LECTIN-DEPENDENT DIVERSITY OF NATURAL KILLER POPULATIONS AND COMMUNICATIONS AGAINST TUMORS AND VIRUSES
https://doi.org/10.15789/1563-0625-2019-4-595-602
Abstract
Response of human natural killer (NK) cell populations (NKP) against tumors in the presence of viruses was evaluated as a quite variable, early adapting for the pathological signals in organism, mobile and selective combination agents. NKP act as a result of co-functioning between the receptor lectins (RL) recognizing glycopatterns (RL as triggers, initiators and basic agents for coupled activities), and Ig-like, cytotoxic and other additional communicative and effector receptors (superstructural, tuning for achievement of final effector-type NKP constructions required), and their ligands (modulators of final cell surface receptor mosaics). Such NKP created play important role in redistribution of NKP-induced antitumor/ antiviral cytokines in organism. Intercellular communicative potential of NKP also involves other innate and innate-like cells. Such extended communications of NKP provide a prospective and universal resource of human protection. NKP must be under consideration upon development of new maneuvre and relilable prophylactic and immunotherapeutic antitumor/ antiviral systems and vaccine strategies. The ways for the fine tuning (RL—KIR/ NCR/ CD/ their combinations) algorithms of RL-based creation of antitumor/ antiviral NKP are revealed. Key role is given to screening spectrum of patient NKP for development of communicative anticancer/ antiviral strategies. The status of NK compartment will characterize resistance of individuum/ contingent of individuums to viral infections of epidemiological significance, will play important role in anti-epidemic protection of regional population.
About the Authors
M. V. LakhtinRussian Federation
PhD (Medicine), Senior Research Associate
125212, Russian Federation, Moscow, Adm. Makarov str., 10
+7 (495) 452-18-16
V. M. Lakhtin
Russian Federation
PhD, MD (Medicine), Chief Research Associate, G.N. Gabrichevsky Research Institute for Epidemiology and Microbiology,
Moscow
V. A. Aleshkin
Russian Federation
PhD, MD Professor (Medicine), Research Director
Moscow
S. S. Afanasiev
Russian Federation
PhD, MD (Medicine), Chief Research Associate – Doctor of Medical Sciences, Professor, Chief Research Officer
Moscow
References
1. Djaoud Z., Guethlein L.A., Horowitz A., Azzi T., Nemat-Gorgani N., Olive D., Nadal D., Norman P.J., Münz C., Parham P. Two alternate strategies for innate immunity to Epstein–Barr virus: One using NK cells and the other NK cells and gamma-delta T cells. J. Exp. Med., 2017, Vol. 214, no. 6, pp. 1827-1841.
2. Lakhtin M.V., Lakhtin V.M., Alyoshkin V.A., Afanasiev M.S., Afanasiev S.S. Lectins in anticancer strategies. Acta Biomedica Scientifica, 2018, Vol. 3, no. 4, pp. 69-77. (In Russ.)
3. Djaoud Z., Riou R., Gavlovsky P.J., Mehlal S., Bressollette C., Gérard N., Gagne K., Charreau B., Retière C. Cytomegalovirus-infected primary endothelial cells trigger NKG2C+ natural killer cells. J. Innate Immun., 2016, Vol. 8, no. 4, pp. 374-385.
4. Lakhtin M.V., Lakhtin V.M., Alyoshkin V.A., Afanasiev S.S. Lectin receptors in communications. News of Science and Education, 2018, Vol. 2, no. 3, pp. 76-98. (In Russ.)
5. Dukovska D., Fernández-Soto D., Valés-Gómez M., Reyburn H.T. NKG2H-expressing T cells negatively regulate immune responses. Front. Immunol., 2018, Vol. 9, p. 390.
6. Lakhtin M.V., Lakhtin V.M., Afanasiev S.S., Bayrakova A.L., Aleshkin V.A., Afanasiev M.S. Candida markers of diseases of urogenital biotopes: Reactivity to lectins of probiotics. Acta Biomedica Scientifica, 2018, Vol. 3, no. 1, pp. 49-53. (In Russ.)
