Abstract
Microbial infections are controlled by host inflammatory responses that are initiated by innate immune receptors after recognition of conserved microbial products. As inflammation can also lead to disease, tissues that are exposed to microbial products such as the intestinal epithelium are subject to stringent regulatory mechanisms to prevent indiscriminate signalling through innate immune receptors. The enteric pathogen Salmonella enterica subsp. enterica serovar Typhimurium, which requires intestinal inflammation to sustain its replication in the intestinal tract, uses effector proteins of its type III secretion systems to trigger an inflammatory response without the engagement of innate immune receptors. Furthermore, S. Typhimurium uses a different set of effectors to restrict the inflammatory response to preserve host homeostasis. The S. Typhimurium–host interface is a remarkable example of the unique balance that emerges from the co-evolution of a pathogen and its host.
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References
Shannon, E. et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clin. Infect. Dis. 50, 882–889 (2010).
Buckle, G., Walker, C. & Black, R. Typhoid fever and paratyphoid fever: systematic review to estimate global morbidity and mortality for 2010. J. Glob. Health 2, 010401 (2012).
Popoff, M., Bockemühl, J. & Brenner, F. Supplement 1998 (no. 42) to the Kauffmann-White scheme. Res. Microbiol. 151, 63–65 (2000).
Brenner, F. W., Villar, R. G., Angulo, F. J., Tauxe, R. & Swaminathan, B. Salmonella nomenclature. J. Clin. Microbiol. 38, 2465–2467 (2000).
House, D., Bishop, A., Parry, C., Dougan, G. & Wain, J. Typhoid fever: pathogenesis and disease. Curr. Opin. Infect. Dis. 14, 573–578 (2001).
Dougan, G. & Baker, S. Salmonella enterica serovar Typhi and the pathogenesis of typhoid fever. Annu. Rev. Microbiol. 68, 317–336 (2014).
Parry, C., Hien, T. T., Dougan, G., White, N. & Farrar, J. Typhoid fever. N. Engl. J. Med. 347, 1770–1782 (2002).
Hohmann, E. Nontyphoidal salmonellosis. Clin. Infect. Dis. 32, 263–269 (2001).
Rivera-Chávez, F. & Bäumler, A. The pyromaniac inside you: Salmonella metabolism in the host gut. Annu. Rev. Microbiol. 69, 31–48 (2015).
Akira, S., Uematsu, S. & Takeuchi, O. Pathogen recognition and innate immunity. Cell 124, 783–801 (2006).
Creagh, E. & O’Neill, L. TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity. Trends Immunol. 27, 352–357 (2006).
Medzhitov, R. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1, 135–145 (2001).
Stecher, B. et al. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 5, 2177–2189 (2007). Seminal work demonstrating the importance of the inflammatory response in allowing S. Typhimurium to overcome the colonization resistance conferred by the resident intestinal microbiota.
Winter, S. et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467, 426–429 (2010). Work demonstrating the role of inflammation in providing S. Typhimurium with essential electron acceptors to sustain its respiration and replication in the intestine.
Buffie, C. & Pamer, E. Microbiota-mediated colonization resistance against intestinal pathogens. Nat. Rev. Immunol. 13, 790–801 (2013).
Rangan, K. & Han, H. Biochemical mechanisms of pathogen restriction by intestinal bacteria. Trends Biochem. Sci. 42, 887–898 (2017).
Olsan, E. et al. Colonization resistance: the deconvolution of a complex trait. J. Biol. Chem. 292, 8577–8581 (2017).
Lupp, C. et al. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2, 204–2012 (2007).
Zeng, M., Inohara, N. & Nuñez, G. Mechanisms of inflammation-driven bacterial dysbiosis in the gut. Mucosal Immunol. 10, 18–26 (2017).
Thiennimitr, P. et al. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc. Natl Acad. Sci. USA. 108, 17480–17485 (2011).
Santos, R. et al. Life in the inflamed intestine, Salmonella style. Trends Microbiol. 17, 498–506 (2009).
Rogers, A., Tsolis, R. & Bäumler, A. Salmonella versus the microbiome. Microbiol. Mol. Biol. Rev. 85, e00027–00019 (2020).
Fattinger, S., Sellin, M. & Hardt, W. Epithelial inflammasomes in the defense against Salmonella gut infection. Curr. Opin. Microbiol. 59, 86–94 (2021).
Ohl, M. E. & Miller, S. I. Salmonella: a model for bacterial pathogenesis. Annu. Rev. Med. 52, 259–274 (2001).
