Viral sequestration of antigen subverts cross presentation to CD8 + T cells

PLoS Pathogens

Volumn 5, Issue 5, 2009, Pages

  Tewalt, Eric F ^a   Grant, Jean M ^a   Granger, Erica L ^a   Palmer, Douglas C ^b   Heuss, Neal D ^c   Gregerson, Dale S ^c   Restifo, Nicholas P ^b   Norbury, Christopher C ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; VIRUS ANTIGEN; VIRUS PROTEIN; VIRUS VACCINE; VIRUS VECTOR; HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2;

ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CROSS PRESENTATION; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNE SYSTEM; KILLER CELL; NONHUMAN; POXVIRUS; T LYMPHOCYTE ACTIVATION; ANIMAL; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; CELL LINE; HUMAN; IMMUNOLOGY; VACCINIA VIRUS; VIROLOGY;

POXVIRIDAE; VACCINIA VIRUS;

ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CROSS-PRIMING; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; VACCINIA VIRUS;

EID: 67249149345     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000457     Document Type: Article

References (49)

1. Yewdell JW, Norbury CC, Bennink JR (1999) Mechanisms of exogenous antigen presentation by MHC class I molecules in vitro and in vivo: implications for generating CD8+ T cell responses to infectious agents, tumors, transplants, and vaccines. Adv Immunol 73: 1-77. (Pubitemid 29300428)
2. Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, et al. (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404: 770-774. (Pubitemid 30212405)
3. Norbury CC, Basta S, Donohue KB, Tscharke DC, Princiotta MF, et al. (2004) CD8+ T cell cross-priming via transfer of proteasome substrates. Science 304: 1318-1321. (Pubitemid 38697427)
4. Norbury CC, Sigal LJ (2003) Cross priming or direct priming: is that really the question? Curr Opin Immunol 15: 82-88.
5. Yewdell JW, Hill AB (2002) Viral interference with antigen presentation. Nat Immunol 3: 1019-1025. (Pubitemid 35363652)
6. Coupar BE, Andrew ME, Both GW, Boyle DB (1986) Temporal regulation of influenza hemagglutinin expression in vaccinia virus recombinants and effects on the immune response. Eur J Immunol 16: 1479-1487. (Pubitemid 17025685)
7. Bronte V, Carroll MW, Goletz TJ, Wang M, Overwijk WW, et al. (1997) Antigen expression by dendritic cells correlates with the therapeutic effectiveness of a model recombinant poxvirus tumor vaccine. Proc Natl Acad Sci U S A 94: 3183-3188. (Pubitemid 27157285)
8. Donohue KB, Grant JM, Tewalt EF, Palmer DC, Theoret MR, et al. (2006) Cross-priming utilizes antigen not available to the direct presentation pathway. Immunology 119: 63-73. (Pubitemid 44201156)
9. Broder CC, Kennedy PE, Michaels F, Berger EA (1994) Expression of foreign genes in cultured human primary macrophages using recombinant vaccinia virus vectors. Gene 142: 167-174. (Pubitemid 24161365)
10. 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. (Pubitemid 34213428)
11. Orr MT, Edelmann KH, Vieira J, Corey L, Raulet DH, et al. (2005) Inhibition of MHC class I is a virulence factor in herpes simplex virus infection of mice. PLoS Pathog 1: e7. 10.1371/journal.ppat.0010007.
12. Holtappels R, Podlech J, Pahl-Seibert MF, Julch M, Thomas D, et al. (2004) Cytomegalovirus misleads its host by priming of CD8 T cells specific for an epitope not presented in infected tissues. J Exp Med 199: 131-136. (Pubitemid 38076485)
13. Kurts C, Sutherland RM, Davey G, Li M, Lew AM, et al. (1999) CD8 T cell ignorance or tolerance to islet antigens depends on antigen dose. Proc Natl Acad Sci U S A 96: 12703-12707. (Pubitemid 29513566)
14. Zinkernagel RM (2002) On cross-priming of MHC class I-specific CTL: rule or exception? Eur J Immunol 32: 2385-2392.
