A Negative Feedback Modulator of Antigen Processing Evolved from a Frameshift in the Cowpox Virus Genome

PLoS Pathogens

Volumn 10, Issue 12, 2014, Pages

  Lin, Jiacheng ^a   Eggensperger, Sabine ^a   Hank, Susanne ^a   Wycisk, Agnes I ^a   Wieneke, Ralph ^a   Mayerhofer, Peter U ^a   Tampé, Robert ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CPXV012 PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MEMBRANE PROTEIN; MESSENGER RNA; PLASMID DNA; PROTEOLIPOSOME; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 2; UNCLASSIFIED DRUG; VIRUS PROTEIN; ABC TRANSPORTER; HLA ANTIGEN CLASS 1; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING (TAP); VIRUS ANTIGEN;

ANIMAL CELL; ANTIGEN BINDING; ANTIGEN PRESENTATION; ARTICLE; ATPASE ACTIVITY ASSAY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; COWPOX VIRUS; ENDOPLASMIC RETICULUM MEMBRANE; FLOW CYTOMETRY; GENETIC TRANSFECTION; GENOME; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; HYDROLYSIS; IMMUNE EVASION; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MOLECULAR CLONING; NEGATIVE FEEDBACK; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RETICULOCYTE LYSATE; SPODOPTERA FRUGIPERDA; VIRUS RECOMBINANT; WESTERN BLOTTING; AMINO ACID SEQUENCE; ANIMAL; ENDOPLASMIC RETICULUM; FEEDBACK SYSTEM; FRAMESHIFT MUTATION; GENETICS; HELA CELL LINE; IMMUNOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; SF9 CELL LINE; VIRUS GENOME;

COWPOX VIRUS; VARIOLA VIRUS;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, VIRAL; ATP-BINDING CASSETTE TRANSPORTERS; COWPOX VIRUS; ENDOPLASMIC RETICULUM; FEEDBACK, PHYSIOLOGICAL; FRAMESHIFT MUTATION; GENOME, VIRAL; HELA CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MOLECULAR SEQUENCE DATA; SF9 CELLS;

EID: 84919623114     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004554     Document Type: Article

References (69)

