The virulence domain of Shigella IcsA contains a subregion with specific host cell adhesion function
Autoři:
Jilong Qin aff001; Matthew Thomas Doyle aff001; Elizabeth Ngoc Hoa Tran aff001; Renato Morona aff001
Působiště autorů:
School of Biological Sciences, Department of Molecular & Biomedical Sciences, Research Centre for Infectious Diseases, University of Adelaide, Adelaide, Australia
aff001
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0227425
Souhrn
Shigella species cause bacillary dysentery, especially among young individuals. Shigellae target the human colon for invasion; however, the initial adhesion mechanism is poorly understood. The Shigella surface protein IcsA, in addition to its role in actin-based motility, acts as a host cell adhesin through unknown mechanism(s). Here we confirmed the role of IcsA in cell adhesion and defined the region required for IcsA adhesin activity. Purified IcsA passenger domain was able block S. flexneri adherence and was also used as a molecular probe that recognised multiple components from host cells. The region within IcsA’s functional passenger domain (aa 138–148) was identified by mutagenesis. Upon the deletion of this region, the purified IcsAΔ138–148 was found to no longer block S. flexneri adherence and had reduced ability to interact with host molecules. Furthermore, S. flexneri expressing IcsAΔ138–148 was found to be significantly defective in both cell adherence and invasion. Taken together, our data identify an adherence region within the IcsA functional domain and provides useful information for designing therapeutics for Shigella infection.
Klíčová slova:
Adhesins – Centrifugation – HeLa cells – Host cells – Nitrocellulose – Shigella – Shigella flexneri – Shigellosis
Zdroje
1. Speelman P, Kabir I, Islam M. Distribution and spread of colonic lesions in shigellosis: a colonoscopic study. J Infect Dis. 1984;150(6):899–903. Epub 1984/12/01. doi: 10.1093/infdis/150.6.899 6501931.
2. Good RC, May BD, Kawatomari T. Enteric pathogens in monkeys. J Bacteriol. 1969;97(3):1048–55. Epub 1969/03/01. 4180466; PubMed Central PMCID: PMC249813.
3. Kotloff KL, Riddle MS, Platts-Mills JA, Pavlinac P, Zaidi AKM. Shigellosis. Lancet. 2018;391(10122):801–12. Epub 2017/12/20. doi: 10.1016/S0140-6736(17)33296-8 29254859.
4. Kozyreva VK, Jospin G, Greninger AL, Watt JP, Eisen JA, Chaturvedi V. Recent outbreaks of shigellosis in California caused by two distinct populations of Shigella sonnei with either increased virulence or fluoroquinolone resistance. Msphere. 2016;1(6). Epub 2016/12/29. doi: 10.1128/mSphere.00344-16 28028547; PubMed Central PMCID: PMC5177732.
5. Anand BS, Malhotra V, Bhattacharya SK, Datta P, Datta D, Sen D, et al. Rectal histology in acute bacillary dysentery. Gastroenterology. 1986;90(3):654–60. Epub 1986/03/01. doi: 10.1016/0016-5085(86)91120-0 3510937.
6. Wassef JS, Keren DF, Mailloux JL. Role of M cells in initial antigen uptake and in ulcer formation in the rabbit intestinal loop model of shigellosis. Infect Immun. 1989;57(3):858–63. Epub 1989/03/01. 2645214; PubMed Central PMCID: PMC313189.
7. Ranganathan S, Doucet M, Grassel CL, Delaine-Elias B, Zachos NC, Barry EM. Evaluating Shigella flexneri pathogenesis in the human enteroid model. Infect Immun. 2019;87(4). Epub 2019/01/16. doi: 10.1128/IAI.00740-18 30642900; PubMed Central PMCID: PMC6434113.
