Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Translocation of a calcium-permeable cation channel induced by insulin-like growth factor-I

Nature Cell Biology volume 1, pages 165–170 (1999)Cite this article

Abstract

Calcium plays a critical part in the regulation of cell growth, and growth factors stimulate calcium entry into cells through calcium-permeable channels. However, the molecular nature and regulation of calcium-permeable channels are still unclear at present. Here we report the molecular characterization of a calcium-permeable cation channel that is regulated by insulin-like growth factor-I (IGF-I). This channel, which we name growth-factor-regulated channel (GRC), belongs to the TRP-channel family and localizes mainly to intracellular pools under basal conditions. Upon stimulation of cells by IGF-I, GRC translocates to the plasma membrane. Thus, IGF-I augments calcium entry through GRC by regulating trafficking of the channel.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Structural characteristics and tissue expression patterns of GRC.
Figure 2: Characterization of GRC as an IGF-I-regulated, calcium-permeable, non-selective cation channel.
Figure 3: Translocation of GRC from intracellular compartments to the plasma membrane.
Figure 4: Translocation of endogenous GRC in MIN6 cells.

Similar content being viewed by others

References

  1. Lu, K. P. & Means, A. Regulation of the cell cycle by calcium and calmodulin. Endocrine Rev. 14, 40–58 (1993).

    Article  CAS  Google Scholar 

  2. Lovisolo, D., Distasi, C., Antoniotti, S. & Munaron, L. Mitogens and calcium channel. News Physiol. Sci. 12, 279–285 (1997).

    CAS  Google Scholar 

  3. LeRoith, D., Werner, H., Beitner-Johnson, D. & Roberts, C. T. Molecular and cellular aspects of the insulin-like growth factor-I receptor. Endocrine Rev. 16, 143–163 (1995).

    Article  CAS  Google Scholar 

  4. Kojima, I., Matsunaga, H., Kurokawa, K., Ogata, E. & Nishimoto, I. Calcium influx: an intracellular message of the mitogenic action of insulin-like growth factor-I. J. Biol. Chem. 263, 16561–16567 (1988).

    CAS  PubMed  Google Scholar 

  5. Kojima, I., Mogami, H. & Ogata, E. Role of calcium entry and protein kinase C in the progression activity of insulin-like growth factor-I. J.Biol. Chem. 268, 1003–1006 (1993).

    Google Scholar 

  6. Tedder, T. F., Forsgre, A., Boyd, A. W., Nadler, L. M. & Schlossman, S. F. Antibodies reactive with the B1 molecule inhibit cell cycle progression but not activation of human B lymphocytes. Eur. J. Immunol. 16, 881–887 (1986).

    Article  CAS  Google Scholar 

  7. Tedder, T. F. & Engel, P. D20: a regulator of cell-cycle progression of B lymphocytes. Immunol. Today 15, 450–454 (1994).

    Article  CAS  Google Scholar 

  8. Bubien, J. K., Zhou, L. J., Bell, P. D., Frizzell, R. A. & Tedder, T. F. Transfection of the CD20 cell surface molecule into ectopic cell types generates a Ca2+ conductance found constitutively in B lymphocytes. J. Cell Biol. 121, 1121–1132 (1993).

    Article  CAS  Google Scholar 

  9. Kanzaki, M., Nie, L., Shibata, H. & Kojima, I. Activation of calcium-permeable cation channel CD20 by insulin-like growth factor-I in Balb/c 3T3 cells. J. Biol. Chem. 272, 4964–4969 (1997).

    Article  CAS  Google Scholar 

  10. Caterina, M. J. et al. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816–824 (1997).

    Article  CAS  Google Scholar 

  11. Kyte, J. & Doolittle, R. F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105–132 (1982).

    Article  CAS  Google Scholar 

  12. Saitou, N. & Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol. Evol. 4, 406-425 (1987).

    Google Scholar 

  13. Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).

    Article  CAS  Google Scholar 

  14. Okada, T., Sakuma, L., Fukui, Y., Hazeki, O. & Ui, M. Blockage of chemotactic peptide-induced stimulation of neutrophils by wortmannin as a result of selective inhibition of phosphatidylinositol 3-kinase. J.Biol.Chem. 269, 3563–3567 (1994).

    CAS  PubMed  Google Scholar 

  15. Vlahos, C. J., Matter, W. F., Hui, Y. & Brown, R. F. A specific inhibitor of phosphoinositide 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269, 5241–5248 (1994).

    CAS  PubMed  Google Scholar 

  16. Caterina, M. J., Rosen, T. A., Tominaga, M., Brake, A. J. & Julius, D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398, 436–441 (1999).

    Article  CAS  Google Scholar 

  17. Hara, K. et al. Phosphatidylinositol 3-kinase activity is required for insulin-stimulated glucose transport but not for RAS activation in CHO cells. Proc. Natl Acad. Sci. USA 91, 7415–7419 (1994).

    Article  CAS  Google Scholar 

  18. Miyazaki, J. et al. Establishment of a pancreatic β-cell line that retains glucose-inducible insulin secretion. Endocrinol. 127, 126–132 (1990).

    Article  CAS  Google Scholar 

  19. Holman, G. D. & Kasuga, M. From receptor to transport: insulin signalling to glucose transport. Diabetologia 40, 991–1003 (1997).

    Article  CAS  Google Scholar 

  20. Marks, M. S., Ohno, H., Kirchhausen, T. & Bonifacino, J. S. Protein sorting by tyrosine-based signals. Trends Cell Biol. 7, 124–128 (1997).

    Article  CAS  Google Scholar 

  21. Shibata, H., Suzuki, Y., Omata, W., Tanaka, S. & Kojima, I. Dissection of GLUT4 recycling pathway into exocytosis and endocytosis. J. Biol. Chem. 270, 11489–11495 (1995).

    Article  CAS  Google Scholar 

  22. Kanzaki, M., Shibata, H., Mogami, H. & Kojima, I. Expression of calcium-permeable cation channel CD20 accelerates cell-cycle progression in Balb/c 3T3 cells. J. Biol. Chem. 270, 13099–13104 (1995).

    Article  Google Scholar 

  23. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685 (1970).

    Article  CAS  Google Scholar 

  24. Matsumoto, B. Cell biological applications of confocal microscopy. Methods Cell Biol. 38, 20–35 (1993).

    Google Scholar 

  25. Hamil, O. P., Marty, M., Neher, E., Sackman, B. & Sigworth, F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. Eur. J. Physiol. 391, (1981).

Download references

Acknowledgements

This study was supported by Grants-in-Aid for Scientific Research on Priority Area from the Ministry of Education, Science, Sports and Culture of Japan. We thank J. Takeda and K. Takata for discussions.

Correspondence and requests for materials should be addressed to I.K. The cDNA sequence for mouse GRC has been deposited at GenBank under accession number AB021665.

Author information

Authors and Affiliations

  1. Department of Cell Biology, Institute for Molecular and Cellular Regulation, Gunma University, Maebashi, 371-8512, Japan

    Makoto Kanzaki, You-Qing Zhang*, Hirosato Mashima*, Lu Li*, Hiroshi Shibata* & Itaru Kojima

Authors
  1. Makoto Kanzaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. You-Qing Zhang*
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hirosato Mashima*
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lu Li*
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hiroshi Shibata*
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Itaru Kojima
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Itaru Kojima.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kanzaki, M., Zhang*, YQ., Mashima*, H. et al. Translocation of a calcium-permeable cation channel induced by insulin-like growth factor-I. Nat Cell Biol 1, 165–170 (1999). https://doi.org/10.1038/11086

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/11086

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing