Research Article
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Bongardia chrysogonum (L.) Spach as a potential medicinal plant against cancer and Alzheimer’s disease management

Year 2021, Volume: 51 Issue: 3, 319 - 325, 29.12.2021

Abstract

Background and Aims: Bongardia chrysogonum (L.) Spach (Berberidaceae), an ancient medicinal plant in Eastern Mediterranean countries, is traditionally used for the treatment of epilepsy, hemorrhoids, urinary system infections and gastrointestinal disorders. This study was designed to evaluate potential neuroprotective and anticancer effects of different parts from B. chrysogonum. Material and Methods: Leaf, stem, and tuber parts of the plant were extracted and subjected to determine cholinesterase enzyme inhibitory potentials and anticancer activities. Enzyme inhibition assays were carried out to screen neuroprotective potentials, while the MTT assay was performed for evaluating anticancer activities of the extracts towards human lung carcinoma (A549), breast adenocarcinoma (MCF-7), brain glioma (C6), and non-tumorous human umbilical vein endothelial cell (HUVEC) lines. Results: Among the tested extracts, the highest enzyme inhibitory activity was exhibited by tuber-water extract (83.81±0.33% and 62.14±0.60% inhibition on AChE and BChE at 400 μg/mL p<0.01, respectively), whilst the lowest enzyme inhibition was exerted by the tuber-chloroform extract. Moreover, the tuber part of the plant was found to have the most cytotoxic activity against all the cancer cells, and the best anticancer activity was determined in tuber ethanol extract against MCF-7 cells (IC50= 28.36±0.04, p<0.01). Conclusion: To the best of our knowledge, this research is the first study that assessed the in vitro neuroprotective effect of the aerial parts and tuber extracts of the plant through inhibition of cholinesterase enzymes alongside an anticancer capacity towards human cancer cells. The results revealed that this plant is a good candidate for performing further clinical studies in cancer and neurodegenerative diseases.

Supporting Institution

This study was financially supported by the Scientific Research Project Unit of Kilis 7 Aralik University, Kilis – Turkey

Project Number

11911/1828MAP1

Thanks

The authors would like to thank Genetics Laboratory, Advanced Technology Application and Research Center, Kilis 7 Aralik University for technical support. The authors are also grateful to Res. Assist. Fatih Yayla for identifying and Biologist Didem Kocum for providing the plant material.

