Structural and biochemical characterization of the folyl-poly-γ- l -glutamate hydrolyzing activity of human glutamate carboxypeptidase II

FEBS Journal

Volumn 281, Issue 14, 2014, Pages 3228-3242

  Navrátil, Michal ^a,b   Ptáček, Jakub ^b,c   Šácha, Pavel ^a,b   Starková, Jana ^a   Lubkowski, Jacek ^d   Bařinka, Cyril ^c   Konvalinka, Jan ^a,b  

^a INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c INSTITUTE OF BIOTECHNOLOGY   (Czech Republic)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

arene binding site; crystal structure; folate hydrolase 1; H475Y(1561C T) polymorphism; zinc metalloprotease

Indexed keywords

FOLYL POLY GAMMA LEVO GLUTAMIC ACID; GLUTAMATE CARBOXYPEPTIDASE II; PTEROPTIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTALLIZATION; CRYSTALLOGRAPHY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SUBSTRATE COMPLEX; HUMAN; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN POLYMORPHISM; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; THERMOSTABILITY;

ARENE-BINDING SITE; CRYSTAL STRUCTURE; FOLATE HYDROLASE 1; H475Y(1561C→T) POLYMORPHISM; ZINC METALLOPROTEASE;

ANTIGENS, SURFACE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; ENZYME STABILITY; GLUTAMATE CARBOXYPEPTIDASE II; HOT TEMPERATURE; HUMANS; KINETICS; MODELS, MOLECULAR; POLYGLUTAMIC ACID; POLYMORPHISM, GENETIC;

EID: 84904732507     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12857     Document Type: Article

References (39)

