Localized Plasmonic Heating for Single-Molecule DNA Rupture Measurements in Optical Tweezers

Kabtiyal, Prerna; Robbins, Ariel; Jergens, Elizabeth; Castro, Carlos E.; Winter, Jessica O.; Poirier, Michael G.; Johnston-Halperin, Ezekiel

doi:10.1021/acs.nanolett.3c04848

Localized Plasmonic Heating for Single-Molecule DNA Rupture Measurements in Optical Tweezers

Journal Article · Wed Feb 28 00:00:00 EST 2024 · Nano Letters

DOI:https://doi.org/10.1021/acs.nanolett.3c04848· OSTI ID:2557985

^[1]; Robbins, Ariel ^[2]; Jergens, Elizabeth ^[2]; ^[2]; ^[2]; ^[2]; ^[2]

The Ohio State Univ., Columbus, OH (United States); The Ohio State University
The Ohio State Univ., Columbus, OH (United States)

To date, studies on the thermodynamic and kinetic processes that underlie biological function and nanomachine actuation in biological- and biology-inspired molecular constructs have primarily focused on photothermal heating of ensemble systems, highlighting the need for probes that are localized within the molecular construct and capable of resolving single-molecule response. Here we present an experimental demonstration of wavelength-selective, localized heating at the single-molecule level using the surface plasmon resonance of a 15 nm gold nanoparticle (AuNP). Our approach is compatible with force-spectroscopy measurements and can be applied to studies of the single-molecule thermodynamic properties of DNA origami nanomachines as well as biomolecular complexes. We further demonstrate wavelength selectivity and establish the temperature dependence of the reaction coordinate for base-pair disruption in the shear-rupture geometry, demonstrating the utility and flexibility of this approach for both fundamental studies of local (nanometer-scale) temperature gradients and rapid and multiplexed nanomachine actuation.

View Accepted Manuscript (DOE)

Research Organization:: The Ohio State Univ., Columbus, OH (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0017270

OSTI ID:: 2557985

Journal Information:: Nano Letters, Journal Name: Nano Letters Journal Issue: 10 Vol. 24; ISSN 1530-6984

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (49)

