Expression and characterization of recombinant vitamin K-dependent γ-glutamyl carboxylase from an invertebrate, Conus textile

European Journal of Biochemistry

Volumn 269, Issue 24, 2002, Pages 6162-6172

  Czerwiec, Eva ^a   Begley, Gail S ^a   Bronstein, Mila ^b   Stenflo, Johan ^a,c   Taylor, Kevin ^a   Furie, Barbara C ^a,b   Furie, Bruce ^a,b  

^a MARINE BIOLOGICAL LABORATORY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c LUND UNIVERSITY   (Sweden)

Author keywords

Blood coagulation; Conotoxins; Hemophilia; Posttranslational processing; Vitamin K

Indexed keywords

AMINO ACID DERIVATIVE; BLOOD CLOTTING FACTOR 9; COMPLEMENTARY DNA; PEPTIDE; PHENYLALANYLLEUCYLGLUTAMYLGLUTAMYLLEUCINE; PROTEIN SUBUNIT; PROTHROMBIN; RECOMBINANT ENZYME; UNCLASSIFIED DRUG; VENOM; VITAMIN K DEPENDENT CARBOXYLASE; VITAMIN K GROUP;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BIOSYNTHESIS; CARBOXYLATION; CATTLE; CELL STRAIN COS1; CONTROLLED STUDY; CONUS TEXTILE; ENZYME ACTIVITY; HUMAN; INVERTEBRATE; MOLECULAR BIOLOGY; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY;

1-CARBOXYGLUTAMIC ACID; AMINO ACID SEQUENCE; ANIMALS; BLOOD COAGULATION; BLOTTING, WESTERN; CARBON-CARBON LIGASES; CELL LINE; CLONING, MOLECULAR; COS CELLS; DNA, COMPLEMENTARY; DOSE-RESPONSE RELATIONSHIP, DRUG; GENETIC VECTORS; HUMANS; INSECTS; KINETICS; MICROSOMES; MOLECULAR SEQUENCE DATA; MOLLUSCA; OPEN READING FRAMES; PLASMIDS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; VITAMIN K;

ANIMALIA; BOS TAURUS; BOVINAE; CONUS TEXTILE; GASTROPODA; INSECTA; INVERTEBRATA; VERTEBRATA;

EID: 0036452863     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2002.03335.x     Document Type: Article

References (54)

