Volumetric Printing Across Melt Electrowritten Scaffolds Fabricates Multi-Material Living Constructs with Tunable Architecture and Mechanics.


Journal

Advanced materials (Deerfield Beach, Fla.)
ISSN: 1521-4095
Titre abrégé: Adv Mater
Pays: Germany
ID NLM: 9885358

Informations de publication

Date de publication:
Aug 2023
Historique:
revised: 17 04 2023
received: 24 01 2023
medline: 14 8 2023
pubmed: 26 4 2023
entrez: 26 4 2023
Statut: ppublish

Résumé

Major challenges in biofabrication revolve around capturing the complex, hierarchical composition of native tissues. However, individual 3D printing techniques have limited capacity to produce composite biomaterials with multi-scale resolution. Volumetric bioprinting recently emerged as a paradigm-shift in biofabrication. This ultrafast, light-based technique sculpts cell-laden hydrogel bioresins into 3D structures in a layerless fashion, providing enhanced design freedom over conventional bioprinting. However, it yields prints with low mechanical stability, since soft, cell-friendly hydrogels are used. Herein, the possibility to converge volumetric bioprinting with melt electrowriting, which excels at patterning microfibers, is shown for the fabrication of tubular hydrogel-based composites with enhanced mechanical behavior. Despite including non-transparent melt electrowritten scaffolds in the volumetric printing process, high-resolution bioprinted structures are successfully achieved. Tensile, burst, and bending mechanical properties of printed tubes are tuned altering the electrowritten mesh design, resulting in complex, multi-material tubular constructs with customizable, anisotropic geometries that better mimic intricate biological tubular structures. As a proof-of-concept, engineered tubular structures are obtained by building trilayered cell-laden vessels, and features (valves, branches, fenestrations) that can be rapidly printed using this hybrid approach. This multi-technology convergence offers a new toolbox for manufacturing hierarchical and mechanically tunable multi-material living structures.

Identifiants

pubmed: 37099802
doi: 10.1002/adma.202300756
doi:

Substances chimiques

Biocompatible Materials 0
Hydrogels 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2300756

