Microextrusion printing cell-laden networks of type I collagen with patterned fiber alignment and geometry
Open accessPublished version of a preprint
Abstract
Type I collagen self-assembles into three-dimensional (3D) fibrous networks. These dynamic viscoelastic materials can be remodeled in response to mechanical and chemical signals to form anisotropic networks, the structure of which influences tissue development, homeostasis, and disease progression. Conventional approaches for fabricating anisotropic networks of type I collagen are often limited to unidirectional fiber alignment over small areas. Here, we describe a new approach for engineering cell-laden networks of aligned type I collagen fibers using 3D microextrusion printing of a collagen-Matrigel ink. We demonstrate hierarchical control of 3D-printed collagen with the ability to spatially pattern collagen fiber alignment and geometry. Our data suggest that collagen alignment results from a combination of molecular crowding in the ink and shear and extensional flows present during 3D printing. We demonstrate that human breast cancer cells cultured on 3D-printed collagen constructs orient along the direction of collagen fiber alignment. We also demonstrate the ability to simultaneously bioprint epithelial cell clusters and control the alignment and geometry of collagen fibers surrounding cells in the bioink. The resulting cell-laden constructs consist of epithelial cell clusters fully embedded in aligned networks of collagen fibers. Such 3D-printed constructs can be used for studies of developmental biology, tissue engineering, and regenerative medicine.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Electrospinning or 3D microextrusion printing enable production of highly aligned collagen sheets or hydrogels with spaces estimated 2-20 μm between aligned fibrils.
“Furthermore, techniques such as electrospinning or 3D microextrusion printing enable the production of highly aligned collagen sheets, or hydrogels with spaces an estimated 2-20 μm between aligned fibrils [34,35].”
From Cancer-on-chip models for metastasis: importance of the tumor microenvironment (2024) · cites this paper as [35]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Molecular Mechanisms of Stress-Responsive Changes in Collagen and Elastin Networks in Skin
Aziz, J., Shezali, H., Radzi, Z., Yahya, N. A., Abu Kassim, N. H., Czernuszka, J., & Rahman, M. T. (2016) · Skin Pharmacology and Physiology · doi:10.1159/000447017 · Cited by 7,323 · see citing works
The extracellular matrix at a glance
Frantz, C., Stewart, K. M., & Weaver, V. M. (2010) · Journal of Cell Science · doi:10.1242/jcs.023820 · Cited by 4,334 · see citing works
Collagen Structure and Stability
Shoulders, M. D., & Raines, R. T. (2009) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.77.032207.120833 · Cited by 3,923 · see citing works
BoneJ: Free and extensible bone image analysis in ImageJ
Doube, M., Kłosowski, M. M., Arganda‐Carreras, I., Cordelières, F. P., Dougherty, R. P., Jackson, J. S., Schmid, B., Hutchinson, J. R., & Shefelbine, S. J. (2010) · Bone · doi:10.1016/j.bone.2010.08.023 · Cited by 2,050 · see citing works
Hinton, T. J., Jallerat, Q., Palchesko, R. N., Park, J. H., Grodzicki, M. S., Shue, H.-J., Ramadan, M. H., Hudson, A. R., & Feinberg, A. W. (2015) · Science Advances · doi:10.1126/sciadv.1500758 · Cited by 1,805 · see citing works
Matrigel: Basement membrane matrix with biological activity
Kleinman, H. K., & Martin, G. R. (2005) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2005.05.004 · Cited by 1,673 · see citing works
3D‐Printing of Lightweight Cellular Composites
Compton, B. G., & Lewis, J. A. (2014) · Advanced Materials · doi:10.1002/adma.201401804 · Cited by 1,625 · see citing works
Aligned Collagen Is a Prognostic Signature for Survival in Human Breast Carcinoma
Conklin, M. W., Eickhoff, J. C., Riching, K. M., Pehlke, C. A., Eliceiri, K. W., Provenzano, P. P., Friedl, A., & Keely, P. J. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2010.11.076 · Cited by 1,273 · see citing works
The bioink: A comprehensive review on bioprintable materials
Hospodiuk, M., Dey, M., Sosnoski, D. M., & Ozbolat, I. T. (2017) · Biotechnology Advances · doi:10.1016/j.biotechadv.2016.12.006 · Cited by 1,139 · see citing works
Direct 3D Printing of Shear‐Thinning Hydrogels into Self‐Healing Hydrogels
Highley, C. B., Rodell, C. B., & Burdick, J. A. (2015) · Advanced Materials · doi:10.1002/adma.201501234 · Cited by 1,048 · see citing works
3D Printing of Highly Stretchable and Tough Hydrogels into Complex, Cellularized Structures
Hong, S., Sycks, D. G., Chan, H. F., Lin, S., López, G. P., Guilak, F., Leong, K. W., & Zhao, X. (2015) · Advanced Materials · doi:10.1002/adma.201501099 · Cited by 875 · see citing works
Omnidirectional Printing of 3D Microvascular Networks
Wu, W., DeConinck, A., & Lewis, J. A. (2011) · Advanced Materials · doi:10.1002/adma.201004625 · Cited by 819 · see citing works
A murine tumor producing a matrix of basement membrane.
Orkin, R. W., Gehron, P., McGoodwin, E. B., Martin, G. R., Valentine, T., & Swarm, R. L. (1977) · The Journal of Experimental Medicine · doi:10.1084/jem.145.1.204 · Cited by 633 · see citing works
Collagen fibril formation. Optimal in vitro conditions and preliminary kinetic results.