Giannella, R. A., Broitman, S. A. & N., Z. Gastric acid barrier to ingested microorganisms in man: studies in vivo and in vitro. Gut 13, 251–256 (1972).
Tsolis, R. M., Xavier, M. N., Santos, R. L. & AJ., B. How to become a top model: impact of animal experimentation on human Salmonella disease research. I. Infect. Immun. 79, 1806–1814 (2011).
Stecher, B. et al. Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect. Immun. 72, 4138–4150 (2004).
Galán, J. E. & Curtiss, III, R. Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc. Natl Acad. Sci. USA 86, 6383–6387 (1989).
Galán, J., Lara-Tejero, M., Marlovits, T. & Wagner, S. Bacterial type III secretion systems: specialized nanomachines for protein delivery into target cells. Annu. Rev. Microbiol. 68, 415–438 (2014).
Figueira, R. & Holden, D. Functions of the Salmonella pathogenicity island 2 (SPI-2) type III secretion system effectors. Microbiology 158, 1147–1161 (2012).
LaRock, D., Chaudhary, A. & Miller, S. Salmonellae interactions with host processes. Nat. Rev. Microbiol. 13, 191–205 (2015).
Takeuchi, A. Electron microscopic studies of experimental Salmonella infection. 1. Penetration into the intestinal epithelium by Salmonella typhimurium. Am. J. Pathol. 50, 109–136 (1967).
Galán, J. E. Salmonella interaction with host cells: type III secretion at work. Annu. Rev. Cell Dev. Biol. 17, 53–86 (2001).
Hume, P., Singh, V., Davidson, A. & Koronakis, V. Swiss army pathogen: the salmonella entry toolkit. Front. Cell Infect. Microbiol. 7, 348–358 (2017).
Hobbie, S., Chen, L. M., Davis, R. & Galán, J. E. Involvement of the mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal cells. J. Immunol. 159, 5550–5559 (1997). First demonstration that S. Typhimurium can stimulate transcriptional responses in cultured intestinal cells in a T3SS-dependent manner.
Bruno, V. M. et al. Salmonella Typhimurium type III secretion effectors stimulate innate immune responses in cultured epithelial cells. PLoS Pathog. 5, e1000538 (2009). Work reporting that in cultured intestinal epithelial cells and through the activity of a subset of its type III secreted effector proteins, S. Typhimurium can trigger transcriptional responses similar to those observed after stimulation by innate immune receptors.
Hardt, W.-D., Chen, L.-M., Schuebel, K. E., Bustelo, X. R. & Galán, J. E. Salmonella typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93, 815–826 (1998).
Patel, J. C. & Galan, J. E. Manipulation of the host actin cytoskeleton by Salmonella–all in the name of entry. Curr. Opin. Microbiol. 8, 10–15 (2005).
Patel, J. C. & Galan, J. E. Differential activation and function of Rho GTPases during Salmonella-host cell interactions. J. Cell Biol. 175, 453–463 (2006).
Zhou, D., Chen, L. M., Hernandez, L., Shears, S. B. & Galan, J. E. A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol. Microbiol. 39, 248–259 (2001).
Zhou, D., Mooseker, M. & Galán, J. E. Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 283, 2092–2095 (1999).
Jennings, E., Thurston, T. & Holden, D. Salmonella SPI-2 type III secretion system effectors: molecular mechanisms and physiological consequences. Cell Host Microbe. 22, 217–231 (2017).
Wotzka, S., Nguyen, B. & Hardt, W. Salmonella typhimurium diarrhea reveals basic principles of enteropathogen infection and disease-promoted DNA exchange. Cell Host Microbe. 21, 443–454 (2017).
Stevens, M., Humphrey, T. & Maskell, D. Molecular insights into farm animal and zoonotic Salmonella infections. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 2709–2723 (2009).
Feasey, N., Dougan, G., Kingsley, R., Heyderman, R. & Gordon, M. Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet 379, 2489–2499 (2012).
Lee, J., Mo, J., Shen, C., Rucker, A. & Raz, E. Toll-like receptor signaling in intestinal epithelial cells contributes to colonic homoeostasis. Curr. Opin. Gastroenterol. 23, 27–31 (2007).
Kelly, D., Conway, S. & Aminov, R. Commensal gut bacteria: mechanisms of immune modulation. Trends Immunol. 26, 326–333 (2005).
Eckmann, L. Sensor molecules in intestinal innate immunity against bacterial infections. Curr. Opin. Gastroenterol. 22, 95–101 (2006).
Shibolet, O. & Podolsky, D. TLRs in the gut. IV. Negative regulation of Toll-like receptors and intestinal homeostasis: addition by subtraction. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G1469–G1473 (2007).