8. Arena ET, Campbell-Valois FX, Tinevez JY, Nigro G, Sachse M, Moya-Nilges M, et al. Bioimage analysis of Shigella infection reveals targeting of colonic crypts. Proc Natl Acad Sci U S A. 2015;112(25):E3282–90. Epub 2015/06/10. doi: 10.1073/pnas.1509091112 26056271; PubMed Central PMCID: PMC4485126.
9. Brotcke-Zumsteg A, Goosmann C, Brinkmann V, Morona R, Zychlinsky A. IcsA is a Shigella flexneri adhesin regulated by the type III secretion system and required for pathogenesis. Cell Host Microbe. 2014;15(4):435–45. doi: 10.1016/j.chom.2014.03.001 24721572
10. Emsley P, Charles IG, Fairweather NF, Isaacs NW. Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature. 1996;381(6577):90–2. Epub 1996/05/02. doi: 10.1038/381090a0 8609998.
11. Charbonneau ME, Janvore J, Mourez M. Autoprocessing of the Escherichia coli AIDA-I autotransporter: a new mechanism involving acidic residues in the junction region. J Biol Chem. 2009;284(25):17340–51. Epub 2009/04/29. doi: 10.1074/jbc.M109.010108 19398552; PubMed Central PMCID: PMC2719369.
12. Heras B, Totsika M, Peters KM, Paxman JJ, Gee CL, Jarrott RJ, et al. The antigen 43 structure reveals a molecular Velcro-like mechanism of autotransporter-mediated bacterial clumping. Proc Natl Acad Sci U S A. 2014;111(1):457–62. Epub 2013/12/18. doi: 10.1073/pnas.1311592111 24335802; PubMed Central PMCID: PMC3890832.
13. Doyle MT, Tran EN, Morona R. The passenger-associated transport repeat promotes virulence factor secretion efficiency and delineates a distinct autotransporter subtype. Mol Microbiol. 2015;97(2):315–29. Epub 2015/04/15. doi: 10.1111/mmi.13027 25869731.
14. Doyle MT, Grabowicz M, Morona R. A small conserved motif supports polarity augmentation of Shigella flexneri IcsA. Microbiology. 2015;161(11):2087–97. Epub 2015/09/01. doi: 10.1099/mic.0.000165 26315462.
15. Kuhnel K, Diezmann D. Crystal structure of the autochaperone region from the Shigella flexneri autotransporter IcsA. J Bacteriol. 2011;193(8):2042–5. Epub 2011/02/22. doi: 10.1128/JB.00790-10 21335457; PubMed Central PMCID: PMC3133035.
16. Leupold S, Busing P, Mas PJ, Hart DJ, Scrima A. Structural insights into the architecture of the Shigella flexneri virulence factor IcsA/VirG and motifs involved in polar distribution and secretion. J Struct Biol. 2017;198(1):19–27. Epub 2017/03/08. doi: 10.1016/j.jsb.2017.03.003 28268178.
17. Goldberg MB, Barzu O, Parsot C, Sansonetti PJ. Unipolar localization and ATPase activity of IcsA, a Shigella flexneri protein involved in intracellular movement. Infect Agents Dis. 1993;2(4):210–1. Epub 1993/08/01. 8173795.
18. Goldberg MB, Theriot JA. Shigella flexneri surface protein IcsA is sufficient to direct actin-based motility. Proc Natl Acad Sci U S A. 1995;92(14):6572–6. Epub 1995/07/03. doi: 10.1073/pnas.92.14.6572 7604035; PubMed Central PMCID: PMC41560.
19. Teh MY, Morona R. Identification of Shigella flexneri IcsA residues affecting interaction with N-WASP, and evidence for IcsA-IcsA co-operative interaction. PloS one. 2013;8(2):e55152. Epub 2013/02/14. doi: 10.1371/journal.pone.0055152 23405119; PubMed Central PMCID: PMC3566212.
