan, Z.; Yin, Y.; Geng, S.; Sun, L.; Jiao, X. Oral and nasal DNA vaccines delivered by attenuated Salmonella enterica serovar Typhimurium induce a protective immune response against infectious bronchitis in chickens. Clin. Vaccine Immunol., 2011, 18, 1041-1045.
14. Schroeder, J.; Brown, N.; Kaye, P.; Aebischer, T. Single dose novel Salmonella vaccine enhances resistance against visceralizing L. major and L. donovani infection in susceptible BALB/c mice. PLoS Negl. Trop. Dis., 2011, 5, e1406.
15. Zeng, S.; Liu, Q.; Wang, S.; Peng, X.; Zhang, J. Intratumor injection of recombinant attenuated Salmonella carrying Mycobacterium tuberculosis heat shock protein 70 and herpes simplex virus thymidine kinase genes to suppress murine melanoma growth. Nan Fang Yi Ke Da Xue Xue Bao, 2012, 32, 101-105.
16. Yoon, W.S.; Chae, Y.S.; Hong, J.; Park, Y.K. Antitumor therapeutic effects of a genetically engineered Salmonella typhimurium harboring TNF-alpha in mice. Appl. Microbiol. Biotechnol., 2011, 89, 1807-1819.
17. Jarosz, M.; Jazowiecka-Rakus, J.; Cichon, T.; Glowala-Kosinska, M.; Smolarczyk, R.; Smagur, A.; Malina, S.; Sochanik, A.; Szala, S. Therapeutic antitumor potential of endoglin-based DNA vaccine combined with immunomodulatory agents. Gene Ther., 2012.
18. Hegazy, W.A.; Hensel, M. Salmonella enterica as a vaccine carrier. Future Microbiol., 2012, 7, 111-127.
19. Coburn, B.; Grassl, G.A., Finlay BB. Salmonella, the host and disease: a brief review. Immunol. Cell Biol., 2007, 85, 112-118.
20. Crump, J.A.; Luby, S.P.; Mintz, E.D. The global burden of typhoid fever. Bull World Health Organ, 2004, 82, 346-353.
21. Kennedy, M.; Villar, R.; Vugia, D.J.; Rabatsky-Her, T.; Farley, M.M.; Pass, M.; Smith, K.; Smith, P.; Cieslak, P.R.; Imhoff, B.; Griffin, P.M. Hospitalizations and deaths due to Salmonella infections, FoodNet, 1996-1999. Clin. Infect. Dis., 2004, 38 Suppl 3, S142-148.
22. Threlfall, E.J. Epidemic Salmonella typhimurium DT 104-a truly international multiresistant clone. J. Antimicrob. Chemother., 2000, 46, 7-10.
23. Holt, K.E.; Phan, M.D.; Baker, S.; Duy, P.T.; Nga, T.V.; Nair, S.; Turner, A.K.; Walsh, C.; Fanning, S.; Farrell-Ward, S.; Dutta, S.; Kariuki, S.; Weill F.X.; Parkhill, J.; Dougan, G.; Wain, J. Emergence of a globally dominant IncHI1 plasmid type associated with multiple drug resistant typhoid. PLoS Negl. Trop. Dis., 2011, 5, e1245.
24. Marcus, L.C.; Froeschle, J.E.; Hill, D.R.; Wolfe, M.S.; Maus, D.; Connor, B.; Acosta, A.M.; Rensimer, E.R.; Roberts, A.; Dardick, K. Safety of typhim Vi vaccine in a postmarketing observational study. J. Travel Med., 2007, 14, 386-391.
25. Levine, M.M.; Ferreccio, C.; Abrego, P.; Martin, O.S.; Ortiz, E.; Cryz, S. Duration of efficacy of Ty21a, attenuated Salmonella typhi live oral vaccine. Vaccine, 1999, 17 Suppl, 2, S22-27.
26. Viret, J.F.; Favre, D.; Wegmuller, B.; Herzog, C.; Que, J.U.; Cryz, S.J.; Lang, A.B. Mucosal and systemic immune responses in humans after primary and booster immunizations with orally administered invasive and noninvasive live attenuated bacteria. Infect. Immun., 1999, 67, 3680-3685.
27. Bullifent, H.L.; Griffin, K.F.; Jones, S.M.; Yates, A.; Harrington, L.; Titball, R.W. Antibody responses to Yersinia pestis F1-antigen expressed in Salmonella typhimurium aroA from in vivo-inducible promoters. Vaccine, 2000, 18, 2668-2676.
28. De Magistris, M.T. Mucosal delivery of vaccine antigens and its advantages in pediatrics. Adv. Drug Deliv. Rev., 2006, 58, 52-67.
29. Gunn, B.M.; Wanda, S.Y.; Burshell, D.; Wang, C.; Curtiss, R. 3rd. Construction of recombinant attenuated Salmonella enterica serovar typhimurium vaccine vector strains for safety in newborn and infant mice. Clin. Vaccine Immunol., 2010, 17, 354-362.
30. McCluskie, M.J.; Davis, H.L. Mucosal immunization with DNA vaccines. Microbes Infect., 1999, 1, 685-698.
31. Ogra, P.L.; Faden, H.; Welliver, R.C. Vaccination strategies for mucosal immune responses. Clin. Microbiol. Rev., 2001, 14, 430-445.
