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Hydrated C60 fullerene enhances parthanatos and induces autophagy-related biomarkers in glioblastoma cell line

Yıl 2022, , 88 - 97, 28.12.2022
https://doi.org/10.46810/tdfd.1172011

Öz

Glioblastoma is one the most aggressive type of brain cancers, which is resistant to resistant chemo- and radio-therapy. Nanoparticles of C60 fullerene derivates develop anticancer activity in various models. In contrast to many chemotherapy agents, this fullerene absolutely nontoxic in wide range of concentrations with respect to normal cells. C60 fullerene is a promising candidate for many biomedical applications. Therefore, we investigated the effect of water soluble hydrated C60 fullerene (HyC60Fn) on the expression of PARP, Beclin1, LC3, and GFAP in human glioblastoma U373 cell. Cell viability and migration were detected by MTT and wound healing-scratch assay, respectively. The expression of PARP, Beclin1, and LC3 were analyzed by western blotting and GFAP was detected with immunocytochemistry. HyC60Fn in a range of doses 0.5 – 2.0 µM decreased cell viability in a dose-dependent manner. Furthermore, the doses of HyC60Fn 1.0 and 2.0 µM noticeably suppressed glioblastoma cell migration. Mechanistically, we defined that HyC60Fn markedly up-regulated Beclin-1 and ratio of LC3-II/LC3-I expression as autophagy markers. Furthermore, water soluble HyC60Fn activated cleaved PARP fragment and consequently parthanatos in glioblastoma U373 cells. Present results demonstrate that HyC60Fn could initiate anti-tumor effect via the combination of severe autophagy flux and parthanatos in glioblastoma cells. Thus, HyC60Fn affects the cell death machinery, at least partially, through modulating glioblastoma cells reactivity and programmed cell death. Our findings suggest that pristine hydrated C60 fullerene could be a promising anti-cancer therapeutics and further study is required

Destekleyen Kurum

Scientific Research Projects Coordination Unit of Bingol University

Proje Numarası

BAP-5-317-2015 and BAP-FEF.2016.00.010.

Teşekkür

Scientific Research Projects Coordination Unit of Bingol University

Kaynakça

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Hydrated C60 fullerene, glioblastoma hücre hattında parthanatosu arttırır ve otofaji ile ilgili biyobelirteçleri indükler

Yıl 2022, , 88 - 97, 28.12.2022
https://doi.org/10.46810/tdfd.1172011

Öz

Glioblastoma, kemo ve radyoterapiye karşı dirençli, en agresif beyin kanseri tiplerinden biridir. C60 fulleren türevi nanopartiküller, çeşitli modellerde antikanser aktivite amacı ile geliştirilmektedir. Birçok kemoterapi ajanının aksine, bu fulleren çeşitli konsantrasyonlarda toksik değildir. C60 fulleren, birçok biyomedikal uygulama için umut verici bir adaydır. Bu nedenle, suda çözünür hydrated C60 fullerene'in (HyC60Fn) insan glioblastoma U373 hücresinde PARP, Beclin1, LC3 ve GFAP ekspresyonu üzerindeki etkileri araştırılmıştır. Hücre canlılığı ve göçü, sırasıyla MTT ve yara iyileşmesi testi ile belirlendi. PARP, Beclin1 ve LC3 ekspresyonu western blot ile ve GFAP ise immünositokimya ile tespit edildi. 0.5 – 2.0 µM doz aralığındaki HyC60Fn, doza bağlı bir şekilde hücre canlılığını azalttığı belirlendi. Ayrıca, HyC60Fn 1.0 ve 2.0 µM dozları, glioblastoma hücre göçünü belirgin şekilde bastırmıştır. Mekanizma olarak, HyC60Fn'nin otofaji belirteçleri olarak Beclin-1'i ve LC3-II/LC3-I ekspresyon oranını belirgin şekilde yukarı regüle ettiği belirlendi. Ayrıca, suda çözünür HyC60Fn’nin PARP fragmanı ve bu durumun doğal sonuç olarak glioblastoma U373 hücrelerinde parthanatos aktive ettiği belirlendi. Mevcut sonuçlar, HyC60Fn'nin, glioblastoma hücrelerinde şiddetli otofaji akışı ve parthanatos kombinasyonu yoluyla anti-tümör etkisini başlatabildiğini göstermektedir. Bu nedenle HyC60Fn, glioblastoma hücrelerinin reaktivitesini ve programlanmış hücre ölümünü modüle ederek en azından kısmen hücre ölüm mekanizmasını etkiler. Bulgularımız, HyC60Fn 'in umut verici bir kanser karşıtı terapötik olabileceğini ve bu konuda daha fazla çalışmanın gerekli olduğunu göstermektedir.

