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Cell Growth and Development

Sustained Activation of p38 Mitogen-Activated Protein Kinase and c-Jun N-Terminal Kinase Pathways by Hepatitis B Virus X Protein Mediates Apoptosis via Induction of Fas/FasL and Tumor Necrosis Factor (TNF) Receptor 1/TNF-α Expression

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Pages 10352-10365 | Received 08 Oct 2003, Accepted 07 Sep 2004, Published online: 27 Mar 2023

REFERENCES

  • Ando, K., Moriyama T., Guidotti L. G., Wirth S., Schreiber R. D., Schlicht H. J., Huang S. N., and Chisari F. V.. 1993. Mechanisms of class I restricted immunopathology. A transgenic mouse model of fulminant hepatitis. J. Exp. Med. 178:1541–1554.
  • Appella, E., and Anderson C. W.. 2000. Signaling to p53: breaking the posttranslational modification code. Pathol. Biol. 48:227–245.
  • Awad, M. M., Enslen H., Boylan J. M., Davis R. J., and Gruppuso P. A.. 2000. Growth regulation via p38 mitogen-activated protein kinase in developing liver. J. Biol. Chem. 275:38716–38721.
  • Badley, A. D., Dockrell D., Simpson M., Schut R., Lynch D. H., Leibson P., and Paya C. V.. 1997. Macrophage-dependent apoptosis of CD4+ T lymphocytes from HIV-infected individuals is mediated by FasL and tumor necrosis factor. J. Exp. Med. 185:55–64.
  • Benn, J., and Schneider R. J.. 1994. Hepatitis B virus HBx protein activates Ras-GTP complex formation and establishes a Ras, Raf, MAP kinase signaling cascade. Proc. Natl. Acad. Sci. USA 91:10350–10354.
  • Benn, J., Su F., Doria M., and Schneider R. J.. 1996. Hepatitis B virus HBx protein induces transcription factor AP-1 by activation of extracellular signal-related and c-Jun N-terminal mitogen-activated protein kinases. J. Virol. 70:4978–4985.
  • Bennett, B. L., Sasaki D. T., Murray B. W., O'Leary E. C., Sakata S. T., Xu W., Leisten J. C., Motiwala A., Pierce S., Satoh Y., Bhagwat S. S., Manning A. M., and Anderson D. W.. 2001. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. USA 98:13681–13686.
  • Berberich, I., Shu G., Siebelt F., Woodgett J. R., Kyriakis J. M., and Clark E. A.. 1996. Cross-linking CD40 on B-cells preferentially induces stress-activated protein kinases rather than mitogen-activated protein kinases. EMBO J. 15:92–101.
  • Bouchard, M. J., Wang L., and Schneider R. J.. 2001. Calcium signaling by HBx protein in hepatitis B virus DNA replication. Science 294:2376–2378.
  • Brancho, D., Tanaka N., Jaeschke A., Ventura J.-J., Kelkar N., Tanaka Y., Kyuuma M., Takeshita T., Flavell R. A., and Davis R. J.. 2003. Mechanism of p38 MAP kinase activation in vivo. Genes Dev. 17:1969–1978.
  • Buendia, M. A. 1998. Hepatitis B viruses and cancerogenesis. Biomed. Pharmacother. 52:34–43.
  • Bulavin, D. V., Saito S., Hollander M. C., Sakaguchi K., Anderson C. W., Appella E., and Fornace A. J., Jr. 1999. Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation. EMBO J. 18:6845–6854.
  • Bulavin, D. V., Higashimoto Y., Popoff I. J., Gaarde W. A., Basrur V., Potapova O., Appella E., and Fornace A. J., Jr. 2001. Initiation of a G2/M checkpoint after ultraviolet radiation requires p38 kinase. Nature 411:102–107.
  • Chervonsky, A. V., Wang Y., Wong F. S., Visintin I., Flavell R. A., Janeway C. A., Jr., and Matis L. A.. 1997. The role of Fas in autoimmune diabetes. Cell 89:17–24.
  • Chirillo, P., Pagano S., Natoli G., Puri P., Burgio V. L., Balsano C., and Levrero M.. 1997. The hepatitis B virus X gene induces p53-mediated programmed cell death. Proc. Natl. Acad. Sci. USA 94:8162–8167.
