Identification and characterization of a unique cysteine residue proximal to the catalytic site of Arabidopsis thaliana carotenoid cleavage enzyme 1

Biochemistry and Cell Biology

Volumn 86, Issue 3, 2008, Pages 262-270

  Guo, Shukui ^a   Boyd, Jason ^a   Sammynaiken, Ramaswami ^b,c   Loewen, Michèle C ^a,c  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Carotenoid cleavage enzymes; Carotenoids; Cysteine mutagenesis; Type II Cu center

Indexed keywords

ABSORPTION; BINDING ENERGY; BINDING SITES; BIOCHEMICAL ENGINEERING; CATALYSTS; ENZYMES; FOOD ADDITIVES; MICROFLUIDICS; PROTEINS; SPECTRUM ANALYSIS; SPECTRUM ANALYZERS; SPEECH; SUBSTRATES; THREE DIMENSIONAL;

(PL) PROPERTIES; ARABIDOPSIS THALIANA (ELIP); CATALYTIC SITES; CU(1 1 0); CYSTEINE RESIDUES; DOUBLE BONDS; HOMOLOGY MODELING; KINETIC (POLYM.); METAL-BINDING AFFINITY; METAL-BINDING SITES; OXIDATIVE CLEAVAGES; PARAMAGNETIC SIGNALS; SEQUENCE ALIGNMENTS; SPECTRAL ANALYSES; STERIC CONSTRAINTS; THALIANA; UV AND VISIBLE LIGHT;

METAL ANALYSIS;

9 EPOXYCAROTENOID CLEAVAGE DIOXYGENASE 3; ALANINE; BETA CAROTENE; CAROTENOID CLEAVAGE DIOXYGENASE 1; CUPRIC ION; CYSTEINE; MUTANT PROTEIN; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; BINDING AFFINITY; BINDING SITE; CHEMICAL BOND; ELECTRON SPIN RESONANCE; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME DEGRADATION; ENZYME KINETICS; ENZYME STRUCTURE; ENZYME SUBSTRATE; LIGHT ABSORPTION; METAL BINDING; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN FUNCTION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; THREE DIMENSIONAL IMAGING; ULTRAVIOLET RADIATION;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CATALYTIC DOMAIN; CYSTEINE; DIOXYGENASES; ELECTRON SPIN RESONANCE SPECTROSCOPY; METALS; MOLECULAR SEQUENCE DATA; MUTATION; OXYGENASES; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROPHOTOMETRY;

ARABIDOPSIS THALIANA;

EID: 44949091723     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/O08-031     Document Type: Article

References (44)

