Salmonella vaccines: Lessons from the mouse model or bad teaching?

Current Opinion in Microbiology

Volumn 17, Issue 1, 2014, Pages 99-105

  Strugnell, Richard A ^a   Scott, Timothy A ^a   Wang, Nancy ^a   Yang, Chenying ^a   Peres, Newton ^a   Bedoui, Sammy ^a   Kupz, Andreas ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SALMONELLOSIS VACCINE;

ADAPTIVE IMMUNITY; BACTERIAL LOAD; CELLULAR IMMUNITY; GASTROENTERITIS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNIZATION; INNATE IMMUNITY; INVASIVE NON TYPHOIDAL SALMONELLOSIS; MOUSE MODEL; NONHUMAN; PARATYPHOID FEVER; PATHOGENESIS; REVIEW; SALMONELLA ENTERICA; SALMONELLA ENTERITIDIS; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; TH17 CELL; TYPHOID FEVER;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; MICE; SALMONELLA INFECTIONS; SALMONELLA VACCINES;

EID: 84892511768     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2013.12.004     Document Type: Review

References (59)

1. Crump J.A., Luby S.P., Mintz E.D. The global burden of typhoid fever. Bull World Health Organ 2004, 82:346-353.
2. Holt K.E., Dutta S., Manna B., Bhattacharya S.K., Bhaduri B., Pickard D.J., Ochiai R.L., Ali M., Clemens J.D., Dougan G. High-resolution genotyping of the endemic Salmonella Typhi population during a Vi (typhoid) vaccination trial in Kolkata. PLoS Negl Trop Dis 2012, 6:e1490.
3. Stoesser N., Moore C.E., Pocock J.M., An K.P., Emary K., Carter M., Sona S., Poda S., Day N., Kumar V., et al. Pediatric bloodstream infections in Cambodia, 2007 to 2011. Pediatr Infect Dis J 2013, 32:e272-e276.
4. Majowicz S.E., Musto J., Scallan E., Angulo F.J., Kirk M., O'Brien S.J., Jones T.F., Fazil A., Hoekstra R.M. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 2010, 50:882-889.
5. Gordon M.A. Invasive nontyphoidal Salmonella disease: epidemiology, pathogenesis and diagnosis. Curr Opin Infect Dis 2011, 24:484-489.
6. Reddy E.A., Shaw A.V., Crump J.A. Community-acquired bloodstream infections in Africa: a systematic review and meta-analysis. Lancet Infect Dis 2010, 10:417-432.
7. Zhang Y., Bi P., Hiller J.E. Projected burden of disease for Salmonella infection due to increased temperature in Australian temperate and subtropical regions. Environ Int 2012, 44:26-30.
8. Gordon M.A., Banda H.T., Gondwe M., Gordon S.B., Boeree M.J., Walsh A.L., Corkill J.E., Hart C.A., Gilks C.F., Molyneux M.E. Non-typhoidal Salmonella bacteraemia among HIV-infected Malawian adults: high mortality and frequent recrudescence. AIDS 2002, 16:1633-1641.
9. Okoro C.K., Kingsley R.A., Connor T.R., Harris S.R., Parry C.M., Al-Mashhadani M.N., Kariuki S., Msefula C.L., Gordon M.A., de Pinna E., et al. Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat Genet 2012, 44:1215-1221.
10. Gordon M.A., Graham S.M., Walsh A.L., Wilson L., Phiri A., Molyneux E., Zijlstra E.E., Heyderman R.S., Hart C.A., Molyneux M.E. Epidemics of invasive Salmonella enterica serovar enteritidis and S. enterica serovar typhimurium infection associated with multidrug resistance among adults and children in Malawi. Clin Infect Dis 2008, 46:963-969.
11. Morpeth S.C., Ramadhani H.O., Crump J.A. Invasive non-Typhi Salmonella disease in Africa. Clin Infect Dis 2009, 49:606-611.
12. Crump J.A., Mintz E.D. Global trends in typhoid and paratyphoid fever. Clin Infect Dis 2010, 50:241-246.
