Viral Inhibition of the Transporter Associated with Antigen Processing (TAP): A Striking Example of Functional Convergent Evolution
Herpesviruses are large DNA viruses that are highly abundant within their host populations. Even in the presence of a healthy immune system, these viruses manage to cause lifelong infections. This persistence is partially mediated by the virus entering latency, a phase of infection characterized by limited viral protein expression. Moreover, herpesviruses have devoted a significant part of their coding capacity to immune evasion strategies. It is believed that the close coexistence of herpesviruses and their hosts has resulted in the evolution of viral proteins that specifically attack multiple arms of the host immune system. Cytotoxic T lymphocytes (CTLs) play an important role in antiviral immunity. CTLs recognize their target through viral peptides presented in the context of MHC molecules at the cell surface. Every herpesvirus studied to date encodes multiple immune evasion molecules that effectively interfere with specific steps of the MHC class I antigen presentation pathway. The transporter associated with antigen processing (TAP) plays a key role in the loading of viral peptides onto MHC class I molecules. This is reflected by the numerous ways herpesviruses have developed to block TAP function. In this review, we describe the characteristics and mechanisms of action of all known virus-encoded TAP inhibitors. Orthologs of these proteins encoded by related viruses are identified, and the conservation of TAP inhibition is discussed. A phylogenetic analysis of members of the family Herpesviridae is included to study the origin of these molecules. In addition, we discuss the characteristics of the first TAP inhibitor identified outside the herpesvirus family, namely, in cowpox virus. The strategies of TAP inhibition employed by viruses are very distinct and are likely to have been acquired independently during evolution. These findings and the recent discovery of a non-herpesvirus TAP inhibitor represent a striking example of functional convergent evolution.
Vyšlo v časopise:
Viral Inhibition of the Transporter Associated with Antigen Processing (TAP): A Striking Example of Functional Convergent Evolution. PLoS Pathog 11(4): e32767. doi:10.1371/journal.ppat.1004743
Kategorie:
Review
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004743
Souhrn
Herpesviruses are large DNA viruses that are highly abundant within their host populations. Even in the presence of a healthy immune system, these viruses manage to cause lifelong infections. This persistence is partially mediated by the virus entering latency, a phase of infection characterized by limited viral protein expression. Moreover, herpesviruses have devoted a significant part of their coding capacity to immune evasion strategies. It is believed that the close coexistence of herpesviruses and their hosts has resulted in the evolution of viral proteins that specifically attack multiple arms of the host immune system. Cytotoxic T lymphocytes (CTLs) play an important role in antiviral immunity. CTLs recognize their target through viral peptides presented in the context of MHC molecules at the cell surface. Every herpesvirus studied to date encodes multiple immune evasion molecules that effectively interfere with specific steps of the MHC class I antigen presentation pathway. The transporter associated with antigen processing (TAP) plays a key role in the loading of viral peptides onto MHC class I molecules. This is reflected by the numerous ways herpesviruses have developed to block TAP function. In this review, we describe the characteristics and mechanisms of action of all known virus-encoded TAP inhibitors. Orthologs of these proteins encoded by related viruses are identified, and the conservation of TAP inhibition is discussed. A phylogenetic analysis of members of the family Herpesviridae is included to study the origin of these molecules. In addition, we discuss the characteristics of the first TAP inhibitor identified outside the herpesvirus family, namely, in cowpox virus. The strategies of TAP inhibition employed by viruses are very distinct and are likely to have been acquired independently during evolution. These findings and the recent discovery of a non-herpesvirus TAP inhibitor represent a striking example of functional convergent evolution.
