Salmonella enterica serovar typhimurium lacking hfq gene confers protective immunity against murine typhoid

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Allam, Uday Shankar ^a   Krishna, M Gopala ^a   Lahiri, Amit ^a   Joy, Omana ^a   Chakravortty, Dipshikha ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G; LIPOPOLYSACCHARIDE; OUTER MEMBRANE PROTEIN; SALMONELLA TYPHIMURIUM VACCINE; SALMONELLOSIS VACCINE; SECRETORY IMMUNOGLOBULIN; UNCLASSIFIED DRUG; GAMMA INTERFERON; IMMUNOGLOBULIN A; INTERLEUKIN 6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ANTIGEN PRESENTATION; ARTICLE; BACTERIAL GENE; CD4 LYMPHOCYTE COUNT; CONTROLLED STUDY; DELETION MUTANT; DENDRITIC CELL; DRUG SAFETY; FEMALE; HFQ GENE; HUMAN; HUMAN CELL; IMMUNITY; IMMUNIZATION; IMMUNOGLOBULIN BLOOD LEVEL; MOUSE; NONHUMAN; PREGNANCY; SALMONELLA TYPHIMURIUM; SINGLE DRUG DOSE; STRAIN DIFFERENCE; TYPHOID FEVER; WILD TYPE; ANIMAL; BLOOD; CD4+ T LYMPHOCYTE; GENE DELETION; GENETICS; HUMORAL IMMUNITY; IMMUNOLOGY; INTESTINE; METABOLISM; MICROBIOLOGY; ORAL DRUG ADMINISTRATION; PATHOGENICITY; SALMONELLA ENTERICA; SPECIES DIFFERENCE; SPLEEN; TIME;

ANIMALIA; BACTERIA (MICROORGANISMS); MURINAE; MUS; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM;

ADMINISTRATION, ORAL; ANIMALS; ANTIGEN PRESENTATION; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; GENES, BACTERIAL; IMMUNITY, HUMORAL; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INTERFERON-GAMMA; INTERLEUKIN-6; INTESTINES; MICE; PREGNANCY; SALMONELLA ENTERICA; SALMONELLA VACCINES; SEQUENCE DELETION; SPECIES SPECIFICITY; SPLEEN; TIME FACTORS; TYPHOID FEVER;

EID: 79951796751     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016667     Document Type: Article

References (64)

1. Andrews-Polymenis HL, Baumler AJ, McCormick BA, Fang FC, (2010) Taming the elephant: Salmonella biology, pathogenesis, and prevention. Infect Immun 78: 2356-2369.
2. Chan K, Baker S, Kim CC, Detweiler CS, Dougan G, et al. (2003) Genomic comparison of Salmonella enterica serovars and Salmonella bongori by use of an S. enterica serovar Typhimurium DNA microarray. J Bacteriol 185: 553-563.
3. Nagarajan AG, Balasundaram SV, Janice J, Karnam G, Eswarappa SM, et al. (2009) SopB of Salmonella enterica serovar Typhimurium is a potential DNA vaccine candidate in conjugation with live attenuated bacteria. Vaccine 27: 2804-2811.
4. Crump JA, Luby SP, Mintz ED, (2004) The global burden of typhoid fever. Bull World Health Organ 82: 346-353.
5. DeRoeck D, Jodar L, Clemens J, (2007) Putting typhoid vaccination on the global health agenda. N Engl J Med 357: 1069-1071.
6. Sagi SS, Paliwal P, Bansal A, Mishra C, Khan N, et al. (2006) Studies on immunogenicity and protective efficacy of DnaJ of Salmonella Typhi against lethal infection by Salmonella Typhimurium in mice. Vaccine 24: 7135-7141.
7. Cheminay C, Hensel M, (2008) Rational design of Salmonella recombinant vaccines. Int J Med Microbiol 298: 87-98.
8. Keitel WA, Bond NL, Zahradnik JM, Cramton TA, Robbins JB, (1994) Clinical and serological responses following primary and booster immunization with Salmonella typhi Vi capsular polysaccharide vaccines. Vaccine 12: 195-199.
