Drug-Cytokine Interactions

  • Kerry B. Goralski
  • Matthew A. Ladda
  • Jenna O. McNeil
Chapter
Part of the Infectious Disease book series (ID)

Abstract

There are many documented examples of altered drug disposition in human conditions that stimulate host cytokine responses. These include viral, bacterial, or parasitic infections, tissue injury, surgery, cancer, and autoimmune conditions. Interferons, interleukins 1 and 6, and tumor necrosis factor are the central mediators. These cytokines have been traditionally viewed with respect to their ability to suppress hepatic cytochrome P450 (CYP)-mediated drug detoxification. The potential result is a temporary conversion from a rapid or normal metabolizer to a poor metabolizer phenotype. Such aberrant drug handling has placed patients at risk for adverse drug responses to low therapeutic index, CYP-metabolized drugs like theophylline. It is now evident that drug-cytokine interactions are broader than once appreciated. They impact CYPs and drug transporter proteins ABCB1 (P-glycoprotein) in the liver, intestine, kidney, blood-brain barrier, placenta, and immune cells. Furthermore, the possibility that anti-cytokine biological therapies may precipitate drug-cytokine interactions is gaining increasing recognition. The consequences of drug-cytokine interactions are altered absorption, elimination, and/or cellular and tissue distribution of drugs. The outcomes can be negative or positive depending on the drug, the anatomical site of the interaction, and the therapeutic objectives. This chapter provides a historical overview of drug-cytokine interactions, discusses recent advances, and examines the clinical scenarios in which infections or inflammation might lead to abnormal drug handling and drug responses.

Keywords

Interleukins Interferons Inflammatory Bowel Disease Cancer Autoimmune Vaccines Immunosuppression Surgery Placenta Tumor Necrosis Factor 

References

  1. 1.
    Brooks MH, Malloy JP, Bartelloni PJ, Sheehy TW, Barry KG (1969) Quinine, pyrimethamine, and sulphorthodimethoxine: clinical response, plasma levels, and urinary excretion during the initial attack of naturally acquired falciparum malaria. Clin Pharmacol Ther 10(1):85–91PubMedGoogle Scholar
  2. 2.
    Place VA, Pyle MM, De la Huerga J (1969) Ethambutol in tuberculous meningitis. Am Rev Respir Dis 99(5):783–785PubMedGoogle Scholar
  3. 3.
    Sippel JE, Mikhail IA, Girgis NI, Youssef HH (1974) Rifampin concentrations in cerebrospinal fluid of patients with tuberculous meningitis. Am Rev Respir Dis 109(5):579–580PubMedGoogle Scholar
  4. 4.
    Renton KW, Mannering GJ (1976) Depression of hepatic cytochrome P-450-dependent monooxygenase systems with administered interferon inducing agents. Biochem Biophys Res Commun 73(2):343–348PubMedGoogle Scholar
  5. 5.
    Renton KW, Mannering GJ (1976) Depression of the hepatic cytochrome P-450 mono-oxygenase system by administered tilorone (2,7-bis(2-(diethylamino)ethoxy)fluoren-9-one dihydrochloride). Drug Metab Dispos 4(3):223–231PubMedGoogle Scholar
  6. 6.
    Soyka LF, Hunt WG, Knight SE, Foster RS Jr (1976) Decreased liver and lung drug-metabolizing activity in mice treated with Corynebacterium parvum. Cancer Res 36(12):4425–4428PubMedGoogle Scholar
  7. 7.
    Cressman AM, Petrovic V, Piquette-Miller M (2012) Inflammation-mediated changes in drug transporter expression/activity: implications for therapeutic drug response. Expert Rev Clin Pharmacol 5(1):69–89.  https://doi.org/10.1586/ecp.11.66 CrossRefPubMedGoogle Scholar
  8. 8.
    Petrovic V, Teng S, Piquette-Miller M (2007) Regulation of drug transporters during infection and inflammation. Mol Interv 7(2):99–111PubMedGoogle Scholar
  9. 9.
    Gonzalez-Gay MA, Gonzalez-Juanatey C, Vazquez-Rodriguez TR, Miranda-Filloy JA, Llorca J (2010) Insulin resistance in rheumatoid arthritis: the impact of the anti-TNF-alpha therapy. Ann N Y Acad Sci 1193(1):153–159.  https://doi.org/10.1111/j.1749-6632.2009.05287.x. NYAS5287 [pii]CrossRefPubMedGoogle Scholar
  10. 10.
    Sugimoto M, Furuta T, Yamaoka Y (2009) Influence of inflammatory cytokine polymorphisms on eradication rates of Helicobacter pylori. J Gastroenterol Hepatol 24(11):1725–1732.  https://doi.org/10.1111/j.1440-1746.2009.06047.x. JGH6047 [pii]CrossRefPubMedCentralPubMedGoogle Scholar
  11. 11.
    Petrovic V, Kojovic D, Cressman A, Piquette-Miller M (2015) Maternal bacterial infections impact expression of drug transporters in human placenta. Int Immunopharmacol 26(2):349–356.  https://doi.org/10.1016/j.intimp.2015.04.020 CrossRefPubMedGoogle Scholar
  12. 12.
    Miller DS (2015) Regulation of ABC transporters blood-brain barrier: the good, the bad, and the ugly. Adv Cancer Res 125:43–70.  https://doi.org/10.1016/bs.acr.2014.10.002 CrossRefPubMedGoogle Scholar
  13. 13.
    Roberts DJ, Goralski KB (2008) A critical overview of the influence of inflammation and infection on P-glycoprotein expression and activity in the brain. Expert Opin Drug Metab Toxicol 4(10):1245–1264PubMedGoogle Scholar
  14. 14.
    Goralski KB, Hartmann G, Piquette-Miller M, Renton KW (2003) Downregulation of mdr1a expression in the brain and liver during CNS inflammation alters the in vivo disposition of digoxin. Br J Pharmacol 139(1):35–48PubMedCentralPubMedGoogle Scholar
  15. 15.
    DX X, Wang JP, Sun MF, Chen YH, Wei W (2006) Lipopolysaccharide downregulates the expressions of intestinal pregnane X receptor and cytochrome P450 3a11. Eur J Pharmacol 536(1–2):162–170.  https://doi.org/10.1016/j.ejphar.2006.02.029. S0014-2999(06)00197-X [pii]CrossRefGoogle Scholar
  16. 16.
    Kalitsky-Szirtes J, Shayeganpour A, Brocks DR, Piquette-Miller M (2004) Suppression of drug-metabolizing enzymes and efflux transporters in the intestine of endotoxin-treated rats. Drug Metab Dispos 32(1):20–27.  https://doi.org/10.1124/dmd.32.1.20. 32/1/20 [pii]CrossRefPubMedGoogle Scholar
  17. 17.
    Heemskerk S, Peters JG, Louisse J, Sagar S, Russel FG, Masereeuw R (2010) Regulation of P-glycoprotein in renal proximal tubule epithelial cells by LPS and TNF-alpha. J Biomed Biotechnol 2010:525180.  https://doi.org/10.1155/2010/525180 CrossRefPubMedCentralPubMedGoogle Scholar
  18. 18.
    Sharma R, Kacevska M, London R, Clarke SJ, Liddle C, Robertson G (2008) Downregulation of drug transport and metabolism in mice bearing extra-hepatic malignancies. Br J Cancer 98(1):91–97.  https://doi.org/10.1038/Sj.Bjc.6604101 CrossRefPubMedGoogle Scholar
  19. 19.
    Long TJ, Cosgrove PA, Dunn RT 2nd, Stolz DB, Hamadeh H, Afshari C, McBride H, Griffith LG (2016) Modeling therapeutic antibody-small molecule drug-drug interactions using a three-dimensional perfusable human liver coculture platform. Drug Metab Dispos 44(12):1940–1948.  https://doi.org/10.1124/dmd.116.071456 CrossRefPubMedCentralPubMedGoogle Scholar
  20. 20.
    Harvey RD, Morgan ET (2014) Cancer, inflammation, and therapy: effects on cytochrome p450-mediated drug metabolism and implications for novel immunotherapeutic agents. Clin Pharmacol Ther 96(4):449–457.  https://doi.org/10.1038/clpt.2014.143 CrossRefPubMedGoogle Scholar
  21. 21.
    Morgan ET, Goralski KB, Piquette-Miller M, Renton KW, Robertson GR, Chaluvadi MR, Charles KA, Clarke SJ, Kacevska M, Liddle C, Richardson TA, Sharma R, Sinal CJ (2008) Regulation of drug-metabolizing enzymes and transporters in infection, inflammation, and cancer. Drug Metab Dispos 36(2):205–216PubMedGoogle Scholar
  22. 22.
    Renton KW (2005) Regulation of drug metabolism and disposition during inflammation and infection. Expert Opin Drug Metab Toxicol 1(4):629–640PubMedGoogle Scholar
  23. 23.
    Aitken AE, Morgan ET (2007) Gene-specific effects of inflammatory cytokines on cytochrome P450 2C, 2B6 and 3A4 mRNA levels in human hepatocytes. Drug Metab Dispos 35(9):1687–1693.  https://doi.org/10.1124/dmd.107.015511. dmd.107.015511 [pii]CrossRefPubMedCentralPubMedGoogle Scholar
  24. 24.
    Bauer B, Hartz AM, Miller DS (2007) Tumor necrosis factor alpha and endothelin-1 increase P-glycoprotein expression and transport activity at the blood-brain barrier. Mol Pharmacol 71(3):667–675PubMedGoogle Scholar
  25. 25.
    Donato MT, Guillen MI, Jover R, Castell JV, Gomez-Lechon MJ (1997) Nitric oxide-mediated inhibition of cytochrome P450 by interferon-gamma in human hepatocytes. J Pharmacol Exp Ther 281(1):484–490PubMedGoogle Scholar
  26. 26.
    Hartz AM, Bauer B, Fricker G, Miller DS (2006) Rapid modulation of P-glycoprotein-mediated transport at the blood-brain barrier by tumor necrosis factor-alpha and lipopolysaccharide. Mol Pharmacol 69(2):462–470PubMedGoogle Scholar
  27. 27.
    Kim RB (2006) Transporters and drug discovery: why, when, and how. Mol Pharm 3(1):26–32PubMedGoogle Scholar
  28. 28.
    Petzinger E, Geyer J (2006) Drug transporters in pharmacokinetics. Naunyn Schmiedeberg’s Arch Pharmacol 372(6):465–475Google Scholar
  29. 29.
    Anzenbacher P, Anzenbacherova E (2001) Cytochromes P450 and metabolism of xenobiotics. Cell Mol Life Sci 58(5–6):737–747PubMedGoogle Scholar
  30. 30.
