Pseudogenization of the Secreted Effector Gene sseI Confers Rapid Systemic Dissemination of S. Typhimurium ST313 within Migratory Dendritic Cells

Cell Host and Microbe

Volumn 21, Issue 2, 2017, Pages 182-194

  Carden, Sarah E ^a   Walker, Gregory T ^b   Honeycutt, Jared ^a   Lugo, Kyler ^a   Pham, Trung ^a   Jacobson, Amanda ^a   Bouley, Donna ^a   Idoyaga, Juliana ^a   Tsolis, Renee M ^b   Monack, Denise ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

evolution; genome degradation; iNTS; niche adaptation; nontyphoidal Salmonella; NTS; pathogenesis; pseudogene; SrfH; T3SS effectors

Indexed keywords

CD11B ANTIGEN; CCR7 PROTEIN, MOUSE; CHEMOKINE RECEPTOR CCR7;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; BACTERIAL STRAIN; CELL MIGRATION; CONTROLLED STUDY; DENDRITIC CELL; GASTROENTERITIS; GENE; GENE EXPRESSION; GENETIC DIFFERENCE; MESENTERY LYMPH NODE; MOUSE; MOUTH INFECTION; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SSEI GENE; ANIMAL; BACTEREMIA; BACTERIAL GENE; C57BL MOUSE; CELL MOTION; DISEASE MODEL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; KNOCKOUT MOUSE; LYMPH NODE; MALE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; SALMONELLOSIS;

ANIMALS; BACTEREMIA; CELL MOVEMENT; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FEMALE; GASTROENTERITIS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HOST-PATHOGEN INTERACTIONS; LYMPH NODES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, CCR7; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM;

EID: 85011931064     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2017.01.009     Document Type: Article

References (45)

