RSUME Enhances Glucocorticoid Receptor SUMOylation and Transcriptional Activity

REFERENCES

• Beato M, Chavez S, Truss M. 1996. Transcriptional regulation by steroid hormones. Steroids 61:240–251.
   PubMedGoogle Scholar
• Barnes PJ. 1998. Anti-inflammatory actions of glucocorticoids: molecular mechanisms. Clin. Sci. (Lond.) 94:557–572.
   PubMed Web of Science ®Google Scholar
• Gross KL, Cidlowski JA. 2008. Tissue-specific glucocorticoid action: a family affair. Trends Endocrinol. Metab. 19:331–339.
   PubMed Web of Science ®Google Scholar
• Sapolsky RM, Romero LM, Munck AU. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrinol. Rev. 21:55–89.
   PubMed Web of Science ®Google Scholar
• Ricketson D, Hostick U, Fang L, Yamamoto KR, Darimont BD. 2007. A conformational switch in the ligand-binding domain regulates the dependence of the glucocorticoid receptor on Hsp90. J. Mol. Biol. 368:729–741.
   PubMedGoogle Scholar
• Bledsoe RK, Montana VG, Stanley TB, Delves CJ, Apolito CJ, McKee DD, Consler TG, Parks DJ, Stewart EL, Willson TM, Lambert MH, Moore JT, Pearce KH, Xu HE. 2002. Crystal structure of the glucocorticoid receptor ligand binding domain reveals a novel mode of receptor dimerization and coactivator recognition. Cell 110:93–105.
   PubMed Web of Science ®Google Scholar
• Davies L, Karthikeyan N, Lynch JT, Sial EA, Gkourtsa A, Demonacos C, Krstic-Demonacos M. 2008. Cross talk of signaling pathways in the regulation of the glucocorticoid receptor function. Mol. Endocrinol. 22:1331–1344.
   PubMed Web of Science ®Google Scholar
• Holmstrom S, Van Antwerp ME, Iniguez-Lluhi JA. 2003. Direct and distinguishable inhibitory roles for SUMO isoforms in the control of transcriptional synergy. Proc. Natl. Acad. Sci. U. S. A. 100:15758–15763.
   PubMed Web of Science ®Google Scholar
• Ismaili N, Garabedian MJ. 2004. Modulation of glucocorticoid receptor function via phosphorylation. Ann. N. Y. Acad. Sci. 1024:86–101.
   PubMed Web of Science ®Google Scholar
• Mason SA, Housley PR. 1993. Site-directed mutagenesis of the phosphorylation sites in the mouse glucocorticoid receptor. J. Biol. Chem. 268:21501–21504.
   PubMedGoogle Scholar
• Tian S, Poukka H, Palvimo JJ, Janne OA. 2002. Small ubiquitin-related modifier-1 (SUMO-1) modification of the glucocorticoid receptor. Biochem. J. 367:907–911.
   PubMedGoogle Scholar
• Wallace AD, Cidlowski JA. 2001. Proteasome-mediated glucocorticoid receptor degradation restricts transcriptional signaling by glucocorticoids. J. Biol. Chem. 276:42714–42721.
   PubMed Web of Science ®Google Scholar
• Hay RT. 2005. SUMO: a history of modification. Mol. Cell 18:1–12.
   PubMed Web of Science ®Google Scholar
• Melchior F. 2000. SUMO—nonclassical ubiquitin. Annu. Rev. Cell Dev. Biol. 16:591–626.
   PubMed Web of Science ®Google Scholar
• Gareau JR, Lima CD. 2010. The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat. Rev. Mol. Cell Biol. 11:861–871.
   PubMed Web of Science ®Google Scholar
• Saitoh H, Hinchey J. 2000. Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 275:6252–6258.
   PubMed Web of Science ®Google Scholar
• Golebiowski F, Tatham MH, Nakamura A, Hay RT. 2010. High-stringency tandem affinity purification of proteins conjugated to ubiquitin-like moieties. Nat. Protoc. 5:873–882.
   PubMedGoogle Scholar
• Tatham MH, Matic I, Mann M, Hay RT. 2011. Comparative proteomic analysis identifies a role for SUMO in protein quality control. Sci. Signal. 4:rs4. doi:10.1126/scisignal.2001484.
   PubMed Web of Science ®Google Scholar
• Doerks T, Copley RR, Schultz J, Ponting CP, Bork P. 2002. Systematic identification of novel protein domain families associated with nuclear functions. Genome Res. 12:47–56.
