记忆性ILCs研究进展
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摘要
近十年来,固有淋巴细胞(ILCs)发育和功能研究进展迅速,目前已形成了包括NK细胞、ILC1s、ILC2s、ILC3s、LTi细胞、ILCregs等构成的完整体系。然而,越来越多的证据表明ILCs同样也具有适应性免疫细胞属性,能够介导长期免疫记忆反应。NK细胞能够记忆半抗原、MCMV病毒抗原、细胞因子IL-12/15/18; ILC1s能够记忆半抗原; ILC2s能够记忆细胞因子刺激。这些进展让国内外学者对于ILCs有了新的认识,记忆性ILCs已然成为新兴的研究领域。此外,基于记忆性ILCs的疫苗免疫以及肿瘤免疫治疗均取得了突破。本文中,我们综述了记忆性ILCs的研究进展,比较了其与记忆性T细胞的共同特征及区别之处,还探讨了记忆性ILCs的应用价值,并提出记忆性ILCs的研究体系。
Over the past decade,development and functions of innate lymphoid cells( ILCs) have been well documented. ILCs,including NK cells,ILC1s,ILC2s,ILC3s,lymphoid tissue-inducer( LTi) cells and ILCregs,compose the first line of immune defense against pathogens and tumors. However,recent studies have revealed the adaptive features of ILCs; for example,NK cells recalling haptens,MCMV and cytokines,ILC1s recalling haptens,and ILC2s recalling cytokines. ILC memory has become an emerging field. These new findings prompt us to rethink the biology of ILCs. Inspiringly,tumor immunotherapies based on memory NK cells have been shown to confer benefits in tumor control. In this review,we aim to update the knowledge of memory ILCs and advance a comprehensive framework of the ILCs memory system.
Over the past decade,development and functions of innate lymphoid cells( ILCs) have been well documented. ILCs,including NK cells,ILC1s,ILC2s,ILC3s,lymphoid tissue-inducer( LTi) cells and ILCregs,compose the first line of immune defense against pathogens and tumors. However,recent studies have revealed the adaptive features of ILCs; for example,NK cells recalling haptens,MCMV and cytokines,ILC1s recalling haptens,and ILC2s recalling cytokines. ILC memory has become an emerging field. These new findings prompt us to rethink the biology of ILCs. Inspiringly,tumor immunotherapies based on memory NK cells have been shown to confer benefits in tumor control. In this review,we aim to update the knowledge of memory ILCs and advance a comprehensive framework of the ILCs memory system.
引文
[1]Spits H,Artis D,Colonna M,et al.Innate lymphoid cells--a proposal for uniform nomenclature[J].Nat Rev Immunol,2013,13(2):145-149.
[2]Artis D,Spits H.The biology of innate lymphoid cells[J].Nature,2015,517(7534):293-301.
[3]Eberl G,Colonna M,Di Santo JP,et al.Innate lymphoid cells:a new paradigm in immunology[J].Science,2015,348(6237):aaa6566.
[4]Vivier E,Artis D,Colonna M,et al.Innate lymphoid cells:10 years on[J].Cell,2018,174(5):1054-1066.
[5]Fuchs A,Vermi W,Lee JS,et al.Intraepithelial Type 1 innate lymphoid cells are a unique subset of IL-12-and IL-15-responsive IFN-gamma-producing cells[J].Immunity,2013,38(4):769-781.
[6]Weizman OE,Adams NM,Schuster IS,et al.ILC1 confer early host protection at initial sites of viral infection[J].Cell,2017,171(4):795-808 e12.
[7]Moro K,Yamada T,Tanabe M,et al.Innate production of TH2 cytokines by adipose tissue-associated c-Kit+Sca-1+lymphoid cells[J].Nature,2009,463:540.
[8]Neill DR,Wong SH,Bellosi A,et al.Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity[J].Nature,2010,464:1367.
[9]Luci C,Reynders A,Ivanov II,et al.Influence of the transcription factor RORγt on the development of NKp46+cell populations in gut and skin[J].Nature Immunol,2008,10:75.
