Crystal structure of the cowpox virus-encoded NKG2D ligand OMCP

Journal of Virology

Volumn 87, Issue 2, 2013, Pages 840-850

  Lazear, Eric ^a   Peterson, Lance W ^a,b   Nelson, Chris A ^a   Fremont, Daved H ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NATURAL KILLER CELL RECEPTOR NKG2D; ORTHOPOXVIRUS MAJOR HISTOCOMPATIBILITY COMPLEX CLASS I LIKE PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ALPHA HELIX; ARTICLE; BETA SHEET; BINDING AFFINITY; COWPOX VIRUS; CRYSTAL STRUCTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; RECEPTOR BLOCKING; STRUCTURE ANALYSIS; VIRUS STRAIN;

AMINO ACID SEQUENCE; ANIMALS; COWPOX VIRUS; CRYSTALLOGRAPHY, X-RAY; HUMANS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL PROTEINS;

COWPOX VIRUS; MONKEYPOX VIRUS; MURINAE; ORTHOPOXVIRUS;

EID: 84871947685     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01948-12     Document Type: Article

References (77)

1. Obeidy P, Sharland AF. 2009. NKG2D and its ligands. Int. J. Biochem. Cell Biol. 41:2364-2367.
2. Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, Spies T. 1999. Activation of NK cells and T cells by NKG2D, a receptor for stressinducible MICA. Science 285:727-729.
3. Bottino C, Castriconi R, Moretta L, Moretta A. 2005. Cellular ligands of activating NK receptors. Trends Immunol. 26:221-226.
4. Coudert JD, Held W. 2006. The role of the NKG2D receptor for tumor immunity. Semin. Cancer Biol. 16:333-343.
5. Groh V, Rhinehart R, Randolph-Habecker J, Topp MS, Riddell SR, Spies T. 2001. Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat. Immunol. 2:255-260.
6. Lanier LL. 2008. Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 9:495-502.
7. Lodoen MB, Lanier LL. 2006. Natural killer cells as an initial defense against pathogens. Curr. Opin. Immunol. 18:391-398.
8. Champsaur M, Lanier LL. 2010. Effect of NKG2D ligand expression on host immune responses. Immunol. Rev. 235:267-285.
9. Cosman D, Mullberg J, Sutherland CL, Chin W, Armitage R, Fanslow W, Kubin M, Chalupny NJ. 2001. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 14:123-133.
10. Radosavljevic M, Cuillerier B, Wilson MJ, Clement O, Wicker S, Gilfillan S, Beck S, Trowsdale J, Bahram S. 2002. A cluster of ten novel MHC class I related genes on human chromosome 6q24.2-q25.3. Genomics 79: 114-123.
11. Schrambach S, Ardizzone M, Leymarie V, Sibilia J, Bahram S. 2007. In vivo expression pattern of MICA and MICB and its relevance to auto-immunity and cancer. PLoS One 2:e518. doi:10.1371/journal.pone.0000518.
12. Mistry AR, O'Callaghan CA. 2007. Regulation of ligands for the activating receptor NKG2D. Immunology 121:439-447.
13. Raulet DH. 2003. Roles of the NKG2D immunoreceptor and its ligands. Nat. Rev. Immunol. 3:781-790.
14. McGilvray RW, Eagle RA, Watson NF, Al-Attar A, Ball G, Jafferji I, Trowsdale J, Durrant LG. 2009. NKG2D ligand expression in human colorectal cancer reveals associations with prognosis and evidence for immunoediting. Clin. Cancer Res. 15:6993-7002.
15. O'Sullivan T, Dunn GP, Lacoursiere DY, Schreiber RD, Bui JD. 2011. Cancer immunoediting of the NK group 2D ligand H60a. J. Immunol. 187:3538-3545.
16. Fernandez-Messina L, Ashiru O, Boutet P, Aguera-Gonzalez S, Skepper JN, Reyburn HT, Vales-Gomez M. 2010. Differential mechanisms of shedding of the glycosylphosphatidylinositol (GPI)-anchored NKG2D ligands. J. Biol. Chem. 285:8543-8551.
17. Groh V, Wu J, Yee C, Spies T. 2002. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419: 734-738.
18. Salih HR, Goehlsdorf D, Steinle A. 2006. Release of MICB molecules by tumor cells: mechanism and soluble MICB in sera of cancer patients. Hum. Immunol. 67:188-195.
