3D-Printed pHEMA Materials for Topographical and Biochemical Modulation of Dorsal Root Ganglion Cell Response

Badea, Adina; McCracken, Joselle M.; Tillmaand, Emily G.; Kandel, Mikhail E.; Oraham, Aaron W.; Mevis, Molly B.; Rubakhin, Stanislav S.; Popescu, Gabriel; Sweedler, Jonathan V.; Nuzzo, Ralph G.

doi:10.1021/acsami.7b06742

Title: 3D-Printed pHEMA Materials for Topographical and Biochemical Modulation of Dorsal Root Ganglion Cell Response

Journal Article · Thu Aug 31 00:00:00 EDT 2017 · ACS Applied Materials and Interfaces

DOI:https://doi.org/10.1021/acsami.7b06742· OSTI ID:1418567

^[1]; McCracken, Joselle M. ^[1]; Tillmaand, Emily G. ^[1];

^[1]; Oraham, Aaron W. ^[1]; Mevis, Molly B. ^[1];

^[1]; Popescu, Gabriel ^[1];

^[1]; Nuzzo, Ralph G. ^[2]

Univ. of Illinois at Urbana-Champaign, IL (United States)
Univ. of Illinois at Urbana-Champaign, IL (United States); KTH Royal Inst. of Technology, Stockholm (Sweden)

Understanding and controlling the interactions occurring between cells and engineered materials are central challenges toward progress in the development of biomedical devices. In this work, we describe materials for direct ink writing (DIW), an extrusion-based type of 3D printing, that embed a custom synthetic protein (RGD-PDL) within the microfilaments of 3D-hydrogel scaffolds to modify these interactions and differentially direct tissue-level organization of complex cell populations in vitro. The RGD-PDL is synthesized by modifying poly-d-lysine (PDL) to varying extents with peptides containing the integrin-binding motif Arg-Gly-Asp (RGD). Compositional gradients of the RGD-PDL presented by both patterned and thin-film poly(2-hydroxyethyl) methacrylate (pHEMA) substrates allow the patterning of cell-growth compliance in a grayscale form. The surface chemistry-dependent guidance of cell growth on the RGD-PDL-modified pHEMA materials is demonstrated using a model NIH-3T3 fibroblast cell line. The formation of a more complex cellular system—organotypic primary murine dorsal root ganglion (DRG)—in culture is also achieved on these scaffolds, where distinctive forms of cell growth and migration guidance are seen depending on their RGD-PDL content and topography. In conclusion, this experimental platform for the study of physicochemical factors on the formation and the reorganization of organotypic cultures offers useful capabilities for studies in tissue engineering, regenerative medicine, and diagnostics.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of Illinois at Urbana-Champaign, IL (United States)

Sponsoring Organization:: National Science Foundation (NSF); Army Research Office (ARO); USDOE

Grant/Contract Number:: FG02-07ER46471; CBET-0939511 STC; DBI 14-50962 EAGER; IIP-1353368

OSTI ID:: 1418567

Journal Information:: ACS Applied Materials and Interfaces, Vol. 9, Issue 36; ISSN 1944-8244

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (80)

