Hydrogen Bonding Stiffens Peptide Amphiphile Supramolecular Filaments by Aza-Glycine Residues

Godbe, Jacqueline M.; Freeman, Ronit; Lewis, Jacob A.; Sasselli, Ivan R.; Sangji, M. Hussain; Stupp, Samuel I.

doi:10.1016/j.actbio.2021.08.044

Title: Hydrogen Bonding Stiffens Peptide Amphiphile Supramolecular Filaments by Aza-Glycine Residues

Journal Article · Thu Sep 02 00:00:00 EDT 2021 · Acta Biomaterialia

DOI:https://doi.org/10.1016/j.actbio.2021.08.044· OSTI ID:1866091

^[1]; Freeman, Ronit ^[1];

^[1];

^[1]; Sangji, M. Hussain ^[1];

^[1]

Northwestern Univ., Evanston, IL (United States)

Peptide amphiphiles (PAs) are a class of molecules comprised of short amino acid sequences conjugated to hydrophobic moieties that may exhibit self-assembly in water into supramolecular structures. Here, we investigate here how mechanical properties of hydrogels formed by PA supramolecular nanofibers are affected by hydrogen bond densities within their internal structure by substituting glycine for aza-glycine (azaG) residues. We found that increasing the number of PA molecules that contain azaG up to 5 mol% in PA supramolecular nanofibers increases their persistence length fivefold and decreases their diffusion coefficients as measured by fluorescence recovery after photobleaching. When these PAs are used to create hydrogels, their bulk storage modulus (G') was found to increase as azaG PA content in the supramolecular assemblies increases up to a value of 10 mol% and beyond this value a decrease was observed, likely due to diminished levels of nanofiber entanglement in the hydrogels as a direct result of increased supramolecular rigidity. Interestingly, we found that the bioactivity of the scaffolds toward dopaminergic neurons derived from induced pluripotent stem cells can be enhanced directly by persistence length independently of storage modulus. We hypothesize that this is due to interactions between the cells and the extracellular environment across different size scales: from filopodia adhering to individual nanofiber bundles to cell adhesion sites that interact with the hydrogel as a bulk substrate. Fine tuning of hydrogen bond density in self-assembling peptide biomaterials such as PAs provides an approach to control nanoscale stiffness as part of an overall strategy to optimize bioactivity in these supramolecular systems. supramolecular biomaterials.

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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)

Grant/Contract Number:: SC0000989

OSTI ID:: 1866091

Alternate ID(s):: OSTI ID: 1846596

Journal Information:: Acta Biomaterialia, Vol. 135; ISSN 1742-7061

Publisher:: Acta Materialia, Inc.Copyright Statement

Country of Publication:: United States

Language:: English

References (55)

