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Identification of p54nrb and the 14-3-3 Protein HS1 as TNF-α-Inducible Genes Related to Cell Cycle Control and Apoptosis in Human Arterial Endothelial Cells

  • Published : 2005.07.31

Abstract

TNF-$\alpha$ plays a pivotal role in inflammation processes which are mainly regulated by endothelial cells. While TNF-$\alpha$ induces apoptosis of several cell types like tumor cells, endothelial cells are resistant to TNFa mediated cell death. The cytotoxic effects of TNF-$\alpha$ on most cells are only evident if RNA or protein synthesis is inhibited, suggesting that de novo RNA or protein synthesis protect cells from TNF-$\alpha$ cytotoxicity, presumably by NF-${\kappa}B$ mediated induction of protective genes. However, the cytoprotective genes involved in NF-${\kappa}B$ dependent endothelial cell survival have not been sufficiently identified. In the present study, the suppression subtractive hybridization (SSH) method was employed to identify rarely transcribed TNF-$\alpha$ inducible genes in human arterial endothelial cells related to cell survival and cell cycle. The TNF-$\alpha$-induced expression of the RNA binding protein $p54^{nrb}$ and the 14-3-3 protein HS1 as shown here for the first time may contribute to the TNF-$\alpha$ mediated cell protection of endothelial cells. These genes have been shown to play pivotal roles in cell survival and cell cycle control in different experimental settings. The concerted expression of these genes together with other genes related to cell protection and cell cycle like DnaJ, $p21^{cip1}$ and the ubiquitin activating enzyme E1 demonstrates the identification of new genes in the context of TNF-$\alpha$ induced gene expression patterns mediating the prosurvival effect of TNF-$\alpha$ in endothelial cells.

