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Associations between genetic polymorphisms of membrane transporter genes and prognosis after chemotherapy: meta-analysis and finding from Seoul Breast Cancer Study (SEBCS)

The Pharmacogenomics Journal volume 18, pages 633–645 (2018)Cite this article

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Abstract

Membrane transporters can be major determinants of the pharmacokinetic profiles of anticancer drugs. The associations between genetic variations of ATP-binding cassette (ABC) and solute carrier (SLC) genes and cancer survival were investigated through a meta-analysis and an association study in the Seoul Breast Cancer Study (SEBCS). Including the SEBCS, the meta-analysis was conducted among 38 studies of genetic variations of transporters on various cancer survivors. The population of SEBCS consisted of 1338 breast cancer patients who had been treated with adjuvant chemotherapy. A total of 7750 SNPs were selected from 453 ABC and/or SLC genes typed by an Affymetrix 6.0 chip. ABCB1 rs1045642 was associated with poor progression-free survival in a meta-analysis (HR = 1.33, 95% CI: 1.07–1.64). ABCB1, SLC8A1, and SLC12A8 were associated with breast cancer survival in SEBCS (Pgene < 0.05). ABCB1 rs1202172 was differentially associated with survival depending on the chemotherapy (Pinteraction = 0.035). Our finding provides suggestive associations of membrane transporters on cancer survival.

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References

  1. Youlden DR, Cramb SM, Yip CH, Baade PD. Incidence and mortality of female breast cancer in the Asia-Pacific region. Cancer Biol Med. 2014;11:101–15.

    PubMed  PubMed Central  Google Scholar 

  2. Oh CM, Won YJ, Jung KW, Kong HJ, Cho H, Lee JK, et al. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2013. Cancer Res Treat. 2016;48:436–50.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Stearns V, Davidson NE, Flockhart DA. Pharmacogenetics in the treatment of breast cancer. Pharmacogenomics J. 2004;4:143–53.

    Article  CAS  PubMed  Google Scholar 

  4. Chen G, Quan S, Hu Q, Wang L, Xia X, Wu J. Lack of association between MDR1 C3435T polymorphism and chemotherapy response in advanced breast cancer patients: evidence from current studies. Mol Biol Rep. 2012;39:5161–8.

    Article  CAS  PubMed  Google Scholar 

  5. Berry DA, Cronin KA, Plevritis SK, Fryback DG, Clarke L, Zelen M, et al. Effect of screening and adjuvant therapy on mortality from breast cancer. N Engl J Med. 2005;353:1784–92.

    Article  CAS  PubMed  Google Scholar 

  6. Han SM, Park J, Lee JH, Lee SS, Kim H, Han H, et al. Targeted Next-Generation Sequencing for Comprehensive Genetic Profiling of Pharmacogenes. Clin Pharmacol Ther. 2017;101:396–405.

    Article  CAS  PubMed  Google Scholar 

  7. Daly AK. Genome-wide association studies in pharmacogenomics. Nat Rev Genet. 2010;11:241–6.

    Article  CAS  PubMed  Google Scholar 

  8. Wang L, Weinshilboum RM. Pharmacogenomics: candidate gene identification, functional validation and mechanisms. Hum Mol Genet. 2008;17(R2):R174–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Motsinger-Reif AA, Jorgenson E, Relling MV, Kroetz DL, Weinshilboum R, Cox NJ, et al. Genome-wide association studies in pharmacogenomics: successes and lessons. Pharmacogenet Genomics. 2013;23:383–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Song N, Choi JY, Sung H, Jeon S, Chung S, Park SK, et al. Prediction of breast cancer survival using clinical and genetic markers by tumor subtypes. PLoS ONE. 2015;10:e0122413.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Vasiliou V, Vasiliou K, Nebert DW. Human ATP-binding cassette (ABC) transporter family. Hum Genomics. 2009;3:281–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Lin L, Yee SW, Kim RB, Giacomini KM. SLC transporters as therapeutic targets: emerging opportunities. Nat Rev Drug Discov. 2015;14:543–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. He L, Vasiliou K, Nebert DW. Analysis and update of the human solute carrier (SLC) gene superfamily. Hum Genomics. 2009;3:195–206.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer. 2002;2:48–58.

