The Cytotoxic Activity of Crude Aqueous Annona Plant-Derived Extracts on Spodoptera frugiperda, Cell Lines

Jesús A. Polo Olivella, Marlinda Lobo de Souza, Ericsson Coy-Barrera, Jhon F. Betancur Pérez, Jorge W. Arboleda Valencia

Abstract

The excessive use of agrochemicals in agriculture to control insect pests has generated several environmental problems related to pollution and health risks for farmers. Therefore, chemical control has been proposed, including using products with plant origin, as an alternative to problematic, chemically-synthetized agents. These natural sources produce great numbers of bioactive molecules, and many have been reported to exhibit insecticidal effects. Recent studies have described the presence of bioactive compounds in tissue extracts from Annona plants, which are now considered useful in support of certain agricultural production processes. The cytotoxic effect of A. squamosa and A. muricata leaf extracts was tested on SF-21 and SF-9 insect cell lines obtained from Spodoptera frugiperda. Results showed that extracts of A. squamosa were more effective, as they gradually reduce cellular viability at 72 hours following exposure. Treatments with A. squamosa were significantly different from the negative control, whereas treatment with A. muricata behaved similarly to the control (i.e., no cytotoxic effect). Morphological changes in cells exposed to A. squamosa extracts were also observed. These included modifications in the structure and the shape of cell nuclei, generalized vacuolization, and membrane lyses. The effect observed by A. squamosa extracts on the tested cell lines represents relevant information regarding the potential use of plant-derived compounds from these species as alternatives for insect-specific pest control.

 

 

Keywords: bioprospecting, Annona sp., biological activity.

 

 


Full Text:

PDF


References


AHMED T., SHAHID M., NOMAN M., NIAZI M. B. K., ZUBAIR M., ALMATROUDI A., KHURSHID M., TARIQ F., MUMTAZ R., and LI B. Bioprospecting a native silver-resistant Bacillus safensis strain for green synthesis and subsequent antibacterial and anticancer activities of silver nanoparticles. Journal of Advanced Research, 2020, 24: 475-483. https://doi.org/10.1016/j.jare.2020.05.011

FERNANDES B., VIDIGAL J., CORREIA R., CARRONDO M. J., ALVES P. M., TEIXEIRA A. P., and ROLDÃO A. Adaptive laboratory evolution of stable insect cell lines for improved HIV-Gag VLPs production. Journal of Biotechnology, 2020, 307: 139-147. https://doi.org/10.1016/j.jbiotec.2019.10.004

VAUGHN J. L., GOODWIN R. H., TOMPKINS G. J., and MCCAWLEY P. The establishment of two cell lines from the insect spodoptera frugiperda (lepidoptera; noctuidae). In Vitro, 1977, 13: 213–217. https://doi.org/10.1007/BF02615077

MISHRA V. A Comprehensive Guide to the Commercial Baculovirus Expression Vector Systems for Recombinant Protein Production. Protein and Peptide Letters, 2020, 27(6): 529-537. https://doi.org/10.2174/0929866526666191112152646

KHATRI S., PAKUWAL P., and KHANAL S. Integrated pest management of fall armyworm infestations in maize fields in Nepal: A review. Archives of Agriculture and Environmental Science, 2020, 5(4): 583-591. https://doi.org/10.26832/24566632.2020.0504023

NAGOSHI R. N., NAGOSHI B. Y., CAÑARTE E., NAVARRETE B., SOLÓRZANO R., and GARCÉS-CARRERA S. Genetic characterization of fall armyworm (Spodoptera frugiperda) in Ecuador and comparisons with regional populations identify likely migratory relationships. Plos One, 2019, 14(9): e0222332. https://doi.org/10.1371/journal.pone.0222332

MARTINELLI S., CLARK P. L., ZUCCHI M. I., SILVA-FILHO M., FOSTER J., and OMOTO C. Genetic structure and molecular variability of Spodoptera frugiperda (Lepidoptera: Noctuidae) collected in maize and cotton fields in Brazil. Bulletin of Entomological Research, 2007, 97: 225–231. https://doi.org/10.1017/S0007485307004944

THUMAR R. K., ZALA M. B., VARMA H. S., DHOBI C. B., PATEL B. N., PATEL M. B., and BORAD P. K. Evaluation of insecticides against fall armyworm, Spodoptera frugiperda (JE Smith) infesting maize. 2020.

