Derleme
BibTex RIS Kaynak Göster

Four-Dimensional Printing Technology at the Frontier of Advanced Modeling and Applications in Brain Tissue Engineering

Yıl 2021, Cilt: 3 Sayı: 2, 46 - 57, 31.12.2021
https://doi.org/10.51934/jomit.1016838

Öz

The complex process behind the brain topology, which has been extensively studied for the last ten years, is still unclear. Therefore, neural tissue engineering studies are needed to better understand cortical folds. With the development of 4-dimensional (4D) bioprinters using cell-loaded smart materials, a promising path has been opened in the mimicry of the neural tissue. In our study, we review the usage areas of 4D printers, which have been developing in recent years, in modelling brain tissue. As a result of development of smart materials printed with 3-dimensional (3D) printers caused emerging of 4D printers, rapidly. Smart materials can change their properties based on physical, chemical and biological stimuli, and this change can be a reversible process. Cell-loaded printed smart materials should have little effect on cell viability of both the incoming stimulus and the physical change. It is also important that the material used is non-toxic and the solvent is suitable for cell viability. On the other hand, hydrogels are frequently studied to mimic the complex neural network of neural tissue. Agents that affect the crosslinking or degree of crosslinking of hydrogels can be easily controlled and changed. In addition, studies with neural stem cells have shown that hydrogels have a supportive effect on the proliferation and maturation of neural stem cells. Since the folding time, strength and location of smart materials cannot be known precisely, it can be an advantage of 4D bioprinters as it can be controlled and studied whether the results of the stress on the cells in this region will affect other cells. It is an ideal methodology to study the effect of cortical folding on neural stem cells, especially thanks to the ease of experimental manipulations provided by 4D bioprinters. It is expected that 4D bioprinters will be adopted and rapid developments will occur in the multidisciplinary field of tissue engineering of brain tissue in the near coming years.

Destekleyen Kurum

Turkish Scientific and Technological Council (TÜBİTAK) and Eskisehir Osmangazi University (Scientific Research Foundation)

Teşekkür

We gratefully acknowledge Turkish Scientific and Technological Council (TÜBİTAK) and Eskisehir Osmangazi University (Scientific Research Foundation) for their support.

