The Direct Influence of Cytomegalovirus Lysate on the Natural Killer Cell Receptor Repertoire
Abstract
Natural killer (NK) cells are essential for controlling certain viral infections, including cytomegalovirus (CMV). In particular, the importance of NK cells in the context of CMV infection is underscored by the adaptive capabilities of these cells. Evidence suggests that some viruses can directly interfere with NK cell compartments and their activation and lead to shape-shifting the NK cell receptor repertoire. Still, it remains unknown whether the CMV can interact with NK cells without intermediaries. Here, we examined whether the direct effects of CMV lysate alter phenotypical properties of NK cells.
To investigate this issue, NK cells were isolated from the blood of CMV seropositive healthy donors by negative magnetic separation. Isolated NK cells were cultured in the presence of CMV lysate and analyzed for the expression of NKG2A, NKG2C, and CD57 by FACS caliber.
The results showed that NKG2C expression is significantly upregulated in the presence of CMV lysate compared to without stimulated group (mean increase, 6.65 %; 95% CI, 0.2582 to 13.02; p=0.043; R square: 0.38). Likewise, results have shown a significant decrease in the frequency of NKG2A+CD57- NK cell subsets (p=0.005; 95% CI, -13.49 to -3.151; R square: 0.5957) in the stimulated group compared to without stimulated ones.
According to these results, CMV may drive a direct influence on NK cell receptor repertoire, including the expansion of NK cells expressing NKG2C receptor, which is needed for further studies.
1. Wetwittayakhlang P, Rujeerapaiboon N, Sripongpun P, Pruphetkaew N, Jandee S, et al. Clinical Features, Endoscopic Findings, and Predictive Factors for Mortality in Tissue-Invasive Gastrointestinal Cytomegalovirus Disease between Immunocompetent and Immunocompromised Patients. Gastroenterol Res Pract. 2021;2021.
2. Janahi EMA, Das S, Bhattacharya SN, Haque S, Akhter N, Jawed A, et al. Cytomegalovirus aggravates the autoimmune phenomenon in systemic autoimmune diseases. Microb Pathog. 2018;120(8):132-9.
3. Tsai WP, Chen MH, Lee MH, Yu KH, Wu MW, Liou LB. Cytomegalovirus infection causes morbidity and mortality in patients with autoimmune diseases, particularly systemic lupus: in a Chinese population in Taiwan. Rheumatol Int. 2012;32(9):2901-8.
4. Rowshani AT, Bemelman FJ, van Leeuwen EM, van Lier RA, ten Berge IJ. Clinical and immunologic aspects of cytomegalovirus infection in solid organ transplant recipients. Transplantation. 2005;79(4):381-6.
5. Afshari A, Yaghobi R, Karimi MH, Darbouy M, Azarpira N, Geramizadeh B, et al. IL-17 mRNA expression and cytomegalovirus infection in liver transplant patients. Exp Clin Transplant. 2015;13(Suppl 1):83-9.
6. Scalzo AA. Successful control of viruses by NK cells–a balance of opposing forces? Trends Microbiol. 2002;10(10):470-4.
7. Herberman RB, Nunn ME, Lavrin DH. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic and allogeneic tumors. I. Distribution of reactivity and specificity. Int J Cancer. 1975;16(2):216-29.
8. Kiessling R, Klein E, Wigzell H. „Natural” ︁ killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur J Immunol. 1975;5(2):112-7.
9. Smyth MJ, Cretney E, Kelly JM, Westwood JA, Street SE, Yagita H, et al. Activation of NK cell cytotoxicity. Mol Immunol. 2005;42(4):501-10.
10. Hendricks DW, Balfour HH, Dunmire SK, Schmeling DO, Hogquist KA, Lanier LL. Cutting edge: NKG2ChiCD57+ NK cells respond specifically to acute infection with cytomegalovirus and not Epstein–Barr virus. J Immunol. 2014;192(10):4492-6.
11. Björkström NK, Svensson A, Malmberg K-J, Eriksson K, Ljunggren H-G. Characterization of natural killer cell phenotype and function during recurrent human HSV-2 infection. PLoS One. 2011;6(11):e27664.
12. Goodier MR, Jonjić S, Riley EM, Juranić Lisnić V. CMV and natural killer cells: shaping the response to vaccination. Eur J Immunol. 2018;48(1):50-65.
