EVALUATION OF NON-CYTOTOXIC DRUGS AS POTENTIAL CANDIDATES FOR BREAST CANCER
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Keywords
Abstract
Suramin, a potent anti-parasitic agent has been used as anti-cancer drug during last years against a vast variety of cancers. This study highlight the use of suramin as an anti-cancer drug in treatment of breast cancer. The goal of the current investigation was to determine whether the breast cancer cell line MCF-7 exhibited increased expression of heparanase-mediated epithelial mesenchymal transition in vitro. Different cancer stem cell markers were examined using reverse transcription quantitative polymerase chain reaction with the following primers: Snail, Slug, E-cadherin, vimentin, NESTIN, NANOG, CXCR-4, OCT3/4, MDR, and MMP's. The effect of the test media on cancer cells was investigated using proliferation and viability assays, as well as gene expression and marker expression. Cell proliferation was identified by the treatment of MCF-7 cell line with suramin and using the test media (containing 200µM suramin) as an inhibitor of heparanase and epithelial‑mesenchymal transition (EMT) in breast cancer cells. Suramin therapy decreased mRNA expression of EMT indicators, cancer stem cell markers, drug resistance proteins, matrix metalloproteinases, and heparanase in a time dependent manner. An inhibitory effect of suramin was also evaluatedin proliferation of cancer cells in MTT assay. In addition, suramin also exhibited a time-dependent inhibition of MCF-7 cell migration in the wound healing assay. As a result, the use of suramin as an anti-cancer agent provides the opportunity for novel drug design to address the issues of drug resistance, metastasis, and chemotherapeutic agent toxicity while improving therapeutic efficacy.
References
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22. Nakajima, M., Irimura, T., & Nicolson, G. L. (1988). Heparanases and tumor metastasis. Journal of cellular biochemistry, 36(2), 157-167.
23. Masola, V., Gambaro, G., Tibaldi, E., Brunati, A. M., Gastaldello, A., D'Angelo, A.,& Lupo, A. (2012). Heparanase and syndecan-1 interplay orchestrates fibroblast growth factor-2-induced epithelial-mesenchymal transition in renal tubular cells. Journal of Biological Chemistry, 287(2), 1478-1488.
24. Masola, V., Zaza, G., Secchi, M. F., Gambaro, G., Lupo, A., & Onisto, M. (2014). Heparanase is a key player in renal fibrosis by regulating TGF-β expression and activity. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1843(9), 2122-2128.
25. Steverding, D. (2010). The development of drugs for treatment of sleeping sickness: a historical review. Parasites & vectors, 3(1), 15.
26. Nakajima, M., DeChavigny, A., Johnson, C. E., Hamada, J. I., Stein, C. A., & Nicolson, G. L. (1991). Suramin. A potent inhibitor of melanoma heparanase and invasion. Journal of Biological Chemistry, 266(15), 9661-9666.
27. Li, H., Qu, H., Zhao, M., Yuan, B., Cao, M., & Cui, J. (2015). Suramin inhibits cell proliferation in ovarian and cervical cancer by downregulating heparanase expression. Cancer Cell Int, 15, 52.
28. Mirza, M. R., Jakobsen, E., Pfeiffer, P., Lindebjerg-Clasen, B., Bergh, J., & Rose, C. (1997). Suramin in non-small cell lung cancer and advanced breast cancer: two parallel phase II studies. Acta Oncologica, 36(2), 171-174.
29. Tayel, A., Abd El Galil, K. H., Ebrahim, M. A., Ibrahim, A. S., El-Gayar, A. M., & Al-Gayyar, M. M. (2014). Suramin inhibits hepatic tissue damage in hepatocellular carcinoma through deactivation of heparanase enzyme. Eur J Pharmacol, 728, 151-160
30. Falcone, A., Pfanner, E., Cianci, C., Danesi, R., Brunetti, I., Del Tacca, M., & Conte, P. F. (1995). Suramin in patients with metastatic colorectal cancer pretreated with fluoropyrimidine-based chemotherapy. A phase II study. Cancer, 75(2), 440-443.