13. Hoffmann S., Batz M.B., Morris J.G. Annual cost of illness and quality-adjusted life year losses in the United States due to 14 foodborne pathogens. J Food Prot 2012, 75:1292-1302.
14. Chesson H.W., Ekwueme D.U., Saraiya M., Watson M., Lowy D.R., Markowitz L.E. Estimates of the annual direct medical costs of the prevention and treatment of disease associated with human papillomavirus in the United States. Vaccine 2012, 30:6016-6019.
15. Kupz A., Scott T.A., Belz G.T., Andrews D.M., Greyer M., Lew A.M., Brooks A.G., Smyth M.J., Curtiss R., Bedoui S., et al. Contribution of Thy1+ NK cells to protective IFN-gamma production during Salmonella typhimurium infections. Proc Natl Acad Sci U S A 2013, 110:2252-2257.
16. Nanton M.R., Way S.S., Shlomchik M.J., McSorley S.J. Cutting edge: B cells are essential for protective immunity against Salmonella independent of antibody secretion. J Immunol 2012, 189:5503-5507.
17. Kupz A., Guarda G., Gebhardt T., Sander L.E., Short K.R., Diavatopoulos D.A., Wijburg O.L., Cao H., Waithman J.C., Chen W., et al. NLRC4 inflammasomes in dendritic cells regulate noncognate effector function by memory CD8(+) T cells. Nat Immunol 2012, 13:162-169.
18. Jenkin C.R., Rowley D. Basis for immunity to typhoid in mice and the question of "cellular immunity". Bacteriol Rev 1963, 27:391-404.
19. MacLennan C.A., Gondwe E.N., Msefula C.L., Kingsley R.A., Thomson N.R., White S.A., Goodall M., Pickard D.J., Graham S.M., Dougan G., et al. The neglected role of antibody in protection against bacteremia caused by nontyphoidal strains of Salmonella in African children. J Clin Invest 2008, 118:1553-1562.
20. Gondwe E.N., Molyneux M.E., Goodall M., Graham S.M., Mastroeni P., Drayson M.T., MacLennan C.A. Importance of antibody and complement for oxidative burst and killing of invasive nontyphoidal Salmonella by blood cells in Africans. Proc Natl Acad Sci U S A 2010, 107:3070-3075.
21. MacLennan C.A., Gilchrist J.J., Gordon M.A., Cunningham A.F., Cobbold M., Goodall M., Kingsley R.A., van Oosterhout J.J., Msefula C.L., Mandala W.L., et al. Dysregulated humoral immunity to nontyphoidal Salmonella in HIV-infected African adults. Science 2010, 328:508-512.
22. Trebicka E., Jacob S., Pirzai W., Hurley B.P., Cherayil B.J. Role of antilipopolysaccharide antibodies in serum bactericidal activity against Salmonella enterica serovar Typhimurium in healthy adults and children in the United States. Clin Vaccine Immunol 2013, 20:1491-1498.
23. Levine M.M. Salmonella enterica Serovar Typhi (Typhoid) Vaccines 2011, vol 20. WHO, Geneva, Switzerland, WHO 2011 Module 20 http://whqlibdoc.who.int/publications/2011/9789241502610_eng.pdf.
24. Wahid R., Pasetti M.F., Maciel M., Simon J.K., Tacket C.O., Levine M.M., Sztein M.B. Oral priming with Salmonella Typhi vaccine strain CVD 909 followed by parenteral boost with the S. Typhi Vi capsular polysaccharide vaccine induces CD27+IgD-S. Typhi-specific IgA and IgG B memory cells in humans. Clin Immunol 2011, 138:187-200.
25. Godinez I., Raffatellu M., Chu H., Paixao T.A., Haneda T., Santos R.L., Bevins C.L., Tsolis R.M., Baumler A.J. Interleukin-23 orchestrates mucosal responses to Salmonella enterica serotype Typhimurium in the intestine. Infect Immun 2009, 77:387-398.
26. Santos R.L., Raffatellu M., Bevins C.L., Adams L.G., Tukel C., Tsolis R.M., Baumler A.J. Life in the inflamed intestine, Salmonella style. Trends Microbiol 2009, 17:498-506.
