Efflux transporter variants as predictors of drug toxicity in lung cancer patients: systematic review and meta-analysis

References

• 1 IARC. Latest world cancer statistics global cancer burden rises to 14.1 million new cases in 2012: marked increase in breast and cervix cancers must be addressed (2012).
  Google Scholar
• 2 Li S, Huang H, Liao H et al. Phase I clinical trial of the novel platin complex dicycloplatin: clinical and pharmacokinetic results. Int. J. Clin. Pharmacol. Ther. 51(2), 96–105 (2013).
  Medline CASGoogle Scholar
• 3 Jiang J, Liang X, Zhou X, Huang R, Chu Z, Zhan Q. Paclitaxel plus platinum or gemcitabine plus platinum in first-line treatment of advanced non-small-cell lung cancer: results from 6 randomized controlled trials. Int. J. Clin. Oncol. 18(6), 1005–1013 (2013).
  Medline CASGoogle Scholar
• 4 Zukin M, Barrios CH, Pereira JR et al. Randomized Phase III trial of single-agent pemetrexed versus carboplatin and pemetrexed in patients with advanced non-small-cell lung cancer and Eastern Cooperative Oncology Group performance status of 2. J. Clin. Oncol. 31(23), 2849–2853 (2013).
  Medline CASGoogle Scholar
• 5 Go RS, Adjei AA. Review of the comparative pharmacology and clinical activity of cisplatin and carboplatin. J. Clin. Oncol. 17(1), 409–422 (1999).
  Medline CASGoogle Scholar
• 6 Sun L, Ma JT, Zhang SL, Zou HW, Han CB. Efficacy and safety of chemotherapy or tyrosine kinase inhibitors combined with bevacizumab versus chemotherapy or tyrosine kinase inhibitors alone in the treatment of non-small cell lung cancer: a systematic review and meta-analysis. Med. Oncol. 32(2), 473 (2015).
  MedlineGoogle Scholar
• 7 Bartholomä MD, Vortherms AR, Hillier S et al. Synthesis, cytotoxicity, and insight into the mode of action of Re(CO)3 thymidine complexes. ChemMedChem 5(9), 1513–1529 (2010).
  MedlineGoogle Scholar
• 8 Garon EB, Ciuleanu TE, Arrieta O et al. Ramucirumab plus docetaxel versus placebo plus docetaxel for second-line treatment of stage IV non-small-cell lung cancer after disease progression on platinum-based therapy (REVEL): a multicentre, double-blind, randomised Phase 3 trial. Lancet 384(9944), 665–673 (2014).
  Medline CASGoogle Scholar
• 9 Provencio M, De Las Peñas R, Camps C et al. Cisplatin plus vinorelbine as first-line treatment for advanced non-small-cell lung cancer: is a hemogram on day 8 essential? Lung Cancer 68(3), 415–419 (2010).
  MedlineGoogle Scholar
• 10 Zaïr ZM, Eloranta JJ, Stieger B, Kullak-Ublick GA. Pharmacogenetics of OATP (SLC21/SLCO), OAT and OCT (SLC22) and PEPT (SLC15) transporters in the intestine, liver and kidney. Pharmacogenomics 9(5), 597–624 (2008).
  CASGoogle Scholar
• 11 ISRCTN registry. www.controlled-trials.com.
  Google Scholar
• 12 ClinicalTrials.gov.www.clinicaltrials.gov.
  Google Scholar
• 13 National Cancer Institute. www.cancer.gov/clinicaltrials/search.
  Google Scholar
• 14 World Health Organization. www.who.int/trialsearch.
  Google Scholar
• 15 Australian New Zealand Clinical Trials Registry. www.anzctr.org.au.
  Google Scholar
• 16 Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339, b2535 (2009).
  MedlineGoogle Scholar
• 17 Casp. Critical appraisal skills programme (2015).
  Google Scholar
• 18 Dupont WD, Plummer WD. Power and sample size calculations for studies involving linear regression. Control Clin. Trials 19(6), 589–601 (1998).