31. Shah, S., Fourgeaud, C., Derieux, S., Mirshahi, S., Contant, G., Pimpie, C., Mirshahi, M. (2018). The close relationship between heparanase and epithelial mesenchymal transition in gastric signet-ring cell adenocarcinoma. Oncotarget, 9(73), 33778.
32. Bhargava, S., Hotz, B., Hines, O. J., Reber, H. A., Buhr, H. J., & Hotz, H. G. (2007). Suramin inhibits not only tumor growth and metastasis but also angiogenesis in experimental pancreatic cancer. J Gastrointest Surg, 11(2), 171-178.
33. Wade, T. P., Kasid, A., Stein, C. A., LaRocca, R. V., Sargent, E. R., Gomella, L. G., Linehan, W. M. (1992). Suramin interference with transforming growth factor-beta inhibition of human renal cell carcinoma in culture. J Surg Res, 53(2), 195-198.
34. Shin, R., Naomoto, Y., Kamikawa, Y., Tanaka, N., & Orita, K. (1997). Effect of suramin on human esophageal cancer cells in vitro and in vivo. [Comparative Study]. Scand J Gastroenterol, 32(8), 824-828.
35. Gansler, T., Vaghmar, N., Olson, J. J., & Graham, S. D. (1992). Suramin inhibits growth factor binding and proliferation by urothelial carcinoma cell cultures. J Urol, 148(3), 910-914.
36. Hensey, C. E., Boscoboinik, D., & Azzi, A. (1989). Suramin, an anti-cancer drug, inhibits protein kinase C and induces differentiation in neuroblastoma cell clone NB2A. [Research Support, Non-U.S. Gov't]. FEBS Lett, 258(1), 156-158.
37. Eisenberger, M. A., Reyno, L. M., Jodrell, D. I., Sinibaldi, V. J., Tkaczuk, K. H., Sridhara, R., & Egorin, M. J. (1993). Suramin, an active drug for prostate cancer: interim observations in a phase I trial. JNCI: Journal of the National Cancer Institute, 85(8), 611-621.
38. Li, J., Pan, Q., Rowan, P. D., Trotter, T. N., Peker, D., Regal, K. M., & Yang, Y. (2016). Heparanase promotes myeloma progression by inducing mesenchymal features and motility of myeloma cells. Oncotarget, 7(10), 11299.
39. Senthilraja, P., & Kathiresan, K. (2015). In vitro cytotoxicity MTT assay in Vero, HepG2 and MCF-7 cell lines study of Marine Yeast. J Appl Pharm Sci, 5(3), 080-084.
40. Masola, V., Bellin, G., Gambaro, G., & Onisto, M. (2018). Heparanase: A multitasking protein involved in extracellular matrix (ECM) remodeling and intracellular events. Cells, 7(12), 236.
41. Jia, L., & Ma, S. (2016). Recent advances in the discovery of heparanase inhibitors as anti-cancer agents. European journal of medicinal chemistry, 121, 209-220.
42. Jayatilleke, K., Duivenvoorden, H., Parker, B., & Hulett, M. (2018). PO-220 Defining the role of heparanase in breast cancer progression using the PyMT-MMTV mouse model: BMJ Publishing Group Limited.
43. La Rocca, R. V., Meer, J., Gilliatt, R. W., Stein, C. A., Cassidy, J., Myers, C. E., & Dalakas, M. C. (1990). Suramin‐induced polyneuropathy. Neurology, 40(6), 954-954.
44. Kobayashi, K., Weiss, R. E., Vogelzang, N. J., Vokes, E. E., Janisch, L., & Ratain, M. J. (1996). Mineralocorticoid insufficiency due to suramin therapy. Cancer: Interdisciplinary International Journal of the American Cancer Society, 78(11), 2411-2420.
45. Figg, W. D., Cooper, M. R., Thibault, A., Headlee, D., Humphrey, J., Bergan, R. C.,& Sartor, O. (1994). Acute renal toxicity associated with suramin in the treatment of prostate cancer. Cancer, 74(5), 1612-1614.
