Apoptosis and the Cytopathic Effects of Reovirus

  • S. M. Oberhaus
  • T. S. Dermody
  • K. L. Tyler
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 233/2)

Abstract

Reoviruses are cytolytic viruses which cause the death of infected cells in vitro and in vivo. The relationship between events involved in the production of virus and death of the infected cell is not clearly understood. Studies of virus-induced biochemical and morphological changes in cells, i.e., cytopathic effects, have begun to define both viral and cellular factors involved in virus-induced cell death. The description and definition of apoptosis as a mechanism of cell death distinct from necrosis has provided a framework for elucidating the roles of these viral and cellular factors in the cell death process. The demonstration that reovirus induces apoptosis in vitro and in vivo identifies apoptosis as an important component of reovirus-induced cytopathic effects and tissue injury. In this chapter we review the current data describing reovirus-induced apoptosis and propose that many of the previously described cytopathic effects of reovirus infection represent events which initiate or comprise steps in the apoptotic process.

Keywords

Permeability Shrinkage Oligomer Polypeptide Compaction 

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References

  1. Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thornberry NA, Wong WW, Yuan J (1996) Human ICE/CED-3 protease nomenclature. Cell 87: 171PubMedCrossRefGoogle Scholar
  2. Belli BA, Samuel CE (1991) Biosynthesis of reovirus-specified polypeptides: expression of reovirus SI encoded sigma INS protein in transfected and infected cells as measured with serotype specific polyclonal antibody. Virology 185:698–709PubMedCrossRefGoogle Scholar
  3. Boise LH, Gottschalk AR, Quintans J, Thompson CB (1995) Bel-2 and Bcl-2-related proteins in apoptosis regulation. In: Kroemer G, Martinez AC (eds) Apoptosis in Immunology. Springer, Berlin Heidelberg New York, pp 107–121 (Current topics in microbiology and immunology, vol 200)Google Scholar
  4. Bursch W, Oberhammer F, Schulte-Hermann R (1992) Cell death by apoptosis and its protective role against disease. Trends Pharmacol Sci 13:245–251PubMedCrossRefGoogle Scholar
  5. Cashdollar LW, Blair P, Van Dyne S (1989) Identification of the sigma is protein in reovirus serotype 2-infected cells with antibody prepared against a bacterial fusion protein. Virology 168:183–186PubMedCrossRefGoogle Scholar
  6. Ceruzzi M, Shatkin AJ (1986) Expression of reovirus p14 in bacteria and identification in the cytoplasm of infected mouse L cells. Virology 153:35–45PubMedCrossRefGoogle Scholar
  7. Chaly N, Johnstone M, Hand R (1980) Alterations in nuclear structure and function in reovirus-infected cells. Clin Invest Med 2:141–152Google Scholar
  8. Cohen JJ, Duke RC (1984) Glucocorticoid activation of a calcium dependent endonuclease in thymocyte nuclei leads to cell death. J Immunol 132:38–42PubMedGoogle Scholar
  9. de Jong D, Prins F, Van Krieken HHJM, Mason DY, Van Ommen GB, Kluin PM (1992) Subcellular localization of bel-2 protein. In: Potter M, Melchers F (eds) Mechanisms in B cell neoplasia. Springer, Berlin Heidelberg New York, pp 287–292 (Current topics in microbiology and immunology, vol 176)Google Scholar
  10. Dermody TS, Nibert ML, Wetzel JD, Tong X, Fields BN (1993) Cells and viruses with mutations affecting viral entry are selected during persistent infections of L cells with mammalian reoviruses. J Virol 67:2055–2063PubMedGoogle Scholar