1. Israeli RS, Powell CT, Fair WR, &, Heston WD, (1993) Molecular cloning of a complementary DNA encoding a prostate-specific membrane antigen. Cancer Res 53, 227-230.
2. Robinson MB, Blakely RD, Couto R, &, Coyle JT, (1987) Hydrolysis of the brain dipeptide N-acetyl-L-aspartyl-L-glutamate. Identification and characterization of a novel N-acetylated alpha-linked acidic dipeptidase activity from rat brain. J Biol Chem 262, 14498-14506.
3. Mesters JR, Barinka C, Li WX, Tsukamoto T, Majer P, Slusher BS, Konvalinka J, &, Hilgenfeld R, (2006) Structure of glutamate carboxypeptidase II, a drug target in neuronal damage and prostate cancer. EMBO J 25, 1375-1384.
4. Klusak V, Barinka C, Plechanovova A, Mlcochova P, Konvalinka J, Rulisek L, &, Lubkowski J, (2009) Reaction mechanism of glutamate carboxypeptidase II revealed by mutagenesis, X-ray crystallography, and computational methods. Biochemistry 48, 4126-4138.
5. Barinka C, Rojas C, Slusher B, &, Pomper M, (2012) Glutamate carboxypeptidase II in diagnosis and treatment of neurologic disorders and prostate cancer. Curr Med Chem 19, 856-870.
6. Pavlicek J, Ptacek J, &, Barinka C, (2012) Glutamate carboxypeptidase II: an overview of structural studies and their importance for structure-based drug design and deciphering the reaction mechanism of the enzyme. Curr Med Chem 19, 1300-1309.
7. Pinto JT, Suffoletto BP, Berzin TM, Qiao CH, Lin S, Tong WP, May F, Mukherjee B, &, Heston WD, (1996) Prostate-specific membrane antigen: a novel folate hydrolase in human prostatic carcinoma cells. Clin Cancer Res 2, 1445-1451.
8. Halsted CH, Wong DH, Peerson JM, Warden CH, Refsum H, Smith AD, Nygard OK, Ueland PM, Vollset SE, &, Tell GS, (2007) Relations of glutamate carboxypeptidase II (GCPII) polymorphisms to folate and homocysteine concentrations and to scores of cognition, anxiety, and depression in a homogeneous Norwegian population: the Hordaland Homocysteine Study. Am J Clin Nutr 86, 514-521.
9. Vargas-Martinez C, Ordovas JM, Wilson PW, &, Selhub J, (2002) The glutamate carboxypeptidase gene II (C>T) polymorphism does not affect folate status in the Framingham Offspring cohort. J Nutr 132, 1176-1179.
10. Chen J, Kyte C, Valcin M, Chan W, Wetmur JG, Selhub J, Hunter DJ, &, Ma J, (2004) Polymorphisms in the one-carbon metabolic pathway, plasma folate levels and colorectal cancer in a prospective study. Int J Cancer 110, 617-620.
11. Devlin AM, Clarke R, Birks J, Evans JG, &, Halsted CH, (2006) Interactions among polymorphisms in folate-metabolizing genes and serum total homocysteine concentrations in a healthy elderly population. Am J Clin Nutr 83, 708-713.
12. Mir MM, (2008) Combined impact of polymorphism of folate metabolism genes; glutamate carboxypeptidase, methylene tetrahydrofolate reductase and methionine synthase reductase on breast cancer susceptibility in Kashmiri women. Clin Chem 54, A126.
13. Zhang AX, Murelli RP, Barinka C, Michel J, Cocleaza A, Jorgensen WL, Lubkowski J, &, Spiegel DA, (2010) A remote arene-binding site on prostate specific membrane antigen revealed by antibody-recruiting small molecules. J Am Chem Soc 132, 12711-12716.
14. Dunn B, (2012) Proteinases as drug targets., 1st edn. RSC Publishing, Cambridge, UK.
15. Barinka C, Rovenska M, Mlcochova P, Hlouchova K, Plechanovova A, Majer P, Tsukamoto T, Slusher BS, Konvalinka J, &, Lubkowski J, (2007) Structural insight into the pharmacophore pocket of human glutamate carboxypeptidase II. J Med Chem 50, 3267-3273.
16. Devlin AM, Ling EH, Peerson JM, Fernando S, Clarke R, Smith AD, &, Halsted CH, (2000) Glutamate carboxypeptidase II: a polymorphism associated with lower levels of serum folate and hyperhomocysteinemia. Hum Mol Genet 9, 2837-2844.
17. Pokorna J, Machala L, Rezacova P, &, Konvalinka J, (2009) Current and novel inhibitors of HIV protease. Viruses 1, 1209-1239.
18. Barinka C, Mlcochova P, Sacha P, Hilgert I, Majer P, Slusher BS, Horejsi V, &, Konvalinka J, (2004) Amino acids at the N- and C-termini of human glutamate carboxypeptidase II are required for enzymatic activity and proper folding. Eur J Biochem 271, 2782-2790.
19. Luthi-Carter R, Barczak AK, Speno H, &, Coyle JT, (1998) Hydrolysis of the neuropeptide N-acetylaspartylglutamate (NAAG) by cloned human glutamate carboxypeptidase II. Brain Res 795, 341-348.
20. Alquicer G, Sedlak D, Byun Y, Pavlicek J, Stathis M, Rojas C, Slusher B, Pomper MG, Bartunek P, &, Barinka C, (2012) Development of a high-throughput fluorescence polarization assay to identify novel ligands of glutamate carboxypeptidase II. J Biomol Screen 17, 1030-1040.
21. Pietrzik K, Bailey L, &, Shane B, (2010) Folic acid and L-5-methyltetrahydrofolate comparison of clinical pharmacokinetics and pharmacodynamics. Clin Pharmacokinet 49, 535-548.
22. Chen C, Ke JY, Zhou XE, Yi W, Brunzelle JS, Li J, Yong EL, Xu HE, &, Melcher K, (2013) Structural basis for molecular recognition of folic acid by folate receptors. Nature 500, 486-489.
23. Barinka C, Hlouchova K, Rovenska M, Majer P, Dauter M, Hin N, Ko YS, Tsukamoto T, Slusher BS, Konvalinka J, et al,. (2008) Structural basis of interactions between human glutamate carboxypeptidase II and its substrate analogs. J Mol Biol 376, 1438-1450.
24. Hlouchova K, Barinka C, Klusak V, Sacha P, Mlcochova P, Majer P, Rulisek L, &, Konvalinka J, (2007) Biochemical characterization of human glutamate carboxypeptidase III. J Neurochem 101, 682-696.
25. Hlouchova K, Barinka C, Konvalinka J, &, Lubkowski J, (2009) Structural insight into the evolutionary and pharmacologic homology of glutamate carboxypeptidases II and III. FEBS J 276, 4448-4462.
26. Collard F, Vertommen D, Constantinescu S, Buts L, &, Van Schaftingen E, (2011) Molecular identification of beta-citrylglutamate hydrolase as glutamate carboxypeptidase 3. J Biol Chem 286, 38220-38230.
27. Barinka C, Rinnova M, Sacha P, Rojas C, Majer P, Slusher BS, &, Konvalinka J, (2002) Substrate specificity, inhibition and enzymological analysis of recombinant human glutamate carboxypeptidase II. J Neurochem 80, 477-487.
28. Tykvart J, Sacha P, Barinka C, Knedlik T, Starkova J, Lubkowski J, &, Konvalinka J, (2012) Efficient and versatile one-step affinity purification of in vivo biotinylated proteins: expression, characterization and structure analysis of recombinant human glutamate carboxypeptidase II. Protein Expr Purif 82, 106-115.
29. Kibbe WA, (2007) OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res 35, W43-W46.
30. Barinka C, Starkova J, Konvalinka J, &, Lubkowski J, (2007) A high-resolution structure of ligand-free human glutamate carboxypeptidase II. Acta Crystallogr F 63, 150-153.
31. Otwinowski Z, &, Minor W, (1997) Processing of X-ray diffraction data collected in oscillation mode. Meth Enzymol 276, 307-326.
32. Krug M, Weiss MS, Heinemann U, &, Mueller U, (2012) XDSAPP: a graphical user interface for the convenient processing of diffraction data using XDS. J Appl Crystallogr 45, 568-572.
33. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AGW, McCoy A, et al,. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D 67, 235-242.
34. Emsley P, Lohkamp B, Scott WG, &, Cowtan K, (2010) Features and development of Coot. Acta Crystallogr D 66, 486-501.
35. Schuttelkopf AW, &, van Aalten DM, (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr D Biol Crystallogr 60, 1355-1363.
36. Chen VB, Arendall WB III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, &, Richardson DC, (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66, 12-21.
37. Leatherbarrow RJ, (1989 -2004) GraFit, Version 5.0.11, Erithacus Software Ltd, Horley, UK.
38. Roth M, (1971) Fluorescence reaction for amino acids. Anal Chem 43, 880.
39. Ericsson UB, Hallberg BM, DeTitta GT, Dekker N, &, Nordlund P, (2006) Thermofluor-based high-throughput stability optimization of proteins for structural studies. Anal Biochem 357, 289-298.