    Ramirez-Alcantara V, Montrose MH (2014) Acute murine colitis reduces colonic 5-aminosalicylic acid metabolism by regulation of N-acetyltransferase-2. Am J Physiol Gastrointest Liver Physiol 306(11):G1002–G1010.  https://doi.org/10.1152/ajpgi.00389.2013 CrossRefPubMedCentralPubMedGoogle Scholar
  31. 31.
    Richardson TA, Sherman M, Kalman D, Morgan ET (2006) Expression of UDP-glucuronosyltransferase isoform mRNAs during inflammation and infection in mouse liver and kidney. Drug Metab Dispos 34(3):351–353.  https://doi.org/10.1124/dmd.105.007435 CrossRefPubMedGoogle Scholar
  32. 32.
    Mimche SM, Nyagode BA, Merrell MD, Lee CM, Prasanphanich NS, Cummings RD, Morgan ET (2014) Hepatic cytochrome P450s, phase II enzymes and nuclear receptors are downregulated in a Th2 environment during Schistosoma mansoni infection. Drug Metab Dispos 42(1):134–140.  https://doi.org/10.1124/dmd.113.054957 CrossRefPubMedCentralPubMedGoogle Scholar
  33. 33.
    Chen C, Han YH, Yang Z, Rodrigues AD (2011) Effect of interferon-alpha2b on the expression of various drug-metabolizing enzymes and transporters in co-cultures of freshly prepared human primary hepatocytes. Xenobiotica 41(6):476–485.  https://doi.org/10.3109/00498254.2011.560971 CrossRefPubMedGoogle Scholar
  34. 34.
    International Transporter C, Giacomini KM, Huang SM, Tweedie DJ, Benet LZ, Brouwer KL, Chu X, Dahlin A, Evers R, Fischer V, Hillgren KM, Hoffmaster KA, Ishikawa T, Keppler D, Kim RB, Lee CA, Niemi M, Polli JW, Sugiyama Y, Swaan PW, Ware JA, Wright SH, Yee SW, Zamek-Gliszczynski MJ, Zhang L (2010) Membrane transporters in drug development. Nat Rev 9(3):215–236.  https://doi.org/10.1038/nrd3028 CrossRefGoogle Scholar
  35. 35.
    He L, Vasiliou K, Nebert DW (2009) Analysis and update of the human solute carrier (SLC) gene superfamily. Hum Genomics 3(2):195–206PubMedCentralPubMedGoogle Scholar
  36. 36.
    Vasiliou V, Vasiliou K, Nebert DW (2009) Human ATP-binding cassette (ABC) transporter family. Hum Genomics 3(3):281–290PubMedCentralPubMedGoogle Scholar
  37. 37.
    Dean M, Rzhetsky A, Allikmets R (2001) The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 11(7):1156–1166PubMedGoogle Scholar
  38. 38.
    Hediger MA, Romero MF, Peng JB, Rolfs A, Takanaga H, Bruford EA (2004) The ABCs of solute carriers: physiological, pathological and therapeutic implications of human membrane transport proteinsIntroduction. Pflugers Arch 447(5):465–468PubMedGoogle Scholar
  39. 39.
    Stieger B, Hagenbuch B (2014) Organic anion-transporting polypeptides. Curr Top Membr 73:205–232.  https://doi.org/10.1016/B978-0-12-800223-0.00005-0 CrossRefPubMedCentralPubMedGoogle Scholar
  40. 40.
    Koepsell H, Schmitt BM, Gorboulev V (2003) Organic cation transporters. Rev Physiol Biochem Pharmacol 150:36–90PubMedGoogle Scholar
  41. 41.
    Rizwan AN, Burckhardt G (2007) Organic anion transporters of the SLC22 family: biopharmaceutical, physiological, and pathological roles. Pharm Res 24(3):450–470PubMedGoogle Scholar
  42. 42.
    Tsuji A, Tamai I (1996) Carrier-mediated intestinal transport of drugs. Pharm Res 13(7):963–977PubMedGoogle Scholar
  43. 43.
    Yang CY, Dantzig AH, Pidgeon C (1999) Intestinal peptide transport systems and oral drug availability. Pharm Res 16(9):1331–1343PubMedGoogle Scholar
  44. 44.
    Tsuruoka S, Sugimoto KI, Fujimura A, Imai M, Asano Y, Muto S (2001) P-glycoprotein-mediated drug secretion in mouse proximal tubule perfused in vitro. J Am Soc Nephrol 12(1):177–181PubMedGoogle Scholar
  45. 45.
    van Asperen J, van Tellingen O, Beijnen JH (2000) The role of mdr1a P-glycoprotein in the biliary and intestinal secretion of doxorubicin and vinblastine in mice. Drug Metab Dispos 28(3):264–267PubMedGoogle Scholar
  46. 46.
    Schinkel AH, Smit JJ, van Tellingen O, Beijnen JH, Wagenaar E, van Deemter L, Mol CA, van der Valk MA, Robanus-Maandag EC, te Riele HP et al (1994) Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 77(4):491–502PubMedGoogle Scholar
  47. 47.
    Steinke JW, Borish L (2006) 3. Cytokines and chemokines. J Allergy Clin Immunol 117(2 Suppl Mini-Primer):S441–S445PubMedGoogle Scholar
  48. 48.
    Commins SP, Borish L, Steinke JW (2010) Immunologic messenger molecules: cytokines, interferons, and chemokines. J Allergy Clin Immunol 125(2 Suppl 2):S53–S72.  https://doi.org/10.1016/j.jaci.2009.07.008 CrossRefPubMedGoogle Scholar
  49. 49.
    Oppenheim JJ, Feldmann M (2000) Introduction to the role of cytokines in innate host defense and adaptive immunity. In: Oppenheim JJ, Feldmann M, Durum SK, Hirano T, Vilcek J, Nicola NA Cytokine reference: a compendium of cytokines and other mediators of host defense. Ligands., vol 1. 1st edn. Academic Press, San DiegoGoogle Scholar
  50. 50.
    Medzhitov R (2010) Inflammation 2010: new adventures of an old flame. Cell 140(6):771–776.  https://doi.org/10.1016/j.cell.2010.03.006 CrossRefPubMedGoogle Scholar
  51. 51.
    Medzhitov R (2008) Origin and physiological roles of inflammation. Nature 454(7203):428–435.  https://doi.org/10.1038/nature07201. nature07201 [pii]CrossRefPubMedGoogle Scholar
  52. 52.
    Barton GM (2008) A calculated response: control of inflammation by the innate immune system. J Clin Invest 118(2):413–420.  https://doi.org/10.1172/JCI34431 CrossRefPubMedCentralPubMedGoogle Scholar
  53. 53.
    Medzhitov R Inflammation (2010) New adventures of an old flame. Cell 140(6):771–776Google Scholar
  54. 54.
    Baumann H, Gauldie J (1994) The acute phase response. Immunol Today 15(2):74–80PubMedGoogle Scholar
  55. 55.
    Gruys E, Toussaint MJ, Niewold TA, Koopmans SJ (2005) Acute phase reaction and acute phase proteins. J Zhejiang Univ Sci B 6(11):1045–1056.  https://doi.org/10.1631/jzus.2005.B1045 CrossRefPubMedCentralPubMedGoogle Scholar
  56. 56.
    Ramadori G, Christ B (1999) Cytokines and the hepatic acute-phase response. Semin Liver Dis 19(2):141–155.  https://doi.org/10.1055/s-2007-1007106 CrossRefPubMedGoogle Scholar
  57. 57.
    Abdel-Razzak Z, Loyer P, Fautrel A, Gautier JC, Corcos L, Turlin B, Beaune P, Guillouzo A (1993) Cytokines down-regulate expression of major cytochrome P-450 enzymes in adult human hepatocytes in primary culture. Mol Pharmacol 44(4):707–715PubMedGoogle Scholar
  58. 58.
    Le Vee M, Gripon P, Stieger B, Fardel O (2008) Down-regulation of organic anion transporter expression in human hepatocytes exposed to the proinflammatory cytokine interleukin 1beta. Drug Metab Dispos 36(2):217–222.  https://doi.org/10.1124/dmd.107.016907. dmd.107.016907 [pii]CrossRefPubMedGoogle Scholar
  59. 59.
    Vee ML, Lecureur V, Stieger B, Fardel O (2009) Regulation of drug transporter expression in human hepatocytes exposed to the proinflammatory cytokines tumor necrosis factor-alpha or interleukin-6. Drug Metab Dispos 37(3):685–693.  https://doi.org/10.1124/dmd.108.023630. dmd.108.023630 [pii]CrossRefPubMedGoogle Scholar
  60. 60.
    Morahan PS, Munson AE, Regelson W, Commerford SL, Hamilton LD (1972) Antiviral activity and side effects of polyriboinosinic-cytidylic acid complexes as affected by molecular size. Proc Natl Acad Sci U S A 69(4):842–846PubMedCentralPubMedGoogle Scholar
  61. 61.
    Nebert DW, Friedman RM (1973) Stimulation of aryl hydrocarbon hydroxylase induction in cell cultures by interferon. J Virol 11(2):193–197PubMedCentralPubMedGoogle Scholar
  62. 62.
    Farquhar D, Loo TL, Gutterman JU, Hersh EM, Luna MA (1976) Inhibition of drug-metabolizing enzymes in the rat after Bacillus Calmette-Guerin treatment. Biochem Pharmacol 25(13):1529–1535PubMedGoogle Scholar
  63. 63.
    Castro JE (1974) The effect of Corynebacterium parvum on the structure and function of the lymphoid system in mice. Eur J Cancer 10(2):115–120PubMedGoogle Scholar
  64. 64.
    Foster RS Jr (1976) The immunostimulant Corynibacterium parvum and hematopoietic toxicity of chemotherapy. Surg Forum 27(62):140–142PubMedGoogle Scholar
  65. 65.
    Soyka LF, Stephens CC, MacPherson BR, Foster RS Jr (1979) Role of mononuclear phagocytes in decreased hepatic drug metabolism following administration of Corynebacterium parvum. Int J Immunopharmacol 1(2):101–112PubMedGoogle Scholar
  66. 66.
    Aitken AE, Richardson TA, Morgan ET (2006) Regulation of drug-metabolizing enzymes and transporters in inflammation. Annu Rev Pharmacol Toxicol 46:123–149PubMedGoogle Scholar
  67. 67.
    Chang KC, Bell TD, Lauer BA, Chai H (1978) Altered theophylline pharmacokinetics during acute respiratory viral illness. Lancet 1(8074):1132–1133PubMedGoogle Scholar
  68. 68.
    Kraemer MJ, Furukawa CT, Koup JR, Shapiro GG, Pierson WE, Bierman CW (1982) Altered theophylline clearance during an influenza B outbreak. Pediatrics 69(4):476–480PubMedGoogle Scholar
  69. 69.
