In Vivo Biosensing Using Resonance Energy Transfer

Shashi Bhuckory; Joshua C. Kays; Allison M. Dennis

doi:10.3390/bios9020076

journal article Open Access Jun 03, 2019

In Vivo Biosensing Using Resonance Energy Transfer

Shashi Bhuckory

Joshua C. Kays Allison M. Dennis

Biosensors Vol. 9 No. 2 pp. 76 · MDPI AG

View at Publisher Save 10.3390/bios9020076

Abstract

Solution-phase and intracellular biosensing has substantially enhanced our understanding of molecular processes foundational to biology and pathology. Optical methods are favored because of the low cost of probes and instrumentation. While chromatographic methods are helpful, fluorescent biosensing further increases sensitivity and can be more effective in complex media. Resonance energy transfer (RET)-based sensors have been developed to use fluorescence, bioluminescence, or chemiluminescence (FRET, BRET, or CRET, respectively) as an energy donor, yielding changes in emission spectra, lifetime, or intensity in response to a molecular or environmental change. These methods hold great promise for expanding our understanding of molecular processes not just in solution and in vitro studies, but also in vivo, generating information about complex activities in a natural, organismal setting. In this review, we focus on dyes, fluorescent proteins, and nanoparticles used as energy transfer-based optical transducers in vivo in mice; there are examples of optical sensing using FRET, BRET, and in this mammalian model system. After a description of the energy transfer mechanisms and their contribution to in vivo imaging, we give a short perspective of RET-based in vivo sensors and the importance of imaging in the infrared for reduced tissue autofluorescence and improved sensitivity.

Topics

No keywords indexed for this article. Browse by subject →

References

170

[1]

Russell "Imaging calcium signals in vivo: A powerful tool in physiology and pharmacology" Br. J. Pharmacol. (2011) 10.1111/j.1476-5381.2010.00988.x

[2]

Koo "Non-invasive in vivo imaging in small animal research" Anal. Cell. Pathol. (2006) 10.1155/2006/245619

[3]

Hemmer "Optical nanoprobes for biomedical applications: Shining a light on upconverting and near-infrared emitting nanoparticles for imaging, thermal sensing, and photodynamic therapy" J. Mater. Chem. B (2017) 10.1039/c7tb00403f

[4]

Rong "In Vivo Biosensing: Progress and Perspectives" ACS Sens. (2017) 10.1021/acssensors.6b00834

[5]

Kang "Bioresorbable silicon electronic sensors for the brain" Nature (2016) 10.1038/nature16492

[6]

Unruh "Preclinical Evaluation of Poly(HEMA-co-acrylamide) Hydrogels Encapsulating Glucose Oxidase and Palladium Benzoporphyrin as Fully Implantable Glucose Sensors" J. Diabetes Sci. Technol. (2015) 10.1177/1932296815590439

[7]

Nanomaterials with enzyme-like characteristics (nanozymes): next-generation artificial enzymes

Hui Wei, Erkang Wang

Chemical Society Reviews 2013 10.1039/c3cs35486e

[8]

Cheng "Integrated Nanozymes with Nanoscale Proximity for in Vivo Neurochemical Monitoring in Living Brains" Anal. Chem. (2016) 10.1021/acs.analchem.6b00975

[9]

Medintz, I., and Hildebrandt, N. (2013). Förster Theory. FRET—Förster Resonance Energy Transfer, Wiley-VCH Verlag GmbH & Co. KGaA. 10.1002/9783527656028

[10]

Curutchet "Fretting about FRET: Failure of the Ideal Dipole Approximation" Biophys. J. (2009) 10.1016/j.bpj.2009.03.052

[11]

Medintz, I., and Hildebrandt, N. (2013). How to Apply FRET: From Experimental Design to Data Analysis. FRET—Förster Resonance Energy Transfer, Wiley-VCH Verlag GmbH & Co. KGaA. 10.1002/9783527656028

[12]

Bernard, V., and Berberan-Santos, M.N. (2012). Molecular Fluorescence: Principles and Applications, Wiley. [2nd ed.].