7. Espinoza J.L., Minami M. Sensing bacterial-induced DNA damaging effects via natural killer group 2 member D immune receptor: From dysbiosis to autoimmunity and carcinogenesis. Front. Immunol., 2018, Vol. 9, p. 52.
8. Bigley A.B., Rezvani K., Shah N., Sekine T., Balneger N., Pistillo M., Agha N., Kunz H., O’Connor D.P., Bollard C.M., Simpson R.J. Latent cytomegalovirus infection enhances anti-tumour cytotoxicity through accumulation of NKG2C+ NK cells in healthy humans. Clin. Exp. Immunol., 2016, Vol. 185, no. 2, pp. 239-251.
9. Espinoza J.L., Nguyen V.H., Ichimura H., Pham T.T., Nguyen C.H., Pham T.V., Elbadry M.I., Yoshioka K., Tanaka J., Trung L.Q.,Takami A., Nakao S. A functional polymorphism in the NKG2D gene modulates NK-cell cytotoxicity and is associated with susceptibility to Human Papilloma Virus-related cancers. Sci. Rep., 2016, Vol. 6, 39231. doi: 10.1038/srep39231.
10. do Carmo F.L.R., Rabah H., de Oliveira Carvalho R.D., Gaucher F., Cordeiro B.F., da Silva S.H., le Loir Y., Azevedo V., Jan G. Extractable bacterial surface proteins in probiotic-host interaction. Front. Microbiol., 2018, Vol. 9, p. 645.
11. Fehniger T.A., Cooper M.A. Harnessing NK cell memory for cancer immunotherapy. Trends Immunol., 2016, Vol. 37, no. 12, pp. 877-888.
12. Chijioke O., Landtwing V., Münz C. NK cell influence on the outcome of primary Epstein–Barr virus infection. Front. Immunol., 2016, Vol. 7, p. 323.
13. Georgountzou A., Papadopoulos N.G. Postnatal innate immune development: From birth to adulthood. Front. Immunol., 2017, Vol. 8, 957. doi: 10.3389/fimmu.2017.00957.
14. Crane C.A., Austgen K., Haberthur K., Hofmann C., Moyes K.W., Avanesyan L., Fong L., Campbell M.J., Cooper S., Oakes S.A., Parsa A.T., Lanier L.L. Immune evasion mediated by tumor-derived lactate dehydrogenase induction of NKG2D ligands on myeloid cells in glioblastoma patients. Proc. Natl. Acad. Sci. USA, 2014, Vol. 111, no. 35, pp. 12823-12828.
15. Grandi N., Cadeddu M., Pisano M.P., Esposito F., Blomberg J., Tramontano E. Identification of a novel HERV-K(HML10): Comprehensive characterization and comparative analysis in non-human primates provide insights about HML10 proviruses structure and diffusion. Mob. DNA, 2017, Vol. 8, p. 15.
16. Djaoud Z., Guethlein L.A., Horowitz A., Azzi T., Nemat-Gorgani N., Olive D., Nadal D., Norman P.J., Münz C., Parham P. Two alternate strategies for innate immunity to Epstein–Barr virus: One using NK cells and the other NK cells and gamma-delta T cells. J. Exp. Med., 2017, Vol. 214, no. 6, pp. 1827-1841.
17. Hatfield S.D., Daniels K.A., O’Donnell C.L., Waggoner S.N., Welsh R.M. Weak vaccinia virus-induced NK cell regulation of CD4 T cells is associated with reduced NK cell differentiation and cytolytic activity. Virology, 2018, Vol. 519, pp. 131-144.
18. Djaoud Z., Riou R., Gavlovsky P.J., Mehlal S., Bressollette C., Gérard N., Gagne K., Charreau B., Retière C. Cytomegalovirus-infected primary endothelial cells trigger NKG2C+ natural killer cells. J. Innate Immun., 2016, Vol. 8, no. 4, pp. 374-385.
