Shaping Synthetic Multicellular and Complex Multimaterial Tissues via Embedded Extrusion-Volumetric Printing of Microgels.
FRESH printing
biofabrication
optogenetics
synthetic biology
volumetric bioprinting
Journal
Advanced materials (Deerfield Beach, Fla.)
ISSN: 1521-4095
Titre abrégé: Adv Mater
Pays: Germany
ID NLM: 9885358
Informations de publication
Date de publication:
Sep 2023
Sep 2023
Historique:
revised:
24
05
2023
received:
21
02
2023
medline:
8
9
2023
pubmed:
3
6
2023
entrez:
3
6
2023
Statut:
ppublish
Résumé
In living tissues, cells express their functions following complex signals from their surrounding microenvironment. Capturing both hierarchical architectures at the micro- and macroscale, and anisotropic cell patterning remains a major challenge in bioprinting, and a bottleneck toward creating physiologically-relevant models. Addressing this limitation, a novel technique is introduced, termed Embedded Extrusion-Volumetric Printing (EmVP), converging extrusion-bioprinting and layer-less, ultra-fast volumetric bioprinting, allowing spatially pattern multiple inks/cell types. Light-responsive microgels are developed for the first time as bioresins (µResins) for light-based volumetric bioprinting, providing a microporous environment permissive for cell homing and self-organization. Tuning the mechanical and optical properties of gelatin-based microparticles enables their use as support bath for suspended extrusion printing, in which features containing high cell densities can be easily introduced. µResins can be sculpted within seconds with tomographic light projections into centimeter-scale, granular hydrogel-based, convoluted constructs. Interstitial microvoids enhanced differentiation of multiple stem/progenitor cells (vascular, mesenchymal, neural), otherwise not possible with conventional bulk hydrogels. As proof-of-concept, EmVP is applied to create complex synthetic biology-inspired intercellular communication models, where adipocyte differentiation is regulated by optogenetic-engineered pancreatic cells. Overall, EmVP offers new avenues for producing regenerative grafts with biological functionality, and for developing engineered living systems and (metabolic) disease models.
Identifiants
pubmed: 37269532
doi: 10.1002/adma.202301673
doi:
Substances chimiques
Microgels
0
Hydrogels
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2301673Subventions
Organisme : European Research Council
ID : 949 806
Pays : International
Informations de copyright
© 2023 The Authors. Advanced Materials published by Wiley-VCH GmbH.
Références
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.
H.-W. Kang, S. J. Lee, I. K. Ko, C. Kengla, J. J. Yoo, A. Atala, Nat. Biotechnol. 2016, 34, 312.
R. Levato, T. Jungst, R. G. Scheuring, T. Blunk, J. Groll, J. Malda, Adv. Mater. 2020, 32, 1906423.
P. N. Bernal, P. Delrot, D. Loterie, Y. Li, J. Malda, C. Moser, R. Levato, Adv. Mater. 2019, 31, 1904209.
P. N. Bernal, M. Bouwmeester, J. Madrid-Wolff, M. Falandt, S. Florczak, N. G. Rodriguez, Y. Li, G. Größbacher, R. 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.
B. E. Kelly, I. Bhattacharya, H. Heidari, M. Shusteff, C. M. Spadaccini, H. K. Taylor, Science 2019, 363, 1075.
a) D. Loterie, P. Delrot, C. Moser, Volumetric 3D Printing of Elastomers by Tomographic Back-Projections 2018, 2;
b) D. Loterie, P. Delrot, C. Moser, Nat. Commun. 2020, 11, 852.
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 2018, 11, 013001.
K. Flégeau, A. Puiggali-Jou, M. Zenobi-Wong, Biofabrication 2022, 14, 034105.
A. Sinclair, M. B. O'Kelly, T. Bai, H.-C. Hung, P. Jain, S. Jiang, Adv. Mater. 2018, 30, 1803087.
T. J. Hinton, Q. Jallerat, R. N. Palchesko, J. H. Park, M. S. Grodzicki, H.-J. Shue, M. H. Ramadan, A. R. Hudson, A. W. Feinberg, Sci. Adv. 2015, 1, e1500758.
