DOI QR코드

DOI QR Code

Protective Role of Tissue Transglutaminase in the Cell Death Induced by TNF-α in SH-SY5Y Neuroblastoma Cells

  • Kweon, Soo-Mi (Vascular System Research Center and Department of Molecular & Cellular Biochemistry, Kangwon National University School of Medicine) ;
  • Lee, Zee-Won (Cell Biology Team, Korea Basic Science Institute) ;
  • Yi, Sun-Ju (Vascular System Research Center and Department of Molecular & Cellular Biochemistry, Kangwon National University School of Medicine) ;
  • Kim, Young-Myeong (Vascular System Research Center and Department of Molecular & Cellular Biochemistry, Kangwon National University School of Medicine) ;
  • Han, Jeong-A (Vascular System Research Center and Department of Molecular & Cellular Biochemistry, Kangwon National University School of Medicine) ;
  • Paik, Sang-Gi (Department of Biology, Chungnam National University) ;
  • Ha, Kwon-Soo (Vascular System Research Center and Department of Molecular & Cellular Biochemistry, Kangwon National University School of Medicine)
  • Published : 2004.03.31

Abstract

Tissue transglutaminase (tTGase) regulates various biological processes, including extracellular matrix organization, cellular differentiation, and apoptosis. Here we report the protective role of tTGase in the cell death that is induced by the tumor necrosis factor $\alpha$ (TNF-$\alpha$) and ceramide, a product of the TNF-$\alpha$ signaling pathway, in human neuroblastoma SH-SY5Y cells. Treatment with retinoic acid (RA) induced the differentiation of the neuroblastoma cells with the formation of extended neurites. Immunostaining and Western blot analysis showed the tTGase expression by RA treatment. TNF-$\alpha$ or $C_2$ ceramide, a cell permeable ceramide analog, induced cell death in normal cells, but cell death was largely inhibited by the RA treatment. The inhibition of tTGase by the tTGase inhibitors, monodansylcadaverine and cystamine, eliminated the protective role of RA-treatment in the cell death that is caused by TNF-$\alpha$ or $C_2$-ceramide. In addition, the co-treatment of TNF-$\alpha$ and cycloheximide ecreased the protein level of tTGase and cell viability in the RA-treated cells, supporting the role of tTGase in the protection of cell death. DNA fragmentation was also induced by the co-treatment of TNF-$\alpha$ and cycloheximide. These results suggest that tTGase expressed by RA treatment plays an important role in the protection of cell death caused by TNF-$\alpha$ and ceramide.