Thermo-Responsive Actuation of a DNA Origami Flexor Turek, Vladimir A.; Chikkaraddy, Rohit; Cormier, Sean Advanced Functional Materials, Vol. 28, Issue 25 https://doi.org/10.1002/adfm.201706410	journal	March 2018
Actuating Single Nano-Oscillators with Light Cormier, Sean; Ding, Tao; Turek, Vladimir Advanced Optical Materials, Vol. 6, Issue 6 https://doi.org/10.1002/adom.201701281	journal	February 2018
Thermoplasmonics with Gold Nanoparticles: A New Weapon in Modern Optics and Biomedicine Guglielmelli, Alexa; Pierini, Filippo; Tabiryan, Nelson Advanced Photonics Research, Vol. 2, Issue 8 https://doi.org/10.1002/adpr.202000198	journal	June 2021
Encapsulation of Gold Nanoparticles in a DNA Origami Cage Zhao, Zhao; Jacovetty, Erica L.; Liu, Yan Angewandte Chemie International Edition, Vol. 50, Issue 9 https://doi.org/10.1002/anie.201006818	journal	January 2011
Near infrared laser-tissue welding using nanoshells as an exogenous absorber Gobin, Andre M.; O'Neal, D. Patrick; Watkins, Daniel M. Lasers in Surgery and Medicine, Vol. 37, Issue 2 https://doi.org/10.1002/lsm.20206	journal	January 2005
Light‐Activated Nanoimpeller‐Controlled Drug Release in Cancer Cells Lu, Jie; Choi, Eunshil; Tamanoi, Fuyuhiko Small, Vol. 4, Issue 4 https://doi.org/10.1002/smll.200700903	journal	April 2008
Reversible Photothermal Melting of DNA in DNA–Gold-Nanoparticle Networks Reismann, Maximilian; Bretschneider, Jan C.; Plessen, Gero von Small, Vol. 4, Issue 5 https://doi.org/10.1002/smll.200701317	journal	May 2008
Kolmogorov-Smirnov Two-Sample Tests Pratt, John W.; Gibbons, Jean D. Springer Series in Statistics https://doi.org/10.1007/978-1-4612-5931-2_7	book	January 1981
Entropy and Heat Capacity of DNA Melting from Temperature Dependence of Single Molecule Stretching Williams, Mark C.; Wenner, Jay R.; Rouzina, Ioulia Biophysical Journal, Vol. 80, Issue 4 https://doi.org/10.1016/S0006-3495(01)76163-2	journal	April 2001
Laser-Induced Heating in Optical Traps Peterman, Erwin J. G.; Gittes, Frederick; Schmidt, Christoph F. Biophysical Journal, Vol. 84, Issue 2 https://doi.org/10.1016/S0006-3495(03)74946-7	journal	February 2003
Applications for atomic force microscopy of DNA Hansma, H. G.; Laney, D. E.; Bezanilla, M. Biophysical Journal, Vol. 68, Issue 5 https://doi.org/10.1016/S0006-3495(95)80343-7	journal	May 1995
Single-molecule studies of DNA mechanics Bustamante, Carlos; Smith, Steven B.; Liphardt, Jan Current Opinion in Structural Biology, Vol. 10, Issue 3 https://doi.org/10.1016/S0959-440X(00)00085-3	journal	June 2000
Single-molecule folding Zhuang, Xiaowei; Rief, Matthias Current Opinion in Structural Biology, Vol. 13, Issue 1 https://doi.org/10.1016/S0959-440X(03)00011-3	journal	February 2003
Single molecule nanobioscience Ishijima, Akihiko; Yanagida, Toshio Trends in Biochemical Sciences, Vol. 26, Issue 7 https://doi.org/10.1016/S0968-0004(01)01860-6	journal	July 2001
Au nanoparticles target cancer Jain, Prashant K.; El-Sayed, Ivan H.; El-Sayed, Mostafa A. Nano Today, Vol. 2, Issue 1 https://doi.org/10.1016/S1748-0132(07)70016-6	journal	February 2007
Laser-Assisted Single-Molecule Refolding (LASR) Zhao, Rui; Marshall, Myles; Alemán, Elvin A. Biophysical Journal, Vol. 99, Issue 6 https://doi.org/10.1016/j.bpj.2010.07.019	journal	September 2010
Pulsed IR Heating Studies of Single-Molecule DNA Duplex Dissociation Kinetics and Thermodynamics Holmstrom, Erik D.; Dupuis, Nicholas F.; Nesbitt, David J. Biophysical Journal, Vol. 106, Issue 1 https://doi.org/10.1016/j.bpj.2013.11.008	journal	January 2014
A Temperature-Jump Optical Trap for Single-Molecule Manipulation de Lorenzo, Sara; Ribezzi-Crivellari, Marco; Arias-Gonzalez, J. Ricardo Biophysical Journal, Vol. 108, Issue 12 https://doi.org/10.1016/j.bpj.2015.05.017	journal	June 2015
