Recycled pequi (Caryocar brasiliense, Camb.) shell ethanolic extract induces apoptosis in canine osteosarcoma cells
DOI:
https://doi.org/10.1590/1809-6891v22e-71198Abstract
Osteosarcoma is a mesenchymal cancer associated with high mortality in dogs and in humans. The biodiversity-rich Cerrado, the predominant biome in the Midwest region of Brazil, is native to locally appreciated fruits such as pequi (Caryocar brasiliense, Camb). Although this plant has been frequently used in folk medicine, the pharmacological properties of pequi fruit shells have not been fully evaluated. Thus, this study aimed to determine the cytotoxic activity of ethanol extract of recycled pequi shells on canine osteosarcoma cells in vitro. Cells were cultured and treated with final extract concentrations of 0, 0.029 µg/µL, 0.29 µg/µL, and 2.91 µg/µL for 24, 48, or 72 hours. Cell viability assay using trypan blue exclusion method and tetrazolium reduction method, cell survival assay, and double labeling with annexin V and propidium iodide were performed in the treated osteosarcoma cells. These allowed the determination of IC50, survival fraction, and type of cell death, respectively. Pequi shell ethanol extract at a concentration of 2.91 µg/µL showed the greatest inhibition of osteosarcoma cell growth in vitro, resulting in a 71.80% decrease in growth compared to the control. The mean IC50 was 155.2 μg/mL at 72 hours. The calculated survival fractions showed that cell growth at 72 hours was 3.33% lower in cells treated with 2.91 µg/µL extract. Results from the double labeling experiment suggest that apoptosis was the predominant type of cell death in cells treated with 2.91 µg/µL extract. These results demonstrate that ethanol extract of recycled pequi shells promotes apoptosis in canine osteosarcoma cells.
Keywords: Antineoplastic; canine osteosarcoma; Cerrado biome; D-17; pequi; sustainability; tannins.
Downloads
References
Wilk SS, Zabielska-Koczywas KA. Molecular mechanisms of canine osteosarcoma metastasis [Internet]. Vol. 22, International journal of molecular sciences. 2021. p. 3639. Available from: https://10.3390/ijms22073639
Leonardi L, Scotlandi K, Pettinari I, Benassi MS, Porcellato I, Pazzaglia L. Mirnas in canine and human osteosarcoma: A highlight review on comparative biomolecular aspects [Internet]. Vol. 10, Cells. 2021. p. 1–9. Available from: https://10.3390/cells10020428
Cortelo PC, Demarque DP, Dusi RG, Albernaz LC, Braz-Filho R, Goncharova EI, Bokesch HR, Gustafson KR, Beutler JA, Espindola LS. A molecular networking strategy: High-throughput screening and chemical analysis of brazilian cerrado plant extracts against cancer cells. Cells. 2021;10(3):1–13. Available from: https://10.3390/cells10030691
Palmeira SM, Silva PRP, Ferrão JSP, Ladd AABL, Dagli MLZ, Grisolia CK, Hernandez-Blazquez FJ. Chemopreventive effects of pequi oil (Caryocar brasiliense Camb.) on preneoplastic lesions in a mouse model of hepatocarcinogenesis. Eur J Cancer Prev. 2016;25(4):299–305. Available from: https://10.1097/CEJ.0000000000000187
Nunes C dos R, Arantes MB, de Faria Pereira SM, da Cruz LL, de Souza Passos M, de Moraes LP, Vieira IJC, de Oliveira DB. Plants as Sources of Anti-Inflammatory Agents [Internet]. Vol. 25, Molecules. 2020. p. 3726. Available from: https://10.3390/molecules25163726
Arnhold E. Package in the R environment for analysis of variance and complementary analyses. Brazilian J Vet Res Anim Sci. 2014;50(6):488–92. Available from: https://10.11606/issn.1678-4456.v50i6p488-492
De Oliveira CB, Comunello LN, Maciel ÉS, Giubel SR, Bruno AN, Chiela ECF, Lenz G, Gnoatto SCB, Buffon A, Gosmann G. The inhibitory effects of phenolic and terpenoid compounds from Baccharis trimera in SiHa cells: Differences in their activity and mechanism of action. Molecules. 2013;18(9):11022–32. Available from: https://10.3390/molecules180911022
Ullah A, Munir S, Badshah SL, Khan N, Ghani L, Poulson BG, Emwas AH, Jaremko M. Important flavonoids and their role as a therapeutic agent [Internet]. Vol. 25, Molecules. 2020. p. 5243. Available from: https://10.3390/molecules25225243
Felipe KB, Kviecinski MR, Da Silva FO, Bücker NF, Farias MS, Castro LSEPW, De Souza Grinevicius VMA, Motta NS, Correia JFG, Rossi MH, Pedrosa RC. Inhibition of tumor proliferation associated with cell cycle arrest caused by extract and fraction from Casearia sylvestris (Salicaceae). J Ethnopharmacol. 2014;155(3):1492–9. Available from: https://10.1016/j.jep.2014.07.040
Cunha BLA, de França JP, Moraes AA de FS, Chaves ALF, Gaiba S, Fontana R, do Sacramento CK, Ferreira LM, de França LP. Evaluation of antimicrobial and antitumoral activity of Garcinia mangostana L. (Mangosteen) grown in Southeast Brazil. Acta Cir Bras. 2014;29(suppl 2):21–8. Available from: https://10.1590/S0102-86502014001400005
Ozi JM, Suffredini IB, Paciencia M, Frana SA, Dib LL. In vitro cytotoxic effects of Brazilian plant extracts on squamous cell carcinoma of the oral cavity. Braz Oral Res. 2011;25(6):519–25.
