Bent DNA Bows as Sensing Amplifiers for Detecting DNA-Interacting Salts and Molecules

Freeland, Jack; Zhang, Lihua; Wang, Shih-Ting; Ruiz, Mason; Wang, Yong

doi:10.3390/s20113112

Title: Bent DNA Bows as Sensing Amplifiers for Detecting DNA-Interacting Salts and Molecules

Journal Article · 31 May 2020 · Sensors

DOI: https://doi.org/10.3390/s20113112 · OSTI ID:1631488

Freeland, Jack ^[1]; Zhang, Lihua ^[2];

^[2]; Ruiz, Mason ^[1];

^[1]

Univ. of Arkansas, Fayetteville, AR (United States)
Brookhaven National Lab. (BNL), Upton, NY (United States)

Due to the central role of DNA, its interactions with inorganic salts and small organic molecules are important. For example, such interactions play important roles in various fundamental cellular processes in living systems and are involved in many DNA-damage related diseases. Strategies to improve the sensitivity of existing techniques for studying DNA interactions with other molecules would be appreciated in situations where the interactions are too weak. Here we report our development and demonstration of bent DNA bows for amplifying, sensing, and detecting the interactions of 14 inorganic salts and small organic molecules with DNA. With the bent DNA bows, these interactions were easily visualized and quantified in gel electrophoresis, which were difficult to measure without bending. In addition, the strength of the interactions of DNA with the various salts/molecules were quantified using the modified Hill equation. This work highlights the amplification effects of the bending elastic energy stored in the DNA bows and the potential use of the DNA bows for quantitatively measuring DNA interactions with small molecules as simple economic methods; it may also pave the way for exploiting the bent DNA bows for other applications such as screening DNA-interacting molecules and drugs.

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Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); Univ. of Arkansas; Arkansas Department of Higher Education; National Science Foundation (NSF)

Grant/Contract Number:: SC0012704; ABI-0189; ABI-0226; ABI-0277; ABI-0326; 003049-00001A; 38596; 1826642

OSTI ID:: 1631488

Alternate ID(s):: OSTI ID: 1661640

Report Number(s):: BNL-219827-2020-JAAM

Journal Information:: Sensors, Vol. 20, Issue 11; ISSN 1424-8220

Publisher:: MDPI AGCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 1 work

Citation information provided by
Web of Science

References (112)