Williams, B. R., Gelman, R. A., Poppke, D. C., & Piez, K. A. (1978) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)46970-6 · Cited by 476 · see citing works
Wood, G. C., & Keech, M. K. (1960) · Biochemical Journal · doi:10.1042/bj0750588 · Cited by 443 · see citing works
Strain-Induced Alignment in Collagen Gels
Vader, D., Kabla, A., Weitz, D. A., & Mahadevan, L. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005902 · Cited by 390 · see citing works
A New 3D Printing Strategy by Harnessing Deformation, Instability, and Fracture of Viscoelastic Inks
Yuk, H., & Zhao, X. (2017) · Advanced Materials · doi:10.1002/adma.201704028 · Cited by 382 · see citing works
Oriented collagen fibers direct tumor cell intravasation
Han, W., Chen, S., Yuan, W., Fan, Q., Tian, J., Wang, X., Chen, L., Zhang, X., Wei, W., Liu, R., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1610347113 · Cited by 376 · see citing works
3D Bioprinting of Spatially Heterogeneous Collagen Constructs for Cartilage Tissue Engineering
Rhee, S., Puetzer, J. L., Mason, B. N., Reinhart‐King, C. A., & Bonassar, L. J. (2016) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.6b00288 · Cited by 367 · see citing works
Structure and Rheology Studies of Poly(oxyethylene−oxypropylene−oxyethylene) Aqueous Solution
Prud’homme, R. K., Wu, G., & Schneider, D. K. (1996) · Langmuir · doi:10.1021/la951506b · Cited by 301 · see citing works
Diamantides, N., Wang, L., Pruiksma, T., Siemiatkoski, J., Dugopolski, C., Shortkroff, S., Kennedy, S. M., & Bonassar, L. J. (2017) · Biofabrication · doi:10.1088/1758-5090/aa780f · Cited by 254 · see citing works
Magnetic alignment of collagen during self-assembly
Torbet, J., & Ronzière, M. (1984) · Biochemical Journal · doi:10.1042/bj2191057 · Cited by 244 · see citing works
Microfluidic alignment of collagen fibers for in vitro cell culture
Lee, P., Lin, R., Moon, J. J., & Lee, L. P. (2006) · Biomedical Microdevices · doi:10.1007/s10544-006-6380-z · Cited by 229 · see citing works
Unexpected Effects of Macromolecular Crowding on Protein Stability
Benton, L. A., Smith, A. E., Young, G. B., & Pielak, G. J. (2012) · Biochemistry · doi:10.1021/bi300909q · Cited by 225 · see citing works
Analysis of the size dependence of macromolecular crowding shows that smaller is better
Sharp, K. A. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1505396112 · Cited by 179 · see citing works
Sung, K. E., Su, G., Pehlke, C. A., Trier, S. M., Eliceiri, K. W., Keely, P. J., Friedl, A., & Beebe, D. J. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2009.05.043 · Cited by 160 · see citing works
Patterned Collagen Fibers Orient Branching Mammary Epithelium through Distinct Signaling Modules
Brownfield, D., Venugopalan, G., Lo, A. T., Mori, H., Tanner, K., Fletcher, D. A., & Bissell, M. J. (2013) · Current Biology · doi:10.1016/j.cub.2013.03.032 · Cited by 155 · see citing works
Development of 3D printed fibrillar collagen scaffold for tissue engineering
Nocera, A. D., Comín, R., Salvatierra, N. A., & Cid, M. P. (2018) · Biomedical Microdevices · doi:10.1007/s10544-018-0270-z · Cited by 148 · see citing works
Anguiano, M., Castilla, C., Maška, M., Ederra, C., Peláez, R., Morales, X., Muñoz-Arrieta, G., Mujika, M., Kozubek, M., Muñoz‐Barrutia, A., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0171417 · Cited by 143 · see citing works
Regulation of wound healing from a connective tissue perspective
Ehrlich, H. P., & Krummel, T. M. (1996) · Wound Repair and Regeneration · doi:10.1046/j.1524-475x.1996.40206.x · Cited by 141 · see citing works
Gjorevski, N., Piotrowski-Daspit, A. S., Varner, V. D., & Nelson, C. M. (2015) · Scientific Reports · doi:10.1038/srep11458 · Cited by 130 · see citing works
Self-citationAligned fibrillar collagen matrices obtained by shear flow deposition
Lanfer, B., Freudenberg, U., Zimmermann, R., Stamov, D. R., Körber, V., & Werner, C. (2008) · Biomaterials · doi:10.1016/j.biomaterials.2008.06.016 · Cited by 129 · see citing works
