Skip to main content
SpringerLink
Log in

Membrane Dynamics Induced by a Phosphatidylinositol 3,4,5-Trisphosphate Optogenetic Tool

  • Published:
Analytical Sciences Aims and scope Submit manuscript

Abstract

Membrane dynamic structures such as filopodia, lamellipodia, and ruffles have important cellular functions in phagocytosis and cell motility, and in pathological states, such as cancer metastasis. Phosphatidylinositol 3,4,5-trisphosphate (PIP3) is a crucial lipid that regulates PIP3 dynamics. Investigations of how PIP3 is involved in these functions have mainly relied on pharmacological interventions, and therefore have not generated detailed spatiotemporal information concerning membrane dynamics upon PIP3 production. In the present study, we applied an optogenetic approach using the CRY2- CIBN system. Using this system, we revealed that local PIP3 generation induced directional cell motility and membrane ruffles in COS7 cells. Furthermore, combined with structured illumination microscopy (SIM), membrane dynamics were investigated with high spatial resolution. We observed PIP3-induced apical ruffles and unique actin fiber behavior in that a single actin fiber protruded from the plasma membrane was taken up into the plasma membrane without depolymerization. This system has the potential to investigate other high-level cell motility and dynamic behaviors, such as cancer cell invasion and wound healing with high spatiotemporal resolution, and could provide new insights of biological sciences for membrane dynamics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. E. S. Chhabra and H. N. Higgs, Nat. Cell Biol., 2007, 9, 1110.

    Article  CAS  PubMed  Google Scholar 

  2. S. J. Heasman and A. J. Ridley, Nat. Rev. Mol. Cell Biol., 2008, 9, 690.

    Article  CAS  PubMed  Google Scholar 

  3. R. H. Insall and O. D. Weiner, Dev. Cell, 2001, 1, 743.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. T. Oikawa, H. Yamaguchi, T. Itoh, M. Kato, T. Ijuin, D. Yamazaki, S. Suetsugu, and T. Takenawa, Nat. Cell Biol., 2004, 6, 420.

    Article  CAS  PubMed  Google Scholar 

  5. M. Shinohara, Y. Terada, A. Iwamatsu, A. Shinohara, N. Mochizuki, M. Higuchi, Y. Gotoh, S. Ihara, S. Nagata, H. Itoh, Y. Fukui, and R. Jessberger, Nature, 2002, 416, 759.

    Article  CAS  PubMed  Google Scholar 

  6. Y. Ueda, Mol. Neurobiol., 2014, 50, 821.

    Article  CAS  PubMed  Google Scholar 

  7. Y. Ueda and Y. Hayashi, J. Neurosci., 2013, 33, 11040.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. K. L. Arendt, M. Royo, M. Fernandez-Monreal, S. Knafo, C. N. Petrok, J. R. Martens, and J. A. Esteban, Nat. Neurosci., 2010, 13, 36.

    Article  CAS  PubMed  Google Scholar 

  9. H. Ogiso and R. Taguchi, Anal. Chem., 2008, 80, 9226.

    Article  CAS  PubMed  Google Scholar 

  10. H. H. Bui, P. E. Sanders, D. Bodenmiller, M. S. Kuo, G. P. Donoho, and A. S. Fischl, Anal. Biochem., 2018, 547, 66.

    Article  CAS  PubMed  Google Scholar 

  11. A. C. Newton, J. Lipid Res., 2009, 50(Suppl), S266.

    Article  PubMed  PubMed Central  Google Scholar 

  12. J. Han, K. Luby-Phelps, B. Das, X. Shu, Y. Xia, R. D. Mosteller, U. M. Krishna, J. R. Falck, M. A. White, and D. Broek, Science, 1998, 279, 558.

    Article  CAS  PubMed  Google Scholar 

  13. M. Innocenti, E. Frittoli, I. Ponzanelli, J. R. Falck, S. M. Brachmann, P. P. Di Fiore, and G. Scita, J. Cell Biol., 2003, 160, 17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. T. Kakumoto and T. Nakata, PLoS One, 2013, 8, e70861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. M. Sato, Y. Ueda, T. Takagi, and Y. Umezawa, Nat. Cell Biol., 2003, 5, 1016.

    Article  CAS  PubMed  Google Scholar 

  16. J. Jaworski, S. Spangler, D. P. Seeburg, C. C. Hoogenraad, and M. Sheng, J. Neurosci., 2005, 25, 11300.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Y. Ueda and M. Sato, ChemBioChem, 2018, 19, 1217.

    Article  CAS  PubMed  Google Scholar 

  18. Y. Nihongaki, H. Suzuki, F. Kawano, and M. Sato, ACS Chem. Biol., 2014, 9, 617.

    Article  CAS  PubMed  Google Scholar 

  19. G. Yu, H. Onodera, Y. Aono, F. Kawano, Y. Ueda, A. Furuya, H. Suzuki, and M. Sato, Sci. Rep., 2016, 6, 35777.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Y. Nihongaki, S. Yamamoto, F. Kawano, H. Suzuki, and M. Sato, Chem. Biol., 2015, 22, 169.

