Glycosylation contributes to variability in expression of murine cytomegalovirus m157 and enhances stability of interaction with the NK-cell receptor Ly49H

European Journal of Immunology

Volumn 40, Issue 9, 2010, Pages 2618-2631

  Guseva, Natalya V ^a   Fullenkamp, Colleen A ^a   Naumann, Paul W ^a   Shey, Michael R ^a   Ballas, Zuhair K ^a   Houtman, Jon C D ^a   Forbes, Catherine A ^b,c   Scalzo, Anthony A ^b,c   Heusel, Jonathan W ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c LIONS EYE INSTITUTE   (Australia)

Author keywords

Glycosylation; Lectin; NK cell; Viral immunity

Indexed keywords

ISOPROTEIN; KLRA8 PROTEIN, MOUSE; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY A; PROTEIN BINDING; VIRUS PROTEIN;

ANIMAL; BONE MARROW CELL; CELL LINE; FIBROBLAST; GENETICS; GLYCOSYLATION; HERPES VIRUS INFECTION; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE; MUROMEGALOVIRUS; MUTATION; NATURAL KILLER CELL; PATHOGENICITY; PATHOLOGY; SITE DIRECTED MUTAGENESIS; TRANSGENE; VIROLOGY;

ANIMALS; CELL LINE; FIBROBLASTS; GLYCOSYLATION; HERPESVIRIDAE INFECTIONS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MICE; MUROMEGALOVIRUS; MUTAGENESIS, SITE-DIRECTED; MUTATION; MYELOID CELLS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY A; PROTEIN BINDING; PROTEIN ISOFORMS; TRANSGENES; VIRAL PROTEINS;

EID: 77956485322     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200940134     Document Type: Article

References (52)

