Research Article
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Curcumin synergistically augments the chemotherapeutic activity of Doxorubicin in prostate cancer cells

Year 2024, Volume: 15 Issue: 51, 10 - 19, 29.04.2024
https://doi.org/10.17944/interdiscip.1297112

Abstract

Objective
Prostate cancer is one of the most commonly diagnosed cancer types in men and many people die every year due to recurring or acquiring aggressive forms of prostate cancer. Numerous chemotherapeutics such as paclitaxel and doxorubicin are commonly used in the treatment of prostate cancer. However, acquired resistance to chemotherapeutics and broad systemic side effects substantially limit their efficacy. Curcumin is one of the most examined phytochemicals of the herbal remedy turmeric. Herein, we aimed to investigate the synergistic capability of curcumin on doxorubicin in prostate cancer cells.
Method
The human adenocarcinoma cell line LNCaP was used in cell culture studies. Cell viability was examined by WST-1 assay. The protein expression levels of Beclin1, p62/SQSTM1, LC3-I/II, Hrd1, gp78, polyubiquitin, PERK, eIF2, phospho-(Ser51) eIF2, IRE1, XBP-1s, PARP-1, caspase-3, AR, PSA, c-Myc, E-cadherin, N-cadherin and VEGF-A were investigated by immunoblotting assay.
Results
Our data indicated that co-administration of curcumin with doxorubicin significantly improved the cytotoxic effect of doxorubicin in LNCaP cells. Also, the combination of curcumin and doxorubicin reduced the autophagic flux and remarkably induced endoplasmic reticulum-associated-degradation (ERAD) and unfolded protein response (UPR) signaling. Also, activation of apoptotic proteins PARP-1 and caspase-3 were strongly enhanced by combined treatment in a dose-dependent manner. Moreover, combined treatment markedly decreased AR, PSA, c-Myc and VEGF-A levels. Additionally, the epithelial-mesenchymal transition (EMT) was reduced by decreasing N-cadherin and increasing E-cadherin protein levels.
Conclusion
Present data strongly suggest that curcumin synergistically improves the anti-cancer features of doxorubicin in prostate cancer cells.

