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Molecular targets for the development of new acaricides against Rhipicephalus microplus: a review

Published online by Cambridge University Press:  18 April 2022

Amanda Ponce Morais Cerqueira ,
Matheus da Cunha Santos ,
Manoelito Coelho dos Santos Júnior  and
Mariana Borges Botura Open the ORCID record for Mariana Borges Botura [Opens in a new window]
Amanda Ponce Morais Cerqueira
Affiliation:
Departamento de Biologia, Programa de Pós-Graduação em Biotecnologia, Universidade Estadual de Feira de Santana, Feira de Santana, BA, Brazil
Matheus da Cunha Santos
Affiliation:
Departamento de Saúde, Universidade Estadual de Feira de Santana, Feira de Santana, BA, Brazil
Manoelito Coelho dos Santos Júnior
Affiliation:
Departamento de Saúde, Universidade Estadual de Feira de Santana, Feira de Santana, BA, Brazil
Mariana Borges Botura*
Affiliation:
Departamento de Saúde, Universidade Estadual de Feira de Santana, Feira de Santana, BA, Brazil
*
Author for correspondence: Mariana Borges Botura, E-mail: mbbotura@uefs.br
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Abstract

The cattle tick Rhipicephalus microplus is an ectoparasite with high economic importance to bovine culture, mainly in tropical and subtropical regions. The resistance of the tick from the commercial acaricides has hindered its control, thus motivating the search for new strategies. The purpose of this study was to perform a critical review about the main molecular targets of R. microplus that are useful for the discovery of new acaricides. Bibliographic search was conducted in the databases PubMed, ScienceDirect and CAB Direct, using the following descriptors: ‘Rhipicephalus microplus’, ‘Boophilus microplus’, ‘molecular targets’ and ‘action’, published between 2010 and 2021. Out of the 212 publications identified, 17 articles were selected for study inclusion. This review described 14 molecular targets and among these 4 are targets from commercial acaricides. Most of them are enzymes to catalyse important reactions to tick survival, related to energetic metabolism, mechanisms of biotransformation and neurotransmission. The data will be helpful in the development of new more effective and selective acaricides.

Keywords

Acaricidesaction mechanismcattle tickenzymereceptor
Type
Review Article
Information
Parasitology , Volume 149 , Issue 8 , July 2022 , pp. 1019 - 1026
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Agwunobi, DO, Yu, Z and Liu, J (2021) A retrospective review on ixodid tick resistance against synthetic acaricides: implications and perspectives for future resistance prevention and mitigation. Pesticide Biochemistry and Physiology 173, 104776.CrossRefGoogle ScholarPubMed
Bae, J-W and Kwon, W-S (2020) Investigating the effects of fipronil on male fertility: insight into the mechanism of capacitation. Reproductive Toxicology 94, 1–7.CrossRefGoogle ScholarPubMed
Bandara, KMUJ and Karunaratne, SHPP (2017) Mechanisms of acaricide resistance in the cattle tick Rhipicephalus (Boophilus) microplus in Sri Lanka. Pesticide Biochemistry and Physiology 139, 68–72. doi: 10.1016/j.pestbp.2017.05.002CrossRefGoogle Scholar
Baron, S, Van Der Merwe, NA, Madder, M and Maritz-Olivier, C (2015) SNP analysis infers that recombination is involved in the evolution of amitraz resistance in Rhipicephalus microplus. PLoS ONE 10. doi: 10.1371/journal.pone.0131341.CrossRefGoogle ScholarPubMed
Baxter, GD and Barker, SC (1998) Acetylcholinesterase cDNA of the cattle tick, Boophilus microplus: characterisation and role in organophosphate resistance. Insect Biochemistry and Molecular Biology 28, 581–589.CrossRefGoogle ScholarPubMed