Keywords

References

  1. Akimov, S. S., Krylov, D., Flrischman, L. F. and Belkin, A. M. (2000) Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin. J. Cell. Biol. 148, 825-838. https://doi.org/10.1083/jcb.148.4.825
  2. Antonyak, M. A., Boehm, J. E. and Cerione, R. A. (2002) Phosphoinositide 3-Kinase activity is required for retinoic acidinduced expression and activation of the tissue transglutaminase. J. Biol. Chem. 277, 14712-14716. https://doi.org/10.1074/jbc.M112259200
  3. Antonyak, M. A., Singh, U., Lee, D. A., Boehm, J. E., Combs, C., Zgola, M. M., Page, R. L. and Cerione, R. A. (2001) Effects of tissue transglutaminase on retinoic acid-induced cellular differentiation and protection against apoptosis. J. Biol. Chem. 276, 33582-33587. https://doi.org/10.1074/jbc.M105318200
  4. Ashkenazi, A. and Dixit, V. M. (1998) Death receptors: signaling and modulation. Science 281, 1305-1308. https://doi.org/10.1126/science.281.5381.1305
  5. Boehm, J. E., Singh, U., Combs, C., Antonyak, M. A. and Cerione, R. A. (2002) Tissue transglutaminase protects against apoptosis by modifying the tumor suppressor protein p110 Rb. J. Biol. Chem. 277, 20127-20130. https://doi.org/10.1074/jbc.C200147200
  6. Chen, G. and Goeddel, D. V. (2002) TNF-R1 signaling: a beautiful pathway. Science 296, 1634-1635. https://doi.org/10.1126/science.1071924
  7. Chen, J. S. K. and Mehta, K. (1999) Tissue transglutaminase: an enzyme with a split personality. Intl. J. Biochem. Cell. Biol. 31, 817-836. https://doi.org/10.1016/S1357-2725(99)00045-X
  8. Chun, W., Lesort, M., Tucholski, J., Ross, C. A. and Johnson, G. V. W. (2001) Tissue transglutaminase does not contribute to the formation of mutant Huntington aggregates. J. Cell. Biol. 153, 25-34. https://doi.org/10.1083/jcb.153.1.25
  9. Cuvillier, O., Pirianov, G., Kleuser, B., Vanek, P. G., Coso, O. A., Gutkind, S. and Spiegel, S. (1996) Suppression of ceramidemediated programmed cell death by sphingosine-1-phosphate. Nature 381, 800-803. https://doi.org/10.1038/381800a0
  10. Declercq, W., Denecker, G., Fiers, W. and Vandenabeele, P. (1998) Cooperation of both TNF receptors in inducing apoptosis: involvement of the TNF receptor-associated factor binding domain of the TNF receptor 75. J. Immunol. 161, 390-399.
  11. Greenberg, C. S., Birckbichler, P. J. and Rice, R. H. (1991) Transglutaminase: multifunctional cross-linking enzymes that stabilize tissues. FASEB J. 5, 3071-3077.
  12. Iismaa, S. E., Wu, M. J., Nanda, N., Church, W. B. and Graham, R. M. (2000) GTP binding and signaling by Gh/transglutaminase II involves distinct residues in a unique GTPbinding pocket. J. Biol. Chem. 275, 18259-18266. https://doi.org/10.1074/jbc.M000583200
  13. Im, M. J. (2001) Regulation of a novel guanine nucleotide binding protein tissue transglutaminase (G$\alpha_h$). J. Biochem. Mol. Biol. 34, 95-101.
  14. Kim, S. -W., Lee, Z. -W., Lee, C., Im, K. -S. and Ha, K. -S. (2001) The role of tissue transglutaminase in the germinal vesicle breakdown of mouse oocytes. Biochem. Biophys. Res. Commun. 286, 229-234. https://doi.org/10.1006/bbrc.2001.5381
  15. Kimura, K., Bowen, C., Spiegel, S. and Gelmann, E. P. (1999) Tumor necrosis factor-alpha sensitizes prostate cancer cells to gamma-irradiation-induced apoptosis. Cancer Res. 59, 1606-1614.
  16. Lee, J. C. and Lim, K. T. (2001) Inhibitory effects of the ethanol extract of Ulmus davidiana on apoptosis induced by glucoseglucose oxidase and cytokine production in cultured mouse primary immune cells. J. Biochem. Mol. Biol. 34, 463-471.
  17. Lesort, M., Attanavanich, K., Zhang, J. and Johnson, G. V. (1998) Distinct nuclear localization and activity of tissue transglutaminase. J. Biol. Chem. 273, 11991-11994. https://doi.org/10.1074/jbc.273.20.11991
  18. Melino, G. and Piacentini, M. (1998) Tissue transglutaminase in cell death: a downstream or a multifunctional upstream effector? FEBS Lett. 430, 59-63. https://doi.org/10.1016/S0014-5793(98)00521-3
  19. Nanda, N., Iismaa, S., Owens, A., Husain, A., Mackay, F. and Graham, R. (2001) Targeted inactivation of Gh/tissue transglutaminase II. J. Biol. Chem. 276, 20673-20678. https://doi.org/10.1074/jbc.M010846200
  20. Oliverio, S., Amendola, A., Rodolfo, C., Spinedi, A. and Piacentini, M. (1999) Inhibition of tissue transglutaminase increases cell survival by preventing apoptosis. J. Biol. Chem. 274, 34123-34128. https://doi.org/10.1074/jbc.274.48.34123
  21. Ou, H., Haendeler, J., Aebly, M. R., Kelly, L. A., Cholewa, B. C., Koike, G., Kwitek-Black, A., Jacob, H. J., Berk, B. C. and Miano, J. M. (2000) Retinoic acidinduced tissue transglutaminase and apoptosis in vascular smooth muscle cells. Circ. Res. 87, 881-887. https://doi.org/10.1161/01.RES.87.10.881
  22. Piredda, L., Farrace, M. G., Bello, M. L., Malorni, W., Melino, G., Petruzzelli, R. and Piacentini, M. (1999) Identification of tissue transglutaminase binding proteins in neural cells committed to apoptosis. FASEB J. 13, 355-364.
  23. Setkov, N. A., Kazakov, V. N., Rosenwald, I. B., Makarova, G. F. and Epifanova, O. I. (1992) Protein synthesis inhibitors, like growth factors, may render resting 3T3 cells competent for DNA synthesis: a radioautographic and cell fusion study. Cell Prolif. 25, 181-191. https://doi.org/10.1111/j.1365-2184.1992.tb01393.x
  24. Singh, U., Li, Q. and Cerione, R. A. (1998) Identification of the eukaryotic initiation factor 5A as a retinoic acid-stimulated cellular binding partner for tissue transglutaminase II. J. Biol. Chem. 273, 1946-1950. https://doi.org/10.1074/jbc.273.4.1946
  25. Suzuki, N., Suzuki, T., Uchida, A., Thompson, E. A. and Hosoya, T. (1992) Effect of dexamethasone on nucleolar casein kinase II activity and phosphorylation of nucleolin in lymphosarcoma P1798 cells. J. Steroid. Biochem. Mol. Biol. 42, 305-312. https://doi.org/10.1016/0960-0760(92)90133-4
  26. Tang, D., Lahti, J. M., Grenet, J. and Kidd, V. J. (1999) Cycloheximide-induced T-cell death is mediated by a Fasassociated death domain-dependent mechanism. J. Biol. Chem. 274, 7245-7252. https://doi.org/10.1074/jbc.274.11.7245
  27. Tucholski, J., Lesort, M. and Johnson, G. V. (2001) Tissue transglutaminase is essential for neurite outgrowth in human neuroblastoma SH-SY5Y cells. Neuroscience 102, 2481-2491.
  28. Woo, C. H., Eom, Y. W., Yoo, M. H., You, H. J., Han, H. J., Song, W. K., Yoo, Y. J., Chun, J. S. and Kim, J. H. (2000) Tumor necrosis factor- generates reactive oxygen species via a cytosolic phospholipase A2-linked cascade. J. Biol. Chem. 275, 32357-32362. https://doi.org/10.1074/jbc.M005638200
  29. Xu, J., Yeh, C. H., Chen, S., He, L., Sensi, S. L., Canzoniero, L. M. T., Choi, D. W. and Hsu, C. Y. (1998) Involvement of de Novo ceramide biosynthesis in tumor necrosis factor-$\alpha$/ cycloheximide-induced cerebral endothelial cell death. J. Biol. Chem. 273, 16521-16526. https://doi.org/10.1074/jbc.273.26.16521
  30. Yoshimura, S. I., Banno, Y., Nakashima, S., Takenaka, K., Sakai, H., Nishimura, Y., Sakai, N., Shimizu, S., Eguchi, Y., Tsujimoto, Y. and Nozawa, Y. (1998) Ceramide formation leads to caspase-3 activation during hypoxic PC12 cell death. J. Biol. Chem. 273, 6921-6927.
  31. Zhou, H., Summers, S., Birnbaum, M. and Pittman, R. (1998) Inhibition of Akt kinase by cell-permeable ceramide and its implications for ceramide-induced apoptosis. J. Biol. Chem. 273, 16568-16575 https://doi.org/10.1074/jbc.273.26.16568