46. Foekens, J. A., Sieuwerts, A. M., Stuurman‐Smeets, E. M., Dorssers, L. C., Berns, E. M., & Klijn, J. G. (1992). Pleiotropic actions of suramin on the proliferation of human breast‐cancer cells in vitro. International journal of cancer, 51(3), 439-444.
47. Vignon, F., Prebois, C., & Rochefort, H. (1992). Inhibition of breast cancer growth by suramin. JNCI: Journal of the National Cancer Institute, 84(1), 38-42.
48. Bao, B., Ahmad, A., Azmi, A. S., Ali, S., & Sarkar, F. H. (2013). Overview of cancer stem cells (CSCs) and mechanisms of their regulation: implications for cancer therapy. Current protocols in pharmacology, 61(1), 14-25.
49. Soltysova, A., Altanerova, V., & Altaner, C. (2005). Cancer stem cells. Neoplasma, 52(6), 435.
50. Borst, P., Evers, R., Kool, M., & Wijnholds, J. (2000). A family of drug transporters: the multidrug resistance-associated proteins. Journal of the National Cancer Institute, 92(16), 1295-1302.
51. Burger, H., Foekens, J. A., Look, M. P., Meijer-van Gelder, M. E., Klijn, J. G., Wiemer, E. A., Nooter, K. (2003). RNA expression of breast cancer resistance protein, lung resistance-related protein, multidrug resistance-associated proteins 1 and 2, and multidrug resistance gene 1 in breast cancer: correlation with chemotherapeutic response. Clinical Cancer Research, 9(2), 827-836.
2. Kitamura, T., Qian, B. Z., Soong, D., Cassetta, L., Noy, R., Sugano, G., Pollard, J. W. (2015). CCL2-induced chemokine cascade promotes breast cancer metastasis by enhancing retention of metastasis-associated macrophages. J Exp Med, 212(7), 1043-1059.
3. Majeed, A. I., Jadoon, M., Riazuddin, S., & Akram, J. (2016). Awareness and screening of breast cancer among rural areas of Islamabad capital territory, Pakistan. Annals of PIMS ISSN, 1815, 2287.
4. Amjad, A., Khan, I., Kausar, Z., Saeed, F., & Azhar, L. (2018). Risk Factors in Breast Cancer Progression and Current Advances in Therapeutic Approaches to Knockdown Breast Cancer. Clin Med Biochem, 4(137), 2471-2663.1000137.
5. Feng, Y., Spezia, M., Huang, S., Yuan, C., Zeng, Z., Zhang, L., Ren, G. (2018). Breast cancer development and progression: Risk factors, cancer stem cells, signaling pathways, genomics, and molecular pathogenesis. [Review]. Genes Dis, 5(2), 77-106.
6. Tariq, R., Huma, S., Butt, M. Z., & Amin, F. (2013). Risk factors and prevalence of breast cancer-a review. Journal of the Pakistan medical association, 63(8), 1075-1078.
7. Giordano, S. H., Lin, Y. L., Kuo, Y. F., Hortobagyi, G. N., & Goodwin, J. S. (2012). Decline in the use of anthracyclines for breast cancer. Journal of clinical oncology, 30(18), 2232.
8. Hung, C. M., Hsu, Y. C., Chen, T. Y., Chang, C. C., & Lee, M. J. (2017). Cyclophosphamide promotes breast cancer cell migration through CXCR4 and matrix metalloproteinases. Cell biology international, 41(3), 345-352.
9. Deveci, H. A., Nazıroğlu, M., & Nur, G. (2018). 5-Fluorouracil-induced mitochondrial oxidative cytotoxicity and apoptosis are increased in MCF-7 human breast cancer cells by TRPV1 channel activation but not Hypericum perforatum treatment. Molecular and cellular biochemistry, 439(1-2), 189-198.
10. Sharma, P., López-Tarruella, S., García-Saenz, J. A., Ward, C., Connor, C. S., Gómez, H. L., & Picornell, A. C. (2017). Efficacy of neoadjuvant carboplatin plus docetaxel in triple-negative breast cancer: combined analysis of two cohorts. Clinical cancer research, 23(3), 649-657.
11. Remesh, A. (2012). Toxicities of anticancer drugs and its management.
12. Ji, X., Lu, Y., Tian, H., Meng, X., Wei, M., & Cho, W. C. (2019). Chemoresistance mechanisms of breast cancer and their countermeasures. Biomedicine & Pharmacotherapy, 114, 108800.
13. Zheng, H. C. (2017). The molecular mechanisms of chemoresistance in cancers. Oncotarget, 8(35), 59950.
14. Huh, H. J., Park, C. J., Jang, S., Seo, E. J., Chi, H. S., Lee, J. H.,& Ghim, T. (2006). Prognostic significance of multidrug resistance gene 1 (MDR1), multidrug resistance-related protein (MRP) and lung resistance protein (LRP) mRNA expression in acute leukemia. Journal of Korean medical science, 21(2), 253-258.
15. Vtorushin, S. V., Khristenko, K. Y., Zavyalova, M. V., Perelmuter, V. M., Litviakov, N. V., Denisov, E. V., & Cherdyntseva, N. V. (2014). The phenomenon of multi-drug resistance in the treatment of malignant tumors. Experimental oncology.
16. Sui, H., Zhu, L., Deng, W., & Li, Q. (2014). Epithelial-mesenchymal transition and drug resistance: role, molecular mechanisms, and therapeutic strategies. Oncology research and treatment, 37(10), 584-589.
17. Hanahan, D., & Weinberg, R. A. (2011). Hallmarks of cancer: the next generation. Cell, 144(5), 646-674.
18. Nieto MA. The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu Rev Cell Dev Biol. 2011; 27:347–76.
19. Thiery, J. P., Acloque, H., Huang, R. Y., & Nieto, M. A. (2009). Epithelial-mesenchymal transitions in development and disease. cell, 139(5), 871-890.
20. Secchi, M. F., Masola, V., Zaza, G., Lupo, A., Gambaro, G., & Onisto, M. (2015). Recent data concerning heparanase: focus on fibrosis, inflammation and cancer. Biomolecular concepts, 6(5-6), 415-421.
21. Wood, R. J., & Hulett, M. D. (2008). Cell surface-expressed cation-independent mannose 6-phosphate receptor (CD222) binds enzymatically active heparanase independently of mannose 6-phosphate to promote extracellular matrix degradation. Journal of Biological Chemistry, 283(7), 4165-4176.
22. Nakajima, M., Irimura, T., & Nicolson, G. L. (1988). Heparanases and tumor metastasis. Journal of cellular biochemistry, 36(2), 157-167.
23. Masola, V., Gambaro, G., Tibaldi, E., Brunati, A. M., Gastaldello, A., D'Angelo, A.,& Lupo, A. (2012). Heparanase and syndecan-1 interplay orchestrates fibroblast growth factor-2-induced epithelial-mesenchymal transition in renal tubular cells. Journal of Biological Chemistry, 287(2), 1478-1488.
24. Masola, V., Zaza, G., Secchi, M. F., Gambaro, G., Lupo, A., & Onisto, M. (2014). Heparanase is a key player in renal fibrosis by regulating TGF-β expression and activity. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1843(9), 2122-2128.
25. Steverding, D. (2010). The development of drugs for treatment of sleeping sickness: a historical review. Parasites & vectors, 3(1), 15.
26. Nakajima, M., DeChavigny, A., Johnson, C. E., Hamada, J. I., Stein, C. A., & Nicolson, G. L. (1991). Suramin. A potent inhibitor of melanoma heparanase and invasion. Journal of Biological Chemistry, 266(15), 9661-9666.
