Objective: We aimed to determine the role of Poly I:C-induced TLR3 activation on oxidative stress in two different prostate cancer cells [PC-3 (hormone insensitive) and LNCaP (hormone-sensitive)] for the first time. For this purpose, lipid peroxidation (MDA), hydrogen peroxide (H2O2) and proline amounts and superoxide dismutase (SOD) enzyme activity were examined. Methods: The optimal concentration and time required for receptor stimulation with Poly I:C cells were determined by WST-1 analysis. Spectrophotometric methods determined biochemical parameters. Results: The less cytotoxic concentration of 5 µM of Poly I:C on PC-3 and LNCaP cells was determined. A significant increase was observed in LNCaP cells in SOD activities after 6 and 24 hours. A significant increase in PC-3 and LNCaP cells' MDA levels was determined over 6 hours, while a significant decrease was observed in Poly I:C LNCaP after 24 hours. A significant increase in H2O2 concentration was detected in LNCaP cells, but a significant decrease was observed in PC-3 after 6 and 24 hours. The proline level showed a significant increase in LNCaP over 24 hours but not in the proline level in PC-3 cells after 6 and 24 hours. Conclusion: The MDA, H2O2 and SOD activity levels were found to be significantly higher in hormone-sensitive LNCaP cells, while no significant changes were found in PC-3 cells treated with Poly I:C. Results were significantly different at the level of p<0.05 and p<0.001.
The authors thank Dr. Ozlem Aksoy from the Department of Biology at Kocaeli University for supporting our experiments.
References
Tamassia N, Le Moigne V, Rossato M, et al. Activation of an immunoregulatory and antiviral gene expression program in Poly (I:C)-transfected human neutrophils. J Immunol. 2008;181(9):6563-6573.
https://doi.org/10.4049/jimmunol.181.9.6563
Wesch D, Beetz S, Oberg HH, Marget M, Krengel K, Kabelitz D. Direct costimulatory effect of TLR3 ligand poly(I:C) on human gamma delta T lymphocytes. J Immunol. 2006;176(3):1348-1354.
https://doi.org/10.4049/jimmunol.176.3.1348
Matijevic T, Pavelic J. The dual role of TLR3 in the metastatic cell line. Clin Exp Metastasis. 2011;28(7):701-712 https://doi.org/10.1007/s10585-011-9402-z
Alkurdi L, Girard F, Vanbervliet B, et al. Release of c-FLIP brake selectively sensitizes human cancer cells to TLR3-mediated apoptosis. Cell Death Dis. 2018;9(9):874. Published 2018 Aug 29. https://doi.org/10.1038/s41419-018-0850-0
Bonnin M, Fares N, Testoni B, et al. Toll-like receptor 3 downregulation is an escape mechanism from apoptosis during hepatocarcinogenesis [published correction appears in J Hepatol. 2020 Mar;72(3):594]. J Hepatol. 2019;71(4):763-772.
