skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Conformations of peptoids in nanosheets result from the interplay of backbone energetics and intermolecular interactions

Abstract

The conformations adopted by the molecular constituents of a supramolecular assembly influence its large-scale order. At the same time, the interactions made in assemblies by molecules can influence their conformations. Here we study this interplay in extended flat nanosheets made from nonnatural sequence-specific peptoid polymers. Nanosheets exist because individual polymers can be linear and untwisted, by virtue of polymer backbone elements adopting alternating rotational states whose twists oppose and cancel. Using molecular dynamics and quantum mechanical simulations, together with experimental data, we explore the design space of flat nanostructures built from peptoids. We show that several sets of peptoid backbone conformations are consistent with their being linear, but the specific combination observed in experiment is determined by a combination of backbone energetics and the interactions made within the nanosheet. Our results provide a molecular model of the peptoid nanosheet consistent with all available experimental data and show that its structure results from a combination of intra- and intermolecular interactions.

Authors:
; ORCiD logo; ; ; ; ORCiD logo; ;
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1437093
Alternate Identifier(s):
OSTI ID: 1506309
Grant/Contract Number:  
AC02-05CH11231; DTRA10027-1587
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 115 Journal Issue: 22; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
36 MATERIALS SCIENCE; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Edison, John R., Spencer, Ryan K., Butterfoss, Glenn L., Hudson, Benjamin C., Hochbaum, Allon I., Paravastu, Anant K., Zuckermann, Ronald N., and Whitelam, Stephen. Conformations of peptoids in nanosheets result from the interplay of backbone energetics and intermolecular interactions. United States: N. p., 2018. Web. doi:10.1073/pnas.1800397115.
Edison, John R., Spencer, Ryan K., Butterfoss, Glenn L., Hudson, Benjamin C., Hochbaum, Allon I., Paravastu, Anant K., Zuckermann, Ronald N., & Whitelam, Stephen. Conformations of peptoids in nanosheets result from the interplay of backbone energetics and intermolecular interactions. United States. doi:10.1073/pnas.1800397115.
Edison, John R., Spencer, Ryan K., Butterfoss, Glenn L., Hudson, Benjamin C., Hochbaum, Allon I., Paravastu, Anant K., Zuckermann, Ronald N., and Whitelam, Stephen. Mon . "Conformations of peptoids in nanosheets result from the interplay of backbone energetics and intermolecular interactions". United States. doi:10.1073/pnas.1800397115.
@article{osti_1437093,
title = {Conformations of peptoids in nanosheets result from the interplay of backbone energetics and intermolecular interactions},
author = {Edison, John R. and Spencer, Ryan K. and Butterfoss, Glenn L. and Hudson, Benjamin C. and Hochbaum, Allon I. and Paravastu, Anant K. and Zuckermann, Ronald N. and Whitelam, Stephen},
abstractNote = {The conformations adopted by the molecular constituents of a supramolecular assembly influence its large-scale order. At the same time, the interactions made in assemblies by molecules can influence their conformations. Here we study this interplay in extended flat nanosheets made from nonnatural sequence-specific peptoid polymers. Nanosheets exist because individual polymers can be linear and untwisted, by virtue of polymer backbone elements adopting alternating rotational states whose twists oppose and cancel. Using molecular dynamics and quantum mechanical simulations, together with experimental data, we explore the design space of flat nanostructures built from peptoids. We show that several sets of peptoid backbone conformations are consistent with their being linear, but the specific combination observed in experiment is determined by a combination of backbone energetics and the interactions made within the nanosheet. Our results provide a molecular model of the peptoid nanosheet consistent with all available experimental data and show that its structure results from a combination of intra- and intermolecular interactions.},
doi = {10.1073/pnas.1800397115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 22,
volume = 115,
place = {United States},
year = {2018},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1073/pnas.1800397115

Citation Metrics:
Cited by: 9 works
Citation information provided by
Web of Science

Figures / Tables:

Fig. 1. Fig. 1. : The trans-peptoid backbone is disposed toward linearity, but the form observed in nanosheets is cis. (A and B) Schematic of a trans- (A) and cis- (B) peptoid backbone showing the dihedral angles of two adjacent residues, i and i + 1. (C and D) Linearity (actual lengthmore » divided by maximum possible length) $L$ of an eight-residue trans-polysarcosine (C) and cis-polysarcosine (D) as a function of backbone dihedral angles Φi and Ψi . Here the dihedral angles of successive residues satisfy (Φi+1, Ψi+1) = (-Ψi, -Φi) (opposed twist). The red contours shown indicate regions that lie within 4 kcal/mol of the minima in the free-energy landscape of a disarcosine peptoid in vacuum. E and F are the same as C and D, but under the design rule (Φi+1, Ψi+1) = (-Φi ,-Ψi) (opposed chirality). G and H show candidate structures used to build models of nanosheets for MD simulations, using design rules 1 and 2, respectively. I and J are Ramachandran probability plots obtained from MD simulations of all-trans and all-cis polymers in nanosheets.« less

Save / Share:

Works referenced in this record:

Free-floating ultrathin two-dimensional crystals from sequence-specific peptoid polymers
journal, April 2010

  • Nam, Ki Tae; Shelby, Sarah A.; Choi, Philip H.
  • Nature Materials, Vol. 9, Issue 5
  • DOI: 10.1038/nmat2742

