Flexible Allyl-Modified Gelatin Photoclick Resin Tailored for Volumetric Bioprinting of Matrices for Soft Tissue Engineering.

adipose-derived stromal cells allyl-modified gelatin photoclick resins soft hydrogels volumetric bioprinting

Journal

Advanced healthcare materials
ISSN: 2192-2659
Titre abrégé: Adv Healthc Mater
Pays: Germany
ID NLM: 101581613

Informations de publication

Date de publication:
12 2023
Historique:
revised: 11 08 2023
received: 27 03 2023
medline: 5 12 2023
pubmed: 12 9 2023
entrez: 12 9 2023
Statut: ppublish

Résumé

Volumetric bioprinting (VBP) is a light-based 3D printing platform, which recently prompted a paradigm shift for additive manufacturing (AM) techniques considering its capability to enable the fabrication of complex cell-laden geometries in tens of seconds with high spatiotemporal control and pattern accuracy. A flexible allyl-modified gelatin (gelAGE)-based photoclick resin is developed in this study to fabricate matrices with exceptionally soft polymer networks (0.2-1.0 kPa). The gelAGE-based resin formulations are designed to exploit the fast thiol-ene crosslinking in combination with a four-arm thiolated polyethylene glycol (PEG4SH) in the presence of a photoinitiator. The flexibility of the gelAGE biomaterial platform allows one to tailor its concentration spanning from 2.75% to 6% and to vary the allyl to thiol ratio without hampering the photocrosslinking efficiency. The thiol-ene crosslinking enables the production of viable cell-material constructs with a high throughput in tens of seconds. The suitability of the gelAGE-based resins is demonstrated by adipogenic differentiation of adipose-derived stromal cells (ASC) after VBP and by the printing of more fragile adipocytes as a proof-of-concept. Taken together, this study introduces a soft photoclick resin which paves the way for volumetric printing applications toward soft tissue engineering.

Identifiants

pubmed: 37699146
doi: 10.1002/adhm.202300977
doi:

Substances chimiques

Gelatin 9000-70-8
Hydrogels 0
Sulfhydryl Compounds 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2300977

Subventions

Organisme : Deutsche Forschungsgemeinschaft
ID : 326998133
Organisme : Horizon 2020
ID : 874827

Informations de copyright

© 2023 The Authors. Advanced Healthcare Materials published by Wiley-VCH GmbH.

