3,292
Views
6
CrossRef citations to date
0
Altmetric
Research Paper

Salmonella effector SopF regulates PANoptosis of intestinal epithelial cells to aggravate systemic infection

, , , , , , & show all
Article: 2180315 | Received 05 Oct 2022, Accepted 08 Feb 2023, Published online: 20 Feb 2023

References

  • Bakkeren E, Huisman JS, Fattinger SA, Hausmann A, Furter M, Egli A, Slack E, Sellin ME, Bonhoeffer S, Regoes RR, et al. Salmonella persisters promote the spread of antibiotic resistance plasmids in the gut. Nature. 2019;573(7773):276–18. doi:10.1038/s41586-019-1521-8.
  • Keestra-Gounder AM, Tsolis RM, Baumler AJ. Now you see me, now you don’t: the interaction of Salmonella with innate immune receptors. Nat Rev Microbiol. 2015;13(4):206–216. doi:10.1038/nrmicro3428.
  • Raffatellu M, Wilson RP, Chessa D, Andrews-Polymenis H, Tran QT, Lawhon S, Khare S, Adams LG, Baumler AJ, Rauch I, et al. SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica Serotype Typhimurium invasion of epithelial cells. Infect Immun. 2005;73(1):146–154. doi:10.1128/IAI.73.1.146-154.2005.
  • Lian H, Jiang K, Tong M, Chen Z, Liu X, Galan JE, Gao X. The Salmonella effector protein SopD targets Rab8 to positively and negatively modulate the inflammatory response. Nat Microbiol. 2021;6:658–671. doi:10.1038/s41564-021-00866-3.
  • Fattinger SA, Sellin ME, Hardt WD. Salmonella effector driven invasion of the gut epithelium: breaking in and setting the house on fire. Curr Opin Microbiol. 2021;64:9–18. doi:10.1016/j.mib.2021.08.007.
  • McGhie EJ. Cooperation between actin-binding proteins of invasive Salmonella: sipA potentiates SipC nucleation and bundling of actin. EMBO J. 2001;20(9):2131–2139. doi:10.1093/emboj/20.9.2131.
  • Zhou D, Mooseker MS, Galan JE. Role of the S. typhimurium Actin-Binding protein SipA in bacterial internalization. Science. 1999;283(5410):2092–2095. doi:10.1126/science.283.5410.2092.
  • Demeter A, Jacomin AC, Gul L, Lister A, Lipscombe J, Invernizzi R, Branchu P, Macaulay I, Nezis IP, Kingsley RA, et al. Computational prediction and experimental validation of Salmonella Typhimurium SopE-mediated fine-tuning of autophagy in intestinal epithelial cells. Front Cell Infect Microbiol. 2022;12:834895. doi:10.3389/fcimb.2022.834895.
  • Lau N, Haeberle AL, O’Keeffe BJ, Latomanski EA, Celli J, Newton HJ, Knodler LA. SopF, a phosphoinositide binding effector, promotes the stability of the nascent Salmonella-containing vacuole. PLoS Pathog. 2019;15(7):e1007959. doi:10.1371/journal.ppat.1007959.
  • Xu Y, Zhou P, Cheng S, Lu Q, Nowak K, Hopp AK, Li L, Shi X, Zhou Z, Gao W, et al. A bacterial effector reveals the V-ATPase-ATG16L1 axis that initiates xenophagy. Cell. 2019;178(3):552–566 e520. doi:10.1016/j.cell.2019.06.007.
  • Cheng S, Wang L, Liu Q, Qi L, Yu K, Wang Z, Wu M, Liu Y, Fu J, Hu M, et al. Identification of a novel Salmonella type III effector by quantitative secretome profiling. Mol Cell Proteomics. 2017;16(12):2219–2228. doi:10.1074/mcp.RA117.000230.
  • Fattinger SA, Sellin ME, Hardt WD. Epithelial inflammasomes in the defense against Salmonella gut infection. Curr Opin Microbiol. 2021;59:86–94. doi:10.1016/j.mib.2020.09.014.