    Article  CAS  PubMed  Google Scholar 

  15. Kap EJ, Seibold P, Scherer D, Habermann N, Balavarca Y, Jansen L, et al. SNPs in transporter and metabolizing genes as predictive markers for oxaliplatin treatment in colorectal cancer patients. Int J Cancer. 2016;138:2993–3001. 10.1002/ijc.30026. Epub 2016 Feb 19.

    Article  CAS  PubMed  Google Scholar 

  16. Wu H, Kang H, Liu Y, Xiao Q, Zhang Y, Sun M, et al. Association of ABCB1 genetic polymorphisms with susceptibility to colorectal cancer and therapeutic prognosis. Pharmacogenomics. 2013;14:897–911.

    Article  CAS  PubMed  Google Scholar 

  17. Campa D, Muller P, Edler L, Knoefel L, Barale R, Heussel CP, et al. A comprehensive study of polymorphisms in ABCB1, ABCC2 and ABCG2 and lung cancer chemotherapy response and prognosis. Int J Cancer. 2012;131:2920–8.

    Article  CAS  PubMed  Google Scholar 

  18. Cuffe S, Azad AK, Qiu X, Qiu X, Brhane Y, Kuang Q, et al. ABCC2 polymorphisms and survival in the Princess Margaret cohort study and the NCIC clinical trials group BR.24 trial of platinum-treated advanced stage non-small cell lung cancer patients. Cancer Epidemiol. 2016;41:50–6. 10.1016/j.canep.2015.12.012. Epub 6 Jan 24.

    Article  PubMed  Google Scholar 

  19. Shitara K, Matsuo K, Ito S, Sawaki A, Kawai H, Yokota T, et al. Effects of genetic polymorphisms in the ABCB1 gene on clinical outcomes in patients with gastric cancer treated by second-line chemotherapy. Asian Pac J Cancer Prev. 2010;11:447–52.

    PubMed  Google Scholar 

  20. Kogan AJ, Haren M. Translating cancer trial endpoints into the language of managed care. Biotechnol Healthc. 2008;5:22–35.

    PubMed  PubMed Central  Google Scholar 

  21. Woo HI, Kim KK, Choi H, Kim S, Jang KT, Yi JH, et al. Effect of genetic polymorphisms on therapeutic response and clinical outcomes in pancreatic cancer patients treated with gemcitabine. Pharmacogenomics. 2012;13:1023–35. https://doi.org/10.2217/pgs.12.82

    Article  CAS  PubMed  Google Scholar 

  22. Chung S, Park SK, Sung H, Song N, Han W, Noh DY, et al. Association between chronological change of reproductive factors and breast cancer risk defined by hormone receptor status: results from the Seoul Breast Cancer Study. Breast Cancer Res Treat. 2013;140:557–65.

    Article  CAS  PubMed  Google Scholar 

  23. Kim HC, Lee JY, Sung H, Choi JY, Park SK, Lee KM, et al. A genome-wide association study identifies a breast cancer risk variant in ERBB4 at 2q34: results from the Seoul Breast Cancer Study. Breast Cancer Res. 2012;14:R56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Yu K, Li Q, Bergen AW, Pfeiffer RM, Rosenberg PS, Caporaso N, et al. Pathway analysis by adaptive combination of P-values. Genet Epidemiol. 2009;33:700–9.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Zhang HWB, Yu K, Yang Y ARTP2: Pathway and Gene-Level Association Test. https://cran.r-project.org/web/packages/ARTP2/index.html2016

  26. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics. 2005;21:263–5.

    Article  CAS  PubMed  Google Scholar 

  27. Stephens M, Smith NJ, Donnelly P. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet. 2001;68:978–89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Fukudo M, Ikemi Y, Togashi Y, Masago K, Kim YH, Mio T, et al. Population pharmacokinetics/pharmacodynamics of erlotinib and pharmacogenomic analysis of plasma and cerebrospinal fluid drug concentrations in Japanese patients with non-small cell lung cancer. Clin Pharmacokinet. 2013;52:593–609. https://doi.org/10.1007/s40262-013-0058-5

    Article  CAS  PubMed  Google Scholar 

  29. Gandara DR, Kawaguchi T, Crowley J, Moon J, Furuse K, Kawahara M, et al. Japanese-US common-arm analysis of paclitaxel plus carboplatin in advanced non-small-cell lung cancer: A model for assessing population-related pharmacogenomics. J Clin Oncol. 2009;27:3540–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Knez L, Kosnik M, Ovcaricek T, Sadikov A, Sodja E, Kern I, et al. Predictive value of ABCB1 polymorphisms G2677T/A, C3435T, and their haplotype in small cell lung cancer patients treated with chemotherapy. J Cancer Res Clin Oncol. 2012;138:1551–60. 10.007/s00432-012-1231-1. Epub 2012 Apr 29.