  • Chisari, F. V. 2000. Viruses, immunity, and cancer: lessons from hepatitis B. Am. J. Pathol. 156:1117–1132.
  • Chuang, S. M., Wang I. C., and Yang J. L.. 2000. Roles of JNK, p38 and ERK mitogen-activated protein kinases in the growth inhibition and apoptosis induced by cadmium. Carcinogenesis 21:1423–1432.
  • Dandri, M., Schirmacher P., and Rogler C. E.. 1996. Woodchuck hepatitis virus X protein is present in chronically infected woodchuck liver and woodchuck hepatocellular carcinomas which are permissive for viral replication. J. Virol. 70:5246–5254.
  • Davies, S. P., Reddy H., Caivano M., and Cohen P.. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351:95–105.
  • Davis, R. J. 2000. Signal transduction by the JNK group of MAP kinases. Cell 103:239–252.
  • Dickens, M., Rogers J. S., Cavanagh J., Raitano A., Xia Z., Halpern J. R., Greenberg M. E., Sawyers C. L., and Davis R. J.. 1997. A cytoplasmic inhibitor of the JNK signal transduction pathway. Science 277:693–696.
  • Donovan, N., Becker E. B., Konishi Y., and Bonni A.. 2002. JNK phosphorylation and activation of BAD couples the stress-activated signaling pathway to the cell death machinery. J. Biol. Chem. 277:40944–40949.
  • Doria, M., Klein N., Lucito R., and Schneider R. J.. 1995. The hepatitis B virus is a dual specificity cytoplasmic activator of Ras and nuclear activator of transcription factors. EMBO J. 14:4747–4757.
  • Dumaz, N., and Meek D. W.. 1999. Serine15 phosphorylation stimulates p53 transactivation but does not directly influence interaction with HDM2. EMBO J. 18:7002–7010.
  • Earnshaw, W. C., Martins L. M., and Kaufmann S. H.. 1999. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem. 68:383–424.
  • Eferl, R., Ricci R., Kenner L., Zenz R., David J.-P., Rath M., and Wagner E. F.. 2003. Liver tumor development: c-Jun antagonizes the proapoptotic activity of p53. Cell 112:181–192.
  • Evan, G. I., and Vousden K. H.. 2001. Proliferation, cell cycle and apoptosis in cancer. Nature 411:342–348.
  • Faris, M., Kokot N., Latinis K., Kasibhatla S., Green D. R., Koretzky G. A., and Nel A.. 1998. The c-Jun N-terminal kinase cascade plays a role in stress-induced apoptosis in Jurkat cells by up-regulating Fas ligand expression. J. Immunol. 160:134–144.
  • Garcia-Fernandez, L. F., Losada A., Alcaide V., Alvarez A. M., Cuadrado A., Gonzalez L., Nakayama K., Nakayama K. I., Fernandez-Sousa J. M., Munoz A., and Sanchez-Puelles J. M.. 2002. Aplidin induces the mitochondrial apoptotic pathway via oxidative stress-mediated JNK and p38 activation and protein kinase C delta. Oncogene 21:7533–7544.
  • Giordano, C., Stassi G., De Maria R., Todaro M., Richiusa P., Papoff G., Ruberti G., Bagnasco M., Testi R., and Galluzzo A.. 1997. Potential involvement of Fas and its ligand in the pathogenesis of Hashimoto's thyroiditis. Science 275:960–963.
  • Hatai, T., Matsuzawa A., Inoshita S., Mochida Y., Kuroda T., Sakamaki K., Kuida K., Yonehara S., Ichijo H., and Takeda K.. 2002. Execution of apoptosis signal-regulating kinase 1 (ASK1)-induced apoptosis by the mitochondria-dependent caspase activation. J. Biol. Chem. 275:26576–26581.
  • Hayashi, N., and Mita E.. 1999. Involvement of Fas system-mediated apoptosis in pathogenesis of viral hepatitis. J. Viral Hepat. 6:357–365.
  • Hengartner, M. O. 2000. The biochemistry of apoptosis. Nature 407:770–775.