13. Lodoen MB, Lanier LL. Natural killer cells as an initial defense against pathogens. Curr Opin Immunol. 2006;18(4):391-8.
14. Soleimanian S, Yaghobi R. Harnessing memory NK cell to protect against COVID-19. Front Pharmacol. 2020;11(2):11-9.
15. Brillantes M, Beaulieu AM. Memory and Memory-Like NK Cell Responses to Microbial Pathogens. Front Cell Infect Microbiol. 2020;10(102):57-9.
16. López-Botet M, Muntasell A, Martínez-Rodríguez JE, López-Montañés M, Costa-García M, Pupuleku A. Development of the adaptive NK cell response to human cytomegalovirus in the context of aging. Mech Ageing Dev. 2016;158(41):23-6.
17. Monsiváis‐Urenda A, Noyola‐Cherpitel D, Hernández‐Salinas A, García‐Sepúlveda C, Romo N, Baranda L, et al. Influence of human cytomegalovirus infection on the NK cell receptor repertoire in children. Eur J Immunol. 2010;40(5):1418-27.
18. Lam VC, Lanier LL. NK cells in host responses to viral infections. Curr Opin Immunol. 2017;44(5):43-51.
19. Heatley SL, Pietra G, Lin J, Widjaja JM, Harpur CM, Lester S, et al. Polymorphism in human cytomegalovirus UL40 impacts on recognition of human leukocyte antigen-E (HLA-E) by natural killer cells. J Biol Chem. 2013;288(12):8679-90.
20. Béziat V, Hervier B, Achour A, Boutolleau D, Marfain-Koka A, Vieillard V. Human NKG2A overrides NKG2C effector functions to prevent autoreactivity of NK cells. Blood. 2011;117(16):4394-6.
21. Hammer Q, Rückert T, Borst EM, Dunst J, Haubner A, Durek P, et al. Peptide-specific recognition of human cytomegalovirus strains controls adaptive natural killer cells. Nat Immunol. 2018;19(5):453-63.
22. Liu LL, Landskron J, Ask EH, Enqvist M, Sohlberg E, Traherne JA, et al. Critical role of CD2 co-stimulation in adaptive natural killer cell responses revealed in NKG2C-deficient humans. Cell Rep. 2016;15(5):1088-99.
23. Béziat V, Liu LL, Malmberg J-A, Ivarsson MA, Sohlberg E, Björklund AT, et al. NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs. Blood. 2013;121(14):2678-88.
24. Adib‐Conquy M, Scott‐Algara D, Cavaillon JM, Souza‐Fonseca‐Guimaraes F. TLR‐mediated activation of NK cells and their role in bacterial/viral immune responses in mammals. Immunol. Cell Biol. 2014;92(3):256-62.
25. Kurt-Jones EA, Chan M, Zhou S, Wang J, Reed G, Bronson R, et al. Herpes simplex virus 1 interaction with Toll-like receptor 2 contributes to lethal encephalitis. PNAS. 2004;101(5):1315-20.
26. Wujcicka W, Wilczyński J, Nowakowska D. Alterations in TLRs as new molecular markers of congenital infections with Human cytomegalovirus? Pathog. Dis. 2014;70(1):3-16.
27. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. 2010;11(5):373-8.
28. Newman KC, Riley EM. Whatever turns you on: accessory-cell-dependent activation of NK cells by pathogens. Nat. Rev. Immunol. 2007;7(4):279-91.
29. Hanna J, Gonen-Gross T, Fitchett J, Rowe T, Daniels M, Arnon TI, et al. Novel APC-like properties of human NK cells directly regulate T cell activation. J Clin Invest. 2004;114(11):1612-23.
30. Schlums H, Cichocki F, Tesi B, Theorell J, Beziat V, Holmes TD, et al. Cytomegalovirus infection drives adaptive epigenetic diversification of NK cells with altered signaling and effector function. Immunity. 2015;42(3):443-56.
31. Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature. 2009;457(7229):557-61.
32. Gumá M, Budt M, Sáez A, Brckalo T, Hengel H, Angulo A, et al. Expansion of CD94/NKG2C+ NK cells in response to human cytomegalovirus-infected fibroblasts. Blood. 2006;107(9):3624-31.
33. Muntasell A, Vilches C, Angulo A, López‐Botet M. Adaptive reconfiguration of the human NK‐cell compartment in response to cytomegalovirus: a different perspective of the host‐pathogen interaction. Eur J Immunol. 2013;43(5):1133-41.
