Zinc-catalyted sulfur alkylation: Insights from protein farnesyltransferase

Current Opinion in Chemical Biology

Volumn 3, Issue 2, 1999, Pages 176-181

  Hightower, Kendra E ^a   Fierke, Carol A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN FARNESYLTRANSFERASE; SULFUR; ZINC; P21(RAS) FARNESYL PROTEIN TRANSFERASE; P21(RAS) FARNESYL-PROTEIN TRANSFERASE; TRANSFERASE;

ALKYLATION; CATALYSIS; ENZYME MECHANISM; ENZYME STRUCTURE; REVIEW; CHEMISTRY; METABOLISM; PROTEIN CONFORMATION;

ALKYL AND ARYL TRANSFERASES; ALKYLATION; CATALYSIS; PROTEIN CONFORMATION; SULFUR; ZINC;

EID: 0032587329     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1367-5931(99)80030-1     Document Type: Article

References (57)

1. Myers LC, Terranova MP, Ferentz AE, Wagner G, Verdine GL: Repair of DNA methylphosphotriesters through a metalloactivated cysteine nucleophile. Science 1993, 261:1164-1167.
2. Myers LC, Verdine GL, Wagner G: Solution structure of the DNA methyl phosphotriester repair domain of Escherichia coli Ada. Biochemistry 1993, 32:14089-14094.
3. a of the free homocysteine thiol results in the release of 1 equivalent, of protons per mol of protein, as determined by changes in the absorbance of the pH indicator phenol red.
4. Goulding CW, Matthews RG: Cobalamin-dependent methionine synthase from Escherichia coli: Involvement of zinc in homocysteine activation. Biochemistry 1997, 36:15749-15757. Cobalamin-dependent methionine synthase contains a zinc ion that is required for homocysteine binding and methyl transfer to homocysteine. Substitution of cadmium for the zinc decreases activity. Binding of homocysteine to the zinc enzyme results in the release of one equivalent of protons per mole of protein. Proton release after addition of homocysteine is not observed for mutant proteins that do not bind zinc.
5. González JC, Peariso K, Penner-Hahn JE, Matthews RG: Cobalamin-independent methionine synthase from Escherichia coli: A zinc metalloenzyme. Biochemistry 1996, 35:12228-12234.
6. Millian NS, Garrow TA: Human betaine-homocysteine methyltransferase is a zinc metalloenzyme. Arch Biochem Biophys 1998, 356:93-98. Human betaine-homocysteine methyltransferase is identified as a zinc enzyme with homology to cobalamin-dependent methionine synthase.
7. LeClerc GM, Grahame DA: Methylcobamide : Coenzyme M methyltransferase isozymes from Methanosarcina barkeri: Physiochemical characterization, cloning, sequence analysis, and heterologous expression. J Biol Chem 1996, 271:18725-18731.
8. Sauer K, Thauer RK: Methanol : Coenzyme M methyltransferase from Methanosarcina barkeri: Zinc dependence and thermodynamics of the methanol : Cob(I)alamin methyltransferase reaction. Eur J Biochem 1997, 249:280-285. Methyltransferase 1 is identified as a zinc enzyme and the zinc dependence of both the methyltransferase 1 and methyltransferase 2 reactions are determined.
9. 2+-substituted farnesyltransferase demonstrate coordination of the peptide cysteine residue to the metal in a ternary complex, as well as coordination of the thioether product.
10. Moomaw JF, Casey PJ: Mammalian protein geranylgeranyltransferase: Subunit composition and metal requirements. J Biol Chem 1992, 267:17438-17443.
11. Witter DJ, Poulter CD: Yeast geranylgeranyltransferase type-II: Steady state kinetic studies of the recombinant enzyme. Biochemistry 1996, 35:10454-10463.
12. Zhang FL, Casey PJ: Protein prenylation: Molecular mechanisms and functional consequences. Annu Rev Biochem 1996, 65:241-269.
13. Park H-W, Boduluri SR, Moomaw JF, Casey PJ, Beese LS: Crystal structure of protein farnesyltransferase at 2.25 angstrom resolution. Science 1997, 275:1800-1804.
14. Long SB, Casey PJ, Beese LS: Cocrystal structure of protein farnesyltransferase complexed with a farnesyl diphosphate substrate. Biochemistry 1998, 37:9612-9618.
15. Dunten P, Kammlott U, Crowther R, Weber D, Palermo R, Birktoft J: Protein farnesyltransferase: Structure and implication for substrate binding. Biochemistry 1998, 37:7907-7912.
