Reversible self-assembly of superstructured networks

Freeman, Ronit; Han, Ming; Álvarez, Zaida; Lewis, Jacob A.; Wester, James R.; Stephanopoulos, Nicholas; McClendon, Mark T.; Lynsky, Cheyenne; Godbe, Jacqueline M.; Sangji, Hussain; Luijten, Erik; Stupp, Samuel I.

doi:10.1126/science.aat6141

Reversible self-assembly of superstructured networks

Journal Article · 04 October 2018 · Science

DOI:https://doi.org/10.1126/science.aat6141· OSTI ID:1566718

; Han, Ming; Álvarez, Zaida; ; ; ; McClendon, Mark T.; ; ; ; ;

Soft structures in nature, such as protein assemblies, can organize reversibly into functional and often hierarchical architectures through noncovalent interactions. Molecularly encoding this dynamic capability in synthetic materials has remained an elusive goal. We report on hydrogels of peptide-DNA conjugates and peptides that organize into superstructures of intertwined filaments that disassemble upon the addition of molecules or changes in charge density. Experiments and simulations demonstrate that this response requires large-scale spatial redistribution of molecules directed by strong noncovalent interactions among them. Simulations also suggest that the chemically reversible structures can only occur within a limited range of supramolecular cohesive energies. Storage moduli of the hydrogels change reversibly as superstructures form and disappear, as does the phenotype of neural cells in contact with these materials.

Research Organization:: Energy Frontier Research Centers (EFRC) (United States). Center for Bio-Inspired Energy Science (CBES); Northwestern Univ., Evanston, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

DOE Contract Number:: FG02-00ER45810; SC0000989

OSTI ID:: 1566718

Journal Information:: Science, Vol. 362, Issue 6416; ISSN 0036-8075

Publisher:: AAAS

Country of Publication:: United States

Language:: English

References (36)

