Crystal structure of the murine cytomegalovirus MHC-I homolog m144

Journal of Molecular Biology

Volumn 358, Issue 1, 2006, Pages 157-171

  Natarajan, Kannan ^a   Hicks, Ashleigh ^a   Mans, Janet ^a,b   Robinson, Howard ^c   Guan, Rongjin ^d   Mariuzza, Roy A ^d   Margulies, David H ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^c BROOKHAVEN NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF MARYLAND   (United States)

Author keywords

Immunoevasin; MHC Iv; NK recognition; Viral virulence; X ray structure

Indexed keywords

AMINO ACID; BETA 2 MICROGLOBULIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEIN M144; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CANONICAL ANALYSIS; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; CYTOMEGALOVIRUS; LIGAND BINDING; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; THERMOSTABILITY;

ANIMALIA; CYTOMEGALOVIRUS; DNA VIRUSES; HERPESVIRIDAE; MURID HERPESVIRUS 1;

EID: 33645108011     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.01.068     Document Type: Article

References (72)

1. S.C. Harrison, B. Alberts, E. Ehrenfeld, L. Enquist, H. Fineberg, and S.L. McKnight Discovery of antivirals against smallpox Proc. Natl Acad. Sci. USA 101 2004 11178 11192
2. D. Tortorella, B.E. Gewurz, M.H. Furman, D.J. Schust, and H.L. Ploegh Viral subversion of the immune system Annu. Rev. Immunol. 18 2000 861 926
3. B. Roizman, R.J. Whitley, and C. Lopez The Human Herpesviruses 1993 Raven Press New York
4. H. Arase, and L.L. Lanier Specific recognition of virus-infected cells by paired NK receptors Rev. Med. Virol. 14 2004 83 93
5. P. Moss, and N. Khan CD8(+) T-cell immunity to cytomegalovirus Hum. Immunol. 65 2004 456 464
6. M. Sester, B.C. Gartner, U. Sester, M. Girndt, N. Mueller-Lantzsch, and H. Kohler Is the cytomegalovirus serologic status always accurate? A comparative analysis of humoral and cellular immunity Transplantation 76 2003 1229 1230
7. H. Farrell, M. Degli-Esposti, E. Densley, E. Cretney, M. Smyth, and N. Davis-Poynter Cytomegalovirus MHC class I homologues and natural killer cells: an overview Microbes Infect. 2 2000 521 532
8. H.R. Smith, J.W. Heusel, I.K. Mehta, S. Kim, B.G. Dorner, and O.V. Naidenko Recognition of a virus-encoded ligand by a natural killer cell activation receptor Proc. Natl Acad. Sci. USA 99 2002 8826 8831
9. S. Basta, and J.R. Bennink A survival game of hide and seek: cytomegaloviruses and MHC class I antigen presentation pathways Viral Immunol. 16 2003 231 242
10. D. Saverino, F. Ghiotto, A. Merlo, S. Bruno, L. Battini, and M. Occhino Specific recognition of the viral protein UL18 by CD85j/LIR-1/ILT2 on CD8+T cells mediates the non-MHC-restricted lysis of human cytomegalovirus-infected cells J. Immunol. 172 2004 5629 5637
11. M. Lopez-Botet, M. Llano, and M. Ortega Human cytomegalovirus and natural killer-mediated surveillance of HLA class I expression: a paradigm of host-pathogen adaptation Immunol. Rev. 181 2001 193 202
12. D. Cosman, N. Fanger, and L. Borges Human cytomegalovirus, MHC class I and inhibitory signalling receptors: more questions than answers Immunol. Rev. 168 1999 177 185
13. D. Cosman, N. Fanger, L. Borges, M. Kubin, W. Chin, L. Peterson, and M.L. Hsu A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules Immunity 7 1997 273 282
14. M. Vitale, R. Castriconi, S. Parolini, D. Pende, M.L. Hsu, and L. Moretta The leukocyte Ig-like receptor (LIR)-1 for the cytomegalovirus UL18 protein displays a broad specificity for different HLA class I alleles: analysis of LIR-1+ NK cell clones Int. Immunol. 11 1999 29 35
