Hostname: page-component-6766d58669-l4t7p Total loading time: 0 Render date: 2026-05-21T05:15:52.282Z Has data issue: false hasContentIssue false
  • English
  • Français

From resting potential to dynamics: advances in membrane voltage indicators and imaging techniques

Published online by Cambridge University Press:  16 January 2025

Reyhaneh Shakibi Open the ORCID record for Reyhaneh Shakibi [Opens in a new window] ,
Fatemeh Yazdipour Open the ORCID record for Fatemeh Yazdipour [Opens in a new window] ,
Hamed Abadijoo Open the ORCID record for Hamed Abadijoo [Opens in a new window] ,
Navid Manoochehri Open the ORCID record for Navid Manoochehri [Opens in a new window] ,
Farshid Rostami Pouria Open the ORCID record for Farshid Rostami Pouria [Opens in a new window] ,
Taraneh Bajooli Open the ORCID record for Taraneh Bajooli [Opens in a new window] ,
Hossein Simaee Open the ORCID record for Hossein Simaee [Opens in a new window] ,
Parviz Abdolmaleki Open the ORCID record for Parviz Abdolmaleki [Opens in a new window] ,
Ali Khatibi Open the ORCID record for Ali Khatibi [Opens in a new window]  and
Mohammad Abdolahad Open the ORCID record for Mohammad Abdolahad [Opens in a new window]
...Show all authors
Reyhaneh Shakibi
Affiliation:
Institute of Biochemistry and Biophysics (IBB), University of Tehran, Tehran, Iran Integrated Biophysics and Bioengineering Lab (iBL), Institute of Biochemistry and Biophysics, University of Tehran, Tehran, Iran Faculty of Biological Sciences, Tarbiat Modares University, Tehran, Iran
Fatemeh Yazdipour
Affiliation:
Institute of Biochemistry and Biophysics (IBB), University of Tehran, Tehran, Iran Integrated Biophysics and Bioengineering Lab (iBL), Institute of Biochemistry and Biophysics, University of Tehran, Tehran, Iran
Hamed Abadijoo
Affiliation:
Institute of Biochemistry and Biophysics (IBB), University of Tehran, Tehran, Iran Integrated Biophysics and Bioengineering Lab (iBL), Institute of Biochemistry and Biophysics, University of Tehran, Tehran, Iran Nano Electronic Center of Excellence, Nano Bio Electronic Devices Lab, School of Electrical and Computer Engineering, University of Tehran, Tehran, Iran
Navid Manoochehri
Affiliation:
Institute of Biochemistry and Biophysics (IBB), University of Tehran, Tehran, Iran Integrated Biophysics and Bioengineering Lab (iBL), Institute of Biochemistry and Biophysics, University of Tehran, Tehran, Iran Nano Electronic Center of Excellence, Nano Bio Electronic Devices Lab, School of Electrical and Computer Engineering, University of Tehran, Tehran, Iran
Farshid Rostami Pouria
Affiliation:
Institute of Biochemistry and Biophysics (IBB), University of Tehran, Tehran, Iran Integrated Biophysics and Bioengineering Lab (iBL), Institute of Biochemistry and Biophysics, University of Tehran, Tehran, Iran Nano Electronic Center of Excellence, Nano Bio Electronic Devices Lab, School of Electrical and Computer Engineering, University of Tehran, Tehran, Iran
Taraneh Bajooli
Affiliation:
Institute of Biochemistry and Biophysics (IBB), University of Tehran, Tehran, Iran Integrated Biophysics and Bioengineering Lab (iBL), Institute of Biochemistry and Biophysics, University of Tehran, Tehran, Iran School of Electrical and Computer Engineering, Faculty of Engineering, University of Tehran, Tehran, Iran
Hossein Simaee
Affiliation:
Institute of Biochemistry and Biophysics (IBB), University of Tehran, Tehran, Iran Integrated Biophysics and Bioengineering Lab (iBL), Institute of Biochemistry and Biophysics, University of Tehran, Tehran, Iran
Parviz Abdolmaleki
Affiliation:
Faculty of Biological Sciences, Tarbiat Modares University, Tehran, Iran
Ali Khatibi
Affiliation:
Department of Biotechnology, Faculty of Biological Sciences, Alzahra University, Tehran, Iran
Mohammad Abdolahad
Affiliation:
Nano Electronic Center of Excellence, Nano Bio Electronic Devices Lab, School of Electrical and Computer Engineering, University of Tehran, Tehran, Iran
Ali Akbar Moosavi-Movahhedi
Affiliation:
Institute of Biochemistry and Biophysics (IBB), University of Tehran, Tehran, Iran
Mohammad Ali Khayamian*
Affiliation:
Institute of Biochemistry and Biophysics (IBB), University of Tehran, Tehran, Iran Integrated Biophysics and Bioengineering Lab (iBL), Institute of Biochemistry and Biophysics, University of Tehran, Tehran, Iran
*
Corresponding author: Mohammad Ali Khayamian; Emails: m.a.khayamian@ut.ac.ir; m.a.khayamian@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

The membrane potential is a critical aspect of cellular physiology, essential for maintaining homeostasis, facilitating signal transduction, and driving various cellular processes. While the resting membrane potential (RMP) represents a key physiological parameter, membrane potential fluctuations, such as depolarization and hyperpolarization, are equally vital in understanding dynamic cellular behavior. Traditional techniques, such as microelectrodes and patch-clamp methods, offer valuable insights but are invasive and less suited for high-throughput applications. Recent advances in voltage indicators, including fast and slow dyes, and novel imaging modalities such as second harmonic generation (SHG) and photoacoustic imaging, enable noninvasive, high-resolution measurement of both RMP and membrane potential dynamics. This review explores the mechanisms, development, and applications of these tools, emphasizing their transformative potential in neuroscience and cellular electrophysiology research.

Keywords

BODIPYsphotoacoustic imagingquantum dotresting membrane potential (RMP)second harmonic generationgenetically encoded voltage indicators

Information

Type
Review
Information
Quarterly Reviews of Biophysics , Volume 58 , 2025 , e7
Copyright
© The Author(s), 2025. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

Footnotes

This article was originally published with incomplete funding information. The error has been corrected and the online HTML and PDF versions updated.

