Seeing the Spikes: The Future of Targetable Synthetic Voltage Sensors
Language English Country United States Media print-electronic
Document type Journal Article, Review
Grant support
R01 DA007418
NIDA NIH HHS - United States
R01 MH122470
NIMH NIH HHS - United States
PubMed
39943826
PubMed Central
PMC11882369
DOI
10.1021/acschemneuro.4c00849
Knihovny.cz E-resources
- Keywords
- cell-selective targeting, fluorescent sensor, imaging probe, membrane potential, voltage-sensitive dye,
- MeSH
- Action Potentials * physiology MeSH
- Fluorescent Dyes * MeSH
- Humans MeSH
- Membrane Potentials physiology MeSH
- Brain physiology MeSH
- Neurons * physiology MeSH
- Voltage-Sensitive Dye Imaging * methods trends MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
- Names of Substances
- Fluorescent Dyes * MeSH
Measuring the transduction of electrical signals within neurons is a key capability in neuroscience. Fluorescent voltage sensitive dyes (VSDs) were early tools that complemented classical electrophysiology by enabling the optical recording of membrane potential changes from many cells simultaneously. Recent advances in the VSD field have led to bright and highly sensitive sensors that can be targeted to the desired cell populations in live brain tissue. Despite this progress, recently, protein-based genetically encoded voltage indicators (GEVIs) have become the go-to tools for targeted voltage imaging in complex environments. In this Perspective, we summarize progress in developing targetable VSDs, discuss areas where these synthetic sensors are or could become relevant, and outline hurdles that need to be overcome to promote the routine use of targetable VSDs in neuroscience research.
Department of Chemistry Columbia University New York New York 10027 United States
Department of Chemistry Faculty of Science Masaryk University Kamenice 5 625 00 Brno Czech Republic
Laboratory of Organic Chemistry ETH Zürich D CHAB Vladimir Prelog Weg 3 8093 Zürich Switzerland
See more in PubMed
Sakmann B.; Neher E. Patch Clamp Techniques for Studying Ionic Channels in Excitable Membranes. Annu. Rev. Physiol. 1984, 46, 455–472. 10.1146/annurev.ph.46.030184.002323. PubMed DOI
Grienberger C.; Konnerth A. Imaging calcium in neurons. Neuron 2012, 73 (5), 862–85. 10.1016/j.neuron.2012.02.011. PubMed DOI
Knöpfel T.; Song C. Optical voltage imaging in neurons: moving from technology development to practical tool. Nat. Rev. Neurosci. 2019, 20 (12), 719–727. 10.1038/s41583-019-0231-4. PubMed DOI
Braubach O.; Cohen L. B.; Choi Y.. Historical Overview and General Methods of Membrane Potential Imaging. In Advances in Experimental Medicine and Biology; Springer International Publishing: 2015; pp 3–26. PubMed
Loew L. M.Design and Use of Organic Voltage Sensitive Dyes. In Advances in Experimental Medicine and Biology; Springer International Publishing: 2015; pp 27–53. PubMed
Peterka D. S.; Takahashi H.; Yuste R. Imaging voltage in neurons. Neuron 2011, 69 (1), 9–21. 10.1016/j.neuron.2010.12.010. PubMed DOI PMC
Loew L. M. Design and characterization of electrochromic membrane probes. Journal of Biochemical and Biophysical Methods 1982, 6 (3), 243–260. 10.1016/0165-022X(82)90047-1. PubMed DOI
