Murine cytomegalovirus infection inhibits IFNγ-induced MHC class ii expression on macrophages. The role of type I interferon

Virology

Volumn 241, Issue 2, 1998, Pages 331-344

  Heise, Mark T ^a   Pollock, Jessica L ^a   O'Guin, Andrew ^a   Barkon, Melissa L ^a   Bromley, Shannon ^a   Virgin IV, Herbert W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON RECEPTOR; INTERCELLULAR ADHESION MOLECULE 1; INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; RECOMBINANT GAMMA INTERFERON; THIOGLYCOLIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; BONE MARROW; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; FEMALE; MACROPHAGE ACTIVATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; SCID MOUSE;

ANIMALIA; CYTOMEGALOVIRUS; DNA VIRUSES; MAIZE CHLOROTIC MOTTLE VIRUS; MOUSE CYTOMEGALOVIRUS 1; MURINAE;

EID: 0032520145     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1006/viro.1997.8969     Document Type: Article

References (70)

1. Allan J. E., Shellam G. R. Characterization of interferon induction in mice of resistant and susceptible strains during murine cytomegalovirus infection. J. Gen. Virol. 66:1985;1105-1112.
2. Austyn J. M., Gordon S. F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur. J. Immunol. 11:1981;805-815.
3. Bancroft G. J., Bosma M. J., Bosma G. C., Unanue E. R. Regulation of macrophage Ia expression in mice with severe combined immunodeficiency: Induction of Ia expression by a T cell-independent mechanism. J. Immunol. 137:1986;4-9.
4. Bancroft G. J., Shellam G. R., Chalmer J. E. Genetic influences on the augmentation of natural killer (NK) cells during murine cytomegalovirus infection: Correlation with patterns of resistance. J. Immunol. 126:1981;988-994.
5. Beersma M. F. C., Bijlmakers M. J. E., Ploegh H. L. Human cytomegalovirus down-regulates HLA class I expression by reducing the stability of class I H chains. J. Immunol. 151:1993;4455-4464.
6. Beller D. I., Ho K. Regulation of macrophage populations. V. Evaluation of the control of macrophage Ia expression in vitro. J. Immunol. 129:1982;971-976.
7. Bixler G. S., Booss J. Adherent spleen cells from mice acutely infected with cytomegalovirus suppress the primary antibody response in vitro. J. Immunol. 127:1981;1294-1299.
8. Brautigam A. R., Dutko F. J., Olding L. B., Oldstone M. B. Pathogenesis of murine cytomegalovirus infection: The macrophage as a permissive cell for cytomegalovirus infection, replication, and latency. J. Gen. Virol. 44:1979;349-359.
9. Britt W. J., Alford C. A. Fields Virology. 1996;Lippincott-Raven, Philadelphia. p. 2493-2523.
10. Bukowski J. F., Woda B. A., Welsh R. M. Pathogenesis of murine cytomegalovirus infection in natural killer cell-depleted mice. J. Virol. 52:1984;119-128.
11. Campbell A. E., Slater J. S. Down-regulation of major histocompatibility complex class I synthesis by murine cytomegalovirus early gene expression. J. Virol. 68:1994;1805-1811.
12. Chong K. T., Gresser I., Mims C. A. Interferon as a defense mechanism in mouse cytomegalovirus infection. J. Gen. Virol. 64:1983;461-464.
13. Collins T. M., Quirk M. R., Jordan M. C. Biphasic viremia and viral gene expression in leukocytes during acute cytomegalovirus infection of mice. J. Virol. 68:1994;6305-6311.
14. Cousens L. P., Orange J. S., Su H. C., Biron C. A. Interferon-alpha/beta inhibition of interleukin 12 and interferon-gamma production in vitro and endogenously during viral infection. Proc. Natl. Acad. Sci. USA. 94:1997;634-639.
15. Custer R. P., Bosma G. C., Bosma M. J. Severe combined immunodeficiency (SCID) in the mouse. Pathology, reconstitution, neoplasms. Am. J. Pathol. 120:1985;464-477.
