Abcc4 together with Abcb1 and Abcg2 form a robust cooperative drug efflux system that restricts the brain entry of camptothecin analogues

Clinical Cancer Research

Volumn 19, Issue 8, 2013, Pages 2084-2095

  Lin, Fan ^a   Marchetti, Serena ^a,c   Pluim, Dick ^a   Iusuf, Dilek ^a   Mazzanti, Roberto ^c   Schellens, Jan H M ^a,b   Beijnen, Jos H ^a,b   Van Tellingen, Olaf ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; CAMPTOTHECIN DERIVATIVE; CARBOXYLESTERASE; ELACRIDAR; FIRTECAN; GIMATECAN; IRINOTECAN; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 4; TOPOTECAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; CONCENTRATION RESPONSE; CONTINUOUS INFUSION; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG BRAIN LEVEL; DRUG DISTRIBUTION; DRUG PENETRATION; DRUG TRANSPORT; ENZYME ACTIVITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; INTRACRANIAL TUMOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; WILD TYPE;

ACRIDINES; ADMINISTRATION, INTRAVENOUS; ADMINISTRATION, ORAL; ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; ATP-BINDING CASSETTE TRANSPORTERS; BLOOD-BRAIN BARRIER; BRAIN; CAMPTOTHECIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; MICE; MICE, KNOCKOUT; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; P-GLYCOPROTEIN; TETRAHYDROISOQUINOLINES; TOPOTECAN;

EID: 84877097707     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-12-3105     Document Type: Article

References (42)

