Regulatory NK cells mediated between immunosuppressive monocytes and dysfunctional T cells in chronic HBV infection

Gut

Volumn 67, Issue 11, 2018, Pages 2035-2044

  Li, Haijun ^a   Zhai, Naicui ^a   Wang, Zhongfeng ^a   Song, Hongxiao ^a   Yang, Yang ^a   Cui, An ^a   Li, Tianyang ^a   Wang, Guangyi ^a   Niu, Junqi ^a   Crispe, Ian Nicholas ^a,b   Su, Lishan ^a,c   Tu, Zhengkun ^a  

^a JILIN UNIVERSITY   (China)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

HBV; HLA E; Monocytes; PD L1; Regulatory NK cells

Indexed keywords

HEPATITIS B SURFACE ANTIGEN; HLA E ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; MYELOID DIFFERENTIATION FACTOR 88; PROGRAMMED DEATH 1 LIGAND 1; TRANSFORMING GROWTH FACTOR BETA; CYTOKINE;

ADULT; ARTICLE; CELL DIFFERENTIATION; CHRONIC HEPATITIS B; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; LYMPHOCYTE ACTIVATION; MONOCYTE; NATURAL KILLER CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAINING; T LYMPHOCYTE; WESTERN BLOTTING; AGED; CELL CULTURE TECHNIQUE; FAR WESTERN BLOTTING; FEMALE; HEPATITIS B VIRUS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; MALE; METABOLISM; MIDDLE AGED;

ADULT; AGED; BLOTTING, FAR-WESTERN; CELL CULTURE TECHNIQUES; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; HUMANS; IMMUNE TOLERANCE; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; MONOCYTES; REAL-TIME POLYMERASE CHAIN REACTION; T-LYMPHOCYTES;

EID: 85042181003     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2017-314098     Document Type: Article

References (58)

