The Use of Graphene and Its Derivatives for Liquid-Phase Transmission Electron Microscopy of Radiation-Sensitive Specimens

Cho, Hoduk; Jones, Matthew R.; Nguyen, Son C.; Hauwiller, Matthew R.; Zettl, Alex; Alivisatos, A. Paul

doi:10.1021/acs.nanolett.6b04383

Title: The Use of Graphene and Its Derivatives for Liquid-Phase Transmission Electron Microscopy of Radiation-Sensitive Specimens

Journal Article · Tue Dec 27 00:00:00 EST 2016 · Nano Letters

DOI:https://doi.org/10.1021/acs.nanolett.6b04383· OSTI ID:1532216

^[1]; Jones, Matthew R. ^[2]; Nguyen, Son C. ^[3]; Hauwiller, Matthew R. ^[1]; Zettl, Alex ^[4];

^[5]

Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of Hamburg (Germany)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States); Kavli Energy NanoScience Institute, Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Kavli Energy NanoScience Institute, Berkeley, CA (United States)

We present that one of the key challenges facing liquid-phase transmission electron microscopy (TEM) of biological specimens has been the damaging effects of electron beam irradiation. The strongly ionizing electron beam is known to induce radiolysis of surrounding water molecules, leading to the formation of reactive radical species. In this study, we employ DNA-assembled Au nanoparticle superlattices (DNA-AuNP superlattices) as a model system to demonstrate that graphene and its derivatives can be used to mitigate electron beam-induced damage. We can image DNA-AuNP superlattices in their native saline environment when the liquid cell window material is graphene, but not when it is silicon nitride. In the latter case, initial dissociation of assembled AuNPs was followed by their random aggregation and etching. Using graphene-coated silicon nitride windows, we were able to replicate the observation of stable DNA-AuNP superlattices achieved with graphene liquid cells. We then carried out a correlative Raman spectroscopy and TEM study to compare the effect of electron beam irradiation on graphene with and without the presence of water and found that graphene reacts with the products of water radiolysis. We attribute the protective effect of graphene to its ability to efficiently scavenge reactive radical species, especially the hydroxyl radicals which are known to cause DNA strand breaks. We confirmed this by showing that stable DNA-AuNP assemblies can be imaged in silicon nitride liquid cells when graphene oxide and graphene quantum dots, which have also recently been reported as efficient radical scavengers, are added directly to the solution. Lastly, we anticipate that our study will open up more opportunities for studying biological specimens using liquid-phase TEM with the use of graphene and its derivatives as biocompatible radical scavengers to alleviate the effects of radiation damage.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

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

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1532216

Journal Information:: Nano Letters, Vol. 17, Issue 1; ISSN 1530-6984

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 89 works

Citation information provided by
Web of Science

References (53)