32. Rosenthal, K.L.; Gallichan, W.S. Challenges for vaccination against sexually-transmitted diseases: induction and long-term maintenance of mucosal immune responses in the female genital tract. Semin. Immunol., 1997, 9, 303-314.
33. Hohmann, E.L.; Oletta, C.A.; Loomis, W.P.; Miller, S.I. Macrophage-inducible expression of a model antigen in Salmonella typhimurium enhances immunogenicity. Proc. Natl. Acad. Sci. U S A., 1995, 92, 2904-2908.
34. Marshall, D.G.; Haque, A.; Fowler, R.; Del Guidice, G.; Dorman, C.J.; Dougan, G.; Bowe, F. Use of the stationary phase inducible promoters, spv and dps, to drive heterologous antigen expression in Salmonella vaccine strains. Vaccine, 2000, 18, 1298-1306.
35. Janis, C.; Grant, A.J.; McKinley, T.J.; Morgan, F.J.; John, V.F.; Houghton, J.; Kingsley, R.A.; Dougan, G.; Mastroeni, P. In vivo regulation of the Vi antigen in Salmonella and induction of immune responses with an in vivo-inducible promoter. Infect. Immun., 2011, 79, 2481-2488.
36. Black, R.; Levine, M.M.; Young, C.; Rooney, J.; Levine, S.; Clements, M.L.; O'Donnell, S.; Hugues, T.; Germanier, R. Immunogenicity of Ty21a attenuated Salmonella Typhi given with sodium bicarbonate or in enteric-coated capsules. Dev. Biol. Stand.; 1983, 53, 9-14.
37. Guzman, C.A.; Borsutzky, S.; Griot-Wenk, M.; Metcalfe, I.C.; Pearman, J.; Collioud, A.; Favre, D.; Dietrich, G. Vaccines against typhoid fever. Vaccine, 2006, 24, 3804-3811.
38. Osorio, M.; Wu, Y.; Singh, S.; Merkel, T.J.; Bhattacharyya, S.; Blake, M.S.; Kopecko, D.J. Anthrax protective antigen delivered by Salmonella enterica serovar Typhi Ty21a protects mice from a lethal anthrax spore challenge. Infect. Immun., 2009, 77, 1475-1482.
39. Niethammer, A.G.A.; Lubenau, H.H.; Mikus, G.G.; Hohmann, N.N.; Leowardi, C.C.; Beckhove, P.P.; Akhisaroglu, M.M.; Ge, Y.Y.; Springer, M.M.; Grenacher, L.L.; Buchler, M.W.M.; Koch, M.M.; Weitz, J.J.; Haefeli, W.E.W.; Schmitz-Winnenthal, F.H.F. Double-blind, placebo-controlled first in human study to investigate an oral vaccine aimed to elicit an immune reaction against the VEGF-Receptor 2 in patients with stage IV and locally advanced pancreatic cancer. BMC Cancer, 2012, 12, 361.
40. Schuetze, N.; Schoeneberger, S.; Mueller, U.; Freudenberg, M.A.; Alber, G.; Straubinger, R.K. IL-12 family members: differential kinetics of their TLR4-mediated induction by Salmonella Enteritidis and the impact of IL-10 in bone marrow-derived macrophages. Int. Immunol.; 2005, 17, 649-459.
41. Takeda, K.; Takeuchi, O.; Akira, S. Recognition of lipopeptides by Toll-like receptors. J. Endotoxin. Res., 2002, 8, 459-463.
42. Murthy, K.G.; Deb, A.; Goonesekera, S.; Szabo, C.; Salzman, A.L. Identification of conserved domains in Salmonella muenchen flagellin that are essential for its ability to activate TLR5 and to induce an inflammatory response in vitro. J. Biol. Chem., 2004, 279, 5667-5675.
43. Cowdery, J.S.; Boerth, N.J.; Norian, L.A.; Myung, P.S.; Koretzky, G.A. Differential regulation of the IL-12 p40 promoter and of p40 secretion by CpG DNA and lipopolysaccharide. J. Immunol., 1999, 162, 6770-6775.
44. Mittrucker, H.W.; Kaufmann, S.H. Immune response to infection with Salmonella Typhimurium in mice. J. Leukoc. Biol.; 2000, 67, 457-463.
45. Salerno-Goncalves, R.; Wyant, T.L.; Pasetti, M.F.; Fernandez-Vina, M.; Tacket, C.O.; Levine, M.M.; Sztein, M.B. Concomitant induction of CD4+ and CD8+ T cell responses in volunteers immunized with Salmonella enterica serovar Typhi strain CVD 908-htrA. J. Immunol., 2003, 170, 2734-2741.
46. Sztein, M.B.; Wasserman, S.S.; Tacket, C.O.; Edelman, R.; Hone, D.; Lindberg, A.A.; Levine, M.M. Cytokine production patterns and lymphoproliferative responses in volunteers orally immunized with attenuated vaccine strains of Salmonella Typhi. J. Infect. Dis., 1994, 170, 1508-1517.