20. Suzuki T, Sasakawa C. N-WASP is an important protein for the actin-based motility of Shigella flexneri in the infected epithelial cells. Jpn J Med Sci Biol. 1998;51 Suppl:S63–8. Epub 1999/04/22. doi: 10.7883/yoken1952.51.supplement1_s63 10211437.
21. Suzuki T, Mimuro H, Suetsugu S, Miki H, Takenawa T, Sasakawa C. Neural Wiskott-Aldrich syndrome protein (N-WASP) is the specific ligand for Shigella VirG among the WASP family and determines the host cell type allowing actin-based spreading. Cell Microbiol. 2002;4(4):223–33. Epub 2002/04/16. doi: 10.1046/j.1462-5822.2002.00185.x 11952639.
22. Egile C, Loisel TP, Laurent V, Li R, Pantaloni D, Sansonetti PJ, et al. Activation of the CDC42 effector N-WASP by the Shigella flexneri IcsA protein promotes actin nucleation by Arp2/3 complex and bacterial actin-based motility. J Cell Biol. 1999;146(6):1319–32. Epub 1999/09/24. doi: 10.1083/jcb.146.6.1319 10491394; PubMed Central PMCID: PMC2156126.
23. Koseoglu VK, Hall CP, Rodriguez-Lopez EM, Agaisse H. The autotransporter IcsA promotes Shigella flexneri biofilm formation in the presence of bile salts. Infect Immun. 2019;87(7):e00861–18. Epub 2019/04/17. doi: 10.1128/IAI.00861-18 30988059; PubMed Central PMCID: PMC6589070.
24. May KL, Morona R. Mutagenesis of the Shigella flexneri autotransporter IcsA reveals novel functional regions involved in IcsA biogenesis and recruitment of host neural Wiscott-Aldrich syndrome protein. J Bacteriol. 2008;190(13):4666–76. Epub 2008/05/06. doi: 10.1128/JB.00093-08 18456802; PubMed Central PMCID: PMC2446779.
25. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A. 2000;97(12):6640–5. Epub 2000/06/01. doi: 10.1073/pnas.120163297 10829079; PubMed Central PMCID: PMC18686.
26. Sambrook J, Russell DW. The inoue method for preparation and transformation of competent E. Coli: "ultra-competent" cells. CSH Protoc. 2006;2006(1). Epub 2006/01/01. doi: 10.1101/pdb.prot3944 22485385.
27. Tartoff KD, Hobbs CA. Improved media for growing plasmid and cosmid clones. Bethesda Research Laboratories Focus. 1987;9(12).
28. Van den Bosch L, Manning PA, Morona R. Regulation of O-antigen chain length is required for Shigella flexneri virulence. Mol Microbiol. 1997;23(4):765–75. Epub 1997/02/01. doi: 10.1046/j.1365-2958.1997.2541625.x 9157247.
29. Lugtenberg B, Meijers J, Peters R, van der Hoek P, van Alphen L. Electrophoretic resolution of the ‘major outer membrane protein’ of Escherichia coli K12 into four bands. FEBS Lett. 1975;58(1–2):254–8. doi: 10.1016/0014-5793(75)80272-9
30. May KL, Grabowicz M, Polyak SW, Morona R. Self-association of the Shigella flexneri IcsA autotransporter protein. Microbiology. 2012;158(Pt 7):1874–83. Epub 2012/04/21. doi: 10.1099/mic.0.056465-0 22516224.
31. Suzuki T, Miki H, Takenawa T, Sasakawa C. Neural Wiskott-Aldrich syndrome protein is implicated in the actin-based motility of Shigella flexneri. The EMBO journal. 1998;17(10):2767–76. Epub 1998/06/10. doi: 10.1093/emboj/17.10.2767 9582270; PubMed Central PMCID: PMC1170617.
32. Laarmann S, Schmidt MA. The Escherichia coli AIDA autotransporter adhesin recognizes an integral membrane glycoprotein as receptor. Microbiology. 2003;149(Pt 7):1871–82. Epub 2003/07/12. doi: 10.1099/mic.0.26264-0 12855738.
