Expression and characterization of protein geranylgeranyltransferase type I from the pathogenic yeast Candida albicans and identification of yeast selective enzyme inhibitors

Biochimica et Biophysica Acta - Protein Structure and Molecular Enzymology

Volumn 1480, Issue 1-2, 2000, Pages 132-144

  Smalera, Isabella ^a   Williamson, Joanne M ^a   Baginsky, Walter ^a   Leiting, Barbara ^a   Mazur, Paul ^a  

^a MERCK RESEARCH LABORATORIES   (United States)

Author keywords

Candida albicans; Enzyme inhibitor; Protein geranylgeranyltransferase I; Substrate inhibition

Indexed keywords

ANTIFUNGAL AGENT; ENZYME INHIBITOR; GERANYLTRANSFERASE; MALTOSE BINDING PROTEIN;

ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; YEAST;

ALKYL AND ARYL TRANSFERASES; AMINO ACID SEQUENCE; BASE SEQUENCE; CANDIDA ALBICANS; ENZYME INHIBITORS; MOLECULAR SEQUENCE DATA; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); CANDIDA ALBICANS;

EID: 0034647876     PISSN: 01674838     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0167-4838(00)00067-4     Document Type: Article

References (44)

1. Zhang F.L., Casey P.J. Protein prenylation: molecular mechanisms and functional consequences. Annu. Rev. Biochem. 65:1996;241-269.
2. Moores S.L., Schaber M.D., Mosser S.D., Rands E., O'Hara M.B., Garsky V.M., Marshall M.S., Pompliano D.L., Gibbs J.B. Sequence dependence of protein isoprenylation. J. Biol. Chem. 22:1991;14603-14610.
3. Yokoyama K., Goodwin G.W., Ghomashchi F., Glomset J.A., Gelb M.H. A protein geranylgeranyltransferase from bovine brain: implications for protein prenylation specificity. Proc. Natl. Acad. Sci. USA. 88:1991;5302-5306.
4. Gelb M.H., Scholten J.D., Sebolt-Leopold J.S. Protein prenylation: from discovery to prospects for cancer treatment. Curr. Opin. Chem. Biol. 2:1998;40-48.
5. Adams E.M., Johnson D.I., Longnecker R.M., Sloat B.F., Pringle J.R. CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae. J. Cell Biol. 111:1990;131-142.
6. Finegold A.A., Johnson D.I., Farnsworth C.C., Gelb M.H., Judd S.R., Glomset J.A., Tamanoi F. Geranylgeranylprotein transferase of Saccharomyces cerevisiae is specific for Cys-Xaa-Xaa-Leu motif proteins and requires the CDC43 gene product, but not the DPR1 gene product. Proc. Natl. Acad. Sci. USA. 88:1991;4448-4452.
7. He B., Chen P., Chen S., Vancura K.L., Michaelis S., Powers S. RAM2, an essential gene of yeast, and RAM1 encode the two polypeptide components of the farnesyltransferase that prenylates a-factor and Ras proteins. Proc. Natl. Acad. Sci. USA. 88:1991;11373-11377.
8. Ohya Y., Goebl M., Goodman L.E., Peterson-Bjorn S., Friesen J.D., Tamanoi F., Anraku Y. Yeast CAL1 is a structural and functional homologue to the DPR1 (RAM) gene involved in ras processing. J. Biol. Chem. 266:1991;12356-12360.
9. Mayer M.L., Caplin B.E., Marshall M.S. CDC43 and RAM2 encode the polypeptide subunits of a yeast type I protein geranylgeranyltransferase. J. Biol. Chem. 267:1992;20589-20593.
10. Kohl N.E., Diehl R.E., Schaber M.D., Rands E., Soderman D.D., He B., Moores S.L., Pompliano D.L., Ferro-Novick S., Powers S., Thomas K.A., Gibbs J.B. Structural homology among mammalian and Saccharomyces cerevisiae isoprenyl-protein transferases. J. Biol. Chem. 266:1991;18884-18888.
11. Arellano M., Coll P.M., Yang W., Duran A., Tamanoi F., Perez P. Characterization of the geranylgeranyl transferase type I from Schizosaccharomyces pombe. Mol. Microbiol. 29:1998;1357-1367.