Proje Numarası

BAP-5-317-2015 and BAP-FEF.2016.00.010.

Kaynakça

  • 1. Sanai N, Polley MY, McDermott MW, Parsa AT, Berger MS. An extent of resection threshold for newly diagnosed glioblastomas: Clinical article. J Neurosurg. 2011 Jul;115(1):3–8.
  • 2. Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, et al. The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Vol. 131, Acta Neuropathologica. Springer Verlag; 2016. p. 803–20.
  • 3. Baldrighi M, Trusel M, Tonini R, Giordani S. Carbon nanomaterials interfacing with neurons: An in vivo perspective. Vol. 10, Frontiers in Neuroscience. Frontiers Media S.A.; 2016. p. 1–27.
  • 4. Song M, Yuan S, Yin J, Wang X, Meng Z, Wang H, et al. Size-dependent toxicity of nano-C60 aggregates: More sensitive indication by apoptosis-related bax translocation in cultured human cells. Environ Sci Technol [Internet]. 2012 Mar 20 [cited 2020 Jul 21];46(6):3457–64.
  • 5. Hsieh FY, Zhilenkov A V., Voronov II, Khakina EA, Mischenko D V., Troshin PA, et al. Water-Soluble Fullerene Derivatives as Brain Medicine: Surface Chemistry Determines if They Are Neuroprotective and Antitumor. ACS Appl Mater Interfaces . 2017;9(13):11482–92.
  • 6. Isakovic A, Markovic Z, Todorovic-Marcovic B, Nikolic N, Vranjes-Djuric S, Mirkovic M, et al. Distinct cytotoxic mechanisms of pristine versus hydroxylated fullerene. Toxicol Sci. 2006;91(1):173–83.
  • 7. Jou MJ. Pathophysiological and pharmacological implications of mitochondria-targeted reactive oxygen species generation in astrocytes. Adv Drug Deliv Rev; 2008 p. 1512–26.
  • 8. Larner SF, Wang J, Goodman J, O’Donoghue Altman MB, Xin M, Wang KKW. In vitro neurotoxicity resulting from exposure of cultured neural cells to several types of nanoparticles. Journal of Cell Death. Libertas Academica Ltd.; 2017
  • 9. Biby TE, Prajitha N, Ashtami J, Sakthikumar D, Maekawa T, Mohanan P V. Toxicity of dextran stabilized fullerene C60 against C6 Glial cells. Brain Res Bull. 2020 Feb 1;155:191–201.
  • 10. Johnston HJ, Hutchison GR, Christensen FM, Aschberger K, Stone V. The Biological Mechanisms and Physicochemical Characteristics Responsible for Driving Fullerene Toxicity. Toxicol Sci . 2010;9;114(2):162–82.
  • 11. Trpkovic A, Todorovic-Markovic B, Trajkovic V. Toxicity of pristine versus functionalized fullerenes: Mechanisms of cell damage and the role of oxidative stress. Archives of Toxicology. Arch Toxicol; 2012 p. 1809–27.
  • 12. Markovic Z, Trajkovic V. Biomedical potential of the reactive oxygen species generation and quenching by fullerenes (C60). Biomaterials. Biomaterials; 2008 p. 3561–73.
  • 13. Li J, Tian M, Cui L, Dwyer J, Fullwood NJ, Shen H, et al. Low-dose carbon-based nanoparticle-induced effects in A549 lung cells determined by biospectroscopy are associated with increases in genomic methylation. Sci Rep. 2016 2;6(1):1–11.