1. Auldridge, M.E., McCarty, D.R., and Klee, H.J. 2006. Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr. Opin. Plant Biol. 9: 315-321. doi:10.1016/j.pbi.2006.03.005. PMID:16616608.
2. Bouvier, F., Isner, J.C., Dogbo, O., and Camara, B. 2005. Oxidative tailoring of carotenoids: a prospect towards novel functions in plants. Trends Plant Sci. 10: 187-194. doi:10.1016/j.tplants. 2005.02.007. PMID:15817420.
3. Britton, G., and Young, A.J. 1993. Methods for the isolation and analysis of carotenoids. Chapman & Hill, London. pp. 409-459.
4. Coufal, D.E., Tavares, P., Pereira, A.S., Hyunh, B.H., and Lippard, S.J. 1999. Reactions of nitric oxide with the reduced non-heme diiron center of the soluble methane monooxygenase hydroxylase. Biochemistry, 38: 4504-4513. doi:10.1021/bi9823378. PMID:10194372.
5. Coulter, E.D., Moon, N., Batie, C.J., Dunham, W.R., and Ballou, D.P. 1999. Electron paramagnetic resonance measurements of the ferrous mononuclear site of phthalate dioxygenase substituted with alternate divalent metal ions: direct evidence for ligation of two histidines in the copper(II)-reconstituted protein. Biochemistry, 38: 11062-11072. doi:10.1021/bi9904499. PMID:10460161.
6. Creighton, T.E. 1984. Disulfide bond formation in proteins. Academic Press Inc., pp. 305-329.
7. D'Autreaux, B., Tucker, N.P., Dixon, R., and Spiro, S. 2005. A non-haem iron centre in the transcription factor NorR senses nitric oxide. Nature, 437: 769-772. doi:10.1038/nature03953. PMID:16193057.
8. Deligiannakis, Y., Boussac, A., Bottin, H., Perrier, V., Barzu, O., and Gilles, A.M. 1997. A new non-heme iron environment in Paracoccus denitrificans adenylate kinase studied by electron paramagnetic resonance and electron spin echo envelope modulation spectroscopy. Biochemistry, 36: 9446-9452. doi:10.1021/bi970021e. PMID:9235989.
9. Fester, T., Hause, B., Schmidt, D., Halfmann, K., Schmidt, J., Wray, V., et al. 2002. Occurrence and localization of apocarotenoids in arbuscular mycorrhizal plant roots. Plant Cell Physiol. 43: 256-265. doi:10.1093/pcp/pcf029. PMID:11917079.
10. Franco, R., Pereira, A.S., Tavares, P., Mangravita, A., Barber, M.J., Moura, I., and Ferreira, G.C. 2001. Substitution of murine ferrochelatase glutamate-287 with glutamine or alanine leads to porphyrin substrate-bound variants. Biochem. J. 356: 217-222. doi:10.1042/0264-6021:3560217. PMID:11336654.
11. Guex, N., and Peitsch, M.C. 1997. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis, 18: 2714-2723. doi:10.1002/elps.1150181505. PMID:9504803.
12. Han, S.Y., Kitahata, N., Sekimata, K., Saito, T., Kobayashi, M., Nakashima, K., et al. 2004. A novel inhibitor of 9-cis-epoxycarotenoid dioxygenase in abscisic acid biosynthesis in higher plants. Plant Physiol. 135: 1574-1582. doi:10.1104/pp.104.039511. PMID:15247398.
13. Hegg, E.L., and Que, L., Jr. 1997. The 2-His-1-carboxylate facial triad-an emerging structural motif in mononuclear non-heme iron(II) enzymes. Eur. J. Biochem. 250: 625-629. doi:10.1111/j.1432-1033.1997.t01-1-00625. x. PMID:9461283.
14. Hegg, E.L., Whiting, A.K., Saari, R.E., McCracken, J., Hausinger, R.P., and Que, L., Jr. 1999. Herbicide-degrading alpha-keto acid-dependent enzyme TfdA: metal coordination environment and mechanistic insights. Biochemistry, 38: 16714-16726. doi:10.1021/bi991796l. PMID:10600135.
15. Hinks, J.A., Evans, M.C., De Miguel, Y., Sartori, A.A., Jiricny, J., and Pearl, L.H. 2002. An iron-sulfur cluster in the family 4 uracil-DNA glycosylases. J. Biol. Chem. 277: 16936-16940. doi:10.1074/jbc. M200668200. PMID:11877410.