19. Salih HR, Rammensee HG, Steinle A. 2002. Cutting edge: downregulation of MICA on human tumors by proteolytic shedding. J. Immunol. 169:4098-4102.
20. Waldhauer I, Steinle A. 2006. Proteolytic release of soluble UL16-binding protein 2 from tumor cells. Cancer Res. 66:2520-2526.
21. Draghi M, Pashine A, Sanjanwala B, Gendzekhadze K, Cantoni C, Cosman D, Moretta A, Valiante NM, Parham P. 2007. NKp46 and NKG2D recognition of infected dendritic cells is necessary for NK cell activation in the human response to influenza infection. J. Immunol. 178: 2688-2698.
22. Dupuy S, Lambert M, Zucman D, Choukem SP, Tognarelli S, Pages C, Lebbe C, Caillat-Zucman S. 2012. Human herpesvirus 8 (HHV8) sequentially shapes the NK cell repertoire during the course of asymptomatic infection and Kaposi sarcoma. PLoS Pathog. 8:e1002486. doi:10.1371/journal.ppat.1002486.
23. Pappworth IY, Wang EC, Rowe M. 2007. The switch from latent to productive infection in Epstein-Barr virus-infected B cells is associated with sensitization to NK cell killing. J. Virol. 81:474-482.
24. Tokuyama M, Lorin C, Delebecque F, Jung H, Raulet DH, Coscoy L. 2011. Expression of the RAE-1 family of stimulatory NK-cell ligands requires activation of the PI3K pathway during viral infection and transformation. PLoS Pathog. 7:e1002265. doi:10.1371/journal.ppat.1002265.
25. Ward J, Bonaparte M, Sacks J, Guterman J, Fogli M, Mavilio D, Barker E. 2007. HIV modulates the expression of ligands important in triggering natural killer cell cytotoxic responses on infected primary T-cell blasts. Blood 110:1207-1214.
26. Welte SA, Sinzger C, Lutz SZ, Singh-Jasuja H, Sampaio KL, Eknigk U, Rammensee HG, Steinle A. 2003. Selective intracellular retention of virally induced NKG2D ligands by the human cytomegalovirus UL16 glycoprotein. Eur. J. Immunol. 33:194-203.
27. Krmpotic A, Hasan M, Loewendorf A, Saulig T, Halenius A, Lenac T, Polic B, Bubic I, Kriegeskorte A, Pernjak-Pugel E, Messerle M, Hengel H, Busch DH, Koszinowski UH, Jonjic S. 2005. NK cell activation through the NKG2D ligand MULT-1 is selectively prevented by the glycoprotein encoded by mouse cytomegalovirus gene m145. J. Exp. Med. 201:211-220.
28. Lenac T, Budt M, Arapovic J, Hasan M, Zimmermann A, Simic H, Krmpotic A, Messerle M, Ruzsics Z, Koszinowski UH, Hengel H, Jonjic S. 2006. The herpesviral Fc receptor fcr-1 down-regulates the NKG2D ligands MULT-1 and H60. J. Exp. Med. 203:1843-1850.
29. Lodoen M, Ogasawara K, Hamerman JA, Arase H, Houchins JP, Mocarski ES, Lanier LL. 2003. NKG2D-mediated natural killer cell protection against cytomegalovirus is impaired by viral gp40 modulation of retinoic acid early inducible 1 gene molecules. J. Exp. Med. 197:1245-1253.
30. Lodoen MB, Abenes G, Umamoto S, Houchins JP, Liu F, Lanier LL. 2004. The cytomegalovirus m155 gene product subverts natural killer cell antiviral protection by disruption of H60-NKG2D interactions. J. Exp. Med. 200:1075-1081.
31. Stern-Ginossar N, Elefant N, Zimmermann A, Wolf DG, Saleh N, Biton M, Horwitz E, Prokocimer Z, Prichard M, Hahn G, Goldman-Wohl D, Greenfield C, Yagel S, Hengel H, Altuvia Y, Margalit H, Mandelboim O. 2007. Host immune system gene targeting by a viral miRNA. Science 317: 376-381.
32. Thomas M, Boname JM, Field S, Nejentsev S, Salio M, Cerundolo V, Wills M, Lehner PJ. 2008. Down-regulation of NKG2D and NKp80 ligands by Kaposi's sarcoma-associated herpesvirus K5 protects against NK cell cytotoxicity. Proc. Natl. Acad. Sci. U. S. A. 105:1656-1661.
33. Byun M, Verweij MC, Pickup DJ, Wiertz EJ, Hansen TH, Yokoyama WM. 2009. Two mechanistically distinct immune evasion proteins of cowpox virus combine to avoid antiviral CD8 T cells. Cell Host Microbe 6:422-432.
34. 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.