Zdroje
1. McGeoch DJ, Gatherer D (2005) Integrating reptilian herpesviruses into the family herpesviridae. J Virol 79: 725–731. 15613300
2. Reits EA, Vos JC, Gromme M, Neefjes J (2000) The major substrates for TAP in vivo are derived from newly synthesized proteins. Nature 404: 774–778. 10783892
3. 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. 12648452
4. Lehner PJ, Surman MJ, Cresswell P (1998) Soluble tapasin restores MHC class I expression and function in the tapasin-negative cell line. 220. Immunity 8: 221–231. 9492003
5. Sadasivan B, Lehner PJ, Ortmann B, Spies T, Cresswell P (1996) Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity 5: 103–114. 8769474
6. Wearsch PA, Cresswell P (2007) Selective loading of high-affinity peptides onto major histocompatibility complex class I molecules by the tapasin-ERp57 heterodimer. Nat Immunol 8: 873–881. 17603487
7. Kienast A, Preuss M, Winkler M, Dick TP (2007) Redox regulation of peptide receptivity of major histocompatibility complex class I molecules by ERp57 and tapasin. Nat Immunol 8: 864–872. 17603488
8. Koch J, Guntrum R, Tampe R (2006) The first N-terminal transmembrane helix of each subunit of the antigenic peptide transporter TAP is essential for independent tapasin binding. FEBS Lett 580: 4091–4096. 16828748
9. Leonhardt RM, Keusekotten K, Bekpen C, Knittler MR (2005) Critical role for the tapasin-docking site of TAP2 in the functional integrity of the MHC class I-peptide-loading complex. J Immunol 175: 5104–5114. 16210614
10. Peaper DR, Wearsch PA, Cresswell P (2005) Tapasin and ERp57 form a stable disulfide-linked dimer within the MHC class I peptide-loading complex. EMBO J 24: 3613–3623. 16193070
11. Raghavan M, Del Cid N, Rizvi SM, Peters LR (2008) MHC class I assembly: out and about. Trends Immunol 29: 436–443. doi: 10.1016/j.it.2008.06.004 18675588
12. Wearsch PA, Cresswell P (2008) The quality control of MHC class I peptide loading. Curr Opin Cell Biol 20: 624–631. doi: 10.1016/j.ceb.2008.09.005 18926908
13. Davison AJ, Eberle R, Ehlers B, Hayward GS, McGeoch DJ, et al. (2009) The order Herpesvirales. Arch Virol 154: 171–177. doi: 10.1007/s00705-008-0278-4 19066710
14. Staras SA, Dollard SC, Radford KW, Flanders WD, Pass RF, et al. (2006) Seroprevalence of cytomegalovirus infection in the United States, 1988–1994. Clin Infect Dis 43: 1143–1151. 17029132
15. Kilgore PE, Kruszon-Moran D, Seward JF, Jumaan A, Van Loon FP, et al. (2003) Varicella in Americans from NHANES III: implications for control through routine immunization. J Med Virol 70 Suppl 1: S111–118. 12627498
16. Epstein MA, Achong BG, Barr YM (1964) VIRUS PARTICLES IN CULTURED LYMPHOBLASTS FROM BURKITT'S LYMPHOMA. Lancet 1: 702–703. 14107961
17. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, et al. (1994) Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266: 1865–1869. 7997879
18. Kenneson A, Cannon MJ (2007) Review and meta-analysis of the epidemiology of congenital cytomegalovirus (CMV) infection. Rev Med Virol 17: 253–276. 17579921
19. Ressing ME, Horst D, Griffin BD, Tellam J, Zuo J, et al. (2008) Epstein-Barr virus evasion of CD8(+) and CD4(+) T cell immunity via concerted actions of multiple gene products. Semin Cancer Biol 18: 397–408. doi: 10.1016/j.semcancer.2008.10.008 18977445
20. Liang C, Lee JS, Jung JU (2008) Immune evasion in Kaposi's sarcoma-associated herpes virus associated oncogenesis. Semin Cancer Biol 18: 423–436. doi: 10.1016/j.semcancer.2008.09.003 18948197
21. Middeldorp JM, Pegtel DM (2008) Multiple roles of LMP1 in Epstein-Barr virus induced immune escape. Semin Cancer Biol 18: 388–396. doi: 10.1016/j.semcancer.2008.10.004 19013244