Références

a) 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;
b) L. Moroni, T. Boland, J. A. Burdick, C. De Maria, B. Derby, G. Forgacs, J. Groll, Q. Li, J. Malda, V. A. Mironov, C. Mota, M. Nakamura, W. Shu, S. Takeuchi, T. B. F. Woodfield, T. Xu, J. J. Yoo, G. Vozzi, Trends Biotechnol. 2018, 36, 384;
c) L. Moroni, J. A. Burdick, C. Highley, S. J. Lee, Y. Morimoto, S. Takeuchi, J. J. Yoo, Nat. Rev. Mater. 2018, 3, 21.
M. Shusteff, A. E. M. Browar, B. E. Kelly, J. Henriksson, T. H. Weisgraber, R. M. Panas, N. X. Fang, C. M. Spadaccini, Sci. Adv. 2017, 3, eaao5496.
B. E. Kelly, I. Bhattacharya, H. Heidari, M. Shusteff, C. M. Spadaccini, H. K. Taylor, Science 2019, 363, 1075.
P. N. Bernal, P. Delrot, D. Loterie, Y. Li, J. Malda, C. Moser, R. Levato, Adv. Mater. 2019, 31, 1904209.
a) K. Yue, G. Trujillo-De Santiago, M. M. Alvarez, A. Tamayol, N. Annabi, A. Khademhosseini, Biomaterials 2015, 73, 254;
b) B. J. Klotz, D. Gawlitta, A. J. W. P. Rosenberg, J. Malda, F. P. W. Melchels, Trends Biotechnol. 2016, 34, 394.
a) Z. Munoz, H. Shih, C.-C. Lin, Biomater. Sci. 2014, 2, 1063;
b) M. J. Kade, D. J. Burke, C. J. Hawker, J. Polym. Sci., Part A: Polym. Chem. 2010, 48, 743;
c) C. E. Hoyle, A. B. Lowe, C. N. Bowman, Chem. Soc. Rev. 2010, 39, 1355;
d) J. J. Roberts, S. J. Bryant, Biomaterials 2013, 34, 9969;
e) O. Llorente, A. Agirre, I. Calvo, M. Olaso, R. Tomovska, H. Sardon, Polym. J. 2021, 53, 1195.
R. Rizzo, D. Ruetsche, H. Liu, M. Zenobi-Wong, Adv. Mater. 2021, 33, 2102900.
S. Bertlein, G. Brown, K. S. Lim, T. Jungst, T. Boeck, T. Blunk, J. Tessmar, G. J. Hooper, T. B. F. Woodfield, J. Groll, Adv. Mater. 2017, 29, 1703404.
B. G. Soliman, G. C. J. Lindberg, T. Jungst, G. J. Hooper, J. Groll, T. B. F. Woodfield, K. S. Lim, Adv. Healthcare Mater. 2020, 9, e1901544.
D. Loterie, P. Delrot, C. Moser, Nat. Commun. 2020, 11, 852.
a) G. S. Major, J. W. Simcock, T. B. F. Woodfield, K. S. Lim, Trends Biotechnol. 2022, 40, 77;
b) C. S. Murphy, L. Liaw, M. R. Reagan, BMC Biomed. Eng. 2019, 1, 27.
a) I. Henriksson, P. Gatenholm, D. A. Hägg, Biofabrication 2017, 9, 015022;
b) F. B. Albrecht, V. Dolderer, S. Nellinger, F. F. Schmidt, P. J. Kluger, Gels 2022, 8, 420.
H. Horder, M. Guaza Lasheras, N. Grummel, A. Nadernezhad, J. Herbig, S. Ergün, J. Teßmar, J. Groll, B. Fabry, P. Bauer-Kreisel, T. Blunk, Cells 2021, 10, 803.
N. Contessi Negrini, N. Celikkin, P. Tarsini, S. Farè, W. Swieszkowski, Biofabrication 2020, 12, 025001.
J. Colle, P. Blondeel, A. De Bruyne, S. Bochar, L. Tytgat, C. Vercruysse, S. Van Vlierberghe, P. Dubruel, H. Declercq, J. Mater. Sci. Mater. Med. 2020, 31, 36.
L. Tytgat, L. Van Damme, M. D. P. O. Arevalo, H. Declercq, H. Thienpont, H. Otteveare, P. Blondeel, P. Dubruel, S. Van Vlierberghe, Int. J. Biol. Macromol. 2019, 140, 929.
J. K. Placone, A. J. Engler, Adv. Healthcare Mater. 2018, 7, 1701161.
H. Genç, A. Cianciosi, R. Lohse, P. Stahlhut, J. Groll, C. Alexiou, I. Cicha, T. Jüngst, Biomacromolecules 2023, 24, 1497.
X. Li, S. Chen, J. Li, X. Wang, J. Zhang, N. Kawazoe, G. Chen, Polymers 2016, 8, 269.
T. R. Cox, J. T. Erler, Dis. Model. Mech. 2011, 4, 165.
a) T. Morita, Y. Horikiri, T. Suzuki, H. Yoshino, Int. J. Pharm. 2001, 219, 127;
b) H. Jizomoto, J. Pharm. Sci. 1984, 73, 879;
c) H. Jizomoto, J. Pharm. Sci. 1985, 74, 469;
d) T. Nezu, H. Maeda, Bull. Chem. Soc. Jpn. 1991, 64, 1618.
M. Yanagisawa, Y. Yamashita, S.-A. Mukai, M. Annaka, M. Tokita, J. Mol. Liq. 2014, 200, 2.
M. W. Tibbitt, K. S. Anseth, Biotechnol. Bioeng. 2009, 103, 655.
K. S. Lim, B. J. Klotz, G. C. J. Lindberg, F. P. W. Melchels, G. J. Hooper, J. Malda, D. Gawlitta, T. B. F. Woodfield, Macromol. Biosci. 2019, 19, e1900098.
B. G. Soliman, A. Longoni, M. Wang, W. Li, P. N. Bernal, A. Cianciosi, G. C. J. Lindberg, J. Malda, J. Groll, T. Jungst, R. Levato, J. Rnjak-Kovacina, T. B. F. Woodfield, Y. S. Zhang, K. S. Lim, Adv. Funct. Mater. 2023, 33, 2210521.
