Natural killer cells are the regulators of T cell immunity_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

LIN Yanyan ¹ , CAO Jie ² , LUO Zhiwen ³ , BAI Bing ¹ , YUE Ping ¹ ,  MENG Wenbo ¹ , LI Xun ⁴

1. Special Minimally Invasive Surgery, The First Hospital of Lanzhou University, Lanzhou 730000, P.R.China;
2. Clinical Laboratory, The First Hospital of Lanzhou University, Lanzhou 730000, P.R.China;
3. The First Clinical College of Lanzhou University, Lanzhou 730000, P.R.China;
4. The Second Department of General Surgery, The First Hospital of Lanzhou University, Lanzhou 730000, P.R.China;

Corresponding author：

MENG Wenbo, Email: mengwb@lzu.edu.cn

Keywords：

natural killer cells; T cells; immune regulation; viral infection

DOI：

10.7507/1007-9424.201609047

Video：

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Objective To summarize research progress of the mechanism of natural killer cells (NK cells) acted in regulating the T cell immunity in chronic infectious disease. Method Literatures about recent studies concerning how NK cells act as a regulator for T cells in chronic infectious disease were reviewed according to the results obtained from PubMed, Embase, CNKI, CBM, and Wanfang databases. Results NK cells that acted as regulators of T cell immunity could affect T cell immune responses through influencing antigen presentation, secreting cytokine, and presenting lytic activities, thus playing an important role in the immunological therapy of chronic infectious diseases. Conclusion NK cells are critical for T cell immune regulation, which could provide noval strategies for immunological therapy of chronic infectious disease, transplantation-related immune rejection, and autoimmune disease.

Citation： LIN Yanyan, CAO Jie, LUO Zhiwen, BAI Bing, YUE Ping, MENG Wenbo, LI Xun. Natural killer cells are the regulators of T cell immunity. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2017, 24(6): 770-774. doi: 10.7507/1007-9424.201609047 Copy