Understanding Nucleic Acid–Ion Interactions Lipfert, Jan; Doniach, Sebastian; Das, Rhiju Annual Review of Biochemistry, Vol. 83, Issue 1 https://doi.org/10.1146/annurev-biochem-060409-092720	journal	June 2014
DNA aggregation induced by Mg ²⁺ ions under different conditions Bui, Van-Chien; Nguyen, Thi-Huong Journal of Molecular Recognition, Vol. 31, Issue 9 https://doi.org/10.1002/jmr.2721	journal	May 2018
Magnesium ions enhance infiltration of osteoblasts in scaffolds via increasing cell motility Kim, Ki-Jung; Choi, Sunkyung; Sang Cho, Yong Journal of Materials Science: Materials in Medicine, Vol. 28, Issue 6 https://doi.org/10.1007/s10856-017-5908-5	journal	May 2017
Ions and RNA Folding Draper, David E.; Grilley, Dan; Soto, Ana Maria Annual Review of Biophysics and Biomolecular Structure, Vol. 34, Issue 1 https://doi.org/10.1146/annurev.biophys.34.040204.144511	journal	June 2005
Critical Role of Magnesium Ions in DNA Polymerase β's Closing and Active Site Assembly Yang, Linjing; Arora, Karunesh; Beard, William A. Journal of the American Chemical Society, Vol. 126, Issue 27 https://doi.org/10.1021/ja049412o	journal	July 2004
Unraveling the three-metal-ion catalytic mechanism of the DNA repair enzyme endonuclease IV Ivanov, I.; Tainer, J. A.; McCammon, J. A. Proceedings of the National Academy of Sciences, Vol. 104, Issue 5 https://doi.org/10.1073/pnas.0603468104	journal	January 2007
Role of magnesium in genomic stability Hartwig, Andrea Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 475, Issue 1-2 https://doi.org/10.1016/S0027-5107(01)00074-4	journal	April 2001
Magnesium–DNA interactions and the possible relation of magnesium to carcinogenesis. Irradiation and free radicals Anastassopoulou, J.; Theophanides, T. Critical Reviews in Oncology/Hematology, Vol. 42, Issue 1 https://doi.org/10.1016/S1040-8428(02)00006-9	journal	April 2002
Effects of copper ions on DNA binding and cytotoxic activity of a chiral salicylidene Schiff base Fei, Bao-Li; Xu, Wu-Shuang; Tao, Hui-Wen Journal of Photochemistry and Photobiology B: Biology, Vol. 132 https://doi.org/10.1016/j.jphotobiol.2014.01.018	journal	March 2014
Interference by toxic metal ions with DNA repair processes and cell cycle control: molecular mechanisms. Hartwig, A.; Asmuss, M.; Ehleben, I. Environmental Health Perspectives, Vol. 110, Issue suppl 5 https://doi.org/10.1289/ehp.02110s5797	journal	October 2002
Interference by toxic metal compounds with isolated zinc finger DNA repair proteins Asmuß, Monika; Mullenders, Leon H. F.; Hartwig, Andrea Toxicology Letters, Vol. 112-113 https://doi.org/10.1016/S0378-4274(99)00273-8	journal	March 2000
Molecular dynamics study on DNA nanotubes as drug delivery vehicle for anticancer drugs Liang, Lijun; Shen, Jia-Wei; Wang, Qi Colloids and Surfaces B: Biointerfaces, Vol. 153 https://doi.org/10.1016/j.colsurfb.2017.02.021	journal	May 2017
DNA as a target for anticancer compounds: methods to determine the mode of binding and the mechanism of action Palchaudhuri, Rahul; Hergenrother, Paul J. Current Opinion in Biotechnology, Vol. 18, Issue 6 https://doi.org/10.1016/j.copbio.2007.09.006	journal	December 2007
DNA and its associated processes as targets for cancer therapy Hurley, Laurence H. Nature Reviews Cancer, Vol. 2, Issue 3 https://doi.org/10.1038/nrc749	journal	March 2002
Intercalation of antitumor drug doxorubicin and its analogue by DNA duplex: Structural features and biological implications Agudelo, Daniel; Bourassa, Philippe; Bérubé, Gervais International Journal of Biological Macromolecules, Vol. 66 https://doi.org/10.1016/j.ijbiomac.2014.02.028	journal	May 2014
