Innate lymphoid cells and gastrointestinal disease

Ziyu Wang; Jun Wang

doi:10.1016/j.jgg.2021.08.004

Volume 48 Issue 9

Sep. 2021

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2021 > 48(9): 763-770

PDF( 669 KB)

Innate lymphoid cells and gastrointestinal disease

doi: 10.1016/j.jgg.2021.08.004

Ziyu Wang^a,b,
Jun Wang^a,b

a. CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Science, Beijing 100101, China;
b. University of Chinese Academy of Sciences, Beijing 100049, China

Funds:

This work is supported by National Key Research and Development Program of China (2018YFC2000500), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB29020000) and the National Natural Science Foundation of China (31771481, 91857101, 81873548).

Received Date: 2021-07-31
Accepted Date: 2021-08-12
Rev Recd Date: 2021-08-09
Publish Date: 2021-08-20

Abstract

Abstract

Innate lymphoid cells (ILCs) are a group of innate immune cells, which constitute the first line of defense in the immune system, together with skin and mucous membrane. ILCs also play an important role in maintaining the homeostasis of the body, particularly in the complex and diverse environment of the intestine. ILCs respond to different microenvironments, maintaining homeostasis directly or indirectly through cytokines. As a result, ILCs, with complex and pleiotropic characteristics, are associated with many gastrointestinal diseases. Their ability of transition among those subgroups makes them function as both promoting and inhibiting cells, thus affecting homeostasis and disease progressing to either alleviation or deterioration. With these special characteristics, ILCs theoretically can be used in the new generation of immunotherapy as an alternative and supplement to current tumor therapy. Our review summarizes the characteristics of ILCs with respect to category, function, and the relationship with intestinal homeostasis and gastrointestinal diseases. In addition, potential tumor immunotherapies involving ILCs are also discussed to shed light on the perspectives of immunotherapy.
- Innate lymphoid cells,
- Gastrointestinal diseases,
- Colorectal cancer,
- Intestinal homeostasis,
- Cytokines,
- Cancer immune therapy

FullText(HTML)

References(95)

References

Abtahi, S., Davani, F., Mojtahedi, Z., Hosseini, S., Bananzadeh, A., Ghaderi, A., 2017. Dual association of serum interleukin-10 levels with colorectal cancer. J. Canc. Res. Therapeut. 13, 252-256.

Arnold, I.C., Artola-Borán, M., Gurtner, A., Bertram, K., Müller, A., 2020. The GM-CSF-IRF5 signaling axis in eosinophils promotes antitumor immunity through activation of type 1 T cell responses. J. Exp. Med. 217, e20190706.

Atreya, I., Kindermann, M., Wirtz, S., 2019. Innate lymphoid cells in intestinal cancer development. Semin. Immunol. 41, 101267.

Babaie, D., Rasouli, S., Darougar, S., Daneshmandii, Z., Mesdaghi, M., Ghadimi, F., 2020. Serum interleukin-17 evaluation in patients with eosinophilic gastrointestinal disease. Immunoregulation 3, 61-66.

Bando, J.K., Gilfillan, S., Di Luccia, B., Fachi, J.L., Secca, C., Cella, M., Colonna, M., 2020. ILC2s are the predominant source of intestinal ILC-derived IL-10. J. Exp. Med. 217, e20191520.

Barrett, J.C., Hansoul, S., Nicolae, D.L., Cho, J.H., Duerr, R.H., Rioux, J.D., Brant, S.R., Silverberg, M.S., Taylor, K.D., Barmada, M.M., 2008. Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat. Genet. 40, 955-962.

Bernink, J.H., Peters, C.P., Munneke, M., te Velde, A.A., Meijer, S.L., Weijer, K., Hreggvidsdottir, H.S., Heinsbroek, S.E., Legrand, N., Buskens, C.J., 2013. Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat. Immunol. 14, 221-229.

Bernink, J.H., Ohne, Y., Teunissen, M.B.M., Wang, J., Wu, J., Krabbendam, L., Guntermann, C., Volckmann, R., Koster, J., van Tol, S., 2019. c-Kit-positive ILC2s exhibit an ILC3-like signature that may contribute to IL-17-mediated pathologies. Nat. Immunol. 20, 992-1003.

Braham, J.A., Balti, M., Mouna, B.A., Sinda, B., Meriem, H., Zribi, A., Sonia, B.N., Sana, F., Haddaoui, A., 2017. The association of the level of serum of interleukin-10 and its polymorphism gene with the risk and the prognosis for colorectal cancer in Tunisia. Ann. Oncol. 28, xi13.

