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. 2019 Nov 2;138(11):1359–1377. doi: 10.1007/s00439-019-02081-x

Table 1.

Worldwide allele frequencies of SLC variants associated with clinical drug response or toxicity phenotypes

Gene (protein) Variant Type MAF (in %) Association References
NFE FIN ASJ LAT EAS SAS AFR
SLC1A1 (EAAC1) rs2228622:G>A Synonymous (T138T) 41.7 33.9 51.7 40.7 24.6 33.9 21.2 Increased risk of antipsychotics-induced obsessive-compulsive symptoms (OR = 3.9) Kwon et al. (2009)
SLC11A1 (NRAMP1) rs17235409:G>A Missense (D543 N) 2.0 2.2 1.4 11.3 14.1 5.4 6.3 Increased risk of failure of tuberculosis therapy (OR = 11) Salinas-Delgado et al. (2015)
SLC12A3 (NCC) rs1529927:G>C Missense (A264G) 3.6 3.1 0.6 0.6 0.0 0.8 0.6 Increased efficacy of diuretics Vormfelde et al. (2007)
SLC12A6 (KCC3) rs7164902:C>T Synonymous (L159L) 24.3 18.1 25.1 18.3 34.2 34.0 21.6 Decreased risk of thalidomide-induced neuropathy (OR = 0.5–0.6) Johnson et al. (2011)
SLC15A2 (PEPT2) rs1143671:C>T; rs1143672:G>A; rs2257212:C>T Missense (P409S; R509 K; L350F) 45.4 40.8 37.9 24.3 71.5 29.9 48.4 Decreased warfarin dose requirement Cai et al. (2017)
Increased PFS of HCC patients following sorafenib therapy (OR = 0.5) Lee et al. (2015)
SLC16A5 (MCT6) rs4788863:C>T Synonymous (L41L) 26.5 18.7 31.9 38.0 65.6 25.8 25.6 Decreased risk of cisplatin-induced ototoxicity (OR = 0.06) Drögemöller et al. (2017)
SLC16A7 (MCT2) rs3763980:G>T Missense (T445S) 24.7 23.4 23.0 13.6 30.7 22.6 21.5 Increased risk of poor response to methotrexate (OR = 1.9) Moncrieffe et al. (2010)
SLC19A1 (RFC) rs1051266:G>A Missense (R27H) 43.2 45.0 39.9 43.7 52.9 40.8 61.8 Decreased risk of methotrexate-induced GI toxicity (OR = 0.38) Lima et al. (2014)
Increased risk of methotrexate-induced hepatotoxicity (OR = 5.3) Suthandiram et al. (2014)
Decreased frequency of methotrexate discontinuation due to toxicity (HR = 0.33) Bohanec Grabar et al. (2012)
Lower rapid response rate to irinotecan (OR = 3.6) Huang et al. (2013)
rs1051296:T>G 3′ UTR 42.3 43.5 38.7 40.6 54.5 46.0 45.4 Lower fraction of patients above the therapeutic threshold of methotrexate (8.6% GG vs. 40% TT; p = 0.02) Wang et al. (2014)
rs1051298:C>T 3′ UTR 43.6 45.0 38.3 45.3 54.3 N/A 51.2 Decreased survival time following pemetrexate treatment (HR = 1.8) Corrigan et al. (2014)
SLC22A1 (OCT1) rs12208357:C>T Missense (R61C) 7.7 5.6 9.5 2.3 < 0.1 2.9 1 Reduced metformin response in healthy subjects after OGTT; reduced morphine clearance and increased AUC after codeine administration; increased plasma concentrations and efficacy of tropisetron and ondansetron Fukuda et al. (2013), Shu et al. (2007), Tzvetkov et al. (2012, 2013)
rs35167514:ATG>del Missense (M420del) 14.5 11.8 9.2 21.9 < 0.1 11.2 5.5
rs34059508:G>A Missense (G465R) 2.3 0.7 1.3 0.7 0 0.2 0.4
rs34130495:G>A Missense (G401S) 2.6 1.9 0.7 0.9 0 0.3 0.5
rs683369:C>G Missense (L160F) 22.3 16.4 16.2 8.7 14.2 15.4 3.8 Decreased major molecular response to imatinib (OR = 0.6) Cargnin et al. (2018)
Increased risk of resistance to imatinib (OR = 1.9–3.3) Makhtar et al. (2018)
Increased risk of imatinib-induced conjunctival hemorrhage (OR = 4.8) Qiu et al. (2018)
25% decreased imatinib clearance Di Paolo et al. (2014)
rs628031:G>A Missense (M408 V) 41.5 45.4 35.1 20.2 27.3 37.7 27.1 Increased risk of imatinib resistance (OR = 1.3–2.6) Makhtar et al. (2018)
Decreased major molecular response to imatinib (OR = 0.6) Cargnin et al. (2018)
Dec. risk of metformin-induced adverse GI effects (OR = 0.39) Tarasova et al. (2012)
SLC22A2 (OCT2) rs316019:A>C Missense (A270S) 10.1 6 14.7 5.2 12.8 12.5 15.2 Increased AUC of metformin Song et al. (2008)
rs145450955:G>A Missense (T201 M) 0 0 0 0 0.4 0 0 Increased AUC of metformin Song et al. (2008)
