Conformation of the EPEC Tir protein in solution: Investigating the impact of serine phosphorylation at positions 434/463

Biophysical Journal

Volumn 93, Issue 2, 2007, Pages 586-596

  Race, Paul R ^a   Solovyova, Alexandra S ^a   Banfield, Mark J ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ASPARTIC ACID; BUFFER; INTIMIN; MONOMER; PHOSPHATE; SERINE; SERINE DERIVATIVE; SODIUM CHLORIDE;

ARTICLE; CIRCULAR DICHROISM; CONCENTRATION (PARAMETERS); CONFORMATIONAL TRANSITION; ENTEROPATHOGENIC ESCHERICHIA COLI; MUTATION; NONHUMAN; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN CONFORMATION; PROTEIN PHOSPHORYLATION; ULTRACENTRIFUGATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 34447339979     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.101766     Document Type: Article

References (49)

1. Nataro, J. P., and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
2. Kenny, B. 2002. Enteropathogenic Escherichia coli (EPEC) - a crafty subversive little bug. Microbiology. 148:1967-1978.
3. Vallance, B. A., and B. B. Finlay. 2000. Exploitation of host cells by enteropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA. 97:8799-8806.
4. Kenny, B., R. DeVinney, M. Stein, D. J. Reinscheid, E. A. Frey, and B. B. Finlay. 1997. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell. 91:511-520.
5. Kenny, B. 1999. Phosphorylation of tyrosine 474 of the enteropathogenic Escherichia coli (EPEC) Tir receptor molecule is essential for actin nucleating activity and is preceded by additional host modifications. Mol. Microbiol. 31:1229-1241.
6. de Grado, M., A. Abe, A. Gauthier, O. Steele-Mortimer, R. DeVinney, and B. B. Finlay. 1999. Identification of the intimin-binding domain of Tir of enteropathogenic Escherichia coli. Cell. Microbiol. 1:7-17.
7. Race, P. R., J. H. Lakey, and M. J. Banfield. 2006. Insertion of the enteropathogenic Escherichia coli Tir virulence protein into membranes in vitro. J. Biol. Chem. 281:7842-7849.
8. Campellone, K. G., A. Giese, D. J. Tipper, and J. M. Leong. 2002. A tyrosine-phosphorylated 12-amino-acid sequence of enteropathogenic Escherichia coli Tir binds the host adaptor protein Nck and is required for Nck localization to actin pedestals. Mol. Microbiol. 43:1227-1241.
9. Gruenheid, S., R. DeVinney, F. Bladt, D. Goosney, S. Gelkop, G. D. Gish, T. Pawson, and B. B. Finlay. 2001. Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells. Nat. Cell Biol. 3:856-859.
10. Campellone, K. G., and J. M. Leong. 2005. Nck-independent actin assembly is mediated by two phosphorylated tyrosines within enteropathogenic Escherichia coli Tir. Mol. Microbiol. 56:416-432.
11. Warawa, J., and B. Kenny. 2001. Phosphoserine modification of the enteropathogenic Escherichia coli Tir molecule is required to trigger conformational changes in Tir and efficient pedestal elongation. Mol. Microbiol. 42:1269-1280.
12. Hawrani, A., C. E. Dempsey, M. J. Banfield, D. J. Scott, A. R. Clarke, and B. Kenny. 2003. Effect of protein kinase A-mediated phosphorylation on the structure and association properties of the enteropathogenic Escherichia coli Tir virulence protein. J. Biol. Chem. 278:25839-25846.
13. Huffine, M. E., and J. M. Scholtz. 1996. Energetic implications for protein phosphorylation. Conformational stability of HPr variants that mimic phosphorylated forms. J. Biol. Chem. 271:28898-28902.
14. Jang, Y. J., S. Ma, Y. Terada, and R. L. Erikson. 2002. Phosphorylation of threonine 210 and the role of serine 137 in the regulation of mammalian polo-like kinase. J. Biol. Chem. 277:44115-44120.
15. Leger, J., M. Kempf, G. Lee, and R. Brandt. 1997. Conversion of serine to aspartate imitates phosphorylation-induced changes in the structure and function of microtubule-associated protein τ. J. Biol. Chem. 272:8441-8446.
16. Receveur-Brechot, V., J. M. Bourhis, V. N. Uversky, B. Canard, and S. Longhi. 2006. Assessing protein disorder and induced folding. Proteins. 62:24-45.
17. Uversky, V. N. 2002. What does it mean to be natively unfolded? Eur. J. Biochem. 269:2-12.
18. Uversky, V. N., J. R. Gillespie, I. S. Millett, A. V. Khodyakova, R. N. Vasilenko, A. M. Vasiliev, I. L. Rodionov, G. D. Kozlovskaya, D. A. Dolgikh, A. L. Fink, S. Doniach, E. A. Permyakov, and V. M. Abramov. 2000. Zn(2+)-mediated structure formation and compaction of the "natively unfolded" human prothymosin α. Biochem. Biophys. Res. Commun. 267:663-668.
19. Li, J., V. N. Uversky, and A. L. Fink. 2002. Conformational behavior of human α-synuclein is modulated by familial Parkinson's disease point mutations A30P and A53T. Neurotoxicology. 23:553-567.
20. Uversky, V. N. 2002. Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 11:739-756.