35. Dunn C, Chalupny NJ, Sutherland CL, Dosch S, Sivakumar PV, Johnson DC, Cosman D. 2003. Human cytomegalovirus glycoprotein UL16 causes intracellular sequestration of NKG2D ligands, protecting against natural killer cell cytotoxicity. J. Exp. Med. 197:1427-1439.
36. Rolle A, Mousavi-Jazi M, Eriksson M, Odeberg J, Soderberg-Naucler C, Cosman D, Karre K, Cerboni C. 2003. Effects of human cytomegalovirus infection on ligands for the activating NKG2D receptor of NK cells: upregulation of UL16-binding protein (ULBP)1 and ULBP2 is counteracted by the viral UL16 protein. J. Immunol. 171:902-908.
37. Vales-Gomez M, Browne H, Reyburn HT. 2003. Expression of the UL16 glycoprotein of human cytomegalovirus protects the virus-infected cell from attack by natural killer cells. BMCImmunol. 4:4. doi:10.1186/1471-2172-4-4.
38. Wu J, Chalupny NJ, Manley TJ, Riddell SR, Cosman D, Spies T. 2003. Intracellular retention of the MHC class I-related chain B ligand of NKG2D by the human cytomegalovirus UL16 glycoprotein. J. Immunol. 170:4196-4200.
39. Chalupny NJ, Rein-Weston A, Dosch S, Cosman D. 2006. Downregulation of the NKG2D ligand MICA by the human cytomegalovirus glycoprotein UL142. Biochem. Biophys. Res. Commun. 346:175-181.
40. Perez-Rodriguez M, Arguello JR, Fischer G, Corell A, Cox ST, Robinson J, Hossain E, McWhinnie A, Travers PJ, Marsh SG, Madrigal JA. 2002. Further polymorphism of the MICA gene. Eur. J. Immunogenet. 29:35-46.
41. Zou Y, Bresnahan W, Taylor RT, Stastny P. 2005. Effect of human cytomegalovirus on expression ofMHCclass I-related chains A. J. Immunol. 174:3098-3104.
42. Karre K, Ljunggren HG, Piontek G, Kiessling R. 1986. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319:675-678.
43. Lanier LL. 2009. DAP10- and DAP12-associated receptors in innate immunity. Immunol. Rev. 227:150-160.
44. McFarland BJ, Kortemme T, Yu SF, Baker D, Strong RK. 2003. Symmetry recognizing asymmetry: analysis of the interactions between the C-type lectin-like immunoreceptor NKG2D and MHC class I-like ligands. Structure 11:411-422.
45. Eagle RA, Trowsdale J. 2007. Promiscuity and the single receptor: NKG2D. Nat. Rev. Immunol. 7:737-744.
46. Fang M, Lanier LL, Sigal LJ. 2008. A role for NKG2D in NK cell-mediated resistance to poxvirus disease. PLoS Pathog. 4:e30. doi:10.1371/journal.ppat.0040030.
47. Jacoby RO, Bhatt PN, Brownstein DG. 1989. Evidence that NK cells and interferon are required for genetic resistance to lethal infection with ectromelia virus. Arch. Virol. 108:49-58.
48. Campbell JA, Trossman DS, Yokoyama WM, Carayannopoulos LN. 2007. Zoonotic orthopoxviruses encode a high-affinity antagonist of NKG2D. J. Exp. Med. 204:1311-1317.
49. Holmes MA, Li P, Petersdorf EW, Strong RK. 2002. Structural studies of allelic diversity of the MHC class I homolog MIC-B, a stress-inducible ligand for the activating immunoreceptor NKG2D. J. Immunol. 169: 1395-1400.
50. Li P, McDermott G, Strong RK. 2002. Crystal structures of RAE-1beta and its complex with the activating immunoreceptor NKG2D. Immunity 16:77-86.
51. Li P, Morris DL, Willcox BE, Steinle A, Spies T, Strong RK. 2001. Complex structure of the activating immunoreceptor NKG2D and its MHC class I-like ligand MICA. Nat. Immunol. 2:443-451.
52. Li P, Willie ST, Bauer S, Morris DL, Spies T, Strong RK. 1999. Crystal structure of the MHC class I homolog MIC-A, a gammadelta T cell ligand. Immunity 10:577-584.
53. Radaev S, Rostro B, Brooks AG, Colonna M, Sun PD. 2001. Conformational plasticity revealed by the cocrystal structure of NKG2D and its class I MHC-like ligand ULBP3. Immunity 15:1039-1049.
54. Strong RK. 2002. Asymmetric ligand recognition by the activating natural killer cell receptor NKG2D, a symmetric homodimer. Mol. Immunol. 38:1029-1037.