Self-assembly of peptide amphiphiles: From molecules to nanostructures to biomaterials Cui, Honggang; Webber, Matthew J.; Stupp, Samuel I. Biopolymers, Vol. 94, Issue 1, p. 1-18 https://doi.org/10.1002/bip.21328	journal	January 2010
Topography, Cell Response, and Nerve Regeneration Hoffman-Kim, Diane; Mitchel, Jennifer A.; Bellamkonda, Ravi V. Annual Review of Biomedical Engineering, Vol. 12, Issue 1 https://doi.org/10.1146/annurev-bioeng-070909-105351	journal	July 2010
Dynamic diversity of synthetic supramolecular polymers in water as revealed by hydrogen/deuterium exchange Lou, Xianwen; Lafleur, René P. M.; Leenders, Christianus M. A. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15420	journal	May 2017
Acute and chronic demyelinated CNS lesions exhibit opposite elastic properties Urbanski, Mateusz M.; Brendel, Matthew B.; Melendez-Vasquez, Carmen V. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-018-37745-7	journal	January 2019
Internal dynamics of a supramolecular nanofibre Ortony, Julia H.; Newcomb, Christina J.; Matson, John B. Nature Materials, Vol. 13, Issue 8 https://doi.org/10.1038/nmat3979	journal	May 2014
An artificial niche preserves the quiescence of muscle stem cells and enhances their therapeutic efficacy Quarta, Marco; Brett, Jamie O.; DiMarco, Rebecca Nature Biotechnology, Vol. 34, Issue 7 https://doi.org/10.1038/nbt.3576	journal	May 2016
Soft microenvironments promote the early neurogenic differentiation but not self-renewal of human pluripotent stem cells Keung, Albert J.; Asuri, Prashanth; Kumar, Sanjay Integrative Biology, Vol. 4, Issue 9 https://doi.org/10.1039/c2ib20083j	journal	August 2012
Matrix Remodeling Enhances the Differentiation Capacity of Neural Progenitor Cells in 3D Hydrogels Madl, Christopher M.; LeSavage, Bauer L.; Dewi, Ruby E. Advanced Science, Vol. 6, Issue 4 https://doi.org/10.1002/advs.201801716	journal	January 2019
Matrices with Compliance Comparable to that of Brain Tissue Select Neuronal over Glial Growth in Mixed Cortical Cultures Georges, Penelope C.; Miller, William J.; Meaney, David F. Biophysical Journal, Vol. 90, Issue 8 https://doi.org/10.1529/biophysj.105.073114	journal	April 2006
Functional Supramolecular Polymers Aida, T.; Meijer, E. W.; Stupp, S. I. Science, Vol. 335, Issue 6070 https://doi.org/10.1126/science.1205962	journal	February 2012
Hydrogen bond strength and β-sheet propensities: The role of a side chain blocking effect Bai, Yawen; Englander, S. Walter Proteins: Structure, Function, and Genetics, Vol. 18, Issue 3 https://doi.org/10.1002/prot.340180307	journal	March 1994
Cell adhesion: integrating cytoskeletal dynamics and cellular tension Parsons, J. Thomas; Horwitz, Alan Rick; Schwartz, Martin A. Nature Reviews Molecular Cell Biology, Vol. 11, Issue 9 https://doi.org/10.1038/nrm2957	journal	September 2010
The effect of hydrogel charge density on cell attachment Schneider, Galen B.; English, Anthony; Abraham, Matthew Biomaterials, Vol. 25, Issue 15 https://doi.org/10.1016/j.biomaterials.2003.09.084	journal	July 2004
Amino Acid Sequence in Constitutionally Isomeric Tetrapeptide Amphiphiles Dictates Architecture of One-Dimensional Nanostructures Cui, Honggang; Cheetham, Andrew G.; Pashuck, E. Thomas Journal of the American Chemical Society, Vol. 136, Issue 35 https://doi.org/10.1021/ja507051w	journal	August 2014
The Neutral Self-Assembling Peptide Hydrogel SPG-178 as a Topical Hemostatic Agent Komatsu, Seiji; Nagai, Yusuke; Naruse, Keiji PLoS ONE, Vol. 9, Issue 7 https://doi.org/10.1371/journal.pone.0102778	journal	July 2014
Mechanical memory and dosing influence stem cell fate Yang, Chun; Tibbitt, Mark W.; Basta, Lena Nature Materials, Vol. 13, Issue 6 https://doi.org/10.1038/nmat3889	journal	March 2014
FiberApp: An Open-Source Software for Tracking and Analyzing Polymers, Filaments, Biomacromolecules, and Fibrous Objects Usov, Ivan; Mezzenga, Raffaele Macromolecules, Vol. 48, Issue 5 https://doi.org/10.1021/ma502264c	journal	February 2015
Optimal Poly( l -lysine) Grafting Density in Hydrogels for Promoting Neural Progenitor Cell Functions Cai, Lei; Lu, Jie; Sheen, Volney Biomacromolecules, Vol. 13, Issue 5 https://doi.org/10.1021/bm300381d	journal	May 2012
General Solution for Stabilizing Triple Helical Collagen Zhang, Yitao; Herling, Madison; Chenoweth, David M. Journal of the American Chemical Society, Vol. 138, Issue 31 https://doi.org/10.1021/jacs.6b03823	journal	July 2016
Sterics and Stereoelectronics in Aza-Glycine: Impact of Aza-Glycine Preorganization in Triple Helical Collagen Harris, Trevor; Chenoweth, David M. Journal of the American Chemical Society, Vol. 141, Issue 45 https://doi.org/10.1021/jacs.9b05524	journal	October 2019
