ATP-binding cassette transporters as pharmacogenetic biomarkers for kidney transplantation

Clinica Chimica Acta

Volumn 413, Issue 17-18, 2012, Pages 1326-1337

  Shuker, Nauras ^a,b   Bouamar, Rachida ^a   Weimar, Willem ^b   van Schaik, Ron H N ^c   van Gelder, Teun ^a,b   Hesselink, Dennis A ^b  

^a Clinical Pharmacology Unit ^*  (Netherlands)

^b Department of Internal Medicine   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

ABCB1; ABCC2; Cyclosporine A; Kidney transplantation; Mycophenolic acid; Tacrolimus

Indexed keywords

BIOLOGICAL MARKER; CALCINEURIN INHIBITOR; CYCLOSPORIN A; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; MYCOPHENOLIC ACID; RAPAMYCIN; TACROLIMUS;

ACUTE GRAFT REJECTION; ANEMIA; AREA UNDER THE CURVE; ATP BINDING CASSETTE B1 GENE; ATP BINDING CASSETTE C2 GENE; BINDING AFFINITY; BINDING SITE; BLOOD TOXICITY; BONE MARROW SUPPRESSION; CELLULAR DISTRIBUTION; DIARRHEA; DOSE RESPONSE; DOWN REGULATION; DRUG ABSORPTION; DRUG BLOOD LEVEL; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG ELIMINATION; DRUG EXCRETION; EDEMA; GENE; GENE EXPRESSION; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENETIC VARIABILITY; GRAFT DYSFUNCTION; GRAFT SURVIVAL; HUMAN; HYPERLIPIDEMIA; INFECTION; KIDNEY TRANSPLANTATION; LEUKOPENIA; NEPHROTOXICITY; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; PNEUMONIA; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEINURIA; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; THROMBOCYTOPENIA; TISSUE DISTRIBUTION; UNSPECIFIED SIDE EFFECT; VOMITING;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOMARKERS, PHARMACOLOGICAL; GENETIC VARIATION; HUMANS; IMMUNOSUPPRESSIVE AGENTS; KIDNEY TRANSPLANTATION; POLYMORPHISM, GENETIC;

EID: 84862765589     PISSN: 00098981     EISSN: 18733492     Source Type: Journal    
DOI: 10.1016/j.cca.2011.09.040     Document Type: Review

References (139)

1. Lamb K.E., Lodhi S., Meier-Kriesche H.U. Long-term renal allograft survival in the United States: a critical reappraisal. Am J Transplant 2011, 11:450-462.
2. van Gelder T., Hesselink D.A., van Hest R.M., Mathot R.A., van Schaik R. Pharmacogenetics in immunosuppressive therapy: the best thing since TDM?. Ther Drug Monit 2004, 26:343-346.
3. Dean M., Hamon Y., Chimini G. The human ATP-binding cassette (ABC) transporter superfamily. J Lipid Res 2001, 42:1007-1017.
4. Mo W., Zhang J.T. Oligomerization of human ATP-binding cassette transporters and its potential significance in human disease. Expert Opin Drug Metab Toxicol 2009, 5:1049-1063.
5. Zhou S.F. Structure, function and regulation of P-glycoprotein and its clinical relevance in drug disposition. Xenobiotica 2008, 38:802-832.
6. Gottesman M.M., Pastan I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem 1993, 62:385-427.
7. Juliano R.L., Ling V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta 1976, 455:152-162.
8. Cascorbi I. Role of pharmacogenetics of ATP-binding cassette transporters in the pharmacokinetics of drugs. Pharmacol Ther 2006, 112:457-473.
9. Ernest S., Rajaraman S., Megyesi J., Bello-Reuss E.N. Expression of MDR1 (multidrug resistance) gene and its protein in normal human kidney. Nephron 1997, 77:284-289.
10. Fojo A.T., Shen D.W., Mickley L.A., Pastan I., Gottesman M.M. Intrinsic drug resistance in human kidney cancer is associated with expression of a human multidrug-resistance gene. J Clin Oncol 1987, 5:1922-1927.
