Intermediate filaments enable pathogen docking to trigger type 3 effector translocation

Nature Microbiology

Volumn 1, Issue 4, 2016, Pages

  Russo, Brian C ^a,b   Stamm, Luisa M ^a,b,e   Raaben, Matthijs ^b,f   Kim, Caleb M ^a   Kahoud, Emily ^a   Robinson, Lindsey R ^b   Bose, Sayantan ^b   Queiroz, Ana L ^a   Herrera, Bobby Brooke ^a,g   Baxt, Leigh A ^a,b   Mor Vaknin, Nirit ^c   Fu, Yang ^a   Molina, Gabriel ^a   Markovitz, David M ^c   Whelan, Sean P ^b   Goldberg, Marcia B ^a,b,d  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d Gilead Sciences ^*  (United States)

^e GILEAD SCIENCES   (United States)

^f NETHERLANDS CANCER INSTITUTE   (Netherlands)

^g HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; CYTOKERATIN 18; IPAC PROTEIN, SHIGELLA; PROTEIN BINDING; VIMENTIN; VIRULENCE FACTOR;

ANIMAL; BACTERIUM ADHERENCE; CELL LINE; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN TRANSPORT; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SHIGELLA FLEXNERI; TYPE III SECRETION SYSTEM; YERSINIA PSEUDOTUBERCULOSIS;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL ADHESION; CELL LINE; HOST-PATHOGEN INTERACTIONS; HUMANS; KERATIN-18; MICE; PROTEIN BINDING; PROTEIN TRANSPORT; SALMONELLA TYPHIMURIUM; SHIGELLA FLEXNERI; TYPE III SECRETION SYSTEMS; VIMENTIN; VIRULENCE FACTORS; YERSINIA PSEUDOTUBERCULOSIS;

EID: 85040936917     PISSN: None     EISSN: 20585276     Source Type: Journal    
DOI: 10.1038/NMICROBIOL.2016.25     Document Type: Article

References (69)

