Antiproliferative activity of Annona squamosa L. fractions on human tumor cell lines
DOI:
https://doi.org/10.5216/rbn.v21i1.74755Keywords:
Antitumoral, Cytocidal, Cytostatic, Pericarp, SeedsAbstract
Annona squamosa Linn. (Annonaceae) is a rich source of bioactive compounds, such as alkaloids, tannin, phenolic compounds, aromatic plyketides, steroids, diterpenes and mineral components. Several parts of this plant are traditionally used in the treatment of diabetes and cancer. The current assay evaluates antiproliferative activity of fractions of sugar-apple (A. squamosa) peel and seeds in eight human tumor cell lines (K-562, HT-29, PC-3, NCI-H460, MCF-7, NCI-ADR/RES, UACC-62, U251 e 786-0) and in a non-tumor cell line (HaCat), with doxorubicin as positive control. Cell differentiation was determined by spectrophometric quantification. Seed and peel fractions showed cytostatic and cytocidal effects on cell lines at different concentrations, except for K562. All fractions were selective for the NCI-H460 strain. However, other fractions had an antiproliferative effect on the other strains, especially on the methanol fraction of seeds, which showed the highest cytocidal percentage (up to 100%). Results indicate the potential of these fractions as sources of new chemotherapeutic and/or chemo-preventive agents to be isolated and identified.
Downloads
References
Alali, F. Q., X. X. Liu & J. L. McLaughlin. 1999. Annonaceous acetogenins: recent progress. J Nat Prod. 62: 504-540. DOI: https://doi.org/10.1021/np980406d
Ambrosio, S. R., K. Schorr & F. B. Costa. 2004. Terpenoids of Viguiera arenaria (Asteraceae). Biochem Syst Ecol. 32: 221-224. DOI: https://doi.org/10.1016/S0305-1978(03)00139-X
Anaya-Esparza, L. M., M. L. García-Magaña, J. A. Domiínguez-Ávila, E. M. Yahia, N. J. Salazar-López, G. A. González-Aguilar & E. Montalvo-González. 2020. Annonas: underutilized species as a potential source of bioactive compounds. Food Res Int. 138. DOI: https://doi.org/10.1016/j.foodres.2020.109775
Bhardwaj, A., G. Satpathy & R. K. Gupta. 2014. Preliminary screening of nutraceutical potential of Annona squamosa, an underutilized exotic fruit of India and its use as a valuable source in functional foods. J Pharmacogn Phytochem. 3: 172-180.
Blanchard, A. 2016. Mapping ethical and social aspects of cancer biomarkers. N Biotechnol. 33: 763-72. DOI: https://doi.org/10.1016/j.nbt.2016.06.1458
Biba, V. S., S. Lakshmi, G. S. Dhanya, & P. Remani. 2013. Phytochemical analysis of Annona squamosa seed extracts. Int Res J Pharm Appl Sci. 3: 29-31.
Carretero, J., P. P. Medina, R. Pio, L. M. Montuenga & M. Sanchez-Cespedes. 2004. Novel and natural knockout lung cancer cell lines for the LKB1/STK11 tumor supressor gene. Oncogene, 23: 4037-4040. DOI: https://doi.org/10.1038/sj.onc.1207502
Chandrababu, N. R., K. A. Niranjana, B. Komuraiah, S. K. V. N. Satya, K. J. Kotesh, K. V. S. Ramakrishna, N. V. Laxman & R. Sistla. 2012. Fatty acid derivatives from seeds of Annona squamosa Linn. J Chem Pharm Res. 4: 4558-4561.
Chang, F. R., J. L. Chen, C. Y. Lin, H. F. Chiu, M. J. Wu & Y. C. Wu. 1999. Bioactive acetogenins from the seeds of Annona atemoya. Phytochem, 51: 883-889. DOI: https://doi.org/10.1016/S0031-9422(99)00142-9
Chen, Y., S. S. Xu, J. W. Chen, Y. Wang, H. Q. Xu, N. B. Fan & L. Xiang. 2012. Anti-tumor activity of Annona squamosa seeds extract containing annonaceous acetogenin compounds. J Ethnopharmacol. 142: 462-466. DOI: https://doi.org/10.1016/j.jep.2012.05.019
Costa, A. C. F. & G. M. Cavalcante. 2018. Atividade Antitumoral in vitro de Prosopis juliflora frente a células de câncer de mama e câncer de ovário. Acta Biomed Bras. 9.
