Swelling-Dependent Shape-Based Transformation of a Human Mesenchymal Stromal Cells-Laden 4D Bioprinted Construct for Cartilage Tissue Engineering.
4D bioprinting
biofabrication
shape-change
smart bioinks
tissue engineering
Journal
Advanced healthcare materials
ISSN: 2192-2659
Titre abrégé: Adv Healthc Mater
Pays: Germany
ID NLM: 101581613
Informations de publication
Date de publication:
01 2023
01 2023
Historique:
revised:
10
10
2022
received:
29
07
2022
pubmed:
30
10
2022
medline:
18
1
2023
entrez:
29
10
2022
Statut:
ppublish
Résumé
3D bioprinting is usually implemented on flat surfaces, posing serious limitations in the fabrication of multilayered curved constructs. 4D bioprinting, combining 3D bioprinting with time-dependent stimuli-induced transformation, enables the fabrication of shape-changing constructs. Here, a 4D biofabrication method is reported for cartilage engineering based on the differential swelling of a smart multi-material system made from two hydrogel-based materials: hyaluronan and alginate. Two ink formulations are used: tyramine-functionalized hyaluronan (HAT, high-swelling) and alginate with HAT (AHAT, low-swelling). Both inks have similar elastic, shear-thinning, and printability behavior. The inks are 3D printed into a bilayered scaffold before triggering the shape-change by using liquid immersion as stimulus. In time (4D), the differential swelling between the two zones leads to the scaffold's self-bending. Different designs are made to tune the radius of curvature and shape. A bioprinted formulation of AHAT and human bone marrow cells demonstrates high cell viability. After 28 days in chondrogenic medium, the curvature is clearly present while cartilage-like matrix production is visible on histology. A proof-of-concept of the recently emerged technology of 4D bioprinting with a specific application for the design of curved structures potentially mimicking the curvature and multilayer cellular nature of native cartilage is demonstrated.
Identifiants
pubmed: 36308047
doi: 10.1002/adhm.202201891
doi:
Substances chimiques
Hyaluronic Acid
9004-61-9
Hydrogels
0
Alginates
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2201891Informations de copyright
© 2022 The Authors. Advanced Healthcare Materials published by Wiley-VCH GmbH.
Références
Y. Chen, J. Zhang, X. Liu, S. Wang, J. Tao, Y. Huang, W. Wu, Y. Li, K. Zhou, X. Wei, S. Chen, X. Li, X. Xu, L. Cardon, Z. Qian, M. Gou, Sci. Adv. 2020, 6, eaba7406.
M. Costantini, S. Testa, P. Mozetic, A. Barbetta, C. Fuoco, E. Fornetti, F. Tamiro, S. Bernardini, J. Jaroszewicz, W. Święszkowski, M. Trombetta, L. Castagnoli, D. Seliktar, P. Garstecki, G. Cesareni, S. Cannata, A. Rainer, C. Gargioli, Biomaterials 2017, 131, 98.
A. Lee, A. R. Hudson, D. J. Shiwarski, J. W. Tashman, T. J. Hinton, S. Yerneni, J. M. Bliley, P. G. Campbell, A. W. Feinberg, Science 2019, 365, 482.
J. Groll, T. Boland, T. Blunk, J. A. Burdick, D.-W. Cho, P. D. Dalton, B. Derby, G. Forgacs, Q. Li, V. A. Mironov, L. Moroni, M. Nakamura, W. Shu, S. Takeuchi, G. Vozzi, T. B. F. Woodfield, T. Xu, J. J. Yoo, J. Malda, Biofabrication 2016, 8, 013001.
T. Jiang, J. G. Munguia-Lopez, S. Flores-Torres, J. Kort-Mascort, J. M. Kinsella, Appl. Phys. Rev. 2019, 6, 011310.
X. Li, B. Liu, B. Pei, J. Chen, D. Zhou, J. Peng, X. Zhang, W. Jia, T. Xu, Chem. Rev. 2020, 120, 10793.
W. L. Ng, J. M. Lee, M. Zhou, Y.-W. Chen, K.-X. A. Lee, W. Y. Yeong, Y.-F. Shen, Biofabrication 2020, 12, 022001.
W. Sun, B. Starly, A. C. Daly, J. A. Burdick, J. Groll, G. Skeldon, W. Shu, Y. Sakai, M. Shinohara, M. Nishikawa, J. Jang, D.-W. Cho, M. Nie, S. Takeuchi, S. Ostrovidov, A. Khademhosseini, R. D. Kamm, V. Mironov, L. Moroni, I. T. Ozbolat, Biofabrication 2020, 12, 022002.
