Substrate specificity of purified recombinant human β-carotene 15,15′-oxygenase (BCO1)

Journal of Biological Chemistry

Volumn 288, Issue 52, 2013, Pages 37094-37103

  Seña, Carlo Dela ^a   Narayanasamy, Sureshbabu ^a   Riedl, Kenneth M ^a   Curley Jr , Robert W ^a   Schwartz, Steven J ^a   Harrison, Earl H ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOCAROTENOIDS; DOUBLE BONDS; HUMAN ENZYMES; OXIDATIVE CLEAVAGES; OXYGENASES; PROVITAMIN A; SUBSTRATE SPECIFICITY; VITAMIN A;

BIOCHEMISTRY; BIOLOGY;

PIGMENTS;

ALPHA CAROTENE; BETA APO 8' CAROTENAL; BETA CAROTENE 15,15' OXYGENASE; BETA CRYPTOXANTHIN; COBALT; LYCOPENE; OXYGENASE; POLYHISTIDINE TAG; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; ENZYME ISOLATION; ENZYME PURIFICATION; ENZYME SPECIFICITY; ESCHERICHIA COLI; HUMAN; IN VITRO STUDY; MICHAELIS MENTEN KINETICS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION;

EID: 84891437288     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.507160     Document Type: Article

References (56)

