Adipose Type One Innate Lymphoid Cells Regulate Macrophage Homeostasis through Targeted Cytotoxicity

Immunity

Volumn 46, Issue 2, 2017, Pages 273-286

  Boulenouar, Selma ^a,b   Michelet, Xavier ^a,b   Duquette, Danielle ^a   Alvarez, David ^b   Hogan, Andrew E ^c   Dold, Christina ^d   O'Connor, Donal ^c   Stutte, Suzanne ^b   Tavakkoli, Ali ^a   Winters, Desmond ^c   Exley, Mark A ^a   O'Shea, Donal ^c   Brenner, Michael B ^a   von Andrian, Ulrich ^b   Lynch, Lydia ^a,b,d  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c ST VINCENT S UNIVERSITY HOSPITAL   (Ireland)

^d TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

adipose tissue; cytotoxicity; macrophages; metabolism; NK cells; obesity

Indexed keywords

CYTOKINE; PERFORIN; TRANSCRIPTION FACTOR T BET;

ADIPOSE TISSUE; ADIPOSE TYPE 1 INNATE LYMPHOID CELL; ADOPTIVE TRANSFER; AGED; ANIMAL TISSUE; ARTICLE; CELL KILLING; CELL MIGRATION; CONTROLLED STUDY; CYTOTOXICITY; DIET INDUCED OBESITY; DIET RESTRICTION; FEMALE; HOMEOSTASIS; HUMAN; HUMAN TISSUE; LIPID DIET; LYMPHOID CELL; MACROPHAGE; MALE; METABOLIC DISORDER; MOUSE; NONHUMAN; PARABIOSIS; PRIORITY JOURNAL; STEADY STATE; WEIGHT REDUCTION; ANIMAL; C57BL MOUSE; CYTOLOGY; IMMUNOLOGY; INNATE IMMUNITY; LYMPHOCYTE; OBESITY; PATHOLOGY;

ADIPOSE TISSUE; ANIMALS; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; HOMEOSTASIS; HUMANS; IMMUNITY, INNATE; LYMPHOCYTES; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; OBESITY;

EID: 85013967225     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2017.01.008     Document Type: Article

References (51)

