Farnesyltransferase - New insights into the zinc-coordination sphere paradigm: Evidence for a carboxylate-shift mechanism

Biophysical Journal

Volumn 88, Issue 1, 2005, Pages 483-494

  Sousa, Sérgio F ^a   Fernandes, Pedro A ^a   Ramos, Maria João ^a  

^a UNIVERSITY OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; CARBOXYLIC ACID; COORDINATION COMPOUND; PROTEIN FARNESYLTRANSFERASE; THIOL DERIVATIVE; ZINC;

ARTICLE; CALCULATION; CATALYSIS; CHEMICAL REACTION; CRYSTALLOGRAPHY; ENERGY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME MECHANISM; GIBBS REACTION; RADIATION ABSORPTION; ROOM TEMPERATURE; X RAY;

EID: 11244321501     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.048207     Document Type: Article

References (79)

1. Alberts, I. L., K. Nadassy, and S. J. Wodak. 1998. Analysis of zinc binding sites in protein crystal structures. Protein Sci. 7:1700-1716.
2. Andrae, D., U. Haussermann, M. Dolg, H. Stoll, and H. Preuss. 1990. Energy-adjusted ab initio pseudopotentials for the second and third row transition elements. Theor. Chim. Acta. 77:123-141.
3. Ayral-Kaloustian, S., and E. J. Salaski. 2002. Protein farnesyltransferase inhibitors. Curr. Med. Chem. 9:1003-1032.
4. Bauschlicher, C. W. 1995. A comparison of the accuracy of different functionals. Chem. Phys. Lett. 246:40-44.
5. Becke, A. D. 1993. Density-functional thermochemistry. III. The role of exact exchange. J. Chem. Phys. 98:5648-5652.
6. Blomberg, M. R. A., P. E. M. Siegbahn, and G. T. Babcock. 1998. Modeling electron transfer in biochemistry: a quantum chemical study of charge separation in Rhodobacter sphaeroides and photosystem II. J. Am. Chem. Soc. 120:8812-8824.
7. Bordier, B. B., J. Ohkanda, P. Liu, S. Y. Lee, F. H. Salazar, P. L. Marion, K. Ohashi, L. Meuse, M. A. Kay, J. L. Casey, S. M. Sebti, A. D. Hamilton, and J. S. Glenn. 2003. In vivo antiviral efficacy of prenylation inhibitors against hepatitis delta virus. J. Clin. Invest. 112:407-414.
8. Brauer, M., M. Kunert, E. Dinjus, M. Klussmann, M. Doring, H. Gorls, and E. Anders. 2000. Evaluation of the accuracy of PM3, AM1 and MNDO/d as applied to zinc compounds. J. Mol. Struct. 505:289-301.
9. Cances, E., B. Mennucci, and J. Tomasi. 1997. A new integral equation formalism for the polarizable continuum model: theoretical background and applications to isotropic and anisotropic dielectrics. J. Chem. Phys. 107:3032-3041.
10. Chakrabarti, P. 1990. Interaction of metal ions with carboxylic and carboxamide groups in protein structures. Protein Eng. 4:49-56.
11. Chakrabarti, D., T. Da Silva, J. Barger, S. Paquette, H. Patel, S. Patterson, and C. M. Allen. 2002. Protein farnesyltransferase and protein prenylation in plasmodium falciparum. J. Biol. Chem. 277:42066-42073.
12. Coleman, J. E. 1998. Zinc enzymes. Curr. Opin. Chem. Biol. 2:222-234.
13. Cossi, M., V. Barone, B. Mennucci, and J. Tomasi. 1998. Ab initio study of ionic solutions by a polarizable continuum dielectric model. Chem. Phys. Lett. 286:253-260.
14. Cossi, M., N. Rega, G. Scalmani, and V. Barone. 2003. Energies, structures, and electronic properties of molecules in solution with the C-PCM solvation model. J. Comput. Chem. 24:669-681.
15. Cossi, M., G. Scalmani, N. Rega, and V. Barone. 2002. New developments in the polarizable continuum model for quantum mechanical and classical calculations on molecules in solution. J. Chem. Phys. 117:43-54.
