A component of retinal light adaptation mediated by the thyroid hormone cascade

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Bedolla, Diana E ^a   Torre, Vincent ^a,b  

^a SISSA   (Italy)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; E1A ASSOCIATED P300 PROTEIN; GAMMA CRYSTALLIN; MYOSIN VA; PRESENILIN 1; RHODOPSIN KINASE; STAT3 PROTEIN; THYROID HORMONE; THYROXINE DEIODINASE; THYROXINE DEIODINASE 2; THYROXINE DEIODINASE 3; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PAX4; UNCLASSIFIED DRUG; IODIDE PEROXIDASE; PRIMER DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CIRCADIAN RHYTHM; CONTROLLED STUDY; CRYGB GENE; CRYGC GENE; CRYGD GENE; DARKNESS; DIO2 GENE; DIO3 GENE; DNA MICROARRAY; DOWN REGULATION; EP300 GENE; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC REGULATION; GRK1 GENE; ILLUMINATION; LIGHT ADAPTATION; MALE; MYO5A GENE; NONHUMAN; PAX4 GENE; PHOTORECEPTOR CELL; PROTEIN ANALYSIS; PSEN1 GENE; RAT; REAL TIME POLYMERASE CHAIN REACTION; RETINA BIPOLAR GANGLION CELL; RETINA DEVELOPMENT; RPGRIP1 GENE; STAT3 GENE; TRANSCRIPTION INITIATION; UPREGULATION; ADAPTATION; ANIMAL; ENZYMOLOGY; GENETICS; IMMUNOHISTOCHEMISTRY; LIGHT; METABOLISM; MOUSE; MOUSE MUTANT; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; RETINA;

RATTUS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BASE SEQUENCE; CIRCADIAN RHYTHM; DARKNESS; DNA PRIMERS; IMMUNOHISTOCHEMISTRY; IODIDE PEROXIDASE; LIGHT; MICE; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; REAL-TIME POLYMERASE CHAIN REACTION; RETINA; THYROID HORMONES;

EID: 80055061278     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026334     Document Type: Article

References (82)

1. Cahill GM, Besharse JC, (1993) Circadian clock functions localized in xenopus retinal photoreceptors. Neuron 10: 573-577.
2. Kramer RH, Molokanova E, (2001) Modulation of cyclic-nucleotide-gated channels and regulation of vertebrate phototransduction. J. Exp. Biol 204: 2921-2931.
3. LaVail MM, (1976) Rod outer segment disk shedding in rat retina: relationship to cyclic lighting. Science 194: 1071-1074.
4. Yoshida K, Kawamura K, Imaki J, (1993) Differential expression of c-fos mRNA in rat retinal cells: regulation by light/dark cycle. Neuron 10: 1049-1054.
5. Imaki J, Yamashita K, Yamakawa A, Yoshida K, (1995) Expression of jun family genes in rat retinal cells: regulation by light/dark cycle. Brain Res. Mol. Brain Res 30: 48-52.
6. Cervetto L, Pasino E, Torre V, (1977) Electrical responses of rods in the retina of Bufo marinus. J. Physiol. (Lond.) 267: 17-51.
7. Torre V, Matthews HR, Lamb TD, (1986) Role of calcium in regulating the cyclic GMP cascade of phototransduction in retinal rods. Proc. Natl. Acad. Sci. U.S.A 83: 7109-7113.
8. Koutalos Y, Yau KW, (1996) Regulation of sensitivity in vertebrate rod photoreceptors by calcium. Trends Neurosci 19: 73-81.
9. Pugh EN, Nikonov S, Lamb TD, (1999) Molecular mechanisms of vertebrate photoreceptor light adaptation. Curr. Opin. Neurobiol 9: 410-418 doi:10.1016/S0959-4388(99)80062-2.
10. Burns ME, Baylor DA, (2001) Activation, deactivation, and adaptation in vertebrate photoreceptor cells. Annu. Rev. Neurosci 24: 779-805 doi:10.1146/annurev.neuro.24.1.779.
11. Fain GL, (2001) Dark adaptation. Prog. Brain Res 131: 383-394.
12. Sokolov M, Lyubarsky AL, Strissel KJ, Savchenko AB, Govardovskii VI, et al. (2002) Massive light-driven translocation of transducin between the two major compartments of rod cells: a novel mechanism of light adaptation. Neuron 34: 95-106.