Yan P.; Acker C. D.; Biasci V.; Judge G.; Monroe A.; Sacconi L.; Loew L. M. Near-infrared voltage-sensitive dyes based on chromene donor. Proc. Natl. Acad. Sci. U. S. A. 2023, 120 (34), e2305093120.10.1073/pnas.2305093120. PubMed DOI PMC
Miller E. W.; Lin J. Y.; Frady E. P.; Steinbach P. A.; Kristan W. B.; Tsien R. Y. Optically monitoring voltage in neurons by photo-induced electron transfer through molecular wires. Proc. Natl. Acad. Sci. U. S. A. 2012, 109 (6), 2114–2119. 10.1073/pnas.1120694109. PubMed DOI PMC
Boggess S. C.; Gandhi S. S.; Benlian B. R.; Miller E. W. Vinyl-Fluorene Molecular Wires for Voltage Imaging with Enhanced Sensitivity and Reduced Phototoxicity. J. Am. Chem. Soc. 2021, 143 (31), 11903–11907. 10.1021/jacs.1c04543. PubMed DOI PMC
Gonzalez M. A.; Walker A. S.; Cao K. J.; Lazzari-Dean J. R.; Settineri N. S.; Kong E. J.; Kramer R. H.; Miller E. W. Voltage Imaging with a NIR-Absorbing Phosphine Oxide Rhodamine Voltage Reporter. J. Am. Chem. Soc. 2021, 143 (5), 2304–2314. 10.1021/jacs.0c11382. PubMed DOI PMC
Grenier V.; Martinez K. N.; Benlian B. R.; García-Almedina D. M.; Raliski B. K.; Boggess S. C.; Maza J. C.; Yang S. J.; Gest A. M. M.; Miller E. W. Molecular Prosthetics for Long-Term Functional Imaging with Fluorescent Reporters. ACS Cent. Sci. 2022, 8 (1), 118–121. 10.1021/acscentsci.1c01153. PubMed DOI PMC
Mccann J. T.; Benlian B. R.; Yaeger-Weiss S. K.; Knudson I. J.; He M.; Miller E. W. Flipping the Switch: Reverse-Demand Voltage-Sensitive Fluorophores. J. Am. Chem. Soc. 2022, 144 (29), 13050–13054. 10.1021/jacs.2c05385. PubMed DOI PMC
Kulkarni R. U.; Vandenberghe M.; Thunemann M.; James F.; Andreassen O. A.; Djurovic S.; Devor A.; Miller E. W. In Vivo Two-Photon Voltage Imaging with Sulfonated Rhodamine Dyes. ACS Cent. Sci. 2018, 4 (10), 1371–1378. 10.1021/acscentsci.8b00422. PubMed DOI PMC
Grinvald A.; Hildesheim R. VSDI: a new era in functional imaging of cortical dynamics. Nat. Rev. Neurosci. 2004, 5 (11), 874–885. 10.1038/nrn1536. PubMed DOI
Kuhn B.; Denk W.; Bruno R. M. In vivo two-photon voltage-sensitive dye imaging reveals top-down control of cortical layers 1 and 2 during wakefulness. Proc. Natl. Acad. Sci. U. S. A. 2008, 105 (21), 7588–7593. 10.1073/pnas.0802462105. PubMed DOI PMC
Kulkarni R. U.; Kramer D. J.; Pourmandi N.; Karbasi K.; Bateup H. S.; Miller E. W. Voltage-sensitive rhodol with enhanced two-photon brightness. Proc. Natl. Acad. Sci. U. S. A. 2017, 114 (11), 2813–2818. 10.1073/pnas.1610791114. PubMed DOI PMC
Wenner P.; Tsau Y.; Cohen L. B.; O’Donovan M. J.; Dan Y. Voltage-sensitive dye recording using retrogradely transported dye in the chicken spinal cord: staining and signal characteristics. J. Neurosci. Methods 1996, 70 (2), 111–20. 10.1016/S0165-0270(96)00108-2. PubMed DOI
Antic S.; Zecevic D. Optical signals from neurons with internally applied voltage-sensitive dyes. J. Neurosci. 1995, 15 (2), 1392–1405. 10.1523/JNEUROSCI.15-02-01392.1995. PubMed DOI PMC
Hinner M. J.; Hübener G.; Fromherz P. Enzyme-Induced Staining of Biomembranes with Voltage-Sensitive Fluorescent Dyes. J. Phys. Chem. B 2004, 108 (7), 2445–2453. 10.1021/jp036811h. PubMed DOI