  11. Duke DC, Chervenak R, Cohen JJ (1983) Endogenous endonuclease-induced DNA fragmentation: an early event in cell mediated cytolysis. Proc Natl Acad Sci USA 80:6361–6365PubMedCrossRefGoogle Scholar
  12. Duncan MR, Stanish SM, Cox DC (1978) Differential sensitivity of normal and transformed human cells to reovin’is infection. J Virol 28:444–449PubMedGoogle Scholar
  13. Ensminger WD, Tamm I (1969a) Cellular DNA and protein synthesis in reovirus-infected cells. Virology 39:357–359CrossRefGoogle Scholar
  14. Ensminger WD, Tamm I (1969b) The step in cellular DNA synthesis blocked by reovirus infection. Virology 39:935–938CrossRefGoogle Scholar
  15. Ernst H, Shatkin AJ (1985) Reovirus hemagglutinin mRNA codes for two polypeptides in overlapping reading frames. Proc Natl Acad Sci USA 82:48–52PubMedCrossRefGoogle Scholar
  16. Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, Henson PM (1992) Exposure of phosphatidyl serine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 148:2207–2216PubMedGoogle Scholar
  17. Farone AL, O’Brien PC, Cox DC (1993) Tumor necrosis factor-alpha induction by reovirus serotype 3. J Leukocyte Biol 53:133–137PubMedGoogle Scholar
  18. Farrow SN, Brown R (1996) New members of the Bc1–2 family and their protein partners. Curr Opin Genet Dev 6:45–49PubMedCrossRefGoogle Scholar
  19. Finkel TH, Tudor-Williams G, Banda NK, Cotton MF, Curiel T, Monks C, Baba TW, Ruprecht RM, Kupfer A (1995) Apoptosis occurs predominately in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nat Med 1:129–134PubMedCrossRefGoogle Scholar
  20. Freeman R, Estus SEM (1994) Analysis of cell-cycle related gene expression in postmitotic neurons: selective induction of cyclin D1 during programmed cell death. Neuron 12:343–355PubMedCrossRefGoogle Scholar
  21. Gaulton GN, Greene MI (1989) Inhibition of cellular DNA synthesis by reovirus occurs through a receptor-linked signaling pathway that is mimicked by antiidiotypic, antireceptor antibody. J Exp Med 169:197–211PubMedCrossRefGoogle Scholar
  22. Gauntt CJ (1973) Induction of interferon in L cells by reoviruses. Infection Immun 7:711–717Google Scholar
  23. Gomatos PJ, Tamm I (1963) Macromolecular synthesis in reovirus infected L cells. Biochim Biophys Acta 72:651–653PubMedCrossRefGoogle Scholar
  24. Gorman AM, McGowan A, O’Neill C, Cotter T (1996) Oxidative stress and apoptosis in neurodegeneration. J Neurol Sci 139:45–52PubMedCrossRefGoogle Scholar
  25. Hand R, Tamm I (1973) Reovirus: effect of noninfective viral components on cellular deoxyribonucleic acid synthesis. J Virol 11:223–231PubMedGoogle Scholar
  26. Hand R, Ensminger WD, Tamm T (1971) Cellular DNA replication in infections with cytocidal RNA viruses. Virology 44:527–536PubMedCrossRefGoogle Scholar
  27. Henderson DR, Joklik WK (1978) The mechanism of interferon induction by UV-irradiated reovirus. Virology 91:389–406PubMedCrossRefGoogle Scholar
  28. Hinshaw VS, Olsen CW, Dybdahl-Sissoko N, Evans D (1994) Apoptosis: a mechanism of cell killing by influenza A and B viruses. J Virol 68:3667–3673PubMedGoogle Scholar
  29. Hockenbery D, Nunez G, Milliman C, Schreiber RD, Korsmeyer SJ (1990) Bel-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348:334–336PubMedCrossRefGoogle Scholar