Stereochemistry of polypeptide chain configurations
journal, July 1963


The Pleated Sheet, A New Layer Configuration of Polypeptide Chains
journal, May 1951

  • Pauling, L.; Corey, R. B.
  • Proceedings of the National Academy of Sciences, Vol. 37, Issue 5
  • DOI: 10.1073/pnas.37.5.251

The crystal and molecular structure of biphenyl
journal, November 1961


Development and use of an atomistic CHARMM-based forcefield for peptoid simulation
journal, November 2013

  • Mirijanian, Dina T.; Mannige, Ranjan V.; Zuckermann, Ronald N.
  • Journal of Computational Chemistry, Vol. 35, Issue 5
  • DOI: 10.1002/jcc.23478

Rings and ribbons in protein structures: Characterization using helical parameters and Ramachandran plots for repeating dipeptides: Rings and Ribbons in Protein Structures
journal, October 2013

  • Hayward, Steven; Leader, David P.; Al-Shubailly, Fawzia
  • Proteins: Structure, Function, and Bioinformatics, Vol. 82, Issue 2
  • DOI: 10.1002/prot.24357

Structure of the N-terminal domain of a type B1 G protein-coupled receptor in complex with a peptide ligand
journal, March 2007

  • Grace, C. R. R.; Perrin, M. H.; Gulyas, J.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 12
  • DOI: 10.1073/pnas.0700682104

Accelerated molecular dynamics: A promising and efficient simulation method for biomolecules
journal, June 2004

  • Hamelberg, Donald; Mongan, John; McCammon, J. Andrew
  • The Journal of Chemical Physics, Vol. 120, Issue 24
  • DOI: 10.1063/1.1755656

Scalable molecular dynamics with NAMD
journal, January 2005

  • Phillips, James C.; Braun, Rosemary; Wang, Wei
  • Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802
  • DOI: 10.1002/jcc.20289

The Ramachandran Number: An Order Parameter for Protein Geometry
journal, August 2016


Sheet structures in alternating poly(D,L-peptides)
journal, January 1981

  • Heitz, F.; Detriche, G.; Vovelle, F.
  • Macromolecules, Vol. 14, Issue 1
  • DOI: 10.1021/ma50002a007

Tandem Incorporation of Enantiomeric Residues Engenders Discrete Peptoid Structures
journal, May 2016


Kinetics and Equilibria of Cis/Trans Isomerization of Backbone Amide Bonds in Peptoids
journal, October 2007

  • Sui, Qiang; Borchardt, Dan; Rabenstein, Dallas L.
  • Journal of the American Chemical Society, Vol. 129, Issue 39
  • DOI: 10.1021/ja0740925

Evidence for cis Amide Bonds in Peptoid Nanosheets
journal, April 2018

  • Hudson, Benjamin C.; Battigelli, Alessia; Connolly, Michael D.
  • The Journal of Physical Chemistry Letters, Vol. 9, Issue 10
  • DOI: 10.1021/acs.jpclett.8b01040

Molecular Engineering of the Peptoid Nanosheet Hydrophobic Core
journal, October 2016


Peptoid nanosheets exhibit a new secondary-structure motif
journal, October 2015

  • Mannige, Ranjan V.; Haxton, Thomas K.; Proulx, Caroline
  • Nature, Vol. 526, Issue 7573
  • DOI: 10.1038/nature15363

Pauling and Corey's  -pleated sheet structure may define the prefibrillar amyloidogenic intermediate in amyloid disease
journal, July 2004

  • Armen, R. S.; DeMarco, M. L.; Alonso, D. O. V.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 32
  • DOI: 10.1073/pnas.0401781101

Shape change in crystallization of biological macromolecules
journal, May 2016

  • Vekilov, Peter G.; Chung, Sungwook; Olafson, Katy N.
  • MRS Bulletin, Vol. 41, Issue 5
  • DOI: 10.1557/mrs.2016.87

α-Sheet:  The Toxic Conformer in Amyloid Diseases?
journal, September 2006

  • Daggett, Valerie
  • Accounts of Chemical Research, Vol. 39, Issue 9
  • DOI: 10.1021/ar0500719

Shaken, Not Stirred: Collapsing a Peptoid Monolayer To Produce Free-Floating, Stable Nanosheets
journal, December 2011

  • Sanii, Babak; Kudirka, Romas; Cho, Andrew
  • Journal of the American Chemical Society, Vol. 133, Issue 51
  • DOI: 10.1021/ja206199d

Folding of a single-chain, information-rich polypeptoid sequence into a highly ordered nanosheet
journal, January 2011

  • Kudirka, Romas; Tran, Helen; Sanii, Babak
  • Biopolymers, Vol. 96, Issue 5
  • DOI: 10.1002/bip.21590

VMD: Visual molecular dynamics
journal, February 1996


The geometry of α-sheet: Implications for its possible function as amyloid precursor in proteins
journal, January 2008

  • Hayward, Steven; Milner-White, E. James
  • Proteins: Structure, Function, and Bioinformatics, Vol. 71, Issue 1
  • DOI: 10.1002/prot.21717

The structure of proteins: Two hydrogen-bonded helical configurations of the polypeptide chain
journal, April 1951

  • Pauling, L.; Corey, R. B.; Branson, H. R.
  • Proceedings of the National Academy of Sciences, Vol. 37, Issue 4, p. 205-211
  • DOI: 10.1073/pnas.37.4.205

    Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.