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Evidence-Based Complementary and Alternative Medicine
Volume 2016, Article ID 1574971, 9 pages
http://dx.doi.org/10.1155/2016/1574971
Research Article

Bothrops jararaca and Bothrops erythromelas Snake Venoms Promote Cell Cycle Arrest and Induce Apoptosis via the Mitochondrial Depolarization of Cervical Cancer Cells

1Programa de Pós Graduação em Ciências Farmacêuticas, Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil
2Programa de Pós Graduação em Ciências da Saúde, Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil
3Laboratório de Imunoquímica, Instituto Butantan, São Paulo, SP, Brazil
4Departamento de Tocoginecologia, Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil
5Maternidade Escola Januário Cicco (MEJC), Natal, RN, Brazil

Received 5 September 2016; Accepted 6 November 2016

Academic Editor: Ki-Wan Oh

Copyright © 2016 Emanuelly Bernardes-Oliveira et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. Chakrabarty, A. Ganguli, A. Das, D. Nag, and G. Chakrabarti, “Epigallocatechin-3-gallate shows anti-proliferative activity in HeLa cells targeting tubulin-microtubule equilibrium,” Chemico-Biological Interactions, vol. 242, pp. 380–389, 2015. View at Publisher · View at Google Scholar · View at Scopus
  2. H. L. Lee, M. H. Park, J. E. Hong et al., “Inhibitory effect of snake venom toxin on NF-κB activity prevents human cervical cancer cell growth via increase of death receptor 3 and 5 expression,” Archives of Toxicology, vol. 90, no. 2, pp. 463–477, 2016. View at Publisher · View at Google Scholar · View at Scopus
  3. A. A. Alshatwi, V. S. Periasamy, J. Athinarayanan, and R. Elango, “Synergistic anticancer activity of dietary tea polyphenols and bleomycin hydrochloride in human cervical cancer cell: caspase-dependent and independent apoptotic pathways,” Chemico-Biological Interactions, vol. 247, pp. 1–10, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. Y. He, J. Lin, Y. Ding et al., “A systematic study on dysregulated microRNAs in cervical cancer development,” International Journal of Cancer, vol. 138, no. 6, pp. 1312–1327, 2016. View at Publisher · View at Google Scholar · View at Scopus
  5. INCA, National Cancer Institute. Estimates 2016: Cancer incidence in Brazil. Rio de Janeiro, 2015.
  6. J. C. Roa, P. Garcia, J. Gomez et al., “HPV genotyping from invasive cervical cancer in Chile,” International Journal of Gynecology and Obstetrics, vol. 105, no. 2, pp. 150–153, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. A. S. Choudhari, S. A. Suryavanshi, and R. Kaul-Ghanekar, “The aqueous extract of ficus religiosa induces cell cycle arrest in human cervical cancer cell lines SiHa (HPV-16 Positive) and apoptosis in HeLa (HPV-18 Positive),” PLoS ONE, vol. 8, no. 7, article e70127, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. S. C. Stone, R. A. M. Rossetti, A. M. Lima, and A. P. Lepique, “HPV associated tumor cells control tumor microenvironment and leukocytosis in experimental models,” Immunity, Inflammation and Disease, vol. 2, no. 2, pp. 63–75, 2014. View at Publisher · View at Google Scholar
  9. Y. Li, S. Xiao, L. Dan et al., “P16INK4A required for cisplatin resistance in cervical carcinoma SiHa cells,” Oncology Letters, vol. 9, no. 3, pp. 1104–1108, 2015. View at Google Scholar
  10. J. B. Vermorken, F. Peyrade, J. Krauss et al., “Cisplatin, 5-fluorouracil, and cetuximab (PFE) with or without cilengitide in recurrent/metastatic squamous cell carcinoma of the head and neck: results of the randomized phase I/II ADVANTAGE trial (phase II part),” Annals of Oncology, vol. 25, no. 3, Article ID mdu003, pp. 682–688, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. G.-L. Fan, Y. Yao, L. Yao, and Y. Li, “PDCD5 transfection increases cisplatin sensitivity and decreases invasion in hepatic cancer cells,” Oncology Letters, vol. 9, no. 1, pp. 411–417, 2015. View at Publisher · View at Google Scholar · View at Scopus