11. Koziolek M.J., Riess R., Geiger H., Thevenod F., Hauser I.A. Expression of multidrug resistance P-glycoprotein in kidney allografts from cyclosporine A-treated patients. Kidney Int 2001, 60:156-166.
12. Thiebaut F., Tsuruo T., Hamada H., Gottesman M.M., Pastan I., Willingham M.C. Cellular localization of the multidrug-resistance gene product P-glycoprotein in normal human tissues. Proc Natl Acad Sci U S A 1987, 84:7735-7738.
13. Naesens M., Lerut E., de Jonge H., Van Damme B., Vanrenterghem Y., Kuypers D.R. Donor age and renal P-glycoprotein expression associate with chronic histological damage in renal allografts. J Am Soc Nephrol 2009, 20:2468-2480.
14. Marzolini C., Paus E., Buclin T., Kim R.B. Polymorphisms in human MDR1 (P-glycoprotein): recent advances and clinical relevance. Clin Pharmacol Ther 2004, 75:13-33.
15. Klimecki W.T., Futscher B.W., Grogan T.M., Dalton W.S. P-glycoprotein expression and function in circulating blood cells from normal volunteers. Blood 1994, 83:2451-2458.
16. Randolph G.J., Beaulieu S., Pope M., et al. A physiologic function for p-glycoprotein (MDR-1) during the migration of dendritic cells from skin via afferent lymphatic vessels. Proc Natl Acad Sci U S A 1998, 95:6924-6929.
17. Doran A., Obach R.S., Smith B.J., et al. The impact of P-glycoprotein on the disposition of drugs targeted for indications of the central nervous system: evaluation using the MDR1A/1B knockout mouse model. Drug Metab Dispos 2005, 33:165-174.
18. Glavinas H., Krajcsi P., Cserepes J., Sarkadi B. The role of ABC transporters in drug resistance, metabolism and toxicity. Curr Drug Deliv 2004, 1:27-42.
19. Huls M., Russel F.G., Masereeuw R. The role of ATP binding cassette transporters in tissue defense and organ regeneration. J Pharmacol Exp Ther 2009, 328:3-9.
20. Szekeres T., Haushofer A. Clinical pharmacogenetics of immunosuppressive drugs in organ transplantation. Pharmacogenomics 2005, 6:163-168.
21. Choudhuri S., Klaassen C.D. Structure, function, expression, genomic organization, and single nucleotide polymorphisms of human ABCB1 (MDR1), ABCC (MRP), and ABCG2 (BCRP) efflux transporters. Int J Toxicol 2006, 25:231-259.
22. Paulusma C.C., Bosma P.J., Zaman G.J., et al. Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science 1996, 271:1126-1128.
23. Buchler M., Konig J., Brom M., et al. cDNA cloning of the hepatocyte canalicular isoform of the multidrug resistance protein, cMrp, reveals a novel conjugate export pump deficient in hyperbilirubinemic mutant rats. J Biol Chem 1996, 271:15091-15098.
24. Chan L.M., Lowes S., Hirst B.H. The ABCs of drug transport in intestine and liver: efflux proteins limiting drug absorption and bioavailability. Eur J Pharm Sci 2004, 21:25-51.
25. Kruh G.D., Belinsky M.G. The MRP family of drug efflux pumps. Oncogene 2003, 22:7537-7552.
26. Jedlitschky G., Hoffmann U., Kroemer H.K. Structure and function of the MRP2 (ABCC2) protein and its role in drug disposition. Expert Opin Drug Metab Toxicol 2006, 2:351-366.
27. Schaub T.P., Kartenbeck J., Konig J., et al. Expression of the MRP2 gene-encoded conjugate export pump in human kidney proximal tubules and in renal cell carcinoma. J Am Soc Nephrol 1999, 10:1159-1169.
28. Dietrich C.G., Geier A., Oude Elferink R.P. ABC of oral bioavailability: transporters as gatekeepers in the gut. Gut Gut 2003, 52:1788-1795.
29. Oselin K., Mrozikiewicz P.M., Pahkla R., Roots I. Quantitative determination of the human MRP1 and MRP2 mRNA expression in FACS-sorted peripheral blood CD4+, CD8+, CD19+, and CD56+ cells. Eur J Haematol 2003, 71:119-123.