22. Fenwick ML, Clark J (1982) Early and delayed shut-off of host protein synthesis in cells infected with herpes simplex virus. J Gen Virol 61 (Pt l): 121–125. 6288847
23. Kwong AD, Frenkel N (1987) Herpes simplex virus-infected cells contain a function(s) that destabilizes both host and viral mRNAs. Proc Natl Acad Sci U S A 84: 1926–1930. 3031658
24. Rowe M, Glaunsinger B, van Leeuwen D, Zuo J, Sweetman D, et al. (2007) Host shutoff during productive Epstein-Barr virus infection is mediated by BGLF5 and may contribute to immune evasion. Proc Natl Acad Sci U S A 104: 3366–3371. 17360652
25. Zuo J, Thomas W, van Leeuwen D, Middeldorp JM, Wiertz EJ, et al. (2008) The DNase of gammaherpesviruses impairs recognition by virus-specific CD8+ T cells through an additional host shutoff function. J Virol 82: 2385–2393. 18094150
26. Glaunsinger B, Chavez L, Ganem D (2005) The exonuclease and host shutoff functions of the SOX protein of Kaposi's sarcoma-associated herpesvirus are genetically separable. J Virol 79: 7396–7401. 15919895
27. Wiertz EJ, Jones TR, Sun L, Bogyo M, Geuze HJ, et al. (1996) The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84: 769–779. 8625414
28. Park B, Spooner E, Houser BL, Strominger JL, Ploegh HL (2010) The HCMV membrane glycoprotein US10 selectively targets HLA-G for degradation. J Exp Med 207: 2033–2041. doi: 10.1084/jem.20091793 20713594
29. Wiertz EJ, Tortorella D, Bogyo M, Yu J, Mothes W, et al. (1996) Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384: 432–438. 8945469
30. Reusch U, Muranyi W, Lucin P, Burgert HG, Hengel H, et al. (1999) A cytomegalovirus glycoprotein re-routes MHC class I complexes to lysosomes for degradation. EMBO J 18: 1081–1091. 10022849
31. Lybarger L, Wang X, Harris MR, Virgin HWt, Hansen TH (2003) Virus subversion of the MHC class I peptide-loading complex. Immunity 18: 121–130. 12530981
32. Stevenson PG, May JS, Smith XG, Marques S, Adler H, et al. (2002) K3-mediated evasion of CD8(+) T cells aids amplification of a latent gamma-herpesvirus. Nat Immunol 3: 733–740. 12101398
33. Wang X, Herr RA, Chua WJ, Lybarger L, Wiertz EJ, et al. (2007) Ubiquitination of serine, threonine, or lysine residues on the cytoplasmic tail can induce ERAD of MHC-I by viral E3 ligase mK3. J Cell Biol 177: 613–624. 17502423
34. Jones TR, Wiertz EJ, Sun L, Fish KN, Nelson JA, et al. (1996) Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class I heavy chains. Proc Natl Acad Sci U S A 93: 11327–11333. 8876135
35. Ziegler H, Thale R, Lucin P, Muranyi W, Flohr T, et al. (1997) A mouse cytomegalovirus glycoprotein retains MHC class I complexes in the ERGIC/cis-Golgi compartments. Immunity 6: 57–66. 9052837
36. Zuo J, Currin A, Griffin BD, Shannon-Lowe C, Thomas WA, et al. (2009) The Epstein-Barr virus G-protein-coupled receptor contributes to immune evasion by targeting MHC class I molecules for degradation. PLoS Pathog 5: e1000255. doi: 10.1371/journal.ppat.1000255 19119421
37. Coscoy L, Ganem D (2000) Kaposi's sarcoma-associated herpesvirus encodes two proteins that block cell surface display of MHC class I chains by enhancing their endocytosis. Proc Natl Acad Sci U S A 97: 8051–8056. 10859362
38. Ishido S, Wang C, Lee BS, Cohen GB, Jung JU (2000) Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins. J Virol 74: 5300–5309. 10799607
39. Lehner PJ, Hoer S, Dodd R, Duncan LM (2005) Downregulation of cell surface receptors by the K3 family of viral and cellular ubiquitin E3 ligases. Immunol Rev 207: 112–125. 16181331
40. Hulpke S, Baldauf C, Tampe 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. doi: 10.1096/fj.12-217489 22923333
41. Koch J, Guntrum R, Heintke S, Kyritsis C, Tampe R (2004) Functional dissection of the transmembrane domains of the transporter associated with antigen processing (TAP). J Biol Chem 279: 10142–10147. 14679198
