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Frontiers of Optoelectronics

ISSN 2095-2759

ISSN 2095-2767(Online)

CN 10-1029/TN

Postal Subscription Code 80-976

Front. Optoelectron.    2020, Vol. 13 Issue (4) : 318-326    https://doi.org/10.1007/s12200-020-1068-1
RESEARCH ARTICLE
Super-resolution imaging of the dynamic cleavage of intercellular tunneling nanotubes
Wanjun GONG, Wenhui PAN, Ying HE, Meina HUANG, Jianguo ZHANG, Zhenyu GU, Dan ZHANG, Zhigang YANG(), Junle QU
Key Laboratory of Optoelectronic Devices and Systems of Ministry of Education and Guangdong Province, College of Physics and Optoelectronic Engineering, Shenzhen University, Shenzhen 518060, China
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Abstract

As a new method of cell–cell communication, tunneling nanotubes (TNTs) play important roles in cell–cell signaling and mass exchanges. However, a lack of powerful tools to visualize dynamic TNTs with high temporal/spatial resolution restricts the exploration of their formation and cleavage, hindering the complete understanding of its mechanism. Herein, we present the first example of using stochastic optical reconstruction microscopy (STORM) to observe the tube-like structures of TNTs linking live cells with an easily prepared fluorescent dye. Because of this new imaging microscopy, the cleavage process of TNTs was observed with a high spatial resolution.

Keywords super-resolution      tunneling nanotubes (TNTs)      live cell     
Corresponding Author(s): Zhigang YANG   
Just Accepted Date: 18 September 2020   Online First Date: 29 October 2020    Issue Date: 31 December 2020
 Cite this article:   
Wanjun GONG,Wenhui PAN,Ying HE, et al. Super-resolution imaging of the dynamic cleavage of intercellular tunneling nanotubes[J]. Front. Optoelectron., 2020, 13(4): 318-326.
 URL:  
https://academic.hep.com.cn/foe/EN/10.1007/s12200-020-1068-1
https://academic.hep.com.cn/foe/EN/Y2020/V13/I4/318
Fig.1  Diagram of the proposed labeling method for probe 1 on TNTs
Fig.2  Photophysical properties of probe 1 were evaluated. (a) Excitation and emission spectra of probe 1 (black and red curves, respectively), with a laser excitation wavelength of 633 nm. (b) Duty cycle calculated for probe 1. (c) Single-molecule fluorescence time traces measured in the absence of bME and oxygen-scavenging system
Fig.3  Fluorescent imaging of the probe in HeLa cells. The co-localization experiment was conducted by co-incubating 1 (1 mmol/L) (a) with a commercially available dye, membrane tracker-Dioctadecylcarbocyanines (DIO) (1 mmol/L) (b). The merged image (c) and Pr coefficient (d) was obtained by overlapping (a) and (b); FITC is the abbreviation of fluoresceinthioisocyanate. (e) Cell viability experiment on HeLa cells when incubating with probe 1
Fig.4  STORM imaging of TNTs and their dynamic changes. (a) One snapshot (t = 0 s) from a 184-s movie (left) and a reconstructed STORM image from 180 frames recorded over 3 s. (b) and (c) Time-series STORM snapshots of intercellular filament dynamics. Each image was reconstructed from 180 frames recorded over 3 s. (d) Magnified images of the circle in the square in (b) obtained by wide-field and STORM imaging. (e) Fluorescence intensity profiles along the white lines in (d). The black line shows the signal in the STORM image, whereas the blue line shows the signal in the wide-field image. FWHM values of these profiles are 133.5±1.5 nm (super-resolution image) and 530.1±14.1 nm (wide-field image), respectively
  
