Clinical implementation of pharmacogenetics in kidney transplantation: Calcineurin inhibitors in the starting blocks

British Journal of Clinical Pharmacology

Volumn 77, Issue 4, 2014, Pages 715-728

  Elens, Laure ^a,b   Bouamar, Rachida ^b   Shuker, Nauras ^b   Hesselink, Dennis A ^b   Van Gelder, Teun ^b   Van Schaik, Ron H N ^b  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

calcineurin inhibitors; ciclosporin; kidney transplantation; pharmacogenetics; tacrolimus

Indexed keywords

CALCINEURIN INHIBITOR; CYCLOSPORIN A; CYTOCHROME P450 3A; CYTOCHROME P450 3A4; CYTOCHROME P450 3A5; CYTOCHROME P450 REDUCTASE; MULTIDRUG RESISTANCE PROTEIN 1; TACROLIMUS; CYCLOSPORIN;

ARTICLE; DRUG EFFICACY; DRUG ELIMINATION; DRUG METABOLISM; GENE FREQUENCY; GENETIC ASSOCIATION; GENOTYPE; GRAFT SURVIVAL; HAPLOTYPE; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY TRANSPLANTATION; NEPHROTOXICITY; PHARMACODYNAMICS; PHARMACOGENETICS; PRIORITY JOURNAL; ALLELE; DRUG INACTIVATION; GENETIC SCREENING; GENETICS; GRAFT REJECTION; PROCEDURES;

ALLELES; CALCINEURIN INHIBITORS; CYCLOSPORINE; GENETIC TESTING; GRAFT REJECTION; HUMANS; INACTIVATION, METABOLIC; KIDNEY TRANSPLANTATION; PHARMACOGENETICS; TACROLIMUS;

EID: 84897909350     PISSN: 03065251     EISSN: 13652125     Source Type: Journal    
DOI: 10.1111/bcp.12253     Document Type: Article

References (101)

1. Hariharan S, Johnson CP, Bresnahan BA, Taranto SE, McIntosh MJ, Stablein D,. Improved graft survival after renal transplantation in the United States, 1988 to 1996. N Engl J Med 2000; 342: 605-612.
2. Dunn CJ, Wagstaff AJ, Perry CM, Plosker GL, Goa KL,. Cyclosporin: an updated review of the pharmacokinetic properties, clinical efficacy and tolerability of a microemulsion-based formulation (neoral)1 in organ transplantation. Drugs 2001; 61: 1957-2016.
3. Staatz CE, Tett SE,. Clinical pharmacokinetics and pharmacodynamics of tacrolimus in solid organ transplantation. Clin Pharmacokinet 2004; 43: 623-653.
4. Bouamar R, Shuker N, Hesselink DA, Weimar W, Ekberg H, Kaplan B, Bernasconi C, van Gelder T,. Tacrolimus predose concentrations do not predict the risk of acute rejection after renal transplantation: a pooled analysis from three randomized-controlled clinical trials. Am J Transplant 2013; 13: 459-461.
5. Pascual M, Theruvath T, Kawai T, Tolkoff-Rubin N, Cosimi AB,. Strategies to improve long-term outcomes after renal transplantation. N Engl J Med 2002; 346: 580-590.
6. Elens L, Hesselink DA, van Schaik RH, van Gelder T,. Pharmacogenetics in kidney transplantation: recent updates and potential clinical applications. Mol Diagn Ther 2012; 16: 331-345.
7. Staatz CE, Goodman LK, Tett SE,. Effect of CYP3A and ABCB1 single nucleotide polymorphisms on the pharmacokinetics and pharmacodynamics of calcineurin inhibitors: part II. Clin Pharmacokinet 2010; 49: 207-221.
8. Staatz CE, Goodman LK, Tett SE,. Effect of CYP3A and ABCB1 single nucleotide polymorphisms on the pharmacokinetics and pharmacodynamics of calcineurin inhibitors: part I. Clin Pharmacokinet 2010; 49: 141-175.
9. Metalidis C, Kuypers D,. Immunosuppressive therapy after kidney transplantation: current and new strategies. Minerva Urol Nefrol 2011; 63: 1-19.
