Intracellular in situ labeling of TiO2 nanoparticles for fluorescence microscopy detection

Brown, Koshonna; Thurn, Ted; Xin, Lun; Liu, William; Bazak, Remon; Chen, Si; Lai, Barry; Vogt, Stefan; Jacobsen, Chris; Paunesku, Tatjana; Woloschak, Gayle E.

doi:10.1007/s12274-017-1654-8

Title: Intracellular in situ labeling of TiO₂ nanoparticles for fluorescence microscopy detection

Journal Article · Wed Jul 19 00:00:00 EDT 2017 · Nano Research

DOI:https://doi.org/10.1007/s12274-017-1654-8· OSTI ID:1437373

Brown, Koshonna ^[1]; Thurn, Ted ^[1]; Xin, Lun ^[1]; Liu, William ^[1]; Bazak, Remon ^[1]; Chen, Si ^[2]; Lai, Barry ^[2]; Vogt, Stefan ^[2]; Jacobsen, Chris ^[3]; Paunesku, Tatjana ^[1]; Woloschak, Gayle E. ^[1]

Northwestern Univ., Chicago, IL (United States). Dept. of Radiation Oncology. Feinberg School of Medicine
Argonne National Lab. (ANL), Argonne, IL (United States). X-ray Science Division. Advanced Photon Source
Northwestern Univ., Evanston, IL (United States). Dept. of Physics & Astronomy. Weinberg College of Arts and Sciences

Titanium dioxide (TiO₂) nanoparticles are produced for many different purposes, including development of therapeutic and diagnostic nanoparticles for cancer detection and treatment, drug delivery, induction of DNA double-strand breaks, and imaging of specific cells and subcellular structures. Currently, the use of optical microscopy, an imaging technique most accessible to biology and medical pathology, to detect TiO₂ nanoparticles in cells and tissues ex vivo is limited with low detection limits, while more sensitive imaging methods (transmission electron microscopy, X-ray fluorescence microscopy, etc.) have low throughput and technical and operational complications. In this paper, we describe two in situ posttreatment labeling approaches to stain TiO₂ nanoparticles taken up by the cells. The first approach utilizes fluorescent biotin and fluorescent streptavidin to label the nanoparticles before and after cellular uptake; the second approach is based on the copper-catalyzed azide-alkyne cycloaddition, the so-called Click chemistry, for labeling and detection of azide-conjugated TiO₂ nanoparticles with alkyneconjugated fluorescent dyes such as Alexa Fluor 488. To confirm that optical fluorescence signals of these nanoparticles match the distribution of the Ti element, we used synchrotron X-ray fluorescence microscopy (XFM) at the Advanced Photon Source at Argonne National Laboratory. Titanium-specific XFM showed excellent overlap with the location of optical fluorescence detected by confocal microscopy. Finally and therefore, future experiments with TiO₂ nanoparticles may safely rely on confocal microscopy after in situ nanoparticle labeling using approaches described here.

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Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States); Northwestern Univ., Chicago, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of Health (NIH) (United States); National Aeronautics and Space Administration (NASA); US Army Research Office (ARO); National Science Foundation (NSF)

Grant/Contract Number:: AC02-06CH11357; CA107467; EB002100; U54CA119341; GM104530; SP0007167; NCI CCSG P30 CA060553; 1S10OD010398-01; NNA06CB93G; NNCI-1542205

OSTI ID:: 1437373

Journal Information:: Nano Research, Vol. 11, Issue 1; ISSN 1998-0124

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 22 works

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References (42)

