Ribosome-induced tuning of GTP hydrolysis by a translational GTPase

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 40, 2014, Pages 14418-14423

  Maracci, Cristina ^b   Peske, Frank ^b   Dannies, Ev ^a   Pohl, Corinna ^b   Rodnina, Marina V ^b  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84907830891     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1412676111     Document Type: Article

References (63)

1. Bourne HR, Sanders DA, McCormick F (1991) The GTPase superfamily: Conserved structure and molecular mechanism. Nature 349(6305):117-127.
2. Hilgenfeld R (1995) Regulatory GTPases. Curr Opin Struct Biol 5(6):810-817.
3. Vetter IR, Wittinghofer A (2001) The guanine nucleotide-binding switch in three dimensions. Science 294(5545):1299-1304.
4. Saraste M, Sibbald PR, Wittinghofer A (1990) The P-loop-A common motif in ATP-and GTP-binding proteins. Trends Biochem Sci 15(11):430-434.
5. Daviter T, Wieden H-J, Rodnina MV (2003) Essential role of histidine 84 in elongation factor Tu for the chemical step of GTP hydrolysis on the ribosome. J Mol Biol 332(3): 689-699.
6. Der CJ, Finkei T, Cooper GM (1986) Biological and biochemical properties of human rasH genes mutated at codon 61. Cell 44(1):167-176.
7. Zeidler W, et al. (1995) Site-directed mutagenesis of Thermus thermophilus elongation factor Tu. Replacement of His85, Asp81 and Arg300. Eur J Biochem 229(3): 596-604.
8. Kamerlin SC, Sharma PK, Prasad RB, Warshel A (2013) Why nature really chose phosphate. Q Rev Biophys 46(1):1-132.
9. Lassila JK, Zalatan JG, Herschlag D (2011) Biological phosphoryl-transfer reactions: Understanding mechanism and catalysis. Annu Rev Biochem 80:669-702.
10. Hengge AC (2005) Mechanistic studies on enzyme-catalyzed phosphoryl transfer. Advances in Physical Organic Chemistry, ed Richard JP (Academic, Amsterdam), Vo I 40, pp 49-108.
11. Li G, Zhang XC (2004) GTP hydrolysis mechanism of Ras-like GTPases. J Mol Biol 340(5): 921-932.
12. Schweins T, Langen R, Warshel A (1994) Why have mutagenesis studies not located the general base in ras p21. Nat Struct Biol 1 (7):476-484.
13. Prasad BP, Plotnikov NV, Lameira J, Warshel A (2013) Quantitative exploration of the molecular origin of the activation of GTPase. Proc Natl Acad Sci USA 110(51): 20509-20514.
14. Pai EF, et al. (1990) Refined crystal structure of the triphosphate conformation of H-ras p21 at 1.35 Á resolution: Implications for the mechanism of GTP hydrolysis. EMBO J 9(8):2351-2359.
15. Voorhees RM, Schmeing TM, Kelley AC, Ramakrishnan V (2010) The mechanism for activation of GTP hydrolysis on the ribosome. Science 330(6005):835-838.
16. Schweins T, et al. (1995) Substrate-assisted catalysis as a mechanism for GTP hydrolysis of p21 ras and other GTP-binding proteins. Nat Struct Biol 2(1):36-44.
17. Plotnikov NV, Prasad BR, Chakrabarty S, Chu ZT, Warshel A (2013) Quantifying the mechanism of phosphate monoester hydrolysis in aqueous solution by evaluating the relevant ab initio QM/MM free-energy surfaces. J Phys Chem B 117(42): 12807-12819.
18. Glennon TM, Villâ J, Warshel A (2000) How does GAP catalyze the GTPase reaction of Ras? A computer simulation study. Biochemistry 39(32):9641-9651.
19. Hilgenfeld R, Mesters JR, Hogg T (2000) Insights into the GTPase mechanism of EF-Tu from structural studies. The Ribosome: Structure, Function, Antibiotics, and Cellular Interactions, eds Garrett RA, et al. (ASM, Washington, DC), pp 347-357.
