Bistable UV pigment in the lamprey pineal

Abstract

Lower vertebrates can detect UV light with the pineal complex independently of eyes. Electrophysiological studies, together with chromophore extraction analysis, have suggested that the underlying pigment in the lamprey pineal exhibits a bistable nature, that is, reversible photoreaction by UV and visible light, which is never achieved by known UV pigments. Here we addressed the molecular identification of the pineal UV receptor. Our results showed that the long-hypothesized pigment is a lamprey homologue of parapinopsin, which exhibits an absorption maximum at 370 nm, in the UV region. UV light causes cis-trans isomerization of its retinal 2 chromophore, forming a stable photoproduct having an absorption maximum at 515 nm, in the green region. The photoproduct reverts to the original pigment upon visible light absorption, showing photoregeneration of the pigment. In situ hybridization showed that parapinopsin is selectively expressed in the cells located in the dorsal region of the pineal organ. We successfully obtained the hyperpolarizing responses with a maximum sensitivity of Ϸ380 nm from the photoreceptor cells at the dorsal region, in which the outer segment was clearly stained with anti-parapinopsin antibody. These results demonstrated that parapinopsin is the pineal UV pigment having photointerconvertible two stable states. The bistable nature of the parapinopsin can account for the photorecovery of the pineal UV sensitivity by background green light in the lamprey. Furthermore, we isolated the parapinopsin homologues from fish and frog pineal complexes that exhibit UV sensitivity, suggesting that parapinopsin is a common molecular basis for pineal UV reception in the vertebrate.

Evolution and diversity of opsins

“…27,35 Interestingly, parapinopsin, which is close to vertebrate bleaching visual pigments, exhibits a bistable nature and possesses a Glu181 counterion. 27,28 The difference in counterion position suggests that counterion displacement from Glu181 to Glu113 occurred during the molecular evolution of vertebrate visual pigments and promoted acquisition of the bleaching property. Counterion displacement resulted in two important amino acid residues, the new counterion Glu113 and the former counterion Glu181, each of which could potentially mediate the acquisition of new functional properties of vertebrate visual pigments as described below.…”

“…40 We investigated the lamprey pineal organ, in which parapinopsin-and rhodopsin-containing cells are located in the dorsal and ventral regions, respectively. 28,41 The spatial separation of the pigments allowed us to easily compare the parapinopsin and rhodopsin systems in the same organ. The results of immunohistochemical studies using antibodies against visual arrestin and transducin indicate that transducin or transducin-like G proteins localize to both parapinopsin-containing and rhodopsin-containing photoreceptor cells, whereas visual arrestin localizes only to rhodopsin-containing cells.…”

“…2,8,25,26 A vertebrate nonvisual pigment, parapinopsin, shows bistable characteristics, although the pigment is classified into the Gt-coupled opsin group, which contains vertebrate visual pigments with 'bleaching property' (the photoproduct of vertebrate visual pigments releases its retinal chromophore and bleaches; Figure 1(c)). 27,28 A cnidarian opsin-based pigment (the jellyfish pigment) is converted to a stable photoproduct that does not revert to its original dark state by subsequent light irradiation, unlike typical bistable pigments. 3 These photoproduct properties imply that bleaching pigments evolved from a nonbleaching opsin-based pigment, possibly a bistable pigment, although it is unclear whether the members of the encephalopsin/TMT-opsin group are bistable in nature.…”

Evolution and the origin of the visual retinoid cycle in vertebrates

“…Another mode of visual cycle in the pineal organ is the photoregeneration of parapinopsin in lamprey (Koyanagi et al 2004). The lamprey parapinopsin is the bistable UV pigment that exhibits an absorption maximum at 370 nm.…”

“…The photoproduct reverts to the original pigment upon visible light absorption, showing photoregeneration of the pigment. The bistable nature of the parapinopsin can account for the photorecovery of the pineal UV sensitivity by background green light in the lamprey (Koyanagi et al 2004). …”