Folding kinetics and thermodynamics of Pseudomonas syringae effector protein AvrPto provide insight into translocation via the type III secretion system

Protein Science

Volumn 17, Issue 7, 2008, Pages 1109-1119

  Dawson, Jennifer E ^a   Nicholson, Linda K ^a  

^a Department of Molecular Biology and Genetics   (United States)

Author keywords

AvrPto; Low stability; pH dependent stability; Pseudomonas syringae; Slow conformational exchange; Type III secretion system

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; PROTEIN AVRPTO;

ANISOTROPY; APOPLAST; AQUEOUS SOLUTION; ARTICLE; CONFORMATIONAL TRANSITION; CYTOPLASM; KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN STABILITY; PSEUDOMONAS SYRINGAE; SECRETION; THERMODYNAMICS;

BACTERIAL PROTEINS; KINETICS; MODELS, MOLECULAR; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN TRANSPORT; PSEUDOMONAS SYRINGAE; THERMODYNAMICS;

LYCOPERSICON ESCULENTUM; NEGIBACTERIA; PSEUDOMONAS SYRINGAE;

EID: 46449093638     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.034223.107     Document Type: Article

References (74)

1. Abragam, A. 1961. Principles of nuclear magnetism, 1st ed., pp. 1-599. Clarendon Press, Oxford.
2. Akeda, Y. and Galan, J.E. 2005. Chaperone release and unfolding of substrates in type III secretion. Nature 437: 911-915.
3. 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.
4. Bezsonova, I., Korzhnev, D.M., Prosser, R.S., Forman-Kay, J.D., and Kay, L.E. 2006. Hydration and packing along the folding pathway of SH3 domains by pressure-dependent NMR. Biochemistry 45: 4711-4719.
5. Blocker, A., Jouihri, N., Larquet, E., Gounon, P., Ebel, F., Parsot, C., Sansonetti, P., and Allaoui, A. 2001. Structure and composition of the Shigella flexneri "needle complex," a part of its type III secretion. Mol. Microbiol. 39: 652-663.
6. Bogdanove, A.J. and Martin, G.B. 2000. AvrPto-dependent Pto-interacting proteins and AvrPto-inteacting proteins in tomato. Proc. Natl. Acad. Sci. 97: 8836-8840.
7. Brown, I.R., Mansfield, J.W., Taira, S., Roine, E., and Romantschuk, M. 2001. Immunocytochemical localization of HrpA and HrpZ supports a role for the Hrp Ilus in the transfer of effector proteins from Pseudomonas syringae pv. tomato across the host plant cell wall. Mol. Plant-Microbe Interact. 14: 394-404.
8. Cavanagh, J., Fairbrother, W.J., Palmer, A.G.I., and Skelton, N.J. 1996. Protein NMR spectroscopy: Principles and practice, pp. 243-299. Academic Press, San Diego, CA.
9. Chang, J.H., Rathjen, J.P., Bernal, A.J., Staskawicz, B.J., and Michelmore, R.W. 2000. AvrPto enhances growth and necrosis caused by Pseudomonas syringae pv. tomato in tomato lines lacking either Pto or Prf. Mol. Plant-Microbe Interact. 13: 568-571.
10. Cheng, L.W. and Schneewind, O. 1999. Yersinia enterocolitica type III secretion. On the role of SycE in targeting YopE into HeLa cells. J. Biol. Chem. 274: 22102-22108.
11. Cordes, F.S., Komoriya, K., Larquet, E., Yang, S., Egelman, E.H., Blocker, A., and Lea, S.M. 2003. Helical structure of the needle of the type III secretion system of Shigella flexneri. J. Biol. Chem. 278: 17103-17107.
12. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J., and Bax, A. 1995. NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6: 277-293.
13. Eichelberg, K., Ginocchio, C.C., and Galan, J.E. 1994. Molecular and functional characterization of the Salmonella typhimurium invasion genes invB and invC: Homology of InvC to the F0F1 ATPase family of proteins. J. Bacteriol. 176: 4501-4510.
