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Selective Cytotoxicity of Chemical Composition of Spirulina platensis Extract In Endometrial Cells: In Vitro and In Silico Approach

Year 2023, , 493 - 503, 30.06.2023

Belkis Atasever Arslan Kaan Yılancıoğlu Ahmet Can Timuçin Zeynep Kalkan Seda Kuşoğlu Gültekin Selim Çetiner

https://doi.org/10.18016/ksutarimdoga.vi.1110478

Abstract

Microalgae are considered as an ample source of bioactive compounds. These wide variety of chemicals possess promising potential to translate into drug candidates. Hence, the aim of this study is to determine potential anti-cancer effects of Spirulina platensis microalgae extract against endometrial cancer cells. The selective cytotoxic effect and cytotoxicity index of S. platensis microalgae extract on the Ishikawa endometrial cancer cell line, the determination of DNA fragmentation and the change in gene expression levels of apoptosis-related Bad, Poly-ADP Ribose Polymerase-1 (PARP1), p53, Akt1 and caspase-3 signaling proteins were determined. ECV304 human umbilical vein endothelial cell line was used for a control cell line. Cytotoxic effects of 500 μg mL-1 of S. platensis microalgae extract on Ishikawa and ECV304 cells were determined as 43±4.87 % and 22±1.87 % respectively. In order to delineate specific compounds in the extract, GC-MS analysis was further conducted and seven major compounds revealed to be abundantly present. Since DNA fragmentation induced by S. platensis extract might be related interaction of GC-MS identified compounds with PARP1, an in silico analysis was further implemented. Results indicated the presence of a possible PARP1 inhibitory mechanism contributing to the apoptotic response. In conclusion, a possible link between a specific compound found in S. platensis microalgae extract and the cytotoxicity in endometrial cells was formed through combining in vitro and in silico approaches. The result of these approaches has contributed to the identification of potential anti-cancer compound candidates found in S. platensis microalgae extract.

Keywords

Apoptosis Endometrial Cancer Cells GC-MS Microalgae Cytotoxicity

Supporting Institution

The Scientific and Technological Research Council of Turkey (TUBITAK) 3501.

Project Number

Project No: 113S251

Thanks

This study was supported by the Scientific and Technological Research Council of Türkiye (TUBITAK) 3501 (Project No: 113S251).