15. Norbury CC, Princiotta MF, Bacik I, Brutkiewicz RR, Wood P, et al. (2001) Multiple antigen-specific processing pathways for activating naive CD8+ T cells in vivo. J Immunol 166: 4355-4362. (Pubitemid 32233717)
16. Staveley-O'Carroll K, Schell TD, Jimenez M, Mylin LM, Tevethia MJ, et al. (2003) In vivo ligation of CD40 enhances priming against the endogenous tumor antigen and promotes CD8+ T cell effector function in SV40 T antigen transgenic mice. J Immunol 171: 697-707.
17. Katsafanas GC, Moss B (2007) Colocalization of transcription and translation within cytoplasmic poxvirus factories coordinates viral expression and subjugates host functions. Cell Host Microbe 2: 221-228. (Pubitemid 47500820)
18. Tolonen N, Doglio L, Schleich S, Krijnse Locker J (2001) Vaccinia virus DNA replication occurs in endoplasmic reticulum-enclosed cytoplasmic mini-nuclei. Mol Biol Cell 12: 2031-2046. (Pubitemid 33049697)
19. Cantin EM, Eberle R, Baldick JL, Moss B, Willey DE, et al. (1987) Expression of herpes simplex virus 1 glycoprotein B by a recombinant vaccinia virus and protection of mice against lethal herpes simplex virus 1 infection. Proc Natl Acad Sci U S A 84: 5908-5912.
20. Fowler AV, Zabin I (1977) The amino acid sequence of beta-galactosidase of Escherichia coli. Proc Natl Acad Sci U S A 74: 1507-1510. (Pubitemid 8086184)
21. Tewari MK, Sinnathamby G, Rajagopal D, Eisenlohr LC (2005) A cytosolic pathway for MHC class II-restricted antigen processing that is proteasome and TAP dependent. Nat Immunol 6: 287-294. (Pubitemid 41724766)
22. Gold MC, Munks MW, Wagner M, Koszinowski UH, Hill AB, et al. (2002) The Murine Cytomegalovirus Immunomodulatory Gene m152 Prevents Recognition of Infected Cells by M45-Specific CTL But Does Not Alter the Immunodominance of the M45-Specific CD8 T Cell Response In Vivo. J Immunol 169: 359-365. (Pubitemid 34686156)
23. Shen L, Rock KL (2004) Cellular protein is the source of cross-priming antigen in vivo. Proc Natl Acad Sci U S A 101: 3035-3040. (Pubitemid 38327730)
24. Husain M, Weisberg AS, Moss B (2007) Sequence-independent targeting of transmembrane proteins synthesized within vaccinia virus factories to nascent viral membranes. J Virol 81: 2646-2655. (Pubitemid 46447030)
25. Kovacsovics-Bankowski M, Rock KL (1995) A phagosome-to-cytosol pathway for exogenous antigens presented on MHC class I molecules. Science 267: 243-246.
26. Norbury CC, Hewlett LJ, Prescott AR, Shastri N, Watts C (1995) Class I MHC presentation of exogenous soluble antigen via macropinocytosis in bone marrow macrophages. Immunity 3: 783-791. (Pubitemid 26091151)
27. Ackerman AL, Giodini A, Cresswell P (2006) A role for the endoplasmic reticulum protein retrotranslocation machinery during crosspresentation by dendritic cells. Immunity 25: 607-617. (Pubitemid 44529035)
28. Lilley BN, Ploegh HL (2004) A membrane protein required for dislocation of misfolded proteins from the ER. Nature 429: 834-840. (Pubitemid 38843291)
29. Moutaftsi M, Peters B, Pasquetto V, Tscharke DC, Sidney J, et al. (2006) A consensus epitope prediction approach identifies the breadth of murine T(CD8+)-cell responses to vaccinia virus. Nat Biotechnol 24: 817-819. (Pubitemid 44086622)
30. 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. (Pubitemid 40130087)
31. Tscharke DC, Woo WP, Sakala IG, Sidney J, Sette A, et al. (2006) Poxvirus CD8+ T-cell determinants and cross-reactivity in BALB/c mice. J Virol 80: 6318-6323. (Pubitemid 43927434)
32. Drexler I, Staib C, Kastenmuller W, Stevanovic S, Schmidt B, et al. (2003) Identification of vaccinia virus epitope-specific HLA-A*0201- restricted T cells and comparative analysis of smallpox vaccines. Proc Natl Acad Sci U S A 100: 217-222. (Pubitemid 36078055)