33. Papayannopoulos V, Co C, Prehoda KE, Snapper S, Taunton J, Lim WA. A polybasic motif allows N-WASP to act as a sensor of PIP(2) density. Mol Cell. 2005;17(2):181–91. Epub 2005/01/25. doi: 10.1016/j.molcel.2004.11.054 15664188.
34. Roy A, Kucukural A, Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc. 2010;5(4):725–38. Epub 2010/04/03. doi: 10.1038/nprot.2010.5 20360767; PubMed Central PMCID: PMC2849174.
35. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, et al. UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem. 2004;25(13):1605–12. Epub 2004/07/21. doi: 10.1002/jcc.20084 15264254.
36. Weinrauch Y, Drujan D, Shapiro SD, Weiss J, Zychlinsky A. Neutrophil elastase targets virulence factors of enterobacteria. Nature. 2002;417(6884):91–4. Epub 2002/05/23. doi: 10.1038/417091a 12018205.
37. Pope LM, Reed KE, Payne SM. Increased protein secretion and adherence to HeLa cells by Shigella spp. following growth in the presence of bile salts. Infect Immun. 1995;63(9):3642–8. Epub 1995/09/01. 7642302; PubMed Central PMCID: PMC173505.
38. Magdalena J, Goldberg MB. Quantification of Shigella IcsA required for bacterial actin polymerization. Cell Motil Cytoskel. 2002;51(4):187–96. Epub 2002/04/27. doi: 10.1002/cm.10024 11977093.
39. Tiwari V, Liu J, Valyi-Nagy T, Shukla D. Anti-heparan sulfate peptides that block herpes simplex virus infection in vivo. J Biol Chem. 2011;286(28):25406–15. Epub 2011/05/21. doi: 10.1074/jbc.M110.201103 21596749; PubMed Central PMCID: PMC3137111.
40. Rose L, Shivshankar P, Hinojosa E, Rodriguez A, Sanchez CJ, Orihuela CJ. Antibodies against PsrP, a novel Streptococcus pneumoniae adhesin, block adhesion and protect mice against pneumococcal challenge. J Infect Dis. 2008;198(3):375–83. Epub 2008/05/30. doi: 10.1086/589775 18507531.
41. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, Sasakawa C. Escape of intracellular Shigella from autophagy. Science. 2005;307(5710):727–31. Epub 2004/12/04. doi: 10.1126/science.1106036 15576571.
42. Zhao WD, Liu DX, Wei JY, Miao ZW, Zhang K, Su ZK, et al. Caspr1 is a host receptor for meningitis-causing Escherichia coli. Nat Commun. 2018;9(1):2296. Epub 2018/06/14. doi: 10.1038/s41467-018-04637-3 29895952; PubMed Central PMCID: PMC5997682.
43. Perez-Zsolt D, Erkizia I, Pino M, Garcia-Gallo M, Martin MT, Benet S, et al. Anti-Siglec-1 antibodies block Ebola viral uptake and decrease cytoplasmic viral entry. Nat Microbiol. 2019;4(9):1558–70. Epub 2019/06/05. doi: 10.1038/s41564-019-0453-2 31160823.
44. Amerighi F, Valeri M, Donnarumma D, Maccari S, Moschioni M, Taddei A, et al. Identification of a monoclonal antibody against pneumococcal pilus 1 ancillary protein impairing bacterial adhesion to human epithelial cells. J Infect Dis. 2016;213(4):516–22. Epub 2015/09/25. doi: 10.1093/infdis/jiv461 26401026.
45. Koseoglu VK, Agaisse H. Evolutionary perspectives on the moonlighting functions of bacterial factors that support actin-based motility. MBio. 2019;10(4). Epub 2019/08/29. doi: 10.1128/mBio.01520-19 31455648; PubMed Central PMCID: PMC6712393.
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