|
|
Natural killer cells in liver diseases |
Meijuan Zheng1(), Haoyu Sun2, Zhigang Tian2,3 |
1. Department of Clinical Laboratory, First Affiliated Hospital of Anhui Medical University, Hefei 230022, China 2. Institute of Immunology, Key Laboratory of Innate Immunity and Chronic Disease of Chinese Academy of Sciences, School of Life Sciences and Medical Center, University of Science and Technology of China, Hefei 230027, China 3. Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou 310003, China |
|
|
Abstract The liver has been characterized as a frontline lymphoid organ with complex immunological features such as liver immunity and liver tolerance. Liver tolerance plays an important role in liver diseases including acute inflammation, chronic infection, autoimmune disease, and tumors. The liver contains a large proportion of natural killer (NK) cells, which exhibit heterogeneity in phenotypic and functional characteristics. NK cell activation, well known for its role in the immune surveillance against tumor and pathogen-infected cells, depends on the balance between numerous activating and inhibitory signals. In addition to the innate direct “killer” functions, NK cell activity contributes to regulate innate and adaptive immunity (helper or regulator). Under the setting of liver diseases, NK cells are of great importance for stimulating or inhibiting immune responses, leading to either immune activation or immune tolerance. Here, we focus on the relationship between NK cell biology, such as their phenotypic features and functional diversity, and liver diseases.
|
Keywords
natural killer cell
phenotype
immune activation
immune tolerance
liver diseases
|
Corresponding Author(s):
Meijuan Zheng
|
Just Accepted Date: 12 February 2018
Online First Date: 17 April 2018
Issue Date: 04 May 2018
|
|
1 |
Crispe IN. The liver as a lymphoid organ. Annu Rev Immunol 2009; 27(1): 147–163
https://doi.org/10.1146/annurev.immunol.021908.132629
pmid: 19302037
|
2 |
Calne RY, Sells RA, Pena JR, Davis DR, Millard PR, Herbertson BM, Binns RM, Davies DA. Induction of immunological tolerance by porcine liver allografts. Nature 1969; 223(5205): 472–476
https://doi.org/10.1038/223472a0
pmid: 4894426
|
3 |
Qian S, Demetris AJ, Murase N, Rao AS, Fung JJ, Starzl TE. Murine liver allograft transplantation: tolerance and donor cell chimerism. Hepatology 1994; 19(4): 916–924
https://doi.org/10.1002/hep.1840190418
pmid: 8138266
|
4 |
Protzer U, Maini MK, Knolle PA. Living in the liver: hepatic infections. Nat Rev Immunol 2012; 12(3): 201–213
https://doi.org/10.1038/nri3169
pmid: 22362353
|
5 |
Bogdanos DP, Gao B, Gershwin ME. Liver immunology. Compr Physiol 2013; 3(2): 567–598
pmid: 23720323
|
6 |
Racanelli V, Rehermann B. The liver as an immunological organ. Hepatology 2006; 43(2 Suppl 1): S54–S62
https://doi.org/10.1002/hep.21060
pmid: 16447271
|
7 |
Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol 2008; 9(5): 503–510
https://doi.org/10.1038/ni1582
pmid: 18425107
|
8 |
Lanier LL. NK cell recognition. Annu Rev Immunol 2005; 23(1): 225–274
https://doi.org/10.1146/annurev.immunol.23.021704.115526
pmid: 15771571
|
9 |
Yokoyama WM, Kim S, French AR. The dynamic life of natural killer cells. Annu Rev Immunol 2004; 22(1): 405–429
https://doi.org/10.1146/annurev.immunol.22.012703.104711
pmid: 15032583
|
10 |
Jinushi M, Takehara T, Tatsumi T, Yamaguchi S, Sakamori R, Hiramatsu N, Kanto T, Ohkawa K, Hayashi N. Natural killer cell and hepatic cell interaction via NKG2A leads to dendritic cell-mediated induction of CD4 CD25 T cells with PD-1-dependent regulatory activities. Immunology 2007; 120(1): 73–82
https://doi.org/10.1111/j.1365-2567.2006.02479.x
pmid: 17052247
|
11 |
Lassen MG, Lukens JR, Dolina JS, Brown MG, Hahn YS. Intrahepatic IL-10 maintains NKG2A+Ly49− liver NK cells in a functionally hyporesponsive state. J Immunol 2010; 184(5): 2693–2701
https://doi.org/10.4049/jimmunol.0901362
pmid: 20124099
|
12 |
Shi CC, Tjwa ET, Biesta PJ, Boonstra A, Xie Q, Janssen HL, Woltman AM. Hepatitis B virus suppresses the functional interaction between natural killer cells and plasmacytoid dendritic cells. J Viral Hepat 2012; 19(2): e26–e33
https://doi.org/10.1111/j.1365-2893.2011.01496.x
pmid: 22239523
|
13 |
Tu Z, Bozorgzadeh A, Pierce RH, Kurtis J, Crispe IN, Orloff MS. TLR-dependent cross talk between human Kupffer cells and NK cells. J Exp Med 2008; 205(1): 233–244
https://doi.org/10.1084/jem.20072195
pmid: 18195076
|
14 |
Knolle PA, Gerken G. Local control of the immune response in the liver. Immunol Rev 2000; 174(1): 21–34
https://doi.org/10.1034/j.1600-0528.2002.017408.x
pmid: 10807504
|
15 |
Gao B. Basic liver immunology. Cell Mol Immunol 2016; 13(3): 265–266
https://doi.org/10.1038/cmi.2016.09
