The transport of nifurtimox, an anti-trypanosomal drug, in an in vitro model of the human blood-brain barrier: Evidence for involvement of breast cancer resistance protein

Brain Research

Volumn 1436, Issue , 2012, Pages 111-121

  Watson, Christopher P ^a   Dogruel, Murat ^a   Mihoreanu, Larisa ^a   Begley, David J ^a   Weksler, Babette B ^b   Couraud, Pierre O ^c,d,e   Romero, Ignacio A ^f   Thomas, Sarah A ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c INSTITUT COCHIN   (France)

^d CNRS   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f OPEN UNIVERSITY   (United Kingdom)

Author keywords

Blood brain barrier; Breast cancer resistance protein; Eflornithine; Human African trypanosomiasis; Nifurtimox

Indexed keywords

1,2,3,4,6,7,12,12A OCTAHYDRO 6 ISOBUTYL 9 METHOXY 1,4 DIOXOPYRAZINO[1',2':1,6]PYRIDO[3,4 B]INDOLE 3 PROPANOIC ACID TERT BUTYL ESTER; 4 AMINOHIPPURIC ACID; BREAST CANCER RESISTANCE PROTEIN; CARRIER PROTEIN; DEXAMETHASONE; EFLORNITHINE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOPROTEIN P; HALOPERIDOL; INDOMETACIN; MELARSOPROL; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 2; NIFURTIMOX; ORGANIC ANION TRANSPORTER; PENTAMIDINE; PHEOPHORBIDE; PROBENECID; SURAMIN; TAUROCHOLIC ACID; TRITON X 100;

AFRICAN TRYPANOSOMIASIS; ARTICLE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; DISEASE COURSE; DRUG ACCUMULATION; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG TRANSPORT; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL;

ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; CELL LINE; HUMANS; NEOPLASM PROTEINS; NIFURTIMOX; ORGANIC ANION TRANSPORTERS; TRYPANOCIDAL AGENTS; VON WILLEBRAND FACTOR;

EID: 84856022612     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2011.11.053     Document Type: Article

References (51)

