Autoregulation of Thyroid-Specific Gene Transcription by Thyroglobulin
Thyroglobulin (TG), the primary synthetic product of the thyroid, is the macromolecular precursor of thyroid hormones. TG synthesis, iodination, storage in follicles, and degradation control thyroid hormone formation and secretion into the circulation. Thyrotropin (TSH), via its receptor (TSHR), inc...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 1998-07, Vol.95 (14), p.8251-8256 |
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| creator | Suzuki, Koichi Lavaroni, Stefano Mori, Atsumi Ohta, Masanori Saito, Jun Pietrarelli, Michele Singer, Dinah S. Kimura, Shioko Katoh, Ryohei Kawaoi, Akira Kohn, Leonard D. |
| description | Thyroglobulin (TG), the primary synthetic product of the thyroid, is the macromolecular precursor of thyroid hormones. TG synthesis, iodination, storage in follicles, and degradation control thyroid hormone formation and secretion into the circulation. Thyrotropin (TSH), via its receptor (TSHR), increases thyroid hormone levels by upregulating expression of the sodium iodide symporter (NIS), thyroid peroxidase (TPO), and TG genes. TSH does this by modulating the expression and activity of several thyroid-specific transcription factors, thyroid transcription factor (TTF)-1, TTF-2, and Pax-8, which coordinately regulate NIS, TPO, TG, and the TSHR. Major histocompatibility complex class I gene expression, which also is regulated by TTF-1 and Pax-8 in the thyroid, is decreased simultaneously. This helps maintain self-tolerance in the face of TSH-increased gene products necessary for thyroid hormone formation. In this report we show that follicular TG counter-regulates TSH-increased, thyroid-specific gene transcription by suppressing expression of the TTF-1, TTF-2, and Pax-8 genes. This decreases expression of the TG, TPO, NIS, and TSHR genes, but increases class I expression. TG acts transcriptionally, targeting, for example, a sequence within 1.15 kb of the 5′flanking region of TTF-1. TG does not affect ubiquitous transcription factors regulating TG, TPO, NIS, and/or TSHR gene expression. The inhibitory effect of TG on gene expression is not duplicated by thyroid hormones or iodide and may be mediated by a TG-binding protein on the apical membrane. We hypothesize that TG-initiated, transcriptional regulation of thyroid-restricted genes is a normal, feedback, compensatory mechanism that limits follicular function and contributes to follicular heterogeneity. |
| doi_str_mv | 10.1073/pnas.95.14.8251 |
| format | Article |
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TG synthesis, iodination, storage in follicles, and degradation control thyroid hormone formation and secretion into the circulation. Thyrotropin (TSH), via its receptor (TSHR), increases thyroid hormone levels by upregulating expression of the sodium iodide symporter (NIS), thyroid peroxidase (TPO), and TG genes. TSH does this by modulating the expression and activity of several thyroid-specific transcription factors, thyroid transcription factor (TTF)-1, TTF-2, and Pax-8, which coordinately regulate NIS, TPO, TG, and the TSHR. Major histocompatibility complex class I gene expression, which also is regulated by TTF-1 and Pax-8 in the thyroid, is decreased simultaneously. This helps maintain self-tolerance in the face of TSH-increased gene products necessary for thyroid hormone formation. In this report we show that follicular TG counter-regulates TSH-increased, thyroid-specific gene transcription by suppressing expression of the TTF-1, TTF-2, and Pax-8 genes. This decreases expression of the TG, TPO, NIS, and TSHR genes, but increases class I expression. TG acts transcriptionally, targeting, for example, a sequence within 1.15 kb of the 5′flanking region of TTF-1. TG does not affect ubiquitous transcription factors regulating TG, TPO, NIS, and/or TSHR gene expression. The inhibitory effect of TG on gene expression is not duplicated by thyroid hormones or iodide and may be mediated by a TG-binding protein on the apical membrane. We hypothesize that TG-initiated, transcriptional regulation of thyroid-restricted genes is a normal, feedback, compensatory mechanism that limits follicular function and contributes to follicular heterogeneity.