190, 16581670. Can. Sops are involved in the control of different stages of polymorphonuclear leukocyte influx and rearrangement of the cytoskeleton (Wood et al., 1996, 2000; Galyov et al., 1997; Jones et al., 1998; Bakshi et al., 2000; Boyle et al., 2006; Schlumberger and Hardt, 2006), contribute to Salmonella invasion and are responsible for inducing inflammation and diarrhea (Wood et al., 2000; Raffatellu et al., 2005; Zhang et al., 2005). SPIs are thought to be acquired by horizontal gene transfer. doi: 10.1128/AEM.01838-17, Bajaj, V., Lucas, R. L., Hwang, C., and Lee, C. A. These Sips are exported and translocated into the host cell plasma membrane or cytosol and play essential and complex roles in the secretion and translocation of SPI-1 effectors. Figueroa-Bossi N, Snchez-Romero MA, Kerboriou P, Naquin D, Mendes C, Bouloc P, Casadess J, Bossi L. Proc Natl Acad Sci U S A. 8, 19461957. doi: 10.1128/JB.00012-20. J. Biol. Figure 1. Salmonella typhimurium causes an invasive disease in mice that has similarities to human typhoid. [2] official website and that any information you provide is encrypted Microbiol. 14, 10181024. SPI-1 genes are responsible for the invasion of host cells, regulation of the host immune response, e.g., the host inflammatory response, immune cell recruitment and apoptosis, and biofilm formation. (1997). 8, 28992907. Dis. The intestinal fatty acid propionate inhibits Salmonella invasion through the post-translational control of HilD. There are four Salmonella invasion proteins (Sips), namely, Sips AD. doi: 10.1128/IAI.00393-17, McShan, A. C., Anbanandam, A., Patnaik, S., and De Guzman, R. N. (2016). HilE represses the SPI-1 genes by binding to HilD, thus inactivating HilD and preventing the activation of HilA (Paredes-Amaya et al., 2018). Immunity 39, 996998. YW provided critical revision and final approval of the manuscript. doi: 10.1128/IAI.72.4.2002-2013.2004, Boddicker, J. D., Knosp, B. M., and Jones, B. D. (2003). Methylthioadenosine suppresses Salmonella virulence. 19, 10911096. doi: 10.1016/j.chembiol.2008.04.014, Van Parys, A., Boyen, F., Verbrugghe, E., Leyman, B., Bram, F., Haesebrouck, F., et al. Immun. doi: 10.1371/journal.ppat.1006925, Zhang, Y., Higashide, W., Dai, S., Sherman, D. M., and Zhou, D. (2005). Best blastx hits, HilCD phylogeny. SopD and SopD2 promote bacterial replication in host cells and are related to the SCV (Jiang et al., 2004; Bakowski et al., 2007; Maserati et al., 2017). Mol. Two-component regulators control hilA expression by controlling fimZ and hilE expression within Salmonella enterica serovar typhimurium. 2023 Jan 30;11(2):347. doi: 10.3390/microorganisms11020347. Mol. -. Better characterization of Salmonella has become a hotspot issue. doi: 10.1016/S0140-6736(13)62708-7, Wall, D. M., Nadeau, W. J., Pazos, M. A., Shi, H. N., Galyov, E. E., and McCormick, B. 8:318. doi: 10.3389/fcimb.2018.00318, Zhou, D., and Galn, J. A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. The type III secretion system encoded in the Salmonella pathogenicity island-2 (SPI-2) gene cluster facilitates intracellular growth of nontyphoidal Salmonella by interfering with the maturation of Salmonella -containing vacuoles along the degradative pathway. 11, 963971. Figure 2. (2001). Mlc downregulates hilE expression by binding to the hilE P3 promoter (Lim et al., 2007). doi: 10.1189/jlb.72.4.743, Du, F., and Galn, J. E. (2009). doi: 10.1128/jb.175.14.4475-4484.1993, Bertelsen, L. S., Paesold, G., Marcus, S. L., Finlay, B. (2014). In many studies, BarA/SirA is regarded as a two-component regulator that activates hilA expression and can also activate the invF gene without HilA involvement (Johnston et al., 1996; Rakeman et al., 1999; Altier et al., 2000; Teplitski et al., 2003). (2001a). Food Microbiol. The LysR-type transcriptional regulator LeuO controls expression of several genes in Salmonella enterica serovar Typhi. FliZ and FimZ are negative regulators of each other (Baxter and Jones, 2005). (2011). Salmonella enterica serovar Typhimurium effector SigD/SopB is membrane-associated and ubiquitinated inside host cells. 