14. Emerson, S.U., Tokuyasu, K., and Simon, M.I. 1970. Bacterial flagella: Polarity of elongation. Science 169: 190-192.
15. Enninga, J., Mounier, J., Sansonetti, P., and Tran Van Nhieu, G. 2005. Secretion of type III effectors into host cells in real time. Nat. Methods 2: 959-965.
16. 15N NMR relaxation. Biochemistry 33: 5984-6003.
17. 15N longitudinal decay and chemical exchange rates of systems in slow equilibrium. J. Biomol. NMR 4: 727-734.
18. Fivaz, M. and van der Goot, F.G. 1999. The tip of a molecular syringe. Trends Microbiol 7: 341-343.
19. Frithz-Lindsten, E., Rosqvist, R., Johansson, L., and Forsberg, A. 1995. The chaperone-like protein YerA of Yersinia pseudotuberculosis stabilizes YopE in the cytoplasm but is dispensible for targeting to the secretion loci. Mol. Microbiol. 16: 635-647.
20. Galan, J.E. and Collmer, A. 1999. Type III secretion machines: Bacterial devices for protein delivery into host cells. Science 284: 1322-1328.
21. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M.R., Appel, R.D., and Bairoch, A. 2005. Protein identification and analysis tools on the ExPASy server. In The proteomics protocols handbook (ed. John M. Walker), pp. 571-607. Humana Press, Totowa, NJ.
22. Ghosh, P. 2004. Process of protein transport by the type III secretion system. Microbiol. Mol. Biol. Rev. 68: 771-795.
23. Gorbalenya, A.E. and Koonin, E.V. 1993. Helicases-amino-acid-sequence comparisons and structure-function-relationships. Curr. Opin. Struct. Biol. 3: 419-429.
24. Hauck, P., Thilmony, R., and He, S.Y. 2003. A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc. Natl. Acad. Sci. 100: 8577-8582.
25. Jayaraman, B. and Nicholson, L.K. 2007. Thermodynamic dissection of the Ezrin FERM/CERMAD interface. Biochemistry 46: 12174-12189.
26. Jin, Q., Thilmony, R., Zwiesler-Vollick, J., and He, S.Y. 2003. Type III protein secretion in Pseudomonas syringae. Microbes Infect. 5: 301-310.
27. Johnson, S., Deane, J.E., and Lea, S.M. 2005. The type III needle and the damage done. Curr. Opin. Struct. Biol. 15: 700-707.
28. Kenniston, J.A., Baker, T.A., Fernandez, J.M., and Sauer, R.T. 2003. Linkage between ATP consumption and mechanical unfolding during the protein processing reactions of an AAA+ degradation machine. Cell 114: 511-520.
29. Koradi, R., Billeter, M., and Wüthrich, K. 1996. MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graph. 14: 51-55.
30. Lee, C., Schwartz, M.P., Prakash, S., Iwakura, M., and Matouschek, A. 2001. ATP-dependent proteases degrade their substrates by processively unraveling them from the degradation signal. Mol. Cell 7: 627-637.
31. Lee, V.T. and Schneewind, O. 2002. Yop fusions to tightly folded protein domains and their effects on Yersinia enterocolitica type III secretion. J. Bacteriol. 184: 3740-3745.
32. Leigh, J.S. 1971. Relaxation times in systems with chemical exchange: Some exact solutions. J. Magn. Reson. 4: 308-311.
33. Levenberg, K. 1944. A method for the solution of certain problems in least squares. Q. Appl. Math. 2: 164-168.
34. Li, C.M., Brown, I., Mansfield, J., Stevens, C., Boureau, T., Romantschuk, M., and Taira, S. 2002. The Hrp pilus of Pseudomonas syringae elongates from its tip and acts as a conduit for translocation of the effector protein HrpZ. EMBO J. 21: 1909-1915.
35. Lipari, G. and Szabo, A. 1982. Model-free analysis to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104: 4559-4570.
