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Title: Self-Repair of Structure and Bioactivity in a Supramolecular Nanostructure

Abstract

Supramolecular nanostructures formed through self-assembly can have energy landscapes, which determine their structures and functions depending on the pathways selected for their synthesis and processing and on the conditions they are exposed to after their initial formation. We report here on the structural damage that occurs in supramolecular peptide amphiphile nanostructures, during freezing in aqueous media, and the self-repair pathways that restore their functions. We found that freezing converts long supramolecular nanofibers into shorter ones, compromising their ability to support cell adhesion, but a single heating and cooling cycle reverses the damage and rescues their bioactivity. Thermal energy in this cycle enables noncovalent interactions to reconfigure the nanostructures into the thermodynamically preferred long nanofibers, a repair process that is impeded by kinetic traps. In addition, we found that nanofibers disrupted during freeze-drying also exhibit the ability to undergo thermal self-repair and recovery of their bioactivity, despite the extra disruption caused by the dehydration step. Following both freezing and freeze-drying, which shorten the 1D nanostructures, their self-repair capacity through thermally driven elongation is inhibited by kinetically trapped states, which contain highly stable noncovalent interactions that are difficult to rearrange. These states decrease the extent of thermal nanostructure repair, an observation wemore » hypothesize applies to supramolecular systems in general and is mechanistically linked to suppressed molecular exchange dynamics.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2]
  1. Northwestern Univ., Evanston, IL (United States)
  2. Northwestern Univ., Evanston, IL (United States); Northwestern Univ., Chicago, IL (United States)
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Center for Bio-Inspired Energy Science (CBES); Argonne National Lab. (ANL), Argonne, IL (United States); Northwestern Univ., Evanston, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1566549
Alternate Identifier(s):
OSTI ID: 1822210; OSTI ID: 1846775
Grant/Contract Number:  
AC02-06CH11357; SC0000989
Resource Type:
Accepted Manuscript
Journal Name:
Nano Letters
Additional Journal Information:
Journal Volume: 18; Journal Issue: 11; Journal ID: ISSN 1530-6984
Publisher:
American Chemical Society
Country of Publication:
United States
Language:
English
Subject:
36 MATERIALS SCIENCE; 99 GENERAL AND MISCELLANEOUS; 77 NANOSCIENCE AND NANOTECHNOLOGY; catalysis (homogeneous); solar (photovoltaic); bio-inspired; charge transport; mesostructured materials; materials and chemistry by design; synthesis (novel materials); synthesis (self-assembly); supramolecular nanostructures; self-assembly; self-repair; biomaterials; regenerative medicine; cell−nanostructure interactions; Nanostructures, Nanofibers, Freezing, Peptides and proteins, Viscosity; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Chen, Charlotte H., Palmer, Liam C., and Stupp, Samuel I. Self-Repair of Structure and Bioactivity in a Supramolecular Nanostructure. United States: N. p., 2018. Web. doi:10.1021/acs.nanolett.8b02709.
Chen, Charlotte H., Palmer, Liam C., & Stupp, Samuel I. Self-Repair of Structure and Bioactivity in a Supramolecular Nanostructure. United States. https://doi.org/10.1021/acs.nanolett.8b02709
Chen, Charlotte H., Palmer, Liam C., and Stupp, Samuel I. Wed . "Self-Repair of Structure and Bioactivity in a Supramolecular Nanostructure". United States. https://doi.org/10.1021/acs.nanolett.8b02709. https://www.osti.gov/servlets/purl/1566549.
@article{osti_1566549,
title = {Self-Repair of Structure and Bioactivity in a Supramolecular Nanostructure},
author = {Chen, Charlotte H. and Palmer, Liam C. and Stupp, Samuel I.},
abstractNote = {Supramolecular nanostructures formed through self-assembly can have energy landscapes, which determine their structures and functions depending on the pathways selected for their synthesis and processing and on the conditions they are exposed to after their initial formation. We report here on the structural damage that occurs in supramolecular peptide amphiphile nanostructures, during freezing in aqueous media, and the self-repair pathways that restore their functions. We found that freezing converts long supramolecular nanofibers into shorter ones, compromising their ability to support cell adhesion, but a single heating and cooling cycle reverses the damage and rescues their bioactivity. Thermal energy in this cycle enables noncovalent interactions to reconfigure the nanostructures into the thermodynamically preferred long nanofibers, a repair process that is impeded by kinetic traps. In addition, we found that nanofibers disrupted during freeze-drying also exhibit the ability to undergo thermal self-repair and recovery of their bioactivity, despite the extra disruption caused by the dehydration step. Following both freezing and freeze-drying, which shorten the 1D nanostructures, their self-repair capacity through thermally driven elongation is inhibited by kinetically trapped states, which contain highly stable noncovalent interactions that are difficult to rearrange. These states decrease the extent of thermal nanostructure repair, an observation we hypothesize applies to supramolecular systems in general and is mechanistically linked to suppressed molecular exchange dynamics.},
doi = {10.1021/acs.nanolett.8b02709},
journal = {Nano Letters},
number = 11,
volume = 18,
place = {United States},
year = {Wed Oct 31 00:00:00 EDT 2018},
month = {Wed Oct 31 00:00:00 EDT 2018}
}