16. Strickland CL, Windsor WT, Syto R, Wang L, Bond R, Wu Z, Schwartz J, Beese LS, Le HV, Weber PC: Crystal structure of farnesyl protein transferase complexed with a CaaX peptide and farnesyl diphosphate analogue. Biochemistry 1998, 37:16601-16611. The structure of a farnesyltransferase ternary complex shows the position of the two substrates, interactions of the substrates with various residues on the enzyme, and coordination of the peptide sulfur with the zinc.
17. Kral AM, Diehl RE, deSolms SJ, Williams TM, Kohl NE, Omer CA: Mutational analysis of conserved residues of the β-subunit of human farnesyl:protein transferase. J Biol Chem 1997, 272:27319-27323. The effect of various farnesyltransferase mutations on zinc binding, farnesyl pyrophosphate binding, and steady-state turnover are analyzed.
18. a of a sulfur residue, most likely the cysteine thiol of the peptide substrate, decreases by approximately two pH units because of interaction of the bound peptide with the metal.
19. Reiss Y, Brown MS, Goldstein JL: Divalent cation and prenyl pyrophosphate specificities of the protein farnesyltransferase from rat brain, a zinc metalloenzyme. J Biol Chem 1992, 267:6403-6408.
20. Chen W-J, Moomaw JF, Overton L, Kost TA, Casey PJ: High level expression of mammalian protein farnesyltransferase in a baculovirus system. J Biol Chem 1993, 268:9675-9680.
21. Fu H-W, Beese LS, Casey PJ: Kinetic analysis of zinc ligand mutants of mammalian protein farnesyltransferase. Biochemistry 1998, 37:4465-4472. Mutation of the zinc ligands Asp297 and His362 does not affect farnesyl pyrophosphate binding but does decrease binding of zinc, binding of H-Ras, and the rate constants for product formation and dissociation.
22. Wilson JM, Bayer RJ, Hupe DJ: Structure-reactivity correlations for the thiol-disulfide interchange reaction. J Am Chem Soc 1977, 99:7922-7926.
23. Szajewski RP, Whitesides GM: Rate constants and equilibrium constants for thiol-disulfide interchange reactions involving oxidized glutathione. J Am Chem Soc 1980, 102:2011-2026.
24. Roberts DD, Lewis SD, Ballou DP, Olson ST, Shafer JA: Reactivity of small thiolate anions and cysteine-25 in papain toward methyl methanethiosulfonate. Biochemistry 1986, 25:5595-5601.
25. Vasák M, Kägi JHR: Spectroscopic properties of metallothionein. In Metal Ions in Biological Systems, vol 15. Edited by Sigel H. New York: Marcel Dekker; 1983:213-273.
26. Pompliano DL, Rands E, Schaber MD, Mosser SD, Anthony NJ, Gibbs JB. Steady-state kinetic mechanism of Ras farnesyl protein transferase. Biochemistry 1992, 31:3800-3807.
27. Dolence JM, Poulter CD: A mechanism for posttranslational modifications of proteins by yeast protein farnesyltransferase. Proc Natl Acad Sci USA 1995, 92:5008-5011.
28. Cassidy PB, Poulter CD: Transition state analogs for protein farnesyltransferase. J Am Chem Soc 1996, 118:8761-8762.
29. Jencks WP: A primer for the bema hapothle. An empirical approach to the characterization of changing transition-state structures. Chem Rev 1985, 85:511-527.
30. Mu Y, Omer CA, Gibbs RA: On the stereochemical course of human protein-farnesyl transferase. J Am Chem Soc 1996, 118:1817-1823.
31. Edelstein RL, Weller VA, Distefano MD, Tung JS: Stereochemical analysis of the reaction catalyzed by yeast protein farnesyltransferase. J Org Chem 1998, 63:5298-5299.
32. Weller VA, Distefano MD: Measurement of the α-secondary kinetic isotope effect for a prenyltransferase by MALDI mass spectrometry. J Am Chem Soc 1998, 120:7975-7976. Secondary kinetic isotope effect experiments suggest that the catalytic mechanism of yeast farnesyltransferase is associative.
33. Matthews RG, Goulding CW: Enzyme-catalyzed methyl transfers to thiols: The role of zinc. Curr Opin Chem Biol 1997, 1:332-339.
34. Peariso K, Goulding CW, Huang S, Matthews RG, Penner-Hahn JE: Characterization of the zinc binding site in methionine synthase enzymes of Escherichia coli: The role of zinc in the methylation of homocysteine. J Am Chem Soc 1998, 120:8410-8416. Using extended X-ray absorption fine structure analysis and X-ray absortion near-edge structure analysis, the zinc coordination of both the cobalamin- independent (two sulfur and two nitrogen/oxygen ligands) and cobalamin- dependent (three sulfur and one nitrogen/oxygen ligands) methionine synthases were determined. Addition of homocysteine to either enzyme results in one additional sulfur ligand and loss of one nitrogen/oxygen ligand, indicating that the homocysteine is directly coordinated to the zinc.