12. Ohya Y., Qadota H., Anraku Y., Pringle J.R., Botstein D. Suppression of the yeast geranylgeranyl transferase I defect by alternative prenylation of two target GTPases, Rho1p and Cdc42p. Mol. Biol. Cell. 4:1993;1017-1025.
13. Trueblood C.E., Ohya Y., Rine J. Genetic evidence for in vivo cross-specificity of the CaaX-box protein prenyltransferases farnesyltransferase and geranylgeranyltransferase-I in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:1993;4260-4275.
14. Mirbod F., Nakashima S., Kitajima Y., Cannon R.D., Nozawa Y. Molecular cloning of a Rho family, CDC42Ca gene from Candida albicans and its mRNA expression changes during morphogenesis. J. Med. Vet. Mycol. 35:1997;173-179.
15. Kondoh O., Tachibana Y., Ohya Y., Arisawa M., Watanabe T. Cloning of the RHO1 gene from Candida albicans and its regulation of β-1,3-glucan synthesis. J. Bacteriol. 179:1997;7734-7741.
16. Drgonová J., Drgon T., Tanaka K., Kollár R., Chen G.-C., Ford R.A., Chan C.S.M., Takai Y., Cabib E. Rho1p, a yeast protein at the interface between cell polarization and morphogenesis. Science. 272:1996;277-279.
17. Mazur P., Baginsky W. In vitro activity of 1,3-β-D-glucan synthase requires the GTP-binding protein Rho1. J. Biol. Chem. 271:1996;14604-14609.
18. Qadota H., Python C.P., Inoue S.B., Arisawa M., Anraku Y., Zheng Y., Watanabe T., Levin D.E., Ohya Y. Identification of yeast Rho1 GTPase as a regulatory subunit of 1,3-β-glucan synthase. Science. 272:1996;279-281.
19. Arellano M., Durán A., Pérez P. Rho1 GTPase activates the (1-3)β-D-glucan synthase and is involved in Schizosaccharomyces pombe morphogenesis. EMBO J. 15:1996;4584-4591.
20. Graybill J.R. The future of antifungal therapy. Clin. Infect. Dis. 22:1996;S166-S178.
21. Mazur P., Register E., Bonfiglio C.A., Yuan X., Kurtz M.B., Williamson J.M., Kelly R. Purification of geranylgeranyltransferase I from Candida albicans and cloning of the CaRAM2 and CaCDC43 genes encoding its subunits. Microbiology. 145:1999;1123-1135.
22. 6-Tag and maltose-binding-protein double-affinity fusion system. Protein Expr. Purif. 10:1997;309-319.
23. Omer C.A., Diehl R.E., Kral A.M. Bacterial expression and purification of human protein prenyltransferases using epitope-tagged, translationally coupled systems. Methods Enzymol. 250:1995;3-12.
24. Kelly R., Card D., Register E., Mazur P., Kelly T., Tanaka K., Onishi J., Williamson J.M., Fan H., Satoh T., Kurtz M. Geranylgeranyltransferase I of Candida albicans: null mutants or enzyme inhibitors produce unexpected phenotypes. J. Bacteriol. 182:2000;704-713.
25. Dolence J.M., Cassidy P.B., Mathis J.R., Poulter C.D. Yeast protein farnesyltransferase steady-state kinetic studies of substrate binding. Biochemistry. 34:1995;16687-16694.
26. Mayer M.P., Prestwich G.D., Dolence J.M., Bond P.D., Wu H., Poulter C.D. Protein farnesyltransferase production in Escherichia coli and immunoaffinity purification of the heterodimer from Saccharomyces cerevisiae. Gene. 132:1993;41-47.
27. Omer C.A., Kral A.M., Diehl R.E., Prendergast G.C., Powers S., Allen C.M., Gibbs J.B., Kohl N.E. Characterization of recombinant human farnesyl-protein transferase: cloning, expression, farnesyl diphosphate binding, and functional homology with yeast prenyl-protein transferases. Biochemistry. 32:1993;5167-5176.
28. Stirtan W.G., Poulter C.D. Yeast protein geranylgeranyltransferase type-I: overproduction, purification, and characterization. Arch. Biochem. Biophys. 321:1995;182-190.
