Tissue-resident memory-like ILCs: innate counterparts of TRM cells
Xianwei Wang, Zhigang Tian, Hui Peng
Tissue-resident memory-like ILCs: innate counterparts of TRM cells
Innate lymphoid cells (ILCs) are defined as lymphocytes that lack RAG recombinase and do not express diverse antigen receptors; however, recent studies have revealed the adaptive features of ILCs. Mouse cytome-galovirus (MCMV)- and cytokine-induced memory natu-ral killer (NK) cells circulate in the blood and are referred to as conventional memory NK cells. In contrast, virus- and hapten-induced memory NK cells, hapten-induced memory ILC1s, and cytokine-induced memory-like ILC2s exhibit long-term residency in the liver or lung, and are referred to as tissue-resident memory ILCs. Considering their similar migration patterns and mem- ory potential, tissue-resident memory ILCs could be regarded as innate counterparts of resident memory T (TRM) cells. Both tissue-resident memory ILCs and TRM cells share common characteristics in terms of dynam- ics, phenotype, and molecular regulation. The emer-gence of ILC memory expands the basic biology of ILCs and prompts us to re-examine their functions in disease progression. This review discusses the evidence sup-porting tissue-resident memory NK cells and other memory ILC subsets, compares them with TRM cells, and highlights key unsolved questions in this emerging field.
tissue-residency / innate lymphoid cells / immunological memory / TRM cells
[1] |
Adachi T, Kobayashi T,Sugihara E, Yamada T, Ikuta K, Pittaluga S, Saya H, Amagai M, Nagao K (2015) Hair follicle-derived IL-7 and IL-15 mediate skin-resident memory T cell homeostasis and lymphoma. Nat Med 21:1272
CrossRef
Google scholar
|
[2] |
Andreotti JP, Paiva AE, Prazeres PHDM, Guerra DAP, Silva WN, Vaz RS, Mintz A, Birbrair A (2018) The role of natural killer cells in the uterine microenvironment during pregnancy. Cell Mol Immunol 15:941–943
CrossRef
Google scholar
|
[3] |
Arase H, Mocarski ES, Campbell AE, Hill AB, Lanier LL (2002) Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296:1323–1326
CrossRef
Google scholar
|
[4] |
Arnon TI, Achdout H, Lieberman N, Gazit R, Gonen-Gross T, Katz G, Bar-Ilan A, Bloushtain N, Lev M, Joseph A
CrossRef
Google scholar
|
[5] |
Artis D, Spits H (2015) The biology of innate lymphoid cells. Nature 517:293–301
CrossRef
Google scholar
|
[6] |
Aw Yeang HX, Piersma SJ, Lin Y, Yang L, Malkova ON, Miner C, Krupnick AS, Chapman WC, Yokoyama WM (2017) Cutting edge: human CD49e− NK cells are tissue resident in the liver. J Immunol 198:1417–1422
CrossRef
Google scholar
|
[7] |
Bergsbaken T, Bevan MJ (2015) Proinflammatory microenviron ments within the intestine regulate the differentiation of tissue- resident CD8+ T cells responding to infection. Nat Immunol 16:406
CrossRef
Google scholar
|
[8] |
Bergsbaken T, Bevan MJ, Fink PJ (2017) Local inflammatory cues regulate differentiation and persistence of CD8+ tissue-resident memory T cells. Cell Rep 19:114–124
CrossRef
Google scholar
|
[9] |
Brown MG, Dokun AO, Heusel JW, Smith HRC, Beckman DL, Blattenberger EA, Dubbelde CE, Stone LR, Scalzo AA, Yokoyama WM (2001) Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 292:934–937
CrossRef
Google scholar
|
[10] |
