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Enzyme Research
Volume 2019, Article ID 6139863, 9 pages
https://doi.org/10.1155/2019/6139863
Research Article

Acetylcholinesterases from Leaf-Cutting ant Atta sexdens: Purification, Characterization, and Capillary Reactors for On-Flow Assays

1Federal University of São Carlos, Department of Chemistry, São Carlos, SP, Brazil
2São Paulo University, Instituto de Ciências Biomédicas (ICB), São Paulo, Brazil
3São Paulo State University, Center for the Study of Social Insects, Rio Claro, SP, Brazil

Correspondence should be addressed to Quezia B. Cass; rb.racsfu@ssacq and Dulce Helena F. Souza; rb.racsfu@eclud

Received 8 February 2019; Accepted 12 May 2019; Published 1 July 2019

Academic Editor: Qi-Zhuang Ye

Copyright © 2019 Adriana M. Dos Santos et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Kaspari and J. D. Majer, “Using ants to monitor environmental change,” in Ants: Standard Methods for Measuring and Monitoring Biodiversity, D. Agosti, J. D. Majer, L. E. Alonso, and R. Schultz, Eds., Smithsonian Institution Press, Washington D.C., USA, 2000. View at Google Scholar
  2. T. G. Pikart, G. K. Souza, T. V. Zanuncio et al., “Dispersion of seeds of tree species by the leaf-cutting ant acromyrmex subterraneus molestans (hymenoptera: Formicidae) in viçosa, Minas Gerais State, Brazil,” Sociobiology, vol. 56, no. 3, pp. 645–652, 2010. View at Google Scholar · View at Scopus
  3. N. J. Mehdiabadi and T. R. Schultz, “Natural history and phylogeny of the fungus-farming ants (Hymenoptera: Formicidae: Myrmicinae: Attini),” Myrmecological News, vol. 13, pp. 37–55, 2009. View at Google Scholar · View at Scopus
  4. U. G. Mueller, N. M. Gerardo, D. K. Aanen, D. L. Six, and T. R. Schultz, “The evolution of agriculture in insects,” Annual Review of Ecology, Evolution and Systematics, vol. 36, no. 1, pp. 563–595, 2005. View at Publisher · View at Google Scholar
  5. T. R. Schultz and S. G. Brady, “Major evolutionary transitions in ant agriculture,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 105, no. 14, pp. 5435–5440, 2008. View at Publisher · View at Google Scholar
  6. T. M. C. Della Lucia, Formigas-Cortadeiras: Da Biologia ao Manejo, Editora UFV, Viçosa, Brazil, 2011.
  7. C. A. Lima, T. M. C. Della Lucia, and N. S. Anjos, Formigas Cortadeiras: Biologia E Controle, Viçosa, Brazil, 2001.
  8. E. Berti filho, L. C. Marchini, O. Nakano, and E. Berti, “Curso de entomologia aplicada à agricultura,” in Formigas Cortadeiras e Cupins, pp. 631–671, FEALQ, Piracicaba, Brazil, 1992. View at Google Scholar
