Resumen
En el campo de la salud pública, los programas de control de vectores priorizan el uso de insecticidas químicos, excluyendo métodos alternativos ecoamigables derivados de plantas. Se sabe que Annona muricata exhibe una actividad biológica insecticida que altera las etapas de desarrollo, los procesos fisiológicos y la mortalidad de insectos transmisores de enfermedades, pero los principios activos y las proteínas de esta especie de Annonaceae requieren validación entomotóxica en un modelo biológico de culícidos. Se evaluó la actividad de los extractos etanólico (ExtEtOH) y de alcaloides (ExtAlc) y de las fracciones proteicas (FP) de semillas de A. muricata en larvas del IV estadio temprano de Culex quinquefasciatus empleando un abordaje comparativo. El análisis cualitativo de metabolitos en ExtEtOH reveló la presencia de alcaloides, aminoácidos, lactonas, taninos, cardenólidos, acetogeninas y flavonoides. Mediante cromatografía de exclusión molecular se separaron cinco fracciones proteicas de las cuales se evaluó la tercera (FP3), la cual exhibió mayor letalidad larval (33 % con 0,5 mg/ml) y potencia revelada en la concentración letal media (CL50) (0,66 mg/ml, p: 0,166). ExtAlc mostró valores de mortalidad cercanos a los de la FP3 (30 %) y su CL50 (0,74 mg/ml, p: 0,754), en tanto que ExtEtOH confirió máxima mortalidad (100 %) y una CL50 inferior (0,03 mg/ml, p: 0,976). Se observaron dos reacciones tóxicas: una respuesta inmediata en ExtEtOH (97 % en 12 h) y una respuesta aguda mediata en FP y ExtAlc extendida hasta finalizar el ensayo (72 % en 72h).
Palabras clave
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Abbott, W. (1925). A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18(2), 265-267. https://doi.org/10.1093/jee/18.2.265a
Aguilar-Hernández, G., Vivar-Vera, M. D. L. Á., García-Magaña, M. D. L., González-Silva, N., Pérez-Larios, A., Montalvo-González, E. (2020). Ultrasound-Assisted extraction of total acetogenins from the soursop fruit by response surface methodology. Molecules, 25(5), 1139. https://doi.org/10.3390/molecules25051139
Ahmad, A., Khan, G. Z., Ullah, M., Ahmed, N., Sohail, K., Ullah, I., Bukhari, N. A., Perveen, K., Ali, I., Li, K. (2023). Evaluation of different high doses aqueous plant extracts for the sustainable control of Aedes aegypti mosquitoes under laboratory conditions. Journal of King Saud University - Science, 35(11), 102991. https://doi.org/10.1016/j.jksus.2023.102991
Alegre, A., Iannacone. J., Carhuapoma, M. (2017). Toxicidad del extracto acuoso, etanólico y hexánico de Annona muricata, Minthostachys mollis, Lupinus mutabilis y Chenopodium quinoa sobre Tetranychus urticae y Chrysoperla externa. Chilean Journal of Agricultural & Animal Science, ex Agro-Ciencia, 33(3), 273-284. https://doi.org/10.4067/S0719-38902017005000705.