34. Guma M, Angulo A, Lopez-Botet M. NK cell receptors involved in the response to human cytomegalovirus infection. Curr Top Microbiol Immunol. 2006;298:207-23.
35. Braud VM, Allan DS, O'callaghan CA, Söderström K, D'andrea A, Ogg GS, et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature. 1998;391(6669):795-9.
36. Kovalenko EI, Streltsova MA, Kanevskiy LM, Erokhina SA, Telford WG. Identification of Human Memory-Like NK Cells. Curr Protoc Cytom. 2017;9:50.1-9.
37. Björkström NK, Riese P, Heuts F, Andersson S, Fauriat C, Ivarsson MA, et al. Expression patterns of NKG2A, KIR, and CD57 define a process of CD56 dim NK-cell differentiation uncoupled from NK-cell education. Blood. 2010;116(19):3853-64.
38. Foley B, Cooley S, Verneris MR, Pitt M, Curtsinger J, Luo X, et al. Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood. 2012;119(11):2665-74.
39. Hammer Q, Rückert T, Romagnani C. Natural killer cell specificity for viral infections. Nat Immunol. 2018;19(8):800-8.
40. Rölle A, Mousavi-Jazi M, Eriksson M, Odeberg J, Söderberg-Nauclér C, Cosman D, et al. Effects of human cytomegalovirus infection on ligands for the activating NKG2D receptor of NK cells: up-regulation of UL16-binding protein (ULBP) 1 and ULBP2 is counteracted by the viral UL16 protein. J Immunol. 2003;171(2):902-8.
41. Prod’homme V, Tomasec P, Cunningham C, Lemberg MK, Stanton RJ, McSharry BP, et al. Human cytomegalovirus UL40 signal peptide regulates cell surface expression of the NK cell ligands HLA-E and gpUL18. J Immunol. 2012;188(6):2794-804.
42. Streltsova MA, Erokhina SA, Kanevskiy LM, Lee DA, Telford WG, Sapozhnikov AM, et al. Analysis of NK cell clones obtained using interleukin-2 and gene-modified K562 cells revealed the ability of “senescent” NK cells to lose CD57 expression and start expressing NKG2A. PLoS One. 2018;13(12):e0208469.
43. Kobyzeva PA, Streltsova MA, Erokhina SA, Kanevskiy LM, Telford WG, Sapozhnikov AM, et al. CD56dimCD57− NKG2C+ NK cells retaining proliferative potential are possible precursors of CD57+ NKG2C+ memory‐like NK cells. J Leukoc Biol. 2020;108(4):1379-95.
44. Björkström NK, Riese P, Heuts F, Andersson S, Fauriat C, Ivarsson MA, et al. Expression patterns of NKG2A, KIR, and CD57 define a process of CD56dim NK-cell differentiation uncoupled from NK-cell education. Blood. 2010;116(19):3853-64.
45. Moretta A, Marcenaro E, Parolini S, Ferlazzo G, Moretta L. NK cells at the interface between innate and adaptive immunity. Cell Death Differ. 2008;15(2):226-33.
46. Kim M, Osborne NR, Zeng W, Donaghy H, McKinnon K, Jackson DC, et al. Herpes simplex virus antigens directly activate NK cells via TLR2, thus facilitating their presentation to CD4 T lymphocytes. J Immunol. 2012;188(9):4158-70.
47. Staege M, Dick T, Ertl R, Jahnel U, Nawrath H, Rammensee H, et al. The antigen self-presentation function of the cytotoxic T-cell clone 10BK. 1 depends on reciprocal peptide presentation. Immunology. 1994;81(3):333-9.
48. Newhook N, Fudge N, Grant M. NK cells generate memory‐type responses to human cytomegalovirus‐infected fibroblasts. Eur J Immunol. 2017;47(6):1032-9.
49. Della Chiesa M, De Maria A, Muccio L, Bozzano F, Sivori S, Moretta L. Human NK cells and Herpesviruses: mechanisms of recognition, response and adaptation. Front Microbiol. 2019;10(4):2297-9.
50. Bortolotti D, Gentili V, Caselli E, Sicolo M, Soffritti I, D’Accolti M, et al. DNA Sensors’ Signaling in NK Cells During HHV-6A, HHV-6B and HHV-7 Infection. Front Microbiol. 2020;11(4):226-31.