16. Hogan, D.A., Smith, S.R., Saari, E.A., McCracken, J., and Hausinger, R.P. 2000. Site-directed mutagenesis of 2,4-dichlorophenoxyacetic acidalpha-ketoglutarate dioxygenase. Identification of residues involved in metallocenter formation and substrate binding. J. Biol. Chem. 275: 12400-12409. doi:10.1074/jbc.275.17.12400. PMID:10777523.
17. Humphrey, W., Dalke, A., and Schulten, K. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14: 27-33.
18. Iuchi, S., Kobayashi, M., Taji, T., Naramoto, M., Seki, M., Kato, T., et al. 2001. Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J. 27: 325-333. doi:10.1046/j.1365- 313x.2001.01096.x. PMID:11532178.
19. Kimura, S., Kikuchi, A., Senda, T., Shiro, Y., and Fukuda, M. 2005. Tolerance of the Rieske-type [2Fe-2S] cluster in recombinant ferredoxin BphA3 from Pseudomonas sp. KKS102 to histidine ligand mutations. Biochem. J. 388: 869-878. doi:10.1042/BJ20042077. PMID:15733056.
20. Kloer, D.P., Ruch, S., Al-Babili, S., Beyer, P., and Schulz, G.E. 2005. The structure of a retinal-forming carotenoid oxygenase. Science, 308: 267-269. doi:10.1126/science.1108965. PMID:15821095.
21. Kosman, D.J., Hassett, R., Yuan, D.S., and McCracken, J. 1998. Spectroscopic characterization of the Cu (II) sites in the Fet3 protein, the multinuclear copper oxidase from yeast required for high-affinity iron uptake. J. Am. Chem. Soc. 120: 4037-4038. doi:10.1021/ja974104u.
22. Mathe, C., Mattioli, T.A., Horner, O., Lombard, M., Latour, J.M., Fontecave, M., and Niviere, V. 2002. Identification of iron(III) peroxo species in the active site of the superoxide reductase SOR from Desulfoarculus baarsii. J. Am. Chem. Soc. 124: 4966-4967. doi:10.1021/ja025707v. PMID:11982354.
23. Mathieu, S., Terrier, N., Procureur, J., Bigey, F., and Gunata, Z. 2005. A carotenoid cleavage dioxygenase from Vitis vinifera L.: functional characterization and expression during grape berry development in relation to C13-norisoprenoid accumulation. J. Exp. Bot. 56: 2721-2731. doi:10.1093/jxb/eri265. PMID:16131507.
24. Moise, A.R., von Lintig, J., and Palczewski, K. 2005. Related enzymes solve evolutionarily recurrent problems in the metabolism of carotenoids. Trends Plant Sci. 10: 178-186. doi:10.1016/j.tplants.2005.02.006. PMID:15817419.
25. Notredame, C., Higgins, D.G., and Heringa, J. 2000. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302: 205-217. doi:10.1006/jmbi.2000.4042. PMID:10964570.
26. Paik, J., During, A., Harrison, E.H., Mendelsohn, C.L., Lai, K., and Blaner, W.S. 2001. Expression and characterization of a murine enzyme able to cleave beta-carotene. The formation of retinoids. J. Biol. Chem. 276: 32160-32168. doi:10.1074/jbc.M010086200. PMID:11418584.
27. Parry, A.D., and Horgan, R. 1991. Carotenoid metabolism and the biosynthesis of abscisic acid. Phytochemistry, 30: 815-821. doi:10.1016/0031-9422(91)85258-2.
28. Poliakov, E., Gentleman, S., Cunningham, F.X., Jr., Miller-Ihli, N.J., and Redmond, T.M. 2005. Key role of conserved histidines in recombinant mouse beta-carotene 15,15'-monooxygenase-1 activity. J. Biol. Chem. 280: 29217-29223. doi:10.1074/jbc.M500409200. PMID:15951442.
29. Rocklin, A.M., Tierney, D.L., Kofman, V., Brunhuber, N.M., Hoffman, B.M., Christoffersen, R.E., et al. 1999. Role of the nonheme Fe(II) center in the biosynthesis of the plant hormone ethylene. Proc. Natl. Acad. Sci. U.S.A. 96: 7905-7909. doi:10.1073/pnas.96.14.7905. PMID:10393920.