Neurogenesis and neuronal communication on micropatterned neurochips Bani-Yaghoub, Mahmud; Tremblay, Roger; Voicu, Raluca Biotechnology and Bioengineering, Vol. 92, Issue 3 https://doi.org/10.1002/bit.20618	journal	January 2005
Micropatterned substrates coated with neuronal adhesion molecules for high-content study of synapse formation Czöndör, Katalin; Garcia, Mikael; Argento, Amélie Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3252	journal	August 2013
Developmental Neurobiology Implications from Fabrication and Analysis of Hippocampal Neuronal Networks on Patterned Silane-Modified Surfaces Ravenscroft, M. S.; Bateman, K. E.; Shaffer, K. M. Journal of the American Chemical Society, Vol. 120, Issue 47 https://doi.org/10.1021/ja973669n	journal	November 1998
Synaptic plasticity in micropatterned neuronal networks Vogt, Angela K.; Wrobel, Günter; Meyer, Wolfgang Biomaterials, Vol. 26, Issue 15 https://doi.org/10.1016/j.biomaterials.2004.07.031	journal	May 2005
Controlled outgrowth of dissociated neurons on patterned substrates Kleinfeld, D.; Kahler, Kh; Hockberger, Pe The Journal of Neuroscience, Vol. 8, Issue 11 https://doi.org/10.1523/JNEUROSCI.08-11-04098.1988	journal	November 1988
Micropatterned Coumarin Polyester Thin Films Direct Neurite Orientation McCormick, Aleesha M.; Maddipatla, Murthy V. S. N.; Shi, Shuojia ACS Applied Materials & Interfaces, Vol. 6, Issue 22 https://doi.org/10.1021/am5044328	journal	October 2014
High fidelity neuronal networks formed by plasma masking with a bilayer membrane: analysis of neurodegenerative and neuroprotective processes Hardelauf, Heike; Sisnaiske, Julia; Taghipour-Anvari, Amir Ali Lab on a Chip, Vol. 11, Issue 16 https://doi.org/10.1039/c1lc20257j	journal	January 2011
Development of multifunctional films for peripheral nerve regeneration Uz, Metin; Sharma, Anup D.; Adhikari, Pratish Acta Biomaterialia, Vol. 56 https://doi.org/10.1016/j.actbio.2016.09.039	journal	July 2017
Synapse microarray identification of small molecules that enhance synaptogenesis Shi, Peng; Scott, Mark A.; Ghosh, Balaram Nature Communications, Vol. 2, Issue 1 https://doi.org/10.1038/ncomms1518	journal	September 2011
Neural Pathfinding on Uni- and Multidirectional Photopolymerized Micropatterns Tuft, Bradley W.; Xu, Linjing; White, Scott P. ACS Applied Materials & Interfaces, Vol. 6, Issue 14 https://doi.org/10.1021/am501622a	journal	June 2014
Micropatterned methacrylate polymers direct spiral ganglion neurite and Schwann cell growth Clarke, Joseph C.; Tuft, Bradley W.; Clinger, John D. Hearing Research, Vol. 278, Issue 1-2 https://doi.org/10.1016/j.heares.2011.05.004	journal	August 2011
Generation of Gradients Having Complex Shapes Using Microfluidic Networks Dertinger, Stephan K. W.; Chiu, Daniel T.; Jeon, Noo Li Analytical Chemistry, Vol. 73, Issue 6 https://doi.org/10.1021/ac001132d	journal	March 2001
A microfluidic culture platform for CNS axonal injury, regeneration and transport Taylor, Anne M.; Blurton-Jones, Mathew; Rhee, Seog Woo Nature Methods, Vol. 2, Issue 8 https://doi.org/10.1038/nmeth777	journal	July 2005
Engineering the morphology and electrophysiological parameters of cultured neurons by microfluidic surface patterning Romanova, Elena V.; Fosser, Kari A.; Rubakhin, Stanislav S. The FASEB Journal, Vol. 18, Issue 11 https://doi.org/10.1096/fj.03-1368fje	journal	June 2004
Regulation of axon guidance and extension by three-dimensional constraints Francisco, H.; Yellen, B.; Halverson, D. Biomaterials, Vol. 28, Issue 23 https://doi.org/10.1016/j.biomaterials.2007.04.015	journal	August 2007
