Role of the GATA Family of Transcription Factors in Endocrine Development, Function, and Disease
Open accessAbstract
The WGATAR motif is a common nucleotide sequence found in the transcriptional regulatory regions of numerous genes. In vertebrates, these motifs are bound by one of six factors (GATA1 to GATA6) that constitute the GATA family of transcriptional regulatory proteins. Although originally considered for their roles in hematopoietic cells and the heart, GATA factors are now known to be expressed in a wide variety of tissues where they act as critical regulators of cell-specific gene expression. This includes multiple endocrine organs such as the pituitary, pancreas, adrenals, and especially the gonads. Insights into the functional roles played by GATA factors in adult organ systems have been hampered by the early embryonic lethality associated with the different Gata-null mice. This is now being overcome with the generation of tissue-specific knockout models and other knockdown strategies. These approaches, together with the increasing number of human GATA-related pathologies have greatly broadened the scope of GATA-dependent genes and, importantly, have shown that GATA action is not necessarily limited to early development. This has been particularly evident in endocrine organs where GATA factors appear to contribute to the transcription of multiple hormone-encoding genes. This review provides an overview of the GATA family of transcription factors as they relate to endocrine function and disease.
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GATA4 is a zinc finger transcription factor essential for development of several organs, including heart, testis, foregut, liver, and ventral pancreas.
“GATA4 is a zinc finger transcription factor essential for the development of various organs, including heart, testis, foregut, liver, and ventral pancreas (37).”
From The DNA damage response induces inflammation and senescence by inhibiting autophagy of GATA4. (2015) · cites this paper as [37]
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Self-citationNovel roles for GATA transcription factors in the regulation of steroidogenesis
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Androgens and Postmeiotic Germ Cells Regulate Claudin-11 Expression in Rat Sertoli Cells
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Differential Expression of GATA-4 and GATA-6 in Fetal and Adult Mouse and Human Adrenal Tissue
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Self-citationModification of GATA-2 Transcriptional Activity in Endothelial Cells by the SUMO E3 Ligase PIASy
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In Vivo Regulation of Grp78/BiP Transcription in the Embryonic Heart
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Self-citationActivation of GATA-4 by Serotonin in Pulmonary Artery Smooth Muscle Cells
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GATA‐4 is required for sex steroidogenic cell development in the fetal mouse
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Self-citationConvergence of Protein Kinase C and JAK-STAT Signaling on Transcription Factor GATA-4
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Modification of the erythroid transcription factor GATA-1 by SUMO-1
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Temporal and Spatial Localization Patterns of Gata4 During Porcine Gonadogenesis1
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Gata4 Regulates Testis Expression of Dmrt1
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Self-citationCyclin D2 and p27 Are Tissue-Specific Regulators of Tumorigenesis in Inhibin α Knockout Mice
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GATA-4 is a granulosa cell factor employed in inhibin-α activation by the TGF-β pathway
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Self-citationThe 25th Volume: Role of the GATA Family of Transcription Factors in Andrology
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Self-citationProstaglandin E2 increases cyp19 expression in rat granulosa cells: Implication of GATA-4
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Expression of GATA-2 in Human Pituitary Adenomas
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Involvement of GATA-4/-5 transcription factors in ovarian carcinogenesis
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Self-citationTranscription factors GATA-6, SF-1, and cell proliferation in human adrenocortical tumors
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Expression of GATA-4 in migrating gonadotropin-releasing neurons of the developing mouse
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Ho, C. K. M., Wood, J. R., Stewart, D. R., Ewens, K. G., Ankener, W., Wickenheisser, J. K., Nelson-DeGrave, V. L., Zhang, Z., Legro, R. S., Dunaif, A. E., et al. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-0890 · Cited by 36 · see citing works
Perlman, S., Bouquin, T., van den Hazel, B., Jensen, T. H., Schambye, H. T., Knudsen, S., & Okkels, J. S. (2006) · Molecular Human Reproduction · doi:10.1093/molehr/gah247 · Cited by 36 · see citing works
Steger, D. J., Hecht, J. H., & Mellon, P. L. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.8.5592-5602.1994 · Cited by 36 · see citing works
Adachi, M., Tachibana, K., Asakura, Y., & Tsuchiya, T. (2006) · Journal of Pediatric Endocrinology and Metabolism · doi:10.1515/jpem.2006.19.1.87 · Cited by 35 · see citing works
LRH-1/NR5A2 cooperates with GATA factors to regulate inhibin α-subunit promoter activity
Robert, N. M., Miyamoto, Y., Taniguchi, H., & Viger, R. S. (2006) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2006.06.011 · Cited by 35 · see citing works
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- Onodera K, Yomogida K, Suwabe N, Takahashi S, Muraosa Y, Hayashi N, Ito E, Gu L, Rassoulzadegan M, Engel JD, Yamamoto M 1997 Conserved structure, reg- 794 Mol Endocrinol, April 2008, 22(4):781-798
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Sorted by citations
The DNA damage response induces inflammation and senescence by inhibiting autophagy of GATA4.