  • Fattinger SA, Geiser P, Samperio Ventayol P, Di Martino ML, Furter M, Felmy B, Bakkeren E, Hausmann A, Barthel-Scherrer M, Gul E, et al. Epithelium-autonomous NAIP/NLRC4 prevents TNF-driven inflammatory destruction of the gut epithelial barrier in Salmonella-infected mice. Mucosal Immunol. 2021;14(3):615–629. doi:10.1038/s41385-021-00381-y.
  • Hausmann A, Bock D, Geiser P, Berthold DL, Fattinger SA, Furter M, Bouman JA, Barthel-Scherrer M, Lang CM, Bakkeren E, et al. Intestinal epithelial NAIP/NLRC4 restricts systemic dissemination of the adapted pathogen Salmonella Typhimurium due to site-specific bacterial PAMP expression. Mucosal Immunol. 2020;13(3):530–544. doi:10.1038/s41385-019-0247-0.
  • Rauch I, Deets KA, Dx J, von Moltke J, Tenthorey JL, Lee AY, Philip NH, Ayres JS, Brodsky IE, Gronert K, et al. NAIP-NLRC4 inflammasomes coordinate intestinal epithelial cell expulsion with eicosanoid and IL-18 release via activation of Caspase-1 and −8. Immunity. 2017;46(4):649–659. doi:10.1016/j.immuni.2017.03.016.
  • Sellin ME, Muller AA, Felmy B, Dolowschiak T, Diard M, Tardivel A, Maslowski KM, Hardt WD. Epithelium-intrinsic NAIP/NLRC4 inflammasome drives infected enterocyte expulsion to restrict Salmonella replication in the intestinal mucosa. Cell Host Microbe. 2014;16(2):237–248. doi:10.1016/j.chom.2014.07.001.
  • Broz P. Getting Rid of the bad apple: inflammasome-induced extrusion of Salmonella -infected enterocytes. Cell Host Microbe. 2014;16(2):153–155. doi:10.1016/j.chom.2014.07.010.
  • Samperio Ventayol P, Geiser P, Di Martino ML, Florbrant A, Fattinger SA, Walder N, Sima E, Shao F, Gekara NO, Sundbom M, et al. Bacterial detection by NAIP/NLRC4 elicits prompt contractions of intestinal epithelial cell layers. Proc Natl Acad Sci U S A. 2021;118. doi:10.1073/pnas.2013963118.
  • Hefele M, Stolzer I, Ruder B, He GW, Mahapatro M, Wirtz S, Neurath MF, Gunther C. Intestinal epithelial Caspase-8 signaling is essential to prevent necroptosis during Salmonella Typhimurium induced enteritis. Mucosal Immunol. 2018;11(4):1191–1202. doi:10.1038/s41385-018-0011-x.
  • Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol. 2010;11(10):700–714. doi:10.1038/nrm2970.
  • Orning P, Weng D, Starheim K, Ratner D, Best Z, Lee B, Brooks A, Xia S, Wu H, Kelliher MA, et al. Pathogen blockade of TAK1 triggers caspase-8-dependent cleavage of gasdermin D and cell death. Science. 2018;362(6418):1064–1069. doi:10.1126/science.aau2818.
  • Oberst A, Dillon CP, Weinlich R, McCormick LL, Fitzgerald P, Pop C, Hakem R, Salvesen GS, Green DR. Catalytic activity of the Caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature. 2011;471(7338):363–367. doi:10.1038/nature09852.
  • Zuo H, Chen C, Ma L, Min QX, Shen YH. Caspase-8 knockdown suppresses apoptosis, while induces autophagy and chemo-sensitivity in non-small cell lung cancer cells. Am J Transl Res. 2020;12:6478–6489.
  • Newton K, Wickliffe KE, Dugger DL, Maltzman A, Roose-Girma M, Dohse M, Komuves L, Webster JD, Dixit VM. Cleavage of RIPK1 by Caspase-8 is crucial for limiting apoptosis and necroptosis. Nature. 2019;574(7778):428–431. doi:10.1038/s41586-019-1548-x.
