Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-17T11:26:05.828Z Has data issue: false hasContentIssue false
  • English
  • Français

Limulus opsins: Diurnal regulation of expression

Published online by Cambridge University Press:  22 January 2004

JASBIR S. DALAL ,
ROBERT N. JINKS ,
CHELSIE CACCIATORE ,
ROBERT M. GREENBERG  and
BARBARA-ANNE BATTELLE
JASBIR S. DALAL
Affiliation:
Whitney Laboratory and Department of Neuroscience, University of Florida, St. Augustine
ROBERT N. JINKS
Affiliation:
Department of Biology and Biological Foundations of Behavior Program, Franklin and Marshall College, Lancaster, PA
CHELSIE CACCIATORE
Affiliation:
Whitney Laboratory and Department of Neuroscience, University of Florida, St. Augustine
ROBERT M. GREENBERG
Affiliation:
Whitney Laboratory and Department of Neuroscience, University of Florida, St. Augustine
BARBARA-ANNE BATTELLE
Affiliation:
Whitney Laboratory and Department of Neuroscience, University of Florida, St. Augustine
Get access Rights & Permissions [Opens in a new window]

Abstract

Much has been learned from studies of Limulus photoreceptors about the role of the circadian clock and light in the removal of photosensitive membrane. However, little is known in this animal about mechanisms regulating photosensitive membrane renewal, including the synthesis of proteins in, and associated with, the photosensitive membrane. To begin to understand renewal, this study examines diurnal changes in the levels of mRNAs encoding opsin, the integral membrane protein component of visual pigment, and the relative roles of light and the circadian clock in producing these changes. We show that at least two distinct opsin genes encoding very similar proteins are expressed in both the lateral and ventral eyes, and that during the day and night in the lateral eye, the average level of mRNA encoding opsin1 is consistently higher than that encoding opsin2. Northern blot assays showed further that total opsin mRNA in the lateral eyes of animals maintained under natural illumination increases during the afternoon (9 & 12 h after sunrise) in the light and falls at night in the dark. This diurnal change occurs whether or not the eyes receive input from the circadian clock, but it is eliminated in eyes maintained in the dark. Thus, it is regulated by light and darkness, not by the circadian clock, with light stimulating an increase in opsin mRNA levels. The rise in opsin mRNA levels observed under natural illumination was seasonal; it occurred during the summer but not the spring and fall. However, a significant increase in opsin mRNA levels could be achieved in the fall by exposing lateral eyes to 3 h of natural illumination followed by 9 h of artificial light. The diurnal regulation of opsin mRNA levels contrasts sharply with the circadian regulation of visual arrestin mRNA levels (Battelle et al., 2000). Thus, in Limulus, distinctly different mechanisms regulate the levels of mRNA encoding two proteins critical for the photoresponse.

Keywords

LimulusOpsin genesDiurnal rhythmsPhotoreceptorsCircadian rhythms
Type
Research Article
Information
Visual Neuroscience , Volume 20 , Issue 5 , September 2003 , pp. 523 - 534
Copyright
2003 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Sequences reported in this article have been deposited in the NCBI database (Accession #s AY190508–AY190515).

