Diversification of non-visual photopigment parapinopsin in spectral sensitivity for diverse pineal functions

BMC Biology

Volumn 13, Issue 1, 2015, Pages

  Koyanagi, Mitsumasa ^a,b   Wada, Seiji ^a,c   Kawano Yamashita, Emi ^a   Hara, Yuichiro ^d   Kuraku, Shigehiro ^d   Kosaka, Shigeaki ^a   Kawakami, Koichi ^e   Tamotsu, Satoshi ^c   Tsukamoto, Hisao ^a   Shichida, Yoshinori ^f   Terakita, Akihisa ^a  

^a Osaka City University   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c NARA WOMEN'S UNIVERSITY   (Japan)

^d RIKEN   (Japan)

^e GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^f KYOTO UNIVERSITY   (Japan)

Author keywords

Animal photoreception; Color vision; Gene duplication; Rhodopsin; Spectral tuning; UV sensitive pigment

Indexed keywords

FISH PROTEIN; SCOTOPSIN;

ANIMAL; COLOR VISION; EVOLUTION; GENETICS; METABOLISM; ONCORHYNCHUS MYKISS; PHYSIOLOGY; PINEAL BODY; TETRAODONTIFORMES; TRANSGENIC ANIMAL; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BIOLOGICAL EVOLUTION; COLOR VISION; FISH PROTEINS; ONCORHYNCHUS MYKISS; PINEAL GLAND; ROD OPSINS; TETRAODONTIFORMES; ZEBRAFISH;

EID: 84942193283     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/s12915-015-0174-9     Document Type: Article

References (64)