Physical properties of alginate hydrogels and their effects on in vitro follicle development West, E.; Xu, M.; Woodruff, T. Biomaterials, Vol. 28, Issue 30 https://doi.org/10.1016/j.biomaterials.2007.07.001	journal	October 2007
Gelator Length Precisely Tunes Supramolecular Hydrogel Stiffness and Neuronal Phenotype in 3D Culture Godbe, Jacqueline M.; Freeman, Ronit; Burbulla, Lena F. ACS Biomaterials Science & Engineering, Vol. 6, Issue 2 https://doi.org/10.1021/acsbiomaterials.9b01585	journal	January 2020
Peptide- and collagen-based hydrogel substrates for in vitro culture of chick cochleae Spencer, Nathaniel J.; Cotanche, Douglas A.; Klapperich, Catherine M. Biomaterials, Vol. 29, Issue 8 https://doi.org/10.1016/j.biomaterials.2007.11.006	journal	March 2008
MicroRNA-21 preserves the fibrotic mechanical memory of mesenchymal stem cells Li, Chen Xi; Talele, Nilesh P.; Boo, Stellar Nature Materials, Vol. 16, Issue 3 https://doi.org/10.1038/nmat4780	journal	October 2016
Intermolecular Forces in the Self-Assembly of Peptide Amphiphile Nanofibers Stendahl, J. C.; Rao, M. S.; Guler, M. O. Advanced Functional Materials, Vol. 16, Issue 4 https://doi.org/10.1002/adfm.200500161	journal	March 2006
A protocol for rheological characterization of hydrogels for tissue engineering strategies: A Protocol for Rheological Characterization of Hydrogels Zuidema, Jonathan M.; Rivet, Christopher J.; Gilbert, Ryan J. Journal of Biomedical Materials Research Part B: Applied Biomaterials, Vol. 102, Issue 5 https://doi.org/10.1002/jbm.b.33088	journal	December 2013
Self-Assembly of Peptide−Amphiphile Nanofibers: The Roles of Hydrogen Bonding and Amphiphilic Packing Paramonov, Sergey E.; Jun, Ho-Wook; Hartgerink, Jeffrey D. Journal of the American Chemical Society, Vol. 128, Issue 22 https://doi.org/10.1021/ja060573x	journal	June 2006
The elastic modulus of Matrigel™ as determined by atomic force microscopy Soofi, Shauheen S.; Last, Julie A.; Liliensiek, Sara J. Journal of Structural Biology, Vol. 167, Issue 3 https://doi.org/10.1016/j.jsb.2009.05.005	journal	September 2009
Aza-Glycine Induces Collagen Hyperstability Zhang, Yitao; Malamakal, Roy M.; Chenoweth, David M. Journal of the American Chemical Society, Vol. 137, Issue 39 https://doi.org/10.1021/jacs.5b04590	journal	September 2015
Hydrogels with tunable stress relaxation regulate stem cell fate and activity Chaudhuri, Ovijit; Gu, Luo; Klumpers, Darinka Nature Materials, Vol. 15, Issue 3 https://doi.org/10.1038/nmat4489	journal	November 2015
Stabilization of Azapeptides by N _amide ···H–N _amide Hydrogen Bonds Baruah, Kalpita; Sahariah, Biswajit; Sakpal, Sushil S. Organic Letters, Vol. 23, Issue 13 https://doi.org/10.1021/acs.orglett.1c01111	journal	June 2021
Calcium Ions to Cross-Link Supramolecular Nanofibers to Tune the Elasticity of Hydrogels over Orders of Magnitude Shi, Junfeng; Gao, Yuan; Zhang, Ye Langmuir, Vol. 27, Issue 23 https://doi.org/10.1021/la2033862	journal	November 2011
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
Layers and Multilayers of Self-Assembled Polymers: Tunable Engineered Extracellular Matrix Coatings for Neural Cell Growth Landry, Michael J.; Rollet, Frédéric-Guillaume; Kennedy, Timothy E. Langmuir, Vol. 34, Issue 30 https://doi.org/10.1021/acs.langmuir.7b04108	journal	February 2018
Shear thickening (dilatancy) in concentrated dispersions: Shear Thickening (Dilatancy) in Concentrated Dispersions Boersma, Willem H.; Laven, Jozua; Stein, Hans N. AIChE Journal, Vol. 36, Issue 3 https://doi.org/10.1002/aic.690360302	journal	March 1990
Type I collagen, fibrin and PuraMatrix matrices provide permissive environments for human endothelial and mesenchymal progenitor cells to form neovascular networks Allen, Patrick; Melero-Martin, Juan; Bischoff, Joyce Journal of Tissue Engineering and Regenerative Medicine, Vol. 5, Issue 4 https://doi.org/10.1002/term.389	journal	January 2011
Maintenance of neural progenitor cell stemness in 3D hydrogels requires matrix remodelling Madl, Christopher M.; LeSavage, Bauer L.; Dewi, Ruby E. Nature Materials, Vol. 16, Issue 12 https://doi.org/10.1038/nmat5020	journal	October 2017
A photo-modulatable material for probing cellular responses to substrate rigidity Frey, Margo T.; Wang, Yu-li Soft Matter, Vol. 5, Issue 9 https://doi.org/10.1039/b818104g	journal	January 2009
Mechanical confinement regulates cartilage matrix formation by chondrocytes Lee, Hong-pyo; Gu, Luo; Mooney, David J. Nature Materials, Vol. 16, Issue 12 https://doi.org/10.1038/nmat4993	journal	October 2017