1.	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): 112-117.
2.	Jiao G, Wang B. NK cell subtypes as regulators of autoimmune liver disease. Gastroenterol Res Pract, 2016, 2016: 6903496.
3.	Hong HS, Rajakumar PA, Billingsley JM, et al. No monkey business: why studying NK cells in non-human primates pays off. Front Immunol, 2013, 4: 32.
4.	Vojvodić S, Popović S. Natural killer cells−biology, functions and clinical relevance. Med Pregl, 2010, 63(1-2): 91-97.
5.	Fugier E, Marche H, Thélu MA, et al. Functions of liver natural killer cells are dependent on the severity of liver inflammation and fibrosis in chronic hepatitis C. PLoS One, 2014, 9(4): e95614.
6.	Waggoner SN, Cornberg M, Selin LK, et al. Natural killer cells act as rheostats modulating antiviral T cells. Nature, 2011, 481(7381): 394-398.
7.	Schuster IS, Coudert JD, Andoniou CE, et al. " Natural regulators”: NK cells as modulators of T cell immunity. Front Immunol, 2016, 7: 235.
8.	Crome SQ, Lang PA, Lang KS, et al. Natural killer cells regulate diverse T cell responses. Trends Immunol, 2013, 34(7): 342-349.
9.	Tu MM, Mahmoud AB, Makrigiannis AP. Licensed and unlicensed NK cells: differential roles in cancer and viral control. Front Immunol, 2016, 7: 166.
10.	Lanier LL. Evolutionary struggles between NK cells and viruses. Nat Rev Immunol, 2008, 8(4): 259-268.
11.	Moretta A, Marcenaro E, Sivori S, et al. Early liaisons between cells of the innate immune system in inflamed peripheral tissues. Trends Immunol, 2005, 26(12): 668-675.
12.	Walzer T, Dalod M, Robbins SH, et al. Natural-killer cells and dendritic cells: " l'union fait la force”. Blood, 2005, 106(7): 2252-2258.
13.	Fort MM, Leach MW, Rennick DM. A role for NK cells as regulators of CD4⁺ T cells in a transfer model of colitis. J Immunol, 1998, 161(7): 3256-3261.
14.	Vankayalapati R, Klucar P, Wizel B, et al. NK cells regulate CD8⁺ T cell effector function in response to an intracellular pathogen. J Immunol, 2004, 172(1): 130-137.
15.	Andrews DM, Estcourt MJ, Andoniou CE, et al. Innate immunity defines the capacity of antiviral T cells to limit persistent infection. J Exp Med, 2010, 207(6): 1333-1343.
16.	Narni-Mancinelli E, Jaeger BN, Bernat C, et al. Tuning of natural killer cell reactivity by NKp46 and Helios calibrates T cell responses. Science, 2012, 335(6066): 344-348.
17.	Cook KD, Whitmire JK. The depletion of NK cells prevents T cell exhaustion to efficiently control disseminating virus infection. J Immunol, 2013, 190(2): 641-649.
18.	Su HC, Nguyen KB, Salazar-Mather TP, et al. NK cell functions restrain T cell responses during viral infections. Eur J Immunol, 2001, 31(10): 3048-3055.
19.	Schuster IS, Wikstrom ME, Brizard G, et al. TRAIL⁺ NK cells control CD4⁺ T cell responses during chronic viral infection to limit autoimmunity. Immunity, 2014, 41(4): 646-656.
20.	Waggoner SN, Taniguchi RT, Mathew PA, et al. Absence of mouse 2B4 promotes NK cell-mediated killing of activated CD8⁺ T cells, leading to prolonged viral persistence and altered pathogenesis. J Clin Invest, 2010, 120(6): 1925-1938.
21.	Shin H, Wherry EJ. CD8 T cell dysfunction during chronic viral infection. Curr Opin Immunol, 2007, 19(4): 408-415.
22.	Wherry EJ, Ha SJ, Kaech SM, et al. Molecular signature of CD8⁺ T cell exhaustion during chronic viral infection. Immunity, 2007, 27(4): 670-684.
23.	Lang PA, Lang KS, Xu HC, et al. Natural killer cell activation enhances immune pathology and promotes chronic infection by limiting CD8⁺ T-cell immunity. Proc Natl Acad Sci U S A, 2012, 109(4): 1210-1215.
