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Year 2024, Volume: 28 Issue: 6, 2236 - 2242, 28.06.2025

Fersu Gül Asya Çalişir Bilge Debeleç Bütüner

https://doi.org/10.29228/jrp.897

Abstract

References

  • [1] Russell WMS, Burch RL. 1959. (as reprinted 1992). The principles of humane experimental technique. Wheathampstead (UK): Universities Federation for Animal Welfare.
  • [2] Hubrecht RC, Carter E. The 3Rs and Humane Experimental Technique: Implementing Change. Animals (Basel). 2019;9(10):754. https://doi.org/10.3390/ani9100754.
  • [3] Tannenbaum J, Bennett BT. Russell and Burch's 3Rs then and now: the need for clarity in definition and purpose. J Am Assoc Lab Anim Sci. 2015;54(2):120-132.
  • [4] Cacciamali A, Villa R, Dotti S. 3D Cell Cultures: Evolution of an Ancient Tool for New Applications. Front Physiol. 2022;13:836480. https://doi.org/10.3389/fphys.2022.836480.
  • [5] Nunes AS, Barros AS, Costa EC, Moreira AF, Correia IJ. 3D tumor spheroids as in vitro models to mimic in vivo human solid tumors resistance to therapeutic drugs. Biotechnol Bioeng. 2019;116(1):206–226. https://doi.org/10.1002/bit.26845.
  • [6] Ravi M, Paramesh V, Kaviya SR, Anuradha E, Solomon FD. 3D cell culture systems: advantages and applications. J Cell Physiol. 2015;230(1):16-26. https://doi.org/10.1002/jcp.24683.
  • [7] Richter M, Piwocka O, Musielak M, Piotrowski I, Suchorska WM, Trzeciak T. From donor to the lab: A Fascinating journey of primary cell lines. Front Cell Dev Biol. 2021;9:711381. https://doi.org/10.3389/fcell.2021.711381.
  • [8] Pamies D, Hartung T. 21st Century Cell Culture for 21st Century Toxicology. Chem Res Toxicol. 2017 Jan;30(1):43-52. https://doi.org/10.1021/acs.chemrestox.6b00269.
  • [9] Rodrigues T, Kundu B, Silva-Correia J, Kundu SC, Oliveira JM, Reis RL, Correlo VM. Emerging tumor spheroids technologies for 3D in vitro cancer modeling. Pharmacol Ther. 2018;184:201-211. https://doi.org/10.1016/j.pharmthera.2017.10.018.
  • [10] Poornima K, Francis AP, Hoda M, Eladl MA, Subramanian S, Veeraraghavan VP, El-Sherbiny M, Asseri SM, Hussamuldin ABA, Surapaneni KM, Mony U, Rajagopalan R. Implications of Three-Dimensional Cell Culture in Cancer Therapeutic Research. Front Oncol. 2022;12:891673. https://doi.org/10.3389/fonc.2022.891673.
  • [11] Abuwatfa WH, Pitt WG, Husseini GA. Scaffold-based 3D cell culture models in cancer research. J Biomed Sci. 2024;31(1):7. https://doi.org/10.1186/s12929-024-00994-y.
  • [12] Kapałczyńska M, Kolenda T, Przybyła W, Zajączkowska M, Teresiak A, Filas V, Ibbs M, Bliźniak R, Łuczewski Ł, Lamperska K. 2D and 3D cell cultures - a comparison of different types of cancer cell cultures. Arch Med Sci. 2018;14(4):910-919. https://doi.org/10.5114/aoms.2016.63743.
  • [13] Costa EC, Moreira AF, de Melo-Diogo D, Gaspar VM, Carvalho MP, Correia IJ. 3D tumor spheroids: an overview on the tools and techniques used for their analysis. Biotechnol Adv. 2016;34(8):1427-1441. https://doi.org/10.1016/j.biotechadv.2016.11.002.
  • [14] Kochanek SJ, Close DA, Johnston PA. High content screening characterization of head and neck squamous cell carcinoma multicellular tumor spheroid cultures generated in 384-well ultra-low attachment plates to screen for better cancer drug leads. Assay Drug Dev Technol. 2019;17(1):17-36. https://doi.org/10.1089/adt.2018.896.
  • [15] Bédard P, Gauvin S, Ferland K, Caneparo C, Pellerin È, Chabaud S, Bolduc S. Innovative Human Three Dimensional Tissue-Engineered Models as an Alternative to Animal Testing. Bioengineering (Basel). 2020;7(3):115. https://doi.org/10.3390/bioengineering7030115.
