High-frequency 94 GHz ENDOR characterization of the metal binding site in wild-type Ras·GDP and its oncogenic mutant G12V in frozen solution

Biochemistry

Volumn 45, Issue 1, 2006, Pages 42-50

  Bennati, M ^a   Hertel, M M ^a   Fritscher, J ^a   Prisner, T F ^a   Weiden, N ^b   Hofweber, R ^c   Sporner M ^c   Horn, G ^c   Kalbitzer, H R ^c  

^a GOETHE UNIVERSITY   (Germany)

^b DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOGENS; IONS; NUCLEAR MAGNETIC RESONANCE; PARAMAGNETIC RESONANCE; PROTEINS; SIGNAL PROCESSING; TUMORS; ULTRAVIOLET SPECTROSCOPY; X RAY ANALYSIS;

FROZEN SOLUTION; HIGH-FREQUENCY 94 GHZ ENDOR; METAL BINDING SITE; ONCOGENIC MUTANT;

METAL ANALYSIS;

CARBON 13; GUANOSINE DIPHOSPHATE; LIGAND; MANGANESE; METAL; PHOSPHORUS; RAS PROTEIN;

ARTICLE; BINDING SITE; COMPLEX FORMATION; CORRELATION ANALYSIS; CRYSTAL STRUCTURE; ELECTRON SPIN RESONANCE; FREEZING; HIGH FREQUENCY ELECTRON NUCLEAR DOUBLE RESONANCE SPECTROSCOPY; ISOTOPE LABELING; LOW TEMPERATURE PROCEDURES; METAL BINDING; MUTANT; MUTATION; ONCOGENE RAS; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPECTROSCOPY;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; ELECTRON SPIN RESONANCE SPECTROSCOPY; FREEZING; GLYCINE; GUANOSINE DIPHOSPHATE; GUANYLYL IMIDODIPHOSPHATE; HUMANS; ISOTOPE LABELING; METALS; MUTATION; NUCLEOTIDES; ONCOGENES; PHOSPHORUS; RAS PROTEINS; SOLUTIONS; VALINE; WATER;

EID: 30144433447     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi051156k     Document Type: Article

References (49)