D. M. Headen, J. R. García, A. J. García, Microsyst. Nanoeng. 2018, 4, 17076.
L. Zhang, K. Chen, H. Zhang, B. Pang, C.-H. Choi, A. S. Mao, H. Liao, S. Utech, D. J. Mooney, H. Wang, D. A. Weitz, Small 2018, 14, 1702955.
G. C. Le Goff, J. Lee, A. Gupta, W. A. Hill, P. S. Doyle, Adv. Sci. 2015, 2, 1500149.
W. Yang, H. Yu, G. Li, Y. Wang, L. Liu, Small 2017, 13, 1602769.
W. Leong, T. T. Lau, D.-A. Wang, Acta Biomater. 2013, 9, 6459.
C. L. Franco, J. Price, J. L. West, Acta Biomater. 2011, 7, 3267.
J. E. Mealy, J. J. Chung, H.-H. Jeong, D. Issadore, D. Lee, P. Atluri, J. A. Burdick, Adv. Mater. 2018, 30, 1705912.
T. H. Qazi, J. A. Burdick, Biomater. Biosyst. 2021, 1, 100008.
A. R. Anderson, E. Nicklow, T. Segura, Acta Biomater. 2022, 150, 111.
E. Sideris, S. Kioulaphides, K. L. Wilson, A. Yu, J. Chen, S. T. Carmichael, T. Segura, Adv. Ther. 2022, 5, 2200048.
A. C. Daly, L. Riley, T. Segura, J. A. Burdick, Nat. Rev. Mater. 2020, 5, 20.
L. Riley, L. Schirmer, T. Segura, Curr. Opin. Biotechnol. 2019, 60, 1.
R.-S. Hsu, P.-Y. Chen, J.-H. Fang, Y.-Y. Chen, C.-W. Chang, Y.-J. Lu, S.-H. Hu, Adv. Sci. 2019, 6, 1900520.
S. Xin, D. Chimene, J. E. Garza, A. K. Gaharwar, D. L. Alge, Biomater. Sci. 2019, 7, 1179.
C. B. Highley, K. H. Song, A. C. Daly, J. A. Burdick, Adv. Sci. 2019, 6, 1801076.
A. Colly, C. Marquette, J.-M. Frances, E.-J. Courtial, MRS Bull. 2022, 48, 69.
D. J. Shiwarski, A. R. Hudson, J. W. Tashman, A. W. Feinberg, APL Bioeng. 2021, 5, 010904.
K. Zhou, Y. Sun, J. Yang, H. Mao, Z. Gu, J. Mater. Chem. B 2022, 10, 1897.
A. Schwab, R. Levato, M. D'Este, S. Piluso, D. Eglin, J. Malda, Chem. Rev. 2020, 120, 11028.
T. Bhattacharjee, S. M. Zehnder, K. G. Rowe, S. Jain, R. M. Nixon, W. G. Sawyer, T. E. Angelini, Sci. Adv. 2015, 1, e1500655.
S. Raees, F. Ullah, F. Javed, H. Md. Akil, M. Jadoon Khan, M. Safdar, I. U. Din, M. A. Alotaibi, A. I. Alharthi, M. A. Bakht, A. Ahmad, A. A. Nassar, Int. J. Biol. Macromol. 2023, 232, 123476.
A. K. Miri, D. Nieto, L. Iglesias, H. Goodarzi Hosseinabadi, S. Maharjan, G. U. Ruiz-Esparza, P. Khoshakhlagh, A. Manbachi, M. R. Dokmeci, S. Chen, S. R. Shin, Y. S. Zhang, A. Khademhosseini, Adv. Mater. 2018, 30, 1800242.
I. Pepelanova, K. Kruppa, T. Scheper, A. Lavrentieva, Bioengineering 2018, 5, 55.
M. Kesti, P. Fisch, M. Pensalfini, E. Mazza, M. Zenobi-Wong, BioNanomaterials 2016, 17, 193.
D. R. Griffin, W. M. Weaver, P. O. Scumpia, D. Di Carlo, T. Segura, Nat. Mater. 2015, 14, 737.
J. Madrid-Wolff, A. Boniface, D. Loterie, P. Delrot, C. Moser, Adv. Sci. 2022, 9, 2105144.
H. Liu, P. Chansoria, P. Delrot, E. Angelidakis, R. Rizzo, D. Rütsche, L. A. Applegate, D. Loterie, M. Zenobi-Wong, Adv. Mater. 2022, 34, 2204301.