15. M.R. Wills, O. Ashiru, M.B. Reeves, G. Okecha, J. Trowsdale, and P. Tomasec Human cytomegalovirus encodes an MHC class I-like molecule (UL142) that functions to inhibit NK cell lysis J. Immunol. 175 2005 7457 7465
16. H. Arase, E.S. Mocarski, A.E. Campbell, A.B. Hill, and L.L. Lanier Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors Science 296 2002 1323 1326
17. V. Voigt, C.A. Forbes, J.N. Tonkin, M.A. Degli-Esposti, H.R. Smith, W.M. Yokoyama, and A.A. Scalzo Murine cytomegalovirus m157 mutation and variation leads to immune evasion of natural killer cells Proc. Natl Acad. Sci. USA 100 2003 13483 13488
18. A.R. French, J.T. Pingel, M. Wagner, I. Bubic, L. Yang, and S. Kim Escape of mutant double-stranded DNA virus from innate immune control Immunity 20 2004 747 756
19. M. Lodoen, K. Ogasawara, J.A. Hamerman, H. Arase, J.P. Houchins, E.S. Mocarski, and L.L. Lanier 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 2003 1245 1253
20. A. Krmpotic, M. Hasan, A. Loewendorf, T. Saulig, A. Halenius, and T. Lenac 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 2005 211 220
21. M.B. Lodoen, G. Abenes, S. Umamoto, J.P. Houchins, F. Liu, and L.L. Lanier The cytomegalovirus m155 gene product subverts natural killer cell antiviral protection by disruption of H60-NKG2D interactions J. Exp. Med. 200 2004 1075 1081
22. T.L. Chapman, and P.J. Bjorkman Characterization of a murine cytomegalovirus class I major histocompatibility complex (MHC) homolog: comparison to MHC molecules and to the human cytomegalovirus MHC homolog J. Virol. 72 1998 460 466
23. H.G. Ljunggren, N.J. Stam, C. Ohlen, J.J. Neefjes, P. Hoglund, and M.T. Heemels Empty MHC class I molecules come out in the cold Nature 346 1990 476 480
24. E. Cretney, M.A. Degli-Esposti, E.H. Densley, H.E. Farrell, N.J. Davis-Poynter, and M.J. Smyth m144, a murine cytomegalovirus (MCMV)-encoded major histocompatibility complex class I homologue, confers tumor resistance to natural killer cell-mediated rejection J. Exp. Med. 190 1999 435 444
25. P. Li, D.L. Morris, B.E. Willcox, A. Steinle, T. Spies, and R.K. Strong Complex structure of the activating immunoreceptor NKG2D and its MHC class I-like ligand MICA Nature Immunol. 2 2001 443 451
26. R.K. Ribaudo, and D.H. Margulies Polymorphism at position nine of the MHC class I heavy chain affects the stability of association with beta 2-microglobulin and presentation of a viral peptide J. Immunol. 155 1995 3481 3493
27. F. Pearl, A. Todd, I. Sillitoe, M. Dibley, O. Redfern, and T. Lewis The CATH Domain Structure Database and related resources Gene3D and DHS provide comprehensive domain family information for genome analysis Nucl. Acids Res. 33 2005 D247 D251
28. M.A. Saper, P.J. Bjorkman, and D.C. Wiley Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 Å resolution J. Mol. Biol. 219 1991 277 319
29. I. Doytchinova, and D. Flower The HLA-A2-supermotif: a QSAR definition Org. Biomol. Chem. 1 2003 2648 2654
30. M. Matsumura, D.H. Fremont, P.A. Peterson, and I.A. Wilson Emerging principles for the recognition of peptide antigens by MHC class I molecules Science 257 1992 927 934
31. T.P. Garrett, M.A. Saper, P.J. Bjorkman, J.L. Strominger, and D.C. Wiley Specificity pockets for the side chains of peptide antigens in HLA-Aw68 Nature 342 1989 692 696