Kaynakça

  • Rothenbücher, T. S., Gürbüz, H., Pereira, M. P., Heiskanen, A., Emneus, J., & Martinez-Serrano, A. (2021). Next generation human brain models: engineered flat brain organoids featuring gyrification. Biofabrication, 13(1), 011001. doi: 10.1088/1758-5090/abc95e
  • Esworthy, T. J., Miao, S., Lee, S. J., Zhou, X., Cui, H., Zuo, Y. Y., & Zhang, L. G. (2019). Advanced 4D-bioprinting technologies for brain tissue modeling and study. International journal of smart and nano materials, 10(3), 177-204. doi: 10.1080/19475411.2019.1631899
  • Matsumoto, N., Shinmyo, Y., Ichikawa, Y., & Kawasaki, H. (2017). Gyrification of the cerebral cortex requires FGF signaling in the mammalian brain. Elife, 6, e29285 doi: 10.7554/eLife.29285
  • Nanda, P., Tandon, N., Mathew, I. T., Giakoumatos, C. I., Abhishekh, H. A., Clementz, B. A., Pearlson, G. D., Sweeney, J., Tamminga, C. A., & Keshavan, M. S. (2014). Local gyrification index in probands with psychotic disorders and their first-degree relatives. Biological psychiatry, 76(6), 447–455. doi: 10.1016/j.biopsych.2013.11.018
  • Thompson AJ, Pillai EK, Dimov IB, Foster SK, Holt CE, Franze K. Rapid changes in tissue mechanics regulate cell behaviour in the developing embryonic brain. Elife. 2019 Jan 15;8:e39356. doi: 10.7554/eLife.39356.
  • Askari, M., Naniz, M. A., Kouhi, M., Saberi, A., Zolfagharian, A., & Bodaghi, M. (2021). Recent progress in extrusion 3D bioprinting of hydrogel biomaterials for tissue regeneration: A comprehensive review with focus on advanced fabrication techniques. Biomaterials science, 9(3), 535-573. doi: 10.1039/D0BM00973C
  • Gao, W., Zhang, Y., Ramanujan, D., Ramani, K., Chen, Y., Williams, C. B., ... & Zavattieri, P. D. (2015). The status, challenges, and future of additive manufacturing in engineering. Computer-Aided Design, 69, 65-89. doi: 10.1016/j.cad.2015.04.001.
  • Farahani, R. D., Dubé, M., & Therriault, D. (2016). Three‐dimensional printing of multifunctional nanocomposites: manufacturing techniques and applications. Advanced materials, 28(28), 5794-5821. doi: 10.1002/adma.201506215
  • Lee Ventola, C. (2014). Medical applications for 3D printing: current and projected uses, P T 39 (2014) 704–711
  • Guvendiren, M., Molde, J., Soares, R. M., & Kohn, J. (2016). Designing biomaterials for 3D printing. ACS biomaterials science & engineering, 2(10), 1679-1693. doi: 10.1021/acsbiomaterials.6b00121.
  • Kahl, M., Gertig, M., Hoyer, P., Friedrich, O., & Gilbert, D. F. (2019). Ultra-low-cost 3D bioprinting: modification and application of an off-the-shelf desktop 3D-printer for biofabrication. Frontiers in bioengineering and biotechnology, 7, 184. doi: 10.3389/fbioe.2019.00184.
  • Gao, B., Yang, Q., Zhao, X., Jin, G., Ma, Y., & Xu, F. (2016). 4D bioprinting for biomedical applications. Trends in biotechnology, 34(9), 746-756. doi: 10.1016/j.tibtech.2016.03.004
  • Mota, C., Camarero-Espinosa, S., Baker, M. B., Wieringa, P., & Moroni, L. (2020). Bioprinting: from tissue and organ development to in vitro models. Chemical reviews, 120(19), 10547-10607. doi: 10.1021/acs.chemrev.9b00789.
  • Cui, H., Nowicki, M., Fisher, J. P., & Zhang, L. G. (2017). 3D bioprinting for organ regeneration. Advanced healthcare materials, 6(1), 1601118. doi: 10.1002/adhm.201601118.
  • Xie, Z., Gao, M., Lobo, A. O., & Webster, T. J. (2020). 3D bioprinting in tissue engineering for medical applications: the classic and the hybrid. Polymers, 12(8), 1717. doi: 10.3390/POLYM12081717.
  • Wan, Z., Zhang, P., Liu, Y., Lv, L., & Zhou, Y. (2020). Four-dimensional bioprinting: Current developments and applications in bone tissue engineering. Acta biomaterialia, 101, 26-42. doi: 10.1016/j.actbio.2019.10.038.
  • Yu, C., Ma, X., Zhu, W., Wang, P., Miller, K. L., Stupin, J., ... & Chen, S. (2019). Scanningless and continuous 3D bioprinting of human tissues with decellularized extracellular matrix. Biomaterials, 194, 1-13. doi: 10.1016/j.biomaterials.2018.12.009.
  • Li, Y. C., Zhang, Y. S., Akpek, A., Shin, S. R., & Khademhosseini, A. (2016). 4D bioprinting: the next-generation technology for biofabrication enabled by stimuli-responsive materials. Biofabrication, 9(1), 012001. doi: 10.1088/1758-5090/9/1/012001.
  • Yang, G. H., Yeo, M., Koo, Y. W., & Kim, G. H. (2019). 4D bioprinting: technological advances in biofabrication. Macromolecular bioscience, 19(5), 1800441. doi: 10.1002/mabi.201800441.
  • Zhang, Z., Demir, K. G., & Gu, G. X. (2019). Developments in 4D-printing: a review on current smart materials, technologies, and applications. International Journal of Smart and Nano Materials, 10(3), 205-224. doi: 10.1080/19475411.2019.1591541.
  • Chadwick, M., Yang, C., Liu, L., Gamboa, C. M., Jara, K., Lee, H., & Sabaawy, H. E. (2020). Rapid processing and drug evaluation in glioblastoma patient-derived organoid models with 4D bioprinted arrays. Iscience, 23(8), 101365. doi: 10.1016/j.isci.2020.101365.
  • Amukarimi, S., & Mozafari, M. (2021). 4D bioprinting of tissues and organs. Bioprinting, e00161. doi: 10.1016/j.bprint.2021.e00161
  • Nadgorny, M., & Ameli, A. (2018). Functional polymers and nanocomposites for 3D printing of smart structures and devices. ACS applied materials & interfaces, 10(21), 17489-17507. doi: 10.1021/acsami.8b01786
  • Yang, Q., Gao, B., & Xu, F. (2020). Recent advances in 4D bioprinting. Biotechnology journal, 15(1), 1900086. doi: 10.1002/biot.201900086
  • Klouda, L., & Mikos, A. G. (2008). Thermoresponsive hydrogels in biomedical applications. European journal of pharmaceutics and biopharmaceutics, 68(1), 34-45. doi: 10.1016/j.ejpb.2007.02.025
  • Wang, X., Sun, Y., Peng, C., Luo, H., Wang, R., & Zhang, D. (2015). Transitional suspensions containing thermosensitive dispersant for three-dimensional printing. ACS applied materials & interfaces, 7(47), 26131-26136. doi: 10.1021/acsami.5b07913
  • Zarek, M., Mansour, N., Shapira, S., & Cohn, D. (2017). 4D printing of shape memory‐based personalized endoluminal medical devices. Macromolecular rapid communications, 38(2), 1600628. doi: 10.1002/marc.201600628
  • Stoychev, G., Puretskiy, N., & Ionov, L. (2011). Self-folding all-polymer thermoresponsive microcapsules. Soft Matter, 7(7), 3277-3279. doi: 10.1039/C1SM05109A
  • Apsite, I., Stoychev, G., Zhang, W., Jehnichen, D., Xie, J., & Ionov, L. (2017). Porous stimuli-responsive self-folding electrospun mats for 4D biofabrication. Biomacromolecules, 18(10), 3178-3184.
  • Fratzl, P., & Barth, F. G. (2009). Biomaterial systems for mechanosensing and actuation. Nature, 462(7272), 442-448.
  • Lui, Y. S., Sow, W. T., Tan, L. P., Wu, Y., Lai, Y., & Li, H. (2019). 4D printing and stimuli-responsive materials in biomedical aspects. Acta biomaterialia, 92, 19-36. doi: 10.1016/j.actbio.2019.05.005
  • Gupta, M. K., Meng, F., Johnson, B. N., Kong, Y. L., Tian, L., Yeh, Y. W., ... & McAlpine, M. C. (2015). 3D printed programmable release capsules. Nano letters, 15(8), 5321-5329. doi: 10.1021/acs.nanolett.5b01688
  • Ahadian, S., Obregón, R., Ramón-Azcón, J., Salazar, G., Shiku, H., Ramalingam, M., & Matsue, T. (2016). Carbon nanotubes and graphene-based nanomaterials for stem cell differentiation and tissue regeneration. Journal of Nanoscience and Nanotechnology, 16(9), 8862-8880. doi: 10.1166/jnn.2016.12729
  • Ramon-Azcon, J., Ahadian, S., Obregon, R., Shiku, H., Ramalingam, M., & Matsue, T. (2014). Applications of carbon nanotubes in stem cell research. Journal of biomedical nanotechnology, 10(10), 2539-2561. doi: 10.1166/jbn.2014.1899
  • Sayyar, S., Bjorninen, M., Haimi, S., Miettinen, S., Gilmore, K., Grijpma, D., & Wallace, G. (2016). UV cross-linkable graphene/poly (trimethylene carbonate) composites for 3D printing of electrically conductive scaffolds. ACS applied materials & interfaces, 8(46), 31916-31925. doi: 10.1021/acsami.6b09962
  • Jakus, A. E., Secor, E. B., Rutz, A. L., Jordan, S. W., Hersam, M. C., & Shah, R. N. (2015). Three-dimensional printing of high-content graphene scaffolds for electronic and biomedical applications. ACS nano, 9(4), 4636-4648. doi: 10.1021/acsnano.5b01179
  • Kocak, G., Tuncer, C. A. N. S. E. L., & Bütün, V. J. P. C. (2017). pH-Responsive polymers. Polymer Chemistry, 8(1), 144-176. doi: 10.1039/C6PY01872F