Hinner M. J.; Hübener G.; Fromherz P. Genetic Targeting of Individual Cells with a Voltage-Sensitive Dye through Enzymatic Activation of Membrane Binding. ChemBioChem. 2006, 7 (3), 495–505. 10.1002/cbic.200500395. PubMed DOI
Ng D. N.; Fromherz P. Genetic Targeting of a Voltage-Sensitive Dye by Enzymatic Activation of Phosphonooxymethyl-ammonium Derivative. ACS Chem. Biol. 2011, 6 (5), 444–451. 10.1021/cb100312d. PubMed DOI
Liu P.; Grenier V.; Hong W.; Muller V. R.; Miller E. W. Fluorogenic Targeting of Voltage-Sensitive Dyes to Neurons. J. Am. Chem. Soc. 2017, 139 (48), 17334–17340. 10.1021/jacs.7b07047. PubMed DOI PMC
Ortiz G.; Liu P.; Naing S. H. H.; Muller V. R.; Miller E. W. Synthesis of Sulfonated Carbofluoresceins for Voltage Imaging. J. Am. Chem. Soc. 2019, 141 (16), 6631–6638. 10.1021/jacs.9b01261. PubMed DOI PMC
Jia H.-R.; Zhu Y.-X.; Duan Q.-Y.; Wu F.-G. Cell surface-localized imaging and sensing. Chem. Soc. Rev. 2021, 50 (10), 6240–6277. 10.1039/D1CS00067E. PubMed DOI
Aronoff M. R.; Hiebert P.; Hentzen N. B.; Werner S.; Wennemers H. Imaging and targeting LOX-mediated tissue remodeling with a reactive collagen peptide. Nat. Chem. Biol. 2021, 17 (8), 865–871. 10.1038/s41589-021-00830-6. PubMed DOI
Grenier V.; Walker A. S.; Miller E. W. A Small-Molecule Photoactivatable Optical Sensor of Transmembrane Potential. J. Am. Chem. Soc. 2015, 137 (34), 10894–10897. 10.1021/jacs.5b05538. PubMed DOI PMC
Sundukova M.; Prifti E.; Bucci A.; Kirillova K.; Serrao J.; Reymond L.; Umebayashi M.; Hovius R.; Riezman H.; Johnsson K.; Heppenstall P. A. A Chemogenetic Approach for the Optical Monitoring of Voltage in Neurons. Angew. Chem., Int. Ed. 2019, 58 (8), 2341–2344. 10.1002/anie.201812967. PubMed DOI PMC
Grenier V.; Daws B. R.; Liu P.; Miller E. W. Spying on Neuronal Membrane Potential with Genetically Targetable Voltage Indicators. J. Am. Chem. Soc. 2019, 141 (3), 1349–1358. 10.1021/jacs.8b11997. PubMed DOI PMC
Deal P. E.; Liu P.; Al-Abdullatif S. H.; Muller V. R.; Shamardani K.; Adesnik H.; Miller E. W. Covalently Tethered Rhodamine Voltage Reporters for High Speed Functional Imaging in Brain Tissue. J. Am. Chem. Soc. 2020, 142 (1), 614–622. 10.1021/jacs.9b12265. PubMed DOI PMC
Ortiz G.; Liu P.; Deal P. E.; Nensel A. K.; Martinez K. N.; Shamardani K.; Adesnik H.; Miller E. W. A silicon-rhodamine chemical-genetic hybrid for far red voltage imaging from defined neurons in brain slice. RSC Chem. Biol. 2021, 2 (6), 1594–1599. 10.1039/D1CB00156F. PubMed DOI PMC
Kirk M. J.; Benlian B. R.; Han Y.; Gold A.; Ravi A.; Deal P. E.; Molina R. S.; Drobizhev M.; Dickman D.; Scott K.; Miller E. W. Voltage Imaging in Drosophila Using a Hybrid Chemical-Genetic Rhodamine Voltage Reporter. Front Neurosci 2021, 15, 75402710.3389/fnins.2021.754027. PubMed DOI PMC
Fiala T.; Wang J.; Dunn M.; Šebej P.; Choi S. J.; Nwadibia E. C.; Fialova E.; Martinez D. M.; Cheetham C. E.; Fogle K. J.; Palladino M. J.; Freyberg Z.; Sulzer D.; Sames D. Chemical Targeting of Voltage Sensitive Dyes to Specific Cells and Molecules in the Brain. J. Am. Chem. Soc. 2020, 142 (20), 9285–9301. 10.1021/jacs.0c00861. PubMed DOI PMC
Fiala T.; Mosharov E. V.; Wang J.; Mendieta A. M.; Choi S. J.; Fialova E.; Hwu C.; Sulzer D.; Sames D. Chemical Targeting of Rhodol Voltage-Sensitive Dyes to Dopaminergic Neurons. ACS Chem. Neurosci. 2022, 13 (8), 1251–1262. 10.1021/acschemneuro.1c00862. PubMed DOI PMC
