Absence of cross-presenting cells in the salivary gland and viral immune evasion confine cytomegalovirus immune control to effector CD4 T cells

PLoS Pathogens

Volumn 7, Issue 8, 2011, Pages

  Walton, Senta M ^a   Mandaric, Sanja ^a   Torti, Nicole ^a   Zimmermann, Albert ^b   Hengel, Hartmut ^b   Oxenius, Annette ^a  

^a ETH ZURICH   (Switzerland)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DISEASE TRANSMISSION; EFFECTOR CELL; EPITHELIUM CELL; IMMUNE EVASION; MOUSE; MURINE CYTOMEGALOVIRUS; NONHUMAN; SALIVARY GLAND; SIGNAL TRANSDUCTION; ANIMAL; ANIMAL MODEL; C57BL MOUSE; CROSS PRESENTATION; FLUORESCENCE MICROSCOPY; IMMUNOLOGY; MOUSE MUTANT; MUROMEGALOVIRUS; PATHOGENICITY; PHYSIOLOGY; SECRETION; VIROLOGY; VIRUS REPLICATION;

CYTOMEGALOVIRUS; MAIZE CHLOROTIC MOTTLE VIRUS; MURINAE;

ANIMALS; ANTIGEN-PRESENTING CELLS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CROSS-PRIMING; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; IMMUNE EVASION; INTERFERON-GAMMA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; MODELS, ANIMAL; MUROMEGALOVIRUS; SALIVARY GLANDS; VIRUS REPLICATION;

EID: 80052321890     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002214     Document Type: Article

References (55)