1. Lindqvist, A., and Andersson, S. (2002) Biochemical properties of purified recombinant human β-carotene 15,15′-monooxygenase. J. Biol. Chem. 277, 23942-23948
2. 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 β-carotene. The formation of retinoids. J. Biol. Chem. 276, 32160-32168
3. Park, C. S., Lee, S. W., Kim, Y. S., Kim, E. J., Sin, H. S., Oh, D. K., Kim, S. W., and Um, S. J. (2008) Utilization of the recombinant human β-carotene- 15,15′-monooxygenase gene in Escherichia coli and mammalian cells. Biotechnol. Lett. 30, 735-741
4. Redmond, T. M., Gentleman, S., Duncan, T., Yu, S., Wiggert, B., Gantt, E., and Cunningham, F. X., Jr. (2001) Identification, expression, and substrate specificity of a mammalian β-carotene 15,15′-dioxygenase. J. Biol. Chem. 276, 6560-6565
5. Wyss, A., Wirtz, G., Woggon, W., Brugger, R., Wyss, M., Friedlein, A., Bachmann, H., and Hunziker, W. (2000) Cloning and expression of β,β- carotene 15,15′-dioxygenase. Biochem. Biophys. Res. Commun. 271, 334-336
6. Lampert, J. M., Holzschuh, J., Hessel, S., Driever, W., Vogt, K., and von Lintig, J. (2003) Provitamin A conversion to retinal via the β,β-carotene- 15,15′-oxygenase (bcox) is essential for pattern formation and differentiation during zebrafish embryogenesis. Development 130, 2173-2186
7. Kim, Y. S., and Oh, D. K. (2009) Substrate specificity of a recombinant chicken β-carotene 15,15′-monooxygenase that converts β-carotene into retinal. Biotechnol. Lett. 31, 403-408
8. Goodman, D. S., and Huang, H. S. (1965) Biosynthesis of Vitamin A with Rat Intestinal Enzymes. Science 149, 879-880
9. Olson, J. A., and Hayaishi, O. (1965) The enzymatic cleavage ofβ-carotene into vitamin A by soluble enzymes of rat liver and intestine. Proc. Natl. Acad. Sci. U.S.A. 54, 1364-1370
10. Fidge, N. H., Smith, F. R., and Goodman, D. S. (1969) Vitamin A and carotenoids. The enzymic conversion of β-carotene into retinal in hog intestinal mucosa. Biochem. J. 114, 689-694
11. Wang, X. D., Tang, G. W., Fox, J. G., Krinsky, N. I., and Russell, R. M. (1991) Enzymatic conversion of β-carotene into β-apo-carotenals and retinoids by human, monkey, ferret, and rat tissues. Arch. Biochem. Biophys. 285, 8-16
12. Devery, J., and Milborrow, B. V. (1994) β-Carotene-15,15′- dioxygenase (EC 1.13.11.21) isolation reaction mechanism and an improved assay procedure. Br. J. Nutr. 72, 397-414
13. During, A., Nagao, A., Hoshino, C., and Terao, J. (1996) Assay of β-carotene 15,15′-dioxygenase activity by reverse-phase high-pressure liquid chromatography. Anal. Biochem. 241, 199-205
14. Grolier, P., Duszka, C., Borel, P., Alexandre-Gouabau, M. C., and Azais-Braesco, V. (1997) In vitro and in vivo inhibition of β-carotene dioxygenase activity by canthaxanthin in rat intestine. Arch. Biochem. Biophys. 348, 233-238
15. Lakshmanan, M. R., Chansang, H., and Olson, J. A. (1972) Purification and properties of carotene 15,15′-dioxygenase of rabbit intestine. J. Lipid Res. 13, 477-482
16. Lakshmanan, M. R., Pope, J. L., and Olson, J. A. (1968) The specificity of a partially purified carotenoid cleavage enzyme of rabbit intestine. Biochem. Biophys. Res. Commun. 33, 347-352
17. Wirtz, G. M., Bornemann, C., Giger, A., Müller, R. K., Schneider, H., Schlotterbeck, G., Schiefer, G., and Woggon, W. (2001) The Substrate Specificity of β,β-Carotene 15,15′-Monooxygenase. Helv. Chim. Acta 84, 2301-2315
18. Chandler, L. A., Schwartz, S. J. (1987) HPLC separation of cis-trans carotene isomers in fresh and processed fruits and vegetables. J. Food Sci. 52, 669-672
19. Gaziano, J. M., Johnson, E. J., Russell, R. M., Manson, J. E., Stampfer, M. J., Ridker, P. M., Frei, B., Hennekens, C. H., and Krinsky, N. I. (1995) Discrimination in absorption or transport ofβ-carotene isomers after oral supplementation with either all-trans- or 9-cis-β-carotene. Am. J. Clin. Nutr. 61, 1248-1252