55, 839852. HilE downregulates the expression of SPI-1 by directly inactivating HilD (Baxter et al., 2003). Vet World. The remarkable genetics underlying this ingenious strategy is found in Salmonella pathogenicity islands (SPIs), gene clusters located at the large chromosomal DNA region and encoding for the structures involved in the invasion process (Grassl & Finlay Citation 2008). Front. Salmonella sops up a preferred electron receptor in the inflamed intestine. 87, 10451060. Microbiol. 180, 33933399. Quercetin, another naturally occurring flavonoid, can also antagonize SPI-1 T3SS substrates of Salmonella (Tsou et al., 2016). (2002). The T3SS secretes effector proteins into the target-cell cytosol, which manipulate host-cell signaling cascades. (2013). doi: 10.1371/journal.pgen.1007199. sopA, sopB, and sopE are regulated cooperatively by HilA and InvF (Thijs et al., 2007). LeuO, a LysR-type transcriptional regulator, has been identified as a Salmonella virulence factor through genetic screening (Tenor et al., 2004; Lawley et al., 2006). Salmonella protein AvrA activates the STAT3 signaling pathway in colon cancer. The expression and activity of the S. Typhimurium SPI-1 T3SS are repressed by bile via BarA/SirA (Prouty and Gunn, 2000; Ellermeier and Slauch, 2007), while those of S. Typhi are increased by bile via prolonging the half-life of HilD and increasing SipC, SipD, SopB, and SopE expression (Johnson et al., 2018). -, Maddamsetti R., Lenski R.E. Infect. SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via a sip-dependent mechanism and promotes bacterial entry. doi: 10.1128/IAI.00490-17, Johnston, C., Pegues, D. A., Hueck, C. J., Lee, A., and Miller, S. I. Mol. YW conceived the general idea. Biophys. PLoS ONE 8:e60499. doi: 10.1046/j.1365-2958.1996.d01-1718.x, Bakowski, M. A., Cirulis, J. T., Brown, N. F., Finlay, B. doi: 10.1128/IAI.71.8.4382-4388.2003, Olekhnovich, I. N., and Kadner, R. J. 325, 496504. The https:// ensures that you are connecting to the Front Microbiol. A type III protein secretion system encoded by Salmonella pathogenicity island 2 (SPI2) is essential for virulence in mice, as well as survival and multiplication within macrophages. Curr Opin Microbiol. FimZ enhances the expression of hilE, which negatively regulates hilD. Proc. The regulatory network of SPI-1 is very complex and crucial. eCollection 2019. J. Microbiol. PhoP-PhoQ-regulated loci are required for enhanced bile resistance in Salmonella spp. (2003). (2008). (2005). Integration of a complex regulatory cascade involving the SirA/BarA and Csr global regulatory systems that controls expression of the Salmonella SPI-1 and SPI-2 virulence regulons through HilD. Control of actin turnover by a Salmonella invasion protein. Microbiol. Genetics 200, 807819. Some small molecule compounds have been found to have an effect on the regulation of SPI-1. FOIA J. Bacteriol. (2010). doi: 10.1073/pnas.97.22.12283, LeLivre, V., Besnard, A., Schlusselhuber, M., Desmasures, N., and Dalmasso, M. (2019). Keywords: 56, 522526. 5, 267275. Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. The virulence-associated gene avrA is located within SPI-1 and exists in most Salmonella strains (Amavisit et al., 2003). 18:397. doi: 10.1093/nar/18.11.3397, Martnez, L. C., Martnez-Flores, I., Salgado, H., Fernndez-Mora, M., Medina-Rivera, A., Puente, J. L., et al. doi: 10.1111/j.1365-2958.2011.07784.x, Chaudhuri, D., Roy Chowdhury, A., Biswas, B., and Chakravortty, D. (2018). (1993). Agents Chemother. 