1932

Abstract

The nanoscale engineering of nucleic acids has led to exciting molecular technologies for high-end biological imaging. The predictable base pairing, high programmability, and superior new chemical and biological methods used to access nucleic acids with diverse lengths and in high purity, coupled with computational tools for their design, have allowed the creation of a stunning diversity of nucleic acid–based nanodevices. Given their biological origin, such synthetic devices have a tremendous capacity to interface with the biological world, and this capacity lies at the heart of several nucleic acid–based technologies that are finding applications in biological systems. We discuss these diverse applications and emphasize the advantage, in terms of physicochemical properties, that the nucleic acid scaffold brings to these contexts. As our ability to engineer this versatile scaffold increases, its applications in structural, cellular, and organismal biology are clearly poised to massively expand.

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2016-06-02
2024-04-19
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Literature Cited

  1. Saenger W. 1.  1984. Principles of Nucleic Acid Structure New York: Springer-Verlag
  2. Jones MR, Seeman NC, Mirkin CA. 2.  2015. Programmable materials and the nature of the DNA bond. Science 347:1260901 [Google Scholar]
  3. Seeman NC. 3.  2010. Nanomaterials based on DNA. Annu. Rev. Biochem. 79:65–87 [Google Scholar]
  4. Winfree E, Liu F, Wenzler LA, Seeman NC. 4.  1998. Design and self-assembly of two-dimensional DNA crystals. Nature 394:539–44 [Google Scholar]
  5. Rothemund PW, Papadakis N, Winfree E. 5.  2004. Algorithmic self-assembly of DNA Sierpinski triangles. PLOS Biol. 2:424 [Google Scholar]
  6. Rothemund PWK. 6.  2006. Folding DNA to create nanoscale shapes and patterns. Nature 440:297–302 [Google Scholar]
  7. Douglas SM, Marblestone AH, Teerapittayanon S, Vazquez A, Church GM, Shih WM. 7.  2009. Rapid prototyping of 3D DNA-origami shapes with caDNAno. Nucleic Acids Res. 37:5001–6 [Google Scholar]
  8. Jungmann R, Avendaño MS, Woehrstein JB, Dai M, Shih WM, Yin P. 8.  2014. Multiplexed 3D cellular super-resolution imaging with DNA-PAINT and Exchange-PAINT. Nat. Methods 11:313–18 [Google Scholar]
  9. Jungmann R, Steinhauer C, Scheible M, Kuzyk A, Tinnefeld P, Simmel FC. 9.  2010. Single-molecule kinetics and super-resolution microscopy by fluorescence imaging of transient binding on DNA origami. Nano Lett. 10:4756–61 [Google Scholar]
  10. Steinhauer C, Jungmann R, Sobey TL, Simmel FC, Tinnefeld P. 10.  2009. DNA origami as a nanoscopic ruler for super-resolution microscopy. Angew. Chem. Int. Ed. Engl. 48:8870–73 [Google Scholar]
  11. Cho EJ, Lee J-W, Ellington AD. 11.  2009. Applications of aptamers as sensors. Annu. Rev. Anal. Chem. 2:241–64 [Google Scholar]
  12. Filonov GS, Moon JD, Svensen N, Jaffrey SR. 12.  2014. Broccoli: rapid selection of an RNA mimic of green fluorescent protein by fluorescence-based selection and directed evolution. J. Am. Chem. Soc. 136:16299–308 [Google Scholar]
  13. Paige JS, Wu KY, Jaffrey SR. 13.  2011. RNA mimics of green fluorescent protein. Science 333:642–46 [Google Scholar]
  14. Paige JS, Nguyen-Duc T, Song W, Jaffrey SR. 14.  2012. Fluorescence imaging of cellular metabolites with RNA. Science 335:1194 [Google Scholar]
  15. Modi S, Swetha MG, Goswami D, Gupta GD, Mayor S, Krishnan Y. 15.  2009. A DNA nanomachine that maps spatial and temporal pH changes inside living cells. Nat. Nanotechnol. 4:325–30 [Google Scholar]
  16. Saha S, Prakash V, Halder S, Chakraborty K, Krishnan Y. 16.  2015. A pH-independent DNA nanodevice for quantifying chloride transport in organelles of living cells. Nat. Nanotechnol. 10:645–51 [Google Scholar]
  17. Surana S, Bhat JM, Koushika SP, Krishnan Y. 17.  2011. An autonomous DNA nanomachine maps spatiotemporal pH changes in a multicellular living organism. Nat. Commun. 2:340 [Google Scholar]