20. Krinsky, N. I., Russett, M. D., Handelman, G. J., and Snodderly, D. M. (1990) Structural and geometrical isomers of carotenoids in human plasma. J. Nutr. 120, 1654-1662
21. Nagao, A., and Olson, J. A. (1994) Enzymatic formation of 9-cis, 13-cis, and all-trans retinals from isomers of β-carotene. FASEB J. 8, 968-973
22. Wang, X. D., Krinsky, N. I., Benotti, P. N., and Russell, R. M. (1994) Biosynthesis of 9-cis retinoic acid from 9-cis β-carotene in human intestinal mucosa in vitro. Arch. Biochem. Biophys. 313, 150-155
23. Hansen, S., and Maret, W. (1988) Retinal is not formed in vitro by enzymatic central cleavage of β-carotene. Biochemistry 27, 200-206
24. Tang, G. W., Wang, X. D., Russell, R. M., and Krinsky, N. I. (1991) Characterization of β-apo-13-carotenone and β-apo-14′-carotenal as enzymatic products of the excentric cleavage of β-carotene. Biochemistry 30, 9829-9834
25. Yeum, K. J., dos Anjos Ferreira, A. L., Smith, D., Krinsky, N. I., and Russell, R. M. (2000) The effect ofβ-tocopherol on the oxidative cleavage ofβ-carotene. Free Radic Biol. Med. 29, 105-114
26. von Lintig, J., and Vogt, K. (2000) Filling the gap in vitamin A research. Molecular identification of an enzyme cleaving β-carotene to retinal. J. Biol. Chem. 275, 11915-11920
27. Yan, W., Jang, G. F., Haeseleer, F., Esumi, N., Chang, J., Kerrigan, M., Campochiaro, M., Campochiaro, P., Palczewski, K., and Zack, D. J. (2001) Cloning and characterization of a human β, β-carotene-15,15′- dioxygenase that is highly expressed in the retinal pigment epithelium. Genomics 72, 193-202
28. Eroglu, A., Hruszkewycz, D. P., dela Sena, C., Narayanasamy, S., Riedl, K. M., Kopec, R. E., Schwartz, S. J., Curley, R. W., Jr., and Harrison, E. H. (2012) Naturally occurring eccentric cleavage products of provitamin A β-carotene function as antagonists of retinoic acid receptors. J. Biol. Chem. 287, 15886-15895
29. Stahl, W., Schwarz, W., and Sies, H. (1993) Human serum concentrations of all-trans β- and α-carotene but not 9-cis β-carotene increase upon ingestion of a natural isomer mixture obtained from Dunaliella salina (Betatene). J. Nutr. 123, 847-851
30. de Pee, S., and West, C. E. (1996) Dietary carotenoids and their role in combating vitamin A deficiency: a review of the literature. Eur. J. Clin. Nutr. 50, S38-S53
31. Maeda, T., Perusek, L., Amengual, J., Babino, D., Palczewski, K., and von Lintig, J. (2011) Dietary 9-cis-β, β-carotene fails to rescue vision in mouse models of leber congenital amaurosis. Mol. Pharmacol. 80, 943-952
32. Fleshman, M. K., Lester, G. E., Riedl, K. M., Kopec, R. E., Narayanasamy, S., Curley, R. W., Jr., Schwartz, S. J., and Harrison, E. H. (2011) Carotene and novel apocarotenoid concentrations in orange-fleshed Cucumis melo melons: determinations of β-carotene bioaccessibility and bioavailability. J. Agric. Food Chem. 59, 4448-4454
33. Mínguez-Mosquera, M. I., Hornero-Méndez, D., and Garrido-Fernández, J. (1995) Detection of bixin, lycopene, canthaxanthin, and β-apo-8′-carotenal in products derived from red pepper. J. AOAC Int. 78, 491-496
34. Ho, C. C., de Moura, F. F., Kim, S. H., and Clifford, A. J. (2007) Excentral cleavage of β-carotene in vivo in a healthy man. Am. J. Clin. Nutr. 85, 770-777
35. Suzuki, T., Matsui, M., and Murayama, A. (1995) Biological activity of (all-E)-β-apo-12′-carotenoic acid and the geometrical isomers on human acute promyelocytic leukemia cell line HL-60. J. Nutr. Sci. Vitaminol. 41, 575-585
36. Tibaduiza, E. C., Fleet, J. C., Russell, R. M., and Krinsky, N. I. (2002) Excentric cleavage products of β-carotene inhibit estrogen receptor positive and negative breast tumor cell growth in vitro and inhibit activator protein- 1-mediated transcriptional activation. J. Nutr. 132, 1368-1375
