Thyroxine affects expression of KSPG-related genes, the carbonic anhydrase II gene, and KS sulfation in the embryonic chicken cornea

Investigative Ophthalmology and Visual Science

Volumn 47, Issue 1, 2006, Pages 120-132

  Conrad, Abigail H ^a   Zhang, Yuntao ^a   Walker, Amy R ^a   Olberding, Lisa A ^a   Hanzlick, Ann ^a   Zimmer, Andrea J ^a   Morffi, Raul ^a   Conrad, Gary W ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONATE DEHYDRATASE II; KERATAN SULFATE; MESSENGER RNA; PROTEOGLYCAN; THYROXINE; THYROXINE RECEPTOR; CRYSTALLIN; LUMICAN; PROTEOCHONDROITIN SULFATE; THYROID HORMONE RECEPTOR; THYROID HORMONE RECEPTOR ALPHA; THYROID HORMONE RECEPTOR BETA;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CORNEA CELL; CORNEA THICKNESS; ELECTROSPRAY MASS SPECTROMETRY; EMBRYO; GENE EXPRESSION; HORMONAL REGULATION; IN SITU HYBRIDIZATION; ION TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SULFATION; WHOLE CELL; ANIMAL; CHICK EMBRYO; CORNEA; DRUG EFFECT; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT;

ANIMALS; CARBONIC ANHYDRASE II; CHICK EMBRYO; CORNEA; CRYSTALLINS; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; KERATAN SULFATE; PROTEOCHONDROITIN SULFATES; RECEPTORS, THYROID HORMONE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; THYROID HORMONE RECEPTORS ALPHA; THYROID HORMONE RECEPTORS BETA; THYROXINE;

EID: 33644837455     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.05-0806     Document Type: Article

References (80)