30. Akita H., Suzuki H., Ito K., et al. Characterization of bile acid transport mediated by multidrug resistance associated protein 2 and bile salt export pump. Biochim Biophys Acta 2001, 1511:7-16.
31. Keitel V., Nies A.T., Brom M., Hummel-Eisenbeiss J., Spring H., Keppler D. A common Dubin-Johnson syndrome mutation impairs protein maturation and transport activity of MRP2 (ABCC2). Am J Physiol Gastrointest Liver Physiol 2003, 284:G165-G174.
32. Konig J., Nies A.T., Cui Y., Leier I., Keppler D. Conjugate export pumps of the multidrug resistance protein (MRP) family: localization, substrate specificity, and MRP2-mediated drug resistance. Biochim Biophys Acta 1999, 1461:377-394.
33. Naruhashi K., Tamai I., Inoue N., et al. Involvement of multidrug resistance-associated protein 2 in intestinal secretion of grepafloxacin in rats. Antimicrob Agents Chemother 2002, 46:344-349.
34. Suzuki H., Sugiyama Y. Role of metabolic enzymes and efflux transporters in the absorption of drugs from the small intestine. Eur J Pharm Sci 2000, 12:3-12.
35. Hesselink D.A., van Hest R.M., Mathot R.A., et al. Cyclosporine interacts with mycophenolic acid by inhibiting the multidrug resistance-associated protein 2. Am J Transplant 2005, 5:987-994.
36. Kobayashi M., Saitoh H., Tadano K., Takahashi Y., Hirano T. Cyclosporin A, but not tacrolimus, inhibits the biliary excretion of mycophenolic acid glucuronide possibly mediated by multidrug resistance-associated protein 2 in rats. J Pharmacol Exp Ther 2004, 309:1029-1035.
37. Kamisako T., Leier I., Cui Y., et al. Transport of monoglucuronosyl and bisglucuronosyl bilirubin by recombinant human and rat multidrug resistance protein 2. Hepatology 1999, 30:485-490.
38. Chen Z.S., Kawabe T., Ono M., et al. Effect of multidrug resistance-reversing agents on transporting activity of human canalicular multispecific organic anion transporter. Mol Pharmacol 1999, 56:1219-1228.
39. Kroetz D.L., Pauli-Magnus C., Hodges L.M., et al. Sequence diversity and haplotype structure in the human ABCB1 (MDR1, multidrug resistance transporter) gene. Pharmacogenetics 2003, 13:481-494.
40. Pauli-Magnus C., Kroetz D.L. Functional implications of genetic polymorphisms in the multidrug resistance gene MDR1 (ABCB1). Pharm Res 2004, 21:904-913.
41. Kimchi-Sarfaty C., Marple A.H., Shinar S., et al. Ethnicity-related polymorphisms and haplotypes in the human ABCB1 gene. Pharmacogenomics 2007, 8:29-39.
42. Hoffmeyer S., Burk O., von Richter O., et al. Functional polymorphisms of the human multidrug-resistance gene: multiple sequence variations and correlation of one allele with P-glycoprotein expression and activity in vivo. Proc Natl Acad Sci U S A 2000, 97:3473-3478.
43. Wang D., Johnson A.D., Papp A.C., Kroetz D.L., Sadee W. Multidrug resistance polypeptide 1 (MDR1, ABCB1) variant 3435 C>T affects mRNA stability. Pharmacogenet Genomics 2005, 15:693-704.
44. Kimchi-Sarfaty C., Oh J.M., Kim I.W., et al. A "silent" polymorphism in the MDR1 gene changes substrate specificity. Science 2007, 315:525-528.
45. Chinn L.W., Kroetz D.L. ABCB1 pharmacogenetics: progress, pitfalls, and promise. Clin Pharmacol Ther 2007, 81:265-269.
46. Itoda M., Saito Y., Soyama A., et al. Polymorphisms in the ABCC2 (cMOAT/MRP2) gene found in 72 established cell lines derived from Japanese individuals: an association between single nucleotide polymorphisms in the 5'-untranslated region and exon 28. Drug Metab Dispos 2002, 30:363-364.
