Opsin co-expression in Limulus photoreceptors: Differential regulation by light and a circadian clock

Journal of Experimental Biology

Volumn 213, Issue 15, 2010, Pages 2589-2601

  Katti, C ^a,b,d   Kempler, K ^a,b   Porter, M L ^c   Legg, A ^a,b   Gonzalez, R ^a,b   Garcia Rivera, E ^a,b   Dugger, D ^b   Battelle, B A ^a,b  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Circadian rhythm; Limulus; Opsin; Opsin co expression; Photoreceptor

Indexed keywords

ANTIBODY; ETHIDIUM; MESSENGER RNA; OPSIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BIOLOGICAL RHYTHM; CELL MEMBRANE; CHEMISTRY; CHEMOLUMINESCENCE; CIRCADIAN RHYTHM; CYTOLOGY; FLUORESCENCE; FROZEN SECTION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LIGHT; LIMULUS; METABOLISM; MOLECULAR GENETICS; PHOTORECEPTOR CELL; PHYLOGENY; RADIATION EXPOSURE; RNA TRANSPORT; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; HORSESHOE CRAB; LUMINESCENCE; RADIATION RESPONSE;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; BIOLOGICAL CLOCKS; CELL MEMBRANE; CHEMILUMINESCENT MEASUREMENTS; CIRCADIAN RHYTHM; ETHIDIUM; FLUORESCENCE; FROZEN SECTIONS; GENE EXPRESSION REGULATION; HORSESHOE CRABS; LIGHT; MOLECULAR SEQUENCE DATA; OPSINS; PHOTORECEPTOR CELLS, INVERTEBRATE; PHYLOGENY; RNA TRANSPORT; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; LUMINESCENT MEASUREMENTS;

ANIMALIA; INVERTEBRATA; LIMULUS; VERTEBRATA;

EID: 77954837047     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.043869     Document Type: Article

References (62)