  Medline CASGoogle Scholar
• 19 Tamura M, Kondo M, Horio M et al. Genetic polymorphisms of the adenosine triphosphate-binding cassette transporters (ABCG2, ABCB1) and gefitinib toxicity. Nagoya J Med. Sci. 74(1–2), 133–140 (2012).
  Medline CASGoogle Scholar
• 20 Han JY, Lim HS, Yoo YK et al. Associations of ABCB1, ABCC2 and ABCG2 polymorphisms with irinotecan-pharmacokinetics and clinical outcome in patients with advanced non-small cell lung cancer. Cancer 110(1), 138–147 (2007).
  MedlineGoogle Scholar
• 21 Han JY, Lim HS, Park YH, Lee SY, Lee JS. Integrated pharmacogenetic prediction of irinotecan pharmacokinetics and toxicity in patients with advanced non-small cell lung cancer. Lung Cancer 63(1), 115–120 (2009).
  MedlineGoogle Scholar
• 22 Cusatis G, Gregorc V, Li J et al. Pharmacogenetics of ABCG2 and adverse reactions to gefitinib. J. Natl Cancer Inst. 98(23), 1739–1742 (2006).
  Medline CASGoogle Scholar
• 23 Akasaka K, Kaburagi T, Yasuda S et al. Impact of functional ABCG2 polymorphisms on the adverse effects of gefitinib in Japanese patients with non-small-cell lung cancer. Cancer Chemother. Pharmacol. 66(4), 691–698 (2010).
  Medline CASGoogle Scholar
• 24 Kobayashi H, Sato K, Niioka T, Miura H, Ito H, Miura M. Relationship among gefitinib exposure, polymorphisms of its metabolizing enzymes and transporters, and side effects in Japanese patients with non-small-cell lung cancer. Clin. Lung Cancer 16(4), 274–281 (2015).
  Medline CASGoogle Scholar
• 25 Cha PC, Mushiroda T, Zembutsu H et al. Single nucleotide polymorphism in ABCG2 is associated with irinotecan-induced severe myelosuppression. J. Hum. Genet. 54(10), 572–580 (2009).
  Medline CASGoogle Scholar
• 26 Dy GK, Mandrekar SJ, Nelson GD et al. A randomized Phase II study of gemcitabine and carboplatin with or without cediranib as first-line therapy in advanced non-small-cell lung cancer North Central Cancer Treatment Group Study N0528. J. Thorac. Oncol. 8(1), 79–88 (2013).
  Medline CASGoogle Scholar
• 27 Innocenti F, Kroetz DL, Schuetz E et al. Comprehensive pharmacogenetic analysis of irinotecan neutropenia and pharmacokinetics. J. Clin. Oncol. 27(16), 2604–2614 (2009).
  Medline CASGoogle Scholar
• 28 Lamba JK, Fridley BL, Ghosh TM, Yu Q, Mehta G, Gupta P. Genetic variation in platinating agent and taxane pathway genes as predictors of outcome and toxicity in advanced non-small-cell lung cancer. Pharmacogenomics 15(12), 1565–1574 (2014).
  CASGoogle Scholar
• 29 Traynor AM, Lee JW, Bayer GK et al. A Phase II trial of Triapine (NSC# 663249) and gemcitabine as second line treatment of advanced non-small-cell lung cancer: Eastern Cooperative Oncology Group Study 1503. Invest. New Drugs 28(1), 91–97 (2010).
  Medline CASGoogle Scholar
• 30 Han BH, Gao G, Wu WT et al. Association of ABCC2 polymorphisms with platinum-based chemotherapy response and severe toxicity in non-small-cell lung cancer patients. Lung Cancer 72(2), 238–243 (2011).
  MedlineGoogle Scholar
• 31 Kiyotani K, Mushiroda T, Kubo M, Zembutsu H, Sugiyama Y, Nakamura Y. Association of genetic polymorphisms in SLCO1B3 and ABCC2 with docetaxel-induced leukopenia. Cancer Sci. 99(5), 967–972 (2008).
