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In silico identification of tetraspanins in monopisthocotylean (Platyhelminthes: Monogenea) parasites of fish

Published online by Cambridge University Press:  24 March 2022

V. Caña-Bozada*
Affiliation:
Centro de Investigación en Alimentación y Desarrollo, A.C., Mazatlán82112, Sinaloa, Mexico
F.N. Morales-Serna
Affiliation:
Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mazatlán82040, Sinaloa, Mexico
J.Á. Huerta-Ocampo
Affiliation:
Centro de Investigación en Alimentación y Desarrollo, Hermosillo83304, Sonora, Mexico Consejo Nacional de Ciencia y Tecnología (CONACYT), Mexico City, Mexico
A. Avalos-Soriano
Affiliation:
Centro de Investigación en Alimentación y Desarrollo, A.C., Mazatlán82112, Sinaloa, Mexico Consejo Nacional de Ciencia y Tecnología (CONACYT), Mexico City, Mexico
*
Author for correspondence: V. Caña-Bozada, E-mail: [email protected]

Abstract

Tetraspanins are a superfamily of transmembrane proteins that in flatworms have structural roles in the development, maturation or stability of the tegument. Several tetraspanins are considered as potential candidates for vaccines or drugs against helminths. Monopisthocotylean monogeneans are ectoparasites of fish that are health hazards for farmed fish. The aim of this study was to identify in silico putative tetraspanins in the genomic datasets of four monopisthocotylean species. The analysis predicted and classified 40 tetraspanins in Rhabdosynochus viridisi, 39 in Scutogyrus longicornis, 22 in Gyrodactylus salaris and 13 in Neobenedenia melleni, belonging to 13 orthologous groups. The high divergence of tetraspanins made it difficult to annotate their function. However, a conserved group was identified in different metazoan taxa. According to this study, metazoan tetraspanins can be divided into 17 monophyletic groups. Of the 114 monogenean tetraspanins, only seven were phylogenetically close to tetraspanins from non-platyhelminth metazoans, which suggests that this group of proteins shows rapid sequence divergence. The similarity of the monopisthocotylean tetraspanins was highest with trematodes, followed by cestodes and then free-living platyhelminths. In total, 27 monopisthocotylean-specific and 34 flatworm-specific tetraspanins were identified. Four monogenean tetraspanins were orthologous to TSP-1, which is a candidate for the development of vaccines and a potential pharmacological target in trematodes and cestodes. Although studies of tetraspanins in parasitic flatworms are scarce, this is an interesting group of proteins for the development of new methods to control monogeneans.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Andree, KB, Roque, A, Duncan, N, Gisbert, E, Estevez, A, Tsertou, MI and Katharios, P (2015) Diplectanum sciaenae (Van Beneden & Hesse, 1863) (Monogenea) infecting meagre, Argyrosomus regius (Asso, 1801) Broodstock in Catalonia, Spain. A case report. Veterinary Parasitology: Regional Studies and Reports 1, 7579.Google Scholar
Andreu, Z and Yáñez-Mó, M (2014) Tetraspanins in extracellular vesicle formation and function. Frontiers in Immunology 5, 442.Google ScholarPubMed
Capella-Gutiérrez, S, Silla-Martínez, JM and Gabaldón, T (2009) Trimal: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 19721973.Google ScholarPubMed
Dang, Z, Yagi, K, Oku, Y, et al. (2009) Evaluation of Echinococcus multilocularis tetraspanins as vaccine candidates against primary alveolar echinococcosis. Vaccine 27, 73397345.Google ScholarPubMed
Dang, Z, Yagi, K, Oku, Y, et al. (2012) A pilot study on developing mucosal vaccine against alveolar echinococcosis (AE) using recombinant tetraspanin 3: vaccine efficacy and immunology. PLoS Neglected Tropical Diseases 6, e1570.Google ScholarPubMed