    Article  CAS  PubMed  Google Scholar 

  31. Tian C, Ambrosone CB, Darcy KM, Krivak TC, Armstrong DK, Bookman MA, et al. Common variants in ABCB1, ABCC2 and ABCG2 genes and clinical outcomes among women with advanced stage ovarian cancer treated with platinum and taxane-based chemotherapy: a Gynecologic Oncology Group study. Gynecol Oncol. 2012;124:575–81. 10.1016/j.ygyno.2011.11.022. Epub Nov 21.

    Article  CAS  PubMed  Google Scholar 

  32. Chang H, Rha SY, Jeung HC, Im CK, Noh SH, Kim JJ, et al. Association of the ABCB1 3435C>T polymorphism and treatment outcomes in advanced gastric cancer patients treated with paclitaxel-based chemotherapy. Oncol Rep. 2010;23:271–8.

    CAS  PubMed  Google Scholar 

  33. Li Y, Yan PW, Huang XE, Li CG. MDR1 gene C3435T polymorphism is associated with clinical outcomes in gastric cancer patients treated with postoperative adjuvant chemotherapy. Asian Pac J Cancer Prev. 2011;12:2405–9.

    PubMed  Google Scholar 

  34. Ameyaw MM, Regateiro F, Li T, Liu X, Tariq M, Mobarek A, et al. MDR1 pharmacogenetics: frequency of the C3435T mutation in exon 26 is significantly influenced by ethnicity. Pharmacogenetics. 2001;11:217–21.

    Article  CAS  PubMed  Google Scholar 

  35. Johnatty SE, Beesley J, Paul J, Fereday S, Spurdle AB, M.webb P, et al. ABCB1 (MDR 1) polymorphisms and progression-free survival among women with ovarian cancer following paclitaxel/carboplatin chemotherapy. Clin Cancer Res. 2008;14:5594–601.

    Article  CAS  PubMed  Google Scholar 

  36. Huang L, Zhang T, Xie C, Liao X, Yu Q, Feng J, et al. SLCO1B1 and SLC19A1 gene variants and irinotecan-induced rapid response and survival: a prospective multicenter pharmacogenetics study of metastatic colorectal cancer. PLoS ONE. 2013;8:e77223.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Ulrich CM, Rankin C, Toriola AT, Makar KW, Altug-Teber O, Benedetti JK, et al. Polymorphisms in folate-metabolizing enzymes and response to 5-fluorouracil among patients with stage II or III rectal cancer (INT-0144; SWOG 9304). Cancer. 2014;120:3329–37. 10.1002/cncr.28830.

    Article  CAS  PubMed  Google Scholar 

  38. Corrigan A, Walker JL, Wickramasinghe S, Hernandez MA, Newhouse SJ, Folarin AA, et al. Pharmacogenetics of pemetrexed combination therapy in lung cancer: pathway analysis reveals novel toxicity associations. Pharm J. 2014;14:411–7. 10.1038/tpj.2014.13.

    CAS  Google Scholar 

  39. Li L, Schaid DJ, Fridley BL, Kalari KR, Jenkins GD, Abo RP, et al. Gemcitabine metabolic pathway genetic polymorphisms and response in patients with non-small cell lung cancer. Pharm Genom. 2012;22:105–16. https://doi.org/10.1097/FPC.0b013e32834dd7e2

    Article  CAS  Google Scholar 

  40. Wu F, Zhang J, Hu N, Wang H, Xu T, Liu Y, et al. Effect of hENT1 polymorphism G-706C on clinical outcomes of gemcitabine-containing chemotherapy for Chinese non-small-cell lung cancer patients. Cancer Epidemiol. 2014;38:728–32. 10.1016/j.canep.2014.08.008.

