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Article

SUMOylation Inhibits SF-1 Activity by Reducing CDK7-Mediated Serine 203 Phosphorylation

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Pages 613-625 | Received 21 Feb 2008, Accepted 31 Oct 2008, Published online: 21 Mar 2023

REFERENCES

  • Ariazi, E. A., R. J. Kraus, M. L. Farrell, V. C. Jordan, and J. E. Mertz. 2007. Estrogen-related receptor α1 transcriptional activities are regulated in part via the ErbB2/HER2 signaling pathway. Mol. Cancer Res. 5:71–85.
  • Babu, P. S., D. L. Bavers, S. Shah, and G. D. Hammer. 2000. Role of phosphorylation, gene dosage and Dax-1 in SF-1 mediated steroidogenesis. Endocr. Res. 26:985–994.
  • Barry, J. B., J. Laganière, and V. Giguère. 2006. A single nucleotide in an estrogen-related receptor α site can dictate mode of binding and peroxisome proliferator-activated receptor γ coactivator 1α activation of target promoters. Mol. Endocrinol. 20:302–310.
  • Berta, M. A., N. Mazure, M. Hattab, J. Pouyssegur, and M. C. Brahimi-Horn. 2007. SUMOylation of hypoxia-inducible factor-1α reduces its transcriptional activity. Biochem. Biophys. Res. Commun. 360:646–652.
  • Bohren, K. M., V. Nadkarni, J. H. Song, K. H. Gabbay, and D. Owerbach. 2004. A M55V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus. J. Biol. Chem. 279:27233–27238.
  • Borud, B., T. Hoang, M. Bakke, A. L. Jacob, J. Lund, and G. Mellgren. 2002. The nuclear receptor coactivators p300/CBP/cointegrator-associated protein (p/CIP) and transcription intermediary factor 2 (TIF2) differentially regulate PKA-stimulated transcriptional activity of steroidogenic factor 1. Mol. Endocrinol. 16:757–773.
  • Bregman, D. B., R. G. Pestell, and V. J. Kidd. 2000. Cell cycle regulation and RNA polymerase II. Front. Biosci. 5:D244–D257.
  • Burris, T. P., W. Guo, T. Le, and E. R. McCabe. 1995. Identification of a putative steroidogenic factor-1 response element in the DAX-1 promoter. Biochem. Biophys. Res. Commun. 214:576–581.
  • Carlone, D. L., and J. R. Richards. 1997. Functional interactions, phosphorylation, and levels of 3′,5′-cyclic adenosine monophosphate-regulatory element binding protein and steroidogenic factor-1 mediate hormone-regulated and constitutive expression of aromatase in bonadal cells. Mol. Endocrinol. 11:292–304.
  • Chen, D., E. Washbrook, N. Sarwar, G. J. Bates, P. E. Pace, V. Thirunuvakkarasu, J. Taylor, R. J. Epstein, F. V. Fuller-Pace, J. M. Egly, R. C. Coombes, and S. Ali. 2002. Phosphorylation of human estrogen receptor alpha at serine 118 by two distinct signal transduction pathways revealed by phosphorylation-specific antisera. Oncogene 21:4921–4931.
  • Chen, W. Y., W. C. Lee, N. C. Hsu, F. Huang, and B. C. Chung. 2004. SUMO modification of repression domains modulates function of nuclear receptor 5A1 (steroidogenic factor-1). J. Biol. Chem. 279:38730–38735.
  • Chun, T., H. Itoh, L. Subramanian, J. A. Iniguez-Lluhi, and K. Nakao. 2003. Modification of GATA-2 transcriptional activity in endothelial cells by the SUMO E3 ligase PIASy. Circ. Res. 92:1201–1208.
  • Chupreta, S., H. Brevig, L. Bai, J. L. Merchant, and J. A. Iniguez-Lluhi. 2007. Sumoylation-dependent control of homotypic and heterotypic synergy by the Kruppel-type zinc finger protein ZBP-89. J. Biol. Chem. 282:36155–36166.
  • Chupreta, S., S. Holmstrom, L. Subramanian, and J. A. Iniguez-Lluhi. 2005. A small conserved surface in SUMO is the critical structural determinant of its transcriptional inhibitory properties. Mol. Cell. Biol. 25:4272–4282.
  • Crawford, P. A., C. Dorn, Y. Sadovsky, and J. Milbrandt. 1998. Nuclear receptor DAX-1 recruits nuclear receptor corepressor N-CoR to steroidogenic factor 1. Mol. Cell. Biol. 18:2949–2956.
  • Crawford, P. A., J. A. Polish, G. Ganpule, and Y. Sadovsky. 1997. The activation function-2 hexamer of steroidogenic factor-1 is required, but not sufficient for potentiation by SRC-1. Mol. Endocrinol. 11:1626–1635.
