Crosstalk between NK cells and hepatic stellate cells in liver fibrosis (Review)
- Authors:
- Yang Zhang
- Yuan Wu
- Wenjuan Shen
- Bingyu Wang
- Xingxing Yuan
-
Affiliations: Department of Gastroenterology, The First Affiliated Hospital of Heilongjiang University of Traditional Chinese Medicine, Harbin, Heilongjiang 150001, P.R. China, The Graduate School, Heilongjiang University of Traditional Chinese Medicine, Harbin, Heilongjiang 150001, P.R. China, Department of Gynaecology, The First Affiliated Hospital of Heilongjiang University of Traditional Chinese Medicine, Harbin, Heilongjiang 150001, P.R. China, Department of Gastroenterology, Heilongjiang Academy of Traditional Chinese Medicine, Harbin, Heilongjiang 150001, P.R. China - Published online on: May 3, 2022 https://doi.org/10.3892/mmr.2022.12724
- Article Number: 208
-
Copyright: © Zhang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
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Abstract
 |
|
Gan J, Mao XR, Zheng SJ and Li JF: Invariant natural killer T cells: Not to be ignored in liver disease. J Dig Dis. 22:136–142. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Yan Y, Zeng J, Xing L and Li C: Extra- and intra-cellular mechanisms of hepatic stellate cell activation. Biomedicines. 9:10142021. View Article : Google Scholar : PubMed/NCBI | |
|
Highton AJ, Schuster IS, Degli-Esposti MA and Altfeld M: The role of natural killer cells in liver inflammation. Semin Immunopathol. 43:519–533. 2021. View Article : Google Scholar | |
|
St-Pierre F, Bhatia S and Chandra S: Harnessing natural killer cells in cancer immunotherapy: A review of mechanisms and novel therapies. Cancers (Basel). 13:19882021. View Article : Google Scholar : PubMed/NCBI | |
|
Zheng M, Sun H and Tian Z: Natural killer cells in liver diseases. Front Med. 12:269–279. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Gao B, Radaeva S and Jeong WI: Activation of natural killer cells inhibits liver fibrosis: A novel strategy to treat liver fibrosis. Expert Rev Gastroenterol Hepatol. 1:173–180. 2007. View Article : Google Scholar | |
|
Schuppan D, Ashfaq-Khan M, Yang AT and Kim YO: Liver fibrosis: Direct antifibrotic agents and targeted therapies. Matrix Biol. 68-69:435–451. 2018. View Article : Google Scholar | |
|
Jeong WI, Park O, Suh YG, Byun JS, Park SY, Choi E, Kim JK, Ko H, Wang H, Miller AM and Gao B: Suppression of innate immunity (natural killer cell/interferon-gamma) in the advanced stages of liver fibrosis in mice. Hepatology. 53:1342–1351. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Roehlen N, Crouchet E and Baumert TF: Liver fibrosis: Mechanistic concepts and therapeutic perspectives. Cells. 9:8752020. View Article : Google Scholar | |
|
Wree A, McGeough MD, Inzaugarat ME, Eguchi A, Schuster S, Johnson CD, Peña CA, Geisler LJ, Papouchado BG, Hoffman HM and Feldstein AE: NLRP3 inflammasome driven liver injury and fibrosis: Roles of IL-17 and TNF in mice. Hepatology. 67:736–749. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Wan M, Han J, Ding L, Hu F and Gao P: Novel immune subsets and related cytokines: Emerging players in the progression of liver fibrosis. Front Med. 8:6048942021. View Article : Google Scholar | |
|
Jiang JX, Mikami K, Venugopal S, Li Y and Török NJ: Apoptotic body engulfment by hepatic stellate cells promotes their survival by the JAK/STAT and Akt/NF-kappaB-dependent pathways. J Hepatol. 51:139–148. 2009. View Article : Google Scholar | |
|
Tanwar S, Rhodes F, Srivastava A, Trembling PM and Rosenberg WM: Inflammation and fibrosis in chronic liver diseases including non-alcoholic fatty liver disease and hepatitis C. World J Gastroenterol. 26:109–133. 2020. View Article : Google Scholar | |