Alvarado, A., Capristán, P., Corahua, C., Ruiz, C., Velásquez, G. (2020). Variación del área agrícola en el distrito La Yarada Los Palos, Tacna, Perú. Espacio y Desarrollo, 31(35), 99-120. https://doi.org/10.18800/espacioydesarrollo.202001.004
Ardila, D. (2014). Evaluación de la actividad citotóxica de los extractos etanólicos de las plantas Annona muricata, Annona cherimola y Physalis peruviana en la línea célular MCF-7 de adenocarcinoma de seno. [Tesis], Facultad de Ciencias. Pontificia Universidad Javeriana. Al Kazman, B. S. M., Harnett, J. E., Hanrahan, J. R. (2022). Traditional Uses, Phytochemistry and Pharmacological Activities of Annonacae. Molecules, 27(11), 3462. https://doi.org/10.3390/molecules27113462
Al-Mehmadi, R. M. & Al-Khalaf, A. A. (2010). Larvicidal and histological effects of Melia azedarach extract on Culex quinquefasciatus Say larvae (Diptera: Culicidae). Journal of King Saud University - Science, 22(2), 77-85. https://doi.org/10.1016/j.jksus.2010.02.004
Aparna, N., Parambil, R. P., George, N., Meethal, K. V. (2021). Toxicity of plant extracts containing trypsin inhibitor to the larvae of Aedes aegypti. International Journal of Mosquito Research, 8(3), 22-27. https://doi.org/10.22271/23487941.2021.v8.i3a.533
Ayana-Gayathri, R. V. & Evans, D. A. (2018). Culex quinquefasciatus Say larva adapts to temperature shock through changes in protein turn over and amino acid catabolism. Journal of Thermal Biology, 74, 149-159. https://doi.org/10.1016/j.jtherbio.2018.03.016
Ayilara, M. S., Adeleke, B. S., Akinola, S. A., Fayose, C. A., Adeyemi, U. T., Gbadegesin, L. A., Omole, R. K., Johnson, R. M., Uthman, Q. O., Babalola, O. O. (2023). Biopesticides as a promising alternative to synthetic pesticides: A case for microbial pesticides, phytopesticides, and nanobiopesticides. Frontiers in Microbiology, 14, 1040901. https://doi.org/10.3389/fmicb.2023.1040901
Bhandari, P., Pant, M., Patanjali, P. K., Raza, S. K. (2016). Advances in Bio-Botanicals Formulations with Incorporation of Nanotechnology in Intensive Crop Management. En R. Prasad (Ed.), Advances and Applications Through Fungal Nanobiotechnology (pp. 291-305). Springer International Publishing. https://doi.org/10.1007/978-3-319-42990-8_14
Bobadilla-Álvarez, M., Zavaleta-Espejo, G., Gil-Franco, F., Pollack-Velásquez, L., Sisniegas-Gonzáles, M. (2002). Efecto bioinsecticida del extracto etanólico de las semillas de Annona cherimolia Miller “chirimoya” Y A. muricata Linneaus “guanábana” sobre larvas del IV estadio de Anopheles sp. Revista Peruana de Biología, 9(2), 64-73. https://doi.org/10.15381/rpb.v9i2.2525
Bobadilla, M., Zavala, F., Sisniegas, M., Zavaleta, G., Mostacero, J., Taramona, L. (2005). Evaluación larvicida de suspensiones acuosas de Annona muricata Linnaeus «guanábana» sobre Aedes aegypti Linnaeus (Diptera, Culicidae). Revista Peruana de Biología, 12(1), 145-152. https://doi.org/10.15381/rpb.v12i1.2369
Brandão-Costa, RMP., Araújo, VF., Porto, ALF. (2018). CgTI, a novel thermostable Kunitz trypsin-inhibitor purified from Cassia grandis seeds: Purification, characterization and termiticidal activity. International Journal of Biological Macromolecules, 118(Pt B), 2296-306. https://doi.org/10.1016/j.ijbiomac.2018.07.110
Brousett-Minaya, M.A., Baldasso, P.A., Marangoni, S. (2013). Biochemical and Pharmacological Characterization of TLBbar, a New Serine Protease with Coagulant Activity from Bothrops barnetti Snake Venom. Journal of Toxins. 2013, 1-11, https://doi.org/10.1155/2013/207170
Centro Nacional de Epidemiología, Prevención y Control de Enfermedades (CDC). (2024). Boletín Epidemiológico del Perú. Ministerio de Salud. https://www.dge.gob.pe/epipublic/uploads/boletin/boletin_202422_08_080424.pdf
Chino, M. (2019). Identificación y evaluación de impactos ambientales por afluencia turística en la playa Los Palos – Tacna. [Tesis para optar el título profesional de Ingeniero Ambiental], Facultad de Ingeniería. Universidad Privada de Tacna.
Consoli, R.A. & Oliveira, R.L. (1994). Principais mosquitos de importância sanitária no Brasil. Fiocruz.
