Block Polyelectrolyte Additives That Modulate the Viscoelasticity and Enhance the Printability of Gelatin Inks at Physiological Temperatures

Göckler, Tobias; Albreiki, Fahed; Li, Defu; Grimm, Alisa; Mecklenburg, Felix; Urueña, Juan Manuel; Schepers, Ute; Srivastava, Samanvaya

doi:10.1021/acsapm.3c01085

Block Polyelectrolyte Additives That Modulate the Viscoelasticity and Enhance the Printability of Gelatin Inks at Physiological Temperatures

Journal Article · Tue Feb 20 23:00:00 EST 2024 · ACS Applied Polymer Materials

DOI:https://doi.org/10.1021/acsapm.3c01085· OSTI ID:2469498

Göckler, Tobias ^[1]; Albreiki, Fahed ^[2]; Li, Defu ^[2]; Grimm, Alisa ^[1]; Mecklenburg, Felix ^[3]; Urueña, Juan Manuel ^[4]; Schepers, Ute ^[3]; ^[2]

Univ. of California, Los Angeles, CA (United States); Karlsruhe Inst. of Technology (KIT) (Germany)
Univ. of California, Los Angeles, CA (United States)
Karlsruhe Inst. of Technology (KIT) (Germany)
Univ. of California, Santa Barbara, CA (United States)

We demonstrate the utility of block polyelectrolyte (bPE) additives to enhance viscosity and resolve challenges with the three-dimensional (3D) printability of extrusion-based biopolymer inks. The addition of oppositely charged bPEs to solutions of photocurable gelatin methacryloyl (GelMA) results in complexation-driven self-assembly of the bPEs, leading to GelMA/bPE inks that are printable at physiological temperatures, representing stark improvements over GelMA inks that suffer from low viscosity at 37 °C, leading to low printability and poor structural stability. The hierarchical microstructure of the self-assemblies (either jammed micelles or 3D networks) formed by the oppositely charged bPEs, confirmed by small-angle X-ray scattering, is attributed to the enhancements in the shear strength and printability of the GelMA/bPE inks. Varying bPE concentration in the inks is shown to enable tunability of the rheological properties to meet the criteria of pre- and postextrusion flow characteristics for 3D printing, including prominent yielding behavior, strong shear thinning, and rapid recovery upon flow cessation. Moreover, the bPE self-assemblies also contribute to the robustness of the photo-cross-linked hydrogels; photo-cross-linked GelMA/bPE hydrogels are shown to exhibit higher shear strength than photo-cross-linked GelMA hydrogels. Last, the assessment of the printability of GelMA/bPE inks indicates excellent printing performance, including minimal swelling postextrusion, satisfactory retention of the filament shape upon deposition, and satisfactory shape fidelity of the various printed constructs. We envision this study to serve as a practical guide for the printing of bespoke extrusion inks where bPEs are used as scaffolds and viscosity enhancers that can be emulated in a range of photocurable precursors.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); National Science Foundation (NSF)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 2469498

Journal Information:: ACS Applied Polymer Materials, Journal Name: ACS Applied Polymer Materials Journal Issue: 5 Vol. 6; ISSN 2637-6105

Publisher:: ACS PublicationsCopyright Statement

Country of Publication:: United States

Language:: English

References (69)

