Abstract
Organs in our body have formed their own unique immune surveillance system that is finely tuned by in situ milieu. Sequestrated tissue-resident immune cells differ from their counterparts in circulation and participate in tissue physiological activities and the maintenance of local homeostasis. Dysregulation of regional immunity leads to organ-specific inflammatory injuries. Here we review the recent developments in the field of tissue-resident immune cells and organ-specific regional immunity, and discuss their clinical implication.
Similar content being viewed by others
References
Acharya, C., Sahingur, S.E., and Bajaj, J.S. (2017). Microbiota, cirrhosis, and the emerging oral-gut-liver axis. JCI Insight 2, pii: 94416.
Agace, W.W., and McCoy, K.D. (2017). Regionalized development and maintenance of the intestinal adaptive immune landscape. Immunity 46, 532–548.
Amit, I., Winter, D.R., and Jung, S. (2016). The role of the local environment and epigenetics in shaping macrophage identity and their effect on tissue homeostasis. Nat Immunol 17, 18–25.
Barabino, S., Chen, Y., Chauhan, S., and Dana, R. (2012). Ocular surface immunity: Homeostatic mechanisms and their disruption in dry eye disease. Prog Retinal Eye Res 31, 271–285.
Bassaganya-Riera, J., Dominguez-Bello, M.G., Kronsteiner, B., Carbo, A., Lu, P., Viladomiu, M., Pedragosa, M., Zhang, X., Sobral, B.W., Mane, S.P., Mohapatra, S.K., Horne, W.T., Guri, A.J., Groeschl, M., Lopez-Velasco, G., and Hontecillas, R. (2012). Helicobacter pylori colonization ameliorates glucose homeostasis in mice through a PPAR γ-dependent mechanism. PLoS ONE 7, e50069.
Berg, E.L., Yoshino, T., Rott, L.S., Robinson, M.K., Warnock, R.A., Kishimoto, T.K., Picker, L.J., and Butcher, E.C. (1991). The cutaneous lymphocyte antigen is a skin lymphocyte homing receptor for the vascular lectin endothelial cell-leukocyte adhesion molecule 1. J Exp Med 174, 1461–1466.
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., Bemelman, W.A., Mjösberg, J.M., and Spits, H. (2013). Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat Immunol 14, 221–229.
Bielekova, B., Catalfamo, M., Reichert-Scrivner, S., Packer, A., Cerna, M., Waldmann, T.A., McFarland, H., Henkart, P.A., and Martin, R. (2006). Regulatory CD56bright natural killer cells mediate immunomodulatory effects of IL-2R-targeted therapy (daclizumab) in multiple sclerosis. Proc Natl Acad Sci USA 103, 5941–5946.
Budden, K.F., Gellatly, S.L., Wood, D.L.A., Cooper, M.A., Morrison, M., Hugenholtz, P., and Hansbro, P.M. (2017). Emerging pathogenic links between microbiota and the gut-lung axis. Nat Rev Micro 15, 55–63.
Burzyn, D., Benoist, C., and Mathis, D. (2013a). Regulatory T cells in nonlymphoid tissues. Nat Immunol 14, 1007–1013.
Burzyn, D., Kuswanto, W., Kolodin, D., Shadrach, J.L., Cerletti, M., Jang, Y., Sefik, E., Tan, T.G., Wagers, A.J., Benoist, C., and Mathis, D. (2013b). A special population of regulatory T cells potentiates muscle repair. Cell 155, 1282–1295.
Caforio, A.L.P., Mahon, N.J., Tona, F., and McKenna, W.J. (2002). Circulating cardiac autoantibodies in dilated cardiomyopathy and myocarditis: pathogenetic and clinical significance. Eur J Heart Failure 4, 411–417.
Campbell, J.J., Haraldsen, G., Pan, J., Rottman, J., Qin, S., Ponath, P., Andrew, D.P., Warnke, R., Ruffing, N., Kassam, N., Wu, L., and Butcher, E.C. (1999). The chemokine receptor CCR4 in vascular recognition by cutaneous but not intestinal memory T cells. Nature 400, 776–780.
Caspi, R.R. (2010). A look at autoimmunity and inflammation in the eye. J Clin Invest 120, 3073–3083.
Cauley, L.S. (2016). Environmental cues orchestrate regional immune surveillance and protection by pulmonary CTLs. J Leukoc Biol 100, 905–912.
