Differential activation of human constitutive androstane receptor and its SV23 and SV24 splice variants by rilpivirine and etravirine

British Journal of Pharmacology

Volumn 172, Issue 5, 2015, Pages 1263-1276

  Sharma, Devinder ^a   Lau, Aik Jiang ^a   Sherman, Matthew A ^b   Chang, Thomas K H ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b Triangle Laboratories Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONSTITUTIVE ANDROSTANE RECEPTOR; CONSTITUTIVE ANDROSTANE RECEPTOR SV23 SPLICE VARIANT; CONSTITUTIVE ANDROSTANE RECEPTOR SV24 SPLICE VARIANT; CYTOCHROME P450 2B6; DELAVIRDINE; EFAVIRENZ; ETRAVIRINE; GREEN FLUORESCENT PROTEIN; NEVIRAPINE; RILPIVIRINE; UNCLASSIFIED DRUG; CELL RECEPTOR; CYP2B6 PROTEIN, HUMAN; PYRIDAZINE DERIVATIVE; RNA DIRECTED DNA POLYMERASE INHIBITOR;

ADOLESCENT; ADULT; AGED; ARTICLE; CONTROLLED STUDY; CYP2B6 GENE; DRUG EFFECT; FEMALE; GENE EXPRESSION; GENETIC TRANSFECTION; HEPG2 CELL LINE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LIVER CELL; MALE; PLASMID; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR ACTIVATION; RECEPTOR INTRINSIC ACTIVITY; REVERSE TRANSCRIPTION; RNA ISOLATION; WILD TYPE; AGONISTS; ALTERNATIVE RNA SPLICING; CHEMICAL STRUCTURE; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; GENETICS; HEP-G2 CELL LINE; METABOLISM; STRUCTURE ACTIVITY RELATION; TUMOR CELL CULTURE; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; ALTERNATIVE SPLICING; CYTOCHROME P-450 CYP2B6; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HEP G2 CELLS; HEPATOCYTES; HUMANS; MALE; MOLECULAR STRUCTURE; PYRIDAZINES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; REVERSE TRANSCRIPTASE INHIBITORS; RILPIVIRINE; STRUCTURE-ACTIVITY RELATIONSHIP; TUMOR CELLS, CULTURED; YOUNG ADULT;

EID: 84922813250     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12997     Document Type: Article

References (57)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013a). The Concise Guide to PHARMACOLOGY 2013/14: Nuclear hormone receptors. Br J Pharmacol 170: 1652-1675.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013b). The Concise Guide to PHARMACOLOGY 2013/14: Catalytic receptors. Br J Pharmacol 170: 1676-1705.
3. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013c). The Concise Guide to PHARMACOLOGY 2013/14: Enzymes. Br J Pharmacol 170: 1797-1867.
4. Arasteh K, Rieger A, Yeni P, Pozniak A, Boogaerts G, van Heeswijk R, et al. (2009). Short-term randomized proof-of-principle trial of TMC278 in patients with HIV type-1 who have previously failed antiretroviral therapy. Antivir Ther 14: 713-722.
5. Arnold KA, Eichelbaum M, Burk O, (2004). Alternative splicing affects the function and tissue-specific expression of the human constitutive androstane receptor. Nucl Recept 2: 1-16.
6. Auerbach SS, Ramsden R, Stoner MA, Verlinde C, Hassett C, Omiecinski CJ, (2003). Alternatively spliced isoforms of the human constitutive androstane receptor. Nucleic Acids Res 31: 3194-3207.
7. Auerbach SS, Stoner MA, Su S, Omiecinski CJ, (2005). Retinoid X receptor-alpha-dependent transactivation by a naturally occurring structural variant of human constitutive androstane receptor (NR1I3). Mol Pharmacol 68: 1239-1253.
8. Burk O, Arnold KA, Nussler AK, Schaeffeler E, Efimova E, Avery BA, et al. (2005). Antimalarial artemisinin drugs induce cytochrome P450 and MDR1 expression by activation of xenosensors pregnane X receptor and constitutive androstane receptor. Mol Pharmacol 67: 1954-1965.
