A multifunctional region of the Shigella type 3 effector IpgB1 is important for secretion from bacteria and membrane targeting in eukaryotic cells

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Costa, Sonia C P ^a   Lesser, Cammie F ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN IPGB1; PROTEIN IPGB2; PROTEIN SPA15; UNCLASSIFIED DRUG; CHAPERONE; IPGB1 PROTEIN, SHIGELLA FLEXNERI; RAC1 PROTEIN; SPA15 PROTEIN, SHIGELLA FLEXNERI;

ALLELE; AMINO TERMINAL SEQUENCE; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EUKARYOTIC CELL; HYDROPHOBICITY; NONHUMAN; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STABILITY; PROTEIN TARGETING; SACCHAROMYCES CEREVISIAE; SHIGELLA; SIGNAL TRANSDUCTION; TYPE III SECRETION SYSTEM; AMINO ACID SEQUENCE; BACTERIAL SECRETION SYSTEM; CELL FRACTIONATION; CHEMICAL PHENOMENA; CHEMISTRY; ENZYME SPECIFICITY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; SECRETION (PROCESS); SHIGELLA FLEXNERI; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CELL MEMBRANE; EUKARYOTIC CELLS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RAC1 GTP-BINDING PROTEIN; SACCHAROMYCES CEREVISIAE; SHIGELLA FLEXNERI; STRUCTURE-ACTIVITY RELATIONSHIP; SUBCELLULAR FRACTIONS; SUBSTRATE SPECIFICITY;

EID: 84899513407     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093461     Document Type: Article

References (32)