1. Furie, B., Bouchard, B.A. & Furie, B.C. (1999) Vitamin K-dependent biosynthesis of gamma-carboxyglutamic acid. Blood 93, 1798-1808.
2. Stenflo, J. (1999) Contributions of Gla and EFG-like domains to the function of vitamin K-dependent coagulation factors. Crit. Rev. Eukaryotic Gene Expression 9, 59-88.
3. Dowd, P., Hershline, R., Ham, S.W. & Naganathan, S. (1995) Vitamin K and energy transduction: A base strength amplification mechanism. Science. 269, 1684.
4. Morris, D.P., Soute, B.A.M., Vermeer, C. & StaRord, D.W. (1993) Characterization of the purified vitamin K-dependent γ-glutamyl carboxylase. J. Biol. Chem. 268, 8735-8742.
5. Jorgensen, M.J., Cantor, A.B., Furie, B.C., Brown, C.L., Shoemaker, C.B. & Furie, B. (1987) Recognition site directing vitamin K-dependent γ-carboxylation resides on the propeptide of factor IX. Cell 48, 185.
6. Ulrich, M.M., Furie, B., Jacobs, M.R., Vermeer, C. & Furie, B.C. (1988) Vitamin K-dependent carboxylation. A synthetic peptide based upon the gamma-carboxylation recognition site sequence of the prothrombin propeptide is an active substrate for the carboxylase in vitro. J. Biol. Chem. 263, 9697-9702.
7. Furie, B.C., Ratcliffe, J.V., Tward, J., Jorgensen, M.J., Blaszkowsky, L.S., DiMichele, D. & Furie, B. (1997) The gamma-carboxylation recognition site is sufficient to direct vitamin K-dependent carboxylation on an adjacent glutamate-rich region of thrombin in a propeptide-thrombin chimera. J. Biol. Chem. 272, 28258-28262.
8. Wu, S.-M., Cheung, W.-F., Frazier, D. & Stafford, D.W. (1991) Cloning and expression of the cDNA for human γ-glutamyl carboxylase. Science 254, 1634-1636.
9. Rehemtulla, A., Roth, D.A., Wasley, L.C., Kuliopulos, A., Walsh, C.T., Furie, B., Furie, B.C. & Kaufman, R.J. (1993) In vitro and in vivo functional characterization of bovine vitamin K-dependent gamma-carboxylase expressed in Chinese hamster ovary cells. Proc. Natl. Acad. Sci. USA 90, 4611-4615.
10. Begley, G.S., Furie, B.C., Czerwiec, E., Taylor, K.L., Furie, G.L., Bronstein, L., Stenflo, J. & Furie, B. (2000) A conserved motif within the vitamin K-dependent carboxylase gene is widely distributed across animal phyla. J. Biol. Chem. 275, 36245-36249.
11. Romero, E.E., Deo, R., Velazquez-Estades, L.J. & Roth, D.A. (1998) Cloning, structural organization, and transcriptional activity of the rat vitamin K-dependent gamma-glutamyl carboxylase gene. Biochem. Biophys. Res. Commun. 248, 783-788.
12. Wu, S.-M., Morris, D.P. & Stafford, D.W. (1991) Identification and purification to near homogeneity of the vitamin K-dependent carboxylase. Proc. Natl. Acad. Sci. USA 88, 2236-2240.
13. Carlisle, T.L. & Suttie, J.W. (1980) Vitamin K dependent carboxylase: Subcellular localization of the carboxylase and enzymes involved in vitamin K metabloism in rat liver. Biochemistry 19, 1161-1167.
14. Bristol, J.A., Ratcliffe, J.V., Roth, D.A., Jacobs, M.A., Furie, B.C & Furie, B. (1996) Biosynthesis of prothrombin: Intracellular localization of the vitamin K-dependent carboxylase and the sites of gamma-carboxylation. Blood 88, 2585-2593.
15. Kuliopulos, A., Nelson, N.P., Yamada, M., Walsh, C.T., Furie, B., Furie, B.C. & Roth, D.A. (1994) Localization of the affinity peptide-substrate inactivator site on recombinant vitamin K-dependent carboxylase. J. Biol. Chem. 269, 21364-21370.
16. Sugiura, I., Furie, B., Walsh, C.T. & Furie, B.C. (1996) Profactor IX propeptide and glutamate substrate binding sites on the vitamin K-dependent carboxylase identified by site-directed mutagenesis. J. Biol. Chem. 271, 17837-17844.
17. Yamada, M., Kuliopulos, A., Nelson, N.P., Roth, D.A., Furie, B., Furie, B.C. & Walsh, C.T. (1995) Localization of the Factor IX propeptide binding site on recombinant vitamin K dependent carboxylase using benzoylphenylalanine photoaffinity peptide inactivators. Biochemistry 34, 481-489.
18. Wu, S.M., Mutucumarana, V.P., Geromanos, S. & Stafford, D.W. (1997) The propeptide binding site of the bovine gamma-glutamyl carboxylase. J. Biol. Chem. 272, 11718-11722.