10. Picard N, Marquet P,. The influence of pharmacogenetics and cofactors on clinical outcomes in kidney transplantation. Expert Opin Drug Metab Toxicol 2011; 7: 731-743.
11. Sprangers B, Kuypers DR, Vanrenterghem Y,. Immunosuppression: does one regimen fit all? Transplantation 2011; 92: 251-261.
12. Kronbach T, Fischer V, Meyer UA,. Cyclosporine metabolism in human liver: identification of a cytochrome P-450III gene family as the major cyclosporine-metabolizing enzyme explains interactions of cyclosporine with other drugs. Clin Pharmacol Ther 1988; 43: 630-635.
13. Dai Y, Iwanaga K, Lin YS, Hebert MF, Davis CL, Huang W, Kharasch ED, Thummel KE,. In vitro metabolism of cyclosporine A by human kidney CYP3A5. Biochem Pharmacol 2004; 68: 1889-1902.
14. Elens L, van Gelder T, Hesselink DA, Haufroid V, van Schaik RH,. CYP3A4*22: promising newly identified CYP3A4 variant allele for personalizing pharmacotherapy. Pharmacogenomics 2013; 14: 47-62.
15. Min DI, Ellingrod VL,. Association of the CYP3A4*1B 5′-flanking region polymorphism with cyclosporine pharmacokinetics in healthy subjects. Ther Drug Monit 2003; 25: 305-309.
16. Amirimani B, Ning B, Deitz AC, Weber BL, Kadlubar FF, Rebbeck TR,. Increased transcriptional activity of the CYP3A4*1B promoter variant. Environ Mol Mutagen 2003; 42: 299-305.
17. Singh R, Srivastava A, Kapoor R, Sharma RK, Mittal DR,. Impact of CYP3A5 and CYP3A4 gene polymorphisms on dose requirement of calcineurin inhibitors, cyclosporine and tacrolimus, in renal allograft recipients of North India. Naunyn Schmiedebergs Arch Pharmacol 2009; 380: 169-177.
18. Hesselink DA, van Schaik RH, van der Heiden IP, van der Werf M, Gregoor PJ, Lindemans J, Weimar W, van Gelder T,. Genetic polymorphisms of the CYP3A4, CYP3A5, and MDR-1 genes and pharmacokinetics of the calcineurin inhibitors cyclosporine and tacrolimus. Clin Pharmacol Ther 2003; 74: 245-254.
19. Rivory LP, Qin H, Clarke SJ, Eris J, Duggin G, Ray E, Trent RJ, Bishop JF,. Frequency of cytochrome P450 3A4 variant genotype in transplant population and lack of association with cyclosporin clearance. Eur J Clin Pharmacol 2000; 56: 395-398.
20. von Ahsen N, Richter M, Grupp C, Ringe B, Oellerich M, Armstrong VW,. No influence of the MDR-1 C3435T polymorphism or a CYP3A4 promoter polymorphism (CYP3A4-V allele) on dose-adjusted cyclosporin A trough concentrations or rejection incidence in stable renal transplant recipients. Clin Chem 2001; 47: 1048-1052.
21. Hesselink DA, van Gelder T, van Schaik RH, Balk AH, van der Heiden IP, van Dam T, van der Werf M, Weimar W, Mathot RA,. Population pharmacokinetics of cyclosporine in kidney and heart transplant recipients and the influence of ethnicity and genetic polymorphisms in the MDR-1, CYP3A4, and CYP3A5 genes. Clin Pharmacol Ther 2004; 76: 545-556.
22. Zochowska D, Wyzgal J, Paczek L,. Impact of CYP3A4*1B and CYP3A5*3 polymorphisms on the pharmacokinetics of cyclosporine and sirolimus in renal transplant recipients. Ann Transplant 2012; 17: 36-44.
23. Kuehl P, Zhang J, Lin Y, Lamba J, Assem M, Schuetz J, Watkins PB, Daly A, Wrighton SA, Hall SD, Maurel P, Relling M, Brimer C, Yasuda K, Venkataramanan R, Strom S, Thummel K, Boguski MS, Schuetz E,. Sequence diversity in CYP3A promoters and characterization of the genetic basis of polymorphic CYP3A5 expression. Nat Genet 2001; 27: 383-391.
