Molecular Mechanisms of Salmonella Effector Proteins: A Comprehensive Review

References

• Khosravani M, Dallal MMS, Norouzi M. marA efflux pump gene expression in Salmonella enteritidis strains treated with Artemisia tournefortiana hydroalcoholic extract and comparison with commercial efflux pump inhibitor, carbonyl cyanide 3-chlorophenylhydrazone (CCCP). Arch Med Lab Sci. 2019;4:1.
   Google Scholar
• Soltan Dallal M, Khalilian M, Masoumi Asl H, et al. Molecular epidemiology and antimicrobial resistance of Salmonella spp. Isolated from resident patients in Mazandaran Province, Northern Iran. J Food Qual Hazards Control. 2016;3(4):146–151.
   Google Scholar
• Sayadnouri S, Dallal MS, Akbarzadeh S, Fard RMN. Evaluation of class 1 and 2 integrons and antibiotic resistance pattern in Salmonella enterica isolated from diarrheal food-borne outbreaks in Iran. J Food Qual Hazards Control. 2019. doi:10.18502/jfqhc.6.3.1384
   Google Scholar
• Nasser A. Prevalence of sulfonamide resistance genes in Salmonella spp. isolated from Milad hospital of Tehran. Iran J Public Health. 2014;43(2):87.
   Google Scholar
• Crump JA, Mintz ED. Global trends in typhoid and paratyphoid fever. Clin Infect Dis. 2010;50(2):241–246. doi:10.1086/64954120014951
   PubMed Web of Science ®Google Scholar
• Rivera-Chavez F, Baumler AJ. The pyromaniac inside you: Salmonella metabolism in the host gut. Annu Rev Microbiol. 2015;69:31–48. doi:10.1146/annurev-micro-091014-10410826002180
   PubMed Web of Science ®Google Scholar
• Kaur J, Jain SK. Role of antigens and virulence factors of Salmonella enterica serovar Typhi in its pathogenesis. Microbiol Res. 2012;167(4):199–210. doi:10.1016/j.micres.2011.08.00121945101
   PubMed Web of Science ®Google Scholar
• Fardsanei F, Dallal MMS, Douraghi M, et al. Antimicrobial resistance, virulence genes and genetic relatedness of Salmonella enterica serotype Enteritidis isolates recovered from human gastroenteritis in Tehran, Iran. J Global Antimicrob Resist. 2018;12:220–226. doi:10.1016/j.jgar.2017.10.005
   PubMed Web of Science ®Google Scholar
• Figueira R, Holden DW. Functions of the Salmonella pathogenicity island 2 (SPI-2) type III secretion system effectors. Microbiology. 2012;158(5):1147–1161. doi:10.1099/mic.0.058115-022422755
   PubMed Web of Science ®Google Scholar
• Galan JE. Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol. 2001;17:53–86. doi:10.1146/annurev.cellbio.17.1.5311687484
   PubMed Web of Science ®Google Scholar
• Rescigno M, Urbano M, Valzasina B, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol. 2001;2(4):361. doi:10.1038/8637311276208
   PubMed Web of Science ®Google Scholar
• Kiss T, Morgan E, Nagy G. Contribution of SPI-4 genes to the virulence of Salmonella enterica. FEMS Microbiol Lett. 2007;275(1):153–159. doi:10.1111/fml.2007.275.issue-117711458
   PubMed Web of Science ®Google Scholar
• Wagner C, Polke M, Gerlach RG, et al. Functional dissection of SiiE, a giant non-fimbrial adhesin of Salmonella enterica. Cell Microbiol. 2011;13(8):1286–1301. doi:10.1111/cmi.2011.13.issue-821729227
   PubMed Web of Science ®Google Scholar
• Gerlach RG, Claudio N, Rohde M, Jackel D, Wagner C, Hensel M. Cooperation of Salmonella pathogenicity islands 1 and 4 is required to breach epithelial barriers. Cell Microbiol. 2008;10(11):2364–2376. doi:10.1111/j.1462-5822.2008.01218.x18671822
   PubMed Web of Science ®Google Scholar
• Main-Hester KL, Colpitts KM, Thomas GA, Fang FC, Libby SJ. Coordinate regulation of Salmonella pathogenicity island 1 (SPI1) and SPI4 in Salmonella enterica serovar Typhimurium. Infect Immun. 2008;76(3):1024–1035. doi:10.1128/IAI.01224-0718160484
   PubMed Web of Science ®Google Scholar
• Wagner C, Polke M, Gerlach RG, et al. Functional dissection of SiiE, a giant non-fimbrial adhesin of Salmonella enterica. Cell Microbiol. 2011;13(8):1286–1301. doi:10.1111/j.1462-5822.2011.01621.x21729227
   PubMed Web of Science ®Google Scholar
• Latasa C, Roux A, Toledo-Arana A, et al. BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol Microbiol. 2005;58(5):1322–1339. doi:10.1111/j.1365-2958.2005.04907.x16313619
   PubMed Web of Science ®Google Scholar
• Romling U, Rohde M, Olsen A, Normark S, Reinkoster J. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol. 2000;36(1):10–23. doi:10.1046/j.1365-2958.2000.01822.x10760159
   PubMed Web of Science ®Google Scholar
• González JF, Tucker L, Fitch J, Wetzel A, White P, Gunn JS. Human bile-mediated regulation of Salmonella curli fimbriae. J Bacteriol. 2019;JB.00055–00019.