[10]Satoh-Takayama N,Vosshenrich CA,Lesjean-Pottier S,et al.Microbial flora drives interleukin 22 production in intestinal NKp46+cells that provide innate mucosal immune defense[J].Immunity,2008,29(6):958-970.
[11]Mebius RE,Rennert P,Weissman IL.Developing lymph nodes collect CD4+CD3-LTβ+cells that can differentiate to APC,NKcells,and follicular cells but not T or B cells[J].Immunity,1997,7(4):493-504.
[12]Wang S,Xia P,Chen Y,et al.Regulatory innate lymphoid cells control innate intestinal inflammation[J].Cell,2017,171(1):201-216.
[13]O'leary JG,Goodarzi M,Drayton DL,et al.T cell-and B cell-independent adaptive immunity mediated by natural killer cells[J].Nat Immunol,2006,7(5):507-516.
[14]Sun JC,Beilke JN,Lanier LL.Adaptive immune features of natural killer cells[J].Nature,2009,457(7229):557-561.
[15]Cooper MA,Elliott JM,Keyel PA,et al.Cytokine-induced memory-like natural killer cells[J].Proc Natl Acad Sci U S A,2009,106(6):1915-1919.
[16]Reeves RK,Li H,Jost S,et al.Antigen-specific NK cell memory in rhesus macaques[J].Nat Immunol,2015,16(9):927-932.
[17]Bjorkstrom NK,Lindgren T,Stoltz M,et al.Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus[J].J Exp Med,2011,208(1):13-21.
[18]Lopez-Verges S,Milush JM,Schwartz BS,et al.Expansion of a unique CD57(+)NKG2Chi natural killer cell subset during acute human cytomegalovirus infection[J].Proc Natl Acad Sci U S A,2011,108(36):14725-14732.
[19]Lee J,Zhang T,Hwang I,et al.Epigenetic modification and antibody-dependent expansion of memory-like NK cells in human cytomegalovirus-infected individuals[J].Immunity,2015,42(3):431-442.
[20]Martinez-Gonzalez I,Matha L,Steer CA,et al.Allergen-experienced group 2 innate lymphoid cells acquire memory-like properties and enhance allergic lung inflammation[J].Immunity,2016,45(1):198-208.
[21]Wang X,Peng H,Cong J,et al.Memory formation and long-term maintenance of IL-7Ralpha(+)ILC1s via a lymph node-liver axis[J].Nat Commun,2018,9(1):4854.
[22]Paust S,Gill HS,Wang BZ,et al.Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses[J].Nat Immunol,2010,11(12):1127-1135.
[23]Peng H,Jiang X,Chen Y,et al.Liver-resident NK cells confer adaptive immunity in skin-contact inflammation[J].J Clin Invest,2013,123(4):1444-1456.
[24]Peng H,Wisse E,Tian Z.Liver natural killer cells:subsets and roles in liver immunity[J].Cell Mol Immunol,2016,13(3):328-336.
[25]Peng H,Sun R.Liver-resident NK cells and their potential functions[J].Cell Mol Immunol,2017,14:890.
[26]Zhang LH,Shin JH,Haggadone MD,et al.The aryl hydrocarbon receptor is required for the maintenance of liver-resident natural killer cells[J].J Exp Med,2016,213(11):2249-2257.
[27]Van Den Boorn JG,Jakobs C,Hagen C,et al.Inflammasome-dependent induction of adaptive NK cell memory[J].Immunity,2016,44(6):1406-1421.
[28]Wight A,Mahmoud AB,Scur M,et al.Critical role for the Ly49family of class I MHC receptors in adaptive natural killer cell responses[J].Proc Natl Acad Sci U S A,2018,115(45):11579-11584.
[29]O'sullivan TE,Sun JC,Lanier LL.Natural killer cell memory[J].Immunity,2015,43(4):634-645.
[30]Nabekura T,Lanier LL.Activating receptors for self-MHC class Ienhance effector functions and memory differentiation of NK cells during mouse cytomegalovirus infection[J].Immunity,2016,45(1):74-82.
