Crystal structure of adenovirus E3-19K bound to HLA-A2 reveals mechanism for immunomodulation

Nature Structural and Molecular Biology

Volumn 19, Issue 11, 2012, Pages 1176-1181

  Li, Lenong ^a   Muzahim, Yasameen ^a   Bouvier, Marlene ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS E3 19K PROTEIN; HLA A ANTIGEN; HLA A2 ANTIGEN; HLA B ANTIGEN; HLA C ANTIGEN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CELLULAR IMMUNITY; CRYSTAL STRUCTURE; ESCHERICHIA COLI; IMMUNOMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN REFOLDING; PROTEIN STRUCTURE;

ADENOVIRUS E3 PROTEINS; CLONING, MOLECULAR; CRYSTALLOGRAPHY; ENDOPLASMIC RETICULUM; ESCHERICHIA COLI; HLA-A2 ANTIGEN; HUMANS; IMMUNOMODULATION; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; T-LYMPHOCYTES;

ADENOVIRIDAE;

EID: 84869092089     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2396     Document Type: Article

References (52)

1. Berk, A.J. Adenoviruses. in Fields Virology 5th edn. (eds. Knipe, D.M., Howley, P.M., Griffin, D.E. & Lamb, R.A.) 2395-2436 (Lippincott Williams & Wilkins, 2007).
2. Wold, W.S.M. & Horwitz, M.S. Adenoviridae: the viruses and their replication. in Fields Virology, 5th edn. (eds. Knipe, D.M., Howley, P.M., Griffin, D.E. & Lamb, R.A.) 2355-2394 (Lippincott Williams & Wilkins, 2007).
3. Hansen, T.H. & Bouvier, M. MHC class I antigen presentation: learning from viral evasion strategies. Nat. Rev. Immunol. 9, 503-513 (2009).
4. Burgert, H.-G. et al. Subversion of host defense mechanisms by adenoviruses. in Viral Proteins Counteracting Host Defenses (eds. Koszinowski, U.H. & Hengel, H.) 273-318 (Springer, 2002). (Pubitemid 34851538)
5. Andersson, M., Paabo, S., Nilsson, T. & Peterson, P.A. Impaired intracellular transport of class I MHC antigens as a possible means for adenoviruses to evade immune surveillance. Cell 43, 215-222 (1985). (Pubitemid 16199707)
6. Andersson, M., McMichael, A. & Peterson, P.A. Reduced allorecognition of adenovirus-2 infected cells. J. Immunol. 138, 3960-3966 (1987). (Pubitemid 17078280)
7. Burgert, H.G. & Kvist, S. An adenovirus type 2 glycoprotein blocks cell surface expression of human histocompatibility class I antigens. Cell 41, 987-997 (1985). (Pubitemid 15243402)
8. Burgert, H.-G. & Kvist, S. The E3/19K protein of adenovirus type 2 binds to the domains of histocompatibility antigens required for CTL recognition. EMBO J. 6, 2019-2026 (1987).
9. Flomenberg, P., Piaskowski, V., Truitt, R.L. & Casper, J.T. Human adenovirus-specific CD8+ T-cell responses are not inhibited by E3-19K in the presence of gamma interferon. J. Virol. 70, 6314-6322 (1996). (Pubitemid 26266851)
10. Rawle, F.C., Tollefson, A.E., Wold, W.S.M. & Gooding, L.R. Mouse anti-adenovirus cytoxic T lymphocytes. J. Immunol. 143, 2031-2037 (1989).
11. Ginsberg, H.S. et al. Role of early region 3 (E3) in pathogenesis of Adenovirus disease. Proc. Natl. Acad. Sci. USA 86, 3823-3827 (1989). (Pubitemid 19141837)
12. Wold, W.S.M. & Gooding, L.R. Adenovirus regions E3 proteins that prevent cytolysis by cytotoxic T cells and tumor necrosis factor. Mol. Biol. Med. 6, 433-452 (1989). (Pubitemid 20146560)
13. Feuerbach, D. et al. Identification of amino acids within the MHC molecule important for the interaction with the adenovirus protein E3/19K. J. Immunol. 153, 1626-1636 (1994). (Pubitemid 24251107)
14. Flomenberg, P., Gutierrez, E. & Hogan, K.T. Identification of class I MHC regions which bind to the adenovirus E3-19K protein. Mol. Immunol. 31, 1277-1284 (1994). (Pubitemid 24348764)
15. Gabathuler, R., Levy, F. & Kvist, S. Requirement for the association of adenovirus type 2 E3-19K wild-type and mutant proteins with HLA antigens. J. Virol. 64, 3679-3685 (1990). (Pubitemid 20227190)
