Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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Twist2 Regulates CD7 Expression and Galectin-1-Induced Apoptosis in Mature T-Cells

  • Koh, Han Seok (Department of Life Science and Center for Efficacy Assessment and Development of Functional Foods and Drugs, Hallym University) ;
  • Lee, Changjin (Department of Biological Sciences, Research Center for Functional Cellulomics, Seoul National University) ;
  • Lee, Kwang Soo (Department of Life Science and Center for Efficacy Assessment and Development of Functional Foods and Drugs, Hallym University) ;
  • Park, Eun Jung (Immune and Cell Therapy Branch, National Cancer Center) ;
  • Seong, Rho H. (Department of Biological Sciences, Research Center for Functional Cellulomics, Seoul National University) ;
  • Hong, Seokmann (Department of Bioscience and Biotechnology, Institute of Bioscience, Sejong University) ;
  • Jeon, Sung Ho (Department of Life Science and Center for Efficacy Assessment and Development of Functional Foods and Drugs, Hallym University)
  • Received : 2009.08.05
  • Accepted : 2009.09.17
  • Published : 2009.12.31
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Abstract

In the periphery, a galectin-1 receptor, CD7, plays crucial roles in galectin-1-mediated apoptosis of activated T-cells as well as progression of T-lymphoma. Previously, we demonstrated that $NF-{\kappa}B$ downregulated CD7 gene expression through the p38 MAPK pathway in developing immature thymocytes. However, its regulatory pathway is not well understood in functional mature T-cells. Here, we show that CD7 expression was downregulated by Twist2 in Jurkat cells, a human acute T-cell lymphoma cell line, and in EL4 cells, a mature murine T-cell lymphoma cell line. Furthermore, ectopic expression of Twist2 in Jurkat cells reduced galectin-1-induced apoptosis. While full-length Twist2 decreased CD7 promoter activity, a C-terminal deletion form of Twist2 reversed its inhibition, suggesting an important role of the C-terminus in CD7 regulation. In addition, CD7 expression was enhanced by histone deacetylase inhibitors such as trichostatin A and sodium butyrate, which indicates that Twist2 might be one of candidate factors involved in histone deacetylation. Based on these results, we conclude that upregulation of Twist2 increases the resistance to galectin-1-mediated-apoptosis, which may have significant implications for the progression of some T-cells into tumors such as Sezary cells.