pmid: 27041634
|
16 |
Bowen DG, McCaughan GW, Bertolino P. Intrahepatic immunity: a tale of two sites? Trends Immunol 2005; 26(10): 512–517
https://doi.org/10.1016/j.it.2005.08.005
pmid: 16109501
|
17 |
Yoneyama H, Ichida T. Recruitment of dendritic cells to pathological niches in inflamed liver. Med Mol Morphol 2005; 38(3): 136–141
https://doi.org/10.1007/s00795-005-0289-0
pmid: 16170461
|
18 |
Grant AJ, Goddard S, Ahmed-Choudhury J, Reynolds G, Jackson DG, Briskin M, Wu L, Hübscher SG, Adams DH. Hepatic expression of secondary lymphoid chemokine (CCL21) promotes the development of portal-associated lymphoid tissue in chronic inflammatory liver disease. Am J Pathol 2002; 160(4): 1445–1455
https://doi.org/10.1016/S0002-9440(10)62570-9
pmid: 11943728
|
19 |
Schildberg FA, Hegenbarth SI, Schumak B, Scholz K, Limmer A, Knolle PA. Liver sinusoidal endothelial cells veto CD8 T cell activation by antigen-presenting dendritic cells. Eur J Immunol 2008; 38(4): 957–967
https://doi.org/10.1002/eji.200738060
pmid: 18383043
|
20 |
Bertolino P, Bowen DG, McCaughan GW, Fazekas de St Groth B. Antigen-specific primary activation of CD8+ T cells within the liver. J Immunol 2001; 166(9): 5430–5438
https://doi.org/10.4049/jimmunol.166.9.5430
pmid: 11313380
|
21 |
Bertolino P, Trescol-Biémont MC, Rabourdin-Combe C. Hepatocytes induce functional activation of naive CD8+ T lymphocytes but fail to promote survival. Eur J Immunol 1998; 28(1): 221–236
https://doi.org/10.1002/(SICI)1521-4141(199801)28:01<221::AID-IMMU221>3.0.CO;2-F
pmid: 9485202
|
22 |
Zheng M, Yu J, Tian Z. Characterization of the liver-draining lymph nodes in mice and their role in mounting regional immunity to HBV. Cell Mol Immunol 2013; 10(2): 143–150
https://doi.org/10.1038/cmi.2012.59
pmid: 23376862
|
23 |
Barbier L, Tay SS, McGuffog C, Triccas JA, McCaughan GW, Bowen DG, Bertolino P. Two lymph nodes draining the mouse liver are the preferential site of DC migration and T cell activation. J Hepatol 2012; 57(2): 352–358
https://doi.org/10.1016/j.jhep.2012.03.023
pmid: 22542491
|
24 |
Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol 2001; 22(11): 633–640
https://doi.org/10.1016/S1471-4906(01)02060-9
pmid: 11698225
|
25 |
Yu J, Mao HC, Wei M, Hughes T, Zhang J, Park IK, Liu S, McClory S, Marcucci G, Trotta R, Caligiuri MA. CD94 surface density identifies a functional intermediary between the CD56bright and CD56dim human NK-cell subsets. Blood 2010; 115(2): 274–281
https://doi.org/10.1182/blood-2009-04-215491
pmid: 19897577
|
26 |
Björkström NK, Riese P, Heuts F, Andersson S, Fauriat C, Ivarsson MA, Björklund AT, Flodström-Tullberg M, Michaëlsson J, Rottenberg ME, Guzmán CA, Ljunggren HG, Malmberg KJ. Expression patterns of NKG2A, KIR, and CD57 define a process of CD56dim NK-cell differentiation uncoupled from NK-cell education. Blood 2010; 116(19): 3853–3864
https://doi.org/10.1182/blood-2010-04-281675
pmid: 20696944
|
27 |
Lopez-Vergès S, Milush JM, Pandey S, York VA, Arakawa-Hoyt J, Pircher H, Norris PJ, Nixon DF, Lanier LL. CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset. Blood 2010; 116(19): 3865–3874
https://doi.org/10.1182/blood-2010-04-282301
pmid: 20733159
|
28 |
Juelke K, Killig M, Luetke-Eversloh M, Parente E, Gruen J, Morandi B, Ferlazzo G, Thiel A, Schmitt-Knosalla I, Romagnani C. CD62L expression identifies a unique subset of polyfunctional CD56dim NK cells. Blood 2010; 116(8): 1299–1307
https://doi.org/10.1182/blood-2009-11-253286
pmid: 20505160
|
29 |
Peritt D, Robertson S, Gri G, Showe L, Aste-Amezaga M, Trinchieri G. Differentiation of human NK cells into NK1 and NK2 subsets. J Immunol 1998; 161(11): 5821–5824
pmid: 9834059
|
30 |
Fu B, Tian Z, Wei H. Subsets of human natural killer cells and their regulatory effects. Immunology 2014; 141(4): 483–489
https://doi.org/10.1111/imm.12224
pmid: 24303897
|
31 |
Chiossone L, Chaix J, Fuseri N, Roth C, Vivier E, Walzer T. Maturation of mouse NK cells is a 4-stage developmental program. Blood 2009; 113(22): 5488–5496
https://doi.org/10.1182/blood-2008-10-187179
pmid: 19234143
|
32 |
Fu B, Wang F, Sun R, Ling B, Tian Z, Wei H. CD11b and CD27 reflect distinct population and functional specialization in human natural killer cells. Immunology 2011; 133(3): 350–359
https://doi.org/10.1111/j.1365-2567.2011.03446.x
pmid: 21506999
|
33 |
Erick TK, Brossay L. Phenotype and functions of conventional and non-conventional NK cells. Curr Opin Immunol 2016; 38: 67–74
https://doi.org/10.1016/j.coi.2015.11.007
pmid: 26706497
|
34 |
Sojka DK, Tian Z, Yokoyama WM. Tissue-resident natural killer cells and their potential diversity. Semin Immunol 2014; 26(2): 127–131
https://doi.org/10.1016/j.smim.2014.01.010
pmid: 24548893
|
35 |