47. Janeway, C.A.J.; Travers, P.; Walport, Mea. Immunobiology: The Immune System in Health and Disease. 5th edition. New York: Garland Science-Principles of innate and adaptive immunity, 2001: http://www.ncbi.nlm.nih.gov/books/NBK27090/.
48. Yamamoto, T.; Tamura, Y.; Yokota, T. Enteroadhesion fimbriae and enterotoxin of Escherichia coli-Genetic transfer to a streptomycin-resistant mutant of the gale oral route live vaccine Salmonella Typhi Ty21a. Infect. Immun., 1985, 50, 925-928.
49. Attridge, S.; Hackett, J.; Morona, R.; Whyte, P. Towards a live oral vaccine against enterotoxigenic Escherichia coli of swine. Vaccine, 1988, 6, 387-389.
50. Oyston, P.C.; Williamson, E.D.; Leary, S.E.; Eley, S.M.; Griffin, K.F.; Titball, R.W. Immunization with live recombinant Salmonella typhimurium aroA producing F1 antigen protects against plague. Infect. Immun., 1995, 63, 563-568.
51. Titball, R.W.; Howells, A.M.; Oyston, P.C.; Williamson, E.D. Expression of the Yersinia pestis capsular antigen (F1 antigen) on the surface of an aroA mutant of Salmonella typhimurium induces high levels of protection against plague. Infect. Immun., 1997, 65, 1926-1930.
52. Wu, S.; Pascual, D.W.; VanCott, J.L.; McGhee, J.R.; Maneval, D.R. Jr., Levine, M.M.; Hone, D.M. Immune responses to novel Escherichia coli and Salmonella typhimurium vectors that express colonization factor antigen I (CFA/I) of enterotoxigenic E. coli in the absence of the CFA/I positive regulator cfaR. Infect. Immun., 1995, 63, 4933-4938.
53. Galán, J.E.; Nakayama, K.; Curtiss, R. 3rd. Cloning and characterization of the asd gene of Salmonella typhimurium: use in stable maintenance of recombinant plasmids in Salmonella vaccine strains. Gene, 1990, 94, 29-35.
54. Hone, D.; Attridge, S.; van den, B.L.; Hackett, J. A chromosomal integration system for stabilization of heterologous genes in Salmonella based vaccine strains. Microb. Pathog.; 1988, 5, 407-418.
55. Stratford, R.; McKelvie, N.D.; Hughes, N.J.; Aldred, E.; Wiseman, C.; Curtis, J.; Bellaby, T.; Bentley, M.; Hindle, Z.; Brennan, F.R.; Chatfield, S.N.; Dougan, G.; Khan, S.A. Optimization of Salmonella enterica serovar typhi DaroC DssaV derivatives as vehicles for delivering heterologous antigens by chromosomal integration and in vivo inducible promoters. Infect. Immun.; 2005, 73, 362-368.
56. Ascón, M.A.; Hone, D.M.; Walters, N.; Pascual, D.W. Oral immunization with a Salmonella typhimurium vaccine vector expressing recombinant enterotoxigenic Escherichia coli K99 fimbriae elicits elevated antibody titers for protective immunity. Infect Immun., 1998, 66, 5470-5476.
57. Juárez-Rodríguez, M.D.; Yang, J.; Kader, R.; Alamuri, P.; Curtiss, R.; 3rd, Clark-Curtiss; J.E. Live attenuated Salmonella vaccines displaying regulated delayed lysis and delayed antigen synthesis to confer protection against Mycobacterium tuberculosis. Infect. Immun.; 2012, 80, 815-831.
58. Hur, J.; Lee, J.H. Immune responses to new vaccine candidates constructed by a live attenuated Salmonella Typhimurium delivery system expressing Escherichia coli F4, F5, F6, F41 and intimin adhesin antigens in a murine model. J. Vet. Med. Sci., 2011, 73, 1265-1273.
59. Wang, S.; Li, Y.; Scarpellini, G.; Kong, W.; Shi, H.; Baek, C.H.; Gunn, B.; Wanda, S.Y.; Roland, K.L.; Zhang, X.; Senechal-Willis, P.; Curtiss, R. 3rd. Salmonella vaccine vectors displaying delayed antigen synthesis in vivo to enhance immunogenicity. Infect. Immun.; 2010, 78, 3969-3980.
60. Wang, S.; Li, Y.; Shi, H.; Sun, W.; Roland, K.L.; Curtiss, R. 3rd. Comparison of a regulated delayed antigen synthesis system with in vivo-inducible promoters for antigen delivery by live attenuated Salmonella vaccines. Infect. Immun., 2011, 79, 937-949.
61. Hegazy, W.A.; Xu, X.; Metelitsa, L.; Hensel, M. Evaluation of Salmonella enterica type III secretion system effector proteins as carriers for heterologous vaccine antigens. Infect. Immun., 2012, 80, 1193-202.
62. Jang, J.I.; Kim, J.S.; Eom, J.S.; Kim, H.G.; Kim, B.H., Lim, S.; Bang, I.S.; Park, Y.K. Expression and delivery of tetanus toxin fragment C fused to the N-terminal domain of SipB enhances specific immune responses in mice. Microbiol. Immunol., 2012, 56, 595-604.