    Schmitt C, Kuhn B, Zhang X, Kivitz AJ, Grange S (2011) Disease-drug-drug interaction involving tocilizumab and simvastatin in patients with rheumatoid arthritis. Clin Pharmacol Ther 89(5):735–740.  https://doi.org/10.1038/clpt.2011.35 CrossRefPubMedGoogle Scholar
  70. 70.
    Chen YL, Le Vraux V, Leneveu A, Dreyfus F, Stheneur A, Florentin I, De Sousa M, Giroud JP, Flouvat B, Chauvelot-Moachon L (1994) Acute-phase response, interleukin-6, and alteration of cyclosporine pharmacokinetics. Clin Pharmacol Ther 55(6):649–660PubMedGoogle Scholar
  71. 71.
    Gidal BE, Reiss WG, Liao JS, Pitterle ME (1996) Changes in interleukin-6 concentrations following epilepsy surgery: potential influence on carbamazepine pharmacokinetics. Ann Pharmacother 30(5):545–546PubMedGoogle Scholar
  72. 72.
    Shelly MP, Mendel L, Park GR (1987) Failure of critically ill patients to metabolise midazolam. Anaesthesia 42(6):619–626PubMedGoogle Scholar
  73. 73.
    O’Neil WM, Gilfix BM, Markoglou N, Di Girolamo A, Tsoukas CM, Wainer IW (2000) Genotype and phenotype of cytochrome P450 2D6 in human immunodeficiency virus-positive patients and patients with acquired immunodeficiency syndrome. Eur J Clin Pharmacol 56(3):231–240PubMedGoogle Scholar
  74. 74.
    Frye RF, Schneider VM, Frye CS, Feldman AM (2002) Plasma levels of TNF-alpha and IL-6 are inversely related to cytochrome P450-dependent drug metabolism in patients with congestive heart failure. J Card Fail 8(5):315–319. doi:S1071916402004232 [pii]PubMedGoogle Scholar
  75. 75.
    Renton KW, Gray JD, Hall RI (1980) Decreased elimination of theophylline after influenza vaccination. Can Med Assoc J 123(4):288–290PubMedCentralPubMedGoogle Scholar
  76. 76.
    Rivory LP, Slaviero KA, Clarke SJ (2002) Hepatic cytochrome P450 3A drug metabolism is reduced in cancer patients who have an acute-phase response. Br J Cancer 87(3):277–280.  https://doi.org/10.1038/sj.bjc.6600448 CrossRefPubMedCentralPubMedGoogle Scholar
  77. 77.
    Williams ML, Bhargava P, Cherrouk I, Marshall JL, Flockhart DA, Wainer IW (2000) A discordance of the cytochrome P450 2C19 genotype and phenotype in patients with advanced cancer. Br J Clin Pharmacol 49(5):485–488PubMedCentralPubMedGoogle Scholar
  78. 78.
    Rubin K, Janefeldt A, Andersson L, Berke Z, Grime K, Andersson TB (2015) HepaRG cells as human-relevant in vitro model to study the effects of inflammatory stimuli on cytochrome P450 isoenzymes. Drug Metab Dispos 43(1):119–125.  https://doi.org/10.1124/dmd.114.059246 CrossRefPubMedGoogle Scholar
  79. 79.
    Aitken AE, Lee CM, Morgan ET (2008) Roles of nitric oxide in inflammatory downregulation of human cytochromes P450. Free Radic Biol Med 44(6):1161–1168.  https://doi.org/10.1016/j.freeradbiomed.2007.12.010. S0891-5849(07)00812-X [pii]CrossRefPubMedGoogle Scholar
  80. 80.
    Lagadic-Gossmann D, Lerche C, Rissel M, Joannard F, Galisteo M, Guillouzo A, Corcos L (2000) The induction of the human hepatic CYP2E1 gene by interleukin 4 is transcriptional and regulated by protein kinase C. Cell Biol Toxicol 16(4):221–233Google Scholar
  81. 81.
    Muntane-Relat J, Ourlin JC, Domergue J, Maurel P (1995) Differential effects of cytokines on the inducible expression of CYP1A1, CYP1A2, and CYP3A4 in human hepatocytes in primary culture. Hepatology 22(4 Pt 1):1143–1153. doi:S0270913995003569 [pii]Google Scholar
  82. 82.
    Sunman JA, Hawke RL, LeCluyse EL, Kashuba AD (2004) Kupffer cell-mediated IL-2 suppression of CYP3A activity in human hepatocytes. Drug Metab Dispos 32(3):359–363.  https://doi.org/10.1124/dmd.32.3.359. 32/3/359 [pii]CrossRefGoogle Scholar
  83. 83.
    Yang J, Hao C, Yang D, Shi D, Song X, Luan X, Hu G, Yan B (2010) Pregnane X receptor is required for interleukin-6 mediated down-regulation of cytochrome P450 3A4 in human hepatocytes. Toxicol Lett.  https://doi.org/10.1016/j.toxlet.2010.06.003. S0378-4274(10)01542-0 [pii]
  84. 84.
    Czerwinski M, Kazmi F, Parkinson A, Buckley DB (2015) Anti-CD28 monoclonal antibody-stimulated cytokines released from blood suppress CYP1A2, CYP2B6, and CYP3A4 in human hepatocytes in vitro. Drug Metab Dispos 43(1):42–52.  https://doi.org/10.1124/dmd.114.060186 CrossRefGoogle Scholar
  85. 85.
    Morcos PN, Moreira SA, Brennan BJ, Blotner S, Shulman NS, Smith PF (2013) Influence of chronic hepatitis C infection on cytochrome P450 3A4 activity using midazolam as an in vivo probe substrate. Eur J Clin Pharmacol 69(10):1777–1784.  https://doi.org/10.1007/s00228-013-1525-5 CrossRefGoogle Scholar
  86. 86.
    Hartmann G, Vassileva V, Piquette-Miller M (2005) Impact of endotoxin-induced changes in P-glycoprotein expression on disposition of doxorubicin in mice. Drug Metab Dispos 33(6):820–828.  https://doi.org/10.1124/dmd.104.002568. dmd.104.002568 [pii]CrossRefGoogle Scholar
  87. 87.
    Piquette-Miller M, Pak A, Kim H, Anari R, Shahzamani A (1998) Decreased expression and activity of P-glycoprotein in rat liver during acute inflammation. Pharm Res 15(5):706–711PubMedGoogle Scholar
  88. 88.
    Sukhai M, Yong A, Kalitsky J, Piquette-Miller M (2000) Inflammation and interleukin-6 mediate reductions in the hepatic expression and transcription of the mdr1a and mdr1b Genes. Mol Cell Biol Res Commun 4(4):248–256.  https://doi.org/10.1006/mcbr.2001.0288. S1522472401902880 [pii]CrossRefPubMedGoogle Scholar
  89. 89.
    Ando H, Nishio Y, Ito K, Nakao A, Wang L, Zhao YL, Kitaichi K, Takagi K, Hasegawa T (2001) Effect of endotoxin on P-glycoprotein-mediated biliary and renal excretion of rhodamine-123 in rats. Antimicrob Agents Chemother 45(12):3462–3467.  https://doi.org/10.1128/AAC.45.12.3462-3467.2001 CrossRefPubMedCentralPubMedGoogle Scholar
  90. 90.
    Wang JH, Scollard DA, Teng S, Reilly RM, Piquette-Miller M (2005) Detection of P-glycoprotein activity in endotoxemic rats by 99mTc-sestamibi imaging. J Nucl Med 46(9):1537–1545. doi:46/9/1537 [pii]Google Scholar
  91. 91.
    Cherrington NJ, Slitt AL, Li N, Klaassen CD (2004) Lipopolysaccharide-mediated regulation of hepatic transporter mRNA levels in rats. Drug Metab Dispos: Biol Fate Chem 32(i):734–741. doi:32/7/734 [pii]Google Scholar
  92. 92.
    Geier A, Dietrich CG, Voigt S, Kim SK, Gerloff T, Kullak-Ublick GA, Lorenzen J, Matern S, Gartung C (2003) Effects of proinflammatory cytokines on rat organic anion transporters during toxic liver injury and cholestasis. Hepatology 38(2):345–354.  https://doi.org/10.1053/jhep.2003.50317. S0270913903005330 [pii]CrossRefGoogle Scholar
  93. 93.
    Hartmann G, Cheung AK, Piquette-Miller M (2002) Inflammatory cytokines, but not bile acids, regulate expression of murine hepatic anion transporters in endotoxemia. J Pharmacol Exp Ther 303(1):273–281.  https://doi.org/10.1124/jpet.102.039404 CrossRefGoogle Scholar
  94. 94.
    Sukhai M, Yong A, Pak A, Piquette-Miller M (2001) Decreased expression of P-glycoprotein in interleukin-1beta and interleukin-6 treated rat hepatocytes. Inflamm Res 50(7):362–370Google Scholar
  95. 95.
    Teng S, Piquette-Miller M (2005) The involvement of the pregnane X receptor in hepatic gene regulation during inflammation in mice. J Pharmacol Exp Ther 312(2):841–848.  https://doi.org/10.1124/jpet.104.076141. jpet.104.076141 [pii]CrossRefGoogle Scholar
  96. 96.
    Siewert E, Dietrich CG, Lammert F, Heinrich PC, Matern S, Gartung C, Geier A (2004) Interleukin-6 regulates hepatic transporters during acute-phase response. Biochem Biophys Res Commun 322(1):232–238.  https://doi.org/10.1016/j.bbrc.2004.07.102. S0006-291X(04)01616-X [pii]CrossRefGoogle Scholar
  97. 97.
    Elferink MG, Olinga P, Draaisma AL, Merema MT, Faber KN, Slooff MJ, Meijer DK, Groothuis GM (2004) LPS-induced downregulation of MRP2 and BSEP in human liver is due to a posttranscriptional process. Am J Physiol Gastrointest Liver Physiol 287(5):G1008–G1016.  https://doi.org/10.1152/ajpgi.00071.2004. 00071.2004 [pii]CrossRefGoogle Scholar
  98. 98.
    Fardel O, Le Vee M (2009) Regulation of human hepatic drug transporter expression by pro-inflammatory cytokines. Expert Opin Drug Metab Toxicol 5(12):1469–1481.  https://doi.org/10.1517/17425250903304056 CrossRefGoogle Scholar
  99. 99.
    Buyse M, Radeva G, Bado A, Farinotti R (2005) Intestinal inflammation induces adaptation of P-glycoprotein expression and activity. Biochem Pharmacol 69(12):1745–1754.  https://doi.org/10.1016/j.bcp.2005.03.025. S0006-2952(05)00199-1 [pii]CrossRefGoogle Scholar
  100. 100.
