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Review

Update on tools for evaluation of uridine diphosphoglucuronosyltransferase polymorphisms

, PhD, & , PhD
Pages 879-894 | Published online: 15 Jul 2008

Bibliography

  • Dutton GJ. Glucuronic acid – free and combined. Academic press: New York and London; 1966
  • Remmel RP, Nagar S, Argikar U. Conjugative metabolism of drugs in Drug metabolism in drug design and development: Wiley Interscience, John Wiley and Sons, Inc. 2008
  • Delaforge M, Pruvost A, Perrin L, Andre F. Cytochrome P450-mediated oxidation of glucuronide derivatives: example of estradiol-17beta-glucuronide oxidation to 2-hydroxy-estradiol-17beta-glucuronide by CYP 2C8. Drug Metab Dispos 2005;33(3):466-73
  • Mohan J, Gandhi AA, Bhavya BC, et al. Caspase-2 triggers Bax-Bak-dependent and -independent cell death in colon cancer cells treated with resveratrol. J Biol Chem 2006;281(26):17599-611
  • Burchell B, Blanckaert N. Bilirubin mono- and di-glucuronide formation by purified rat liver microsomal bilirubin UDP-glucuronyltransferase. Biochem J 1984;223(2):461-5
  • Peters WH, Jansen PL, Nauta H. The molecular weights of UDP-glucuronyltransferase determined with radiation-inactivation analysis. A molecular model of bilirubin UDP-glucuronyltransferase. J Biol Chem 1984;259(19):11701-05
  • Ritter JK, Crawford JM, Owens IS. Cloning of two human liver bilirubin UDP-glucuronosyltransferase cDNAs with expression in COS-1 cells. J Biol Chem 1991;266(2):1043-7
  • Bock KW, Gschaidmeier H, Seidel A, et al. Mono- and diglucuronide formation from chrysene and benzo(a)pyrene phenols by 3-methylcholanthrene-inducible phenol UDP-glucuronosyltransferase (UGT1A1). Mol Pharmacol 1992;42(4):613-8
  • Gschaidmeier H, Bock KW. Radiation inactivation analysis of microsomal UDP-glucuronosyltransferases catalysing mono- and diglucuronide formation of 3,6-dihydroxybenzo(a)pyrene and 3,6-dihydroxychrysene. Biochem Pharmacol 1994;48(8):1545-9
  • Ritter JK, Chen F, Sheen YY, et al. A novel complex locus UGT1 encodes human bilirubin, phenol, and other UDP-glucuronosyltransferase isozymes with identical carboxyl termini. J Biol Chem 1992;267(5):3257-61
  • Mackenzie PI, Walter Bock K, Burchell B, et al. Nomenclature update for the mammalian UDP glycosyltransferase (UGT) gene superfamily. Pharmacogenet Genomics 2005;15(10):677-85
  • Jedlitschky G, Cassidy AJ, Sales M, et al. Cloning and characterization of a novel human olfactory UDP-glucuronosyltransferase. Biochem J 1999;340(Pt 3):837-43
  • Available from: http://som.flinders.edu.au/FUSA/ClinPharm/UGT/
  • Tukey RH, Strassburg CP. Human UDP-glucuronosyltransferases: metabolism, expression, and disease. Ann Rev Pharmacol Toxicol 2000;40:581-616
  • Levesque E, Turgeon D, Carrier JS, et al. Isolation and characterization of the UGT2B28 cDNA encoding a novel human steroid conjugating UDP-glucuronosyltransferase. Biochemistry 2001;40(13):3869-81
  • Ung D, Nagar S. Variable sulfation of dietary polyphenols by recombinant human sulfotransferase (SULT) 1A1 genetic variants and SULT1E1. Drug Metab Dispos 2007;35(5):740-6
  • Guillemette C. Pharmacogenomics of human UDP-glucuronosyltransferase enzymes. Pharmacogenomics J 2003;3:136-58
  • Nagar S, Remmel RP. Uridine diphosphoglucuronosyltransferase pharmacogenetics and cancer. Oncogene 2006;25(11):1659-72
  • Saeki M, Saito Y, Jinno H, et al. Genetic variations and haplotypes of UGT1A4 in a Japanese population. Drug Metab Pharmacokinet 2005;20(2):144-51