63. Dautin, N.; Bernstein, H.D. Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu. Rev. Microbiol., 2007, 61, 89-112.
64. Jong, W.S.; Soprova, Z.; de Punder, K.; Ten Hagen-Jongman, C.M.; Wagner, S.; Wickstrom, D.; de Gier, J.W.; Andersen, P.; van der Wel, N.N.; Luirink, J. A structurally informed autotransporter platform for efficient heterologous protein secretion and display. Microb Cell Fact, 2012, 11, 85.
65. Yang X, Suo Z, Thornburg T, Holderness K, Cao L, Lim T, Walters N, Kellerman L, Loetterle L, Avci L, Pascual DW. Expression of Escherichia coli virulence usher protein attenuates wild-type Salmonella. Virulence, 2012, 3, 29-41.
66. Cao, L.; Lim, T.; Jun, S.; Thornburg, T.; Avci, R.; Yang, X. Vulnerabilities in Yersinia pestis caf operon are unveiled by a Salmonella vector. PLoS One, 2012, 7, e36283.
67. Yang, X., Thornburg, T.; Suo, Z.; Jun, S.; Robison, A.; Li, J.; Lim, T.; Cao, L.; Hoyt, T.; Avci, R.; Pascual, D.W. Flagella overexpression attenuates Salmonella pathogenesis. PLoS One, 2012, 7, e46828.
68. Zheng, S.; Yu, B.; Zhang, K.; Chen, M.; Hua, Y.; Yuan, S.; Watt, R.; Zheng, B.; Yuen, K.; Huang, J. Comparative immunological evaluation of recombinant Salmonella Typhimurium strains expressing model antigens as live oral vaccines. BMC Immunol., 2012, 13, 54.
69. Haga, T.; Kumabe, S.; Ikejiri, A.; Shimizu, Y.; Li, H.; Goto, Y.; Matsui, H.; Miyata, H.; Miura, T. In vitro and in vivo stability of plasmids in attenuated Salmonella enterica serovar Typhimurium used as a carrier of DNA vaccine is associated with its replication origin. Exp. Anim., 2006, 55, 405-409.
70. Bauer, H.; Darji, A.; Chakraborty, T.; Weiss, S. Salmonellamediated oral DNA vaccination using stabilized eukaryotic expression plasmids. Gene Ther., 2005, 12, 364-372.
71. Bartolome, A.; Herrero-Gil, A.; Horcajo, P.; Orden, J.A.; de Fuente, R.; Dominguez-Bernal, G. Salmonella enterica serovar Choleraesuis derivatives harbouring deletions in rpoS and phoP regulatory genes as vehicles for DNA vaccines. Vet. Microbiol., 2010, 141, 81-88.
72. Baud, D.; Benyacoub, J.; Revaz, V.; Kok, M.; Ponci, F.; Bobst, M.; Curtiss, R.; 3rd, De Grandi, P.; Nardelli-Haefliger, D. Immunogenicity against human papillomavirus type 16 virus-like particles is strongly enhanced by the PhoPc phenotype in Salmonella enterica serovar Typhimurium. Infect. Immun., 2004, 72, 750-756.
73. Homolka, S.; Niemann, S.; Russell, D.G.; Rohde, K.H. Functional genetic diversity among Mycobacterium tuberculosis complex clinical isolates: delineation of conserved core and lineage-specific transcriptomes during intracellular survival. PLoS Pathog., 2010, 6, e1000988.
74. Celli, J.; Olivier, M. Finlay BB. Enteropathogenic Escherichia coli mediates antiphagocytosis through the inhibition of PI 3-kinasedependent pathways. EMBO J., 2001, 20, 1245-1258.
75. Walker, R.I.; Steele, D.; Aguado, T. Analysis of strategies to successfully vaccinate infants in developing countries against enterotoxigenic E. coli (ETEC) disease. Vaccine, 2007, 25, 2545-2566.
76. Jiang, Z.D.; Dupont, H.L.; Brown, E.L.; Nandy, R.K.; Ramamurthy, T.; Sinha, A.; Ghosh, S.; Guin, S.; Gurleen, K.; Rodrigues, S.; Chen, J.J.; McKenzie, R.; Steffen, R. Microbial etiology of travelers' diarrhea in Mexico, Guatemala, and India: importance of enterotoxigenic Bacteroides fragilis and Arcobacter species. J. Clin. Microbiol., 2010, 48, 1417-1419.
77. Sahl, J.W.; Steinsland, H.; Redman, J.C.; Angiuoli, S.V.; Nataro, J.P.; Sommerfelt, H.; Rasko, D.A. A comparative genomic analysis of diverse clonal types of enterotoxigenic Escherichia coli reveals pathovar-specific conservation. Infect. Immun., 2011, 79, 950-960.
78. Wenneras, C.; Erling, V. Prevalence of enterotoxigenic Escherichia coli-associated diarrhoea and carrier state in the developing world. J. Health Popul. Nutr., 2004, 22, 370-382.
79. WHO. Future directions for research on enterotoxigenic Escherichia coli vaccines for developing countries. Wkly. Epidemiol. Record., 2006, 81, 97-104.
