1932

Abstract

Förster resonance energy transfer (FRET) is a widely used fluorescence-based sensing mechanism. To date, most implementations of FRET sensors have relied on a discrete donor-acceptor pair for detection of each analytical target. FRET networks are an emerging concept in which target recognition perturbs a set of interconnected FRET pathways between multiple emitters. Here, we review the energy transfer topologies and scaffold materials for FRET networks, propose a general nomenclature, and qualitatively summarize the dynamics of the competitive, sequential, homoFRET, and heteroFRET pathways that constitute FRET networks. Implementations of FRET networks for sensing are also described, including concentric FRET probes, other single-vector multiplexing, and logic gates and switches. Unresolved questions and future research directions for current systems are discussed, as are potential but currently unexplored applications of FRET networks in sensing.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-anchem-061020-014925
2022-06-13
2024-05-12
Loading full text...

Full text loading...

/deliver/fulltext/anchem/15/1/annurev-anchem-061020-014925.html?itemId=/content/journals/10.1146/annurev-anchem-061020-014925&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Algar WR, Hildebrandt N, Vogel SS, Medintz IL. 2019. FRET as a biomolecular research tool—understanding its potential while avoiding pitfalls. Nat. Methods 16:9815–29
    [Google Scholar]
  2. 2.
    Wu L, Huang C, Emery BP, Sedgwick AC, Bull SD et al. 2020. Förster resonance energy transfer (FRET)-based small-molecule sensors and imaging agents. Chem. Soc. Rev. 49:155110–39
    [Google Scholar]
  3. 3.
    Greenwald EC, Mehta S, Zhang J. 2018. Genetically encoded fluorescent biosensors illuminate the spatiotemporal regulation of signaling networks. Chem. Rev. 118:2411707–94
    [Google Scholar]
  4. 4.
    Whitney M, Savariar EN, Friedman B, Levin RA, Crisp JL et al. 2013. Ratiometric activatable cell-penetrating peptides provide rapid in vivo readout of thrombin activation. Angew. Chem. Int. Ed. 52:1325–30
    [Google Scholar]
  5. 5.
    Sapsford KE, Algar WR, Berti L, Gemmill KB, Casey BJ et al. 2013. Functionalizing nanoparticles with biological molecules: developing chemistries that facilitate nanotechnology. Chem. Rev. 113:31904–2074
    [Google Scholar]
  6. 6.
    Algar WR, Massey M, Rees K, Higgins R, Krause KD et al. 2021. Photoluminescent nanoparticles for chemical and biological analysis and imaging. Chem. Rev. 121:159243–358
    [Google Scholar]
  7. 7.
    Shen L, Wang P, Ke Y. 2021. DNA nanotechnology-based biosensors and therapeutics. Adv. Healthc. Mater. 10:152002205
    [Google Scholar]
  8. 8.
    Seeman NC, Sleiman HF. 2017. DNA nanotechnology. Nat. Rev. Mater. 3:17068
    [Google Scholar]
  9. 9.
    Mathur D, Medintz IL. 2019. The growing development of DNA nanostructures for potential healthcare-related applications. Adv. Healthc. Mater. 8:91801546
    [Google Scholar]
  10. 10.
    Ke Y, Castro C, Choi JH. 2018. Structural DNA nanotechnology: artificial nanostructures for biomedical research. Annu. Rev. Biomed. Eng. 20:375–401
    [Google Scholar]
  11. 11.
    Rindermann JJ, Akhtman Y, Richardson J, Brown T, Lagoudakis PG. 2011. Gauging the flexibility of fluorescent markers for the interpretation of fluorescence resonance energy transfer. J. Am. Chem. Soc. 133:2279–85
    [Google Scholar]
  12. 12.
    Badali D, Gradinaru CC. 2011. The effect of Brownian motion of fluorescent probes on measuring nanoscale distances by Förster resonance energy transfer. J. Chem. Phys. 134:22225102
    [Google Scholar]
  13. 13.
    Mathur D, Kim YC, Díaz SA, Cunningham PD, Rolczynski BS et al. 2021. Can a DNA origami structure constrain the position and orientation of an attached dye molecule?. J. Phys. Chem. C 125:21509–22
    [Google Scholar]
  14. 14.
