Actin filaments play a significant role in multiple essential cellular processes, including cell motility, vesicle and organelle movement, cell signaling, and cellular mechanosensing mechanisms. However, an important cellular processes, mechanosensing, remains debatable. This is because intracellular proteins such as actin filaments, focal adhesion complexes, and cell-nuclear junctions are dynamic structures that fluctuate minutely, although their binding is closely related to the mechanosensing mechanism. We established an original quasi-super-resolution image analysis method and revealed the existence of 3 Hz fluctuations in actin filaments in living cells at approximately 0.2 to 0.5 μm. We speculated that cells sense mechanical stresses such as fluid shear stress through the network structure of actin filaments and their connections to the substrate and cell nucleus. This study analyzed the fluctuations in actin filaments in the network structure of living cells using our quasi-super-resolution image analysis method under static culture conditions. In particular, we focused on the correlations between each actin fluctuation in the network structure. Fluorescence images showed that actin networks were well developed in the NIH3T3 cells. The maximum amplitude of actin filament fluctuations near the central region of the cell was 0.99 μm. Correlation coefficients of actin filament fluctuations in the network remained unchanged between the central and peripheral regions, with a maximum value of 0.23. These results suggested that actin filaments fluctuated independently within the network structure. Moreover, the distance between two actin filaments changed over time at the connecting point of the three actin filaments. These results suggest that strain occurs at the actin filament connecting points even when cells are under static culture conditions and that more complex mechanical states arise upon mechanical stimulation.
Published in | International Journal of Biomedical Science and Engineering (Volume 11, Issue 3) |
DOI | 10.11648/j.ijbse.20231103.11 |
Page(s) | 33-43 |
Creative Commons |
This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited. |
Copyright |
Copyright © The Author(s), 2023. Published by Science Publishing Group |
Actin Filament, Fluctuation, Lifeact-GFP, Living Cell, Network Structure, Super-Resolution Technique
[1] | Priyamvada Chugh, Andrew G. Clark, Matthew B. Smith, Davide A. D. Cassani, Kai Dierkes, Anan Ragab, Philippe P. Roux, Guillaume Charras, Guillaume Salbreux & Ewa K. Paluch. (2017). Actin Cortex Architecture Regulates Cell Surface Tension. Nature Cell Biology (6). doi: 10.1038/ncb3525. |
[2] | Toshiro Anno, Naoya Sakamoto & Masaaki Sato. (2012). Role of Nesprin-1 in Nuclear Deformation in Cells under Static and Uniaxial Stretching Conditions. Biochemical and Biophysical Research Communications (1). doi: 10.1016/j.bbrc.2012.06.073. |
[3] | Pakorn Kanchanawong, Gleb Shtengel, Ana M. Pasapera, Ericka B. Ramko, Michael W. Davidson, Harald F. Hess & Clare M. Waterman. (2010). Nanoscale Architecture of Integrin-Based Cell Adhesions. Natures (7323). doi: 10.1038/nature09621. |
[4] | Laura M. Hoffman, Mark A. Smith, Christopher C. Jensen, Masaaki Yoshigi, Elizabeth Blankman, Katharine S. Ullman & Mary C. Beckerle. (2020). Mechanical Stress Triggers Nuclear Remodeling and the Formation of Transmembrane Actin Nuclear Lines with Associated Nuclear Pore Complexes. Molecular Biology of the Cell (16). doi: 10.1091/mbc.E19-01-0027. |
[5] | Jason A. Mellad, Derek T. Warren & Catherine M. Shanahan. (2010). Nesprins LINC the Nucleus and Cytoskeleton. Current Opinion in Cell Biology (1). doi: 10.1016/j.ceb.2010.11.006. |
[6] | Kazuaki Nagayama, Yuki Yahiro & Takeo Matsumoto. (2011). Stress Fibers Stabilize the Position of Intranuclear DNA through Mechanical Connection with the Nucleus in Vascular Smooth Muscle Cells. FEBS Letters (24). doi: 10.1016/j.febslet.2011.11.006. |
[7] | Francis J. Alenghat & David E. Golan. (2013). Membrane Protein Dynamics and Functional Implications in Mammalian Cells. Current Topics in Membranes. doi: 10.1016/B978-0-12-417027-8.00003-9. |
[8] | Carmine Di Rienzo, Vincenzo Piazza, Enrico Gratton, Fabio Beltram & Francesco Cardarelli. (2014). Probing Short-Range Protein Brownian Motion in the Cytoplasm of Living Cells. Nature Communications (5891). doi: 10.1038/ncomms6891. |
