Research Article
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The effects of prochloraz on the levels of nuclear receptor genes expressions and global DNA methylation in human prostate carcinoma cells

Year 2021, Volume: 51 Issue: 2, 191 - 197, 31.08.2021

Abstract

Background and Aims: Prochloraz (PCZ) is an imidazole fungicide which is used in agriculture and gardening. PCZ, with endocrine disrupting effect, disrupts reproductive and developmental functions. Previously, the effects of PCZ on the estrogen and androgen receptors have been shown in vitro and in vivo. Because of endocrine disrupting effects, PCZ could influence nuclear receptors which acted as ER and AR antagonists. Besides, PCZ has been thought to have no genotoxic effects. Therefore, we aimed to investigate possible effects of PCZ on nuclear receptor genes and epigenetic mechanisms in human prostate carcinoma (PC-3) cells. Methods: In the present study, MTT and LDH tests were applied to evaluate the cell viability. Expression levels of nuclear receptor genes such as AhR, PXR, PPARα, PPARγ were studied on real-time quantitative PCR. For global DNA methylation analysis, the levels of 5-methylcytosine (5-mC%) were measured by elisa kit. Results: According to MTT and LDH test results, IC50 value of PCZ has been determined as 144.19 and 116.65 μM, respectively. There were significant changes for the expression levels of AhR, PPARα and PPARγ genes after 5-50 μM of PCZ treatments. 5 and 50 μM of PCZ decreased the levels of 5-mC% in the rates of 22.6% and 26.9%, respectively. Conclusion: It has been suggested that PCZ may cause alterations on the expressions of nuclear receptor genes which could be related to endocrine disrupting effects and may have implications on global DNA methylation.

Supporting Institution

Scientific Research Projects Coordination Unit of Istanbul University

Project Number

TLO-2017-23409; TLO-2017-27475

Thanks

This work was supported in part by the Scientific Research Projects Coordination Unit of Istanbul University (Project numbers: TLO-2017-23409; TLO-2017-27475) and TUBITAK-BIDEB (Project numbers: 2211-C/2015-2 Grant for Ecem Fatma Karaman).

