Suppression of cytochrome P450 3A4 function by UDP-glucuronosyltransferase 2B7 through a protein-protein interaction: Cooperative roles of the cytosolic carboxyl-terminal domain and the luminal anchoring region

Molecular Pharmacology

Volumn 88, Issue 4, 2015, Pages 800-812

  Miyauchi, Yuu ^a   Nagata, Kiyoshi ^b   Yamazoe, Yasushi ^c   Mackenzie, Peter I ^d   Yamada, Hideyuki ^a   Ishii, Yuji ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b TOHOKU PHARMACEUTICAL UNIVERSITY   (Japan)

^c Food Safety Commission of Japan   (Japan)

^d FLINDERS UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CALNEXIN; CYSTEINE; CYTOCHROME P450 3A4; GLUCURONOSYLTRANSFERASE 2B7; IMIDAZOLE; TESTOSTERONE; CYP3A4 PROTEIN, HUMAN; CYTOCHROME P450 3A; GLUCURONOSYLTRANSFERASE; PROTEIN BINDING; UGT2B7 PROTEIN, HUMAN;

ARTICLE; BACULOVIRIDAE; CARBOXY TERMINAL SEQUENCE; CHIMERA; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REPRESSION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; KINETIC PARAMETERS; LIPOPHILICITY; LUMINAL ANCHORING REGION; MEMBRANE STRUCTURE; MICHAELIS MENTEN KINETICS; MICROSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; SF9 CELL LINE; SUBSTRATE CONCENTRATION; ANIMAL; BINDING SITE; CELL LINE; CYTOSOL; ENZYMOLOGY; INSECT; LIVER MICROSOME; METABOLISM; PHYSIOLOGY; PROTEIN DOMAIN;

ANIMALS; BINDING SITES; CELL LINE; CYTOCHROME P-450 CYP3A; CYTOSOL; GLUCURONOSYLTRANSFERASE; HUMANS; INSECTS; MICROSOMES, LIVER; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS;

EID: 84946560163     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.115.098582     Document Type: Article

References (59)