Brand, S., Beigel, F., Olszak, T., Zitzmann, K., Eichhorst, S.T., Otte, J.M., Diepolder, H., Marquardt, A., Jagla, W., Popp, A., 2006. IL-22 is increased in active Crohn's disease and promotes proinflammatory gene expression and intestinal epithelial cell migration. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G827-G838.

Brandacher, G., Perathoner, A., Ladurner, R., Schneeberger, S., Obrist, P., Winkler, C., Werner, E.R., Werner-Felmayer, G., Weiss, H.G., Göbel, G., 2006. Prognostic value of indoleamine 2,3-dioxygenase expression in colorectal cancer: effect on tumor-infiltrating T cells. Clin. Cancer. Res. 12, 1144-1151.

Castro-Dopico, T., Fleming, A., Dennison, T.W., Ferdinand, J.R., Harcourt, K., Stewart, B.J., Cader, Z., Tuong, Z.K., Jing, C., Lok, L.S.C., 2020. GM-CSF calibrates macrophage defense and wound healing programs during intestinal infection and inflammation. Cell Rep. 32, 107857.

Chun, E., Lavoie, S., Fonseca-Pereira, D., Bae, S., Michaud, M., Hoveyda, H.R., Fraser, G.L., Gallini Comeau, C.A., Glickman, J.N., Fuller, M.H., 2019. Metabolite-sensing receptor Ffar2 regulates colonic group 3 innate lymphoid cells and gut immunity. Immunity 51, 871-884.

Cianferoni, A., Spergel, J.M., 2015. Eosinophilic esophagitis and gastroenteritis. Curr. Allergy Asthma Rep. 15, 58.

De Luca, A., Carvalho, A., Cunha, C., Iannitti, R.G., Pitzurra, L., Giovannini, G., Mencacci, A., Bartolommei, L., Moretti, S., Massi-Benedetti, C., IL-22 and DO1 affect immunity and tolerance to murine and human vaginal candidiasis. PLoS Pathog. 9 e1003486-e1003486.

Dekker, E., Tanis, P.J., Vleugels, J.L.A., Kasi, P.M., Wallace, M.B., 2019. Colorectal cancer. Lancet 394, 1467-1480.

Doherty, T.A., Baum, R., Newbury, R.O., Yang, T., Dohil, R., Aquino, M., Doshi, A., Walford, H.H., Kurten, R.C., Broide, D.H., 2015. Group 2 innate lymphocytes (ILC2) are enriched in active eosinophilic esophagitis. J. Allergy Clin. Immunol. 136, 792-794. e793.

Ducimetiere, L., Vermeer, M., Tugues, S., 2019. The interplay between innate lymphoid cells and the tumor microenvironment. Front. Immunol. 10, 2895.

Ebert, P., Cheung, J., Yang, Y., Mcnamara, E., Hong, R., Moskalenko, M., Gould, S.E., Maecker, H., Irving, B.A., Kim, J.M., 2016. MAP kinase inhibition promotes T cell and anti-tumor activity in combination with PD-L1 checkpoint blockade. Immunity 44, 609-621.

Eisenring, M., vom Berg, J., Kristiansen, G., Saller, E., Becher, B., 2010. IL-12 initiates tumor rejection via lymphoid tissue-inducer cells bearing the natural cytotoxicity receptor NKp46. Nat. Immunol. 11, 1030-1038.

Ercolano, G., Moretti, A., Lozano Hoyos, T.W., Salvatore, S., Jandus, C., Trabanelli, S., 2020. TGM2+ IFN-gamma secreting circulating innate lymphoid cell precursors (ILCPs) are enhanced in children with celiac disease. World Aller. Organ 13, 100427.

Ettersperger, J., Montcuquet, N., Malamut, G., Guegan, N., Lopez-Lastra, S., Gayraud, S., Reimann, C., Vidal, E., Cagnard, N., Villarese, P., 2016. Interleukin-15-dependent T-cell-like innate intraepithelial lymphocytes develop in the intestine and transform into lymphomas in celiac disease. Immunity 45, 610-625.

Fahey, L.M., Liacouras, C.A., 2017. Eosinophilic gastrointestinal disorders. Pediatr. Clin. 64, 475-485.

Friedrich, M., Pohin, M., Powrie, F., 2019. Cytokine networks in the pathophysiology of inflammatory bowel disease. Immunity 50, 992-1006.