1. Hay ED, Revel J-P. Fine structure of the developing avian cornea. Monogr Dev Biol. 1969;1:1-144.
2. Johnston MC, Noden DM, Hazelton RD, Coulombre JL, Coulombre AJ. Origins of avian ocular and periocular tissues. Exp Eye Res. 1979;29:27-43.
3. Hart GW. Biosynthesis of glycosaminoglycans during corneal development. J Biol Chem. 1976;251:6513-6521.
4. Funderburgh JL, Caterson B, Conrad GW. Keratan sulfate proteoglycan during embryonic development of the chick cornea. Dev Biol. 1986;116:267-277.
5. Funderburgh JL, Caterson B, Conrad GW. Distribution of proteoglycans antigenically related to corneal keratan sulfate proteoglycans. J Biol Chem. 1987;262:11634-11640.
6. Cuthbertson RA, Tomarev SI, Piatigorsky J. Taxon-specific recruitment of enzymes as major soluble proteins in the corneal epithelium of three mammals, chicken, and squid. Proc Natl Acad Sci USA. 1992;89:4004-4008.
7. Jester JV, Møller-Pedersen T, Huang J, et al. The cellular basis of corneal transparency: evidence for "corneal crystallins." J Cell Sci. 1999;112:613-622.
8. Coulombre AJ, Coulombre JL. Corneal development. I. Corneal transparency. J Cell Physiol. 1958;51:1-11.
9. Coulombre AJ, Coulombre JL. Corneal development. III. The role of the thyroid in dehydration and the development of transparency. Exp Eye Res. 1964;3:105-114.
10. Prati M, Calvo R, Morreale de Escobar G. L-Thyroxine and 3,5,3′-triiodothryonine concentration in the chicken egg and in the embryo before and after the onset of thyroid function. Endrocrinology. 1992;130:2651-2659.
11. Trunnell JB, Wade P. Factors governing the development of the chick embryo thyroid. II. Chronology of the synthesis of iodinated compounds studied by chromatographic analysis. J Clin Endocrinol Metab. 1955;15:107-117.
12. Sandler B, Webb P, Apriletti JW, et al. Thyroxine-thyroid hormone receptor interactions. J Biol Chem. 2004;279:55801-55808.
13. Sjoberg M, Vennstrom B, Forrest D. Thyroid hormone receptors in chick retinal development: differential expression of mRNAs for α and N-terminal variant β receptors. Development. 1992;114:39-47.
14. Forrest D, Sjoberg M, Vennstrom B. Contrasting developmental and tissue-specific expressions of α and β thyroid hormone receptor genes. EMBO J. 1990;9:1519-1528.
15. Lam SK, Harvey S, Hall TR. In vitro release of triiodothryonine and thyroxine from thyroid glands of the domestic fowl (Gallus domesticus). Gen Comp Endrocrinol. 1986;63:178-185.
16. Darras VM, Mol KA, van der Geyten S, Kuhn ER. Control of peripheral thyroid hormone levels by activating and inactivating deiodinases. Ann N Y Acad Sci. 1998;839:80-86.
17. Leonard JL, Keohrle J. Intracellular pathways of iodothyronine metabolism. In: Braverman LE, Utiger RD, eds. Werner and Ingbar's The Thyroid. 7th ed. New York: Lippincott-Raven Publishers; 1996;125-161.
18. Reyns GE, Venken K, Morreale de Escobar G, Kuhn ER, Darras VM. Dynamics and regulation of intracellular thyroid hormone concentrations in embryonic chicken liver, kidney, brain, and blood. Gen Comp Endrocrinol. 2003;134:80-87.
19. Bianco AC, Salvatore D, Gereben B, Berry MJ, Larsen PR. Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocrine Reviews. 2002;23:38-89.
20. Conrad AH, Conrad GW. The keratocan gene is expressed in both ocular and non-ocular tissues during early chick development. Matrix Biol. 2003;22:323-337.
21. Blochberger TC, Vergnes JP, Hempel J, Hassell JR. cDNA to chick lumican (corneal keratan sulfate proteoglycan) reveals homology to the small intestinal proteoglycan gene family and expression in muscle and intestine. J Biol Chem. 1992;267:347-352.
22. Corpuz LM, Funderburgh JL, Funderburgh ML, Bottomley GS, Prakash S, Conrad GW. Molecular cloning and tissue distribution of keratocan: bovine corneal keratan sulfate proteoglycan 37A. J Biol Chem. 1996;271:9759-9763.
23. Funderburgh JL, Corpuz LM, Roth MR, et al. Mimecan, the 25-kDa corneal keratan sulfate proteoglycan, is a product of the gene producing osteoglycin. J Biol Chem. 1997;272:28089-28095.
24. Dunlevy JR, Beales MP, Berryhill BL, Cornuet PK, Hassell JR. Expression of the keratan sulfate proteoglycans lumican, keratocan, osteoglycin/mimecan during chick corneal development. Exp Eye Res. 2000;70:349-362.
25. Iozzo RV. The biology of the small leucine-rich proteoglycans: functional network of interactive proteins. J Biol Chem. 1999;274:18843-18846.
26. Tasheva ES, Koester A, Paulsen AQ, et al. Mimecan/osteoglycin-deficient mice have collagen fibril abnormalities. Mol Vis. 2002;8:407-415.
