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

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 se...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 115; no. 22; pp. 5647 - 5651
Main Authors Edison, John R., Spencer, Ryan K., Butterfoss, Glenn L., Hudson, Benjamin C., Hochbaum, Allon I., Paravastu, Anant K., Zuckermann, Ronald N., Whitelam, Stephen
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 29.05.2018
Proceedings of the National Academy of Sciences
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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 intraand intermolecular interactions.
AbstractList 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 intraand intermolecular interactions.
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.
Significance Commonly observed secondary structures of proteins, such as α -helices and β -sheets, are built from a trans- amide backbone with residues sampling a single region of the Ramachandran plot. Here we report a secondary structure displayed by biomimetic peptoid polymers in which the backbone exhibits the cis conformation and alternating residues display rotational states of opposed (pseudo)chirality. This structure is linear and untwisted and enables strands to pack densely into extended bilayer nanosheets. 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.
Commonly observed secondary structures of proteins, such as α -helices and β -sheets, are built from a trans- amide backbone with residues sampling a single region of the Ramachandran plot. Here we report a secondary structure displayed by biomimetic peptoid polymers in which the backbone exhibits the cis conformation and alternating residues display rotational states of opposed (pseudo)chirality. This structure is linear and untwisted and enables strands to pack densely into extended bilayer nanosheets. 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.
Author Edison, John R.
Hochbaum, Allon I.
Hudson, Benjamin C.
Spencer, Ryan K.
Zuckermann, Ronald N.
Paravastu, Anant K.
Whitelam, Stephen
Butterfoss, Glenn L.
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Keywords peptoid secondary structure
biomimetic sequence-specific polymers
cis-amide
2D supramolecular assembly
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Author contributions: J.R.E., R.K.S., R.N.Z., and S.W. designed research; J.R.E., R.K.S., and G.L.B. performed research; J.R.E., R.K.S., G.L.B., B.C.H., A.I.H., and A.K.P. analyzed data; J.R.E. and S.W. wrote the paper.
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Snippet The conformations adopted by the molecular constituents of a supramolecular assembly influence its large-scale order. At the same time, the interactions made...
Significance Commonly observed secondary structures of proteins, such as α -helices and β -sheets, are built from a trans- amide backbone with residues...
Commonly observed secondary structures of proteins, such as α -helices and β -sheets, are built from a trans- amide backbone with residues sampling a single...
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StartPage 5647
SubjectTerms Backbone
BASIC BIOLOGICAL SCIENCES
Bioenergetics
Biological Sciences
Biomimetic Materials - chemistry
Computer simulation
Experimental data
MATERIALS SCIENCE
Molecular biology
Molecular dynamics
Molecular Dynamics Simulation
Molecular structure
Nanosheets
Nanostructure
Nanostructures - chemistry
Nanostructures - ultrastructure
Peptides
Peptoids - chemistry
Physical Sciences
Polymers
Protein Structure, Secondary
Quantum mechanics
Quantum physics
Rotational states
Title Conformations of peptoids in nanosheets result from the interplay of backbone energetics and intermolecular interactions
URI https://www.jstor.org/stable/26509908
https://www.ncbi.nlm.nih.gov/pubmed/29760077
https://www.proquest.com/docview/2101971743/abstract/
https://search.proquest.com/docview/2039284565
https://www.osti.gov/biblio/1437093
https://pubmed.ncbi.nlm.nih.gov/PMC5984518
Volume 115
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