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.95.14.8251</identifier><identifier>PMID: 9653173</identifier><language>eng</language><publisher>United States: National Academy of Sciences of the United States of America</publisher><subject>Animals ; Autocrine Communication - genetics ; Biological Sciences ; Cells, Cultured ; DNA-Binding Proteins - genetics ; Follicles ; Forkhead Transcription Factors ; Gene Expression Regulation ; Genes ; Histocompatibility Antigens Class I - genetics ; Hormones ; Iodides ; Medical research ; Messenger RNA ; Nuclear Proteins - genetics ; Paired Box Transcription Factors ; PAX8 Transcription Factor ; Rats ; Repressor Proteins - genetics ; RNA ; Thyroglobulin - physiology ; Thyroid gland ; Thyroid Gland - physiology ; Thyroid hormones ; Thyroid Hormones - genetics ; Thyroid Hormones - metabolism ; Thyroid Nuclear Factor 1 ; Trans-Activators - genetics ; Transcription factors ; Transcription Factors - genetics ; Transcription, Genetic ; Transcriptional regulatory elements ; Ungulates</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 1998-07, Vol.95 (14), p.8251-8256</ispartof><rights>Copyright 1993-1998 National Academy of Sciences</rights><rights>Copyright National Academy of Sciences Jul 7, 1998</rights><rights>Copyright © 1998, The National Academy of Sciences 1998</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c586t-877f1b063320e11fe10fbdc7fc8b4e17c5c2f1367a96c71e82452f7388020863</citedby><cites>FETCH-LOGICAL-c586t-877f1b063320e11fe10fbdc7fc8b4e17c5c2f1367a96c71e82452f7388020863</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/95/14.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/45735$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/45735$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,315,729,782,786,805,887,27931,27932,53798,53800,58024,58257</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/9653173$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Suzuki, Koichi</creatorcontrib><creatorcontrib>Lavaroni, Stefano</creatorcontrib><creatorcontrib>Mori, Atsumi</creatorcontrib><creatorcontrib>Ohta, Masanori</creatorcontrib><creatorcontrib>Saito, Jun</creatorcontrib><creatorcontrib>Pietrarelli, Michele</creatorcontrib><creatorcontrib>Singer, Dinah S.</creatorcontrib><creatorcontrib>Kimura, Shioko</creatorcontrib><creatorcontrib>Katoh, Ryohei</creatorcontrib><creatorcontrib>Kawaoi, Akira</creatorcontrib><creatorcontrib>Kohn, Leonard D.</creatorcontrib><title>Autoregulation of Thyroid-Specific Gene Transcription by Thyroglobulin</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Thyroglobulin (TG), the primary synthetic product of the thyroid, is the macromolecular precursor of thyroid hormones. TG synthesis, iodination, storage in follicles, and degradation control thyroid hormone formation and secretion into the circulation. Thyrotropin (TSH), via its receptor (TSHR), increases thyroid hormone levels by upregulating expression of the sodium iodide symporter (NIS), thyroid peroxidase (TPO), and TG genes. TSH does this by modulating the expression and activity of several thyroid-specific transcription factors, thyroid transcription factor (TTF)-1, TTF-2, and Pax-8, which coordinately regulate NIS, TPO, TG, and the TSHR. Major histocompatibility complex class I gene expression, which also is regulated by TTF-1 and Pax-8 in the thyroid, is decreased simultaneously. This helps maintain self-tolerance in the face of TSH-increased gene products necessary for thyroid hormone formation. In this report we show that follicular TG counter-regulates TSH-increased, thyroid-specific gene transcription by suppressing expression of the TTF-1, TTF-2, and Pax-8 genes. This decreases expression of the TG, TPO, NIS, and TSHR genes, but increases class I expression. TG acts transcriptionally, targeting, for example, a sequence within 1.15 kb of the 5′flanking region of TTF-1. TG does not affect ubiquitous transcription factors regulating TG, TPO, NIS, and/or TSHR gene expression. The inhibitory effect of TG on gene expression is not duplicated by thyroid hormones or iodide and may be mediated by a TG-binding protein on the apical membrane. We hypothesize that TG-initiated, transcriptional regulation of thyroid-restricted genes is a normal, feedback, compensatory mechanism that limits follicular function and contributes to follicular heterogeneity.</description><subject>Animals</subject><subject>Autocrine Communication - genetics</subject><subject>Biological Sciences</subject><subject>Cells, Cultured</subject><subject>DNA-Binding Proteins - genetics</subject><subject>Follicles</subject><subject>Forkhead Transcription Factors</subject><subject>Gene Expression Regulation</subject><subject>Genes</subject><subject>Histocompatibility Antigens Class I - genetics</subject><subject>Hormones</subject><subject>Iodides</subject><subject>Medical research</subject><subject>Messenger RNA</subject><subject>Nuclear Proteins - genetics</subject><subject>Paired Box Transcription Factors</subject><subject>PAX8 Transcription Factor</subject><subject>Rats</subject><subject>Repressor Proteins - genetics</subject><subject>RNA</subject><subject>Thyroglobulin - physiology</subject><subject>Thyroid gland</subject><subject>Thyroid Gland - physiology</subject><subject>Thyroid hormones</subject><subject>Thyroid Hormones - genetics</subject><subject>Thyroid Hormones - metabolism</subject><subject>Thyroid Nuclear Factor 1</subject><subject>Trans-Activators - genetics</subject><subject>Transcription factors</subject><subject>Transcription Factors - genetics</subject><subject>Transcription, Genetic</subject><subject>Transcriptional regulatory elements</subject><subject>Ungulates</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1998</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFks1vEzEUxC0EKmnhjIQEijjAadPnb1viUlVtQarEgdwtr2Onjjbrxd6tyH-PQ6KocIDTO8xvxs8eI_QGwwKDpJdDb8tC8wVmC0U4foZmGDRuBNPwHM0AiGwUI-wlOi9lAwCaKzhDZ1pwiiWdoduraUzZr6fOjjH18xTmy4ddTnHVfB-8iyG6-Z3v_XyZbV9cjsNvrN0dsHWX2qmL_Sv0Itiu-NfHeYGWtzfL6y_N_be7r9dX943jSoyNkjLgFgSlBDzGwWMI7crJ4FTLPJaOOxIwFdJq4ST2ijBOgqRKAQEl6AX6fIgdpnbrV873Y7adGXLc2rwzyUbzp9LHB7NOj4aAFqTaPx7tOf2YfBnNNhbnu872Pk3FSK0V5wT-C2LBJNegK_jhL3CTptzXJ6hHYiqF4rRClwfI5VRK9uG0MAazb9HsWzSaG8zMvsXqePf0nif-WFvV3x_1vfGkPg349E_AhKnrRv9zrOTbA7kp9SOcUMYl5fQX7hS5-A</recordid><startdate>19980707</startdate><enddate>19980707</enddate><creator>Suzuki, Koichi</creator><creator>Lavaroni, Stefano</creator><creator>Mori, Atsumi</creator><creator>Ohta, Masanori</creator><creator>Saito, Jun</creator><creator>Pietrarelli, Michele</creator><creator>Singer, Dinah S.</creator><creator>Kimura, Shioko</creator><creator>Katoh, Ryohei</creator><creator>Kawaoi, Akira</creator><creator>Kohn, Leonard D.</creator><general>National Academy of Sciences of the United States of America</general><general>National Acad Sciences</general><general>National Academy of Sciences</general><general>The National Academy of Sciences</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>19980707</creationdate><title>Autoregulation of Thyroid-Specific Gene Transcription by Thyroglobulin</title><author>Suzuki, Koichi ; 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TG synthesis, iodination, storage in follicles, and degradation control thyroid hormone formation and secretion into the circulation. Thyrotropin (TSH), via its receptor (TSHR), increases thyroid hormone levels by upregulating expression of the sodium iodide symporter (NIS), thyroid peroxidase (TPO), and TG genes. TSH does this by modulating the expression and activity of several thyroid-specific transcription factors, thyroid transcription factor (TTF)-1, TTF-2, and Pax-8, which coordinately regulate NIS, TPO, TG, and the TSHR. Major histocompatibility complex class I gene expression, which also is regulated by TTF-1 and Pax-8 in the thyroid, is decreased simultaneously. This helps maintain self-tolerance in the face of TSH-increased gene products necessary for thyroid hormone formation. In this report we show that follicular TG counter-regulates TSH-increased, thyroid-specific gene transcription by suppressing expression of the TTF-1, TTF-2, and Pax-8 genes. This decreases expression of the TG, TPO, NIS, and TSHR genes, but increases class I expression. TG acts transcriptionally, targeting, for example, a sequence within 1.15 kb of the 5′flanking region of TTF-1. TG does not affect ubiquitous transcription factors regulating TG, TPO, NIS, and/or TSHR gene expression. The inhibitory effect of TG on gene expression is not duplicated by thyroid hormones or iodide and may be mediated by a TG-binding protein on the apical membrane. We hypothesize that TG-initiated, transcriptional regulation of thyroid-restricted genes is a normal, feedback, compensatory mechanism that limits follicular function and contributes to follicular heterogeneity.</abstract><cop>United States</cop><pub>National Academy of Sciences of the United States of America</pub><pmid>9653173</pmid><doi>10.1073/pnas.95.14.8251</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Autocrine Communication - genetics Biological Sciences Cells, Cultured DNA-Binding Proteins - genetics Follicles Forkhead Transcription Factors Gene Expression Regulation Genes Histocompatibility Antigens Class I - genetics Hormones Iodides Medical research Messenger RNA Nuclear Proteins - genetics Paired Box Transcription Factors PAX8 Transcription Factor Rats Repressor Proteins - genetics RNA Thyroglobulin - physiology Thyroid gland Thyroid Gland - physiology Thyroid hormones Thyroid Hormones - genetics Thyroid Hormones - metabolism Thyroid Nuclear Factor 1 Trans-Activators - genetics Transcription factors Transcription Factors - genetics Transcription, Genetic Transcriptional regulatory elements Ungulates |
| title | Autoregulation of Thyroid-Specific Gene Transcription by Thyroglobulin |
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