30. Rocklin, A.M., Kato, K., Liu, H.W., Que, L., Jr., and Lipscomb, J.D. 2004. Mechanistic studies of 1-aminocyclopropane-1-carboxylic acid oxidase: single turnover reaction. J. Biol. Inorg. Chem. 9: 171-182. doi:10.1007/s00775-003-0510-3. PMID:14714198.
31. Ruch, S., Beyer, P., Ernst, H., and Al-Babili, S. 2005. Retinal biosynthesis in Eubacteria: in vitro characterization of a novel carotenoid oxygenase from Synechocystis sp. PCC 6803. Mol. Microbiol. 55: 1015-1024. doi:10.1111/j.1365-2958.2004.04460.x. PMID:15686550.
32. Ryle, M.J., and Hausinger, R.P. 2002. Non-heme iron oxygenases. Curr. Opin. Chem. Biol. 6: 193-201. doi:10.1016/S1367-5931(02)00302-2. PMID:12039004.
33. Scherzinger, D., Ruch, S., Kloer, D.P., Wilde, A., and Al-Babili, S. 2006. Retinal is formed from apo-carotenoids in Nostoc sp. PCC7120: in vitro characterization of an apo-carotenoid oxygenase. Biochem. J. 398: 361-369. doi:10.1042/BJ20060592. PMID:16759173.
34. Schmidt, H., Kurtzer, R., Eisenreich, W., and Schwab, W. 2006. The carotenase AtCCD1 from Arabidopsis thaliana is a dioxygenase. J. Biol. Chem. 281: 9845-9851. doi:10.1074/jbc.M511668200. PMID:16459333.
35. Schwartz, S.H., Tan, B.C., Gage, D.A., Zeevaart, J.A., and McCarty, D.R. 1997. Specific oxidative cleavage of carotenoids by VP14 of maize. Science, 276: 1872-1874. doi:10.1126/science.276.5320.1872. PMID:9188535.
36. Schwartz, S.H., Qin, X., and Zeevaart, J.A. 2001. Characterization of a novel carotenoid cleavage dioxygenase from plants. J. Biol. Chem. 276: 25208-25211. doi:10.1074/jbc.M102146200. PMID:11316814.
37. Schwartz, S.H., Tan, B.C., McCarty, D.R., Welch, W., and Zeevaart, J.A. 2003. Substrate specificity and kinetics for VP14, a carotenoid cleavage dioxygenase in the ABA biosynthetic pathway. Biochim. Biophys. Acta, 1619: 9-14. PMID:12495810.
38. Schwede, T., Kopp, J., Guex, N., and Peitsch, M.C. 2003. SWISSMODEL: An automated protein homology-modeling server. Nucleic Acids Res. 31: 3381-3385. doi:10.1093/nar/gkg520. PMID:12824332.
39. Smith, D.B., and Johnson, K.S. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione-S-transferase. Gene, 67: 31-40. doi:10.1016/0378- 1119(88)90005-4. PMID:3047011.
40. Solomon, E.I. 2001. Invited award contribution for ACS Award in Inorganic Chemistry. Geometric and electronic structure contributions to function in bioinorganic chemistry: active sites in non-heme iron enzymes. Inorg. Chem. 40: 3656-3669. doi:10.1021/ic010348a. PMID:11442362.
41. Tan, B.C., Joseph, L.M., Deng, W.T., Liu, L., Li, Q.B., Cline, K., and McCarty, D.R. 2003. Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J. 35: 44-56. doi:10.1046/j.1365-313X.2003.01786.x. PMID:12834401.
42. Tocheva, E.I., Rosell, F.I., Mauk, A.G., and Murphy, M.E. 2004. Side-on copper-nitrosyl coordination by nitrite reductase. Science, 304: 867-870. doi:10.1126/science.1095109. PMID:15131305.
43. Whiting, A.K., Que, L., Jr., Saari, R.E., Hausinger, R.P., Fredrick, M.A., and McCracken, J. 1997. Metal coordination environment of a Cu(II)-substituted a -keto acid-dependent dioxygenase that degrades the herbicide 2,4-D. J. Am. Chem. Soc. 119: 3413-3414. doi:10.1021/ja964449x.
44. Wolz, E., Liechti, H., Notter, B., Oesterhelt, G., and Kistler, A. 1999. Characterization of metabolites of astaxanthin in primary cultures of rat hepatocytes. Drug Metab. Dispos. 27: 456-462. PMID:10101140.