19. Roth, D.A., Whirl, M.L., Velazquez-Estades, L.J., Walsh, C.T., Furie, B. & Furie, B.C. (1995) Mutagenesis of vitamin K-dependent carboxylase demonstrates a carboxyl terminus-mediated interaction with vitamin K hydroquinone. J. Biol. Chem. 270, 5305-5311.
20. Maillet, M., Morris, D., Gaudry, M. & Marquet, M. (1997) The active site region of the vitaminK-dependent carboxylase includes both the amino-terminal hydrophobic and carboxy-terminal hydrophilic domains of the protein. FEBS Lett. 413, 1.
21. Bouchard, B.A., Furie, B. & Furie, B.C. (1999) Glutamyl substrate-induced exposure of a free cysteine residue in the vitamin K-dependent gamma-glutamyl carboxylase is critical for vitamin K epoxidation. Biochemistry 38, 9517-9523.
22. Pudota, B.N., Miyagi, M., Hallgren, K.W., West, K.A., Crabb, J.W., Misono, K.S. & Berkner, K.L. (2000) Identification of the vitamin K-dependent carboxylase active site: Cys-99 and Cys-450 are required for both epoxidation and carboxylation. Proc. Natl. Acad. Sci. USA 97, 13033-13038.
23. McIntosh, J., Olivera, B., Cruz, L. & Gray, W. (1984) Gamma-carboxyglutamate in a neuroactive toxin. J. Biol. Chem. 259, 14343-14346.
24. Hauschka, P.V., Mullen, E.A., Hintsch, G. & Jazwinski, S. (1988) Abundant occurrence of γ-carboxyglutamic acid (Gla)-containing peptides in the marine gastropod family conidae. Current Advances in Vitamin K Research (Suttie, J.W., ed.), pp. 237-243. Elsevier, New York.
25. Olivera, B.M., Gray, W.R., Zeikus, R., McIntosh, J.M., Varga, J., Rivier, J., de Santos, V. & Cruz, L.J. (1985) Peptide neurotoxins from fish-hunting cone snails. Science 230, 1338-1343.
26. Olivera, B.M., Rivier, J., Scott, J.K., Hillyard, D.R. & Cruz, L.J. (1991) Conotoxins. J. Biol. Chem. 266, 22067-22070.
27. Haack, J.A., Rivier, J., Parks, T.N., Mena, E.E., Cruz, L.J. & Olivera, B.M. (1990) Conantokin-T. A gamma-carboxyglutamate containing peptide with N-methyl-D-aspartate antagonist activity. J. Biol. Chem. 265, 6025-6029.
28. Fainzilber, M., Gordon, D., Hasson, A., Spira, M.E. & Zlotkin, E. (1991) Mollusc-specific toxins from the venom of Conus textile neovicarius. Eur. J. Biochem. 202, 589-595.
29. Nakamura, T., Yu. Z., Fainzilber, M. & Burlingame, A.L. (1996) Mass spectrometric-based revision of the structure of a cysteine-rich peptide toxin with gamma-carboxyglutamic acid, TxVIIA, from the sea snail, Conus textile. Protein Sci. 5, 524-530.
30. Kalume, D.E., Stenflo, J., Czerwiec, E., Hambe, B., Furie, B.C., Furie, B. & Roepstorff, P. (2000) Structure determination of two conotoxins from Conus textile by a combination of matrix-assisted laser desorption/ionization time-of-flight and electrospray ionization mass spectrometry and biochemical methods. J. Mass Spectrom. 35, 145-156.
31. Fainzilber, M., Nakamura, T., Lodder, J.C., Zlotkin, E., Kits, K.S. & Burlingame, A.L. (1998) gamma-Conotoxin-PnVIIA, a gamma-carboxyglutamate-containing peptide agonist of neuronal pacemaker cation currents. Biochemistry 37, 1470-1477.
32. Prorok, M., Warder, S.E., Blandl, T. & Castellino, F.J. (1996) Calcium binding properties of synthetic gamma-carboxyglutamic acid-containing marine cone snail 'sleeper' peptides, conantokin-G and conantokin-T. Biochemistry 35, 16528-16534.
33. Blandl, T., Zajicek, J., Prorok, M. & Castellino, F.J. (1997) Metal-ion-binding properties of synthetic conantokin-G. Biochem. J. 328, 777-783.
34. Prorok, M. & Castellino, F.J. (1998) Thermodynamics of binding of calcium, magnesium, and zinc to the N-methyl-D-aspartate receptor ion channel peptidic inhibitors, conantokin-G and conantokin-T. J. Biol. Chem. 273, 19573-19578.
35. Blandl, T., Warder, S.E., Prorok, M. & Castellino, F.J. (2000) Structure-function relationships of the NMDA receptor antagonist peptide, conantokin-R. FEBS Lett. 470, 139-146.
36. Skjaerbaek, N., Nielsen, K.J., Lewis, R.J., Alewood, P. & Craik, D.J. (1997) Determination of the solution structures of conantokin-G and conantokin-T by CD and NMR spectroscopy. J. Biol. Chem. 272, 2291-2299.