Carbone T, Nasorri F, Pennino D, Eyerich K, Foerster S, Cifaldi L, Traidl-Hoffman C, Behrendt H, Cavani A (2010) CD56highCD16 CD62L-NK cells accumulate in allergic contact dermatitis and contribute to the expression of allergic responses. J Immunol 184:1102–1110
CrossRef
Google scholar
|
[11] |
Cella M, Fuchs A, Vermi W, Facchetti F, Otero K, Lennerz JKM, Doherty JM, Mills JC, Colonna M (2008) A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 457:722
CrossRef
Google scholar
|
[12] |
Cepek KL, Shaw SK, Parker CM, Russell GJ, Morrow JS, Rimm DL, Brenner MB (1994) Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the αEβ7 integrin. Nature 372:190–193
CrossRef
Google scholar
|
[13] |
Cerwenka A, Lanier LL (2016) Natural killer cell memory in infection, inflammation and cancer. Nat Rev Immunol 16:112
CrossRef
Google scholar
|
[14] |
Cheuk S, Schlums H, Gallais Sérézal I, Martini E, Chiang SC, Marquardt N, Gibbs A, Detlofsson E, Introini A, Forkel M
CrossRef
Google scholar
|
[15] |
Cichocki F, Wu CY, Zhang B, Felices M, Tesi B, Tuininga K, Dougherty P, Taras E, Hinderlie P, Blazar BR
CrossRef
Google scholar
|
[16] |
Cong J, Wang X, Zheng X, Wang D, Fu B, Sun R, Tian Z, Wei H (2018) Dysfunction of natural killer cells by FBP1-induced inhibition of glycolysis during lung cancer progression. Cell Metab 28(243–255):e245
CrossRef
Google scholar
|
[17] |
Cooper MA (2018) Natural killer cells might adapt their inhibitory receptors for memory. Proc Natl Acad Sci 115:11357
CrossRef
Google scholar
|
[18] |
Cooper MA, Elliott JM, Keyel PA, Yang L, Carrero JA, Yokoyama WM (2009) Cytokine-induced memory-like natural killer cells. Proc Natl Acad Sci USA 106:1915–1919
CrossRef
Google scholar
|
[19] |
Cortez VS, Cervantes-Barragan L, Robinette ML, Bando JK, Wang Y, Geiger TL, Gilfillan S, Fuchs A, Vivier E, Sun JC
CrossRef
Google scholar
|
[20] |
Cuff AO, Robertson FP, Stegmann KA, Pallett LJ, Maini MK, Davidson BR, Male V (2016) Eomeshi NK cells in human liver are long-lived and do not recirculate but can be replenished from the circulation. J Immunol 197:4283–4291
CrossRef
Google scholar
|
[21] |
Cui G, Staron MM, Gray SM, Ho PC, Amezquita RA, Wu J, Kaech SM (2015) IL-7-Induced glycerol transport and TAG synthesis promotes memory CD8+ T cell longevity. Cell 161:750–761
CrossRef
Google scholar
|
[22] |
Cupedo T, Crellin NK, Papazian N, Rombouts EJ, Weijer K, Grogan JL, Fibbe WE, Cornelissen JJ, Spits H (2008) Human fetal lymphoid tissue-inducer cells are interleukin 17-producing pre cursors to RORC+ CD127+ natural killer-like cells. Nat Immunol 10:66
CrossRef
Google scholar
|
[23] |
Diefenbach A, Colonna M, Koyasu S (2014) Development, differen tiation, and diversity of innate lymphoid cells. Immunity 41:354–365
CrossRef
Google scholar
|
[24] |
Eberl G, Colonna M, Di Santo JP, McKenzie AN (2015) Innate lymphoid cells. Innate lymphoid cells: a new paradigm in immunology. Science 348:aaa6566
CrossRef
Google scholar
|
[25] |
Fernandez-Ruiz D, Ng Wei Y, Holz LE, Ma Joel Z, Zaid A, Wong Yik C, Lau Lei S, Mollard V, Cozijnsen A, Collins N
CrossRef
Google scholar
|
[26] |
Filipovic I, Chiossone L, Vacca P, Hamilton RS, Ingegnere T, Doisne J-M, Hawkes DA, Mingari MC, Sharkey AM, Moretta L
CrossRef
Google scholar
|
[27] |
Firth MA, Madera S, Beaulieu AM, Gasteiger G, Castillo EF, Schluns KS, Kubo M, Rothman PB, Vivier E, Sun JC (2013) Nfil3 independent lineage maintenance and antiviral response of natural killer cells. J Exp Med 210:2981–2990
