Enhancement of Host Immune Responses by Oral Vaccination to Salmonella enterica serovar Typhimurium Harboring Both FliC and FljB Flagella

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Eom, Jeong Seon ^a   Seok Kim, Jin ^a   Im Jang, Jung ^a   Kim, Bae Hoon ^a,d   Young Yoo, So ^a   Hyeon Choi, Ji ^a   Bang, Iel Soo ^b   Lee, In Soo ^c   Keun Park, Yong ^a  

^a Korea University   (South Korea)

^b Chosun University   (South Korea)

^c Hannam University   (South Korea)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G; PROTEIN FLIC; PROTEIN FLJB; SALMONELLOSIS VACCINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGENICITY; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; FEMALE; FLAGELLUM; GENE EXPRESSION; IMMUNE RESPONSE; MACROPHAGE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SALMONELLA TYPHIMURIUM; SALMONELLOSIS;

ADMINISTRATION, ORAL; ANIMALS; ANTIGENS, BACTERIAL; CELL LINE; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; FEMALE; FLAGELLA; FLAGELLIN; GENE EXPRESSION; INFLAMMATION MEDIATORS; MACROPHAGES; MICE; MUTATION; NF-KAPPA B; PROTEIN TRANSPORT; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SALMONELLA VACCINES; VACCINATION;

EID: 84884252019     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074850     Document Type: Article

References (40)

