Phosphorylation-dependent sumoylation of estrogen-related receptor α1

Biochemistry

Volumn 46, Issue 34, 2007, Pages 9795-9804

  Vu, Elizabeth H ^a   Kraus, Richard J ^a   Mertz, Janet E ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COACTIVATORS; ESTROGEN RESPONSE ELEMENTS (ERE); SUMOYLATION; TRANSCRIPTIONAL ACTIVITIES;

AMINO ACIDS; ELECTROPHORETIC MOBILITY; LIGANDS; MUTAGENESIS; PHOSPHORYLATION;

HORMONES;

ALANINE; ESTROGEN RELATED RECEPTOR ALPHA; ESTROGEN RELATED RECEPTOR ALPHA1; FLUORESCENT DYE; FULVESTRANT; LYSINE; NUCLEAR RECEPTOR COACTIVATOR 2; SERINE; STEROID RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN MCF 7; CONTROLLED STUDY; DNA PROTEIN COMPLEX; ESTROGEN RESPONSIVE ELEMENT; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; SITE DIRECTED MUTAGENESIS; SUMOYLATION; TRANSCRIPTION REGULATION;

BREAST NEOPLASMS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PLASMIDS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, ESTROGEN; SUMO-1 PROTEIN; TRANSCRIPTION, GENETIC; TUMOR CELLS, CULTURED;

EID: 34548363925     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700316g     Document Type: Article

References (43)