Thermodynamic studies of the assembly in vitro of native collagen fibrils
Cooper, A. J. (1970) · Biochemical Journal · doi:10.1042/bj1180355 · Cited by 110 · see citing works
Lareu, R. R., Arsianti, I., Harve, K. S., Yanxian, P., & Raghunath, M. (2007) · Tissue Engineering · doi:10.1089/ten.2006.0224 · Cited by 109 · see citing works
Molecular crowding of collagen: A pathway to produce highly-organized collagenous structures
Saeidi, N., Karmelek, K. P., Paten, J. A., Zareian, R., DiMasi, E., & Ruberti, J. W. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.06.041 · Cited by 103 · see citing works
Dynamic shear-influenced collagen self-assembly
Saeidi, N., Sander, E. A., & Ruberti, J. W. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2009.07.070 · Cited by 85 · see citing works
Aligned Nanofibrillar Collagen Regulates Endothelial Organization and Migration
Lai, E. S., Huang, N. F., Cooke, J. P., & Fuller, G. G. (2012) · Regenerative Medicine · doi:10.2217/rme.12.48 · Cited by 74 · see citing works
Collagen Fiber Orientation Regulates 3D Vascular Network Formation and Alignment
McCoy, M. G., Wei, J. M., Choi, S., Goerger, J. P., Zipfel, W. R., & Fischbach, C. (2018) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.8b00384 · Cited by 63 · see citing works
Production of highly aligned collagen lamellae by combining shear force and thin film confinement
Saeidi, N., Sander, E. A., Zareian, R., & Ruberti, J. W. (2011) · Acta Biomaterialia · doi:10.1016/j.actbio.2011.02.038 · Cited by 61 · see citing works
Visualization of Flow-Aligned Type I Collagen Self-Assembly in Tunable pH Gradients
Köster, S., Leach, J. B., Struth, B., Pfohl, T., & Wong, J. Y. (2006) · Langmuir · doi:10.1021/la062473a · Cited by 59 · see citing works
Dynamics of Tissue-Induced Alignment of Fibrous Extracellular Matrix
Piotrowski-Daspit, A. S., Nerger, B. A., Wolf, A. E., Sundaresan, S., & Nelson, C. M. (2017) · Biophysical Journal · doi:10.1016/j.bpj.2017.06.046 · Cited by 57 · see citing works
Self-citationCollagen aggregation phenomena
Cassel, J. M. (1966) · Biopolymers · doi:10.1002/bip.1966.360040904 · Cited by 54 · see citing works
Topographical guidance of 3D tumor cell migration at an interface of collagen densities
Bordeleau, F., Tang, L. N., & Reinhart‐King, C. A. (2013) · Physical Biology · doi:10.1088/1478-3975/10/6/065004 · Cited by 45 · see citing works
Generation of Spatially Aligned Collagen Fiber Networks Through Microtransfer Molding
Naik, N., Caves, J. M., Chaikof, E. L., & Allen, M. G. (2013) · Advanced Healthcare Materials · doi:10.1002/adhm.201300112 · Cited by 40 · see citing works
Pluronics as crosslinking agents for collagen: novel amphiphilic hydrogels
Homenick, C. M., de Silveira, G., Sheardown, H. D., & Adronov, A. (2010) · Polymer International · doi:10.1002/pi.2969 · Cited by 32 · see citing works
Mimicking Tissue Boundaries by Sharp Multiparameter Matrix Interfaces
Sapudom, J., Rubner, S., Martin, S., & Pompe, W. (2016) · Advanced Healthcare Materials · doi:10.1002/adhm.201600295 · Cited by 26 · see citing works
Microfabrication of Custom Collagen Structures Capable of Guiding Cell Morphology and Alignment
Kwak, E., Ahn, S., & Jaworski, J. W. (2015) · Biomacromolecules · doi:10.1021/acs.biomac.5b00295 · Cited by 18 · see citing works
Development of a Collagen/Clay Nanocomposite Biomaterial
Reyna-Valencia, A., Chevallier, P., & Mantovani, D. (2012) · Materials science forum · doi:10.4028/www.scientific.net/msf.706-709.461 · Cited by 7 · see citing works
Flagged first, then by citations
Research works printed but not linked: 4
- [7]Cassel JM, Biopolymers, 1966, 4, 989– 997.
- [25]Nicole D, Louis W, Tylar P, Joseph S, Caroline D, Sonya S, Stephen K and Lawrence JB, Biofabrication, 2017, 9, 034102.28677597
- [29]Francois B, Lauren NT and Cynthia AR-K, Physical Biology, 2013, 10, 065004.24304905
- [36]Prud’homme RK, Wu G and Schneider DK, Langmuir, 1996, 12, 4651– 4659.
