Graphical Abstract

Four-dimensional (4D) printing is an emerging and highly innovative additive manufacturing process by which to fabricate pre-designed, self-assembly structures with the ability to transform over time. However, one of the critical challenges of 4D printing is the lack of advanced 4D printing systems that not only meet all the essential requirements of shape change but also possess smart, dynamic capabilities to spatiotemporally and instantly control the shape-transformation process. Here, we present a facile 4D printing platform which incorporates nanomaterials into the conventional stimuli-responsive polymer, allowing the 4D printed object to achieve a dynamic and remote controlled, on-time and position shape transformation. A proof-of-concept 4D printed brain model was created using near-infrared light (NIR) responsive nanocomposite to evaluate the capacity for controllable 4D transformation, and the feasibility of photothermal stimulation for modulating neural stem cell behaviors. This novel 4D printing strategy can not only be used to create dynamic 3D patterned biological structures that can spatiotemporally control their shapes or behaviors of transformation under a human benign stimulus (NIR), but can also provide a potential method for building complex self-morphing objects for widespread applications.
Miao, S. D.; Castro, N.; Nowicki, M.; Xia, L.; Cui, H. T.; Zhou, X.; Zhu, W.; Lee, S. J.; Sarkar, K.; Vozzi, G. et al. 4D printing of polymeric materials for tissue and organ regeneration. Mater. Today 2017, 20, 577-591.
Shin, D. G.; Kim, T. H.; Kim, D. E. Review of 4D printing materials and their properties. Int. J. Precis. Eng. Manuf. -Green Tech. 2017, 4, 349-357.
Cui, H. T.; Nowicki, M.; Fisher, J. P.; Zhang, L. G. 3D bioprinting for organ regeneration. Adv. Healthc. Mater. 2017, 6, 1601118.
Cui, H. T.; Miao, S. D.; Esworthy, T.; Zhou, X.; Lee, S. J.; Liu, C. Y.; Yu, Z. X.; Fisher, J. P.; Mohiuddin, M.; Zhang, L. G. 3D bioprinting for cardiovascular regeneration and pharmacology. Adv. Drug Deliv. Rev. 2018, 132, 252-269.
Deng, C. J.; Yao, Q. Q.; Feng, C.; Li, J. Y.; Wang, L. M.; Cheng, G. F.; Shi, M. C.; Chen, L.; Chang, J.; Wu, C. T. 3D printing of bilineage constructive biomaterials for bone and cartilage regeneration. Adv. Funct. Mater. 2017, 27, 1703117.
Yang, B. W.; Yin, J. H.; Chen, Y.; Pan, S. S.; Yao, H. L.; Gao, Y. S.; Shi, J. L. 2D-black-phosphorus-reinforced 3D-printed scaffolds: A stepwise countermeasure for osteosarcoma. Adv. Mater. 2018, 30, 1705611.
Lalwani, G.; D'Agati, M.; Khan, A. M.; Sitharaman, B. Toxicology of graphene-based nanomaterials. Adv. Drug Deliv. Rev. 2016, 105, 109-144.
Zhao, Q. L.; Wang, J.; Cui, H. Q.; Chen, H. X.; Wang, Y. L.; Du, X. M. Programmed shape-morphing scaffolds enabling facile 3D endothelialization. Adv. Funct. Mater. 2018, 28, 1801027.
Li, Y. C.; Zhang, Y. S.; Akpek, A.; Shin, S. R.; Khademhosseini, A. 4D bioprinting: The next-generation technology for biofabrication enabled by stimuli-responsive materials. Biofabrication 2016, 9, 012001.
Choi, J.; Kwon, O. C.; Jo, W.; Lee, H. J.; Moon, M. W. 4D printing technology: A review. 3D Print. Addit. Manuf. 2015, 2, 159-167.
Miao, S. D.; Cui, H. T.; Nowicki, M.; Xia, L.; Zhou, X.; Lee, S. J.; Zhu, W.; Sarkar, K.; Zhang, Z. Y.; Zhang, L. G. Stereolithographic 4D bioprinting of multiresponsive architectures for neural engineering. Adv. Biosyst. 2018, 2, 1800101.
Gladman, A. S.; Matsumoto, E. A.; Nuzzo, R. G.; Mahadevan, L.; Lewis, J. A. Biomimetic 4D printing. Nat. Mater. 2016, 15, 413-418.
Huang, L. M.; Jiang, R. Q.; Wu, J. J.; Song, J. Z.; Bai, H.; Li, B. G.; Zhao, Q.; Xie, T. Ultrafast digital printing toward 4D shape changing materials. Adv. Mater. 2017, 29, 1605390.
Lee, A. Y.; An, J.; Chua, C. K. Two-way 4D printing: A review on the reversibility of 3D-printed shape memory materials. Engineering 2017, 3, 663-674.
Ding, Z.; Yuan, C.; Peng, X. R.; Wang, T. J.; Qi, H. J.; Dunn, M. L. Direct 4D printing via active composite materials. Sci. Adv. 2017, 3, e1602890.
Li, W. B.; Liu, Y. J.; Leng, J. S. Selectively actuated multi-shape memory effect of a polymer multicomposite. J. Mater. Chem. A 2015, 3, 24532-24539.
Wei, H. Q.; Zhang, Q. W.; Yao, Y. T.; Liu, L. W.; Liu, Y. J.; Leng, J. S. Direct-write fabrication of 4D active shape-changing structures based on a shape memory polymer and its nanocomposite. ACS Appl. Mater. Interfaces 2017, 9, 876-883.