Baxter, GD and Barker, SC (2002) Analysis of the sequence and expression of a second putative acetylcholinesterase cDNA from organophosphate susceptible and organophosphate-resistant cattle ticks. Insect Biochemistry and Molecular Biology 32, 815–820.CrossRefGoogle ScholarPubMed
Braz, V, Gomes, H, Galina, A, Saramago, L, Braz, G, Vaz, I Jr., Logullo, C, Fonseca, RN, Campos, E and Moraes, J (2019) Inhibition of energy metabolism by 3-bromopyruvate in the hard tick Rhipicephalus microplus. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 218, 55–61.Google ScholarPubMed
Brock, CM, Temeyer, KB, Tidwell, J, Yang, Y, Blandon, MA, Carreón-Camacho, D, Longnecker, MT, Almazán, C, Pérez De León, AA and Pietrantonio, PV (2019) The leucokinin-like peptide receptor from the cattle fever tick, Rhipicephalus microplus, is localized in the midgut periphery and receptor silencing with validated double-stranded RNAs causes a reproductive fitness cost. International Journal for Parasitology 49, 287–299.CrossRefGoogle ScholarPubMed
Calvano, MPCA, Brumatti, RC, Barros, JC, Garcia, MV, Martins, KR and Andreotti, R (2021) Bioeconomic simulation of Rhipicephalus microplus infestation in different beef cattle production systems in the Brazilian Cerrado. Agricultural Systems 194, 103247.CrossRefGoogle Scholar
Cerqueira, APM, Santana, IB, Araújo, JSC, Lima, HG, Batatinha, MJM, Branco, A, Santos Junior, MCD and Botura, MB (2021) Homology modeling, docking, molecular dynamics and in vitro studies to identify Rhipicephalus microplus acetylcholinesterase inhibitors. Journal of Biomolecular Structure & Dynamics 1, 1–11. doi: 10.1080/07391102.2021.1889666CrossRefGoogle Scholar
Chang, TC, Park, JH, Colquhoun, AN, Khoury, CB, Seangmany, NA and Schwans, JP (2018) Evaluating the catalytic importance of a conserved Glu97 residue in triosephosphate isomerase. Biochemical and Biophysical Research Communications 505, 492–497.CrossRefGoogle ScholarPubMed
Cossío-Bayúgar, R, Miranda-Miranda, E, Narváez Padilla, V, Olvera-Valencia, F and Reynaud, E (2012) Perturbation of tyraminergic/octopaminergic function inhibits oviposition in the cattle tick Rhipicephalus (Boophilus) microplus. Journal of Insect Physiology 58, 628–633.CrossRefGoogle ScholarPubMed
Cossío-Bayúgar, R, Miranda-Miranda, E, Fernández-Rubalcaba, M, Padilla, V and Reynaud, E (2015) Adrenergic ligands that block oviposition in the cattle tick Rhipicephalus microplus affect ovary contraction. Scientific Reports 5, 15109.CrossRefGoogle ScholarPubMed
Davis, RL (2020) Mechanism of action and target identification: a matter of timing in drug discovery. iScience 23. doi: 10.1016/j.isci.2020.101487.CrossRefGoogle ScholarPubMed
Dionisio, L, Rosa, MJR, Bouzat, C and Esandi, MDC (2011) An intrinsic GABAergic system in human lymphocytes. Neuropharmacology 60, 513–519.CrossRefGoogle ScholarPubMed
Fournier, D, Mutero, A and Rungger, D (1992) Drosophila acetylcholinesterase – expression of a functional precursor in Xenopus oocytes. European Journal of Biochemistry 203, 513–519.CrossRefGoogle ScholarPubMed
Fraga, A, Ribeiro, L, Lobato, M, Santos, V and Silva, JR (2013) Glycogen and glucose metabolism are essential for early embryonic development of the red flour beetle Tribolium castaneum. PLoS ONE 8. doi: 10.1371/journal.pone.0065125.CrossRefGoogle ScholarPubMed
Freitas, DRJ, Rosa, RM, Moraes, J, Campos, E, Logullo, C, Vaz, IS Jr. and Masuda, A (2007) Relationship between glutathione S-transferase, catalase, oxygen consumption, lipid peroxidation and oxidative stress in eggs and larvae of Boophilus microplus (Acarina: Ixodidae). Comparative Biochemistry and Physiology – Part. A Molecular & Integrative Physiology 146, 688–694.CrossRefGoogle Scholar