Fan, S., Q. Meng, K. Auborn, T. Carter & E. M. Rosen. 2006. BRCA1 and BRCA2 as molecular targets for phytochemicals indole-3-carbinol and genistein in breast and prostate cancer cells. Brit J Cancer. 94: 407-426. DOI: https://doi.org/10.1038/sj.bjc.6602935
Fernando, W & H. P. V. Rupasinghe. 2013. Anticancer properties of phytochemicals presente in medicinal plants of north America. pp. 159-180. In: M. Kulka (Ed.), Using old solutions to new problems - natural drug Discovery in the 21st century. Croatia: (InTech).
Fouche, G., G. M. Cragg, P. Pillary, N. Kolesnikova, V. J. Maharaj & J. Senabe. 2008. In vitro anticancer screening of South African plants. J Ethnopharmacol. 119: 455-461. DOI: https://doi.org/10.1016/j.jep.2008.07.005
Fujimoto, Y., C. Murasaki, K. Kakinuma, T. Eguchi, N. Ikekawa, M. Furuya, K. Hirayama, T. Ikekawa, M. Sahai, Y. K. Gupta & A. B. Ray. 1990. Squamostatin-A: unprecedented bis-tetrahydrofuran acetogenin from Annona squamosa. Tetrahedron Lett. 31: 535-538. DOI: https://doi.org/10.1016/0040-4039(90)87027-W
Gordaliza, M. 2007. Natural products as leads to anticancer drugs. Clin Transl Oncol. 9: 767-776. DOI: https://doi.org/10.1007/s12094-007-0138-9
Gray, I. D., A. R. Kross, M. E. Renfrew & P. Wood. 2019. Precision medicine in lifestyle medicine: the way of the future? Am J Lifestyle Med. 14: 169-86.
Guidoti, D. G. G., D. T. Guidoti, A. L. Romero, A. L. T. G. Ruiz, M. A. Foglio, J. E. Carvalho & C. L. M. S. C. Rocha. 2019. Kaurenoic acid from Annona squamosa L. exhibits antiproliferative effect on human tumor cell lines and induces apoptosis in Aspergillus nidulans. Fitos. 13: 122-136. DOI: https://doi.org/10.17648/2446-4775.2019.716
Guidoti, D. G. G., D. T. Guidoti, A. L. Romero & C. L. M. S. C. Rocha. 2021. Bioatividade de frações de sementes e pericarpo de Annona squamosa (Annonaceae) em Aspergillus nidulans. Rev Saúde Biol. 16. DOI: https://doi.org/10.54372/sb.2021.v16.2917
Hardie, D. G., F. A. Ross & S. A. Hawley. 2012. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol. 13: 251-62. DOI: https://doi.org/10.1038/nrm3311
Hirsch, H. A., D. Iliopoulos, P. N. Tsichlis & K. Struhl. 2009. Metformin selectively targets cancer stem cells and acts together with chemotherapy to block tumor growth and prolong remission. Cancer Res. 69: 7507-7511. DOI: https://doi.org/10.1158/0008-5472.CAN-09-2994
Holbeck, S. L. 2004. Update on NCI in vitro drug screen utilities. Eur J Cancer. 40: 785-793. DOI: https://doi.org/10.1016/j.ejca.2003.11.022
Hoop, D. C., L. Zeng, Z. Gu & J. L. S. McLaughlin. 1996. Squamotacin: an annonaceous acetogenin with cytotoxic seletivity for the human prostate tumor cell line (PC-3). J Nat Prod. 59: 97-99. DOI: https://doi.org/10.1021/np960124i
Inca. Instituto Nacional de Câncer, Ministério da Saúde. 2022. O que é cancer. Disponível em: <https://www.gov.br/inca/pt-br/assuntos/cancer/o-que-e-cancer>. Acesso em 10 dez. 2022.