1. Schroeder GN, Hilbi H (2008) Molecular pathogenesis of Shigella spp.: controlling host cell signaling, invasion, and death by type III secretion. Clin Microbiol Rev 21: 134-156. (Pubitemid 351160013)
2. Huang Z, Sutton S, Wallenfang AJ, Orchard RC, Wu X, et al. (2009) Structural insights into host GTPase isoform selection by a family of bacterial GEF mimics. Nat Struct Mol Biol 16: 853-860.
3. Hachani A, Biskri L, Rossi G, Marty A, Ménard R, et al. (2008) 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.
4. Alto NM, Shao F, Lazar CS, Brost RL, Chua G, et al. (2006) Identification of a bacterial type III effector family with G protein mimicry functions. Cell 124: 133-145. (Pubitemid 43069315)
5. Handa Y, Susuki M, Ohya K, Iwai H, Ishijima N, et al. (2007) Shigella IpgB1 promotes bacterial entry through the ELMO-Dock180 machinery. Nat Cell Biol 9: 121-128. (Pubitemid 46024206)
6. Ohya K, Handa Y, Ogawa M, Suzuki M, Sasakawa C (2005) IpgB1 is a novel Shigella effector protein involved in bacterial invasion of host cells. Its activity to promote membrane ruffling via Rac1 and Cdc42 activation. J Biol Chem 280: 24022-24034. (Pubitemid 40884890)
7. Page AL, Sansonetti P, Parsot C (2002) Spa15 of Shigella flexneri, a third type of chaperone in the type III secretion pathway. Mol Microbiol 43: 1533-1542. (Pubitemid 34595544)
8. Niebuhr K, Jouihri N, Allaoui A, Gounon P, Sansonetti PJ, et al. (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 Microbiol 38: 8-19.
9. Ogawa M, Susuki T, Tatsuno I, Abe H, Sasakawa C (2003) IcsB, secreted via the type III secretion system, is chaperoned by IpgA and required at the post-invasion stage of Shigella pathogenicity. Mol Microbiol 48: 913-931. (Pubitemid 36628259)
10. Schmitz AM, Morrison M, Agunwamba AO, Nibert ML, Lesser CF (2009) Protein interaction platforms: visualization of interacting proteins in yeast. Nat Methods 6: 500-502.
11. Costa SC, Schmitz SA, Jahufar FF, Boyd JD, Cho MY, et al. (2012) A new means to identify type 3 secreted effectors: functionally interchangeable class IB chaperones recognize a conserved sequence. MBio 3: pii: e00243-00211.
12. Siggers KA, Lesser C (2008) The Yeast Saccharomyces cerevisiae: a versatile model system for the identification and characterization of bacterial virulence proteins. Cell Host Microbe 4: 8-15. (Pubitemid 351944055)
13. Valdivia R (2004) Modeling the function of bacterial virulence factors in Saccharomyces cerevisiae. Eukaryot Cell 3.
14. Slagowski NL, Kramer R, Morrison MF, LaBaer J, Lesser CF (2008) A functional genomic yeast screen to identify pathogenic bacterial proteins. PLoS Pathog 4: e9. doi:.
15. Huang J, Lesser CF, Lory S (2008) The essential role of the CopN protein in Chlamydia pneumoniae intracellular growth. Nature 456: 112-115.
16. Datsenko KA, Wanner B (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645. (Pubitemid 30412767)
17. Lesser CF, Miller S (2001) Expression of microbial virulence proteins in Saccharomyces cerevisiae models mammalian infection. EMBO J 20: 1840-1849. (Pubitemid 32397387)
18. Sisko JL, Spaeth K, Kumar Y, Valdivia RH (2006) Multifunctional analysis of Chlamydia-specific genes in a yeast expression system. Mol Microbiol 60: 51-66. (Pubitemid 43363287)
19. Klink BU, Barden S, Heidler TV, Borchers C, Ladwein M, et al. (2010) Structure of Shigella IpgB2 in complex with human RhoA: implications for the mechanism of bacterial guanine nucleotide exchange factor mimicry. J Biol Chem 285: 17197-17208.
20. Geissler B (2012) Bacterial toxin effector-membrane targeting: outside in, then back again. Front Cell Infect Microbiol 2: 75.
21. Hicks SW, Charron G, Hang HC, Galán JE (2001) Subcellular targeting of Salmonella virulence proteins by host-mediated S-palmitoylation. Cell Host Microbe 10: 9-20.
22. Reinicke AT, Hutchinson J, Magee AI, Mastroeni P, Trowsdale J, et al. (2005) A Salmonella typhimurium effector protein SifA is modified by host cell prenylation and S-acylation machinery. J Biol Chem 280: 14620-14627. (Pubitemid 40562807)
23. Knodler LA, Ibarra J, Perez-Rueda E, Yip CK, Steele-Mortimer O (2011) Coiled-coil domains enhance the membrane association of Salmonella type III effectors. Cell Microbiol 13: 1497-1517.
24. Krall R, Zhang Y, Barbieri JT (2004) Intracellular membrane localization of pseudomonas ExoS and Yersinia YopE in mammalian cells. J Biol Chem 279: 2747-2753. (Pubitemid 38114264)
25. Isaksson EL, Aili M, Fahlgren A, Carlsson SE, Rosqvist R, et al. (2009) The Membrane Localization Domain Is Required for Intracellular Localization and Autoregulation of YopE in Yersinia pseudotuberculosis. Infect Immun 77: 4740-4749.
26. Zhang Y, Barbieri J (2005) A leucine-rich motif targets Pseudomonas aeruginosa ExoS within mammalian cells. Infect Immun 73: 7938-7945. (Pubitemid 41740278)
27. French CT, Panina E, Yeh SH, Griffith N, Arambula DG, et al. (2009) The Bordetella type III secretion system effector BteA contains a conserved N-terminal motif that guides bacterial virulence factors to lipid rafts. Cell Microbiol 11: 1735-1749.
28. Letzelter M, Sorg I, Mota LJ, Meyer S, Stalder J, et al. (2006) The discovery of SycO highlights a new function for type III secretion effector chaperones. EMBO J 25: 3223-3233. (Pubitemid 44106772)
29. Zhang Y, Deng Q, Barbieri JT (2007) Intracellular localization of type III-delivered Pseudomonas ExoS with endosome vesicles. J Biol Chem 282: 13022-13032. (Pubitemid 47100584)
30. Birtalan SC, Phillips R, Ghosh P (2002) Three-dimensional secretion signals in chaperone-effector complexes of bacterial pathogens. Mol Cell 9: 971-980. (Pubitemid 34632625)
31. Lilic M, Vujanac M, Stebbins CE (2006) A common structural motif in the binding of virulence factors to bacterial secretion chaperones. Mol Cell 21: 653-664. (Pubitemid 43290732)
32. Rodgers L, Mukerjea R, Birtalan S, Friedberg D, Ghosh P (2010) A Solvent-Exposed Patch in Chaperone-Bound YopE Is Required for Translocation by the Type III Secretion System. J Bacteriol 12.