Micropatterning neuronal networks Hardelauf, Heike; Waide, Sarah; Sisnaiske, Julia The Analyst, Vol. 139, Issue 13 https://doi.org/10.1039/C4AN00608A	journal	January 2014
A modified microstamping technique enhances polylysine transfer and neuronal cell patterning Chang, John C.; Brewer, Gregory J.; Wheeler, Bruce C. Biomaterials, Vol. 24, Issue 17 https://doi.org/10.1016/S0142-9612(03)00116-9	journal	August 2003
Topographical and Physicochemical Modification of Material Surface to Enable Patterning of Living Cells Jung, D. R.; Kapur, R.; Adams, T. Critical Reviews in Biotechnology, Vol. 21, Issue 2 https://doi.org/10.1080/20013891081700	journal	January 2001
Portable Micropatterns of Neuronal Cells Supported by Thin Hydrogel Films Nagamine, Kuniaki; Hirata, Takuya; Okamoto, Kohei ACS Biomaterials Science & Engineering, Vol. 1, Issue 5 https://doi.org/10.1021/acsbiomaterials.5b00020	journal	April 2015
Soft Lithography in Biology and Biochemistry Whitesides, George M.; Ostuni, Emanuele; Takayama, Shuichi Annual Review of Biomedical Engineering, Vol. 3, Issue 1 https://doi.org/10.1146/annurev.bioeng.3.1.335	journal	August 2001
Recent progress in soft lithography Rogers, John A.; Nuzzo, Ralph G. Materials Today, Vol. 8, Issue 2 https://doi.org/10.1016/S1369-7021(05)00702-9	journal	February 2005
Geometric Control of Cell Life and Death Chen, C. S. Science, Vol. 276, Issue 5317 https://doi.org/10.1126/science.276.5317.1425	journal	May 1997
Microcontact Printing of Proteins Bernard, A.; Renault, J. P.; Michel, B. Advanced Materials, Vol. 12, Issue 14 https://doi.org/10.1002/1521-4095(200007)12:14<1067::AID-ADMA1067>3.3.CO;2-D	journal	July 2000
Microcontact printing of proteins for neuronal cell guidance Offenhäusser, Andreas; Böcker-Meffert, Simone; Decker, Tanja Soft Matter, Vol. 3, Issue 3 https://doi.org/10.1039/B607615G	journal	January 2007
Microstamp patterns of biomolecules for high-resolution neuronal networks Branch, D. W.; Corey, J. M.; Weyhenmeyer, J. A. Medical & Biological Engineering & Computing, Vol. 36, Issue 1 https://doi.org/10.1007/BF02522871	journal	January 1998
Patterning proteins and cells using soft lithography Kane, Ravi S.; Takayama, Shuichi; Ostuni, Emanuele Biomaterials, Vol. 20, Issue 23-24, p. 2363-2376 https://doi.org/10.1016/S0142-9612(99)00165-9	journal	December 1999
Patterned polymer growth on silicon surfaces using microcontact printing and surface-initiated polymerization Jeon, Noo Li; Choi, Insung S.; Whitesides, George M. Applied Physics Letters, Vol. 75, Issue 26 https://doi.org/10.1063/1.125582	journal	December 1999
Plasma stencilling methods for cell patterning Frimat, Jean-Philippe; Menne, Heike; Michels, Antje Analytical and Bioanalytical Chemistry, Vol. 395, Issue 3 https://doi.org/10.1007/s00216-009-2824-7	journal	May 2009
Digital microfluidic programmable stencil (dMPS) for protein and cell patterning Gao, Yibo; Tian, Jingxuan; Wu, Jinbo RSC Advances, Vol. 6, Issue 104 https://doi.org/10.1039/C6RA17633J	journal	January 2016
Tissue Engineering--Current Challenges and Expanding Opportunities Griffith, L. G. Science, Vol. 295, Issue 5557 https://doi.org/10.1126/science.1069210	journal	February 2002
A Systems-Level Analysis of the Peripheral Nerve Intrinsic Axonal Growth Program Chandran, Vijayendran; Coppola, Giovanni; Nawabi, Homaira Neuron, Vol. 89, Issue 5 https://doi.org/10.1016/j.neuron.2016.01.034	journal	March 2016
The neuropathic pain triad: neurons, immune cells and glia Scholz, Joachim; Woolf, Clifford J. Nature Neuroscience, Vol. 10, Issue 11 https://doi.org/10.1038/nn1992	journal	October 2007