Kang, C., Xu, Q., Martin, T. D., Li, M. Z., Demaria, M., Aron, L., Lu, T., Yankner, B. A., Campisi, J., & Elledge, S. J. (2015) · Science · doi:10.1126/science.aaa5612 · Cited by 982 · see citing works
Decreased expression of synapse-related genes and loss of synapses in major depressive disorder
Kang, H. J., Voleti, B., Hajszan, T., Rajkowska, G., Stockmeier, C. A., Licznerski, P., Lepack, A., Majik, M. S., Jeong, L. S., Banasr, M., et al. (2012) · Nature Medicine · doi:10.1038/nm.2886 · Cited by 808 · see citing works
The Emerging Field of Human Social Genomics
Slavich, G. M., & Cole, S. W. (2013) · Clinical Psychological Science · doi:10.1177/2167702613478594 · Cited by 523 · see citing works
Volkmar, M., Dedeurwaerder, S., Cunha, D. A., Ndlovu, M. N., Defrance, M., Deplus, R., Calonne, E., Volkmar, U., Igoillo‐Esteve, M., Naamane, N., et al. (2012) · The EMBO Journal · doi:10.1038/emboj.2011.503 · Cited by 420 · see citing works
“Interestingly, the GATA transcription factor family members are critical regulators in endocrine development, function and pathologies (Viger et al , 2008).”
Anjali, Kumar, S., Korra, T., Thakur, R., Arutselvan, R., Kashyap, A. S., Nehela, Y., Chaplygin, V. A., Minkina, T., & Keswani, C. (2023) · Plant Stress · doi:10.1016/j.stress.2023.100154 · Cited by 390 · see citing works
Kaimal, V., Bardes, E. E., Tabar, S., Jegga, A. G., & Aronow, B. J. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq418 · Cited by 369 · see citing works
“The pancreas-specific genes show enrichment for the transcription factor GATA1, which is known to be involved in cell-specific regulation of genes in multiple endocrine organs including the pancreas (28).”
BackgroundStow, L. R., Jacobs, M. E., Wingo, C. S., & Cain, B. D. (2010) · The FASEB Journal · doi:10.1096/fj.10-161612 · Cited by 253 · see citing works
“dermal and endodermal derived tissues (104).”
Molecular Pathogenesis of Granulosa Cell Tumors of the Ovary
Jamieson, S., & Fuller, P. J. (2012) · Endocrine Reviews · doi:10.1210/er.2011-0014 · Cited by 199 · see citing works
“Indeed, GATA-4 has been shown to regulate the sex-determining genes SRY (sexdetermining region Y chromosome), SOX9 (SRY-box containing gene 9), and MIS as well as key steroidogenic factors in the ovary, including steroidogenic acute regulatory protein (StAR), P450 aromatase (CYP19A1), the inhibin -subunit (INHA), and…”
BackgroundMolecular regulation of steroidogenesis in endocrine Leydig cells
Tremblay, J. (2015) · Steroids · doi:10.1016/j.steroids.2015.08.001 · Cited by 196 · see citing works
At the Crossroads of Fate—Somatic Cell Lineage Specification in the Fetal Gonad
Rotgers, E., Jørgensen, A., & Yao, H. H. (2018) · Endocrine Reviews · doi:10.1210/er.2018-00010 · Cited by 181 · see citing works
The role of the GATA2 transcription factor in normal and malignant hematopoiesis
Vicente, C., Conchillo, A., García-Sánchez, M. A., & Odero, M. D. (2011) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2011.04.007 · Cited by 175 · see citing works
“Several non-finger omains of GATA2 have been described: two transactivation omains (TAD), located in the N- and C-terminal regions; nuclear localization signal (NLS); a negative regulatory omain (NRD); and regions that appear to be important for ts degradation [66,67].”
BackgroundGATA2 deficiency and related myeloid neoplasms
Włodarski, M. W., Collin, M. P., & Horwitz, M. S. (2017) · Seminars in Hematology · doi:10.1053/j.seminhematol.2017.05.002 · Cited by 171 · see citing works
“Additionally, other non-finger domains are distinguished: two transactivation domains, a nuclear localization signal, and a negative regulatory domain [18,19].”
BackgroundMammalian sex determination—insights from humans and mice
Eggers, S., & Sinclair, A. H. (2012) · Chromosome Research · doi:10.1007/s10577-012-9274-3 · Cited by 168 · see citing works
“Those complexes regulate key steroidogenic genes, such as STAR (encoding steroidogenic acute regulatory protein), CYP19A1 (encoding aromatase), INHA (encoding inhibin α-subunit), and HSD3B2 (encoding 3 beta-hydroxysteroid dehydrogenase/delta 5-4-isomerase type 2) (Viger et al. 2008; Nishida et al. 2008; Miyamoto et al…”
BackgroundEngels, M., Span, P. N., van Herwaarden, A. E., Sweep, F. C. G. J., Stikkelbroeck, N. M. M. L., & Claahsen-van der Grinten, H. L. (2019) · Endocrine Reviews · doi:10.1210/er.2018-00258 · Cited by 163 · see citing works
Loss-of-function mutation in GATA4 causes anomalies of human testicular development
Lourenço, D., Brauner, R., Rybczyńska, M., Nihoul‐Feketé, C., McElreavey, K., & Bashamboo, A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010257108 · Cited by 160 · see citing works
“However, GATA4 is expressed in the developing ovary as well as in adult granulosa and thecal cells (5), which suggests that either the p.”
BackgroundLi, J., Berman, B. P., Jariwala, U., Yan, X., Cogan, J. P., Walters, A., Chen, T., Buchanan, G., Frenkel, B., & Coetzee, G. A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003645 · Cited by 147 · see citing works
“GATA family members are able to bind to DNA at their response elements and mediate the ‘opening’ of compacted chromatin [46] and have been proposed to play major roles in endocrine function and disease [47].”
