Thyroid hormone receptor beta mutations alter photoreceptor development and function in Danio rerio (zebrafish)
Autoři:
Ciana Deveau aff001; Xiaodong Jiao aff002; Sachihiro C. Suzuki aff003; Asha Krishnakumar aff001; Takeshi Yoshimatsu aff004; J Fielding Hejtmancik aff002; Ralph F. Nelson aff001
Působiště autorů:
National Institute of Neurological Disorders and Stroke, National Institutes of Health, Rockville, Maryland, United States of America
aff001; National Eye Institute, National Institutes of Health, Rockville, Maryland, United States of America
aff002; Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan
aff003; University of Sussex, Brighton, United Kingdom
aff004
Vyšlo v časopise:
Thyroid hormone receptor beta mutations alter photoreceptor development and function in Danio rerio (zebrafish). PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008869
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008869
Souhrn
We investigate mutations in trβ2, a splice variant of thrb, identifying changes in function, structure, and behavior in larval and adult zebrafish retinas. Two N-terminus CRISPR mutants were identified. The first is a 6BP+1 insertion deletion frameshift resulting in a truncated protein. The second is a 3BP in frame deletion with intact binding domains. ERG recordings of isolated cone signals showed that the 6BP+1 mutants did not respond to red wavelengths of light while the 3BP mutants did respond. 6BP+1 mutants lacked optomotor and optokinetic responses to red/black and green/black contrasts. Both larval and adult 6BP+1 mutants exhibit a loss of red-cone contribution to the ERG and an increase in UV-cone contribution. Transgenic reporters show loss of cone trβ2 activation in the 6BP+1 mutant but increase in the density of cones with active blue, green, and UV opsin genes. Antibody reactivity for red-cone LWS1 and LWS2 opsin was absent in the 6BP+1 mutant, as was reactivity for arrestin3a. Our results confirm a critical role for trβ2 in long-wavelength cone development.
Klíčová slova:
Eyes – Fish physiology – Fluorescence imaging – Frameshift mutation – Larvae – Photoreceptors – Retina – Zebrafish
Zdroje
1. Ng L, Hurley JB, Dierks B, Srinivas M, Saltó C, Vennström B, et al. A thyroid hormone receptor that is required for the development of green cone photoreceptors. Nature genetics. 2001;27(1):94–8. doi: 10.1038/83829 11138006
2. Liu Y-W, Lo L-J, Chan W-K. Temporal expression and T3 induction of thyroid hormone receptors α1 and β1 during early embryonic and larval development in zebrafish, Danio rerio. Molecular and cellular endocrinology. 2000;159(1–2):187–95. doi: 10.1016/s0303-7207(99)00193-8 10687864
3. Campi I, Cammarata G, Bianchi Marzoli S, Beck-Peccoz P, Santarsiero D, Dazzi D, et al. Retinal photoreceptor functions are compromised in patients with resistance to thyroid hormone syndrome (RTHβ). The Journal of Clinical Endocrinology & Metabolism. 2017;102(7):2620–7.
4. Weiss AH, Kelly JP, Bisset D, Deeb SS. Reduced L-and M-and increased S-cone functions in an infant with thyroid hormone resistance due to mutations in the THRβ2 gene. Ophthalmic genetics. 2012;33(4):187–95. doi: 10.3109/13816810.2012.681096 22551329
5. Sjöberg M, Vennström B. Ligand-dependent and-independent transactivation by thyroid hormone receptor beta 2 is determined by the structure of the hormone response element. Molecular and Cellular Biology. 1995;15(9):4718–26. doi: 10.1128/mcb.15.9.4718 7651389
6. Ng L, Lu A, Swaroop A, Sharlin DS, Swaroop A, Forrest D. Two transcription factors can direct three photoreceptor outcomes from rod precursor cells in mouse retinal development. Journal of Neuroscience. 2011;31(31):11118–25. doi: 10.1523/JNEUROSCI.1709-11.2011 21813673
7. Darras VM, Van Herck SL, Heijlen M, De Groef B. Thyroid hormone receptors in two model species for vertebrate embryonic development: chicken and zebrafish. Journal of thyroid research. 2011;2011.
8. Deeb SS. Genetics of variation in human color vision and the retinal cone mosaic. Current opinion in genetics & development. 2006;16(3):301–7.