29. Davison J. Mechanism of control of DNA replication and incompatibility in ColE1-type plasmids-a review. Gene. 28:1984;1-15.
30. Tomizawa J., Itoh T. Plasmid ColE1 incompatibility determined by interaction of RNAI with primer transcript. Proc. Natl. Acad. Sci. USA. 78:1981;6096-6100.
31. -ras farnesyltransferase. J. Biol. Chem. 266:1991;10672-10677.
32. Reiss Y. Substrate interactions of protein prenyltransferases. Methods Enzymol. 250:1995;21-30.
33. Yokoyama K., Zimmerman K., Scholten J., Gelb M.H. Differential prenyl pyrophosphate binding to mammalian protein geranylgeranyltransferase-I and protein farnesyltransferase and its consequence on the specificity of protein prenylation. J. Biol. Chem. 272:1997;3944-3952.
34. Whiteway M., Dignard D., Thomas D.Y. Dominant negative selection of heterologous genes: Isolation of Candida albicans genes that interfere with Saccharomyces cerevisiae mating factor-induced cell cycle arrest. Proc. Natl. Acad. Sci. USA. 89:1992;9410-9414.
35. James G.L., Goldstein J.L., Brown M.S. Polylysine and CVIM sequences of K-RasB dictate specificity of prenylation and confer resistance to benzodiazepine peptidomimetic in vitro. J. Biol. Chem. 270:1995;6221-6226.
36. Zhang F.L., Kirschmeier P., Carr D., James L., Bond R.W., Wang L., Patton R., Windsor W.T., Syto R., Zhang R., Bishop W.R. Characterization of Ha-Ras, N-Ras, Ki-Ras4A, and Ki-Ras4B as in vitro substrates for farnesyl transferase and geranylgeranyl protein transferase type I. J. Biol. Chem. 272:1997;10232-10239.
37. Chen W., Moomaw J.F., Overton L., Kost T.A., Casey P.J. High level expression of mammalian protein farnesyltransferase in a baculovirus system. J. Biol. Chem. 268:1993;9675-9680.
38. Tsao K.-L., Waugh D.S. Balancing the production of two recombinant proteins in Escherichia coli by manipulating plasmid copy number: high-level expression of heterodimeric ras farnesyltransferase. Protein Expr. Purif. 11:1997;233-240.
39. Wu Z., Demma M., Strickland C.L., Syto R., Le H.V., Windsor W.T., Weber P.C. High-level expression, purification, kinetic characterization and crystallization of protein farnesyltransferase β-subunit C-terminal mutants. Prot. Eng. 12:1999;341-348.
40. Pompliano D.L., Schaber M.D., Mosser S.D., Omer C.A., Schafer J.A., Gibbs J.B. Isoprenoid diphosphate utilization by recombinant human farnesyl:protein transferase interactive binding between substrates and a preferred kinetic pathway. Biochemistry. 32:1993;8341-8347.
41. Yokoyama K., McGeady P., Gelb M.H. Mammalian protein geranylgeranyltransferase-I: substrate specificity, kinetic mechanism, metal requirements, and affinity labelling. Biochemistry. 34:1995;1344-1354.
42. Stirtan W.G., Poulter C.D. Yeast protein geranylgeranyltransferase type I: steady-state kinetics and substrate binding. Biochemistry. 36:1997;4552-4557.
43. Caplin B.E., Hettich L.A., Marshall M.S. Substrate characterization of the Saccharomyces cerevisiae protein farnesyltransferase and type-I protein geranylgeranyltransferase. Biochim. Biophys. Acta. 1205:1994;39-48.
44. Williams T.M., Ciccarone T.M., MacTough S.C., Bock R.L., Conner M.W., Davide J.P., Hamilton K., Koblan K.S., Kohl N.E., Kral A.M., Mosser S.D., Omer C.A., Pompliano D.L., Rands E., Schaber M.D., Shah D., Wilson F.R., Gibbs J.B., Graham S.L., Hartman G.D., Oliff A.I., Smith R.L. 2-substituted piperazines as constrained amino acids. Application to the synthesis of potent, non carboxylic acid inhibitors of farnesyltransferase. J. Med. Chem. 39:1996;1345-1348.