    Article  CAS  PubMed  Google Scholar 

  21. Y. Nihongaki, Y. Furuhata, T. Otabe, S. Hasegawa, K. Yoshimoto, and M. Sato, Nat. Methods, 2017, 14, 963.

    Article  CAS  PubMed  Google Scholar 

  22. J. Miyazaki, S. Takaki, K. Araki, F. Tashiro, A. Tominaga, K. Takatsu, and K. Yamamura, Gene, 1989, 79, 269.

    Article  CAS  PubMed  Google Scholar 

  23. M. Endo, N. Mochizuki, T. Suzuki, and A. Nagatani, Plant. Cell., 2007, 19, 84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. P. A. Salome, J. P. To, J. J. Kieber, and C. R. McClung, Plant. Cell., 2006, 18, 55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. A. Apolloni, I. A. Prior, M. Lindsay, R. G. Parton, and J. F. Hancock, Mol. Cell Biol., 2000, 20, 2475.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. J. Downward, Curr. Opin. Cell Biol., 1998, 10, 262.

    Article  CAS  PubMed  Google Scholar 

  27. J. Clark, K. E. Anderson, V. Juvin, T. S. Smith, F. Karpe, M. J. Wakelam, L. R. Stephens, and P. T. Hawkins, Nat. Methods, 2011, 8, 267.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. M. Yamao, H. Naoki, K. Kunida, K. Aoki, M. Matsuda, and S. Ishii, Sci. Rep., 2015, 5, 17527.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. T. Nishioka, K. Aoki, K. Hikake, H. Yoshizaki, E. Kiyokawa, and M. Matsuda, Mol. Biol. Cell, 2008, 19, 4213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Y. I. Wu, D. Frey, O. I. Lungu, A. Jaehrig, I. Schlichting, B. Kuhlman, and K. M. Hahn, Nature, 2009, 461, 104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. K. Aoki, Y. Kondo, H. Naoki, T. Hiratsuka, R. E. Itoh, and M. Matsuda, Dev. Cell., 2017, 43, 305.

    Article  CAS  PubMed  Google Scholar 

  32. Y. Hirano, A. Matsuda, and Y. Hiraoka, Microscopy (Oxf), 2015, 64, 237.

    Article  CAS  PubMed  Google Scholar 

  33. J. Riedl, A. H. Crevenna, K. Kessenbrock, J. H. Yu, D. Neukirchen, M. Bista, F. Bradke, D. Jenne, T. A. Holak, Z. Werb, M. Sixt, and R. Wedlich-Soldner, Nat. Methods, 2008, 5, 605.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. S. Nishi, C. Yamamoto, S. Yoneda, and S. Sueda, Anal. Sci., 2017, 33, 897.

    Article  CAS  PubMed  Google Scholar 

  35. J. H. Kim, S. R. Lee, L. H. Li, H. J. Park, J. H. Park, K. Y. Lee, M. K. Kim, B. A. Shin, and S. Y. Choi, PLoS One, 2011, 6, e18556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. A. Furuya, F. Kawano, T. Nakajima, Y. Ueda, and M. Sato, ACS Synth. Biol., 2017, 6, 1086.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro, Tokyo, 153-8902, Japan

    Yoshibumi Ueda, Yuki Aono & Moritoshi Sato

  2. AMED-PRIME, Japan Agency for Medical Research and Development, Tokyo, Japan

    Yoshibumi Ueda

  3. Department of Veterinary Pathology, School of Veterinary Medicine, Nippon Veterinary and Life Science University, 1-7-1 Kyonan-cho, Musashino, Tokyo, 180-8602, Japan

    Tatsuhito Ii

  4. Department of Physiology, Graduate School of Medical Science, Kanazawa University, Kanazawa, Ishikawa, Japan

    Naotoshi Sugimoto

  5. Department of Gastrointestinal and Hepato-Biliary-Pancreatic Surgery, Nippon Medical School, Bunkyo, Tokyo, 113-8603, Japan

    Seiichi Shinji & Hiroshi Yoshida

Authors
  1. Yoshibumi Ueda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tatsuhito Ii
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuki Aono
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Naotoshi Sugimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Seiichi Shinji
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hiroshi Yoshida
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Moritoshi Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ueda, Y., Ii, T., Aono, Y. et al. Membrane Dynamics Induced by a Phosphatidylinositol 3,4,5-Trisphosphate Optogenetic Tool. ANAL. SCI. 35, 57–63 (2019). https://doi.org/10.2116/analsci.18SDP06

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2116/analsci.18SDP06

Keywords

Search

Navigation