The inside story of shigella invasion of intestinal epithelial cells

Cold Spring Harbor Perspectives in Medicine

Volumn 3, Issue 10, 2013, Pages

  Carayol, Nathalie ^a,b,c,d   Van Nhieu, Guy Tran ^a,b,c,d  

^a l'alimentation et l'Environnement   (France)

^b INSERM   (France)

^c CNRS   (France)

^d French Federation of Seed Potato Growers   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN;

ADAPTATION; COLON; GENETICS; HUMAN; INTESTINE MUCOSA; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; REVIEW; SHIGELLA; SHIGELLOSIS; VIRULENCE;

ADAPTATION, PHYSIOLOGICAL; BACTERIAL PROTEINS; COLON; DYSENTERY, BACILLARY; HUMANS; INTESTINAL MUCOSA; SHIGELLA; VIRULENCE;

EID: 84885048391     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a016717     Document Type: Article

References (84)

1. Alto NM, Shao F, Lazar CS, Brost RL, Chua G, Mattoo S, McMahon SA, Ghosh P, Hughes TR, Boone C, et al. 2006. Identification of a bacterial typeIII effector family with G protein mimicry functions. Cell 124: 133-145.
2. Arbibe L, Kim DW, Batsche E, Pedron T, Mateescu B, Mu-chardt C, Parsot C, Sansonetti PJ. 2007. An injected bacterial effector targets chromatin access for transcription factor NF-kB to alter transcription of host genes involved in immune responses. Nat Immunol 8: 47-56.
3. Ashida H, Kim M, Schmidt-Supprian M, Ma A, Ogawa M, Sasakawa C. 2010.Abacterial E3 ubiquitin ligase IpaH9.8 targets NEMO/IKKg to dampen the host NF-kB-medi-ated inflammatory response. Nat Cell Biol 12: 66-73.
4. Ashida H, Ogawa M, Kim M, Suzuki S, Sanada T, Punginelli C, Mimuro H, Sasakawa C. 2011. Shigella deploys multiple countermeasures against host innate immune responses. Curr Opin Microbiol 14: 16-23.
5. Bergounioux J, Elisee R, Prunier AL, Donnadieu F, Speran-dio B, Sansonetti P, Arbibe L. 2012. Calpain activation by the Shigellaflexneri effector VirA regulates key steps in the formation and life of the bacterium's epithelial niche. Cell Host Microbe 11: 240-252.
6. Bliven KA, Maurelli AT. 2012. Antivirulence genes: Insights into pathogen evolution through gene loss. Infect Immun 80: 4061-4070.
7. Blocker AJ, Deane JE, Veenendaal AK, Roversi P, Hodgkin-son JL, Johnson S, Lea SM. 2008. What's the point of the type III secretion system needle? Proc Natl Acad Sci 105: 6507-6513.
8. Botteaux A, Sory MP, Biskri L, Parsot C, Allaoui A. 2009. MxiC is secreted by and controls the substrate specificity of the Shigella flexneri type III secretion apparatus. Mol Microbiol 71: 449-460.
9. Bougnéres L, Girardin SE, Weed SA, Karginov AV, Olivo-Marin JC, Parsons JT, Sansonetti PJ, Tran Van Nhieu G. 2004. Cortactin and Crk cooperate to trigger actin polymerization during Shigella invasion of epithelial cells. J Cell Biol 166: 225-235.
10. Bourdet-Sicard R, Rüdiger M, Jockusch BM, Gounon P, Sansonetti PJ, Tran Van Nhieu G. 1999. Binding of the Shigella protein IpaA to vinculin induces F-actin depoly-merization. EMBO J 18: 5853-5862.
11. Bulgin R, Raymond B, Garnett JA, Frankel G, Crepin VF, Berger CN, Arbeloa A. 2010. Bacterial guanine nucleo-tide exchange factors SopE-like and WxxxE effectors. Infect Immun 78: 1417-1425.
12. Burton EA, Plattner R, Pendergast AM. 2003. Abl tyrosine kinases are required for infection by Shigella flexneri. EMBO J 22: 5471-5479.
13. Burton EA, Oliver TN, Pendergast AM. 2005. Abl kinases regulate actin comet tail elongation via an N-WASP-de-pendent pathway. Mol Cell Biol 25: 8834-8843.
