Expansion and protection by a virus-specific NK Cell subset lacking expression of the inhibitory NKR-P1B receptor during murine cytomegalovirus infection

Journal of Immunology

Volumn 197, Issue 6, 2016, Pages 2325-2337

  Rahim, Mir Munir A ^a,e   Wight, Andrew ^a   Mahmoud, Ahmad Bakur ^a,b   Aguilar, Oscar A ^c   Lee, Seung Hwan ^a   Vidal, Silvia M ^d   Carlyle, James R ^c   Makrigiannis, Andrew P ^a,e  

^a UNIVERSITY OF OTTAWA   (Canada)

^b TAIBAH UNIVERSITY   (Saudi Arabia)

^c Sunnybrook Health Sciences Centre   (Canada)

^d MCGILL UNIVERSITY   (Canada)

^e DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD161 ANTIGEN; CD27 ANTIGEN; CD45 ANTIGEN; CD94 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 15; INTERLEUKIN 2; KI 67 ANTIGEN; LECTIN RECEPTOR; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL RECEPTOR NKG2A; KLRB1B PROTEIN, MOUSE; LIGAND; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY B;

ADOPTIVE TRANSFER; ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CELL EXPANSION; CELL MATURATION; CELL PROLIFERATION; CELL PROTECTION; CELL SUBPOPULATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; DEGRANULATION; EMBRYO; FLOW CYTOMETRY; IMMUNE RESPONSE; IN VITRO STUDY; INTERFERON PRODUCTION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEADY STATE; VIRAL CLEARANCE; ANIMAL; C57BL MOUSE; DEFICIENCY; GENETICS; HERPES VIRUS INFECTION; IMMUNOLOGY; MUROMEGALOVIRUS; PHYSIOLOGY;

ANIMALS; HERPESVIRIDAE INFECTIONS; KILLER CELLS, NATURAL; LIGANDS; MICE; MICE, INBRED C57BL; MUROMEGALOVIRUS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY B;

EID: 84988982948     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1600776     Document Type: Article

References (71)

