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Glial cells expressing visual cycle genes are vital for photoreceptor survival in the zebrafish pineal gland.

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  • معلومة اضافية
    • المصدر:
      Publisher: Wiley Country of Publication: England NLM ID: 8504412 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1600-079X (Electronic) Linking ISSN: 07423098 NLM ISO Abbreviation: J Pineal Res Subsets: MEDLINE
    • بيانات النشر:
      Publication: : Oxford : Wiley
      Original Publication: New York : Liss, c1984-
    • الموضوع:
    • نبذة مختصرة :
      Photoreceptors in the vertebrate eye are dependent on the retinal pigmented epithelium for a variety of functions including retinal re-isomerization and waste disposal. The light-sensitive pineal gland of fish, birds, and amphibians is evolutionarily related to the eye but lacks a pigmented epithelium. Thus, it is unclear how these functions are performed. Here, we ask whether a subpopulation of zebrafish pineal cells, which express glial markers and visual cycle genes, is involved in maintaining photoreceptors. Selective ablation of these cells leads to a loss of pineal photoreceptors. Moreover, these cells internalize exorhodopsin that is secreted by pineal rod-like photoreceptors, and in turn release CD63-positive extracellular vesicles (EVs) that are taken up by pdgfrb-positive phagocytic cells in the forebrain meninges. These results identify a subpopulation of glial cells that is critical for pineal photoreceptor survival and indicate the existence of cells in the forebrain meninges that receive EVs released by these pineal cells and potentially function in waste disposal.
      (© 2023 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.)
    • References:
      Chen P, Hao W, Rife L, et al. A photic visual cycle of rhodopsin regeneration is dependent on Rgr. Nat Genet. 2001;28:256-260.
      Moiseyev G, Chen Y, Takahashi Y, Wu BX, Ma J. RPE65 is the isomerohydrolase in the retinoid visual cycle. Proc Natl Acad Sci USA. 2005;102:12413-12418.
      Jacobson SG, Aleman TS, Cideciyan AV, et al. Human cone photoreceptor dependence on RPE65 isomerase. Proc Natl Acad Sci USA. 2007;104:15123-15128.
      Parker RO, Crouch RK. Retinol dehydrogenases (RDHs) in the visual cycle. Exp Eye Res. 2010;91:788-792.
      Organisciak DT, Vaughan DK. Retinal light damage: mechanisms and protection. Prog Retinal Eye Res. 2010;29:113-134.
      Kwon W, Freeman SA. Phagocytosis by the retinal pigment epithelium: recognition, resolution, recycling. Front Immunol. 2020;11:604205.
      Ropelewski P, Imanishi Y. RPE cells engulf microvesicles secreted by degenerating rod photoreceptors. eNeuro. 2020;7(3):ENEURO.0507-19.2020.
      Klingeborn M, Stamer WD, Bowes Rickman C. Polarized exosome release from the retinal pigmented epithelium. Adv Exp Med Biol. 2018;1074:539-544.
      Somasundaran S, Constable IJ, Mellough CB, Carvalho LS. Retinal pigment epithelium and age-related macular degeneration: a review of major disease mechanisms. Clin Exp Ophthalmol. 2020;48:1043-1056.
      Ekström P, Meissl H. Evolution of photosensory pineal organs in new light: the fate of neuroendocrine photoreceptors. Philos Trans R Soc Lond Ser B Biol Sci. 2003;358:1679-1700.
      Mano H, Fukada Y. A median third eye: pineal gland retraces evolution of vertebrate photoreceptive organs. Photochem Photobiol. 2007;83:11-18.
      Falcón J, Thibault C, Begay V, Zachmann A, Collin J-P. Regulation of the rhythmic melatonin secretion by fish pineal photoreceptor cells. In: Ali MA, ed. Rhythms in Fishes. Plenum Press; 1992:167-198.
      Li X, Montgomery J, Cheng W, Noh JH, Hyde DR, Li L. Pineal photoreceptor cells are required for maintaining the circadian rhythms of behavioral visual sensitivity in zebrafish. PLoS One. 2012;7:e40508.
      Breder CM, Rasquin P. A preliminary report on the role of the pineal organ in the control of pigment cells and light reactions in recent teleost fishes. Science. 1950;111:10-12.
      Gibson R, Burns JG, Rodd FH. Flexibility in the colouration of the meninx (brain covering) in the guppy (Poecilia reticulata): investigations of potential function. Can J Zool. 2009;87:529-536.
