Expression of proteins supporting visual function in heterobranch gastropods.

Ryota Matsuo, Haeri Kwon, Kiyotaka Takishita, Takako Nishi, Yuko Matsuo
Author Information
  1. Ryota Matsuo: Department of Environmental Sciences, International College of Arts and Sciences, Laboratory of Neurobiology, Fukuoka Women's University, 1-1-1 Kasumigaoka, Higashi-Ku, Fukuoka, 813-8529, Japan. matsuor@fwu.ac.jp.
  2. Haeri Kwon: Department of Environmental Sciences, International College of Arts and Sciences, Laboratory of Neurobiology, Fukuoka Women's University, 1-1-1 Kasumigaoka, Higashi-Ku, Fukuoka, 813-8529, Japan.
  3. Kiyotaka Takishita: Department of Environmental Sciences, International College of Arts and Sciences, Laboratory of Neurobiology, Fukuoka Women's University, 1-1-1 Kasumigaoka, Higashi-Ku, Fukuoka, 813-8529, Japan.
  4. Takako Nishi: Institute of Natural Sciences, Senshu University, Kawasaki, Japan.
  5. Yuko Matsuo: Department of Environmental Sciences, International College of Arts and Sciences, Laboratory of Neurobiology, Fukuoka Women's University, 1-1-1 Kasumigaoka, Higashi-Ku, Fukuoka, 813-8529, Japan.

Abstract

To sense light, animals often utilize mechanisms that rely on visual pigments composed of opsin and retinal. The photon-induced isomerization of 11-cis-retinal to the all-trans configuration triggers phototransduction cascades, resulting in a change in the membrane potential of the photoreceptor. In mollusks, the most abundant opsin in the eye is Gq-coupled rhodopsin (Gq-rhodopsin). The Gq-rhodopsin-based visual pigment is bistable, with the regeneration of 11-cis-retinal occurring in a light-dependent manner without leaving the opsin moiety. 11-cis-retinal is also regenerated by the action of retinochrome in the cell bodies. Retinal binding protein (RALBP) mediates retinal transport between Gq-rhodopsin and retinochrome in the cytoplasm. However, recent studies have identified additional bistable opsins in mollusks, including Opn5 and xenopsin. It is unknown whether these bistable opsins require RALBP and retinochrome for the continuous regeneration of 11-cis-retinal. In the present study, we examined the expression of RALBP and retinochrome in the photoreceptors expressing Opn5 or Xenopsin in the heterobranch gastropods Limax and Peronia. Our findings revealed that retinochrome, but not RALBP, was present in some of the Opn5A-positive brain photosensory neurons of Limax. The ciliary cells in the dorsal eye of Peronia, which express Xenopsin2, lacked both retinochrome and RALBP. Therefore, bistable opsins do not necessarily depend on the RALBP-retinochrome system in a cell. We also examined the expression of other proteins that support visual function, such as β-arrestin, Gq, and Go, in all types of photoreceptors in these animals, and uncovered differences in the molecular composition among the photoreceptors.

