Bacterial internalization, localization, and effectors shape the epithelial immune response during Shigella flexneri infection

Infection and Immunity

Volumn 83, Issue 9, 2015, Pages 3624-3637

  Lippmann, Juliane ^a   Gwinner, Frederik ^a,c   Rey, Camille ^a   Tamir, Uyanga ^a,b   Law, Helen K W ^a,d   Schwikowski, Benno ^a   Enninga, Jost ^a  

^a INSTITUT PASTEUR   (France)

^b PRINCETON UNIVERSITY   (United States)

^c INSERM   (France)

^d HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; CXCL2 CHEMOKINE; CYCLIN DEPENDENT KINASE INHIBITOR 1A; GENTAMICIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 6; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE; X BOX BINDING PROTEIN 1;

APOPTOSIS; ARTICLE; AUTOPHAGY; BACTERIAL TRANSLOCATION; BYSTANDER EFFECT; CACO 2 CELL LINE; CELL SHAPE; CELLULAR DISTRIBUTION; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INTERNALIZATION; LIPID METABOLISM; MULTIGENE FAMILY; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SHIGELLA FLEXNERI; SHIGELLOSIS; SIGNAL TRANSDUCTION; SINGLE CELL ANALYSIS; TYPE III SECRETION SYSTEM; FLOW CYTOMETRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC TRANSFECTION; IMMUNOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

DYSENTERY, BACILLARY; FLOW CYTOMETRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HELA CELLS; HUMANS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SHIGELLA FLEXNERI; TRANSFECTION;

EID: 84939558037     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00574-15     Document Type: Article

References (33)