Perry S. W.; Norman J. P.; Barbieri J.; Brown E. B.; Gelbard H. A. Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. BioTechniques 2011, 50 (2), 98–115. 10.2144/000113610. PubMed DOI PMC
Lin B.; Liu Y.; Zhang X.; Fan L.; Shu Y.; Wang J. Membrane-Activated Fluorescent Probe for High-Fidelity Imaging of Mitochondrial Membrane Potential. ACS Sensors 2021, 6 (11), 4009–4018. 10.1021/acssensors.1c01390. PubMed DOI
Klier P. E. Z.; Martin J. G.; Miller E. W. Imaging Reversible Mitochondrial Membrane Potential Dynamics with a Masked Rhodamine Voltage Reporter. J. Am. Chem. Soc. 2021, 143 (11), 4095–4099. 10.1021/jacs.0c13110. PubMed DOI PMC
Hernández-Juárez C.; Flores-Cruz R.; Jiménez-Sánchez A. Fluorescent probe for early mitochondrial voltage dynamics. Chem. Commun. 2021, 57 (45), 5526–5529. 10.1039/D1CC01944A. PubMed DOI
Saminathan A.; Devany J.; Veetil A. T.; Suresh B.; Pillai K. S.; Schwake M.; Krishnan Y. A DNA-based voltmeter for organelles. Nat. Nanotechnol. 2021, 16 (1), 96–103. 10.1038/s41565-020-00784-1. PubMed DOI PMC
Klier P. E. Z.; Gest A. M. M.; Martin J. G.; Roo R.; Navarro M. X.; Lesiak L.; Deal P. E.; Dadina N.; Tyson J.; Schepartz A.; Miller E. W. Bioorthogonal, Fluorogenic Targeting of Voltage-Sensitive Fluorophores for Visualizing Membrane Potential Dynamics in Cellular Organelles. J. Am. Chem. Soc. 2022, 144 (27), 12138–12146. 10.1021/jacs.2c02664. PubMed DOI PMC
Adam Y. All-optical electrophysiology in behaving animals. J. Neurosci. Methods 2021, 353, 10910110.1016/j.jneumeth.2021.109101. PubMed DOI
Shcherbakova D. M. Near-infrared and far-red genetically encoded indicators of neuronal activity. J. Neurosci. Methods 2021, 362, 10931410.1016/j.jneumeth.2021.109314. PubMed DOI PMC
Dong C.; Zheng Y.; Long-Iyer K.; Wright E. C.; Li Y.; Tian L. Fluorescence Imaging of Neural Activity, Neurochemical Dynamics, and Drug-Specific Receptor Conformation with Genetically Encoded Sensors. Annu. Rev. Neurosci. 2022, 45 (1), 273–294. 10.1146/annurev-neuro-110520-031137. PubMed DOI PMC
Abdelfattah A. S.; Kawashima T.; Singh A.; Novak O.; Liu H.; Shuai Y.; Huang Y.-C.; Campagnola L.; Seeman S. C.; Yu J.; Zheng J.; Grimm J. B.; Patel R.; Friedrich J.; Mensh B. D.; Paninski L.; Macklin J. J.; Murphy G. J.; Podgorski K.; Lin B.-J.; Chen T.-W.; Turner G. C.; Liu Z.; Koyama M.; Svoboda K.; Ahrens M. B.; Lavis L. D.; Schreiter E. R. Bright and photostable chemigenetic indicators for extended in vivo voltage imaging. Science 2019, 365 (6454), 699–704. 10.1126/science.aav6416. PubMed DOI
Abdelfattah A. S.; Zheng J.; Singh A.; Huang Y. C.; Reep D.; Tsegaye G.; Tsang A.; Arthur B. J.; Rehorova M.; Olson C. V. L.; Shuai Y.; Zhang L.; Fu T. M.; Milkie D. E.; Moya M. V.; Weber T. D.; Lemire A. L.; Baker C. A.; Falco N.; Zheng Q.; Grimm J. B.; Yip M. C.; Walpita D.; Chase M.; Campagnola L.; Murphy G. J.; Wong A. M.; Forest C. R.; Mertz J.; Economo M. N.; Turner G. C.; Koyama M.; Lin B. J.; Betzig E.; Novak O.; Lavis L. D.; Svoboda K.; Korff W.; Chen T. W.; Schreiter E. R.; Hasseman J. P.; Kolb I. Sensitivity optimization of a rhodopsin-based fluorescent voltage indicator. Neuron 2023, 111 (10), 1547–1563.e9. 10.1016/j.neuron.2023.03.009. PubMed DOI PMC