References

  • • Abuhamdah, S., Abuirmeile, A. N., Thaer, F., Al-Olimat, S., Abdel, E., & Chazot, P. L. (2017a). Anti-convulsant effects of Bongardia chrysogonum L. tuber in the pentylenetetrazole-induced seizure model. International Journal of Pharmacology, 14(1), 127–135. https:// doi.org/10.3923/ijp.2018.127.135.
  • • Abuhamdah, S., Shatarat, A., Al-Essa, M., Al-Ameer, H., Al-Olimat, S., & Chazot, P. (2017b). Spasmolytic and antimicrobial activities of crude extract of Bongardia chrysogonum L. tubers. International Journal of Pharmacology, 14(1), 52–60. https://doi.org/10.3923/ijp.2018.52.60.
  • • Ahmad, S. S., Waheed, T., Rozeen, S., Mahmood, S., & Kamal, M. A. (2019). Therapeutic study of phytochemicals against cancer and Alzheimer’s disease management. Current Drug Metabolism, 20(13), 1006–1013. https://doi.org/10.2174/13892002216662001 03092719.
  • • Alamgir, A.N.M. (2017). Therapeutic use of medicinal plants and their extracts: volume 1: pharmacognosy. K.D. Rainsford (Ed.), Progress in Drug Research 73, Springer International Publishing AG. https://doi.org/10.1007/987-3-319-63862-1.
  • • Alfatafta, A. A., Abu Zarga, M. H., Sabri, S. S., Freyer, A. J., & Shamma, M. (1989). An investigation of Bongardia chrysogonum. Journal of Natural Products, 52(4), 818–821. https://doi.org/10.1021/ np50064a024.
  • • Baydoun, S., Chalak, L., Dalleh, H., & Arnold, N. (2015). Ethnopharmacological survey of medicinal plants used in traditional medicine by the communities of Mount Hermon, Lebanon. Journal of Ethnopharmacology, 173, 139–156. https://doi.org/10.1016/j.jep.2015.06.052.
  • • Chen, L., Lin, L., Dong, Z., Zhang, L., & Du, H. (2018). Comparison of neuroprotective effect of Forsythia suspensa leaf extract and forsythiaside, one of its metabolites. Natural Product Research, 32(22), 2705–2708. https://doi.org/10.1080/14786419.2018.1514401.
  • • Dokuyucu, R., Gozukara, K. H., Ozcan, O., Sefil, N. K., Nacar, A., Dokuyucu, A., & Inci, M. (2016). The effect of Bongardia chrysogonum on prostate tissue in a rat model of STZ-induced diabetes. SpringerPlus, 5(1), 1–7. https://doi.org/10.1186/s40064-016-2973-z.
  • • Ellman, G. L., Courtney, K. D., Andres Jr, V., & Featherstone, R. M. (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology, 7(2), 88–95. https://doi.org/10.1016/0006-2952(61)90145-9.
  • • Fang, J., Wang, L., Wu, T., Yang, C., Gao, L., Cai, H., ... & Wang, Q. (2017). Network pharmacology-based study on the mechanism of action for herbal medicines in Alzheimer treatment. Journal of Ethnopharmacology, 196, 281-292. https://doi.org/10.1016/j. jep.2016.11.034.
  • • Gezici, S., Sekeroglu, N., & Kijjoa, A. (2017). In vitro anticancer activity and antioxidant properties of essential oils from Populus alba L. and Rosmarinus officinalis L. from South Eastern Anatolia of Turkey. Indian Journal of Pharmaceutical Education and Research, 51(3), 498-503. https://doi.org/10.5530/ijper.51.3s.74.
  • • Gezici, S. (2018). Promising anticancer activity of lavender (Lavandula angustifolia Mill.) essential oil through induction of both apoptosis and necrosis. Annals of Phytomedicine, 7(2), 38-45. https://doi.org/10.21276/ap.2018.7.2.55.
  • • Gezici, S. (2019). Comparative anticancer activity analysis of saffron extracts and a principle component, crocetin for prevention and treatment of human malignancies. Journal of Food Science and Technology, 56(12), 5435-5443. https://doi.org/10.1007/ s13197-019-04014-y.
  • • Gezici, S., & Sekeroglu, N. (2019a). Neuroprotective potential and phytochemical composition of acorn fruits. Industrial Crops and Products, 128, 13-17. https://doi.org/10.1016/j.indcrop. 2018.10.082.
  • • Gezici, S., & Sekeroglu, N. (2019b). Current perspectives in the application of medicinal plants against cancer: novel therapeutic agents. Anti-Cancer Agents in Medicinal Chemistry, 19(1), 101-111. https://doi.org/10.2174/1871520619666181224121004.
