Evaluation of the toxicity of Caralluma europaea (C.E) extracts and their effects on apoptosis and chemoresistance in pancreatic cancer cells

References

• Abijeth, B., & Ezhilarasan, D. (2020). Syringic acid induces apoptosis in human oral squamous carcinoma cells through mitochondrial pathway. Journal of Oral and Maxillofacial Pathology, 24(1), 40–45. https://doi.org/10.4103/jomfp.JOMFP_178_19
   PubMedGoogle Scholar
• Adnan, M., Jan, S., Mussarat, S., Tariq, A., Begum, S., Afroz, A., & Shinwari, Z. K. (2014). A review on ethnobotany, phytochemistry and pharmacology of plant genus Caralluma R. Br. The Journal of Pharmacy and Pharmacology, 66(10), 1351–1368. https://doi.org/10.1111/jphp.12265
   PubMed Web of Science ®Google Scholar
• Aly, A. A., Sayed, S. M., Abdelhafez, E. S., Abdelhafez, S. M. N., Abdelzaher, W. Y., Raslan, M. A., Ahmed, A. E., Thabet, K., El-Reedy, A. A. M., Brown, A. B., & Bräse, S. (2020). New quinoline-2-one/pyrazole derivatives; design, synthesis, molecular docking, anti-apoptotic evaluation, and caspase-3 inhibition assay. Bioorganic Chemistry, 94, 103348. https://doi.org/10.1016/j.bioorg.2019.103348
   PubMed Web of Science ®Google Scholar
• Amrati, F. E, Z., Bourhia, M., Slighoua, M., Ibnemoussa, S., Bari, A., Ullah, R., Amaghnouje, A., Di Cristo, F., El Mzibri, M., Calarco, A., Benbacer, L., & Bousta, D. (2020). Phytochemical study on antioxidant and antiproliferative activities of moroccan Caralluma europaea extract and its bioactive compound classes [WWW Document]. Evidence-Based Complementary and Alternative Medicine, 2020, 8409718. https://doi.org/10.1155/2020/8409718
   PubMed Web of Science ®Google Scholar
• Amrati, F. E.-Z., Bourhia, M., Slighoua, M., Boukhira, S., Ullah, R., Ezzeldin, E., Mostafa, G., Grafov, A. E., & Bousta, D. (2021). Protective effect of chemically characterized polyphenol-rich fraction from Apteranthes europaea (Guss.) Murb. subsp. maroccana (Hook.f.) plowes on carbon tetrachloride-induced liver injury in mice. Applied Sciences, 11(2), 554. https://doi.org/10.3390/app11020554
   Google Scholar
• Amrati, F. E.-Z., Bourhia, M., Slighoua, M., Mohammad Salamatullah, A., Alzahrani, A., Ullah, R., Bari, A., & Bousta, D. (2021). Traditional medicinal knowledge of plants used for cancer treatment by communities of mountainous areas of Fez-Meknes-Morocco. Saudi Pharmaceutical Journal, 29(10), 1185–1204. https://doi.org/10.1016/j.jsps.2021.09.005
   PubMed Web of Science ®Google Scholar
• Antunes-Ricardo, M., Guardado-Félix, D., Rocha-Pizaña, M. R., Garza-Martínez, J., Acevedo-Pacheco, L., Gutiérrez-Uribe, J. A., Villela-Castrejón, J., López-Pacheco, F., & Serna-Saldívar, S. O. (2021). Opuntia ficus-indica extract and Isorhamnetin-3-O-glucosyl-rhamnoside diminish tumor growth of colon cancer cells xenografted in immune-suppressed mice through the activation of apoptosis intrinsic pathway. Plant Foods for Human Nutrition, 76(4), 434–441. https://doi.org/10.1007/s11130-021-00934-3
   PubMed Web of Science ®Google Scholar
• Antunes-Ricardo, M., Moreno-García, B. E., Gutiérrez-Uribe, J. A., Aráiz-Hernández, D., Alvarez, M. M., & Serna-Saldivar, S. O. (2014). Induction of apoptosis in colon cancer cells treated with isorhamnetin glycosides from opuntia ficus-indica pads. Plant Foods for Human Nutrition (Dordrecht, Netherlands), 69(4), 331–336. https://doi.org/10.1007/s11130-014-0438-5
