Foxp3 protein stability is regulated by cyclin-dependent kinase 2

Journal of Biological Chemistry

Volumn 288, Issue 34, 2013, Pages 24494-24502

  Morawski, Peter A ^a   Mehra, Parul ^a   Chen, Chunxia ^a   Bhatti, Tricia ^a   Wells, Andrew D ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-INFLAMMATORY CAPACITIES; CYCLIN-DEPENDENT KINASE; EXTRACELLULAR SIGNALS; INFLAMMATORY BOWEL DISEASE; INFLAMMATORY DISEASE; NEGATIVE REGULATORS; PRIMARY STRUCTURES; REGULATORY T CELLS;

AMINO ACIDS; CELL PROLIFERATION; CELLS; CYTOLOGY; DISEASES; ENZYMES; PROTEINS; SIGNAL TRANSDUCTION; STABILITY;

T-CELLS;

ALANINE; CYCLIN DEPENDENT KINASE 2; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; SERINE; THREONINE; TRANSCRIPTION FACTOR FOXP3;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; COLITIS; CONTROLLED STUDY; FEMALE; GENE INDUCTION; GENE REPRESSION; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN STRUCTURE; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; SITE DIRECTED MUTAGENESIS;

CDK (CYCLIN-DEPENDENT KINASE); FOXP3; PROTEIN PHOSPHORYLATION; T CELL; T CELL BIOLOGY; TRANSCRIPTION FACTORS;

AMINO ACID MOTIFS; ANIMALS; CYCLIN-DEPENDENT KINASE 2; DISEASE MODELS, ANIMAL; FORKHEAD TRANSCRIPTION FACTORS; HEK293 CELLS; HUMANS; INFLAMMATORY BOWEL DISEASES; MICE; MICE, MUTANT STRAINS; PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY;

EID: 84883164348     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.467704     Document Type: Article

References (46)