Supporting Institution

Suleyman Demirel University

Project Number

TSG-2021-8302, TAB-2020-8253

References

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  • Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, Chi KN, et al. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N Engl J Med 2004;351:1502–1512. https://doi.org/10.1056/NEJMoa040720
  • Deserti M, Tavolari S, Naldi M, Frega G, Brandi G. Antitumoral Efficacy of Two Turmeric Extracts According to Different Extraction Methods in Hepatocellular Carcinoma Cell Lines. Med Aromat Plants 2018;7:6.
  • Oliveira AC, Miyagawa LM, Monteiro KM, Dias AL, Longato GB, Spindola H, et al. Phenolic composition, antiproliferative and antiulcerogenic activities of a polyphenol‐rich purified extract from açai ( Euterpe oleracea ) fruits. Int J Food Sci Technol 2021;56:6626–6634
  • Ravindran J, Prasad S, Aggarwal BB. Curcumin and cancer cells: how many ways can curry kill tumor cells selectively? AAPS J 2009;11:495–510. https://doi.org/10.1208/s12248-009-9128-x
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  • Jordan BC, Mock CD, Thilagavathi R, Selvam C. Molecular mechanisms of curcumin and its semisynthetic analogues in prostate cancer prevention and treatment. Life Sci 2016;152:135–144. https://doi.org/10.1016/j.lfs.2016.03.036
  • Teiten M-H, Gaascht F, Cronauer M, Henry E, Dicato M, Diederich M. Anti-proliferative potential of curcumin in androgen-dependent prostate cancer cells occurs through modulation of the Wingless signaling pathway. Int J Oncol 2011;38:603–611. https://doi.org/10.3892/ijo.2011.905
  • Ak KA, Uzunhisarcıklı E, Yerer MB, Bishayee A. The golden spice curcumin in cancer: A perspective on finalized clinical trials during the last 10 years. J Cancer Res Ther 2022;18(1):19-26. https://doi.org/10.4103/jcrt.JCRT_1017_20
  • Verma SP, Goldin BR, Lin PS. The inhibition of the estrogenic effects of pesticides and environmental chemicals by curcumin and isoflavonoids. Environmental Health Perspectives 1998;106:807–812. https://doi.org/10.1289/ehp.106-1533252
  • Bharti AC, Donato N, Singh S, Aggarwal BB. Curcumin (diferuloylmethane) down-regulates the constitutive activation of nuclear factor-kappa B and IkappaBalpha kinase in human multiple myeloma cells, leading to suppression of proliferation and induction of apoptosis. Blood 2003;101:1053–1062. https://doi.org/10.1182/blood-2002-05-1320
  • Harbottle A, Daly AK, Atherton K, Campbell FC. Role of glutathione S-transferase P1, P-glycoprotein and multidrug resistance-associated protein 1 in acquired doxorubicin resistance. Int J Cancer 2001;92:777–783. https://doi.org/10.1002/ijc.1283
  • Hernández DE, Pérez JR. Advanced epidemic Kaposi’s sarcoma: treatment with bleomycin or combination of doxorubicin, bleomycin, and vincristine. Int J Dermatol 1996;35(11):831–3. https://doi.org/10.1111/j.1365-4362.1996.tb02990.x
  • Itoh K, Sasaki Y, Fujii H, Minami H, Ohtsu T, Wakita H, et al. Study of dose escalation and sequence switching of administration of the combination of docetaxel and doxorubicin in advanced breast cancer. Clin Cancer Res 2000;6(10):4082–90.
  • Martin M, Villar A, Sole-Calvo A, Gonzalez R, Massuti B, Lizon J, et al. Doxorubicin in combination with fluorouracil and cyclophosphamide (i.v. FAC regimen, day 1, 21) versus methotrexate in combination with fluorouracil and cyclophosphamide (i.v. CMF regimen, day 1, 21) as adjuvant chemotherapy for operable breast cancer: a study by the GEICAM group. Ann Oncol 2003;14(6):833–42. https://doi.org/10.1093/annonc/mdg260