1. Ahn T, Guengerich FP, and Yun CH (1998) Membrane insertion of cytochrome P450 1A2 promoted by anionic phospholipids. Biochemistry 37:12860-12866.
2. Backes WL and Kelley RW (2003) Organization of multiple cytochrome P450s with NADPH-cytochrome P450 reductase in membranes. Pharmacol Ther 98:221-233.
3. Barbier O, Girard C, Breton R, Bélanger A, and Hum DW (2000) N-glycosylation and residue 96 are involved in the functional properties of UDP-glucuronosyltransferase enzymes. Biochemistry 39:11540-11552.
4. Bergeron JJ, Brenner MB, Thomas DY, and Williams DB (1994) Calnexin: A membrane- bound chaperone of the endoplasmic reticulum. Trends Biochem Sci 19: 124-128.
5. Bridges A, Gruenke L, Chang YT, Vakser IA, Loew G, and Waskell L (1998) Identification of the binding site on cytochrome P450 2B4 for cytochrome b5 and cytochrome P450 reductase. J Biol Chem 273:17036-17049.
6. Chefson A, Zhao J, and Auclair K (2006) Replacement of natural cofactors by selected hydrogen peroxide donors or organic peroxides results in improved activity for CYP3A4 and CYP2D6. Chem Bio Chem 7:916-919.
7. Cole C, Barber JD, and Barton GJ (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36:W197-W201.
8. Crespi CL and Miller VP (1999) The use of heterologously expressed drug metabolizing enzymes-state of the art and prospects for the future. Pharmacol Ther 84: 121-131.
9. David V, Hochstenbach F, Rajagopalan S, and Brenner MB (1993) Interaction with newly synthesized and retained proteins in the endoplasmic reticulum suggests a chaperone function for human integral membrane protein IP90 (calnexin). J Biol Chem 268:9585-9592.
10. Davydov DR (2011) Microsomal monooxygenase as a multienzyme system: The role of P450-P450 interactions. Expert Opin Drug Metab Toxicol 7:543-558.
11. Fujiwara R, Nakajima M, Yamanaka H, Katoh M, and Yokoi T (2007) Interactions between human UGT1A1, UGT1A4, and UGT1A6 affect their enzymatic activities. Drug Metab Dispos 35:1781-1787.
12. Guengerich FP (1999) Cytochrome P-450 3A4: regulation and role in drug metabolism. Annu Rev Pharmacol Toxicol 39:1-17.
13. Hildebrandt A and Estabrook RW(1971) Evidence for the participation of cytochrome b5 in hepatic microsomal mixed-function oxidation reactions. Arch Biochem Biophys 143:66-79.
14. Hirota T, Ieiri I, Takane H, Maegawa S, Hosokawa M, Kobayashi K, Chiba K, Nanba E, Oshimura M, and Sato T et al. (2004) Allelic expression imbalance of the human CYP3A4 gene and individual phenotypic status. Hum Mol Genet 13:2959-2969.
15. Imai Y (1976) The use of 8-aminooctyl sepharose for the separation of some components of the hepatic microsomal electron transfer system. J Biochem 80:267-276.
16. Ishii Y, Iwanaga M, Nishimura Y, Takeda S, Ikushiro S, Nagata K, Yamazoe Y, Mackenzie PI, and Yamada H (2007) Protein-protein interactions between rat hepatic cytochromes P450 (P450s) and UDP-glucuronosyltransferases (UGTs): evidence for the functionally active UGT in P450-UGT complex. Drug Metab Pharmacokinet 22:367-376.
17. Ishii Y, Koba H, Kinoshita K, Oizaki T, Iwamoto Y, Takeda S, Miyauchi Y, Nishimura Y, Egoshi N, and Taura F et al. (2014) Alteration of the function of the UDPUGT2B7 glucuronosyltransferase 1A subfamily by cytochrome P450 3A4: different susceptibility for UGT isoforms and UGT1A1/7 variants. Drug Metab Dispos 42:229-238.
18. Ishii Y, Miyoshi A, Watanabe R, Tsuruda K, Tsuda M, Yamaguchi-Nagamatsu Y, Yoshisue K, Tanaka M, Maji D, and Ohgiya S et al. (2001) Simultaneous expression of guinea pig UDP-glucuronosyltransferase 2B21 and 2B22 in COS-7 cells enhances UDP-glucuronosyltransferase 2B21-catalyzed morphine-6-glucuronide formation. Mol Pharmacol 60:1040-1048.
19. Ishii Y, Takeda S, and Yamada H (2010) Modulation of UDP-glucuronosyltransferase activity by protein-protein association. Drug Metab Rev 42:145-158.