A novel design for magnetic tweezers with wide-range temperature control Zhou, Yu; Tang, Qingnan; Zhao, Xiaodan Biophysical Journal, Vol. 122, Issue 19 https://doi.org/10.1016/j.bpj.2023.08.004	journal	October 2023
Photothermal Temperature Control of a Chemical Reaction on a Microchip Using an Infrared Diode Laser Slyadnev, Maxim N.; Tanaka, Yuki; Tokeshi, Manabu Analytical Chemistry, Vol. 73, Issue 16 https://doi.org/10.1021/ac010318p	journal	July 2001
Chiral Photomelting of DNA-Nanocrystal Assemblies Utilizing Plasmonic Photoheating Ávalos-Ovando, Oscar; Besteiro, Lucas V.; Movsesyan, Artur Nano Letters, Vol. 21, Issue 17 https://doi.org/10.1021/acs.nanolett.1c02479	journal	August 2021
Reciprocal Control of Hierarchical DNA Origami-Nanoparticle Assemblies Johnson, Joshua A.; Dehankar, Abhilasha; Winter, Jessica O. Nano Letters, Vol. 19, Issue 12 https://doi.org/10.1021/acs.nanolett.9b02786	journal	October 2019
High-Force Application by a Nanoscale DNA Force Spectrometer Darcy, Michael; Crocker, Kyle; Wang, Yuchen ACS Nano, Vol. 16, Issue 4 https://doi.org/10.1021/acsnano.1c10698	journal	April 2022
Modulation of Local Cellular Activities using a Photothermal Dye-Based Subcellular-Sized Heat Spot No authors listed ACS Nano, Vol. 16, Issue 6 https://doi.org/10.1021/acsnano.2c00285	journal	June 2022
Ordering Gold Nanoparticles with DNA Origami Nanoflowers Schreiber, Robert; Santiago, Ibon; Ardavan, Arzhang ACS Nano, Vol. 10, Issue 8 https://doi.org/10.1021/acsnano.6b03076	journal	July 2016
Thermodynamic Origins of Monovalent Facilitated RNA Folding Holmstrom, Erik D.; Fiore, Julie L.; Nesbitt, David J. Biochemistry, Vol. 51, Issue 18 https://doi.org/10.1021/bi201420a	journal	April 2012
Enthalpy-Driven RNA Folding: Single-Molecule Thermodynamics of Tetraloop−Receptor Tertiary Interaction ^† Fiore, Julie L.; Kraemer, Benedikt; Koberling, Felix Biochemistry, Vol. 48, Issue 11 https://doi.org/10.1021/bi8019788	journal	March 2009
Calculated Absorption and Scattering Properties of Gold Nanoparticles of Different Size, Shape, and Composition: Applications in Biological Imaging and Biomedicine Jain, Prashant K.; Lee, Kyeong Seok; El-Sayed, Ivan H. The Journal of Physical Chemistry B, Vol. 110, Issue 14 https://doi.org/10.1021/jp057170o	journal	April 2006
Surface Plasmon-Mediated Photothermal Chemistry Qiu, Jingjing; Wei, Wei David The Journal of Physical Chemistry C, Vol. 118, Issue 36 https://doi.org/10.1021/jp5042553	journal	July 2014
Real-Time Infrared Overtone Laser Control of Temperature in Picoliter H ₂ O Samples: “Nanobathtubs” for Single Molecule Microscopy Holmstrom, Erik D.; Nesbitt, David J. The Journal of Physical Chemistry Letters, Vol. 1, Issue 15 https://doi.org/10.1021/jz100663e	journal	July 2010
Sequence-Dependent Stability of DNA-Modified Gold Nanoparticles Storhoff, James J.; Elghanian, Robert; Mirkin, Chad A. Langmuir, Vol. 18, Issue 17 https://doi.org/10.1021/la0202428	journal	August 2002
The Role of Metal Nanoparticles in Remote Release of Encapsulated Materials Skirtach, Andre G.; Dejugnat, Christophe; Braun, Dieter Nano Letters, Vol. 5, Issue 7 https://doi.org/10.1021/nl050693n	journal	June 2005
Gold NanoStoves for Microsecond DNA Melting Analysis Stehr, Joachim; Hrelescu, Calin; Sperling, Ralph A. Nano Letters, Vol. 8, Issue 2 https://doi.org/10.1021/nl073028i	journal	February 2008
Evolution of Light-Induced Vapor Generation at a Liquid-Immersed Metallic Nanoparticle Fang, Zheyu; Zhen, Yu-Rong; Neumann, Oara Nano Letters, Vol. 13, Issue 4 https://doi.org/10.1021/nl4003238	journal	March 2013
Optical Injection of Gold Nanoparticles into Living Cells Li, Miao; Lohmüller, Theobald; Feldmann, Jochen Nano Letters, Vol. 15, Issue 1 https://doi.org/10.1021/nl504497m	journal	December 2014