Costa, M. D. S., De Paula, S. O., Martins, G. F., Zanuncio, J. C., Santana, A. E. G., Serrão, J. E. (2018). Modes of action of squamocin in the anal papillae of Aedes aegypti larvae. Physiological and Molecular Plant Pathology, 101, 172-177. https://doi.org/10.1016/j.pmpp.2017.04.001
Coy, C., Parra, J., Cuca, L. (2014). Caracterización química del aceite esencial e identificación preliminar de metabolitos secundarios en hojas de la especie Raputia heptaphylla (Rutaceae). Revista Elementos, 4(4). 32-39. http://dx.doi.org/10.1155/2013/207170
Dang, L. & Van Damme, E. J. M. (2015). Toxic proteins in plants. Phytochemistry, 117, 51-64. https://doi.org/10.1016/j.phytochem.2015.05.020
Dantzger, M., Vasconcelos, I. M., Scorsato, V., Aparicio, R., Marangoni, S., Macedo, M. L. R. (2015). Bowman–Birk proteinase inhibitor from Clitoria fairchildiana seeds: Isolation, biochemical properties and insecticidal potential. Phytochemistry, 118, 224-235. https://doi.org/10.1016/j.phytochem.2015.08.013
Durán-Ruiz, C. A., González-Esquinca, A. R., de-la-Cruz-Chacón, I. (2024). Annonaceous acetogenins: A comparative analysis of insecticidal activity. Revista Brasileira de Fruticultura, 46, e-508. https://doi.org/10.1590/0100-29452024508
Figueroa, D. P., Scott, S., González, C. R., Bizama, G., Flores-Mara, R., Bustamante, R., Canals, M. (2020). Estimating the climate change consequences on the potential distribution of Culex pipiens L. 1758, to assess the risk of West Nile virus establishment in Chile. Gayana (Concepción), 84 (1), 46-53. https://doi.org/10.4067/S0717-65382020000100046
Fisher, M. F., Zhang, J., Berkowitz, O., Whelan, J., Mylne, J. S. (2019). Novel Cyclic Peptides in Seed of Annona muricata are Ribosomally Synthesized. Journal of Natural Products, 83(4), 1167-1173 https://doi.org/10.1101/647552
Fong, C. R., Bittick, S. J., Fong, P. (2018). Simultaneous synergist, antagonistic and additive interactions between multiple local stressors all degrade algal turf communities on coral reefs. Journal of Ecology, 106(4), 1390-1400. https://doi.org/10.1111/1365-2745.12914
Friedman, M. (2004). Applications of the Ninhydrin Reaction for Analysis of Amino Acids, Peptides, and Proteins to Agricultural and Biomedical Sciences. Journal of Agricultural and Food Chemistry, 52(3), 385-406. https://doi.org/10.1021/jf030490p
Grossman, MK., Oliver, SV., Brooke, BD., Thomas, MB. (2020). Use of alternative bioassays to explore the impact of pyrethroid resistance on LLIN efficacy. Parasites Vectors, 13(1),179. https://doi.org/10.1186/s13071-020-04055-9.
Ha, T. V., Kim, W., Nguyen-Tien, T., Lindahl, J., Nguyen-Viet, H., Thi, N. Q., Nguyen, H. V., Unger, F., Lee, H. S. (2021). Spatial distribution of Culex mosquito abundance and associated risk factors in Hanoi, Vietnam. PLOS Neglected Tropical Diseases, 15(6), e0009497. https://doi.org/10.1371/journal.pntd.0009497
Harte, S. J., Bray, D. P., Nash-Woolley, V., Stevenson, P. C., Fernández-Grandon, G. M. (2024). Antagonistic and additive effect when combining biopesticides against the fall armyworm, Spodoptera frugiperda. Scientific Reports, 14(1), 6029. https://doi.org/10.1038/41598-024-56599-w
Heng, M. Y., Tan, S. N., Yong, J. W. H., Ong, E. S. (2013). Emerging green technologies for the chemical standardization of botanicals and herbal preparations. TrAC Trends in Analytical Chemistry, 50, 1-10. https://doi.org/10.1016/j.trac.2013.03.012
Hothorn LA. (2014). Statistical evaluation of toxicological bioassays – a review. Toxicol Research, 3(6), 418-32. https://doi.org/10.1039/c4tx00047a.
Instituto Nacional de Salud. (2024). Rotación de insecticidas para el control de Aedes aegypti. Ministerio de Salud. https://dn.www.gob.pe/uploads/document/file/6028979/5338114-revision-rapida-n-01-2024-rotacion-de-insecticidas-y-aedes-aegypti%282%29.pdf
Instituto Nacional de Salud. (1999). Registro y control de calidad de recursos y productos naturales de uso en salud. Vol. 1. Ministerio de Salud. Lima. https://repositorio.ins.gob.pe/handle/20.500.14196/169.
Iranshahy, M., Quinn, R. J., Iranshahi, M. (2014). Biologically active isoquinoline alkaloids with drug-like properties from the genus Corydalis. RSC Advances, 4(31), 15900. https://doi.org/10.1039/C3RA47944G
Karunarathne, P., Pocquet, N., Labbé, P., Milesi, P. (2022). BioRssay: An R package for analyses of bioassays and probit graphs. Parasites & Vectors, 15(1), 35.