19. Heiberg I.L., Pallett L.J., Winther T.N., Høgh B., Maini M.K., Peppa D. Defective natural killer cell anti-viral capacity in paediatric HBV infection. Clin. Exp. Immunol., 2015, Vol. 179, no. 3, pp. 466-476.
20. Dukovska D., Fernández-Soto D., Valés-Gómez M., Reyburn H.T. NKG2H-expressing T cells negatively regulate immune responses. Front. Immunol., 2018, Vol. 9, p. 390.
21. Janelle V., Langlois M.P., Tarrab E., Lapierre P., Poliquin L., Lamarre A. Transient complement inhibition promotes a tumor-specific immune response through the implication of natural killer cells. Cancer Immunol. Res., 2014, Vol. 2, no. 3, pp. 200-206.
22. Espinoza J.L., Minami M. Sensing bacterial-induced DNA damaging effects via natural killer group 2 member D immune receptor: From dysbiosis to autoimmunity and carcinogenesis. Front. Immunol., 2018, Vol. 9, p. 52.
23. Jud A., Kotur M., Berger C., Gysin C., Nadal D., Lünemann A. Tonsillar CD56brightNKG2A+ NK cells restrict primary Epstein–Barr virus infection in B cells via IFN-gamma. Oncotarget, 2017, Vol. 8, no. 4, pp. 6130-6141.
24. Espinoza J.L., Nguyen V.H., Ichimura H., Pham T.T., Nguyen C.H., Pham T.V., Elbadry M.I., Yoshioka K., Tanaka J., Trung L.Q.,Takami A., Nakao S. A functional polymorphism in the NKG2D gene modulates NK-cell cytotoxicity and is associated with susceptibility to Human Papilloma Virus-related cancers. Sci. Rep., 2016, Vol. 6, 39231. doi: 10.1038/srep39231.
25. Keydar Y., le Saux G., Pandey A., Avishay E., Bar-Hanin N., Esti T., Bhingardive V., Hadad U., Porgador A., Schvartzman M. Natural killer cells’ immune response requires a minimal nanoscale distribution of activating antigens. Nanoscale, 2018, Vol. 10, no. 30, pp. 14651-14659.
26. Fehniger T.A., Cooper M.A. Harnessing NK cell memory for cancer immunotherapy. Trends Immunol., 2016, Vol. 37, no. 12, pp. 877-888.
27. Koltan S., Debski R., Koltan A., Grzesk E., Tejza B., Eljaszewicz A., Gackowska L., Kubicka M., Kolodziej B., Kurylo-Rafinska B., Kubiszewska I., Wiese M., Januszewska M., Michalkiewicz J., Wysocki M., Styczynski J., Grzesk G. Phenotype of NK cells determined on the basis of selected immunological parameters in children treated due to acute lymphoblastic leukemia. Medicine (Baltimore), 2015, Vol. 94, no. 52, e2369. doi: 10.1097/MD.0000000000002369.
28. Georgountzou A., Papadopoulos N.G. Postnatal innate immune development: From birth to adulthood. Front. Immunol., 2017, Vol. 8, 957. doi: 10.3389/fimmu.2017.00957.
29. Kurioka A., Cosgrove C., Simoni Y., van Wilgenburg B., Geremia A., Björkander S., Sverremark-Ekström E., Thurnheer C., Günthard H.F., Khanna N., Walker L.J., Arancibia-Cárcamo C.V., Newell E.W., Willberg C.B., Klenerman P. CD161 defines a functionally distinct subset of pro-inflammatory natural killer cells. Front. Immunol., 2018, Vol. 9, 486. doi: 10.3389/fimmu.2018.00486.
30. Grandi N., Cadeddu M., Pisano M.P., Esposito F., Blomberg J., Tramontano E. Identification of a novel HERV-K(HML10): Comprehensive characterization and comparative analysis in non-human primates provide insights about HML10 proviruses structure and diffusion. Mob. DNA, 2017, Vol. 8, p. 15.