Lang, T. & Mansell, A. The negative regulation of Toll-like receptor and associated pathways. Immunol. Cell Biol. 85, 425–434 (2007).
Chen, L. M., Hobbie, S. & Galan, J. E. Requirement of CDC42 for Salmonella-induced cytoskeletal and nuclear responses. Science 274, 2115–2118 (1996). Work demonstrating that S. Typhimurium can stimulate transcriptional responses in a CDC42-dependent manner.
Miao, E. et al. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc. Natl Acad. Sci. USA 107, 3076–3080 (2010).
Jessen, D. et al. Type III secretion needle proteins induce cell signaling and cytokine secretion via Toll-like receptors. Infect. Immun. 82, 2300–2309 (2014).
Friebel, A. et al. SopE and SopE2 from Salmonella typhimurium activate different sets of RhoGTPases of the host cell. J. Biol. Chem. 276, 34035–34040 (2001).
Norris, F. A., Wilson, M. P., Wallis, T. S., Galyov, E. E. & Majerus, P. W. SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc. Natl Acad. Sci. USA 95, 14057–14059 (1998).
Keestra, A. et al. Manipulation of small Rho GTPases is a pathogen-induced process detected by NOD1. Nature 496, 233–237 (2013).
Lara-Tejero, M. et al. Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J. Exp. Med. 203, 1407–1412 (2006).
Sun, H., Kamanova, J., Lara-Tejero, M. & Galán, J. E. Salmonella stimulates pro-inflammatory signalling through p21-activated kinases bypassing innate immune receptors. Nat. Microbiol. 3, 1122–1130 (2018). Work showing that activation of CDC42 by S. Typhimurium leads to the formation of a non-canonical proinflammatory signalling complex formed by PAK1, TRAF6 and TAK1.
Walsh, M., Lee, J., Choi, Y. & Ibrahim, M. Tumor necrosis factor receptor- associated factor 6 (TRAF6) regulation of development, function, and homeostasis of the immune system. Immunol. Rev. 266, 72–92 (2015).
Ajibade, A., Wang, H. & Wang, R. Cell type-specific function of TAK1 in innate immune signaling. Trends Immunol. 34, 307–316 (2013).
Wood, M. W. et al. The secreted effector protein of Salmonella dublin, SopA, is translocated into eukaryotic cells and influences the induction of enteritis. Cell Microbiol. 2, 293–303 (2000).
Zhang, Y., Higashide, W., McCormick, B., Chen, J. & Zhou, D. The inflammation-associated Salmonella SopA is a HECT-like E3 ubiquitin ligase. Mol. Microbiol. 62, 786–793 (2006).
Kamanova, J., Sun, H., Lara-Tejero, M. & Galán, J. The salmonella effector protein sopa modulates innate immune responses by targeting TRIM E3 ligase family members. PLoS Pathog. 12, e1005552 (2016).
Rajsbaum, R., García-Sastre, A. & Versteeg, G. TRIMmunity: the roles of the TRIM E3-ubiquitin ligase family in innate antiviral immunity. J. Mol. Biol. 426, 1265–1284 (2014).
Yap, M. & Stoye, J. TRIM proteins and the innate immune response to viruses. Adv. Exp. Med. Biol. 770, 93–104 (2012).
Ikeda, K. & Inoue, S. TRIM proteins as RING finger E3 ubiquitin ligases. Adv. Exp. Med. Biol. 770, 27–37 (2012).
Tsuchida, T. et al. The ubiquitin ligase TRIM56 regulates innate immune responses to intracellular double-stranded DNA. Immunity 33, 765–776 (2010).
Dixit, E. & Kagan, J. Intracellular pathogen detection by RIG-I-like receptors. Adv. Immunol. 117, 99–125 (2013).
Reikine, S., Nguyen, J. & Modis, Y. Pattern recognition and signaling mechanisms of RIG-I and MDA5. Front. Immunol. 23, 5:342 (2014).
Schmolke, M. et al. RIG-I detects mRNA of intracellular Salmonella enterica serovar Typhimurium during bacterial infection. mBio 5, e01006–e01014 (2014).
Fiskin, E. et al. Structural basis for the recognition and degradation of host TRIM proteins by Salmonella effector SopA. Nat. Commun. 8, 14004 (2017).
Jones, M. A. et al. Secreted effector proteins of Salmonella dublin act in concert to induce enteritis. Infect. Immun. 66, 5799–5804 (1998).