[9] | Tomoteru Oka, Yasuyuki Oguma & Noriyuki Kataoka. (2022). Real-Time analysis of F-actin Fluctuation in Living Cells with Quasi Super-Resolution Technique. Journal of Biomechanical Science and Engineering (3). doi: 10.1299/jbse.22-00081. |
[10] | Tai Kiuchi, Makio Higuchi, Akihiro Takamura, Masahiro Maruoka & Naoki Watanabe. (2015). Multitarget Super-Resolution Microscopy with High-density Labeling by Exchangeable Probes. Nature Methods (8). doi: 10.1038/nmeth.3466. |
[11] | Toshihiro Sera, Marie Terada & Susumu Kudo. (2020). Heterogeneous Reorganization of Actin Filaments in Living Endothelial Cells in Response to Shear Stress. Journal of Biorheology (1). doi: 10.17106/jbr.34.18. |
[12] | Hui Chen, Dilshad M. Choudhury & Susan W. Craig. (2006). Coincidence of Actin Filaments and Talin is Required to Activate Vinculin. Journal of Biological Chemistry (52). doi: 10.1074/jbc.M607324200. |
[13] | Shigenobu Yonemura, Yuko Wada, Toshiyuki Watanabe, Akira Watanabe, Akira Nagafuchi & Mai Shibata. (2010). Alpha-Catenin as a Tension Transducer Induces Adherens Junction Development. Nature Cell Biology (6). doi: 10.1038/ncb2055. |
[14] | Kandice Tanner, Aaron Boudreau, Mina J. Bissell & Sanjay Kumar. (2010). Dissecting Regional Variations in Stress Fiber Mechanics. In Living Cell with Laser Nanosurgery. Biophysical Journal (9). doi: 10.1016/j.bpj.2010.08.071. |
[15] | Brian P. Helmke, Robert D. Goldman & Peter F. Davies. (2000). Rapid Displacement of Vimentin Intermediate Filaments in Living Endothelial Cells Exposed to Flow. Circulation Research (7). doi: 10.1161/01.res.86.7.745. |
[16] | Ning Wang, James P. Butler & Donald E. Ingber. (1993). Mechanotransduction Across the Cell Surface and Through the Cytoskeleton. Science (5111). Doi: 10.1126/science.7684161. |
[17] | Yuika Ueda, Daiki Matsunaga & Shinji Deguchi. (2022). A Statistical Mechanics Model for Determining the Length Distribution of Actin Filaments under Cellular Tensional Homeostasis. Scientific Reports (1). doi: 10.1038/s41598-022-18833-1. |
[18] | Shinji Deguchi, Toshiro Ohashi & Masaaki Aato. (2006). Mechanical Properties of Stress Fiber in Adherent Vascular Cells Characterized by In Vitro Micromanipulation. Future Medical Engineering Based on Bionanotechnology. doi: org/10.1142/9781860948800_0007. |
[19] | David B. Wells & Aleksei Aksimentiev. (2010). Mechanical Properties of a Complete Microtubule Revealed Through Molecular Dynamics Simulation. Biophysical Journal (2). doi: 10.1016/j.bpj.2010.04.038. |
[20] | Gun S. Buntara. (2020). Computational Modeling of Tensegrity Structures. Springer. |
[21] | Arif Md Rashedul Kabir, Daisuke Inoue, Yoshimi Hamano, Hiroyuki Mayama, Kazuki Sada & Akira Kakugo. (2014). Biomolecular Motor Modulates Mechanical Property of Microtuble. Biomacromolecules (5). doi: 10.1021/bm5001789. |
APA Style
Tomoteru Oka, Kouki Furukawa, Yasuyuki Oguma, Buntara Sthenly Gan, Noriyuki Kataoka. (2023). Actin Filaments That Form Networks in Living Cells Fluctuate Rapidly and Independently of Each Other. International Journal of Biomedical Science and Engineering, 11(3), 33-43. https://doi.org/10.11648/j.ijbse.20231103.11
ACS Style
Tomoteru Oka; Kouki Furukawa; Yasuyuki Oguma; Buntara Sthenly Gan; Noriyuki Kataoka. Actin Filaments That Form Networks in Living Cells Fluctuate Rapidly and Independently of Each Other. Int. J. Biomed. Sci. Eng. 2023, 11(3), 33-43. doi: 10.11648/j.ijbse.20231103.11
AMA Style
Tomoteru Oka, Kouki Furukawa, Yasuyuki Oguma, Buntara Sthenly Gan, Noriyuki Kataoka. Actin Filaments That Form Networks in Living Cells Fluctuate Rapidly and Independently of Each Other. Int J Biomed Sci Eng. 2023;11(3):33-43. doi: 10.11648/j.ijbse.20231103.11
@article{10.11648/j.ijbse.20231103.11, author = {Tomoteru Oka and Kouki Furukawa and Yasuyuki Oguma and Buntara Sthenly Gan and Noriyuki Kataoka}, title = {Actin Filaments That Form Networks in Living Cells Fluctuate Rapidly and Independently of Each Other}, journal = {International Journal of Biomedical Science and Engineering}, volume = {11}, number = {3}, pages = {33-43}, doi = {10.11648/j.ijbse.20231103.11}, url = {https://doi.org/10.11648/j.ijbse.20231103.11}, eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.ijbse.20231103.11}, abstract = {Actin filaments play a significant role in multiple essential cellular processes, including cell motility, vesicle and organelle movement, cell signaling, and cellular