pH and Thrombin Concentration Are Decisive in Synthesizing Stiff, Stable, and Open-Porous Fibrin-Collagen Hydrogel Blends without Chemical Cross-Linker.
cross-linking mechanisms
hydrogels
interpenetrating networks
microstructures
Journal
Advanced healthcare materials
ISSN: 2192-2659
Titre abrégé: Adv Healthc Mater
Pays: Germany
ID NLM: 101581613
Informations de publication
Date de publication:
04 2023
04 2023
Historique:
received:
19
12
2022
medline:
18
4
2023
pubmed:
23
12
2022
entrez:
22
12
2022
Statut:
ppublish
Résumé
Fibrin-collagen hydrogel blends exhibit high potential for tissue engineering applications. However, it is still unclear whether the underlying cross-linking mechanisms are of chemical or physical nature. It is here hypothesized that chemical cross-linkers play a negligible role and that instead pH and thrombin concentration are decisive for synthetizing blends with high stiffness and hydrolytic stability. Different fibrin-collagen formulations (pure and with additional transglutaminase) are used and the blends' compaction rate, hydrolytic stability, compressive strength, and hydrogel microstructure are investigated. The effect of thrombin concentration on gel compaction is examined and the importance of pH control during synthesis observed. It is revealed that transglutaminase impairs gel stability and it is deduced that fibrin-collagen blends mainly cross-link by mechanical interactions due to physical fibril entanglement as opposed to covalent bonds from chemical cross-linking. High thrombin concentrations and basic pH during synthesis reduce gel compaction and enhance stiffness and long-term stability. Scanning electron microscopy reveals a highly interpenetrating fibrous network with unique, interconnected open-porous microstructures. Endothelial cells proliferate on the blends and form a confluent monolayer. This study reveals the underlying cross-linking mechanisms and presents enhanced fibrin-collagen blends with high stiffness, hydrolytic stability, and large, interconnected pores; findings that offer high potential for advanced tissue engineering applications.
Identifiants
pubmed: 36546310
doi: 10.1002/adhm.202203302
doi:
Substances chimiques
Thrombin
EC 3.4.21.5
Fibrin
9001-31-4
Biocompatible Materials
0
Collagen
9007-34-5
Hydrogels
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2203302Informations de copyright
© 2023 The Authors. Advanced Healthcare Materials published by Wiley-VCH GmbH.
Références
M. Tenje, F. Cantoni, A. M. P. Hernández, S. S. Searle, S. Johansson, L. Barbe, M. Antfolk, H. Pohlit, Organs-on-a-Chip 2020, 2, 100003.