1. Vossen MT, Westerhout EM, Soderberg-Naucler C, Wiertz EJ, (2002) Viral immune evasion: a masterpiece of evolution. Immunogenetics 54: 527–542.
2. Brodsky FM, (1999) Stealth, sabotage and exploitation. Immunol Rev 168: 5–11.
3. Hansen TH, Bouvier M, (2009) MHC class I antigen presentation: learning from viral evasion strategies. Nat Rev Immunol 9: 503–513.
4. Abendroth A, Arvin A, (1999) Varicella-zoster virus immune evasion. Immunol Rev 168: 143–156.
5. Blum JS, Wearsch PA, Cresswell P, (2013) Pathways of antigen processing. Annu Rev Immunol 31: 443–473.
6. Ouwendijk WJ, Mahalingam R, de Swart RL, Haagmans BL, van Amerongen G, et al. (2013) T-Cell tropism of simian varicella virus during primary infection. PLoS Pathog 9: e1003368.
7. Voigt S, Mesci A, Ettinger J, Fine JH, Chen P, et al. (2007) Cytomegalovirus evasion of innate immunity by subversion of the NKR-P1B:Clr-b missing-self axis. Immunity 26: 617–627.
8. Neefjes JJ, Hämmerling GJ, Momburg F, (1993) Folding and assembly of major histocompatibility complex class I heterodimers in the endoplasmic reticulum of intact cells precedes the binding of peptide. J Exp Med 178: 1971–1980.
9. Parcej D, Tampé R, (2010) ABC proteins in antigen translocation and viral inhibition. Nat Chem Biol 6: 572–580.
10. Hulpke S, Tampé R, (2013) The MHC I loading complex: a multitasking machinery in adaptive immunity. Trends Biochem Sci 38: 412–420.
11. Koch J, Guntrum R, Heintke S, Kyritsis C, Tampé R, (2004) Functional dissection of the transmembrane domains of the transporter associated with antigen processing (TAP). J Biol Chem 279: 10142–10147.
12. Procko E, Raghuraman G, Wiley DC, Raghavan M, Gaudet R, (2005) Identification of domain boundaries within the N-termini of TAP1 and TAP2 and their importance in tapasin binding and tapasin-mediated increase in peptide loading of MHC class I. Immunol Cell Biol 83: 475–482.
13. Hulpke S, Tomioka M, Kremmer E, Ueda K, Abele R, et al. (2012) Direct evidence that the N-terminal extensions of the TAP complex act as autonomous interaction scaffolds for the assembly of the MHC I peptide-loading complex. Cell Mol Life Sci 69: 3317–3327.
14. Hulpke S, Baldauf C, Tampé R, (2012) Molecular architecture of the MHC I peptide-loading complex: one tapasin molecule is essential and sufficient for antigen processing. FASEB J 26: 5071–5080.
15. Alzhanova D, Edwards DM, Hammarlund E, Scholz IG, Horst D, et al. (2009) Cowpox virus inhibits the transporter associated with antigen processing to evade T cell recognition. Cell Host Microbe 6: 433–445.
16. Byun M, Verweij MC, Pickup DJ, Wiertz EJ, Hansen TH, et al. (2009) Two mechanistically distinct immune evasion proteins of cowpox virus combine to avoid antiviral CD8 T cells. Cell Host Microbe 6: 422–432.
17. Vorou RM, Papavassiliou VG, Pierroutsakos IN, (2008) Cowpox virus infection: an emerging health threat. Curr Opin Infect Dis 21: 153–156.
18. Bourquain D, Dabrowski PW, Nitsche A, (2013) Comparison of host cell gene expression in cowpox, monkeypox or vaccinia virus-infected cells reveals virus-specific regulation of immune response genes. Virol J 10: 61.
19. Czerny CP, Eis-Hubinger AM, Mayr A, Schneweis KE, Pfeiff B, (1991) Animal poxviruses transmitted from cat to man: current event with lethal end. Zentralbl Veterinarmed B 38: 421–431.
20. Pelkonen PM, Tarvainen K, Hynninen A, Kallio ER, Henttonen K, et al. (2003) Cowpox with severe generalized eruption, Finland. Emerg Infect Dis 9: 1458–1461.
21. Ahn K, Meyer TH, Uebel S, Sempé P, Djaballah H, et al. (1996) Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47. EMBO J 15: 3247–3255.
22. Tomazin R, Hill AB, Jugovic P, York I, van Endert P, et al. (1996) Stable binding of the herpes simplex virus ICP47 protein to the peptide binding site of TAP. EMBO J 15: 3256–3266.
23. Aisenbrey C, Sizun C, Koch J, Herget M, Abele R, et al. (2006) Structure and dynamics of membrane-associated ICP47, a viral inhibitor of the MHC I antigen-processing machinery. J Biol Chem 281: 30365–30372.
24. Hewitt EW, Gupta SS, Lehner PJ, (2001) The human cytomegalovirus gene product US6 inhibits ATP binding by TAP. EMBO J 20: 387–396.