16. Del Val M., Hengel H., Hacker H., Hartlaub U., Ruppert T., Lucin P., Koszinowski U. H. Cytomegalovirus prevents antigen presentation by blocking the transport of peptide-loaded major histocompatibility complex class I molecules into the medial-Golgi compartment. J. Exp. Med. 176:1992;729-738.
17. Eron J. J., Gorczyca P., Kaplan J. C., D'Aquila R. T. Susceptibility testing by polymerase chain reaction DNA quantitation: A method to measure drug resistance of human immunodeficiency virus type 1 isolates. Proc. Natl. Acad. Sci. USA. 89:1992;3241-3245.
18. Fennie E. H., Lie Y. S., Low M. A., Gribling P., Anderson K. P. Reduced mortality in murine cytomegalovirus infected mice following prophylactic murine interferon-gamma treatment. Antiviral Res. 10:1988;27-39.
19. Fischer H.-G., Frosch S., Reske K., Reske-Kunz A. B. Granulocyte-macrophage colony-stimulating factor activates macrophages derived from bone marrow cultures to synthesis of MHC class II molecules and to augmented antigen presentation function. J. Immunol. 141:1988;3882-3888.
20. Fish K. N., Britt W., Nelson J. A. A novel mechanism for persistence of human cytomegalovirus in macrophages. J. Virol. 70:1996;1855-1862.
21. Fish K. N., Depto A. S., Moses A. V., Britt W., Nelson J. A. Growth kinetics of human cytomegalovirus are altered in monocyte-derived macrophages. J. Virol. 69:1995;3737-3743.
22. Gilbert M. J., Riddell S. R., Li C.-R., Greenberg P. D. Selective interference with class I major histocompatability complex presentation of the major immediate-early protein following infection with human cytomegalovirus. J. Virol. 67:1993;3461-3469.
23. Gresser I., Tovey M. G., Bandu M.-T., Maury C., Brouty-Boye D. Role of interferon in the pathogenesis of virus diseases in mice as demonstrated by the use of anti-interferon serum I. Rapid evolution of encephalomyocarditis virus infection. J. Exp. Med. 144:1976;1305-1315.
24. Grundy J. E., Trapman J., Allan J. E., Shellam G. R., Melief C. J. Evidence for a protective role of interferon in resistance to murine cytomegalovirus and its control by non-H-2-linked genes. Infect. Immun. 37:1982;143-150.
25. Hamilton J. R., Overall J. C. Synergistic infection with murine cytomegalovirus andPseudomonas aeruginosa. J. Infect. Dis. 137:1978;775-782.
26. Hamilton J. R., Overall J. C., Glasgow L. A. Synergistic effect on mortality in mice with murine cytomegalovirus infection andPseudomonas aeruginosa, Staphlococcus aureus,Candida albicans. Infect. Immun. 14:1976;982-989.
27. Heise M. T., Virgin H. W. The T cell independent role of IFN-gamma and TNF-alpha in macrophage activation during murine cytomegalovirus and herpes simplex virus infection. J. Virol. 69:1995;904-909.
28. Ibanez C. E., Schrier R., Ghazal P., Wiley C., Nelson J. A. Human cytomegalovirus productively infects primary differentiated macrophages. J. Virol. 65:1991;6581-6588.
29. Inaba K., Kitaura M., Kato T., Watanabe Y., Kawade Y., Muramatsu S. Contrasting effect of alfa/beta- and gama-interferons on expression of macrophage Ia antigens. J. Exp. Med. 163:1986;1030-1035.
30. Jones T. R., Hanson L. K., Sun L., Slater J. S., Stenberg R. M., Campbell A. E. Multiple independent loci within the human cytomegalovirus unique short region down-regulate expression of major histocompatibility complex class I heavy chains. J. Virol. 69:1995;4830-4841.
31. Jonjic S., Mutter W., Weiland F., Reddehase M. J., Koszinowski U. H. Site-restricted persistent cytomegalovirus infection after selective long-term depletion of CD4+ T lymphocytes. J. Exp. Med. 169:1989;1199-1212.
32. Jonjic S., Pavic I., Lucin P., Rukavina D., Koszinowski U. H. Efficacious control of cytomegalovirus infection after long-term depletion of CD8+ T lymphocytes. J. Virol. 64:1990;5457-5464.
