Skip to main content
SpringerLink
Log in

A green cone-like pigment in the ‘blind’ mole-rat Spalax ehrenbergi: functional expression and photochemical characterization

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

The degenerate subcutaneous eye of the blind mole rat belonging to the Spalax ehrenbergi superspecies has been shown to contain a long wavelength sensitive (LWS) cone pigment. Baculovirus expression of this LWS pigment and subsequent IMAC purification yields a photosensitive protein, that according to absorbance maximum (530 ± 2 nm), kinetics of late phototransitions, and transducin activation, has all characteristics of a functional green cone pigment. The absorbance spectrum of the Spalax pigment is strongly red-shifted relative to the very homologous mouse, rabbit and rat green cone pigments (508–510 nm). Also in contrast to the rodent pigments, the Spalax pigment exhibits anion-dependent spectral properties, displaying a 12 nm blue-shift upon substitution of chloride ions by nitrate ions. Finally, the slow part of the photocascade deviates in some aspects from that of sighted mammals. The possible relevance of these findings for the evolutionary adaptation of Spalax to a subterranean ecotope is discussed.

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

Abbreviations

LWS:

long wavelength sensitive

SGH:

histidine-tagged Spalax green cone pigment

SCN:

suprachiasmatic nucleus

DoM:

n-dodecyl-ß-1-d-maltoside

MOI:

multiplicity of infection

dpi:

days post infection

IMAC:

immobilized metal affinity chromatography

NTA:

nitriloacetic acid

NRO:

N-retinylidene-opsin

DTE:

dithioerythritol

Hepps:

N-(2-hydroxyethyl)piperazine-N-(3-propanesulfonic acid).

References

  1. E. Nevo, Mosaic evolution of subterranean mammals–Regression, progression, and global convergence, Oxford University Press, Oxford, UK.

  2. S. Sanyal, H. G. Jansen, W. J. DeGrip, E. Nevo, and W. W. DeJong, The eye of the blind mole-rat Spalax ehrenbergi. Rudiment with hidden function? Invest. Ophthalmol. Visual Sci., 1990, 31, 1398–1404.

    CAS  Google Scholar 

  3. H. M. Cooper, M. Herbin, and E. Nevo, Ocular regression conceals adaptive progression of the visual system in a blind subterranean mammal, Nature, 1993, 361, 156–159.

    Article  CAS  Google Scholar 

  4. R. Necker, G. Rehkämper, and E. Nevo, Electrophysiological mapping of body representation in the cortex of the blind mole rat, NeuroRep., 1992, 3, 505–508.

    Article  CAS  Google Scholar 

  5. G. Rehkämper, R. Necker, and E. Nevo, Functional anatomy of the thalamus in the blind mole rat Spalax ehrenbergi: An architectonic and electrophysiologically controlled tracing study, J. Comp. Neurol., 1994, 347, 570–584.

    Article  Google Scholar 

  6. Z. K. David-Gray, J. W. H. Janssen, W. J. DeGrip, E. Nevo, and R. G. Foster, Light detection in a ‘blind’ mammal, Nature Neurosci., 1998, 1, 655–656.

    Article  CAS  Google Scholar 

  7. J. W. H. Janssen, P. H. M. Bovee-Geurts, A. P. A. Peeters, J. K. Bowmaker, H. M. Cooper, Z. K. David-Gray, E. Nevo, and W. J. DeGrip, A fully functional rod visual pigment in a blind mammal–A case for adaptive functional reorganization? J. Biol. Chem., 2000, 275, 38674–38679.

    Article  CAS  Google Scholar 

  8. S. Yokoyama, and F. B. Radlwimmer, The molecular genetics of red and green color vision in mammals, Genetics, 1999, 153, 919–932.

    Article  CAS  Google Scholar 

  9. A. B. Asenjo, J. Rim, and D. D. Oprian, Molecular determinants of human red/green color discrimination, Neuron, 1994, 12, 1131–1138.

    Article  CAS  Google Scholar 

  10. H. Sun, J. P. Macke, and J. Nathans, Mechanisms of spectral tuning in the mouse green cone pigment, Proc. Nat. Acad. Sci. USA, 1997, 94, 8860–8865.

    Article  CAS  Google Scholar 

  11. P. M. A. M. Vissers, P. H. M. Bovee-Geurts, M. D. Portier, C. H. W. Klaassen, and W. J. DeGrip, Large-scale production and purification of the human green cone pigment: Characterization of late photo-intermediates, Biochem. J., 1998, 330, 1201–1208.

    Article  CAS  Google Scholar 

  12. C. H. W. Klaassen, P. H. M. Bovee-Geurts, G. L. J. DeCaluwé, and W. J. DeGrip, Large-scale production and purification of functional recombinant bovine rhodopsin using the baculovirus expression system, Biochem. J., 1999, 342, 293–300.

    Article  CAS  Google Scholar 

  13. W. J. DeGrip, J. VanOostrum, P. H. M. Bovee-Geurts, Selective detergent-extraction from mixed detergent/lipid/protein micelles, using cyclodextrin inclusion compounds: A novel generic approach for the preparation of proteoliposomes, Biochem. J., 1998, 330, 667–674.

    Article  CAS  Google Scholar 

  14. K. Fahmy, and T. P. Sakmar, Light-dependent transducin activation by an ultraviolet-absorbing rhodopsin mutant, Biochemistry, 1993, 32, 9165–9171.