Stretching DNA with optical tweezers Wang, M. D.; Yin, H.; Landick, R. Biophysical Journal, Vol. 72, Issue 3 https://doi.org/10.1016/S0006-3495(97)78780-0	journal	March 1997
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
Ionic effects on the elasticity of single DNA molecules Baumann, C. G.; Smith, S. B.; Bloomfield, V. A. Proceedings of the National Academy of Sciences, Vol. 94, Issue 12 https://doi.org/10.1073/pnas.94.12.6185	journal	June 1997
Dual Binding Modes for an HMG Domain from Human HMGB2 on DNA McCauley, Micah; Hardwidge, Philip R.; Maher, L. James Biophysical Journal, Vol. 89, Issue 1 https://doi.org/10.1529/biophysj.104.052068	journal	July 2005
Force-Induced Melting of the DNA Double Helix 1. Thermodynamic Analysis Rouzina, Ioulia; Bloomfield, Victor A. Biophysical Journal, Vol. 80, Issue 2 https://doi.org/10.1016/S0006-3495(01)76067-5	journal	February 2001
Force-Induced Melting of the DNA Double Helix. 2. Effect of Solution Conditions Rouzina, Ioulia; Bloomfield, Victor A. Biophysical Journal, Vol. 80, Issue 2 https://doi.org/10.1016/S0006-3495(01)76068-7	journal	February 2001
Sequence-Dependent DNA Curvature and Flexibility from Scanning Force Microscopy Images Scipioni, Anita; Anselmi, Claudio; Zuccheri, Giampaolo Biophysical Journal, Vol. 83, Issue 5 https://doi.org/10.1016/S0006-3495(02)75254-5	journal	November 2002
Determination of thermodynamics and kinetics of RNA reactions by force Tinoco, Ignacio; T. X. Li, Pan; Bustamante, Carlos Quarterly Reviews of Biophysics, Vol. 39, Issue 4 https://doi.org/10.1017/S0033583506004446	journal	October 2006
Studies of DNA-protein interactions by gel electrophoresis Ceglarek, John A.; Revzin, Arnold Electrophoresis, Vol. 10, Issue 5-6 https://doi.org/10.1002/elps.1150100514	journal	January 1989
A gel electrophoresis method for quantifying the binding of proteins to specific DNA regions: application to components of the Escherichia coli lactose operon regulatory system Garner, Mark M.; Revzin, Arnold Nucleic Acids Research, Vol. 9, Issue 13 https://doi.org/10.1093/nar/9.13.3047	journal	January 1981
Circular dichroism to determine binding mode and affinity of ligand–DNA interactions Garbett, Nichola C.; Ragazzon, Patricia A.; Chaires, Jonathan B. Nature Protocols, Vol. 2, Issue 12 https://doi.org/10.1038/nprot.2007.475	journal	December 2007
Advances in the analysis of isothermal titration calorimetry data for ligand–DNA interactions Buurma, Niklaas J.; Haq, Ihtshamul Methods, Vol. 42, Issue 2 https://doi.org/10.1016/j.ymeth.2007.01.010	journal	June 2007
Electron Paramagnetic Resonance as a Tool for Studying the Mechanisms of Paramagnetic Anticancer Metallodrugs: Electron Paramagnetic Resonance as a Tool for Studying the Mechanisms of Paramagnetic Anticancer Metallodrugs Prosser, Kathleen E.; Walsby, Charles J. European Journal of Inorganic Chemistry, Vol. 2017, Issue 12 https://doi.org/10.1002/ejic.201601142	journal	December 2016
Raman spectroscopy of DNA-metal complexes. II. The thermal denaturation of DNA in the presence of Sr2+, Ba2+, Mg2+, Ca2+, Mn2+, Co2+, Ni2+, and Cd2+ Duguid, J. G.; Bloomfield, V. A.; Benevides, J. M. Biophysical Journal, Vol. 69, Issue 6 https://doi.org/10.1016/S0006-3495(95)80133-5	journal	December 1995
Nuclear magnetic resonance analysis of protein–DNA interactions Campagne, S.; Gervais, V.; Milon, A. Journal of The Royal Society Interface, Vol. 8, Issue 61 https://doi.org/10.1098/rsif.2010.0543	journal	January 2011
The elastic energy of sharply bent nicked DNA Qu, Hao; Tseng, Chiao-Yu; Wang, Yong EPL (Europhysics Letters), Vol. 90, Issue 1 https://doi.org/10.1209/0295-5075/90/18003	journal	April 2010
