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Liganded T3 receptor β2 inhibits the positive feedback autoregulation of the gene for GATA2, a transcription factor critical for thyrotropin production

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Hirahara, Naoko, Nakamura, Hiroko Misawa, Sasaki, Shigekazu, Matsushita, Akio, Ohba, Kenji, Kuroda, Go, Sakai, Yuki, Shinkai, Shinsuke +5 more·2020·PLOS ONE
DOI 10.1371/journal.pone.0227646PMC PMC6961892
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Abstract

The serum concentration of thyrotropin (thyroid stimulating hormone, TSH) is drastically reduced by small increase in the levels of thyroid hormones (T3 and its prohormone, T4); however, the mechanism underlying this relationship is unknown. TSH consists of the chorionic gonadotropin α (CGA) and the β chain (TSHβ). The expression of both peptides is induced by the transcription factor GATA2, a determinant of the thyrotroph and gonadotroph differentiation in the pituitary. We previously reported that the liganded T3 receptor (TR) inhibits transactivation activity of GATA2 via a tethering mechanism and proposed that this mechanism, but not binding of TR with a negative T3-responsive element, is the basis for the T3-dependent inhibition of the TSHβ and CGA genes. Multiple GATA-responsive elements (GATA-REs) also exist within the GATA2 gene itself and mediate the positive feedback autoregulation of this gene. To elucidate the effect of T3 on this non-linear regulation, we fused the GATA-REs at -3.9 kb or +9.5 kb of the GATA2 gene with the chloramphenicol acetyltransferase reporter gene harbored in its 1S-promoter. These constructs were co-transfected with the expression plasmids for GATA2 and the pituitary specific TR, TRβ2, into kidney-derived CV1 cells. We found that liganded TRβ2 represses the GATA2-induced transactivation of these reporter genes. Multi-dimensional input function theory revealed that liganded TRβ2 functions as a classical transcriptional repressor. Then, we investigated the effect of T3 on the endogenous expression of GATA2 protein and mRNA in the gonadotroph-derived LβT2 cells. In this cell line, T3 reduced GATA2 protein independently of the ubiquitin proteasome system. GATA2 mRNA was drastically suppressed by T3, the concentration of which corresponds to moderate hypothyroidism and euthyroidism. These results suggest that liganded TRβ2 inhibits the positive feedback autoregulation of the GATA2 gene; moreover this mechanism plays an important role in the potent reduction of TSH production by T3.

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  • T3 represses transcription of the TSHβ subunit in pituitary thyrotrophs by inhibiting via TRβ2 the autoregulation of GATA2.

    “In the pituitary thyrotrophs, T3 represses the transcription of the TSHβ subunit by inhibiting via TRβ2 the autoregulation of GATA2, a key transcription factor that mediates the TRH-stimulated TSH production (18).”

    From Intrathyroidal feedforward and feedback network regulating thyroid hormone synthesis and secretion (2022) · cites this paper as [18]

    The Discussion (Fig. 7) says liganded TRβ2 inhibits TSHβ transcription and suggests that it also inhibits GATA2 positive-feedback autoregulation. The Abstract reports the autoregulation experiments in kidney-derived CV1 cells and the T3 response in gonadotroph-derived LβT2 cells. The proposed causal route is therefore supported, but the claim presents it as established in pituitary thyrotrophs rather than as a mechanism suggested by those experiments. (LLM, conf=0.84)

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Cited by

Sorted by citations

Authors
Hirahara, N., Nakamura, H. M., Sasaki, S., Matsushita, A., Ohba, K., Kuroda, G., Sakai, Y., Shinkai, S., Haeno, H., Nishio, T., Yoshida, S., Oki, Y., & Suda, T.
Affiliations
  • Shizuoka Red Cross Hospital (JP)
  • Hamamatsu University School of Medicine (JP)
  • The University of Tokyo (JP)
  • Hamamatsu University (JP)
Corresponding author
Sasaki, Shigekazu
ORCID
Venue
PLOS ONE
Publisher
Public Library of Science (PLoS)
Published
2020-01-15
Volume
15
Issue
1
Pages
e0227646
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0227646
PMC
PMC6961892
OpenAlex
W2999874021
Cited by
9
References
5
Citations by year
2026: 2 · 2025: 3 · 2023: 1 · 2022: 1 · 2021: 1 · 2020: 1
FWCI
0.73
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
The Ministry of Education, Culture, Sports, Science and Technology of Japan (Aid for Scientific Research 24590689)
Topics
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Disorders and Treatments
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords
GATA2, thyroid-stimulating hormone, transcriptional repression, gonadotrophs, thyroid hormone regulation, hypothyroidism, LβT2 cells, transcriptional repressor
MeSH terms
Animals, Cell Line, Gene Expression Regulation, Homeostasis, Ligands, Promoter Regions, Genetic, Receptors, Thyroid Hormone, Thyroid Hormones, Thyrotropin, Transcription Factors, Triiodothyronine, Glycoprotein Hormones, alpha Subunit, Transcriptional Activation, Genes, Reporter, Thyrotropin, beta Subunit, GATA2 Transcription Factor, Mice, Rats, Thyrotrophs

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