33. Kapasi K., Rice G. P. Role of the monocyte in cytomegalovirus-mediated immunosuppression in vitro. J. Infect. Dis. 154:1986;881-884.
34. Keil G. M., Ebeling-Keil A., Koszinowski U. H. Temporal regulation of murine cytomegalovirus transcription and mapping of viral RNA synthesized at immediate early times after infection. J. Virol. 50:1984;784-795.
35. Kelsey D. K., Olsen G. A., Overall J. C., Glasgow L. A. Alteration of host defense mechanisms by murine cytomegalovirus infection. Infect. Immun. 18:1977;754-760.
36. Kondo K., Kaneshima H., Mocarski E. S. Human cytomegalovirus latent infection of granulocyte-macrophage progenitors. Proc. Natl. Acad. Sci. USA. 91:1994;11879-11883.
37. Lathey J. L., Spector S. A. Unrestricted replication of human cytomegalovirus in hydrocortisone-treated macrophages. J. Virol. 65:1991;6371-6375.
38. Lindahl-Magnusson P., Leary P., Gresser I. Interferon inhibits DNA synthesis induced in mouse lymphocyte suspensions by phytohaemagglutinin or by allogeneic cells. Nature New Biol. 237:1972;120-121.
39. Loh L., Hudson J. B. Murine cytomegalovirus-induced immunosuppression. Infect. Immun. 36:1982;89-95.
40. Lucin P., Pavic I., Polic B., Jonjic S., Koszinowski U. H. Gamma interferon-dependent clearance of cytomegalovirus infection in salivary glands. J. Virol. 66:1992;1977-1984.
41. Maciejewski J. P., Bruening E. E., Donahue R. E., Mocarski E. S., Young N. S., St Jeor S. C. Infection of hematopoietic progenitor cells by human cytomegalovirus. Blood. 80:1992;170-178.
42. Maciejewski J. P., Bruening E. E., Donahue R. E., Sellers S. E., Carter C., Young N. S., St Jeor S. Infection of mononucleated phagocytes with human cytomegalovirus. Virology. 195:1993;327-336.
43. Minton E. J., Tysoe C., Sinclair J. H., Sissons J. P. G. Human cytomegalovirus infection of the monocyte/macrophage lineage in bone marrow. J. Virol. 68:1994;4017-4021.
44. Muller U., Steinhoff S., Reis L. F. L., Hemmi S., Pavlovic J., Zinkernagel R. M., Aguet M. Functional role of type I and type II interferons in antiviral defense. Science. 264:1994;1918-1921.
45. Orange J. S., Biron C. A. Characterization of early IL-12, IFN-alpha/beta, and TNF effects on antiviral state and NK cell responses during murine cytomegalovirus infection. J. Immunol. 156:1996;4746-4756.
46. Orange J. S., Wang B., Terhorst C., Biron C. A. Requirement for natural killer cell-produced interferon-gamma in defense against murine cytomegalovirus infection and enhancement of this defense pathway by interleukin 12 administration. J. Exp. Med. 182:1995;1045-1056.
47. Osborn J. E., Blazkovec A. A., Walker D. L. Immunosuppression during acute murine cytomegalovirus infection. J. Immunol. 100:1968;835-844.
48. Pavic I., Polic B., Crnkovic I., Lucin P., Jonjic S., Koszinowski U. H. Participation of endogenous tumour necrosis factor-alpha in host resistance to cytomegalovirus infection. J. Gen. Virol. 74:1993;2215-2223.
49. Pollock J. L., Presti R. M., Paetzold S., Virgin H. W. Latent murine cytomegalovirus infection in macrophages. Virology. 227:1997;168-179.
50. Pollock J. L., Virgin H. W. Latency, without persistence, of murine cytomegalovirus in spleen and kidney. J. Virol. 69:1995;1762-1768.
51. Price P., Winter J. G., Shellam G. R. Genetically determined resistance to murine cytomegalovirus: A role for lymphocytostatic macrophages. J. Gen. Virol. 68:1987;2997-3008.
52. Reddehase M. J., Mutter W., Munch K., Buhring H. J., Koszinowski U. H. CD8-positive T lymphocytes specific for murine cytomegalovirus immediate-early antigens mediate protective immunity. J. Virol. 61:1987;3102-3108.