47. Haenisch S., May K., Wegner D., Caliebe A., Cascorbi I., Siegmund W. Influence of genetic polymorphisms on intestinal expression and rifampicin-type induction of ABCC2 and on bioavailability of talinolol. Pharmacogenet Genomics 2008, 18:357-365.
48. Ito S., Ieiri I., Tanabe M., Suzuki A., Higuchi S., Otsubo K. Polymorphism of the ABC transporter genes, MDR1, MRP1 and MRP2/cMOAT, in healthy Japanese subjects. Pharmacogenetics 2001, 11:175-184.
49. Suzuki H., Sugiyama Y. Single nucleotide polymorphisms in multidrug resistance associated protein 2 (MRP2/ABCC2): its impact on drug disposition. Adv Drug Deliv Rev 2002, 54:1311-1331.
50. 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 2007, 7:56-65.
51. Hirouchi M., Suzuki H., Itoda M., et al. Characterization of the cellular localization, expression level, and function of SNP variants of MRP2/ABCC2. Pharm Res 2004, 21:742-748.
52. Foote C.J., Greer W., Kiberd B.A., et al. MDR1 C3435T polymorphisms correlate with cyclosporine levels in de novo renal recipients. Transplant Proc 2006, 38:2847-2849.
53. Hesselink D.A., van Gelder T., van Schaik R.H., et al. 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.
54. Bouamar R., Hesselink D.A., van Schaik R.H., et al. Polymorphisms in CYP3A5, CYP3A4, and ABCB1 are not associated with cyclosporine pharmacokinetics nor with cyclosporine clinical end points after renal transplantation. Ther Drug Monit 2011, 33:178-184.
55. Fanta S., Niemi M., Jonsson S., et al. Pharmacogenetics of cyclosporine in children suggests an age-dependent influence of ABCB1 polymorphisms. Pharmacogenet Genomics 2008, 18:77-90.
56. 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.
57. Qiu X.Y., Jiao Z., Zhang M., et al. 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.
58. Anglicheau D., Verstuyft C., Laurent-Puig P., et al. Association of the multidrug resistance-1 gene single-nucleotide polymorphisms with the tacrolimus dose requirements in renal transplant recipients. J Am Soc Nephrol 2003, 14:1889-1896.
59. Fredericks S., Moreton M., Reboux S., et al. Multidrug resistance gene-1 (MDR-1) haplotypes have a minor influence on tacrolimus dose requirements. Transplantation 2006, 82:705-708.
60. MacPhee I.A., Fredericks S., Tai T., et al. The influence of pharmacogenetics on the time to achieve target tacrolimus concentrations after kidney transplantation. Am J Transplant 2004, 4:914-919.
61. Zheng H., Webber S., Zeevi A., et al. Tacrolimus dosing in pediatric heart transplant patients is related to CYP3A5 and MDR1 gene polymorphisms. Am J Transplant 2003, 3:477-483.
62. Hesselink D.A., van Schaik R.H., van Agteren M., et al. CYP3A5 genotype is not associated with a higher risk of acute rejection in tacrolimus-treated renal transplant recipients. Pharmacogenet Genomics 2008, 18:339-348.
63. Wei-lin W., Jing J., Shu-sen Z., et al. Tacrolimus dose requirement in relation to donor and recipient ABCB1 and CYP3A5 gene polymorphisms in Chinese liver transplant patients. Liver Transpl 2006, 12:775-780.
64. Bonhomme-Faivre L., Picard V., Saliba F., et al. Effect of the ABCB1 3435 C>T polymorphism on tacrolimus concentrations and dosage requirements in liver transplant recipients. Am J Health Syst Pharm 2009, 66:1645-1651.
65. Jiang Z.P., Wang Y.R., Xu P., Liu R.R., Zhao X.L., Chen F.P. Meta-analysis of the effect of MDR1 C3435T polymorphism on cyclosporine pharmacokinetics. Basic Clin Pharmacol Toxicol 2008, 103:433-444.
