Research Article
BibTex RIS Cite

The Effect of the Morphology of Silver Nanoparticles on Their Interactions with Proteins

Year 2024, Volume: 26 Issue: 76, 82 - 89, 23.01.2024
https://doi.org/10.21205/deufmd.2024267610

Abstract

In parallel with the developments in nanotechnology, there has been a rapid increase in the number of nanoparticles used in biomedical applications. Silver nanoparticles stand out among different metallic nanoparticle groups because the advantages they offer (e.g., antibacterial activity) mostly overlap with the needs of medical applications. However, the structural features and surface properties that make silver nanoparticles advantageous in biomedical applications can be altered as a result of interactions with the biological environment, which, in turn, is reflected in the biological activity and functionality of nanoparticles. It is well-reported in the literature that the main factor responsible for the changing surface properties of nanoparticles in biological environments is the proteins attached to their surfaces, forming a so-called protein-corona layer around nanoparticles. However, the effect of the morphological properties of nanoparticles on the composition and amount of this protein corona layer formed has not been fully elucidated. In this study, the effect of silver nanoparticles’ morphology on nanoparticle-protein interactions was investigated. To that end, silver nanoparticles of spherical and prismatic shape were characterized in detail and the proteins attached to their surfaces were determined qualitatively by the sodium dodecyl sulfate–polyacrylamide gel electrophoresis (SDS–PAGE) method. More specifically, silver nanoparticles with spherical and prismatic morphology were incubated in protein-suplemented cell culture medium at different durations (15 min, 2 h and 24 h) and temperatures (22 oC and 37 oC), and the proteins attached to their surfaces were compared in terms of type and amount.