  Fig. S1 Reversible and spontaneous fluorescence blinking over tens of seconds in the PBS buffer at different times. (a) 10 s. (b) 150 s. (c) 300 s. (d) 450 s. (e) 600 s. (f) 760 s. The bright spots are still observed under long-time illumination by a laser beam (656 nm)
  Fig. S2 Wide field imaging (a) of TNTs and STORM imaging of TNTs at different time. (b) 8 s. (c) 40 s. (d) 88 s. (e) 144 s. (f) 196 s
  Fig. S3 1H NMR spectrum for 1
  Fig. S4 13C NMR (300 MHz, CDCl3) spectra of 1
1 Q Sattentau. Avoiding the void: cell-to-cell spread of human viruses. Nature Reviews Microbiology, 2008, 6(11): 815–826
https://doi.org/10.1038/nrmicro1972 pmid: 18923409
2 N M Sherer, M J Lehmann, L F Jimenez-Soto, C Horensavitz, M Pypaert, W Mothes. Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nature Cell Biology, 2007, 9(3): 310–315
https://doi.org/10.1038/ncb1544 pmid: 17293854
3 A Rustom, R Saffrich, I Markovic, P Walther, H H Gerdes. Nanotubular highways for intercellular organelle transport. Science, 2004, 303(5660): 1007–1010
https://doi.org/10.1126/science.1093133 pmid: 14963329
4 X Wang, M L Veruki, N V Bukoreshtliev, E Hartveit, H H Gerdes. Animal cells connected by nanotubes can be electrically coupled through interposed gap-junction channels. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(40): 17194–17199
https://doi.org/10.1073/pnas.1006785107 pmid: 20855598
5 K Hase, S Kimura, H Takatsu, M Ohmae, S Kawano, H Kitamura, M Ito, H Watarai, C C Hazelett, C Yeaman, H Ohno. M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex. Nature Cell Biology, 2009, 11(12): 1427–1432
https://doi.org/10.1038/ncb1990 pmid: 19935652
6 D Zhu, K S Tan, X Zhang, A Y Sun, G Y Sun, J C Lee. Hydrogen peroxide alters membrane and cytoskeleton properties and increases intercellular connections in astrocytes. Journal of Cell Science, 2005, 118(16): 3695–3703
https://doi.org/10.1242/jcs.02507 pmid: 16046474
7 X Wang, N V Bukoreshtliev, H H Gerdes. Developing neurons form transient nanotubes facilitating electrical coupling and calcium signaling with distant astrocytes. PLoS One, 2012, 7(10): e47429
https://doi.org/10.1371/journal.pone.0047429 pmid: 23071805
8 B Önfelt, S Nedvetzki, R K P Benninger, M A Purbhoo, S Sowinski, A N Hume, M C Seabra, M A A Neil, P M W French, D M Davis. Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria. Journal of Immunology (Baltimore, Md.: 1950), 2006, 177(12): 8476–8483
9 A Cselenyák, E Pankotai, E M Horváth, L Kiss, Z Lacza. Mesenchymal stem cells rescue cardiomyoblasts from cell death in an in vitro ischemia model via direct cell-to-cell connections. BMC Cell Biology, 2010, 11(1): 29
https://doi.org/10.1186/1471-2121-11-29 pmid: 20406471
10 S Naphade, J Sharma, H P Gaide Chevronnay, M A Shook, B A Yeagy, C J Rocca, S N Ur, A J Lau, P J Courtoy, S Cherqui. Brief reports: lysosomal cross-correction by hematopoietic stem cell-derived macrophages via tunneling nanotubes. Stem Cells (Dayton, Ohio), 2015, 33(1): 301–309
https://doi.org/10.1002/stem.1835 pmid: 25186209
11 X Wang, H H Gerdes. Transfer of mitochondria via tunneling nanotubes rescues apoptotic PC12 cells. Cell Death and Differentiation, 2015, 22(7): 1181–1191
https://doi.org/10.1038/cdd.2014.211 pmid: 25571977
12 M Osswald, E Jung, F Sahm, G Solecki, V Venkataramani, J Blaes, S Weil, H Horstmann, B Wiestler, M Syed, L Huang, M Ratliff, K Karimian Jazi, F T Kurz, T Schmenger, D Lemke, M Gömmel, M Pauli, Y Liao, P Häring, S Pusch, V Herl, C Steinhäuser, D Krunic, M Jarahian, H Miletic, A S Berghoff, O Griesbeck, G Kalamakis, O Garaschuk, M Preusser, S Weiss, H Liu, S Heiland, M Platten, P E Huber, T Kuner, A von Deimling, W Wick, F Winkler. Brain tumour cells interconnect to a functional and resistant network. Nature, 2015, 528(7580): 93–98
https://doi.org/10.1038/nature16071 pmid: 26536111