Electrical and Neurotrophin Enhancement of Neurite Outgrowth Within a 3D Collagen Scaffold Adams, Robert D.; Rendell, Sara R.; Counts, Lauren R. Annals of Biomedical Engineering, Vol. 42, Issue 6 https://doi.org/10.1007/s10439-014-1001-0	journal	April 2014
An aligned 3D neuronal-glial co-culture model for peripheral nerve studies Daud, Muhammad F. B.; Pawar, Kiran C.; Claeyssens, Frederik Biomaterials, Vol. 33, Issue 25 https://doi.org/10.1016/j.biomaterials.2012.05.008	journal	September 2012
Aligned neurite outgrowth and directed cell migration in self-assembled monodomain gels Berns, Eric J.; Sur, Shantanu; Pan, Liuliu Biomaterials, Vol. 35, Issue 1 https://doi.org/10.1016/j.biomaterials.2013.09.077	journal	January 2014
Two pole air gap electrospinning: Fabrication of highly aligned, three-dimensional scaffolds for nerve reconstruction Jha, Balendu S.; Colello, Raymond J.; Bowman, James R. Acta Biomaterialia, Vol. 7, Issue 1 https://doi.org/10.1016/j.actbio.2010.08.004	journal	January 2011
Nanofibrous Collagen Nerve Conduits for Spinal Cord Repair Liu, Ting; Houle, John D.; Xu, Jinye Tissue Engineering Part A, Vol. 18, Issue 9-10 https://doi.org/10.1089/ten.tea.2011.0430	journal	May 2012
Neuronal Electrophysiological Function and Control of Neurite Outgrowth on Electrospun Polymer Nanofibers Are Cell Type Dependent Bourke, Justin L.; Coleman, Harold A.; Pham, Vi Tissue Engineering Part A, Vol. 20, Issue 5-6 https://doi.org/10.1089/ten.tea.2013.0295	journal	March 2014
Nerve Guidance Conduits Based on Double-Layered Scaffolds of Electrospun Nanofibers for Repairing the Peripheral Nervous System Xie, Jingwei; MacEwan, Matthew R.; Liu, Wenying ACS Applied Materials & Interfaces, Vol. 6, Issue 12 https://doi.org/10.1021/am5018557	journal	May 2014
3D Printed Anatomical Nerve Regeneration Pathways Johnson, Blake N.; Lancaster, Karen Z.; Zhen, Gehua Advanced Functional Materials, Vol. 25, Issue 39 https://doi.org/10.1002/adfm.201501760	journal	September 2015
Cytoscribing: A method for micropositioning cells and the construction of two- and three-dimensional synthetic tissues Klebe, R. Experimental Cell Research, Vol. 179, Issue 2 https://doi.org/10.1016/0014-4827(88)90275-3	journal	December 1988
Complex heterogeneous tissue constructs containing multiple cell types prepared by inkjet printing technology Xu, Tao; Zhao, Weixin; Zhu, Jian-Ming Biomaterials, Vol. 34, Issue 1 https://doi.org/10.1016/j.biomaterials.2012.09.035	journal	January 2013
Inkjet printing of viable mammalian cells Xu, Tao; Jin, Joyce; Gregory, Cassie Biomaterials, Vol. 26, Issue 1 https://doi.org/10.1016/j.biomaterials.2004.04.011	journal	January 2005
Thermal Inkjet Printing in Tissue Engineering and Regenerative Medicine Cui, Xiaofeng; Boland, Thomas; D. D'Lima, Darryl Recent Patents on Drug Delivery & Formulation, Vol. 6, Issue 2 https://doi.org/10.2174/187221112800672949	journal	May 2012
Direct Freeform Fabrication of Seeded Hydrogels in Arbitrary Geometries Cohen, Daniel L.; Malone, Evan; Lipson, Hod Tissue Engineering, Vol. 12, Issue 5 https://doi.org/10.1089/ten.2006.12.1325	journal	May 2006
Bio rapid prototyping by extruding/aspirating/refilling thermoreversible hydrogel Iwami, K.; Noda, T.; Ishida, K. Biofabrication, Vol. 2, Issue 1 https://doi.org/10.1088/1758-5082/2/1/014108	journal	March 2010
Precision extruding deposition (PED) fabrication of polycaprolactone (PCL) scaffolds for bone tissue engineering Shor, Lauren; Güçeri, Selçuk; Chang, Robert Biofabrication, Vol. 1, Issue 1 https://doi.org/10.1088/1758-5082/1/1/015003	journal	March 2009
Biological Laser Printing: A Novel Technique for Creating Heterogeneous 3-dimensional Cell Patterns Barron, J. A.; Wu, P.; Ladouceur, H. D. Biomedical Microdevices, Vol. 6, Issue 2 https://doi.org/10.1023/B:BMMD.0000031751.67267.9f	journal	June 2004