Eyayu, T, Zeleke, AJ and Worku, L (2020) Current status and future prospects of protein vaccine candidates against Schistosoma mansoni infection. Parasite Epidemiology and Control 11, e00176.Google ScholarPubMed
Finn, RD, Coggill, P, Eberhardt, RY, Eddy, SR, Mistry, J and Mitchell, AL (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Research 44, D279D285.Google ScholarPubMed
García-Frigola, C, Burgaya, F, de Lecea, L and Soriano, E (2001) Pattern of expression of the tetraspanin Tspan-5 during brain development in the mouse. Mechanisms of Development 106, 207212.Google ScholarPubMed
Garcia-España, A, Chung, PJ, Sarkar, IN, Stiner, E, Sun, TT and DeSalle, R (2008) Appearance of new tetraspanin genes during vertebrate evolution. Genomics 91, 326334.Google ScholarPubMed
Goldberg, AF (2006) Role of peripherin/rds in vertebrate photoreceptor architecture and inherited retinal degenerations. International Review of Cytology 253, 131175.Google ScholarPubMed
Goldberg, AF (2013) Essential tetraspanin functions in the vertebrate retina. pp. 321343 in Berditchevski, F and Rubinstein, E (Eds) Tetraspanins. Dordrecht, Springer.Google Scholar
Hahn, C, Fromm, B and Bachmann, L (2014) Comparative genomics of flatworms (Platyhelminthes) reveals shared genomic features of ecto-and endoparastic neodermata. Genome Biology and Evolution 6, 11051117.Google ScholarPubMed
Hemler, ME (2003) Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annual Review of Cell and Developmental Biology 19, 397422.Google ScholarPubMed
Howe, KL, Bolt, BJ, Shafie, M, Kersey, P and Berriman, M (2017) Wormbase ParaSite − a comprehensive resource for helminth genomics. Molecular and Biochemical Parasitology 215, 210.Google ScholarPubMed
Huang, S, Tian, H, Chen, Z, Yu, T and Xu, A (2010) The evolution of vertebrate tetraspanins: Gene loss, retention, and massive positive selection after whole genome duplications. BMC Evolutionary Biology 10, 117.Google ScholarPubMed
Huang, S, Yuan, S, Dong, M, et al. (2005) The phylogenetic analysis of tetraspanins projects the evolution of cell–cell interactions from unicellular to multicellular organisms. Genomics 86, 674684.Google ScholarPubMed
Hu, D, Song, X, Xie, Y, et al. (2015) Molecular insights into a tetraspanin in the hydatid tapeworm Echinococcus granulosus. Parasites & Vectors 8, 110.Google ScholarPubMed
Iwai, K, Ishii, M, Ohshima, S, Miyatake, K and Saeki, Y (2007) Expression and function of transmembrane-4 superfamily (tetraspanin) proteins in osteoclasts: reciprocal roles of Tspan-5 and NET-6 during osteoclastogenesis. Allergology International 56, 457463.Google ScholarPubMed
Käll, L, Krogh, A and Sonnhammer, EL (2007) Advantages of combined transmembrane topology and signal peptide prediction—the Phobius web server. Nucleic Acids Research 35, W429W432.Google ScholarPubMed
Kalyaanamoorthy, S, Minh, BQ, Wong, TK, Von Haeseler, A and Jermiin, LS (2017) Modelfinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587589.Google ScholarPubMed
Karamatic Crew, V, Burton, N, Kagan, A, et al. (2004) CD151, the first member of the tetraspanin (TM4) superfamily detected on erythrocytes, is essential for the correct assembly of human basement membranes in kidney and skin. Blood 104, 22172223.Google ScholarPubMed
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772780.Google ScholarPubMed
Laumer, CE, Hejnol, A and Giribet, G (2015) Nuclear genomic signals of the ‘microturbellarian’ roots of platyhelminth evolutionary innovation. eLife 4, e05503.Google ScholarPubMed
Letunic, I and Bork, P (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Research 49, W293W296.Google ScholarPubMed
