1,809
Views
1
CrossRef citations to date
0
Altmetric
Research Paper

Epithelial talin-1 protects mice from Citrobacter rodentium-induced colitis by restricting bacterial crypt intrusion and enhancing T cell immunity

, , , , , , , , , , , & ORCID Icon show all
Article: 2192623 | Received 22 Aug 2022, Accepted 13 Mar 2023, Published online: 23 Mar 2023

References

  • Allaire JM, Crowley SM, Law HT, Chang S-Y, Ko H-J, Vallance BA. The intestinal epithelium: central coordinator of mucosal immunity. Trends Immunol. 2018;39(9):677–20. PMID: 29716793. doi:10.1016/j.it.2018.04.002.
  • Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, et al. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet. 2013;382(9888):209–222. PMID: 23680352. doi:10.1016/S0140-6736(13)60844-2.
  • Pakbin B, Brück WM, Rossen JWA. Virulence factors of enteric pathogenic Escherichia coli: a review. Int J Mol Sci. 2021;22(18):9922. PMID: 34576083. doi:10.3390/ijms22189922.
  • Nataro JP, Kaper JB. Diarrheagenic Escherichia coli. Clin Microbiol Rev. 1998;11(1):142–201. PMID: 9457432. doi:10.1128/CMR.11.1.142.
  • Collins JW, Keeney KM, Crepin VF, Rathinam VAK, Fitzgerald KA, Finlay BB, Frankel G. Citrobacter rodentium: infection, inflammation and the microbiota. Nat Rev Microbiol. 2014;12(9):612–623. PMID: 25088150. doi:10.1038/nrmicro3315.
  • Freeman NL, Zurawski DV, Chowrashi P, Ayoob JC, Huang L, Mittal B, Sanger JM, Sanger JW. Interaction of the enteropathogenic Escherichia coli protein, translocated intimin receptor (Tir), with focal adhesion proteins. Cell Motil Cytoskeleton. 2000;47(4):307–318. PMID: 11093251. doi:10.1002/1097-0169(200012)47:4<307:AID-CM5>3.0.CO;2-Q.
  • Goosney DL, DeVinney R, Finlay BB. Recruitment of cytoskeletal and signaling proteins to enteropathogenic and enterohemorrhagic Escherichia coli pedestals. Infect Immun. 2001;69(5):3315–3322. PMID: 11292754. doi:10.1128/IAI.69.5.3315-3322.2001.
  • Burridge K, Connell L. A new protein of adhesion plaques and ruffling membranes. J Cell Biol. 1983;97:359–367. PMID: 6684120. doi:10.1083/jcb.97.2.359.
  • Critchley DR. Biochemical and structural properties of the integrin-associated cytoskeletal protein talin. Annu Rev Biophys. 2009;38(1):235–254. PMID: 19416068. doi:10.1146/annurev.biophys.050708.133744.
  • Kukkurainen S, Azizi L, Zhang P, Jacquier M-C, Baikoghli M, von Essen M, Tuukkanen A, Laitaoja M, Liu X, Rahikainen R, et al. The F1 loop of the talin head domain acts as a gatekeeper in integrin activation and clustering. J Cell Sci. 2020;133(19):jcs239202. PMID: 33046605. doi:10.1242/jcs.239202.
  • Elliott PR, Goult BT, Kopp PM, Bate N, Grossmann JG, Roberts GCK, Critchley DR, Barsukov IL. The Structure of the talin head reveals a novel extended conformation of the FERM domain. Structure. 2010;18:1289–1299. PMID: 20947018. doi:10.1016/j.str.2010.07.011.
  • Bosanquet DC, Ye L, Harding KG, Jiang WG. FERM family proteins and their importance in cellular movements and wound healing. Int J Mol Med. 2014;34(1):3–12. PMID: 24820650. doi:10.3892/ijmm.2014.1775.