24.	Pembroke T, Rees I, Gallagher K, et al. Rapid early innate control of hepatitis C virus during IFN-α treatment compromises adaptive CD4⁺ T-cell immunity. Eur J Immunol, 2012, 42(9): 2383-2394.
25.	Schuch A, Hoh A, Thimme R. The role of natural killer cells and CD8(+) T cells in hepatitis B virus infection. Front Immunol, 2014, 5: 258.
26.	Khakoo SI, Thio CL, Martin MP, et al. HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science, 2004, 305(5685): 872-874.
27.	Yoon JC, Yang CM, Song Y, et al. Natural killer cells in hepatitis C: current progress. World J Gastroenterol, 2016, 22(4): 1449-1460.
28.	林延延. PegIFNα 治疗慢乙肝用药指导指标的筛选及 NK 细胞在慢性乙肝病毒感染中作用的初步探索. 厦门: 厦门大学, 2014.
29.	McNerney ME, Lee KM, Zhou P, et al. Role of natural killer cell subsets in cardiac allograft rejection. Am J Transplant, 2006, 6(3): 505-513.
30.	Beilke JN, Kuhl NR, Van Kaer L, et al. NK cells promote islet allograft tolerance via a perforin-dependent mechanism. Nat Med, 2005, 11(10): 1059-1065.
31.	Bose A, Inoue Y, Kokko KE, et al. Cutting edge: perforin down-regulates CD4 and CD8 T cell-mediated immune responses to a transplanted organ. J Immunol, 2003, 170(4): 1611-1614.
32.	Noval Rivas M, Hazzan M, Weatherly K, et al. NK cell regulation of CD4 T cell-mediated graft-versus-host disease. J Immunol, 2010, 184(12): 6790-6798.
33.	Takeda K, Dennert G. The development of autoimmunity in C57BL/6 lpr mice correlates with the disappearance of natural killer type 1-positive cells: evidence for their suppressive action on bone marrow stem cell proliferation, B cell immunoglobulin secretion, and autoimmune symptoms. J Exp Med, 1993, 177(1): 155-164.
34.	Lu L, Ikizawa K, Hu D, et al. Regulation of activated CD4⁺ T cells by NK cells via the Qa-1-NKG2A inhibitory pathway. Immunity, 2007, 26(5): 593-604.
35.	Lu L, Kim HJ, Werneck MB, et al. Regulation of CD8⁺ regulatory T cells: interruption of the NKG2A-Qa-1 interaction allows robust suppressive activity and resolution of autoimmune disease. Proc Natl Acad Sci U S A, 2008, 105(49): 19420-19425.
36.	Pallmer K, Oxenius A. Recognition and regulation of T cells by NK cells. Front Immunol, 2016, 7: 251.
37.	De Rose V, Cappello P, Sorbello V, et al. IFN-gamma inhibits the proliferation of allergen-activated T lymphocytes from atopic, asthmatic patients by inducing Fas/FasL-mediated apoptosis. J Leukoc Biol, 2004, 76(2): 423-432.
38.	Zhu J, Paul WE. CD4 T cells: fates, functions, and faults. Blood, 2008, 112(5): 1557-1569.
39.	Lee SH, Kim KS, Fodil-Cornu N, et al. Activating receptors promote NK cell expansion for maintenance, IL-10 production, and CD8 T cell regulation during viral infection. J Exp Med, 2009, 206(10): 2235-2251.
40.	Deniz G, Erten G, Kücüksezer UC, et al. Regulatory NK cells suppress antigen-specific T cell responses. J Immunol, 2008, 180(2): 850-857.
41.	Soderquest K, Walzer T, Zafirova B, et al. Cutting edge: CD8⁺ T cell priming in the absence of NK cells leads to enhanced memory responses. J Immunol, 2011, 186(6): 3304-3308.
42.	Li HJ, Zhai NC, Song HX, et al. The role of immune cells in chronic HBV infection. J Clin Transl Hepatol, 2015, 3(4): 277-283.
43.	Mandal A, Viswanathan C. Natural killer cells: in health and disease. Hematol Oncol Stem Cell Ther, 2015, 8(2): 47-55.
44.	姜峰奇, 姜涛, 张哲男, 等. 异基因免疫治疗中控制 GVHD 发生的研究进展. 现代生物医学进展, 2015, 15(9): 1760-1763.