1. Hori, S., Nomura, T., and Sakaguchi, S. (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299, 1057-1061
2. + immune regulatory cells are required for induction of tolerance to alloantigen via costimulatory blockade. J. Exp. Med. 193, 1311-1318
3. + regulatory T cells. Nat. Immunol. 4, 330-336
4. + T regulatory cells. Nat. Immunol. 4, 337-342
5. + T cell effector function. J. Immunol. 171, 1216-1223
6. Chen, C., Rowell, E. A., Thomas, R. M., Hancock, W. W., and Wells, A. D. (2006) Transcriptional regulation by Foxp3 is associated with direct promoter occupancy and modulation of histone acetylation. J. Biol. Chem. 281, 36828-36834
7. Li, B., Samanta, A., Song, X., Iacono, K. T., Bembas, K., Tao, R., Basu, S., Riley, J. L., Hancock, W. W., Shen, Y., Saouaf, S. J., and Greene, M. I. (2007) FOXP3 interactions with histone acetyltransferase and class II histone deacetylases are required for repression. Proc. Natl. Acad. Sci. U.S.A. 104, 4571-4576
8. + T-cell differentiation regulated by networks of cytokines and transcription factors. Immunol. Rev. 238, 247-262
9. Samanta, A., Li, B., Song, X., Bembas, K., Zhang, G., Katsumata, M., Saouaf, S. J., Wang, Q., Hancock, W. W., Shen, Y., and Greene, M. I. (2008) TGF-β and IL-6 signals modulate chromatin binding and promoter occupancy by acetylated FOXP3. Proc. Natl. Acad. Sci. U.S.A. 105, 14023-14027
10. Kwon, H.-S., Lim, H. W., Wu, J., Schnölzer, M., Verdin, E., and Ott, M. (2012) Three novel acetylation sites in the Foxp3 transcription factor regulate the suppressive activity of regulatory T cells. J. Immunol. 188, 2712-2721
11. van Loosdregt, J., Vercoulen, Y., Guichelaar, T., Gent, Y. Y., Beekman, J. M., van Beekum, O., Brenkman, A. B., Hijnen, D.-J., Mutis, T., Kalkhoven, E., Prakken, B. J., and Coffer, P. J. (2010) Regulation of Treg functionality by acetylation-mediated Foxp3 protein stabilization. Blood 115, 965-974
12. van Loosdregt, J., Brunen, D., Fleskens, V., Pals, C. E. G. M., Lam, E. W. F., and Coffer, P. J. (2011) Rapid temporal control of Foxp3 protein degradation by sirtuin-1. PLoS ONE 6, e19047
13. Dang, E. V., Barbi, J., Yang, H.-Y., Jinasena, D., Yu, H., Zheng, Y., Bordman, Z., Fu, J., Kim, Y., Yen, H.-R., Luo, W., Zeller, K., Shimoda, L., Topalian, S. L., Semenza, G. L., Dang, C. V., Pardoll, D. M., and Pan, F. (2011) Control of TH17/Treg balance by hypoxia-inducible factor 1. Cell 146, 772-784
14. Chunder, N., Wang, L., Chen, C., Hancock, W. W., and Wells, A. D. (2012) Cyclin-dependent kinase 2 controls peripheral immune tolerance. J. Immunol. 189, 5659-5666
15. Pear, W. S., Nolan, G. P., Scott, M. L., and Baltimore, D. (1993) Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. U.S.A. 90, 8392-8396
16. Wells, A. D., Gudmundsdottir, H., and Turka, L. A. (1997) Following the fate of individual T cells throughout activation and clonal expansion. Signals from T cell receptor and CD28 differentially regulate the induction and duration of a proliferative response. J. Clin. Invest. 100, 3173-3183
17. + T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int. Immunol. 5, 1461-1471
18. + T cells. Immunity 1, 553-562
19. Conner, E. M., Brand, S., Davis, J. M., Laroux, F. S., Palombella, V. J., Fuseler, J. W., Kang, D. Y., Wolf, R. E., and Grisham, M. B. (1997) Proteasome inhibition attenuates nitric oxide synthase expression, VCAM-1 transcription, and the development of chronic colitis. J. Pharmacol. Exp. Ther. 282, 1615-1622
20. +, CD45RBhigh T cells to SCID recipients. J. Immunol. 158, 3464-3473
21. Bettelli, E., Dastrange, M., and Oukka, M. (2005) Foxp3 interacts with nuclear factor of activated T cells and NF-κB to repress cytokine gene expression and effector functions of T helper cells. Proc. Natl. Acad. Sci. U.S.A. 102, 5138-5143
22. Lopes, J. E., Torgerson, T. R., Schubert, L. A., Anover, S. D., Ocheltree, E. L., Ochs, H. D., and Ziegler, S. F. (2006) Analysis of FOXP3 reveals multiple domains required for its function as a transcriptional repressor. J. Immunol. 177, 3133-3142