[13]

Forster "Energiewanderung und Fluoreszenz" Naturwissenschaften (1946) 10.1007/bf00585226

[14]

"Zwischenmolekulare Energiewanderung und Fluoreszenz" Ann. Phys. (1948) 10.1002/andp.19484370105

[15]

Chou "Förster Resonance Energy Transfer between Quantum Dot Donors and Quantum Dot Acceptors" Sensors (2015) 10.3390/s150613288

[16]

Lakowicz, J.R. (2006). Principles of Fluorescence Spectroscopy, Springer. 10.1007/978-0-387-46312-4

[17]

Clapp "Fluorescence Resonance Energy Transfer Between Quantum Dot Donors and Dye-Labeled Protein Acceptors" J. Am. Chem. Soc. (2004) 10.1021/ja037088b

[18]

Sapsford "Materials for Fluorescence Resonance Energy Transfer Analysis: Beyond Traditional Donor–Acceptor Combinations" Angew. Chem. Int. Ed. (2006) 10.1002/anie.200503873

[19]

Pediani "Applications of fluorescence and bioluminescence resonance energy transfer to drug discovery at G protein coupled receptors" Anal. Bioanal. Chem. (2010) 10.1007/s00216-010-3823-4

[20]

Roda "Bioluminescence in analytical chemistry and in vivo imaging" TrAC Trends Anal. Chem. (2009) 10.1016/j.trac.2008.11.015

[21]

Badr "Bioluminescence imaging: Progress and applications" Trends Biotechnol. (2011) 10.1016/j.tibtech.2011.06.010

[22]

Engineered Luciferase Reporter from a Deep Sea Shrimp Utilizing a Novel Imidazopyrazinone Substrate

Mary P. Hall, James Unch, Brock F. Binkowski et al.

ACS Chemical Biology 2012 10.1021/cb3002478

[23]

BIOLUMINESCENCE

Thérèse Wilson, J. Woodland Hastings

Annual Review of Cell and Developmental Biology 1998 10.1146/annurev.cellbio.14.1.197

[24]

Prescher "Guided by the light: Visualizing biomolecular processes in living animals with bioluminescence" Curr. Opin. Chem. Biol. (2010) 10.1016/j.cbpa.2009.11.001

[25]

De "An Improved Bioluminescence Resonance Energy Transfer Strategy for Imaging Intracellular Events in Single Cells and Living Subjects" Cancer Res. (2007) 10.1158/0008-5472.can-06-4623

[26]

So "Self-illuminating quantum dot conjugates for in vivo imaging" Nat. Biotechnol. (2006) 10.1038/nbt1188

[27]

Wu "In vivo far-red luminescence imaging of a biomarker based on BRET from Cypridina bioluminescence to an organic dye" Proc. Natl. Acad. Sci. USA (2009) 10.1073/pnas.0908594106

[28]

Shakhmin "Coelenterazine analogues emit red-shifted bioluminescence with NanoLuc" Org. Biomol. Chem. (2017) 10.1039/c7ob01985h

[29]

Khan "Luminol-Based Chemiluminescent Signals: Clinical and Non-clinical Application and Future Uses" Appl. Biochem. Biotechnol. (2014) 10.1007/s12010-014-0850-1

[30]

Medintz, I., and Hildebrandt, N. (2013). Materials for FRET Analysis: Beyond Traditional Dye–Dye Combinations. FRET—Förster Resonance Energy Transfer, Wiley-VCH Verlag GmbH & Co. KGaA. 10.1002/9783527656028

[31]

Kurose "Bioluminescence of the Ca2+-binding photoprotein aequorin after cysteine modification" Proc. Natl. Acad. Sci. USA (1989) 10.1073/pnas.86.1.80

[32]

Roda "Discovery and development of the green fluorescent protein, GFP: The 2008 Nobel Prize" Anal. Bioanal. Chem. (2010) 10.1007/s00216-010-3452-y

[33]

Xia "Biosensing and imaging based on bioluminescence resonance energy transfer" Curr. Opin. Biotechnol. (2009) 10.1016/j.copbio.2009.01.001

[34]

De "BRET3: A red-shifted bioluminescence resonance energy transfer (BRET)-based integrated platform for imaging protein–protein interactions from single live cells and living animals" FASEB J. (2009) 10.1096/fj.08-118919

[35]

Cai, W. (2014). Engineering Aspects of Bioluminescence Resonance Energy Transfer Systems. Engineering in Translational Medicine, Springer. 10.1007/978-1-4471-4372-7

[36]

NanoBRET—A Novel BRET Platform for the Analysis of Protein–Protein Interactions

Thomas Machleidt, Carolyn C. Woodroofe, Marie K. Schwinn et al.