Dynamic microscopy of nanoscale cluster growth at the solid–liquid interface Williamson, M. J.; Tromp, R. M.; Vereecken, P. M. Nature Materials, Vol. 2, Issue 8 https://doi.org/10.1038/nmat944	journal	July 2003
Opportunities and challenges in liquid cell electron microscopy Ross, F. M. Science, Vol. 350, Issue 6267 https://doi.org/10.1126/science.aaa9886	journal	December 2015
Electron microscopy of whole cells in liquid with nanometer resolution Jonge, N. d.; Peckys, D. B.; Kremers, G. J. Proceedings of the National Academy of Sciences, Vol. 106, Issue 7 https://doi.org/10.1073/pnas.0809567106	journal	January 2009
Visualizing Gold Nanoparticle Uptake in Live Cells with Liquid Scanning Transmission Electron Microscopy Peckys, Diana B.; de Jonge, Niels Nano Letters, Vol. 11, Issue 4 https://doi.org/10.1021/nl200285r	journal	April 2011
Real-Time Visualization of Nanoparticles Interacting with Glioblastoma Stem Cells Pohlmann, Elliot S.; Patel, Kaya; Guo, Sujuan Nano Letters, Vol. 15, Issue 4 https://doi.org/10.1021/nl504481k	journal	March 2015
The Effect of Electron Beam Irradiation in Environmental Scanning Transmission Electron Microscopy of Whole Cells in Liquid Hermannsdörfer, Justus; Tinnemann, Verena; Peckys, Diana B. Microscopy and Microanalysis, Vol. 22, Issue 3 https://doi.org/10.1017/S1431927616000763	journal	May 2016
Electron microscopy of specimens in liquid de Jonge, Niels; Ross, Frances M. Nature Nanotechnology, Vol. 6, Issue 11, p. 695-704 https://doi.org/10.1038/nnano.2011.161	journal	October 2011
Imaging Protein Structure in Water at 2.7 nm Resolution by Transmission Electron Microscopy Mirsaidov, Utkur M.; Zheng, Haimei; Casana, Yosune Biophysical Journal, Vol. 102, Issue 4 https://doi.org/10.1016/j.bpj.2012.01.009	journal	February 2012
Gold Nanoparticle Uptake in Whole Cells in Liquid Examined by Environmental Scanning Electron Microscopy Peckys, Diana B.; de Jonge, Niels Microscopy and Microanalysis, Vol. 20, Issue 1 https://doi.org/10.1017/S1431927613013986	journal	January 2014
Correlative Electron and Fluorescence Microscopy of Magnetotactic Bacteria in Liquid: Toward In Vivo Imaging Woehl, Taylor J.; Kashyap, Sanjay; Firlar, Emre Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep06854	journal	October 2014
Radiation damage in the TEM and SEM Egerton, R. F.; Li, P.; Malac, M. Micron, Vol. 35, Issue 6 https://doi.org/10.1016/j.micron.2004.02.003	journal	August 2004
Reactions of oxyl radicals with DNA Breen, Anthony P.; Murphy, John A. Free Radical Biology and Medicine, Vol. 18, Issue 6 https://doi.org/10.1016/0891-5849(94)00209-3	journal	June 1995
DNA strand breaking by the hydroxyl radical is governed by the accessible surface areas of the hydrogen atoms of the DNA backbone Balasubramanian, B.; Pogozelski, W. K.; Tullius, T. D. Proceedings of the National Academy of Sciences, Vol. 95, Issue 17 https://doi.org/10.1073/pnas.95.17.9738	journal	August 1998
Oxidative Nucleobase Modifications Leading to Strand Scission Burrows, Cynthia J.; Muller, James G. Chemical Reviews, Vol. 98, Issue 3 https://doi.org/10.1021/cr960421s	journal	May 1998
Oxidative Strand Scission of Nucleic Acids: Routes Initiated by Hydrogen Abstraction from the Sugar Moiety Pogozelski, Wendy Knapp; Tullius, Thomas D. Chemical Reviews, Vol. 98, Issue 3 https://doi.org/10.1021/cr960437i	journal	April 1998
High-Resolution EM of Colloidal Nanocrystal Growth Using Graphene Liquid Cells Yuk, Jong Min; Park, Jungwon; Ercius, Peter Science, Vol. 336, Issue 6077 https://doi.org/10.1126/science.1217654	journal	April 2012
Impermeable Graphenic Encasement of Bacteria Mohanty, Nihar; Fahrenholtz, Monica; Nagaraja, Ashvin Nano Letters, Vol. 11, Issue 3 https://doi.org/10.1021/nl104292k	journal	March 2011
3D Motion of DNA-Au Nanoconjugates in Graphene Liquid Cell Electron Microscopy Chen, Qian; Smith, Jessica M.; Park, Jungwon Nano Letters, Vol. 13, Issue 9 https://doi.org/10.1021/nl402694n	journal	August 2013
Studies of the dynamics of biological macromolecules using Au nanoparticle–DNA artificial molecules Chen, Qian; Smith, Jessica M.; Rasool, Haider I. Faraday Discuss., Vol. 175 https://doi.org/10.1039/C4FD00149D	journal	January 2014
High-Resolution Electron Microscopy and Spectroscopy of Ferritin in Biocompatible Graphene Liquid Cells and Graphene Sandwiches Wang, Canhui; Qiao, Qiao; Shokuhfar, Tolou Advanced Materials, Vol. 26, Issue 21 https://doi.org/10.1002/adma.201306069	journal	February 2014
Direct Observation of Wet Biological Samples by Graphene Liquid Cell Transmission Electron Microscopy Park, Jungwon; Park, Hyesung; Ercius, Peter Nano Letters, Vol. 15, Issue 7 https://doi.org/10.1021/acs.nanolett.5b01636	journal	June 2015
Graphene as a transparent conductive support for studying biological molecules by transmission electron microscopy Nair, R. R.; Blake, P.; Blake, J. R. Applied Physics Letters, Vol. 97, Issue 15 https://doi.org/10.1063/1.3492845	journal	October 2010
Control of Radiation Damage in MoS ₂ by Graphene Encapsulation Zan, Recep; Ramasse, Quentin M.; Jalil, Rashid ACS Nano, Vol. 7, Issue 11 https://doi.org/10.1021/nn4044035	journal	October 2013
The pristine atomic structure of MoS ₂ monolayer protected from electron radiation damage by graphene Algara-Siller, Gerardo; Kurasch, Simon; Sedighi, Mona Applied Physics Letters, Vol. 103, Issue 20 https://doi.org/10.1063/1.4830036	journal	November 2013
DNA-programmable nanoparticle crystallization Park, Sung Yong; Lytton-Jean, Abigail K. R.; Lee, Byeongdu Nature, Vol. 451, Issue 7178, p. 553-556 https://doi.org/10.1038/nature06508	journal	January 2008
DNA-guided crystallization of colloidal nanoparticles Nykypanchuk, Dmytro; Maye, Mathew M.; van der Lelie, Daniel Nature, Vol. 451, Issue 7178, p. 549-552 https://doi.org/10.1038/nature06560	journal	January 2008
Programmable materials and the nature of the DNA bond Jones, M. R.; Seeman, N. C.; Mirkin, C. A. Science, Vol. 347, Issue 6224 https://doi.org/10.1126/science.1260901	journal	February 2015
