Advertisement

Cellular and Molecular Basis of the Protective Immune Response to Cytomegalovirus Infection

  • U. H. Koszinowski
  • M. Del Val
  • M. J. Reddehase
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 154)

Abstract

Cytomegalovirus (CMV) infection can occur throughout life. Similar to other herpesviruses, after primary infection CMV remains in the host in a latent state. Infection of the immunocompetent host does not cause clinical symptoms, whereas infection of the immunocompromised host can cause severe and even fatal disease. Morbidity and mortality associated with primary CMV infection or with reactivation from latency is common in immunosuppressed transplant recipients and in patients with immunodeficiency caused by HIV infection. CMV pneumonia is considered the immediate cause of death in these patients.

Keywords

Major Histocompatibility Complex Major Histocompatibility Complex Class Cytomegalovirus Infection Protective Immune Response Salivary Gland Tissue 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adorini L, Appella E, Doria G, Nagy ZA (1988) Mechanisms influencing the immunodominance of T cell determinants. J Exp Med 168: 2091–2104.PubMedCrossRefGoogle Scholar
  2. Ahmed R, Butler LD, Bhatti L (1988) T4+ T helper cell function in vivo: differential requirement for induction of antiviral cytotoxic T-cell and antibody responses. J Virol 62: 2102–2106.PubMedGoogle Scholar
  3. Allen PM, Matsueda GR, Evans RJ, Dunbar JB Jr, Marshall GR, Unanue ER (1987) Identification of the T cell and Ia contact residues of a T cell antigenic epitope. Nature 327: 713–715.PubMedCrossRefGoogle Scholar
  4. Bale JF, O’Neil ME, Giller R, Perlman S, Koszinowski UH (1987) Murine cytomegalovirus genomic material in marrow cells: relation to altered leukocyte counts during sublethal infection of mice. J Infect Dis 155:207–212.PubMedCrossRefGoogle Scholar
  5. Bernards R, Schrier PI, Houweling A, Bos JL, van der Eb AJ, Zijlstra M, Melief CJM (1983) Tumorigenicity of cells transformed by adenovirus type 12 by evasion of T-cell immunity. Nature 305: 776–779.PubMedCrossRefGoogle Scholar
  6. Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC (1987) Structure of the human class I histocompatibility antigen HLA-A2. Nature 329: 506–518.PubMedCrossRefGoogle Scholar
  7. Borysiewicz LK, Hickling JK, Graham S, Sinclair J, Cranage MP, Smith GL, Sissons JGP (1988) Human cytomegalovirus-specific cytotoxic T cells. Relative frequency of stage specific CTL recognizing the 72 kD immediate early protein and glycoprotein B expressed by recombinant vaccinia virus. J Exp Med 168:919–932.PubMedCrossRefGoogle Scholar
  8. Boshart M, Weber F, Jahn G, Dorsch-Häsler K, Fleckenstein B, Schaffner W (1985) A very strong enhancer is located upstream of an immediate early gene of human cytomegalovirus. Cell 41: 521–530.PubMedCrossRefGoogle Scholar
  9. Braun RW, Reiser HC (1986) Replication of human cytomegalovirus in human peripheral blood T cells. J Virol 60: 29–36.PubMedGoogle Scholar
  10. Brautigam AR, Dutko FJ, Olding LB, Oldstone MBA (1979) Pathogenesis of murine cytomegalovirus infection: the macrophage as a permissive cell for cytomegalovirus infection, replication and latency. J Gen Virol 44: 349–359.PubMedCrossRefGoogle Scholar
  11. Brody AR, Craighead JE (1974) Pathogenesis of pulmonary cytomegalovirus infection in im-munosuppressed mice. J Infect Dis 129: 677–689.PubMedCrossRefGoogle Scholar
  12. Bukowski JF, Woda BA, Habu S, Okumura K, Welsh RM (1983) Natural killer cell depletion enhances virus synthesis and virus-induced hepatitis in vivo. J Immunol 131: 1531–1537.PubMedGoogle Scholar