Sojka DK, Plougastel-Douglas B, Yang L, Pak-Wittel MA, Artyomov MN, Ivanova Y, Zhong C, Chase JM, Rothman PB, Yu J, Riley JK, Zhu J, Tian Z, Yokoyama WM. Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells. eLife 2014; 3e01659
|
36 |
Doisne JM, Balmas E, Boulenouar S, Gaynor LM, Kieckbusch J, Gardner L, Hawkes DA, Barbara CF, Sharkey AM, Brady HJ, Brosens JJ, Moffett A, Colucci F. Composition, development, and function of uterine innate lymphoid cells. J Immunol 2015; 195(8): 3937–3945
https://doi.org/10.4049/jimmunol.1500689
pmid: 26371244
|
37 |
Victorino F, Sojka DK, Brodsky KS, McNamee EN, Masterson JC, Homann D, Yokoyama WM, Eltzschig HK, Clambey ET. Tissue-resident NK cells mediate ischemic kidney injury and are not depleted by anti-Asialo-GM1 antibody. J Immunol 2015; 195(10): 4973–4985
https://doi.org/10.4049/jimmunol.1500651
pmid: 26453755
|
38 |
Peng H, Jiang X, Chen Y, Sojka DK, Wei H, Gao X, Sun R, Yokoyama WM, Tian Z. Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J Clin Invest 2013; 123(4): 1444–1456
https://doi.org/10.1172/JCI66381
pmid: 23524967
|
39 |
Han Q, Zhang C, Zhang J, Tian Z. The role of innate immunity in HBV infection. Semin Immunopathol 2013; 35(1): 23–38
https://doi.org/10.1007/s00281-012-0331-y
pmid: 22814721
|
40 |
Sun H, Sun C, Tian Z, Xiao W. NK cells in immunotolerant organs. Cell Mol Immunol 2013; 10(3): 202–212
https://doi.org/10.1038/cmi.2013.9
pmid: 23563087
|
41 |
Peng H, Wisse E, Tian Z. Liver natural killer cells: subsets and roles in liver immunity. Cell Mol Immunol 2016; 13(3): 328–336
https://doi.org/10.1038/cmi.2015.96
pmid: 26639736
|
42 |
Walch M, Dotiwala F, Mulik S, Thiery J, Kirchhausen T, Clayberger C, Krensky AM, Martinvalet D, Lieberman J. Cytotoxic cells kill intracellular bacteria through granulysin-mediated delivery of granzymes. Cell 2014; 157(6): 1309–1323
https://doi.org/10.1016/j.cell.2014.03.062
pmid: 24906149
|
43 |
Peppa D, Gill US, Reynolds G, Easom NJ, Pallett LJ, Schurich A, Micco L, Nebbia G, Singh HD, Adams DH, Kennedy PT, Maini MK. Up-regulation of a death receptor renders antiviral T cells susceptible to NK cell-mediated deletion. J Exp Med 2013; 210(1): 99–114
https://doi.org/10.1084/jem.20121172
pmid: 23254287
|
44 |
Krueger PD, Narayanan S, Surette FA, Brown MG, Sung SJ, Hahn YS. Murine liver-resident group 1 innate lymphoid cells regulate optimal priming of anti-viral CD8+ T cells. J Leukoc Biol 2017; 101(1): 329–338
https://doi.org/10.1189/jlb.3A0516-225R
pmid: 27493244
|
45 |
Shi FD, Ljunggren HG, La Cava A, Van Kaer L. Organ-specific features of natural killer cells. Nat Rev Immunol 2011; 11(10): 658–671
https://doi.org/10.1038/nri3065
pmid: 21941294
|
46 |
Crome SQ, Lang PA, Lang KS, Ohashi PS. Natural killer cells regulate diverse T cell responses. Trends Immunol 2013; 34(7): 342–349
https://doi.org/10.1016/j.it.2013.03.002
pmid: 23601842
|
47 |
Zhang C, Zhang J, Tian Z. The regulatory effect of natural killer cells: do “NK-reg cells” exist? Cell Mol Immunol 2006; 3(4): 241–254
pmid: 16978532
|
48 |
Schafer JL, Müller-Trutwin MC, Reeves RK. NK cell exhaustion: bad news for chronic disease? Oncotarget 2015; 6(26): 21797–21798
https://doi.org/10.18632/oncotarget.5490
pmid: 26392410
|
49 |
Long EO, Kim HS, Liu D, Peterson ME, Rajagopalan S. Controlling natural killer cell responses: integration of signals for activation and inhibition. Annu Rev Immunol 2013; 31(1): 227–258
https://doi.org/10.1146/annurev-immunol-020711-075005
pmid: 23516982
|
50 |
Lanier LL. Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol 2008; 9(5): 495–502
https://doi.org/10.1038/ni1581
pmid: 18425106
|
51 |
Watzl C, Long EO. Signal transduction during activation and inhibition of natural killer cells. Curr Protoc Immunol 2010; Chapter 11 Unit 11 19B
|
52 |
Tian Z, Chen Y, Gao B. Natural killer cells in liver disease. Hepatology 2013; 57(4): 1654–1662
https://doi.org/10.1002/hep.26115
pmid: 23111952
|
53 |
Robinson MW, Harmon C, O’Farrelly C. Liver immunology and its role in inflammation and homeostasis. Cell Mol Immunol 2016; 13(3): 267–276
https://doi.org/10.1038/cmi.2016.3
pmid: 27063467
|
54 |
Bertoletti A, Wang FS. Overview of the special issue on HBV immunity. Cell Mol Immunol 2015; 12(3): 253–254
https://doi.org/10.1038/cmi.2015.24
pmid: 25864914
|
55 |
Timm J, Walker CM. Mutational escape of CD8+ T cell epitopes: implications for prevention and therapy of persistent hepatitis virus infections. Med Microbiol Immunol (Berl) 2015; 204(1): 29–38
https://doi.org/10.1007/s00430-014-0372-z
pmid: 25537849
|
56 |
Shuai Z, Leung MW, He X, Zhang W, Yang G, Leung PS, Eric Gershwin M. Adaptive immunity in the liver. Cell Mol Immunol 2016; 13(3): 354–368
https://doi.org/10.1038/cmi.2016.4
pmid: 26996069
|
57 |