Cited by
Sorted by citations
Self-Healing Injectable Hydrogels for Tissue Regeneration
Bertsch, P., Diba, M., Mooney, D. J., & Leeuwenburgh, S. C. G. (2022) · Chemical Reviews · doi:10.1021/acs.chemrev.2c00179 · Cited by 926 · see citing works
Natural Biomaterials and Their Use as Bioinks for Printing Tissues
Benwood, C., Chrenek, J., Kirsch, R. L., Masri, N. Z., Richards, H., Teetzen, K., & Willerth, S. M. (2021) · Bioengineering · doi:10.3390/bioengineering8020027 · Cited by 230 · see citing works
Ahrens, J. H., Uzel, S. G. M., Skylar‐Scott, M., Mata, M. M., Lu, A., Kroll, K. T., & Lewis, J. A. (2022) · Advanced Materials · doi:10.1002/adma.202200217 · Cited by 143 · see citing works
Design aspects and characterization of hydrogel-based bioinks for extrusion-based bioprinting
Karvinen, J., & Kellomäki, M. (2023) · Bioprinting · doi:10.1016/j.bprint.2023.e00274 · Cited by 141 · see citing works
Chen, Q., Pei, Y., Tang, K., & Albu‐Kaya, M. G. (2023) · Collagen and Leather · doi:10.1186/s42825-023-00127-5 · Cited by 124 · see citing works
Budharaju, H., Sundaramurthi, D., & Sethuraman, S. (2023) · Bioactive Materials · doi:10.1016/j.bioactmat.2023.10.012 · Cited by 116 · see citing works
Engineering Complex Anisotropic Scaffolds beyond Simply Uniaxial Alignment for Tissue Engineering
Xing, J., Liu, N., Xu, N., Chen, W., & Xing, D. (2021) · Advanced Functional Materials · doi:10.1002/adfm.202110676 · Cited by 109 · see citing works
Mechanical Roles in Formation of Oriented Collagen Fibers
Lin, J., Shi, Y., Men, Y., Wang, X., Ye, J., & Zhang, C. (2019) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2019.0243 · Cited by 98 · see citing works
Schwab, A., Hélary, C., Richards, R. G., Alini, M., Eglin, D., & D’Este, M. (2020) · Materials Today Bio · doi:10.1016/j.mtbio.2020.100058 · Cited by 97 · see citing works
Prendergast, M. E., Davidson, M. D., & Burdick, J. A. (2021) · Biofabrication · doi:10.1088/1758-5090/ac25cc · Cited by 93 · see citing works
Vernengo, J., Grad, S., Eglin, D., Alini, M., & Li, Z. (2020) · Advanced Functional Materials · doi:10.1002/adfm.201909044 · Cited by 84 · see citing works
Dewle, A., Pathak, N., Rakshasmare, P., & Srivastava, A. (2020) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.9b01225 · Cited by 83 · see citing works
Tumor-associated collagen signatures: pushing tumor boundaries
Brett, E. A., Sauter, M. A., Machens, H., & Duscher, D. (2020) · Cancer & Metabolism · doi:10.1186/s40170-020-00221-w · Cited by 80 · see citing works
Wu, Z., Xie, S., Kang, Y., Shan, X., Li, Q., & Cai, Z. (2021) · Materials Science and Engineering C · doi:10.1016/j.msec.2021.112393 · Cited by 76 · see citing works
Marangoni flows drive the alignment of fibrillar cell-laden hydrogels
Nerger, B. A., Brun, P. ‐., & Nelson, C. M. (2020) · Science Advances · doi:10.1126/sciadv.aaz7748 · Cited by 71 · see citing works
Self-citationPreparation of oriented collagen fiber scaffolds and its application in bone tissue engineering
Ma, C., Wang, H., Chi, Y., Wang, Y., Jiang, L., Xu, N., Wu, Q., Feng, Q., & Sun, X. (2020) · Applied Materials Today · doi:10.1016/j.apmt.2020.100902 · Cited by 70 · see citing works
Bakhtiari, S. S. E., Bakhsheshi‐Rad, H. R., Karbasi, S., Razzaghi, M., Tavakoli, M., Ismail, A. F., Sharif, S., Ramakrishna, S., Chen, D., & Berto, F. (2021) · Advanced Engineering Materials · doi:10.1002/adem.202100477 · Cited by 69 · see citing works
Collagen Fibril Orientation Instructs Fibroblast Differentiation Via Cell Contractility
Sapudom, J., Karaman, S., Quartey, B. C., Mohamed, W. K. E. A., Mahtani, N., Garcia‐Sabaté, A., & Teo, J. C. M. (2023) · Advanced Science · doi:10.1002/advs.202301353 · Cited by 68 · see citing works
Redmond, J., McCarthy, H. O., Buchanan, P., Levingstone, T. J., & Dunne, N. (2021) · Materials Science and Engineering C · doi:10.1016/j.msec.2021.111944 · Cited by 67 · see citing works
Current Trends on Protein Driven Bioinks for 3D Printing
Veiga, A., Silva, I. V., Duarte, M. M., & Oliveira, A. L. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13091444 · Cited by 67 · see citing works
Cancer-on-chip models for metastasis: importance of the tumor microenvironment
Jouybar, M., de Winde, C. M., Wolf, K., Friedl, P., Mebius, R. E., & den Toonder, J. M. J. (2024) · Trends in Biotechnology · doi:10.1016/j.tibtech.2023.10.001 · Cited by 66 · see citing works
Zhou, L., Wolfes, A. C., Li, Y., Chan, D. C. W., Ko, H., Szele, F. G., & Bayley, H. (2020) · Advanced Materials · doi:10.1002/adma.202002183 · Cited by 63 · see citing works
Printing Technologies as an Emerging Approach in Gas Sensors: Survey of Literature
