Varicellovirus UL49.5 proteins differentially affect the function of the transporter associated with antigen processing, TAP

PLoS Pathogens

Volumn 4, Issue 5, 2008, Pages

  Koppers Lalic, Danijela ^a   Verweij, Marieke C ^a   Lipińska, Andrea D ^b   Wang, Ying ^c   Quinten, Edwin ^a   Reits, Eric A ^d   Koch, Joachim ^e   Loch, Sandra ^e   Rezende, Marisa Marcondes ^a   Daus, Franz ^f   Bieńkowska Szewczyk, Krystyna ^b   Osterrieder, Nikolaus ^g,h   Mettenleiter, Thomas C ⁱ   Heemskerk, Mirjam H M ^a   Tampé, Robert ^e   Neefjes, Jacques J ^j   Chowdhury, Shafiqul I ^c   Ressing, Maaike E ^a   Rijsewijk, Frans A M ^f   Wiertz, Emmanuel J H J ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF GDA SK   (Poland)

^c KANSAS STATE UNIVERSITY   (United States)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

^e GOETHE UNIVERSITY   (Germany)

^f Virus Discovery Unit   (Netherlands)

^g Department of Obstetrics Gynecology   (United States)

^h Institute for Virology   (Germany)

ⁱ FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^j NETHERLANDS CANCER INSTITUTE   (Netherlands)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEIN TAP; PROTEIN UL49.5; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1; VIRUS PROTEIN; ABC TRANSPORTER; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING (TAP); UL49.5 PROTEIN, BOVINE HERPESVIRUS TYPE 1; VIRUS ENVELOPE PROTEIN;

ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; ARTICLE; BOVINE HERPES VIRUS; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; ENDOPLASMIC RETICULUM; EQUINE HERPES VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; PSEUDORABIES HERPETOVIRUS; VARICELLA ZOSTER VIRUS; VIRUS INFECTION; ANIMAL; CATTLE; CELL SURVIVAL; DOG; GENETIC RECOMBINATION; GENETIC TRANSDUCTION; GENETICS; HORSE; HUMAN; IMMUNOLOGY; INFECTIOUS BOVINE RHINOTRACHEITIS VIRUS; PATHOGENICITY; PHYSIOLOGY; SWINE; TUMOR CELL LINE;

BOVINE HERPESVIRUS 1; EQUID HERPESVIRUS 1; EQUID HERPESVIRUS 4; SUID HERPESVIRUS 1; VARICELLOVIRUS;

ANIMALS; ANTIGEN PRESENTATION; ATP-BINDING CASSETTE TRANSPORTERS; CATTLE; CELL LINE, TUMOR; CELL SURVIVAL; DOGS; HERPESVIRUS 1, BOVINE; HERPESVIRUS 1, EQUID; HERPESVIRUS 1, SUID; HORSES; HUMANS; PROTEIN TRANSPORT; RECOMBINATION, GENETIC; SWINE; TRANSDUCTION, GENETIC; VARICELLOVIRUS; VIRAL ENVELOPE PROTEINS;

EID: 44949148014     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000080     Document Type: Article

References (71)