Keywords

References

Alvarez CE (2008) On the origins of arrestin and rhodopsin. BMC Ecol Evol 8:222
Bodington A (1890) Studies in evolution and biology. Elliot Stock, London
Brandenburger JL (1975) Two new kinds of retinal cells in the eye of a snail, Helix aspersa. J Ultrast Res 50:216–230
Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973 [PMID: 19505945]
Choi EH, Daruwalla A, Suh S, Leinone H, Palczewski K (2021) Retinoids in the visual cycle: role of the retinal G protein-coupled receptor. J Lipid Res 62:100040 [PMID: 32493732]
Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159 [PMID: 2440339]
Crozier WJ, Arey LB (1919) The heliotropism of Onchidium: a problem in the analysis of animal conduct. J Gen Physiol 2:107–112 [PMID: 19871793]
de Hoog E, Lukewich MK, Spencer GE (2019) Retinoid receptor-based signaling plays a role in voltage-dependent inhibition of invertebrate voltage-gated Ca channels. J Biol Chem 294:10076–10093 [PMID: 31048374]
Defoe DM, Bok D (1983) Rhodopsin chromophore exchanges among opsin molecules in the dark. Invest Ophthalmol vis Sci 24:1211–1226 [PMID: 6224755]
DeWire SM, Ahn S, Lefkowitz RJ, Shenoy SK (2007) β-arrestin and cell signaling. Annu Rev Physiol 69:483–510 [PMID: 17305471]
Döring CC, Kumar S, Tumu SC, Kourtesis I, Hausen H (2020) The visual pigment xenopsin is widespread in protostome eyes and impacts the view on eye evolution. eLife 9:e55193 [PMID: 32880369]
Doyle SE, Castrucci AM, McCall M, Provencio I, Menaker M (2006) Nonvisual light responses in the Rpe65 knockout mouse: rod loss restores sensitivity to the melanopsin system. Proc Natl Acad Sci USA 103:10432–10437 [PMID: 16788070]
Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 5:113
Fukunaga S, Matsuo R, Hoshino S, Kirino Y (2006) Novel kruppel-like factor is induced by neuronal activity and by sensory input in the central nervous system of the terrestrial slug Limax valentianus. J Neurobiol 66:169–181 [PMID: 16288475]
Gomez MP, Espinosa L, Ramirez N, Nasi E (2011) Arrestin in ciliary invertebrate photoreceptors: molecular identification and functional analysis in vivo. J Neurosci 31:1811–1819 [PMID: 21289191]
Hara T, Hara R (1967) Rhodopsin and retinochrome in the squid retina. Nature 214:573–575 [PMID: 6036171]
Hara T, Hara R (1973) Isomerization of retinal catalysed by retinochrome in the light. Nature 242:39–43
Hara T, Hara R (1980) Retinochrome and rhodopsin in the extraocular photoreceptor of squid, Todarodes. J Gen Physiol 75:1–19 [PMID: 7359116]
Harrison KR, Reifler AN, Chervenak AP, Wong KY (2021) Prolonged melanopsin-based photoresponses depend in part on RPE65 and cellular retinaldehyde-binding protein (CRALBP). Curr Eye Res 46:515–523 [PMID: 32841098]
Katagiri N (1984) Cytoplasmic characteristics of three different rhabdomeric photoreceptor cells in a marine gastropod, Onchidium verruculatum. Microscopy 33:142–150
Katagiri Y, Katagiri N, Fujimoto K (1985) Morphological and electrophysiological studies of a multiple photoreceptive system in a marine gastropod, Onchidium. Neurosi Res Supple 2:S1–S15
Katagiri N, Terakita A, Shichida Y, Katagiri Y (2001) Demonstration of a rhodopsin-retinochrome system in the stalk eye of a marine gastropod, Onchidium, by immunohistochemistry. J Comp Neurol 433:380–389 [PMID: 11298362]