  13. Bukowski JF, Woda BA, Welsh RM (1984) Pathogenesis of murine cytomegalovirus infection in natural killer cell-depleted mice. J Virol 52: 119–128.PubMedGoogle Scholar
  14. Bukowski JF, Warner JF, Dennert G, Welsh RM (1985) Adoptive transfer studies demonstrating the antiviral effect of natural killer cells in vivo. J Exp Med 161: 40–52.PubMedCrossRefGoogle Scholar
  15. Buller RML, Holmes KL, Hügin A, Frederickson TN, Morse HC III (1987) Induction of cytotoxic T-cell responses in vivo in the absence of CD4 helper cells. Nature 328: 77–79.PubMedCrossRefGoogle Scholar
  16. Burgert HG, Kvist S (1985) An adenovirus type 2 glycoprotein blocks cell surface expression of human histocompatibility class I antigens. Cell 41: 987–997.PubMedCrossRefGoogle Scholar
  17. Carney WP, Hirsch MS (1981) Mechanism of immunosuppression in cytomegalovirus mononucleosis. II. Virus-monocyte interactions. J Infect Dis 144: 47–54.PubMedCrossRefGoogle Scholar
  18. Chong KT, Mims CA (1981) Murine cytomegalovirus particle types in relation to sources of virus and pathogenicity. J Gen Virol 57: 415–419.PubMedCrossRefGoogle Scholar
  19. Cobbold SP, Jayasuriya A, Nash A, Prospero TD, Waldmann H (1984) Therapy with monoclonal antibodies by elimination of T-cell subsets in vivo. Nature 312: 548–551.PubMedCrossRefGoogle Scholar
  20. Cole R, Kuttner AG (1926) A filterable virus present in the submaxillary glands of guinea pigs. J Exp Med 44: 855–873.PubMedCrossRefGoogle Scholar
  21. Craighead JE (1969) Immunologic response to cytomegalovirus infection in renal allograft recipients. Am J Epidemiol 90: 506–513.PubMedGoogle Scholar
  22. Davis MM, Bjorkman PJ (1988) T-cell antigen receptor genes and T-cell recognition. Nature 334: 395–402.PubMedCrossRefGoogle Scholar
  23. Del Val M, Volkmer H, Rothbard JB, Jonjić S, Messerle M, Schickedanz J, Reddehase MJ, Koszinowski UH (1988) Molecular basis for cytolytic T lymphocyte recognition of the murine cytomegalovirus immediate-early protein pp89. J Virol 62: 3965–3972.PubMedGoogle Scholar
  24. Del Val M, Münch K, Reddehase MJ, Koszinowski UH (1989) Presentation of CMV immediate-early antigen to cytolytic T lymphocytes is selectively prevented by viral genes expressed in the early phase. Cell 58: 305–315.PubMedCrossRefGoogle Scholar
  25. Dorsch-Häsler K, Keil GM, Weber F, Jasin M, Schaffner W, Koszinowski UH (1985) A long and complex enhancer activates transcription of the gene coding for the highly abundant immediate early mRNA in murine cytomegalovirus. Proc Natl Acad Sci USA 82: 8325–8329.PubMedCrossRefGoogle Scholar
  26. Drew WL (1988) Cytomegalovirus infection in patients with AIDS. J Infect Dis 158: 449–456.PubMedCrossRefGoogle Scholar
  27. Drew WL, Mintz L (1984) What is the role of cytomegalovirus in AIDS? Ann NY Acad Sci 439: 320–324.CrossRefGoogle Scholar
  28. Ebeling A, Keil GM, Knust E, Koszinowski UH (1983) Molecular cloning and physical mapping of murine cytomegalovirus DNA. J Virol 47: 421–433.PubMedGoogle Scholar
  29. Einhorn L, Öst Å (1984) Cytomegalovirus infection of human blood cells. J Infect Dis 149: 207–214.PubMedCrossRefGoogle Scholar
  30. Eizura Y, Minamishima Y (1979) Co-variation of pathogenicity and antigenicity in murine cytomegalovirus. Microbiol Immunol 23: 559–564.Google Scholar
  31. Emanuel D, Cunningham I, Jules-Elysee K, Brochstein JA, Kernan NA, Laver J, Stover D, et al. (1988) Cytomegalovirus pneumonia after bone marrow transplantation successfully treated with the combination of ganciclovir and high-dose intravenous immune globulin. Ann Intern Med 109: 777–782.PubMedGoogle Scholar