36. Luo, Y., Bertero, M.G., Frey, E.A., Pfuetzner, R.A., Wenk, M.R., Creagh, L., Marcus, S.L., Lim, D., Sicheri, F., Kay, C., et al. 2001. Structural and biochemical characterization of the type III secretions chaperones CesT and SigE. Nat. Struct. Biol. 8: 1031-1036.
37. Lupas, A.N. and Martin, J. 2002. AAA proteins. Curr. Opin. Struct. Biol. 12: 746-753.
38. Marquardt, D. 1963. An algorithm of least-squares estimation of nonlinear parameters. SIAM J. Appl. Math. 11: 431-441.
39. Matouschek, A. 2003. Protein unfolding - an important process in vivo? Curr. Opin. Struct. Biol. 13: 98-109.
40. McConnell, H.M. 1958. Reaction rates by nuclear magnetic resonance. J. Chem. Phys. 28: 430-431.
41. Minamino, T., Imae, Y., Oosawa, F., Kobayashi, Y., and Oosawa, K. 2003. Effect of intracellular pH on rotational speed of bacterial flagellar motors. J. Bacteriol. 185: 1190-1194.
42. Montelione, G.T. and Wagner, G. 1989. 2D chemical-exchange NMR-spectroscopy by proton-detected heteronuclear correlation. J. Am. Chem. Soc. 111: 3096-3098.
43. Mulder, F.A.A., Spronk, C.A.E.A., Slijper, M., Kaptein, R., and Boelens, R. 1996. Improved HSQC experiments for the observation of exchange broadened signals. J. Biomol. NMR 8: 223-228.
44. Nishiguchi, S., Goto, Y., and Takahashi, S. 2007. Solvation and desolvation dynamics in apomyoglobin folding monitored by time-resolved infrared spectroscopy. J. Mol. Biol. 373: 491-502.
45. Palmer, A.G.I. 2001. NMR probes of molecular dynamics: Overview and comparison with other techniques. Annu. Rev. Biophys. Biomol. Struct. 30: 129-155.
46. 15N relaxation parameters. J. Biomol. NMR 20: 149-165.
47. Pawley, N.H., Gans, J.D., and Nicholson, L.K. 2002. Factors determining the reliable description of global tumbling parameters in solution NMR. J. Biomol. NMR 24: 215-229.
48. Pedley, K.F. and Martin, G.B. 2003. Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato. Annu. Rev. Phytopathol. 41: 215-243.
49. Piaggio, M.V., Peirotti, M.B., and Deiber, J.A. 2007. On the application of CZE to the study of protein denaturation. Electrophoresis 28: 2223-2234.
50. Press, W.H., Flannery, B.P., Teukolsky, S.A., and Vetterling, W.T. 1988. Numerical recipes in C, pp. 521-522. Cambridge University Press, Cambridge.
51. Preston, G., Huang, H.C., He, S.Y., and Collmer, A. 1995. The HrpZ proteins of Pseudomonas syringae pvs. Syringae, glycinea, and tomato are encoded by an operon containing Yersinia ysc homologs and elicit the hypersensitive response in tomato but not soybean. Mol Plant-Microbe Interact. 8: 717-732.
52. Rahme, L.G., Mindrinos, M.N., and Panopoulos, N.J. 1992. Plant and environmental sensory signals control the expression of hrp genes in Pseudomonas syringae pv. phaseolicola. J. Bacteriol. 174: 3499-3507.
53. Rosqvist, R., Magnusson, K.E., and Wolf-Wantz, H. 1994. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 13: 964-972.
54. Schlumberger, M.C., Müller, A.J., Ehrbar, K., Winnen, B., Duss, I., Stecher, B., and Hardt, W.D. 2005. Real-time imaging of type III secretion: Salmonella SipA injection into host cells. Proc. Natl. Acad. Sci. 102: 12548-12553.
55. Schurr, J.M., Babcock, H.P., and Fujimoto, B.S. 1994. A test of the model-free formulas. Effects of anisotropic rotational diffusion and dimerization. J. Magn. Reson. B. 105: 211-224.
56. Scofield, S.R., Tobias, C.M., Rathjen, J.P., Chang, J.H., Lavelle, D.T., Michelmore, R.W., and Staskawicz, B.J. 1996. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274: 2063-2065.