R. C. Hurley, S. A. Hall, J. E. Andrade, J. Wright, Phys. Rev. Lett. 2016, 117, 098005.
X. Li, S. Chen, J. Li, X. Wang, J. Zhang, N. Kawazoe, G. Chen, Polymers 2016, 8, 269.
H. E. Park, N. Gasek, J. Hwang, D. J. Weiss, P. C. Lee, Phys. Fluids 2020, 32, 033102.
W. Schuurman, P. A. Levett, M. W. Pot, P. R. van Weeren, W. J. A. Dhert, D. W. Hutmacher, F. P. W. Melchels, T. J. Klein, J. Malda, Macromol. Biosci. 2013, 13, 551.
L. Rebers, T. Granse, G. E. M. Tovar, A. Southan, K. Borchers, Gels 2019, 5, 4.
A. C. Daly, M. D. Davidson, J. A. Burdick, Nat. Commun. 2021, 12, 753.
R. Rizzo, D. Ruetsche, H. Liu, M. Zenobi-Wong, Adv. Mater. 2021, 33, 2102900.
R. J. H. Stenekes, O. Franssen, E. M. G. van Bommel, D. J. A. Crommelin, W. E. Hennink, Pharm. Res. 1998, 15, 557.
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. 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.
L. R. Nih, E. Sideris, S. T. Carmichael, T. Segura, Adv. Mater. 2017, 29, 1606471.
D. Lam, H. A. Enright, J. Cadena, S. K. G. Peters, A. P. Sales, J. J. Osburn, D. A. Soscia, K. S. Kulp, E. K. Wheeler, N. O. Fischer, Sci. Rep. 2019, 9, 4159.
J. Kajtez, M. F. Wesseler, M. Birtele, F. R. Khorasgani, D. Rylander Ottosson, A. Heiskanen, T. Kamperman, J. Leijten, A. Martínez-Serrano, N. B. Larsen, T. E. Angelini, M. Parmar, J. U. Lind, J. Emnéus, Adv. Sci. 2022, 9, 2201392.
E. Sideris, D. R. Griffin, Y. Ding, S. Li, W. M. Weaver, D. Di Carlo, T. Hsiai, T. Segura, ACS Biomater. Sci. Eng. 2016, 2, 2034.
M. N. Collins, C. Birkinshaw, Carbohydr. Polym. 2013, 92, 1262.
N. Alkhouli, J. Mansfield, E. Green, J. Bell, B. Knight, N. Liversedge, J. C. Tham, R. Welbourn, A. C. Shore, K. Kos, C. P. Winlove, Am. J. Physiol. Endocrinol. Metab. 2013, 305, E1427.