A. Schwab, R. Levato, M. D'Este, S. Piluso, D. Eglin, J. Malda, Chem. Rev. 2020, 120, 11028.
H.-J. Jeong, H. Nam, J. Jang, S.-J. Lee, Bioengineering 2020, 7, 32.
A. A. Giannopoulos, D. Mitsouras, S.-J. Yoo, P. P. Liu, Y. S. Chatzizisis, F. J. Rybicki, Nat. Rev. Cardiol. 2016, 13, 701.
D. Richards, J. Jia, M. Yost, R. Markwald, Y. Mei, Ann. Biomed. Eng. 2017, 45, 132.
T. Van Manen, S. Janbaz, K. M. B. Jansen, A. A. Zadpoor, Commun. Mater. 2021, 2, 56.
B. Gao, Q. Yang, X. Zhao, G. Jin, Y. Ma, F. Xu, Trends Biotechnol. 2016, 34, 746.
Y.-C. Li, Y. S. Zhang, A. Akpek, S. R. Shin, A. Khademhosseini, Biofabrication 2016, 9, 012001.
T. Van Manen, S. Janbaz, A. A. Zadpoor, Mater. Horiz. 2017, 4, 1064.
W. J. Hendrikson, J. Rouwkema, F. Clementi, C. A. Van Blitterswijk, S. Farè, L. Moroni, Biofabrication 2017, 9, 031001.
S. H. Kim, Y. B. Seo, Y. K. Yeon, Y. J. Lee, H. S. Park, Md. T. Sultan, J. M. Lee, J. S. Lee, O J. Lee, H. Hong, H. Lee, O. Ajiteru, Y. J. Suh, S.-H. Song, K.-H. Lee, C. H. Park, Biomaterials 2020, 260, 120281.
G. H. Yang, W. Kim, J. Kim, G. Kim, Theranostics 2021, 11, 48.
V. Du, N. Luciani, S. Richard, G. T. Mary, C. Gay, F. §. O. Mazuel, M. Reffay, P. Menasché, O. Agbulut, C. Wilhelm, Nat. Commun. 2017, 8, 400.
Y. Luo, X. Lin, B. Chen, X. Wei, Biofabrication 2019, 11, 045019.
Y. bin Lee, O. Jeon, S. J. Lee, A. Ding, D. Wells, E. Alsberg, Adv. Funct. Mater. 2021, 31, 2010104.
A. Ding, S. J. Lee, R. Tang, K. L. Gasvoda, F. He, E. Alsberg, Small 2022, 18, 2202196.
A. Ding, O. Jeon, D. Cleveland, K. L. Gasvoda, D. Wells, S. J. Lee, E. Alsberg, Adv. Mater. 2022, 34, 2109394.
A. Kirillova, R. Maxson, G. Stoychev, C. T. Gomillion, L. Ionov, Adv. Mater. 2017, 29, 1703443.
C. Vergallo, L. Dini, Sustainability 2018, 10, 2776.
M. G. Li, X. Y. Tian, X. Chen, Artif. Organs 2011, 35, 741.
M. Klak, M. Gomółka, T. Dobrzański, G. Tymicki, P. Cywoniuk, P. Kowalska, K. Kosowska, T. Bryniarski, A. Berman, A. Dobrzyå„, J. Idaszek, PLoS One 2020, 15, e0235052.
