Crystal structure of a phosphatase-resistant mutant of sporulation response regulator Spo0F from Bacillus subtilis

Structure

Volumn 4, Issue 6, 1996, Pages 679-690

  Madhusudan, ^a   Zapf, James ^a   Whiteley, John M ^a   Hoch, James A ^a   Xuong, Nguyen H ^b   Varughese, Kottayil I ^a,b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aspartate pocket; Crystal structure; Phosphotransfer; Sporulation response regulator; Two component system

Indexed keywords

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS);

BACTERIAL PROTEIN; CALCIUM; PHOSPHATASE; PHOSPHOTRANSFERASE; SPO0F PROTEIN, BACILLUS SUBTILIS;

AMINO ACID SEQUENCE; ARTICLE; BACILLUS SUBTILIS; BACTERIAL SPORE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; SALMONELLA TYPHIMURIUM; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BINDING SITES; CALCIUM; CRYSTALLOGRAPHY, X-RAY; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PHOSPHOTRANSFERASES; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; SALMONELLA TYPHIMURIUM; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SPORES, BACTERIAL;

EID: 0030585421     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(96)00074-3     Document Type: Article

References (60)

1. Stock, J.B., Surette, M.G., Levit, M. & Park, P. (1995). Two-component signal transduction systems: structure-function relationships and mechanisms of catalysis. In Two-component Signal Transduction (Hoch, J.A. & Silhavy, T.J., eds), pp. 25-51, ASM Press, Washington DC.
2. Stock, J.B., Ninfa, A.J. & Stock, A.M. (1989). Protein phosphorylation and regulation of adaptive responsed in bacteria. Microbiol. Rev. 53, 450-490.
3. Parkinson, J.S. & Kofoid, E.C. (1992). Communication modules in bacterial signaling proteins. Annu. Rev. Genet. 26, 71-112.
4. Hoch, J.A. (1993). Regulation of the phosphorelay and the initiation of sporulation in Bacillus subtilis. Annu. Rev. Microbiol. 47, 441-465.
5. Burbulys, D., Trach, K.A. & Hoch, J.A. (1991). Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell 64, 545-552.
6. Simms, S.A., Keane, M.G. & Stock, J. (1985). Multiple forms of the CheB methylesterase in bacterial chemosensing. J. Biol. Chem. 260, 10161-10168.
7. Grimsley, J.K., et al., & Hoch, J.A. (1994). Subunit composition and domain structure of the Spo0A sporulaiton transcription factor of Bacillus subtilis. J. Biol. Chem. 269, 16977-16982.
8. Stock, A.M., Mottonen, J.M., Stock, J.B. & Schutt, C.E. (1989). Three-dimensional structure of CheY, the response regulator of bacterial chemotaxis. Nature 337, 745-749.
9. Volz, K. (1995). Structural and functional conservation in response regulators. In Two-component Signal Transduction. (Hoch, J.A. & Silhavy, T.J., eds), pp. 53-64, ASM Press, Washington DC.
10. Ganguli, S., Wang, H., Matsumura, P. & Volz, K. (1995). Uncoupled phosphorylation and activation in bacterial chemotaxis. The 2.1-Å structure of a threonine to isoleucine mutant at position 87 of CheY. J. Biol. Chem. 270, 17386-17393.
11. Zapf, J.W., Hoch, J.A. & Whiteley, J.M. (1996). A phosphotransferase activity of the Bacillus subtilis sporulation protein Spo0F that employs phosphoramidate substrates. Biochemistry 35, 2926-2933.
12. Perego, M. & Hoch, J.A. (1996). Cell-cell communication regulates the effects of protein aspartate phosphatases on the phosphorelay controlling development in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 93, 1549-1553.
13. Hess, J.F., Bourret, R.B. & Simon, M.I. (1988). Histidine phosphorylation and phosphoryl group transfer in bacterial chemotaxis. Nature 336, 139-143.