References

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  • • Ahmadnejad, M., Amirizadeh, N., Mehrasa, R., Karkhah, A., Nikougoftar, M., & Oodi, A. (2017). Elevated expression of DNMT1 is associated with increased expansion and proliferation of hematopoietic stem cells co-cultured with human MSCs. Blood Research, 52(1), 25-30.
  • • Alley, M. C., Scudiere, D. A., Monks, A., Hursey, M. L., Czerwinski, M. J., Fine, D. L. … Boyd, M. R. (1988). Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay. Cancer Research, 48, 589-601.
  • • Alpertunga, B., Kara, M., Abudayyak, M., Oztas, E., Ozden, S., & Özhan, G. (2014). Effects of prochloraz on DNA damage, lipid peroxidation and antioxidant system in vitro. Toxicology Mechanisms and Methods, 24(4), 268-275.
  • • Andersen, H. R., Vinggaard, A. M., Rasmussen, T. H., Gjermandsen, I. M., & Bonefeld-Jørgensen, E. C. (2002). Effects of currently used pesticides in assays for estrogenicity, androgenicity and aromatase activity in vitro. Toxicology and Applied Pharmacology, 179, 1–12.
  • • Anderson, O. S., Sant, K. E., & Dolinoy, D. C. (2012). Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation. The Journal of Nutritional Biochemistry, 23(8), 853-859.
  • • Ayed-Boussema, I., Pascussi, J. M., Maurel, P., Bacha, H., & Hassen, W. (2011). Zearalenone activates pregnane X receptor, constitutive androstane receptor and aryl hydrocarbon receptor and corresponding phase I target genes mRNA in primary cultures of human hepatocytes. Environmental Toxicology and Pharmacology, 31(1), 79-87.
  • • Baylin, S. B. (1997). Tying it all together: epigenetics, genetics, cell cycle, and cancer. Science, 277(5334), 1948-1949.
  • • Bock, K. W., & Kohle, C. (2005). Ah receptor- and TCDD-mediated liver tumor promotion: clonal selection and expansion of cells evading growth arrest and apoptosis. Biochemical Pharmacology, 69(10), 1403–1408.
  • • Casati, L., Sendra, R., Sibilia, V., & Celotti, F. (2015). Endocrine disrupters: the new players able to affect the epigenome. Frontiers in Cell and Developmental Biology, 3, 37.
  • • Claeys, W. L., Schmit, J. F., Bragard, C., Maghuin-Rogister, G., Pussemier, L., & Schiffers, B. (2011). Exposure of several Belgian consumer groups to pesticide residues through fresh fruit and vegetable consumption. Food Control, 22, 508–16.
  • • Das, P. M., & Singal, R. (2004). DNA methylation and cancer. Journal of Clinical Oncology, 22(22), 4632-4642.
  • • Decker, T., & Lohmann-Matthes, M. L. (1988). A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. Journal of Immunological Methods, 115(1), 61-69.
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  • • Greally, J. M., & Jacobs, M. N. (2013). In vitro and in vivo testing methods of epigenomic endpoints for evaluating endocrine disruptors. Altex, 30(4), 445-71.
  • • Halwachs, S., Wassermann, L., Lindner, S., Zizzadoro, C., & Honscha, W. (2013). Fungicide prochloraz and environmental pollutant dioxin induce the ABCG2 transporter in bovine mammary epithelial cells by the arylhydrocarbon receptor signaling pathway. Toxicological Sciences, 131(2), 491-501.
  • • Harada, K., Isse, K., Kamihira, T., Shimoda, S., & Nakanuma, Y. (2005). Th1 cytokine–induced downregulation of PPARγ in human biliary cells relates to cholangitis in primary biliary cirrhosis. Hepatology, 41(6), 1329-1338.
  • • Heise, T., Schmidt, F., Knebel, C., Rieke, S., Haider, W., Geburek, I. … Marx-Stoelting, P. (2018). Hepatotoxic combination effects of three azole fungicides in a broad dose range. Archives of Toxicology, 92(2), 859-872.
  • • Heise, T., Schmidt, F., Knebel, C., Rieke, S., Haider, W., Pfeil, R. … Marx-Stoelting, P. (2015). Hepatotoxic effects of (tri) azole fungicides in a broad dose range. Archives of Toxicology, 89(11), 2105- 2117.
  • • Henry, M. J., & Sisler, H. D. (1984). Effects of sterol biosynthesisinhibiting (SBI) fungicides on cytochrome P-450 oxygenations in fungi. Pesticide Biochemistry and Physiology, 22, 262–275.
  • • JMPR (The Joint FAO/WHO Meeting of Pesticide Residues). (2001). Report of the Joint Meeting of the FAO Panel of Experts on Pesticide Residues in Food and the Environment and the WHO. Core Assessment Group on Pesticide Residues, Geneva, Switzerland, pp. 17e26. September 2001, Report 2001.