1. Yewdell JW, Hill AB (2002) Viral interference with antigen presentation. Nat Immunol 3: 1019-1025.
2. Lilley BN, Ploegh HL (2005) Viral modulation of antigen presentation: manipulation of cellular targets in the ER and beyond. Immunol Rev 207: 126-144.
3. Vossen MT, Westerhout EM, Soderberg-Naucler C, Wiertz EJ (2002) Viral immune evasion: a masterpiece of evolution. Immunogenetics 54: 527-542.
4. Abele R, Tampe R (2006) Modulation of the antigen transport machinery TAP by friends and enemies. FEBS Lett 580: 1156-1163.
5. Abele R, Tampe R (2004) The ABCs of immunology: structure and function of TAP, the transporter associated with antigen processing. Physiology (Bethesda ) 19: 216-224.
6. 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.
7. Garbi N, Tanaka S, van den BM, Momburg F, Hammerling GJ (2005) Accessory molecules in the assembly of major histocompatibility complex class I/peptide complexes: how essential are they for CD8(+) T-cell immune responses? Immunol Rev 207: 77-88.
8. Garbi N, Hammerling G, Tanaka S (2007) Interaction of ERp57 and tapasin in the generation of MHC class I-peptide complexes. Curr Opin Immunol 19: 99-105.
9. 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.
10. Koch J, Tampe R (2006) The macromolecular peptide-loading complex in MHC class I-dependent antigen presentation. Cell Mol Life Sci 63: 653-662.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. 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.
18. 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.
19. 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.
20. 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.
21. 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.
22. Hewitt EW, Gupta SS, Lehner PJ (2001) The human cytomegalovirus gene product US6 inhibits ATP binding by TAP. EMBO J 20: 387-396.
23. 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.
24. 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.
25. Stevenson PG, Efstathiou S, Doherty PC, Lehner PJ (2000) Inhibition of MHC class I-restricted antigen presentation by gamma 2-herpesviruses. Proc Natl Acad Sci U S A 97: 8455-8460.
26. Boname JM, Stevenson PG (2001) MHC class I ubiquitination by a viral PHD/LAP finger protein. Immunity 15: 627-636.
27. Lybarger L, Wang X, Harris MR, Virgin HW, Hansen TH (2003) Virus subversion of the MHC class I peptide-loading complex. Immunity 18: 121-130.
28. 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.
29. Yu YY, Harris MR, Lybarger L, Kimpler LA, Myers NB, et al. (2002) Physical association of the K3 protein of gamma-2 herpesvirus 68 with major histocompatibility complex class I molecules with impaired peptide and beta(2)-microglobulin assembly. J Virol 76: 2796-2803.
30. Boname JM, de Lima BD, Lehner PJ, Stevenson PG (2004) Viral degradation of the MHC class I peptide loading complex. Immunity 20: 305-317.
31. Wang X, Lybarger L, Connors R, Harris MR, Hansen TH (2004) Model for the interaction of gammaherpesvirus 68 RING-CH finger protein mK3 with major histocompatibility complex class I and the peptide-loading complex. J Virol 78: 8673-8686.
32. Boname JM, May JS, Stevenson PG (2005) The murine gamma-herpesvirus-68 MK3 protein causes TAP degradation independent of MHC class I heavy chain degradation. Eur J Immunol 35: 171-179.
33. Wang X, Connors R, Harris MR, Hansen TH, Lybarger L (2005) Requirements for the selective degradation of endoplasmic reticulum-resident major histocompatibility complex class I proteins by the viral immune evasion molecule mK3. J Virol 79: 4099-4108.
34. Wang X, Ye Y, Lencer W, Hansen TH (2006) The viral E3 ubiquitin ligase mK3 uses the Derlin/p97 endoplasmic reticulum-associated degradation pathway to mediate down-regulation of major histocompatibility complex class I proteins. J Biol Chem 281: 8636-8644.
35. 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.
36. + T cell immune evasion protein specific to Epstein-Barr virus and its close relatives in Old World primates. J Exp Med In press.
37. Barnett BC, Dolan A, Telford EA, Davison AJ, McGeoch DJ (1992) A novel herpes simplex virus gene (UL49A) encodes a putative membrane protein with counterparts in other herpesviruses. J Gen Virol 73 ( Pt 8): 2167-2171.
38. Davison AJ (2002) Evolution of the herpesviruses. Vet Microbiol 86: 69-88.
39. McGeoch DJ, Rixon FJ, Davison AJ (2006) Topics in herpesvirus genomics and evolution. Virus Res 117: 90-104.
40. Mach M, Osinski K, Kropff B, Schloetzer-Schrehardt U, Krzyzaniak M, et al. (2007) The carboxy-terminal domain of glycoprotein N of human cytomegalovirus is required for virion morphogenesis. J Virol 81: 5212-5224.
41. Jons A, Dijkstra JM, Mettenleiter TC (1998) Glycoproteins M and N of pseudorabies virus form a disulfide-linked complex. J Virol 72: 550-557.
42. 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.
43. 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.
44. 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.
