UGT1A1*6 polymorphisms are correlated with irinotecan-induced toxicity: A system review and meta-analysis in Asians

Cancer Chemotherapy and Pharmacology

Volumn 73, Issue 3, 2014, Pages 551-560

  Cheng, Lei ^a   Li, Ming ^a   Hu, Jing ^a   Ren, Wei ^a   Xie, Li ^a   Sun, Zhan Peng ^b   Liu, Bao Rui ^a   Xu, Gen Xing ^a   Dong, Xiao Liang ^a   Qian, Xiao Ping ^a  

^a NANJING UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

Cancer; Irinotecan; Meta analysis; Polymorphisms; Toxicity; UGT1A1*6

Indexed keywords

GLUCURONOSYLTRANSFERASE 1A1; IRINOTECAN; ANTINEOPLASTIC AGENT; CAMPTOTHECIN; DRUG DERIVATIVE; GLUCURONOSYLTRANSFERASE; UGT1A1 ENZYME;

ASIAN; DIARRHEA; EMBASE; GENE MUTATION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; MEDLINE; META ANALYSIS; NEUTROPENIA; PRIORITY JOURNAL; REVIEW; SYSTEMATIC REVIEW; ENZYMOLOGY; GENETICS; METABOLISM; NEOPLASM;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; ASIAN CONTINENTAL ANCESTRY GROUP; CAMPTOTHECIN; GLUCURONOSYLTRANSFERASE; HUMANS; NEOPLASMS; POLYMORPHISM, GENETIC;

EID: 84896051392     PISSN: 03445704     EISSN: 14320843     Source Type: Journal    
DOI: 10.1007/s00280-014-2382-3     Document Type: Review

References (47)