  • Calderwood DA, Zent R, Grant R, Rees DJG, Hynes RO, Ginsberg MH. The talin head domain binds to integrin β subunit cytoplasmic tails and regulates integrin activation. J Biol Chem. 1999;274(40):28071–28074. PMID: 10497155. doi:10.1074/jbc.274.40.28071.
  • Vinogradova O, Velyvis A, Velyviene A, Hu B, Haas TA, Plow EF, Qin J. A structural mechanism of integrin αIIbβ3 “inside-out” activation as regulated by its cytoplasmic face. Cell. 2002;110:587–597. PMID: 12230976. doi:10.1016/s0092-8674(02)00906-6.
  • Tadokoro S, Shattil SJ, Eto K, Tai V, Liddington RC, de Pereda JM, Ginsberg MH, Calderwood DA. Talin binding to integrin ß tails: a final common step in integrin activation. Science. 2003;302(5642):103–106. 1979 PMID: 14526080. doi:10.1126/science.1086652.
  • Kopp PM, Bate N, Hansen TM, Brindle NPJ, Praekelt U, Debrand E, Coleman S, Mazzeo D, Goult BT, Gingras AR, et al. Studies on the morphology and spreading of human endothelial cells define key inter-and intramolecular interactions for talin1. Eur J Cell Biol. 2010;89(9):661–673. PMID: 20605055. doi:10.1016/j.ejcb.2010.05.003.
  • Zhang X, Jiang G, Cai Y, Monkley SJ, Critchley DR, Sheetz MP. Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nat Cell Biol. 2008;10(9):1062–1068. PMID: 19160486. doi:10.1038/ncb1765.
  • Giannone G, Jiang G, Sutton DH, Critchley DR, Sheetz MP. Talin1 is critical for force-dependent reinforcement of initial integrin–cytoskeleton bonds but not tyrosine kinase activation. J Cell Biol. 2003;163(2):409–419. PMID: 14581461. doi:10.1083/jcb.200302001.
  • Finlay BB, Rosenshine I, Donnenberg MS, Kaper JB. Cytoskeletal composition of attaching and effacing lesions associated with enteropathogenic Escherichia coli adherence to HeLa cells. Infect Immun. 1992;60(6):2541–2543. PMID: 1587620. doi:10.1128/iai.60.6.2541-2543.1992.
  • Cantarelli VV, Takahashi A, Yanagihara I, Akeda Y, Imura K, Kodama T, Kono G, Sato Y, Honda T. Talin, a host cell protein, interacts directly with the translocated intimin receptor, Tir, of enteropathogenic Escherichia coli, and is essential for pedestal formation. Cell Microbiol. 2001;3(11):745–751. PMID: 11696034. doi:10.1046/j.1462-5822.2001.00156.x.
  • Singh K, Al-Greene NT, Verriere TG, Coburn LA, Asim M, Barry DP, Allaman MM, Hardbower DM, Delgado AG, Piazuelo MB, et al. The L-arginine transporter solute carrier family 7 member 2 mediates the immunopathogenesis of attaching and effacing bacteria. PLoS Pathog. 2016;12(10):e1005984. PMID: 27783672. doi:10.1371/journal.ppat.1005984.
  • Petrich BG, Marchese P, Ruggeri ZM, Spiess S, Weichert RAM, Ye F, Tiedt R, Skoda RC, Monkley SJ, Critchley DR, et al. Talin is required for integrin-mediated platelet function in hemostasis and thrombosis. J Exp Med. 2007;204(13):3103–3111. PMID: 18086863. doi:10.1084/jem.20071800.
  • Mathew S, Palamuttam RJ, Mernaugh G, Ramalingam H, Lu Z, Zhang M-Z, Ishibe S, Critchley DR, Fässler R, Pozzi A, et al. Talin regulates integrin β1-dependent and -independent cell functions in ureteric bud development. Development. 2017;144:4148–4158. PMID: 28993400. doi:10.1242/dev.149914.
