The mouse cytomegalovirus glycoprotein m155 inhibits CD40 expression and restricts CD4 T cell responses

Journal of Virology

Volumn 85, Issue 10, 2011, Pages 661-664

  Loewendorf, Andrea I ^a   Steinbrueck, Lars ^b   Peter, Christoph ^b   Busche, Andreas ^b   Benedict, Chris A ^a   Kay Jackson, Penelope C ^b  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; GLYCOPROTEIN M155; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL SURFACE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOMEGALOVIRUS; DOWN REGULATION; MACROPHAGE; MOUSE; MURINE CYTOMEGALOVIRUS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN CELL;

CYTOMEGALOVIRUS; MAIZE CHLOROTIC MOTTLE VIRUS;

EID: 79955368567     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02178-10     Document Type: Article

References (50)

1. Abenes, G., et al. 2004. Murine cytomegalovirus with a transposon insertional mutation at open reading frame m155 is deficient in growth and virulence in mice. J. Virol. 78:6891-6899.
2. Adams, E. J., et al. 2007. Structural elucidation of the m157 mouse cyto-megalovirus ligand for Ly49 natural killer cell receptors. Proc. Natl. Acad. Sci. U. S. A. 104:10128-10133.
3. Andrews, D. M., C. E. Andoniou, F. Granucci, P. Ricciardi-Castagnoli, and M. A. Degli-Esposti. 2001. Infection of dendritic cells by murine cytomega-lovirus induces functional paralysis. Nat. Immunol. 2:1077-1084.
4. Arapovic, J., R. T. Lenac, A. B. Reddy, A. Krmpotic, and S. Jonjic. 2009. Promiscuity of MCMV immunoevasin of NKG2D: m138/fcr-1 down-modulates RAE-1epsilon in addition to MULT-1 and H60. Mol. Immunol. 47: 114-122.
5. Arase, H., E. S. Mocarski, A. E. Campbell, A. B. Hill, and L. L. Lanier. 2002. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296:1323-1326.
6. Arens, R., et al. 2008. Cutting edge: murine cytomegalovirus induces a polyfunctional CD4 T cell response. J. Immunol. 180:6472-6476.
7. Beck, K., U. Meyer-Konig, M. Weidmann, C. Nern, and F. T. Hufert. 2003. Human cytomegalovirus impairs dendritic cell function: a novel mechanism of human cytomegalovirus immune escape. Eur. J. Immunol. 33:1528-1538.
8. Benedict, C. A., A. Loewendorf, Z. Garcia, B. R. Blazar, and E. M. Janssen. 2008. Dendritic cell programming by cytomegalovirus stunts naive T cell responses via the PD-L1/PD-1 pathway. J. Immunol. 180:4836-4847.
9. Borst, E. M., C. Benkartek, and M. Messerle. 2007. Use of bacterial artificial chromosomes in generating targeted mutations in human and mouse cyto-megaloviruses. Curr. Protoc. Immunol. Chapter 10:Unit 10.32.
10. Carney, W. P., and M. S. Hirsch. 1981. Mechanisms of immunosuppression in cytomegalovirus mononucleosis. II. Virus-monocyte interactions. J. Infect. Dis. 144:47-54.
11. Contin, C., et al. 2003. Membrane-anchored CD40 is processed by the tumor necrosis factor-alpha-converting enzyme: implications for CD40 signaling. J. Biol. Chem. 278:32801-32809.
12. Crough, T., and R. Khanna. 2009. Immunobiology of human cytomegalovi-rus: from bench to bedside. Clin. Microbiol. Rev. 22:76-98.
13. Diefenbach, A., A. M. Jamieson, S. D. Liu, N. Shastri, and D. H. Raulet. 2000. Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat. Immunol. 1:119-126.
14. Elgueta, R., et al. 2009. Molecular mechanism and function of CD40/CD40L engagement in the immune system. Immunol. Rev. 229:152-172.
15. Frascaroli, G., et al. 2006. Dendritic cell function in cytomegalovirus-in-fected patients with mononucleosis. J. Leukoc. Biol. 79:932-940.
16. Gredmark, S., and C. Soderberg-Naucler. 2003. Human cytomegalovirus inhibits differentiation of monocytes into dendritic cells with the consequence of depressed immunological functions. J. Virol. 77:10943-10956.
17. Gredmark, S., T. Tilburgs, and C. Soderberg-Naucler. 2004. Human cyto-megalovirus inhibits cytokine-induced macrophage differentiation. J. Virol. 78:10378-10389.
18. Grewal, I. S., J. Xu, and R. A. Flavell. 1995. Impairment of antigen-specific T-cell priming in mice lacking CD40 ligand. Nature 378:617-620.
19. Grigoleit, U., et al. 2002. Human cytomegalovirus induces a direct inhibitory effect on antigen presentation by monocyte-derived immature dendritic cells. Br. J. Haematol. 119:189-198.
20. Hasan, M., et al. 2005. Selective down-regulation of the NKG2D ligand H60 by mouse cytomegalovirus m155 glycoprotein. J. Virol. 79:2920-2930.
21. Heise, M. T., M. Connick, and H. W. Virgin. 1998. Murine cytomegalovirus inhibits interferon gamma-induced antigen presentation to CD4 T cells by macrophages via regulation of expression of major histocompatibility complex class II-associated genes. J. Exp. Med. 187:1037-1046.
22. Hertel, L., V. G. Lacaille, H. Strobl, E. D. Mellins, and E. S. Mocarski. 2003. Susceptibility of immature and mature Langerhans cell-type dendritic cells to infection and immunomodulation by human cytomegalovirus. J. Virol. 77: 7563-7574.