Billerbeck E, Wolfisberg R, Fahnoe U, Xiao JW, Quirk C, Luna JM, Cullen JM, Hartlage AS, Chiriboga L, Ghoshal K, Lipkin WI, Bukh J, Scheel TKH, Kapoor A, Rice CM. Mouse models of acute and chronic hepacivirus infection. Science 2017; 357(6347): 204–208
https://doi.org/10.1126/science.aal1962
pmid: PMID:28706073
|
58 |
Fu QX, Yan SD, Wang LC, Duan XG, Wang L, Wang Y, Wu T, Wang XH, An J, Zhang YL, Zhou QQ, Zhan LS. Hepatic NK cell-mediated hypersensitivity to ConA-induced liver injury in mouse liver expressing hepatitis C virus polyprotein. Oncotarget 2017; 8(32): 52178–52192
https://doi.org/10.18632/oncotarget.11052
pmid: PMID:28881722
|
59 |
Tjwa ETTL, van Oord GW, Hegmans JP, Janssen HLA, Woltman AM. Viral load reduction improves activation and function of natural killer cells in patients with chronic hepatitis B. J Hepatol 2011; 54(2): 209–218
https://doi.org/10.1016/j.jhep.2010.07.009
pmid: 21095036
|
60 |
Oliviero B, Varchetta S, Paudice E, Michelone G, Zaramella M, Mavilio D, De Filippi F, Bruno S, Mondelli MU. Natural killer cell functional dichotomy in chronic hepatitis B and chronic hepatitis C virus infections. Gastroenterology 2009; 137(3): 1151–1160.e7
https://doi.org/10.1053/j.gastro.2009.05.047
pmid: 19470388
|
61 |
Shimoda S, Harada K, Niiro H, Shirabe K, Taketomi A, Maehara Y, Tsuneyama K, Nakanuma Y, Leung P, Ansari AA, Gershwin ME, Akashi K. Interaction between Toll-like receptors and natural killer cells in the destruction of bile ducts in primary biliary cirrhosis. Hepatology 2011; 53(4): 1270–1281
https://doi.org/10.1002/hep.24194
pmid: 21400555
|
62 |
Hudspeth K, Pontarini E, Tentorio P, Cimino M, Donadon M, Torzilli G, Lugli E, Della Bella S, Gershwin ME, Mavilio D. The role of natural killer cells in autoimmune liver disease: a comprehensive review. J Autoimmun 2013; 46: 55–65
https://doi.org/10.1016/j.jaut.2013.07.003
pmid: 23880068
|
63 |
Cai L, Zhang Z, Zhou L, Wang H, Fu J, Zhang S, Shi M, Zhang H, Yang Y, Wu H, Tien P, Wang FS. Functional impairment in circulating and intrahepatic NK cells and relative mechanism in hepatocellular carcinoma patients. Clin Immunol 2008; 129(3): 428–437
https://doi.org/10.1016/j.clim.2008.08.012
pmid: 18824414
|
64 |
Horst AK, Neumann K, Diehl L, Tiegs G. Modulation of liver tolerance by conventional and nonconventional antigen-presenting cells and regulatory immune cells. Cell Mol Immunol 2016; 13(3): 277–292
https://doi.org/10.1038/cmi.2015.112
pmid: 27041638
|
65 |
Golden-Mason L, Rosen HR. Natural killer cells: multifaceted players with key roles in hepatitis C immunity. Immunol Rev 2013; 255(1): 68–81
https://doi.org/10.1111/imr.12090
pmid: 23947348
|
66 |
Serti E, Chepa-Lotrea X, Kim YJ, Keane M, Fryzek N, Liang TJ, Ghany M, Rehermann B. Successful interferon-free therapy of chronic hepatitis C virus infection normalizes natural killer cell function. Gastroenterology 2015; 149(1):190–200.e2
https://doi.org/10.1053/j.gastro.2015.03.004
pmid: PMID: 25754160
|
67 |
Zhao J, Li Y, Jin L, Zhang S, Fan R, Sun Y, Zhou C, Shang Q, Li W, Zhang Z, Wang FS. Natural killer cells are characterized by the concomitantly increased interferon-g and cytotoxicity in acute resolved hepatitis B patients. PLoS One 2012; 7(11): e49135
https://doi.org/10.1371/journal.pone.0049135
pmid: 23133672
|
68 |
Golden-Mason L, Cox AL, Randall JA, Cheng L, Rosen HR. Increased natural killer cell cytotoxicity and NKp30 expression protects against hepatitis C virus infection in high-risk individuals and inhibits replication in vitro. Hepatology 2010; 52(5): 1581–1589
https://doi.org/10.1002/hep.23896
pmid: 20812318
|
69 |
Knapp S, Warshow U, Hegazy D, Brackenbury L, Guha IN, Fowell A, Little AM, Alexander GJ, Rosenberg WM, Cramp ME, Khakoo SI. Consistent beneficial effects of killer cell immunoglobulin-like receptor 2DL3 and group 1 human leukocyte antigen-C following exposure to hepatitis C virus. Hepatology 2010; 51(4): 1168–1175
https://doi.org/10.1002/hep.23477
pmid: 20077564
|
70 |
Abdelrahman MM, Fawzy IO, Bassiouni AA, Gomaa AI, Esmat G, Waked I, Abdelaziz AI. Enhancing NK cell cytotoxicity by miR-182 in hepatocellular carcinoma. Hum Immunol 2016; 77(8): 667–673
https://doi.org/10.1016/j.humimm.2016.04.020
pmid: 27262453
|
71 |
Lasfar A, de laTorre A, Abushahba W, Cohen-Solal KA, Castaneda I, Yuan Y, Reuhl K, Zloza A, Raveche E, Laskin DL, Kotenko SV. Concerted action of IFN-α and IFN-l induces local NK cell immunity and halts cancer growth. Oncotarget 2016; 7(31): 49259–49267
https://doi.org/10.18632/oncotarget.10272
pmid: 27363032
|
72 |
Maini MK, Peppa D. NK cells: a double-edged sword in chronic hepatitis B virus infection. Front Immunol 2013; 4: 57
https://doi.org/10.3389/fimmu.2013.00057
pmid: 23459859
|
73 |
