Tuning Superfast Curing Thiol-Norbornene-Functionalized Gelatin Hydrogels for 3D Bioprinting.

3D bioprinting bioinks cell encapsulation gelatin hydrogels thiol-ene chemistry 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:
07 2021
Historique:
revised: 08 04 2021
received: 31 01 2021
pubmed: 20 6 2021
medline: 6 8 2021
entrez: 19 6 2021
Statut: ppublish

Résumé

Photocurable gelatin-based hydrogels have established themselves as powerful bioinks in tissue engineering due to their excellent biocompatibility, biodegradability, light responsiveness, thermosensitivity and bioprinting properties. While gelatin methacryloyl (GelMA) has been the gold standard for many years, thiol-ene hydrogel systems based on norbornene-functionalized gelatin (GelNB) and a thiolated crosslinker have recently gained increasing importance. In this paper, a highly reproducible water-based synthesis of GelNB is presented, avoiding the use of dimethyl sulfoxide (DMSO) as organic solvent and covering a broad range of degrees of functionalization (DoF: 20% to 97%). Mixing with thiolated gelatin (GelS) results in the superfast curing photoclick hydrogel GelNB/GelS. Its superior properties over GelMA, such as substantially reduced amounts of photoinitiator (0.03% (w/v)), superfast curing (1-2 s), higher network homogeneity, post-polymerization functionalization ability, minimal cross-reactivity with cellular components, and improved biocompatibility of hydrogel precursors and degradation products lead to increased survival of primary cells in 3D bioprinting. Post-printing viability analysis revealed excellent survival rates of > 84% for GelNB/GelS bioinks of varying crosslinking density, while cell survival for GelMA bioinks is strongly dependent on the DoF. Hence, the semisynthetic and easily accessible GelNB/GelS hydrogel is a highly promising bioink for future medical applications and other light-based biofabrication techniques.

Identifiants

pubmed: 34145799
doi: 10.1002/adhm.202100206
doi:

Substances chimiques

Hydrogels 0
Norbornanes 0
Sulfhydryl Compounds 0
Gelatin 9000-70-8

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2100206

Informations de copyright

© 2021 The Authors. Advanced Healthcare Materials published by Wiley-VCH GmbH.