  • Daniel, A. R., E. J. Faivre, and C. A. Lange. 2007. Phosphorylation-dependent antagonism of sumoylation derepresses progesterone receptor action in breast cancer cells. Mol. Endocrinol. 21:2890–2906.
  • De Santa Barbara, P., N. Bonneaud, B. Boizet, M. Desclozeaux, B. Moniot, P. Sudbeck, G. Scherer, F. Poulat, and P. Berta. 1998. Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Mullerian hormone gene. Mol. Cell. Biol. 18:6653–6665.
  • Dorn, C., Q. Ou, J. Svaren, P. A. Crawford, and Y. Sadovsky. 1999. Activation of luteinizing hormone β gene by gonadotropin-releasing hormone requires the synergy of early growth response-1 and steroidogenic factor-1. J. Biol. Chem. 274:13870–13876.
  • Garrett, S., W. A. Barton, R. Knights, P. Jin, D. O. Morgan, and R. P. Fisher. 2001. Reciprocal activation by cyclin-dependent kinases 2 and 7 is directed by substrate specificity determinants outside the T loop. Mol. Cell. Biol. 21:88–99.
  • Gill, G. 2004. SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev. 18:2046–2059.
  • Gizard, F., B. Lavallee, F. DeWitte, E. Teissier, B. Staels, and D. W. Hum. 2002. The transcriptional regulating protein of 132 kDa (TReP-132) enhances P450scc gene transcription through interaction with steroidogenic factor-1 in human adrenal cells. J. Biol. Chem. 277:39144–39155.
  • Gong, Z., M. Brackertz, and R. Renkawitz. 2006. SUMO modification enhances p66-mediated transcriptional repression of the Mi-2/NuRD complex. Mol. Cell. Biol. 26:4519–4528.
  • Guo, B., S. H. Yang, J. Witty, and A. D. Sharrocks. 2007. Signalling pathways and the regulation of SUMO modification. Biochem. Soc. Trans. 35:1414–1418.
  • Halvorson, L. M., M. Ito, J. L. Jameson, and W. W. Chin. 1998. Steroidogenic factor-1 and early growth response protein 1 act through two composite DNA binding sites to regulate luteinizing hormone β-subunit gene expression. J. Biol. Chem. 273:14712–14720.
  • Hammer, G. D., I. Krylova, Y. Zhang, B. D. Darimont, K. Simpson, N. L. Weigel, and H. A. Ingraham. 1999. Phosphorylation of the nuclear receptor SF-1 modulates cofactor recruitment: integration of hormone signaling in reproduction and stress. Mol. Cell 3:521–526.
  • Hay, R. T. 2005. SUMO: A history of modification. Mol. Cell 18:1–12.
  • Herzog, B., J. Cardenas, R. K. Hall, J. A. Villena, P. J. Budge, V. Giguère, D. K. Granner, and A. Kralli. 2006. Estrogen-related receptor α is a repressor of phosphoenolpyruvate carboxykinase gene transcription. J. Biol. Chem. 281:99–106.
  • HietaKangas, V., J. Anckar, H. A. Blomster, M. Fujimoto, J. J. Palvimo, A. Nakai, and L. Sistonen. 2006. PDSM, a motif for phosphorylation-dependent SUMO modification. Proc. Natl. Acad. Sci. USA 103:45–50.
  • Holmstrom, S., M. E. Van Antwerp, and J. A. Iniguez-Lluhi. 2003. Direct and distinguishable inhibitory roles for SUMO isoforms in the control of transcriptional synergy. Proc. Natl. Acad. Sci. USA 100:15758–15763.
  • Hossain, A., and G. F. Saunders. 2003. Role of Wilms tumor 1 (WT1) in the transcriptional regulation of the Mullerian-inhibiting substance promoter. Biol. Reprod. 69:1808–1814.
  • Iniguez-Lluhi, J. A., and D. Pearce. 2000. A common motif within the negative regulatory regions of multiple factors inhibits their transcriptional synergy. Mol. Cell. Biol. 20:6040–6050.
  • Ito, M., R. N. Yu, and J. L. Jameson. 1998. Steroidogenic factor-1 contains a carboxy-terminal transcriptional activation domain that interacts with steroid receptor coactivator-1. Mol. Endocrinol. 12:290–301.
  • Ito, M., R. N. Yu, and J. L. Jameson. 1997. DAX-1 inhibits SF-1-mediated transactivation via a carboxy-terminal domain that is deleted in adrenal hypoplasia congenita. Mol. Cell. Biol. 17:1476–1483.
  • Johnson, E. S. 2004. Protein modification by SUMO. Annu. Rev. Biochem. 73:355–382.
  • Kabe, Y., M. Goto, D. Shima, T. Imai, T. Wada, K. Morohashi, M. Shirakawa, S. Hirose, and H. Handa. 1999. The role of human MBF1 as a transcriptional coactivator. J. Biol. Chem. 274:34196–34202.