14. Carneiro LA, Travassos LH, Soares F, Tattoli I, Magalhaes JG, Bozza MT, Plotkowski MC, Sansonetti PJ, Molkentin JD, Philpott DJ, et al. 2009. Shigella induces mitochondrial dysfunction and cell death in nonmyleoid cells. Cell Host Microbe 5: 123-136.
15. Clair C, Combettes L, Pierre F, Sansonetti P, Tran Van Nhieu G. 2008. Extracellular-loop peptide antibodies reveal a predominant hemichannel organization of connexins in polarized intestinal cells. Exp Cell Res 314: 1250-1265.
16. Cossart P, Sansonetti PJ. 2004. Bacterial invasion: The paradigms of enteroinvasive pathogens. Science 304: 242-248.
17. Del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheetz MP. 2009. Stretching single talin rod molecules activates vinculin binding. Science 323: 638-641.
18. Demali KA, Jue AL, Burridge K. 2006. IpaA targets b1 in-tegrins and r to promote actin cytoskeleton rearrangements necessary for Shigella entry. J Biol Chem 281: 39534-39541.
19. Dickenson NE, Zhang L, Epler CR, Adam PR, Picking WL, Picking WD. 2011. Conformational changes in IpaD from Shigella flexneri upon binding bile salts provide insight into the second step of type III secretion. Biochemistry 50: 172-180.
20. Dong N, Zhu Y, Lu Q, Hu L, Zheng Y, Shao F. 2012. Structurally distinct bacterial TBC-like GAPs link Arf GTPase to Rab1 inactivation to counteract host defenses. Cell 150: 1029-1041.
21. Dorman CJ, McKenna S, Beloin C. 2001. Regulation of virulence gene expression in Shigella flexneri, a facultative intracellular pathogen. Int J Med Microbiol 291: 89-96.
22. Dragoi AM, Talman AM, Agaisse H. 2012. Bruton's tyrosine kinase regulates Shigella flexneri dissemination in HT-29 intestinal cells. Infect Immun 81: 598-607.
23. Duménil G, Sansonetti P, Tran Van Nhieu G. 2000. Src ty-rosine kinase activity down-regulates r-dependent responses during Shigella entry into epithelial cells and stress fibre formation. J Cell Sci 113: 71-80.
24. Dupont N, Lacas-Gervais S, Bertout J, Paz I, Freche B, Tran Van Nhieu G, van der Goot FG, Sansonetti PJ, Lafont F. 2009. Shigella phagocytic vacuolar membrane remnants participate in the cellular response to pathogen invasion and are regulated by autophagy. Cell Host Microbe 6: 137-149.
25. Egile C, Loisel TP, Laurent V, Li R, Pantaloni D, Sansonetti PJ, Carlier MF. 1999. Activation ofthe CDC42 effector N-WASP by the Shigellaflexneri IcsA protein promotes actin nucleation by Arp2/3 complex and bacterial actin-based motility. J Cell Biol 146: 1319-1332.
26. Ehsani S, Santos JC, Rodrigues CD, Henriques R, Audry L, Zimmer C, Sansonetti P, Tran Van Nhieu G, Enninga J. 2012. Hierarchies of host factor dynamics at the entry site of Shigellaflexneri during host cell invasion. Infect Immun 80: 2548-2557.
27. Epler CR, Dickenson NE, Bullitt E, Picking WL. 2012. Ul-trastructural analysis of IpaD at the tip of the nascent MxiH type III secretion apparatus of Shigella flexneri. J Mol Biol 420: 29-39.
28. Fujii T, Cheung M, Blanco A, Kato T, Blocker AJ, Namba K. 2012. Structure of a type III secretion needle at 7-A resolution provides insights into its assembly and signaling mechanisms. Proc Natl Acad Sci 109: 4461-4466.
29. Fukazawa A, Alonso C, Kurachi K, Gupta S, Lesser CF, Mc-Cormick BA, Reinecker HC. 2008. GEF-H1 mediated control ofNOD1 dependent NF-kB activationby Shigella effectors. PLoS Pathog 4: e1000228.
30. Fukumatsu M, Ogawa M, Arakawa S, Suzuki M, Nakayama K, Shimizu S, Kim M, Mimuro H, Sasakawa C. 2012. Shigella targets epithelial tricellular junctions and uses a noncanonical clathrin-dependent endocytic pathway to spread between cells. Cell Host Microbe 11: 325-336.