24. Hu YF, Tu JH, Tan ZR, Liu ZQ, Zhou G, He J, Wang D, Zhou HH,. Association of CYP3A4*18B polymorphisms with the pharmacokinetics of cyclosporine in healthy subjects. Xenobiotica 2007; 37: 315-327.
25. Meng XG, Guo CX, Feng GQ, Zhao YC, Zhou BT, Han JL, Chen X, Shi Y, Shi HY, Yin JY, Peng XD, Pei Q, Zhang W, Wang G, He M, Liu M, Yang JK, Zhou HH,. Association of CYP3A polymorphisms with the pharmacokinetics of cyclosporine A in early post-renal transplant recipients in China. Acta Pharmacol Sin 2012; 33: 1563-1570.
26. Qiu XY, Jiao Z, Zhang M, Zhong LJ, Liang HQ, Ma CL, Zhang L, Zhong MK,. Association of MDR1, CYP3A4*18B, and CYP3A5*3 polymorphisms with cyclosporine pharmacokinetics in Chinese renal transplant recipients. Eur J Clin Pharmacol 2008; 64: 1069-1084.
27. Li DY, Teng RC, Zhu HJ, Fang Y,. CYP3A4/5 polymorphisms affect the blood level of cyclosporine and tacrolimus in Chinese renal transplant recipients. Int J Clin Pharmacol Ther 2013; 51: 466-474.
28. Zheng S, Tasnif Y, Hebert MF, Davis CL, Shitara Y, Calamia JC, Lin YS, Shen DD, Thummel KE,. CYP3A5 gene variation influences cyclosporine A metabolite formation and renal cyclosporine disposition. Transplantation 2013; 95: 821-827.
29. Haehner BD, Gorski JC, Vandenbranden M, Wrighton SA, Janardan SK, Watkins PB, Hall SD,. Bimodal distribution of renal cytochrome P450 3A activity in humans. Mol Pharmacol 1996; 50: 52-59.
30. Haufroid V, Mourad M, Van Kerckhove V, Wawrzyniak J, De Meyer M, Eddour DC, Malaise J, Lison D, Squifflet JP, Wallemacq P,. The effect of CYP3A5 and MDR1 (ABCB1) polymorphisms on cyclosporine and tacrolimus dose requirements and trough blood levels in stable renal transplant patients. Pharmacogenetics 2004; 14: 147-154.
31. Anglicheau D, Thervet E, Etienne I, Hurault De Ligny B, Le Meur Y, Touchard G, Buchler M, Laurent-Puig P, Tregouet D, Beaune P, Daly A, Legendre C, Marquet P,. CYP3A5 and MDR1 genetic polymorphisms and cyclosporine pharmacokinetics after renal transplantation. Clin Pharmacol Ther 2004; 75: 422-433.
32. Kreutz R, Zurcher H, Kain S, Martus P, Offermann G, Beige J,. The effect of variable CYP3A5 expression on cyclosporine dosing, blood pressure and long-term graft survival in renal transplant patients. Pharmacogenetics 2004; 14: 665-671.
33. Zhao Y, Song M, Guan D, Bi S, Meng J, Li Q, Wang W,. Genetic polymorphisms of CYP3A5 genes and concentration of the cyclosporine and tacrolimus. Transplant Proc 2005; 37: 178-181.
34. Tang HL, Ma LL, Xie HG, Zhang T, Hu YF,. Effects of the CYP3A5*3 variant on cyclosporine exposure and acute rejection rate in renal transplant patients: a meta-analysis. Pharmacogenet Genomics 2010; 20: 525-531.
35. Fukushima-Uesaka H, Saito Y, Watanabe H, Shiseki K, Saeki M, Nakamura T, Kurose K, Sai K, Komamura K, Ueno K, Kamakura S, Kitakaze M, Hanai S, Nakajima T, Matsumoto K, Saito H, Goto Y, Kimura H, Katoh M, Sugai K, Minami N, Shirao K, Tamura T, Yamamoto N, Minami H, Ohtsu A, Yoshida T, Saijo N, Kitamura Y, Kamatani N, Ozawa S, Sawada J,. Haplotypes of CYP3A4 and their close linkage with CYP3A5 haplotypes in a Japanese population. Hum Mutat 2004; 23: 100.