31. Kurioka A., Klenerman P., Willberg C.B. Innate-like CD8+ T-cells and NK cells: converging functions and phenotypes. Immunology, 2018. doi: 10.1111/imm.12925.
32. Hatfield S.D., Daniels K.A., O’Donnell C.L., Waggoner S.N., Welsh R.M. Weak vaccinia virus-induced NK cell regulation of CD4 T cells is associated with reduced NK cell differentiation and cytolytic activity. Virology, 2018, Vol. 519, pp. 131-144.
33. Mahapatra S., Mace E.M., Minard C.G., Forbes L.R., Vargas-Hernandez A., Duryea T.K., Makedonas G., Banerjee P.P., Shearer W.T., Orange J.S. High-resolution phenotyping identifies NK cell subsets that distinguish healthy children from adults. PLoS ONE, 2017, Vol. 12, no. 8, e0181134. doi: 10.1371/journal.pone.0181134.
34. Heiberg I.L., Pallett L.J., Winther T.N., Høgh B., Maini M.K., Peppa D. Defective natural killer cell anti-viral capacity in paediatric HBV infection. Clin. Exp. Immunol., 2015, Vol. 179, no. 3, pp. 466-476.
35. Mahaweni N.M., Ehlers F.A.I., Sarkar S., Janssen J.W.H., Tilanus M.G.J., Bos G.M.J., Wieten L. NKG2A expression is not per se detrimental for the anti-multiple myeloma activity of activated natural killer cells in an in vitro system mimicking the tumor microenvironment. Front. Immunol., 2018, Vol. 9, 1415. doi: 10.3389/fimmu.2018.01415.
36. Janelle V., Langlois M.P., Tarrab E., Lapierre P., Poliquin L., Lamarre A. Transient complement inhibition promotes a tumor-specific immune response through the implication of natural killer cells. Cancer Immunol. Res., 2014, Vol. 2, no. 3, pp. 200-206.
37. Malone D.F.G., Lunemann S., Hengst J., Ljunggren H.G., Manns M.P., Sandberg J.K., Cornberg M., Wedemeyer H., Björkström N.K. Cytomegalovirus-driven adaptive-like natural killer cell expansions are unaffected by concurrent chronic hepatitis virus infections. Front. Immunol., 2017, Vol. 8, 525. doi: 10.3389/fimmu.2017.00525.
38. Jud A., Kotur M., Berger C., Gysin C., Nadal D., Lünemann A. Tonsillar CD56brightNKG2A+ NK cells restrict primary Epstein–Barr virus infection in B cells via IFN-gamma. Oncotarget, 2017, Vol. 8, no. 4, pp. 6130-6141.
39. Marrufo A.M., Mathew S.O., Chaudhary P., Malaer J.D., Vishwanatha J.K., Mathew P.A. Blocking LLT1 (CLEC2D, OCIL)-NKRP1A (CD161) interaction enhances natural killer cell-mediated lysis of triple-negative breast cancer cells. Am. J. Cancer Res., 2018, Vol. 8, no. 6, pp. 1050-1063.
40. Keydar Y., le Saux G., Pandey A., Avishay E., Bar-Hanin N., Esti T., Bhingardive V., Hadad U., Porgador A., Schvartzman M. Natural killer cells’ immune response requires a minimal nanoscale distribution of activating antigens. Nanoscale, 2018, Vol. 10, no. 30, pp. 14651-14659.
41. Martinez D.R., Permar S.R., Fouda G.G. Contrasting adult and infant immune responses to HIV infection and vaccination. Clin. Vaccine Immunol., 2015, Vol. 23, no. 2, pp. 84-94.
42. Koltan S., Debski R., Koltan A., Grzesk E., Tejza B., Eljaszewicz A., Gackowska L., Kubicka M., Kolodziej B., Kurylo-Rafinska B., Kubiszewska I., Wiese M., Januszewska M., Michalkiewicz J., Wysocki M., Styczynski J., Grzesk G. Phenotype of NK cells determined on the basis of selected immunological parameters in children treated due to acute lymphoblastic leukemia. Medicine (Baltimore), 2015, Vol. 94, no. 52, e2369. doi: 10.1097/MD.0000000000002369.