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Works referenced in this record:

Gel Scaffolds of BMP-2-Binding Peptide Amphiphile Nanofibers for Spinal Arthrodesis
journal, April 2014

  • Lee, Sungsoo S.; Hsu, Erin L.; Mendoza, Marco
  • Advanced Healthcare Materials, Vol. 4, Issue 1
  • DOI: 10.1002/adhm.201400129

Microvilli and blebs as sources of reserve surface membrane during cell spreading
journal, May 1976


A bioengineered peripheral nerve construct using aligned peptide amphiphile nanofibers
journal, October 2014


Directed migration of cancer cells guided by the graded texture of the underlying matrix
journal, March 2016

  • Park, JinSeok; Kim, Deok-Ho; Kim, Hong-Nam
  • Nature Materials, Vol. 15, Issue 7
  • DOI: 10.1038/nmat4586

Nanoscale surfaces for the long-term maintenance of mesenchymal stem cell phenotype and multipotency
journal, July 2011

  • McMurray, Rebecca J.; Gadegaard, Nikolaj; Tsimbouri, P. Monica
  • Nature Materials, Vol. 10, Issue 8
  • DOI: 10.1038/nmat3058

Reversible Polymers Formed from Self-Complementary Monomers Using Quadruple Hydrogen Bonding
journal, November 1997


Multiphase design of autonomic self-healing thermoplastic elastomers
journal, April 2012

  • Chen, Yulin; Kushner, Aaron M.; Williams, Gregory A.
  • Nature Chemistry, Vol. 4, Issue 6
  • DOI: 10.1038/nchem.1314

Self-Assembly and Mineralization of Peptide-Amphiphile Nanofibers
journal, November 2001

  • Hartgerink, Jeffrey D.; Beniash, Elia; Stupp, Samuel I.
  • Science, Vol. 294, Issue 5547, p. 1684-1688
  • DOI: 10.1126/science.1063187

A Healable Supramolecular Polymer Blend Based on Aromatic π−π Stacking and Hydrogen-Bonding Interactions
journal, September 2010

  • Burattini, Stefano; Greenland, Barnaby W.; Merino, Daniel Hermida
  • Journal of the American Chemical Society, Vol. 132, Issue 34
  • DOI: 10.1021/ja104446r

Evidence of partial unfolding of proteins at the ice/freeze-concentrate interface by infrared microscopy
journal, September 2009

  • Schwegman, J. Jeff; Carpenter, John F.; Nail, Steven L.
  • Journal of Pharmaceutical Sciences, Vol. 98, Issue 9
  • DOI: 10.1002/jps.21843

A self-assembling peptide acting as an immune adjuvant
journal, December 2009

  • Rudra, J. S.; Tian, Y. F.; Jung, J. P.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 2
  • DOI: 10.1073/pnas.0912124107

Energy landscapes and functions of supramolecular systems
journal, January 2016

  • Tantakitti, Faifan; Boekhoven, Job; Wang, Xin
  • Nature Materials, Vol. 15, Issue 4
  • DOI: 10.1038/nmat4538

On the pH memory of lyophilized compounds containing protein functional groups
journal, February 1997


Water Dynamics from the Surface to the Interior of a Supramolecular Nanostructure
journal, June 2017

  • Ortony, Julia H.; Qiao, Baofu; Newcomb, Christina J.
  • Journal of the American Chemical Society, Vol. 139, Issue 26
  • DOI: 10.1021/jacs.7b02969

Simultaneous covalent and noncovalent hybrid polymerizations
journal, January 2016


Supramolecular design of self-assembling nanofibers for cartilage regeneration
journal, February 2010

  • Shah, Ramille N.; Shah, Nirav A.; Del Rosario Lim, Marc M.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 8
  • DOI: 10.1073/pnas.0906501107

Tunable Mechanics of Peptide Nanofiber Gels
journal, March 2010

  • Greenfield, Megan A.; Hoffman, Jessica R.; Olvera de la Cruz, Monica
  • Langmuir, Vol. 26, Issue 5
  • DOI: 10.1021/la9030969