  • Rutlin M, Rastelli D, Kuo WT, Estep JA, Louis A, Riccomagno MM, Turner JR, Rao M. The Villin1 gene promoter drives Cre recombinase expression in extraintestinal tissues. Cell Mol Gastroenterol Hepatol. 2020;10(4):864. PMID: 32464312. doi:10.1016/j.jcmgh.2020.05.009.
  • Whitehead RH, VanEeden PE, Noble MD, Ataliotis P, Jat PS. Establishment of conditionally immortalized epithelial cell lines from both colon and small intestine of adult H-2Kb-tsA58 transgenic mice. Proc Natl Acad Sci. 1993;90:587–591. PMID: 7678459. doi:10.1073/pnas.90.2.587.
  • Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676–682. PMID: 22743772. doi:10.1038/nmeth.2019.
  • Gobert AP, Finley JL, Latour YL, Asim M, Smith TM, Verriere TG, Barry DP, Allaman MM, Delagado AG, Rose KL. Hypusination orchestrates the antimicrobial response of macrophages. Cell Rep. 2020;33(11):108510. PMID: 33326776. doi:10.1016/j.celrep.2020.108510.
  • Gobert AP, Al-Greene NT, Singh K, Coburn LA, Sierra JC, Verriere TG, Luis PB, Schneider C, Asim M, Allaman MM. Distinct immunomodulatory effects of spermine oxidase in colitis induced by epithelial injury or infection. Front Immunol. 2018;9:1242. PMID: 29922289. doi:10.3389/fimmu.2018.01242.
  • Singh K, Al-Greene NT, Verriere TG, Coburn LA, Asim M, Barry DP, Allaman MM, Hardbower DM, Delgado AG, Piazuelo MB, et al. The L-arginine transporter solute carrier family 7 member 2 mediates the immunopathogenesis of attaching and effacing bacteria. PLoS Pathog. 2016;12(10):e1005984. PMID: 27783672. doi:10.1371/journal.ppat.1005984.
  • Gobert AP, Cheng Y, Akhtar M, Mersey BD, Blumberg DR, Cross RK, Chaturvedi R, Drachenberg CB, Boucher J-L, Hacker A, et al. Protective role of arginase in a mouse model of colitis. J Immunol. 2004;173(3):2109 LP–2117. 2109. PMID. doi:10.4049/jimmunol.173.3.
  • Eisenberg T, Abdellatif M, Zimmermann A, Schroeder S, Pendl T, Harger A, Stekovic S, Schipke J, Magnes C, Schmidt A, et al. Dietary spermidine for lowering high blood pressure. Autophagy. 2017;13(4):767–769. PMID. doi:10.1080/15548627.2017.1280225.
  • Luperchio SA, Schauer DB. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect. 2001;3(4):333–340. PMID: 11334751. doi:10.1016/s1286-4579(01)01387-9.
  • Watson AJM, Hughes KR. TNF-α-induced intestinal epithelial cell shedding: implications for intestinal barrier function. Ann N Y Acad Sci. 2012;1258(1):1–8. PMID: 22731709. doi:10.1111/j.1749-6632.2012.06523.x.
  • Wang P, Ballestrem C, Streuli CH. The C terminus of talin links integrins to cell cycle progression. J Cell Biol. 2011;195:499–513. PMID: 22042621. doi:10.1083/jcb.201104128.
  • Campellone KG, Rankin S, Pawson T, Kirschner MW, Tipper DJ, Leong JM. Clustering of Nck by a 12-residue Tir phosphopeptide is sufficient to trigger localized actin assembly. J Cell Biol. 2004;164(3):407–416. PMID: 14757753. doi:10.1083/jcb.200306032.
  • Deng W, Vallance BA, Li Y, Puente JL, Finlay BB. Citrobacter rodentium translocated intimin receptor (Tir) is an essential virulence factor needed for actin condensation, intestinal colonization and colonic hyperplasia in mice. Mol Microbiol. 2003;48(1):95–115. PMID: 12657048. doi:10.1046/j.1365-2958.2003.03429.x.