  • Hildesheim, J., Bulavin D. V., Anver M. R., Alvord W. G., Hollander M. C., Vardanian L., and Fornace A. J., Jr. 2002. Gadd45a protects against UV irradiation-induced skin tumors, and promotes apoptosis and stress signaling via MAPK and p53. Cancer Res. 62:7305–7315.
  • Hsu, S.-C., Gavrilin M. A., Tsai M.-H., Han J., and Lai M. Z.. 1999. p38 mitogen-activated protein kinase is involved in Fas ligand expression. J. Biol. Chem. 274:25769–25776.
  • Huang, C., Ma W. Y., Maxiner A., Sun Y., and Dong Z.. 1999. p38 kinase mediates UV-induced phosphorylation of p53 protein at serine 389. J. Biol. Chem. 274:12229–12235.
  • Ichijo, H., Nishida E., Irie K., ten Dijke P., Saitoh M., Moriguchi T., Takagi M., Matsumoto K., Miyazono K., and Gotoh Y.. 1997. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 275:90–94.
  • Iyoda, K., Sasaki Y., Horimoto M., Toyama T., Yakushijin T., Sakakibara M., Takehara T., Fujimoto J., Hori M., Wands J. R., and Hayashi N.. 2003. Involvement of the p38 mitogen-activated protein kinase cascade in hepatocellular carcinoma. Cancer 97:3017–3026.
  • Johnson, G. L., and Lapadat R.. 2002. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298:1911–1912.
  • Johnson, N. L., Gardner A. M., Diener K. M., Lange-Carter C. A., Gleavy J., Jarpe M. B., Minden A., Karin M., Zon L. I., and Johnson G. L.. 1996. Signal transduction pathways regulated by mitogen-activated/extracellular response kinase kinase induce cell death. J. Biol. Chem. 271:3229–3237.
  • Kanamoto, T., Mota M., Takeda K., Rubin L. L., Miyazono K., Ichijo H., and Bazenet C. E.. 2000. Role of apoptosis signal-regulating kinase in regulation of the c-Jun N-terminal kinase pathway and apoptosis in sympathetic neurons. Mol. Cell. Biol. 20:196–204.
  • Kaplowitz, N. 2000. Mechanisms of liver cell injury. J. Hepatol. 32:39–47.
  • Kim, K.-H., and Seong B. L.. 2003. Pro-apoptotic function of HBV X protein is mediated by interaction with c-FLIP and enhancement of death-inducing signal. EMBO J. 22:2104–2116.
  • Klein, N. P., and Schneider R. J.. 1997. Activation of Src family kinases by hepatitis B virus HBx protein and coupled signal to Ras. Mol. Cell. Biol. 17:6427–6436.
  • Kondo, T., Suda T., Fukuyama H., Adachi M., and Nagata S.. 1997. Essential roles of the Fas ligand in the development of hepatitis. Nat. Med. 3:409–413.
  • Korsmeyer, S. J., Wei M. C., Saito M., Weiler S., Oh K. J., and Schlesinger P. H.. 2000. Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ. 12:1166–1173.
  • Kyriakis, J. M., and Avruch J.. 2001. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81:807–869.
  • Lambert, P. F., Kashanchi F., Radonovich M. F., Shiekhattar R., and Brady J. N.. 1998. Phosphorylation of p53 serine 15 increases interaction with CBP. J. Biol. Chem. 273:33048–33053.
  • Lee, S., Tarn C., Wang W.-H., Chen S., Hullinger R. L., and Andrisani O. M.. 2002. Hepatitis B virus X protein differentially regulates cell cycle progression in X-transforming versus non-transforming hepatocyte (AML12) cell lines. J. Biol. Chem. 277:8730–8740.
  • Lei, K., and Davis R. J.. 2003. JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc. Natl. Acad. Sci. USA 100:2432–2437.
  • Lei, K., Nimnual A., Zong W.-X., Kennedy N. J., Flavell R. A., Thompson C. B., Bar-Sagi D., and Davis R. J.. 2002. The Bax subfamily of Bcl2-related proteins is essential for apoptotic signal transduction by c-Jun NH2-terminal kinase. Mol. Cell. Biol. 22:4929–4942.
