1921
Volume 90, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

We assessed interferon-gamma (IFN-γ) responses via enzyme-linked immunosorbent spot (ELISPOT) to a number of Typhi antigens in samples from humans with Typhi bacteremia and typhoid fever in Bangladesh. Compared with responses in healthy endemic zone controls, there were significantly increased IFN-γ responses at the time of clinical presentation (acute phase) and at convalescence 14–28 days later. The majority (80–90%) of IFN-γ expressing T cells were CD4+. We observed a significant increase in interleukin-17 (IL-17) positive CD4 + T cells at convalescent versus acute stage of infection using an intracellular cytokine staining assay. We also found that stimulated peripheral blood mononuclear cells (PBMCs) produced significantly increased levels of a number of cytokines at the convalescent versus acute phase of infection, including IFN-γ, MIP-1β, sCD40L, TNF-β, IL-13, and IL-9. These results suggest that Typhi antigens induce a predominantly Th1 response, but that elevations in other cytokines may be modulatory.

[open-access] This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.13-0261
2014-06-04
2017-09-23
Loading full text...

Full text loading...

/deliver/fulltext/14761645/90/6/1024.html?itemId=/content/journals/10.4269/ajtmh.13-0261&mimeType=html&fmt=ahah

References

  1. Crump JA, Luby SP, Mintz ED, , 2004. The global burden of typhoid fever. Bull World Health Organ 82: 346353.
  2. Hornick RB, Greisman SE, Woodward TE, DuPont HL, Dawkins AT, Snyder MJ, , 1970. Typhoid fever: pathogenesis and immunologic control. 2. N Engl J Med 283: 739746.[Crossref]
  3. Sztein MB, , 2007. Cell-mediated immunity and antibody responses elicited by attenuated Salmonella enterica serovar Typhi strains used as live oral vaccines in humans. Clin Infect Dis 45 (Suppl 1): S15S19.[Crossref]
  4. Moon JJ, McSorley SJ, , 2009. Tracking the dynamics of Salmonella specific T cell responses. Curr Top Microbiol Immunol 334: 179198.
  5. Wahid R, Salerno-Goncalves R, Tacket CO, Levine MM, Sztein MB, , 2007. Cell-mediated immune responses in humans after immunization with one or two doses of oral live attenuated typhoid vaccine CVD 909. Vaccine 25: 14161425.[Crossref]
  6. Salerno-Goncalves R, Wyant TL, Pasetti MF, Fernandez-Vina M, Tacket CO, Levine MM, Sztein MB, , 2003. Concomitant induction of CD4+ and CD8+ T cell responses in volunteers immunized with Salmonella enterica serovar Typhi strain CVD 908-htrA . J Immunol 170: 27342741.[Crossref]
  7. Sheikh A, Khanam F, Sayeed MA, Rahman T, Pacek M, Hu Y, Rollins A, Bhuiyan MS, Rollins S, Kalsy A, Arifuzzaman M, Leung DT, Sarracino DA, Krastins B, Charles RC, LaRocque RC, Cravioto A, Calderwood SB, Brooks WA, Harris JB, Labaer J, Qadri F, Ryan ET, , 2011. Interferon-gamma and proliferation responses to Salmonella enterica serotype Typhi proteins in patients with S. Typhi bacteremia in Dhaka, Bangladesh. PLoS Negl Trop Dis 5: e1193.[Crossref]
  8. Harris JB, Baresch-Bernal A, Rollins SM, Alam A, LaRocque RC, Bikowski M, Peppercorn AF, Handfield M, Hillman JD, Qadri F, Calderwood SB, Hohmann E, Breiman RF, Brooks WA, Ryan ET, , 2006. Identification of in vivo-induced bacterial protein antigens during human infection with Salmonella enterica serovar Typhi. Infect Immun 74: 51615168.[Crossref]
  9. Naheed A, Ram PK, Brooks WA, Hossain MA, Parsons MB, Talukder KA, Mintz E, Luby S, Breiman RF, , 2010. Burden of typhoid and paratyphoid fever in a densely populated urban community, Dhaka, Bangladesh. Int J Infect Dis 14 (Suppl 3): e93e99.[Crossref]