  • 14. Sosnowska M, Kutwin M, Jaworski S, Strojny B, Wierzbicki M, Szczepaniak J, et al. <p>Mechano-signalling, induced by fullerene C60 nanofilms, arrests the cell cycle in the G2/M phase and decreases proliferation of liver cancer cells</p>. Int J Nanomedicine. 2019, 6 14:6197–215.
  • 15. Wierzbicki M, Sawosz E, Grodzik M, Prasek M, Jaworski S, Chwalibog A. Comparison of anti-angiogenic properties of pristine carbon nanoparticles. Nanoscale Res Lett. 2013;8(1):1–8.
  • 16. Ye S, Chen M, Jiang Y, Chen M, Zhou T, Wang Y, et al. Polyhydroxylated fullerene attenuates oxidative stress-induced apoptosis via a fortifying Nrf2-regulated cellular antioxidant defence system. Int J Nanomedicine . 2014 29;9(1):2073–87.
  • 17. Demir E, Nedzvetsky VS, Ağca CA, Kirici M. Pristine C60 Fullerene Nanoparticles Ameliorate Hyperglycemia-Induced Disturbances via Modulation of Apoptosis and Autophagy Flux. Neurochem Res. 2020;1;45(10):2385–97. 18. Kumari S, Badana AK, Murali Mohan G, Shailender G, Malla RR. Reactive Oxygen Species: A Key Constituent in Cancer Survival. Biomarker Insights. SAGE Publications Ltd; 2018.
  • 19. Yang H, Villani RM, Wang H, Simpson MJ, Roberts MS, Tang M, et al. The role of cellular reactive oxygen species in cancer chemotherapy. Journal of Experimental and Clinical Cancer Research. BioMed Central Ltd.; 2018 p. 266.
  • 20. Mijatović S, Savić-Radojević A, Plješa-Ercegovac M, Simić T, Nicoletti F, Maksimović-Ivanić D. The Double-Faced Role of Nitric Oxide and Reactive Oxygen Species in Solid Tumors. Antioxidants. 2020; 30;9(5):374.
  • 21. Moloney JN, Cotter TG. ROS signalling in the biology of cancer. Seminars in Cell and Developmental Biology. Elsevier Ltd; 2018. p. 50–64.
  • 22. Galadari S, Rahman A, Pallichankandy S, Thayyullathil F. Reactive oxygen species and cancer paradox: To promote or to suppress? Free Radical Biology and Medicine. Elsevier Inc.; 2017. p. 144–64.
  • 23. Etem EO, Bal R, Akaǧaç AE, Kuloglu T, Tuzcu M, Andrievsky G V., et al. The effects of hydrated C(60) fullerene on gene expression profile of TRPM2 and TRPM7 in hyperhomocysteinemic mice. J Recept Signal Transduct. 2014;34(4):317–24.
  • 24. Eisele G, Weller M. Targeting apoptosis pathways in glioblastoma [Internet]. Vol. 332, Cancer Letters. Elsevier Ireland Ltd; 2013. p. 335–45.
  • 25. Wong RSY. Apoptosis in cancer: From pathogenesis to treatment [Internet]. Vol. 30, Journal of Experimental and Clinical Cancer Research. BioMed Central; 2011. p. 87.
  • 26. Kaza N, Kohli L, Roth KA. Autophagy in brain tumors: A new target for therapeutic intervention. In: Brain Pathology. 2012. p. 89–98.
  • 27. Yang K, Niu L, Bai Y, Le W. Glioblastoma: Targeting the autophagy in tumorigenesis. Vol. 153, Brain Research Bulletin. Elsevier Inc.; 2019. p. 334–40.
  • 28. Levine B, Kroemer G. Autophagy in the Pathogenesis of Disease. Vol. 132, Cell. 2008. p. 27–42.