Effect of cryoprotectants on the porosity and stability of insulin-loaded PLGA nanoparticles after freeze-drying
journal, October 2012

  • Fonte, Pedro; Soares, Sandra; Costa, Ana
  • Biomatter, Vol. 2, Issue 4
  • DOI: 10.4161/biom.23246

Surface topography enhances differentiation of mesenchymal stem cells towards osteogenic and adipogenic lineages
journal, August 2015


Supramolecular Assembly of Peptide Amphiphiles
journal, September 2017


Protein Stability During Freezing: Separation of Stresses and Mechanisms of Protein Stabilization
journal, January 2007

  • Bhatnagar, Bakul S.; Bogner, Robin H.; Pikal, Michael J.
  • Pharmaceutical Development and Technology, Vol. 12, Issue 5
  • DOI: 10.1080/10837450701481157

Cryobiology: The Freezing of Biological Systems
journal, May 1970


Spreading of trypsinized cells: cytoskeletal dynamics and energy requirements
journal, May 1990

  • Bereiter-Hahn, J.; Luck, M.; Miebach, T.
  • Journal of Cell Science, Vol. 96, Issue 1
  • DOI: 10.1242/jcs.96.1.171

Optically healable supramolecular polymers
journal, April 2011

  • Burnworth, Mark; Tang, Liming; Kumpfer, Justin R.
  • Nature, Vol. 472, Issue 7343, p. 334-337
  • DOI: 10.1038/nature09963

Peptide-amphiphile nanofibers: A versatile scaffold for the preparation of self-assembling materials
journal, April 2002

  • Hartgerink, J. D.; Beniash, E.; Stupp, S. I.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 8, p. 5133-5138
  • DOI: 10.1073/pnas.072699999

The triage of damaged proteins: degradation by the ubiquitin‐proteasome pathway or repair by molecular chaperones
journal, February 2006

  • Marques, Carla; Guo, Weimin; Pereira, Paulo
  • The FASEB Journal, Vol. 20, Issue 6
  • DOI: 10.1096/fj.05-5080fje

Restoration of testis function in hypogonadotropic hypogonadal mice harboring a misfolded GnRHR mutant by pharmacoperone drug therapy
journal, December 2013

  • Janovick, J. A.; Stewart, M. D.; Jacob, D.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 52
  • DOI: 10.1073/pnas.1315194110

Aligned neurite outgrowth and directed cell migration in self-assembled monodomain gels
journal, January 2014


Super-resolution microscopy reveals structural diversity in molecular exchange among peptide amphiphile nanofibres
journal, May 2016

  • da Silva, Ricardo M. P.; van der Zwaag, Daan; Albertazzi, Lorenzo
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms11561

Depolymerizable, adaptive supramolecular polymer nanoparticles and networks
journal, January 2014

  • Kaitz, Joshua A.; Possanza, Catherine M.; Song, Yang
  • Polym. Chem., Vol. 5, Issue 12
  • DOI: 10.1039/C3PY01690K

Controlling the dimensions of amyloid fibrils: Toward homogenous components for bionanotechnology
journal, November 2011

  • Domigan, Laura J.; Healy, Jackie P.; Meade, Susie J.
  • Biopolymers, Vol. 97, Issue 2
  • DOI: 10.1002/bip.21709

Injectable biomimetic liquid crystalline scaffolds enhance muscle stem cell transplantation
journal, September 2017

  • Sleep, Eduard; Cosgrove, Benjamin D.; McClendon, Mark T.
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 38
  • DOI: 10.1073/pnas.1708142114

β1-Integrin and Integrin Linked Kinase Regulate Astrocytic Differentiation of Neural Stem Cells
journal, August 2014


Blebs lead the way: how to migrate without lamellipodia
journal, July 2008

  • Charras, Guillaume; Paluch, Ewa
  • Nature Reviews Molecular Cell Biology, Vol. 9, Issue 9
  • DOI: 10.1038/nrm2453

Self-healing and thermoreversible rubber from supramolecular assembly
journal, February 2008

  • Cordier, Philippe; Tournilhac, François; Soulié-Ziakovic, Corinne
  • Nature, Vol. 451, Issue 7181, p. 977-980
  • DOI: 10.1038/nature06669

A self-assembly pathway to aligned monodomain gels
journal, June 2010

  • Zhang, Shuming; Greenfield, Megan A.; Mata, Alvaro
  • Nature Materials, Vol. 9, Issue 7
  • DOI: 10.1038/nmat2778

Volatile buffers can override the "pH memory" of subtilisin catalysis in organic media
journal, February 1999

