Deletion mutant of human cytomegalovirus lacking US2-US6 and US11 maintains MHC class I expression and antigen presentation by infected dendritic cells

Virus Research

Volumn 155, Issue 2, 2011, Pages 446-454

  Schempp, Susanne ^a   Topp, Max ^b   Kessler, Tobias ^c   Sampaio, Kerstin Laib ^c   Dennehy, Kevin M ^c   Einsele, Hermann ^b   Hahn, Gabriele ^c   Grigoleit, Götz Ulrich ^b   Jahn, Gerhard ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c KLINIKUM INGOLSTADT   (Germany)

Author keywords

Adaptive immune response; Dendritic cells; Human cytomegalovirus; Stem cell transplantation

Indexed keywords

B7 ANTIGEN; CD40 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEIN US11; VIRUS PROTEIN;

ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ARTICLE; CD8+ T LYMPHOCYTE; CELL STRAIN; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOMEGALOVIRUS INFECTION; DELETION MUTANT; DENDRITIC CELL; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; HUMAN TISSUE; INTERFERON PRODUCTION; LYMPHOCYTE ACTIVATION; MAJOR HISTOCOMPATIBILITY COMPLEX; PRIORITY JOURNAL; T LYMPHOCYTE; VIRAL GENE DELIVERY SYSTEM; VIRUS MUTANT;

ANTIGEN PRESENTATION; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CYTOMEGALOVIRUS; DENDRITIC CELLS; DOWN-REGULATION; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; SEQUENCE DELETION;

HUMAN HERPESVIRUS 5;

EID: 78751706435     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2010.11.014     Document Type: Article

References (44)