32. D.M. Zajonc, I. Maricic, D. Wu, R. Halder, K. Roy, and C.H. Wong Structural basis for CD1d presentation of a sulfatide derived from myelin and its implications for autoimmunity J. Exp. Med. 202 2005 1517 1526
33. M.G. Rudolph, J.G. Luz, and I.A. Wilson Structural and thermodynamic correlates of T cell signaling Annu. Rev. Biophys. Biomol. Struct. 31 2002 121 149
34. K. Natarajan, N. Dimasi, J. Wang, R.A. Mariuzza, and D.H. Margulies Structure and function of natural killer cell receptors: multiple molecular solutions to self, nonself discrimination Annu. Rev. Immunol. 20 2002 853 885
35. R.K. Strong, and B.J. McFarland NKG2D and related immunoreceptors Advan. Protein Chem. 68 2004 281 312
36. P.S. Kern, M.K. Teng, A. Smolyar, J.H. Liu, J. Liu, and R.E. Hussey Structural basis of CD8 coreceptor function revealed by crystallographic analysis of a murine CD8alphaalpha ectodomain fragment in complex with H-2Kb Immunity 9 1998 519 530
37. G.F. Gao, J. Tormo, U.C. Gerth, J.R. Wyer, A.J. McMichael, and D.I. Stuart Crystal structure of the complex between human CD8alpha(alpha) and HLA-A2 Nature 387 1997 630 634
38. Y. Liu, Y. Xiong, O.V. Naidenko, J.H. Liu, R. Zhang, and A. Joachimiak The crystal structure of a TL/CD8alphaalpha complex at 2.1 Å resolution: implications for modulation of T cell activation and memory Immunity 18 2003 205 215
39. b Nature Immunol. 4 2003 1213 1222
40. J. Tormo, K. Natarajan, D.H. Margulies, and R.A. Mariuzza Crystal structure of a lectin-like natural killer cell receptor bound to its MHC class I ligand Nature 402 1999 623 631
41. b and thymic leukemia antigen, while similarly with their alpha 3 domains J. Immunol. 168 2002 3881 3886
42. N. Matsumoto, W.M. Yokoyama, S. Kojima, and K. Yamamoto The NK cell MHC class I receptor Ly49A detects mutations on H-2Dd inside and outside of the peptide binding groove J. Immunol. 166 2001 4422 4428
43. N. Matsumoto, M. Mitsuki, K. Tajima, W.M. Yokoyama, and K. Yamamoto The functional binding site for the C-type lectin-like natural killer cell receptor Ly49A spans three domains of its major histocompatibility complex class I ligand J. Exp. Med. 193 2001 147 158
44. d and β2-microglobulin J. Biol. Chem. 277 2002 1433 1442
45. I. Bubic, M. Wagner, A. Krmpotic, T. Saulig, S. Kim, and W.M. Yokoyama Gain of virulence caused by loss of a gene in murine cytomegalovirus J. Virol. 78 2004 7536 7544
46. D.M. Andrews, C.E. Andoniou, F. Granucci, P. Ricciardi-Castagnoli, and M.A. Degli-Esposti Infection of dendritic cells by murine cytomegalovirus induces functional paralysis Nature Immunol. 2 2001 1077 1084
47. H.E. Farrell, H. Vally, D.M. Lynch, P. Fleming, G.R. Shellam, A.A. Scalzo, and N.J. Davis-Poynter Inhibition of natural killer cells by a cytomegalovirus MHC class I homologue in vivo Nature 386 1997 510 514
48. A. Kubota, S. Kubota, H.E. Farrell, N. Davis-Poynter, and F. Takei Inhibition of NK cells by murine CMV-encoded class I MHC homologue m144 Cell. Immunol. 191 1999 145 151
49. S.I. Hodgetts, M.J. Spencer, and M.D. Grounds A role for natural killer cells in the rapid death of cultured donor myoblasts after transplantation Transplantation 75 2003 863 871
50. E. Pamer, and P. Cresswell Mechanisms of MHC class I - restricted antigen processing Annu. Rev. Immunol. 16 1998 323 358
51. H.R. Turnquist, S.E. Vargas, E.L. Schenk, M.M. McIlhaney, A.J. Reber, and J.C. Solheim The interface between tapasin and MHC class I: identification of amino acid residues in both proteins that influence their interaction Immunol. Res. 25 2002 261 269
