Skip to main content
SpringerLink
Log in

Anion sensitivity and spectral tuning of middle- and long-wavelength-sensitive (MWS/LWS) visual pigments

  • Research Article
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

The long-wavelength-sensitive (LWS) opsins form one of four classes of vertebrate cone visual pigment and exhibit peak spectral sensitivities (λmax) that generally range from 525 to 560 nm for rhodopsin/vitamin-A1 photopigments. Unique amongst the opsin classes, many LWS pigments show anion sensitivity through the interaction of chloride ions with a histidine residue at site 197 (H197) to give a long-wavelength spectral shift in peak sensitivity. Although it has been shown that amino acid substitutions at five sites (180, 197, 277, 285 and 308) are useful in predicting the λmax values of the LWS pigment class, some species, such as the elephant shark and most marine mammals, express LWS opsins that possess λmax values that are not consistent with this ‘five-site’ rule, indicating that other interactions may be involved. This study has taken advantage of the natural mutation at the chloride-binding site in the mouse LWS pigment. Through the use of a number of mutant pigments generated by site-directed mutagenesis, a new model has been formulated that takes into account the role of charge and steric properties of the side chains of residues at sites 197 and 308 in the function of the chloride-binding site in determining the peak sensitivity of LWS photopigments.

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

Similar content being viewed by others

References

  1. Yokoyama S, Radlwimmer FB (2001) The molecular genetics and evolution of red and green color vision in vertebrates. Genetics 158:1697–1710

    PubMed  CAS  Google Scholar 

  2. Crescitelli F (1977) Ionochromic behavior of Grecko visual pigments. Science 195:187–188

    Article  PubMed  CAS  Google Scholar 

  3. Crescitelli F, Karvaly B (1991) The gecko visual pigment: the anion hypsochromic effect. Vis Res 31:945–950

    Article  PubMed  CAS  Google Scholar 

  4. Fager RS, Goldman SL, Abrahamson EW (1979) Ethanolamine attack of the bovine rhodopsin chromophore. Exp Eye Res 29:393–399

    Article  PubMed  CAS  Google Scholar 

  5. Kleinschmidt J, Harosi FI (1992) Anion sensitivity and spectral tuning of cone visual pigments in situ. Proc Natl Acad Sci USA 89:9181–9185

    Article  PubMed  CAS  Google Scholar 

  6. Shichida Y, Kato T, Sasayama S, Fukada Y, Yoshizawa T (1990) Effects of chloride on chicken iodopsin and the chromophore transfer reactions from iodopsin to scotopsin and B-photopsin. Biochemistry 29:5843–5848

    Article  PubMed  CAS  Google Scholar 

  7. Wang Z, Asenjo AB, Oprian DD (1993) Identification of the Cl(−)-binding site in the human red and green color vision pigments. Biochemistry 32:2125–2130

    Article  PubMed  CAS  Google Scholar 

  8. Radlwimmer FB, Yokoyama S (1998) Genetic analyses of the green visual pigments of rabbit (Oryctolagus cuniculus) and rat (Rattus norvegicus). Gene 218:103–109

    Article  PubMed  CAS  Google Scholar 

  9. Sun H, Macke JP, Nathans J (1997) Mechanisms of spectral tuning in the mouse green cone pigment. Proc Natl Acad Sci USA 94:8860–8865

    Article  PubMed  CAS  Google Scholar 

  10. Fasick JI, Cronin TW, Hunt DM, Robinson PR (1998) The visual pigments of the bottlenose dolphin (Tursiops truncatus). Vis Neurosci 15:643–651

    Article  PubMed  CAS  Google Scholar 

  11. Fasick JI, Robsinson PR (1998) Mechanism of spectral tuning in the dolphin visual pigments. Biochemistry 37:433–438

    Article  PubMed  CAS  Google Scholar 

  12. Davies WL, Carvalho LS, Tay BH, Brenner S, Hunt DM, Venkatesh B (2009) Into the blue: gene duplication and loss underlie color vision adaptations in a deep-sea chimaera, the elephant shark Callorhinchus milii. Genome Res 19:415–426