Ghosh S, Nandi M, Pal S, Mukhopadhyay D, Chakraborty BC, Khatun M, Bhowmick D, Mondal RK, Das S, Das K, Ghosh R, Banerjee S, Santra A, Chatterjee M, Chowdhury A, Datta S. Natural killer cells contribute to hepatic injury and help in viral persistence during progression of hepatitis B e-antigen-negative chronic hepatitis B virus infection. Clin Microbiol Infect 2016; 22(8):733.e9–733.e19
https://doi.org/10.1016/j.cmi.2016.05.009
pmid: 27208430
|
74 |
Zheng Q, Zhu YY, Chen J, Ye YB, Li JY, Liu YR, Hu ML, Zheng YC, Jiang JJ. Activated natural killer cells accelerate liver damage in patients with chronic hepatitis B virus infection. Clin Exp Immunol 2015; 180(3): 499–508
https://doi.org/10.1111/cei.12597
pmid: 25639451
|
75 |
Abu-Tair L, Axelrod JH, Doron S, Ovadya Y, Krizhanovsky V, Galun E, Amer J, Safadi R. Natural killer cell-dependent anti-fibrotic pathway in liver injury via Toll-like receptor-9. PLoS One 2013; 8(12): e82571
https://doi.org/10.1371/journal.pone.0082571
pmid: 24340043
|
76 |
Glässner A, Eisenhardt M, Krämer B, Körner C, Coenen M, Sauerbruch T, Spengler U, Nattermann J. NK cells from HCV-infected patients effectively induce apoptosis of activated primary human hepatic stellate cells in a TRAIL-, FasL- and NKG2D-dependent manner. Lab Invest 2012; 92(7): 967–977
https://doi.org/10.1038/labinvest.2012.54
pmid: 22449797
|
77 |
Radaeva S, Sun R, Jaruga B, Nguyen VT, Tian Z, Gao B. Natural killer cells ameliorate liver fibrosis by killing activated stellate cells in NKG2D-dependent and tumor necrosis factor-related apoptosis-inducing ligand-dependent manners. Gastroenterology 2006; 130(2): 435–452
https://doi.org/10.1053/j.gastro.2005.10.055
pmid: 16472598
|
78 |
Doherty DG. Immunity, tolerance and autoimmunity in the liver: a comprehensive review. J Autoimmun 2016; 66: 60–75
https://doi.org/10.1016/j.jaut.2015.08.020
pmid: 26358406
|
79 |
Tian Z, Gershwin ME, Zhang C. Regulatory NK cells in autoimmune disease. J Autoimmun 2012; 39(3): 206–215
https://doi.org/10.1016/j.jaut.2012.05.006
pmid: 22704425
|
80 |
Chuang YH, Lian ZX, Cheng CM, Lan RY, Yang GX, Moritoki Y, Chiang BL, Ansari AA, Tsuneyama K, Coppel RL, Gershwin ME. Increased levels of chemokine receptor CXCR3 and chemokines IP-10 and MIG in patients with primary biliary cirrhosis and their first degree relatives. J Autoimmun 2005; 25(2): 126–132
https://doi.org/10.1016/j.jaut.2005.08.009
pmid: 16243485
|
81 |
Liang Y, Yang Z, Li C, Zhu Y, Zhang L, Zhong R. Characterisation of TNF-related apoptosis-inducing ligand in peripheral blood in patients with primary biliary cirrhosis. Clin Exp Med 2008; 8(1): 1–7
https://doi.org/10.1007/s10238-008-0149-z
pmid: 18385934
|
82 |
Lanier LL. Evolutionary struggles between NK cells and viruses. Nat Rev Immunol 2008; 8(4): 259–268
https://doi.org/10.1038/nri2276
pmid: 18340344
|
83 |
Martín-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A, Sallusto F. Induced recruitment of NK cells to lymph nodes provides IFN-γ for T(H)1 priming. Nat Immunol 2004; 5(12): 1260–1265
https://doi.org/10.1038/ni1138
pmid: 15531883
|
84 |
Zheng M, Sun R, Wei H, Tian Z. NK cells help induce anti-hepatitis B virus CD8+ T cell immunity in mice. J Immunol 2016; 196(10): 4122–4131
https://doi.org/10.4049/jimmunol.1500846
pmid: 27183639
|
85 |
Combe CL, Curiel TJ, Moretto MM, Khan IA. NK cells help to induce CD8+-T-cell immunity against Toxoplasma gondii in the absence of CD4+ T cells. Infect Immun 2005; 73(8): 4913–4921
https://doi.org/10.1128/IAI.73.8.4913-4921.2005
pmid: 16041005
|
86 |
Geldhof AB, Van Ginderachter JA, Liu Y, Noël W, Raes G, De Baetselier P. Antagonistic effect of NK cells on alternatively activated monocytes: a contribution of NK cells to CTL generation. Blood 2002; 100(12): 4049–4058
https://doi.org/10.1182/blood-2001-11-0106
pmid: 12393627
|
87 |
Allen F, Rauhe P, Askew D, Tong AA, Nthale J, Eid S, Myers JT, Tong C, Huang AY. CCL3 enhances antitumor immune priming in the lymph node via IFN γ with dependency on natural killer cells. Front Immunol 2017; 8 :1390
https://doi.org/10.3389/fimmu.2017.01390
pmid: PMID: 29109732
|
88 |
Adam C, King S, Allgeier T, Braumüller H, Lüking C, Mysliwietz J, Kriegeskorte A, Busch DH, Röcken M, Mocikat R. DC-NK cell cross talk as a novel CD4+ T-cell-independent pathway for antitumor CTL induction. Blood 2005; 106(1): 338–344
https://doi.org/10.1182/blood-2004-09-3775
pmid: 15769894
|
89 |
Yuan D. Interactions between NK cells and B lymphocytes. Adv Immunol 2004; 84: 1–42
https://doi.org/10.1016/S0065-2776(04)84001-X
pmid: 15246249
|
90 |
Krebs P, Barnes MJ, Lampe K, Whitley K, Bahjat KS, Beutler B, Janssen E, Hoebe K. NK-cell-mediated killing of target cells triggers robust antigen-specific T-cell-mediated and humoral responses. Blood 2009; 113(26): 6593–6602