  • Pourjavadi, A., Ebrahimi, A. A., & Barzegar, S. (2013). Preparation and evaluation of bioactive and compatible starch based superabsorbent for oral drug delivery systems. Journal of Drug Delivery Science and Technology, 23(5), 511-517. doi: 10.1016/S1773-2247(13)50074-8
  • Kwon, S. S., Kong, B. J., & Park, S. N. (2015). Physicochemical properties of pH-sensitive hydrogels based on hydroxyethyl cellulose–hyaluronic acid and for applications as transdermal delivery systems for skin lesions. European journal of pharmaceutics and biopharmaceutics, 92, 146-154. doi: 10.1016/j.ejpb.2015.02.025
  • Fundueanu, G., Constantin, M., Asmarandei, I., Harabagiu, V., Ascenzi, P., & Simionescu, B. C. (2013). The thermosensitivity of pH/thermoresponsive microspheres activated by the electrostatic interaction of pH‐sensitive units with a bioactive compound. Journal of Biomedical Materials Research Part A, 101(6), 1661-1669. doi: 10.1002/jbm.a.34469
  • Kim, S. H., Seo, Y. B., Yeon, Y. K., Lee, Y. J., Park, H. S., Sultan, M. T., ... & Park, C. H. (2020). 4D-bioprinted silk hydrogels for tissue engineering. Biomaterials, 260, 120281. doi: 10.1016/j.biomaterials.2020.120281
  • Ramos, M. L. P., González, J. A., Fabian, L., Pérez, C. J., Villanueva, M. E., & Copello, G. J. (2017). Sustainable and smart keratin hydrogel with pH-sensitive swelling and enhanced mechanical properties. Materials Science and Engineering: C, 78, 619-626. doi: 10.1016/j.msec.2017.04.120
  • Narupai, B., Smith, P. T., & Nelson, A. (2021). 4D Printing of Multi‐Stimuli Responsive Protein‐Based Hydrogels for Autonomous Shape Transformations. Advanced Functional Materials, 2011012. doi: 10.1002/adfm.202011012
  • Yoshida, T., Lai, T. C., Kwon, G. S., & Sako, K. (2013). pH-and ion-sensitive polymers for drug delivery. Expert opinion on drug delivery, 10(11), 1497-1513. doi: 10.1517/17425247.2013.821978
  • Dong, Y., Wang, S., Ke, Y., Ding, L., Zeng, X., Magdassi, S., & Long, Y. (2020). 4D printed hydrogels: fabrication, materials, and applications. Advanced Materials Technologies, 5(6), 2000034. doi: 10.1002/admt.202000034
  • Rudko, M., Urbaniak, T., & Musiał, W. (2021). Recent Developments in Ion-Sensitive Systems for Pharmaceutical Applications. Polymers, 13(10), 1641. doi: 10.3390/polym13101641
  • Wang, B., Liu, L., & Liao, L. (2019). Light and ferric ion responsive fluorochromic hydrogels with high strength and self-healing ability. Polymer Chemistry, 10(47), 6481-6488. doi: 10.1039/C9PY01459D
  • Wu, Q., Wang, L., Yu, H., Wang, J., & Chen, Z. (2011). Organization of glucose-responsive systems and their properties. Chemical reviews, 111(12), 7855-7875. doi: 10.1021/cr200027j
  • Adams, A., Malkoc, A., & La Belle, J. T. (2018). The development of a glucose dehydrogenase 3D-printed glucose sensor: a proof-of-concept study. Journal of diabetes science and technology, 12(1), 176-182. doi: 10.1177/1932296817715272
  • Matsumoto, A., Ishii, T., Nishida, J., Matsumoto, H., Kataoka, K., & Miyahara, Y. (2012). A synthetic approach toward a self‐regulated insulin delivery system. Angewandte Chemie International Edition, 51(9), 2124-2128. doi: 10.1002/anie.201106252
  • Brownlee, M., & Cerami, A. (1979). A glucose-controlled insulin-delivery system: semisynthetic insulin bound to lectin. Science, 206(4423), 1190-1191. doi: 10.1126/science.505005
  • Wang, J., Zhang, H., Wang, F., Ai, X., Huang, D., Liu, G., & Mi, P. (2018). Enzyme-responsive polymers for drug delivery and molecular imaging. In Stimuli Responsive Polymeric Nanocarriers for Drug Delivery Applications, Volume 1 (pp. 101-119). Woodhead Publishing. doi: 10.1016/B978-0-08-101997-9.00004-7
  • Zelzer, M., Todd, S. J., Hirst, A. R., McDonald, T. O., & Ulijn, R. V. (2013). Enzyme responsive materials: design strategies and future developments. Biomaterials Science, 1(1), 11-39. doi: 10.1039/C2BM00041E
  • Wang, X., Qin, X. H., Hu, C., Terzopoulou, A., Chen, X. Z., Huang, T. Y., ... & Nelson, B. J. (2018). 3D printed enzymatically biodegradable soft helical microswimmers. Advanced Functional Materials, 28(45), 1804107. doi: 10.1002/adfm.201804107
  • Banerjee, A., Arha, M., Choudhary, S., Ashton, R. S., Bhatia, S. R., Schaffer, D. V., Kane, R. S. (2009). The influence of hydrogel modulus on the proliferation and differentiation of encapsulated neural stem cells. Biomaterials. Sep;30(27):4695-9. doi: 10.1016/j.biomaterials.2009.05.050. Epub 2009 Jun 17.
  • Chang, Y. J., Tsai, C. J., Tseng, F. G., Chen, T. J., Wang, T. W. (2013). Micropatterned stretching system for the investigation of mechanical tension on neural stem cells behavior. Nanomedicine. Apr;9(3):345-55. doi: 10.1016/j.nano.2012.07.008. Epub 2012 Aug 24.
  • Lozano, R., Stevens, L., Thompson, B. C., Gilmore, K. J., Gorkin III, R., Stewart, E. M., in het Panhuis, M., Romero-Ortega, M. and Wallace, G.G. (2015). 3D printing of layered brain-like structures using peptide modified gellan gum substrates. Biomaterials, 67, 264-273. doi:10.1016/j.biomaterials.2015.07.022
  • Lorber, B., Hsiao, W. K., Hutchings, I. M., & Martin, K. R. (2013). Adult rat retinal ganglion cells and glia can be printed by piezoelectric inkjet printing. Biofabrication, 6(1), 015001. doi:10.1088/1758-5082/6/1/015001
  • Miao, S., Castro, N., Nowicki, M., Xia, L., Cui, H., Zhou, X., Zhu, W., Lee, S. J., Sarkar, K., Vozzi, G., Tabata, Y., Fisher, J., & Zhang, L. G. (2017). 4D printing of polymeric materials for tissue and organ regeneration. Materials today (Kidlington, England), 20(10), 577–591. doi: 10.1016/j.mattod.2017.06.005
  • Miao, S., Cui, H., Nowicki, M., Lee, S.J., Almeida, J., Zhou, X., Zhu, W., Yao, X., Masood, F., Plesniak, M.W. and Mohiuddin, M., 2018. Photolithographic-stereolithographic-tandem fabrication of 4D smart scaffolds for improved stem cell cardiomyogenic differentiation. Biofabrication, 10(3), p.035007. https://doi.org/10.1088/1758-5090/aabe0b
  • Miao, S., Cui, H., Nowicki, M., Xia, L., Zhou, X., Lee, S. J., ... & Zhang, L. G. (2018). Stereolithographic 4D bioprinting of multiresponsive architectures for neural engineering. Advanced biosystems, 2(9), 1800101. https://doi.org/10.1002/adbi.201800101
  • Cui, C., Kim, D. O., Pack, M. Y., Han, B., Han, L., Sun, Y., & Han, L. H. (2020). 4D printing of self-folding and cell-encapsulating 3D microstructures as scaffolds for tissue-engineering applications. Biofabrication, 12(4), 045018.
  • Zhu, W., George, J. K., Sorger, V. J., & Grace Zhang, L. (2017). 3D printing scaffold coupled with low level light therapy for neural tissue regeneration. Biofabrication, 9(2), 025002. doi:10.1088/1758-5090/aa6999
  • Melissinaki, V., Gill, A. A., Ortega, I., Vamvakaki, M., Ranella, A., Haycock, J. W., … Claeyssens, F. (2011). Direct laser writing of 3D scaffolds for neural tissue engineering applications. Biofabrication, 3(4), 045005. doi:10.1088/1758-5082/3/4/045005
  • Raviv, D., Zhao, W., McKnelly, C., Papadopoulou, A., Kadambi, A., Shi, B., ... & Tibbits, S. (2014). Active printed materials for complex self-evolving deformations. Scientific reports, 4(1), 1-8. doi: 10.1038/srep07422
  • Zhang, Y. S., Aleman, J., Shin, S. R., Kilic, T., Kim, D., Shaegh, S. A. M., ... & Khademhosseini, A. (2017). Multisensor-integrated organs-on-chips platform for automated and continual in situ monitoring of organoid behaviors. Proceedings of the National Academy of Sciences, 114(12), E2293-E2302. doi: 10.1073/pnas.1612906114
  • Shin, S. R., Zhang, Y. S., Kim, D. J., Manbohi, A., Avci, H., Silvestri, A., ... & Khademhosseini, A. (2016). Aptamer-based microfluidic electrochemical biosensor for monitoring cell-secreted trace cardiac biomarkers. Analytical chemistry, 88(20), 10019-10027. doi: 10.1021/acs.analchem.6b02028
  • Shin, S. R., Kilic, T., Zhang, Y. S., Avci, H., Hu, N., Kim, D., ... & Khademhosseini, A. (2017). Label‐Free and Regenerative Electrochemical Microfluidic Biosensors for Continual Monitoring of Cell Secretomes. Advanced Science, 4(5), 1600522. doi: 10.1002/advs.201600522
  • Hüseyin, A. V. C. I., GÜZEL, F. D., Salim, E. R. O. L., & Akpek, A. (2017). Recent advances in organ-on-a-chip technologies and future challenges: a review. Turkish Journal of Chemistry, 42(3), 587-610. doi:10.3906/kim-1611-35
  • Akpek, A., Öztürk, A. B., Alarçin, E., Huseyin, A. V. C. İ., & ADALI, M. A. Recent Advances in 4D Bioprinting. Research Journal of Biomedical and Biotechnology, 1(1), 20-23.