|
Luo DZ, Vermijlen D, Ahishali B, Triantis V, Plakoutsi G, Braet F, Vanderkerken K and Wisse E: On the cell biology of pit cells, the liver-specific NK cells. World J Gastroenterol. 6:1–11. 2000. View Article : Google Scholar | |
|
Wisse E, van't Noordende JM, van der Meulen J and Daems WT: The pit cell: Description of a new type of cell occurring in rat liver sinusoids and peripheral blood. Cell Tissue Res. 173:423–435. 1976. View Article : Google Scholar : PubMed/NCBI | |
|
Tang L, Peng H, Zhou J, Chen Y, Wei H, Sun R, Yokoyama WM and Tian Z: Differential phenotypic and functional properties of liver-resident NK cells and mucosal ILC1s. J Autoimmun. 67:29–35. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Wang Y and Zhang C: The Roles of Liver-resident lymphocytes in liver diseases. Front Immunol. 10:15822019. View Article : Google Scholar | |
|
Lunemann S, Martrus G, Goebels H, Kautz T, Langeneckert A, Salzberger W, Koch M, J Bunders M, Nashan B, van Gisbergen KPJM and Altfeld M: Hobit expression by a subset of human liver-resident CD56bright Natural Killer cells. Sci Rep. 7:66762017. View Article : Google Scholar : PubMed/NCBI | |
|
Hudspeth K, Donadon M, Cimino M, Pontarini E, Tentorio P, Preti M, Hong M, Bertoletti A, Bicciato S, Invernizzi P, et al: Human liver-resident CD56(bright)/CD16(neg) NK cells are retained within hepatic sinusoids via the engagement of CCR5 and CXCR6 pathways. J Autoimmun. 66:40–50. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang C, Hu Y, Xiao W and Tian Z: Chimeric antigen receptor- and natural killer cell receptor-engineered innate killer cells in cancer immunotherapy. Cell Mol Immunol. 18:2083–2100. 2021. View Article : Google Scholar | |
|
Obajdin J, Davies DM and Maher J: Engineering of chimeric natural killer cell receptors to develop precision adoptive immunotherapies for cancer. Clin Exp Immunol. 202:11–27. 2020. View Article : Google Scholar | |
|
Vrazo AC, Hontz AE, Figueira SK, Butler BL, Ferrell JM, Binkowski BF, Li J and Risma KA: Live cell evaluation of granzyme delivery and death receptor signaling in tumor cells targeted by human natural killer cells. Blood. 126:e1–e10. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Saparbay J, Tanaka Y, Tanimine N, Ohira M and Ohdan H: Everolimus enhances TRAIL-mediated anti-tumor activity of liver resident natural killer cells in mice. Transpl Int. 33:229–243. 2020. View Article : Google Scholar | |
|
Choi WM, Ryu T, Lee JH, Shim YR, Kim MH, Kim HH, Kim YE, Yang K, Kim K, Choi SE, et al: Metabotropic glutamate receptor 5 in natural killer cells attenuates liver fibrosis by exerting cytotoxicity to activated stellate cells. Hepatology. 74:2170–2185. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Jin H, Jia Y, Yao Z, Huang J, Hao M, Yao S, Lian N, Zhang F, Zhang C, Chen X, et al: Hepatic stellate cell interferes with NK cell regulation of fibrogenesis via curcumin induced senescence of hepatic stellate cell. Cell Signal. 33:79–85. 2017. View Article : Google Scholar | |
|
Gur C, Doron S, Kfir-Erenfeld S, Horwitz E, Abu-Tair L, Safadi R and Mandelboim O: NKp46-mediated killing of human and mouse hepatic stellate cells attenuates liver fibrosis. Gut. 61:885–893. 2012. View Article : Google Scholar | |
|
Li W, Jiang Y, Wang X, Jin J, Qi Y, Chi X, Zhang H, Feng X and Niu J: Natural killer p46 controls hepatitis B virus replication and modulates liver inflammation. PLoS One. 10:e01358742015. View Article : Google Scholar : PubMed/NCBI | |
|
Nattermann J, Feldmann G, Ahlenstiel G, Langhans B, Sauerbruch T and Spengler U: Surface expression and cytolytic function of natural killer cell receptors is altered in chronic hepatitis C. Gut. 55:869–877. 2006. View Article : Google Scholar | |