1. Giguère, V., Yang, N., Segui, P., and Evans, R. M. (1988) Identification of a new class of steroid hormone receptors, Nature 331, 91-94.
2. Chen, F., Zhang, Q., McDonald, T., Davidoff, M. J., Bailey, W., Bai, C., Liu, Q., and Caskey, C. T. (1999) Identification of two hERR2-related novel nuclear receptors utilizing bioinformatics and inverse PCR, Gene 228, 101-109.
3. Heard, D. J., Norby, P. L., Holloway, J., and Vissing, H. (2000) Human ERRγ, a third member of the estrogen receptor-related (ERR) subfamily of orphan receptors: Tissue-specific isoforms are expressed during development and in the adult, Mol. Endocrinol. 14, 382-392.
4. Giguère, V. (2002) To ERR in the estrogen pathway, Trends Endocrinol. Metab. 13, 220-225.
5. Ariazi, E. A., and Jordan, V. C. (2006) Estrogen-related receptors as emerging targets in cancer and metabolic disorders, Curr. Top. Med. Chem. 6, 203-215.
6. Stein, R. A., and McDonnell, D. P. (2006) Estrogen-related receptor {alpha} as a therapeutic target in cancer, Endocr. Relat. Cancer 13, S25-S32.
7. Yang, N., Shigeta, H., Shi, H., and Teng, C. T. (1996) Estrogen-related receptor, hERR1, modulates estrogen receptor-mediated response of human lactoferrin gene promoter, J. Biol. Chem. 271, 5795-5804.
8. Xie, W., Hong, H., Yang, N. N., Lin, R. J., Simon, C. M., Stallcup, M. R., and Evans, R. M. (1999) Constitutive activation of transcription and binding of coactivator by estrogen-related receptors 1 and 2, Mol. Endocrinol. 13, 2151-2162.
9. Sladek, R., Bader, J.-A., and Giguere, V. (1997) The orphan nuclear receptor estrogen-related receptor a is a transcriptional regulator of the human medium-chain acyl coenzyme A dehydrogenase gene, Mol. Cell. Biol. 17, 5400-5409.
10. Johnston, S. D., Liu, X., Zuo, F., Eisenbraun, T. L., Wiley, S. R., Kraus, R. J., and Mertz, J. E. (1997) Estrogen-related receptor α1 functionally binds as a monomer to extended half-site sequences including ones contained within estrogen-response elements, Mol. Endocrinol. 11, 342-352.
11. Yang, C., Zhou, D., and Chen, S. (1998) Modulation of aromatase expression in the breast tissue by ERRα-1 orphan receptor, Cancer Res. 58, 5695-5700.
12. Kraus, R. J., Ariazi, E. A., Farrell, M. L., and Mertz, J. E. (2002) Estrogen-related receptor α1 actively antagonizes estrogen receptor regulated transcription in MCF-7 mammary cells, J. Biol. Chem. 277, 24826-24834.
13. Barry, J. B., Laganière, J., and Giguère, V. (2006) A single nucleotide in an estrogen-related receptor a site can dictate mode of binding and peroxisome proliferator-activated receptor y coactivator 1alpha activation of target promoters, Mol. Endocrinol. 20, 302-310.
14. Herzog, B., Cardenas, J., Hall, R. K., Villena, J. A., Budge, P. J., Giguère, V., Granner, D. K., and Kralli, A. (2006) Estrogen-related receptor a is a repressor of phosphoenolpyruvate carboxykinase gene transcription, J. Biol. Chem. 281, 99-106.
15. Ariazi, E. A., Kraus, R. J., Farrell, M. L., Jordan, V. C., and Mertz, J. E. (2007) Estrogen-related receptor α1 transcriptional activities are regulated in part via the ErbB2/HER2 signaling pathway, Mol. Cancer Res. 5, 71-85.
16. Barry, J. B., and Giguère, V. (2005) Epidermal growth factor-induced signaling in breast cancer cells results in selective target gene activation by orphan nuclear receptor estrogen-related receptor α, Cancer Res. 65, 6120-6129.
17. Ichida, M., Nemoto, S., and Finkel, T. (2002) Identification of a specific molecular repressor of the peroxisome proliferator-activated receptor γ coactivator-1 α (PGC-1α), J. Biol. Chem. 227, 50991-50995.
18. Castet, A., Herledan, A., Bonnet, S., Jalaguier, S., Vanacker, J.-M., and Cavaillès, V. (2006) Receptor-interacting protein 140 differentially regulates estrogen receptor-related receptor transactivation depending on target genes, Mol. Endocrinol. 20, 1035-1047.
19. Watanabe, A., Kinoshita, Y., Hosokawa, K., Mori, T., Yamaguchi, T., and Honjo, H. (2006) Function of estrogen-related receptor a in human endometrial cancer, J. Clin. Endocrinol. Metab. 91, 1573-577.
20. Hietakangas, V., Anckar, J., Blomster, H. A., Fujimoto, M., Palvimo, J. J., Nakai, A., and Sistonen, L. (2006) PDSM, a motif for phosphorylation- dependent SUMO modification, Proc. Natl. Acad. Sci. U.S.A. 103, 45-50.
21. Iñiguez-Lluhí, J. A., and Pearce, D. (2000) A common motif within the negative regulatory regions of multiple factors inhibits their transcriptional synergy, Mol. Cell. Biol. 20, 6040-6050.