   PubMed Web of Science ®Google Scholar
• Arai, M. A., Fujimatsu, T., Uchida, K., Sadhu, S. K., Ahmed, F., & Ishibashi, M. (2013). Hh signaling inhibitors from Vitex negundo; naturally occurring inhibitors of the GLI1–DNA complex. Molecular bioSystems, 9(5), 1012–1018. https://doi.org/10.1039/C3MB25567K
   PubMedGoogle Scholar
• Banerjee, K., Gupta, U., Gupta, S., Wadhwa, G., Gabrani, R., Sharma, S. K., & Jain, C. K. (2011). Molecular docking of glucosamine-6-phosphate synthase in Rhizopus oryzae. Bioinformation, 7(6), 285–290. https://doi.org/10.6026/007/97320630007285
   PubMedGoogle Scholar
• Bayraktar, S., Bayraktar, U. D., & Rocha-Lima, C. M. (2010). Recent developments in palliative chemotherapy for locally advanced and metastatic pancreas cancer. World Journal of Gastroenterology, 16(6), 673–682. https://doi.org/10.3748/wjg.v16.i6.673
   PubMed Web of Science ®Google Scholar
• Bellamakondi, P. K., Godavarthi, A., Ibrahim, M., Kulkarni, S., Naik, R. M., & Maradam, S. (2014). In vitro cytotoxicity of caralluma species by mtt and trypan blue dye exclusion. Asian Journal of Pharmaceutical and Clinical Research, 7, 17–19. https://innovareacademics.in/journals/index.php/ajpcr/article/view/836
   Google Scholar
• Boubaker, J., Bhouri, W., Ben Sghaier, M., Ghedira, K., Dijoux Franca, M. G., & Chekir-Ghedira, L. (2011). Ethyl acetate extract and its major constituent, isorhamnetin 3-O-rutinoside, from Nitraria retusa leaves, promote apoptosis of human myelogenous erythroleukaemia cells. Cell Proliferation, 44(5), 453–461. https://doi.org/10.1111/j.1365-2184.2011.00772.x
   PubMed Web of Science ®Google Scholar
• Chang, W. C., Hsieh, C. H., Hsiao, M. W., Lin, W. C., Hung, Y. C., & Ye, J. C. (2010). Caffeic acid induces apoptosis in human cervical cancer cells through the mitochondrial pathway. Taiwanese Journal of Obstetrics & Gynecology, 49(4), 419–424. https://doi.org/10.1016/S1028-4559(10)60092-7
   PubMed Web of Science ®Google Scholar
• Chen, W., Ai, Q., Mai, K., Xu, W., Liufu, Z., Zhang, W., & Cai, Y. (2011). Effects of dietary soybean saponins on feed intake, growth performance, digestibility and intestinal structure in juvenile Japanese flounder (Paralichthys olivaceus). Aquaculture, 318(1–2), 95–100. https://doi.org/10.1016/j.aquaculture.2011.04.050
   Web of Science ®Google Scholar
• Conroy, T., Desseigne, F., Ychou, M., Bouché, O., Guimbaud, R., Bécouarn, Y., Adenis, A., Raoul, J.-L., Gourgou-Bourgade, S., de la Fouchardière, C., Bennouna, J., Bachet, J.-B., Khemissa-Akouz, F., Péré-Vergé, D., Delbaldo, C., Assenat, E., Chauffert, B., Michel, P., Montoto-Grillot, C., & Ducreux, M. (2011). FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. New England Journal of Medicine, 364(19), 1817–1825. https://doi.org/10.1056/NEJMoa1011923
   PubMed Web of Science ®Google Scholar
• Dra, L. A., Aghraz, A., Boualy, B., Oubaassine, S., Barakate, M., Markouk, M., & Larhsini, M. (2019). Chemical characterization and in vitro antimicrobial activity of Caralluma europaea essential oil and its synergistic potential with conventional antibiotics. Journal of Advances in Medical and Pharmaceutical Sciences, 19(4), 1–11. https://doi.org/10.9734/jamps/2018/v19i430094
   Google Scholar
