Small ubiquitin-like modifier (SUMO) modification mediates function of the inhibitory domains of developmental regulators FOXC1 and FOXC2

Journal of Biological Chemistry

Volumn 287, Issue 22, 2012, Pages 18318-18329

  Danciu, Theodora E ^a   Chupreta, Sergey ^b   Cruz, Osvaldo ^b   Fox, Jennifer E ^a   Whitman, Malcolm ^c   Iñiguez Lluhí, Jorge A ^b  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FORKHEAD TRANSCRIPTIONS; IN-VITRO; INHIBITORY DOMAINS; INHIBITORY FUNCTION; ISOFORMS; N-TERMINALS; POST-TRANSLATIONAL MODIFICATIONS; PROTEIN LEVEL; REGULATORY REGIONS; SMALL UBIQUITIN-LIKE MODIFIERS; SUBCELLULAR LOCALIZATIONS; SUMOYLATION; TRANSCRIPTIONAL ACTIVITY; WILD TYPES;

CELL CULTURE; PHOSPHORYLATION;

TRANSCRIPTION FACTORS;

SUMO 2 PROTEIN; SUMO 3 PROTEIN; SUMO PROTEIN; TRANSCRIPTION FACTOR FOXC1; TRANSCRIPTION FACTOR FOXC2;

AMINO TERMINAL SEQUENCE; ARTICLE; CELLULAR DISTRIBUTION; CONJUGATION; CONTROLLED STUDY; EMBRYO; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REGULATORY MECHANISM; STRUCTURE ACTIVITY RELATION; SUMOYLATION; SYNERGY CONTROL MOTIF;

BASE SEQUENCE; BLOTTING, WESTERN; CELL LINE; DNA PRIMERS; FLUORESCENT ANTIBODY TECHNIQUE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; PHOSPHORYLATION; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS;

EID: 84861551937     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.339424     Document Type: Article

References (62)