  18. Morris V, Kirby A, Gunning A. 18.  2010. Atomic Force Microscopy for Biologists London: Imp. Coll.
  19. Lyubchenko YL, Shlyakhtenko LS, Ando T. 19.  2011. Imaging of nucleic acids with atomic force microscopy. Methods 54:274–83 [Google Scholar]
  20. Rajendran A, Endo M, Sugiyama H. 20.  2012. Single-molecule analysis using DNA origami. Angew. Chem. Int. Ed. Engl. 51:874–90 [Google Scholar]
  21. Rivetti C, Guthold M, Bustamante C. 21.  1999. Wrapping of DNA around the E. coli RNA polymerase open promoter complex. EMBO J. 18:4464–75 [Google Scholar]
  22. Seeman NC. 22.  1982. Nucleic acid junctions and lattices. J. Theor. Biol. 99:237–47 [Google Scholar]
  23. Yan H, Park SH, Finkelstein G, Reif JH, LaBean TH. 23.  2003. DNA-templated self-assembly of protein arrays and highly conductive nanowires. Science 301:1882–84 [Google Scholar]
  24. Rinker S, Ke Y, Liu Y, Chhabra R, Yan H. 24.  2008. Self-assembled DNA nanostructures for distance-dependent multivalent ligand-protein binding. Nat. Nanotechnol. 3:418–22 [Google Scholar]
  25. Chhabra R, Sharma J, Ke Y, Liu Y, Rinker S. 25.  et al. 2007. Spatially addressable multiprotein nanoarrays templated by aptamer-tagged DNA nanoarchitectures. J. Am. Chem. Soc. 129:10304–5 [Google Scholar]
  26. Wilner OI, Weizmann Y, Gill R, Lioubashevski O, Freeman R, Willner I. 26.  2009. Enzyme cascades activated on topologically programmed DNA scaffolds. Nat. Nanotechnol. 4:249–54 [Google Scholar]
  27. Delebecque CJ, Lindner AB, Silver PA, Aldaye FA. 27.  2011. Organization of intracellular reactions with rationally designed RNA assemblies. Science 333:470–74 [Google Scholar]
  28. Ando T, Uchihashi T, Kodera N. 28.  2013. High-speed AFM and applications to biomolecular systems. Annu. Rev. Biophys. 42:393–414 [Google Scholar]
  29. Rajendran A, Endo M, Hidaka K, Tran PLT, Mergny JL. 29.  et al. 2013. HIV-1 nucleocapsid proteins as molecular chaperones for tetramolecular antiparallel G-quadruplex formation. J. Am. Chem. Soc. 135:18575–85 [Google Scholar]
  30. Endo M, Tatsumi K, Terushima K, Katsuda Y, Hidaka K. 30.  et al. 2012. Direct visualization of the movement of a single T7 RNA polymerase and transcription on a DNA nanostructure. Angew. Chem. Int. Ed. Engl. 51:8778–82 [Google Scholar]
  31. Suzuki Y, Endo M, Katsuda Y, Ou K, Hidaka K, Sugiyama H. 31.  2014. DNA origami based visualization system for studying site-specific recombination events. J. Am. Chem. Soc. 136:211–18 [Google Scholar]
  32. Voigt NV, Tørring T, Rotaru A, Jacobsen MF, Ravnsbaek JB. 32.  et al. 2010. Single-molecule chemical reactions on DNA origami. Nat. Nanotechnol. 5:200–3 [Google Scholar]
  33. Youngblood B, Reich NO. 33.  2006. Conformational transitions as determinants of specificity for the DNA methyltransferase EcoRI. J. Biol. Chem. 281:26821–31 [Google Scholar]
  34. Endo M, Katsuda Y, Hidaka K, Sugiyama H. 34.  2010. Regulation of DNA methylation using different tensions of double strands constructed in a defined DNA nanostructure. J. Am. Chem. Soc. 132:1592–97 [Google Scholar]
  35. Yamamoto S, De D, Hidaka K, Kim KK, Endo M, Sugiyama H. 35.  2014. Single molecule visualization and characterization of Sox2-Pax6 complex formation on a regulatory DNA element using a DNA origami frame. Nano Lett. 14:2286–92 [Google Scholar]
  36. Endo M, Katsuda Y, Hidaka K, Sugiyama H. 36.  2010. A versatile DNA nanochip for direct analysis of DNA base-excision repair. Angew. Chem. Int. Ed. Engl. 49:9412–16 [Google Scholar]
