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In Silico Binding Affinities of the Molecules in Camellia Sinensis Teas to NLRP3 NACHT Domain

Yıl 2023, Cilt: 12 Sayı: 3, 910 - 917, 26.09.2023
https://doi.org/10.37989/gumussagbil.1273863

Öz

NLRP3 inflammasome secretes proinflammatory cytokines in response to microbial infection and cellular damage, induces pyroptotic cell death, and triggers many pathological conditions. For this reason, it is important to determine the products that can inhibit the NLRP3 protein. In this study, the affinities of 27 molecules in Camellia sinensis tea species to ADP and inhibitor cavities in the NACHT domain of NLRP3 were analyzed in silico using molecular docking, molecular dynamics simulation, and free energy calculation method MM/GBSA. Among the components, theaflavic acid, (-)-epicatechin gallate and (-)-epigallocatechin gallate gave better binding affinities. It was concluded that it would be beneficial to conduct advanced studies on whether these three compounds contribute to the preventability of NLRP3-mediated inflammatory diseases.

Teşekkür

The numerical calculations expressed in this paper were performed at TUBITAK ULAKBIM, High Performance, and Grid Computing Center (TRUBA resources).

Kaynakça

  • 1. Fan, F. S. (2022). "Inhibition of NLRP3 inflammasome activation by caffeine might be a potential mechanism to reduce the risk of squamous cell carcinoma of the oral cavity and oropharynx with coffee drinking". Frontiers in Oral Health, 3(1), 1-4.
  • 2. Xu, J. and Núñez, G. (2022). "The NLRP3 inflammasome: activation and regulation". Trends in Biochemical Sciences, 48(4), 331-344.
  • 3. Zheng, Y, Xu, L, Dong, N. and Li, F. (2022). "NLRP3 inflammasome: The rising star in cardiovascular diseases". Frontiers in Cardiovascular Medicine, 9(1), 1-20.
  • 4. El-Sayed, S, Freeman, S. and Bryce, R. A. (2022). "A Selective Review and Virtual Screening Analysis of Natural Product Inhibitors of the NLRP3 Inflammasome". Molecules, 27(19), 6213.
  • 5. Toldo, S, Mezzaroma, E, Buckley, L. F, Potere, N, Di Nisio, M, Biondi-Zoccai, G, Van Tassell, B. W. and Abbate, A. (2022). "Targeting the NLRP3 inflammasome in cardiovascular diseases". Pharmacology & therapeutics, 236(1), 1-20.
  • 6. Zhao, T, Li, C, Wang, S. and Song, X. (2022). "Green tea (Camellia sinensis): A review of its phytochemistry, pharmacology, and toxicology". Molecules, 27(12), 3909.
  • 7. Abudureheman, B, Yu, X, Fang, D. and Zhang, H. (2022). "Enzymatic oxidation of tea catechins and its mechanism". Molecules, 27(3), 942.
  • 8. Bag, S, Mondal, A, Majumder, A. and Banik, A. (2022). "Tea and its phytochemicals: Hidden health benefits & modulation of signaling cascade by phytochemicals". Food Chemistry, 371(1), 1-13. 9. Jhang, J.-J, Lu, C.-C, Ho, C.-Y, Cheng, Y.-T. and Yen, G.-C. (2015). "Protective effects of catechin against monosodium urate-induced inflammation through the modulation of NLRP3 inflammasome activation". Journal of Agricultural and Food Chemistry, 63(33), 7343-7352.
  • 10. Vargas-Pozada, E. E, Ramos-Tovar, E, Rodriguez-Callejas, J. D, Cardoso-Lezama, I, Galindo-Gómez, S, Talamás-Lara, D, Vásquez-Garzón, V. R, Arellanes-Robledo, J, Tsutsumi, V. and Villa-Treviño, S. (2022). "Caffeine inhibits NLRP3 inflammasome activation by downregulating TLR4/MAPK/NF-κB signaling pathway in an experimental NASH model". International Journal of Molecular Sciences, 23(17), 9954.
  • 11. Zhao, W, Ma, L, Cai, C. and Gong, X. (2019). "Caffeine inhibits NLRP3 inflammasome activation by suppressing MAPK/NF-κB and A2aR signaling in LPS-Induced THP-1 macrophages". International Journal of Biological Sciences, 15(8), 1571.
  • 12. Jiao, P, Li, W, Shen, L, Li, Y, Yu, L. and Liu, Z. (2020). "The protective effect of doxofylline against lipopolysaccharides (LPS)-induced activation of NLRP3 inflammasome is mediated by SIRT1 in human pulmonary bronchial epithelial cells". Artificial cells, nanomedicine, and biotechnology, 48(1), 687-694.
  • 13. Wu, C, Li, F, Zhang, X, Xu, W, Wang, Y, Yao, Y, Han, Z. and Xia, D. (2022). "(−)-Epicatechin ameliorates monosodium urate-induced acute gouty arthritis through inhibiting NLRP3 inflammasome and the NF-κB signaling pathway". Frontiers in Pharmacology, 13
  • 14. Jena, A. B, Dash, U. C. and Duttaroy, A. K. (2022). "An in silico investigation on the interactions of curcumin and epigallocatechin-3-gallate with NLRP3 inflammasome complex". Biomedicine and Pharmacotherapy, 156113890.
  • 15. El-Shaer, N. O, Hegazy, A. M. and Muhammad, M. H. (2023). "Protective effect of quercetin on pulmonary dysfunction in streptozotocin-induced diabetic rats via inhibition of NLRP3 signaling pathway". Environmental Science and Pollution Research1-9.
  • 16. Burley, S. K, Bhikadiya, C, Bi, C, Bittrich, S, Chen, L, Crichlow, G. V, Christie, C. H, Dalenberg, K, Di Costanzo, L. and Duarte, J. M. (2021). "RCSB Protein Data Bank: powerful new tools for exploring 3D structures of biological macromolecules for basic and applied research and education in fundamental biology, biomedicine, biotechnology, bioengineering and energy sciences". Nucleic Acids Research, 49(D1), 437-451.