      Lamanna F, Hervas-Sotomayor F, Oel AP, et al. Reconstructing the ancestral vertebrate brain using a lamprey neural cell type atlas. Biorxiv. 2022:2022.02.28.482278.
      Bailey MJ, Beremand PD, Hammer R, Reidel E, Thomas TL, Cassone VM. Transcriptional profiling of circadian patterns of mRNA expression in the chick retina. J Biol Chem. 2004;279:52247-52254.
      Khuansuwan S, Gamse JT. Identification of differentially expressed genes during development of the zebrafish pineal complex using RNA sequencing. Dev Biol. 2014;395:144-153.
      Thisse C, Thisse B. High Throughput Expression Analysis of ZF-Models Consortium Clones. 2005.
      Toyama R, Chen X, Jhawar N, et al. Transcriptome analysis of the zebrafish pineal gland. Dev Dyn. 2009;238:1813-1826.
      Shainer I, Michel M, Marquart GD, et al. Agouti-related protein 2 is a new player in the teleost stress response system. Curr Biol. 2019;29:2009-2019.
      Braasch I, Postlethwait JH. The teleost agouti-related protein 2 gene is an ohnolog gone missing from the tetrapod genome. Proc Natl Acad Sci USA. 2011;108:E47-E48.
      Satija R, Farrell JA, Gennert D, Schier AF, Regev A. Spatial reconstruction of single-cell gene expression data. Nat Biotechnol. 2015;33:495-502.
      Tabor KM, Marquart GD, Hurt C, et al. Brain-wide cellular resolution imaging of Cre transgenic zebrafish lines for functional circuit-mapping. eLife. 2019;8:1-40.
      Gilmour DT, Maischein H-M, Nüsslein-Volhard C. Migration and function of a glial subtype in the vertebrate peripheral nervous system. Neuron. 2002;34:577-588.
      Shainer I, Buchshtab A, Hawkins TA, Wilson SW, Cone RD, Gothilf Y. Novel hypophysiotropic AgRP2 neurons and pineal cells revealed by BAC transgenesis in zebrafish. Sci Rep. 2017;7:44777.
      Davison JM, Akitake CM, Goll MG, et al. Transactivation from Gal4-VP16 transgenic insertions for tissue-specific cell labeling and ablation in zebrafish. Dev Biol. 2007;304:811-824.
      Ando K, Fukuhara S, Izumi N, et al. Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish. Development. 2016;143:1328-1339.
      Yong Wan W, Otsuna H, Chi-Bin chien C, Hansen C. An interactive visualization tool for multi-channel confocal microscopy data in neurobiology research. IEEE Trans Vis Comput Graph. 2009;15:1489-1496.
      Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9:676-682.
      Bolte S, Cordelières FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc. 2006;224:213-232.
      Ho J, Tumkaya T, Aryal S, Choi H, Claridge-Chang A. Moving beyond P values: data analysis with estimation graphics. Nat Methods. 2019;16:565-566.
      Calin-Jageman RJ, Cumming G. The new statistics for better science: ask how much, how uncertain, and what else is known. Am Stat. 2019;73:271-80.
      Lange C, Rost F, Machate A, et al. Single cell sequencing of radial glia progeny reveals the diversity of newborn neurons in the adult zebrafish brain. Development. 2020;147:dev185595.
      Roesch K, Jadhav AP, Trimarchi JM, et al. The transcriptome of retinal Müller glial cells. J Comp Neurol. 2008;509:225-238.
      Curado S, Anderson RM, Jungblut B, Mumm J, Schroeter E, Stainier DYR. Conditional targeted cell ablation in zebrafish: a new tool for regeneration studies. Dev Dyn. 2007;236:1025-1035.
      Ile KE, Kassen S, Cao C, et al. Zebrafish class 1 phosphatidylinositol transfer proteins: PITPβ and double cone cell outer segment integrity in retina. Traffic. 2010;11:1151-1167.
      Clanton JA, Hope KD, Gamse JT. Fgf signaling governs cell fate in the zebrafish pineal complex. Development. 2013;140:323-332.
      Noche RR, Lu P-N, Goldstein-Kral L, Glasgow E, Liang JO. Circadian rhythms in the pineal organ persist in zebrafish larvae that lack ventral brain. BMC Neurosci. 2011;12:7.
      Mano H, Kojima D, Fukada Y. Exo-rhodopsin: a novel rhodopsin expressed in the zebrafish pineal gland. Mol Brain Res. 1999;73:110-118.