Cipolletta, D., Cohen, P., Spiegelman, B.M., Benoist, C., and Mathis, D. (2015). Appearance and disappearance of the mRNA signature characteristic of Treg cells in visceral adipose tissue: Age, diet, and PPARγ effects. Proc Natl Acad Sci USA 112, 482–487.
Cipolletta, D., Feuerer, M., Li, A., Kamei, N., Lee, J., Shoelson, S.E., Benoist, C., and Mathis, D. (2012). PPAR-gamma is a major driver of the accumulation and phenotype of adipose tissue Treg cells. Nature 486, 549-553.
Clark, R.A. (2015). Resident memory T cells in human health and disease. Sci Transl Med 7, 269rv1.
Codarri, L., Greter, M., and Becher, B. (2013). Communication between pathogenic T cells and myeloid cells in neuroinflammatory disease. Trends Immunol 34, 114–119.
Colombo, E., and Farina, C. (2016). Astrocytes: key regulators of neuroinflammation. Trends Immunol 37, 608–620.
Curato, C., Slavic, S., Dong, J., Skorska, A., Altarche-Xifro, W., Miteva, K., Kaschina, E., Thiel, A., Imboden, H., Wang, J., Steckelings, U., Steinhoff, G., Unger, T., and Li, J. (2010). Identification of noncytotoxic and IL-10-producing CD8+AT2R+ T cell population in response to ischemic heart injury. J Immunol 185, 6286–6293.
de Heer, H.J., Hammad, H., Soullié, T., Hijdra, D., Vos, N., Willart, M.A.M., Hoogsteden, H.C., and Lambrecht, B.N. (2004). Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J Exp Med 200, 89–98.
Dickson, R.P., Erb-Downward, J.R., Martinez, F.J., and Huffnagle, G.B. (2016). The microbiome and the respiratory tract. Annu Rev Physiol 78, 481–504.
Dudda, J.C., Perdue, N., Bachtanian, E., and Campbell, D.J. (2008). Foxp3+ regulatory T cells maintain immune homeostasis in the skin. J Exp Med 205, 1559–1565.
Dyring-Andersen, B., Geisler, C., Agerbeck, C., Lauritsen, J.P.H., Gúdjonsdottir, S.D., Skov, L., and Bonefeld, C.M. (2014). Increased number and frequency of group 3 innate lymphoid cells in nonlesional psoriatic skin. Br J Dermatol 170, 609–616.
Eberl, G., Colonna, M., Di Santo, J.P., and McKenzie, A.N. (2015). Innate lymphoid cells. Innate lymphoid cells: a new paradigm in immunology. Science 348, aaa6566.
Epelman, S., Liu, P.P., and Mann, D.L. (2015). Role of innate and adaptive immune mechanisms in cardiac injury and repair. Nat Rev Immunol 15, 117–129.
Ernandez, T., and Mayadas, T.N. (2016). The changing landscape of renal inflammation. Trends Mol Med 22, 151–163.
Fabrizi, M., Marchetti, V., Mavilio, M., Marino, A., Casagrande, V., Cavalera, M., Moreno-Navarrete, J.M., Mezza, T., Sorice, G.P., Fiorentino, L., Menghini, R., Lauro, R., Monteleone, G., Giaccari, A., Fernandez Real, J.M., and Federici, M. (2014). IL-21 is a major negative regulator of IRF4-dependent lipolysis affecting Tregs in adipose tissue and systemic insulin sensitivity. Diabetes 63, 2086–2096.
Fagarasan, S., Kawamoto, S., Kanagawa, O., and Suzuki, K. (2010). Adaptive immune regulation in the gut: T cell-dependent and T cell-independent IgA synthesis. Annu Rev Immunol 28, 243–273.
Feuerer, M., Herrero, L., Cipolletta, D., Naaz, A., Wong, J., Nayer, A., Lee, J., Goldfine, A.B., Benoist, C., Shoelson, S., and Mathis, D. (2009). Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med 15, 930–939.
Fu, B., and Wei, H. (2016). Decidual natural killer cells and the immune microenvironment at the maternal-fetal interface. Sci China Life Sci 59, 1224–1231.
Fujii, T. (2014). Direct and indirect pathogenic of autoantibodies in systemic autoimmune diseases. Allergol Int 63, 515–522.