  10. Rollenhagen JE, Kalsy A, Cerda F, John M, Harris JB, Larocque RC, Qadri F, Calderwood SB, Taylor RK, Ryan ET, , 2006. Transcutaneous immunization with toxin-coregulated pilin A induces protective immunity against Vibrio cholerae O1 El Tor challenge in mice. Infect Immun 74: 58345839.[Crossref]
  11. Johnson RA, Uddin T, Aktar A, Mohasin M, Alam MM, Chowdhury F, Harris JB, LaRocque RC, Bufano MK, Yu Y, Wu-Freeman Y, Leung DT, Sarracino D, Krastins B, Charles RC, Xu P, Kovac P, Calderwood SB, Qadri F, Ryan ET, , 2012. Comparison of immune responses to the O-specific polysaccharide and lipopolysaccharide of Vibrio cholerae O1 in Bangladeshi adult patients with cholera. Clin Vaccine Immunol 19: 17121721.[Crossref]
  12. Tarique AA, Kalsy A, Arifuzzaman M, Rollins SM, Charles RC, Leung DT, Harris JB, LaRocque RC, Sheikh A, Bhuiyan MS, Saksena R, Clements JD, Calderwood SB, Qadri F, Kovac P, Ryan ET, , 2012. Transcutaneous immunization with a Vibrio cholerae O1 Ogawa synthetic hexasaccharide conjugate following oral whole-cell cholera vaccination boosts vibriocidal responses and induces protective immunity in mice. Clin Vaccine Immunol 19: 594602.[Crossref]
  13. Sheikh A, Bhuiyan MS, Khanam F, Chowdhury F, Saha A, Ahmed D, Jamil KM, LaRocque RC, Harris JB, Ahmad MM, Charles R, Brooks WA, Calderwood SB, Cravioto A, Ryan ET, Qadri F, , 2009. Salmonella enterica serovar Typhi-specific immunoglobulin A antibody responses in plasma and antibody in lymphocyte supernatant specimens in Bangladeshi patients with suspected typhoid fever. Clin Vaccine Immunol 16: 15871594.[Crossref]
  14. Kuchta A, Rahman T, Sennott EL, Bhuyian TR, Uddin T, Rashu R, Chowdhury F, Kahn AI, Arifuzzaman M, Weil AA, Podolsky M, LaRocque RC, Ryan ET, Calderwood SB, Qadri F, Harris JB, , 2011. Vibrio cholerae O1 infection induces proinflammatory CD4+ T-cell responses in blood and intestinal mucosa of infected humans. Clin Vaccine Immunol 18: 13711377.[Crossref]
  15. Levine MM, Tacket CO, Sztein MB, , 2001. Host-Salmonella interaction: human trials. Microbes Infect 3: 12711279.[Crossref]
  16. Pulickal AS, Gautam S, Clutterbuck EA, Thorson S, Basynat B, Adhikari N, Makepeace K, Rijpkema S, Borrow R, Farrar JJ, Pollard AJ, , 2009. Kinetics of the natural, humoral immune response to Salmonella enterica serovar Typhi in Kathmandu, Nepal. Clin Vaccine Immunol 16: 14131419.[Crossref]
  17. Hess J, Ladel C, Miko D, Kaufmann SH, , 1996. Salmonella typhimurium aroA- infection in gene-targeted immunodeficient mice: major role of CD4+ TCR-alpha beta cells and IFN-gamma in bacterial clearance independent of intracellular location. J Immunol 156: 33213326.
  18. Pie S, Truffa-Bachi P, Pla M, Nauciel C, , 1997. Th1 response in Salmonella typhimurium-infected mice with a high or low rate of bacterial clearance. Infect Immun 65: 45094514.
  19. Butler T, Ho M, Acharya G, Tiwari M, Gallati H, , 1993. Interleukin-6, gamma interferon, and tumor necrosis factor receptors in typhoid fever related to outcome of antimicrobial therapy. Antimicrob Agents Chemother 37: 24182421.[Crossref]
  20. Thompson LJ, Dunstan SJ, Dolecek C, Perkins T, House D, Dougan G, Nguyen TH, Tran TP, Doan CD, Le TP, Nguyen TD, Tran TH, Farrar JJ, Monack D, Lynn DJ, Popper SJ, Falkow S, , 2009. Transcriptional response in the peripheral blood of patients infected with Salmonella enterica serovar Typhi. Proc Natl Acad Sci USA 106: 2243322438.[Crossref]
  21. Kumar G, Pratap CB, Mishra OP, Kumar K, Nath G, , 2012. Use of urine with nested PCR targeting the flagellin gene (fliC) for diagnosis of typhoid fever. J Clin Microbiol 50: 19641967.[Crossref]