66. Staatz C.E., Goodman L.K., Tett S.E. Effect of CYP3A and ABCB1 single nucleotide polymorphisms on the pharmacokinetics and pharmacodynamics of calcineurin inhibitors: Part I. Clin Pharmacokinet 2010, 49:141-175.
67. Renders L., Frisman M., Ufer M., et al. CYP3A5 genotype markedly influences the pharmacokinetics of tacrolimus and sirolimus in kidney transplant recipients. Clin Pharmacol Ther 2007, 81:228-234.
68. Zhao W., Elie V., Roussey G., et al. Population pharmacokinetics and pharmacogenetics of tacrolimus in de novo pediatric kidney transplant recipients. Clin Pharmacol Ther 2009, 86:609-618.
69. Monchaud C., Marquet P. Pharmacokinetic optimization of immunosuppressive therapy in thoracic transplantation: part II. Clin Pharmacokinet 2009, 48:489-516.
70. Crowe A., Lemaire M. In vitro and in situ absorption of SDZ-RAD using a human intestinal cell line (Caco-2) and a single pass perfusion model in rats: comparison with rapamycin. Pharm Res 1998, 15:1666-1672.
71. Anglicheau D., Le Corre D., Lechaton S., et al. Consequences of genetic polymorphisms for sirolimus requirements after renal transplant in patients on primary sirolimus therapy. Am J Transplant 2005, 5:595-603.
72. Miao L.Y., Huang C.R., Hou J.Q., Qian M.Y. Association study of ABCB1 and CYP3A5 gene polymorphisms with sirolimus trough concentration and dose requirements in Chinese renal transplant recipients. Biopharm Drug Dispos 2008, 29:1-5.
73. Mourad M., Mourad G., Wallemacq P., et al. 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.
74. Naesens M., Kuypers D.R., Verbeke K., Vanrenterghem Y. Multidrug resistance protein 2 genetic polymorphisms influence mycophenolic acid exposure in renal allograft recipients. Transplantation 2006, 82:1074-1084.
75. Grinyo J.M., Ekberg H., Mamelok R.D., et al. The pharmacokinetics of mycophenolate mofetil in renal transplant recipients receiving standard-dose or low-dose cyclosporine, low-dose tacrolimus or low-dose sirolimus: the Symphony Pharmacokinetic Substudy. Nephrol Dial Transplant 2009, 24:2269-2276.
76. Kuypers D.R., Ekberg H., Grinyo J., et al. Mycophenolic acid exposure after administration of mycophenolate mofetil in the presence and absence of cyclosporin in renal transplant recipients. Clin Pharmacokinet 2009, 48:329-341.
77. Lloberas N., Torras J., Cruzado J.M., et al. Influence of MRP2 on MPA pharmacokinetics in renal transplant recipients-results of the Pharmacogenomic Substudy within the Symphony Study. Nephrol Dial Transplant 2011.
78. Zhang W.X., Chen B., Jin Z., et al. Influence of uridine diphosphate (UDP)-glucuronosyltransferases and ABCC2 genetic polymorphisms on the pharmacokinetics of mycophenolic acid and its metabolites in Chinese renal transplant recipients. Xenobiotica 2008, 38:1422-1436.
79. Levesque E., Benoit-Biancamano M.O., Delage R., Couture F., Guillemette C. Pharmacokinetics of mycophenolate mofetil and its glucuronide metabolites in healthy volunteers. Pharmacogenomics 2008, 9:869-879.
80. Miura M., Kagaya H., Satoh S., et al. Influence of drug transporters and UGT polymorphisms on pharmacokinetics of phenolic glucuronide metabolite of mycophenolic acid in Japanese renal transplant recipients. Ther Drug Monit 2008, 30:559-564.
81. van Schaik R.H., van Agteren M., de Fijter J.W., et al. UGT1A9-275 T>A/-2152 C>T polymorphisms correlate with low MPA exposure and acute rejection in MMF/tacrolimus-treated kidney transplant patients. Clin Pharmacol Ther 2009, 86:319-327.