  Medline CASGoogle Scholar
• 32 De Jong FA, Scott-Horton TJ, Kroetz DL et al. Irinotecan-induced diarrhea: functional significance of the polymorphic ABCC2 transporter protein. Clin. Pharmacol. Ther. 81(1), 42–49 (2007).
  Medline CASGoogle Scholar
• 33 Lemos C, Giovannetti E, Zucali PA et al. Impact of ABCG2 polymorphisms on the clinical outcome and toxicity of gefitinib in non-small-cell lung cancer patients. Pharmacogenomics 12(2), 159–170 (2011).
  CASGoogle Scholar
• 34 Akasaka K, Kaburagi T, Yasuda S et al. Impact of functional ABCG2 polymorphisms on the adverse effects of gefitinib in Japanese patients with non-small-cell lung cancer. Curr. Microbiol. 61(4), 691–698 (2010).
  Google Scholar
• 35 Liu Y, Hu M. P-glycoprotein and bioavailability-implication of polymorphism. Clinical Chemistry and Laboratory Medicine 38(9), 877–881 (2000).
  Medline CASGoogle Scholar
• 36 Liu JJ, Lu J, McKeage MJ. Membrane transporters as determinants of the pharmacology of platinum anticancer drugs. Curr. Cancer Drug Targets 12(8), 962–986 (2012).
  Medline CASGoogle Scholar
• 37 Adjei AA, Salavaggione OE, Mandrekar SJ et al. Correlation between polymorphisms of the reduced folate carrier gene (SLC19A1) and survival after pemetrexed-based therapy in non-small cell lung cancer: a North Central Cancer Treatment Group-based exploratory study. J. Thoracic Oncol. 5(9), 1346–1353 (2010).
  Google Scholar
• 38 Hasmats J, Kupershmidt I, Rodriguez-Antona C et al. Identification of candidate SNPs for drug induced toxicity from differentially expressed genes in associated tissues. Gene 506(1), 62–68 (2012).
  Medline CASGoogle Scholar
• 39 Johnson C, Pankratz VS, Velazquez AI et al. Candidate pathway-based genetic association study of platinum and platinum–taxane related toxicity in a cohort of primary lung cancer patients. J. Neurol. Sci. 349(1), 124–128 (2015).
  Medline CASGoogle Scholar
• 40 Adjei AA, Mandrekar SJ, Dy GK et al. Phase II trial of pemetrexed plus bevacizumab for second-line therapy of patients with advanced non-small-cell lung cancer: NCCTG and SWOG study N0426. J. Clin. Oncol. 28(4), 614–619 (2010).
  Medline CASGoogle Scholar
• 41 Choi J, Kim J, Kang D et al. Genetic variations of drug transporters can influence on drug response in patients treated with docetaxel chemotherapy. Cancer Res. Treat. 47(3), 509–517 (2015).
  Medline CASGoogle Scholar
• 42 Sprowl JA, Gregorc V, Lazzari C, Mathijssen RH, Loos WJ, Sparreboom A. Associations between ABCC2 polymorphisms and cisplatin disposition and efficacy. Clin Pharmacol. Ther. 91(6), 1022–1026 (2012).
  Medline CASGoogle Scholar
• 43 Han JY, Shin ES, Lee YS et al. A genome-wide association study for irinotecan-related severe toxicities in patients with advanced non-small-cell lung cancer. Pharmacogenomics J. 13(5), 417–422 (2013).
  Medline CASGoogle Scholar
• 44 Chen X, Zhang L, Ren S et al. Genomic polymorphisms of SLC29A3 associated with overall survival in advanced non-small-cell lung cancer treated with gemcitabine. Med. Oncol. 31(4), (2014).
  Google Scholar
• 45 Liu G, Cheng D, Ding K et al. Pharmacogenetic analysis of BR.21, a placebo-controlled randomized Phase III clinical trial of erlotinib in advanced non-small-cell lung cancer. J. Thorac. Oncol. 7(2), 316–322 (2012).
  Medline CASGoogle Scholar
• 46 Wu F, Zhang J, Hu N 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. 38(6), 728–732 (2014).