C. Huang, Z. Wang, D. Quinn, S. Suresh, K. J. Hsia, Proc. Natl. Acad. Sci. USA 2018, 115, 12359.
R. Kempaiah, Z. Nie, J. Mater. Chem. B 2014, 2, 2357.
D. Petta, A. R. Armiento, D. Grijpma, M. Alini, D. Eglin, M. D'Este, Biofabrication 2018, 10, 044104.
M. N. Collins, C. Birkinshaw, Carbohydr. Polym. 2013, 92, 1262.
S. Stichler, T. Böck, N. Paxton, S. Bertlein, R. Levato, V. Schill, W. Smolan, J. Malda, J. Teßmar, T. Blunk, J. Groll, Biofabrication 2017, 9, 044108.
A. Abbadessa, V. H. M. Mouser, M. M. Blokzijl, D. Gawlitta, W. J. A. Dhert, W. E. Hennink, J. Malda, T. Vermonden, Biomacromolecules 2016, 17, 2137.
K.-C. Hung, C.-S. Tseng, L.-G. Dai, S.-H. Hsu, Biomaterials 2016, 83, 156.
J. Kundu, J.-H. Shim, J. Jang, S.-W. Kim, D.-W. Cho, J. Tissue Eng. Regener. Med. 2015, 9, 1286.
K. Markstedt, A. Mantas, I. Tournier, H. Martínez Ávila, D. Hägg, P. Gatenholm, Biomacromolecules 2015, 16, 1489.
M. Müller, E. Öztürk, Ø. Arlov, P. Gatenholm, M. Zenobi-Wong, Ann. Biomed. Eng. 2017, 45, 210.
A. Dimaraki, P. J. Díaz-Payno, M. Minneboo, M. Nouri-Goushki, M. Hosseini, N. Kops, R. Narcisi, M. J. Mirzaali, G. J. V. M. Van Osch, L. E. Fratila-Apachitei, A. A. Zadpoor, Appl. Sci. 2021, 11, 7821.
P. Rastogi, B. Kandasubramanian, Biofabrication 2019, 11, 042001.
E. Axpe, M. Oyen, Int. J. Mol. Sci. 2016, 17, 1976.
B. Wang, P. J. Díaz-Payno, D. C. Browe, F. E. Freeman, J. Nulty, R. Burdis, D. J. Kelly, Acta Biomater. 2021, 128, 130.
W. J. C. M. Marijnissen, G. J. V. M. Van Osch, J. Aigner, S. W. van der Veen, A. P. Hollander, H. T. L. Verwoerd-Verhoef, J. A. N. Verhaar, Biomaterials 2002, 23, 1511.
H. J. Hauselmann, K. Masuda, E. B. Hunziker, M. Neidhart, S. S. Mok, B. A. Michel, E. J. Thonar, Am. J. Physiol.: Cell Physiol. 1996, 271, C742.
N. Hendrijantini, Dent. J. 2019, 52, 36.
D. M. W. Anderson, W. G. Brydon, M. A. Eastwood, D. M. Sedgwick, Food Addit. Contam. 1991, 8, 237.
A. R. Kim, J. H. Hwang, H. M. Kim, H. N. Kim, J. E. Song, Y. I. Yang, K. H. Yoon, D. Lee, G. Khang, J. Biomater. Sci., Polym. Ed. 2013, 24, 1084.
S. N. Pawar, K. J. Edgar, Biomaterials 2012, 33, 3279.
N. E. Simpson, C. L. Stabler, C. P. Simpson, A. Sambanis, I. Constantinidis, Biomaterials 2004, 25, 2603.
D. Petta, D. W. Grijpma, M. Alini, D. Eglin, M. D'Este, ACS Biomater. Sci. Eng. 2018, 4, 3088.
W. Ostwald, Kolloid-Z. 1929, 47, 176.
A. J. Lin, J. L. Bernstein, J. A. Spector, Curr. Surg. Rep. 2018, 6, 4.
G. M. Cunniffe, P. J. Díaz-Payno, E. J. Sheehy, S. E. Critchley, H. V. Almeida, P. Pitacco, S. F. Carroll, O. R. Mahon, A. Dunne, T. J. Levingstone, C. J. Moran, R. T. Brady, F. J. O'brien, P. A. J. Brama, D. J. Kelly, Biomaterials 2019, 188, 63.