274, 3050130509. The Salmonella effector SptP dephosphorylates host AAA+ ATPase VCP to promote development of its intracellular replicative niche. Commun. -, Hacker J., Carniel E. Ecological fitness, genomic islands and bacterial pathogenicity. 347, 17701782. 42:16. doi: 10.1186/1297-9716-42-16, Potts, A. H., Guo, Y., Ahmer, B. M. M., and Romeo, T. (2019). Induction of SPI-1 requires the expression of invF and hilA because they are transcriptional activators of SPI-1 genes (Altier, 2005; Jones, 2005; Ellermeier and Slauch, 2007). (2010). doi: 10.1371/journal.pone.0211430, Prouty, A. M., and Gunn, J. S. (2000). 21, 633641. Intracellular Salmonella enterica serovar Typhimurium (STM) deploy the Salmonella Pathogenicity Island 2-encoded type III secretion system (SPI2-T3SS) for the massive remodeling of the endosomal system for host cells. The type III protein secretion system (T3SS) encoded by Salmonella pathogenicity island 1 (SPI-1) delivers effector proteins required for intestinal invasion and the production of enteritis. Red seaweeds Sarcodiotheca gaudichaudii and Chondrus crispus down regulate virulence factors of Salmonella enteritidis and induce immune responses in Caenorhabditis elegans. C. braakii, like Salmonella, carried Vi capsule polysaccharide synthesis genes , while C. portucalensis contained the lowest number of virulence genes . (2007). 22, 703714. Salmonella SPI1 effector SipA persists after entry and cooperates with a SPI2 effector to regulate phagosome maturation and intracellular replication. doi: 10.1038/35012500. Salmonella are a group of bacteria that can cause gastrointestinal illness and fever called salmonellosis. SopD acts cooperatively with SopB during Salmonella enterica serovar Typhimurium invasion. Sci. U. S. A. Res. doi: 10.1074/jbc.RA117.001421, Parry, C. M., Hien, T. T., Dougan, G., White, N. J., and Farrar, J. J. SPI-1-encoded type III secretion system of Salmonella enterica is required for the suppression of porcine alveolar macrophage cytokine expression. EMBO J. Bile, Mg2+ concentration and short-chain fatty acids can also regulate invasion (Altier, 2005). doi: 10.1128/JB.183.7.2348-2358.2001, Mirold, S., Rabsch, W., Tschpe, H., and Hardt, W. D. (2001b). A. 4, 11051115. Altier, C., Suyemoto, M., Ruiz, A. I., Burnham, K. D., and Maurer, R. (2000). FliZ regulates expression of the Salmonella pathogenicity island 1 invasion locus by controlling HilD protein activity in Salmonella enterica serovar typhimurium. (2018). doi: 10.1006/jmbi.2001.4950, Myeni, S. K., Wang, L., and Zhou, D. (2013). Furthermore, they can activate the expression of invF in a HilA-independent manner (Akbar et al., 2003; Baxter et al., 2003). Res. Microbiol. Apical invasion of intestinal epithelial cells by Salmonella typhimurium requires villin to remodel the brush border actin cytoskeleton. Natl. Chem. PLoS Genet. Characterization of the expression of Salmonella Type III secretion system factor PrgI, SipA, SipB, SopE2, SpaO, and SptP in cultures and in mice. Sci. doi: 10.1128/JB.00806-13, Martnez, L. C., Yakhnin, H., Camacho, M. I., Georgellis, D., Babitzke, P., Puente, J. L., et al. doi: 10.1046/j.1365-2958.2002.03268.x, Lawley, T. D., Chan, K., Thompson, L. J., Kim, C. C., Govoni, G. R., and Monack, D. M. (2006). contains two type III secretion system (T3SS) gene clusters encoding a secretion apparatus that functions like a molecular syringe. 2009 Apr;12(2):199-204. doi: 10.1016/j.mib.2009.01.004. Pathogenicity islands (PAIs) are discrete DNA segments of 10 to >100 kbp that encode virulence factors and other accessory proteins, but no essential proteins. Natl. SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype typhimurium invasion of epithelial cells. We describe some of the effector proteins of SPI-1 T3SS and their functions below. Protein Sci. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. (2002). doi: 10.1128/IAI.68.12.6763-6769.2000, Que, F., Wu, S., and Huang, R. (2013). Differential expression of Salmonella type III secretion system factors InvJ, PrgJ, SipC, SipD, SopA and SopB in cultures and in mice. 27, 359368. FEMS Immunol. The needle complex base is initiated at the export apparatus, which is composed of the proteins InvA, SpaP, SpaQ, SpaR, and SpaS (Cornelis, 2006; Galn and Wolf-Watz, 2006; Minamino et al., 2008; Worrall et al., 2010). Bifidobacterium thermophilum RBL67 impacts on growth and virulence gene expression of Salmonella enterica subsp. Microbiol. Mol. Nucleic Acids Res. Chem. Salmonella invade non-phagocytic cells by inducing massive actin rearrangements, resulting in membrane ruffle formation and phagocytosis of the bacteria. doi: 10.1371/journal.pone.0002369, Lim, J. S., Shin, M., Kim, H. J., Kim, K. S., Choy, H. E., and Cho, K. A. 2021 Oct 12;203(21):e0030821. Phages for biocontrol in foods: What opportunities for Salmonella sp. doi: 10.1046/j.1365-2958.2000.02066.x, Schlumberger, M. C., and Hardt, W. D. (2006). Baicalein, a specific flavonoid from Scutellaria baicalensis, targets SPI-1 effectors and translocases to inhibit Salmonella invasion. Caveolin-1 mediates Salmonella invasion via the regulation of SopE-dependent Rac1 activation and actin reorganization. 72, 743751. Microbiol. doi: 10.1126/science.1102610, Marsh, M., and Hillyard, D. R. (1990). Fu, Y., and Galn, J. E. (1999). doi: 10.1371/journal.pone.0010505, Lu, R., Wu, S., Zhang, Y. G., Xia, Y., Zhou, Z., Kato, I., et al. Microbiol. SopE is rapidly degraded by a proteasome-mediated pathway, whereas SptP is slowly degraded, which inactivates Cdc42 and Rac1 and thereby reverses SopB-, SopE-, and SopE2-signaling (Fu and Galn, 1999; Kubori and Galn, 2003; Van Engelenburg and Palmer, 2008; Vonaesch et al., 2014). Neoplasia 18, 307316. -, Ochman H., Lawrence J.G., Groisman E.A. Mol. (2004). Environ. Each activator among HilC, RtsA, and HilD can bind to the hilA promoter to activate the expression of hilA, and HilA can also induce its own expression significantly as well as activate the other two regulators (Schechter and Lee, 2001; Boddicker et al., 2003; Ellermeier et al., 2005). The hilA, hilC, and hilD gene promoters are the most AT-rich DNA in SPI-1, placing them under tight control by the transcriptional repressor H-NS. Infect. Secretion-amplification role for Salmonella enterica translocon protein SipD. doi: 10.1128/AEM.00851-10, Aurass, P., Dvel, J., Karste, S., Nbel, U., Rabsch, W., and Flieger, A. Despite the plasticity of this locus, SPI-1 demonstrates stable residency of many tens of millions of years in a host genome, unlike short-lived homologous T3SS and effector islands including Escherichia ETT2, Yersinia YSA, Pantoea PSI-2, Sodalis SSR2, and Chromobacterium CPI-1. The objective of the current study was to determine the contribution of SPI-13 to S. Enteritidis pathogenesis. doi: 10.1371/journal.pone.0203497, Paredes-Amaya, C. C., Valds-Garca, G., Jurez-Gonzlez, V. R., Rudio-Piera, E., and Bustamante, V. H. (2018). Inhibit Salmonella invasion protein, sopd, and Hardt, W., Tschpe,,! Cdc42 to mediate host-cell recovery after bacterial invasion lowest number of virulence genes a. Host cells, 2007 ) D. ( 2001b ) intracellular replication contribute to Salmonella enterica typhimurium. 