1. Welsh Jr. R. M. 1978. Cytotoxic cells induced during lymphocytic choriomeningitis virus infection of mice. I. Characterization of natural killer cell induction. J. Exp. Med. 148: 163-181.
2. Santoli, D., G. Trinchieri, and H. Koprowski. 1978. Cell-mediated cytotoxicity against virus-infected target cells in humans. II. Interferon induction and activation of natural killer cells. J. Immunol. 121: 532-538.
3. Dix, R. D., E. R. Podack, and S. W. Cousins. 2003. Loss of the perforin cytotoxic pathway predisposes mice to experimental cytomegalovirus retinitis. J. Virol. 77: 3402-3408.
4. Riera, L., M. Gariglio, G. Valente, A. Müllbacher, C. Museteanu, S. Landolfo, and M. M. Simon. 2000. Murine cytomegalovirus replication in salivary glands is controlled by both perforin and granzymes during acute infection. Eur. J. Immunol. 30: 1350-1355.
5. Heise, M. T., and H. W. Virgin, IV. 1995. The T-cell-independent role of g interferon and tumor necrosis factor a in macrophage activation during murine cytomegalovirus and herpes simplex virus infections. J. Virol. 69: 904-909.
6. Orange, J. S., B. Wang, C. Terhorst, and C. A. Biron. 1995. Requirement for natural killer cell-produced interferon g in defense against murine cytomegalovirus infection and enhancement of this defense pathway by interleukin 12 administration. J. Exp. Med. 182: 1045-1056.
7. Presti, R. M., J. L. Pollock, A. J. Dal Canto, A. K. O'Guin, and H. W. Virgin, IV. 1998. Interferon g regulates acute and latent murine cytomegalovirus infection and chronic disease of the great vessels. J. Exp. Med. 188: 577-588.
8. Loh, J., D. T. Chu, A. K. O'Guin, W. M. Yokoyama, and H. W. Virgin, IV. 2005. Natural killer cells utilize both perforin and g interferon to regulate murine cytomegalovirus infection in the spleen and liver. J. Virol. 79: 661-667.
9. Robbins, S. H., G. Bessou, A. Cornillon, N. Zucchini, B. Rupp, Z. Ruzsics, T. Sacher, E. Tomasello, E. Vivier, U. H. Koszinowski, and M. Dalod. 2007. Natural killer cells promote early CD8 T cell responses against cytomegalovirus. PLoS Pathog. 3: e123.
10. Mitrović, M., J. Arapović, S. Jordan, N. Fodil-Cornu, S. Ebert, S. M. Vidal, A. Krmpotić, M. J. Reddehase, and S. Jonjić. 2012. The NK cell response to mouse cytomegalovirus infection affects the level and kinetics of the early CD8+ T-cell response. J. Virol. 86: 2165-2175.
11. Su, H. C., K. B. Nguyen, T. P. Salazar-Mather, M. C. Ruzek, M. Y. Dalod, and C. A. Biron. 2001. NK cell functions restrain T cell responses during viral infections. Eur. J. Immunol. 31: 3048-3055.
12. Waggoner, S. N., M. Cornberg, L. K. Selin, and R. M. Welsh. 2011. Natural killer cells act as rheostats modulating antiviral T cells. Nature 481: 394-398.
13. Lang, P. A., K. S. Lang, H. C. Xu, M. Grusdat, I. A. Parish, M. Recher, A. R. Elford, S. Dhanji, N. Shaabani, C. W. Tran, et al. 2012. Natural killer cell activation enhances immune pathology and promotes chronic infection by limiting CD8+ T-cell immunity. Proc. Natl. Acad. Sci. USA 109: 1210-1215.
14. Orange, J. S. 2006. Human natural killer cell deficiencies. Curr. Opin. Allergy Clin. Immunol. 6: 399-409.
15. Orange, J. S. 2002. Human natural killer cell deficiencies and susceptibility to infection. Microbes Infect. 4: 1545-1558.
16. Biron, C. A., K. S. Byron, and J. L. Sullivan. 1989. Severe herpesvirus infections in an adolescent without natural killer cells. N. Engl. J. Med. 320: 1731-1735.
17. Scalzo, A. A., N. A. Fitzgerald, C. R. Wallace, A. E. Gibbons, Y. C. Smart, R. C. Burton, and G. R. Shellam. 1992. The effect of the Cmv-1 resistance gene, which is linked to the natural killer cell gene complex, is mediated by natural killer cells. J. Immunol. 149: 581-589.
18. Bukowski, J. F., B. A. Woda, and R. M. Welsh. 1984. Pathogenesis of murine cytomegalovirus infection in natural killer cell-depleted mice. J. Virol. 52: 119-128.