13. Elias RV, Sezate SS, Cao W, McGinnis JF, (2004) Temporal kinetics of the light/dark translocation and compartmentation of arrestin and alpha-transducin in mouse photoreceptor cells. Mol. Vis 10: 672-681.
14. Nair KS, Hanson SM, Mendez A, Gurevich EV, Kennedy MJ, et al. (2005) Light-dependent redistribution of arrestin in vertebrate rods is an energy-independent process governed by protein-protein interactions. Neuron 46: 555-567 doi:10.1016/j.neuron.2005.03.023.
15. Strissel KJ, Sokolov M, Trieu LH, Arshavsky VY, (2006) Arrestin translocation is induced at a critical threshold of visual signaling and is superstoichiometric to bleached rhodopsin. J. Neurosci 26: 1146-1153 doi:10.1523/JNEUROSCI.4289-05.2006.
16. Ngo JT, Klisak I, Sparkes RS, Mohandas T, Yamaki K, et al. (1990) Assignment of the S-antigen gene (SAG) to human chromosome 2q24-q37. Genomics 7: 84-87.
17. Dizhoor AM, Olshevskaya EV, Henzel WJ, Wong SC, Stults JT, et al. (1995) Cloning, sequencing, and expression of a 24-kDa Ca(2+)-binding protein activating photoreceptor guanylyl cyclase. J. Biol. Chem 270: 25200-25206.
18. Palczewski K, Subbaraya I, Gorczyca WA, Helekar BS, Ruiz CC, et al. (1994) Molecular cloning and characterization of retinal photoreceptor guanylyl cyclase-activating protein. Neuron 13: 395-404.
19. Codega P, Della Santina L, Gargini C, Bedolla DE, Subkhankulova T, et al. (2009) Prolonged illumination up-regulates arrestin and two guanylate cyclase activating proteins: a novel mechanism for light adaptation. J. Physiol. (Lond.) 587: 2457-2472 doi:10.1113/jphysiol.2009.168609.
20. Kelley MW, Turner JK, Reh TA, (1995) Ligands of steroid/thyroid receptors induce cone photoreceptors in vertebrate retina. Development 121: 3777-3785.
21. Marsh-Armstrong N, Huang H, Remo BF, Liu TT, Brown DD, (1999) Asymmetric growth and development of the Xenopus laevis retina during metamorphosis is controlled by type III deiodinase. Neuron 24: 871-878.
22. Trimarchi JM, Harpavat S, Billings NA, Cepko CL, (2008) Thyroid hormone components are expressed in three sequential waves during development of the chick retina. BMC Dev. Biol 8: 101 doi:10.1186/1471-213X-8-101.
23. Opitz R, Kloas W, (2010) Developmental regulation of gene expression in the thyroid gland of Xenopus laevis tadpoles. Gen. Comp. Endocrinol 168: 199-208 doi:10.1016/j.ygcen.2010.04.013.
24. Glaschke A, Weiland J, Del Turco D, Steiner M, Peichl L, et al. (2011) Thyroid hormone controls cone opsin expression in the retina of adult rodents. J. Neurosci 31: 4844-4851 doi:10.1523/jneurosci.6181-10.2011.
25. Wu Y, Koenig RJ, (2000) Gene regulation by thyroid hormone. Trends Endocrinol. Metab 11: 207-211.
26. Bianco AC, Salvatore D, Gereben B, Berry MJ, Larsen PR, (2002) Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr. Rev 23: 38-89.
27. Yen PM, Ando S, Feng X, Liu Y, Maruvada P, et al. (2006) Thyroid hormone action at the cellular, genomic and target gene levels. Mol. Cell. Endocrinol 246: 121-127 doi:10.1016/j.mce.2005.11.030.
28. Gereben B, Zavacki AM, Ribich S, Kim BW, Huang SA, et al. (2008) Cellular and molecular basis of deiodinase-regulated thyroid hormone signaling. Endocr. Rev 29: 898-938 doi:10.1210/er.2008-0019.
29. Galton VA, Wood ET, St Germain EA, Withrow C-A, Aldrich G, et al. (2007) Thyroid hormone homeostasis and action in the type 2 deiodinase-deficient rodent brain during development. Endocrinology 148: 3080-3088 doi:10.1210/en.2006-1727.
