Observation of slow dynamic exchange processes in Ras protein crystals by 31P solid state NMR spectroscopy

Journal of Molecular Biology

Volumn 323, Issue 5, 2002, Pages 899-907

  Stumber, Michael ^a   Geyer, Matthias ^a   Graf, Robert ^b   Robert Kalbitzer, Hans ^c   Scheffzek, Klaus ^d   Haeberlen, Ulrich ^a  

^a MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^b MAX PLANCK INSTITUTE FOR POLYMER RESEARCH   (Germany)

^c UNIVERSITY OF REGENSBURG   (Germany)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Dynamics in crystals; MAS NMR; Protein dynamics; Ras; Solid state NMR

Indexed keywords

GUANOSINE TRIPHOSPHATASE; NUCLEOTIDE; PHOSPHORUS; PROTEIN; PROTEIN RAS; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; CRYSTALLIZATION; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE; SENSITIVITY ANALYSIS; TEMPERATURE DEPENDENCE; X RAY DIFFRACTION;

EID: 0036430139     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)01010-0     Document Type: Article

References (40)

1. Bourne, H. R., Sanders, D. A. & McCormick, F. (1990). The GTPase superfamily: A conserved switch for diverse cell functions. Nature, 348, 125-132.
2. Marshall, M. S. (1995). Ras target proteins in eukary-otic cells. FASEB J. 9, 1311-1318.
3. Barbacid, M. (1987). Ras genes. Annu. Rev. Biochem. 56, 779-827.
4. Bos, J. L. (1989). Ras oncogenes in human cancer: A review. Cancer Res. 49, 4682-4689.
5. Milburn, M. V., Tong, L., deVos, A. M., Brünger, A., Yamaizumi, Z., Nishimura, S. & Kim, S. H. (1990). Molecular switch for signal transduction: Structural differences between active and inactive forms of proto-oncogenic Ras proteins. Science, 247, 939-945.
6. Pai, E. F., Krengel, U., Petsko, G. A., Goody, R. S., Kabsch, W. & Wittinghofer, A. (1990). Refined crystal structure of the triphosphate conformation of H-ras p21 at 1.35 Å resolution: Implications for the mechanism of GTP hydrolysis. EMBO J. 9, 2351-2359.
7. Scheidig, A. J., Burmester, C. & Goody, R. S. (1999). The pre-hydrolysis state of p21(ras) in complex with GTP: New insights into the role of water molecules in the GTP hydrolysis reaction of ras-like proteins. Struct. Fold. Des. 7, 1311-1324.
8. Kraulis, P. J., Domaille, P. J., Campbell, S. L., van Aken, T. & Laue, E. D. (1994). Solution structure and dynamics of Ras p21.GDP determined by hetero-nuclear three and four-dimensional NMR spectroscopy. Biochemistry, 33, 3515-3531.
9. Ito, Y., Yamasaki, K., Iwahara, J., Terada, T., Kamiya, A., Shirouzu, M. et al. (1997). Regional polysterism in the GTP-bound form of the human c-Ha-Ras protein. Biochemistry, 36, 9109-9119.
10. Schlichting, I., Almo, S. C., Rapp, G., Wilson, K., Petratos, K., Lentfer, A. et al. (1990). Time resolved X-ray crystallographic study of the conformational change in Ha-Ras p21 protein on GTP hydrolysis. Nature, 345, 309-315.
11. ras and in its complexes with the effector protein Raf-RBD and the GTPase activating protein GAP. Biochemistry, 35, 10308-10320.
12. Ganguly, A. K., Wang, Y. S., Pramanick, B. N., Doll, R. J., Snow, M. E., Taveras, A. G. et al. (1998). Interaction of a novel GDP exchange inhibitor with the Ras protein. Biochemistry, 37, 15631-15637.
13. Geyer, M. & Schlichting, I. (1999). Information contained in protein structures determined by NMR in solution or by X-ray diffraction in crystals. In Simplicity and Complexity in Proteins and Nucleic Acids (Frauenfelder, H., Deisenhofer, J. & Wolynes, P. G., eds), pp. 59-79, Dahlem University Press, Berlin.
14. Ménétrey, J. & Cherfils, J. (1999). Structure of the small G protein Rap2 in a non-catalytic complex with GTP. Proteins: Struct. Funct. Genet. 37, 465-473.
15. Pines, A., Gibby, M. G. & Waugh, J. S. (1972). Proton-enhanced nuclear induction spectroscopy. A method for high resolution n.m.r. of dilute spins in solids. J. Chem. Phys. 56, 1776-1777.
16. Haeberlen, U. (1996). Optimizing sensitivity in solid state NMR. Bull. Ampere, 45, 13-30.