52. M. Bouvier Accessory proteins and the assembly of human class I MHC molecules: a molecular and structural perspective Mol. Immunol. 39 2003 697 706
53. P. Li, S.T. Willie, S. Bauer, D.L. Morris, T. Spies, and R.K. Strong Crystal structure of the MHC class I homolog MIC-A, a gammadelta T cell ligand Immunity 10 1999 577 584
54. O. Nylenna, C. Naper, J.T. Vaage, P.Y. Woon, D. Gauguier, and E. Dissen The genes and gene organization of the Ly49 region of the rat natural killer cell gene complex Eur. J. Immunol. 35 2005 261 272
55. W.D. Rawlinson, H.E. Farrell, and B.G. Barrell Analysis of the complete DNA sequence of murine cytomegalovirus J. Virol. 70 1996 8833 8849
56. M.J. Shields, L.E. Moffat, and R.K. Ribaudo Functional comparison of bovine, murine, and human beta2-microglobulin: interactions with murine MHC I molecules Mol. Immunol. 35 1998 919 928
57. Otiwinowski, Z. & Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. In Macromolecular Crystallography (Carter, C. W. & Sweet, R. M., eds), part A, pp. 307-326, Academic Press, San Diego.
58. J. Navaza AMoRe: an automated package for molecular replacement Acta Crystallog. sect. A 50 1994 157 163
59. Collaborative Computational Project, No. 4 The CCP4 suite: programs for protein crystallography Acta Crystallog. sect. D 50 1994 760 763
60. J.A. Lebron, M.J. Bennett, D.E. Vaughn, A.J. Chirino, P.M. Snow, and G.A. Mintier Crystal structure of the hemochromatosis protein HFE and characterization of its interaction with transferrin receptor Cell 93 1998 111 123
61. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, and H. Weissig The Protein Data Bank Nucl. Acids Res. 28 2000 235 242
62. D.E. McRee XtalView/Xfit - Aa versatile program for manipulating atomic coordinates and electron density J. Struct. Biol. 125 1999 156 165
63. G.N. Murshudov Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallog. sect. D 53 1997 240 255
64. A. Perrakis, R. Morris, and V.S. Lamzin Automated protein model building combined with iterative structure refinement Nature Struct. Biol. 6 1999 458 463
65. A.T. Brunger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, and R.W. Grosse-Kunstleve Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallog. sect. D 54 1998 905 921
66. S.C. Lovell, I.W. Davis, W.B. Arendall III, P.I. de Bakker, J.M. Word, and M.G. Prisant Structure validation by Calpha geometry: phi, psi and Cbeta deviation Proteins: Struct. Funct. Genet. 50 2003 437 450
67. R.A. Laskowski, D.S. Moss, and J.M. Thornton Main-chain bond lengths and bond angles in protein structures J. Mol. Biol. 231 1993 1049 1067
68. M.D. Winn, M.N. Isupov, and G.N. Murshudov Use of TLS parameters to model anisotropic displacements in macromolecular refinement Acta Crystallog. sect. D 57 2001 122 133
69. B. Rost, G. Yachdav, and J. Liu The PredictProtein server Nucl. Acids Res. 32 2004 W321 W326
70. P. Gouet, E. Courcelle, D.I. Stuart, and F. Metoz ESPript: analysis of multiple sequence alignments in PostScript Bioinformatics 15 1999 305 308
71. P. Gouet, X. Robert, and E. Courcelle ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins Nucl. Acids Res. 31 2003 3320 3323
72. J. Risler, M. Delorme, H. Delacroix, and A. Henaut Amino acid substitutions in structurally related proteins. A pattern recognition approach. Determination of a new and efficient scoring matrix J. Mol. Biol. 204 1988 1019 1029