  9. F. A. Mariconi, “As Saúvas. Agronomica Ceres, Viçosa,” 1970.
  10. E. C. Antunes and T. M. C. Della Lucia, “Consumo foliar em Eucalyptus urophylla POR Acromyrmex laticeps nigrosetosus forel (Hymenoptera-Formicidae) leaf-consumption in Eucalyptus urophylla BY Acromyrmex laticeps,” Ciênc. e Agrotec, vol. 23, pp. 208–211, 1999. View at Google Scholar
  11. J. S. Britto, L. C. de Forti, M. A. Oliveira et al., “Use of alternatives to PFOS, its salts and PFOSF for the control of leaf-cutting ants Atta and Acromyrmex,” International Journal of Environmental Studies, vol. 3, pp. 11–92, 2016. View at Google Scholar
  12. Y. H. Kim, J. Y. Choi, Y. H. Je, Y. H. Koh, and S. H. Lee, “Functional analysis and molecular characterization of two acetylcholinesterases from the German cockroach, Blattella germanica,” Insect Molecular Biology, vol. 19, no. 6, pp. 765–776, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Fournier, J. Bergé, M. C. de Almeida, and C. Bordier, “Acetylcholinesterases from musca domestica and drosophila melanogaster brain are linked to membranes by a glycophospholipid anchor sensitive to an endogenous phospholipase,” Journal of Neurochemistry, vol. 50, no. 4, pp. 1158–1163, 1988. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. H. Kim, D. J. Cha, J. W. Jung, H. W. Kwon, S. H. Lee, and J. Vontas, “Molecular and kinetic properties of two acetylcholinesterases from the western honey bee, apis mellifera,” PLoS ONE, vol. 7, no. 11, pp. 17–19, 2012. View at Publisher · View at Google Scholar
  15. M. Weill, P. Fort, A. Berthomieu, M. P. Dubois, N. Pasteur, and M. Raymond, “A novel acetylcholinesterase gene in mosquitoes codes for the insecticide target and is non-homologous to the ace gene in Drosophila,” Proceedings of the Royal Society B Biological Science, vol. 269, no. 1504, pp. 2007–2016, 2002. View at Publisher · View at Google Scholar
  16. G. He, Y. Sun, and F. Li, “Rna interference of two acetylcholinesterase genes in plutella xylostella reveals their different functions,” Archives of Insect Biochemistry and Physiology, vol. 79, no. 2, pp. 75–86, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. H. Kim and S. H. Lee, “Which acetylcholinesterase functions as the main catalytic enzyme in the Class Insecta?” Insect Biochemistry and Molecular Biology, vol. 43, no. 1, pp. 47–53, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Kumar, G. P. Gupta, and M. V. Rajam, “Silencing of acetylcholinesterase gene of Helicoverpa armigera by siRNA affects larval growth and its life cycle,” Journal of Insect Physiology, vol. 55, no. 3, pp. 273–278, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. Y. Lu, Y. Park, X. Gao et al., “Cholinergic and non-cholinergic functions of two acetylcholinesterase genes revealed by gene-silencing in Tribolium castaneum,” Scientific Reports, vol. 2, no. 1, pp. 1–7, 2012. View at Publisher · View at Google Scholar
  20. L. Revuelta, M. D. Piulachs, X. Bellés et al., “RNAi of ace1 and ace2 in Blattella germanica reveals their differential contribution to acetylcholinesterase activity and sensitivity to insecticides,” Insect Biochemistry and Molecular Biology, vol. 39, no. 12, pp. 913–919, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. D. Fournier, J.-M. Bride, F. Hoffmann, and F. Karch, “Acetylcholinesterase. two types of modifications confer resistance to insecticide,” The Journal of Biological Chemistry, vol. 267, no. 20, pp. 14270–14274, 1992. View at Google Scholar · View at Scopus
  22. D. Fournier and A. Mutero, “Modification of acetylcholinesterase as a mechanism of resistance to insecticides,” Comparative Biochemistry and Physiology - Part C: Toxicology & Pharmacology, vol. 108, no. 1, pp. 19–31, 1994. View at Publisher · View at Google Scholar