  32. Ermak TH, Steger HJ (1988) CD4-CD8- T cells: amplification in spleens of mice following in vivo treatment with monoclonal antibody anti-L3T4. Eur J Immunol 18: 231–235.PubMedCrossRefGoogle Scholar
  33. Gammon G, Shastri N, Cogswell J, Willbur S, Sadegh-Nasseri S, Krzych U, Miller A, Sercarz EE (1987) The choice of T cell epitopes utilized on a protein antigen depends on multiple factors distant from as well as at the determinant site. Immunol Rev 98: 53–74.PubMedCrossRefGoogle Scholar
  34. Gardner MB, Officer JE, Parker J, Estes JD, Rongey RW (1974) Induction of disseminated virulent cytomegalovirus infection by immunosuppression of naturally chronically infected wild mice. Infect Immun 10: 966–969.PubMedGoogle Scholar
  35. Germain RN (1986) The ins and outs of antigen processing and presentation. Nature 332: 687–689.CrossRefGoogle Scholar
  36. Germain RN (1988) Antigen processing and CD4+ T cell depletion in AIDS. Cell 54: 441–444.PubMedCrossRefGoogle Scholar
  37. Gooding LR (1982) Characterization of a progressive tumor from C3H fibroblasts transformed in vitro with SV40 virus. Immunoresistance in vivo correlates with phenotypic loss of H-2Kk. J Immunol 129:1306–1312.PubMedGoogle Scholar
  38. Goronzy J, Weyand CM, Fathman CG (1986) Long-term humoral unresponsiveness in vivo, induced by treatment with monoclonal antibody against L3T4. J Exp Med 164: 911–925.PubMedCrossRefGoogle Scholar
  39. Heber-Katz E, Dietzschold B (1986) Immune response to synthetic herpes simplex virus peptides: the feasibility of a vaccine. Curr Top Microbiol Immunol 130: 51–64.PubMedCrossRefGoogle Scholar
  40. Henson D, Strano AJ (1972) Mouse cytomegalovirus: necrosis of infected and morphologically normal submaxillary gland acinar cells during termination of chronic infection. Am J Pathol 68: 183–202.PubMedGoogle Scholar
  41. Henson D, Smith RD, Gehrke J (1966) Nonfatal mouse cytomegalovirus hepatitis: combined morphological, virological, and immunological observations. Am J Pathol 49: 871–888.PubMedGoogle Scholar
  42. Ho M (1980) Role of specific cytotoxic lymphocytes in cellular immunity against murine cytomegalovirus. Infect Immun 27: 767–776.PubMedGoogle Scholar
  43. Ho M, Ashman RB (1979) Development in vitro of cytotoxic lymphocytes against murine cytomegalovirus. Aust J Exp Biol Med Sci 57: 425–428.PubMedCrossRefGoogle Scholar
  44. Hudson JB, Misra V, Mosmann TR (1976) Properties of the multicapsid virions of murine cytomegalovirus. Virology 72: 224–234.PubMedCrossRefGoogle Scholar
  45. Jennings SR, Rice PL, Kloszewski ED, Anderson RW, Thompson DL, Tevethia SS (1985) Effect of herpes simplex virus types 1 and 2 on surface expression of class I major histocompatibility complex antigens on infected cells. J Virol 56: 757–766.PubMedGoogle Scholar
  46. Jonjić S, del Val M, Keil GM, Reddehase MJ, Koszinowski UH (1988) A nonstructural viral protein expressed by a recombinant vaccinia virus protects against lethal cytomegalovirus infection. J Virol 62: 1653–1658.PubMedGoogle Scholar
  47. Jonjić S, Mutter W, Weiland F, Reddehase MJ, Koszinowski UH (1989) Site-restricted persistent cytomegalovirus infection after selective long-term depletion of CD4-positive T lymphocytes. J Exp Med 169: 1199–1212.PubMedCrossRefGoogle Scholar
  48. Jordan MC (1978) Interstitial pneumonia and subclinical infection after intranasal inoculation of murine cytomegalovirus. Infect Immun 21: 275–280.PubMedGoogle Scholar
  49. Jordan MC, Mar VL (1982) Spontaneous activation of latent cytomegalovirus from murine spleen expiants. Role of lymphocytes and macrophages in release and replication of virus. J Clin Invest 70:762–768.PubMedCrossRefGoogle Scholar