1. Galan, J. E., Lara-Tejero, M., Marlovits, T. C. & Wagner, S. Bacterial type III secretion systems: Specialized nanomachines for protein delivery into target cells. Annu. Rev. Microbiol. 68, 415-438 (2014).
2. Galan, J. E. & Wolf-Watz, H. Protein delivery into eukaryotic cells by type III secretion machines. Nature 444, 567-573 (2006).
3. Cheung, M. et al. Three-dimensional electron microscopy reconstruction and cysteine-mediated crosslinking provide a model of the type III secretion system needle tip complex. Mol. Microbiol. 95, 31-50 (2015).
4. Kubori, T. et al. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280, 602-605 (1998).
5. Menard, R., Sansonetti, P. & Parsot, C. The secretion of the Shigella flexneri Ipa invasins is activated by epithelial cells and controlled by IpaB and IpaD. EMBO J. 13, 5293-5302 (1994).
6. Veenendaal, A. K. et al. The type III secretion system needle tip complex mediates host cell sensing and translocon insertion. Mol. Microbiol. 63, 1719-1730 (2007).
7. Blocker, A. et al. The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J. Cell Biol. 147, 683-693 (1999).
8. Kenjale, R. et al. The needle component of the type III secreton of Shigella regulates the activity of the secretion apparatus. J. Biol. Chem. 280, 42929-42937 (2005).
9. Meghraoui, A., Schiavolin, L. & Allaoui, A. Single amino acid substitutions on the needle tip protein IpaD increased Shigella virulence. Microbes Infect. 16, 532-539 (2014).
10. Schiavolin, L. et al. Functional insights into the Shigella type III needle tip IpaD in secretion control and cell contact. Mol. Microbiol. 88, 268-282 (2013).
11. Stamm, L. M. & Goldberg, M. B. Microbiology. Establishing the secretion hierarchy. Science 331, 1147-1148 (2011).
12. Lara-Tejero, M., Kato, J., Wagner, S., Liu, X. & Galan, J. E. A sorting platform determines the order of protein secretion in bacterial type III systems. Science 331, 1188-1191 (2011).
13. Misselwitz, B. et al. Salmonella enterica serovar Typhimurium binds to HeLa cells via Fim-mediated reversible adhesion and irreversible type three secretion system 1-mediated docking. Infect. Immun. 79, 330-341 (2011).
14. Lara-Tejero, M. & Galan, J. E. Salmonella enterica serovar typhimurium pathogenicity island 1-encoded type III secretion system translocases mediate intimate attachment to nonphagocytic cells. Infect. Immun. 77, 2635-2642 (2009).
15. Nhieu, G. T. & Sansonetti, P. J. Mechanism of Shigella entry into epithelial cells. Curr. Opin. Microbiol. 2, 51-55 (1999).
16. Ogawa, M. & Sasakawa, C. Intracellular survival of Shigella. Cell. Microbiol. 8, 177-184 (2006).
17. Tran Van Nhieu, G., Ben-Ze’ev, A. & Sansonetti, P. J. Modulation of bacterial entry into epithelial cells by association between vinculin and the Shigella IpaA invasin. EMBO J. 16, 2717-2729 (1997).
18. Mounier, J. et al. Rho family GTPases control entry of Shigella flexneri into epithelial cells but not intracellular motility. J. Cell Sci. 112(Pt 13), 2069-2080 (1999).
19. Handa, Y. et al. Shigella IpgB1 promotes bacterial entry through the ELMODock180 machinery. Nature Cell Biol. 9, 121-128 (2007).
20. Hachani, A. et al. IpgB1 and IpgB2, two homologous effectors secreted via the Mxi-Spa type III secretion apparatus, cooperate to mediate polarized cell invasion and inflammatory potential of Shigella flexenri. Microbes Infect. 10, 260-268 (2008).
21. Garza-Mayers, A. C., Miller, K. A., Russo, B. C., Nagda, D. V. & Goldberg, M. B. Shigella flexneri regulation of ARF6 activation during bacterial entry via an IpgD-mediated positive feedback loop. MBio 6, e02584 (2015).
22. Carette, J. E. et al. Haploid genetic screens in human cells identify host factors used by pathogens. Science 326, 1231-1235 (2009).
23. Carette, J. E. et al. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 477, 340-343 (2011).
24. Bernardini, M. L., Mounier, J., d’Hauteville, H., Coquis-Rondon, M. & Sansonetti, P. J. Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra- and intercellular spread through interaction with F-actin. Proc. Natl Acad. Sci. USA 86, 3867-3871 (1989).