16. Dapprich, S., I. Komaromi, K. S. Byun, K. Morokuma, and M. J. Frisch. 1999. A new ONIOM implementation in Gaussian98. Part I. The calculation of energies, gradients, vibrational frequencies and electric field derivatives. J. Mol. Struct. 461:1-21.
17. Dolence, J. M., and C. D. Poulter. 1995. A mechanism for posttranslational modifications of proteins by yeast protein farnesyltransferase. Proc. Natl. Acad. Sci. USA. 92:5008-5011.
18. Dolence, J. M., D. B. Rozema, and C. D. Poulter. 1997. Yeast protein farnesyltransferase. Site-directed mutagenesis of conserved residues in the beta-subunit. Biochemistry. 36:9246-9252.
19. Dolg, M., U. Wedig, H. Stoll, and H. Preuss. 1987. Energy-adjusted ab initio pseudopotentials for the first row transition elements. J. Chem. Phys. 86:866-872.
20. Dunten, P., U. Kammlott, R. Crowther, D. Weber, R. Palermo, and J. Birktoft. 1998. Protein farnesyltransferase: structure and implications for substrate binding. Biochemistry. 37:7907-7912.
21. Fernandes, P. A., L. A. Eriksson, and M. J. Ramos. 2002. The reduction of ribonucleotides catalyzed by the enzyme ribonucleotide reductase. Theor. Chem. Acc. 108:352-364.
22. Fernandes, P. A., and M. J. Ramos. 2003a. Theoretical studies on the mechanism of inhibition of ribonucleotide reductase by (E)-2′-fluoro- methylene-2′-deoxycitidine-5′-diphosphate. J. Am. Chem. Soc. 125:6311-6322.
23. Fernandes, P. A., and M. J. Ramos. 2003b. Theoretical studies on the mode of inhibition of ribonucleotide reductase by 2′-substituted substrate analogues. Chemistry. 9:5916-5925.
24. Fernandes, P. A., and M. J. Ramos. 2004. Theoretical insights into the mechanism for thiol/disulfide exchange. Chemistry. 10:257-266.
25. Frenking, G., I. Antes, M. Bohme, S. Dapprich, A. W. Ehlers, V. Jonas, A. Neubaus, M. Otto, R. Stegmann, A. Veldkamp, and S. F. Vyboishchikov. 1996. Pseudopotential calculations of transition metal compounds: scope and limitations. Rev. Comp. Chem. 8:63-144.
26. Frisch, M. J., G. W. Trucks, H. B. Schlegel, G. E. Scuseria, M. A. Robb, J. R. Cheeseman, J. A. Montgomery, T. Vreven, K. N. Kudin, J. C. Burant, J. M. Millam, S. S. Iyengar, J. Tomasi, V. Barone, B. Mennucci, M. Cossi, G. Scalmani, N. Rega, G. A. Petersson, H. Nakatsuji, M. Hada, M. Ehara, K. Toyota, R. Fukuda, J. Hasegawa, M. Ishida, T. Nakajima, Y. Honda, O. Kitao, H. Nakai, M. Klene, X. Li, J. E. Knox, H. P. Hratchin, J. B. Cross, C. Adamo, J. Jaramillo, R. Gomperts, R. E. Stratmann, O. Yazyev, A. J. Austin, R. Cammi, C. Pomelli, J. W. Ochterski, P. Y. Ayala, K. Morokuma, G. A. Voth, P. Salvador, J. J. Dannenberg, V. G. Zakrzewski, S. Dapprich, A. D. Daniels, M. C. Strain, O. Farkas, D. K. Malik, A. D. Rabuck, K. Raghavachari, J. B. Foresman, J. V. Ortiz, Q. Cui, A. G. Baboul, S. Clifford, J. Cioslowski, B. B. Stefanov, G. Liu, A. Liashenko, P. Piskorz, I. Komaromi, R. L. Martin, D. J. Fox, T. Keith, A. Al-Lahan, C. Y. Peng, A. Nanayakkara, M. Challacombe, P. M. W. Gill, B. Johnson, W. Chen, M. W. Wong, C. Gonzalez, and J. A. Pople. 2003. Gaussian 03: Revision A.1. Gaussian, Pittsburg, PA.