  • Young MM, Takahashi Y, Khan O, Park S, Hori T, Yun J, Sharma AK, Amin S, Hu CD, Zhang J, et al. Autophagosomal membrane serves as platform for intracellular death-inducing signaling complex (iDISC)-mediated caspase-8 activation and apoptosis. J Biol Chem. 2012;287(15):12455–12468. doi:10.1074/jbc.M111.309104.
  • Yang ZH, Wu XN, He P, Wang X, Wu J, Ai T, Zhong CQ, Wu X, Cong Y, Zhu R, et al. A Non-canonical PDK1-RSK signal diminishes pro-Caspase-8-mediated necroptosis blockade. Mol Cell. 2020;80(2):296–310 e296. doi:10.1016/j.molcel.2020.09.004.
  • Barthel M, Hapfelmeier S, Quintanilla-Martinez L, Kremer M, Rohde M, Hogardt M, Pfeffer K, Russmann H, Hardt WD. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium Colitis model that Allows analysis of both pathogen and host. Infect Immun. 2003;71(5):2839–2858. doi:10.1128/iai.71.5.2839-2858.2003.
  • Millar AD, Rampton DS, Chander CL, Claxson AW, Blades S, Coumbe A, Panetta J, Morris CJ, Blake DR. Evaluating the antioxidant potential of new treatments for inflammatory bowel disease using a rat model of colitis. Gut. 1996;39(3):407–415. doi:10.1136/gut.39.3.407.
  • Zhang J, Yu Q, Jiang D, Yu K, Yu W, Chi Z, Chen S, Li M, Yang D, Wang Z, et al. Epithelial Gasdermin D shapes the host-microbial interface by driving mucus layer formation. Sci Immunol. 2022;7(68):eabk2092. doi:10.1126/sciimmunol.abk2092.
  • Naseer N, Zhang J, Bauer R, Constant DA, Nice TJ, Brodsky IE, Rauch I, Shin S, Raffatellu M. Salmonella enterica Serovar Typhimurium induces NAIP/NLRC4- and NLRP3/ASC-independent, Caspase-4-dependent inflammasome activation in human intestinal epithelial cells. Infect Immun. 2022;90(7):e0066321. doi:10.1128/iai.00663-21.
  • Place DE, Lee S, Kanneganti TD. PANoptosis in microbial infection. Curr Opin Microbiol. 2021;59:42–49. doi:10.1016/j.mib.2020.07.012.
  • Tan G, Huang C, Chen J, Chen B, Zhi F. Gasdermin-E-mediated pyroptosis participates in the pathogenesis of Crohn’s disease by promoting intestinal inflammation. Cell Rep. 2021;35(11):109265. doi:10.1016/j.celrep.2021.109265.
  • Co JY, Margalef-Catala M, Li X, Mah AT, Kuo CJ, Monack DM, Amieva MR. Controlling epithelial polarity: a human enteroid model for host-pathogen interactions. Cell Rep. 2019;26(9):2509–2520 e2504. doi:10.1016/j.celrep.2019.01.108.
  • Fritsch M, Gunther SD, Schwarzer R, Albert MC, Schorn F, Werthenbach JP, Schiffmann LM, Stair N, Stocks H, Seeger JM, et al. Caspase-8 is the molecular switch for apoptosis, necroptosis and pyroptosis. Nature. 2019;575(7784):683–687. doi:10.1038/s41586-019-1770-6.
  • Zhu J, Huang JW, Tseng PH, Yang YT, Fowble J, Shiau CW, Shaw YJ, Kulp SK, Chen CS. From the cyclooxygenase-2 inhibitor celecoxib to a novel class of 3-phosphoinositide-dependent protein kinase-1 inhibitors. Cancer Res. 2004;64(12):4309–4318. doi:10.1158/0008-5472.CAN-03-4063.