  • • Jones, P. A., & Baylin, S. B. (2007). The epigenomics of cancer. Cell, 128(4), 683-692.
  • • Karaman, E. F., & Ozden, S. (2019). Alterations in global DNA methylation and metabolism-related genes caused by zearalenone in MCF7 and MCF10F cells. Mycotoxin Research, 35(3), 309-320.
  • • Korzeniewski, C., & Callewaert, D. M. (1983). An enzyme-release assay for natural cytotoxicity. Journal of Immunological Methods, 64(3), 313-320.
  • • Kulis, M., & Esteller, M. (2010). DNA methylation and cancer. Advances in Genetics, 70(10), 27-56.
  • • Lai, J. C., Cheng, Y. W., Goan, Y. G., Chang, J. T., Wu, T. C., Chen, C. Y., & Lee, H. (2008). Promoter methylation of O 6-methylguanine- DNA-methyltransferase in lung cancer is regulated by p53. DNA Repair, 7(8), 1352-1363.
  • • Laier, P., Metzdorff, S. B., Borch, J., Hagen, M. L., Hass, U., Christiansen, S. … Vinggaard. A. M. (2006). Mechanisms of action underlying the antiandrogenic effects of the fungicide prochloraz. Toxicology and Applied Pharmacology, 213(2), 160-171.
  • • Laignelet, L., Riviere, J. L., & Lhuguenot, J. C. (1992). Metabolism of an imidazole fungicide (prochloraz) in the rat after oral administration. Food and Chemical Toxicology, 30, 575-583.
  • • Long, M., Laier, P., Vinggaard, A. M., Andersen, H. R., Lynggaard, J., & Bonefeld-Jørgensen, E. C. (2003). Effects of currently used pesticides in the AhR-CALUX assay: comparison between the human TV101L and the rat H4IIE cell line. Toxicology, 194(1-2), 77-93.
  • • Lundqvist, J., Hellman, B., & Oskarsson, A. (2016). Fungicide prochloraz induces oxidative stress and DNA damage in vitro. Food and Chemical Toxicology, 91, 36-41.
  • • Maqbool, F., Mostafalou, S., Bahadar, H., & Abdollahi, M. (2016). Review of endocrine disorders associated with environmental toxicants and possible involved mechanisms. Life Sciences, 145, 265-273.
  • • Marx-Stoelting, P., Ganzenberg, K., Knebel, C., Schmidt, F., Rieke, S., Hammer, H. ... Braeuning, A. (2017). Hepatotoxic effects of cyproconazole and prochloraz in wild-type and hCAR/hPXR mice. Archives of Toxicology, 91(8), 2895-2907.
  • • McIntosh, B. E., Hogenesch, J. B., & Bradfield, C. A. (2010). Mammalian Per-Arnt-Sim proteins in environmental adaptation. Annual Review of Physiology, 72, 625–645.
  • • Michalik, L., & Wahli, W. (2006). Involvement of PPAR nuclear receptors in tissue injury and wound repair. The Journal of Clinical Investigation, 116(3), 598-606.
  • • Moggs, J. G., Goodman, J. I., Trosko, J. E., & Roberts, R. A. (2004). Epigenetics and cancer: implications for drug discovery and safety assessment. Toxicology and Applied Pharmacology, 196(3), 422-430.
  • • 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.
  • • Ohlsson, Å., Ullerås, E., & Oskarsson, A. (2009). A biphasic effect of the fungicide prochloraz on aldosterone, but not cortisol, secretion in human adrenal H295R cellseunderlying mechanisms. Toxicology Letters, 191, 174-180.
  • • Olokpa, E., Bolden, A., & Stewart, L. V. (2016). The androgen receptor regulates PPARγ expression and activity in human prostate cancer cells. Journal of Cellular Physiology, 231, 2664–2672.
  • • Pathania, R., Ramachandran, S., Elangovan, S., Padia, R., Yang, P., Cinghu, S. … Thangaraju, M. (2015). DNMT1 is essential for mammary and cancer stem cell maintenance and tumorigenesis. Nature Communications, 6, 6910.
  • • Pradhan, S., Bacolla, A., Wells, R. D., & Roberts, R. J. (1999). Recombinant human DNA (cytosine-5) methyltransferase I. Expression, purification, and comparison of de novo and maintenance methylation. Journal of Biological Chemistry, 274(46), 33002-33010.
  • • Rieke, S., Koehn, S., Hirsch-Ernst, K., Pfeil, R., Kneuer, C., & Marx- Stoelting, P. (2014). Combination effects of (tri)azole fungicides on hormone production and xenobiotic metabolism in a human placental cell line. International Journal of Environmental Research and Public Health, 11(9), 9660-9679.
  • • Robitaille, C. N., Rivest, P., & Sanderson, J. T. (2015). Antiandrogenic mechanisms of pesticides in human LNCaP prostate and H295R adrenocortical carcinoma cells. Toxicological Sciences, 143(1), 126- 135.
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Year 2021, Volume: 51 Issue: 2, 191 - 197, 31.08.2021