KALLESHWARASWAMY C. M., MARUTHI M. S., and PAVITHRA H. B. Biology of invasive fall army worm Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) on maize. Indian Journal of Entomology, 2018, 80(3): 540-543. https://doi.org/10.5958/0974-8172.2018.00238.9

BATEMAN M. L., DAY R. K., LUKE B., EDGINGTON S., KUHLMANN U., and COCK M. J. Assessment of potential biopesticide options for managing fall armyworm (Spodoptera frugiperda) in Africa. Journal of Applied Entomology, 2018, 142(9): 805-819. https://doi.org/10.1111/jen.12565

LEMES A. R., MARUCCI S. C., COSTA JR. V., et al. Selection of strains from Bacillus thuringiensis genes containing effective in the control of Spodoptera frugiperda. Bt Research, 2015, 6: 8.

DOS SANTOS C. A. M., DO NASCIMENTO J., GONÇALVES K. C., SMANIOTTO G., DE FREITAS ZECHIN L., DA COSTA FERREIRA M., and POLANCZYK R. A. Compatibility of Bt biopesticides and adjuvants for Spodoptera frugiperda control. Scientific Reports, 2021, 11(1): 1-8. https://doi.org/10.1038/s41598-021-84871-w

ALVES D. S., MACHADO A. R. T., CAMPOS V. A. C., OLIVEIRA D. F., and CARVALHO G. A. Selection of Annonaceae Species for the Control of Spodoptera frugiperda (Lepidoptera: Noctuidae) and Metabolic Profiling of Duguetia lanceolata Using Nuclear Magnetic Resonance Spectroscopy. Journal of Economic Entomology, 2016, 109: 649–659. https://doi.org/10.1093/jee/tov396

KEDIA A., PRAKASH B., MISHRA P. K., SINGH P., and DUBEY N. K. Botanicals as eco friendly biorational alternatives of synthetic pesticides against Callosobruchus spp. (Coleoptera: Bruchidae)—a review. Journal of Food Science and Technology, 2015, 52: 1239–1257. https://doi.org/10.1007/s13197-013-1167-8

SHANIBA V. S., AZIZ A. A., JOSEPH J., JAYASREE P. R., and KUMAR P. M. Synthesis, Characterization and Evaluation of Antioxidant and Cytotoxic Potential of Annona muricata Root Extract-derived Biogenic Silver Nanoparticles. Journal of Cluster Science, 2021. https://doi.org/10.1007/s10876-021-01981-1

FREITAS A. F., PEREIRA F. F., FORMAGIO A. S. N., LUCCHETTA J. T., VIEIRA M. C., and MUSSURY R. M. Effects of Methanolic Extracts of Annona Species on the Development and Reproduction of Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae). Neotropical Entomology, 2014, 43: 446–452. https://doi.org/10.1007/s13744-014-0225-x

SIB COLOMBIA ¿Cuántas especies registradas hay en Colombia? 2021. https://cifras.biodiversidad.co/

FERRAZ R. P. C., BOMFIM D. S., CARVALHO N. C., SOARES M. B. P., PINHEIRO M. L. B., COSTA E. V., and BEZERRA D. P. Cytotoxic properties of the leaf essential oils of Guatteria blepharophylla and Guatteria hispida (Annonaceae). Flavour and Fragrance Journal, 2014, 29: 228–232. https://doi.org/10.1002/ffj.3199

OWOLABI M. S., OGUNDAJO A. L., DOSOKY N. S., and SETZER W. N. The Cytotoxic Activity of Annona muricata Leaf Oil from Badagary, Nigeria. American Journal of Essential Oils and Natural Products, 2013, 1(1): 1–3. https://www.essencejournal.com/archives/2013/1/1/A/1

WANG D. S., RIZWANI G. H., GUO H., AHMED M., AHMED M., HASSAN S. Z., HASSAN A., CHEN Z. S., and XU R. H. Annona squamosa Linn: cytotoxic activity found in leaf extract against human tumor cell lines. Pakistan Journal of Pharmaceutical Sciences, 2014, 27: 1559–1563.