References

Aalinkeel, R, Nair, B, Reynolds, JL, Sykes, DE, Law, W-C, Mahajan, SD, Prasad, PN and Schwartz, SA (2012) Quantum rods as nanocarriers of gene therapy. Drug Delivery 19(4), 220–231.CrossRefGoogle ScholarPubMed
Abdul Kadir, L, Stacey, M and Barrett-Jolley, R (2018) Emerging roles of the membrane potential: action beyond the action potential. Frontiers in Physiology 9, 1661.CrossRefGoogle ScholarPubMed
Adams, DS and Levin, M (2012a) General principles for measuring resting membrane potential and ion concentration using fluorescent bioelectricity reporters. Cold Spring Harbor Protocols 2012(4), pdb. top067710.Google ScholarPubMed
Adams, DS and Levin, M (2012b) Measuring resting membrane potential using the fluorescent voltage reporters DiBAC4 (3) and CC2-DMPE. Cold Spring Harbor Protocols 2012(4), pdb. prot067702.Google ScholarPubMed
Aghigh, A, Bancelin, S, Rivard, M, Pinsard, M, Ibrahim, H and Légaré, F (2023) Second harmonic generation microscopy: a powerful tool for bio-imaging. Biophysical Reviews 15(1), 43–70.CrossRefGoogle ScholarPubMed
Aguilar, AA, Ho, MC, Chang, E, Carlson, KW, Natarajan, A, Marciano, T, Bomzon, Ze and Patel, CB (2021) Permeabilizing cell membranes with electric fields. Cancers 13(9), 2283.Google ScholarPubMed
Ansaryan, S, Khayamian, MA, Saghafi, M, Shalileh, S, Nikshoar, MS, Abbasvandi, F, Mahmoudi, M, Bahrami, F and Abdolahad, M (2019) Stretch induces invasive phenotypes in breast cells due to activation of aerobic-glycolysis-related pathways. Advanced Biosystems 3(7), 1800294. https://doi.org/10.1002/adbi.201800294.Google ScholarPubMed
Azimi Hashemi, N, Bergs, AC, Schüler, C, Scheiwe, AR, Steuer Costa, W, Bach, M, Liewald, JF and Gottschalk, A (2019) Rhodopsin-based voltage imaging tools for use in muscles and neurons of Caenorhabditis elegans . Proceedings of the National Academy of Sciences 116(34), 17051–17060.Google ScholarPubMed
Bacalum, M, Wang, L, Boodts, S, Yuan, P, Leen, V, Smisdom, N, Fron, E, Knippenberg, S, Fabre, G and Trouillas, P (2016) A blue-light-emitting BODIPY probe for lipid membranes. Langmuir 32(14), 3495–3505.Google ScholarPubMed
Bai, L, Cong, L, Shi, Z, Zhao, Y, Zhang, Y, Lu, B, Zhang, J, Xiong, Z-Q, Xu, N and Mu, Y (2024) Volumetric voltage imaging of neuronal populations in the mouse brain by confocal light-field microscopy. Nature Methods, 1–11.Google ScholarPubMed
Bajar, BT, Wang, ES, Zhang, S, Lin, MZ and Chu, J (2016) A guide to fluorescent protein FRET pairs. Sensors 16(9), 1488.Google ScholarPubMed
Baker, B, Mutoh, H, Dimitrov, D, Akemann, W, Perron, A, Iwamoto, Y, Jin, L, Cohen, L, Isacoff, E and Pieribone, V (2008) Genetically encoded fluorescent sensors of membrane potential. Brain cell biology 36, 53–67.Google ScholarPubMed
Bando, Y, Grimm, C, Cornejo, VH and Yuste, R (2019) Genetic voltage indicators. BMC biology 17, 1–12.CrossRefGoogle ScholarPubMed
Barbosa, RCS and Mendes, PM (2022) A comprehensive review on photoacoustic-based devices for biomedical applications. Sensors 22(23), 9541.Google ScholarPubMed
Barykina, NV, Subach, OM, Doronin, DA, Sotskov, VP, Roshchina, MA, Kunitsyna, TA, Malyshev, AY, Smirnov, IV, Azieva, AM and Sokolov, IS (2016) A new design for a green calcium indicator with a smaller size and a reduced number of calcium-binding sites. Scientific Reports 6(1), 34447.Google Scholar
Bassett, JJ and Monteith, GR (2017) Genetically encoded calcium indicators as probes to assess the role of calcium channels in disease and for high-throughput drug discovery. Advances in Pharmacology 79, 141–171.Google ScholarPubMed
Baxter, DF, Kirk, M, Garcia, AF, Raimondi, A, Holmqvist, MH, Flint, KK, Bojanic, D, Distefano, PS, Curtis, R and Xie, Y (2002) A novel membrane potential-sensitive fluorescent dye improves cell-based assays for ion channels. Journal of biomolecular screening 7(1), 79–85.CrossRefGoogle ScholarPubMed
Beard, P (2011) Biomedical photoacoustic imaging. Interface focus 1(4), 602–631.Google ScholarPubMed
Beck, C, Zhang, D and Gong, Y (2019) Enhanced genetically encoded voltage indicators advance their applications in neuroscience. Current Opinion in Biomedical Engineering 12, 111–117.Google ScholarPubMed
Beck, C and Gong, Y (2019) A high-speed, bright, red fluorescent voltage sensor to detect neural activity. Scientific Reports 9(1), 15878.Google ScholarPubMed
Boens, N, Leen, V and Dehaen, W (2012) Fluorescent indicators based on BODIPY. Chemical Society Reviews 41(3), 1130–1172.CrossRefGoogle ScholarPubMed
Boggess, SC, Gandhi, SS, Benlian, BR and Miller, EW (2021) Vinyl-fluorene molecular wires for voltage imaging with enhanced sensitivity and reduced phototoxicity. Journal of the American Chemical Society 143(31), 11903–11907.CrossRefGoogle ScholarPubMed
Bonzanni, M, Payne, SL, Adelfio, M, Kaplan, DL, Levin, M and Oudin, MJ (2020) Defined extracellular ionic solutions to study and manipulate the cellular resting membrane potential. Biology open 9(1), bio048553.Google ScholarPubMed
Bortner, CD, Gómez-Angelats, M and Cidlowski, JA (2001) Plasma membrane depolarization without repolarization is an early molecular event in anti-Fas-induced apoptosis. Journal of Biological Chemistry 276(6), 4304–4314.Google Scholar
Bradley, J, Luo, R, Otis, TS and DA, DiGregorio (2009) Submillisecond optical reporting of membrane potential in situ using a neuronal tracer dye. Journal of Neuroscience 29(29), 9197–9209.Google ScholarPubMed
Braubach, O, Cohen, LB and Choi, Y (2015) Historical overview and general methods of membrane potential imaging. Membrane Potential Imaging in the Nervous System and Heart, 859, 3–26.CrossRefGoogle ScholarPubMed
Brown, AP and Greenberg, HZ (2016) Patch clamp. British Journal of Hospital Medicine 77(5), C74–C77.Google ScholarPubMed
Buttress, JA, Halte, M, Te Winkel, JD, Erhardt, M, Popp, PF and Strahl, H (2022) A guide for membrane potential measurements in Gram-negative bacteria using voltage-sensitive dyes. Microbiology 168(9), 001227.CrossRefGoogle ScholarPubMed
Caglar, M, Pandya, R, Xiao, J, Foster, SK, Divitini, G, Chen, RY, Greenham, NC, Franze, K, Rao, A and Keyser, UF (2019) All-optical detection of neuronal membrane depolarization in live cells using colloidal quantum dots. Nano letters 19(12), 8539–8549.Google ScholarPubMed
Cai, J, Niu, H, Zhao, P, Ji, Y, Ma, L, Wang, C, Bai, X and Wang, W (2013) Multicolored near-infrared electrochromic polyimides: Synthesis, electrochemical, and electrochromic properties. Dyes and Pigments 99(3), 1124–1131.Google Scholar
Campagnola, PJ and Loew, LM (2003) Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms. Nature biotechnology 21(11), 1356–1360.Google ScholarPubMed
Carter, M and Shieh, J (2015) Chapter 7 Visualizing Neural Function. Guide to Research Techniques in Neuroscience, 167–183.Google Scholar
Carvalho, PM, Makowski, M, Domingues, MM, Martins, IC and Santos, NC (2021) Lipid membrane-based therapeutics and diagnostics. Archives of Biochemistry and Biophysics 704, 108858.Google ScholarPubMed
Casa, S and Henary, M (2021) Synthesis and applications of selected fluorine-containing fluorophores. Molecules 26(4), 1160.Google Scholar