  • Houles T, Roux PP. Defining the role of the RSK isoforms in cancer. Semin Cancer Biol. 2018;48:53–61. doi:10.1016/j.semcancer.2017.04.016.
  • Chen D, Burford WB, Pham G, Zhang L, Alto LT, Ertelt JM, Winter MG, Winter SE, Way SS, Alto NM. Systematic reconstruction of an effector-gene network reveals determinants of Salmonella cellular and tissue tropism. Cell Host Microbe. 2021;29(10):1531–1544 e1539. doi:10.1016/j.chom.2021.08.012.
  • Fulde M, van Vorst K, Zhang K, Westermann AJ, Busche T, Huei YC, Welitschanski K, Froh I, Pagelow D, Plendl J, et al. SPI2 T3SS effectors facilitate enterocyte apical to basolateral transmigration of Salmonella-containing vacuoles in vivo. Gut Microbes. 2021;13(1):1973836. doi:10.1080/19490976.2021.1973836.
  • Ma S, Liu X, Ma S, Jiang L. SopA inactivation or reduced expression is selected in intracellular Salmonella and contributes to systemic Salmonella infection. Res Microbiol. 2021;172(2):103795. doi:10.1016/j.resmic.2020.103795.
  • Zuo L, Zhou L, Wu C, Wang Y, Li Y, Huang R, Wu S. Salmonella spvC gene inhibits pyroptosis and intestinal inflammation to aggravate systemic infection in mice. Front Microbiol. 2020;11:562491. doi:10.3389/fmicb.2020.562491.
  • Knodler LA, Vallance BA, Celli J, Winfree S, Hansen B, Montero M, Steele-Mortimer O. Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia. Proc Natl Acad Sci U S A. 2010;107(41):17733–17738. doi:10.1073/pnas.1006098107.
  • Geiser P, Di Martino ML, Samperio Ventayol P, Eriksson J, Sima E, Al-Saffar AK, Ahl D, Phillipson M, Webb DL, Sundbom M, et al. Salmonella enterica Serovar Typhimurium exploits cycling through epithelial cells to colonize human and murine enteroids. mBio. 2021;12. doi:10.1128/mBio.02684-20.
  • Wotzka SY, Nguyen BD, Hardt WD. Salmonella Typhimurium diarrhea reveals basic principles of enteropathogen infection and disease-promoted DNA exchange. Cell Host Microbe. 2017;21(4):443–454. doi:10.1016/j.chom.2017.03.009.
  • Galan JE. Salmonella Typhimurium and inflammation: a pathogen-centric affair. Nat Rev Microbiol. 2021;19(11):716–725. doi:10.1038/s41579-021-00561-4.
  • Lee BL, Mirrashidi KM, Stowe IB, Kummerfeld SK, Watanabe C, Haley B, Cuellar TL, Reichelt M, Kayagaki N. ASC- and caspase-8-dependent apoptotic pathway diverges from the NLRC4 inflammasome in macrophages. Sci Rep. 2018;8(1):3788. doi:10.1038/s41598-018-21998-3.
  • Van Opdenbosch N, Van Gorp H, Verdonckt M, Saavedra PHV, de Vasconcelos NM, Goncalves A, Vande Walle L, Demon D, Matusiak M, Van Hauwermeiren F, et al. Caspase-1 engagement and TLR-Induced c-FLIP expression suppress ASC/Caspase-8-dependent apoptosis by inflammasome sensors NLRP1b and NLRC4. Cell Rep. 2017;21(12):3427–3444. doi:10.1016/j.celrep.2017.11.088.
  • Dong K, Zhu Y, Deng Q, Sun L, Yang S, Huang K, Cao Y, Li Y, Wu S, Huang R. Salmonella pSLT-encoded effector SpvB promotes RIPK3-dependent necroptosis in intestinal epithelial cells. Cell Death Discov. 2022;8(1):44. doi:10.1038/s41420-022-00841-9.