Geuking, M.B., Cahenzli, J., Lawson, M.A.E., Ng, D.C.K., Slack, E., Hapfelmeier, S., McCoy, K.D., and Macpherson, A.J. (2011). Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity 34, 794–806.
Grégoire, C., Chasson, L., Luci, C., Tomasello, E., Geissmann, F., Vivier, E., and Walzer, T. (2007). The trafficking of natural killer cells. Immunol Rev 220, 169–182.
Grosicki, G.J., Fielding, R.A., and Lustgarten, M.S. (2017). Gut microbiota contribute to age-related changes in skeletal muscle size, composition, and function: biological basis for a gut-muscle axis. Calcif Tissue Int, doi: 10.1007/s00223-017-0345-5.
Hams, E., Armstrong, M.E., Barlow, J.L., Saunders, S.P., Schwartz, C., Cooke, G., Fahy, R.J., Crotty, T.B., Hirani, N., Flynn, R.J., Voehringer, D., McKenzie, A.N.J., Donnelly, S.C., and Fallon, P.G. (2014). IL-25 and type 2 innate lymphoid cells induce pulmonary fibrosis. Proc Natl Acad Sci USA 111, 367–372.
Han, C.Z., Juncadella, I.J., Kinchen, J.M., Buckley, M.W., Klibanov, A.L., Dryden, K., Onengut-Gumuscu, S., Erdbrügger, U., Turner, S.D., Shim, Y.M., Tung, K.S., and Ravichandran, K.S. (2016). Macrophages redirect phagocytosis by non-professional phagocytes and influence inflammation. Nature 539, 570–574.
Hashimoto, D., Chow, A., Noizat, C., Teo, P., Beasley, M.B., Leboeuf, M., Becker, C.D., See, P., Price, J., Lucas, D., Greter, M., Mortha, A., Boyer, S.W., Forsberg, E.C., Tanaka, M., van Rooijen, N., García-Sastre, A., Stanley, E.R., Ginhoux, F., Frenette, P.S., and Merad, M. (2013). Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38, 792–804.
Hazenberg, M.D., and Spits, H. (2014). Human innate lymphoid cells. Blood 124, 700–709.
Hegazy, A.N., and Powrie, F. (2015). MICROBIOME. Microbiota RORgulates intestinal suppressor T cells. Science 349, 929-930.
Herz, J., Filiano, A.J., Smith, A., Yogev, N., and Kipnis, J. (2017). Myeloid cells in the central nervous system. Immunity 46, 943–956.
Hofmann, U., and Frantz, S. (2015). Role of lymphocytes in myocardial injury, healing, and remodeling after myocardial infarction. Circulation Res 116, 354–367.
Hofmann, U., and Frantz, S. (2016). Role of T-cells in myocardial infarction. Eur Heart J 37, 873–879.
Homey, B., Alenius, H., Müller, A., Soto, H., Bowman, E.P., Yuan, W., McEvoy, L., Lauerma, A.I., Assmann, T., Bünemann, E., Lehto, M., Wolff, H., Yen, D., Marxhausen, H., To, W., Sedgwick, J., Ruzicka, T., Lehmann, P., and Zlotnik, A. (2002). CCL27-CCR10 interactions regulate T cell-mediated skin inflammation. Nat Med 8, 157–165.
Hong, K.H., Ryu, J., and Han, K.H. (2005). Monocyte chemoattractant protein-1-induced angiogenesis is mediated by vascular endothelial growth factor-A. Blood 105, 1405–1407.
Horai, R., Zárate-Bladés, C.R., Dillenburg-Pilla, P., Chen, J., Kielczewski, J.L., Silver, P.B., Jittayasothorn, Y., Chan, C.C., Yamane, H., Honda, K., and Caspi, R.R. (2015). Microbiota-dependent activation of an autoreactive T cell receptor provokes autoimmunity in an immunologically privileged site. Immunity 43, 343–353.
Hu, S.Y., Jia, X.Y., Li, J.N., Zheng, X., Ao, J., Liu, G., Cui, Z., and Zhao, M.H. (2016). T cell infiltration is associated with kidney injury in patients with anti-glomerular basement membrane disease. Sci China Life Sci 59, 1282–1289.