  MedlineGoogle Scholar
• 47 Xu XJ, Ren HY, Zhou BT et al. Prediction of copper transport protein 1 (CTR1) genotype on severe cisplatin induced toxicity in non-small cell lung cancer (NSCLC) patients. Lung Cancer 77(2), 438–442 (2012).
  MedlineGoogle Scholar
• 48 Chen JS, Chao Y, Bang YJ et al. A Phase I/II and pharmacogenomic study of pemetrexed and cisplatin in patients with unresectable, advanced gastric carcinoma. Anti-Cancer Drugs 21(8), 777–784 (2010).
  Medline CASGoogle Scholar
• 49 Han J-Y, Lim H-S, Yoo Y-K et al. Associations of ABCB1, ABCC2 and ABCG2 polymorphisms with irinotecan-pharmacokinetics and clinical outcome in patients with advanced non-small cell lung cancer. Cancer 110(1), 138–147 (2007). [Erratum appears in Cancer 116 (15), 3749 (2010)].
  MedlineGoogle Scholar
• 50 Han J-Y, Lim H-S, Park YH, Lee SY, Lee JS. Integrated pharmacogenetic prediction of irinotecan pharmacokinetics and toxicity in patients with advanced non-small cell lung cancer. Lung Cancer 63(1), 115–120 (2009).
  MedlineGoogle Scholar
• 51 Isla D, Sarries C, Rosell R et al. Single nucleotide polymorphisms and outcome in docetaxel-cisplatin-treated advanced non-small-cell lung cancer. Ann. Oncol. 15(8), 1194–1203 (2004).
  Medline CASGoogle Scholar
• 52 Pan JH, Han JX, Wu JM, Sheng LJ, Huang HN, Yu QZ. MDR1 single nucleotide polymorphisms predict response to vinorelbine-based chemotherapy in patients with non-small-cell lung cancer. Respiration 75(4), 380–385 (2008).
  Medline CASGoogle Scholar
• 53 Pan JH, Han JX, Wu JM, Huang HN, Yu QZ, Sheng LJ. MDR1 single nucleotide polymorphism G2677T/A and haplotype are correlated with response to docetaxel-cisplatin chemotherapy in patients with non-small-cell lung cancer. Respiration 78(1), 49–55 (2009).
  Medline CASGoogle Scholar
• 54 Viñolas N, Provencio M, Reguart N et al. Single nucleotide polymorphisms in MDR1 gene correlates with outcome in advanced non-small-cell lung cancer patients treated with cisplatin plus vinorelbine. Lung Cancer 71(2), 191–198 (2011).
  Medline CASGoogle Scholar
• 55 Kobayashi H, Murakami Y, Uemura K et al. Human equilibrative nucleoside transporter 1 expression predicts survival of advanced cholangiocarcinoma patients treated with gemcitabine-based adjuvant chemotherapy after surgical resection. Ann. Surg. 256(2), 288–296 (2012).
  MedlineGoogle Scholar
• 56 Kobayashi H, Sato K, Niioka T, Miura H, Ito H, Miura M. Relationship among gefitinib exposure, polymorphisms of its metabolizing enzymes and transporters, and side effects in Japanese patients with non-small-cell lung cancer. Clin. Lung Cancer 16(4), 274–281 (2014).
  MedlineGoogle Scholar
• 57 Van Erp NP, Eechoute K, Van Der Veldt AA et al. Pharmacogenetic pathway analysis for determination of sunitinib-induced toxicity. J. Clin. Oncol. 27(26), 4406–4412 (2009).
  Medline CASGoogle Scholar
• 58 Rudin CM, Liu WQ, Desai A et al. Pharmacogenomic and pharmacokinetic determinants of erlotinib toxicity. J. Clin. Oncol. 26(7), 1119–1127 (2008).
  Medline CASGoogle Scholar
• 59 Shepherd FA, Rodrigues Pereira J, Ciuleanu T et al. Erlotinib in previously treated non-small-cell lung cancer. N. Engl. J. Med. 353(2), 123–132 (2005).
  Medline CASGoogle Scholar
• 60 Juliano RL, Ling V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim. Biophys. Acta 455(1), 152–162 (1976).