45. 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.
46. Cohen JI (1998) Infection of cells with varicella-zoster virus down-regulates surface expression of class I major histocompatibility complex antigens. J Infect Dis 177: 1390-1393.
47. 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.
48. Park B, Kim Y, Shin J, Lee S, Cho K, Fruh K, Lee S, Ahn K (2004) Human cytomegalovirus inhibits tapasin-dependent peptide loading and optimization of the MHC class I peptide cargo for immune evasion. Immunity 20: 71-85.
49. Park B, Lee S, Kim E, Cho K, Riddell SR, Cho S, Ahn K (2006) Redox regulation facilitates optimal peptide selection by MHC class I during antigen processing. Cell 127: 369-382.
50. Ambagala AP, Hinkley S, Srikumaran S (2000) An early pseudorabies virus protein down-regulates porcine MHC class I expression by inhibition of transporter associated with antigen processing (TAP). J Immunol 164: 93-99.
51. Ambagala AP, Gopinath RS, Srikumaran S (2004) Peptide transport activity of the transporter associated with antigen processing (TAP) is inhibited by an early protein of equine herpesvirus-1. J Gen Virol 85: 349-353.
52. Koppers-Lalic D, Rijsewijk FA, Verschuren SB, van Gaans-Van den Brink JA, Neisig A, Ressing ME, Neefjes J, Wiertz EJ (2001) The UL41-encoded virion host shutoff (vhs) protein and vhs-independent mechanisms are responsible for down-regulation of MHC class I molecules by bovine herpesvirus 1. J Gen Virol 82: 2071-2081.
53. Uebel S, Meyer TH, Kraas W, Kienle S, Jung G, Wiesmuller KH, Tampe R (1995) Requirements for peptide binding to the human transporter associated with antigen processing revealed by peptide scans and complex peptide libraries. J Biol Chem 270: 18512-18516.
54. Meyer TH, van Endert PM, Uebel S, Ehring B, Tampe R (1994) Functional expression and purification of the ABC transporter complex associated with antigen processing (TAP) in insect cells. FEBS Lett 351: 443-447.
55. Neefjes JJ, Momburg F, Hammerling GJ (1993) Selective and ATP-dependent translocation of peptides by the MHC-encoded transporter. Science 261: 769-771.
56. Gorbulev S, Abele R, Tampe 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.
57. 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.
58. Klupp BG, Nixdorf R, Mettenleiter TC (2000) Pseudorabies virus glycoprotein M inhibits membrane fusion. J Virol 74: 6760-6768.
59. Osterrieder N, Neubauer A, Brandmuller C, Braun B, Kaaden OR, Baines JD (1996) The equine herpesvirus 1 glycoprotein gp21/22a, the herpes simplex virus type 1 gM homolog, is involved in virus penetration and cell-to-cell spread of virions. J Virol 70: 4110-4115.
60. van Hall T, Laban S, Koppers-Lalic D, Koch J, Precup C, Asmawidjaja P, Offringa R, Wiertz EJ (2007) The varicellovirus-encoded TAP inhibitor UL49.5 regulates the presentation of CTL epitopes by Qa-1b1. J Immunol 178: 657-662.
61. Garcia-Borges CN, Phanavanh B, Crew MD (2006) Characterization of porcine TAP genes: alternative splicing of TAP1. Immunogenetics 58: 374-382.
62. Loch S, Klauschies F, Scholz C, Verweij MC, Wiertz EJ, Koch J, Tampe R (2008) Signaling of a varicelloviral factor across the ER membrane induces destruction of the peptide-loading complex and immune evasion. J Biol Chem.
63. Dugan GE, Hewitt EW (2008) Structural and Functional Dissection of the Human Cytomegalovirus Immune Evasion Protein US6. J Virol 82: 3271-3282.
64. Koppers-Lalic D, Rychlowski M, van Leeuwen D, Rijsewijk FA, Ressing ME, Neefjes JJ, Bienkowska-Szewczyk K, Wiertz EJ (2003) Bovine herpesvirus 1 interferes with TAP-dependent peptide transport and intracellular trafficking of MHC class I molecules in human cells. Arch Virol 148: 2023-2037.
65. Chowdhury SI, Ross CS, Lee BJ, Hall V, Chu HJ (1999) Construction and characterization of a glycoprotein E gene-deleted bovine herpesvirus type 1 recombinant. Am J Vet Res 60: 227-232.
66. Chowdhury SI, Lee BJ, Ozkul A, Weiss ML (2000) Bovine herpesvirus 5 glycoprotein E is important for neuroinvasiveness and neurovirulence in the olfactory pathway of the rabbit. J Virol 74: 2094-2106.
67. Jons A, Granzow H, Kuchling R, Mettenleiter TC (1996) The UL49.5 gene of pseudorabies virus codes for an O-glycosylated structural protein of the viral envelope. J Virol 70: 1237-1241.
68. Blevitt JM, Fruh K, Glass C, Jackson MR, Peterson PA, Huang S (1999) A Fluorescence-Based High Throughput Screen for the Transporter Associated with Antigen Processing. J Biomol Screen 4: 87-91.
69. Al Mubarak A, Zhou Y, Chowdhury SI (2004) A glycine-rich bovine herpesvirus 5 (BHV-5) gE-specific epitope within the ectodomain is important for BHV-5 neurovirulence. J Virol 78: 4806-4816.
70. Schrodt S, Koch J, Tampe R (2006) Membrane topology of the transporter associated with antigen processing (TAP1) within an assembled functional peptide-loading complex. J Biol Chem 281: 6455-6462.
71. 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.