1. de Boer AG, Gaillard PJ. Drug targeting to the brain. Annu Rev Pharmacol Toxicol 2007;47:323-55.
2. Agarwal S, Sane R, Oberoi R, Ohlfest JR, Elmquist WF. Delivery of molecularly targeted therapy to malignant glioma, a disease of the whole brain. Expert Rev Mol Med 2011;13:e17.
3. Muldoon LL, Soussain C, Jahnke K, Johanson C, Siegal T, Smith QR, et al. Chemotherapy delivery issues in central nervous system malignancy: a reality check. J Clin Oncol 2007;25:2295-305. (Pubitemid 46954658)
4. de Vries NA, Beijnen JH, Boogerd W, van Tellingen O. Blood-brain barrier and chemotherapeutic treatment of brain tumors. Expert Rev Neurother 2006;6:1199-209. (Pubitemid 44231977)
5. Urquhart BL, Kim RB. Blood-brain barrier transporters and response to CNS-active drugs. Eur J Clin Pharmacol 2009;65:1063-70.
6. Deeken JF, Loscher W. The blood-brain barrier and cancer: transporters, treatment, and trojan horses. Clin Cancer Res 2007;13:1663-74. (Pubitemid 46952931)
7. Schinkel AH, Smit JJ, van Tellingen O, Beijnen JH, Wagenaar E, van Deemter L, et al. Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 1994;77:491-502. (Pubitemid 24153990)
8. de Vries NA, Zhao J, Kroon E, Buckle T, Beijnen JH, van Tellingen O. P-glycoprotein and breast cancer resistance protein: two dominant transporters working together in limiting the brain penetration of topotecan. Clin Cancer Res 2007;13:6440-9. (Pubitemid 350075034)
9. Devore R III, Johnson D, Crawford J, Dimery I, Eckardt J, Eckhardt SG. Irinotecan plus cisplatin in patients with advanced non-small-cell lung cancer. Oncology (Williston Park) 1998;12:79-83.
10. Gershenson DM. Irinotecan in epithelial ovarian cancer. Oncology (Williston Park) 2002;16:29-31.
11. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 2004;350:2335-42. (Pubitemid 38702844)
12. Chu XY, Suzuki H, Ueda K, Kato Y, Akiyama S, Sugiyama Y. Active efflux of CPT-11 and its metabolites in human KB-derived cell lines. J Pharmacol Exp Ther 1999;288:735-41. (Pubitemid 29119689)
13. Nakatomi K, Yoshikawa M, Oka M, Ikegami Y, Hayasaka S, Sano K, et al. Transport of 7-ethyl-10-hydroxycamptothecin (SN-38) by breast cancer resistance protein ABCG2 in human lung cancer cells. Biochem Biophys Res Commun 2001;288:827-32. (Pubitemid 33140956)
14. Smith NF, Figg WD, Sparreboom A. Pharmacogenetics of irinotecan metabolism and transport: an update. Toxicol In Vitro 2006;20:163-75. (Pubitemid 43087700)
15. Maliepaard M, van Gastelen MA, de Jong LA, Pluim D, van Waardenburg RC, Ruevekamp-Helmers MC, et al. Overexpression of the BCRP/MXR/ABCP gene in a topotecan-selected ovarian tumor cell line. Cancer Res 1999;59:4559-63. (Pubitemid 29428958)
16. Hendricks CB, Rowinsky EK, Grochow LB, Donehower RC, Kaufmann SH. Effect of P-glycoprotein expression on the accumulation and cytotoxicity of topotecan (SK&F 104864), a new camptothecin analogue. Cancer Res 1992;52:2268-78.
17. Marchetti S, Oostendorp RL, Pluim D, van Eijndhoven M, van Tellingen O, Schinkel AH, et al. In vitro transport of gimatecan (7-t- butoxyiminomethylcamptothecin) by breast cancer resistance protein, P-glycoprotein, and multidrug resistance protein 2. Mol Cancer Ther 2007;6:3307-13.
18. Gounder MK, Nazar AS, Saleem A, Pungaliya P, Kulkarni D, Versace R, et al. Effects of drug efflux proteins and topoisomerase I mutations on the camptothecin analogue gimatecan. Invest New Drugs 2008;26:205-13. (Pubitemid 351579682)
19. Perego P, De Cesare M, De Isabella P, Carenini N, Beggiolin G, Pezzoni G, et al. A novel 7-modified camptothecin analog overcomes breast cancer resistance protein-associated resistance in a mitoxantrone-selected colon carcinoma cell line. Cancer Res 2001;61:6034-7. (Pubitemid 32762534)
20. Leggas M, Adachi M, Scheffer GL, Sun D, Wielinga P, Du G, et al. Mrp4 confers resistance to topotecan and protects the brain from chemotherapy. Mol Cell Biol 2004;24:7612-21. (Pubitemid 39121487)
21. Borst P, de Wolf C, van de Wetering K. Multidrug resistance-associated proteins 3, 4, and 5. Pflugers Arch 2007;453:661-73. (Pubitemid 46192537)
22. Tian Q, Zhang J, Chan SY, Tan TM, Duan W, Huang M, et al. Topotecan is a substrate for multidrug resistance associated protein 4. Curr Drug Metab 2006;7:105-18.
23. Tian Q, Zhang J, Tan TM, Chan E, Duan W, Chan SY, et al. Human multidrug resistance associated protein 4 confers resistance to camptothecins. Pharm Res 2005;22:1837-53. (Pubitemid 41504337)
24. Russel FG, Koenderink JB, Masereeuw R. Multidrug resistance protein 4 (MRP4/ABCC4): a versatile efflux transporter for drugs and signalling molecules. Trends Pharmacol Sci 2008;29:200-7.