   Web of Science ®Google Scholar
• Rosselin M, Virlogeux-Payant I, Roy C, et al. Rck of Salmonella enterica, subspecies enterica serovar Enteritidis, mediates Zipper-like internalization. Cell Res. 2010;20(6):647. doi:10.1038/cr.2010.4520368731
   PubMed Web of Science ®Google Scholar
• Heffernan EJ, Reed S, Hackett J, Fierer J, Roudier C, Guiney D. Mechanism of resistance to complement-mediated killing of bacteria encoded by the Salmonella typhimurium virulence plasmid gene rck. J Clin Invest. 1992;90(3):953–964. doi:10.1172/JCI1159721522243
   PubMed Web of Science ®Google Scholar
• Wiedemann A, Mijouin L, Ayoub MA, et al. Identification of the epidermal growth factor receptor as the receptor for Salmonella Rck-dependent invasion. FASEB J. 2016;30(12):4180–4191. doi:10.1096/fj.201600701R27609774
   PubMed Web of Science ®Google Scholar
• Wiedemann A, Rosselin M, Mijouin L, Bottreau E, Velge P. Involvement of c-Src tyrosine kinase upstream of class I phosphatidylinositol (PI) 3-kinases in Salmonella Enteritidis Rck protein-mediated invasion. J Biol Chem. 2012;287(37):31148–31154. doi:10.1074/jbc.M112.39213422810232
   PubMed Web of Science ®Google Scholar
• Lambert MA, Smith SG. The PagN protein of Salmonella enterica serovar Typhimurium is an adhesin and invasin. BMC Microbiol. 2008;8(1):142. doi:10.1186/1471-2180-8-14218778463
   PubMed Web of Science ®Google Scholar
• Lambert MA, Smith SG. The PagN protein mediates invasion via interaction with proteoglycan. FEMS Microbiol Lett. 2009;297(2):209–216. doi:10.1111/j.1574-6968.2009.01666.x19552707
   PubMed Web of Science ®Google Scholar
• Lambert MA, Smith SGJ. The PagN protein mediates invasion via interaction with proteoglycan. FEMS Microbiol Lett. 2009;297(2):209–216. doi:10.1111/j.1574-6968.2009.01666.x19552707
   PubMed Web of Science ®Google Scholar
• Prost LR, Miller SI. The Salmonellae PhoQ sensor: mechanisms of detection of phagosome signals. Cell Microbiol. 2008;10(3):576–582. doi:10.1111/cmi.2008.10.issue-318182085
   PubMed Web of Science ®Google Scholar
• Chowdhury R, Das S, Ta A, Das S. Epithelial invasion by Salmonella Typhi using STIV–met interaction. Cell Microbiol. 2019;21(3):e12982.30426648
   PubMed Web of Science ®Google Scholar
• Chowdhury R, Mandal RS, Ta A, Das S. An AIL family protein promotes type three secretion system-1-independent invasion and pathogenesis of Salmonella enterica serovar Typhi. Cell Microbiol. 2015;17(4):486–503. doi:10.1111/cmi.2015.17.issue-425308535
   PubMed Web of Science ®Google Scholar
• Dorsey CW, Laarakker MC, Humphries AD, Weening EH, Bäumler AJ. Salmonella enterica serotype Typhimurium MisL is an intestinal colonization factor that binds fibronectin. Mol Microbiol. 2005;57(1):196–211. doi:10.1111/j.1365-2958.2005.04666.x15948960
   PubMed Web of Science ®Google Scholar
• Kingsley RA, Santos RL, Keestra AM, Adams LG, Bäumler AJ. Salmonella enterica serotype Typhimurium ShdA is an outer membrane fibronectin-binding protein that is expressed in the intestine. Mol Microbiol. 2002;43(4):895–905. doi:10.1046/j.1365-2958.2002.02805.x11929540
   PubMed Web of Science ®Google Scholar
• Cooley MB, Miller WG, Mandrell RE. Colonization of Arabidopsis thaliana with Salmonella enterica and enterohemorrhagic Escherichia coli O157: h7and competition by Enterobacter asburiae. Appl Environ Microbiol. 2003;69(8):4915–4926. doi:10.1128/AEM.69.8.4915-4926.200312902287
   PubMed Web of Science ®Google Scholar
• Tan MSF, White AP, Rahman S, Dykes GA. Role of fimbriae, flagella and cellulose on the attachment of Salmonella typhimurium ATCC 14028 to plant cell wall models. PLoS One. 2016;11(6):e0158311. doi:10.1371/journal.pone.015831127355584
   PubMed Web of Science ®Google Scholar
• Hara-Kaonga B, Pistole TG. OmpD but not OmpC is involved in adherence of Salmonella enterica serovar Typhimurium to human cells. Can J Microbiol. 2004;50(9):719–727. doi:10.1139/w04-05615644926
   PubMed Web of Science ®Google Scholar
• Schmidt H, Hensel M. Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev. 2004;17(1):14–56. doi:10.1128/CMR.17.1.14-56.200414726454
   PubMed Web of Science ®Google Scholar
• Ilyas B, Tsai CN, Coombes BK. Evolution of Salmonella-host cell interactions through a dynamic bacterial genome. Front Cell Infect Microbiol. 2017;7:428. doi:10.3389/fcimb.2017.0042829034217
   PubMed Web of Science ®Google Scholar
• Wallis TS, Galyov EE. Molecular basis of Salmonella‐induced enteritis: microReview. Mol Microbiol. 2000;36(5):997–1005. doi:10.1046/j.1365-2958.2000.01892.x10844685
   PubMed Web of Science ®Google Scholar
• Jantsch J, Chikkaballi D, Hensel M. Cellular aspects of immunity to intracellular Salmonella enterica. Immunol Rev. 2011;240(1):185–195. doi:10.1111/imr.2011.240.issue-121349094
   PubMed Web of Science ®Google Scholar
• Mason D, Mallo GV, Terebiznik MR, et al. Alteration of epithelial structure and function associated with PtdIns (4, 5) P2 degradation by a bacterial phosphatase. J Gen Physiol. 2007;129(4):267–283. doi:10.1085/jgp.20060965617389247
   PubMed Web of Science ®Google Scholar
• Knodler LA, Finlay BB, Steele-Mortimer O. The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt. J Biol Chem. 2005;280(10):9058–9064. doi:10.1074/jbc.M41258820015642738
   PubMed Web of Science ®Google Scholar
• Garcia-Gil A, Galan-Enriquez CS, Perez-Lopez A, Nava P, Alpuche-Aranda C, Ortiz-Navarrete V. SopB activates the Akt-YAP pathway to promote Salmonella survival within B cells. Virulence. 2018;9(1):1390–1402. doi:10.1080/21505594.2018.150966430103648
   PubMed Web of Science ®Google Scholar
• Kum WWS, Lo BC, Yu HB, Finlay BB. Protective role of Akt2 in Salmonella enterica serovar typhimurium-induced gastroenterocolitis. Infect Immun. 2011;79(7):2554. doi:10.1128/IAI.01235-1021555401
   PubMed Web of Science ®Google Scholar
• Bakowski MA, Braun V, Lam GY, et al. The phosphoinositide phosphatase SopB manipulates membrane surface charge and trafficking of the Salmonella-containing vacuole. Cell Host Microbe. 2010;7(6):453–462. doi:10.1016/j.chom.2010.05.01120542249
   PubMed Web of Science ®Google Scholar
• Truong D, Boddy KC, Canadien V, et al. Salmonella exploits host Rho GTPase signalling pathways through the phosphatase activity of SopB. Cell Microbiol. 2018;20(10):e12938. doi:10.1111/cmi.v20.1030010242
