Modern Methods of Fluorescence Nanoscopy in Biology

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Abstract

Optical microscopy has undergone significant changes in recent decades due to the breaking of the diffraction limit of optical resolution and the development of high-resolution imaging techniques, which are collectively known as fluorescence nanoscopy. These techniques allow researchers to observe biological structures and processes at a nanoscale level of detail, revealing previously hidden features and aiding in answering fundamental biological questions. Among the advanced methods of fluorescent nanoscopy are: STED (Stimulated Emission Depletion Microscopy), STORM (STochastic Optical Reconstruction Microscopy), PALM (Photo-activated Localization Microscopy), TIRF (Total Internal Reflection Fluorescence), SIM (Structured Illumination Microscopy), MINFLUX (Minimal Photon Fluxes), PAINT (Points Accumulation for Imaging in Nanoscale Topography) и RESOLFT (REversible Saturable Optical Fluorescence Transitions) and others. In addition, most of these methods make it possible to obtain volumetric (3D) images of the objects under study. In this review, we will look at the principles of these methods, their advantages and disadvantages, and their application in biological researches.

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About the authors

D. O. Solovyeva

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry

Author for correspondence.
Email: d.solovieva@mail.ru
Russian Federation, ul. Miklukho-Maklaya 16/10, Moscow, 117997

A. V. Altunina

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry; Moscow Institute of Physics and Technology (National Research University)

Email: d.solovieva@mail.ru
Russian Federation, ul. Miklukho-Maklaya 16/10, Moscow, 117997; Institutskiy per. 9, Dolgoprudny, 141701

M. V. Tretyak

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry

Email: d.solovieva@mail.ru
Russian Federation, ul. Miklukho-Maklaya 16/10, Moscow, 117997

K. E. Mochalov

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry

Email: d.solovieva@mail.ru
Russian Federation, ul. Miklukho-Maklaya 16/10, Moscow, 117997

V. A. Oleinikov

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry; National Research Nuclear University “MEPhI”

Email: d.solovieva@mail.ru
Russian Federation, ul. Miklukho-Maklaya 16/10, Moscow, 117997; Kashirskoye sh. 31, Moscow, 115409

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Supplementary files

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2. Fig. 1. Schematic diagram showing the resolution of a light optical microscope.

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3. Fig. 2. Classification of super-resolution microscopy methods. (a), (b) – Deterministic methods based on information about the spatial distribution: (a) – embedded in the illumination pattern (sequential illumination of the sample by a standing wave): SIM (Structured Illumination Microscopy), SMI (Spatially Modulated Illumination Microscopy), SSIM (Saturated Structured Illumination Microscopy); (b) – about the size of the light-emitting region (the response of the fluorophore to light excitation that stimulates emission): RESOLFT (REversible Saturable Optical Fluorescence Transitions), STED (Stimulated Emission Depletion Microscopy), SPEM (Scanning PhotoElectron Microscope), GSD (Ground State Depletion Microscopy), TIRF (Total Internal Reflection Fluorescence); (c) – stochastic methods based on the ability to localize single molecules with virtually any accuracy, which is determined by the number of registered photons: PAINT (Points Accumulation for Imaging in Nanoscale Topography), DNA-PAINT (DNA Points Accumulation for Imaging in Nanoscale Topography), STORM (STochastic Optical Reconstruction Microscopy), dSTORM (Direct Stochastic Optical Reconstruction Microscopy), PALM (Photo-activated Localization Microscopy), fPALM (DNA structure fluctuation-assisted BALM), BALM (Binding-Activated Localization Microscopy), MINFLUX (Minimal Photon Fluxes), SOFI (Super-resolution Optical Fluctuation Imaging).

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4. Fig. 3. 3D-STED imaging of fixed HeLa cells with fluorescently labeled membranes (green) and DNA (red), achieving near isotropic resolution, scale bar 5 μm [24].

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5. Fig. 4. STORM imaging sequence using a hypothetical hexameric object labeled with red fluorophores that can be switched between fluorescent and dark states using red and green lasers. All fluorophores are first switched to the dark state by a red laser pulse. In each imaging cycle, a green laser pulse is used to turn on only a subset of the fluorophores, forming an optically resolved set of active fluorophores. These molecules then emit fluorescence under red illumination until they are switched off, allowing their positions to be determined with high precision (white crosses). The overall image is then reconstructed based on the fluorophore positions obtained from multiple imaging cycles [36].

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6. Fig. 5. (a) Unoptimized STORM image of a horizontal cell labeled with calbindin. Putative synapses are unclear, with little defining morphology or continuous structure (unoptimized inset); (b) under optimized RAIN-STORM conditions, both the cells’ horizontal synapses and their connecting structures are labeled and juxtaposed (optimized inset), revealing clear structural detail throughout the neuronal arbor. Images are representative of n = 3 animals. STORM images are color-coded by depth (purple = 0 μm to yellow = 10 μm). Scale bars are 10 and 1 μm [41].

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7. Fig. 6. Effects of inhibition of Rho/ROCK-myosin IIA signaling on nocodazole-induced podosome cluster disassembly. Representative two-color STORM results of actin and myosin IIA in individual macrophages cultured for 16 h and then treated with Noc (10 μM), Noc (10 μM) + Y27632 (20 μM), and Noc (10 μM) + Bleb (20 μM) for 2 h. Shown are individual images of actin (purple) and myosin IIA (green) as well as an overlay image, respectively.

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8. Fig. 7. MINFLUX nanoscopy of U-2 OS cells expressing Nup96, a nuclear pore complex (NPC) protein, labeled with the organic fluorophore Alexa Fluor 647 (top). Magnified sections (bottom) show individual nuclear pores, where each dot highlights groups of localizations representing individual proteins via their fluorescent labels. Scale bars: 500 nm (top), 50 nm (insets) [64].

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9. Fig. 8. Capabilities of multicolor high-speed SIM. Field of view 33 × 33 μm, microtubules are shown in red, mitochondria in green. Scale bar 5 μm [85].

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10. Fig. 9. 3D-SIM and enlarged 2D/3D image of living HeLa cells incubated with 25 nM h-RBD-SiR for 10 h. Scale bar 2 μm [92].

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11. Fig. 10. Localization of L-selectin and CD44 on the 3D surface topography of T cells. (a) 3D reconstruction of the resting membrane surface of human T cells using MA-TIRFM; (b) localization map of L-selectin molecules (orange dots) superimposed on the 3D surface reconstruction map from panel (a). Scale bar 0.5 μm [105].

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