  37. Rajendran A, Endo M, Hidaka K, Sugiyama H. 37.  2014. Direct and single-molecule visualization of the solution-state structures of G-hairpin and G-triplex intermediates. Angew. Chem. Int. Ed. Engl. 53:4107–12 [Google Scholar]
  38. Pardue ML, Gall JG. 38.  1969. Molecular hybridization of radioactive DNA to the DNA of cytological preparations. PNAS 64:600–4 [Google Scholar]
  39. Rudkin GT, Stollar BD. 39.  1977. High resolution detection of DNA-RNA hybrids in situ by indirect immunofluorescence. Nature 265:472–73 [Google Scholar]
  40. Bauman JG, Wiegant J, Borst P, van Duijn P. 40.  1980. A new method for fluorescence microscopical localization of specific DNA sequences by in situ hybridization of fluorochromelabelled RNA. Exp. Cell Res. 128:485–90 [Google Scholar]
  41. Femino AM, Fay FS, Fogarty K, Singer RH. 41.  1998. Visualization of single RNA transcripts in situ. Science 280:585–90 [Google Scholar]
  42. Raj A, van den Bogaard P, Rifkin SA, van Oudenaarden A, Tyagi S. 42.  2008. Imaging individual mRNA molecules using multiple singly labeled probes. Nat. Methods 5:877–79 [Google Scholar]
  43. Martens UM, Zijlmans JM, Poon SS, Dragowska W, Yui J. 43.  et al. 1998. Short telomeres on human chromosome 17p. Nat. Genet. 18:76–80 [Google Scholar]
  44. Wienholds E, Kloosterman WP, Miska E, Alvarez-Saavedra E, Berezikov E. 44.  et al. 2005. MicroRNA expression in zebrafish embryonic development. Science 309:310–11 [Google Scholar]
  45. Kloosterman WP, Wienholds E, de Bruijn E, Kauppinen S, Plasterk RHA. 45.  2006. In situ detection of miRNAs in animal embryos using LNA-modified oligonucleotide probes. Nat. Methods 3:27–29 [Google Scholar]
  46. Lansdorp PM, Verwoerd NP, Van De Rijke FM, Dragowska V, Little MT. 46.  et al. 1996. Heterogeneity in telomere length of human chromosomes. Hum. Mol. Genet. 5:685–91 [Google Scholar]
  47. Lu J, Tsourkas A. 47.  2009. Imaging individual microRNAs in single mammalian cells in situ. Nucleic Acids Res. 37:1–10 [Google Scholar]
  48. Brown J, Saracoglu K, Uhrig S, Speicher MR, Eils R, Kearney L. 48.  2001. Subtelomeric chromosome rearrangements are detected using an innovative 12-color FISH assay (M-TEL). Nat. Med. 7:497–501 [Google Scholar]
  49. Speicher MR, Gwyn Ballard S, Ward DC. 49.  1996. Karyotyping human chromosomes by combinatorial multi-fluor FISH. Nat. Genet. 12:368–75 [Google Scholar]
  50. Speicher MR, Carter NP. 50.  2005. The new cytogenetics: blurring the boundaries with molecular biology. Nat. Rev. Genet. 6:782–92 [Google Scholar]
  51. Evanko D. 51.  2004. Hybridization chain reaction. Nat. Methods 1:186–87 [Google Scholar]
  52. Choi HMT, Chang JY, Trinh LA, Padilla JE, Fraser SE, Pierce NA. 52.  2010. Programmable in situ amplification for multiplexed imaging of mRNA expression. Nat. Biotechnol. 28:1208–12 [Google Scholar]
  53. Qian X, Lloyd RV. 53.  2003. Recent developments in signal amplification methods for in situ hybridization. Diagn. Mol. Pathol. 12:1–13 [Google Scholar]
  54. Bagasra O. 54.  2007. Protocols for the in situ PCR-amplification and detection of mRNA and DNA sequences. Nat. Protoc. 2:2782–95 [Google Scholar]
  55. Larsson C, Koch J, Nygren A, Janssen G, Raap AK. 55.  et al. 2004. In situ genotyping individual DNA molecules by target-primed rolling-circle amplification of padlock probes. Nat. Methods 1:227–32 [Google Scholar]
  56. Larsson C, Grundberg I, Söderberg O, Nilsson M. 56.  2010. In situ detection and genotyping of individual mRNA molecules. Nat. Methods 7:395–97 [Google Scholar]