  12. G. Hernandez-Flores, P. C. Ortiz-Lazareno, J. M. Lerma-Diaz et al., “Pentoxifylline sensitizes human cervical tumor cells to cisplatin-induced apoptosis by suppressing NF-kappa B and decreased cell senescence,” BMC Cancer, vol. 11, article 483, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Singh, K. Bhui, R. Singh, and Y. Shukla, “Tea polyphenols enhance cisplatin chemosensitivity in cervical cancer cells via induction of apoptosis,” Life Sciences, vol. 93, no. 1, pp. 7–16, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. C.-C. Liu, H. Yang, L.-L. Zhang, Q. Zhang, B. Chen, and Y. Wang, “Biotoxins for cancer therapy,” Asian Pacific Journal of Cancer Prevention, vol. 15, no. 12, pp. 4753–4758, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. G. Z. Justo, A. C. S. Souza, A. Fátima et al., “The medicinal value of biodiversity: new hits to fight cancer,” in Biological Diversity and Sustainable Resources Use, O. Grillo and G. Venora, Eds., InTech, Rijeka, Croatia, 1st edition, 2011. View at Google Scholar
  16. C. S. Almeida, V. Andrade-Oliveira, N. O. S. Câmara, J. F. Jacysyn, and E. L. Faquim-Mauro, “Crotoxin from Crotalus durissus terrificus is able to down-modulate the acute intestinal inflammation in mice,” PLoS ONE, vol. 10, no. 4, Article ID e0121427, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. P. V. Dubovskii and Y. N. Utkin, “Cobra cytotoxins: structural organization and antibacterial activity,” Acta Naturae, vol. 6, no. 3, pp. 11–18, 2014. View at Google Scholar · View at Scopus
  18. L. F. D. Passero, T. Y. Tomokane, C. E. P. Corbett, M. D. Laurenti, and M. H. Toyama, “Comparative studies of the anti-leishmanial activity of three Crotalus durissus ssp. venoms,” Parasitology Research, vol. 101, no. 5, pp. 1365–1371, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Díaz-García, L. Morier-Díaz, Y. Frión-Herrera et al., “In vitro anticancer effect of venom from Cuban scorpion Rhopalurus junceus against a panel of human cancer cell lines,” Journal of Venom Research, vol. 4, pp. 5–12, 2013. View at Google Scholar
  20. D. Jain and S. Kumar, “Snake venom: a potent anticancer agent,” Asian Pacific Journal of Cancer Prevention, vol. 13, no. 10, pp. 4855–4860, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. D. A. Maria, M. G. L. da Silva, M. C. Correia, and I. R. G. Ruiz, “Antiproliferative effect of the jararhagin toxin on B16F10 murine melanoma,” BMC Complementary and Alternative Medicine, vol. 14, no. 1, article 446, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Ebrahim, F. H. Shirazi, H. Vatanpour, A. Zare, F. Kobarfard, and H. Rabiei, “Anticancer activity of cobra venom polypeptide, Cytotoxin-II, against human breast adenocarcinoma cell line (MCF-7) via the induction of apoptosis,” Journal of Breast Cancer, vol. 17, no. 4, pp. 314–322, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. M. H. Park, M. Jo, D. Won et al., “Snake venom toxin from Vipera lebetina turanica induces apoptosis of colon cancer cells via upregulation of ROS- and JNK-mediated death receptor expression,” BMC Cancer, vol. 12, article 228, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. P. S. Kollipara, D. H. Won, C. J. Hwang et al., “Enhanced anti-cancer effect of snake venom activated nk cells on lung cancer cells by inactivation of NF-κB,” Biomolecules & Therapeutics, vol. 22, no. 2, pp. 106–113, 2014. View at Publisher · View at Google Scholar