82. Sawamoto T., Van Gelder T., Christians U., Okamura N., Jacobsen W., Benet L. Membrane transport of mycophenolate mofetil and its active metabolite, mycophenolic acid in MDCK and MDR1-MDCK cell monolayers. J Heart Lung Transplant 2001, 20:234-235.
83. Wang J., Figurski M., Shaw L.M., Burckart G.J. The impact of P-glycoprotein and Mrp2 on mycophenolic acid levels in mice. Transpl Immunol 2008, 19:192-196.
84. Joy M.S., Boyette T., Hu Y., et al. Effects of uridine diphosphate glucuronosyltransferase 2B7 and 1A7 pharmacogenomics and patient clinical parameters on steady-state mycophenolic acid pharmacokinetics in glomerulonephritis. Eur J Clin Pharmacol 2010, 66:1119-1130.
85. Lo A., Burckart G.J. P-glycoprotein and drug therapy in organ transplantation. J Clin Pharmacol 1999, 39:995-1005.
86. Zanker B., Barth C., Stachowski J., Baldamus C.A., Land W. Multidrug resistance gene MDR1 expression: a gene transfection in vitro model and clinical analysis in cyclosporine-treated patients rejecting their renal grafts. Transplant Proc 1997, 29:1507-1508.
87. Melk A., Daniel V., Weimer R., et al. P-glycoprotein expression is not a useful predictor of acute or chronic kidney graft rejection. Transpl Int 1999, 12:10-17.
88. Zheng H.X., Zeevi A., McCurry K., et al. The impact of pharmacogenomic factors on acute persistent rejection in adult lung transplant patients. Transpl Immunol 2005, 14:37-42.
89. Barnard J.B., Richardson S., Sheldon S., et al. The MDR1/ABCB1 gene, a high-impact risk factor for cardiac transplant rejection. Transplantation 2006, 82:1677-1682.
90. Elens L., Capron A., Kerckhove V.V., et al. 1199 G>A and 2677 G>T/A polymorphisms of ABCB1 independently affect tacrolimus concentration in hepatic tissue after liver transplantation. Pharmacogenet Genomics 2007, 17:873-883.
91. Grinyo J., Vanrenterghem Y., Nashan B., et al. Association of four DNA polymorphisms with acute rejection after kidney transplantation. Transpl Int 2008, 21:879-891.
92. Kuypers D.R., 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.
93. Roy J.N., 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.
94. Quteineh L., Verstuyft C., Furlan V., et al. Influence of CYP3A5 genetic polymorphism on tacrolimus daily dose requirements and acute rejection in renal graft recipients. Basic Clin Pharmacol Toxicol 2008, 103:546-552.
95. Cattaneo D., Ruggenenti P., Baldelli S., et al. ABCB1 genotypes predict cyclosporine-related adverse events and kidney allograft outcome. J Am Soc Nephrol 2009, 20:1404-1415.
96. Min S.I., Kim S.Y., Ahn S.H., et al. CYP3A5 *1 allele: impacts on early acute rejection and graft function in tacrolimus-based renal transplant recipients. Transplantation 2010, 90:1394-1400.
97. von Ahsen N., Richter M., Grupp C., Ringe B., Oellerich M., Armstrong V.W. 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.
98. Taegtmeyer A.B., Breen J.B., Smith J., et al. ATP-binding cassette subfamily B member 1 polymorphisms do not determine cyclosporin exposure, acute rejection or nephrotoxicity after heart transplantation. Transplantation 2010, 89:75-82.
99. Le Meur Y., Buchler M., Thierry A., et al. Individualized mycophenolate mofetil dosing based on drug exposure significantly improves patient outcomes after renal transplantation. Am J Transplant 2007, 7:2496-2503.
100. Satoh S., Tada H., Murakami M., et al. Circadian pharmacokinetics of mycophenolic acid and implication of genetic polymorphisms for early clinical events in renal transplant recipients. Transplantation 2006, 82:486-493.
101. van Gelder T., Silva H.T., de Fijter J.W., et al. Comparing mycophenolate mofetil regimens for de novo renal transplant recipients: the fixed-dose concentration-controlled trial. Transplantation 2008, 86:1043-1051.