Z. Sun, B. D. Gepner, S.-H. Lee, J. Rigby, P. S. Cottler, J. J. Hallman, J. R. Kerrigan, Acta Biomater. 2021, 129, 188.
L. Dilworth, A. Facey, F. Omoruyi, Int. J. Mol. Sci. 2021, 22, 7644.
T. Ronti, G. Lupattelli, E. Mannarino, Clin. Endocrinol. 2006, 64, 355.
P. S. Gungor-Ozkerim, I. Inci, Y. S. Zhang, A. Khademhosseini, M. R. Dokmeci, Biomater. Sci. 2018, 6, 915.
J. Adhikari, A. Roy, A. Das, M. Ghosh, S. Thomas, A. Sinha, J. Kim, P. Saha, Macromol. Biosci. 2021, 21, 2000179.
O. Jeon, Y. B. Lee, H. Jeong, S. J. Lee, D. Wells, E. Alsberg, Mater. Horiz. 2019, 6, 1625.
D. Wu, Y. Yu, J. Tan, L. Huang, B. Luo, L. Lu, C. Zhou, Mater. Des. 2018, 160, 486.
D. Ribezzi, R. Pinos, L. Bonetti, M. Cellani, F. Barbaglio, C. Scielzo, S. Farè, Front. Biomater. Sci. 2023, 2, 1081065.
P. Datta, M. Dey, Z. Ataie, D. Unutmaz, I. T. Ozbolat, npj Precis. Oncol. 2020, 4, 18.
E. M. Langer, B. L. Allen-Petersen, S. M. King, N. D. Kendsersky, M. A. Turnidge, G. M. Kuziel, R. Riggers, R. Samatham, T. S. Amery, S. L. Jacques, B. C. Sheppard, J. E. Korkola, J. L. Muschler, G. Thibault, Y. H. Chang, J. W. Gray, S. C. Presnell, D. G. Nguyen, R. C. Sears, Cell Rep. 2019, 26, 608.
A. Ribeiro, M. M. Blokzijl, R. Levato, C. W. Visser, M. Castilho, W. E. Hennink, T. Vermonden, J. Malda, Biofabrication 2017, 10, 014102.
V. H. M. Mouser, F. P. W. Melchels, J. Visser, W. J. A. Dhert, D. Gawlitta, J. Malda, Biofabrication 2016, 8, 035003.
S. Chen, W. S. Tan, M. A. Bin Juhari, Q. Shi, X. S. Cheng, W. L. Chan, J. Song, Biomed. Eng. Lett. 2020, 10, 453.
T. J. Hinton, A. Hudson, K. Pusch, A. Lee, A. W. Feinberg, ACS Biomater. Sci. Eng. 2016, 2, 1781.
M. Becker, M. Gurian, M. Schot, J. Leijten, Adv. Sci. 2023, 10, 2204609.
G. Größbacher, M. Bartolf-Kopp, C. Gergely, P. N. Bernal, S. Florczak, M. de Ruijter, J. Groll, J. Malda, T. Jüngst, R. Levato, Adv. Mater. 2023.
C. M. Rackson, K. M. Champley, J. T. Toombs, E. J. Fong, V. Bansal, H. K. Taylor, M. Shusteff, R. R. McLeod, Addit. Manuf. 2021, 48, 102367.
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.
M. Mansouri, S. Xue, M.-D. Hussherr, T. Strittmatter, G. Camenisch, M. Fussenegger, Small 2021, 17, 2101939.
A. Essaouiba, R. Jellali, M. Shinohara, B. Scheidecker, C. Legallais, Y. Sakai, E. Leclerc, J. Biotechnol. 2021, 330, 45.
D. Balboa, T. Barsby, V. Lithovius, J. Saarimäki-Vire, M. Omar-Hmeadi, O. Dyachok, H. Montaser, P.-E. Lund, M. Yang, H. Ibrahim, A. Näätänen, V. Chandra, H. Vihinen, E. Jokitalo, J. Kvist, J. Ustinov, A. I. Nieminen, E. Kuuluvainen, V. Hietakangas, P. Katajisto, J. Lau, P.-O. Carlsson, S. Barg, A. Tengholm, T. Otonkoski, Nat. Biotechnol. 2022, 40, 1042.
A. Garcia, A. Sekowski, V. Subramanian, D. L. Brasaemle, J. Biol. Chem. 2003, 278, 625.
C. Sztalryd, D. L. Brasaemle, Biochim. Biophys. Acta 2017, 1862, 1221.
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. Falandt, P. N. Bernal, O. Dudaryeva, S. Florczak, G. Größbacher, M. Schweiger, A. Longoni, C. Greant, m. Assunção, O. Nijssen, S. van Vlierberghe, J. Malda, T. Vermonden, R. Levato, Adv. Mater. Technol. 2023.
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.
D. Scholz, D. Pöltl, A. Genewsky, M. Weng, T. Waldmann, S. Schildknecht, M. Leist, J. Neurochem. 2011, 119, 957.
M. Imamura, E. Ozawa, Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 6139.
E. P. Knott, M. Assi, D. D. Pearse, Biomed Res. Int. 2014, 2014, 651625.
K. Krawczyk, S. Xue, P. Buchmann, G. Charpin-El-Hamri, P. Saxena, M.-D. Hussherr, J. Shao, H. Ye, M. Xie, M. Fussenegger, Science 2020, 368, 993.