Enzyme-Free Nucleic Acid Logic Circuits Seelig, G.; Soloveichik, D.; Zhang, D. Y. Science, Vol. 314, Issue 5805 https://doi.org/10.1126/science.1132493	journal	December 2006
Actin Binding Proteins: Regulation of Cytoskeletal Microfilaments Dos Remedios, C. G.; Chhabra, D.; Kekic, M. Physiological Reviews, Vol. 83, Issue 2 https://doi.org/10.1152/physrev.00026.2002	journal	April 2003
The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors Ridley, Anne J.; Hall, Alan Cell, Vol. 70, Issue 3 https://doi.org/10.1016/0092-8674(92)90163-7	journal	August 1992
Astrocyte cell lineage. V. Similarity of astrocytes that form in the presence of dBcAMP in cultures to reactive astrocytes in vivo Fedoroff, S.; McAuley, W. A. J.; Houkle, J. D. Journal of Neuroscience Research, Vol. 12, Issue 1 https://doi.org/10.1002/jnr.490120103	journal	January 1984
Multidimensional hierarchical self-assembly of amphiphilic cylindrical block comicelles Qiu, H.; Hudson, Z. M.; Winnik, M. A. Science, Vol. 347, Issue 6228 https://doi.org/10.1126/science.1261816	journal	March 2015
Molecular assembly and mechanical properties of the extracellular matrix: A fibrous protein perspective Muiznieks, Lisa D.; Keeley, Fred W. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Vol. 1832, Issue 7 https://doi.org/10.1016/j.bbadis.2012.11.022	journal	July 2013
Atomistic Molecular Dynamics Simulations of Peptide Amphiphile Self-Assembly into Cylindrical Nanofibers Lee, One-Sun; Stupp, Samuel I.; Schatz, George C. Journal of the American Chemical Society, Vol. 133, Issue 10 https://doi.org/10.1021/ja110966y	journal	March 2011
Glial Tissue Mechanics and Mechanosensing by Glial Cells Pogoda, Katarzyna; Janmey, Paul A. Frontiers in Cellular Neuroscience, Vol. 12 https://doi.org/10.3389/fncel.2018.00025	journal	February 2018
The MARTINI Coarse-Grained Force Field: Extension to Proteins Monticelli, Luca; Kandasamy, Senthil K.; Periole, Xavier Journal of Chemical Theory and Computation, Vol. 4, Issue 5 https://doi.org/10.1021/ct700324x	journal	April 2008
Cell culture models for reactive gliosis: New perspectives Wu, Vivian W.; Schwartz, Joan P. Journal of Neuroscience Research, Vol. 51, Issue 6 https://doi.org/10.1002/(SICI)1097-4547(19980315)51:6<675::AID-JNR2>3.0.CO;2-8	journal	March 1998
The effect of the composition of PLA films and lactate release on glial and neuronal maturation and the maintenance of the neuronal progenitor niche Álvarez, Zaida; Mateos-Timoneda, Miguel A.; Hyroššová, Petra Biomaterials, Vol. 34, Issue 9 https://doi.org/10.1016/j.biomaterials.2012.12.001	journal	March 2013
The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors Ridley, A. J.; Hall, A. Trends in Cell Biology, Vol. 2, Issue 11 https://doi.org/10.1016/0962-8924(92)90173-k	journal	November 1992
Self-Assembly at All Scales Whitesides, George M.; Grzybowski, Bartosz Science, Vol. 295, Issue 5564, p. 2418-2421 https://doi.org/10.1126/science.1070821	journal	March 2002
Multi-hierarchical self-assembly of a collagen mimetic peptide from triple helix to nanofibre and hydrogel O'Leary, Lesley E. R.; Fallas, Jorge A.; Bakota, Erica L. Nature Chemistry, Vol. 3, Issue 10 https://doi.org/10.1038/nchem.1123	journal	August 2011
Active matter at the interface between materials science and cell biology Needleman, Daniel; Dogic, Zvonimir Nature Reviews Materials, Vol. 2, Issue 9 https://doi.org/10.1038/natrevmats.2017.48	journal	July 2017
Hierarchical self-assembly of chiral rod-like molecules as a model for peptide -sheet tapes, ribbons, fibrils, and fibers Aggeli, A.; Nyrkova, I. A.; Bell, M. Proceedings of the National Academy of Sciences, Vol. 98, Issue 21 https://doi.org/10.1073/pnas.191250198	journal	October 2001
Structural Remodeling of Astrocytes in the Injured CNS Sun, Daniel; Jakobs, Tatjana C. The Neuroscientist, Vol. 18, Issue 6 https://doi.org/10.1177/1073858411423441	journal	October 2011
Amino-acid-encoded biocatalytic self-assembly enables the formation of transient conducting nanostructures Kumar, Mohit; Ing, Nicole L.; Narang, Vishal Nature Chemistry, Vol. 10, Issue 7 https://doi.org/10.1038/s41557-018-0047-2	journal	April 2018
Extracellular matrix dynamics in development and regenerative medicine Daley, W. P.; Peters, S. B.; Larsen, M. Journal of Cell Science, Vol. 121, Issue 3 https://doi.org/10.1242/jcs.006064	journal	January 2008
Inducing functional radial glia-like progenitors from cortical astrocyte cultures using micropatterned PMMA Mattotti, Marta; Alvarez, Zaida; Ortega, Juan A. Biomaterials, Vol. 33, Issue 6 https://doi.org/10.1016/j.biomaterials.2011.10.086	journal	February 2012
Modeling the Self-Assembly of Peptide Amphiphiles into Fibers Using Coarse-Grained Molecular Dynamics Lee, One-Sun; Cho, Vince; Schatz, George C. Nano Letters, Vol. 12, Issue 9 https://doi.org/10.1021/nl302487m	journal	January 2012
Super-resolution microscopy reveals structural diversity in molecular exchange among peptide amphiphile nanofibres da Silva, Ricardo M. P.; van der Zwaag, Daan; Albertazzi, Lorenzo Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11561	journal	May 2016
Remodelling the extracellular matrix in development and disease Bonnans, Caroline; Chou, Jonathan; Werb, Zena Nature Reviews Molecular Cell Biology, Vol. 15, Issue 12 https://doi.org/10.1038/nrm3904	journal	November 2014
Fabrication of novel biomaterials through molecular self-assembly Zhang, Shuguang Nature Biotechnology, Vol. 21, Issue 10 https://doi.org/10.1038/nbt874	journal	September 2003
Thermally Active Hybridization Drives the Crystallization of DNA-Functionalized Nanoparticles Li, Ting I. N. G.; Sknepnek, Rastko; Olvera de la Cruz, Monica Journal of the American Chemical Society, Vol. 135, Issue 23 https://doi.org/10.1021/ja312644h	journal	May 2013
A self-assembly pathway to aligned monodomain gels Zhang, Shuming; Greenfield, Megan A.; Mata, Alvaro Nature Materials, Vol. 9, Issue 7 https://doi.org/10.1038/nmat2778	journal	June 2010
The soft mechanical signature of glial scars in the central nervous system Moeendarbary, E.; Weber, Ip; Sheridan, Gk Nature Publishing Group https://doi.org/10.17863/cam.9109	journalarticle	January 2017
The MARTINI Force Field: Coarse Grained Model for Biomolecular Simulations Marrink, Siewert J.; Risselada, H. Jelger; Yefimov, Serge The Journal of Physical Chemistry B, Vol. 111, Issue 27 https://doi.org/10.1021/jp071097f	journal	July 2007
The stem cell potential of glia: lessons from reactive gliosis Robel, Stefanie; Berninger, Benedikt; Götz, Magdalena Nature Reviews Neuroscience, Vol. 12, Issue 2 https://doi.org/10.1038/nrn2978	journal	January 2011
OligoCalc: an online oligonucleotide properties calculator Kibbe, W. A. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm234	journal	May 2007
Transmutable nanoparticles with reconfigurable surface ligands Kim, Y.; Macfarlane, R. J.; Jones, M. R. Science, Vol. 351, Issue 6273 https://doi.org/10.1126/science.aad2212	journal	February 2016
Reactive Astrocytes: Production, Function, and Therapeutic Potential Liddelow, Shane A.; Barres, Ben A. Immunity, Vol. 46, Issue 6 https://doi.org/10.1016/j.immuni.2017.06.006	journal	June 2017
The soft mechanical signature of glial scars in the central nervous system Moeendarbary, Emad; Weber, Isabell P.; Sheridan, Graham K. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14787	journal	March 2017
Self-Assembly of Large and Small Molecules into Hierarchically Ordered Sacs and Membranes Capito, R. M.; Azevedo, H. S.; Velichko, Y. S. Science, Vol. 319, Issue 5871, p. 1812-1816 https://doi.org/10.1126/science.1154586	journal	March 2008
Interaction of reactive astrocytes with type I collagen induces astrocytic scar formation through the integrin–N-cadherin pathway after spinal cord injury Hara, Masamitsu; Kobayakawa, Kazu; Ohkawa, Yasuyuki Nature Medicine, Vol. 23, Issue 7 https://doi.org/10.1038/nm.4354	journal	June 2017
Reactive Oxygen Species from Human Astrocytes Induced Functional Impairment and Oxidative Damage Sheng, Wen S.; Hu, Shuxian; Feng, Amy Neurochemical Research, Vol. 38, Issue 10 https://doi.org/10.1007/s11064-013-1123-z	journal	August 2013