1. Kaestner, K. H., Knochel, W., and Martinez, D. E. (2000) Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev. 14, 142-146 (Pubitemid 30070978)
2. Carlsson, P., and Mahlapuu, M. (2002) Forkhead transcription factors: key players in development and metabolism. Dev. Biol. 250, 1-23
3. Hiemisch, H., Schütz, G., and Kaestner, K. H. (1998) The mouse Fkh1/Mf1 gene: cDNA sequence, chromosomal localization, and expression in adult tissues. Gene 220, 77-82 (Pubitemid 28470325)
4. Tümer, Z., and Bach-Holm, D. (2009) Axenfeld-Rieger syndrome and spectrum of PITX2 and FOXC1 mutations. Eur. J. Hum. Genet. 17, 1527-1539
5. Hong, H. K., Lass, J. H., and Chakravarti, A. (1999) Pleiotropic skeletal and ocular phenotypes of the mouse mutation congenital hydrocephalus (ch/Mf1) arise from a winged helix/forkhead transcription factor gene. Hum. Mol. Genet. 8, 625-637 (Pubitemid 29139977)
6. Kume, T., Deng, K. Y., Winfrey, V., Gould, D. B., Walter, M. A., and Hogan, B. L. (1998) The forkhead/winged helix gene Mf1 is disrupted in the pleiotropic mouse mutation congenital hydrocephalus. Cell 93, 985-996 (Pubitemid 28280792)
7. Winnier, G. E., Kume, T., Deng, K., Rogers, R., Bundy, J., Raines, C., Walter, M. A., Hogan, B. L., and Conway, S. J. (1999) Roles for the winged helix transcription factors MF1 and MFH1 in cardiovascular development revealed by nonallelic noncomplementation of null alleles. Dev. Biol. 213, 418-431 (Pubitemid 29444350)
8. Kume, T. (2008) Foxc2 transcription factor: a newly described regulator of angiogenesis. Trends Cardiovasc. Med. 18, 224-228
9. Iida, K., Koseki, H., Kakinuma, H., Kato, N., Mizutani-Koseki, Y., Ohuchi, H., Yoshioka, H., Noji, S., Kawamura, K., Kataoka, Y., Ueno, F., Taniguchi, M., Yoshida, N., Sugiyama, T., and Miura, N. (1997) Essential roles of the winged helix transcription factor MFH-1 in aortic arch patterning and skeletogenesis. Development 124, 4627-4638 (Pubitemid 27519257)
10. Kume, T., Jiang, H., Topczewska, J. M., and Hogan, B. L. (2001) The murine winged helix transcription factors, Foxc1 and Foxc2, are both required for cardiovascular development and somitogenesis. Genes Dev. 15, 2470-2482 (Pubitemid 32899749)
11. Saitoh, H., and Hinchey, J. (2000) Functional heterogeneity of small ubiquitin- related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 275, 6252-6258 (Pubitemid 30129915)
12. Su, H. L., and Li, S. S. (2002) Molecular features of human ubiquitin-like SUMO genes and their encoded proteins. Gene 296, 65-73
13. Gareau, J. R., and Lima, C. D. (2010) The SUMO pathway: emerging mechanisms that shape specificity, conjugation, and recognition. Nat. Rev. Mol. Cell Biol. 11, 861-871
14. Bohren, K. M., Nadkarni, V., Song, J. H., Gabbay, K. H., and Owerbach, D. (2004) An 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 (Pubitemid 38812561)
15. Owerbach, D., McKay, E. M., Yeh, E. T., Gabbay, K. H., and Bohren, K. M. (2005) A proline 90 residue unique to SUMO-4 prevents maturation and sumoylation. Biochem. Biophys. Res. Commun. 337, 517-520 (Pubitemid 41429315)
16. Olsen, S. K., Capili, A. D., Lu, X., Tan, D. S., and Lima, C. D. (2010) Active site remodeling accompanies thioester bond formation in the SUMO E1. Nature 463, 906-912
17. Johnson, E. S., and Blobel, G. (1997) Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J. Biol. Chem. 272, 26799-26802 (Pubitemid 27452622)
18. Bernier-Villamor, V., Sampson, D. A., Matunis, M. J., and Lima, C. D. (2002) Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108, 345-356 (Pubitemid 34178399)
19. Palvimo, J. J. (2007) PIAS proteins as regulators of small ubiquitin-related modifier (SUMO) modifications and transcription. Biochem. Soc Trans. 35, 1405-1408
20. Yeh, E. T. (2009) SUMOylation and de-SUMOylation: wrestling with life's processes. J. Biol. Chem. 284, 8223-8227
21. Iñiguez-Lluhí, J. A. (2009) Control of Transcription by SUMO modification. in SUMO Regulation of Cellular Processes (Wilson, V. G. ed) pp. 13-40, Springer-Verlag New York Inc., New York
22. 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 (Pubitemid 30613052)
23. Poukka, H., Karvonen, U., Janne, O. A., and Palvimo, J. J. (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 (Pubitemid 32016544)
