Interactions at the Dimer Interface Influence the Relative Efficiencies for Purine Nucleotide Synthesis and Pyrophosphorolysis in a Phosphoribosyltransferase

Journal of Molecular Biology

Volumn 335, Issue 4, 2004, Pages 905-921

  Canyuk, Bhutorn ^b,c   Medrano, Francisco J ^a,b,d   Wenck, Mary Anne ^a,b,e   Focia, Pamela J ^b,f   Eakin, Ann E ^a,b,g   Craig III, Sydney P ^a,b  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c PRINCE OF SONGKLA UNIVERSITY   (Thailand)

^d LABORATÓRIO NACIONAL DE LUZ SÍNCROTRON   (Brazil)

^e IL   (United States)

^f NORTHWESTERN UNIVERSITY   (United States)

^g ASTRAZENECA   (United Kingdom)

Author keywords

Evolution; Hypoxanthine; Mutagenesis; Phosphoribosyltransferase; Structure

Indexed keywords

AMINO ACID; DIMER; GLYCINE; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; LEUCINE; LYSINE; PHOSPHORIBOSYLTRANSFERASE; PURINE NUCLEOTIDE;

AMINO ACID SEQUENCE; ANALYTIC METHOD; ARTICLE; CATALYSIS; CATALYST; CHAGAS DISEASE; CIS TRANS ISOMERISM; CRYSTAL STRUCTURE; DIMERIZATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; EUKARYOTE; NONHUMAN; NUCLEOTIDE METABOLISM; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTOZOON; SITE DIRECTED MUTAGENESIS; TRYPANOSOMA CRUZI; X RAY CRYSTALLOGRAPHY;

EUKARYOTA; PROTOZOA; TRYPANOSOMA; TRYPANOSOMA CRUZI;

EID: 0346493091     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.11.012     Document Type: Article

References (50)