Fular, A, Sharma, AK, Kumar, S, Nagar, G, Chigure, G, Ray, D and Ghosh, S (2018) Establishment of a multi-acaricide resistant reference tick strain (IVRI-V) of Rhipicephalus microplus. Ticks and Tick-borne Diseases 9, 1184–1191. doi: 10.1016/j.ttbdis.2018.04.014CrossRefGoogle ScholarPubMed
Gassel, M, Wolf, C, Noack, S, Williams, H and Ilg, T (2014) The novel isoxazoline ectoparasiticide fluralaner: selective inhibition of arthropod γ-aminobutyric acid- and l-glutamate-gated chloride channels and insecticidal/acaricidal activity. Insect Biochemistry and Molecular Biology 45, 111–124.CrossRefGoogle ScholarPubMed
Ghosh, S, Gupta, S, Ajith Kumar, KG, Sharma, AK, Kumar, S, Nagar, G, Kumar, R, Paul, S, Fular, A, Chigure, G, Nandi, A, Manjunathachar, HV, Mohammad, A, Verma, MR, Saravanan, BC and Ray, D (2017) Characterization and establishment of a reference deltamethrin and cypermethrin resistant tick line (IVRI-IV) of Rhipicephalus (Boophilus) microplus. Pesticide Biochemistry and Physiology 138, 66–70.CrossRefGoogle ScholarPubMed
Gross, A, Temeyer, K, Day, T, Pérez De León, A, Kimber, M and Coats, J (2015) Pharmacological characterization of a tyramine receptor from the southern cattle tick, Rhipicephalus (Boophilus) microplus. Insect Biochemistry and Molecular Biology 63, 47–53.CrossRefGoogle ScholarPubMed
Gross, AD, Temeyer, KB, Day, TA, Pérez De León, AA, Kimber, MJ and Coats, JR (2017) Interaction of plant essential oil terpenoids with the southern cattle tick tyramine receptor: a potential biopesticide target. Chemico-Biological Interactions 263, 1–6.CrossRefGoogle ScholarPubMed
He, R, Zhang, H, Shen, N, Guo, C, Ren, Y, Xie, Y, Gu, X, Lai, W, Peng, X and Yang, G (2018) Molecular characterization and allergenicity potential of triosephosphate isomerase from Sarcoptes scabiei. Veterinary Parasitology 257, 40–47.CrossRefGoogle ScholarPubMed
Hernandez, RH, He, H, Chen, AC, Ivie, GW, George, JE and Wagner, GG (1999) Cloning and sequencing of a putative acetylcholinesterase cDNA from Boophilus microplus (Acari: Ixodidae). Journal of Medical Entomology 36, 764–770.CrossRefGoogle Scholar
Holmes, SP, He, H, Chen, AC, Lvie, GW and Pietrantonio, PV (2000) Cloning and transcriptional expression of a leucokinin-like peptide receptor from the Southern cattle tick, Boophilus microplus (Acari: Ixodidae). Insect Molecular Biology 9, 457–465.CrossRefGoogle Scholar
Ilg, T, Schmalz, S, Werr, M and Cramer, J (2010) Acetylcholinesterases of the cat flea Ctenocephalides felis: identification of two distinct genes and biochemical characterization of recombinant and in vivo enzyme activities. Insect Biochemistry and Molecular Biology 2, 153–164.CrossRefGoogle Scholar
Ilg, T, Berger, M, Noack, S, Rohwer, A and Gaßel, M (2013) Glutamate decarboxylase of the parasitic arthropods Ctenocephalides felis and Rhipicephalus microplus: gene identification, cloning, expression, assay development, identification of inhibitors by high throughput screening and comparison with the orthologs from Drosophila melanogaster and mouse. Insect Biochemistry and Molecular Biology 43, 162–177.CrossRefGoogle ScholarPubMed
Jia, M, He, Q, Wang, W, Dai, J and Zhu, L (2018) Chemical composition and acaricidal activity of Arisaema anurans essential oil and its major constituents against Rhipicephalus microplus (Acari: Ixodidae). Veterinary Parasitology 261, 59–66.CrossRefGoogle Scholar
Kersch, CN and Pietrantonio, PV (2011) Mosquito Aedes aegypti (L.) leucokinin receptor is critical for in vivo fluid excretion post blood feeding. FEBS Letters 585, 3507–3512.CrossRefGoogle ScholarPubMed
