The immunoevasive function encoded by the mouse cytomegalovirus gene m152 protects the virus against T cell control in vivo

Journal of Experimental Medicine

Volumn 190, Issue 9, 1999, Pages 1285-1295

  Krmpotic, Astrid ^a   Messerle, Martin ^b   Crnkovic Mertens, Irena ^b   Polic, Bojan ^a   Jonjic, Stipan ^a   Koszinowski, Ulrich H ^b  

^a UNIVERSITY OF RIJEKA   (Croatia)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

CD8 T lymphocytes; Cytomegalovirus; Immune evasion; MHC class I; Virus mutants

Indexed keywords

BETA 2 MICROGLOBULIN; CD8 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; GENE DELETION; GENE FUNCTION; GENE INSERTION; IMMUNITY; LYMPHOCYTE DEPLETION; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; VIRUS GENE; VIRUS REPLICATION;

3T3 CELLS; ANIMALS; ANTIGEN PRESENTATION; CD8-POSITIVE T-LYMPHOCYTES; CYTOTOXICITY TESTS, IMMUNOLOGIC; GENE DELETION; GENES, MHC CLASS I; IMMUNITY; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED STRAINS; MUTATION; T-LYMPHOCYTES; VIRAL PROTEINS; VIRULENCE; VIRUS REPLICATION;

EID: 0033230906     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.190.9.1285     Document Type: Article

References (51)