• Dra, L. A., Sellami, S., Rais, H., Aziz, F., Aghraz, A., Bekkouche, K., Markouk, M., & Larhsini, M. (2019). Antidiabetic potential of Caralluma europaea against alloxan-induced diabetes in mice. Saudi Journal of Biological Sciences, 26(6), 1171–1178. https://doi.org/10.1016/j.sjbs.2018.05.028
   PubMed Web of Science ®Google Scholar
• Edderkaoui, M., Chheda, C., Soufi, B., Zayou, F., Hu, R. W., Ramanujan, V. K., Pan, X., Boros, L. G., Tajbakhsh, J., Madhav, A., Bhowmick, N. A., Wang, Q., Lewis, M., Tuli, R., Habtezion, A., Murali, R., & Pandol, S. J. (2018). An inhibitor of GSK3B and HDACs kills pancreatic cancer cells and slows pancreatic tumor growth and metastasis in mice. Gastroenterology, 155(6), 1985–1998.e5. https://doi.org/10.1053/j.gastro.2018.08.028
   PubMed Web of Science ®Google Scholar
• Gawlik-Rzemieniewska, N., & Bednarek, I. (2016). The role of NANOG transcriptional factor in the development of malignant phenotype of cancer cells. Cancer Biology & Therapy, 17(1), 1–10. https://doi.org/10.1080/15384047.2015.1121348
   PubMed Web of Science ®Google Scholar
• Glumac, P. M., & LeBeau, A. M. (2018). The role of CD133 in cancer: A concise review. Clinical and Translational Medicine, 7(1), 18. https://doi.org/10.1186/s40169-018-0198-1
   PubMedGoogle Scholar
• Goni, O., Khan, M. F., Rahman, M., Hasan, M., Kader, F. B., Sazzad, N., Sakib, M. A., Romano, B., Haque, M., & Capasso, R. (2021). Pharmacological insights on the antidepressant, anxiolytic and aphrodisiac potentials of Aglaonema hookerianum Schott. Journal of Ethnopharmacology, 268, 113664. https://doi.org/10.1016/j.jep.2020.113664
   PubMed Web of Science ®Google Scholar
• Goodarzi, S., Tabatabaei, M. J., Mohammad Jafari, R., Shemirani, F., Tavakoli, S., Mofasseri, M., & Tofighi, Z. (2020). Cuminum cyminum fruits as source of luteolin- 7-O-glucoside, potent cytotoxic flavonoid against breast cancer cell lines. Natural Product Research, 34(11), 1602–1606. https://doi.org/10.1080/14786419.2018.1519824
   PubMed Web of Science ®Google Scholar
• Hao, K., Tian, X. D., Qin, C. F., Xie, X. H., & Yang, Y. M. (2013). Hedgehog signaling pathway regulates human pancreatic cancer cell proliferation and metastasis. Oncology Reports, 29(3), 1124–1132. https://doi.org/10.3892/or.2012.2210
   PubMed Web of Science ®Google Scholar
• Ho, C. T., Chen, Q., Shi, H., Zhang, K. Q., & Rosen, R. T. (1992). Antioxidative effect of polyphenol extract prepared from various Chinese teas. Preventive Medicine, 21(4), 520–525. https://doi.org/10.1016/0091-7435(92)90059-Q
   PubMed Web of Science ®Google Scholar
• Hossain, S., Urbi, Z., Karuniawati, H., Mohiuddin, R. B., Moh Qrimida, A., Allzrag, A. M. M., Ming, L. C., Pagano, E., & Capasso, R. (2021). Andrographis paniculata (Burm. f.) Wall. ex nees: An updated review of phytochemistry, antimicrobial pharmacology, and clinical safety and efficacy. Life (Basel), 11(4), 348. https://doi.org/10.3390/life11040348
   PubMed Web of Science ®Google Scholar
• Huang, W. W., Chiu, Y. J., Fan, M. J., Lu, H. F., Yeh, H. F., Li, K. H., Chen, P. Y., Chung, J. G., & Yang, J. S. (2010). Kaempferol induced apoptosis via endoplasmic reticulum stress and mitochondria-dependent pathway in human osteosarcoma U-2 OS cells. Molecular Nutrition & Food Research, 54(11), 1585–1595. https://doi.org/10.1002/mnfr.201000005
   PubMed Web of Science ®Google Scholar