36. Zeng Y, He YJ, He FY, Fan L, Zhou HH,. Effect of bifendate on the pharmacokinetics of cyclosporine in relation to the CYP3A4*18B genotype in healthy subjects. Acta Pharmacol Sin 2009; 30: 478-484.
37. Elens L, Bouamar R, Hesselink DA, Haufroid V, van Gelder T, van Schaik RH,. The new CYP3A4 intron 6 C>T polymorphism (CYP3A4*22) is associated with an increased risk of delayed graft function and worse renal function in cyclosporine-treated kidney transplant patients. Pharmacogenet Genomics 2012; 22: 373-380.
38. Elens L, Nieuweboer A, Clarke SJ, Charles KA, de Graan AJ, Haufroid V, Mathijssen RH, van Schaik RH,. CYP3A4 intron 6 C>T SNP (CYP3A4*22) encodes lower CYP3A4 activity in cancer patients, as measured with probes midazolam and erythromycin. Pharmacogenomics 2013; 14: 137-149.
39. Wang D, Guo Y, Wrighton SA, Cooke GE, Sadee W,. Intronic polymorphism in CYP3A4 affects hepatic expression and response to statin drugs. Pharmacogenomics J 2011; 11: 274-286.
40. Elens L, van Schaik RH, Panin N, de Meyer M, Wallemacq P, Lison D, Mourad M, Haufroid V,. Effect of a new functional CYP3A4 polymorphism on calcineurin inhibitors' dose requirements and trough blood levels in stable renal transplant patients. Pharmacogenomics 2011; 12: 1383-1396.
41. Elens L, Bouamar R, Hesselink DA, Haufroid V, van der Heiden IP, van Gelder T, van Schaik RH,. A new functional CYP3A4 intron 6 polymorphism significantly affects tacrolimus pharmacokinetics in kidney transplant recipients. Clin Chem 2011; 57: 1574-1583.
42. Metalidis C, Lerut E, Naesens M, Kuypers DR,. Expression of CYP3A5 and P-glycoprotein in renal allografts with histological signs of calcineurin inhibitor nephrotoxicity. Transplantation 2011; 91: 1098-1102.
43. Hauser IA, Schaeffeler E, Gauer S, Scheuermann EH, Wegner B, Gossmann J, Ackermann H, Seidl C, Hocher B, Zanger UM, Geiger H, Eichelbaum M, Schwab M,. ABCB1 genotype of the donor but not of the recipient is a major risk factor for cyclosporine-related nephrotoxicity after renal transplantation. J Am Soc Nephrol 2005; 16: 1501-1511.
44. Kato R, Nishide M, Kozu C, Iwamoto A, Urashima K, Suzuki K, Ijiri Y, Hayashi T, Tanaka K,. Is cyclosporine A transport inhibited by pravastatin via multidrug resistant protein 2? Eur J Clin Pharmacol 2010; 66: 153-158.
45. Shuker N, Bouamar R, Weimar W, van Schaik RH, van Gelder T, Hesselink DA,. ATP-binding cassette transporters as pharmacogenetic biomarkers for kidney transplantation. Clin Chim Acta 2012; 413: 1326-1337.
46. Naesens M, Lerut E, de Jonge H, Van Damme B, Vanrenterghem Y, Kuypers DR,. Donor age and renal P-glycoprotein expression associate with chronic histological damage in renal allografts. J Am Soc Nephrol 2009; 20: 2468-2480.
47. Joy MS, Nickeleit V, Hogan SL, Thompson BD, Finn WF,. Calcineurin inhibitor-induced nephrotoxicity and renal expression of P-glycoprotein. Pharmacotherapy 2005; 25: 779-789.
48. Kimchi-Sarfaty C, Oh JM, Kim IW, Sauna ZE, Calcagno AM, Ambudkar SV, Gottesman MM,. A 'silent' polymorphism in the MDR1 gene changes substrate specificity. Science 2007; 315: 525-528.
49. Wang D, Johnson AD, Papp AC, Kroetz DL, Sadee W,. Multidrug resistance polypeptide 1 (MDR1, ABCB1) variant 3435C>T affects mRNA stability. Pharmacogenet Genomics 2005; 15: 693-704.