  50. Jordan MC, Shanley JD, Stevens JG (1977) Immunosuppression reactivates and disseminates latent murine cytomegalovirus. J Gen Virol 37: 419–423.PubMedCrossRefGoogle Scholar
  51. Jordan MC, Takagi JL, Stevens JG (1982) Activation of latent murine cytomegalovirus in vivo and in vitro: a pathogenic role for acute infection. J Infect Dis 145: 699–705.PubMedCrossRefGoogle Scholar
  52. Kapasi K, Rice GPA (1988) Cytomegalovirus infection of peripheral blood mononuclear cells: effects on interleukin-1 and-2 production and responsiveness. J Virol 62: 3603–3607.PubMedGoogle Scholar
  53. Keil GM, Ebeling-Keil A, Koszinowski UH (1984) Temporal regulation of murine cytomegalovirus transcription and mapping of viral RNA synthesized at immediate early times after infection. J Virol 50:784–795.PubMedGoogle Scholar
  54. Keil GM, Ebeling-Keil A, Koszinowski UH (1987a) Immediate-early genes of murine cytomegalovirus: location, transcripts, and translation products. J Virol 61: 526–533.PubMedGoogle Scholar
  55. Keil GM, Ebeling-Keil A, Koszinowski UH (1987b) Sequence and structural organization of murine cytomegalovirus immediate-early gene 1. J Virol 61: 1901–1908.PubMedGoogle Scholar
  56. Keil GM, Fibi MR, Koszinowski UH (1985) Characterization of the major immediate-early polypeptides encoded by murine cytomegalovirus. J Virol 54: 422–428.PubMedGoogle Scholar
  57. Klatzmann D, Barre-Sinoussi F, Nugeyre MT, Dauguet C, Valmer E, Griscelli C, Brun-Vezinet F, et al. (1984) Selective tropism of lymphoadenopathy-associated virus (LAV) for helper-inducer T lymphocytes. Science 225: 59–63.PubMedCrossRefGoogle Scholar
  58. Koszinowski UH, Keil GM, Volkmer H, Fibi MR, Ebeling-Keil A, Münch K (1986) The 89,000-Mr murine cytomegalovirus immediate-early protein activates gene transcription. J Virol 58: 59–66.PubMedGoogle Scholar
  59. Koszinowski UH, Keil GM, Schwarz H, Schickedanz J, Reddehase MJ (1987a) A nonstructural polypeptide encoded by immediate-early transcription unit 1 of murine cytomegalovirus is recognized by cytolytic T lymphocytes. J Exp Med 166: 289–294.PubMedCrossRefGoogle Scholar
  60. Koszinowski UH, Reddehase MJ, Keil GM, Schickedanz J (1987b) Host immune response to cytomegalovirus: products of transfected viral immediate-early genes are recognized by cloned cytolytic T lymphocytes. J Virol 61: 2054–2058.PubMedGoogle Scholar
  61. Kuttner AG (1927) Further studies concerning the filterable virus present in the submaxillary glands of guinea pigs. J Exp Med 46: 935–956.PubMedCrossRefGoogle Scholar
  62. Kuttner AG, Wang S-H (1934) The problem of the significance of the inclusion bodies found in the salivary glands of infants, and the occurrence of inclusion bodies in the submaxillary glands of hamsters, white mice, and wild rats (Peiping). J Exp Med 60: 773–791.PubMedCrossRefGoogle Scholar
  63. Loh L, Hudson JB (1982) Murine cytomegalovirus-induced immunosuppression. Infect Immun 36: 89–95.PubMedGoogle Scholar
  64. Lussier G, Berthiaume L, Payment P (1974) Electron microscopy of murine cytomegalovirus: development of the virus in vivo and in vitro. Arch Gesamte Virusforsch 46: 269–280.PubMedCrossRefGoogle Scholar
  65. MacDonald HR, Blanc D, Less RK, Sordat B (1986) Abnormal distribution of T cell subsets in athymic mice. J Immunol 136: 4337–4339.PubMedGoogle Scholar
  66. Magli MC, Iscove NN, Odartchenko N (1982) Transient nature of early haematopoietic spleen colonies. Nature 295: 527–529.PubMedCrossRefGoogle Scholar