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  • Yoshii SR, Mizushima N. Monitoring and Measuring Autophagy. Int J Mol Sci 2017;18(9):1865. https://doi.org/10.3390/ijms18091865
  • Tran S, Douglas Fairlie W, Lee EF. BECLIN1: Protein Structure, Function and Regulation. Cells 2021;10(6):1522. https://doi.org/10.3390/cells10061522
  • Bjørkøy G, Lamark T, Pankiv S, Øvervatn A, Brech A, Johansen T. Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol 2009;452:181-97. https://doi.org/10.1016/S0076-6879(08)03612-4
  • Tanida I, Ueno T, Kominami E. LC3 and Autophagy. Methods Mol Biol 2008;445:77-88. https://doi.org/10.1007/978-1-59745-157-4_4
  • Hwang J, Qi L. Quality Control in the Endoplasmic Reticulum: Crosstalk between ERAD and UPR pathways. Trends Biochem Sci 2018;43:593–605. https://doi.org/10.1016/j.tibs.2018.06.005
  • Braakman I, Hebert DN. Protein folding in the endoplasmic reticulum. Cold Spring Harb Perspect Biol 2013;5(5):a013201. https://doi.org/10.1101/cshperspect.a013201
  • Erzurumlu Y, Ballar P. Androgen Mediated Regulation of Endoplasmic Reticulum-Associated Degradation and its Effects on Prostate Cancer. Sci Rep 2017;7:1–12. https://doi.org/10.1038/srep40719
  • Storm M, Sheng X, Arnoldussen YJ, Saatcioglu F. Prostate cancer and the unfolded protein response. Oncotarget 2016;7:54051–54066. https://doi.org/10.18632/oncotarget.9912
  • Clarke R, Cook KL. Unfolding the role of stress response signaling in endocrine resistant breast cancers. Front Oncol 2015;5:140. https://doi.org/10.3389/fonc.2015.00140
  • Hetz C, Chevet E, Oakes SA. Proteostasis control by the unfolded protein response. Nat Cell Biol 2015;17:829. https://doi.org/10.1038/ncb3184
  • Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 2003;11:381–389. https://doi.org/10.1038/sj.cdd.4401373
  • Shi Y. Mechanisms of caspase activation and inhibition during apoptosis. Mol Cell 2002;9:459–470. https://doi.org/10.1016/s1097-2765(02)00482-3
  • Fernandes-Alnemri T, Litwack G, Alnemri ES. CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1 beta-converting enzyme. J Biol Chem 1994;269:30761–30764.
  • Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, et al. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995;376:37–43. https://doi.org/10.1038/376037a0
  • Tewari M, Quan LT, O’Rourke K, Desnoyers S, Zeng Z, Beidler DR, et al. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 1995;81:801–809. https://doi.org/10.1016/0092-8674(95)90541-3
  • Dai C, Heemers H, Sharifi N. Androgen Signaling in Prostate Cancer. Cold Spring Harb Perspect Med 2017;7(9):a030452. https://doi.org/10.1101/cshperspect.a030452
  • Bai S, Cao S, Jin L, Kobelski M, Schouest B, Wang X, et al. A positive role of c-Myc in regulating androgen receptor and its splice variants in prostate cancer. Oncogene 2019;38:4977–4989. https://doi.org/10.1038/s41388-019-0768-8
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  • Chen F-Z, Zhao X-K. Prostate Cancer: Current Treatment and Prevention Strategies. Iran Red Crescent Med J 2013;15:279–284. https://doi.org/10.5812/ircmj.6499
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Year 2024, Volume: 15 Issue: 51, 10 - 19, 29.04.2024
https://doi.org/10.17944/interdiscip.1297112