Kumar, K, Bhargava, P and Roy, U (2012) Cloning, overexpression and characterization of Leishmania donovani triosephosphate isomerase. Experimental Parasitology 130, 430–436.CrossRefGoogle ScholarPubMed
Kumar, R, Kumar Sharma, A and Ghosh, S (2019) Menace of acaricide resistance in cattle tick, Rhipicephalus microplus in India: status and possible mitigation strategies. Veterinary Parasitology 278, 108993.CrossRefGoogle ScholarPubMed
Le Gall, VL, Klafke, GM and Torres, TT (2018) Detoxification mechanisms involved in ivermectin resistance in the cattle tick, Rhipicephalus (Boophilus) microplus. Scientific Reports 8. doi:10.1038/s41598-018-30907-7.CrossRefGoogle ScholarPubMed
Leveridge, M, Chung, CW, Gross, JW, Phelps, CB and Green, D (2018) Integration of lead discovery tactics and the evolution of the lead discovery toolbox. SLAS Discovery: Advances 23, 881–897.CrossRefGoogle ScholarPubMed
Lew-Tabor, AE and Rodriguez Valle, M (2016) A review of reverse vaccinology approaches for the development of vaccines against ticks and tick borne diseases. Ticks and Tick-borne Diseases 7, 573–585.CrossRefGoogle ScholarPubMed
Li, M, Wang, L, Qiu, L, Wang, W, Xin, L, Xu, J, Wang, H and Song, L (2016) A glutamic acid decarboxylase (CgGAD) highly expressed in hemocytes of Pacific oyster Crassostrea gigas. Developmental and Comparative Immunology 63, 56–65.CrossRefGoogle ScholarPubMed
Logullo, C, Witola, WH, Andrade, C, Abreu, L, Gomes, J, Vaz, IS, Imamura, S, Konnai, S, Ohashi, K and Onuma, M (2009) Expression and activity of glycogen synthase kinase during vitellogenesis and embryogenesis of Rhipicephalus (Boophilus) microplus. Veterinary Parasitology 161, 261–269.CrossRefGoogle ScholarPubMed
Lopez-Zavala, AA, Carrasco-Miranda, JS, Ramirez-Aguirre, CD, López-Hidalgo, M, Benitez-Cardoza, CG, Ochoa-Leyva, A, Cardona-Felix, CS, Diaz-Quezada, C, Rudiño-Piñera, E, Sotelo-Mundo, RR and Brieba, LG (2016) Structural insights from a novel invertebrate triosephosphate isomerase from Litopenaeus vannamei. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics 1864, 696–1706.CrossRefGoogle ScholarPubMed
Massoulié, J, Anselmet, A, Bon, S, Krejci, E, Legay, C, Morel, N and Simon, S (1998) Acetylcholinesterase: C-terminal domains, molecular forms and functional localization. Journal of Physiology 92, 183–190.Google ScholarPubMed
Moraes, J, Galina, A, Alvarenga, PH, Rezende, GL, Masuda, A, Vaz, IS Jr. and Logullo, C (2007) Glucose metabolism during embryogenesis of the hard tick Boophilus microplus. Comparative Biochemistry and Physiology. B, Biochemistry & Molecular Biology 146, 528–533.Google ScholarPubMed
Moraes, J, Arreola, R, Cabrera, N, Saramago, L, Freitas, D, Masuda, A, Vaz, IS Jr., Gomez-Puyou, MT, Perez-Montfort, R, Gomez-Puyou, A and Logulloet, C (2011) Structural and biochemical characterization of a recombinant triosephosphate isomerase from Rhipicephalus (Boophilus) microplus. Insect Biochemistry and Molecular Biology 41, 400–409.CrossRefGoogle ScholarPubMed
Nachman, RJ, Wang, XJ, Etzkorn, FA, Kaczmarek, K, Zabrocki, J, Lopez, J and Coast, GM (2013) Evaluation of insect CAP2b analogs with either an (E)-alkene, trans- or a (Z)-alkene, cis-Pro isostere identifies the Pro orientation for antidiuretic activity in the stink bug. Peptides 41, 101–106.CrossRefGoogle Scholar
Nandi, A, Singh, H and Singh, NK (2015) Esterase and glutathione S-transferase levels associated with synthetic pyrethroid resistance in Hyalomma anatolicum and Rhipicephalus microplus ticks from Punjab, India. Experimental & Applied Acarology 66, 141–157.CrossRefGoogle ScholarPubMed