BackgroundBaranova, A. V., Tran, T., Birerdinc, A., & Younossi, Z. M. (2011) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2011.04579.x · Cited by 146 · see citing works
“2, a critical islet transcription factor.(49) Interestingly, CYP11A is suppressed in response to fenofibrate, a hypolipidemic ligand for PPARa used in the treatment of hypertriglyceridemia and combined hyperlipidemia, being partic-”
Blood-testis barrier and spermatogenesis: lessons from genetically-modified mice
Shi, Q., Jiang, X., Bukhari, I., Wei, Z., Yin, S., Wang, Z., & Cooke, H. (2014) · Asian Journal of Andrology · doi:10.4103/1008-682x.125401 · Cited by 131 · see citing works
Weirauch, M. T., & Hughes, T. R. (2011) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-90-481-9069-0_3 · Cited by 127 · see citing works
“Mutations in GATA TFs have been implicated in numerous human diseases, including cancer, congenital heart defects, and down syndrome [38, 39].”
BackgroundInteractive Features of Proteins Composing Eukaryotic Circadian Clocks
Crane, B. R., & Young, M. W. (2014) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060713-035644 · Cited by 125 · see citing works
Tiyaboonchai, A., Cardenas-Diaz, F. L., Ying, L., Maguire, J., Sim, X., Jobaliya, C. D., Gagne, A. L., Kishore, S., Stanescu, D. E., Hughes, N., et al. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2016.12.026 · Cited by 64 · see citing works
“All members of the GATA transcription factor family share conserved DNA activation and zinc finger DNA-binding domains (Molkentin, 2000; Viger et al., 2008).”
GATA4 regulates Sertoli cell function and fertility in adult male mice☆
Kyrönlahti, A., Euler, R., Bielińska, M., Schoeller, E. L., Moley, K. H., Toppari, J., Heikinheimo, M., & Wilson, D. B. (2010) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2010.12.019 · Cited by 119 · see citing works
“Introduction Transcription factor GATA4 has been implicated in the development and function of the mammalian testis (Viger et al., 2008).”
BackgroundSelf-citationAdams, B. D., Cowee, D. M., & White, B. A. (2009) · Molecular Endocrinology · doi:10.1210/me.2009-0062 · Cited by 111 · see citing works
How trophoblasts fuse: an in-depth look into placental syncytiotrophoblast formation
Renaud, S. J., & Jeyarajah, M. J. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04475-z · Cited by 112 · see citing works
Human sex-determination and disorders of sex-development (DSD)
Bashamboo, A., & McElreavey, K. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.10.030 · Cited by 104 · see citing works
Cell Type- and Sex-Dependent Transcriptome Profiles of Rat Anterior Pituitary Cells
Fletcher, P. A., Smiljanić, K., Prévide, R. M., Iben, J., Li, T., Rokic, M. B., Sherman, A., Coon, S. L., & Stojilković, S. S. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00623 · Cited by 100 · see citing works
“Gata2 is well-established to be critical in the development of T (together with Pou1f1) and G (without Pou1f1) (74).”
BackgroundInfluentialMutation update for the NR5A1 gene involved in DSD and infertility
Fabbri‐Scallet, H., de Sousa, L. M., Maciel‐Guerra, A. T., Guerra‐Júnior, G., & de Mello, M. P. (2019) · Human Mutation · doi:10.1002/humu.23916 · Cited by 98 · see citing works
Manuylov, N. L., Zhou, B., Ma, Q., Fox, S. C., Pu, W. T., & Tevosian, S. G. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.02.032 · Cited by 90 · see citing works
“…genes (e.g., Mis/Amh (Viger et al., 1998; Watanabe et al., 2000), Sf1 and aromatase (Cyp19a1) (Tremblay and Viger, 1999), Inha (Ketola et al., 1999), StAR (Nishida et al., 2008; Silverman et al., 2006) and Rhox5 (Bhardwaj et al., 2008); see (Lavoie and King, 2009; Viger et al., 2008) for review).”
BackgroundGonadal transactivation of STARD1, CYP11A1 and HSD3B
Steven, R. K. (2011) · Frontiers in bioscience · doi:10.2741/3959 · Cited by 85 · see citing works
“Multiple signaling pathways also control GATA4 generation and activity in gonadal cells (reviewed in (176)).”
Taieb, J., Grynberg, M., Pierre, A., Arouche, N., Massart, P., Belville, C., Hesters, L., Frydman, R., Catteau-Jonard, S., Fanchin, R. R. F., et al. (2011) · Molecular Endocrinology · doi:10.1210/me.2010-0297 · Cited by 83 · see citing works
Bennett, J., Wu, Y.-G., Gossen, J. A., Zhou, P., & Stocco, C. O. (2012) · Endocrinology · doi:10.1210/en.2011-1969 · Cited by 78 · see citing works
MANAGEMENT OF ENDOCRINE DISEASE: Gonadal dysfunction in congenital adrenal hyperplasia
Claahsen-van der Grinten, H. L., Stikkelbroeck, N., Falhammar, H., & Reisch, N. (2021) · European Journal of Endocrinology · doi:10.1530/eje-20-1093 · Cited by 72 · see citing works
Mechanism of Sex Determination in Humans: Insights from Disorders of Sex Development
Bashamboo, A., & McElreavey, K. (2016) · Sexual Development · doi:10.1159/000452637 · Cited by 68 · see citing works
“GATA4 cooperatively interacts with NR5A1 to regulate the expression of genes critical for testis determination and differentiation [Viger et al., 2008].”
