1887

Abstract

Poliovirus (PV)-induced apoptosis seems to play a major role in central nervous system (CNS) tissue injury, a crucial feature of the pathogenesis of poliomyelitis. We have previously shown that calcium (Ca) flux from the endoplasmic reticulum (ER) to the cytosol during PV infection is involved in apoptosis induction in human neuroblastoma cells. We show here that PV infection is associated with a transient upregulation of Herp (homocysteine-induced ER protein), a protein known to promote the degradation of ER-resident Ca channels. Herp gene transcription is controlled by the transcription factor CREB3 (cAMP response element-binding protein 3). We found that the CREB3/Herp pathway limited the increase in cytosolic Ca concentration and apoptosis early in PV infection. This may reduce the extent of PV-induced damage to the CNS during poliomyelitis.

Keyword(s): apoptosis , calcium flux , CREB3 , Herp and Poliovirus
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2016-09-01
2024-03-29
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References

  1. Agol V. I., Belov G. A., Bienz K., Egger D., Kolesnikova M. S., Romanova L. I., Sladkova L. V., Tolskaya E. A. 2000; Competing death programs in poliovirus-infected cells: commitment switch in the middle of the infectious cycle. J Virol 74:5534–5541 [View Article][PubMed]
    [Google Scholar]
  2. Asada R., Kanemoto S., Kondo S., Saito A., Imaizumi K. 2011; The signalling from endoplasmic reticulum-resident bZIP transcription factors involved in diverse cellular physiology. J Biochem 149:507–518 [View Article][PubMed]
    [Google Scholar]
  3. Autret A., Martin-Latil S., Mousson L., Wirotius A., Petit F., Arnoult D., Colbère-Garapin F., Estaquier J., Blondel B. 2007; Poliovirus induces Bax-dependent cell death mediated by c-Jun NH2- terminal kinase. J Virol 81:7504–7516 [View Article][PubMed]
    [Google Scholar]
  4. Autret A., Martin-Latil S., Brisac C., Mousson L., Colbère-Garapin F., Blondel B. 2008; Early phosphatidylinositol 3-kinase/Akt pathway activation limits poliovirus-induced JNK-mediated cell death. J Virol 82:3796–3802 [View Article][PubMed]
    [Google Scholar]
  5. Belal C., Ameli N. J., El Kommos A., Bezalel S., Al'Khafaji A. M., Mughal M. R., Mattson M. P., Kyriazis G. A., Tyrberg B., Chan S. L. 2012; The homocysteine-inducible endoplasmic reticulum (ER) stress protein Herp counteracts mutant α-synuclein-induced ER stress via the homeostatic regulation of ER-resident calcium release channel proteins. Hum Mol Genet 21:963–977 [View Article][PubMed]
    [Google Scholar]
  6. Belov G. A., Romanova L. I., Tolskaya E. A., Kolesnikova M. S., Lazebnik Y. A., Agol V. I. 2003; The major apoptotic pathway activated and suppressed by poliovirus. J Virol 77:45–56 [View Article][PubMed]
    [Google Scholar]
  7. Belov G. A., van Kuppeveld F. J. 2012; (+)RNA viruses rewire cellular pathways to build replication organelles. Curr Opin Virol 2:740–747 [View Article][PubMed]
    [Google Scholar]
  8. Brisac C., Téoulé F., Autret A., Pelletier I., Colbère-Garapin F., Brenner C., Lemaire C., Blondel B. 2010; Calcium flux between the endoplasmic reticulum and mitochondrion contributes to poliovirus-induced apoptosis. J Virol 84:12226–12235 [View Article][PubMed]
    [Google Scholar]
  9. Chami M., Oulès B., Paterlini-Bréchot P. 2006; Cytobiological consequences of calcium-signaling alterations induced by human viral proteins. Biochim Biophys Acta 1763:1344–1362 [View Article][PubMed]
    [Google Scholar]
  10. Chan C.-P., Kok K.-H., Jin D.-Y. 2011; CREB3 subfamily transcription factors are not created equal: recent insights from global analyses and animal models. Cell Biosci 1:6 [View Article]
    [Google Scholar]
  11. Chan S. L., Fu W., Zhang P., Cheng A., Lee J., Kokame K., Mattson M. P. 2004; Herp stabilizes neuronal Ca2+ homeostasis and mitochondrial function during endoplasmic reticulum stress. J Biol Chem 279:28733–28743 [View Article][PubMed]
    [Google Scholar]
  12. Dougherty J. D., Park N., Gustin K. E., Lloyd R. E. 2010; Interference with cellular gene. In The Picornaviruses pp. 165–180 Edited by Ehrenfeld E., Domingo E., Roos R. P. Washington, DC: ASM Press; [CrossRef]
    [Google Scholar]
