Nature of Amorphous Hydrophilic Block Affects Self-Assembly of an Artificial Viral Coat Polypeptide

Lione Willems, Larissa Van Westerveld, Stefan Roberts, Isaac Weitzhandler, Carlos Calcines Cruz, Armando Hernandez-Garcia, Ashutosh Chilkoti, Enrico Mastrobattista, John Van Der Oost, Renko De Vries*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Consensus motifs for sequences of both crystallizable and amorphous blocks in silks and natural structural analogues of silks vary widely. To design novel silklike polypeptides, an important question is therefore how the nature of either the crystallizable or the amorphous block affects the self-assembly and resulting physical properties of silklike polypeptides. We address herein the influence of the amorphous block on the self-assembly of a silklike polypeptide that was previously designed to encapsulate single DNA molecules into rod-shaped viruslike particles. The polypeptide has a triblock architecture, with a long N-terminal amorphous block, a crystallizable midblock, and a C-terminal DNA-binding block. We compare the self-assembly behavior of a triblock with a very hydrophilic collagen-like amorphous block (GXaaYaa)132 to that of a triblock with a less hydrophilic elastin-like amorphous block (GSGVP)80. The amorphous blocks have similar lengths and both adopt a random coil structure in solution. Nevertheless, atomic force microscopy revealed significant differences in the self-assembly behavior of the triblocks. If collagen-like amorphous blocks are used, there is a clear distinction between very short polypeptide-only fibrils and much longer fibrils with encapsulated DNA. If elastin-like amorphous blocks are used, DNA is still encapsulated, but the polypeptide-only fibrils are now much longer and their size distribution partially overlaps with that of the encapsulated DNA fibrils. We attribute the difference to the more hydrophilic nature of the collagen-like amorphous block, which more strongly opposes the growth of polypeptide-only fibrils than the elastin-like amorphous blocks. Our work illustrates that differences in the chemical nature of amorphous blocks can strongly influence the self-assembly and hence the functionality of engineered silklike polypeptides.

Original languageEnglish
Pages (from-to)3641-3647
JournalBiomacromolecules
Volume20
Issue number10
Early online date16 Aug 2019
DOIs
Publication statusPublished - Oct 2019

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Polypeptides
Self assembly
Peptides
DNA
Elastin
Collagen
Silk
Atomic force microscopy
Physical properties

Cite this

Willems, L., Van Westerveld, L., Roberts, S., Weitzhandler, I., Calcines Cruz, C., Hernandez-Garcia, A., ... De Vries, R. (2019). Nature of Amorphous Hydrophilic Block Affects Self-Assembly of an Artificial Viral Coat Polypeptide. Biomacromolecules, 20(10), 3641-3647. https://doi.org/10.1021/acs.biomac.9b00512
Willems, Lione ; Van Westerveld, Larissa ; Roberts, Stefan ; Weitzhandler, Isaac ; Calcines Cruz, Carlos ; Hernandez-Garcia, Armando ; Chilkoti, Ashutosh ; Mastrobattista, Enrico ; Van Der Oost, John ; De Vries, Renko. / Nature of Amorphous Hydrophilic Block Affects Self-Assembly of an Artificial Viral Coat Polypeptide. In: Biomacromolecules. 2019 ; Vol. 20, No. 10. pp. 3641-3647.
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abstract = "Consensus motifs for sequences of both crystallizable and amorphous blocks in silks and natural structural analogues of silks vary widely. To design novel silklike polypeptides, an important question is therefore how the nature of either the crystallizable or the amorphous block affects the self-assembly and resulting physical properties of silklike polypeptides. We address herein the influence of the amorphous block on the self-assembly of a silklike polypeptide that was previously designed to encapsulate single DNA molecules into rod-shaped viruslike particles. The polypeptide has a triblock architecture, with a long N-terminal amorphous block, a crystallizable midblock, and a C-terminal DNA-binding block. We compare the self-assembly behavior of a triblock with a very hydrophilic collagen-like amorphous block (GXaaYaa)132 to that of a triblock with a less hydrophilic elastin-like amorphous block (GSGVP)80. The amorphous blocks have similar lengths and both adopt a random coil structure in solution. Nevertheless, atomic force microscopy revealed significant differences in the self-assembly behavior of the triblocks. If collagen-like amorphous blocks are used, there is a clear distinction between very short polypeptide-only fibrils and much longer fibrils with encapsulated DNA. If elastin-like amorphous blocks are used, DNA is still encapsulated, but the polypeptide-only fibrils are now much longer and their size distribution partially overlaps with that of the encapsulated DNA fibrils. We attribute the difference to the more hydrophilic nature of the collagen-like amorphous block, which more strongly opposes the growth of polypeptide-only fibrils than the elastin-like amorphous blocks. Our work illustrates that differences in the chemical nature of amorphous blocks can strongly influence the self-assembly and hence the functionality of engineered silklike polypeptides.",
author = "Lione Willems and {Van Westerveld}, Larissa and Stefan Roberts and Isaac Weitzhandler and {Calcines Cruz}, Carlos and Armando Hernandez-Garcia and Ashutosh Chilkoti and Enrico Mastrobattista and {Van Der Oost}, John and {De Vries}, Renko",
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Willems, L, Van Westerveld, L, Roberts, S, Weitzhandler, I, Calcines Cruz, C, Hernandez-Garcia, A, Chilkoti, A, Mastrobattista, E, Van Der Oost, J & De Vries, R 2019, 'Nature of Amorphous Hydrophilic Block Affects Self-Assembly of an Artificial Viral Coat Polypeptide', Biomacromolecules, vol. 20, no. 10, pp. 3641-3647. https://doi.org/10.1021/acs.biomac.9b00512