References

REFERENCES

Alloway, P.G., Howard, L., & Dolph, P.J. (2000). The formation of stable rhodopsin–arrestin complexes induces apoptosis and photoreceptor cell degeneration. Neuron 28, 129–138.CrossRefGoogle Scholar
Applebury, M.L., Antoch, M.P., Baxter, L.C., Chun, L.L., Falk, J.D., Farhangfar, F., Kage, K., Krzystolik, M.G., Lyass, L.A., & Robbins, J.T. (2000). The murine cone photoreceptor: A single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27, 513–523.CrossRefGoogle Scholar
Arikawa, K., Mizuno, S., Kinoshita, M., & Stavenga, D.G. (2003). Coexpression of two visual pigments in a photoreceptor causes an abnormally broad spectral sensitivity in the eye of the butterfly Papilio xuthus. Journal of Neuroscience 23, 4527–4532.Google Scholar
Baehr, W., Falk, J.D., Bugra, K., Triantafyllos, J.T., & McGinnis, J.F. (1988). Isolation and analysis of the mouse opsin gene. FEBS Letters 238, 253–256.CrossRefGoogle Scholar
Barlow, R.B.Jr., Kaplan, E., Renninger, G.H., & Saito, T. (1985). Efferent control of circadian rhythms in the Limulus lateral eye. Neuroscience Research (Suppl.) 2, S65–S78.Google Scholar
Basinger, S.F., Hoffman, R., & Matthes, M. (1976). Photoreceptor shedding is initiated by light in the frog retina. Science 194, 1074–1076.CrossRefGoogle Scholar
Battelle, B.-A. (2002). Circadian efferent input to Limulus eyes: Anatomy, circuitry and impact. Microscopy Research and Technique 58, 345–355.CrossRefGoogle Scholar
Battelle, B.-A. & LaVail, M.M. (1978). Rhodopsin content and rod outer segment length in albino rat eyes. Experimental Eye Research 26, 487–497.CrossRefGoogle Scholar
Battelle, B.-A., Williams, C.D., Schremser-Berlin, J.-L., & Cacciatore, C. (2000). Regulation of arrestin mRNA levels in Limulus lateral eyes: Separate and combined influences of circadian efferent input and light. Visual Neuroscience 17, 217–227.Google Scholar
Battelle, B.-A., Dabdoub, A., Malone, M.A., Andrews, A.W., Cacciatore, C., Calman, B.G., Smith, W.C., & Payne, R. (2001). Immunocytochemical localization of opsin, visual arrestin, myosin III, and calmodulin in Limulus lateral eye retinular cells and ventral photoreceptors. Journal of Comparative Neurology 435, 211–225.CrossRefGoogle Scholar
Besharse, J.C., Hollyfield, J.G., & Rayborn, M.E. (1977). Turnover of rod photoreceptor outer segments. II. Membrane addition and loss in relationship to light. Journal of Cell Biology 75, 507–527.Google Scholar
Blest, A.D. (1978). The rapid synthesis and destruction of photoreceptor membrane by a dinopid spider: A daily cycle. Proceedings of the Royal Society B (London) 200, 463–483.CrossRefGoogle Scholar
Bok, D. & Hall, M.O. (1971). The role of the pigment epithelium in the etiology of inherited retinal dystrophy in the rat. Journal of Cell Biology 49, 664–682.CrossRefGoogle Scholar
Briscoe, A.D. (1999). Intron splice sites of Papilio glaucus Pgl Rh3 corroborate insect opsin phylogeny. Gene 230, 101–109.Google Scholar
Briscoe, A.D. (2000). Six opsins from the butterfly Papilio glaucus: Molecular phylogenetic evidence for paralogous origins of red-sensitive visual pigments in insects. Journal of Molecular Evolution 51, 110–121.CrossRefGoogle Scholar
Byk, T., Bar-Yaccov, M., Doz, Y.N., Minke, B., & Selinger, Z. (1993). Regulation of arrestin cycle secures the fidelity and maintenance of the fly photoreceptor cell. Proceedings of the National Academy of Sciences of the U.S.A. 90, 1907–1911.CrossRefGoogle Scholar
Chamberlain, S.C. & Barlow, R.B., Jr. (1979). Light and efferent activity control rhabdom turnover in Limulus photoreceptors. Science 206, 361–363.CrossRefGoogle Scholar
Chamberlain, S.C. & Barlow, R.B., Jr. (1984). Transient membrane shedding in Limulus photoreceptors: Control mechanisms under natural lighting. Journal of Neuroscience 7, 2135–2144.Google Scholar
Chen, F., Ukhanova, M., Thomas, D., Afshar, G., Tanda, S., Battelle, B.-A., & Payne, R. (1999). Molecular cloning of a putative cyclic nucleotide-gated ion channel cDNA from Limulus polyphemus. Journal of Neurochemistry 72, 461–471.CrossRefGoogle Scholar