Références

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. M. Shu, S. Takeuchi, G. Vozzi, T. B. F. Woodfield, T. Xu, J. J. Yoo, J. Malda, Biofabrication 2016, 8, 013001
M. L. Bedell, A. M. Navara, Y. Y. Du, S. M. Zhang, A. G. Mikos, Chem. Rev. 2020, 120, 10744.
J. Malda, J. Visser, F. P. Melchels, T. Jungst, W. E. Hennink, W. J. Dhert, J. Groll, D. W. Hutmacher, Adv. Mater. 2013, 25, 5011.
A. Arslan-Yildiz, R. El Assal, P. Chen, S. Guven, F. Inci, U. Demirci, Biofabrication 2016, 8, 014103.
A. Panwar, L. P. Tan, Molecules 2016, 21, 685.
I. Donderwinkel, J. C. M. van Hest, N. R. Cameron, Polym. Chem. 2017, 8, 4451.
K. Holzl, S. M. Lin, L. Tytgat, S. Van Vlierberghe, L. X. Gu, A. Ovsianikov, Biofabrication 2016, 8, 032002
J. Groll, J. A. Burdick, D. W. Cho, B. Derby, M. Gelinsky, S. C. Heilshorn, T. Jungst, J. Malda, V. A. Mironov, K. Nakayama, A. Ovsianikov, W. Sun, S. Takeuchi, J. J. Yoo, T. B. F. Woodfield, Biofabrication 2018, 11, 013001.
J. M. Zhu, R. E. Marchant, Expert Rev. Med. Devices 2011, 8, 607.
M. Guvendiren, H. D. Lu, J. A. Burdick, Soft Matter 2012, 8, 260.
M. Hospodiuk, M. Dey, D. Sosnoski, I. T. Ozbolat, Biotechnol. Adv. 2017, 35, 217.
X.-H. Qin, A. Ovsianikov, J. Stampfl, R. Liska, BioNanomaterials 2014, 15, 49.
A. I. Van Den Bulcke, B. Bogdanov, N. De Rooze, E. H. Schacht, M. Cornelissen, H. Berghmans, Biomacromolecules 2000, 1, 31.
J. A. Benton, C. A. DeForest, V. Vivekanandan, K. S. Anseth, Tissue Eng. Part A 2009, 15, 3221.
K. Yue, G. Trujillo-de Santiago, M. M. Alvarez, A. Tamayol, N. Annabi, A. Khademhosseini, Biomaterials 2015, 73, 254.
J. W. Nichol, S. T. Koshy, H. Bae, C. M. Hwang, S. Yamanlar, A. Khademhosseini, Biomaterials 2010, 31, 5536.
W. T. Brinkman, K. Nagapudi, B. S. Thomas, E. L. Chaikof, Biomacromolecules 2003, 4, 890.
R. Ravichandran, M. M. Islam, E. I. Alarcon, A. Samanta, S. Wang, P. Lundstrom, J. Hilborn, M. Griffith, J. Phopase, J. Mater. Chem. B 2016, 4, 318.
I. D. Gaudet, D. I. Shreiber, Biointerphases 2012, 7, 7.
K. A. Smeds, A. Pfister-Serres, D. Miki, K. Dastgheib, M. Inoue, D. L. Hatchell, M. W. Grinstaff, J. Biomed. Mater. Res. 2001, 54, 115.
J. Baier Leach, K. A. Bivens, C. W. Patrick Jr., C. E. Schmidt, Biotechnol. Bioeng. 2003, 82, 578.
J. A. Burdick, C. Chung, X. Jia, M. A. Randolph, R. Langer, Biomacromolecules 2005, 6, 386.
K. S. Masters, D. N. Shah, L. A. Leinwand, K. S. Anseth, Biomaterials 2005, 26, 2517.
Z. Munoz, H. Shih, C. C. Lin, Biomater. Sci. 2014, 2, 1063.
M. W. Tibbitt, A. M. Kloxin, L. Sawicki, K. S. Anseth, Macromolecules 2013, 46, 2785.
R. Z. Lin, Y. C. Chen, R. Moreno-Luna, A. Khademhosseini, J. M. Melero-Martin, Biomaterials 2013, 34, 6785.
L. E. Bertassoni, J. C. Cardoso, V. Manoharan, A. L. Cristino, N. S. Bhise, W. A. Araujo, P. Zorlutuna, N. E. Vrana, A. M. Ghaemmaghami, M. R. Dokmeci, A. Khademhosseini, Biofabrication 2014, 6, 024105.
R. Masuma, S. Kashima, M. Kurasaki, T. Okuno, J. Photoch. Photobio. B 2013, 125, 202.
K. S. Lim, J. H. Galarraga, X. Cui, G. C. J. Lindberg, J. A. Burdick, T. B. F. Woodfield, Chem. Rev. 2020, 120, 10662.
S. Knowlton, B. Yenilmez, S. Anand, S. Tasoglu, Bioprinting 2017, 5, 10.
Y. Hong, F. Zhou, Y. Hua, X. Zhang, C. Ni, D. Pan, Y. Zhang, D. Jiang, L. Yang, Q. Lin, Y. Zou, D. Yu, D. E. Arnot, X. Zou, L. Zhu, S. Zhang, H. Ouyang, Nat. Commun. 2019, 10, 2060.
Y. Yang, J. Zhang, Z. Liu, Q. Lin, X. Liu, C. Bao, Y. Wang, L. Zhu, Adv. Mater. 2016, 28, 2724.
J. D. McCall, K. S. Anseth, Biomacromolecules 2012, 13, 2410.
N. B. Cramer, C. N. Bowman, J. Polym. Sci. Pol. Chem. 2001, 39, 3311.
C. C. Lin, C. S. Ki, H. Shih, J. Appl. Polym. Sci. 2015, 132, 41563.
R. F. Pereira, P. J. Bartolo, Engineering 2015, 1, 090.
C. E. Hoyle, C. N. Bowman, Angew. Chem. Int. Ed. 2010, 49, 1540.
T. Greene, C. C. Lin, ACS Biomater. Sci. Eng. 2015, 1, 1314.
J. Van Hoorick, P. Gruber, M. Markovic, M. Rollot, G. J. Graulus, M. Vagenende, M. Tromayer, J. Van Erps, H. Thienpont, J. C. Martins, S. Baudis, A. Ovsianikov, P. Dubruel, S. Van Vlierberghe, Macromol. Rapid Commun. 2018, 39, 1800181.
W. M. Gramlich, I. L. Kim, J. A. Burdick, Biomaterials 2013, 34, 9803.