1. 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): 112-117.
2. Jiao G, Wang B. NK cell subtypes as regulators of autoimmune liver disease. Gastroenterol Res Pract, 2016, 2016: 6903496.
3. Hong HS, Rajakumar PA, Billingsley JM, et al. No monkey business: why studying NK cells in non-human primates pays off. Front Immunol, 2013, 4: 32.
4. Vojvodić S, Popović S. Natural killer cells−biology, functions and clinical relevance. Med Pregl, 2010, 63(1-2): 91-97.
5. Fugier E, Marche H, Thélu MA, et al. Functions of liver natural killer cells are dependent on the severity of liver inflammation and fibrosis in chronic hepatitis C. PLoS One, 2014, 9(4): e95614.
6. Waggoner SN, Cornberg M, Selin LK, et al. Natural killer cells act as rheostats modulating antiviral T cells. Nature, 2011, 481(7381): 394-398.
7. Schuster IS, Coudert JD, Andoniou CE, et al. " Natural regulators”: NK cells as modulators of T cell immunity. Front Immunol, 2016, 7: 235.
8. Crome SQ, Lang PA, Lang KS, et al. Natural killer cells regulate diverse T cell responses. Trends Immunol, 2013, 34(7): 342-349.
9. Tu MM, Mahmoud AB, Makrigiannis AP. Licensed and unlicensed NK cells: differential roles in cancer and viral control. Front Immunol, 2016, 7: 166.
10. Lanier LL. Evolutionary struggles between NK cells and viruses. Nat Rev Immunol, 2008, 8(4): 259-268.
11. Moretta A, Marcenaro E, Sivori S, et al. Early liaisons between cells of the innate immune system in inflamed peripheral tissues. Trends Immunol, 2005, 26(12): 668-675.
12. Walzer T, Dalod M, Robbins SH, et al. Natural-killer cells and dendritic cells: " l'union fait la force”. Blood, 2005, 106(7): 2252-2258.
13. Fort MM, Leach MW, Rennick DM. A role for NK cells as regulators of CD4⁺ T cells in a transfer model of colitis. J Immunol, 1998, 161(7): 3256-3261.
14. Vankayalapati R, Klucar P, Wizel B, et al. NK cells regulate CD8⁺ T cell effector function in response to an intracellular pathogen. J Immunol, 2004, 172(1): 130-137.
15. Andrews DM, Estcourt MJ, Andoniou CE, et al. Innate immunity defines the capacity of antiviral T cells to limit persistent infection. J Exp Med, 2010, 207(6): 1333-1343.
16. Narni-Mancinelli E, Jaeger BN, Bernat C, et al. Tuning of natural killer cell reactivity by NKp46 and Helios calibrates T cell responses. Science, 2012, 335(6066): 344-348.
17. Cook KD, Whitmire JK. The depletion of NK cells prevents T cell exhaustion to efficiently control disseminating virus infection. J Immunol, 2013, 190(2): 641-649.
18. Su HC, Nguyen KB, Salazar-Mather TP, et al. NK cell functions restrain T cell responses during viral infections. Eur J Immunol, 2001, 31(10): 3048-3055.
19. Schuster IS, Wikstrom ME, Brizard G, et al. TRAIL⁺ NK cells control CD4⁺ T cell responses during chronic viral infection to limit autoimmunity. Immunity, 2014, 41(4): 646-656.
20. Waggoner SN, Taniguchi RT, Mathew PA, et al. Absence of mouse 2B4 promotes NK cell-mediated killing of activated CD8⁺ T cells, leading to prolonged viral persistence and altered pathogenesis. J Clin Invest, 2010, 120(6): 1925-1938.
21. Shin H, Wherry EJ. CD8 T cell dysfunction during chronic viral infection. Curr Opin Immunol, 2007, 19(4): 408-415.
22. Wherry EJ, Ha SJ, Kaech SM, et al. Molecular signature of CD8⁺ T cell exhaustion during chronic viral infection. Immunity, 2007, 27(4): 670-684.
23. Lang PA, Lang KS, Xu HC, et al. Natural killer cell activation enhances immune pathology and promotes chronic infection by limiting CD8⁺ T-cell immunity. Proc Natl Acad Sci U S A, 2012, 109(4): 1210-1215.
24. Pembroke T, Rees I, Gallagher K, et al. Rapid early innate control of hepatitis C virus during IFN-α treatment compromises adaptive CD4⁺ T-cell immunity. Eur J Immunol, 2012, 42(9): 2383-2394.
25. Schuch A, Hoh A, Thimme R. The role of natural killer cells and CD8(+) T cells in hepatitis B virus infection. Front Immunol, 2014, 5: 258.
26. Khakoo SI, Thio CL, Martin MP, et al. HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science, 2004, 305(5685): 872-874.
27. Yoon JC, Yang CM, Song Y, et al. Natural killer cells in hepatitis C: current progress. World J Gastroenterol, 2016, 22(4): 1449-1460.
28. 林延延. PegIFNα 治疗慢乙肝用药指导指标的筛选及 NK 细胞在慢性乙肝病毒感染中作用的初步探索. 厦门: 厦门大学, 2014.
29. McNerney ME, Lee KM, Zhou P, et al. Role of natural killer cell subsets in cardiac allograft rejection. Am J Transplant, 2006, 6(3): 505-513.
30. Beilke JN, Kuhl NR, Van Kaer L, et al. NK cells promote islet allograft tolerance via a perforin-dependent mechanism. Nat Med, 2005, 11(10): 1059-1065.
31. Bose A, Inoue Y, Kokko KE, et al. Cutting edge: perforin down-regulates CD4 and CD8 T cell-mediated immune responses to a transplanted organ. J Immunol, 2003, 170(4): 1611-1614.
32. Noval Rivas M, Hazzan M, Weatherly K, et al. NK cell regulation of CD4 T cell-mediated graft-versus-host disease. J Immunol, 2010, 184(12): 6790-6798.
33. Takeda K, Dennert G. The development of autoimmunity in C57BL/6 lpr mice correlates with the disappearance of natural killer type 1-positive cells: evidence for their suppressive action on bone marrow stem cell proliferation, B cell immunoglobulin secretion, and autoimmune symptoms. J Exp Med, 1993, 177(1): 155-164.
34. Lu L, Ikizawa K, Hu D, et al. Regulation of activated CD4⁺ T cells by NK cells via the Qa-1-NKG2A inhibitory pathway. Immunity, 2007, 26(5): 593-604.
35. Lu L, Kim HJ, Werneck MB, et al. Regulation of CD8⁺ regulatory T cells: interruption of the NKG2A-Qa-1 interaction allows robust suppressive activity and resolution of autoimmune disease. Proc Natl Acad Sci U S A, 2008, 105(49): 19420-19425.
36. Pallmer K, Oxenius A. Recognition and regulation of T cells by NK cells. Front Immunol, 2016, 7: 251.
37. De Rose V, Cappello P, Sorbello V, et al. IFN-gamma inhibits the proliferation of allergen-activated T lymphocytes from atopic, asthmatic patients by inducing Fas/FasL-mediated apoptosis. J Leukoc Biol, 2004, 76(2): 423-432.
38. Zhu J, Paul WE. CD4 T cells: fates, functions, and faults. Blood, 2008, 112(5): 1557-1569.
39. Lee SH, Kim KS, Fodil-Cornu N, et al. Activating receptors promote NK cell expansion for maintenance, IL-10 production, and CD8 T cell regulation during viral infection. J Exp Med, 2009, 206(10): 2235-2251.
40. Deniz G, Erten G, Kücüksezer UC, et al. Regulatory NK cells suppress antigen-specific T cell responses. J Immunol, 2008, 180(2): 850-857.
41. Soderquest K, Walzer T, Zafirova B, et al. Cutting edge: CD8⁺ T cell priming in the absence of NK cells leads to enhanced memory responses. J Immunol, 2011, 186(6): 3304-3308.
42. Li HJ, Zhai NC, Song HX, et al. The role of immune cells in chronic HBV infection. J Clin Transl Hepatol, 2015, 3(4): 277-283.
43. Mandal A, Viswanathan C. Natural killer cells: in health and disease. Hematol Oncol Stem Cell Ther, 2015, 8(2): 47-55.
44. 姜峰奇, 姜涛, 张哲男, 等. 异基因免疫治疗中控制 GVHD 发生的研究进展. 现代生物医学进展, 2015, 15(9): 1760-1763.

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Natural killer cells are the regulators of T cell immunity

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