42. Androlewicz MJ, Cresswell P (1994) Human transporters associated with antigen processing possess a promiscuous peptide-binding site. Immunity 1: 7–14. 7889401
43. Koopmann JO, Post M, Neefjes JJ, Hammerling GJ, Momburg F (1996) Translocation of long peptides by transporters associated with antigen processing (TAP). Eur J Immunol 26: 1720–1728. 8765012
44. Momburg F, Roelse J, Hammerling GJ, Neefjes JJ (1994) Peptide size selection by the major histocompatibility complex-encoded peptide transporter. J Exp Med 179: 1613–1623. 8163941
45. 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. 8294864
46. van Endert PM, Tampe R, Meyer TH, Tisch R, Bach JF, et al. (1994) A sequential model for peptide binding and transport by the transporters associated with antigen processing. Immunity 1: 491–500. 7895159
47. Nijenhuis M, Hammerling GJ (1996) Multiple regions of the transporter associated with antigen processing (TAP) contribute to its peptide binding site. J Immunol 157: 5467–5477. 8955196
48. Armandola EA, Momburg F, Nijenhuis M, Bulbuc N, Fruh K, et al. (1996) A point mutation in the human transporter associated with antigen processing (TAP2) alters the peptide transport specificity. Eur J Immunol 26: 1748–1755. 8765016
49. Corradi V, Singh G, Tieleman DP (2012) The human transporter associated with antigen processing: molecular models to describe peptide binding competent states. J Biol Chem 287: 28099–28111. doi: 10.1074/jbc.M112.381251 22700967
50. Procko E, Ferrin-O'Connell I, Ng SL, Gaudet R (2006) Distinct structural and functional properties of the ATPase sites in an asymmetric ABC transporter. Mol Cell 24: 51–62. 17018292
51. Chen M, Abele R, Tampe R (2003) Peptides induce ATP hydrolysis at both subunits of the transporter associated with antigen processing. J Biol Chem 278: 29686–29692. 12777379
52. Lapinski PE, Raghuraman G, Raghavan M (2003) Nucleotide interactions with membrane-bound transporter associated with antigen processing proteins. J Biol Chem 278: 8229–8237. 12501238
53. Perria CL, Rajamanickam V, Lapinski PE, Raghavan M (2006) Catalytic site modifications of TAP1 and TAP2 and their functional consequences. J Biol Chem 281: 39839–39851. 17068338
54. Saveanu L, Daniel S, van Endert PM (2001) Distinct functions of the ATP binding cassettes of transporters associated with antigen processing: a mutational analysis of Walker A and B sequences. J Biol Chem 276: 22107–22113. 11290739
55. Dawson RJ, Locher KP (2006) Structure of a bacterial multidrug ABC transporter. Nature 443: 180–185. 16943773
56. Hohl M, Briand C, Grutter MG, Seeger MA (2012) Crystal structure of a heterodimeric ABC transporter in its inward-facing conformation. Nat Struct Mol Biol 19: 395–402. doi: 10.1038/nsmb.2267 22447242
57. Kim J, Wu S, Tomasiak TM, Mergel C, Winter MB, et al. (2015) Subnanometre-resolution electron cryomicroscopy structure of a heterodimeric ABC exporter. Nature 517: 396–400. doi: 10.1038/nature13872 25363761
58. Kodan A, Yamaguchi T, Nakatsu T, Sakiyama K, Hipolito CJ, et al. (2014) Structural basis for gating mechanisms of a eukaryotic P-glycoprotein homolog. Proc Natl Acad Sci U S A 111: 4049–4054. doi: 10.1073/pnas.1321562111 24591620
59. Srinivasan V, Pierik AJ, Lill R (2014) Crystal structures of nucleotide-free and glutathione-bound mitochondrial ABC transporter Atm1. Science 343: 1137–1140. doi: 10.1126/science.1246729 24604199
60. Geng J, Sivaramakrishnan S, Raghavan M (2013) Analyses of conformational states of the transporter associated with antigen processing (TAP) protein in a native cellular membrane environment. J Biol Chem 288: 37039–37047. doi: 10.1074/jbc.M113.504696 24196954
