YscU/FlhB of Yersinia pseudotuberculosis harbors a C-terminal type III secretion signal

Journal of Biological Chemistry

Volumn 290, Issue 43, 2015, Pages 26082-26291

  Login, Frédéric H ^a   Wolf Watz, Hans ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINS;

C-TERMINAL PEPTIDES; N-TERMINALS; REPORTER PROTEIN; TYPE III SECRETION SYSTEM; TYPE III SECRETIONS; YERSINIA PSEUDOTUBERCULOSIS;

PHYSIOLOGY;

BACTERIAL PROTEIN; GLUTATHIONE TRANSFERASE; PROTEIN FLHB; PROTEIN YOP; PROTEIN YSCF; PROTEIN YSCN; PROTEIN YSCU; UNCLASSIFIED DRUG; YERSINIA OUTER PROTEIN E; FLHB PROTEIN, BACTERIA; MEMBRANE PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOTOXICITY; GENE DELETION; HUMAN; HUMAN CELL; HYDRODYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TYPE III SECRETION SYSTEM; YERSINIA PSEUDOTUBERCULOSIS; CHEMISTRY; METABOLISM; SECRETION (PROCESS);

BACTERIAL PROTEINS; GLUTATHIONE TRANSFERASE; MEMBRANE PROTEINS; YERSINIA PSEUDOTUBERCULOSIS;

EID: 84944937160     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.633677     Document Type: Article

References (53)