9. Germanier R, Fuer E, (1975) Isolation and characterization of Gal E mutant Ty 21a of Salmonella typhi: a candidate strain for a live, oral typhoid vaccine. J Infect Dis 131: 553-558.
10. Ivanoff B, Levine MM, Lambert PH, (1994) Vaccination against typhoid fever: present status. Bull World Health Organ 72: 957-971.
11. Khan SA, Stratford R, Wu T, McKelvie N, Bellaby T, et al. (2003) Salmonella typhi and S Typhimurium derivatives harbouring deletions in aromatic biosynthesis and Salmonella Pathogenicity Island-2 (SPI-2) genes as vaccines and vectors. Vaccine 21: 538-548.
12. Kirkpatrick BD, McKenzie R, O'Neill JP, Larsson CJ, Bourgeois AL, et al. (2006) Evaluation of Salmonella enterica serovar Typhi (Ty2 aroC-ssaV-) M01ZH09, with a defined mutation in the Salmonella pathogenicity island 2, as a live, oral typhoid vaccine in human volunteers. Vaccine 24: 116-123.
13. Hoiseth SK, Stocker BA, (1981) Aromatic-dependent Salmonella Typhimurium are non-virulent and effective as live vaccines. Nature 291: 238-239.
14. Tacket CO, Sztein MB, Losonsky GA, Wasserman SS, Nataro JP, et al. (1997) Safety of live oral Salmonella typhi vaccine strains with deletions in htrA and aroC aroD and immune response in humans. Infect Immun 65: 452-456.
15. Galan JE, Curtiss R 3rd, (1989) Virulence and vaccine potential of phoP mutants of Salmonella Typhimurium. Microb Pathog 6: 433-443.
16. Coynault C, Robbe-Saule V, Norel F, (1996) Virulence and vaccine potential of Salmonella Typhimurium mutants deficient in the expression of the RpoS (sigma S) regulon. Mol Microbiol 22: 149-160.
17. Nagy G, Dobrindt U, Hacker J, Emody L, (2004) Oral immunization with an rfaH mutant elicits protection against salmonellosis in mice. Infect Immun 72: 4297-4301.
18. Garcia-Del Portillo F, Pucciarelli MG, Casadesus J, (1999) DNA adenine methylase mutants of Salmonella Typhimurium show defects in protein secretion, cell invasion, and M cell cytotoxicity. Proc Natl Acad Sci U S A 96: 11578-11583.
19. Heithoff DM, Sinsheimer RL, Low DA, Mahan MJ, (1999) An essential role for DNA adenine methylation in bacterial virulence. Science 284: 967-970.
20. Dueger EL, House JK, Heithoff DM, Mahan MJ, (2001) Salmonella DNA adenine methylase mutants elicit protective immune responses to homologous and heterologous serovars in chickens. Infect Immun 69: 7950-7954.
21. Peters SE, Paterson GK, Bandularatne ES, Northen HC, Pleasance S, et al. (2009) Salmonella enterica serovar Typhimurium trxA mutants are protective against virulent challenge and induce less inflammation than the live-attenuated vaccine strain SL3261. Infect Immun 78: 326-336.
22. Northen H, Paterson GK, Constantino-Casas F, Bryant CE, Clare S, et al. (2009) Salmonella enterica serovar Typhimurium mutants completely lacking the F(0)F(1) ATPase are novel live attenuated vaccine strains. Vaccine 28: 940-949.
23. Franze de Fernandez MT, Eoyang L, August JT, (1968) Factor fraction required for the synthesis of bacteriophage Qbeta-RNA. Nature 219: 588-590.
24. Tsui HC, Leung HC, Winkler ME, (1994) Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12. Mol Microbiol 13: 35-49.
25. Brown L, Elliott T, (1996) Efficient translation of the RpoS sigma factor in Salmonella Typhimurium requires host factor I, an RNA-binding protein encoded by the hfq gene. J Bacteriol 178: 3763-3770.
26. Muffler A, Fischer D, Hengge-Aronis R, (1996) The RNA-binding protein HF-I, known as a host factor for phage Qbeta RNA replication, is essential for rpoS translation in Escherichia coli. Genes Dev 10: 1143-1151.
27. Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, et al. (2008) Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet 4: e1000163.