30. Ng L, Lyubarsky A, Nikonov SS, Ma M, Srinivas M, et al. (2010) Type 3 deiodinase, a thyroid-hormone-inactivating enzyme, controls survival and maturation of cone photoreceptors. J. Neurosci 30: 3347-3357 doi:10.1523/JNEUROSCI.5267-09.2010.
31. Reidel B, Orisme W, Goldmann T, Smith WC, Wolfrum U, (2006) Photoreceptor vitality in organotypic cultures of mature vertebrate retinas validated by light-dependent molecular movements. Vision Res 46: 4464-4471 doi:10.1016/j.visres.2006.07.019.
32. Williams GR, Bassett D, (2011) Local control of thyroid hormone action- role of type 2 deiodinase. J Endocrinol. Available: http://www.ncbi.nlm.nih.gov/pubmed/21292729. Accessed 21 Feb 2011.
33. Zhang SS-M, Wei J, Qin H, Zhang L, Xie B, et al. (2004) STAT3-mediated signaling in the determination of rod photoreceptor cell fate in mouse retina. Invest. Ophthalmol. Vis. Sci 45: 2407-2412.
34. Peng G-H, Chen S, (2007) Crx activates opsin transcription by recruiting HAT-containing co-activators and promoting histone acetylation. Hum. Mol. Genet 16: 2433-2452 doi:10.1093/hmg/ddm200.
35. Rath MF, Bailey MJ, Kim J-S, Coon SL, Klein DC, et al. (2009) Developmental and daily expression of the Pax4 and Pax6 homeobox genes in the rat retina: localization of Pax4 in photoreceptor cells. J. Neurochem 108: 285-294 doi:10.1111/j.1471-4159.2008.05765.x.
36. Zhang J, Lazar MA, (2000) The mechanism of action of thyroid hormones. Annu. Rev. Physiol 62: 439-466 doi:10.1146/annurev.physiol.62.1.439.
37. Feigenspan A, Wässle H, Bormann J, (1993) Pharmacology of GABA receptor Cl- channels in rat retinal bipolar cells. Nature 361: 159-162 doi:10.1038/361159a0.
38. Qian H, Dowling JE, (1993) Novel GABA responses from rod-driven retinal horizontal cells. Nature 361: 162-164 doi:10.1038/361162a0.
39. Yang X-L, (2004) Characterization of receptors for glutamate and GABA in retinal neurons. Prog. Neurobiol 73: 127-150 doi:10.1016/j.pneurobio.2004.04.002.
40. Ball SL, Powers PA, Shin H-S, Morgans CW, Peachey NS, et al. (2002) Role of the beta(2) subunit of voltage-dependent calcium channels in the retinal outer plexiform layer. Invest. Ophthalmol. Vis. Sci 43: 1595-1603.
41. Lolley RN, Craft CM, Lee RH, (1992) Photoreceptors of the retina and pinealocytes of the pineal gland share common components of signal transduction. Neurochem. Res 17: 81-89.
42. Osawa S, Jo R, Weiss ER, (2008) Phosphorylation of GRK7 by PKA in cone photoreceptor cells is regulated by light. J. Neurochem 107: 1314-1324 doi:10.1111/j.1471-4159.2008.05691.x.
43. Liu Y, Fu L, Chen D-G, Deeb SS, (2007) Identification of novel retinal target genes of thyroid hormone in the human WERI cells by expression microarray analysis. Vision Res 47: 2314-2326 doi:10.1016/j.visres.2007.04.023.
44. Glaschke A, Weiland J, Del Turco D, Steiner M, Peichl L, et al. (2011) Thyroid hormone controls cone opsin expression in the retina of adult rodents. J. Neurosci 31: 4844-4851 doi:10.1523/JNEUROSCI.6181-10.2011.
45. Scheetz TE, Kim K-YA, Swiderski RE, Philp AR, Braun TA, et al. (2006) Regulation of gene expression in the mammalian eye and its relevance to eye disease. Proceedings of the National Academy of Sciences 103: 14429-14434 doi:10.1073/pnas.0602562103.