Catterall, WA (2011) Voltage-gated calcium channels. Cold Spring Harbor perspectives in biology 3(8), a003947.Google ScholarPubMed
Chatterjee, K, Pratiwi, FW, Wu, FCM, Chen, P and Chen, B-C (2018) Recent progress in light sheet microscopy for biological applications. Applied Spectroscopy 72(8), 1137–1169.Google ScholarPubMed
Chen, C-Y, Liu, Y-T, Lu, C-H, Lee, P-Y, Tsai, Y-C, Wu, J-S, Chen, P and Chen, B-C (2019a) The applications of lattice light-sheet microscopy for functional volumetric imaging of hippocampal neurons in a three-dimensional culture system. Micromachines 10(9), 599.Google Scholar
Chen, G, Zhang, Y, Peng, Z, Huang, D, Li, C and Wang, Q (2019b) Glutathione-capped quantum dots for plasma membrane labeling and membrane potential imaging. Nano Research 12, 1321–1326.CrossRefGoogle Scholar
Chen, J, Hu, C-L, Kong, F and Mao, J-G (2021) High-performance second-harmonic-generation (SHG) materials: new developments and new strategies. Accounts of chemical research 54(12), 2775–2783.Google ScholarPubMed
Chern, M, Kays, JC, Bhuckory, S and Dennis, AM (2019) Sensing with photoluminescent semiconductor quantum dots. Methods and applications in fluorescence 7(1), 012005.Google ScholarPubMed
Clarke, RJ (2010) Electric field sensitive dyes. Advanced fluorescence reporters in chemistry and biology I: Fundamentals and molecular design 331–344.Google Scholar
Coster, H (2003) The physics of cell membranes. Journal of Biological Physics 29, 363–399.Google ScholarPubMed
Crespo, GA, Cuartero, M and Bakker, E (2015) Thin layer ionophore-based membrane for multianalyte ion activity detection. Analytical chemistry 87(15), 7729–7737.CrossRefGoogle ScholarPubMed
Crocini, C, Coppini, R, Ferrantini, C, Yan, P, Loew, LM, Tesi, C, Cerbai, E, Poggesi, C, Pavone, FS and Sacconi, L (2014) Defects in T-tubular electrical activity underlie local alterations of calcium release in heart failure. Proceedings of the National Academy of Sciences 111(42), 15196–15201.CrossRefGoogle ScholarPubMed
Cuartero, M, Crespo, GA and Bakker, E (2016) Ionophore-based voltammetric ion activity sensing with thin layer membranes. Analytical chemistry 88(3), 1654–1660.CrossRefGoogle ScholarPubMed
de Lera Ruiz, M and Kraus, RL (2015) Voltage-gated sodium channels: structure, function, pharmacology, and clinical indications. Journal of medicinal chemistry 58(18), 7093–7118.CrossRefGoogle ScholarPubMed
Demarche, S, Sugihara, K, Zambelli, T, Tiefenauer, L and Vörös, J (2011) Techniques for recording reconstituted ion channels. Analyst 136(6), 1077–1089.CrossRefGoogle ScholarPubMed
Denac, H, Mevissen, M and Scholtysik, G (2000) Structure, function and pharmacology of voltage-gated sodium channels. Naunyn-Schmiedeberg’s archives of pharmacology 362, 453–479.CrossRefGoogle ScholarPubMed
Denk, W, Strickler, JH and Webb, WW (1990) Two-photon laser scanning fluorescence microscopy. Science 248(4951), 73–76.Google ScholarPubMed
Diaspro, A (2001) Confocal and two-photon microscopy: foundations, applications and advances.Google Scholar
Dorta, D, Plazaola, C, Carrasco, J, Alves-Rosa, MF, Coronado, LM, Correa, R, Zambrano, M, Gutiérrez-Medina, B, Sarmiento-Gómez, E and Spadafora, C (2024) Mechanical characterization of the erythrocyte membrane using a capacitor-based technique. Micromachines 15(5), 590.Google ScholarPubMed
Dyer, AL, Bulloch, RH, Zhou, Y, Kippelen, B, Reynolds, JR and Zhang, F (2014) A vertically integrated solar-powered electrochromic window for energy efficient buildings. Advanced Materials 26(28), 4895–4900.CrossRefGoogle ScholarPubMed
Efros, AL, Rosen, M, Kuno, M, Nirmal, M, Norris, DJ and Bawendi, M (1996) Band-edge exciton in quantum dots of semiconductors with a degenerate valence band: Dark and bright exciton states. Physical Review B 54(7), 4843.CrossRefGoogle ScholarPubMed
Efros, AL, Delehanty, JB, Huston, AL, Medintz, IL, Barbic, M and Harris, TD (2018) Evaluating the potential of using quantum dots for monitoring electrical signals in neurons. Nature nanotechnology 13(4), 278–288.Google ScholarPubMed
Egawa, T, Hanaoka, K, Koide, Y, Ujita, S, Takahashi, N, Ikegaya, Y, Matsuki, N, Terai, T, Ueno, T and Komatsu, T (2011) Development of a far-red to near-infrared fluorescence probe for calcium ion and its application to multicolor neuronal imaging. Journal of the American Chemical Society 133(36), 14157–14159.Google ScholarPubMed
Ehrenberg, B, Montana, V, Wei, M, Wuskell, J and Loew, L (1988) Membrane potential can be determined in individual cells from the nernstian distribution of cationic dyes. Biophysical Journal 53(5), 785–794.Google ScholarPubMed
Entcheva, E and Kay, MW (2021) Cardiac optogenetics: a decade of enlightenment. Nature Reviews Cardiology 18(5), 349–367.CrossRefGoogle ScholarPubMed
Ernst, OP, Lodowski, DT, Elstner, M, Hegemann, P, Brown, LS and Kandori, H (2014) Microbial and animal rhodopsins: structures, functions, and molecular mechanisms. Chemical reviews 114(1), 126–163.CrossRefGoogle ScholarPubMed
Fairless, R, Beck, A, Kravchenko, M, Williams, SK, Wissenbach, U, Diem, R and Cavalié, A (2013) Membrane potential measurements of isolated neurons using a voltage-sensitive dye. PloS one 8(3), e58260.CrossRefGoogle ScholarPubMed
Feiner, A-S and McEvoy, A (1994) The nernst equation. Journal of Chemical Education 71(6), 493.Google Scholar
Flytzanis, NC, Bedbrook, CN, Chiu, H, Engqvist, MK, Xiao, C, Chan, KY, Sternberg, PW, Arnold, FH and Gradinaru, V (2014) Archaerhodopsin variants with enhanced voltage-sensitive fluorescence in mammalian and Caenorhabditis elegans neurons. Nature communications 5(1), 4894.Google ScholarPubMed
Foley, J and Muschol, M (2008) Action spectra of electrochromic voltage sensitive dyes in an intact excitable tissue. Journal of Biomedical Optics 13(6), 064015.Google Scholar
Franke, JM (2019) Water-Soluble BODIPY Dyes for Membrane Potential Imaging. Berkeley: University of California.Google ScholarPubMed
Franke, JM, Raliski, BK, Boggess, SC, Natesan, DV, Koretsky, ET, Zhang, P, Kulkarni, RU, Deal, PE and Miller, EW (2019) BODIPY fluorophores for membrane potential imaging. Journal of the American Chemical Society 141(32), 12824–12831.CrossRefGoogle ScholarPubMed
Frey, W, White, J, Price, R, Blackmore, P, Joshi, R, Nuccitelli, R, Beebe, S, Schoenbach, K and Kolb, J (2006) Plasma membrane voltage changes during nanosecond pulsed electric field exposure. Biophysical journal 90(10), 3608–3615.Google ScholarPubMed
Fromherz, P, Hübener, G, Kuhn, B and Hinner, MJ (2008) ANNINE-6plus, a voltage-sensitive dye with good solubility, strong membrane binding and high sensitivity. European Biophysics Journal 37, 509–514.Google ScholarPubMed
Galisteo-González, F, Monasterio, BG, Gil, D, Valle, M and Goñi, FM (2020) Photoacoustic effect applied on model membranes and living cells: direct observation with multiphoton excitation microscopy and long-term viability analysis. Scientific Reports 10(1), 299.CrossRefGoogle ScholarPubMed
Garcia, MI, Chen, JJ and Boehning, D (2017) Genetically encoded calcium indicators for studying long-term calcium dynamics during apoptosis. Cell Calcium 61, 44–49.CrossRefGoogle ScholarPubMed