The complete bending energy function for nicked DNA Qu, Hao; Zocchi, Giovanni EPL (Europhysics Letters), Vol. 94, Issue 1 https://doi.org/10.1209/0295-5075/94/18003	journal	March 2011
Mechanical-energy-based amplifiers for probing interactions of DNA with metal ions Freeland, Jack; Khadka, Prabhat; Wang, Yong Physical Review E, Vol. 98, Issue 6 https://doi.org/10.1103/PhysRevE.98.062403	journal	December 2018
Critical Torque for Kink Formation in Double-Stranded DNA Qu, Hao; Wang, Yong; Tseng, Chiao-Yu Physical Review X, Vol. 1, Issue 2 https://doi.org/10.1103/PhysRevX.1.021008	journal	November 2011
Mechanochemistry: The Mechanical Activation of Covalent Bonds Beyer, Martin K.; Clausen-Schaumann, Hauke Chemical Reviews, Vol. 105, Issue 8 https://doi.org/10.1021/cr030697h	journal	August 2005
Biasing reaction pathways with mechanical force Hickenboth, Charles R.; Moore, Jeffrey S.; White, Scott R. Nature, Vol. 446, Issue 7134 https://doi.org/10.1038/nature05681	journal	March 2007
Fiji: an open-source platform for biological-image analysis Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2019	journal	June 2012
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
The structure of DNA by direct imaging Marini, Monica; Falqui, Andrea; Moretti, Manola Science Advances, Vol. 1, Issue 7 https://doi.org/10.1126/sciadv.1500734	journal	August 2015
DNA curvature and flexibility in vitro and in vivo Peters, Justin P.; Maher, L. James Quarterly Reviews of Biophysics, Vol. 43, Issue 1 https://doi.org/10.1017/S0033583510000077	journal	February 2010
The effects of lithium, rubidium, cesium and magnesium ions on the close packing of persistence-length DNA fragments Trohalaki, S.; Frisch, H. L.; Lerman, L. S. Biophysical Chemistry, Vol. 40, Issue 2 https://doi.org/10.1016/0301-4622(91)87009-T	journal	May 1991
A multi‐level response to DNA damage induced by aluminium Chen, Poyu; Sjogren, Caroline A.; Larsen, Paul B. The Plant Journal, Vol. 98, Issue 3 https://doi.org/10.1111/tpj.14231	journal	March 2019
A comet assay study reveals that aluminium induces DNA damage and inhibits the repair of radiation-induced lesions in human peripheral blood lymphocytes Lankoff, Anna; Banasik, Anna; Duma, Anna Toxicology Letters, Vol. 161, Issue 1 https://doi.org/10.1016/j.toxlet.2005.07.012	journal	February 2006
Effects of Zinc Supplementation on DNA Damage in Rats with Experimental Kidney Deficiency Yegin, Sevim Çiftçi; Dede, Semiha; Mis, Leyla Biological Trace Element Research, Vol. 176, Issue 2 https://doi.org/10.1007/s12011-016-0826-9	journal	September 2016
DNA interaction with zinc(II) ions Nejdl, Lukas; Ruttkay-Nedecky, Branislav; Kudr, Jiri International Journal of Biological Macromolecules, Vol. 64 https://doi.org/10.1016/j.ijbiomac.2013.12.013	journal	March 2014
Toxicity of silver ions, metallic silver, and silver nanoparticle materials after in vivo dermal and mucosal surface exposure: A review Hadrup, Niels; Sharma, Anoop K.; Loeschner, Katrin Regulatory Toxicology and Pharmacology, Vol. 98 https://doi.org/10.1016/j.yrtph.2018.08.007	journal	October 2018
Role of potassium in regulating blood flow and blood pressure Haddy, Francis J.; Vanhoutte, Paul M.; Feletou, Michel American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, Vol. 290, Issue 3 https://doi.org/10.1152/ajpregu.00491.2005	journal	March 2006
Potassium Channels: Structures, Diseases, and Modulators Tian, Chuan; Zhu, Ruixin; Zhu, Lixin Chemical Biology & Drug Design, Vol. 83, Issue 1 https://doi.org/10.1111/cbdd.12237	journal	December 2013
Calcium Signaling Clapham, David E. Cell, Vol. 131, Issue 6 https://doi.org/10.1016/j.cell.2007.11.028	journal	December 2007