    Platnich CM, Rizzuto FJ, Cosa G, Sleiman HF. 2020. Single-molecule methods in structural DNA nanotechnology. Chem. Soc. Rev. 49:134220–33
    [Google Scholar]
  15. 15.
    Mathur D, Medintz IL. 2017. Analyzing DNA nanotechnology: a call to arms for the analytical chemistry community. Anal. Chem. 89:52646–63
    [Google Scholar]
  16. 16.
    Klein WP, Díaz SA, Buckhout-White S, Melinger JS, Cunningham PD et al. 2018. Utilizing homoFRET to extend DNA-scaffolded photonic networks and increase light-harvesting capability. Adv. Opt. Mater. 6:11700679
    [Google Scholar]
  17. 17.
    Buckhout-White S, Spillmann CM, Algar WR, Khachatrian A, Melinger JS et al. 2014. Assembling programmable FRET-based photonic networks using designer DNA scaffolds. Nat. Commun. 5:15615
    [Google Scholar]
  18. 18.
    Sapsford KE, Tyner KM, Dair BJ, Deschamps JR, Medintz IL. 2011. Analyzing nanomaterial bioconjugates: a review of current and emerging purification and characterization techniques. Anal. Chem. 83:124453–88
    [Google Scholar]
  19. 19.
    Wang S, Vyas R, Dwyer C. 2016. Fluorescent taggants with temporally coded signatures. Opt. Express 24:1415528–45
    [Google Scholar]
  20. 20.
    Nellore V, Dwyer C. 2017. Modeling and experimental validation of large scale fluorescence sensor networks. 2017 IEEE 17th International Conference on Bioinformatics and Bioengineering (BIBE)217–22 Piscataway, NJ: IEEE
    [Google Scholar]
  21. 21.
    Nakagawa M, Miyata Y, Tate N, Nishimura T, Shimomura S et al. 2021. Spatiotemporal model for FRET networks with multiple donors and acceptors: multicomponent exponential decay derived from the master equation. J. Opt. Soc. Am. B 38:2294–99
    [Google Scholar]
  22. 22.
    Melinger JS, Khachatrian A, Ancona MG, Buckhout-White S, Goldman ER et al. 2016. FRET from multiple pathways in fluorophore-labeled DNA. ACS Photon 3:4659–69
    [Google Scholar]
  23. 23.
    Cunningham PD, Spillmann CM, Melinger JS, Ancona MG, Kim YC et al. 2021. Förster resonance energy transfer in linear DNA multifluorophore photonic wires: comparing dual versus split rail building block designs. Adv. Opt. Mater. 9:212100884
    [Google Scholar]
  24. 24.
    Nicoli F, Barth A, Bae W, Neukirchinger F, Crevenna AH et al. 2017. Directional photonic wire mediated by homo-Förster resonance energy transfer on a DNA origami platform. ACS Nano 11:1111264–72
    [Google Scholar]
  25. 25.
    Díaz SA, Buckhout-White S, Ancona MG, Spillmann CM, Goldman ER et al. 2016. Extending DNA-based molecular photonic wires with homogeneous Förster resonance energy transfer. Adv. Opt. Mater. 4:3399–412
    [Google Scholar]
  26. 26.
    Klein WP, Rolczynski BS, Oliver SM, Zadegan R, Buckhout-White S et al. 2020. DNA origami chromophore scaffold exploiting homoFRET energy transport to create molecular photonic wires. ACS Appl. Nano Mater. 3:43323–36
    [Google Scholar]
  27. 27.
    Mazuski RJ, Díaz SA, Wood RE, Lloyd LT, Klein WP et al. 2020. Ultrafast excitation transfer in Cy5 DNA photonic wires displays dye conjugation and excitation energy dependency. J. Phys. Chem. Lett. 11:104163–72
    [Google Scholar]
  28. 28.
    Tsai H-Y, Kim H, Massey M, Krause KD, Algar WR. 2019. Concentric FRET: a review of the emerging concept, theory, and applications. Methods Appl. Fluoresc. 7:4042001
    [Google Scholar]
  29. 29.
    Massey M, Kim H, Conroy EM, Algar WR. 2017. Expanded quantum dot-based concentric Förster resonance energy transfer: adding and characterizing energy-transfer pathways for triply multiplexed biosensing. J. Phys. Chem. C 121:2413345–56
    [Google Scholar]
  30. 30.