Abstract

Project Number

TLO-2017-23409; TLO-2017-27475

References

  • • Ahmad, I., Mui, E., Galbraith, L., Patel, R., Tan, E. H., Salji, M., & Loveridge, C. (2016). Sleeping Beauty screen reveals Pparg activation in metastatic prostate cancer. Proceedings of the National Academy of Sciences, 113(29), 8290-8295.
  • • Ahmadnejad, M., Amirizadeh, N., Mehrasa, R., Karkhah, A., Nikougoftar, M., & Oodi, A. (2017). Elevated expression of DNMT1 is associated with increased expansion and proliferation of hematopoietic stem cells co-cultured with human MSCs. Blood Research, 52(1), 25-30.
  • • Alley, M. C., Scudiere, D. A., Monks, A., Hursey, M. L., Czerwinski, M. J., Fine, D. L. … Boyd, M. R. (1988). Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay. Cancer Research, 48, 589-601.
  • • Alpertunga, B., Kara, M., Abudayyak, M., Oztas, E., Ozden, S., & Özhan, G. (2014). Effects of prochloraz on DNA damage, lipid peroxidation and antioxidant system in vitro. Toxicology Mechanisms and Methods, 24(4), 268-275.
  • • Andersen, H. R., Vinggaard, A. M., Rasmussen, T. H., Gjermandsen, I. M., & Bonefeld-Jørgensen, E. C. (2002). Effects of currently used pesticides in assays for estrogenicity, androgenicity and aromatase activity in vitro. Toxicology and Applied Pharmacology, 179, 1–12.
  • • Anderson, O. S., Sant, K. E., & Dolinoy, D. C. (2012). Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation. The Journal of Nutritional Biochemistry, 23(8), 853-859.
  • • Ayed-Boussema, I., Pascussi, J. M., Maurel, P., Bacha, H., & Hassen, W. (2011). Zearalenone activates pregnane X receptor, constitutive androstane receptor and aryl hydrocarbon receptor and corresponding phase I target genes mRNA in primary cultures of human hepatocytes. Environmental Toxicology and Pharmacology, 31(1), 79-87.
  • • Baylin, S. B. (1997). Tying it all together: epigenetics, genetics, cell cycle, and cancer. Science, 277(5334), 1948-1949.
  • • Bock, K. W., & Kohle, C. (2005). Ah receptor- and TCDD-mediated liver tumor promotion: clonal selection and expansion of cells evading growth arrest and apoptosis. Biochemical Pharmacology, 69(10), 1403–1408.
  • • Casati, L., Sendra, R., Sibilia, V., & Celotti, F. (2015). Endocrine disrupters: the new players able to affect the epigenome. Frontiers in Cell and Developmental Biology, 3, 37.
  • • Claeys, W. L., Schmit, J. F., Bragard, C., Maghuin-Rogister, G., Pussemier, L., & Schiffers, B. (2011). Exposure of several Belgian consumer groups to pesticide residues through fresh fruit and vegetable consumption. Food Control, 22, 508–16.
  • • Das, P. M., & Singal, R. (2004). DNA methylation and cancer. Journal of Clinical Oncology, 22(22), 4632-4642.
  • • Decker, T., & Lohmann-Matthes, M. L. (1988). A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. Journal of Immunological Methods, 115(1), 61-69.
  • • Demirel, G., Alpertunga, B., & Ozden, S. (2015). Role of fumonisin B1 on DNA methylation changes in rat kidney and liver cells. Pharmaceutical Biology, 53(9), 1302-1310.
  • • Derosa, G., Sahebkar, A., & Maffioli, P. (2018). The role of various peroxisome proliferator‐activated receptors and their ligands in clinical practice. Journal of Cellular Physiology, 233(1), 153-161.
  • • EFSA (European Food Safety Authority). (2011). Conclusion on the peer review of the pesticide risk assessment of the active substance prochloraz. EFSA Journal, 9, 2323–443.
  • • Evans, B. R., Karchner, S. I., Allan, L. L., Pollenz, R. S., Tanguay, R. L., Jenny, M. J. … Hahn, M. E. (2008). Repression of aryl hydrocarbon receptor (AHR) signaling by AHR repressor: Role of DNA binding and competition for AHR nuclear translocator. Molecular Pharmacology, 73, 387–398.
  • • Gama-Sosa, M. A., Slagel, V. A., Trewyn, R. W., Oxenhandler, R., Kuo, K. C., Gehrke, C. W., & Ehrlich, M. (1983). The 5-methylcytosine content of DNA from human tumors. Nucleic Acids Research, 11(19), 6883-6894.
  • • Goettel, M., Melching-Kollmuss, S., Honarvar, N., Marxfeld, H., Elcombe, C. R., & Fegert, I. (2015). Mouse liver tumors induced by prochloraz have a CAR-like mode of action and are not relevant to humans. Toxicological Sciences, 144(1), 351.
  • • Greally, J. M., & Jacobs, M. N. (2013). In vitro and in vivo testing methods of epigenomic endpoints for evaluating endocrine disruptors. Altex, 30(4), 445-71.
  • • Halwachs, S., Wassermann, L., Lindner, S., Zizzadoro, C., & Honscha, W. (2013). Fungicide prochloraz and environmental pollutant dioxin induce the ABCG2 transporter in bovine mammary epithelial cells by the arylhydrocarbon receptor signaling pathway. Toxicological Sciences, 131(2), 491-501.
  • • Harada, K., Isse, K., Kamihira, T., Shimoda, S., & Nakanuma, Y. (2005). Th1 cytokine–induced downregulation of PPARγ in human biliary cells relates to cholangitis in primary biliary cirrhosis. Hepatology, 41(6), 1329-1338.
  • • Heise, T., Schmidt, F., Knebel, C., Rieke, S., Haider, W., Geburek, I. … Marx-Stoelting, P. (2018). Hepatotoxic combination effects of three azole fungicides in a broad dose range. Archives of Toxicology, 92(2), 859-872.