33. Oseroff C, Kos F, Bui HH, Peters B, Pasquetto V, et al. (2005) HLA class I-restricted responses to vaccinia recognize a broad array of proteins mainly involved in virulence and viral gene regulation. Proc Natl Acad Sci U S A 102: 13980-13985. (Pubitemid 41377689)
34. Pasquetto V, Bui HH, Giannino R, Banh C, Mirza F, et al. (2005) HLA-A*0201, HLA-A*1101, and HLA-B*0702 transgenic mice recognize numerous poxvirus determinants from a wide variety of viral gene products. J Immunol 175: 5504-5515. (Pubitemid 41456438)
35. Moutaftsi M, Bui HH, Peters B, Sidney J, Salek-Ardakani S, et al. (2007) Vaccinia virus-specific CD4+ T cell responses target a set of antigens largely distinct from those targeted by CD8+ T cell responses. J Immunol 178: 6814-6820. (Pubitemid 46847406)
36. Risco C, Rodriguez JR, Demkowicz W, Heljasvaara R, Carrascosa JL, et al. (1999) The vaccinia virus 39-kDa protein forms a stable complex with the p4a/4a major core protein early in morphogenesis. Virology 265: 375-386. (Pubitemid 30022231)
37. Gubser C, Hue S, Kellam P, Smith GL (2004) Poxvirus genomes: a phylogenetic analysis. J Gen Virol 85: 105-117. (Pubitemid 38128875)
38. Dasgupta A, Hammarlund E, Slifka MK, Fruh K (2007) Cowpox Virus Evades CTL Recognition and Inhibits the Intracellular Transport of MHC Class I Molecules. J Immunol 178: 1654-1661. (Pubitemid 46154637)
39. Byun M, Wang X, Pak M, Hansen TH, Yokoyama WM (2007) Cowpox virus exploits the endoplasmic reticulum retention pathway to inhibit MHC class I transport to the cell surface. Cell Host Microbe 2: 306-315. (Pubitemid 350056394)
40. Hogquist KA, Jameson SC, Heath WR, Howard JL, Bevan MJ, et al. (1994) T cell receptor antagonist peptides induce positive selection. Cell 76: 17-27. (Pubitemid 24035278)
41. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, et al. (1992) RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68: 869-877.
42. Mueller SN, Heath W, McLain JD, Carbone FR, Jones CM (2002) Characterization of two TCR transgenic mouse lines specificfor herpes simplex virus. Immunol Cell Biol 80: 156-163. (Pubitemid 34298088)
43. Kouskoff V, Signorelli K, Benoist C, Mathis D (1995) Cassette vectors directing expression of T cell receptor genes in transgenic mice. J Immunol Methods 180: 273-280.
44. Broder CC, Berger EA (1993) CD4 molecules with a diversity of mutations encompassing the CDR3 region efficiently support human immunodeficiency virus type 1 envelope glycoprotein-mediated cell fusion. J Virol 67: 913-926. (Pubitemid 23032070)
45. Overwijk WW, Surman DR, Tsung K, Restifo NP (1997) Identification of a Kb-restricted CTL epitope of beta-galactosidase: potential use in development of immunization protocols for "self" antigens. Methods 12: 117-123.
46. Blasco R, Moss B (1995) Selection of recombinant vaccinia viruses on the basis of plaque formation. Gene 158: 157-162.
47. Pretell J, Greenfield RS, Tevethia SS (1979) Biology of simian virus 40 (SV40) transplantation antigen (TrAg). V In vitro demonstration of SV40 TrAg in SV40 infected nonpermissive mouse cells by the lymphocyte mediated cytotoxicity assay. Virology 97: 32-41.
48. Norbury CC, Chambers BJ, Prescott AR, Ljunggren HG, Watts C (1997) Constitutive macropinocytosis allows TAP-dependent major histocompatibility complex class I presentation of exogenous soluble antigen by bone marrow-derived dendritic cells. Eur J Immunol 27: 280-288. (Pubitemid 27046089)
49. Yuwen H, Cox JH, Yewdell JW, Bennink JR, Moss B (1993) Nuclear localization of a double-stranded RNA-binding protein encoded by the vaccinia virus E3L gene. Virology 195: 732-744. (Pubitemid 23226198)