20. Rodnina MV, et al. (2000) GTPase mechanisms and functions of translation factors on the ribosome. Biol Chem 381 (5-6):377-387.
21. Gromadski KB, Wieden H-J, Rodnina MV (2002) Kinetic mechanism of elongation factor Ts-catalyzed nucleotide exchange in elongation factor Tu. Biochemistry 41 (1): 162-169.
22. Rodnina MV, Fricke R, Kuhn L, Wintermeyer W (1995) Codon-dependent conformational change of elongation factor Tu preceding GTP hydrolysis on the ribosome. EMBO J 14(11):2613-2619.
23. Rodnina MV, Fricke R, Wintermeyer W (1994) Transient conformational states of aminoacyl-tRNA during ribosome binding catalyzed by elongation factor Tu. Biochemistry 33(40):12267-12275.
24. Schmeing TM, et al. (2009) The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science 326(5953):688-694.
25. Villa E, et al. (2009) Ribosome-induced changes in elongation factor Tu conformation control GTP hydrolysis. Proc Natl Acad Sci USA 106(4): 1063-1068.
26. Schuette J-C, et al. (2009) GTPase activation of elongation factor EF-Tu by the ribosome during decoding. EMBO J 28(6):755-765.
27. Adamczyk AJ, Warshel A (2011) Converting structural information into an allostericenergy-based picture for elongation factor Tu activation by the ribosome. Proc Natl Acad Sci USA 108(24):9827-9832.
28. Scarano G, Krab IM, Bocchini V, Parmeggiani A (1995) Relevance of histidine-84 in the elongation factor Tu GTPase activity and in poly(Phe) synthesis: Its substitution by glutamine and alanine. FEBS Lett 365(2-3):214-218.
29. Wallin G, Kamerlin SC, Aqvist J (2013) Energetics of activation of GTP hydrolysis on the ribosome. Nat Commun 4:1733.
30. Aleksandrov A, Field M (2013) Mechanism of activation of elongation factor Tu by ribosome: Catalytic histidine activates GTP by protonation. RNA 19(9):1218 -1225.
31. Grigorenko BL, Shadrina MS, Topol IA, Collins JR, Nemukhin AV (2008) Mechanism of the chemical step for the guanosine triphosphate (GTP) hydrolysis catalyzed by elongation factor Tu. Biochim Biophys Acta 1784(12):1908-1917.
32. Farrar CT, Ma J, Singel DJ, Halkides CJ (2000) Structural changes induced in p21 Ras upon GAP-334 complexation as probed by ESEEM spectroscopy and moleculardynamics simulation. Structure 8(12):1279-1287.
33. Chung HH, Benson DR, Schultz PG (1993) Probing the structure and mechanism of Ras protein with an expanded genetic code. Science 259(5096):806-809.
34. Bos JL, et al. (1985) Amino-acid substitutions at codon 13 of the N-ras oncogene in human acute myeloid leukaemia. Nature 315(6022):726-730.
35. Kozma SC, et al. (1987) The human c-Kirsten ras gene is activated by a novel mutation in codon 13 in the breast carcinoma cell line MDA-MB231. Nucleic Acids Res 15(15): 5963-5971.
36. Levinson AD (1986) Normal and activated ras oncogenes and their encoded products. Trends Genet 2:81-85.
37. Berchtold H, et al. (1993) Crystal structure of active elongation factor Tu reveals major domain rearrangements. Nature 365(6442): 126-132.
38. Ash MR, et al. (2010) Potassium-activated GTPase reaction in the G protein-coupled ferrous iron transporter B. J Biol Chem 285(19): 14594-14602.
39. Scrima A, Wittinghofer A (2006) Dimerisation-dependent GTPase reaction of MnmE: How potassium acts as GTPase-activating element. EMBO J 25(12):2940-2951.
40. Kuhle B, Ficner R (2014) elF5B employs a novel domain release mechanism to catalyze ribosomal subunit joining. EMBO J 33(10):1177-1191.
41. Hwang Y-W, McCabe PG, Innis MA, Miller DL (1989) Site-directed mutagenesis of the GDP binding domain of bacterial elongation factor Tu. Arch Biochem Biophys 274(2): 394-403.