https://doi.org/10.1016/j.jhep.2019.05.031
Bianchi F, Alexiadis S, Camisaschi C, et al. TLR3 Expression Induces Apoptosis in Human Non-Small-Cell Lung Cancer. Int J Mol Sci. 2020;21(4):1440. https://doi.org/10.3390/ijms21041440
Simon HU, Haj-Yehia A, Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis. 2000;5(5): 415-418. https://doi.org/10.1023/A:1009616228304
Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019;69(1):7-34. https://doi.org/10.3322/caac.21551
Shukla S, Srivastava JK, Shankar E, et al. Oxidative Stress and Antioxidant Status in High-Risk Prostate Cancer Subjects. Diagnostics (Basel). 2020;10(3):126. https://doi.org/10.3390/diagnostics10030126
Tan BL, Norhaizan ME. Oxidative Stress, Diet and Prostate Cancer. World J Men's Health. 2021;39(2):195-207. doi: 10.5534/wjmh.200014
Kruk J, Aboul-Enein HY. Reactive Oxygen and Nitrogen Species in Carcinogenesis: Implications of Oxidative Stress on the Progression and Development of Several Cancer Types. Mini Rev Med Chem. 2017;17(11):904-919. https://doi.org/10.2174/1389557517666170228115324
Cekic SD, Çetinkaya A, Avan AN, Apak R. Correlation of total antioxidant capacity with reactive oxygen species (ROS) consumption measured by oxidative conversion. J Agric Food Chem. 2013;61(22): 5260-70. https://doi.org/10.1021/jf3051297
Cramer SL, Saha A, Liu J, et al. Systemic depletion of L-cyst(e)ine with cyst(e)inase increases reactive oxygen species and suppresses tumour growth. Nat Med. 2017;23(1): 120-127. https://doi.org/10.1038/nm.4232
Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev Cancer. 2011;11(2):85-95. https://doi.org/10.1038/nrc2981
Lu JM, Lin PH, Yao Q, Chen C. Chemical and molecular mechanisms of antioxidants: experimental approaches and model systems. J Cell Mol Med. 2010;14(4):840-860. https://doi.org/10.1111/j.1582-4934.2009.00897.x
Litwin MS, Tan HJ. The Diagnosis and Treatment of Prostate Cancer: A Review. JAMA. 2017;317(24):2532-2542. doi:10.1001/jama.2017.7248
Bradford MM. A rapid and sensitive method for quantitating microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-254. https://doi.org/10.1016/0003-2697(76)90527-3
Beauchamp C, Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem. 1971;44(1):276-287. https://doi.org/10.1016/0003-2697(71)90370-8
Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by the thiobarbituric acid reaction. Anal Biochem. 1979;95(2):351-358. https://doi.org/10.1016/0003-2697(79)90738-3
Krantev A, Yordanova R, Janda T, Szalai G, Popova L. Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol. 2008;165(9):920-931. https://doi.org/10.1016/j.jplph.2006.11.014
Liu J, Wang YS. Proline metabolism and molecular cloning of AmP5CS in the mangrove Avicennia marina under heat stress. Ecotoxicology. 2020;29(6):698-706. https://doi.org/10.1007/s10646-020-02198-0
Jana S, Choudhuri MA. Glycolate metabolism of three submersed aquatic angiosperms: effect of heavy metals. Aquat Bot. 1981.11, 67-77. https://doi.org/10.1016/0304-3770(81)90047-4
Ozkan AD, Sarihan M, Kaleli S. Evaluation of the Effects of Nobiletin on Toll-Like Receptor 3 Signaling Pathways in Prostate Cancer In Vitro. Nutr Cancer. 2021;73(7):1138-1144. https://doi.org/10.1080/01635581.2020.1841247
Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39(1):44-84. https://doi.org/10.1016/j.biocel.2006.07.001
Li N, Oberley TD, Oberley LW, Zhong W. Overexpression of manganese superoxide dismutase in DU145 human prostate carcinoma cells has multiple effects on cell phenotype. Prostate. 1998;35: 221–33. https://doi.org/10.1002/(SICI)1097-0045(19980515)35:3<221::AID-PROS8>3.0.CO;2-J
Li H, Kantoff PW, Giovannucci E, et al. Manganese superoxide dismutase polymorphism, prediagnostic antioxidant status, and risk of clinically significant prostate cancer. Cancer Res. 2005;65(6):2498-2504.
Wallace DC. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet. 2005;39,:359-407. 10.1158/0008-5472.CAN-04-3535
Korai A, Sugiura H, Yanagisawa S, et al. Oxidative stress enhances toll-like receptor 3 response to double-stranded RNA in airway epithelial cells. Am J Respir Cell Mol Biol. 2010;42(6):651-660. https://doi.org/10.1165/rcmb.2008-0345OC
Barrera G. Oxidative stress and lipid peroxidation products in cancer progression and therapy. ISRN Oncol. 2012;2012:137289. doi:10.5402/2012/137289
Kokoszka JE, Coskun P, Esposito L, Wallace DC. Increased mitochondrial oxidative stress in the Sod2 (+/−) mouse results in the age-related decline of mitochondrial function, culminating in increased apoptosis. Proc Natl Acad Sci. 2001;98:2278–83. https://doi.org/10.1073/pnas.051627098
Van Remmen H, Ikeno Y, Hamilton M, et al. Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate ageing. Physiol Genomics. 2003;16(1):29-37. Published 2003 Dec 16. https://doi.org/10.1152/physiolgenomics.00122.2003
Arif M, Rashid A, Majeed A, Qaiser F, Razak S. Evaluation of correlation between expression of P53 and Malondialdehyde levels in prostate cancer patients. J Pak Med Assoc. 2018;68(9):1373-1377.