https://doi.org/10.1182/blood-2009-01-201467
pmid: 19406986
|
91 |
Li F, Tian Z. The liver works as a school to educate regulatory immune cells. Cell Mol Immunol 2013; 10(4): 292–302
https://doi.org/10.1038/cmi.2013.7
pmid: 23604044
|
92 |
Yang Y, Han Q, Hou Z, Zhang C, Tian Z, Zhang J. Exosomes mediate hepatitis B virus (HBV) transmission and NK-cell dysfunction. Cell Mol Immunol 2017; 14(5): 465–475
https://doi.org/10.1038/cmi.2016.24
pmid: 27238466
|
93 |
Zhang QF, Yin WW, Xia Y, Yi YY, He QF, Wang X, Ren H, Zhang DZ. Liver-infiltrating CD11b−CD27− NK subsets account for NK-cell dysfunction in patients with hepatocellular carcinoma and are associated with tumor progression. Cell Mol Immunol 2017; 14(10): 819–829
pmid: 27321064
|
94 |
Cai L, Zhang Z, Zhou L, Wang H, Fu J, Zhang S, Shi M, Zhang H, Yang Y, Wu H, Tien P, Wang FS. Functional impairment in circulating and intrahepatic NK cells and relative mechanism in hepatocellular carcinoma patients. Clin Immunol 2008; 129(3): 428–437
https://doi.org/10.1016/j.clim.2008.08.012
pmid: 18824414
|
95 |
Chen T, Zhu L, Shi AC, Ding L, Zhang XP, Tan ZM, Guo W, Yan WM, Han MF, Jia JD, Luo XP, Schuppan D, Ning Q. Functional restoration of CD56bright NK cells facilitates immune control via IL-15 and NKG2D in patients under antiviral treatment for chronic hepatitis B. Hepatol Int 2017; 11(5): 419–428
https://doi.org/10.1007/s12072-017-9803-4
pmid: 28639033
|
96 |
Podhorzer A, Dirchwolf M, Machicote A, Belen S, Montal S, Paz S, Fainboim H, Podesta L G, Fainboim L. The clinical features of patients with chronic hepatitis C virus infections are associated with killer cell immunoglobulin-like receptor genes and their expression on the surface of natural killer cells. Front Immunol 2018; 8:1912
https://doi.org/10.3389/fimmu.2017.01912
pmid: PMID:29354127
|
97 |
Tatsumi T, Takehara T. Impact of natural killer cells on chronic hepatitis C and hepatocellular carcinoma. Hepatol Res 2016; 46(5): 416–422
https://doi.org/10.1111/hepr.12619
pmid: PMID:26574168
|
98 |
Cerwenka A, Lanier LL. Natural killer cells, viruses and cancer. Nat Rev Immunol 2001; 1(1): 41–49
https://doi.org/10.1038/35095564
pmid: 11905813
|
99 |
Sun C, Sun H, Zhang C, Tian Z. NK cell receptor imbalance and NK cell dysfunction in HBV infection and hepatocellular carcinoma. Cell Mol Immunol 2015; 12(3): 292–302
https://doi.org/10.1038/cmi.2014.91
pmid: 25308752
|
100 |
Liu KJ, Wang CJ, Chang CJ, Hu HI, Hsu PJ, Wu YC, Bai CH, Sytwu HK, Yen BL. Surface expression of HLA-G is involved in mediating immunomodulatory effects of placenta-derived multipotent cells (PDMCs) towards natural killer lymphocytes. Cell Transplant 2011; 20(11-12): 1721–1730
https://doi.org/10.3727/096368911X580590
pmid: 21669042
|
101 |
Ju Y, Hou N, Meng J, Wang X, Zhang X, Zhao D, Liu Y, Zhu F, Zhang L, Sun W, Liang X, Gao L, Ma C. T cell immunoglobulin- and mucin-domain-containing molecule-3 (Tim-3) mediates natural killer cell suppression in chronic hepatitis B. J Hepatol 2010; 52(3): 322–329
https://doi.org/10.1016/j.jhep.2009.12.005
pmid: 20133006
|
102 |
Sun C, Fu B, Gao Y, Liao X, Sun R, Tian Z, Wei H. TGF-β1 down-regulation of NKG2D/DAP10 and 2B4/SAP expression on human NK cells contributes to HBV persistence. PLoS Pathog 2012; 8(3): e1002594
https://doi.org/10.1371/journal.ppat.1002594
pmid: 22438812
|
103 |
Li F, Wei H, Wei H, Gao Y, Xu L, Yin W, Sun R, Tian Z. 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(2): 392–401
https://doi.org/10.1053/j.gastro.2012.10.039
pmid: 23103614
|
104 |
Wang JM, Cheng YQ, Shi L, Ying RS, Wu XY, Li GY, Moorman JP, Yao ZQ. KLRG1 negatively regulates natural killer cell functions through the Akt pathway in individuals with chronic hepatitis C virus infection. J Virol 2013; 87(21): 11626–11636
https://doi.org/10.1128/JVI.01515-13
pmid: 23966413
|
105 |
Golden-Mason L, Waasdorp Hurtado CE, Cheng L, Rosen HR. Hepatitis C viral infection is associated with activated cytolytic natural killer cells expressing high levels of T cell immunoglobulin- and mucin-domain-containing molecule-3. Clin Immunol 2015; 158(1): 114–125
https://doi.org/10.1016/j.clim.2015.03.008
pmid: 25797693
|
106 |
Peppa D, Micco L, Javaid A, Kennedy PT, Schurich A, Dunn C, Pallant C, Ellis G, Khanna P, Dusheiko G, Gilson RJ, Maini MK. Blockade of immunosuppressive cytokines restores NK cell antiviral function in chronic hepatitis B virus infection. PLoS Pathog 2010; 6(12): e1001227
https://doi.org/10.1371/journal.ppat.1001227
pmid: 21187913
|
107 |
Sun C, Xu J, Huang Q, Huang M, Wen H, Zhang C, Wang J, Song J, Zheng M, Sun H, Wei H, Xiao W, Sun R, Tian Z. High NKG2A expression contributes to NK cell exhaustion and predicts a poor prognosis of patients with liver cancer. OncoImmunology 2017; 6(1): e1264562