31. García-Sáez AJ, Buschhorn SB, Keller H, Anderluh G, Simons K, Schwille P. 2011. Oligomerization and pore formation by equinatoxin II inhibit endocytosis and lead to plasma membrane reorganization. J Biol Chem 286: 37768-37777.
32. Hachani A, Biskri L, Rossi G, Marty A, Ménard R, Sansonetti P, Parsot C, Tran Van Nhieu G, Bernardini ML, Allaoui A. 2008. IpgB1 and IpgB2, two homologous effectors secreted via the Mxi-Spatype III secretion apparatus, cooperate to mediate polarized cell invasion and inflammatory potential of Shigella flexenri. Microbes Infect 10: 260-268.
33. Handa Y, Suzuki M, Ohya K, Iwai H, Ishijima N, Koleske AJ, Fukui Y, Sasakawa C. 2007. Shigella IpgB1 promotes bacterial entry through the ELMO-Dock180 machinery. Nat Cell Biol 9: 121-128.
34. Hänisch J, Kölm R, Wozniczka M, Bumann D, Rottner K, Stradal TE. 2011. Activation of a RhoA/myosin II-depen-dent but Arp2/3 complex-independent pathway facilitates Salmonella invasion. Cell Host Microbe 9: 273-285.
35. Harris TJ, Tepass U. 2012. Adherens junctions: From molecules to morphogenesis. Nat Rev Mol Cell Biol 11: 502-514.
36. Hermant D, Ménard R, Arricau N, Parsot C, Popoff MY. 1995. Functional conservation of the Salmonella and Shi-gella effectors of entry into epithelial cells. Mol Microbiol 17: 781-789.
37. Humphreys D, Davidson A, Hume PJ, Koronakis V. 2012. Salmonella virulence effector SopE and Host GEF ARNO cooperate to recruit and activate WAVE to trigger bacterial invasion. Cell Host Microbe 11: 129-139.
38. Izard T, Tran Van Nhieu G, Bois PR. 2006. Shigella applies molecular mimicry to subvert vinculin and invade host cells. J Cell Biol 175: 465-475.
39. Kim DW, Lenzen G, Page AL, 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 102: 14046-14051.
40. Kim M, Ogawa M, Fujita Y, Yoshikawa Y, Nagai T, Koyama T, Nagai S, Lange A, Fässler R, Sasakawa C. 2009. Bacteria hijack integrin-linked kinase to stabilize focal adhesions and block cell detachment. Nature 459: 578-582.
41. Klink BU, Barden S, Heidler TV, Borchers C, Ladwein M, Stradal TE, Rottner K, Heinz DW. 2010. Structure of Shigella IpgB2 in complex with human rA: Implications for the mechanism of bacterial guanine nucleotide exchange factor mimicry. J Biol Chem 285: 17197-17208.
42. Lafont F, Tran Van Nhieu G, Hanada K, Sansonetti P, van der Goot FG. 2002. Initial steps of Shigella infection depend on the cholesterol/sphingolipid raft-mediated CD44-IpaB interaction. EMBO J 21: 4449-4457.
43. Leung Y, Ally S, Goldberg MB. 2008. Bacterial actin assembly requires toca-1 to relieve N-wasp autoinhibition. Cell Host Microbe 3: 39-47.
44. 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.
45. Marteyn B, West NP, Browning DF, Cole JA, Shaw JG, Palm F, Mounier J, Prévost MC, Sansonetti P, Tang CM. 2010. Modulation of Shigella virulence in response to available oxygen in vivo. Nature 465: 355-358.
46. Marteyn B, Gazi A, Sansonetti P. 2012. Shigella: A model of virulence regulation in vivo. Gut Microbes 3: 104-120.
47. Mattëi PJ, Faudry E, Job V, Izoré T, Attree I, Dessen A. 2011. Membrane targeting and pore formation by the type III secretion system translocon. FEBS J 278: 414-426.
48. Mavris M, Sansonetti PJ, Parsot C. 2002. Identification of the cis-acting site involved in activation of promoters regulated by activity of the type III secretion apparatus in Shigella flexneri. J Bacteriol 184: 6751-6759.
49. Mostowy S, Bonazzi M, Hamon MA, Tham TN, Mallet A, Lelek M, Gouin E, Demangel C, Brosch R, Zimmer C, et al. 2010. Entrapment of intracytosolic bacteria by sep-tin cage-like structures. Cell Host Microbe 8: 433-444.