References

  • Poole, C.P., Owens, F.J. 2003. Introduction to Nanotechnology.
  • Hulla, J., Sahu, S., Hayes, A. 2015. Nanotechnology: History and future. Human & experimental toxicology, Cilt. 34(12), s. 1318-1321. DOI: 10.1177/0960327115603588
  • Tran, L., M.A. Bañares, and R. Rallo, Modelling the toxicity of nanoparticles. 2017: Springer. DOI: 10.1007/978-3-319-47754-1
  • Tantra, R., et al., A method for assessing nanomaterial dispersion quality based on principal component analysis of particle size distribution data. Particuology, 2015. 22: p. 30-38. DOI: 10.1016/j.partic.2014.10.004
  • Akhter, M.H., et al., Impact of protein corona on the biological identity of nanomedicine: understanding the fate of nanomaterials in the biological milieu. Biomedicines, 2021. 9(10): p. 1496. DOI: 10.3390/biomedicines9101496
  • Joudeh, N., Linke, D. 2022. Nanoparticle classification, physicochemical properties, characterization, and applications: a comprehensive review for biologists. Journal of Nanobiotechnology, Cilt. 20(1), s. 262. DOI: 10.1186/s12951-022-01477-8
  • Ravindran, A., Chandran, P., Khan, S.S. 2013. Biofunctionalized silver nanoparticles: advances and prospects. Colloids and Surfaces B: Biointerfaces, Cilt. 105, s. 342-352. DOI: 10.1016/j.colsurfb.2012.07.036
  • Rai, M., Yadav, A., Gade, A. 2009. Silver nanoparticles as a new generation of antimicrobials. Biotechnology advances, Cilt. 27(1), s. 76-83. DOI: 10.1016/j.biotechadv.2008.09.002
  • Podila, R., et al., Effects of surface functional groups on the formation of nanoparticle-protein corona. Applied physics letters, 2012. 101(26): p. 263701. DOI: 10.1063/1.4772509
  • Shannahan, J.H., et al., Silver nanoparticle protein corona composition in cell culture media. PloS one, 2013. 8(9): p. e74001. DOI: 10.1371/journal.pone.0074001
  • Lai, W., et al., Interaction of gold and silver nanoparticles with human plasma: Analysis of protein corona reveals specific binding patterns. Colloids and Surfaces B: Biointerfaces, 2017. 152: p. 317-325. DOI: 10.1016/j.colsurfb.2017.01.037
  • Barbalinardo, M., et al., Protein corona mediated uptake and cytotoxicity of silver nanoparticles in mouse embryonic fibroblast. Small, 2018. 14(34): p. 1801219. DOI: 10.1002/smll.201801219
  • Ban, D.K. and S. Paul, Protein corona over silver nanoparticles triggers conformational change of proteins and drop in bactericidal potential of nanoparticles: Polyethylene glycol capping as preventive strategy. Colloids and Surfaces B: Biointerfaces, 2016. 146: p. 577-584. DOI: 10.1016/j.colsurfb.2016.06.050
  • Spagnoletti, F.N., et al., Protein corona on biogenic silver nanoparticles provides higher stability and protects cells from toxicity in comparison to chemical nanoparticles. Journal of Environmental Management, 2021. 297: p. 113434. DOI: 10.1016/j.jenvman.2021.113434
  • Walkey, C.D., et al., Protein corona fingerprinting predicts the cellular interaction of gold and silver nanoparticles. ACS nano, 2014. 8(3): p. 2439-2455. DOI: 10.1021/nn406018q
  • Ashkarran, A.A., et al., Bacterial effects and protein corona evaluations: crucial ignored factors in the prediction of bio-efficacy of various forms of silver nanoparticles. Chemical research in toxicology, 2012. 25(6): p. 1231-1242. DOI: 10.1021/tx300083s
  • Fertsch-Gapp, S., et al., Binding of polystyrene and carbon black nanoparticles to blood serum proteins. Inhalation Toxicology, 2011. 23(8): p. 468-475. DOI: 10.3109/08958378.2011.583944
  • Podila, R. and J.M. Brown, Toxicity of engineered nanomaterials: a physicochemical perspective. Journal of biochemical and molecular toxicology, 2013. 27(1): p. 50-55. DOI: 10.1002/jbt.21442
  • Tomak, A., Cesmeli, S., Hanoglu, B. D., Winkler, D., Oksel Karakus, C. 2021. Nanoparticle-protein corona complex: understanding multiple interactions between environmental factors, corona formation, and biological activity. Nanotoxicology, Cilt. 15(10), s. 1331-1357. DOI: 10.1080/17435390.2022.2025467
  • Lundqvist, M., et al., The evolution of the protein corona around nanoparticles: a test study. ACS nano, 2011. 5(9): p. 7503-7509. DOI: 10.1021/nn202458g
  • Lundqvist, M., et al., Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proceedings of the National Academy of Sciences, 2008. 105(38): p. 14265-14270. DOI: 10.1073/pnas.0805135105