80. Yoder, J.S.; Cesario, S.; Plotkin, V.; Ma, X.; Kelly-Shannon, K.; Dworkin, M.S. Outbreak of enterotoxigenic Escherichia coli infection with an unusually long duration of illness. Clin. Infect. Dis., 2006, 42, 1513-1517.
81. WHO. Initiative for Vaccine Research (IVR), Diarrhoeal Diseases (Updated February 2009), Enterotoxigenic Escherichia coli (ETEC). 2012.
82. Cao, L.; Suo, Z.; Lim, T.; Jun, S.; Deliorman, M.; Riccardi, C.; Kellerman, L.; Avci, R.; Yang, X. Role of overexpressed CFA/I fimbriae in bacterial swimming. Phys. Biol.; 2012, 9, 036005.
83. Suo, Z.; Yang, X.; Avci, R.; Deliorman, M.; Rugheimer, P.; Pascual, D.W.; Idzerda, Y. Antibody selection for immobilizing living bacteria. Anal. Chem., 2009, 81, 7571-7578.
84. Lásaro, M.O.; Luiz, W.B.; Sbrogio-Almeida, M.E.; Nishimura, L.S.; Guth, B.E.; Ferreira, L.C. Combined vaccine regimen based on parenteral priming with a DNA vaccine and administration of an oral booster consisting of a recombinant Salmonella enterica serovar Typhimurium vaccine strain for immunization against infection with human-derived enterotoxigenic Escherichia coli strains. Infect. Immun., 2004, 72, 6480-6491.
85. Armstrong, G.L., Hollingsworth, J.; Morris, J.G. Jr. Emerging foodborne pathogens: Escherichia coli O157:H7 as a model of entry of a new pathogen into the food supply of the developed world. Epidemiol. Rev., 1996, 18, 29-51.
86. Brady, M.J.; Lisay, C.M.; Yurkovetskiy, A.V.; Sawan, S.P. Persistent silver disinfectant for the environmental control of pathogenic bacteria. Am. J. Infect. Control., 2003, 31, 208-2014.
87. Mattick, K.; Durham, K.; Domingue, G.; Jorgensen, F.; Sen, M.; Schaffner, D.W.; Humphrey, T. The survival of foodborne pathogens during domestic washing-up and subsequent transfer onto washing-up sponges, kitchen surfaces and food. Int. J. Food Microbiol., 2003, 85, 213-226.
88. Berry, E.D.; Dorsa, W.J.; Siragusa, G.R.; Koohmaraie, M. Bacterial cross-contamination of meat during liquid nitrogen immersion freezing. J. Food Prot., 1998, 61, 1103-1108.
89. Uhitil, S.; Jaksic, S.; Petrak, T.; Botka-Petrak, K. Presence of Escherichia coli O157:H7 in ground beef and ground baby beef meat. J. Food Prot., 2001, 64, 862-864.
90. Riley, L.W.; Remis, R.S.; Helgerson, S.D.; McGee, H.B.; Wells, J.G.; Davis, B.R.; Hebert, R.J.; Olcott, E.S.; Johnson, L.M.; Hargrett, N.T.; Blake, P.A.; Cohen, M.L. Hemorrhagic colitis associated with a rare Escherichia coli serotype. N. Engl. J. Med., 1983, 308, 681-685.
91. Berin, M.C.; Darfeuille-Michaud, A.; Egan, L.J.; Miyamoto, Y.; Kagnoff, M.F. Role of EHEC O157:H7 virulence factors in the activation of intestinal epithelial cell NF-kappaB and MAP kinase pathways and the upregulated expression of interleukin 8. Cell Microbiol, 2002, 4, 635-648.
92. Croxen, M.A., Finlay BB. Molecular mechanisms of Escherichia coli pathogenicity. Nat. Rev. Microbiol., 2010, 8, 26-38.
93. Oliveira, A.F.; Cardoso, S.A.; Almeida, F.B.; de Oliveira, L.L.; Pitondo-Silva, A.; Soares, S.G.; Hanna, E.S. Oral immunization with attenuated Salmonella vaccine expressing Escherichia coli O157:H7 intimin gamma triggers both systemic and mucosal humoral immunity in mice. Microbiol. Immunol., 2012, 56, 513-522.
94. Gu, J.; Ning, Y.; Wang, H.; Xiao, D.; Tang, B.; Luo, P.; Cheng, Y.; Jiang, M., Li, N.; Zou, Q.; Mao, X. Vaccination of attenuated EISproducing Salmonella induces protective immunity against enterohemorrhagic Escherichia coli in mice. Vaccine, 2011, 29, 7395-7403.
95. Khare, S.; Alali, W.; Zhang, S.; Hunter, D.; Pugh, R.; Fang, F.C.; Libby, S.J.; Adams, L.G. Vaccination with attenuated Salmonella enterica Dublin expressing E coli O157:H7 outer membrane protein Intimin induces transient reduction of fecal shedding of E coli O157:H7 in cattle. BMC. Vet. Res., 2010, 6, 35.
96. Polk, D.B.; Peek, R.M. Jr. Helicobacter pylori: gastric cancer and beyond. Nat. Rev. Cancer, 2010, 10, 403-414.
97. Peek, R.M. Jr., Blaser, M.J. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat. Rev. Cancer, 2002, 2, 28-37.
98. Herrera, V.; Parsonnet, J. Helicobacter pylori and gastric adenocarcinoma. Clin. Microbiol. Infect.; 2009, 15, 971-976.