Zhang, S. et al. The Salmonella enterica serotype typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves. Infect. Immun. 70, 3843–3855 (2002).
Lian, H. et al. The Salmonella effector protein SopD targets Rab8 to positively and negatively modulate the inflammatory response. Nat. Microbiol. https://doi.org/10.1038/s41564-021-00866-3 (2020).
Wall, A. et al. Small GTPase Rab8a-recruited phosphatidylinositol 3-Kinase γ regulates signaling and cytokine outputs from endosomal toll-like receptors. J. Biol. Chem. 292, 4411–4422 (2017).
Luo, L. et al. TLR crosstalk activates LRP1 to recruit Rab8a and PI3Kγ for suppression of inflammatory responses. Cell Rep. 24, 3033–3044 (2018).
Tong, S., Wall, A., Hung, Y., Luo, L. & Stow, J. Guanine nucleotide exchange factors activate Rab8a for Toll-like receptor signalling. Small GTPases 7, 1–17 (2019).
de Vasconcelos, N. & Lamkanfi, M. Recent insights on inflammasomes, gasdermin pores, and pyroptosis. Cold Spring Harb. Perspect. Biol. 12, a036392 (2020).
Broz, P. Recognition of intracellular bacteria by inflammasomes. Microbiol. Spectr. https://doi.org/10.1128/microbiolspec.BAI-0003-2019 (2019).
Hayward, J., Mathur, A., Ngo, C. & Man, S. Cytosolic recognition of microbes and pathogens: inflammasomes in action. Microbiol. Mol. Biol. Rev. 82, e00015–e00018 (2018).
Deets, K. & Vance, R. Inflammasomes and adaptive immune responses. Nat. Immunol. https://doi.org/10.1038/s41590-021-00869-6 (2021).
Ta, A. & Vanaja, S. Inflammasome activation and evasion by bacterial pathogens. Curr. Opin. Immunol. 68, 125–133 (2021).
von Moltke, J., Ayres, J., Kofoed, E., Chavarría-Smith, J. & Vance, R. Recognition of bacteria by inflammasomes. Annu. Rev. Immunol. 31, 73–106 (2013).
Monack, D. M., Raupach, B., Hromockyj, A. E. & Falkow, S. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc. Natl Acad. Sci. USA 93, 9833–9838 (1996).
Chen, L. M., Kaniga, K. & Galan, J. E. Salmonella spp. are cytotoxic for cultured macrophages. Mol. Microbiol. 21, 1101–1115 (1996).
Fattinger, S., Sellin, M. & Hardt, W. Epithelial inflammasomes in the defense against Salmonella gut infection. Curr. Opin. Microbiol. 59, 86–94 (2020).
Crowley, S., Knodler, L. & Vallance, B. Salmonella and the inflammasome: battle for intracellular dominance. Curr. Top. Microbiol. Immunol. 397, 43–67 (2016).
Miao, E. et al. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat. Immunol. 7, 569–575 (2006).
Knodler, L. et al. Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia. Proc. Natl Acad. Sci. USA. 107, 17733–17738 (2010).
Haneda, T. et al. Salmonella type III effector SpvC, a phosphothreonine lyase, contributes to reduction in inflammatory response during intestinal phase of infection. Cell Microbiol. 14, 485–499 (2012).
Lu, R. et al. Chronic effects of a Salmonella type III secretion effector protein AvrA in vivo. PLoS ONE 5, e10505 (2010).
Sun, H., Kamanova, J., Lara-Tejero, M. & Galán, J. A family of salmonella type III secretion effector proteins selectively targets the NF-κB Signaling pathway to preserve host homeostasis. PLoS Pathog. 12, e1005484 (2016).
Fu, Y. & Galan, J. E. A salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401, 293–297 (1999). First demonstration that a type III secreted effector protein antagonizes responses stimulated by other effector proteins to help the host recover its homeostasis.
Newson, J. et al. Salmonella effectors SseK1 and SseK3 target death domain proteins in the TNF and TRAIL signaling pathways. Mol. Cell Proteomics. 18, 1138–1156 (2019).
Günster, R., Matthews, S., Holden, D. & Thurston, T. SseK1 and SseK3 type III secretion system effectors inhibit NF-kappaB signaling and necroptotic cell death in Salmonella-infected macrophages. Infect. Immun. 85, e00010-17 (2017).
Rolhion, N. et al. Inhibition of nuclear transport of NF-ĸB p65 by the Salmonella type III secretion system effector SpvD. PLoS Pathog. 12, e1005653 (2016).