  • Kharazian, B., N. Hadipour, and M. Ejtehadi, Understanding the nanoparticle–protein corona complexes using computational and experimental methods. The international journal of biochemistry & cell biology, 2016. 75: p. 162-174. DOI: 10.1016/j.biocel.2016.02.008
  • Gräfe, C., et al., Intentional formation of a protein corona on nanoparticles: Serum concentration affects protein corona mass, surface charge, and nanoparticle–cell interaction. The international journal of biochemistry & cell biology, 2016. 75: p. 196-202. DOI: 10.1016/j.biocel.2015.11.005
  • Cedervall, T., et al., Understanding the nanoparticle–protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proceedings of the National Academy of Sciences, 2007. 104(7): p. 2050-2055. DOI: 10.1073/pnas.0608582104
  • Monopoli, M.P., et al., Formation and characterization of the nanoparticle–protein corona. Nanomaterial Interfaces in Biology: Methods and Protocols, 2013: p. 137-155. DOI: 10.1007/978-1-62703-462-3_11
  • Gossmann, R., et al., Comparative examination of adsorption of serum proteins on HSA-and PLGA-based nanoparticles using SDS–PAGE and LC–MS. European Journal of Pharmaceutics and Biopharmaceutics, 2015. 93: p. 80-87. DOI: 10.1016/j.ejpb.2015.03.021
  • Di Silvio, D., et al., Technical tip: high-resolution isolation of nanoparticle–protein corona complexes from physiological fluids. Nanoscale, 2015. 7(28): p. 11980-11990. DOI: 10.1039/C5NR02618K
  • Madathiparambil Visalakshan, R., et al., The influence of nanoparticle shape on protein corona formation. Small, 2020. 16(25): p. 2000285. DOI: 10.1002/smll.202000285
  • Tomak, A., Yilancioglu, B., Winkler, D., Karakus, C. O. 2022. Protein corona formation on silver nanoparticles under different conditions. Colloids and Surfaces A: Physicochemical and Engineering Aspects, Cilt. 651, DOI: 10.1016/j.colsurfa.2022.129666
  • Kopac, T. 2021. Protein corona, understanding the nanoparticle–protein interactions and future perspectives: A critical review. International Journal of Biological Macromolecules, Cilt. 169, s. 290-301. DOI: 10.1016/j.ijbiomac.2020.12.108
  • Tuan Anh, M. N., Nguyen, D. T. D., Ke Thanh, N. V., Phuong Phong, N. T., Nguyen, D. H., Nguyen-Le, M. T. 2020. Photochemical synthesis of silver nanodecahedrons under blue LED irradiation and their SERS activity. Processes, Cilt. 8(3), s. 292. DOI: 10.3390/pr8030292
  • Sharifi-Rad, M., Pohl, P. 2020. Synthesis of biogenic silver nanoparticles (Agcl-NPs) using a pulicaria vulgaris gaertn. aerial part extract and their application as antibacterial, antifungal and antioxidant agents. Nanomaterials, Cilt. 10(4), s. 638. DOI: 10.3390/nano10040638
  • Yu, P., Huang, J., & Tang, J. 2011. Observation of coalescence process of silver nanospheres during shape transformation to nanoprisms. Nanoscale Res Lett, Cilt. 6, s. 1-7. DOI: 10.1007/s11671-010-9808-6
  • Miclăuş, T., Beer, C., Chevallier, J., Scavenius, C., Bochenkov, V. E., Enghild, J. J., Sutherland, D. S. 2016. Dynamic protein coronas revealed as a modulator of silver nanoparticle sulphidation in vitro. Nature Communications, Cilt. 7(1), s. 11770. DOI: 10.1038/ncomms11770
  • Akhtar, M. J., Kumar, S., Alhadlaq, H. A., Alrokayan, S. A., Abu-Salah, K. M., Ahamed, M. 2016. Dose-dependent genotoxicity of copper oxide nanoparticles stimulated by reactive oxygen species in human lung epithelial cells. Toxicology and industrial health, Cilt. 32(5), s. 809-821. DOI: 10.1177/0748233713511512
  • Mohammad-Beigi, H., Hayashi, Y., Zeuthen, C. M., Eskandari, H., Scavenius, C., Juul-Madsen, K., Sutherland, D. S. 2020. Mapping and identification of soft corona proteins at nanoparticles and their impact on cellular association. Nature Communications, Cilt. 11(1), s. 4535. DOI: 10.1038/s41467-020-18237-7
  • Jurašin, D. D., Ćurlin, M., Capjak, I., Crnković, T., Lovrić, M., Babič, M., Gajović, S. 2016. Surface coating affects behavior of metallic nanoparticles in a biological environment. Beilstein Journal of Nanotechnology, Cilt. 7(1), s. 246-262. DOI: :10.3762/bjnano.7.23
  • Braun, N.J., et al., Modification of the protein corona–nanoparticle complex by physiological factors. Materials Science and Engineering: C, 2016. 64: p. 34-42. DOI: 10.1016/j.msec.2016.03.0

