Mst1/Mst2 regulate development and function of regulatory T cells through modulation of Foxo1/Foxo3 stability in autoimmune disease

Journal of Immunology

Volumn 192, Issue 4, 2014, Pages 1525-1535

  Du, Xingrong ^a   Shi, Hao ^a   Li, Jiang ^a   Dong, Yongli ^a   Liang, Jieliang ^a   Ye, Jian ^a   Kong, Shanshan ^a   Zhang, Shujing ^a   Zhong, Tao ^a   Yuan, Zengqiang ^b   Xu, Tian ^a,c   Zhuang, Yuan ^a,d   Zheng, Biao ^e   Geng, Jian Guo ^f   Tao, Wufan ^a  

^a FUDAN UNIVERSITY   (China)

^b INSTITUTE OF BIOPHYSICS   (China)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

MST1 KINASE; MST2 KINASE; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; INFLAMMATION; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; REGULATORY T LYMPHOCYTE; SPLENOMEGALY; T LYMPHOCYTE ACTIVATION;

ADOPTIVE TRANSFER; ANIMALS; AUTOIMMUNE DISEASES; AUTOIMMUNITY; CELL LINE; FORKHEAD TRANSCRIPTION FACTORS; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY;

EID: 84896733607     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301060     Document Type: Article

References (45)