1. Rothenberg ML, Eckardt JR, Kuhn JG, Burris HA 3rd, Nelson J, Hilsenbeck SG, Rodriguez GI, Thurman AM, Smith LS, Eckhardt SG, Weiss GR, Elfring GL, Rinaldi DA, Schaaf LJ, Von Hoff DD (1996) Phase II trial of irinotecan in patients with progressive or rapidly recurrent colorectal cancer. J Clin Oncol 14(4):1128-1135 (Pubitemid 26105519)
2. Lara PN Jr, Natale R, Crowley J, Lenz HJ, Redman MW, Carleton JE, Jett J, Langer CJ, Kuebler JP, Dakhil SR, Chansky K, Gandara DR (2009) Phase III trial of irinotecan/cisplatin compared with etoposide/cisplatin in extensive-stage small-cell lung cancer: clinical and pharmacogenomic results from SWOG S0124. J Clin Oncol 27(15):2530-2535. doi:10.1200/jco.2008.20.1061
3. Lim WT, Lim ST, Wong NS, Koo WH (2003) CPT-11 and cisplatin in the treatment of advanced gastric cancer in Asians. J Chemother 15(4):400-405
4. Yamamoto K, Kokawa K, Umesaki N, Nishimura R, Hasegawa K, Konishi I, Saji F, Nishida M, Noguchi H, Takizawa K (2009) Phase I study of combination chemotherapy with irinotecan hydrochloride and nedaplatin for cervical squamous cell carcinoma: Japanese gynecologic oncology group study. Oncol Rep 21(4):1005-1009
5. de Forni M, Bugat R, Chabot GG, Culine S, Extra JM, Gouyette A, Madelaine I, Marty ME, Mathieu-Boue A (1994) Phase I and pharmacokinetic study of the camptothecin derivative irinotecan, administered on a weekly schedule in cancer patients. Cancer Res 54(16):4347-4354 (Pubitemid 24273146)
6. Iyer L, King CD, Whitington PF, Green MD, Roy SK, Tephly TR, Coffman BL, Ratain MJ (1998) Genetic predisposition to the metabolism of irinotecan (CPT-11). Role of uridine diphosphate glucuronosyltransferase isoform 1A1 in the glucuronidation of its active metabolite (SN-38) in human liver microsomes. J Clin Investig 101(4):847-854. doi:10.1172/jci915 (Pubitemid 28096082)
7. Toffoli G, Cecchin E, Corona G, Russo A, Buonadonna A, D'Andrea M, Pasetto LM, Pessa S, Errante D, De Pangher V, Giusto M, Medici M, Gaion F, Sandri P, Galligioni E, Bonura S, Boccalon M, Biason P, Frustaci S (2006) The role of UGT1A1*28 polymorphism in the pharmacodynamics and pharmacokinetics of irinotecan in patients with metastatic colorectal cancer. J Clin Oncol 24(19):3061-3068. doi:10.1200/jco.2005.05.5400 (Pubitemid 46638941)
8. Cote JF, Kirzin S, Kramar A, Mosnier JF, Diebold MD, Soubeyran I, Thirouard AS, Selves J, Laurent-Puig P, Ychou M (2007) UGT1A1 polymorphism can predict hematologic toxicity in patients treated with irinotecan. Clin Cancer Res 13(11):3269-3275. doi:10.1158/1078-0432.ccr-06-2290 (Pubitemid 46944912)
9. Rouits E, Charasson V, Petain A, Boisdron-Celle M, Delord JP, Fonck M, Laurand A, Poirier AL, Morel A, Chatelut E, Robert J, Gamelin E (2008) Pharmacokinetic and pharmacogenetic determinants of the activity and toxicity of irinotecan in metastatic colorectal cancer patients. Br J Cancer 99(8):1239-1245. doi:10.1038/sj.bjc.6604673
10. Marcuello E, Altes A, Menoyo A, Del Rio E, Gomez-Pardo M, Baiget M (2004) UGT1A1 gene variations and irinotecan treatment in patients with metastatic colorectal cancer. Br J Cancer 91(4):678-682. doi:10.1038/sj.bjc.6602042 (Pubitemid 39141623)
11. Ando Y, Chida M, Nakayama K, Saka H, Kamataki T (1998) The UGT1A1*28 allele is relatively rare in a Japanese population. Pharmacogenetics 8(4):357-360 (Pubitemid 28372330)
12. Mackenzie PI, Bock KW, Burchell B, Guillemette C, Ikushiro S, Iyanagi T, Miners JO, Owens IS, Nebert DW (2005) Nomenclature update for the mammalian UDP glycosyltransferase (UGT) gene superfamily. Pharmacogenet Genomics 15(10):677-685 (Pubitemid 41345319)
13. Han JY, Lim HS, Shin ES, Yoo YK, Park YH, Lee JE, Jang IJ, Lee DH, Lee JS (2006) Comprehensive analysis of UGT1A polymorphisms predictive for pharmacokinetics and treatment outcome in patients with non-small-cell lung cancer treated with irinotecan and cisplatin. J Clin Oncol 24(15):2237-2244. doi:10.1200/jco.2005.03.0239
14. Gao J, Zhou J, Li Y, Lu M, Jia R, Shen L (2013) UGT1A1 6/28 polymorphisms could predict irinotecan-induced severe neutropenia not diarrhea in Chinese colorectal cancer patients. Med Oncol 30(3):604. doi:10.1007/s12032-013-0604-x
15. Inoue K, Sonobe M, Kawamura Y, Etoh T, Takagi M, Matsumura T, Kikuyama M, Kimura M, Minami S, Utsuki H, Yamazaki T, Suzuki T, Tsuji D, Hayashi H, Itoh K (2013) Polymorphisms of the UDP-glucuronosyl transferase 1A genes are associated with adverse events in cancer patients receiving irinotecan-based chemotherapy. Tohoku J Exp Med 229(2):107-114