19. Welsh, R. M., P. L. Dundon, E. E. Eynon, J. O. Brubaker, G. C. Koo, and C. L. O'Donnell. 1990. Demonstration of the antiviral role of natural killer cells in vivo with a natural killer cell-specific monoclonal antibody (NK 1.1). Nat. Immun. Cell Growth Regul. 9: 112-120.
20. Hsu, A. P., E. P. Sampaio, J. Khan, K. R. Calvo, J. E. Lemieux, S. Y. Patel, D. M. Frucht, D. C. Vinh, R. D. Auth, A. F. Freeman, et al. 2011. Mutations in GATA2 are associated with the autosomal dominant and sporadic monocytopenia and mycobacterial infection (MonoMAC) syndrome. Blood 118: 2653-2655.
21. Lanier, L. L. 1998. NK cell receptors. Annu. Rev. Immunol. 16: 359-393.
22. Carlyle, J. R., A. Mesci, J. H. Fine, P. Chen, S. Bélanger, L. H. Tai, and A. P. Makrigiannis. 2008. Evolution of the Ly49 and Nkrp1 recognition systems. Semin. Immunol. 20: 321-330.
23. Arase, H., E. S. Mocarski, A. E. Campbell, A. B. Hill, and L. L. Lanier. 2002. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296: 1323-1326.
24. Smith, H. R., J. W. Heusel, I. K. Mehta, S. Kim, B. G. Dorner, O. V. Naidenko, K. Iizuka, H. Furukawa, D. L. Beckman, J. T. Pingel, et al. 2002. Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc. Natl. Acad. Sci. USA 99: 8826-8831.
25. Lee, S. H., S. Girard, D. Macina, M. Busa, A. Zafer, A. Belouchi, P. Gros, and S. M. Vidal. 2001. Susceptibility to mouse cytomegalovirus is associated with deletion of an activating natural killer cell receptor of the C-type lectin superfamily. Nat. Genet. 28: 42-45.
26. Brown, M. G., A. O. Dokun, J. W. Heusel, H. R. Smith, D. L. Beckman, E. A. Blattenberger, C. E. Dubbelde, L. R. Stone, A. A. Scalzo, and W. M. Yokoyama. 2001. Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 292: 934-937.
27. Biron, C. A., L. R. Turgiss, and R. M. Welsh. 1983. Increase in NK cell number and turnover rate during acute viral infection. J. Immunol. 131: 1539-1545.
28. Dokun, A. O., S. Kim, H. R. C. Smith, H. S. P. Kang, D. T. Chu, and W. M. Yokoyama. 2001. Specific and nonspecific NK cell activation during virus infection. Nat. Immunol. 2: 951-956.
29. Robbins, S. H., M. S. Tessmer, T. Mikayama, and L. Brossay. 2004. Expansion and contraction of the NK cell compartment in response to murine cytomegalovirus infection. J. Immunol. 173: 259-266.
30. Gumá, M., A. Angulo, C. Vilches, N. Gómez-Lozano, N. Malats, and M. López-Botet. 2004. Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 104: 3664-3671.
31. Orr, M. T.,W. J. Murphy, and L. L. Lanier. 2010. 'Unlicensed' natural killer cells dominate the response to cytomegalovirus infection. Nat. Immunol. 11: 321-327.
32. Corbett, A. J., J. D. Coudert, C. A. Forbes, and A. A. Scalzo. 2011. Functional consequences of natural sequence variation of murine cytomegalovirus m157 for Ly49 receptor specificity and NK cell activation. J. Immunol. 186: 1713-1722.
33. Forbes, C. A., A. A. Scalzo, M. A. Degli-Esposti, and J. D. Coudert. 2014. Ly49C-dependent control of MCMV Infection by NK cells is cis-regulated by MHC class I molecules. PLoS Pathog. 10: e1004161.
34. Kung, S. K., R. C. Su, J. Shannon, and R. G. Miller. 1999. The NKR-P1B gene product is an inhibitory receptor on SJL/J NK cells. J. Immunol. 162: 5876-5887.
35. Carlyle, J. R., A. Mesci, B. Ljutic, S. Belanger, L. H. Tai, E. Rousselle, A. D. Troke, M. F. Proteau, and A. P. Makrigiannis. 2006. Molecular and genetic basis for strain-dependent NK1.1 alloreactivity of mouse NK cells. J. Immunol. 176: 7511-7524.
36. Carlyle, J. R., A. Martin, A. Mehra, L. Attisano, F. W. Tsui, and J. C. Zúniga-Pflücker. 1999. Mouse NKR-P1B, a novel NK1.1 antigen with inhibitory function. J. Immunol. 162: 5917-5923.