  • 17. Dekker, C, Mattes, H, Wright, M, Boettcher, A, Hinniger, A, Hughes, N, Kapps-Fouthier, S, Eder, J, Erbel, P. and Stiefl, N. (2021). "Crystal structure of NLRP3 NACHT domain with an inhibitor defines mechanism of inflammasome inhibition". Journal of Molecular Biology, 433(24), 167309.
  • 18. Colovos, C. and Yeates, T. O. (1993). "Verification of protein structures: patterns of nonbonded atomic interactions". Protein Science, 2(9), 1511-1519.
  • 19. Wiederstein, M. and Sippl, M. J. (2007). "ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins". Nucleic Acids Research, 35(suppl_2), W407-W410.
  • 20. Trott, O. and Olson, A. J. (2010). "AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading". Journal of Computational Chemistry, 31(2), 455-461. 21. Kim, S, Chen, J, Cheng, T, Gindulyte, A, He, J, He, S, Li, Q, Shoemaker, B. A, Thiessen, P. A. and Yu, B. (2023). "PubChem 2023 update". Nucleic Acids Research, 51(D1), D1373-D1380.
  • 22. O'Boyle, N. M, Banck, M, James, C. A, Morley, C, Vandermeersch, T. and Hutchison, G. R. (2011). "Open Babel: An open chemical toolbox". Journal of Cheminformatics, 3(1), 1-14.
  • 23. Samdani, A. and Vetrivel, U. (2018). "POAP: A GNU parallel based multithreaded pipeline of open babel and AutoDock suite for boosted high throughput virtual screening". Computational Biology and Chemistry, 74, 39-48.
  • 24. Halgren, T. A. (1996). "Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94". Journal of Computational Chemistry, 17(5&6), 490-519.
  • 25. Pettersen, E. F, Goddard, T. D, Huang, C. C, Meng, E. C, Couch, G. S, Croll, T. I, Morris, J. H. and Ferrin, T. E. (2021). "UCSF ChimeraX: Structure visualization for researchers, educators, and developers". Protein science, 30(1), 70-82.
  • 26. Pettersen, E. F, Goddard, T. D, Huang, C. C, Couch, G. S, Greenblatt, D. M, Meng, E. C. and Ferrin, T. E. (2004). "UCSF Chimera-A visualization system for exploratory research and analysis". Journal of Computational Chemistry, 25(13), 1605-1612.
  • 27. Sousa da Silva, A. W. and Vranken, W. F. (2012). "ACPYPE-Antechamber python parser interface". BMC Research Notes, 51-8.
  • 28. Jakalian, A, Bush, B. L, Jack, D. B. and Bayly, C. I. (2000). "Fast, efficient generation of high-quality atomic charges. AM1-BCC model: I. Method". Journal of computational chemistry, 21(2), 132-146.
  • 29. Abraham, M. J, Murtola, T, Schulz, R, Páll, S, Smith, J. C, Hess, B. and Lindahl, E. (2015). "GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers". SoftwareX, 1, 119-25.
  • 30. Lindorff-Larsen, K, Piana, S, Palmo, K, Maragakis, P, Klepeis, J. L, Dror, R. O. and Shaw, D. E. (2010). "Improved side‐chain torsion potentials for the Amber ff99SB protein force field". Proteins: Structure, Function, and Bioinformatics, 78(8), 1950-1958.
  • 31. Makov, G. and Payne, M. (1995). "Periodic boundary conditions in ab initio calculations". Physical Review B Condens Matter, 51(7), 4014-4022.
  • 32. Hess, B, Bekker, H, Berendsen, H. J. and Fraaije, J. G. (1997). "LINCS: A linear constraint solver for molecular simulations". Journal of Computational Chemistry, 18(12), 1463-1472.
  • 33. Berendsen, H. J, Postma, J. v, Van Gunsteren, W. F, DiNola, A. and Haak, J. R. (1984). "Molecular dynamics with coupling to an external bath". The Journal of chemical physics, 81(8), 3684-3690.
  • 34. Martoňák, R, Laio, A. and Parrinello, M. (2003). "Predicting crystal structures: the Parrinello-Rahman method revisited". Physical Review Letters, 90(7), 075503.
  • 35. Darden, T, York, D. and Pedersen, L. (1993). "Particle mesh Ewald: An N⋅ log (N) method for Ewald sums in large systems". The Journal of chemical physics, 98(12), 10089-10092.
  • 36. Genheden, S. and Ryde, U. (2015). "The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities". Expert Opinion on Drug Discovery, 10(5), 449-461.
  • 37. Valdés-Tresanco, M. S, Valdés-Tresanco, M. E, Valiente, P. A. and Moreno, E. (2021). "gmx_MMPBSA: a new tool to perform end-state free energy calculations with GROMACS". Journal of Chemical Theory and Computation, 17(10), 6281-6291.
  • 38. Bell, E. W. and Zhang, Y. (2019). "DockRMSD: an open-source tool for atom mapping and RMSD calculation of symmetric molecules through graph isomorphism". Journal of Cheminformatics, 11(1), 1-9. 39. Di, M, Zhang, Q, Wang, J, Xiao, X, Huang, J, Ma, Y, Yang, H. and Li, M. (2022). "Epigallocatechin-3-gallate (EGCG) attenuates inflammatory responses and oxidative stress in lipopolysaccharide (LPS)-induced endometritis via silent information regulator transcript-1 (SIRT1)/nucleotide oligomerization domain (NOD)-like receptor pyrin domain-containing 3 (NLRP3) pathway". Journal of Biochemical and Molecular Toxicology, 36(12), e23203.
  • 40. Yang, R, Chen, J, Jia, Q, Yang, X. and Mehmood, S. (2022). "Epigallocatechin-3-gallate ameliorates renal endoplasmic reticulum stress-mediated inflammation in type 2 diabetic rats". Experimental Biology and Medicine, 247(16), 1410-1419.