Assessment of DNA damage and molecular responses in Labeo rohita (Hamilton, 1822) following short-term exposure to silver nanoparticles Sharma, Niti; Rather, Mohd Ashraf; Ajima, Malachy N. O. Food and Chemical Toxicology, Vol. 96 https://doi.org/10.1016/j.fct.2016.06.020	journal	October 2016
A mechanistic study of the antibacterial effect of silver ions onEscherichia coli andStaphylococcus aureus Feng, Q. L.; Wu, J.; Chen, G. Q. Journal of Biomedical Materials Research, Vol. 52, Issue 4 https://doi.org/10.1002/1097-4636(20001215)52:4<662::AID-JBM10>3.0.CO;2-3	journal	January 2000
The Hill equation and the origin of quantitative pharmacology Gesztelyi, Rudolf; Zsuga, Judit; Kemeny-Beke, Adam Archive for History of Exact Sciences, Vol. 66, Issue 4 https://doi.org/10.1007/s00407-012-0098-5	journal	March 2012
Identifying Chaotropic and Kosmotropic Agents by Nanorheology Casanova-Morales, Nathalie; Alavi, Zahra; Wilson, Christian A. M. The Journal of Physical Chemistry B, Vol. 122, Issue 14 https://doi.org/10.1021/acs.jpcb.7b12782	journal	March 2018
Understanding the Guanidine-Like Cationic Moiety for Optimal Binding into the DNA Minor Groove O'Sullivan, Patrick; Rozas, Isabel ChemMedChem, Vol. 9, Issue 9 https://doi.org/10.1002/cmdc.201402264	journal	August 2014
Biophysical characterization of the DNA interaction with the biogenic polyamine putrescine: A single molecule study Publio, B. C.; Moura, T. A.; Lima, C. H. M. International Journal of Biological Macromolecules, Vol. 112 https://doi.org/10.1016/j.ijbiomac.2018.01.142	journal	June 2018
Structural determinants of spermidine-DNA interactions Vertino, Paula M.; Bergeron, R. J.; Cavanaugh, Paul F. Biopolymers, Vol. 26, Issue 5 https://doi.org/10.1002/bip.360260510	journal	May 1987
Synthesis of a novel 4H-pyran analog as minor groove binder to DNA using ethidium bromide as fluorescence probe Ramana, M. M. V.; Betkar, Rahul; Nimkar, Amey Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, Vol. 152 https://doi.org/10.1016/j.saa.2015.07.037	journal	January 2016
Development of a SYBR safe™ technique for the sensitive detection of DNA in cesium chloride density gradients for stable isotope probing assays Martineau, Christine; Whyte, Lyle G.; Greer, Charles W. Journal of Microbiological Methods, Vol. 73, Issue 2 https://doi.org/10.1016/j.mimet.2008.01.016	journal	May 2008
Inhibition of DNA-ethidium bromide intercalation due to free radical attack upon DNA: II. Copper(II)-Catalysed DNA Damage by O 2 ? ? Pr�tz, Walter A. Radiation and Environmental Biophysics, Vol. 23, Issue 1 https://doi.org/10.1007/BF01326732	journal	March 1984
Inhibition by ganciclovir of cell growth and DNA synthesis of cells biochemically transformed with herpesvirus genetic information. St Clair, M. H.; Lambe, C. U.; Furman, P. A. Antimicrobial Agents and Chemotherapy, Vol. 31, Issue 6 https://doi.org/10.1128/AAC.31.6.844	journal	June 1987
Ganciclovir Inhibits Lymphocyte Proliferation by Impairing DNA Synthesis Battiwalla, Minoo; Wu, Yiyuan; Bajwa, Rajinder P. S. Biology of Blood and Marrow Transplantation, Vol. 13, Issue 7 https://doi.org/10.1016/j.bbmt.2007.03.009	journal	July 2007
Thiamine Deprivation Produces a Liver ATP Deficit and Metabolic and Genomic Effects in Mice: Findings Are Parallel to Those of Biotin Deficiency and Have Implications for Energy Disorders Hernandez-Vazquez, Alain de J.; Garcia-Sanchez, Josue Andres; Moreno-Arriola, Elizabeth Journal of Nutrigenetics and Nutrigenomics, Vol. 9, Issue 5-6 https://doi.org/10.1159/000456663	journal	January 2016