[31]Nabekura T,Lanier LL.Antigen-specific expansion and differentiation of natural killer cells by alloantigen stimulation[J].J Exp Med,2014,211(12):2455-2465.
[32]Nabekura T,Kanaya M,Shibuya A,et al.Costimulatory molecule DNAM-1 is essential for optimal differentiation of memory natural killer cells during mouse cytomegalovirus infection[J].Immunity,2014,40(2):225-234.
[33]Madera S,Rapp M,Firth MA,et al.Type I IFN promotes NK cell expansion during viral infection by protecting NK cells against fratricide[J].J Exp Med,2016,213(2):225-233.
[34]Nabekura T,Girard JP,Lanier LL.IL-33 receptor ST2 amplifies the expansion of NK cells and enhances host defense during mouse cytomegalovirus infection[J].J Immunol,2015,194(12):5948-5952.
[35]Sun JC,Madera S,Bezman NA,et al.Proinflammatory cytokine signaling required for the generation of natural killer cell memory[J].J Exp Med,2012,209(5):947-954.
[36]Madera S,Sun JC.Cutting edge:stage-specific requirement of IL-18 for antiviral NK cell expansion[J].J Immunol,2015,194(4):1408-1412.
[37]Beaulieu AM,Zawislak CL,Nakayama T,et al.The transcription factor Zbtb32 controls the proliferative burst of virus-specific natural killer cells responding to infection[J].Nat Immunol,2014,15(6):546-553.
[38]Rapp M,Lau CM,Adams NM,et al.Core-binding factor β and Runx transcription factors promote adaptive natural killer cell responses[J].Science Immunology,2017,2(18):eaan3796.
[39]Geary CD,Krishna C,Lau CM,et al.Non-redundant ISGF3 components promote NK cell survival in an Auto-regulatory Manner during viral infection[J].Cell Reports,2018,24(8):1949-1957.
[40]Min-Oo G,Bezman NA,Madera S,et al.Proapoptotic Bim regulates antigen-specific NK cell contraction and the generation of the memory NK cell pool after cytomegalovirus infection[J].JExp Med,2014,211(7):1289-1296.
[41]O'sullivan TE,Johnson LR,Kang HH,et al.BNIP3-and BNIP3L-mediated mitophagy promotes the generation of natural killer cell memory[J].Immunity,2015,43(2):331-342.
[42]Firth M A,Madera S,Beaulieu A M,et al.Nfil3-independent lineage maintenance and antiviral response of natural killer cells[J].J Exp Med,2013,210(13):2981-2990.
[43]Lau CM,Adams NM,Geary CD,et al.Epigenetic control of innate and adaptive immune memory[J].Nat Immunol,2018,19(9):963-972.
[44]Bantug GR,Galluzzi L,Kroemer G,et al.The spectrum of T cell metabolism in health and disease[J].Nat Rev Immunol,2018,18(1):19-34.
[45]Cui G,Staron MM,Gray SM,et al.IL-7-induced glycerol transport and TAG synthesis promotes memory CD8+T cell longevity[J].Cell,2015,161(4):750-761.
[46]Cong J,Wang X,Zheng X,et al.Dysfunction of natural killer cells by FBP1-induced inhibition of glycolysis during lung cancer progression[J].Cell Metab,2018,28(2):243-255.
[47]Cichocki F,Wu CY,Zhang B,et al.ARID5B regulates metabolic programming in human adaptive NK cells[J].J Exp Med,2018,215(9):2379-2395.
[48]Beziat V,Dalgard O,Asselah T,et al.CMV drives clonal expansion of NKG2C+NK cells expressing self-specific KIRs in chronic hepatitis patients[J].Eur J Immunol,2012,42(2):447-457.
[49]Ram DR,Manickam C,Hueber B,et al.Tracking KLRC2(NKG2C)+memory-like NK cells in SIV+and rh CMV+rhesus macaques[J].PLo S Pathog,2018,14(5):e1007104.