BackgroundPadua, M. B., Jiang, T., Morse, D. A., Fox, S. C., Hatch, H. M., & Tevosian, S. G. (2015) · Endocrinology · doi:10.1210/en.2014-1907 · Cited by 67 · see citing works
REVIEW PAPER: Origin and Molecular Pathology of Adrenocortical Neoplasms
Bielińska, M., Parviainen, H., Kiiveri, S., Heikinheimo, M., & Wilson, D. B. (2009) · Veterinary Pathology · doi:10.1354/vp.08-vp-0179-w-rev · Cited by 67 · see citing works
Self-citationLung cancer deficient in the tumor suppressor GATA4 is sensitive to TGFBR1 inhibition
Gao, L., Hu, Y., Tian, Y., Fan, Z., Wang, K., Li, H., Zhou, Q., Zeng, G., Hu, X., Yu, L., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09295-7 · Cited by 67 · see citing works
MacLean, J. A., & Wilkinson, M. (2010) · Reproduction · doi:10.1530/rep-10-0100 · Cited by 65 · see citing works
“Other candidates are GATA4 and GATA6, as they are expressed at high levels in Sertoli cells (Viger et al. 2008).”
Bonnefond, A., Sand, O., Guerin, B., Durand, E., Graeve, F. D., Huyvaert, M., Rachdi, L., Kerr-Conte, J. A., Pattou, F. N., Vaxillaire, M., et al. (2012) · Diabetologia · doi:10.1007/s00125-012-2645-7 · Cited by 65 · see citing works
“In mice, in which GATA6 has been further studied, expression-based analyses suggest that GATA6 could play a role in very early pancreas specification [6–8].”
BackgroundFigueiredo, A. F. A., França, L. R., Hess, R. A., & Costa, G. M. J. (2016) · Cell Cycle · doi:10.1080/15384101.2016.1207835 · Cited by 65 · see citing works
“This transcription factor is mainly expressed in Sertoli and Leydig cells and has been implicated in the development and function of the mammalian testis, particularly in the regulation of gene expression and cell differentiation.(47,48) In the current study, 5-10% of the SCs in the transition region did not express G…”
BackgroundGATA4 Deficiency Impairs Ovarian Function in Adult Mice1
Kyrönlahti, A., Vetter, M., Euler, R., Bielińska, M., Jay, P. Y., Anttonen, M., Heikinheimo, M., & Wilson, D. B. (2011) · Biology of Reproduction · doi:10.1095/biolreprod.110.086850 · Cited by 63 · see citing works
Self-citationGATA4 Regulates Estrogen Receptor-α-Mediated Osteoblast Transcription
Miranda‐Carboni, G. A., Güemes, M., Bailey, S. T., Anaya, E. P., Corselli, M., Péault, B., & Krum, S. A. (2011) · Molecular Endocrinology · doi:10.1210/me.2010-0463 · Cited by 62 · see citing works
Receptors and signaling pathways involved in proliferation and differentiation of Sertoli cells
Lucas, T. F. G., Nascimento, A. R., Pisolato, R., Pimenta, M. T., Lazari, M. F. M., & Porto, C. S. (2014) · Spermatogenesis · doi:10.4161/spmg.28138 · Cited by 61 · see citing works
Anttonen, M., Pihlajoki, M., Andersson, N., Georges, A. B., L’Hôte, D., Vattulainen, S., Färkkilä, A., Unkila‐Kallio, L., Veitia, R. A., & Heikinheimo, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085545 · Cited by 61 · see citing works
“GATA4 plays a key role in normal granulosa cell function [23,24] and GCTs [25–27]; high GATA4 immunoreactivity denotes a more aggressive human GCT with increased recurrence risk [25].”
BackgroundSelf-citationGATA4 regulates angiogenesis and persistence of inflammation in rheumatoid arthritis
Jia, W., Wu, W., Yang, D., Xiao, C., Huang, M., Long, F., Su, Z., Qin, M., Liu, X., & Zhu, Y. Z. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0570-5 · Cited by 61 · see citing works
GATA4 Regulates Blood-Testis Barrier Function and Lactate Metabolism in Mouse Sertoli Cells
Schrade, A., Kyrönlahti, A., Akinrinade, O., Pihlajoki, M., Fischer, S., Rodriguez, V. M., Otte, K., Velagapudi, V., Toppari, J., Wilson, D. B., et al. (2016) · Endocrinology · doi:10.1210/en.2015-1927 · Cited by 60 · see citing works
Self-citationLucas, T. F. G., Lazari, M. F. M., & Porto, C. S. (2013) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2013.09.015 · Cited by 59 · see citing works
Telugu, B. P. V. L., Adachi, K., Schlitt, J. M., Ezashi, T., Schust, D. J., Roberts, R. M., & Schulz, L. C. (2013) · Placenta · doi:10.1016/j.placenta.2013.03.016 · Cited by 57 · see citing works
“GATA6, a marker of primitive endoderm, also widely expressed in endocrine tissues [37], was robustly expressed in placental/HLA-G+ cells (Fig.”
BackgroundPadua, M. B., Fox, S. C., Jiang, T., Morse, D. A., & Tevosian, S. G. (2014) · Biology of Reproduction · doi:10.1095/biolreprod.113.117002 · Cited by 55 · see citing works
“In the postnatal ovary, GATA4 and GATA6 are present in granulosa cells where they (directly or indirectly) regulate expression of numerous genes [2, 3].”
BackgroundInfluentialEvidence of a genetic link between endometriosis and ovarian cancer
Lee, A. W., Templeman, C. E., Stram, D. A., Beesley, J., Tyrer, J. P., Berchuck, A., Pharoah, P. D. P., Chenevix‐Trench, G., Pearce, C. L., Ness, R. B., et al. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.09.023 · Cited by 55 · see citing works
“In addition, rs1333052 lies within a binding site for GATA2, one of six factors that constitute the GATA family of transcriptional regulatory proteins which has been shown to play a role in ovarian function; it was identified by genome-wide ChIP-sequencing (30).”