24. Subramanian, L., Benson, M. D., and Iñiguez-Lluhí, J. A. (2003) A synergy control motif within the attenuator domain of CCAAT/enhancer-binding protein α inhibits transcriptional synergy through its PIASy-enhanced modification by SUMO-1 or SUMO-3. J. Biol. Chem. 278, 9134-9141 (Pubitemid 36800394)
25. Holmstrom, S., Van Antwerp, M. E., and Iñiguez-Lluhi, 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, 15758-15763 (Pubitemid 38021063)
26. Holmstrom, S. R., Chupreta, S., So, A. Y., and Iñiguez- Lluhí, J. A. (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
27. Berry, F. B., Saleem, R. A., and Walter, M. A. (2002) FOXC1 transcriptional regulation is mediated by N- and C-terminal activation domains and contains a phosphorylated transcriptional inhibitory domain. J. Biol. Chem. 277, 10292-10297 (Pubitemid 34968145)
28. Fujita, H., Kang, M., Eren, M., Gleaves, L. A., Vaughan, D. E., and Kume, T. (2006) Foxc2 is a common mediator of insulin and transforming growth factor β signaling to regulate plasminogen activator inhibitor type I gene expression. Circ. Res. 98, 626-634
29. Danciu, T. E., and Whitman, M. (2010) Oxidative stress drives disulfide bond formation between basic helix-loop-helix transcription factors. J. Cell Biochem. 109, 417-424
30. Makarova, O., Kamberov, E., and Margolis, B. (2000) Generation of deletion and point mutations with one primer in a single cloning step. Bio- Techniques 29, 970-972
31. Iñiguez-Lluhí, J. A., Lou, D. Y., and Yamamoto, K. R. (1997) Three amino acid substitutions selectively disrupt the activation but not the repression function of the glucocorticoid receptor N terminus. J. Biol. Chem. 272, 4149-4156 (Pubitemid 27078481)
32. Saleem, R. A., Banerjee-Basu, S., Berry, F. B., Baxevanis, A. D., and Walter, M. A. (2001) Analyses of the effects that disease-causing missense mutations have on the structure and function of the winged helix protein FOXC1. Am. J. Hum. Genet. 68, 627-641 (Pubitemid 32202758)
33. Watanabe, M., and Whitman, M. (1999) FAST-1 is a key maternal effector of mesoderm inducers in the early Xenopus embryo. Development 126, 5621-5634 (Pubitemid 30035011)
34. Nieuwkoop, P. D., and Faber, J. (1994) Normal Table of Xenopus laevis (Daudin): A Systematical and Chronological Survey of the Development from the Fertilized Egg till the End of Metamorphosis, Garland Pub., New York
35. Chupreta, S., Brevig, H., Bai, L., Merchant, J. L., and Iñiguez-Lluhí, J. A. (2007) Sumoylation-dependent control of homotypic and heterotypic synergy by the Kruppel-type zinc finger protein ZBP-89. J. Biol. Chem. 282, 36155-36166
36. Reverter, D., and Lima, C. D. (2006) Structural basis for SENP2 protease interactions with SUMO precursors and conjugated substrates. Nat. Struct. Mol. Biol. 13, 1060-1068 (Pubitemid 44885915)
37. Benson, M. D., Li, Q. J., Kieckhafer, K., Dudek, D., Whorton, M. R., Sunahara, R. K., Iñiguez-Lluhí, J. A., and Martens, J. R. (2007) SUMO modification regulates inactivation of the voltage-gated potassium channel Kv1.5. Proc. Natl. Acad. Sci. U.S.A. 104, 1805-1810 (Pubitemid 46239860)
38. 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 (Pubitemid 44658526)
39. Yang, W. H., Heaton, J. H., Brevig, H., Mukherjee, S., Iñiguez-Lluhí, J. A., and Hammer, G. D. (2009) SUMOylation inhibits SF-1 activity by reducing CDK7-mediated serine 203 phosphorylation. Mol. Cell Biol. 29, 613-625
40. Obenauer, J. C., Cantley, L. C., and Yaffe, M. B. (2003) Scansite 2.0: proteome- wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31, 3635-3641 (Pubitemid 37442212)
41. Berry, F. B., Mirzayans, F., and Walter, M. A. (2006) Regulation of FOXC1 stability and transcriptional activity by an epidermal growth factor-activated mitogen-activated protein kinase signaling cascade. J. Biol. Chem. 281, 10098-10104 (Pubitemid 43864545)
42. Pierrou, S., Enerbäck, S., and Carlsson, P. (1995) Selection of high-affinity binding sites for sequence-specific, DNA-binding proteins from random sequence oligonucleotides. Anal. Biochem. 229, 99-105
43. Gerin, I., Bommer, G. T., Lidell, M. E., Cederberg, A., Enerback, S., and Macdougald, O. A. (2009) On the role of FOX transcription factors in adipocyte differentiation and insulin-stimulated glucose uptake. J. Biol. Chem. 284, 10755-10763
44. Dotzlaw, H., Moehren, U., Mink, S., Cato, A. C., Iñiguez Lluhí, J. A., and Baniahmad, A. (2002) The amino terminus of the human AR is target for corepressor action and antihormone agonism. Mol. Endocrinol. 16, 661-673 (Pubitemid 34297738)