1. N.J. Abbott, L. Ronnback, and E. Hansson Astrocyte-endothelial interactions at the blood-brain barrier Nat. Rev. Neurosci. 7 2006 41 53 (Pubitemid 41828930)
2. B. Bouteille, O. Oukem, S. Bisser, and M. Dumas Treatment perspectives for human African trypanosomiasis Fundam. Clin. Pharmacol. 17 2003 171 181 (Pubitemid 36513208)
3. R. Brun, J. Blum, F. Chappuis, and C. Burri Human African trypanosomiasis Lancet 375 2010 148 159
4. S.M. Carl, D.J. Lindley, P.O. Couraud, B.B. Weksler, I. Romero, S.A. Mowery, and G.T. Knipp ABC and SLC transporter expression and pot substrate characterization across the human CMEC/D3 blood-brain barrier cell line Mol. Pharm. 7 2010 1057 1068
5. F. Checchi, P. Piola, H. Ayikoru, F. Thomas, D. Legros, and G. Priotto Nifurtimox plus Eflornithine for late-stage sleeping sickness in Uganda: a case series PLoS Negl. Trop. Dis. 1 2007 e64
6. M. Chishty, D.J. Begley, N.J. Abbott, and A. Reichel Interaction of nucleoside analogues with nucleoside transporters in rat brain endothelial cells J. Drug Target. 12 2004 265 272 (Pubitemid 39294867)
7. S. Dauchy, F. Miller, P.O. Couraud, R.J. Weaver, B. Weksler, I.A. Romero, J.M. Scherrmann, I. De Waziers, and X. Decleves Expression and transcriptional regulation of ABC transporters and cytochromes P450 in hCMEC/D3 human cerebral microvascular endothelial cells Biochem. Pharmacol. 77 2009 897 909
8. F. Elahian, F. Kalalinia, and J. Behravan Evaluation of indomethacin and dexamethasone effects on BCRP-mediated drug resistance in MCF-7 parental and resistant cell lines Drug Chem. Toxicol. 33 2010 113 119
9. F. Garcia-Bournissen, J. Altcheh, A. Panchaud, and S. Ito Is use of nifurtimox for the treatment of Chagas disease compatible with breast feeding? A population pharmacokinetics analysis Arch. Dis. Child. 95 2010 224 228
10. J.E. Gibbs, and S.A. Thomas The distribution of the anti-HIV drug, 2′3′-dideoxycytidine (ddC), across the blood-brain and blood-cerebrospinal fluid barriers and the influence of organic anion transport inhibitors J. Neurochem. 80 2002 392 404 (Pubitemid 36383023)
11. R. Gonnert, and M. Bock The effect of nifurtimox on Trypanosoma cruzi in tissue cultures Arzneimittelforschung 22 1972 1582 1586
12. A. Haberkorn The effect of nifurtimox on experimental infections with trypanosomatidae other than Trypanosoma cruzi Zentralbl. Bakteriol. Orig. A 244 1979 331 338 (Pubitemid 9247240)
13. A. Haberkorn, and R. Gonnert Animal experimental investigation into the activity of nifurtimox against Trypanosoma cruzi Arzneimittelforschung 22 1972 1570 1582
14. S. Jeganathan, L. Sanderson, M. Dogruel, J. Rodgers, S. Croft, and S.A. Thomas The distribution of nifurtimox across the healthy and trypanosome-infected murine blood-brain and blood-CSF barriers J. Pharmacol. Exp. Ther. 336 2011 506 515
15. L. Jorgensen, J. Van Beek, S. Lund, A. Schousboe, and L. Badolo Evidence of Oatp and Mdr1 in cryopreserved rat hepatocytes Eur. J. Pharm. Sci. 30 2007 181 189 (Pubitemid 46149281)
16. K. Kristensson, M. Nygard, G. Bertini, and M. Bentivoglio African trypanosome infections of the nervous system: parasite entry and effects on sleep and synaptic functions Prog. Neurobiol. 91 2010 152 171
17. V. Lutje, J. Seixas, and A. Kennedy Chemotherapy for second-stage Human African trypanosomiasis Cochrane Database Syst. Rev. 8 2010 CD006201
18. P.J. Mark, and B.J. Waddell P-glycoprotein restricts access of cortisol and dexamethasone to the glucocorticoid receptor in placental BeWo cells Endocrinology 147 2006 5147 5152 (Pubitemid 44790568)
19. B.L. Mason, C.M. Pariante, and S.A. Thomas A revised role for P-glycoprotein in the brain distribution of dexamethasone, cortisol, and corticosterone in wild-type and ABCB1A/B-deficient mice Endocrinology 149 2008 5244 5253
20. P. Matsson, J.M. Pedersen, U. Norinder, C.A. Bergstrom, and P. Artursson Identification of novel specific and general inhibitors of the three major human ATP-binding cassette transporters P-gp, BCRP and MRP2 among registered drugs Pharm. Res. 26 2009 1816 1831