Huang, D.R., Shi, F.D., Jung, S., Pien, G.C., Wang, J., Salazar-Mather, T.P., He, T.T., Weaver, J.T., Ljunggren, H.G., Biron, C.A., Littman, D.R., and Ransohoff, R.M. (2006). The neuronal chemokine CX3CL1/fractalkine selectively recruits NK cells that modify experimental autoimmune encephalomyelitis within the central nervous system. FASEB J 20, 896–905.
Huang, W., Zhou, L., Guo, H., Xu, Y., and Xu, Y. (2017). The role of shortchain fatty acids in kidney injury induced by gut-derived inflammatory response. Metabolism 68, 20–30.
Intlekofer, A.M., Takemoto, N., Wherry, E.J., Longworth, S.A., Northrup, J.T., Palanivel, V.R., Mullen, A.C., Gasink, C.R., Kaech, S.M., Miller, J.D., Gapin, L., Ryan, K., Russ, A.P., Lindsten, T., Orange, J.S., Goldrath, A.W., Ahmed, R., and Reiner, S.L. (2005). Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat Immunol 6, 1236–1244.
Iwamoto, T., Okamoto, H., Toyama, Y., and Momohara, S. (2008). Molecular aspects of rheumatoid arthritis: chemokines in the joints of patients. FEBS J 275, 4448–4455.
Jiang, X., Clark, R.A., Liu, L., Wagers, A.J., Fuhlbrigge, R.C., and Kupper, T.S. (2012). Skin infection generates non-migratory memory CD8+ TRM cells providing global skin immunity. Nature 483, 227–231.
Kaya, Z., Leib, C., and Katus, H.A. (2012). Autoantibodies in heart failure and cardiac dysfunction. Circulation Res 110, 145–158.
Kayama, H., and Takeda, K. (2012). Regulation of intestinal homeostasis by innate and adaptive immunity. Int Immunol 24, 673–680.
Kim, C.H., Hashimoto-Hill, S., and Kim, M. (2016). Migration and tissue tropism of innate lymphoid cells. Trends Immunol 37, 68–79.
Kiryluk, K., Li, Y., Scolari, F., Sanna-Cherchi, S., Choi, M., Verbitsky, M., Fasel, D., Lata, S., Prakash, S., Shapiro, S., Fischman, C., Snyder, H.J., Appel, G., Izzi, C., Viola, B.F., Dallera, N., Del Vecchio, L., Barlassina, C., Salvi, E., Bertinetto, F.E., Amoroso, A., Savoldi, S., Rocchietti, M., Amore, A., Peruzzi, L., Coppo, R., Salvadori, M., Ravani, P., Magistroni, R., Ghiggeri, G.M., Caridi, G., Bodria, M., Lugani, F., Allegri, L., Delsante, M., Maiorana, M., Magnano, A., Frasca, G., Boer, E., Boscutti, G., Ponticelli, C., Mignani, R., Marcantoni, C., Di Landro, D., Santoro, D., Pani, A., Polci, R., Feriozzi, S., Chicca, S., Galliani, M., Gigante, M., Gesualdo, L., Zamboli, P., Battaglia, G.G., Garozzo, M., Maixnerová, D., Tesar, V., Eitner, F., Rauen, T., Floege, J., Kovacs, T., Nagy, J., Mucha, K., Pączek, L., Zaniew, M., Mizerska-Wasiak, M., Roszkowska-Blaim, M., Pawlaczyk, K., Gale, D., Barratt, J., Thibaudin, L., Berthoux, F., Canaud, G., Boland, A., Metzger, M., Panzer, U., Suzuki, H., Goto, S., Narita, I., Caliskan, Y., Xie, J., Hou, P., Chen, N., Zhang, H., Wyatt, R.J., Novak, J., Julian, B.A., Feehally, J., Stengel, B., Cusi, D., Lifton, R.P., and Gharavi, A.G. (2014). Discovery of new risk loci for IgA nephropathy implicates genes involved in immunity against intestinal pathogens. Nat Genet 46, 1187–1196.
Klein, R.S., and Hunter, C.A. (2017). Protective and pathological immunity during central nervous system infections. Immunity 46, 891–909.
Klonowski, K.D., Williams, K.J., Marzo, A.L., Blair, D.A., Lingenheld, E.G., and Lefrançois, L. (2004). Dynamics of blood-borne CD8 memory T cell migration in vivo. Immunity 20, 551–562.