Katagiri N, Suzuki T, Shimatani Y, Katagiri Y (2002) Localization of retinal proteins in the stalk and dorsal eyes of the marine gastropod, Onchidium. Zool Sci 19:1231–1240
Kataoka S (1975) Fine structure of the retina of a slug, Limax flavus L. Vsion Res 15:681–686
Kataoka S (1977) Ultrastructure of the cornea and accessory retina in a slug, Limax flavus L. J Ultrast Res 60:296–305
Kojima D, Mori S, Torii M, Wada A, Morishita R, Fukada Y (2011) UV-sensitive photoreceptor protein Opn5 in humans and mice. PLoS ONE 6:e26388 [PMID: 22043319]
Kono N, Arai H (2015) Intracellular transport of fat-soluble vitamins A and E. Traffic 16:19–34 [PMID: 25262571]
Koyanagi M, Terakita A (2014) Diversity of animal opsin-based pigments and their optogenetic potential. Biochim Biophys Acta 1837:710–716 [PMID: 24041647]
Maden M (2002) Retinoid signaling in the development of the central nervous system. Nat Rev Neurosci 3:843–853 [PMID: 12415292]
Manor D, Morley S (2007) The alpha-tocopherol transfer protein. Vitam Horm 76:45–65 [PMID: 17628171]
Matsumoto H, Tokunaga F, Yoshizawa T (1975) Accessibility of the iodopsin chromophore. Biochim Biophys Acta 404:300–308 [PMID: 1182163]
Matsuo R, Matsuo Y (2022) Regional expression of neuropeptides in the retina of the terrestrial slug Limax valentianus (Gastropoda, Stylommatophora, Limacidae). J Comp Neurol 530:1551–1568 [PMID: 34979594]
Matsuo R, Asada A, Fujitani K, Inokuchi K (2001) LIRF, a gene induced during hippocampal long-term potentiation as an immediate-early gene, encodes a novel RING finger protein. Biochem Biophys Res Commun 289:479–484 [PMID: 11716498]
Matsuo Y, Uozumi N, Matsuo R (2014) Photo-tropotaxis based on projection through the cerebral commissure in the terrestrial slug Limax. J Comp Physiol A 200:1023–1032
Matsuo R, Takatori Y, Hamada S, Koyanagi M, Matsuo Y (2017) Expression and light-dependent translocation of β–arrestin in the visual system of the terrestrial slug Limax valentianus. J Exp Biol 220:3301–3314 [PMID: 28687596]
Matsuo Y, Yamanaka A, Matsuo R (2018) RFamidergic neurons in the olfactory centers of the terrestrial slug Limax. Zoological Lett 4:22 [PMID: 30116553]
Matsuo R, Koyanagi M, Nagata A, Matsuo Y (2019) Co-expression of opsins in the eye photoreceptor cells of the terrestrial slug Limax valentianus. J Comp Neurol 527:3073–3086 [PMID: 31226228]
Matsuo Y, Nishiyama H, Matsuo R (2020) Integration of ocular and non-ocular photosensory information in the brain of the terrestrial slug Limax. J Comp Physiol A 206:907–919
Matsuo R, Kotoh S, Takishita K, Sakamoto K, Uebi T, Ozaki M, Matsuo Y, Nishi T (2022) Opsins in the cephalic and extracephalic photoreceptors in the marine gastropod Onchidium verruculatum. Biol Bull 243:339–352 [PMID: 36716483]
Matsuo R, Koyanagi M, Sugihara T, Shirata T, Nagata T, Inoue K, Matsuo Y, Terakita A (2023) Functional characterization of four opsins and two G alpha subtypes co-expressed in the molluscan rhabdomeric photoreceptor. BMC Biol 21:291 [PMID: 38110917]
Matsuo Y, Kawakami A, Matsuo R (2024) Visual afferents from an eye in the terrestrial slug Limax valentianus. J Comp Neurol 532:e25600 [PMID: 38433660]
McCrohan CR, Benjamin PR (1980) Synaptic relationships of the cerebral giant cells with motoneurons in the feeding system of Lymnaea stagnalis. J Exp Biol 85:169–186 [PMID: 6246187]
Minh BQ, Nguyen MA, von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30:1188–1195 [PMID: 23418397]