  • Kang, J., C. B. Gocke, and H. Yu. 2006. Phosphorylation-facilitated sumoylation of MEF2C negatively regulates its transcriptional activity. BMC Biochem. 7:5–19.
  • Kawabe, K., T. Shikayama, H. Tsuboi, S. Oka, K. Oba, T. Yanase, H. Nawata, and K. Morahashi. 1999. Dax-1 as one of the target genes of Ad4BP/SF-1. Mol. Endocrinol. 13:1267–1284.
  • Kelly, S. N., T. J. McKenna, and L. S. Young. 2004. Modulation of steroidogenic enzymes by orphan nuclear transcriptional regulation may control diverse production of cortisol and androgens in the human adrenal. J. Endocrinol. 181:355–365.
  • Komatsu, T., H. Mizusaki, T. Mukai, H. Ogawa, D. Baba, M. Shirakawa, S. Hatakeyama, K. I. Nakayama, H. Yamamoto, A. Kikuchi, and K. Morohashi. 2004. Small ubiquitin-like modifier 1 (SUMO-1) modification of the synergy control motif of Ad4 binding protein/steroidogenic factor 1 (Ad4BP/SF-1) regulates synergistic transcription between Ad4BP/SF-1 and Sox9. Mol. Endocrinol. 18:2451–2462.
  • Kraus, R. J., E. A. Ariazi, M. L. Farrell, and J. E. Mertz. 2002. Estrogen-related receptor α1 actively antagonizes estrogen receptor regulated transcription in MCF-7 mammary cells. J. Biol. Chem. 277:24826–24834.
  • Lee, M. B., L. A. Lebeveda, M. Suzawa, S. A. Wadekar, M. Desclozeaux, and H. A. Ingraham. 2005. The DEAD-box protein DP103 (Ddx20 or Gemin-3) represses orphan nuclear receptor activity via SUMO modification. Mol. Cell. Biol. 25:1879–1890.
  • Leers-Sucheta, S., K. Morahashi, J. I. Mason, and M. H. Melner. 1997. Synergistic activation of the human type II 3β-hydroxysteroid dehydrogenase/δ5-δ4 isomerase promoter by the transcription factor steroidogenic factor-1/adrenal 4-binding protein and phorbol ester. J. Biol. Chem. 272:7960–7967.
  • Lewis, A. E., M. Rusten, E. A. Hoivik, E. L. Vikse, M. L. Hansson, A. E. Wallberg, and M. Bakke. 2008. Phosphorylation of steroidogenic factor 1 is mediated by cyclin-dependent kniase 7. Mol. Endocrinol. 22:91–104.
  • Liu, Z., and E. R. Simpson. 1997. Steroidogenic factor 1 (SF-1) and SP1 are required for regulation of bovine CYP11A gene expression in bovine luteal cells and adrenal Y1 cells. Mol. Endocrinol. 11:127–137.
  • Mizusaki, H., K. Kawabe, T. Mukai, E. Ariyoshi, M. Kasahara, H. Yoshioka, A. Swain, and K. Morohashi. 2003. Dax-1 (dosage-sensitive sex reversal-adrenal hypoplasia congenita critical region on the X chromosome, gene 1) gene transcription is regulated by wnt4 in the female developing gonad. Mol. Endocrinol. 17:507–519.
  • Monte, D., F. DeWitte, and D. W. Hum. 1998. Regulation of the human P450scc gene by steroidogenic factor 1 is mediated by CBP/p300. J. Biol. Chem. 273:4585–4591.
  • Nachtigal, M. W., Y. Hirokawa, D. L. Enyeart-VanHouten, J. N. Flanagan, G. D. Hammer, and H. A. Ingraham. 1998. Wilms' tumor 1 and Dax-1 modulate the orphan nuclear receptor SF-1 in sex-specific gene expression. Cell 93:445–454.
  • Nishida, T., M. Terashima, K. Fukami, and Y. Yamada. 2007. Repression of E1AF transcriptional activity by sumoylation and PIASy. Biochem. Biophys. Res. Commun. 360:226–232.
  • Ou, Q., J. F. Mouillet, X. Yan, C. Dorn, P. A. Crawford, and Y. Sadovsky. 2001. The DEAD box protein DP103 is a regulator of steroidogenic factor-1. Mol. Endocrinol. 15:69–79.
  • Owerbach, D., E. M. McKay, E. T. Yeh, K. H. Gabbay, and K. M. Bohren. 2005. A praline-90 residue unique to SUMO-4 prevents maturation and sumoylation. Biochem. Biophys. Res. Commun. 337:517–520.
  • Pichler, A., A. Gast, J. S. Seeler, A. Dejean, and F. Melchior. 2002. The Nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108:109–120.