50. Woillard JB, Rerolle JP, Picard N, Rousseau A, Guillaudeau A, Munteanu E, Essig M, Drouet M, Le Meur Y, Marquet P,. Donor P-gp polymorphisms strongly influence renal function and graft loss in a cohort of renal transplant recipients on cyclosporine therapy in a long-term follow-up. Clin Pharmacol Ther 2010; 88: 95-100.
51. Moore J, McKnight AJ, Dohler B, Simmonds MJ, Courtney AE, Brand OJ, Briggs D, Ball S, Cockwell P, Patterson CC, Maxwell AP, Gough SC, Opelz G, Borrows R,. Donor ABCB1 variant associates with increased risk for kidney allograft failure. J Am Soc Nephrol 2012; 23: 1891-1899.
52. Huls M, Kramers C, Levtchenko EN, Wilmer MJ, Dijkman HB, Kluijtmans LA, van der Hoorn JW, Russel FG, Masereeuw R,. P-glycoprotein-deficient mice have proximal tubule dysfunction but are protected against ischemic renal injury. Kidney Int 2007; 72: 1233-1241.
53. Huls M, Schoeber JP, Verfaillie CM, Luttun A, Ulloa-Montoya F, Menke AL, van Bolderen LR, Woestenenk RM, Merkx GF, Wetzels JF, Russel FG, Masereeuw R,. Deficiency of either P-glycoprotein or breast cancer resistance protein protect against acute kidney injury. Cell Transplant 2010; 19: 1195-1208.
54. Bandur S, Petrasek J, Hribova P, Novotna E, Brabcova I, Viklicky O,. Haplotypic structure of ABCB1/MDR1 gene modifies the risk of the acute allograft rejection in renal transplant recipients. Transplantation 2008; 86: 1206-1213.
55. Crettol S, Venetz JP, Fontana M, Aubert JD, Ansermot N, Fathi M, Pascual M, Eap CB,. Influence of ABCB1 genetic polymorphisms on cyclosporine intracellular concentration in transplant recipients. Pharmacogenet Genomics 2008; 18: 307-315.
56. Grinyo J, Vanrenterghem Y, Nashan B, Vincenti F, Ekberg H, Lindpaintner K, Rashford M, Nasmyth-Miller C, Voulgari A, Spleiss O, Truman M, Essioux L,. Association of four DNA polymorphisms with acute rejection after kidney transplantation. Transpl Int 2008; 21: 879-891.
57. Hubbard PA, Shen AL, Paschke R, Kasper CB, Kim JJ,. NADPH-cytochrome P450 oxidoreductase. Structural basis for hydride and electron transfer. J Biol Chem 2001; 276: 29163-29170.
58. Huang N, Agrawal V, Giacomini KM, Miller WL,. Genetics of P450 oxidoreductase: sequence variation in 842 individuals of four ethnicities and activities of 15 missense mutations. Proc Natl Acad Sci U S A 2008; 105: 1733-1738.
59. Elens L, Hesselink DA, Bouamar R, Budde K, de Fijter JW, De Meyer M, Mourad M, Kuypers DR, Haufroid V, van Gelder T, van Schaik RH,. Impact of POR*28 on the pharmacokinetics of Tacrolimus and Cyclosporine a in renal transplant patients. Ther Drug Monit 2013 September 20. [Epub ahead of print].
60. Kamdem LK, Streit F, Zanger UM, Brockmoller J, Oellerich M, Armstrong VW, Wojnowski L,. Contribution of CYP3A5 to the in vitro hepatic clearance of tacrolimus. Clin Chem 2005; 51: 1374-1381.
61. Elens L, Capron A, Kerckhove VV, Lerut J, Mourad M, Lison D, Wallemacq P, Haufroid V,. 1199G>A and 2677G>T/A polymorphisms of ABCB1 independently affect tacrolimus concentration in hepatic tissue after liver transplantation. Pharmacogenet Genomics 2007; 17: 873-883.
62. Goto M, Masuda S, Kiuchi T, Ogura Y, Oike F, Okuda M, Tanaka K, Inui K,. CYP3A5*1-carrying graft liver reduces the concentration/oral dose ratio of tacrolimus in recipients of living-donor liver transplantation. Pharmacogenetics 2004; 14: 471-478.
