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Cephalochordate Melanopsin: Evolutionary Linkage between Invertebrate Visual Cells and Vertebrate Photosensitive Retinal Ganglion Cells

2005; Elsevier BV; Volume: 15; Issue: 11 Linguagem: Inglês

10.1016/j.cub.2005.04.063

1879-0445

Mitsumasa Koyanagi, Kaoru Kubokawa, Hisao Tsukamoto, Yoshinori Shichida, Akihisa Terakita,

Neurobiology and Insect Physiology Research

Animal photoreceptor cells can be classified into two distinct types, depending on whether the photopigment is borne on the membrane of a modified cilium (ciliary type) or apical microvilli (rhabdomeric type) [1Eakin R.M. Evolution of photoreceptors.Cold Spring Harb. Symp. Quant. Biol. 1965; 30: 363-370Crossref PubMed Scopus (82) Google Scholar]. Ciliary photoreceptors are well known as vertebrate rods and cones and are also found in several invertebrates. The rhabdomeric photoreceptor, in contrast, is a predominant type of invertebrate visual cell, but morphologically identifiable rhabdomeric photoreceptors have never been found in vertebrates. It is hypothesized that the rhabdomeric photoreceptor cell had evolved to be the photosensitive retinal ganglion cell for the vertebrate circadian photoentrainment [2Lucas R.J. Douglas R.H. Foster R.G. Characterization of an ocular photopigment capable of driving pupillary constriction in mice.Nat. Neurosci. 2001; 4: 621-626Crossref PubMed Scopus (471) Google Scholar, 3Panda S. Provencio I. Tu D.C. Pires S.S. Rollag M.D. Castrucci A.M. Pletcher M.T. Sato T.K. Wiltshire T. Andahazy M. et al.Melanopsin is required for non-image-forming photic responses in blind mice.Science. 2003; 301: 525-527Crossref PubMed Scopus (539) Google Scholar, 4Hattar S. Lucas R.J. Mrosovsky N. Thompson S. Douglas R.H. Hankins M.W. Lem J. Biel M. Hofmann F. Foster R.G. et al.Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice.Nature. 2003; 424: 76-81Crossref PubMed Scopus (877) Google Scholar] owing to the fact that some molecules involved in cell differentiation are common among them [5Arendt D. Evolution of eyes and photoreceptor cell types.Int. J. Dev. Biol. 2003; 47: 563-571PubMed Google Scholar]. We focused on the cephalochordate amphioxus because it is the closest living invertebrate to the vertebrates, and interestingly, it has rhabdomeric photoreceptor cells for putative nonvisual functions [6Lacalli T.C. Sensory systems in amphioxus: A window on the ancestral chordate condition.Brain Behav. Evol. 2004; 64: 148-162Crossref PubMed Scopus (112) Google Scholar]. Here, we show that the amphioxus homolog of melanopsin [7Provencio I. Jiang G. De Grip W.J. Hayes W.P. Rollag M.D. Melanopsin: An opsin in melanophores, brain, and eye.Proc. Natl. Acad. Sci. USA. 1998; 95: 340-345Crossref PubMed Scopus (703) Google Scholar, 8Provencio I. Rodriguez I.R. Jiang G. Hayes W.P. Moreira E.F. Rollag M.D. A novel human opsin in the inner retina.J. Neurosci. 2000; 20: 600-605Crossref PubMed Google Scholar, 9Bellingham J. Whitmore D. Philp A.R. Wells D.J. Foster R.G. Zebrafish melanopsin: Isolation, tissue localisation and phylogenetic position.Brain Res. Mol. Brain Res. 2002; 107: 128-136Crossref PubMed Scopus (85) Google Scholar], the circadian photopigment in the photosensitive retinal ganglion cells of vertebrates, is expressed in the rhabdomeric photoreceptor cells of the amphioxus and that its biochemical and photochemical properties, not just its primary structure, are considerably similar to those of the visual rhodopsins in the rhabdomeric photoreceptor cells of higher invertebrates. The cephalochordate rhabdomeric photoreceptor represents an evolutionary link between the invertebrate visual photoreceptor and the vertebrate circadian photoreceptor.