61. 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. doi: 10.1038/ncomms6419 25377891
62. Mayerhofer PU, Tampe R (2014) Antigen Translocation Machineries in Adaptive Immunity and Viral Immune Evasion. J Mol Biol. 427: 1102–1118 doi: 10.1016/j.jmb.2014.09.006 25224907
63. Spies T, DeMars R (1991) Restored expression of major histocompatibility class I molecules by gene transfer of a putative peptide transporter. Nature 351: 323–324. 2034277
64. Spies T, Cerundolo V, Colonna M, Cresswell P, Townsend A, et al. (1992) Presentation of viral antigen by MHC class I molecules is dependent on a putative peptide transporter heterodimer. Nature 355: 644–646. 1538752
65. de la Salle H, Hanau D, Fricker D, Urlacher A, Kelly A, et al. (1994) Homozygous human TAP peptide transporter mutation in HLA class I deficiency. Science 265: 237–241. 7517574
66. de la Salle H, Zimmer J, Fricker D, Angenieux C, Cazenave JP, et al. (1999) HLA class I deficiencies due to mutations in subunit 1 of the peptide transporter TAP1. J Clin Invest 103: R9–R13. 10074495
67. Moins-Teisserenc HT, Gadola SD, Cella M, Dunbar PR, Exley A, et al. (1999) Association of a syndrome resembling Wegener's granulomatosis with low surface expression of HLA class-I molecules. Lancet 354: 1598–1603. 10560675
68. de la Salle H, Saulquin X, Mansour I, Klayme S, Fricker D, et al. (2002) Asymptomatic deficiency in the peptide transporter associated to antigen processing (TAP). Clin Exp Immunol 128: 525–531. 12067308
69. Ahn K, Meyer TH, Uebel S, Sempe P, Djaballah H, et al. (1996) Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47. EMBO J 15: 3247–3255. 8670825
70. Fruh K, Ahn K, Djaballah H, Sempe P, van Endert PM, et al. (1995) A viral inhibitor of peptide transporters for antigen presentation. Nature 375: 415–418. 7760936
71. Hill A, Jugovic P, York I, Russ G, Bennink J, et al. (1995) Herpes simplex virus turns off the TAP to evade host immunity. Nature 375: 411–415. 7760935
72. 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. 8670826
73. Beinert D, Neumann L, Uebel S, Tampe R (1997) Structure of the viral TAP-inhibitor ICP47 induced by membrane association. Biochemistry 36: 4694–4700. 9109681
74. Galocha B, Hill A, Barnett BC, Dolan A, Raimondi A, et al. (1997) The active site of ICP47, a herpes simplex virus-encoded inhibitor of the major histocompatibility complex (MHC)-encoded peptide transporter associated with antigen processing (TAP), maps to the NH2-terminal 35 residues. J Exp Med 185: 1565–1572. 9151894
75. Neumann L, Kraas W, Uebel S, Jung G, Tampe R (1997) The active domain of the herpes simplex virus protein ICP47: a potent inhibitor of the transporter associated with antigen processing. J Mol Biol 272: 484–492. 9325106
76. 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. 9651323
77. Seyffer F, Tampe R (2015) ABC transporters in adaptive immunity. Biochim Biophys Acta 1850: 449–460. doi: 10.1016/j.bbagen.2014.05.022 24923865
78. Bigger JE, Martin DW (2004) Identification of an ICP47 homologue in simian agent 8 (SA8). Virus Genes 28: 223–225. 15077611
79. Tomazin R, van Schoot NE, Goldsmith K, Jugovic P, Sempe P, et al. (1998) Herpes simplex virus type 2 ICP47 inhibits human TAP but not mouse TAP. J Virol 72: 2560–2563. 9499125
80. Vasireddi M, Hilliard J (2012) Herpes B virus, macacine herpesvirus 1, breaks simplex virus tradition via major histocompatibility complex class I expression in cells from human and macaque hosts. J Virol 86: 12503–12511. doi: 10.1128/JVI.01350-12 22973043
81. McGeoch DJ, Davison AJ (1999) The molecular evolutionary history of the herpesviruses.; Domingo E, Webster R, Holland J, editors. London: Academic Press. 441–465 p.