  23. G.-J. Lang, K. Y. Zhu, and C.-X. Zhang, “Can acetylcholinesterase serve as a target for developing more selective insecticides?” Current Drug Targets, vol. 13, no. 4, pp. 495–501, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. H.-J. Chen, Z. Liao, X.-M. Hui, G.-Q. Li, F. Li, and Z.-J. Han, “Ace2, rather than acel, is the major acetylcholinesterase in the silkworm, Bombyx mori,” Insect Science, vol. 16, no. 4, pp. 297–303, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. E. Huchard, M. Martinez, H. Alout et al., “Acetylcholinesterase genes within the Diptera: takeover and loss in true flies,” Proceedings of the Royal Society B Biological Science, vol. 273, no. 1601, pp. 2595–2604, 2006. View at Publisher · View at Google Scholar
  26. C. J. dos Santos, R. Zanetti, D. Ferreira De Oliveira, G. C. Gajo, and D. S. Alves, “Plant–derived products for leaf–cutting ants control,” in Insecticides - Development of Safer and More Effective Technologies, 2013. View at Publisher · View at Google Scholar
  27. R. Zanetti, J. C. Zanuncio, J. C. Santos, W. L. P. Da Silva, G. T. Ribeiro, and P. G. Lemes, “An overview of integrated management of leaf-cutting ants (Hymenoptera: Formicidae) in Brazilian forest plantations,” Forests, vol. 5, no. 3, pp. 439–454, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Rahimi, S. Nikfar, and M. Abdollahi, “Increased morbidity and mortality in acute human organophosphate-poisoned patients treated by oximes: a meta-analysis of clinical trials,” Human & Experimental Toxicology, vol. 25, no. 3, pp. 157–162, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Shadnia, E. Azizi, R. Hosseini et al., “Evaluation of oxidative stress and genotoxicity in organophosphorus insecticide workers,” Human & Experimental Toxicology, vol. 24, no. 9, pp. 439–445, 2016. View at Publisher · View at Google Scholar
  30. J. R. Suarez-Lopez, D. R. Jacobs Jr., J. H. Himes, and B. H. Alexander, “Acetylcholinesterase activity, cohabitation with floricultural workers, and blood pressure in Ecuadorian children,” Environmental Health Perspectives, vol. 121, no. 5, pp. 619–624, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Ye, J. Beach, J. W. Martin, and A. Senthilselvan, “Occupational pesticide exposures and respiratory health,” International Journal of Environmental Research and Public Health, vol. 10, no. 12, pp. 6442–6471, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. G. L. Ellman, K. D. Courtney, V. Andres Jr., and R. M. Featherstone, “A new and rapid colorimetric determination of acetylcholinesterase activity,” Biochemical Pharmacology, vol. 7, no. 2, pp. 88–95, 1961. View at Publisher · View at Google Scholar · View at Scopus
  33. M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding,” Analytical Biochemistry, vol. 72, no. 1-2, pp. 248–254, 1976. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Shevchenko, M. Wilm, O. Vorm, and M. Mann, “Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels,” Analytical Chemistry, vol. 68, no. 5, pp. 850–858, 1996. View at Publisher · View at Google Scholar · View at Scopus
  35. P. R. Adalberto, C. C. Golfeto, A. C. Moreira et al., “Characterization of an exopolygalacturonase from leucoagaricus gongylophorus, the symbiotic fungus of Atta sexdens,” Advances in Enzyme Research, vol. 04, no. 01, pp. 7–19, 2016. View at Publisher · View at Google Scholar
  36. P. T. Ike, A. C. Moreira, F. G. de Almeida et al., “Functional characterization of a yellow laccase from Leucoagaricus gongylophorus,” SpringerPlus, vol. 4, no. 1, article 654, 2015. View at Publisher · View at Google Scholar
  37. A. Dereeper, V. Guignon, G. Blanc et al., “Phylogeny.fr: robust phylogenetic analysis for the non-specialist,” Nucleic Acids Research, vol. 36, pp. W465–W469, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Kumar, G. Stecher, and K. Tamura, “MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets,” Molecular Biology and Evolution, vol. 33, no. 7, pp. 1870–1874, 2016. View at Publisher · View at Google Scholar
  39. K. L. Vanzolini, L. C. C. Vieira, A. G. Correîa, C. L. Cardoso, and Q. B. Cass, “Acetylcholinesterase immobilized capillary reactors-tandem mass spectrometry: An on-flow tool for ligand screening,” Journal of Medicinal Chemistry, vol. 56, no. 5, pp. 2038–2044, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. A. C. Moreira, A. M. Santos, R. L. Carneiro, O. C. Bueno, and D. H. Souza, “Validation of reference genes in leaf-cutting ant Atta sexdens rubropilosa in different developmental stages and tissues,” International Journal of Environment, Agriculture and Biotechnology, vol. 2, no. 2, pp. 743–755, 2017. View at Publisher · View at Google Scholar