Study on the effect of thiamine on the metabolism of yeast by intrinsic fluorescence Wang, Jun; Cai, Ruxiu; Xu, Jing Luminescence, Vol. 20, Issue 3 https://doi.org/10.1002/bio.822	journal	January 2005
Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression Winkler, Wade; Nahvi, Ali; Breaker, Ronald R. Nature, Vol. 419, Issue 6910 https://doi.org/10.1038/nature01145	journal	October 2002
Silver Ions Caused Faster Diffusive Dynamics of Histone-Like Nucleoid-Structuring Proteins in Live Bacteria Sadoon, Asmaa A.; Khadka, Prabhat; Freeland, Jack Applied and Environmental Microbiology, Vol. 86, Issue 6 https://doi.org/10.1128/AEM.02479-19	journal	January 2020
Therapies targeting DNA and RNA in Huntington's disease Wild, Edward J.; Tabrizi, Sarah J. The Lancet Neurology, Vol. 16, Issue 10 https://doi.org/10.1016/S1474-4422(17)30280-6	journal	October 2017
Transition Metal-based Anticancer Drugs Targeting Nucleic Acids: A Tandem Mass Spectrometric Investigation Eberle, RahelP.; Hari, Yvonne; Schürch, Stefan CHIMIA International Journal for Chemistry, Vol. 71, Issue 3 https://doi.org/10.2533/chimia.2017.120	journal	March 2017
Extreme Bendability of DNA Less than 100 Base Pairs Long Revealed by Single-Molecule Cyclization Vafabakhsh, R.; Ha, T. Science, Vol. 337, Issue 6098 https://doi.org/10.1126/science.1224139	journal	August 2012
Cyclization of short DNA fragments and bending fluctuations of the double helix Du, Q.; Smith, C.; Shiffeldrim, N. Proceedings of the National Academy of Sciences, Vol. 102, Issue 15 https://doi.org/10.1073/pnas.0500983102	journal	April 2005
Application of the method of phage T4 DNA ligase-catalyzed ring-closure to the study of DNA structure Hagerman, Paul J.; Ramadevi, V. A. Journal of Molecular Biology, Vol. 212, Issue 2 https://doi.org/10.1016/0022-2836(90)90130-E	journal	March 1990
Protein-induced bending and DNA cyclization. Kahn, J. D.; Crothers, D. M. Proceedings of the National Academy of Sciences, Vol. 89, Issue 14 https://doi.org/10.1073/pnas.89.14.6343	journal	July 1992
Multimerization-Cyclization of DNA Fragments as a Method of Conformational Analysis Podtelezhnikov, Alexei A.; Mao, Chengde; Seeman, Nadrian C. Biophysical Journal, Vol. 79, Issue 5 https://doi.org/10.1016/S0006-3495(00)76507-6	journal	November 2000
DNA flexibility studied by covalent closure of short fragments into circles. Shore, D.; Langowski, J.; Baldwin, R. L. Proceedings of the National Academy of Sciences, Vol. 78, Issue 8 https://doi.org/10.1073/pnas.78.8.4833	journal	August 1981
Application of the method of phage T4 DNA ligase-catalyzed ring-closure to the study of DNA structure Taylor, William H.; Hagerman, Paul J. Journal of Molecular Biology, Vol. 212, Issue 2 https://doi.org/10.1016/0022-2836(90)90131-5	journal	March 1990
Contribution of the intrinsic curvature to measured DNA persistence length Vologodskaia, Maria; Vologodskii, Alexander Journal of Molecular Biology, Vol. 317, Issue 2 https://doi.org/10.1006/jmbi.2001.5366	journal	March 2002
High-throughput approach for detection of DNA bending and flexibility based on cyclization Zhang, Y.; Crothers, D. M. Proceedings of the National Academy of Sciences, Vol. 100, Issue 6 https://doi.org/10.1073/pnas.0530189100	journal	March 2003
Ring-closure probabilities for twisted wormlike chains. Application to DNA Shimada, Jiro; Yamakawa, Hiromi Macromolecules, Vol. 17, Issue 4 https://doi.org/10.1021/ma00134a028	journal	July 1984
Euler buckling and nonlinear kinking of double-stranded DNA Fields, Alexander P.; Meyer, Elisabeth A.; Cohen, Adam E. Nucleic Acids Research, Vol. 41, Issue 21 https://doi.org/10.1093/nar/gkt739	journal	August 2013