Gest, AM, Yaeger-Weiss, SK, Lazzari-Dean, JR, and Miller, EW (2021) VoltageFluor dyes and fluorescence lifetime imaging for optical measurement of membrane potential. In Methods in enzymology. Elsevier, 267–293.Google Scholar
Gong, Y, Li, JZ and Schnitzer, MJ (2013) Enhanced archaerhodopsin fluorescent protein voltage indicators. PloS one 8(6), e66959.CrossRefGoogle ScholarPubMed
Gong, Y, Wagner, MJ, Zhong Li, J and Schnitzer, MJ (2014) Imaging neural spiking in brain tissue using FRET-opsin protein voltage sensors. Nature communications 5(1), 3674.CrossRefGoogle ScholarPubMed
Gong, Y, Huang, C, Li, JZ, Grewe, BF, Zhang, Y, Eismann, S and Schnitzer, MJ (2015) High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor. Science 350(6266), 1361–1366.Google ScholarPubMed
Gonzalez, JE and Tsien, RY (1997) Improved indicators of cell membrane potential that use fluorescence resonance energy transfer. Chemistry & biology 4(4), 269–277.CrossRefGoogle ScholarPubMed
Grazon, C, Chern, M, Lally, P, Baer, R, Fan, A, Lecommandoux, S, Klapperich, C, Dennis, AM, Galagan, JE and Grinstaff, MW (2022) The quantum dot vs. organic dye conundrum for ratiometric FRET-based biosensors: which one would you chose? Chemical Science 13(22), 6715–6731.CrossRefGoogle ScholarPubMed
Greene, LE, Lincoln, R and Cosa, G (2019) Tuning photo-induced electron transfer efficiency of fluorogenic BODIPY‐α‐tocopherol analogues. Photochemistry and Photobiology 95(1), 192–201.CrossRefGoogle Scholar
Grimm, C, Sims, RR, Tanese, D, Mohamed Lafirdeen, AS, Chan, CY, Faini, G, Putti, E, Del Bene, F, Papagiakoumou, E and Emiliani, V (2024) Two-photon voltage imaging with rhodopsin-based sensors. bioRxiv, 2024.2005.2010.593541.CrossRefGoogle Scholar
Guharay, J, Chaudhuri, R, Chakrabarti, A and Sengupta, PK (1997) Excited state proton transfer fluorescence of 3-hydroxyflavone in model membranes. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 53(3), 457–462.CrossRefGoogle Scholar
Guo, L and Wong, MS (2014) Multiphoton excited fluorescent materials for frequency upconversion emission and fluorescent probes. Advanced materials 26(31), 5400–5428.CrossRefGoogle ScholarPubMed
Hahn, A, Reed, MB, Vraka, C, Godbersen, GM, Klug, S, Komorowski, A, Falb, P, Nics, L, Traub-Weidinger, T and Hacker, M (2024) High-temporal resolution functional PET/MRI reveals coupling between human metabolic and hemodynamic brain response. European Journal of Nuclear Medicine and Molecular Imaging 51(5), 1310–1322.Google ScholarPubMed
Haider, TA and Knöpfel, T (2020) Voltage-sensitive fluorescent proteins for optical electrophysiology . In Neural Interface Engineering: Linking the Physical World and the Nervous System, pp. 383–407.CrossRefGoogle Scholar
Hammond, C (2015) Ionic gradients, membrane potential and ionic currents. In Cellular and Molecular Neurophysiology, (4th ed., pp. 39–54). Elsevier.CrossRefGoogle Scholar
Han, Z, Jin, L, Platisa, J, Cohen, LB, Baker, BJ and Pieribone, VA (2013) Fluorescent protein voltage probes derived from ArcLight that respond to membrane voltage changes with fast kinetics. PloS one 8(11), e81295.CrossRefGoogle ScholarPubMed
Helmchen, F and Denk, W (2005) Deep tissue two-photon microscopy. Nature Methods 2(12), 932–940.CrossRefGoogle ScholarPubMed
Hill, CL and Stephens, GJ (2021) An introduction to patch clamp recording. Patch Clamp Electrophysiology: Methods and Protocols, 1–19.Google Scholar
Hillman, EM, Voleti, V, Li, W and Yu, H (2019) Light-sheet microscopy in neuroscience. Annual review of neuroscience 42(1), 295–313.CrossRefGoogle ScholarPubMed
Hochbaum, DR, Zhao, Y, Farhi, SL, Klapoetke, N, Werley, CA, Kapoor, V, Zou, P, Kralj, JM, Maclaurin, D and Smedemark-Margulies, N (2014) All-optical electrophysiology in mammalian neurons using engineered microbial rhodopsins. Nature Methods 11(8), 825–833.CrossRefGoogle ScholarPubMed
Hofmann, KP and Lamb, TD (2023) Rhodopsin, light-sensor of vision. Progress in Retinal and Eye Research 93, 101116.Google ScholarPubMed
Holcomb, MR, Woods, MC, Uzelac, I, Wikswo, JP, Gilligan, JM and Sidorov, VY (2009) The potential of dual camera systems for multimodal imaging of cardiac electrophysiology and metabolism. Experimental biology and medicine 234(11), 1355–1373.CrossRefGoogle ScholarPubMed
Hou, JH, Venkatachalam, V and Cohen, AE (2014) Temporal dynamics of microbial rhodopsin fluorescence reports absolute membrane voltage. Biophysical journal 106(3), 639–648.CrossRefGoogle ScholarPubMed
Hu, B, Hu, L-L, M-L, Chen and Wang, J-H (2013) A FRET ratiometric fluorescence sensing system for mercury detection and intracellular colorimetric imaging in live Hela cells. Biosensors and Bioelectronics 49, 499–505.Google ScholarPubMed
Jha, KK, Prabhakaran, A, Spantzel, L, Sia, RC, Pérez, I, RA, ArellanoReyes, Elmanova, A, Dasgupta, A, Eggeling, C and Börsch, M. (2023) A BODIPY‐based molecular rotor in giant unilamellar vesicles: A case study by polarization‐resolved time‐resolved emission and transient absorption spectroscopy. ChemPhotoChem 7(11), e202300091.Google Scholar
Jooken, S, de Coene, Y, Deschaume, O, Zámbó, D, Aubert, T, Hens, Z, Dorfs, D, Verbiest, T, Clays, K and Callewaert, G (2021) Enhanced electric field sensitivity of quantum dot/rod two-photon fluorescence and its relevance for cell transmembrane voltage imaging. Nanophotonics 10(9), 2407–2420.Google Scholar
Joshi, J, Rubart, M and Zhu, W (2020) Optogenetics: background, methodological advances and potential applications for cardiovascular research and medicine. Frontiers in bioengineering and biotechnology 7, 466.Google ScholarPubMed
Kamkaew, A, Lim, SH, Lee, HB, Kiew, LV, Chung, LY and Burgess, K (2013) BODIPY dyes in photodynamic therapy. Chemical Society Reviews 42(1), 77–88.CrossRefGoogle ScholarPubMed
Kandori, H (2015) Ion-pumping microbial rhodopsins. Frontiers in Molecular Biosciences 2, 52.Google ScholarPubMed
Kannan, M, Vasan, G and Pieribone, VA (2019) Optimizing strategies for developing genetically encoded voltage indicators. Frontiers in Cellular Neuroscience 13, 53.CrossRefGoogle ScholarPubMed
Kao, W, Davis, CE, Kim, Y and Beach, J (2001) Fluorescence emission spectral shift measurements of membrane potential in single cells. Biophysical journal 81(2), 1163–1170.Google ScholarPubMed
Kaushik, S, He, H and Dalbey, RE (2022) Bacterial signal peptides-navigating the journey of proteins. Frontiers in Physiology 13, 933153.Google ScholarPubMed
Kawanishi, S, Kojima, K, Shibukawa, A, Sakamoto, M and Sudo, Y (2023) Detection of membrane potential-dependent rhodopsin fluorescence using low-intensity light emitting diode for long-term imaging. ACS Omega 8(5), 4826–4834.Google ScholarPubMed
Khadria, A (2022) Tools to measure membrane potential of neurons. biomedical journal 45(5), 749–762.CrossRefGoogle ScholarPubMed
Khitrin, A, Khitrin, K and Model, M (2014) A model for membrane potential and intracellular ion distribution. Chemistry and Physics of Lipids 184, 76–81.Google Scholar