https://doi.org/10.1080/2162402X.2016.1264562
pmid: 28197391
|
108 |
Waggoner SN, Taniguchi RT, Mathew PA, Kumar V, Welsh RM. 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
https://doi.org/10.1172/JCI41264
pmid: 20440077
|
109 |
Soderquest K, Walzer T, Zafirova B, Klavinskis LS, Polić B, Vivier E, Lord GM, Martín-Fontecha A. Cutting edge: CD8+ T cell priming in the absence of NK cells leads to enhanced memory responses. J Immunol 2011; 186(6): 3304–3308
https://doi.org/10.4049/jimmunol.1004122
pmid: 21307295
|
110 |
Lang PA, Lang KS, Xu HC, Grusdat M, Parish IA, Recher M, Elford AR, Dhanji S, Shaabani N, Tran CW, Dissanayake D, Rahbar R, Ghazarian M, Brüstle A, Fine J, Chen P, Weaver CT, Klose C, Diefenbach A, Häussinger D, Carlyle JR, Kaech SM, Mak TW, Ohashi PS. Natural killer cell activation enhances immune pathology and promotes chronic infection by limiting CD8+ T-cell immunity. Proc Natl Acad Sci USA 2012; 109(4): 1210–1215
https://doi.org/10.1073/pnas.1118834109
pmid: 22167808
|
111 |
Deniz G, Erten G, Kücüksezer UC, Kocacik D, Karagiannidis C, Aktas E, Akdis CA, Akdis M. Regulatory NK cells suppress antigen-specific T cell responses. J Immunol 2008; 180(2): 850–857
https://doi.org/10.4049/jimmunol.180.2.850
pmid: 18178824
|
112 |
Crouse J, Bedenikovic G, Wiesel M, Ibberson M, Xenarios I, Von Laer D, Kalinke U, Vivier E, Jonjic S, Oxenius A. Type I interferons protect T cells against NK cell attack mediated by the activating receptor NCR1. Immunity 2014; 40(6): 961–973
https://doi.org/10.1016/j.immuni.2014.05.003
pmid: 24909889
|
113 |
Xu HC, Grusdat M, Pandyra AA, Polz R, Huang J, Sharma P, Deenen R, Köhrer K, Rahbar R, Diefenbach A, Gibbert K, Löhning M, Höcker L, Waibler Z, Häussinger D, Mak TW, Ohashi PS, Lang KS, Lang PA. Type I interferon protects antiviral CD8+ T cells from NK cell cytotoxicity. Immunity 2014; 40(6): 949–960
https://doi.org/10.1016/j.immuni.2014.05.004
pmid: 24909887
|
114 |
De Rose V, Cappello P, Sorbello V, Ceccarini B, Gani F, Bosticardo M, Fassio S, Novelli F. IFN-γ 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
https://doi.org/10.1189/jlb.0503247
pmid: 15123769
|
115 |
Zhu J, Paul WE. CD4 T cells: fates, functions, and faults. Blood 2008; 112(5): 1557–1569
https://doi.org/10.1182/blood-2008-05-078154
pmid: 18725574
|
116 |
De Pelsmaeker S, Devriendt B, Leclercq G, Favoreel HW. Porcine NK cells display features associated with antigen-presenting cells. J Leukocyte Biol 2018; 103(1):129–140
https://doi.org/10.1002/JLB.4A0417-163RR PMID:29345060
|
117 |
Iraolagoitia XLR, Spallanzani RG, Torres NI, Araya RE, Ziblat A, Domaica CI, Sierra JM, Nunez SY, Secchiari F, Gajewski TF, Zwirner NW, Fuertes MB. NK cells restrain spontaneous antitumor CD8+ T cell priming through PD-1/PD-L1 interactions with dendritic cells. J Immunol 2016; 197(3):953–961
https://doi.org/10.4049/jimmunol.1502291
pmid: PMID:27342842
|
118 |
Meazza R, Falco M, Marcenaro S, Loiacono F, Canevali P, Bellora F, Tuberosa C, Locatelli F, Micalizzi C, Moretta A, Mingari MC, Moretta L, Arico M, Bottino C, Pende D. Inhibitory 2B4 contributes to NK cell education and immunological derangements in XLP1 patients. Eur J Immunol 2017; 47(6):1051–1061
https://doi.org/10.1002/eji.201646885
pmid: PMID:28386908
|
119 |
Cairo C, Surendran N, Harris KM, Mazan-Mamczarz K, Sakoda Y, Diaz-Mendez F, Tamada K, Gartenhaus RB, Mann DL, Pauza CD. Vγ2Vδ2 T-cell co-stimulation increases natural killer cell killing of monocyte-derived dendritic cells. Immunology 2015; 144(3): 422–430
https://doi.org/10.1111/imm.12386
|
120 |
Andrews DM, Estcourt MJ, Andoniou CE, Wikstrom ME, Khong A, Voigt V, Fleming P, Tabarias H, Hill GR, van der Most RG, Scalzo AA, Smyth MJ, Degli-Esposti MA. Innate immunity defines the capacity of antiviral T cells to limit persistent infection. J Exp Med 2010; 207(6): 1333–1343
https://doi.org/10.1084/jem.20091193
pmid: 20513749
|
121 |
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
https://doi.org/10.4049/jimmunol.1202448
pmid: 23241878
|
122 |
Schafer JL, Li H, Evans TI, Estes JD, Reeves RK. Accumulation of cytotoxic CD16+ NK cells in simian immunodeficiency virus-infected lymph nodes associated with in situ differentiation and functional anergy. J Virol 2015; 89(13): 6887–6894
https://doi.org/10.1128/JVI.00660-15
pmid: 25903330
|
123 |
Gill S, Vasey AE, De Souza A, Baker J, Smith AT, Kohrt HE, Florek M, Gibbs KD Jr, Tate K, Ritchie DS, Negrin RS. Rapid development of exhaustion and down-regulation of eomesodermin limit the antitumor activity of adoptively transferred murine natural killer cells. Blood 2012; 119(24): 5758–5768
https://doi.org/10.1182/blood-2012-03-415364