46. Roberts MR, Hendrickson A, McGuire CR, Reh TA, (2005) Retinoid X receptor (gamma) is necessary to establish the S-opsin gradient in cone photoreceptors of the developing mouse retina. Invest. Ophthalmol. Vis. Sci 46: 2897-2904 doi:10.1167/iovs.05-0093.
47. Ng L, Hurley JB, Dierks B, Srinivas M, Saltó C, et al. (2001) A thyroid hormone receptor that is required for the development of green cone photoreceptors. Nat. Genet 27: 94-98 doi:10.1038/83829.
48. Attia RR, Sharma P, Janssen RC, Friedman JE, Deng X, et al. (2011) Regulation of Pyruvate Dehydrogenase Kinase 4 (PDK4) by CCAAT/Enhancer-binding Protein β (C/EBPβ). Journal of Biological Chemistry 286: 23799-23807 doi:10.1074/jbc.M111.246389.
49. Barrera-Hernandez G, Park KS, Dace A, Zhan Q, Cheng SY, (1999) Thyroid hormone-induced cell proliferation in GC cells is mediated by changes in G1 cyclin/cyclin-dependent kinase levels and activity. Endocrinology 140: 5267-5274.
50. Martins RAP, Linden R, Dyer MA, (2006) Glutamate regulates retinal progenitors cells proliferation during development. Eur. J. Neurosci 24: 969-980 doi:10.1111/j.1460-9568.2006.04966.x.
51. Politi LE, Rotstein NP, Carri NG, (2001) Effect of GDNF on neuroblast proliferation and photoreceptor survival: additive protection with docosahexaenoic acid. Invest. Ophthalmol. Vis. Sci 42: 3008-3015.
52. Roomets E, Kivelä T, Tyni T, (2008) Carnitine palmitoyltransferase I and Acyl-CoA dehydrogenase 9 in retina: insights of retinopathy in mitochondrial trifunctional protein defects. Invest. Ophthalmol. Vis. Sci 49: 1660-1664 doi:10.1167/iovs.07-1094.
53. St Germain DL, Galton VA, Hernandez A, (2009) Minireview: Defining the roles of the iodothyronine deiodinases: current concepts and challenges. Endocrinology 150: 1097-1107 doi:10.1210/en.2008-1588.
54. Bai L, Zimmer S, Rickes O, Rohleder N, Holthues H, et al. (2008) Daily oscillation of gene expression in the retina is phase-advanced with respect to the pineal gland. Brain Res 1203: 89-96 doi:10.1016/j.brainres.2008.01.073.
55. Revel FG, Saboureau M, Pévet P, Mikkelsen JD, Simonneaux V, (2006) Melatonin regulates type 2 deiodinase gene expression in the Syrian hamster. Endocrinology 147: 4680-4687 doi:10.1210/en.2006-0606.
56. Yasuo S, Yoshimura T, Ebihara S, Korf H-W, (2007) Temporal dynamics of type 2 deiodinase expression after melatonin injections in Syrian hamsters. Endocrinology 148: 4385-4392 doi:10.1210/en.2007-0497.
57. Forrest D, Reh TA, Rüsch A, (2002) Neurodevelopmental control by thyroid hormone receptors. Curr. Opin. Neurobiol 12: 49-56.
58. Fischer AJ, Bongini R, Bastaki N, Sherwood P, (2011) The maturation of photoreceptors in the avian retina is stimulated by thyroid hormone. Neuroscience 178: 250-260 doi:16/j.neuroscience.2011.01.022.
59. Bruhn SL, Cepko CL, (1996) Development of the pattern of photoreceptors in the chick retina. J. Neurosci 16: 1430-1439.
60. Paul BD, Buchholz DR, Fu L, Shi Y-B, (2007) SRC-p300 coactivator complex is required for thyroid hormone-induced amphibian metamorphosis. J. Biol. Chem 282: 7472-7481 doi:10.1074/jbc.M607589200.
61. Bianco AC, Silva JE, (1987) Intracellular conversion of thyroxine to triiodothyronine is required for the optimal thermogenic function of brown adipose tissue. J. Clin. Invest 79: 295-300 doi:10.1172/JCI112798.
62. de Jesus LA, Carvalho SD, Ribeiro MO, Schneider M, Kim SW, et al. (2001) The type 2 iodothyronine deiodinase is essential for adaptive thermogenesis in brown adipose tissue. J. Clin. Invest 108: 1379-1385 doi:10.1172/JCI13803.