1. Ahn K., Angulo A., Ghazal P., Peterson P.A., Yang Y., Fruh K. Human cytomegalovirus inhibits antigen presentation by a sequential multistep process. Proc. Natl. Acad. Sci. 1996, 93:10990-10995.
2. Andrews D.M., Andoniou C.E., Granucci F., Ricciardi-Castagnoli P., Degli-Esposti M.A. Infection of dendritic cells by murine cytomegalovirus induces functional paralysis. Nat. Immunol. 2001, 2:1077-1084.
3. Banchereau J., Briere F., Caux C., Davoust J., Lebecque S., Liu Y.J., Pulendran B., Palucka K. Immunobiology of dendritic cells. Annu. Rev. Immunol. 2000, 18:767-811.
4. Bolovan-Fritts C.A., Mocarski E.S., Wiedeman J.A. Peripheral blood CD14(+) cells from healthy subjects carry a circular conformation of latent cytomegalovirus genome. Blood 1999, 93:394-398.
5. Borst E.M., Hahn G., Koszinowski U.H., Messerle M. Cloning of the human cytomegalovirus (HCMV) genome as an infectious bacterial artificial chromosome in Escherichia coli: a new approach for construction of HCMV mutants. J. Virol. 1999, 73:8320-8329.
6. Cebulla C.M., Miller D.M., Zhang Y., Rahill B.M., Zimmerman P., Robinson J.M., Sedmak D.D. Human cytomegalovirus disrupts constitutive MHC class II expression. J. Immunol. 2002, 169:167-176.
7. Chevalier M.S., Daniels G.M., Johnson D.C. Binding of human cytomegalovirus US2 to major histocompatibility complex class I and II proteins is not sufficient for their degradation. J. Virol. 2002, 76:8265-8275.
8. Falk C.S., Mach M., Schendel D.J., Weiss E.H., Hilgert I., Hahn G. NK cell activity during human cytomegalovirus infection is dominated by US2-11-mediated HLA class I down-regulation. J. Immunol. 2002, 169:3257-3266.
9. Gerna G., Percivalle E., Lilleri D., Lozza L., Fornara C., Hahn G., Baldanti F., Revello M.G. Dendritic-cell infection by human cytomegalovirus is restricted to strains carrying functional UL131-128 genes and mediates efficient viral antigen presentation to CD8+ T-Cells. J. Gen. Virol. 2005, 86:275-284.
10. Grigoleit U., Riegler S., Einsele H., Laib Sampaio K., Jahn G., Hebart H., Brossart P., Frank F., Sinzger C. Human cytomegalovirus induces a direct inhibitory effect on antigen presentation by monocyte-derived immature dendritic cells. Br. J. Haematol. 2002, 119:189-198.
11. Hahn G., Jores R., Mocarski E.S. Cytomegalovirus remains latent in a common precursor of dendritic and myeloid cells. Proc. Natl. Acad. Sci. 1998, 95:3937-3942.
12. Hahn G., Khan H., Baldanti F., Koszinowski U.H., Revello M.G., Gerna G. The human cytomegalovirus ribonucleotide reductase homolog UL45 is dispensable for growth in endothelial cells, as determined by a BAC-cloned clinical isolate of human cytomegalovirus with preserved wild-type characteristics. J. Virol. 2002, 76:9551-9555.
13. Hegde N.R., Johnson D.C. Human cytomegalovirus US2 causes similar effects on both major histocompatibility complex class I and II proteins in epithelial and glial cells. J. Virol. 2003, 77:9287-9294.
14. Hegde N.R., Tomazin R.A., Wisner T.W., Dunn C., Boname J.M., Lewinsohn D.M., Johnson D.C. Inhibition of HLA-DR assembly, transport, and loading by human cytomegalovirus glycoprotein US3: a novel mechanism for evading major histocompatibility complex class II antigen presentation. J. Virol. 2002, 76:10929-10941.
15. Hengel H., Koopmann J.O., Flohr T., Muranyi W., Goulmy E., Hammerling G.J., Koszinowski U.H., Momburg F. A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity 1997, 6:623-632.
16. Hertel L., Lacaille V.G., Strobl H., Mellins E.D., Mocarski E.S. Susceptibility of immature and mature Langerhans cell-type dendritic cells to infection and immunomodulation by human cytomegalovirus. J. Virol. 2003, 77:7563-7574.
17. Jahn G., Stenglein S., Riegler S., Einsele H., Sinzger C. Human cytomegalovirus infection of immature dendritic cells and macrophages. Intervirology 1999, 42:365-372.
18. 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. 1995, 69:4830-4841.
19. Jones T.R., Sun L. Human cytomegalovirus US2 destabilizes major histocompatibility complex class I heavy chains. J. Virol. 1997, 71:2970-2979.
20. Jones T.R., Wiertz E.J., Sun L., Fish K.N., Nelson J.A., Ploegh H.L. Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class I heavy chains. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:11327-11333.
21. Kessler T., Reich M., Jahn G., Tolosa E., Beck A., Kalbacher H., Overkleeft H., Schempp S., Driessen C. Human cytomegalovirus infection interferes with major histocompatibility complex type II maturation and endocytic proteases in dendritic cells at multiple levels. J. Gen. Virol. 2008, 89:2427-2436.
22. Khan N., Bruton R., Taylor G.S., Cobbold M., Jones T.R., Rickinson A.B., Moss P.A. Identification of cytomegalovirus-specific cytotoxic T lymphocytes in vitro is greatly enhanced by the use of recombinant virus lacking the US2 to US11 region or modified vaccinia virus Ankara expressing individual viral genes. J. Virol. 2005, 79:2869-2879.
23. Lehner P.J., Karttunen J.T., Wilkinson G.W., Cresswell P. The human cytomegalovirus US6 glycoprotein inhibits transporter associated with antigen processing-dependent peptide translocation. Proc. Natl. Acad. Sci. 1997, 94:6904-6909.