    Article  PubMed  Google Scholar 

  41. Zeng H, Yu H, Lu L, Jain D, Kidd MS, Saif MW, et al. Genetic effects and modifiers of radiotherapy and chemotherapy on survival in pancreatic cancer. Pancreas. 2011;40:657–63. https://doi.org/10.1097/MPA.0b013e31821268d1

    Article  PubMed  PubMed Central  Google Scholar 

  42. Paik H, Lee E, Park I, Kim J, Lee D. Prediction of cancer prognosis with the genetic basis of transcriptional variations. Genomics. 2011;97:350–7.

    Article  CAS  PubMed  Google Scholar 

  43. Hlavac V, Brynychova V, Vaclavikova R, Ehrlichova M, Vrana D, Pecha V, et al. The expression profile of ATP-binding cassette transporter genes in breast carcinoma. Pharmacogenomics. 2013;14:515–29.

    Article  CAS  PubMed  Google Scholar 

  44. Ween MP, Armstrong MA, Oehler MK, Ricciardelli C. The role of ABC transporters in ovarian cancer progression and chemoresistance. Crit Rev Oncol Hematol. 2015;96:220–56.

    Article  CAS  PubMed  Google Scholar 

  45. Coelho D, Kim JC, Miousse IR, Fung S, du Moulin M, Buers I, et al. Mutations in ABCD4 cause a new inborn error of vitamin B12 metabolism. Nat Genet. 2012;44:1152–5.

    Article  CAS  PubMed  Google Scholar 

  46. Kawaguchi K, Okamoto T, Morita M, Imanaka T. Translocation of the ABC transporter ABCD4 from the endoplasmic reticulum to lysosomes requires the escort protein LMBD1. Sci Rep. 2016;6:30183.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Choi SW. Vitamin B12 deficiency: a new risk factor for breast cancer? Nutr Rev. 1999;57:250–3.

    CAS  PubMed  Google Scholar 

  48. Janvilisri T, Venter H, Shahi S, Reuter G, Balakrishnan L, van Veen HW. Sterol transport by the human breast cancer resistance protein (ABCG2) expressed in Lactococcus lactis. J Biol Chem. 2003;278:20645–51.

    Article  CAS  PubMed  Google Scholar 

  49. Yu L, von Bergmann K, Lutjohann D, Hobbs HH, Cohen JC. Selective sterol accumulation in ABCG5/ABCG8-deficient mice. J Lipid Res. 2004;45:301–7.

    Article  CAS  PubMed  Google Scholar 

  50. Lytton J. Na+/Ca2+exchangers: three mammalian gene families control Ca2+transport. Biochem J. 2007;406:365–82.

    Article  CAS  PubMed  Google Scholar 

  51. Munoz JJ, Drigo SA, Barros-Filho MC, Marchi FA, Scapulatempo-Neto C, Pessoa GS, et al. Down-regulation of SLC8A1 as a putative apoptosis evasion mechanism by modulation of calcium levels in penile carcinoma. J Urol. 2015;194:245–51.

    Article  CAS  PubMed  Google Scholar 

  52. Januchowski R, Zawierucha P, Rucinski M, Andrzejewska M, Wojtowicz K, Nowicki M, et al. Drug transporter expression profiling in chemoresistant variants of the A2780 ovarian cancer cell line. Biomed Pharmacother. 2014;68:447–53.

    Article  CAS  PubMed  Google Scholar 

  53. Daigle ND, Carpentier GA, Frenette-Cotton R, Simard MG, Lefoll MH, Noel M, et al. Molecular characterization of a human cation-Cl- cotransporter (SLC12A8A, CCC9A) that promotes polyamine and amino acid transport. J Cell Physiol. 2009;220:680–9.

    Article  CAS  PubMed  Google Scholar 

  54. Gagnon KB, Delpire E. Physiology of SLC12 transporters: lessons from inherited human genetic mutations and genetically engineered mouse knockouts. Am J Physiol Cell Physiol. 2013;304:C693–714.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Minois N, Carmona-Gutierrez D, Madeo F. Polyamines in aging and disease. Aging. 2011;3:716–32.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Hahm HA, Dunn VR, Butash KA, Deveraux WL, Woster PM, Casero RA Jr., et al. Combination of standard cytotoxic agents with polyamine analogues in the treatment of breast cancer cell lines. Clin Cancer Res. 2001;7:391–9.