Isani G, Bertocchi M, Andreani G, Farruggia G, Cappadone C, Salaroli R, Forni M, Bernardini C. Cytotoxic Effects of Artemisia annua L. And pure artemisinin on the D-17 canine osteosarcoma cell line. Oxid Med Cell Longev. 2019;2019. Available from: https://10.1155/2019/1615758
De Oliveira TS, Thomaz DV, da Silva Neri HF, Cerqueira LB, Garcia LF, Gil HPV, Pontarolo R, Campos FR, Costa EA, Dos Santos FCA, De Souza Gil E, Ghedini PC. Neuroprotective effect of caryocar brasiliense camb. leaves is associated with anticholinesterase and antioxidant properties. Oxid Med Cell Longev. 2018;2018:9842908. Available from: https://10.1155/2018/9842908
Eom T, Kim E, Kim JS. In vitro antioxidant, antiinflammation, and anticancer activities and anthraquinone content from rumex crispus root extract and fractions. Antioxidants. 2020;9(8):1–13. Available from: https://10.3390/antiox9080726
Spiegler V, Greiffer L, Jacobtorweihen J, Asase A, Lanvers-Kaminsky C, Hempel G, Agyare C, Hensel A. In vitro screening of plant extracts traditionally used as cancer remedies in Ghana – 15-Hydroxyangustilobine A as the active principle in Alstonia boonei leaves. J Ethnopharmacol. 2021;265:113359. Available from: https://10.1016/j.jep.2020.113359
Ke H, Wang X, Zhou Z, Ai W, Wu Z, Zhang Y. Effect of weimaining on apoptosis and Caspase-3 expression in a breast cancer mouse model. J Ethnopharmacol. 2021;264:113363. Available from: https://10.1016/j.jep.2020.113363
Henklewska M, Pawlak A, Kutkowska J, Pruchnik H, Rapak A, Obminska-Mrukowicz B. In vitro effects of the activity of novel platinum (II) complex in canine and human cell lines. Vet Comp Oncol. 2019;17(4):497–506. Available from: https://10.1111/vco.12511
Shehata MG, Abu-Serie MM, Abd El-Aziz NM, El-Sohaimy SA. Nutritional, phytochemical, and in vitro anticancer potential of sugar apple (Annona squamosa) fruits. Sci Rep. 2021;11(1):6224. Available from: https://10.1038/s41598-021-85772-8
Chang Z, Jian P, Zhang Q, Liang W, Zhou K, Hu Q, Liu Y, Liu R, Zhang L. Tannins in: Terminalia bellirica inhibit hepatocellular carcinoma growth by regulating EGFR-signaling and tumor immunity. Food Funct. 2021;12(8):3720–39. Available from: https://10.1039/d1fo00203a
Yang HL, Liu HW, Shrestha S, Thiyagarajan V, Huang HC, Hseu YC. Antrodia Salmonea Induces Apoptosis and Enhances Cytoprotective Autophagy in Colon Cancer Cells. Aging (Albany NY). 2021;13(12):15964–89. Available from: https://10.18632/aging.203019
Chaudhry GES, Islamiah M, Zafar MN, Bakar K, Aziz NA, Saidin J, Sung YY, Muhammad TST. Induction of Apoptosis by Acanthaster planci sp., and Diadema setosum sp., Fractions in Human Cervical Cancer Cell Line, HeLa. Asian Pacific J Cancer Prev. 2021;22(5):1365–73. Available from: https://10.31557/APJCP.2021.22.5.1365
Ryu S, Park S, Lim W, Song G. Effects of luteolin on canine osteosarcoma: Suppression of cell proliferation and synergy with cisplatin. J Cell Physiol. 2019;234(6):9504–14. Available from: https://10.1002/jcp.27638
Park H, Park S, Bazer FW, Lim W, Song G. Myricetin treatment induces apoptosis in canine osteosarcoma cells by inducing DNA fragmentation, disrupting redox homeostasis, and mediating loss of mitochondrial membrane potential. J Cell Physiol. 2018;233(9):7457–66. Available from: https://10.1002/jcp.26598
Levine CB, Bayle J, Biourge V, Wakshlag JJ. Cellular effects of a turmeric root and rosemary leaf extract on canine neoplastic cell lines. BMC Vet Res. 2017;13(1). Available from: https://10.1186/s12917-017-1302-2
Jiang X, Wang X. Cytochrome C-mediated apoptosis [Internet]. Vol. 73, Annual Review of Biochemistry. 2004. p. 87–106. Available from: https://10.1146/annurev.biochem.73.011303.073706
Cruz VS, Rodrigues FA, Braga KMS, Machado PA, Filho CB, Prado YCL, Araújo EG. β Lapachone blocks the cell cycle and induces apoptosis in canine osteosarcoma cells1. Pesqui Vet Bras. 2018;38(12):2224–32. Available from: https://10.1590/1678-5150-PVB-5524
Soares NP, Nepomuceno LL, Cruz V de S, Arnhold E, Vieira V de S, Borges JC de A, Pereira DKS, Pereira KF, Araújo EG de. Curcumina promove apoptose extrínseca em células de osteossarcoma canino. Res Soc Dev. 2020;9(10):e7289109231. Available from: https://10.33448/rsd-v9i10.9231
Mans DRA, Rocha AB, Schwartsmann G. Anti‐Cancer Drug Discovery and Development in Brazil: Targeted Plant Collection as a Rational Strategy to Acquire Candidate Anti‐Cancer Compounds. Oncologist. 2000;5(3):185–98. Available from: https://10.1634/theoncologist.5-3-185
Published
How to Cite
Issue
Section
License
Copyright (c) 2022 CIÊNCIA ANIMAL BRASILEIRA (Brazilian Animal Science)
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g. in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