DNA gel electrophoresis: The reptation model(s) Slater, Gary W. ELECTROPHORESIS, Vol. 30, Issue S1 https://doi.org/10.1002/elps.200900154	journal	June 2009
Electrophoresis of DNA in agarose gels, polyacrylamide gels and in free solution Stellwagen, Nancy C. ELECTROPHORESIS, Vol. 30, Issue S1 https://doi.org/10.1002/elps.200900052	journal	June 2009
Modeling the Dynamics of Gel Electrophorresis in the High School Classroom Saucedo, Skyler R. The Physics Teacher, Vol. 51, Issue 1 https://doi.org/10.1119/1.4772034	journal	January 2013
Bending of DNA by gene-regulatory proteins: construction and use of a DNA bending vector Kim, Jin; Zwieb, Christian; Wu, Carl Gene, Vol. 85, Issue 1 https://doi.org/10.1016/0378-1119(89)90459-9	journal	December 1989
Revisiting the Anomalous Bending Elasticity of Sharply Bent DNA Cong, Peiwen; Dai, Liang; Chen, Hu Biophysical Journal, Vol. 109, Issue 11 https://doi.org/10.1016/j.bpj.2015.10.016	journal	December 2015
Structural basis for preferential binding of H-NS to curved DNA Thei Dame, Remus; Wyman, Claire; Goosen, Nora Biochimie, Vol. 83, Issue 2 https://doi.org/10.1016/S0300-9084(00)01213-X	journal	February 2001
An Escherichia coli Protein That Preferentially Binds to Sharply Curved DNA1 Yamada, Hisami; Muramatsu, Shuji; Mizuno, Takeshi The Journal of Biochemistry, Vol. 108, Issue 3 https://doi.org/10.1093/oxfordjournals.jbchem.a123216	journal	September 1990
Base-Pair Mismatch Can Destabilize Small DNA Loops through Cooperative Kinking Jeong, Jiyoun; Kim, Harold D. Physical Review Letters, Vol. 122, Issue 21 https://doi.org/10.1103/PhysRevLett.122.218101	journal	May 2019
Single-Molecule Conformational Analysis of G-Quadruplex Formation in the Promoter DNA Duplex of the Proto-Oncogene C-Kit Shirude, Pravin S.; Okumus, Burak; Ying, Liming Journal of the American Chemical Society, Vol. 129, Issue 24 https://doi.org/10.1021/ja070497d	journal	June 2007
Extreme conformational diversity in human telomeric DNA Lee, J. Y.; Okumus, B.; Kim, D. S. Proceedings of the National Academy of Sciences, Vol. 102, Issue 52 https://doi.org/10.1073/pnas.0506144102	journal	December 2005
Determinants of cyclization–decyclization kinetics of short DNA with sticky ends Jeong, Jiyoun; Kim, Harold D. Nucleic Acids Research, Vol. 48, Issue 9 https://doi.org/10.1093/nar/gkaa207	journal	April 2020
Single-molecule fluorescence studies on DNA looping Jeong, Jiyoun; Le, Tung T.; Kim, Harold D. Methods, Vol. 105 https://doi.org/10.1016/j.ymeth.2016.04.005	journal	August 2016
Studies of DNA-protein interactions by gel electrophoresis Ceglarek, John A.; Revzin, Arnold Electrophoresis, Vol. 10, Issue 5-6 https://doi.org/10.1002/elps.1150100514	journal	January 1989
Contribution of the intrinsic curvature to measured DNA persistence length Vologodskaia, Maria; Vologodskii, Alexander Journal of Molecular Biology, Vol. 317, Issue 2 https://doi.org/10.1006/jmbi.2001.5366	journal	March 2002
Heavy Metal Toxicity and the Environment Tchounwou, Paul B.; Yedjou, Clement G.; Patlolla, Anita K. Experientia Supplementum https://doi.org/10.1007/978-3-7643-8340-4_6	book	January 2012
Effects of Zinc Supplementation on DNA Damage in Rats with Experimental Kidney Deficiency Yegin, Sevim Çiftçi; Dede, Semiha; Mis, Leyla Biological Trace Element Research, Vol. 176, Issue 2 https://doi.org/10.1007/s12011-016-0826-9	journal	September 2016
Bending of DNA by gene-regulatory proteins: construction and use of a DNA bending vector Kim, Jin; Zwieb, Christian; Wu, Carl Gene, Vol. 85, Issue 1 https://doi.org/10.1016/0378-1119(89)90459-9	journal	December 1989