27. Godinez I., Keestra A.M., Spees A., Baumler A.J. The IL-23 axis in Salmonella gastroenteritis. Cell Microbiol 2011, 13:1639-1647.
28. Raffatellu M., Santos R.L., Chessa D., Wilson R.P., Winter S.E., Rossetti C.A., Lawhon S.D., Chu H., Lau T., Bevins C.L., et al. The capsule encoding the viaB locus reduces interleukin-17 expression and mucosal innate responses in the bovine intestinal mucosa during infection with Salmonella enterica serotype Typhi. Infect Immun 2007, 75:4342-4350.
29. Dandekar S., George M.D., Baumler A.J. Th17 cells, HIV and the gut mucosal barrier. Curr Opin HIV AIDS 2010, 5:173-178.
30. Raffatellu M., Santos R.L., Verhoeven D.E., George M.D., Wilson R.P., Winter S.E., Godinez I., Sankaran S., Paixao T.A., Gordon M.A., et al. Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat Med 2008, 14:421-428.
31. Sheikh S.Z., Matsuoka K., Kobayashi T., Li F., Rubinas T., Plevy S.E. Cutting edge: IFN-gamma is a negative regulator of IL-23 in murine macrophages and experimental colitis. J Immunol 2010, 184:4069-4073.
32. MacLennan C., Fieschi C., Lammas D.A., Picard C., Dorman S.E., Sanal O., MacLennan J.M., Holland S.M., Ottenhoff T.H., Casanova J.L., et al. Interleukin (IL)-12 and IL-23 are key cytokines for immunity against Salmonella in humans. J Infect Dis 2004, 190:1755-1757.
33. Xu D., Cisar J.O., Poly F., Yang J., Albanese J., Dharmasena M., Wai T., Guerry P., Kopecko D.J. Genome sequence of Salmonella enterica serovar Typhi oral vaccine strain Ty21a. Genome Announc 2013, 1.
34. Slayton R.B., Date K.A., Mintz E.D. Vaccination for typhoid fever in sub-Saharan Africa. Hum Vaccin Immunother 2013, 9:903-906.
35. Roland K.L., Brenneman K.E. Salmonella as a vaccine delivery vehicle. Expert Rev Vaccines 2013, 12:1033-1045.
36. Hoiseth S.K., Stocker B.A. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 1981, 291:238-239.
37. Frey S.E., Lottenbach K.R., Hill H., Blevins T.P., Yu Y., Zhang Y., Brenneman K.E., Kelly-Aehle S.M., McDonald C., Jansen A., et al. A Phase I, dose-escalation trial in adults of three recombinant attenuated Salmonella Typhi vaccine vectors producing Streptococcus pneumoniae surface protein antigen PspA. Vaccine 2013, 31:4874-4880.
38. Jones C., Lee C.K., Ahn C., Shin J., Knezevic I. Working group on quality, safety and efficacy of typhoid Vi capsular polysaccharide conjugate, vaccines, Jeju, Republic of Korea, 5-7 September 2012. Vaccine 2013, 31:4466-4469.
39. Simon R., Tennant S.M., Wang J.Y., Schmidlein P.J., Lees A., Ernst R.K., Pasetti M.F., Galen J.E., Levine M.M. Salmonella enterica serovar enteritidis core O polysaccharide conjugated to H:g,m flagellin as a candidate vaccine for protection against invasive infection with S. enteritidis. Infect Immun 2011, 79:4240-4249.
40. Simon R., Wang J.Y., Boyd M.A., Tulapurkar M.E., Ramachandran G., Tennant S.M., Pasetti M., Galen J.E., Levine M.M. Sustained protection in mice immunized with fractional doses of Salmonella enteritidis core and O polysaccharide-flagellin glycoconjugates. PLoS ONE 2013, 8:e64680.
41. Song J., Gao X., Galan J.E. Structure and function of the Salmonella Typhi chimaeric A(2)B(5) typhoid toxin. Nature 2013, 499:350-354.