High-throughput laser printing of cells and biomaterials for tissue engineering Guillemot, F.; Souquet, A.; Catros, S. Acta Biomaterialia, Vol. 6, Issue 7 https://doi.org/10.1016/j.actbio.2009.09.029	journal	July 2010
Laser assisted bioprinting of engineered tissue with high cell density and microscale organization Guillotin, Bertrand; Souquet, Agnès; Catros, Sylvain Biomaterials, Vol. 31, Issue 28 https://doi.org/10.1016/j.biomaterials.2010.05.055	journal	October 2010
Direct-Write Assembly of 3D Silk/Hydroxyapatite Scaffolds for Bone Co-Cultures Sun, Lin; Parker, Sara T.; Syoji, Daisuke Advanced Healthcare Materials, Vol. 1, Issue 6 https://doi.org/10.1002/adhm.201200057	journal	May 2012
A review of rapid prototyping techniques for tissue engineering purposes Peltola, Sanna M.; Melchels, Ferry P. W.; Grijpma, Dirk W. Annals of Medicine, Vol. 40, Issue 4 https://doi.org/10.1080/07853890701881788	journal	January 2008
High-Throughput Printing via Microvascular Multinozzle Arrays Hansen, Christopher J.; Saksena, Rajat; Kolesky, David B. Advanced Materials, Vol. 25, Issue 1 https://doi.org/10.1002/adma.201203321	journal	October 2012
Hydrogels for tissue engineering: scaffold design variables and applications Drury, Jeanie L.; Mooney, David J. Biomaterials, Vol. 24, Issue 24 https://doi.org/10.1016/S0142-9612(03)00340-5	journal	November 2003
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
Biomimetic 4D printing Sydney Gladman, A.; Matsumoto, Elisabetta A.; Nuzzo, Ralph G. Nature Materials, Vol. 15, Issue 4 https://doi.org/10.1038/nmat4544	journal	January 2016
Hydrogels in healthcare: From static to dynamic material microenvironments Kirschner, Chelsea M.; Anseth, Kristi S. Acta Materialia, Vol. 61, Issue 3 https://doi.org/10.1016/j.actamat.2012.10.037	journal	February 2013
Coating process and early stage adhesion evaluation of poly(2-hydroxy-ethyl-methacrylate) hydrogel coating of 316L steel surface for stent applications Indolfi, Laura; Causa, Filippo; Netti, Paolo Antonio Journal of Materials Science: Materials in Medicine, Vol. 20, Issue 7 https://doi.org/10.1007/s10856-009-3699-z	journal	March 2009
Hydrophilic Gels for Biological Use Wichterle, O.; LÍM, D. Nature, Vol. 185, Issue 4706 https://doi.org/10.1038/185117a0	journal	January 1960
2-Hydroxyethyl Methacrylate (HEMA): Chemical Properties and Applications in Biomedical Fields Montheard, Jean-Pierre; Chatzopoulos, Michel; Chappard, Daniel Journal of Macromolecular Science, Part C: Polymer Reviews, Vol. 32, Issue 1 https://doi.org/10.1080/15321799208018377	journal	February 1992
Programming Mechanical and Physicochemical Properties of 3D Hydrogel Cellular Microcultures via Direct Ink Writing McCracken, Joselle M.; Badea, Adina; Kandel, Mikhail E. Advanced Healthcare Materials, Vol. 5, Issue 9 https://doi.org/10.1002/adhm.201500888	journal	February 2016
3D Microperiodic Hydrogel Scaffolds for Robust Neuronal Cultures Hanson Shepherd, Jennifer N.; Parker, Sara T.; Shepherd, Robert F. Advanced Functional Materials, Vol. 21, Issue 1 https://doi.org/10.1002/adfm.201001746	journal	November 2010
New perspectives in cell adhesion: RGD and integrins Ruoslahti, E.; Pierschbacher, M. Science, Vol. 238, Issue 4826 https://doi.org/10.1126/science.2821619	journal	October 1987
Integrins Hynes, Richard O. Cell, Vol. 110, Issue 6 https://doi.org/10.1016/S0092-8674(02)00971-6	journal	September 2002
Spatial light interference microscopy (SLIM) Wang, Zhuo; Millet, Larry; Mir, Mustafa Optics Express, Vol. 19, Issue 2 https://doi.org/10.1364/OE.19.001016	journal	January 2011