1. Amano, S.U., Cohen, J.L., Vangala, P., Tencerova, M., Nicoloro, S.M., Yawe, J.C., Shen, Y., Czech, M.P., Aouadi, M., Local proliferation of macrophages contributes to obesity-associated adipose tissue inflammation. Cell Metab. 19 (2014), 162–171.
2. Bellora, F., Castriconi, R., Dondero, A., Reggiardo, G., Moretta, L., Mantovani, A., Moretta, A., Bottino, C., The interaction of human natural killer cells with either unpolarized or polarized macrophages results in different functional outcomes. Proc. Natl. Acad. Sci. USA 107 (2010), 21659–21664.
3. 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., et al. Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat. Immunol. 14 (2013), 221–229.
4. Bernink, J.H., Krabbendam, L., Germar, K., de Jong, E., Gronke, K., Kofoed-Nielsen, M., Munneke, J.M., Hazenberg, M.D., Villaudy, J., Buskens, C.J., et al. Interleukin-12 and -23 control plasticity of CD127(+) group 1 and group 3 innate lymphoid cells in the intestinal lamina propria. Immunity 43 (2015), 146–160.
5. Björkström, N.K., Ljunggren, H.-G., Michaëlsson, J., Emerging insights into natural killer cells in human peripheral tissues. Nat. Rev. Immunol. 16 (2016), 310–320.
6. Boulenouar, S., Doisne, J.M., Sferruzzi-Perri, A., Gaynor, L.M., Kieckbusch, J., Balmas, E., Yung, H.W., Javadzadeh, S., Volmer, L., Hawkes, D.A., et al. The residual innate lymphoid cells in NFIL3-deficient mice support suboptimal maternal adaptations to pregnancy. Front. Immunol., 7, 2016, 43.
7. Brestoff, J.R., Artis, D., Immune regulation of metabolic homeostasis in health and disease. Cell 161 (2015), 146–160.
8. Brestoff, J.R., Kim, B.S., Saenz, S.A., Stine, R.R., Monticelli, L.A., Sonnenberg, G.F., Thome, J.J., Farber, D.L., Lutfy, K., Seale, P., Artis, D., Group 2 innate lymphoid cells promote beiging of white adipose tissue and limit obesity. Nature 519 (2015), 242–246.
9. Chiossone, L., Chaix, J., Fuseri, N., Roth, C., Vivier, E., Walzer, T., Maturation of mouse NK cells is a 4-stage developmental program. Blood 113 (2009), 5488–5496.
10. Chung, J.J., Markiewicz, M.A., Polić, B., Shaw, A.S., Role of NKG2D in obesity-induced adipose tissue inflammation and insulin resistance. PLoS ONE, 9, 2014, e110108.
11. Cortez, V.S., Colonna, M., Diversity and function of group 1 innate lymphoid cells. Immunol. Lett. 179 (2016), 19–24.
12. Cortez, V.S., Fuchs, A., Cella, M., Gilfillan, S., Colonna, M., Cutting edge: Salivary gland NK cells develop independently of Nfil3 in steady-state. J. Immunol. 192 (2014), 4487–4491.
13. Cortez, V.S., Cervantes-Barragan, L., Robinette, M.L., Bando, J.K., Wang, Y., Geiger, T.L., Gilfillan, S., Fuchs, A., Vivier, E., Sun, J.C., et al. Transforming growth factor-β signaling guides the differentiation of innate lymphoid cells in salivary glands. Immunity 44 (2016), 1127–1139.
14. Daussy, C., Faure, F., Mayol, K., Viel, S., Gasteiger, G., Charrier, E., Bienvenu, J., Henry, T., Debien, E., Hasan, U.A., et al. T-bet and Eomes instruct the development of two distinct natural killer cell lineages in the liver and in the bone marrow. J. Exp. Med. 211 (2014), 563–577.
15. Diefenbach, A., Colonna, M., Koyasu, S., Development, differentiation, and diversity of innate lymphoid cells. Immunity 41 (2014), 354–365.
16. Exley, M.A., Hand, L., O'Shea, D., Lynch, L., Interplay between the immune system and adipose tissue in obesity. J. Endocrinol. 223 (2014), R41–R48.
17. Feuerer, M., Herrero, L., Cipolletta, D., Naaz, A., Wong, J., Nayer, A., Lee, J., Goldfine, A.B., Benoist, C., Shoelson, S., Mathis, D., Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat. Med. 15 (2009), 930–939.
18. Finotto, S., Neurath, M.F., Glickman, J.N., Qin, S., Lehr, H.A., Green, F.H., Ackerman, K., Haley, K., Galle, P.R., Szabo, S.J., et al. Development of spontaneous airway changes consistent with human asthma in mice lacking T-bet. Science 295 (2002), 336–338.
19. Fischer-Posovszky, P., Wang, Q.A., Asterholm, I.W., Rutkowski, J.M., Scherer, P.E., Targeted deletion of adipocytes by apoptosis leads to adipose tissue recruitment of alternatively activated M2 macrophages. Endocrinology 152 (2011), 3074–3081.
20. Gordon, S.M., Chaix, J., Rupp, L.J., Wu, J., Madera, S., Sun, J.C., Lindsten, T., Reiner, S.L., The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity 36 (2012), 55–67.
21. Hotamisligil, G.S., Shargill, N.S., Spiegelman, B.M., Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259 (1993), 87–91.
22. Ji, Y., Sun, S., Xu, A., Bhargava, P., Yang, L., Lam, K.S., Gao, B., Lee, C.H., Kersten, S., Qi, L., Activation of natural killer T cells promotes M2 macrophage polarization in adipose tissue and improves systemic glucose tolerance via interleukin-4 (IL-4)/STAT6 protein signaling axis in obesity. J. Biol. Chem. 287 (2012), 13561–13571.
23. Kägi, D., Ledermann, B., Bürki, K., Seiler, P., Odermatt, B., Olsen, K.J., Podack, E.R., Zinkernagel, R.M., Hengartner, H., Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369 (1994), 31–37.
24. Kahn, B.B., Flier, J.S., Obesity and insulin resistance. J. Clin. Invest. 106 (2000), 473–481.
25. Kamizono, S., Duncan, G.S., Seidel, M.G., Morimoto, A., Hamada, K., Grosveld, G., Akashi, K., Lind, E.F., Haight, J.P., Ohashi, P.S., et al. Nfil3/E4bp4 is required for the development and maturation of NK cells in vivo. J. Exp. Med. 206 (2009), 2977–2986.