   PubMed Web of Science ®Google Scholar
• Hernandez LD, Hueffer K, Wenk MR, Galán JE. Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science. 2004;304(5678):1805. doi:10.1126/science.109818815205533
   PubMed Web of Science ®Google Scholar
• Mallo GV, Espina M, Smith AC, et al. SopB promotes phosphatidylinositol 3-phosphate formation on Salmonella vacuoles by recruiting Rab5 and Vps34. J Cell Biol. 2008;182(4):741–752. doi:10.1083/jcb.20080413118725540
   PubMed Web of Science ®Google Scholar
• Sana TG, Flaugnatti N, Lugo KA, et al. Salmonella Typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut. Proc National Acad Sci. 2016;113(34):E5044–E5051. doi:10.1073/pnas.1608858113
   PubMed Web of Science ®Google Scholar
• Kaur J, Jain S. Role of antigens and virulence factors of Salmonella enterica serovar Typhi in its pathogenesis. Microbiol Res. 2012;167(4):199–210. doi:10.1016/j.micres.2011.08.00121945101
   PubMed Web of Science ®Google Scholar
• Hart PJ, O’Shaughnessy CM, Siggins MK, et al. Differential killing of Salmonella enterica serovar typhi by antibodies targeting Vi and lipopolysaccharide o:9 antigen. PLoS One. 2016;11(1):e0145945. doi:10.1371/journal.pone.014594526741681
   PubMed Web of Science ®Google Scholar
• Reid RR, Prodeus AP, Khan W, Hsu T, Rosen FS, Carroll MC. Endotoxin shock in antibody-deficient mice: unraveling the role of natural antibody and complement in the clearance of lipopolysaccharide. J Immunol. 1997;159(2):970–975.9218618
   PubMed Web of Science ®Google Scholar
• Pickard D, Wain J, Baker S, et al. Composition, acquisition, and distribution of the Vi exopolysaccharide-encoding Salmonella enterica pathogenicity island SPI-7. J Bacteriol. 2003;185(17):5055–5065. doi:10.1128/JB.185.17.5055-5065.200312923078
   PubMed Web of Science ®Google Scholar
• Seth-Smith HMB, Fookes MC, Okoro CK, et al. Structure, diversity, and mobility of the pathogenicity island 7 family of integrative and conjugative elements within enterobacteriaceae. J Bacteriol. 2012;194(6):1494.22247511
   PubMed Web of Science ®Google Scholar
• Zhang X-L, Tsui ISM, Yip CMC, et al. Salmonella enterica serovar typhi uses type IVB pili to enter human intestinal epithelial cells. Infect Immun. 2000;68(6):3067. doi:10.1128/IAI.68.6.3067-3073.200010816445
   PubMed Web of Science ®Google Scholar
• Winter SE, Winter MG, Thiennimitr P, et al. The TviA auxiliary protein renders the Salmonella enterica serotype Typhi RcsB regulon responsive to changes in osmolarity. Mol Microbiol. 2009;74(1):175–193. doi:10.1111/mmi.2009.74.issue-119703107
   PubMed Web of Science ®Google Scholar
• Bajaj V, Hwang C, Lee CA. hilA is a novel ompR/toxR family member that activates the expression of Salmonella typhimurium invasion genes. Mol Microbiol. 1995;18(4):715–727. doi:10.1111/mmi.1995.18.issue-48817493
   PubMed Web of Science ®Google Scholar
• Hiyoshi H, Wangdi T, Lock G, et al. Mechanisms to Evade the Phagocyte Respiratory Burst Arose by Convergent Evolution in Typhoidal Salmonella Serovars. Cell Rep. 2018;22(7):1787–1797. doi:10.1016/j.celrep.2018.01.01629444431
   PubMed Web of Science ®Google Scholar
• Sharma A, Qadri A. Vi polysaccharide of Salmonella typhi targets the prohibitin family of molecules in intestinal epithelial cells and suppresses early inflammatory responses. Proc Natl Acad Sci U S A. 2004;101(50):17492–17497. doi:10.1073/pnas.040753610115576509
   PubMed Web of Science ®Google Scholar
• Raffatellu M, Chessa D, Wilson RP, Dusold R, Rubino S, Bäumler AJ. The Vi capsular antigen of salmonella enterica serotype typhi reduces toll-like receptor-dependent interleukin-8 expression in the intestinal mucosa. Infect Immun. 2005;73(6):3367. doi:10.1128/IAI.73.6.3367-3374.200515908363
   PubMed Web of Science ®Google Scholar
• Hirose K, Ezaki T, Miyake M, et al. Survival of Vi-capsulated and Vi-deleted Salmonella typhi strains in cultured macrophage expressing different levels of CD14 antigen. FEMS Microbiol Lett. 1997;147(2):259–265. doi:10.1111/j.1574-6968.1997.tb10251.x9119202
   PubMed Web of Science ®Google Scholar
• Kong Q, Yang J, Liu Q, Alamuri P, Roland KL, Curtiss R. Effect of deletion of genes involved in lipopolysaccharide core and O-antigen synthesis on virulence and immunogenicity of Salmonella enterica serovar Typhimurium. Infect Immun. 2011;79(10):4227. doi:10.1128/IAI.00040-1121768282
   PubMed Web of Science ®Google Scholar
• Nevola JJ, Laux DC, Cohen PS. In vivo colonization of the mouse large intestine and in vitro penetration of intestinal mucus by an avirulent smooth strain of Salmonella typhimurium and its lipopolysaccharide-deficient mutant. Infect Immun. 1987;55(12):2884–2890.3316026
   PubMed Web of Science ®Google Scholar
• Raetz CR, Whitfield C. Lipopolysaccharide endotoxins. Annu Rev Biochem. 2002;71(1):635–700. doi:10.1146/annurev.biochem.71.110601.13541412045108
   PubMed Web of Science ®Google Scholar
• Murray GL, Attridge SR, Morona R. Altering the length of the lipopolysaccharide O antigen has an impact on the interaction of Salmonella enterica serovar Typhimurium with macrophages and complement. J Bacteriol. 2006;188(7):2735–2739. doi:10.1128/JB.188.7.2735-2739.200616547065
   PubMed Web of Science ®Google Scholar
• Vaara M. Antibiotic-supersusceptible mutants of Escherichia coli and Salmonella typhimurium. Antimicrob Agents Chemother. 1993;37(11):2255. doi:10.1128/AAC.37.11.22558285603
   PubMed Web of Science ®Google Scholar
• Pawlak A, Rybka J, Dudek B, et al. Salmonella O48 serum resistance is connected with the elongation of the lipopolysaccharide O-antigen containing sialic acid. Int J Mol Sci. 2017;18:10. doi:10.3390/ijms18102022
   Web of Science ®Google Scholar
• Delgado MA, Mouslim C, Groisman EA. The PmrA/PmrB and RcsC/YojN/RcsB systems control expression of the Salmonella O‐antigen chain length determinant. Mol Microbiol. 2006;60(1):39–50. doi:10.1111/mmi.2006.60.issue-116556219
   PubMed Web of Science ®Google Scholar
• McCONNELL M, Wright A. Variation in the structure and bacteriophage-inactivating capacity of Salmonella anatum lipopolysaccharide as a function of growth temperature. J Bacteriol. 1979;137(2):746–751.422511