1. Abascal, F., Zardoya, R. and Posada, D. (2005). ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104-2105.
2. Adamus, G., Arendt, A., Zam, Z. S., McDowell, J. H. and Hargrave, P. A. (1988). Use of peptides to select for anti-rhodopsin antibodies with desired amino acid sequence specificities. Peptide Res. 1, 42-47.
3. Adamus, G., Zam, Z. S., Arendt, A., Palczewski, K., McDowell, J. H. and Hargrave, P. A. (1991). Anti-rhodopsin monoclonal-antibodies of defined specificity-characterization and application. Vis. Res. 31, 17-31.
4. Applebury, M. L., Antoch, M. P., Baxter, L. C., Chun, L. L. Y., Falk, J. D., Farhangfar, F., Kage, K., Krzystolik, M. G., Lyass, L. A. and 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.
5. Arendt, D., Tessmar-Raible, K., Snyman, H., Dorresteijn, A. W. and Wittbrodt, J. (2004). Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 306, 869-871. (Pubitemid 39446995)
6. Arikawa, K., Mizuno, S., Kinoshita, M. and Stavenga, D. (2003). Coexpression of two visual pigments in a photoreceptor causes an abnormally broad spectral sensitivity in the eye of the butterfly Papilio xuthus. J. Neurosci. 23, 4527-4532. (Pubitemid 36706183)
7. Bailey, M. J. and Cassone, V. M. (2005). Melanopsin expression in the chick retina and pineal gland. Mol. Brain Res. 134, 345-348.
8. Barlow, R. B., Jr (1983). Circadian rhythms in the Limulus visual system. J. Neurosci. 3, 856-870.
9. Barlow, R. B., Jr, Bolanowski, S. J., Jr and Brachman, M. L. (1977). Efferent optic nerve fibers mediate circadian rhythms in the Limulus eye. Science 197, 86-89.
10. Barlow, R. B., Jr, Chamberlain, S. and Levinson, J. (1980). Limulus brain modulates the structure and function of the lateral eyes. Science 210, 1037-1039.
11. Barlow, R. B., Jr, Kaplan, E., Renninger, G. H. and Saito, T. (1987). Circadian rhythms in Limulus photoreceptors. I. Intracellular studies. J. Gen. Physiol. 89, 353-378.
12. Battelle, B. (2002). Circadian efferent input to Limulus eyes: anatomy, circuitry, and impact. Microsc. Res. Tech. 58, 345-355.
13. Battelle, B.-A., Andrews, A., Kempler, K., Edwards, S. and Smith, W. (2000a). Visual arrestin in Limulus is phosphorylated at multiple sites in the light and in the dark. Vis. Neurosci. 17, 813-822. (Pubitemid 32046115)
14. Battelle, B.-A., Williams, C. D., Schremser-Berlin, J. L. and Cacciatore, C. (2000b). Regulation of arrestin mRNA levels in Limulus lateral eye: Separate and combined influences of circadian efferent input and light. Vis. Neurosci. 17, 217-227.
15. Battelle, B., Dabdoub, A., Malone, M., Andrews, A., Cacciatore, C., Caiman, B., Smith, W. and Payne, R. (2001). Immunocytochemical localization of opsin, visual arrestin, myosin III, and calmodulin in Limulus lateral eye retinular cells and ventral photoreceptors. J. Comp. Neurol. 435, 211-225. (Pubitemid 32480008)
16. Bayer, D. and Barlow, R. B., Jr (1978). Limulus ventral eye. Physiological properties of photoreceptor cells in an organ culture medium. J. Gen. Physiol. 72, 539-563.
17. Briscoe, A. D. and Chittka, L. (2001). The evolution of color vision in insects. Annu. Rev. Entornol. 46, 471-510.
18. Calman, B. G. and Battelle, B.-A. (1991). Central origin of the efferent neurons projecting to the eyes of Limulus-polyphemus. Vis. Neurosci. 6, 481-495.
19. Chamberlain, S. C. and Barlow, R. B., Jr (1984). Transient membrane shedding in Limulus photoreceptors: control mechanisms under natural lighting. J. Neurosci. 4, 2792-2810.
20. Chamberlain, S. and Barlow, R. (1987). Control of structural rhythms in the lateral eye of Limulus- interactions of natural lighting and circadian efferent activity. J. Neurosci. 7, 2135-2144.
21. Chen, F. H., Ukhanova, M., Thomas, D., Afshar, G., Tanda, S., Battelle, B.-A. and Payne, R. (1999). Molecular cloning of a putative cyclic nucleotide-gated ion channel cDNA from Limulus polyphemus. J. Neurochem. 72, 461-471. (Pubitemid 29055207)
22. Dalal, J., Jinks, R., Cacciatore, C., Greenberg, R. and Battelle, B.-A. (2003). Limulus opsins: diurnal regulation of expression. Vis. Neurosci. 20, 523-534. (Pubitemid 38468626)
23. De Voe, R. D. (1972). Dual sensitivity of cells in wolf spider eyes at ultraviolet and visible wavelengths of light. J. Gen. Physiol. 59, 247-269.
24. Frank, T. M., Porter, M. and Cronin, T. W. (2009). Spectral sensitivity, visual pigments and screening pigments in two life history stages of the ontogenetic migrator Gnathophausia ingens. J. Mar. Biol. Assoc. UK 89, 119-129.
25. Gao, N., Foster, R. G. and Hardie, J. (2000). Two opsin genes from the vetch aphid, Megoura viciae. Insect Mol. Biol. 9, 197-202.
26. Gartner, W. and Towner, P. (1995). Invertebrate visual pigments. Photochem. Photobiol. 62, 1-16.
27. Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704. (Pubitemid 37365050)
28. Guindon, S., Lethiec, F., Duroux, P. and Gascuel, O. (2005). PHYML Online - a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res. 33, W557-W559.
29. Hillis, D. M. and Bull, J. J. (1993). An empirical-test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 42, 182-192.
30. Hubbard, R. and Wald, G. (1960). Visual pigment of the horseshoe crab, Limulus-polyphemus. Nature 186, 213-215.
31. Kaplan, E. and Barlow, R. B., Jr (1980). Circadian clock in Limulus brain increases response and decreases noise of retinal photoreceptors. Nature 286, 393-395.
32. Kaplan, E., Barlow, R. B., Renninger, G. and Purpura, K. (1990). Circadian rhythms in Limulus photoreceptors. II. Quantum bumps. J. Gen. Physiol. 96, 665-685. (Pubitemid 20301280)