51. Mao H, Tu W, Qin G, Law HKW, Sia SF, Chan P-L, et al. Influenza virus directly infects human natural killer cells and induces cell apoptosis. J Virol. 2009;83(18):9215-22.
52. Chiesa S, Mingueneau M, Fuseri N, Malissen B, Raulet DH, Malissen M, et al. Multiplicity and plasticity of natural killer cell signaling pathways. Blood. 2006;107(6):2364-72.
53. Hammer Q, Romagnani C. About training and memory: NK-cell adaptation to viral infections. Adv Immunol. 2017;133(5):171-207.
2. Janahi EMA, Das S, Bhattacharya SN, Haque S, Akhter N, Jawed A, et al. Cytomegalovirus aggravates the autoimmune phenomenon in systemic autoimmune diseases. Microb Pathog. 2018;120(8):132-9.
3. Tsai WP, Chen MH, Lee MH, Yu KH, Wu MW, Liou LB. Cytomegalovirus infection causes morbidity and mortality in patients with autoimmune diseases, particularly systemic lupus: in a Chinese population in Taiwan. Rheumatol Int. 2012;32(9):2901-8.
4. Rowshani AT, Bemelman FJ, van Leeuwen EM, van Lier RA, ten Berge IJ. Clinical and immunologic aspects of cytomegalovirus infection in solid organ transplant recipients. Transplantation. 2005;79(4):381-6.
5. Afshari A, Yaghobi R, Karimi MH, Darbouy M, Azarpira N, Geramizadeh B, et al. IL-17 mRNA expression and cytomegalovirus infection in liver transplant patients. Exp Clin Transplant. 2015;13(Suppl 1):83-9.
6. Scalzo AA. Successful control of viruses by NK cells–a balance of opposing forces? Trends Microbiol. 2002;10(10):470-4.
7. Herberman RB, Nunn ME, Lavrin DH. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic and allogeneic tumors. I. Distribution of reactivity and specificity. Int J Cancer. 1975;16(2):216-29.
8. Kiessling R, Klein E, Wigzell H. „Natural” ︁ killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur J Immunol. 1975;5(2):112-7.
9. Smyth MJ, Cretney E, Kelly JM, Westwood JA, Street SE, Yagita H, et al. Activation of NK cell cytotoxicity. Mol Immunol. 2005;42(4):501-10.
10. Hendricks DW, Balfour HH, Dunmire SK, Schmeling DO, Hogquist KA, Lanier LL. Cutting edge: NKG2ChiCD57+ NK cells respond specifically to acute infection with cytomegalovirus and not Epstein–Barr virus. J Immunol. 2014;192(10):4492-6.
11. Björkström NK, Svensson A, Malmberg K-J, Eriksson K, Ljunggren H-G. Characterization of natural killer cell phenotype and function during recurrent human HSV-2 infection. PLoS One. 2011;6(11):e27664.
12. Goodier MR, Jonjić S, Riley EM, Juranić Lisnić V. CMV and natural killer cells: shaping the response to vaccination. Eur J Immunol. 2018;48(1):50-65.
13. Lodoen MB, Lanier LL. Natural killer cells as an initial defense against pathogens. Curr Opin Immunol. 2006;18(4):391-8.
14. Soleimanian S, Yaghobi R. Harnessing memory NK cell to protect against COVID-19. Front Pharmacol. 2020;11(2):11-9.
15. Brillantes M, Beaulieu AM. Memory and Memory-Like NK Cell Responses to Microbial Pathogens. Front Cell Infect Microbiol. 2020;10(102):57-9.
16. López-Botet M, Muntasell A, Martínez-Rodríguez JE, López-Montañés M, Costa-García M, Pupuleku A. Development of the adaptive NK cell response to human cytomegalovirus in the context of aging. Mech Ageing Dev. 2016;158(41):23-6.
17. Monsiváis‐Urenda A, Noyola‐Cherpitel D, Hernández‐Salinas A, García‐Sepúlveda C, Romo N, Baranda L, et al. Influence of human cytomegalovirus infection on the NK cell receptor repertoire in children. Eur J Immunol. 2010;40(5):1418-27.