1. Park JJ, Wong DK, Wahed AS, et al. HBV-specific and global T-cell dysfunction in chronic hepatitis B. Gastroenterology 2015;15:01736-9.
2. Ye B, Liu X, Li X, et al. T-cell exhaustion in chronic hepatitis B infection: current knowledge and clinical significance. Cell Death Dis 2015;6:e1694.
3. Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature 2009;457:557-61.
4. Artis D, Spits H. The biology of innate lymphoid cells. Nature 2015;517:293-301.
5. Shi J, Zhao Y, Wang Y, et al. Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 2014;514:187-92.
6. Dammermann W, Bentzien F, Stiel EM, et al. Development of a novel IGRA assay to test T cell responsiveness to HBV antigens in whole blood of chronic hepatitis B patients. J Transl Med 2015;13:157.
7. Wang S, Chen Z, Hu C, et al. Hepatitis B virus surface antigen selectively inhibits TLR2 ligand-induced IL-12 production in monocytes/macrophages by interfering with JNK activation. J Immunol 2013;190:5142-51.
8. Boltjes A, Groothuismink ZM, van Oord GW, et al. Monocytes from chronic HBV patients react in vitro to HBsAg and TLR by producing cytokines irrespective of stage of disease. PLoS One 2014;9:e97006.
9. Netea MG, Joosten LA, Latz E, et al. Trained immunity: a program of innate immune memory in health and disease. Science 2016;352:aaf1098.
10. Freeman BE, Raué HP, Hill AB, et al. Cytokine-mediated activation of NK cells during viral infection. J Virol 2015;89:7922-31.
11. Sepulveda FE, Maschalidi S, Vosshenrich CA, et al. A novel immunoregulatory role for NK-cell cytotoxicity in protection from HLH-like immunopathology in mice. Blood 2015;125:1427-34.
12. Wagage S, John B, Krock BL, et al. The aryl hydrocarbon receptor promotes IL-10 production by NK cells. J Immunol 2014;192:1661-70.
13. Ostapchuk YO, Cetin EA, Perfilyeva YV, et al. Peripheral blood NK cells expressing HLA-G, IL-10 and TGF-? in healthy donors and breast cancer patients. Cell Immunol 2015;298(1-2):37-46.
14. Stelma F, de Niet A, Tempelmans Plat-Sinnige MJ, et al. Natural killer cell characteristics in patients with chronic hepatitis B virus (HBV) infection are associated with HBV surface antigen clearance after combination treatment with pegylated interferon alfa-2a and adefovir. J Infect Dis 2015;212:1042-51.
15. Tjwa ET, van Oord GW, Hegmans JP, et al. Viral load reduction improves activation and function of natural killer cells in patients with chronic hepatitis B. J Hepatol 2011;54:209-18.
16. Micco L, Peppa D, Loggi E, et al. Differential boosting of innate and adaptive antiviral responses during pegylated-interferon-alpha therapy of chronic hepatitis B. J Hepatol 2013;58:225-33.
17. Lunemann S, Malone DF, Hengst J, et al. Compromised function of natural killer cells in acute and chronic viral hepatitis. J Infect Dis 2014;209:1362-73.
18. Tan AT , Hoang LT , Chin D, et al. Reduction of HBV replication prolongs the early immunological response to IFN? therapy. J Hepatol 2014;60:54-61.
19. Wu Y, Kuang DM, Pan WD, et al. Monocyte/macrophage-elicited natural killer cell dysfunction in hepatocellular carcinoma is mediated by CD48/2B4 interactions. Hepatology 2013;57:1107-16.
20. Spallanzani RG, Torres NI, Avila DE, et al. Regulatory dendritic cells restrain NK Cell IFN-? production through mechanisms involving NKp46, IL-10, and MHC class I-specific inhibitory receptors. J Immunol 2015;195:2141-8.
21. Welte S, Kuttruff S, Waldhauer I, et al. Mutual activation of natural killer cells and monocytes mediated by NKp80-AICL interaction. Nat Immunol 2006;7:1334-42.
22. Chaudhry UI, Kingham TP, Plitas G, et al. Combined stimulation with interleukin-18 and CpG induces murine natural killer dendritic cells to produce IFN-gamma and inhibit tumor growth. Cancer Res 2006;66:10497-504.
23. Zhang Q, Wang Y, Zhai N, et al. HCV core protein inhibits polarization and activity of both M1 and M2 macrophages through the TLR2 signaling pathway. Sci Rep 2016;6:36160.
24. Tian Y, Kuo CF, Akbari O, et al. Maternal-derived hepatitis B virus e antigen alters macrophage function in offspring to drive viral persistence after vertical transmission. Immunity 2016;44:1204-14.
25. Xiang KH, Michailidis E, Ding H, et al. Effects of amino acid substitutions in hepatitis B virus surface protein on virion secretion, antigenicity, HBsAg and viral DNA. J Hepatol 2017;66:288-96.
26. Li M, Sun R, Xu L, et al. Kupffer cells support hepatitis B virus-mediated CD8+ T cell exhaustion via hepatitis B core antigen-TLR2 interactions in mice. J Immunol 2015;195:3100-9.
27. Liu M, Xu Y, Han X, et al. Dioscin alleviates alcoholic liver fibrosis by attenuating hepatic stellate cell activation via the TLR4/MyD88/NF-?B signaling pathway. Sci Rep 2015;5:18038.
28. Mori N, Yamada Y, Ikeda S, et al. Bay 11-7082 inhibits transcription factor NF-kappaB and induces apoptosis of HTLV-I-infected T-cell lines and primary adult T-cell leukemia cells. Blood 2002;100:1828-34.
29. McMahon BJ. The natural history of chronic hepatitis B virus infection. Hepatology 2009;49:S45-55.