  67. Marrack P, Kappler J (1987) The T-cell receptor. Science 238: 1073–1079.PubMedCrossRefGoogle Scholar
  68. Masucci MG, Torsteinsdottir S, Colombani J, Brautbar C, Klein E, Klein G (1987) Down-regulation of class I HLA antigens and of the Epstein-Barr virus-encoded latent membrane protein in Burkitt lymphoma lines. Proc Natl Acad Sci USA 84: 4567–4571.PubMedCrossRefGoogle Scholar
  69. Matis LA, Cron R, Bluestone JA (1987) Major histocompatibility complex-linked specificity of γ/δ receptor-bearing T lymphocytes. Nature 330: 262–264.PubMedCrossRefGoogle Scholar
  70. Mayo DR, Armstrong JA, Ho M (1977) Reactivation of murine cytomegalovirus by cyclophosphamide. Nature 267: 721–723.PubMedCrossRefGoogle Scholar
  71. McCordock HA, Smith MG (1936) The visceral lesions produced in mice by the salivary gland virus of mice. J Exp Med 63: 303–310.PubMedCrossRefGoogle Scholar
  72. Mercer JA, Spector DH (1986) Pathogenesis of acute murine cytomegalovirus infection in resistant and susceptible strains of mice. J Virol 57: 497–504.PubMedGoogle Scholar
  73. Mercer JA, Wiley CA, Spector DH (1988) Pathogenesis of murine cytomegalovirus infection: identification of infected cells in the spleen during acute and latent infections. J Virol 62: 987–997.PubMedGoogle Scholar
  74. Meyers JD (1984) Cytomegalovirus infection following marrow transplantation: risk, treatment, and prevention. Birth Defects 20: 101–117.PubMedGoogle Scholar
  75. Mims CA, Gould J (1978) The role of macrophages in mice infected with murine cytomegalovirus. J Gen Virol 41: 143–153.PubMedCrossRefGoogle Scholar
  76. Moingeon P, Jitsukawa S, Faure F, Troalen F, Triebel F, Graziani M, Forestier F, et al. (1987) A γ-chain complex forms a functional receptor on cloned human lymphocytes with natural killer-like activity. Nature 325: 723–726.PubMedCrossRefGoogle Scholar
  77. Moore MW, Carbone FR, Bevan MJ (1988) Introduction of soluble protein into the class I pathway of antigen processing and presentation. Cell 54: 777–785.PubMedCrossRefGoogle Scholar
  78. Münch K, Keil GM, Messerle M, Koszinowski UH (1988) Interaction of the 89K murine cytomegalovirus immediate-early protein with core histones. Virology 163: 405–412.PubMedCrossRefGoogle Scholar
  79. Mutter W, Reddehase MJ, Busch FW, Bühring H-J, Koszinowski UH (1988) Failure in generating hemopoietic stem cells is the primary cause of death from cytomegalovirus disease in the immunocompromised host. J Exp Med 167: 1645–1658.PubMedCrossRefGoogle Scholar
  80. Neiman P, Wasserman PB, Wentworth BB, Kao GF, Lerner KG, Storb R, Buckner CD, et al. (1973) Interstitial pneumonia and cytomegalovirus infection as complications of human marrow transplantation. Transplantation 15: 478–485.PubMedCrossRefGoogle Scholar
  81. Olding LB, Jensen FC, Oldstone MBA (1975) Pathogenesis of cytomegalovirus infection. I. Activation of virus from bone marrow-derived lymphocytes by in vitro allogenic reaction. J Exp Med 141: 561–571.PubMedCrossRefGoogle Scholar
  82. Osborn JE, Shahidi NT (1973) Thrombocytopenia in murine cytomegalovirus infection. J Lab Clin Med 81:53–63.PubMedGoogle Scholar
  83. Osborn JE, Walker DL (1971) Virulence and attenuation of murine cytomegalovirus. Infect Immun 3: 228–236.PubMedGoogle Scholar
  84. Petursson SR, Chervenick PA, Wu B (1984) Megakaryocytopoiesis and granulopoiesis after murine cytomegalovirus infection. J Lab Clin Med 104: 381–390.PubMedGoogle Scholar
  85. Price P, Winter JG, Nikoletti S, Hudson JB, Shellam GR (1987) Functional changes in murine macrophages infected with cytomegalovirus relate to H-2 determined sensitivity to infection. J Virol 61:3602–3606.PubMedGoogle Scholar
