Skip to main content

Advertisement

SpringerLink
Log in

Electrochemical microwell sensor with Fe–N co-doped carbon catalyst to monitor nitric oxide release from endothelial cell spheroids

  • Original Paper
  • Published:
Analytical Sciences Aims and scope Submit manuscript

Abstract

Endothelial cells have been widely used for vascular biology studies; recent progress in tissue engineering have offered three-dimensional (3D) culture systems for vascular endothelial cells which can be considered as physiologically relevant models. To facilitate the studies, we developed an electrochemical device to detect nitric oxide (NO), a key molecule in the vasculature, for the evaluation of 3D cultured endothelial cells. Using an NO-sensitive catalyst composed of Fe–N co-doped reduced graphene oxide, the real-time monitoring of NO release from the endothelial cell spheroids was demonstrated.

Graphical abstract

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

Authors can confirm that all relevant data are included in the article and/or its supporting information files.

References

  1. S.H. Bhang, S. Lee, T.-J. Lee, W.-G. La, H.-S. Yang, S.-W. Cho, B.-S. Kim, Tissue Eng. Part A 18, 310–319 (2012)

    Article  CAS  PubMed  Google Scholar 

  2. T.-W. Hsu, Y.-J. Lu, Y.-J. Lin, Y.-T. Huang, L.-H. Hsieh, B.-H. Wu, Y.-C. Lin, L.-C. Chen, H.-W. Wang, J.-C. Chuang, Y.-Q. Fang, C.-C. Huang, Biomaterials 272, 120765 (2021)

    Article  CAS  PubMed  Google Scholar 

  3. K. Ino, A. Ito, H. Kumazawa, H. Kagami, M. Ueda, H. Honda, J. Chem. Eng. Jpn. 40, 51–58 (2007)

    Article  CAS  Google Scholar 

  4. R. Obregón, J. Ramón-Azcón, S. Ahadian, H. Shiku, H. Bae, M. Ramalingam, T. Matsue, J. Nanosci. Nanotechnol 14, 487–500 (2014)

    Article  PubMed  Google Scholar 

  5. J.H. Yeon, H.R. Ryu, M. Chung, Q.P. Hu, N.L. Jeon, Lab Chip 12, 2815–2822 (2012)

    Article  CAS  PubMed  Google Scholar 

  6. Y. Nashimoto, R. Okada, S. Hanada, Y. Arima, K. Nishiyama, T. Miura, R. Yokokawa, Biomaterials 229, 119547 (2020)

    Article  CAS  PubMed  Google Scholar 

  7. L.A. Kunz-Schughart, J.A. Schroeder, M. Wondrak, F. van Rey, K. Lehle, F. Hofstaedter, D.N. Wheatley, Am. J. Physiol. Cell Physiol. 290, C1385-1398 (2006)

    Article  CAS  PubMed  Google Scholar 

  8. K. Hiramoto, H.-J. Pai, K. Ino, Y. Nashimoto, H. Shiku, Electrochim. Acta 340, 135979 (2020)

    Article  CAS  Google Scholar 

  9. A.M. Laib, A. Bartol, A. Alajati, T. Korff, H. Weber, H.G. Augustin, Nat. Protoc. 4, 1202–1215 (2009)

    Article  CAS  PubMed  Google Scholar 

  10. M. Heiss, M. Hellström, M. Kalén, T. May, H. Weber, M. Hecker, H.G. Augustin, T. Korff, FASEB J. 29, 3076–3084 (2015)

    Article  CAS  PubMed  Google Scholar 

  11. N. Taira, Y. Nashimoto, K. Ino, H. Ida, T. Imaizumi, A. Kumatani, Y. Takahashi, H. Shiku, Anal. Chem. 93, 4902–4908 (2021)

    Article  CAS  PubMed  Google Scholar 

  12. R.C. Jin, J.J. Loscalzo, Blood Med. 2010, 147–162 (2010)

    Google Scholar 

  13. K. Shibuki, Neurosci. Res. 9, 69–76 (1990)

    Article  CAS  PubMed  Google Scholar 

  14. M.D. Brown, M.H. Schoenfisch, Chem. Rev. 119, 11551–11575 (2019)

    Article  CAS  PubMed  Google Scholar 

  15. U. Förstermann, T. Münzel, Circulation 113, 1708–1714 (2006)

    Article  PubMed  Google Scholar 

  16. W.M. Kuebler, U. Uhlig, T. Goldmann, G. Schael, A. Kerem, K. Exner, C. Martin, E. Vollmer, S. Uhlig, Am. J. Respir. Crit. Care Med. 168, 1391–1398 (2003)

    Article  PubMed  Google Scholar 

  17. S. Isik, W. Schuhmann, Angew. Chem. Int. Ed. 45, 7451–7454 (2006)

    Article  CAS  Google Scholar 

  18. Y.-L. Liu, X.-Y. Wang, J.-Q. Xu, C. Xiao, Y.-H. Liu, X.-W. Zhang, J.-T. Liu, W.-H. Huang, Chem. Sci. 6, 1853–1858 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. H. Xu, C. Liao, Y. Liu, B.-C. Ye, B. Liu, Anal. Chem. 90, 4438–4444 (2018)

    Article  CAS  PubMed  Google Scholar 

  20. Y.L. Liu, Y. Qin, Z.H. Jin, X.B. Hu, M.M. Chen, R. Liu, C. Amatore, W.H. Huang, Angew. Chem. Int. Ed 56, 9454–9458 (2017)

    Article  CAS  Google Scholar 

  21. R. Li, H. Qi, Y. Ma, Y. Deng, S. Liu, Y. Jie, J. Jing, J. He, X. Zhang, L. Wheatley, C. Huang, X. Sheng, M. Zhang, L. Yin, Nat. Commun. 11, 3207 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Y.-S. Torisawa, A. Takagi, H. Shiku, T. Yasukawa, T. Matsue, Oncol. Rep. 13, 1107–1112 (2005)