102. Michelon H., Konig J., Durrbach A., et al. SLCO1B1 genetic polymorphism influences mycophenolic acid tolerance in renal transplant recipients. Pharmacogenomics 2010, 11:1703-1713.
103. Hesselink D.A., Bouamar R., van Gelder T. The pharmacogenetics of calcineurin inhibitor-related nephrotoxicity. Ther Drug Monit 2010, 32:387-393.
104. Naesens M., Kuypers D.R., Sarwal M. Calcineurin inhibitor nephrotoxicity. Clin J Am Soc Nephrol 2009, 4:481-508.
105. Garcia del Moral R., O'Valle F., Andujar M., et al. Relationship between P-glycoprotein expression and cyclosporin A in kidney. An immunohistological and cell culture study. Am J Pathol 1995, 146:398-408.
106. Garcia del Moral R., Olmo A., Osuna A., et al. Role of P-glycoprotein in chronic cyclosporine nephrotoxicity and its relationship to intrarenal angiotensin II deposits. Transplant Proc 1998, 30:2014-2016.
107. Joy M.S., Nickeleit V., Hogan S.L., Thompson B.D., Finn W.F. Calcineurin inhibitor-induced nephrotoxicity and renal expression of P-glycoprotein. Pharmacotherapy 2005, 25:779-789.
108. Hauser I.A., Schaeffeler E., Gauer S., et al. 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.
109. Hawwa A.F., McKiernan P.J., Shields M., Millership J.S., Collier P.S., McElnay J.C. Influence of ABCB1 polymorphisms and haplotypes on tacrolimus nephrotoxicity and dosage requirements in children with liver transplant. Br J Clin Pharmacol 2009, 68:413-421.
110. Hebert M.F., Dowling A.L., Gierwatowski C., et al. Association between ABCB1 (multidrug resistance transporter) genotype and post-liver transplantation renal dysfunction in patients receiving calcineurin inhibitors. Pharmacogenetics 2003, 13:661-674.
111. Klauke B., Wirth A., Zittermann A., et al. No association between single nucleotide polymorphisms and the development of nephrotoxicity after orthotopic heart transplantation. J Heart Lung Transplant 2008, 27:741-745.
112. Chapman J.R., O'Connell P.J., Nankivell B.J. Chronic renal allograft dysfunction. J Am Soc Nephrol 2005, 16:3015-3026.
113. Woillard J.B., Rerolle J.P., Picard N., et al. 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.
114. Woillard J.B., Rerolle J.P., Picard N., et al. Risk of diarrhoea in a long-term cohort of renal transplant patients given mycophenolate mofetil: the significant role of the UGT1A8 2 variant allele. Br J Clin Pharmacol 2010, 69:675-683.
115. Knoll G.A., MacDonald I., Khan A., Van Walraven C. Mycophenolate mofetil dose reduction and the risk of acute rejection after renal transplantation. J Am Soc Nephrol 2003, 14:2381-2386.
116. Maes B.D., Dalle I., Geboes K., et al. Erosive enterocolitis in mycophenolate mofetil-treated renal-transplant recipients with persistent afebrile diarrhea. Transplantation 2003, 75:665-672.
117. Heller T., van Gelder T., Budde K., et al. Plasma concentrations of mycophenolic acid acyl glucuronide are not associated with diarrhea in renal transplant recipients. Am J Transplant 2007, 7:1822-1831.
118. Hesselink D.A., van Gelder T. Genetic and nongenetic determinants of between-patient variability in the pharmacokinetics of mycophenolic acid. Clin Pharmacol Ther 2005, 78:317-321.
119. Ohmann E.L., Burckart G.J., Brooks M.M., et al. Genetic polymorphisms influence mycophenolate mofetil-related adverse events in pediatric heart transplant patients. J Heart Lung Transplant 2010, 29:509-516.
120. Miura M., Satoh S., Inoue K., et al. Influence of SLCO1B1, 1B3, 2B1 and ABCC2 genetic polymorphisms on mycophenolic acid pharmacokinetics in Japanese renal transplant recipients. Eur J Clin Pharmacol 2007, 63:1161-1169.
