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Functional Expression of Tcoat1 Reveals It to Be a P1-Type Nucleoside Transporter with No Capacity for Diminazene Uptake

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Functional Expression of Tcoat1 Reveals It to Be a P1-Type Nucleoside Transporter with No Capacity for Diminazene Uptake Edinburgh Research Explorer Functional expression of TcoAT1 reveals it to be a P1-type nucleoside transporter with no capacity for diminazene uptake Citation for published version: Munday, JC, Rojas López, KE, Eze, AA, Delespaux, V, Van Den Abbeele, J, Rowan, T, Barrett, MP, Morrison, LJ & de Koning, HP 2013, 'Functional expression of TcoAT1 reveals it to be a P1-type nucleoside transporter with no capacity for diminazene uptake', International Journal for Parasitology: Drugs and Drug Resistance, vol. 3, pp. 69-76. https://doi.org/10.1016/j.ijpddr.2013.01.004 Digital Object Identifier (DOI): 10.1016/j.ijpddr.2013.01.004 Link: Link to publication record in Edinburgh Research Explorer Document Version: Publisher's PDF, also known as Version of record Published In: International Journal for Parasitology: Drugs and Drug Resistance Publisher Rights Statement: This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial- ShareAlike License, which permits non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited. General rights Copyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorer content complies with UK legislation. If you believe that the public display of this file breaches copyright please contact [email protected] providing details, and we will remove access to the work immediately and investigate your claim. Download date: 27. Sep. 2021 International Journal for Parasitology: Drugs and Drug Resistance 3 (2013) 69–76 Contents lists available at SciVerse ScienceDirect International Journal for Parasitology: Drugs and Drug Resistance journal homepage: www.elsevier.com/locate/ijpddr Functional expression of TcoAT1 reveals it to be a P1-type nucleoside transporter with no capacity for diminazene uptake q Jane C. Munday a,b, Karla E. Rojas López b, Anthonius A. Eze b, Vincent Delespaux c, ⇑ Jan Van Den Abbeele c, Tim Rowan d, Michael P. Barrett a,b, Liam J. Morrison a,b,e, Harry P. de Koning b, a Wellcome Trust Centre for Molecular Parasitology, University of Glasgow, Glasgow, United Kingdom b Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom c Institute of Tropical Medicine, Nationalestraat 155, B-2000 Antwerp, Belgium d GALVmed, Pentlands Science Park, Bush Loan, Edinburgh, United Kingdom e Roslin Institute, University of Edinburgh, Easter Bush, Midlothian, United Kingdom article info abstract Article history: It has long been established that the Trypanosoma brucei TbAT1/P2 aminopurine transporter is involved in Received 14 December 2012 the uptake of diamidine and arsenical drugs including pentamidine, diminazene aceturate and melarso- Received in revised form 19 January 2013 prol. Accordingly, it was proposed that the closest Trypanosoma congolense paralogue, TcoAT1, might per- Accepted 23 January 2013 form the same function in this parasite, and an apparent correlation between a Single Nucleotide Available online 10 February 2013 Polymorphism (SNP) in that gene and diminazene tolerance was reported for the strains examined. Here, we report the functional cloning and expression of TcoAT1 and show that in fact it is the syntenic homo- Keywords: logue of another T. brucei gene of the same Equilibrative Nucleoside Transporter (ENT) family: TbNT10. Trypanosoma congolense The T. congolense genome does not seem to contain a syntenic equivalent to TbAT1. Two TcoAT1 alleles, Diminazene aceturate Drug resistance differentiated by three independent SNPs, were expressed in the T. brucei clone B48, a TbAT1-null strain TcoAT1 that further lacks the High Affinity Pentamidine Transporter (HAPT1); TbAT1 was also expressed as a con- trol. The TbAT1 and TcoAT1 transporters were functional and increased sensitivity to cytotoxic nucleoside analogues. However, only TbAT1 increased sensitivity to diamidines and to cymelarsan. Uptake of [3H]- diminazene was detectable only in the B48 cells expressing TbAT1 but not TcoAT1, whereas uptake of [3H]-inosine was increased by both TcoAT1 alleles but not by TbAT1. Uptake of [3H]-adenosine was increased by all three ENT genes. We conclude that TcoAT1 is a P1-type purine nucleoside transporter and the syntenic equivalent to the previously characterised TbNT10; it does not mediate diminazene uptake and is therefore unlikely to play a role in diminazene resistance in T. congolense. Ó 2013 Australian Society for Parasitology Published by Elsevier Ltd. All rights reserved. 