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Physiology and Molecular Biology of Plants

, Volume 24, Issue 6, pp 1185–1201 | Cite as

Cytotoxic effect of Semialarium mexicanum (Miers) Mennega root bark extracts and fractions against breast cancer cells

  • Juan Maldonado-Cubas
  • Eduardo San Martin-Martínez
  • Cinthya Nathaly Quiroz-Reyes
  • Rocio Guadalupe Casañas-PimentelEmail author
Research Article
  • 64 Downloads

Abstract

The root bark of Semialarium mexicanum (Miers) Mennega (cancerina) is traditionally used in Mexico to treat cancer. However, there are no studies supporting its use. We evaluated whether S. mexicanum root bark induces cytotoxicity in breast cancer cells to determine if it has potential applications in the treatment of this disease. Extracts of S. mexicanum root bark in petroleum ether, ethanol, and water were obtained by ultrasound-assisted extraction. MTT and WST-1 assays were used to evaluate the cytotoxicity of the extracts toward breast cancer cells (MDA-MB-231 and MCF7), non-tumorigenic breast-derived cells (MCF 10A), and peripheral blood mononuclear cells (PBMCs). For the extract with greatest cytotoxicity, induction of apoptosis and oxidative stress were determined using flow cytometry. The extract was fractionated, and the cytotoxicity of its fractions was evaluated with the four cell types. The fractions were also analyzed by HPLC. Only the petroleum ether extract was cytotoxic for all cell types (MDA-MB-231 > MCF 10A/MCF7 > PBMCs). Cell death occurred by apoptosis, which could be associated with the induction of oxidative stress. Two fractions that were highly cytotoxic for breast cancer cells were obtained from this extract (IC50 ≤ 4.15 µg/mL for the most active fraction at 72 h). The MCF 10A cells were less affected, while PBMCs were not affected after 72 h of treatment. Pristimerin was identified in both fractions and may be partially responsible for the cytotoxic effect. These results suggest that S. mexicanum root bark has a potential application in breast cancer treatment.

Keywords

Cancer Cytotoxicity Cancerina Celestraceae Pristimerin Hippocratea 

Notes

Acknowledgements

This work was supported by the Instituto Politécnico Nacional and the National Council of Science and Technology, Mexico (CONACYT, Proyecto de Cátedras No. 1728).