Controlling Shear Stress in 3D Bioprinting is a Key Factor to Balance Printing Resolution and Stem Cell Integrity Blaeser, Andreas; Duarte Campos, Daniela Filipa; Puster, Uta Advanced Healthcare Materials, Vol. 5, Issue 3 https://doi.org/10.1002/adhm.201500677	journal	December 2015
Extrusion Bioprinting of Shear‐Thinning Gelatin Methacryloyl Bioinks Liu, Wanjun; Heinrich, Marcel A.; Zhou, Yixiao Advanced Healthcare Materials, Vol. 6, Issue 12 https://doi.org/10.1002/adhm.201601451	journal	May 2017
Tuning Superfast Curing Thiol‐Norbornene‐Functionalized Gelatin Hydrogels for 3D Bioprinting Göckler, Tobias; Haase, Sonja; Kempter, Xenia Advanced Healthcare Materials, Vol. 10, Issue 14 https://doi.org/10.1002/adhm.202100206	journal	June 2021
Tunable, High Modulus Hydrogels Driven by Ionic Coacervation Hunt, Jasmine N.; Feldman, Kathleen E.; Lynd, Nathaniel A. Advanced Materials, Vol. 23, Issue 20 https://doi.org/10.1002/adma.201004230	journal	April 2011
25th Anniversary Article: Engineering Hydrogels for Biofabrication Malda, Jos; Visser, Jetze; Melchels, Ferry P. Advanced Materials, Vol. 25, Issue 36 https://doi.org/10.1002/adma.201302042	journal	August 2013
3D Bioprinting of Vascularized, Heterogeneous Cell-Laden Tissue Constructs Kolesky, David B.; Truby, Ryan L.; Gladman, A. Sydney Advanced Materials, Vol. 26, Issue 19 https://doi.org/10.1002/adma.201305506	journal	February 2014
From Shape to Function: The Next Step in Bioprinting Levato, Riccardo; Jungst, Tomasz; Scheuring, Ruben G. Advanced Materials, Vol. 32, Issue 12 https://doi.org/10.1002/adma.201906423	journal	February 2020
A Quantitative Description for Designing the Extrudability of Shear‐Thinning Physical Hydrogels Lopez Hernandez, Hector; Souza, Jason W.; Appel, Eric A. Macromolecular Bioscience, Vol. 21, Issue 2 https://doi.org/10.1002/mabi.202000295	journal	November 2020
Correlation of dynamic and steady flow viscosities Cox, W. P.; Merz, E. H. Journal of Polymer Science, Vol. 28, Issue 118 https://doi.org/10.1002/pol.1958.1202811812	journal	April 1958
3D Printable Gelatin Methacryloyl (GelMA)‐Dextran Aqueous Two‐Phase System with Tunable Pores Structure and Size Enables Physiological Behavior of Embedded Cells In Vitro Ben Messaoud, Ghazi; Aveic, Sanja; Wachendoerfer, Mattis Small, Vol. 19, Issue 44 https://doi.org/10.1002/smll.202208089	journal	July 2023
Shear flow properties of concentrated solutions of linear and star branched polystyrenes Yasuda, K.; Armstrong, R. C.; Cohen, R. E. Rheologica Acta, Vol. 20, Issue 2 https://doi.org/10.1007/BF01513059	journal	March 1981
Improved properties of bone and cartilage tissue from 3D inkjet-bioprinted human mesenchymal stem cells by simultaneous deposition and photocrosslinking in PEG-GelMA Gao, Guifang; Schilling, Arndt F.; Hubbell, Karen Biotechnology Letters, Vol. 37, Issue 11 https://doi.org/10.1007/s10529-015-1921-2	journal	July 2015
Characterization of Methacrylated Type-I Collagen as a Dynamic, Photoactive Hydrogel Gaudet, Ian D.; Shreiber, David I. Biointerphases, Vol. 7, Issue 1 https://doi.org/10.1007/s13758-012-0025-y	journal	March 2012
Hydrodynamic properties of gelatin in dilute solutions Bohidar, Himadri B. International Journal of Biological Macromolecules, Vol. 23, Issue 1 https://doi.org/10.1016/S0141-8130(98)00003-8	journal	July 1998
Cell-laden microengineered gelatin methacrylate hydrogels Nichol, Jason W.; Koshy, Sandeep T.; Bae, Hojae Biomaterials, Vol. 31, Issue 21 https://doi.org/10.1016/j.biomaterials.2010.03.064	journal	July 2010
Synthesis, properties, and biomedical applications of gelatin methacryloyl (GelMA) hydrogels Yue, Kan; Trujillo-de Santiago, Grissel; Alvarez, Mario Moisés Biomaterials, Vol. 73 https://doi.org/10.1016/j.biomaterials.2015.08.045	journal	December 2015
Current advances and future perspectives in extrusion-based bioprinting Ozbolat, Ibrahim T.; Hospodiuk, Monika Biomaterials, Vol. 76 https://doi.org/10.1016/j.biomaterials.2015.10.076	journal	January 2016