33. Kashiyama, K., Seki, T., Numata, H. and Goto, S. G. (2009). Molecular characterization of visual pigments in Branchiopoda and the evolution of opsins in Arthropoda. Mol. Biol. Evol. 26, 299-311.
34. Katoh, K. and Toh, H. (2008). Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 9, 286-298. (Pubitemid 351890825)
35. Katoh, K., Misawa, K., Kuma, K. and Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059-3066. (Pubitemid 34851225)
36. Kier, C. K. and Chamberlain, S. C. (1990). Dual controls of screening pigment movement in photoreceptors of the Limulus lateral eye: Circadian efferent input and light. Vis. Neurosci. 4, 237-255.
37. Kitamoto, J., Sakamoto, K., Ozaki, K., Mishina, Y. and 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. J. Exp. Biol. 201, 1255-1261.
38. Knox, B., Salcedo, E., Mathiesz, K., Schaefer, J., Chou, W., Chadwell, L., Smith, W., Britt, S. and Barlow, R. (2003). Heterologous expression of Limulus rhodopsin. J. Biol. Chem. 278, 40493-40502.
39. Laemmli, U. K. (1970). Cleavage of structural proteins during assembly of head of bacteriophages. Nature 227, 680-685.
40. Lukats, A., Dkhissi-Benyahya, O., Szepessy, Z., Rohlich, P., Vigh, B., Bennett, N. C., Cooper, H. M. and Szel, A. (2002). Visual pigment coexpression in all cones of two rodents, the Siberian hamster, and the pouched mouse. Invest. Ophthalmol. Vis. Sci. 43, 2468-2473.
41. Lukats, A., Szabo, A., Rohlich, P., Vigh, B. and Szel, A. (2005). Photopigment coexpression in mammals: comparative and developmental aspects. Histol. Histopathol. 20, 551-574.
42. Matz, M. V. (2003). Amplification of representative cDNA pools from microscopic amounts of animal tissue. Methods Mol. Biol. 221, 103-116.
43. Mazzoni, E. O., CeMk, A., Mathias, F. W. C., Vasiliauskas, D., Johnston, R. J., Cook, T. A., Pichaud, F. and Desplan, C. (2008). Iroquois complex genes induce co-expression of rhodopsins in Drosophila. PLoS Biol. 6, 825-835.
44. Nolte, J. and Brown, J. E. (1970). Spectral sensitivities of single receptor cells in lateral, median, and ventral eyes of normal and white-eyed Limulus. J. Gen. Physiol. 55, 787-801.
45. Nolte, J. and Brown, J. E. (1972). Electrophysiological properties of cells in median ocellus of Limulus. J. Gen. Physiol. 59, 167-185.
46. Oakley, T. H. and Huber, D. R. (2004). Differential expression of duplicated opsin genes in two eye types of ostracod crustaceans. J. Mol. Evol. 59, 239-249.
47. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le Trong, I., Teller, D. C., Okada, T., Stenkamp, R. E. et al. (2000). Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289, 739-745.
48. Pieprzyk, A., Weiner, W. and Chamberlain, S. (2003). Mechanisms controlling the sensitivity of the Limulus lateral eye in natural lighting. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 189, 643-653.
49. Porter, M., Cronin, T., McClellan, D. and Crandall, K. (2007). Molecular characterization of crustacean visual pigments and the evolution of pancrustacean opsins. Mol. Biol. Evol. 24, 253-268.
50. Porter, M. L., Bok, M. J., Robinson, P. R. and Cronin, T. W. (2009). Molecular diversity of visual pigments in Stomatopoda (Crustacea). Vis. Neurosci. 26, 255-265.
51. Rohlich, P., Vanveen, T. and Szel, A. (1994). Two different visual pigments in one retinal cone cell. Neuron 13, 1159-1166.
52. Sacunas, R., Papuga, M., Malone, M., Pearson, A. J., Marjanovic, M., Stroope, D., Weiner, W., Chamberlain, S. and Battelle, B. (2002). Multiple mechanisms of rhabdom shedding in the lateral eye of Limulus polyphemus. J. Comp. Neurol. 449, 26-42.
53. Sakamoto, K., Hisatomi, O., Tokunaga, F. and Eguchi, E. (1996). Two opsins from the compound eye of the crab Hemigrapsus sanguineus. J. Exp. Biol. 199, 441-450.
54. Salcedo, E., Zheng, L. J., Phistry, M., Bagg, E. E. and Britt, S. G. (2003). Molecular basis for ultraviolet vision in invertebrates. J. Neurosci. 23, 10873-10878.
55. Salcedo, E., Farrell, D. M., Zheng, L. J., Phistry, M., Bagg, E. E. and Britt, S. G. (2009). The green-absorbing Drosophila Rh6 visual pigment contains a blue-shifting amino acid substitution that is conserved in vertebrates. J. Biol. Chem. 284, 5717-5722.
56. Smith, W. C., Friedman, M. A. and Goldsmith, T. H. (1992). Retinoids in the lateral eye of Limulus-evidence for a retinal photoisomerase. Vis. Neurosci. 8, 329-336.
57. Smith, W. C., Price, D. A., Greenberg, R. M. and Battelle, B.-A. (1993). Opsins from the lateral eyes and ocelli of the horseshoe-crab, Limulus-polyphemus. Proc. Natl. Acad. Sci. USA 90, 6150-6154.
58. Su, C. Y., Luo, D. G., Terakita, A., Shichida, Y., Liao, H. W., Kazmi, M. A., Sakmar, T. P. and Yau, K. W. (2006). Parietal-eye phototransduction components and their potential evolutionary implications. Science 311, 1617-1621.
59. Takahashi, Y. and Ebrey, T. G. (2003). Molecular basis of spectral tuning in the newt short wavelength sensitive visual pigment. Biochemistry 42, 6025-6034.
60. Terakita, A., Koyanagi, M., Tsukamoto, H., Yamashita, T., Miyata, T. and Shichida, Y. (2004). Counterion displacement in the molecular evolution of the rhodopsin family. Nat. Struct. Mol. Biol. 11, 284-289.
61. Vogt, K. and Kirschfeld, K. (1984). Chemical identity of the chromophores of fly visual pigment. Naturwissenschaften 71, 211-213.
62. Wasserman, G. S. (1969). Limulus receptor action spectra. Vis. Res. 9, 611-620.