• Issiki, Z., Moundir, C., Marnissi, F., Seddik, N., Benjelloun, N., Zaid, Y., & Oudghiri, M. (2017). Toxicological evaluation of the aqueous extract of Caralluma europaea and its immunomodulatory and inflammatory activities. Pharmacognosy Research, 9(4), 390–395. https://doi.org/10.4103/pr.pr_24_17
   PubMed Web of Science ®Google Scholar
• Janakiraman, K., Kathiresan, S., & Mariadoss, A. (2014). Influence of sinapic acid on induction of apoptosis in human laryngeal carcinoma cell line. International Journal of Modern Research and Reviews, 2, 165–170. https://www.semanticscholar.org/paper/INFLUENCE-OF-SINAPIC-ACID-ON-INDUCTION-OF-APOPTOSIS-Janakiraman-Kathiresan/06d808dc9211dc2592a97e4a79b938712ec1f44b
   Google Scholar
• Jiang, J., & Hui, C. (2008). Hedgehog signaling in development and cancer. Developmental Cell, 15(6), 801–812. https://doi.org/10.1016/j.devcel.2008.11.010
   PubMed Web of Science ®Google Scholar
• Kashaw, S. K., Agarwal, S., Mishra, M., Sau, S., & Iyer, A. K. (2019). Molecular docking analysis of caspase-3 activators as potential anticancer agents. Current Computer-Aided Drug Design, 15(1), 55–66. https://doi.org/10.2174/1573409914666181015150731
   PubMed Web of Science ®Google Scholar
• Kebbou, A., Laaradia, M. A., Oufquir, S., Aarab, A., Gabbas, Z. E., Rais, H., Zyad, A., & Chait, A. (2019). Antioxidant activity, anti-inflammatory and analgesic effects of Caralluma europaea (Eddaghmouss) in mice. OnLine Journal of Biological Sciences, 19(4), 272–285. https://doi.org/10.3844/ojbsci.2019.272.285
   Google Scholar
• Kregiel, D., Berlowska, J., Witonska, I., Antolak, H., Proestos, C., Babic, M., Babic, L., & Zhang, B. (2017). Saponin-Based, Biological-Active Surfactants from Plants. International Journal of Pharma and Bio Sciences, 4, B42–B48. https://doi.org/10.5772/68062
   Google Scholar
• Kumar, V., Chaudhary, A. K., Dong, Y., Zhong, H. A., Mondal, G., Lin, F., Kumar, V., & Mahato, R. I. (2017). Design, synthesis and biological evaluation of novel hedgehog inhibitors for treating pancreatic cancer. Scientific Reports, 7(1), 15. https://doi.org/10.1038/s41598-017-01942-7
   PubMedGoogle Scholar
• Li, Z., Zhang, Y., Chen, L., & Li, H. (2018). The dietary compound luteolin inhibits pancreatic cancer growth by targeting BCL-2. Food & Function, 9(5), 3018–3027. https://doi.org/10.1039/C8FO00033F
   PubMed Web of Science ®Google Scholar
• Moni, J. N. R., Adnan, M., Tareq, A. M., Kabir, M. I., Reza, A., Nasrin, M. S., Chowdhury, K. H., Sayem, S. A. J., Rahman, M. A., Alam, A. K., Alam, S. B., Sakib, M. A., Oh, K. K., Cho, D. H., & Capasso, R. (2021). Therapeutic potentials of Syzygium fruticosum fruit (seed) reflected into an array of pharmacological assays and prospective receptors-mediated pathways. Life, 11(2), 155. https://doi.org/10.3390/life11020155
   PubMedGoogle Scholar
• Mousavi, N., Rahimi, S., Emami, H., Kazemi, A. H., Mohammad Taghi Kashi, R., & Heidarian, R. (2021). The effect of quercetin nanosuspension on prostate cancer cell line LNCaP via hedgehog signaling pathway. Reports of Biochemistry & Molecular Biology, 10(1), 69–75. https://doi.org/10.52547/rbmb.10.1.69
   PubMed Web of Science ®Google Scholar
• National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals. (2011). Guide for the care and use of laboratory animals, 8th ed, the national academies collection: Reports funded by national institutes of health. National Academies Press (US).