20. Ishii Y, Takeda S, Yamada H, and Oguri K (2005) Functional protein-protein interaction of drug metabolizing enzymes. Front Biosci 10:887-895.
21. Isin EM and Guengerich FP (2008) Substrate binding to cytochromes P450. Anal Bioanal Chem 392:1019-1030.
22. Jin CJ, Miners JO, Burchell B, and Mackenzie PI (1993) The glucuronidation of hydroxylated metabolites of benzo[a]pyrene and 2-acetylaminofluorene by cDNAexpressed human UDP-glucuronosyltransferases. Carcinogenesis 14:2637-2639.
23. Kaminsky LS, Guengerich FP, Dannan GA, and Aust SD (1983) Comparisons of warfarin metabolism by liver microsomes of rats treated with a series of polybrominated biphenyl congeners and by the component-purified cytochrome P-450 isozymes. Arch Biochem Biophys 225:398-404.
24. Kim KH, Ahn T, and Yun CH (2003) Membrane properties induced by anionic phospholipids and phosphatidylethanolamine are critical for the membrane binding and catalytic activity of human cytochrome P450 3A4. Biochemistry 42:15377-15387.
25. Lakhman SS, Ma Q, and Morse GD (2009) Pharmacogenomics of CYP3A: considerations for HIV treatment. Pharmacogenomics 10:1323-1339.
26. Lamba JK, Lin YS, Schuetz EG, and Thummel KE (2002) Genetic contribution to variable human CYP3A-mediated metabolism. Adv Drug Deliv Rev 54:1271-1294.
27. Laursen T, Jensen K, and Møller BL (2011) Conformational changes of the NADPHdependent cytochrome P450 reductase in the course of electron transfer to cytochromes P450. Biochim Biophys Acta 1814:132-138.
28. Lewis BC, Mackenzie PI, and Miners JO (2011) Homodimerization of UDPglucuronosyltransferase 2B7 (UGT2B7) and identification of a putative dimerization domain by protein homology modeling. Biochem Pharmacol 82:2016-2023.
29. Locuson CW, Wienkers LC, Jones JP, and Tracy TS (2007) CYP2C9 protein interactions with cytochrome b5: effects on the coupling of catalysis. Drug Metab Dispos 35:1174-1181.
30. Lowry OH, Rosebrough NJ, Farr AL, and Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275.
31. Lu AY, Junk KW, and Coon MJ (1969) Resolution of the cytochrome P-450-containing v-hydroxylation system of liver microsomes into three components. J Biol Chem 244:3714-3721.
32. Mackenzie PI (1986) Rat liver UDP-glucuronosyltransferase. cDNA sequence and expression of a form glucuronidating 3-hydroxyandrogens. J BiolChem 261:14112-14117.
33. Mackenzie PI (1990) The effect of N-linked glycosylation on the substrate preferences of UDP glucuronosyltransferases. Biochem Biophys Res Commun 166:1293-1299.
34. Mackenzie PI, Hjelmeland LM, and Owens IS (1984) Purification and immunochemical characterization of a low-pI form of UDP glucuronosyltransferase from mouse liver. Arch Biochem Biophys 231:487-497.
35. Meech R and Mackenzie PI (1998) Determinants of UDP glucuronosyltransferase membrane association and residency in the endoplasmic reticulum. Arch Biochem Biophys 356:77-85.
36. Miwa GT and Lu AY (1984) The association of cytochrome P-450 and NADPHcytochrome P-450 reductase in phospholipid membranes. Arch Biochem Biophys 234:161-166.
37. Möller S, Croning MD, and Apweiler R (2001) Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17:646-653.
38. Nakajima M, Koga T, Sakai H, Yamanaka H, Fujiwara R, and Yokoi T (2010) N-Glycosylation plays a role in protein folding of human UGT1A9. Biochem Pharmacol 79:1165-1172.
39. Omura T (2011) Recollection of the early years of the research on cytochrome P450. Proc Jpn Acad, Ser B, Phys Biol Sci 87:617-640.
40. Omura T and Sato R (1964) The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. J Biol Chem 239:2370-2378.
41. Ouzzine M, Magdalou J, Burchell B, and Fournel-Gigleux S (1999) An internal signal sequence mediates the targeting and retention of the human UDPglucuronosyltransferase 1A6 to the endoplasmic reticulum. J Biol Chem 274: 31401-31409.