63. Haufroid V, Wallemacq P, VanKerckhove V, Elens L, De Meyer M, Eddour DC, Malaise J, Lison D, Mourad M,. CYP3A5 and ABCB1 polymorphisms and tacrolimus pharmacokinetics in renal transplant candidates: guidelines from an experimental study. Am J Transplant 2006; 6: 2706-2713.
64. Hesselink DA, van Schaik RH, van Agteren M, de Fijter JW, Hartmann A, Zeier M, Budde K, Kuypers DR, Pisarski P, Le Meur Y, Mamelok RD, van Gelder T,. CYP3A5 genotype is not associated with a higher risk of acute rejection in tacrolimus-treated renal transplant recipients. Pharmacogenet Genomics 2008; 18: 339-348.
65. Kuypers DR, de Jonge H, Naesens M, Lerut E, Verbeke K, Vanrenterghem Y,. CYP3A5 and CYP3A4 but not MDR1 single nucleotide polymorphisms determine long-term tacrolimus disposition and drug-related nephrotoxicity in renal recipients. Clin Pharmacol Ther 2007; 82: 711-725.
66. Macphee IA, Fredericks S, Mohamed M, Moreton M, Carter ND, Johnston A, Goldberg L, Holt DW,. Tacrolimus pharmacogenetics: the CYP3A5*1 allele predicts low dose-normalized tacrolimus blood concentrations in whites and South Asians. Transplantation 2005; 79: 499-502.
67. Thervet E, Anglicheau D, King B, Schlageter MH, Cassinat B, Beaune P, Legendre C, Daly AK,. Impact of cytochrome p450 3A5 genetic polymorphism on tacrolimus doses and concentration-to-dose ratio in renal transplant recipients. Transplantation 2003; 76: 1233-1235.
68. Tsuchiya N, Satoh S, Tada H, Li Z, Ohyama C, Sato K, Suzuki T, Habuchi T, Kato T,. Influence of CYP3A5 and MDR1 (ABCB1) polymorphisms on the pharmacokinetics of tacrolimus in renal transplant recipients. Transplantation 2004; 78: 1182-1187.
69. van Gelder T, Hesselink DA,. Dosing tacrolimus based on CYP3A5 genotype: will it improve clinical outcome? Clin Pharmacol Ther 2010; 87: 640-641.
70. Zheng H, Webber S, Zeevi A, Schuetz E, Zhang J, Bowman P, Boyle G, Law Y, Miller S, Lamba J, Burckart GJ,. Tacrolimus dosing in pediatric heart transplant patients is related to CYP3A5 and MDR1 gene polymorphisms. Am J Transplant 2003; 3: 477-483.
71. Zheng H, Zeevi A, Schuetz E, Lamba J, McCurry K, Griffith BP, Webber S, Ristich J, Dauber J, Iacono A, Grgurich W, Zaldonis D, McDade K, Zhang J, Burckart GJ,. Tacrolimus dosing in adult lung transplant patients is related to cytochrome P4503A5 gene polymorphism. J Clin Pharmacol 2004; 44: 135-140.
72. MacPhee IA, Fredericks S, Tai T, Syrris P, Carter ND, Johnston A, Goldberg L, Holt DW,. The influence of pharmacogenetics on the time to achieve target tacrolimus concentrations after kidney transplantation. Am J Transplant 2004; 4: 914-919.
73. Undre NA,. Pharmacokinetics of tacrolimus-based combination therapies. Nephrol Dial Transplant 2003; 18 (Suppl. 1): i12-15.
74. Undre NA, van Hooff J, Christiaans M, Vanrenterghem Y, Donck J, Heeman U, Kohnle M, Zanker B, Land W, Morales JM, Andres A, Schafer A, Stevenson P,. Low systemic exposure to tacrolimus correlates with acute rejection. Transplant Proc 1999; 31: 296-298.
75. Chen JS, Li LS, Cheng DR, Ji SM, Sun QQ, Cheng Z, Wen JQ, Sha GZ, Liu ZH,. Effect of CYP3A5 genotype on renal allograft recipients treated with tacrolimus. Transplant Proc 2009; 41: 1557-1561.