Abstract

Project Number

TSG-2021-8302, TAB-2020-8253

References

  • Siegel RL, Miller KD, Wagle NS, Jemal A. Cancer statistics. CA Cancer J. Clin. 2023; 73:17-48. https://doi.org/10.3322/caac.21763
  • Lawrentschuk N, Trottier G, Kuk C, Zlotta AR. Role of Surgery in High-Risk Localized Prostate Cancer. Current Oncology 2010;17:25–32. https://doi.org/10.3747/co.v17i0.705
  • Ramsay AK, Leung HY. Signalling pathways in prostate carcinogenesis: potentials for molecular-targeted therapy. Clin Sci 2009;117:209–228. https://doi.org/10.1042/CS20080391
  • Huggins C, Hodges CV. Studies on prostatic cancer: I. The effect of castration, of estrogen and of androgen injection on serum phosphatases in metastatic carcinoma of the prostate. 1941. J Urol 2002;168:9–12. https://doi.org/10.1016/s0022-5347(05)64820-3
  • Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, Chi KN, et al. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N Engl J Med 2004;351:1502–1512. https://doi.org/10.1056/NEJMoa040720
  • Deserti M, Tavolari S, Naldi M, Frega G, Brandi G. Antitumoral Efficacy of Two Turmeric Extracts According to Different Extraction Methods in Hepatocellular Carcinoma Cell Lines. Med Aromat Plants 2018;7:6.
  • Oliveira AC, Miyagawa LM, Monteiro KM, Dias AL, Longato GB, Spindola H, et al. Phenolic composition, antiproliferative and antiulcerogenic activities of a polyphenol‐rich purified extract from açai ( Euterpe oleracea ) fruits. Int J Food Sci Technol 2021;56:6626–6634
  • Ravindran J, Prasad S, Aggarwal BB. Curcumin and cancer cells: how many ways can curry kill tumor cells selectively? AAPS J 2009;11:495–510. https://doi.org/10.1208/s12248-009-9128-x
  • Schmidt KT, Figg WD. The potential role of curcumin in prostate cancer: the importance of optimizing pharmacokinetics in clinical studies. Transl Cancer Res 2016;5(6): S1107-S1110. https://doi.org/10.21037/tcr.2016.11.04
  • Abd Wahab NA, Lajis NH, Abas F, Othman I, Naidu R. Mechanism of Anti-Cancer Activity of Curcumin on Androgen-Dependent and Androgen-Independent Prostate Cancer. Nutrients. 2020;12(3):679. https://doi.org/10.3390/nu12030679
  • Mukhopadhyay A, Bueso-Ramos C, Chatterjee D, Pantazis P, Aggarwal BB. Curcumin downregulates cell survival mechanisms in human prostate cancer cell lines. Oncogene 2001;20:7597–7609. https://doi.org/10.1038/sj.onc.1204997
  • Tan BL, Norhaizan ME. Curcumin Combination Chemotherapy: The Implication and Efficacy in Cancer. Molecules 2019;24(14):2527. https://doi.org/10.3390/molecules24142527
  • Gewirtz DA. A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem Pharmacol 1999;57:727–741. https://doi.org/10.1016/s0006-2952(98)00307-4
  • Wagner H. Synergy research: approaching a new generation of phytopharmaceuticals. Fitoterapia 2011;82:34–37. https://doi.org/10.1016/j.fitote.2010.11.016
  • Klippstein R, Bansal SS, Al-Jamal KT. Doxorubicin enhances curcumin’s cytotoxicity in human prostate cancer cells in vitro by enhancing its cellular uptake. Int J Pharm 2016;514(1):169–75. https://doi.org/10.1016/j.ijpharm.2016.08.003
  • Soldani C, Lazzè MC, Bottone MG, Tognon G, Biggiogera M, Pellicciari CE, et al. Poly(ADP-ribose) Polymerase Cleavage during Apoptosis: When and Where? Experimental Cell Research 2001;269:193–201. https://doi.org/10.1006/excr.2001.5293
  • Florea A-M, Büsselberg D. Cisplatin as an anti-tumor drug: cellular mechanisms of activity, drug resistance and induced side effects. Cancers 2011;3:1351–1371. https://doi.org/10.3390/cancers3011351
  • Yu H, Chen L, Qiu Y, Yang S-F. The Fate of Cancer: Focusing on Pure Compounds Derived From Traditional Chinese Medicine. Frontiers Media SA. 2022.