    CAS  PubMed  Google Scholar 

  23. A. Weltin, S. Hammer, F. Noor, Y. Kaminski, J. Kieninger, G.A. Urban, Biosens. Bioelectron. 87, 941–948 (2017)

    Article  CAS  PubMed  Google Scholar 

  24. K. Hiramoto, K. Ino, K. Komatsu, Y. Nashimoto, H. Shiku, Biosens. Bioelectron. 181, 113123 (2021)

    Article  CAS  PubMed  Google Scholar 

  25. E. Flampouri, S. Imar, K. Oconnell, B. Singh, ACS Sensors 4, 660–669 (2019)

    Article  CAS  PubMed  Google Scholar 

  26. C. Caviglia, R.P. Carletto, S. De Roni, Y.M. Hassan, S. Hemanth, M. Dufva, S.S. Keller, Electrochim. Acta 359, 136951 (2020)

    Article  CAS  Google Scholar 

  27. Z. Liu, H. Forsyth, N. Khaper, A. Chen, Analyst 141, 4074–4083 (2016)

    Article  CAS  PubMed  Google Scholar 

  28. F. Du, W. Huang, Y. Shi, Z. Wang, J. Cheng, Biosens. Bioelectron. 24, 415–421 (2008)

    Article  CAS  PubMed  Google Scholar 

  29. P.-H. Ling, X.-N. Zang, C.-H. Qian, F. Gao, Analyst 146, 2609–2616 (2021)

    Article  CAS  PubMed  Google Scholar 

  30. S.L. Vilakazi, T. Nyokong, J. Electroanal. Chem. 512, 56–63 (2001)

    Article  CAS  Google Scholar 

  31. N. Diab, J. Oni, W. Schuhmann, Bioelectrochemistry 66, 105–110 (2005)

    Article  CAS  PubMed  Google Scholar 

  32. N. Morimoto, T. Kubo, Y. Nishina, Sci. Rep. 6, 21715 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. B.M. Leung, S.C. Lesher-Perez, T. Matsuoka, C. Moraes, S. Takayama, Biomater. Sci. 3, 336–344 (2015)

    Article  CAS  PubMed  Google Scholar 

  34. J. Maruyama, I. Abe, Chem. Mater. 17, 4660–4667 (2005)

    Article  CAS  Google Scholar 

  35. K. Kamiya, K. Hashimoto, S. Nakanishi, Chem. Commun. 48, 10213–10215 (2012)

    Article  CAS  Google Scholar 

  36. C.A. Caro, J.H. Zagal, F. Bedioui, J. Electrochem. Soc. 150, E95–E103 (2003)

    Article  CAS  Google Scholar 

  37. L. Zhang, Y. Ni, X. Wang, G. Zhao, Talanta 82, 196–201 (2010)

    Article  CAS  PubMed  Google Scholar 

  38. F. Wang, X. Deng, W. Wang, Z. Chen, J. Solid State Electrochem. 15, 829–836 (2011)

    Article  CAS  Google Scholar 

  39. C. Zhang, F. Hu, X. Hao, Q. Rao, T. Hu, W. Sun, C. Guo, C.M. Li, Adv. Sci. 9, 2104066 (2022)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by JST COI (Grant No. JPMJCE1303), Grant-in-Aid for JSPS Fellows (No.20J21401), KAKENHI programs (No. 20K15374), and Grant-in-Aid for Scientific Research (B) (Nos. 18H01840, 18H01999, 21H01957, and 21H03803), from the Japan Society for the Promotion of Science (JSPS). This work was also supported by System Design of Inclusive Society Living with Infectious Diseases (SDGS-ID), Tohoku University, the Shimadzu Science Foundation, the Kato Foundation for Promotion for Science, the Murata Science Foundation, the Electrochemical Society of Japan, and the Japan Association for Chemical Innovation. We thank Mr. H. Magara (Tohoku University) for his help with SEM imaging.

Author information

Author notes

  1. Kaoru Hiramoto and Kazuyuki Iwase have contributed equally to this work.

Authors and Affiliations

  1. Frontier Research Institute for Interdisciplinary Sciences, Tohoku University, Sendai, 980-0845, Japan

    Kaoru Hiramoto

  2. Institute of Multidisciplinary Research for Advanced Materials, Tohoku University, Sendai, 980-8577, Japan

    Kazuyuki Iwase & Itaru Honma

  3. Graduate School of Environmental Studies, Tohoku University, Sendai, 980-8579, Japan

    Yoshinobu Utagawa

  4. Institute of Biomaterials and Bioengineering, Tokyo Medical and Dental University, Tokyo, 101-0062, Japan

    Yuji Nashimoto

  5. Graduate School of Engineering, Tohoku University, Sendai, 980-8579, Japan

    Kosuke Ino & Hitoshi Shiku

Authors
  1. Kaoru Hiramoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kazuyuki Iwase
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yoshinobu Utagawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yuji Nashimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Itaru Honma
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kosuke Ino
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hitoshi Shiku
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Kazuyuki Iwase, Kosuke Ino or Hitoshi Shiku.

Ethics declarations

Conflict of interest

There are no conflicts to declare.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 12609 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hiramoto, K., Iwase, K., Utagawa, Y. et al. Electrochemical microwell sensor with Fe–N co-doped carbon catalyst to monitor nitric oxide release from endothelial cell spheroids. ANAL. SCI. 38, 1297–1304 (2022). https://doi.org/10.1007/s44211-022-00160-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s44211-022-00160-0

Keywords

Search

Navigation