17. Haeberlen, U. (1976). Advances in Magnetic Resonance (Waugh, J. S., ed.), Suppl. 1, Academic Press, New York.
18. Herzfeld, J. & Berger, A. E. (1980). Sideband intensities in NMR spectra of samples spinning at the magic angle. J. Chem. Phys. 73, 6021-6030.
19. Nassar, N., Horn, G., Herrmann, C., Scherer, A., McCormick, F. & Wittinghofer, A. (1995). The 2.2 Å crystal structure of the Ras binding domain of the serine/threonine kinase c-Raf1 in complex with Rap1A and a GTP analogue. Nature, 375, 554-560.
20. Wittinghofer, A. & Nassar, N. (1996). How Ras-related proteins talk to their effectors. Trends Biochem. Sci. 21, 488-491.
21. Cherfils, J., Ménétrey, J., Le Bras, G., Janoueix-Lerosey, I., de Gunzburg, J., Garel, J. R. & Auzat, I. (1997). Crystal structure of the small G protein Rap2A in complex with its substrate GTP, with GDP and with GTPγS. EMBO J. 16, 5582-5591.
22. Frauenfelder, H., Parak, F. & Young, R. D. (1988). Conformational substates in proteins. Annu. Rev. Biophys. Chem. 17, 451-479.
23. Ringe, D. & Petsko, G. A. (1986). Study of protein dynamics by X-ray diffraction. Methods Enzymol. 131, 389-433.
24. Feher, V. A. & Cavanagh, J. (1999). Millisecond-time-scale motions contribute to the function of the bacterial response regulator protein Spo0F. Nature, 400, 289-293.
25. Mulder, F. A., Mittermaier, A., Hon, B., Dahlquist, F. W. & Kay, L. E. (2001). Studying excited states of proteins by NMR spectroscopy. Nature Struct. Biol. 8, 932-935.
26. Sydor, J. R., Engelhard, M., Wittinghofer, A., Goody, R. S. & Herrmann, C. (1998). Transient kinetic studies on the interaction of Ras and the Ras-binding domain of c-Raf-1 reveal rapid equilibration of the complex. Biochemistry, 37, 14292-14299.
27. Spoerner, M., Herrmann, C., Vetter, I. R., Kalbitzer, H. R. & Wittinghofer, A. (2001). Dynamic properties of the Ras switch I region and its importance for binding to effectors. Proc. Natl Acad. Sci. USA, 98, 4944-4949.
28. Geyer, M., Assheuer, R., Klebe, C., Kuhlmann, J., Becker, J., Wittinghofer, A. & Kalbitzer, H. R. (1999). Conformational states of the nuclear GTP-binding protein Ran and its complexes with the exchange factor RCC1 and the effector protein RanBP1. Biochemistry, 38, 11250-11260.
29. Ma, J. & Karplus, M. (1997). Molecular switch in signal transduction: Reaction paths of the conformational changes in ras p21. Proc. Natl Acad. Sci. USA, 94, 1905-11910.
30. Soares, T. A., Miller, J. H. & Straatsma, T. P. (2001). Revisiting the structural flexibility of the complex p21(ras)-GTP: The catalytic conformation of the molecular switch II. Proteins, 45, 297-312.
31. Westheimer, F. H. (1987). Why nature chose phosphates. Science, 235, 1173-1178.
32. gF″. Eur. J. Biochem. 269, 3270-3278.
33. Palmer, A. G., III (1997). Probing molecular motion by NMR. Curr. Opin. Struct. Biol. 7, 732-737.
34. Kay, L. E. (1998). Protein dynamics from NMR. Nature Struct. Biol. 5, 145-152.
35. Ishima, R. & Torchia, D. A. (2000). Protein dynamics from NMR. Nature Struct. Biol. 7, 740-743.
36. Wand, A. J. (2001). Dynamic activation of protein function: A view emerging from NMR spectroscopy. Nature Struct. Biol. 8, 926-931.
37. Scherer, A., John, J., Linke, R., Goody, R. S., Wittinghofer, A., Pai, E. F. & Holmes, K. C. (1989). Crystallization and preliminary X-ray analysis of the human c-H-ras-oncogene product p21 complexed with GTP analogues. J. Mol. Biol. 206, 257-259.
38. Franken, S. M., Scheidig, A. J., Krengel, U., Rensland, H., Lautwein, A., Geyer, M. et al. (1993). Three-dimensional structures and properties of a transforming and a non-transforming glycine-12 mutant of p21H-ras. Biochemistry, 32, 8411-8420.
39. 31P-Festkörper-NMR und Aufbau des dazu erforderlichen Spektrometers. Dissertation, Universität Heidelberg.
40. Kraulis, P. J. (1991). MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.