Fluorescence Resonance Energy Transfer-Based DNA Tetrahedron Nanotweezer for Highly Reliable Detection of Tumor-Related mRNA in Living Cells.

Accurate detection and imaging of tumor-related mRNA in living cells hold great promise for early cancer detection. However, currently, most probes designed to image intracellular mRNA confront intrinsic interferences arising from complex biological matrices and resulting in inevitable false-positive signals. To circumvent this problem, an intracellular DNA nanoprobe, termed DNA tetrahedron nanotweezer (DTNT), was developed to reliably image tumor-related mRNA in living cells based on the FRET (fluorescence resonance energy transfer) "off" to "on" signal readout mode. DTNT was self-assembled from four single-stranded DNAs. In the absence of target mRNA, the respectively labeled donor and acceptor fluorophores are separated, thus inducing low FRET efficiency. However, in the presence of target mRNA, DTNT alters its structure from the open to closed state, thus bringing the dual fluorophores into close proximity for high FRET efficiency. The DTNT exhibited high cellular permeability, fast response and excellent biocompatibility. Moreover, intracellular imaging experiments showed that DTNT could effectively distinguish cancer cells from normal cells and, moreover, distinguish among changes of mRNA expression levels in living cells. The DTNT nanoprobe also exhibits minimal effect of probe concentration, distribution and laser power as other ratiometric probe. More importantly, as a result of the FRET "off" to "on" signal readout mode, the DTNT nanoprobe almost entirely avoids false-positive signals due to intrinsic interferences, such as nuclease digestion, protein binding and thermodynamic fluctuations in complex biological matrices. This design blueprint can be applied to the development of powerful DNA nanomachines for biomedical research and clinical early diagnosis.

[1]  H. Funabashi,et al.  Continuous Monitoring of Specific mRNA Expression Responses with a Fluorescence Resonance Energy Transfer-Based DNA Nano-tweezer Technique That Does Not Require Gene Recombination. , 2016, Analytical chemistry.

[2]  Penghui Zhang,et al.  In situ amplification of intracellular microRNA with MNAzyme nanodevices for multiplexed imaging, logic operation, and controlled drug release. , 2015, ACS nano.

[3]  Chunhai Fan,et al.  Reconfigurable three-dimensional DNA nanostructures for the construction of intracellular logic sensors. , 2012, Angewandte Chemie.

[4]  H. D. Vanguilder,et al.  Twenty-five years of quantitative PCR for gene expression analysis. , 2008, BioTechniques.

[5]  G R Stark,et al.  Detection of specific RNAs or specific fragments of DNA by fractionation in gels and transfer to diazobenzyloxymethyl paper. , 1979, Methods in enzymology.

[6]  Jonas W Perez,et al.  Hairpin DNA-functionalized gold colloids for the imaging of mRNA in live cells. , 2010, Journal of the American Chemical Society.

[7]  D. Scherman,et al.  A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Cuichen Wu,et al.  Self-assembly of DNA Nanohydrogels with Controllable Size and Stimuli-Responsive Property for Targeted Gene Regulation Therapy , 2015, Journal of the American Chemical Society.

[9]  Antony K. Chen,et al.  Avoiding false-positive signals with nuclease-vulnerable molecular beacons in single living cells , 2007, Nucleic acids research.

[10]  Na Li,et al.  A multicolor nanoprobe for detection and imaging of tumor-related mRNAs in living cells. , 2012, Angewandte Chemie.

[11]  H. Pei,et al.  Self-assembled multivalent DNA nanostructures for noninvasive intracellular delivery of immunostimulatory CpG oligonucleotides. , 2011, ACS nano.

[12]  Liguang Xu,et al.  Gold-Quantum Dot Core-Satellite Assemblies for Lighting Up MicroRNA In Vitro and In Vivo. , 2016, Small.

[13]  Igor L. Medintz,et al.  Materials for Fluorescence Resonance Energy Transfer Analysis: Beyond Traditional Donor—Acceptor Combinations , 2006 .

[14]  이혁진 Molecularly Self-Assembled Nucleic Acid Nanoparticles for Targeted In Vivo siRNA Delivery , 2012 .

