Enzymatic synthesis of apigenin glucosides by glucosyltransferase (YjiC) from Bacillus licheniformis DSM 13

Molecules and Cells

Volumn 36, Issue 4, 2013, Pages 355-361

  Gurung, Rit Bahadur ^a   Kim, Eun Hee ^b   Oh, Tae Jin ^a   Sohng, Jae Kyung ^a  

^a SunMoon University   (South Korea)

^b Korea Basic Science Institute (KBSI)   (South Korea)

Author keywords

apigenin; enzymatic synthesis; glucosides; UDP glucosyltransferase; YjiC

Indexed keywords

APIGETRIN; SUCROSE SYNTHASE; URIDINE DIPHOSPHATE GLUCOSE;

ARTICLE; BACILLUS LICHENIFORMIS; BACTERIAL STRAIN; ENZYME PURIFICATION; ENZYME STRUCTURE; ENZYME SYNTHESIS; GLYCOSYLATION; IN VITRO STUDY; MOLECULAR CLONING; NONHUMAN; PROTEIN EXPRESSION;

APIGENIN; BACILLUS; BACTERIAL PROTEINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; GLUCOSIDES; GLUCOSYLTRANSFERASES; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; MOLECULAR STRUCTURE; URIDINE DIPHOSPHATE GLUCOSE;

EID: 84888400278     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.1007/s10059-013-0164-0     Document Type: Article

References (55)