Subventions

Organisme : European Research Council
Pays : International

Informations de copyright

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

Références

R. Levato, T. Jungst, R. G. Scheuring, T. Blunk, J. Groll, J. Malda, Adv. Mater. 2020, 32, 1906423.
J. Groll, J. A. Burdick, D. W. Cho, B. Derby, M. Gelinsky, S. C. Heilshorn, T. Jüngst, J. Malda, V. A. Mironov, K. Nakayama, A. Ovsianikov, W. Sun, S. Takeuchi, J. J. Yoo, T. B. F. Woodfield, Biofabrication 2019, 11, 013001.
K. S. Lim, R. Levato, P. F. Costa, M. D. Castilho, C. R. Alcala-Orozco, K. M. A. Van Dorenmalen, F. P. W. Melchels, D. Gawlitta, G. J. Hooper, J. Malda, T. B. F. Woodfield, Biofabrication 2018, 10, 034101.
F. P. W. Melchels, J. Feijen, D. W. Grijpma, Biomaterials 2010, 31, 6121.
H. W. Kang, S. J. Lee, I. K. Ko, C. Kengla, J. J. Yoo, A. Atala, Nat. Biotechnol. 2016, 34, 312.
S. L. Ding, X. Liu, X. Y. Zhao, K. T. Wang, W. Xiong, Z. L. Gao, C. Y. Sun, M. X. Jia, C. Li, Q. Gu, M. Z. Zhang, Bioact. Mater. 2022, 17, 81.
N. V. Mekhileri, K. S. Lim, G. C. J. Brown, I. Mutreja, B. S. Schon, G. J. Hooper, T. B. F. Woodfield, Biofabrication 2018, 10, 024103.
A. C. Daly, D. J. Kelly, Biomaterials 2019, 197, 194.
M. Nakamura, A. Kobayashi, F. Takagi, A. Watanabe, Y. Hiruma, K. Ohuchi, Y. Iwasaki, M. Horie, I. Morita, S. Takatani, Tissue Eng. 2005, 11, 1658.
P. D. Dalton, Curr. Opin. Biomed. Eng. 2017, 2, 49.
T. M. Robinson, D. W. Hutmacher, P. D. Dalton, Adv. Funct. Mater. 2019, 29, 1904664.
M. Castilho, M. de Ruijter, S. Beirne, C. C. Villette, K. Ito, G. G. Wallace, J. Malda, Trends Biotechnol. 2020, 38, 1316.
M. Tavafoghi, M. A. Darabi, M. Mahmoodi, R. Tutar, C. Xu, A. Mirjafari, F. Billi, W. Swieszkowski, F. Nasrollahi, S. Ahadian, V. Hosseini, A. Khademhosseini, N. Ashammakhi, Biofabrication 2021, 13, 042002.
P. N. Bernal, P. Delrot, D. Loterie, Y. Li, J. Malda, C. Moser, R. Levato, Adv. Mater. 2019, 31, 1904209.
D. Loterie, P. Delrot, C. Moser, Nat. Commun. 2020, 11, 852.
T. Zandrini, S. Florczak, R. Levato, A. Ovsianikov, Trends Biotechnol. 2022, 41, 604.
J. Visser, F. P. W. Melchels, J. E. Jeon, E. M. Van Bussel, L. S. Kimpton, H. M. Byrne, W. J. A. Dhert, P. D. Dalton, D. W. Hutmacher, J. Malda, Nat. Commun. 2015, 6, 6933.
T. D. Brown, P. D. Dalton, D. W. Hutmacher, Prog. Polym. Sci. 2016, 56, 116.
N. Abbasi, A. Abdal-Hay, S. Hamlet, E. Graham, S. Ivanovski, ACS Biomater. Sci. Eng. 2019, 5, 3448.
M. Castilho, G. Hochleitner, W. Wilson, B. Van Rietbergen, P. D. Dalton, J. Groll, J. Malda, K. Ito, Sci. Rep. 2018, 8, 1245.
J. C. Kade, P. D. Dalton, Adv. Healthcare Mater. 2021, 10, 2001232.
R. Sanchez Diaz, J. R. Park, L. L. Rodrigues, P. D. Dalton, E. M. De-Juan-Pardo, T. R. Dargaville, Adv. Mater. Technol. 2021, 7, 2100508.
M. J. Ainsworth, O. Lotz, A. Gilmour, A. Zhang, M. J. Chen, D. R. McKenzie, M. M. M. Bilek, J. Malda, B. Akhavan, M. Castilho, Adv. Funct. Mater. 2022, 33, 2206583.
M. Castilho, R. Levato, P. N. Bernal, M. De Ruijter, C. Y. Sheng, J. Van Duijn, S. Piluso, K. Ito, J. Malda, Biomacromolecules 2021, 22, 855.
E. McColl, J. Groll, T. Jungst, P. D. Dalton, Mater. Des. 2018, 155, 46.
T. Jungst, M. L. Muerza-Cascante, T. D. Brown, M. Standfest, D. W. Hutmacher, J. Groll, P. D. Dalton, Polym. Int. 2015, 64, 1086.
T. D. Brown, A. Slotosch, L. Thibaudeau, A. Taubenberger, D. Loessner, C. Vaquette, P. D. Dalton, D. W. Hutmacher, Biointerphases 2012, 7, 13.
A. M. van Genderen, K. Jansen, M. Kristen, J. van Duijn, Y. Li, C. C. L. Schuurmans, J. Malda, T. Vermonden, J. Jansen, R. Masereeuw, M. Castilho, Front. Bioeng. Biotechnol. 2021, 8, 617364.
Z. Qiao, M. Lian, Y. Han, B. Sun, X. Zhang, W. Jiang, H. Li, Y. Hao, K. Dai, Biomaterials 2021, 266, 120385.