82. Koppers-Lalic D, Reits EA, Ressing ME, Lipinska AD, Abele R, et al. (2005) Varicelloviruses avoid T cell recognition by UL49.5-mediated inactivation of the transporter associated with antigen processing. Proc Natl Acad Sci U S A 102: 5144–5149. 15793001
83. Verweij MC, Lipinska AD, Koppers-Lalic D, Quinten E, Funke J, et al. (2011) Structural and functional analysis of the TAP-inhibiting UL49.5 proteins of varicelloviruses. Mol Immunol 48: 2038–2051. doi: 10.1016/j.molimm.2011.06.438 21764135
84. Koppers-Lalic D, Verweij MC, Lipinska AD, Wang Y, Quinten E, et al. (2008) Varicellovirus UL 49.5 proteins differentially affect the function of the transporter associated with antigen processing, TAP. PLoS Pathog 4: e1000080. doi: 10.1371/journal.ppat.1000080 18516302
85. Verweij MC, Lipinska AD, Koppers-Lalic D, van Leeuwen WF, Cohen JI, et al. (2011) The capacity of UL49.5 proteins to inhibit TAP is widely distributed among members of the genus Varicellovirus. J Virol 85: 2351–2363. doi: 10.1128/JVI.01621-10 21159875
86. Jons A, Dijkstra JM, Mettenleiter TC (1998) Glycoproteins M and N of pseudorabies virus form a disulfide-linked complex. J Virol 72: 550–557. 9420258
87. Rudolph J, Seyboldt C, Granzow H, Osterrieder N (2002) The gene 10 (UL49.5) product of equine herpesvirus 1 is necessary and sufficient for functional processing of glycoprotein M. J Virol 76: 2952–2963. 11861861
88. Wu SX, Zhu XP, Letchworth GJ (1998) Bovine herpesvirus 1 glycoprotein M forms a disulfide-linked heterodimer with the U(L)49.5 protein. J Virol 72: 3029–3036. 9525625
89. Lipinska AD, Koppers-Lalic D, Rychlowski M, Admiraal P, Rijsewijk FA, et al. (2006) Bovine herpesvirus 1 UL49.5 protein inhibits the transporter associated with antigen processing despite complex formation with glycoprotein M. J Virol 80: 5822–5832. 16731921
90. Ahn K, Gruhler A, Galocha B, Jones TR, Wiertz EJ, et al. (1997) The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity 6: 613–621. 9175839
91. Hengel H, Koopmann JO, Flohr T, Muranyi W, Goulmy E, et al. (1997) A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity 6: 623–632. 9175840
92. Lehner PJ, Karttunen JT, Wilkinson GW, Cresswell P (1997) The human cytomegalovirus US6 glycoprotein inhibits transporter associated with antigen processing-dependent peptide translocation. Proc Natl Acad Sci U S A 94: 6904–6909. 9192664
93. Hewitt EW, Gupta SS, Lehner PJ (2001) The human cytomegalovirus gene product US6 inhibits ATP binding by TAP. EMBO J 20: 387–396. 11157746
94. van Endert PM, Saveanu L, Hewitt EW, Lehner P (2002) Powering the peptide pump: TAP crosstalk with energetic nucleotides. Trends Biochem Sci 27: 454–461. 12217520
95. Halenius A, Momburg F, Reinhard H, Bauer D, Lobigs M, et al. (2006) Physical and functional interactions of the cytomegalovirus US6 glycoprotein with the transporter associated with antigen processing. J Biol Chem 281: 5383–5390. 16356928
96. Rawlinson WD, Farrell HE, Barrell BG (1996) Analysis of the complete DNA sequence of murine cytomegalovirus. J Virol 70: 8833–8849. 8971012
97. Davison AJ, Holton M, Dolan A, Dargan DJ, Gatherer D, et al. (2013) Comparative Genomics of Primate Cytomegaloviruses; Reddehase MJ, editor. Norwich, UK: Caister Academic Press.