ACS Chemical Biology 2015 10.1021/acschembio.5b00143

[37]

"Recent Applications of Chemiluminescence Assays in Clinical Immunology" Mini-Rev. Med. Chem. (2010) 10.2174/138955710793564142

[38]

Roda "Analytical chemiluminescence and bioluminescence: Latest achievements and new horizons" Anal. Bioanal. Chem. (2012) 10.1007/s00216-011-5455-8

[39]

Gravier "Fluorescent Nanoprobes Dedicated to in Vivo Imaging: From Preclinical Validations to Clinical Translation" Molecules (2012) 10.3390/molecules17055564

[40]

Garland "A bright future for precision medicine: Advances in fluorescent chemical probe design and their clinical application" Cell Chem. Biol. (2016) 10.1016/j.chembiol.2015.12.003

[41]

Hemmer "Exploiting the biological windows: Current perspectives on fluorescent bioprobes emitting above 1000 nm" Nanoscale Horiz. (2016) 10.1039/c5nh00073d

[42]

Clement "Optimising the design of a broad-band light source for the treatment of skin" J. Cosmet. Laser Ther. (2005) 10.1080/14764170500344575

[43]

Light in diagnosis, therapy and surgery

Seok Hyun Yun, Sheldon J. J. Kwok

Nature Biomedical Engineering 2017 10.1038/s41551-016-0008

[44]

Kobayashi "New Strategies for Fluorescent Probe Design in Medical Diagnostic Imaging" Chem. Rev. (2010) 10.1021/cr900263j

[45]

Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer

Roger Heim, Roger Y Tsien

Current Biology 1996 10.1016/s0960-9822(02)00450-5

[46]

Chang "Protease-activated quantum dot probes" Biochem. Biophys. Res. Commun. (2005) 10.1016/j.bbrc.2005.07.028

[47]

Clapp "Quantum Dot-Based Multiplexed Fluorescence Resonance Energy Transfer" J. Am. Chem. Soc. (2005) 10.1021/ja054630i

[48]

Kuningas "Homogeneous Assay Technology Based on Upconverting Phosphors" Anal. Chem. (2005) 10.1021/ac0510944

[49]

Xu "A self-assembled quantum dot probe for detecting β-lactamase activity" Biochem. Biophys. Res. Commun. (2006) 10.1016/j.bbrc.2006.03.225

[50]

Kuningas "Upconversion Fluorescence Enables Homogeneous Immunoassay in Whole Blood" Clin. Chem. (2007) 10.1373/clinchem.2006.076687

Showing 50 of 170 references

Metrics

51

Citations

170

References

Details

Published: Jun 03, 2019
Vol/Issue: 9(2)
Pages: 76
License: View

Authors

S

Shashi Bhuckory

Department of Biomedical Engineering, Boston University, Boston, MA 02215, USA

J

Joshua C. Kays

Department of Biomedical Engineering, Boston University, Boston, MA 02215, USA

A

Allison M. Dennis

Department of Biomedical Engineering, Boston University, Boston, MA 02215, USA; Division of Materials Science and Engineering, Boston University, Boston, MA 02215, USA

Funding

National Institutes of Health Award: T32 GM008764

Cite This Article

Shashi Bhuckory, Joshua C. Kays, Allison M. Dennis (2019). In Vivo Biosensing Using Resonance Energy Transfer. Biosensors, 9(2), 76. https://doi.org/10.3390/bios9020076

In Vivo Biosensing Using Resonance Energy Transfer

You May Also Like