    Iizasa H, Genda N, Kitano T, Tomita M, Nishihara K, Hayashi M, Nakamura K, Kobayashi S, Nakashima E (2003) Altered expression and function of P-glycoprotein in dextran sodium sulfate-induced colitis in mice. J Pharm Sci 92(3):569–576.  https://doi.org/10.1002/jps.10326 CrossRefPubMedGoogle Scholar
  101. 101.
    Masubuchi Y, Enoki K, Horie T (2008) Down-regulation of hepatic cytochrome P450 enzymes in rats with trinitrobenzene sulfonic acid-induced colitis. Drug Metab Dispos 36(3):597–603.  https://doi.org/10.1124/dmd.107.018754. dmd.107.018754 [pii]CrossRefPubMedGoogle Scholar
  102. 102.
    Naud J, Michaud J, Boisvert C, Desbiens K, Leblond FA, Mitchell A, Jones C, Bonnardeaux A, Pichette V (2007) Down-regulation of intestinal drug transporters in chronic renal failure in rats. J Pharmacol Exp Ther 320(3):978–985.  https://doi.org/10.1124/jpet.106.112631. jpet.106.112631 [pii]CrossRefPubMedGoogle Scholar
  103. 103.
    Veau C, Faivre L, Tardivel S, Soursac M, Banide H, Lacour B, Farinotti R (2002) Effect of interleukin-2 on intestinal P-glycoprotein expression and functionality in mice. J Pharmacol Exp Ther 302(2):742–750PubMedGoogle Scholar
  104. 104.
    Niessner M, Volk BA (1995) Altered Th1/Th2 cytokine profiles in the intestinal mucosa of patients with inflammatory bowel disease as assessed by quantitative reversed transcribed polymerase chain reaction (RT-PCR). Clin Exp Immunol 101(3):428–435PubMedCentralPubMedGoogle Scholar
  105. 105.
    Sawa Y, Oshitani N, Adachi K, Higuchi K, Matsumoto T, Arakawa T (2003) Comprehensive analysis of intestinal cytokine messenger RNA profile by real-time quantitative polymerase chain reaction in patients with inflammatory bowel disease. Int J Mol Med 11(2):175–179PubMedGoogle Scholar
  106. 106.
    Gutmann H, Hruz P, Zimmermann C, Straumann A, Terracciano L, Hammann F, Lehmann F, Beglinger C, Drewe J (2008) Breast cancer resistance protein and P-glycoprotein expression in patients with newly diagnosed and therapy-refractory ulcerative colitis compared with healthy controls. Digestion 78(2–3):154–162.  https://doi.org/10.1159/000179361. 000179361 [pii]CrossRefPubMedGoogle Scholar
  107. 107.
    Englund G, Jacobson A, Rorsman F, Artursson P, Kindmark A, Ronnblom A (2007) Efflux transporters in ulcerative colitis: decreased expression of BCRP (ABCG2) and Pgp (ABCB1). Inflamm Bowel Dis 13(3):291–297.  https://doi.org/10.1002/ibd.20030 CrossRefPubMedGoogle Scholar
  108. 108.
    Ufer M, Hasler R, Jacobs G, Haenisch S, Lachelt S, Faltraco F, Sina C, Rosenstiel P, Nikolaus S, Schreiber S, Cascorbi I (2009) Decreased sigmoidal ABCB1 (P-glycoprotein) expression in ulcerative colitis is associated with disease activity. Pharmacogenomics 10(12):1941–1953.  https://doi.org/10.2217/pgs.09.128 CrossRefPubMedGoogle Scholar
  109. 109.
    Blokzijl H, Vander Borght S, Bok LI, Libbrecht L, Geuken M, van den Heuvel FA, Dijkstra G, Roskams TA, Moshage H, Jansen PL, Faber KN (2007) Decreased P-glycoprotein (P-gp/MDR1) expression in inflamed human intestinal epithelium is independent of PXR protein levels. Inflamm Bowel Dis 13(6):710–720.  https://doi.org/10.1002/ibd.20088 CrossRefPubMedGoogle Scholar
  110. 110.
    Langmann T, Moehle C, Mauerer R, Scharl M, Liebisch G, Zahn A, Stremmel W, Schmitz G (2004) Loss of detoxification in inflammatory bowel disease: dysregulation of pregnane X receptor target genes. Gastroenterology 127(1):26–40. doi:S0016508504007140 [pii]PubMedGoogle Scholar
  111. 111.
    Kawauchi S, Nakamura T, Miki I, Inoue J, Hamaguchi T, Tanahashi T, Mizuno S (2014) Downregulation of CYP3A and P-glycoprotein in the secondary inflammatory response of mice with dextran sulfate sodium-induced colitis and its contribution to cyclosporine A blood concentrations. J Pharmacol Sci 124(2):180–191PubMedGoogle Scholar
  112. 112.
    Kusunoki Y, Ikarashi N, Hayakawa Y, Ishii M, Kon R, Ochiai W, Machida Y, Sugiyama K (2014) Hepatic early inflammation induces downregulation of hepatic cytochrome P450 expression and metabolic activity in the dextran sulfate sodium-induced murine colitis. Eur J Pharm Sci 54:17–27.  https://doi.org/10.1016/j.ejps.2013.12.019 CrossRefPubMedGoogle Scholar
  113. 113.
    Kusunoki Y, Ikarashi N, Matsuda S, Matsukawa Y, Kitaoka S, Kon R, Tajima M, Wakui N, Ochiai W, Machida Y, Sugiyama K (2015) Expression of hepatic cytochrome P450 in a mouse model of ulcerative colitis changes with pathological conditions. J Gastroenterol Hepatol 30(11):1618–1626.  https://doi.org/10.1111/jgh.12966 CrossRefPubMedGoogle Scholar
  114. 114.
    Liu J, Zhou F, Chen Q, Kang A, Lu M, Liu W, Zang X, Wang G, Zhang J (2015) Chronic inflammation up-regulates P-gp in peripheral mononuclear blood cells via the STAT3/Nf-kappab pathway in 2,4,6-trinitrobenzene sulfonic acid-induced colitis mice. Sci Rep 5:13558.  https://doi.org/10.1038/srep13558 CrossRefPubMedCentralPubMedGoogle Scholar
  115. 115.
    Nyagode BA, Jahangardi R, Merrell MD, Tansey MG, Morgan ET (2014) Selective effects of a therapeutic protein targeting tumor necrosis factor-alpha on cytochrome P450 regulation during infectious colitis: implications for disease-dependent drug-drug interactions. Pharmacol Res Perspect 2(1):e00027.  https://doi.org/10.1002/prp2.27 CrossRefPubMedCentralPubMedGoogle Scholar
  116. 116.
    Nyagode BA, Lee CM, Morgan ET (2010) Modulation of hepatic cytochrome P450s by Citrobacter rodentium infection in interleukin-6- and interferon-{gamma}-null mice. J Pharmacol Exp Ther 335(2):480–488.  https://doi.org/10.1124/jpet.110.171488 CrossRefPubMedCentralPubMedGoogle Scholar
  117. 117.
    Sugimoto M, Furuta T, Shirai N, Ikuma M, Hishida A, Ishizaki T (2006) Influences of proinflammatory and anti-inflammatory cytokine polymorphisms on eradication rates of clarithromycin-sensitive strains of Helicobacter pylori by triple therapy. Clin Pharmacol Ther 80(1):41–50.  https://doi.org/10.1016/j.clpt.2006.03.007. S0009-9236(06)00120-2 [pii]CrossRefPubMedGoogle Scholar
  118. 118.
    Miftahussurur M, Yamaoka Y (2015) Helicobacter pylori virulence genes and host genetic polymorphisms as risk factors for peptic ulcer disease. Expert Rev Gastroenterol Hepatol 9(12):1535–1547.  https://doi.org/10.1586/17474124.2015.1095089 CrossRefPubMedCentralPubMedGoogle Scholar
  119. 119.
    Zambon CF, Fasolo M, Basso D, D’Odorico A, Stranges A, Navaglia F, Fogar P, Greco E, Schiavon S, Padoan A, Fadi E, Sturniolo GC, Plebani M, Pedrazzoli S (2007) Clarithromycin resistance, tumor necrosis factor alpha gene polymorphism and mucosal inflammation affect H. pylori eradication success. J Gastrointest Surg 11(11):1506–1514.; discussion 1514.  https://doi.org/10.1007/s11605-007-0246-4 CrossRefPubMedGoogle Scholar
  120. 120.
    Furuta T, Shirai N, Takashima M, Xiao F, Sugimura H (2002) Effect of genotypic differences in interleukin-1 beta on gastric acid secretion in Japanese patients infected with Helicobacter pylori. Am J Med 112(2):141–143. doi:S0002934301010361 [pii]PubMedGoogle Scholar
  121. 121.
    Furuta T, Shirai N, Xiao F, El-Omar EM, Rabkin CS, Sugimura H, Ishizaki T, Ohashi K (2004) Polymorphism of interleukin-1beta affects the eradication rates of Helicobacter pylori by triple therapy. Clin Gastroenterol Hepatol 2(1):22–30. doi:S154235650300288X [pii]PubMedGoogle Scholar
  122. 122.
    Schmidt C, Hocherl K, Bucher M (2007) Cytokine-mediated regulation of urea transporters during experimental endotoxemia. Am J Physiol Renal Physiol 292(5):F1479–F1489.  https://doi.org/10.1152/ajprenal.00460.2006. 00460.2006 [pii]CrossRefPubMedGoogle Scholar
  123. 123.
    Schmidt C, Hocherl K, Bucher M (2007) Regulation of renal glucose transporters during severe inflammation. Am J Physiol Renal Physiol 292(2):F804–F811.  https://doi.org/10.1152/ajprenal.00258.2006. 00258.2006 [pii]CrossRefPubMedGoogle Scholar
  124. 124.
    Schmidt C, Hocherl K, Schweda F, Kurtz A, Bucher M (2007) Regulation of renal sodium transporters during severe inflammation. J Am Soc Nephrol 18(4):1072–1083.  https://doi.org/10.1681/ASN.2006050454. ASN.2006050454 [pii]CrossRefPubMedGoogle Scholar
  125. 125.
    Heemskerk S, Wouterse AC, Russel FG, Masereeuw R (2008) Nitric oxide down-regulates the expression of organic cation transporters (OCT) 1 and 2 in rat kidney during endotoxemia. Eur J Pharmacol 584(2–3):390–397.  https://doi.org/10.1016/j.ejphar.2008.02.006. S0014-2999(08)00153-2 [pii]CrossRefPubMedGoogle Scholar
  126. 126.
