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
Super-resolution imaging of the dynamic cleavage of intercellular tunneling nanotubes
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.
super-resolution / tunneling nanotubes (TNTs) / live cell
[1] |
Sattentau Q. Avoiding the void: cell-to-cell spread of human viruses. Nature Reviews Microbiology, 2008, 6(11): 815–826
CrossRef
Pubmed
Google scholar
|
[2] |
Sherer N M, Lehmann M J, Jimenez-Soto L F, Horensavitz C, Pypaert M, Mothes W. Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nature Cell Biology, 2007, 9(3): 310–315
CrossRef
Pubmed
Google scholar
|
[3] |
Rustom A, Saffrich R, Markovic I, Walther P, Gerdes H H. Nanotubular highways for intercellular organelle transport. Science, 2004, 303(5660): 1007–1010
CrossRef
Pubmed
Google scholar
|
[4] |
Wang X, Veruki M L, Bukoreshtliev N V, Hartveit E, Gerdes H H. 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
CrossRef
Pubmed
Google scholar
|
[5] |
Hase K, Kimura S, Takatsu H, Ohmae M, Kawano S, Kitamura H, Ito M, Watarai H, Hazelett C C, Yeaman C, Ohno H. M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex. Nature Cell Biology, 2009, 11(12): 1427–1432
CrossRef
Pubmed
Google scholar
|
[6] |
Zhu D, Tan K S, Zhang X, Sun A Y, Sun G Y, Lee J C. Hydrogen peroxide alters membrane and cytoskeleton properties and increases intercellular connections in astrocytes. Journal of Cell Science, 2005, 118(16): 3695–3703
CrossRef
Pubmed
Google scholar
|
[7] |
Wang X, Bukoreshtliev N V, Gerdes H H. Developing neurons form transient nanotubes facilitating electrical coupling and calcium signaling with distant astrocytes. PLoS One, 2012, 7(10): e47429
CrossRef
Pubmed
Google scholar
|
[8] |
Önfelt B, Nedvetzki S, Benninger R K P, Purbhoo M A, Sowinski S, Hume A N, Seabra M C, Neil M A A, French P M W, Davis D M. 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] |
Cselenyák A, Pankotai E, Horváth E M, Kiss L, Lacza Z. 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
CrossRef
Pubmed
Google scholar
|
[10] |
Naphade S, Sharma J, Gaide Chevronnay H P, Shook M A, Yeagy B A, Rocca C J, Ur S N, Lau A J, Courtoy P J, Cherqui S. Brief reports: lysosomal cross-correction by hematopoietic stem cell-derived macrophages via tunneling nanotubes. Stem Cells (Dayton, Ohio), 2015, 33(1): 301–309
CrossRef
Pubmed
Google scholar
|
[11] |
Wang X, Gerdes H H. Transfer of mitochondria via tunneling nanotubes rescues apoptotic PC12 cells. Cell Death and Differentiation, 2015, 22(7): 1181–1191
CrossRef
Pubmed
Google scholar
|
[12] |
Osswald M, Jung E, Sahm F, Solecki G, Venkataramani V, Blaes J, Weil S, Horstmann H, Wiestler B, Syed M, Huang L, Ratliff M, Karimian Jazi K, Kurz F T, Schmenger T, Lemke D, Gömmel M, Pauli M, Liao Y, Häring P, Pusch S, Herl V, Steinhäuser C, Krunic D, Jarahian M, Miletic H, Berghoff A S, Griesbeck O, Kalamakis G, Garaschuk O, Preusser M, Weiss S, Liu H, Heiland S, Platten M, Huber P E, Kuner T, von Deimling A, Wick W, Winkler F. Brain tumour cells interconnect to a functional and resistant network. Nature, 2015, 528(7580): 93–98
CrossRef
Pubmed
Google scholar
|
[13] |
Chauveau A, Aucher A, Eissmann P, Vivier E, Davis D M. 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
CrossRef
Pubmed
Google scholar
|
[14] |