27. Fu, H. W., L. S. Beese, and P. J. Casey. 1998. Kinetic analysis of zinc ligand mutants of mammalian protein farnesyltransferase. Biochemistry. 37:4465-4472.
28. Goodman, L. E., S. R. Judd, C. C. Farnsworth, S. Powers, M. H. Gelb, J. A. Glomset, and F. Tamanoi. 1990. Mutants of Saccharomyces cerevisiae defective in the farnesylation of Ras proteins. Proc. Natl. Acad. Sci. USA. 87:9665-9669.
29. Hancock, J. F., A. I. Magee, J. E. Childs, and C. J. Marshall. 1989. All Ras proteins are polyisoprenylated but only some are palmitoylated. Cell. 57:1167-1177.
30. Harding. M. M. 2001. Geometry of metal-ligand interactions in proteins. Acta. Crystallogr. D. Biol. Crystallogr. 57:401-411.
31. Hightower, K. E., C. C. Huang, P. J. Casey, and C. A. Fierke. 1998. H-Ras peptide and protein substrates bind protein farnesyltransferase as an ionized thiolate. Biochemistry. 37:15555-15562.
32. Holthausen, M. C., M. Mohr, and W. Koch. 1995. The performance of density functional/Hartree-Fock hybrid methods: the bonding in cationic first-row transition metal methylene complexes. Chem. Phys. Lett. 240:245-252.
33. Huang, C. C., P. J. Casey, and C. A. Fierke. 1997. Evidence for a catalytic role of zinc in protein farnesyltransferase. J. Biol. Chem. 272:20-23.
34. Huang, C. Y., and L. Rokosz. 2004. Farnesyltransferase inhibitors: recent advances. Expert Opin. Ther. Pat. 14:175-186.
35. Jackson, J. H., C. G. Cochrane, J. R. Bourne, P. A. Solski, J. E. Buss, and C. J. Der. 1990. Farnesol modification of Kirsten-Ras exon 4B protein is essential for transformation. Proc. Natl. Acad. Sci. USA. 87:3042-3046.
36. James, G., J. L. Goldstein, and M. S. Brown. 1996. Resistance of K-RasBV12 proteins to farnesyltransferase inhibitors in Rat1 cells. Proc. Natl. Acad. Sci. USA. 93:4454-4458.
37. Johnston, S. R. 2001. Farnesyl transferase inhibitors: a novel targeted therapy for cancer. Lancet Oncol. 2:18-26.
38. Kato, K., A. D. Cox, M. M. Hisaka, S. M. Graham, J. E. Buss, and C. J. Der. 1992. Isoprenoid addition to Ras protein is the critical modification for its membrane association and transforming activity. Proc. Natl. Acad. Sci. USA. 89:6403-6407.
39. Krai, A. M., R. E. Diehl, S. J. deSolms, T. M. Williams, N. E. Kohl, and C. A. Omer. 1997. Mutational analysis of conserved residues of the beta-subunit of human farnesyl:protein transferase. J. Biol. Chem. 272:27319-27323.
40. Kuno, M., S. Hannongbua, and K. Morokuma. 2003. Theoretical investigation on nevirapine and HIV-1 reverse transcriptase binding site interaction, based on ONIOM method. Chem. Phys. Lett. 380:456-463.
41. Lee, C., W. T. Yang, and R. G. Parr. 1988. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys. Rev. B. 37:785-789.
42. Lipscomb, W. N., and N. Strater. 1996. Recent advances in zinc enzymology. Chem. Rev. 96:2375-2434.
43. Long, S. B., P. J. Casey, and L. S. Beese. 1998. Cocrystal structure of protein farnesyltransferase complexed with a farnesyl diphosphate substrate. Biochemistry. 37:9612-9618.
44. Long, S. B., P. J. Casey, and L. S. Beese. 2000. The basis for K-Ras4B binding specificity to protein farnesyltransferase revealed by 2 A resolution ternary complex structures. Struct. Fold. Des. 8:209-222.
45. Long, S. B., P. J. Casey, and L. S. Beese. 2002. Reaction path of protein farnesyltransferase at atomic resolution. Nature. 419:645-650.
