Spider Silk Peptide Is a Compact, Linear Nanospring Ideal for Intracellular Tension Sensing

Michael D. Brenner, Ruobo Zhou, Daniel E. Conway, Luca Lanzano, Enrico Gratton, Martin A. Schwartz, Taekjip Ha

Research output: Contribution to journalArticle

Abstract

Recent development and applications of calibrated, fluorescence resonance energy transfer (FRET)-based tension sensors have led to a new understanding of single molecule mechanotransduction in a number of biological systems. To expand the range of accessible forces, we systematically measured FRET versus force trajectories for 25, 40, and 50 amino acid peptide repeats derived from spider silk. Single molecule fluorescence-force spectroscopy showed that the peptides behaved as linear springs instead of the nonlinear behavior expected for a disordered polymer. Our data are consistent with a compact, rodlike structure that measures 0.26 nm per 5 amino acid repeat that can stretch by 500% while maintaining linearity, suggesting that the remarkable elasticity of spider silk proteins may in part derive from the properties of individual chains. We found the shortest peptide to have the widest range of force sensitivity: between 2 pN and 11 pN. Live cell imaging of the three tension sensor constructs inserted into vinculin showed similar force values around 2.4 pN. We also provide a lookup table for force versus intracellular FRET for all three constructs.

Original languageEnglish (US)
Pages (from-to)2096-2102
Number of pages7
JournalNano Letters
Volume16
Issue number3
DOIs
StatePublished - Mar 9 2016

Fingerprint

spiders
silk
Silk
Peptides
peptides
Amino acids
resonance fluorescence
Vinculin
Amino Acids
Table lookup
Molecules
energy transfer
Sensors
Biological systems
amino acids
Elasticity
Polymers
Fluorescence
Trajectories
Spectroscopy

Keywords

  • FLIM
  • force-fluorescence spectroscopy
  • Force-sensor
  • optical tweezers
  • single-molecule FRET
  • spider flagelliform silk

ASJC Scopus subject areas

  • Bioengineering
  • Chemistry(all)
  • Materials Science(all)
  • Condensed Matter Physics
  • Mechanical Engineering

Cite this

Brenner, M. D., Zhou, R., Conway, D. E., Lanzano, L., Gratton, E., Schwartz, M. A., & Ha, T. (2016). Spider Silk Peptide Is a Compact, Linear Nanospring Ideal for Intracellular Tension Sensing. Nano Letters, 16(3), 2096-2102. https://doi.org/10.1021/acs.nanolett.6b00305

Spider Silk Peptide Is a Compact, Linear Nanospring Ideal for Intracellular Tension Sensing. / Brenner, Michael D.; Zhou, Ruobo; Conway, Daniel E.; Lanzano, Luca; Gratton, Enrico; Schwartz, Martin A.; Ha, Taekjip.

In: Nano Letters, Vol. 16, No. 3, 09.03.2016, p. 2096-2102.

Research output: Contribution to journalArticle

Brenner, MD, Zhou, R, Conway, DE, Lanzano, L, Gratton, E, Schwartz, MA & Ha, T 2016, 'Spider Silk Peptide Is a Compact, Linear Nanospring Ideal for Intracellular Tension Sensing', Nano Letters, vol. 16, no. 3, pp. 2096-2102. https://doi.org/10.1021/acs.nanolett.6b00305
Brenner MD, Zhou R, Conway DE, Lanzano L, Gratton E, Schwartz MA et al. Spider Silk Peptide Is a Compact, Linear Nanospring Ideal for Intracellular Tension Sensing. Nano Letters. 2016 Mar 9;16(3):2096-2102. https://doi.org/10.1021/acs.nanolett.6b00305
Brenner, Michael D. ; Zhou, Ruobo ; Conway, Daniel E. ; Lanzano, Luca ; Gratton, Enrico ; Schwartz, Martin A. ; Ha, Taekjip. / Spider Silk Peptide Is a Compact, Linear Nanospring Ideal for Intracellular Tension Sensing. In: Nano Letters. 2016 ; Vol. 16, No. 3. pp. 2096-2102.
@article{cff0de94cae94f139b33364169f0fec4,
title = "Spider Silk Peptide Is a Compact, Linear Nanospring Ideal for Intracellular Tension Sensing",
abstract = "Recent development and applications of calibrated, fluorescence resonance energy transfer (FRET)-based tension sensors have led to a new understanding of single molecule mechanotransduction in a number of biological systems. To expand the range of accessible forces, we systematically measured FRET versus force trajectories for 25, 40, and 50 amino acid peptide repeats derived from spider silk. Single molecule fluorescence-force spectroscopy showed that the peptides behaved as linear springs instead of the nonlinear behavior expected for a disordered polymer. Our data are consistent with a compact, rodlike structure that measures 0.26 nm per 5 amino acid repeat that can stretch by 500{\%} while maintaining linearity, suggesting that the remarkable elasticity of spider silk proteins may in part derive from the properties of individual chains. We found the shortest peptide to have the widest range of force sensitivity: between 2 pN and 11 pN. Live cell imaging of the three tension sensor constructs inserted into vinculin showed similar force values around 2.4 pN. We also provide a lookup table for force versus intracellular FRET for all three constructs.",
keywords = "FLIM, force-fluorescence spectroscopy, Force-sensor, optical tweezers, single-molecule FRET, spider flagelliform silk",
author = "Brenner, {Michael D.} and Ruobo Zhou and Conway, {Daniel E.} and Luca Lanzano and Enrico Gratton and Schwartz, {Martin A.} and Taekjip Ha",
year = "2016",
month = "3",
day = "9",
doi = "10.1021/acs.nanolett.6b00305",
language = "English (US)",
volume = "16",
pages = "2096--2102",
journal = "Nano Letters",
issn = "1530-6984",
publisher = "American Chemical Society",
number = "3",