    CAS  PubMed  Google Scholar 

  57. Sun W, Wu RR, van Poelje PD, Erion MD. Isolation of a family of organic anion transporters from human liver and kidney. Biochem Biophys Res Commun. 2001;283:417–22.

    Article  CAS  PubMed  Google Scholar 

  58. Gligorov J, Lotz JP. Preclinical pharmacology of the taxanes: implications of the differences. Oncologist. 2004;9(Suppl 2):3–8.

    Article  CAS  PubMed  Google Scholar 

  59. Bray J, Sludden J, Griffin MJ, Cole M, Verrill M, Jamieson D, et al. Influence of pharmacogenetics on response and toxicity in breast cancer patients treated with doxorubicin and cyclophosphamide. Br J Cancer. 2010;102:1003–9. 10.38/sj.bjc.6605587.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Ji M, Tang J, Zhao J, Xu B, Qin J, Lu J. Polymorphisms in genes involved in drug detoxification and clinical outcomes of anthracycline-based neoadjuvant chemotherapy in Chinese Han breast cancer patients. Cancer Biol Ther. 2012;13:264–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Lee SY, Im SA, Park YH, Woo SY, Kim S, Choi MK, et al. Genetic polymorphisms of SLC28A3, SLC29A1 and RRM1 predict clinical outcome in patients with metastatic breast cancer receiving gemcitabine plus paclitaxel chemotherapy. Eur J Cancer. 2014;50:698–705.

    Article  CAS  PubMed  Google Scholar 

  62. Kim HJ, Im SA, Keam B, Ham HS, Lee KH, Kim TY, et al. ABCB1 polymorphism as prognostic factor in breast cancer patients treated with docetaxel and doxorubicin neoadjuvant chemotherapy. Cancer Sci. 2015;106:86–93.

    Article  CAS  PubMed  Google Scholar 

  63. Yue AM, Xie ZB, Zhao HF, Guo SP, Shen YH, Wang HP. Associations of ABCB1 and XPC genetic polymorphisms with susceptibility to colorectal cancer and therapeutic prognosis in a Chinese population. Asian Pac J Cancer Prev. 2013;14:3085–91.

    Article  PubMed  Google Scholar 

  64. Chen X, Chen D, Yang S, Ma R, Pan Y, Li X, et al. Impact of ABCG2 polymorphisms on the clinical outcome of TKIs therapy in Chinese advanced non-small-cell lung cancer patients. Cancer Cell Int. 2015;15:43. 10.1186/s12935-015-0191-3.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Dogu GG, Kargi A, Turgut S, Ayada C, Taskoylu BY, Demiray G, et al. MDR1 single nucleotide polymorphism C3435T in Turkish patients with non-small-cell lung cancer. Gene. 2012;506:404–7. 10.1016/j.gene.2012.06.057.

    Article  CAS  PubMed  Google Scholar 

  66. Lee Y, Yoon KA, Joo J, Lee D, Bae K, Han JY, et al. Prognostic implications of genetic variants in advanced non-small cell lung cancer: A genome-wide association study. Carcinogenesis. 2013;34:307–13.

    Article  CAS  PubMed  Google Scholar 

  67. Moyer AM, Sun Z, Batzler AJ, Li A, Schaid DJ, Yang P, et al. Glutathione pathway genetic polymorphisms and lung cancer survival after platinum-based chemotherapy. Cancer Epidemiol Biomark Prev. 2010;19:811–21.

    Article  CAS  Google Scholar 

  68. Müller PJ, Dally H, Klappenecker CN, Edler L, Jäger B, Gerst M, et al. Polymorphisms in ABCG2, ABCC3 and CNT1 genes and their possible impact on chemotherapy outcome of lung cancer patients. Int J Cancer. 2009;124:1669–74.

    Article  PubMed  Google Scholar 

  69. Soo RA, Wang LZ, Ng SS, Chong PY, Yong WP, Lee SC, et al. Distribution of gemcitabine pathway genotypes in ethnic Asians and their association with outcome in non-small cell lung cancer patients. Lung Cancer. 2009;63:121–7. 10.1016/j.lungcan.2008.04.010.