21. G. Merino, J.W. Jonker, E. Wagenaar, A.E. Van Herwaarden, and A.H. Schinkel The breast cancer resistance protein (BCRP/ABCG2) affects pharmacokinetics, hepatobiliary excretion, and milk secretion of the antibiotic nitrofurantoin Mol. Pharmacol. 67 2005 1758 1764 (Pubitemid 40594177)
22. G. Merino, A.I. Alvarez, M.M. Pulido, A.J. Molina, A.H. Schinkel, and J.G. Prieto Breast cancer resistance protein (BCRP/ABCG2) transports fluoroquinolone antibiotics and affects their oral availability, pharmacokinetics, and milk secretion Drug Metab. Dispos. 34 2006 690 695
23. F. Moens, M. De Wilde, and K. Ngato Clinical trial of nifurtimox in human African trypanosomiasis Ann. Soc. Belg. Med. Trop. 64 1984 37 43 (Pubitemid 14143746)
24. V.S. Narang, C. Fraga, N. Kumar, J. Shen, S. Throm, C.F. Stewart, and C.M. Waters Dexamethasone increases expression and activity of multidrug resistance transporters at the rat blood-brain barrier Am. J. Physiol. Cell Physiol. 295 2008 C440 C450
25. T. Nozawa, H. Minami, S. Sugiura, A. Tsuji, and I. Tamai Role of organic anion transporter OATP1B1 (OATP-C) in hepatic uptake of irinotecan and its active metabolite, 7-ethyl-10-hydroxycamptothecin: in vitro evidence and effect of single nucleotide polymorphisms Drug Metab. Dispos. 33 2005 434 439 (Pubitemid 40279945)
26. G. Pan, N. Giri, and W.F. Elmquist Abcg2/Bcrp1 mediates the polarized transport of antiretroviral nucleosides abacavir and zidovudine Drug Metab. Dispos. 35 2007 1165 1173 (Pubitemid 46956438)
27. J.M. Parepally, H. Mandula, and Q.R. Smith Brain uptake of nonsteroidal anti-inflammatory drugs: ibuprofen, flurbiprofen, and indomethacin Pharm. Res. 23 2006 873 881 (Pubitemid 43781395)
28. B. Poller, H. Gutmann, S. Krahenbuhl, B. Weksler, I. Romero, P.O. Couraud, G. Tuffin, J. Drewe, and J. Huwyler The human brain endothelial cell line hCMEC/D3 as a human blood-brain barrier model for drug transport studies J. Neurochem. 107 2008 1358 1368
29. H. Potschka, S. Baltes, and W. Loscher Inhibition of multidrug transporters by verapamil or probenecid does not alter blood-brain barrier penetration of levetiracetam in rats Epilepsy Res. 58 2004 85 91 (Pubitemid 38553945)
30. G. Priotto, S. Kasparian, D. Ngouama, S. Ghorashian, U. Arnold, S. Ghabri, and U. Karunakara Nifurtimox-eflornithine combination therapy for second-stage Trypanosoma brucei gambiense sleeping sickness: a randomized clinical trial in Congo Clin. Infect. Dis. 45 2007 1435 1442 (Pubitemid 351411872)
31. G. Priotto, S. Kasparian, W. Mutombo, D. Ngouama, S. Ghorashian, U. Arnold, S. Ghabri, E. Baudin, V. Buard, S. Kazadi-Kyanza, M. Ilunga, W. Mutangala, G. Pohlig, C. Schmid, U. Karunakara, E. Torreele, and V. Kande Nifurtimox-eflornithine combination therapy for second-stage African Trypanosoma brucei gambiense trypanosomiasis: a multicentre, randomised, phase III, non-inferiority trial Lancet 374 2009 56 64
32. C. Rosenbaum, S. Rohrs, O. Muller, and H. Waldmann Modulation of MRP-1-mediated multidrug resistance by indomethacin analogues J. Med. Chem. 48 2005 1179 1187 (Pubitemid 40270460)
33. L. Sanderson, A. Khan, and S. Thomas Distribution of suramin, an antitrypanosomal drug, across the blood-brain and blood-cerebrospinal fluid interfaces in wild-type and P-glycoprotein transporter-deficient mice Antimicrob. Agents Chemother. 51 2007 3136 3146 (Pubitemid 350067520)
34. L. Sanderson, M. Dogruel, J. Rodgers, B. Bradley, and S.A. Thomas The blood-brain barrier significantly limits eflornithine entry into Trypanosoma brucei brucei infected mouse brain J. Neurochem. 107 2008 1136 1146
35. L. Sanderson, M. Dogruel, J. Rodgers, H.P. De Koning, and S.A. Thomas Pentamidine movement across the murine blood-brain and blood-cerebrospinal fluid barriers: effect of trypanosome infection, combination therapy, P-glycoprotein, and multidrug resistance-associated protein J. Pharmacol. Exp. Ther. 329 2009 967 977