  • Saeki M, Saito Y, Jinno H, et al. Genetic polymorphisms of UGT1A6 in a Japanese population. Drug Metab Pharmacokinet 2005;20(1):85-90
  • Saeki M, Saito Y, Jinno H, et al. Single nucleotide polymorphisms and haplotype frequencies of UGT2B4 and UGT2B7 in a Japanese population. Drug Metab Dispos 2004;32(9):1048-54
  • Carlini LE, Meropol NJ, Bever J, et al. UGT1A7 and UGT1A9 polymorphisms predict response and toxicity in colorectal cancer patients treated with capecitabine/irinotecan. Clin Cancer Res 2005;11(3):1226-36
  • Kimchi-Sarfaty C, Oh JM, Kim IW, et al. A “silent” polymorphism in the MDR1 gene changes substrate specificity. Science (New York NY) 2007;315(5811):525-8
  • Nebert DW, Zhang G, Vesell ES. From human genetics and genomics to pharmacogenetics and pharmacogenomics: past lessons, future directions. Drug Metab Rev 2008;40(2):187-224
  • Cartegni L, Chew SL, Krainer AR. Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat Rev Genet 2002;3(4):285-98
  • Bosma PJ, Chowdhury JR, Bakker C, et al. The genetic basis of the reduced expression of bilirubin UDP-glucuronosyltransferase 1 in Gilbert's syndrome. N Engl J Med 1995;333(18):1171-5
  • Innocenti F, Undevia SD, Iyer L, et al. Genetic variants in the UDP-glucuronosyltransferase 1A1 gene predict the risk of severe neutropenia of irinotecan. J Clin Oncol 2004;22(8):1382-8
  • Guillemette C, Millikan RC, Newman B, Housman DE. Genetic polymorphisms in uridine diphospho-glucuronosyltransferase 1A1 and association with breast cancer among African Americans. Cancer Res 2000;60(4):950-6
  • Burchell B. Genetic variation of human UDP-glucuronosyltransferase. Implications in disease and drug glucuronidation. Am J Pharmacogenomics 2003;3:37-52
  • Nagar S, Blanchard RL. Pharmacogenetics of uridine diphosphoglucuronosyltransferase (UGT) 1A family members and its role in patient response to irinotecan. Drug Metab Rev 2006;38(3):393-409
  • Burchell B, Brierley CH, Rance D. Specificity of human UDP-glucuronosyltransferases and xenobiotic glucuronidation. Life Sci 1995;57(20):1819-31
  • Burchell B, Coughtrie MW. Genetic and environmental factors associated with variation of human xenobiotic glucuronidation and sulfation. Environ Health Perspect 1997;105(Suppl 4):739-47
  • Mackenzie PI, Owens IS, Burchell B, et al. The UDP glycosyltransferase gene superfamily: recommended nomenclature update based on evolutionary divergence. Pharmacogenetics 1997;7(4):255-69
  • de Wildt SN, Kearns GL, Leeder JS, van den Anker JN. Glucuronidation in humans. Pharmacogenetic and developmental aspects. Clin Pharmacokinet 1999;36(6):439-52
  • Walker J, Rapley R. Molecular biology and biotechnology. 4th edition. Royal Society of Chemistry; 2001
  • de Wet JR, Wood KV, DeLuca M, et al. Firefly luciferase gene: structure and expression in mammalian cells. Mol Cell Biol 1987;7(2):725-37
  • Bosma PJ, Chowdhury JR, Huang TJ, et al. Mechanisms of inherited deficiencies of multiple UDP-glucuronosyltransferase isoforms in two patients with Crigler-Najjar syndrome, type I. FASEB J 1992;6(10):2859-63
  • Beutler E, Gelbart T, Demina A. Racial variability in the UDP-glucuronosyltransferase 1 (UGT1A1) promoter: a balanced polymorphism for regulation of bilirubin metabolism? Proc Natl Acad Sci USA 1998;95(14):8170-4
  • Hsieh TY, Shiu TY, Huang SM, et al. Molecular pathogenesis of Gilbert's syndrome: decreased TATA-binding protein binding affinity of UGT1A1 gene promoter. Pharmacogenet Genomics 2007;17(4):229-36