46. Long, S. B., P. J. Hancock, A. M. Kral, H. W. Hellinga, and L. S. Beese. 2001. The crystal structure of human protein farnesyltransferase reveals the basis for inhibition by CaaX tetrapeptides and their mimetics. Proc. Natl. Acad. Sci. USA. 98:12948-12953.
47. Lucas, M. F., P. A. Fernandes, L. A. Eriksson, and M. J. Ramos. 2003. Pyruvate formate lyase: a new perspective. J. Phys. Chem. B. 107:5751-5757.
48. McCall, K. A., C. C. Huang, and C. A. Fierke. 2000. Function and mechanism of zinc metalloenzymes. J. Nutr. 130:1437-1446.
49. Melo, A., M. J. Ramos, W. B. Floriano, J. A. N. F. Gomes, J. F. R. Leão, A. L. Magalhães, B. Maigret, M. C. Nascimento, and N. Reuter. 1999. Theoretical study of arginine-carboxylate interactions. J. Mol. Struct. 463:81-90.
50. Mennucci, B., and J. Tomasi. 1997. Continuum solvation models: a new approach to the problem of solutes's charge distribution and cavity boundaries. J. Chem. Phys. 106:5151-5158.
51. Moores, S. L., M. D. Schaber, S. D. Mosser, E. Rands, M. B. O'Hara, V. M. Garsky, M. S. Marshall, D. L. Pompliano, and J. B. Gibbs. 1991. Sequence dependence of protein isoprenylation. J. Biol. Chem. 266:14603-14610.
52. Morokuma, K., D. G. Musaev, T. Vreven, H. Basch, M. Torrent, and D. V. Khoroshun. 2001. Model studies of the structures, reactivities, and reaction mechanisms of metalloenzymes. IBM. J. Res. and Dev. 45:367-395.
53. Ohkanda, J., F. S. Buckner, J. W. Lockman, K. Yokoyama, D. Carrico, R. Eastman, K. Luca-Fradley, W. Davies, S. L. Croft, W. C. Van Voorhis, M. H. Gelb, S. M. Sebti, and A. D. Hamilton. 2004. Design and synthesis of peptidomimetic protein farnesyltransferase inhibitors as anti-Trypanosoma brucei agents. J. Med. Chem. 47:432-445.
54. Ohkanda, J., D. B. Knowles, M. A. Blaskovich, S. M. Sebti, and A. D. Hamilton. 2002. Inhibitors of protein farnesyltransferase as novel anticancer agents. Curr. Top. Med. Chem. 2:303-323.
55. Park, H. W., S. R. Boduluri, J. F. Moomaw, P. J. Casey, and L. S. Beese. 1997. Crystal structure of protein farnesyltransferase at 2.25 angstrom resolution. Science. 275:1800-1804.
56. Pelmenschikov, V., and P. E. Siegbahn. 2002. Catalytic mechanism of matrix metalloproteinases: two-layered ONIOM study. Inorg. Chem. 41:5659-5666.
57. Pereira, S., P. A. Fernandes, and M. J. Ramos. 2004. Theoretical study of ribonucleotide reductase mechanism-based inhibition by 2′-azido-2′- deoxyribonucleoside 5′-diphosphates. J. Comput. Chem. 25:227-237.
58. Pickett, J. S., K. E. Bowers, and C. A. Fierke. 2003a. Mutagenesis studies of protein farnesyltransferase implicate aspartate β352 as a magnesium ligand. J. Biol. Chem. 278:51243-51250.
59. Pickett, J. S., K. E. Bowers, H. L. Hartman, H. W. Fu, A. C. Embry, P. J. Casey, and C. A. Fierke. 2003b. Kinetic studies of protein farnesyltransferase mutants establish active substrate conformation. Biochemistry. 42:9741-9748.
60. Reiss, Y., M. S. Brown, and J. L. Goldstein. 1992. Divalent cation and prenyl pyrophosphate specificities of the protein farnesyltransferase from rat brain, a zinc metalloenzyme. J. Biol. Chem. 267:6403-6408.
61. Reiss, Y., J. L. Goldstein, M. C. Seabra, P. J. Casey, and M. S. Brown. 1990. Inhibition of purified p21ras farnesyl:protein transferase by Cys-AAX tetrapeptides. Cell. 62:81-88.