37. Aust, J. G., F. Gays, K. M. Mickiewicz, E. Buchanan, and C. G. Brooks. 2009. The expression and function of the NKRP1 receptor family in C57BL/6 mice. J. Immunol. 183: 106-116.
38. Rahim, M. M. A., P. Chen, A. N. Mottashed, A. B. Mahmoud, M. J. Thomas, Q. Zhu, C. G. Brooks, V. Kartsogiannis, M. T. Gillespie, J. R. Carlyle, and A. P. Makrigiannis. 2015. The mouse NKR-P1B:Clr-b recognition system is a negative regulator of innate immune responses. Blood 125: 2217-2227.
39. Carlyle, J. R., A. M. Jamieson, S. Gasser, C. S. Clingan, H. Arase, and D. H. Raulet. 2004. Missing self-recognition of Ocil/Clr-b by inhibitory NKR-P1 natural killer cell receptors. Proc. Natl. Acad. Sci. USA 101: 3527-3532.
40. Iizuka, K., O. V. Naidenko, B. F. Plougastel, D. H. Fremont, and W. M. Yokoyama. 2003. Genetically linked C-type lectin-related ligands for the NKRP1 family of natural killer cell receptors. Nat. Immunol. 4: 801-807.
41. Hao, L., J. Klein, and M. Nei. 2006. Heterogeneous but conserved natural killer receptor gene complexes in four major orders of mammals. Proc. Natl. Acad. Sci. USA 103: 3192-3197.
42. Voigt, S., A. Mesci, J. Ettinger, J. H. Fine, P. Chen, W. Chou, and J. R. Carlyle. 2007. Cytomegalovirus evasion of innate immunity by subversion of the NKRP1B: Clr-b missing-self axis. Immunity 26: 617-627.
43. Aguilar, O. A., A. Mesci, J. Ma, P. Chen, C. L. Kirkham, J. Hundrieser, S. Voigt, D. S. J. Allan, and J. R. Carlyle. 2015. Modulation of Clr ligand expression and NKR-P1 receptor function during murine cytomegalovirus infection. J. Innate Immun. 7: 584-600.
44. Fodil-Cornu, N., S. H. Lee, S. Belanger, A. P. Makrigiannis, C. A. Biron, R. M. Buller, and S. M. Vidal. 2008. Ly49h-deficient C57BL/6 mice: a new mouse cytomegalovirus-susceptible model remains resistant to unrelated pathogens controlled by the NK gene complex. J. Immunol. 181: 6394-6405.
45. Brune, W., H. Hengel, and U. H. Koszinowski. 1999. A mouse model for cytomegalovirus infection. Curr. Protoc. Immunol. Chapter 19: 19.7.1-19.7.13.
46. Bubić, I., M. Wagner, A. Krmpotić, T. Saulig, S. Kim, W. M. Yokoyama, S. Jonjić, and U. H. Koszinowski. 2004. Gain of virulence caused by loss of a gene in murine cytomegalovirus. J. Virol. 78: 7536-7544.
47. Bélanger, S., M. M. Tu, M. M. Rahim, A. B. Mahmoud, R. Patel, L. H. Tai, A. D. Troke, B. T. Wilhelm, J. R. Landry, Q. Zhu, et al. 2012. Impaired natural killer cell self-education and "missing-self" responses in Ly49-deficient mice. Blood 120: 592-602.
48. Alter, G., J. M. Malenfant, and M. Altfeld. 2004. CD107a as a functional marker for the identification of natural killer cell activity. J. Immunol. Methods 294: 15-22.
49. Scholzen, T., and J. Gerdes. 2000. The Ki-67 protein: from the known and the unknown. J. Cell. Physiol. 182: 311-322.
50. Hayakawa, Y., and M. J. Smyth. 2006. CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J. Immunol. 176: 1517-1524.
51. Chiossone, L., J. Chaix, N. Fuseri, C. Roth, E. Vivier, and T. Walzer. 2009. Maturation of mouse NK cells is a 4-stage developmental program. Blood 113: 5488-5496.
52. Vivier, E., E. Tomasello, M. Baratin, T. Walzer, and S. Ugolini. 2008. Functions of natural killer cells. Nat. Immunol. 9: 503-510.
53. Lee, S. H., M. F. Fragoso, and C. A. Biron. 2012. Cutting edge: a novel mechanism bridging innate and adaptive immunity: IL-12 induction of CD25 to form high-affinity IL-2 receptors on NK cells. J. Immunol. 189: 2712-2716.
54. Pyzik, M., B. Charbonneau, E. M. Gendron-Pontbriand, M. Babić, A. Krmpotić, S. Jonjić, and S. M. Vidal. 2011. Distinct MHC class I-dependent NK cellactivating receptors control cytomegalovirus infection in different mouse strains. J. Exp. Med. 208: 1105-1117.
55. Sun, J. C., J. N. Beilke, and L. L. Lanier. 2009. Adaptive immune features of natural killer cells. Nature 457: 557-561.