  • Yamanaka H, Nakajima M, Katoh M, et al. A novel polymorphism in the promoter region of human UGT1A9 gene (UGT1A9*22) and its effects on the transcriptional activity. Pharmacogenetics 2004;14(5):329-32
  • Girard H, Villeneuve L, Court MH, et al. The novel UGT1A9 intronic I399 polymorphism appears as a predictor of 7-ethyl-10-hydroxycamptothecin glucuronidation levels in the liver. Drug Metab Dispos 2006;34(7):1220-8
  • Ramirez J, Liu W, Mirkov S, et al. Lack of association between common polymorphisms in UGT1A9 and gene expression and activity. Drug Metab Dispos 2007;35(12):2149-53
  • Iyer L, Hall D, Das S, et al. Phenotype-genotype correlation of in vitro SN-38 (active metabolite of irinotecan) and bilirubin glucuronidation in human liver tissue with UGT1A1 promoter polymorphism. Clin Pharmacol Ther 1999;65(5):576-82
  • Fang JL, Lazarus P. Correlation between the UDP-glucuronosyltransferase (UGT1A1) TATAA box polymorphism and carcinogen detoxification phenotype: significantly decreased glucuronidating activity against benzo(a)pyrene-7,8-dihydrodiol(-) in liver microsomes from subjects with the UGT1A1*28 variant. Cancer Epidemiol Biomarkers Prev 2004;13(1):102-9
  • Raijmakers MT, Jansen PL, Steegers EA, Peters WH. Association of human liver bilirubin UDP-glucuronyltransferase activity with a polymorphism in the promoter region of the UGT1A1 gene. J Hepatol 2000;33(3):348-51
  • Yoder Graber AL, Ramirez J, Innocenti F, Ratain MJ. UGT1A1*28 genotype affects the in vitro glucuronidation of thyroxine in human livers. Pharmacogenet Genomics 2007;17(8):619-27
  • Berens C, Hillen W. Gene regulation by tetracyclines. Constraints of resistance regulation in bacteria shape TetR for application in eukaryotes. Eur J Biochem 2003;270(15):3109-21
  • Yueh MF, Tukey RH. Nrf2-Keap1 signaling pathway regulates human UGT1A1 expression in vitro and in transgenic UGT1 mice. J Biol Chem 2007;282(12):8749-58
  • Bonzo JA, Belanger A, Tukey RH. The role of chrysin and the ah receptor in induction of the human UGT1A1 gene in vitro and in transgenic UGT1 mice. Hepatology 2007;45(2):349-60
  • Liu X, Tam VH, Hu M. Disposition of flavonoids via enteric recycling: determination of the UDP-glucuronosyltransferase isoforms responsible for the metabolism of flavonoids in intact Caco-2 TC7 cells using siRNA. Mol Pharm 2007; 4(6):873-82
  • Chouinard S, Barbier O, Belanger A. UDP-glucuronosyltransferase 2B15 (UGT2B15) and UGT2B17 enzymes are major determinants of the androgen response in prostate cancer LNCaP cells. J Biol Chem 2007;282(46):33466-74
  • Soutschek J, Akinc A, Bramlage B, et al. Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature 2004;432(7014):173-8
  • Gong H, Sinz MW, Feng Y, et al. Animal models of xenobiotic receptors in drug metabolism and diseases. Methods Enzymol 2005;400:598-618
  • Tateno C, Yoshizane Y, Saito N, et al. Near completely humanized liver in mice shows human-type metabolic responses to drugs. Am J Pathol 2004;165(3):901-12
  • Katoh M, Matsui T, Nakajima M, et al. Expression of human cytochromes P450 in chimeric mice with humanized liver. Drug Metab Dispos 2004;32(12):1402-10
  • Katoh M, Watanabe M, Tabata T, et al. In vivo induction of human cytochrome P450 3A4 by rifabutin in chimeric mice with humanized liver. Xenobiotica 2005;35(9):863-75
  • Nishimura M, Yoshitsugu H, Yokoi T, et al. Evaluation of mRNA expression of human drug-metabolizing enzymes and transporters in chimeric mouse with humanized liver. Xenobiotica 2005;35(9):877-90
  • Katoh M, Yokoi T. Application of chimeric mice with humanized liver for predictive ADME. Drug Metab Rev 2007;39(1):145-57
