Isolation and characterization of glutaminyl cyclases from Drosophila: Evidence for enzyme forms with different subcellular localization

Biochemistry

Volumn 46, Issue 38, 2007, Pages 10921-10930

  Schilling, Stephan ^a   Lindner, Christiane ^b   Koch, Birgit ^a   Wermann, Michael ^a   Rahfeld, Jens Ulrich ^a   Von Bohlen, Alex ^c   Rudolph, Thomas ^b   Reuter, Gunter ^b   Demuth, Hans Ulrich ^a  

^a PROBIODRUG AG   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^c LEIBNIZ INSTITUT FÜR ANALYTISCHE WISSENSCHAFTEN ISAS E V   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMINYL CYCLASES (QC); IMMUNOCHEMISTRY; ISOENZYMES; SUBCELLULAR LOCALIZATION;

ESCHERICHIA COLI; GENES; HORMONES; PEPTIDES; PH EFFECTS;

ENZYME KINETICS;

ENZYME; GLUTAMINYL CYCLASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ISOLATION; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME SUBSTRATE; ESCHERICHIA COLI; GENE EXPRESSION; GENE SEQUENCE; GENE STRUCTURE; MITOCHONDRION; NONHUMAN; PICHIA PASTORIS; PRIORITY JOURNAL; PROTEIN TARGETING;

AMINO ACID SEQUENCE; AMINOACYLTRANSFERASES; ANIMALS; CATALYSIS; CELL LINE; CHROMATOGRAPHY, LIQUID; CIRCULAR DICHROISM; CLONING, MOLECULAR; DNA PRIMERS; DROSOPHILA; ENZYME ACTIVATION; ESCHERICHIA COLI; GLUTAMINE; HUMANS; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; PICHIA; PYRROLIDONECARBOXYLIC ACID; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; SUBCELLULAR FRACTIONS; SUBSTRATE SPECIFICITY;

ESCHERICHIA COLI; INVERTEBRATA; MAMMALIA; PICHIA PASTORIS; VERTEBRATA;

EID: 34648825027     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701043x     Document Type: Article

References (34)