18. Lam VC, Lanier LL. NK cells in host responses to viral infections. Curr Opin Immunol. 2017;44(5):43-51.
19. Heatley SL, Pietra G, Lin J, Widjaja JM, Harpur CM, Lester S, et al. Polymorphism in human cytomegalovirus UL40 impacts on recognition of human leukocyte antigen-E (HLA-E) by natural killer cells. J Biol Chem. 2013;288(12):8679-90.
20. Béziat V, Hervier B, Achour A, Boutolleau D, Marfain-Koka A, Vieillard V. Human NKG2A overrides NKG2C effector functions to prevent autoreactivity of NK cells. Blood. 2011;117(16):4394-6.
21. Hammer Q, Rückert T, Borst EM, Dunst J, Haubner A, Durek P, et al. Peptide-specific recognition of human cytomegalovirus strains controls adaptive natural killer cells. Nat Immunol. 2018;19(5):453-63.
22. Liu LL, Landskron J, Ask EH, Enqvist M, Sohlberg E, Traherne JA, et al. Critical role of CD2 co-stimulation in adaptive natural killer cell responses revealed in NKG2C-deficient humans. Cell Rep. 2016;15(5):1088-99.
23. Béziat V, Liu LL, Malmberg J-A, Ivarsson MA, Sohlberg E, Björklund AT, et al. NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs. Blood. 2013;121(14):2678-88.
24. Adib‐Conquy M, Scott‐Algara D, Cavaillon JM, Souza‐Fonseca‐Guimaraes F. TLR‐mediated activation of NK cells and their role in bacterial/viral immune responses in mammals. Immunol. Cell Biol. 2014;92(3):256-62.
25. Kurt-Jones EA, Chan M, Zhou S, Wang J, Reed G, Bronson R, et al. Herpes simplex virus 1 interaction with Toll-like receptor 2 contributes to lethal encephalitis. PNAS. 2004;101(5):1315-20.
26. Wujcicka W, Wilczyński J, Nowakowska D. Alterations in TLRs as new molecular markers of congenital infections with Human cytomegalovirus? Pathog. Dis. 2014;70(1):3-16.
27. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. 2010;11(5):373-8.
28. Newman KC, Riley EM. Whatever turns you on: accessory-cell-dependent activation of NK cells by pathogens. Nat. Rev. Immunol. 2007;7(4):279-91.
29. Hanna J, Gonen-Gross T, Fitchett J, Rowe T, Daniels M, Arnon TI, et al. Novel APC-like properties of human NK cells directly regulate T cell activation. J Clin Invest. 2004;114(11):1612-23.
30. Schlums H, Cichocki F, Tesi B, Theorell J, Beziat V, Holmes TD, et al. Cytomegalovirus infection drives adaptive epigenetic diversification of NK cells with altered signaling and effector function. Immunity. 2015;42(3):443-56.
31. Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature. 2009;457(7229):557-61.
32. Gumá M, Budt M, Sáez A, Brckalo T, Hengel H, Angulo A, et al. Expansion of CD94/NKG2C+ NK cells in response to human cytomegalovirus-infected fibroblasts. Blood. 2006;107(9):3624-31.
33. Muntasell A, Vilches C, Angulo A, López‐Botet M. Adaptive reconfiguration of the human NK‐cell compartment in response to cytomegalovirus: a different perspective of the host‐pathogen interaction. Eur J Immunol. 2013;43(5):1133-41.
34. Guma M, Angulo A, Lopez-Botet M. NK cell receptors involved in the response to human cytomegalovirus infection. Curr Top Microbiol Immunol. 2006;298:207-23.
35. Braud VM, Allan DS, O'callaghan CA, Söderström K, D'andrea A, Ogg GS, et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature. 1998;391(6669):795-9.
36. Kovalenko EI, Streltsova MA, Kanevskiy LM, Erokhina SA, Telford WG. Identification of Human Memory-Like NK Cells. Curr Protoc Cytom. 2017;9:50.1-9.
37. Björkström NK, Riese P, Heuts F, Andersson S, Fauriat C, Ivarsson MA, et al. Expression patterns of NKG2A, KIR, and CD57 define a process of CD56 dim NK-cell differentiation uncoupled from NK-cell education. Blood. 2010;116(19):3853-64.
38. Foley B, Cooley S, Verneris MR, Pitt M, Curtsinger J, Luo X, et al. Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood. 2012;119(11):2665-74.