   PubMed Web of Science ®Google Scholar
• McClelland M, Sanderson KE, Clifton SW, et al. Comparison of genome degradation in Paratyphi A and Typhi, human-restricted serovars of Salmonella enterica that cause typhoid. Nat Genet. 2004;36(12):1268. doi:10.1038/ng147015531882
   PubMed Web of Science ®Google Scholar
• Verma N, Reeves P. Identification and sequence of rfbS and rfbE, which determine antigenic specificity of group A and group D salmonellae. J Bacteriol. 1989;171(10):5694. doi:10.1128/jb.171.10.5694-5701.19892793833
   PubMed Web of Science ®Google Scholar
• Vázquez-Torres A. Less is best in the convergent evolution of typhoidal Salmonella. Cell Host Microbe. 2018;23(2):151–153. doi:10.1016/j.chom.2018.01.00929447692
   PubMed Web of Science ®Google Scholar
• Knodler LA, Steele-Mortimer O. Taking possession: biogenesis of the Salmonella-containing vacuole. Traffic. 2003;4(9):587–599. doi:10.1034/j.1600-0854.2003.00118.x12911813
   PubMed Web of Science ®Google Scholar
• Stebbins CE, Galan JE. Modulation of host signaling by a bacterial mimic: structure of the Salmonella effector SptP bound to Rac1. Mol Cell. 2000;6(6):1449–1460. doi:10.1016/S1097-2765(00)00141-611163217
   PubMed Web of Science ®Google Scholar
• Bonifacino JS, Glick BS. The mechanisms of vesicle budding and fusion. Cell. 2004;116(2):153–166. doi:10.1016/S0092-8674(03)01079-114744428
   PubMed Web of Science ®Google Scholar
• Semerdjieva S, Shortt B, Maxwell E, et al. Coordinated regulation of AP2 uncoating from clathrin-coated vesicles by rab5 and hRME-6. J Cell Biol. 2008;183(3):499–511. doi:10.1083/jcb.20080601618981233
   PubMed Web of Science ®Google Scholar
• Steele-Mortimer O, Meresse S, Gorvel JP, Toh BH, Finlay BB. Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell Microbiol. 1999;1(1):33–49. doi:10.1046/j.1462-5822.1999.00003.x11207539
   PubMed Web of Science ®Google Scholar
• Martinez-Lorenzo MJ, Meresse S, de Chastellier C, Gorvel JP. Unusual intracellular trafficking of Salmonella typhimurium in human melanoma cells. Cell Microbiol. 2001;3(6):407–416. doi:10.1046/j.1462-5822.2001.00123.x11422083
   PubMed Web of Science ®Google Scholar
• Cai H, Reinisch K, Ferro-Novick S. Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev Cell. 2007;12(5):671–682. doi:10.1016/j.devcel.2007.04.00517488620
   PubMed Web of Science ®Google Scholar
• Scott CC, Cuellar-Mata P, Matsuo T, Davidson HW, Grinstein S. Role of 3-phosphoinositides in the maturation of Salmonella-containing vacuoles within host cells. J Biol Chem. 2002;277(15):12770–12776. doi:10.1074/jbc.M11039920011821391
   PubMed Web of Science ®Google Scholar
• Sindhwani A, Arya SB, Kaur H, Jagga D, Tuli A, Sharma M. Salmonella exploits the host endolysosomal tethering factor HOPS complex to promote its intravacuolar replication. PLoS Pathog. 2017;13(10):e1006700.29084291
   PubMed Web of Science ®Google Scholar
• Mills IG, Jones AT, Clague MJ. Involvement of the endosomal autoantigen EEA1 in homotypic fusion of early endosomes. Curr Biol. 1998;8(15):881–884. doi:10.1016/S0960-9822(07)00351-X9705936
   PubMed Web of Science ®Google Scholar
• Méresse S, Steele‐Mortimer O, Finlay BB, Gorvel JP. The rab7 GTPase controls the maturation of Salmonella typhimurium‐containing vacuoles in HeLa cells. EMBO J. 1999;18(16):4394–4403. doi:10.1093/emboj/18.16.439410449405
   PubMed Web of Science ®Google Scholar
• Kaniuk NA, Canadien V, Bagshaw RD, et al. Salmonella exploits Arl8B‐directed kinesin activity to promote endosome tubulation and cell‐to‐cell transfer. Cell Microbiol. 2011;13(11):1812–1823.21824248
   PubMed Web of Science ®Google Scholar
• Harrison RE, Brumell JH, Khandani A, et al. Salmonella impairs RILP recruitment to Rab7 during maturation of invasion vacuoles. Mol Biol Cell. 2004;15(7):3146–3154. doi:10.1091/mbc.e04-02-009215121880
   PubMed Web of Science ®Google Scholar
• Bujny MV, Ewels PA, Humphrey S, Attar N, Jepson MA, Cullen PJ. Sorting nexin-1 defines an early phase of Salmonella-containing vacuole-remodeling during Salmonella infection. J Cell Sci. 2008;121(12):2027–2036.18505799
   PubMed Web of Science ®Google Scholar
• McGourty K, Thurston TL, Matthews SA, Pinaud L, Mota LJ, Holden DW. Salmonella inhibits retrograde trafficking of mannose-6-phosphate receptors and lysosome function. Science. 2012;338(6109):963–967. doi:10.1126/science.122703723162002
   PubMed Web of Science ®Google Scholar
• Carlton J, Bujny M, Peter BJ, et al. Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high- curvature membranes and 3-phosphoinositides. Curr Biol. 2004;14(20):1791–1800. doi:10.1016/j.cub.2004.09.07715498486
   PubMed Web of Science ®Google Scholar
• Chakraborty S, Mizusaki H, Kenney LJ. A FRET-based DNA biosensor tracks OmpR-dependent acidification of Salmonella during macrophage infection. PLoS Biol. 2015;13(4):e1002116. doi:10.1371/journal.pbio.100211625875623
   PubMed Web of Science ®Google Scholar
• Krieger V, Liebl D, Zhang Y, et al. Reorganization of the endosomal system in Salmonella-infected cells: the ultrastructure of Salmonella-induced tubular compartments. PLoS Pathog. 2014;10(9):e1004374. doi:10.1371/journal.ppat.100437425254663
   PubMed Web of Science ®Google Scholar
• Hannemann S, Gao B, Galán JE. Salmonella modulation of host cell gene expression promotes its intracellular growth. PLoS Pathog. 2013;9(10):e1003668. doi:10.1371/journal.ppat.100366824098123
   PubMed Web of Science ®Google Scholar
• Tuli A, Sharma M. How to do business with lysosomes: Salmonella leads the way. Curr Opin Microbiol. 2019;47:1–7. doi:10.1016/j.mib.2018.10.00330391777
   PubMed Web of Science ®Google Scholar
• Drecktrah D, Levine‐Wilkinson S, Dam T, et al. Dynamic behavior of Salmonella‐induced membrane tubules in epithelial cells. Traffic. 2008;9(12):2117–2129. doi:10.1111/j.1600-0854.2008.00830.x18785994
   PubMed Web of Science ®Google Scholar
• Perrett CA, Zhou D. Salmonella type III effector SopB modulates host cell exocytosis. Emerging Microbes Infect. 2013;2(1):1–6. doi:10.1038/emi.2013.37
   PubMed Web of Science ®Google Scholar
• Santos JC, Enninga J. At the crossroads: communication of bacteria-containing vacuoles with host organelles. Cell Microbiol. 2016;18(3):330–339. doi:10.1111/cmi.v18.326762760