Keywords

References

  1. Aggarwal, B. B. (2000) Tumour necrosis factors receptor associated signalling molecules and their role in activation of apoptosis, JNK and NF-kappaB. Ann. Rheum. Dis. 59, 6-16 https://doi.org/10.1136/ard.59.suppl_1.i6
  2. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic. Acids Res. 25, 3389-3402 https://doi.org/10.1093/nar/25.17.3389
  3. Baeuerle, P. A. and Henkel, T. (1994) Function and activation of NF-kappa B in the immune system. Annu. Rev. Immunol. 12, 141-179 https://doi.org/10.1146/annurev.iy.12.040194.001041
  4. Baeuerle, P. A. and Baichwal, V. R. (1997) NF-kappa B as a frequent target for immunosuppressive and anti-inflammatory molecules. Adv. Immunol. 65, 111-137 https://doi.org/10.1016/S0065-2776(08)60742-7
  5. Barnes, P. J. and Karin M. (1997) Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N. Engl. J. Med. 336, 1066-1071 https://doi.org/10.1056/NEJM199704103361506
  6. Basu, A., Dong, B., Krainer, A. R. and Howe, C. C. (1997) The intracisternal A-particle proximal enhancer-binding protein activates transcription and is identical to the RNA- and DNAbinding protein p54nrb/NonO. Mol. Cell. Biol. 17, 677-686
  7. Beg, A. A. and Baltimore, D. (1996) An essential role for NFkappaB in preventing TNF-alpha-induced cell death. Science 274, 782-784 https://doi.org/10.1126/science.274.5288.782
  8. Champlin, D. T. and Lis, J. T. (1994) Distribution of B52 within a chromosomal locus depends on the level of transcription. Mol. Biol. Cell 5, 71-79 https://doi.org/10.1091/mbc.5.1.71
  9. Chu, Z. L., McKinsey, T. A., Liu, L., Gentry, J. J., Malim, M. H. and Ballard, D. W. (1997) Suppression of tumor necrosis factor-induced cell death by inhibitor of apoptosis c-IAP2 is under NF-kappaB control. Proc. Natl. Acad. Sci. USA 94, 10057-10062 https://doi.org/10.1073/pnas.94.19.10057
  10. Diatchenko, L., Lau, Y. F., Campbell, A. P., Chenchik, A., Moqadam, F., Huang, B., Lukyanov, S., Lukyanov, K., Gurskaya, N., Sverdlov, E. D. and Siebert, P. D. (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc. Natl. Acad. Sci. USA 93, 6025-6030 https://doi.org/10.1073/pnas.93.12.6025
  11. Dong, B., Horowitz, D. S., Kobayashi, R. and Krainer, A. R. (1993) Purification and cDNA cloning of HeLa cell p54nrb, a nuclear protein with two RNA recognition motifs and extensive homology to human splicing factor PSF and Drosophila NONA/BJ6. Nucleic Acids Res. 21, 4085-4092 https://doi.org/10.1093/nar/21.17.4085
  12. Dormond, O., Lejeune, F. J. and Ruegg, C. (2002) Modulation of cdk2, cyclin D1, p16INK4a, p21WAF and p27Kip1 expression in endothelial cells by TNF/IFN gamma. Anticancer Res. 22, 3159-3163
  13. Frater-Schroder, M., Risau, W., Hallmann, R., Gautschi, P. and Bohlen, P. (1987) Tumor necrosis factor type alpha, a potent inhibitor of endothelial cell growth in vitro, is angiogenic in vivo. Proc. Natl. Acad. Sci. USA 84, 5277-5281 https://doi.org/10.1073/pnas.84.15.5277
  14. Heller, R. A. and Kronke, M. (1994) Tumor necrosis factor receptor-mediated signaling pathways. J. Cell. Biol. 126, 5-9 https://doi.org/10.1083/jcb.126.1.5
  15. Hermeking, H., Lengauer, C., Polyak, K., He, T. C., Zhang, L., Thiagalingam, S., Kinzler, K. W. and Vogelstein, B. (1997) 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol. Cell 1, 3-11 https://doi.org/10.1016/S1097-2765(00)80002-7
  16. Honda, R., Ohba, Y. and Yasuda, H. (1997) 14-3-3 zeta protein binds to the carboxyl half of mouse weel kinase. Biochem. Biophys. Res. Commun. 230, 262-265 https://doi.org/10.1006/bbrc.1996.5933
  17. Karsan, A., Yee, E. and Harlan, J. M. (1996) Endothelial cell death induced by tumor necrosis factor-alpha is inhibited by the Bcl-2 family member, Al. J. Biol. Chem. 271, 27201-27204. https://doi.org/10.1074/jbc.271.44.27201
  18. Kishore, R., Luedemann, C., Bord, E., Goukassian, D. and Losordo, D. W. (2003) Tumor necrosis factor-mediated E2F1 suppression in endothelial cells: differential requirement of c-Jun N-terminal kinase and p38 mitogen-activated protein kinase signal transduction pathways. Circ. Res. 93, 932-940 https://doi.org/10.1161/01.RES.0000102400.22370.20
  19. Ko, Y., Totzke, G., Schiermeyer, B., Zeitler, H., Schmitz, U., Vetter, H. and Sachinidis, A. (1995) Reverse transcriptasepolymerase chain reaction (RT-PCR): a sensitive method to examine basic fibroblast growth factor-induced expression of the early growth response gene-1 (egr-1) in human umbilical arterial endothelial cells. Mol. Cell. Probes 9, 215-222 https://doi.org/10.1016/S0890-8508(95)90070-5
  20. Lademann, U., Kallunki, T. and Jaattela, M. (2001) A20 zinc finger protein inhibits TNF-induced apoptosis and stress response early in the signaling cascades and independently of binding to TRAF2 or 14-3-3 proteins. Cell Death Differ. 8, 265-272 https://doi.org/10.1038/sj.cdd.4400805
  21. Laronga, C., Yang, H. Y., Neal, C. and Lee, M. H. (2000) Association of the cyclin-dependent kinases and 14-3-3 sigma negatively regulates cell cycle progression. J. Biol. Chem. 275, 23106-23112 https://doi.org/10.1074/jbc.M905616199