14. Perego, M., Hanstein, C., Welsh, K.M., Djavakhishvili, T., Glaser, P. & Hoch, J.A. (1994). Multiple protein-aspartate phosphatases provide a mechanism for the integration of diverse signals in the control of development in B. subtilis. Cell 79, 1047-1055.
15. Sanna, M.G., Swanson, R.V., Bourret, R.B. & Simon, M.I. (1995). Mutations in the chemotactivc response regulator, CheY, that confer resistance to the phosphatase activity of CheZ. Mol. Microbiol. 15, 1069-1079.
16. Stock, A.M., et al., Petsko, G.A. (1993). Strucuture of the Mg(2+)-bound form of CheY and mechanism of phosphoryl transfer in bacterial chemotaxis. Biochemistry 32, 13375-13380.
17. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. (1993). PROCHECK - a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26, 283-291.
18. McDonald, I.K. & Thornton, J.M. (1994). Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238, 777-793.
19. Richardson, J. (1981). The anatomy and taxonomy of protein structure. Adv. Protein Chem. 34, 167-339.
20. Lee, J., Rieu, P., Arnaout, M.A. Liddington, R. (1995). Crystal structure of the A domain from the α subunit of integrin CR3 (CD11b/CD18), Cell 80, 631-638.
21. Burnett, R.M., et al., & Ludwig, M.L. (1974). The structure of the oxidized from of clostridial flavo doxin at 1.9Å resolution. J. Biol. Chem. 249, 4383-4392.
22. Stuart, D.I., Levine, M., Muirhead, H. & Stammers, D.K. (1979). Crystal structure of cat muscle pyruvate kinase at a resolution of 2.6 Å. J. Mol. Biol. 134, 109-142.
23. Su, X., Taddel, N., Stefani, M., Ramponi, G. & Nordlund, P. (1994). The crystal structure of a low-molecular weight phosphotyrosine protein phosphatase. Nature 370, 575-578.
24. Li, R., Bianchet, M.A., Talalay, P. Amzel, M. (1995). The three-dimensional structure of NAD(P)H: quinone reductase, a flavotprotein, involved in cancer chemoprotenction and chemotheraoy: mechanism of two-electron reduction. Proc. Natl. Acad. Sci. USA 92, 8846-8850.
25. Volz, K. (1993). Structural conservation in the CheY superfamily. Biochemistry 32, 11741-11753.
26. Stock, J.B., Stock, A.M. Mottonen, J.M. (1993). Signal transduction in bacteria. Nature 344, 395-400.
27. Chauvaux, S., Souchon, H., Alzari, P.M., Chariot, P. & Beguin, P. (1995). Structural and functional analysis of the metal-binding sites of Clostridium thermocullum endoglucanase CelD. J. Biol. Chem. 270, 9757-9762.
28. 3 calcium complex. Int. J. Pept. Protein Res. 27, 118-122.
29. Chakrabarti, P. (1994). Conformaitonal analysis of carboxylate and carboxamide side-chains bound to cations. J. Mol. Biol. 269, 306-314.
30. Knowles, J.R. (1980). Enzyme-catalyzed phosphoryl transfer reactions. Annu. Rev. Biochem. 49, 877-919.
31. Sanders, D.A., Gillece-Castro, B.L., Stock, A.M., Burlingame, A.L. & Koshland, D.E., Jr. (1989). Identification of the site of phosphorylation of the chemotaxis response regulator protein, CheY. J. Biol. Chem. 264, 21770-21778.
32. Sanders, D.A., Gillece-Castro, B.L., Burlingame, A.L. & Koshland, D.E., Jr. (1992). Phosphorylation sits of NtrC, a protein phosphatase whose covalent intermediate activates transcription. J. Bacteriol. 174, 5117-5122.
33. Lukat, G.S., Lee, B.H., Mottonen, J.M., Stock, A.M. & Strock, J.B. (1991). Roles of the highly conserved aspartate and lysine residues in the response regulator of bacterial chemotaxis. J. Biol. Chem. 266, 8348-8354.
34. 19F NMR and protein engineering. J. Biol. Chem. 268, 13089-13096.
35. Nicholls, A., Bharadwaj, R. & Honig, B. (1993). GRASP: graphical representation and analysis of surface properties. Biophys. J. 64, 166-170.
36. Swanson, R.V., Lowry, D.F., Matsumura, P., McEvoy, M.M., Simon, M.I. & Dahlquist, F.W. (1995). Localized perturbations in CheY structure monitored by NMR identify a CheA binding interface. Nat. Struct. Biol. 10, 906-910.