Camellia Sinensis Çaylarındaki Moleküllerin NLRP3 NACHT Domainine İn Siliko Bağlanma Afiniteleri

Yıl 2023, Cilt: 12 Sayı: 3, 910 - 917, 26.09.2023
https://doi.org/10.37989/gumussagbil.1273863

Öz

NLRP3 inflamazomu, mikrobiyal enfeksiyona ve hücresel hasara yanıt olarak proinflamatuar sitokinleri salgılar, piroptotik hücre ölümüne neden olur ve birçok patolojik durumu tetikler. Bu nedenle NLRP3 proteinini inhibe edebilen ürünlerin belirlenmesi önemlidir. Bu çalışmada, Camellia sinensis çay türünde bulunan 27 molekülün, NLRP3'ün NACHT domainindeki ADP ve inhibitör kavitelere afiniteleri, moleküler yerleştirme, moleküler dinamik simülasyonu ve serbest enerji hesaplama yöntemi MM/GBSA kullanılarak in siliko olarak analiz edildi. Bileşenler arasında tiflavik asit, (-)-epikateşin gallat ve (-)-epigallokateşin gallat daha iyi bağlanma afiniteleri verdi. Bu üç bileşiğin NLRP3 aracılı inflamatuvar hastalıkların önlenebilirliğine katkı sağlayıp sağlamadığına yönelik ileri çalışmaların yapılmasının faydalı olacağı kanısına varıldı.