  • Le-Niculescu, H., Bonfoco E., Kasuya Y., Claret F.-X., Green D. R., and Karin M.. 1999. Withdrawal of survival factors results in activation of the JNK pathway in neuronal cells leading to Fas ligand induction and cell death. Mol. Cell. Biol. 19:751–763.
  • Li, H., Zhu H., Xu C. J., and Yuan J.. 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491–501.
  • Lin, A., and Karin M.. 2003. NF-κB in cancer: a marked target. Semin. Cancer Biol. 13:107–114.
  • Luo, X., Budihardjo I., Zou H., Slaughter C., and Wang X.. 1998. Bid, a Bc12 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94:481–490.
  • MacFarlane, M., Cohen G. M., and Dickens M.. 2000. JNK (c-Jun N-terminal kinase) and p38 activation in receptor-mediated and chemically-induced apoptosis of T-cells: differential requirements for caspase activation. Biochem. J. 348:93–101.
  • Mansouri, A., Ridgway L. D., Korapati A. L., Zhang Q., Tian L., Wang T., Siddik Z. H., Mills G. B., and Claret F. X.. 2003. Sustained activation of JNK/p38MAPK pathways in response to cisplatin leads to Fas ligand induction and cell death in ovarian carcinoma cells. J. Biol. Chem. 278:19245–19256.
  • Meier, P., Finch A., and Evan G.. 2000. Apoptosis in development. Nature 407:796–801.
  • Munsch, D., Watanabe-Fukunaga R., Bourdon J.-C., Nagata S., May E., Yonish-Rouach E., and Reisdorf P.. 2000. Human and mouse Fas (APO-1/CD95) death receptor genes each contain a p53-responsive element that is activated by p53 mutants unable to induce apoptosis. J. Biol. Chem. 275:3867–3872.
  • Nagata, S. 1996. Fas ligand and immune evasion. Nat. Med. 2:1306–1307.
  • Nagata, S. 1999. Fas ligand-induced apoptosis. Annu. Rev. Genet. 33:29–55.
  • Nagata, Y., and Todokoro K.. 1999. Requirement of activation of JNK and p38 for environmental stress-induced erythroid differentiation and apoptosis and of inhibition of ERK for apoptosis. Blood 94:853–863.
  • Namgung, U., and Xia Z.. 2000. Arsenite-induced apoptosis in cortical neurons is mediated by c-Jun N-terminal protein kinase 3 and p38 mitogen-activated protein kinase. J. Neurosci. 20:6442–6451.
  • Ono, K., and Han J.. 2000. The p38 signal transduction pathway activation and function. Cell. Signal. 12:13.
  • Roulston, A., Reinhard C., Amiri P., and Williams L. T.. 1998. Early activation of c-Jun N-terminal kinase and p38 kinase regulate cell survival in response to tumor necrosis factor α. J. Biol. Chem. 273:10232–10239.
  • Shieh, S.-Y., Ikeda M., Taya Y., and Prives C.. 1997. DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91:325–334.
  • Sluss, H. K., Barrett T., Derijard T., and Davis R. J.. 1994. Signal transduction by tumor necrosis factor mediated by JNK protein kinases. Mol. Cell. Biol. 14:8376–8384.
  • Strand, S., Hofmann W. J., Hug H., Müller M., Otto G., Strand D., Mariani S. M., Stremmel W., Krammer P. H., and Galle P. R.. 1996. Lymphocyte apoptosis induced by CD95 (APO-1/Fas) ligand-expressing tumor cells—a mechanism of immune evasion? Nat. Med. 2:1361–1366.
  • Su, F., and Schneider R. J.. 1997. Hepatitis B virus HBx protein sensitizes cells to apoptotic killing by tumor necrosis factor alpha. Proc. Natl. Acad. Sci. USA 94:8744–8749.
  • Su, F., Theodosis C. N., and Schneider R. J.. 2001. Role of NF-κB and Myc proteins in apoptosis induced by hepatitis B virus HBx protein. J. Virol. 75:215–225.
  • Tarn, C., Bilodeau M. L., Hullinger R. L., and Andrisani O. M.. 1999. Differential immediate early gene expression in conditional hepatitis B virus pX-transforming versus nontransforming hepatocyte cell lines. J. Biol. Chem. 74:2327–2336.