References

  • Arslan, B. A., Isik, F. B., Gur, H., Ozen, F., & Catal, T. (2017). Apoptotic Effect Of Nigella sativa On Human Lymphoma U937 Cells. Pharmacognosy Magazine, 13(3), 628-632. https://doi.org/ 10.4103/pm.pm_93_17.
  • Atasever-Arslan, B., Yilancioglu, K., Bekaroglu, M. G., Taskin, E., Altinoz, E, & Cetiner, S. (2015). Cytotoxic Effect Of Extract From Dunaliella salina Against SH-SY5Y Neuroblastoma Cells, General Physiology and Biophysics, 34(2), 201-207. https://doi.org/10.4149/gpb_2014034.
  • Atasever-Arslan B, Yilancioglu K, Kalkan Z, Timucin AC, Gür H, Isik FB, Deniz E, Erman B, & Cetiner, S. (2016). Screening Of New Antileukemic Agents From Essential Oils Of Algae Extracts And Computational Modeling Of Their Interactions With Intracellular Signaling Nodes. European Journal of Pharmaceutical Sciences, 83, 120-131. https://doi.org/10.1016/j.ejps.2015.12.001.
  • Atasever-Arslan, B.,, Yilancioglu, K., Kuşoğlu-Gültekin, S., & Albayrak, İ. G. (2022). Chemical Constituent Of Isochrysis galbana Microalgae Extract And Its Cytotoxic Activities On Leukemic Cell Lines. İstanbul Journal of Pharmacy, 52(1), 64-68. https://doi.org/10.26650/IstanbulJPharm.2022. 1057338
  • Brooks, B. R., Brooks , C. L., Mackerell, A. D., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., … Karplus, M. (2009). CHARMM: The Biomolecular Simulation Program. Journal of Computational Chemistry, 30, 1545-1614. https://doi.org/10.1002/jcc.21287
  • Del Carmen, M., Boruta, D., & Schorge J (2011). Recurrent Endometrial Cancer. Clinical Obstetrics and Gynecology, 54(2), 266-277. https://doi.org/ 10.1097/ GRF.0b013e318218c6d1.
  • Feig, M., MacKerell, A. D., & Brooks, C. L. (2003). Force Field Influence on The Observation of Π-Helical Protein Structures In Molecular Dynamics Simulations. The Journal of Physical Chemistry B, 107, 2831-2836. https://doi.org/10.1021/jp027293y
  • Hevir-Kene, N., & Rizner, T. L. (2015). The Endometrial Cancer Cell Lines Ishikawa And HEC-1A, And The Control Cell Line HIEEC, Differ In Expression Of Estrogen Biosynthetic And Metabolic Genes, And In Androstenedione And Estrone-Sulfate Metabolism. Chemico-Biological Interactions, 234, 309-319. https://doi.org/10.1016/ j.cbi.2014.11.015.
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual Molecular Dynamics. Journal of Molecular Graphics and Modelling, 14, 33-38. https://doi.org/ 10.1016/0263-7855(96)00018-5.
  • Iwashita, A., Hattori, K., Yamamoto, H., Ishida, J., Kido, Y., Kamijo, K., Murano, K., Miyake, H., Kinoshita, T., Warizaya, M., Ohkubo, M., Matsuoka, N., & Mutoh, S. (2005). Discovery Of Quinazolinone And Quinoxaline Derivatives As Potent And Selective Poly(ADP-Ribose) Polymerase-1/2 Inhibitors. FEBS Letters, 579, 1389-1393. https://doi.org/10.1016/j.febslet.2005. 01.036.
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  • Karthikeyan, S. C., Velmurugan, S., Donio, M. B., Michaelbabu, M., & Citarasu, T. (2014). Studies On The Antimicrobial Potential And Structural Characterization Of Fatty Acids Extracted From Sydney Rock Oyster Saccostrea glomerata. Annals of Clinical Microbiology and Antimicrobials, 13, 332-343. https://doi.org/10.1186/s12941-014- 0057-x
  • Kaya, B., Atasever-Arslan, B., Kalkan, Z., Gur, H., & Ulkuseven, B. (2016). Apoptotic Mechanisms Of N1-Acetylacetone, N4-4-Methoxy-Salicylidene-Thiosemicarbazide Chelating With Nickel(II) On HL60 Leukemia Cells. General Physiology and Biophysics, 35(4), 451-458. https://doi.org/10.4149/ gpb_2016006.
  • Khan, A. A., Alanazi, A.M., Jabeen, M., Chauhan, A., & Abdelhameed, A. S. (2013). Design, Synthesis And in Vitro Anticancer Evaluation Of A Stearic Acid-Based Ester Conjugate. Anticancer Research, 33, 2517-2524. https://pubmed.ncbi.nlm.nih.gov/ 23749903/
  • Kok, Y. Y., Chu, W. L., Phang, S. M., Mohamed, S. M., Naidu, R., Lai, P. J., Ling, S. N., Mak, J. W., Lim, P. K. C., Balraj, P., & Khoo, A. S. B. (2011). Inhibitory Activities Of Microalgal Extracts Against Epstein-Barr Virus DNA Release From Lymphoblastoid Cells. Journal of Zhejiang University Science, 12, 335-345. https://doi.org/ 10.1631/jzus.B1000336
  • Konickova, R., Vankova, K., Vanikova, J., Vánová, V., Muchová, L., Subhanová, I., Zadinová, M., Zelenka, J., Dvořák, A., Kolář, M., Strnad, H., Rimpelová, S., Ruml, T., Wong, R. J., & Vítek, L. (2014). Anti-Cancer Effects Of Blue-Green Alga Spirulina platensis, A Natural Source Of Bilirubin-Like Tetrapyrrolic Compounds. Annals of Hepatology, 13, 273-283. https://doi.org/10.1016/S1665-2681(19)30891-9