    Heemskerk S, van Koppen A, van den Broek L, Poelen GJ, Wouterse AC, Dijkman HB, Russel FG, Masereeuw R (2007) Nitric oxide differentially regulates renal ATP-binding cassette transporters during endotoxemia. Pflugers Arch 454(2):321–334.  https://doi.org/10.1007/s00424-007-0210-x CrossRefPubMedCentralPubMedGoogle Scholar
  127. 127.
    Huls M, van den Heuvel JJ, Dijkman HB, Russel FG, Masereeuw R (2006) ABC transporter expression profiling after ischemic reperfusion injury in mouse kidney. Kidney Int 69(12):2186–2193.  https://doi.org/10.1038/sj.ki.5000407. 5000407 [pii]CrossRefPubMedGoogle Scholar
  128. 128.
    Masereeuw R, Moons MM, Russel FG (1997) Rhodamine 123 accumulates extensively in the isolated perfused rat kidney and is secreted by the organic cation system. Eur J Pharmacol 321(3):315–323. doi:S0014-2999(96)00957-0 [pii]PubMedGoogle Scholar
  129. 129.
    Graff CL, Pollack GM (2004) Drug transport at the blood-brain barrier and the choroid plexus. Curr Drug Metab 5(1):95–108PubMedGoogle Scholar
  130. 130.
    Kusuhara H, Sugiyama Y (2005) Active efflux across the blood-brain barrier: role of the solute carrier family. NeuroRx 2(1):73–85PubMedCentralPubMedGoogle Scholar
  131. 131.
    de Vries HE, Kuiper J, de Boer AG, Van Berkel TJ, Breimer DD (1997) The blood-brain barrier in neuroinflammatory diseases. Pharmacol Rev 49(2):143–155PubMedGoogle Scholar
  132. 132.
    Eikelenboom P, Bate C, Van Gool WA, Hoozemans JJ, Rozemuller JM, Veerhuis R, Williams A (2002) Neuroinflammation in Alzheimer’s disease and prion disease. Glia 40(2):232–239PubMedGoogle Scholar
  133. 133.
    Ghafouri M, Amini S, Khalili K, Sawaya BE (2006) HIV-1 associated dementia: symptoms and causes. Retrovirology 3:28PubMedCentralPubMedGoogle Scholar
  134. 134.
    Whitton PS (2007) Inflammation as a causative factor in the aetiology of Parkinson’s disease. Br J Pharmacol 150(8):963–976PubMedCentralPubMedGoogle Scholar
  135. 135.
    Bauer B, Hartz AM, Pekcec A, Toellner K, Miller DS, Potschka H (2008) Seizure-induced up-regulation of P-glycoprotein at the blood-brain barrier through glutamate and cyclooxygenase-2 signaling. Mol Pharmacol 73(5):1444–1453PubMedGoogle Scholar
  136. 136.
    Kortekaas R, Leenders KL, van Oostrom JC, Vaalburg W, Bart J, Willemsen AT, Hendrikse NH (2005) Blood-brain barrier dysfunction in parkinsonian midbrain in vivo. Ann Neurol 57(2):176–179PubMedGoogle Scholar
  137. 137.
    Langford D, Grigorian A, Hurford R, Adame A, Ellis RJ, Hansen L, Masliah E (2004) Altered P-glycoprotein expression in AIDS patients with HIV encephalitis. J Neuropathol Exp Neurol 63(10):1038–1047PubMedGoogle Scholar
  138. 138.
    Loscher W, Potschka H (2005) Drug resistance in brain diseases and the role of drug efflux transporters. Nat Rev Neurosci 6(8):591–602PubMedGoogle Scholar
  139. 139.
    Roberts DJ, Goralski KB, Renton KW, Julien LC, Webber AM, Sleno L, Volmer DA, Hall RI (2009) Effect of acute inflammatory brain injury on accumulation of morphine and morphine 3- and 6-glucuronide in the human brain. Crit Care Med 37(10):2767–2774.  https://doi.org/10.1097/CCM.0b013e3181b755d5. 00003246-200910000-00014 [pii]CrossRefPubMedGoogle Scholar
  140. 140.
    Vogelgesang S, Warzok RW, Cascorbi I, Kunert-Keil C, Schroeder E, Kroemer HK, Siegmund W, Walker LC, Pahnke J (2004) The role of P-glycoprotein in cerebral amyloid angiopathy; implications for the early pathogenesis of Alzheimer’s disease. Curr Alzheimer Res 1(2):121–125PubMedCentralPubMedGoogle Scholar
  141. 141.
    Beaulieu E, Demeule M, Ghitescu L, Beliveau R (1997) P-glycoprotein is strongly expressed in the luminal membranes of the endothelium of blood vessels in the brain. Biochem J 326(Pt 2):539–544PubMedCentralPubMedGoogle Scholar
  142. 142.
    Virgintino D, Robertson D, Errede M, Benagiano V, Girolamo F, Maiorano E, Roncali L, Bertossi M (2002) Expression of P-glycoprotein in human cerebral cortex microvessels. J Histochem Cytochem 50(12):1671–1676PubMedGoogle Scholar
  143. 143.
    Choo EF, Leake B, Wandel C, Imamura H, Wood AJ, Wilkinson GR, Kim RB (2000) Pharmacological inhibition of P-glycoprotein transport enhances the distribution of HIV-1 protease inhibitors into brain and testes. Drug Metab Dispos 28(6):655–660PubMedGoogle Scholar
  144. 144.
    King M, Su W, Chang A, Zuckerman A, Pasternak GW (2001) Transport of opioids from the brain to the periphery by P-glycoprotein: peripheral actions of central drugs. Nat Neurosci 4(3):268–274PubMedGoogle Scholar
  145. 145.
    Lankas GR, Cartwright ME, Umbenhauer D (1997) P-glycoprotein deficiency in a subpopulation of CF-1 mice enhances avermectin-induced neurotoxicity. Toxicol Appl Pharmacol 143(2):357–365PubMedGoogle Scholar
  146. 146.
    Luurtsema G, Molthoff CF, Windhorst AD, Smit JW, Keizer H, Boellaard R, Lammertsma AA, Franssen EJ (2003) (R)- and (S)-[11C]verapamil as PET-tracers for measuring P-glycoprotein function: in vitro and in vivo evaluation. Nucl Med Biol 30(7):747–751PubMedGoogle Scholar
  147. 147.
    Thuerauf N, Fromm MF (2006) The role of the transporter P-glycoprotein for disposition and effects of centrally acting drugs and for the pathogenesis of CNS diseases. Eur Arch Psychiatry Clin Neurosci 256(5):281–286PubMedGoogle Scholar
  148. 148.
    Uhr M, Tontsch A, Namendorf C, Ripke S, Lucae S, Ising M, Dose T, Ebinger M, Rosenhagen M, Kohli M, Kloiber S, Salyakina D, Bettecken T, Specht M, Putz B, Binder EB, Muller-Myhsok B, Holsboer F (2008) Polymorphisms in the drug transporter gene ABCB1 predict antidepressant treatment response in depression. Neuron 57(2):203–209PubMedGoogle Scholar
  149. 149.
    Greenberg ML, Fisher PG, Freeman C, Korones DN, Bernstein M, Friedman H, Blaney S, Hershon L, Zhou T, Chen Z, Kretschmar C (2005) Etoposide, vincristine, and cyclosporin A with standard-dose radiation therapy in newly diagnosed diffuse intrinsic brainstem gliomas: a pediatric oncology group phase I study. Pediatr Blood Cancer 45(5):644–648PubMedGoogle Scholar
  150. 150.
    Sadeque AJ, Wandel C, He H, Shah S, Wood AJ (2000) Increased drug delivery to the brain by P-glycoprotein inhibition. Clin Pharmacol Ther 68(3):231–237PubMedGoogle Scholar
  151. 151.
    Chen X, Zhou ZW, Xue CC, Li XX, Zhou SF (2007) Role of P-glycoprotein in restricting the brain penetration of tanshinone IIA, a major active constituent from the root of Salvia miltiorrhiza Bunge, across the blood-brain barrier. Xenobiotica 37(6):635–678PubMedGoogle Scholar
  152. 152.
    Imbert F, Jardin M, Fernandez C, Gantier JC, Dromer F, Baron G, Mentre F, Van Beijsterveldt L, Singlas E, Gimenez F (2003) Effect of efflux inhibition on brain uptake of itraconazole in mice infected with Cryptococcus neoformans. Drug Metab Dispos 31(3):319–325PubMedGoogle Scholar
  153. 153.
    XY Y, Lin SG, Chen X, Zhou ZW, Liang J, Duan W, Chowbay B, Wen JY, Chan E, Cao J, Li CG, Zhou SF (2007) Transport of cryptotanshinone, a major active triterpenoid in Salvia miltiorrhiza Bunge widely used in the treatment of stroke and Alzheimer’s disease, across the blood-brain barrier. Curr Drug Metab 8(4):365–378Google Scholar
  154. 154.
    Zhao YL, Du J, Kanazawa H, Cen XB, Takagi K, Kitaichi K, Tatsumi Y, Takagi K, Ohta M, Hasegawa T (2002) Shiga-like toxin II modifies brain distribution of a P-glycoprotein substrate, doxorubicin, and P-glycoprotein expression in mice. Brain Res 956(2):246–253PubMedGoogle Scholar
  155. 155.
    Zhao YL, Du J, Kanazawa H, Sugawara A, Takagi K, Kitaichi K, Tatsumi Y, Takagi K, Hasegawa T (2002) Effect of endotoxin on doxorubicin transport across blood-brain barrier and P-glycoprotein function in mice. Eur J Pharmacol 445(1–2):115–123PubMedGoogle Scholar
  156. 156.
    Hartz AM, Bauer B, Block ML, Hong JS, Miller DS (2008) Diesel exhaust particles induce oxidative stress, proinflammatory signaling, and P-glycoprotein up-regulation at the blood-brain barrier. FASEB J 22(8):2723–2733PubMedCentralPubMedGoogle Scholar
  157. 157.
    Seelbach MJ, Brooks TA, Egleton RD, Davis TP (2007) Peripheral inflammatory hyperalgesia modulates morphine delivery to the brain: a role for P-glycoprotein. J Neurochem 102(5):1677–1690PubMedGoogle Scholar
  158. 158.
    McCaffrey G, Staatz WD, Sanchez-Covarrubias L, Finch JD, Demarco K, Laracuente ML, Ronaldson PT, Davis TP (2012) P-glycoprotein trafficking at the blood-brain barrier altered by peripheral inflammatory hyperalgesia. J Neurochem 122(5):962–975.  https://doi.org/10.1111/j.1471-4159.2012.07831.x CrossRefPubMedGoogle Scholar
  159. 159.
