The type VII secretion system of Staphylococcus aureus secretes a nuclease toxin that targets competitor bacteria (original) (raw)
Costa, T. R. et al. Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat. Rev. Microbiol.13, 343–359 (2015). ArticleCAS Google Scholar
Pym, A. S. et al. Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat. Med.9, 533–539 (2003). ArticleCAS Google Scholar
Hsu, T. et al. The primary mechanism of attenuation of bacillus Calmette–Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc. Natl Acad. Sci. USA100, 12420–12425 (2003). ArticleCAS Google Scholar
Stanley, S. A., Raghavan, S., Hwang, W. W. & Cox, J. S. Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proc. Natl Acad. Sci. USA100, 13001–13006 (2003). ArticleCAS Google Scholar
Abdallah, A. M. et al. A specific secretion system mediates PPE41 transport in pathogenic mycobacteria. Mol. Microbiol.62, 667–679 (2006). ArticleCAS Google Scholar
Cole, S. T. et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature393, 537–544 (1998). ArticleCAS Google Scholar
Abdallah, A. M. et al. Type VII secretion—mycobacteria show the way. Nat. Rev. Microbiol.5, 883–891 (2007). ArticleCAS Google Scholar
Baptista, C., Barreto, H. C. & Sao-Jose, C. High levels of DegU-P activate an Esat-6-like secretion system in Bacillus subtilis. PLoS ONE8, e67840 (2013). ArticleCAS Google Scholar
Huppert, L. A. et al. The ESX system in Bacillus subtilis mediates protein secretion. PLoS ONE9, e96267 (2014). Article Google Scholar
Burts, M. L., Williams, W. A., DeBord, K. & Missiakas, D. M. EsxA and EsxB are secreted by an ESAT-6-like system that is required for the pathogenesis of Staphylococcus aureus infections. Proc. Natl Acad Sci. USA102, 1169–1174 (2005). ArticleCAS Google Scholar
Pallen, M. J. The ESAT-6/WXG100 superfamily—and a new Gram-positive secretion system? Trends Microbiol.10, 209–212 (2002). ArticleCAS Google Scholar
Rosenberg, O. S. et al. Substrates control multimerization and activation of the multi-domain ATPase motor of type VII secretion. Cell161, 501–512 (2015). ArticleCAS Google Scholar
Renshaw, P. S. et al. Structure and function of the complex formed by the tuberculosis virulence factors CFP-10 and ESAT-6. EMBO J.24, 2491–2498 (2005). ArticleCAS Google Scholar
Sundaramoorthy, R., Fyfe, P. K. & Hunter, W. N. Structure of Staphylococcus aureus EsxA suggests a contribution to virulence by action as a transport chaperone and/or adaptor protein. J. Mol. Biol.383, 603–614 (2008). ArticleCAS Google Scholar
Sysoeva, T. A., Zepeda-Rivera, M. A., Huppert, L. A. & Burton, B. M. Dimer recognition and secretion by the ESX secretion system in Bacillus subtilis. Proc. Natl Acad Sci. USA111, 7653–7658 (2014). ArticleCAS Google Scholar
Kneuper, H. et al. Heterogeneity in ess transcriptional organization and variable contribution of the Ess/Type VII protein secretion system to virulence across closely related Staphylocccus aureus strains. Mol. Microbiol.93, 928–943 (2014). ArticleCAS Google Scholar
Jäger, F., Zoltner, M., Kneuper, H., Hunter, W. N. & Palmer, T. Membrane interactions and self-association of components of the Ess/Type VII secretion system of Staphylococcus aureus. FEBS Lett.590, 349–357 (2016). Article Google Scholar
Warne, B. et al. The Ess/Type VII secretion system of Staphylococcus aureus shows unexpected genetic diversity. BMC Genomics17, 222 (2016). Article Google Scholar
Burts, M. L., DeDent, A. C. & Missiakas, D. M. EsaC substrate for the ESAT-6 secretion pathway and its role in persistent infections of Staphylococcus aureus. Mol. Microbiol.69, 736–746 (2008). ArticleCAS Google Scholar
Anderson, M., Aly, K. A., Chen, Y. H. & Missiakas, D. Secretion of atypical protein substrates by the ESAT-6 secretion system of Staphylococcus aureus. Mol. Microbiol.90, 734–743 (2013). ArticleCAS Google Scholar
Wang, Y. et al. Role of the ESAT-6 secretion system in virulence of the emerging community-associated Staphylococcus aureus lineage ST398. Sci. Rep.6, 25163 (2016). ArticleCAS Google Scholar
Korea, C. G. et al. Staphylococcal Esx proteins modulate apoptosis and release of intracellular Staphylococcus aureus during infection in epithelial cells. Infect. Immun.82, 4144–4153 (2014). Article Google Scholar
Anderson, M., Chen, Y. H., Butler, E. K. & Missiakas, D. M. EsaD, a secretion factor for the Ess pathway in Staphylococcus aureus. J. Bacteriol.193, 1583–1589 (2011). ArticleCAS Google Scholar
Tabor, S. & Richardson, C. C. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl Acad Sci. USA82, 1074–1078 (1985). ArticleCAS Google Scholar
Butala, M., Zgur-Bertok, D. & Busby, S. J. The bacterial LexA transcriptional repressor. Cell Mol. Life Sci.66, 82–93 (2009). ArticleCAS Google Scholar
Hill, T. M., Sharma, B., Valjavec-Gratian, M. & Smith, J. _sfi_-independent filamentation in Escherichia coli is lexA dependent and requires DNA damage for induction. J. Bacteriol.179, 1931–1939 (1997). ArticleCAS Google Scholar