1. Nathans J, Thomas D, Hogness DS. Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. Science. 1986;232:193-202.
2. Okano T, Kojima D, Fukada Y, Shichida Y, Yoshizawa T. Primary structures of chicken cone visual pigments: vertebrate rhodopsins have evolved out of cone visual pigments. Proc Natl Acad Sci U S A. 1992;89:5932-6.
3. Nagata T, Koyanagi M, Tsukamoto H, Saeki S, Isono K, Shichida Y, et al. Depth perception from image defocus in a jumping spider. Science. 2012;335:469-71.
4. Peirson SN, Halford S, Foster RG. The evolution of irradiance detection: melanopsin and the non-visual opsins. Philos Trans R Soc Lond B Biol Sci. 2009;364:2849-65.
5. Do MT, Yau KW. Intrinsically photosensitive retinal ganglion cells. Physiol Rev. 2010;90:1547-81.
6. Lucas RJ. Mammalian inner retinal photoreception. Curr Biol. 2013;23:R125-33.
7. Terakita A, Nagata T. Functional properties of opsins and their contribution to light-sensing physiology. Zoolog Sci. 2014;31:653-9.
8. Bellingham J, Chaurasia SS, Melyan Z, Liu C, Cameron MA, Tarttelin EE, et al. Evolution of melanopsin photoreceptors: discovery and characterization of a new melanopsin in nonmammalian vertebrates. PLoS Biol. 2006;4:e254.
9. Matos-Cruz V, Blasic J, Nickle B, Robinson PR, Hattar S, Halpern ME. Unexpected diversity and photoperiod dependence of the zebrafish melanopsin system. PLoS One. 2011;6:e25111.
10. Davies WI, Zheng L, Hughes S, Tamai TK, Turton M, Halford S, et al. Functional diversity of melanopsins and their global expression in the teleost retina. Cell Mol Life Sci. 2011;68:4115-32.
11. Kojima D, Torii M, Fukada Y, Dowling JE. Differential expression of duplicated VAL-opsin genes in the developing zebrafish. J Neurochem. 2008;104:1364-71.
12. Hang CY, Kitahashi T, Parhar IS. Brain area-specific diurnal and photic regulation of val-opsinA and val-opsinB genes in the zebrafish. J Neurochem. 2015;133:501-10.
13. Zhdanova IV. Sleep and its regulation in zebrafish. Rev Neurosci. 2011;22:27-36.
14. Elbaz I, Foulkes NS, Gothilf Y, Appelbaum L. Circadian clocks, rhythmic synaptic plasticity and the sleep-wake cycle in zebrafish. Front Neural Circuits. 2013;7:9.
15. Oksche A. Evolution of the pineal complex: correlation of structure and function. Ophthalmic Res. 1984;16:88-95.
16. Okano T, Yoshizawa T, Fukada Y. Pinopsin is a chicken pineal photoreceptive molecule. Nature. 1994;372:94-7.
17. Max M, McKinnon PJ, Seidenman KJ, Barrett RK, Applebury ML, Takahashi JS, et al. Pineal opsin: a nonvisual opsin expressed in chick pineal. Science. 1995;267:1502-6.
18. Taniguchi Y, Hisatomi O, Yoshida M, Tokunaga F. Pinopsin expressed in the retinal photoreceptors of a diurnal gecko. FEBS Lett. 2001;496:69-74.
19. Frigato E, Vallone D, Bertolucci C, Foulkes NS. Isolation and characterization of melanopsin and pinopsin expression within photoreceptive sites of reptiles. Naturwissenschaften. 2006;93:379-85.
20. Deguchi T. Rhodopsin-like photosensitivity of isolated chicken pineal gland. Nature. 1981;290:706-7.
21. Okano T, Takanaka Y, Nakamura A, Hirunagi K, Adachi A, Ebihara S, et al. Immunocytochemical identification of pinopsin in pineal glands of chicken and pigeon. Brain Res Mol Brain Res. 1997;50:190-6.
22. Blackshaw S, Snyder SH. Parapinopsin, a novel catfish opsin localized to the parapineal organ, defines a new gene family. J Neurosci. 1997;17:8083-92.
23. Koyanagi M, Kawano E, Kinugawa Y, Oishi T, Shichida Y, Tamotsu S, et al. Bistable UV pigment in the lamprey pineal. Proc Natl Acad Sci U S A. 2004;101:6687-91.
24. Mano H, Kojima D, Fukada Y. Exo-rhodopsin: a novel rhodopsin expressed in the zebrafish pineal gland. Brain Res Mol Brain Res. 1999;73:110-8.
25. Su CY, Luo DG, Terakita A, Shichida Y, Liao HW, Kazmi MA, et al. Parietal-eye phototransduction components and their potential evolutionary implications. Science. 2006;311:1617-21.
26. Wada S, Kawano-Yamashita E, Koyanagi M, Terakita A. Expression of UV-sensitive parapinopsin in the iguana parietal eyes and its implication in UV-sensitivity in vertebrate pineal-related organs. PLoS One. 2012;7:e39003.
27. Dodt E, Meissl H. The pineal and parietal organs of lower vertebrates. Experientia. 1982;38:996-1000.
28. Morita Y, Dodt E. Slow Photic Responses of the Isolated Pineal Organ of Lamprey. Nova Acta Leopoldina. 1973;38:331-9.
29. Morita Y. Lead pattern of the pineal neuron of the rainbow trout (Salmo irideus) by illumination of the diencephalon. Pflugers Arch. 1966;289:155-67.
30. Falcon J, Meissl H. The photosensory function of the pineal organ of the pike (Esox lucius L.). Correlation between structure and function. J Comp Physiol A. 1981;144:127-37.
31. Dodt E, Heerd E. Mode of action of pineal nerve fibers in frogs. J Neurophysiol. 1962;25:405-29.
32. Korf HW, Liesner R, Meissl H, Kirk A. Pineal complex of the clawed toad, Xenopus laevis Daud.: structure and function. Cell Tissue Res. 1981;216:113-30.
33. Jenison G, Nolte J. An ultraviolet-sensitive mechanism in the reptilian parietal eye. Brain Res. 1980;194:506-10.
34. Nakane Y, Ikegami K, Iigo M, Ono H, Takeda K, Takahashi D, et al. The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nat Commun. 2013;4:2108.