Gelişmiş Modellemede Yeni Alan Dört Boyutlu Baskı Teknolojisi ve Beyin Doku Mühendisliğinde Uygulamaları

Yıl 2021, Cilt: 3 Sayı: 2, 46 - 57, 31.12.2021
https://doi.org/10.51934/jomit.1016838

Öz

Son on yıldır kapsamlı çalışmalar yapılan beyin topolojisinin arkasında yatan süreç henüz belirsizdir. Kortikal katlanmaların daha iyi anlaşılabilmesi için nöral doku mühendisliği çalışmalarına ihtiyaç vardır. Hücre yüklü akıllı malzemelerin kullanıldığı 4 boyutlu (4B) biyoyazıcıların gelişmesi ile nöral dokunun mimik edilmesinde umut verici bir yol açılmıştır. Çalışmamızda son yıllarda gelişmekte olan 4B yazıcıların beyin dokusunun modellenmesinde kullanım alanlarını gözden geçirmekteyiz. 3 boyutlu (3B) yazıcılar ile basılan akıllı malzemelerin gelişmesiyle 4B yazıcılar ortaya çıkmıştır. Akıllı malzemeler fiziksel, kimyasal ve biyolojik uyaranlara dayalı olarak özelliklerini değiştirebilirler ve bu değişiklik geri dönüşümlü bir süreçtir. Hücre yüklü olarak basılan akıllı malzemeler hem gelen uyarıcının hem de fiziksel değişimin hücre canlılığı üzerinde çok az bir etki yaratması gerekir. Ayrıca kullanılan malzemenin toksik olmaması ve çözücünü hücre canlılığına uygun olması da önemlidir. Nöral dokunun karmaşık sinir ağının mimik edilebilmesi için hidrojeller ile sıklıkla çalışılmaktadır. Hidrojellerin çapraz bağlanmasını veya çapraz bağlanma derecesini etkileyen ajanlar kolaylıkla kontrol edilebilir ve değiştirilebilir. Ayrıca nöral kök hücreler ile yapılan çalışmalarda hidrojellerin nöral kök hücrelerin proliferasyon ve olgunlaşması üzerinde destekleyici bir etkiye sahip olduğu gösterilmiştir. Akıllı malzemelerin katlanma zamanı, kuvveti ve yeri kesin olarak bilinemediği için bu bölgede bulunan hücreler üzerindeki stresin sonuçlarının diğer hücreleri etkileyip etkilemeyeceğinin ön görülmesi zorluğu 4B biyoyazıcıların bir avantajı olarak karşımıza çıkma ihtimalini göstermektedir. Burada özellikle 4B biyoyazıcıların sağladığı deneysel manipülasyonların kolaylığı sayesinde kortikal katlanmanın nöral kök hücreler üzerine etkisini incelemek için ideal bir metodolojidir. Önümüzdeki yakın yıllarda multidisipliner olan beyin doku mühendisliği alanında 4B biyoyazıcıların benimseneceği ve hızlı gelişmelerin olacağını düşünmekteyiz.