Miao, S. D.; Zhu, W.; Castro, N. J.; Nowicki, M.; Zhou, X.; Cui, H. T.; Fisher, J. P.; Zhang, L. G. 4D printing smart biomedical scaffolds with novel soybean oil epoxidized acrylate. Sci. Rep. 2016, 6, 27226.
Miao, S. D.; Cui, H. T.; Nowicki, M.; Lee, S. J.; Almeida, J.; Zhou, X.; Zhu, W.; Yao, X. L.; Masood, F.; Plesniak, M. W. et al. Photolithographic-stereolithographic-tandem fabrication of 4D smart scaffolds for improved stem cell cardiomyogenic differentiation. Biofabrication 2018, 10, 035007.
Miao, S. D.; Zhu, W.; Castro, N. J.; Leng, J. S.; Zhang, L. G. Four-dimensional printing hierarchy scaffolds with highly biocompatible smart polymers for tissue engineering applications. Tissue Eng. Part C Methods 2016, 22, 952-963.
Chen, A. C.; Chatterjee, S. Nanomaterials based electrochemical sensors for biomedical applications. Chem. Soc. Rev. 2013, 42, 5425-5438.
Chung, C.; Kim, Y. K.; Shin, D.; Ryoo, S. R.; Hong, B. H.; Min, D. H. Biomedical applications of graphene and graphene oxide. Acc. Chem. Res. 2013, 46, 2211-2224.
Gao, J. H.; Gu, H. W.; Xu, B. Multifunctional magnetic nanoparticles: Design, synthesis, and biomedical applications. Acc. Chem. Res. 2009, 42, 1097-1107.
Blum, A. P.; Kammeyer, J. K.; Rush, A. M.; Callmann, C. E.; Hahn, M. E.; Gianneschi, N. C. Stimuli-responsive nanomaterials for biomedical applications. J. Am. Chem. Soc. 2015, 137, 2140-2154.
Shen, H.; Zhang, L. M.; Liu, M.; Zhang, Z. J. Biomedical applications of graphene. Theranostics 2012, 2, 283-294.
Yang, Y. Q.; Asiri, A. M.; Tang, Z. W.; Du, D.; Lin, Y. H. Graphene based materials for biomedical applications. Mater. Today 2013, 16, 365-373.
Jakus, A. E.; Secor, E. B.; Rutz, A. L.; Jordan, S. W.; Hersam, M. C.; Shah, R. N. Three-dimensional printing of high-content graphene scaffolds for electronic and biomedical applications. ACS Nano 2015, 9, 4636-4648.
Zhou, X.; Nowicki, M.; Cui, H. T.; Zhu, W.; Fang, X. Q.; Miao, S. D.; Lee, S. J.; Keidar, M.; Zhang, L. J. G. 3D bioprinted graphene oxide-incorporated matrix for promoting chondrogenic differentiation of human bone marrow mesenchymal stem cells. Carbon 2017, 116, 615-624.
Xie, T.; Rousseau, I. A. Facile tailoring of thermal transition temperatures of epoxy shape memory polymers. Polymer 2009, 50, 1852-1856.
Wei, J. C.; Atif, R.; Vo, T.; Inam, F. Graphene nanoplatelets in epoxy system: Dispersion, reaggregation, and mechanical properties of nanocomposites. J. Nanomater. 2015, 2015, Article ID 561742.
Cui, H. T.; Liu, Y. D.; Cheng, Y. L.; Zhang, Z.; Zhang, P. B.; Chen, X. S.; Wei, Y. In vitro study of electroactive tetraaniline-containing thermosensitive hydrogels for cardiac tissue engineering. Biomacromolecules 2014, 15, 1115-1123.
Zhu, W.; Ye, T.; Lee, S. J.; Cui, H. T.; Miao, S. D.; Zhou, X.; Shuai, D. M.; Zhang, L. G. Enhanced neural stem cell functions in conductive annealed carbon nanofibrous scaffolds with electrical stimulation. Nanomedicine 2018, 14, 2485-2494.
Cui, H. T.; Wang, Y.; Cui, L. G.; Zhang, P. B.; Wang, X. H.; Wei, Y.; Chen, X. S. In vitro studies on regulation of osteogenic activities by electrical stimulus on biodegradable electroactive polyelectrolyte multilayers. Biomacromolecules 2014, 15, 3146-3157.
Cui, H. T.; Shao, J.; Wang, Y.; Zhang, P. B.; Chen, X. S.; Wei, Y. PLA-PEG-PLA and its electroactive tetraaniline copolymer as multi-interactive injectable hydrogels for tissue engineering. Biomacromolecules 2013, 14, 1904-1912.
Zhou, X.; Cui, H. T.; Nowicki, M.; Miao, S. D.; Lee, S. J.; Masood, F.; Harris, B. T.; Zhang, L. G. Three-dimensional-bioprinted dopamine-based matrix for promoting neural regeneration. ACS Appl. Mater. Interfaces 2018, 10, 8993-9001.
Cui, H. T.; Zhu, W.; Holmes, B.; Zhang, L. G. Biologically inspired smart release system based on 3D bioprinted perfused scaffold for vascularized tissue regeneration. Adv. Sci. 2016, 3, 1600058.
Cui, H. T.; Zhu, W.; Nowicki, M.; Zhou, X.; Khademhosseini, A.; Zhang, L. G. Hierarchical fabrication of engineered vascularized bone biphasic constructs via dual 3D bioprinting: Integrating regional bioactive factors into architectural design. Adv. Healthc. Mater. 2016, 5, 2174-2181.