24. Lozza L., Lilleri D., Percivalle E., Fornara C., Comolli G., Revello M.G., Gerna G. Simultaneous quantification of human cytomegalovirus (HCMV)-specific CD4+ and CD8+ T-Cells by a novel method using monocyte-derived HCMV-infected immature dendritic cells. Eur. J. Immunol. 2005, 35:1795-1804.
25. Manley T.J., Luy L., Jones T., Boeckh M., Mutimer H., Riddell S.R. Immune evasion proteins of human cytomegalovirus do not prevent a diverse CD8+ cytotoxic T-cellresponse in natural infection. Blood 2004.
26. Miller D.M., Rahill B.M., Boss J.M., Lairmore M.D., Durbin J.E., Waldman J.W., Sedmak D.D. Human cytomegalovirus inhibits major histocompatibility complex class II expression by disruption of the Jak/Stat pathway. J. Exp. Med. 1998, 187:675-683.
27. Moutaftsi M., Mehl A.M., Borysiewicz L.K., Tabi Z. Human cytomegalovirus inhibits maturation and impairs function of monocyte-derived dendritic cells. Blood 2002, 99:2913-2921.
28. Nyquist A.C., Zhang L., Weinberg A. Human fibroblasts transfected with cytomegalovirus immediate-early genes show increased MHC class I expression and are targets for natural killer cell-mediated cytotoxicity. Viral. Immunol. 2002, 15:147-154.
29. Odeberg J., Plachter B., Branden L., Soderberg-Naucler C. Human cytomegalovirus protein pp65 mediates accumulation of HLA-DR in lysosomes and destruction of the HLA-DR alpha-chain. Blood 2003, 101:4870-4877.
30. Raftery M.J., Schwab M., Eibert S.M., Samstag Y., Walczak H., Schonrich G. Targeting the function of mature dendritic cells by human cytomegalovirus: a multilayered viral defense strategy. Immunity 2001, 15:997-1009.
31. Rauser G., Einsele H., Sinzger C., Wernet D., Kuntz G., Assenmacher M., Campbell J.D., Topp M.S. Rapid generation of combined CMV-specific CD4+ and CD8+ T-celllines for adoptive transfer into recipients of allogeneic stem cell transplants. Blood 2004, 103:3565-3572.
32. Rehm A., Engelsberg A., Tortorella D., Korner I.J., Lehmann I., Ploegh H.L., Hopken U.E. Human cytomegalovirus gene products US2 and US11 differ in their ability to attack major histocompatibility class I heavy chains in dendritic cells. J. Virol. 2002, 76:5043-5050.
33. Riegler S., Hebart H., Einsele H., Brossart P., Jahn G., Sinzger C. Monocyte-derived dendritic cells are permissive to the complete replicative cycle of human cytomegalovirus. J. Gen. Virol. 2000, 81:393-399.
34. Senechal B., Boruchov A.M., Reagan J.L., Hart D.N., Young J.W. Infection of mature monocyte-derived dendritic cells with human cytomegalovirus inhibits stimulation of T-cellproliferation via the release of soluble CD83. Blood 2004, 103:4207-4215.
35. Sinzger C., Eberhardt K., Cavignac Y., Weinstock C., Kessler T., Jahn G., Davignon J.L. Macrophage cultures are susceptible to lytic productive infection by endothelial-cell-propagated human cytomegalovirus strains and present viral IE1 protein to CD4+ T-cells despite late downregultation of MHC class II molecules. J. Gen. Virol. 2006, 87:1853-1862.
36. Sinzger C., Hahn G., Digel M., Katona R., Sampaio K.L., Messerle M., Hengel H., Koszinowski U., Brune W., Adler B. Cloning and sequencing of a highly productive, endotheliotropic virus strain derived from human cytomegalovirus TB40/E. J. Gen. Virol. 2008, 89:359-368.
37. Sinzger C., Plachter B., Grefte A., The T.H., Jahn G. Tissue macrophages are infected by human cytomegalovirus in vivo. J. Infect. Dis. 1996, 173:240-245.
38. Sinzger C., Schmidt K., Knapp J., Kahl M., Beck R., Waldman J., Hebart H., Einsele H., Jahn G. Modification of human cytomegalovirus tropism through propagation in vitro is associated with changes in the viral genome. J. Gen. Virol. 1999, 80:2867-2877.
39. Soderberg-Naucler C., Streblow D.N., Fish K.N., Allan-Yorke J., Smith P.P., Nelson J.A. Reactivation of latent human cytomegalovirus in CD14(+) monocytes is differentiation dependent. J. Virol. 2001, 75:7543-7554.
40. Tomazin R., Boname J., Hegde N.R., Lewinsohn D.M., Altschuler Y., Jones T.R., Cresswell P., Nelson J.A., Riddell S.R., Johnson D.C. Cytomegalovirus US2 destroys two components of the MHC class II pathway, preventing recognition by CD4+ T-cells. Nat. Med. 1999, 5:1039-1043.
41. Topp M.S., Riddell S.R., Akatsuka Y., Jensen M.C., Blattman J.N., Greenberg P.D. Restoration of CD28 expression in CD28- CD8+ memory effector T-Cells reconstitutes antigen-induced IL-2 production. J. Exp. Med. 2003, 198:947-955.
42. Varani S., Frascaroli G., Gibellini D., Potena L., Lazzarotto T., Lemoli R.M., Magelli C., Soderberg-Naucler C., Landini M.P. Impaired dendritic cell immunophenotype and function in heart transplant patients undergoing active cytomegalovirus infection. Transplantation 2005, 79:219-227.
43. Wiertz E.J., Jones T.R., Sun L., Bogyo M., Geuze H.J., Ploegh H.L. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 1996, 84:769-779.
44. Wiertz E.J., Tortorella D., Bogyo M., Yu J., Mothes W., Jones T.R., Rapoport T.A., Ploegh H.L. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 1996, 384:432-438.