28. Sittka A, Pfeiffer V, Tedin K, Vogel J, (2007) The RNA chaperone Hfq is essential for the virulence of Salmonella Typhimurium. Mol Microbiol 63: 193-217.
29. Wilson JW, Ott CM, Honer zu Bentrup K, Ramamurthy R, Quick L, et al. (2007) Space flight alters bacterial gene expression and virulence and reveals a role for global regulator Hfq. Proc Natl Acad Sci U S A 104: 16299-16304.
30. 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.
31. Garcia-del Portillo F, (2001) Salmonella intracellular proliferation: where, when and how? Microbes Infect 3: 1305-1311.
32. Pejcic-Karapetrovic B, Gurnani K, Russell MS, Finlay BB, Sad S, et al. (2007) Pregnancy impairs the innate immune resistance to Salmonella Typhimurium leading to rapid fatal infection. J Immunol 179: 6088-6096.
33. Cagiola M, Severi G, Forti K, Menichelli M, Papa P, et al. (2007) Abortion due to Salmonella enterica serovar Abortusovis (S. Abortusovis) in ewes is associated to a lack of production of IFN-gamma and can be prevented by immunization with inactivated S. Abortusovis vaccine. Vet Microbiol 121: 330-337.
34. Krishnan L, Guilbert LJ, Russell AS, Wegmann TG, Mosmann TR, et al. (1996) Pregnancy impairs resistance of C57BL/6 mice to Leishmania major infection and causes decreased antigen-specific IFN-gamma response and increased production of T helper 2 cytokines. J Immunol 156: 644-652.
35. Negi VD, Nagarajan AG, Chakravortty D, (2010) A Safe Vaccine (DV-STM-07) against Salmonella Infection Prevents Abortion and Confers Protective Immunity to the Pregnant and New Born Mice. PLoS One 5: e9139.
36. Karem KL, Kanangat S, Rouse BT, (1996) Cytokine expression in the gut associated lymphoid tissue after oral administration of attenuated Salmonella vaccine strains. Vaccine 14: 1495-1502.
37. Mittrucker HW, Kaufmann SH, (2000) Immune response to infection with Salmonella Typhimurium in mice. J Leukoc Biol 67: 457-463.
38. Viret JF, Favre D, Wegmuller B, Herzog C, Que JU, et al. (1999) Mucosal and systemic immune responses in humans after primary and booster immunizations with orally administered invasive and noninvasive live attenuated bacteria. Infect Immun 67: 3680-3685.
39. Hopkins SA, Niedergang F, Corthesy-Theulaz IE, Kraehenbuhl JP, (2000) A recombinant Salmonella Typhimurium vaccine strain is taken up and survives within murine Peyer's patch dendritic cells. Cell Microbiol 2: 59-68.
40. Cheminay C, Mohlenbrink A, Hensel M, (2005) Intracellular Salmonella inhibit antigen presentation by dendritic cells. J Immunol 174: 2892-2899.
41. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, et al. (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18: 767-811.
42. Chao Y, Vogel J, (2010) The role of Hfq in bacterial pathogens. Curr Opin Microbiol.
43. Ansong C, Yoon H, Porwollik S, Mottaz-Brewer H, Petritis BO, et al. (2009) Global systems-level analysis of Hfq and SmpB deletion mutants in Salmonella: implications for virulence and global protein translation. PLoS One 4: e4809.
44. Moon K, Gottesman S, (2009) A PhoQ/P-regulated small RNA regulates sensitivity of Escherichia coli to antimicrobial peptides. Mol Microbiol 74: 1314-1330.
45. Angelakopoulos H, Hohmann EL, (2000) Pilot study of phoP/phoQ-deleted Salmonella enterica serovar Typhimurium expressing Helicobacter pylori urease in adult volunteers. Infect Immun 68: 2135-2141.
46. Hindle Z, Chatfield SN, Phillimore J, Bentley M, Johnson J, et al. (2002) Characterization of Salmonella enterica derivatives harboring defined aroC and Salmonella pathogenicity island 2 type III secretion system (ssaV) mutations by immunization of healthy volunteers. Infect Immun 70: 3457-3467.