  • 29. Feng F, Zhang M, Yang C, Heng X, Wu X. The dual roles of autophagy in gliomagenesis and clinical therapy strategies based on autophagic regulation mechanisms. Biomedicine and Pharmacotherapy. 2019.
  • 30. Mizushima N, Levine B. Autophagy in mammalian development and differentiation. Vol. 12, Nature Cell Biology. Nature Publishing Group; 2010. p. 823–30.
  • 31. Wang F, Jin C, Liang H, Tang Y, Zhang H, Yang Y. Effects of fullerene C60 nanoparticles on A549 cells. Environ Toxicol Pharmacol. 2014;1;37(2):656–61.
  • 32. Hu Z, Guan W, Wang W, Zhu Z, Wang Y. Folacin C60 derivative exerts a protective activity against oxidative stress-induced apoptosis in rat pheochromocytoma cells. Bioorganic Med Chem Lett. 2010;15;20(14):4159–62.
  • 33. Zhou YY, Li Y, Jiang WQ, Zhou LF. MAPK/JNK signalling: A potential autophagy regulation pathway. Biosci Rep. 2015;35(3):1–10.
  • 34. Lee CM, Huang ST, Huang SH, Lin HW, Tsai HP, Wu JY, et al. C60 fullerene-pentoxifylline dyad nanoparticles enhance autophagy to avoid cytotoxic effects caused by the β-amyloid peptide. Nanomedicine Nanotechnology, Biol Med. 2011;1;7(1):107–14.
  • 35. Hartman ML. Non-Apoptotic Cell Death Signaling Pathways in Melanoma. Int J Mol Sci. 2020; 23;21(8):2980.
  • 36. Fatokun A. Parthanatos: Poly adp ribose polymerase (parp)-mediated cell death. In: Apoptosis and Beyond: The Many Ways Cells Die. 2018. p. 535–58.
  • 37. Liu SY, Song JY, Fan B, Wang Y, Pan YR, Che L, et al. Resveratrol protects photoreceptors by blocking caspase- and PARP-dependent cell death pathways. Free Radic Biol Med. 2018 Dec 1;129:569–81.
  • 38. Harhaji L, Isakovic A, Raicevic N, Markovic Z, Todorovic-Markovic B, Nikolic N, et al. Multiple mechanisms underlying the anticancer action of nanocrystalline fullerene. Eur J Pharmacol. 2007 Jul 30;568(1–3):89–98.
  • 39. Pan Y, Jing R, Pitre A, Williams BJ, Skalli O. Intermediate filament protein synemin contributes to the migratory properties of astrocytoma cells by influencing the dynamics of the actin cytoskeleton. FASEB J. 2008;22(9):3196–206.
  • 40. Moeton M, Stassen OMJA, Sluijs JA, van der Meer VWN, Kluivers LJ, van Hoorn H, et al. GFAP isoforms control intermediate filament network dynamics, cell morphology, and focal adhesions. Cell Mol Life Sci. 2016;3 ;73(21):4101–20.
  • 41. Agca CA, Tykhomyrov AA, Baydas G, Nedzvetsky VS. Effects of a Propolis Extract on the Viability of and Levels of Cytoskeletal and Regulatory Proteins in Rat Brain Astrocytes: an In Vitro Study. Neurophysiology. 2017 Aug 1;49(4):261–71.
  • 42. Tykhomyrov A, Nedzvetsky V, Shemet S, Ağca CA. Production and characterization of polyclonal antibodies to human recombinant domain B-free antihemophilic factor VIII. Turkish J Biol. 2017;41(6):857–67.
  • 43. Thayyullathil F, Rahman A, Pallichankandy S, Patel M, Galadari S. ROS-dependent prostate apoptosis response-4 (Par-4) up-regulation and ceramide generation are the prime signaling events associated with curcumin-induced autophagic cell death in human malignant glioma. FEBS Open Bio. 2014;1;4:763–76.
