Naturally occurring Phe151Leu substitution near a conserved folding module lowers stability of glutathione transferase P1-1

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1649, Issue 1, 2003, Pages 16-23

  Lin, Henry J ^a   Johansson, Ann Sofie ^b,e   Stenberg, Gun ^b   Materi, Alicia M ^a   Park, Jae Man ^a   Dai, Aihua ^a   Zhou, Haiyan ^a   Gim, Jason S Y ^a   Kau, Irving H ^a   Hardy, Steven I ^c   Parker, Michael W ^d   Mannervik, Bengt ^b  

^a HARBOR UCLA MEDICAL CENTER   (United States)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^e MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Folding module; GST motif II; GSTP1 variant

Indexed keywords

BENZYL THIOCYANATE; GLUTATHIONE TRANSFERASE; LEUCINE; PHENETHYL ISOTHIOCYANATE; PHENYLALANINE; SERINE; SULFORAPHANE; 1 CHLORO 2,4 DINITROBENZENE; GLUTATHIONE TRANSFERASE P1; GSTP1 PROTEIN, HUMAN; ISOENZYME;

ALLELE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CANCER PREVENTION; CHEMOPROPHYLAXIS; CONJUGATION; DNA POLYMORPHISM; ENZYME BINDING; ENZYME KINETICS; ENZYME METABOLISM; ENZYME POLYMORPHISM; ENZYME PURIFICATION; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; ESCHERICHIA COLI; GENE EXPRESSION SYSTEM; GENETIC CONSERVATION; HALF LIFE TIME; HYDROPHOBICITY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FOLDING; PROTEIN FUNCTION; STRUCTURE ANALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENETICS; HUMAN; KINETICS; METABOLISM; NEGRO; PROTEIN MOTIF;

ESCHERICHIA COLI;

AFRICAN CONTINENTAL ANCESTRY GROUP; AMINO ACID MOTIFS; AMINO ACID SUBSTITUTION; DINITROCHLOROBENZENE; ENZYME STABILITY; GLUTATHIONE S-TRANSFERASE PI; GLUTATHIONE TRANSFERASE; HALF-LIFE; HUMANS; HYDROPHOBICITY; ISOENZYMES; KINETICS; LEUCINE; MODELS, MOLECULAR; PHENYLALANINE; POLYMORPHISM, GENETIC; PROTEIN FOLDING; VARIATION (GENETICS);

EID: 0041620483     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1570-9639(03)00149-3     Document Type: Article

References (44)