Skrzydlewska E, Stankiewicz A, Sulkowska M, Sulkowski S, Kasacka I. Antioxidant status and lipid peroxidation in colorectal cancer. J Toxicol Environ Health A. 2001;64(3):213-222. https://doi.org/10.1080/15287390152543690
Young O, Crotty T, O'Connell R, O'Sullivan J, Curran AJ. Levels of oxidative damage and lipid peroxidation in thyroid neoplasia. Head Neck. 2010;32(6):750-756. https://doi.org/10.1002/hed.21247
Juric-Sekhar G, Zarkovic K, Waeg G, Cipak A, Zarkovic N. Distribution of 4-hydroxynonenal-protein conjugates as a marker of lipid peroxidation and parameter of malignancy in astrocytic and ependymal tumours of the brain. Tumori. 2009;95(6):762-768. https://doi.org/10.1177/030089160909500620
Xiao D, Herman-Antosiewicz A, Antosiewicz J, et al. Diallyl trisulfide- induced G2-M phase cell cycle arrest in human prostate cancer cells is caused by reactive oxygen species-dependent destruction and hyper- phosphorylation of Cdc25C. Oncogene 2005;24:6256–68. https://doi.org/10.1038/sj.onc.1208759
Savitsky PA, Finkel T. Redox regulation of Cdc25C. J Biol Chem. 2002;277(23):20535-20540. https://doi.org/10.1074/jbc.M201589200
Phang JM, Liu W, Hancock CN, Fischer JW. Proline metabolism and cancer: emerging links to glutamine and collagen. Curr Opin Clin Nutr Metab Care. 2015;18(1):71-77. 10.1097/MCO.0000000000000121
Phang JM. Proline Metabolism in Cell Regulation and Cancer Biology: Recent Advances and Hypotheses. Antioxid Redox Signal. 2019;30(4):635-649. https://doi.org/10.1089/ars.2017.7350
Ahn CS, Metallo CM. Mitochondria as biosynthetic factories for cancer proliferation. Cancer Metab. 2015;3(1):1. https://doi.org/10.1186/s40170-015-0128-2
Olivares O, Vasseur S. Metabolic rewiring of pancreatic ductal adenocarcinoma: New routes to follow within the maze. Int J Cancer. 2016;138(4):787-796. https://doi.org/10.1002/ijc.29501
Pavlova NN, Thompson CB. The Emerging Hallmarks of Cancer Metabolism. Cell Metab. 2016;23(1):27-47. https://doi.org/10.1016/j.cmet.2015.12.006
Yüksel B , Deveci Özkan A . The Role of Citrus Nobiletin on Oxidative Stress Levels and Superoxide Dismutase Activities in Metastatic Castration-Resistant Prostate Cancer. Comm. J. Biol. 2021; 5(1): 84-89. https://doi.org/10.31594/commagene.895415
Poly I:C'nin İndüklediği TLR3 Aktivasyonunun Prostat Kanseri Hücreleri Olan PC-3 (Hormona Duyarsız) ve LNCaP'ın (Hormona Duyarlı) Oksidatif Stres Düzeyine Etkileri
