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Molecular & Biochemical Parasitology
journal homepage: www.elsevier.com/locate/molbiopara
Genome-wide identification of ABC transporters in monogeneans
Víctor Caña-Bozada
a
, F. Neptalí Morales-Serna
a,b,
*, Alejandra García-Gasca
a
, Raúl Llera-Herrera
c
,
Emma J. Fajer-Ávila
a
a
Centro de Investigación en Alimentación y Desarrollo, Unidad Mazatlán en Acuicultura y Manejo Ambiental, Mazatlán 82112, Sinaloa, Mexico
b
Consejo Nacional de Ciencia y Tecnología (CONACYT), Ciudad de México, Mexico
c
Unidad Académica Mazatlán, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mazatlán 82040, Sinaloa, Mexico
ARTICLE INFO
Keywords:
Platyhelminthes
Flatworms
Fish parasite
Detoxification
In silico
ABC genes
ABSTRACT
ATP-Binding Cassette (ABC) transporters are proteins that actively mediate the transport of a wide variety of
molecules, including drugs. Thus, in parasitology, ABC transporters have gained attention as potential targets for
therapeutic drugs. Among the parasitic Platyhelminthes, ABC transporters have been identified and classified in
a few species of Trematoda and Cestoda but not in Monogenea. Monogeneans are mainly ectoparasites of marine
and freshwater fish, although they can also be found on other aquatic organisms. Severe epizootics caused by
monogeneans have been reported around the world, mainly in confined and/or overcrowded fish. The purpose
of this study was to identify the ABC transporters in four species of monogeneans (Gyrodactylus salaris,
Protopolystoma xenopodis, Eudiplozoon nipponicum and Neobenedenia melleni) for which genomic resources are
publicly available. For comparative purposes, ABC transporters were also identified in endoparasitic
(Schistosoma mansoni and Echinococcus granulosus) and free-living (Macrostomun lignano and Schmidtea medi-
terranea) platyhelminths. Thirty-two putative ABC transporters were identified in the genome of G. salaris, 40 in
the genome of P. xenopodis, 46 in the transcriptome of E. nipponicum and 9 in a rather limited ESTs set available
for N. melleni. Of the eight ABC subfamilies (A–H) known in metazoans, subfamily H was the only one not found
in any monogenean species. In contrast, ABCC was the best represented subfamily. Phylogenetic analyses
showed a few cases of one-to-one orthologous relationships, which agree with results from other metazoan
species. We found some monogenean ABC members related to subfamilies B, C and G involved in drug resistance
in humans. This information may be useful for future functional studies on ABC transporters in monogeneans.
1. Introduction
All organisms have cellular mechanisms of detoxification that
comprise the biotransformation and transport of toxic xenobiotics, in-
cluding drugs. Among transporter proteins, the ATP-Binding Cassette
(ABC) transporters have been recognized by their ability to translocate
a variety of substrates, as well as by their ubiquity, with both influx and
efflux functions in prokaryotes but only efflux function in eukaryotes
([1] and references therein). The ABC transporters exist on plasma
membranes and intracellular compartments. In many genomes, the ABC
gene family is the largest family of transporters, which splits into eight
subfamilies, designated ABCA through ABCH, although humans have
only seven subfamilies (ABCA–ABCG) and plants do not have ABCH but
ABCI [2,3]. These proteins contain typically two conserved domains:
nucleotide binding domain (NBD) and transmembrane domain (TMD).
The NBD binds and hydrolyzes ATP to generate the energy required by
the TMD to create a pore for translocation of substrates through the
membrane [4].
ABC transporters have gained attention as anti-parasitic drug tar-
gets. In parasitic platyhelminths (particularly trematodes), the few
studies have been mostly focused on identification and characterization
of ABCB and ABCC given their involvement in parasite resistance to
different drugs [5,6]. Nonetheless, all other subfamilies have also been
found, except for ABCD and ABCH in Schistosoma spp., and ABCE and
ABCH in Opisthorchis felineus [5,7]. Interestingly, it was found that in-
hibitors of mammalian ABC transporters suppressed the activity of P-
glycoproteins (Pgp, member of the subfamily ABCB) in O. felineus,
preventing the removal of xenobiotics from the parasite [7].
On this basis, we consider that studies related to ABC transporters
should be also performed in flatworms of the class Monogenea, which
are mostly ectoparasites of aquatic organisms, infecting mainly gills,
skin and fins of marine and freshwater fish around the world. There are
https://doi.org/10.1016/j.molbiopara.2019.111234
Received 13 August 2019; Received in revised form 2 November 2019; Accepted 7 November 2019
⁎
Corresponding author at: Centro de Investigación en Alimentación y Desarrollo, Unidad Mazatlán en Acuicultura y Manejo Ambiental, Mazatlán 82112, Sinaloa,
Mexico.
E-mail address: francisco.morales@ciad.mx (F.N. Morales-Serna).
Molecular & Biochemical Parasitology 234 (2019) 111234
Available online 09 November 2019
0166-6851/ © 2019 Elsevier B.V. All rights reserved.
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