    Bauer B, Hartz AM, Fricker G, Miller DS (2005) Modulation of p-glycoprotein transport function at the blood-brain barrier. Exp Biol Med (Maywood, NJ) 230(2):118–127Google Scholar
  160. 160.
    Hartz AM, Bauer B, Fricker G, Miller DS (2004) Rapid regulation of P-glycoprotein at the blood-brain barrier by endothelin-1. Mol Pharmacol 66(3):387–394PubMedGoogle Scholar
  161. 161.
    Poller B, Drewe J, Krahenbuhl S, Huwyler J, Gutmann H (2010) Regulation of BCRP (ABCG2) and P-glycoprotein (ABCB1) by cytokines in a model of the human blood-brain barrier. Cell Mol Neurobiol 30(1):63–70.  https://doi.org/10.1007/s10571-009-9431-1 CrossRefPubMedGoogle Scholar
  162. 162.
    Ronaldson PT, Ashraf T, Bendayan R (2010) Regulation of multidrug resistance protein 1 by tumor necrosis factor alpha in cultured glial cells: involvement of nuclear factor-kappaB and c-Jun N-terminal kinase signaling pathways. Mol Pharmacol 77(4):644–659.  https://doi.org/10.1124/mol.109.059410. mol.109.059410 [pii]CrossRefPubMedGoogle Scholar
  163. 163.
    Ronaldson PT, Bendayan R (2006) HIV-1 viral envelope glycoprotein gp120 triggers an inflammatory response in cultured rat astrocytes and regulates the functional expression of P-glycoprotein. Mol Pharmacol 70(3):1087–1098PubMedGoogle Scholar
  164. 164.
    Lazarowski A, Czornyj L, Lubienieki F, Girardi E, Vazquez S, D’Giano C (2007) ABC transporters during epilepsy and mechanisms underlying multidrug resistance in refractory epilepsy. Epilepsia 48(Suppl 5):140–149PubMedGoogle Scholar
  165. 165.
    Spudich A, Kilic E, Xing H, Kilic U, Rentsch KM, Wunderli-Allenspach H, Bassetti CL, Hermann DM (2006) Inhibition of multidrug resistance transporter-1 facilitates neuroprotective therapies after focal cerebral ischemia. Nat Neurosci 9(4):487–488PubMedGoogle Scholar
  166. 166.
    Jin L, Li J, Nation RL, Nicolazzo JA (2011) Impact of p-glycoprotein inhibition and lipopolysaccharide administration on blood-brain barrier transport of colistin in mice. Antimicrob Agents Chemother 55(2):502–507.  https://doi.org/10.1128/AAC.01273-10 CrossRefPubMedGoogle Scholar
  167. 167.
    Daniels BP, Holman DW, Cruz-Orengo L, Jujjavarapu H, Durrant DM, Klein RS (2014) Viral pathogen-associated molecular patterns regulate blood-brain barrier integrity via competing innate cytokine signals. MBio 5(5):e01476–e01414.  https://doi.org/10.1128/mBio.01476-14 CrossRefPubMedCentralPubMedGoogle Scholar
  168. 168.
    Wong D, Dorovini-Zis K, Vincent SR (2004) Cytokines, nitric oxide, and cGMP modulate the permeability of an in vitro model of the human blood-brain barrier. Exp Neurol 190(2):446–455.  https://doi.org/10.1016/j.expneurol.2004.08.008 CrossRefPubMedGoogle Scholar
  169. 169.
    Tsao N, Hsu HP, CM W, Liu CC, Lei HY (2001) Tumour necrosis factor-alpha causes an increase in blood-brain barrier permeability during sepsis. J Med Microbiol 50(9):812–821.  https://doi.org/10.1099/0022-1317-50-9-812 CrossRefPubMedGoogle Scholar
  170. 170.
    Vahakangas K, Myllynen P (2009) Drug transporters in the human blood-placental barrier. Br J Pharmacol 158(3):665–678.  https://doi.org/10.1111/j.1476-5381.2009.00336.x. BPH336 [pii]CrossRefPubMedCentralPubMedGoogle Scholar
  171. 171.
    Evseenko DA, Paxton JW, Keelan JA (2006) ABC drug transporter expression and functional activity in trophoblast-like cell lines and differentiating primary trophoblast. Am J Physiol Regul Integr Comp Physiol 290(5):R1357–R1365.  https://doi.org/10.1152/ajpregu.00630.2005. 00630.2005 [pii]CrossRefPubMedGoogle Scholar
  172. 172.
    Jonker JW, Smit JW, Brinkhuis RF, Maliepaard M, Beijnen JH, Schellens JH, Schinkel AH (2000) Role of breast cancer resistance protein in the bioavailability and fetal penetration of topotecan. J Natl Cancer Inst 92(20):1651–1656PubMedGoogle Scholar
  173. 173.
    Lankas GR, Wise LD, Cartwright ME, Pippert T, Umbenhauer DR (1998) Placental P-glycoprotein deficiency enhances susceptibility to chemically induced birth defects in mice. Reprod Toxicol 12(4):457–463. doi:S0890623898000276 [pii]PubMedGoogle Scholar
  174. 174.
    Evseenko DA, Paxton JW, Keelan JA (2007) Independent regulation of apical and basolateral drug transporter expression and function in placental trophoblasts by cytokines, steroids, and growth factors. Drug Metab Dispos 35(4):595–601.  https://doi.org/10.1124/dmd.106.011478. dmd.106.011478 [pii]CrossRefPubMedGoogle Scholar
  175. 175.
    Smit JW, Huisman MT, van Tellingen O, Wiltshire HR, Schinkel AH (1999) Absence or pharmacological blocking of placental P-glycoprotein profoundly increases fetal drug exposure. J Clin Invest 104(10):1441–1447.  https://doi.org/10.1172/JCI7963 CrossRefPubMedCentralPubMedGoogle Scholar
  176. 176.
    Zhou L, Naraharisetti SB, Wang H, Unadkat JD, Hebert MF, Mao Q (2008) The breast cancer resistance protein (Bcrp1/Abcg2) limits fetal distribution of glyburide in the pregnant mouse: an Obstetric-Fetal Pharmacology Research Unit Network and University of Washington Specialized Center of Research Study. Mol Pharmacol 73(3):949–959.  https://doi.org/10.1124/mol.107.041616. mol.107.041616 [pii]CrossRefGoogle Scholar
  177. 177.
    Molsa M, Heikkinen T, Hakkola J, Hakala K, Wallerman O, Wadelius M, Wadelius C, Laine K (2005) Functional role of P-glycoprotein in the human blood-placental barrier. Clin Pharmacol Ther 78(2):123–131.  https://doi.org/10.1016/j.clpt.2005.04.014. S0009-9236(05)00188-8 [pii]CrossRefGoogle Scholar
  178. 178.
    Sudhakaran S, Rayner CR, Li J, Kong DC, Gude NM, Nation RL (2008) Inhibition of placental P-glycoprotein: impact on indinavir transfer to the foetus. Br J Clin Pharmacol 65(5):667–673.  https://doi.org/10.1111/j.1365-2125.2007.03067.x. BCP3067 [pii]CrossRefGoogle Scholar
  179. 179.
    Hemauer SJ, Patrikeeva SL, Nanovskaya TN, Hankins GD, Ahmed MS (2010) Role of human placental apical membrane transporters in the efflux of glyburide, rosiglitazone, and metformin. Am J Obstet Gynecol 202(4):383 e381–383 e387.  https://doi.org/10.1016/j.ajog.2010.01.035. S0002-9378(10)00065-7 [pii]CrossRefGoogle Scholar
  180. 180.
    Pollex E, Lubetsky A, Koren G (2008) The role of placental breast cancer resistance protein in the efflux of glyburide across the human placenta. Placenta 29(8):743–747.  https://doi.org/10.1016/j.placenta.2008.05.001. S0143-4004(08)00148-3 [pii]CrossRefGoogle Scholar
  181. 181.
    Lye P, Bloise E, Javam M, Gibb W, Lye SJ, Matthews SG (2015) Impact of bacterial and viral challenge on multidrug resistance in first- and third-trimester human placenta. Am J Pathol 185(6):1666–1675.  https://doi.org/10.1016/j.ajpath.2015.02.013 CrossRefGoogle Scholar
  182. 182.
    Hamai Y, Fujii T, Yamashita T, Nishina H, Kozuma S, Mikami Y, Taketani Y (1997) Evidence for an elevation in serum interleukin-2 and tumor necrosis factor-alpha levels before the clinical manifestations of preeclampsia. Am J Reprod Immunol 38(2):89–93Google Scholar
  183. 183.
    Saji F, Samejima Y, Kamiura S, Sawai K, Shimoya K, Kimura T (2000) Cytokine production in chorioamnionitis. J Reprod Immunol 47(2):185–196. doi:S0165-0378(00)00064-4 [pii]Google Scholar
  184. 184.
    Steinborn A, Niederhut A, Solbach C, Hildenbrand R, Sohn C, Kaufmann M (1999) Cytokine release from placental endothelial cells, a process associated with preterm labour in the absence of intrauterine infection. Cytokine 11(1):66–73.  https://doi.org/10.1006/cyto.1998.0399. S1043-4666(98)90399-4 [pii]CrossRefGoogle Scholar
  185. 185.
    Chen YH, Wang JP, Wang H, Sun MF, Wei LZ, Wei W, DX X (2005) Lipopolysaccharide treatment downregulates the expression of the pregnane X receptor, cyp3a11 and mdr1a genes in mouse placenta. Toxicology 211(3):242–252.  https://doi.org/10.1016/j.tox.2005.03.011. S0300-483X(05)00168-X [pii]CrossRefGoogle Scholar
  186. 186.
    Petrovic V, Wang JH, Piquette-Miller M (2008) Effect of endotoxin on the expression of placental drug transporters and glyburide disposition in pregnant rats. Drug Metab Dispos 36(9):1944–1950.  https://doi.org/10.1124/dmd.107.019851. dmd.107.019851 [pii]CrossRefGoogle Scholar
  187. 187.
    Gedeon C, Behravan J, Koren G, Piquette-Miller M (2006) Transport of glyburide by placental ABC transporters: implications in fetal drug exposure. Placenta 27(11–12):1096–1102.  https://doi.org/10.1016/j.placenta.2005.11.012. S0143-4004(05)00312-7 [pii]CrossRefGoogle Scholar
  188. 188.
    Mason CW, Buhimschi IA, Buhimschi CS, Dong Y, Weiner CP, Swaan PW (2011) ATP-binding cassette transporter expression in human placenta as a function of pregnancy condition. Drug Metab Dispos 39(6):1000–1007.  https://doi.org/10.1124/dmd.111.038166 CrossRefPubMedCentralPubMedGoogle Scholar
  189. 189.