      Pols MS, Klumperman J. Trafficking and function of the tetraspanin CD63. Exp Cell Res. 2009;315:1584-1592.
      Mathieu M, Névo N, Jouve M, et al. Specificities of exosome versus small ectosome secretion revealed by live intracellular tracking of CD63 and CD9. Nat Commun. 2021;12:4389.
      Jung HM, Castranova D, Swift MR, et al. Development of the larval lymphatic system in zebrafish. Development. 2017;144:2070-2081.
      Okuda KS, Astin JW, Misa JP, Flores MV, Crosier KE, Crosier PS. lyve1 expression reveals novel lymphatic vessels and new mechanisms for lymphatic vessel development in zebrafish. Development. 2012;139:2381-2391.
      Esposito R, Racioppi C, Pezzotti MR, et al. The ascidian pigmented sensory organs: structures and developmental programs. Genesis. 2015;53:15-33.
      Sharma S, Wang W, Stolfi A. Single-cell transcriptome profiling of the Ciona larval brain. Dev Biol. 2019;448:226-36.
      Takimoto N, Kusakabe T, Tsuda M. Origin of the vertebrate visual cycle. Photochem Photobiol. 2007;83:242-247.
      Sung C, Makino C, Baylor D, Nathans J. A rhodopsin gene mutation responsible for autosomal dominant retinitis pigmentosa results in a protein that is defective in localization to the photoreceptor outer segment. J Neurosci. 1994;14:5818-5833.
      Li T, Snyder WK, Olsson JE, Dryja TP. Transgenic mice carrying the dominant rhodopsin mutation P347S: evidence for defective vectorial transport of rhodopsin to the outer segments. Proc Natl Acad Sci USA. 1996;93:14176-14181.
      Steinberg RH. Interactions between the retinal pigment epithelium and the neural retina. Doc Ophthalmol. 1985;60:327-346.
      van Lessen M, Shibata-Germanos S, van Impel A, Hawkins TA, Rihel J, Schulte-Merker S. Intracellular uptake of macromolecules by brain lymphatic endothelial cells during zebrafish embryonic development. eLife. 2017;6:e25932.
      Castranova D, Samasa B, Venero Galanternik M, Jung HM, Pham VN, Weinstein BM. Live imaging of intracranial lymphatics in the zebrafish. Circ Res. 2021;128:42-58.
      Baba K, Goyal V, Tosini G. Circadian regulation of retinal pigment epithelium function. Int J Mol Sci. 2022;23:2699.
      LaVail MM. Rod outer segment disk shedding in rat retina: relationship to cyclic lighting. Science. 1976;194:1071-1074.
      DeVera C, Dixon J, Chrenek MA, et al. The circadian clock in the retinal pigment epithelium controls the diurnal rhythm of phagocytic activity. Int J Mol Sci. 2022;23:5302.
      Laurent V, Sengupta A, Sánchez-Bretaño A, Hicks D, Tosini G. Melatonin signaling affects the timing in the daily rhythm of phagocytic activity by the retinal pigment epithelium. Exp Eye Res. 2017;165:90-95.
      Goyal V, DeVera C, Laurent V, et al. Dopamine 2 receptor signaling controls the daily burst in phagocytic activity in the mouse retinal pigment epithelium. Investig Ophthalmol Visual Sci. 2020;61:10.
      Ben-Moshe Z, Foulkes NS, Gothilf Y. Functional development of the circadian clock in the zebrafish pineal gland. BioMed Res Int. 2014;2014:1-8.
      Boehmler W, Obrecht-Pflumio S, Canfield V, Thisse C, Thisse B, Levenson R. Evolution and expression of D2 and D3 dopamine receptor genes in zebrafish. Dev Dyn. 2004;230:481-493.
    • Grant Information:
      6276/17 Israel Science Foundation; NRF2017-NRF-ISF002-2676 National Research Foundation of Singapore; RG34/20 Singapore Ministry of Education
    • Contributed Indexing:
      Keywords: clearance; extracellular vesicles; glia; meninges; rhodopsin; visual cycle
    • الرقم المعرف:
      0 (exorhodopsin)
      JL5DK93RCL (Melatonin)
      9009-81-8 (Rhodopsin)
      0 (Tetraspanin 30)
      0 (exorh protein, zebrafish)
    • الموضوع:
      Date Created: 20230124 Date Completed: 20231026 Latest Revision: 20231026
    • الموضوع:
      20231215
    • الرقم المعرف:
      10.1111/jpi.12854
    • الرقم المعرف:
      36692235