22. Rogatsky, I., Zarember, K. A., and Yamamoto, K. R. (2001) Factor recruitment and TIF2/GRIP1 corepressor activity at a collagenase-3 response element that mediates regulation by phorbol esters and hormones, EMBO J. 20, 6071-6083.
23. Holmstrom, S., Van Antwerp, M. E., and Iñiguez-Lluhí, J. A. (2003) Direct and distinguishable inhibitory roles for SUMO isoforms in the control of transcriptional synergy, Proc. Natl. Acad. Sci. U.S.A. 100, 15758-1563.
24. Bailey, D., and O'Hare, P. (2002) Herpes simplex virus 1 ICP0 co-localizes with a SUMO- specific protease, J. Gen. Virol. 83, 2951-2964.
25. Jiang, S.-Y., Wolf, D. M., Yingling, J. M., Chang, C., and Jordan, V. C. (1992) An estrogen receptor positive MCF-7 clone that is resistant to antiestrogens and estradiol, Mol. Cell. Endocrinol. 90, 77-86.
26. Levenson, A. S., and Jordan, V. C. (1997) MCF-7: The first hormone-responsive breast cancer cell line, Cancer Res. 57, 3071-3078.
27. Adams, M., Reginato, M. J., Shao, D., Lazar, M. A., and Chatterjee, V. K. (1997) Transcriptional activation by peroxisome proliferator-activated receptor γ is inhibited by phosphorylation at a consensus mitogen-activated protein kinase site, J. Biol. Chem. 272, 5128-5132.
28. Metivier, R., Stark, A., Flouriot, G., Hübner, M. R., Brand, H., Penot, G., Manu, D., Denger, S., Reid, G., Koš, M., Russell, R. B., Kah, O., Pakdel, F., and Gannon, F. (2002) A dynamic structural model for estrogen receptor a activation by ligands, emphasizing the role of interactions between distant A and E domains, Mol. Cell 10, 1019-1032.
29. Wang, L., Lin, H.-K., Hu, Y.-C., Xie, S., Yang, L., and Chang, C. (2004) Suppression of androgen receptor-mediated transactivation and cell growth by glycogen synthase kinase 3β in prostate cancer cells, J. Biol. Chem. 279, 32444-32452.
30. Weigel, N. L. (1996) Steroid hormone receptors and their regulation by phosphorylation, Biochem. J. 319, 657-667.
31. Zhang, Z., and Teng, C. T. (2000) Estrogen receptor-related receptor α1 interacts with coactivator and constitutively activates the estrogen response elements of the human lactoferrin gene, J. Biol. Chem. 275, 20837-20846.
32. Hauser, S., Adelmant, G., Sarraf, P., Wright, H. M., Mueller, E., and Spiegelman, B. M. (2000) Degradation of the peroxisome proliferator-activated receptor γ is linked to ligand- dependent activation, J. Biol. Chem. 275, 18527-18533.
33. Kopf, E., Plassat, J. L., Vivat, V., de The, H., Chambon, P., and Rochette-Egly, C. (2000) Dimerization with retinoid X receptors and phosphorylation modulate the retinoic acid-induced degradation of retinoic acid receptors α and γ through the ubiquitin-proteasome pathway, J. Biol. Chem. 275, 33280-33288.
34. Lonard, D. M., Nawaz, Z., Smith, C. L. and O'Malley, B. W. (2000) The 26S proteasome is required for estrogen receptor α and coactivator turnover and for efficient estrogen receptor- α transactivation, Mol Cell 5, 939-948.
35. Gill, G. (2005) Something about SUMO inhibits transcription, Curr. Opin. Genet. Dev. 15, 536-541.
36. Johnson, E. S. (2004) Protein modification by SUMO, Annu. Rev. Biochem. 73, 355-382.
37. Yang, S.-H., Galanis, A., Witty, J., and Sharrocks, A. D. (2006) An extended consensus motif enhances the specificity of substrate modification by SUMO, EMBO J. 25, 5083-5093.
38. Stankovic-Valentin, N., Deltour, S., Seeler J., Pinte, S., Vergoten, G., Guerardel, C., Dejean, A., and Leprince, D. (2007) An acetylation/deacetylation- SUMOylation switch through a phylogenetically conserved ψKXEP motif in the tumor suppressor HICI regulates transcriptional repression activity, Mol. Cell. Biol. 27, 2661-2675.
39. Wang, L., Hsu, C.-L., and Chang, C. (2005) Androgen receptor corepressors: an overview, Prostate 63, 117-130.
40. Abdel-Hafiz, H., Takimoto, G. S., Tung, L., and Horwitz, K. B. (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.
41. Poukka, H., Karvonen, U., Jänne, O.A., and Palvimo, J. J. (2000) Covalent modification of the androgen receptor by small ubiquitin-like modifier 1 (SUMO-1), PNAS 97, 14145-14150.
42. Schreiber, S. N., Knutti, D., Brogli, K., Uhlmann, T., and Kralli, A. (2003) The transcriptional coactivator PGC-1 regulates the expression and activity of the orphan nuclear receptor estrogen-related receptor α (ERRα), J. Biol. Chem. 278, 9013-9018.
43. Atalay, G., Cardoso, F., Awada, A., and Piccart, M. J. (2003) Novel therapeutic strategies targeting the epidermal growth factor receptor (EGFR) family and its downstream effectors in breast cancer, Ann. Oncol. 14, 1346-1363.