1. Lanier, L. L., Evolutionary struggles between NK cells and viruses. Nat. Rev. Immunol. 2008. 8: 259-268.
2. Scalzo, A. A. and Yokoyama, W. M., Cmv1 and natural killer cell responses to murine cytomegalovirus infection. Curr. Top. Microbiol. Immunol. 2008. 321: 101-122.
3. Yokoyama, W. M., Specific and non-specific natural killer cell responses to viral infection. Adv. Exp. Med. Biol. 2005. 560: 57-61.
4. Orange, J. S., Human natural killer cell deficiencies and susceptibility to infection. Microbes Infect. 2002. 4: 1545-1558.
5. Zelensky, A. N. and Gready, J. E., The C-type lectin-like domain super-family. FEBS J. 2005. 272: 6179-6217.
6. Yokoyama,W. M. and Plougastel, B. F., Immune functions encoded by the natural killer gene complex. Nat. Rev. Immunol. 2003. 3: 304-316.
7. Kumar, V. and McNerney, M. E., A new self: MHC-class-I-independent natural-killer-cell self-tolerance. Nat. Rev. Immunol. 2005. 5: 363-374.
8. Arase, H., Mocarski, E. S., Campbell, A. E., Hill, A. B. and Lanier, L. L., Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. [comment]. Science 2002. 296: 1323-1326.
9. Scalzo, A. A., Corbett, A. J., Rawlinson, W. D., Scott, G. M. and Degli- Esposti, M. A., The interplay between host and viral factors in shaping the outcome of cytomegalovirus infection. Immunol. Cell. Biol. 2007. 85: 46-54.
10. Voigt, V., Forbes, C. A., Tonkin, J. N., Degli-Esposti, M. A., Smith, H. R. C., Yokoyama, W. M. and Scalzo, A. A., Murine cytomegalovirus m157 mutation and variation leads to immune evasion of natural killer cells. Proc. Natl. Acad. Sci. 2003. 100: 13483-13488.
11. Cerwenka, A. and Lanier, L. L., NKG2D ligands: unconventional MHC class I-like molecules exploited by viruses and cancer. Tissue Antigens 2003. 61: 335-343.
12. Voigt, S., Mesci, A., Ettinger, J., Fine, J. H., Chen, P., Chou, W. and Carlyle, J. R., Cytomegalovirus evasion of innate immunity by subversion of the NKR-P1B:Clr-b missing-self axis. Immunity 2007. 26: 617-627.
13. Lenac, T., Arapovic, J., Traven, L., Krmpotic, A. and Jonjic, S., Murine cytomegalovirus regulation of NKG2D ligands. Med. Microbiol. Immunol. 2008. 197: 159-166.
14. Smith, H. R., Heusel, J. W., Mehta, I. K., Kim, S., Dorner, B. G., Naidenko, O. V., Iizuka, K. et al., Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc. Natl. Acad. Sci. USA 2002. 99: 8826-8831.
15. Scalzo, A. A., Fitzgerald, N. A., Simmons, A., La Vista, A. B. and Shellam, G. R., Cmv-1, a genetic locus that controls murine cytomegalovirus replication in the spleen. J. Exp. Med. 1990. 171: 1469-1483.
16. Brown, M. G., Dokun, A. O., Heusel, J. W., Smith, H. R., Beckman, D. L., Blattenberger, E. A., Dubbelde, C. E. et al., Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 2001. 292: 934-937.
17. Daniels, K. A., Devora, G., Lai, W. C., O'Donnell, C. L., Bennett, M. and Welsh, R. M., Murine cytomegalovirus is regulated by a discrete subset of natural killer cells reactive with monoclonal antibody to Ly49H. J. Exp. Med. 2001. 194: 29-44.
18. Lee, S. H., Girard, S., Macina, D., Busa, M., Zafer, A., Belouchi, A., Gros, P. and Vidal, S. M., Susceptibility to mouse cytomegalovirus is associated with deletion of an activating natural killer cell receptor of the C- type lectin superfamily. [comment]. Nat. Genet. 2001. 28: 42-45.
19. Abi-Rached, L. and Parham, P., Natural selection drives recurrent formation of activating killer cell immunoglobulin-like receptor and Ly49 from inhibitory homologues. J. Exp. Med. 2005. 201: 1319-1332.
20. Arase, H. and Lanier, L. L., Virus-driven evolution of natural killer cell receptors. Microbes Infect. 2002. 4: 1505-1512.
21. Sun, J. C. and Lanier, L. L., Tolerance of NK cells encountering their viral ligand during development. J. Exp. Med. 2008. 205: 1819-1828.
22. Deng, L. and Mariuzza, R. A., Structural basis for recognition of MHC and MHC-like ligands by natural killer cell receptors. Semin. Immunol. 2006. 18: 159-166.
23. Strong, R. K., Asymmetric ligand recognition by the activating natural killer cell receptor NKG2D, a symmetric homodimer. Mol. Immunol. 2002. 38: 1029-1037.
24. Hudrisier, J. E., What is trogocytosis and what is its purpose? Nat. Immunol. 2003. 4: 815.
25. Sjostrom,A., Eriksson, M., Cerboni, C., Johansson, M. H., Sentman, C. L., Karre, K. and Hoglund, P., Acquisition of external major histocompatibility complex class I molecules by natural killer cells expressing inhibitory Ly49 receptors. J. Exp. Med. 2001. 194: 1519-1530.
26. Zimmer, J., Ioannidis, V. and Held, W., H-2D ligand expression by Ly49A+natural killer (NK) cells precludes ligand uptake from environmental cells: implications for NK cell function. J. Exp. Med. 2001. 194: 1531-1539.
27. Roda-Navarro, P., Vales-Gomez, M., Chisholm, S. E. and Reyburn, H. T., Transfer of NKG2D and MICB at the cytotoxic NK cell immune synapse correlates with a reduction in NK cell cytotoxic function. Proc. Natl. Acad. Sci. USA 2006. 103: 11258-11263.