  25. M. H. Park, D. J. Son, D. H. Kwak et al., “Snake venom toxin inhibits cell growth through induction of apoptosis in neuroblastoma cells,” Archives of Pharmacal Research, vol. 32, no. 11, pp. 1545–1554, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. D. L. Gomes, C. B. S. Telles, M. S. S. P. Costa et al., “Methanolic extracts from brown seaweeds Dictyota cilliolata and Dictyota menstrualis induce apoptosis in human cervical adenocarcinoma HeLa cells,” Molecules, vol. 20, no. 4, pp. 6573–6591, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. C. Tavares, T. Maciel, S. Burin et al., “L-Amino acid oxidase isolated from Calloselasma rhodostomasnake venom induces cytotoxicity and apoptosis in JAK2V617F-positive cell lines,” Revista Brasileira de Hematologia e Hemoterapia, vol. 38, no. 2, pp. 128–134, 2016. View at Publisher · View at Google Scholar
  28. O. Zakraoui, C. Marcinkiewicz, Z. Aloui et al., “Lebein, a snake venom disintegrin, suppresses human colon cancer cells proliferation and tumor-induced angiogenesis through cell cycle arrest, apoptosis induction and inhibition of VEGF expression,” Molecular Carcinogenesis, 2016. View at Publisher · View at Google Scholar · View at Scopus
  29. A. A. D. Moura, A. M. Kayano, G. A. Oliveira et al., “Purification and biochemical characterization of three myotoxins from Bothrops mattogrossensis snake venom with toxicity against Leishmania and tumor cells,” BioMed Research International, vol. 2014, Article ID 195356, 13 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. M. A. Aranda-Souza, F. A. Rossato, R. A. P. Costa et al., “A lectin from Bothrops leucurus snake venom raises cytosolic calcium levels and promotes B16-F10 melanoma necrotic cell death via mitochondrial permeability transition,” Toxicon, vol. 82, pp. 97–103, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. E. S. Nunes, M. A. A. Souza, A. F. M. Vaz et al., “Cytotoxic effect and apoptosis induction by Bothrops leucurus venom lectin on tumor cell lines,” Toxicon, vol. 59, no. 7-8, pp. 667–671, 2012. View at Publisher · View at Google Scholar
  32. C. Prinholato da Silva, T. R. Costa, R. M. A. Paiva et al., “Antitumor potential of the myotoxin BthTX-I from Bothrops jararacussu snake venom: Evaluation of cell cycle alterations and death mechanisms induced in tumor cell lines,” Journal of Venomous Animals and Toxins Including Tropical Diseases, vol. 21, article 44, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Nolte, D. de Castro Damasio, A. C. Baréa et al., “BJcuL, a lectin purified from Bothrops jararacussu venom, induces apoptosis in human gastric carcinoma cells accompanied by inhibition of cell adhesion and actin cytoskeleton disassembly,” Toxicon, vol. 59, no. 1, pp. 81–85, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. L. Zhang and L.-J. Wei, “ACTX-8, a cytotoxic l-amino acid oxidase isolated from Agkistrodon acutus snake venom, induces apoptosis in Hela cervical cancer cells,” Life Sciences, vol. 80, no. 13, pp. 1189–1197, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. Ž. Gudlevičienė, A. Stumbrytė, G. Juknė, V. Simanavičienė, and A. Žvirblienė, “Distribution of human papillomavirus type 16 variants in Lithuanian women with cervical cancer,” Medicina, vol. 51, no. 6, pp. 328–335, 2015. View at Publisher · View at Google Scholar
  36. R. K. Rajeshkumar, R. Vennila, S. Karthikeyan et al., “Antiproliferative activity of marine stingray Dasyatis sephen venom on human cervical carcinoma cell line,” The Journal of Venomous Animals and Toxins Including Tropical Diseases, vol. 21, article 41, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. D. J. Son, M. H. Park, S. J. Chae et al., “Inhibitory effect of snake venom toxin from Vipera lebetina turanica on hormone-refractory human prostate cancer cell growth: induction of apoptosis through inactivation of nuclear factor κB,” Molecular Cancer Therapeutics, vol. 6, no. 2, pp. 675–683, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. L. M. Gabriel, E. F. Sanchez, S. G. Silva, and R. G. dos Santos, “Tumor cytotoxicity of leucurolysin-B, a P-III snake venom metalloproteinase from Bothrops leucurus,” Journal of Venomous Animals and Toxins Including Tropical Diseases, vol. 18, no. 1, pp. 24–33, 2012. View at Google Scholar · View at Scopus