63. Carvalho SD, Kimura ET, Bianco AC, Silva JE, (1991) Central role of brown adipose tissue thyroxine 5'-deiodinase on thyroid hormone-dependent thermogenic response to cold. Endocrinology 128: 2149-2159.
64. Bassett JHD, Williams GR, (2008) Critical role of the hypothalamic-pituitary-thyroid axis in bone. Bone 43: 418-426 doi:10.1016/j.bone.2008.05.007.
65. Ng L, Goodyear RJ, Woods CA, Schneider MJ, Diamond E, et al. (2004) Hearing loss and retarded cochlear development in mice lacking type 2 iodothyronine deiodinase. Proc. Natl. Acad. Sci. U.S.A 101: 3474-3479 doi:10.1073/pnas.0307402101.
66. Schneider MJ, Fiering SN, Pallud SE, Parlow AF, St Germain DL, et al. (2001) Targeted disruption of the type 2 selenodeiodinase gene (DIO2) results in a phenotype of pituitary resistance to T4. Mol. Endocrinol 15: 2137-2148.
67. Galton VA, Schneider MJ, Clark AS, St Germain DL, (2009) Life without thyroxine to 3,5,3'-triiodothyronine conversion: studies in mice devoid of the 5'-deiodinases. Endocrinology 150: 2957-2963 doi:10.1210/en.2008-1572.
68. Sharanjeet-Kaur, Dickinson CM, O'Donoghue E, Murray IJ, (1997) Spectral sensitivity in patients with dysthyroid eye disease. Ophthalmic Physiol Opt 17: 232-238.
69. Shaaban SA, Deeb SS, (1998) Functional analysis of the promoters of the human red and green visual pigment genes. Invest. Ophthalmol. Vis. Sci 39: 885-896.
70. Deeb SS, Liu Y, Hayashi T, (2006) Mutually exclusive expression of the L and M pigment genes in the human retinoblastoma cell line WERI: Resetting by cell division. Vis. Neurosci 23: 371-378 doi:10.1017/S0952523806233030.
71. Pugh EN Jr, Lamb TD, (2000) Chapter 5 Phototransduction in vertebrate rods and cones: Molecular mechanisms of amplification, recovery and light adaptation. Molecular Mechanisms in Visual Transduction Handbook of Biological Physics. Elsevier, Vol. 3 pp. 183-255.
72. Chen S, Wang QL, Nie Z, Sun H, Lennon G, et al. (1997) Crx, a novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron 19: 1017-1030.
73. Qian J, Esumi N, Chen Y, Wang Q, Chowers I, et al. (2005) Identification of regulatory targets of tissue-specific transcription factors: application to retina-specific gene regulation. Nucleic Acids Res 33: 3479-3491 doi:10.1093/nar/gki658.
74. Morgan R, (2006) Hox genes: a continuation of embryonic patterning? Trends Genet 22: 67-69 doi:10.1016/j.tig.2005.11.004.
75. Rath MF, Muñoz E, Ganguly S, Morin F, Shi Q, et al. (2006) Expression of the Otx2 homeobox gene in the developing mammalian brain: embryonic and adult expression in the pineal gland. J. Neurochem 97: 556-566 doi:10.1111/j.1471-4159.2006.03773.x.
76. Nishida A, Furukawa A, Koike C, Tano Y, Aizawa S, et al. (2003) Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nat. Neurosci 6: 1255-1263 doi:10.1038/nn1155.
77. Furukawa T, Morrow EM, Li T, Davis FC, Cepko CL, (1999) Retinopathy and attenuated circadian entrainment in Crx-deficient mice. Nat. Genet 23: 466-470 doi:10.1038/70591.
78. Schremser JL, Williams TP, (1995) Rod outer segment (ROS) renewal as a mechanism for adaptation to a new intensity environment. II. Rhodopsin synthesis and packing density. Exp. Eye Res 61: 25-32.
79. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
80. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
81. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408 doi:10.1006/meth.2001.1262.
82. Yuan JS, Reed A, Chen F, Stewart CN, (2006) Statistical analysis of real-time PCR data. BMC Bioinformatics 7: 85 doi:10.1186/1471-2105-7-85.