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.

  • Letter
  • Published:

Cyclophilin-related protein RanBP2 acts as chaperone for red/green opsin

Nature volume 383, pages 637–640 (1996)Cite this article

Abstract

CYCLOPHILINS are ubiquitous and abundant proteins that exhibit peptidyl prolyl cis-trans isomerization (PPlase) activity in vitro1,2. Their functions in vivo, however, are not well understood. Two new retinal cyclophilin isoforms, types I and II, are highly expressed in cone photoreceptors of the vertebrate retina3. Type-II cyclophilin is identical to RanBP2, a large protein that binds the GTPase Ran4,5. Here we report that two contiguous domains in RanBP2, Ran-binding domain 4 (RBD4) and cyclophilin, act in concert as a chaperone for the opsin molecule of the red/green-sensitive visual pigment of a dichromatic vertebrate. In Drosophila, the cyclophilin NinaA6,7 is expressed in all photoreceptors8 and is required for the expression of only a subset of opsins8,9. The molecular basis of these photoreceptor class-specific effects and the functions of NinaA and other cyclophilins in vivo remain unclear10. Unlike NinaA, which forms a stable complex with opsin from retinular cells Rl–611, we find that the cyclophilin domain of RanBP2 does not bind opsin directly; rather, it augments and stabilizes the interaction between red/green (R/G) opsin and the RBD4 domain. This involves a cyclophilin-mediated modification of R/G opsin, possibly involving proline isomerization. The RBD4–cyclophilin supradomain of RanBP2, therefore, is a form of vertebrate chaperone of defined substrate specificity, which may be involved in the processing and/or transport of long-wavelength opsin in cone photoreceptor cells.

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

Similar content being viewed by others

References

  1. Fisher, G., Wittmann-Liebold, B., Lang, K., Kiefhaber, T. & Schmid, F. Nature 337, 476–478 (1989).

    Article  ADS  Google Scholar 

  2. Bergsma, D. et al. J. Biol. Chem. 266, 23204–23214 (1991).

    CAS  PubMed  Google Scholar 

  3. Ferreira, P., Hom, J. & Pak, W. J. Biol. Chem. 270, 23179–23188 (1995).

    Article  CAS  Google Scholar 

  4. Yokoyama, N. et al. Nature 376, 184–188 (1995).

    Article  ADS  CAS  Google Scholar 

  5. Wu, J., Manutis, M., Kraemer, D., Blobel, G. & Coutavas, E. J. Biol. Chem. 270, 14209–14213 (1995).

    Article  CAS  Google Scholar 

  6. Schneuwly, S. et al. Proc. Natl Acad. Sci. USA 86, 5390–5394 (1989).

    Article  ADS  CAS  Google Scholar 

  7. Shieh, B.-H., Stammes, M., Seavello, S., Harris, G. & Zuker, C. Nature 338, 67–70 (1989).

    Article  ADS  CAS  Google Scholar 

  8. Stamnes, A., Shieh, B.-H., Chuman, L., Harris, L. & Zuker, C. Cell 65, 219–227 (1991).

    Article  CAS  Google Scholar 

  9. Larrivee, D., Conrad, S., Stepheson, R. & Pak, W. J. Gen. Physiol. 78, 521–545 (1981).

    Article  CAS  Google Scholar 

  10. Ferreira, P. & Pak, W. In Degenerative Diseases of the Retina (eds Angerson, ?, La Vail, ? & Hollyfield, ?) 263–274 (Plenum, New York, 1995).

    Book  Google Scholar 

  11. Baker, E., Colley, N. & Zuker, C. EMBO J. 13, 4886–4895 (1994).

    Article  CAS  Google Scholar 

  12. Wang, Y. et al. Neuron 9, 429–440 (1992).

    Article  CAS  Google Scholar 

  13. Nathans, J., Thomas, D. & Hogness, D. Science 232, 193–202 (1986).

    Article  ADS  CAS  Google Scholar 

  14. Nathans, J. & Hogness, D. Cell 34, 807–814 (1983).

    Article  CAS  Google Scholar 

  15. Travis, G., Sutcliffe, J. & Bok, D. Neuron 6, 61–70 (1991).

    Article  CAS  Google Scholar 

  16. Zydowsky, L. et al. Protein Sci. 1, 1092–1099 (1992).

    Article  CAS  Google Scholar 

  17. Kallen, H. & Walkinshaw, M. FEBS Lett. 300, 286–290 (1992).

    Article  CAS  Google Scholar 

  18. Ke, H., Mayrose, D. & Cao, W. Proc. Natl Acad. Sci. USA 90, 3324–3328 (1993).

    Article  ADS  CAS  Google Scholar 

  19. Kamps, K., De Grip, W. & Daemen, F. Biochim. Biophys. Acta 687, 296–302 (1982).

    Article  CAS  Google Scholar 

  20. Walter, A., Shuster, T. & Farber, D. Invest. Ophthalmol. Vis. Sci. 27, 1609–1614 (1986).

    CAS  PubMed  Google Scholar 

  21. Stephenson, R. S., O'Tousa, J., Scavarda, N. J., Randall, L. L. & Pak, W. L. in The Biology of Photoreception (eds Cosens, D. J. & Vince-Price, D.) 447–501 (Cambridge Univ. Press, 1983).

    Google Scholar 

  22. Pak, W. L. Invest. Ophthalmol. Vis. Sci. 36, 2340–2357 (1995).

    CAS  PubMed  Google Scholar 

  23. Molday, R. S. & Molday, L. L. J. Cell Biol. 105, 2598–2601 (1987).

    Article  Google Scholar 

  24. Schlenstedt, G., Saavedra, C., Loeb, J., Cole, C. & Silver, P. Proc. Natl Acad. Sci. USA 92, 225–229 (1995).

    Article  ADS  CAS  Google Scholar 

  25. Ren, M. et al. Mol. Cell. Biol. 15, 2117–2124 (1995).

    Article  CAS  Google Scholar 

  26. Klebe, C., Bischoff, F. R., Ponstingl, H. & Wittinghofer, A. Biochemistry 34, 639–647 (1995).

    Article  CAS  Google Scholar 

  27. Roepman, R. et al. Hum. Mol. Genet. 5, 827–833 (1996).

    Article  CAS  Google Scholar 

  28. Roepman, R. et al. Hum. Mol. Genet. 5, 1035–1041 (1996).

    Article  CAS  Google Scholar 

  29. Meindl, A. et al. Nature Genet. 13, 35–42 (1992).

    Article  Google Scholar 

  30. Nakayama, T. A. & Khorana, H. G. J. Biol. Chem. 266, 4269–4275 (1991).

    CAS  PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Tomoko A. Nakayama: Department of Biostructure and Function, The University of Connecticut Health Center, 263 Farmington Avenue, Farmington, Connecticut 06030-3705, USA

  2. William L. Pak: Department of Biological Sciences, Lilly Hall of Life Sciences, Purdue University, West Lafayette, Indiana 47907, USA

Authors and Affiliations

  1. Department of Psychiatry and Program in Neuroscience, University of Texas Southwestern Medical Center, 5323 Harry Mines Boulevard, Dallas, Texas, 75235-9111, USA

    Paulo A. Ferreira, Tomoko A. Nakayama, William L. Pak & Gabriel H. Travis

Authors
  1. Paulo A. Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tomoko A. Nakayama
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. William L. Pak
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gabriel H. Travis
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ferreira, P., Nakayama, T., Pak, W. et al. Cyclophilin-related protein RanBP2 acts as chaperone for red/green opsin. Nature 383, 637–640 (1996). https://doi.org/10.1038/383637a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/383637a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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