The maturation of photoreceptors in the avian retina is stimulated by thyroid hormone

Neuroscience

Volumn 178, Issue , 2011, Pages 250-260

  Fischer, A J ^a   Bongini, R ^a   Bastaki, N ^b   Sherwood, P ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Islet2; Lim3; Photoreceptor; Retina; RLIM; Thyroid hormone

Indexed keywords

AXONIN 1; BINDING PROTEIN; CALBINDIN; OPSIN; RED GREEN OPSIN; RHODOPSIN; RING FINGER LIM DOMAIN BINDING PROTEIN; THYROID HORMONE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ISLET2; TRANSCRIPTION FACTOR LIM3; UNCLASSIFIED DRUG; VIOLET OPSIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHICKEN; CONTROLLED STUDY; CORRELATION ANALYSIS; DOWN REGULATION; HORMONAL REGULATION; NONHUMAN; PHOTORECEPTOR DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA; RETINA DEVELOPMENT; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CHICKENS; CONTACTIN 2; DOWN-REGULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; INJECTIONS, INTRAOCULAR; OPSINS; PHOTORECEPTOR CELLS, VERTEBRATE; RETINA; THYROXINE; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 79952008477     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.01.022     Document Type: Article

References (50)

1. Allison W.T., Dann S.G., Veldhoen K.M., Hawryshyn C.W. Degeneration and regeneration of ultraviolet cone photoreceptors during development in rainbow trout. J Comp Neurol 2006, 499:702-715.
2. Bianco A.C., Kim B.W. Deiodinases: implications of the local control of thyroid hormone action. J Clin Invest 2006, 116:2571-2579.
3. Bradford R.L., Wang C., Zack D.J., Adler R. Roles of cell-intrinsic and microenvironmental factors in photoreceptor cell differentiation. Dev Biol 2005, 286:31-45.
4. Bruhn S.L., Cepko C.L. Development of the pattern of photoreceptors in the chick retina. J Neurosci 1996, 16:1430-1439.
5. Cornish E.E., Hendrickson A.E., Provis J.M. Distribution of short-wavelength-sensitive cones in human fetal and postnatal retina: early development of spatial order and density profiles. Vision Res 2004, 44:2019-2026.
6. Cornish E.E., Madigan M.C., Natoli R., Hales A., Hendrickson A.E., Provis J.M. Gradients of cone differentiation and FGF expression during development of the foveal depression in macaque retina. Vis Neurosci 2005, 22:447-459.
7. Drenhaus U., Morino P., Rager G. Expression of axonin-1 in developing amacrine cells in the chick retina. J Comp Neurol 2004, 468:496-508.
8. Edqvist P.H., Hallbook F. Newborn horizontal cells migrate bi-directionally across the neuroepithelium during retinal development. Development 2004, 131:1343-1351.
9. Edqvist P.H., Myers S.M., Hallbook F. Early identification of retinal subtypes in the developing, pre-laminated chick retina using the transcription factors Prox1, Lim1, Ap2alpha, Pax6, Isl1, Isl2, Lim3 and Chx10. Eur J Histochem 2006, 50:147-154.
10. Elshatory Y., Everhart D., Deng M., Xie X., Barlow R.B., Gan L. Islet-1 controls the differentiation of retinal bipolar and cholinergic amacrine cells. J Neurosci 2007, 27:12707-12720.
11. Fischer A.J., Dierks B.D., Reh T.A. Exogenous growth factors induce the production of ganglion cells at the retinal margin. Development 2002, 129:2283-2291.
12. Fischer A.J., Foster S., Scott M.A., Sherwood P. Transient expression of LIM-domain transcription factors is coincident with delayed maturation of photoreceptors in the chicken retina. J Comp Neurol 2008, 506:584-603.