  • • Heise, T., Schmidt, F., Knebel, C., Rieke, S., Haider, W., Pfeil, R. … Marx-Stoelting, P. (2015). Hepatotoxic effects of (tri) azole fungicides in a broad dose range. Archives of Toxicology, 89(11), 2105- 2117.
  • • Henry, M. J., & Sisler, H. D. (1984). Effects of sterol biosynthesisinhibiting (SBI) fungicides on cytochrome P-450 oxygenations in fungi. Pesticide Biochemistry and Physiology, 22, 262–275.
  • • JMPR (The Joint FAO/WHO Meeting of Pesticide Residues). (2001). Report of the Joint Meeting of the FAO Panel of Experts on Pesticide Residues in Food and the Environment and the WHO. Core Assessment Group on Pesticide Residues, Geneva, Switzerland, pp. 17e26. September 2001, Report 2001.
  • • Jones, P. A., & Baylin, S. B. (2007). The epigenomics of cancer. Cell, 128(4), 683-692.
  • • Karaman, E. F., & Ozden, S. (2019). Alterations in global DNA methylation and metabolism-related genes caused by zearalenone in MCF7 and MCF10F cells. Mycotoxin Research, 35(3), 309-320.
  • • Korzeniewski, C., & Callewaert, D. M. (1983). An enzyme-release assay for natural cytotoxicity. Journal of Immunological Methods, 64(3), 313-320.
  • • Kulis, M., & Esteller, M. (2010). DNA methylation and cancer. Advances in Genetics, 70(10), 27-56.
  • • Lai, J. C., Cheng, Y. W., Goan, Y. G., Chang, J. T., Wu, T. C., Chen, C. Y., & Lee, H. (2008). Promoter methylation of O 6-methylguanine- DNA-methyltransferase in lung cancer is regulated by p53. DNA Repair, 7(8), 1352-1363.
  • • Laier, P., Metzdorff, S. B., Borch, J., Hagen, M. L., Hass, U., Christiansen, S. … Vinggaard. A. M. (2006). Mechanisms of action underlying the antiandrogenic effects of the fungicide prochloraz. Toxicology and Applied Pharmacology, 213(2), 160-171.
  • • Laignelet, L., Riviere, J. L., & Lhuguenot, J. C. (1992). Metabolism of an imidazole fungicide (prochloraz) in the rat after oral administration. Food and Chemical Toxicology, 30, 575-583.
  • • Long, M., Laier, P., Vinggaard, A. M., Andersen, H. R., Lynggaard, J., & Bonefeld-Jørgensen, E. C. (2003). Effects of currently used pesticides in the AhR-CALUX assay: comparison between the human TV101L and the rat H4IIE cell line. Toxicology, 194(1-2), 77-93.
  • • Lundqvist, J., Hellman, B., & Oskarsson, A. (2016). Fungicide prochloraz induces oxidative stress and DNA damage in vitro. Food and Chemical Toxicology, 91, 36-41.
  • • Maqbool, F., Mostafalou, S., Bahadar, H., & Abdollahi, M. (2016). Review of endocrine disorders associated with environmental toxicants and possible involved mechanisms. Life Sciences, 145, 265-273.
  • • Marx-Stoelting, P., Ganzenberg, K., Knebel, C., Schmidt, F., Rieke, S., Hammer, H. ... Braeuning, A. (2017). Hepatotoxic effects of cyproconazole and prochloraz in wild-type and hCAR/hPXR mice. Archives of Toxicology, 91(8), 2895-2907.
  • • McIntosh, B. E., Hogenesch, J. B., & Bradfield, C. A. (2010). Mammalian Per-Arnt-Sim proteins in environmental adaptation. Annual Review of Physiology, 72, 625–645.
  • • Michalik, L., & Wahli, W. (2006). Involvement of PPAR nuclear receptors in tissue injury and wound repair. The Journal of Clinical Investigation, 116(3), 598-606.
  • • Moggs, J. G., Goodman, J. I., Trosko, J. E., & Roberts, R. A. (2004). Epigenetics and cancer: implications for drug discovery and safety assessment. Toxicology and Applied Pharmacology, 196(3), 422-430.
  • • 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.
  • • Ohlsson, Å., Ullerås, E., & Oskarsson, A. (2009). A biphasic effect of the fungicide prochloraz on aldosterone, but not cortisol, secretion in human adrenal H295R cellseunderlying mechanisms. Toxicology Letters, 191, 174-180.
  • • Olokpa, E., Bolden, A., & Stewart, L. V. (2016). The androgen receptor regulates PPARγ expression and activity in human prostate cancer cells. Journal of Cellular Physiology, 231, 2664–2672.
  • • Pathania, R., Ramachandran, S., Elangovan, S., Padia, R., Yang, P., Cinghu, S. … Thangaraju, M. (2015). DNMT1 is essential for mammary and cancer stem cell maintenance and tumorigenesis. Nature Communications, 6, 6910.
  • • Pradhan, S., Bacolla, A., Wells, R. D., & Roberts, R. J. (1999). Recombinant human DNA (cytosine-5) methyltransferase I. Expression, purification, and comparison of de novo and maintenance methylation. Journal of Biological Chemistry, 274(46), 33002-33010.
  • • Rieke, S., Koehn, S., Hirsch-Ernst, K., Pfeil, R., Kneuer, C., & Marx- Stoelting, P. (2014). Combination effects of (tri)azole fungicides on hormone production and xenobiotic metabolism in a human placental cell line. International Journal of Environmental Research and Public Health, 11(9), 9660-9679.
  • • Robitaille, C. N., Rivest, P., & Sanderson, J. T. (2015). Antiandrogenic mechanisms of pesticides in human LNCaP prostate and H295R adrenocortical carcinoma cells. Toxicological Sciences, 143(1), 126- 135.
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There are 60 citations in total.

