Involvement of metals in enzymatic and nonenzymatic decomposition of C-terminal α-hydroxyglycine to amide: an implication for the catalytic role of enzyme-bound zinc in the peptidylamidoglycolate lyase reaction

Biochemistry

Volumn 48, Issue 7, 2009, Pages 1654-1662

  Takahashi, Kenichi ^a   Harada, Saori ^a   Higashimoto, Yuichiro ^a   Shimokawa, Chizu ^a   Sato, Hideaki ^a   Sugishima, Masakazu ^a   Kaida, Yasuhiko ^b   Noguchi, Masato ^a  

^a KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE GROUPS; BIOLOGICAL ACTIVITIES; BOUND METALS; BOUND WATERS; BOUND ZINCS; CATALYTIC ROLES; CONCENTRATION DEPENDENTS; DIVALENT METALS; GENERAL BASE; GLYOXYLATE; METAL CATALYSIS; MONOOXYGENASE; NON-ENZYMATIC; PEPTIDE HORMONES; SECOND-ORDER RATE CONSTANTS; SERIES OF TRANSITIONS; STEADY-STATE PARAMETERS; WILD-TYPE ENZYMES;

AMIDES; AMINES; ENZYMES; HORMONES; HYDRATES; MANGANESE; MANGANESE COMPOUNDS; METAL RECOVERY; METALS; RATE CONSTANTS; ZINC;

ENZYME ACTIVITY;

AMIDE; CADMIUM; COBALT; LYASE; WATER; ZINC; AMIDINE LYASE; GLYCINE; PEPTIDYLAMIDOGLYCOLATE LYASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CHEMICAL REACTION; DECOMPOSITION; ENZYMATIC DEGRADATION; ENZYME BINDING; ENZYME SUBSTRATE; HYDRATION; NONHUMAN; PH; PRIORITY JOURNAL; WILD TYPE; BIOCATALYSIS; METABOLISM; PHYSIOLOGY;

AMIDES; AMIDINE-LYASES; BIOCATALYSIS; GLYCINE; ZINC;

EID: 61749093394     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi8018866     Document Type: Article

References (40)