Claridge-Chang, A., Wijnen, H., Naef, F., Boothroyd, C., Rajewsky, N., & Young, M.W. (2001). Circadian regulation of gene expression systems in the Drosophila head. Neuron 32, 657–671.CrossRefGoogle Scholar
Dolph, P.J., Ranganathan, R., Colley, N.J., Hardy, R.W., Socolich, M., & Zuker, C.S. (1993). Arrestin function in inactivation of G protein-coupled receptor rhodopsin in vivo. Science 260, 1910–1916.CrossRefGoogle Scholar
Ferguson, S.G. (2001). Evolving concepts in G protein coupled receptor endocytosis: The role in receptor desensitization and signaling. Pharmacological Reviews 53, 1–24.Google Scholar
Goldman, A.I., Tierstein, P.S., & O'Brien, P.J. (1980). The role of ambient lighting in circadian disk shedding in the rod outer segment of the rat retina. Investigative Ophthalmology and Visual Science 19, 1257–1267.Google Scholar
Grace, M.S., Chiba, A., & Menaker, M. (1999). Circadian control of photoreceptor outer segment membrane turnover in mice genetically incapable of melatonin synthesis. Visual Neuroscience 16, 909–918.Google Scholar
Green, C.B. & Besharse, J.C. (1996). Use of a high stringency differential display screen for identification of retinal mRNAs that are regulated by a circadian clock. Molecular Brain Research 37, 157–165.CrossRefGoogle Scholar
Hanna, W.J.B., Pinkhasov, E., Renninger, G.H., Kaplan, E., & Barlow, R.B., Jr. (1985). The tail of Limulus contains photoreceptors that modulate a circadian clock. Biological Bulletin 169, 552.Google Scholar
Hanna, W.J.B., Horne, J.A., & Renninger, G.H. (1988). Circadian photoreceptor organs in Limulus. II. The telson. Journal of Comparative Physiology A 162, 133–140.CrossRefGoogle Scholar
Hartman, S.J., Menon, I., Haug-Collet, K., & Colley, N.J. (2001). Expression of rhodopsin and arrestin during the light–dark cycle in Drosophila. Molecular Vision 17(7), 95–100.Google Scholar
Horne, J.A. & Renninger, G.H. (1988). Circadian photoreceptor organs in Limulus I. Ventral, median and lateral eyes. Journal of Comparative Physiology A 162, 127–132.Google Scholar
Kiselev, A., Socolich, M., Vinos, J., Hardy, R.W., Zuker, C.S., & Ranganathan, R. (2000). A molecular pathway for light-dependent photoreceptor apoptosis in Drosophila. Neuron 28, 139–152.CrossRefGoogle Scholar
Kitamoto, J., Sakamoto, K., Ozaki, K., Mishina, Y., & Arikawa, K. (1998). Two visual pigments in a single photoreceptor cell: Identification and histological localization of three mRNAs encoding visual pigment opsins in the retina of the butterfly Papilio xuthus. Journal of Experimental Biology 201, 1255–1261.Google Scholar
Korenbrot, J.I. & Fernald, R.D. (1989). Circadian rhythm and light regulate opsin mRNA in rod photoreceptors. Nature 337, 454–457.CrossRefGoogle Scholar
LaVail, M.M., (1976). Rod outer segment disk shedding in the retina: Relationship to cyclic lighting. Science 194, 1071–1074.CrossRefGoogle Scholar
Leonard, D.S., Bowman, V.D., Ready, D.F., & Pak, W.L. (1992). Degeneration of photoreceptors in rhodopsin mutants of Drosophila. Journal of Neurobiology 23, 605–626.CrossRefGoogle Scholar
Li, W.-H. (1997). Molecular Evolution. Southerland, Massachusetts: Sinauer Associates, pp. 1–487.
Liu, X., Vansant, G., Udovichenko, I.P., Wolfrum, U., & Williams, D.S. (1997). Myosin VIIa, the product of the Usher 1B syndrome gene, is concentrated in the connecting cilia of photoreceptors. Cell Motility and Cytoskeleton 37, 240–252.3.0.CO;2-A>CrossRefGoogle Scholar
Lukáts, Á., Dkhisst-Benyahya, O., Szepessy, Z., Röhlich, P., Vigh, B., Bennett, N.C., Cooper, H.M., & Szél, Á. (2002). Visual pigment co-expression in all cones of two rodents, the Siberian hamster and the pouched mouse. Investigative Ophthalmology and Visual Science 43, 2468–2473.Google Scholar
Moritz, O.L., Tam, B.M., Hurd, L.L., Peranen, J., Deretic, D., & Papermaster, D.S. (2001). Mutant rab8 impairs docking and fusion of rhodopsin-bearing post-golgi membranes and causes cell death of transgenic Xenopus rods. Molecular Biology of the Cell 12, 2341–2351.CrossRefGoogle Scholar
Moutsaki, P., Bellingham, J., Soni, B.G., David-Gray, Z.K., & Foster, R.G. (2000). Sequence, genome structure and tissue expression of carp (Cyprinus carpio L.) vertebrate ancient (VA) opsin. FEBS Letters 473, 316–322.Google Scholar