45. Lin, D. Y., Huang, Y. S., Jeng, J. C., Kuo, H. Y., Chang, C. C., Chao, T. T., Ho, C. C., Chen, Y. C., Lin, T. P., Fang, H. I., Hung, C. C., Suen, C. S., Hwang, M. J., Chang, K. S., Maul, G. G., and Shih, H. M. (2006) Role of SUMOinteracting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors. Mol. Cell 24, 341-354 (Pubitemid 44647910)
46. Rosendorff, A., Sakakibara, S., Lu, S., Kieff, E., Xuan, Y., DiBacco, A., Shi, Y., Shi, Y., and Gill, G. (2006) NXP-2 association with SUMO-2 depends on lysines required for transcriptional repression. Proc. Natl. Acad. Sci. U.S.A. 103, 5308-5313
47. Stielow, B., Sapetschnig, A., Wink, C., Krüger, I., and Suske, G. (2008) SUMO-modified Sp3 represses transcription by provoking local heterochromatic gene silencing. EMBO Rep 9, 899-906
48. Paws, P., and Stanier, P. (2009) SUMOylation in craniofacial disorders. in SUMO Regulation of Cellular Processes (Wilson, V. G. ed.) pp. 301-313, Springer-Verlag New York Inc., New York
49. Zhang, F. P., Mikkonen, L., Toppari, J., Palvimo, J. J., Thesleff, I., and Jänne, O. A. (2008) Sumo-1 function is dispensable in normal mouse development. Mol. Cell Biol. 28, 5381-5390
50. Alkuraya, F. S., Saadi, I., Lund, J. J., Turbe-Doan, A., Morton, C. C., and Maas, R. L. (2006) SUMO1 haploinsufficiency leads to cleft lip and palate. Science 313, 1751 (Pubitemid 44461865)
51. Lehmann, O. J., Ebenezer, N. D., Jordan, T., Fox, M., Ocaka, L., Payne, A., Leroy, B. P., Clark, B. J., Hitchings, R. A., Povey, S., Khaw, P. T., and Bhattacharya, S. S. (2000) Chromosomal duplication involving the forkhead transcription factor gene FOXC1 causes iris hypoplasia and glaucoma. Am. J. Hum. Genet. 67, 1129-1135
52. Berry, F. B., Lines, M. A., Oas, J. M., Footz, T., Underhill, D. A., Gage, P. J., and Walter, M. A. (2006) Functional interactions between FOXC1 and PITX2 underlie the sensitivity to FOXC1 gene dose in Axenfeld-Rieger syndrome and anterior segment dysgenesis. Hum. Mol. Genet. 15, 905-919 (Pubitemid 43338232)
53. Andreou, A. M., Pauws, E., Jones, M. C., Singh, M. K., Bussen, M., Doudney, K., Moore, G. E., Kispert, A., Brosens, J. J., and Stanier, P. (2007) TBX22 missense mutations found in patients with X-linked cleft palate affect DNA binding, sumoylation, and transcriptional repression. Am. J. Hum. Genet. 81, 700-712 (Pubitemid 47596539)
54. Ghioni, P., D'Alessandra, Y., Mansueto, G., Jaffray, E., Hay, R. T., La Mantia, G., and Guerrini, L. (2005) The protein stability and transcriptional activity of p63α are regulated by SUMO-1 conjugation. Cell Cycle 4, 183-190 (Pubitemid 41038949)
55. Huang, Y. P., Wu, G., Guo, Z., Osada, M., Fomenkov, T., Park, H. L., Trink, B., Sidransky, D., Fomenkov, A., and Ratovitski, E. A. (2004) Altered sumoylation of p63α contributes to the split-hand/foot malformation phenotype. Cell Cycle 3, 1587-1596 (Pubitemid 40521413)
56. Walsh, D. A., Klein, N. W., Hightower, L. E., and Edwards, M. J. (1987) Heat shock and thermotolerance during early rat embryo development. Teratology 36, 181-191 (Pubitemid 17161541)
57. Tamimi, Y., Lines, M., Coca-Prados, M., and Walter, M. A. (2004) Identification of target genes regulated by FOXC1 using nickel-agarose-based chromatin enrichment. Invest. Ophthalmol Vis. Sci. 45, 3904-3913 (Pubitemid 39411140)
58. Tamimi, Y., Skarie, J. M., Footz, T., Berry, F. B., Link, B. A., and Walter, M. A. (2006) FGF19 is a target for FOXC1 regulation in ciliary bodyderived cells. Hum. Mol. Genet. 15, 3229-3240 (Pubitemid 44605502)
59. Rice, R., Rice, D. P., Olsen, B. R., and Thesleff, I. (2003) Progression of calvarial bone development requires Foxc1 regulation of Msx2 and Alx4. Dev. Biol. 262, 75-87 (Pubitemid 37153105)
60. Rice, R., Rice, D. P., and Thesleff, I. (2005) Foxc1 integrates Fgf and Bmp signaling independently of twist or noggin during calvarial bone development. Dev. Dyn. 233, 847-852 (Pubitemid 40853461)
61. Hayashi, H., and Kume, T. (2008) Foxc transcription factors directly regulate Dll4 and Hey2 expression by interacting with the VEGF-Notch signaling pathways in endothelial cells. PLoS ONE 3, e2401
62. Mani, S. A., Yang, J., Brooks, M., Schwaninger, G., Zhou, A., Miura, N., Kutok, J. L., Hartwell, K., Richardson, A. L., and Weinberg, R. A. (2007) Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proc. Natl. Acad. Sci. U.S.A. 104, 10069-10074 (Pubitemid 47175264)