  • [16] Thoma CR, Zimmermann M, Agarkova I, Kelm JM, Krek W. 3D cell culture systems modeling tumor growth determinants in cancer target discovery. Adv Drug Deliv Rev. 2014;69–70:29–41. https://doi.org/10.1016/j.addr.2014.03.001.
  • [17] Cacciamali A, Villa R, Dotti S. 3D Cell Cultures: Evolution of an Ancient Tool for New Applications. Front Physiol. 2022;13:836480. https://doi.org/10.3389/fphys.2022.836480.
  • [18] Habanjar O, Diab-Assaf M, Caldefie-Chezet F, Delort L. 3D Cell Culture Systems: Tumor Application, Advantages, and Disadvantages. Int J Mol Sci. 2021;22(22):12200. https://doi.org/10.3390/ijms222212200.
  • [19] Fitzgerald KA, Malhotra M, Curtin CM, O’Brien FJ, O’Driscoll CM. Life in 3D is never flat: 3D models to optimise drug delivery. J Control Release. 2015;215:39–54. https://doi.org/10.1016/j.jconrel.2015.07.020.
  • [20] Peela N, Sam FS, Christenson W, Truong D, Watson AW, Mouneimne G, Ros R, Nikkhah M. A three dimensional micropatterned tumor model for breast cancer cell migration studies. Biomaterials. 2016;81:72-83. https://doi.org/10.1016/j.biomaterials.2015.11.039.
  • [21] Chaicharoenaudomrung N, Kunhorm P, Noisa P. Three-dimensional cell culture systems as an in vitro platform for cancer and stem cell modeling. World J Stem Cells. 2019;11(12):1065-1083. https://doi.org/10.4252/wjsc.v11.i12.1065.
  • [22] Fang Y, Eglen RM. Three-Dimensional Cell Cultures in Drug Discovery and Development. SLAS Discov. 2017;22(5):456-472. https://doi.org/10.1177/1087057117696795.
  • [23] Tung YC, Hsiao AY, Allen SG, Torisawa YS, Ho M, Takayama S. High-throughput 3D spheroid culture and drug testing using a 384 hanging drop array. Analyst. 2011;136(3):473-478. https://doi.org/10.1039/c0an00609b.
  • [24] Haisler WL, Timm DM, Gage JA, Tseng H, Killian TC, Souza GR. Three-dimensional cell culturing by magnetic levitation. Nat Protoc. 2013;8(10):1940-1949. https://doi.org/10.1038/nprot.2013.125.
  • [25] Sant S, Johnston PA. The production of 3D tumor spheroids for cancer drug discovery. Drug Discov Today Technol. 2017;23:27-36. https://doi.org/10.1016/j.ddtec.2017.03.002.
  • [26] Imamura Y, Mukohara T, Shimono Y, Funakoshi Y, Chayahara N, Toyoda M, Kiyota N, Takao S, Kono S, Nakatsura T, Minami H. Comparison of 2D- and 3D-culture models as drug-testing platforms in breast cancer. Oncol Rep. 2015;33(4):1837-1843. https://doi.org/10.3892/or.2015.3767.
  • [27] Costa EC, de Melo-Diogo D, Moreira AF, Carvalho MP, Correia IJ. Spheroids Formation on Non-Adhesive Surfaces by Liquid Overlay Technique: Considerations and Practical Approaches. Biotechnol J. 2018; 13(1). https://doi.org/10.1002/biot.201700417.
  • [28] Zanoni M, Piccinini F, Arienti C, Zamagni A, Santi S, Polico R, Bevilacqua A, Tesei A. 3D tumor spheroid models for in vitro therapeutic screening: a systematic approach to enhance the biological relevance of data obtained. Sci Rep. 2016;6:19103. https://doi.org/10.1038/srep19103.
  • [29] Simian M, Bissell MJ. Organoids: A historical perspective of thinking in three dimensions. J Cell Biol. 2017;216(1):31-40. https://doi.org/10.1083/jcb.201610056.
  • [30] Sakalem ME, De Sibio MT, da Costa FADS, de Oliveira M. Historical evolution of spheroids and organoids, and possibilities of use in life sciences and medicine. Biotechnol J. 2021;16(5):e2000463. https://doi.org/10.1002/biot.202000463.
  • [31] Huang BW, Gao JQ. Application of 3D cultured multicellular spheroid tumor models in tumor-targeted drug delivery system research. J Control Release. 2018;270:246-259. https://doi.org/10.1016/j.jconrel.2017.12.005.