The bioink: A comprehensive review on bioprintable materials Hospodiuk, Monika; Dey, Madhuri; Sosnoski, Donna Biotechnology Advances, Vol. 35, Issue 2 https://doi.org/10.1016/j.biotechadv.2016.12.006	journal	March 2017
Thixotropy Mewis, Jan; Wagner, Norman J. Advances in Colloid and Interface Science, Vol. 147-148 https://doi.org/10.1016/j.cis.2008.09.005	journal	March 2009
Application areas of 3D bioprinting Ozbolat, Ibrahim T.; Peng, Weijie; Ozbolat, Veli Drug Discovery Today, Vol. 21, Issue 8 https://doi.org/10.1016/j.drudis.2016.04.006	journal	August 2016
3D Printing of Buildings: Construction of the Sustainable Houses of the Future by BIM Sakin, Mehmet; Kiroglu, Yusuf Caner Energy Procedia, Vol. 134 https://doi.org/10.1016/j.egypro.2017.09.562	journal	October 2017
A global sustainability perspective on 3D printing technologies Gebler, Malte; Schoot Uiterkamp, Anton J. M.; Visser, Cindy Energy Policy, Vol. 74 https://doi.org/10.1016/j.enpol.2014.08.033	journal	November 2014
3-D bioprinting technologies in tissue engineering and regenerative medicine: Current and future trends Bishop, Elliot S.; Mostafa, Sami; Pakvasa, Mikhail Genes & Diseases, Vol. 4, Issue 4 https://doi.org/10.1016/j.gendis.2017.10.002	journal	December 2017
Environmental assessment of additive manufacturing in the automotive industry Böckin, Daniel; Tillman, Anne-Marie Journal of Cleaner Production, Vol. 226 https://doi.org/10.1016/j.jclepro.2019.04.086	journal	July 2019
Yield stress fluid flows: A review of experimental data Coussot, P. Journal of Non-Newtonian Fluid Mechanics, Vol. 211 https://doi.org/10.1016/j.jnnfm.2014.05.006	journal	September 2014
AM and aerospace: an ideal combination Nickels, Liz Metal Powder Report, Vol. 70, Issue 6 https://doi.org/10.1016/j.mprp.2015.06.005	journal	November 2015
How does the automotive industry benefit from 3D metal printing? Nichols, Megan R. Metal Powder Report, Vol. 74, Issue 5 https://doi.org/10.1016/j.mprp.2019.07.002	journal	October 2019
Bioinks and bioprinting technologies to make heterogeneous and biomimetic tissue constructs Ashammakhi, N.; Ahadian, S.; Xu, C. Materials Today Bio, Vol. 1 https://doi.org/10.1016/j.mtbio.2019.100008	journal	January 2019
Flow behavior prior to crosslinking: The need for precursor rheology for placement of hydrogels in medical applications and for 3D bioprinting Townsend, Jakob M.; Beck, Emily C.; Gehrke, Stevin H. Progress in Polymer Science, Vol. 91 https://doi.org/10.1016/j.progpolymsci.2019.01.003	journal	April 2019
Gelatin-Methacryloyl Hydrogels: Towards Biofabrication-Based Tissue Repair Klotz, Barbara J.; Gawlitta, Debby; Rosenberg, Antoine J. W. P. Trends in Biotechnology, Vol. 34, Issue 5 https://doi.org/10.1016/j.tibtech.2016.01.002	journal	May 2016
Pushing the rheological and mechanical boundaries of extrusion-based 3D bioprinting Ouyang, Liliang Trends in Biotechnology, Vol. 40, Issue 7 https://doi.org/10.1016/j.tibtech.2022.01.001	journal	July 2022
Physical and Chemical Factors Influencing the Printability of Hydrogel-based Extrusion Bioinks Lee, Sang Cheon; Gillispie, Gregory; Prim, Peter Chemical Reviews, Vol. 120, Issue 19 https://doi.org/10.1021/acs.chemrev.0c00015	journal	August 2020
Strategies and Molecular Design Criteria for 3D Printable Hydrogels Jungst, Tomasz; Smolan, Willi; Schacht, Kristin Chemical Reviews, Vol. 116, Issue 3 https://doi.org/10.1021/acs.chemrev.5b00303	journal	October 2015
Polymeric Systems for Bioprinting Bedell, Matthew L.; Navara, Adam M.; Du, Yingying Chemical Reviews, Vol. 120, Issue 19 https://doi.org/10.1021/acs.chemrev.9b00834	journal	May 2020
Physicochemical Response of Gelatin in a Coulombic Soup of Monovalent Salt: A Molecular Simulation and Experimental Study Swain, Pinaki; Ronghe, Anshaj; Bhutani, Utkarsh The Journal of Physical Chemistry B, Vol. 123, Issue 5 https://doi.org/10.1021/acs.jpcb.8b11379	journal	January 2019