98. Hislop AD, Ressing ME, van Leeuwen D, Pudney VA, Horst D, et al. (2007) A CD8+ T cell immune evasion protein specific to Epstein-Barr virus and its close relatives in Old World primates. J Exp Med 204: 1863–1873. 17620360
99. 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. doi: 10.4049/jimmunol.0803218 19201886
100. 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. doi: 10.4049/jimmunol.1002656 21296983
101. York IA, Roop C, Andrews DW, Riddell SR, Graham FL, et al. (1994) A cytosolic herpes simplex virus protein inhibits antigen presentation to CD8+ T lymphocytes. Cell 77: 525–535. 8187174
102. Yuan J, Cahir-McFarland E, Zhao B, Kieff E (2006) Virus and cell RNAs expressed during Epstein-Barr virus replication. J Virol 80: 2548–2565. 16474161
103. 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. doi: 10.1371/journal.ppat.1000490 19557156
104. Quinn LL, Zuo J, Abbott RJ, Shannon-Lowe C, Tierney RJ, et al. (2014) Cooperation between Epstein-Barr virus immune evasion proteins spreads protection from CD8+ T cell recognition across all three phases of the lytic cycle. PLoS Pathog 10: e1004322. doi: 10.1371/journal.ppat.1004322 25144360
105. Goldsmith K, Chen W, Johnson DC, Hendricks RL (1998) Infected cell protein (ICP)47 enhances herpes simplex virus neurovirulence by blocking the CD8+ T cell response. J Exp Med 187: 341–348. 9449714
106. Burgos JS, Serrano-Saiz E, Sastre I, Valdivieso F (2006) ICP47 mediates viral neuroinvasiveness by induction of TAP protein following intravenous inoculation of herpes simplex virus type 1 in mice. J Neurovirol 12: 420–427. 17162658
107. Jugovic P, Hill AM, Tomazin R, Ploegh H, Johnson DC (1998) Inhibition of major histocompatibility complex class I antigen presentation in pig and primate cells by herpes simplex virus type 1 and 2 ICP47. J Virol 72: 5076–5084. 9573278
108. Verweij MC, Ressing ME, Knetsch W, Quinten E, Halenius A, et al. (2011) Inhibition of mouse TAP by immune evasion molecules encoded by non-murine herpesviruses. Mol Immunol 48: 835–845. doi: 10.1016/j.molimm.2010.12.008 21292324
109. Pande NT, Powers C, Ahn K, Fruh K (2005) Rhesus cytomegalovirus contains functional homologues of US2, US3, US6, and US11. J Virol 79: 5786–5798. 15827193
110. Hansen SG, Powers CJ, Richards R, Ventura AB, Ford JC, et al. (2010) Evasion of CD8+ T cells is critical for superinfection by cytomegalovirus. Science 328: 102–106. doi: 10.1126/science.1185350 20360110
111. 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. doi: 10.1016/j.chom.2009.09.013 19917498
112. 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. doi: 10.1016/j.chom.2009.09.012 19917497
113. 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: 1578–89. doi: 10.4049/jimmunol.1400964 25024387
114. Lin J, Eggensperger S, Hank S, Wycisk AI, Wieneke R, et al. (2014) A negative feedback modulator of antigen processing evolved from a frameshift in the cowpox virus genome. PLoS Pathog 10: e1004554. doi: 10.1371/journal.ppat.1004554 25503639
115. Elena SF, Sanjuan R (2005) Adaptive value of high mutation rates of RNA viruses: separating causes from consequences. J Virol 79: 11555–11558. 16140732
116. Finlay BB, McFadden G (2006) Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell 124: 767–782. 16497587
117. Abendroth A, Lin I, Slobedman B, Ploegh H, Arvin AM (2001) Varicella-zoster virus retains major histocompatibility complex class I proteins in the Golgi compartment of infected cells. J Virol 75: 4878–4888. 11312359