  86. Quinnan GV Jr, Manischewitz JF (1987) Genetically determined resistance to lethal murine cytomegalovirus infection is mediated by interferon-dependent and-independent restriction of virus replication. J Virol 61:1875–1881.PubMedGoogle Scholar
  87. Quinnan GV, Manschiewitz JE, Ennis FA (1978) Cytotoxic T lymphocyte response to murine cytomegalovirus infection. Nature 273: 541–543.PubMedCrossRefGoogle Scholar
  88. Quinnan GV, Kirmani N, Rook AH, Manischewitz J, Jackson L, Moreschi G, Santos GW, et al. (1982) HLA-restricted T-lymphocyte and non T-lymphocyte cytotoxic responses correlate with recovery from cytomegalovirus infection in bone-marrow-transplant recipients. N Engl J Med 307: 7–13.PubMedCrossRefGoogle Scholar
  89. Reddehase MJ, Koszinowski UH (1984) Significance of herpesvirus immediate early gene expression in cellular immunity to cytomegalovirus infection. Nature 312: 369–371.PubMedCrossRefGoogle Scholar
  90. Reddehase MJ, Keil GM, Koszinowski UH (1984a) The cytolytic T lymphocyte response to the murine cytomegalovirus. I. Distinct maturation stages of cytolytic T lymphocytes constitute the cellular immune response during acute infection of mice with the murine cytomegalovirus. J Immunol 132:482–489.PubMedGoogle Scholar
  91. Reddehase MJ, Keil GM, Koszinowski UH (1984b) The cytolytic T lymphocyte response to the murine cytomegalovirus. II. Detection of virus replication stage-specific antigens by separate populations of in vivo active cytolytic T lymphocyte precursors. Eur J Immunol 14: 56–61.PubMedCrossRefGoogle Scholar
  92. Reddehase MJ, Weiland F, Münch K, Jonjić S, Lüske A, Koszinowski UH (1985) Interstitial murine cytomegalovirus pneumonia after irradiation: characterization of cells that limit viral replication during established infection of the lungs. J Virol 55: 264–273.PubMedGoogle Scholar
  93. Reddehase MJ, Bühring H-J, Koszinowski UH (1986a) Cloned long-term cytolytic T-lymphocyte line with specificity for an immediate-early membrane antigen of murine cytomegalovirus. J Virol 57: 408–412.PubMedGoogle Scholar
  94. Reddehase MJ, Fibi MR, Keil GM, Koszinowski UH (1986b) Late-phase expression of a murine cytomegalovirus immediate-early antigen recognized by cytolytic T lymphocytes. J Virol 60: 1125–1129.PubMedGoogle Scholar
  95. Reddehase MJ, Mutter W, Koszinowski UH (1987a) In vivo application of recombinant interleukin-2 in the immunotherapy of established cytomegalovirus infection. J Exp Med 165: 650–656.PubMedCrossRefGoogle Scholar
  96. Reddehase MJ, Mutter W, Münch K, Bühring H-J, Koszinowski UH (1987b) CD8-positive T lymphocytes specific for murine cytomegalovirus immediate-early antigens mediate protective immunity. J Virol 61: 3102–3108.PubMedGoogle Scholar
  97. Reddehase MJ, Zawatzky R, Weiland F, Bühring H-J, Mutter W, Koszinowski UH (1987c) Stable expression of clonal specificity in murine cytomegalovirus-specific large granular lymphoblast lines propagated long-term in recombinant interleukin-2. Immunobiology 174: 420–431.PubMedCrossRefGoogle Scholar
  98. Reddehase MJ, Jonjić S, Weiland F, Mutter W, Koszinowski UH (1988) Adoptive immunotherapy of murine cytomegalovirus adrenalitis in the immunocompromised host: CD4-helper-independent antiviral function of CD8-positive memory T lymphocytes derived from latently infected donors. J Virol 62: 1061–1065.PubMedGoogle Scholar
  99. Reddehase MJ, Rothbard JB, Koszinowski UH (1989) A pentapeptide as minimal antigenic determinant for MHC class I-restricted T lymphocytes. Nature 337: 651–653.PubMedCrossRefGoogle Scholar