Experimental and Theoretical Studies of Light-to-Heat Conversion and Collective Heating Effects in Metal Nanoparticle Solutions Richardson, Hugh H.; Carlson, Michael T.; Tandler, Peter J. Nano Letters, Vol. 9, Issue 3 https://doi.org/10.1021/nl8036905	journal	March 2009
Ten years of tension: single-molecule DNA mechanics Bustamante, Carlos; Bryant, Zev; Smith, Steven B. Nature, Vol. 421, Issue 6921 https://doi.org/10.1038/nature01405	journal	January 2003
DNA-based self-assembly of chiral plasmonic nanostructures with tailored optical response Kuzyk, Anton; Schreiber, Robert; Fan, Zhiyuan Nature, Vol. 483, Issue 7389 https://doi.org/10.1038/nature10889	journal	March 2012
Reconfigurable 3D plasmonic metamolecules Kuzyk, Anton; Schreiber, Robert; Zhang, Hui Nature Materials, Vol. 13, Issue 9 https://doi.org/10.1038/nmat4031	journal	July 2014
Simultaneous, coincident optical trapping and single-molecule fluorescence Lang, Matthew J.; Fordyce, Polly M.; Engh, Anita M. Nature Methods, Vol. 1, Issue 2 https://doi.org/10.1038/nmeth714	journal	October 2004
Temperature-cycle single-molecule FRET microscopy on polyprolines Yuan, Haifeng; Xia, Ted; Schuler, Benjamin Phys. Chem. Chem. Phys., Vol. 13, Issue 5 https://doi.org/10.1039/C0CP01772H	journal	January 2011
Combining temperature and force to study folding of an RNA hairpin Stephenson, William; Keller, Sean; Santiago, Rachel Phys. Chem. Chem. Phys., Vol. 16, Issue 3 https://doi.org/10.1039/C3CP52042K	journal	January 2014
Single-molecule denaturation mapping of DNA in nanofluidic channels Reisner, W.; Larsen, N. B.; Silahtaroglu, A. Proceedings of the National Academy of Sciences, Vol. 107, Issue 30 https://doi.org/10.1073/pnas.1007081107	journal	July 2010
Two distinct overstretched DNA structures revealed by single-molecule thermodynamics measurements Zhang, Xinghua; Chen, Hu; Fu, Hongxia Proceedings of the National Academy of Sciences, Vol. 109, Issue 21 https://doi.org/10.1073/pnas.1109824109	journal	April 2012
Light-induced actuating nanotransducers Ding, Tao; Valev, Ventsislav K.; Salmon, Andrew R. Proceedings of the National Academy of Sciences, Vol. 113, Issue 20 https://doi.org/10.1073/pnas.1524209113	journal	May 2016
Single metallic nanoparticle imaging for protein detection in cells Cognet, L.; Tardin, C.; Boyer, D. Proceedings of the National Academy of Sciences, Vol. 100, Issue 20 https://doi.org/10.1073/pnas.1534635100	journal	September 2003
Temperature Control Methods in a Laser Tweezers System Mao, Hanbin; Ricardo Arias-Gonzalez, J.; Smith, Steven B. Biophysical Journal, Vol. 89, Issue 2 https://doi.org/10.1529/biophysj.104.054536	journal	August 2005
Laser-Driven Microsecond Temperature Cycles Analyzed by Fluorescence Polarization Microscopy Zondervan, Rob; Kulzer, Florian; van der Meer, Harmen Biophysical Journal, Vol. 90, Issue 8 https://doi.org/10.1529/biophysj.105.075168	journal	April 2006
Subpiconewton Dynamic Force Spectroscopy Using Magnetic Tweezers Kruithof, M.; Chien, F.; de Jager, M. Biophysical Journal, Vol. 94, Issue 6 https://doi.org/10.1529/biophysj.107.121673	journal	March 2008

Similar Records

Hierarchical Assembly of Plasmonic Nanostructures using Virus Capsid Scaffolds on DNA Origami Tiles

Journal Article · Mon Jul 07 00:00:00 EDT 2014 · ACS Nano, 8(8):7896-7904 · OSTI ID:1171891

Reciprocal Control of Hierarchical DNA Origami-Nanoparticle Assemblies

Journal Article · Tue Oct 29 20:00:00 EDT 2019 · Nano Letters · OSTI ID:1657521

Hierarchical Assembly of Plasmonic Nanostructures using Virus Capsid Scaffolds and DNA Origami Tiles

Journal Article · Tue Aug 26 00:00:00 EDT 2014 · ACS Nano · OSTI ID:1526973

Related Subjects

77 NANOSCIENCE AND NANOTECHNOLOGY
DNA
force spectroscopy
optical tweezers
plasmonic heating
single-molecule

Localized Plasmonic Heating for Single-Molecule DNA Rupture Measurements in Optical Tweezers

Citation Formats

References (49)

Similar Records

Related Subjects