42. Pan YZ, Gao W, and Yu AM (2009) MicroRNAs regulate CYP3A4 expression via direct and indirect targeting. Drug Metab Dispos 37:2112-2117.
43. Radominska-Pandya A, Czernik PJ, Little JM, Battaglia E, and Mackenzie PI (1999) Structural and functional studies of UDP-glucuronosyltransferases. Drug Metab Rev 31:817-899.
44. Reed JR and Backes WL (2012) Formation of P450×P450 complexes and their effect on P450 function. Pharmacol Ther 133:299-310.
45. Schenkman JB and Jansson I (2006) Spectral analyses of cytochromes P450. Methods Mol Biol 320:11-18.
46. Schenkman JB, Remmer H, and Estabrook RW (1967) Spectral studies of drug interaction with hepatic microsomal cytochrome. Mol Pharmacol 3:113-123.
47. Shimada T, Yamazaki H, Mimura M, Inui Y, and Guengerich FP (1994) Interindividual variations in human liver cytochrome P-450 enzymes involved in the oxidation of drugs, carcinogens and toxic chemicals: studies with liver microsomes of 30 Japanese and 30 Caucasians. J Pharmacol Exp Ther 270:414-423.
48. Singh D, Kashyap A, Pandey RV, and Saini KS (2011) Novel advances in cytochrome P450 research. Drug Discov Today 16:793-799.
49. Sonderfan AJ, Arlotto MP, Dutton DR, McMillen SK, and Parkinson A (1987) Regulation of testosterone hydroxylation by rat liver microsomal cytochrome P-450. Arch Biochem Biophys 255:27-41.
50. Takagi S, Nakajima M, Mohri T, and Yokoi T (2008) Post-transcriptional regulation of human pregnane X receptor by micro-RNA affects the expression of cytochrome P450 3A4. J Biol Chem 283:9674-9680.
51. Takeda S, Ishii Y, Iwanaga M, Mackenzie PI, Nagata K, Yamazoe Y, Oguri K, and Yamada H (2005) Modulation of UDP-glucuronosyltransferase function by cytochrome P450: evidence for the alteration of UGT2B7-catalyzed glucuronidation of morphine by CYP3A4. Mol Pharmacol 67:665-672.
52. Takeda S, Ishii Y, Iwanaga M, Nurrochmad A, Ito Y, Mackenzie PI, Nagata K, Yamazoe Y, Oguri K, and Yamada H (2009) Interaction of cytochrome P450 3A4 and UDPglucuronosyltransferase 2B7: evidence for protein-protein association and possible involvement of CYP3A4 J-helix in the interaction. Mol Pharmacol 75:956-964.
53. Taura K, Naito E, Ishii Y, Mori MA, Oguri K, and Yamada H (2004) Cytochrome P450 1A1 (CYP1A1) inhibitor a-naphthoflavone interferes with UDP-glucuronosyltransferase (UGT) activity in intact but not in permeabilized hepatic microsomes from 3-methylcholanthrene-treated rats: possible involvement of UGT-P450 interactions. Biol Pharm Bull 27:56-60.
54. Taura K, Yamada H, Hagino Y, Ishii Y, Mori MA, and Oguri K (2000) Interaction between cytochrome P450 and other drug-metabolizing enzymes: evidence for an association of CYP1A1 with microsomal epoxide hydrolase and UDPglucuronosyltransferase. Biochem Biophys Res Commun 273:1048-1052.
55. Thummel KE and Wilkinson GR (1998) In vitro and in vivo drug interactions involving human CYP3A. Annu Rev Pharmacol Toxicol 38:389-430.
56. West SB and Lu AY (1972) Reconstituted liver microsomal enzyme system that hydroxylates drugs, other foreign compounds and endogenous substrates. V. Competition between cytochromes P-450 and P-448 for reductase in 3, 4-benzpyrene hydroxylation. Arch Biochem Biophys 153:298-303.
57. Wood AW, Ryan DE, Thomas PE, and Levin W (1983) Regio- And stereoselective metabolism of two C19 steroids by five highly purified and reconstituted rat hepatic cytochrome P-450 isozymes. J Biol Chem 258:8839-8847.
58. Yasukochi Y and Masters BS (1976) Some properties of a detergent-solubilized NADPH-cytochrome c (cytochrome P-450) reductase purified by biospecific affinity chromatography. J Biol Chem 251:5337-5344.
59. Zhang H, Patana AS, Mackenzie PI, Ikushiro S, Goldman A, and Finel M (2012) Human UDP-glucuronosyltransferase expression in insect cells: ratio of active to inactive recombinant proteins and the effects of a C-terminal his-tag on glucuronidation kinetics. Drug Metab Dispos 40:1935-1944.