  • [32] Mittler F, Obeïd P, Rulina AV, Haguet V, Gidrol X, Balakirev MY. High-Content Monitoring of Drug Effects in a 3D Spheroid Model. Front Oncol. 2017;7:293. https://doi.org/10.3389/fonc.2017.00293.
  • [33] Nath S, Devi GR. Three-dimensional culture systems in cancer research: Focus on tumor spheroid model. Pharmacol Ther. 2016;163:94-108. https://doi.org/10.1016/j.pharmthera.2016.03.013.
  • [34] Atat OE, Farzaneh Z, Pourhamzeh M, Taki F, Abi-Habib R, Vosough M, El-Sibai M. 3D modeling in cancer studies. Hum Cell. 2022;35(1):23-36. https://doi.org/10.1007/s13577-021-00642-9.
  • [35] Wang H, Brown PC, Chow ECY, Ewart L, Ferguson SS, Fitzpatrick S, Freedman BS, Guo GL, Hedrich W, Heyward S, Hickman J, Isoherranen N, Li AP, Liu Q, Mumenthaler SM, Polli J, Proctor WR, Ribeiro A, Wang JY, Wange RL, Huang SM. 3D cell culture models: Drug pharmacokinetics, safety assessment, and regulatory consideration. Clin Transl Sci. 2021;14(5):1659-1680. https://doi.org/10.1111/cts.13066.
  • [36] Kim SA, Lee EK, Kuh HJ. Co-culture of 3D tumor spheroids with fibroblasts as a model for epithelial mesenchymal transition in vitro. Exp Cell Res. 2015;335(2):187-196. https://doi.org/10.1016/j.yexcr.2015.05.016.
  • [37] Yeung YWS, Ma Y, Deng Y, Khoo BL, Chua SL. Bacterial Iron Siderophore Drives Tumor Survival and Ferroptosis Resistance in a Biofilm-Tumor Spheroid Coculture Model. Adv Sci (Weinh). 2024:e2404467. https://doi.org/10.1002/advs.202404467.
  • [38] Wang X, Sun Y, Zhang DY, Ming GL, Song H. Glioblastoma modeling with 3D organoids: progress and challenges. Oxf Open Neurosci. 2023;2:kvad008. https://doi.org/10.1093/oons/kvad008.
  • [39] Farouk SM, Khafaga AF, Abdellatif AM. Bladder cancer: therapeutic challenges and role of 3D cell culture systems in the screening of novel cancer therapeutics. Cancer Cell Int. 2023;23(1):251. https://doi.org/10.1186/s12935-023-03069-4.
  • [40] Yousafzai NA, El Khalki L, Wang W, Szpendyk J, Sossey-Alaoui K. Advances in 3D Culture Models to Study Exosomes in Triple-Negative Breast Cancer. Cancers (Basel). 2024;16(5):883. https://doi.org/10.3390/cancers16050883.
  • [41] Yan L, Wu X. Exosomes produced from 3D cultures of umbilical cord mesenchymal stem cells in a hollow-fiber bioreactor show improved osteochondral regeneration activity. Cell Biol Toxicol. 2020;36(2):165-178. https://doi.org/10.1007/s10565-019-09504-5.
  • [42] Gao W, Liang T, He R, Ren J, Yao H, Wang K, Zhu L, Xu Y. Exosomes from 3D culture of marrow stem cells enhances endothelial cell proliferation, migration, and angiogenesis via activation of the HMGB1/AKT pathway. Stem Cell Res. 2020;50:102122. https://doi.org/10.1016/j.scr.2020.102122.
  • [43] Abbasi J. Patient-Derived Organoids Predict Cancer Treatment Response. JAMA. 2018;319(14):1427. https://doi.org/10.1001/jama.2018.3760.
  • [44] Taverna JA, Hung CN, Williams M, Williams R, Chen M, Kamali S, Sambandam V, Hsiang-Ling Chiu C, Osmulski PA, Gaczynska ME, DeArmond DT, Gaspard C, Mancini M, Kusi M, Pandya AN, Song L, Jin L, Schiavini P, Chen CL. Ex vivo drug testing of patient-derived lung organoids to predict treatment responses for personalized medicine. Lung Cancer. 2024;190:107533. https://doi.org/10.1016/j.lungcan.2024.107533.
  • [45] Beumer J, Geurts MH, Lamers MM, Puschhof J, Zhang J, van der Vaart J, Mykytyn AZ, Breugem TI, Riesebosch S, Schipper D, van den Doel PB, de Lau W, Pleguezuelos-Manzano C, Busslinger G, Haagmans BL, Clevers H. A CRISPR/Cas9 genetically engineered organoid biobank reveals essential host factors for coronaviruses. Nat Commun. 2021;12(1):5498. https://doi.org/10.1038/s41467-021-25729-7.