A. D. Doyle, N. Carvajal, A. Jin, K. Matsumoto, K. M. Yamada, Nat. Commun. 2015, 6, 8720.
K. Bott, Z. Upton, K. Schrobback, M. Ehrbar, J. A. Hubbell, M. P. Lutolf, S. C. Rizzi, Biomaterials 2010, 31, 8454.
R. DeVolder, H.-J. Kong, Wiley Interdiscip. Rev.: Syst. Biol. Med. 2012, 4, 351.
G. Charras, E. Sahai, Nat. Rev. Mol. Cell Biol. 2014, 15, 813.
T. G. Vladkova, Int. J. Polym. Sci. 2010, 2010, 1.
A. Leal-Egaña, A. Díaz-Cuenca, A. R. Boccaccini, Adv. Mater. 2013, 25, 4049.
M. Guvendiren, J. A. Burdick, Nat. Commun. 2012, 3, 792.
X. Tong, F. Yang, Biomaterials 2014, 35, 1807.
J. Yang, Y. Li, Y. Liu, D. Li, L. Zhang, Q. Wang, Y. Xiao, X. Zhang, Acta Biomater. 2019, 91, 159.
Y. Liu, S. Rayatpisheh, S. Y. Chew, M. B. Chan-Park, ACS Appl. Mater. Interfaces 2012, 4, 1378.
S. R. Caliari, J. A. Burdick, Nat. Methods 2016, 13, 405.
F. Akther, P. Little, Z. Li, N.-T. Nguyen, H. T. Ta, RSC Adv. 2020, 10, 43682.
H. Liu, Y. Wang, K. Cui, Y. Guo, X. Zhang, J. Qin, Adv. Mater. 2019, 31, 1902042.
V. Dhote, S. Skaalure, U. Akalp, J. Roberts, S. J. Bryant, F. J. Vernerey, J. Mech. Behav. Biomed. Mater. 2013, 19, 61.
G. D. Nicodemus, S. J. Bryant, Tissue Eng., Part B 2008, 14, 149.
J. Wedgwood, A. J. Freemont, N. Tirelli, Macromol. Symp. 2013, 334, 117.
A. C. Brown, T. H. Barker, Acta Biomater. 2014, 10, 1502.
T. A. E. Ahmed, E. V. Dare, M. Hincke, Tissue Eng., Part B 2008, 14, 199.
S. H. Bhang, O. Jeon, C. Y. Choi, Y. H. K. Kwon, B.-S. Kim, J. Biomed. Mater. Res. 2007, 80, 998.
B. Bujoli, J.-C. Scimeca, E. Verron, Pharmaceutics 2019, 11, 556.
Y. Li, H. Meng, Y. Liu, B. P. Lee, Sci. World J. 2015, 2015, 685690.
R. A. Shirwaiker, M. F. Purser, R. A. Wysk, in Rapid Prototyping of Biomaterials, Elsevier, New York 2014, p. 176.
Y. Morimoto, M. Kiyosawa, S. Takeuchi, Sens. Actuators, B 2018, 274, 491.
S. Ricard-Blum, Cold Spring Harbor Perspect. Biol. 2011, 3, a004978.
G.-Z. Jin, H.-W. Kim, Tissue Eng. Regener. Med. 2017, 14, 383.
L. Debbi, B. Zohar, M. Shuhmaher, Y. Shandalov, I. Goldfracht, S. Levenberg, Biomaterials 2022, 280, 121286.
J. Xie, M. Bao, S. M. C. Bruekers, W. T. S. Huck, ACS Appl. Mater. Interfaces 2017, 9, 19630.
V. Nele, J. P. Wojciechowski, J. P. K. Armstrong, M. M. Stevens, Adv. Funct. Mater. 2020, 30, 2002759.
C. M. Brougham, T. J. Levingstone, S. Jockenhoevel, T. C. Flanagan, F. J. O'Brien, Acta Biomater. 2015, 26, 205.
S. L. Rowe, S. Lee, J. P. Stegemann, Acta Biomater. 2007, 3, 59.
J. Schöneberg, F. de Lorenzi, B. Theek, A. Blaeser, D. Rommel, A. J. C. Kuehne, F. Kießling, H. Fischer, Sci. Rep. 2018, 8, 10430.
C. M. A. P. Schuh, A. G. E. Day, H. Redl, J. Phillips, Tissue Eng., Part A 2018, 24, 1332.
M. Gomez-Florit, A. Pardo, R. M. A. Domingues, A. L. Graça, P. S. Babo, R. L. Reis, M. E. Gomes, Molecules 2020, 25, 5858.
V. K. Lai, S. P. Lake, C. R. Frey, R. T. Tranquillo, V. H. Barocas, J. Biomech. Eng. 2012, 134, 11004.
F. Duckert, D. Nyman, Suppl. Thromb. Haemostasis 1978, 63, 391.
A. Stemberger, F. Jilek, H. Hörmann, G. Blümel, in VIth Int. Congress on Thrombosis and Haemostasis, Schattauer GmbH, Stuttgart 1977.