Author Contributions Statement

ESMM, JM-C, CNQ-R and RGC-P conceived, designed and performed the experiments. JM-C, CNQ-R and RGC-P analyzed the data. ESMM contributed with reagents, materials and analysis tools. JM-C, RGC-P, CNQ-R and ESMM wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Alexandre J, Hu Y, Lu W, Pelicano H, Huang P (2007) Novel action of paclitaxel against cancer cells: bystander effect mediated by reactive oxygen species. Cancer Res 67:3512–3517.  https://doi.org/10.1158/0008-5472.can-06-3914 CrossRefPubMedGoogle Scholar
  2. Alonso-Castro AJ, Villarreal ML, Salazar-Olivo LA, Gomez-Sanchez M, Dominguez F, Garcia-Carranca A (2011) Mexican medicinal plants used for cancer treatment: pharmacological, phytochemical and ethnobotanical studies. J Ethnopharmacol 133:945–972.  https://doi.org/10.1016/j.jep.2010.11.055 CrossRefPubMedGoogle Scholar
  3. Araujo Leon J-A, Ruiz Ciau D-V, Coral Martinez T-I, Cantillo Ciau Z-O (2015) Comparative fingerprint analyses of extracts from the root bark of wild Hippocratea excelsa and “Cancerina” by high-performance liquid chromatography. J Sep Sci 38:3870–3875.  https://doi.org/10.1002/jssc.201401480 CrossRefPubMedGoogle Scholar
  4. Arjunan V, Subramanian S, Mohan S (2001) Fourier transform infrared and Raman spectral analysis of trans-1,4-polyisoprene. Spectrochim Acta Part A Mol Biomol Spectrosc 57:2547–2554.  https://doi.org/10.1016/S1386-1425(01)00426-7 CrossRefGoogle Scholar
  5. Badisa RB, Darling-Reed SF, Joseph P, Cooperwood JS, Latinwo LM, Goodman CB (2009) Selective cytotoxic activities of two novel synthetic drugs on human breast carcinoma MCF-7 cells. Anticancer Res 29:2993–2996PubMedPubMedCentralGoogle Scholar
  6. Bashir AY, Hozeifa MH, Lu-Yong Z, Zhen-Zhou J (2017) Anticancer potential and molecular targets of pristimerin: a mini- review. Curr Cancer Drug Targets 17:100–108.  https://doi.org/10.2174/1568009616666160112105824 CrossRefGoogle Scholar
  7. Cáceres-Castillo D, Mena-Rejón GJ, Cedillo-Rivera R, Quijano L (2008) 21β-Hydroxy-oleanane-type triterpenes from Hippocratea excelsa. Phytochemistry 69:1057–1064.  https://doi.org/10.1016/j.phytochem.2007.10.016 CrossRefPubMedGoogle Scholar
  8. Chen D, Shao H, Yao W, Huang B (2013) Fourier transform infrared spectral analysis of polyisoprene of a different microstructure. Int J Polym Sci 2013:5.  https://doi.org/10.1155/2013/937284 CrossRefGoogle Scholar
  9. Cos P, Vlietinck AJ, Berghe DV, Maes L (2006) Anti-infective potential of natural products: How to develop a stronger in vitro ‘proof-of-concept’. J Ethnopharmacol 106:290–302.  https://doi.org/10.1016/j.jep.2006.04.003 CrossRefPubMedGoogle Scholar
  10. Dholwani KK, Saluja AK, Gupta AR, Shah DR (2008) A review on plant-derived natural products and their analogs with anti-tumor activity. Indian J Pharmacol 40:49–58.  https://doi.org/10.4103/0253-7613.41038 CrossRefPubMedPubMedCentralGoogle Scholar
  11. dos Santos KAM, Suarez PAZ, Rubim JC (2005) Photo-degradation of synthetic and natural polyisoprenes at specific UV radiations. Polym Degrad Stab 90:34–43.  https://doi.org/10.1016/j.polymdegradstab.2005.01.038 CrossRefGoogle Scholar
  12. Fitzpatrick FA, Wheeler R (2003) The immunopharmacology of paclitaxel (Taxol®), docetaxel (Taxotere®), and related agents. Int Immunopharmacol 3:1699–1714.  https://doi.org/10.1016/j.intimp.2003.08.007 CrossRefPubMedGoogle Scholar
  13. Global Burden of Disease Cancer C (2017) Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 32 cancer groups, 1990 to 2015: a systematic analysis for the global burden of disease study. JAMA Oncol 3:524–548.  https://doi.org/10.1001/jamaoncol.2016.5688 CrossRefGoogle Scholar
  14. Gomes JP, Cardoso CRP, Varanda EA, Molina JM, Fernandez MF, Olea N, Carlos IZ, Vilegas W (2011) Antitumoral, mutagenic and (anti)estrogenic activities of tingenone and pristimerin. Revista Brasileira de Farmacognosia 21:963–971.  https://doi.org/10.1590/S0102-695X2011005000153 CrossRefGoogle Scholar