   Google Scholar
• Pérez-Soto, E., Estanislao-Gómez, C. C., Pérez-Ishiwara, D. G., Ramirez-Celis, C., & Gómez-García, M. d C. (2019). Cytotoxic effect and mechanisms from some plant-derived compounds in breast cancer. Cytotoxicity - definition, identification, and cytotoxic compounds. Erman Salih Istifli.
   Google Scholar
• Philip, P. A. (2008). Targeted therapies for pancreatic cancer. Gastrointestinal Cancer Research, 2(4), S16–S19. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2661543/
   PubMedGoogle Scholar
• Rahib, L., Smith, B. D., Aizenberg, R., Rosenzweig, A. B., Fleshman, J. M., & Matrisian, L. M. (2014). Projecting cancer incidence and deaths to 2030: The unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Research, 74(11), 2913–2921. https://doi.org/10.1158/0008-5472.CAN-14-0155
   PubMed Web of Science ®Google Scholar
• Ramadan, A., Soliman, G., Mahmoud, S. S., Nofal, S. M., & Abdel-Rahman, R. F. (2012). Evaluation of the safety and antioxidant activities of Crocus sativus and Propolis ethanolic extracts. Journal of Saudi Chemical Society, 16(1), 13–21. https://doi.org/10.1016/j.jscs.2010.10.012
   Web of Science ®Google Scholar
• Reyes-Farias, M., & Carrasco-Pozo, C. (2019). The anti-cancer effect of quercetin: Molecular implications in cancer metabolism. International Journal of Molecular Sciences, 20(13), 3177. https://doi.org/10.3390/ijms20133177
   PubMed Web of Science ®Google Scholar
• Rhallab, A., Chakir, S., Elbadaoui, K., Alaoui, & T., lmolek. (2014). Evaluation of acute and subacute toxicity of aqueous extracts from Marrubium vulgare L in rodents. Journal of Pharmacy Research, 8, 684–688. http://eprints.umi.ac.ma/id/eprint/1031.
   Google Scholar
• Salama, Y. A., El-karef, A., El Gayyar, A. M., & Abdel-Rahman, N. (2019). Beyond its antioxidant properties: Quercetin targets multiple signalling pathways in hepatocellular carcinoma in rats. Life Sciences, 236, 116933. https://doi.org/10.1016/j.lfs.2019.116933
   PubMed Web of Science ®Google Scholar
• Siegel, R., Ma, J., Zou, Z., & Jemal, A. (2014). Cancer statistics, 2014. CA: A Cancer Journal for Clinicians, 64(1), 9–29. https://doi.org/10.3322/caac.21208
   PubMed Web of Science ®Google Scholar
• Siegel, R. L., Miller, K. D., & Jemal, A. (2019). Cancer statistics, 2019. CA: A Cancer Journal for Clinicians, 69(1), 7–34. https://doi.org/10.3322/caac.21551
   PubMed Web of Science ®Google Scholar
• Slee, E. A., Adrain, C., & Martin, S. J. (2001). Executioner caspase-3, -6, and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis*. The Journal of Biological Chemistry, 276(10), 7320–7326. https://doi.org/10.1074/jbc.M008363200
   PubMed Web of Science ®Google Scholar
• Sohal, D. P. S., Mangu, P. B., Khorana, A. A., Shah, M. A., Philip, P. A., O'Reilly, E. M., Uronis, H. E., Ramanathan, R. K., Crane, C. H., Engebretson, A., Ruggiero, J. T., Copur, M. S., Lau, M., Urba, S., & Laheru, D. (2016). Metastatic pancreatic cancer: American society of clinical oncology clinical practice guideline. Journal of Clinical Oncology, 34(23), 2784–2796. https://doi.org/10.1200/JCO.2016.67.1412