25. Ose A, Ito M, Kusuhara H, Yamatsugu K, Kanai M, Shibasaki M, et al. Limited brain distribution of [3R,4R,5S]-4-acetamido-5-amino-3-(1-ethylpropoxy)- 1-cyclohexene-1-carboxylate phosphate (Ro 64-0802), a pharmacologically active form of oseltamivir, by active efflux across the blood-brain barrier mediated by organic anion transporter 3 (Oat3/Slc22a8) and multidrug resistance-associated protein 4 (Mrp4/Abcc4). Drug Metab Dispos 2009;37:315-21.
26. Morimoto K, Nakakariya M, Shirasaka Y, Kakinuma C, Fujita T, Tamai I, et al. Oseltamivir (Tamiflu) efflux transport at the blood-brain barrier via P-glycoprotein. Drug Metab Dispos 2008;36:6-9.
27. Dai H, Marbach P, Lemaire M, Hayes M, Elmquist WF. Distribution of STI-571 to the brain is limited by P-glycoprotein-mediated efflux. J Pharmacol Exp Ther 2003;304:1085-92. (Pubitemid 36254421)
28. Schoemaker NE, Rosing H, Jansen S, Schellens JH, Beijnen JH. High-performance liquid chromatographic analysis of the anticancer drug irinotecan (CPT-11) and its active metabolite SN-38 in human plasma. Ther Drug Monit 2003;25:120-4. (Pubitemid 36139838)
29. de Vries NA, Ouwehand M, Buckle T, Beijnen JH, van Tellingen O. Determination of topotecan in human and mouse plasma and in mouse tissue homogenates by reversed-phase high-performance liquid chromatography. Biomed Chromatogr 2007;21:1191-200. (Pubitemid 350200900)
30. Guemei AA, Cottrell J, Band R, Hehman H, Prudhomme M, Pavlov MV, et al. Human plasma carboxylesterase and butyrylcholinesterase enzyme activity: correlations with SN-38 pharmacokinetics during a prolonged infusion of irinotecan. Cancer Chemother Pharmacol 2001;47:283-90. (Pubitemid 32640767)
31. Zhang Y, Han H, Elmquist WF, Miller DW. Expression of various multidrug resistance-associated protein (MRP) homologues in brain microvessel endothelial cells [In Process Citation]. Brain Res 2000;876:148-53.
32. Kodaira H, Kusuhara H, Ushiki J, Fuse E, Sugiyama Y. Kinetic analysis of the cooperation of P-glycoprotein (P-gp/Abcb1) and breast cancer resistance protein (Bcrp/Abcg2) in limiting the brain and testis penetration of erlotinib, flavopiridol, and mitoxantrone. J Pharmacol Exp Ther 2010;333:788-96.
33. Polli JW, Olson KL, Chism JP, John-Williams LS, Yeager RL, Woodard SM, et al. An unexpected synergist role of P-glycoprotein and breast cancer resistance protein on the central nervous system penetration of the tyrosine kinase inhibitor lapatinib (N-{3-chloro-4-[(3-fluorobenzyl)oxy]phenyl}-6-[5-({[2- (methylsulfonyl)ethyl]amino}methyl)-2-furyl]-4-quinazolinamine; GW572016). Drug Metab Dispos 2009;37:439-42.
34. Reardon DA, Friedman HS, Powell JB Jr, Gilbert M, Yung WK. Irinotecan: promising activity in the treatment of malignant glioma. Oncology (Williston Park) 2003;17:9-14.
35. Reardon DA, Quinn JA, Rich JN, Gururangan S, Vredenburgh J, Sampson JH, et al. Phase 2 trial of BCNU plus irinotecan in adults with malignant glioma. Neuro Oncol 2004;6:134-44. (Pubitemid 38455760)
36. Reardon DA, Quinn JA, Rich JN, Desjardins A, Vredenburgh J, Gururangan S, et al. Phase I trial of irinotecan plus temozolomide in adults with recurrent malignant glioma. Cancer 2005;104:1478-86. (Pubitemid 41356163)
37. Reardon DA, Quinn JA, Vredenburgh J, Rich JN, Gururangan S, Badruddoja M, et al. Phase II trial of irinotecan plus celecoxib in adults with recurrent malignant glioma. Cancer 2005;103:329-38. (Pubitemid 40129293)
38. Rivory LP, Haaz MC, Canal P, Lokiec F, Armand JP, Robert J. Pharmacokinetic interrelationships of irinotecan (CPT-11) and its three major plasma metabolites in patients enrolled in phase I/II trials. Clin Cancer Res 1997;3:1261-6. (Pubitemid 27362386)
39. Zamboni WC, Houghton PJ, Thompson J, Cheshire PJ, Hanna SK, Richmond LB, et al. Altered irinotecan and SN-38 disposition after intravenous and oral administration of irinotecan in mice bearing human neuroblastoma xenografts. Clin Cancer Res 1998;4:455-62. (Pubitemid 28122763)
40. De Cesare M, Pratesi G, Veneroni S, Bergottini R, Zunino F. Efficacy of the novel camptothecin gimatecan against orthotopic and metastatic human tumor xenograft models. Clin Cancer Res 2004;10:7357-64. (Pubitemid 39487725)
41. Agarwal S, Sane R, Gallardo JL, Ohlfest JR, Elmquist WF. Distribution of gefitinib to the brain is limited by P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2)-mediated active efflux. J Pharmacol Exp Ther 2010;334:147-55.
42. Tang SC, Lagas JS, Lankheet NA, Poller B, Hillebrand MJ, Rosing H, et al. Brain accumulation of sunitinib is restricted by P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2) and can be enhanced by oral elacridar and sunitinib coadministration. Int J Cancer 2012;130:223-33.