D. C. Browe, P. J. Díaz-Payno, F. E. Freeman, R. Schipani, R. Burdis, D. P. Ahern, J. M. Nulty, S. Guler, L. D. Randall, C. T. Buckley, P. A. J. Brama, D. J. Kelly, Acta Biomater. 2022, 143, 266.
A. Schwab, C. Hélary, R. G. Richards, M. Alini, D. Eglin, M. D'este, Mater. Today Bio 2020, 7, 100058.
T. Gao, G. J. Gillispie, J. S. Copus, A. K. Pr, Y.-J. Seol, A. Atala, J. J. Yoo, S. J. Lee, Biofabrication 2018, 10, 034106.
I. Gorroñogoitia, U. Urtaza, A. Zubiarrain-Laserna, A. Alonso-Varona, A. M. Zaldua, Polymers 2022, 14, 354.
T. Billiet, E. Gevaert, T. De Schryver, M. Cornelissen, P. Dubruel, Biomaterials 2014, 35, 49.
A. Skardal, J. Zhang, G. D. Prestwich, Biomaterials 2010, 31, 6173.
M. A. Leroux, F. Guilak, L. A. Setton, J. Biomed. Mater. Res. 1999, 47, 46.
C. B. Shah, S. M. Barnett, J. Appl. Polym. Sci. 1992, 45, 293.
T. van Manen, A. A. Zadpoor, Theoretical stiffness limits of 4D printed self-folding metamaterials, arXiv, 2021, https://doi.org/10.48550/ARXIV.2106.05790.
I. Apsite, G. Constante, M. Dulle, L. Vogt, A. Caspari, A. R. Boccaccini, A. Synytska, S. Salehi, L. Ionov, Biofabrication 2020, 12, 035027.
N. Paxton, W. Smolan, T. Böck, F. Melchels, J. Groll, T. Jungst, Biofabrication 2017, 9, 044107.
K. A. Deo, K. A. Singh, C. W. Peak, D. L. Alge, A. K. Gaharwar, Tissue Eng., Part A 2020, 26, 318.
R. Taymour, D. Kilian, T. Ahlfeld, M. Gelinsky, A. Lode, Sci. Rep. 2021, 11, 5130.
C. Norotte, F. S. Marga, L. E. Niklason, G. Forgacs, Biomaterials 2009, 30, 5910.
F. Xu, J. Celli, I. Rizvi, S. Moon, T. Hasan, U. Demirci, Biotechnol. J. 2011, 6, 204.
J. A. Brassard, M. Nikolaev, T. Hasan, M. Hofer, M. P. Lutolf, Nat. Mater. 2021, 20, 22.
S.-H. Park, S. R. Park, S. I. Chung, K. S. Pai, B.-H. Min, Artif. Organs 2005, 29, 838.
R. Ziadlou, S. Rotman, A. Teuschl, E. Salzer, A. Barbero, I. Martin, M. Alini, D. Eglin, S. Grad, Mater. Sci. Eng., C 2021, 120, 111701.
F. Z. Cui, W. M. Tian, S. P. Hou, Q. Y. Xu, I. - S. Lee, J. Mater. Sci.: Mater. Med. 2006, 17, 1393.
R. Mhanna, J. Becher, M. Schnabelrauch, R. L. Reis, I. Pashkuleva, Adv. Biosyst. 2017, 1, 1700043.
S. Talukdar, Q. T. Nguyen, A. C. Chen, R. L. Sah, S. C. Kundu, Biomaterials 2011, 32, 8927.
R. L. Mauck, C. C. - B. Wang, E. S. Oswald, G. A. Ateshian, C. T. Hung, Osteoarthritis Cartilage 2003, 11, 879.
G. M. Williams, T. J. Klein, R. L. Sah, Acta Biomater. 2005, 1, 625.
A. Troken, N. Marion, S. Hollister, J. Mao, Proc. Inst. Mech. Eng., Part H 2007, 221, 429.
J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, A. Cardona, Nat. Methods 2012, 9, 676.
R. Narcisi, W. J. L. M. Koevoet, G. J. V. M. van Osch, in Osteoporosis and Osteoarthritis. Methods in Molecular Biology (Eds: A. J. van Wijnen, M. S. Ganshina), vol. 2221, Humana, New York, NY, 2021, pp. 15-28.