Kolodin, D., van Panhuys, N., Li, C., Magnuson, A.M., Cipolletta, D., Miller, C.M., Wagers, A., Germain, R.N., Benoist, C., and Mathis, D. (2015). Antigen-and cytokine-driven accumulation of regulatory T cells in visceral adipose tissue of lean mice. Cell Metab 21, 543–557.
Kopf, M., Schneider, C., and Nobs, S.P. (2015). The development and function of lung-resident macrophages and dendritic cells. Nat Immunol 16, 36–44.
Korn, T., and Kallies, A. (2017). T cell responses in the central nervous system. Nat Rev Immunol 17, 179–194.
Kuklin, N.A., Rott, L., Darling, J., Campbell, J.J., Franco, M., Feng, N., Müller, W., Wagner, N., Altman, J., Butcher, E.C., and Greenberg, H.B. (2000). α4β7 independent pathway for CD8+ T cell-mediated intestinal immunity to rotavirus. J Clin Invest 106, 1541–1552.
Kuol, N., Stojanovska, L., Nurgali, K., and Apostolopoulos, V. (2017). The mechanisms tumor cells utilize to evade the host’s immune system. Maturitas 105, 8–15.
Kurts, C., Panzer, U., Anders, H.J., and Rees, A.J. (2013). The immune system and kidney disease: basic concepts and clinical implications. Nat Rev Immunol 13, 738–753.
Lambrecht, B.N., and Hammad, H. (2012). The airway epithelium in asthma. Nat Med 18, 684–692.
Liddelow, S.A., and Barres, B.A. (2017). Reactive astrocytes: production, function, and therapeutic potential. Immunity 46, 957–967.
Liddiard, K., and Taylor, P.R. (2015). Understanding local macrophage phenotypes in disease: Shape-shifting macrophages. Nat Med 21, 119–120.
Liu, Y., Teige, I., Birnir, B., and Issazadeh-Navikas, S. (2006). Neuronmediated generation of regulatory T cells from encephalitogenic T cells suppresses EAE. Nat Med 12, 518–525.
Lloyd, C.M., and Marsland, B.J. (2017). Lung homeostasis: influence of age, microbes, and the immune system. Immunity 46, 549–561.
Lu, Y., Lin, H., Zhai, K., Wang, X., Zhou, Q., and Shi, H. (2016). Interleukin-17 inhibits development of malignant pleural effusion via interleukin-9-dependent mechanism. Sci China Life Sci 59, 1297–1304.
Mackay, C.R., and von Andrian, U.H. (2001). Immunology. Memory T cells—local heroes in the struggle for immunity. Science 291, 2323–2324.
Mackay, L.K., Braun, A., Macleod, B.L., Collins, N., Tebartz, C., Bedoui, S., Carbone, F.R., and Gebhardt, T. (2015). Cutting edge: CD69 interference with sphingosine-1-phosphate receptor function regulates peripheral T cell retention. J Immunol 194, 2059–2063.
Marks, B.R., and Craft, J. (2009). Barrier immunity and IL-17. Seminars Immunol 21, 164–171.
Marshall, E.A., Ng, K.W., Kung, S.H.Y., Conway, E.M., Martinez, V.D., Halvorsen, E.C., Rowbotham, D.A., Vucic, E.A., Plumb, A.W., Becker-Santos, D.D., Enfield, K.S.S., Kennett, J.Y., Bennewith, K.L., Lockwood, W.W., Lam, S., English, J.C., Abraham, N., and Lam, W.L. (2016). Emerging roles of T helper 17 and regulatory T cells in lung cancer progression and metastasis. Mol Cancer 15, 67.
McKinley, L., Alcorn, J.F., Peterson, A., DuPont, R.B., Kapadia, S., Logar, A., Henry, A., Irvin, C.G., Piganelli, J.D., Ray, A., and Kolls, J.K. (2008). TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J Immunol 181, 4089–4097.
Meng, X., Yang, J., Dong, M., Zhang, K., Tu, E., Gao, Q., Chen, W., Zhang, C., and Zhang, Y. (2016). Regulatory T cells in cardiovascular diseases. Nat Rev Cardiol 13, 167–179.
Mochizuki, M., Sugita, S., and Kamoi, K. (2013). Immunological homeostasis of the eye. Prog Retinal Eye Res 33, 10–27.