13. Fischer A.J., Omar G. Transitin, a nestin-related intermediate filament, is expressed by neural progenitors and can be induced in Muller glia in the chicken retina. J Comp Neurol 2005, 484:1-14.
14. Fischer A.J., Reh T.A. Growth factors induce neurogenesis in the ciliary body. Dev Biol 2003, 259:225-240.
15. Fischer A.J., Ritchey E.R., Scott M.A., Wynne A. Bullwhip neurons in the retina regulate the size and shape of the eye. Dev Biol 2008, 317:196-212.
16. Fischer A.J., Scott M.A., Tuten W. Mitogen-activated protein kinase-signaling stimulates Muller glia to proliferate in acutely damaged chicken retina. Glia 2009, 57:166-181.
17. Fischer A.J., Stanke J.J., Aloisio G., Hoy H., Stell W.K. Heterogeneity of horizontal cells in the chicken retina. J Comp Neurol 2007, 500:1154-1171.
18. Fischer A.J., Stanke J.J., Ghai K., Scott M., Omar G. Development of bullwhip neurons in the embryonic chicken retina. J Comp Neurol 2007, 503:538-549.
19. Galli-Resta L., Resta G., Tan S.S., Reese B.E. Mosaics of islet-1-expressing amacrine cells assembled by short-range cellular interactions. J Neurosci 1997, 17:7831-7838.
20. Galton V.A. The roles of the iodothyronine deiodinases in mammalian development. Thyroid 2005, 15:823-834.
21. Ghai K., Stanke J.J., Fischer A.J. Patterning of the circumferential marginal zone of progenitors in the chicken retina. Brain Res 2008, 1192:76-89.
22. Ghai K., Zelinka C., Fischer A.J. Serotonin released from amacrine neurons is scavenged and degraded in bipolar neurons in the retina. J Neurochem 2009, 111:1-14.
23. Hawryshyn C.W., Arnold M.G., Chaisson D.J., Martin P.C. The ontogeny of ultraviolet photosensitivity in rainbow trout (Salmo gairdneri). Vis Neurosci 1989, 2:247-254.
24. Hendrickson A., Hicks D. Distribution and density of medium- and short-wavelength selective cones in the domestic pig retina. Exp Eye Res 2002, 74:435-444.
25. Linser P., Moscona A.A. Hormonal induction of glutamine synthetase in cultures of embryonic retina cells: requirement for neuron-glia contact interactions. Dev Biol 1983, 96:529-534.
26. Lu J.W., McMurtry J.P., Coon C.N. Developmental changes of plasma insulin, glucagon, insulin-like growth factors, thyroid hormones, and glucose concentrations in chick embryos and hatched chicks. Poult Sci 2007, 86:673-683.
27. Morris V.B. Symmetry in a receptor mosaic demonstrated in the chick from the frequencies, spacing and arrangement of the types of retinal receptor. J Comp Neurol 1970, 140:359-398.
28. Moscona M., Moscona A.A. The development of inducibility for glutamine synthetase in embryonic neural retina: inhibition by BrdU. Differentiation 1979, 13:165-172.
29. Ng L., Hurley J.B., Dierks B., Srinivas M., Salto C., Vennstrom B., Reh T.A., Forrest D. A thyroid hormone receptor that is required for the development of green cone photoreceptors. Nat Genet 2001, 27:94-98.
30. Ng L., Lyubarsky A., Nikonov S.S., Ma M., Srinivas M., Kefas B., St Germain D.L., Hernandez A., Pugh E.N., Forrest D. Type 3 deiodinase, a thyroid-hormone-inactivating enzyme, controls survival and maturation of cone photoreceptors. J Neurosci 2010, 30:3347-3357.
31. Ostendorff H.P., Peirano R.I., Peters M.A., Schluter A., Bossenz M., Scheffner M., Bach I. Ubiquitination-dependent cofactor exchange on LIM homeodomain transcription factors. Nature 2002, 416:99-103.
32. Pak W., Hindges R., Lim Y.S., Pfaff S.L., O'Leary D.D. Magnitude of binocular vision controlled by islet-2 repression of a genetic program that specifies laterality of retinal axon pathfinding. Cell 2004, 119:567-578.