    Article  PubMed  Google Scholar 

  70. Szczyrek M, Mlak R, Krawczyk P, Wojas-Krawczyk K, Powrozek T, Szudy-Szczyrek A, et al. Polymorphisms of genes encoding multidrug resistance proteins as a predictive factor for second-line docetaxel therapy in advanced non-small cell lung cancer. Pathol Oncol Res. 2016;17:17.

    Google Scholar 

  71. Qiao R, Wu W, Lu D, Han B. Influence of single nucleotide polymorphisms in ABCB1, ABCG2 and ABCC2 on clinical outcomes to paclitaxel-platinum chemotherapy in patients with non-small-cell lung cancer. International. J Clin Exp Med. 2016;9:298–307.

    CAS  Google Scholar 

  72. Bergmann TK, Gréen H, Brasch-Andersen C, Mirza MR, Herrstedt J, Hølund B, et al. Retrospective study of the impact of pharmacogenetic variants on paclitaxel toxicity and survival in patients with ovarian cancer. Eur J Clin Pharmacol. 2011;67:693–700.

    Article  CAS  PubMed  Google Scholar 

  73. Peethambaram P, Fridley BL, Vierkant RA, Larson MC, Kalli KR, Elliott EA, et al. Polymorphisms in ABCB1 and ERCC2 associated with ovarian cancer outcome. Int J Mol Epidemiol Genet. 2011;2:185–95.

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Tanaka M, Okazaki T, Suzuki H, Abbruzzese JL, Li D. Association of multi-drug resistance gene polymorphisms with pancreatic cancer outcome. Cancer . 2011;117:744–51. 10.1002/cncr.25510.

    Article  CAS  PubMed  Google Scholar 

  75. Li Z, Xing X, Shan F, Li S, Li Z, Xiao A, et al. ABCC2-24C>T polymorphism is associated with the response to platinum/5-Fu-based neoadjuvant chemotherapy and better clinical outcomes in advanced gastric cancer patients. Oncotarget. 2016;7:55449–57. 10.18632/oncotarget.0961.

    PubMed  PubMed Central  Google Scholar 

  76. Shim HJ, Yun JY, Hwang JE, Bae WK, Cho SH, Lee JH, et al. BRCA1 and XRCC1 polymorphisms associated with survival in advanced gastric cancer treated with taxane and cisplatin. Cancer Sci. 2010;101:1247–54. 10.111/j.349-7006.2010.01514.x.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by grant 0320150110 (2015-1126) from the Seoul National University Hospital Research Fund and Seoul National University Hospital (2017).

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Authors and Affiliations

  1. Department of Biomedical Sciences, Seoul National University Graduate School, Seoul, Korea

    Ji-Eun Kim, Jaesung Choi, JooYong Park, Chulbum Park, Sue K. Park, Daehee Kang & Ji-Yeob Choi

  2. College of Pharmacy Chonnam National University, Gwangju, Korea

    Se Mi Lee

  3. College of Pharmacy, Duksung Women’s university, Seoul, Korea

    Seong Eun Park

  4. Cancer Research Institute, Seoul National University, Seoul, Korea

    Nan Song, Wonshik Han, Sue K. Park, Dong-Young Noh, Daehee Kang & Ji-Yeob Choi

  5. Division for New Health Technology Assessment, National Evidence-based Healthcare Collaborating Agency, Seoul, Korea

    Seokang Chung

  6. Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, USA

    Hyuna Sung

  7. Department of Surgery, Seoul National University College of Medicine, Seoul, Korea

    Wonshik Han & Dong-Young Noh

  8. Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea

    Jong Won Lee

  9. Department of Preventive Medicine, Seoul National University College of Medicine, Seoul, Korea

    Sue K. Park, Keun-Young Yoo, Daehee Kang & Ji-Yeob Choi

  10. Division of Cancer Epidemiology and Management, National Cancer Center, Goyang, Korea

    Mi Kyung Kim

  11. The Armed Forces Capital Hospital, Seongnam, Korea

    Keun-Young Yoo

  12. Institute of Environmental Medicine, Seoul National University Medical Research Center, Seoul, Korea

    Daehee Kang

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Kim, JE., Choi, J., Park, J. et al. Associations between genetic polymorphisms of membrane transporter genes and prognosis after chemotherapy: meta-analysis and finding from Seoul Breast Cancer Study (SEBCS). Pharmacogenomics J 18, 633–645 (2018). https://doi.org/10.1038/s41397-018-0016-6

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