Plasma membrane: rapid isolation and exposure of the cytoplasmic surface by use of positively charged beads Jacobson, B.; Branton, D. Science, Vol. 195, Issue 4275 https://doi.org/10.1126/science.831278	journal	January 1977
Interaction of basic polyamino acids with the red blood cell I. combination of polylysine with single cells Nevo, A.; De Vries, A.; Katchalsky, A. Biochimica et Biophysica Acta, Vol. 17 https://doi.org/10.1016/0006-3002(55)90416-9	journal	January 1955
Protein thiolation and reversible protein-protein conjugation. N-Succinimidyl 3-(2-pyridyldithio)propionate, a new heterobifunctional reagent Carlsson, J.; Drevin, H.; Axén, R. Biochemical Journal, Vol. 173, Issue 3 https://doi.org/10.1042/bj1730723	journal	September 1978
Indirect coating of RGD peptides using a poly-L-lysine spacer enhances jaw periosteal cell adhesion, proliferation, and differentiation into osteogenic tissue Ardjomandi, N.; Klein, C.; Kohler, K. Journal of Biomedical Materials Research Part A, Vol. 100A, Issue 8 https://doi.org/10.1002/jbm.a.34062	journal	May 2012
Quantification of α-polylysine: a comparison of four UV/Vis spectrophotometric methods Grotzky, Andrea; Manaka, Yuichi; Fornera, Sara Analytical Methods, Vol. 2, Issue 10 https://doi.org/10.1039/c0ay00116c	journal	January 2010
An Efficient Method for Dorsal Root Ganglia Neurons Purification with a One-Time Anti-Mitotic Reagent Treatment Liu, Rui; Lin, Gou; Xu, Hanpeng PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0060558	journal	April 2013
Monoclonal antibody to Thy-1 enhances regeneration of processes by rat retinal ganglion cells in culture Leifer, D.; Lipton, S.; Barnstable, C. Science, Vol. 224, Issue 4646 https://doi.org/10.1126/science.6143400	journal	April 1984
Multidimensional long-term time-lapse microscopy of in vitro peripheral nerve regeneration: Time-Lapse Recording of Nerve Regeneration Öztürk, Gürkan; Erdoǧan, Ender Microscopy Research and Technique, Vol. 64, Issue 3 https://doi.org/10.1002/jemt.20075	journal	June 2004
Synergistic hierarchical silicone-modified polysaccharide hybrid as a soft scaffold to control cell adhesion and proliferation Huang, Wei-Chen; Liu, Kun-Ho; Liu, Ta-Chung Acta Biomaterialia, Vol. 10, Issue 8 https://doi.org/10.1016/j.actbio.2014.04.025	journal	August 2014
A new chemotaxis device for cell migration studies Raja, Waseem Khan; Gligorijevic, Bojana; Wyckoff, Jeff Integrative Biology, Vol. 2, Issue 11-12 https://doi.org/10.1039/c0ib00044b	journal	January 2010
Label-free intracellular transport measured by spatial light interference microscopy Wang, Zhuo; Millet, Larry; Chan, Vincent Journal of Biomedical Optics, Vol. 16, Issue 2 https://doi.org/10.1117/1.3549204	journal	January 2011
Label-Free Imaging of Single Microtubule Dynamics Using Spatial Light Interference Microscopy Kandel, Mikhail E.; Teng, Kai Wen; Selvin, Paul R. ACS Nano, Vol. 11, Issue 1 https://doi.org/10.1021/acsnano.6b06945	journal	December 2016
Label-Free Characterization of Emerging Human Neuronal Networks Mir, Mustafa; Kim, Taewoo; Majumder, Anirban Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep04434	journal	March 2014
Dispersion-relation phase spectroscopy of intracellular transport Wang, Ru; Wang, Zhuo; Millet, Larry Optics Express, Vol. 19, Issue 21 https://doi.org/10.1364/OE.19.020571	journal	January 2011
Three‐dimensional intracellular transport in neuron bodies and neurites investigated by label‐free dispersion‐relation phase spectroscopy Kandel, Mikhail E.; Fernandes, Daniel; Taylor, Alison M. Cytometry Part A, Vol. 91, Issue 5 https://doi.org/10.1002/cyto.a.23081	journal	March 2017