   PubMed Web of Science ®Google Scholar
• Santos JC, Duchateau M, Fredlund J, et al. The COPII complex and lysosomal VAMP7 determine intracellular Salmonella localization and growth. Cell Microbiol. 2015;17(12):1699–1720. doi:10.1111/cmi.1247526084942
   PubMed Web of Science ®Google Scholar
• D’Costa VM, Braun V, Landekic M, et al. Salmonella disrupts host endocytic trafficking by SopD2-mediated inhibition of Rab7. Cell Rep. 2015;12(9):1508–1518. doi:10.1016/j.celrep.2015.07.06326299973
   PubMed Web of Science ®Google Scholar
• McEwan DG, Richter B, Claudi B, et al. PLEKHM1 regulates Salmonella-containing vacuole biogenesis and infection. Cell Host Microbe. 2015;17(1):58–71. doi:10.1016/j.chom.2014.11.01125500191
   PubMed Web of Science ®Google Scholar
• Zhang Y, Higashide WM, McCormick BA, Chen J, Zhou D. The inflammation-associated Salmonella SopA is a HECT-like E3 ubiquitin ligase. Mol Microbiol. 2006;62(3):786–793. doi:10.1111/mmi.2006.62.issue-317076670
   PubMed Web of Science ®Google Scholar
• McGhie EJ, Brawn LC, Hume PJ, Humphreys D, Koronakis V. Salmonella takes control: effector-driven manipulation of the host. Curr Opin Microbiol. 2009;12(1):117–124. doi:10.1016/j.mib.2008.12.00119157959
   PubMed Web of Science ®Google Scholar
• Kolodziejek AM, Altura MA, Fan J, et al. Salmonella translocated effectors recruit OSBP1 to the phagosome to promote vacuolar membrane integrity. Cell Rep 2019;27:2147–2156. doi:10.2139/ssrn.318841531091452
   PubMed Web of Science ®Google Scholar
• Abrahams GL, Muller P, Hensel M. Functional dissection of SseF, a type III effector protein involved in positioning the salmonella-containing vacuole. Traffic. 2006;7(8):950–965. doi:10.1111/j.1600-0854.2006.00454.x16800847
   PubMed Web of Science ®Google Scholar
• Yu XJ, Liu M, Holden DW. Salmonella effectors SseF and SseG interact with mammalian protein ACBD3 (GCP60) to anchor salmonella-containing vacuoles at the golgi network. MBio. 2016;7:4. doi:10.1128/mBio.00474-16
   Web of Science ®Google Scholar
• Mesquita FS, Thomas M, Sachse M, Santos AJ, Figueira R, Holden DW. The Salmonella deubiquitinase SseL inhibits selective autophagy of cytosolic aggregates. PLoS Pathog. 2012;8(6):e1002743. doi:10.1371/journal.ppat.100274322719249
   PubMed Web of Science ®Google Scholar
• Domingues L, Ismail A, Charro N, et al. The Salmonella effector SteA binds phosphatidylinositol 4-phosphate for subcellular targeting within host cells. Cell Microbiol. 2016;18(7):949–969. doi:10.1111/cmi.1255826676327
   PubMed Web of Science ®Google Scholar
• Bayer-Santos E, Durkin CH, Rigano LA, et al. The Salmonella effector SteD mediates MARCH8-dependent ubiquitination of MHC II molecules and inhibits T cell activation. Cell Host Microbe. 2016;20(5):584–595. doi:10.1016/j.chom.2016.10.00727832589
   PubMed Web of Science ®Google Scholar
• Odendall C, Rolhion N, Forster A, et al. The Salmonella kinase SteC targets the MAP kinase MEK to regulate the host actin cytoskeleton. Cell Host Microbe. 2012;12(5):657–668. doi:10.1016/j.chom.2012.09.01123159055
   PubMed Web of Science ®Google Scholar
• Freeman JA, Rappl C, Kuhle V, Hensel M, Miller SI. SpiC is required for translocation of Salmonella pathogenicity island 2 effectors and secretion of translocon proteins SseB and SseC. J Bacteriol. 2002;184(18):4971–4980. doi:10.1128/JB.184.18.4971-4980.200212193612
   PubMed Web of Science ®Google Scholar
• Bakowski MA, Braun V, Brumell JH. Salmonella-containing vacuoles: directing traffic and nesting to grow. Traffic. 2008;9(12):2022–2031. doi:10.1111/tra.2008.9.issue-1218778407
   PubMed Web of Science ®Google Scholar
• Jackson LK, Nawabi P, Hentea C, Roark EA, Haldar K. The Salmonella virulence protein SifA is a G protein antagonist. Proc National Acad Sci. 2008;105(37):14141–14146. doi:10.1073/pnas.0801872105
   PubMed Web of Science ®Google Scholar
• Brawn LC, Hayward RD, Koronakis V. Salmonella SPI1 effector SipA persists after entry and cooperates with a SPI2 effector to regulate phagosome maturation and intracellular replication. Cell Host Microbe. 2007;1(1):63–75. doi:10.1016/j.chom.2007.02.00118005682
   PubMed Web of Science ®Google Scholar
• Freeman JA, Ohl ME, Miller SI. The Salmonella enterica serovar typhimurium translocated effectors SseJ and SifB are targeted to the Salmonella-containing vacuole. Infect Immun. 2003;71(1):418–427. doi:10.1128/IAI.71.1.418-427.200312496192
   PubMed Web of Science ®Google Scholar
• Núñez-Hernández C, Alonso A, Pucciarelli MG, Casadesús J, García-del Portillo F. Dormant intracellular Salmonella enterica serovar Typhimurium discriminates among Salmonella pathogenicity island 2 effectors to persist inside fibroblasts. Infect Immun. 2014;82(1):221–232. doi:10.1128/IAI.01304-1324144726
   PubMed Web of Science ®Google Scholar
• Abrahams GL, Hensel M. Manipulating cellular transport and immune responses: dynamic interactions between intracellular Salmonella enterica and its host cells. Cell Microbiol. 2006;8(5):728–737. doi:10.1111/cmi.2006.8.issue-516611223
   PubMed Web of Science ®Google Scholar
• Henry T, Couillault C, Rockenfeller P, et al. The Salmonella effector protein PipB2 is a linker for kinesin-1. Proc National Acad Sci. 2006;103(36):13497–13502. doi:10.1073/pnas.0605443103
   PubMed Web of Science ®Google Scholar
• Knodler LA, Celli J, Hardt W-D, Vallance BA, Yip C, Finlay BB. Salmonella effectors within a single pathogenicity island are differentially expressed and translocated by separate type III secretion systems. Mol Microbiol. 2002;43(5):1089–1103. doi:10.1046/j.1365-2958.2002.02820.x11918798
   PubMed Web of Science ®Google Scholar
• Miao EA, Mao DP, Yudkovsky N, et al. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci U S A. 2010;107(7):3076–3080. doi:10.1073/pnas.091308710720133635
   PubMed Web of Science ®Google Scholar
• Reyes Ruiz VM, Ramirez J, Naseer N, et al. Broad detection of bacterial type III secretion system and flagellin proteins by the human NAIP/NLRC4 inflammasome. Proc Natl Acad Sci U S A. 2017;114(50):13242–13247. doi:10.1073/pnas.171043311429180436
   PubMed Web of Science ®Google Scholar