99. Graham, D.Y.; Lu, H.; Yamaoka, Y. A report card to grade Helicobacter pylori therapy. Helicobacter, 2007, 12, 275-278.
100. Liu, K.Y.; Shi, Y.; Luo, P.; Yu, S.; Chen, L.; Zhao, Z.; Mao, X.H.; Guo, G.; Wu, C.; Zou, Q.M. Therapeutic efficacy of oral immunization with attenuated Salmonella typhimurium expressing Helicobacter pylori CagA, VacA and UreB fusion proteins in mice model. Vaccine, 2011, 29, 6679-6685.
101. Chen, J.; Lin, M.; Li, N.; Lin, L.; She, F. Therapeutic vaccination with Salmonella-delivered codon-optimized outer inflammatory protein DNA vaccine enhances protection in Helicobacter pylori infected mice. Vaccine, 2012, 30, 5310-5315.
102. DiPetrillo, M.D.; Tibbetts, T.; Kleanthous, H.; Killeen, K.P.; Hohmann, E.L. Safety and immunogenicity of phoP/phoQ-deleted Salmonella typhi expressing Helicobacter pylori urease in adult volunteers. Vaccine, 1999, 18, 449-459.
103. Bumann, D.; Metzger, W.G.; Mansouri, E.; Palme, O.; Wendland, M.; Hurwitz, R.; Haas, G.; Aebischer, T.; von Specht, B.U.; Meyer, T.F. Safety and immunogenicity of live recombinant Salmonella enterica serovar Typhi Ty21a expressing urease A and B from Helicobacter pylori in human volunteers. Vaccine, 2001, 20, 845-852.
104. Aebischer, T.; Bumann, D.; Epple, H.J.; Metzger, W.; Schneider, T.; Cherepnev, G.; Walduck, A.K.; Kunkel, D.; Moos, V.; Loddenkemper, C.; Jiadze, I.; Panasyuk, M.; Stolte, M.; Graham, D.Y.; Zeitz, M.; Meyer, T.F. Correlation of T cell response and bacterial clearance in human volunteers challenged with Helicobacter pylori revealed by randomised controlled vaccination with Ty21a-based Salmonella vaccines. Gut, 2008, 57, 1065-1072.
105. Nauciel, C.; Espinasse-Maes, F. Role of gamma interferon and tumor necrosis factor alpha in resistance to Salmonella typhimurium infection. Infect. Immun., 1992, 60, 450-454.
106. Mastroeni, P.; Villarreal-Ramos, B.; Hormaeche, C.E. Role of T cells, TNFa and IFNg in recall of immunity to oral challenge with virulent salmonellae in mice vaccinated with live attenuated aro-salmonella vaccines. Microb. Pathog., 1992, 13, 477-491.
107. VanCott, J.L.; Staats, H.F.; Pascual, D.W.; Roberts, M.; Chatfield, S.N.; Yamamoto, M.; Coste, M.; Carter, P.B.; Kiyono, H.; McGhee, J.R. Regulation of mucosal and systemic antibody responses by T helper cell subsets, macrophages, and derived cytokines following oral immunization with live recombinant Salmonella. J. Immunol., 1996, 156, 1504-1514.
108. Ravindran, R.; Foley, J.; Stoklasek, T.; Glimcher, L.H.; McSorley, S.J. Expression of T-bet by CD4 T cells is essential for resistance to Salmonella infection. J. Immunol., 2005, 175, 4603-4610.
109. Becher, D.; Deutscher, M.E.; Simpfendorfer, K.R.; Wijburg, O.L.; Pederson, J.S.; Lew, A.M.; Strugnell, R.A.; Walduck, A.K. Local recall responses in the stomach involving reduced regulation and expanded help mediate vaccine-induced protection against Helicobacter pylori in mice. Eur. J. Immunol., 2010, 40, 2778-2790.
110. WHO. World Health Organization. Global tuberculosis control surveillance, planning, financing: WHO report 2010. Document WHO/HTM/TB/2010.104. World Health Organization, Geneva, Switzerland., 2010.
111. Nuttall, J.J.; Eley, B.S. BCG vaccination in HIV-Infected children. Tuberc. Res. Treat., 2011, 712-736.
112. Hesseling, A.C.; Marais, B.J.; Gie, R.P.; Schaaf, H.S.; Fine, P.E.; Godfrey-Faussett, P.; Beyers, N. The risk of disseminated Bacille Calmette-Guerin (BCG) disease in HIV-infected children. Vaccine, 2007, 25, 14-18.
113. Juárez-Rodríguez, M.D.; Arteaga-Cortés, L.T.; Kader, R.; Curtiss, R.; 3rd, Clark-Curtiss, J.E. Live attenuated Salmonella vaccines against Mycobacterium tuberculosis with antigen delivery via the type III secretion system. Infect, Immun., 2012, 80, 798-814.
114. Huang, J.M.; Sali, M.; Leckenby, M.W.; Radford, D.S.; Huynh, H.A.; Delogu, G.; Cranenburgh, R.M.; Cutting, S.M. Oral delivery of a DNA vaccine against tuberculosis using operator-repressor titration in a Salmonella enterica vector. Vaccine, 2010, 28, 7523-7528.