28. McCann, F. E., Eissmann, P., Onfelt, B., Leung, R. and Davis, D. M., The activating NKG2D ligand MHC class I-related chain A transfers from target cells to NK cells in a manner that allows functional consequences. J. Immunol. 2007. 178: 3418-3426.
29. Davis, A. H., Guseva, N. V., Ball, B. L. and Heusel, J. W., Characterization of murine cytomegalovirus m157 from infected cells and identification of critical residues mediating recognition by the NK cell receptor Ly49H. J. Immunol. 2008. 181: 265-275.
30. Gasteiger, E. G. A., Hoogland, C., Ivanyi, I., Appel, R. D., Bairoch, A., ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 2003. 31: 3784-3788.
31. Tripathy, S. K., Smith, H. R. C., Holroyd, E. A., Pingel, J. T. and Yokoyama, W. M., Expression of m157, a murine cytomegalovirus-encoded putative major histocompatibility class I (MHC-I)-like protein, is independent of viral regulation of host MHC-I. J. Virol. 2006. 80: 545-550.
32. Linstedt, A. D. and Hauri, H. P., Giantin, a novel conserved Golgi membrane protein containing a cytoplasmic domain of at least 350 kDa. Mol. Biol. Cell 1993. 4: 679-693.
33. Dorner, B. G., Smith, H. R., French, A. R., Kim, S., Poursine-Laurent, J., Beckman, D. L., Pingel, J. T. et al., Coordinate expression of cytokines and chemokines by NK cells during murine cytomegalovirus infection. J. Immunol. 2004. 172: 3119-3131.
34. Smith, H. R., Chuang, H. H., Wang, L. L., Salcedo, M., Heusel, J. W. and Yokoyama, W. M., Nonstochastic coexpression of activation receptors on murine natural killer cells. J. Exp. Med. 2000. 191: 1341-1354.
35. Dokun, A. O., Kim, S., Smith, H. R., Kang, H. S., Chu, D. T. and Yokoyama, W. M., Specific and nonspecific NK cell activation during virus infection. Nat. Immunol. 2001. 2: 951-956.
36. Ahmed, K. A., Munegowda, M. A., Xie, Y. and Xiang, J., Intercellular trogocytosis plays an important role in modulation of immune responses. Cell. Mol. Immunol. 2008. 5: 261-269.
37. Caumartin, J., Lemaoult, J. and Carosella, E. D., Intercellular exchanges of membrane patches (trogocytosis) highlight the next level of immune plasticity. Transpl. Immunol. 2006. 17: 20-22.
38. Carlin, L. M., Eleme, K., McCann, F. E. and Davis, D. M., Intercellular transfer and supramolecular organization of human leukocyte antigen C at inhibitory natural killer cell immune synapses. J. Exp. Med. 2001. 194: 1507-1517.
39. Helenius, A. and Aebi, M., Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 2004. 73: 1019-1049.
40. Helenius, A., How N-linked oligosaccharides affect glycoprotein folding in the endoplasmic reticulum. Mol. Biol. Cell 1994. 5: 253-265.
41. Adams, E. J., Juo, Z. S., Venook, R. T., Boulanger, M. J., Arase, H., Lanier, L. L. and Garcia, K. C., Structural elucidation of the m157 mouse cytomegalovirus ligand for Ly49 natural killer cell receptors. Proc. Natl. Acad. Sci. USA 2007. 104: 10128-10133.
42. Jones, J., Krag, S. S. and Betenbaugh, M. J., Controlling N-linked glycan site occupancy. Biochim. Biophys. Acta 2005. 1726: 121-137.
43. Lederkeremer, G. Z. and Glickman, M. H., A window of opportunity: timing protein degradation by trimming of sugars and ubiquitins. Trends Biochem. Sci. 2005. 30: 297-303.
44. Everts, I., Villmann, C. and Hollmann, M., N-Glycosylation is not a prerequisite for glutamate receptor function but is essential for lectin modulation. Mol. Pharmacol. 1997. 52: 861-873.
45. He, Y., Ramsay, A. J., Hunt, M. L., Whitbread, A. K., Myers, S. A. and Hooper, J. D., N-glycosylation analysis of the human Tweety family of putative chloride ion channels supports a penta-spanning membrane arrangement: impact of N-glycosylation on cellular processing of Tweety homologue 2 (TTYH2). Biochem. J. 2008. 412: 45-55.
46. Vigerust, D. J. and Shepherd, V. L., Virus glycosylation: role in virulence and immune interactions. Trends Microbiol. 2007. 15: 211-218.
47. McFarland, B. J. and Strong, R. K., Thermodynamic analysis of degenerate recognition by the NKG2D immunoreceptor: not induced fit but rigid adaptation. Immunity 2003. 19: 803-812.
48. Andersson, K. E., Williams, G. S., Davis, D. M. and Hoglund, P., Quantifying the reduction in accessibility of the inhibitory NK cell receptor Ly49A caused by binding MHC class I proteins in cis. Eur. J. Immunol. 2007. 37: 516-527.
49. Lian, R. H., Freeman, J. D., Mager, D. L. and Takei, F., Role of conserved glycosylation site unique to murine class I MHC in recognition by Ly-49 NK cell receptor. J. Immunol. 1998. 161: 2301-2306.
50. van Den Pol, A. N., Mocarski, E., Saederup, N., Vieira, J. and Meier, T. J., Cytomegalovirus cell tropism, replication, and gene transfer in brain. J. Neurosci. 1999. 19: 10948-10965.
51. Karttunen, J. and Shastri, N., Measurement of ligand-induced activation in single viable T cells using the lacZ reporter gene. Proc. Natl. Acad. Sci. 1991. 88: 3972-3976.
52. Shey, M. R. and Ballas, Z. K., Assessment of natural killer (NK) and NKT cells in murine spleens and livers. Methods Mol. Biol. 2008: 447: 259-276.