  • • Gezici, S., & Sekeroglu, N. (2021). Comparative biological analyses on kenger and kenger coffee as novel functional food products. Journal of Food Science and Technology, 1-11. https://doi. org/10.1007/s13197-021-05248-5.
  • • Grutzendler, J., & Morris, J. C. (2001). Cholinesterase inhibitors for Alzheimer’s disease. Drugs, 61(1), 41-52. https://doi. org/10.2165/00003495-200161010-00005. • Harris, R. E. (2019). Epidemiology of chronic disease: global perspectives. (chapter 48, pp. 753-769). Second Edition, Jones & Bartlett Learning.
  • • Ismail, H., Amanat, M. A., Iqbal, A., & Mirza, B. (2018). Medicinal plants: a complementary and alternative antidepressant therapy. Current Pharmaceutical Design, 24(22), 2609-2624. https://doi.org/ 10.2174/1381612824666180727123950.
  • • Karl, R., & Strid, A. (2009). Bongardia chrysogonum (Berberidaceae) rediscovered on the East Aegean island of Chios. Phytologia Balcanica, 15, 337-342. https://citeseerx.ist.psu.edu/viewdoc/downl oad?doi=10.1.1.482.7088&rep=rep1&type=pdf.
  • • Khan, T., Ali, M., Khan, A., Nisar, P., Jan, S. A., Afridi, S., & Shinwari, Z. K. (2020). Anticancer plants: A review of the active phytochemicals, applications in animal models, and regulatory aspects. Biomolecules, 10(1), 47. https://doi.org/10.3390/biom10010047.
  • • Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods, 65(1-2), 55-63. https://doi. org/10.1016/0022-1759(83)90303-4.
  • • Rahman, A. U., Shahwar, D., Parween, Z., Choudhary, M. I., Sener, B., Toker, G., & Can Baser, K. H. (1998). New alkaloids from Bongardia chrysogonum. Natural Product Letters, 12(3), 161-173. https://doi. org/10.1080/10575639808048287.
  • • Rahman, A.U, Shahwar, D., Choudhary, M.I., Sener, B., Toker, G., & Baser, K.H.C. (2000). Triterpenoid saponins from Bongardia chrysogonum. Journal of Natural Products, 63(2), 251-253. https://doi. org/10.1021/np9801312.
  • • Roleira, F. M., Tavares-da-Silva, E. J., Varela, C. L., Costa, S. C., Silva, T., Garrido, J., & Borges, F. (2015). Plant derived and dietary phenolic antioxidants: Anticancer properties. Food Chemistry, 183, 235-258. https://doi.org/10.1016/j.foodchem.2015.03.039.
  • • Safarzadeh, E., Shotorbani, S. S., & Baradaran, B. (2014). Herbal medicine as inducers of apoptosis in cancer treatment. Advanced Pharmaceutical Bulletin, 4(1), 421. https://doi.org/10.5681/ apb.2014.062.
  • • Sahoo, A. K., Dandapat, J., Dash, U. C., & Kanhar, S. (2018). Features and outcomes of drugs for combination therapy as multi-targets strategy to combat Alzheimer’s disease. Journal of Ethnopharmacology, 215, 42-73. https://doi.org/10.1016/j.jep.2017.12.015.
  • • Santos, T. C. D., Gomes, T. M., Pinto, B. A. S., Camara, A. L., & Paes, A. M. D. A. (2018). Naturally occurring acetylcholinesterase inhibitors and their potential use for Alzheimer’s disease therapy. Frontiers in Pharmacology, 9, 1192. https://doi.org/10.3389/fphar.2018.01192.
  • • Sekeroglu, N., & Gezici, S. (2019). Astragalus neurocarpus Bioss. as a potential source of natural enzyme inhibitor associated with Alzheimer’s and Parkinson diseases along with its rich polyphenolic content and antioxidant activities. Annals of Phytomedicine, 8(1), 82-87. https://doi.org/10.21276/ap.2019.8.1.9.
  • • Sekeroglu, N., Senol, F. S., Orhan, I. E., Gulpinar, A. R., Kartal, M., & Sener, B. (2012). In vitro prospective effects of various traditional herbal coffees consumed in Anatolia linked to neurodegeneration. Food Research International, 45(1), 197-203. https://doi. org/10.1016/j.foodres.2011.10.0088.
  • • Senol, F. S., Sekeroglu, N., Gezici, S., Kilic, E., Orhan, I. E. (2018). Neuroprotective potential of the fruit (acorn) from Quercus coccifera L. Turkish Journal of Agriculture and Forestry, 42(2), 82-87. https://doi. org/10.3906/tar-1711-18.
  • • Shahwar, D., Choudhary, M. I., Sener, B., Toker, G., & Baser, K. H. C. (1999). Alkaloids of Bongardia chrysogonum. Phytochemistry, 50(2), 333-336. https://doi.org/10.1016/S0031-9422(98)00484-1.
Year 2021, Volume: 51 Issue: 3, 319 - 325, 29.12.2021