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Functionalized DNA nanostructures as scaffolds for guided mineralization Kim, Francesca; Chen, Tong; Burgess, Trevor Chemical Science, Vol. 10, Issue 45 https://doi.org/10.1039/c9sc02811k	journal	January 2019
The Ultrafast Assembly of a Dipeptide Supramolecular Organogel and its Phase Transition from Gel to Crystal Yuan, Tingting; Xu, Youqian; Fei, Jinbo Angewandte Chemie International Edition, Vol. 58, Issue 32 https://doi.org/10.1002/anie.201903829	journal	July 2019
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Helical antimicrobial peptides assemble into protofibril scaffolds that present ordered dsDNA to TLR9 Lee, Ernest Y.; Zhang, Changsheng; Di Domizio, Jeremy Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08868-w	journal	March 2019
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Hierarchically oriented organization in supramolecular peptide crystals Yuan, Chengqian; Ji, Wei; Xing, Ruirui Nature Reviews Chemistry, Vol. 3, Issue 10 https://doi.org/10.1038/s41570-019-0129-8	journal	September 2019
Designing stable, hierarchical peptide fibers from block co-polypeptide sequences van Rijt, Mark M. J.; Ciaffoni, Adriano; Ianiro, Alessandro Chemical Science, Vol. 10, Issue 39 https://doi.org/10.1039/c9sc00800d	journal	January 2019
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