1. Ziegler, S. F. 2006. FOXP3: of mice and men. Annu. Rev. Immunol. 24: 209-226.
2. Ono, M., H. Yaguchi, N. Ohkura, I. Kitabayashi, Y. Nagamura, T. Nomura, Y. Miyachi, T. Tsukada, and S. Sakaguchi. 2007. Foxp3 controls regulatory T-cell function by interacting with AML1/Runx1. Nature 446: 685-689.
3. Allan, S. E., A. N. Alstad, N. Merindol, N. K. Crellin, M. Amendola, R. Bacchetta, L. Naldini, M. G. Roncarolo, H. Soudeyns, and M. K. Levings. 2008. Generation of potent and stable human CD4+ T regulatory cells by activation-independent expression of FOXP3. Mol. Ther. 16: 194-202.
4. Harada, Y., Y. Harada, C. Elly, G. Ying, J. H. Paik, R. A. DePinho, and Y. C. Liu. 2010. Transcription factors Foxo3a and Foxo1 couple the E3 ligase Cbl-b to the induction of Foxp3 expression in induced regulatory T cells. J. Exp. Med. 207: 1381-1391.
5. Ouyang, W., O. Beckett, Q. Ma, J. H. Paik, R. A. DePinho, and M. O. Li. 2010. Foxo proteins cooperatively control the differentiation of Foxp3+ regulatory T cells. Nat. Immunol. 11: 618-627.
6. Kerdiles, Y. M., E. L. Stone, D. R. Beisner, M. A. McGargill, I. L. Ch'en, C. Stockmann, C. D. Katayama, and S. M. Hedrick. 2010. Foxo transcription factors control regulatory T cell development and function. Immunity 33: 890-904.
7. Brunet, A., A. Bonni, M. J. Zigmond, M. Z. Lin, P. Juo, L. S. Hu, M. J. Anderson, K. C. Arden, J. Blenis, and M. E. Greenberg. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857-868.
8. Huang, H., K. M. Regan, F. Wang, D. Wang, D. I. Smith, J. M. van Deursen, and D. J. Tindall. 2005. Skp2 inhibits FOXO1 in tumor suppression through ubiquitin-mediated degradation. Proc. Natl. Acad. Sci. USA 102: 1649-1654.
9. Matsuzaki, H., H. Daitoku, M. Hatta, K. Tanaka, and A. Fukamizu. 2003. Insulin-induced phosphorylation of FKHR (Foxo1) targets to proteasomal degradation. Proc. Natl. Acad. Sci. USA 100: 11285-11290.
10. Haxhinasto, S., D. Mathis, and C. Benoist. 2008. The AKT-mTOR axis regulates de novo differentiation of CD4+Foxp3+ cells. J. Exp. Med. 205: 565-574.
11. Merkenschlager, M., and H. von Boehmer. 2010. PI3 kinase signalling blocks Foxp3 expression by sequestering Foxo factors. J. Exp. Med. 207: 1347-1350.
12. Fruman, D. A., and G. Bismuth. 2009. Fine tuning the immune response with PI3K. Immunol. Rev. 228: 253-272.
13. Zeng, Q., and W. Hong. 2008. The emerging role of the hippo pathway in cell contact inhibition, organ size control, and cancer development in mammals. Cancer Cell 13: 188-192.
14. Zhou, D., C. Conrad, F. Xia, J. S. Park, B. Payer, Y. Yin, G. Y. Lauwers, W. Thasler, J. T. Lee, J. Avruch, and N. Bardeesy. 2009. Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 16: 425-438.
15. Lu, L., Y. Li, S. M. Kim, W. Bossuyt, P. Liu, Q. Qiu, Y. Wang, G. Halder, M. J. Finegold, J. S. Lee, and R. L. Johnson. 2010. Hippo signaling is a potent in vivo growth and tumor suppressor pathway in the mammalian liver. Proc. Natl. Acad. Sci. USA 107: 1437-1442.
16. Song, H., K. K. Mak, L. Topol, K. Yun, J. Hu, L. Garrett, Y. Chen, O. Park, J. Chang, R. M. Simpson, et al. 2010. Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression. Proc. Natl. Acad. Sci. USA 107: 1431-1436.
17. Zhou, D., Y. Zhang, H. Wu, E. Barry, Y. Yin, E. Lawrence, D. Dawson, J. E. Willis, S. D. Markowitz, F. D. Camargo, and J. Avruch. 2011. Mst1 and Mst2 protein kinases restrain intestinal stem cell proliferation and colonic tumorigenesis by inhibition of Yes-associated protein (Yap) overabundance. Proc. Natl. Acad. Sci. USA 108: E1312-E1320.
18. Kim, T. S., D. H. Lee, S. K. Kim, S. Y. Shin, E. J. Seo, and D. S. Lim. 2012. Mammalian sterile 20-like kinase 1 suppresses lymphoma development by promoting faithful chromosome segregation. Cancer Res. 72: 5386-5395.
19. Cheung, W. L., K. Ajiro, K. Samejima, M. Kloc, P. Cheung, C. A. Mizzen, A. Beeser, L. D. Etkin, J. Chernoff, W. C. Earnshaw, and C. D. Allis. 2003. Apoptotic phosphorylation of histone H2B is mediated by mammalian sterile twenty kinase. Cell 113: 507-517.
20. Lehtinen, M. K., Z. Yuan, P. R. Boag, Y. Yang, J. Villén, E. B. Becker, S. DiBacco, N. de la Iglesia, S. Gygi, T. K. Blackwell, and A. Bonni. 2006. A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 125: 987-1001.
21. Yuan, Z., M. K. Lehtinen, P. Merlo, J. Villén, S. Gygi, and A. Bonni. 2009. Regulation of neuronal cell death by MST1-FOXO1 signaling. J. Biol. Chem. 284: 11285-11292.
22. Cinar, B., P. K. Fang, M. Lutchman, D. Di Vizio, R. M. Adam, N. Pavlova, M. A. Rubin, P. C. Yelick, and M. R. Freeman. 2007. The pro-apoptotic kinase Mst1 and its caspase cleavage products are direct inhibitors of Akt1. EMBO J. 26: 4523-4534.
23. Abdollahpour, H., G. Appaswamy, D. Kotlarz, J. Diestelhorst, R. Beier, A. A. Schäffer, E. M. Gertz, A. Schambach, H. H. Kreipe, D. Pfeifer, et al. 2012. The phenotype of human STK4 deficiency. Blood 119: 3450-3457.