NAIK A. V., DESSAI S. N., and SELLAPPAN K. Antitumour activity of Annona muricata L. leaf methanol extracts against Ehrlich Ascites Carcinoma and Dalton’s Lymphoma Ascites mediated tumours in Swiss albino mice. Libyan Journal of Medicine, 2021, 16(1): 1846862. https://doi.org/10.1080/19932820.2020.1846862

HAYKAL T., NASR P., HODROJ M. H., TALEB R. I., SARKIS R., MOUJABBER M. N. E., and RIZK S. Annona cherimola seed extract activates extrinsic and intrinsic apoptotic pathways in leukemic cells. Toxins, 2019, 11(9): 506. https://doi.org/10.3390/toxins11090506

BRÍGIDO H. P. C., CORREA-BARBOSA J., DA SILVA-SILVA J. V., COSTA E. V. S., PERCÁRIO S., and DOLABELA M. F. Antileishmanial activity of Annona species (Annonaceae). SN Applied Sciences, 2020, 2(9): 1524. https://doi.org/10.1007/s42452-020-03340-7

YAMTHE L. R. T., FOKOU P. V. T., MBOUNA C. D. J., KEUMOE R., NDJAKOU B. L., DJOUONZO P. T., MFOPA A. N., LEGAC J., TSABANG N., GUT J., ROSENTHAL P. J., and BOYOM F. F. Extracts from Annona Muricata L. and Annona Reticulata L. (Annonaceae) Potently and Selectively Inhibit Plasmodium Falciparum. Medicines, 2015, 2(2): 55–66. https://doi.org/10.3390/medicines2020055

ALI S. S., AHMAD S., AHMED S. S., RIZWANA H., SIDDIQUI S., ALI S. S., RATTAR I. A., and SHAH M. A. Effect of Biopesticides Against Sucking Insect Pests of Brinjal Crop Under Field Conditions. Journal of Basic & Applied Sciences, 2016, 12: 41–49. http://dx.doi.org/10.6000/1927-5129.2016.12.06

CHEN Y. Y., MA C. Y., WANG M. L., LU J. H., HU P., CHEN J. W., LI X., and CHEN Y. Five new ent-kaurane diterpenes from Annona squamosa L. pericarps. Natural Product Research, 2020, 34(15): 2243-2247. https://doi.org/10.1080/14786419.2019.1582048

GEORGE V. C., KUMAR D. R. N., RAJKUMAR V., SURESH P. K., and KUMAR R. A. Quantitative assessment of the relative antineoplastic potential of the n-butanolic leaf extract of Annona Muricata Linn. in normal and immortalized human cell lines. Asian Pacific Journal of Cancer Prevention, 2012, 13: 699–704. https://doi.org/10.7314/APJCP.2012.13.2.699

STROBER W. Trypan Blue Exclusion Test of Cell Viability. Current Protocols in Immunology, 2015, 111: 1–3. https://doi.org/10.1002/0471142735.ima03bs111

PINTO M. F. S., FENSTERSEIFER I. C. M., MIGLIOLO L., SOUSA D. A., DE CAPDVILLE G., ARBOLEDA-VALENCIA J. W., COLGRAVE M. L., CRAIK D. J., MAGALHÃES B. S., DIAS S. C., and FRANCO O. L. Identification and structural characterization of novel cyclotide with activity against an insect pest of sugar cane. Journal of Biological Chemistry, 2012, 287: 134–147. https://doi.org/10.1074/jbc.M111.294009

SINGLETON V. L., ORTHOFER R., and LAMUELA-RAVENTÓS R. M. Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods in Enzymology, 1998, 299: 152–178. https://doi.org/10.1016/S0076-6879(99)99017-1

BAJČAN D., HARANGOZO Ľ., HRABOVSKÁ D., and BONČÍKOVÁ D. Optimizing conditions for spectrophotometric determination of total polyphenols in wines using Folin-Ciocalteu reagent. Journal of Microbiology, Biotechnology and Food Sciences, 2013, 2: 1271-1280. https://www.jmbfs.org/18_jmbs_bajcan2_fbp_f/?issue_id=1716&article_id=17

PÜNTENER W. Manual for Field Trials in Plant Protection. Google Books. 1992. https://books.google.com.co/books/about/Manual_for_Field_Trials_in_Plant_Protect.html?id=hEWxnAEACAAJ&redir_esc=y

BAKR E. Abbot and Henderson-Tilton calculations. http://www.ehabsoft.com/ldpline/onlinecontrol.htm