  41. M. A. Mohamed, E.-S. M. E. Mahdy, A.-E. M. Ghazy, N. M. Ibrahim, H. A. El-Mezayen, and M. M. E. Ghanem, “The activity of detoxifying enzymes in the infective juveniles of Heterorhabditis bacteriophora strains: purification and characterization of two acetylcholinesterases,” Comparative Biochemistry and Physiology Part - C: Toxicology and Pharmacology, vol. 180, pp. 11–22, 2016. View at Publisher · View at Google Scholar · View at Scopus
  42. Q. B. Cass and N. Cassiano, “Cromatografia líquida,” in Obtenção E Caracterização De Enzimas Para Aplicação Em Cromatografia Líquida, P. R. Adalberto and D. H. F. Souza, Eds., Elsevier, Rio de Janeiro, Brazil, 1st edition, 2015. View at Google Scholar
  43. L.-S. Xiao, W. Dou, Y. Li, and J.-J. Wang, “Comparative studies of acetylcholinesterase purified from three field populations of Liposcelis entomophila (enderlein) (psocoptera: liposcelididae),” Archives of Insect Biochemistry and Physiology, vol. 75, no. 3, pp. 158–173, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. J. I. da Silva, M. C. de Moraes, L. C. C. Vieira, A. G. Corrêa, Q. B. Cass, and C. L. Cardoso, “Acetylcholinesterase capillary enzyme reactor for screening and characterization of selective inhibitors,” Journal of Pharmaceutical and Biomedical Analysis, vol. 73, pp. 44–52, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Bisswanger, “Enzyme assays,” Perspectives in Science, vol. 1, no. 1-6, pp. 41–55, 2014. View at Publisher · View at Google Scholar
  46. H. Cui, W. Wu, M. Li, X. Song, Y. Lv, and T. Zhang, “Biosensors and Bioelectronics graphene nanocomposites for detection of organophosphate pesticides,” Biosensors and Bioelectronics, vol. 99, pp. 223–229, 2018. View at Publisher · View at Google Scholar
  47. K. Gabrovska, I. Marinov, T. Godjevargova et al., “The influence of the support nature on the kinetics parameters, inhibition constants and reactivation of immobilized acetylcholinesterase,” International Journal of Biological Macromolecules, vol. 43, no. 4, pp. 339–345, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. T. A. Houndété, D. Fournier, G. K. Ketoh, I. A. Glitho, R. Nauen, and T. Martin, “Biochemical determination of acetylcholinesterase genotypes conferring resistance to the organophosphate insecticide chlorpyriphos in field populations of Bemisia tabaci from Benin, West Africa,” Pesticide Biochemistry and Physiology, vol. 98, no. 1, pp. 115–120, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Moyo, A. R. Ndhlala, J. F. Finnie, and J. Van Staden, “Phenolic composition, antioxidant and acetylcholinesterase inhibitory activities of Sclerocarya birrea and Harpephyllum caffrum (Anacardiaceae) extracts,” Food Chemistry, vol. 123, no. 1, pp. 69–76, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. B. Wang, F. Li, K. Xu et al., “Effects of mutations on the structure and function of silkworm type 1 acetylcholinesterase,” Pesticide Biochemistry and Physiology, vol. 129, pp. 1–6, 2016. View at Publisher · View at Google Scholar
  51. Y.-H. Ye, C. Li, J. Yang et al., “Construction of an immobilised acetylcholinesterase column and its application in screening insecticidal constituents from Magnolia officinalis,” Pest Management Science, vol. 71, no. 4, pp. 607–615, 2015. View at Publisher · View at Google Scholar · View at Scopus
  52. D.-M. Wang, B.-X. Zhang, X.-M. Liu et al., “Molecular characterization of two acetylcholinesterase genes from the rice leaffolder, cnaphalocrocis medinalis (lepidoptera: pyralidae),” Archives of Insect Biochemistry and Physiology, vol. 93, no. 3, pp. 129–142, 2016. View at Publisher · View at Google Scholar · View at Scopus
  53. G. Bicker, M. Naujock, and A. Haase, “Cellular expression patterns of acetylcholinesterase activity during grasshopper development,” Cell and Tissue Research, vol. 317, no. 2, pp. 207–220, 2004. View at Publisher · View at Google Scholar · View at Scopus