9. Camacho R, Teofilo E, (2011). Antiretroviral therapy in treatment-naive patients with HIV infection. Curr Opin HIV AIDS 6 (Suppl. 1): S3-S11.
10. Chang TKH, Waxman DJ, (2006). Synthetic drugs and natural products as modulators of constitutive androstane receptor (CAR) and pregnane X receptor (PXR). Drug Metab Rev 38: 51-73.
11. Chang TKH, Yu L, Maurel P, Waxman DJ, (1997). Enhanced cyclophosphamide and ifosfamide activation in primary human hepatocyte cultures: response to cytochrome P-450 inducers and autoinduction by oxazaphosphorines. Cancer Res 57: 1946-1954.
12. Chang TKH, Bandiera SM, Chen J, (2003). Constitutive androstane receptor and pregnane X receptor gene expression in human liver: interindividual variability and correlation with CYP2B6 mRNA levels. Drug Metab Dispos 31: 7-10.
13. Chen T, Tompkins LM, Li L, Li H, Kim G, Zheng Y, et al. (2010). A single amino acid controls the functional switch of human constitutive androstane receptor (CAR) 1 to the xenobiotic-sensitive splicing variant CAR3. J Pharmacol Exp Ther 332: 106-115.
14. Choi EJ, Jang YJ, Cha EY, Shin JG, Lee SS, (2013). Identification and characterization of novel alternative splice variants of human constitutive androstane receptor in liver samples of Koreans and Caucasians. Drug Metab Dispos 41: 888-896.
15. De Clercq E, (2009). Anti-HIV drugs: 25 compounds approved within 25 years after the discovery of HIV. Int J Antimicrob Agents 33: 307-320.
16. De Clercq E, (2012). Where rilpivirine meets with tenofovir, the start of a new anti-HIV drug combination era. Biochem Pharmacol 84: 241-248.
17. DeKeyser JG, Stagliano MC, Auerbach SS, Prabhu KS, Jones AD, Omiecinski CJ, (2009). Di(2-ethylhexyl) phthalate is a highly potent agonist for the human constitutive androstane receptor splice variant CAR2. Mol Pharmacol 75: 1005-1013.
18. DeKeyser JG, Laurenzana EM, Peterson EC, Chen T, Omiecinski CJ, (2011). Selective phthalate activation of naturally occurring human constitutive androstane receptor splice variants and the pregnane X receptor. Toxicol Sci 120: 381-391.
19. Dring AM, Anderson LE, Qamar S, Stoner MA, (2010). Rational quantitative structure-activity relationship (RQSAR) screen for PXR and CAR isoform-specific nuclear receptor ligands. Chem Biol Interact 188: 512-525.
20. Erickson DA, Mather G, Trager WF, Levy RH, Keirns JJ, (1999). Characterization of the in vitro biotransformation of the HIV-1 reverse transcriptase inhibitor nevirapine by human hepatic cytochromes P-450. Drug Metab Dispos 27: 1488-1495.
21. Faucette SR, Zhang TC, Moore R, Sueyoshi T, Omiecinski CJ, LeCluyse EL, et al. (2007). Relative activation of human pregnane X receptor versus constitutive androstane receptor defines distinct classes of CYP2B6 and CYP3A4 inducers. J Pharmacol Exp Ther 320: 72-80.
22. Fofana DB, Soulie C, Maiga AI, Fourati S, Malet I, Wirden M, et al. (2013). Genetic barrier to the development of resistance to rilpivirine and etravirine between HIV-1 subtypes CRF02-AG and B. J Antimicrob Chemother 68: 2515-2520.
23. Gagliardini R, Fabbiani M, Fortuna S, Visconti E, Navarra P, Cauda R, et al. (2014). Pharmacokinetics of etravirine in HIV-infected patients concomitantly treated with rifampin for tuberculosis. Infection 42: 775-778.
24. Gazzard B, Duvivier C, Zagler C, Castagna A, Hill A, van Delft Y, et al. (2011). Phase 2 double-blind, randomized trial of etravirine versus efavirenz in treatment-naive patients: 48-week results. AIDS 25: 2249-2258.
25. Goebel F, Yakovlev A, Pozniak AL, Vinogradova E, Boogaerts G, Hoetelmans R, et al. (2006). Short-term antiviral activity of TMC278-a novel NNRTI-in treatment-naive HIV-1-infected subjects. AIDS 20: 1721-1726.