BackgroundRodríguez‐López, M., Gonzalez, S., Hillson, O., Tunnacliffe, E., Codlin, S., Tallada, V. A., Bähler, J., & Rallis, C. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.02.058 · Cited by 55 · see citing works
“The mouse and human ortholog of Gaf1, GATA6, is involved in differentiation, stem cell maintenance, and cancer (Viger et al., 2008; Wamaitha et al., 2015; Zhong et al., 2011).”
BackgroundVilleneuve, D. L., Wang, R., Bencic, D. C., Biales, A. D., Martinović‐Weigelt, D., Lazorchak, J. M., Toth, G. P., & Ankley, G. T. (2009) · Environmental Toxicology and Chemistry · doi:10.1897/08-653.1 · Cited by 54 · see citing works
“The GATA motifs, particularly GATA-1, -2, and -3, are involved in the regulation of hematopoiesis [39], suggesting this as a potential function altered by fadrozole exposure.”
BackgroundChia, C. Y., Madrigal, P., Denil, S. L. I. J., Martinez, I., Garcia‐Bernardo, J., El‐Khairi, R., Chhatriwala, M., Shepherd, M. H., Hattersley, A. T., Dunn, N. R., et al. (2019) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.12.003 · Cited by 54 · see citing works
“GATA6 encodes a highly conserved zinc-finger transcription factor that recognizes and binds the (A/T)GATA(A/G) regulatory motif, two of which are located in the mouse Pdx1 and human PDX1 promoters (Carrasco et al., 2012; Lentjes et al., 2016; Patient and McGhee, 2002; Viger et al., 2008; Xuan et al., 2012).”
BackgroundOvando, B. J., Ellison, C. A., Vezina, C. M., & Olson, J. R. (2010) · BMC Genomics · doi:10.1186/1471-2164-11-583 · Cited by 52 · see citing works
“Expression of Gata6 is significantly depressed in most human adrenocortical tumors [46,47] and it has been hypothesized that decreased expression of Gata6 may be an important event for the escape of tumor cells from normal control mechanisms [48].”
BackgroundPihlajoki, M., Gretzinger, E., Cochran, R. S., Kyrönlahti, A., Schrade, A., Hiller, T., Sullivan, L., Shoykhet, M., Schoeller, E. L., Brooks, M. D., et al. (2013) · Endocrinology · doi:10.1210/en.2012-1892 · Cited by 51 · see citing works
“GATA6 acts in synergy with SF1 and other transcription factors to enhance the expression of genes involved in adrenal steroid biosynthesis (20, 23).”
BackgroundSelf-citationGATA6 Is a Crucial Regulator of Shh in the Limb Bud
Kozhemyakina, E. A., Ionescu, A. M., & Lassar, A. B. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004072 · Cited by 51 · see citing works
“[51]), it seems plausible that both GATA4 and GATA6, which are”
Miller, S. A., & Weinmann, A. S. (2008) · Immunology · doi:10.1111/j.1365-2567.2008.03040.x · Cited by 51 · see citing works
GATA4 Is a Key Regulator of Steroidogenesis and Glycolysis in Mouse Leydig Cells
Schrade, A., Kyrönlahti, A., Akinrinade, O., Pihlajoki, M., Häkkinen, M. R., Fischer, S., Alastalo, T., Velagapudi, V., Toppari, J., Wilson, D. B., et al. (2015) · Endocrinology · doi:10.1210/en.2014-1931 · Cited by 51 · see citing works
Self-citationGupta, V., Khan, A. A., Sasi, B. K., & Mahapatra, N. R. (2015) · Journal of Neurochemistry · doi:10.1111/jnc.13099 · Cited by 50 · see citing works
Kristiansen, W., Karlsson, R., Rounge, T. B., Whitington, T., Andreassen, B. K., Magnusson, P. K. E., Fosså, S. D., Adami, H., Turnbull, C., Haugen, T. B., et al. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv129 · Cited by 50 · see citing works
Pilon, N., Raiwet, D. L., Viger, R. S., & Silversides, D. W. (2008) · Developmental Dynamics · doi:10.1002/dvdy.21496 · Cited by 50 · see citing works
“In a variety of cell types, GATA4 is known for its involvement in cell fate decisions and it also appears to be involved in the process of cell migration (Molkentin, 2000; Viger et al., 2008).”
BackgroundSelf-citationDubé, C., Bergeron, F., Vaillant, M.-J., Robert, N. M., Brousseau, C., & Tremblay, J. (2008) · Cancer Letters · doi:10.1016/j.canlet.2008.10.008 · Cited by 49 · see citing works
Bennett, J., Baumgarten, S. C., & Stocco, C. (2013) · Endocrinology · doi:10.1210/en.2013-1410 · Cited by 50 · see citing works
“These are intriguing findings, because the expression of AMH has been shown to be stimulated by GATA4 (20).”
BackgroundMurayama, C., Miyazaki, H., Miyamoto, A., & Shimizu, T. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.11.014 · Cited by 47 · see citing works
“The studies have reported that GATA-4 is essential for the gonadal function (Viger et al., 2008).”
SOX Genes and Their Role in Disorders of Sex Development
Sreenivasan, R., Gonen, N., & Sinclair, A. (2022) · Sexual Development · doi:10.1159/000524453 · Cited by 37 · see citing works
“An additional factor, GATA binding protein 4 (GATA4), interacts with SF-1 and zinc finger protein FOG family member 2 (FOG2/ZFPM2) to regulate the expression of SRY and SOX9 [Miyamoto et al., 2008; Viger et al., 2008].”
BackgroundGene Mutations Associated with Anomalies of Human Gonad Formation
Bashamboo, A., & McElreavey, K. (2012) · Sexual Development · doi:10.1159/000342188 · Cited by 45 · see citing works
“GATA4 cooperatively interacts with several proteins including NR5A1 to regulate the expression of critical genes known to be involved in testis determination and differentiation (SRY, SOX9, AMH, STAR, CYP19A1, INHA, HSD3B2) [Viger et al., 2008].”