  57. Lee JH, Daugharthy ER, Scheiman J, Kalhor R, Ferrante TC. 57.  et al. 2015. Fluorescent in situ sequencing (FISSEQ) of RNA for gene expression profiling in intact cells and tissues. Nat. Protoc. 10:442–58 [Google Scholar]
  58. Kim DN, Kilchherr F, Dietz H, Bathe M. 58.  2012. Quantitative prediction of 3D solution shape and flexibility of nucleic acid nanostructures. Nucleic Acids Res. 40:2862–68 [Google Scholar]
  59. Castro CE, Kilchherr F, Kim DN, Shiao EL, Wauer T. 59.  et al. 2011. A primer to scaffolded DNA origami. Nat. Methods 8:221–29 [Google Scholar]
  60. Huang B, Bates M, Zhuang X. 60.  2009. Super-resolution fluorescence microscopy. Annu. Rev. Biochem. 78:993–1016 [Google Scholar]
  61. Gordon MP, Ha T, Selvin PR. 61.  2004. Single-molecule high-resolution imaging with photobleaching. PNAS 101:6462–65 [Google Scholar]
  62. Steinhauer C, Forthmann C, Vogelsang J, Tinnefeld P. 62.  2008. Superresolution microscopy on the basis of engineered dark states. J. Am. Chem. Soc. 130:16840–41 [Google Scholar]
  63. Schermelleh L, Heintzmann R, Leonhardt H. 63.  2010. A guide to super-resolution fluorescence microscopy. J. Cell Biol. 190:165–75 [Google Scholar]
  64. Schmied JJ, Gietl A, Holzmeister P, Forthmann C, Steinhauer C. 64.  et al. 2012. Fluorescence and super-resolution standards based on DNA origami. Nat. Methods 9:1133–34 [Google Scholar]
  65. Schmied JJ, Raab M, Forthmann C, Pibiri E, Wünsch B. 65.  et al. 2014. DNA origami-based standards for quantitative fluorescence microscopy. Nat. Protoc. 9:1367–91 [Google Scholar]
  66. Schmied JJ, Forthmann C, Pibiri E, Lalkens B, Nickels P. 66.  et al. 2013. DNA origami nanopillars as standards for three-dimensional superresolution microscopy. Nano Lett. 13:781–85 [Google Scholar]
  67. Sharonov A, Hochstrasser RM. 67.  2006. Wide-field subdiffraction imaging by accumulated binding of diffusing probes. PNAS 103:18911–16 [Google Scholar]
  68. Giannone G, Hosy E, Levet F, Constals A, Schulze K. 68.  et al. 2010. Dynamic superresolution imaging of endogenous proteins on living cells at ultra-high density. Biophys. J. 99:1303–10 [Google Scholar]
  69. Derr ND, Goodman BS, Jungmann R, Leschziner AE, Shih WM, Reck-Peterson SL. 69.  2012. Tug-of-war in motor protein ensembles revealed with a programmable DNA origami scaffold. Science 338:662–65 [Google Scholar]
  70. Molenaar C, Abdulle A, Gena A, Tanke HJ, Dirks RW. 70.  2004. Poly(A)+ RNAs roam the cell nucleus and pass through speckle domains in transcriptionally active and inactive cells. J. Cell Biol. 165:191–202 [Google Scholar]
  71. Molenaar C, Marras SA, Slats JCM, Truffert J-C, Lemaitre M. 71.  et al. 2001. Linear 2′ O-Methyl RNA probes for the visualization of RNA in living cells. Nucleic Acids Res. 29:e89 [Google Scholar]
  72. Bao G, Tsourkas A, Santangelo PJ. 72.  2004. Engineering nanostructured probes for sensitive intracellular gene detection. Mech. Chem. Biosyst. 1:23–36 [Google Scholar]
  73. Bratu DP, Cha BJ, Mhlanga MM, Kramer FR, Tyagi S. 73.  2003. Visualizing the distribution and transport of mRNAs in living cells. PNAS 100:13308–13 [Google Scholar]
  74. Nitin N, Santangelo PJ, Kim G, Nie S, Bao G. 74.  2004. Peptide-linked molecular beacons for efficient delivery and rapid mRNA detection in living cells. Nucleic Acids Res. 32:e58 [Google Scholar]
  75. Tyagi S, Alsmadi O. 75.  2004. Imaging native β-actin mRNA in motile fibroblasts. Biophys. J. 87:4153–62 [Google Scholar]
  76. Tyagi S, Kramer FR. 76.  1996. Molecular beacons: probes that fluoresce upon hybridization. Nat. Biotechnol. 14:303–8 [Google Scholar]