36. M. Sands, M.A. Kron, and R.B. Brown Pentamidine: a review Rev. Infect. Dis. 7 1985 625 634
37. S.W. Sauer, S. Opp, A. Mahringer, M.M. Kaminski, C. Thiel, J.G. Okun, G. Fricker, M.A. Morath, and S. Kolker Glutaric aciduria type I and methylmalonic aciduria: simulation of cerebral import and export of accumulating neurotoxic dicarboxylic acids in in vitro models of the blood-brain barrier and the choroid plexus Biochim. Biophys. Acta 1802 2010 552 560
38. M.T. Schram, N. Chaturvedi, C. Schalkwijk, F. Giorgino, P. Ebeling, J.H. Fuller, and C.D. Stehouwer Vascular risk factors and markers of endothelial function as determinants of inflammatory markers in type 1 diabetes: the EURODIAB prospective complications study Diabetes Care 26 2003 2165 2173 (Pubitemid 41184269)
39. D. Sugiyama, H. Kusuhara, Y. Shitara, T. Abe, P.J. Meier, T. Sekine, H. Endou, H. Suzuki, and Y. Sugiyama Characterization of the efflux transport of 17beta-estradiol-D-17beta-glucuronide from the brain across the blood-brain barrier J. Pharmacol. Exp. Ther. 298 2001 316 322 (Pubitemid 32574542)
40. M. Suzuki, H. Suzuki, Y. Sugimoto, and Y. Sugiyama ABCG2 transports sulfated conjugates of steroids and xenobiotics J. Biol. Chem. 278 2003 22644 22649 (Pubitemid 36830322)
41. L.M. Tai, A.J. Loughlin, D.K. Male, and I.A. Romero P-glycoprotein and breast cancer resistance protein restrict apical-to-basolateral permeability of human brain endothelium to amyloid-beta J. Cereb. Blood Flow Metab. 29 2009 1079 1083
42. L.M. Tai, P.S. Reddy, M.A. Lopez-Ramirez, H.A. Davies, D.K. Male, A.J. Loughlin, and I.A. Romero Polarized P-glycoprotein expression by the immortalised human brain endothelial cell line, hCMEC/D3, restricts apical-to-basolateral permeability to rhodamine 123 Brain Res. 1292 2009 14 24
43. K. Ueda, N. Okamura, M. Hirai, Y. Tanigawara, T. Saeki, N. Kioka, T. Komano, and R. Hori Human P-glycoprotein transports cortisol, aldosterone, and dexamethasone, but not progesterone J. Biol. Chem. 267 1992 24248 24252
44. S. Van Nieuwenhove Advances in sleeping sickness therapy Ann. Soc. Belg. Med. Trop. 72 Suppl 1 1992 39 51
45. S. Vander Borght, J. Van Pelt, H. Van Malenstein, D. Cassiman, M. Renard, C. Verslype, L. Libbrecht, and T.A. Roskams Up-regulation of breast cancer resistance protein expression in hepatoblastoma following chemotherapy: a study in patients and in vitro Hepatol. Res. 38 2008 1112 1121
46. Q. Wang, B. Liang, N.A. Shirwany, and M.H. Zou 2-Deoxy-d-glucose treatment of endothelial cells induces autophagy by reactive oxygen species-mediated activation of the AMP-activated protein kinase PLoS One 6 2011 e17234
47. J. Weiss, J. Rose, C.H. Storch, N. Ketabi-Kiyanvash, A. Sauer, W.E. Haefeli, and T. Efferth Modulation of human BCRP (ABCG2) activity by anti-HIV drugs J. Antimicrob. Chemother. 59 2007 238 245 (Pubitemid 47072063)
48. B.B. Weksler, E.A. Subileau, N. Perriere, P. Charneau, K. Holloway, M. Leveque, H. Tricoire-Leignel, A. Nicotra, S. Bourdoulous, P. Turowski, D.K. Male, F. Roux, J. Greenwood, I.A. Romero, and P.O. Couraud Blood-brain barrier-specific properties of a human adult brain endothelial cell line FASEB J. 19 2005 1872 1874 (Pubitemid 41598779)
49. M. Whiteman, D.C. Hooper, G.S. Scott, H. Koprowski, and B. Halliwell Inhibition of hypochlorous acid-induced cellular toxicity by nitrite Proc. Natl. Acad. Sci. U. S. A. 99 2002 12061 12066
50. K.A. Wojtal, E. De Vries, D. Hoekstra, and S.C. Van Ijzendoorn Efficient trafficking of MDR1/P-glycoprotein to apical canalicular plasma membranes in HepG2 cells requires PKA-RIIalpha anchoring and glucosylceramide Mol. Biol. Cell 17 2006 3638 3650 (Pubitemid 44156455)
51. O. Yun, G. Priotto, J. Tong, L. Flevaud, and F. Chappuis NECT is next: implementing the new drug combination therapy for Trypanosoma brucei gambiense sleeping sickness PLoS Negl. Trop. Dis. 4 2010 e720