Fuchs, A., Vermi, W., Lee, J.S., Lonardi, S., Gilfillan, S., Newberry, R.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.

Fulmer, Tim, 2009. Intercepting IL15 in celiac disease. SciBX Science-Business Exch. 2, 1362.

Gerald Brandacher, A.P., Ladurner, R., Schneeberger, S., Obrist, P., Winkler, C., Werner, E.R., Werner-Felmayer, G., Weiss, H.G., Georg, G., Margreiter, R., 2006. Prognostic value of indoleamine 2,3-dioxygenase expression in colorectal cancer effect on tumor-infiltrating T cells. Clin. Cancer. Res. 12, 1144-1151.

Ganal-Vonarburg, S.C., Duerr, C.U., 2020. The interaction of intestinal microbiota and innate lymphoid cells in health and disease throughout life. Immunology 159, 39-51.

Gerbe, F., Sidot, E., Smyth, D.J., Ohmoto, M., Matsumoto, I., Dardalhon, V., Cesses, P., Garnier, L., Pouzolles, M., Brulin, B., 2016. Intestinal epithelial tuft cells initiate type 2 mucosal immunity to helminth parasites. Nature 529, 226-230.

Geremia, A., Arancibia-Cárcamo, C.V., 2017. Innate lymphoid cells in intestinal inflammation. Front. Immunol. 8, 1296.

Ghaedi, M., Takei, F., 2021. Innate lymphoid cell development. J. Allergy Clin. Immunol. 147, 1549-1560.

Godinho-Silva, C., Domingues, R.G., Rendas, M., Raposo, B., Ribeiro, H., da Silva, J.A., Vieira, A., Costa, R.M., Barbosa-Morais, N.L., Carvalho, T., 2019. Light-entrained and brain-tuned circadian circuits regulate ILC3s and gut homeostasis. Nature 574, 254-258.

Gong, J., Chehrazi-Raffle, A., Reddi, S., Salgia, R., 2018. Development of PD-1 and PD-L1 inhibitors as a form of cancer immunotherapy: a comprehensive review of registration trials and future considerations. J. Immunother. Cancer 6, 8.

Gonsalves, N., 2019. Eosinophilic gastrointestinal disorders. Clin. Rev. Allergy Immunol. 57, 272-285.

Green, P.H.R., Jabri, B., 2003. Coeliac disease. Lancet 362, 383-391.

Grivennikov, S., Karin, E., Terzic, J., Mucida, D., Yu, G.Y., Vallabhapurapu, S., Scheller, J., Rose-John, S., Cheroutre, H., Eckmann, L., 2009. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Canc. Cell 15, 103-113.

Grivennikov, S.I., Wang, K., Mucida, D., Stewart, C.A., Schnabl, B., Jauch, D., Taniguchi, K., Yu, G.Y., Osterreicher, C.H., Hung, K.E., 2012. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 491, 254-258.

Gronke, K., Hernandez, P.P., Zimmermann, J., Klose, C.S.N., Kofoed-Branzk, M., Guendel, F., Witkowski, M., Tizian, C., Amann, L., Schumacher, F., 2019. Interleukin-22 protects intestinal stem cells against genotoxic stress. Nature 566, 249-253.

Gury-BenAri, M., Thaiss, C.A., Serafini, N., Winter, D.R., Giladi, A., Lara-Astiaso, D., Levy, M., Salame, T.M., Weiner, A., David, E., 2016. The spectrum and regulatory landscape of intestinal innate lymphoid cells are shaped by the microbiome. Cell 166, 1231-1246. e13.

Hanahan, D., Weinberg, R.A., 2011. Hallmarks of cancer: the next generation. Cell 144, 646-674.

Hayakawa, Y., Wang, T.C., 2018. The Tuft Cell-ILC2 circuit integrates intestinal defense and homeostasis. Cell 174, 251-253.

Huber, S., Gagliani, N., Zenewicz, L.A., Huber, F.J., Bosurgi, L., Hu, B., Hedl, M., Zhang, W., O'Connor, W., Murphy, A.J., 2012. IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 491, 259-263.

Jiao, Y., Wu, L., Huntington, N.D., Zhang, X., 2020. Crosstalk between gut microbiota and innate immunity and its implication in autoimmune diseases. Front. Immunol. 11, 282.

Jobin, G., Rodriguez-Suarez, R., Betito, K., 2017. Association between natural killer cell activity and colorectal cancer in high-risk subjects undergoing colonoscopy. Gastroenterology 153, 980-987.