F. Afghah, N. B. Iyison, A. Nadernezhad, A. Midi, O. Sen, B. Saner Okan, M. Culha, B. Koc, Adv. Healthcare Mater. 2022, 11, 2102068.
T. Jungst, I. Pennings, M. Schmitz, A. J. W. P. Rosenberg, J. Groll, D. Gawlitta, Adv. Funct. Mater. 2019, 29, 1905987.
M. de Ruijter, A. Ribeiro, I. Dokter, M. Castilho, J. Malda, Adv. Healthcare Mater. 2019, 8, 1800418.
P. N. Bernal, M. Bouwmeester, J. Madrid-Wolff, M. Falandt, S. Florczak, N. G. Rodriguez, Y. Li, G. Größbacher, 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. Bartnikowski, T. R. Dargaville, S. Ivanovski, D. W. Hutmacher, Prog. Polym. Sci. 2019, 96, 1.
N. Golafshan, E. Vorndran, S. Zaharievski, H. Brommer, F. B. Kadumudi, A. Dolatshahi-Pirouz, U. Gbureck, R. van Weeren, M. Castilho, J. Malda, Biomaterials 2020, 261, 120302.
P. Diloksumpan, F. Abinzano, M. de Ruijter, A. Mensinga, S. Plomp, I. Khan, H. Brommer, I. Smit, M. Dias Castilho, P. R. van Weeren, J. Malda, R. Levato, J. Trial Error 2021, 2, 7.
A. Daghrery, J. A. Ferreira, J. Xu, N. Golafshan, D. Kaigler, S. B. Bhaduri, J. Malda, M. Castilho, M. C. Bottino, Bioact. Mater. 2023, 19, 268.
B. E. Kelly, I. Bhattacharya, H. Heidari, M. Shusteff, C. M. Spadaccini, H. K. Taylor, Science 2019, 363, 1075.
R. Rizzo, D. Ruetsche, H. Liu, M. Zenobi-Wong, Adv. Mater. 2021, 33, 2102900.
J. Gehlen, W. Qiu, G. N. Schädli, R. Müller, X. H. Qin, Acta Biomater. 2022, 156, 49.
M. Castilho, A. van Mil, M. Maher, C. H. G. Metz, G. Hochleitner, J. Groll, P. A. Doevendans, K. Ito, J. P. G. Sluijter, J. Malda, Adv. Funct. Mater. 2018, 28, 1803151.
D. B. Camasão, D. Mantovani, Mater Today Bio 2021, 10, 100106.
J. Schöneberg, F. De Lorenzi, B. Theek, A. Blaeser, D. Rommel, A. J. C. Kuehne, F. Kießling, H. Fischer, Sci. Rep. 2018, 8, 10430.
P. Zilla, D. Bezuidenhout, P. Human, Biomaterials 2007, 28, 5009.
M. Stekelenburg, M. C. M. Rutten, L. H. E. H. Snoeckx, F. P. T. Baaijens, Tissue Eng., Part A 2009, 15, 1081.
X. Li, H. Zhao, J. Biomater. Appl. 2019, 33, 1017.
C. M. Brennan, K. F. Eichholz, D. A. Hoey, Biomed. Mater. 2019, 14, 065016.
A. B. McCosker, M. E. Snowdon, R. Lamont, M. A. Woodruff, N. C. Paxton, Adv. Mater. Technol. 2022, 7, 2200259.
E. Pickering, N. C. Paxton, A. Bo, B. O'Connell, M. King, M. A. Woodruff, Adv. Eng. Mater. 2022, 24, 2200479.
V. Kasjanovs, I. Ozolanta, B. Purina, Mech. Compos. Mater. 1999, 35, 155.
T. D. Brown, P. D. Dalton, D. W. Hutmacher, Adv. Mater. 2011, 23, 5651.
G. Hochleitner, T. Jüngst, T. D. Brown, K. Hahn, C. Moseke, F. Jakob, P. D. Dalton, J. Groll, Biofabrication 2015, 7, 035002.
N. Pien, M. Bartolf-Kopp, L. Parmentier, J. Delaey, L. De Vos, D. Mantovani, S. Van Vlierberghe, P. Dubruel, T. Jungst, Macromol. Mater. Eng. 2022, 307, 2200097.
N. Diban, S. Haimi, L. Bolhuis-Versteeg, S. Teixeira, S. Miettinen, A. Poot, D. Grijpma, D. Stamatialis, Acta Biomater. 2013, 9, 6450.
V. Thomas, X. Zhang, Y. K. Vohra, Biotechnol. Bioeng. 2009, 104, 1025.
K. W. M. Boere, J. Visser, H. Seyednejad, S. Rahimian, D. Gawlitta, M. J. Van Steenbergen, W. J. A. Dhert, W. E. Hennink, T. Vermonden, J. Malda, Acta Biomater. 2014, 10, 2602.
A. Ribeiro, M. M. Blokzijl, R. Levato, C. W. Visser, M. Castilho, W. E. Hennink, T. Vermonden, J. Malda, Biofabrication 2018, 10, 014102.
C. Xie, Q. Gao, P. Wang, L. Shao, H. Yuan, J. Fu, W. Chen, Y. He, Mater. Des. 2019, 181, 108092.
W. G. Roberts, G. E. Palade, Cancer Res. 1997, 57, 765.
S. C. Satchell, F. Braet, Am. J. Physiol. Renal. Physiol. 2009, 296, F947.
J. Bernier-Latmani, C. Mauri, R. Marcone, F. Renevey, S. Durot, L. He, M. Vanlandewijck, C. Maclachlan, S. Davanture, N. Zamboni, G. W. Knott, S. A. Luther, C. Betsholtz, M. Delorenzi, C. Brisken, T. V. Petrova, Nat. Commun. 2022, 13, 3983.