EGYDIO-BRANDÃO A. P. M., NOVAES P., and SANTOS D. Y. A. C. Alkaloids from Annona: Review from 2005 to 2016. JSM Biochemistry & Molecular Biology, 2017, 4(3): 1031. https://www.researchgate.net/profile/Anary-Egydio/publication/322102874_Central_Bringing_Excellence_in_Open_Access_Alkaloids_from_Annona_Review_from_2005_to_2016/links/5a452acf0f7e9ba868a93161/Central-Bringing-Excellence-in-Open-Access-Alkaloids-from-Annona-Review-from-2005-to-2016.pdf

CASSOU E., TRAN D. N., NGUYEN T. H., DINH T. X., NGUYEN C. V., CAO B. T., JAFFEE S., and RU J. An overview of agricultural pollution in Vietnam: summary report 2017. World Bank, Washington, District of Columbia, 2017. https://openknowledge.worldbank.org/handle/10986/29242

KHALID M. A., & SHAHID S. M. A. Environmental Pollution and Climate Change Impacts on Human Health with Particular Reference to Brain: A Review. In: KHALID M. A., & SHAHID S. M. A. Phytopharmaceuticals for Brain Health. CRC Press, New York, 2017: 39-68. https://www.taylorfrancis.com/chapters/edit/10.1201/9781315152998-3/environmental-pollution-climate-change-impacts-human-health-particular-reference-brain-monowar-alam-khalid-syed-monowar-alam-shahid?context=ubx&refId=da23a50c-8997-4fa4-a745-27a38c90e327

HAJEK A. E., & EILENBERG J. Natural enemies: an introduction to biological control. Cambridge University Press, 2018. https://doi.org/10.1017/9781107280267

ZHOU K., GOODMAN C. L., RINGBAUER J., SONG Q., BEERNTSEN B., and STANLEY D. Establishment of two midgut cell lines from the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae). In Vitro Cellular & Developmental Biology-Animal, 2020, 56(1): 10-14. https://doi.org/10.1007/s11626-019-00420-w

VALENCIA J. W. A., BUSTAMANTE A. L. G., JIMÉNEZ A. V., and GROSSI-DE-SÁ M. F. Cytotoxic activity of fungal metabolites from the pathogenic fungus Beauveria bassiana: An intraspecific evaluation of beauvericin production. Current Microbiology, 2011, 63: 306–312. https://doi.org/10.1007/s00284-011-9977-2

MINATEL I. O., BORGES C. V., FERREIRA M. I., GOMEZ H. A. G., CHEN C. Y. O., and LIMA G. P. P. Phenolic compounds: Functional properties, impact of processing and bioavailability. In: SOTO-HERNÁNDEZ M., PALMA-TENANGO M., and GARCÍA-MATEOS R. (eds.) Phenolic Compounds - Biological Activity. IntechOpen, London, 2017: 1-24. https://doi.org/10.5772/66368

CHEN L., TENG H., XIE Z., CAO H., CHEANG W. S., SKALICKA-WONIAK K., GEORGIEV M. I., and XIAO J. Modifications of dietary flavonoids towards improved bioactivity: An update on structure–activity relationship. Critical Reviews in Food Science and Nutrition, 2018, 58(4): 513-527. https://doi.org/10.1080/10408398.2016.1196334

KUNDU N., ROY S., MUKHERJEE D., MAITI T. K., and SARKAR N. Unveiling the interaction between fatty-acid-modified membrane and hydrophilic imidazolium-based ionic liquid: understanding the mechanism of ionic liquid cytotoxicity. The Journal of Physical Chemistry B, 2017, 121(34): 8162-8170. https://doi.org/10.1021/acs.jpcb.7b06231

CORIA-TÉLLEZ A. V., MONTALVO-GÓNZALEZ E., YAHIA E. M., and OBLEDO-VÁZQUEZ E. N. Annona muricata: A comprehensive review on its traditional medicinal uses, phytochemicals, pharmacological activities, mechanisms of action and toxicity. Arabian Journal of Chemistry, 2018, 11(5): 662-691. https://doi.org/10.1016/j.arabjc.2016.01.004

MUTLU ALTUNDAĞ E., YILMAZ A. M., KOÇTÜRK S., TAGA Y., and YALÇIN A. S. Synergistic induction of apoptosis by quercetin and curcumin in chronic myeloid leukemia (K562) cells. Nutrition and Cancer, 2018, 70(1): 97-108. https://doi.org/10.1080/01635581.2018.1380208


Refbacks

  • There are currently no refbacks.