• Karki R, Lee E, Place D, et al. IRF8 regulates transcription of naips for NLRC4 inflammasome activation. Cell. 2018;173(4):920–933.e913. doi:10.1016/j.cell.2018.02.05529576451
   PubMed Web of Science ®Google Scholar
• Cummings LA, Barrett SLR, Wilkerson WD, Fellnerova I, Cookson BT. FliC-specific CD4+ T cell responses are restricted by bacterial regulation of antigen expression. J Immunol. 2005;174(12):7929–7938. doi:10.4049/jimmunol.174.12.792915944299
   PubMed Web of Science ®Google Scholar
• Miao EA, Leaf IA, Treuting PM, et al. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol. 2010;11:1136. doi:10.1038/ni.196021057511
   PubMed Web of Science ®Google Scholar
• Humphries F, Yang S, Wang B, Moynagh P. RIP kinases: key decision makers in cell death and innate immunity. Cell Death Differ. 2015;22(2):225. doi:10.1038/cdd.2014.12625146926
   PubMed Web of Science ®Google Scholar
• Behnsen J, Perez-Lopez A, Nuccio S-P, Raffatellu M. Exploiting host immunity: the Salmonella paradigm. Trends Immunol. 2015;36(2):112–120. doi:10.1016/j.it.2014.12.00325582038
   PubMed Web of Science ®Google Scholar
• McCoy MW, Moreland SM, Detweiler CS. Hemophagocytic macrophages in murine typhoid fever have an anti-inflammatory phenotype. Infect Immun. 2012;80(10):3642–3649. doi:10.1128/IAI.00656-1222868497
   PubMed Web of Science ®Google Scholar
• Libby SJ, Lesnick M, Hasegawa P, Weidenhammer E, Guiney DG. The Salmonella virulence plasmid spv genes are required for cytopathology in human monocyte-derived macrophages. Cell Microbiol. 2000;2(1):49–58. doi:10.1046/j.1462-5822.2000.00030.x11207562
   PubMed Web of Science ®Google Scholar
• Browne SH, Lesnick ML, Guiney DG. Genetic requirements for salmonella-induced cytopathology in human monocyte-derived macrophages. Infect Immun. 2002;70(12):7126–7135. doi:10.1128/IAI.70.12.7126-7135.200212438395
   PubMed Web of Science ®Google Scholar
• Haneda T, Ishii Y, Shimizu H, et al. Salmonella type III effector SpvC, a phosphothreonine lyase, contributes to reduction in inflammatory response during intestinal phase of infection. Cell Microbiol. 2012;14(4):485–499. doi:10.1111/j.1462-5822.2011.01733.x22188134
   PubMed Web of Science ®Google Scholar
• Mazurkiewicz P, Thomas J, Thompson JA, et al. SpvC is a Salmonella effector with phosphothreonine lyase activity on host mitogen-activated protein kinases. Mol Microbiol. 2008;67(6):1371–1383. doi:10.1111/mmi.2008.67.issue-618284579
   PubMed Web of Science ®Google Scholar
• Singh Y, Saxena A, Kumar R, Saxena MK. Virulence system of salmonella with special reference to Salmonella enterica. Salmonella. 2018;41.
   Google Scholar
• Kim Y-G, Kim J-H, Kim K-J. Crystal structure of the Salmonella enterica serovar typhimurium virulence factor SrfJ, a glycoside hydrolase family enzyme. J Bacteriol. 2009;191(21):6550–6554. doi:10.1128/JB.00641-0919717598
   PubMed Web of Science ®Google Scholar
• Bishop AL, Hall A. Rho GTPases and their effector proteins. Biochem J. 2000;348(Pt 2):241–255. doi:10.1042/bj348024110816416
   PubMed Web of Science ®Google Scholar
• Friebel A, Ilchmann H, Aepfelbacher M, Ehrbar K, Machleidt W, Hardt W-D. SopE and SopE2 from Salmonella typhimurium activate different sets of RhoGTPases of the host cell. J Biol Chem. 2001;276(36):34035–34040. doi:10.1074/jbc.M10060920011440999
   PubMed Web of Science ®Google Scholar
• Hardt WD, Chen LM, Schuebel KE, Bustelo XR, Galan JE. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell. 1998;93(5):815–826. doi:10.1016/S0092-8674(00)81442-79630225
   PubMed Web of Science ®Google Scholar
• Keestra AM, Winter MG, Auburger JJ, et al. Manipulation of small Rho GTPases is a pathogen-induced process detected by NOD1. Nature. 2013;496(7444):233. doi:10.1038/nature1202523542589
   PubMed Web of Science ®Google Scholar
• Johnson R, Byrne A, Berger CN, et al. The type III secretion system effector SptP of Salmonella enterica serovar Typhi. J Bacteriol. 2017;199(4):e00647–e00616. doi:10.1128/JB.00647-1627920299
   PubMed Web of Science ®Google Scholar
• Pearson G, Robinson F, Beers Gibson T, et al. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev. 2001;22(2):153–183. doi:10.1210/edrv.22.2.042811294822
   PubMed Web of Science ®Google Scholar
• Lin SL, Le TX, Cowen DS. SptP, a Salmonella typhimurium type III-secreted protein, inhibits the mitogen-activated protein kinase pathway by inhibiting Raf activation. Cell Microbiol. 2003;5(4):267–275. doi:10.1046/j.1462-5822.2003.t01-1-00274.x12675684
   PubMed Web of Science ®Google Scholar
• Arricau N, Hermant D, Waxin H, Popoff M. Molecular characterization of the Salmonella typhi StpA protein that is related to both Yersinia YopE cytotoxin and YopH tyrosine phosphatase. Res Microbiol. 1997;148(1):21–26. doi:10.1016/S0923-2508(97)81896-79404501
   PubMed Web of Science ®Google Scholar
• Sabbagh SC, Forest CG, Lepage C, Leclerc J-M, Daigle F. So similar, yet so different: uncovering distinctive features in the genomes of Salmonella enterica serovars Typhimurium and Typhi. FEMS Microbiol Lett. 2010;305(1):1–13. doi:10.1111/fml.2010.305.issue-120146749
   PubMed Web of Science ®Google Scholar
• McIntosh A, Meikle LM, Ormsby MJ, et al. SipA activation of caspase-3 is a decisive mediator of host cell survival at early stages of Salmonella enterica serovar Typhimurium infection. Infect Immun. 2017;85(9):e00393–e00317. doi:10.1128/IAI.00393-1728630067
   PubMed Web of Science ®Google Scholar
• Singh PK, Kapoor A, Lomash RM, et al. Salmonella SipA mimics a cognate SNARE for host Syntaxin8 to promote fusion with early endosomes. J Cell Biol. 2018;217(12):4199. doi:10.1083/jcb.20180215530309979
   PubMed Web of Science ®Google Scholar
• Xu J, Luo F, Zhang Z, et al. SNARE proteins synaptobrevin, SNAP-25, and syntaxin are involved in rapid and slow endocytosis at synapses. Cell Rep. 2013;3(5):1414–1421. doi:10.1016/j.celrep.2013.03.01023643538
   PubMed Web of Science ®Google Scholar
• Hallstrom KN, McCormick BA. The type three secreted effector SipC regulates the trafficking of PERP during Salmonella infection. Gut Microbes. 2016;7(2):136–145. doi:10.1080/19490976.2015.112862627078059
   PubMed Web of Science ®Google Scholar
• Hallstrom KN, Srikanth C, Agbor TA, et al. PERP, a host tetraspanning membrane protein, is required for S almonella‐induced inflammation. Cell Microbiol. 2015;17(6):843–859. doi:10.1111/cmi.2015.17.issue-625486861