  • Koru, E., & Cirik, S. (2003). The effects of temperature on growth and some biochemical characteristics of microalgae Spirulina platensis (Cyanophyceae). E.U. Journal of Fisheries & Aquatic Sciences, 20(3-4), 419 – 422. https://doi.org/10.12714/egejfas. 2003.20.3.5000157094
  • Lazebnik, Y. A., Kaufmann, S. H., Desnoyers, S., Poirier, G. G., & Earnshaw, W. C. (1994). Cleavage Of Poly(ADP-Ribose) Polymerase By A Proteinase With Properties Like ICE. Nature, 371, 346-347. https://doi.org/10.1038/371346a0.
  • MacKerell, A. D., Bashford, D., Bellott, M., Dunbrack, R. L., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., … Karplus, M. (1998). All-Atom Empirical Potential For Molecular Modeling And Dynamics Studies Of Proteins. The Journal of Physical Chemistry B, 102, 3586-3616. https://doi.org/10.1021/jp973084f
  • MacKerell, A. D., Feig, M., Brooks, C. L. (2004). Improved Treatment Of The Protein Backbone İn Empirical Force Fields. Journal of the American Chemical Society, 126, 698-699. https://doi.org/ 10.1021/ja036959e
  • Nicholson, D. W., Ali, A., Thornberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Griffin, P. R., Labelle, M., Lazebnik, Y. A., Munday, N. A., Raju, S. M., Smulson, M. E., Yamin, T, Yu,V. L. , & Miller, D. K. (1995). Identification And Inhibition Of The ICE/CED-3 Protease Necessary For Mammalian Apoptosis. Nature, 376, 37-43. https://doi.org/10.1038/376037a0.
  • Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kalé, L., & Schulten, K. (2005). Scalable Molecular Dynamics With NAMD. Journal of Computational Chemistry, 26, 1781-1802. https://doi.org/10.1002/ jcc.20289.
  • Pirildar, S., Sutlupinar, N., Atasever, B., Erdem-Kuruca, S., Papouskova, B., & Šimánek, V. (2010). Chemical Constituents Of The Different Parts Of Colchicum Baytopiorum And Their Cytotoxic Activities On K562 And HL60 Cell Lines. Pharmaceutical Biology, 48, 32-39. https://doi.org/ 10.3109/13880200903029373
  • Russo, A., Cardile, V., Graziano, A. C., Formisano, C., Rigano, D., Canzoneri, M., Bruno, M., & Senatore, F. (2015). Comparison Of Essential Oil Components And İn Vitro Anticancer Activity İn Wild And Cultivated Salvia verbenaca. Natural Product Research, 29, 1630-1640. https://doi.org/10.1080/ 14786419.2014.994212.
  • Saini, M. K., & Sanyal, S. N. (2014). Piroxicam And C-Phycocyanin Prevent Colon Carcinogenesis By İnhibition Of Membrane Fluidity And Canonical Wnt/Beta-Catenin Signaling While Up-Regulating Ligand Dependent Transcription Factor PPARgamma. Biomedicine & Pharmacotherapy, 68, 537-550. https://doi.org/10.1016/ j.biopha. 2014.03.007
  • Suda, K., Rothen-Rutishauser, B., Gunthert, M., & Wunderli-Allenspach, H. (2011). Phenotypic Characterization Of Human Umbilical Vein Endothelial (ECV304) And Urinary Carcinoma (T24) Cells: Endothelial Versus Epithelial Features. In Vitro Cellular & Developmental Biology, 37, 505-514. https://doi.org/10.1290/1071-2690(2001)037<0505:PCOHUV>2.0.CO;2
  • Şeker Karatoprak, G., Ökdem, B., İlgün, S., & Koşar, M. (2022). Evaluation of Antioxidant and Antimicrobial Activities of Potentilla recta L. KSU Journal of Agriculture and Nature, 25(3), 439-448. https://doi.org/10.18016/ksutarimdoga.vi.894015.
  • Takeara, R., Jimenez, P. C., Wilke, D. V., Moraes, M. O., Pessoa, C., Lopes, N. P., Lopes, J. L. C., Lotufo, T. M. C., & Costa-Lotufo, L. V. (2008). Antileukemic Effects Of Didemnum psammatodes (Tunicata: Ascidiacea) Constituents. Comparative Biochemistry And Physiology - Part A, 151, 363-369. https://doi.org/10.1016/j.cbpa.2007.02.011.
  • Vanommeslaeghe, K., Hatcher, E., Acharya, C., Kundu, S., Zhong, S., Shim, J., Darian, E., Guvench, O., Lopes, P., Vorobyov, I., & Mackerell, A. D. (2010). CHARMM General Force Field: A Force Field For Drug-Like Molecules Compatible With The CHARMM All-Atom Additive Biological Force Fields. Journal of Computational Chemistry, 31, 671-690. https://doi.org/10.1002/jcc.21367.
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Endometriyal Hücrelerde Spirulina platensis Ekstresinin Kimyasal Bileşiminin Seçici Sitotoksisitesi: İn Vitro ve İn Siliko Yaklaşım