Tetanus toxin C fragment-conjugated nanoparticles for targeted drug delivery to neurons Townsend, Seth A.; Evrony, Gilad D.; Gu, Frank X. Biomaterials, Vol. 28, Issue 34 https://doi.org/10.1016/j.biomaterials.2007.08.011	journal	December 2007
A nanobiosensor for the detection of arginase activity Malalasekera, Aruni P.; Wang, Hongwang; Samarakoon, Thilani N. Nanomedicine: Nanotechnology, Biology and Medicine, Vol. 13, Issue 2 https://doi.org/10.1016/j.nano.2016.08.014	journal	February 2017
Polymer–iron oxide composite nanoparticles for EPR-independent drug delivery Park, Jinho; Kadasala, Naveen Reddy; Abouelmagd, Sara A. Biomaterials, Vol. 101 https://doi.org/10.1016/j.biomaterials.2016.06.007	journal	September 2016
Density functional study of the TiO2–dopamine complex Vega-Arroyo, Manuel; LeBreton, Pierre R.; Rajh, Tijana Chemical Physics Letters, Vol. 406, Issue 4-6 https://doi.org/10.1016/j.cplett.2005.03.029	journal	May 2005
Uptake and Distribution of Ultrasmall Anatase TiO ₂ Alizarin Red S Nanoconjugates in Arabidopsis thaliana Kurepa, Jasmina; Paunesku, Tatjana; Vogt, Stefan Nano Letters, Vol. 10, Issue 7 https://doi.org/10.1021/nl903518f	journal	July 2010
The Bionanoprobe: hard X-ray fluorescence nanoprobe with cryogenic capabilities Chen, S.; Deng, J.; Yuan, Y. Journal of Synchrotron Radiation, Vol. 21, Issue 1 https://doi.org/10.1107/S1600577513029676	journal	December 2013
Dopamine Adsorption on TiO ₂ Anatase Surfaces Urdaneta, I.; Keller, A.; Atabek, O. The Journal of Physical Chemistry C, Vol. 118, Issue 35 https://doi.org/10.1021/jp506156e	journal	August 2014
X-ray fluorescence microprobe imaging in biology and medicine Paunesku, Tatjana; Vogt, Stefan; Maser, Jörg Journal of Cellular Biochemistry, Vol. 99, Issue 6 https://doi.org/10.1002/jcb.21047	journal	January 2006
Cu-Catalyzed Azide−Alkyne Cycloaddition Meldal, Morten; Tornøe, Christian Wenzel Chemical Reviews, Vol. 108, Issue 8 https://doi.org/10.1021/cr0783479	journal	August 2008
Direct In-Gel Fluorescence Detection and Cellular Imaging of O -GlcNAc-Modified Proteins Clark, Peter M.; Dweck, Jessica F.; Mason, Daniel E. Journal of the American Chemical Society, Vol. 130, Issue 35 https://doi.org/10.1021/ja8030467	journal	September 2008
Methods for assessing DNA hybridization of peptide nucleic acid–titanium dioxide nanoconjugates Brown, Eric M. B.; Paunesku, Tatjana; Wu, AiGuo Analytical Biochemistry, Vol. 383, Issue 2 https://doi.org/10.1016/j.ab.2008.08.020	journal	December 2008
Biology of TiO2–oligonucleotide nanocomposites Paunesku, Tatjana; Rajh, Tijana; Wiederrecht, Gary Nature Materials, Vol. 2, Issue 5 https://doi.org/10.1038/nmat875	journal	April 2003
Photocatalytic killing effect of TiO ₂ nanoparticles on Ls-174-t human colon carcinoma cells Zhang, Ai-Ping World Journal of Gastroenterology, Vol. 10, Issue 21 https://doi.org/10.3748/wjg.v10.i21.3191	journal	January 2004
Synthesis, characterization and particle size distribution of TiO2 colloidal nanoparticles Abbas, Zareen; Holmberg, Jenny Perez; Hellström, Anna Karin Colloids and Surfaces A: Physicochemical and Engineering Aspects, Vol. 384, Issue 1-3 https://doi.org/10.1016/j.colsurfa.2011.03.064	journal	July 2011
Fabricating Appropriate Band-Edge-Staggered Heterosemiconductors with Optically Activated Au Nanoparticles via Click Chemistry for Photoelectrochemical Water Splitting Upadhyay, Arun Prakash; Behara, Dilip Kumar; Sharma, Gyan Prakash ACS Sustainable Chemistry & Engineering, Vol. 4, Issue 9 https://doi.org/10.1021/acssuschemeng.6b00335	journal	August 2016