  77. Monroy-Contreras R, Vaca L. 77.  2011. Molecular beacons: powerful tools for imaging RNA in living cells. J. Nucleic Acids 2011:741723 [Google Scholar]
  78. Bao G, Rhee WJ, Tsourkas A. 78.  2009. Fluorescent probes for live-cell RNA detection. Annu. Rev. Biomed. Eng. 11:25–47 [Google Scholar]
  79. Giles RV, Spiller DG, Grzybowski J, Clark RE, Nicklin P, Tidd DM. 79.  1998. Selecting optimal oligonucleotide composition for maximal antisense effect following streptolysin O-mediated delivery into human leukaemia cells. Nucleic Acids Res. 26:1567–75 [Google Scholar]
  80. Santangelo PJ, Alonas E, Jung J, Lifland AW, Zurla C. 80.  2012. Probes for intracellular RNA imaging in live cells. Methods Enzymol. 505:383–99 [Google Scholar]
  81. Bertrand E, Chartrand P, Schaefer M, Shenoy SM, Singer RH, Long RM. 81.  1998. Localization of ASH1 mRNA particles in living yeast. Mol. Cell 2:437–45 [Google Scholar]
  82. Fusco D, Accornero N, Lavoie B, Shenoy SM, Blanchard JM. 82.  et al. 2003. Single mRNA molecules demonstrate probabilistic movement in living mammalian cells. Curr. Biol. 13:161–67 [Google Scholar]
  83. Shav-Tal Y, Darzacq X, Shenoy SM, Fusco D, Janicki SM. 83.  et al. 2004. Dynamics of single mRNPs in nuclei of living cells. Science 304:1797–800 [Google Scholar]
  84. Park HY, Lim H, Yoon YJ, Follenzi A, Nwokafor C. 84.  et al. 2014. Visualization of dynamics of single endogenous mRNA labeled in live mouse. Science 343:422–24 [Google Scholar]
  85. Daigle N, Ellenberg J. 85.  2007. λN-GFP: an RNA reporter system for live-cell imaging. Nat. Methods 4:633–36 [Google Scholar]
  86. Ozawa T, Natori Y, Sato M, Umezawa Y. 86.  2007. Imaging dynamics of endogenous mitochondrial RNA in single living cells. Nat. Methods 4:413–19 [Google Scholar]
  87. Tilsner J. 87.  2015. Pumilio-based RNA in vivo imaging. Methods Mol. Biol. 1217:295–328 [Google Scholar]
  88. Tilsner J, Linnik O, Christensen NM, Bell K, Roberts IM. 88.  et al. 2009. Live-cell imaging of viral RNA genomes using a Pumilio-based reporter. Plant J. 57:758–70 [Google Scholar]
  89. Song W, Strack RL, Svensen N, Jaffrey SR. 89.  2014. Plug-and-play fluorophores extend the spectral properties of Spinach. J. Am. Chem. Soc. 136:1198–201 [Google Scholar]
  90. Bradshaw RA, Dennis EA. 90.  2004. Handbook of Cell Signaling New York: Academic
  91. Krishnan Y, Simmel FC. 91.  2011. Nucleic acid based molecular devices. Angew. Chem. Int. Ed. Engl. 50:3124–56 [Google Scholar]
  92. Krishnan Y, Bathe M. 92.  2012. Designer nucleic acids to probe and program the cell. Trends Cell Biol. 22:624–33 [Google Scholar]
  93. Gallie DR. 93.  1991. The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev. 5:2108–16 [Google Scholar]
  94. Zhang J, Campbell RE, Ting AY, Tsien RY. 94.  2002. Creating new fluorescent probes for cell biology. Nat. Rev. Mol. Cell Biol. 3:906–18 [Google Scholar]
  95. Frommer WB, Davidson MW, Campbell RE. 95.  2009. Genetically encoded biosensors based on engineered fluorescent proteins. Chem. Soc. Rev. 38:2833–41 [Google Scholar]
  96. Lakowicz JR. 96.  1999. Principles of Fluorescence Spectroscopy New York: Springer
  97. Lindenburg L, Merkx M. 97.  2014. Engineering genetically encoded FRET sensors. Sensors 14:11691–713 [Google Scholar]
  98. Song W, Strack RL, Jaffrey SR. 98.  2013. Imaging bacterial protein expression using genetically encoded RNA sensors. Nat. Methods 10:873–75 [Google Scholar]
  99. Kellenberger CA, Wilson SC, Sales-Lee J, Hammond MC. 99.  2013. RNA-based fluorescent biosensors for live cell imaging of second messengers cyclic di-GMP and cyclic AMP-GMP. J. Am. Chem. Soc. 135:4906–9 [Google Scholar]