Electrolyte-Mediated Assembly of Charged Nanoparticles Kewalramani, Sumit; Guerrero-García, Guillermo I.; Moreau, Liane M. ACS Central Science, Vol. 2, Issue 4 https://doi.org/10.1021/acscentsci.6b00023	journal	April 2016
Nanoscale Forces and Their Uses in Self-Assembly Bishop, Kyle J. M.; Wilmer, Christopher E.; Soh, Siowling Small, Vol. 5, Issue 14 https://doi.org/10.1002/smll.200900358	journal	July 2009
Formation and Repair of Interstrand Cross-Links in DNA Noll, David M.; Mason, Tracey McGregor; Miller, Paul S. Chemical Reviews, Vol. 106, Issue 2 https://doi.org/10.1021/cr040478b	journal	February 2006
DNA interstrand crosslink repair and cancer Deans, Andrew J.; West, Stephen C. Nature Reviews Cancer, Vol. 11, Issue 7 https://doi.org/10.1038/nrc3088	journal	June 2011
Desorption-Mediated Motion of Nanoparticles at the Liquid–Solid Interface Chee, See Wee; Baraissov, Zhaslan; Loh, N. Duane The Journal of Physical Chemistry C, Vol. 120, Issue 36 https://doi.org/10.1021/acs.jpcc.6b07983	journal	September 2016
Electron–Water Interactions and Implications for Liquid Cell Electron Microscopy Schneider, Nicholas M.; Norton, Michael M.; Mendel, Brian J. The Journal of Physical Chemistry C, Vol. 118, Issue 38 https://doi.org/10.1021/jp507400n	journal	September 2014
Transferring and Identification of Single- and Few-Layer Graphene on Arbitrary Substrates Reina, Alfonso; Son, Hyungbin; Jiao, Liying The Journal of Physical Chemistry C, Vol. 112, Issue 46 https://doi.org/10.1021/jp807380s	journal	October 2008
Large-Area Synthesis of High-Quality and Uniform Graphene Films on Copper Foils Li, X.; Cai, W.; An, J. Science, Vol. 324, Issue 5932, p. 1312-1314 https://doi.org/10.1126/science.1171245	journal	May 2009
The graphene/nucleic acid nanobiointerface Tang, Longhua; Wang, Ying; Li, Jinghong Chemical Society Reviews, Vol. 44, Issue 19 https://doi.org/10.1039/C4CS00519H	journal	January 2015
Real-Time Observation of Water-Soluble Mineral Precipitation in Aqueous Solution by In Situ High-Resolution Electron Microscopy Yuk, Jong Min; Zhou, Qin; Chang, Jiyoung ACS Nano, Vol. 10, Issue 1 https://doi.org/10.1021/acsnano.5b04064	journal	December 2015
Raman spectroscopy as a versatile tool for studying the properties of graphene Ferrari, Andrea C.; Basko, Denis M. Nature Nanotechnology, Vol. 8, Issue 4 https://doi.org/10.1038/nnano.2013.46	journal	April 2013
Raman spectroscopy of graphene and graphite: Disorder, electron–phonon coupling, doping and nonadiabatic effects Ferrari, Andrea C. Solid State Communications, Vol. 143, Issue 1-2, p. 47-57 https://doi.org/10.1016/j.ssc.2007.03.052	journal	July 2007
Nanocrystal Diffusion in a Liquid Thin Film Observed by in Situ Transmission Electron Microscopy Zheng, Haimei; Claridge, Shelley A.; Minor, Andrew M. Nano Letters, Vol. 9, Issue 6 https://doi.org/10.1021/nl9012369	journal	June 2009
Correlations between ionization radiation damage and charging effects in transmission electron microscopy Cazaux, J. Ultramicroscopy, Vol. 60, Issue 3 https://doi.org/10.1016/0304-3991(95)00077-1	journal	October 1995
Experimental procedures to mitigate electron beam induced artifacts during in situ fluid imaging of nanomaterials Woehl, Taylor J.; Jungjohann, Katherine L.; Evans, James E. Ultramicroscopy, Vol. 127 https://doi.org/10.1016/j.ultramic.2012.07.018	journal	April 2013
Charged Nanoparticle Dynamics in Water Induced by Scanning Transmission Electron Microscopy White, E. R.; Mecklenburg, Matthew; Shevitski, Brian Langmuir, Vol. 28, Issue 8 https://doi.org/10.1021/la2048486	journal	February 2012
In situ liquid-cell electron microscopy of silver–palladium galvanic replacement reactions on silver nanoparticles Sutter, E.; Jungjohann, K.; Bliznakov, S. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5946	journal	September 2014
Interaction Potentials of Anisotropic Nanocrystals from the Trajectory Sampling of Particle Motion using in Situ Liquid Phase Transmission Electron Microscopy Chen, Qian; Cho, Hoduk; Manthiram, Karthish ACS Central Science, Vol. 1, Issue 1 https://doi.org/10.1021/acscentsci.5b00001	journal	March 2015
Antioxidant chemistry of graphene-based materials and its role in oxidation protection technology Qiu, Yang; Wang, Zhongying; Owens, Alisa C. E. Nanoscale, Vol. 6, Issue 20 https://doi.org/10.1039/C4NR03275F	journal	January 2014
Making Graphene Holey . Gold-Nanoparticle-Mediated Hydroxyl Radical Attack on Reduced Graphene Oxide Radich, James G.; Kamat, Prashant V. ACS Nano, Vol. 7, Issue 6 https://doi.org/10.1021/nn401794k	journal	May 2013
Engineering nano-porous graphene oxide by hydroxyl radicals Yu, Chuhong; Zhang, Bowu; Yan, Feng Carbon, Vol. 105 https://doi.org/10.1016/j.carbon.2016.04.050	journal	August 2016
Crossover between Anti- and Pro-oxidant Activities of Graphene Quantum Dots in the Absence or Presence of Light Chong, Yu; Ge, Cuicui; Fang, Ge ACS Nano, Vol. 10, Issue 9 https://doi.org/10.1021/acsnano.6b04061	journal	September 2016
Mammalian Cells Are Not Killed by DNA Single-Strand Breaks Caused by Hydroxyl Radicals from Hydrogen Peroxide Ward, John F.; Blakely, William F.; Joner, Eva I. Radiation Research, Vol. 103, Issue 3 https://doi.org/10.2307/3576760	journal	September 1985
Single- and Double-Strand Break Formation in DNA Irradiated in Aqueous Solution: Dependence on Dose and OH Radical Scavenger Concentration Siddiqi, M. Aslam; Bothe, E. Radiation Research, Vol. 112, Issue 3 https://doi.org/10.2307/3577098	journal	December 1987
Radiation Chemical Mechanisms of Single- and Double-Strand Break Formation in Irradiated SV40 DNA Krisch, Robert E.; Flick, Maryann B.; Trumbore, Conrad N. Radiation Research, Vol. 126, Issue 2 https://doi.org/10.2307/3577826	journal	May 1991
Graphene oxide as a chemically tunable platform for optical applications Loh, Kian Ping; Bao, Qiaoliang; Eda, Goki Nature Chemistry, Vol. 2, Issue 12 https://doi.org/10.1038/nchem.907	journal	November 2010