Adam Y.; Kim J. J.; Lou S.; Zhao Y.; Xie M. E.; Brinks D.; Wu H.; Mostajo-Radji M. A.; Kheifets S.; Parot V.; Chettih S.; Williams K. J.; Gmeiner B.; Farhi S. L.; Madisen L.; Buchanan E. K.; Kinsella I.; Zhou D.; Paninski L.; Harvey C. D.; Zeng H.; Arlotta P.; Campbell R. E.; Cohen A. E. Voltage imaging and optogenetics reveal behaviour-dependent changes in hippocampal dynamics. Nature 2019, 569 (7756), 413–417. 10.1038/s41586-019-1166-7. PubMed DOI PMC
Zhu M. H.; Jang J.; Milosevic M. M.; Antic S. D. Population imaging discrepancies between a genetically-encoded calcium indicator (GECI) versus a genetically-encoded voltage indicator (GEVI). Sci. Rep. 2021, 11 (1), 5295.10.1038/s41598-021-84651-6. PubMed DOI PMC
Weber T. D.; Moya M. V.; Kılıç K.; Mertz J.; Economo M. N. High-speed multiplane confocal microscopy for voltage imaging in densely labeled neuronal populations. Nat. Neurosci. 2023, 26 (9), 1642–1650. 10.1038/s41593-023-01408-2. PubMed DOI PMC
Song C.; Matlashov M.; Shcherbakova D.; Antic S. D.; Verkhusha V.; Knöpfel T. Characterization of two near-infrared genetically encoded voltage indicators. Neurophotonics 2024, 11 (2), 02420110.1117/1.NPh.11.2.024201. PubMed DOI PMC
Liu S.; Lin C.; Xu Y.; Luo H.; Peng L.; Zeng X.; Zheng H.; Chen P. R.; Zou P. A far-red hybrid voltage indicator enabled by bioorthogonal engineering of rhodopsin on live neurons. Nat. Chem. 2021, 13 (5), 472–479. 10.1038/s41557-021-00641-1. PubMed DOI
Jang M. J.; Coughlin G. M.; Jackson C. R.; Chen X.; Chuapoco M. R.; Vendemiatti J. L.; Wang A. Z.; Gradinaru V. Spatial transcriptomics for profiling the tropism of viral vectors in tissues. Nat. Biotechnol. 2023, 41 (9), 1272–1286. 10.1038/s41587-022-01648-w. PubMed DOI PMC
Gubernator N. G.; Zhang H.; Staal R. G. W.; Mosharov E. V.; Pereira D. B.; Yue M.; Balsanek V.; Vadola P. A.; Mukherjee B.; Edwards R. H.; Sulzer D.; Sames D. Fluorescent False Neurotransmitters Visualize Dopamine Release from Individual Presynaptic Terminals. Science 2009, 324 (5933), 1441–1444. 10.1126/science.1172278. PubMed DOI PMC
Dunn M.; Henke A.; Clark S.; Kovalyova Y.; Kempadoo K. A.; Karpowicz R. J.; Kandel E. R.; Sulzer D.; Sames D. Designing a norepinephrine optical tracer for imaging individual noradrenergic synapses and their activity in vivo. Nat. Commun. 2018, 9 (1), 2838.10.1038/s41467-018-05075-x. PubMed DOI PMC
Tjahjono N.; Jin Y.; Hsu A.; Roukes M.; Tian L. Letting the little light of mind shine: Advances and future directions in neurochemical detection. Neurosci. Res. 2022, 179, 65–78. 10.1016/j.neures.2021.11.012. PubMed DOI PMC
Blaxter M.; Archibald J. M.; Childers A. K.; Coddington J. A.; Crandall K. A.; Di Palma F.; Durbin R.; Edwards S. V.; Graves J. A. M.; Hackett K. J.; Hall N.; Jarvis E. D.; Johnson R. N.; Karlsson E. K.; Kress W. J.; Kuraku S.; Lawniczak M. K. N.; Lindblad-Toh K.; Lopez J. V.; Moran N. A.; Robinson G. E.; Ryder O. A.; Shapiro B.; Soltis P. S.; Warnow T.; Zhang G.; Lewin H. A. Why sequence all eukaryotes?. Proc. Natl. Acad. Sci. U. S. A. 2022, 119 (4), e211563611810.1073/pnas.2115636118. PubMed DOI PMC
Gross D.; Loew L. M.; Webb W. W. Optical Imaging of Cell Membrane Potential Chenges Induced by Applied Electric Fields. Biophys. J. 1986, 50, 339–348. 10.1016/S0006-3495(86)83467-1. PubMed DOI PMC