Kaynakça

  • 1. Fan, F. S. (2022). "Inhibition of NLRP3 inflammasome activation by caffeine might be a potential mechanism to reduce the risk of squamous cell carcinoma of the oral cavity and oropharynx with coffee drinking". Frontiers in Oral Health, 3(1), 1-4.
  • 2. Xu, J. and Núñez, G. (2022). "The NLRP3 inflammasome: activation and regulation". Trends in Biochemical Sciences, 48(4), 331-344.
  • 3. Zheng, Y, Xu, L, Dong, N. and Li, F. (2022). "NLRP3 inflammasome: The rising star in cardiovascular diseases". Frontiers in Cardiovascular Medicine, 9(1), 1-20.
  • 4. El-Sayed, S, Freeman, S. and Bryce, R. A. (2022). "A Selective Review and Virtual Screening Analysis of Natural Product Inhibitors of the NLRP3 Inflammasome". Molecules, 27(19), 6213.
  • 5. Toldo, S, Mezzaroma, E, Buckley, L. F, Potere, N, Di Nisio, M, Biondi-Zoccai, G, Van Tassell, B. W. and Abbate, A. (2022). "Targeting the NLRP3 inflammasome in cardiovascular diseases". Pharmacology & therapeutics, 236(1), 1-20.
  • 6. Zhao, T, Li, C, Wang, S. and Song, X. (2022). "Green tea (Camellia sinensis): A review of its phytochemistry, pharmacology, and toxicology". Molecules, 27(12), 3909.
  • 7. Abudureheman, B, Yu, X, Fang, D. and Zhang, H. (2022). "Enzymatic oxidation of tea catechins and its mechanism". Molecules, 27(3), 942.
  • 8. Bag, S, Mondal, A, Majumder, A. and Banik, A. (2022). "Tea and its phytochemicals: Hidden health benefits & modulation of signaling cascade by phytochemicals". Food Chemistry, 371(1), 1-13. 9. Jhang, J.-J, Lu, C.-C, Ho, C.-Y, Cheng, Y.-T. and Yen, G.-C. (2015). "Protective effects of catechin against monosodium urate-induced inflammation through the modulation of NLRP3 inflammasome activation". Journal of Agricultural and Food Chemistry, 63(33), 7343-7352.
  • 10. Vargas-Pozada, E. E, Ramos-Tovar, E, Rodriguez-Callejas, J. D, Cardoso-Lezama, I, Galindo-Gómez, S, Talamás-Lara, D, Vásquez-Garzón, V. R, Arellanes-Robledo, J, Tsutsumi, V. and Villa-Treviño, S. (2022). "Caffeine inhibits NLRP3 inflammasome activation by downregulating TLR4/MAPK/NF-κB signaling pathway in an experimental NASH model". International Journal of Molecular Sciences, 23(17), 9954.
  • 11. Zhao, W, Ma, L, Cai, C. and Gong, X. (2019). "Caffeine inhibits NLRP3 inflammasome activation by suppressing MAPK/NF-κB and A2aR signaling in LPS-Induced THP-1 macrophages". International Journal of Biological Sciences, 15(8), 1571.
  • 12. Jiao, P, Li, W, Shen, L, Li, Y, Yu, L. and Liu, Z. (2020). "The protective effect of doxofylline against lipopolysaccharides (LPS)-induced activation of NLRP3 inflammasome is mediated by SIRT1 in human pulmonary bronchial epithelial cells". Artificial cells, nanomedicine, and biotechnology, 48(1), 687-694.
  • 13. Wu, C, Li, F, Zhang, X, Xu, W, Wang, Y, Yao, Y, Han, Z. and Xia, D. (2022). "(−)-Epicatechin ameliorates monosodium urate-induced acute gouty arthritis through inhibiting NLRP3 inflammasome and the NF-κB signaling pathway". Frontiers in Pharmacology, 13
  • 14. Jena, A. B, Dash, U. C. and Duttaroy, A. K. (2022). "An in silico investigation on the interactions of curcumin and epigallocatechin-3-gallate with NLRP3 inflammasome complex". Biomedicine and Pharmacotherapy, 156113890.
  • 15. El-Shaer, N. O, Hegazy, A. M. and Muhammad, M. H. (2023). "Protective effect of quercetin on pulmonary dysfunction in streptozotocin-induced diabetic rats via inhibition of NLRP3 signaling pathway". Environmental Science and Pollution Research1-9.
  • 16. Burley, S. K, Bhikadiya, C, Bi, C, Bittrich, S, Chen, L, Crichlow, G. V, Christie, C. H, Dalenberg, K, Di Costanzo, L. and Duarte, J. M. (2021). "RCSB Protein Data Bank: powerful new tools for exploring 3D structures of biological macromolecules for basic and applied research and education in fundamental biology, biomedicine, biotechnology, bioengineering and energy sciences". Nucleic Acids Research, 49(D1), 437-451.
  • 17. Dekker, C, Mattes, H, Wright, M, Boettcher, A, Hinniger, A, Hughes, N, Kapps-Fouthier, S, Eder, J, Erbel, P. and Stiefl, N. (2021). "Crystal structure of NLRP3 NACHT domain with an inhibitor defines mechanism of inflammasome inhibition". Journal of Molecular Biology, 433(24), 167309.
  • 18. Colovos, C. and Yeates, T. O. (1993). "Verification of protein structures: patterns of nonbonded atomic interactions". Protein Science, 2(9), 1511-1519.
  • 19. Wiederstein, M. and Sippl, M. J. (2007). "ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins". Nucleic Acids Research, 35(suppl_2), W407-W410.