118. Eisfeld AJ, Yee MB, Erazo A, Abendroth A, Kinchington PR (2007) Downregulation of class I major histocompatibility complex surface expression by varicella-zoster virus involves open reading frame 66 protein kinase-dependent and-independent mechanisms. J Virol 81: 9034–9049. 17567702
119. Glosson NL, Gonyo P, May NA, Schneider CL, Ristow LC, et al. (2010) Insight into the mechanism of human herpesvirus 7 U21-mediated diversion of class I MHC molecules to lysosomes. J Biol Chem 285: 37016–37029. doi: 10.1074/jbc.M110.125849 20833720
120. Glosson NL, Hudson AW (2007) Human herpesvirus-6A and -6B encode viral immunoevasins that downregulate class I MHC molecules. Virology 365: 125–135. 17467766
121. Powers CJ, Fruh K (2008) Signal peptide-dependent inhibition of MHC class I heavy chain translation by rhesus cytomegalovirus. PLoS Pathog 4: e1000150. doi: 10.1371/journal.ppat.1000150 18833297
122. Zuo J, Quinn LL, Tamblyn J, Thomas WA, Feederle R, et al. (2011) The Epstein-Barr virus-encoded BILF1 protein modulates immune recognition of endogenously processed antigen by targeting major histocompatibility complex class I molecules trafficking on both the exocytic and endocytic pathways. J Virol 85: 1604–1614. doi: 10.1128/JVI.01608-10 21123379
123. Boname JM, Stevenson PG (2001) MHC class I ubiquitination by a viral PHD/LAP finger protein. Immunity 15: 627–636. 11672544
124. 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. 18005752
125. Cox JH, Yewdell JW, Eisenlohr LC, Johnson PR, Bennink JR (1990) Antigen presentation requires transport of MHC class I molecules from the endoplasmic reticulum. Science 247: 715–718. 2137259
126. 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. doi: 10.1371/journal.pbio.1001432 23209377
127. Long EO, Kim HS, Liu D, Peterson ME, Rajagopalan S (2013) Controlling natural killer cell responses: integration of signals for activation and inhibition. Annu Rev Immunol 31: 227–258. doi: 10.1146/annurev-immunol-020711-075005 23516982
128. Wilkinson GW, Tomasec P, Stanton RJ, Armstrong M, Prod'homme V, et al. (2008) Modulation of natural killer cells by human cytomegalovirus. J Clin Virol 41: 206–212. 18069056
129. Campbell JA, Trossman DS, Yokoyama WM, Carayannopoulos LN (2007) Zoonotic orthopoxviruses encode a high-affinity antagonist of NKG2D. J Exp Med 204: 1311–1317. 17548517
130. Grauwet K, Cantoni C, Parodi M, De Maria A, Devriendt B, et al. (2014) Modulation of CD112 by the alphaherpesvirus gD protein suppresses DNAM-1-dependent NK cell-mediated lysis of infected cells. Proc Natl Acad Sci U S A 111: 16118–16123. doi: 10.1073/pnas.1409485111 25352670
131. Nachmani D, Stern-Ginossar N, Sarid R, Mandelboim O (2009) Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell Host Microbe 5: 376–385. doi: 10.1016/j.chom.2009.03.003 19380116
132. Verweij MC, Koppers-Lalic D, Loch S, Klauschies F, de la Salle H, et al. (2008) The varicellovirus UL49.5 protein blocks the transporter associated with antigen processing (TAP) by inhibiting essential conformational transitions in the 6+6 transmembrane TAP core complex. J Immunol 181: 4894–4907. 18802093
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2015 Číslo 4
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Role of Hypoxia Inducible Factor-1α (HIF-1α) in Innate Defense against Uropathogenic Infection
- Toxin-Induced Necroptosis Is a Major Mechanism of Lung Damage
- Transgenic Fatal Familial Insomnia Mice Indicate Prion Infectivity-Independent Mechanisms of Pathogenesis and Phenotypic Expression of Disease
- A Temporal Gate for Viral Enhancers to Co-opt Toll-Like-Receptor Transcriptional Activation Pathways upon Acute Infection