1. Introduction 35 million doses are administered annually (Geerts and Holmes, 1998). However, the effectiveness of DA and the only other com- The most common drug to treat animal trypanosomiasis in sub- mon drug for trypanosomiasis, isometamidium chloride, are threa- Saharan Africa is the diamidine compound diminazene aceturate tened by drug resistance (Geerts et al., 2001; Delespaux et al., (DA) and the effective treatment of livestock with trypanocides re- 2008a). In order to manage the situation effectively, it is necessary mains of the highest importance for farmers in the tsetse belt to understand the resistance mechanism and devise predictive where an estimated 46–62 million head of cattle are at risk of try- tests that distinguish between drug sensitive and resistant popula- panosomiasis (Swallow, 2000). Control of the disease is largely tions (Delespaux et al., 2008a). either by vector control or chemotherapy, of which an estimated The diamidine trypanocides were developed in the late 1930s (Lourie and Yorke, 1939) and as early as 1944 Hawking reported that aromatic diamidines are actively accumulated by live but q This is an open-access article distributed under the terms of the Creative not by dead Trypanosoma brucei to intracellular concentrations Commons Attribution-NonCommercial-ShareAlike License, which permits non- commercial use, distribution, and reproduction in any medium, provided the up to three orders of magnitude higher than the extracellular con- original author and source are credited. centration (Hawking, 1944). He proposed that the massive drug ⇑ Corresponding author. Address: Institute of Infection, Immunity and Inflam- accumulation, not observed in the surrounding blood cells, was mation, College of Medical, Veterinary and Life Sciences, University of Glasgow, 120 the basis of the selective trypanocidal action. A similar accumula- University Place, Glasgow G12 8TA, United Kingdom. Tel.: +44 141 3303753; fax: +44 141 3306900. tion, apparently energy dependent, has also been reported for DA E-mail address: [email protected] (H.P. de Koning). (Girgis-Takla and James, 1974; De Koning et al., 2004) and for 2211-3207/$ - see front matter Ó 2013 Australian Society for Parasitology Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijpddr.2013.01.004 70 J.C. Munday et al. / International Journal for Parasitology: Drugs and Drug Resistance 3 (2013) 69–76 pentamidine (Damper and Patton, 1976), a related diamidine drug in T. congolense strains of the regions investigated. The observation used to treat human African trypanosomiasis (Delespaux and De that the RFLP-identified SNP was also common in T. congolense iso- Koning, 2007). Dependent on the extracellular concentration, lated from wildlife in areas with no history of prior trypanocide use about 50% of the uptake of pentamidine in T. b. brucei is mediated (Chitanga et al., 2011) does appear to show that this is a common by the TbAT1/P2 transporter (Carter et al., 1995; De Koning and polymorphism and unlikely to be the result of drug pressure. Jarvis, 2001; Bray et al., 2003). The rest is transported by a High Therefore, the similarity between TcoAT1 and TbAT1, and the Affinity Pentamidine Transporter (HAPT1) and a Low Affinity Pent- apparent association with DA-resistance in T. congolense are tem- amidine Transporter (LAPT1) (De Koning, 2001, 2008). However, pered by the lack of total correlation. Moreover, no functional the uptake of DA is almost exclusively through TbAT1/P2 (De Kon- expression or characterization has been performed for this mem- ing et al., 2004), with only a very minor contribution from HAPT1 ber of Equilibrative Nucleoside Transporter (ENT) family. In order (Teka et al., 2011). The most likely explanation for the differences to provide a definitive test on whether TcoAT1 is involved in in DA and pentamidine transport is the flexibility of the linker diamidine transport, and whether TcoAT1 mutations are involved chain between the pentamidine benzamidine ends, allowing the in resistance, we have expressed two separate TcoAT1 alleles molecule to assume many different conformations whereas the (‘sensitive’ and ‘resistant’) as well as TbAT1, in a well-character- diminazene structure is rigid, locking the benzamidine moieties ised DA-resistant TbAT1 null strain of T. b. brucei (Bridges et al., in a fixed position. 2007). There is abundant evidence that diamidine resistance in T. bru- cei complex species is linked to loss of transport (Delespaux and De 2. Materials and methods Koning, 2007). A stilbamidine-resistant T. b. rhodesiense strain was deficient in accumulation of the
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