Gümüş Nanopartiküllerin Morfolojisinin Protein Etkileşimleri Üzerindeki Etkisi

Year 2024, Volume: 26 Issue: 76, 82 - 89, 23.01.2024
https://doi.org/10.21205/deufmd.2024267610

Abstract

Nanoteknolojideki gelişmelere paralel olarak biyomedikal uygulamalarda kullanılan nanopartiküllerin sayısında hızlı bir artış yaşanmıştır. Gümüş nanopartiküller, farklı metalik nanopartikül grupları arasında başta antibakteriyel etkinlik olmak üzere tıbbi uygulamaların gereksinimleriyle örtüşen çeşitli avantajlara sahip olmalari dolayısıyla öne çıkmakta ve yaygın olarak kullanılmaktadır. Gümüş nanopartikülleri avantajlı kılan yapı ve yüzey özellikleri biyolojik ortam etkileşimleri sonucunda değişiklik gösterebilmekte ve bu değişimler dolayısıyla biyolojik aktivite ve foksiyonellik gibi nanopartikül özellikleri de doğrudan etkilenmektedir. Nanopartiküllerin biyolojik ortamlarda değişen yüzey özelliklerinin en büyük nedeninin yüzeylerine tutunan proteinler olduğu bilinmektedir. Ancak nanopartiküllerin morfolojik özelliklerinin etraflarında oluşan bu protein halkasının bileşimine ve miktarına olan etkisi tam olarak aydınlatılmamıştır. Bu çalışmada, partikül morfolojisinin nanopartikül-protein etkileşimleri üzerine etkisi incelenmiştir. Bu amaçla küresel ve prizma-benzeri yapıya sahip gümüş nanopartikülleri detaylı olarak karakterize edilmiş ve yüzeylerine tutunan proteinler sodyum dodesil sülfat–poliakrilamid jel elektroforezi (SDS–PAGE) yöntemiyle analitik olarak tayin edilmiştir. Spesifik olarak, küresel ve prizmatik morfolojiye sahip gümüş nanopartikülleri protein eklentili hücre kültürü ortamı içerisinde farklı süre (15 dk, 2 sa ve 24 sa) ve sıcaklıklarda (22 oC ve 37 oC) inkübe edilmiş ve yüzeylerine tutunan proteinler tür ve miktar açısından karşılaştırılmıştır.