G. F. Acosta-Velez, C. S. Linsley, M. C. Craig, B. M. Wu, Bioengineering (Basel) 2017, 4, 11.
A. A. Aimetti, A. J. Machen, K. S. Anseth, Biomaterials 2009, 30, 6048.
B. D. Fairbanks, M. P. Schwartz, A. E. Halevi, C. R. Nuttelman, C. N. Bowman, K. S. Anseth, Adv. Mater. 2009, 21, 5005.
H. Shih, C. C. Lin, Biomacromolecules 2012, 13, 2003.
A. Dobos, J. Van Hoorick, W. Steiger, P. Gruber, M. Markovic, O. G. Andriotis, A. Rohatschek, P. Dubruel, P. J. Thurner, S. Van Vlierberghe, S. Baudis, A. Ovsianikov, Adv. Healthcare Mater. 2020, 9, 1900752.
J. Van Hoorick, A. Dobos, M. Markovic, T. Gheysens, L. Van Damme, P. Gruber, L. Tytgat, J. Van Erps, H. Thienpont, P. Dubruel, A. Ovsianikov, S. Van Vlierberghe, Biofabrication 2021, 13, 1.
L. Tytgat, L. Van Damme, J. Van Hoorick, H. Declercq, H. Thienpont, H. Ottevaere, P. Blondeel, P. Dubruel, S. Van Vlierberghe, Acta Biomater. 2019, 94, 340.
D. Seliktar, Science 2012, 336, 1124.
G. D. Nicodemus, S. J. Bryant, Tissue Eng. Part B 2008, 14, 149.
W. Sun, B. Starly, A. C. Daly, J. A. Burdick, J. Groll, G. Skeldon, W. M. Shu, Y. Sakai, M. Shinohara, M. Nishikawa, J. Jang, D. W. Cho, M. H. Nie, S. Takeuchi, S. Ostrovidov, A. Khademhosseini, R. D. Kamm, V. Mironov, L. Moroni, I. T. Ozbolat, Biofabrication 2020, 12, 022002.
P. S. Gungor-Ozkerim, I. Inci, Y. S. Zhang, A. Khademhosseini, M. R. Dokmeci, Biomater. Sci. 2018, 6, 915.
M. C. Catoira, L. Fusaro, D. Di Francesco, M. Ramella, F. Boccafoschi, J. Mater. Sci. Mater. Med. 2019, 30, 115.
M. Alvarado-Velez, S. B. Pai, R. V. Bellamkonda, IEEE Trans. BioMed. Eng. 2014, 61, 1474.
H. Shirahama, B. H. Lee, L. P. Tan, N. J. Cho, Sci. Rep. 2016, 6, 31036.
J. Galvao, B. Davis, M. Tilley, E. Normando, M. R. Duchen, M. F. Cordeiro, FASEB J. 2014, 28, 1317.
X. Yi, M. Liu, Q. Luo, H. Zhuo, H. Cao, J. Wang, Y. Han, FEBS Open Bio 2017, 7, 485.
L. de Abreu Costa, M. Henrique Fernandes Ottoni, M. G. Dos Santos, A. B. Meireles, V. Gomes de Almeida, W. de Fatima Pereira, B. Alves de Avelar-Freitas, G. Eustaquio Alvim Brito-Melo, Molecules 2017, 22.
ThermoScientific, Crosslinking Technical Handbook, 2012. http://tools.thermofisher.com/content/sfs/brochures/1602163-Crosslinking-Reagents-Handbook.pdf
S. Van Vlierberghe, E. Schacht, P. Dubruel, Eur. Polym. J. 2011, 47, 1039.
T. B. Dorsey, A. Grath, A. Wang, C. Xu, Y. Hong, G. Dai, Bioact. Mater. 2018, 3, 64.
I. Pepelanova, K. Kruppa, T. Scheper, A. Lavrentieva, Bioengineering (Basel) 2018, 5, 55.
X. Li, S. Chen, J. Li, X. Wang, J. Zhang, N. Kawazoe, G. Chen, Polymers (Basel) 2016, 8, 269.
N. B. Cramer, T. Davies, A. K. O'Brien, C. N. Bowman, Macromolecules 2003, 36, 4631.
B. H. Northrop, R. N. Coffey, J. Am. Chem. Soc. 2012, 134, 13804.
C. M. Madl, S. C. Heilshorn, Adv. Funct. Mater. 2018, 28, 1706046.
M. A. Gauthier, M. I. Gibson, H. A. Klok, Angew. Chem. Int. Ed. Engl. 2009, 48, 48.
A. S. Goldmann, M. Glassner, A. J. Inglis, C. Barner-Kowollik, Macromol. Rapid Commun. 2013, 34, 810.
R. Stevens, L. Stevens, N. C. Price, Biochem. Educ. 1983, 11, 70.
R. Munday, Free Radic. Biol. Med. 1989, 7, 659.
K. D. Held, F. C. Sylvester, K. L. Hopcia, J. E. Biaglow, Radiat. Res. 1996, 145, 542.
E. Ruoslahti, Annu. Rev. Cell Dev. Biol. 1996, 12, 697.
F. Yang, C. G. Williams, D. A. Wang, H. Lee, P. N. Manson, J. Elisseeff, Biomaterials 2005, 26, 5991.
M. P. Lutolf, J. L. Lauer-Fields, H. G. Schmoekel, A. T. Metters, F. E. Weber, G. B. Fields, J. A. Hubbell, Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 5413.
M. P. Lutolf, G. P. Raeber, A. H. Zisch, N. Tirelli, J. A. Hubbell, Adv. Mater. 2003, 15, 888.
J. A. Benton, B. D. Fairbanks, K. S. Anseth, Biomaterials 2009, 30, 6593.
M. Larsen, V. V. Artym, J. A. Green, K. M. Yamada, Curr. Opin. Cell Biol. 2006, 18, 463.
S. T. Kelly, A. L. Zydney, Biotechnol. Bioeng. 1994, 44, 972.
R. Kale, A. Bajaj, J. Young Pharm. 2010, 2, 90.
ThermoScientific, User Guide: Ellman's Reagent, 2011. https://www.thermofisher.com/document-connect/document-connect.html?url=https%3A%2F%2Fassets.thermofisher.com%2FTFSAssets%2FLSG%2Fmanuals%2FMAN0011216_Ellmans_Reag_UG.pdf&title=VXNlciBHdWlkZTogIEVsbG1hbiZyc3F1bztzIFJlYWdlbnQ