Judd, L.M., Heine, R.G., Menheniott, T.R., Buzzelli, J., O'Brien-Simpson, N., Pavlic, D., O'Connor, L., Al Gazali, K., Hamilton, O., Scurr, M., 2016. Elevated IL-33 expression is associated with pediatric eosinophilic esophagitis, and exogenous IL-33 promotes eosinophilic esophagitis development in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 310, G13-G25.

Kirchberger, S., Royston, D.J., Boulard, O., Thornton, E., Franchini, F., Szabady, R.L., Harrison, O., Powrie, F., 2013. Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model. J. Exp. Med. 210, 917-931.

Kooy-Winkelaar, Y., Schmitz, F., Mearin, M.L., Bouma, G., Mulder, C.J., Koning, F., van Bergen, J., Sa1772 ILC-like lymphomas in refractory celiac disease type II respond to multiple common γ-chain cytokines and are sensitive to JAK-inhibitors. Gastroenterology 148, S-328.

Kortekaas Krohn, I., Shikhagaie, M.M., Golebski, K., Bernink, J.H., Breynaert, C., Creyns, B., Diamant, Z., Fokkens, W.J., Gevaert, P., Hellings, P., 2018. Emerging roles of innate lymphoid cells in inflammatory diseases: clinical implications. Allergy 73, 837-850.

Kotas, M.E., Locksley, R.M., 2018. Why innate lymphoid cells?. Immunity 48, 1081-1090.

Kühn, R., Löhler, J., Rennick, D., Rajewsky, K., Müller, W., 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75, 263-274.

Lasry, A., Zinger, A., Ben-Neriah, Y., 2016. Inflammatory networks underlying colorectal cancer. Nat. Immunol. 17, 230-240.

Lauret, E., Rodrigo, L., 2013. Celiac disease and autoimmune-associated conditions. BioMed Res. Int. 2013, 127589.

Le, D.T., Uram, J.N., Wang, H., Bartlett, B.R., Kemberling, H., Eyring, A.D., Skora, A.D., Luber, B.S., Azad, N.S., Laheru, D., 2015. PD-1 blockade in tumors with mismatch-repair deficiency. N. Engl. J. Med. 372, 2509-2520.

Lehmann, F.M., von Burg, N., Ivanek, R., Teufel, C., Horvath, E., Peter, A., Turchinovich, G., Staehli, D., Eichlisberger, T., Gomez de Aguero, M., 2020. Microbiota-induced tissue signals regulate ILC3-mediated antigen presentation. Nat. Commun. 11, 1794.

Li, J., Glover, S.C., 2018. Innate lymphoid cells in inflammatory bowel disease. Arch. Immunol. Ther. Exp. 66, 415-421.

Lichtenstern, C.R., Ngu, R.K., Shalapour, S., Karin, M., 2020. Immunotherapy, inflammation and colorectal cancer. Cells 9, 618.

Lindemans, C.A., Calafiore, M., Mertelsmann, A.M., O'Connor, M.H., Dudakov, J.A., Jenq, R.R., Velardi, E., Young, L.F., Smith, O.M., Lawrence, G., 2015. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature 528, 560-564.

Loyon, R., Jary, M., Salomé, B., Gomez-Cadena, A., Galaine, J., Kroemer, M., Romero, P., Trabanelli, S., Adotévi, O., Borg, C., 2019. Peripheral innate lymphoid cells are increased in first line metastatic colorectal carcinoma patients: a negative correlation with Th1 immune responses. Front. Immunol. 10, 2121.

Luci, C., Vieira, E., Perchet, T., Gual, P., Golub, R., 2019. Natural killer cells and type 1 innate lymphoid cells are new actors in non-alcoholic fatty liver disease. Front. Immunol. 10, 1192.

Manuzak, J., Dillon, S., Wilson, C., 2012. Differential interleukin-10 (IL-10) and IL-23 production by human blood monocytes and dendritic cells in response to commensal enteric bacteria. Clin. Vaccine Immunol. 19, 1207-1217.

Marafini, I., Monteleone, I., Di Fusco, D., Cupi, M.L., Paoluzi, O.A., Colantoni, A., Ortenzi, A., Izzo, R., Vita, S., De Luca, E., 2015. TNF-α producing innate lymphoid cells (ILCs) are increased in active celiac disease and contribute to promote intestinal atrophy in mice. PLoS One 10, e0126291.