G. Grevers, U. Herrmann, Arch Otorhinolaryngol 1987, 244, 55.
S. Parab, R. E. Quick, R. L. Matsuoka, Elife 2021, 10, e64295.
F. Benz, S. Liebner, Physiology, Pharmacology and Pathology of the Blood-Brain Barrier, (Eds.: Z. Cader, W. Neuhaus), Springer Nature, Cham, Switzerland 2020, pp. 3-31.
M. Kaya, L. Chang, A. Truong, M. W. Brightman, Exp. Neurol. 1996, 142, 6.
P. A. Stewart, K. Hayakawa, E. Hayakawa, C. L. Farrell, R. F. Del Maestro, Acta Neuropathol. 1985, 67, 96.
T. F. Browne, D. Hartley, S. Purchas, M. Rosenberg, G. Van Schie, M. Lawrence-Brown, Eur. J. Vasc. Endovasc. Surg. 1999, 18, 445.
P. M. Bungay, N. Burfitt, K. Sritharan, L. Muir, S. L. Khan, M. C. De Nunzio, K. Lingam, A. H. Davies, J. Vasc. Surg. 2011, 54, 1832.
B. M. Stanley, J. B. Semmens, M. Lawrence-Brown, M. A. Goodman, D. E. Hartley, J. Endovasc. Ther. 2001, 8, 16.
W. J. Kim, G. H. Kim, Theranostics 2020, 10, 2495.
M. Gallois, T. Gidenne, L. Fortun-Lamothe, I. L. Huerou-Luron, J. P. Lallès, Reprod., Nutr., Dev. 2005, 45, 109.
R. Abbasi, T. B. Lefevre, A. D. Benjamin, I. J. Thornton, J. N. Wilking, Lab Chip 2021, 21, 2050.
T. Wang, Z. Xu, W. Jiang, A. Ma, Int. J. Cardiol. 2006, 109, 74.
K. Kurpinski, H. Lam, J. Chu, A. Wang, A. Kim, E. Tsay, S. Agrawal, D. V. Schaffer, S. Li, Stem Cells 2010, 28, 734.
A. Augello, C. De Bari, Hum. Gene Ther. 2010, 21, 1226.
D. B. Kolesky, K. A. Homan, M. A. Skylar-Scott, J. A. Lewis, Proc. Natl. Acad. Sci. USA 2016, 113, 3179.
L. Ouyang, J. P. K. Armstrong, Q. Chen, Y. Lin, M. M. Stevens, Adv. Funct. Mater. 2020, 30, 1908349.
L. Shao, Q. Gao, C. Xie, J. Fu, M. Xiang, Y. He, Biofabrication 2020, 12, 035014.
C. Dikyol, M. Altunbek, B. Koc, J. Mater. Res. 2021, 36, 3851.
M. A. Skylar-Scott, S. G. M. Uzel, L. L. Nam, J. H. Ahrens, R. L. Truby, S. Damaraju, J. A. Lewis, Sci. Adv. 2019, 5, eaaw2459.
R. Levato, K. S. Lim, W. Li, A. U. Asua, L. B. Peña, M. Wang, M. Falandt, P. N. Bernal, D. Gawlitta, Y. S. Zhang, T. B. F. Woodfield, J. Malda, Mater Today Bio 2021, 12, 100162.
W. Zhu, X. Qu, J. Zhu, X. Ma, S. Patel, J. Liu, P. Wang, C. S. E. Lai, M. Gou, Y. Xu, K. Zhang, S. Chen, Biomaterials 2017, 124, 106.
B. Grigoryan, S. J. Paulsen, D. C. Corbett, D. W. Sazer, C. L. Fortin, A. J. Zaita, P. T. Greenfield, N. J. Calafat, J. P. Gounley, A. H. Ta, F. Johansson, A. Randles, J. E. Rosenkrantz, J. D. Louis-Rosenberg, P. A. Galie, K. R. Stevens, J. S. Miller, Science 2019, 364, 458.
D. Petta, V. Basoli, D. Pellicciotta, R. Tognato, J. Barcik, C. Arrigoni, E. D. Bella, A. R. Armiento, C. Candrian, R. G. Richards, M. Alini, M. Moretti, D. Eglin, T. Serra, Biofabrication 2020, 13, 015004.
B. Kang, J. Shin, H. J. Park, C. Rhyou, D. Kang, S. J. Lee, Y. S. Yoon, S. W. Cho, H. Lee, Nat. Commun. 2018, 9, 5402.
L. de Silva, P. N. Bernal, A. J. W. Rosenberg, J. Malda, R. Levato, D. Gawlitta, Acta Biomater. 2022, 156, 250.
M. Castilho, D. Feyen, M. Flandes-Iparraguirre, G. Hochleitner, J. Groll, P. A. F. Doevendans, T. Vermonden, K. Ito, J. P. G. Sluijter, J. Malda, Adv. Healthcare Mater. 2017, 6, 1700311.
G. Cedillo-Servin, O. Dahri, J. Meneses, J. van Duijn, F. Sage, J. Silva, A. Pereira, F. D. Magalhães, J. Malda, N. Geijsen, M. Castilho, bioRxiv 2017, https://doi.org/10.1101/2023.01.19.524679.
K. S. Lim, F. Abinzano, P. N. Bernal, A. Albillos Sanchez, P. Atienza-Roca, I. A. Otto, Q. C. Peiffer, M. Matsusaki, T. B. F. Woodfield, J. Malda, R. Levato, Adv. Healthcare Mater. 2020, 9, 1901792.
M. L. Terpstra, J. Li, A. Mensinga, M. De Ruijter, M. H. P. Van Rijen, C. Androulidakis, C. Galiotis, I. Papantoniou, M. Matsusaki, J. Malda, R. Levato, Biofabrication 2022, 14, 034104.