1. Prigge, S. T., Mains, R. E., Eipper, B. A., and Amzel, L. M. (2000) New insights into copper monooxygenases and peptide amidation; structure, mechanism and function. Cell. Mol. Life Sci. 57, 1236-1259.
2. Eipper, B. A., Mains, R. E., and Glembotski, C. C. (1983) Identification in pituitary tissue of a peptide α-amidation activity that acts on glycine-extended peptides and requires molecular oxygen, copper, and ascorbic acid. Proc. Natl. Acad. Sci. U.S.A. 80, 5144-5148.
3. Zabriskie, T. M., Cheng, H., and Vederas, J. C. (1991) Incorporation of aerobic oxygen into the hydroxyglycyl intermediate during formation of C-terminal peptide amides by peptidylglycine α-ami-dating monooxygenase. J. Chem. Soc., Chem. Commun., 571-572.
4. Noguchi, M., Seino, H., Kochi, H., Okamoto, H., Tanaka, T., and Hirama, M. (1992) The source of the oxygen atom in the α-hydroxyglycine intermediate of the peptidylglycine α-amidating reaction. Biochem. J. 283, 883-888.
5. 13C NMR shift as proof that bifunctional peptidylglycine α-amidating enzyme is a monooxygenase. Biochemistry 31, 7282-7288.
6. Katopodis, A. G., Ping, D., and May, S. W. (1990) A novel enzyme from bovine neurointermediate pituitary catalyzes dealkylation of α-hydroxyglycine derivatives, thereby functioning sequentially with peptidylglycine α-amidating monooxygenase in peptide amidation. Biochemistry 29, 6115-6120.
7. Takahashi, K., Okamoto, H., Seino, H., and Noguchi, M. (1990) Peptidylglycine α-amidating reaction: evidence for a two-step mechanism involving a stable intermediate at neutral pH. Biochem. Biophys. Res. Commun. 169, 524-530.
8. Perkins, S. N, Husten, E. J., and Eipper, B. A. (1990) The 108-kDa peptidylglycine α-amidating monooxygenase precursor contains two separable enzymatic activities involved in peptide amidation. Biochem. Biophys. Res. Commun. 171, 926-932.
9. Kato, I., Yonekura, H., Tajima, M., Yanagi, M., Yamamoto, H., and Okamoto, H. (1990) Two enzymes concerned in peptide hormone α-amidation are synthesized from a single mRNA. Biochem. Biophys. Res. Commun. 172, 197-203.
10. Eipper, B. A., Stoffers, D. A., and Mains, R. E. (1992) The biosynthesis of neuropeptides: peptide α-amidation. Annu. ReV. Neurosci. 15, 57-85.
11. Czyzyk, T. A., Ning, Y., Hsu, M., Peng, B., Mains, R. E., Eipper, B. A., and Pintar, J. E. (2005) Deletion of peptide amidation enzymatic activity leads to edema and embryonic lethality in the mouse. Dev. Biol. 287, 301-313.
12. Klinman, J. P. (1996) Mechanisms whereby mononuclear copper proteins functionalize organic substrates. Chem. ReV. 96, 2541-2561.
13. Tenn, W. J., French, N. L., and Nagorski, R. W. (2000) Kinetic dependence of the aqueous reaction of N-(hydroxymethyl)benza-mide derivatives upon addition of electron-withdrawing groups. Org. Lett. 3, 75-78.
14. Bundgaad, H, and Kahns, A. H. (1991) Chemical stability and plasma-catalyzed dealkylation of peptidyl-α-hydroxyglycine derivatives, intermediates in peptide α- amidation. Peptides 12, 745-748.
15. Mennenga, A. G., Johnson, A. L., and Nagorski, R. W. (2005) General-buffer catalysis of the reaction of N-(hydroxymethyl)ben-zamide: a new pathway for the aqueous reaction of carbinolamides. Tetrahedron Lett. 46, 3079-3083.
16. Bell, J., Ash, D. E., Snyder, L. M., Kulathila, R., Blackburn, N. J., and Merkler, D. J. (1997) Structural and functional investigations on the role of zinc in bifunctional rat peptidylglycine α-amidating enzyme. Biochemistry 36, 16239-16246.
17. Kolhekar, A. S., Bell, J., Shiozaki, E. N., Jin, L., Keutmann, H. T, Hand, T. A., Mains, R. E., and Eipper, B. A. (2002) Essential features of the catalytic core of peptidyl-α-hydroxyglycine α-amidating lyase. Biochemistry 41, 12384-12394.
18. Eipper, B. A., Perkins, S. N, Husten, E. J., Johnson, R. C., Keutmann, H. T., and Mains, R. E. (1991) Peptidyl-α-hydroxyglycine α-amidating lyase: purification, characterization, and expression. J. Biol. Chem. 266, 7827-7833.