  • 44. Gong K, Chen C, Zhan Y, Chen Y, Huang Z, Li W. Autophagy-related gene 7 (ATG7) and reactive oxygen species/extracellular signal-regulated kinase regulate tetrandrine-induced autophagy in human hepatocellular carcinoma. J Biol Chem. 2012 Oct 12;287(42):35576–88.
  • 45. Dal Forno GO, Kist LW, De Azevedo MB, Fritsch RS, Pereira TCB, Britto RS, et al. Intraperitoneal exposure to nano/microparticles of fullerene (C 60) increases acetylcholinesterase activity and lipid peroxidation in adult zebrafish (danio rerio) Brain. Biomed Res Int. 2013.
  • 46. Peng Y, Yang D, Lu W, Hu X, Hong H, Cai T. Positron emission tomography (PET) guided glioblastoma targeting by a fullerene-based nanoplatform with fast renal clearance. Acta Biomater. 2017; 1 ;61:193–203.
  • 47. Butler D, Bahr BA. Oxidative stress and lysosomes: CNS-related consequences and implications for lysosomal enhancement strategies and induction of autophagy. Antioxidants and Redox Signaling. Antioxid Redox Signal; 2006 p. 185–96.
  • 48. Gonzalez CD, Lee MS, Marchetti P, Pietropaolo M, Towns R, Vaccaro MI, et al. The emerging role of autophagy in the pathophysiology of diabetes mellitus. Autophagy. Taylor and Francis Inc.; 2011. p. 2–11.
  • 49. Maiuri MC, Le Toumelin G, Criollo A, Rain JC, Gautier F, Juin P, et al. Functional and physical interaction between Bcl-XL and a BH3-like domain in Beclin-1. EMBO J. 2007 ;16;26(10):2527–39.
  • 50. Seyfried TN, Shelton LM. Cancer as a metabolic disease [Internet]. Vol. 7, Nutrition and Metabolism. 2010. p. 1–22.
  • 51. Decuypere J-P, Parys JB, Bultynck G. Regulation of the Autophagic Bcl-2/Beclin 1 Interaction. Cells . 2012 ;6;1(3):284–312.
  • 52. Fatokun AA, Dawson VL, Dawson TM. Parthanatos: Mitochondrial-linked mechanisms and therapeutic opportunities [Internet]. Vol. 171, British Journal of Pharmacology. Nature Publishing Group; 2014 ; p. 2000–16.
  • 53. Jannetti SA, Carlucci G, Carney B, Kossatz S, Shenker L, Carter LM, et al. PARP-1-targeted radiotherapy in mouse models of glioblastoma. J Nucl Med. 2018;1;59(8):1225–33.
  • 54. Majuelos-Melguizo J, Rodríguez MI, López-Jiménez L, Rodríguez-Vargas JM, Martín-Consuegra JMM, Serrano-Sáenz S, et al. PARP targeting counteracts gliomagenesis through induction of mitotic catastrophe and aggravation of deficiency in homologous recombination in PTEN-mutant glioma. Oncotarget. 2015;6(7):4790–803.
  • 55. Dugan LL, Gabrielsen JK, Yu SP, Lin TS, Choi DW. Buckminsterfullerenol free radical scavengers reduce excitotoxic and apoptotic death of cultured cortical neurons. Neurobiol Dis. 1996;3(2):129–35.
  • 56. Makarova EG, Gordon RY, Podolski IY. Fullerene C 60 prevents neurotoxicity induced by intrahippocampal microinjection of amyloid-β peptide. In: Journal of Nanoscience and Nanotechnology. J Nanosci Nanotechnol; 2012. p. 119–26.