43. Mavers M., Bertaina A. High-risk leukemia: Past, present, and future role of NK cells. J. Immunol. Res., 2018. Vol. 2018, 1586905. doi: 10.1155/2018/1586905.
44. Kurioka A., Cosgrove C., Simoni Y., van Wilgenburg B., Geremia A., Björkander S., Sverremark-Ekström E., Thurnheer C., Günthard H.F., Khanna N., Walker L.J., Arancibia-Cárcamo C.V., Newell E.W., Willberg C.B., Klenerman P. CD161 defines a functionally distinct subset of pro-inflammatory natural killer cells. Front. Immunol., 2018, Vol. 9, 486. doi: 10.3389/fimmu.2018.00486.
45. 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, Vol. 43, no. 5, pp. 1133-1141.
46. Kurioka A., Klenerman P., Willberg C.B. Innate-like CD8+ T-cells and NK cells: converging functions and phenotypes. Immunology, 2018. doi: 10.1111/imm.12925.
47. Münz C. Epstein–Barr virus-specific immune control by innate lymphocytes. Front. Immunol., 2017, Vol. 8, 1658. doi: 10.3389/fimmu.2017.01658.
48. Mahapatra S., Mace E.M., Minard C.G., Forbes L.R., Vargas-Hernandez A., Duryea T.K., Makedonas G., Banerjee P.P., Shearer W.T., Orange J.S. High-resolution phenotyping identifies NK cell subsets that distinguish healthy children from adults. PLoS ONE, 2017, Vol. 12, no. 8, e0181134. doi: 10.1371/journal.pone.0181134.
49. Muta T., Yoshihiro T., Jinnouchi F., Aoki K., Kochi Y., Shima T., Takenaka K., Ogawa R., Akashi K., Oshima K. Expansion of NKG2C-expressing natural killer cells after umbilical cord blood transplantation in a patient with peripheral T-cell lymphoma with cytotoxic molecules. Intern. Med., 2018, Vol. 57, no. 6, pp. 861-866.
50. Mahaweni N.M., Ehlers F.A.I., Sarkar S., Janssen J.W.H., Tilanus M.G.J., Bos G.M.J., Wieten L. NKG2A expression is not per se detrimental for the anti-multiple myeloma activity of activated natural killer cells in an in vitro system mimicking the tumor microenvironment. Front. Immunol., 2018, Vol. 9, 1415. doi: 10.3389/fimmu.2018.01415.
51. Peled J.U., Jenq R.R. Not just leukemia: CMV may protect against lymphoma recurrence after allogeneic transplant. Leuk. Lymphoma, 2017, Vol. 58, no. 4, pp. 759-761.
52. Malone D.F.G., Lunemann S., Hengst J., Ljunggren H.G., Manns M.P., Sandberg J.K., Cornberg M., Wedemeyer H., Björkström N.K. Cytomegalovirus-driven adaptive-like natural killer cell expansions are unaffected by concurrent chronic hepatitis virus infections. Front. Immunol., 2017, Vol. 8, 525. doi: 10.3389/fimmu.2017.00525.
53. Peppa D. Natural killer cells in human immunodeficiency virus-1 infection: Spotlight on the impact of human cytomegalovirus. Front. Immunol., 2017, Vol. 8, 1322. doi: 10.3389/fimmu.2017.01322.
54. Marrufo A.M., Mathew S.O., Chaudhary P., Malaer J.D., Vishwanatha J.K., Mathew P.A. Blocking LLT1 (CLEC2D, OCIL)-NKRP1A (CD161) interaction enhances natural killer cell-mediated lysis of triple-negative breast cancer cells. Am. J. Cancer Res., 2018, Vol. 8, no. 6, pp. 1050-1063.