1. Mireles JR 2nd, Toguchi A, Harshey RM, (2001) Salmonella enterica serovar Typhimurium swarming mutants with altered biofilm-forming abilities: surfactin inhibits biofilm formation. J Bacteriol 183: 5848-5854. doi:10.1128/JB.183.20.5848-5854.2001. PubMed: 11566982.
2. Foley SL, Lynne AM, (2008) Food animal-associated Salmonella challenges: pathogenicity and antimicrobial resistance. J Anim Sci 86: E173-E187. PubMed: 17878285.
3. Olusesan AG, Nonyelum O, Ebere OCL, Olorunmola EJ, (2010) Plasmid DNA analysis and conjugative study of antibiotic resistant Salmonella typhi and paratyphi to ten selected antibiotics in Zaria, Nigeria. J Postgrad Med 4: 151-157.
4. de Jong HK, Parry CM, van der Poll T, Wiersinga WJ, (2012) Host-pathogen interaction in invasive Salmonellosis. PLOS Pathog 8(10):: e1002933. PubMed: 23055923.
5. Mogensen TH, (2009) Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 22: 240-273. doi:10.1128/CMR.00046-08. PubMed: 19366914.
6. Blair DF, (1995) How Bacteria Sense and Swim. Annu Rev Microbiol 49: 489-522. doi:10.1146/annurev.mi.49.100195.002421. PubMed: 8561469.
7. Eom JS, Kim JS, Jang JI, Kim HG, Bang IS, et al. (2012) Effect of iacP mutation on flagellar phase variation in Salmonella enterica serovar Typhimurium strain UK-1. J Bacteriol 194: 4332-4341. doi:10.1128/JB.00076-12. PubMed: 22685287.
8. Yang X, Thornburg T, Suo Z, Jun S, Robison A, et al. (2012) Flagella overexpression attenuates Salmonella pathogenesis. PLOS ONE 7: e46828. doi:10.1371/journal.pone.0046828. PubMed: 23056473.
9. Miao EA, Andersen-Nissen E, Warren SE, Aderem A, (2007) TLR5 and Ipaf: dual sensors of bacterial flagellin in the innate immune system. Semin Immunopathol 29: 275-288. doi:10.1007/s00281-007-0078-z. PubMed: 17690885.
10. Simon R, Samuel CE, (2007) Activation of NF-kappaB-dependent gene expression by Salmonella flagellins FliC and FljB. Biochem Biophys Res Commun 355: 280-285. doi:10.1016/j.bbrc.2007.01.148. PubMed: 17292856.
11. Yamamoto S, Kutsukake K, (2006) FljA-mediated posttranscriptional control of phase 1 flagellin expression in flagellar phase variation of Salmonella enterica serovar Typhimurium. J Bacteriol 188: 958-967. doi:10.1128/JB.188.3.958-967.2006. PubMed: 16428400.
12. McSorley SJ, Ehst BD, Yu Y, Gewirtz AT, (2002) Bacterial flagellin is an effective adjuvant for CD4+ T cells in vivo. J Immunol 169: 3914-3919. PubMed: 12244190.
13. Dunstan SJ, Simmons CP, Strugnell RA, (1998) Comparison of the abilities of different attenuated Salmonella typhimurium strains to elicit humoral immune responses against a heterologous antigen. Infect Immun 66: 732-740. PubMed: 9453634.
14. Datsenko KA, Wanner BL, (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645. doi:10.1073/pnas.120163297. PubMed: 10829079.
15. Uchiya K, Nikai T, (2008) Salmonella virulence factor SpiC is involved in expression of flagellin protein and mediates activation of the signal transduction pathways in macrophages. Microbiology 154: 3491-3502. PubMed: 18957602.
16. Kutsukake K, Nakashima H, Tominaga A, Abo T, (2006) Two DNA invertases contribute to flagellar phase variation in Salmonella enterica serovar Typhimurium strain LT2. J Bacteriol 188: 950-957. doi:10.1128/JB.188.3.950-957.2006. PubMed: 16428399.
17. Liang HY, Xia LQ, Wu ZH, Jian JC, Lu YS, (2010) Expression, purification and antibody preparation of flagellin FlaA from Vibrio alginolyticus strain HY9901. Lett Appl Microbiol 50: 181-186. doi:10.1111/j.1472-765X.2009.02768.x. PubMed: 19951364.
18. Rosu V, Chevance FF, Karlinsey JE, Hirano T, Hughes KT, (2006) Translation inhibition of the Salmonella fliC gene by the fliC 5' untranslated region, fliC coding sequences, and FlgM. J Bacteriol 188: 4497-4507. doi:10.1128/JB.01552-05. PubMed: 16740956.
19. Pieper GM, Olds C, Hilton G, Lindholm PF, Adams MB, et al. (2001) Antioxidant treatment inhibits activation of myocardial nuclear factor kappa B and inhibits nitrosylation of myocardial heme protein in cardiac transplant rejection. Antioxid Redox Signal 3: 81-88. doi:10.1089/152308601750100542. PubMed: 11291601.
20. Wang S, Kotamraju S, Konorev E, Kalivendi S, Joseph J, et al. (2002) Activation of nuclear factor-kappaB during doxorubicin-induced apoptosis in endothelial cells and myocytes is pro-apoptotic: The role of hydrogen peroxide. Biochem J 367: 729-740. doi:10.1042/BJ20020752. PubMed: 12139490.