   PubMed Web of Science ®Google Scholar
• Lara-Tejero M, Galán JE. Salmonella enterica serovar typhimurium pathogenicity island 1-encoded type III secretion system translocases mediate intimate attachment to nonphagocytic cells. Infect Immun. 2009;77(7):2635–2642. doi:10.1128/IAI.00077-0919364837
   PubMed Web of Science ®Google Scholar
• Eswarappa SM, Janice J, Nagarajan AG, et al. Differentially evolved genes of Salmonella pathogenicity islands: insights into the mechanism of host specificity in Salmonella. PLoS One. 2008;3(12):e3829. doi:10.1371/journal.pone.000382919050757
   PubMed Web of Science ®Google Scholar
• Shivcharan S, Yadav J, Qadri A. Host lipid sensing promotes invasion of cells with pathogenic Salmonella. Sci Rep. 2018;8(1):15501. doi:10.1038/s41598-018-33319-930341337
   PubMed Web of Science ®Google Scholar
• Knodler LA, Nair V, Steele-Mortimer O. Quantitative assessment of cytosolic Salmonella in epithelial cells. PLoS One. 2014;9(1):e84681. doi:10.1371/journal.pone.008468124400108
   PubMed Web of Science ®Google Scholar
• Jones RM, Wu H, Wentworth C, Luo L, Collier-Hyams L, Neish AS. Salmonella AvrA coordinates suppression of host immune and apoptotic defenses via JNK pathway blockade. Cell Host Microbe. 2008;3(4):233–244. doi:10.1016/j.chom.2008.02.01618407067
   PubMed Web of Science ®Google Scholar
• Fedor Y, Vignard J, Nicolau-Travers ML, et al. From single-strand breaks to double-strand breaks during S-phase: a new mode of action of the Escherichia coli cytolethal distending toxin. Cell Microbiol. 2013;15(1):1–15. doi:10.1111/cmi.1202822978660
   PubMed Web of Science ®Google Scholar
• Guidi R, Guerra L, Levi L, et al. Chronic exposure to the cytolethal distending toxins of Gram-negative bacteria promotes genomic instability and altered DNA damage response. Cell Microbiol. 2013;15(1):98–113. doi:10.1111/cmi.1203422998585
   PubMed Web of Science ®Google Scholar
• Del Bel Belluz L, Guidi R, Pateras IS, et al. The typhoid toxin promotes host survival and the establishment of a persistent asymptomatic infection. PLoS Pathog. 2016;12(4):e1005528–e1005528. doi:10.1371/journal.ppat.100552827055274
   PubMed Web of Science ®Google Scholar
• Chong A, Lee S, Yang Y-A, Song J. The role of typhoid toxin in Salmonella typhi virulence. Yale J Biol Med. 2017;90(2):283–290.28656014
   PubMed Web of Science ®Google Scholar
• Haghjoo E, Galan JE. Salmonella typhi encodes a functional cytolethal distending toxin that is delivered into host cells by a bacterial-internalization pathway. Proc Natl Acad Sci U S A. 2004;101(13):4614–4619. doi:10.1073/pnas.040093210115070766
   PubMed Web of Science ®Google Scholar
• Spanò S, Ugalde JE, Galán JE. Delivery of a Salmonella Typhi exotoxin from a host intracellular compartment. Cell Host Microbe. 2008;3(1):30–38.18191792
   PubMed Web of Science ®Google Scholar
• Eichelberg K, Galán JE. Differential regulation of Salmonella typhimurium type III secreted proteins by pathogenicity island 1 (SPI-1)-encoded transcriptional activators InvF and HilA. Infect Immun. 1999;67(8):4099.10417179
   PubMed Web of Science ®Google Scholar
• Ellermeier JR, Slauch JM. Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr Opin Microbiol. 2007;10(1):24–29. doi:10.1016/j.mib.2006.12.00217208038
   PubMed Web of Science ®Google Scholar
• Olekhnovich IN, Kadner RJ. Crucial roles of both flanking sequences in silencing of the hilA promoter in Salmonella enterica. J Mol Biol. 2006;357(2):373–386. doi:10.1016/j.jmb.2006.01.00716443238
   PubMed Web of Science ®Google Scholar
• Fabrega A, Vila J. Salmonella enterica serovar Typhimurium skills to succeed in the host: virulence and regulation. Clin Microbiol Rev. 2013;26(2):308–341.23554419
   PubMed Web of Science ®Google Scholar
• Ellermeier CD, Ellermeier JR, Slauch JM. HilD, HilC and RtsA constitute a feed forward loop that controls expression of the SPI1 type three secretion system regulator hilA in Salmonella enterica serovar Typhimurium. Mol Microbiol. 2005;57(3):691–705. doi:10.1111/mmi.2005.57.issue-316045614
   PubMed Web of Science ®Google Scholar
• Kenney LJ. The role of acid stress in Salmonella pathogenesis. Curr Opin Microbiol. 2019;47:45–51. doi:10.1016/j.mib.2018.11.00630529007
   PubMed Web of Science ®Google Scholar
• Cheeseman G, Fuller R. Changes in the pH activity profile of the lysine decarboxylase during incubation of Escherichia coli. J Appl Bacteriol. 1968;31(2):253–258. doi:10.1111/jam.1968.31.issue-24882105
   PubMedGoogle Scholar
• Crawford RW, Rosales-Reyes R, de la Luz Ramírez-aguilar M, Chapa-Azuela O, Alpuche-Aranda C, Gunn JS. Gallstones play a significant role in Salmonella spp. gallbladder colonization and carriage. Proc National Acad Sci. 2010;107(9):4353–4358. doi:10.1073/pnas.1000862107
   PubMed Web of Science ®Google Scholar
• Quinn HJ, Cameron AD, Dorman CJ. Bacterial regulon evolution: distinct responses and roles for the identical OmpR proteins of Salmonella Typhimurium and Escherichia coli in the acid stress response. PLoS Genet. 2014;10(3):e1004215. doi:10.1371/journal.pgen.100421524603618
   PubMed Web of Science ®Google Scholar
• Bustamante VH, Martínez LC, Santana FJ, Knodler LA, Steele-Mortimer O, Puente JL. HilD-mediated transcriptional cross-talk between SPI-1 and SPI-2. Proc National Acad Sci. 2008;105(38):14591–14596. doi:10.1073/pnas.0801205105
   Web of Science ®Google Scholar
• Pérez-Morales D, Banda MM, Chau NYE, et al. The transcriptional regulator SsrB is involved in a molecular switch controlling virulence lifestyles of Salmonella. PLoS Pathog. 2017;13(7):e1006497. doi:10.1371/journal.ppat.100649728704543
   PubMed Web of Science ®Google Scholar
• Gantois I, Ducatelle R, Pasmans F, et al. Butyrate specifically down-regulates salmonella pathogenicity island 1 gene expression. Appl Environ Microbiol. 2006;72(1):946. doi:10.1128/AEM.72.1.946-949.200616391141
   PubMed Web of Science ®Google Scholar
• Bronner DN, Faber F, Olsan EE, et al. Genetic ablation of butyrate utilization attenuates gastrointestinal Salmonella disease. Cell Host Microbe. 2018;23(2):266–273.e264. doi:10.1016/j.chom.2018.01.00429447698