26. Hesse LM, Venkatakrishnan K, Court MH, von Moltke LL, Duan SX, Shader RI, et al. (2000). CYP2B6 mediates the in vitro hydroxylation of bupropion: potential drug interactions with other antidepressants. Drug Metab Dispos 28: 1176-1183.
27. Hesse LM, von Moltke LL, Shader RI, Greenblatt DJ, (2001). Ritonavir, efavirenz, and nelfinavir inhibit CYP2B6 activity in vitro: potential drug interactions with bupropion. Drug Metab Dispos 29: 100-102.
28. Jauregui HO, Hayner NT, Driscoll JL, Williams-Holland R, Lipsky MH, Galletti PM, (1981). Trypan blue dye uptake and lactate dehydrogenase in adult rat hepatocytes-freshly isolated cells, cell suspensions, and primary monolayer cultures. In Vitro 17: 1100-1110.
29. Jiang M, Xie W, (2013). Role of the constitutive androstane receptor in obesity and type 2 diabetes: a case study of the endobiotic function of a xenobiotic receptor. Drug Metab Rev 45: 156-163.
30. Jinno H, Tanaka-Kagawa T, Hanioka N, Ishida S, Saeki M, Soyama A, et al. (2004). Identification of novel alternative splice variants of human constitutive androstane receptor and characterization of their expression in the liver. Mol Pharmacol 65: 496-502.
31. Kodama S, Negishi M, (2013). PXR cross-talks with internal and external signals in physiological and pathophysiological responses. Drug Metab Rev 45: 300-310.
32. Lamba J, Lamba V, Schuetz E, (2005). Genetic variants of PXR (NR1I2) and CAR (NR1I3) and their implications in drug metabolism and pharmacogenetics. Curr Drug Metab 6: 369-383.
33. Lang TA, Talerico C, Siontis GC, (2012). Documenting clinical and laboratory images in publications: the CLIP principles. Chest 141: 1626-1632.
34. Lau AJ, Chang TKH, (2009). Inhibition of human CYP2B6-catalyzed bupropion hydroxylation by Ginkgo biloba extract: effect of terpene trilactones and flavonols. Drug Metab Dispos 37: 1931-1937.
35. Lau AJ, Chang TKH, (2013). Indirect activation of the SV23 and SV24 splice variants of human constitutive androstane receptor: analysis with 3-hydroxyflavone and its analogues. Br J Pharmacol 170: 403-414.
36. Lau AJ, Chang TKH, (2014). Fetal bovine serum and human constitutive androstane receptor: evidence for activation of the SV23 splice variant by artemisinin, artemether, and arteether in a serum-free cell culture system. Toxicol Appl Pharmacol 277: 221-230.
37. Lau AJ, Yang G, Chang TKH, (2011a). Isoform-selective activation of human constitutive androstane receptor by Ginkgo biloba extract: functional analysis of the SV23, SV24, and SV25 splice variants. J Pharmacol Exp Ther 339: 704-715.
38. Lau AJ, Yang G, Rajaraman G, Baucom CC, Chang TKH, (2011b). Differential effect of meclizine on the activity of human pregnane X receptor and constitutive androstane receptor. J Pharmacol Exp Ther 336: 816-826.
39. Li H, Chen T, Cottrell J, Wang H, (2009). Nuclear translocation of adenoviral-enhanced yellow fluorescent protein-tagged-human constitutive androstane receptor (hCAR): a novel tool for screening hCAR activators in human primary hepatocytes. Drug Metab Dispos 37: 1098-1106.
40. Maglich JM, Parks DJ, Moore LB, Collins JL, Goodwin B, Billin AN, et al. (2003). Identification of a novel human constitutive androstane receptor (CAR) agonist and its use in the identification of CAR target genes. J Biol Chem 278: 17277-17283.
41. Moore LB, Parks DJ, Jones SA, Bledsoe RK, Consler TG, Stimmel JB, et al. (2000). Orphan nuclear receptors constitutive androstane receptor and pregnane X receptor share xenobiotic and steroid ligands. J Biol Chem 275: 15122-15127.