Auteurs

Gabriel Größbacher (G)

Department of Orthopaedics, University Medical Center Utrecht, Utrecht University, Utrecht, 3584 CX, The Netherlands.

Michael Bartolf-Kopp (M)

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

Csaba Gergely (C)

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

Paulina Núñez Bernal (PN)

Department of Orthopaedics, University Medical Center Utrecht, Utrecht University, Utrecht, 3584 CX, The Netherlands.

Sammy Florczak (S)

Department of Orthopaedics, University Medical Center Utrecht, Utrecht University, Utrecht, 3584 CX, The Netherlands.

Mylène de Ruijter (M)

Department of Orthopaedics, University Medical Center Utrecht, Utrecht University, Utrecht, 3584 CX, The Netherlands.

Núria Ginés Rodriguez (NG)

Department of Orthopaedics, University Medical Center Utrecht, Utrecht University, Utrecht, 3584 CX, The Netherlands.

Jürgen Groll (J)

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

Jos Malda (J)

Department of Orthopaedics, University Medical Center Utrecht, Utrecht University, Utrecht, 3584 CX, The Netherlands.
Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, Utrecht, 3584 CT, The Netherlands.

Tomasz Jungst (T)

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

Riccardo Levato (R)

Department of Orthopaedics, University Medical Center Utrecht, Utrecht University, Utrecht, 3584 CX, The Netherlands.
Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, Utrecht, 3584 CT, The Netherlands.

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