1. Townsend, A., and H. Bodmer. 1989. Antigen recognition by class I-restricted T lymphocytes. Annu. Rev. Immunol. 7:601-624.
2. Heemels, M.T., and H.L. Ploegh. 1995. Generation, translocation, and presentation of MHC class I-restricted peptides. Annu. Rev. Biochem. 64:463-491.
3. Koopmann, J.O., G.J. Hämmerling, and F. Momburg. 1997. Generation, intracellular transport and loading of peptides associated with MHC class I molecules. Curr. Opin. Immunol. 9:80-88.
4. Hengel, H., and U.H. Koszinowski. 1998. Inhibition of MHC class 1 function by cytomegalovirus. In Herpesviruses and Immunity. P.G. Medvczky, H. Friedman, and M. Bendinelli, editors. Plenum Press, New York. 247-264.
5. Burgert, H.G., and S. Kvist. 1985. An adenovirus type 2 glyco-protein blocks cell surface expression of human histocompatibility class I antigens. Cell. 41:987-997.
6. + T lymphocytes. Cell. 77:525-535.
7. Hill, A., P. Jugovic, I. York, G. Russ, J. Bennink, J. Yewdell, H. Ploegh, and D. Johnson. 1995. Herpes simplex virus turns off the TAP to evade host immunity. Nature. 375:411-415.
8. Früh, K., K. Ahn, H. Djaballah, P. Sempe, P.M. van Endert, R. Tampe, P.A. Peterson, and Y. Yang. 1995. A viral inhibitor of peptide transporters for antigen presentation. Nature. 375:415-418.
9. Wiertz, E.J., D. Tortorella, M. Bogyo, J. Yu, W. Mothes, T.R. Jones, T.A. Rapoport, and H.L. Ploegh. 1996. Sec61-mediated transfer of a membrane protein from endoplasmic reticuluni to the proteasome for destruction. Nature. 384: 432-438.
10. Wiertz, E.J., T.R. Jones, L. Sun, M. Bogyo, H.J. Geuze, and H.L. Ploegh. 1996. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell. 84:769-779.
11. Jones, T.R., E.J. Wiertz, L. Sun, K.N. Fish, J.A. Nelson, and H.L. Ploegh. 1996. Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class I heavy chains. Proc. Natl. Acad. Sci. USA. 93: 11327-11333.
12. Ahn, K., A. Angulo, P. Ghazal, P.A. Peterson, Y. Yang, and K. Früh. 1996. Human cytomegalovirus inhibits antigen presentation by a sequential multistep process. Proc. Natl. Acad. Sci. USA. 93:10990-10995.
13. Ahn, K., A. Gruhler, B. Galocha, T.R. Jones, E.J. Wiertz, H.L. Ploegh, P.A. Peterson, Y. Yang, and K. Früh. 1997. The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity. 6:613-621.
14. Hengel, H., J.O. Koopmann, T. Flohr, W. Muranyi, E. Goulmy, G.J. Hämmerling, U.H. Koszinowski, and F. Momburg. 1997. A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity. 6:623-632.
15. Lehner, P.J., J.T. Karttunen, G.W. Wilkinson, and P. Cresswell. 1997. The human cytomegalovirus US6 glycoprotein inhibits transporter associated with antigen processing-dependent peptide translocation. Proc. Natl. Acad. Sci., USA. 94: 6904-6909.
16. Ziegler, H., R. Thäle, P. Lucin, W. Muranyi, T. Flohr, H. Hengel, H. Farrell, W. Rawlinson, and U.H. Koszinowski. 1997. A mouse cytomegalovirus glycoprotein retains MHC class I complexes in the ERGIC/cis-Golgi compartments. Immunity. 6:57-66.
17. Kleijnen, M.F., J.B. Huppa, P. Lucin, S. Mukherjee, H. Farrell, A.E. Campbell, U.H. Koszinowski, A.B. Hill, and H.L. Ploegh. 1997. A mouse cytomegalovirus glycoprotein gp34 forms a complex with folded class I MHC molecules in the ER which is not retained but is transported to the cell surface. EMBO (Eur. Mol. Biol. Organ.) J. 16:685-694.
18. Reusch, U., W. Muranyi, P. Lucin, H.G. Burgert, H. Hengel, and U.H. Koszinowski. 1999. A cytomegalovirus glyco-protein re-routes MHC class I complexes to lysosomes for degradation. EMBO (Eur. Mol. Biol. Organ.) J. 18:1081-1091.
19. von Herrath, M.G., S. Efrat, M.B. Oldstone, and M.S. Horwitz. 1997. Expression of adenoviral E3 transgenes in beta cells prevents autoimmune diabetes. Proc. Natl. Acad. Sci. USA. 94:9808-9813.
20. + T cell response. J. Exp. Med. 187:341-348.
21. del Val, M., K. Münch, M.J. Reddehase, and U.H. Koszinowski. 1989. Presentation of cytomegalovirus immediate-early antigens to cytolytic T lymphocytes is selectively blocked by viral genes expressed in the early phase. Cell. 58: 305-315.
22. del Val, M., H. Hengel, H. Häcker, U. Hartlaub, T. Ruppert, P. Lucin, and U.H. Koszinowski. 1992. 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: 729-738.
23. Thäle, R., U. Szepan, H. Hengel, G. Geginat, P. Lucin, and U.H. Koszinowski. 1995. Identification of the mouse cytomegalovirus genomic region affecting major histocompatibility complex class 1 molecule transport. J. Virol. 69:6098-6105.
24. del Val, M., H.J. Schlicht, T. Ruppert, M.J. Reddehase, and U.H. Koszinowski. 1991. Efficient processing of an antigenic sequence for presentation by MHC class I molecules depends on its neighboring residues in the protein. Cell. 66:1145-1153.
25. Sambrook, J., E. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 1659 pp.
26. Crnkovic-Mertens, I., M. Messerle, I. Milotic, U. Szepan, N. Kucic, A. Krmpotic, S. Jonjic, and U.H. Koszinowski. 1998. Virus attenuation after deletion of the cytomegalovirus Fc receptor is not due to antibody control. J. Virol. 72:1377-1382.