1. Mocarski ES, Shenk T, Pass RF, (2007) Cytomegaloviruses; In: Howley DKKaPM, editors. Philadelphia Lippincott, Williams & Wilkins.
2. Boppana SB, Fowler KB, (2007) Persistence in the population: epidemiology and transmisson. In: Arvin A C-FG, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K, editors. Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis Cambridge Cambridge University Press 2011/02/25 ed.
3. Britt W, (2007) Virus entry into host, establishment of infection, spread in host, mechanisms of tissue damage. In: Arvin A C-FG, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K, editors. Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis Cambridge Cambridge University Press 2011/02/25 ed.
4. Campbell AE, Cavanaugh VJ, Slater JS, (2008) The salivary glands as a privileged site of cytomegalovirus immune evasion and persistence. Med Microbiol Immunol 197: 205-213.
5. Jonjic S, Mutter W, Weiland F, Reddehase MJ, Koszinowski UH, (1989) Site-restricted persistent cytomegalovirus infection after selective long-term depletion of CD4+ T lymphocytes. J Exp Med 169: 1199-1212.
6. Lucin P, Pavic I, Polic B, Jonjic S, Koszinowski UH, (1992) Gamma interferon-dependent clearance of cytomegalovirus infection in salivary glands. J Virol 66: 1977-1984.
7. Pavic I, Polic B, Crnkovic I, Lucin P, Jonjic S, et al. (1993) Participation of endogenous tumour necrosis factor alpha in host resistance to cytomegalovirus infection. J Gen Virol 74 (Pt10): 2215-2223.
8. Walton SM, Wyrsch P, Munks MW, Zimmermann A, Hengel H, et al. (2008) The dynamics of mouse cytomegalovirus-specific CD4 T cell responses during acute and latent infection. J Immunol 181: 1128-1134.
9. Arens R, Wang P, Sidney J, Loewendorf A, Sette A, et al. (2008) Cutting edge: murine cytomegalovirus induces a polyfunctional CD4 T cell response. J Immunol 180: 6472-6476.
10. Jonjic S, Pavic I, Lucin P, Rukavina D, Koszinowski UH, (1990) Efficacious control of cytomegalovirus infection after long-term depletion of CD8+ T lymphocytes. J Virol 64: 5457-5464.
11. Polic B, Jonjic S, Pavic I, Crnkovic I, Zorica I, et al. (1996) Lack of MHC class I complex expression has no effect on spread and control of cytomegalovirus infection in vivo. J Gen Virol 77 (Pt 2): 217-225.
12. Jonjic S, Pavic I, Polic B, Crnkovic I, Lucin P, et al. (1994) Antibodies are not essential for the resolution of primary cytomegalovirus infection but limit dissemination of recurrent virus. J Exp Med 179: 1713-1717.
13. Scalzo AA, Manzur M, Forbes CA, Brown MG, Shellam GR, (2005) NK gene complex haplotype variability and host resistance alleles to murine cytomegalovirus in wild mouse populations. Immunol Cell Biol 83: 144-149.
14. Brown MG, Scalzo AA, Stone LR, Clark PY, Du Y, et al. (2001) Natural killer gene complex (Nkc) allelic variability in inbred mice: evidence for Nkc haplotypes. Immunogenetics 53: 584-591.
15. Casazza JP, Betts MR, Price DA, Precopio ML, Ruff LE, et al. (2006) Acquisition of direct antiviral effector functions by CMV-specific CD4+ T lymphocytes with cellular maturation. J Exp Med 203: 2865-2877.
16. Klenovsek K, Weisel F, Schneider A, Appelt U, Jonjic S, et al. (2007) Protection from CMV infection in immunodeficient hosts by adoptive transfer of memory B cells. Blood 110: 3472-3479.
17. Munks MW, Pinto AK, Doom CM, Hill AB, (2007) Viral interference with antigen presentation does not alter acute or chronic CD8 T cell immunodominance in murine cytomegalovirus infection. J Immunol 178: 7235-7241.
18. Sierro S, Rothkopf R, Klenerman P, (2005) Evolution of diverse antiviral CD8+ T cell populations after murine cytomegalovirus infection. Eur J Immunol 35: 1113-1123.
19. Wiesel M, Walton S, Richter K, Oxenius A, (2009) Virus-specific CD8 T cells: activation, differentiation and memory formation. APMIS 117: 356-381.
20. Snyder CM, Loewendorf A, Bonnett EL, Croft M, Benedict CA, et al. (2009) CD4+ T cell help has an epitope-dependent impact on CD8+ T cell memory inflation during murine cytomegalovirus infection. J Immunol 183: 3932-3941.
21. Reddehase MJ, Jonjic 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.
22. Walton SM, Torti N, Mandaric S, Oxenius A, (2011) T cell help permits memory CD8(+) T cell inflation during cytomegalovirus latency. Eur J Immunol. May 17 doi:10.1002/eji.201141575.
23. Cavanaugh VJ, Deng Y, Birkenbach MP, Slater JS, Campbell AE, (2003) Vigorous innate and virus-specific cytotoxic T-lymphocyte responses to murine cytomegalovirus in the submaxillary salivary gland. J Virol 77: 1703-1717.
24. Nakanishi Y, Lu B, Gerard C, Iwasaki A, (2009) CD8(+) T lymphocyte mobilization to virus-infected tissue requires CD4(+) T-cell help. Nature 462: 510-513.
25. Lu X, Pinto AK, Kelly AM, Cho KS, Hill AB, (2006) Murine cytomegalovirus interference with antigen presentation contributes to the inability of CD8 T cells to control virus in the salivary gland. J Virol 80: 4200-4202.
26. Redpath S, Angulo A, Gascoigne NR, Ghazal P, (1999) Murine cytomegalovirus infection down-regulates MHC class II expression on macrophages by induction of IL-10. J Immunol 162: 6701-6707.