[50]Hammer Q,Ruckert T,Borst EM,et al.Peptide-specific recognition of human cytomegalovirus strains controls adaptive natural killer cells[J].Nat Immunol,2018,19(5):453-463.
[51]Rolle A,Pollmann J,Ewen EM,et al.IL-12-producing monocytes and HLA-E control HCMV-driven NKG2C+NK cell expansion[J].J Clin Invest,2014,124(12):5305-5316.
[52]Luetke-Eversloh M,Hammer Q,Durek P,et al.Human cytomegalovirus drives epigenetic imprinting of the IFNG locus in NKG2Chi natural killer cells[J].PLo S Pathog,2014,10(10):e1004441.
[53]Keppel MP,Yang L,Cooper MA.Murine NK cell intrinsic cytokine-induced memory-like responses are maintained following homeostatic proliferation[J].J Immunol,2013,190(9):4754-4762.
[54]Ni J,Holsken O,Miller M,et al.Adoptively transferred natural killer cells maintain long-term antitumor activity by epigenetic imprinting and CD4(+)T cell help[J].Oncoimmunology,2016,5(9):e1219009.
[55]Romee R,Schneider SE,Leong JW,et al.Cytokine activation induces human memory-like NK cells[J].Blood,2012,120(24):4751-4760.
[56]Ni J,Miller M,Stojanovic A,et al.Sustained effector function of IL-12/15/18-preactivated NK cells against established tumors[J].J Exp Med,2012,209(13):2351-2365.
[57]Romee R,Rosario M,Berrien-Elliott MM,et al.Cytokine-induced memory-like natural killer cells exhibit enhanced responses against myeloid leukemia[J].Science Translational Medicine,2016,8(357):357ra123.
[58]Li T,Wang J,Wang Y,et al.Respiratory influenza virus infection induces memory-like liver NK cells in mice[J].J Immunol,2017,198(3):1242-1252.
[59]Dou Y,Fu B,Sun R,et al.Influenza vaccine induces intracellular immune memory of human NK cells[J].PLo S One,2015,10(3):e0121258.
[60]Vosshenrich CA,Garcia-Ojeda ME,Samson-Villeger SI,et al.Athymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127[J].Nat Immunol,2006,7(11):1217-1224.
[61]Luther C,Warner K,Takei F.Unique progenitors in mouse lymph node develop into CD127+NK cells:thymus-dependent and thymus-independent pathways[J].Blood,2011,117(15):4012-4021.
[62]Knolle PA,Wohlleber D.Immunological functions of liver sinusoidal endothelial cells[J].Cell Mol Immunol,2016,13:347.
[63]Liang B,Hara T,Wagatsuma K,et al.Role of hepatocyte-derived IL-7 in maintenance of intrahepatic NKT cells and T cells and development of B cells in fetal liver[J].J Immunol,2012,189(9):4444-4450.
[64]Sawa Y,Arima Y,Ogura H,et al.Hepatic Interleukin-7 expression regulates T cell responses[J].Immunity,2009,30(3):447-457.
[65]Carbone T,Nasorri F,Pennino D,et al.CD56highCD16-CD62L-NK cells accumulate in allergic contact dermatitis and contribute to the expression of allergic responses[J].J Immunol,2010,184(2):1102-1110.
[66]Martinez-Gonzalez I,Matha L,Steer CA,et al.Immunological memory of group 2 innate lymphoid cells[J].Trends Immunol,2017,38(6):423-431.
[2]Artis D,Spits H.The biology of innate lymphoid cells[J].Nature,2015,517(7534):293-301.
[3]Eberl G,Colonna M,Di Santo JP,et al.Innate lymphoid cells:a new paradigm in immunology[J].Science,2015,348(6237):aaa6566.
[4]Vivier E,Artis D,Colonna M,et al.Innate lymphoid cells:10 years on[J].Cell,2018,174(5):1054-1066.
[5]Fuchs A,Vermi W,Lee JS,et al.Intraepithelial Type 1 innate lymphoid cells are a unique subset of IL-12-and IL-15-responsive IFN-gamma-producing cells[J].Immunity,2013,38(4):769-781.