|
Nel I, Lucar O, Petitdemange C, Béziat V, Lapalus M, Bédossa P, Debré P, Asselah T, Marcellin P and Vieillard V: Accumulation of intrahepatic TNF-α-producing NKp44+ NK cells correlates with liver fibrosis and viral load in chronic HCV infection. Medicine (Baltimore). 95:e36782016. View Article : Google Scholar : PubMed/NCBI | |
|
Wijaya RS, Read SA, Schibeci S, Eslam M, Azardaryany MK, El-Khobar K, van der Poorten D, Lin R, Yuen L, Lam V, et al: KLRG1+ natural killer cells exert a novel antifibrotic function in chronic hepatitis B. J Hepatol. 71:252–264. 2019. View Article : Google Scholar | |
|
Abu-Tair L, Axelrod JH, Doron S, Ovadya Y, Krizhanovsky V, Galun E, Amer J and Safadi R: Natural killer cell-dependent anti-fibrotic pathway in liver injury via Toll-like receptor-9. PLoS One. 8:e825712013. View Article : Google Scholar : PubMed/NCBI | |
|
Cai X, Wang J, Wang J, Zhou Q, Yang B, He Q and Weng Q: Intercellular crosstalk of hepatic stellate cells in liver fibrosis: New insights into therapy. Pharmacol Res. 155:1047202020. View Article : Google Scholar : PubMed/NCBI | |
|
Muhanna N, Abu Tair L, Doron S, Amer J, Azzeh M, Mahamid M, Friedman S and Safadi R: Amelioration of hepatic fibrosis by NK cell activation. Gut. 60:90–98. 2011. View Article : Google Scholar | |
|
Schölzel K, Schildberg FA, Welz M, Börner C, Geiger S, Kurts C, Heikenwälder M, Knolle PA and Wohlleber D: Transfer of MHC-class-I molecules among liver sinusoidal cells facilitates hepatic immune surveillance. J Hepatol. 61:600–608. 2014. View Article : Google Scholar | |
|
Arriola Benitez PC, Pesce Viglietti AI, Elizalde MM, Giambartolomei GH, Quarleri JF and Delpino MV: Hepatic stellate cells and hepatocytes as liver Antigen-presenting cells during B. abortus Infection. Pathogens. 9:5272020. View Article : Google Scholar | |
|
Chen Y, Lu D, Churov A and Fu R: Research progress on NK cell receptors and their signaling pathways. Mediators Inflamm. 2020:64370572020. View Article : Google Scholar : PubMed/NCBI | |
|
Radaeva S, Wang L, Radaev S, Jeong WI, Park O and Gao B: Retinoic acid signaling sensitizes hepatic stellate cells to NK cell killing via upregulation of NK cell activating ligand RAE1. Am J Physiol Gastrointest Liver Physiol. 293:G809–G816. 2007. View Article : Google Scholar | |
|
Park O, Jeong WI, Wang L, Wang H, Lian ZX, Gershwin ME and Gao B: Diverse roles of invariant natural killer T cells in liver injury and fibrosis induced by carbon tetrachloride. Hepatology. 49:1683–1694. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Fugier E, Marche H, Thelu MA, Macek Jílková Z, Van Campenhout N, Dufeu-Duchesne T, Leroy V, Zarski JP, Sturm N, Marche PN and Jouvin-Marche E: Functions of liver natural killer cells are dependent on the severity of liver inflammation and fibrosis in chronic hepatitis C. PLoS One. 9:e956142014. View Article : Google Scholar : PubMed/NCBI | |
|
Radaeva S, Sun R, Jaruga B, Nguyen VT, Tian Z and 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. 130:435–452. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Jeong WI, Park O, Radaeva S and Gao B: STAT1 inhibits liver fibrosis in mice by inhibiting stellate cell proliferation and stimulating NK cell cytotoxicity. Hepatology. 44:1441–1451. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Ma PF, Gao CC, Yi J, Zhao JL, Liang SQ, Zhao Y, Ye YC, Bai J, Zheng QJ, Dou KF, et al: Cytotherapy with M1-polarized macrophages ameliorates liver fibrosis by modulating immune microenvironment in mice. J Hepatol. 67:770–779. 2017. View Article : Google Scholar | |