}

TY - JOUR

T1 - Spider Silk Peptide Is a Compact, Linear Nanospring Ideal for Intracellular Tension Sensing

AU - Brenner, Michael D.

AU - Zhou, Ruobo

AU - Conway, Daniel E.

AU - Lanzano, Luca

AU - Gratton, Enrico

AU - Schwartz, Martin A.

AU - Ha, Taekjip

PY - 2016/3/9

Y1 - 2016/3/9

N2 - Recent development and applications of calibrated, fluorescence resonance energy transfer (FRET)-based tension sensors have led to a new understanding of single molecule mechanotransduction in a number of biological systems. To expand the range of accessible forces, we systematically measured FRET versus force trajectories for 25, 40, and 50 amino acid peptide repeats derived from spider silk. Single molecule fluorescence-force spectroscopy showed that the peptides behaved as linear springs instead of the nonlinear behavior expected for a disordered polymer. Our data are consistent with a compact, rodlike structure that measures 0.26 nm per 5 amino acid repeat that can stretch by 500% while maintaining linearity, suggesting that the remarkable elasticity of spider silk proteins may in part derive from the properties of individual chains. We found the shortest peptide to have the widest range of force sensitivity: between 2 pN and 11 pN. Live cell imaging of the three tension sensor constructs inserted into vinculin showed similar force values around 2.4 pN. We also provide a lookup table for force versus intracellular FRET for all three constructs.

AB - Recent development and applications of calibrated, fluorescence resonance energy transfer (FRET)-based tension sensors have led to a new understanding of single molecule mechanotransduction in a number of biological systems. To expand the range of accessible forces, we systematically measured FRET versus force trajectories for 25, 40, and 50 amino acid peptide repeats derived from spider silk. Single molecule fluorescence-force spectroscopy showed that the peptides behaved as linear springs instead of the nonlinear behavior expected for a disordered polymer. Our data are consistent with a compact, rodlike structure that measures 0.26 nm per 5 amino acid repeat that can stretch by 500% while maintaining linearity, suggesting that the remarkable elasticity of spider silk proteins may in part derive from the properties of individual chains. We found the shortest peptide to have the widest range of force sensitivity: between 2 pN and 11 pN. Live cell imaging of the three tension sensor constructs inserted into vinculin showed similar force values around 2.4 pN. We also provide a lookup table for force versus intracellular FRET for all three constructs.

KW - FLIM

KW - force-fluorescence spectroscopy

KW - Force-sensor

KW - optical tweezers

KW - single-molecule FRET

KW - spider flagelliform silk

UR - http://www.scopus.com/inward/record.url?scp=84960494069&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84960494069&partnerID=8YFLogxK

U2 - 10.1021/acs.nanolett.6b00305

DO - 10.1021/acs.nanolett.6b00305

M3 - Article

C2 - 26824190

AN - SCOPUS:84960494069

VL - 16

SP - 2096

EP - 2102

JO - Nano Letters

JF - Nano Letters

SN - 1530-6984

IS - 3

ER -