Simonenko, N. P., Fisenko, N. A., Fedorov, F. S., Simonenko, T. L., Mokrushin, A. S., Симоненко, Е. П., Korotcenkov, G. S., Sysoev, V. V., Sevastyanov, V. G., & Kuznetsov, N. T. (2022) · Sensors · doi:10.3390/s22093473 · Cited by 60 · see citing works
Mierke, C. T. (2024) · Cells · doi:10.3390/cells13191638 · Cited by 54 · see citing works
Gao, Q., Lee, J., Kim, B. S., & Gao, G. (2022) · International Journal of Bioprinting · doi:10.18063/ijb.v9i1.638 · Cited by 52 · see citing works
Recent advancements in cardiovascular bioprinting and bioprinted cardiac constructs
Budharaju, H., Subramanian, A., & Sethuraman, S. (2021) · Biomaterials Science · doi:10.1039/d0bm01428a · Cited by 52 · see citing works
Guiding Cell Network Assembly using Shape‐Morphing Hydrogels
Viola, J. M., Porter, C. M., Gupta, A., Long, M. A., Prahl, L. S., & Hughes, A. J. (2020) · Advanced Materials · doi:10.1002/adma.202002195 · Cited by 50 · see citing works
García‐Villén, F., Ruíz, S., Lafuente‐Merchan, M., Gallego, I., Sainz-Ramos, M., del Burgo, L. S., & Pedraz, J. L. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13111806 · Cited by 48 · see citing works
Cancer-on-a-chip for precision cancer medicine
Liu, L., Wang, H., Chen, R., Song, Y., Wei, W., Baek, D. S. H., Gillin, M., Kurabayashi, K., & Chen, W. (2025) · Lab on a Chip · doi:10.1039/d4lc01043d · Cited by 47 · see citing works
Nerger, B. A., Jaslove, J. M., Elashal, H. E., Mao, S., Košmrlj, A., Link, A. J., & Nelson, C. M. (2021) · Current Biology · doi:10.1016/j.cub.2021.02.015 · Cited by 47 · see citing works
Self-citationGarcía‐Astrain, C., Henriksen‐Lacey, M., Lenzi, E., Renero‐Lecuna, C., Langer, J., Piñeiro, P., Molina-Martínez, B., Plou, J., de Aberasturi, D. J., & Liz‐Marzán, L. M. (2024) · ACS Nano · doi:10.1021/acsnano.4c00543 · Cited by 46 · see citing works
Composite Inks for Extrusion Printing of Biological and Biomedical Constructs
Ravanbakhsh, H., Bao, G., Luo, Z., Mongeau, L., & Zhang, Y. S. (2020) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.0c01158 · Cited by 45 · see citing works
Adhikari, J., Roy, A., Chanda, A., Gouripriya, D. A., Thomas, S., Ghosh, M., Kim, J., & Saha, P. (2022) · Biomaterials Science · doi:10.1039/d2bm01499h · Cited by 43 · see citing works
3D bioprinting for the repair of articular cartilage and osteochondral tissue
Chartrain, N. A., Gilchrist, K. H., Ho, V. B., & Klarmann, G. J. (2022) · Bioprinting · doi:10.1016/j.bprint.2022.e00239 · Cited by 42 · see citing works
The importance of 3D fibre architecture in cancer and implications for biomaterial model design
Ashworth, J., & Cox, T. R. (2024) · Nature reviews. Cancer · doi:10.1038/s41568-024-00704-8 · Cited by 42 · see citing works
Engineering fiber anisotropy within natural collagen hydrogels
Ahmed, A., Joshi, I. M., Mansouri, M., Ahamed, N. N. N., Hsu, M.-C., Gaborski, T. R., & Abhyankar, V. V. (2021) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00036.2021 · Cited by 41 · see citing works
Reconstruction of Muscle Fascicle‐Like Tissues by Anisotropic 3D Patterning
Jin, Y., Jeon, E. J., Jeong, S., Min, S., Choi, Y. S., Ys, K., Lee, J. S., Shin, J., Yu, J. H., Ahn, D., et al. (2021) · Advanced Functional Materials · doi:10.1002/adfm.202006227 · Cited by 41 · see citing works
Zhou, X., Ren, L., Liu, Q., Song, Z., Wu, Q., He, Y., Li, B., & Ren, L. (2021) · Macromolecular Bioscience · doi:10.1002/mabi.202100332 · Cited by 41 · see citing works
Biopolymers for Tissue Engineering: Crosslinking, Printing Techniques, and Applications
Patrocinio, D., Galván-Chacón, V., Gómez-Blanco, J. C., Miguel, S. P., Loureiro, J., Ribeiro, M. P., Coutinho, P., Pagador, J. B., & Sanchez-Margallo, F. M. (2023) · Gels · doi:10.3390/gels9110890 · Cited by 39 · see citing works
Budharaju, H., Sundaramurthi, D., & Sethuraman, S. (2023) · Biomaterials Advances · doi:10.1016/j.bioadv.2023.213486 · Cited by 38 · see citing works
Application of three-dimensional (3D) bioprinting in anti-cancer therapy
Wu, B., Wu, Z. Q., Hou, Y.-Y., Fang, Z.-X., Deng, Y., Wu, H.-T., & Liu, J. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e20475 · Cited by 37 · see citing works
Tunable Mesoscopic Collagen Island Architectures Modulate Stem Cell Behavior
Nguyen, R. Y., Cabral, A. T., Rossello‐Martinez, A., Zulli, A., Gong, X., Zhang, Q., Yan, J. Q., & Mak, M. (2023) · Advanced Materials · doi:10.1002/adma.202207882 · Cited by 36 · see citing works
Hierarchical Design of Tissue‐Mimetic Fibrillar Hydrogel Scaffolds