37. Ziouzenkova, O., Orasanu, G., Sukhova, G., Lau, E., Berger, J. P., Tang, G., Krinsky, N. I., Dolnikowski, G. G., and Plutzky, J. (2007) Asymmetric cleavage of β-carotene yields a transcriptional repressor of retinoid X receptor and peroxisome proliferator-activated receptor responses. Mol. Endocrinol. 21, 77-88
38. Eroglu, A., Hruszkewycz, D. P., Curley, R. W., Jr., and Harrison, E. H. (2010) The eccentric cleavage product of β-carotene, β-apo-13- carotenone, functions as an antagonist of RXRα. Arch. Biochem. Biophys. 504, 11-16
39. Ben-Amotz, A., and Levy, Y. (1996) Bioavailability of a natural isomer mixture compared with synthetic all-trans β-carotene in human serum. Am. J. Clin. Nutr. 63, 729-734
40. You, C. S., Parker, R. S., Goodman, K. J., Swanson, J. E., and Corso, T. N. (1996) Evidence of cis-trans isomerization of 9-cis-β-carotene during absorption in humans. Am. J. Clin. Nutr. 64, 177-183
41. Heyman, R. A., Mangelsdorf, D. J., Dyck, J. A., Stein, R. B., Eichele, G., Evans, R. M., and Thaller, C. (1992) 9-cis retinoic acid is a high affinity ligand for the retinoid X receptor. Cell 68, 397-406
42. Levin, A. A., Sturzenbecker, L. J., Kazmer, S., Bosakowski, T., Huselton, C., Allenby, G., Speck, J., Ratzeisen, C., Rosenberger, M., Lovey, A., and Grippo, J. F. (1992) 9-Cis retinoic acid stereoisomer binds and activates the nuclear receptor RXRα. Nature 355, 359-361
43. Kane, M. A. (2012) Analysis, occurrence, and function of 9-cis retinoic acid. Biochim. Biophys. Acta 1821, 10-20
44. Urbach, J., and Rando, R. R. (1994) Thiol dependent isomerization of all-trans retinoic acid to 9-cis retinoic acid. FEBS Lett. 351, 429-432
45. Urbach, J., and Rando, R. R. (1994) Isomerization of all-trans retinoic acid to 9-cis retinoic acid. Biochem. J. 299, 459-465
46. Lidén, M., and Eriksson, U. (2005) Development of a versatile reporter assay for studies of retinol uptake and metabolism in vivo. Exp. Cell Res. 310, 401-408
47. Kotake-Nara, E., Kim, S. J., Kobori, M., Miyashita, K., and Nagao, A. (2002) Acyclo-retinoic acid induces apoptosis in human prostate cancer cells. Anticancer Res. 22, 689-695
48. Ben-Dor, A., Nahum, A., Danilenko, M., Giat, Y., Stahl, W., Martin, H. D., Emmerich, T., Noy, N., Levy, J., and Sharoni, Y. (2001) Effects of acycloretinoic acid and lycopene on activation of the retinoic acid receptor and proliferation of mammary cancer cells. Arch. Biochem. Biophys. 391, 295-302
49. Stahl, W., von Laar, J., Martin, H. D., Emmerich, T., and Sies, H. (2000) Stimulation of gap junctional communication: comparison of acyclo-retinoic acid and lycopene. Arch. Biochem. Biophys. 373, 271-274
50. Kopec, R. E., Riedl, K. M., Harrison, E. H., Curley, R. W., Jr., Hruszkewycz, D. P., Clinton, S. K., and Schwartz, S. J. (2010) Identification and quantification of apo-lycopenals in fruits, vegetables, and human plasma. J. Agric. Food Chem. 58, 3290-3296
51. Gajic, M., Zaripheh, S., Sun, F., and Erdman, J. W., Jr. (2006) Apo-8′- lycopenal and apo-12′-lycopenal are metabolic products of lycopene in rat liver. J. Nutr. 136, 1552-1557
52. Khachik, F., Beecher, G. R., and Smith, J. C., Jr. (1995) Lutein, lycopene, and their oxidative metabolites in chemoprevention of cancer. J. Cell Biochem. Suppl 22, 236-246
53. Khachik, F., Spangler, C. J., Smith, J. C., Jr., Canfield, L. M., Steck, A., and Pfander, H. (1997) Identification, quantification, and relative concentrations of carotenoids and their metabolites in human milk and serum. Anal. Chem. 69, 1873-1881
54. Richelle, M., Sanchez, B., Tavazzi, I., Lambelet, P., Bortlik, K., and Williamson, G. (2010) Lycopene isomerisation takes place within enterocytes during absorption in human subjects. Br. J. Nutr. 103, 1800-1807
55. 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
56. West, C. E., and Castenmiller, J. J. (1998) Quantification of the "SLAMENGHI" factors for carotenoid bioavailability and bioconversion. Int. J. Vitam. Nutr. Res. 68, 371-377