16. Choi YH, Kim TW, Kim KP, Lee SS, Hong YS, Ryu MH, Lee JL, Chang HM, Ryoo BY, Kim HS, Shin JG, Kang YK (2012) A phase II study of clinical outcomes of 3-week cycles of irinotecan and S-1 in patients with previously untreated metastatic colorectal cancer: influence of the UGT1A1 and CYP2A6 polymorphisms on clinical activity. Oncology 82(5):290-297. doi:10.1159/000337989
17. Nakamura Y, Soda H, Oka M, Kinoshita A, Fukuda M, Fukuda M, Takatani H, Nagashima S, Soejima Y, Kasai T, Nakatomi K, Masuda N, Tsukamoto K, Kohno S (2011) Randomized phase II trial of irinotecan with paclitaxel or gemcitabine for non-small cell lung cancer: association of UGT1A1*6 and UGT1A1*27 with severe neutropenia. J Thorac Oncol 6(1):121-127. doi:10.1097/JTO.0b013e318200e4e8
18. Okuyama Y, Hazama S, Nozawa H, Kobayashi M, Takahashi K, Fujikawa K, Kato T, Nagata N, Kimura H, Oba K, Sakamoto J, Mishima H (2011) Prospective phase II study of FOLFIRI for mCRC in Japan, including the analysis of UGT1A1 28/6 polymorphisms. Jpn J Clin Oncol 41(4):477-482. doi:10.1093/jjco/hyr001
19. Seo BG, Kwon HC, Oh SY, Lee S, Kim SG, Kim SH, Han H, Kim HJ (2009) Comprehensive analysis of excision repair complementation group 1, glutathione S-transferase, thymidylate synthase and uridine diphosphate glucuronosyl transferase 1A1 polymorphisms predictive for treatment outcome in patients with advanced gastric cancer treated with FOLFOX or FOLFIRI. Oncol Rep 22(1):127-136
20. Takano M, Kato M, Yoshikawa T, Sasaki N, Hirata J, Furuya K, Takahashi M, Yokota H, Kino N, Horie K, Goto T, Fujiwara K, Ishii K, Kikuchi Y, Kita T (2009) Clinical significance of UDP-glucuronosyltransferase 1A1*6 for toxicities of combination chemotherapy with irinotecan and cisplatin in gynecologic cancers: a prospective multi-institutional study. Oncology 76(5):315-321. doi:10.1159/000209335
21. Jada SR, Lim R, Wong CI, Shu X, Lee SC, Zhou Q, Goh BC, Chowbay B (2007) Role of UGT1A1*6, UGT1A1*28 and ABCG2 c.421C> A polymorphisms in irinotecan-induced neutropenia in Asian cancer patients. Cancer Sci 98(9):1461-1467. doi:10.1111/j.1349-7006.2007.00541.x (Pubitemid 47241771)
22. Onoue M, Terada T, Kobayashi M, Katsura T, Matsumoto S, Yanagihara K, Nishimura T, Kanai M, Teramukai S, Shimizu A, Fukushima M, Inui K (2009) UGT1A1*6 polymorphism is most predictive of severe neutropenia induced by irinotecan in Japanese cancer patients. Int J Clin Oncol 14(2):136-142. doi:10.1007/s10147-008-0821-z
23. Satoh T, Ura T, Yamada Y, Yamazaki K, Tsujinaka T, Munakata M, Nishina T, Okamura S, Esaki T, Sasaki Y, Koizumi W, Kakeji Y, Ishizuka N, Hyodo I, Sakata Y (2011) Genotype-directed, dose-finding study of irinotecan in cancer patients with UGT1A1*28 and/or UGT1A1*6 polymorphisms. Cancer Sci 102(10):1868-1873. doi:10.1111/j.1349-7006.2011.02030.x
24. Takahara N, Nakai Y, Isayama H, Sasaki T, Satoh Y, Takai D, Hamada T, Uchino R, Mizuno S, Miyabayashi K, Mohri D, Kawakubo K, Kogure H, Yamamoto N, Sasahira N, Hirano K, Ijichi H, Tada M, Yatomi Y, Koike K (2013) Uridine diphosphate glucuronosyl transferase 1 family polypeptide A1 gene (UGT1A1) polymorphisms are associated with toxicity and efficacy in irinotecan monotherapy for refractory pancreatic cancer. Cancer Chemother Pharmacol 71(1):85-92. doi:10.1007/s00280-012-1981-0
25. Wang Y, Shen L, Xu N, Wang JW, Jiao SC, Liu ZY, Xu JM (2012) UGT1A1 predicts outcome in colorectal cancer treated with irinotecan and fluorouracil. World J Gastroenterol (WJG) 18(45):6635-6644. doi:10.3748/wjg.v18.i45.6635
26. Sunakawa Y, Ichikawa W, Fujita K, Nagashima F, Ishida H, Yamashita K, Mizuno K, Miwa K, Kawara K, Akiyama Y, Araki K, Yamamoto W, Miya T, Narabayashi M, Ando Y, Hirose T, Saji S, Sasaki Y (2011) UGT1A1*1/*28 and *1/*6 genotypes have no effects on the efficacy and toxicity of FOLFIRI in Japanese patients with advanced colorectal cancer. Cancer Chemother Pharmacol 68(2):279-284. doi:10.1007/s00280-010-1485-8
27. Ando Y, Saka H, Ando M, Sawa T, Muro K, Ueoka H, Yokoyama A, Saitoh S, Shimokata K, Hasegawa Y (2000) Polymorphisms of UDP-glucuronosyltransferase gene and irinotecan toxicity: a pharmacogenetic analysis. Cancer Res 60(24):6921-6926 (Pubitemid 32059164)