Pardo, A., Gómez‐Florit, M., Davidson, M. D., Öztürk-Öncel, M. Ö., Domingues, R. M. A., Burdick, J. A., & Gomes, M. E. (2024) · Advanced Healthcare Materials · doi:10.1002/adhm.202303167 · Cited by 35 · see citing works
Tunable Macroscopic Alignment of Self-Assembling Peptide Nanofibers
Farsheed, A. C., Delgado, C. Z., Yu, L. T., Saeidifard, S., Swain, J. W. R., Makhoul, J. T., Thomas, A. J., Cole, C. C., Huitron, E. I. G., Grande-Allen, K. J., et al. (2024) · ACS Nano · doi:10.1021/acsnano.4c02030 · Cited by 34 · see citing works
Three‑dimensional models to study breast cancer (Review)
Huerta‐Reyes, M., & Aguilar‐Rojas, A. (2021) · International Journal of Oncology · doi:10.3892/ijo.2021.5176 · Cited by 34 · see citing works
Alexa, R. L., Iovu, H., Trică, B., Zaharia, C., Serafim, A., Alexandrescu, E., Radu, I., Vlăsceanu, G. M., Preda, S., Ninciuleanu, C. M., et al. (2021) · Nanomaterials · doi:10.3390/nano11030703 · Cited by 34 · see citing works
Amr, M. M., Dykes, I., Counts, M., Kernan, J., Mallah, A. H., Mendenhall, J., Wie, B. V., Abu‐Lail, N. I., & Gozen, B. A. (2021) · Bioprinting · doi:10.1016/j.bprint.2021.e00133 · Cited by 31 · see citing works
Bioengineering structural anisotropy in living tissues
Mostert, D., van der Putten, C., Sahlgren, C., Kurniawan, N. A., & Bouten, C. V. C. (2025) · Nature Reviews Bioengineering · doi:10.1038/s44222-025-00338-x · Cited by 30 · see citing works
Local extensional flows promote long-range fiber alignment in 3D collagen hydrogels
Ahmed, A., Mansouri, M., Joshi, I. M., Byerley, A. M., Day, S. W., Gaborski, T. R., & Abhyankar, V. V. (2022) · Biofabrication · doi:10.1088/1758-5090/ac7824 · Cited by 27 · see citing works
Gao, Z., Liu, X., Zhao, H., Xia, S., Liu, W., Bai, H., Lv, F., Zheng, X., Huang, Y., Gu, Q., et al. (2023) · Science China Chemistry · doi:10.1007/s11426-022-1472-6 · Cited by 27 · see citing works
Stress ball morphogenesis: How the lizard builds its lung
Palmer, M. A., Nerger, B. A., Goodwin, K., Sudhakar, A., Lemke, S. B., Ravindran, P. T., Toettcher, J. E., Košmrlj, A., & Nelson, C. M. (2021) · Science Advances · doi:10.1126/sciadv.abk0161 · Cited by 25 · see citing works
Self-citationPhosphate-Functionalized Fibrous Adsorbent for Effectively Extracting Uranium from Seawater
Lin, C., Chen, J., Wu, Z., Chi, R., Lin, H., Liu, Y., Lv, Y., Ye, X., & Luo, W. (2022) · Industrial & Engineering Chemistry Research · doi:10.1021/acs.iecr.1c04355 · Cited by 25 · see citing works
Microengineering 3D Collagen Matrices with Tumor‐Mimetic Gradients in Fiber Alignment
Joshi, I. M., Mansouri, M., Ahmed, A., Silva, D. D., Simon, R. A., Esmaili, P., Desa, D. E., Elias, T. M., Brown, E. B., & Abhyankar, V. V. (2023) · Advanced Functional Materials · doi:10.1002/adfm.202308071 · Cited by 24 · see citing works
Suspension bath bioprinting and maturation of anisotropic meniscal constructs
Prendergast, M. E., Heo, S., Mauck, R. L., & Burdick, J. A. (2023) · Biofabrication · doi:10.1088/1758-5090/acc3c3 · Cited by 23 · see citing works
Schmitt, T., Kajave, N. S., Cai, H., Gu, L., Albanna, M. Z., & Kishore, V. (2020) · Journal of Biomaterials Applications · doi:10.1177/0885328220959162 · Cited by 22 · see citing works
Flores-Torres, S., Jiang, T., Kort-Mascort, J., Yang, Y. K., Peza-Chavez, O., Pal, S., Mainolfi, A., Pardo, L. A., Ferri, L. E., Bertos, N., et al. (2023) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.2c00998 · Cited by 22 · see citing works
Cheng, S., Li, Y., Yu, C., Deng, Z., Huang, J., & Zhang, Z. (2023) · Chemical Engineering Journal · doi:10.1016/j.cej.2023.146685 · Cited by 20 · see citing works
Lan, X., Adesida, A. B., & Boluk, Y. (2022) · Biomedical Materials · doi:10.1088/1748-605x/ac9b06 · Cited by 19 · see citing works
Chen, Y., Le, Y., Yang, J., Yang, Y., Feng, X., Cai, J., Shang, Y., Sugiarto, S., Wei, Q., Kai, D., et al. (2024) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.3c01636 · Cited by 19 · see citing works
Coral-Derived Collagen Fibers for Engineering Aligned Tissues
Shelah, O., Wertheimer, S., Haj-Ali, R. M., & Lesman, A. (2020) · Tissue Engineering Part A · doi:10.1089/ten.tea.2020.0116 · Cited by 19 · see citing works
Parisi, C., Qin, K., & Fernandes, F. M. (2021) · Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences · doi:10.1098/rsta.2020.0344 · Cited by 19 · see citing works
Injectable Hydrogels: A Paradigm Tailored with Design, Characterization, and Multifaceted Approaches
Singhal, R., Sarangi, M. K., & Rath, G. (2024) · Macromolecular Bioscience · doi:10.1002/mabi.202400049 · Cited by 17 · see citing works
Stress-Controlled Shear Flow Alignment of Collagen Type I Hydrogel Systems