27. Heise MT, Connick M, Virgin HWt, (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.
28. Mathys S, Schroeder T, Ellwart J, Koszinowski UH, Messerle M, 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.
29. Doom CM, Hill AB, (2008) MHC class I immune evasion in MCMV infection. Med Microbiol Immunol 197: 191-204.
30. Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H, et al. (2008) Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 322: 1097-1100.
31. del Rio ML, Bernhardt G, Rodriguez-Barbosa JI, Forster R, (2010) Development and functional specialization of CD103+ dendritic cells. Immunol Rev 234: 268-281.
32. Bedoui S, Whitney PG, Waithman J, Eidsmo L, Wakim L, et al. (2009) Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat Immunol 10: 488-495.
33. Ruedl C, Storni T, Lechner F, Bachi T, Bachmann MF, (2002) Cross-presentation of virus-like particles by skin-derived CD8(-) dendritic cells: a dispensable role for TAP. Eur J Immunol 32: 818-825.
34. Wagner M, Gutermann A, Podlech J, Reddehase MJ, Koszinowski UH, (2002) Major histocompatibility complex class I allele-specific cooperative and competitive interactions between immune evasion proteins of cytomegalovirus. J Exp Med 196: 805-816.
35. Pearce EL, Shedlock DJ, Shen H, (2004) Functional characterization of MHC class II-restricted CD8+CD4- and CD8-CD4- T cell responses to infection in CD4-/- mice. J Immunol 173: 2494-2499.
36. Tyznik AJ, Sun JC, Bevan MJ, (2004) The CD8 population in CD4-deficient mice is heavily contaminated with MHC class II-restricted T cells. J Exp Med 199: 559-565.
37. Wirtz N, Schader SI, Holtappels R, Simon CO, Lemmermann NA, et al. (2008) Polyclonal cytomegalovirus-specific antibodies not only prevent virus dissemination from the portal of entry but also inhibit focal virus spread within target tissues. Med Microbiol Immunol 197: 151-158.
38. Lucin P, Jonjic S, Messerle M, Polic B, Hengel H, et al. (1994) Late phase inhibition of murine cytomegalovirus replication by synergistic action of interferon-gamma and tumour necrosis factor. J Gen Virol 75 (Pt1): 101-110.
39. Bukowski JF, Welsh RM, (1985) Inability of interferon to protect virus-infected cells against lysis by natural killer (NK) cells correlates with NK cell-mediated antiviral effects in vivo. J Immunol 135: 3537-3541.
40. Orange JS, Wang B, Terhorst C, Biron CA, (1995) 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: 1045-1056.
41. Orange JS, Biron CA, (1996) An absolute and restricted requirement for IL-12 in natural killer cell IFN-gamma production and antiviral defense. Studies of natural killer and T cell responses in contrasting viral infections. J Immunol 156: 1138-1142.
42. Tessmer MS, Reilly EC, Brossay L, (2011) Salivary gland NK cells are phenotypically and functionally unique. PLoS Pathog 7: e1001254.
43. Babic M, Pyzik M, Zafirova B, Mitrovic M, Butorac V, et al. (2010) Cytomegalovirus immunoevasin reveals the physiological role of "missing self" recognition in natural killer cell dependent virus control in vivo. J Exp Med 207: 2663-2673.
44. Andrews DM, Estcourt MJ, Andoniou CE, Wikstrom ME, Khong A, et al. (2010) Innate immunity defines the capacity of antiviral T cells to limit persistent infection. J Exp Med 207: 1333-1343.
45. Kontgen F, Suss G, Stewart C, Steinmetz M, Bluethmann H, (1993) Targeted disruption of the MHC class II Aa gene in C57BL/6 mice. Int Immunol 5: 957-964.
46. Rahemtulla A, Fung-Leung WP, Schilham MW, Kundig TM, Sambhara SR, et al. (1991) Normal development and function of CD8+ cells but markedly decreased helper cell activity in mice lacking CD4. Nature 353: 180-184.
47. Gu H, Zou YR, Rajewsky K, (1993) Independent control of immunoglobulin switch recombination at individual switch regions evidenced through Cre-loxP-mediated gene targeting. Cell 73: 1155-1164.
48. Marino MW, Dunn A, Grail D, Inglese M, Noguchi Y, et al. (1997) Characterization of tumor necrosis factor-deficient mice. Proc Natl Acad Sci U S A 94: 8093-8098.
49. Kagi D, Ledermann B, Burki K, Seiler P, Odermatt B, et al. (1994) Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369: 31-37.
50. 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.
51. Storni T, Bachmann MF, (2004) Loading of MHC class I and II presentation pathways by exogenous antigens: a quantitative in vivo comparison. J Immunol 172: 6129-6135.
52. Hasan M, Krmpotic A, Ruzsics Z, Bubic I, Lenac T, et al. (2005) Selective down-regulation of the NKG2D ligand H60 by mouse cytomegalovirus m155 glycoprotein. J Virol 79: 2920-2930.
53. Brune W, Hengel H, Koszinowski UH, (2001) A mouse model for cytomegalovirus infection. Curr Protoc Immunol Chapter 19: Unit 19-17.
54. Altman JD, Moss PA, Goulder PJ, Barouch DH, McHeyzer-Williams MG, et al. (1996) Phenotypic analysis of antigen-specific T lymphocytes. Science 274: 94-96.
55. Joller N, Sporri R, Hilbi H, Oxenius A, (2007) Induction and protective role of antibodies in Legionella pneumophila infection. Eur J Immunol 37: 3414-3423.