    Algar WR, Ancona MG, Malanoski AP, Susumu K, Medintz IL. 2012. Assembly of a concentric Förster resonance energy transfer relay on a quantum dot scaffold: characterization and application to multiplexed protease sensing. ACS Nano 6:1211044–58
    [Google Scholar]
  31. 31.
    Wang B, Wang X, Wei B, Huang F, Yao D, Liang H. 2017. DNA photonic nanowires with tunable FRET signals on the basis of toehold-mediated DNA strand displacement reactions. Nanoscale 9:92981–85
    [Google Scholar]
  32. 32.
    Hu J, Li W-C, Qiu J-G, Jiang B, Zhang C-Y. 2020. A multifunctional DNA nanostructure based on multicolor FRET for nuclease activity assay. Analyst 145:186054–60
    [Google Scholar]
  33. 33.
    Hu J, Liu M-H, Zhang C-Y. 2019. Construction of tetrahedral DNA-quantum dot nanostructure with the integration of multistep Förster resonance energy transfer for multiplex enzymes assay. ACS Nano 13:67191–201
    [Google Scholar]
  34. 34.
    Algar WR, Malanoski AP, Susumu K, Stewart MH, Hildebrandt N, Medintz IL. 2012. Multiplexed tracking of protease activity using a single color of quantum dot vector and a time-gated Förster resonance energy transfer relay. Anal. Chem. 84:2210136–46
    [Google Scholar]
  35. 35.
    Algar WR, Wegner D, Huston AL, Blanco-Canosa JB, Stewart MH et al. 2012. Quantum dots as simultaneous acceptors and donors in time-gated Förster resonance energy transfer relays: characterization and biosensing. J. Am. Chem. Soc. 134:31876–91
    [Google Scholar]
  36. 36.
    Samanta A, Walper SA, Susumu K, Dwyer CL, Medintz IL. 2015. An enzymatically-sensitized sequential and concentric energy transfer relay self-assembled around semiconductor quantum dots. Nanoscale 7:177603–14
    [Google Scholar]
  37. 37.
    Conroy EM, Algar WR. 2014. Evaluation of quantum dot-based concentric FRET configurations with a fluorescent dye and dark quencher for multiplexed bioanalyses. Proc. SPIE 8955, Colloid. Nanoparticles Biomed. Appl. IX, 89550U. https://doi.org/10.1117/12.2040585
    [Crossref] [Google Scholar]
  38. 38.
    Li JJ, Algar WR. 2016. A long-wavelength quantum dot-concentric FRET configuration: characterization and application in a multiplexed hybridization assay. Analyst 141:123636–47
    [Google Scholar]
  39. 39.
    Wu M, Petryayeva E, Algar WR. 2014. Quantum dot-based concentric FRET configuration for the parallel detection of protease activity and concentration. Anal. Chem. 86:2211181–88
    [Google Scholar]
  40. 40.
    Wu M, Algar WR. 2015. Concentric Förster resonance energy transfer imaging. Anal. Chem. 87:168078–83
    [Google Scholar]
  41. 41.
    Wu M, Massey M, Petryayeva E, Algar WR. 2015. Energy transfer pathways in a quantum dot-based concentric FRET configuration. J. Phys. Chem. C 119:4626183–95
    [Google Scholar]
  42. 42.
    Conroy EM, Li JJ, Kim H, Algar WR. 2016. Self-quenching, dimerization, and homo-FRET in hetero-FRET assemblies with quantum dot donors and multiple dye acceptors. J. Phys. Chem. C 120:3117817–28
    [Google Scholar]
  43. 43.
    Samanta A, Buckhout-White S, Oh E, Susumu K, Medintz IL. 2018. Exploring attachment chemistry with FRET in hybrid quantum dot dye-labeled DNA dendrimer composites. Mol. Syst. Des. Eng. 3:2314–27
    [Google Scholar]
  44. 44.
    Sapsford KE, Pons T, Medintz IL, Higashiya S, Brunel FM et al. 2007. Kinetics of metal-affinity driven self-assembly between proteins or peptides and CdSe-ZnS quantum dots. J. Phys. Chem. C 111:3111528–38
    [Google Scholar]
  45. 45.