Lou E, Fujisawa S, Morozov A, Barlas A, Romin Y, Dogan Y, Gholami S, Moreira A L, Manova-Todorova K, Moore M A. Tunneling nanotubes provide a unique conduit for intercellular transfer of cellular contents in human malignant pleural mesothelioma. PLoS One, 2012, 7(3): e33093
CrossRef
Pubmed
Google scholar
|
[15] |
Austefjord M W, Gerdes H H, Wang X. Tunneling nanotubes: diversity in morphology and structure. Communicative & Integrative Biology, 2014, 7(1): e27934
CrossRef
Pubmed
Google scholar
|
[16] |
Dubois F, Jean-Jacques B, Roberge H, Bénard M, Galas L, Schapman D, Elie N, Goux D, Keller M, Maille E, Bergot E, Zalcman G, Levallet G. A role for RASSF1A in tunneling nanotube formation between cells through GEFH1/Rab11 pathway control. Cell Communication and Signaling, 2018, 16(1): 66
CrossRef
Pubmed
Google scholar
|
[17] |
Sun X, Wang Y, Zhang J, Tu J, Wang X J, Su X D, Wang L, Zhang Y. Tunneling-nanotube direction determination in neurons and astrocytes. Cell Death & Disease, 2012, 3(12): e438
CrossRef
Pubmed
Google scholar
|
[18] |
Tang B L. Unconventional secretion and intercellular transfer of mutant huntingtin. Cells, 2018, 7(6): 59
CrossRef
Pubmed
Google scholar
|
[19] |
Weng Z, Zhang B, Tsilioni I, Theoharides T C. Nanotube formation: a rapid form of “alarm signaling”? Clinical Therapeutics, 2016, 38(5): 1066–1072
CrossRef
Pubmed
Google scholar
|
[20] |
Omsland M, Pise-Masison C, Fujikawa D, Galli V, Fenizia C, Parks R W, Gjertsen B T, Franchini G, Andresen V. 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
CrossRef
Pubmed
Google scholar
|
[21] |
Delage E, Cervantes D C, Pénard E, Schmitt C, Syan S, Disanza A, Scita G, Zurzolo C. Differential identity of filopodia and tunneling nanotubes revealed by the opposite functions of actin regulatory complexes. Scientific Reports, 2016, 6(1): 39632
CrossRef
Pubmed
Google scholar
|
[22] |
Rust M J, Bates M, Zhuang X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nature Methods, 2006, 3(10): 793–796
CrossRef
Pubmed
Google scholar
|
[23] |
Bates M, Huang B, Dempsey G T, Zhuang X. Multicolor super-resolution imaging with photo-switchable fluorescent probes. Science, 2007, 317(5845): 1749–1753
CrossRef
Pubmed
Google scholar
|
[24] |
Huang B, Wang W, Bates M, Zhuang X. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science, 2008, 319(5864): 810–813
CrossRef
Pubmed
Google scholar
|
[25] |
Wang B, Fan J, Sun S, Wang L, Song B, Peng X. 1-(Carbamoylmethyl)-3H-indolium squaraine dyes: synthesis, spectra, photo-stability and association with BSA. Dyes and Pigments, 2010, 85(1–2): 43–50
CrossRef
Google scholar
|
[26] |
Roberts R M, Edwards M B. Acetoacetic ester-type cleavage by aniline1. Journal of the American Chemical Society, 1950, 72(12): 5537–5539
CrossRef
Google scholar
|
[27] |
Loeber D E, Russell S W, Toube T P, Weedon B C L, Diment J. Carotenoids and related compounds. Part XXVIII. Synthesis of zeaxanthin, -cryptoxanthin, and zeinoxanthin (-cryptoxanthin). Journal of the Chemical Society C: Organic, 1971, 404–408
CrossRef
Google scholar
|
[28] |
Min J, Vonesch C, Kirshner H, Carlini L, Olivier N, Holden S, Manley S, Ye J C, Unser M. FALCON: fast and unbiased reconstruction of high-density super-resolution microscopy data. Scientific Reports, 2014, 4(1): 4577
CrossRef
Pubmed
Google scholar
|
/
〈 | 〉 |