Immunodomination during Peripheral Vaccinia Virus Infection

PLoS Pathogens

Volumn 9, Issue 4, 2013, Pages

  Lin, Leon C W ^a   Flesch, Inge E A ^a   Tscharke, David C ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD69 ANTIGEN; CD86 ANTIGEN; GLYCOPROTEIN B; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXICITY; HERPES SIMPLEX VIRUS; IMMUNODOMINATION; IMMUNOMODULATION; MOUSE; NONHUMAN; SPLEEN; T LYMPHOCYTE ACTIVATION; VACCINIA VIRUS; VIRUS CULTURE; VIRUS INFECTION; VIRUS TITRATION;

ANIMALS; ANTIGENS, CD80; ANTIGENS, CD86; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CRICETINAE; EPITOPES, T-LYMPHOCYTE; IMMUNODOMINANT EPITOPES; LYMPH NODES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SMALLPOX VACCINE; VACCINIA; VACCINIA VIRUS; VIRAL ENVELOPE PROTEINS;

SIMPLEXVIRUS; VACCINIA VIRUS;

EID: 84876865164     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003329     Document Type: Article

References (77)

1. Yewdell JW, (2006) Confronting Complexity: Real-World Immunodominance in Antiviral CD8+ T Cell Responses. Immunity 25: 533-543.
2. Yewdell JW, Bennink JR, (1999) Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annual Review of Immunology 17: 51-88.
3. Bousso P, Levraud JP, Kourilsky P, Abastado JP, (1999) The Composition of a Primary T Cell Response Is Largely Determined by the Timing of Recruitment of Individual T Cell Clones. J Exp Med 189: 1591-1600.
4. Busch DH, Pamer EG, (1998) MHC class I/peptide stability: implications for immunodominance, in vitro proliferation, and diversity of responding CTL. J Immunol 160: 4441-4448.
5. Chen W, Anton LC, Bennink JR, Yewdell JW, (2000) Dissecting the multifactorial causes of immunodominance in class I- restricted T cell responses to viruses. Immunity 12: 83-93.
6. Chen W, Norbury CC, Cho Y, Yewdell JW, Bennink JR, (2001) Immunoproteasomes shape immunodominance hierarchies of antiviral CD8(+) T cells at the levels of T cell repertoire and presentation of viral antigens. J Exp Med 193: 1319-1326.
7. Del Val M, Schlicht HJ, Ruppert T, Reddehase MJ, Koszinowski UH, (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.
8. Deng Y, Yewdell JW, Eisenlohr LC, Bennink JR, (1997) MHC affinity, peptide liberation, T cell repertoire, and immunodominance all contribute to the paucity of MHC class I-restricted peptides recognized by antiviral CTL. J Immunol 158: 1507-1515.
9. Eisenlohr LC, Yewdell JW, Bennink JR, (1992) Flanking sequences influence the presentation of an endogenously synthesized peptide to cytotoxic T lymphocytes. J Exp Med 175: 481-487.
10. Kotturi MF, Scott I, Wolfe T, Peters B, Sidney J, et al. (2008) Naive precursor frequencies and MHC binding rather than the degree of epitope diversity shape CD8+ T cell immunodominance. J Immunol 181: 2124-2133.
11. La Gruta NL, Kedzierska K, Pang K, Webby R, Davenport M, et al. (2006) A virus-specific CD8+ T cell immunodominance hierarchy determined by antigen dose and precursor frequencies. PNAS 103: 994-999.
12. Pang KC, Sanders MT, Monaco JJ, Doherty PC, Turner SJ, et al. (2006) Immunoproteasome subunit deficiencies impact differentially on two immunodominant influenza virus-specific CD8+ T cell responses. J Immunol 177: 7680-7688.
13. Probst HC, Tschannen K, Gallimore A, Martinic M, Basler M, et al. (2003) Immunodominance of an antiviral cytotoxic T cell response is shaped by the kinetics of viral protein expression. J Immunol 171: 5415-5422.