Son on yıldır kapsamlı çalışmalar yapılan beyin topolojisinin arkasında yatan süreç henüz belirsizdir. Kortikal katlanmaların daha iyi anlaşılabilmesi için nöral doku mühendisliği çalışmalarına ihtiyaç vardır. Hücre yüklü akıllı malzemelerin kullanıldığı 4 boyutlu (4B) biyoyazıcıların gelişmesi ile nöral dokunun mimik edilmesinde umut verici bir yol açılmıştır. Çalışmamızda son yıllarda gelişmekte olan 4B yazıcıların beyin dokusunun modellenmesinde kullanım alanlarını gözden geçirmekteyiz. 3 boyutlu (3B) yazıcılar ile basılan akıllı malzemelerin gelişmesiyle 4B yazıcılar ortaya çıkmıştır. Akıllı malzemeler fiziksel, kimyasal ve biyolojik uyaranlara dayalı olarak özelliklerini değiştirebilirler ve bu değişiklik geri dönüşümlü bir süreçtir. Hücre yüklü olarak basılan akıllı malzemeler hem gelen uyarıcının hem de fiziksel değişimin hücre canlılığı üzerinde çok az bir etki yaratması gerekir. Ayrıca kullanılan malzemenin toksik olmaması ve çözücünü hücre canlılığına uygun olması da önemlidir. Nöral dokunun karmaşık sinir ağının mimik edilebilmesi için hidrojeller ile sıklıkla çalışılmaktadır. Hidrojellerin çapraz bağlanmasını veya çapraz bağlanma derecesini etkileyen ajanlar kolaylıkla kontrol edilebilir ve değiştirilebilir. Ayrıca nöral kök hücreler ile yapılan çalışmalarda hidrojellerin nöral kök hücrelerin proliferasyon ve olgunlaşması üzerinde destekleyici bir etkiye sahip olduğu gösterilmiştir. Akıllı malzemelerin katlanma zamanı, kuvveti ve yeri kesin olarak bilinemediği için bu bölgede bulunan hücreler üzerindeki stresin sonuçlarının diğer hücreleri etkileyip etkilemeyeceğinin ön görülmesi zorluğu 4B biyoyazıcıların bir avantajı olarak karşımıza çıkma ihtimalini göstermektedir. Burada özellikle 4B biyoyazıcıların sağladığı deneysel manipülasyonların kolaylığı sayesinde kortikal katlanmanın nöral kök hücreler üzerine etkisini incelemek için ideal bir metodolojidir. Önümüzdeki yakın yıllarda multidisipliner olan beyin doku mühendisliği alanında 4B biyoyazıcıların benimseneceği ve hızlı gelişmelerin olacağını düşünmekteyiz