1. Vance RE, Isberg RR, Portnoy DA. 2009. Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6:10-21. http://dx.doi.org/10.1016/j.chom.2009.06.007.
2. Randow F, MacMicking JD, James LC. 2013. Cellular self-defense: how cell-autonomous immunity protects against pathogens. Science 340:701-706. http://dx.doi.org/10.1126/science.1233028.
3. Takeuchi O, Akira S. 2010. Pattern recognition receptors and inflammation. Cell 140:805-820. http://dx.doi.org/10.1016/j.cell.2010.01.022.
4. Blander JM, Sander LE. 2012. Beyond pattern recognition: five immune checkpoints for scaling the microbial threat. Nat Rev Immunol 12:215-225. http://dx.doi.org/10.1038/nri3167.
5. Buchrieser C, Glaser P, Rusniok C, Nedjari H, de Hauteville H, Kunst F, Sansonetti P, Parsot C. 2000. The virulence plasmid pWR100 and the repertoire of proteins secreted by the type III secretion apparatus of Shigella flexneri. Mol Microbiol 38:760-771. http://dx.doi.org/10.1046/j.1365-2958.2000.02179.x.
6. Le Gall T, Mavris M, Martino MC, Bernardini ML, Denamur E, Parsot C. 2005. Analysis of virulence plasmid gene expression defines three classes of effectors in the type III secretion system of Shigella flexneri. Microbiology 151:951-962. http://dx.doi.org/10.1099/mic.0.27639-0.
7. Ehsani S, Santos JC, Rodrigues CD, Henriques R, Audry L, Zimmer C, Sansonetti P, Van Nhieu GT, Enninga J. 2012. Hierarchies of host factor dynamics at the entry site of Shigella flexneri during host cell invasion. Infect Immun 80:2548-2557. http://dx.doi.org/10.1128/IAI.06391-11.
8. Ray K, Bobard A, Danckaert A, Paz-Haftel I, Clair C, Ehsani S, Tang C, Sansonetti P, Van Nhieu GT, Enninga J. 2010. Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time. Cell Microbiol 12:545-556. http://dx.doi.org/10.1111/j.1462-5822.2010.01428.x.
9. Pendaries C, Tronchère H, Arbibe L, Mounier J, Gozani O, Cantley L, Fry MJ, Gaits-Iacovoni F, Sansonetti PJ, Payrastre B. 2006. PtdIns5P activates the host cell PI3-kinase/Akt pathway during Shigella flexneri infection. EMBO J 25:1024-1034. http://dx.doi.org/10.1038/sj.emboj.7601001.
10. Puhar A, Tronchère H, Payrastre B, Van Nhieu GT, Sansonetti PJ. 2013. A Shigella effector dampens inflammation by regulating epithelial release of danger signal ATP through production of the lipid mediator PtdIns5P. Immunity 39:1121-1131. http://dx.doi.org/10.1016/j.immuni.2013.11.013.
11. Pruneda JN, Smith FD, Daurie A, Swaney DL, Villén J, Scott JD, Stadnyk AW, Le Trong I, Stenkamp RE, Klevit RE, Rohde JR, Brzovic PS. 2014. E2~Ub conjugates regulate the kinase activity of Shigella effector OspG during pathogenesis. EMBO J 33:437-449. http://dx.doi.org/10.1002/embj.201386386.
12. Zhou Y, Dong N, Hu L, Shao F. 2013. The Shigella type three secretion system effector OspG directly and specifically binds to host ubiquitin for activation. PLoS One 8:e57558. http://dx.doi.org/10.1371/journal.pone.0057558.
13. Arbibe L, Kim DW, Batsche E, Pedron T, Mateescu B, Muchardt C, Parsot C, Sansonetti PJ. 2007. An injected bacterial effector targets chromatin access for transcription factor NF-κB to alter transcription of host genes involved in immune responses. Nat Immunol 8:47-56. http://dx.doi.org/10.1038/ni1423.
14. Li H, Xu H, Zhou Y, Zhang J, Long C, Li S, Chen S, Zhou JM, Shao F. 2007. The phosphothreonine lyase activity of a bacterial type III effector family. Science 315:1000-1003. http://dx.doi.org/10.1126/science.1138960.
15. Ablasser A, Schmid-Burgk JL, Hemmerling I, Horvath GL, Schmidt T, Latz E, Hornung V. 2013. Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature 503:530-534. http://dx.doi.org/10.1038/nature12640.
16. Kasper CA, Sorg I, Schmutz C, Tschon T, Wischnewski H, Kim ML, Arrieumerlou C. 2010. Cell-cell propagation of NF-κB transcription factor andMAPkinase activation amplifies innate immunity against bacterial infection. Immunity 33:804-816. http://dx.doi.org/10.1016/j.immuni.2010.10.015.
17. Kim DW, Lenzen G, Page A-L, Legrain P, Sansonetti PJ, Parsot C. 2005. The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc Natl Acad Sci U S A 102:14046-14051. http://dx.doi.org/10.1073/pnas.0504466102.