1. Atif, S.M., Uematsu, S., Akira, S., McSorley, S.J., CD103-CD11b+ dendritic cells regulate the sensitivity of CD4 T-cell responses to bacterial flagellin. Mucosal Immunol. 7 (2014), 68–77.
2. Atif, S.M., Winter, S.E., Winter, M.G., McSorley, S.J., Bäumler, A.J., Salmonella enterica serovar Typhi impairs CD4 T cell responses by reducing antigen availability. Infect. Immun. 82 (2014), 2247–2254.
3. Barthel, M., Hapfelmeier, S., Quintanilla-Martínez, L., Kremer, M., Rohde, M., Hogardt, M., Pfeffer, K., Rüssmann, H., Hardt, W.D., Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 71 (2003), 2839–2858.
4. Bogunovic, M., Ginhoux, F., Helft, J., Shang, L., Hashimoto, D., Greter, M., Liu, K., Jakubzick, C., Ingersoll, M.A., Leboeuf, M., et al. Origin of the lamina propria dendritic cell network. Immunity 31 (2009), 513–525.
5. 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 490 (2012), 288–291.
6. Carden, S., Okoro, C., Dougan, G., Monack, D., Non-typhoidal Salmonella Typhimurium ST313 isolates that cause bacteremia in humans stimulate less inflammasome activation than ST19 isolates associated with gastroenteritis. Pathog. Dis., 73, 2015, ftu023.
7. Cerovic, V., Houston, S.A., Scott, C.L., Aumeunier, A., Yrlid, U., Mowat, A.M., Milling, S.W.F., Intestinal CD103(-) dendritic cells migrate in lymph and prime effector T cells. Mucosal Immunol. 6 (2013), 104–113.
8. Cheminay, C., Chakravortty, D., Hensel, M., Role of neutrophils in murine salmonellosis. Infect. Immun. 72 (2004), 468–477.
9. Coombes, J.L., Siddiqui, K.R.R., Arancibia-Cárcamo, C.V., Hall, J., Sun, C.-M., Belkaid, Y., Powrie, F., A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med. 204 (2007), 1757–1764.
10. Diehl, G.E., Longman, R.S., Zhang, J.X., Breart, B., Galan, C., Cuesta, A., Schwab, S.R., Littman, D.R., Microbiota restricts trafficking of bacteria to mesenteric lymph nodes by CX(3)CR1(hi) cells. Nature 494 (2013), 116–120.
11. Feasey, N.A., Dougan, G., Kingsley, R.A., Heyderman, R.S., Gordon, M.A., Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet 379 (2012), 2489–2499.
12. Feasey, N.A., Everett, D., Faragher, E.B., Roca-Feltrer, A., Kang'ombe, A., Denis, B., Kerac, M., Molyneux, E., Molyneux, M., Jahn, A., et al. Modelling the contributions of malaria, HIV, malnutrition and rainfall to the decline in paediatric invasive non-typhoidal Salmonella disease in Malawi. PLoS Negl. Trop. Dis., 9, 2015, e0003979.
13. Förster, R., Schubel, A., Breitfeld, D., Kremmer, E., Renner-Müller, I., Wolf, E., Lipp, M., CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99 (1999), 23–33.
14. Geem, D., Medina-Contreras, O., Kim, W., Huang, C.S., Denning, T.L., Isolation and characterization of dendritic cells and macrophages from the mouse intestine. J. Vis. Exp., 63, 2012, e4040.
15. Gordon, M.A., Invasive nontyphoidal Salmonella disease: epidemiology, pathogenesis and diagnosis. Curr. Opin. Infect. Dis. 24 (2011), 484–489.
16. 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. 46 (2008), 963–969.
17. Hoiseth, S.K., Stocker, B.A.D., Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291 (1981), 238–239.
18. Kariuki, S., Gordon, M.A., Feasey, N., Parry, C.M., Antimicrobial resistance and management of invasive Salmonella disease. Vaccine 33:Suppl 3 (2015), C21–C29.
19. 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. 19 (2009), 2279–2287.
20. Kingsley, R.A., Kay, S., Connor, T., Barquist, L., Sait, L., Holt, K.E., Sivaraman, K., Wileman, T., Goulding, D., Clare, S., et al. Genome and transcriptome adaptation accompanying emergence of the definitive type 2 host-restricted Salmonella enterica serovar Typhimurium pathovar. MBio, 4, 2013 e00565–e13.
21. Klemm, E., Dougan, G., Advances in understanding bacterial pathogenesis gained from whole-genomes and phylogenetics. Cell Host Microbe 19 (2016), 599–610.
22. Klemm, E.J., Gkrania-Klotsas, E., Hadfield, J., Forbester, J.L., Harris, S.R., Hale, C., Heath, J.N., Wileman, T., Clare, S., Kane, L., et al. Emergence of host-adapted Salmonella Enteritidis through rapid evolution in an immunocompromised host. Nat. Microbiol., 1, 2016, 15023.
23. Kurtz, J.R., Petersen, H.E., Frederick, D.R., Morici, L.A., McLachlan, J.B., Vaccination with a single CD4 T cell peptide epitope from a Salmonella type III-secreted effector protein provides protection against lethal infection. Infect. Immun. 82 (2014), 2424–2433.
24. Lokken, K.L., Mooney, J.P., Butler, B.P., Xavier, M.N., Chau, J.Y., Schaltenberg, N., Begum, R.H., Müller, W., Luckhart, S., Tsolis, R.M., Malaria parasite infection compromises control of concurrent systemic non-typhoidal Salmonella infection via IL-10-mediated alteration of myeloid cell function. PLoS Pathog., 10, 2014, e1004049.