115. Kotloff, K.L.; Winickoff, J.P.; Ivanoff, B.; Clemens, J.D.; Swerdlow, D.L.; Sansonetti, P.J.; Adak, G.K.; Levine, M.M. Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull World Health Organ, 1999, 77, 651-666.
116. WHO. Initiative for Vaccine Research (IVR): Diarrhoeal Diseases-Shigellosis. http://www.who.int/vaccine_research/diseases/diarrhoeal/en/index6.html, 2009.
117. Oberhelman, R.A.; opecko, D.J.; Salazar-Lindo, E.; Gotuzzo, E.; Buysse, J.M.; Venkatesan, M.M.; Yi, A.; Fernandez-Prada, C.; Guzman, M.; Leon-Barua, R. Prospective study of systemic and mucosal immune responses in dysenteric patients to specific Shigella invasion plasmid antigens and lipopolysaccharides. Infect. Immun.; 1991, 59, 2341-2350.
118. Winsor, D.K.; Mathewson, J.J.; Dupont, H.L. Comparison of serum and fecal antibody-responses of patients with naturally acquired Shigella sonnei infection. J. Infect. Dis., 1988, 158, 1108-1112.
119. Xu de, Q.; Cisar, J.O.; Osorio, M.; Wai, T.T.; Kopecko, D.J. Corelinked LPS expression of Shigella dysenteriae serotype 1 O-antigen in live Salmonella Typhi vaccine vector Ty21a: preclinical evidence of immunogenicity and protection. Vaccine, 2007, 25, 6167-6175.
120. Alvarez, M.L.; Cardineau, G.A. Prevention of bubonic and pneumonic plague using plant-derived vaccines. Biotechnol. Adv., 2010, 28, 184-96.
121. Williamson ED. Plague. Vaccine, 2009, 27 Suppl 4, D56-60.
122. Russell, P.; Eley, S.M.; Hibbs, S.E.; Manchee, R.J.; Stagg, A.J.; Titball, R.W. A comparison of plague vaccine, USP and EV76 vaccine induced protection against Yersinia pestis in a murine model. Vaccine, 1995, 13, 1551-1556.
123. Perry, R.D.; Fetherston, J.D. Yersiniabactin iron uptake: mechanisms and role in Yersinia pestis pathogenesis. Microbes Infect., 2011, 13, 808-817.
124. Prentice, M.B.; Rahalison, L. Plague. Lancet, 2007, 369, 1196-1207.
125. CDC. Emergency Preparedness and Response: Facts about Pneumonic Plague. Centers for Disease Control and Prevention. http://www.bt.cdc.gov/agent/plague/factsheet.asp., 2004.
126. Waterer, G.W.; Robertson, H. Bioterrorism for the respiratory physician. Respirology, 2009, 14, 5-11.
127. Kool, J.L. Risk of person-to-person transmission of pneumonic plague. Clin. Infect. Dis., 2005, 40, 1166-1172.
128. Rosenzweig, J.A.; Chopra, A.K. The future of plague vaccines: hopes raised by a surrogate, live-attenuated recombinant vaccine candidate. Expert. Rev. Vaccines, 2012, 11, 659-661.
129. Andrews, G.P.; Heath, D.G.; Anderson, G.W. Jr., Welkos, S.L.; Friedlander, A.M. Fraction 1 capsular antigen (F1) purification from Yersinia pestis CO92 and from an Escherichia coli recombinant strain and efficacy against lethal plague challenge. Infect. Immun., 1996, 64, 2180-2187.
130. Espina, M.; Ausar, S.F.; Middaugh, C.R.; Baxter, M.A.; Picking, W.D.; Picking, W.L. Conformational stability and differential structural analysis of LcrV, PcrV, BipD, and SipD from type III secretion systems. Protein Sci., 2007, 16, 704-714.
131. Leary, S.E.; Eley, S.M.; Williamson, E.D.; Titball, R.W. Expression of Yersinia pestis V antigen in attenuated Salmonella typhimurium: development of a novel vaccine for plague. Contrib. Microbiol. Immunol., 1995, 13, 216-217.
132. Meka-Mechenko, T.V. F1-negative natural Y. pestis strains. Adv. Exp. Med. Biol., 2003, 529, 379-381.
133. Yang, X.H.; Hinnebusch, B.J.; Trunkle, T.; Bosio, C.M.; Suo, Z.Y.; Tighe, M.; Harmsen, A.; Becker, T.; Crist, K.; Walters, N.; Avci, R.; Pascual, D.W. Oral vaccination with Salmonella simultaneously expressing Yersinia pestis F1 and V antigens protects against bubonic and pneumonic plague. J. Immunol., 2007, 178, 1059-1067.
134. Sizemore, D.; Warner, E.; Lawrence, J.; Thomas, L.J.; Roland, K.; Killeen, K. Construction and screening of attenuated ΔphoP/Q Salmonella typhimurium vectored plague vaccine candidates. Hum. Vaccin Immunother., 2012, 8.