1. Agrawal, P.K., and Bansal, M.C. (1989). Flavonoid glycosides. In Carbon-13 NMR of Flavonoids, P.K. Agrawal, ed. (Amsterdam, Oxford, New York, Tokyo: Elsevier), pp. 283-364.
2. Akingbala, J.O. (1991). Effect of processing on flavonoids in Millet (Pennisetum americanum) flour. Cereal Chem. 68, 180-183.
3. Breton, C., Fournel-Gigleux, S., and Palcic, M.M. (2012). Recent structures, evolution and mechanisms of glycosyltransferases. Curr. Opin. Struct. Biol. 22, 540-549.
4. Campbell, J.A., Davies, G.J., Bulone, V., and Henrissat, B. (1997). A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities. Biochem. J. 326, 929-939.
5. Cantarel, B.L., Coutinho, P.M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009). The carbohydrate-active enzymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37, 233-238.
6. Choo, C.Y., Sulong, N.Y., Man, F., and Wong, T.W. (2012). Vitexin and isovitexin from the leaves of Ficus deltoidea with in-vivo á-glucosidase inhibition. J. Ethnopharmacol. 1142, 776-781.
7. Desmet, T., Soetaert, W., Bojarová, P., Kren, V., Dijkhuizen, L., Eastwick-Field, V., and Schiller, A. (2012) enzymatic glycosylation of small molecules: challenging substrates require tailored catalysts. Chemistry 18, 10786-10801.
8. Erb, A., Weiss, H., Härle, J., and Bechthold, A. (2009). A bacterial glycosyltransferase gene toolbox: generation and applications. Phytochemistry 70, 1812-1821.
9. Ersoz, T., Harput, U. S., Saracoglu, I., and Calis, I. (2002). Phenolic compounds from Scutellaria pontica. Turk. J. Chem. 26, 581-588.
10. Essokne, R.S., Grayer, R.J., Porter, E., Kite, G.C., Simmonds, M.S. J., and Jury, S.L. (2012). Flavonoids as chemosystematic markers for the genus Adenocarpus. Biochem. Syst. Ecol. 42, 49-52.
11. Gupta, S., Afaq, F., and Mukhtar, H. (2002). Involvement of nuclear factor kappa B, Bax and Bcl2 in induction of cell cycle arrest and apoptosis by apigenin in human prostate carcinoma cells. Oncogene 21, 3727-3738.
12. Ha, S.K., Lee, P., Park, J.A., Oh, H.R., Lee, S.Y., Park, J.H., Lee, E.H., Ryu, J.H., Lee, K.R., and Kim, S.Y. (2008). Apigenin inhibits the production of NO and PGE2 in microglia and inhibits neuronal cell death in a middle cerebral artery occlusion-induced focal ischemia mice model. Neurochem. Int. 52, 878-886.
13. Harle, J., and Bechthold, A. (2009). The power of glycosyltransferases to generate bioactive natural compounds. In Methods Enzymol. (Complex Enzymes in Microbial Natural Product Biosynthesis, Part A: Overview Articles and Peptides) D.A. Hopwood, ed. (USA, Academic Press), 458, pp. 309-333.
14. Hattori, S., and Matsuda, H. (1952). Rhoifolin, a new flavone glycoside, isolated from the leaves of Rhus succedanea. Arch. Biochem. Biophys. 37, 85-89.
15. Havsteen, B. (1983). Flavonoids, a class of natural products of high pharmacological potency. Biochem. Pharmacol. 32, 1141-1148.
16. Ielpo, M.T., Basile, A., Miranda, R., Moscatiello, V., Nappo, C., Sorbo, S., Laghi E., Ricciardi, M.M., Ricciardi, L., and Vuotto, M.L. (2000). Immunopharmacological properties of flavonoids. Fitoterapia 71, S101-S109.
17. Jäger, A.K., and Saaby, L. (2011). Flavonoids and the CNS. Molecules 16, 1471-1485.
18. Jones, P., and Vogt, T. (2001). Glycosyltransferases in secondary plant metabolism: tranquilizers and stimulant controllers. Planta 213, 164-174.
19. Ko, J.H., Kim, B.G., and Ahn, J.H. (2006). Glycosylation of flavonoids with a glycosyltransferase from Bacillus cereus. FEMS Microbiol. Lett. 258, 263-268.
20. Kobayashi, T., Nakata, T., and Kusumaki, T. (2002). Effect of flavonoids on cell cycle progression in prostate cancer cells. Cancer Lett. 176, 17-23.
21. Lim, E.K., and Bowles, D.J. (2004). A class of plant glycosyltransferases involved in cellular homeostasis. EMBO J. 23, 2915-2922.
22. Lin, J.K., Chen, Y.C., Huang, Y.T., and Lin-Shiau, S.Y. (1997). Suppression of protein kinase C and nuclear oncogene expression as possible molecular mechanisms of cancer chemoprevention by apigenin and curcumin. J. Cell. Biochem. 67, 39-48.
23. Lin, Y.L., Kuo, Y.H., and Shiao, M.S. (2000). Flavonoid glycosides from Terminalia catappa L. J. Chinese Chem. Soc. 47, 253-256.
24. Mackenzie, P.I., Owens, I.S., Burchell, B., Bock, K.W., Bairoch, A., Belanger, A., Fournel-Gigleux, S., Green, M., Hum, D.W., Iyanagi, T., et al. (1997). The UDP-glycosyltransferase gene superfamily: Recommended nomenclature update based on evolutionary divergence. Pharmacogenetics 7, 255-269.
25. Makino, T., Shimizu, R., Kanemaru, M., Suzuki, Y., Moriwaki, M., and Mizukami, H. (2009). Enzymatically modified isoquercitrin, á- oligoglucosyl quercetin 3-O-glucoside, is absorbed more easily than other quercetin glycosides or aglycone after oral administration in rats. Biol. Pharm. Bull. 32, 2034-2040.
26. Manach, C., Scalbert, A., Morand, C., Remesy, C., and Jimenez, L. (2004). Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 79, 727-747.
27. 1H nuclear magnetic resonance spectroscopy of flavonoids and their glycosides in hexadeuterodimethylsulfoxide. In the Flavonoids, Advances in Research Since 1986, J.B. Harborne, ed. (London, UK: Chapman & Hall), pp. 441-497.
28. Merfort, I., Heilmann, J., Hagedorn-Leweke, U., and Lippold, B.C. (1994). In vivo skin penetration studies of chamomile flavones. Pharmazie 49, 509-511.