  Medline CASGoogle Scholar
• 61 Thiebaut F, Tsuruo T, Hamada H, Gottesman MM, Pastan I, Willingham MC. Cellular localization of the multidrug-resistance gene product P-glycoprotein in normal human tissues. Proc. Natl Acad. Sci. USA 84(21), 7735–7738 (1987).
  Medline CASGoogle Scholar
• 62 Fromm MF. P-glycoprotein: a defense mechanism limiting oral bioavailability and CNS accumulation of drugs. Int. J. Clin. Pharmacol. Ther. 38(2), 69–74 (2000).
  Medline CASGoogle Scholar
• 63 Greiner B, Eichelbaum M, Fritz P et al. The role of intestinal P-glycoprotein in the interaction of digoxin and rifampin. J. Clin. Invest. 104(2), 147–153 (1999).
  Medline CASGoogle Scholar
• 64 Ueda K, Clark DP, Chen CJ, Roninson IB, Gottesman MM, Pastan I. The human multidrug resistance (mdr1) gene. cDNA cloning and transcription initiation. J. Biol. Chem. 262(2), 505–508 (1987).
  Medline CASGoogle Scholar
• 65 Zhao JY, Ikeguchi M, Eckersberg T, Kuo MT. Modulation of multidrug resistance gene expression by dexamethasone in cultured hepatoma cells. Endocrinology 133(2), 521–528 (1993).
  Medline CASGoogle Scholar
• 66 Sissung TM, Baum CE, Deeken J et al. ABCB1 genetic variation influences the toxicity and clinical outcome of patients with androgen independent prostate cancer treated with docetaxel. Clin. Cancer Res. 14(14), 4543–4549 (2008).
  Medline CASGoogle Scholar
• 67 Sissung TM, Mross K, Steinberg SM et al. Association of ABCB1 genotypes with paclitaxel-mediated peripheral neuropathy and neutropenia. Eur. J. Cancer 42(17), 2893–2896 (2006).
  Medline CASGoogle Scholar
• 68 Watanabe T, Kusuhara H, Maeda K, Shitara Y, Sugiyama Y. Physiologically based pharmacokinetic modeling to predict transporter-mediated clearance and distribution of pravastatin in humans. J. Pharmacol. Exp. Ther. 328(2), 652–662 (2009).
  Medline CASGoogle Scholar
• 69 Breuninger LM, Paul S, Gaughan K et al. Expression of multidrug resistance-associated protein in NIH/3T3 cells confers multidrug resistance associated with increased drug efflux and altered intracellular drug distribution. Cancer Res. 55(22), 5342–5347 (1995).
  Medline CASGoogle Scholar
• 70 Stride BD, Grant CE, Loe DW, Hipfner DR, Cole SP, Deeley RG. Pharmacological characterization of the murine and human orthologs of multidrug-resistance protein in transfected human embryonic kidney cells. Mol. Pharmacol. 52(3), 344–353 (1997).
  Medline CASGoogle Scholar
• 71 Saito S, Iida A, Sekine A et al. Identification of 779 genetic variations in eight genes encoding members of the ATP-binding cassette, subfamily C (ABCC/MRP/CFTR). J. Hum. Genet. 47(4), 147–171 (2002).
  Medline CASGoogle Scholar
• 72 Leabman MK, Huang CC, Deyoung J et al. Natural variation in human membrane transporter genes reveals evolutionary and functional constraints. Proc. Natl Acad. Sci. 100(10), 5896–5901 (2003).
  Medline CASGoogle Scholar
• 73 Smith NF, Figg WD, Sparreboom A. Pharmacogenetics of irinotecan metabolism and transport: an update. Toxicol. in vitro 20(2), 163–175 (2006).
  Medline CASGoogle Scholar
• 74 De Jong FA, De Jonge MJA, Verweij J, Mathijssen RHJ. Role of pharmacogenetics in irinotecan therapy. Cancer Lett. 234(1), 90–106 (2006).