References

  • Poole, C.P., Owens, F.J. 2003. Introduction to Nanotechnology.
  • Hulla, J., Sahu, S., Hayes, A. 2015. Nanotechnology: History and future. Human & experimental toxicology, Cilt. 34(12), s. 1318-1321. DOI: 10.1177/0960327115603588
  • Tran, L., M.A. Bañares, and R. Rallo, Modelling the toxicity of nanoparticles. 2017: Springer. DOI: 10.1007/978-3-319-47754-1
  • Tantra, R., et al., A method for assessing nanomaterial dispersion quality based on principal component analysis of particle size distribution data. Particuology, 2015. 22: p. 30-38. DOI: 10.1016/j.partic.2014.10.004
  • Akhter, M.H., et al., Impact of protein corona on the biological identity of nanomedicine: understanding the fate of nanomaterials in the biological milieu. Biomedicines, 2021. 9(10): p. 1496. DOI: 10.3390/biomedicines9101496
  • Joudeh, N., Linke, D. 2022. Nanoparticle classification, physicochemical properties, characterization, and applications: a comprehensive review for biologists. Journal of Nanobiotechnology, Cilt. 20(1), s. 262. DOI: 10.1186/s12951-022-01477-8
  • Ravindran, A., Chandran, P., Khan, S.S. 2013. Biofunctionalized silver nanoparticles: advances and prospects. Colloids and Surfaces B: Biointerfaces, Cilt. 105, s. 342-352. DOI: 10.1016/j.colsurfb.2012.07.036
  • Rai, M., Yadav, A., Gade, A. 2009. Silver nanoparticles as a new generation of antimicrobials. Biotechnology advances, Cilt. 27(1), s. 76-83. DOI: 10.1016/j.biotechadv.2008.09.002
  • Podila, R., et al., Effects of surface functional groups on the formation of nanoparticle-protein corona. Applied physics letters, 2012. 101(26): p. 263701. DOI: 10.1063/1.4772509
  • Shannahan, J.H., et al., Silver nanoparticle protein corona composition in cell culture media. PloS one, 2013. 8(9): p. e74001. DOI: 10.1371/journal.pone.0074001
  • Lai, W., et al., Interaction of gold and silver nanoparticles with human plasma: Analysis of protein corona reveals specific binding patterns. Colloids and Surfaces B: Biointerfaces, 2017. 152: p. 317-325. DOI: 10.1016/j.colsurfb.2017.01.037
  • Barbalinardo, M., et al., Protein corona mediated uptake and cytotoxicity of silver nanoparticles in mouse embryonic fibroblast. Small, 2018. 14(34): p. 1801219. DOI: 10.1002/smll.201801219
  • Ban, D.K. and S. Paul, Protein corona over silver nanoparticles triggers conformational change of proteins and drop in bactericidal potential of nanoparticles: Polyethylene glycol capping as preventive strategy. Colloids and Surfaces B: Biointerfaces, 2016. 146: p. 577-584. DOI: 10.1016/j.colsurfb.2016.06.050
  • Spagnoletti, F.N., et al., Protein corona on biogenic silver nanoparticles provides higher stability and protects cells from toxicity in comparison to chemical nanoparticles. Journal of Environmental Management, 2021. 297: p. 113434. DOI: 10.1016/j.jenvman.2021.113434
  • Walkey, C.D., et al., Protein corona fingerprinting predicts the cellular interaction of gold and silver nanoparticles. ACS nano, 2014. 8(3): p. 2439-2455. DOI: 10.1021/nn406018q
  • Ashkarran, A.A., et al., Bacterial effects and protein corona evaluations: crucial ignored factors in the prediction of bio-efficacy of various forms of silver nanoparticles. Chemical research in toxicology, 2012. 25(6): p. 1231-1242. DOI: 10.1021/tx300083s
  • Fertsch-Gapp, S., et al., Binding of polystyrene and carbon black nanoparticles to blood serum proteins. Inhalation Toxicology, 2011. 23(8): p. 468-475. DOI: 10.3109/08958378.2011.583944
  • Podila, R. and J.M. Brown, Toxicity of engineered nanomaterials: a physicochemical perspective. Journal of biochemical and molecular toxicology, 2013. 27(1): p. 50-55. DOI: 10.1002/jbt.21442
  • Tomak, A., Cesmeli, S., Hanoglu, B. D., Winkler, D., Oksel Karakus, C. 2021. Nanoparticle-protein corona complex: understanding multiple interactions between environmental factors, corona formation, and biological activity. Nanotoxicology, Cilt. 15(10), s. 1331-1357. DOI: 10.1080/17435390.2022.2025467
  • Lundqvist, M., et al., The evolution of the protein corona around nanoparticles: a test study. ACS nano, 2011. 5(9): p. 7503-7509. DOI: 10.1021/nn202458g
  • Lundqvist, M., et al., Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proceedings of the National Academy of Sciences, 2008. 105(38): p. 14265-14270. DOI: 10.1073/pnas.0805135105