14. Sette A, Vitiello A, Reherman B, Fowler P, Nayersina R, et al. (1994) The relationship between class I binding affinity and immunogenicity of potential cytotoxic T cell epitopes. J Immunol 153: 5586-5592.
15. van der Most RG, Murali-Krishna K, Lanier JG, Wherry EJ, Puglielli MT, et al. (2003) Changing immunodominance patterns in antiviral CD8 T-cell responses after loss of epitope presentation or chronic antigenic stimulation. Virology 315: 93-102.
16. van der Most RG, Sette A, Oseroff C, Alexander J, Murali-Krishna K, et al. (1996) Analysis of cytotoxic T cell responses to dominant and subdominant epitopes during acute and chronic lymphocytic choriomeningitis virus infection. J Immunol 157: 5543-5554.
17. Weidt G, Utermohlen O, Heukeshoven J, Lehmann-Grube F, Deppert W, (1998) Relationship among immunodominance of single CD8+ T cell epitopes, virus load, and kinetics of primary antiviral CTL response. J Immunol 160: 2923-2931.
18. Badovinac VP, Tvinnereim AR, Harty JT, (2000) Regulation of antigen-specific CD8+ T Cell homeostasis by perforin and interferon-gamma. Sci 290: 1354.
19. Choi EY, Christianson GJ, Yoshimura Y, Sproule TJ, Jung NJ, et al. (2002) Immunodominance of H60 is caused by an abnormally high precursor T cell pool directed against its unique minor histocompatibility antigen peptide. Immunity 17: 593-603.
20. Daly K, Nguyen P, Woodland DL, Blackman MA, (1995) Immunodominance of major histocompatibility complex class I-restricted influenza virus epitopes can be influenced by the T-cell receptor repertoire. J Virol 69: 7416-7422.
21. Dzutsev AH, Belyakov IM, Isakov DV, Margulies DH, Berzofsky JA, (2007) Avidity of CD8 T cells sharpens immunodominance. Int Immunol 19: 497-507.
22. Flesch IE, Woo WP, Wang Y, Panchanathan V, Wong YC, et al. (2010) Altered CD8+ T cell immunodominance after vaccinia virus infection and the naïve repertoire in inbred and F1 mice. J Immunol 184: 45-55.
23. Haeryfar SMM, Hickman HD, Irvine KR, Tscharke DC, Bennink JR, et al. (2008) Terminal deoxynucleotidyl transferase establishes and broadens anti-viral CD8+ T cell immunodominance hierarchies. J Immunol 181: 649-659.
24. Liu F, Whitton JL, Slifka MK, (2004) The rapidity with which virus-specific CD8+ T cells initiate IFN-γ synthesis increases markedly over the course of infection and correlates with immunodominance. J Immunol 173: 456-462.
25. Obar JJ, Khanna KM, Lefrançois L, (2008) Endogenous naive CD8+ T cell crecursor frequency regulates primary and memory responses to infection. Immunity 28: 859-869.
26. Perkins DL, Wang YS, Fruman D, Seidman JG, Rimm IJ, (1991) Immunodominance is altered in T cell receptor (beta-chain) transgenic mice without the generation of a hole in the repertoire. J Immunol 146: 2960-2964.
27. Trautmann L, Rimbert M, Echasserieau K, Saulquin X, Neveu B, et al. (2005) Selection of T cell clones expressing high-affinity public TCRs within human cytomegalovirus-specific CD8 T cell responses. J Immunol 175: 6123-6132.
28. Wallace ME, Bryden M, Cose SC, Coles RM, Schumacher TN, et al. (2000) Junctional biases in the naive TCR repertoire control the CTL response to an immunodominant determinant of HSV-1. Immunity 12: 547-556.