30. Hadziyannis SJ, Vassilopoulos D. Hepatitis B e antigen-negative chronic hepatitis B. Hepatology 2001;34:617-24.
31. Fang Z, Li J, Yu X, et al. Polarization of monocytic myeloid-derived suppressor cells by hepatitis B surface antigen is mediated via ERK/IL-6/STAT 3 signaling feedback and restrains the activation of T cells in chronic hepatitis B virus infection. J Immunol 2015;195:4873-83.
32. Cros J, Cagnard N, Woollard K, et al. Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 2010;33:375-86.
33. Chen S, Akbar SM, Abe M, et al. Immunosuppressive functions of hepatic myeloidderived suppressor cells of normal mice and in a murine model of chronic hepatitis B virus. Clin Exp Immunol 2011;166:134-42.
34. Pallett LJ, Gill US, Quaglia A, et al. Metabolic regulation of hepatitis B immunopathology by myeloid-derived suppressor cells. Nat Med 2015;21:591-600.
35. Zhang Z, Zhang S, Zou Z, et al. Hypercytolytic activity of hepatic natural killer cells correlates with liver injury in chronic hepatitis B patients. Hepatology 2011;53:73-85.
36. Dunn C, Brunetto M, Reynolds G, et al. Cytokines induced during chronic hepatitis B virus infection promote a pathway for NK cell-mediated liver damage. J Exp Med 2007;204:667-80.
37. Davis ZB, Cogswell A, Scott H, et al. A conserved HIV-1-derived peptide presented by HLA-E renders infected T-cells highly susceptible to attack by NKG2A/CD94-bearing natural killer cells. PLoS Pathog 2016;12:e1005421.
38. Della Chiesa M, Pesce S, Muccio L, et al. Features of memory-like and PD-1(+) human NK cell subsets. Front Immunol 2016;7:351.
39. Nattermann J, Feldmann G, Ahlenstiel G, et al. Surface expression and cytolytic function of natural killer cell receptors is altered in chronic hepatitis C. Gut 2006;55:869-77.
40. Li F, Wei H, Wei H, et al. Blocking the natural killer cell inhibitory receptor NKG2A increases activity of human natural killer cells and clears hepatitis B virus infection in mice. Gastroenterology 2013;144:392-401.
41. Shi B, Ren G, Hu Y, et al. HBsAg inhibits IFN-? production in plasmacytoid dendritic cells through TNF-? and IL-10 induction in monocytes. PLoS One 2012;7:e44900.
42. Nishio A, Tatsumi T, Nawa T, et al. CD14(+) monocyte-derived galectin-9 induces natural killer cell cytotoxicity in chronic hepatitis C. Hepatology 2017;65:18-31.
43. Tu Z, Bozorgzadeh A, Pierce RH, et al. TLR-dependent cross talk between human kupffer cells and NK cells. J Exp Med 2008;205:233-44.
44. Tripp CS, Wolf SF, Unanue ER. Interleukin 12 and tumor necrosis factor alpha are costimulators of interferon gamma production by natural killer cells in severe combined immunodeficiency mice with listeriosis, and interleukin 10 is a physiologic antagonist. Proc Natl Acad Sci U S A 1993;90:3725-9.
45. Vivier E, Ugolini S. Regulatory natural killer cells: new players in the IL-10 antiinflammatory response. Cell Host Microbe 2009;6:493-5.
46. Maier H, Isogawa M, Freeman GJ, et al. PD-1:PD-L1 interactions contribute to the functional suppression of virus-specific CD8+ T lymphocytes in the liver. J Immunol 2007;178:2714-20.
47. Tian Y, Kuo CF, Akbari O, et al. Maternal-derived hepatitis B virus e antigen alters macrophage function in offspring to drive viral persistence after vertical transmission. Immunity 2016;44:1204-14.
48. Martinet J, Dufeu-Duchesne T, Bruder Costa J, et al. Altered functions of plasmacytoid dendritic cells and reduced cytolytic activity of natural killer cells in patients with chronic HBV infection. Gastroenterology 2012;143:1586-96.
49. Boltjes A, van Montfoort N, Biesta PJ, et al. Kupffer cells interact with hepatitis B surface antigen in vivo and in vitro, leading to proinflammatory cytokine production and natural killer cell function. J Infect Dis 2015;211:1268-78.
50. Zannetti C, Roblot G, Charrier E, et al. Characterization of the inflammasome in human kupffer cells in response to synthetic agonists and pathogens. J Immunol 2016;197:356-67.
51. Fu B, Tian Z, Wei H. Subsets of human natural killer cells and their regulatory effects. Immunology 2014;141:483-9.
52. Zhang C, Zhang J, Tian Z. The regulatory effect of natural killer cells: do 'NK-reg cells' exist? Cell Mol Immunol 2006;3:241-54.
53. Arck PC, Hecher K. Fetomaternal immune cross-talk and its consequences for maternal and offspring's health. Nat Med 2013;19:548-56.
54. Tian Z, Chen Y, Gao B. Natural killer cells in liver disease. Hepatology 2013;57:1654-62.
55. Clark SE, Filak HC, Guthrie BS, et al. Bacterial manipulation of NK cell regulatory activity increases susceptibility to listeria monocytogenes infection. PLoS Pathog 2016;12:e1005708.
56. French AR, Yokoyama WM. Natural killer cells and viral infections. Curr Opin Immunol 2003;15:45-51.
57. Biron CA, Nguyen KB, Pien GC, et al. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol 1999;17:189-220.
58. Peppa D, Gill US, Reynolds G, et al. Up-regulation of a death receptor renders antiviral T cells susceptible to NK cell-mediated deletion. J Exp Med 2013;210:99-114.