  Medline CASGoogle Scholar
• 75 Nguyen TD, Markova S, Liu W et al. Functional characterization of ABCC2 promoter polymorphisms and allele-specific expression. Pharmacogenomics J. 13(5), 396–402 (2013).
  Medline CASGoogle Scholar
• 76 Deng XY, Wang CX, Wang XD et al. Genetic polymorphisms of UGT1A8, UGT1A9, UGT2B7 and ABCC2 in Chinese renal transplant recipients and a comparison with other ethnic populations. Pharmazie 68(4), 240–244 (2013).
  Medline CASGoogle Scholar
• 77 Choi JH, Ahn BM, Yi J et al. MRP2 haplotypes confer differential susceptibility to toxic liver injury. Pharmacogenet. Genomics 17(6), 403–415 (2007).
  Medline CASGoogle Scholar
• 78 Laechelt S, Turrini E, Ruehmkorf A, Siegmund W, Cascorbi I, Haenisch S. Impact of ABCC2 haplotypes on transcriptional and posttranscriptional gene regulation and function. Pharmacogenomics J. 11(1), 25–34 (2011).
  Medline CASGoogle Scholar
• 79 Haenisch S, Zimmermann U, Dazert E et al. Influence of polymorphisms of ABCB1 and ABCC2 on mRNA and protein expression in normal and cancerous kidney cortex. Pharmacogenomics J. 7(1), 56–65 (2007).
  Medline CASGoogle Scholar
• 80 Zamboni WC, Ramanathan RK, Mcleod HL et al. Disposition of 9-nitrocamptothecin and its 9-aminocamptothecin metabolite in relation to ABC transporter genotypes. Invest. New Drugs 24(5), 393–401 (2006).
  Medline CASGoogle Scholar
• 81 Sparreboom A, Danesi R, Ando Y, Chan J, Figg WD. Pharmacogenomics of ABC transporters and its role in cancer chemotherapy. Drug Resist. Updat. 6(2), 71–84 (2003).
  Medline CASGoogle Scholar
• 82 Yang X, Hu Z, Chan SY et al. Novel agents that potentially inhibit irinotecan-induced diarrhea. Curr. Med. Chem. 12(11), 1343–1358 (2005).
  Medline CASGoogle Scholar
• 83 Buda G, Ricci D, Huang CC et al. Polymorphisms in the multiple drug resistance protein 1 and in P-glycoprotein 1 are associated with time to event outcomes in patients with advanced multiple myeloma treated with bortezomib and pegylated liposomal doxorubicin. Ann. Hematol. 89(11), 1133–1140 (2010).
  Medline CASGoogle Scholar
• 84 Panczyk M, Balcerczak E, Piaskowski S, Jamroziak K, Pasz-Walczak G, Mirowski M. ABCB1 gene polymorphisms and haplotype analysis in colorectal cancer. Int. J. Colorectal Dis. 24(8), 895–905 (2009).
  MedlineGoogle Scholar
• 85 Gréen H, Söderkvist P, Rosenberg P, Horvath G, Peterson C. mdr-1 single nucleotide polymorphisms in ovarian cancer tissue: G2677T/A correlates with response to paclitaxel chemotherapy. Clin. Cancer Res. 12(3), 854–859 (2006).
  Medline CASGoogle Scholar
• 86 Stieger B, Meier PJ. Pharmacogenetics of drug transporters in the enterohepatic circulation. Pharmacogenomics 12(5), 611–631 (2011).
  CASGoogle Scholar
• 87 Pao W, Kris MG, Iafrate AJ et al. Integration of molecular profiling into the lung cancer clinic. Clin. Cancer Res. 15(17), 5317–5322 (2009).
  MedlineGoogle Scholar
• 88 Singer DRJ, Watkins J. Using companion and coupled diagnostics within strategy to personalize targeted medicines. Personalized Med. 9(7), 751–761 (2012).
  CASGoogle Scholar
• 89 US FDA. List of Cleared or Approved Companion Diagnostic Devices (In vitro and Imaging Tools). www.fda.gov/MedicalDevices/ProductsandMedicalProcedures/InVitroDiagnostics/ucm301431.htm.
  Google Scholar