BackgroundQin, F., Zhang, J., Zan, L., Guo, W., Wang, J., Chen, L., Cao, Y., Shen, O., & Tong, J. (2015) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2015.07.009 · Cited by 42 · see citing works
“Several studies have indicated that GATA-4 regulates the promoters of SF-1 (NR5A1) (Viger et al., 2008), StAR (Silverman et al., 2006), HSD17β1 (Piao et al., 1997), Cyp19 (Cai et al., 2007), human HSD3β1 (Peng et al., 2004), Cyp17 (Flück and Miller, 2004), and Cyp11A (Shih et al., 2011) (Tremblay and Viger, 2001).”
BackgroundGATA3 inhibits GCM1 activity and trophoblast cell invasion
Chiu, Y.-H., & Chen, H. (2016) · Scientific Reports · doi:10.1038/srep21630 · Cited by 43 · see citing works
de la Piscina, I. M., Mingo, C. D., Riedl, S., Rodriguez, A., Pandey, A. V., Fernández‐Cancio, M., Camats, N., Sinclair, A. H., Castaño, L. A., Audı́, L., et al. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00142 · Cited by 41 · see citing works
“Moreover, GATA4 functionally interacts with NR5A1 in Sertoli cell cultures to positively regulate the expression of AMH, and therefore, it has been reported that mutations in NR5A1 may cause 46,XY DSD due to lack of interaction with GATA (15).”
BackgroundBianco, S., Bellefleur, A., Beaulieu, É., Beauparlant, C. J., Bertolin, K., Droit, A., Schoonjans, K., Murphy, B. D., & Gévry, N. Y. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.07.088 · Cited by 40 · see citing works
Functional Cooperation Between GATA Factors and cJUN on the Star Promoter in MA‐10 Leydig Cells
Martin, L. J., Bergeron, F., Viger, R. S., & Tremblay, J. (2011) · Journal of Andrology · doi:10.2164/jandrol.110.012039 · Cited by 41 · see citing works
Self-citationThe Essential Role of GATA6 in the Activation of Estrogen Synthesis in Endometriosis
Bernardi, L. A., Dyson, M. T., Tokunaga, H., Sison, C., Oral, M., Robins, J. C., & Bulun, S. E. (2019) · Reproductive Sciences · doi:10.1177/1933719118756751 · Cited by 40 · see citing works
“The NR5A1 is a nuclear receptor important for sexual development and differentiation of steroidogenic tissues and has been established as a key factor regulating steroidogenesis.8,9 The NR5A1 is expressed in steroidogenic tissues, specifically the adrenal cortex and gonads,8 and coordinates the expression of multiple…”
BackgroundInfluentialRecent advances in senescence-associated secretory phenotype and osteoporosis
Fan, H., Qiao, Z., Li, J., Shang, G., Shang, C., Chen, S., Leng, Z., Su, H., Kou, H., & Liu, H. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e25538 · Cited by 42 · see citing works
“GATA factors are a set of transcription regulators that are ubiquitous in eukaryotic cells and regulate development and differentiation [48].”
BackgroundMolecular basis of crosstalk between oncogenic Ras and the master regulator of hematopoiesis GATA‐2
Katsumura, K. R., Yang, C., Boyer, M. E., Li, L., & Bresnick, E. H. (2014) · EMBO Reports · doi:10.15252/embr.201438808 · Cited by 38 · see citing works
“As GATA transcription factors control genetic networks in diverse contexts [1 – 3], and pathological GATA factor mutants have been described [4, 5], it is instructive to consider the consequences of such mutations.”
Wang, J., Wan, C. C., Shuju, Z., Yang, Z., Celi, P., Ding, X., Bai, S., Zeng, Q., Mao, X., Xu, S., et al. (2020) · Poultry Science · doi:10.1016/j.psj.2020.10.024 · Cited by 38 · see citing works
“(Viger et al., 2008), mediate the stimulatory effects of FSH on several ovarian genes (Lavoie, 2003), and increase StAR promoter activity (Gillio-Meina, 2002; Lavoie, 2003).”
BackgroundGenetic Mutations of Pancreatic Cancer and Genetically Engineered Mouse Models
Saiki, Y., Jiang, C., Ohmuraya, M., & Furukawa, T. (2021) · Cancers · doi:10.3390/cancers14010071 · Cited by 38 · see citing works
Taniguchi, H., Komiyama, J., Viger, R. S., & Okuda, K. (2009) · Molecular Reproduction and Development · doi:10.1002/mrd.21054 · Cited by 37 · see citing works
“A large number of in vitro studies have suggested that GATA4 is essential for the gonadal function (Viger et al., 2008).”
BackgroundInfluentialSelf-citationYorifuji, T., Kawakita, R., Hosokawa, Y., Fujimaru, R., Yamaguchi, E., & Tamagawa, N. (2012) · Journal of Medical Genetics · doi:10.1136/jmedgenet-2012-101161 · Cited by 37 · see citing works
“GATA6 is a member of a GATA family of zinc-finger transcriptional regulators, which bind to the common WGATAR motif in the regulatory regions of many genes.(6) Although GATA6 is expressed during the embryogenesis of a variety of endodermally derived organs, including the heart, pancreas, ovary, lung, and liver, its mu…”
BackgroundGATA4 knockdown in MA-10 Leydig cells identifies multiple target genes in the steroidogenic pathway
Bergeron, F., Nadeau, G., & Viger, R. S. (2014) · Reproduction · doi:10.1530/rep-14-0369 · Cited by 36 · see citing works
“Following gonadal differentiation, GATA4 remains highly expressed in all gonadal somatic lineages of both sexes throughout ontogeny (reviewed in LaVoie (2003), Viger et al. (2004, 2008) and Zaytouni et al. (2011)).”