Year 2023, , 493 - 503, 30.06.2023

Belkis Atasever Arslan Kaan Yılancıoğlu Ahmet Can Timuçin Zeynep Kalkan Seda Kuşoğlu Gültekin Selim Çetiner

https://doi.org/10.18016/ksutarimdoga.vi.1110478

Abstract

Microalgae are considered as an ample source of bioactive compounds. These wide variety of chemicals possess promising potential to translate into drug candidates. Hence, the aim of this study is to determine potential anti-cancer effects of Spirulina platensis microalgae extract against endometrial cancer cells. The selective cytotoxic effect and cytotoxicity index of S. platensis microalgae extract on the Ishikawa endometrial cancer cell line, the determination of DNA fragmentation and the change in gene expression levels of apoptosis-related Bad, Poly-ADP Ribose Polymerase-1 (PARP1), p53, Akt1 and caspase-3 signaling proteins were determined. ECV304 human umbilical vein endothelial cell line was used for a control cell line. Cytotoxic effects of 500 μg mL-1 of S. platensis microalgae extract on Ishikawa and ECV304 cells were determined as 43±4.87 % and 22±1.87 % respectively. In order to delineate specific compounds in the extract, GC-MS analysis was further conducted and seven major compounds revealed to be abundantly present. Since DNA fragmentation induced by S. platensis extract might be related interaction of GC-MS identified compounds with PARP1, an in silico analysis was further implemented. Results indicated the presence of a possible PARP1 inhibitory mechanism contributing to the apoptotic response. In conclusion, a possible link between a specific compound found in S. platensis microalgae extract and the cytotoxicity in endometrial cells was formed through combining in vitro and in silico approaches. The result of these approaches has contributed to the identification of potential anti-cancer compound candidates found in S. platensis microalgae extract.