19. Satani, M., Takahashi, K., Sakamoto, H, Harada, S., Kaida, Y., and Noguchi, M. (2003) Expression and characterization of human bifunctional peptidylglycine α-amidating monooxygenase. Protein Expression Purif. 28, 293-302.
20. Kulathila, R., Consalvo, A. P., Fitzpatrick, P. F., Freeman, J. C., Snyder, L. M., Villafranca, J. J., and Merkler, D. J. (1994) Bifunctional peptidylglycine α-amidating enzyme requires two copper atoms for maximum activity. Arch. Biochem. Biophys. 311, 191-195.
21. De, M., Bell, J., Blackburn, N. J., Mains, R. E., and Eipper, B. A. (2006) Role for an essential tyrosine in peptide amidation. J. Biol. Chem. 281, 20873-20882.
22. Takahashi, K., Onami, T., and Noguchi, M. (1998) Kinetic isotope effects of peptidylglycine α-hydroxylating mono-oxygenase reaction. Biochem. J. 336, 131-137.
23. Takahashi, K., Satani, M., Harada, S., and Noguchi, M. (2003) Expression and characterization of frog peptidylglycine α-hydroxylating monooxygenase. Protein Expression Purif. 27, 35-41.
24. + during dioxygen activation in a copper amine oxidase from yeast. J. Am. Chem. Soc. 122, 9897-9904.
25. Agostinelli, E., De Matteis, G., Sinibaldi, A., Mondovi, B., and Morpurgo, L. (1997) Reactions of the oxidized organic cofactor in copper-depleted bovine serum amine oxidase. Biochem. J. 324, 497-501.
26. Suzuki, S., Sakurai, T., Nakahara, A., Manabe, T., and Okuyama, T. (1983) Effect of metal substitution on the chromophore of bovine serum amine oxidase. Biochemistry 22, 1630-1635.
27. Mounier, C. E., Shi, J., Sirimanne, S. R., Chen, B., Moore, A. B., Gill-Woznichak, M. M., Ping, D., and May, S. W. (1997) Pyruvate-extended amino acid derivatives as highly potent inhibitors of carboxyl-terminal peptide amidation. J. Biol. Chem. 272, 5016-5023.
28. Perrin, D. D. (1982) Ionization constants of inorganic acids and bases in aqueous solution, 2nd ed., Pergamon Press, New York.
29. Burgess, J. (1978) Metal ions in solution, Halsted Press, New York.
30. Vallee, B. L., and Auld, D. S. (1992) Active zinc binding sites of zinc metalloenzymes. MATRIX Suppl. 1, 5-19.
31. Vallee, B. L., and Galdes, A. (1984) The metallobiochemistry of zinc enzyme. Adv. Enzymol. Relat. Areas Mol. Biol. 56, 283-430.
32. Jackman, J. E., Raetz, C. R. H., and Fierke, C. A. (1999) UDP-3-O-(R-3-hydroxymyristoyl)-N-acetylglucosamine deacetylase of Escherichia coli is a zinc metalloenzyme. Biochemistry 38, 1902-1911.
33. Hernick, M., and Fierke, C. A. (2005) Zinc hydrolases: the mechanisms of zinc-dependent deacetylases. Arch. Biochem. Bio-phys. 433, 71-84.
34. Vallee, B. L., and Auld, D. S. (1990) Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 29, 5647-5659.
35. Vallee, B. L., and Auld, D. S. (1993) Cocatalytic zinc motifs in enzyme catalysis. Proc. Natl. Acad. Sci. U.S.A. 90, 2715-2718.
36. Eriksson, A. E., Jones, T. A., and Liljas, A. (1988) The refined structure of human carbonic anhydrase II at 2.0 Å resolution. Proteins 4, 274-282.
37. Gomez-Ortiz, M., Gomis-Rüth, F. X., Huber, R., and Avilés, F. X. (1997) Inhibition of carboxypeptidase A by excess zinc: analysis of the structural determinants by X-ray crystallography. FEBS Lett. 400, 336-340.
38. Larsen, K. S., and Auld, D. S. (1991) Characterization of an inhibitory metal binding site in carboxypeptidase A. Biochemistry 30, 2613-2618.
39. Liaw, S. H., Chen, S. J., Ko, T. P., Hsu, C. S., Chen, C. J., Wang, A. H. J., and Tsai, Y. C. (2003) Crystal structure of D-aminoacylase from Alcaligenes faecalis DA1, a novel subset of amidohydrolases and insights into the enzyme mechanism. J. Biol. Chem. 278, 4957-4962.
40. Whittington, D. A., Rusche, K. M., Shin, H., Fierke, C. A., and Christianson, D. W. (2003) Crystal structure of LpxC, a zinc-dependent deacetylase essential for endotoxin biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 100, 8146-8150.