BackgroundInfluentialSelf-citationChen, H., Libertini, S. J., George, M. D., Dandekar, S., Tepper, C. G., Al-Bataina, B., Kung, H.-J., Ghosh, P., & Mudryj, M. M. (2010) · Endocrine Related Cancer · doi:10.1677/erc-10-0081 · Cited by 36 · see citing works
“GATA proteins have been proposed to play major roles in endocrine function and disease (Viger et al. 2008).”
BackgroundCurrent Knowledge on Endometriosis Etiology: A Systematic Review of Literature
Михалева, Л. М., Radzinsky, V. E., Orazov, M. R., Николаевна, Х. Т., Sorokina, A. V., Александрович, М. С., Владимировна, В. С., Shustova, V. B., & Sinelnikov, M. Y. (2021) · International Journal of Women s Health · doi:10.2147/ijwh.s306135 · Cited by 37 · see citing works
Notch signaling represses GATA4-induced expression of genes involved in steroid biosynthesis
George, R. M., Hahn, K. L., Rawls, A., Viger, R. S., & Wilson‐Rawls, J. (2015) · Reproduction · doi:10.1530/rep-15-0226 · Cited by 36 · see citing works
“Steroidogenesis genes have well-studied promoters that are transactivated by GATA4 (Tremblay & Viger 2001a,b, Tremblay et al. 2002, Viger et al. 2004, 2008, Bergeron et al. 2015, Schrade et al. 2015).”
Self-citationDaems, C., Di‐Luoffo, M., Paradis, E., & Tremblay, J. (2015) · Endocrinology · doi:10.1210/en.2014-1964 · Cited by 36 · see citing works
“Although 2 GATA factors (GATA4 and GATA6) have been identified in Leydig cells, GATA4 is the predominant member present in these cells (reviewed in Viger et al [47]).”
BackgroundCell Type-Specific Sexual Dimorphism in Rat Pituitary Gene Expression During Maturation1
Bjelobaba, I. M., Janjic, M. M., Kučka, M., & Stojilković, S. S. (2015) · Biology of Reproduction · doi:10.1095/biolreprod.115.129320 · Cited by 35 · see citing works
“The hormone-secreting anterior pituitary cells differentiate in a temporal- and spatial-specific fashion as three separate lineages under the influence of various transcriptional factors [20–22].”
BackgroundWatanabe, M., Yasuoka, Y., Mawaribuchi, S., Kuretani, A., Ito, M., Kondo, M., Ochi, H., Ogino, H., Fukui, A., Taira, M., et al. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.09.017 · Cited by 35 · see citing works
Deng, S., Zhang, Y., Yu, K., Wang, X., Chen, S., Han, D., Cheng, C. Y., Lian, Z., & Liu, Y. (2017) · Oncotarget · doi:10.18632/oncotarget.22855 · Cited by 34 · see citing works
“However, in steroidogenic cells, not all cAMP-regulated genes, such as StAR, have a consensus cAMP response element (CRE), but many of them have a regulatory sequence recognized by a GATA family transcription factor [69].”
BackgroundInfluentialGATA transcription factors regulate LHβ gene expression
Lo, A., Zheng, W., Gong, Y., Crochet, J. R., & Halvorson, L. M. (2011) · Journal of Molecular Endocrinology · doi:10.1530/jme-10-0137 · Cited by 34 · see citing works
Koster, R., Mitra, N., D'Andrea, K. P., Vardhanabhuti, S., Chung, C. C., Wang, Z., Erickson, R. L., Vaughn, D. J., Litchfield, K., Rahman, N., et al. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddu305 · Cited by 33 · see citing works
GATA4 protects granulosa cell tumors from TRAIL-induced apoptosis
Kyrönlahti, A., Kauppinen, M., Lind, E., Unkila‐Kallio, L., Bützow, R. C., Klefström, J. T., Wilson, D. B., Anttonen, M., & Heikinheimo, M. (2010) · Endocrine Related Cancer · doi:10.1677/erc-10-0041 · Cited by 33 · see citing works
“Recently, GATA4 has emerged as an important factor in the development and function of endocrine tissues (Viger et al. 2008).”
BackgroundSelf-citationGenetic regulation of RNA splicing in human pancreatic islets
Atla, G., Bonàs‐Guarch, S., Cuenca-Ardura, M., Beucher, A., Crouch, D. J. M., García-Hurtado, J., Morán, I., Cnop, M., Eliasson, L., Esguerra, J. L. S., et al. (2022) · Genome biology · doi:10.1186/s13059-022-02757-0 · Cited by 31 · see citing works
Adrenal Development in Mice Requires GATA4 and GATA6 Transcription Factors
Tevosian, S. G., Jiménez, E., Hatch, H. M., Jiang, T., Morse, D. A., Fox, S. C., & Padua, M. B. (2015) · Endocrinology · doi:10.1210/en.2014-1815 · Cited by 32 · see citing works
Wu, C., Wei, K., Chou, J., Lu, C., Hsieh, C., Lin, J. M. J., Deng, Y.-F., Hsu, W.-T., Wang, H.-M., Leung, C., et al. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17091467 · Cited by 31 · see citing works
“In humans, GATA1/2/3 are expressed in hematopoietic cells, whereas GATA4/5/6 are expressed in the cardiovascular system and endoderm-derived tissue, including the liver, lung, and pancreas [7].”