  • 20. Trott, O. and Olson, A. J. (2010). "AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading". Journal of Computational Chemistry, 31(2), 455-461. 21. Kim, S, Chen, J, Cheng, T, Gindulyte, A, He, J, He, S, Li, Q, Shoemaker, B. A, Thiessen, P. A. and Yu, B. (2023). "PubChem 2023 update". Nucleic Acids Research, 51(D1), D1373-D1380.
  • 22. O'Boyle, N. M, Banck, M, James, C. A, Morley, C, Vandermeersch, T. and Hutchison, G. R. (2011). "Open Babel: An open chemical toolbox". Journal of Cheminformatics, 3(1), 1-14.
  • 23. Samdani, A. and Vetrivel, U. (2018). "POAP: A GNU parallel based multithreaded pipeline of open babel and AutoDock suite for boosted high throughput virtual screening". Computational Biology and Chemistry, 74, 39-48.
  • 24. Halgren, T. A. (1996). "Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94". Journal of Computational Chemistry, 17(5&6), 490-519.
  • 25. Pettersen, E. F, Goddard, T. D, Huang, C. C, Meng, E. C, Couch, G. S, Croll, T. I, Morris, J. H. and Ferrin, T. E. (2021). "UCSF ChimeraX: Structure visualization for researchers, educators, and developers". Protein science, 30(1), 70-82.
  • 26. Pettersen, E. F, Goddard, T. D, Huang, C. C, Couch, G. S, Greenblatt, D. M, Meng, E. C. and Ferrin, T. E. (2004). "UCSF Chimera-A visualization system for exploratory research and analysis". Journal of Computational Chemistry, 25(13), 1605-1612.
  • 27. Sousa da Silva, A. W. and Vranken, W. F. (2012). "ACPYPE-Antechamber python parser interface". BMC Research Notes, 51-8.
  • 28. Jakalian, A, Bush, B. L, Jack, D. B. and Bayly, C. I. (2000). "Fast, efficient generation of high-quality atomic charges. AM1-BCC model: I. Method". Journal of computational chemistry, 21(2), 132-146.
  • 29. Abraham, M. J, Murtola, T, Schulz, R, Páll, S, Smith, J. C, Hess, B. and Lindahl, E. (2015). "GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers". SoftwareX, 1, 119-25.
  • 30. Lindorff-Larsen, K, Piana, S, Palmo, K, Maragakis, P, Klepeis, J. L, Dror, R. O. and Shaw, D. E. (2010). "Improved side‐chain torsion potentials for the Amber ff99SB protein force field". Proteins: Structure, Function, and Bioinformatics, 78(8), 1950-1958.
  • 31. Makov, G. and Payne, M. (1995). "Periodic boundary conditions in ab initio calculations". Physical Review B Condens Matter, 51(7), 4014-4022.
  • 32. Hess, B, Bekker, H, Berendsen, H. J. and Fraaije, J. G. (1997). "LINCS: A linear constraint solver for molecular simulations". Journal of Computational Chemistry, 18(12), 1463-1472.
  • 33. Berendsen, H. J, Postma, J. v, Van Gunsteren, W. F, DiNola, A. and Haak, J. R. (1984). "Molecular dynamics with coupling to an external bath". The Journal of chemical physics, 81(8), 3684-3690.
  • 34. Martoňák, R, Laio, A. and Parrinello, M. (2003). "Predicting crystal structures: the Parrinello-Rahman method revisited". Physical Review Letters, 90(7), 075503.
  • 35. Darden, T, York, D. and Pedersen, L. (1993). "Particle mesh Ewald: An N⋅ log (N) method for Ewald sums in large systems". The Journal of chemical physics, 98(12), 10089-10092.
  • 36. Genheden, S. and Ryde, U. (2015). "The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities". Expert Opinion on Drug Discovery, 10(5), 449-461.
  • 37. Valdés-Tresanco, M. S, Valdés-Tresanco, M. E, Valiente, P. A. and Moreno, E. (2021). "gmx_MMPBSA: a new tool to perform end-state free energy calculations with GROMACS". Journal of Chemical Theory and Computation, 17(10), 6281-6291.
  • 38. Bell, E. W. and Zhang, Y. (2019). "DockRMSD: an open-source tool for atom mapping and RMSD calculation of symmetric molecules through graph isomorphism". Journal of Cheminformatics, 11(1), 1-9. 39. Di, M, Zhang, Q, Wang, J, Xiao, X, Huang, J, Ma, Y, Yang, H. and Li, M. (2022). "Epigallocatechin-3-gallate (EGCG) attenuates inflammatory responses and oxidative stress in lipopolysaccharide (LPS)-induced endometritis via silent information regulator transcript-1 (SIRT1)/nucleotide oligomerization domain (NOD)-like receptor pyrin domain-containing 3 (NLRP3) pathway". Journal of Biochemical and Molecular Toxicology, 36(12), e23203.
  • 40. Yang, R, Chen, J, Jia, Q, Yang, X. and Mehmood, S. (2022). "Epigallocatechin-3-gallate ameliorates renal endoplasmic reticulum stress-mediated inflammation in type 2 diabetic rats". Experimental Biology and Medicine, 247(16), 1410-1419.
Toplam 37 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Sağlık Kurumları Yönetimi
Bölüm Araştırma Makaleleri
Yazarlar