Keywords

Apoptoz Endometriyal Kanser Hücreleri GC-MS Mikroalg Sitotoksisite

Project Number

Project No: 113S251

References

  • Arslan, B. A., Isik, F. B., Gur, H., Ozen, F., & Catal, T. (2017). Apoptotic Effect Of Nigella sativa On Human Lymphoma U937 Cells. Pharmacognosy Magazine, 13(3), 628-632. https://doi.org/ 10.4103/pm.pm_93_17.
  • Atasever-Arslan, B., Yilancioglu, K., Bekaroglu, M. G., Taskin, E., Altinoz, E, & Cetiner, S. (2015). Cytotoxic Effect Of Extract From Dunaliella salina Against SH-SY5Y Neuroblastoma Cells, General Physiology and Biophysics, 34(2), 201-207. https://doi.org/10.4149/gpb_2014034.
  • Atasever-Arslan B, Yilancioglu K, Kalkan Z, Timucin AC, Gür H, Isik FB, Deniz E, Erman B, & Cetiner, S. (2016). Screening Of New Antileukemic Agents From Essential Oils Of Algae Extracts And Computational Modeling Of Their Interactions With Intracellular Signaling Nodes. European Journal of Pharmaceutical Sciences, 83, 120-131. https://doi.org/10.1016/j.ejps.2015.12.001.
  • Atasever-Arslan, B.,, Yilancioglu, K., Kuşoğlu-Gültekin, S., & Albayrak, İ. G. (2022). Chemical Constituent Of Isochrysis galbana Microalgae Extract And Its Cytotoxic Activities On Leukemic Cell Lines. İstanbul Journal of Pharmacy, 52(1), 64-68. https://doi.org/10.26650/IstanbulJPharm.2022. 1057338
  • Brooks, B. R., Brooks , C. L., Mackerell, A. D., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., … Karplus, M. (2009). CHARMM: The Biomolecular Simulation Program. Journal of Computational Chemistry, 30, 1545-1614. https://doi.org/10.1002/jcc.21287
  • Del Carmen, M., Boruta, D., & Schorge J (2011). Recurrent Endometrial Cancer. Clinical Obstetrics and Gynecology, 54(2), 266-277. https://doi.org/ 10.1097/ GRF.0b013e318218c6d1.
  • Feig, M., MacKerell, A. D., & Brooks, C. L. (2003). Force Field Influence on The Observation of Π-Helical Protein Structures In Molecular Dynamics Simulations. The Journal of Physical Chemistry B, 107, 2831-2836. https://doi.org/10.1021/jp027293y
  • Hevir-Kene, N., & Rizner, T. L. (2015). The Endometrial Cancer Cell Lines Ishikawa And HEC-1A, And The Control Cell Line HIEEC, Differ In Expression Of Estrogen Biosynthetic And Metabolic Genes, And In Androstenedione And Estrone-Sulfate Metabolism. Chemico-Biological Interactions, 234, 309-319. https://doi.org/10.1016/ j.cbi.2014.11.015.
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual Molecular Dynamics. Journal of Molecular Graphics and Modelling, 14, 33-38. https://doi.org/ 10.1016/0263-7855(96)00018-5.
  • Iwashita, A., Hattori, K., Yamamoto, H., Ishida, J., Kido, Y., Kamijo, K., Murano, K., Miyake, H., Kinoshita, T., Warizaya, M., Ohkubo, M., Matsuoka, N., & Mutoh, S. (2005). Discovery Of Quinazolinone And Quinoxaline Derivatives As Potent And Selective Poly(ADP-Ribose) Polymerase-1/2 Inhibitors. FEBS Letters, 579, 1389-1393. https://doi.org/10.1016/j.febslet.2005. 01.036.
  • Jorgensen, W. L., & Madura, J. D. (1983). Quantum And Statistical Mechanical Studies Of Liquids. 25. Solvation And Conformation Of Methanol in Water. Journal of the American Chemical Society, 105, 1407-1413. https://doi.org/10.1021/ja00344a001
  • Karthikeyan, S. C., Velmurugan, S., Donio, M. B., Michaelbabu, M., & Citarasu, T. (2014). Studies On The Antimicrobial Potential And Structural Characterization Of Fatty Acids Extracted From Sydney Rock Oyster Saccostrea glomerata. Annals of Clinical Microbiology and Antimicrobials, 13, 332-343. https://doi.org/10.1186/s12941-014- 0057-x
  • Kaya, B., Atasever-Arslan, B., Kalkan, Z., Gur, H., & Ulkuseven, B. (2016). Apoptotic Mechanisms Of N1-Acetylacetone, N4-4-Methoxy-Salicylidene-Thiosemicarbazide Chelating With Nickel(II) On HL60 Leukemia Cells. General Physiology and Biophysics, 35(4), 451-458. https://doi.org/10.4149/ gpb_2016006.
  • Khan, A. A., Alanazi, A.M., Jabeen, M., Chauhan, A., & Abdelhameed, A. S. (2013). Design, Synthesis And in Vitro Anticancer Evaluation Of A Stearic Acid-Based Ester Conjugate. Anticancer Research, 33, 2517-2524. https://pubmed.ncbi.nlm.nih.gov/ 23749903/
  • Kok, Y. Y., Chu, W. L., Phang, S. M., Mohamed, S. M., Naidu, R., Lai, P. J., Ling, S. N., Mak, J. W., Lim, P. K. C., Balraj, P., & Khoo, A. S. B. (2011). Inhibitory Activities Of Microalgal Extracts Against Epstein-Barr Virus DNA Release From Lymphoblastoid Cells. Journal of Zhejiang University Science, 12, 335-345. https://doi.org/ 10.1631/jzus.B1000336