BackgroundTransgenic mouse models in the study of reproduction: insights into GATA protein function
Tevosian, S. G. (2014) · Reproduction · doi:10.1530/rep-14-0086 · Cited by 30 · see citing works
“In the postnatal ovaries, GATA4 is abundantly expressed in the granulosa cells of primary, preantral, and antral follicles as well as in endocrine theca cells, but not in primordial follicles or luteal cells (Viger et al. 2008).”
BackgroundFunctions of PIT1 in GATA2-dependent transactivation of the thyrotropin β promoter
Kashiwabara, Y., Sasaki, S., Matsushita, A., Nagayama, K., Ohba, K., Iwaki, H., Matsunaga, H., Suzuki, S., Misawa, H., Ishizuka, K., et al. (2008) · Journal of Molecular Endocrinology · doi:10.1677/jme-08-0099 · Cited by 30 · see citing works
“The Zn finger domain of GATA2 (GATA2-Zf) has high homology with that of GATA1 and 3, while the amino acid sequences of N- and C-terminal regions show diversity (Viger et al. 2008).”
BackgroundThurisch, B., Liang, S. Y., Sarioglu, N. M. E., Schomburg, L., Bungert, J., & Dame, C. (2009) · Journal of Molecular Endocrinology · doi:10.1677/jme-09-0030 · Cited by 30 · see citing works
“Although various putative GATA4 target genes have been identified in the testis and ovary by means of in vitro studies (for review see (Viger et al. 2008)), to our knowledge no in vivo genetic model is currently available that elucidates GATA4 function in the ovary.”
BackgroundHu, S., Yang, S., Lu, Y., Deng, Y., Li, L., Zhu, J., Zhang, Y., Hu, B., Hu, J., Xia, L., et al. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00196 · Cited by 29 · see citing works
Eisermann, K., Tandon, S., Bazarov, A., Brett, A., Fraizer, G. C., & Piontkivska, H. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-337 · Cited by 29 · see citing works
“bind the WGATAR consensus motif and are expressed in multiple tissues, including endocrine glands [50-52].”
BackgroundYau, D., Franco, E. D., Flanagan, S. E., Ellard, S., Blumenkrantz, M., & Mitchell, J. J. (2017) · Diagnostic Pathology · doi:10.1186/s13000-016-0592-1 · Cited by 28 · see citing works
“GATA6 is one of a family of evolutionarily conserved transcription factors recognizing the A/T-GATA-A/G consensus sequence, with key roles in the development and differentiation of multiple cell lineages and tissues [17, 18].”
BackgroundKouri, C., Sommer, G., & Flück, C. E. (2021) · Hormone Research in Paediatrics · doi:10.1159/000519691 · Cited by 29 · see citing works
“It interacts with several proteins including ZFPM2, SF-1, and WT1 to regulate the expression of sex determining genes SRY, SOX9, and AMH, as well as genes involved in sex differentiation including STAR, CYP17A1, CYP19A1, INHA, and HSD3B2 [38–42].”
BackgroundInfluentialGATA4 regulates osteoblastic differentiation and bone remodeling via p38-mediated signaling
Zhou, T., Guo, S., Zhang, Y., Weng, Y., Wang, L. Q., & Ma, J. (2017) · Journal of Molecular Histology · doi:10.1007/s10735-017-9719-2 · Cited by 28 · see citing works
“GATA4, a transcription factor, has been reported to regulate transcription in many organs (Mazaud et al. 2007; Molkentin et al. 1998; Viger et al. 2008).”
BackgroundGATA6+ Peritoneal Resident Macrophage: The Immune Custodian in the Peritoneal Cavity
Jayakumar, P., Laganson, A., & Deng, M. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.866993 · Cited by 27 · see citing works
- Authors
- Viger, R. S., Guittot, S. M., Anttonen, M., Wilson, D. B., & Heikinheimo, M.
- Affiliations
- Centre hospitalier universitaire de Québec (CA)
- Ontogeny-Reproduction Research Unit (R.S.V., S.M.G.), CHUQ Research Centre, Quebec City, Canada G1V 4G2
- Department of Obstetrics and Gynecology and Women’s Health Research Program (M.A.), FI-00014 Helsinki, Finland
- St. Louis Children's Hospital (US)
- Corresponding author
- Viger, Robert S
- Heikinheimo, Markku
- Venue
- Molecular Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2008-04-01
- Volume
- 22
- Issue
- 4
- Pages
- 781-798
- ISSN
- 0888-8809 (ISSN-L)
- 1944-9917
- PMC
- PMC2276466
- OpenAlex
- W2013216633
- Cited by
- 270
- References
- 235
- Citations by year
- 2026: 3 · 2025: 11 · 2024: 12 · 2023: 10 · 2022: 15 · 2021: 21 · 2020: 12 · 2019: 15 · 2018: 12 · 2017: 11 · 2016: 19 · 2015: 21 · 2014: 24 · 2013: 13 · 2012: 16
- FWCI
- 1.42
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Molecular Endocrinology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Helsingin Yliopisto
- Turun Yliopisto
- National Institutes of Health
- Canadian Institutes of Health Research
- National Institute of Diabetes and Digestive and Kidney Diseases (DK075618, R01DK075618)
- Institute of Gender and Health
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- Keywords
- GATA transcription factors, GATA-1, GATA2, GATA3, GATA4, GATA5, GATA6, endocrine development, endocrine function, gonads, pituitary gland, pancreas, adrenal gland, tissue-specific knockout mice
- MeSH terms
- Animals, Endocrine System Diseases, Endocrine System, Humans, Models, Biological, Transcription, Genetic, Protein Isoforms, GATA Transcription Factors
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