  30. Houge G, Robaye B, Elkhom TS, Golstein J, Mellgren G, Gjertsen BT, Lanotte M, Doskeland SO (1995) Fine mapping of 28S rRNA sites specifically cleaved in cells undergoing apoptosis. Mol Cell Biol 15:2051–2062PubMedGoogle Scholar
  31. Hrdy DB, Duby DN, Fields BN (1982) Molecular basis of reovirus neurovirulence: role of the M2 gene in avirulence. Proc Natl Acad Sci USA 79:1298–1302PubMedCrossRefGoogle Scholar
  32. Inoue Y, Yasukawa M, Fujita S (1997) Induction of T-cell apoptosis by human herpesvirus 6. J Virol 71:3751–3759PubMedGoogle Scholar
  33. Jacobs JL, Ferguson RE (1991) The Lang strain of reovirus serotype 1 and the Dearing strain of reovirus serotype 3 differ in their sensitivities to beta interferon. J Virol 65:5102–5104PubMedGoogle Scholar
  34. Jacobs JL, Samuel CE (1985) Biosynthesis of reovirus-specified polypeptides: the reovirus SI mRNA encodes two primary translation products. Virology 143:63–74PubMedCrossRefGoogle Scholar
  35. Kerr JFR, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239–257PubMedCrossRefGoogle Scholar
  36. Koopman G, Reutelingsperger CPM, Kuijten GAM, Keehnen RMJ, Pals ST, Van Oers MHJ (1994) Annexin V for flow cytometric detection of phosphatidyl-serine expression on B cells undergoing apoptosis. Blood 84:1415–1420PubMedGoogle Scholar
  37. Korsmeyer SJ (1992) Bd-2 initiates a new category of oncogenes: regulators of cell death. Blood 80: 879–886PubMedGoogle Scholar
  38. Lai M-HT, Joklik WK (1973) The induction of interferon by temperature-sensitive mutants of reovirus, UV-irradiated reovirus, and subviral reovirus particles. Virology 51:191–204PubMedCrossRefGoogle Scholar
  39. Lai M-HT, Werenne JJ, Joklik WK (1973) The preparation of reovirus top component and its effect on host DNA and protein synthesis. Virology 53:237–244CrossRefGoogle Scholar
  40. Lee PW, Hayes EC, Joklik WK (1981) Protein sigma I is the reovirus cell attachment protein. Virology 108:156–163PubMedCrossRefGoogle Scholar
  41. Levine B, Huang Q, Issacs JT, Reed JC, Griffin DE, Hardwick JM (1993) Conversion of lytic to persistent alphavirus infection by the bc1–2 oncogene. Nature 361:739–742PubMedCrossRefGoogle Scholar
  42. Lewis J, Wesselingh SL, Griffin DE, Hardwick JM (1996) Alphavirus-induced apoptosis in mouse brains correlates with neurovirulence. J Virol 70:1828–1835PubMedGoogle Scholar
  43. Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86(1):147–157PubMedCrossRefGoogle Scholar
  44. Long WF, Burke DC (1971) Interferon production by double-stranded RNA: a comparison of interferon induction by reovirus RNA to that by a synthetic double-stranded polynucleotide. J Gen Virol 12: 1–11PubMedCrossRefGoogle Scholar
  45. Lucia-Jandris P, Hooper JW, Fields BN (1993) Reovirus M2 gene is associated with chromium release from L cells. J Virol 67:5339–5345PubMedGoogle Scholar
  46. MacDonald RG, Martin TP, Cidlowski JA (1980) Glucocorticoids stimulate protein degradation in lymphocytes: a possible mechanism of steroid-induced cell death. Endocrinology 107:1512–1524PubMedCrossRefGoogle Scholar
  47. Majno G, Joris I (1995) Apoptosis, oncosis, and necrosis. Am J Pathol 146:3–15PubMedGoogle Scholar
  48. Matoba Y, Sherry B, Fields BN, Smith TW (1991) Identification of the viral genes responsible for growth of reovirus in cultured mouse heart cells. J Clin Invest 87:1628–1633PubMedCrossRefGoogle Scholar
  49. Matoba Y, Colucci WS, Fields BN, Smith TW (1993) The reovirus MI gene determines the relative capacity of growth of reovirus in cultured bovine aortic endothelial cells. J Clin Invest 92:2883–2888PubMedCrossRefGoogle Scholar