  • Tarn, C., Zou L., Hullinger R. L., and Andrisani O. M.. 2002. Hepatitis B virus X protein activates the p38 mitogen-activated protein kinase pathway in dedifferentiated hepatocytes. J. Virol. 76:9763–9772.
  • Tarn, C., Lee S., Hu Y., Ashendal C., and Andrisani O. M.. 2001. Hepatitis B virus X protein differentially activates RAS-RAF-MAPK and JNK pathways in X-transforming versus non-transforming AML-12 hepatocytes. J. Biol. Chem. 276:34671–34680.
  • Terradillos, O., de La Coste A., Pollicino T., Neuveut C., Sitterlin D., Lecoeur H., Gougeon M.-L., Kahn A., and Buendia M.-A.. 2002. The hepatitis B virus X protein abrogates Bcl-2-mediated protection against Fas apoptosis in the liver. Oncogene 21:377–386.
  • Thompson, C. B. 1995. Apoptosis in the pathogenesis and treatment of disease. Science 267:1456–1462.
  • Tibbles, L. A., and Woodgett J. R.. 1999. The stress-activated protein kinase pathways. Cell. Mol. Life Sci. 55:1230–1254.
  • Tilly, J. L., and Hsueh A. J.. 1993. Microscale autoradiographic method for the qualitative and quantitative analysis of apoptotic DNA fragmentation. J. Cell. Physiol. 154:519–526.
  • Tobiume, K., Matsuzawa A., Takahashi T., Nishitoh H., Morita K., Takeda K., Minowa O., Miyazono K., Noda T., and Ichijo H.. 2001. ASK1 is required for sustained activations of JNK and p38 MAP kinases and apoptosis. EMBO Rep. 2:222–228.
  • Tournier, C., Hess P., Yang D. D., Xu J., Turner T. K., Nimnual A., A., Bar-Sagi D., Jones S. N., Flavell R. A., and Davis R. J.. 2000. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288:870–874.
  • Wang, K., Yin X. M., Chao D. T., Milliman C. L., and Korsmeyer S. J.. 1996. BID: a novel BH3 domain-only death agonist. Genes Dev. 10:2859–2869.
  • Wang, X. 2001. The expanding role of mitochondria in apoptosis. Genes Dev. 15:2922–2933.
  • Wang, X., McGowan C. H., Zhao M., He L., Downey J. S., Fearns C., Wang Y., Huang S., and Han J.. 2000. Involvement of the MKK6-p38γ cascade in γ-radiation-induced cell cycle arrest. Mol. Cell. Biol. 20:4543–4552.
  • Watanabe, T., et al. 2002. 1/MKK4-mediated SAPK/JNK signaling participates in embryonic hepatoblast proliferation via a pathway different from NF-κB-induced anti-apoptosis. Dev. Biol. 250:332–347.
  • Wong, B., and Choi Y.. 1997. Pathways leading to cell death in T cells. Curr. Opin. Immunol. 9:358–364.
  • Xia, Z., Dickens M., Raingeaud J., Davis R. J., and Greenberg M. E.. 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270:1326–1331.
  • Yin, X. M. 2000. Bid, a critical mediator for apoptosis induced by the activation of Fas/TNF-R1 death receptors in hepatocytes. J. Mol. Med. 78:203–211.
  • Yin, X. M., Wang K., Gross A., Zhao Y., Zinkel S., Klocke B., Roth K. A., and Korsmeyer S. J.. 1999. Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature 400:886–891.
  • Yuan, J., and Yankner B. A.. 2000. Apoptosis in the nervous system. Nature 407:802–809.
  • Zhang, J., Gao J.-X., Salojin K., Shao Q., Grattan M., Meagher C., Laird D. W., and Delovitch T. L.. 2000. Regulation of Fas ligand expression during activation-induced cell death in T cells by p38 mitogen-activated protein kinase and c-Jun NH2-terminal kinase. J. Exp. Med. 191:1017–1029.
  • Zoulim, F., Saputelli J., and Seeger C.. 1994. Woodchuck hepatitis virus X protein is required for viral infection in vivo. J. Virol. 68:2026–2030.

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