Dedroog, L., Deschaume, O., Abrego, C. J. G., Koos, E., de Coene, Y., Vananroye, A., Thielemans, W., Bartic, C., & Lettinga, M. P. (2022) · Acta Biomaterialia · doi:10.1016/j.actbio.2022.07.008 · Cited by 16 · see citing works
Do, T., Synan, L., Ali, G., & Gappa‐Fahlenkamp, H. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-03134-1 · Cited by 16 · see citing works
Correa, S. O., Luo, X., & Raub, C. B. (2020) · Journal of Micromechanics and Microengineering · doi:10.1088/1361-6439/ab8ebf · Cited by 14 · see citing works
Development of a hyaluronic acid—collagen bioink for shear-induced fibers and cells alignment
Palladino, S., Schwab, A., Copes, F., D’Este, M., Candiani, G., & Mantovani, D. (2023) · Biomedical Materials · doi:10.1088/1748-605x/acfd77 · Cited by 13 · see citing works
Progressive Insights into 3D Bioprinting for Corneal Tissue Restoration
Namlı, İ., Gupta, D., Singh, Y. P., Datta, P., Rizwan, M., Baykara, M., & Ozbolat, I. T. (2025) · Advanced Healthcare Materials · doi:10.1002/adhm.202503372 · Cited by 13 · see citing works
Kim, D., & Kim, G. (2023) · Biofabrication · doi:10.1088/1758-5090/ace740 · Cited by 12 · see citing works
Aligned and Oriented Collagen Nanocomposite Fibers as Substrates to Activate Fibroblasts
Spiaggia, G., Taladriz‐Blanco, P., Septiadi, D., Ortuso, R. D., Lee, A., Trappe, V., Rothen‐Rutishauser, B., & Petri‐Fink, A. (2021) · ACS Applied Bio Materials · doi:10.1021/acsabm.1c00844 · Cited by 12 · see citing works
Pasquier, E., Rosendahl, J., Solberg, A., Ståhlberg, A., Håkansson, J., & Chinga‐Carrasco, G. (2023) · Bioengineering · doi:10.3390/bioengineering10060682 · Cited by 11 · see citing works
van Than, Chatelin, R., Courtial, E., Boulocher, C., & Rieger, R. (2025) · Computer Methods in Biomechanics & Biomedical Engineering · doi:10.1080/10255842.2024.2448557 · Cited by 10 · see citing works
Verma, S. K., Yaghoobi, H., Slaine, P. D., Baldwin, S. J., Rainey, J. K., Kreplak, L., & Frampton, J. P. (2022) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2022.112525 · Cited by 10 · see citing works
Lin, Y., Tsou, K.-L., Fay, C., Liu, X., Chung, J. H.-Y., Sharma, D., Jeiranikhameneh, A., Kuo, P., Tzeng, C., Wallace, G. G., et al. (2020) · Bioprinting · doi:10.1016/j.bprint.2020.e00097 · Cited by 9 · see citing works
Kim, K., Jin, S., & Shin, M. (2023) · Advanced Therapeutics · doi:10.1002/adtp.202300170 · Cited by 9 · see citing works
Bera, A. K., Rizvi, M. S., Vijayasankar, K. N., & Pati, F. (2024) · Biofabrication · doi:10.1088/1758-5090/ad86ec · Cited by 9 · see citing works
Nerger, B. A., & Nelson, C. M. (2020) · Current Opinion in Biomedical Engineering · doi:10.1016/j.cobme.2019.12.013 · Cited by 9 · see citing works
Self-citationDual-orientation of collagen fibers to guide cell alignment in 3D-printed constructs
Singhal, D., Christakopoulos, F., Brunel, L. G., Borkar, S., Doulames, V. M., Mozipo, E. A. T., Myung, D. J., Fuller, G. G., & Heilshorn, S. C. (2025) · Acta Biomaterialia · doi:10.1016/j.actbio.2025.11.013 · Cited by 8 · see citing works
Zhou, Y. L., Lian, X., Lu, Y., Zhu, Q., Fu, T., Feng, H., Lei, Q., & Huang, D. (2024) · Biomedical Materials · doi:10.1088/1748-605x/ad5244 · Cited by 8 · see citing works
Koskinen, L. M., Nieminen, L., Arjonen, A., Guzmán, C., Peurla, M., & Peuhu, E. (2024) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-024-09557-1 · Cited by 7 · see citing works
Tuning collagen and collagen-alginate mechanics through extrusion bioprinting process parameters
Hu, G., Cebrero, K. G., Venkataraman, N., Ravichandran, D., Lin, Y., Jin, Z., Gartner, Z. J., & Gu, G. X. (2025) · RSC Advances · doi:10.1039/d5ra03922c · Cited by 6 · see citing works
Step‐Ladder Bioprinting to Align Collagen Fibers for Anisotropic Tissue Fabrication
Namlı, İ., Singh, Y. P., Gupta, D., Rizvi, S. H. A., Yilmaz, Y. O., Robazzi, J. V. S., Sarıkaya, M. D., Baykara, M., & Ozbolat, I. T. (2026) · Small · doi:10.1002/smll.202510498 · Cited by 6 · see citing works
Nair, M., Inwald, E., Ives, L., See, K. R. M., & Kar‐Narayan, S. (2023) · Journal of Physics Materials · doi:10.1088/2515-7639/acca4a · Cited by 6 · see citing works
Design and Production of Customizable and Highly Aligned Fibrillar Collagen Scaffolds
Martin, C. L., Zhai, C., Paten, J. A., Yeo, J., & Deravi, L. F. (2021) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.1c00566 · Cited by 6 · see citing works
Nabavi, S. F., & Garmestani, H. (2026) · Journal of Manufacturing Processes · doi:10.1016/j.jmapro.2025.12.035 · Cited by 5 · see citing works
Recent progress of dermal implants for aged skin rejuvenation: a review