CrossRef
Google scholar
|
[28] |
Fu B, Zhou Y, Ni X, Tong X, Xu X, Dong Z, Sun R, Tian Z, Wei H (2017) Natural killer cells promote fetal development through the secretion of growth-promoting factors. Immunity 47(1100–1113): e1106
CrossRef
Google scholar
|
[29] |
Fuchs A, Vermi W, Lee Jacob S, Lonardi S, Gilfillan S, Newberry Rodney D, Cella M, Colonna M (2013) Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12- and IL-15 responsive IFN-γ-producing cells. Immunity 38:769–781
CrossRef
Google scholar
|
[30] |
Gamliel M, Goldman-Wohl D, Isaacson B, Gur C, Stein N, Yamin R, Berger M, Grunewald M, Keshet E, Rais Y
CrossRef
Google scholar
|
[31] |
Gasteiger G, Fan X, Dikiy S, Lee SY, Rudensky AY (2015) Tissue residency of innate lymphoid cells in lymphoid and nonlymphoid organs. Science 350:981–985
CrossRef
Google scholar
|
[32] |
Gillard GO, Bivas-Benita M, Hovav A-H, Grandpre LE, Panas MW, Seaman MS, Haynes BF, Letvin NL (2011) Thy1+ Nk cells from vaccinia virus-primed mice confer protection against vaccinia virus challenge in the absence of adaptive lymphocytes. PLOS Pathog 7:e1002141
CrossRef
Google scholar
|
[33] |
Hammer Q, Ruckert T, Borst EM, Dunst J, Haubner A, Durek P, Heinrich F, Gasparoni G, Babic M, Tomic A
CrossRef
Google scholar
|
[34] |
Hudspeth K, Donadon M, Cimino M, Pontarini E, Tentorio P, Preti M, Hong M, Bertoletti A, Bicciato S, Invernizzi P
CrossRef
Google scholar
|
[35] |
Hydes T, Noll A, Salinas-Riester G, Abuhilal M, Armstrong T, Hamady Z, Primrose J, Takhar A, Walter L, Khakoo SI (2017) IL 12 and IL-15 induce the expression of CXCR6 and CD49a on peripheral natural killer cells. Immun Inflamm Dis 6:34–46
CrossRef
Google scholar
|
[36] |
Jiang X, Clark RA, Liu L, Wagers AJ, Fuhlbrigge RC, Kupper TS (2012) Skin infection generates non-migratory memory CD8+ T (RM) cells providing global skin immunity. Nature 483:227–231
CrossRef
Google scholar
|
[37] |
Kamimura Y, Lanier LL (2015) Homeostatic control of memory cell progenitors in the natural killer cell lineage. Cell Rep 10:280–291
CrossRef
Google scholar
|
[38] |
Kaplan DH, Igyarto BZ, Gaspari AA (2012) Early immune events in the induction of allergic contact dermatitis. Nat Rev Immunol 12:114–124
CrossRef
Google scholar
|
[39] |
Klose CSN, Flach M, Mohle L, Rogell L, Hoyler T, Ebert K, Fabiunke C, Pfeifer D, Sexl V, Fonseca-Pereira D
CrossRef
Google scholar
|
[40] |
Laidlaw Brian J, Zhang N, Marshall Heather D, Staron Mathew M, Guan T, Hu Y, Cauley Linda S, Craft J, Kaech Susan M (2014) CD4+ T cell help guides formation of CD103+ lung-resident memory CD8+ T cells during influenza viral infection. Immunity 41:633–645
CrossRef
Google scholar
|
[41] |
Lau CM, Adams NM, Geary CD, Weizman OE, Rapp M, Pritykin Y, Leslie CS, Sun JC (2018) Epigenetic control of innate and adaptive immune memory. Nat Immunol 19:963–972
CrossRef
Google scholar
|
[42] |
Li T, Wang J, Wang Y, Chen Y, Wei H, Sun R, Tian Z (2017) Respiratory influenza virus infection induces memory-like liver NK cells in mice. J Immunol 198:1242–1252
CrossRef
Google scholar
|
[43] |
Liang B, Hara T, Wagatsuma K, Zhang J, Maki K, Miyachi H, Kitano S, Yabe-Nishimura C, Tani-Ichi S, Ikuta K (2012) Role of hepatocyte-derived IL-7 in maintenance of intrahepatic NKT cells and T cells and development of B cells in fetal liver. J Immunol 189:4444–4450