  • Lin HH, Chen HL, Weng CC, Janapatla RP, Chen CL, Chiu CH. Activation of apoptosis by Salmonella pathogenicity island-1 effectors through both intrinsic and extrinsic pathways in Salmonella-infected macrophages. J Microbiol Immunol Infect. 2021;54(4):616–626. doi:10.1016/j.jmii.2020.02.008.
  • Newson JPM, Scott NE, Yeuk Wah Chung I, Wong Fok Lung T, Giogha C, Gan J, Wang N, Strugnell RA, Brown NF, Cygler M, et al. Salmonella effectors SseK1 and SseK3 target death domain proteins in the TNF and TRAIL signaling pathways. Mol Cell Proteomics. 2019;18(6):1138–1156. doi:10.1074/mcp.RA118.001093.
  • Gunster RA, Matthews SA, Holden DW, Thurston TLM. SseK1 and SseK3 type III secretion system effectors inhibit NF-κB signaling and necroptotic cell death in Salmonella-infected macrophages. Infect Immun. 2017:85. doi:10.1128/IAI.00010-17.
  • Han JH, Park J, Kang TB, Lee KH. Regulation of Caspase-8 activity at the crossroads of pro-inflammation and anti-inflammation. Int J Mol Sci. 2021;23(1):22. doi:10.3390/ijms22073318.
  • Hu GQ, Yang YJ, Qin XX, Qi S, Zhang J, Yu SX, Du CT, Chen W. Salmonella outer protein B suppresses colitis development via protecting cell from necroptosis. Front Cell Infect Microbiol. 2019;9:87. doi:10.3389/fcimb.2019.00087.
  • 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:10.1080/21505594.2018.1509664.
  • Hu GQ, Song PX, Chen W, Qi S, Yu SX, Du CT, Deng XM, Ouyang HS, Yang YJ. Critical role for Salmonella effector SopB in regulating inflammasome activation. Mol Immunol. 2017;90:280–286. doi:10.1016/j.molimm.2017.07.011.
  • Levina A, Fleming KD, Burke JE, Leonard TA. Activation of the essential kinase PDK1 by phosphoinositide-driven trans-autophosphorylation. Nat Commun. 2022;13(1):1874. doi:10.1038/s41467-022-29368-4.
  • Alfonso M, David K, Daan MF, Dario RA. PDK1, the master regulator of AGC kinase signal transduction. Semin Cell Dev Biol. 2004;15(2):161–170. doi:10.1016/j.semcdb.2003.12.022.
  • Qu Y, Misaghi S, Izrael-Tomasevic A, Newton K, Gilmour LL, Lamkanfi M, Louie S, Kayagaki N, Liu J, Komuves L, et al. Phosphorylation of NLRC4 is critical for inflammasome activation. Nature. 2012;490(7421):539–542. doi:10.1038/nature11429.
  • Mauvezin C, Neufeld TP. Bafilomycin A1 disrupts autophagic flux by inhibiting both V-ATPase-dependent acidification and Ca-P60A/SERCA-dependent autophagosome-lysosome fusion. Autophagy. 2015;11(8):1437–1438. doi:10.1080/15548627.2015.1066957.
  • Wu S, Shen Y, Zhang S, Xiao Y, Shi S. Salmonella interacts with autophagy to offense or defense. Front Microbiol. 2020;11:721. doi:10.3389/fmicb.2020.00721.
  • Mandal R, Barron JC, Kostova I, Becker S, Strebhardt K. Caspase-8: the double-edged sword. Biochim Biophys Acta Rev Cancer. 2020;1873(2):188357. doi:10.1016/j.bbcan.2020.188357.
  • Choi CY, Vo MT, Nicholas J, Choi YB. Autophagy-competent mitochondrial translation elongation factor TUFM inhibits Caspase-8-mediated apoptosis. Cell Death Differ. 2022;29(2):451–464. doi:10.1038/s41418-021-00868-y.
  • Nenci A, Becker C, Wullaert A, Gareus R, van Loo G, Danese S, Huth M, Nikolaev A, Neufert C, Madison B, et al. Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature. 2007;446(7135):557–561. doi:10.1038/nature05698.