56. Kartsogiannis, V., N. A. Sims, J. M. Quinn, C. Ly, M. Cipetic, I. J. Poulton, E. C. Walker, H. Saleh, N. E. McGregor, M. E. Wallace, et al. 2008. Osteoclast inhibitory lectin, an immune cell product that is required for normal bone physiology in vivo. J. Biol. Chem. 283: 30850-30860.
57. Béziat, V., L. L. Liu, J. A. Malmberg, M. A. Ivarsson, E. Sohlberg, A. T. Björklund, C. Retiere, E. Sverremark-Ekström, J. Traherne, P. Ljungman, et al. 2013. NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs. Blood 121: 2678-2688.
58. Ali, A. K., J. S. Oh, E. Vivier, M. Busslinger, and S. H. Lee. 2016. NK cellspecific Gata3 ablation identifies the maturation program required for bone marrow exit and control of proliferation. J. Immunol. 196: 1753-1767.
59. Andrews, D. M., A. A. Scalzo, W. M. Yokoyama, M. J. Smyth, and M. A. Degli-Esposti. 2003. Functional interactions between dendritic cells and NK cells during viral infection. Nat. Immunol. 4: 175-181.
60. Vance, R. E., J. R. Kraft, J. D. Altman, P. E. Jensen, and D. H. Raulet. 1998. Mouse CD94/NKG2A is a natural killer cell receptor for the nonclassical major histocompatibility complex (MHC) class I molecule Qa-1(b). J. Exp. Med. 188: 1841-1848.
61. Karlhofer, F. M., R. K. Ribaudo, and W. M. Yokoyama. 1992. MHC class I alloantigen specificity of Ly-49+ IL-2-activated natural killer cells. Nature 358: 66-70.
62. Yokoyama, W. M. 1995. Natural killer cell receptors specific for major histocompatibility complex class I molecules. Proc. Natl. Acad. Sci. USA 92: 3081-3085.
63. Tomasec, P., V. M. Braud, C. Rickards, M. B. Powell, B. P. McSharry, S. Gadola, V. Cerundolo, L. K. Borysiewicz, A. J. McMichael, and G. W. G. Wilkinson. 2000. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287: 1031-1033.
64. Ulbrecht, M., S. Martinozzi, M. Grzeschik, H. Hengel, J. W. Ellwart, M. Pla, and E. H. Weiss. 2000. Cutting edge: the human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cell-mediated lysis. J. Immunol. 164: 5019-5022.
65. Wang, E. C. Y., B. McSharry, C. Retiere, P. Tomasec, S.Williams, L. K. Borysiewicz, V. M. Braud, and G. W. G. Wilkinson. 2002. UL40-mediated NK evasion during productive infection with human cytomegalovirus. Proc. Natl. Acad. Sci. USA 99: 7570-7575.
66. Cavanaugh, V. J., D. H. Raulet, and A. E. Campbell. 2007. Upregulation of CD94/NKG2A receptors and Qa-1b ligand during murine cytomegalovirus infection of salivary glands. J. Gen. Virol. 88: 1440-1445.
67. Orr, M. T., J. Wu, M. Fang, L. J. Sigal, P. Spee, T. Egebjerg, E. Dissen, S. Fossum, J. H. Phillips, and L. L. Lanier. 2010. Development and function of CD94-deficient natural killer cells. PLoS One 5: e15184.
68. Chen, P., O. A. Aguilar, M. M. A. Rahim, D. S. J. Allan, J. H. Fine, C. L. Kirkham, J. Ma, M. Tanaka, M. M. Tu, A. Wight, et al. 2015. Genetic investigation of MHC-independent missing-self recognition by mouse NK cells using an in vivo bone marrow transplantation model. J. Immunol. 194: 2909-2918.
69. Chen, P., S. Bélanger, O. A. Aguilar, Q. Zhang, A. St-Laurent, M. M. Rahim, A. P. Makrigiannis, and J. R. Carlyle. 2011. Analysis of the mouse 129-strain Nkrp1-Clr gene cluster reveals conservation of genomic organization and functional receptor-ligand interactions despite significant allelic polymorphism. Immunogenetics 63: 627-640.
70. Kveberg, L., K. Z. Dai, M. Inngjerdingen, C. G. Brooks, S. Fossum, and J. T. Vaage. 2011. Phylogenetic and functional conservation of the NKR-P1F and NKR-P1G receptors in rat and mouse. Immunogenetics 63: 429-436.
71. Leibelt, S., M. E. Friede, C. Rohe, D. Gütle, E. Rutkowski, A. Weigert, L. Kveberg, J. T. Vaage, M. W. Hornef, and A. Steinle. 2015. Dedicated immunosensing of the mouse intestinal epithelium facilitated by a pair of genetically coupled lectin-like receptors. Mucosal Immunol. 8: 232-242.