28. Sai K, Saito Y, Sakamoto H, Shirao K, Kurose K, Saeki M, Ozawa S, Kaniwa N, Hirohashi S, Saijo N, Sawada J, Yoshida T (2008) Importance of UDP-glucuronosyltransferase 1A1*6 for irinotecan toxicities in Japanese cancer patients. Cancer Lett 261(2):165-171. doi:10.1016/j.canlet.2007.11.009
29. Akie K, Oizumi S, Ogura S, Shinagawa N, Kikuchi E, Fukumoto S, Harada M, Kinoshita I, Kojima T, Harada T, Fujita Y, Ohsaki Y, Dosaka-Akita H, Isobe H, Nishimura M (2011) Phase II study of irinotecan plus S-1 combination for previously untreated advanced non-small cell lung cancer: Hokkaido Lung Cancer Clinical Study Group Trial (HOT) 0601. Oncology 81(2):84-90. doi:10.1159/000331681
30. Gao J, Zhou J, Li Y, Peng Z, Li Y, Wang X, Shen L (2013) Associations between UGT1A1*6/*28 polymorphisms and irinotecan-induced severe toxicity in Chinese gastric or esophageal cancer patients. Med Oncol 30(3):630. doi:10.1007/s12032-013-0630-8
31. Ando Y, Ueoka H, Sugiyama T, Ichiki M, Shimokata K, Hasegawa Y (2002) Polymorphisms of UDP-glucuronosyltransferase and pharmacokinetics of irinotecan. Ther Drug Monit 24(1):111-116 (Pubitemid 34106739)
32. Moher D (2010) Corrigendum to: preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement International Journal of Surgery 8:336-341. Int J Surg. doi:10.1016/j.ijsu.2010.07.299
33. Mantel N, Haenszel W (1959) Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 22(4):719-748
34. Zintzaras E, Ioannidis JP (2005) Heterogeneity testing in meta-analysis of genome searches. Genet Epidemiol 28(2):123-137. doi:10.1002/gepi.20048
35. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629-634 (Pubitemid 27387172)
36. Duval S, Tweedie R (2000) A nonparametric "Trim and Fill" method of accounting for publication bias in meta-analysis. Biometrics 56(2):455-463 (Pubitemid 30422636)
37. Jorgensen AL, Williamson PR (2008) Methodological quality of pharmacogenetic studies: issues of concern. Stat Med 27(30):6547-6569. doi:10.1002/sim.3420
38. Liu X, Cheng D, Kuang Q, Liu G, Xu W (2013) Association of UGT1A1*28 polymorphisms with irinotecan-induced toxicities in colorectal cancer: a meta-analysis in Caucasians. Pharmacogenomics J. doi:10.1038/tpj.2013. 10
39. Balram C, Sabapathy K, Fei G, Khoo KS, Lee EJ (2002) Genetic polymorphisms of UDP-glucuronosyltransferase in Asians: UGT1A1*28 is a common allele in Indians. Pharmacogenetics 12(1):81-83 (Pubitemid 34112247)
40. Gagne JF, Montminy V, Belanger P, Journault K, Gaucher G, Guillemette C (2002) Common human UGT1A polymorphisms and the altered metabolism of irinotecan active metabolite 7-ethyl-10-hydroxycamptothecin (SN-38). Mol Pharmacol 62(3):608-617 (Pubitemid 36329379)
41. Jinno H, Tanaka-Kagawa T, Hanioka N, Saeki M, Ishida S, Nishimura T, Ando M, Saito Y, Ozawa S, Sawada J (2003) Glucuronidation of 7-ethyl-10- hydroxycamptothecin (SN-38), an active metabolite of irinotecan (CPT-11), by human UGT1A1 variants, G71R, P229Q, and Y486D. Drug Metab Dispos 31(1):108-113 (Pubitemid 36735264)
42. Hu ZY, Yu Q, Pei Q, Guo C (2010) Dose-dependent association between UGT1A1*28 genotype and irinotecan-induced neutropenia: low doses also increase risk. Clin Cancer Res 16(15):3832-3842. doi:10.1158/1078-0432.ccr-10- 1122
43. Cortejoso L, Garcia MI, Garcia-Alfonso P, Gonzalez-Haba E, Escolar F, Sanjurjo M, Lopez-Fernandez LA (2013) Differential toxicity biomarkers for irinotecan- and oxaliplatin-containing chemotherapy in colorectal cancer. Cancer Chemother Pharmacol 71(6):1463-1472. doi:10.1007/s00280-013-2145-6
44. Fukushima M, Sakamoto K, Ohshimo H, Nakagawa F, Taguchi T (2010) Irinotecan overcomes the resistance to 5-fluorouracil in human colon cancer xenografts by down-regulation of intratumoral thymidylate synthase. Oncol Rep 24(4):835-842
45. Ide H, Kikuchi E, Hasegawa M, Hattori S, Yasumizu Y, Miyajima A, Oya M (2013) Therapeutic enhancement of S-1 with CPT-11 through down-regulation of thymidylate synthase in bladder cancer. Cancer medicine 2(4):488-495. doi:10.1002/cam4.95
46. Raida M, Schwabe W, Hausler P, Van Kuilenburg AB, Van Gennip AH, Behnke D, Hoffken K (2001) Prevalence of a common point mutation in the dihydropyrimidine dehydrogenase (DPD) gene within the 5′-splice donor site of intron 14 in patients with severe 5-fluorouracil (5-FU)-related toxicity compared with controls. Clin Cancer Res 7(9):2832-2839 (Pubitemid 32911393)
47. Hu ZY, Yu Q, Zhao YS (2010) Dose-dependent association between UGT1A1*28 polymorphism and irinotecan-induced diarrhoea: a meta-analysis. Eur J Cancer 46(10):1856-1865. doi:10.1016/j.ejca.2010.02.049