Cited By (11)

In Situ Transmission Electron Microscopy Study of Nanocrystal Formation for Electrocatalysis Shi, Fenglei; Li, Fan; Ma, Yanling ChemNanoMat, Vol. 5, Issue 12 https://doi.org/10.1002/cnma.201900497	journal	October 2019
Liquid-Phase Transmission Electron Microscopy for Studying Colloidal Inorganic Nanoparticles Kim, Byung Hyo; Yang, Jiwoong; Lee, Donghoon Advanced Materials, Vol. 30, Issue 4 https://doi.org/10.1002/adma.201703316	journal	November 2017
Improving in situ liquid SEM imaging of particles Yu, Xiao‐Ying; Arey, Bruce; Chatterjee, Sayandev Surface and Interface Analysis, Vol. 51, Issue 13 https://doi.org/10.1002/sia.6700	journal	September 2019
State-of-the-Art and Future Prospects for Atomically Thin Membranes from 2D Materials Prozorovska, Liudmyla; Kidambi, Piran R. Advanced Materials, Vol. 30, Issue 52 https://doi.org/10.1002/adma.201801179	journal	August 2018
Graphene Liquid Cells Assembled through Loop‐Assisted Transfer Method and Located with Correlated Light‐Electron Microscopy Deursen, Pauline M. G.; Koning, Roman I.; Tudor, Viorica Advanced Functional Materials, Vol. 30, Issue 11 https://doi.org/10.1002/adfm.201904468	journal	February 2020
Advances in Graphene‐Based Liquid Cell Electron Microscopy: Working Principles, Opportunities, and Challenges Ghodsi, Seyed Mohammadreza; Megaridis, Constantine M.; Shahbazian‐Yassar, Reza Small Methods, Vol. 3, Issue 5 https://doi.org/10.1002/smtd.201900026	journal	January 2019
Transmission electron microscopy of the iron oxide core in ferritin proteins: current status and future directions Narayanan, Surya; Shahbazian-Yassar, Reza; Shokuhfar, Tolou Journal of Physics D: Applied Physics, Vol. 52, Issue 45 https://doi.org/10.1088/1361-6463/ab353b	journal	August 2019
Localized corrosion of low-carbon steel at the nanoscale Hayden, Steven C.; Chisholm, Claire; Grudt, Rachael O. npj Materials Degradation, Vol. 3, Issue 1 https://doi.org/10.1038/s41529-019-0078-1	journal	April 2019
Investigation of the magnetosome biomineralization in magnetotactic bacteria using graphene liquid cell – transmission electron microscopy Firlar, Emre; Ouy, Meagan; Bogdanowicz, Agata Nanoscale, Vol. 11, Issue 2 https://doi.org/10.1039/c8nr08647h	journal	January 2019
Liquid electron microscopy: then, now and future Bharda, Anahita Vispi; Jung, Hyun Suk Applied Microscopy, Vol. 49, Issue 1 https://doi.org/10.1186/s42649-019-0011-7	journal	October 2019
On the structure and chemistry of iron oxide cores in human heart and human spleen ferritins using graphene liquid cell electron microscopy Narayanan, Surya; Firlar, Emre; Rasul, Md Golam Nanoscale, Vol. 11, Issue 36 https://doi.org/10.1039/c9nr01541h	journal	January 2019