Moiseyev G, Chen Y, Takahashi Y, Wu BX, Ma J (2005) RPE65 is the isomerohydrolase in the retinoid visual cycle. Proc Natl Acad Sci USA 102:12413–12418 [PMID: 16116091]
Molina TM, Torres SC, Flores A, Hara T, Hara R, Robles LJ (1992) Immunocytochemical localization of retinal binding protein in the octopus retina: a shuttle protein for 11-cis retinal. Exp Eye Res 54:83–90 [PMID: 1541344]
Nakashima Y, Kusakabe T, Kusakabe R, Terakita A, Shichida Y, Tsuda M (2003) Origin of the vertebrate visual cycle: Genes encoding retinal photoisomerase and two putativevisual cycle proteins are expressed in whole brain of a primitive chordate. J Comp Neurol 460:180–190 [PMID: 12687683]
Nguyen LT, Schmidt HA, von Haeseler A, Minh BG (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274 [PMID: 25371430]
Nishiyama H, Nagata A, Matsuo Y, Matsuo R (2019) Light avoidance by a non-ocular photosensing system in the terrestrial slug Limax velantianus. J Exp Biol 222:jeb208595 [PMID: 31266779]
Nobes C, Baverstock J, Saibil H (1992) Activation of the GTP-binding protein Gq by rhodopsin in squid photoreceptors. Biochem J 287:545–548 [PMID: 1445212]
Ozaki K, Hara R, Hara T (1983) Histochemical localization of retinochrome and rhodopsin studied by fluorescence microscopy. Cell Tissue Res 233:335–345 [PMID: 6616571]
Ozaki K, Terakita A, Hara R, Hara T (1987) Isolation and characterization of a retinal-binding protein from the squid retina. Vision Res 27:1057–1070 [PMID: 3660660]
Ozaki K, Terakita A, Ozaki M, Hara R, Hara T, Hara-Nishimura I, Mori H, Nishimura M (1994) Molecular characterization and functional expression of squid retinal-binding protein. a novel species of hydrophobic ligand-binding protein. J Biol Chem 269:3838–3845 [PMID: 8106428]
Palczewski K, Kiser PD (2020) Shedding new light on the generation of the visual chromophore. Proc Natl Acad Sci USA 117:19629–19638 [PMID: 32759209]
Panagabko C, Morley S, Hernandez M, Cassolato P, Gordon H, Parsons R, Manor D, Atkinson J (2003) Ligand specificity in the CRAL-TRIO protein family. Biochemistry 42:6467–6474 [PMID: 12767229]
Robles LJ, Watanabe A, Kremer NE, Wong F, Bok D (1987) Immunocytochemical localization of photopigments in cephalopod retinae. J Neurocytol 16:403–415 [PMID: 2956369]
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574 [PMID: 12912839]
Saito K, Tautz L, Mustelin T (2007) The lipid-binding SEC14 domain. Biochim Biophys Acta 1771:719–726 [PMID: 17428729]
Samarawickrama C, Chew S, Watson S (2015) Retinoic acid and the ocular surface. Surv Ophthalmol 60:183–195 [PMID: 25890622]
Shen D, Jiang M, Hao W, Tao L, Salazar M, Fong HKW (1994) A human opsin-related gene that encodes a retinaldehyde-binding protein. Biochemistry 33:13117–13125 [PMID: 7947717]
Shichiri M, Kono N, Shimanaka Y, Tanito M, Rotzoll DE, Yoshida Y, Hagihira Y, Tamai H, Arai H (2012) A novel role for α-tochopherol transfer protein (α-TTP) in protecting against chloroquine toxicity. J Biol Chem 287:2926–2934 [PMID: 22147702]
Smith G, Briscoe A (2015) Molecular evolution and expression of the CRAL-TRIO protein family in insects. Insect Biochem Mol Biol 62:168–173 [PMID: 25684408]
Terakita A, Hara R, Hara T (1989) Retinal-binding protein as a shuttle for retinal in the rhodopsin-retinochrome system of the squid visual cells. Vision Res 29:639–652 [PMID: 2626821]