Markman, J.L., Shiao, S.L., 2015. Impact of the immune system and immunotherapy in colorectal cancer. J. Gastrointest. Oncol. 6, 208-223.

Marmol, I., Sanchez-de-Diego, C., Pradilla Dieste, A., Cerrada, E., Rodriguez Yoldi, M.J., 2017. Colorectal carcinoma: a general overview and future perspectives in colorectal cancer. Int. J. Mol. Sci. 18, 197-236.

Melo-Gonzalez, F., Kammoun, H., Evren, E., Dutton, E.E., Papadopoulou, M., Bradford, B.M., Tanes, C., Fardus-Reid, F., Swann, J.R., Bittinger, K., 2019. Antigen-presenting ILC3 regulate T cell-dependent IgA responses to colonic mucosal bacteria. J. Exp. Med. 216, 728-742.

Moral, J.A., Leung, J., Rojas, L.A., Ruan, J., Zhao, J., Sethna, Z., Ramnarain, A., Gasmi, B., Gururajan, M., Redmond, D., 2020. ILC2s amplify PD-1 blockade by activating tissue-specific cancer immunity. Nature 579, 130-135.

Morita, H., Moro, K., Koyasu, S., 2016. Innate lymphoid cells in allergic and nonallergic inflammation. J. Allergy Clin. Immunol. 138, 1253-1264.

Nussbaum, J.C., Van Dyken, S.J., von Moltke, J., Cheng, L.E., Mohapatra, A., Molofsky, A.B., Thornton, E.E., Krummel, M.F., Chawla, A., Liang, H.E., 2013. Type 2 innate lymphoid cells control eosinophil homeostasis. Nature 502, 245-248.

Ohne, Y., 2020. OMIP-066: identification of novel subpopulations of human group 2 innate lymphoid cells in peripheral blood. Cytometry 97, 1028-1031.

Pasha, M.A., Patel, G., Hopp, R., Yang, Q., 2019. Role of innate lymphoid cells in allergic diseases. Allergy Asthma Proc. 40, 138-145.

Pearson, C., Thornton, E.E., McKenzie, B., Schaupp, A.L., Huskens, N., Griseri, T., West, N., Tung, S., Seddon, B.P., Uhlig, H.H., 2016. ILC3 GM-CSF production and mobilisation orchestrate acute intestinal inflammation. Elife 5, e10066.

Pelczar, P., Witkowski, M., Perez, L.G., Kempski, J., Hammel, A.G., Brockmann, L., Kleinschmidt, D., Wende, S., Haueis, C., Bedke, T., 2016. A pathogenic role for T cell–derived IL-22BP in inflammatory bowel disease. Science 354, 358-362.

Priscilla, C., Brenna, H., Oswaldo, A., Jason, K., Brian, M., Raffaele, G., Jason, H., Cal, M., Michael, Z., Thomas, F., 2017. Innate lymphoid cells are dysregulated after intestinal transplantation and play a critical role in regulating allograft homeostasis. Transplantation 101, S63.

Rao, A., Strauss, O., Kokkinou, E., Bruchard, M., Tripathi, K.P., Schlums, H., Carrasco, A., Mazzurana, L., Konya, V., Villablanca, E.J., 2020. Cytokines regulate the antigen-presenting characteristics of human circulating and tissue-resident intestinal ILCs. Nat. Commun. 11, 2049.

Robinette, M.L., Colonna, M., 2016. Immune modules shared by innate lymphoid cells and T cells. J. Allergy Clin. Immunol. 138, 1243-1251.

Robinette, M.L., Colonna, M., 2016. Innate lymphoid cells and the MHC. HLA 87, 5-11.

Rolot, M., O'Sullivan, T.E., 2020. Living with yourself: innate lymphoid cell immunometabolism. Cells 9, 334.

Rothenberg, M.E., 2004. Eosinophilic gastrointestinal disorders (EGID). J. Allergy Clin. Immunol. 113, 11-28.

Salimi, M., Wang, R., Yao, X., Li, X., Wang, X., Hu, Y., Chang, X., Fan, P., Dong, T., Ogg, G., 2018. Activated innate lymphoid cell populations accumulate in human tumour tissues. BMC Canc. 18, 341-350.

Seehus, C.R., Kadavallore, A., Torre, B.d.l., Yeckes, A.R., Wang, Y., Tang, J., Kaye, J., 2017. Alternative activation generates IL-10 producing type 2 innate lymphoid cells. Nat. Commun. 8, 1900.