33. Perrin F.E., Rathjen F.G., Stoeckli E.T. Distinct subpopulations of sensory afferents require F11 or axonin-1 for growth to their target layers within the spinal cord of the chick. Neuron 2001, 30:707-723.
34. Poche R.A., Furuta Y., Chaboissier M.C., Schedl A., Behringer R.R. Sox9 is expressed in mouse multipotent retinal progenitor cells and functions in Muller glial cell development. J Comp Neurol 2008, 510:237-250.
35. Prada C., Puga J., Perez-Mendez L., Lopez R., Ramirez G. Spatial and temporal patterns of neurogenesis in the chick retina. Eur J Neurosci 1991, 3:559-569.
36. Raine J.C., Coffin A.B., Hawryshyn C.W. Systemic thyroid hormone is necessary and sufficient to induce ultraviolet-sensitive cone loss in the juvenile rainbow trout retina. J Exp Biol 2010, 213:493-501.
37. Raine J.C., Hawryshyn C.W. Changes in thyroid hormone reception precede SWS1 opsin downregulation in trout retina. J Exp Biol 2009, 212:2781-2788.
38. Retaux S., Bachy I. A short history of LIM domains (1993-2002): from protein interaction to degradation. Mol Neurobiol 2002, 26:269-281.
39. Roberts M.R., Srinivas M., Forrest D., Morreale de Escobar G., Reh T.A. Making the gradient: thyroid hormone regulates cone opsin expression in the developing mouse retina. Proc Natl Acad Sci U S A 2006, 103:6218-6223.
40. Sears S., Erickson A., Hendrickson A. The spatial and temporal expression of outer segment proteins during development of Macaca monkey cones. Invest Ophthalmol Vis Sci 2000, 41:971-979.
41. Sjoberg M., Vennstrom B., Forrest D. Thyroid hormone receptors in chick retinal development: differential expression of mRNAs for alpha and N-terminal variant beta receptors. Development 1992, 114:39-47.
42. Sonderegger P., Kunz S., Rader C., Buchstaller A., Berger P., Vogt L., Kozlov S.V., Ziegler U., Kunz B., Fitzli D., Stoeckli E.T. Discrete clusters of axonin-1 and NgCAM at neuronal contact sites: facts and speculations on the regulation of axonal fasciculation. Prog Brain Res 1998, 117:93-104.
43. Stepanek L., Stoker A.W., Stoeckli E., Bixby J.L. Receptor tyrosine phosphatases guide vertebrate motor axons during development. J Neurosci 2005, 25:3813-3823.
44. Stoeckli E.T. Molecular mechanisms of commissural axon pathfinding. Prog Brain Res 1998, 117:105-114.
45. Stoeckli E.T., Landmesser L.T. Axonin-1, Nr-CAM, and Ng-CAM play different roles in the in vivo guidance of chick commissural neurons. Neuron 1995, 14:1165-1179.
46. Thaler J.P., Koo S.J., Kania A., Lettieri K., Andrews S., Cox C., Jessell T.M., Pfaff S.L. A postmitotic role for Isl-class LIM homeodomain proteins in the assignment of visceral spinal motor neuron identity. Neuron 2004, 41:337-350.
47. Thaler J.P., Lee S.K., Jurata L.W., Gill G.N., Pfaff S.L. LIM factor Lhx3 contributes to the specification of motor neuron and interneuron identity through cell-type-specific protein-protein interactions. Cell 2002, 110:237-249.
48. Trimarchi J.M., Harpavat S., Billings N.A., Cepko C.L. Thyroid hormone components are expressed in three sequential waves during development of the chick retina. BMC Dev Biol 2008, 8:101.
49. Vardimon L., Fox L.E., Moscona A.A. Developmental regulation of glutamine synthetase and carbonic anhydrase II in neural retina. Proc Natl Acad Sci U S A 1986, 83:9060-9064.
50. Xiang M., Zhou L., Macke J.P., Yoshioka T., Hendry S.H., Eddy R.L., Shows T.B., Nathans J. The Brn-3 family of POU-domain factors: primary structure, binding specificity, and expression in subsets of retinal ganglion cells and somatosensory neurons. J Neurosci 1995, 15:4762-4785.