16. Hermiston, T.W., Tripp, R.A., Sparer, R.A., Gooding, L.R. & Wold, W.S.M. Deletion mutation analysis of the adenovirus type 2 E3-gp19K protein: identification of sequences within the endoplasmic reticulum lumenal domain that are required for class I antigen binding and protection from adenovirus-specific cytotoxic T lymphocytes. J. Virol. 67, 5289-5298 (1993). (Pubitemid 23241360)
17. Cox, J.H., Bennink, J.R. & Yewdell, J.W. Retention of adenovirus E19 glycoprotein in the endoplasmic reticulum is essential to its ability to block antigen presentation. J. Exp. Med. 174, 1629-1637 (1991).
18. Pääbo, S., Bhat, B.M., Wold, W.S.M. & Peterson, P.A. A short sequence in the COOH-terminus makes an adenovirus membrane glycoprotein a resident of the endoplasmic reticulum. Cell 50, 311-317 (1987).
19. Severinsson, L., Martens, I. & Peterson, P.A. Differential association between two human MHC class I antigens and an adenoviral glycoprotein. J. Immunol. 137, 1003-1009 (1986). (Pubitemid 16072046)
20. Deryckere, F. & Burgert, H.-G. Early region 3 of adenovirus type 19 (subgroup D) encodes an HLA-binding protein distinct from that of subgroups B and C. J. Virol. 70, 2832-2841 (1996). (Pubitemid 26121895)
21. Körner, H. & Burgert, H.-G. Down-regulation of HLA antigens by the adenovirus type 2 E3/19K protein in a T-lymphoma cell line. J. Virol. 68, 1442-1448 (1994). (Pubitemid 24065707)
22. Liu, H., Fu, J. & Bouvier, M. Allele-and locus-specific recognition of class I MHC molecules by the immunomodulatory E3-19K protein from adenovirus. J. Immunol. 178, 4567-4575 (2007). (Pubitemid 46492409)
23. Fu, J., Li, L. & Bouvier, M. Adenovirus E3-19K proteins of different serotypes and subgroups have similar, yet distinct, immunomodulatory functions towards major histocompatibility class I molecules. J. Biol. Chem. 286, 17631-17639 (2011).
24. Hermiston, T.W., Tripp, R.A., Sparer, R.A., Gooding, L.R. & Wold, W.S.M. Deletion mutation analysis of the adenovirus type 2 E3-gp19K protein: identification of sequences within the endoplasmic reticulum lumenal domain that are required for class I antigen binding and protection from adenovirus-specific cytotoxic T lymphocytes. J. Virol. 67, 5289-5298 (1993). (Pubitemid 23241360)
25. Flomenberg, P., Szmulewicz, J., Gutierrez, E. & Lupatkin, H. Role of the adenovirus E3-19K conserved region in binding major histocompatibility complex class I molecules. J. Virol. 66, 4778-4783 (1992).
26. Chatterjee, D. & Maizel, J.V. Homology of adenoviral E3 glycoprotein with HLA-DR heavy chain. Proc. Natl. Acad. Sci. USA 81, 6039-6043 (1984). (Pubitemid 15219591)
27. Sester, M. et al. Conserved amino acids within the adenovirus 2 E3/19K protein differentially affect downregulation of MHC class I and MICA/B proteins. J. Immunol. 184, 255-267 (2010).
28. Menz, B., Sester, M., Koebernick, K., Schmid, R. & Burgert, H.-G. Structural analysis of the adenovirus type 2 E3-/19K protein using mutagenesis and a panel of conformation-sensitive monoclonal antibodies. Mol. Immunol. 46, 16-26 (2008).
29. Fu, J. & Bouvier, M. Determinants of the endoplasmic reticulum (ER) lumenal-domain of the Adenovirus serotype 2 E3-19K protein for association with and ER-retention of major histocompatibility complex class I molecules. Mol. Immunol. 48, 532-538 (2011).
30. Wold, W.S.M., Cladaras, C., Deutscher, S.L. & Kapoor, Q.S. The 19-kDa glycoprotein coded by region E3 of adenovirus. Purification, characterization, and structural analysis. J. Biol. Chem. 260, 2424-2431 (1985). (Pubitemid 15104849)