Keywords

Acknowledgement

Supported by : Korea Research Foundation

References

  1. Bannister, A.J., and Kouzarides, T. (1996). The CBP co-activator is a histone acetyltransferase. Nature 384, 641-643 https://doi.org/10.1038/384641a0
  2. Bialek, P., Kern, B., Yang, X., Schrock, M., Sosic, D., Hong, N., Wu, H., Yu, K., Ornitz, D.M., Olson, E.N., et al. (2004). A twist code determines the onset of osteoblast differentiation. Dev. Cell 6, 423-435 https://doi.org/10.1016/S1534-5807(04)00058-9
  3. Castanon, I., von Stetina, S., Kass, J., and Baylies, M.K. (2001). Dimerization partners determine the activity of the Twist bHLH protein during Drosophila mesoderm development. Development 128, 3142-3159
  4. Dupont, J., Fernandez, A.M., Glackin, C.A., Helman, L., and Le- Roith, D. (2001). Insulin-like growth factor 1 (IGF-1)-induced twist expression is involved in the anti-apoptotic effects of the IGF-1 receptor. J. Biol. Chem. 276, 26699-26707 https://doi.org/10.1074/jbc.M102664200
  5. Fukumori, T., Takenaka, Y., Yoshii, T., Kim, H.R., Hogan, V., Inohara, H., Kagawa, S., and Raz, A. (2003). CD29 and CD7 mediate galecin-3-induced type II T-cell apoptosis. Cancer Res. 63, 8302-8311
  6. Gong, X.Q., and Li, L. (2002). Dermo-1, a multifunctional basic helix-loop-helix protein, represses MyoD transactivation via the HLH domain, MEF2 interaction, and chromatin deacetylation. J. Biol. Chem. 277, 12310-12317 https://doi.org/10.1074/jbc.M110228200
  7. Hamamori, Y., Sartorelli, V., Ogryzko, V., Puri, P.L., Wu, H.Y., Wang, J.Y., Nakatani, Y., and Kedes, L. (1999). Regulation of histone acetyltransferases p300 and PCAF by the bHLH protein twist and adenoviral oncoprotein E1A. Cell 96, 405-413 https://doi.org/10.1016/S0092-8674(00)80553-X
  8. Hebrok, M., Wertz, K., and Füchtbauer, E.M., (1994). M-twist is an inhibitor of muscle differentiation. Dev. Biol. 165, 537-544 https://doi.org/10.1006/dbio.1994.1273
  9. Khoshnan, A., Tindell, C., Laux, I., Bae, D., Bennett, B., and Nel, A.E. (2000). The NF-kappa B cascade is important in Bcl-xL expression and for the anti-apoptotic effects of the CD28 receptor in primary human CD4+ lymphocytes, J. Immunol. 165, 1743- 1754 https://doi.org/10.4049/jimmunol.165.4.1743
  10. Koh, H.S., Lee, C., Lee, K.S., Ham, C.S., Seong, R.H., Kim, S.S., and Jeon, S.H. (2008). CD7 expression and galectin-1-induced apoptosis of immature thymocytes are directly regulated by NFkappaB upon T-cell activation. Biochem. Biophys. Res. Commun. 370, 149-153 https://doi.org/10.1016/j.bbrc.2008.03.049
  11. Kwon, S.H., and Workman, J.L. (2008). The heterochromatin protein 1 (HP1) family: put away a bias toward HP1. Mol. Cells 26, 217-227
  12. Lee, D.M., Staats, H.F., Sundy, J.S., Patel, D.D., Sempowski, G.D., Scearce, R.M., Jones, D.M., and Haynes, B.F. (1998). Immunologic characterization of CD7-deficient mice. J. Immunol. 160, 5949-5757
  13. Lee, Y.S., Lee, H.H., Park, J., Yoo, E.J., Glackin, C.A., Choi, Y.I., Jeon, S.H., Seong, R.H., Park, S.D., and Kim, J.B. (2003). Twist2, a novel ADD1/SREBP1c interacting protein, represses the transcriptional activity of ADD1/SREBP1c. Nucleic Acids Res. 31, 7165-7174 https://doi.org/10.1093/nar/gkg934
  14. Liu, T.Y., Chen, C.Y., Tien, H.F., and Lin, C.W. (2009). Loss of CD7, independent of galectin-3 expression, implies a worse prognosis in adult T-cell leukaemia/lymphoma. Histopathology 54, 214-220 https://doi.org/10.1111/j.1365-2559.2008.03199.x
  15. Lo, H.W., Hsu, S.C., Xia, W., Cao, X., Shih, J.Y., Wei, Y., Abbruzzese, J.L., Hortobagyi, G.N., and Hung, M.C. (2007). Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression. Cancer Res. 67, 9066-9076 https://doi.org/10.1158/0008-5472.CAN-07-0575
  16. Murakami, M., Ohkuma, M., and Nakamura. M. (2008). Molecular mechanism of transforming growth factor-beta-mediated inhibition of growth arrest and differentiation in a myoblast cell line. Dev. Growth Differ. 50, 121-130 https://doi.org/10.1111/j.1440-169X.2007.00982.x
  17. Murray, S.S., Glackin, C.A., Winters, K.A., Gazit, D., Kahn, A.J., and Murray, E.J. (1992). Expression of helix-loop-helix regulatory genes during differentiation of mouse osteoblastic cells. J. Bone Miner. Res. 7, 1131-1138 https://doi.org/10.1002/jbmr.5650071004
  18. O''Rourke, M.P., and Tam, P.P. (2002). Twist functions in mouse development. Int. J. Dev. Biol. 46, 401-413
  19. Pace, K.E., Hahn, H.P., Pang, M., Nguyen, J.T., and Baum, L.G. (2000). CD7 delivers a pro-apoptotic signal during galectin-1- induced T cell death. J. Immunol. 165, 2331-2334 https://doi.org/10.4049/jimmunol.165.5.2331
  20. Qiu, P., Ritchie, R.P., Gong, X.Q., Hamamori, Y., and Li, L. (2006). Dynamic changes in chromatin acetylation and the expression of histone acetyltransferases and histone deacetylases regulate the SM22alpha transcription in response to Smad3-mediated TGFbeta1 signaling. Biochem. Biophys. Res. Commun. 348, 351-358 https://doi.org/10.1016/j.bbrc.2006.07.009
  21. Rappl, G., Abken, H., Muche, J.M., Sterry, W., Tilgen, W., André, S., Kaltner, H., Ugurel, S., Gabius, H.J., and Reinhold, U. (2002). CD4+CD7- leukemic T cells from patients with Sézary syndrome are protected from galectin-1-triggered T cell death. Leukemia 16, 840-845 https://doi.org/10.1038/sj.leu.2402438
  22. Sharabi, A.B., Aldrich, M., Sosic, D., Olson, E.N., Friedman, A.D., Lee, S.H., and Chen, S.Y. (2008). Twist2 controls myeloid lineage development and function. PLos Biol. 6, 2786-2800
  23. Sosic, D., Richardson, J.A., Yu, K., Ornitz, D.M., and Olson, E.N. (2003). Twist regulates cytokine gene expression through a negative feedback loop that represses NF-kappaB activity. Cell 112, 169-180 https://doi.org/10.1016/S0092-8674(03)00002-3
  24. Spicer, D.B., Rhee, J., Cheung, W.L., and Lassar, A.B. (1996). Inhibition of myogenic bHLH and MEF2 transcription factors by the bHLH protein Twist. Science 272, 1476-1480 https://doi.org/10.1126/science.272.5267.1476
  25. Stillman, B.N., Hsu, D.K., Pang, M., Brewer, C.F., Johnson, P., Liu, F.T., and Baum, L.G. (2006). Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death. J. Immunol. 176, 778-789 https://doi.org/10.4049/jimmunol.176.2.778
  26. Vacchio, M.S., and Ashwell, J.D. (1997). Thymus-derived glucocorticoids regulate antigen-specific positive selection. J. Exp. Med. 185, 2033-2038 https://doi.org/10.1084/jem.185.11.2033
  27. van Doorn, R., Dijkman, R., Vermeer, M.H., Out-Luiting, J.J., van der Raaij-Helmer, E.M., Willemze, R., and Tensen, C.P. (2004). Aberrant expression of the tyrosine kinase receptor EphA4 and the transcription factor twist in Sézary syndrome identified by gene expression analysis. Cancer Res. 64, 5578-86 https://doi.org/10.1158/0008-5472.CAN-04-1253
  28. Yang, J., Mani, S.A., Donaher, J.L., Ramaswamy, S., Itzykson, R.A., Come, C., Savagner, P., Gitelman, I., Richardson, A., and Weinberg, R.A. (2004). Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927-939 https://doi.org/10.1016/j.cell.2004.06.006
  29. Yoshikawa, K., Seto, M., Ueda, R., Obata, Y., Fukatsu, H., Segawa, A., and Takahashi, T. (1993). Isolation and characterization of mouse CD7 cDNA. Immunogenetics 37, 114-119

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