[6]Weizman OE,Adams NM,Schuster IS,et al.ILC1 confer early host protection at initial sites of viral infection[J].Cell,2017,171(4):795-808 e12.
[7]Moro K,Yamada T,Tanabe M,et al.Innate production of TH2 cytokines by adipose tissue-associated c-Kit+Sca-1+lymphoid cells[J].Nature,2009,463:540.
[8]Neill DR,Wong SH,Bellosi A,et al.Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity[J].Nature,2010,464:1367.
[9]Luci C,Reynders A,Ivanov II,et al.Influence of the transcription factor RORγt on the development of NKp46+cell populations in gut and skin[J].Nature Immunol,2008,10:75.
[10]Satoh-Takayama N,Vosshenrich CA,Lesjean-Pottier S,et al.Microbial flora drives interleukin 22 production in intestinal NKp46+cells that provide innate mucosal immune defense[J].Immunity,2008,29(6):958-970.
[11]Mebius RE,Rennert P,Weissman IL.Developing lymph nodes collect CD4+CD3-LTβ+cells that can differentiate to APC,NKcells,and follicular cells but not T or B cells[J].Immunity,1997,7(4):493-504.
[12]Wang S,Xia P,Chen Y,et al.Regulatory innate lymphoid cells control innate intestinal inflammation[J].Cell,2017,171(1):201-216.
[13]O'leary JG,Goodarzi M,Drayton DL,et al.T cell-and B cell-independent adaptive immunity mediated by natural killer cells[J].Nat Immunol,2006,7(5):507-516.
[14]Sun JC,Beilke JN,Lanier LL.Adaptive immune features of natural killer cells[J].Nature,2009,457(7229):557-561.
[15]Cooper MA,Elliott JM,Keyel PA,et al.Cytokine-induced memory-like natural killer cells[J].Proc Natl Acad Sci U S A,2009,106(6):1915-1919.
[16]Reeves RK,Li H,Jost S,et al.Antigen-specific NK cell memory in rhesus macaques[J].Nat Immunol,2015,16(9):927-932.
[17]Bjorkstrom NK,Lindgren T,Stoltz M,et al.Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus[J].J Exp Med,2011,208(1):13-21.
[18]Lopez-Verges S,Milush JM,Schwartz BS,et al.Expansion of a unique CD57(+)NKG2Chi natural killer cell subset during acute human cytomegalovirus infection[J].Proc Natl Acad Sci U S A,2011,108(36):14725-14732.
[19]Lee J,Zhang T,Hwang I,et al.Epigenetic modification and antibody-dependent expansion of memory-like NK cells in human cytomegalovirus-infected individuals[J].Immunity,2015,42(3):431-442.
[20]Martinez-Gonzalez I,Matha L,Steer CA,et al.Allergen-experienced group 2 innate lymphoid cells acquire memory-like properties and enhance allergic lung inflammation[J].Immunity,2016,45(1):198-208.
[21]Wang X,Peng H,Cong J,et al.Memory formation and long-term maintenance of IL-7Ralpha(+)ILC1s via a lymph node-liver axis[J].Nat Commun,2018,9(1):4854.
[22]Paust S,Gill HS,Wang BZ,et al.Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses[J].Nat Immunol,2010,11(12):1127-1135.
[23]Peng H,Jiang X,Chen Y,et al.Liver-resident NK cells confer adaptive immunity in skin-contact inflammation[J].J Clin Invest,2013,123(4):1444-1456.
[24]Peng H,Wisse E,Tian Z.Liver natural killer cells:subsets and roles in liver immunity[J].Cell Mol Immunol,2016,13(3):328-336.
[25]Peng H,Sun R.Liver-resident NK cells and their potential functions[J].Cell Mol Immunol,2017,14:890.
[26]Zhang LH,Shin JH,Haggadone MD,et al.The aryl hydrocarbon receptor is required for the maintenance of liver-resident natural killer cells[J].J Exp Med,2016,213(11):2249-2257.