|
Glassner A, Eisenhardt M, Kramer B, Körner C, Coenen M, Sauerbruch T, Spengler U and 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. 92:967–977. 2012. View Article : Google Scholar | |
|
Oh Y, Park O, Swierczewska M, Hamilton JP, Park JS, Kim TH, Lim SM, Eom H, Jo DG, Lee CE, et al: Systemic PEGylated TRAIL treatment ameliorates liver cirrhosis in rats by eliminating activated hepatic stellate cells. Hepatology. 64:209–223. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Rockey DC, Maher JJ, Jarnagin WR, Gabbiani G and Friedman SL: Inhibition of rat hepatic lipocyte activation in culture by interferon-gamma. Hepatology. 16:776–784. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Hou X, Yu F, Man S, Huang D, Zhang Y, Liu M, Ren C and Shen J: Negative regulation of Schistosoma japonicum egg-induced liver fibrosis by natural killer cells. PLoS Negl Trop Dis. 6:e14562012. View Article : Google Scholar : PubMed/NCBI | |
|
Parola M and Pinzani M: Liver fibrosis: Pathophysiology, pathogenetic targets and clinical issues. Mol Aspects Med. 65:37–55. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang M, Serna-Salas S, Damba T, Borghesan M, Demaria M and Moshage H: Hepatic stellate cell senescence in liver fibrosis: Characteristics, mechanisms and perspectives. Mech Ageing Dev. 199:1115722021. View Article : Google Scholar : PubMed/NCBI | |
|
Fan Y, Zhang W, Wei H, Sun R, Tian Z and Chen Y: Hepatic NK cells attenuate fibrosis progression of non-alcoholic steatohepatitis in dependent of CXCL10-mediated recruitment. Liver Int. 40:598–608. 2020. View Article : Google Scholar | |
|
Wu Y, Min J, Ge C, Shu J, Tian D, Yuan Y and Zhou D: Interleukin 22 in liver injury, inflammation and cancer. Int J Biol Sci. 16:2405–2413. 2020. View Article : Google Scholar | |
|
Huang YH, Chen MH, Guo QL, Chen YX, Zhang LJ, Chen ZX and Wang XZ: Interleukin-10 promotes primary rat hepatic stellate cell senescence by upregulating the expression levels of p53 and p21. Mol Med Rep. 17:5700–5707. 2018.PubMed/NCBI | |
|
Huang YH, Chen MH, Guo QL, Chen ZX, Chen QD and Wang XZ: Interleukin-10 induces senescence of activated hepatic stellate cells via STAT3-p53 pathway to attenuate liver fibrosis. Cell Signal. 66:1094452020. View Article : Google Scholar | |
|
Kong X, Feng D, Wang H, Hong F, Bertola A, Wang FS and Gao B: Interleukin-22 induces hepatic stellate cell senescence and restricts liver fibrosis in mice. Hepatology. 56:1150–1159. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Chen J, Xu T, Zhu D, Wang J, Huang C, Lyu L, Hu B, Sun W and Duan Y: Egg antigen p40 of Schistosoma japonicum promotes senescence in activated hepatic stellate cells by activation of the STAT3/p53/p21 pathway. Cell Death Dis. 7:e23152016. View Article : Google Scholar : PubMed/NCBI | |
|
Jin H, Lian N, Zhang F, Chen L, Chen Q, Lu C, Bian M, Shao J, Wu L and Zheng S: Activation of PPARγ/P53 signaling is required for curcumin to induce hepatic stellate cell senescence. Cell Death Dis. 7:e21892016. View Article : Google Scholar : PubMed/NCBI | |
|
Sagiv A, Biran A, Yon M, Simon J, Lowe SW and Krizhanovsky V: Granule exocytosis mediates immune surveillance of senescent cells. Oncogene. 32:1971–1977. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Muhanna N, Doron S, Wald O, Horani A, Eid A, Pappo O, Friedman SL and Safadi R: Activation of hepatic stellate cells after phagocytosis of lymphocytes: A novel pathway of fibrogenesis. Hepatology. 48:963–977. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Shi J, Zhao J, Zhang X, Cheng Y, Hu J, Li Y, Zhao X, Shang Q, Sun Y, Tu B, et al: Activated hepatic stellate cells impair NK cell anti-fibrosis capacity through a TGF-β-dependent emperipolesis in HBV cirrhotic patients. Sci Rep. 7:445442017. View Article : Google Scholar : PubMed/NCBI | |