42. Jacquet E, Parmeggiani A (1988) Structure-function relationships in the GTP binding domain of EF-Tu: Mutation of Val20, the residue homologous to position 12 in p21. EMBO J 7(9):2861-2867.
43. Mistou M-Y, Cool RH, Parmeggiani A (1992) Effects of ions on the intrinsic activities of c-H-ras protein p21. A comparison with elongation factor Tu. Eur J Biochem 204(1): 179-185.
44. Quinn DM (2006) in Isotope Effects in Chemistry and Biology, eds Kohen A, Limbach H-H (CRC Taylor and Francis, Boca Raton, FL), pp 995-1018.
45. Fersht A (1984) Enzyme Structure and Mechanism (Freeman, New York), 2nd Ed.
46. Fasano O, De Vendittis E, Parmeggiani A (1982) Hydrolysis of GTP by elongation factor Tu can be induced by monovalent cations in the absence of other effectors. J Biol Chem 257(6):3145-3150.
47. Ash M-R, Maher MJ, Guss JM, Jormakka M (2012) The cation-dependent G-proteins: In a class of their own. FEBS Lett 586(16):2218-2224.
48. Chappie JS, Acharya S, Leonard M, Schmid SL, Dyda F (2010) G domain dimerization controls dynamin's assembly-stimulated GTPase activity. Nature 465(7297):435-440.
49. Liang Z, Mather T, Li G (2000) GTPase mechanism and function: New insights from systematic mutational analysis of the phosphate-binding loop residue Ala30 of Rab5. Biochem J 346(Pt 2):501-508.
50. Zhu G, et al. (2003) High resolution crystal structures of human Rab5a and five mutants with substitutions in the catalytically important phosphate-binding loop. J Biol Chem 278(4):2452-2460.
51. Gromadski KB, Rodnina MV (2004) Kinetic determinants of high-fidelity tRNA discrimination on the ribosome. Mol Cell 13(2):191-200.
52. Rodnina MV, Pape T, Fricke R, Kuhn L, Wintermeyer W (1996) Initial binding of the elongation factor Tu-GTP-aminoacyl-tRNA complex preceding codon recognition on the ribosome. J Biol Chem 271 (2):646-652.
53. Agirrezabala X, et al. (2011) Structural insights into cognate versus near-cognate discrimination during decoding. EMBO J 30(8):1497-1507.
54. Liljas A, Ehrenberg M, Áqvist J, Ramakrishnan V (2011) Comment on "The mechanism for activation of GTP hydrolysis on the ribosome." Science 333(6038):37, author reply 37.
55. Kuhlenkoetter S, Wintermeyer W, Rodnina MV (2011) Different substrate-dependent transition states in the active site of the ribosome. Nature 476(7360):351-354.
56. Admiraal SJ, Herschlag D (1995) Mapping the transition state for ATP hydrolysis: Implications for enzymatic catalysis. Chem Biol 2(11):729-739.
57. Kjeldgaard M, Nissen P, Thirup S, Nyborg J (1993) The crystal structure of elongation factor EF-Tu from Thermus aquaticus in the GTP conformation. Structure 1 (1):35-50.
58. Nissen P, et al. (1995) Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu, and a GTP analog. Science 270(5241):1464-1472.
59. Tourigny DS, Fernández IS, Kelley AC, Ramakrishnan V (2013) Elongation factor G bound to the ribosome in an intermediate state of translocation. Science 340(6140): 1235490.
60. Rodnina MV, Savelsbergh A, Katunin VI, Wintermeyer W (1997) Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. Nature 385(6611):37-41.
61. Kobayashi K, et al. (2010) Structural basis for mRNA surveillance by archaeal Pelota and GTP-bound EF1a complex. Proc Natl Acad Sci USA 107(41):17575-17579.
62. Sondek J, Lambright DG, Noel JP, Hamm HE, Sigler PB (1994) GTPase mechanism of Gproteins from the 1.7-Á crystal structure of transducin alpha-GDP-AIF-4. Nature 372(6503):276-279.
63. Doudna JA, Lorsch JR (2005) Ribozyme catalysis: Not different, just worse. Nat Struct Mol Biol 12(5):395-402.