L. Bian, C. Hou, E. Tous, R. Rai, R. L. Mauck, J. A. Burdick, Biomaterials 2013, 34, 413.
S. Lee, X. Tong, F. Yang, Acta Biomater. 2014, 10, 4167.
X. Unamuno, J. Gómez-Ambrosi, S. Becerril, F. J. Álvarez-Cienfuegos, B. Ramírez, A. Rodríguez, S. Ezquerro, V. Valentí, R. Moncada, A. Mentxaka, M. Llorente, C. Silva, M. D. L. R. Elizalde, V. Catalán, G. Frühbeck, Acta Biomater. 2022, 141, 264.
K. Elkhoury, M. Morsink, Y. Tahri, C. Kahn, F. Cleymand, S. R. Shin, E. Arab-Tehrany, L. Sanchez-Gonzalez, L. Sanchez-Gonzalez, Int. J. Biol. Macromol. 2021, 183, 918.
R. Levato, W. R. Webb, I. A. Otto, A. Mensinga, Y. Zhang, M. Van Rijen, R. Van Weeren, I. M. Khan, J. Malda, Acta Biomater. 2017, 61, 41.
K. Comley, N. Fleck, Int. J. Impact Eng. 2012, 46, 1.
K. Comley, N. A. Fleck, Int. J. Solids Struct. 2010, 47, 2982.
P. N. Bernal, M. Bouwmeester, J. Madrid-Wolff, M. Falandt, S. Florczak, N. G. Rodriguez, Y. Li, G. Groessbacher, R.-A. Samsom, M. Van Wolferen, L. J. W. Van Der Laan, P. Delrot, D. Loterie, J. Malda, C. Moser, B. Spee, R. Levato, Adv. Mater. 2022, 34, 2110054.
M. Xie, L. Lian, X. Mu, Z. Luo, C. E. Garciamendez-Mijares, Z. Zhang, A. López, J. Manríquez, X. Kuang, J. Wu, J. K. Sahoo, F. Z. González, G. Li, G. Tang, S. Maharjan, J. Guo, D. L. Kaplan, Y. S. Zhang, Nat. Commun. 2023, 14, 210.
W. Borchard, B. Burg, in Proc. 1990 Progress in Colloid & Polymer Science, Steinkopff, Heidelberg 2007, p. 83.
A. Matsumoto, J. Chen, A. L. Collette, U.-J. Kim, G. H. Altman, P. Cebe, D. L. Kaplan, J. Phys. Chem. B 2006, 110, 21630.
A. I. Van Den Bulcke, B. Bogdanov, N. De Rooze, E. H. Schacht, M. Cornelissen, H. Berghmans, Biomacromolecules 2000, 1, 31.
a) C. Michon, G. Cuvelier, B. Launay, Rheol. Acta 1993, 32, 94;
b) S.-H. Hsu, A. M. Jamieson, Polymer 1993, 34, 2602.
a) J. Malda, J. Visser, F. P. Melchels, T. Jüngst, W. E. Hennink, W. J. A. Dhert, J. Groll, D. W. Hutmacher, Adv. Mater. 2013, 25, 5011;
b) R. Levato, T. Jungst, R. G. Scheuring, T. Blunk, J. Groll, J. Malda, Adv. Mater. 2020, 32, 1906423.
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.
Y. Chen, Y. Liu, J. Zhang, H. Liu, J. Wang, Q. Liu, Y. Zhang, Mater. Des. 2021, 200, 109467.
F. Louis, M. Piantino, H. Liu, D.-H. Kang, Y. Sowa, S. Kitano, M. Matsusaki, Cyborg Bionic Syst. 2021, 2021, 1412542.
a) L. Hyväri, M. Ojansivu, M. Juntunen, K. Kartasalo, S. Miettinen, S. Vanhatupa, Stem Cells Int. 2018, 2018, 2190657;
b) J.-J. Li, D. Xie, Biochem. Biophys. Res. Commun. 2007, 357, 648.
a) N. J. Hogrebe, J. W. Reinhardt, N. K. Tram, A. C. Debski, G. Agarwal, M. A. Reilly, K. J. Gooch, Acta Biomater. 2018, 70, 110;
b) J.-H. Hwang, M. R. Byun, A. R. Kim, K. M. Kim, H. J. Cho, Y. H. Lee, J. Kim, M. G. Jeong, E. S. Hwang, J.-H. Hong, PLoS One 2015, 10, e0135519;
c) D. A. Young, Y. S. Choi, A. J. Engler, K. L. Christman, Biomaterials 2013, 34, 8581.
D. Ribezzi, M. Gueye, S. Florczak, F. Dusi, D. De Vos, F. Manente, A. Hierholzer, M. Fussenegger, M. Caiazzo, T. Blunk, J. Malda, R. Levato, Adv. Mater. 2023, 35, 2301673.
a) Y. Li, A. S. Mao, B. R. Seo, X. Zhao, S. K. Gupta, M. Chen, Y. L. Han, T.-Y. Shih, D. J. Mooney, M. Guo, Sci. Adv. 2020, 6, eaax5611;
b) V. Pellegrinelli, J. Heuvingh, O. Du Roure, C. Rouault, A. Devulder, C. Klein, M. Lacasa, E. Clément, D. Lacasa, K. Clément, J. Pathol. 2014, 233, 183.
F. B. Albrecht, F. F. Schmidt, A.-C. Volz, P. J. Kluger, Gels 2022, 8, 611.
D. Contador, F. Ezquer, M. Espinosa, M. Arango-Rodriguez, C. Puebla, L. Sobrevia, P. Conget, Exp. Biol. Med. 2015, 240, 1235.
a) K. S. Lim, B. S. Schon, N. V. Mekhileri, G. C. J. Brown, C. M. Chia, S. Prabakar, G. J. Hooper, T. B. F. Woodfield, ACS Biomater. Sci. Eng. 2016, 2, 1752;
b) B. G. Soliman, G. S. Major, P. Atienza-Roca, C. A. Murphy, A. Longoni, C. R. Alcala-Orozco, J. Rnjak-Kovacina, D. Gawlitta, T. B. F. Woodfield, K. S. Lim, Adv. Healthcare Mater. 2022, 11, 2101873.
K. J. Livak, T. D. Schmittgen, Methods 2001, 25, 402.