Kim, S-Y, Cho, Y-J, Son, H-J, Cho, DW and Kang, SO (2018) Photo-induced electron transfer in a BODIPY-Ortho-carborane dyad investigated by time-resolved transient absorption spectroscopy. The Journal of Physical Chemistry A 122(13), 3391–3397.Google Scholar
Klapperstück, T, Glanz, D, Klapperstück, M and Wohlrab, J (2009) Methodological aspects of measuring absolute values of membrane potential in human cells by flow cytometry. Cytometry Part A: The Journal of the International Society for Advancement of Cytometry 75(7), 593–608.Google Scholar
Klejchova, M, Silva-Alvim, FA, Blatt, MR and Alvim, JC (2021) Membrane voltage as a dynamic platform for spatiotemporal signaling, physiological, and developmental regulation. Plant Physiology 185(4), 1523–1541.Google ScholarPubMed
Knöpfel, T and Song, C (2019) Optical voltage imaging in neurons: moving from technology development to practical tool. Nature Reviews Neuroscience 20(12), 719–727.CrossRefGoogle ScholarPubMed
Kowacz, M and Pollack, GH (2020) Cells in new light: Ion concentration, voltage, and pressure gradients across a hydrogel membrane. Acs Omega 5(33), 21024–21031.Google ScholarPubMed
Kramer, RH, Miller, EW, Abdelfattah, A and Baker, B (2022) Fluorescent reporters for sensing membrane potential: Tools for bioelectricity. Bioelectricity 4(2), 108–116.Google ScholarPubMed
Krasne, S (1980) Interactions of voltage-sensing dyes with membranes. I. Steady-state permeability behaviors induced by cyanine dyes. Biophysical journal 30(3), 415–439.Google ScholarPubMed
Krasznai, Z, Márián, T, Balkay, L, Emri, M and Trón, L (1995) Flow cytometric determination of absolute membrane potential of cells. Journal of Photochemistry and Photobiology B: Biology 28(1), 93–99.CrossRefGoogle ScholarPubMed
Krasznai, Z, Márián, T, Izumi, H, Damjanovich, S, Balkay, L, Trón, L and Morisawa, M (2000) Membrane hyperpolarization removes inactivation of Ca2+ channels, leading to Ca2+ influx and subsequent initiation of sperm motility in the common carp. Proceedings of the National Academy of Sciences 97(5), 2052–2057.CrossRefGoogle ScholarPubMed
Kuang, Q, Purhonen, P and Hebert, H (2015) Structure of potassium channels. Cellular and molecular life sciences 72, 3677–3693.CrossRefGoogle ScholarPubMed
Kuhn, B and Fromherz, P (2003) Anellated hemicyanine dyes in a neuron membrane: molecular Stark effect and optical voltage recording. The Journal of Physical Chemistry B 107(31), 7903–7913.CrossRefGoogle Scholar
Kuo, Y, Li, J and Michalet, X (2018) Characterizing the quantum-confined stark effect in semiconductor quantum dots and nanorods for single-molecule electrophysiology. ACS Photonics, 5 (12), 4788–4800.CrossRefGoogle Scholar
Langton, MJ (2021) Engineering of stimuli-responsive lipid-bilayer membranes using supramolecular systems. Nature Reviews Chemistry 5(1), 46–61.CrossRefGoogle ScholarPubMed
Lazzari-Dean, JR, Gest, AM and Miller, EW (2021) Measuring absolute membrane potential across space and time. Annual review of biophysics 50(1), 447–468.CrossRefGoogle ScholarPubMed
Lee, JW (2020) Protonic conductor: Better understanding neural resting and action potential. Journal of Neurophysiology 124(4), 1029–1044.Google ScholarPubMed
Lee, S, Geiller, T, Jung, A, Nakajima, R, Y-K, Song and Baker, BJ (2017) Improving a genetically encoded voltage indicator by modifying the cytoplasmic charge composition. Scientific Reports 7(1), 8286.CrossRefGoogle ScholarPubMed
Lee, S, Kang, BE, Y-K, Song and Baker, BJ (2022) A trafficking motif alters GEVI activity implicating persistent protein interactions at the membrane. Biophysical Reports 2(2).Google ScholarPubMed
Lee, S, Piao, HH, Sepheri-Rad, M, Jung, A, Sung, U, Y-K, Song and Baker, BJ (2016) Imaging membrane potential with two types of genetically encoded fluorescent voltage sensors. JoVE (Journal of Visualized Experiments) (108), e53566.Google ScholarPubMed
Lee, SY, Jeon, SI, Jung, S, Chung, IJ and Ahn, C-H (2014) Targeted multimodal imaging modalities. Advanced drug delivery reviews 76, 60–78.CrossRefGoogle ScholarPubMed
Li, C, Li, Y, Wu, Q, Sun, T and Xie, Z (2021) Multifunctional BODIPY for effective inactivation of Gram-positive bacteria and promotion of wound healing. Biomaterials Science 9(22), 7648–7654.CrossRefGoogle ScholarPubMed
Lin, L and Wang, LV (2021) Photoacoustic imaging. In Optical Imaging in Human Disease and Biological Research. Springer, 147–175.CrossRefGoogle Scholar
Lin, MZ and Schnitzer, MJ (2016) Genetically encoded indicators of neuronal activity. Nature neuroscience 19(9), 1142–1153.Google ScholarPubMed
Liu, P and Miller, EW (2019) Electrophysiology, unplugged: imaging membrane potential with fluorescent indicators. Accounts of chemical research 53(1), 11–19.CrossRefGoogle ScholarPubMed
Liu, S, Ling, J, Chen, P, Cao, C, Peng, L, Zhang, Y, Ji, G, Guo, Y, Chen, PR and Zou, P (2023) Orange/far-red hybrid voltage indicators with reduced phototoxicity enable reliable long-term imaging in neurons and cardiomyocytes. Proceedings of the National Academy of Sciences 120(34), e2306950120.CrossRefGoogle ScholarPubMed
Loew, LM (2011) Design and use of organic voltage sensitive dyes. Membrane potential imaging in the nervous system: methods and applications, 13–23.Google Scholar
Lohr, C, Beiersdorfer, A, Fischer, T, Hirnet, D, Rotermund, N, Sauer, J, Schulz, K and Gee, CE (2021) Using genetically encoded calcium indicators to study astrocyte physiology: a field guide. Frontiers in Cellular Neuroscience 15, 690147.Google ScholarPubMed
Ludwig, A, Serna, P, Morgenstein, L, Yang, G, Bar-Elli, O, Ortiz, G, Miller, E, Oron, D, Grupi, A and Weiss, S (2020) Development of lipid-coated semiconductor nanosensors for recording of membrane potential in neurons. ACS Photonics 7(5), 1141–1152.CrossRefGoogle Scholar
Lulevich, V, Shih, Y-P, Lo, SH and Liu, G-y (2009) Cell tracing dyes significantly change single cell mechanics. The Journal of Physical Chemistry B 113(18), 6511–6519.CrossRefGoogle ScholarPubMed
Luo, F, Wei, Y, Wang, Z, Luo, M and Hu, J (2018) Genetically encoded neural activity indicators. Brain Science Advances 4(1), 1–15.Google Scholar
Lv, X, Li, J, Zhang, L, Ouyang, M, Tameev, A, Nekrasov, A, Kim, G and Zhang, C (2022) High-performance electrochromic supercapacitor based on quinacridone dye with good specific capacitance, fast switching time and robust stability. Chemical Engineering Journal 431, 133733.Google Scholar
Müllenbroich, MC, Kelly, A, Acker, C, Bub, G, Bruegmann, T, Di Bona, A, Entcheva, E, Ferrantini, C, Kohl, P and Lehnart, SE (2021) Novel optics-based approaches for cardiac electrophysiology: a review. Frontiers in Physiology 12, 769586.CrossRefGoogle ScholarPubMed
Madhusoodanan, J (2019) Genetic light bulbs illuminate the brain. Nature 574(7778), 437–439.Google ScholarPubMed
Mank, M and Griesbeck, O (2008) Genetically encoded calcium indicators. Chemical reviews 108(5), 1550–1564.CrossRefGoogle ScholarPubMed
Marchal, GA, Biasci, V, Yan, P, Palandri, C, Campione, M, Cerbai, E, Loew, LM and Sacconi, L (2023) Recent advances and current limitations of available technology to optically manipulate and observe cardiac electrophysiology. Pflügers Archiv-European Journal of Physiology 475(11), 1357–1366.Google ScholarPubMed