27. Li, H., Qu, H., Zhao, M., Yuan, B., Cao, M., & Cui, J. (2015). Suramin inhibits cell proliferation in ovarian and cervical cancer by downregulating heparanase expression. Cancer Cell Int, 15, 52.
28. Mirza, M. R., Jakobsen, E., Pfeiffer, P., Lindebjerg-Clasen, B., Bergh, J., & Rose, C. (1997). Suramin in non-small cell lung cancer and advanced breast cancer: two parallel phase II studies. Acta Oncologica, 36(2), 171-174.
29. Tayel, A., Abd El Galil, K. H., Ebrahim, M. A., Ibrahim, A. S., El-Gayar, A. M., & Al-Gayyar, M. M. (2014). Suramin inhibits hepatic tissue damage in hepatocellular carcinoma through deactivation of heparanase enzyme. Eur J Pharmacol, 728, 151-160
30. Falcone, A., Pfanner, E., Cianci, C., Danesi, R., Brunetti, I., Del Tacca, M., & Conte, P. F. (1995). Suramin in patients with metastatic colorectal cancer pretreated with fluoropyrimidine-based chemotherapy. A phase II study. Cancer, 75(2), 440-443.
31. Shah, S., Fourgeaud, C., Derieux, S., Mirshahi, S., Contant, G., Pimpie, C., Mirshahi, M. (2018). The close relationship between heparanase and epithelial mesenchymal transition in gastric signet-ring cell adenocarcinoma. Oncotarget, 9(73), 33778.
32. Bhargava, S., Hotz, B., Hines, O. J., Reber, H. A., Buhr, H. J., & Hotz, H. G. (2007). Suramin inhibits not only tumor growth and metastasis but also angiogenesis in experimental pancreatic cancer. J Gastrointest Surg, 11(2), 171-178.
33. Wade, T. P., Kasid, A., Stein, C. A., LaRocca, R. V., Sargent, E. R., Gomella, L. G., Linehan, W. M. (1992). Suramin interference with transforming growth factor-beta inhibition of human renal cell carcinoma in culture. J Surg Res, 53(2), 195-198.
34. Shin, R., Naomoto, Y., Kamikawa, Y., Tanaka, N., & Orita, K. (1997). Effect of suramin on human esophageal cancer cells in vitro and in vivo. [Comparative Study]. Scand J Gastroenterol, 32(8), 824-828.
35. Gansler, T., Vaghmar, N., Olson, J. J., & Graham, S. D. (1992). Suramin inhibits growth factor binding and proliferation by urothelial carcinoma cell cultures. J Urol, 148(3), 910-914.
36. Hensey, C. E., Boscoboinik, D., & Azzi, A. (1989). Suramin, an anti-cancer drug, inhibits protein kinase C and induces differentiation in neuroblastoma cell clone NB2A. [Research Support, Non-U.S. Gov't]. FEBS Lett, 258(1), 156-158.
37. Eisenberger, M. A., Reyno, L. M., Jodrell, D. I., Sinibaldi, V. J., Tkaczuk, K. H., Sridhara, R., & Egorin, M. J. (1993). Suramin, an active drug for prostate cancer: interim observations in a phase I trial. JNCI: Journal of the National Cancer Institute, 85(8), 611-621.
38. Li, J., Pan, Q., Rowan, P. D., Trotter, T. N., Peker, D., Regal, K. M., & Yang, Y. (2016). Heparanase promotes myeloma progression by inducing mesenchymal features and motility of myeloma cells. Oncotarget, 7(10), 11299.
39. Senthilraja, P., & Kathiresan, K. (2015). In vitro cytotoxicity MTT assay in Vero, HepG2 and MCF-7 cell lines study of Marine Yeast. J Appl Pharm Sci, 5(3), 080-084.
40. Masola, V., Bellin, G., Gambaro, G., & Onisto, M. (2018). Heparanase: A multitasking protein involved in extracellular matrix (ECM) remodeling and intracellular events. Cells, 7(12), 236.
41. Jia, L., & Ma, S. (2016). Recent advances in the discovery of heparanase inhibitors as anti-cancer agents. European journal of medicinal chemistry, 121, 209-220.
