A substrate-specific cytochrome P450 monooxygenase, CYP6AB11, from the polyphagous navel orangeworm (Amyelois transitella)

Insect Biochemistry and Molecular Biology

Volumn 41, Issue 4, 2011, Pages 244-253

  Niu, Guodong ^a   Rupasinghe, Sanjeewa G ^b   Zangerl, Arthur R ^a   Siegel, Joel P ^c   Schuler, Mary A ^b   Berenbaum, May R ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Amyelois transitella; Cytochrome P450 monooxygenase; Imperatorin; Insect plant interactions; Piperonyl butoxide

Indexed keywords

CYTOCHROME P450; INSECT PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; MOLECULAR GENETICS; MOTH; PARASITOLOGY; PHYLOGENY; PLANT DISEASE; SEQUENCE ALIGNMENT; TREE;

AMINO ACID SEQUENCE; ANIMALS; CYTOCHROME P-450 ENZYME SYSTEM; INSECT PROTEINS; LARVA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOTHS; PHYLOGENY; PLANT DISEASES; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY; TREES;

AMYELOIS TRANSITELLA; HEXAPODA; JUGLANS; LEPIDOPTERA; PISTACIA VERA; PRUNUS DULCIS; PYRALIDAE;

EID: 79952193511     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2010.12.009     Document Type: Article

References (69)