  22. Liu, Y., Yin, G., Surapisitchat, J., Berk, B. C. and Min, W. (2001) Laminar flow inhibits TNF-induced ASKl activation by preventing dissociation of ASKl from its inhibitor 14-3-3. J. Clin. Invest. 107, 917-923 https://doi.org/10.1172/JCI11947
  23. Liu, Z. G., Hsu, H., Goeddel, D. V. and Karin, M. (1996) Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell 87, 565-576 https://doi.org/10.1016/S0092-8674(00)81375-6
  24. Lopez-Marure, R., Ventura, J. L., Sanchez, L., Montano, L. F. and Zentella, A. (2000) Ceramide mimics tumour necrosis factoralpha in the induction of cell cycle arrest in endothelial cells. Induction of the tumour suppressor p53 with decrease in retinoblastoma/protein levels. Eur. J. Biochem. 267, 4325-4333 https://doi.org/10.1046/j.1432-1327.2000.01436.x
  25. Pober, J. S. and Cotran, R. S. (1990) Cytokines and endothelial cell biology. Physiol. Rev. 70, 427-451
  26. Pohlman, T. H. and Harlan, J. M. (1989) Human endothelial cell response to lipopolysaccharide, interleukin-1, and tumor necrosis factor is regulated by protein synthesis. Cell Immunol. 119, 41-52 https://doi.org/10.1016/0008-8749(89)90222-0
  27. Secchiero, P., Gonelli, A., Carnevale, E., Milani, D., Pandolfi, A., Zella, D. and Zauli, G. (2003) TRAIL promotes the survival and proliferation of primary human vascular endothelial cells by activating the Akt and ERK pathways. Circulation 107, 2250-2256 https://doi.org/10.1161/01.CIR.0000062702.60708.C4
  28. Shav-Tal, Y. and Zipori, D. (2002) PSF and p54(nrb)/NonO--multi-functional nuclear proteins. FEBS Lett. 531, 109-114 https://doi.org/10.1016/S0014-5793(02)03447-6
  29. Stier, S., Totzke, G., Grunewald, E., Neuhaus, T., Fronhoffs, S., Sachinidis, A., Vetter, H., Schulze-Osthoff, K. and Ko, Y. (2000) Identification of syntenin and other TNF-inducible genes in human umbilical arterial endothelial cells by suppression subtractive hybridization. FEBS Lett. 467, 299-304 https://doi.org/10.1016/S0014-5793(00)01177-7
  30. Subramanian, R. R., Masters, S. C., Zhang, H. and Fu, H. (2001) Functional conservation of 14-3-3 isoforms in inhibiting badinduced apoptosis. Exp. Cell. Res. 271, 142-151 https://doi.org/10.1006/excr.2001.5376
  31. Van Antwerp, D. J., Martin, S. J., Kafri, T., Green, D. R. and Verma, I. M. (1996) Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 274, 787-789 https://doi.org/10.1126/science.274.5288.787
  32. van Hemert, M. J., Steensma, H. Y. and van Heusden, G. P. (2001) 14-3-3 proteins: key regulators of cell division, signalling and apoptosis. Bioessays 23, 936-946 https://doi.org/10.1002/bies.1134
  33. Vincenz, C. and Dixit, V. M. (1996) 14-3-3 proteins associate with A20 in an isoform-specific manner and function both as chaperone and adapter molecules. J. Biol. Chem. 271, 20029-20034 https://doi.org/10.1074/jbc.271.33.20029
  34. Wang, Y., Jacobs, C., Hook, K. E., Duan, H., Booher, R. N. and Sun, Y. (2000) Binding of 14-3-3beta to the carboxyl terminus of Wee1 increases Wee1 stability, kinase activity, and G2-M cell population. Cell Growth Differ. 11, 211-219
  35. Waterman, M. J., Stavridi, E. S., Waterman, J. L. and Halazonetis, T. D. (1998) ATM-dependent activation of p53 involves dephosphorylation and association with 14-3-3 proteins. Nat. Genet. 19, 175-178 https://doi.org/10.1038/542
  36. Wong, G. H., Elwell, J. H., Oberley, L. W. and Goeddel, D. V. (1989) Manganous superoxide dismutase is essential for cellular resistance to cytotoxicity of tumor necrosis factor. Cell 58, 923-931 https://doi.org/10.1016/0092-8674(89)90944-6
  37. Xing, H., Zhang, S., Weinheimer, C., Kovacs, A. and Muslin, A. J. (2000) 14-3-3 proteins block apoptosis and differentially regulate MAPK cascades. Embo J. 19, 349-358 https://doi.org/10.1093/emboj/19.3.349
  38. Xing, Y., Johnson, C. V., Dobner, P. R. and Lawrence, J. B. (1993) Higher level organization of individual gene transcription and RNA splicing. Science 259, 1326-1330 https://doi.org/10.1126/science.8446901
  39. Yang, Y. S., Hanke, J. H., Carayannopoulos, L., Craft, C. M., Capra, J. D. and Tucker, P. W. (1993) NonO, a non-POUdomain-containing, octamer-binding protein, is the mammalian homolog of Drosophila nonAdiss. Mol. Cell. Biol. 13, 5593-5603
  40. Yilmaz, A., Bieler, G., Spertini, O., Lejeune, F. J. and Ruegg, C. (1998) Pulse treatment of human vascular endothelial cells with high doses of tumor necrosis factor and interferon-gamma results in simultaneous synergistic and reversible effects on proliferation and morphology. Int. J. Cancer 77, 592-599 https://doi.org/10.1002/(SICI)1097-0215(19980812)77:4<592::AID-IJC20>3.0.CO;2-7
  41. Zha, J., Harada, H., Yang, E., Jockel, J. and Korsmeyer, S. J. (1996) Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 87, 619-628 https://doi.org/10.1016/S0092-8674(00)81382-3
  42. Zhang, L., Chen, J. and Fu, H. (1999) Suppression of apoptosis signal-regulating kinase 1-induced cell death by 14-3-3 proteins. Proc. Natl. Acad. Sci. USA 96, 8511-8515 https://doi.org/10.1073/pnas.96.15.8511
  43. Zhang, Z. and Carmichael, G. G. (2001) The fate of dsRNA in the nucleus: a p54(nrb)-containing complex mediates the nuclear retention of promiscuously A-to-I edited RNAs. Cell 106, 465-475 https://doi.org/10.1016/S0092-8674(01)00466-4

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