Abstract

Project Number

11911/1828MAP1

References

  • • Abuhamdah, S., Abuirmeile, A. N., Thaer, F., Al-Olimat, S., Abdel, E., & Chazot, P. L. (2017a). Anti-convulsant effects of Bongardia chrysogonum L. tuber in the pentylenetetrazole-induced seizure model. International Journal of Pharmacology, 14(1), 127–135. https:// doi.org/10.3923/ijp.2018.127.135.
  • • Abuhamdah, S., Shatarat, A., Al-Essa, M., Al-Ameer, H., Al-Olimat, S., & Chazot, P. (2017b). Spasmolytic and antimicrobial activities of crude extract of Bongardia chrysogonum L. tubers. International Journal of Pharmacology, 14(1), 52–60. https://doi.org/10.3923/ijp.2018.52.60.
  • • Ahmad, S. S., Waheed, T., Rozeen, S., Mahmood, S., & Kamal, M. A. (2019). Therapeutic study of phytochemicals against cancer and Alzheimer’s disease management. Current Drug Metabolism, 20(13), 1006–1013. https://doi.org/10.2174/13892002216662001 03092719.
  • • Alamgir, A.N.M. (2017). Therapeutic use of medicinal plants and their extracts: volume 1: pharmacognosy. K.D. Rainsford (Ed.), Progress in Drug Research 73, Springer International Publishing AG. https://doi.org/10.1007/987-3-319-63862-1.
  • • Alfatafta, A. A., Abu Zarga, M. H., Sabri, S. S., Freyer, A. J., & Shamma, M. (1989). An investigation of Bongardia chrysogonum. Journal of Natural Products, 52(4), 818–821. https://doi.org/10.1021/ np50064a024.
  • • Baydoun, S., Chalak, L., Dalleh, H., & Arnold, N. (2015). Ethnopharmacological survey of medicinal plants used in traditional medicine by the communities of Mount Hermon, Lebanon. Journal of Ethnopharmacology, 173, 139–156. https://doi.org/10.1016/j.jep.2015.06.052.
  • • Chen, L., Lin, L., Dong, Z., Zhang, L., & Du, H. (2018). Comparison of neuroprotective effect of Forsythia suspensa leaf extract and forsythiaside, one of its metabolites. Natural Product Research, 32(22), 2705–2708. https://doi.org/10.1080/14786419.2018.1514401.
  • • Dokuyucu, R., Gozukara, K. H., Ozcan, O., Sefil, N. K., Nacar, A., Dokuyucu, A., & Inci, M. (2016). The effect of Bongardia chrysogonum on prostate tissue in a rat model of STZ-induced diabetes. SpringerPlus, 5(1), 1–7. https://doi.org/10.1186/s40064-016-2973-z.
  • • Ellman, G. L., Courtney, K. D., Andres Jr, V., & Featherstone, R. M. (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology, 7(2), 88–95. https://doi.org/10.1016/0006-2952(61)90145-9.
  • • Fang, J., Wang, L., Wu, T., Yang, C., Gao, L., Cai, H., ... & Wang, Q. (2017). Network pharmacology-based study on the mechanism of action for herbal medicines in Alzheimer treatment. Journal of Ethnopharmacology, 196, 281-292. https://doi.org/10.1016/j. jep.2016.11.034.
  • • Gezici, S., Sekeroglu, N., & Kijjoa, A. (2017). In vitro anticancer activity and antioxidant properties of essential oils from Populus alba L. and Rosmarinus officinalis L. from South Eastern Anatolia of Turkey. Indian Journal of Pharmaceutical Education and Research, 51(3), 498-503. https://doi.org/10.5530/ijper.51.3s.74.
  • • Gezici, S. (2018). Promising anticancer activity of lavender (Lavandula angustifolia Mill.) essential oil through induction of both apoptosis and necrosis. Annals of Phytomedicine, 7(2), 38-45. https://doi.org/10.21276/ap.2018.7.2.55.
  • • Gezici, S. (2019). Comparative anticancer activity analysis of saffron extracts and a principle component, crocetin for prevention and treatment of human malignancies. Journal of Food Science and Technology, 56(12), 5435-5443. https://doi.org/10.1007/ s13197-019-04014-y.
  • • Gezici, S., & Sekeroglu, N. (2019a). Neuroprotective potential and phytochemical composition of acorn fruits. Industrial Crops and Products, 128, 13-17. https://doi.org/10.1016/j.indcrop. 2018.10.082.
  • • Gezici, S., & Sekeroglu, N. (2019b). Current perspectives in the application of medicinal plants against cancer: novel therapeutic agents. Anti-Cancer Agents in Medicinal Chemistry, 19(1), 101-111. https://doi.org/10.2174/1871520619666181224121004.