55. Phan M.T., Chun S., Kim S.H., Ali A.K., Lee S.H., Kim S., Kim S.H., Cho D. Natural killer cell subsets and receptor expression in peripheral blood mononuclear cells of a healthy Korean population: Reference range, influence of age and sex, and correlation between NK cell receptors and cytotoxicity. Hum. Immunol., 2017, Vol. 78, no. 2, pp. 103-112.
56. Martinez D.R., Permar S.R., Fouda G.G. Contrasting adult and infant immune responses to HIV infection and vaccination. Clin. Vaccine Immunol., 2015, Vol. 23, no. 2, pp. 84-94.
57. Prado Acosta M., Ruzal S.M., Cordo S.M. S-layer proteins from Lactobacillus sp. inhibit bacterial infection by blockage of DC-SIGN cell receptor. Int. J. Biol. Macromol., 2016, Vol. 92, pp. 998-1005.
58. Mavers M., Bertaina A. High-risk leukemia: Past, present, and future role of NK cells. J. Immunol. Res., 2018. Vol. 2018, 1586905. doi: 10.1155/2018/1586905.
59. Przemska-Kosicka A., Childs C.E., Maidens C., Dong H., Todd S., Gosney M.A., Tuohy K.M., Yaqoob P. Age-related changes in the natural killer cell response to seasonal influenza vaccination are not influenced by a synbiotic: A randomised controlled trial. Front. Immunol., 2018. Vol. 9, 591. doi: 10.3389/fimmu.2018.00591.
60. 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, Vol. 43, no. 5, pp. 1133-1141.
61. Pupuleku A., Costa-García M., Farré D., Hengel H., Angulo A., Muntasell A., López-Botet M. Elusive role of the CD94/NKG2C NK cell receptor in the response to cytomegalovirus: Novel experimental observations in a reporter cell system. Front. Immunol., 2017, Vol. 8, 1317. doi: 10.3389/fimmu.2017.01317.
62. Münz C. Epstein–Barr virus-specific immune control by innate lymphocytes. Front. Immunol., 2017, Vol. 8, 1658. doi: 10.3389/fimmu.2017.01658.
63. Ramsuran V., Naranbhai V., Horowitz A., Qi Y., Martin M.P., Yuki Y., Gao X., Walker-Sperling V., del Prete G.Q., Schneider D.K., Lifson J.D., Fellay J., Deeks S.G., Martin J.N., Goedert J.J., Wolinsky S.M., Michael N.L., Kirk G.D., Buchbinder S., Haas D., Ndung’u T., Goulder P., Parham P., Walker B.D., Carlson J.M., Carrington M. Elevated HLA-A expression impairs HIV control through inhibition of NKG2A-expressing cells. Science, 2018, Vol. 359, no. 6371, pp. 86-90.
64. Muta T., Yoshihiro T., Jinnouchi F., Aoki K., Kochi Y., Shima T., Takenaka K., Ogawa R., Akashi K., Oshima K. Expansion of NKG2C-expressing natural killer cells after umbilical cord blood transplantation in a patient with peripheral T-cell lymphoma with cytotoxic molecules. Intern. Med., 2018, Vol. 57, no. 6, pp. 861-866.
65. Ruggeri L., Urbani E., André P., Mancusi A., Tosti A., Topini F., Bléry M., Animobono L., Romagné F., Wagtmann N., Velardi A. Effects of anti-NKG2A antibody administration on leukemia and normal hematopoietic cells. Haematologica, 2016, Vol. 101, no. 5, pp. 626-633.
66. Peled J.U., Jenq R.R. Not just leukemia: CMV may protect against lymphoma recurrence after allogeneic transplant. Leuk. Lymphoma, 2017, Vol. 58, no. 4, pp. 759-761.
67. Stojanovic A., Correia M.P., Cerwenka A. The NKG2D/NKG2DL axis in the crosstalk between lymphoid and myeloid cells in health and disease. Front. Immunol., 2018, Vol. 9, 827. doi: 10.3389/fimmu.2018.00827.
68. Peppa D. Natural killer cells in human immunodeficiency virus-1 infection: Spotlight on the impact of human cytomegalovirus. Front. Immunol., 2017, Vol. 8, 1322. doi: 10.3389/fimmu.2017.01322.