Jones, R. et al. Salmonella AvrA coordinates suppression of host immune and apoptotic defenses via JNK pathway blockade. Cell Host Microbe 3, 233–244 (2008).
Du, F. & Galan, J. E. Selective inhibition of type III secretion activated signaling by the Salmonella effector AvrA. PLoS Pathog. 5, e1000595 (2009).
Li, H. et al. The phosphothreonine lyase activity of a bacterial type III effector family. Science 315, 1000–1003 (2007).
Mazurkiewicz, P. et al. SpvC is a Salmonella effector with phosphothreonine lyase activity on host mitogen-activated protein kinases. Mol. Microbiol. 67, 1371–1383 (2008).
Sivars, U., Aivazian, D. & Pfeffer, S. Yip3 catalyses the dissociation of endosomal Rab-GDI complexes. Nature 425, 856–859 (2003).
Yamashita, T. & Tohyama, M. The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat. Neurosci. 6, 461–467 (2003).
Panagi, I. et al. Salmonella effector SteE converts the mammalian serine/threonine Kinase GSK3 into a tyrosine kinase to direct macrophage polarization. Cell Host Microbe. 27, 41–53 (2020). Work showing, together with Gibbs et al. (2020), an unusual mechanism of STAT3 activation by a S. Typhimurium effector protein.
Gibbs, K. et al. The salmonella secreted effector SarA/SteE mimics cytokine receptor signaling to activate STAT3. Cell Host Microbe. 27, 129–139 (2020).
Leppkes, M., Neurath, M., Herrmann, M. & Becker, C. Immune deficiency vs. immune excess in inflammatory bowel diseases-STAT3 as a rheo-STAT of intestinal homeostasis. J. Leukoc. Biol. 99, 57–66 (2016).
Hillmer, E., Zhang, H., Li, H. & Watowich, S. STAT3 signaling in immunity. Cytokine Growth Factor. Rev. 31, 1–15 (2016).
Hannemann, S., Gao, B. & Galán, J. Salmonella modulates host cell gene expression to promote its intracellular growth. PLoS Pathog. 9, e1003668 (2013).
Hu, B., Lara-Tejero, M., Kong, Q., Galán, J. & Liu, J. In situ molecular architecture of the salmonella type III secretion machine. Cell 168, 1065–1074 (2017).
Park, D. et al. Visualization of the type III secretion mediated Salmonella-host cell interface using cryo-electron tomography. eLife 7, e39514 (2018).
Acknowledgements
The author apologizes to many colleagues whose important work could not be discussed or cited due to space limitations. The author thanks M. Lara-Tejero for critical reading of the manuscript. Work in the author’s laboratory is supported by NIH grants R01AI114618, R01AI055472 and R01AI030492.
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Glossary
- Serovars
-
Types of Salmonella enterica based on their surface antigenic composition.
- Innate immune receptors
-
Surface receptors in immune cells that can recognize conserved bacterial products and stimulate an inflammatory response.
- Bacterial-associated molecular patterns
-
Conserved bacterial molecules that can stimulate innate immune receptors.
- Dysbiosis
-
A condition in which the composition of the resident intestinal microbiota is altered in a manner that leads to disruption of intestinal physiology.
- Type III secretion systems
-
(T3SSs). Complex molecular machines evolved by many bacterial pathogens to modulate host-cell processes through the delivery of bacterially encoded effector proteins directly into the target host cells.
- Injectisomes
-
A name used to refer to the entire type III protein secretion nanomachine that injects effector proteins into host cells.
- Flagella
-
A bacterial organelle that serves to propel the bacteria through liquid environments.
- Salmonella pathogenicity island 1
-
(SPI-1). A discrete region of the Salmonella enterica genome that encodes several genes associated with pathogenesis, including one of its type III secretion systems.
- Rho-family GTPases
-
A family of low molecular weight signalling proteins with intrinsic GTPase activity that regulate several cellular processes.
- Macropinocytosis
-
A process by which cells can take up extracellular material.
- Guanine nucleotide exchange factors
-
(GEFs). Proteins that can activate GTPases by stimulating the release of GDP to allow the binding of GTP.
- Inflammasome
-
A cytoplasmic signalling platform that leads to the activation of caspase 1 or caspase 11 and the subsequent stimulation of inflammation.
- Pyroptosis
-
A form of cell death that leads to inflammation.
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Galán, J.E. Salmonella Typhimurium and inflammation: a pathogen-centric affair. Nat Rev Microbiol 19, 716–725 (2021). https://doi.org/10.1038/s41579-021-00561-4
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DOI: https://doi.org/10.1038/s41579-021-00561-4
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