Chemically Directed Assembly of Photoactive Metal Oxide Nanoparticle Heterojunctions via the Copper-Catalyzed Azide–Alkyne Cycloaddition “Click” Reaction Cardiel, Allison C.; Benson, Michelle C.; Bishop, Lee M. ACS Nano, Vol. 6, Issue 1 https://doi.org/10.1021/nn203585r	journal	December 2011
Surface Restructuring of Nanoparticles: An Efficient Route for Ligand−Metal Oxide Crosstalk Rajh, T.; Chen, L. X.; Lukas, K. The Journal of Physical Chemistry B, Vol. 106, Issue 41 https://doi.org/10.1021/jp021235v	journal	October 2002
Comparison of the Chase Effects of Avidin, Streptavidin, Neutravidin, and Avidin-Ferritin on a Radiolabeled Biotinylated Anti-tumor Monoclonal Antibody Kobayashi, Hisataka; Sakahara, Harumi; Endo, Keigo Japanese Journal of Cancer Research, Vol. 86, Issue 3 https://doi.org/10.1111/j.1349-7006.1995.tb03056.x	journal	March 1995
Epidermal Growth Factor Receptor Targeted Nuclear Delivery and High-Resolution Whole Cell X-ray Imaging of Fe ₃ O ₄ @TiO ₂ Nanoparticles in Cancer Cells Yuan, Ye; Chen, Si; Paunesku, Tatjana ACS Nano, Vol. 7, Issue 12 https://doi.org/10.1021/nn4033294	journal	November 2013
Cu(I)-Catalyzed Huisgen Azide−Alkyne 1,3-Dipolar Cycloaddition Reaction in Nucleoside, Nucleotide, and Oligonucleotide Chemistry Amblard, Franck; Cho, Jong Hyun; Schinazi, Raymond F. Chemical Reviews, Vol. 109, Issue 9 https://doi.org/10.1021/cr9001462	journal	September 2009
DNA−TiO ₂ Nanoconjugates Labeled with Magnetic Resonance Contrast Agents Endres, Paul J.; Paunesku, Tatjana; Vogt, Stefan Journal of the American Chemical Society, Vol. 129, Issue 51 https://doi.org/10.1021/ja0772389	journal	December 2007
Endocytosis of titanium dioxide nanoparticles in prostate cancer PC-3M cells Thurn, Kenneth T.; Arora, Hans; Paunesku, Tatjana Nanomedicine: Nanotechnology, Biology and Medicine, Vol. 7, Issue 2 https://doi.org/10.1016/j.nano.2010.09.004	journal	April 2011
Nanocarriers Enhance Doxorubicin Uptake in Drug-Resistant Ovarian Cancer Cells Arora, H. C.; Jensen, M. P.; Yuan, Y. Cancer Research, Vol. 72, Issue 3 https://doi.org/10.1158/0008-5472.CAN-11-2890	journal	December 2011
Sodium Dependent Multivitamin Transporter (SMVT): A Potential Target for Drug Delivery Dutt Vadlapudi, Aswani; Krishna Vadlapatla, Ramya; K. Mitra, Ashim Current Drug Targets, Vol. 13, Issue 7 https://doi.org/10.2174/138945012800675650	journal	May 2012
TiO2 nanocomposites with high refractive index and transparency Tao, Peng; Li, Yu; Rungta, Atri Journal of Materials Chemistry, Vol. 21, Issue 46 https://doi.org/10.1039/c1jm13093e	journal	January 2011
Synchrotron-based X-ray fluorescence imaging of human cells labeled with CdSe quantum dots Corezzi, Silvia; Urbanelli, Lorena; Cloetens, Peter Analytical Biochemistry, Vol. 388, Issue 1 https://doi.org/10.1016/j.ab.2009.01.044	journal	May 2009
Labeling TiO ₂ Nanoparticles with Dyes for Optical Fluorescence Microscopy and Determination of TiO ₂ -DNA Nanoconjugate Stability Thurn, Kenneth T.; Paunesku, Tatjana; Wu, Aiguo Small, Vol. 5, Issue 11 https://doi.org/10.1002/smll.200801458	journal	June 2009
Fluorescent dyes of the esculetin and alizarin families respond to zinc ions ratiometrically Zhang, Lu; Dong, Shen; Zhu, Lei Chemical Communications, Issue 19 https://doi.org/10.1039/b618413h	journal	January 2007
A chemical method for fast and sensitive detection of DNA synthesis in vivo Salic, A.; Mitchison, T. J. Proceedings of the National Academy of Sciences, Vol. 105, Issue 7 https://doi.org/10.1073/pnas.0712168105	journal	February 2008