Three-dimensional cell culture systems in drug development studies

Year 2024, Volume: 28 Issue: 6, 2236 - 2242, 28.06.2025

Fersu Gül Asya Çalişir Bilge Debeleç Bütüner

https://doi.org/10.29228/jrp.897

Abstract

Three-dimensional (3D) cell culture methods have been widely used in many research areas including the investigation of disease pathology such as carcinogenesis mechanisms, tissue engineering, and drug discovery. It has been known that 3D cell culture models have many advantages in comparison to both the monolayer two-dimensional (2D) cell culture methods in terms of better representing the in vivo cellular conditions and animal models due to their lower cost and higher applicability. 3D cell culture systems consist of validated models such as spheroids and organoids generated w/w.o. extracellular matrix components. Applications of these models can be seen in cancer research, highthroughput drug screening, and prediction of drug response on patient-derived 3D cellular models. Establishing novel 3D systems also has great potential to support the development of biotechnological therapeutics such as cellular therapies or therapeutic efficacy tests of various candidates on 3D models. This review article aims to briefly describe the recent literature on types, advantages, limitations, and applications of 3D cell culture models in various stages of drug development studies such as disease models, and drug response tests.

Keywords

Three-dimensional cell culture 3D disease models 3D drug testing spheroid organoid

References

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  • [2] Hubrecht RC, Carter E. The 3Rs and Humane Experimental Technique: Implementing Change. Animals (Basel). 2019;9(10):754. https://doi.org/10.3390/ani9100754.
  • [3] Tannenbaum J, Bennett BT. Russell and Burch's 3Rs then and now: the need for clarity in definition and purpose. J Am Assoc Lab Anim Sci. 2015;54(2):120-132.
  • [4] Cacciamali A, Villa R, Dotti S. 3D Cell Cultures: Evolution of an Ancient Tool for New Applications. Front Physiol. 2022;13:836480. https://doi.org/10.3389/fphys.2022.836480.
  • [5] Nunes AS, Barros AS, Costa EC, Moreira AF, Correia IJ. 3D tumor spheroids as in vitro models to mimic in vivo human solid tumors resistance to therapeutic drugs. Biotechnol Bioeng. 2019;116(1):206–226. https://doi.org/10.1002/bit.26845.
  • [6] Ravi M, Paramesh V, Kaviya SR, Anuradha E, Solomon FD. 3D cell culture systems: advantages and applications. J Cell Physiol. 2015;230(1):16-26. https://doi.org/10.1002/jcp.24683.
  • [7] Richter M, Piwocka O, Musielak M, Piotrowski I, Suchorska WM, Trzeciak T. From donor to the lab: A Fascinating journey of primary cell lines. Front Cell Dev Biol. 2021;9:711381. https://doi.org/10.3389/fcell.2021.711381.
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  • [9] Rodrigues T, Kundu B, Silva-Correia J, Kundu SC, Oliveira JM, Reis RL, Correlo VM. Emerging tumor spheroids technologies for 3D in vitro cancer modeling. Pharmacol Ther. 2018;184:201-211. https://doi.org/10.1016/j.pharmthera.2017.10.018.
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  • [17] Cacciamali A, Villa R, Dotti S. 3D Cell Cultures: Evolution of an Ancient Tool for New Applications. Front Physiol. 2022;13:836480. https://doi.org/10.3389/fphys.2022.836480.