D. F. Mosher, P. E. Schad, J. Clin. Invest. 1979, 64, 781.
E. Lai, B. Bao, Y. Zhu, H. Lin, Front. Bioeng. Biotechnol. 2022, 10, 824747.
K. Yokoyama, N. Nio, Y. Kikuchi, Appl. Microbiol. Biotechnol. 2004, 64, 447.
M. Kieliszek, A. Misiewicz, Folia Microbiol. 2014, 59, 241.
N. J. Kaiser, R. J. Kant, A. J. Minor, K. L. K. Coulombe, ACS Biomater. Sci. Eng. 2019, 5, 887.
A. Collen, R. Hanemaaijer, F. Lupu, P. H. A. Quax, N. van Lent, J. Grimbergen, E. Peters, P. Koolwijk, V. W. M. van Hinsbergh, Blood 2003, 101, 1810.
S. L. Rowe, J. P. Stegemann, Biomacromolecules 2006, 7, 2942.
D. K. Jarrell, E. J. Vanderslice, M. L. Lennon, A. C. Lyons, M. C. VeDepo, J. G. Jacot, PLoS One 2021, 16, e0239242.
Y. Takegawa, T. Takao, H. Sakaguchi, T. Nakai, K. Takeo, Y. Morita, T. Toyonaga, Y. Kodama, Sci. Rep. 2022, 12, 6986.
P. A. Janmey, J. P. Winer, J. W. Weisel, J. R. Soc. Interface 2009, 6, 1.
D. B. Kolesky, K. A. Homan, M. A. Skylar-Scott, J. A. Lewis, Proc. Natl. Acad. Sci. USA 2016, 113, 3179.
M. Wachendörfer, P. Schräder, E. M. Buhl, A. L. Palkowitz, G. B. Messaoud, W. Richtering, H. Fischer, Biomater. Sci. 2022, 10, 5552.
S. Zippusch, F. Helms, S. Lau, M. Klingenberg, C. Schrimpf, A. Haverich, M. Wilhelmi, U. Böer, Int. J. Artif. Organs 2021, 44, 130.
E. Potier, J. Noailly, C. M. Sprecher, K. Ito, J. Mater. Sci. 2010, 45, 2494.
A. Koroleva, A. Deiwick, A. Nguyen, R. Narayan, A. Shpichka, O. Kufelt, R. Kiyan, V. Bagratashvili, P. Timashev, T. Scheper, B. Chichkov, BioNanomaterials 2016, 17, 19.
N. Laurens, P. Koolwijk, M. P. M. de Maat, J. Thromb. Haemostasis 2006, 4, 932.
I. Catelas, N. Sese, B. M. Wu, J. C. Y. Dunn, S. Helgerson, B. Tawil, Tissue Eng. 2006, 12, 2385.
W. Ho, B. Tawil, J. C. Y. Dunn, B. M. Wu, Tissue Eng. 2006, 12, 1587.
H. Jiang, M. Zheng, X. Liu, S. Zhang, X. Wang, Y. Chen, M. Hou, J. Zhu, ACS Omega 2019, 4, 12606.
D. Y. S. Chau, R. J. Collighan, E. A. M. Verderio, V. L. Addy, M. Griffin, Biomaterials 2005, 26, 6518.
M. Torsten, L. Aaron, Front. Pediatr. 2018, 6, 389.
T. Q. Bui, V. D. Cao, N. B. D. Do, T. E. Christoffersen, W. Wang, A.-L. Kjøniksen, ACS Appl. Mater. Interfaces 2018, 10, 22218.
X. Zhao, S. A. Irvine, A. Agrawal, Y. Cao, P. Q. Lim, S. Y. Tan, S. S. Venkatraman, Acta Biomater. 2015, 26, 159.
S. Eliyahu, A. Galitsky, E. Ritov, H. Bianco-Peled, Polymers 2021, 13, 266.
K. M. Lorentz, S. Kontos, P. Frey, J. A. Hubbell, Biomaterials 2011, 32, 430.
X. Zuo, H. Zhang, T. Zhou, Y. Duan, H. Shou, S. Yu, C. Gao, Research 2020, 2020, 8970480.
N. A. Kurniawan, T. H. S. van Kempen, S. Sonneveld, T. T. Rosalina, B. E. Vos, K. A. Jansen, G. W. M. Peters, F. N. van de Vosse, G. H. Koenderink, Langmuir 2017, 33, 6342.