  • Dehelean CA, Marcovici I, Soica C, Mioc M, Coricovac D, Iurciuc S, et al. Plant-Derived Anticancer Compounds as New Perspectives in Drug Discovery and Alternative Therapy. Molecules 2021;26(4):1109. https://doi.org/10.3390/molecules26041109
  • Amalraj A, Pius A, Gopi S, Gopi S. Biological activities of curcuminoids, other biomolecules from turmeric and their derivatives – A review. Afr J Tradit Complement Altern Med 2017;7(2):205-233. https://doi.org/10.1016/j.jtcme.2016.05.005
  • Jordan BC, Mock CD, Thilagavathi R, Selvam C. Molecular mechanisms of curcumin and its semisynthetic analogues in prostate cancer prevention and treatment. Life Sci 2016;152:135–144. https://doi.org/10.1016/j.lfs.2016.03.036
  • Teiten M-H, Gaascht F, Cronauer M, Henry E, Dicato M, Diederich M. Anti-proliferative potential of curcumin in androgen-dependent prostate cancer cells occurs through modulation of the Wingless signaling pathway. Int J Oncol 2011;38:603–611. https://doi.org/10.3892/ijo.2011.905
  • Ak KA, Uzunhisarcıklı E, Yerer MB, Bishayee A. The golden spice curcumin in cancer: A perspective on finalized clinical trials during the last 10 years. J Cancer Res Ther 2022;18(1):19-26. https://doi.org/10.4103/jcrt.JCRT_1017_20
  • Verma SP, Goldin BR, Lin PS. The inhibition of the estrogenic effects of pesticides and environmental chemicals by curcumin and isoflavonoids. Environmental Health Perspectives 1998;106:807–812. https://doi.org/10.1289/ehp.106-1533252
  • Bharti AC, Donato N, Singh S, Aggarwal BB. Curcumin (diferuloylmethane) down-regulates the constitutive activation of nuclear factor-kappa B and IkappaBalpha kinase in human multiple myeloma cells, leading to suppression of proliferation and induction of apoptosis. Blood 2003;101:1053–1062. https://doi.org/10.1182/blood-2002-05-1320
  • Harbottle A, Daly AK, Atherton K, Campbell FC. Role of glutathione S-transferase P1, P-glycoprotein and multidrug resistance-associated protein 1 in acquired doxorubicin resistance. Int J Cancer 2001;92:777–783. https://doi.org/10.1002/ijc.1283
  • Hernández DE, Pérez JR. Advanced epidemic Kaposi’s sarcoma: treatment with bleomycin or combination of doxorubicin, bleomycin, and vincristine. Int J Dermatol 1996;35(11):831–3. https://doi.org/10.1111/j.1365-4362.1996.tb02990.x
  • Itoh K, Sasaki Y, Fujii H, Minami H, Ohtsu T, Wakita H, et al. Study of dose escalation and sequence switching of administration of the combination of docetaxel and doxorubicin in advanced breast cancer. Clin Cancer Res 2000;6(10):4082–90.
  • Martin M, Villar A, Sole-Calvo A, Gonzalez R, Massuti B, Lizon J, et al. Doxorubicin in combination with fluorouracil and cyclophosphamide (i.v. FAC regimen, day 1, 21) versus methotrexate in combination with fluorouracil and cyclophosphamide (i.v. CMF regimen, day 1, 21) as adjuvant chemotherapy for operable breast cancer: a study by the GEICAM group. Ann Oncol 2003;14(6):833–42. https://doi.org/10.1093/annonc/mdg260
  • Sadzuka Y, Nagamine M, Toyooka T, Ibuki Y, Sonobe T. Beneficial effects of curcumin on antitumor activity and adverse reactions of doxorubicin. Int J Pharm 2012;432(1-2):42–9. https://doi.org/10.1016/j.ijpharm.2012.04.062
  • Yun CW, Lee SH. The Roles of Autophagy in Cancer. Int J Mol Sci 2018;19:3466. https://doi.org/10.3390/ijms19113466
  • Badadani M. Autophagy Mechanism, Regulation, Functions, and Disorders. ISRN Cell Biology 2012;2012:1-11.
  • Yoshii SR, Mizushima N. Monitoring and Measuring Autophagy. Int J Mol Sci 2017;18(9):1865. https://doi.org/10.3390/ijms18091865
  • Tran S, Douglas Fairlie W, Lee EF. BECLIN1: Protein Structure, Function and Regulation. Cells 2021;10(6):1522. https://doi.org/10.3390/cells10061522
  • Bjørkøy G, Lamark T, Pankiv S, Øvervatn A, Brech A, Johansen T. Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol 2009;452:181-97. https://doi.org/10.1016/S0076-6879(08)03612-4