69. Sundström Y., Nilsson C., Lilja G., Kärre K., Troye-Blomberg M., Berg L. The expression of human natural killer cell receptors in early life. Scand. J. Immunol., 2007, Vol. 66, no. 2-3, pp. 335-344.
70. Phan M.T., Chun S., Kim S.H., Ali A.K., Lee S.H., Kim S., Kim S.H., Cho D. Natural killer cell subsets and receptor expression in peripheral blood mononuclear cells of a healthy Korean population: Reference range, influence of age and sex, and correlation between NK cell receptors and cytotoxicity. Hum. Immunol., 2017, Vol. 78, no. 2, pp. 103-112.
71. Thompson T.W., Jackson B.T., Li P.J., Wang J., Kim A.B., Huang K.T.H., Zhang L., Raulet D.H. Tumorderived CSF-1 induces the NKG2D ligand RAE-1-delta on tumor-infiltrating macrophages. Elife, 2018, Vol. 7, pii: e32919. doi: 10.7554/eLife.32919.
72. Prado Acosta M., Ruzal S.M., Cordo S.M. S-layer proteins from Lactobacillus sp. inhibit bacterial infection by blockage of DC-SIGN cell receptor. Int. J. Biol. Macromol., 2016, Vol. 92, pp. 998-1005.
73. Uemura Y., Isobe Y., Uchida A., Asano J., Nishio Y., Sakai H., Hoshikawa M., Takagi M., Nakamura N., Miura I. Expression of activating natural killer-cell receptors is a hallmark of the innate-like T-cell neoplasm in peripheral T-cell lymphomas. Cancer Sci., 2018, Vol. 109, no. 4, pp. 1254-1262.
74. Przemska-Kosicka A., Childs C.E., Maidens C., Dong H., Todd S., Gosney M.A., Tuohy K.M., Yaqoob P. Age-related changes in the natural killer cell response to seasonal influenza vaccination are not influenced by a synbiotic: A randomised controlled trial. Front. Immunol., 2018. Vol. 9, 591. doi: 10.3389/fimmu.2018.00591.
75. Uppendahl L.D., Dahl C.M., Miller J.S., Felices M., Geller M.A. Natural killer cell-based immunotherapy in gynecologic malignancy: A review. Front. Immunol., 2018, Vol. 8, 1825. doi: 10.3389/fimmu.2017.01825.
76. Pupuleku A., Costa-García M., Farré D., Hengel H., Angulo A., Muntasell A., López-Botet M. Elusive role of the CD94/NKG2C NK cell receptor in the response to cytomegalovirus: Novel experimental observations in a reporter cell system. Front. Immunol., 2017, Vol. 8, 1317. doi: 10.3389/fimmu.2017.01317.
77. Walter L., Petersen B. Diversification of both KIR and NKG2 natural killer cell receptor genes in macaques – implications for highly complex MHC-dependent regulation of natural killer cells. Immunology, 2017, Vol. 150, no. 2, pp. 139-145.
78. Ramsuran V., Naranbhai V., Horowitz A., Qi Y., Martin M.P., Yuki Y., Gao X., Walker-Sperling V., del Prete G.Q., Schneider D.K., Lifson J.D., Fellay J., Deeks S.G., Martin J.N., Goedert J.J., Wolinsky S.M., Michael N.L., Kirk G.D., Buchbinder S., Haas D., Ndung’u T., Goulder P., Parham P., Walker B.D., Carlson J.M., Carrington M. Elevated HLA-A expression impairs HIV control through inhibition of NKG2A-expressing cells. Science, 2018, Vol. 359, no. 6371, pp. 86-90.
79. Wang Z., Guo L., Song Y., Zhang Y., Lin D., Hu B., Mei Y., Sandikin D., Liu H. Augmented anti-tumor activity of NK-92 cells expressing chimeric receptors of TGF-beta-R II and NKG2D. Cancer Immunol. Immunother., 2017, Vol. 66, no. 4, pp. 537-548.