29. Meyer, H., Bolarinwa, A., Wolfram, G., and Linseisen, J. (2006). Bioavailability of apigenin from apiin-rich parsley in humans. Ann. Nutr. Metab. 50, 167-172.
30. Middleton, Jr. E. (1998). Effect of plant flavonoids on immune and inflammatory cell function. Adv. Exp. Med. Biol. 439,175-182.
31. Moussaoui, F., Zellagui, A., Segueni, N., Touil, A., and Rhouati, S. (2010). Flavonoid constituents from Algerian Launaea resedifolia (O.K.) and their antimicrobial activity. Rec. Nat. Prod. 4, 91-95.
32. Myhrstad, M.C., Carlsen, H., Nordstrom, O., Blomhoff, R., and Moskaug, J.O. (2002). Flavonoids increase the intracellular glutathione level by transactivation of the gamma-glutamylcysteine synthetase catalytical subunit promoter. Free Radic. Biol. Med. 32, 386-393.
33. Nakazaki, E., Soninkhishig, T., Han, J., and Isoda, H. (2013). Proteomic study of granulocytic differentiation induced by apigenin 7-glucoside in human promyelocytic leukemia HL-60 cells. Eur. J. Nutr. 52, 25-35.
34. Pandey, R.P., Li, T.F., Kim, E.H., Yamaguchi, T., Park, Y.I., Kim, J.S., and Sohng, J.K. (2013). Enzymatic synthesis of novel phloretin glucosides. Appl. Environ. Microbiol. 79, 3516-3521
35. Patel, D., Shukla, S., and Gupta, S. (2007). Apigenin and cancer chemoprevention: Progress, potential and promise. Int. J. Oncol. 30, 233-245.
36. Rajbhandari, A., and Roberts, M.F. (1983). The flavonoids of Stevia rebaudiana. J. Nat. Prod. 46, 194-195.
37. Rice-Evans, C.A., Miller, N.J., and Paganga, G. (1996). Structureantioxidant activity relationships of flavonoids and phenolic acids. Free Radic. Biol. Med. 20, 933-956.
38. Richman, A., Swanson, A., Humphrey, T., Chapman, R., McGarvey, B., Pocs, R., and Brandle, J. (2005). Functional genomics uncovers three glucosyltransferases involved in the synthesis of the major sweet glucosides of Stevia rebaudiana. Plant J. 41, 56-67.
39. Ross, J.A., and Kasum, C.M. (2002). Dietary flavonoids: bioavailabilty, metabolic effects and safety. Annu. Rev. Nutr. 22, 19-34.
40. Segaert, S., Courtois, S., Garmyn, M., Degreef, H., and Bouillon, R. (2000). The flavonoid apigenin suppresses vitamin D receptor expression and vitamin D responsiveness in normal human keratinocytes. Biochem. Biophys. Res. Commun. 268, 237-241.
41. She, G., Guo, Z., Lv, H., and She, D. (2009). New flavonoid glycosides from Elsholtzia rugulosa Hemsl. Molecules 14, 4190-4196.
42. Shimoda, K., Otsuka, T., Morimoto, Y., Hamada, H., and Hamada, H. (2007). Glycosylation and malonylation of quercitin, epicatechin, and catechin by cultured plant cells. Chem. Lett. 36, 1292-1293.
43. Shukla, S., and Gupta, S. (2010). Apigenin: a promising molecule for cancer prevention. Pharm. Res. 27, 962-978.
44. Singh, J.P., Selvendiran, K., Banu, S.M., Padmavathi, R., and Sakthisekaran, D. (2004). Protective role of apigenin on the status of lipid peroxidation and antioxidant defense against hepatocarcinogenesis in Wistar albino rats. Phytomedicine 11, 309-314.
45. Surh, Y.J. (2003). Cancer chemoprevention with dietary phytochemicals. Nat. Rev. Cancer 3, 768-780.
46. Švehlíková, V., Bennett, R.N., Mellon, F.A., Needs, P.W., Piacente, S., Kroon, P.A., and Bao, Y. (2004). Isolation, identification and stability of acylated derivatives of apigenin 7-O-glucoside from chamomile (Chamomilla recutita [L.] Rauschert). Phytochemistry 65, 2323-2332.
47. Terasaka, K., Misutani, Y., Nagatsu, A., and Mizukami, H. (2012). In situ UDP-glucose regeneration unravels diverse functions of plant secondary product glycosyltransferases. FEBS Lett. 586, 4344-4350.
48. Toker G., Küpeli, E., Memisoglu, M., and Yesilada, E. (2004). Flavonoids with antinociceptive and anti-inflammatory activities from the leaves of Tilia argentea (silver linden). J. Ethnopharmacol. 95, 393-397.
49. Tsolmon, S., Nakazaki, E., Han, J., and Isoda, H. (2011). Apigetrin induces erythroid differentiation of human leukemia cells K562: proteomics approach. Mol. Nutr. Food Res. 55, S93-S102.
50. Wang, H.K., Xia, Y., Yang, Z.Y., Natschke, S.L., and Lee, K.H. (1998). Recent advances in the discovery and development of flavonoids and their analogues as antitumor and anti-HIV agents. Adv. Exp. Med. Biol. 439, 191-225.
51. Wei, H., Tye, L., Bresnick, E., and Birt, D.F. (1990). Inhibitory effect of apigenin, a plant flavonoid, on epidermal ornithine decarboxylase and skin tumor promotion in mice. Cancer Res. 50, 499-502.
52. Weymouth-Wilson, A.C. (1997). The role of carbohydrates in biologically active natural products. Nat. Prod. Rep. 14, 99-110.
53. Wu, C.Z., Jang, J.H., Woo, M., Ahn, J.S., Kim, J.S., and Hong, Y.S. (2012). Enzymatic glycosylation of non-benzoquinone geldanamycin analogs via Bacillus UDP-glycosyltransferase. Appl. Environ. Microbiol. 78, 7680-7686.
54. Yassa, N., Saeidnia, S., Pirouzi, R., Akbaripour, M., and Shafiee, A. (2007). Three phenolic glycosides and immunological properties of Achillea millefolium from Iran, population of Golestan. Daru 15, 49-52.
55. Zhang, Y., Jiao, J., Liu, C., Wu, X., and Zhang, Y. (2008). Isolation and purification of four flavone C-glycosides from antioxidant bamboo leaves by macroporous resin column chromatography and preparative high-performance liquid chromatography. Food Chem. 107, 1326-1336.