Auteurs

Tobias Göckler (T)

Karlsruhe Institute of Technology (KIT), Institute of Functional Interfaces (IFG), Hermann-von-Helmholtz-Platz 1, Eggenstein-Leopoldshafen, 76344, Germany.

Sonja Haase (S)

Karlsruhe Institute of Technology (KIT), Institute of Functional Interfaces (IFG), Hermann-von-Helmholtz-Platz 1, Eggenstein-Leopoldshafen, 76344, Germany.

Xenia Kempter (X)

Karlsruhe Institute of Technology (KIT), Institute of Functional Interfaces (IFG), Hermann-von-Helmholtz-Platz 1, Eggenstein-Leopoldshafen, 76344, Germany.

Rebecca Pfister (R)

Karlsruhe Institute of Technology (KIT), Institute of Functional Interfaces (IFG), Hermann-von-Helmholtz-Platz 1, Eggenstein-Leopoldshafen, 76344, Germany.

Bruna R Maciel (BR)

Karlsruhe Institute of Technology (KIT), Institute of Mechanical Process Engineering and Mechanics (MVM), Gotthard-Franz-Straße 3, Karlsruhe, 76131, Germany.

Alisa Grimm (A)

Karlsruhe Institute of Technology (KIT), Institute of Functional Interfaces (IFG), Hermann-von-Helmholtz-Platz 1, Eggenstein-Leopoldshafen, 76344, Germany.

Tamara Molitor (T)

Karlsruhe Institute of Technology (KIT), Institute of Functional Interfaces (IFG), Hermann-von-Helmholtz-Platz 1, Eggenstein-Leopoldshafen, 76344, Germany.

Norbert Willenbacher (N)

Karlsruhe Institute of Technology (KIT), Institute of Mechanical Process Engineering and Mechanics (MVM), Gotthard-Franz-Straße 3, Karlsruhe, 76131, Germany.

Ute Schepers (U)

Karlsruhe Institute of Technology (KIT), Institute of Functional Interfaces (IFG), Hermann-von-Helmholtz-Platz 1, Eggenstein-Leopoldshafen, 76344, Germany.
Karlsruhe Institute of Technology (KIT), Institute of Organic Chemistry (IOC), Fritz-Haber-Weg 6, Karlsruhe, 76131, 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