  15. Kaneno R, Shurin GV, Kaneno FM, Naiditch H, Luo J, Shurin MR (2011) Chemotherapeutic agents in low noncytotoxic concentrations increase immunogenicity of human colon cancer cells. Cell Oncol 34:97–106.  https://doi.org/10.1007/s13402-010-0005-5 CrossRefGoogle Scholar
  16. Mena-Rejón GJ, Pérez-Espadas AR, Moo-Puc RE, Cedillo-Rivera R, Bazzocchi IL, Jiménez-Diaz IA, Quijano L (2007) Antigiardial activity of triterpenoids from root bark of Hippocratea excelsa. J Nat Prod 70:863–865.  https://doi.org/10.1021/np060559y CrossRefPubMedGoogle Scholar
  17. Mullen PJ, Yu R, Longo J, Archer MC, Penn LZ (2016) The interplay between cell signalling and the mevalonate pathway in cancer. Nat Rev Cancer 16:718.  https://doi.org/10.1038/nrc.2016.76 CrossRefPubMedGoogle Scholar
  18. Ozben T (2007) Oxidative stress and apoptosis: impact on cancer therapy. J Pharm Sci 96:2181–2196.  https://doi.org/10.1002/jps.20874 CrossRefPubMedGoogle Scholar
  19. Popoca J, Al Aguilar, Alonso D, Villarreal ML (1998) Cytotoxic activity of selected plants used as antitumorals in Mexican traditional medicine. J Ethnopharmacol 59:173–177.  https://doi.org/10.1016/S0378-8741(97)00110-4 CrossRefPubMedGoogle Scholar
  20. Reyes-Chilpa R, Jiménez-Estrada M, Cristóbal-Telésforo E, Torres-Colín L, Villavicencio MA, Pérez-Escandón BE, Mercado-González R (2003) Natural insecticides from Hippocratea excelsa and Hippocratea celastroides. Econ Bot 57:54–64.  https://doi.org/10.1663/0013-0001(2003)057[0054:NIFHEA]2.0.CO;2 CrossRefGoogle Scholar
  21. Schmid I, Krall WJ, Uittenbogaart CH, Braun J, Giorgi JV (1992) Dead cell discrimination with 7-amino-actinomcin D in combination with dual color immunofluorescence in single laser flow cytometry. Cytometry 13:204–208.  https://doi.org/10.1002/cyto.990130216 CrossRefPubMedGoogle Scholar
  22. Seelinger M, Popescu R, Giessrigl B, Jarukamjorn K, Unger C, Wallnöfer B, Fritzer-Szekeres M, Szekeres T, Diaz R, Jäger W, Frisch R, Kopp B, Krupitza G (2012) Methanol extract of the ethnopharmaceutical remedy Smilax spinosa exhibits anti-neoplastic activity. Int J Oncol 41:1164–1172.  https://doi.org/10.3892/ijo.2012.1538 CrossRefPubMedGoogle Scholar
  23. Singh M, McKenzie K, Xiaoling M (2017) Effect of dimethyl sulfoxide on in vitro proliferation of skin fibroblast cells. J Biotech Res 8:78–82Google Scholar
  24. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2015) Global cancer statistics, 2012. CA Cancer J Clin 65:87–108.  https://doi.org/10.3322/caac.21262 CrossRefPubMedGoogle Scholar
  25. Varbiro G, Veres B, Gallyas F, Sumegi B (2001) Direct effect of Taxol on free radical formation and mitochondrial permeability transition. Free Radic Biol Med 31:548–558.  https://doi.org/10.1016/S0891-5849(01)00616-5 CrossRefPubMedGoogle Scholar
  26. Wang TH, Wang HS, Soong YK (2000) Paclitaxel-induced cell death. Cancer 88:2619–2628. doi: 10.1002/1097-0142(20000601)88:11<2619:aid-cncr26>3.0.co;2-jCrossRefPubMedGoogle Scholar
  27. Wen J, Tong Y, Zu Y (2015) Low concentration DMSO stimulates cell growth and in vitro transformation of human multiple myeloma cells. Br J Med Med Res 5:65–74.  https://doi.org/10.9734/BJMMR/2015/5276 CrossRefGoogle Scholar
  28. Yadav N, Kumar S, Marlowe T, Chaudhary AK, Kumar R, Wang J, O’Malley J, Boland PM, Jayanthi S, Kumar TKS, Yadava N, Chandra D (2015) Oxidative phosphorylation-dependent regulation of cancer cell apoptosis in response to anticancer agents. Cell Death Dis 6:e1969.  https://doi.org/10.1038/cddis.2015.305 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Zhang L, Yu Y, Joubert C, Bruder G, Liu Y, Chang CC, Simon M, Walker S, Rafailovich M (2016) Differentiation of dental pulp stem cells on gutta-percha scaffolds. Polymers 8:193.  https://doi.org/10.3390/polym8050193 CrossRefGoogle Scholar

Copyright information

© Prof. H.S. Srivastava Foundation for Science and Society 2018

Authors and Affiliations

  1. 1.Instituto Politécnico Nacional, Centro de Investigación en Ciencia Aplicada y Tecnología AvanzadaUnidad LegariaCiudad de MéxicoMéxico
  2. 2.CONACYT-Instituto Politécnico Nacional, Centro de Investigación en Ciencia Aplicada y Tecnología AvanzadaUnidad LegariaCiudad de MéxicoMéxico

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