37. Shukla, D. & Matsumura, P. (1995). Mutations leading to altered CheA binding cluster on a face of CheY. J. Biol. Chem. 270, 24414-24419.
38. McEvoy, M.M., et al., & Dahlquist, F.W. (1995). Nuclear magnetic resonance assignments and global fold of a CheY-binding domain in CheA, the chemotaxis-specific kinase of Escherichia coli, Biochemistry 34, 13871-13880.
39. Brunger, A.T. (1992). X-PLOR Version 3.1 Manual. Yale Univeristy, New Haven, CT.
40. Lee, B. & Richards, F.M. (1971). The interpretation of protein structure: estimation of static accessibility. J. Mol. Biol. 55, 379-400.
41. Volz, K. & Matsumura, P. (1991). Crystal structure of Escherichia coli CheY refined at 1.7-Å resolution. J. Biol. Chem. 266, 15511-15519.
42. Bellsolell, L., Prieto, J., Serrano, L. & Coll, M. (1994). Magnesium binding to the bacterial chemotaxis protein CheY results in large conformational changes involving its funcitonal surface. J. Mol. Biol. 238, 489-495.
43. 13C backbone chemical shift assignments, secondary structure, and magnesium binding characteristics of the Bacillus subtilis response regulator. Spo0F, determinde by heteronuclear high resolution NMR. Protein Sci. 4, 1801-1814.
44. Welch, M., Oosawa, K., Aizawa, S. & Eisenbach, M. (1993). Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria. Proc. Natl. Acad. Sci. USA 90, 8787-8791.
45. 15N) NMR spectroscopy. Biochemistry 33, 10731-10742.
46. Pao, G.M. & Saier, M.H. (1995). Response regulators of bacterial signal transduction systems: selective domain shuffling during evolution. J. Mol. Evol. 40, 136-154.
47. Madhusudan, Zapl, J., Whiteley, J.M., Hoch, J.A., Hoch, J.A., Xuong, N.H. & Varughese, K.I. (1996). Crystallization and preliminary X-reay analysis of a Y13S mutant of Spo0F form Bacillus subtilis. Acta Cryst. D. in press.
48. Hamlin, R. (1985). Multiwire area X-ray diffractometers. Methods Enzymol. 114, 416-452.
49. Howard, A.J., Nielsen, C. & Xuong, N.H. (1985). Software for a diffractometer with multiware area detector. Methods Enzymol. 114, 452-472.
50. Furey, W. & Swaminathan, S. (1996). PHASES: a program package for the processing and analysis of diffraction data form macromolecules. Methods Enzymol., in press.
51. Wang, B.C. (1985). Resolution of phase ambiguity in macromolecular crystallography. Methdos Enzymol. 115, 90-112.
52. Cambillau, C. & Horjales, E. (1987). TOM: A FRODO subpakage for protein ligand fitting with interactive energy minimization. J. Mol. Graphics 5, 174-177.
53. Jones, T.A., Zou, J. Y., Cowan, S.W. & Kjeldgaard, M. (1991). Improved methods for binding protein models in electron-density maps and the location of errors in these models. Acta Cryst. A-Found. Crystallor. 47, 110-119.
54. Otwinowski, Z. (1998), DENZO. A program for automatic evaluation of film densities. Yale University, New Haven. CT.
55. Read, R.J. (1986). Improved Fourier coefficients for maps using phases form partial structures with error. Acta Cryst. A 42, 140-149.
56. Tronrud, D.E., Ten Eyck, L.F. & Matthws, B.W. (1987). An efficient general purpose least-squares refinement program for macromolecular structures. Acta Crystallogr A-Found. Cryst. 43, 489-501.
57. Ramachandran, G.N. & Sasisekharan, V. (1968). Conformation of polypeptides and proteins. Adv. Protein Chem. 23, 283-438.
58. Luzzati, P.V. (1952). Traitement statistique des erreus dans la determination des structures cristallines. Acta Cryst. 5, 802-810.
59. Evans, S.V. (1993). SETOR: hardware-lighted three-dimensional solid model representatins of macromolecules. J. Mol. Graphics 11, 134-138.
60. Kraulis, P.J. (1991). MOLSCRIPT - a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24, 946-950.