  • [18] Habanjar O, Diab-Assaf M, Caldefie-Chezet F, Delort L. 3D Cell Culture Systems: Tumor Application, Advantages, and Disadvantages. Int J Mol Sci. 2021;22(22):12200. https://doi.org/10.3390/ijms222212200.
  • [19] Fitzgerald KA, Malhotra M, Curtin CM, O’Brien FJ, O’Driscoll CM. Life in 3D is never flat: 3D models to optimise drug delivery. J Control Release. 2015;215:39–54. https://doi.org/10.1016/j.jconrel.2015.07.020.
  • [20] Peela N, Sam FS, Christenson W, Truong D, Watson AW, Mouneimne G, Ros R, Nikkhah M. A three dimensional micropatterned tumor model for breast cancer cell migration studies. Biomaterials. 2016;81:72-83. https://doi.org/10.1016/j.biomaterials.2015.11.039.
  • [21] Chaicharoenaudomrung N, Kunhorm P, Noisa P. Three-dimensional cell culture systems as an in vitro platform for cancer and stem cell modeling. World J Stem Cells. 2019;11(12):1065-1083. https://doi.org/10.4252/wjsc.v11.i12.1065.
  • [22] Fang Y, Eglen RM. Three-Dimensional Cell Cultures in Drug Discovery and Development. SLAS Discov. 2017;22(5):456-472. https://doi.org/10.1177/1087057117696795.
  • [23] Tung YC, Hsiao AY, Allen SG, Torisawa YS, Ho M, Takayama S. High-throughput 3D spheroid culture and drug testing using a 384 hanging drop array. Analyst. 2011;136(3):473-478. https://doi.org/10.1039/c0an00609b.
  • [24] Haisler WL, Timm DM, Gage JA, Tseng H, Killian TC, Souza GR. Three-dimensional cell culturing by magnetic levitation. Nat Protoc. 2013;8(10):1940-1949. https://doi.org/10.1038/nprot.2013.125.
  • [25] Sant S, Johnston PA. The production of 3D tumor spheroids for cancer drug discovery. Drug Discov Today Technol. 2017;23:27-36. https://doi.org/10.1016/j.ddtec.2017.03.002.
  • [26] Imamura Y, Mukohara T, Shimono Y, Funakoshi Y, Chayahara N, Toyoda M, Kiyota N, Takao S, Kono S, Nakatsura T, Minami H. Comparison of 2D- and 3D-culture models as drug-testing platforms in breast cancer. Oncol Rep. 2015;33(4):1837-1843. https://doi.org/10.3892/or.2015.3767.
  • [27] Costa EC, de Melo-Diogo D, Moreira AF, Carvalho MP, Correia IJ. Spheroids Formation on Non-Adhesive Surfaces by Liquid Overlay Technique: Considerations and Practical Approaches. Biotechnol J. 2018; 13(1). https://doi.org/10.1002/biot.201700417.
  • [28] Zanoni M, Piccinini F, Arienti C, Zamagni A, Santi S, Polico R, Bevilacqua A, Tesei A. 3D tumor spheroid models for in vitro therapeutic screening: a systematic approach to enhance the biological relevance of data obtained. Sci Rep. 2016;6:19103. https://doi.org/10.1038/srep19103.
  • [29] Simian M, Bissell MJ. Organoids: A historical perspective of thinking in three dimensions. J Cell Biol. 2017;216(1):31-40. https://doi.org/10.1083/jcb.201610056.
  • [30] Sakalem ME, De Sibio MT, da Costa FADS, de Oliveira M. Historical evolution of spheroids and organoids, and possibilities of use in life sciences and medicine. Biotechnol J. 2021;16(5):e2000463. https://doi.org/10.1002/biot.202000463.
  • [31] Huang BW, Gao JQ. Application of 3D cultured multicellular spheroid tumor models in tumor-targeted drug delivery system research. J Control Release. 2018;270:246-259. https://doi.org/10.1016/j.jconrel.2017.12.005.
  • [32] Mittler F, Obeïd P, Rulina AV, Haguet V, Gidrol X, Balakirev MY. High-Content Monitoring of Drug Effects in a 3D Spheroid Model. Front Oncol. 2017;7:293. https://doi.org/10.3389/fonc.2017.00293.