  100. Reed EC, Bowden RA, Dandliker PS, Lilleby KE, Meyers JD (1988) Treatment of cytomegalovirus pneumonia with ganciclovir and intravenous cytomegalovirus immunoglobulin in patients with bone marrow transplants. Ann Intern Med 109: 783–788.PubMedGoogle Scholar
  101. Reiser HC, Kühn J, Doerr HW, Kirchner H, Munk K, Braun RW (1986) Human cytomegalovirus replicates in primary human bone marrow cells. J Gen Virol 67: 2595–2604.PubMedCrossRefGoogle Scholar
  102. Rice GPA, Schrier RD, Oldstone MBA (1984) Cytomegalovirus infects human lymphocytes and monocytes: virus expression is restricted to immediate-early gene products. Proc Natl Acad Sci USA 81:6134–6138.PubMedCrossRefGoogle Scholar
  103. Rodgers BC, Scott DM, Mundin J, Sissons JGP (1985) Monocyte-derived inhibitor of IL-1 induced by human CMV. J Virol 55: 527–532.PubMedGoogle Scholar
  104. Rothbard JB, Taylor RW (1988) A sequence pattern common to T cell epitopes. EMBO J 7: 93–100.PubMedGoogle Scholar
  105. Rothbard JB, Lechler RI, Howland K, Bal V, Eckels DD, Sekaly R, Long EO, et al. (1988) Structural model of HLA-DR1 restricted T cell antigen recognition. Cell 52: 515–523.PubMedCrossRefGoogle Scholar
  106. Sattentau QJ, Weiss RA (1988) The CD4 antigen: physiological ligand and HIV receptor. Cell 52: 631–633.PubMedCrossRefGoogle Scholar
  107. Schickedanz J, Philipson L, Ansorge W, Pepperkok R, Klein R, Koszinowski UH (1988) The 89,000-Mr murine cytomegalovirus immediate-early protein stimulates c-fos expression and cellular DNA synthesis. J Virol 62: 3341–3347.PubMedGoogle Scholar
  108. Schrier RD, Nelson JA, Oldstone MBA (1985) Detection of human cytomegalovirus in peripheral blood lymphocytes in a natural infection. Science 230: 1048–1051.PubMedCrossRefGoogle Scholar
  109. Schrier RD, Rice GPA, Oldstone MBA (1986) Suppression of NK activity and T cell proliferation induced by fresh isolates of CMV. J Infect Dis 153: 1084–1091.PubMedCrossRefGoogle Scholar
  110. Selgrade MK, Ahmed A, Sell KW, Gershwin ME, Steinberg AD (1976) Effect of murine cytomegalovirus on the in vitro responses of T and B cells to mitogens. J Immunol 116: 1459–1465.PubMedGoogle Scholar
  111. Selgrade MK, Nedrud JG, Collier AM, Gardner DE (1981) Effects of cell source, mouse strain, and immunosuppressive treatment on production of virulent and attenuated murine cytomegalovirus. Infect Immun 33: 840–847.PubMedGoogle Scholar
  112. Selgrade MK, Collier AM, Saxton L, Daniels MJ, Graham JA (1984) Comparison of the pathogenesis of murine cytomegalovirus in lung and liver following intraperitoneal or intratracheal infection. J Gen Virol 65: 515–523.PubMedCrossRefGoogle Scholar
  113. Sethi KK, Brandis H (1979) Induction of virus specific and H-2 restricted cytotoxic T cells by UV inactivated murine cytomegalovirus. Arch Virol 60: 227–238.PubMedCrossRefGoogle Scholar
  114. Shanley JD (1987) Modification of acute murine cytomegalovirus adrenal gland infection by adoptive spleen cell transfer. J Virol 61: 23–28.PubMedGoogle Scholar
  115. Shanley JD, Pesanti EL (1985) The relation of viral replication to interstitial pneumonitis in murine cytomegalovirus lung infection. J Infect Dis 151: 454–458.PubMedCrossRefGoogle Scholar
  116. Shanley JD, Pesanti EL (1986) Murine cytomegalovirus adrenalitis in athymic nude mice. Arch Virol 88: 27–35.PubMedCrossRefGoogle Scholar
  117. Shanley JD, Jordan MC, Cook ML, Stevens JG (1979) Pathogenesis of reactivated latent murine cytomegalovirus infection. Am J Pathol 95: 67–77.PubMedGoogle Scholar
  118. Shellam GR, Allan JE, Papadimitriou JM, Bancroft GJ (1981) Increased susceptibility to cytomegalovirus infection in beige mutant mice. Proc Natl Acad Sci USA 78: 5104–5108.PubMedCrossRefGoogle Scholar