  • 57. Giust D, Da Ros T, Martín M, Albasanz JL. [C60]Fullerene derivative modulates adenosine and metabotropic glutamate receptors gene expression: A possible protective effect against hypoxia. J Nanobiotechnology . 2014 14;12(1):27.
  • 58. Tsumoto H, Kawahara S, Fujisawa Y, Suzuki T, Nakagawa H, Kohda K, et al. Syntheses of water-soluble [60]fullerene derivatives and their enhancing effect on neurite outgrowth in NGF-treated PC12 cells. Bioorganic Med Chem Lett. 2010;15;20(6):1948–52.
  • 59. Kraemer ÂB, Parfitt GM, Acosta D da S, Bruch GE, Cordeiro MF, Marins LF, et al. Fullerene (C60) particle size implications in neurotoxicity following infusion into the hippocampi of Wistar rats. Toxicol Appl Pharmacol. 2018 ; 1;338:197–203.
  • 60. Mori T, Takada H, Ito S, Matsubayashi K, Miwa N, Sawaguchi T. Preclinical studies on safety of fullerene upon acute oral administration and evaluation for no mutagenesis. Toxicology. 2006 ;1;225(1):48–54.
  • 61. Takahashi M, Kato H, Doi Y, Hagiwara A, Hirata-Koizumi M, Ono A, et al. Sub-acute oral toxicity study with fullerene C60 in rats. J Toxicol Sci. 2012;37(2):353–61.
  • 62. Sayes CM, Gobin AM, Ausman KD, Mendez J, West JL, Colvin VL. Nano-C60 cytotoxicity is due to lipid peroxidation. Biomaterials. 2005;26(36):7587–95.
  • 63. Lagos-Cabré R, Alvarez A, Kong M, Burgos-Bravo F, Cárdenas A, Rojas-Mancilla E, et al. αVβ3 Integrin regulates astrocyte reactivity. J Neuroinflammation. 2017;14(1).
  • 64. Yang HY, Lieska N, Shao D, Kriho V, Pappas GD. Proteins of the intermediate filament cytoskeleton as markers for astrocytes and human astrocytomas. Mol Chem Neuropathol. 1994;21(2–3):155–76.
  • 65. Baydas G, Nedzvetskii VS, Kirichenko S V., Nerush PA. Astrogliosis in the hippocampus and cortex and cognitive deficits in rats with streptozotocin-induced diabetes: Effects of melatonin. Neurophysiology. 2008;40(2):91–7.
  • 66. Tykhomyrov AA, Nedzvetsky VS, Klochkov VK, Andrievsky G V. Nanostructures of hydrated C60 fullerene (C60HyFn) protect rat brain against alcohol impact and attenuate behavioral impairments of alcoholized animals. Toxicology. 2008 Apr 18;246(2–3):158–65.
  • 67. Nedzvetsky V, Andrievsky G. Differences in Antioxidant/Protective Efficacy of Hydrated C60 Fullerene Nanostructures in Liver and Brain of Rats with Streptozotocin-Induced Diabetes. J Diabetes Metab. 2012;03(08).
  • 68. Nedzvetskii VS, Pryshchepa I V., Tykhomyrov AA, Baydas G. Inhibition of Reactive Gliosis in the Retina of Rats with Streptozotocin-Induced Diabetes under the Action of Hydrated C60 Fullerene. Neurophysiology. 2016 Apr 1;48(2):130–40.
  • 69. Rozhkov SP, Goryunov AS, Sukhanova GA, Borisova AG, Rozhkova NN, Andrievsky G V. Protein interaction with hydrated C60 fullerene in aqueous solutions. Biochem Biophys Res Commun [Internet]. 2003 Apr 4 [cited 2021 Feb 25];303(2):562–6.
Toplam 68 adet kaynakça vardır.