   PubMed Web of Science ®Google Scholar
• Carbia-Nagashima A, Gerez J, Perez-Castro C, Paez-Pereda M, Silberstein S, Stalla GK, Holsboer F, Arzt E. 2007. RSUME, a small RWD-containing protein, enhances SUMO conjugation and stabilizes HIF-1alpha during hypoxia. Cell 131:309–323.
   PubMed Web of Science ®Google Scholar
• Le Drean Y, Mincheneau N, Le Goff P, Michel D. 2002. Potentiation of glucocorticoid receptor transcriptional activity by sumoylation. Endocrinology 143:3482–3489.
   PubMedGoogle Scholar
• Chupreta S, Brevig H, Bai L, Merchant JL, Iniguez-Lluhi JA. 2007. Sumoylation-dependent control of homotypic and heterotypic synergy by the Kruppel-type zinc finger protein ZBP-89. J. Biol. Chem. 282:36155–36166.
   PubMed Web of Science ®Google Scholar
• Subramanian L, Benson MD, Iniguez-Lluhi JA. 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.
   PubMed Web of Science ®Google Scholar
• Abdel-Hafiz H, Takimoto GS, Tung L, Horwitz KB. 2002. The inhibitory function in human progesterone receptor N termini binds SUMO-1 protein to regulate autoinhibition and transrepression. J. Biol. Chem. 277:33950–33956.
   PubMed Web of Science ®Google Scholar
• Iniguez-Lluhi JA, Pearce D. 2000. A common motif within the negative regulatory regions of multiple factors inhibits their transcriptional synergy. Mol. Cell. Biol. 20:6040–6050.
   PubMedGoogle Scholar
• Poukka H, Karvonen U, Janne OA, Palvimo JJ. 2000. Covalent modification of the androgen receptor by small ubiquitin-like modifier 1 (SUMO-1). Proc. Natl. Acad. Sci. U. S. A. 97:14145–14150.
   PubMed Web of Science ®Google Scholar
• Vu EH, Kraus RJ, Mertz JE. 2007. Phosphorylation-dependent sumoylation of estrogen-related receptor alpha1. Biochemistry 46:9795–9804.
   PubMedGoogle Scholar
• Holmstrom SR, Chupreta S, So AY, Iniguez-Lluhi JA. 2008. SUMO-mediated inhibition of glucocorticoid receptor synergistic activity depends on stable assembly at the promoter but not on DAXX. Mol. Endocrinol. 22:2061–2075.
   PubMedGoogle Scholar
• Gottlicher M, Heck S, Doucas V, Wade E, Kullmann M, Cato AC, Evans RM, Herrlich P. 1996. Interaction of the Ubc9 human homologue with c-Jun and with the glucocorticoid receptor. Steroids 61:257–262.
   PubMedGoogle Scholar
• Cho S, Kagan BL, Blackford JAJr, Szapary D, Simons SSJr. 2005. Glucocorticoid receptor ligand binding domain is sufficient for the modulation of glucocorticoid induction properties by homologous receptors, coactivator transcription intermediary factor 2, and Ubc9. Mol. Endocrinol. 19:290–311.
   PubMedGoogle Scholar
• Kaul S, Blackford JAJr, Cho S, Simons SSJr. 2002. Ubc9 is a novel modulator of the induction properties of glucocorticoid receptors. J. Biol. Chem. 277:12541–12549.
   PubMedGoogle Scholar
• Kotaja N, Aittomaki S, Silvennoinen O, Palvimo JJ, Janne OA. 2000. ARIP3 (androgen receptor-interacting protein 3) and other PIAS (protein inhibitor of activated STAT) proteins differ in their ability to modulate steroid receptor-dependent transcriptional activation. Mol. Endocrinol. 14:1986–2000.
   PubMedGoogle Scholar
• Tirard M, Jasbinsek J, Almeida OF, Michaelidis TM. 2004. The manifold actions of the protein inhibitor of activated STAT proteins on the transcriptional activity of mineralocorticoid and glucocorticoid receptors in neural cells. J. Mol. Endocrinol. 32:825–841.
   PubMedGoogle Scholar
• Lee GS, Simons SSJr. 2011. Ligand binding domain mutations of the glucocorticoid receptor selectively modify the effects with, but not binding of, cofactors. Biochemistry 50:356–366.
   PubMedGoogle Scholar
• Tao YG, Xu Y, Xu HE, Simons SSJr. 2008. Mutations of glucocorticoid receptor differentially affect AF2 domain activity in a steroid-selective manner to alter the potency and efficacy of gene induction and repression. Biochemistry 47:7648–7662.
   PubMedGoogle Scholar
• Kotaja N, Karvonen U, Janne OA, Palvimo JJ. 2002. The nuclear receptor interaction domain of GRIP1 is modulated by covalent attachment of SUMO-1. J. Biol. Chem. 277:30283–30288.