    Mantovani A, Allavena P, Sica A, Balkwill F (2008) Cancer-related inflammation. Nature 454(7203):436–444.  https://doi.org/10.1038/nature07205. nature07205 [pii]CrossRefGoogle Scholar
  190. 190.
    Conze D, Weiss L, Regen PS, Bhushan A, Weaver D, Johnson P, Rincon M (2001) Autocrine production of interleukin 6 causes multidrug resistance in breast cancer cells. Cancer Res 61(24):8851–8858Google Scholar
  191. 191.
    Wang Y, Niu XL, Qu Y, Wu J, Zhu YQ, Sun WJ, Li LZ (2010) Autocrine production of interleukin-6 confers cisplatin and paclitaxel resistance in ovarian cancer cells. Cancer Lett 295(1):110–123.  https://doi.org/10.1016/j.canlet.2010.02.019. S0304-3835(10)00120-5 [pii]CrossRefGoogle Scholar
  192. 192.
    Kacevska M, Robertson GR, Clarke SJ, Liddle C (2008) Inflammation and CYP3A4-mediated drug metabolism in advanced cancer: impact and implications for chemotherapeutic drug dosing. Expert Opin Drug Metab Toxicol 4(2):137–149.  https://doi.org/10.1517/17425255.4.2.137 CrossRefGoogle Scholar
  193. 193.
    Gottesman MM, Fojo T, Bates SE (2002) Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2(1):48–58Google Scholar
  194. 194.
    Chen Z, Shi T, Zhang L, Zhu P, Deng M, Huang C, Hu T, Jiang L, Li J (2016) Mammalian drug efflux transporters of the ATP binding cassette (ABC) family in multidrug resistance: a review of the past decade. Cancer Lett 370(1):153–164.  https://doi.org/10.1016/j.canlet.2015.10.010 CrossRefGoogle Scholar
  195. 195.
    Longley DB, Johnston PG (2005) Molecular mechanisms of drug resistance. J Pathol 205(2):275–292Google Scholar
  196. 196.
    Szakacs G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM (2006) Targeting multidrug resistance in cancer. Nat Rev 5(3):219–234Google Scholar
  197. 197.
    Duan Z, Lamendola DE, Penson RT, Kronish KM, Seiden MV (2002) Overexpression of IL-6 but not IL-8 increases paclitaxel resistance of U-2OS human osteosarcoma cells. Cytokine 17(5):234–242.  https://doi.org/10.1006/cyto.2001.1008. S1043466601910087 [pii]CrossRefPubMedGoogle Scholar
  198. 198.
    Mosaffa F, Lage H, Afshari JT, Behravan J (2009) Interleukin-1 beta and tumor necrosis factor-alpha increase ABCG2 expression in MCF-7 breast carcinoma cell line and its mitoxantrone-resistant derivative, MCF-7/MX. Inflamm Res 58(10):669–676.  https://doi.org/10.1007/s00011-009-0034-6 CrossRefPubMedGoogle Scholar
  199. 199.
    Mosaffa F, Kalalinia F, Lage H, Afshari JT, Behravan J (2012) Pro-inflammatory cytokines interleukin-1 beta, interleukin 6, and tumor necrosis factor-alpha alter the expression and function of ABCG2 in cervix and gastric cancer cells. Mol Cell Biochem 363(1–2):385–393.  https://doi.org/10.1007/s11010-011-1191-9 CrossRefPubMedGoogle Scholar
  200. 200.
    Charles KA, Rivory LP, Brown SL, Liddle C, Clarke SJ, Robertson GR (2006) Transcriptional repression of hepatic cytochrome P450 3A4 gene in the presence of cancer. Clin Cancer Res 12(24):7492–7497.  https://doi.org/10.1158/1078-0432.CCR-06-0023. 12/24/7492 [pii]CrossRefPubMedGoogle Scholar
  201. 201.
    Helsby NA, Lo WY, Sharples K, Riley G, Murray M, Spells K, Dzhelai M, Simpson A, Findlay M (2008) CYP2C19 pharmacogenetics in advanced cancer: compromised function independent of genotype. Br J Cancer 99(8):1251–1255.  https://doi.org/10.1038/sj.bjc.6604699. 6604699 [pii]CrossRefPubMedCentralPubMedGoogle Scholar
  202. 202.
    Okuno H, Kitao Y, Takasu M, Kano H, Kunieda K, Seki T, Shiozaki Y, Sameshima Y (1990) Depression of drug metabolizing activity in the human liver by interferon-alpha. Eur J Clin Pharmacol 39(4):365–367PubMedGoogle Scholar
  203. 203.
    Williams SJ, Farrell GC (1986) Inhibition of antipyrine metabolism by interferon. Br J Clin Pharmacol 22(5):610–612PubMedCentralPubMedGoogle Scholar
  204. 204.
    Pageaux GP, le Bricquir Y, Berthou F, Bressot N, Picot MC, Blanc F, Michel H, Larrey D (1998) Effects of interferon-alpha on cytochrome P-450 isoforms 1A2 and 3A activities in patients with chronic hepatitis C. Eur J Gastroenterol Hepatol 10(6):491–495PubMedGoogle Scholar
  205. 205.
    Becquemont L, Chazouilleres O, Serfaty L, Poirier JM, Broly F, Jaillon P, Poupon R, Funck-Brentano C (2002) Effect of interferon alpha-ribavirin bitherapy on cytochrome P450 1A2 and 2D6 and N-acetyltransferase-2 activities in patients with chronic active hepatitis C. Clin Pharmacol Ther 71(6):488–495.  https://doi.org/10.1067/mcp.2002.124468. S0009923602000097 [pii]CrossRefPubMedGoogle Scholar
  206. 206.
    Islam M, Frye RF, Richards TJ, Sbeitan I, Donnelly SS, Glue P, Agarwala SS, Kirkwood JM (2002) Differential effect of IFNalpha-2b on the cytochrome P450 enzyme system: a potential basis of IFN toxicity and its modulation by other drugs. Clin Cancer Res 8(8):2480–2487PubMedGoogle Scholar
  207. 207.
    Ghany MG, Strader DB, Thomas DL, Seeff LB, American Association for the Study of Liver D (2009) Diagnosis, management, and treatment of hepatitis C: an update. Hepatology 49(4):1335–1374.  https://doi.org/10.1002/hep.22759 CrossRefPubMedGoogle Scholar
  208. 208.
    Brennan BJ, ZX X, Grippo JF (2013) Effect of peginterferon alfa-2a (40KD) on cytochrome P450 isoenzyme activity. Br J Clin Pharmacol 75(2):497–506.  https://doi.org/10.1111/j.1365-2125.2012.04373.x CrossRefPubMedGoogle Scholar
  209. 209.
    Gupta SK, Kolz K, Cutler DL (2011) Effects of multiple-dose pegylated interferon alfa-2b on the activity of drug-metabolizing enzymes in persons with chronic hepatitis C. Eur J Clin Pharmacol 67(6):591–599.  https://doi.org/10.1007/s00228-010-0972-5 CrossRefPubMedGoogle Scholar
  210. 210.
    Scavone C, Sportiello L, Rafaniello C, Mascolo A, Sessa M, Rossi F, Capuano A (2016) New era in treatment options of chronic hepatitis C: focus on safety of new direct-acting antivirals (DAAs). Expert Opin Drug Saf 15(sup2):85–100.  https://doi.org/10.1080/14740338.2016.1221396 CrossRefPubMedGoogle Scholar
  211. 211.
    AASLD-IDSA (2017) Recommendations for testing, managing and treating hepatitis C. http://www.hcvguidelines.org. Accessed 2 Feb 2017
  212. 212.
    Myers RP, Shah H, Burak KW, Cooper C, Feld JJ (2015) An update on the management of chronic hepatitis C: 2015 Consensus guidelines from the Canadian Association for the Study of the Liver. Can J Gastroenterol Hepatol 29(1):19–34PubMedCentralPubMedGoogle Scholar
  213. 213.
    Burgess S, Partovi N, Yoshida EM, Erb SR, Azalgara VM, Hussaini T (2015) Drug interactions with direct-acting antivirals for hepatitis C: implications for HIV and transplant patients. Ann Pharmacother 49(6):674–687.  https://doi.org/10.1177/1060028015576180 CrossRefPubMedGoogle Scholar
  214. 214.
    Micromedex® 2.0 (electronic version). Truven Health Analytics, Greenwood Village. http://www.micromedexsolutions.com/. Accessed 2 Feb 2017
  215. 215.
    Reesink HW, Fanning GC, Farha KA, Weegink C, Van Vliet A, Van ‘t Klooster G, Lenz O, Aharchi F, Marien K, Van Remoortere P, de Kock H, Broeckaert F, Meyvisch P, Van Beirendonck E, Simmen K, Verloes R (2010) Rapid HCV-RNA decline with once daily TMC435: a phase I study in healthy volunteers and hepatitis C patients. Gastroenterology 138(3):913–921.  https://doi.org/10.1053/j.gastro.2009.10.033 CrossRefPubMedGoogle Scholar
  216. 216.
    Kumar D (2010) Emerging viruses in transplantation. Curr Opin Infect Dis 23(4):374–378.  https://doi.org/10.1097/QCO.0b013e32833bc19d. 00001432-201008000-00013 [pii]CrossRefPubMedGoogle Scholar
  217. 217.
    Sayegh MH, Carpenter CB (2004) Transplantation 50 years later--progress, challenges, and promises. N Engl J Med 351(26):2761–2766.  https://doi.org/10.1056/NEJMon043418. 351/26/2761 [pii]CrossRefPubMedGoogle Scholar
  218. 218.
    Dharnidharka VR, Stablein DM, Harmon WE (2004) Post-transplant infections now exceed acute rejection as cause for hospitalization: a report of the NAPRTCS. Am J Transplant 4(3):384–389PubMedGoogle Scholar
  219. 219.
    Monforte V, Bullich S, Pou L, Bravo C, Lopez R, Gavalda J, Roman A (2003) Blood cyclosporine C0 and C2 concentrations and cytomegalovirus infections following lung transplantation. Transplant Proc 35(5):1992–1993. doi:S0041134503006894 [pii]PubMedGoogle Scholar
  220. 220.
    Kuypers DR, Claes K, Evenepoel P, Maes B, Vanrenterghem Y (2004) Clinical efficacy and toxicity profile of tacrolimus and mycophenolic acid in relation to combined long-term pharmacokinetics in de novo renal allograft recipients. Clin Pharmacol Ther 75(5):434–447.  https://doi.org/10.1016/j.clpt.2003.12.009. S0009923603007707 [pii]CrossRefPubMedGoogle Scholar
  221. 221.