M. Okude, A. Yamanaka, S. Akihama, Biol. Pharm. Bull. 1995, 18, 203.
D. Eyrich, F. Brandl, B. Appel, H. Wiese, G. Maier, M. Wenzel, R. Staudenmaier, A. Goepferich, T. Blunk, Biomaterials 2007, 28, 55.
A. Karimizade, S. Takallu, E. Mirzaei, Nanomed. J. 2018, 5, 180.
J. Rosenblatt, B. Devereux, D. G. Wallace, Biomaterials 1994, 15, 985.
E. E. Antoine, P. P. Vlachos, M. N. Rylander, Tissue Eng., Part B 2014, 20, 683.
L. Shi, H. Tian, Y. Wang, G. Hao, J. Chen, W. Weng, J. Sci. Food Agric. 2020, 100, 4801.
H. Liu, M. Wu, Y. Jia, L. Niu, G. Huang, F. Xu, NPG Asia Mater 2020, 12, 45.
T. T. Tower, M. R. Neidert, R. T. Tranquillo, Ann. Biomed. Eng. 2002, 30, 1221.
M. T. J. J. M. Punter, B. E. Vos, B. M. Mulder, G. H. Koenderink, Soft Matter 2020, 16, 1298.
MacKintosh, Käs, Janmey, Phys. Rev. Lett. 1995, 75, 4425.
J. Raeburn, A. Z. Cardoso, D. J. Adams, Chem. Soc. Rev. 2013, 42, 5143.
G. B. Messaoud, P. L. Griel, D. Hermida-Merino, S. L. K. W. Roelants, W. Soetaert, C. V. Stevens, N. Baccile, Chem. Mater. 2019, 31, 4817.
L. H. Sperling, Interpenetrating Polymer Networks and Related Materials, Springer International Publishing, Cham 1981.
A. Krüger-Genge, S. Hauser, A. T. Neffe, Y. Liu, A. Lendlein, J. Pietzsch, F. Jung, ACS Biomater. Sci. Eng. 2021, 7, 527.
D. Lam, H. A. Enright, S. K. G. Peters, M. L. Moya, D. A. Soscia, J. Cadena, J. A. Alvarado, K. S. Kulp, E. K. Wheeler, N. O. Fischer, J. Neurosci. Methods 2020, 329, 108460.
R. Picetti, H. Shakur-Still, R. L. Medcalf, J. F. Standing, I. Roberts, Blood Coagulation Fibrinolysis 2019, 30, 1.
S. Jockenhoevel, T. C. Flanagan, in Tissue Engineering for Tissue and Organ Regeneration (Ed: D. Eberli), InTech, London 2011.
B. Sarker, R. Singh, R. Silva, J. A. Roether, J. Kaschta, R. Detsch, D. W. Schubert, I. Cicha, A. R. Boccaccini, PLoS One 2014, 9, e107952.
K. A. Ahmann, J. S. Weinbaum, S. L. Johnson, R. T. Tranquillo, Tissue Eng., Part A 2010, 16, 3261.
B. Trappmann, B. M. Baker, W. J. Polacheck, C. K. Choi, J. A. Burdick, C. S. Chen, Nat. Commun. 2017, 8, 371.
L. T. Vu, G. Jain, B. D. Veres, P. Rajagopalan, Tissue Eng., Part B 2015, 21, 67.
X. Li, Y. Dai, T. Shen, C. Gao, Regener. Biomater. 2017, 4, 139.
A. Bertz, S. Wöhl-Bruhn, S. Miethe, B. Tiersch, J. Koetz, M. Hust, H. Bunjes, H. Menzel, J. Biotechnol. 2013, 163, 243.
H. Muri, L. Hoang, D. Hjelme, Appl. Sci. 2018, 8, 2446.
K. Stuart, A. Panitch, Biopolymers 2008, 89, 841.