  • Barker N, van de Wetering M, Clevers H. The intestinal stem cell. Genes Dev. 2008;22(14):1856–1864. PMID: 18628392. doi:10.1101/gad.1674008.
  • Lopez CA, Miller BM, Rivera-Chávez F, Velazquez EM, Byndloss MX, Chávez-Arroyo A, Lokken KL, Tsolis RM, Winter SE, Bäumler AJ. Virulence factors enhance Citrobacter rodentium expansion through aerobic respiration. Sci. 2016;353:1249–1253. 1979 PMID: 27634526. doi:10.1126/science.aag3042.
  • Kaemmerer E, Kuhn P, Schneider U, Clahsen T, Jeon MK, Klaus C, Andruszkow J, Härer M, Ernst S, Schippers A. Beta-7 integrin controls enterocyte migration in the small intestine. World J Gastroenterol: WJG. 2015;21(6):1759. PMID: 25684940. doi:10.3748/wjg.v21.i6.1759.
  • Parker A, Maclaren OJ, Fletcher AG, Muraro D, Kreuzaler PA, Byrne HM, Maini PK, Watson AJM, Pin C. Cell proliferation within small intestinal crypts is the principal driving force for cell migration on villi. FASEB J. 2017;31:636–649. PMID: 27811059. doi:10.1096/fj.201601002.
  • Rankin CR, Hilgarth RS, Leoni G, Kwon M, Ka DB, Parkos CA, Nusrat A. Annexin A2 regulates β1 integrin internalization and intestinal epithelial cell migration. J Biol Chem. 2013;288(21):15229–15239. PMID: 23558678. doi:10.1074/jbc.M112.440909.
  • Silberger DJ, Zindl CL, Weaver CT. Citrobacter rodentium: a model enteropathogen for understanding the interplay of innate and adaptive components of type 3 immunity. Mucosal Immunol. 2017;10(5):1108–1117. PMID: 28612839. doi:10.1038/mi.2017.47.
  • Khan MA, Ma C, Knodler LA, Valdez Y, Rosenberger CM, Deng W, Finlay BB, Vallance BA. Toll-like receptor 4 contributes to colitis development but not to host defense during Citrobacter rodentium infection in mice. Infect Immun. 2006;74(5):2522–2536. PMID: 16622187. doi:10.1128/IAI.74.5.2522-2536.2006.
  • Vallance BA, Deng W, Knodler LA, Finlay BB. Mice lacking T and B lymphocytes develop transient colitis and crypt hyperplasia yet suffer impaired bacterial clearance during Citrobacter rodentium infection. Infect Immun. 2002;70(4):2070–2081. PMID: 11895973. doi:10.1128/IAI.70.4.2070-2081.2002.
  • Chan JM, Bhinder G, Sham HP, Ryz N, Huang T, Bergstrom KS, Vallance BA, Bäumler AJ. CD4+ T cells drive goblet cell depletion during Citrobacter rodentium infection. Infect Immun. 2013;81(12):4649–4658. PMID: 24101690. doi:10.1128/IAI.00655-13.
  • Zheng Y, Valdez PA, Danilenko DM, Hu Y, Sa SM, Gong Q, Abbas AR, Modrusan Z, Ghilardi N, de Sauvage FJ, et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med. 2008;14(3):282–289. PMID: 18264109. doi:10.1038/nm1720.
  • Basu R, O’quinn DB, Silberger DJ, Schoeb TR, Fouser L, Ouyang W, Hatton RD, Weaver CT. Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria. Immunity. 2012;37:1061–1075. PMID: 23200827. doi:10.1016/j.immuni.2012.08.024.
  • Zindl CL, Witte SJ, Laufer VA, Gao M, Yue Z, Janowski KM, Cai B, Frey BF, Silberger DJ, Harbour SN, et al. A nonredundant role for T cell-derived interleukin 22 in antibacterial defense of colonic crypts. Immunity. 2022;55(3):494–511.e11. PMID: 35263568. doi:10.1016/j.immuni.2022.02.003.