1. Craig S.P., Eakin A.E. Purine phosphoribosyltransferases. J. Biol. Chem. 275:2000;20231-20234.
2. Yuan L., Craig S.P., McKerrow J.H., Wang C.C. Steady-state kinetics of the schistosomal hypoxanthine-guanine phosphoribosyltransferase. Biochemistry. 31:1992;806-810.
3. Xu Y., Eads J., Sacchettini J.C., Grubmeyer C. Kinetic mechanism of human hypoxanthine-guanine phosphoribosyltransferase: rapid phosphoribosyl transfer chemistry. Biochemistry. 36:1997;3700-3712.
4. Munagala N.R., Chin M.S., Wang C.C. Steady-state kinetics of the hypoxanthine-guanine-xanthine phosphoribosyltransferase from Tritrichomonas foetus: the role of threonine-47. Biochemistry. 37:1998;4045-4051.
5. Sculley D.G., Dawson P.A., Emmerson B.T., Gordon R.B. A review of the molecular basis of hypoxanthine-guanine phosphoribosyltransferase (HPRT) deficiency. Hum. Genet. 90:1992;195-207.
6. Walsh C.J., Sherman I.W. Purine and pyrimidine synthesis by the avian malaria parasite Plasmodium lophurae. J. Protozool. 15:1968;763-770.
7. Berens R.L., Krug E.C., Marr J.J. Purine and pyrimidine metabolism. Marr J.J., Muller M. Biochemistry of Parasitic Organisms and its Molecular Foundations. 1995;89-117 Academic Press, San Diego.
8. Ullman B., Carter D. Hypoxanthine-guanine phosphoribosyltransferase as a therapeutic target in protozoal infections. Infect. Agents Dis. 4:1995;29-40.
9. Craig S.P., Eakin A.E. Purine salvage enzymes of parasites as targets for structure based inhibitor design. Parasitol. Today. 13:1997;238-241.
10. Freymann D.M., Wenck M.A., Engel J.C., Feng J., Focia P.J., Eakin A.E., Craig S.P. Efficient identification of inhibitors targeting the closed active site conformation of the HPRT from Trypanosoma cruzi. Chem. Biol. 7:2000;957-968.
11. Medrano F.J., Wenck M.A., Engel J.C., Craig S.P. Analysis of 6-(2,2-dichloroacetamido)chrysene interaction with the hypoxanthine phosphoribosyltransferase from Trypanosoma cruzi. J. Med. Chem. 46:2003;2548-2550.
12. Eads J.C., Scapin G., Xu Y., Grubmeyer C., Sacchettini J.C. The crystal structure of human hypoxanthine-guanine phosphoribosyltransferase with bound GMP. Cell. 78:1994;325-334.
13. Focia P.J., Craig S.P., Nieves-Alicea R., Fletterick R.J., Eakin A.E. A 1.4 Å crystal structure for the hypoxanthine phosphoribosyltransferase of Trypanosoma cruzi. Biochemistry. 37:1998;15066-15075.
14. Focia P.J., Craig S.P., Eakin A.E. Approaching the transition state in the crystal structure of a phosphoribosyltransferase. Biochemistry. 37:1998;17120-17127.
15. Héroux A., White E.L., Ross L.J., Borhani D.W. Crystal structures of the Toxoplasma gondii hypoxanthine-guanine phosphoribosyltransferase-GMP and -IMP complexes: comparison of purine binding interactions with the XMP complex. Biochemistry. 38:1999;14485-14494.
16. 2+ions bound: insights into the catalytic mechanism. Biochemistry. 38:1999;14495-14506.
17. Héroux A., White E.L., Ross L.J., Kuzin A.P., Borhani D.W. Substrate deformation in a hypoxanthine-guanine phosphoribosyltransferase ternary complex: the structural basis for catalysis. Structure. 8:2000;1309-1318.
18. Shi W., Li C.M., Tyler P.C., Furneaux R.H., Grubmeyer C., Schramm V.L., Almo S.C. The 2.0 Å structure of human hypoxanthine-guanine phosphoribosyltransferase in complex with a transition-state analog inhibitor. Nature Struct. Biol. 6:1999;588-593.
19. Shi W., Li C.M., Tyler P.C., Furneaux R.H., Cahill S.M., Girvin M.E., et al. The 2.0 Å structure of malarial purine phosphoribosyltransferase in complex with a transition-state analogue inhibitor. Biochemistry. 38:1999;9872-9880.
20. Shi W., Munagala N.R., Wang C.C., Li C.M., Tyler P.C., Furneaux R.H., et al. Crystal structures of Giardia lamblia guanine phosphoribosyltransferase at 1.75 Å Biochemistry. 39:2000;6781-6790.
21. Somoza J.R., Chin M.S., Focia P.J., Wang C.C., Fletterick R.J. Crystal structure of the hypoxanthine-guanine-xanthine phosphoribosyltransferase from the protozoan parasite Tritrichomonas foetus. Biochemistry. 35:1996;7032-7040.
22. Schumacher M.A., Carter D., Roos D.S., Ullman B., Brennan R.G. Crystal structures of Toxoplasma gondii HGXPRTase reveal the catalytic role of a long flexible loop. Nature Struct. Biol. 3:1996;881-887.
23. Allen T.E., Ullman B. Molecular characterization and overexpression of the hypoxanthine-guanine phosphoribosyltransferase gene from Trypanosoma cruzi. Mol. Biochem. Parasitol. 65:1994;233-245.