Structure, Morphology, and Rheology of Polyelectrolyte Complex Hydrogels Formed by Self-Assembly of Oppositely Charged Triblock Polyelectrolytes Srivastava, Samanvaya; Levi, Adam E.; Goldfeld, David J. Macromolecules, Vol. 53, Issue 14 https://doi.org/10.1021/acs.macromol.0c00847	journal	July 2020
Structure and Relaxation Dynamics for Complex Coacervate Hydrogels Formed by ABA Triblock Copolymers Kim, Jung-Min; Heo, Tae-Young; Choi, Soo-Hyung Macromolecules, Vol. 53, Issue 21 https://doi.org/10.1021/acs.macromol.0c01600	journal	October 2020
Polyelectrolyte Complex-Covalent Interpenetrating Polymer Network Hydrogels Li, Defu; Göckler, Tobias; Schepers, Ute Macromolecules, Vol. 55, Issue 11 https://doi.org/10.1021/acs.macromol.2c00590	journal	June 2022
Controlled Degradation and Mechanical Behavior of Photopolymerized Hyaluronic Acid Networks Burdick, Jason A.; Chung, Cindy; Jia, Xinqiao Biomacromolecules, Vol. 6, Issue 1 https://doi.org/10.1021/bm049508a	journal	November 2004
Structural and Rheological Properties of Methacrylamide Modified Gelatin Hydrogels Van Den Bulcke, An I.; Bogdanov, Bogdan; De Rooze, Nadine Biomacromolecules, Vol. 1, Issue 1 https://doi.org/10.1021/bm990017d	journal	March 2000
Effects of Polymer and Salt Concentration on the Structure and Properties of Triblock Copolymer Coacervate Hydrogels Krogstad, Daniel V.; Lynd, Nathaniel A.; Choi, Soo-Hyung Macromolecules, Vol. 46, Issue 4 https://doi.org/10.1021/ma302299r	journal	February 2013
3D bioprinting of tissues and organs Murphy, Sean V.; Atala, Anthony Nature Biotechnology, Vol. 32, Issue 8 https://doi.org/10.1038/nbt.2958	journal	August 2014
Gel phase formation in dilute triblock copolyelectrolyte complexes Srivastava, Samanvaya; Andreev, Marat; Levi, Adam E. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14131	journal	February 2017
Biofabrication strategies for 3D in vitro models and regenerative medicine Moroni, Lorenzo; Burdick, Jason A.; Highley, Christopher Nature Reviews Materials, Vol. 3, Issue 5 https://doi.org/10.1038/s41578-018-0006-y	journal	April 2018
Multilayer 3D bioprinting and complex mechanical properties of alginate-gelatin mesostructures Ahmadi Soufivand, Anahita; Faber, Jessica; Hinrichsen, Jan Scientific Reports, Vol. 13, Issue 1 https://doi.org/10.1038/s41598-023-38323-2	journal	July 2023
Bioinks for 3D bioprinting: an overview Gungor-Ozkerim, P. Selcan; Inci, Ilyas; Zhang, Yu Shrike Biomaterials Science, Vol. 6, Issue 5 https://doi.org/10.1039/C7BM00765E	journal	January 2018
Chemical insights into bioinks for 3D printing Valot, Laurine; Martinez, Jean; Mehdi, Ahmad Chemical Society Reviews, Vol. 48, Issue 15 https://doi.org/10.1039/C7CS00718C	journal	January 2019
Porous scaffolds with the structure of an interpenetrating polymer network made by gelatin methacrylated nanoparticle-stabilized high internal phase emulsion polymerization targeted for tissue engineering Safaei-Yaraziz, Atefeh; Akbari-Birgani, Shiva; Nikfarjam, Nasser RSC Advances, Vol. 11, Issue 37 https://doi.org/10.1039/D1RA03333F	journal	January 2021
Polyelectrolyte complex scaffoldings for photocrosslinked hydrogels Li, Defu; Ghovvati, Mahsa; Annabi, Nasim Molecular Systems Design & Engineering, Vol. 8, Issue 5 https://doi.org/10.1039/D2ME00171C	journal	January 2023
Transient network topology of interconnected polyelectrolyte complex micelles Lemmers, Marc; Voets, Ilja K.; Cohen Stuart, Martien A. Soft Matter, Vol. 7, Issue 4 https://doi.org/10.1039/c0sm00767f	journal	January 2011
The rheology of direct and suspended extrusion bioprinting Cooke, Megan E.; Rosenzweig, Derek H. APL Bioengineering, Vol. 5, Issue 1 https://doi.org/10.1063/5.0031475	journal	February 2021
Role of temperature on bio-printability of gelatin methacryloyl bioink in two-step cross-linking strategy for tissue engineering applications Janmaleki, Mohsen; Liu, Jun; Kamkar, Milad Biomedical Materials, Vol. 16, Issue 1 https://doi.org/10.1088/1748-605X/abbcc9	journal	December 2020