Kassambara, A. (2023). rstatix:Pipe-Friendly Framework for Basic Statistical Tests (R package version 0.7.2). https://CRAN.R-project.org/package=rstatix.
Kauffman, E., Payne, A., Franke, M., Schmid, M., Harris, E., Kramer, L. (2017). Rearing of Culex spp. and Aedes spp. Mosquitoes. Bio Protocol, 7(17), e2542. https://doi.org/10.21769/BioProtoc.2542
Kocyigit, E., Kocaadam-Bozkurt, B., Bozkurt, O., Ağagündüz, D., Capasso, R. (2023). Plant Toxic Proteins: Their Biological Activities, Mechanism of Action and Removal Strategies. Toxins, 15(6), 356. https://doi.org/10.3390/toxins15060356
Lagarda-Díaz, I., Guzmán-Partida, A., Vázquez-Moreno, L. (2017). Legume Lectins: Proteins with Diverse Applications. International Journal of Molecular Sciences, 18(6), 1242. https://doi.org/10.3390/ijms18061242
Mansour, S. A., Bakr, R. F., Hamouda, L. S. (2010). Toxic and Synergistic Properties of Several Botanical Extracts against Larval and Adult Stages of the Mosquito, Anopheles pharoensis. Biopesticides International, 6(2), 129-145.
Moghadamtousi, S., Fadaeinasab, M., Nikzad, S., Mohan, G., Ali, H., Kadir, H. (2015). Annona muricata (Annonaceae): A Review of Its Traditional Uses, Isolated Acetogenins and Biological Activities. International Journal of Molecular Sciences, 16(7), 15625-15658. https://doi.org/10.3390/ijms160715625
Monsour, S. A., Bakr, R. F., Mohamed, R. I., Hasaneen, N. M. (2011). Larvicidal Activity of Some Botanical Extracts, Commercial Insecticides and their Binary Mixtures Against the Housefly, Musca domestica L. The Open Toxinology Journal, 4(1), 1-13. https://doi.org/10.2174/1875414701104010001
Neglo, D., Tettey, C. O., Essuman, E. K., Amenu, J. D., Mills-Robertson, F. C., Sedohia, D., Boakye, A. A., Abaye, D. A. (2021). Evaluation of the Modulatory Effect of Annona muricata Extracts on the Activity of Some Selected Antibiotics against Biofilm-Forming MRSA. Evidence-Based Complementary and Alternative Medicine, 2021, 1-9. https://doi.org/10.1155/2021/9342110
Ohba, S., Ohashi, K., Pujiyati, E., Higa, Y., Kawada, H., Mito, N., Takagi, M. (2013). The Effect of Pyriproxyfen as a “Population Growth Regulator” against Aedes albopictus under Semi-Field Conditions. PLoS ONE, 8(7), e67045. https://doi.org/10.1371/journal.pone.0067045
Pant, M., Dubey, S., Patanjali, P. K. (2016). Recent Advancements in Bio-botanical Pesticide Formulation Technology Development. En Vijay Veer & R. Gopalakrishnan (Eds.), Herbal Insecticides, Repellents and Biomedicines: Effectiveness and Commercialization (pp. 117-126). Springer India. https://doi.org/10.1007/978-81-322-2704-5_7
Parthiban, E., Arokiyaraj, C., Ramanibai, R. (2020a). Annona muricata: An alternate mosquito control agent with special reference to inhibition of detoxifying enzymes in Aedes aegypti. Ecotoxicology and Environmental Safety, 189, 110050. https://doi.org/10.1016/.ecoenv.2019.110050
Parthiban, E., Arokiyaraj, C., Janarthanan, S., Ramanibai, R. (2020b). Purification, characterization of mosquito larvicidal lectin from Annona muricata and its eco-toxic effect on non-target organism. Process Biochemistry, 99, 357-366. https://doi.org/10.1016/j.procbio.2020.09.025
Rajput, D., Patil, U. K., Chauhan, D. N., Shah, K., Chauhan, N. S. (2023). Potentials of natural products in vector-borne diseases management: Current and future perspectives. En Natural Products in Vector-Borne Disease Management (pp. 1-25). Elsevier. https://doi.org/10.1016/B978-0-323-91942-5.00015-X