Amaç: Poly I:C ile indüklenen TLR3 aktivasyonunun iki farklı prostat kanseri hücresinde [PC-3 (hormona duyarsız) ve LNCaP (hormona duyarlı)] oksidatif stres üzerindeki rolünü ilk kez belirlemeyi amaçladık. Bu amaçla lipid peroksidasyonu (MDA), hidrojen peroksit (H2O2) ve prolin miktarlarına, süperoksit dismutaz (SOD) enzim aktivitesine bakılmıştır. Yöntem: Reseptör uyarımı için gerekli olan ve hücre canlılığını destekleyen optimal Poly I:C doz ve süresi WST-1 analizi ile belirlendi. Biyokimyasal parametrelere spektrofotometrik yöntemler ile tayin edildi. Bulgular: Poly I:C'nin PC-3 ve LNCaP hücreleri üzerinde daha az sitotoksik konsantrasyonunu olarak 5 µM belirlendi. SOD aktivitelerininde LNCaP hücrelerinde önemli bir artış 6 ve 24 saat sonra gözlenmedi. 6 saat boyunca PC-3 ve LNCaP hücrelerinin MDA seviyelerinde önemli bir artış belirlenirken, 24 saat sonra Poly I:C LNCaP hücrelerinde önemli bir düşüş gözlemlendi. LNCaP hücrelerininde H2O2 konsantrasyonunda önemli artış tespit edildi. Buna karşın 6 ve 24 saatlik Poly I:C uygulamalarından sonra PC-3 hücrelerinde H2O2 konsantrasyonunda önemli bir düşüş gözlendi. Prolin seviyesi LNCaP hücrelerinde 24 saat boyunca önemli bir artış gösterdi ancak PC-3 hücrelerinde hem 6 hem de 24 saat sonra prolin seviyesinde değişiklik olmadı. Sonuç: Hormona duyarlı LNCaP hücrelerinde MDA, H2O2 ve SOD aktivite düzeyleri anlamlı olarak yüksek bulunurken Poly I:C ile tedavi edilen metastatik ve hormona duyarsız PC-3 hücrelerinde önemli bir değişiklik bulunmamıştır. İstatiksel veriler kontrol grubuyla karşılaştırıldığında p<0,05 ve p<0,001 düzeyinde anlamlı olarak farklıdır.
Tamassia N, Le Moigne V, Rossato M, et al. Activation of an immunoregulatory and antiviral gene expression program in Poly (I:C)-transfected human neutrophils. J Immunol. 2008;181(9):6563-6573.
https://doi.org/10.4049/jimmunol.181.9.6563
Wesch D, Beetz S, Oberg HH, Marget M, Krengel K, Kabelitz D. Direct costimulatory effect of TLR3 ligand poly(I:C) on human gamma delta T lymphocytes. J Immunol. 2006;176(3):1348-1354.
https://doi.org/10.4049/jimmunol.176.3.1348
Matijevic T, Pavelic J. The dual role of TLR3 in the metastatic cell line. Clin Exp Metastasis. 2011;28(7):701-712 https://doi.org/10.1007/s10585-011-9402-z
Alkurdi L, Girard F, Vanbervliet B, et al. Release of c-FLIP brake selectively sensitizes human cancer cells to TLR3-mediated apoptosis. Cell Death Dis. 2018;9(9):874. Published 2018 Aug 29. https://doi.org/10.1038/s41419-018-0850-0
Bonnin M, Fares N, Testoni B, et al. Toll-like receptor 3 downregulation is an escape mechanism from apoptosis during hepatocarcinogenesis [published correction appears in J Hepatol. 2020 Mar;72(3):594]. J Hepatol. 2019;71(4):763-772.