25. Ivaska, J., Pallari, H. M., Nevo, J. & Eriksson, J. E. Novel functions of vimentin in cell adhesion, migration, and signalling. Exp. Cell Res. 313, 2050-2062 (2007).
26. Eriksson, J. E. et al. Introducing intermediate filaments: From discovery to disease. J. Clin. Invest. 119, 1763-1771 (2009).
27. Mor-Vaknin, N. et al. Murine colitis is mediated by vimentin. Sci. Rep. 3, 1045 (2013).
28. Colucci-Guyon, E. et al. Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell 79, 679-694 (1994).
29. Chu, P. G. & Weiss, L. M. Keratin expression in human tissues and neoplasms. Histopathology 40, 403-439 (2002).
30. Jepson, M. A., Mason, C. M., Bennett, M. K., Simmons, N. L. & Hirst, B. H. Coexpression of vimentin and cytokeratins in M cells of rabbit intestinal lymphoid follicle-associated epithelium. Histochem. J. 24, 33-39 (1992).
31. Leube, R. E., Moch, M. & Windoffer, R. Intermediate filaments and the regulation of focal adhesion. Curr. Opin. Cell Biol. 32, 13-20 (2015).
32. Mor-Vaknin, N., Punturieri, A., Sitwala, K. & Markovitz, D. M. Vimentin is secreted by activated macrophages. Nature Cell Biol. 5, 59-63 (2003).
33. Zou, Y., He, L. & Huang, S. H. Identification of a surface protein on human brain microvascular endothelial cells as vimentin interacting with Escherichia coli invasion protein IbeA. Biochem. Biophys. Res. Commun. 351, 625-630 (2006).
34. Picking, W. L. et al. Identification of functional regions within invasion plasmid antigen C (IpaC) of Shigella flexneri. Mol. Microbiol. 39, 100-111 (2001).
35. Harrington, A. et al. Characterization of the interaction of single tryptophan containing mutants of IpaC from Shigella flexneri with phospholipid membranes. Biochemistry 45, 626-636 (2006).
36. Kuwae, A. et al. Shigella invasion of macrophage requires the insertion of IpaC into the host plasma membrane. Functional analysis of IpaC. J. Biol. Chem. 276, 32230-32239 (2001).
37. Scherer, C. A., Cooper, E. & Miller, S. I. The Salmonella type III secretion translocon protein SspC is inserted into the epithelial cell plasma membrane upon infection. Mol. Microbiol. 37, 1133-1145 (2000).
38. Carlson, S. A., Omary, M. B. & Jones, B. D. Identification of cytokeratins as accessory mediators of Salmonella entry into eukaryotic cells. Life Sci. 70, 1415-1426 (2002).
39. Schmitz, A. M., Morrison, M. F., Agunwamba, A. O., Nibert, M. L. & Lesser, C. F. Protein interaction platforms: Visualization of interacting proteins in yeast. Nature Methods 6, 500-502 (2009).
40. Terry, C. M. et al. The C-terminus of IpaC is required for effector activities related to Shigella invasion of host cells. Microb. Pathog. 45, 282-289 (2008).
41. Kwuan, L., Adams, W. & Auerbuch, V. Impact of host membrane pore formation by the Yersinia pseudotuberculosis type III secretion system on the macrophage innate immune response. Infect. Immun. 81, 905-914 (2013).
42. Viboud, G. I. & Bliska, J. B. Measurement of pore formation by contactdependent type III protein secretion systems. Methods Enzymol. 358, 345-350 (2002).
43. Viboud, G. I. & Bliska, J. B. A bacterial type III secretion system inhibits actin polymerization to prevent pore formation in host cell membranes. EMBO J. 20, 5373-5382 (2001).
44. Reeves, A. Z. et al. Engineering Escherichia coli into a protein delivery system for mammalian cells. ACS Synth. Biol. 4, 644-654 (2015).
45. Vanaja, S. K., Rathinam, V. A. & Fitzgerald, K. A. Mechanisms of inflammasome activation: Recent advances and novel insights. Trends Cell Biol. 25, 308-315 (2015).
46. Shi, J. et al. Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514, 187-192 (2014).
47. Dos Santos, G. et al. Vimentin regulates activation of the NLRP3 inflammasome. Nature Commun. 6, 6574 (2015).
48. Batchelor, M. et al. Involvement of the intermediate filament protein cytokeratin-18 in actin pedestal formation during EPEC infection. EMBO Rep. 5, 104-110 (2004).