42. Mutoh S, Sobhany M, Moore R, Perera L, Pedersen L, Sueyoshi T, et al. (2013). Phenobarbital indirectly activates the constitutive active androstane receptor (CAR) by inhibition of epidermal growth factor receptor signaling. Sci Signal 6: ra31.
43. Nanzigu S, Eriksen J, Makumbi F, Lanke S, Mahindi M, Kiguba R, et al. (2012). Pharmacokinetics of the nonnucleoside reverse transcriptase inhibitor efavirenz among HIV-infected Ugandans. HIV Med 13: 193-201.
44. Omiecinski CJ, Coslo DM, Chen T, Laurenzana EM, Peffer RC, (2011). Multi-species analyses of direct activators of the constitutive androstane receptor. Toxicol Sci 123: 550-562.
45. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, et al.; NC-IUPHAR (2014). The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledgebase of drug targets and their ligands. Nucl Acids Res 42 (Database Issue): D1098-106.
46. Qiu H, Durand K, Rabinovitch-Chable H, Rigaud M, Gazaille V, Clavere P, et al. (2007). Gene expression of HIF-1alpha and XRCC4 measured in human samples by real-time RT-PCR using the sigmoidal curve-fitting method. Biotechniques 42: 355-362.
47. Robertson SM, Maldarelli F, Natarajan V, Formentini E, Alfaro RM, Penzak SR, (2008). Efavirenz induces CYP2B6-mediated hydroxylation of bupropion in healthy subjects. J Acquir Immune Defic Syndr 49: 513-519.
48. Santos JR, Llibre JM, Domingo P, Imaz A, Ferrer E, Podzamczer D, et al. (2011). Short communication: high effectiveness of etravirine in routine clinical practice in treatment-experienced HIV type 1-infected patients. AIDS Res Hum Retroviruses 27: 713-717.
49. Sharma D, Lau AJ, Sherman MA, Chang TKH, (2013). Agonism of human pregnane X receptor by rilpivirine and etravirine: comparison with first generation non-nucleoside reverse transcriptase inhibitors. Biochem Pharmacol 85: 1700-1711.
50. Simpson DA, Feeney S, Boyle C, Stitt AW, (2000). Retinal VEGF mRNA measured by SYBR green I fluorescence: A versatile approach to quantitative PCR. Mol Vis 6: 178-183.
51. Sueyoshi T, Kawamoto T, Zelko I, Honkakoski P, Negishi M, (1999). The repressed nuclear receptor CAR responds to phenobarbital in activating the human CYP2B6 gene. J Biol Chem 274: 6043-6046.
52. Svard J, Spiers JP, Mulcahy F, Hennessy M, (2010). Nuclear receptor-mediated induction of CYP450 by antiretrovirals: functional consequences of NR1I2 (PXR) polymorphisms and differential prevalence in whites and sub-Saharan Africans. J Acquir Immune Defic Syndr 55: 536-549.
53. Usach I, Melis V, Peris JE, (2013). Non-nucleoside reverse transcriptase inhibitors: a review on pharmacokinetics, pharmacodynamics, safety and tolerability. J Int AIDS Soc 16: 1-14.
54. Wang H, Faucette S, Moore R, Sueyoshi T, Negishi M, LeCluyse E, (2004). Human constitutive androstane receptor mediates induction of CYP2B6 gene expression by phenytoin. J Biol Chem 279: 29295-29301.
55. Ward BA, Gorski JC, Jones DR, Hall SD, Flockhart DA, Desta Z, (2003). The cytochrome P450 2B6 (CYP2B6) is the main catalyst of efavirenz primary and secondary metabolism: implication for HIV/AIDS therapy and utility of efavirenz as a substrate marker of CYP2B6 catalytic activity. J Pharmacol Exp Ther 306: 287-300.
56. Weiss J, Haefeli WE, (2013). Potential of the novel antiretroviral drug rilpivirine to modulate the expression and function of drug transporters and drug-metabolising enzymes in vitro. Int J Antimicrob Agents 41: 484-487.
57. Yang H, Wang H, (2014). Signaling control of the constitutive androstane receptor (CAR). Protein Cell 5: 113-123.