  • Riedl, T., and J. M. Egly. 2000. Phosphorylation in transcription: the CTD and more. Gene Expr. 9:3–13.
  • Rui, X., J. Tsao, J. O. Scheys, G. D. Hammer, and B. P. Schimmer. 2008. Contributions of specificity protein-1 and steroidogenic factor 1 to Adcy4 expression in Y1 mouse adrenal cells. Endocrinology 149:3668–3678.
  • Rytinki, M. M., and J. J. Palvimo. 2008. SUMOylation modulates the transcription repressor function of RIP140. J. Biol. Chem. 283:11586–11595.
  • Sachdev, S., L. Bruhn, H. Sieber, A. Pichler, F. Melchior, and R. Grosschedl. 2001. PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev. 15:3088–3103.
  • Saotoh, H., and J. Hinchey. 2000. Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 275:6252–6258.
  • Song, L., S. Bhattacharya, A. A. Yunus, C. D. Lima, and C. Schindler. 2006. Stat1 and SUMO modification. Blood 108:3237–3244.
  • Spengler, M. L., L. W. Guo, and M. G. Brattain. 2008. Phosphorylation mediates Sp1 coupled activities of proteolytic processing, desumoylation and degradation. Cell Cycle. 7:623–630.
  • Su, H. L., and S. S. Li. 2002. Molecular features of human ubiquitin-like SUMO genes and their encoded proteins. Gene 296:65–73.
  • Subramanian, L., M. D. Benson, and J. A. Iniguez-Lluhi. 2003. A synergy control motif within the attenuator domain of CCAAT/enhancer-binding protein alpha inhibits transcriptional synergy through its PIASy-enhanced modification by SUMO-1 or SUMO-3. J. Biol. Chem. 278:9134–9141.
  • Sugawara, T., J. A. Holt, M. Kiriakidou, and J. F. Strauss III. 1996. Steroidogenic factor 1-dependent promoter activity of the human steroidogenic acute regulatory protein (StAR) gene. Biochemistry 35:9052–9059.
  • Tremblay, A. M., B. J. Wilson, X. J. Yang, and V. Giguere. 2008. Phosphorylation-dependent sumoylation regulates estrogen-related receptor-α and -γ transcriptional activity through a synergy control motif. Mol. Endocrinol. 22:570–584.
  • Tremblay, J. J., A. Marcil, Y. Gauthier, and J. Drouin. 1999. Ptx1 regulates SF-1 activity by an interaction that mimics the role of the ligand-binding domain. EMBO J. 18:3431–3441.
  • Tremblay, J. J., and R. S. Viger. 1999. Transcription factor GATA-4 enhances Mullerian inhibiting substance gene transcription through a direct interaction with the nuclear receptor SF-1. Mol. Endocrinol. 13:1388–1401.
  • Vanhatupa, S., D. Ungureanu, M. Paakkunainen, and O. Silvennoinen. 2008. MAPK-induced Ser727 phosphorylation promotes SUMOylation of STAT1. Biochem. J. 409:179–185.
  • Vu, E. H., R. J. Kraus, and J. E. Mertz. 2007. Phosphorylation-dependent sumoylation of estrogen-related receptor α1. Biochemistry 46:9795–9804.
  • Wang, M., Y. Ikeda, X. Lou, K. M. Caron, T. J. Weber, A. Swain, B. P. Schimmer, and K. L. Parker. 1997. Steroidogenic factor 1 plays multiple roles in endocrine development and function. Recent Prog. Horm. Res. 52:167–182.
  • Watanabe, K., T. R. Clarke, A. H. Lane, X. Wang, and P. K. Donahoe. 2000. Endogenous expression of Müllerian inhibiting substance in early postnatal rat Sertoli cells requires multiple steroidogenic factor-1 and GATA-4-binding sites. Proc. Natl. Acad. Sci. USA 97:1624–1629.
  • Winnay, J. N., and G. D. Hammer. 2006. Adrenocorticotropic hormone-mediated signaling cascades coordinate a cyclic pattern of steroidogenic factor 1-dependent transcriptional activation. Mol. Endocrinol. 20:147–166.
  • Yang, C., D. Zhou, and S. Chen. 1998. Modulation of aromatase expression in the breast tissue by ERRα-1 orphan receptor. Cancer Res. 58:5695–5700.
  • Yang, S. H., A. Galanis, J. Witty, and A. D. Sharrocks. 2006. An extended consensus motif enhances the specificity of substrate modification by SUMO. EMBO J. 25:5083–5093.
  • Zhang, P., and S. H. Mellon. 1996. The orphan nuclear receptor steroidogenic factor-1 regulates the cyclic adenosine 3′,5′-monophosphate-mediated transcriptional activation of rat cytochrome P450c17 (17 alpha-hydroxylase/c17-20 lyase). Mol. Endocrinol. 10:147–158.

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