https://doi.org/10.1016/j.jhep.2019.05.031
Bianchi F, Alexiadis S, Camisaschi C, et al. TLR3 Expression Induces Apoptosis in Human Non-Small-Cell Lung Cancer. Int J Mol Sci. 2020;21(4):1440. https://doi.org/10.3390/ijms21041440
Simon HU, Haj-Yehia A, Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis. 2000;5(5): 415-418. https://doi.org/10.1023/A:1009616228304
Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019;69(1):7-34. https://doi.org/10.3322/caac.21551
Shukla S, Srivastava JK, Shankar E, et al. Oxidative Stress and Antioxidant Status in High-Risk Prostate Cancer Subjects. Diagnostics (Basel). 2020;10(3):126. https://doi.org/10.3390/diagnostics10030126
Tan BL, Norhaizan ME. Oxidative Stress, Diet and Prostate Cancer. World J Men's Health. 2021;39(2):195-207. doi: 10.5534/wjmh.200014
Kruk J, Aboul-Enein HY. Reactive Oxygen and Nitrogen Species in Carcinogenesis: Implications of Oxidative Stress on the Progression and Development of Several Cancer Types. Mini Rev Med Chem. 2017;17(11):904-919. https://doi.org/10.2174/1389557517666170228115324
Cekic SD, Çetinkaya A, Avan AN, Apak R. Correlation of total antioxidant capacity with reactive oxygen species (ROS) consumption measured by oxidative conversion. J Agric Food Chem. 2013;61(22): 5260-70. https://doi.org/10.1021/jf3051297
Cramer SL, Saha A, Liu J, et al. Systemic depletion of L-cyst(e)ine with cyst(e)inase increases reactive oxygen species and suppresses tumour growth. Nat Med. 2017;23(1): 120-127. https://doi.org/10.1038/nm.4232
Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev Cancer. 2011;11(2):85-95. https://doi.org/10.1038/nrc2981
Lu JM, Lin PH, Yao Q, Chen C. Chemical and molecular mechanisms of antioxidants: experimental approaches and model systems. J Cell Mol Med. 2010;14(4):840-860. https://doi.org/10.1111/j.1582-4934.2009.00897.x
Litwin MS, Tan HJ. The Diagnosis and Treatment of Prostate Cancer: A Review. JAMA. 2017;317(24):2532-2542. doi:10.1001/jama.2017.7248
Bradford MM. A rapid and sensitive method for quantitating microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-254. https://doi.org/10.1016/0003-2697(76)90527-3
Beauchamp C, Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem. 1971;44(1):276-287. https://doi.org/10.1016/0003-2697(71)90370-8
Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by the thiobarbituric acid reaction. Anal Biochem. 1979;95(2):351-358. https://doi.org/10.1016/0003-2697(79)90738-3
Krantev A, Yordanova R, Janda T, Szalai G, Popova L. Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol. 2008;165(9):920-931. https://doi.org/10.1016/j.jplph.2006.11.014
Liu J, Wang YS. Proline metabolism and molecular cloning of AmP5CS in the mangrove Avicennia marina under heat stress. Ecotoxicology. 2020;29(6):698-706. https://doi.org/10.1007/s10646-020-02198-0
Jana S, Choudhuri MA. Glycolate metabolism of three submersed aquatic angiosperms: effect of heavy metals. Aquat Bot. 1981.11, 67-77. https://doi.org/10.1016/0304-3770(81)90047-4
Ozkan AD, Sarihan M, Kaleli S. Evaluation of the Effects of Nobiletin on Toll-Like Receptor 3 Signaling Pathways in Prostate Cancer In Vitro. Nutr Cancer. 2021;73(7):1138-1144. https://doi.org/10.1080/01635581.2020.1841247
Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39(1):44-84. https://doi.org/10.1016/j.biocel.2006.07.001
Li N, Oberley TD, Oberley LW, Zhong W. Overexpression of manganese superoxide dismutase in DU145 human prostate carcinoma cells has multiple effects on cell phenotype. Prostate. 1998;35: 221–33. https://doi.org/10.1002/(SICI)1097-0045(19980515)35:3<221::AID-PROS8>3.0.CO;2-J
Li H, Kantoff PW, Giovannucci E, et al. Manganese superoxide dismutase polymorphism, prediagnostic antioxidant status, and risk of clinically significant prostate cancer. Cancer Res. 2005;65(6):2498-2504.