  50. McCrae MA. Joklik WK (1978) The nature of the polypeptide encoded by each of the ten double-stranded RNA segments of reovirus type 3. Virology 89:578–593PubMedCrossRefGoogle Scholar
  51. Meikrantz W, Schlegel R (1995) Apoptosis and the cell cycle. J Cell Biochem 58:160–174PubMedCrossRefGoogle Scholar
  52. Mustoe TA, Ramig RF, Sharpe AH, Fields BN (1978) Genetics of reovirus: identification of the dsRNA segments encoding the polypeptides of the mu and sigma size classes. Virology 89:594–604Google Scholar
  53. Nibert ML, Fields BN (1992) A carboxy-terminal fragment of p1/plc is present in infectious subvirion particles of mammalian reoviruses and is proposed to have a role in penetration. J Virol 66:6408–6418PubMedGoogle Scholar
  54. Nibert ML, Schiff LA, Fields BN (1996) Reoviruses and their replication. In: Fields BN, Knipe DM, Howley PM et al (eds) Fields virology, 3rd edn. Raven, New York, pp 1557–1596Google Scholar
  55. Oberhaus SM, Smith RL, Clayton GH, Dermody TS, Tyler KL (1997) Reovirus infection and tissue injury in the mouse central nervous system are associated with apoptosis. J Virol 71:2100–2106PubMedGoogle Scholar
  56. Ramig RF, Ward RL (1991) Genomic segment reassortment in rotaviruses and other reoviridae. Adv Virus Res 39:163–207PubMedCrossRefGoogle Scholar
  57. Rodgers SE, Barton ES, Oberhaus SM, Pike B, Gibson CA, Tyler KL, Dermody TS (1997) Reovirusinduced apoptosis of MDCK cells is not linked to viral yield and is blocked by Bel-2. J Virol 71:25402546Google Scholar
  58. Saragovi HU, Bhandoola A, Lemercier MA, Mohamad Akbar GK, Greene MI (1995) A receptor that subserves reovirus binding can inhibit lymphocyte proliferation triggered by mitogenic signals. DNA Cell Biol 14:653–664PubMedCrossRefGoogle Scholar
  59. Sarkar G, Pelletier J, Bassel-Duby R, Jayasuriya A, Fields BN, Sonnenberg N (1985) Identification of a new polypeptide coded by reovirus gene SI.I Virol 54:720–725Google Scholar
  60. Schwartzman RA, Cidlowski JA (1993) Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocr Rev 14:133–151PubMedGoogle Scholar
  61. Sharpe AH, Fields BN (1981) Reovirus inhibition of cellular DNA synthesis: role of the SI gene. J Virol 38:389–392PubMedGoogle Scholar
  62. Sharpe AH, Fields BN (1982) Reovirus inhibition of cellular RNA and protein synthesis: role of the S4 gene. Virology 122:381–391PubMedCrossRefGoogle Scholar
  63. Sharpe AH, Chen LB, Fields BN (1982) The interaction of mammalian reoviruses with the cytoskeleton of monkey kidney CV-1 cells. Virology 120:399–411PubMedCrossRefGoogle Scholar
  64. Shaw JE, Cox DC (1973) Early inhibition of cellular DNA synthesis by high multiplicities of infectious and UV-inactivated reovirus. J Virol 12:704–710PubMedGoogle Scholar
  65. Shen Y, Shenk TE (1995) Viruses and apoptosis. Curr Opin Genet Dev 5:105–111PubMedCrossRefGoogle Scholar
  66. Squier MKT, Cohen JJ (1997) Calpain, an upstream regulator of thymocyte apoptosis. J Immunol 158:3690–3697PubMedGoogle Scholar
  67. Squier MKT, Miller ACK, Malkinson AM, Cohen JJ (1994) Calpain activation in apoptosis. J Cell Physiol 159:229–237PubMedCrossRefGoogle Scholar
  68. Tardieu M, Powers ML, Weiner HL (1983) Age dependent susceptibility to reovirus type 3 encephalitis: role of viral and host factors. Ann Neurol 13:602–607PubMedCrossRefGoogle Scholar