31. Liu, H., Stafford, W.F. & Bouvier, M. The endoplasmic reticulum lumenal domain of the adenovirus type 2 E3-19K binds to peptide-filled and peptide-deficient HLA-A*1101 molecules. J. Virol. 79, 13317-13325 (2005). (Pubitemid 41508146)
32. Sester, M. & Burgert, H.-G. Conserved cysteine residues within the E3/19K protein of adenovirus type 2 are essential for binding to major histocompatibility complex antigens. J. Virol. 68, 5423-5432 (1994). (Pubitemid 24258554)
33. Holm, L. & Sander, C. Touring protein fold space with Dali/FSSP. Nucleic Acids Res. 26, 316-319 (1998). (Pubitemid 28291549)
34. Krissinel, E. & Henrick, K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three-dimension. Acta Crystallogr. D Biol. Crystallogr. 60, 2256-2268 (2004). (Pubitemid 41742778)
35. Lawrence, M.C. & Colman, P.M. Shape complementarity at protein/protein interfaces. J. Mol. Biol. 234, 946-950 (1993). (Pubitemid 24027225)
36. Bouvier, M. Accessory proteins and the assembly of human class I MHC molecules. A molecular and structural perspective. Mol. Immunol. 39, 697-706 (2003). (Pubitemid 36078363)
37. Yu, Y.Y.L. et al. Definition and transfer of a serological epitope specific for peptide-empty forms of MHC class I. Int. Immunol. 11, 1897-1906 (1999).
38. Morris, C.R. et al. The amyloid precursor-like protein 2 and the adenoviral E3/19K protein both bind to a conformational site on H-2Kd and regulate H-2Kd expression. J. Biol. Chem. 278, 12618-12623 (2003). (Pubitemid 36800021)
39. Mage, M.G. et al. The peptide-receptive transition state of MHC class I molecules: insight from structure and molecular dynamics. J. Immunol. 189, 1391-1399 (2012).
40. Gewurz, B.E., Wang, E.W., Tortorella, D., Schust, D.J. & Ploegh, H.L. Human cytomegalovirus US2 endoplasmic reticulum-lumenal domain dictates association with major histocompatibility complex class I in a locus-specific manner. J. Virol. 75, 5197-5204 (2001). (Pubitemid 32448542)
41. Ishido, S., Wang, C., Lee, B.-S., Cohen, G.B. & Jung, J.U. Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins. J. Virol. 74, 5300-5309 (2000). (Pubitemid 30313872)
42. Cohen, G.B. et al. The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 10, 661-671 (1999). (Pubitemid 29302919)
43. McSharry, B.P. et al. Adenovirus E3/19K promotes evasion of NK cell recognition by intracellular sequestration of the NKG2D ligands major histocompatibility complex class I chain-related proteins A and B. J. Virol. 82, 4585-4594 (2008). (Pubitemid 351563695)
44. Gewurz, B.E. et al. Antigen presentation subverted: structure of the human cytomegalovirus protein US2 bound to the class I molecule HLA-A2. Proc. Natl. Acad. Sci. USA 98, 6794-6799 (2001). (Pubitemid 32538296)
45. Guex, N. & Peitsch, M.C. SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling. Electrophoresis 18, 2714-2723 (1997). (Pubitemid 28059943)
46. Garboczi, D.N., Hung, D.T. & Wiley, D.C. HLA-A2-peptide complexes: refolding and crystallization of molecules expressed in Escherichia coli and complexed with single antigenic peptides. Proc. Natl. Acad. Sci. USA 89, 3429-3433 (1992).
47. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997). (Pubitemid 27085611)
48. Navaza, J. AMoRe: an automated package for molecular replacement. Acta Crystallogr. A 50, 157-163 (1994).
49. Cowtan, K.D. & Main, P. Improvement of macromolecular electron-density maps by the simultaneous application of real and reciprocal space constraints. Acta Crystallogr. D Biol. Crystallogr. 49, 148-157 (1993).
50. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004). (Pubitemid 41742764)
51. Brünger, A.T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921 (1998).
52. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291 (1993).