Martí-Bonmatí, L, Sopena, R, Bartumeus, P and Sopena, P (2010) Multimodality imaging techniques. Contrast media & molecular imaging 5(4), 180–189.Google ScholarPubMed
Mendes, C, Thirupathi, A, Zaccaron, RP, Corrêa, MEAB, Bittencourt, JV, Casagrande, LdR, de Lima, AC, de Oliveira, LL, de Andrade, TA and Gu, Y (2022) Microcurrent and gold nanoparticles combined with hyaluronic acid accelerates wound healing. Antioxidants 11(11), 2257.Google ScholarPubMed
Mendive-Tapia, L, Zhao, C, Akram, AR, Preciado, S, Albericio, F, Lee, M, Serrels, A, Kielland, N, Read, ND and Lavilla, R (2016) Spacer-free BODIPY fluorogens in antimicrobial peptides for direct imaging of fungal infection in human tissue. Nature Communications 7(1), 10940.CrossRefGoogle ScholarPubMed
Millard, AC, Jin, L, Wuskell, JP, Lewis, A and Loew, LM (2004) Sensitivity of second harmonic generation from styryl dyes to transmembrane potential. Biophysical journal 86(2), 1169–1176.CrossRefGoogle ScholarPubMed
Miller, EW (2016) Small molecule fluorescent voltage indicators for studying membrane potential. Current Opinion in Chemical Biology 33, 74–80.Google ScholarPubMed
Miller, EW, Lin, JY, Frady, EP, Steinbach, PA, Kristan, WB Jr and Tsien, RY (2012) Optically monitoring voltage in neurons by photo-induced electron transfer through molecular wires. Proceedings of the National Academy of Sciences 109(6), 2114–2119.Google ScholarPubMed
Miyawaki, A, Llopis, J, Heim, R, McCaffery, JM, Adams, JA, Ikura, M and Tsien, RY (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388(6645), 882–887.Google Scholar
Mizuguchi, T and Nuriya, M (2020) Applications of second harmonic generation (SHG)/sum-frequency generation (SFG) imaging for biophysical characterization of the plasma membrane. Biophysical Reviews 12(6), 1321–1329.Google ScholarPubMed
Model, M, Mahajana, A, Düsterwald, K and Dmitriev, A (2023) Nucleic Acids Regulate Intracellular Ions and Membrane Potential. Cell Physiol Biochem 13.Google Scholar
Mohamed, WA, Abd El-Gawad, H, Mekkey, S, Galal, H, Handal, H, Mousa, H and Labib, A (2021) Quantum dots synthetization and future prospect applications. Nanotechnology Reviews 10(1), 1926–1940.CrossRefGoogle Scholar
Mollinedo-Gajate, I, Song, C and Knöpfel, T (2021) Genetically encoded voltage indicators. Optogenetics: Light-Sensing Proteins and Their Applications in Neuroscience and Beyond, 209–224.Google Scholar
Momose-Sato, Y, Sato, K, Arai, Y, Yazawa, I, Mochida, H and Kamino, K (1999) Evaluation of voltage-sensitive dyes for long-term recording of neural activity in the hippocampus. The Journal of membrane biology 172, 145–157.Google ScholarPubMed
Monteleone, A, Schary, W, Wenzel, F, Langhals, H and Dietrich, DR (2021) Label-free identification and differentiation of different microplastics using phasor analysis of fluorescence lifetime imaging microscopy (FLIM)-generated data. Chemico-Biological Interactions 342, 109466.CrossRefGoogle Scholar
Moreaux, L, Pons, T, Dambrin, V, Blanchard-Desce, M and Mertz, J (2003) Electro-optic response of second-harmonic generation membrane potential sensors. Optics letters 28(8), 625–627.Google ScholarPubMed
Moreaux, L, Sandre, O, Blanchard-Desce, M and Mertz, J (2000) Membrane imaging by simultaneous second-harmonic generation and two-photon microscopy. Optics letters 25(5), 320–322.Google ScholarPubMed
Mutoh, H, Akemann, W and Knöpfel, T (2012) Genetically engineered fluorescent voltage reporters. ACS chemical neuroscience 3(8), 585–592.CrossRefGoogle ScholarPubMed
Nadeau, JL (2015) Initial photophysical characterization of the proteorhodopsin optical proton sensor (PROPS). Frontiers in Neuroscience 9, 315.Google ScholarPubMed
Nag, OK, Muroski, ME, Hastman, DA, Almeida, B, Medintz, IL, Huston, AL and Delehanty, JB (2020) Nanoparticle-mediated visualization and control of cellular membrane potential: Strategies, progress, and remaining issues. ACS Nano 14(3), 2659–2677.Google ScholarPubMed
Nag, OK, Stewart, MH, Deschamps, JR, Susumu, K, Oh, E, Tsytsarev, V, Tang, Q, Efros, AL, Vaxenburg, R and Black, BJ (2017) Quantum dot–peptide–fullerene bioconjugates for visualization of in vitro and in vivo cellular membrane potential. Acs Nano 11(6), 5598–5613.CrossRefGoogle ScholarPubMed
Nevian, T and Helmchen, F (2007) Calcium indicator loading of neurons using single-cell electroporation. Pflügers Archiv-European Journal of Physiology 454, 675–688.Google ScholarPubMed
Nguyen, PT, Deisl, C, Fine, M, Tippetts, TS, Uchikawa, E, Bai, X-c and Levine, B (2022) Structural basis for gating mechanism of the human sodium-potassium pump. Nature communications 13(1), 5293.Google ScholarPubMed
Nikolaev, DM, Mironov, VN, Shtyrov, AA, Kvashnin, ID, Mereshchenko, AS, Vasin, AV, Panov, MS and Ryazantsev, MN (2023) Fluorescence imaging of cell membrane potential: From relative changes to absolute values. International Journal of Molecular Sciences 24(3), 2435.CrossRefGoogle ScholarPubMed
Noori, H (2011) The impact of the glial spatial buffering on the k+ nernst potential. Cognitive neurodynamics 5, 285–291.Google ScholarPubMed
Novilla, MN (2018) Ionophores. In Veterinary Toxicology. Elsevier, 1073–1092.Google Scholar
Obaid, A, Loew, L, Wuskell, J and Salzberg, B (2004) Novel naphthylstyryl-pyridinium potentiometric dyes offer advantages for neural network analysis. Journal of neuroscience methods 134(2), 179–190.CrossRefGoogle ScholarPubMed
Oh, J, Lee, C and Kaang, B-K (2019) Imaging and analysis of genetically encoded calcium indicators linking neural circuits and behaviors. The Korean Journal of Physiology & Pharmacology 23(4), 237–249.Google ScholarPubMed
Palmer, LM (2019) Two-Photon Imaging of Dendritic Calcium Dynamics In Vivo. Multiphoton Microscopy, 279–295.CrossRefGoogle Scholar
Pantazis, P, Maloney, J, Wu, D and Fraser, SE (2010) Second harmonic generating (SHG) nanoprobes for in vivo imaging. Proceedings of the National Academy of Sciences 107(33), 14535–14540.CrossRefGoogle ScholarPubMed
Parodi, V, Jacchetti, E, Osellame, R, Cerullo, G, Polli, D and Raimondi, MT (2020) Nonlinear optical microscopy: From fundamentals to applications in live bioimaging. Frontiers in Bioengineering and Biotechnology 8, 585363.CrossRefGoogle ScholarPubMed
Pavlou, M, Babutzka, S and Michalakis, S (2022) A Bioengineered in vitro Model to Assess AAV-Based Gene Therapies for Cyclic GMP-Related Disorders. International Journal of Molecular Sciences 23(9), 4538.Google ScholarPubMed
Pei, D (2022) How do biomolecules cross the cell membrane? Accounts of chemical research 55(3), 309–318.Google ScholarPubMed
Peng, L, Xu, Y and Zou, P (2017) Genetically-encoded voltage indicators. Chinese Chemical Letters 28(10), 1925–1928.Google Scholar
Peterka, DS, Takahashi, H and Yuste, R (2011) Imaging voltage in neurons. Neuron 69(1), 9–21.CrossRefGoogle ScholarPubMed
Pethig, R (1986) Ion, electron, and proton transport in membranes: A review of the physical processes involved. Modern Bioelectrochemistry, 199–239.Google Scholar