1. Baek N.I., Ahn E.M., Kim H.Y., Park Y.D. Furanocoumarins from the root of Angelica dahurica. Arch. Pharm. Res. 2000, 23:467-470.
2. Berenbaum M.R. Coumarins in Herbivores: Their Interactions with Secondary Plant Metabolites 1991, vol 1:221-249. San Diego. G. Rosenthal, M. Berenbaum (Eds.).
3. Berenbaum M.R., Zangerl A.R. Chemical phenotype matching between a plant and its insect herbivore. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:13743-13748.
4. Bolling B.W., DolnikowskiG.Blumberg J.B., Oliver Chen C.Y. Quantification of almond skin polyphenols by liquid chromatography-mass spectrometry. J. Food Sci. 2009, 74:C326-C332.
5. Byard J., Needham D. Metabolism and excretion of piperonyl butoxide in the rat. Xenobiotica 2006, 36:1259-1272.
6. Campbell B.C., Molyneux R.J., Schatzi T.F. Current research on reducing pre- and post-harvest aflatoxin contamination of US almond, pistachio, and walnut. J. Toxicol. Toxin Rev. 2003, 22:225-266.
7. Chen J.S., Berenbaum M.R., Schuler M.A. Amino acids in SRS1 and SRS6 are critical for furanocoumarin metabolism by CYP6B1v1, a cytochrome P450 monooxygenase. Insect Mol. Biol. 2002, 11:175-186.
8. Cohen M.B., Schuler M.A., Berenbaum M.R. A host-inducible cytochrome P-450 from a host-specific caterpillar: molecular cloning and evolution. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:10920-10924.
9. Connell J.H. Leading edge of plant protection for almond. Hort. Technol. 2001, 12:619-622.
10. Feyereisen R. Insect P450 enzymes. Annu. Rev. Entomol. 1999, 44:507-533.
11. Feyereisen R. Evolution of insect P450. Biochem. Soc. Trans. 2006, 34:1252-1255.
12. Halgren T.A. Merck molecular force field: I. basis, form, scope, parameterization and performance of MMFF94. J. Comp. Chem. 1996, 17:490-519.
13. Heppner J.B. Arthropods of Florida and neighboring land areas. Lepidoptera of Florida Part 1. Introduction and Catalogue 2003, vol. 17. Florida Department of Agriculture and Consumer Services, Gainesville.
14. Hung C.F., Prapaipong H., Berenbaum M.R., Schuler M.A. Differential induction of cytochrome P450 transcripts in Papilio polyxenes by linear and angular furanocoumarins. Insect Biochem. Mol. Biol. 1995, 25:89-99.
15. Hung C.F., Harrison T.L., Berenbaum M.R., Schuler M.A. CYP6B3: a second furanocoumarin-inducible cytochrome P450 expressed in Papilio polyxenes. Insect Mol. Biol. 1995, 4:149-160.
16. Hung C.F., Berenbaum M.R., Schuler M.A. Isolation and characterization of CYP6B4, a furanocoumarin-inducible cytochrome P450 from a polyphagous caterpillar (Lepidoptera: Papilionidae). Insect Biochem. Mol. Biol. 1997, 27:377-385.
17. Kimball C.P. The Lepidoptera of Florida: An Annotated Checklist 1965, Florida Department of Agriculture, Gainesville.
18. Kumar S., Tamura K., Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 2004, 5:150-163.
19. Lee S.E., Campbell B.C. In vitro metabolism of aflatoxin B1 by larvae of navel orangeworm, Amyelois transitella (Walker) (Insecta, Lepidoptera, Pyralidae) and codling moth, Cydia pomonella (L.) (Insecta, Lepidoptera, Tortricidae). Arch. Insect Biochem. Physiol. 2000, 45:166-174.
20. Li W., Petersen R.A., Schuler M.A., Berenbaum M.R. CYP6B cytochrome P450 monooxygenases from Papilio canadensis and Papilio glaucus, potential contributions of sequence divergence to host plant associations. Insect Mol. Biol. 2002, 11:543-551.
21. Li X., Berenbaum M.R., Schuler M.A. Plant allelochemicals differentially regulate Helicoverpa zea cytochrome P450 genes. Insect Mol. Biol. 2002, 11:343-351.
22. Li W., Schuler M.A., Berenbaum M.R. Diversification of furanocoumarin-metabolizing cytochrome P450 monooxygenases in two papilionids: specificity and substrate encounter rate. Proc. Natl. Acad. Sci. U.S.A. 2003, 100(Suppl. 2):14593-14598.
23. Li W., Zangerl A.R., Schuler M.A., Berenbaum M.R. Characterization and evolution of furanocoumarin-inducible cytochrome P450s in the parsnip webworm, Depressaria pastinacella. Insect Mol. Biol. 2004, 13:603-613.
24. Li X., Baudry J., Berenbaum M.R., Schuler M.A. Structural and functional divergence of insect CYP6B proteins: from specialist to generalist cytochrome P450. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:2939-2944.