47. Kotton CN, Lankowski AJ, Scott N, Sisul D, Chen LM, et al. (2006) Safety and immunogenicity of attenuated Salmonella enterica serovar Typhimurium delivering an HIV-1 Gag antigen via the Salmonella Type III secretion system. Vaccine 24: 6216-6224.
48. Abd El Ghany M, Jansen A, Clare S, Hall L, Pickard D, et al. (2007) Candidate live, attenuated Salmonella enterica serotype Typhimurium vaccines with reduced fecal shedding are immunogenic and effective oral vaccines. Infect Immun 75: 1835-1842.
49. Nauciel C, (1990) Role of CD4+ T cells and T-independent mechanisms in acquired resistance to Salmonella Typhimurium infection. J Immunol 145: 1265-1269.
50. Mastroeni P, Villarreal-Ramos B, Hormaeche CE, (1992) Role of T cells, TNF alpha and IFN gamma in recall of immunity to oral challenge with virulent Salmonellae in mice vaccinated with live attenuated aro- Salmonella vaccines. Microb Pathog 13: 477-491.
51. Srinivasan A, Nanton M, Griffin A, McSorley SJ, (2009) Culling of activated CD4 T cells during typhoid is driven by Salmonella virulence genes. J Immunol 182: 7838-7845.
52. Luu RA, Gurnani K, Dudani R, Kammara R, van Faassen H, et al. (2006) Delayed expansion and contraction of CD8+ T cell response during infection with virulent Salmonella Typhimurium. J Immunol 177: 1516-1525.
53. Matsui H, Suzuki M, Isshiki Y, Kodama C, Eguchi M, et al. (2003) Oral immunization with ATP-dependent protease-deficient mutants protects mice against subsequent oral challenge with virulent Salmonella enterica serovar Typhimurium. Infect Immun 71: 30-39.
54. Eckmann L, Fierer J, Kagnoff MF, (1996) Genetically resistant (Ityr) and susceptible (Itys) congenic mouse strains show similar cytokine responses following infection with Salmonella dublin. J Immunol 156: 2894-2900.
55. Mizuno Y, Takada H, Nomura A, Jin CH, Hattori H, et al. (2003) Th1 and Th1-inducing cytokines in Salmonella infection. Clin Exp Immunol 131: 111-117.
56. 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: 4509-4514.
57. O'Brien AD, Scher I, Metcalf ES, (1981) Genetically conferred defect in anti-Salmonella antibody formation renders CBA/N mice innately susceptible to Salmonella Typhimurium infection. J Immunol 126: 1368-1372.
58. Secundino I, Lopez-Macias C, Cervantes-Barragan L, Gil-Cruz C, Rios-Sarabia N, et al. (2006) Salmonella porins induce a sustained, lifelong specific bactericidal antibody memory response. Immunology 117: 59-70.
59. Singh SP, Williams YU, Benjamin WH, Klebba PE, Boyd D, (1996) Immunoprotection by monoclonal antibodies to the porins and lipopolysaccharide of Salmonella Typhimurium. Microb Pathog 21: 249-263.
60. Gil-Cruz C, Bobat S, Marshall JL, Kingsley RA, Ross EA, et al. (2009) The porin OmpD from nontyphoidal Salmonella is a key target for a protective B1b cell antibody response. Proc Natl Acad Sci U S A 106: 9803-9808.
61. Michetti P, Mahan MJ, Slauch JM, Mekalanos JJ, Neutra MR, (1992) Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella Typhimurium. Infect Immun 60: 1786-1792.
62. Kulesus RR, Diaz-Perez K, Slechta ES, Eto DS, Mulvey MA, (2008) Impact of the RNA chaperone Hfq on the fitness and virulence potential of uropathogenic Escherichia coli. Infect Immun 76: 3019-3026.
63. Karasova D, Sebkova A, Vrbas V, Havlickova H, Sisak F, et al. (2009) Comparative analysis of Salmonella enterica serovar Enteritidis mutants with a vaccine potential. Vaccine 27: 5265-5270.
64. Hamid N, Jain SK, (2008) Characterization of an outer membrane protein of Salmonella enterica serovar Typhimurium that confers protection against typhoid. Clin Vaccine Immunol 15: 1461-1471.