Neupert, S, Predel, R, Russell, WK, Davies, R, Pietrantonio, PV and Nachman, RJ (2005) Identification of tick periviscerokinin, the first neurohormone of Ixodidae: single cell analysis by means of MALDI-TOF/TOF mass spectrometry. Biochemical and Biophysical Research Communications 338, 1860–1864.CrossRefGoogle ScholarPubMed
Nicaretta, JE, Zapa, DMB, Couto, LFM, Heller, LM, Cavalcante, ASA, Cruvinel, LB, Melo Júnior, RD, Ferreira, LL, Nascimento, RMD, Soares, VE, Borges, LMF, Monteiro, CMO and Lopes, WDZ (2021) Rhipicephalus microplus seasonal dynamic in a Cerrado biome, Brazil: an update data considering the global warming. Veterinary Parasitology 296, 109506.CrossRefGoogle Scholar
Ohta, H and Ozoe, Y (2014) Molecular signalling, pharmacology, and physiology of octopamine and tyramine receptors as potential insect pest control targets. Advances in Insect Physiology 46, 73–166.CrossRefGoogle Scholar
Ozoe, Y (2013) γ-Aminobutyrate- and glutamate-gated chloride channels as targets of insecticides. Advances in Insect Physiology 44, 211–286.CrossRefGoogle Scholar
Parizi, LF, Utiumi, KU, Imamura, S, Onuma, M, Ohashi, K, Masuda, A and Vaz, IS Jr (2011) Cross immunity with Haemaphysalis longicornis glutathione S-transferase reduces an experimental Rhipicephalus (Boophilus) microplus infestation. Experimental Parasitology 127, 113–118.CrossRefGoogle ScholarPubMed
Pietrantonio, PV, Xiong, C, Nachman, RJ and Shen, Y (2018) G protein-coupled receptors in arthropod vectors: omics and pharmacological approaches to elucidate ligand-receptor interactions and novel organismal functions. Current Opinion in Insect Science 29, 12–20.CrossRefGoogle ScholarPubMed
Prado-Ochoa, MG, Ramírez-Noguera, P, Díaz-Torres, R, Garrido-Fariña, GI, Vázquez-Valadez, VH, Velázquez-Sánchez, AM, Muñoz-Guzmán, MA, Angeles, E and Alba-Hurtado, F (2014) The action of two ethyl carbamates on acetylcholinesterase and reproductive organs of Rhipicephalus microplus. Veterinary Parasitology 199, 215–224.CrossRefGoogle ScholarPubMed
Romero-Romero, S, Becerril-Sesín, LA, Costas, M, Rodríguez-Romero, A and Fernández-Velasco, DA (2018) Structure and conformational stability of the triosephosphate isomerase from Zea mays. Comparison with the chemical unfolding pathways of other eukaryotic TIMs. Archives of Biochemistry and Biophysics 658, 66–76.CrossRefGoogle ScholarPubMed
Rufener, L, Danelli, V, Bertrand, D and Sager, H (2017) The novel isoxazoline ectoparasiticide lotilaner (Credelio™): a non-competitive antagonist specific to invertebrates γ-aminobutyric acid-gated chloride channels (GABACls). Parasites & Vectors 10. doi: 10.1186/s13071-017-2470-4CrossRefGoogle Scholar
Sabadin, GA, Salomon, TB, Leite, MS, Benfato, MS, Oliveira, PL and Silva Vaz, I Jr. (2021) An insight into the functional role of antioxidant and detoxification enzymes in adult Rhipicephalus microplus female ticks. Parasitology International 81, 102274.CrossRefGoogle ScholarPubMed
Santos, FO, Lima, HG, de Souza Santa Rosa, S, das Mercês, NB, Serra, TM, Uzeda, RS, Reis, IMA, Botura, MB, Branco, A and Batatinha, MJM (2018) In vitro acaricide and anticholinesterase activities of digitaria insularis (Poaceae) against Rhipicephalus (Boophilus) microplus. Veterinary Parasitology 255, 102–106.CrossRefGoogle ScholarPubMed
Saraswati, AP, Ali Hussaini, SM, Krishna, NH, Babu, BN and Kamal, A (2018) Glycogen synthase kinase-3 and its inhibitors: potential target for various therapeutic conditions. European Journal of Medicinal Chemistry 144, 843–858.CrossRefGoogle ScholarPubMed
Selzer, PM and Epe, C (2021). Antiparasitics in animal health: quo vadis? Trends in Parasitology 37, 77–89.CrossRefGoogle Scholar
Silva, RM, Vital, WO, Fonseca, RN, Martins, YPM, Lemos, FJA, Vaz, IS Jr. and Logullo, C (2019) Hypometabolic strategy and glucose metabolism maintenance of Aedes aegypti egg desiccation. Comparative Biochemistry and Physiology 227, 56–63.CrossRefGoogle ScholarPubMed