[15]  Tania Nolan,et al.  Quantification of mRNA using real-time RT-PCR , 2006, Nature Protocols.

[16]  Weihong Tan,et al.  Simultaneous monitoring of the expression of multiple genes inside of single breast carcinoma cells. , 2005, Analytical chemistry.

[17]  Diana P Bratu,et al.  Visualizing the distribution and transport of mRNAs in living cells , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[18]  W. Tan,et al.  Molecular beacons in biomedical detection and clinical diagnosis. , 2008, International journal of clinical and experimental pathology.

[19]  Jennifer Couzin,et al.  Microarray Data Reproduced, But Some Concerns Remain , 2006, Science.

[20]  Kemin Wang,et al.  FRET Nanoflares for Intracellular mRNA Detection: Avoiding False Positive Signals and Minimizing Effects of System Fluctuations. , 2015, Journal of the American Chemical Society.

[21]  Kemin Wang,et al.  A DNA tetrahedron-based molecular beacon for tumor-related mRNA detection in living cells. , 2016, Chemical Communications.

[22]  Gang Bao,et al.  Dual FRET molecular beacons for mRNA detection in living cells. , 2004, Nucleic acids research.

[23]  Na Li,et al.  Multiplexed detection and imaging of intracellular mRNAs using a four-color nanoprobe. , 2013, Analytical chemistry.

[24]  Weihong Tan,et al.  Programmable and Multiparameter DNA-Based Logic Platform For Cancer Recognition and Targeted Therapy , 2014, Journal of the American Chemical Society.

[25]  Matthew J. A. Wood,et al.  DNA cage delivery to mammalian cells. , 2011, ACS nano.

[26]  B. Armitage,et al.  Fluorescent DNA nanotags based on a self-assembled DNA tetrahedron. , 2009, ACS nano.

[27]  Jiye Shi,et al.  Single-particle tracking and modulation of cell entry pathways of a tetrahedral DNA nanostructure in live cells. , 2014, Angewandte Chemie.

[28]  Nan Ma,et al.  Catalytic Molecular Imaging of MicroRNA in Living Cells by DNA-Programmed Nanoparticle Disassembly. , 2016, Angewandte Chemie.

[29]  Gurman Singh Pall,et al.  Carbodiimide-mediated cross-linking of RNA to nylon membranes improves the detection of siRNA, miRNA and piRNA by northern blot , 2007, Nucleic acids research.

[30]  Genxi Li,et al.  Gold-Nanoparticle-Based Multicolor Nanobeacons for Sequence-Specific DNA Analysis , 2010 .

[31]  D. Hanahan,et al.  The Hallmarks of Cancer , 2000, Cell.

[32]  Russell P. Goodman,et al.  Reconfigurable, braced, three-dimensional DNA nanostructures. , 2008, Nature nanotechnology.

[33]  Zhan Wu,et al.  Electrostatic nucleic acid nanoassembly enables hybridization chain reaction in living cells for ultrasensitive mRNA imaging. , 2015, Journal of the American Chemical Society.

[34]  Weihong Tan,et al.  DNA nanoflowers for multiplexed cellular imaging and traceable targeted drug delivery. , 2014, Angewandte Chemie.

[35]  R. Yuan,et al.  Multicolor-Encoded Reconfigurable DNA Nanostructures Enable Multiplexed Sensing of Intracellular MicroRNAs in Living Cells. , 2016, ACS Applied Materials and Interfaces.

[36]  A. Hölscher,et al.  Advances in Brief Epidermal Growth Factor Receptor and HER 2-neu mRNA Expression in Non-Small Cell Lung Cancer Is Correlated with Survival , 2001 .

[37]  James J. Chen,et al.  Key aspects of analyzing microarray gene-expression data. , 2007, Pharmacogenomics.

[38]  Klaus Pantel,et al.  Cell-free nucleic acids as biomarkers in cancer patients , 2011, Nature Reviews Cancer.

[39]  P. Carmeliet,et al.  Angiogenesis in cancer and other diseases , 2000, Nature.

[40]  Chor Yong Tay,et al.  Nature-inspired DNA nanosensor for real-time in situ detection of mRNA in living cells. , 2015, ACS nano.