Assessment of the antioxidant, cytotoxic, and genotoxic potential of the Annona muricata leaves and their influence on genomic stability

References

• Adeyemi, D. O. , O. A. Komolafe , O. S. Adewole , E. M. Obuotor , and T. K. Adenowo . 2009. Anti hyperglycemic activities of Annona muricata (Linn). African Journal of Traditional, Complementary and Alternative Medicines 6:62–69.
   Google Scholar
• Agil, F. , I. Ahmad , and Z. Mehmood . 2006. Antioxidant and free radical scavenging properties of twelve traditionally used Indian medicinal plants. Turkish Journal of Biology 30:177–183.
   Google Scholar
• Alali, F. Q. , L. Xiao-Xi , and J. L. McLaughlin . 1999. Annonaceous acetogenins: Recent progress. Journal of Natural Products 62:504–540. doi:10.1021/np980406d.
   PubMed Web of Science ®Google Scholar
• Anderson, D. , T. W. Yu , B. J. Phillips , and P. Schmezer . 1994. The effect of various antioxidants and other modifying agents on oxygen-radical-generated DNA damage in human lymphocytes in the Comet Assay. Mutation Research 307:261–271. doi:10.1016/0027-5107(94)90300-X.
   PubMed Web of Science ®Google Scholar
• Baskar, R. , V. Rajeswari , and T. S. Kumar . 2007. In vitro antioxidant studies in leaves of Annona species. Indian Journal of Experimental Biology 45:480–485.
   PubMed Web of Science ®Google Scholar
• Bento, E. B. , E. F. F. Matias , F. E. Brito, Jr , D. R. Oliveira , H. D. M. Coutinho , J. G. M. Costa , M. R. Kerntopf , and I. R. A. Menezes . 2013. Association between food and drugs: Antimicrobial and synergistic activity of Annona muricata L. International Journal of Food Properties 16:738–744. doi:10.1080/10942912.2011.565905.
   Web of Science ®Google Scholar
• Bories, C. , P. Loiseau , D. Cortes , S. H. Myint , R. Hocquemiller , P. Gayral , A. Cavé , and A. Laurens . 1991. Antiparasitic activity of Annona muricata and Annona cherimola seeds. Planta Medica 57:434–436. doi:10.1055/s-2006-960143.
   PubMed Web of Science ®Google Scholar
• Brown, J. E. , H. Khodr , R. C. Hider , and C. A. Rice-Evans . 1998. Structural dependence of flavonoid interactions with Cu2+ ions: Implications for their antioxidant properties. Journal of Biochemistry 330:1173–1178. doi:10.1042/bj3301173.
   Google Scholar
• Carmona, E. R. , M. Reyes-Díaz , J. Parodi , and C. Inostroza-Blancheteau . 2017. Antimutagenic evaluation of traditional medicinal plants from South America Peumus boldus and Cryptocarya alba using Drosophila melanogaster . Journal of Toxicology and Environmental Health, Part A 80:208–217. doi:10.1080/15287394.2017.1279574.
   PubMed Web of Science ®Google Scholar
• Chatrou, L. W. , M. D. Pirie , R. H. J. Erkens , T. L. P. Couvreur , K. M. Neubig , R. J. Abbott , J. B. Mols , J. W. Maas , R. M. K. Saunders , and M. W. Chase . 2012. A new higher-level classification of the pantropical flowering plant family Annonaceae informed by molecular phylogenetics. Botanical Journal of the Linnean Society 169:5–40. doi:10.1111/j.1095-8339.2012.01235.x.
   Web of Science ®Google Scholar
• De Quadros, A. P. O. , D. E. C. Mazzeo , M. A. Marin-Morales , F. F. Perazzo , P. C. P. Rosa , and E. L. Maistro . 2017. Fruit extract of the medicinal plant Crataegus oxyacantha exerts genotoxic and mutagenic effects in cultured cells. Journal ofToxicology and Environmental Health, Part A 80:161–170. doi:10.1080/15287394.2016.1272517.