    Latorre A, Morales E, Gonzalez E, Herrero JC, Ortiz M, Sierra P, Dominguez-Gil B, Torres A, Munoz MA, Andres A, Manzanares C, Morales JM (2002) Clinical management of renal transplant patients with hepatitis C virus infection treated with cyclosporine or tacrolimus. Transplant Proc 34(1):63–64. doi:S0041134501026781 [pii]PubMedGoogle Scholar
  222. 222.
    Mignogna MD, Fedele S, Lo Russo L, Bonadies G, Nappa S, Lo Muzio L (2005) Acute cyclosporine nephrotoxicity in a patient with oral pemphigus vulgaris and HIV infection on antiretroviral therapy. J Am Acad Dermatol 53(6):1089–1090.  https://doi.org/10.1016/j.jaad.2005.07.054. S0190-9622(05)02326-1 [pii]CrossRefPubMedGoogle Scholar
  223. 223.
    Vercauteren SB, Bosmans JL, Elseviers MM, Verpooten GA, De Broe ME (1998) A meta-analysis and morphological review of cyclosporine-induced nephrotoxicity in auto-immune diseases. Kidney Int 54(2):536–545.  https://doi.org/10.1046/j.1523-1755.1998.00017.x CrossRefPubMedGoogle Scholar
  224. 224.
    Strehlau J, Pape L, Offner G, Nashan B, Ehrich JH (2000) Interleukin-2 receptor antibody-induced alterations of ciclosporin dose requirements in paediatric transplant recipients. Lancet 356(9238):1327–1328PubMedGoogle Scholar
  225. 225.
    Elkahwaji J, Robin MA, Berson A, Tinel M, Letteron P, Labbe G, Beaune P, Elias D, Rougier P, Escudier B, Duvillard P, Pessayre D (1999) Decrease in hepatic cytochrome P450 after interleukin-2 immunotherapy. Biochem Pharmacol 57(8):951–954PubMedGoogle Scholar
  226. 226.
    Kuek A, Hazleman BL, Ostor AJ (2007) Immune-mediated inflammatory diseases (IMIDs) and biologic therapy: a medical revolution. Postgrad Med J 83(978):251–260.  https://doi.org/10.1136/pgmj.2006.052688. 83/978/251 [pii]CrossRefPubMedCentralPubMedGoogle Scholar
  227. 227.
    Keizer RJ, Huitema AD, Schellens JH, Beijnen JH (2010) Clinical pharmacokinetics of therapeutic monoclonal antibodies. Clin Pharmacokinet 49(8):493–507.  https://doi.org/10.2165/11531280-000000000-00000 CrossRefPubMedGoogle Scholar
  228. 228.
    Reichert JM (2016) Antibodies to watch in 2016. MAbs 8(2):197–204.  https://doi.org/10.1080/19420862.2015.1125583 CrossRefPubMedGoogle Scholar
  229. 229.
    Morgan ET (2009) Impact of infectious and inflammatory disease on cytochrome P450-mediated drug metabolism and pharmacokinetics. Clin Pharmacol Ther 85(4):434–438.  https://doi.org/10.1038/clpt.2008.302. clpt2008302 [pii]CrossRefPubMedCentralPubMedGoogle Scholar
  230. 230.
    Gupta R, JJ W, Levin E, Koo JY, Liao W (2013) Possible drug-drug interaction between adalimumab and duloxetine and/or pregabalin in a psoriasis patient. J Drugs Dermatol 12(10):1089PubMedGoogle Scholar
  231. 231.
    Zhou H, Parks V, Patat A, Le Coz F, Simcoe D, Korth-Bradley J (2004) Absence of a clinically relevant interaction between etanercept and digoxin. J Clin Pharmacol 44(11):1244–1251.  https://doi.org/10.1177/0091270004268050. 44/11/1244 [pii]CrossRefPubMedGoogle Scholar
  232. 232.
    Zhou H, Patat A, Parks V, Buckwalter M, Metzger D, Korth-Bradley J (2004) Absence of a pharmacokinetic interaction between etanercept and warfarin. J Clin Pharmacol 44(5):543–550.  https://doi.org/10.1177/0091270004264164. 44/5/543 [pii]CrossRefPubMedGoogle Scholar
  233. 233.
    Lee EB, Daskalakis N, Xu C, Paccaly A, Miller B, Fleischmann R, Bodrug I, Kivitz A (2016) Disease-drug interaction of sarilumab and simvastatin in patients with rheumatoid arthritis. Clin Pharmacokinet.  https://doi.org/10.1007/s40262-016-0462-8
  234. 234.
    Zhuang Y, de Vries DE, Xu Z, Marciniak SJ Jr, Chen D, Leon F, Davis HM, Zhou H (2015) Evaluation of disease-mediated therapeutic protein-drug interactions between an anti-interleukin-6 monoclonal antibody (sirukumab) and cytochrome P450 activities in a phase 1 study in patients with rheumatoid arthritis using a cocktail approach. J Clin Pharmacol 55(12):1386–1394.  https://doi.org/10.1002/jcph.561 CrossRefPubMedGoogle Scholar
  235. 235.
    Tran JQ, Othman AA, Wolstencroft P, Elkins J (2016) Therapeutic protein-drug interaction assessment for daclizumab high-yield process in patients with multiple sclerosis using a cocktail approach. Br J Clin Pharmacol 82(1):160–167.  https://doi.org/10.1111/bcp.12936 CrossRefPubMedCentralPubMedGoogle Scholar
  236. 236.
    Enioutina EY, Bareyan D, Daynes RA (2009) TLR-induced local metabolism of vitamin D3 plays an important role in the diversification of adaptive immune responses. J Immunol 182(7):4296–4305PubMedGoogle Scholar
  237. 237.
    Pellegrino P, Perrotta C, Clementi E, Radice S (2015) Vaccine-drug interactions: cytokines, cytochromes, and molecular mechanisms. Drug Saf 38(9):781–787.  https://doi.org/10.1007/s40264-015-0330-8 CrossRefPubMedGoogle Scholar
  238. 238.
    Kuo AM, Brown JN, Clinard V (2012) Effect of influenza vaccination on international normalized ratio during chronic warfarin therapy. J Clin Pharm Ther 37(5):505–509.  https://doi.org/10.1111/j.1365-2710.2012.01341.x CrossRefPubMedGoogle Scholar
  239. 239.
    Raaska K, Neuvonen PJ (2014) Infections and possible vaccine-drug interactions. Eur J Clin Pharmacol 70(7):889–890.  https://doi.org/10.1007/s00228-014-1688-8 CrossRefPubMedGoogle Scholar
  240. 240.
    Scavone JM, Blyden GT, Greenblatt DJ (1989) Lack of effect of influenza vaccine on the pharmacokinetics of antipyrine, alprazolam, paracetamol (acetaminophen) and lorazepam. Clin Pharmacokinet 16(3):180–185.  https://doi.org/10.2165/00003088-198916030-00004 CrossRefPubMedGoogle Scholar
  241. 241.
    Pasanen M, Rannala Z, Tooming A, Sotaniemi EA, Pelkonen O, Rautio A (1997) Hepatitis A impairs the function of human hepatic CYP2A6 in vivo. Toxicology 123(3):177–184. doi:S0300483X97001194 [pii]PubMedGoogle Scholar
  242. 242.
    Anolik R, Kolski GB, Schaible DH, Ratner J (1982) Transient alteration of theophylline half-life: possible association with Herpes simplex infection. Ann Allergy 49(2):109–111PubMedGoogle Scholar
  243. 243.
    Trenholme GM, Williams RL, Rieckmann KH, Frischer H, Carson PE (1976) Quinine disposition during malaria and during induced fever. Clin Pharmacol Ther 19(4):459–467PubMedGoogle Scholar
  244. 244.
    Masimirembwa CM, Beke M, Hasler JA, Tang BK, Kalow W (1995) Low CYP1A2 activity in rural Shona children of Zimbabwe. Clin Pharmacol Ther 57(1):25–31.  https://doi.org/10.1016/0009-9236(95)90262-7. 0009-9236(95)90262-7 [pii]CrossRefPubMedGoogle Scholar
  245. 245.
    Satarug S, Lang MA, Yongvanit P, Sithithaworn P, Mairiang E, Mairiang P, Pelkonen P, Bartsch H, Haswell-Elkins MR (1996) Induction of cytochrome P450 2A6 expression in humans by the carcinogenic parasite infection, opisthorchiasis viverrini. Cancer Epidemiol Biomark Prev 5(10):795–800Google Scholar
  246. 246.
    Shedlofsky SI, Israel BC, McClain CJ, Hill DB, Blouin RA (1994) Endotoxin administration to humans inhibits hepatic cytochrome P450-mediated drug metabolism. J Clin Invest 94(6):2209–2214.  https://doi.org/10.1172/JCI117582 CrossRefPubMedCentralPubMedGoogle Scholar
  247. 247.
    Shedlofsky SI, Israel BC, Tosheva R, Blouin RA (1997) Endotoxin depresses hepatic cytochrome P450-mediated drug metabolism in women. Br J Clin Pharmacol 43(6):627–632PubMedCentralPubMedGoogle Scholar
  248. 248.
    Haas CE, Kaufman DC, Jones CE, Burstein AH, Reiss W (2003) Cytochrome P450 3A4 activity after surgical stress. Crit Care Med 31(5):1338–1346.  https://doi.org/10.1097/01.CCM.0000063040.24541.49 CrossRefPubMedGoogle Scholar
  249. 249.
    Carcillo JA, Doughty L, Kofos D, Frye RF, Kaplan SS, Sasser H, Burckart GJ (2003) Cytochrome P450 mediated-drug metabolism is reduced in children with sepsis-induced multiple organ failure. Intensive Care Med 29(6):980–984.  https://doi.org/10.1007/s00134-003-1758-3 CrossRefPubMedGoogle Scholar
  250. 250.
    Novotny AR, Emmanuel K, Maier S, Westerholt A, Weighardt H, Stadler J, Bartels H, Schwaiger M, Siewert JR, Holzmann B, Heidecke CD (2007) Cytochrome P450 activity mirrors nitric oxide levels in postoperative sepsis: predictive indicators of lethal outcome. Surgery 141(3):376–384.  https://doi.org/10.1016/j.surg.2006.08.011. S0039-6060(06)00568-X [pii]CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  • Kerry B. Goralski
    • 2
    • 1
  • Matthew A. Ladda
    • 2
  • Jenna O. McNeil
    • 3
  1. 1.Department of PharmacologyDalhousie UniversityHalifaxCanada
  2. 2.College of Pharmacy, Faculty of Health Professions, Dalhousie UniversityHalifaxCanada
  3. 3.Department of Family MedicineDalhousie UniversityHalifaxCanada

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