Kaynakça

  • Rothenbücher, T. S., Gürbüz, H., Pereira, M. P., Heiskanen, A., Emneus, J., & Martinez-Serrano, A. (2021). Next generation human brain models: engineered flat brain organoids featuring gyrification. Biofabrication, 13(1), 011001. doi: 10.1088/1758-5090/abc95e
  • Esworthy, T. J., Miao, S., Lee, S. J., Zhou, X., Cui, H., Zuo, Y. Y., & Zhang, L. G. (2019). Advanced 4D-bioprinting technologies for brain tissue modeling and study. International journal of smart and nano materials, 10(3), 177-204. doi: 10.1080/19475411.2019.1631899
  • Matsumoto, N., Shinmyo, Y., Ichikawa, Y., & Kawasaki, H. (2017). Gyrification of the cerebral cortex requires FGF signaling in the mammalian brain. Elife, 6, e29285 doi: 10.7554/eLife.29285
  • Nanda, P., Tandon, N., Mathew, I. T., Giakoumatos, C. I., Abhishekh, H. A., Clementz, B. A., Pearlson, G. D., Sweeney, J., Tamminga, C. A., & Keshavan, M. S. (2014). Local gyrification index in probands with psychotic disorders and their first-degree relatives. Biological psychiatry, 76(6), 447–455. doi: 10.1016/j.biopsych.2013.11.018
  • Thompson AJ, Pillai EK, Dimov IB, Foster SK, Holt CE, Franze K. Rapid changes in tissue mechanics regulate cell behaviour in the developing embryonic brain. Elife. 2019 Jan 15;8:e39356. doi: 10.7554/eLife.39356.
  • Askari, M., Naniz, M. A., Kouhi, M., Saberi, A., Zolfagharian, A., & Bodaghi, M. (2021). Recent progress in extrusion 3D bioprinting of hydrogel biomaterials for tissue regeneration: A comprehensive review with focus on advanced fabrication techniques. Biomaterials science, 9(3), 535-573. doi: 10.1039/D0BM00973C
  • Gao, W., Zhang, Y., Ramanujan, D., Ramani, K., Chen, Y., Williams, C. B., ... & Zavattieri, P. D. (2015). The status, challenges, and future of additive manufacturing in engineering. Computer-Aided Design, 69, 65-89. doi: 10.1016/j.cad.2015.04.001.
  • Farahani, R. D., Dubé, M., & Therriault, D. (2016). Three‐dimensional printing of multifunctional nanocomposites: manufacturing techniques and applications. Advanced materials, 28(28), 5794-5821. doi: 10.1002/adma.201506215
  • Lee Ventola, C. (2014). Medical applications for 3D printing: current and projected uses, P T 39 (2014) 704–711
  • Guvendiren, M., Molde, J., Soares, R. M., & Kohn, J. (2016). Designing biomaterials for 3D printing. ACS biomaterials science & engineering, 2(10), 1679-1693. doi: 10.1021/acsbiomaterials.6b00121.
  • Kahl, M., Gertig, M., Hoyer, P., Friedrich, O., & Gilbert, D. F. (2019). Ultra-low-cost 3D bioprinting: modification and application of an off-the-shelf desktop 3D-printer for biofabrication. Frontiers in bioengineering and biotechnology, 7, 184. doi: 10.3389/fbioe.2019.00184.
  • Gao, B., Yang, Q., Zhao, X., Jin, G., Ma, Y., & Xu, F. (2016). 4D bioprinting for biomedical applications. Trends in biotechnology, 34(9), 746-756. doi: 10.1016/j.tibtech.2016.03.004
  • Mota, C., Camarero-Espinosa, S., Baker, M. B., Wieringa, P., & Moroni, L. (2020). Bioprinting: from tissue and organ development to in vitro models. Chemical reviews, 120(19), 10547-10607. doi: 10.1021/acs.chemrev.9b00789.
  • Cui, H., Nowicki, M., Fisher, J. P., & Zhang, L. G. (2017). 3D bioprinting for organ regeneration. Advanced healthcare materials, 6(1), 1601118. doi: 10.1002/adhm.201601118.
  • Xie, Z., Gao, M., Lobo, A. O., & Webster, T. J. (2020). 3D bioprinting in tissue engineering for medical applications: the classic and the hybrid. Polymers, 12(8), 1717. doi: 10.3390/POLYM12081717.
  • Wan, Z., Zhang, P., Liu, Y., Lv, L., & Zhou, Y. (2020). Four-dimensional bioprinting: Current developments and applications in bone tissue engineering. Acta biomaterialia, 101, 26-42. doi: 10.1016/j.actbio.2019.10.038.
  • Yu, C., Ma, X., Zhu, W., Wang, P., Miller, K. L., Stupin, J., ... & Chen, S. (2019). Scanningless and continuous 3D bioprinting of human tissues with decellularized extracellular matrix. Biomaterials, 194, 1-13. doi: 10.1016/j.biomaterials.2018.12.009.
  • Li, Y. C., Zhang, Y. S., Akpek, A., Shin, S. R., & Khademhosseini, A. (2016). 4D bioprinting: the next-generation technology for biofabrication enabled by stimuli-responsive materials. Biofabrication, 9(1), 012001. doi: 10.1088/1758-5090/9/1/012001.
  • Yang, G. H., Yeo, M., Koo, Y. W., & Kim, G. H. (2019). 4D bioprinting: technological advances in biofabrication. Macromolecular bioscience, 19(5), 1800441. doi: 10.1002/mabi.201800441.
  • Zhang, Z., Demir, K. G., & Gu, G. X. (2019). Developments in 4D-printing: a review on current smart materials, technologies, and applications. International Journal of Smart and Nano Materials, 10(3), 205-224. doi: 10.1080/19475411.2019.1591541.
  • Chadwick, M., Yang, C., Liu, L., Gamboa, C. M., Jara, K., Lee, H., & Sabaawy, H. E. (2020). Rapid processing and drug evaluation in glioblastoma patient-derived organoid models with 4D bioprinted arrays. Iscience, 23(8), 101365. doi: 10.1016/j.isci.2020.101365.
  • Amukarimi, S., & Mozafari, M. (2021). 4D bioprinting of tissues and organs. Bioprinting, e00161. doi: 10.1016/j.bprint.2021.e00161
  • Nadgorny, M., & Ameli, A. (2018). Functional polymers and nanocomposites for 3D printing of smart structures and devices. ACS applied materials & interfaces, 10(21), 17489-17507. doi: 10.1021/acsami.8b01786
  • Yang, Q., Gao, B., & Xu, F. (2020). Recent advances in 4D bioprinting. Biotechnology journal, 15(1), 1900086. doi: 10.1002/biot.201900086
  • Klouda, L., & Mikos, A. G. (2008). Thermoresponsive hydrogels in biomedical applications. European journal of pharmaceutics and biopharmaceutics, 68(1), 34-45. doi: 10.1016/j.ejpb.2007.02.025
  • Wang, X., Sun, Y., Peng, C., Luo, H., Wang, R., & Zhang, D. (2015). Transitional suspensions containing thermosensitive dispersant for three-dimensional printing. ACS applied materials & interfaces, 7(47), 26131-26136. doi: 10.1021/acsami.5b07913
  • Zarek, M., Mansour, N., Shapira, S., & Cohn, D. (2017). 4D printing of shape memory‐based personalized endoluminal medical devices. Macromolecular rapid communications, 38(2), 1600628. doi: 10.1002/marc.201600628
  • Stoychev, G., Puretskiy, N., & Ionov, L. (2011). Self-folding all-polymer thermoresponsive microcapsules. Soft Matter, 7(7), 3277-3279. doi: 10.1039/C1SM05109A
  • Apsite, I., Stoychev, G., Zhang, W., Jehnichen, D., Xie, J., & Ionov, L. (2017). Porous stimuli-responsive self-folding electrospun mats for 4D biofabrication. Biomacromolecules, 18(10), 3178-3184.
  • Fratzl, P., & Barth, F. G. (2009). Biomaterial systems for mechanosensing and actuation. Nature, 462(7272), 442-448.
  • Lui, Y. S., Sow, W. T., Tan, L. P., Wu, Y., Lai, Y., & Li, H. (2019). 4D printing and stimuli-responsive materials in biomedical aspects. Acta biomaterialia, 92, 19-36. doi: 10.1016/j.actbio.2019.05.005
  • Gupta, M. K., Meng, F., Johnson, B. N., Kong, Y. L., Tian, L., Yeh, Y. W., ... & McAlpine, M. C. (2015). 3D printed programmable release capsules. Nano letters, 15(8), 5321-5329. doi: 10.1021/acs.nanolett.5b01688
  • Ahadian, S., Obregón, R., Ramón-Azcón, J., Salazar, G., Shiku, H., Ramalingam, M., & Matsue, T. (2016). Carbon nanotubes and graphene-based nanomaterials for stem cell differentiation and tissue regeneration. Journal of Nanoscience and Nanotechnology, 16(9), 8862-8880. doi: 10.1166/jnn.2016.12729
  • Ramon-Azcon, J., Ahadian, S., Obregon, R., Shiku, H., Ramalingam, M., & Matsue, T. (2014). Applications of carbon nanotubes in stem cell research. Journal of biomedical nanotechnology, 10(10), 2539-2561. doi: 10.1166/jbn.2014.1899
  • Sayyar, S., Bjorninen, M., Haimi, S., Miettinen, S., Gilmore, K., Grijpma, D., & Wallace, G. (2016). UV cross-linkable graphene/poly (trimethylene carbonate) composites for 3D printing of electrically conductive scaffolds. ACS applied materials & interfaces, 8(46), 31916-31925. doi: 10.1021/acsami.6b09962
  • Jakus, A. E., Secor, E. B., Rutz, A. L., Jordan, S. W., Hersam, M. C., & Shah, R. N. (2015). Three-dimensional printing of high-content graphene scaffolds for electronic and biomedical applications. ACS nano, 9(4), 4636-4648. doi: 10.1021/acsnano.5b01179
  • Kocak, G., Tuncer, C. A. N. S. E. L., & Bütün, V. J. P. C. (2017). pH-Responsive polymers. Polymer Chemistry, 8(1), 144-176. doi: 10.1039/C6PY01872F
  • Pourjavadi, A., Ebrahimi, A. A., & Barzegar, S. (2013). Preparation and evaluation of bioactive and compatible starch based superabsorbent for oral drug delivery systems. Journal of Drug Delivery Science and Technology, 23(5), 511-517. doi: 10.1016/S1773-2247(13)50074-8