24. Nehme, N. T., J. Pachlopnik Schmid, F. Debeurme, I. André-Schmutz, A. Lim, P. Nitschke, F. Rieux-Laucat, P. Lutz, C. Picard, N. Mahlaoui, et al. 2012. MST1 mutations in autosomal recessive primary immunodeficiency characterized by defective naive T-cell survival. Blood 119: 3458-3468.
25. Zhou, D., B. D. Medoff, L. Chen, L. Li, X. F. Zhang, M. Praskova, M. Liu, A. Landry, R. S. Blumberg, V. A. Boussiotis, et al. 2008. The Nore1B/Mst1 complex restrains antigen receptor-induced proliferation of naïve T cells. Proc. Natl. Acad. Sci. USA 105: 20321-20326.
26. Dong, Y., X. Du, J. Ye, M. Han, T. Xu, Y. Zhuang, and W. Tao. 2009. A cellintrinsic role for Mst1 in regulating thymocyte egress. J. Immunol. 183: 3865-3872.
27. Katagiri, K., T. Katakai, Y. Ebisuno, Y. Ueda, T. Okada, and T. Kinashi. 2009. Mst1 controls lymphocyte trafficking and interstitial motility within lymph nodes. EMBO J. 28: 1319-1331.
28. Mou, F., M. Praskova, F. Xia, D. Van Buren, H. Hock, J. Avruch, and D. Zhou. 2012. The Mst1 and Mst2 kinases control activation of rho family GTPases and thymic egress of mature thymocytes. J. Exp. Med. 209: 741-759.
29. Ueda, Y., K. Katagiri, T. Tomiyama, K. Yasuda, K. Habiro, T. Katakai, S. Ikehara, M. Matsumoto, and T. Kinashi. 2012. Mst1 regulates integrin-dependent thymocyte trafficking and antigen recognition in the thymus. Nat. Commun. 3: 1098.
30. Peng, C., J. Ye, S. Yan, S. Kong, Y. Shen, C. Li, Q. Li, Y. Zheng, K. Deng, T. Xu, and W. Tao. 2012. Ablation of vacuole protein sorting 18 (Vps18) gene leads to neurodegeneration and impaired neuronal migration by disrupting multiple vesicle transport pathways to lysosomes. J. Biol. Chem. 287: 32861-32873.
31. Li, H., M. Dai, and Y. Zhuang. 2004. A T cell intrinsic role of Id3 in a mouse model for primary Sjogren's syndrome. Immunity 21: 551-560.
32. Vanvalkenburgh, J., D. I. Albu, C. Bapanpally, S. Casanova, D. Califano, D. M. Jones, L. Ignatowicz, S. Kawamoto, S. Fagarasan, N. A. Jenkins, et al. 2011. Critical role of Bcl11b in suppressor function of T regulatory cells and prevention of inflammatory bowel disease. J. Exp. Med. 208: 2069-2081.
33. Venken, K., M. Thewissen, N. Hellings, V. Somers, K. Hensen, J. L. Rummens, and P. Stinissen. 2007. A CFSE based assay for measuring CD4+CD25+ regulatory T cell mediated suppression of auto-antigen specific and polyclonal T cell responses. J. Immunol. Methods 322: 1-11.
34. Yan, S., I. M. Berquin, B. R. Troen, and B. F. Sloane. 2000. Transcription of human cathepsin B is mediated by Sp1 and Ets family factors in glioma. DNA Cell Biol. 19: 79-91.
35. Bäckdahl, L., A. Bushell, and S. Beck. 2009. Inflammatory signalling as mediator of epigenetic modulation in tissue-specific chronic inflammation. Int. J. Biochem. Cell Biol. 41: 176-184.
36. Chen, W., W. Jin, N. Hardegen, K. J. Lei, L. Li, N. Marinos, G. McGrady, and S. M. Wahl. 2003. Conversion of peripheral CD4+CD252 naive T cells to CD4 +CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198: 1875-1886.
37. Ouyang, W., and M. O. Li. 2011. Foxo: in command of T lymphocyte homeostasis and tolerance. Trends Immunol. 32: 26-33.
38. Katagiri, K., M. Imamura, and T. Kinashi. 2006. Spatiotemporal regulation of the kinase Mst1 by binding protein RAPL is critical for lymphocyte polarity and adhesion. Nat. Immunol. 7: 919-928.
39. Deane, J. A., and D. A. Fruman. 2004. Phosphoinositide 3-kinase: diverse roles in immune cell activation. Annu. Rev. Immunol. 22: 563-598.
40. Wing, K., and S. Sakaguchi. 2010. Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat. Immunol. 11: 7-13.
41. Oh, S., D. Lee, T. Kim, T. S. Kim, H. J. Oh, C. Y. Hwang, Y. Y. Kong, K. S. Kwon, and D. S. Lim. 2009. Crucial role for Mst1 and Mst2 kinases in early embryonic development of the mouse. Mol. Cell. Biol. 29: 6309-6320.
42. Choi, J., S. Oh, D. Lee, H. J. Oh, J. Y. Park, S. B. Lee, and D. S. Lim. 2009. Mst1-FoxO signaling protects naïve T lymphocytes from cellular oxidative stress in mice. PLoS ONE 4: e8011.
43. Yuan, Z., D. Kim, S. Shu, J. Wu, J. Guo, L. Xiao, S. Kaneko, D. Coppola, and J. Q. Cheng. 2010. Phosphoinositide 3-kinase/Akt inhibits MST1-mediated proapoptotic signaling through phosphorylation of threonine 120. J. Biol. Chem. 285: 3815-3824.
44. Ouyang, W., W. Liao, C. T. Luo, N. Yin, M. Huse, M. V. Kim, M. Peng, P. Chan, Q. Ma, Y. Mo, et al. 2012. Novel Foxo1-dependent transcriptional programs control T(reg) cell function. Nature 491: 554-559.
45. Tomiyama, T., Y. Ueda, T. Katakai, N. Kondo, K. Okazaki, and T. Kinashi. 2013. Antigen-specific suppression and immunological synapse formation by regulatory T cells require the mst1 kinase. PLoS ONE 8: e73874.