  • Kharazian, B., N. Hadipour, and M. Ejtehadi, Understanding the nanoparticle–protein corona complexes using computational and experimental methods. The international journal of biochemistry & cell biology, 2016. 75: p. 162-174. DOI: 10.1016/j.biocel.2016.02.008
  • Gräfe, C., et al., Intentional formation of a protein corona on nanoparticles: Serum concentration affects protein corona mass, surface charge, and nanoparticle–cell interaction. The international journal of biochemistry & cell biology, 2016. 75: p. 196-202. DOI: 10.1016/j.biocel.2015.11.005
  • Cedervall, T., et al., Understanding the nanoparticle–protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proceedings of the National Academy of Sciences, 2007. 104(7): p. 2050-2055. DOI: 10.1073/pnas.0608582104
  • Monopoli, M.P., et al., Formation and characterization of the nanoparticle–protein corona. Nanomaterial Interfaces in Biology: Methods and Protocols, 2013: p. 137-155. DOI: 10.1007/978-1-62703-462-3_11
  • Gossmann, R., et al., Comparative examination of adsorption of serum proteins on HSA-and PLGA-based nanoparticles using SDS–PAGE and LC–MS. European Journal of Pharmaceutics and Biopharmaceutics, 2015. 93: p. 80-87. DOI: 10.1016/j.ejpb.2015.03.021
  • Di Silvio, D., et al., Technical tip: high-resolution isolation of nanoparticle–protein corona complexes from physiological fluids. Nanoscale, 2015. 7(28): p. 11980-11990. DOI: 10.1039/C5NR02618K
  • Madathiparambil Visalakshan, R., et al., The influence of nanoparticle shape on protein corona formation. Small, 2020. 16(25): p. 2000285. DOI: 10.1002/smll.202000285
  • Tomak, A., Yilancioglu, B., Winkler, D., Karakus, C. O. 2022. Protein corona formation on silver nanoparticles under different conditions. Colloids and Surfaces A: Physicochemical and Engineering Aspects, Cilt. 651, DOI: 10.1016/j.colsurfa.2022.129666
  • Kopac, T. 2021. Protein corona, understanding the nanoparticle–protein interactions and future perspectives: A critical review. International Journal of Biological Macromolecules, Cilt. 169, s. 290-301. DOI: 10.1016/j.ijbiomac.2020.12.108
  • Tuan Anh, M. N., Nguyen, D. T. D., Ke Thanh, N. V., Phuong Phong, N. T., Nguyen, D. H., Nguyen-Le, M. T. 2020. Photochemical synthesis of silver nanodecahedrons under blue LED irradiation and their SERS activity. Processes, Cilt. 8(3), s. 292. DOI: 10.3390/pr8030292
  • Sharifi-Rad, M., Pohl, P. 2020. Synthesis of biogenic silver nanoparticles (Agcl-NPs) using a pulicaria vulgaris gaertn. aerial part extract and their application as antibacterial, antifungal and antioxidant agents. Nanomaterials, Cilt. 10(4), s. 638. DOI: 10.3390/nano10040638
  • Yu, P., Huang, J., & Tang, J. 2011. Observation of coalescence process of silver nanospheres during shape transformation to nanoprisms. Nanoscale Res Lett, Cilt. 6, s. 1-7. DOI: 10.1007/s11671-010-9808-6
  • Miclăuş, T., Beer, C., Chevallier, J., Scavenius, C., Bochenkov, V. E., Enghild, J. J., Sutherland, D. S. 2016. Dynamic protein coronas revealed as a modulator of silver nanoparticle sulphidation in vitro. Nature Communications, Cilt. 7(1), s. 11770. DOI: 10.1038/ncomms11770
  • Akhtar, M. J., Kumar, S., Alhadlaq, H. A., Alrokayan, S. A., Abu-Salah, K. M., Ahamed, M. 2016. Dose-dependent genotoxicity of copper oxide nanoparticles stimulated by reactive oxygen species in human lung epithelial cells. Toxicology and industrial health, Cilt. 32(5), s. 809-821. DOI: 10.1177/0748233713511512
  • Mohammad-Beigi, H., Hayashi, Y., Zeuthen, C. M., Eskandari, H., Scavenius, C., Juul-Madsen, K., Sutherland, D. S. 2020. Mapping and identification of soft corona proteins at nanoparticles and their impact on cellular association. Nature Communications, Cilt. 11(1), s. 4535. DOI: 10.1038/s41467-020-18237-7
  • Jurašin, D. D., Ćurlin, M., Capjak, I., Crnković, T., Lovrić, M., Babič, M., Gajović, S. 2016. Surface coating affects behavior of metallic nanoparticles in a biological environment. Beilstein Journal of Nanotechnology, Cilt. 7(1), s. 246-262. DOI: :10.3762/bjnano.7.23
  • Braun, N.J., et al., Modification of the protein corona–nanoparticle complex by physiological factors. Materials Science and Engineering: C, 2016. 64: p. 34-42. DOI: 10.1016/j.msec.2016.03.0
There are 38 citations in total.