9. Marelli F, Carra S, Agostini M, Cotelli F, Peeters R, Chatterjee K, et al. Patterns of thyroid hormone receptor expression in zebrafish and generation of a novel model of resistance to thyroid hormone action. Molecular and cellular endocrinology. 2016;424:102–17. doi: 10.1016/j.mce.2016.01.020 26802880
10. Suzuki SC, Bleckert A, Williams PR, Takechi M, Kawamura S, Wong RO. Cone photoreceptor types in zebrafish are generated by symmetric terminal divisions of dedicated precursors. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(37):15109–14. doi: 10.1073/pnas.1303551110 23980162
11. Chinen A, Hamaoka T, Yamada Y, Kawamura S. Gene duplication and spectral diversification of cone visual pigments of zebrafish. Genetics. 2003;163(2):663–75. 12618404
12. Mitchell DM, Stevens CB, Frey RA, Hunter SS, Ashino R, Kawamura S, et al. Retinoic acid signaling regulates differential expression of the tandemly-duplicated long wavelength-sensitive cone opsin genes in zebrafish. PLoS genetics. 2015;11(8):e1005483. doi: 10.1371/journal.pgen.1005483 26296154
13. DuVal MG, Allison WT. Photoreceptor Progenitors Depend Upon Coordination of gdf6a, thrβ, and tbx2b to Generate Precise Populations of Cone Photoreceptor Subtypes. Investigative ophthalmology & visual science. 2018;59(15):6089–101.
14. Jones I, Srinivas M, Ng L, Forrest D. The thyroid hormone receptor β gene: structure and functions in the brain and sensory systems. Thyroid. 2003;13(11):1057–68. doi: 10.1089/105072503770867228 14651789
15. Renninger SL, Gesemann M, Neuhauss SC. Cone arrestin confers cone vision of high temporal resolution in zebrafish larvae. European Journal of Neuroscience. 2011;33(4):658–67. doi: 10.1111/j.1460-9568.2010.07574.x 21299656
16. Larison KD, Bremiller R. Early onset of phenotype and cell patterning in the embryonic zebrafish retina. Development. 1990;109(3):567–76. 2401210
17. Allison WT, Barthel LK, Skebo KM, Takechi M, Kawamura S, Raymond PA. Ontogeny of cone photoreceptor mosaics in zebrafish. Journal of Comparative Neurology. 2010;518(20):4182–95. doi: 10.1002/cne.22447 20878782
18. Nelson RF, Balraj A, Suresh T, Torvund MM, Patterson SS. Strain variations in opsin peaks in situ during zebrafish development. Visual neuroscience [Internet]. 2019; 36:[E010 p.]. Available from: https://doi.org/10.1017/S0952523819000075.
19. Orger MB, Baier H. Channeling of red and green cone inputs to the zebrafish optomotor response. Visual neuroscience. 2005;22(03):275–81.
20. Krauss A, Neumeyer C. Wavelength dependence of the optomotor response in zebrafish (Danio rerio). Vision research. 2003;43(11):1275–84.
21. Brockerhoff SE, Hurley JB, Janssen-Bienhold U, Neuhauss SCF, Driever W, Dowling JE. A behavioral screen for isolating zebrafish mutants with visual system defects. Proc Natl Acad Sci U S A. 1995;92(23):10545–9. doi: 10.1073/pnas.92.23.10545 7479837
22. Shibusawa N, Hollenberg AN, Wondisford FE. Thyroid hormone receptor DNA binding is required for both positive and negative gene regulation. Journal of Biological Chemistry. 2003;278(2):732–8. doi: 10.1074/jbc.M207264200 12419821
23. Tsujimura T, Hosoya T, Kawamura S. A single enhancer regulating the differential expression of duplicated red-sensitive opsin genes in zebrafish. PLoS genetics. 2010;6(12):e1001245. doi: 10.1371/journal.pgen.1001245 21187910
24. Takechi M, Kawamura S. Temporal and spatial changes in the expression pattern of multiple red and green subtype opsin genes during zebrafish development. Journal of Experimental Biology. 2005;208(7):1337–45.