An active-site titrant for chymotrypsin, and evidence that azapeptide esters are less susceptible to nucleophilic attack than ordinary esters Gassman, Jill M.; Magrath, Joe Bioorganic & Medicinal Chemistry Letters, Vol. 6, Issue 15 https://doi.org/10.1016/0960-894X(96)00308-3	journal	August 1996
Tuning supramolecular mechanics to guide neuron development Sur, Shantanu; Newcomb, Christina J.; Webber, Matthew J. Biomaterials, Vol. 34, Issue 20 https://doi.org/10.1016/j.biomaterials.2013.03.025	journal	July 2013
Structural Basis for Aza-Glycine Stabilization of Collagen Kasznel, Alexander J.; Zhang, Yitao; Hai, Yang Journal of the American Chemical Society, Vol. 139, Issue 28 https://doi.org/10.1021/jacs.7b03398	journal	July 2017
Hippo/YAP-mediated rigidity-dependent motor neuron differentiation of human pluripotent stem cells Sun, Yubing; Yong, Koh Meng Aw; Villa-Diaz, Luis G. Nature Materials, Vol. 13, Issue 6 https://doi.org/10.1038/nmat3945	journal	April 2014
Towards a general synthesis of di-aza-amino acids containing peptides Bizet, Faustine; Tonali, Nicolo; Soulier, Jean-Louis New Journal of Chemistry, Vol. 42, Issue 20 https://doi.org/10.1039/C8NJ03635G	journal	January 2018
Shear‐Thickening (“Dilatancy”) in Suspensions of Nonaggregating Solid Particles Dispersed in Newtonian Liquids Barnes, H. A. Journal of Rheology, Vol. 33, Issue 2 https://doi.org/10.1122/1.550017	journal	February 1989
Azapeptide Synthesis Methods for Expanding Side-Chain Diversity for Biomedical Applications Chingle, Ramesh; Proulx, Caroline; Lubell, William D. Accounts of Chemical Research, Vol. 50, Issue 7 https://doi.org/10.1021/acs.accounts.7b00114	journal	June 2017
The combined effects of matrix stiffness and growth factor immobilization on the bioactivity and differentiation capabilities of adipose-derived stem cells Banks, Jessica M.; Mozdzen, Laura C.; Harley, Brendan A. C. Biomaterials, Vol. 35, Issue 32 https://doi.org/10.1016/j.biomaterials.2014.07.012	journal	October 2014
Toward Assessing the Position-Dependent Contributions of Backbone Hydrogen Bonding to β-Sheet Folding Thermodynamics Employing Amide-to-Ester Perturbations Deechongkit, Songpon; Dawson, Philip E.; Kelly, Jeffery W. Journal of the American Chemical Society, Vol. 126, Issue 51 https://doi.org/10.1021/ja045934s	journal	December 2004
Supramolecular Exchange among Assemblies of Opposite Charge Leads to Hierarchical Structures Wester, James R.; Lewis, Jacob A.; Freeman, Ronit Journal of the American Chemical Society, Vol. 142, Issue 28 https://doi.org/10.1021/jacs.0c03529	journal	June 2020
Stress-stiffening-mediated stem-cell commitment switch in soft responsive hydrogels Das, Rajat K.; Gocheva, Veronika; Hammink, Roel Nature Materials, Vol. 15, Issue 3 https://doi.org/10.1038/nmat4483	journal	November 2015
Tuning Supramolecular Rigidity of Peptide Fibers through Molecular Structure Pashuck, E. Thomas; Cui, Honggang; Stupp, Samuel I. Journal of the American Chemical Society, Vol. 132, Issue 17 https://doi.org/10.1021/ja908560n	journal	May 2010
Effect of filament diameter and extracellular matrix molecule precoating on neurite outgrowth and Schwann cell behavior on multifilament entubulation bridging devicein vitro Wen, Xuejun; Tresco, Patrick A. Journal of Biomedical Materials Research Part A, Vol. 76A, Issue 3 https://doi.org/10.1002/jbm.a.30520	journal	March 2006
Hydrogel Modulus Affects Proliferation Rate and Pluripotency of Human Mesenchymal Stem Cells Grown in Three-Dimensional Culture Goldshmid, Revital; Seliktar, Dror ACS Biomaterials Science & Engineering, Vol. 3, Issue 12 https://doi.org/10.1021/acsbiomaterials.7b00266	journal	November 2017
Tuning the Range of Polyacrylamide Gel Stiffness for Mechanobiology Applications Denisin, Aleksandra K.; Pruitt, Beth L. ACS Applied Materials & Interfaces, Vol. 8, Issue 34 https://doi.org/10.1021/acsami.5b09344	journal	January 2016
Reversible self-assembly of superstructured networks Freeman, Ronit; Han, Ming; Álvarez, Zaida Science, Vol. 362, Issue 6416 https://doi.org/10.1126/science.aat6141	journal	October 2018

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36 MATERIALS SCIENCE
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
aza-Glycine
hydrogen bonding
nanofibers
peptide amphiphiles
β-sheet
99 GENERAL AND MISCELLANEOUS
Aza-Glycine

Title: Hydrogen Bonding Stiffens Peptide Amphiphile Supramolecular Filaments by Aza-Glycine Residues

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