49. Campbell-Valois, F. X. et al. A fluorescent reporter reveals on/off regulation of the Shigella type III secretion apparatus during entry and cell-to-cell spread. Cell Host Microbe 15, 177-189 (2014).
50. Picking, W. L. et al. IpaD of Shigella flexneri is independently required for regulation of Ipa protein secretion and efficient insertion of IpaB and IpaC into host membranes. Infect. Immun. 73, 1432-1440 (2005).
51. Roehrich, A. D., Guillossou, E., Blocker, A. J. & Martinez-Argudo, I. Shigella IpaD has a dual role: Signal transduction from the type III secretion system needle tip and intracellular secretion regulation. Mol. Microbiol. 87, 690-706 (2013).
52. Labrec, E. H., Schneider, H., Magnani, T. J. & Formal, S. B. Epithelial cell penetration as an essential step in the pathogenesis of bacillary dysentery. J. Bacteriol. 88, 1503-1518 (1964).
53. Maurelli, A. T., Baudry, B., d’Hauteville, H., Hale, T. L. & Sansonetti, P. J. Cloning of plasmid DNA sequences involved in invasion of HeLa cells by Shigella flexneri. Infect. Immun. 49, 164-171 (1985).
54. Menard, R., Sansonetti, P. J. & Parsot, C. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J. Bacteriol. 175, 5899-5906 (1993).
55. Russo, B. C. et al. A Francisella tularensis locus required for spermine responsiveness is necessary for virulence. Infect. Immun. 79, 3665-3676 (2011).
56. Labigne-Roussel, A. F., Lark, D., Schoolnik, G. & Falkow, S. Cloning and expression of an afimbrial adhesin (AFA-I) responsible for P blood groupindependent, mannose-resistant hemagglutination from a pyelonephritic Escherichia coli strain. Infect. Immun. 46, 251-259 (1984).
57. Carette, J. E. et al. Global gene disruption in human cells to assign genes to phenotypes by deep sequencing. Nature Biotechnol. 29, 542-546 (2011).
58. Reimand, J., Arak, T. & Vilo, J. g:Profiler-a web server for functional interpretation of gene lists (2011 update). Nucleic Acids Res. 39, W307-W315 (2011).
59. Heindl, J. E., Saran, I., Yi, C. R., Lesser, C. F. & Goldberg, M. B. Requirement for formin-induced actin polymerization during spread of Shigella flexneri. Infect. Immun. 78, 193-203 (2010).
60. Costa, S. C. & Lesser, C. F. A multifunctional region of the Shigella type 3 effector IpgB1 is important for secretion from bacteria and membrane targeting in eukaryotic cells. PLoS ONE 9, e93461 (2014).
61. Bahrani, F. K., Sansonetti, P. J. & Parsot, C. Secretion of Ipa proteins by Shigella flexneri: Inducer molecules and kinetics of activation. Infect. Immun. 65, 4005-4010 (1997).
62. Soyer, M. & Dumenil, G. A laminar-flow chamber assay for measuring bacterial adhesion under shear stress. Methods Mol. Biol. 799, 185-195 (2012).
63. Mikaty, G. et al. Extracellular bacterial pathogen induces host cell surface reorganization to resist shear stress. PLoS Pathog. 5, e1000314 (2009).
64. Moreau-Marquis, S. et al. The ΔF508-CFTR mutation results in increased biofilm formation by Pseudomonas aeruginosa by increasing iron availability. Am. J. Physiol. Lung Cell. Mol. Physiol. 295, L25-L37 (2008).
65. Muller, N. F. et al. Trimeric autotransporter adhesin-dependent adherence of Bartonella henselae, Bartonella quintana, and Yersinia enterocolitica to matrix components and endothelial cells under static and dynamic flow conditions. Infect. Immun. 79, 2544-2553 (2011).
66. Yi, C. R. et al. Systematic analysis of bacterial effector-postsynaptic density 95/disc large/zonula occludens-1 (PDZ) domain interactions demonstrates Shigella OspE protein promotes protein kinase C activation via PDLIM proteins. J. Biol. Chem. 289, 30101-30113 (2014).
67. Costa, S. C. et al. A new means to identify type 3 secreted effectors: Functionally interchangeable class IB chaperones recognize a conserved sequence. MBio 3, e00243-11 (2012).
68. Baxt, L. A. & Goldberg, M. B. Host and bacterial proteins that repress recruitment of LC3 to Shigella early during infection. PLoS ONE 9, e94653 (2014).
69. Sievers, F. & Higgins, D. G. Clustal omega. Curr. Protoc. Bioinformatics 48, 3.13.11-13.13.16 (2014).