  • • Gezici, S., & Sekeroglu, N. (2021). Comparative biological analyses on kenger and kenger coffee as novel functional food products. Journal of Food Science and Technology, 1-11. https://doi. org/10.1007/s13197-021-05248-5.
  • • Grutzendler, J., & Morris, J. C. (2001). Cholinesterase inhibitors for Alzheimer’s disease. Drugs, 61(1), 41-52. https://doi. org/10.2165/00003495-200161010-00005. • Harris, R. E. (2019). Epidemiology of chronic disease: global perspectives. (chapter 48, pp. 753-769). Second Edition, Jones & Bartlett Learning.
  • • Ismail, H., Amanat, M. A., Iqbal, A., & Mirza, B. (2018). Medicinal plants: a complementary and alternative antidepressant therapy. Current Pharmaceutical Design, 24(22), 2609-2624. https://doi.org/ 10.2174/1381612824666180727123950.
  • • Karl, R., & Strid, A. (2009). Bongardia chrysogonum (Berberidaceae) rediscovered on the East Aegean island of Chios. Phytologia Balcanica, 15, 337-342. https://citeseerx.ist.psu.edu/viewdoc/downl oad?doi=10.1.1.482.7088&rep=rep1&type=pdf.
  • • Khan, T., Ali, M., Khan, A., Nisar, P., Jan, S. A., Afridi, S., & Shinwari, Z. K. (2020). Anticancer plants: A review of the active phytochemicals, applications in animal models, and regulatory aspects. Biomolecules, 10(1), 47. https://doi.org/10.3390/biom10010047.
  • • Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods, 65(1-2), 55-63. https://doi. org/10.1016/0022-1759(83)90303-4.
  • • Rahman, A. U., Shahwar, D., Parween, Z., Choudhary, M. I., Sener, B., Toker, G., & Can Baser, K. H. (1998). New alkaloids from Bongardia chrysogonum. Natural Product Letters, 12(3), 161-173. https://doi. org/10.1080/10575639808048287.
  • • Rahman, A.U, Shahwar, D., Choudhary, M.I., Sener, B., Toker, G., & Baser, K.H.C. (2000). Triterpenoid saponins from Bongardia chrysogonum. Journal of Natural Products, 63(2), 251-253. https://doi. org/10.1021/np9801312.
  • • Roleira, F. M., Tavares-da-Silva, E. J., Varela, C. L., Costa, S. C., Silva, T., Garrido, J., & Borges, F. (2015). Plant derived and dietary phenolic antioxidants: Anticancer properties. Food Chemistry, 183, 235-258. https://doi.org/10.1016/j.foodchem.2015.03.039.
  • • Safarzadeh, E., Shotorbani, S. S., & Baradaran, B. (2014). Herbal medicine as inducers of apoptosis in cancer treatment. Advanced Pharmaceutical Bulletin, 4(1), 421. https://doi.org/10.5681/ apb.2014.062.
  • • Sahoo, A. K., Dandapat, J., Dash, U. C., & Kanhar, S. (2018). Features and outcomes of drugs for combination therapy as multi-targets strategy to combat Alzheimer’s disease. Journal of Ethnopharmacology, 215, 42-73. https://doi.org/10.1016/j.jep.2017.12.015.
  • • Santos, T. C. D., Gomes, T. M., Pinto, B. A. S., Camara, A. L., & Paes, A. M. D. A. (2018). Naturally occurring acetylcholinesterase inhibitors and their potential use for Alzheimer’s disease therapy. Frontiers in Pharmacology, 9, 1192. https://doi.org/10.3389/fphar.2018.01192.
  • • Sekeroglu, N., & Gezici, S. (2019). Astragalus neurocarpus Bioss. as a potential source of natural enzyme inhibitor associated with Alzheimer’s and Parkinson diseases along with its rich polyphenolic content and antioxidant activities. Annals of Phytomedicine, 8(1), 82-87. https://doi.org/10.21276/ap.2019.8.1.9.
  • • Sekeroglu, N., Senol, F. S., Orhan, I. E., Gulpinar, A. R., Kartal, M., & Sener, B. (2012). In vitro prospective effects of various traditional herbal coffees consumed in Anatolia linked to neurodegeneration. Food Research International, 45(1), 197-203. https://doi. org/10.1016/j.foodres.2011.10.0088.
  • • Senol, F. S., Sekeroglu, N., Gezici, S., Kilic, E., Orhan, I. E. (2018). Neuroprotective potential of the fruit (acorn) from Quercus coccifera L. Turkish Journal of Agriculture and Forestry, 42(2), 82-87. https://doi. org/10.3906/tar-1711-18.
  • • Shahwar, D., Choudhary, M. I., Sener, B., Toker, G., & Baser, K. H. C. (1999). Alkaloids of Bongardia chrysogonum. Phytochemistry, 50(2), 333-336. https://doi.org/10.1016/S0031-9422(98)00484-1.
There are 31 citations in total.