25. Kyritsis C, Gorbulev S, Hutschenreiter S, Pawlitschko K, Abele R, et al. (2001) Molecular mechanism and structural aspects of transporter associated with antigen processing inhibition by the cytomegalovirus protein US6. J Biol Chem 276: 48031–48039.
26. Ressing ME, Keating SE, van Leeuwen D, Koppers-Lalic D, Pappworth IY, et al. (2005) Impaired transporter associated with antigen processing-dependent peptide transport during productive EBV infection. J Immunol 174: 6829–6838.
27. Horst D, van Leeuwen D, Croft NP, Garstka MA, Hislop AD, et al. (2009) Specific targeting of the EBV lytic phase protein BNLF2a to the transporter associated with antigen processing results in impairment of HLA class I-restricted antigen presentation. J Immunol 182: 2313–2324.
28. Croft NP, Shannon-Lowe C, Bell AI, Horst D, Kremmer E, et al. (2009) Stage-specific inhibition of MHC class I presentation by the Epstein-Barr virus BNLF2a protein during virus lytic cycle. PLoS Pathog 5: e1000490.
29. Wycisk AI, Lin J, Loch S, Hobohm K, Funke J, et al. (2011) Epstein-Barr viral BNLF2a protein hijacks the tail-anchored protein insertion machinery to block antigen processing by the transport complex TAP. J Biol Chem 286: 41402–41412.
30. McCoy WHt, Wang X, Yokoyama WM, Hansen TH, Fremont DH, (2013) Cowpox virus employs a two-pronged strategy to outflank MHCI antigen presentation. Mol Immunol 55: 156–158.
31. Demirel O, Jan I, Wolters D, Blanz J, Saftig P, et al. (2012) The lysosomal polypeptide transporter TAPL is stabilized by interaction with LAMP-1 and LAMP-2. J Cell Sci 125: 4230–4240.
32. Horst D, Favaloro V, Vilardi F, van Leeuwen HC, Garstka MA, et al. (2011) EBV protein BNLF2a exploits host tail-anchored protein integration machinery to inhibit TAP. J Immunol 186: 3594–3605.
33. Lacaille VG, Androlewicz MJ, (1998) Herpes simplex virus inhibitor ICP47 destabilizes the transporter associated with antigen processing (TAP) heterodimer. J Biol Chem 273: 17386–17390.
34. Carroll DS, Emerson GL, Li Y, Sammons S, Olson V, et al. (2011) Chasing Jenner's vaccine: revisiting cowpox virus classification. PLoS One 6: e23086.
35. Shchelkunov SN, Safronov PF, Totmenin AV, Petrov NA, Ryazankina OI, et al. (1998) The genomic sequence analysis of the left and right species-specific terminal region of a cowpox virus strain reveals unique sequences and a cluster of intact ORFs for immunomodulatory and host range proteins. Virology 243: 432–460.
36. Gubser C, Hue S, Kellam P, Smith GL, (2004) Poxvirus genomes: a phylogenetic analysis. J Gen Virol 85: 105–117.
37. Uebel S, Kraas W, Kienle S, Wiesmuller KH, Jung G, et al. (1997) Recognition principle of the TAP transporter disclosed by combinatorial peptide libraries. Proc Natl Acad Sci U S A 94: 8976–8981.
38. Gorbulev S, Abele R, Tampé R, (2001) Allosteric crosstalk between peptide-binding, transport, and ATP hydrolysis of the ABC transporter TAP. Proc Natl Acad Sci U S A 98: 3732–3737.
39. Schumacher TN, Kantesaria DV, Heemels MT, Ashton-Rickardt PG, Shepherd JC, et al. (1994) Peptide length and sequence specificity of the mouse TAP1/TAP2 translocator. J Exp Med 179: 533–540.
40. Schölz C, Parcej D, Ejsing CS, Robenek H, Urbatsch IL, et al. (2011) Specific lipids modulate the transporter associated with antigen processing (TAP). J Biol Chem 286: 13346–13356.
41. Grossmann N, Vakkasoglu AS, Hulpke S, Abele R, Gaudet R, et al. (2014) Mechanistic determinants of the directionality and energetics of active export by a heterodimeric ABC transporter. Nat Commun 5: 5419.
42. Revilleza MJ, Wang R, Mans J, Hong M, Natarajan K, et al. (2011) How the virus outsmarts the host: function and structure of cytomegalovirus MHC-I-like molecules in the evasion of natural killer cell surveillance. J Biomed Biotechnol 2011: 724607.
43. Ressing ME, Luteijn RD, Horst D, Wiertz EJ, (2013) Viral interference with antigen presentation: trapping TAP. Mol Immunol 55: 139–142.
44. Lehner PJ, Hewitt EW, Römisch K, (2000) Antigen presentation: peptides and proteins scramble for the exit. Curr Biol 10: R839–842.
45. Todd DJ, Lee AH, Glimcher LH, (2008) The endoplasmic reticulum stress response in immunity and autoimmunity. Nat Rev Immunol 8: 663–674.
46. Ulianich L, Terrazzano G, Annunziatella M, Ruggiero G, Beguinot F, et al. (2011) ER stress impairs MHC Class I surface expression and increases susceptibility of thyroid cells to NK-mediated cytotoxicity. Biochim Biophys Acta 1812: 431–438.