57. Shan, L., He, P., Zhou, J.M., and Tang, X. 2000. A cluster of mutations disrupt the antivirulence but not the virulence function of AvrPto. Mol. Plant-Microbe Interact. 13: 592-598.
58. Shea, J.E., Onuchic, J.N., and Brooks III, C.L. 2002. Probing the folding free energy landscape of the Src-SH3 protein domain. Proc. Natl. Acad. Sci. 99: 16064-16068.
59. Sorg, J.A., Miller, N.C., Marketon, M.M., and Schneewind, O. 2005. Rejection of impassable substrates by Yerinia type III secretion machines. J. Bacteriol. 187: 7090-7102.
60. Sory, M.P. and Cornelis, G.R. 1994. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14: 583-594.
61. Stebbins, C.E. and Galan, J.E. 2001. Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414: 77-81.
62. Tamano, K., Aizawa, S., Katayama, E., Nonaka, T., Imajoh-Ohmi, S., Kuwae, A., Nagai, S., and Sasakawa, C. 2000. Supramolecular structure of the Shigella type III secretion machinery: The needle part is changeable in length and essential for delivery of effectors. EMBO J. 19: 3876-3887.
63. Tang, X., Xie, M., Kim, Y.J., Zhou, J., Klessing, D.F., and Martin, G.B. 1999. Overexpression of Pto activates defense responses and confers broad resistance. Plant Cell 11: 15-29.
64. van Dijk, K., Fouts, D.E., Rehm, A.H., Hill, A.R., Collmer, A., and Alfano, J.R. 1999. The Avr (effector) proteins HrmA (HopPsyA) and AvrPto are secreted in culture from Pseudomonas syringae pathovars via the Hrp (type III) protein secretion system in a temperature- and pH-sensitive manner. J. Bacteriol. 181: 4790-4797.
65. Walker, P.A., Leong, L.E., Ng, P.W., Tan, S.H., Waller, S., Murphy, D., and Porter, A.G. 1994. Efficient and rapid affinity purification of proteins using recombinant fusion proteases. Biotechnology (N. Y.) 12: 601-605.
66. Weast, R.C. 1982. CRC handbook of chemistry and physics, 63rd ed. CRC Press, Boca Raton, FL.
67. Wilharm, G., Lehmann, V., Krauss, K., Lehnert, B., Richter, S., Ruckdeschel, K., Heesemann, J., and Trulzsch, K. 2004. Yersinia enterocolitica type III secretion depends on the proton motive force but not on the flagellar motor components MotA and MotB. Infect. Immun. 72: 4004-4009.
68. Woessner, D.E. 1962. Nuclear spin relaxation in ellipsoids undergoing rotational Brownian motion. J. Chem. Phys. 37: 647-654.
69. Woestyn, S., Allaoui, A., Wattiau, P., and Cornelis, G.R. 1994. YscN, the putative energizer of the Yersinia Yop secretion machinery. J. Bacteriol. 176: 1561-1569.
70. Wulf, J., Pascuzzi, P.E., Fahmy, A., Martin, G.B., and Nicholson, L.K. 2004. The solution structure of type III effector protein AvrPto reveals conformational and dynamic features important for plant pathogenesis. Structure 12: 1257-1268.
71. Wulff-Strobel, C.R., Williams, A.W., and Straley, S.C. 2002. LcrQ and SycH function together a the Ysc type III secretion system in Yersinia pestis to impose a hierarchy of secretion. Mol. Microbiol. 43: 411-423.
72. Xiao, Y., Lu, Y., Heu, S., and Hutcheson, S.W. 1992. Organization and environmental regulation of the Pseudomonas syringae pv. syringae 61 hrp cluster. J. Bacteriol. 174: 1734-1741.
73. Yonekura, K., Maki-Yonekura, S., and Namba, K. 2003. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424: 643-650.
74. Zhang, Z.Y., Clemens, J.C., Schubert, H.L., Stuckey, J.A., Fischer, M.W., Hume, D.M., Saper, M.A., and Dixon, J.E. 1992. Expression, purification, and physiochemical characterization of a recombinant Yersinia protein tyrosine phosphatase. J. Biol. Chem. 267: 23759-23766.