mechanosensing mechanisms. However, an important cellular processes, mechanosensing, remains debatable. This is because intracellular proteins such as actin filaments, focal adhesion complexes, and cell-nuclear junctions are dynamic structures that fluctuate minutely, although their binding is closely related to the mechanosensing mechanism. We established an original quasi-super-resolution image analysis method and revealed the existence of 3 Hz fluctuations in actin filaments in living cells at approximately 0.2 to 0.5 μm. We speculated that cells sense mechanical stresses such as fluid shear stress through the network structure of actin filaments and their connections to the substrate and cell nucleus. This study analyzed the fluctuations in actin filaments in the network structure of living cells using our quasi-super-resolution image analysis method under static culture conditions. In particular, we focused on the correlations between each actin fluctuation in the network structure. Fluorescence images showed that actin networks were well developed in the NIH3T3 cells. The maximum amplitude of actin filament fluctuations near the central region of the cell was 0.99 μm. Correlation coefficients of actin filament fluctuations in the network remained unchanged between the central and peripheral regions, with a maximum value of 0.23. These results suggested that actin filaments fluctuated independently within the network structure. Moreover, the distance between two actin filaments changed over time at the connecting point of the three actin filaments. These results suggest that strain occurs at the actin filament connecting points even when cells are under static culture conditions and that more complex mechanical states arise upon mechanical stimulation.}, year = {2023} }
TY - JOUR T1 - Actin Filaments That Form Networks in Living Cells Fluctuate Rapidly and Independently of Each Other AU - Tomoteru Oka AU - Kouki Furukawa AU - Yasuyuki Oguma AU - Buntara Sthenly Gan AU - Noriyuki Kataoka Y1 - 2023/09/27 PY - 2023 N1 - https://doi.org/10.11648/j.ijbse.20231103.11 DO - 10.11648/j.ijbse.20231103.11 T2 - International Journal of Biomedical Science and Engineering JF - International Journal of Biomedical Science and Engineering JO - International Journal of Biomedical Science and Engineering SP - 33 EP - 43 PB - Science Publishing Group SN - 2376-7235 UR - https://doi.org/10.11648/j.ijbse.20231103.11 AB - Actin filaments play a significant role in multiple essential cellular processes, including cell motility, vesicle and organelle movement, cell signaling, and cellular mechanosensing mechanisms. However, an important cellular processes, mechanosensing, remains debatable. This is because intracellular proteins such as actin filaments, focal adhesion complexes, and cell-nuclear junctions are dynamic structures that fluctuate minutely, although their binding is closely related to the mechanosensing mechanism. We established an original quasi-super-resolution image analysis method and revealed the existence of 3 Hz fluctuations in actin filaments in living cells at approximately 0.2 to 0.5 μm. We speculated that cells sense mechanical stresses such as fluid shear stress through the network structure of actin filaments and their connections to the substrate and cell nucleus. This study analyzed the fluctuations in actin filaments in the network structure of living cells using our quasi-super-resolution image analysis method under static culture conditions. In particular, we focused on the correlations between each actin fluctuation in the network structure. Fluorescence images showed that actin networks were well developed in the NIH3T3 cells. The maximum amplitude of actin filament fluctuations near the central region of the cell was 0.99 μm. Correlation coefficients of actin filament fluctuations in the network remained unchanged between the central and peripheral regions, with a maximum value of 0.23. These results suggested that actin filaments fluctuated independently within the network structure. Moreover, the distance between two actin filaments changed over time at the connecting point of the three actin filaments. These results suggest that strain occurs at the actin filament connecting points even when cells are under static culture conditions and that more complex mechanical states arise upon mechanical stimulation. VL - 11 IS - 3 ER -