27. Conrad GW. Biological roles of keratan sulfate proteoglycans. In: Ernst B, Hart GW, Sinay P. Carbohydrates in Chemistry and Biology. Vol 4: Part II. Biology of Saccharides. Lectins and Saccharides Biology. Weinheim, Germany: Wiley-VCH, Weinheim; 2000:717-727.
28. Chakravarti S. The cornea through the eyes of knockout mice. Exp Eye Res. 2001;73:411-419.
29. Hart GW, Lennarz WJ. Effects of tunicamycin on the biosynthesis of glycosaminoglycans by embryonic chick cornea. J Biol Chem. 1978;253:5795-5801.
30. Funderburgh JL. Keratan sulfate biosynthesis. IUBMB Life. 2002;54:187-194.
31. Funderburgh JL. Keratan sulfate: structure, biosynthesis, and function. Glycobiology. 2000;10:951-958.
32. Hart GW. Glycosaminoglycan sulfotransferases of the developing chick cornea. J Cell Biol. 1978;72:347-353.
33. Conrad GW, Woo M-L. Synthesis of 3′-phosphoadenosine-5′- phosphosulfate (PAPS) increases during corneal development. J Biol Chem. 1980;255:3086-3091.
34. Zhang Y, Conrad AH, Tasheva ES, et al. Detection and quantification of sulfated disaccharides from keratan sulfate and chondroitin/dermatan sulfate during chick corneal development by ESI-MS/MS. Invest Ophthalmol Vis Sci. 2005;46:1604-1614.
35. Piatigorsky J. Review: a case for corneal crystallins. J Ocul Pharmacol Ther. 2000;16:173-180.
36. Piatigorsky J, Wistow G. Enzyme/crystallins: gene sharing as an evolutionary strategy. Cell. 1989;57:197-199.
37. Masterson E, Edelhauser HF, Van Horn DL. Development of corneal transparency in embryonic chick: influence of exogenous thyroxine and thiouracil on structure, water, and electrolyte content. Dev Biol. 1975;43:233-239.
38. Kaye GI, Tice LW. Studies on the cornea. V. Electron microscopic localization of adenosine triphosphatase activity in the rabbit cornea in relation to transport. Invest Ophthalmol. 1966;5:22-31.
39. Leuenberger PM, Novikoff AB. Localization of transport adenosine triphosphatase in rat cornea. J Cell Biol. 1974;60:721-731.
40. Wigham C, Hodson S. The movement of sodium across short-circuited rabbit corneal endothelium. Curr Eye Res. 1985;4:1241-1245.
41. Swan JS, Hodson SA. Rabbit corneal hydration and the bicarbonate pump. J Membr Biol. 2004;201:33-40.
42. Bonanno JA. Identity and regulation of ion transport mechanisms in the corneal endothelium. Prog Retin Eye Res. 2003;22:69-94.
43. Sterling D, Reithmeier RAF, Casey JR. Carbonic anhydrase: in the driver's seat for bicarbonate transport. Journal of the Pancreas. 2001;2(4 suppl):165-170.
44. Beckenhauer DM, Conrad GW. The effect of thyroxine on transparency and PAPS synthesis in the avian cornea. Dev Biol. 1981;84:225-229.
45. Henrique D, Adam J, Myat A, Chitnis A, Lewis J, Ish-Horowicz D. Expression of a Delta homologue in prospective neurons in the chick. Nature. 1995;375:787-790.
46. Moorman AFM, Houweling AC, de Boer PAJ, Christoffels VM. Sensitive nonradioactive determination of mRNA in tissue sections: novel application of the whole-mount in situ hybridization protocol. J Histochem Cytochem. 2001;49:1-8.
47. Boardman PE, Sanz-Ezquerro J, Overton IM, et al. A comprehensive collection of chicken cDNAs. Curr Biol. 2002;12:1965-1969.
48. Puymirat J, Etongue-Mayer P, Dussault JH. Thyroid hormones stabilize acetylcholinesterase mRNA in neuro-2A cells that overexpress the beta 1 thyroid receptor. J Biol Chem. 1995;270:30651-30656.
49. Sturges SA, Conrad GW. Acetylcholinesterase activity in the cornea of the developing chick embryo. Invest Ophthalmol Vis Sci. 1987;28:850-858.
50. Tenbaum SP, Juenemann S, Schlitt T, et al. Alien/CSN2 gene expression is regulated by thyroid hormone in rat brain. Dev Biol. 2003;254:149-160.
51. Wang Y, Zhang Y, Hillgartner FB. Chicken ovalbumin upstream-promoter transcription factor and E-box-binding proteins enhance thyroid-hormone responsiveness of the malic enzyme gene in avian hepatocytes. Biochem J. 2002;361:391-400.
52. Chakravarti S, Magnuson T, Lass JH, Jepsen KJ, LaMantia C, Carroll H. Lumican regulates collagen fibril assembly: skin fragility and corneal opacity in the absence of lumican. J Cell Biol. 1998;141:1277-1286.
53. Eckey M, Moehren U, Baniahmad A. Gene silencing by the thyroid hormone receptor. Mol Cell Endocrinol. 2002;213:13-22.
54. Harvey CB, Williams GR. Mechanism of thyroid hormone action. Thyroid. 2002;12:441-446.
55. Rietveld LE, Caldenhoven E, Stunnenberg HG. In vivo repression of an erythroid-specific gene by distinct corepressor complexes. EMBO J. 2003;21:1389-1397.
56. Suzuki S, Miyamoto T, Opsahl A, Sakurai A, DeGroot LJ. Two thyroid hormone response elements are present in the promoter of human thyroid hormone receptor beta 1. Mol Endocrinol. 1994;8:305-314.