121. Yang J.W., Lee P.H., Hutchinson I.V., Pravica V., Shah T., Min D.I. Genetic polymorphisms of MRP2 and UGT2B7 and gastrointestinal symptoms in renal transplant recipients taking mycophenolic acid. Ther Drug Monit 2009, 31:542-548.
122. Jacobson P.A., Schladt D., Oetting W.S., et al. Genetic determinants of mycophenolate-related anemia and leukopenia after transplantation. Transplantation 2011, 91:309-316.
123. Kahan B. Toxicity spectrum of inhibitors of mammalian target of rapamycin in organ transplantation: etiology, pathogenesis and treatment. Expert Opin Drug Saf 2011.
124. Yamauchi A., Ieiri I., Kataoka Y., et al. Neurotoxicity induced by tacrolimus after liver transplantation: relation to genetic polymorphisms of the ABCB1 (MDR1) gene. Transplantation 2002, 74:571-572.
125. Vincenti F. A decade of progress in kidney transplantation. Transplantation 2004, 77:S52-S61.
126. Davidson J., Wilkinson A., Dantal J., et al. New-onset diabetes after transplantation: 2003 International consensus guidelines. Proceedings of an international expert panel meeting. Barcelona, Spain, 19 February 2003. Transplantation 2003, 75:SS3-24.
127. Numakura K., Satoh S., Tsuchiya N., et al. Clinical and genetic risk factors for posttransplant diabetes mellitus in adult renal transplant recipients treated with tacrolimus. Transplantation 2005, 80:1419-1424.
128. Plaumann S., Blume R., Borchers S., Steinfelder H.J., Knepel W., Oetjen E. Activation of the dual-leucine-zipper-bearing kinase and induction of beta-cell apoptosis by the immunosuppressive drug cyclosporin A. Mol Pharmacol 2008, 73:652-659.
129. Kutkuhn B., Hollenbeck M., Heering P., et al. Development of insulin resistance and elevated blood pressure during therapy with cyclosporine A. Blood Press 1997, 6:13-17.
130. Capron A., Mourad M., De Meyer M., et al. CYP3A5 and ABCB1 polymorphisms influence tacrolimus concentrations in peripheral blood mononuclear cells after renal transplantation. Pharmacogenomics 2010, 11:703-714.
131. Capron A., Musuamba F., Latinne D., et al. Validation of a liquid chromatography-mass spectrometric assay for tacrolimus in peripheral blood mononuclear cells. Ther Drug Monit 2009, 31:178-186.
132. Crettol S., Venetz J.P., Fontana M., et al. Influence of ABCB1 genetic polymorphisms on cyclosporine intracellular concentration in transplant recipients. Pharmacogenet Genomics 2008, 18:307-315.
133. Falck P., Asberg A., Guldseth H., et al. Declining intracellular T-lymphocyte concentration of cyclosporine a precedes acute rejection in kidney transplant recipients. Transplantation 2008, 85:179-184.
134. Hitzl M., Drescher S., van der Kuip H., et al. The C3435T mutation in the human MDR1 gene is associated with altered efflux of the P-glycoprotein substrate rhodamine 123 from CD56+ natural killer cells. Pharmacogenetics 2001, 11:293-298.
135. Clase C.M., Mahalati K., Kiberd B.A., et al. Adequate early cyclosporin exposure is critical to prevent renal allograft rejection: patients monitored by absorption profiling. Am J Transplant 2002, 2:789-795.
136. Macphee I.A. Use of pharmacogenetics to optimize immunosuppressive therapy. Ther Drug Monit 2010, 32:261-264.
137. Undre N.A., van Hooff J., Christiaans M., et al. Low systemic exposure to tacrolimus correlates with acute rejection. Transplant Proc 1999, 31:296-298.
138. Thervet E., Loriot M.A., Barbier S., et al. Optimization of initial tacrolimus dose using pharmacogenetic testing. Clin Pharmacol Ther 2010, 87:721-726.
139. van Gelder T., Hesselink D.A. Dosing tacrolimus based on CYP3A5 genotype: will it improve clinical outcome?. Clin Pharmacol Ther 2010, 87:640-641.