76. Tang HL, Xie HG, Yao Y, Hu YF,. Lower tacrolimus daily dose requirements and acute rejection rates in the CYP3A5 nonexpressers than expressers. Pharmacogenet Genomics 2011; 21: 713-720.
77. Birdwell KA, Grady B, Choi L, Xu H, Bian A, Denny JC, Jiang M, Vranic G, Basford M, Cowan JD, Richardson DM, Robinson MP, Ikizler TA, Ritchie MD, Stein CM, Haas DW,. The use of a DNA biobank linked to electronic medical records to characterize pharmacogenomic predictors of tacrolimus dose requirement in kidney transplant recipients. Pharmacogenet Genomics 2012; 22: 32-42.
78. Hesselink DA, Bouamar R, van Gelder T,. The pharmacogenetics of calcineurin inhibitor-related nephrotoxicity. Ther Drug Monit 2010; 32: 387-393.
79. MacPhee IA,. Pharmacogenetic biomarkers: cytochrome P450 3A5. Clin Chim Acta 2012; 413: 1312-1317.
80. Thervet E, Loriot MA, Barbier S, Buchler M, Ficheux M, Choukroun G, Toupance O, Touchard G, Alberti C, Le Pogamp P, Moulin B, Le Meur Y, Heng AE, Subra JF, Beaune P, Legendre C,. Optimization of initial tacrolimus dose using pharmacogenetic testing. Clin Pharmacol Ther 2010; 87: 721-726.
81. Passey C, Birnbaum AK, Brundage RC, Oetting WS, Israni AK, Jacobson PA,. Dosing equation for tacrolimus using genetic variants and clinical factors. Br J Clin Pharmacol 2011; 72: 948-957.
82. Boughton O, Borgulya G, Cecconi M, Fredericks S, Moreton-Clack M, Macphee IA,. A published pharmacogenetic algorithm was poorly predictive of tacrolimus clearance in an independent cohort of renal transplant recipients. Br J Clin Pharmacol 2013; 76: 425-431.
83. Elens L, Hesselink DA, van Schaik RH, van Gelder T,. The CYP3A4*22 allele affects the predictive value of a pharmacogenetic algorithm predicting tacrolimus predose concentrations. Br J Clin Pharmacol 2012; 75: 1545-1547.
84. Elens L, Capron A, van Schaik RH, De Meyer M, De Pauw L, Eddour DC, Latinne D, Wallemacq P, Mourad M, Haufroid V,. Impact of CYP3A4*22 allele on tacrolimus pharmacokinetics in early period after renal transplantation: toward updated genotype-based dosage guidelines. Ther Drug Monit 2013; 35: 608-616.
85. Gijsen VM, van Schaik RH, Elens L, Soldin OP, Soldin SJ, Koren G, de Wildt SN,. CYP3A4*22 and CYP3A combined genotypes both correlate with tacrolimus disposition in pediatric heart transplant recipients. Pharmacogenomics 2013; 14: 1027-1036.
86. Capron A, Lerut J, Latinne D, Rahier J, Haufroid V, Wallemacq P,. Correlation of tacrolimus levels in peripheral blood mononuclear cells with histological staging of rejection after liver transplantation: preliminary results of a prospective study. Transpl Int 2012; 25: 41-47.
87. Capron A, Mourad M, De Meyer M, De Pauw L, Eddour DC, Latinne D, Elens L, Haufroid V, Wallemacq P,. CYP3A5 and ABCB1 polymorphisms influence tacrolimus concentrations in peripheral blood mononuclear cells after renal transplantation. Pharmacogenomics 2010; 11: 703-714.
88. De Meyer M, Haufroid V, Elens L, Fusaro F, Patrono D, De Pauw L, Kanaan N, Goffin E, Mourad M,. Donor age and ABCB1 1199G>A genetic polymorphism are independent factors affecting long-term renal function after kidney transplantation. J Surg Res 2012; 178: 988-995.
89. de Jonge H, Metalidis C, Naesens M, Lambrechts D, Kuypers DR,. The P450 oxidoreductase*28 SNP is associated with low initial tacrolimus exposure and increased dose requirements in CYP3A5-expressing renal recipients. Pharmacogenomics 2011; 12: 1281-1291.