80. Ruggeri L., Urbani E., André P., Mancusi A., Tosti A., Topini F., Bléry M., Animobono L., Romagné F., Wagtmann N., Velardi A. Effects of anti-NKG2A antibody administration on leukemia and normal hematopoietic cells. Haematologica, 2016, Vol. 101, no. 5, pp. 626-633.
81. Wensveen F.M., Jelenčić V., Polić B. NKG2D: A master regulator of immune cell responsiveness. Front. Immunol., 2018, Vol. 9, 441. doi: 10.3389/fimmu.2018.00441.
82. Stojanovic A., Correia M.P., Cerwenka A. The NKG2D/NKG2DL axis in the crosstalk between lymphoid and myeloid cells in health and disease. Front. Immunol., 2018, Vol. 9, 827. doi: 10.3389/fimmu.2018.00827.
83. Zingoni A., Molfetta R., Fionda C., Soriani A., Paolini R., Cippitelli M., Cerboni C, Santoni A. NKG2D and its ligands: “One for all, all for one”. Front. Immunol., 2018, Vol. 9, 476. doi: 10.3389/fimmu.2018.00476.
84. Sundström Y., Nilsson C., Lilja G., Kärre K., Troye-Blomberg M., Berg L. The expression of human natural killer cell receptors in early life. Scand. J. Immunol., 2007, Vol. 66, no. 2-3, pp. 335-344.
85. Thompson T.W., Jackson B.T., Li P.J., Wang J., Kim A.B., Huang K.T.H., Zhang L., Raulet D.H. Tumorderived CSF-1 induces the NKG2D ligand RAE-1-delta on tumor-infiltrating macrophages. Elife, 2018, Vol. 7, pii: e32919. doi: 10.7554/eLife.32919.
86. Uemura Y., Isobe Y., Uchida A., Asano J., Nishio Y., Sakai H., Hoshikawa M., Takagi M., Nakamura N., Miura I. Expression of activating natural killer-cell receptors is a hallmark of the innate-like T-cell neoplasm in peripheral T-cell lymphomas. Cancer Sci., 2018, Vol. 109, no. 4, pp. 1254-1262.
87. Uppendahl L.D., Dahl C.M., Miller J.S., Felices M., Geller M.A. Natural killer cell-based immunotherapy in gynecologic malignancy: A review. Front. Immunol., 2018, Vol. 8, 1825. doi: 10.3389/fimmu.2017.01825.
88. Walter L., Petersen B. Diversification of both KIR and NKG2 natural killer cell receptor genes in macaques – implications for highly complex MHC-dependent regulation of natural killer cells. Immunology, 2017, Vol. 150, no. 2, pp. 139-145.
89. Wang Z., Guo L., Song Y., Zhang Y., Lin D., Hu B., Mei Y., Sandikin D., Liu H. Augmented anti-tumor activity of NK-92 cells expressing chimeric receptors of TGF-beta-R II and NKG2D. Cancer Immunol. Immunother., 2017, Vol. 66, no. 4, pp. 537-548.
90. Wensveen F.M., Jelenčić V., Polić B. NKG2D: A master regulator of immune cell responsiveness. Front. Immunol., 2018, Vol. 9, 441. doi: 10.3389/fimmu.2018.00441.
91. Zingoni A., Molfetta R., Fionda C., Soriani A., Paolini R., Cippitelli M., Cerboni C, Santoni A. NKG2D and its ligands: “One for all, all for one”. Front. Immunol., 2018, Vol. 9, 476. doi: 10.3389/fimmu.2018.00476.
Review
For citations:
Lakhtin M.V., Lakhtin V.M., Aleshkin V.A., Afanasiev S.S. LECTIN-DEPENDENT DIVERSITY OF NATURAL KILLER POPULATIONS AND COMMUNICATIONS AGAINST TUMORS AND VIRUSES. Medical Immunology (Russia). 2019;21(4):595-602. https://doi.org/10.15789/1563-0625-2019-4-595-602