Ayrıntılar

Birincil Dil Türkçe
Konular Sağlık Kurumları Yönetimi
Bölüm Makaleler
Yazarlar

Aryan M. Faraj 0000-0002-7229-3717

Victor Nedzvetsky 0000-0001-7352-441X

Artem Tykhomyrov 0000-0003-2063-4636

Gıyasettin Baydaş 0000-0002-9206-3177

Abdullah Aslan 0000-0002-6243-4221

Can Ali Agca 0000-0002-0244-3767

Proje Numarası BAP-5-317-2015 and BAP-FEF.2016.00.010.
Yayımlanma Tarihi 28 Aralık 2022
Yayımlandığı Sayı Yıl 2022

Kaynak Göster

APA Faraj, A. M., Nedzvetsky, V., Tykhomyrov, A., Baydaş, G., vd. (2022). Hydrated C60 fullerene, glioblastoma hücre hattında parthanatosu arttırır ve otofaji ile ilgili biyobelirteçleri indükler. Türk Doğa Ve Fen Dergisi, 11(4), 88-97. https://doi.org/10.46810/tdfd.1172011
AMA Faraj AM, Nedzvetsky V, Tykhomyrov A, Baydaş G, Aslan A, Agca CA. Hydrated C60 fullerene, glioblastoma hücre hattında parthanatosu arttırır ve otofaji ile ilgili biyobelirteçleri indükler. TDFD. Aralık 2022;11(4):88-97. doi:10.46810/tdfd.1172011
Chicago Faraj, Aryan M., Victor Nedzvetsky, Artem Tykhomyrov, Gıyasettin Baydaş, Abdullah Aslan, ve Can Ali Agca. “Hydrated C60 Fullerene, Glioblastoma hücre hattında Parthanatosu arttırır Ve Otofaji Ile Ilgili biyobelirteçleri indükler”. Türk Doğa Ve Fen Dergisi 11, sy. 4 (Aralık 2022): 88-97. https://doi.org/10.46810/tdfd.1172011.
EndNote Faraj AM, Nedzvetsky V, Tykhomyrov A, Baydaş G, Aslan A, Agca CA (01 Aralık 2022) Hydrated C60 fullerene, glioblastoma hücre hattında parthanatosu arttırır ve otofaji ile ilgili biyobelirteçleri indükler. Türk Doğa ve Fen Dergisi 11 4 88–97.
IEEE A. M. Faraj, V. Nedzvetsky, A. Tykhomyrov, G. Baydaş, A. Aslan, ve C. A. Agca, “Hydrated C60 fullerene, glioblastoma hücre hattında parthanatosu arttırır ve otofaji ile ilgili biyobelirteçleri indükler”, TDFD, c. 11, sy. 4, ss. 88–97, 2022, doi: 10.46810/tdfd.1172011.
ISNAD Faraj, Aryan M. vd. “Hydrated C60 Fullerene, Glioblastoma hücre hattında Parthanatosu arttırır Ve Otofaji Ile Ilgili biyobelirteçleri indükler”. Türk Doğa ve Fen Dergisi 11/4 (Aralık 2022), 88-97. https://doi.org/10.46810/tdfd.1172011.
JAMA Faraj AM, Nedzvetsky V, Tykhomyrov A, Baydaş G, Aslan A, Agca CA. Hydrated C60 fullerene, glioblastoma hücre hattında parthanatosu arttırır ve otofaji ile ilgili biyobelirteçleri indükler. TDFD. 2022;11:88–97.
MLA Faraj, Aryan M. vd. “Hydrated C60 Fullerene, Glioblastoma hücre hattında Parthanatosu arttırır Ve Otofaji Ile Ilgili biyobelirteçleri indükler”. Türk Doğa Ve Fen Dergisi, c. 11, sy. 4, 2022, ss. 88-97, doi:10.46810/tdfd.1172011.
Vancouver Faraj AM, Nedzvetsky V, Tykhomyrov A, Baydaş G, Aslan A, Agca CA. Hydrated C60 fullerene, glioblastoma hücre hattında parthanatosu arttırır ve otofaji ile ilgili biyobelirteçleri indükler. TDFD. 2022;11(4):88-97.