27. Rawlinson, W.D., H. Farrell, and B.G. Barrell. 1996. Analysis of the complete DNA sequence of murine cytomegalovirus. J. Virol. 70:8833-8849.
28. Vieira J., H.E. Farrell, W.D. Rawlinson, and E.S. Mocarski. 1994. Genes in the HindIII J fragment of the murine cytomegalovirus genome are dispensable for growth in cultured cells: insertion mutagenesis with a lacZ/gpt cassette. J. Virol. 68:4837-4846.
29. Greaves, R.F., J.M. Brown, J. Vieira, and E.S. Mocarski. 1995. Selectable insertion and deletion mutagenesis of the human cytomegalovirus genome using the Escherichia coli guanosine phosphoribosyl transferase (gpt) gene. J. Gen. Virol. 76:2151-2160.
30. del Val, M., H. Volkmer, B. Rothbard, S. Jonjic, M. Messerle, J. Schickedanz, M.J. Reddehase, and U.H. Koszinowski. 1988. Molecular basis for cytolytic T-lymphocyte recognition of the murine cytomegalovirus immediate-early protein pp89. J. Virol. 62:3965-3972.
31. Kitamura, D., J. Roes, R. Kühn, and K. Rajewsky. 1991. B cell-deficient mouse by targeting disruption of the membrane exon of the immunoglobulin μ chain gene. Nature. 350: 423-426.
32. Klein-Schneegans, A.S., C. Gaveriaux, P. Fonteneau, and F. Loor. 1989. Indirect double sandwich ELISA for the specific and quantitative measurement of mouse IgM, IgA and IgG subclasses. J. Immunol. Methods. 119:117-125.
33. + cytolytic T cells. Nature. 344:742-746.
34. Polic, B., S. Jonjic, I. Pavic, I. Crnkovic, I. Zorica, H. Hengel, P. Lucin, and U.H. Koszinowski. 1996. Lack of MHC class I complex expression has no effect on spread and control of cytomegalovirus infection in vivo. J. Gen. Virol. 77:217-225.
35. Jonjic, S., I. Pavic, B. Polic, I. Crnkovic, P. Lucin, and U.H. Koszinowski. 1994. Antibodies are not essential for the resolution of primary cytomegalovirus infection but limit dissemination of recurrent virus. J. Exp. Med. 179:1713-1717.
36. Reddehase, M.J., G.M. Keil, and U.H. Koszinowski. 1984. 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.
37. Reddehase, M.J., F. Weiland, K. Münch, S. Jonjic, A. Lüske, and U.H. Koszinowski. 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.
38. Cobbold, S.P., A. Jayasuriya, A. Nash, T.D. Prospero, and H. Waldman. 1984. Therapy with monoclonal antibodies by elimination of T-cell subsets in vivo. Nature. 312:548-550.
39. Reddehase, M.J., M. Balthesen, M. Rapp, S. Jonjic, I. Pavic, and U.H. Koszinowski. 1994. The conditions of primary infection define the load of latent viral genome in organs and the risk of recurrent cytomegalovirus disease. J. Exp. Med. 179:185-193.
40. Trgovcich, J., E. Pernjak-Pugel, J. Tomac, U.H. Koszinowski, and S. Jonjic. 1998. Pathogenesis of murine cytomegalovirus infection in mice. In CMV-related Immunopathology. Monographs in Virology. Vol. 21. M. Scholz, H.F. Rabenau, H.W. Doerr, and J. Cinatl, Jr., editors. Karger Publishers, Basel, Switzerland. 42-53.
41. + T lymphocytes. J. Exp. Med. 169:1199-1212.
42. Reddehase, M.J., S. Jonjic, F. Weiland, W. Mutter, and U.H. Koszinowski. 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.
43. Thäle, R., P. Lucin, K. Schneider, M. Eggers, and U.H. Koszinowski. 1994. Identification and expression of a murine cytomegalovirus early gene coding for an Fc receptor. J. Virol. 68: 7757-7765.
44. Bukowski, J.F., J.F. Warner, G. Dennert, and R.M. Welsh. 1985. Adoptive transfer studies demonstrating the antiviral effect of natural killer cells in vivo. J. Exp. Med. 161:40-52.
45. Lanier, L.L., B. Corliss, and J.H. Phillips. 1997. Arousal and inhibition of human NK cells. Immunol. Rev. 155:145-154.
46. Moretta, A., C. Bottino, M. Vitale, D. Pende, R. Biassoni, M.C. Mingari, and L. Moretta. 1996. Receptors for HLA class-I molecules in human natural killer cells. Annu. Rev. Immunol. 14:619-648.
47. Beck, S., and B.G. Barrell. 1988. Human cytomegalovirus encodes a glycoprotein homologous to MHC class-I antigens. Nature. 331:269-271.
48. Farrell, H.E., H. Vally, D.M. Lynch, P. Fleming, G.R. Shellam, A.A. Scalzo, and N.J. Davis-Poynter. 1997. Inhibition of natural killer cells by a cytomegalovirus MHC class I homologue in vivo. Nature. 386:510-514.
49. Leong, C.C., T.L. Chapman, P.J. Bjorkman, D. Formankova, E.S. Mocarski, J.H. Phillips, and L.L. Lanier. 1998. Modulation of natural killer cell cytotoxicity in human cytomegalovirus infection: the role of endogenous class I major histocompatibility complex and a viral class I homolog. J. Exp. Med. 187:1681-1687.
50. Messerle, M., I. Crnkovic, W. Hammerschmidt, H. Ziegler, and U.H. Koszinowski. 1997. Cloning and mutagenesis of a herpesvirus genome as an infectious bacterial artificial chromosome. Proc. Natl. Acad. Sci. USA. 94:14759-14763.
51. Brune, W., C. Ménard, U. Hobom, S. Odenbreit, M. Messerle, and U.H. Koszinowski. 1999. Rapid identification of essential and nonessential herpesvirus genes by direct transposon mutagenesis. Nat. Biotechnol. 17:360-364.