Details

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

Ecem Fatma Karaman 0000-0002-1504-4546

Esma Doğan 0000-0002-0613-7433

Dilara Alga 0000-0002-2693-6080

Sibel Özden 0000-0002-1662-2504

Project Number TLO-2017-23409; TLO-2017-27475
Publication Date August 31, 2021
Submission Date January 11, 2021
Published in Issue Year 2021 Volume: 51 Issue: 2

Cite

APA Karaman, E. F., Doğan, E., Alga, D., Özden, S. (2021). The effects of prochloraz on the levels of nuclear receptor genes expressions and global DNA methylation in human prostate carcinoma cells. İstanbul Journal of Pharmacy, 51(2), 191-197.
AMA Karaman EF, Doğan E, Alga D, Özden S. The effects of prochloraz on the levels of nuclear receptor genes expressions and global DNA methylation in human prostate carcinoma cells. iujp. August 2021;51(2):191-197.
Chicago Karaman, Ecem Fatma, Esma Doğan, Dilara Alga, and Sibel Özden. “The Effects of Prochloraz on the Levels of Nuclear Receptor Genes Expressions and Global DNA Methylation in Human Prostate Carcinoma Cells”. İstanbul Journal of Pharmacy 51, no. 2 (August 2021): 191-97.
EndNote Karaman EF, Doğan E, Alga D, Özden S (August 1, 2021) The effects of prochloraz on the levels of nuclear receptor genes expressions and global DNA methylation in human prostate carcinoma cells. İstanbul Journal of Pharmacy 51 2 191–197.
IEEE E. F. Karaman, E. Doğan, D. Alga, and S. Özden, “The effects of prochloraz on the levels of nuclear receptor genes expressions and global DNA methylation in human prostate carcinoma cells”, iujp, vol. 51, no. 2, pp. 191–197, 2021.
ISNAD Karaman, Ecem Fatma et al. “The Effects of Prochloraz on the Levels of Nuclear Receptor Genes Expressions and Global DNA Methylation in Human Prostate Carcinoma Cells”. İstanbul Journal of Pharmacy 51/2 (August 2021), 191-197.
JAMA Karaman EF, Doğan E, Alga D, Özden S. The effects of prochloraz on the levels of nuclear receptor genes expressions and global DNA methylation in human prostate carcinoma cells. iujp. 2021;51:191–197.
MLA Karaman, Ecem Fatma et al. “The Effects of Prochloraz on the Levels of Nuclear Receptor Genes Expressions and Global DNA Methylation in Human Prostate Carcinoma Cells”. İstanbul Journal of Pharmacy, vol. 51, no. 2, 2021, pp. 191-7.
Vancouver Karaman EF, Doğan E, Alga D, Özden S. The effects of prochloraz on the levels of nuclear receptor genes expressions and global DNA methylation in human prostate carcinoma cells. iujp. 2021;51(2):191-7.