  • Konickova, R., Vankova, K., Vanikova, J., Vánová, V., Muchová, L., Subhanová, I., Zadinová, M., Zelenka, J., Dvořák, A., Kolář, M., Strnad, H., Rimpelová, S., Ruml, T., Wong, R. J., & Vítek, L. (2014). Anti-Cancer Effects Of Blue-Green Alga Spirulina platensis, A Natural Source Of Bilirubin-Like Tetrapyrrolic Compounds. Annals of Hepatology, 13, 273-283. https://doi.org/10.1016/S1665-2681(19)30891-9
  • Koru, E., & Cirik, S. (2003). The effects of temperature on growth and some biochemical characteristics of microalgae Spirulina platensis (Cyanophyceae). E.U. Journal of Fisheries & Aquatic Sciences, 20(3-4), 419 – 422. https://doi.org/10.12714/egejfas. 2003.20.3.5000157094
  • Lazebnik, Y. A., Kaufmann, S. H., Desnoyers, S., Poirier, G. G., & Earnshaw, W. C. (1994). Cleavage Of Poly(ADP-Ribose) Polymerase By A Proteinase With Properties Like ICE. Nature, 371, 346-347. https://doi.org/10.1038/371346a0.
  • MacKerell, A. D., Bashford, D., Bellott, M., Dunbrack, R. L., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., … Karplus, M. (1998). All-Atom Empirical Potential For Molecular Modeling And Dynamics Studies Of Proteins. The Journal of Physical Chemistry B, 102, 3586-3616. https://doi.org/10.1021/jp973084f
  • MacKerell, A. D., Feig, M., Brooks, C. L. (2004). Improved Treatment Of The Protein Backbone İn Empirical Force Fields. Journal of the American Chemical Society, 126, 698-699. https://doi.org/ 10.1021/ja036959e
  • Nicholson, D. W., Ali, A., Thornberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Griffin, P. R., Labelle, M., Lazebnik, Y. A., Munday, N. A., Raju, S. M., Smulson, M. E., Yamin, T, Yu,V. L. , & Miller, D. K. (1995). Identification And Inhibition Of The ICE/CED-3 Protease Necessary For Mammalian Apoptosis. Nature, 376, 37-43. https://doi.org/10.1038/376037a0.
  • Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kalé, L., & Schulten, K. (2005). Scalable Molecular Dynamics With NAMD. Journal of Computational Chemistry, 26, 1781-1802. https://doi.org/10.1002/ jcc.20289.
  • Pirildar, S., Sutlupinar, N., Atasever, B., Erdem-Kuruca, S., Papouskova, B., & Šimánek, V. (2010). Chemical Constituents Of The Different Parts Of Colchicum Baytopiorum And Their Cytotoxic Activities On K562 And HL60 Cell Lines. Pharmaceutical Biology, 48, 32-39. https://doi.org/ 10.3109/13880200903029373
  • Russo, A., Cardile, V., Graziano, A. C., Formisano, C., Rigano, D., Canzoneri, M., Bruno, M., & Senatore, F. (2015). Comparison Of Essential Oil Components And İn Vitro Anticancer Activity İn Wild And Cultivated Salvia verbenaca. Natural Product Research, 29, 1630-1640. https://doi.org/10.1080/ 14786419.2014.994212.
  • Saini, M. K., & Sanyal, S. N. (2014). Piroxicam And C-Phycocyanin Prevent Colon Carcinogenesis By İnhibition Of Membrane Fluidity And Canonical Wnt/Beta-Catenin Signaling While Up-Regulating Ligand Dependent Transcription Factor PPARgamma. Biomedicine & Pharmacotherapy, 68, 537-550. https://doi.org/10.1016/ j.biopha. 2014.03.007
  • Suda, K., Rothen-Rutishauser, B., Gunthert, M., & Wunderli-Allenspach, H. (2011). Phenotypic Characterization Of Human Umbilical Vein Endothelial (ECV304) And Urinary Carcinoma (T24) Cells: Endothelial Versus Epithelial Features. In Vitro Cellular & Developmental Biology, 37, 505-514. https://doi.org/10.1290/1071-2690(2001)037<0505:PCOHUV>2.0.CO;2
  • Şeker Karatoprak, G., Ökdem, B., İlgün, S., & Koşar, M. (2022). Evaluation of Antioxidant and Antimicrobial Activities of Potentilla recta L. KSU Journal of Agriculture and Nature, 25(3), 439-448. https://doi.org/10.18016/ksutarimdoga.vi.894015.
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There are 36 citations in total.

Details

Primary Language English
Subjects Structural Biology
Journal Section RESEARCH ARTICLE
Authors

Belkis Atasever Arslan 0000-0001-5827-8484

Kaan Yılancıoğlu 0000-0001-7105-0898

Ahmet Can Timuçin 0000-0002-9483-3593

Zeynep Kalkan 0000-0002-4495-766X

Seda Kuşoğlu Gültekin 0000-0003-0674-1582

Selim Çetiner 0000-0002-9679-2748

Project Number Project No: 113S251
Publication Date June 30, 2023
Submission Date May 5, 2022
Acceptance Date October 12, 2022
Published in Issue Year 2023

Cite

APA Atasever Arslan, B., Yılancıoğlu, K., Timuçin, A. C., Kalkan, Z., et al. (2023). Selective Cytotoxicity of Chemical Composition of Spirulina platensis Extract In Endometrial Cells: In Vitro and In Silico Approach. Kahramanmaraş Sütçü İmam Üniversitesi Tarım Ve Doğa Dergisi, 26(3), 493-503. https://doi.org/10.18016/ksutarimdoga.vi.1110478

21082



2022-JIF = 0.500

2022-JCI = 0.170

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