|
Yu J, Wei M, Becknell B, Trotta R, Liu S, Boyd Z, Jaung MS, Blaser BW, Sun J, Benson DM Jr, et al: Pro- and antiinflammatory cytokine signaling: Reciprocal antagonism regulates interferon-gamma production by human natural killer cells. Immunity. 24:575–590. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Jeong WI, Park O and Gao B: Abrogation of the antifibrotic effects of natural killer cells/interferon-gamma contributes to alcohol acceleration of liver fibrosis. Gastroenterology. 134:248–258. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Peppa D, Micco L, Javaid A, Kennedy PT, Schurich A, Dunn C, Pallant C, Ellis G, Khanna P, Dusheiko G, et al: Blockade of immunosuppressive cytokines restores NK cell antiviral function in chronic hepatitis B virus infection. PLoS Pathog. 6:e10012272010. View Article : Google Scholar : PubMed/NCBI | |
|
Dasgupta S, Bhattacharya-Chatterjee M, O'Malley BW Jr and Chatterjee SK: Inhibition of NK cell activity through TGF-beta 1 by down-regulation of NKG2D in a murine model of head and neck cancer. J Immunol. 175:5541–5550. 2005. View Article : Google Scholar | |
|
Sene D, Levasseur F, Abel M, Lambert M, Camous X, Hernandez C, Pène V, Rosenberg AR, Jouvin-Marche E, Marche PN, et al: Hepatitis C virus (HCV) evades NKG2D-dependent NK cell responses through NS5A-mediated imbalance of inflammatory cytokines. PLoS Pathog. 6:e10011842010. View Article : Google Scholar : PubMed/NCBI | |
|
Sun C, Fu B, Gao Y, Liao X, Sun R, Tian Z and Wei H: TGF-β1 down-regulation of NKG2D/DAP10 and 2B4/SAP expression on human NK cells contributes to HBV persistence. PLoS Pathog. 8:e10025942012. View Article : Google Scholar : PubMed/NCBI | |
|
Peng Y, Huang K, Shen L, Tao YY and Liu CH: Cultured mycelium cordyceps sinensis alleviates CCl4-induced liver inflammation and fibrosis in mice by activating hepatic natural killer cells. Acta Pharmacol Sin. 37:204–216. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Peng Y, Yang T, Huang K, Shen L, Tao Y and Liu C: Salvia miltiorrhiza ameliorates liver fibrosis by activating hepatic natural killer cells in vivo and in vitro. Front Pharmacol. 9:7622018. View Article : Google Scholar | |
|
Xia Y, Yu B, Ma C, Tu Y, Zhai L, Yang Y, Liu D, Liu Y, Wu H, Dan H and You P: Yu Gan Long reduces rat liver fibrosis by blocking TGF-β 1/Smad pathway and modulating the immunity. Biomed Pharmacother. 106:1332–1338. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
van Dijk F, Olinga P, Poelstra K and Beljaars L: Targeted therapies in liver fibrosis: Combining the best parts of Platelet-Derived growth factor BB and interferon gamma. Front Med (Lausanne). 2:722015.PubMed/NCBI | |
|
Polo ML, Ghiglione YA, Salido JP, Urioste A, Poblete G, Sisto AE, Martinez A, Rolón MJ, Ojeda DS, Cahn PE, et al: Liver cirrhosis in HIV/HCV-coinfected individuals is related to NK cell dysfunction and exhaustion, but not to an impaired NK cell modulation by CD4+ T-cells. J Int AIDS Soc. 22:e253752019. View Article : Google Scholar | |
|
Li Y, Wang JJ, Gao S, Liu Q, Bai J, Zhao XQ, Hao YH, Ding HH, Zhu F, Yang DL and Zhao XP: Decreased peripheral natural killer cells activity in the immune activated stage of chronic hepatitis B. PLoS One. 9:e869272014. View Article : Google Scholar : PubMed/NCBI | |
|
Han QJ, Mu YL, Zhao HJ, Zhao RR, Guo QJ, Su YH and Zhang J: Fasudil prevents liver fibrosis via activating natural killer cells and suppressing hepatic stellate cells. World J Gastroenterol. 27:3581–3594. 2021. View Article : Google Scholar |