1. Galán, J. E., and Wolf-Watz, H. (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature 444, 567-573
2. Portnoy, D. A., Wolf-Watz, H., Bolin, I., Beeder, A. B., and Falkow, S. (1984) Characterization of common virulence plasmids in Yersinia species and their role in the expression of outer membrane proteins. Infect. Immun. 43, 108-114
3. Rosqvist, R., Forsberg, A., Rimpiläinen, M., Bergman, T., and Wolf-Watz, H. (1990) The cytotoxic protein YopE of Yersinia obstructs the primary host defence. Mol. Microbiol. 4, 657-667
4. Rosqvist, R., Magnusson, K. E., and Wolf-Watz, H. (1994) Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 13, 964-972
5. Portnoy, D. A., and Falkow, S. (1981) Virulence-associated plasmids from Yersinia enterocolitica and Yersinia pestis. J. Bacteriol. 148, 877-883
6. Bölin, I., Portnoy, D. A., and Wolf-Watz, H. (1985) Expression of the temperature-inducible outer membrane proteins of yersiniae. Infect. Immun. 48, 234-240
7. Kubori, T., Matsushima, Y., Nakamura, D., Uralil, J., Lara-Tejero, M., Sukhan, A., Galán, J. E., and Aizawa, S. I. (1998) Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280, 602-605
8. Marlovits, T. C., Kubori, T., Sukhan, A., Thomas, D. R., Galán, J. E., and Unger, V. M. (2004) Structural insights into the assembly of the type III secretion needle complex. Science 306, 1040-1042
9. Schraidt, O., and Marlovits, T. C. (2011) Three-dimensional model of Salmonella's needle complex at subnanometer resolution. Science 331, 1192-1195
10. Radics, J., Königsmaier, L., and Marlovits, T. C. (2014) Structure of a pathogenic type 3 secretion system in action. Nat. Struct. Mol. Biol. 21, 82-87
11. Edqvist, P. J., Olsson, J., Lavander, M., Sundberg, L., Forsberg, A., Wolf-Watz, H., and Lloyd, S. A. (2003) YscP and YscU regulate substrate specificity of the Yersinia type III secretion system. J. Bacteriol. 185, 2259-2266
12. Agrain, C., Callebaut, I., Journet, L., Sorg, I., Paroz, C., Mota, L. J., and Cornelis, G. R. (2005) Characterization of a Type III secretion substrate specificity switch (T3S4) domain in YscP from Yersinia enterocolitica. Mol. Microbiol. 56, 54-67
13. Minamino,. T, and Macnab, R. M. (2000) Domain structure of Salmonella FlhB, a flagellar export component responsible for substrate specificity switching. J. Bacteriol. 182, 4906-4914
14. Ferris, H. U., Furukawa, Y., Minamino, T., Kroetz, M. B., Kihara, M., Namba, K., and Macnab, R. M. (2005) FlhB regulates ordered export of flagellar components via autocleavage mechanism. J. Biol. Chem. 280, 41236-41242
15. Sory, M. P., Boland, A., Lambermont, I., and Cornelis, G. R. (1995) Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc. Natl. Acad. Sci. U. S. A. 92, 11998-12002
16. Anderson, D. M., and Schneewind, O. (1997) A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica. Science 278, 1140-1143
17. Lloyd, S. A., Norman, M., Rosqvist, R., and Wolf-Watz, H. (2001) Yersinia YopE is targeted for type III secretion by N-terminal, not mRNA, signals. Mol. Microbiol. 39, 520-531
18. Wang, Y., Sun, M., Bao, H., Zhang, Q., and Guo, D. (2013) Effective identification of bacterial type III secretion signals using joint element features. PLoS ONE 8:e59754
19. Wang, Y., Zhang, Q., Sun, M-A., and Guo, D. (2011) High-accuracy prediction of bacterial type III secreted effectors based on position-specific amino acid composition profiles. Bioinformatics 27, 777-784
20. Yang, Y., Zhao, J., Morgan, R. L., Ma, W., and Jiang, T. (2010) Computational prediction of type III secreted proteins from gram-negative bacteria. BMC Bioinformatics 11, Suppl. 1:S47
21. Vinatzer, B. A., Jelenska, J., and Greenberg, J. T. (2005) Bioinformatics correctly identifies many type III secretion substrates in the plant pathogen Pseudomonas syringae and the biocontrol isolate P. fluorescens SBW25. Mol. Plant Microbe Interact. 18, 877-888
22. Lloyd, S. A., Sjöström, M., Andersson, S., and Wolf-Watz, H. (2002) Molecular characterization of type III secretion signals via analysis of synthetic N-terminal amino acid sequences. Mol. Microbiol. 43, 51-59
23. Arnold, R., Brandmaier, S., Kleine, F., Tischler, P., Heinz, E., Behrens, S., Niinikoski, A., Mewes, H-W., Horn, M., and Rattei, T. (2009) Sequencebased prediction of type III secreted proteins. PLoS Pathog. 5:e1000376
24. Sorg, J. A., Blaylock, B., and Schneewind, O. (2006) Secretion signal recognition by YscN, the Yersinia type III secretion ATPase. Proc. Natl. Acad. Sci. U. S. A. 103, 16490-16495
25. Akeda, Y., and Galán, J. E. (2005) Chaperone release and unfolding of substrates in type III secretion. Nature 437, 911-915
26. Frost, S., Ho, O., Login, F. H., Weise, C. F., Wolf-Watz, H., and Wolf-Watz, M. (2012) Autoproteolysis and intramolecular dissociation of Yersinia YscU precedes secretion of its C-terminal polypeptide YscU (CC). PLoS ONE 7:e49349
27. Allaoui, A., Woestyn, S., Sluiters, C., and Cornelis, G. R. (1994) YscU, a Yersinia enterocolitica inner membrane protein involved in Yop secretion. J. Bacteriol. 176, 4534-4542
28. Zarivach, R., Deng, W., Vuckovic, M., Felise, H. B., Nguyen, H. V., Miller, S. I., Finlay, B. B., and Strynadka, N. C. J. (2008) Structural analysis of the essential self-cleaving type III secretion proteins EscU and SpaS. Nature 453, 124-127