Details

Primary Language English
Subjects Pharmacology and Pharmaceutical Sciences
Journal Section Original Article
Authors

Sevgi Gezici 0000-0002-4856-0221

Nazım Şekeroğlu 0000-0002-0630-0106

Project Number 11911/1828MAP1
Publication Date December 29, 2021
Submission Date March 7, 2021
Published in Issue Year 2021 Volume: 51 Issue: 3

Cite

APA Gezici, S., & Şekeroğlu, N. (2021). Bongardia chrysogonum (L.) Spach as a potential medicinal plant against cancer and Alzheimer’s disease management. İstanbul Journal of Pharmacy, 51(3), 319-325.
AMA Gezici S, Şekeroğlu N. Bongardia chrysogonum (L.) Spach as a potential medicinal plant against cancer and Alzheimer’s disease management. iujp. December 2021;51(3):319-325.
Chicago Gezici, Sevgi, and Nazım Şekeroğlu. “Bongardia Chrysogonum (L.) Spach As a Potential Medicinal Plant Against Cancer and Alzheimer’s Disease Management”. İstanbul Journal of Pharmacy 51, no. 3 (December 2021): 319-25.
EndNote Gezici S, Şekeroğlu N (December 1, 2021) Bongardia chrysogonum (L.) Spach as a potential medicinal plant against cancer and Alzheimer’s disease management. İstanbul Journal of Pharmacy 51 3 319–325.
IEEE S. Gezici and N. Şekeroğlu, “Bongardia chrysogonum (L.) Spach as a potential medicinal plant against cancer and Alzheimer’s disease management”, iujp, vol. 51, no. 3, pp. 319–325, 2021.
ISNAD Gezici, Sevgi - Şekeroğlu, Nazım. “Bongardia Chrysogonum (L.) Spach As a Potential Medicinal Plant Against Cancer and Alzheimer’s Disease Management”. İstanbul Journal of Pharmacy 51/3 (December 2021), 319-325.
JAMA Gezici S, Şekeroğlu N. Bongardia chrysogonum (L.) Spach as a potential medicinal plant against cancer and Alzheimer’s disease management. iujp. 2021;51:319–325.
MLA Gezici, Sevgi and Nazım Şekeroğlu. “Bongardia Chrysogonum (L.) Spach As a Potential Medicinal Plant Against Cancer and Alzheimer’s Disease Management”. İstanbul Journal of Pharmacy, vol. 51, no. 3, 2021, pp. 319-25.
Vancouver Gezici S, Şekeroğlu N. Bongardia chrysogonum (L.) Spach as a potential medicinal plant against cancer and Alzheimer’s disease management. iujp. 2021;51(3):319-25.