   PubMed Web of Science ®Google Scholar
• De Sousa, O. V. , V. G. Del-Vechio. , J. J. R. G. Pinho , C. H. Yamamoto , and M. S. Alves . 2010. Antinociceptive and anti-inflammatory activities of the ethanol extract of Annona muricata L. leaves in animal models. International Journal of Molecular Sciences 11:2067–2078. doi:10.3390/ijms11052067.
   PubMed Web of Science ®Google Scholar
• Dreher, D. , and A. F. Junod . 1996. Role of oxygen free radicals in cancer development. European Journal of Cancer 32A:30–38. doi:10.1016/0959-8049(95)00531-5.
   PubMed Web of Science ®Google Scholar
• Eastmond, D. A. , and J. D. Tucker . 1989. Identification of aneuploidy-inducing agents using cytokinesis-blocked human lymphocytes and an antikinetochore antibody. Environmental and Molecular Mutagenesis 13:34–43. doi:10.1002/(ISSN)1098-2280.
   PubMed Web of Science ®Google Scholar
• Fenech, M. 2000. The in vitro micronucleus technique. Mutation Research 455:81–95. doi:10.1016/S0027-5107(00)00065-8.
   PubMed Web of Science ®Google Scholar
• Ferguson, L. R. , and W. A. Denny . 2007. Genotoxicity of non-covalent interactions: DNA intercalators. Mutation Research 623:14–23. doi:10.1016/j.mrfmmm.2007.03.014.
   PubMed Web of Science ®Google Scholar
• Fernandes, D. C. , L. O. Regasini , J. C. R. Vellosa , P. M. Pauletti , I. Castro-Gamboa , V. S. Bolzani , O. M. M. Oliveira , and D. H. S. Silva . 2008. Myeloperoxidase inhibitory and radical scavenging activities of flavones from Pterogyne nitens. Chem . Chemical & Pharmaceutical Bulletin 56:723–726. doi:10.1248/cpb.56.723.
   PubMed Web of Science ®Google Scholar
• Ferreira, N. H. , K. J. Andrade , L. F. Leandro , N. O. Acésio , S. A. Mendes , L. S. Cintra , A. H. Januário , and D. C. Tavares . 2016. Testing of Schefflera vinosa extract in mammalian cells in vitro and in vivo for potential toxicity, genetic damage, and role of oxidation. Journal of Toxicology and Environmental Health, Part A 79:1201–1210. doi:10.1080/15287394.2016.1229238.
   PubMed Web of Science ®Google Scholar
• Franken, N. A. P. , H. M. Rodermond , P. Stap , J. Haveman , and C. Van Bree . 2006. Clonogenic assay of cells in vitro . Natural Protocols 1:2315–2319. doi:10.1038/nprot.2006.339.
   PubMed Web of Science ®Google Scholar
• Furtado, R. A. , F. R. R. Araújo , F. A. Resende , W. R. Cunha , and D. C. Tavares . 2010. Protective effect of rosmarinic acid on V79 cells evaluated by micronucleus and comet assay. Journal of Applied Toxicology 30:254–259.
   PubMed Web of Science ®Google Scholar
• Gbeassor, M. , A. Y. Kedjagni , K. Koumaglo , C. De Souza , K. Agbo , K. Aklikokou , and K. A. Amegbo . 1990. In vitro antimalarial activity of six medicinal plants. Phytotherapy Research 4:115–117. doi:10.1002/(ISSN)1099-1573.
   Web of Science ®Google Scholar
• George, V. C. , D. R. Kumar , P. K. Suresh , and R. A. Kumar . 2015. Antioxidant, DNA protective efficacy and HPLC analysis of Annona muricata (soursop) extracts. Journal of Food Science and Technology 52:2328–2335. doi:10.1007/s13197-014-1289-7.
   PubMed Web of Science ®Google Scholar
• George, V. C. , N. D. R. Kumar , V. Rajkumar , P. K. Suresh , and R. A. Kumar . 2012. 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 13:699–704. doi:10.7314/APJCP.2012.13.2.699.