21. Sanchez-Puig, N., D. B. Veprintsev, and A. R. Fersht. 2005. Human fulllength Securin is a natively unfolded protein. Protein Sci. 14:1410-1418.
22. Batra-Safferling, R., K. Abarca-Heidemann, H. G. Korschen, C. Tziatzios, M. Stoldt, I. Budyak, D. Willbold, H. Schwalbe, J. Klein-Seetharaman, and U. B. Kaupp. 2006. Glutamic acid-rich proteins of rod photoreceptors are natively unfolded. J. Biol. Chem. 281:1449-1460.
23. Brown, P. H., and P. Schuck. 2006. Macromolecular size-and-shape distributions by sedimentation velocity analytical ultracentrifugation. Biophys. J. 90:4651-4661.
24. Sambrook, J., and D. W. Russell. 2001. Molecular Cloning. A Laboratory Manual, 3rd ed. Coldspring Harbor Laboratory Press, Woodbury, NY.
25. Whitmore, L., and B. A. Wallace. 2004. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 32:W668-W673.
26. Provencher, S. W., and J. Glockner. 1981. Estimation of globular protein secondary structure from circular dichroism. Biochemistry. 20:33-37.
27. Laue, T. M., B. D. Shah, T. M. Ridgeway, and S. Pelletier. 1992. Analytical Ultracentrifugation in Biochemistry and Polymer Science. Redwood Press, Melksham, UK.
28. Durchschlag, H. 1986. Specific volumes of macromolecules and some other molecules of biological interest. In Thermodynamic Data for Biochemistry and Biotechnology. H.-J. Hinz, editor. Springer-Verlag, Berlin. 45-128.
29. Schuck, P. 2000. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys. J. 78:1606-1619.
30. Lamm, O. 1929. Die Differentialgleichung der Ultrazentrifugierung. Ark. Mat. Astr. Fys. 21B:1-4.
31. Schuck, P. 1998. Sedimentation analysis of noninteracting and self-associating solutes using numerical solutions to the Lamm equation. Biophys. J. 75:1503-1512.
32. Schuck, P. 2003. On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation. Anal. Biochem. 320:104-124.
33. Dam, J., and P. Schuck. 2004. Calculating sedimentation coefficient distributions by direct modeling of sedimentation velocity concentration profiles. Methods Enzymol. 384:185-212.
34. Romero, P., Z. Obradovic, X. Li, E. C. Garner, C. J. Brown, and A. K. Dunker. 2001. Sequence complexity of disordered protein. Proteins. 42:38-48.
35. Lebowitz, J., M. S. Lewis, and P. Schuck. 2002. Modern analytical ultracentrifugation in protein science: a tutorial review. Protein Sci. 11:2067-2079.
36. Tompa, P. 2002. Intrinsically unstructured proteins. Trends Biochem. Sci. 27:527-533.
37. Stapley, B. J., and T. P. Creamer. 1999. A survey of left-handed polyproline II helices. Protein Sci. 8:587-595.
38. Fink, A. L. 2005. Natively unfolded proteins. Curr. Opin. Struct. Biol. 15:35-41.
39. Uversky, V. N., C. J. Oldfield, and A. K. Dunker. 2005. Showing your ID: intrinsic disorder as an ID for recognition, regulation and cell signaling. J. Mol. Recognit. 18:343-384.
40. Oldfield, C. J., Y. Cheng, M. S. Cortese, P. Romero, V. N. Uversky, and A. K. Dunker. 2005. Coupled folding and binding with a-helix-forming molecular recognition elements. Biochemistry. 44:12454-12470.
41. Mohan, A., C. J. Oldfield, P. Radivojac, V. Vacic, M. S. Cortese, A. K. Dunker, and V. N. Uversky. 2006. Analysis of molecular recognition features (MoRFs). J. Mol. Biol. 362:1043-1059.
42. Belmont, L., T. Mitchison, and H. W. Deacon. 1996. Catastrophic revelations about Op18/stathmin. Trends Biochem. Sci. 21:197-198.
43. Campbell, K. M., A. R. Terrell, P. J. Laybourn, and K. J. Lumb. 2000. Intrinsic structural disorder of the C-terminal activation domain from the bZIP transcription factor Fos. Biochemistry. 39:2708-2713.
44. Ptitsyn, O. 1995. Molten globule and protein folding. Adv. Protein Chem. 47:83-229.
45. Nimmo, G. A., and P. Cohen. 1978. The regulation of glycogen metabolism. Purification and characterisation of protein phosphatase inhibitor-1 from rabbit skeletal muscle. Eur. J. Biochem. 87:341-351.
46. Hemmings, H. C., Jr., A. C. Nairn, D. W. Aswad, and P. Greengard. 1984. DARPP-32, a dopamine- and adenosine 3′:5′-monophosphate-regulated phosphoprotein enriched in dopamine-innervated brain regions. II. Purification and characterization of the phosphoprotein from bovine caudate nucleus. J. Neurosci. 4:99-110.
47. Uversky, V. N. 1993. Use of fast protein size-exclusion liquid chromatography to study the unfolding of proteins which denature through the molten globule. Biochemistry. 32:13288-13298.
48. 2+ entry into sperm. J. Cell Biol. 142:473-484.
49. Josefsson, E., D. O'Connell, T. J. Foster, I. Durussel, and J. A. Cox. 1998. The binding of calcium to the B-repeat segment of SdrD, a cell surface protein of Staphylococcus aureus. J. Biol. Chem. 273:31145-31152.