1. Johansson A.-S., Mannervik B. Interindividual variability of glutathione transferase expression. Pacifici G.M., Pelkonen O. Interindividual Variability in Human Drug Metabolism. 2001;460-519 Taylor & Francis, London.
2. Guthenberg C., Åkerfeldt K., Mannervik B. Purification of glutathione-S-transferase from human placenta. Acta Chem. Scand., B. 33:1979;595-596.
3. Polidoro G., Di Ilio C., Del Boccio G., Zulli P., Federici G. Glutathione S-transferase activity in human placenta. Biochem. Pharmacol. 29:1980;1677-1680.
4. Guthenberg C., Mannervik B. Glutathione S-transferase (transferase π) from human placenta is identical or closely related to glutathione S-transferase (transferase ρ) from erythrocytes. Biochim. Biophys. Acta. 661:1981;255-260.
5. Soma Y., Satoh K., Sato K. Purification and subunit-structural and immunological characterization of five glutathione S-transferases in human liver, and the acidic form as a hepatic tumor marker. Biochim. Biophys. Acta. 869:1986;247-258.
6. Mannervik B. The isoenzymes of glutathione transferase. Advan. Enzymol. Relat. Areas Mol. Biol. 57:1985;357-417.
7. Kitahara A., Satoh K., Nishimura K., Ishikawa T., Ruike K., Sato K., Tsuda H., Ito N. Changes in molecular forms of rat hepatic glutathione S-transferase during chemical hepatocarcinogenesis. Cancer Res. 44:1984;2698-2703.
8. Satoh K., Kitahara A., Soma Y., Inaba Y., Hatayama I., Sato K. Purification, induction, and distribution of placental glutathione transferase: a new marker enzyme of preneoplastic cells in the rat chemical hepatocarcinogenesis. Proc. Natl. Acad. Sci. U. S. A. 82:1985;3964-3968.
9. Knoll B.J., Longley M., Sell S. Cloning of a cDNA encoding the rat placental glutathione S-transferase: overproduction of the mRNA in hepatocellular carcinomas. Tumour Biol. 7:1986;123-135.
10. Moscow J.A., Townsend A.J., Goldsmith M.E., Whang-Peng J., Vickers P.J., Poisson R., Legault-Poisson S., Myers C.E., Cowan K.H. Isolation of the human anionic glutathione S-transferase cDNA and the relation of its gene expression to estrogen-receptor content in primary breast cancer. Proc. Natl. Acad. Sci. U. S. A. 85:1988;6518-6522.
11. Morrow C.S., Cowan K.H., Goldsmith M.E. Structure of the human genomic glutathione S-transferase-π gene. Gene. 75:1989;3-11.
12. Ahmad H., Wilson D.E., Fritz R.R., Singh S.V., Medh R.D., Nagle G.T., Awasthi Y.C., Kurosky A. Primary and secondary structural analyses of glutathione S-transferase pi from human placenta. Arch. Biochem. Biophys. 278:1990;398-408.
13. Zimniak P., Nanduri B., Pikula S., Bandorowicz-Pikula J., Singhal S.S., Srivastava S.K., Awasthi S., Awasthi Y.C. Naturally occurring human glutathione S-transferase GSTP1-1 isoforms with isoleucine and valine in position 104 differ in enzymic properties. Eur. J. Biochem. 224:1994;893-899.
14. Ali-Osman F., Akande O., Antoun G., Mao J.-X., Buolamwini J. Molecular cloning, characterization, and expression in Escherichia coli of full-length cDNAs of three human glutathione S-transferase pi gene variants. Evidence for differential catalytic activity of the encoded proteins. J. Biol. Chem. 272:1997;10004-10012.
15. Johansson A.-S., Stenberg G., Widersten M., Mannervik B. Structure-activity relationships and thermal stability of human glutathione transferase P1-1 governed by the H-site residue 105. J. Mol. Biol. 278:1998;687-698.
16. Welfare M., Adeokun A.M., Bassendine M.F., Daly A.K. Polymorphisms in GSTP1, GSTM1, and GSTT1 and susceptibility to colorectal cancer. Cancer Epidemiol. Biomark. Prev. 8:1999;289-292.
17. Millikan R., Pittman G., Tse C.-K., Savitz D.A., Newman B., Bell D. Glutathione S-transferases M1, T1, and P1 and breast cancer. Cancer Epidemiol. Biomark. Prev. 9:2000;567-573.
18. Shepard T.F., Platz E.A., Kantoff P.W., Nelson W.G., Isaacs W.B., Freije D., Febbo P.G., Stampfer M.J., Giovannucci E. No association between the I105V polymorphism of the glutathione S-transferase P1 gene (GSTP1) and prostate cancer risk: a prospective study. Cancer Epidemiol. Biomark. Prev. 9:2000;1267-1268.
19. Henderson C.J., Smith A.G., Ure J., Brown K., Bacon E.J., Wolf C.R. Increased skin tumorigenesis in mice lacking pi class glutathione S-transferases. Proc. Natl. Acad. Sci. U. S. A. 95:1998;5275-5280.
20. 105Val polymorphism. Cancer Res. 60:2000;5621-5624.
21. Stoehlmacher J., Park D.J., Zhang W., Groshen S., Tsao-Wei D.D., Yu M.C., Lenz H.-J. Association between glutathione S-transferase P1, T1, and M1 genetic polymorphism and survival of patients with metastatic colorectal cancer. J. Natl. Cancer Inst. 94:2002;936-942.
22. Allan J.M., Wild C.P., Rollinson S., Willett E.V., Moorman A.V., Dovey G.J., Roddam P.L., Roman E., Cartwright R.A., Morgan G.J. Polymorphism in glutathione S-transferase P1 is associated with susceptibility to chemotherapy-induced leukemia. Proc. Natl. Acad. Sci. U. S. A. 98:2001;11592-11597.