   PubMedGoogle Scholar
• Halliwell, B. , and O. I. Aruoma . 1991. DNA damage by oxygen-derived species Its mechanism and measurement in mammalian systems. FEBS Letters 281:9–19. doi:10.1016/0014-5793(91)80347-6.
   PubMed Web of Science ®Google Scholar
• Halliwell, B. , and J. M. C. Gutteridge . 1998. In Free Radicals in Biology and Medicine . Oxford: Oxford University Press.
   Google Scholar
• Hayashi, M. , J. T. MacGregor , D. G. Gatehouse , I. Adler , D. H. Blakey , S. D. Dertinger , G. Krishna , T. Morita , A. Russo , and S. Sutou . 2000. In vivo rodent micronucleus assay. II. Some aspects of protocol design including repeated treatments, integration with toxicity testing, and automated scoring. Environmental and Molecular Mutagenesis 5:234–252. doi:10.1002/(SICI)1098-2280(2000)35:3<234::AID-EM10>3.0.CO;2-L.
   Web of Science ®Google Scholar
• Jaramillo, M. C. , G. J. Arango , M. C. González , S. M. Robledo , and I. D. Velez . 2000. Cytotoxicity and antileishmanial activity of Annona muricata pericarp. Fitoterapia 71:183–186. doi:10.1016/S0367-326X(99)00138-0.
   PubMed Web of Science ®Google Scholar
• Kanazawa, L. K. , D. D. Vecchia , E. M. Wendler , P. A. Hocayen , P. S. Berão, Jr , M. L. Mélo , F. A. R. Lívero , C. R. Corso , M. C. Stipp , A. Acco , and R. Andreatini . 2017. Effects of acute and chronic quercetin administration on methylphenidate-induced hyper-locomotion and oxidative stress. Life Sciences 171:1–8. doi:10.1016/j.lfs.2017.01.007.
   PubMed Web of Science ®Google Scholar
• Kirsch-Volders, M. , T. Sofuni , M. Aardema , S. Albertini , D. Eastmond , M. Fenech , M. Ishidate , S. Kirchner , E. Lorge , T. Morita , H. Norppa , J. Surrallés , A. Vanhauwaert , and A. Wakata . 2004. Corrigendum to “Report from the in vitro micronucleus assay working group” [Mutat. Res. 540 (2003) 153–163]. Mutation Research 564:97–100. doi:10.1016/j.mrgentox.2004.07.002.
   Web of Science ®Google Scholar
• Kirsch-Volders, M. , T. Sofuni , M. Aardema , D. Eastmond , S. Albertini , D. Eastmond , M. Fenech , M. Ishidate, Jr. , S. Kirchner , E. Lorge , T. Morita , H. Norppa , J. Surrallés , A. Vanhauwaert , and A. Wakata 2003. Report from the in vitro micronucleus assay working group. Mutat. Res . 540: 153–163. 10.1016/j.mrgentox.2003.07.005
   Google Scholar
• Liu, H. , R. Lightfoot , and J. L. Stevens . 1996. Activation of heat shock factor by alkylating agents is triggered by glutathione depletion and oxidant of protein thiols. Journal of Biological Chemistry 271:4805–4812.
   PubMed Web of Science ®Google Scholar
• Luna, J. S. , J. M. De Carvalho , M. R. De Lima , L. W. Bieber , E. S. Bento , X. Franck , and A. E. Sant’ana . 2006. Acetogenins in Annona muricata L. (Annonaceae) leaves are potent molluscicides. Natural Product Research 20:253–257. doi:10.1080/14786410500161445.
   PubMed Web of Science ®Google Scholar
• Maver, T. , U. Maver , K. S. Kleinschek , D. M. Smrke , and S. Kreft . 2015. A review of herbal medicines in wound healing. International Journal of Dermatology 54:740–751. doi:10.1111/ijd.2015.54.issue-7.