Vitamin-mediated targeting as a potential mechanism to increase drug uptake by tumours Russell-Jones, Gregory; McTavish, Kirsten; McEwan, John Journal of Inorganic Biochemistry, Vol. 98, Issue 10 https://doi.org/10.1016/j.jinorgbio.2004.07.009	journal	October 2004
Nanoparticles for Applications in Cellular Imaging Thurn, K. Ted; Brown, Eric M. B.; Wu, Aiguo Nanoscale Research Letters, Vol. 2, Issue 9 https://doi.org/10.1007/s11671-007-9081-5	journal	August 2007
Intracellular Distribution of TiO ₂ −DNA Oligonucleotide Nanoconjugates Directed to Nucleolus and Mitochondria Indicates Sequence Specificity Paunesku, Tatjana; Vogt, Stefan; Lai, Barry Nano Letters, Vol. 7, Issue 3 https://doi.org/10.1021/nl0624723	journal	March 2007
Synthesis of a hybrid assembly composed of titanium dioxide nanoparticles and thin multi-walled carbon nanotubes using “click chemistry” Yadav, Santosh Kumar; Madeshwaran, Sekkarapatti Ramasamy; Cho, Jae Whan Journal of Colloid and Interface Science, Vol. 358, Issue 2 https://doi.org/10.1016/j.jcis.2011.03.040	journal	June 2011
Biotinylation of TiO ₂ Nanoparticles and Their Conjugation with Streptavidin Ye, Lu; Pelton, Robert; Brook, Michael A. Langmuir, Vol. 23, Issue 10 https://doi.org/10.1021/la0626656	journal	May 2007
The Molecular Probes handbook. A guide to fluorescent probes and labeling technologies: (I. Johnson and M. Spence (eds.) 11th Edition, Life Technologies, 2010, 1060 p., $100) Wiederschain, G. Ya. Biochemistry (Moscow), Vol. 76, Issue 11 https://doi.org/10.1134/S0006297911110101	journal	November 2011
Photocatalytic probing of DNA sequence by using TiO2/dopamine-DNA triads Liu, Jianqin; de la Garza, Linda; Zhang, Ligang Chemical Physics, Vol. 339, Issue 1-3 https://doi.org/10.1016/j.chemphys.2007.07.040	journal	October 2007
PEGylation of Nanosubstrates (Titania) with Multifunctional Reagents: At the Crossroads between Nanoparticles and Nanocomposites Kotsokechagia, Tania; Zaki, Noha M.; Syres, Karen Langmuir, Vol. 28, Issue 31 https://doi.org/10.1021/la3012958	journal	July 2012
Adsorption of DNA Oligonucleotides by Titanium Dioxide Nanoparticles Zhang, Xu; Wang, Feng; Liu, Biwu Langmuir, Vol. 30, Issue 3 https://doi.org/10.1021/la404633p	journal	January 2014
Cytotoxicity and DNA cleavage with core–shell nanocomposites functionalized by a KH domain DNA binding peptide Bazak, Remon; Ressl, Jan; Raha, Sumita Nanoscale, Vol. 5, Issue 23 https://doi.org/10.1039/c3nr02203j	journal	January 2013
Gadolinium-conjugated TiO2-DNA oligonucleotide nanoconjugates show prolonged intracellular retention period and T1-weighted contrast enhancement in magnetic resonance images Paunesku, Tatjana; Ke, Tianyi; Dharmakumar, Rohan Nanomedicine: Nanotechnology, Biology and Medicine, Vol. 4, Issue 3 https://doi.org/10.1016/j.nano.2008.04.004	journal	September 2008
Selective identification of newly synthesized proteins in mammalian cells using bioorthogonal noncanonical amino acid tagging (BONCAT) Dieterich, D. C.; Link, A. J.; Graumann, J. Proceedings of the National Academy of Sciences, Vol. 103, Issue 25 https://doi.org/10.1073/pnas.0601637103	journal	June 2006
Assembly and Charge Transfer in Hybrid TiO ₂ Architectures Using Biotin−Avidin as a Connector Dimitrijevic, Nada M.; Saponjic, Zoran V.; Rabatic, Bryan M. Journal of the American Chemical Society, Vol. 127, Issue 5 https://doi.org/10.1021/ja0458118	journal	February 2005

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Title: Intracellular in situ labeling of TiO2 nanoparticles for fluorescence microscopy detection

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Title: Intracellular in situ labeling of TiO₂ nanoparticles for fluorescence microscopy detection