1. Wittinghofer, A., and Waldmann, H. (2000) Ras: a molecular switch involved in tumor formation, Angew. Chem., Int. Ed. 39, 4192-4214.
2. Barbacid, M. (1987) Ras Genes, Annu. Rev. Biochem. 56, 779-827.
3. Schlichting, I., Almo, S. C., Rapp, G., Wilson, K., Petratos, K., Lentfer, A., Wittinghofer, A., Kabsch, W., Pai, E. F., Petsko, G., and Goody, R. S. (1990) Time-resolved X-ray crystallographic study of the conformational change in Ha-Ras p21 protein on GTP hydrolysis, Nature 345, 309-315.
4. Tong, L., deVos, A. M., Milburn, M. V., Brunger, A., and Kim, S.-H. (1991) Crystal structures at 2.2 Å resolution of the catalytic domains of normal ras protein and an oncogenic mutant complexed with GDP, J. Mol. Biol. 217, 503-516.
5. Wei, Y., Zhang, Y., Derewenda, U., Liu, X., Minor, W., Nakamoto, R. K., and Somlyo, A. V. (1997) Crystal structure of RhoA-GDP and its functional implications, Nat. Struct. Biol. 4, 699-703.
6. Prive, G. G., Milburn, M. V., Tong, L., de Vos, A. M., Yamaizumi, Z., Nishimura, S., and Kim, S.-H. (1992) X-ray crystal structures of transforming p21 ras mutants suggest a transition-state stabilization mechanism for GTP hydrolysis, Proc. Natl. Acad. Sci. U.S.A. 89, 3649-3653.
7. Krengel, U., Schlichting, I., Scherer, A., Schumann, R., Frech, M., John, J., Kabsch, W., Pai, E. F., and Wittinghofer, A. (1990) Three-dimensional structures of H-ras p21 mutants: molecular basis for their inability to function as signal switch molecules, Cell 62, 539-548.
8. Franken, S. M., Scheidig, A. J., Krengel, U., Rensland, H., Lautwein, A., Geyer, M., Scheffzek, K., Goody, R. S., Kalbitzer, H. R., Pai, E. F., and Wittinghofer, A. (1993) Three-dimensional structures and properties of a transforming and a nontransforming glycine-12 mutant of p21H-ras, Biochemistry 32, 8411-8420.
9. Ito, Y., Yamasaki, K., Iwahara, J., Tereda, T., Kamiya, A., Shirouzu, M., Muto, Y., Kawai, G., Yokoyama, S., Laue, E. D., Wälchi, M., Shibata, T., Nishimura, S., and Miyazawa, T. (1997) Regional polysterism in the GTP-bound form of the human c-Haras protein, Biochemistry 36, 9109-9119.
10. Hu, J. S., and Redfield, A. G. (1997) Conformational and dynamic differences between N-ras p21 bound to GTPγS and to GMPPNP as studied by NMR, Biochemistry 36, 5045-5052.
11. Spörner, 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. U.S.A. 98, 4944-4949.
12. 31P solid-state NMR spectroscopy, J. Mol. Biol. 323, 899-907.
13. Geyer, M., Schweins, T., Herrmann, C., Prisner, T. F., Wittinghofer, A., and Kalbitzer, H. R. (1996) Conformational transitions in p21ras and in its complexes with the effector protein Raf-RBD and the GTPase activating protein GAP, Biochemistry 35, 10308-10320.
14. Cheng, H., Sukal, S., Deng, H., Leyh, T. S., and Callender, R. (2001) Vibrational structure of GDP and GTP bound to RAS: an isotope-edited FTIR study, Biochemistry 40, 4035-4043.
15. Allin, C., and Gerwert, K. (2001) Ras catalyzes GTP hydrolysis by shifting negative charges from γ- to β-phosphate as revealed by time-resolved FTIR difference spectroscopy, Biochemistry 40, 3037-3046.
16. Allin, C., Ahmadian, M. R., Wittinghofer, A., and Gerwert, K. (2001) Monitoring the GAP catalyzed H-Ras GTPase reaction at atomic resolution in real time, Proc. Natl. Acad. Sci. U.S.A. 98, 7754-7759.
17. Wang, J. H., Xiao, D. G., Deng, H., Webb, M. R., and Callender, R. (1998) Raman difference studies of GDP and GTP binding to c-Harvey ras, Biochemistry 37, 11106-11116.
18. Futatsugi, N., and Tsuda, M. (2001) Molecular dynamics simulations of Gly-12Val mutant of p21ras: dynamic inhibition mechanism, Biophys. J. 81, 3483-3488.
19. Ma, J., and Karplus, M. (1997) Molecular switch in signal transduction: Reaction paths of the conformational changes in rasp21, Proc. Natl. Acad. Sci. U.S.A. 94, 11905-11910.
20. Glennon, T. M., Villa, J., and Warshel, A. (2000) How does GAP catalyze the GTPase reaction of Ras?: A computer simulation study, Biochemistry 39, 9641-9651.
21. 31P NMR spectroscopy, Biochemistry 40, 1884-1889.
22. Spörner, M., Nuehs, A., Ganser, P., Herrmann, C., Wittinghofer, A., and Kalbitzer, H. R. (2005) Conformational states of Ras complexed with the GTP-analogs GppNHp or GppCH2p, implications for the interaction with effector proteins, Biochemistry 44, 2225-2236.
23. 31P NMR spectroscopy, FEBS Lett. 578, 305-310.