24. Vos S., Parry R.J., Burns M.R., de Jersey J., Martin J.L. Structures of free and complexed forms of Escherichia coli xanthine-guanine phosphoribosyltransferase. J. Mol. Biol. 282:1998;875-889.
25. Canyuk B., Focia P.J., Eakin A.E. The role for an invariant aspartic acid in hypoxanthine phosphoribosyltransferases is examined using saturation mutagenesis, functional analysis, and X-ray crystallography. Biochemistry. 40:2001;2754-2765.
26. Eakin A.E., Guerra A., Focia P.J., Torres-Martinez J., Craig S.P. Hypoxanthine phosphoribosyltransferase from Trypanosoma cruzi as a target for structure-based inhibitor design: crystallization and inhibition studies with purine analogs. Antimicrob. Agents Chemother. 41:1997;1686-1692.
27. Lee, C. C. (1999). Structure-function studies of hypoxanthine phosphoribosyltransferases. PhD thesis, University of North Carolina at Chapel Hill.
28. Jones T.A., Zhou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
29. Ramachandran G.N., Mitra A.K. An explanation for the rare occurrence of cis peptide units in proteins and polypeptides. J. Mol. Biol. 107:1976;85-92.
30. Vos S., de Jersey J., Martin J.L. Crystal structure of Escherichia coli xanthine phosphoribosyltransferase. Biochemistry. 36:1997;4125-4134.
31. Lee C.C., Craig S.P., Eakin A.E. A single amino acid substitution in the human and a bacterial hypoxanthine phosphoribosyltransferase modulates specificity for the binding of guanine. Biochemistry. 37:1998;3491-3498.
32. Chin M.S., Wang C.C. Isolation, sequencing and expression of the gene encoding hypoxanthine-guanine-xanthine phosphoribosyltransferase of Tritrichomonas foetus. Mol. Biochem. Parasitol. 63:1994;221-229.
33. Sommer J.M., Ma H., Wang C.C. Cloning, expression and characterization of an unusual guanine phosphoribosyltransferase from Giardia lamblia. Mol. Biochem. Parasitol. 78:1996;185-193.
34. Page J.P., Munagala N.R., Wang C.C. Point mutations in the guanine phosphoribosyltransferase from Giardia lamblia modulate pyrophosphate binding and enzyme catalysis. Eur. J. Biochem. 259:1999;565-571.
35. 2+, and the inhibitor HPP reveals the involvement of the flexible loop in substrate binding. Protein Sci. 8:1999;1023-1031.
36. Jochimsen B., Nygaard P., Vestergaard T. Location on the chromosome of Escherichia coli of genes governing purine metabolism. Mol. Gen. Genet. 143:1975;85-91.
37. Craig S.P., Yuan L., Kuntz D.A., McKerrow J.H., Wang C.C. High level expression in Escherichia coli of soluble, enzymatically active schistosomal hypoxanthine/guanine phosphoribosyltransferase and trypanosomal ornithine decarboxylase. Proc. Natl Acad. Sci. USA. 88:1991;2500-2504.
38. Sambrook J., Fritsch E.F., Maniatis T. Nolan C. Molecular Cloning. A Laboratory Manual. 2nd edit. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
39. Canyuk B., Craig S.P., Eakin A.E. Bacterial complementation as a means to test enzyme-ligand interactions. Appl. Microbiol. Biotechnol. 50:1998;181-186.
40. Giacomello A., Salerno C. Human hypoxanthine-guanine phosphoribosyltransferase-steady state kinetics of the forward and reverse reactions. J. Biol. Chem. 253:1978;6038-6044.
41. Kalckar H.M. Differential spectrophotometry of purine compounds by means of specific enzymes. I. Determination of hydroxypurine compounds. J. Biol. Chem. 167:1947;429-443.
42. Segel I.H. Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-state Enzyme Systems. 1975;Wiley, New York.
43. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Carter C.W.J., Sweet R.M. Methods in Enzymology, Macromolecular Crystallography, Part A. vol. 276:1997;307-326 Academic Press, New York.
44. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763.
45. Brünger A.T. XPLOR, Version 3.1, A System for Crystallography and NMR. 1992;Yale University Press, New Haven, CT.
46. Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallog. sect. A. 50:1994;157-163.
47. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921.
48. Roussel, A. & Cambilleau, C. (1992). TURBO-FRODO, Biographics, LCCMB, Marseille, France.
49. Laskowski R.A., McArthur M.W., Moss D.S., Thornton J. PROCHECK: a program to check the quality of protein structures. J. Appl. Crystallog. 26:1993;282-291.
50. Evans S.V. SETOR: hardware lighted three-dimensional solid model representations of macromolecules. J. Mol. Graph. 11:134-138