  100. Kellenberger CA, Chen C, Whiteley AT, Portnoy DA, Hammond MC. 100.  2015. RNA-based fluorescent biosensors for live cell imaging of second messenger cyclic di-AMP. J. Am. Chem. Soc. 137:6432–35 [Google Scholar]
  101. Kellenberger CA, Wilson SC, Hickey SF, Gonzalez TL, Su Y. 101.  et al. 2015. GEMM-I riboswitches from Geobacter sense the bacterial second messenger cyclic AMP-GMP. PNAS 112:5383–88 [Google Scholar]
  102. Sharma S, Zaveri A, Visweswariah SS, Krishnan Y. 102.  2014. A fluorescent nucleic acid nanodevice quantitatively images elevated cyclic adenosine monophosphate in membrane-bound compartments. Small 10:1–5 [Google Scholar]
  103. Nahvi A, Sudarsan N, Ebert MS, Zou X, Brown KL, Breaker RR. 103.  2002. Genetic control by a metabolite binding mRNA. Chem. Biol. 9:1043–49 [Google Scholar]
  104. Serganov A, Nudler E. 104.  2013. A decade of riboswitches. Cell 152:17–24 [Google Scholar]
  105. You M, Litke JL, Jaffrey SR. 105.  2015. Imaging metabolite dynamics in living cells using a Spinach-based riboswitch. PNAS 112:E2756–65 [Google Scholar]
  106. Kellenberger CA, Hammond MC. 106.  2015. In vitro analysis of riboswitch-Spinach aptamer fusions as metabolite-sensing fluorescent biosensors. Methods Enzymol. 550:147–72 [Google Scholar]
  107. Tuerk C, Gold L. 107.  1990. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249:505–10 [Google Scholar]
  108. Ellington AD, Szostak JW. 108.  1990. In vitro selection of RNA molecules that bind specific ligands. Nature 346:818–22 [Google Scholar]
  109. Stoltenburg R, Reinemann C, Strehlitz B. 109.  2007. SELEX—a (r)evolutionary method to generate high-affinity nucleic acid ligands. Biomol. Eng. 24:381–403 [Google Scholar]
  110. Strack RL, Jaffrey SR. 110.  2013. New approaches for sensing metabolites and proteins in live cells using RNA. Curr. Opin. Chem. Biol. 17:651–55 [Google Scholar]
  111. Klug SJ, Famulok M. 111.  1994. All you wanted to know about SELEX. Mol. Biol. Rep. 20:97–107 [Google Scholar]
  112. Bhatia D, Sharma S, Krishnan Y. 112.  2011. Synthetic, biofunctional nucleic acid-based molecular devices. Curr. Opin. Biotechnol. 22:475–84 [Google Scholar]
  113. Halder S, Krishnan Y. 113.  2015. Design of ultrasensitive DNA-based fluorescent pH sensitive nanodevices. Nanoscale 7:10008–12 [Google Scholar]
  114. Liu D, Balasubramanian S. 114.  2003. A proton-fuelled DNA nanomachine. Angew. Chem. Int. Ed. Engl. 42:5734–36 [Google Scholar]
  115. Modi S, Nizak C, Surana S, Halder S, Krishnan Y. 115.  2013. Two DNA nanomachines map pH changes along intersecting endocytic pathways inside the same cell. Nat. Nanotechnol. 8:459–67 [Google Scholar]
  116. Modi S, Halder S, Nizak C, Krishnan Y. 116.  2014. Recombinant antibody mediated delivery of organelle-specific DNA pH sensors along endocytic pathways. Nanoscale 6:1144–52 [Google Scholar]
  117. Idili A, Vallée-Bélisle A, Ricci F. 117.  2014. Programmable pH-triggered DNA nanoswitches. J. Am. Chem. Soc. 136:5836–39 [Google Scholar]
  118. Lannes L, Halder S, Krishnan Y, Schwalbe H. 118.  2015. Tuning the pH response of i-motif DNA oligonucleotides. ChemBioChem 16:1647–56 [Google Scholar]
  119. Koizumi M, Breaker RR. 119.  2000. Molecular recognition of cAMP by an RNA aptamer. Biochemistry 39:8983–92 [Google Scholar]
  120. Sonawane ND, Thiagarajah JR, Verkman AS. 120.  2002. Chloride concentration in endosomes measured using a ratioable fluorescent Cl indicator: evidence for chloride accumulation during acidification. J. Biol. Chem. 277:5506–13 [Google Scholar]