50. Mounier J, Popoff MR, Enninga J, Frame MC, Sansonetti PJ, Tran Van Nhieu G. 2009. The IpaC carboxy terminal effector domain mediates Src-dependent actin polymerization during Shigella invasion of epithelial cells. PLoS Pathog 5: e1000271.
51. Mounier J, Boncompain G, Senerovic L, Lagache T, Chrétien F, Perez F, Kolbe M, Olivo-Marin JC, Sansonetti PJ, Sau-vonnet N. 2012. Shigella effector IpaB-induced cholesterol relocation disrupts the Golgi complex and recycling network to inhibit host cell secretion. Cell Host Microbe 12: 381-389.
52. Mueller CA, Broz P, Cornelis GR. 2008. The type III secretion system tip complex and translocon. Mol Microbiol 68: 1085-1095.
53. Münter S, Way M, Frischknecht F. 2006. Signaling during pathogen infection. Sci STKE 2006: pre5.
54. Newton HJ, Pearson JS, Badea L, Kelly M, Lucas M, Hollo-way G, Wagstaff KM, Dunstone MA, Sloan J, Whisstock JC, et al. 2010. The type III effectors NleE and NleB from enteropathogenic E. Coli and OspZ from Shigella block nuclear translocation of NF-kB p65. PLoS Pathog 6: e1000898.
55. Niebuhr K, Jouihri N, Allaoui A, Gounon P, Sansonetti PJ, Parsot C. 2000. IpgD, a protein secreted by the type III secretion machinery of Shigella flexneri, is chaperoned by IpgE and implicated in entry focus formation. Mol Mi-crobiol 38: 8-19.
56. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, Sasakawa C. 2005. Escape of intracellular Shigella from autophagy. Science 307: 727-731.
57. Orchard RC, Alto NM. 2012. Mimicking GEFs: A common theme for bacterial pathogens. Cell Microbiol 14: 10-18.
58. Parsons JT, Horwitz AR, Schwartz MA. 2010. Cell adhesion: Integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 11: 633-643.
59. Parsot C. 2009. Shigella type III secretion effectors: How, where, when, for what purposes? Curr Opin Microbiol 12: 110-116.
60. Parsot C, Ageron E, Penno C, Mavris M, Jamoussi K, D'Hau-teville H, Sansonetti P, Demers B. 2005. A secreted anti-activator, OspD1, and its chaperone, Spa15, are involved in the control of transcription by the type III secretion apparatus activity in Shigella flexneri. Mol Microbiol 56: 1627-1635.
61. Pendaries C, Tronchère H, Arbibe L, Mounier J, Gozani O, Cantley L, Fry MJ, Gaits-Iacovoni F, Sansonetti PJ, Pay-rastre B. 2006. PtdIns5Pactivatesthe host cell PI3-kinase/ Akt pathway during Shigella flexneri infection. EMBO J 25: 1024-1034.
62. Phalipon A, Sansonetti PJ. 2007. Shigella's ways of manipulating the host intestinal innate and adaptive immune system: A tool box for survival? Immunol Cell Biol 85: 119-129.
63. Plattner R, Kadlec L, DeMali KA, Kazlauskas A, Pendergast AM. 1999. c-Abl is activated by growth factors and Src family kinases and has a role in the cellular response to PDGF. Genes Dev 13: 2400-2411.
64. Prosseda G, Di Martino ML, Campilongo R, Fioravanti R, Micheli G, Casalino M, Colonna B. 2012. Shedding of genes that interfere with the pathogenic lifestyle: The Shigella model. Res Microbiol 163: 399-406.
65. Ramarao N, Le Clainche C, Izard T, Bourdet-Sicard R, Ageron E, Sansonetti PJ, Carlier MF, Tran Van Nhieu G. 2007. Capping of actin filaments by vinculin activated by the Shigella IpaA carboxyl-terminal domain. FEBS Lett 581: 853-857.
66. Rathman M, de Lanerolle P, Ohayon H, Gounon P, Sanso-netti P. 2000. Myosin light chain kinase plays an essential role in S. flexneri dissemination. J Cell Sci 113: 3375-3386.