Urrego D.; Sánchez A.; Tomczak A. P.; Pardo L. A. The electric fence to cell-cycle progression: Do local changes in membrane potential facilitate disassembly of the primary cilium?. BioEssays 2017, 39 (6), 160019010.1002/bies.201600190. PubMed DOI
Cornejo V. H.; Ofer N.; Yuste R. Voltage compartmentalization in dendritic spines in vivo. Science 2022, 375, 82–86. 10.1126/science.abg0501. PubMed DOI PMC
Wybo W. A. M.; Torben-Nielsen B.; Nevian T.; Gewaltig M. O. Electrical Compartmentalization in Neurons. Cell Reports 2019, 26 (7), 1759–1773.e7. 10.1016/j.celrep.2019.01.074. PubMed DOI
Rizzuto R.; Pozzan T. Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol. Rev. 2006, 86 (1), 369–408. 10.1152/physrev.00004.2005. PubMed DOI
Tour O.; Adams S. R.; Kerr R. A.; Meijer R. M.; Sejnowski T. J.; Tsien R. W.; Tsien R. Y. Calcium Green FlAsH as a genetically targeted small-molecule calcium indicator. Nat. Chem. Biol. 2007, 3 (7), 423–431. 10.1038/nchembio.2007.4. PubMed DOI PMC
Kim T. H.; Schnitzer M. J. Fluorescence imaging of large-scale neural ensemble dynamics. Cell 2022, 185 (1), 9–41. 10.1016/j.cell.2021.12.007. PubMed DOI PMC
Gest A. M. M.; Lazzari-Dean J. R.; Ortiz G.; Yaeger-Weiss S. K.; Boggess S. C.; Miller E. W. A red-emitting carborhodamine for monitoring and measuring membrane potential. Proc. Natl. Acad. Sci. U. S. A. 2024, 121 (14), e2315264121.10.1073/pnas.2315264121. PubMed DOI PMC
Roome C. J.; Kuhn B. Voltage imaging with ANNINE dyes and two-photon microscopy of Purkinje dendrites in awake mice. Neurosci. Res. 2020, 152, 15–24. 10.1016/j.neures.2019.11.007. PubMed DOI
Martin A.; Rivera-Fuentes P. A general strategy to develop fluorogenic polymethine dyes for bioimaging. Nat. Chem. 2024, 16 (1), 28–35. 10.1038/s41557-023-01367-y. PubMed DOI PMC
Treger J. S.; Priest M. F.; Iezzi R.; Bezanilla F. Real-Time Imaging of Electrical Signals with an Infrared FDA-Approved Dye. Biophys. J. 2014, 107 (6), L09–L12. 10.1016/j.bpj.2014.07.054. PubMed DOI PMC
Lee W.-L.; Westergaard X.; Hwu C.; Hwu J.; Fiala T.; Lacefield C.; Boltaev U.; Mendieta A. M.; Lin L.; Sonders M. S.; Brown K. R.; He K.; Asher W. B.; Javitch J. A.; Sulzer D.; Sames D. Molecular Design of SERTlight: A Fluorescent Serotonin Probe for Neuronal Labeling in the Brain. J. Am. Chem. Soc. 2024, 146 (14), 9564–9574. 10.1021/jacs.3c11617. PubMed DOI
Wang J.; Li B.; Qiu L.; Qiao X.; Yang H. Dendrimer-based drug delivery systems: history, challenges, and latest developments. J. Biol. Eng. 2022, 16 (1), 18.10.1186/s13036-022-00298-5. PubMed DOI PMC
Kazemipour A.; Novak O.; Flickinger D.; Marvin J. S.; Abdelfattah A. S.; King J.; Borden P. M.; Kim J. J.; Al-Abdullatif S. H.; Deal P. E.; Miller E. W.; Schreiter E. R.; Druckmann S.; Svoboda K.; Looger L. L.; Podgorski K. Kilohertz frame-rate two-photon tomography. Nat. Methods 2019, 16 (8), 778–786. 10.1038/s41592-019-0493-9. PubMed DOI PMC
Wu J.; Liang Y.; Chen S.; Hsu C.-L.; Chavarha M.; Evans S. W.; Shi D.; Lin M. Z.; Tsia K. K.; Ji N. Kilohertz two-photon fluorescence microscopy imaging of neural activity in vivo. Nat. Methods 2020, 17 (3), 287–290. 10.1038/s41592-020-0762-7. PubMed DOI PMC