CrossRef
Google scholar
|
[44] |
Lopez-Verges S, Milush JM, Schwartz BS, Pando MJ, Jarjoura J, York VA, Houchins JP, Miller S, Kang SM, Norris PJ
CrossRef
Google scholar
|
[45] |
Mackay LK, Braun A, Macleod BL, Collins N, Tebartz C, Bedoui S, Carbone FR, Gebhardt T (2015a) Cutting edge: CD69 interfer ence with sphingosine-1-phosphate receptor function regulates peripheral T cell retention. J Immunol 194:2059–2063
CrossRef
Google scholar
|
[46] |
Mackay LK, Minnich M, Kragten NAM, Liao Y, Nota B, Seillet C, Zaid A, Man K, Preston S, Freestone D
CrossRef
Google scholar
|
[47] |
Mackay LK, Rahimpour A, Ma JZ, Collins N, Stock AT, Hafon M-L, Vega-Ramos J, Lauzurica P, Mueller SN, Stefanovic T
CrossRef
Google scholar
|
[48] |
Mackay LK, Wynne-Jones E, Freestone D, Pellicci DG, Mielke LA, Newman DM, Braun A, Masson F, Kallies A, Belz GT
CrossRef
Google scholar
|
[49] |
Majewska-Szczepanik M, Paust S, von Andrian UH, Askenase PW, Szczepanik M (2013) Natural killer cell-mediated contact sensi tivity develops rapidly and depends on interferon-alpha, inter- feron-gamma and interleukin-12. Immunology 140:98–110
CrossRef
Google scholar
|
[50] |
Marquardt N, Béziat V, Nyström S, Hengst J, Ivarsson MA, Kekäläinen E, Johansson H, Mjösberg J, Westgren M, Lankisch TO
CrossRef
Google scholar
|
[51] |
Martinez-Gonzalez I, Matha L, Steer CA, Ghaedi M, Poon GF, Takei F (2016) Allergen-experienced group 2 innate lymphoid cells acquire memory-like properties and enhance allergic lung inflammation. Immunity 45:198–208
CrossRef
Google scholar
|
[52] |
Martinez-Gonzalez I,Matha L, Steer CA, Takei F (2017) Immuno logical memory of group 2 innate lymphoid cells. Trends Immunol 38:423–431
CrossRef
Google scholar
|
[53] |
Moro K, Yamada T, Tanabe M, Takeuchi T, Ikawa T, Kawamoto H, Furusawa J-I, Ohtani M, Fujii H, Koyasu S (2009) Innate production of TH2 cytokines by adipose tissue-associated c-Kit+Sca-1+ lymphoid cells. Nature 463:540
CrossRef
Google scholar
|
[54] |
Mueller SN, Gebhardt T, Carbone FR, Heath WR (2013) Memory T cell subsets, migration patterns, and tissue residence. Annu Rev Immunol 31:137–161
CrossRef
Google scholar
|
[55] |
Mueller SN, Mackay LK (2015) Tissue-resident memory T cells: local specialists in immune defence. Nat Rev Immunol 16:79
CrossRef
Google scholar
|
[56] |
Neill DR, Wong SH, Bellosi A, Flynn RJ, Daly M, Langford TKA, Bucks C, Kane CM, Fallon PG, Pannell R
CrossRef
Google scholar
|
[57] |
O’Leary JG, Goodarzi M, Drayton DL, von Andrian UH (2006) T cell and B cell-independent adaptive immunity mediated by natural killer cells. Nat Immunol 7:507–516
CrossRef
Google scholar
|
[58] |
O’Sullivan TE, Sun JC, Lanier LL (2015) Natural killer cell memory. Immunity 43:634–645
CrossRef
Google scholar
|
[59] |
O’Brien KL, Finlay DK (2019) Immunometabolism and natural killer cell responses. Nat Rev Immunol 19:282–290
CrossRef
Google scholar
|
[60] |
Pahl JHW, Cerwenka A, Ni J (2018) Memory-like NK cells: remembering a previous activation by cytokines and NK cell receptors. Front Immunol 9:2796
CrossRef
Google scholar
|
[61] |
Paust S, Gill HS, Wang BZ, Flynn MP, Moseman EA, Senman B, Szczepanik M, Telenti A, Askenase PW, Compans RW
CrossRef
Google scholar
|
[62] |