  22. Bobat S, Flores-Langarica A, Hitchcock J, Marshall JL, Kingsley RA, Goodall M, Gil-Cruz C, Serre K, Leyton DL, Letran SE, Gaspal F, Chester R, Chamberlain JL, Dougan G, Lopez-Macias C, Henderson IR, Alexander J, MacLennan IC, Cunningham AF, , 2011. Soluble flagellin, FliC, induces an Ag-specific Th2 response, yet promotes T-bet-regulated Th1 clearance of Salmonella typhimurium infection. Eur J Immunol 41: 16061618.[Crossref]
  23. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, Wain J, Churcher C, Mungall KL, Bentley SD, Holden MT, Sebaihia M, Baker S, Basham D, Brooks K, Chillingworth T, Connerton P, Cronin A, Davis P, Davies RM, Dowd L, White N, Farrar J, Feltwell T, Hamlin N, Haque A, Hien TT, Holroyd S, Jagels K, Krogh A, Larsen TS, Leather S, Moule S, O'Gaora P, Parry C, Quail M, Rutherford K, Simmonds M, Skelton J, Stevens K, Whitehead S, Barrell BG, , 2001. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413: 848852.[Crossref]
  24. Weening EH, Barker JD, Laarakker MC, Humphries AD, Tsolis RM, Baumler AJ, , 2005. The Salmonella enterica serotype Typhimurium lpf, bcf, stb, stc, std, and sth fimbrial operons are required for intestinal persistence in mice. Infect Immun 73: 33583366.[Crossref]
  25. Townsend SM, Kramer NE, Edwards R, Baker S, Hamlin N, Simmonds M, Stevens K, Maloy S, Parkhill J, Dougan G, Baumler AJ, , 2001. Salmonella enterica serovar Typhi possesses a unique repertoire of fimbrial gene sequences. Infect Immun 69: 28942901.[Crossref]
  26. Zeiner SA, Dwyer BE, Clegg S, , 2012. FimA, FimF, and FimH are necessary for assembly of type 1 fimbriae on Salmonella enterica serovar Typhimurium. Infect Immun 80: 32893296.[Crossref]
  27. Taga ME, Semmelhack JL, Bassler BL, , 2001. The LuxS-dependent autoinducer AI-2 controls the expression of an ABC transporter that functions in AI-2 uptake in Salmonella typhimurium . Mol Microbiol 42: 777793.[Crossref]
  28. Choi J, Shin D, Kim M, Park J, Lim S, Ryu S, , 2012. LsrR-mediated quorum sensing controls invasiveness of Salmonella typhimurium by regulating SPI-1 and flagella genes. PLoS ONE 7: e37059.[Crossref]
  29. Gerstel U, Romling U, , 2003. The csgD promoter, a control unit for biofilm formation in Salmonella typhimurium . Res Microbiol 154: 659667.[Crossref]
  30. Dorner BG, Scheffold A, Rolph MS, Huser MB, Kaufmann SH, Radbruch A, Flesch IE, Kroczek RA, , 2002. MIP-1alpha, MIP-1beta, RANTES, and ATAC/lymphotactin function together with IFN-gamma as type 1 cytokines. Proc Natl Acad Sci USA 99: 61816186.[Crossref]
  31. McDyer JF, Goletz TJ, Thomas E, June CH, Seder RA, , 1998. CD40 ligand/CD40 stimulation regulates the production of IFN-gamma from human peripheral blood mononuclear cells in an IL-12- and/or CD28-dependent manner. J Immunol 160: 17011707.
  32. Raffatellu M, Santos RL, Verhoeven DE, George MD, Wilson RP, Winter SE, Godinez I, Sankaran S, Paixao TA, Gordon MA, Kolls JK, Dandekar S, Baumler AJ, , 2008. Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat Med 14: 421428.[Crossref]
  33. Mayuzumi H, Inagaki-Ohara K, Uyttenhove C, Okamoto Y, Matsuzaki G, , 2010. Interleukin-17A is required to suppress invasion of Salmonella enterica serovar Typhimurium to enteric mucosa. Immunology 131: 377385.[Crossref]
  34. Geddes K, Rubino SJ, Magalhaes JG, Streutker C, Le Bourhis L, Cho JH, Robertson SJ, Kim CJ, Kaul R, Philpott DJ, Girardin SE, , 2011. Identification of an innate T helper type 17 response to intestinal bacterial pathogens. Nat Med 17: 837844.[Crossref]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.13-0261
Loading
/content/journals/10.4269/ajtmh.13-0261
Loading

Data & Media loading...

Supplementary Data

Supplementary PDF

  • Received : 14 May 2013
  • Accepted : 05 Feb 2014

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error