23. Hunter, T. (2007) The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol. Cell 28, 730-738
24. + T cell suppressor function. J. Immunol. 172, 6519-6523
25. Beier, U. H., Wang, L., Bhatti, T. R., Liu, Y., Han, R., Ge, G., and Hancock, W. W. (2011) Sirtuin-1 targeting promotes Foxp3′ T-regulatory cell function and prolongs allograft survival. Mol. Cell Biol. 31, 1022-1029
26. Nie, H., Zheng, Y., Li, R., Guo, T. B., He, D., Fang, L., Liu, X., Xiao, L., Chen, X., Wan, B., Chin, Y. E., and Zhang, J. Z. (2013) Phosphorylation of FOXP3 controls regulatory T cell function and is inhibited by TNF-α in rheumatoid arthritis. Nat. Med. 19, 322-328
27. Kim, Y. H., Proust, J. J., Buchholz, M. J., Chrest, F. J., and Nordin, A. A. (1992) Expression of the murine homologue of the cell cycle control protein p34cdc2 in T lymphocytes. J. Immunol. 149, 17-23
28. Kim, Y. H., Buchholz, M. A., Chrest, F. J., and Nordin, A. A. (1994) Upregulation of c-myc induces the gene expression of the murine homologues of p34cdc2 and cyclin-dependent kinase-2 in T lymphocytes. J. Immunol. 152, 4328-4335
29. 1/S transition by 12-O-tetradecanoylphorbol-13-acetate (TPA) by modulation of CDK2 activity. Exp. Cell Res. 221, 92-102
30. 1/S phase transition. Nat. Cell Biol. 7, 831-836
31. Bashir, T., and Pagano, M. (2005) Cdk1: the dominant sibling of Cdk2. Nat. Cell Biol. 7, 779-781
32. Satyanarayana, A., and Kaldis, P. (2009) Mammalian cell-cycle regulation: several Cdks, numerous cyclins, and diverse compensatory mechanisms. Oncogene 28, 2925-2939
33. Berthet, C., Aleem, E., Coppola, V., Tessarollo, L., and Kaldis, P. (2003) Cdk2 knockout mice are viable. Curr. Biol. 13, 1775-1785
34. Ortega, S., Prieto, I., Odajima, J., Martín, A., Dubus, P., Sotillo, R., Barbero, J. L., Malumbres, M., and Barbacid, M. (2003) Cyclin-dependent kinase 2 is essential for meiosis but not for mitotic cell division in mice. Nat. Genet. 35, 25-31
35. Berthet, C., Rodriguez-Galan, M. C., Hodge, D. L., Gooya, J., Pascal, V., Young, H. A., Keller, J., Bosselut, R., and Kaldis, P. (2007) Hematopoiesis and thymic apoptosis are not affected by the loss of Cdk2. Mol. Cell Biol. 27, 5079-5089
36. Rubtsov, Y. P., Niec, R. E., Josefowicz, S., Li, L., Darce, J., Mathis, D., Benoist, C., and Rudensky, A. Y. (2010) Stability of the regulatory T cell lineage in vivo. Science 329, 1667-1671
37. König, S., Probst-Kepper, M., Reinl, T., Jeron, A., Huehn, J., Schraven, B., and Jänsch, L. (2012) First insight into the kinome of human regulatory T cells. PLoS ONE 7, e40896
38. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198, 1875-1886
39. 1 cyclin-Cdk protein kinase activity, is related to p21. Cell 78, 67-74
40. Kip1 mRNA and protein in murine B cells. J. Immunol. 160, 770-777
41. Koepp, D. M., Schaefer, L. K., Ye, X., Keyomarsi, K., Chu, C., Harper, J. W., and Elledge, S. J. (2001) Phosphorylation-dependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase. Science 294, 173-177
42. Besson, A., Gurian-West, M., Chen, X., Kelly-Spratt, K. S., Kemp, C. J., and Roberts, J. M. (2006) A pathway in quiescent cells that controls p27Kip1 stability, subcellular localization, and tumor suppression. Genes Dev. 20, 47-64
43. Nakayama, K. I., and Nakayama, K. (2006) Ubiquitin ligases: cell-cycle control and cancer. Nat. Rev. Cancer 6, 369-381
44. De Azevedo, W. F., Leclerc, S., Meijer, L., Havlicek, L., Strnad, M., and Kim, S. H. (1997) Inhibition of cyclin-dependent kinases by purine analogues: crystal structure of human cdk2 complexed with roscovitine. Eur. J. Biochem. 243, 518-526
45. Gallorini, M., Cataldi, A., and di Giacomo, V. (2012) Cyclin-dependent kinase modulators and cancer therapy. BioDrugs 26, 377-391
46. Li, L., Wang, H., Kim, J.s., Pihan, G., and Boussiotis, V. (2009) The cyclin dependent kinase inhibitor (R)-roscovitine prevents alloreactive T cell clonal expansion and protects against acute GvHD. Cell Cycle 8, 1794-1802