  • [33] Nath S, Devi GR. Three-dimensional culture systems in cancer research: Focus on tumor spheroid model. Pharmacol Ther. 2016;163:94-108. https://doi.org/10.1016/j.pharmthera.2016.03.013.
  • [34] Atat OE, Farzaneh Z, Pourhamzeh M, Taki F, Abi-Habib R, Vosough M, El-Sibai M. 3D modeling in cancer studies. Hum Cell. 2022;35(1):23-36. https://doi.org/10.1007/s13577-021-00642-9.
  • [35] Wang H, Brown PC, Chow ECY, Ewart L, Ferguson SS, Fitzpatrick S, Freedman BS, Guo GL, Hedrich W, Heyward S, Hickman J, Isoherranen N, Li AP, Liu Q, Mumenthaler SM, Polli J, Proctor WR, Ribeiro A, Wang JY, Wange RL, Huang SM. 3D cell culture models: Drug pharmacokinetics, safety assessment, and regulatory consideration. Clin Transl Sci. 2021;14(5):1659-1680. https://doi.org/10.1111/cts.13066.
  • [36] Kim SA, Lee EK, Kuh HJ. Co-culture of 3D tumor spheroids with fibroblasts as a model for epithelial mesenchymal transition in vitro. Exp Cell Res. 2015;335(2):187-196. https://doi.org/10.1016/j.yexcr.2015.05.016.
  • [37] Yeung YWS, Ma Y, Deng Y, Khoo BL, Chua SL. Bacterial Iron Siderophore Drives Tumor Survival and Ferroptosis Resistance in a Biofilm-Tumor Spheroid Coculture Model. Adv Sci (Weinh). 2024:e2404467. https://doi.org/10.1002/advs.202404467.
  • [38] Wang X, Sun Y, Zhang DY, Ming GL, Song H. Glioblastoma modeling with 3D organoids: progress and challenges. Oxf Open Neurosci. 2023;2:kvad008. https://doi.org/10.1093/oons/kvad008.
  • [39] Farouk SM, Khafaga AF, Abdellatif AM. Bladder cancer: therapeutic challenges and role of 3D cell culture systems in the screening of novel cancer therapeutics. Cancer Cell Int. 2023;23(1):251. https://doi.org/10.1186/s12935-023-03069-4.
  • [40] Yousafzai NA, El Khalki L, Wang W, Szpendyk J, Sossey-Alaoui K. Advances in 3D Culture Models to Study Exosomes in Triple-Negative Breast Cancer. Cancers (Basel). 2024;16(5):883. https://doi.org/10.3390/cancers16050883.
  • [41] Yan L, Wu X. Exosomes produced from 3D cultures of umbilical cord mesenchymal stem cells in a hollow-fiber bioreactor show improved osteochondral regeneration activity. Cell Biol Toxicol. 2020;36(2):165-178. https://doi.org/10.1007/s10565-019-09504-5.
  • [42] Gao W, Liang T, He R, Ren J, Yao H, Wang K, Zhu L, Xu Y. Exosomes from 3D culture of marrow stem cells enhances endothelial cell proliferation, migration, and angiogenesis via activation of the HMGB1/AKT pathway. Stem Cell Res. 2020;50:102122. https://doi.org/10.1016/j.scr.2020.102122.
  • [43] Abbasi J. Patient-Derived Organoids Predict Cancer Treatment Response. JAMA. 2018;319(14):1427. https://doi.org/10.1001/jama.2018.3760.
  • [44] Taverna JA, Hung CN, Williams M, Williams R, Chen M, Kamali S, Sambandam V, Hsiang-Ling Chiu C, Osmulski PA, Gaczynska ME, DeArmond DT, Gaspard C, Mancini M, Kusi M, Pandya AN, Song L, Jin L, Schiavini P, Chen CL. Ex vivo drug testing of patient-derived lung organoids to predict treatment responses for personalized medicine. Lung Cancer. 2024;190:107533. https://doi.org/10.1016/j.lungcan.2024.107533.
  • [45] Beumer J, Geurts MH, Lamers MM, Puschhof J, Zhang J, van der Vaart J, Mykytyn AZ, Breugem TI, Riesebosch S, Schipper D, van den Doel PB, de Lau W, Pleguezuelos-Manzano C, Busslinger G, Haagmans BL, Clevers H. A CRISPR/Cas9 genetically engineered organoid biobank reveals essential host factors for coronaviruses. Nat Commun. 2021;12(1):5498. https://doi.org/10.1038/s41467-021-25729-7.
There are 45 citations in total.