  • Katoh M, Matsui T, Okumura H, et al. Expression of human Phase II enzymes in chimeric mice with humanized liver. Drug Metab Dispos 2005;33(9):1333-40
  • Okumura H, Katoh M, Sawada T, et al. Humanization of excretory pathway in chimeric mice with humanized liver. Toxicol Sci 2007;97(2):533-8
  • Chen S, Beaton D, Nguyen N, et al. Tissue-specific, inducible, and hormonal control of the human UDP-glucuronosyltransferase-1 (UGT1) locus. J Biol Chem 2005;280(45):37547-57
  • Senekeo-Effenberger K, Chen S, Brace-Sinnokrak E, et al. Expression of the human UGT1 locus in transgenic mice by 4-chloro-6-(2,3-xylidino)-2-pyrimidinylthioacetic acid (WY-14643) and implications on drug metabolism through peroxisome proliferator-activated receptor alpha activation. Drug Metab Dispos 2007;35(3):419-27
  • Verreault M, Senekeo-Effenberger K, Trottier J, et al. The liver X-receptor alpha controls hepatic expression of the human bile acid-glucuronidating UGT1A3 enzyme in human cells and transgenic mice. Hepatology 2006;44(2):368-78
  • Ariyoshi N, Imaoka S, Nakayama K, et al. Comparison of the levels of enzymes involved in drug metabolism between transgenic or gene-knockout and the parental mice. Toxicol Pathol 2001;29(Suppl):161-72
  • Girard H, Levesque E, Bellemare J, et al. Genetic diversity at the UGT1 locus is amplified by a novel 3′ alternative splicing mechanism leading to nine additional UGT1A proteins that act as regulators of glucuronidation activity. Pharmacogenet Genomics 2007;17(12):1077-89
  • Levesque E, Girard H, Journault K, et al. Regulation of the UGT1A1 bilirubin-conjugating pathway: role of a new splicing event at the UGT1A locus. Hepatology 2007;45(1):128-38
  • Vogel A, Ockenga J, Ehmer U, et al. Polymorphisms of the carcinogen detoxifying UDP-glucuronosyltransferase UGT1A7 in proximal digestive tract cancer. Z Gastroenterol 2002;40(7):497-502
  • Strassburg CP, Kneip S, Topp J, et al. Polymorphic gene regulation and interindividual variation of UDP-glucuronosyltransferase activity in human small intestine. J Biol Chem 2000;275(46):36164-71
  • Patten C. New technologies for assessing UDP-glucuronosyltransferase (UGT) metabolism in drug discovery and development. Drug Discov Today Technol 2006;3(1):73-8
  • Miners JO, Knights KM, Houston JB, Mackenzie PI. In vitro-in vivo correlation for drugs and other compounds eliminated by glucuronidation in humans: pitfalls and promises. Biochem Pharmacol 2006;71(11):1531-9
  • Court MH. Isoform-selective probe substrates for in vitro studies of human UDP-glucuronosyltransferases. Methods Enzymol 2005;400:104-16
  • Hirota T, Ieiri I, Takane H, et al. Sequence variability and candidate gene analysis in two cancer patients with complex clinical outcomes during morphine therapy. Drug Metab Dispos 2003;31(5):677-80
  • Koiwai O, Nishizawa M, Hasada K, et al. Gilbert's syndrome is caused by a heterozygous missense mutation in the gene for bilirubin UDP-glucuronosyltransferase. Hum Mol Genet 1995;4(7):1183-6
  • Iwai M, Maruo Y, Ito M, et al. Six novel UDP-glucuronosyltransferase (UGT1A3) polymorphisms with varying activity. J Hum Genet 2004;49(3):123-8
  • Ehmer U, Vogel A, Schutte JK, et al. Variation of hepatic glucuronidation: Novel functional polymorphisms of the UDP-glucuronosyltransferase UGT1A4. Hepatology 2004;39(4):970-7
  • Nagar S, Zalatoris JJ, Blanchard RL. Human UGT1A6 pharmacogenetics: identification of a novel SNP, characterization of allele frequencies and functional analysis of recombinant allozymes in human liver tissue and in cultured cells. Pharmacogenetics 2004;14(8):487-99