37. Rigby, A.C., Baleja, J.D., Furie, B.C. & Furie, B. (1997) Three-dimensional structure of a gamma-carboxyglutamic acid-containing conotoxin, conantokin G, from the marine snail Conus geographus: The metal-free conformer. Biochemistry 36, 6906-6914.
38. Chen, Z., Blandl, T., Prorok, M., Warder, S.E., Li, L., Zhu, Y., Pedersen, L.G., Ni, F. & Castellino, F.J. (1998) Conformational changes in conantokin-G induced upon binding of calcium and magnesium as revealed by NMR structural analysis. J. Biol. Chem. 273, 16248-16258.
39. Rigby, A.C., Baleja, J.D., Li, L., Pedersen, L.G., Furie, B.C. & Furie, B. (1997) Role of gamma-carboxyglutamic acid in the calcium-induced structural transition of conantokin G, a conotoxin from the marine snail Conus geographus. Biochemistry 36, 15677-15684.
40. 2+ influx. Proc. Natl Acad. Sci. USA 96, 5758-5763.
41. Stanley, T.B., Stafford, D.W., Olivera, B.M. & Bandyopadhyay, P.K. (1997) Identification of a vitamin K-dependent carboxylase in the venom duct of a Conus snail. FEBS Lett. 407, 85-88.
42. Bandyopadhyay, P.K., Colledge, C.J., Walker, C.S., Zhou, L.M., Hillyard, D.R. & Olivera, B.M. (1998) Conantokin-G precursor and its role in gamma-carboxylation by a vitamin K-dependent carboxylase from a Conus snail. J. Biol. Chem. 273, 5447-5450.
43. Bush, K.A., Stenflo, J., Roth, D.A., Czerwiec, E., Harrist, A., Begley, G.S., Furie, B.C. & Furie, B. (1999) Hydrophobic amino acids define the carboxylation recognition site in the precursor of the gamma-carboxyglutamic-acid-containing conotoxin epsilon-TxIX from the marine cone snail Conus textile. Biochemistry 38, 14660-14666.
44. Li, T., Yang, C. & Stafford, D. (2000) Identification of a Drosophila vitamin K-dependent gamma-glutamyl carboxylase. J. Biol. Chem. 275, 18291-18296.
45. Walker, C.S., Shetty, R.P., Clark, K., Kazuko, S.G., Letsou, A., Olivera, B.M. & Bandyopadhyay, P.K. (2001) On a potential global role for vitamin K-dependent gamma-carboxylation in animal systems. Evidence for a gamma-glutamyl carboxylase in Drosophila. J. Biol. Chem. 276, 7769-7774.
46. Jacobs, M., Freedman, S.J., Furie, B.C. & Furie, B. (1994) Membrane binding properties of the Factor IX γ-carboxyglutamic acid-rich domain prepared by chemical synthesis. J. Biol. Chem. 269, 25494-25501.
47. Tie, J., Wu, S.M., Jin, D., Nicchitta, C.V. & Stafford, D.W. (2000) A topological study of the human gamma-glutamyl carboxylase. Blood 96, 973-978.
48. Hubbard, B.R., Jacobs, M., Ulrich, M.M., Walsh, C., Furie, B. & Furie, B.C. (1989) Vitamin K-dependent carboxylation. In vitro modification of synthetic peptides containing the gamma-carboxylation recognition site. J. Biol. Chem. 264, 14145-14150.
49. Knobloch, J.E. & Suttie, J.W. (1987) Control of enzyme activity by the 'propeptide' region of factor X. J. Biol. Chem. 262, 15334.
50. Soute, B.A.M., Acher, F., Azerad, R. & Vermeer, C. (1990) Vitamin K-dependent carboxylase: Effect of ammonium sulfate on substrate carboxylation and on inhibition by stereospific substrate analogs. Biochim. Biophys. Acta 1034, 11-16.
51. Bandyopadhyay, P.K., Garrett, J.E., Shetty, R.P., Keate, T., Walker, C.S. & Olivera, B.M. (2002) Gamma-glutamyl carboxylation: An extracellular posttranslational modification that antedates the divergence of molluscs, arthropods, and chordates. Proc. Natl. Acad. Sci. USA 99, 1264-1269.
52. Houben, R.J., Rijkers, D.T., Stanley, T.B., Acher, F., Azerad, R., Kakonen, S.M., Vermeer, C. & Soute, B.A. (2002) Characteristics and composition of the vitamin K-dependent gamma-glutamyl carboxylase-binding domain on osteocalcin. Biochem. J. 364, 323-328.
53. Stenflo, J., Ferlund, P., Egan, W. & Roepstorff, P. (1974) Vitamin K dependent modifications of glutamic acid residues in prothrombin. Proc. Natl. Acad. Sci. USA 71, 2730-2733.
54. Nelsestuen, G.L., Zytkovicz, T.H. & Howard, J.B. (1974) The mode of action of vitamin K. Identification of gamma-carboxyglutamic acid as a component of prothrombin. J. Biol. Chem. 249, 6347-6350.