Auteurs

Alessandro Cianciosi (A)

Department of Functional Materials in Medicine and Dentistry, Institute of Biofabrication and Functional Materials, University of Würzburg and KeyLab Polymers for Medicine of the Bavarian Polymer Institute (BPI), Pleicherwall 2, 97070, Würzburg, Germany.

Sabrina Stecher (S)

Department of Trauma, Hand, Plastic and Reconstructive Surgery, University Hospital Würzburg, 97080, Würzburg, Germany.

Maxi Löffler (M)

Department of Functional Materials in Medicine and Dentistry, Institute of Biofabrication and Functional Materials, University of Würzburg and KeyLab Polymers for Medicine of the Bavarian Polymer Institute (BPI), Pleicherwall 2, 97070, Würzburg, Germany.

Petra Bauer-Kreisel (P)

Department of Trauma, Hand, Plastic and Reconstructive Surgery, University Hospital Würzburg, 97080, Würzburg, Germany.

Khoon S Lim (KS)

School of Medical Sciences, University of Sydney, Sydney, 2006, Australia.

Tim B F Woodfield (TBF)

Department of Orthopaedic Surgery and Musculoskeletal Medicine, Centre for Bioengineering and Nanomedicine, University of Otago, Christchurch, 8011, New Zealand.

Jürgen Groll (J)

Department of Functional Materials in Medicine and Dentistry, Institute of Biofabrication and Functional Materials, University of Würzburg and KeyLab Polymers for Medicine of the Bavarian Polymer Institute (BPI), Pleicherwall 2, 97070, Würzburg, Germany.

Torsten Blunk (T)

Department of Trauma, Hand, Plastic and Reconstructive Surgery, University Hospital Würzburg, 97080, Würzburg, Germany.

Tomasz Jungst (T)

Department of Functional Materials in Medicine and Dentistry, Institute of Biofabrication and Functional Materials, University of Würzburg and KeyLab Polymers for Medicine of the Bavarian Polymer Institute (BPI), Pleicherwall 2, 97070, Würzburg, Germany.

Articles similaires

Organoids Humans Tissue Engineering Coculture Techniques Regenerative Medicine
Animals Osteogenesis Osteoporosis Mesenchymal Stem Cells Humans
Organoids Animals Kidney Mice Humans

Classifications MeSH