Platisa, J and Pieribone, VA (2018) Genetically encoded fluorescent voltage indicators: are we there yet? Current opinion in neurobiology 50, 146–153.Google ScholarPubMed
Pons, T, Moreaux, L, Mongin, O, Blanchard-Desce, M and Mertz, J (2003) Mechanisms of membrane potential sensing with second-harmonic generation microscopy. Journal of Biomedical Optics 8(3), 428–431.CrossRefGoogle ScholarPubMed
Poola, PK, Afzal, MI, Yoo, Y, Kim, KH and Chung, E (2019) Light sheet microscopy for histopathology applications. Biomedical engineering letters 9, 279–291.Google ScholarPubMed
Pucihar, G, Kotnik, T and Miklavčič, D (2009) Measuring the induced membrane voltage with Di-8-ANEPPS. Journal of visualized experiments: JoVE (33).CrossRefGoogle ScholarPubMed
Rai, R, Bhandari, R, Kaleem, M, Shraogi, N, Patnaik, S, Mishra, H and Misra, A (2024) An imidazole-naphthalimide-based pH sensitive molecular probe for selective detection of picric acid and cell imaging. Industrial & Engineering Chemistry Research 63, 10077–10092.Google Scholar
Rao, B, Zhang, R, Li, L, Shao, J-Y and Wang, LV (2017) Photoacoustic imaging of voltage responses beyond the optical diffusion limit. Scientific Reports 7(1), 2560.Google ScholarPubMed
Rhee, JK, Leong, LM, Mukim, MSI, Kang, BE, Lee, S, Bilbao-Broch, L and Baker, BJ (2020) Biophysical parameters of GEVIs: considerations for imaging voltage. Biophysical journal 119(1), 1–8.CrossRefGoogle ScholarPubMed
Rong, G, Kim, EH, Poskanzer, KE and Clark, HA (2017) A method for estimating intracellular ion concentration using optical nanosensors and ratiometric imaging. Scientific Reports 7(1), 10819.Google ScholarPubMed
Roome, CJ and Kuhn, B (2019) Voltage imaging with ANNINE dyes and two-photon microscopy. Multiphoton Microscopy, 297–334.Google Scholar
Roux, B, Allen, T, Berneche, S and Im, W (2004) Theoretical and computational models of biological ion channels. Quarterly reviews of biophysics 37(1), 15–103.Google ScholarPubMed
Rowland, CE, Susumu, K, Stewart, MH, Oh, E, Mäkinen, AJ, O’Shaughnessy, TJ, Kushto, G, Wolak, MA, Erickson, JS and Efros, L. A (2015) Electric field modulation of semiconductor quantum dot photoluminescence: insights into the design of robust voltage-sensitive cellular imaging probes. Nano letters 15(10), 6848–6854.Google ScholarPubMed
Roy, D, Shapira, Z and Weiss, S (2022) Membrane potential sensing: Material design and method development for single particle optical electrophysiology. The Journal of Chemical Physics 156(8).Google ScholarPubMed
Sacconi, L, D’Amico, M, Vanzi, F, Biagiotti, T, Antolini, R, Olivotto, M and Pavone, FS (2005) Second-harmonic generation sensitivity to transmembrane potential in normal and tumor cells. Journal of Biomedical Optics 10(2), 024014–024014-024018.CrossRefGoogle ScholarPubMed
Sacconi, L, Dombeck, D and Webb, W (2006) Overcoming photodamage in second-harmonic generation microscopy: real-time optical recording of neuronal action potentials. Proceedings of the National Academy of Sciences 103(9), 3124–3129.Google ScholarPubMed
Sacconi, L, Ferrantini, C, Lotti, J, Coppini, R, Yan, P, Loew, LM, Tesi, C, Cerbai, E, Poggesi, C and Pavone, FS (2012) Action potential propagation in transverse-axial tubular system is impaired in heart failure. Proceedings of the National Academy of Sciences 109(15), 5815–5819.CrossRefGoogle ScholarPubMed
Sacconi, L, Silvestri, L, Rodríguez, EC, Armstrong, GA, Pavone, FS, Shrier, A and Bub, G (2022) KHz-rate volumetric voltage imaging of the whole Zebrafish heart. Biophysical Reports 2(1).Google ScholarPubMed
Sadhu, S and Patra, A (2013) A brief overview of some physical studies on the relaxation dynamics and förster resonance energy transfer of semiconductor quantum dots. ChemPhysChem 14(12), 2641–2653.CrossRefGoogle ScholarPubMed
Schaffer, P, Ahammer, H, Müller, W, Koidl, B and Windisch, H (1994) Di-4-ANEPPS causes photodynamic damage to isolated cardiomyocytes. Pflügers Archiv 426, 548–551.CrossRefGoogle ScholarPubMed
Scipioni, L, Rossetta, A, Tedeschi, G and Gratton, E (2021) Phasor S-FLIM: a new paradigm for fast and robust spectral fluorescence lifetime imaging. Nature methods 18(5), 542–550.Google ScholarPubMed
Semonin, OE, Luther, JM and Beard, MC (2012) Quantum dots for next-generation photovoltaics. Materials today 15(11), 508–515.Google Scholar
Shalileh, S, Khayamian, MA, Ghaderinia, M, Abadijoo, H, Hassanzadeh-Moghadam, H, Dalman, A, Simaee, H, Faramarzpour, M, Ghaznavi, P, Soltan Khamsi, P, Abbasvandi, F, Faranoush, M, Anbiaei, R, Eftekhari-Yazdi, P and Abdolahad, M (2021) Label-free mechanoelectrical investigation of single cancer cells by dielectrophoretic-induced stretch assay. Sensors and Actuators B: Chemical 346, 130409. https://doi.org/10.1016/j.snb.2021.130409.CrossRefGoogle Scholar
Shamirian, A, Ghai, A and Snee, PT (2015) QD-based FRET probes at a glance. Sensors 15(6), 13028–13051.CrossRefGoogle ScholarPubMed
Shapira, Z, Degani-Katzav, N, Yudovich, S, Grupi, A and Weiss, S (2021) Optical probing of local membrane potential with fluorescent polystyrene beads. Biophysical Reports 1(2).CrossRefGoogle ScholarPubMed
Shapiro, HM (2000) Membrane potential estimation by flow cytometry. Methods 21(3), 271–279.CrossRefGoogle ScholarPubMed
Sims, RR, Bendifallah, I, Grimm, C, Lafirdeen, ASM, Domínguez, S, Chan, CY, Lu, X, Forget, BC, St-Pierre, F and Papagiakoumou, E (2024) Scanless two-photon voltage imaging. Nature Communications 15(1), 5095.Google ScholarPubMed
So, PT, Dong, CY, Masters, BR and Berland, KM (2000) Two-photon excitation fluorescence microscopy. Annual review of biomedical engineering 2(1), 399–429.CrossRefGoogle ScholarPubMed
Strathmann, H (2004) Ion-exchange membrane separation processes. Elsevier.Google Scholar
Sudarshan, VP, Li, S, Jamadar, SD, Egan, GF, Awate, SP and Chen, Z (2020) Improved temporal resolution for mapping brain metabolism using functional PET and anatomical MRI knowledge. bioRxiv, 2020.2007.2008.192872.Google Scholar
Suhling, K, Hirvonen, LM, Levitt, JA, Chung, P-H, Tregidgo, C, Le Marois, A, Rusakov, DA, Zheng, K, Ameer-Beg, S and Poland, S (2015) Fluorescence lifetime imaging (FLIM): Basic concepts and some recent developments. Medical photonics 27, 3–40.Google Scholar
Suzuki, J, Kanemaru, K and Iino, M (2016) Genetically encoded fluorescent indicators for organellar calcium imaging. Biophysical journal 111(6), 1119–1131.Google ScholarPubMed
Theer, P, Denk, W, Sheves, M, Lewis, A and Detwiler, PB (2011) Second-harmonic generation imaging of membrane potential with retinal analogues. Biophysical journal 100(1), 232–242.CrossRefGoogle ScholarPubMed
Thestrup, T, Litzlbauer, J, Bartholomäus, I, Mues, M, Russo, L, Dana, H, Kovalchuk, Y, Liang, Y, Kalamakis, G and Laukat, Y (2014) Optimized ratiometric calcium sensors for functional in vivo imaging of neurons and T lymphocytes. Nature methods 11(2), 175–182.Google ScholarPubMed
Torralba, A, Palenciano, L, Reija, A, Rigla, JP, Peñas, J, Llerena, JJ, Contreras-Martínez, R, Benlliure, J, Vega, A and Aguado-Barrera, ME (2022) Experimental setup for irradiation of cell cultures at L2A2. Quantum Beam Science 6(1), 10.CrossRefGoogle Scholar