    Article  CAS  Google Scholar 

  15. T. Higashijima, and K. M. Ferguson, Tryptophan fluorescence of G proteins: Analysis of guanine nucleotide binding and hydrolysis, Methods Enzymol., 1991, 195, 321–328.

    Article  CAS  Google Scholar 

  16. E. Faurobert, A. E. Otto-Bruc, P. Chardin, and M. Chabre, Tryptophan W207 in transducin Ta is the fluorescence sensor of the G protein activation switch and is involved in the effector binding, EMBO J., 1993, 12, 4191–4198.

    Article  CAS  Google Scholar 

  17. H. Kühn, Interactions between photoexcited rhodopsin and light-activated enzymes in rods, Prog. Retin. Res., 1984, 3, 123–156.

    Article  Google Scholar 

  18. Z. K. David-Gray, H. M. Cooper, J. W. H. Janssen, E. Nevo, and R. G. Foster, Spectral tuning of a circadian photopigment in a subterranean ‘blind’ mammal (Spalax ehrenbergi), FEBS Lett., 1999, 461, 343–347.

    Article  CAS  Google Scholar 

  19. Z. Y. Wang, A. B. Asenjo, and D. D. Oprian, Identification of the Cl−-binding site in the human red and green color vision pigments, Biochemistry, 1993, 32, 2125–2130.

    Article  CAS  Google Scholar 

  20. K. Palczewski, T. Kumasaka, T. Hori, C. A. Behnke, H. Motoshima, B. A. Fox, I. LeTrong, D. C. Teller, T. Okada, R. E. Stenkamp, M. Yamamoto, and M. Miyano, Crystal structure of rhodopsin: A G protein-coupled receptor, Science, 2000, 289, 739–745.

    Article  CAS  Google Scholar 

  21. T. Okada, and K. Palczewski, Crystal structure of rhodopsin: Implications for vision and beyond, Curr. Opin. Struct. Biol., 2001, 11, 420–426.

    Article  CAS  Google Scholar 

  22. T. Yoshizawa, and Y. Imamoto, Structure and photobleaching process of chicken iodopsin, Biophys. Chem., 1995, 56, 57–62.

    Article  CAS  Google Scholar 

  23. H. Imai, A. Terakita, and Y. Shichida, Analysis of amino acid residues in rhodopsin and cone visual pigments that determine their molecular properties, Methods Enzymol., 2000, 315, 293–312.

    Article  CAS  Google Scholar 

  24. J. W. Lewis, and D. S. Kliger, Absorption spectroscopy in studies of visual pigments: Spectral and kinetic characterization of intermediates, Methods Enzymol., 2000, 315, 164–178.

    Article  CAS  Google Scholar 

  25. H. Imai, Y. Imamoto, T. Yoshizawa, and Y. Shichida, Difference in molecular properties between chicken green and rhodopsin as related to the functional difference between cone and rod photoreceptor cells, Biochemistry, 1995, 34, 10525–10531.

    Article  CAS  Google Scholar 

  26. F. DeLange, M. Merkx, P. H. M. Bovee-Geurts, A. M. A. Pistorius, and W. J. DeGrip, Modulation of the metarhodopsin I/metarhodopsin II equilibrium of bovine rhodopsin by ionic strength–Evidence for a surface charge effect, Eur. J. Biochem., 1997, 243, 174–180.

    Article  CAS  Google Scholar 

  27. J. H. Parkes, and P. A. Liebman, Temperature and pH dependence of the metarhodopsin I-Metarhodopsin II kinetics and equilibria in de bovine rod disk membrane suspensions, Biochemistry, 1984, 23, 5054–5061.

    Article  CAS  Google Scholar 

  28. S. Tachibanaki, Y. Imamoto, H. Imai, and Y. Shichida, Effect of chloride on the thermal reverse reaction of intermediates of iodopsin, Biochemistry, 1995, 34, 13170–13175.

    Article  CAS  Google Scholar 

  29. T. Okada, T. Matsuda, H. Kandori, Y. Fukada, T. Yoshizawa, and Y. Shichida, Circular dichroism of metaiodopsin II and its binding to transducin: A comparative study between meta II intermediates of iodopsin and rhodopsin, Biochemistry, 1994, 33, 4940–4946.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry UMC-160, Nijmegen Center for Molecular Life Sciences, University of Nijmegen Medical School, P.O. Box 9101, Nijmegen, The Netherlands

    Jannie W. H. Janssen, Petra H. M. Bovee-Geurts & Willem J. DeGrip

  2. Department of Integrative & Molecular Neuroscience, Division of Neuroscience & Psychological Medicine, Imperial College School of Medicine, Charing Cross Hospital, Fulham Palace Road, London, UK, W6 8RF

    Zoë K. David-Gray & Russell G. Foster

  3. Institute of Evolution, University of Haifa, Haifa, 31905, Israel

    Eviatar Nevo

Authors
  1. Jannie W. H. Janssen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zoë K. David-Gray
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Petra H. M. Bovee-Geurts
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eviatar Nevo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Russell G. Foster
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Willem J. DeGrip
    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

Janssen, J.W.H., David-Gray, Z.K., Bovee-Geurts, P.H.M. et al. A green cone-like pigment in the ‘blind’ mole-rat Spalax ehrenbergi: functional expression and photochemical characterization. Photochem Photobiol Sci 2, 1287–1291 (2003). https://doi.org/10.1039/b300059c

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/b300059c

Search

Navigation