Cited By (3)

3D-Printed Hydrogel Composites for Predictive Temporal (4D) Cellular Organizations and Patterned Biogenic Mineralization McCracken, Joselle M.; Rauzan, Brittany M.; Kjellman, Jacob C. E. Advanced Healthcare Materials, Vol. 8, Issue 1 https://doi.org/10.1002/adhm.201800788	journal	November 2018
Hydrogel scaffolds for tissue engineering: the importance of polymer choice Spicer, Christopher D. Polymer Chemistry, Vol. 11, Issue 2 https://doi.org/10.1039/c9py01021a	journal	January 2020
Three-dimensional mesostructures as high-temperature growth templates, electronic cellular scaffolds, and self-propelled microrobots Yan, Zheng; Han, Mengdi; Shi, Yan Proceedings of the National Academy of Sciences, Vol. 114, Issue 45 https://doi.org/10.1073/pnas.1713805114	journal	October 2017

Similar Records

Bortezomib activation of mTORC1 pathway mediated by NOX2-drived reactive oxygen species results in apoptosis in primary dorsal root ganglion neurons

Journal Article · Mon Mar 15 00:00:00 EDT 2021 · Experimental Cell Research · OSTI ID:1418567

Dong, Xiaoqing; Zuo, Yifan; Zhou, Min; +3 more

A comparison of peripheral and central axotomy effects on neurofilament and tubulin gene expression in rat dorsal root ganglion neurons

Journal Article · Sun Jul 01 00:00:00 EDT 1990 · Journal of Neuroscience; (USA) · OSTI ID:1418567

Wong, J; Oblinger, M M

beta 1 integrin inhibition dramatically enhances radiotherapy efficacy in human breast cancer xenografts

Journal Article · Mon Jun 02 00:00:00 EDT 2008 · Cancer Research · OSTI ID:1418567

Park, Catherine C; Park, Catherine C; Zhang, Hui J; +3 more

Related Subjects

36 MATERIALS SCIENCE
4D printing
biologically compliant materials
programmable cell-scaffold interactions
3D cell culture
functional soft materials
dorsal root ganglion (DRG)
gels

Title: 3D-Printed pHEMA Materials for Topographical and Biochemical Modulation of Dorsal Root Ganglion Cell Response

Citation Formats

References (80)

Cited By (3)

Similar Records

Related Subjects