Levy, S and Shoham, T (2005) The tetraspanin web modulates immune-signaling complexes. Nature Reviews Immunology 5, 136148.Google Scholar
Li, W and Godzik, A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 16581659.Google ScholarPubMed
Lok, JB, Shao, H, Massey, HC and Li, X (2017) Transgenesis in Strongyloides and related parasitic nematodes: historical perspectives, current functional genomic applications, and progress towards gene disruption and editing. Parasitology 144, 327342.Google ScholarPubMed
Loukas, A, Tran, M and Pearson, MS (2007) Schistosome membrane proteins as vaccines. International Journal for Parasitology 37, 257263.Google ScholarPubMed
Maecker, HT, Todd, SC and Levy, S (1997) The tetraspanin superfamily: molecular facilitators. The FASEB Journal 11, 428442.Google ScholarPubMed
McVeigh, P, McCusker, P, Robb, E, et al. (2018) Reasons to be nervous about flukicide discovery. Trends in Parasitology 34, 184196.Google ScholarPubMed
Mousavi, SM, Afgar, A, Mohammadi, MA, Mortezaei, S, Faridi, A, Sadeghi, B and Fasihi Harandi, M (2020) Biological and morphological consequences of dsRNA-induced suppression of tetraspanin mRNA in developmental stages of Echinococcus granulosus. Parasites & Vectors 13, 110.Google ScholarPubMed
Navarro-Hernandez, IC, López-Ortega, O, Acevedo-Ochoa, E, et al. (2020) Tetraspanin 33 (TSPAN33) regulates endocytosis and migration of human B lymphocytes by affecting the tension of the plasma membrane. The FEBS Journal 287, 34493471.Google Scholar
Nguyen, LT, Schmidt, HA, Von Haeseler, A and Minh, BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268274.Google ScholarPubMed
Ogawa, K (2015) Diseases of cultured marine fishes caused by Platyhelminthes (Monogenea, Digenea, Cestoda). Parasitology 142, 178195.Google Scholar
Pike, AW and Wink, R (1986) Aspects of photoreceptor structure and phototactic behavior in Platyhelminthes, with particular reference to the symbiotic turbellarian Paravortex. Hydrobiologia 132, 101104.Google Scholar
Piratae, S, Tesana, S, Jones, MK, et al. (2012) Molecular characterization of a tetraspanin from the human liver fluke, Opisthorchis viverrini. PLoS Neglected Tropical Diseases 6, e1939.Google ScholarPubMed
Potter, SC, Luciani, A, Eddy, SR, Park, Y, Lopez, R and Finn, RD (2018) HMMER web server: 2018 update. Nucleic Acids Research 46, W200W204.Google ScholarPubMed
Seigneuret, M, Conjeaud, H, Zhang, HT and Kong, XP (2013) Structural bases for tetraspanin functions. pp. 129 in Berditchevski F and Rubinstein E (Eds) Tetraspanins. Dordrecht, Springer.Google Scholar
Shinn, A, Pratoomyot, J, Bron, J, Paladini, G, Brooker, E and Brooker, A (2015) Economic impacts of aquatic parasites on global finfish production. Global Aquaculture Advocate 2015, 5861.Google Scholar
Tran, MH, Pearson, MS, Bethony, JM, et al. (2006) Tetraspanins on the surface of Schistosoma mansoni are protective antigens against schistosomiasis. Nature Medicine 12, 835840.Google ScholarPubMed
Tran, MH, Freitas, TC, Cooper, L, et al. (2010) Suppression of mRNAs encoding tegument tetraspanins from Schistosoma mansoni results in impaired tegument turnover. PLoS Pathogens 6, e1000840.Google ScholarPubMed
Vorel, J, Cwiklinski, K, Roudnický, P, et al. (2021) Eudiplozoon nipponicum (Monogenea, Diplozoidae) and its adaptation to haematophagy as revealed by transcriptome and secretome profiling. BMC Genomics 22, 117.Google ScholarPubMed
Wang, J, Zhou, Y, Li, D, Sun, X, Deng, Y and Zhao, Q (2017) TSPAN 31 is a critical regulator on transduction of survival and apoptotic signals in hepatocellular carcinoma cells. FEBS Letters 591, 29052918.Google Scholar
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