1. Abraham, G. N., and Podell, D. N. (1981) Pyroglutamic acid. Nonmetabolic formation, function in proteins and peptides, and characteristics of the enzymes effecting its removal, Mol. Cell. Biochem. 38, 181-190.
2. Fischer, W. H., and Spiess, J. (1987) Identification of a mammalian glutaminyl cyclase converting glutaminyl into pyroglutamyl peptides, Proc. Natl. Acad. Sci. U.S.A. 84, 3628-3632.
3. Saido, T. C., Iwatsubo, T., Mann, D. M., Shimada, H., Ihara, Y., and Kawashima, S. (1995) Dominant and differential deposition of distinct beta-amyloid peptide species, A beta N3(pE), in senile plaques, Neuron 14, 457-466.
4. Ghiso, J., Revesz, T., Holton, J., Rostagno, A., Lashley, T., Houlden, H., Gibb, G., Anderton, B., Bek, T., Bojsen-Moller, M., Wood, N., Vidal, R., Braendgaard, H., Plant, G., and Frangione, B. (2001) Chromosome 13 dementia syndromes as models of neurodegeneration. Amyloid, Amyloid 8, 277-284.
5. Cynis, H., Schilling, S., Bodnar, M., Hoffmann, T., Heiser, U., Saido, T. C., and Demuth, H. U. (2006) Inhibition of glutaminyl cyclase alters pyroglutamate formation in mammalian cells, Biochim. Biophys. Acta 1764, 1618-1625.
6. Busby, W. H. J., Quackenbush, G. E., Humm, J., Youngblood, W. W., and Kizer, J. S. (1987) An enzyme(s) that converts glutaminyl-peptides into pyroglutamyl-peptides. Presence in pituitary, brain, adrenal medulla, and lymphocytes, J. Biol. Chem. 262, 8532-8536.
7. Messer, M. (1963) Enzymatic cyclization of L-glutamine and L-glutaminyl peptides, Nature 4874, 1299.
8. Schilling, S., Hoffmann, T., Manhart, S., Hoffmann, M., and Demuth, H. U. (2004) Glutaminyl cyclases unfold glutamyl cyclase activity under mild acid conditions, FEBS Lett. 563, 191-196.
9. Wintjens, R., Belrhali, H., Clantin, B., Azarkan, M., Bompard, C., Baeyens-Volant, D., Looze, Y., and Villeret, V. (2006) Crystal structure of papaya glutaminyl cyclase, an archetype for plant and bacterial glutaminyl cyclases, J. Mol. Biol. 357, 457-470.
10. Huang, K. F., Liu, Y. L., Cheng, W. J., Ko, T. P., and Wang, A. H. (2005) Crystal structures of human glutaminyl cyclase, an enzyme responsible for protein N-terminal pyroglutamate formation, Proc. Natl. Acad. Sci. U.S.A. 102, 13117-13122.
11. Dahl, S. W., Slaughter, C., Lauritzen, C., Bateman, R. C., Jr., Connerton, I., and Pedersen, J. (2000) Carica papaya glutamine cyclotransferase belongs to a novel plant enzyme subfamily: cloning and characterization of the recombinant enzyme, Protein Expression Purif. 20, 27-36.
12. Pohl, T., Zimmer, M., Mugele, K., and Spiess, J. (1991) Primary structure and functional expression of a glutaminyl cyclase, Proc. Natl. Acad. Sci. U.S.A. 88, 10059-10063.
13. Sykes, P. A., Watson, S. J., Temple, J. S., and Bateman, R. C. J. (1999) Evidence for tissue-specific forms of glutaminyl cyclase, FEBS Lett. 455, 159-161.
14. Bockers, T. M., Kreutz, M. R., and Pohl, T. (1995) Glutaminyl-cyclase expression in the bovine/porcine hypothalamus and pituitary, J. Neuroendocrinal. 7, 445-453.
15. Baggerman, G., Cerstiaens, A., De Loof, A., and Schoofs, L. (2002) Peptidomics of the larval Drosophila melanogaster central nervous system, J. Biol. Chem. 277, 40368-40374.
16. Schaffer, M. H., Noyes, B. E., Slaughter, C. A., Thorne, G. C., and Gaskell, S. J. (1990) The fruitfly Drosophila melanogaster contains a novel charged adipokinetic-hormone-family peptide, Biochem. J. 269, 315-320.
17. Schilling, S., Niestroj, A. J., Rahfeld, J.-U., Hoffmann, T., Wermann, M., Zunkel, K., Wasternack, C., and Demuth, H.-U. (2003) Identification of human glutaminyl cyclase as a metalloenzyme: Inhibition by imidazole derivatives and heterocyclic chelators, J. Biol. Chem. 278, 49773-49779.
18. Crosby, M. A., Goodman, J. L., Strelets, V. B., Zhang, P., and Gelbart, W. M. (2007) FlyBase: genomes by the dozen, Nucleic Acids Res. 35, D486-D491.
19. Igaki, T., Kanuka, H., Inohara, N., Sawamoto, K., Nunez, G., Okano, H., and Miura, M. (2000) Drob-1, a Drosophila member of the Bcl-2/CED-9 family that promotes cell death, Proc. Natl. Acad. Sci. U.S.A. 97, 662-667.
20. Schilling, S., Hoffmann, T., Rosche, F., Manhart, S., Wasternack, C., and Demuth, H. U. (2002) Heterologous expression and characterization of human glutaminyl cyclase: evidence for a disulfide bond with importance for catalytic activity, Biochemistry 41, 10849-10857.
21. Schilling, S., Manhart, S., Hoffmann, T., Ludwig, H.-H., Wasternack, C., and Demuth, H.-U. (2003) Substrate specificity of glutaminyl cyclases from plants and animals, Biol. Chem. 384, 1583-1592.
22. Schilling, S., Cynis, H., von Bohlen, A., Hoffmann, T., Wermann, M., Heiser, U., Buchholz, M., Zunkel, K., and Demuth, H. U. (2005) Isolation, catalytic properties, and competitive inhibitors of the zinc-dependent murine glutaminyl cyclase, Biochemistry 44, 13415-13424.
23. Schilling, S., Hoffmann, T., Wermann, M., Heiser, U., Wasternack, C., and Demuth, H.-U. (2002) Continuous spectrometric assays for glutaminyl cyclase activity, Anal. Biochem. 303, 49-56.
24. Ellis, K. J., and Morrison, J. F. (1982) Buffers of constant ionic strength for studying pH-dependent processes, Methods Enzymol. 87, 405-426.
25. Gill, S. C., and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data, Anal. Biochem. 182, 319-326.
26. Yang, J. T., Wu, C. S., and Martinez, H. M. (1986) Calculation of protein conformation from circular dichroism, Methods Enzymol. 130, 208-269.
27. Buchholz, M., Heiser, U., Schilling, S., Niestroj, A. J., Zunkel, K., and Demuth, H. U. (2006) The first potent inhibitors for human glutaminyl cyclase: synthesis and structure-activity relationship, J. Med. Chem. 49, 664-677.
28. Bendtsen, J. D., Nielsen, H., von Heijne, G., and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0, J. Mol. Biol. 340, 783-795.
29. Claros, M. G., and Vincens, P. (1996) Computational method to predict mitochondrially imported proteins and their targeting sequences, Eur. J. Biochem. 241, 779-786.
30. Morty, R. E., Bulau, P., Pelle, R., Wilk, S., and Abe, K. (2006) Pyroglutamyl peptidase type I from Trypanosoma brucei: a new virulence factor from African trypanosomes that de-blocks regulatory peptides in the plasma of infected hosts, Biochem. J. 394, 635-645.
31. Goren, H. J., Bauce, L. G., and Vale, W. (1977) Forces and structural limitations of binding of thyrotrophin-releasing factor to the thyrotrophin-releasing receptor: the pyroglutamic acid moiety, Mol. Pharmacol. 13, 606-614.
32. Garden, R. W., Moroz, T. P., Gleeson, J. M., Floyd, P. D., Li, L., Rubakhin, S. S., and Sweedler, J. V. (1999) Formation of N-pyroglutamyl peptides from N-Glu and N-Gln precursors in Aplysia neurons, J. Neurochem. 72, 676-681.
33. Furukawa, Y., Nakamaru, K., Wakayama, H., Fujisawa, Y., Minakata, H., Ohta, S., Morishita, F., Matsushima, O., Li, L., Romanova, E., Sweedler, J. V., Park, J. H., Romero, A., Cropper, E. C., Dembrow, N. C., Jing, J., Weiss, K. R., and Vilim, F. S. (2001) The enterins: a novel family of neuropeptides isolated from the enteric nervous system and CNS of Aplysia, J. Neurosci. 21, 8247-8261.
34. Schilling, S., Stenzel, I., von Bohlen, A., Wermann, M., Schulz, K., Demuth, H. U., and Wasternack, C. (2007) Isolation and characterization of the glutaminyl cyclases from Solanum tuberosum and Arabidopsis thaliana: implications for physiological functions, Biol. Chem. 388, 145-153.