  119. Sinigaglia F, Guttinger M, Kilgus J, Doran DM, Matile H, Etlinger H, Trzeciak A et al. (1988) A malaria T-cell epitope recognized in association with most mouse and human MHC class II molecules. Nature 336: 778–780.PubMedCrossRefGoogle Scholar
  120. Smith MG (1954) Propagation of salivary gland virus of the mouse in tissue cultures. Proc Soc Exp Biol Med 86: 435–440.PubMedGoogle Scholar
  121. Starr SE, Allison AC (1977) Role of T lymphocytes in recovery from murine cytomegalovirus infection. Infect Immun 17: 458–462.PubMedGoogle Scholar
  122. Stenberg RM, Thomsen DR, Stinski MF (1984) Structural analysis of the major immediate early gene of human cytomegalovirus. J Virol 49: 190–199.PubMedGoogle Scholar
  123. Stenberg RM, Witte PR, Stinski MF (1985) Multiple spliced and unspliced transcripts from human cytomegalovirus immediate early region 2 and evidence for a common initiation site within immediate early region 1. J Virol 56: 665–675.PubMedGoogle Scholar
  124. Sullivan KM (1987) Immunoglobulin therapy in bone marrow transplantation. Am J Med [Suppl4A] 83: 34–45.CrossRefGoogle Scholar
  125. Tegtmeyer PJ, Craighead JE (1968) Infection of adult mouse macrophages in vitro with cytomegalovirus. Proc Soc Exp Biol Med 129: 690–694.PubMedGoogle Scholar
  126. Townsend ARM, Rothbard J, Gotch FM, Bahadur G, Wraith D, McMichael AJ (1986) The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell 44: 959–968.PubMedCrossRefGoogle Scholar
  127. Townsend ARM, Bastin J, Gould K, Brownlee G, Andrew M, Coupar B, Boyle D, et al. (1988) Defective presentation to class I-restricted cytotoxic T lymphocytes in vaccinia-infected cells is overcome by enhanced degradation of antigen. J Exp Med 168: 1211–1224.PubMedCrossRefGoogle Scholar
  128. Volkmer H, Bertholet C, Jonjić S, Wittek R, Koszinowski UH (1987) Cytolytic T lymphocyte recognition of the murine cytomegalovirus nonstructural immediate-early protein pp89 expressed by recombinant vaccinia virus. J Exp Med 166: 668–677.PubMedCrossRefGoogle Scholar
  129. Wabuke-Bunoti MAN, Fan DP, Braciale TJ (1981) Stimulation of anti-influenza cytolytic T lymphocytes by CnBr cleavage fragments of the viral hemagglutinin. J Immunol 127: 1122–1125.PubMedGoogle Scholar
  130. Weiland F, Keil GM, Reddehase MJ, Koszinowski UH (1986) Studies on the morphogenesis of murine cytomegalovirus. Intervirology 26: 192–201.PubMedCrossRefGoogle Scholar
  131. Weller TH, Hanshaw JB, Scott DE (1960) Serological differentiation of viruses responsible for cytomegalic inclusion disease. Virology 12: 130–132.PubMedCrossRefGoogle Scholar
  132. Wise TG, Manischewitz JF, Quinnan GV, Aulakh GS, Ennis FA (1979) Latent cytomegalovirus infection of BALB/c mouse spleens detected by an explant culture technique. J Gen Virol 44: 551–556.PubMedCrossRefGoogle Scholar
  133. Wofsy D, Mayes DC, Woodcock J, Seaman WE (1985) Inhibition of humoral immunity in vivo by monoclonal antibody to L3T4: studies with soluble antigens in intact mice. J Immunol 135: 1698–1701.PubMedGoogle Scholar
  134. Zinkernagel RM, Doherty PC (1979) MHC-restricted cytotoxic T cells: studies on the biological role of polymorphic major transplantation antigens determining T cell restriction specificity, function and responsiveness. Adv Immunol 27: 52–177.Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1990

Authors and Affiliations

  • U. H. Koszinowski
    • 1
  • M. Del Val
    • 1
  • M. J. Reddehase
    • 1
  1. 1.Department of Virology, Institute for MicrobiologyUniversity of UlmUlmGermany

Personalised recommendations