  • Kwon, S. S., Kong, B. J., & Park, S. N. (2015). Physicochemical properties of pH-sensitive hydrogels based on hydroxyethyl cellulose–hyaluronic acid and for applications as transdermal delivery systems for skin lesions. European journal of pharmaceutics and biopharmaceutics, 92, 146-154. doi: 10.1016/j.ejpb.2015.02.025
  • Fundueanu, G., Constantin, M., Asmarandei, I., Harabagiu, V., Ascenzi, P., & Simionescu, B. C. (2013). The thermosensitivity of pH/thermoresponsive microspheres activated by the electrostatic interaction of pH‐sensitive units with a bioactive compound. Journal of Biomedical Materials Research Part A, 101(6), 1661-1669. doi: 10.1002/jbm.a.34469
  • Kim, S. H., Seo, Y. B., Yeon, Y. K., Lee, Y. J., Park, H. S., Sultan, M. T., ... & Park, C. H. (2020). 4D-bioprinted silk hydrogels for tissue engineering. Biomaterials, 260, 120281. doi: 10.1016/j.biomaterials.2020.120281
  • Ramos, M. L. P., González, J. A., Fabian, L., Pérez, C. J., Villanueva, M. E., & Copello, G. J. (2017). Sustainable and smart keratin hydrogel with pH-sensitive swelling and enhanced mechanical properties. Materials Science and Engineering: C, 78, 619-626. doi: 10.1016/j.msec.2017.04.120
  • Narupai, B., Smith, P. T., & Nelson, A. (2021). 4D Printing of Multi‐Stimuli Responsive Protein‐Based Hydrogels for Autonomous Shape Transformations. Advanced Functional Materials, 2011012. doi: 10.1002/adfm.202011012
  • Yoshida, T., Lai, T. C., Kwon, G. S., & Sako, K. (2013). pH-and ion-sensitive polymers for drug delivery. Expert opinion on drug delivery, 10(11), 1497-1513. doi: 10.1517/17425247.2013.821978
  • Dong, Y., Wang, S., Ke, Y., Ding, L., Zeng, X., Magdassi, S., & Long, Y. (2020). 4D printed hydrogels: fabrication, materials, and applications. Advanced Materials Technologies, 5(6), 2000034. doi: 10.1002/admt.202000034
  • Rudko, M., Urbaniak, T., & Musiał, W. (2021). Recent Developments in Ion-Sensitive Systems for Pharmaceutical Applications. Polymers, 13(10), 1641. doi: 10.3390/polym13101641
  • Wang, B., Liu, L., & Liao, L. (2019). Light and ferric ion responsive fluorochromic hydrogels with high strength and self-healing ability. Polymer Chemistry, 10(47), 6481-6488. doi: 10.1039/C9PY01459D
  • Wu, Q., Wang, L., Yu, H., Wang, J., & Chen, Z. (2011). Organization of glucose-responsive systems and their properties. Chemical reviews, 111(12), 7855-7875. doi: 10.1021/cr200027j
  • Adams, A., Malkoc, A., & La Belle, J. T. (2018). The development of a glucose dehydrogenase 3D-printed glucose sensor: a proof-of-concept study. Journal of diabetes science and technology, 12(1), 176-182. doi: 10.1177/1932296817715272
  • Matsumoto, A., Ishii, T., Nishida, J., Matsumoto, H., Kataoka, K., & Miyahara, Y. (2012). A synthetic approach toward a self‐regulated insulin delivery system. Angewandte Chemie International Edition, 51(9), 2124-2128. doi: 10.1002/anie.201106252
  • Brownlee, M., & Cerami, A. (1979). A glucose-controlled insulin-delivery system: semisynthetic insulin bound to lectin. Science, 206(4423), 1190-1191. doi: 10.1126/science.505005
  • Wang, J., Zhang, H., Wang, F., Ai, X., Huang, D., Liu, G., & Mi, P. (2018). Enzyme-responsive polymers for drug delivery and molecular imaging. In Stimuli Responsive Polymeric Nanocarriers for Drug Delivery Applications, Volume 1 (pp. 101-119). Woodhead Publishing. doi: 10.1016/B978-0-08-101997-9.00004-7
  • Zelzer, M., Todd, S. J., Hirst, A. R., McDonald, T. O., & Ulijn, R. V. (2013). Enzyme responsive materials: design strategies and future developments. Biomaterials Science, 1(1), 11-39. doi: 10.1039/C2BM00041E
  • Wang, X., Qin, X. H., Hu, C., Terzopoulou, A., Chen, X. Z., Huang, T. Y., ... & Nelson, B. J. (2018). 3D printed enzymatically biodegradable soft helical microswimmers. Advanced Functional Materials, 28(45), 1804107. doi: 10.1002/adfm.201804107
  • Banerjee, A., Arha, M., Choudhary, S., Ashton, R. S., Bhatia, S. R., Schaffer, D. V., Kane, R. S. (2009). The influence of hydrogel modulus on the proliferation and differentiation of encapsulated neural stem cells. Biomaterials. Sep;30(27):4695-9. doi: 10.1016/j.biomaterials.2009.05.050. Epub 2009 Jun 17.
  • Chang, Y. J., Tsai, C. J., Tseng, F. G., Chen, T. J., Wang, T. W. (2013). Micropatterned stretching system for the investigation of mechanical tension on neural stem cells behavior. Nanomedicine. Apr;9(3):345-55. doi: 10.1016/j.nano.2012.07.008. Epub 2012 Aug 24.
  • Lozano, R., Stevens, L., Thompson, B. C., Gilmore, K. J., Gorkin III, R., Stewart, E. M., in het Panhuis, M., Romero-Ortega, M. and Wallace, G.G. (2015). 3D printing of layered brain-like structures using peptide modified gellan gum substrates. Biomaterials, 67, 264-273. doi:10.1016/j.biomaterials.2015.07.022
  • Lorber, B., Hsiao, W. K., Hutchings, I. M., & Martin, K. R. (2013). Adult rat retinal ganglion cells and glia can be printed by piezoelectric inkjet printing. Biofabrication, 6(1), 015001. doi:10.1088/1758-5082/6/1/015001
  • Miao, S., Castro, N., Nowicki, M., Xia, L., Cui, H., Zhou, X., Zhu, W., Lee, S. J., Sarkar, K., Vozzi, G., Tabata, Y., Fisher, J., & Zhang, L. G. (2017). 4D printing of polymeric materials for tissue and organ regeneration. Materials today (Kidlington, England), 20(10), 577–591. doi: 10.1016/j.mattod.2017.06.005
  • Miao, S., Cui, H., Nowicki, M., Lee, S.J., Almeida, J., Zhou, X., Zhu, W., Yao, X., Masood, F., Plesniak, M.W. and Mohiuddin, M., 2018. Photolithographic-stereolithographic-tandem fabrication of 4D smart scaffolds for improved stem cell cardiomyogenic differentiation. Biofabrication, 10(3), p.035007. https://doi.org/10.1088/1758-5090/aabe0b
  • Miao, S., Cui, H., Nowicki, M., Xia, L., Zhou, X., Lee, S. J., ... & Zhang, L. G. (2018). Stereolithographic 4D bioprinting of multiresponsive architectures for neural engineering. Advanced biosystems, 2(9), 1800101. https://doi.org/10.1002/adbi.201800101
  • Cui, C., Kim, D. O., Pack, M. Y., Han, B., Han, L., Sun, Y., & Han, L. H. (2020). 4D printing of self-folding and cell-encapsulating 3D microstructures as scaffolds for tissue-engineering applications. Biofabrication, 12(4), 045018.
  • Zhu, W., George, J. K., Sorger, V. J., & Grace Zhang, L. (2017). 3D printing scaffold coupled with low level light therapy for neural tissue regeneration. Biofabrication, 9(2), 025002. doi:10.1088/1758-5090/aa6999
  • Melissinaki, V., Gill, A. A., Ortega, I., Vamvakaki, M., Ranella, A., Haycock, J. W., … Claeyssens, F. (2011). Direct laser writing of 3D scaffolds for neural tissue engineering applications. Biofabrication, 3(4), 045005. doi:10.1088/1758-5082/3/4/045005
  • Raviv, D., Zhao, W., McKnelly, C., Papadopoulou, A., Kadambi, A., Shi, B., ... & Tibbits, S. (2014). Active printed materials for complex self-evolving deformations. Scientific reports, 4(1), 1-8. doi: 10.1038/srep07422
  • Zhang, Y. S., Aleman, J., Shin, S. R., Kilic, T., Kim, D., Shaegh, S. A. M., ... & Khademhosseini, A. (2017). Multisensor-integrated organs-on-chips platform for automated and continual in situ monitoring of organoid behaviors. Proceedings of the National Academy of Sciences, 114(12), E2293-E2302. doi: 10.1073/pnas.1612906114
  • Shin, S. R., Zhang, Y. S., Kim, D. J., Manbohi, A., Avci, H., Silvestri, A., ... & Khademhosseini, A. (2016). Aptamer-based microfluidic electrochemical biosensor for monitoring cell-secreted trace cardiac biomarkers. Analytical chemistry, 88(20), 10019-10027. doi: 10.1021/acs.analchem.6b02028
  • Shin, S. R., Kilic, T., Zhang, Y. S., Avci, H., Hu, N., Kim, D., ... & Khademhosseini, A. (2017). Label‐Free and Regenerative Electrochemical Microfluidic Biosensors for Continual Monitoring of Cell Secretomes. Advanced Science, 4(5), 1600522. doi: 10.1002/advs.201600522
  • Hüseyin, A. V. C. I., GÜZEL, F. D., Salim, E. R. O. L., & Akpek, A. (2017). Recent advances in organ-on-a-chip technologies and future challenges: a review. Turkish Journal of Chemistry, 42(3), 587-610. doi:10.3906/kim-1611-35
  • Akpek, A., Öztürk, A. B., Alarçin, E., Huseyin, A. V. C. İ., & ADALI, M. A. Recent Advances in 4D Bioprinting. Research Journal of Biomedical and Biotechnology, 1(1), 20-23.
Toplam 70 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Doku Mühendisliği, Biyomateryaller
Bölüm Derlemeler
Yazarlar