26. Kanneganti, T.D., Dixit, V.D., Immunological complications of obesity. Nat. Immunol. 13 (2012), 707–712.
27. Kosteli, A., Sugaru, E., Haemmerle, G., Martin, J.F., Lei, J., Zechner, R., Ferrante, A.W. Jr., Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue. J. Clin. Invest. 120 (2010), 3466–3479.
28. Lapaque, N., Walzer, T., Méresse, S., Vivier, E., Trowsdale, J., Interactions between human NK cells and macrophages in response to Salmonella infection. J. Immunol. 182 (2009), 4339–4348.
29. Lee, B.C., Kim, M.S., Pae, M., Yamamoto, Y., Eberlé, D., Shimada, T., Kamei, N., Park, H.S., Sasorith, S., Woo, J.R., et al. Adipose natural killer cells regulate adipose tissue macrophages to promote insulin resistance in obesity. Cell Metab. 23 (2016), 685–698.
30. Lumeng, C.N., Bodzin, J.L., Saltiel, A.R., Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 117 (2007), 175–184.
31. Lynch, L., O'Shea, D., Winter, D.C., Geoghegan, J., Doherty, D.G., O'Farrelly, C., Invariant NKT cells and CD1d(+) cells amass in human omentum and are depleted in patients with cancer and obesity. Eur. J. Immunol. 39 (2009), 1893–1901.
32. Lynch, L.A., O'Connell, J.M., Kwasnik, A.K., Cawood, T.J., O'Farrelly, C., O'Shea, D.B., Are natural killer cells protecting the metabolically healthy obese patient?. Obesity (Silver Spring) 17 (2009), 601–605.
33. Lynch, L., Nowak, M., Varghese, B., Clark, J., Hogan, A.E., Toxavidis, V., Balk, S.P., O'Shea, D., O'Farrelly, C., Exley, M.A., Adipose tissue invariant NKT cells protect against diet-induced obesity and metabolic disorder through regulatory cytokine production. Immunity 37 (2012), 574–587.
34. Lynch, L., Michelet, X., Zhang, S., Brennan, P.J., Moseman, A., Lester, C., Besra, G., Vomhof-Dekrey, E.E., Tighe, M., Koay, H.F., et al. Regulatory iNKT cells lack expression of the transcription factor PLZF and control the homeostasis of T(reg) cells and macrophages in adipose tissue. Nat. Immunol. 16 (2015), 85–95.
35. Michel, T., Hentges, F., Zimmer, J., Consequences of the crosstalk between monocytes/macrophages and natural killer cells. Front. Immunol., 3, 2013, 403.
36. Nedvetzki, S., Sowinski, S., Eagle, R.A., Harris, J., Vély, F., Pende, D., Trowsdale, J., Vivier, E., Gordon, S., Davis, D.M., Reciprocal regulation of human natural killer cells and macrophages associated with distinct immune synapses. Blood 109 (2007), 3776–3785.
37. O'Sullivan, T.E., Rapp, M., Fan, X., Weizman, O.E., Bhardwaj, P., Adams, N.M., Walzer, T., Dannenberg, A.J., Sun, J.C., Adipose-resident group 1 innate lymphoid cells promote obesity-associated insulin resistance. Immunity 45 (2016), 428–441.
38. Peng, H., Jiang, X., Chen, Y., Sojka, D.K., Wei, H., Gao, X., Sun, R., Yokoyama, W.M., Tian, Z., Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J. Clin. Invest. 123 (2013), 1444–1456.
39. Raulet, D.H., Gasser, S., Gowen, B.G., Deng, W., Jung, H., Regulation of ligands for the NKG2D activating receptor. Annu. Rev. Immunol. 31 (2013), 413–441.
40. Reinhardt, R.L., Liang, H.E., Locksley, R.M., Cytokine-secreting follicular T cells shape the antibody repertoire. Nat. Immunol. 10 (2009), 385–393.
41. Rosen, E.D., Spiegelman, B.M., What we talk about when we talk about fat. Cell 156 (2014), 20–44.
42. Schipper, H.S., Rakhshandehroo, M., van de Graaf, S.F., Venken, K., Koppen, A., Stienstra, R., Prop, S., Meerding, J., Hamers, N., Besra, G., et al. Natural killer T cells in adipose tissue prevent insulin resistance. J. Clin. Invest. 122 (2012), 3343–3354.
43. Seillet, C., Belz, G.T., Differentiation and diversity of subsets in group 1 innate lymphoid cells. Int. Immunol. 28 (2016), 3–11.
44. Serafini, N., Vosshenrich, C.A.J., Di Santo, J.P., Transcriptional regulation of innate lymphoid cell fate. Nat. Rev. Immunol. 15 (2015), 415–428.
45. Sojka, D.K., Plougastel-Douglas, B., Yang, L., Pak-Wittel, M.A., Artyomov, M.N., Ivanova, Y., Zhong, C., Chase, J.M., Rothman, P.B., Yu, J., et al. Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells. eLife, 3, 2014, e01659.
46. Spits, H., Bernink, J.H., Lanier, L., NK cells and type 1 innate lymphoid cells: partners in host defense. Nat. Immunol. 17 (2016), 758–764.
47. Sun, K., Kusminski, C.M., Scherer, P.E., Adipose tissue remodeling and obesity. J. Clin. Invest. 121 (2011), 2094–2101.
48. Vosshenrich, C.A., Samson-Villéger, S.I., Di Santo, J.P., Distinguishing features of developing natural killer cells. Curr. Opin. Immunol. 17 (2005), 151–158.
49. Wensveen, F.M., Jelenčić, V., Valentić, S., Šestan, M., Wensveen, T.T., Theurich, S., Glasner, A., Mendrila, D., Štimac, D., Wunderlich, F.T., et al. NK cells link obesity-induced adipose stress to inflammation and insulin resistance. Nat. Immunol. 16 (2015), 376–385.
50. Wu, D., Molofsky, A.B., Liang, H.E., Ricardo-Gonzalez, R.R., Jouihan, H.A., Bando, J.K., Chawla, A., Locksley, R.M., Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 332 (2011), 243–247.
51. Xu, X., Grijalva, A., Skowronski, A., van Eijk, M., Serlie, M.J., Ferrante, A.W. Jr., Obesity activates a program of lysosomal-dependent lipid metabolism in adipose tissue macrophages independently of classic activation. Cell Metab. 18 (2013), 816–830.