  • Zacharis, E.; Halling, P. J.; Rees, D. G.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 4
  • DOI: 10.1073/pnas.96.4.1201

Self-Assembled Tat Nanofibers as Effective Drug Carrier and Transporter
journal, June 2013

  • Zhang, Pengcheng; Cheetham, Andrew G.; Lin, Yi-an
  • ACS Nano, Vol. 7, Issue 7
  • DOI: 10.1021/nn401667z

Pathway complexity in supramolecular polymerization
journal, January 2012

  • Korevaar, Peter A.; George, Subi J.; Markvoort, Albert J.
  • Nature, Vol. 481, Issue 7382
  • DOI: 10.1038/nature10720

Constructing the equilibrium ensemble of folding pathways from short off-equilibrium simulations
journal, November 2009

  • Noé, Frank; Schütte, Christof; Vanden-Eijnden, Eric
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 45
  • DOI: 10.1073/pnas.0905466106

Supramolecular Nanofibrils Inhibit Cancer Progression In Vitro and In Vivo
journal, February 2014


Freeze–Thaw Cycling Induced Isotropic–Nematic Coexistence of Amyloid Fibrils Suspensions
journal, March 2016


Pathway Selection in Peptide Amphiphile Assembly
journal, June 2014

  • Korevaar, Peter A.; Newcomb, Christina J.; Meijer, E. W.
  • Journal of the American Chemical Society, Vol. 136, Issue 24
  • DOI: 10.1021/ja503882s

Tuning Supramolecular Rigidity of Peptide Fibers through Molecular Structure
journal, May 2010

  • Pashuck, E. Thomas; Cui, Honggang; Stupp, Samuel I.
  • Journal of the American Chemical Society, Vol. 132, Issue 17
  • DOI: 10.1021/ja908560n

Selective Differentiation of Neural Progenitor Cells by High-Epitope Density Nanofibers
journal, February 2004

  • Silva, Gabriel A.; Czeisler, Catherine; Niece, Krista L.
  • Science, Vol. 303, Issue 5662, p. 1352-1355
  • DOI: 10.1126/science.1093783

Mechanism of the pH-Controlled Self-Assembly of Nanofibers from Peptide Amphiphiles
journal, July 2014

  • Cote, Yoann; Fu, Iris W.; Dobson, Eric T.
  • The Journal of Physical Chemistry C, Vol. 118, Issue 29
  • DOI: 10.1021/jp5048024

Works referencing / citing this record:

In Situ Self‐Assembled Nanofibers Precisely Target Cancer‐Associated Fibroblasts for Improved Tumor Imaging
journal, September 2019

  • Zhao, Xiao‐Xiao; Li, Li‐Li; Zhao, Ying
  • Angewandte Chemie, Vol. 131, Issue 43
  • DOI: 10.1002/ange.201908185

β-Galactosidase instructed supramolecular hydrogelation for selective identification and removal of senescent cells
journal, January 2019

  • Xu, Tengyan; Cai, Yanbin; Zhong, Xinglong
  • Chemical Communications, Vol. 55, Issue 50
  • DOI: 10.1039/c9cc03056e

Sequence isomerism-dependent self-assembly of glycopeptide mimetics with switchable antibiofilm properties
journal, January 2019

  • Chen, Limin; Feng, Jie; Yang, Dan
  • Chemical Science, Vol. 10, Issue 35
  • DOI: 10.1039/c9sc00193j

A self-assembling amphiphilic peptide nanoparticle for the efficient entrapment of DNA cargoes up to 100 nucleotides in length
text, January 2020


A self-assembling amphiphilic peptide nanoparticle for the efficient entrapment of DNA cargoes up to 100 nucleotides in length
journal, January 2020

  • Tarvirdipour, Shabnam; Schoenenberger, Cora-Ann; Benenson, Yaakov
  • Soft Matter, Vol. 16, Issue 6
  • DOI: 10.1039/c9sm01990a

In Situ Self‐Assembled Nanofibers Precisely Target Cancer‐Associated Fibroblasts for Improved Tumor Imaging
journal, October 2019

  • Zhao, Xiao‐Xiao; Li, Li‐Li; Zhao, Ying
  • Angewandte Chemie International Edition, Vol. 58, Issue 43
  • DOI: 10.1002/anie.201908185

A self-assembling amphiphilic peptide nanoparticle for the efficient entrapment of DNA cargoes up to 100 nucleotides in length
text, January 2020

  • Tarvirdipour, Shabnam; Schoenenberger, Cora-Ann; Benenson, Yaakov
  • Royal Society of Chemistry
  • DOI: 10.5451/unibas-ep74894