Inoki, K., T. Zhu & K. L. Guan. 2003. TSC2 mediates cellular energy response to control cell growth and survival. Cell. 115: 577-590. DOI: https://doi.org/10.1016/S0092-8674(03)00929-2
Iriart, J. A. B. 2019. Medicina de precisão/medicina personalizada: análise crítica dos movimentos de transformação da biomedicina no início do século XXI. Cad Saúde Pública. 35. DOI: https://doi.org/10.1590/0102-311X00153118
Jacobo-Herrera, N. J., F. E. Jacobo-Herrera, A. Zentella-Dehesa, A. Andrade-Cetto, M. Heinrich & C. Pérez-Plasencia. 2016. Medicinal plants used in Mexican traditional medicine for the treatment of colorectal cancer. J Ethnopharmacol. 179: 391-402. DOI: https://doi.org/10.1016/j.jep.2015.12.042
Joy, B. & E. P. Remani. 2008. Antitumor constituents from Annona squamosa fruit pericarp. Med Chem Res. 17: 345-355. DOI: https://doi.org/10.1007/s00044-007-9070-3
Karna, P., S. Chagani, S. R. Gundala, P. C. Rida, G. Asif, V. Sharma, M. V. Gupta & R. Aneja. 2012. Benefits of whole ginger extract in prostate cancer. Brit J Nutr. 107: 473-484. DOI: https://doi.org/10.1017/S0007114511003308
Leung, H. Y, L. H. Yung, C. H. Poon, G. Shi, L. A. Lu & L. K. Leung. 2009. Genistein protects agains polycyclic aromatic hydrocarbon-induced oxidative DNA damage in non-cancerous breast cells MCF-10A. Brit J Nutr. 101: 257-262. DOI: https://doi.org/10.1017/S0007114508998457
Liaw, C. C., T. Y. Wu, F. R. Chang & Y. C. Wu. 2010. Historic perspectives on annonaceous acetogenins from the chemical bench to preclinical trials. Planta Med. 76: 1390-1404. DOI: https://doi.org/10.1055/s-0030-1250006
Liu, R. H. 2003. Health benefits of fruit and vegetables are from additive and synergistic combinations of phytochemicals. Am J Clin Nutr. 78: 517S-520S. DOI: https://doi.org/10.1093/ajcn/78.3.517S
Lizarte-Neto, F. S., D. P. C. Tirapelli, S. R. Ambrosio, C. R. Tirapelli, F. M. Oliveira, P. C. Novais, F. M. Peria, F. F. Oliveira, C. G. Carlotti & L. F. Tirapelli. 2013. Kaurene diterpene induces apoptosis in U87 human malignant glioblastoma cells by supression of anti-apoptotic signals and activation of cysteine proteases. Braz J Med Biol Res. 46: 71-78. DOI: https://doi.org/10.1590/1414-431X20121423
Lu, Z., J. L. McLaughlin & H. W. Mi. 1995. Asitribin and asimenins A and B, novel bioactive annonaceous acetogenins from the seeds of Asimia triloba. Heterocycles. 41: 1731-1742.
McLaughlin, J. L. 2008. Paw paw and cancer: annonaceous acetogenins from discovery to commercial products. J Nat Prod. 71: 1311-1321. DOI: https://doi.org/10.1021/np800191t
Mongelli, E., A. B. Pomilio, J. B. Sanchez, F. M. Guerra & G. M. Massanet. 2002. Ent-kaur-16-em-19-oic-acid, a KB cells cytotoxic diterpenoid from Elaeoselium foetidum. Phytother, 16, 387-388. DOI: https://doi.org/10.1002/ptr.955
Monks, A., D. Scudiero & P. Skenah. 1991. Feasibility of a high-flux anticancer drug screen using a diverse panel of cultured human tumor cell lines. J Natl Cancer Inst. 83: 757-766. DOI: https://doi.org/10.1093/jnci/83.11.757
Ndob, I. B., P. Champy, C. Gleye, G. Lewin & B. Akendengue. 2009. Annonaceous acetogenins: precursors from the seeds of Annona squamosa. Phytochem Lett. 29: 72-76. DOI: https://doi.org/10.1016/j.phytol.2008.11.006
Newman, D. J. 2008. Natural products as leads to potential drugs: an old process or the new hope for drug discovery? J Med Chem. 51: 2589-2599. DOI: https://doi.org/10.1021/jm0704090
Newman, D. J., G. M. Cragg, S. Holbeck & E. A. Sausville. 2002. Natural products and derivatives as leads to cell cycle pathway targets in cancer chemotherapy. Curr Cancer Drug Targets. 2: 279-308. DOI: https://doi.org/10.2174/1568009023333791
Newman, D. J. & G. M. Cragg. 2012. Natural products as a source of new drugs over the period 1981-2010. J Nat Prod. 75: 311. DOI: https://doi.org/10.1021/np200906s
Pandey, N. & D. Barve. 2011. Phytochemical and pharmacological review on Annona squamosa (Linn.). Int J Res Pharm Biomed Sci. 2: 1404-1412.