   PubMedGoogle Scholar
• Teyssier C, Ou CY, Khetchoumian K, Losson R, Stallcup MR. 2006. Transcriptional intermediary factor 1alpha mediates physical interaction and functional synergy between the coactivator-associated arginine methyltransferase 1 and glucocorticoid receptor-interacting protein 1 nuclear receptor coactivators. Mol. Endocrinol. 20:1276–1286.
   PubMedGoogle Scholar
• Desterro JM, Rodriguez MS, Hay RT. 1998. SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol. Cell 2:233–239.
   PubMed Web of Science ®Google Scholar
• Jaffray EG, Hay RT. 2006. Detection of modification by ubiquitin-like proteins. Methods 38:35–38.
   PubMedGoogle Scholar
• Tatham MH, Jaffray E, Vaughan OA, Desterro JM, Botting CH, Naismith JH, Hay RT. 2001. Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J. Biol. Chem. 276:35368–35374.
   PubMed Web of Science ®Google Scholar
• Ayaydin F, Dasso M. 2004. Distinct in vivo dynamics of vertebrate SUMO paralogues. Mol. Biol. Cell 15:5208–5218.
   PubMed Web of Science ®Google Scholar
• Rupprecht R, Arriza JL, Spengler D, Reul JM, Evans RM, Holsboer F, Damm K. 1993. Transactivation and synergistic properties of the mineralocorticoid receptor: relationship to the glucocorticoid receptor. Mol. Endocrinol. 7:597–603.
   PubMedGoogle Scholar
• Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494–498.
   PubMed Web of Science ®Google Scholar
• Paakinaho V, Makkonen H, Jaaskelainen T, Palvimo JJ. 2010. Glucocorticoid receptor activates poised FKBP51 locus through long-distance interactions. Mol. Endocrinol. 24:511–525.
   PubMedGoogle Scholar
• Tatham MH, Geoffroy MC, Shen L, Plechanovova A, Hattersley N, Jaffray EG, Palvimo JJ, Hay RT. 2008. RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 10:538–546.
   PubMed Web of Science ®Google Scholar
• Rytinki M, Kaikkonen S, Sutinen P, Paakinaho V, Rahkama V, Palvimo JJ. 2012. Dynamic SUMOylation is linked to the activity cycles of androgen receptor in the cell nucleus. Mol. Cell. Biol. 32:4195–4205.
   PubMedGoogle Scholar
• Kotaja N, Karvonen U, Janne OA, Palvimo JJ. 2002. PIAS proteins modulate transcription factors by functioning as SUMO-1 ligases. Mol. Cell. Biol. 22:5222–5234.
   PubMed Web of Science ®Google Scholar
• Yokota K, Shibata H, Kurihara I, Kobayashi S, Suda N, Murai-Takeda A, Saito I, Kitagawa H, Kato S, Saruta T, Itoh H. 2007. Coactivation of the N-terminal transactivation of mineralocorticoid receptor by Ubc9. J. Biol. Chem. 282:1998–2010.
   PubMedGoogle Scholar
• Suda N, Shibata H, Kurihara I, Ikeda Y, Kobayashi S, Yokota K, Murai-Takeda A, Nakagawa K, Oya M, Murai M, Rainey WE, Saruta T, Itoh H. 2011. Coactivation of SF-1-mediated transcription of steroidogenic enzymes by Ubc9 and PIAS1. Endocrinology 152:2266–2277.
   PubMedGoogle Scholar
• Li DP, Periyasamy S, Jones TJ, Sanchez ER. 2000. Heat and chemical shock potentiation of glucocorticoid receptor transactivation requires heat shock factor (HSF) activity. Modulation of HSF by vanadate and wortmannin. J. Biol. Chem. 275:26058–26065.
   PubMedGoogle Scholar
• Sanchez ER, Hu JL, Zhong S, Shen P, Greene MJ, Housley PR. 1994. Potentiation of glucocorticoid receptor-mediated gene expression by heat and chemical shock. Mol. Endocrinol. 8:408–421.
   PubMedGoogle Scholar
• Leonard MO, Godson C, Brady HR, Taylor CT. 2005. Potentiation of glucocorticoid activity in hypoxia through induction of the glucocorticoid receptor. J. Immunol. 174:2250–2257.
   PubMed Web of Science ®Google Scholar
• Sanchez ER. 1992. Heat shock induces translocation to the nucleus of the unliganded glucocorticoid receptor. J. Biol. Chem. 267:17–20.
   PubMed Web of Science ®Google Scholar