135. Parent, M.A.; Wilhelm, L.B.; Kummer, L.W.; Szaba, F.M.; Mullarky, I.K.; Smiley, S.T. Gamma interferon, tumor necrosis factor alpha, and nitric oxide synthase 2, key elements of cellular immunity, perform critical protective functions during humoral defense against lethal pulmonary Yersinia pestis infection. Infect. Immun., 2006, 74, 3381-3386.
136. Charles, R.C.; Harris, J.B.; Chase, M.R.; Lebrun, L.M.; Sheikh, A.; LaRocque, R.C.; Logvinenko, T.; Rollins, S.M.; Tarique, A.; Hohmann, E.L.; Rosenberg, I.; Krastins, B.; Sarracino, D.A.; Qadri, F.; Calderwood, S.B.; Ryan, E.T. Comparative proteomic analysis of the PhoP regulon in Salmonella enterica serovar Typhi versus Typhimurium. PLoS One, 2009, 4, e6994.
137. Li, Y.; Wang, S.; Xin, W.; Scarpellini, G.; Shi, Z.; Gunn, B.; Roland, K.L.; Curtiss, R. 3rd. A sopB deletion mutation enhances the immunogenicity and protective efficacy of a heterologous antigen delivered by live attenuated Salmonella enterica vaccines. Infect. Immun., 2008, 76, 5238-5246.
138. Kong, Q.; Six, D.A.; Roland, K.L.; Liu, Q.; Gu, L.; Reynolds, C.M.; Wang, X.; Raetz, C.R.; Curtiss, R. 3rd. Salmonella synthesizing 1-dephosphorylated [corrected] lipopolysaccharide exhibits low endotoxic activity while retaining its immunogenicity. J. Immunol., 2011, 187, 412-4123.
139. Pascual, D.W.; Ochoa-Repáraz, J.; Rynda, A.; Yang, X. Tolerance in the absence of autoantigen. Endocr. Metab. Immune Disord Drug Targets, 2007, 7, 203-210.
140. Ochoa-Repáraz, J.; Rynda, A.; Ascón, M.A.; Yang, X.; Kochetkova, I.; Riccardi, C.; Callis, G.; Trunkle, T.; Pascual, D.W. IL-13 production by regulatory T cells protects against experimental autoimmune encephalomyelitis independently of autoantigen. J. Immunol.; 2008, 181, 954-968.
141. Kochetkova, I.; Thornburg, T.; Callis, G.; Pascual, D.W. Segregated regulatory CD39+CD4+ T cell function: TGF-bproducing Foxp3-and IL-10-producing Foxp3+ cells are interdependent for protection against collagen-induced arthritis. J. Immunol., 2011, 187, 4654-4666.
142. Bobat, S.; Flores-Langarica, A.; Hitchcock, J.; Marshall, J.L.; Kingsley, R.A.; Goodall, M.; Gil-Cruz, C.; Serre, K.; Leyton, D.L.; Letran, S.E.; Gaspal, F.; Chester, R.; Chamberlain, J.L.; Dougan, G.; Lopez-Macias, C.; Henderson, I.R.; Alexander, J.; MacLennan, I.C.; Cunningham, A.F. Soluble flagellin, FliC, induces an Agspecific Th2 response, yet promotes T-bet-regulated Th1 clearance of Salmonella typhimurium infection. Eur. J. Immunol., 2011, 41, 1606-1618.
143. Kruh, N.A.; Troudt, J.; Izzo, A.; Prenni, J.; Dobos, K.M. Portrait of a pathogen: the Mycobacterium tuberculosis proteome in vivo. PLoS One, 2010, 5, e13938.
144. Pujol, C.; Grabenstein, J.P.; Perry, R.D.; Bliska, J.B. Replication of Yersinia pestis in interferon gamma-activated macrophages requires ripA, a gene encoded in the pigmentation locus. Proc. Natl. Acad. Sci. U S A., 2005, 102, 12909-12914.
145. Kidd, P. Th1/Th2 balance: the hypothesis, its limitations, and implications for health and disease. Altern. Med. Rev., 2003, 8, 223-246.
146. Bonnel, C.; Arteaga-Cortes, L.; Ench, Y.; Leland, M.; Dube, P.; Kraig, E. Effects of age on the immune response in baboons to the Y. pestis F1 vaccine antigen. J. Immunol., 2012, 188.
147. Lee, J.S.; Jung, I.D.; Lee, C.M.; Park, J.W.; Chun, S.H.; Jeong, S.K.; Ha, T.K.; Shin, Y.K.; Kim, D.J.; Park, Y.M. Outer membrane protein a of Salmonella enterica serovar Typhimurium activates dendritic cells and enhances Th1 polarization. BMC Microbiol, 2010, 10, 263.
148. McFarland, L.V. Epidemiology, risk factors and treatments for antibiotic-associated diarrhea. Dig. Dis., 1998, 16, 292-307.
149. Jakobsson, H.E.; Jernberg, C.; Andersson, A.F.; Sjolund-Karlsson, M.; Jansson, J.K.; Engstrand, L. Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS One, 2010, 5, 9836.
150. Donskey, C.J. The role of the intestinal tract as a reservoir and source for transmission of nosocomial pathogens. Clin. Infect. Dis., 2004, 39, 219-226.