47. Bartoszewski R, Brewer JW, Rab A, Crossman DK, Bartoszewska S, et al. (2011) The unfolded protein response (UPR)-activated transcription factor X-box-binding protein 1 (XBP1) induces microRNA-346 expression that targets the human antigen peptide transporter 1 (TAP1) mRNA and governs immune regulatory genes. J Biol Chem 286: 41862–41870.
48. Shepherd JC, Schumacher TN, Ashton-Rickardt PG, Imaeda S, Ploegh HL, et al. (1993) TAP1-dependent peptide translocation in vitro is ATP dependent and peptide selective. Cell 74: 577–584.
49. Koopmann JO, Albring J, Huter E, Bulbuc N, Spee P, et al. (2000) Export of antigenic peptides from the endoplasmic reticulum intersects with retrograde protein translocation through the Sec61p channel. Immunity 13: 117–127.
50. Seet BT, Johnston JB, Brunetti CR, Barrett JW, Everett H, et al. (2003) Poxviruses and immune evasion. Annu Rev Immunol 21: 377–423.
51. 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.
52. 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.
53. McCoy WHt, Wang X, Yokoyama WM, Hansen TH, Fremont DH, (2012) Structural mechanism of ER retrieval of MHC class I by cowpox. PLoS Biol 10: e1001432.
54. Gainey MD, Rivenbark JG, Cho H, Yang L, Yokoyama WM, (2012) Viral MHC class I inhibition evades CD8+ T-cell effector responses in vivo but not CD8+ T-cell priming. Proc Natl Acad Sci U S A 109: E3260–3267.
55. Campbell KS, Hasegawa J, (2013) Natural killer cell biology: an update and future directions. J Allergy Clin Immunol 132: 536–544.
56. Ljunggren HG, Karre K, (1990) In search of the ‘missing self’: MHC molecules and NK cell recognition. Immunol Today 11: 237–244.
57. Campbell JA, Trossman DS, Yokoyama WM, Carayannopoulos LN, (2007) Zoonotic orthopoxviruses encode a high-affinity antagonist of NKG2D. J Exp Med 204: 1311–1317.
58. Raulet DH, (2003) Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol 3: 781–790.
59. Iizuka K, Naidenko OV, Plougastel BF, Fremont DH, Yokoyama WM, (2003) Genetically linked C-type lectin-related ligands for the NKRP1 family of natural killer cell receptors. Nat Immunol 4: 801–807.
60. Carlyle JR, Jamieson AM, Gasser S, Clingan CS, Arase H, et al. (2004) Missing self-recognition of Ocil/Clr-b by inhibitory NKR-P1 natural killer cell receptors. Proc Natl Acad Sci U S A 101: 3527–3532.
61. Luteijn RD, Hoelen H, Kruse E, van Leeuwen WF, Grootens J, et al. (2014) Cowpox virus protein CPXV012 eludes CTLs by blocking ATP binding to TAP. J Immunol 193: 1578–1589.
62. Parcej D, Guntrum R, Schmidt S, Hinz A, Tampé R, (2013) Multicolour fluorescence-detection size-exclusion chromatography for structural genomics of membrane multiprotein complexes. PLoS One 8: e67112.
63. Herget M, Kreissig N, Kolbe C, Schölz C, Tampé R, et al. (2009) Purification and reconstitution of the antigen transport complex TAP: a prerequisite for determination of peptide stoichiometry and ATP hydrolysis. J Biol Chem 284: 33740–33749.
64. Meyer TH, van Endert PM, Uebel S, Ehring B, Tampé R, (1994) Functional expression and purification of the ABC transporter complex associated with antigen processing (TAP) in insect cells. FEBS Lett 351: 443–447.
65. Nijenhuis M, Hämmerling GJ, (1996) Multiple regions of the transporter associated with antigen processing (TAP) contribute to its peptide binding site. J Immunol 157: 5467–5477.
66. Abacioglu YH, Fouts TR, Laman JD, Claassen E, Pincus SH, et al. (1994) Epitope mapping and topology of baculovirus-expressed HIV-1 gp160 determined with a panel of murine monoclonal antibodies. AIDS Res Hum Retroviruses 10: 371–381.
67. Stam NJ, Spits H, Ploegh HL, (1986) Monoclonal antibodies raised against denatured HLA-B locus heavy chains permit biochemical characterization of certain HLA-C locus products. J Immunol 137: 2299–2306.
68. Saksena S, Shao Y, Braunagel SC, Summers MD, Johnson AE, (2004) Cotranslational integration and initial sorting at the endoplasmic reticulum translocon of proteins destined for the inner nuclear membrane. Proc Natl Acad Sci U S A 101: 12537–12542.
69. Henkel RD, VandeBerg JL, Walsh RA, (1988) A microassay for ATPase. Anal Biochem 169: 312–318.