Details

Primary Language English
Subjects Pharmaceutical Biotechnology
Journal Section Articles
Authors

Fersu Gül Asya Çalişir 0000-0003-2244-940X

Bilge Debeleç Bütüner 0000-0001-8112-9241

Publication Date June 28, 2025
Submission Date April 22, 2024
Acceptance Date June 5, 2024
Published in Issue Year 2024 Volume: 28 Issue: 6

Cite

APA Çalişir, F. G. A., & Debeleç Bütüner, B. (2025). Three-dimensional cell culture systems in drug development studies. Journal of Research in Pharmacy, 28(6), 2236-2242. https://doi.org/10.29228/jrp.897
AMA Çalişir FGA, Debeleç Bütüner B. Three-dimensional cell culture systems in drug development studies. J. Res. Pharm. July 2025;28(6):2236-2242. doi:10.29228/jrp.897
Chicago Çalişir, Fersu Gül Asya, and Bilge Debeleç Bütüner. “Three-Dimensional Cell Culture Systems in Drug Development Studies”. Journal of Research in Pharmacy 28, no. 6 (July 2025): 2236-42. https://doi.org/10.29228/jrp.897.
EndNote Çalişir FGA, Debeleç Bütüner B (July 1, 2025) Three-dimensional cell culture systems in drug development studies. Journal of Research in Pharmacy 28 6 2236–2242.
IEEE F. G. A. Çalişir and B. Debeleç Bütüner, “Three-dimensional cell culture systems in drug development studies”, J. Res. Pharm., vol. 28, no. 6, pp. 2236–2242, 2025, doi: 10.29228/jrp.897.
ISNAD Çalişir, Fersu Gül Asya - Debeleç Bütüner, Bilge. “Three-Dimensional Cell Culture Systems in Drug Development Studies”. Journal of Research in Pharmacy 28/6 (July 2025), 2236-2242. https://doi.org/10.29228/jrp.897.
JAMA Çalişir FGA, Debeleç Bütüner B. Three-dimensional cell culture systems in drug development studies. J. Res. Pharm. 2025;28:2236–2242.
MLA Çalişir, Fersu Gül Asya and Bilge Debeleç Bütüner. “Three-Dimensional Cell Culture Systems in Drug Development Studies”. Journal of Research in Pharmacy, vol. 28, no. 6, 2025, pp. 2236-42, doi:10.29228/jrp.897.
Vancouver Çalişir FGA, Debeleç Bütüner B. Three-dimensional cell culture systems in drug development studies. J. Res. Pharm. 2025;28(6):2236-42.