25. McClelland, M., Sanderson, K.E., Clifton, S.W., Latreille, P., Porwollik, S., Sabo, A., Meyer, R., Bieri, T., Ozersky, P., McLellan, M., et al. Comparison of genome degradation in Paratyphi A and Typhi, human-restricted serovars of Salmonella enterica that cause typhoid. Nat. Genet. 36 (2004), 1268–1274.
26. McLaughlin, L.M., Govoni, G.R., Gerke, C., Gopinath, S., Peng, K., Laidlaw, G., Chien, Y.-H., Jeong, H.-W., Li, Z., Brown, M.D., et al. The Salmonella SPI2 effector SseI mediates long-term systemic infection by modulating host cell migration. PLoS Pathog., 5, 2009, e1000671.
27. McLaughlin, L.M., Xu, H., Carden, S.E., Fisher, S., Reyes, M., Heilshorn, S.C., Monack, D.M., A microfluidic-based genetic screen to identify microbial virulence factors that inhibit dendritic cell migration. Integr Biol (Camb) 6 (2014), 438–449.
28. Merad, M., Sathe, P., Helft, J., Miller, J., Mortha, A., The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu. Rev. Immunol. 31 (2013), 563–604.
29. Monack, D.M., Hersh, D., Ghori, N., Bouley, D., Zychlinsky, A., Falkow, S., Salmonella exploits caspase-1 to colonize Peyer's patches in a murine typhoid model. J. Exp. Med. 192 (2000), 249–258.
30. Mooney, J.P., Butler, B.P., Lokken, K.L., Xavier, M.N., Chau, J.Y., Schaltenberg, N., Dandekar, S., George, M.D., Santos, R.L., Luckhart, S., Tsolis, R.M., The mucosal inflammatory response to non-typhoidal Salmonella in the intestine is blunted by IL-10 during concurrent malaria parasite infection. Mucosal Immunol. 7 (2014), 1302–1311.
31. Mooney, J.P., Lokken, K.L., Byndloss, M.X., George, M.D., Velazquez, E.M., Faber, F., Butler, B.P., Walker, G.T., Ali, M.M., Potts, R., et al. Inflammation-associated alterations to the intestinal microbiota reduce colonization resistance against non-typhoidal Salmonella during concurrent malaria parasite infection. Sci. Rep., 5, 2015, 14603.
32. Nuccio, S.P., Bäumler, A.J., Comparative analysis of Salmonella genomes identifies a metabolic network for escalating growth in the inflamed gut. MBio, 5, 2014 e00929–e14.
33. 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. 44 (2012), 1215–1221.
34. Okoro, C.K., Barquist, L., Connor, T.R., Harris, S.R., Clare, S., Stevens, M.P., Arends, M.J., Hale, C., Kane, L., Pickard, D.J., et al. Signatures of adaptation in human invasive Salmonella Typhimurium ST313 populations from sub-Saharan Africa. PLoS Negl. Trop. Dis., 9, 2015, e0003611.
35. Parsons, B.N., Humphrey, S., Salisbury, A.M., Mikoleit, J., Hinton, J.C.D., Gordon, M.A., Wigley, P., Invasive non-typhoidal Salmonella typhimurium ST313 are not host-restricted and have an invasive phenotype in experimentally infected chickens. PLoS Negl. Trop. Dis., 7, 2013, e2487.
36. Porwollik, S., Boyd, E.F., Choy, C., Cheng, P., Florea, L., Proctor, E., McClelland, M., Characterization of Salmonella enterica subspecies I genovars by use of microarrays. J. Bacteriol. 186 (2004), 5883–5898.
37. Raffatellu, M., Santos, R.L., Verhoeven, D.E., George, M.D., Wilson, R.P., Winter, S.E., Godinez, I., Sankaran, S., Paixão, T.A., Gordon, M.A., et al. Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat. Med. 14 (2008), 421–428.
38. Roux, C.M., Butler, B.P., Chau, J.Y., Paixao, T.A., Cheung, K.W., Santos, R.L., Luckhart, S., Tsolis, R.M., Both hemolytic anemia and malaria parasite-specific factors increase susceptibility to Nontyphoidal Salmonella enterica serovar typhimurium infection in mice. Infect. Immun. 78 (2010), 1520–1527.
39. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 (2012), 676–682.
40. Scott, C.L., Bain, C.C., Wright, P.B., Sichien, D., Kotarsky, K., Persson, E.K., Luda, K., Guilliams, M., Lambrecht, B.N., Agace, W.W., et al. CCR2(+)CD103(-) intestinal dendritic cells develop from DC-committed precursors and induce interleukin-17 production by T cells. Mucosal Immunol. 8 (2015), 327–339.
41. Singletary, L.A., Karlinsey, J.E., Libby, S.J., Mooney, J.P., Lokken, K.L., Tsolis, R.M., Byndloss, M.X., Hirao, L.A., Gaulke, C.A., Crawford, R.W., et al. Loss of multicellular behavior in epidemic African nontyphoidal Salmonella enterica Serovar Typhimurium ST313 strain D23580. MBio, 7, 2016 e02265–e15.
42. van der Velden, A.W.M., Velasquez, M., Starnbach, M.N., Salmonella rapidly kill dendritic cells via a caspase-1-dependent mechanism. J. Immunol. 171 (2003), 6742–6749.
43. Vazquez-Torres, A., Jones-Carson, J., Bäumler, A.J., Falkow, S., Valdivia, R., Brown, W., Le, M., Berggren, R., Parks, W.T., Fang, F.C., Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 401 (1999), 804–808.
44. Watson, K.G., Holden, D.W., Dynamics of growth and dissemination of Salmonella in vivo. Cell. Microbiol. 12 (2010), 1389–1397.
45. Yang, J., Barrila, J., Roland, K.L., Kilbourne, J., Ott, C.M., Forsyth, R.J., Nickerson, C.A., Characterization of the invasive, multidrug resistant non-typhoidal Salmonella strain D23580 in a murine model of infection. PLoS Negl. Trop. Dis., 9, 2015, e0003839.