35. Taylor JS, Braasch I, Frickey T, Meyer A, Van de Peer Y. Genome duplication, a trait shared by 22000 species of ray-finned fish. Genome Res. 2003;13:382-90.
36. Kuraku S, Meyer A. The evolution and maintenance of Hox gene clusters in vertebrates and the teleost-specific genome duplication. Int J Dev Biol. 2009;53:765-73.
37. Hoegg S, Brinkmann H, Taylor JS, Meyer A. Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol. 2004;59:190-203.
38. Crow KD, Stadler PF, Lynch VJ, Amemiya C, Wagner GP. The "fish-specific" Hox cluster duplication is coincident with the origin of teleosts. Mol Biol Evol. 2006;23:121-36.
39. Terakita A, Koyanagi M, Tsukamoto H, Yamashita T, Miyata T, Shichida Y. Counterion displacement in the molecular evolution of the rhodopsin family. Nat Struct Mol Biol. 2004;11:284-9.
40. Underwood H. Pineal melatonin rhythms in the lizard Anolis carolinensis: effects of light and temperature cycles. J Comp Physiol A. 1985;157:57-65.
41. Gern WA, Greenhouse SS. Examination of in vitro melatonin secretion from superfused trout (Salmo gairdneri) pineal organs maintained under diel illumination or continuous darkness. Gen Comp Endocrinol. 1988;71:163-74.
42. Falcon J, Marmillon JB, Claustrat B, Collin JP. Regulation of melatonin secretion in a photoreceptive pineal organ: an in vitro study in the pike. J Neurosci. 1989;9:1943-50.
43. Samejima M, Tamotsu S, Uchida K, Moriguchi Y, Morita Y. Melatonin excretion rhythms in the cultured pineal organ of the lamprey, Lampetra japonica. Biol Signals. 1997;6:241-6.
44. Samejima M, Shavali S, Tamotsu S, Uchida K, Morita Y, Fukuda A. Light- and temperature-dependence of the melatonin secretion rhythm in the pineal organ of the lamprey, Lampetra japonica. Jpn J Physiol. 2000;50:437-42.
45. Tamotsu S, Oishi T, Nakao K, Fukada Y, Shichida Y, Yoshizawa T, et al. Localization of Iodopsin and Rod-Opsin Immunoreactivity in the Retina and Pineal Complex of the River Lamprey, Lampetra-Japonica. Cell Tissue Res. 1994;278:1-10.
46. Shi Y, Yokoyama S. Molecular analysis of the evolutionary significance of ultraviolet vision in vertebrates. Proc Natl Acad Sci U S A. 2003;100:8308-13.
47. Yokoyama S, Starmer WT, Takahashi Y, Tada T. Tertiary structure and spectral tuning of UV and violet pigments in vertebrates. Gene. 2006;365:95-103.
48. Salcedo E, Zheng L, Phistry M, Bagg EE, Britt SG. Molecular basis for ultraviolet vision in invertebrates. J Neurosci. 2003;23:10873-8.
49. Ziv L, Tovin A, Strasser D, Gothilf Y. Spectral sensitivity of melatonin suppression in the zebrafish pineal gland. Exp Eye Res. 2007;84:92-9.
50. Koyanagi M, Nagata T, Katoh K, Yamashita S, Tokunaga F. Molecular evolution of arthropod color vision deduced from multiple opsin genes of jumping spiders. J Mol Evol. 2008;66:130-7.
51. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772-80.
52. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972-3.
53. Lartillot N, Lepage T, Blanquart S. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics. 2009;25:2286-8.
54. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312-3.
55. Louis A, Nguyen NT, Muffato M, Roest Crollius H. Genomicus update 2015: KaryoView and MatrixView provide a genome-wide perspective to multispecies comparative genomics. Nucleic Acids Res. 2015;43:D682-9.
56. Kuraku S, Zmasek CM, Nishimura O, Katoh K. aLeaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Res. 2013;41:W22-8.
57. Koyanagi M, Takada E, Nagata T, Tsukamoto H, Terakita A. Homologs of vertebrate Opn3 potentially serve as a light sensor in nonphotoreceptive tissue. Proc Natl Acad Sci U S A. 2013;110:4998-5003.
58. Chinen A, Hamaoka T, Yamada Y, Kawamura S. Gene duplication and spectral diversification of cone visual pigments of zebrafish. Genetics. 2003;163:663-75.
59. Koyanagi M, Takano K, Tsukamoto H, Ohtsu K, Tokunaga F, Terakita A. Jellyfish vision starts with cAMP signaling mediated by opsin-G(s) cascade. Proc Natl Acad Sci U S A. 2008;105:15576-80.
60. Gothilf Y, Toyama R, Coon SL, Du SJ, Dawid IB, Klein DC. Pineal-specific expression of green fluorescent protein under the control of the serotonin-N-acetyltransferase gene regulatory regions in transgenic zebrafish. Dev Dyn. 2002;225:241-9.
61. Urasaki A, Morvan G, Kawakami K. Functional dissection of the Tol2 transposable element identified the minimal cis-sequence and a highly repetitive sequence in the subterminal region essential for transposition. Genetics. 2006;174:639-49.
62. Asakawa K, Suster ML, Mizusawa K, Nagayoshi S, Kotani T, Urasaki A, et al. Genetic dissection of neural circuits by Tol2 transposon-mediated Gal4 gene and enhancer trapping in zebrafish. Proc Natl Acad Sci U S A. 2008;105:1255-60.
63. Tsujimura T, Hosoya T, Kawamura S. A single enhancer regulating the differential expression of duplicated red-sensitive opsin genes in zebrafish. PLoS Genet. 2010;6, e1001245.
64. Koyanagi M, Kubokawa K, Tsukamoto H, Shichida Y, Terakita A. Cephalochordate melanopsin: evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Curr Biol. 2005;15:1065-9.