Wallace DC. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet. 2005;39,:359-407. 10.1158/0008-5472.CAN-04-3535
Korai A, Sugiura H, Yanagisawa S, et al. Oxidative stress enhances toll-like receptor 3 response to double-stranded RNA in airway epithelial cells. Am J Respir Cell Mol Biol. 2010;42(6):651-660. https://doi.org/10.1165/rcmb.2008-0345OC
Barrera G. Oxidative stress and lipid peroxidation products in cancer progression and therapy. ISRN Oncol. 2012;2012:137289. doi:10.5402/2012/137289
Kokoszka JE, Coskun P, Esposito L, Wallace DC. Increased mitochondrial oxidative stress in the Sod2 (+/−) mouse results in the age-related decline of mitochondrial function, culminating in increased apoptosis. Proc Natl Acad Sci. 2001;98:2278–83. https://doi.org/10.1073/pnas.051627098
Van Remmen H, Ikeno Y, Hamilton M, et al. Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate ageing. Physiol Genomics. 2003;16(1):29-37. Published 2003 Dec 16. https://doi.org/10.1152/physiolgenomics.00122.2003
Arif M, Rashid A, Majeed A, Qaiser F, Razak S. Evaluation of correlation between expression of P53 and Malondialdehyde levels in prostate cancer patients. J Pak Med Assoc. 2018;68(9):1373-1377.
Skrzydlewska E, Stankiewicz A, Sulkowska M, Sulkowski S, Kasacka I. Antioxidant status and lipid peroxidation in colorectal cancer. J Toxicol Environ Health A. 2001;64(3):213-222. https://doi.org/10.1080/15287390152543690
Young O, Crotty T, O'Connell R, O'Sullivan J, Curran AJ. Levels of oxidative damage and lipid peroxidation in thyroid neoplasia. Head Neck. 2010;32(6):750-756. https://doi.org/10.1002/hed.21247
Juric-Sekhar G, Zarkovic K, Waeg G, Cipak A, Zarkovic N. Distribution of 4-hydroxynonenal-protein conjugates as a marker of lipid peroxidation and parameter of malignancy in astrocytic and ependymal tumours of the brain. Tumori. 2009;95(6):762-768. https://doi.org/10.1177/030089160909500620
Xiao D, Herman-Antosiewicz A, Antosiewicz J, et al. Diallyl trisulfide- induced G2-M phase cell cycle arrest in human prostate cancer cells is caused by reactive oxygen species-dependent destruction and hyper- phosphorylation of Cdc25C. Oncogene 2005;24:6256–68. https://doi.org/10.1038/sj.onc.1208759
Savitsky PA, Finkel T. Redox regulation of Cdc25C. J Biol Chem. 2002;277(23):20535-20540. https://doi.org/10.1074/jbc.M201589200
Phang JM, Liu W, Hancock CN, Fischer JW. Proline metabolism and cancer: emerging links to glutamine and collagen. Curr Opin Clin Nutr Metab Care. 2015;18(1):71-77. 10.1097/MCO.0000000000000121
Phang JM. Proline Metabolism in Cell Regulation and Cancer Biology: Recent Advances and Hypotheses. Antioxid Redox Signal. 2019;30(4):635-649. https://doi.org/10.1089/ars.2017.7350
Ahn CS, Metallo CM. Mitochondria as biosynthetic factories for cancer proliferation. Cancer Metab. 2015;3(1):1. https://doi.org/10.1186/s40170-015-0128-2
Olivares O, Vasseur S. Metabolic rewiring of pancreatic ductal adenocarcinoma: New routes to follow within the maze. Int J Cancer. 2016;138(4):787-796. https://doi.org/10.1002/ijc.29501
Pavlova NN, Thompson CB. The Emerging Hallmarks of Cancer Metabolism. Cell Metab. 2016;23(1):27-47. https://doi.org/10.1016/j.cmet.2015.12.006
Yüksel B , Deveci Özkan A . The Role of Citrus Nobiletin on Oxidative Stress Levels and Superoxide Dismutase Activities in Metastatic Castration-Resistant Prostate Cancer. Comm. J. Biol. 2021; 5(1): 84-89. https://doi.org/10.31594/commagene.895415
There are 43 citations in total.