23. Koonin E.V., Mushegian A.R., Tatusov R.L., Altschul S.F., Bryant S.H., Bork P., Valencia A. Eukaryotic translation elongation factor 1 gamma contains a glutathione transferase domain - study of a diverse, ancient protein superfamily using motif search and structural modeling. Protein Sci. 3:1994;2045-2054.
24. Muñoz V., Blanco F.J., Serrano L. The hydrophobic-staple motif and a role for loop-residues in α-helix stability and protein folding. Nat. Struct. Biol. 2:1995;380-385.
25. Stenberg G., Dragani B., Cocco R., Mannervik B., Aceto A. A conserved "hydrophobic staple motif" plays a crucial role in the refolding of human glutathione transferase P1-1. J. Biol. Chem. 275:2000;10421-10428.
26. Cocco R., Stenberg G., Dragani B., Principe D.R., Paludi D., Mannervik B., Aceto A. The folding and stability of human alpha class glutathione transferase A1-1 depend on distinct roles of a conserved N-capping box and hydrophobic staple motif. J. Biol. Chem. 276:2001;32177-32183.
27. Lin H.J., Han C.-Y., Lin B.K., Hardy S. Ethnic distribution of slow acetylator mutations in the polymorphic N-acetyltransferase (NAT2) gene. Pharmacogenetics. 4:1994;125-134.
28. Ganguly A., Rock M.J., Prockop D.J. Conformation-sensitive gel electrophoresis for rapid detection of single-base differences in double-stranded PCR products and DNA fragments: evidence for solvent-induced bends in DNA heteroduplexes. Proc. Natl. Acad. Sci. U. S. A. 90:1993;10325-10329.
29. Körkkö J., Annunen S., Pihlajamaa T., Prockop D.J., Ala-Kokko L. Conformation sensitive gel electrophoresis for simple and accurate detection of mutations: comparison with denaturing gradient gel electrophoresis and nucleotide sequencing. Proc. Natl. Acad. Sci. U. S. A. 95:1998;1681-1685.
30. Jones T.A., Zou J.-Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron-density maps and the location of errors in these models. Acta Crystallogr. A47:1991;110-119.
31. Hayes J.D., Strange R.C. Glutathione S-transferase polymorphisms and their biological consequences. Pharmacology. 61:2000;154-166.
32. Watson M.A., Stewart R.K., Smith G.B.J., Massey T.E., Bell D.A. Human glutathione S-transferase P1 polymorphisms: relationship to lung tissue enzyme activity and population frequency distribution. Carcinogenesis. 19:1998;275-280.
33. Fenwick G.R., Heaney R.K., Mullin W.J. Glucosinolates and their breakdown products in food and food plants. C.R.C., Crit. Rev. Food Sci. Nutr. 18:1983;123-201.
34. Fahey J.W., Zalcmann A.T., Talalay P. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry. 56:2001;5-51.
35. Kolm R.H., Danielson U.H., Zhang Y., Talalay P., Mannervik B. Isothiocyanates as substrates for human glutathione transferases: structure-activity studies. Biochem. J. 311:1995;453-459.
36. Zhang Y., Kolm R.H., Mannervik B., Talalay P. Reversible conjugation of isothiocyanates with glutathione catalyzed by human glutathione transferases. Biochem. Biophys. Res. Commun. 206:1995;748-755.
37. Shapiro T.A., Fahey J.W., Wade K.L., Stephenson K.K., Talalay P. Human metabolism and excretion of cancer chemoprotective glucosinolates and isothiocyanates of cruciferous vegetables. Cancer Epidemiol. Biomark. Prev. 7:1998;1091-1100.
38. Aceto A., Dragani B., Melino S., Allocati N., Masulli M., Di Ilio C., Petruzzelli R. Identification of an N-capping box that affects the α6-helix propensity in glutathione S-transferase superfamily proteins: a role for an invariant aspartic residue. Biochem. J. 322:1997;229-234.
39. Eriksson A.E., Baase W.A., Zhang X.-J., Heinz D.W., Blaber M., Baldwin E.P., Matthews B.W. Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect. Science. 255:1992;178-183.
40. Rossjohn J., McKinstry W.J., Oakley A.J., Parker M.W., Stenberg G., Mannervik B., Dragani B., Cocco R., Aceto A. Structures of thermolabile mutants of human glutathione transferase P1-1. J. Mol. Biol. 302:2000;295-302.
41. Dragani B., Stenberg G., Melino S., Petruzzelli R., Mannervik B., Aceto A. The conserved N-capping box in the hydrophobic core of glutathione S-transferase P1-1 is essential for refolding. Identification of a buried and conserved hydrogen bond important for protein stability. J. Biol. Chem. 272:1997;25518-25523.
42. Antonarakis S.E. Recommendations for a nomenclature system for human gene mutations. Human Mutat. 11:1998;1-3.
43. Kraulis P.J. MOLSCRIPT - a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24:1991;946-950.
44. Oakley A.J., Rossjohn J., Lo Bello M., Caccuri A.M., Federici G., Parker M.W. The three-dimensional structure of the human Pi class glutathione transferase P1-1 in complex with the inhibitor ethacrynic acid and its glutathione conjugate. Biochemistry. 36:1997;576-585.