42. Lee S.J., McLachlan J.B., Kurtz J.R., Fan D., Winter S.E., Baumler A.J., Jenkins M.K., McSorley S.J. Temporal expression of bacterial proteins instructs host CD4 T cell expansion and Th17 development. PLoS Pathog 2012, 8:e1002499.
43. Lee S.J., Liang L., Juarez S., Nanton M.R., Gondwe E.N., Msefula C.L., Kayala M.A., Necchi F., Heath J.N., Hart P., et al. Identification of a common immune signature in murine and human systemic Salmonellosis. Proc Natl Acad Sci U S A 2012, 109:4998-5003.
44. Jansen A.M., Hall L.J., Clare S., Goulding D., Holt K.E., Grant A.J., Mastroeni P., Dougan G., Kingsley R.A. A Salmonella Typhimurium-Typhi genomic chimera: a model to study Vi polysaccharide capsule function in vivo. PLoS Pathog 2011, 7:e1002131.
45. Baker S., Dougan G. The genome of Salmonella enterica serovar Typhi. Clin Infect Dis 2007, 45(Suppl 1):S29-S33.
46. Mian M.F., Pek E.A., Chenoweth M.J., Coombes B.K., Ashkar A.A. Humanized mice for Salmonella typhi infection: new tools for an old problem. Virulence 2011, 2:248-252.
47. Firoz Mian M., Pek E.A., Chenoweth M.J., Ashkar A.A. Humanized mice are susceptible to Salmonella typhi infection. Cell Mol Immunol 2011, 8:83-87.
48. Libby S.J., Brehm M.A., Greiner D.L., Shultz L.D., McClelland M., Smith K.D., Cookson B.T., Karlinsey J.E., Kinkel T.L., Porwollik S., et al. Humanized nonobese diabetic-scid IL2rgammanull mice are susceptible to lethal Salmonella Typhi infection. Proc Natl Acad Sci U S A 2010, 107:15589-15594.
49. Song J., Willinger T., Rongvaux A., Eynon E.E., Stevens S., Manz M.G., Flavell R.A., Galan J.E. A mouse model for the human pathogen Salmonella typhi. Cell Host Microbe 2010, 8:369-376.
50. Broz P., Ruby T., Belhocine K., Bouley D.M., Kayagaki N., Dixit V.M., Monack D.M. Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 2012, 490:288-291.
51. Mathur R., Oh H., Zhang D., Park S.G., Seo J., Koblansky A., Hayden M.S., Ghosh S. A mouse model of Salmonella typhi infection. Cell 2012, 151:590-602.
52. Fang F.C., Baumler A.J. A tollgate for typhoid. Cell 2012, 151:473-475.
53. Paterson J.C. Typhoid and the paratyphoids: a review. Postgrad Med J 1949, 25:413-420.
54. Simon R., Tennant S.M., Galen J.E., Levine M.M. Mouse models to assess the efficacy of non-typhoidal Salmonella vaccines: revisiting the role of host innate susceptibility and routes of challenge. Vaccine 2011, 29:5094-5106.
55. Tsolis R.M., Xavier M.N., Santos R.L., Baumler A.J. How to become a top model: impact of animal experimentation on human Salmonella disease research. Infect Immun 2011, 79:1806-1814.
56. Wattiau P., Boland C., Bertrand S. Methodologies for Salmonella enterica subsp. enterica subtyping: gold standards and alternatives. Appl Environ Microbiol 2011, 77:7877-7885.
57. Ochiai R.L., Acosta C.J., Danovaro-Holliday M.C., Baiqing D., Bhattacharya S.K., Agtini M.D., Bhutta Z.A., Canh do G., Ali M., Shin S., et al. A study of typhoid fever in five Asian countries: disease burden and implications for controls. Bull World Health Organ 2008, 86:260-268.
58. Kingsley R.A., Msefula C.L., Thomson N.R., Kariuki S., Holt K.E., Gordon M.A., Harris D., Clarke L., Whitehead S., Sangal V., et al. Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res 2009, 19:2279-2287.
59. Santos R.L., Zhang S., Tsolis R.M., Kingsley R.A., Adams L.G., Baumler A.J. Animal models of Salmonella infections: enteritis versus typhoid fever. Microbes Infect 2001, 3:1335-1344.