[27]Van Den Boorn JG,Jakobs C,Hagen C,et al.Inflammasome-dependent induction of adaptive NK cell memory[J].Immunity,2016,44(6):1406-1421.
[28]Wight A,Mahmoud AB,Scur M,et al.Critical role for the Ly49family of class I MHC receptors in adaptive natural killer cell responses[J].Proc Natl Acad Sci U S A,2018,115(45):11579-11584.
[29]O'sullivan TE,Sun JC,Lanier LL.Natural killer cell memory[J].Immunity,2015,43(4):634-645.
[30]Nabekura T,Lanier LL.Activating receptors for self-MHC class Ienhance effector functions and memory differentiation of NK cells during mouse cytomegalovirus infection[J].Immunity,2016,45(1):74-82.
[31]Nabekura T,Lanier LL.Antigen-specific expansion and differentiation of natural killer cells by alloantigen stimulation[J].J Exp Med,2014,211(12):2455-2465.
[32]Nabekura T,Kanaya M,Shibuya A,et al.Costimulatory molecule DNAM-1 is essential for optimal differentiation of memory natural killer cells during mouse cytomegalovirus infection[J].Immunity,2014,40(2):225-234.
[33]Madera S,Rapp M,Firth MA,et al.Type I IFN promotes NK cell expansion during viral infection by protecting NK cells against fratricide[J].J Exp Med,2016,213(2):225-233.
[34]Nabekura T,Girard JP,Lanier LL.IL-33 receptor ST2 amplifies the expansion of NK cells and enhances host defense during mouse cytomegalovirus infection[J].J Immunol,2015,194(12):5948-5952.
[35]Sun JC,Madera S,Bezman NA,et al.Proinflammatory cytokine signaling required for the generation of natural killer cell memory[J].J Exp Med,2012,209(5):947-954.
[36]Madera S,Sun JC.Cutting edge:stage-specific requirement of IL-18 for antiviral NK cell expansion[J].J Immunol,2015,194(4):1408-1412.
[37]Beaulieu AM,Zawislak CL,Nakayama T,et al.The transcription factor Zbtb32 controls the proliferative burst of virus-specific natural killer cells responding to infection[J].Nat Immunol,2014,15(6):546-553.
[38]Rapp M,Lau CM,Adams NM,et al.Core-binding factor β and Runx transcription factors promote adaptive natural killer cell responses[J].Science Immunology,2017,2(18):eaan3796.
[39]Geary CD,Krishna C,Lau CM,et al.Non-redundant ISGF3 components promote NK cell survival in an Auto-regulatory Manner during viral infection[J].Cell Reports,2018,24(8):1949-1957.
[40]Min-Oo G,Bezman NA,Madera S,et al.Proapoptotic Bim regulates antigen-specific NK cell contraction and the generation of the memory NK cell pool after cytomegalovirus infection[J].JExp Med,2014,211(7):1289-1296.
[41]O'sullivan TE,Johnson LR,Kang HH,et al.BNIP3-and BNIP3L-mediated mitophagy promotes the generation of natural killer cell memory[J].Immunity,2015,43(2):331-342.
[42]Firth M A,Madera S,Beaulieu A M,et al.Nfil3-independent lineage maintenance and antiviral response of natural killer cells[J].J Exp Med,2013,210(13):2981-2990.
[43]Lau CM,Adams NM,Geary CD,et al.Epigenetic control of innate and adaptive immune memory[J].Nat Immunol,2018,19(9):963-972.
[44]Bantug GR,Galluzzi L,Kroemer G,et al.The spectrum of T cell metabolism in health and disease[J].Nat Rev Immunol,2018,18(1):19-34.
[45]Cui G,Staron MM,Gray SM,et al.IL-7-induced glycerol transport and TAG synthesis promotes memory CD8+T cell longevity[J].Cell,2015,161(4):750-761.
[46]Cong J,Wang X,Zheng X,et al.Dysfunction of natural killer cells by FBP1-induced inhibition of glycolysis during lung cancer progression[J].Cell Metab,2018,28(2):243-255.