Direct-write bioprinting of cell-laden methacrylated gelatin hydrogels Bertassoni, Luiz E.; Cardoso, Juliana C.; Manoharan, Vijayan Biofabrication, Vol. 6, Issue 2 https://doi.org/10.1088/1758-5082/6/2/024105	journal	April 2014
Fabrication of poly(ethylene glycol): gelatin methacrylate composite nanostructures with tunable stiffness and degradation for vascular tissue engineering Kim, Peter; Yuan, Alex; Nam, Ki-Hwan Biofabrication, Vol. 6, Issue 2 https://doi.org/10.1088/1758-5082/6/2/024112	journal	April 2014
Towards artificial tissue models: past, present, and future of 3D bioprinting Arslan-Yildiz, Ahu; Assal, Rami El; Chen, Pu Biofabrication, Vol. 8, Issue 1 https://doi.org/10.1088/1758-5090/8/1/014103	journal	March 2016
Bioink properties before, during and after 3D bioprinting Hölzl, Katja; Lin, Shengmao; Tytgat, Liesbeth Biofabrication, Vol. 8, Issue 3 https://doi.org/10.1088/1758-5090/8/3/032002	journal	September 2016
Effect of bioink properties on printability and cell viability for 3D bioplotting of embryonic stem cells Ouyang, Liliang; Yao, Rui; Zhao, Yu Biofabrication, Vol. 8, Issue 3 https://doi.org/10.1088/1758-5090/8/3/035020	journal	September 2016
Proposal to assess printability of bioinks for extrusion-based bioprinting and evaluation of rheological properties governing bioprintability Paxton, Naomi; Smolan, Willi; Böck, Thomas Biofabrication, Vol. 9, Issue 4 https://doi.org/10.1088/1758-5090/aa8dd8	journal	November 2017
The bioprinting roadmap Sun, Wei; Starly, Binil; Daly, Andrew C. Biofabrication, Vol. 12, Issue 2 https://doi.org/10.1088/1758-5090/ab5158	journal	February 2020
Synthesis and Characterization of Tunable Poly(Ethylene Glycol): Gelatin Methacrylate Composite Hydrogels Hutson, Che B.; Nichol, Jason W.; Aubin, Hug Tissue Engineering Part A, Vol. 17, Issue 13-14 https://doi.org/10.1089/ten.tea.2010.0666	journal	July 2011
Enhanced Chondrogenic Differentiation of Dental Pulp Stem Cells Using Nanopatterned PEG-GelMA-HA Hydrogels Nemeth, Cameron L.; Janebodin, Kajohnkiart; Yuan, Alex E. Tissue Engineering Part A, Vol. 20, Issue 21-22 https://doi.org/10.1089/ten.tea.2013.0614	journal	November 2014
From consumer to prosumer: a supply chain revolution in 3D printing Halassi, Sam; Semeijn, Janjaap; Kiratli, Nadine International Journal of Physical Distribution & Logistics Management, Vol. 49, Issue 2 https://doi.org/10.1108/IJPDLM-03-2018-0139	journal	March 2019
Prosumption perspectives on additive manufacturing: reconfiguration of consumer products with 3D printing Yoo, Byounghyun; Ko, Heedong; Chun, Sungkuk Rapid Prototyping Journal, Vol. 22, Issue 4 https://doi.org/10.1108/RPJ-01-2015-0004	journal	June 2016
Bioprinting Toward Organ Fabrication: Challenges and Future Trends Ozbolat, I. T. IEEE Transactions on Biomedical Engineering, Vol. 60, Issue 3 https://doi.org/10.1109/TBME.2013.2243912	journal	March 2013
The rheology of solutions of associating polymers: Comparison of experimental behavior with transient network theory Annable, Tom; Buscall, Richard; Ettelaie, Rammile Journal of Rheology, Vol. 37, Issue 4 https://doi.org/10.1122/1.550391	journal	July 1993
Structure and Unique Functions of Anisotropic Hydrogels Comprising Uniaxially Aligned Lamellar Bilayers Yue, Youfeng; Gong, Jian Ping Bulletin of the Chemical Society of Japan, Vol. 94, Issue 9 https://doi.org/10.1246/bcsj.20210209	journal	July 2021
Organ printing: promises and challenges Mironov, Vladimir; Kasyanov, Vladimir; Drake, Christopher Regenerative Medicine, Vol. 3, Issue 1 https://doi.org/10.2217/17460751.3.1.93	journal	January 2008
Architectural Evaluation of 3D-Printed Buildings García-Alvarado, Rodrigo; Moroni-Orellana, Ginnia; Banda-Pérez, Pablo Buildings, Vol. 11, Issue 6 https://doi.org/10.3390/buildings11060254	journal	June 2021
Protocols of 3D Bioprinting of Gelatin Methacryloyl Hydrogel Based Bioinks Xie, Mingjun; Yu, Kang; Sun, Yuan Journal of Visualized Experiments, Issue 154 https://doi.org/10.3791/60545	journal	December 2019

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