Ganciclovir Inhibits Lymphocyte Proliferation by Impairing DNA Synthesis Battiwalla, Minoo; Wu, Yiyuan; Bajwa, Rajinder P. S. Biology of Blood and Marrow Transplantation, Vol. 13, Issue 7 https://doi.org/10.1016/j.bbmt.2007.03.009	journal	July 2007
DNA as a target for anticancer compounds: methods to determine the mode of binding and the mechanism of action Palchaudhuri, Rahul; Hergenrother, Paul J. Current Opinion in Biotechnology, Vol. 18, Issue 6 https://doi.org/10.1016/j.copbio.2007.09.006	journal	December 2007
Assessment of DNA damage and molecular responses in Labeo rohita (Hamilton, 1822) following short-term exposure to silver nanoparticles Sharma, Niti; Rather, Mohd Ashraf; Ajima, Malachy N. O. Food and Chemical Toxicology, Vol. 96 https://doi.org/10.1016/j.fct.2016.06.020	journal	October 2016
Synthesis of a novel 4H-pyran analog as minor groove binder to DNA using ethidium bromide as fluorescence probe Ramana, M. M. V.; Betkar, Rahul; Nimkar, Amey Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, Vol. 152 https://doi.org/10.1016/j.saa.2015.07.037	journal	January 2016
Single-Molecule Conformational Analysis of G-Quadruplex Formation in the Promoter DNA Duplex of the Proto-Oncogene C-Kit Shirude, Pravin S.; Okumus, Burak; Ying, Liming Journal of the American Chemical Society, Vol. 129, Issue 24 https://doi.org/10.1021/ja070497d	journal	June 2007
Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression Winkler, Wade; Nahvi, Ali; Breaker, Ronald R. Nature, Vol. 419, Issue 6910 https://doi.org/10.1038/nature01145	journal	October 2002
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
DNA flexibility studied by covalent closure of short fragments into circles. Shore, D.; Langowski, J.; Baldwin, R. L. Proceedings of the National Academy of Sciences, Vol. 78, Issue 8 https://doi.org/10.1073/pnas.78.8.4833	journal	August 1981
Protein-induced bending and DNA cyclization. Kahn, J. D.; Crothers, D. M. Proceedings of the National Academy of Sciences, Vol. 89, Issue 14 https://doi.org/10.1073/pnas.89.14.6343	journal	July 1992
Euler buckling and nonlinear kinking of double-stranded DNA Fields, Alexander P.; Meyer, Elisabeth A.; Cohen, Adam E. Nucleic Acids Research, Vol. 41, Issue 21 https://doi.org/10.1093/nar/gkt739	journal	August 2013
Nuclear magnetic resonance analysis of protein–DNA interactions Campagne, S.; Gervais, V.; Milon, A. Journal of The Royal Society Interface, Vol. 8, Issue 61 https://doi.org/10.1098/rsif.2010.0543	journal	January 2011
The structure of DNA by direct imaging Marini, Monica; Falqui, Andrea; Moretti, Manola Science Advances, Vol. 1, Issue 7 https://doi.org/10.1126/sciadv.1500734	journal	August 2015
Extreme Bendability of DNA Less than 100 Base Pairs Long Revealed by Single-Molecule Cyclization Vafabakhsh, R.; Ha, T. Science, Vol. 337, Issue 6098 https://doi.org/10.1126/science.1224139	journal	August 2012
The complete bending energy function for nicked DNA Qu, Hao; Zocchi, Giovanni EPL (Europhysics Letters), Vol. 94, Issue 1 https://doi.org/10.1209/0295-5075/94/18003	journal	March 2011
Interference by toxic metal ions with DNA repair processes and cell cycle control: molecular mechanisms. Hartwig, A.; Asmuss, M.; Ehleben, I. Environmental Health Perspectives, Vol. 110, Issue suppl 5 https://doi.org/10.1289/ehp.02110s5797	journal	October 2002
Dual Binding Modes for an HMG Domain from Human HMGB2 on DNA McCauley, Micah; Hardwidge, Philip R.; Maher, L. James Biophysical Journal, Vol. 89, Issue 1 https://doi.org/10.1529/biophysj.104.052068	journal	July 2005
Revisiting the anomalous bending elasticity of sharply bent DNA Cong, Peiwen; Dai, Liang; Chen, Hu arXiv https://doi.org/10.48550/arxiv.1507.06354	text	January 2015