van Munster, EB and Gadella, TWJ (2005) Fluorescence lifetime imaging microscopy (FLIM). In Advances in Biochemical Engineering (Vol. 95, pp. 143–175). Springer.Google Scholar
Vidal-Iglesias, FJ, Solla-Gullón, J, Rodes, A, Herrero, E and Aldaz, A (2012) Understanding the Nernst equation and other electrochemical concepts: an easy experimental approach for students. Journal of Chemical Education 89(7), 936–939.Google Scholar
Waggoner, A (1979) Dye indicators of membrane potential. Annual Review of Biophysics and Bioengineering 8(1), 47–68.CrossRefGoogle ScholarPubMed
Wang, D, Zhu, Z, Xu, Z and Zhang, D (2022) Neuroimaging with light field microscopy: a mini review of imaging systems. The European Physical Journal Special Topics 231(4), 749–761.Google Scholar
Wang, H, Zhao, W, Liu, X, Wang, S and Wang, Y (2019a) BODIPY-based fluorescent surfactant for cell membrane imaging and photodynamic therapy. ACS Applied Bio Materials 3(1), 593–601.CrossRefGoogle ScholarPubMed
Wang, X, Bou, S, Klymchenko, AS, Anton, N and Collot, M (2021) Ultrabright green-emitting nanoemulsions based on natural lipids-BODIPY conjugates. Nanomaterials 11(3), 826.CrossRefGoogle ScholarPubMed
Wang, XF, Periasamy, A, Herman, B and Coleman, DM (1992) Fluorescence lifetime imaging microscopy (FLIM): instrumentation and applications. Critical Reviews in Analytical Chemistry 23(5), 369–395.Google Scholar
Wang, Y, Han, X, Cui, Z and Shi, D (2019b) Bioelectricity, Its Fundamentals, Characterization Methodology, and Applications in Nano-Bioprobing and Cancer Diagnosis. Advanced Biosystems 3(10), 1900101.Google Scholar
Wang, Z, Hu, M, Ai, X, Zhang, Z and Xing, B (2019c) Near-infrared manipulation of membrane ion channels via upconversion optogenetics. Advanced Biosystems 3(1), 1800233.Google ScholarPubMed
Wang, S, Song, H, Ong, WY, Han, MY and Huang, D (2009) Positively charged and pH self-buffering quantum dots for efficient cellular uptake by charge mediation and monitoring cell membrane permeability. Nanotechnology 20(42), 425102.Google ScholarPubMed
Ward, KR, Dickinson, EJ and Compton, RG (2010) Dynamic theory of membrane potentials. The Journal of Physical Chemistry B 114(33), 10763–10773.Google ScholarPubMed
Whitaker, M (2010) Genetically encoded probes for measurement of intracellular calcium. In Methods in Cell Biology. Elsevier, pp. 153–182.Google Scholar
Wilson, SA, Millard, A, Lewis, A and Loew, LM (2014) Monitoring membrane potential with second-harmonic generation. Cold Spring Harbor Protocols 2014(6), pdb. prot081786.CrossRefGoogle ScholarPubMed
Wlodarczyk, A, McMillan, PF and Greenfield, SA (2006) High pressure effects in anaesthesia and narcosis. Chemical Society Reviews 35(10), 890–898.Google ScholarPubMed
Wright, SH (2004) Generation of resting membrane potential. Advances in physiology education 28(4), 139–142.Google ScholarPubMed
Xu, Y, Deng, M, Zhang, S, Yang, J, Peng, L, Chu, J and Zou, P (2019) Imaging neuronal activity with fast and sensitive red-shifted electrochromic FRET indicators. ACS Chemical Neuroscience 10(12), 4768–4775.CrossRefGoogle ScholarPubMed
Xu, Y, Zou, P and Cohen, AE (2017) Voltage imaging with genetically encoded indicators. Current Opinion in Chemical Biology 39, 1–10.CrossRefGoogle ScholarPubMed
Yamada, A, Gaja, N, Ohya, S, Muraki, K, Narita, H, Ohwada, T and Imaizumi, Y (2001) Usefulness and limitation of DiBAC4 (3), a voltage-sensitive fluorescent dye, for the measurement of membrane potentials regulated by recombinant large conductance Ca2+−activated K+ channels in HEK293 cells. Japanese journal of pharmacology 86(3), 342–350.Google ScholarPubMed
Yan, P, Acker, CD, Biasci, V, Judge, G, Monroe, A, Sacconi, L and Loew, LM (2023) Near-infrared voltage-sensitive dyes based on chromene donor. Proceedings of the National Academy of Sciences 120(34), e2305093120.Google ScholarPubMed
Yan, P, Acker, CD, Zhou, W-L, Lee, P, Bollensdorff, C, Negrean, A, Lotti, J, Sacconi, L, Antic, SD and Kohl, P (2012) Palette of fluorinated voltage-sensitive hemicyanine dyes. Proceedings of the National Academy of Sciences 109(50), 20443–20448.CrossRefGoogle ScholarPubMed
Yang, HH and St-Pierre, F (2016) Genetically encoded voltage indicators: opportunities and challenges. Journal of Neuroscience 36(39), 9977–9989.CrossRefGoogle ScholarPubMed
Yang, Z, Li, L, Ling, J, Liu, T, Huang, X, Ying, Y, Zhao, Y, Zhao, Y, Lei, K and Chen, L (2020) Cyclooctatetraene-conjugated cyanine mitochondrial probes minimize phototoxicity in fluorescence and nanoscopic imaging. Chemical Science 11(32), 8506–8516.Google ScholarPubMed
Yao, J and Wang, LV (2011) Photoacoustic tomography: fundamentals, advances and prospects. Contrast media & molecular imaging 6(5), 332–345.CrossRefGoogle ScholarPubMed
Yong, K-T, Hu, R, Roy, I, Ding, H, Vathy, LA, Bergey, EJ, Mizuma, M, Maitra, A and Prasad, PN (2009) Tumor targeting and imaging in live animals with functionalized semiconductor quantum rods. ACS applied materials & interfaces 1(3), 710–719.CrossRefGoogle ScholarPubMed
Yosinski, J, Clune, J, Nguyen, A, Fuchs, T and Lipson, H (2015) Understanding neural networks through deep visualization. arXiv preprint arXiv:1506.06579. Google Scholar
Yu, Q, Wang, X and Nie, L (2021) Optical recording of brain functions based on voltage-sensitive dyes. Chinese Chemical Letters 32(6), 1879–1887.CrossRefGoogle Scholar
Zakany, F, Kovacs, T, Panyi, G and Varga, Z (2020) Direct and indirect cholesterol effects on membrane proteins with special focus on potassium channels. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids 1865(8), 158706.Google ScholarPubMed
Zhang, HK, Yan, P, Kang, J, Abou, DS, Le, HN, Jha, AK, Thorek, DL, Kang, JU, Rahmim, A and Wong, DF (2017) Listening to membrane potential: photoacoustic voltage-sensitive dye recording. Journal of Biomedical Optics 22(4), 045006.Google ScholarPubMed
Zhang, P-C, Keleshian, AM and Sachs, F (2001) Voltage-induced membrane movement. Nature 413(6854), 428–432.Google ScholarPubMed
Zhang, XM, Yokoyama, T and Sakamoto, M (2021) Imaging voltage with microbial rhodopsins. Frontiers in Molecular Biosciences 8, 738829.CrossRefGoogle ScholarPubMed
Zhou, Y, Liu, E, Muller, H and Cui, B (2021) Optical electrophysiology: toward the goal of label-free voltage imaging. Journal of the American Chemical Society 143(28), 10482–10499.CrossRefGoogle ScholarPubMed
Zifarelli, G and Pusch, M (2007) CLC chloride channels and transporters: a biophysical and physiological perspective. Reviews of physiology, biochemistry and pharmacology, 23–76.CrossRefGoogle ScholarPubMed
Zou, P, Zhao, Y, Douglass, AD, Hochbaum, DR, Brinks, D, Werley, CA, Harrison, DJ, Campbell, RE and Cohen, AE (2014a) Bright and fast multicoloured voltage reporters via electrochromic FRET. Nature Communications 5(1), 4625.CrossRefGoogle Scholar
Zou, P, Zhao, Y, Douglass, AD, Hochbaum, DR, Brinks, D, Werley, CA, Harrison, DJ, Campbell, RE and Cohen, AE (2014b) Bright and fast voltage reporters across the visible spectrum via electrochromic FRET (eFRET). Preprint, arXiv:1403.4636.Google Scholar