    Article  PubMed  CAS  Google Scholar 

  13. Franke RR, Sakmar TP, Oprian DD, Khorana HG (1988) A single amino acid substitution in rhodopsin (lysine 248 to leucine) prevents activation of transducin. J Biol Chem 263:2119–2122

    PubMed  CAS  Google Scholar 

  14. Molday RS, MacKenzie D (1983) Monoclonal antibodies to rhodopsin: characterization, cross-reactivity, and application as structural probes. Biochemistry 22:653–660

    Article  PubMed  CAS  Google Scholar 

  15. Davies WL, Collin SP, Hunt DM (2009) Adaptive gene loss reflects differences in the visual ecology of basal vertebrates. Mol Biol Evol 26:1803–1809

    Article  PubMed  CAS  Google Scholar 

  16. Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K (2000) In search of the visual pigment template. Vis Neurosci 17:509–528

    Article  PubMed  CAS  Google Scholar 

  17. Davies WL, Cowing JA, Carvalho LS, Potter IC, Trezise AE, Hunt DM, Collin SP (2007) Functional characterization, tuning, and regulation of visual pigment gene expression in an anadromous lamprey. FASEB J 21:2713–2724

    Article  PubMed  CAS  Google Scholar 

  18. Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723

    Article  PubMed  CAS  Google Scholar 

  19. Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res 31:3381–3385

    Article  PubMed  CAS  Google Scholar 

  20. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201

    Article  PubMed  CAS  Google Scholar 

  21. Bordoli L, Kiefer F, Arnold K, Benkert P, Battey J, Schwede T (2009) Protein structure homology modeling using SWISS-MODEL workspace. Nat Protoc 4:1–13

    Article  PubMed  CAS  Google Scholar 

  22. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I, Teller DC, Okada T, Stenkamp RE, Yamamoto M, Miyano M (2000) Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289:739–745

    Article  PubMed  CAS  Google Scholar 

  23. Okada T, Sugihara M, Bondar AN, Elstner M, Entel P, Buss V (2004) The retinal conformation and its environment in rhodopsin in light of a new 2.2 A crystal structure. J Mol Biol 342:571–583

    Article  PubMed  CAS  Google Scholar 

  24. Kaushal S, Khorana HG (1994) Structure and function in rhodopsin. 7. Point mutations associated with autosomal dominant retinitis pigmentosa. Biochemistry 33:6121–6128

    Article  PubMed  CAS  Google Scholar 

  25. Yokoyama S, Takenaka N, Agnew DW, Shoshani J (2005) Elephants and human color-blind deuteranopes have identical sets of visual pigments. Genetics 170:335–344

    Article  PubMed  CAS  Google Scholar 

  26. Arrese CA, Beazley LD, Ferguson MC, Oddy A, Hunt DM (2006) Spectral tuning of the long wavelength-sensitive cone pigment in four Australian marsupials. Gene 381:13–17

    Article  PubMed  CAS  Google Scholar 

  27. Lamb TD, Pugh EN Jr (2006) Phototransduction, dark adaptation, and rhodopsin regeneration the proctor lecture. Invest Ophthalmol Vis Sci 47:5137–5152

    Article  PubMed  Google Scholar 

  28. Baylor DA, Matthews G, Yau KW (1980) Two components of electrical dark noise in toad retinal rod outer segments. J Physiol 309:591–621

    PubMed  CAS  Google Scholar 

  29. Ebrey T, Koutalos Y (2001) Vertebrate photoreceptors. Prog Retin Eye Res 20:49–94

    Article  PubMed  CAS  Google Scholar 

  30. Kefalov VJ, Estevez ME, Kono M, Goletz PW, Crouch RK, Cornwall MC, Yau KW (2005) Breaking the covalent bond—a pigment property that contributes to desensitization in cones. Neuron 46:879–890

    Article  PubMed  CAS  Google Scholar 

  31. Miller JL, Picones A, Korenbrot JI (1994) Differences in transduction between rod and cone photoreceptors: an exploration of the role of calcium homeostasis. Curr Opin Neurobiol 4:488–495