    Aldeek F, Safi M, Zhan N, Palui G, Mattoussi H. 2013. Understanding the self-assembly of proteins onto gold nanoparticles and quantum dots driven by metal-histidine coordination. ACS Nano 7:1110197–210
    [Google Scholar]
  46. 46.
    Bradburne CE, Delehanty JB, Gemmill KB, Mei BC, Mattoussi H et al. 2013. Cytotoxicity of quantum dots used for in vitro cellular labeling: role of QD surface ligand, delivery modality, cell type, and direct comparison to organic fluorophores. Bioconjug. Chem. 24:91570–83
    [Google Scholar]
  47. 47.
    Tsoi KM, Dai Q, Alman BA, Chan WCW. 2013. Are quantum dots toxic? Exploring the discrepancy between cell culture and animal studies. Acc. Chem. Res. 46:3662–71
    [Google Scholar]
  48. 48.
    Yong K-T, Law W-C, Hu R, Ye L, Liu L et al. 2013. Nanotoxicity assessment of quantum dots: from cellular to primate studies. Chem. Soc. Rev. 42:31236–50
    [Google Scholar]
  49. 49.
    Tsai H-Y, Algar WR 2022. A dendrimer-based time-gated concentric FRET configuration for multiplexed sensing. ACS Nano https://doi.org/10.1021/acsnano.2c01473
    [Crossref] [Google Scholar]
  50. 50.
    Sednev MV, Belov VN, Hell SW. 2015. Fluorescent dyes with large Stokes shifts for super-resolution optical microscopy of biological objects: a review. Methods Appl. Fluoresc. 3:4042004
    [Google Scholar]
  51. 51.
    Chen C, Fang C. 2020. Devising efficient red-shifting strategies for bioimaging: a generalizable donor-acceptor fluorophore prototype. Chem. Asian J. 15:101514–23
    [Google Scholar]
  52. 52.
    Meza Ramirez CA, Greenop M, Ashton L, Rehman IU 2021. Applications of machine learning in spectroscopy. Appl. Spectrosc. Rev. 56:733–63
    [Google Scholar]
  53. 53.
    Spillmann CM, Ancona MG, Buckhout-White S, Algar WR, Stewart MH et al. 2013. Achieving effective terminal exciton delivery in quantum dot antenna-sensitized multistep DNA photonic wires. ACS Nano 7:87101–18
    [Google Scholar]
  54. 54.
    Lin Y, Nienhaus K, Nienhaus GU. 2018. Nanoparticle probes for super-resolution fluorescence microscopy. ChemNanoMat 4:3253–64
    [Google Scholar]
  55. 55.
    Wei Y, Quan L, Zhou C, Zhan Q. 2018. Factors relating to the biodistribution & clearance of nanoparticles & their effects on in vivo application. Nanomedicine 13:121495–512
    [Google Scholar]
  56. 56.
    Dehaini D, Fang RH, Zhang L. 2016. Biomimetic strategies for targeted nanoparticle delivery. Bioeng. Transl. Med. 1:130–46
    [Google Scholar]
  57. 57.
    Singh N, Marets C, Boudon J, Millot N, Saviot L, Maurizi L. 2021. In vivo protein corona on nanoparticles: Does the control of all material parameters orient the biological behavior?. Nanoscale Adv 3:51209–29
    [Google Scholar]
  58. 58.
    Rampado R, Crotti S, Caliceti P, Pucciarelli S, Agostini M. 2020. Recent advances in understanding the protein corona of nanoparticles and in the formulation of “stealthy” nanomaterials. Front. Bioeng. Biotechnol. 8:166
    [Google Scholar]
  59. 59.
    Kong B, Seog JH, Graham LM, Lee SB. 2011. Experimental considerations on the cytotoxicity of nanoparticles. Nanomedicine 6:5929–41
    [Google Scholar]
  60. 60.
    Joris F, Manshian BB, Peynshaert K, De Smedt SC, Braeckmans K, Soenen SJ. 2013. Assessing nanoparticle toxicity in cell-based assays: influence of cell culture parameters and optimized models for bridging the in vitro-in vivo gap. Chem. Soc. Rev. 42:218339–59
    [Google Scholar]
  61. 61.