29. Lavander, M., Sundberg, L., Edqvist, P. J., Lloyd, S. A., Wolf-Watz, H., and Forsberg, A. (2002) Proteolytic cleavage of the FlhB homologue YscU of Yersinia pseudotuberculosis is essential for bacterial survival but not for type III secretion. J. Bacteriol. 184, 4500-4509
30. Riordan, K. E., and Schneewind, O. (2008) YscU cleavage and the assembly of Yersinia type III secretion machine complexes. Mol. Microbiol. 68, 1485-1501
31. Björnfot, A-C., Lavander, M., Forsberg, A., and Wolf-Watz, H. (2009) Autoproteolysis of YscU of Yersinia pseudotuberculosis is important for regulation of expression and secretion of Yop proteins. J. Bacteriol. 191, 4259-4267
32. Lountos, G. T., Austin, B. P., Nallamsetty, S., and Waugh, D. S. (2009) Atomic resolution structure of the cytoplasmic domain of Yersinia pestis YscU, a regulatory switch involved in type III secretion. Protein Sci. 18, 467-474
33. Kutsukake, K., Minamino, T., and Yokoseki, T. (1994) Isolation and characterization of FliK-independent flagellation mutants from Salmonella typhimurium. J. Bacteriol. 176, 7625-7629
34. Williams, A. W., Yamaguchi, S., Togashi, F., Aizawa, S. I., Kawagishi, I., and Macnab, R. M. (1996) Mutations in fliK and flhB affecting flagellar hook and filament assembly in Salmonella typhimurium. J. Bacteriol. 178, 2960-2970
35. Feldman, M. F., and Cornelis, G. R. (2003) The multitalented type III chaperones: all you can do with 15 kDa. FEMS Microbiol. Lett. 219, 151-158
36. Schesser, K., Frithz-Lindsten, E., and Wolf-Watz, H. (1996) Delineation and mutational analysis of the Yersinia pseudotuberculosis YopE domains which mediate translocation across bacterial and eukaryotic cellular membranes. J. Bacteriol. 178, 7227-7233
37. Lara-Tejero, M., Kato, J., Wagner, S., Liu, X., and Galán, J. E. (2011) A sorting platform determines the order of protein secretion in bacterial type III systems. Science 331, 1188-1191
38. Kimura, S. R., Brower, R. C., Vajda, S., and Camacho, C. J. (2001) Dynamical view of the positions of key side chains in protein-protein recognition. Biophys. J. 80, 635-642
39. Jones, S., and Thornton, J. M. (1996) Principles of protein-protein interactions. Proc. Natl. Acad. Sci. U. S. A. 93, 13-20
40. Allison, S. E., Tuinema, B. R., Everson, E. S., Sugiman-Marangos, S., Zhang, K., Junop, M. S., and Coombes, B. K. (2014) Identification of the Docking Site between a Type III Secretion System ATPase and a Chaperone for Effector Cargo. J. Biol. Chem. 289, 23734-23744
41. Chen, L., Ai, X., Portaliou, A. G., Minetti, C. A. S. A., Remeta, D. P., Economou, A., and Kalodimos, C. G. (2013) Substrate-activated conformational switch on chaperones encodes a targeting signal in type III secretion. Cell Rep. 3, 709-715
42. Thomas, N. A., Deng, W., Puente, J. L., Frey, E. A., Yip, C. K., Strynadka, N. C. J., and Finlay, B. B. (2005) CesT is a multi-effector chaperone and recruitment factor required for the efficient type III secretion of both LEEand non-LEE-encoded effectors of enteropathogenic Escherichia coli. Mol. Microbiol. 57, 1762-1779
43. Botteaux, A., Kayath, C. A., Page, A-L., Jouihri, N., Sani, M., Boekema, E., Biskri, L., Parsot, C., and Allaoui, A. (2010) The 33 carboxyl-terminal residues of Spa40 orchestrate the multi-step assembly process of the type III secretion needle complex in Shigella flexneri. Microbiology 156, 2807-2817
44. Journet, L., Agrain, C., Broz, P., and Cornelis, G. R. (2003) The needle length of bacterial injectisomes is determined by a molecular ruler. Science 302, 1757-1760
45. Sorg, I., Wagner, S., Amstutz, M., Müller, S. A., Broz, P., Lussi, Y., Engel, A., and Cornelis, G. R. (2007) YscU recognizes translocators as export substrates of the Yersinia injectisome. EMBO J. 26, 3015-3024
46. Panthel, K., Meinel, K. M., Sevil Domènech, V. E., Trülzsch, K., and Rüssmann, H. (2008) Salmonella type III-mediated heterologous antigen delivery: a versatile oral vaccination strategy to induce cellular immunity against infectious agents and tumors. Int. J. Med. Microbiol. 298, 99-103
47. Metcalf, K. J., Finnerty, C., Azam, A., Valdivia, E., and Tullman-Ercek, D. (2014) Using transcriptional control to increase titers of secreted heterologous proteins by the type III secretion system. Appl. Environ. Microbiol. 80, 5927-5934
48. Feldman, M. F., Müller, S., Wüest, E., and Cornelis, G. R. (2002) SycE allows secretion of YopE-DHFR hybrids by the Yersinia enterocolitica type III Ysc system. Mol. Microbiol. 46, 1183-1197
49. Wilharm, G., Lehmann, V., Neumayer, W., Trcek, J., and Heesemann, J. (2004) Yersinia enterocolitica type III secretion: evidence for the ability to transport proteins that are folded prior to secretion. BMC Microbiol. 4, 27
50. Rodgers, L., Gamez, A., Riek, R., and Ghosh, P. (2008) The type III secretion chaperone SycE promotes a localized disorder-to-order transition in the natively unfolded effector YopE. J. Biol. Chem. 283, 20857-20863
51. Zolkiewski, M. (2006) A camel passes through the eye of a needle: protein unfolding activity of Clp ATPases. Mol. Microbiol. 61, 1094-1100
52. Weise, C. F., Login, F. H., Ho, O., Gröbner, G., Wolf-Watz, H., and Wolf-Watz, M. (2014) Negatively Charged Lipid Membranes Promote a Disorder-Order Transition in the Yersinia YscU Protein. Biophys. J. 107, 1950-1961
53. Riordan, K. E., Sorg, J. A., Berube, B. J., and Schneewind, O. (2008) Impassable YscP substrates and their impact on the Yersinia enterocolitica type III secretion pathway. J. Bacteriol. 190, 6204-6216