Nature of Amorphous Hydrophilic Block Affects Self-Assembly of an Artificial Viral Coat Polypeptide. / Willems, Lione; Van Westerveld, Larissa; Roberts, Stefan; Weitzhandler, Isaac; Calcines Cruz, Carlos; Hernandez-Garcia, Armando; Chilkoti, Ashutosh; Mastrobattista, Enrico; Van Der Oost, John; De Vries, Renko.

In: Biomacromolecules, Vol. 20, No. 10, 10.2019, p. 3641-3647.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - Willems, Lione

AU - Van Westerveld, Larissa

AU - Roberts, Stefan

AU - Weitzhandler, Isaac

AU - Calcines Cruz, Carlos

AU - Hernandez-Garcia, Armando

AU - Chilkoti, Ashutosh

AU - Mastrobattista, Enrico

AU - Van Der Oost, John

AU - De Vries, Renko

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N2 - Consensus motifs for sequences of both crystallizable and amorphous blocks in silks and natural structural analogues of silks vary widely. To design novel silklike polypeptides, an important question is therefore how the nature of either the crystallizable or the amorphous block affects the self-assembly and resulting physical properties of silklike polypeptides. We address herein the influence of the amorphous block on the self-assembly of a silklike polypeptide that was previously designed to encapsulate single DNA molecules into rod-shaped viruslike particles. The polypeptide has a triblock architecture, with a long N-terminal amorphous block, a crystallizable midblock, and a C-terminal DNA-binding block. We compare the self-assembly behavior of a triblock with a very hydrophilic collagen-like amorphous block (GXaaYaa)132 to that of a triblock with a less hydrophilic elastin-like amorphous block (GSGVP)80. The amorphous blocks have similar lengths and both adopt a random coil structure in solution. Nevertheless, atomic force microscopy revealed significant differences in the self-assembly behavior of the triblocks. If collagen-like amorphous blocks are used, there is a clear distinction between very short polypeptide-only fibrils and much longer fibrils with encapsulated DNA. If elastin-like amorphous blocks are used, DNA is still encapsulated, but the polypeptide-only fibrils are now much longer and their size distribution partially overlaps with that of the encapsulated DNA fibrils. We attribute the difference to the more hydrophilic nature of the collagen-like amorphous block, which more strongly opposes the growth of polypeptide-only fibrils than the elastin-like amorphous blocks. Our work illustrates that differences in the chemical nature of amorphous blocks can strongly influence the self-assembly and hence the functionality of engineered silklike polypeptides.

AB - Consensus motifs for sequences of both crystallizable and amorphous blocks in silks and natural structural analogues of silks vary widely. To design novel silklike polypeptides, an important question is therefore how the nature of either the crystallizable or the amorphous block affects the self-assembly and resulting physical properties of silklike polypeptides. We address herein the influence of the amorphous block on the self-assembly of a silklike polypeptide that was previously designed to encapsulate single DNA molecules into rod-shaped viruslike particles. The polypeptide has a triblock architecture, with a long N-terminal amorphous block, a crystallizable midblock, and a C-terminal DNA-binding block. We compare the self-assembly behavior of a triblock with a very hydrophilic collagen-like amorphous block (GXaaYaa)132 to that of a triblock with a less hydrophilic elastin-like amorphous block (GSGVP)80. The amorphous blocks have similar lengths and both adopt a random coil structure in solution. Nevertheless, atomic force microscopy revealed significant differences in the self-assembly behavior of the triblocks. If collagen-like amorphous blocks are used, there is a clear distinction between very short polypeptide-only fibrils and much longer fibrils with encapsulated DNA. If elastin-like amorphous blocks are used, DNA is still encapsulated, but the polypeptide-only fibrils are now much longer and their size distribution partially overlaps with that of the encapsulated DNA fibrils. We attribute the difference to the more hydrophilic nature of the collagen-like amorphous block, which more strongly opposes the growth of polypeptide-only fibrils than the elastin-like amorphous blocks. Our work illustrates that differences in the chemical nature of amorphous blocks can strongly influence the self-assembly and hence the functionality of engineered silklike polypeptides.

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Willems L, Van Westerveld L, Roberts S, Weitzhandler I, Calcines Cruz C, Hernandez-Garcia A et al. Nature of Amorphous Hydrophilic Block Affects Self-Assembly of an Artificial Viral Coat Polypeptide. Biomacromolecules. 2019 Oct;20(10):3641-3647. https://doi.org/10.1021/acs.biomac.9b00512