Peng H, Jiang X, Chen Y, Sojka DK, Wei H, Gao X, Sun R, Yokoyama WM, Tian Z (2013a) Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J Clin Invest 123:1444–1456
CrossRef
Google scholar
|
[63] |
Peng H, Sun R (2017) Liver-resident NK cells and their potential functions. Cell Mol Immunol 14:890
CrossRef
Google scholar
|
[64] |
Peng H, Sun R, Tang L, Wei H, Tian Z (2013b) CD62L is critical for maturation and accumulation of murine hepatic NK cells in response to viral infection. J Immunol 190:4255
CrossRef
Google scholar
|
[65] |
Rapp M, Wiedemann GM, Sun JC (2018) Memory responses of innate lymphocytes and parallels with T cells. Semin Immuno pathol 40:343–355
CrossRef
Google scholar
|
[66] |
Robinette ML, Bando JK, Song W, Ulland TK, Gilfillan S, Colonna M (2017) IL-15 sustains IL-7R-independent ILC2 and ILC3 devel opment. Nat Commun 8:14601
CrossRef
Google scholar
|
[67] |
Romee R, Schneider SE, Leong JW, Chase JM, Keppel CR, Sullivan RP, Cooper MA, Fehniger TA (2012) Cytokine activation induces human memory-like NK cells. Blood 120:4751–4760
CrossRef
Google scholar
|
[68] |
Salimi M, Barlow JL, Saunders SP, Xue L, Gutowska-Owsiak D, Wang X, Huang L-C, Johnson D, Scanlon ST, McKenzie ANJ
CrossRef
Google scholar
|
[69] |
Sanos SL, Bui VL, Mortha A, Oberle K, Heners C, Johner C, Diefenbach A (2008) RORγt and commensal microflora are required for the differentiation of mucosal interleukin 22-produc ing NKp46+ cells. Nat Immunol 10:83
CrossRef
Google scholar
|
[70] |
Satoh-Takayama N, Vosshenrich CAJ, Lesjean-Pottier S, Sawa S, Lochner M, Rattis F, Mention J-J, Thiam K, Cerf-Bensussan N, Mandelboim O
CrossRef
Google scholar
|
[71] |
Schenkel Jason M, Masopust D (2014) Tissue-resident memory T cells. Immunity 41:886–897
CrossRef
Google scholar
|
[72] |
Sheridan Brian S, Pham Q-M, Lee Y-T, Cauley Linda S, Puddington L, Lefrançois L (2014) Oral infection drives a distinct population of intestinal resident memory CD8+ T cells with enhanced protective function. Immunity 40:747–757
CrossRef
Google scholar
|
[73] |
Shiow LR, Rosen DB, Brdičková N, Xu Y, An J, Lanier LL, Cyster JG, Matloubian M (2006) CD69 acts downstream of interferon-α/β to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440:540–544
CrossRef
Google scholar
|
[74] |
Skon CN, Lee J-Y, Anderson KG, Masopust D, Hogquist KA, Jameson SC (2013) Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells. Nat Immunol 14:1285–1293
CrossRef
Google scholar
|
[75] |
Smolders J, Heutinck KM, Fransen NL, Remmerswaal EBM, Hombrink P, ten Berge IJM, van Lier RAW, Huitinga I, Hamann J (2018) Tissue-resident memory T cells populate the human brain. Nat Commun 9:4593
CrossRef
Google scholar
|
[76] |
Sojka DK, Plougastel-Douglas B, Yang L, Pak-Wittel MA, Artyomov MN, Ivanova Y, Zhong C, Chase JM, Rothman PB, Yu J
CrossRef
Google scholar
|
[77] |
Sojka DK, Yang L, Plougastel-Douglas B, Higuchi DA, Croy BA, Yokoyama WM (2018) Cutting edge: local proliferation of uterine tissue-resident NK cells during decidualization in mice. J Immunol 201:2551–2556
CrossRef
Google scholar
|
[78] |
Stegmann KA, Robertson F, Hansi N, Gill U, Pallant C, Christo phides T, Pallett LJ, Peppa D, Dunn C, Fusai G
CrossRef
Google scholar
|
[79] |
Sun JC, Beilke JN, Lanier LL (2009) Adaptive immune features of natural killer cells. Nature 457:557–561
CrossRef