25. Li X., Berenbaum M.R., Schuler M.A. Molecular cloning and expression of CYP6B8: a xanthotoxin-inducible cytochrome P450 cDNA from Helicoverpa zea. Insect Biochem. Mol. Biol. 2000, 30:75-84.
26. Li X., Schuler M.A., Berenbaum M.R. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu. Rev. Entomol. 2007, 52:231-253.
27. MacKerell A.D., Bashford D., Bellott M., Dunbrack R.L., Evanseck J.D., Field M.J., Fischer S., Gao J., Guo H., Ha S. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 1998, 102:3586-3616.
28. Mahoney N.E., Roitman J.N., Chan B.C. Structure-activity relationship of flavones as growth inhibitors of the navel orangeworm. J. Chem. Ecol. 1989, 15:285-290.
29. Mao W., Berhow M.A., Zangerl A.R., McGovern J., Berenbaum M.R. Cytochrome P450-mediated metabolism of xanthotoxin by Papilio multicaudatus. J. Chem. Ecol. 2006, 32:523-536.
30. Mao W., Rupasinghe S., Zangerl A.R., Schuler M.A., Berenbaum M.R. Remarkable substrate-specificity of CYP6AB3 in Depressaria pastinacella, a highly specialized caterpillar. Insect Mol. Biol. 2006, 15:169-179.
31. Mao W., Schuler M.A., Berenbaum M.R. Cytochrome P450s in Papilio multicaudatus and the transition from oligophagy to polyphagy in the Papilionidae. Insect Mol. Biol. 2007, 16:481-490.
32. Mao W., Rupasinghe S.G., Zangerl A.R., Berenbaum M.R., Schuler M.A. Allelic variation in the Depressaria pastinacella CYP6AB3 protein enhances metabolism of plant allelochemicals by altering a proximal surface residue and potential interactions with cytochrome P450 reductase. J. Biol. Chem. 2007, 282:10544-10552.
33. Mao W., Berenbaum M.R., Schuler M.A. Modifications in the N-terminus of an insect P450 enhance production of catalytically active protein in baculovirus-Sf9 cell expression systems. Insect Biochem. Mol. Biol. 2008, 38:66-75.
34. Mao W., Zangerl A.R., Berenbaum M.R., Schuler M.A. Metabolism of myristicin by Depressaria pastinacella CYP6AB3v2 and inhibition by its metabolite. Insect Biochem. Mol. Biol. 2008, 38:645-651.
35. McKay F., Gandalfo D. Phytophagous insects associated with the reproductive structures of mesquite (Prosopis spp.) in Argentina and their potential as biological control agents in South Africa. Afr. Entomol. 2007, 15:121-131.
36. Molyneux R.J., Mahoney N., Kim J.H., Campbell B.C. Mycotoxins in edible tree nuts. Int. J. Food Microbiol. 2007, 119:72-78.
37. Monteiro V.de F.F., Mathias L., Vieira I.J.C., Schripsema J., Braz-Filho R. Prenylated coumarins, chalcones and new cinnamic acid and dihydrocinnamic acid derivatives from Brosimum gaudichaudii. J. Brazil. Chem. Soc. 2002, 13.
38. Mote D.C. A new orange pest in Arizona. California State Dept. Agric. Mon. Bull. 1922, 11:628.
39. Murray R.D.H., Brown S.A., Mendez J. The Natural Coumarins: Occurrence, Chemistry and Biochemistry 1982, J. Wiley, New York.
40. Nelson D.R. Metazoan cytochrome P450 evolution. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 1998, 121:15-22.
41. Niu G., Wen Z., Rupasinghe S.G., Zeng R.S., Berenbaum M.R., Schuler M.A. Aflatoxin B1 detoxification by CYP321A1 in Helicoverpa zea. Arch. Insect Biochem. Physiol. 2008, 69:32-45.
42. Niu G., Siegel J., Schuler M.A., Berenbaum M.R. Comparative toxicity of mycotoxins to navel orangeworm (Amyelois transitella) and corn earworm (Helicoverpa zea). J. Chem. Ecol. 2009, 35:951-957.
43. Omura T., Sato R. The carbon monoxide-binding pigment of liver microsomes. II. Solubilization, purification, and properties. J. Biol. Chem. 1964, 239:2379-2385.
44. Ortiz de Montellano P.R. Cytochrome P450: Structure, Mechanism, and Biochemistry 2005, Kluwer Academic/Plenum Publishers, New York. third ed.
45. Pan L., Wen Z., Baudry J., Berenbaum M.R., Schuler M.A. Identification of variable amino acids in the SRS1 region of CYP6B1 modulating furanocoumarin metabolism. Arch. Biochem. Biophys. 2004, 422:31-41.
46. Ravichandran K.G., Boddupalli S.S., Hasemann C.A., Peterson J.A., Deisenhofer J. Crystal structure of hemoprotein domain of P450BM-3, a prototype for microsomal P450s. Science 1993, 261:731-736.
47. Rubilar M., Pinelo M., Shene C., Sineiro J., Nuñez M.J. Separation and HPLC-MS identification of phenolic antioxidants from agricultural residues: almond hulls and grape pomace. J. Agric. Food Chem. 2007, 55:10101-10109.