    Article  PubMed  CAS  Google Scholar 

  32. Pugh EN Jr, Nikonov S, Lamb TD (1999) Molecular mechanisms of vertebrate photoreceptor light adaptation. Curr Opin Neurobiol 9:410–418

    Article  PubMed  CAS  Google Scholar 

  33. Travis GH (2005) DISCO! Dissociation of cone opsins: the fast and noisy life of cones explained. Neuron 46:840–842

    Article  PubMed  CAS  Google Scholar 

  34. Yau KW (1994) Phototransduction mechanism in retinal rods and cones. The Friedenwald Lecture. Invest Ophthalmol Vis Sci 35:9–32

    PubMed  CAS  Google Scholar 

  35. Yokoyama S (2000) Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res 19:385–419

    Article  PubMed  CAS  Google Scholar 

  36. Davies WL (2011) Adaptive gene loss in vertebrates: photosensitivity as a model case. Encyclopedia of life sciences

  37. Newman LA, Robinson PR (2005) Cone visual pigments of aquatic mammals. Vis Neurosci 22:873–879

    Article  PubMed  Google Scholar 

  38. Merbs SL, Nathans J (1992) Absorption spectra of human cone pigments [see comments]. Nature 356:433–435

    Article  PubMed  CAS  Google Scholar 

  39. Newman LA, Robinson PR (2006) The visual pigments of the West Indian manatee (Trichechus manatus). Vis Res 46:3326–3330

    Article  PubMed  CAS  Google Scholar 

  40. Fasick JI, Cronin TW, Hunt DM, Robinson PR (1998) The visual pigments of the bottlenose dolphin (Tursiops truncatus). Vis Neurosci 15:643–651

    Article  PubMed  CAS  Google Scholar 

  41. Arrese CA, Hart NS, Thomas N, Beazley LD, Shand J (2002) Trichromacy in Australian marsupials. Curr Biol 12:657–660

    Article  PubMed  CAS  Google Scholar 

  42. Deeb SS, Wakefield MJ, Tada T, Marotte L, Yokoyama S, Marshall Graves JA (2003) The cone visual pigments of an Australian marsupial, the tammar wallaby (Macropus eugenii): sequence, spectral tuning, and evolution. Mol Biol Evol 20:1642–1649

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the BBSRC. We are grateful to Dr. Rosalie Crouch of the Storm Eye Institute, Medical University of South Carolina, USA, for the kind gift of 11-cis-retinal.

Author information

Authors and Affiliations

  1. UCL Institute of Ophthalmology, 11–43 Bath Street, London, EC1V 9EL, UK

    Wayne I. L. Davies, Susan E. Wilkie, Jill A. Cowing & David M. Hunt

  2. Nuffield Laboratory of Ophthalmology, Nuffield Department of Clinical Neuroscience, University of Oxford, John Radcliffe Hospital, Headley Way, Oxford, OX3 9DU, UK

    Wayne I. L. Davies & Mark W. Hankins

  3. School of Animal Biology and UWA Oceans Institute, University of Western Australia, 35 Stirling Highway, Perth, WA, 6009, Australia

    Wayne I. L. Davies & David M. Hunt

  4. Lions Eye Institute, 2 Verdun Street, Perth, WA, 6009, Australia

    David M. Hunt

Authors
  1. Wayne I. L. Davies
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susan E. Wilkie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jill A. Cowing
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mark W. Hankins
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David M. Hunt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David M. Hunt.

Additional information

Wayne I. L. Davies and Susan E. Wilkie contributed equally to this research.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Davies, W.I.L., Wilkie, S.E., Cowing, J.A. et al. Anion sensitivity and spectral tuning of middle- and long-wavelength-sensitive (MWS/LWS) visual pigments. Cell. Mol. Life Sci. 69, 2455–2464 (2012). https://doi.org/10.1007/s00018-012-0934-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-012-0934-4

Keywords

Search

Navigation