21. Tallant T, Deb A, Kar N, Lupica J, de Veer MJ, et al. (2004) Flagellin acting via TLR5 is the major activator of key signaling pathways leading to NF-kappa B and proinflammatory gene program activation in intestinal epithelial cells. BMC Microbiol 4: 33. doi:10.1186/1471-2180-4-33. PubMed: 15324458.
22. Hur J, Lee JH, (2011) Enhancement of immune responses by an attenuated Salmonella enterica serovar Typhimurium strain secreting an Escherichia coli heat-labile enterotoxin B subunit protein as an adjuvant for a live Salmonella vaccine candidate. Clin Vaccine Immunol 18: 203-209. doi:10.1128/CVI.00407-10. PubMed: 21159921.
23. Gauley J, Pisetsky DS, (2010) The release of microparticles by RAW 264.7 macrophage cells stimulated with TLR ligands. J Leukoc Biol 87: 1115-1123. doi:10.1189/jlb.0709465. PubMed: 20335312.
24. Nalbantsoy A, Karaboz I, Ivanova R, Deliloglu-Gurhan I, (2010) Isolation and purification of O and H antigens from Salmonella Enteritidis as diagnostic tool. Ann Microbiol 60: 565-571. doi:10.1007/s13213-010-0093-5.
25. Lyons S, Wang L, Casanova JE, Sitaraman SV, Merlin D, et al. (2004) Salmonella typhimurium transcytoses flagellin via an SPI2-mediated vesicular transport pathway. J Cell Sci 117: 5771-5780. doi:10.1242/jcs.01500. PubMed: 15507487.
26. Sun YH, Rolán HG, Tsolis RM, (2007) Injection of flagellin into the host cell cytosol by Salmonella enterica serotype Typhimurium. J Biol Chem 282: 33897-33901. doi:10.1074/jbc.C700181200. PubMed: 17911114.
27. Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, et al. (2006) Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 7: 569-575. doi:10.1038/ni1344. PubMed: 16648853.
28. Franchi L, Amer A, Body-Malapel M, Kanneganti TD, Ozören N, et al. (2006) Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat Immunol 7: 576-582. doi:10.1038/ni1346. PubMed: 16648852.
29. Simon R, Samuel CE, (2008) Interleukin-1 beta secretion is activated comparably by FliC and FljB flagellins but differentially by wild-type and DNA adenine methylase-deficient Salmonella. J Interferon Cytokine Res 28: 661-666. doi:10.1089/jir.2008.0022. PubMed: 18844581.
30. Pietilä TE, Veckman V, Kyllönen P, Lähteenmäki K, Korhonen TK, et al. (2005) Activation, cytokine production, and intracellular survival of bacteria in Salmonella-infected human monocyte-derived macrophages and dendritic cells. J Leukoc Biol 78: 909-920. doi:10.1189/jlb.1204721. PubMed: 16033811.
31. Bandyopadhaya A, Sarkar M, Chaudhuri K, (2008) IL-1beta expression in Int407 is induced by flagellin of Vibrio cholerae through TLR5 mediated pathway. Microb Pathog 44: 524-536. doi:10.1016/j.micpath.2008.01.004. PubMed: 18314303.
32. Mizel SB, Bates JT, (2010) Flagellin as an Adjuvant: Cellular Mechanisms and Potential. J Immunol 185: 5677-5682. doi:10.4049/jimmunol.1002156. PubMed: 21048152.
33. Kim JS, Eom JS, Jang JI, Kim HG, Seo DW, et al. (2011) Role of Salmonella pathogenicity island 1 protein IacP in Salmonella enterica serovar Typhimurium pathogenesis. Infect Immun 79: 1440-1450. doi:10.1128/IAI.01231-10. PubMed: 21263021.
34. Yu Y, Nagai S, Wu H, Neish AS, Koyasu S, et al. (2006) TLR5-mediated phosphoinositide 3-kinase activation negatively regulates flagellin-induced proinflammatory gene expression. J Immunol 176: 6194-6201. PubMed: 16670329.
35. Berg HC, (2003) The rotary motor of bacterial flagella. Annu Rev Biochem 72: 19-54. doi:10.1146/annurev.biochem.72.121801.161737. PubMed: 12500982.
36. Scharf B, (2002) Real-time imaging of fluorescent flagellar filaments of Rhizobium lupini H13-3: flagellar rotation and pH-induced polymorphic transitions. J Bacteriol 184: 5979-5986. doi:10.1128/JB.184.21.5979-5986.2002. PubMed: 12374832.
37. Moreno M, Audia JP, Bearson SM, Webb C, Foster JW, (2000) Regulation of sigma S degradation in Salmonella enterica var Typhimurium: in vivo interactions between sigma S, the response regulator MviA(RssB) and ClpX. J Mol Microbiol Biotechnol 2: 245-254. PubMed: 10939250.
38. Chatfield SN, Charles IG, Makoff AJ, Oxer MD, Dougan G, et al. (1992) Use of the nirB promoter to direct the stable expression of heterologous antigens in Salmonella oral vaccine strains: Development of a single-dose oral tetanus vaccine. Biotechnology (N Y) 10: 888-892. doi:10.1038/nbt0892-888. PubMed: 1368983.
39. Ehrbar K, Winnen B, Hardt WD, (2006) The chaperone binding domain of SopE inhibits transport via flagellar and SPI-1 TTSS in the absence of InvB. Mol Microbiol 59: 248-264. doi:10.1111/j.1365-2958.2005.04931.x. PubMed: 16359332.
40. Guzman LM, Belin D, Carson MJ, Beckwith J, (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130. PubMed: 7608087.