  13. Estaquier J., Idziorek T., de Bels F., Barre-Sinoussi F., Hurtrel B., Aubertin A. M., Venet A., Mehtali M., Muchmore E., Michel P. 1994; Programmed cell death and AIDS: significance of T-cell apoptosis in pathogenic and nonpathogenic primate lentiviral infections. Proc Natl Acad Sci U S A 91:9431–9435 [View Article]
    [Google Scholar]
  14. Girard S., Couderc T., Destombes J., Thiesson D., Delpeyroux F., Blondel B. 1999; Poliovirus induces apoptosis in the mouse central nervous system. J Virol 73:6066–6072[PubMed]
    [Google Scholar]
  15. Gosselin A. S., Simonin Y., Guivel-Benhassine F., Rincheval V., Vayssière J. L., Mignotte B., Colbère-Garapin F., Couderc T., Blondel B. 2003; Poliovirus-induced apoptosis is reduced in cells expressing a mutant CD155 selected during persistent poliovirus infection in neuroblastoma cells. J Virol 77:790–798 [View Article][PubMed]
    [Google Scholar]
  16. Kokame K., Agarwala K. L., Kato H., Miyata T. 2000; Herp, a new ubiquitin-like membrane protein induced by endoplasmic reticulum stress. J Biol Chem 275:32846–32853 [View Article][PubMed]
    [Google Scholar]
  17. Leitman J., Shenkman M., Gofman Y., Shtern N. O., Ben-Tal N., Hendershot L. M., Lederkremer G. Z. 2014; Herp coordinates compartmentalization and recruitment of HRD1 and misfolded proteins for ERAD. Mol Biol Cell 25:1050–1060 [View Article][PubMed]
    [Google Scholar]
  18. Liang G., Audas T. E., Li Y., Cockram G. P., Dean J. D., Martyn A. C., Kokame K., Lu R. 2006; Luman/CREB3 induces transcription of the endoplasmic reticulum (ER) stress response protein Herp through an ER stress response element. Mol Cell Biol 26:7999–8010 [View Article][PubMed]
    [Google Scholar]
  19. Livak K. J., Schmittgen T. D. 2001; Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408 [View Article][PubMed]
    [Google Scholar]
  20. Pallansch M., Roos R. 2007; Enteroviruses: polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. In Fields Virology vol. 1 pp. 839–893 Edited by Knipe D. M., Howley P. M. Philadelphia: Lippincott Williams and Wilkins;
    [Google Scholar]
  21. Paul A., Wimmer E. 2015; Initiation of protein-primed picornavirus RNA synthesis. Virus Research 206:12–26 [View Article]
    [Google Scholar]
  22. Raggo C., Rapin N., Stirling J., Gobeil P., Smith-Windsor E., O'Hare P., Misra V. 2002; Luman, the cellular counterpart of herpes simplex virus VP16, is processed by regulated intramembrane proteolysis. Mol Cell Biol 22:5639–5649 [View Article][PubMed]
    [Google Scholar]
  23. Sai X., Kokame K., Shiraishi H., Kawamura Y., Miyata T., Yanagisawa K., Komano H. 2003; The ubiquitin-like domain of Herp is involved in Herp degradation, but not necessary for its enhancement of amyloid β-protein generation. FEBS Letters 553:151–156 [View Article]
    [Google Scholar]
  24. Schulze A., Standera S., Buerger E., Kikkert M., van Voorden S., Wiertz E., Koning F., Kloetzel P. M., Seeger M. 2005; The ubiquitin-domain protein HERP forms a complex with components of the endoplasmic reticulum associated degradation pathway. J Mol Biol 354:1021–1027 [View Article][PubMed]
    [Google Scholar]
  25. Téoulé F., Brisac C., Pelletier I., Vidalain P. O., Jégouic S., Mirabelli C., Bessaud M., Combelas N., Autret A. et al. 2013; The Golgi protein ACBD3, an interactor for poliovirus protein 3A, modulates poliovirus replication. J Virol 87:11031–11046 [View Article][PubMed]
    [Google Scholar]
  26. Thastrup O., Cullen P. J., Drøbak B. K., Hanley M. R., Dawson A. P. 1990; Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci U S A 87:2466–2470 [View Article][PubMed]
    [Google Scholar]
  27. van Kuppeveld F., Belov G., Ehrenfeld E. 2010; Remodeling cellular membranes. In The Picornaviruses pp. 181–193 Edited by Ehrenfeld E., Domingo E., Roos R. P. Washington, DC: ASM Press; [CrossRef]
    [Google Scholar]
  28. Yan L., Liu W., Zhang H., Liu C., Shang Y., Ye Y., Zhang X., Li W. 2014; Ube2g2-gp78-mediated HERP polyubiquitylation is involved in ER stress recovery. J Cell Sci 127:1417–1427 [View Article][PubMed]
    [Google Scholar]
  29. Ying Z., Zhang R., Verge V. M., Misra V. 2014; Cloning and characterization of rat Luman/CREB3, a transcription factor highly expressed in nervous system tissue. J Mol Neurosci doi.10.1007/s12031-014-0330-7 [View Article][PubMed]
    [Google Scholar]
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