Similar Records

Photon-In/Photon-Out X-ray Free-Electron Laser Studies of Radiolysis

Journal Article · Wed Jan 13 00:00:00 EST 2021 · Applied Sciences · OSTI ID:1532216

Young, Linda; Nienhuis, Emily T.; Koulentianos, Dimitris; +7 more

Radiolysis of DNA and other biopolymers

Conference · Sun Jul 01 00:00:00 EDT 1979 · Int. J. Radiat. Oncol., Biol. Phys.; (United States) · OSTI ID:1532216

Myers, Jr, L S; Kay, E

An evidence on G2/M arrest, DNA damage and caspase mediated apoptotic effect of biosynthesized gold nanoparticles on human cervical carcinoma cells (HeLa)

Journal Article · Tue Apr 01 00:00:00 EDT 2014 · Materials Research Bulletin · OSTI ID:1532216

Jeyaraj, M.; Arun, R.; Sathishkumar, G.; +6 more

Related Subjects

36 MATERIALS SCIENCE
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
Liquid-phase TEM
graphene liquid cell
DNA nanotechnology
bioimaging
radical scavenger
radiation damage

Title: The Use of Graphene and Its Derivatives for Liquid-Phase Transmission Electron Microscopy of Radiation-Sensitive Specimens

Citation Formats

References (53)

Cited By (11)

Similar Records

Related Subjects