[47]Cichocki F,Wu CY,Zhang B,et al.ARID5B regulates metabolic programming in human adaptive NK cells[J].J Exp Med,2018,215(9):2379-2395.
[48]Beziat V,Dalgard O,Asselah T,et al.CMV drives clonal expansion of NKG2C+NK cells expressing self-specific KIRs in chronic hepatitis patients[J].Eur J Immunol,2012,42(2):447-457.
[49]Ram DR,Manickam C,Hueber B,et al.Tracking KLRC2(NKG2C)+memory-like NK cells in SIV+and rh CMV+rhesus macaques[J].PLo S Pathog,2018,14(5):e1007104.
[50]Hammer Q,Ruckert T,Borst EM,et al.Peptide-specific recognition of human cytomegalovirus strains controls adaptive natural killer cells[J].Nat Immunol,2018,19(5):453-463.
[51]Rolle A,Pollmann J,Ewen EM,et al.IL-12-producing monocytes and HLA-E control HCMV-driven NKG2C+NK cell expansion[J].J Clin Invest,2014,124(12):5305-5316.
[52]Luetke-Eversloh M,Hammer Q,Durek P,et al.Human cytomegalovirus drives epigenetic imprinting of the IFNG locus in NKG2Chi natural killer cells[J].PLo S Pathog,2014,10(10):e1004441.
[53]Keppel MP,Yang L,Cooper MA.Murine NK cell intrinsic cytokine-induced memory-like responses are maintained following homeostatic proliferation[J].J Immunol,2013,190(9):4754-4762.
[54]Ni J,Holsken O,Miller M,et al.Adoptively transferred natural killer cells maintain long-term antitumor activity by epigenetic imprinting and CD4(+)T cell help[J].Oncoimmunology,2016,5(9):e1219009.
[55]Romee R,Schneider SE,Leong JW,et al.Cytokine activation induces human memory-like NK cells[J].Blood,2012,120(24):4751-4760.
[56]Ni J,Miller M,Stojanovic A,et al.Sustained effector function of IL-12/15/18-preactivated NK cells against established tumors[J].J Exp Med,2012,209(13):2351-2365.
[57]Romee R,Rosario M,Berrien-Elliott MM,et al.Cytokine-induced memory-like natural killer cells exhibit enhanced responses against myeloid leukemia[J].Science Translational Medicine,2016,8(357):357ra123.
[58]Li T,Wang J,Wang Y,et al.Respiratory influenza virus infection induces memory-like liver NK cells in mice[J].J Immunol,2017,198(3):1242-1252.
[59]Dou Y,Fu B,Sun R,et al.Influenza vaccine induces intracellular immune memory of human NK cells[J].PLo S One,2015,10(3):e0121258.
[60]Vosshenrich CA,Garcia-Ojeda ME,Samson-Villeger SI,et al.Athymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127[J].Nat Immunol,2006,7(11):1217-1224.
[61]Luther C,Warner K,Takei F.Unique progenitors in mouse lymph node develop into CD127+NK cells:thymus-dependent and thymus-independent pathways[J].Blood,2011,117(15):4012-4021.
[62]Knolle PA,Wohlleber D.Immunological functions of liver sinusoidal endothelial cells[J].Cell Mol Immunol,2016,13:347.
[63]Liang B,Hara T,Wagatsuma K,et al.Role of hepatocyte-derived IL-7 in maintenance of intrahepatic NKT cells and T cells and development of B cells in fetal liver[J].J Immunol,2012,189(9):4444-4450.
[64]Sawa Y,Arima Y,Ogura H,et al.Hepatic Interleukin-7 expression regulates T cell responses[J].Immunity,2009,30(3):447-457.
[65]Carbone T,Nasorri F,Pennino D,et al.CD56highCD16-CD62L-NK cells accumulate in allergic contact dermatitis and contribute to the expression of allergic responses[J].J Immunol,2010,184(2):1102-1110.
[66]Martinez-Gonzalez I,Matha L,Steer CA,et al.Immunological memory of group 2 innate lymphoid cells[J].Trends Immunol,2017,38(6):423-431.