Zekeriya Düzgün 0000-0001-6420-6292

Birgül Kural 0000-0003-0730-9660

Yayımlanma Tarihi 26 Eylül 2023
Yayımlandığı Sayı Yıl 2023 Cilt: 12 Sayı: 3

Kaynak Göster

APA Düzgün, Z., & Kural, B. (2023). In Silico Binding Affinities of the Molecules in Camellia Sinensis Teas to NLRP3 NACHT Domain. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi, 12(3), 910-917. https://doi.org/10.37989/gumussagbil.1273863
AMA Düzgün Z, Kural B. In Silico Binding Affinities of the Molecules in Camellia Sinensis Teas to NLRP3 NACHT Domain. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi. Eylül 2023;12(3):910-917. doi:10.37989/gumussagbil.1273863
Chicago Düzgün, Zekeriya, ve Birgül Kural. “In Silico Binding Affinities of the Molecules in Camellia Sinensis Teas to NLRP3 NACHT Domain”. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi 12, sy. 3 (Eylül 2023): 910-17. https://doi.org/10.37989/gumussagbil.1273863.
EndNote Düzgün Z, Kural B (01 Eylül 2023) In Silico Binding Affinities of the Molecules in Camellia Sinensis Teas to NLRP3 NACHT Domain. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi 12 3 910–917.
IEEE Z. Düzgün ve B. Kural, “In Silico Binding Affinities of the Molecules in Camellia Sinensis Teas to NLRP3 NACHT Domain”, Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi, c. 12, sy. 3, ss. 910–917, 2023, doi: 10.37989/gumussagbil.1273863.
ISNAD Düzgün, Zekeriya - Kural, Birgül. “In Silico Binding Affinities of the Molecules in Camellia Sinensis Teas to NLRP3 NACHT Domain”. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi 12/3 (Eylül 2023), 910-917. https://doi.org/10.37989/gumussagbil.1273863.
JAMA Düzgün Z, Kural B. In Silico Binding Affinities of the Molecules in Camellia Sinensis Teas to NLRP3 NACHT Domain. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi. 2023;12:910–917.
MLA Düzgün, Zekeriya ve Birgül Kural. “In Silico Binding Affinities of the Molecules in Camellia Sinensis Teas to NLRP3 NACHT Domain”. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi, c. 12, sy. 3, 2023, ss. 910-7, doi:10.37989/gumussagbil.1273863.
Vancouver Düzgün Z, Kural B. In Silico Binding Affinities of the Molecules in Camellia Sinensis Teas to NLRP3 NACHT Domain. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi. 2023;12(3):910-7.