Details

Primary Language Turkish
Subjects Nanomaterials
Journal Section Research Article
Authors

Aysel Tomak 0000-0003-2544-5201

Ceyda Öksel Karakuş 0000-0001-5282-4114

Early Pub Date January 22, 2024
Publication Date January 23, 2024
Published in Issue Year 2024 Volume: 26 Issue: 76

Cite

APA Tomak, A., & Öksel Karakuş, C. (2024). Gümüş Nanopartiküllerin Morfolojisinin Protein Etkileşimleri Üzerindeki Etkisi. Dokuz Eylül Üniversitesi Mühendislik Fakültesi Fen Ve Mühendislik Dergisi, 26(76), 82-89. https://doi.org/10.21205/deufmd.2024267610
AMA Tomak A, Öksel Karakuş C. Gümüş Nanopartiküllerin Morfolojisinin Protein Etkileşimleri Üzerindeki Etkisi. DEUFMD. January 2024;26(76):82-89. doi:10.21205/deufmd.2024267610
Chicago Tomak, Aysel, and Ceyda Öksel Karakuş. “Gümüş Nanopartiküllerin Morfolojisinin Protein Etkileşimleri Üzerindeki Etkisi”. Dokuz Eylül Üniversitesi Mühendislik Fakültesi Fen Ve Mühendislik Dergisi 26, no. 76 (January 2024): 82-89. https://doi.org/10.21205/deufmd.2024267610.
EndNote Tomak A, Öksel Karakuş C (January 1, 2024) Gümüş Nanopartiküllerin Morfolojisinin Protein Etkileşimleri Üzerindeki Etkisi. Dokuz Eylül Üniversitesi Mühendislik Fakültesi Fen ve Mühendislik Dergisi 26 76 82–89.
IEEE A. Tomak and C. Öksel Karakuş, “Gümüş Nanopartiküllerin Morfolojisinin Protein Etkileşimleri Üzerindeki Etkisi”, DEUFMD, vol. 26, no. 76, pp. 82–89, 2024, doi: 10.21205/deufmd.2024267610.
ISNAD Tomak, Aysel - Öksel Karakuş, Ceyda. “Gümüş Nanopartiküllerin Morfolojisinin Protein Etkileşimleri Üzerindeki Etkisi”. Dokuz Eylül Üniversitesi Mühendislik Fakültesi Fen ve Mühendislik Dergisi 26/76 (January 2024), 82-89. https://doi.org/10.21205/deufmd.2024267610.
JAMA Tomak A, Öksel Karakuş C. Gümüş Nanopartiküllerin Morfolojisinin Protein Etkileşimleri Üzerindeki Etkisi. DEUFMD. 2024;26:82–89.
MLA Tomak, Aysel and Ceyda Öksel Karakuş. “Gümüş Nanopartiküllerin Morfolojisinin Protein Etkileşimleri Üzerindeki Etkisi”. Dokuz Eylül Üniversitesi Mühendislik Fakültesi Fen Ve Mühendislik Dergisi, vol. 26, no. 76, 2024, pp. 82-89, doi:10.21205/deufmd.2024267610.
Vancouver Tomak A, Öksel Karakuş C. Gümüş Nanopartiküllerin Morfolojisinin Protein Etkileşimleri Üzerindeki Etkisi. DEUFMD. 2024;26(76):82-9.

Dokuz Eylül Üniversitesi, Mühendislik Fakültesi Dekanlığı Tınaztepe Yerleşkesi, Adatepe Mah. Doğuş Cad. No: 207-I / 35390 Buca-İZMİR.