  69. Thompson CB (1995) Apoptosis in the pathogenesis and treatment of disease. Science 267:1456–1462PubMedCrossRefGoogle Scholar
  70. Tyler KL, Fields BN (1996) Reoviruses. In: Fields BN, Knipe DM, Howley PM et al (eds) Fields virology, 3rd edn. Raven, New York, pp 1597–1624Google Scholar
  71. Tyler KL, Squier MKT, Rodgers SE, Schneider BE, Oberhaus SM, Grdina TA, Cohen JJ, Dermody TS (1995) Differences in the capacity of reovirus strains to induce apoptosis are determined by the viral attachment protein 01. J Virol 69:6972–6979PubMedGoogle Scholar
  72. Tyler KL, Squier MKT, Brown AL, Pike B, Willis D, Oberhaus SM, Dermody TS, Cohen JJ (1996) Linkage between reovirus-induced apoptosis and inhibition of cellular DNA synthesis: role of the SI and M2 genes. J Virol 70:7984–7991PubMedGoogle Scholar
  73. Ucker DS (1991) Death by suicide: one way to go in mammalian cellular, development. New Biol 3: 103–109PubMedGoogle Scholar
  74. Weiner HL, Drayna D, Averill DR, Fields B (1977) Molecular basis of reovirus virulence: role of the SI gene. Proc Natl Acad Sci USA 74:5744–5748PubMedCrossRefGoogle Scholar
  75. Weiner HL, Ault KA, Fields BN (1980a) Interaction of reovirus with cell surface receptors. I. Murine and human lymphocytes have a receptor for the hemagglutinin of reovirus type 3. J Immunol 124:2143–2148Google Scholar
  76. Weiner HL, Powers ML, Fields BN (1980b) Absolute linkage of virulence and central nervous system tropism of reoviruses to viral hemagglutinin. J Infect Dis 141:609–616CrossRefGoogle Scholar
  77. Wetzel JD, Wilson GJ, Baer GS, Dunnigan LR, Wright JP, Tang DSH, Dermody TS (1997) Reovirus variants selected during persistent infections of L cells contain mutations in the viral SI and S4 genes and are altered in viral disassembly. J Virol 71:1362–1369Google Scholar
  78. Wilson GJ, Wetzel JD, Puryear W, Bassel-Duby R, Dermody TS (1996) Persistent reovirus infections of L cells select mutations in viral attachment protein 61 that alter oligomer stability. J Virol 70:6598–6606PubMedGoogle Scholar
  79. Wyllie AH, Morris RG, Smith AL, Dunlop D (1984) Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J Pathol 142:67–77PubMedCrossRefGoogle Scholar
  80. Yonish-Rouach E (1996) The p53 tumour suppressor gene: a mediator of a GI growth arrest and of apoptosis. Experientia 52:1001–1007PubMedCrossRefGoogle Scholar
  81. Zamzami N, Susin SA, Marchetti P, Hirsh T, Gomez-Monterrey I, Castedo M, Guido K (1996) Mitochondrial control of nuclear apoptosis. J Exp Med 183:1533–1544PubMedCrossRefGoogle Scholar
  82. Zhivotovsky B, Burgess DH, Vanags DM, Orrenius S (1996) Involvement of cellular proteolytic machinery in apoptosis. Biochem Biophys Res Commun 230:481–488CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1998

Authors and Affiliations

  • S. M. Oberhaus
    • 1
    • 2
  • T. S. Dermody
    • 3
  • K. L. Tyler
    • 4
    • 5
  1. 1.Department of NeurologyUniversity of Colorado Health Sciences CenterDenverUSA
  2. 2.Department of Microbiology and ImmunologyEast Carolina University School of MedicineGreenvilleUSA
  3. 3.Departments of Pediatrics, and Microbiology and Immunology and Elizabeth B. Lamb Center for Pediatric ResearchVanderbilt University School of MedicineNashvilleUSA
  4. 4.Departments of Neurology, and Microbiology, Immunology, and MedicineUniversity of Colorado Health Sciences CenterDenverUSA
  5. 5.Neurology ServiceDenver Veterans Affairs Medical CenterDenverUSA

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