   PubMed Web of Science ®Google Scholar
• McLaughlin, J. L. J. 2008. Paw paw and cancer: Annonaceous acetogenins from discovery to commercial products ⊥. Journal of Natural Products 71:1311–1321. doi:10.1021/np800191t.
   PubMed Web of Science ®Google Scholar
• Mikhed, Y. , A. Görlach , U. G. Knaus , and A. Daiber . 2015. Redox regulation of genome stability by effects on gene expression, epigenetic pathways and DNA damage/repair. Redox Biology 5:275–289. doi:10.1016/j.redox.2015.05.008.
   PubMed Web of Science ®Google Scholar
• Mirzayans, R. , M. Liuzzi , and M. G. Patersnon . 1988. Methyl methanesulfonate-induced DNA damage and its repair in culture human fibroblasts: Normal rates of induction and removal of alkali-labile sites in xeroderma pigmentosum (group A) cells. Carcinogenesis 12:2257–2263. doi:10.1093/carcin/9.12.2257.
   Web of Science ®Google Scholar
• Moghadamtousi, S. Z. , M. Fadaeinasab , S. Nikzad , G. Mohan , H. M. Ali , and H. A. Kadir . 2015. Annona muricata (Annonaceae): A review of its traditional uses, isolated acetogenins and biological activities. International Journal of Molecular Sciences 16:15625–15658. doi:10.3390/ijms160715625.
   PubMed Web of Science ®Google Scholar
• Moghadamtousi, S. Z. , H. Karimian , E. Rouhollahi , M. Paydar , M. Fadaeinasab , and H. A. Kadir . 2014. Annona muricata leaves induce G1 cell cycle arrest and apoptosis through mitochondria-mediated pathway in human HCT-116 and HT-29 colon cancer cells. Journal of Ethnopharmacology 156:277–289. doi:10.1016/j.jep.2014.08.011.
   PubMed Web of Science ®Google Scholar
• OECD . 2016. Test No. 474: Mammalian Erythrocyte Micronucleus Test . Paris: OECD Publishing.
   Google Scholar
• Oliveira, P. F. , R. A. Furtado , N. O. Acésio , L. F. Leandro , G. Montanheiro , F. C. Pádua , M. B. Corrêa , C. G. Braguini , P. M. Pauletti , and D. C. Tavares . 2012. In vivo protective activity of Styrax camporum hydroalcoholic extract against genotoxicity induced by doxorubicin and methyl methanesulfonate in the micronucleus and comet assays. Planta Medica 78:1899–1905. doi:10.1055/s-00000058.
   PubMed Web of Science ®Google Scholar
• Owolabi, M. S. , A. L. Ogundajo , N. S. Dosoky , and W. N. Setzer . 2013. The cytotoxic activity of Annona muricata leaf oil from Badagary, Nigeria. American Journal of Essential Oils Natural Products 1:1–3.
   Google Scholar
• Ozbek, N. , E. B. Bali , and C. Karasu . 2015. Quercetin and hydroxytyrosol attenuates xanthine/xanthine oxidase-induced toxicity in H9c2 cardiomyocytes by regulation of oxidative stress and stress-sensitive signaling pathways. General Physiology and Biophysics 34:407–414.
   PubMed Web of Science ®Google Scholar
• Padma, P. , J. P. N. Chansauria , R. L. Khosa , and A. K. Ray . 2001. Effect of Annona muricata and Polyalthia cerasoides on brain neurotransmitters and enzyme monoamine oxidase following cold immobilization stress. Journal of Natural Remedies 1:144–146.
   Google Scholar
• Padma, P. , N. P. Pramod , S. P. Thyagarajan , and R. L. Khosa . 1998. Effect of the extract of Annona muricata and Petunia nyctaginiflora on Herpes simplex virus. Journal of Ethnopharmacology 61:81–83. doi:10.1016/S0378-8741(98)00013-0.