pmid: 22544698
|
124 |
Mamessier E, Sylvain A, Thibult ML, Houvenaeghel G, Jacquemier J, Castellano R, Gonçalves A, André P, Romagné F, Thibault G, Viens P, Birnbaum D, Bertucci F, Moretta A, Olive D. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J Clin Invest 2011; 121(9): 3609–3622
https://doi.org/10.1172/JCI45816
pmid: 21841316
|
125 |
da Silva IP, Gallois A, Jimenez-Baranda S, Khan S, Anderson AC, Kuchroo VK, Osman I, Bhardwaj N. Reversal of NK-cell exhaustion in advanced melanoma by Tim-3 blockade. Cancer Immunol Res 2014; 2(5): 410–422
https://doi.org/10.1158/2326-6066.CIR-13-0171
pmid: 24795354
|
126 |
Odorizzi PM, Pauken KE, Paley MA, Sharpe A, Wherry EJ. Genetic absence of PD-1 promotes accumulation of terminally differentiated exhausted CD8+ T cells. J Exp Med 2015; 212(7): 1125–1137
https://doi.org/10.1084/jem.20142237
pmid: 26034050
|
127 |
Lee SH, Kim KS, Fodil-Cornu N, Vidal SM, Biron CA. 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
https://doi.org/10.1084/jem.20082387
pmid: 19720840
|
128 |
Brooks DG, Trifilo MJ, Edelmann KH, Teyton L, McGavern DB, Oldstone MB. Interleukin-10 determines viral clearance or persistence in vivo. Nat Med 2006; 12(11): 1301–1309
https://doi.org/10.1038/nm1492
pmid: 17041596
|
129 |
Harmon C, Robinson MW, Fahey R, Whelan S, Houlihan DD, Geoghegan J, O’Farrelly C. Tissue-resident Eomes(hi) T-bet(lo) CD56(bright) NK cells with reduced proinflammatory potential are enriched in the adult human liver. Eur J Immunol 2016; 46(9): 2111–2120
https://doi.org/10.1002/eji.201646559
pmid: 27485474
|
130 |
Stegmann KA, Robertson F, Hansi N, Gill U, Pallant C, Christophides T, Pallett LJ, Peppa D, Dunn C, Fusai G, Male V, Davidson BR, Kennedy P, Maini MK. CXCR6 marks a novel subset of T-bet(lo)Eomes(hi) natural killer cells residing in human liver. Sci Rep-Uk 2016; 6:26157
https://doi.org/DOI: 10.1038/srep26157
|
131 |
Hudspeth K, Donadon M, Cimino M, Pontarini E, Tentorio P, Preti M, Hong M, Bertoletti A, Bicciato S, Invernizzi P, Lugli E, Torzilli G, Gershwin ME, Mavilio D. Human liver-resident CD56(bright)/CD16(neg) NK cells are retained within hepatic sinusoids via the engagement of CCR5 and CXCR6 pathways. J Autoimmun 2016; 66: 40–50
https://doi.org/10.1016/j.jaut.2015.08.011
pmid: 26330348
|
132 |
Cuff AO, Robertson FP, Stegmann KA, Pallett LJ, Maini MK, Davidson BR, Male V. Eomeshi NK cells in human liver are long-lived and do not recirculate but can be replenished from the circulation. J Immunol 2016; 197(11): 4283–4291
https://doi.org/10.4049/jimmunol.1601424
pmid: 27798170
|
133 |
Lugli E, Hudspeth K, Roberto A, Mavilio D. Tissue-resident and memory properties of human T-cell and NK-cell subsets. Eur J Immunol 2016; 46(8): 1809–1817
https://doi.org/10.1002/eji.201545702
pmid: 27431095
|
134 |
Paust S, Gill HS, Wang BZ, Flynn MP, Moseman EA, Senman B, Szczepanik M, Telenti A, Askenase PW, Compans RW, von Andrian UH. Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat Immunol 2010; 11(12): 1127–1135
https://doi.org/10.1038/ni.1953
pmid: 20972432
|
135 |
Sojka DK, Plougastel-Douglas B, Yang L, Pak-Wittel MA, Artyomov MN, Ivanova Y, Zhong C, Chase JM, Rothman PB, Yu J, Riley JK, Zhu J, Tian Z, Yokoyama WM. Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells. eLife 2014; 3: e01659
https://doi.org/10.7554/eLife.01659
pmid: 24714492
|
136 |
Yu M, Li ZH. Natural killer cells in hepatocellular carcinoma: current status and perspectives for future immunotherapeutic approaches. Front Med 2017; 11(4): 509–521
https://doi.org/10.1007/s11684-017-0546-3
pmid: PMID:28780700
|
137 |
BoudreauJE, Hsu KC. Natural killer cell education and the response to infection and cancer therapy: stay tuned. Trends Immunol 2018 Jan 31. pii: S1471-4906(17)30230-2. [Epub ahead of print]
https://doi.org/10.1016/j.it.2017.12.001
pmid: 29397297
|
138 |
Cheng M, Chen Y, Xiao W, Sun R, Tian Z. NK cell-based immunotherapy for malignant diseases. Cell Mol Immunol 2013; 10(3): 230–252
https://doi.org/10.1038/cmi.2013.10
pmid: 23604045
|
139 |
Serti E, Park H, Keane M, O’Keefe AC, Rivera E, Liang TJ, Ghany M, Rehermann B. Rapid decrease in hepatitis C viremia by direct acting antivirals improves the natural killer cell response to IFNα. Gut 2017; 66(4): 724–735
https://doi.org/10.1136/gutjnl-2015-310033
pmid: 26733671
|
140 |
Textor S, Bossler F, Henrich KO, Gartlgruber M, Pollmann J, Fiegler N, Arnold A, Westermann F, Waldburger N, Breuhahn K, Golfier S, Witzens-Harig M, Cerwenka A. The proto-oncogene Myc drives expression of the NK cell-activating NKp30 ligand B7-H6 in tumor cells. OncoImmunology 2016; 5(7): e1116674
https://doi.org/10.1080/2162402X.2015.1116674
pmid: 27622013
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|