67. Romero S, Grompone G, Carayol N, Mounier J, Guadagnini S, Prevost MC, Sansonetti PJ, Tran Van Nhieu G. 2011. ATP-mediated Erk1/2 activation stimulates bacterial capture by filopodia, which precedes Shigella invasion of epithelial cells. Cell Host Microbe 9: 508-519.
68. Romero S, Quatela A, Bornschlög T, Guadagnini S, Basser-eau P, Tran Van Nhieu G. 2012. Filopodium retraction is controlled by adhesion to its tip. J Cell Sci 125: 4999-5004.
69. Sanada T, Kim M, Mimuro H, Suzuki M, Ogawa M, Oyama A, Ashida H, Kobayashi T, Koyama T, Nagai S, et al. 2012. The Shigella flexneri effector OspI deamidates UBC13 to dampen the inflammatory response. Nature 483: 623-626.
70. Sansonetti PJ, Phalipon A. 1999. M cells as ports of entry for enteroinvasive pathogens: Mechanisms of interaction, consequences for the disease process. Semin Immunol 11: 193-203.
71. Sansonetti PJ, Mounier J, Prévost MC, Mège RM. 1994. Cadherin expression is required for the spread of Shigella flexneri between epithelial cells. Cell 76: 829-839.
72. Sansonetti PJ, Phalipon A, Arondel J, Thirumalai K, Baner-jee S, Akira S, Takeda K, Zychlinsky A. 2000. Caspase-1 activation of IL-1b and IL-18 are essential for Shigella flexneri-induced inflammation. Immunity 12: 581-590.
73. Schiavolin L, Meghraoui A, Cherradi Y, Biskri L, Botteaux A, Allaoui A. 2013. Functional insights into the Shigella type III needle tip IpaD in secretion control and cell contact. Mol Microbiol 88: 268-282.
74. Schuch R, Sandlin RC, Maurelli AT. 1999. A system for identifying post-invasion functions of invasion genes: Requirements for the Mxi-Spa type III secretion pathway of Shigella flexneri in intercellular dissemination. Mol Microbiol 34: 675-689.
75. Srikanth CV, Wall DM, Maldonado-Contreras A, Shi HN, Zhou D, Demma Z, Mumy KL, McCormick BA. 2010. Salmonella pathogenesis and processing of secreted effectors by caspase-3. Science 330: 390-393.
76. Tran Van Nhieu G, Ben-Ze'Ev A, Sansonetti PJ. 1997. Modulation of bacterial entry into epithelial cells by association between vinculin and the Shigella IpaA invasin. EMBO J 16: 2717-2729.
77. Tran Van Nhieu G, Clair C, Bruzzone R, Mesnil M, Sanso-netti P, Combettes L. 2003. Connexin-dependent intercellular communication increases invasion and dissemination of Shigella in epithelial cells. Nat Cell Biol 5: 720-726.
78. Tran Van Nhieu G, Kai Liu B, Zhang J, Pierre F, Prigent S, Sansonetti P, Erneux C, Kuk Kim J, Suh PG, Dupont G, et al. 2013. Actin-based confinement of calcium responses during Shigella invasion. Nat Commun 4: 1567.
79. Vuori K, Ruoslahti E. 1995. Tyrosine phosphorylation of p130Cas and cortactin accompanies integrin-mediated cell adhesion to extracellular matrix. J Biol Chem 270: 22259-22262.
80. Wang F, Jiang Z, Li Y, He X, Zhao J, Yang X, Zhu L, Yin Z, Li X, Wang X, et al. 2013. Shigella flexneri T3SS effector IpaH4.5 modulates the host inflammatory response via interaction with NF-kB p65 protein. Cell Microbiol 15: 474-485.
81. Yoshida S, Handa Y, Suzuki T, Ogawa M, Suzuki M, Tamai A, Abe A, Katayama E, Sasakawa C. 2006. Microtubule-se-vering activity of Shigella is pivotal for intercellular spreading. Science 314: 985-989.
82. Zhang L, Ding X, Cui J, Xu H, Chen J, Gong YN, Hu L, Zhou Y, Ge J, Lu Q, et al. 2011. Cysteine methylation disrupts ubiquitin-chain sensingin NF-kB activation. Nature 481: 204-208.
83. Zhou D, Chen LM, Hernandez L, Shears SB, Galán JE. 2001. A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial in-ternalization. Mol Microbiol 39: 248-259.
84. Zychlinsky A, Prevost MC, Sansonetti PJ. 1992. Shigella flex-neri induces apoptosis in infected macrophages. Nature 358: 167-169.