29. Haeryfar SMM, DiPaolo RJ, Tscharke DC, Bennink JR, Yewdell JW, (2005) Regulatory T cells suppress CD8+ T cell responses induced by direct priming and cross-priming and moderate immunodominance disparities. J Immunol 174: 3344-3351.
30. Andreansky SS, Stambas J, Thomas PG, Xie W, Webby RJ, et al. (2005) Consequences of immunodominant epitope deletion for minor influenza virus-specific CD8+ T cell responses. J Virol 79: 4329-4339.
31. Kastenmuller W, Gasteiger G, Gronau JH, Baier R, Ljapoci R, et al. (2007) Cross-competition of CD8+ T cells shapes the immunodominance hierarchy during boost vaccination. J Exp Med 204: 2187-2198.
32. Webby RJ, Andreansky S, Stambas J, Rehg JE, Webster RG, et al. (2003) Protection and compensation in the influenza virus-specific CD8+ T cell response. PNAS 100: 7235-7240.
33. Chen W, Pang K, Masterman K-A, Kennedy G, Basta S, et al. (2004) Reversal in the immunodominance hierarchy in secondary CD8+ T cell responses to influenza A virus: Roles for cross-presentation and lysis-independent immunodomination. J Immunol 173: 5021-5027.
34. Crowe SR, Turner SJ, Miller SC, Roberts AD, Rappolo RA, et al. (2003) Differential Antigen Presentation Regulates the Changing Patterns of CD8+ T Cell Immunodominance in Primary and Secondary Influenza Virus Infections. J Exp Med 198: 399-410.
35. Stock AT, Jones CM, Heath WR, Carbone FR, (2006) CTL response compensation for the loss of an immunodominant class I-restricted HSV-1 determinant. Immunol Cell Biol 84: 543-550.
36. Rodriguez F, Harkins S, Slifka MK, Whitton JL, (2002) Immunodominance in virus-induced CD8+ T-cell responses is dramatically modified by DNA immunization and is regulated by gamma interferon. J Virol 76: 4251-4259.
37. Wang Y, Flesch IEA, Tscharke DC, (2009) Vaccinia virus CD8+ T cell dominance hierarchies cannot be altered by prior immunization with individual peptides. J Virol 83: 9008-9012.
38. Kedl RM, Rees WA, Hildeman DA, Schaefer B, Mitchell T, et al. (2000) T Cells Compete for Access to Antigen-bearing Antigen-presenting Cells. J Exp Med 192: 1105-1114.
39. Palmowski MJ, Choi EM-L, Hermans IF, Gilbert SC, Chen JL, et al. (2002) Competition between CTL narrows the immune response induced by prime-boost vaccination protocols. J Immunol 168: 4391-4398.
40. Wolpert EZ, Grufman P, Sandberg JK, Tegnesjo A, Karre K, (1998) Immunodominance in the CTL response against minor histocompatibility antigens: interference between responding T cells, rather than with presentation of epitopes. J Immunol 161: 4499-4505.
41. Moutaftsi M, Peters B, Pasquetto V, Tscharke DC, Sidney J, et al. (2006) A consensus epitope prediction approach identifies the breadth of murine TCD8+-cell responses to vaccinia virus. Nat Biotechnol 24: 817-819.
42. Tscharke DC, Karupiah G, Zhou J, Palmore T, Irvine KR, et al. (2005) Identification of poxvirus CD8+ T cell determinants to enable rational design and characterization of smallpox vaccines. J Exp Med 201: 95-104.
43. Yuen TJ, Flesch IEA, Hollett NA, Dobson BM, Russell TA, et al. (2010) Analysis of A47, an immunoprevalent protein of vaccinia virus, leads to a reevaluation of the total antiviral CD8+ T cell response. J Virol 84: 10220-10229.
44. Cornberg M, Sheridan BS, Saccoccio FM, Brehm MA, Selin LK, (2006) Protection against vaccinia virus (VV) challenge by CD8 memory T cells resolved by molecular mimicry. J Virol 81: 934-44 JVI.01280-01206.