55. Nelson CA, Fremont MD, Sedy JR, Norris PS, Ware CF, Murphy KM, Fremont DH. 2008. Structural determinants of herpesvirus entry mediator recognition by murine B and T lymphocyte attenuator. J. Immunol. 180:940-947.
56. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Macromol. Crystallogr. A 276:307-326.
57. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, Terwilliger TC. 2002. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58:1948-1954.
58. Chen VB, Arendall WB, III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66:12-21.
59. Vonrhein C, Blanc E, Roversi P, Bricogne G. 2007. Automated structure solution with autoSHARP. Methods Mol. Biol. 364:215-230.
60. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
61. Schrodinger LLC. 2010. The PyMOL molecular graphics system, version 1.3r1. Schrodinger LLC, Portland, OR.
62. Luca VC, AbiMansour J, Nelson CA, Fremont DH. 2012. Crystal structure of the Japanese encephalitis virus envelope protein. J. Virol. 86:2337-2346.
63. Carayannopoulos LN, Naidenko OV, Kinder J, Ho EL, Fremont DH, Yokoyama WM. 2002. Ligands for murine NKG2D display heterogeneous binding behavior. Eur. J. Immunol. 32:597-605.
64. Campbell JA, Davis RS, Lilly LM, Fremont DH, French AR, Carayannopoulos LN. 2010. Cutting edge: FcR-like 5 on innate B cells is targeted by a poxvirus MHC class I-like immunoevasin. J. Immunol. 185:28-32.
65. O'Callaghan CA, Cerwenka A, Willcox BE, Lanier LL, Bjorkman PJ. 2001. Molecular competition for NKG2D: H60 and RAE1 compete unequally for NKG2D with dominance of H60. Immunity 15:201-211.
66. Schepis D, D'Amato M, Studahl M, Bergstrom T, Karre K, Berg L. 2009. Herpes simplex virus infection downmodulates NKG2D ligand expression. Scand. J. Immunol. 69:429-436.
67. Carayannopoulos LN, Naidenko OV, Fremont DH, Yokoyama WM. 2002. Cutting edge: murine UL16-binding protein-like transcript 1: a newly described transcript encoding a high-affinity ligand for murine NKG2D. J. Immunol. 169:4079-4083.
68. Holm L, Rosenstrom P. 2010. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38:W545-W549.
69. Adams EJ, Chien YH, Garcia KC. 2005. Structure of a gammadelta T cell receptor in complex with the nonclassical MHC T22. Science 308:227-231.
70. Natarajan K, Hicks A, Mans J, Robinson H, Guan R, Mariuzza RA, Margulies DH. 2006. Crystal structure of the murine cytomegalovirus MHC-I homolog m144. J. Mol. Biol. 358:157-171.
71. Wingren C, Crowley MP, Degano M, Chien Y, Wilson IA. 2000. Crystal structure of a gammadelta T cell receptor ligand T22: a truncated MHClike fold. Science 287:310-314.
72. Hansen TH, Bouvier M. 2009.MHCclass I antigen presentation: learning from viral evasion strategies. Nat. Rev. Immunol. 9:503-513.
73. Lefkowitz EJ, Upton C, Changayil SS, Buck C, Traktman P, Buller RM. 2005. Poxvirus Bioinformatics Resource Center: a comprehensive Poxviridae informational and analytical resource. Nucleic Acids Res. 33: D311-D316.
74. Strong RK, McFarland BJ. 2004. NKG2D and related immunoreceptors. Adv. Protein Chem. 68:281-312.
75. Lewis-Jones S. 2004. Zoonotic poxvirus infections in humans. Curr. Opin. Infect. Dis. 17:81-89.
76. Rimoin AW, Mulembakani PM, Johnston SC, Lloyd Smith JO, Kisalu NK, Kinkela TL, Blumberg S, Thomassen HA, Pike BL, Fair JN, Wolfe ND, Shongo RL, Graham BS, Formenty P, Okitolonda E, Hensley LE, Meyer H, Wright LL, Muyembe JJ. 2010. Major increase in human monkeypox incidence 30 years after smallpox vaccination campaigns cease in the Democratic Republic of Congo. Proc. Natl. Acad. Sci. U. S. A. 107:16262-16267.
77. Essbauer S, Pfeffer M, Meyer H. 2010. Zoonotic poxviruses. Vet. Microbiol. 140:229-236.