Silva, GD, Lima, HG, Freitas, HF, Rocha Pita, SS, Santos Luz, Y, Figueiredo, MP, Uzêda, RS, Branco, A, Costa, SL, Batatinha, MJM and Botura, MB (2021) In vitro and in silico studies of the larvicidal and anticholinesterase activities of berberine and piperine alkaloids on Rhipicephalus microplus. Ticks and Tick Borne Diseases 12. doi: 10.1016/j.ttbdis.2020.101643CrossRefGoogle ScholarPubMed
Sutherland, C (2011) What are the bona fide GSK3 substrates? International Journal of Alzheimer's Disease 505607. doi: 10.4061/2011/505607.Google ScholarPubMed
Swale, DR, Tong, F, Temeyer, KB, Li, A, Lam, PC, Totrov, MM, Carlier, PR, Pérez De León, AA and Bloomquist, JR (2013) Inhibitor profile of bis(n)-tacrines and N-methylcarbamates on acetylcholinesterase from Rhipicephalus (Boophilus) microplus and Phlebotomus papatasi. Pesticide Biochemistry and Physiology 106. https://doi.org/10.1016/j.pestbp.2013.03.005.CrossRefGoogle ScholarPubMed
Tang, CD, Li, X, Shi, HL, Jia, YY, Dong, ZX, Jiao, ZJ, Wang, LF, Xu, JH, Yao, LG and Kan, YC (2020) Efficient expression of novel glutamate decarboxylases and high level production of γ-aminobutyric acid catalyzed by engineered Escherichia coli. International Journal of Biological Macromolecules 160, 372–379.CrossRefGoogle ScholarPubMed
Temeyer, KB, Darvey, RB and Chen, AC (2004) Identification of a third Boophilus microplus (Acari: Ixodidae) cDNA presumptively encoding an acetylcholinesterase. Journal of Medicine and Entomology 41, 259–268.CrossRefGoogle ScholarPubMed
Temeyer, KB, Pruett, J and Olafson, P (2010) Baculovirus expression, biochemical characterization and organophosphate sensitivity of rBmAChE1, rBmAChE2, and rBmAChE3 of Rhipicephalus (Boophilus) microplus. Veterinary Parasitology 172, 114–121.CrossRefGoogle ScholarPubMed
Temeyer, KB, Olafson, PU, Brake, DK, Tuckow, AP, Li, AY and Perez de Leon, AA (2013) Acetylcholinesterase of Rhipicephalus (Boophilus) microplus and Phlebotomus papatasi: gene identification, expression, and biochemical properties of recombinant proteins. Pesticide Biochemistry and Physiology 106, 118–123.CrossRefGoogle Scholar
Tungtur, S, Meinhardt, S and Swint-Kruse, L (2010) Comparing the functional roles of nonconserved sequence positions in homologous transcription repressors: implications for sequence/function analyses. Journal of Molecular Biology 395, 785–802.CrossRefGoogle ScholarPubMed
Ueno, H (2000) Enzymatic and structural aspects on glutamate decarboxylase. Journal of Molecular Catalysis B: Enzymatic 10, 67–79.CrossRefGoogle Scholar
Waltero, C, Martins, R, Calixto, C, Fonseca, RN, Abreu, LA, Silva Vaz, I Jr. and Logullo, C (2020) The hallmarks of GSK-3 in morphogenesis and embryonic development metabolism in arthropods. Insect Biochemistry and Molecular Biology 118, 103307.CrossRefGoogle ScholarPubMed
Wu, SF, Xu, G, Qi, YX, Xia, RY, Huang, J and Ye, GY (2014) Two splicing variants of a novel family of octopamine receptors with different signalling properties. Journal of Neurochemistry 129, 37–47.CrossRefGoogle Scholar
Yang, Y, Bajracharya, P, Castillo, P, Nachman, RJ and Pietrantonio, PV (2013) Molecular and functional characterization of the first tick CAP2b (periviscerokinin) receptor from Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). General and Comparative Endocrinology 194, 142–151.CrossRefGoogle Scholar
Yang, Y, Chen, Z-W, Hurlburt, B, Li, G-L, Zhang, Y-X, Fei, D-X, Shen, H-W, Cao, M-J and Liu, G-M (2017) Identification of triosephosphate isomerase as a novel allergen in Octopus fangsiao. Molecular Immunology 85, 35–46.CrossRefGoogle ScholarPubMed