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Primary Language
Turkish
Subjects
Analytical Biochemistry, Biochemistry and Cell Biology (Other)
Deveci Özkan, A., & Yüksel, B. (2022). Poly I:C’nin İndüklediği TLR3 Aktivasyonunun Prostat Kanseri Hücreleri Olan PC-3 (Hormona Duyarsız) ve LNCaP’ın (Hormona Duyarlı) Oksidatif Stres Düzeyine Etkileri. Kocaeli Üniversitesi Sağlık Bilimleri Dergisi, 8(1), 18-24. https://doi.org/10.30934/kusbed.915511
AMA
Deveci Özkan A, Yüksel B. Poly I:C’nin İndüklediği TLR3 Aktivasyonunun Prostat Kanseri Hücreleri Olan PC-3 (Hormona Duyarsız) ve LNCaP’ın (Hormona Duyarlı) Oksidatif Stres Düzeyine Etkileri. KOU Sag Bil Derg. March 2022;8(1):18-24. doi:10.30934/kusbed.915511
Chicago
Deveci Özkan, Asuman, and Burcu Yüksel. “Poly I:C’nin İndüklediği TLR3 Aktivasyonunun Prostat Kanseri Hücreleri Olan PC-3 (Hormona Duyarsız) Ve LNCaP’ın (Hormona Duyarlı) Oksidatif Stres Düzeyine Etkileri”. Kocaeli Üniversitesi Sağlık Bilimleri Dergisi 8, no. 1 (March 2022): 18-24. https://doi.org/10.30934/kusbed.915511.
EndNote
Deveci Özkan A, Yüksel B (March 1, 2022) Poly I:C’nin İndüklediği TLR3 Aktivasyonunun Prostat Kanseri Hücreleri Olan PC-3 (Hormona Duyarsız) ve LNCaP’ın (Hormona Duyarlı) Oksidatif Stres Düzeyine Etkileri. Kocaeli Üniversitesi Sağlık Bilimleri Dergisi 8 1 18–24.
IEEE
A. Deveci Özkan and B. Yüksel, “Poly I:C’nin İndüklediği TLR3 Aktivasyonunun Prostat Kanseri Hücreleri Olan PC-3 (Hormona Duyarsız) ve LNCaP’ın (Hormona Duyarlı) Oksidatif Stres Düzeyine Etkileri”, KOU Sag Bil Derg, vol. 8, no. 1, pp. 18–24, 2022, doi: 10.30934/kusbed.915511.
ISNAD
Deveci Özkan, Asuman - Yüksel, Burcu. “Poly I:C’nin İndüklediği TLR3 Aktivasyonunun Prostat Kanseri Hücreleri Olan PC-3 (Hormona Duyarsız) Ve LNCaP’ın (Hormona Duyarlı) Oksidatif Stres Düzeyine Etkileri”. Kocaeli Üniversitesi Sağlık Bilimleri Dergisi 8/1 (March 2022), 18-24. https://doi.org/10.30934/kusbed.915511.
JAMA
Deveci Özkan A, Yüksel B. Poly I:C’nin İndüklediği TLR3 Aktivasyonunun Prostat Kanseri Hücreleri Olan PC-3 (Hormona Duyarsız) ve LNCaP’ın (Hormona Duyarlı) Oksidatif Stres Düzeyine Etkileri. KOU Sag Bil Derg. 2022;8:18–24.
MLA
Deveci Özkan, Asuman and Burcu Yüksel. “Poly I:C’nin İndüklediği TLR3 Aktivasyonunun Prostat Kanseri Hücreleri Olan PC-3 (Hormona Duyarsız) Ve LNCaP’ın (Hormona Duyarlı) Oksidatif Stres Düzeyine Etkileri”. Kocaeli Üniversitesi Sağlık Bilimleri Dergisi, vol. 8, no. 1, 2022, pp. 18-24, doi:10.30934/kusbed.915511.
Vancouver
Deveci Özkan A, Yüksel B. Poly I:C’nin İndüklediği TLR3 Aktivasyonunun Prostat Kanseri Hücreleri Olan PC-3 (Hormona Duyarsız) ve LNCaP’ın (Hormona Duyarlı) Oksidatif Stres Düzeyine Etkileri. KOU Sag Bil Derg. 2022;8(1):18-24.