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Shape-Shifting Peptide Nanomaterials: Surface Asymmetry Enables pH-Dependent Formation and Interconversion of Collagen Tubes and Sheets

  • Andrea D. Merg
    Andrea D. Merg
    Department of Chemistry, Emory University, Atlanta, Georgia 30322, United States
  • Gavin Touponse
    Gavin Touponse
    Department of Chemistry, Emory University, Atlanta, Georgia 30322, United States
  • Eric van Genderen
    Eric van Genderen
    Paul Scherrer Institut, CH-5232 Villigen, Switzerland
  • Thorsten B. Blum
    Thorsten B. Blum
    Paul Scherrer Institut, CH-5232 Villigen, Switzerland
  • Xiaobing Zuo
    Xiaobing Zuo
    X-ray Science Division, Argonne National Laboratory, Lemont, Illinois 60439, United States
    More by Xiaobing Zuo
  • Alisina Bazrafshan
    Alisina Bazrafshan
    Department of Chemistry, Emory University, Atlanta, Georgia 30322, United States
  • Hew Ming Helen Siaw
    Hew Ming Helen Siaw
    Department of Chemistry, Emory University, Atlanta, Georgia 30322, United States
  • Arthur McCanna
    Arthur McCanna
    The Robert P. Apkarian Integrated Electron Microscopy Core, Emory University, Atlanta, Georgia 30322, United States
  • R. Brian Dyer
    R. Brian Dyer
    Department of Chemistry, Emory University, Atlanta, Georgia 30322, United States
  • Khalid Salaita
    Khalid Salaita
    Department of Chemistry, Emory University, Atlanta, Georgia 30322, United States
  • Jan Pieter Abrahams
    Jan Pieter Abrahams
    Paul Scherrer Institut, CH-5232 Villigen, Switzerland
    Center for Cellular Imaging and NanoAnalytics, Biozentrum, University of Basel, CH-4058 Basel, Switzerland
  • , and 
  • Vincent P. Conticello*
    Vincent P. Conticello
    Department of Chemistry, Emory University, Atlanta, Georgia 30322, United States
    *Email: [email protected]
Cite this: J. Am. Chem. Soc. 2020, 142, 47, 19956–19968
Publication Date (Web):November 10, 2020
https://doi.org/10.1021/jacs.0c08174
Copyright © 2020 American Chemical Society

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    Abstract

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    The fabrication of dynamic, transformable biomaterials that respond to environmental cues represents a significant step forward in the development of synthetic materials that rival their highly functional, natural counterparts. Here, we describe the design and synthesis of crystalline supramolecular architectures from charge-complementary heteromeric pairs of collagen-mimetic peptides (CMPs). Under appropriate conditions, CMP pairs spontaneously assemble into either 1D ultraporous (pore diameter >100 nm) tubes or 2D bilayer nanosheets due to the structural asymmetry that arises from heteromeric self-association. Crystalline collagen tubes represent a heretofore unobserved morphology of this common biomaterial. In-depth structural characterization from a suite of biophysical methods, including TEM, AFM, high-resolution cryo-EM, and SAXS/WAXS measurements, reveals that the sheet and tube assemblies possess a similar underlying lattice structure. The experimental evidence suggests that the tubular structures are a consequence of the self-scrolling of incipient 2D layers of collagen triple helices and that the scrolling direction determines the formation of two distinct structural isoforms. Furthermore, we show that nanosheets and tubes can spontaneously interconvert through manipulation of the assembly pH and systematic adjustment of the CMP sequence. Altogether, we establish initial guidelines for the construction of dynamically responsive 1D and 2D assemblies that undergo a structurally programmed morphological transition.

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