   PubMed Web of Science ®Google Scholar
• Su, D., Liao, Z., Feng, B., Wang, T., shan, B., Zeng, Q., Song, J., & Song, Y. (2020). Pulsatilla Chinensis saponins cause liver injury through interfering ceramide/sphingomyelin balance that promotes lipid metabolism dysregulation and apoptosis. Phytomedicine: International Journal of Phytotherapy and Phytopharmacology, 76, 153265. https://doi.org/10.1016/j.phymed.2020.153265
   PubMed Web of Science ®Google Scholar
• Velmurugan, B. K., Lin, J. T., Mahalakshmi, B., Chuang, Y. C., Lin, C. C., Lo, Y. S., Hsieh, M. J., & Chen, M. K. (2020). Luteolin-7-O-glucoside inhibits oral cancer cell migration and invasion by regulating matrix metalloproteinase-2 expression and extracellular signal-regulated kinase pathway. Biomolecules, 10(4), 502. https://doi.org/10.3390/biom10040502
   PubMed Web of Science ®Google Scholar
• Villodre, E. S., Kipper, F. C., Pereira, M. B., & Lenz, G. (2016). Roles of OCT4 in tumorigenesis, cancer therapy resistance and prognosis. Cancer Treatment Reviews, 51, 1–9. https://doi.org/10.1016/j.ctrv.2016.10.003
   PubMed Web of Science ®Google Scholar
• Volk-Draper, L., Hall, K., Griggs, C., Rajput, S., Kohio, P., DeNardo, D., & Ran, S. (2014). Paclitaxel therapy promotes breast cancer metastasis in a TLR4-dependent manner. Cancer Research, 74(19), 5421–5434. https://doi.org/10.1158/0008-5472.CAN-14-0067
   PubMed Web of Science ®Google Scholar
• Walsh, J. G., Cullen, S. P., Sheridan, C., Lüthi, A. U., Gerner, C., & Martin, S. J. (2008). Executioner caspase-3 and caspase-7 are functionally distinct proteases. Proceedings of the National Academy of Sciences, 105(35), 12815–12819. https://doi.org/10.1073/pnas.0707715105
   PubMed Web of Science ®Google Scholar
• Wang, T., Gong, X., Jiang, R., Li, H., Du, W., & Kuang, G. (2016). Ferulic acid inhibits proliferation and promotes apoptosis via blockage of PI3K/Akt pathway in osteosarcoma cell. American Journal of Translational Research, 8(2), 968–980. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4846940/
   PubMed Web of Science ®Google Scholar
• Weina, K., & Utikal, J. (2014). SOX2 and cancer: Current research and its implications in the clinic. Clinical and Translational Medicine, 3, 19. https://doi.org/10.1186/2001-1326-3-19
   PubMedGoogle Scholar
• Yang, M., Wu, Z., Wang, Y., Kai, G., Singor Njateng, G. S., Cai, S., Cao, J., & Cheng, G. (2019). Acute and subacute toxicity evaluation of ethanol extract from aerial parts of Epigynum auritum in mice. Food and Chemical Toxicology, 131, 110534. https://doi.org/10.1016/j.fct.2019.05.042
   PubMed Web of Science ®Google Scholar
• Zhang, J., Wu, D., Song, J., Wang, J., Yi, J., & Dong, W. (2015). Hesperetin induces the apoptosis of gastric cancer cells via activating mitochondrial pathway by increasing reactive oxygen species. Digestive Diseases and Sciences, 60(10), 2985–2995. https://doi.org/10.1007/s10620-015-3696-7
   PubMed Web of Science ®Google Scholar