35. 2O of zinc enzymes. Proc Natl Acad Sci USA 1990, 87:220-224.
36. Vallee BL, Auld DS: Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 1990, 29:5647-5659.
37. Wilker JJ, Lippard SJ: Modeling the DNA repair site in Escherichia coli Ada. Why zinc and four cysteines? J Am Chem Soc 1995, 117:8682-8683.
38. 3PO. A small decrease in activity is also observed after substitution of the zinc ion with cobalt or cadmium.
39. Wilker JJ, Wetterhahn KE, Lippard SJ: Methyl transfer to mercury thiolates: Effects of coordination number and ligand dissociation. Inorg Chem 1997, 36:2079-2083.
40. Myers LC, Cushing TD, Wagner G, Verdine GL: Metal-coordination sphere in the methylated Ada protein-DNA co-complex. Chem Biol 1994, 1:91-97.
41. Ohkubo T, Sakashita H, Sakuma T, Kainosho M, Sekiguchi M, Morikawa K: Methylation dependent functional switch mechanism newly found in the Escherichia coli Ada protein. J Am Chem Soc 1994, 116:6035-6036.
42. 2 as a model of zinc sulfur-methylation proteins. Inorg Chem 1998, 37:4052-4058. Model compounds mimicking the Ada system are used to examine dissociation of the active thiolate from and coordination of the product thioether to the zinc.
43. Furfine ES, Leban JJ, Landavazo A, Moomaw JF, Casey PJ: Protein farnesyltransferase: Kinetics of farnesyl pyrophosphate binding and product release. Biochemistry 1995, 34:6857-6862.
44. Tschantz WR, Furfine ES, Casey PJ: Substrate is required for release of product from mammalian protein farnesyltransferase. J Biol Chem 1997, 272:9989-9993.
45. Myers LC, Jackow F, Verdine GL: Metal dependence of transcriptional switching in Escherichia coli Ada. J Biol Chem 1995, 270:6664-6670.
46. Fu H-W, Moomaw JF, Moomaw CR, Casey PJ: Identification of a cysteine residue essential for activity of protein farnesyltransferase. J Biol Chem 1996, 271:28541-28548.
47. Zhang FL, Diehl RE, Kohl NE, Gibbs JB, Giros B, Casey PJ, Omer CA: cDNA cloning and expression of rat and human protein geranylgeranyltransferase type-I. J Biol Chem 1994, 269:3175-3180.
48. Goulding CW, Postigo D, Matthews RG: Cobalamin-dependent methionine synthase is a modular protein with distinct regions for binding homocysteine, methyltetrahydrofolate, cobalamin, and adenosylmethionine. Biochemistry 1997, 36:8082-8091.
49. Lovejoy B, Cleasby A, Hassell AM, Longley K, Luther MA, Weigl D, McGeehan G, McElroy AB, Drewry D, Lambert MH, Jordan SR: Structure of the catalytic domain of fibroblast collagenase complexed with an inhibitor. Science 1994, 263:375-377.
50. Rees DC, Lewis M, Lipscomb WN: Refined crystal structure of carboxypeptidase A at 1.54 Å resolution. J Mol Biol 1983, 168:367-387.
51. Liljas A, Kannan KK, Bergsten P-C, Waara I, Fridborg K, Strandberg B, Carlbom U, Järup L, Lövgren S, Petef M: Cystal structure of human carbonic anhydrase C. Nat New Biol 1972, 235:131-137.
52. Bracey MH, Christiansen J, Tovar P, Cramer SP, Bartlett SG: Spinach carbonic anhydrase: Investigation of the zinc-binding ligands by site-directed mutagenesis, elemental analysis, and EXAFS. Biochemistry 1994, 33:13126-13131.
53. Cedergen-Zepperzauer ES, Andersson I, Ottonello S, Bignetti E: X-ray analysis of structural changes induced by reduced nicotinamide adenine dinucleotide when bound to cysteine-46-carboxymethylated liver alcohol dehydrogenase. Biochemistry 1985, 24:4000-4010.
54. Betts L, Xiang S, Short SA, Wolfenden R, Carter CWJ: Cytidine deaminase. The 2.3 Å crystal structure of an enzyme : Transition-state analog complex. J Mol Biol 1994, 235:635-656.
55. Luisi BF, Xu WX, Otwinowski Z, Freedman LP, Yamamoto KR, Sigle PB: Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA. Nature 1991, 352: 497-505.
56. Fuiji T, Hata Y, Oozeki M, Moriyama H, Wakagi T, Tanaka N, Oshima T: The crystal structure of the zinc-containing ferredoxin from the thermoacidophilic archeon Sulfolobus sp. strain 7. Biochemistry 1997, 36:1505-1513.
57. Paveltich NP, Pabo CO: Zinc finger-DNA recognition: Crystal structure of a Zif268-DNA complex at 2.1 Å. Science 1991, 252:809-817.