  121. Doherty GJ, McMahon HT. 121.  2009. Mechanisms of endocytosis. Annu. Rev. Biochem. 78:857–902 [Google Scholar]
  122. Tomas A, Futter CE, Eden ER. 122.  2014. EGF receptor trafficking: consequences for signaling and cancer. Trends Cell Biol. 24:26–34 [Google Scholar]
  123. Sabharanjak S, Mayor S. 123.  2004. Folate receptor endocytosis and trafficking. Adv. Drug Deliv. Rev. 56:1099–109 [Google Scholar]
  124. Qian ZM, Li H, Sun H, Ho K. 124.  2002. Targeted drug delivery via the transferrin receptor-mediated endocytosis pathway. Pharmacol. Rev. 54:561–87 [Google Scholar]
  125. Lee H, Lytton-Jean AKR, Chen Y, Love KT, Park AI. 125.  et al. 2012. Molecularly self-assembled nucleic acid nanoparticles for targeted in vivo siRNA delivery. Nat. Nanotechnol. 7:389–93 [Google Scholar]
  126. Albrecht C. 126.  2008. Review of Joseph R. Lakowicz: Principles of Fluorescence Spectroscopy, 3rd edition.. Anal. Bioanal. Chem. 390:1223–24 [Google Scholar]
  127. Canton J, Neculai D, Grinstein S. 127.  2013. Scavenger receptors in homeostasis and immunity. Nat. Rev. Immunol. 13:621–34 [Google Scholar]
  128. Bhatia D, Surana S, Chakraborty S, Koushika SP, Krishnan Y. 128.  2011. A synthetic icosahedral DNA-based host-cargo complex for functional in vivo imaging. Nat. Commun. 2:339 [Google Scholar]
  129. Chang M, Yang CS, Huang DM. 129.  2011. Aptamer-conjugated DNA icosahedral nanoparticles as a carrier of doxorubicin for cancer therapy. ACS Nano 5:6156–63 [Google Scholar]
  130. Charoenphol P, Bermudez H. 130.  2014. Aptamer-targeted DNA nanostructures for therapeutic delivery. Mol. Pharm. 11:1721–25 [Google Scholar]
  131. Chen C-hB, Dellamaggiore KR, Ouellette CP, Sedano CD, Lizadjohry M. 131.  et al. 2008. Aptamer-based endocytosis of a lysosomal enzyme. PNAS 105:15908–13 [Google Scholar]
  132. Chu TC, Marks JW, Lavery LA, Faulkner S, Rosenblum MG. 132.  et al. 2006. Aptamer:toxin conjugates that specifically target prostate tumor cells. Cancer Res. 66:5989–92 [Google Scholar]
  133. Molloy SS, Thomas L, VanSlyke JK, Stenberg PE, Thomas G. 133.  1994. Intracellular trafficking and activation of the furin proprotein convertase: localization to the TGN and recycling from the cell surface. EMBO J. 13:18–33 [Google Scholar]
  134. Selmi DN, Adamson RJ, Attrill H, Goddard AD, Gilbert RJC. 134.  et al. 2011. DNA-templated protein arrays for single-molecule imaging. Nano Lett. 11:657–60 [Google Scholar]
  135. Bai X-C, Martin TG, Scheres SHW, Dietz H. 135.  2012. Cryo-EM structure of a 3D DNA-origami object. PNAS 109:20012–17 [Google Scholar]
  136. Barbalat R, Ewald SE, Mouchess ML, Barton GM. 136.  2011. Nucleic acid recognition by the innate immune system. Annu. Rev. Immunol. 29:185–214 [Google Scholar]
  137. Hwang H-W, Wentzel EA, Mendell JT. 137.  2007. A hexanucleotide element directs microRNA nuclear import. Science 315:97–100 [Google Scholar]
  138. Muddashetty RS, Nalavadi VC, Gross C, Yao X, Xing L. 138.  et al. 2011. Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling. Mol. Cell 42:673–88 [Google Scholar]
  139. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C, Gonzalez S, Sanchez-Cabo F. 139.  et al. 2011. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat. Commun. 2:282 [Google Scholar]
  140. Martin KC, Ephrussi A. 140.  2009. mRNA localization: gene expression in the spatial dimension. Cell 136:719–30 [Google Scholar]