Merve Nur Soykan 0000-0003-1231-9791

Tayfun Şengel 0000-0002-1162-6979

Aliakbar Ebrahimi 0000-0001-6437-7796

Murat Kaya 0000-0002-4277-6304

Burcugül Altuğ Tasa 0000-0003-4460-8467

Hamed Ghorbanpoor 0000-0002-2665-8172

Onur Uysal 0000-0001-6800-5607

Ayla Eker Sarıboyacı 0000-0003-4536-9859

Huseyin Avci 0000-0002-2475-1963

Yayımlanma Tarihi 31 Aralık 2021
Yayımlandığı Sayı Yıl 2021 Cilt: 3 Sayı: 2

Kaynak Göster

APA Soykan, M. N., Şengel, T., Ebrahimi, A., Kaya, M., vd. (2021). Four-Dimensional Printing Technology at the Frontier of Advanced Modeling and Applications in Brain Tissue Engineering. Journal of Medical Innovation and Technology, 3(2), 46-57. https://doi.org/10.51934/jomit.1016838
AMA Soykan MN, Şengel T, Ebrahimi A, Kaya M, Altuğ Tasa B, Ghorbanpoor H, Uysal O, Eker Sarıboyacı A, Avci H. Four-Dimensional Printing Technology at the Frontier of Advanced Modeling and Applications in Brain Tissue Engineering. Journal of Medical Innovation and Technology. Aralık 2021;3(2):46-57. doi:10.51934/jomit.1016838
Chicago Soykan, Merve Nur, Tayfun Şengel, Aliakbar Ebrahimi, Murat Kaya, Burcugül Altuğ Tasa, Hamed Ghorbanpoor, Onur Uysal, Ayla Eker Sarıboyacı, ve Huseyin Avci. “Four-Dimensional Printing Technology at the Frontier of Advanced Modeling and Applications in Brain Tissue Engineering”. Journal of Medical Innovation and Technology 3, sy. 2 (Aralık 2021): 46-57. https://doi.org/10.51934/jomit.1016838.
EndNote Soykan MN, Şengel T, Ebrahimi A, Kaya M, Altuğ Tasa B, Ghorbanpoor H, Uysal O, Eker Sarıboyacı A, Avci H (01 Aralık 2021) Four-Dimensional Printing Technology at the Frontier of Advanced Modeling and Applications in Brain Tissue Engineering. Journal of Medical Innovation and Technology 3 2 46–57.
IEEE M. N. Soykan, T. Şengel, A. Ebrahimi, M. Kaya, B. Altuğ Tasa, H. Ghorbanpoor, O. Uysal, A. Eker Sarıboyacı, ve H. Avci, “Four-Dimensional Printing Technology at the Frontier of Advanced Modeling and Applications in Brain Tissue Engineering”, Journal of Medical Innovation and Technology, c. 3, sy. 2, ss. 46–57, 2021, doi: 10.51934/jomit.1016838.
ISNAD Soykan, Merve Nur vd. “Four-Dimensional Printing Technology at the Frontier of Advanced Modeling and Applications in Brain Tissue Engineering”. Journal of Medical Innovation and Technology 3/2 (Aralık 2021), 46-57. https://doi.org/10.51934/jomit.1016838.
JAMA Soykan MN, Şengel T, Ebrahimi A, Kaya M, Altuğ Tasa B, Ghorbanpoor H, Uysal O, Eker Sarıboyacı A, Avci H. Four-Dimensional Printing Technology at the Frontier of Advanced Modeling and Applications in Brain Tissue Engineering. Journal of Medical Innovation and Technology. 2021;3:46–57.
MLA Soykan, Merve Nur vd. “Four-Dimensional Printing Technology at the Frontier of Advanced Modeling and Applications in Brain Tissue Engineering”. Journal of Medical Innovation and Technology, c. 3, sy. 2, 2021, ss. 46-57, doi:10.51934/jomit.1016838.
Vancouver Soykan MN, Şengel T, Ebrahimi A, Kaya M, Altuğ Tasa B, Ghorbanpoor H, Uysal O, Eker Sarıboyacı A, Avci H. Four-Dimensional Printing Technology at the Frontier of Advanced Modeling and Applications in Brain Tissue Engineering. Journal of Medical Innovation and Technology. 2021;3(2):46-57.