62. Reiss, Y., S. J. Stradley, L. M. Gierasch, M. S. Brown, and J. L. Goldstein. 1991. Sequence requirement for peptide recognition by rat brain p21ras protein farnesyltransferase. Proc. Natl. Acad. Sci. USA. 88:732-736.
63. Ricca, A., and C. W. Bauschlicher. 1995. A comparison of density functional theory with ab initio approaches for systems involving first transition row metals. Theor. Chim. Acta. 92:123-131.
64. Ryde, U. 1999. Carboxylate binding modes in zinc proteins: a theoretical study. Biophys. J. 77:2777-2787.
65. Siegbahn, P. E. M. 1998. Theoretical study of the substrate mechanism of ribonucleotide reductase. J. Am. Chem. Soc. 120:8417-8429.
66. Siegbahn, P. E. M., L. A. Eriksson, F. Himo, and M. Pavlov. 1998. Hidroge atom transfer in ribonucleotide reductase (RNR). J. Phys. Chem. B. 102:10622-10629.
67. Stewart. J. J. P. 1989a. Optimization of parameters for semiempirical methods. 1. Method. J. Comput. Chem. 10:209-220.
68. Stewart, J. J. P. 1989b. Optimization of parameters for semiempirical methods. 2. Applications. J. Comput. Chem. 10:221-264.
69. Stewart, J. J. P. 1991. Optimization of parameters for semiempirical methods. 3. Extension of PM3 to Be, Mg, Zn, Ga, Ge, As, Se, Cd, In, Sn, Sb, Te, Hg, T1, Pb, and Bi. J. Comput. Chem. 12:320-341.
70. Strickland, C. L., W. T. Windsor, R. Syto, L. Wang, R. Bond, Z. Wu, J. Schwartz, H. V. Le, L. S. Beese, and P. C. Weber. 1998. Crystal structure of farnesyl protein transferase complexed with a CaaX peptide and farnesyl diphosphate analogue. Biochemistry. 37:16601-16611.
71. Takai, Y., T. Sasaki, and T. Matozaki. 2001. Small GTP-binding proteins. Physiol. Rev. 81:153-208.
72. Tobin, D. A., J. S. Pickett, H. L. Hartman, C. A. Fierke, and J. E. Penner-Hahn. 2003. Structural characterization of the zinc site in protein farnesyltransferase. J. Am. Chem. Soc. 125:9962-9969.
73. Torrent, M., T. Vreven, D. G. Musaev, K. Morokuma, O. Farkas, and H. B. Schlegel. 2002. Effects of the protein environment on the structure and energetics of active sites of metalloenzymes. ONIOM study of methane monooxygenase and ribonucleotide reductase. J. Am. Chem. Soc. 124:192-193.
74. Tschantz, W. R., E. S. Furfine, and P. J. Casey. 1997. Substrate binding is required for release of product from mammalian protein farnesyltransferase. J. Biol. Chem. 272:9989-9993.
75. Vallee, B. L., and D. S. Auld. 1990. Active-site zinc ligands and activated H2O of zinc enzymes. Proc. Natl. Acad. Sci. USA. 87:220-224.
76. Vreven, T., and K. Morokuma. 2000. On the application of the IMOMO (integrated molecular orbital plus molecular orbital) method. J. Comput. Chem. 21:1419-1432.
77. Wiesner, J., K. Kettler, J. Sakowski, R. Ortmann, A. Katzin, E. Kimura, K. Silber, G. Klebe, H. Jomaa, and M. Schlitzer. 2004. Farnesyltransferase inhibitors inhibit the growth of malaria parasites in vitro and in vivo. Angew. Chem. Int. Ed. 43:251-254.
78. Zhang. F. L., H. W. Fu, P. J. Casey, and W. R. Bishop. 1996. Substitution of cadmium for zinc in farnesyl:protein transferase alters its substrate specificity. Biochemistry. 35:8166-8171.
79. Ziegler, T. 1991. Approximate density functional theory as a practical tool in molecular energetics and dynamics. Chem. Rev. 91:651-667.