23. Humphreys, I. R., et al. 2007. OX40 costimulation promotes persistence of cytomegalovirus-specific CD8 T Cells: a CD4-dependent mechanism. J. Immunol. 179:2195-2202.
24. Krmpotic, A., et al. 2005. NK cell activation through the NKG2D ligand MULT-1 is selectively prevented by the glycoprotein encoded by mouse cytomegalovirus gene m145. J. Exp. Med. 201:211-220.
25. Lenac, T., et al. 2006. The herpesviral Fc receptor fcr-1 down-regulates the NKG2D ligands MULT-1 and H60. J. Exp. Med. 203:1843-1850.
26. Lodoen, M., et al. 2003. NKG2D-mediated natural killer cell protection against cytomegalovirus is impaired by viral gp40 modulation of retinoic acid early inducible 1 gene molecules. J. Exp. Med. 197:1245-1253.
27. Lodoen, M. B., et al. 2004. The cytomegalovirus m155 gene product subverts natural killer cell antiviral protection by disruption of H60-NKG2D interactions. J. Exp. Med. 200:1075-1081.
28. Loewendorf, A., et al. 2004. Identification of a mouse cytomegalovirus gene selectively targeting CD86 expression on antigen-presenting cells. J. Virol. 78:13062-13071.
29. Ma, D. Y., and E. A. Clark. 2009. The role of CD40 and CD154/CD40L in dendritic cells. Semin. Immunol. 21:265-272.
30. Malarkannan, S., et al. 1998. The molecular and functional characterization of a dominant minor H antigen, H60. J. Immunol. 161:3501-3509.
31. Mans, J., et al. 2007. Cellular expression and crystal structure of the murine cytomegalovirus major histocompatibility complex class I-like glycoprotein, m153. J. Biol. Chem. 282:35247-35258.
32. Mans, J., et al. 2009. Structure and function of murine cytomegalovirus MHC-I-like molecules: how the virus turned the host defense to its advantage. Immunol. Res. 43:264-279.
33. Mathys, S., et al. 2003. Dendritic cells under influence of mouse cytomegalovirus have a physiologic dual role: to initiate and to restrict T cell activation. J. Infect. Dis. 187:988-999.
34. Mocarski, E. S., T. Shenk, and R. F. Pass. 2007. Cytomegaloviruses, p. 2701-2772. In D. M. Knipe, et al. Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
35. Moutaftsi, M., A. M. Mehl, L. K. Borysiewicz, and Z. Tabi. 2002. Human cytomegalovirus inhibits maturation and impairs function of monocyte-derived dendritic cells. Blood 99:2913-2921.
36. Munks, M. W., et al. 2006. Genome-wide analysis reveals a highly diverse CD8 T cell response to murine cytomegalovirus. J. Immunol. 176:3760-3766.
37. Rawlinson, W. D., H. E. Farrell, and B. G. Barrell. 1996. Analysis of the complete DNA sequence of murine cytomegalovirus. J. Virol. 70:8833-8849.
38. Razonable, R R 2005. Epidemiology of cytomegalovirus disease in solid organ and hematopoietic stem cell transplant recipients. Am. J. Health Syst. Pharm. 62(8 Suppl. 1):S7-S13.
39. Redpath, S., A. Angulo, N. R Gascoigne, and P. Ghazal. 1999. Murine cytomegalovirus infection down-regulates MHC class II expression on macrophages by induction of IL-10. J. Immunol. 162:6701-6707.
40. Redwood, A. J., et al. 2005. Use of a murine cytomegalovirus K181-derived bacterial artificial chromosome as a vaccine vector for immunocontracep-tion. J. Virol. 79:2998-3008.
41. Shen, Z., G. Reznikoff, G. Dranoff, and K. L. Rock. 1997. Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J. Immunol. 158:2723-2730.
42. Smith, H. R, et al. 2002. Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc. Natl. Acad. Sci. U. S. A. 99:8826-8831.
43. + T cell memory inflation during murine cytomegalovirus infection. J. Immunol. 183:3932-3941.
44. Varani, S., et al. 2005. Impaired dendritic cell immunophenotype and function in heart transplant patients undergoing active cytomegalovirus infection. Transplantation 79:219-227.
45. Whitmire, J. K., et al. 1999. CD40-CD40 ligand costimulation is required for generating antiviral CD4 T cell responses but is dispensable for CD8 T cell responses. J. Immunol. 163:3194-3201.
46. Wiesel, M., S. Walton, K. Richter, and A. Oxenius. 2009. Virus-specific CD8 T cells: activation, differentiation and memory formation. APMIS 117:356-381.
47. Yang, Y., et al. 1996. Transient subversion of CD40 ligand function diminishes immune responses to adenovirus vectors in mouse liver and lung tissues. J. Virol. 70:6370-6377.
48. Zanghellini, F., S. B. Boppana, V. C. Emery, P. D. Griffiths, and R. F. Pass. 1999. Asymptomatic primary cytomegalovirus infection: virologic and immunologic features. J. Infect. Dis. 180:702-707.
49. Zhan, X., et al. 2000. Mutagenesis of murine cytomegalovirus using a Tn3-based transposon. Virology 266:264-274.
50. Ziegler, H., et al. 1997. A mouse cytomegalovirus glycoprotein retains MHC class I complexes in the ERGIC/cis-Golgi compartments. Immunity 6:57-66.