Pessina, A., A. Raimondi, A. Cerri, M. Piccirillo, M. G. Neri, C. Croera, P. Foti & E. Berti. 2001. High sensitity of human epidermal keratinocytes (HaCaT) to topoisomerase inhibitors. Cell Prolif. 34: 243-252. DOI: https://doi.org/10.1046/j.0960-7722.2001.00214.x
Pilatova, M., L. Varinska, P. Perjesi, M. Sarissky, L. Mirossay, P. Solar, A. Ostro & J. Mojzis. 2010. In vitro antiproliferative and antiangiogenic effects of synthetic chalcone analogues. Toxicol In Vitro. 24: 1347-1355. DOI: https://doi.org/10.1016/j.tiv.2010.04.013
Pillay, P., V. J. Maharaj & P. J. Smith. 2008. Investigating South African plants as a source of new antimalarial drugs. J Ethnopharmacol. 119: 438-454. DOI: https://doi.org/10.1016/j.jep.2008.07.003
Pontes, A. F, M. R. V. Barbosa & P. M. J. Maas. 2004. Flora paraibana: Annonaceae Juss. Acta Bot Bras. 18: 281-293. DOI: https://doi.org/10.1590/S0102-33062004000200008
Prakash, O., A. Kumar, P. Kumar & Ajeet. 2013. Anticancer potential of plants and natural products: a review. American J Pharmacol Sci. 1: 104-115. DOI: https://doi.org/10.12691/ajps-1-6-1
Sabir, S. M., S. D. Ahmad, A. Hamid, M. Q. Khan, M. I. Athayde, D. B. Santos, A. A. Boligon & J. B. T. Rocha. 2012. Antioxidant and hepatoprotective activity of ethanolic extract of leaves of Solidago microglossa containing polyphenolic compounds. Food Chem. 131: 741-747. DOI: https://doi.org/10.1016/j.foodchem.2011.09.026
Shah, S. C., V. Kayamba, R. M. Peek Jr & D. Heimburger. 2019. Cancer control in low-and Middle-income countries: is it time to consider screening? J Glob Oncol. 5: 1-8. DOI: https://doi.org/10.1200/JGO.18.00200
Sharma, A., A. K. Sharma, T. Chand, M. Khardiya & S. Agarwal. 2013. Preliminary phytochemical screening of fruit peel extracts of Annona squamosa Linn. J Curr Pharma Res. 4: 1038-1043.
Solowey, E., M. Lichtenstein, S. Sallon, H. Paavilainen, E. Solowey & H. Lorberboum-Galski. 2014. Evaluating medicinal plants for anticancer activity. Sci World J. 1-12. DOI: https://doi.org/10.1155/2014/721402
Srivastava, V., A. S. Negi, J. K. Kumar, M. M. Gupta & S. P. S. Khanuja. 2005. Plant-based anticancer molecules: a chemical and biological profile of some important leads. Bioorg Med Chem. 13: 5892-5908. DOI: https://doi.org/10.1016/j.bmc.2005.05.066
Sturdy, S. 2017. Personalised medicine and the economy of biotechnological promise. New Bioeth. 23: 30-37. DOI: https://doi.org/10.1080/20502877.2017.1314892
Tsiftsoglou, A. S., I. S. Pappas & I. S. Vizirianakis. 2003. Mechanisms involved in the induced differentiation of leukemia cells. Pharmacol Ther. 100: 257-290. DOI: https://doi.org/10.1016/j.pharmthera.2003.09.002
Zakaria, Z. A, M. S. Rofiee, A. M. Mohamed, L. K. The & M. Z. Salleh. 2011. In vitro antiproliferative and antioxidant activities and total phenolic contents of the extracts of Melastoma malabathricum leaves. J Acupunc Meridian Stud. 4: 248-56. DOI: https://doi.org/10.1016/j.jams.2011.09.016
Zhang, Y. 2006. Preparation of Annona squamosa lactone antitumor monomer compound and its application for preparing antitumor agent (Nanjing University of Traditional Chinese Medicine, Peop. Rep. China). Faming Zhuanli Shenqing Gongkai Shuomingshu. Patente: 1869031 A 20061129. Patent written in Chinese. Aplicação: CN 1008-578120060630.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Revista de Biologia Neotropical / Journal of Neotropical Biology
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
The expontaneos submmition of the manuscript automaticaly implies in the cession of all patrimonial rights for the Journal of Neotropical Bilogy (RBN) after publication. The autor allow the right of first publication of the article to the RBN, under Creative Commons Attribution 4.0 (CC BY-NC 4.0) Licence.
There are garanties for the authors to the authorial and moral rights, for each one of the articles published by RBN, with permissions:
1. The use of article and contents for the education and researches.
2. The use of the article and their contents, linking to the Article on the web site of the RBN, allowing the divulgation on:
- institutional closed web (intranet).
- open access repositories.
3. Preparation and divulgation of the other publication derived from the article and its content, if there is citation of the original publication by RBN.
4. Make printed copies in small quatinties for personal use.