25. Mackin RD, Frey RA, Gutierrez C, Farre AA, Kawamura S, Mitchell DM, et al. Endocrine regulation of multichromatic color vision. Proceedings of the National Academy of Sciences. 2019;116(34):16882–91.
26. Raymond PA, Barthel LK. A moving wave patterns the cone photoreceptor mosaic array in the zebrafish retina. International Journal of Developmental Biology. 2004;48(8–9):935–45. doi: 10.1387/ijdb.041873pr 15558484
27. Zou J, Wang X, Wei X. Crb apical polarity proteins maintain zebrafish retinal cone mosaics via intercellular binding of their extracellular domains. Developmental cell. 2012;22(6):1261–74. doi: 10.1016/j.devcel.2012.03.007 22579223
28. Harvey CB, Williams GR. Mechanism of thyroid hormone action. Thyroid. 2002;12(6):441–6. doi: 10.1089/105072502760143791 12165104
29. Baier H. Zebrafish on the move: towards a behavior–genetic analysis of vertebrate vision. Current opinion in neurobiology. 2000;10(4):451–5. doi: 10.1016/s0959-4388(00)00116-1 10981613
30. Woods AJ, Yuen KL, Karvinen KS. Characterizing crosstalk in anaglyphic stereoscopic images on LCD monitors and plasma displays. Journal of the Society for Information Display. 2007;15(11):889–98.
31. Marks WB, Dobelle WH, Macnichol EF Jr. Visual Pigments of Single Primate Cones. Science. 1964;143(3611):1181–3. doi: 10.1126/science.143.3611.1181 14108303
32. Srinivas M, Ng L, Liu H, Jia L, Forrest D. Activation of the blue opsin gene in cone photoreceptor development by retinoid-related orphan receptor β. Molecular endocrinology. 2006;20(8):1728–41. doi: 10.1210/me.2005-0505 16574740
33. Li YN, Matsui JI, Dowling JE. Specificity of the horizontal cell-photoreceptor connections in the zebrafish (Danio rerio) retina. J Comp Neurol. 2009;516(5):442–53. doi: 10.1002/cne.22135 19655401
34. Jao L-E, Wente SR, Chen W. Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. Proceedings of the National Academy of Sciences. 2013;110(34):13904–9.
35. Nelson RF, Singla N. A spectral model for signal elements isolated from zebrafish photopic electroretinogram. Visual Neuroscience. 2009;26(4):349–63. doi: 10.1017/S0952523809990113 19723365
36. Dartnall H, JA. The interpretation of spectral sensitivity curves. British Medical Bulletin. 1953;9(1):24–30. doi: 10.1093/oxfordjournals.bmb.a074302 13032421
37. Hughes A, Saszik S, Bilotta J, Demarco PJ Jr., Patterson WF 2nd. Cone contributions to the photopic spectral sensitivity of the zebrafish ERG. Visual Neuroscience. 1998;15(6):1029– doi: 10.1017/s095252389815602x 9839967
38. Palacios AG, Goldsmith TH, Bernard GD. Sensitivity of cones from a cyprinid fish (Danio aequipinnatus) to ultraviolet and visible light. Visual Neuroscience. 1996;13(3):411–21. doi: 10.1017/s0952523800008099 8782369
39. Yin J, Brocher J, Linder B, Hirmer A, Sundaramurthi H, Fischer U, et al. The 1D4 antibody labels outer segments of long double cone but not rod photoreceptors in zebrafish. Investigative ophthalmology & visual science. 2012;53(8):4943–51.
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 6
- Případ Bulovka: Jak postupují jiné nemocnice, aby podobným tragédiím zabránily?
- Jak často se u masových střelců vyskytují duševní choroby?
- FDA varuje před selfmonitoringem cukru pomocí chytrých hodinek. Jak je to v Česku?
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Není statin jako statin aneb praktický přehled rozdílů jednotlivých molekul
Nejčtenější v tomto čísle
- AXR1 affects DNA methylation independently of its role in regulating meiotic crossover localization
- Super-resolution imaging of RAD51 and DMC1 in DNA repair foci reveals dynamic distribution patterns in meiotic prophase
- Reciprocal regulation between nicotinamide adenine dinucleotide metabolism and abscisic acid and stress response pathways in Arabidopsis
- Osteocalcin promotes bone mineralization but is not a hormone