Murry, G. (1966). Intracelluar absorption difference spectrum of Limulus extra-ocular photolabile pigment. Science 154, 1182–1183.CrossRefGoogle Scholar
Nathans, J. & Hogness, D.S. (1983). Isolation, sequence analysis and intron-exon arrangement of the gene encoding bovine rhodopsin. Cell 34, 807–814.CrossRefGoogle Scholar
Nathans, J. & Hogness, D.S. (1984). Isolation and nucleotide sequence of the gene encoding human rhodopsin. Proceedings of the National Academy of Sciences of the U.S.A. 81, 4851–4855.CrossRefGoogle Scholar
Nathans, J., Thomas, D., & Hogness, D.S. (1986). Molecular genetics of human color vision: The genes encoding blue, green, and red pigments. Science 232, 193–202.CrossRefGoogle Scholar
Nguyen-Legros, J. & Hicks, D.S. (2000). Renewal of photoreceptor outer segments and their phagocytosis by retinal pigment epithelium. International Review of Cytology 196, 245–313.CrossRefGoogle Scholar
Nolte, J. & Brown, J.E. (1972). The spectral sensitivities of single photoreceptor cells in the lateral, ventral and median eyes of normal and white-eyed Limulus. Journal of General Physiology 55, 787–801.Google Scholar
Organisciak, D.T., Xie, A., Wang, H.-M., Jiang, Y.-L., Darrow, R.M., & Donoso, L.A. (1991). Adaptive changes in visual cell transduction protein levels: Effect of light. Experimental Eye Research 53, 773–779.CrossRefGoogle Scholar
Ranganathan, R., Malicki, D.M., & Zuker, C.S . (1995). Signal transduction in Drosophila photoreceptors. Annual Review of Neuroscience 18, 283–317.CrossRefGoogle Scholar
Renninger, G.H., Lajolie, C., Hanna, W.J.B., Fong, D., House, C., & Zelin, J. (1997). Phase shifting and entrainment of a circadian rhythm in Limulus polyphemus by ocular and exraocular photoreceptors. Biological Rhythms Research 28, 50–68.CrossRefGoogle Scholar
Sacunas, R.B., Papuga, M.O., Malone, M.A., Pearson, A.C., Jr., Marjanovic, M., Stroope, D.G., Weiner, W.W., Chamberlain, S.C., & Battelle, B.-A. (2002). Multiple mechanisms of rhabdom shedding in the lateral eye of Limulus polyphemus. Journal of Comparative Neurology 449, 26–42.CrossRefGoogle Scholar
Sakamoto, K., Hisatomi, O., Tokunaga, F., & Eguchi, E. (1996). Two opsins from the compound eye of the crab Hemigrapsus sanguineus. Journal of Experimental Biology 199, 441–450.Google Scholar
Schremser, J.-L. & Williams, T.P. (1995a). Rod outer segment (ROS) renewal as a mechanism for adaptation to a new intensity environment. I. Rhodopsin levels and ROS length. Experimental Eye Research 61, 17–23.Google Scholar
Schremser, J.-L. & Williams, T.P. (1995b). Rod outer segment (ROS) renewal as a mechanism for adaptation to a new intensity environment. II. Rhodopsin synthesis and packing density. Experimental Eye Research 61, 25–32.Google Scholar
Smith, W.C., Price, D.A., Greenberg, R.M., & Battelle, B.-A. (1993). Opsins from the lateral eyes and ocelli of the horseshoe crab, Limulus polyphemus. Proceedings of the National Academy of Sciences of the U.S.A. 90, 6150–6154.CrossRefGoogle Scholar
von Schantz, M., Lulcas, R.J., & Foster, R.G. (1999). Circadian oscillation of photopigment transcript levels in the mouse. Molecular Brain Research 72, 108–114.CrossRefGoogle Scholar
White, R.H. & Lord, E. (1975). Diminution and enlargement of the mosquito rhabdom in light and darkness. Journal of General Physiology 65, 583–598.CrossRefGoogle Scholar
Williams, D.S. (1991). Actin filaments and photoreceptor membrane turnover. Bioessays 4, 171–178.CrossRefGoogle Scholar
Wolfrum, U. & Schmitt, A. (2000). Rhodopsin transport in the membrane of the connecting cilium of mammalian photoreceptor cells. Cell Motility and Cytoskeleton 46, 95–107.3.0.CO;2-Q>CrossRefGoogle Scholar
Xu, J., Dodd, R.L., Makino, C.L., Simon, M.I., Baylor, D.A., & Chen, J. (1997). Prolonged photoresponses in transgenic mouse rods lacking arrestin. Nature 389, 505–509.Google Scholar
Yarfitz, S. & Hurley, J.B. (1994). Transduction mechanisms of vertebrate and invertebrate photoreceptors. Journal of Biological Chemistry 20, 14329–14332.Google Scholar
Zuker, C.S., Cowman, A.F., & Rubin, G.M. (1985). Isolation and structure of a rhodopsin gene from D. melanogaster. Cell 40, 851–858.Google Scholar