53. Rice G. P. A., Schrier R. D., Oldstone M. B. Cytomegalovirus infects human lymphocytes and monocytes: Virus expression is restricted to immediate-early gene products. Proc. Natl. Acad. Sci. USA. 81:1984;6134-6138.
54. Saltzman R. L., Quirk M. R., Jordan M. C. Disseminated cytomegalovirus infection: Molecular analysis of virus and leukocyte interactions in viremia. J. Clin. Invest. 81:1988;75-81.
55. Scholz M., Hammann A., Blaheta R. A., Auth M. K. H., Encke A., Markus B. H. Cytomegalovirus- and interferon-related effects on human endothelial cells: Cytomegalovirus infection reduces upregulation of HLA class II antigen expression after treatment with interferon-gamma. Hum. Immunol. 35:1992;230-238.
56. Schreiber R. D., Hicks L. J., Celada A., Buchmeier N. A., Gray P. W. Monoclonal antibodies to murine gamma interferon which differentially modulate macrophage activation and antiviral activity. J. Immunol. 134:1985;1609-1618.
57. Sedmak D. D., Chaiwiriyakul S., Knight D. A., Waldmann W. J. The role of interferon β in human cytomegalovirus-mediated inhibition of HLA DR induction on endothelial cells. Arch. Virol. 140:1995;111-126.
58. Sedmak D. D., Guglielmo A. M., Knight D. A., Birmingham D. J., Huang E. H., Waldman W. J. Cytomegalovirus inhibits major histocompatibility class II expression on infected endothelial cells. Am. J. Pathol. 144:1994;683-692.
59. Shanley J. D. In vivo administration of monoclonal antibody to the NK 1.1 antigen of natural killer cells: Effect on acute murine cytomegalovirus infection. J. Med. Virol. 30:1990;58-60.
60. Shanley J. D., Pesanti E. L. Murine peritoneal macrophages support murine cytomegalovirus replication. Infect. Immun. 41:1983;1352-1359.
61. Smith M. G. Propagation of salivary gland virus of the mouse in tissue culture. Proc. Soc. Exp. Biol. Med. 86:1954;435-440.
62. Starkey P. M., Turley L., Gordon S. The mouse macrophage-specific glycoprotein defined by monoclonal antibody F4/80: Characterization, biosynthesis and demonstration of a rat analogue. Immunology. 60:1987;117-122.
63. Stoddart C. A., Cardin R. D., Boname J. M., Manning W. C., Abenes G. B., Mocarski E. S. Peripheral blood mononuclear phagocytes mediate dissemination of murine cytomegalovirus. J. Virol. 68:1994;6243-6253.
64. Tarr G. C., Armstrong J. A., Ho M. Production of interferon and serum hyporeactivity factor in mice infected with murine cytomegalovirus. Infect. Immun. 19:1978;903-907.
65. Taswell C. Limiting dilution assays for the determination of immunocompetent cell frequencies. J. Immunol. 126:1981;1614-1619.
66. Taylor-Wiedeman J., Sissons J. P. G., Borysiewicz L. K., Sinclair J. H. Monocytes are a major site of persistence of human cytomegalovirus in peripheral blood mononuclear cells. J. Gen. Virol. 72:1991;2059-2064.
67. Taylor-Wiedeman J., Sissons P., Sinclair J. Induction of endogenous human cytomegalovirus gene expression after differentiation of monocytes from healthy carriers. J. Virol. 68:1994;1597-1604.
68. Unanue E. R., Allen P. M. The basis for the immunoregulatory role of macrophages and other accessory cells. Science. 236:1987;551-557.
69. Villarete L., De Fries R., Kohlhekar S., Howard D., Ahmed R., Wu-Hsieh B. Impaired responsiveness to gamma interferon of macrophages infected with lymphocytic choriomeningitis virus clone 13: Susceptibility to histoplasmosis. Infect. Immun. 63:1995;1468-1472.
70. Welsh R. M., Brubaker J. O., Vargas Cortes M., O'Donnell C. L. Natural killer (NK) cell response to virus infections in mice with severe combined immunodeficiency: The stimulation of NK cells and the NK cell-dependent control of virus infections occur independently of T and B cell function. J. Exp. Med. 173:1991;1053-1063.