13 A Chauveau, A Aucher, P Eissmann, E Vivier, D M Davis. Membrane nanotubes facilitate long-distance interactions between natural killer cells and target cells. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(12): 5545–5550
https://doi.org/10.1073/pnas.0910074107 pmid: 20212116
14 E Lou, S Fujisawa, A Morozov, A Barlas, Y Romin, Y Dogan, S Gholami, A L Moreira, K Manova-Todorova, M A Moore. Tunneling nanotubes provide a unique conduit for intercellular transfer of cellular contents in human malignant pleural mesothelioma. PLoS One, 2012, 7(3): e33093
https://doi.org/10.1371/journal.pone.0033093 pmid: 22427958
15 M W Austefjord, H H Gerdes, X Wang. Tunneling nanotubes: diversity in morphology and structure. Communicative & Integrative Biology, 2014, 7(1): e27934
https://doi.org/10.4161/cib.27934 pmid: 24778759
16 F Dubois, B Jean-Jacques, H Roberge, M Bénard, L Galas, D Schapman, N Elie, D Goux, M Keller, E Maille, E Bergot, G Zalcman, G Levallet. A role for RASSF1A in tunneling nanotube formation between cells through GEFH1/Rab11 pathway control. Cell Communication and Signaling, 2018, 16(1): 66
https://doi.org/10.1186/s12964-018-0276-4 pmid: 30305100
17 X Sun, Y Wang, J Zhang, J Tu, X J Wang, X D Su, L Wang, Y Zhang. Tunneling-nanotube direction determination in neurons and astrocytes. Cell Death & Disease, 2012, 3(12): e438
https://doi.org/10.1038/cddis.2012.177 pmid: 23222508
18 B L Tang. Unconventional secretion and intercellular transfer of mutant huntingtin. Cells, 2018, 7(6): 59
https://doi.org/10.3390/cells7060059 pmid: 29904030
19 Z Weng, B Zhang, I Tsilioni, T C Theoharides. Nanotube formation: a rapid form of “alarm signaling”? Clinical Therapeutics, 2016, 38(5): 1066–1072
https://doi.org/10.1016/j.clinthera.2016.02.030 pmid: 27085584
20 M Omsland, C Pise-Masison, D Fujikawa, V Galli, C Fenizia, R W Parks, B T Gjertsen, G Franchini, V Andresen. Inhibition of tunneling nanotube (TNT) formation and human T-cell leukemia virus type 1 (HTLV-1) transmission by cytarabine. Scientific Reports, 2018, 8(1): 11118
https://doi.org/10.1038/s41598-018-29391-w pmid: 30042514
21 E Delage, D C Cervantes, E Pénard, C Schmitt, S Syan, A Disanza, G Scita, C Zurzolo. Differential identity of filopodia and tunneling nanotubes revealed by the opposite functions of actin regulatory complexes. Scientific Reports, 2016, 6(1): 39632
https://doi.org/10.1038/srep39632 pmid: 28008977
22 M J Rust, M Bates, X Zhuang. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nature Methods, 2006, 3(10): 793–796
https://doi.org/10.1038/nmeth929 pmid: 16896339
23 M Bates, B Huang, G T Dempsey, X Zhuang. Multicolor super-resolution imaging with photo-switchable fluorescent probes. Science, 2007, 317(5845): 1749–1753
https://doi.org/10.1126/science.1146598 pmid: 17702910
24 B Huang, W Wang, M Bates, X Zhuang. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science, 2008, 319(5864): 810–813
https://doi.org/10.1126/science.1153529 pmid: 18174397
25 B Wang, J Fan, S Sun, L Wang, B Song, X Peng. 1-(Carbamoylmethyl)-3H-indolium squaraine dyes: synthesis, spectra, photo-stability and association with BSA. Dyes and Pigments, 2010, 85(1–2): 43–50
https://doi.org/10.1016/j.dyepig.2009.10.002
26 R M Roberts, M B Edwards. Acetoacetic ester-type cleavage by aniline1. Journal of the American Chemical Society, 1950, 72(12): 5537–5539
https://doi.org/10.1021/ja01168a047
27 D E Loeber, S W Russell, T P Toube, B C L Weedon, J Diment. Carotenoids and related compounds. Part XXVIII. Synthesis of zeaxanthin, -cryptoxanthin, and zeinoxanthin (-cryptoxanthin). Journal of the Chemical Society C: Organic, 1971, 404–408
https://doi.org/10.1039/j39710000404
28 J Min, C Vonesch, H Kirshner, L Carlini, N Olivier, S Holden, S Manley, J C Ye, M Unser. FALCON: fast and unbiased reconstruction of high-density super-resolution microscopy data. Scientific Reports, 2014, 4(1): 4577
https://doi.org/10.1038/srep04577 pmid: 24694686
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