18. Mavris M, Page A-L, Tournebize R, Demers B, Sansonetti P, Parsot C. 2002. Regulation of transcription by the activity of the Shigella flexneri type III secretion apparatus. Mol Microbiol 43:1543-1553. http://dx.doi.org/10.1046/j.1365-2958.2002.02836.x.
19. Allaoui A, Ménard R, Sansonetti PJ, Parsot C. 1993. Characterization of the Shigella flexneri ipgD and ipgF genes, which are located in the proximal part of the mxi locus. Infect Immun 61:1707-1714.
20. Allaoui A, Sansonetti PJ, Parsot C. 1993. MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri lpa invasins. Mol Microbiol 7:59-68. http://dx.doi.org/10.1111/j.1365-2958.1993.tb01097.x.
21. Sorensen M, Lippuner C, Kaiser T, Misslitz A, Aebischer T, Bumann D. 2003. Rapidly maturing red fluorescent protein variants with strongly enhanced brightness in bacteria. FEBS Lett 552:110-114. http://dx.doi.org/10.1016/S0014-5793(03)00856-1.
22. Simeone R, Bobard A, Lippmann J, Bitter W, Majlessi L, Brosch R, Enninga J. 2012. Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog 8:e1002507. http://dx.doi.org/10.1371/journal.ppat.1002507.
23. Tattoli I, Sorbara MT, Vuckovic D, Ling A, Soares F, Carneiro LAM, Yang C, Emili A, Philpott DJ, Girardin SE. 2012. Amino acid starvation induced by invasive bacterial pathogens triggers an innate host defense program. Cell Host Microbe 11:563-575. http://dx.doi.org/10.1016/j.chom.2012.04.012.
24. Pillich H, Loose M, Zimmer KP, Chakraborty T. 2012. Activation of the unfolded protein response by Listeria monocytogenes. Cell Microbiol 14:949-964. http://dx.doi.org/10.1111/j.1462-5822.2012.01769.x.
25. Mostowy S, Sancho-Shimizu V, Hamon MA, Simeone R, Brosch R, Johansen T, Cossart P. 2011. p62 and NDP52 proteins target intracytosolic Shigella and Listeria to different autophagy pathways. J Biol Chem 286:26987-26995. http://dx.doi.org/10.1074/jbc.M111.223610.
26. McDavid A, Finak G, Chattopadyay PK, Dominguez M, Lamoreaux L, Ma SS, Roederer M, Gottardo R. 2013. Data exploration, quality control and testing in single-cell qPCR-based gene expression experiments. Bioinformatics 29:461-467. http://dx.doi.org/10.1093/bioinformatics/bts714.
27. Shalek AK, Satija R, Shuga J, Trombetta JJ, Gennert D, Lu D, Chen P, Gertner RS, Gaublomme JT, Yosef N, Schwartz S, Fowler B, Weaver S, Wang J, Wang X, Ding R, Raychowdhury R, Friedman N, Hacohen N, Park H, May AP, Regev A. 2014. Single-cell RNA-seq reveals dynamic paracrine control of cellular variation. Nature 510:363-369. http://dx.doi.org/10.1038/nature13437.
28. Pizarro-Cerda J, Cossart P. 2006. Bacterial adhesion and entry into host cells. Cell 124:715-727. http://dx.doi.org/10.1016/j.cell.2006.02.012.
29. Casson CN, Copenhaver AM, Zwack EE, Nguyen HT, Strowig T, Javdan B, Bradley WP, Fung TC, Flavell RA, Brodsky IE, Shin S. 2013. Caspase-11 activation in response to bacterial secretion systems that access the host cytosol. PLoS Pathog 9:e1003400. http://dx.doi.org/10.1371/journal.ppat.1003400.
30. Schmutz C, Ahrne E, Kasper CA, Tschon T, Sorg I, Dreier RF, Schmidt A, Arrieumerlou C. 2013. Systems-level overview of host protein phosphorylation during Shigella flexneri infection revealed by phosphoproteomics. Mol Cell Proteomics 12:2952-2968. http://dx.doi.org/10.1074/mcp.M113.029918.
31. Guo G, Huss M, Tong GQ, Wang C, Li Sun L, Clarke ND, Robson P. 2010. Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev Cell 18:675-685. http://dx.doi.org/10.1016/j.devcel.2010.02.012.
32. Dong S, Maiella S, Xhaard A, Pang Y, Wenandy L, Larghero J, Becavin C, Benecke A, Bianchi E, Socié G, Rogge L. 1 July 2013. Multi-parameter single-cell profiling of human CD4+FOXP3+ regulatory T cell populations in homeostatic conditions and during graft-versus-host disease. Blood http://dx.doi.org/10.1182/blood-2013-02-482539.
33. Zopf CJ, Quinn K, Zeidman J, Maheshri N. 2013. Cell-cycle dependence of transcription dominates noise in gene expression. PLoS Comput Biol 9:e1003161. http://dx.doi.org/10.1371/journal.pcbi.1003161.