   PubMed Web of Science ®Google Scholar
• Sousa, C. M. , H. Rocha E Silva , G. M. Vieira-Jr , M. C. C. Ayres , C. L. S. Costa , D. S. Araújo , L. C. D. Cavalcante , E. D. S. Barros , P. B. Araújo , M. S. Brandão , and M. H. Chaves . 2007. Total phenolics and antioxidant activity of five medicinal plants. Química Nova 30:351–355. doi:10.1590/S0100-40422007000200021.
   Web of Science ®Google Scholar
• Tavares, D. C. , C. C. Munari , M. G. Araújo , M. C. Beltrame , M. A. Furtado , C. C. Gonçalves , R. F. Tiossi , J. K. Bastos , W. R. Cunha , and R. C. Veneziani . 2011. Antimutagenic potential of Solanum lycocarpum against induction of chromosomal aberrations in V79 cells and micronuclei in mice by doxorubicin. Planta Medica 77:1489–1494. doi:10.1055/s-0030-1270886.
   PubMed Web of Science ®Google Scholar
• Teixeira, M. P. , L. Cruz , J. L. Franco , R. B. Vieira , and V. M. Stefenon . 2016. Ethnobotany and antioxidant evaluation of commercialized medicinal plants from the Brazilian Pampa. Acta Botanic Bras 30:47–59. doi:10.1590/0102-33062015abb0150.
   Web of Science ®Google Scholar
• Trindade, C. , G. V. Bortolini , B. S. Costa , J. C. Anghinoni , T. N. Guecheva , X. Arias , M. V. Césio , H. Heinzen , D. J. Moura , J. Saffi , M. Salvador , and J. A. Henriques . 2016. Antimutagenic and antioxidant properties of the aqueous extracts of organic and conventional grapevine Vitis labrusca cv. Isabella leaves in V79 cells. Journal of Toxicology and Environmental Health, Part A 79:825–836. doi:10.1080/15287394.2016.1190675.
   PubMed Web of Science ®Google Scholar
• Tundis, R. , J. Xiao , and M. R. Loizzo . 2017. Annona species (Annonaceae): A rich source of potential antitumor agents? Annals of the New York Academy of Sciences . 1–7. doi:10.1111/nyas.13339. http://onlinelibrary-wiley.ez249.periodicos.capes.gov.br/doi/10.1111/nyas.13339/pdf
   Web of Science ®Google Scholar
• Ursini, F. , M. Maiorino , P. Morazzoni , A. Roveri , and G. Pifferi . 1994. A novel antioxidant flavonoid (IdB 1031) affecting molecular mechanisms of cellular activation. Free Radical Biology and Medicine 16:547–553. doi:10.1016/0891-5849(94)90054-X.
   PubMed Web of Science ®Google Scholar
• Van Der Walter, B. , J. P. Zoeteweij , and J. F. Nagelkerke . 1996. Alkylation-induced oxidative cell injury of renal proximal tubular cells: Involvement of glutathione redox-cycle inhibition. Archives of Biochemistry and Biophysics 327:71–80. doi:10.1006/abbi.1996.0094.
   PubMed Web of Science ®Google Scholar
• Waters, M. D. , A. L. Brady , H. F. Stack , and H. E. Brockman . 1990. Antimutagenicity profiles for some model compounds. Mutation Research 238:57–85. doi:10.1016/0165-1110(90)90039-E.
   PubMed Web of Science ®Google Scholar
• Yuan, S. S. , H. L. Chang , H. W. Chen , Y. T. Yeh , Y. H. Kao , K. H. Lin , Y. C. Wu , and J. H. Su . 2003. Annonacin, a mono-tetrahydrofuran acetogenin, arrests cancer cells at the G1 phase and causes cytotoxicity in a Bax- and caspase-3-related pathway. Life Sciences 72:2853–2861. doi:10.1016/S0024-3205(03)00190-5.
   PubMed Web of Science ®Google Scholar
• Zeiger, E. 2003. Illusions of safety: Antimutagens can be mutagens, and anticarcinogens can be carcinogens. Mutation Research 543:191–194. doi:10.1016/S1383-5742(02)00111-4.
   PubMed Web of Science ®Google Scholar