24. 17O interactions in GDP and GTP forms of p21 ras, Biochemistry 35, 12186-12193.
25. Latwesen, D. G., Poe, M., Leigh, J. S., and Reed, G. H. (1992) Electron paramagnetic resonance studies of a ras p21-MnIIGDP complex in solution, Biochemistry 31, 4946-4950.
26. 2+, J. Mol. Biol. 266, 847-856.
27. 2+· GDP complexes of N-ras p21 with selective nitrogen-15 labeling, J. Am. Chem. Soc. 114, 9608-9611.
28. Halkides, C. J., Farrar, C. T., Larsen, R. G., Redfield, A. G., and Singel, D. J. (1994) Characterization of the active site of p21 ras by electron spin-echo envelope modulation spectroscopy with selective labeling: Comparisons between GDP and GTP forms, Biochemistry 33, 4019-4035.
29. Halkides, C. J., Farrar, C. T., Redfield, A. G., and Singel, D. J. (1996) The active site of p21 ras: conformational changes induced by the binding of nucleotides, in Biological Structure and Dynamics (Sarma, R. H., Sarma, M. H., Eds.) pp 249-255, Adenine Press, Schenectady, NY.
30. Arieli, D., and Goldfarb, D. (2004) Spin distribution and the location of protons in parmagnetic proteins, Annu. Rev. Biophys. Biomol. Struct. 33, 441-468.
31. Bennati, M., and Prisner, T. F. (2005) New developments in HF-EPR with application in structural biology, Rep. Prog. Phys. 68, 411-448.
32. Tucker, J., Sczakiel, G., Feuerstein, J., John, J., Goody, R. S., and Wittinghofer, A. (1986) Expression of p21 proteins in Escherichia coli and stereochemistry of the nucleotide-binding site, EMBO J. 5, 1351-1358.
33. John, J., Sohmen, R., Feuerstein, J., Linke, R., Wittinghofer, A., and Goody, R. S. (1990) Kinetics of interaction of nucleotides with nucleotide-free H-ras p21, Biochemistry 29, 6058-6065.
34. Herrmann, C., Martin, G. A., and Wittinghofer, A. (1995) Quantitative analysis of the complex between p21ras and the Ras-binding domain of the human Raf-1 protein kinase, J. Biol. Chem. 2707, 2901-2905.
35. Davis, J., Thompson, D., and Beckler, G. S. (1996) Large scale dialysis reaction using E. coli S30 extract systems, Promega Notes Magn. 56, 14-18.
36. Zawadzki, V. and Gross, H. J. (1991) Kinetics of interaction of nucleotides with nucleotide-free H-ras p21, Nucleic Acids Res. 19, 1948.
37. Pratt, J. M. (1984) Coupled transcription translation in prokaryotic cell-free systems, in Transcription and Translation. A Practical Approach (Hames, B. D., Higgins, S. J., Eds.) pp 179-209, IRL Press, Oxford.
38. Kiwaga, T., Muto, Y. and Yokoyama, S. (1995) Cell-free synthesis and amino acid- selective stable isotope labelling of proteins for NMR analysis, J. Biomol. NMR 6, 129-134.
39. Bennati, M., Farrar, C. T., Bryant, J. A., Inati, S. J., Weis, V., Gerfen, G. J., Riggs-Gelasco, P., Stubbe, J., and Griffin, R. G. (1999) Pulsed electron nuclear double resonance (ENDOR) at 140 GHz, J. Magn. Reson. 138, 232-243.
40. 17O Pulsed electron nuclear double resonance study of gadolinium complexes with water, J. Phys. Chem. 108, 7318-7323.
41. 2+, J. Chem. Phys. 102, 2675-2690.
42. Manikandan, P., Carmieli, R., Shane, T., Kalb, A. J., and Goldfarb, D. (2000) W-Band ENDOR investigation of the manganese-binding site of concanavalin A: determination of proton hyperfine couplings and their signs, J. Am. Chem. Soc. 122, 3488-3494.
43. 2+ binding site of concanavalin A as determined by single-crystal high-field ENDOR spectroscopy, J. Am. Chem. Soc. 123, 8378-8386.
44. Milburn, M. V., Tong, L., de Vos, A. M., Brunger, A., Yamaizumi, Z., Nishimura, S., and Kim, S.-H. (1990) Molecular switch for signal transduction: Structural differences between active and inactive forms of protooncogenic ras proteins, Science 247, 939-945.
45. Hall, B. E., Bar-Sagi, D., and Nassar, N. (2002) The structural basis for the transition from Ras-GTP to Ras-GDP, Proc. Natl. Acad. Sci. U.S.A. 99, 12138-12142.
46. 31P ENDOR and ESE-EPR, J. Am. Chem. Soc. 127, 8310-8319.
47. Pai, E. F., Krengel, U., Goody, R. S., Kabsch, W., and 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.
48. Wittinghofer, F., Krengel, U., John, J., Kabsch, W., and Pai, E. F. (1991) Three-dimensional structure of p21 in the active conformation and analysis of an oncogenic mutant. Environ. Health Perspect. 93, 11-15.
49. Reed, G. H., and Markham, G. D. (1984) EPR of Mn(II) complexes with enzymes and other proteins, Biol. Magn. Res. 6, 73-142.