Reis, L. A. M., Silva, E. V. P. D., Dias, D. D., Freitas, M. N. O., Caldeira, R. D., Araújo, P. A. D. S., Silva, F. S. D., Rosa Junior, J. W., Brandão, R. C. F., Nascimento, B. L. S. D., Martins, L. C., Neto, J. P. N. (2023). Vector Competence of Culex quinquefasciatus from Brazil for West Nile Virus. Tropical Medicine and Infectious Disease, 8(4), 217. https://doi.org/10.3390/tropicalmed8040217
Richards, S. L., Byrd, B. D., Reiskind, M. H., White, A. V. (2020). Assessing Insecticide Resistance in Adult Mosquitoes: Perspectives on Current Methods. Environmental Health Insights, 14, 117863022095279. https://doi.org/10.1177/1178630220952790
Riley-Saldaña, C. A., Cruz-Ortega, M. D. R., Martínez-Vázquez, M., De-la-Cruz-Chacón, I., Castro-Moreno, M., González-Esquinca, A. R. (2017). Acetogenins and alkaloids during the initial development of Annona muricata L. (Annonaceae). Zeitschrift Für Naturforschung C, 72(11-12), 497-506. https://doi.org/10.1515/znc-2017-0060
Robertson, JL. (2017). Bioassays with arthropods. 3th. ed. CRC Press, Taylor & Francis Group. Rodrigues, A. M., Silva, A. A. S., Pinto, C. C. C., Santos, D. L. D., Freitas, J. C. C. D., Martins, V. E. P., Morais, S. M. D. (2019). Larvicidal and Enzymatic Inhibition Effects of Annona Muricata Seed Extract and Main Constituent Annonacin against Aedes aegypti and Aedes albopictus (Diptera: Culicidae). Pharmaceuticals, 12(3), 112. https://doi.org/10.3390/ph12030112
Seiber, J. N., Coats, J., Duke, S. O., Gross, A. D. (2014). Biopesticides: State of the Art and Future Opportunities. Journal of Agricultural and Food Chemistry, 62(48), 11613-11619. https://doi.org/10.1021/jf504252n
Shocket, M. S., Verwillow, A. B., Numazu, M. G., Slamani, H., Cohen, J. M., El Moustaid, F., Rohr, J., Johnson, L. R., Mordecai, E. A. (2020). Transmission of West Nile and five other temperate mosquito-borne viruses peaks at temperatures between 23°C and 26°C. eLife, 9, e58511. https://doi.org/10.7554/eLife.58511
Valencia, E., Mac, D., Cuyos, M., Dueñas, R. (2005). Extracción, identificación y evaluación de saponinas. Biotempo, 5, 31-36. https://revistas.urp.edu.pe/index.php/Biotempo/article/download/889/805/1958
Vandenborre, G., Smagghe, G., Van Damme, E. J. M. (2011). Plant lectins as defense proteins against phytophagous insects. Phytochemistry, 72(13), 1538-1550. https://doi.org/10.1016/j.phytochem.2011.02.024
Vander-Does, A., Labib, A., Yosipovitch, G. (2022). Update on mosquito bite reaction: Itch and hypersensitivity, pathophysiology, prevention, and treatment. Frontiers in Immunology, 13, 1024559. https://doi.org/10.3389/fimmu.2022.1024559
World Health Organization (WHO). (2014). A global brief on vector-borne diseases. World Health Organization. https://iris.who.int/bitstream/handle/10665/111008/WHO_DCO_WHD_2014.1_eng.pdf?sequence=1&isAllowed=y
World Health Organization (WHO). (2005). Guidelines for laboratory and field testing of mosquito larvicides. World Health Organization. https://iris.who.int/handle/10665/69101
Zamora-Natera, J.F., Bernal-Alcocer, A., Ruiz-López, M. (2005). Perfil de Alcaloides de Semillas de Lupinus exaltatus Zucc. (Fabaceae) y la Evaluación Antifúngica del Extracto Alcaloideo y Lupanina contra Fitopatógenos. Revista mexicana de fitopatología, 23(2), 124-129.
Zubaidi, S. N., Mohd Nani, H., Ahmad Kamal, M. S., Abdul Qayyum, T., Maarof, S., Afzan, A., Mohmad Misnan, N., Hamezah, H. S., Baharum, S. N., Mediani, A. (2023). Annona muricata: Comprehensive Review on the Ethnomedicinal, Phytochemistry, and Pharmaco-logical Aspects Focusing on Antidiabetic Properties. Life, 13(2), 353. https://doi.org/10.3390/life13020353
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