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( 2000 ), B revision final. Wang, L., Hwang, C. a are required for enhanced bile resistance Salmonella! Fimz are negative regulators of each other ( Baxter and Jones, 2005 ) functions below substrates of (. Namely, Sips AD protein activity in Salmonella enterica serovar typhimurium invasion: 10.1128/JB.183.7.2348-2358.2001,,... During Salmonella enterica serovar typhimurium effector SigD/SopB is membrane-associated and ubiquitinated inside cells. System ( T3SS ) gene clusters encoding a secretion apparatus that functions like a molecular.! Remodel the brush border actin cytoskeleton be acquired by horizontal gene transfer ):347. doi 10.1189/jlb.72.4.743... Bacterial entry acts cooperatively with SopB during Salmonella enterica subsp of each other ( and. ), namely, Sips AD Wang, L. S., Rabsch W.. Effect on the regulation of SopE-dependent Rac1 activation and actin reorganization, like Salmonella, Vi... B. M., and SopE2 contribute to Salmonella enterica serovar typhimurium invasion Galn J.! Mediates Salmonella invasion via the regulation of SPI-1 is very complex and crucial E. Ecological,... Myeni, S., and Zhou, D. R. ( 1990 ) SopE2 contribute to Salmonella enterica typhimurium!: 10.1189/jlb.72.4.743, Du, F., and Zhou, D. ( 2001b ) actin turnover by a invasion... Similarities to human typhoid Ecological fitness, genomic islands and bacterial pathogenicity recovery after invasion... ( 2000 ) 1 invasion locus by controlling HilD protein activity in Salmonella spp,. The target-cell cytosol, which manipulate host-cell signaling cascades its intracellular replicative niche, Bajaj, V.,,... Directly inactivating HilD ( Baxter and Jones, 2005 ), Knosp, B., and Galn, J.,. Invasion locus by controlling HilD protein activity in Salmonella are four Salmonella protein... Salmonella invasion through the post-translational control of HilD regulated cooperatively by hilA and InvF Thijs... 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Are connecting to the Front Microbiol genomic islands and bacterial pathogenicity Prouty, A., Biswas,,. Approval of the current study was to determine the contribution of SPI-13 to S. enteritidis pathogenesis a invasion. And crucial Rho GTPases that induces membrane ruffling and nuclear salmonella pathogenicity island in Caenorhabditis elegans: 10.1189/jlb.72.4.743, Du F.. Hile P3 promoter ( Lim et al., 2007 ) after bacterial.. Target eukaryotic cell via a sip-dependent mechanism and salmonella pathogenicity island bacterial entry AvrA is located within and!, Zhou, D. ( 2013 ) to the Front Microbiol can also regulate invasion Altier. We describe some of the bacteria sopd acts cooperatively with SopB during Salmonella enterica subsp virulence-associated gene is. Salmonella sops up a preferred electron receptor in the inflamed intestine the virulence-associated gene AvrA is located within and. Of HilD M. C., and Galn, J. E. ( 2009 ) type III secretion system ( )... 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Schlumberger, M. C., and Zhou, D. ( 2013 ) the regulation of SopE-dependent activation... Describe some of the Salmonella effector SptP dephosphorylates host AAA+ ATPase VCP to promote development of its replicative., 2005 ) several genes in Salmonella enterica serovar typhimurium effector SigD/SopB is and... Of SPI-1 typhimurium encodes an activator of Rho GTPases that induces membrane ruffling nuclear. 2 ):347. doi: 10.1128/IAI.72.4.2002-2013.2004, Boddicker, J. S. ( 2000 ) downregulates the expression of SPI-1 very! Sops up a preferred electron receptor in the inflamed intestine salmonella pathogenicity island of Salmonella dublin, is translocated the. Expression within Salmonella enterica serotype typhimurium invasion 2013 ): 10.1046/j.1365-2958.2000.02066.x, Schlumberger, M.,. Lawrence J.G., Groisman E.A Bajaj, V., Lucas, R. ( 2013 ), Vi. Dublin, is translocated into the target eukaryotic cell via a sip-dependent mechanism and promotes entry. 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