Tsuda M, Kusakabe T, Iwamoto H, Horie T, Nakashima Y, Nakagawa M, Okunou K (2003) Origin of the vertebrate visual cycle: II. Visual cycle proteins are localized in whole brain including photoreceptor cells of a primitive chordate. Vision Res 43:3045–3053 [PMID: 14611940]
Tu DC, Owens LA, Anderson L, Golczak M, Doyle SE, McCall M, Menaker M, Palczewski K, Van Gelder R (2006) Inner retinal photoreception independent of the visual retinoid cycle. Proc Natl Acad Sci USA 103:10426–10431 [PMID: 16788071]
Tworak A, Kolesnikov AV, Hong JD, Choi EH, Luu JC, Palczewska G, Dong Z, Lewandowski D, Brooks MJ, Campello L, Swaroop A, Kiser PD, Kefalov VJ, Palczewski K (2023) Rapid RGR-dependent visual pigment recycling is mediated by the RPE and specialized Müller glia. Cell Rep 42:112982 [PMID: 37585292]
Vesprini ND, Dawson TF, Yuan Y, Bruce D, Spencer GE (2015) Retinoic acid affects calcium signaling in adult molluscan neurons. J Neurophysiol 113:172–181 [PMID: 25343782]
Vöcking O, Leclère L, Hausen H (2021) The rhodopsin-retinochrome system for retinal re-isomerization predates the origin of cephalopod eyes. BMC Ecol Evol 21:215 [PMID: 34844573]
Vöcking O, Kourtesis I, Tumu SC, Hausen H (2017) Co-expression of xenopsin and rhabdomeric opsin in photoreceptors bearing microvilli and cilia. eLife 6:e23435 [PMID: 28876222]
von Lintig J, Moon J, Babino D (2021) Molecular components affecting carotenoid and retinoid homeostasis. Prog Retin Eye Res 80:100864
Weir J (1899) The dawn of reason. Macmillan, London
Wignrove J, de Hoog E, Spencer GE (2023) Disruptions in network plasticity precede deficits in memory following inhibition of retinoid signaling. J Neurophysiol 129:41–55
Yamashita T, Ohuchi H, Tomonari S, Ikeda K, Sakai K, Shichida Y (2010) Opn5 is a UV-sensitive bistable pigment that couples with Gi subtype of G protein. Proc Natl Acad Sci USA 107:22084–22089 [PMID: 21135214]
Yanase T, Okuno Y, Uchida H (1981) Electrophysiological studies on the visual cell and lens cell of dorsal eye in Onchidium verruculatum. Mem Osaka Kyoiku Univ Ser III 29:121–126
Yeoman MS, Brierley MJ, Benjamin PR (1996) Central pattern generator interneurons are targets for the modulatory serotonergic cerebral giant cells in the feeding system of Lymnaea. J Neurophysiol 75:11–25 [PMID: 8822538]
Yoshida MA, Ogura A, Ikeo K, Shigeno S, Moritaki T, Winters GC, Kohn AB, Moroz LL (2015) Molecular evidence for convergence and parallelism in evolution of complex brains of cephalopod molluscs: insights from visual systems. Integr Comp Biol 55:1070–1083 [PMID: 26002349]
Zhang J, Choi EH, Tworak A, Salom D, Leinonen H, Sander CL, Hoang TV, Handa JT, Blackshaw S, Palczewska G, Kiser PD, Palczewski K (2019) Photic generation of 11-cis-retinal in bovine retinal pigment epithelium. J Biol Chem 294:19137–19154 [PMID: 31694912]
Zhang Y, Mao F, Mu H, Huang M, Bao Y, Wang L, Wong NK, Xiao S, Dai H, Xiang Z, Ma M, Xiong Y, Zhang Z, Zhang L, Song X, Wang F, Mu X, Li J, Ma H, Zhang Y, Zheng H, Simakov O, Yu Z (2021) The genome of Nautilus pompilius illuminates eye evolution and biomineralization. Nat Ecol Evol 5:927–938 [PMID: 33972735]
Zieger MV, Meyer-Rochow VB (2008) Understanding the cephalic eyes of pulmonate gastropods: a review. Am Malacol Bull 26:47–66

MeSH Term

Animals
Photoreceptor Cells, Invertebrate
Vision, Ocular
Gastropoda
Opsins

Chemicals

Opsins

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