    Algar WR, Khachatrian A, Melinger JS, Huston AL, Stewart MH et al. 2017. Concurrent modulation of quantum dot photoluminescence using a combination of charge transfer and Förster resonance energy transfer: competitive quenching and multiplexed biosensing modality. J. Am. Chem. Soc. 139:1363–72
    [Google Scholar]
  62. 62.
    Li Y, Du H, Wang W, Zhang P, Xu L et al. 2016. A versatile multiple target detection system based on DNA nano-assembled linear FRET arrays. Sci. Rep. 6:126879
    [Google Scholar]
  63. 63.
    Nishimura T, Ogura Y, Tanida J. 2012. Fluorescence resonance energy transfer-based molecular logic circuit using a DNA scaffold. Appl. Phys. Lett. 101:23233703
    [Google Scholar]
  64. 64.
    Cannon BL, Kellis DL, Davis PH, Lee J, Kuang W et al. 2015. Excitonic AND logic gates on DNA brick nanobreadboards. ACS Photon 2:3398–404
    [Google Scholar]
  65. 65.
    Massey M, Medintz IL, Ancona MG, Algar WR. 2017. Time-gated FRET and DNA-based photonic molecular logic gates: AND, OR, NAND, and NOR. ACS Sens 2:81205–14
    [Google Scholar]
  66. 66.
    Buckhout-White S, Claussen JC, Melinger JS, Dunningham Z, Ancona MG et al. 2014. A triangular three-dye DNA switch capable of reconfigurable molecular logic. RSC Adv. 4:9048860–71
    [Google Scholar]
  67. 67.
    Buckhout-White S, Brown CW3rd, Hastman DA, Ancona MG, Melinger JS, et al. 2016. Expanding molecular logic capabilities in DNA-scaffolded multiFRET triads. RSC Adv 6:10097587–98
    [Google Scholar]
  68. 68.
    LaBoda CD, Lebeck AR, Dwyer CL. 2017. An optically modulated self-assembled resonance energy transfer pass gate. Nano Lett 17:63775–81
    [Google Scholar]
  69. 69.
    LaBoda C, Dwyer C, Lebeck AR. 2017. Exploiting dark fluorophore states to implement resonance energy transfer pre-charge logic. IEEE Micro 37:452–62
    [Google Scholar]
  70. 70.
    Bui H, Brown CW3rd, Buckhout-White S, Díaz SA, Stewart MH et al. 2019. Transducing protease activity into DNA output for developing smart bionanosensors. Small 15:141805384
    [Google Scholar]
  71. 71.
    Peng H-Q, Niu L-Y, Chen Y-Z, Wu L-Z, Tung C-H, Yang Q-Z. 2015. Biological applications of supramolecular assemblies designed for excitation energy transfer. Chem. Rev. 115:157502–42
    [Google Scholar]
  72. 72.
    Şener M, Strümpfer J, Hsin J, Chandler D, Scheuring S et al. 2011. Förster energy transfer theory as reflected in the structures of photosynthetic light-harvesting systems. ChemPhysChem 12:3518–31
    [Google Scholar]
  73. 73.
    Brown CW3rd, Samanta A, Díaz SA, Buckhout-White S, Walper SA et al. 2017. Dendrimeric DNA nanostructures as scaffolds for efficient bidirectional BRET-FRET cascades. Adv. Opt. Mater. 5:141700181
    [Google Scholar]
  74. 74.
    Bigdeli A, Ghasemi F, Golmohammadi H, Abbasi-Moayed S, Nejad MAF et al. 2017. Nanoparticle-based optical sensor arrays. Nanoscale 9:4316546–63
    [Google Scholar]
  75. 75.
    Geng Y, Peveler WJ, Rotello VM. 2019. Array-based “chemical nose” sensing in diagnostics and drug discovery. Angew. Chem. Int. Ed. 58:165190–200
    [Google Scholar]
  76. 76.
    Li Z, Askim JR, Suslick KS. 2019. The optoelectronic nose: colorimetric and fluorometric sensor arrays. Chem. Rev. 119:1231–92
    [Google Scholar]
  77. 77.
    Ralbovsky NM, Lednev IK. 2020. Towards development of a novel universal medical diagnostic method: Raman spectroscopy and machine learning. Chem. Soc. Rev. 49:207428–53
    [Google Scholar]
/content/journals/10.1146/annurev-anchem-061020-014925
Loading
/content/journals/10.1146/annurev-anchem-061020-014925
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error