45. Moutaftsi M, Tscharke DC, Vaughan K, Koelle DM, Stern L, et al. (2010) Uncovering the interplay between CD8, CD4 and antibody responses to complex pathogens. Future Microbiology 5: 221-239.
46. Oseroff C, Peters B, Pasquetto V, Moutaftsi M, Sidney J, et al. (2008) Dissociation between epitope hierarchy and immunoprevalence in CD8 responses to vaccinia virus Western Reserve. J Immunol 180: 7193-7202.
47. Flesch IEA, Hollett NA, Wong YC, Tscharke DC, (2012) Linear fidelity in quantification of anti-viral CD8+ T cells. PLoS ONE 7: e39533.
48. Blaney JE Jr, Nobusawa E, Brehm MA, Bonneau RH, Mylin LM, et al. (1998) Immunization with a single major histocompatibility complex class I-restricted cytotoxic T-lymphocyte recognition epitope of herpes simplex virus type 2 confers protective immunity. J Virol 72: 9567-9574.
49. Tscharke DC, Smith GL, (1999) A model for vaccinia virus pathogenesis and immunity based on intradermal injection of mouse ear pinnae. J Gen Virol 80: 2751-2755.
50. Fischer MA, Davies ML, Reider IE, Heipertz EL, Epler MR, et al. (2011) CD11b+, Ly6G+ cells produce type I interferon and exhibit tissue protective properties following peripheral virus infection. PLoS Pathog 7: e1002374.
51. Buller RM, Smith GL, Cremer K, Notkins AL, Moss B, (1985) Decreased virulence of recombinant vaccinia virus expression vectors is associated with a thymidine kinase-negative phenotype. Nat 317: 813-815.
52. Coles RM, Mueller SN, Heath WR, Carbone FR, Brooks AG, (2002) Progression of armed CTL from draining lymph node to spleen shortly after localized infection with herpes simplex virus 1. J Immunol 168: 834-838.
53. Norbury CC, Malide D, Gibbs JS, Bennink JR, Yewdell JW, (2002) Visualizing priming of virus-specific CD8+ T cells by infected dendritic cells in vivo. Nat Immunol 3: 265-271.
54. Princiotta MF, Finzi D, Qian SB, Gibbs J, Schuchmann S, et al. (2003) Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 18: 343-354.
55. Jenkins MR, Webby R, Doherty PC, Turner SJ, (2006) Addition of a prominent epitope affects influenza A virus-specific CD8+ T cell immunodominance hierarchies when antigen is limiting. J Immunol 177: 2917-2925.
56. Johnson AJ, Njenga MK, Hansen MJ, Kuhns ST, Chen L, et al. (1999) Prevalent Class I-Restricted T-Cell Response to the Theiler's Virus Epitope Db:VP2121-130 in the Absence of Endogenous CD4 Help, Tumor Necrosis Factor Alpha, Gamma Interferon, Perforin, or Costimulation through CD28. J Virol 73: 3702-3708.
57. Chen W, Bennink JR, Morton PA, Yewdell JW, (2002) Mice deficient in perforin, CD4+ T Cells, or CD28-mediated signaling maintain the typical immunodominance hierarchies of CD8+ T-cell responses to influenza virus. J Virol 76: 10332-10337.
58. Salek-Ardakani S, Arens R, Flynn R, Sette A, Schoenberger SP, et al. (2009) Preferential Use of B7.2 and Not B7.1 in Priming of Vaccinia Virus-Specific CD8 T Cells. J Immunol 182: 2909-2918.
59. Hickman HD, Takeda K, Skon CN, Murray FR, Hensley SE, et al. (2008) Direct priming of antiviral CD8+ T cells in the peripheral interfollicular region of lymph nodes. Nat Immunol 9: 155-165.
60. Xu RH, Remakus S, Ma X, Roscoe F, Sigal LJ, (2010) Direct presentation is sufficient for an efficient anti-viral CD8 T cell response. PLoS Pathog 6: e1000768.