Cited by

  1. Scorpion venom (Odontobuthus doriae) induces apoptosis by depolarization of mitochondria and reduces S-phase population in human breast cancer cells (MCF-7) vol.25, pp.8, 2011, https://doi.org/10.1016/j.tiv.2011.09.002
  2. Polyamines and apoptosis vol.9, pp.3, 2005, https://doi.org/10.1111/j.1582-4934.2005.tb00493.x
  3. Transglutaminase 2 inhibits apoptosis induced by calciumoverload through down-regulation of Bax vol.42, pp.9, 2010, https://doi.org/10.3858/emm.2010.42.9.063
  4. Scorpion (Odontobuthus doriae) venom induces apoptosis and inhibits DNA synthesis in human neuroblastoma cells vol.348, pp.1-2, 2011, https://doi.org/10.1007/s11010-010-0652-x
  5. Scorpion (Androctonus crassicauda) venom limits growth of transformed cells (SH-SY5Y and MCF-7) by cytotoxicity and cell cycle arrest vol.91, pp.1, 2011, https://doi.org/10.1016/j.yexmp.2011.04.008
  6. The 55 kDa tissue transglutaminase cross-linking active isoform TG induces cell death vol.54, pp.9, 2015, https://doi.org/10.1002/mc.22134
  7. Transglutaminase-2 Is Involved in All-Trans Retinoic Acid-Induced Invasion and Matrix Metalloproteinases Expression of SH-SY5Y Neuroblastoma Cells via NF-κB Pathway vol.20, pp.3, 2012, https://doi.org/10.4062/biomolther.2012.20.3.286
  8. Transglutaminase 2 has opposing roles in the regulation of cellular functions as well as cell growth and death vol.7, pp.6, 2016, https://doi.org/10.1038/cddis.2016.150
  9. Transglutaminase 2 expression levels regulate sensitivity to cystamine plus TRAIL-mediated apoptosis vol.287, pp.2, 2010, https://doi.org/10.1016/j.canlet.2009.06.013
  10. Biochemical and Physiological Evaluations of Limonoids as Potential Cancer Destroyers vol.9, pp.7, 2010, https://doi.org/10.3923/javaa.2010.1099.1107
  11. Doxorubicin induces the persistent activation of intracellular transglutaminase 2 that protects from cell death vol.33, pp.3, 2012, https://doi.org/10.1007/s10059-012-2201-9