48. Rupasinghe S.G., Wen Z., Chiu T.L., Schuler M.A. Helicoverpa zea CYP6B8 and CYP321A1: different molecular solutions to the problem of metabolizing plant toxins and insecticides. Protein Eng. Design Select 2007, 20:615-624.
49. Sang S., Lapsley K., Rosen R.T., Ho C.T. New prenylated benzoic acid and other constituents from almond hulls (Prunus amygdalus Batsch). J. Agric. Food Chem. 2002, 50:607-609.
50. Sasabe M., Wen Z., Berenbaum M.R., Schuler M.A. Molecular analysis of CYP321A1, a novel cytochrome P450 involved in metabolism of plant allelochemicals (furanocoumarins) and insecticides (cypermethrin) in Helicoverpa zea. Gene 2004, 338:163-175.
51. Schatzki T.F., Ong M.S. Distribution of aflatoxin in almonds. 2. Distribution in almonds with heavy insect damage. J. Agric. Food Chem. 2000, 48:489-492.
52. Schatzki T.F., Ong M.S. Dependence of aflatoxin in almonds on the type and amount of insect damage. J. Agric. Food Chem. 2001, 49:4513-4519.
53. Schoch G.A., Yano J.K., Wester M.R., Griffin K.J., Stout C.D., Johnson E.F. Structure of human microsomal cytochrome P450 2C8. Evidence for a peripheral fatty acid binding site. J. Biol. Chem. 2004, 279:9497-9503.
54. Staples W.G., Elevitch C.R. Samanea saman (rain tree) Fabaceae (legume family). Traditional Trees of Pacific Islands: Their Culture, Environment, and Use 2006, 661-674. C.R. Elevitch (Ed.).
55. Tebbets J.S., Curtis C.E., Fries R.D. Mortality of immature stages of the navel orangeworm stored at 3.5 °C. J. Econ. Entomol 1978, 71:875-876.
56. Teets A.S., Minardi C.S., Sundararaman M., Hughey C.A., Were L.M. Extraction, identification, and quantification of flavonoids and phenolic acids in electron beam-irradiated almond skin powder. J. Food Sci. 2009, 74:C298-C305.
57. Towers G.H.N. Significance of phototoxic phytochemicals in insect herbivory. J. Chem. Ecol. 1986, 12:813-821.
58. UC IPM Online UC Pest Management guidelines: almond, navel orangeworm http://www.ipm.ucdavis.edu/PMG/r3300311.html.
59. Vaya J., Mahmood S. Flavonoid content in leaf extracts of the fig (Ficus carica L.), carob (Ceratonia siliqua L.) and pistachio (Pistacia lentiscus L.). Biofactors 2006, 28:169-175.
60. Veitch N.C. Isoflavonoids of the Leguminosae. Nat. Prod. Rep. 2009, 24:417-464.
61. Wen Z., Pan L., Berenbaum M.R., Schuler M.A. Metabolism of linear and angular furanocoumarins by Papilio polyxenes CYP6B1 co-expressed with NADPH cytochrome P450 reductase. Insect Biochem. Mol. Biol. 2003, 33:937-947.
62. Wen Z., Baudry J., Berenbaum M.R., Schuler M.A. Ile115Leu mutation in the SRS1 region of an insect cytochrome P450 (CYP6B1) compromises substrate turnover via changes in a predicted product release channel. Prot. Eng. Design Select 2005, 18:1-199.
63. Wen Z., Berenbaum M.R., Schuler M.A. Inhibition of CYP6B1-mediated detoxification of xanthotoxin by plant allelochemicals in the black swallowtail (Papilio polyxenes). J. Chem. Ecol. 2006, 32:507-522.
64. Wen Z., Rupasinghe S., Niu G., Berenbaum M.R., Schuler M.A. CYP6B1 and CYP6B3 of the black swallowtail (Papilio polyxenes): adaptive evolution through subfunctionalization. Mol. Biol. Evol. 2006, 23:2434-2443.
65. Wester M.R., Johnson E.F., Marques-Soares C., Dansette P.M., Mansuy D., Stout C.D. Structure of a substrate complex of mammalian cytochrome P450 2C5 at 2.3 Å resolution: evidence for multiple substrate binding modes. Biochemistry 2003, 42:6370-6379.
66. Widstrom N.W., Lillehoj B.E., Sparks N.A., Kwolek F.W. Corn earworm damage and aflatoxin B, on corn ears protected with insecticide. J. Econ. Entomol. 1976, 69:677-679.
67. Williams P.A., Cosme J., Ward A., Angove H.C., Vinković D.M., Jhoti H. Crystal structure of human cytochrome P450 2C9 with bound warfarin. Nature 2003, 424:464-468.
68. Yano J.K., Wester M.R., Schoch G.A., Griffin K.J., Stout C.D., Johnson E.F. The structure of human microsomal cytochrome P450 3A4 determined by X-ray crystallography to 2.05-A resolution. J. Biol. Chem. 2004, 279:38091-38094.
69. Zaynoun S.T., Aftimos B.G., Abi Ali L., Tenekjian K.K., Khalidi U., Kurban A.K. Ficus carica: isolation and quantification of the photoactive components. Contact Dermatitis 1984, 11:21-25.