39. Hammer Q, Rückert T, Romagnani C. Natural killer cell specificity for viral infections. Nat Immunol. 2018;19(8):800-8.
40. Rölle A, Mousavi-Jazi M, Eriksson M, Odeberg J, Söderberg-Nauclér C, Cosman D, et al. Effects of human cytomegalovirus infection on ligands for the activating NKG2D receptor of NK cells: up-regulation of UL16-binding protein (ULBP) 1 and ULBP2 is counteracted by the viral UL16 protein. J Immunol. 2003;171(2):902-8.
41. Prod’homme V, Tomasec P, Cunningham C, Lemberg MK, Stanton RJ, McSharry BP, et al. Human cytomegalovirus UL40 signal peptide regulates cell surface expression of the NK cell ligands HLA-E and gpUL18. J Immunol. 2012;188(6):2794-804.
42. Streltsova MA, Erokhina SA, Kanevskiy LM, Lee DA, Telford WG, Sapozhnikov AM, et al. Analysis of NK cell clones obtained using interleukin-2 and gene-modified K562 cells revealed the ability of “senescent” NK cells to lose CD57 expression and start expressing NKG2A. PLoS One. 2018;13(12):e0208469.
43. Kobyzeva PA, Streltsova MA, Erokhina SA, Kanevskiy LM, Telford WG, Sapozhnikov AM, et al. CD56dimCD57− NKG2C+ NK cells retaining proliferative potential are possible precursors of CD57+ NKG2C+ memory‐like NK cells. J Leukoc Biol. 2020;108(4):1379-95.
44. Björkström NK, Riese P, Heuts F, Andersson S, Fauriat C, Ivarsson MA, et al. Expression patterns of NKG2A, KIR, and CD57 define a process of CD56dim NK-cell differentiation uncoupled from NK-cell education. Blood. 2010;116(19):3853-64.
45. Moretta A, Marcenaro E, Parolini S, Ferlazzo G, Moretta L. NK cells at the interface between innate and adaptive immunity. Cell Death Differ. 2008;15(2):226-33.
46. Kim M, Osborne NR, Zeng W, Donaghy H, McKinnon K, Jackson DC, et al. Herpes simplex virus antigens directly activate NK cells via TLR2, thus facilitating their presentation to CD4 T lymphocytes. J Immunol. 2012;188(9):4158-70.
47. Staege M, Dick T, Ertl R, Jahnel U, Nawrath H, Rammensee H, et al. The antigen self-presentation function of the cytotoxic T-cell clone 10BK. 1 depends on reciprocal peptide presentation. Immunology. 1994;81(3):333-9.
48. Newhook N, Fudge N, Grant M. NK cells generate memory‐type responses to human cytomegalovirus‐infected fibroblasts. Eur J Immunol. 2017;47(6):1032-9.
49. Della Chiesa M, De Maria A, Muccio L, Bozzano F, Sivori S, Moretta L. Human NK cells and Herpesviruses: mechanisms of recognition, response and adaptation. Front Microbiol. 2019;10(4):2297-9.
50. Bortolotti D, Gentili V, Caselli E, Sicolo M, Soffritti I, D’Accolti M, et al. DNA Sensors’ Signaling in NK Cells During HHV-6A, HHV-6B and HHV-7 Infection. Front Microbiol. 2020;11(4):226-31.
51. Mao H, Tu W, Qin G, Law HKW, Sia SF, Chan P-L, et al. Influenza virus directly infects human natural killer cells and induces cell apoptosis. J Virol. 2009;83(18):9215-22.
52. Chiesa S, Mingueneau M, Fuseri N, Malissen B, Raulet DH, Malissen M, et al. Multiplicity and plasticity of natural killer cell signaling pathways. Blood. 2006;107(6):2364-72.
53. Hammer Q, Romagnani C. About training and memory: NK-cell adaptation to viral infections. Adv Immunol. 2017;133(5):171-207.
| Files | ||
| Issue | Vol 20 No 6 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v20i6.8023 | |
| Keywords | ||
| Cytomegalovirus Natural killer cells NK cell lectin-like receptor subfamily | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Soleimanian S, Yaghobi R, Karimi MH, Geramizadeh B, Roozbeh J. The Direct Influence of Cytomegalovirus Lysate on the Natural Killer Cell Receptor Repertoire. Iran J Allergy Asthma Immunol. 2021;20(6):721-733.