61. Holst PJ, Ørskov C, Thomsen AR, Christensen JP, (2010) Quality of the Transgene-Specific CD8+ T Cell Response Induced by Adenoviral Vector Immunization Is Critically Influenced by Virus Dose and Route of Vaccination. J Immunol 184: 4431-4439.
62. Venturi V, Davenport MP, Swan NG, Doherty PC, Kedzierska K, (2011) Consequences of suboptimal priming are apparent for low-avidity T-cell responses. Immunol Cell Biol 90: 216-23.
63. Liu L, Zhong Q, Tian T, Dubin K, Athale SK, et al. (2010) Epidermal injury and infection during poxvirus immunization is crucial for the generation of highly protective T cell-mediated immunity. Nat Med AOP 16: 224-7.
64. Shen XF, Wong SBJ, Buck CB, Zhang JW, Siliciano RF, (2002) Direct priming and cross-priming contribute differentially to the induction of CD8(+) CTL following exposure to vaccinia virus via different routes. J Immunol 169: 4222-4229.
65. Ranasinghe C, Turner SJ, McArthur C, Sutherland DB, Kim J-H, et al. (2007) Mucosal HIV-1 Pox Virus Prime-Boost Immunization Induces High-Avidity CD8+ T Cells with Regime-Dependent Cytokine/Granzyme B Profiles. J Immunol 178: 2370-2379.
66. Kaech SM, Ahmed R, (2001) Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nature Immunology 2: 415-422.
67. van Stipdonk MJB, Lemmens EE, Schoenberger SP, (2001) Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nature Immunology 2: 423-429.
68. Fang M, Sigal LJ, (2006) Direct CD28 costimulation is required for CD8+ T cell-mediated resistance to an acute viral disease in a natural host. J Immunol 177: 8027-8036.
69. Fuse S, Zhang W, Usherwood EJ, (2008) Control of Memory CD8+ T Cell Differentiation by CD80/CD86-CD28 Costimulation and Restoration by IL-2 during the Recall Response. J Immunol 180: 1148-1157.
70. Kundig TM, Shahinian A, Kawai K, Mittrucker HW, Sebzda E, et al. (1996) Duration of TCR stimulation determines costimulatory requirement of T cells. Immunity 5: 41-52.
71. Sigal LJ, Reiser H, Rock KL, (1998) The role of B7-1 and B7-2 costimulation for the generation of CTL responses in vivo. J Immunol 161: 2740-2745.
72. Chamberlain RS, Carroll MW, Bronte V, Hwu P, Warren S, et al. (1996) Costimulation enhances the active immunotherapy effect of recombinant anticancer vaccines. Cancer Research 56: 2832-2836.
73. Hodge JW, Chakraborty M, Kudo-Saito C, Garnett CT, Schlom J, (2005) Multiple Costimulatory Modalities Enhance CTL Avidity. J Immunol 174: 5994-6004.
74. Yang S, Hodge JW, Grosenbach DW, Schlom J, (2005) Vaccines with Enhanced Costimulation Maintain High Avidity Memory CTL. J Immunol 175: 3715-3723.
75. Norbury CC, Basta S, Donohue KB, Tscharke DC, Princiotta MF, et al. (2004) CD8+ T cell cross-priming via transfer of proteasome substrates. Sci 304: 1318-1321.
76. Chakrabarti S, Brechling K, Moss B, (1985) Vaccinia virus expression vector: coexpression of β-galactosidase provides visual screening of recombinant virus plaques. Mol Cell Biol 5: 3403-3409.
77. Lin LCW, Smith SA, Tscharke DC (2012) An intradermal model for vaccinia virus pathogenesis in mice. In: Isaacs SN, editor. Vaccinia virus and poxvirology: Methods and protocols. 2nd edition. Totowa, N.J.: Humana Press. pp. 147-159.