Morita, H., Arae, K., Unno, H., Miyauchi, K., Toyama, S., Nambu, A., Oboki, K., Ohno, T., Motomura, K., Matsuda, A., Yamaguchi, S., Narushima, S., Kajiwara, N., Iikura, M., Suto, H., McKenzie, A.N.J., Takahashi, T., Karasuyama, H., Okumura, K., Azuma, M., Moro, K., Akdis, C.A., Galli, S.J., Koyasu, S., Kubo, M., Sudo, K., Saito, H., Matsumoto, K., and Nakae, S. (2015). An interleukin-33-mast cell-interleukin-2 axis suppresses papain-induced allergic inflammation by promoting regulatory T cell numbers. Immunity 43, 175–186.
Mortensen, E.S., and Rekvig, O.P. (2009). Nephritogenic potential of anti-DNA antibodies against necrotic nucleosomes. J Am Soc Nephrol 20, 696–704.
Mowat, A.M., and Agace, W.W. (2014). Regional specialization within the intestinal immune system. Nat Rev Immunol 14, 667–685.
Mueller, S.N., Gebhardt, T., Carbone, F.R., and Heath, W.R. (2013). Memory T cell subsets, migration patterns, and tissue residence. Annu Rev Immunol 31, 137–161.
Mueller, S.N., and Mackay, L.K. (2016). Tissue-resident memory T cells: local specialists in immune defence. Nat Rev Immunol 16, 79–89.
Murray, P.J., Allen, J.E., Biswas, S.K., Fisher, E.A., Gilroy, D.W., Goerdt, S., Gordon, S., Hamilton, J.A., Ivashkiv, L.B., Lawrence, T., Locati, M., Mantovani, A., Martinez, F.O., Mege, J.L., Mosser, D.M., Natoli, G., Saeij, J.P., Schultze, J.L., Shirey, K.A., Sica, A., Suttles, J., Udalova, I., van Ginderachter, J.A., Vogel, S.N., and Wynn, T.A. (2014). Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41, 14–20.
Nakamura, A., Ebina-Shibuya, R., Itoh-Nakadai, A., Muto, A., Shima, H., Saigusa, D., Aoki, J., Ebina, M., Nukiwa, T., and Igarashi, K. (2013). Transcription repressor Bach2 is required for pulmonary surfactant homeostasis and alveolar macrophage function. J Exp Med 210, 2191–2204.
Nakamura, Y.K., Metea, C., Karstens, L., Asquith, M., Gruner, H., Moscibrocki, C., Lee, I., Brislawn, C.J., Jansson, J.K., Rosenbaum, J.T., and Lin, P. (2016). Gut microbial alterations associated with protection from autoimmune uveitis. Invest Ophthalmol Vis Sci 57, 3747–3758.
Panduro, M., Benoist, C., and Mathis, D. (2016). Tissue Tregs. Annu Rev Immunol 34, 609–633.
Peng, H., and Tian, Z. (2016). Tissue-resident natural killer cells in the livers. Sci China Life Sci 59, 1218–1223.
Pierson, E., Simmons, S.B., Castelli, L., and Goverman, J.M. (2012). Mechanisms regulating regional localization of inflammation during CNS autoimmunity. Immunol Rev 248, 205–215.
Podolska, M.J., Biermann, M.H., Maueroder, C., Hahn, J., and Herrmann, M. (2015). Inflammatory etiopathogenesis of systemic lupus erythematosus: an update. J Inflamm Res 8, 161–171.
Pridgeon, C., Lennon, G.P., Pazmany, L., Thompson, R.N., Christmas, S.E., and Moots, R.J. (2003). Natural killer cells in the synovial fluid of rheumatoid arthritis patients exhibit a CD56bright, CD94bright, CD158negative phenotype. Rheumatology 42, 870–878.
Qiu, Y., Shan, B., Yang, L., and Liu, Y. (2016). Adipose tissue macrophage in immune regulation of metabolism. Sci China Life Sci 59, 1232–1240.