Seliger, B., Ruiz-Cabello, F., Garrido, F., 2008. IFN inducibility of major histocompatibility antigens in tumors. Adv. Cancer Res. 101, 249-276.

Shoda, T., Matsuda, A., Arai, K., Shimizu, H., Morita, H., Orihara, K., Okada, N., Narita, M., Ohya, Y., Saito, H., 2016. Sera of patients with infantile eosinophilic gastroenteritis showed a specific increase in both thymic stromal lymphopoietin and IL-33 levels. J. Allergy Clin. Immunol. 138, 299-303.

Simoni, Y., Fehlings, M., Kloverpris, H.N., McGovern, N., Koo, S.L., Loh, C.Y., Lim, S., Kurioka, A., Fergusson, J.R., Tang, C.L., 2017. Human innate lymphoid cell subsets possess tissue-type based heterogeneity in phenotype and frequency. Immunity 46, 148-161.

Sonnenberg, G.F., 2014. Regulation of intestinal health and disease by innate lymphoid cells. Int. Immunol. 26, 501-507.

Taylor, S., Huang, Y., Mallett, G., Stathopoulou, C., Felizardo, T.C., Sun, M.A., Martin, E.L., Zhu, N., Woodward, E.L., Elias, M.S., 2017. PD-1 regulates KLRG1+ group 2 innate lymphoid cells. J. Exp. Med. 214, 1663-1678.

Uhde, M., Yu, X., Bunin, A., Brauner, C., Lewis, S.K., Lebwohl, B., Krishnareddy, S., Alaedini, A., Reizis, B., Ghosh, S., 2020. Phenotypic shift of small intestinal intra-epithelial type 1 innate lymphoid cells in celiac disease is associated with enhanced cytotoxic potential. Clin. Exp. Immunol. 200, 163-175.

Verdu, E.F., Galipeau, H.J., Jabri, B., 2015. Novel players in coeliac disease pathogenesis: role of the gut microbiota. Nat. Rev. Gastroenterol. Hepatol. 12, 497-506.

Vivier, E., Artis, D., Colonna, M., Diefenbach, A., Di Santo, J.P., Eberl, G., Koyasu, S., Locksley, R.M., McKenzie, A.N.J., Mebius, R.E., 2018. Innate lymphoid cells: 10 years on. Cell 174, 1054-1066.

von Burg, N., Chappaz, S., Baerenwaldt, A., Horvath, E., Bose Dasgupta, S., Ashok, D., Pieters, J., Tacchini-Cottier, F., Rolink, A., Acha-Orbea, H., 2014. Activated group 3 innate lymphoid cells promote T-cell-mediated immune responses. Proc. Natl. Acad. Sci. U. S. A. 111, 12835-12840.

Waldmann, T.A., 2018. Cytokines in cancer immunotherapy. Cold Spring Harb. Perspect. Biol. 10, a028472.

Wallrapp, A., Riesenfeld, S.J., Burkett, P.R., Abdulnour, R.E., Nyman, J., Dionne, D., Hofree, M., Cuoco, M.S., Rodman, C., Farouq, D., 2017. The neuropeptide NMU amplifies ILC2-driven allergic lung inflammation. Nature 549, 351-356.

Wang, S., Qu, Y., Xia, P., Chen, Y., Zhu, X., Zhang, J., Wang, G., Tian, Y., Ying, J., Fan, Z., 2020. Transdifferentiation of tumor infiltrating innate lymphoid cells during progression of colorectal cancer. Cell Res. 30, 610-622.

Wang, S., Xia, P., Chen, Y., Qu, Y., Xiong, Z., Ye, B., Du, Y., Tian, Y., Yin, Z., Xu, Z., 2017. Regulatory innate lymphoid cells control innate intestinal inflammation. Cell 171, 201-216. e218.

Yaghoubi, N., Soltani, A., Ghazvini, K., Hassanian, S.M., Hashemy, S.I., 2019. PD-1/PD-L1 blockade as a novel treatment for colorectal cancer. Biomed. Pharmacother. 110, 312-318.

Zhong, C., Zheng, M., Zhu, J., 2018. Lymphoid tissue inducer-A divergent member of the ILC family. Cytokine Growth Factor Rev. 42, 5-12.

Zhou, L., Sonnenberg, G.F., 2018. Essential immunologic orchestrators of intestinal homeostasis. Sci. Immunol. 3, eaao1605.

Relative Articles

Supplements(0)

Cited By

Proportional views