42. Jayatilleke, K., Duivenvoorden, H., Parker, B., & Hulett, M. (2018). PO-220 Defining the role of heparanase in breast cancer progression using the PyMT-MMTV mouse model: BMJ Publishing Group Limited.
43. La Rocca, R. V., Meer, J., Gilliatt, R. W., Stein, C. A., Cassidy, J., Myers, C. E., & Dalakas, M. C. (1990). Suramin‐induced polyneuropathy. Neurology, 40(6), 954-954.
44. Kobayashi, K., Weiss, R. E., Vogelzang, N. J., Vokes, E. E., Janisch, L., & Ratain, M. J. (1996). Mineralocorticoid insufficiency due to suramin therapy. Cancer: Interdisciplinary International Journal of the American Cancer Society, 78(11), 2411-2420.
45. Figg, W. D., Cooper, M. R., Thibault, A., Headlee, D., Humphrey, J., Bergan, R. C.,& Sartor, O. (1994). Acute renal toxicity associated with suramin in the treatment of prostate cancer. Cancer, 74(5), 1612-1614.
46. Foekens, J. A., Sieuwerts, A. M., Stuurman‐Smeets, E. M., Dorssers, L. C., Berns, E. M., & Klijn, J. G. (1992). Pleiotropic actions of suramin on the proliferation of human breast‐cancer cells in vitro. International journal of cancer, 51(3), 439-444.
47. Vignon, F., Prebois, C., & Rochefort, H. (1992). Inhibition of breast cancer growth by suramin. JNCI: Journal of the National Cancer Institute, 84(1), 38-42.
48. Bao, B., Ahmad, A., Azmi, A. S., Ali, S., & Sarkar, F. H. (2013). Overview of cancer stem cells (CSCs) and mechanisms of their regulation: implications for cancer therapy. Current protocols in pharmacology, 61(1), 14-25.
49. Soltysova, A., Altanerova, V., & Altaner, C. (2005). Cancer stem cells. Neoplasma, 52(6), 435.
50. Borst, P., Evers, R., Kool, M., & Wijnholds, J. (2000). A family of drug transporters: the multidrug resistance-associated proteins. Journal of the National Cancer Institute, 92(16), 1295-1302.
51. Burger, H., Foekens, J. A., Look, M. P., Meijer-van Gelder, M. E., Klijn, J. G., Wiemer, E. A., Nooter, K. (2003). RNA expression of breast cancer resistance protein, lung resistance-related protein, multidrug resistance-associated proteins 1 and 2, and multidrug resistance gene 1 in breast cancer: correlation with chemotherapeutic response. Clinical Cancer Research, 9(2), 827-836.
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Jan 4, 2024
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Mariam Davis, Sadia Rafique, Sidra Meer, Zunaira Afzal, Abdul Qader, Anum Asghar, & Muhammad Sajid Hamid Akash. (2024). EVALUATION OF NON-CYTOTOXIC DRUGS AS POTENTIAL CANDIDATES FOR BREAST CANCER. Journal of Population Therapeutics and Clinical Pharmacology, 31(1), 90–100. https://doi.org/10.53555/jptcp.v31i1.3810
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Author Biographies
Mariam Davis
Department of Pharmacology, Government College University, Faisalabad, Pakistan
Sadia Rafique
Department of Pharmacy, The University of Faisalabad, Faisalabad, Pakistan
Sidra Meer
Department of Pharmacy, New Indus institute of medical sciences, Mianwali, Pakistan
Zunaira Afzal
Department of Pharmacy, The University of Agriculture, Faisalabad, Pakistan
Abdul Qader
Primary and Secondary Health Care Department Government of Punjab Pakistan
Anum Asghar
Department of Pharmacy, Riphah International University, Faisalabad Campus, Faisalabad, Pakistan
Muhammad Sajid Hamid Akash
Department of Pharmaceutical Chemistry Government College University Faisalabad Pakistan