  • Ciotti M, Marrone A, Potter C, Owens IS. Genetic polymorphism in the human UGT1A6 (planar phenol) UDP-glucuronosyltransferase: pharmacological implications. Pharmacogenetics 1997;7(6):485-95
  • Villeneuve L, Girard H, Fortier LC, et al. Novel functional polymorphisms in the UGT1A7 and UGT1A9 glucuronidating enzymes in Caucasian and African-American subjects and their impact on the metabolism of 7-ethyl-10-hydroxycamptothecin and flavopiridol anticancer drugs. J Pharmacol Exp Ther 2003;307(1):117-28
  • Guillemette C, Ritter JK, Auyeung DJ, et al. Structural heterogeneity at the UDP-glucuronosyltransferase 1 locus: functional consequences of three novel missense mutations in the human UGT1A7 gene. Pharmacogenetics 2000;10(7):629-44
  • Huang YH, Galijatovic A, Nguyen N, et al. Identification and functional characterization of UDP-glucuronosyltransferases UGT1A8*1, UGT1A8*2 and UGT1A8*3. Pharmacogenetics 2002;12(4):287-97
  • Girard H, Court MH, Bernard O, et al. Identification of common polymorphisms in the promoter of the UGT1A9 gene: evidence that UGT1A9 protein and activity levels are strongly genetically controlled in the liver. Pharmacogenetics 2004;14(8):501-15
  • Saeki M, Saito Y, Jinno H, et al. Three novel single nucleotide polymorphisms in UGT1A9. Drug Metab Pharmacokinet 2003;18(2):146-9
  • Jinno H, Hanioka N, Tanaka-Kagawa T, et al. Transfection assays with allele-specific constructs: functional analysis of UDP-glucuronosyltransferase variants. Methods Mol Biol 2005;311:19-29
  • Saeki M, Ozawa S, Saito Y, et al. Three novel single nucleotide polymorphisms in UGT1A10. Drug Metab Pharmacokinet 2002;17(5):488-90
  • Elahi A, Bendaly J, Zheng Z, et al. Detection of UGT1A10 polymorphisms and their association with orolaryngeal carcinoma risk. Cancer 2003;98(4):872-80
  • Levesque E, Beaulieu M, Hum DW, Belanger A. Characterization and substrate specificity of UGT2B4 (E458): a UDP-glucuronosyltransferase encoded by a polymorphic gene. Pharmacogenetics 1999;9(2):207-16
  • Bhasker CR, McKinnon W, Stone A, et al. Genetic polymorphism of UDP-glucuronosyltransferase 2B7 (UGT2B7) at amino acid 268: ethnic diversity of alleles and potential clinical significance. Pharmacogenetics 2000;10(8):679-85
  • Levesque E, Beaulieu M, Green MD, et al. Isolation and characterization of UGT2B15(Y85): a UDP-glucuronosyltransferase encoded by a polymorphic gene. Pharmacogenetics 1997;7(4):317-25
  • Court MH, Hao Q, Krishnaswamy S, et al. UDP-glucuronosyltransferase (UGT) 2B15 pharmacogenetics: UGT2B15 D85Y genotype and gender are major determinants of oxazepam glucuronidation by human liver. J Pharmacol Exp Ther 2004;310(2):656-65
  • Iida A, Saito S, Sekine A, et al. Catalog of 86 single-nucleotide polymorphisms (SNPs) in three uridine diphosphate glycosyltransferase genes: UGT2A1, UGT2B15, and UGT8. J Hum Genet 2002;47(10):505-10
  • Sugatani J, Mizushima K, Osabe M, et al. Transcriptional regulation of human UGT1A1 gene expression through distal and proximal promoter motifs: implication of defects in the UGT1A1 gene promoter. Naunyn Schmiedebergs Arch Pharmacol 2008
  • Caillier B, Lepine J, Tojcic J, et al. A pharmacogenomics study of the human estrogen glucuronosyltransferase UGT1A3. Pharmacogenet Genomics 2007;17(7):481-95
  • Strassburg CP, Vogel A, Kneip S, et al. Polymorphisms of the human UDP-glucuronosyltransferase (UGT) 1A7 gene in colorectal cancer. Gut 2002;50(6):851-6