  • Tanida I, Ueno T, Kominami E. LC3 and Autophagy. Methods Mol Biol 2008;445:77-88. https://doi.org/10.1007/978-1-59745-157-4_4
  • Hwang J, Qi L. Quality Control in the Endoplasmic Reticulum: Crosstalk between ERAD and UPR pathways. Trends Biochem Sci 2018;43:593–605. https://doi.org/10.1016/j.tibs.2018.06.005
  • Braakman I, Hebert DN. Protein folding in the endoplasmic reticulum. Cold Spring Harb Perspect Biol 2013;5(5):a013201. https://doi.org/10.1101/cshperspect.a013201
  • Erzurumlu Y, Ballar P. Androgen Mediated Regulation of Endoplasmic Reticulum-Associated Degradation and its Effects on Prostate Cancer. Sci Rep 2017;7:1–12. https://doi.org/10.1038/srep40719
  • Storm M, Sheng X, Arnoldussen YJ, Saatcioglu F. Prostate cancer and the unfolded protein response. Oncotarget 2016;7:54051–54066. https://doi.org/10.18632/oncotarget.9912
  • Clarke R, Cook KL. Unfolding the role of stress response signaling in endocrine resistant breast cancers. Front Oncol 2015;5:140. https://doi.org/10.3389/fonc.2015.00140
  • Hetz C, Chevet E, Oakes SA. Proteostasis control by the unfolded protein response. Nat Cell Biol 2015;17:829. https://doi.org/10.1038/ncb3184
  • Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 2003;11:381–389. https://doi.org/10.1038/sj.cdd.4401373
  • Shi Y. Mechanisms of caspase activation and inhibition during apoptosis. Mol Cell 2002;9:459–470. https://doi.org/10.1016/s1097-2765(02)00482-3
  • Fernandes-Alnemri T, Litwack G, Alnemri ES. CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1 beta-converting enzyme. J Biol Chem 1994;269:30761–30764.
  • Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, et al. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995;376:37–43. https://doi.org/10.1038/376037a0
  • Tewari M, Quan LT, O’Rourke K, Desnoyers S, Zeng Z, Beidler DR, et al. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 1995;81:801–809. https://doi.org/10.1016/0092-8674(95)90541-3
  • Dai C, Heemers H, Sharifi N. Androgen Signaling in Prostate Cancer. Cold Spring Harb Perspect Med 2017;7(9):a030452. https://doi.org/10.1101/cshperspect.a030452
  • Bai S, Cao S, Jin L, Kobelski M, Schouest B, Wang X, et al. A positive role of c-Myc in regulating androgen receptor and its splice variants in prostate cancer. Oncogene 2019;38:4977–4989. https://doi.org/10.1038/s41388-019-0768-8
  • Carmeliet P. VEGF as a key mediator of angiogenesis in cancer. Oncology 2005;69(3): 4-10. https://doi.org/10.1159/000088478
  • Loh C-Y, Chai JY, Tang TF, Wong WF, Sethi G, Shanmugam MK, et al. The E-Cadherin and N-Cadherin Switch in Epithelial-to-Mesenchymal Transition: Signaling, Therapeutic Implications, and Challenges. Cells 2019;8(10):1118. https://doi.org/10.3390/cells8101118
  • Siegel RL, Miller KD, Fedewa SA, Ahnen DJ, Meester RGS, Barzi A, et al. Colorectal cancer statistics, 2017. CA Cancer J Clin 2017;67:177–193. https://doi.org/10.3322/caac.21395
  • Chen F-Z, Zhao X-K. Prostate Cancer: Current Treatment and Prevention Strategies. Iran Red Crescent Med J 2013;15:279–284. https://doi.org/10.5812/ircmj.6499
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There are 55 citations in total.

Details

Primary Language English
Subjects Clinical Sciences
Journal Section Research Articles
Authors

Yalçın Erzurumlu 0000-0001-6835-4436

Deniz Çataklı 0000-0001-7327-5396

Hatice Kübra Doğan 0000-0002-6061-1300

Project Number TSG-2021-8302, TAB-2020-8253
Publication Date April 29, 2024
Submission Date May 15, 2023
Published in Issue Year 2024 Volume: 15 Issue: 51

Cite

Vancouver Erzurumlu Y, Çataklı D, Doğan HK. Curcumin synergistically augments the chemotherapeutic activity of Doxorubicin in prostate cancer cells. Interdiscip Med J. 2024;15(51):10-9.