Wang, Q., Yan, H., & Xiao, J. (2025) · Journal of Materials Chemistry B · doi:10.1039/d5tb01263e · Cited by 5 · see citing works
Efficient wet-spinning of pre-aligned microtissues for 3D bioprinting complex tissue alignment
Vogt, C. D., Broomhead, J. R., Kunisaki, K. Y., Teegarden, J. M., Frett, K. L., Pacello, K. Q., Vitale, A. H., & Panoskaltsis‐Mortari, A. (2025) · Biofabrication · doi:10.1088/1758-5090/add37f · Cited by 5 · see citing works
Advancing Engineered Heart Muscle Tissue Complexity with Hydrogel Composites
Dickerson, D. A. (2022) · Advanced Biology · doi:10.1002/adbi.202200067 · Cited by 5 · see citing works
Getting the measure of living biomaterials
Gartner, Z. J., & Hughes, A. J. (2019) · Nature · doi:10.1038/d41586-019-02263-7 · Cited by 5 · see citing works
Du, Y., Li, J., Qiu, C., Shen, L. C., Li, T., Cai, B., Bo, L., & Tian, Z. (2025) · Materials Advances · doi:10.1039/d5ma00271k · Cited by 4 · see citing works
Epigenetic and Transcriptional Reprogramming in 3D Culture Models in Breast Cancer
Flores-García, L. C., Rubio, K., Ibarra-Sierra, E., Silva-Cázares, M. B., Flores, C. P., & López‐Camarillo, C. (2025) · Cancers · doi:10.3390/cancers17233830 · Cited by 4 · see citing works
Biosynthesis Application and Modification of Protein Fiber
Fazal‐ur‐Rehman, Fatima, A., Adeel, S., Qayyum, M. A., & Tanveer, H. A. (2024) · Springer eBooks · doi:10.1007/978-981-97-0684-6_11 · Cited by 4 · see citing works
Bioprinting Cell-Laden Hydrogels for Studies of Epithelial Tissue Morphogenesis
Nerger, B. A., & Nelson, C. M. (2024) · Methods in molecular biology · doi:10.1007/978-1-0716-3854-5_7 · Cited by 3 · see citing works
Self-citationMechanical Methods of Producing Biomaterials with Aligned Collagen Fibrils
Yunoki, S., Kondo, E., & Yasuda, K. (2022) · IntechOpen eBooks · doi:10.5772/intechopen.104734 · Cited by 2 · see citing works
Four-Dimensional Bioprinting: Harnessing Active Mechanics to Build with Living InksPreprint
Kim, H., Hu, G., Graham, A. J., Gu, G. X., & Gartner, Z. J. (2024) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a041557 · Cited by 2 · see citing works
Embedded cell-only bioprinting to engineer structurally aligned meniscal fibrocartilage
Karam, A., Kronemberger, G. S., Chattahy, K., Sanchez-Amador, D. E., Monaghan, M. G., & Kelly, D. J. (2026) · Materials Today Bio · doi:10.1016/j.mtbio.2026.103308 · Cited by 1 · see citing works
3D bioprinting: overview and recent developments
Kulkarni, R., & Pandya, A. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-90984-6.00007-6 · Cited by 1 · see citing works
Microengineered Breast Cancer Models: Shaping the Future of Personalized Oncology
Popoiu, T.-A., Cîmpean, A. M., Bojin, F. M., Cerbu, S., Gug, M.-C., Pirvu, C.-A., Pantea, Ș., & Neagu, A. (2025) · Cancers · doi:10.3390/cancers17193160 · Cited by 1 · see citing works
Alavije, A. A., Barati, F., Barati, M. A., Nazari, H., & Karimi, I. (2020) · Biomedical Physics & Engineering Express · doi:10.1088/2057-1976/abd67f · Cited by 1 · see citing works
Potter, M., & Richardson, W. J. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.09.049 · Cited by 1 · see citing works
Schwab, A., Hélary, C., Richards, G., Alini, M., Eglin, D., & D’Este, M. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.02.26.966564 · Cited by 1 · see citing works
- Authors
- Nerger, B. A., Brun, P.-T., & Nelson, C. M.
- Affiliations
- Princeton University (US)
- Corresponding author
- Nelson, Celeste M.
- Venue
- Soft Matter
- Publisher
- Royal Society of Chemistry (RSC)
- Published
- 2019
- Volume
- 15
- Issue
- 28
- Pages
- 5728-5738
- ISSN
- 1744-683X (ISSN-L)
- 1744-6848
- PMC
- PMC6639139
- OpenAlex
- W2954261474
- Cited by
- 111
- References
- 48
- Citations by year
- 2026: 9 · 2025: 12 · 2024: 14 · 2023: 19 · 2022: 15 · 2021: 21 · 2020: 18 · 2019: 3
- FWCI
- 5.02
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Locations
- Soft Matter (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (HL118532, HL120142, CA187692)
- National Science Foundation (CMMI-1435853)
- David and Lucile Packard Foundation
- Camille and Henry Dreyfus Foundation
- Princeton University
- Natural Sciences and Engineering Research Council of Canada
- Howard Hughes Medical Institute (55108548)
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Hydrogels: synthesis, properties, applications
- Keywords
- type I collagen, collagen fiber alignment, cell-laden constructs, breast cancer cells, macromolecular crowding, tissue engineering scaffolds, regenerative medicine
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