  • Bernard O, Tojcic J, Journault K, et al. Influence of nonsynonymous polymorphisms of UGT1A8 and UGT2B7 metabolizing enzymes on the formation of phenolic and acyl glucuronides of mycophenolic acid. Drug Metab Dispos 2006;34(9):1539-45
  • Thibaudeau J, Lepine J, Tojcic J, et al. Characterization of common UGT1A8, UGT1A9, and UGT2B7 variants with different capacities to inactivate mutagenic 4-hydroxylated metabolites of estradiol and estrone. Cancer Res 2006;66(1):125-33
  • Jinno H, Saeki M, Saito Y, et al. Functional characterization of human UDP-glucuronosyltransferase 1A9 variant, D256N, found in Japanese cancer patients. J Pharmacol Exp Ther 2003;306(2):688-93
  • Jinno H, Saeki M, Tanaka-Kagawa T, et al. Functional characterization of wild-type and variant (T202I and M59I) human UDP-glucuronosyltransferase 1A10. Drug Metab Dispos 2003;31(5):528-32
  • Martineau I, Tchernof A, Belanger A. Amino acid residue ILE211 is essential for the enzymatic activity of human UDP-glucuronosyltransferase 1A10 (UGT1A10). Drug Metab Dispos 2004;32(4):455-9
  • Holthe M, Rakvag TN, Klepstad P, et al. Sequence variations in the UDP-glucuronosyltransferase 2B7 (UGT2B7) gene: identification of 10 novel single nucleotide polymorphisms (SNPs) and analysis of their relevance to morphine glucuronidation in cancer patients. Pharmacogenomics J 2003;3(1):17-26
  • Duguay Y, Baar C, Skorpen F, Guillemette C. A novel functional polymorphism in the uridine diphosphate-glucuronosyltransferase 2B7 promoter with significant impact on promoter activity. Clin Pharmacol Ther 2004;75(3):223-33
  • Fisher MB, Vandenbranden M, Findlay K, et al. Tissue distribution and interindividual variation in human UDP-glucuronosyltransferase activity: relationship between UGT1A1 promoter genotype and variability in a liver bank. Pharmacogenetics 2000;10(8):727-39
  • Innocenti F, Grimsley C, Das S, et al. Haplotype structure of the UDP-glucuronosyltransferase 1A1 promoter in different ethnic groups. Pharmacogenetics 2002;12(9):725-33
  • Innocenti F, Liu W, Chen P, et al. Haplotypes of variants in the UDP-glucuronosyltransferase1A9 and 1A1 genes. Pharmacogenet Genomics 2005;15(5):295-301
  • Peters WH, te Morsche RH, Roelofs HM. Combined polymorphisms in UDP-glucuronosyltransferases 1A1 and 1A6: implications for patients with Gilbert's syndrome. J Hepatol 2003;38(1):3-8
  • Peterkin VC, Bauman JN, Goosen TC, et al. Limited influence of UGT1A1*28 and no effect of UGT2B7*2 polymorphisms on UGT1A1 or UGT2B7 activities and protein expression in human liver microsomes. Br J Clin Pharmacol 2007;64(4):458-68
  • Wiener D, Fang JL, Dossett N, Lazarus P. Correlation between UDP-glucuronosyltransferase genotypes and 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone glucuronidation phenotype in human liver microsomes. Cancer Res 2004;64(3):1190-6
  • Krishnaswamy S, Hao Q, Al-Rohaimi A, et al. UDP glucuronosyltransferase (UGT) 1A6 pharmacogenetics: II. Functional impact of the three most common nonsynonymous UGT1A6 polymorphisms (S7A, T181A, and R184S). J Pharmacol Exp Ther 2005;313(3):1340-6
  • Chen G, Blevins-Primeau AS, et al. Glucuronidation of nicotine and cotinine by UGT2B10: loss of function by the UGT2B10 Codon 67 (Asp>Tyr) polymorphism. Cancer Res 2007;67(19):9024-9
  • Chen G, Dellinger RW, Gallagher CJ, et al. Identification of a prevalent functional missense polymorphism in the UGT2B10 gene and its association with UGT2B10 inactivation against tobacco-specific nitrosamines. Pharmacogenet Genomics 2008;18(3):181-91

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