  141. Weinberg Z, Wang JX, Bogue J, Yang J, Corbino K. 141.  et al. 2010. Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes. Genome Biol. 11:R31 [Google Scholar]
  142. Barrick JE, Corbino KA, Winkler WC, Nahvi A, Mandal M. 142.  et al. 2004. New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. PNAS 101:6421–26 [Google Scholar]
  143. Baker JL, Sudarsan N, Weinberg Z, Roth A, Stockbridge RB, Breaker RR. 143.  2012. Widespread genetic switches and toxicity resistance proteins for fluoride. Science 335:233–35 [Google Scholar]
  144. Weinberg Z, Barrick JE, Yao Z, Roth A, Kim JN. 144.  et al. 2007. Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline. Nucleic Acids Res. 35:4809–19 [Google Scholar]
  145. Mandal M, Lee M, Barrick JE, Weinberg Z, Emilsson GM. 145.  et al. 2004. A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 306:275–79 [Google Scholar]
  146. Nelson JW, Sudarsan N, Furukawa K, Weinberg Z, Wang JX, Breaker RR. 146.  2013. Riboswitches in eubacteria sense the second messenger c-di-AMP. Nat. Chem. Biol. 9:834–39 [Google Scholar]
  147. Teo YN, Kool ET. 147.  2009. Polyfluorophore excimers and exciplexes as FRET donors in DNA. Bioconjug. Chem. 20:2371–80 [Google Scholar]
  148. Teo YN, Wilson JN, Kool ET. 148.  2009. Polyfluorophores on a DNA backbone: a multicolor set of labels excited at one wavelength. J. Am. Chem. Soc. 131:3923–33 [Google Scholar]
  149. Wilson JN, Gao J, Kool ET. 149.  2007. Oligodeoxyfluorosides: strong sequence dependence of fluorescence emission. Tetrahedron 63:3427–33 [Google Scholar]
  150. Wilson JN, Kool ET. 150.  2006. Fluorescent DNA base replacements: reporters and sensors for biological systems. Org. Biomol. Chem. 4:4265–74 [Google Scholar]
  151. Kwon H, Jiang W, Kool ET. 151.  2015. Pattern-based detection of anion pollutants in water with DNA polyfluorophores. Chem. Sci. 6:2575–83 [Google Scholar]
  152. Samain F, Dai N, Kool ET. 152.  2011. Differentiating a diverse range of volatile organic compounds with polyfluorophore sensors built on a DNA scaffold. Chemistry 17:174–83 [Google Scholar]
  153. Farlow J, Seo D, Broaders KE, Taylor MJ, Gartner ZJ, Jun Y-W. 153.  2013. Formation of targeted monovalent quantum dots by steric exclusion. Nat. Methods 10:1203–5 [Google Scholar]
  154. Banerjee A, Grazon C, Nadal B, Pons T, Krishnan Y, Dubertret B. 154.  2015. Fast, efficient, and stable conjugation of multiple DNA strands on colloidal quantum dots. Bioconjug. Chem. 26:1582–89 [Google Scholar]
  155. Yuan Z, Chen Y-C, Li H-W, Chang H-T. 155.  2014. Fluorescent silver nanoclusters stabilized by DNA scaffolds. Chem. Commun. 50:9800–15 [Google Scholar]
  156. Dolgosheina EV, Jeng SCY, Panchapakesan SSS, Cojocaru R, Chen PSK. 156.  et al. 2014. RNA Mango aptamer-fluorophore: a bright, high-affinity complex for RNA labeling and tracking. ACS Chem. Biol. 9:2412–20 [Google Scholar]
  157. Keppler A, Gendreizig S, Gronemeyer T, Pick H, Vogel H, Johnsson K. 157.  2003. A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat. Biotechnol. 21:86–89 [Google Scholar]
  158. Muyldermans S. 158.  2013. Nanobodies: natural single-domain antibodies. Annu. Rev. Biochem. 82:775–97 [Google Scholar]
  159. Baskin JM, Prescher JA, Laughlin ST, Agard NJ, Chang PV. 159.  et al. 2007. Copper-free click chemistry for dynamic in vivo imaging. PNAS 104:16793–97 [Google Scholar]
  160. Charron G, Zhang MM, Yount JS, Wilson J, Raghavan AS. 160.  et al. 2009. Robust fluorescent detection of protein fatty-acylation with chemical reporters. J. Am. Chem. Soc. 131:4967–75 [Google Scholar]
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