57. Machuca I, Esslemont G, Fairclough L, Tata JR. Analysis of structure and expression of the Xenopus thyroid hormone receptor-beta gene to explain its autoinduction. Mol Endocrinol. 1995;9:96-107.
58. Lee A, Beck L, Markovich D. The mouse sulfate anion transporter gene Sat1 (Slc26a1): cloning, tissue distribution, gene structure, functional characterization, and transcriptional regulation by thyroid hormone. DNA Cell Biol. 2003;22:19-31.
59. Ciana P, Braliou GG, Demay FG, et al. Leukemic transformation by the v-ErbA oncoprotein entails constitutive binding to and repression of an erythroid enhancer in vivo. EMBO J. 1998;17:7382-7394.
60. Bassett JH, Harvey CB, Williams GR. Mechanisms of thyroid hormone receptor-specific nuclear and extra nuclear actions. Mol Cell Endocrinol. 2003;213:1-11.
61. Ridderstrale Y, Wistrand PJ, Brechue WF. Membrane-associated CA activity in the eye of the CA II-deficient mouse. Invest Ophthalmol Vis Sci. 1994;35:2577-2584.
62. Hageman GS, Zhu ZL, Waheed A, Sly WS. Localization of carbonic anhydrase IV in a specific capillary bed of the human eye. Proc Natl Acad Sci USA. 1991;88:2716-2720.
63. Sterling D, Reithmeier RA, Casey JR. A transport metabolon; functional interaction of carbonic anhydrase II and chloride/bicarbonate exchangers. J Biol Chem. 2001;276:47886-47894.
64. Amma LL, Campos-Barros A, Wang Z, Vennstrom B, Forrest D. Distinct tissue-specific roles for thyroid hormone receptors β and α1 in regulation of type I deiodinase expression. Mol Endocrinol. 2001;15:467-475.
65. Martinez-deMena R, Hernandez A, Obregon MJ. Triiodothyronine is required for the stimulation of type II 5′-deiodinase mRNA in rat brown adipocytes. Am J Physiol Endocrinol Metab. 2002;282:E1119-E1127.
66. Hernandez A, Obregon M-J. Presence and mRNA expression of T3 receptors in differentiating rat brown adipocytes. Mol Cell Endocrinol. 1996;121:347-346.
67. Murray MB, Zila ND, McCreary NL, MacDonald MJ, Towle HC. Isolation and characterization of rat cDNA clones for two distinct thyroid hormone receptors. J Biol Chem. 1988;263:12770-12777.
68. Williams GR. Cloning and characterization of two novel thyroid hormone receptor β isoforms. Mol Cell Biol. 2000;20:8329-8342.
69. Harvey CB, Williams GR. Thyroid hormone receptor (TR) activity is modulated by TRdeltabeta3 in a cell-, response element-, and TR isoform-specific manner. Endocrine Abstr. 2003;5:254.
70. Frankton S, Harvey CB, Gleason LM, Fadel A, Williams GR. Multiple messenger ribonucleic acid variants regulate cell-specific expression of human thyroid hormone receptor beta1. Mol Endocrinol. 2004;18:1631-1642.
71. Norman B, Davis J, Piatigorsky J. Postnatal gene expression in the normal mouse cornea by SAGE. Invest Ophthalmol Vis Sci. 2004;45:429-440.
72. Mitsuhashi T, Tennyson GE, Nikodem VM. Alternative splicing generates messages encoding rat c-erbA proteins that do not bind thyroid hormone. Proc Natl Acad Sci USA. 1988;85:5804-5808.
73. Mitsuhashi T, Nikodem VM. Regulation of expression of the alternative mRNAs of the α-thyroid hormone receptor gene. J Biol Chem. 1989;264:8900-8904.
74. Chassande O, Fraichard A, Gauthier K, et al. Identification of transcripts initiated from an internal promoter in the c-erbAα locus that encode inhibitors of retinoic acid receptor-α and triiodothyronine receptor activities. Mol Endocrinol. 1997;11:1278-1290.
75. Thompson CC, Weinberger C, Lebo R, Evans RM. Identification of a novel thyroid hormone receptor expressed in the mammalian central nervous system. Science. 1987;237:1610-1614.
76. Oppenheimer JH, Schwartz HL, Surks MI. Tissue differences in the concentration of triiodothyronine nuclear binding sites in the rat: liver, kidney, pituitary, heart, brain, spleen, and testis. Endocrinology. 1974;95:897-903.
77. Dressel U, Thormeyer D, Altincicek B, et al. Alien, a highly conserved protein with characteristics of a corepressor for members of the nuclear hormone receptor superfamily. Mol Cell Biol. 1999;19:3383-3394.
78. Feng X, Jiang Y, Meltzer P, Yen PM. Thyroid hormone regulation of hepatic genes in vivo detected by complementary DNA microarray. Mol Endocrinol. 2000;14:947-955.
79. Moeller LC, Dumitrescu AM, Walker RL, Meltzer PS, Refetoff S. Thyroid hormone responsive genes in cultured human fibroblasts. J Clin Endocrinol Metab. 2005;90:936-943.
80. Li X, Zelenka PS, Piatigorsky J. Differential expression of the two delta-crystallin genes in lens and non-lens tissues: shift favoring delta 2 expression from embryonic to adult chickens. Dev Dyn. 1993;196:114-123.