90. Op den Buijsch RA, Christiaans MH, Stolk LM, de Vries JE, Cheung CY, Undre NA, van Hooff JP, van Dieijen-Visser MP, Bekers O,. Tacrolimus pharmacokinetics and pharmacogenetics: influence of adenosine triphosphate-binding cassette B1 (ABCB1) and cytochrome (CYP) 3A polymorphisms. Fundam Clin Pharmacol 2007; 21: 427-435.
91. Tirelli S, Ferraresso M, Ghio L, Meregalli E, Martina V, Belingheri M, Mattiello C, Torresani E, Edefonti A,. The effect of CYP3A5 polymorphisms on the pharmacokinetics of tacrolimus in adolescent kidney transplant recipients. Med Sci Monit 2008; 14: CR251-254.
92. Zhang X, Liu ZH, Zheng JM, Chen ZH, Tang Z, Chen JS, Li LS,. Influence of CYP3A5 and MDR1 polymorphisms on tacrolimus concentration in the early stage after renal transplantation. Clin Transplant 2005; 19: 638-643.
93. Loh PT, Lou HX, Zhao Y, Chin YM, Vathsala A,. Significant impact of gene polymorphisms on tacrolimus but not cyclosporine dosing in Asian renal transplant recipients. Transplant Proc 2008; 40: 1690-1695.
94. Renders L, Frisman M, Ufer M, Mosyagin I, Haenisch S, Ott U, Caliebe A, Dechant M, Braun F, Kunzendorf U, Cascorbi I,. CYP3A5 genotype markedly influences the pharmacokinetics of tacrolimus and sirolimus in kidney transplant recipients. Clin Pharmacol Ther 2007; 81: 228-234.
95. Satoh S, Kagaya H, Saito M, Inoue T, Miura M, Inoue K, Numakura K, Tsuchiya N, Tada H, Suzuki T, Habuchi T,. Lack of tacrolimus circadian pharmacokinetics and CYP3A5 pharmacogenetics in the early and maintenance stages in Japanese renal transplant recipients. Br J Clin Pharmacol 2008; 66: 207-214.
96. Roy JN, Barama A, Poirier C, Vinet B, Roger M,. CYP3A4, CYP3A5, and MDR-1 genetic influences on tacrolimus pharmacokinetics in renal transplant recipients. Pharmacogenet Genomics 2006; 16: 659-665.
97. Mourad M, Wallemacq P, De Meyer M, Brandt D, Van Kerkhove V, Malaise J, Chaib Eddour D, Lison D, Haufroid V,. The influence of genetic polymorphisms of cytochrome P450 3A5 and ABCB1 on starting dose- and weight-standardized tacrolimus trough concentrations after kidney transplantation in relation to renal function. Clin Chem Lab Med 2006; 44: 1192-1198.
98. Fredericks S, Moreton M, Reboux S, Carter ND, Goldberg L, Holt DW, MacPhee IA,. Multidrug resistance gene-1 (MDR-1) haplotypes have a minor influence on tacrolimus dose requirements. Transplantation 2006; 82: 705-708.
99. Tada H, Tsuchiya N, Satoh S, Kagaya H, Li Z, Sato K, Miura M, Suzuki T, Kato T, Habuchi T,. Impact of CYP3A5 and MDR1(ABCB1) C3435T polymorphisms on the pharmacokinetics of tacrolimus in renal transplant recipients. Transplant Proc 2005; 37: 1730-1732.
100. Mourad M, Mourad G, Wallemacq P, Garrigue V, Van Bellingen C, Van Kerckhove V, De Meyer M, Malaise J, Eddour DC, Lison D, Squifflet JP, Haufroid V,. Sirolimus and tacrolimus trough concentrations and dose requirements after kidney transplantation in relation to CYP3A5 and MDR1 polymorphisms and steroids. Transplantation 2005; 80: 977-984.
101. Cheung CY, Op den Buijsch RA, Wong KM, Chan HW, Chau KF, Li CS, Leung KT, Kwan TH, de Vrie JE, Wijnen PA, van Dieijen-Visser MP, Bekers O,. Influence of different allelic variants of the CYP3A and ABCB1 genes on the tacrolimus pharmacokinetic profile of Chinese renal transplant recipients. Pharmacogenomics 2006; 7: 563-574.