rs316019:G>T Missense (S270A) 10.1 6.0 14.7 5.2 12.8 12.5 15.2 Increased Cmax and AUC of metformin Yoon et al. (2013)
Decreased risk of cisplatin-induced ototoxicity (OR = 0.12) Lanvers-Kaminsky et al. (2015)
SLC22A4 (OCTN1) rs1050152:C>T Missense (L503F) 42.2 31 41.5 21.7 0.1 12 7.2 30% reduced renal clearance of gapapentin Urban et al. (2008)
SLC22A5 (OCTN2) rs274558:A>G Synonymous (L269L) 39.1 50.9 40.1 31.6 64.4 62.7 35.8 Increased risk of imatinib-induced edema (OR = 3.2) Qiu et al. (2018)
SLC22A7 (OAT2) rs4149178:A>G 3’ UTR 15.5 15 24.5 20.4 4.3 N/A 34.6 Increased risk of anthracycline-induced cardiotoxicity Visscher et al. (2015)
Increased risk of severe capecitabine toxicity Pellicer et al. (2017)
SLC22A8 (OAT3) rs11568482:A>T Missense (I305F) 0.0 0.0 0.0 0.1 5.9 0.1 0.1 50% decreased renal clearance of cefotaxime Yee et al. (2013)
SLC22A16 (FLIPT2) rs714368:A>G Missense (H49R) 36.9 22.5 30.4 41.7 18.1 21.7 27.5 Increased risk of FAC-induced nausea (OR = 1.8) Tecza et al. (2018)
Decreased requirement for dose delay in AC therapy Bray et al. (2010)
rs723685:T>C Missense (V252A) 8.8 6.8 11.7 12.1 6.9 7.5 11.2 Decreased requirement for dose delay in AC therapy Bray et al. (2010)
rs6907567:T>C Synonymous (N104 N) 21.8 18.2 30.5 22.5 41.6 27.6 36.9 Increased hetatological toxicity of FAC (OR = 3.2) Tecza et al. (2018)
Decreased requirement for dose delay in AC therapy Bray et al. (2010)
rs12210538:T>C Missense (M409T) 23.5 15.8 27.4 11.7 < 0.1 11.3 3.8 Increased requirement for dose delay in AC therapy Bray et al. (2010)
SLC28A1 (CNT1) rs2242046:G>A Missense (D521 N) 50.1 45.2 55.3 20.8 7.6 30.3 8.8 Increased risk of gemcitabine-induced hematologic toxicity Soo et al. (2009)
SLC28A2 (CNT2) rs1060896:C>A Missense (S75R) 65.4 59.2 58.3 30.2 8.6 47.8 17.6 Increased OS of NSCLC patients on gemcitabine Soo et al. (2009)
rs11854484:C>T Missense (P22L) 62.2 58.2 50.9 28.4 7.9 45.4 17.1 Increased risk of gemcitabine-induced hematologic toxicity but increased OS of NSCLC patients Soo et al. (2009)
Increased ribavirin serum levels Rau et al. (2013)
Increased risk of anemia in HCV patients treated with telaprevir or boceprevir (OR = 2.3) Ampuero et al. (2015)
SLC28A3 (CNT3) rs56350726:A>T Missense (Y513F) 5.9 12.7 4.9 2.8 11.5 7.6 15.4 Higher chance of reaching sustained virological response in HCV treatment Rau et al. (2013)
twofold reduced incidence of anemia in HCV patient treated with ribavirin Doehring et al. (2011)
SLC30A8 (ZnT8) rs16889462:G>A Missense (R325Q) 0.1 0.0 0.2 0.6 8.0 0.3 10.5 Increased repaglinide efficacy Huang et al. (2010)
rs13266634:C>T Missense (R325 W) 30.4 38.0 26.1 25.7 44.0 23.0 8.9 Increased repaglinide efficacy Huang et al. (2010)
SLC30A9 (ZnT9) rs1047626:G>A Missense (M50 V) 23.8 20.3 29.1 19.3 4.1 22.4 80.2 Decreased risk of aspirin-exacerbated respiratory disease (OR = 0.13) Shin et al. (2014)
SLC47A1 (MATE1) rs2252281:T>C 5′ UTR 31.2 23.3 36.0 17.6 21.5 N/A 35.1 Enhanced metformin response Stocker et al. (2013)
SLC47A2 (MATE2-K) rs12943590:G>A 5′UTR 27.2 26.7 34.8 34.5 46.9 N/A 21.5 Decreased metformin response Choi et al. (2011) and Stocker et al. (2013)

MAF minor allele frequency, NFE non-Finnish Europeans, FIN Finns, ASJ Ashkenazi Jews, LAT Latinos, EAS East Asians, SAS South Asians, AFR Africans, Cmax peak serum concentration, AUC area under the concentration time curve; HCC hepatocellular carcinoma; NSCLC non-small cell lung cancer; OR odds ratio; HR hazard ratio; PFS progression-free survival; GI gastrointestinal; FAC fluorouracil, anthracycline and cyclophosphamide combination therapy; AC anthracycline and cyclophosphamide combination therapy; OS overall survival; OGTT oral glucose tolerance test