Google scholar
|
[80] |
Tan Z, Liu Q, Jiang R, Lv L, Shoto SS, Maillet I, Quesniaux V, Tang J, Zhang W, Sun B
CrossRef
Google scholar
|
[81] |
Tang L, Peng H, Zhou J, Chen YY, Wei HM, Sun R, Yokoyama WM, Tian ZG (2016) Differential phenotypic and functional properties of liver-resident NK cells and mucosal ILC1s. J Autoimmun 67:29–35
CrossRef
Google scholar
|
[82] |
Teijaro JR, Turner D, Pham Q, Wherry EJ, Lefrançois L, Farber DL (2011) Cutting edge: tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection. J Im munol 187:5510
CrossRef
Google scholar
|
[83] |
van den Boorn JG, Jakobs C, Hagen C, Renn M, Luiten RM, Melief CJ, Tuting T, Garbi N, Hartmann G, Hornung V (2016) Inflam masome-dependent induction of adaptive NK cell memory. Immunity 44:1406–1421
CrossRef
Google scholar
|
[84] |
Vivier E, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, Koyasu S, Locksley RM, McKenzie ANJ, Mebius RE
CrossRef
Google scholar
|
[85] |
Wakim LM, Woodward-Davis A, Bevan MJ (2010) Memory T cells persisting within the brain after local infection show functional adaptations to their tissue of residence. Proc Natl Acad Sci USA 107:17872
CrossRef
Google scholar
|
[86] |
Wang X, Peng H, Cong J, Wang X, Lian Z, Wei H, Sun R, Tian Z (2018) Memory formation and long-term maintenance of IL 7Ralpha(+) ILC1s via a lymph node-liver axis. Nat Commun 9:4854
CrossRef
Google scholar
|
[87] |
Wang X, Peng H, Tian Z (2019) Innate lymphoid cell memory. Cell Mol Immunol 16:423–429
CrossRef
Google scholar
|
[88] |
Weiskirchen R, Tacke F (2017) Interleukin-33 in the pathogenesis of liver fibrosis: alarming ILC2 and hepatic stellate cells. Cell Mol Immunol 14:143
CrossRef
Google scholar
|
[89] |
Weizman OE, Adams NM, Schuster IS, Krishna C, Pritykin Y, Lau C, Degli-Esposti MA, Leslie CS, Sun JC, O’Sullivan TE (2017) ILC1 confer early host protection at initial sites of viral infection. Cell 171(795–808):e712
CrossRef
Google scholar
|
[90] |
Wight A, Mahmoud AB, Scur M, Tu MM, Rahim MMA, Sad S, Makrigiannis AP (2018) Critical role for the Ly49 family of class I MHC receptors in adaptive natural killer cell responses. Proc Natl Acad Sci USA 115:11579–11584
CrossRef
Google scholar
|
[91] |
Wittig O, Paez-Cortez J, Cardier JE (2010) Liver sinusoidal endothelial cells promote B lymphopoiesis from primitive hematopoietic cells. Stem Cells Dev 19:341–350
CrossRef
Google scholar
|
[92] |
Wu LS-H, Wang J-Y (2018) Warm up, cool down, and tearing apart in NK cell memory. Cell Mol Immunol 15:1095–1097
CrossRef
Google scholar
|
[93] |
Zaid A, Hor JL, Christo SN, Groom JR, Heath WR, Mackay LK, Mueller SN (2017) Chemokine receptor-dependent control of skin tissue-resident memory T cell formation. J Immunol 199:2451
CrossRef
Google scholar
|
[94] |
Zhang LH, Shin JH, Haggadone MD, Sunwoo JB (2016) The aryl hydrocarbon receptor is required for the maintenance of liver- resident natural killer cells. J Exp Med 213:2249–2257
CrossRef
Google scholar
|
[95] |
Zhang Q-F, Yin W-W, Xia Y, Yi Y-Y, He Q-F, Wang X, Ren H, Zhang D-Z (2017) 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 14:819
CrossRef
Google scholar
|
[96] |
Zundler S, Becker E, Spocinska M, Slawik M, Parga-Vidal L, Stark R, Wiendl M, Atreya R, Rath T, Leppkes M
CrossRef
Google scholar
|
/
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