   PubMed Web of Science ®Google Scholar
• Wick MJ. The role of dendritic cells during Salmonella infection. Curr Opin Immunol. 2002;14(4):437–443. doi:10.1016/S0952-7915(02)00364-312088677
   PubMed Web of Science ®Google Scholar
• Cheminay C, Schoen M, Hensel M, et al. Migration of Salmonella typhimurium –harboring bone marrow–derived dendritic cells towards the chemokines CCL19 and CCL21. Microb Pathog. 2002;32(5):207–218. doi:10.1006/mpat.2002.049712071677
   PubMed Web of Science ®Google Scholar
• Carden SE, Walker GT, Honeycutt J, et al. Pseudogenization of the secreted effector gene sseI confers rapid systemic dissemination of S. Typhimurium ST313 within migratory dendritic cells. Cell Host Microbe. 2017;21(2):182–194. doi:10.1016/j.chom.2017.01.00928182950
   PubMed Web of Science ®Google Scholar
• Reyes M, Fisher S, McLaughlin LM, et al. A microfluidic-based genetic screen to identify microbial virulence factors that inhibit dendritic cell migration. Integr Biol. 2014;6(4):438–449. doi:10.1039/C3IB40177D
   Google Scholar
• Riol-Blanco L, Sanchez-Sanchez N, Torres A, et al. The chemokine receptor CCR7 activates in dendritic cells two signaling modules that independently regulate chemotaxis and migratory speed. J Immunol. 2005;174(7):4070–4080. doi:10.4049/jimmunol.174.7.407015778365
   PubMed Web of Science ®Google Scholar
• Miao EA, Brittnacher M, Haraga A, Jeng RL, Welch MD, Miller SI. Salmonella effectors translocated across the vacuolar membrane interact with the actin cytoskeleton. Mol Microbiol. 2003;48(2):401–415. doi:10.1046/j.1365-2958.2003.t01-1-03456.x12675800
   PubMed Web of Science ®Google Scholar
• McLaughlin LM, Govoni GR, Gerke C, et al. The Salmonella SPI2 effector SseI mediates long-term systemic infection by modulating host cell migration. PLoS Pathog. 2009;5(11):e1000671. doi:10.1371/journal.ppat.100067119956712
   PubMed Web of Science ®Google Scholar
• Arpaia N, Godec J, Lau L, et al. TLR signaling is required for Salmonella typhimurium virulence. Cell. 2011;144(5):675–688. doi:10.1016/j.cell.2011.01.03121376231
   PubMed Web of Science ®Google Scholar
• Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol. 2004;5(10):987. doi:10.1038/ni111215454922
   PubMed Web of Science ®Google Scholar
• Hsu LC, Park JM, Zhang K, et al. The protein kinase PKR is required for macrophage apoptosis after activation of Toll-like receptor 4. Nature. 2004;428(6980):341–345. doi:10.1038/nature0240515029200
   PubMed Web of Science ®Google Scholar
• Park JM, Greten FR, Li ZW, Karin M. Macrophage apoptosis by anthrax lethal factor through p38 MAP kinase inhibition. Science. 2002;297(5589):2048–2051. doi:10.1126/science.107316312202685
   PubMed Web of Science ®Google Scholar
• Forstner J, Oliver M, Sylvester F. Production, structure and biologic relevance of gastrointestinal mucins. Infect Gastrointest Tract. 1995;1995:71–88.
   Google Scholar
• Vimal DB, Khullar M, Gupta S, Ganguly NK. Intestinal mucins: the binding sites for Salmonella typhimurium. Mol Cell Biochem. 2000;204(1–2):107–117. doi:10.1023/A:100701531203610718631
   PubMed Web of Science ®Google Scholar
• Arabyan N, Weis AM, Huang BC, Weimer BC. Implication of sialidases in Salmonella infection: genome release of sialidase knockout strains from Salmonella enterica serovar typhimurium LT2. Genome Announc. 2017;5(19):e00341–e00317. doi:10.1128/genomeA.00341-1728495784
   PubMedGoogle Scholar
• Songhet P, Barthel M, Stecher B, et al. Stromal IFN-γR-signaling modulates goblet cell function during Salmonella typhimurium infection. PLoS One. 2011;6(7):e22459. doi:10.1371/journal.pone.002245921829463
   PubMed Web of Science ®Google Scholar
• Johansson C, Ingman M, Wick MJ. Elevated neutrophil, macrophage and dendritic cell numbers characterize immune cell populations in mice chronically infected with Salmonella. Microb Pathog. 2006;41(2–3):49–58. doi:10.1016/j.micpath.2006.03.00416782300
   PubMed Web of Science ®Google Scholar
• Broz P, Newton K, Lamkanfi M, Mariathasan S, Dixit VM, Monack DM. Redundant roles for inflammasome receptors NLRP3 and NLRC4 in host defense against Salmonella. J Exp Med. 2010;207(8):1745. doi:10.1084/jem.2010025720603313
   PubMed Web of Science ®Google Scholar
• De Groote MA, Ochsner UA, Shiloh MU, et al. Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. Proc Natl Acad Sci U S A. 1997;94(25):13997–14001. doi:10.1073/pnas.94.25.139979391141
   PubMed Web of Science ®Google Scholar
• Godinez I, Raffatellu M, Chu H, et al. Interleukin-23 orchestrates mucosal responses to Salmonella enterica serotype typhimurium in the intestine. Infect Immun. 2009;77(1):387.18955477
   PubMed Web of Science ®Google Scholar
• Zindl CL, Lai J-F, Lee YK, et al. IL-22–producing neutrophils contribute to antimicrobial defense and restitution of colonic epithelial integrity during colitis. Proc National Acad Sci. 2013;110(31):12768–12773. doi:10.1073/pnas.1300318110
   PubMed Web of Science ®Google Scholar
• Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, Mills KH. Interleukin-1 and IL-23 induce innate IL-17 production from γδ T cells, amplifying Th17 responses and autoimmunity. Immunity. 2009;31(2):331–341. doi:10.1016/j.immuni.2009.08.00119682929
   PubMed Web of Science ®Google Scholar
• Mooney JP, Galloway LJ, Riley EM. Malaria, anemia, and invasive bacterial disease: a neutrophil problem? J Leukoc Biol. 2019;105(4):645–655. doi:10.1002/jlb.2019.105.issue-430570786
   PubMed Web of Science ®Google Scholar
• Corbin BD, Seeley EH, Raab A, et al. Metal chelation and inhibition of bacterial growth in tissue abscesses. Science. 2008;319(5865):962. doi:10.1126/science.115244918276893
   PubMed Web of Science ®Google Scholar
• Diaz-Ochoa Vladimir E, Lam D, Lee Carlin S, et al. Salmonella mitigates oxidative stress and thrives in the inflamed gut by evading calprotectin-mediated manganese sequestration. Cell Host Microbe. 2016;19(6):814–825. doi:10.1016/j.chom.2016.05.00527281571
   PubMed Web of Science ®Google Scholar
• Lin D, Kim B, Slauch JM. DsbL and DsbI contribute to periplasmic disulfide bond formation in Salmonella enterica serovar typhimurium. Microbiology. 2009;155(Pt 12):4014–4024. doi:10.1099/mic.0.032904-019797361
   PubMed Web of Science ®Google Scholar