Gavrieli, Y., Sherman, Y. & Ben-Sasson, S. A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol.119, 493–501 (1992). ArticleCAS Google Scholar
Bos, J., Yakhnina, A. A. & Gitai, Z. BapE DNA endonuclease induces an apoptotic-like response to DNA damage in Caulobacter. Proc. Natl Acad Sci. USA109, 18096–18101 (2012). ArticleCAS Google Scholar
Blower, T. R., Salmond, G. P. & Luisi, B. F. Balancing at survival's edge: the structure and adaptive benefits of prokaryotic toxin–antitoxin partners. Curr. Opin. Struct. Biol.21, 109–118 (2011). ArticleCAS Google Scholar
Daleke, M. H. et al. Specific chaperones for the type VII protein secretion pathway. J. Biol. Chem.287, 31939–31947 (2012). ArticleCAS Google Scholar
Ekiert, D. C. & Cox, J. S. Structure of a PE–PPE–EspG complex from Mycobacterium tuberculosis reveals molecular specificity of ESX protein secretion. Proc. Natl Acad Sci. USA111, 14758–14763 (2014). ArticleCAS Google Scholar
Korotkova, N. et al. Structure of the Mycobacterium tuberculosis type VII secretion system chaperone EspG5 in complex with PE25–PPE41 dimer. Mol. Microbiol.94, 367–382 (2014). ArticleCAS Google Scholar
Zoltner, M. et al. EssC: domain structures inform on the elusive translocation channel in the Type VII secretion system. Biochem. J.473, 1941–1952 (2016). ArticleCAS Google Scholar
Russell, A. B. et al. Type VI secretion delivers bacteriolytic effectors to target cells. Nature475, 343–347 (2011). ArticleCAS Google Scholar
Murdoch, S. L. et al. The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. J. Bacteriol.193, 6057–6069 (2011). ArticleCAS Google Scholar
Souza, D. P. et al. Bacterial killing via a type IV secretion system. Nat. Commun.6, 6453 (2015). ArticleCAS Google Scholar
Hood, R. D. et al. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe7, 25–37 (2010). ArticleCAS Google Scholar
Aoki, S. K. et al. Contact-dependent inhibition of growth in Escherichia coli. Science309, 1245–1248 (2005). ArticleCAS Google Scholar
Zhang, D., de Souza, R. F., Anantharaman, V., Iyer, L. M. & Aravind, L. Polymorphic toxin systems: comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol. Direct7, 18 (2012). ArticleCAS Google Scholar
Jamet, A. & Nassif, X. New players in the toxin field: polymorphic toxin systems in bacteria. MBio6, e0028 5 (2015). Article Google Scholar
Ma, A. T., McAuley, S., Pukatzki, S. & Mekalanos, J. J. Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe5, 234–243 (2009). ArticleCAS Google Scholar
Akpe San Roman, S. et al. A heterodimer of EsxA and EsxB is involved in sporulation and is secreted by a type VII secretion system in Streptomyces coelicolor. Microbiology156, 1719–1729 (2010). Article Google Scholar
Holberger, L. E., Garza-Sanchez, F., Lamoureux, J., Low, D. A. & Hayes, C. S. A novel family of toxin/antitoxin proteins in Bacillus species. FEBS Lett.586, 132–136 (2012). ArticleCAS Google Scholar
Housden, N. G. & Kleanthous, C. Colicin translocation across the Escherichia coli outer membrane. Biochem. Soc. Trans.40, 1475–1479 (2012). ArticleCAS Google Scholar
Willett, J. L., Gucinski, G. C., Fatherree, J. P., Low, D. A. & Hayes, C. S. Contact-dependent growth inhibition toxins exploit multiple independent cell-entry pathways. Proc. Natl Acad. Sci. USA112, 11341–11346 (2015). ArticleCAS Google Scholar
Monk, I. R., Shah, I. M., Xu, M., Tan, M. W. & Foster, T. J. Transforming the untransformable: application of direct transformation to manipulate genetically Staphylococcus aureus and Staphylococcus epidermidis. MBio3, e00277 (2012). ArticleCAS Google Scholar
Helle, L. et al. Vectors for improved Tet repressor-dependent gradual gene induction or silencing in Staphylococcus aureus. Microbiology157, 3314–3323 (2011). ArticleCAS Google Scholar
Karimova, G., Pidoux, J., Ullmann, A. & Ladant, D. A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc. Natl Acad Sci. USA95, 5752–5756 (1998). ArticleCAS Google Scholar
Sambrook, J. & Russell, D. W. Molecular Cloning: A Laboratory Manual 3rd edn (Cold Spring Harbor Laboratory Press, 2001). Google Scholar
Miller, J. H. A Short Course in Bacterial Genetics. A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria (Cold Spring Harbor Laboratory Press, 1992). Google Scholar
Lei, M. G. et al. A single copy integration vector that integrates at an engineered site on the Staphylococcus aureus chromosome. BMC Res. Notes5, 5 (2012). ArticleCAS Google Scholar
Novick, R. P. Genetic systems in staphylococci. Methods Enzymol.204, 587–636 (1991). ArticleCAS Google Scholar
Keller, R., de Keyzer, J., Driessen, A. J. M. & Palmer, T. Co-operation between different targeting pathways during integration of a membrane protein. J. Cell Biol.199, 303–315 (2012). ArticleCAS Google Scholar
Miller, M. et al. Staphylococcal PknB as the first prokaryotic representative of the proline-directed kinases. PLoS ONE5, e9057 (2010). Article Google Scholar