Robinette, M.L., Fuchs, A., Cortez, V.S., Lee, J.S., Wang, Y., Durum, S.K., Gilfillan, S., Colonna, M., Shaw, L., Yu, B., Goldrath, A., Mostafavi, S., Regev, A., Kim, E.Y., Dwyer, D.F., Brenner, M.B., Austen, K.F., Rhoads, A., Moodley, D., Yoshida, H., Mathis, D., Benoist, C., Nabekura, T., Lam, V., Lanier, L.L., Brown, B., Merad, M., Cremasco, V., Turley, S., Monach, P., Dustin, M.L., Li, Y., Shinton, S.A., Hardy, R.R., Shay, T., Qi, Y., Sylvia, K., Kang, J., Fairfax, K., Randolph, G.J., Robinette, M.L., Fuchs, A., and Colonna, M. (2015). Transcriptional programs define molecular characteristics of innate lymphoid cell classes and subsets. Nat Immunol 16, 306–317.
Rosenblum, M.D., Gratz, I.K., Paw, J.S., Lee, K., Marshak-Rothstein, A., and Abbas, A.K. (2011). Response to self antigen imprints regulatory memory in tissues. Nature 480, 538–542.
Salter, M.W., and Stevens, B. (2017). Microglia emerge as central players in brain disease. Nat Med 23, 1018–1027.
Samstein, R.M., Josefowicz, S.Z., Arvey, A., Treuting, P.M., and Rudensky, A.Y. (2012). Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict. Cell 150, 29–38.
Schiering, C., Krausgruber, T., Chomka, A., Fröhlich, A., Adelmann, K., Wohlfert, E.A., Pott, J., Griseri, T., Bollrath, J., Hegazy, A.N., Harrison, O.J., Owens, B.M.J., Löhning, M., Belkaid, Y., Fallon, P.G., and Powrie, F. (2014). The alarmin IL-33 promotes regulatory T-cell function in the intestine. Nature 513, 564–568.
Sefik, E., Geva-Zatorsky, N., Oh, S., Konnikova, L., Zemmour, D., McGuire, A.M., Burzyn, D., Ortiz-Lopez, A., Lobera, M., Yang, J., Ghosh, S., Earl, A., Snapper, S.B., Jupp, R., Kasper, D., Mathis, D., and Benoist, C. (2015). MUCOSAL IMMUNOLOGY. Individual intestinal symbionts induce a distinct population of RORgamma(+) regulatory T cells. Science 349, 993–997.
Shi, F.D., Ljunggren, H.G., La Cava, A., and Van Kaer, L. (2011). Organspecific features of natural killer cells. Nat Rev Immunol 11, 658–671.
Skon, C.N., Lee, J.Y., Anderson, K.G., Masopust, D., Hogquist, K.A., and Jameson, S.C. (2013). Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells. Nat Immunol 14, 1285–1293.
Soroosh, P., Doherty, T.A., Duan, W., Mehta, A.K., Choi, H., Adams, Y.F., Mikulski, Z., Khorram, N., Rosenthal, P., Broide, D.H., and Croft, M. (2013). Lung-resident tissue macrophages generate Foxp3+ regulatory T cells and promote airway tolerance. J Exp Med 210, 775–788.
Stein-Streilein, J., and Taylor, A.W. (2007). An eye’s view of T regulatory cells. J Leukocyte Biol 81, 593–598.
Streilein, J.W. (1999). Immunoregulatory mechanisms of the eye. Prog Retinal Eye Res 18, 357–370.
Suárez-Fueyo, A., Bradley, S.J., Klatzmann, D., and Tsokos, G.C. (2017). T cells and autoimmune kidney disease. Nat Rev Nephrol 13, 329–343.
Tait Wojno, E.D., and Artis, D. (2016). Emerging concepts and future challenges in innate lymphoid cell biology. J Exp Med 213, 2229–2248.
Tang, T.T., Yuan, J., Zhu, Z.F., Zhang, W.C., Xiao, H., Xia, N., Yan, X.X., Nie, S.F., Liu, J., Zhou, S.F., Li, J.J., Yao, R., Liao, M.Y., Tu, X., Liao, Y.H., and Cheng, X. (2012). Regulatory T cells ameliorate cardiac remodeling after myocardial infarction. Basic Res Cardiol 107, 232.
Tanoue, T., Atarashi, K., and Honda, K. (2016). Development and maintenance of intestinal regulatory T cells. Nat Rev Immunol 16, 295–309.
Tate, M.D., Pickett, D.L., van Rooijen, N., Brooks, A.G., and Reading, P.C. (2010). Critical role of airway macrophages in modulating disease severity during influenza virus infection of mice. J Virol 84, 7569–7580.
Tian, Z., Cao, X., Chen, Y., and Lyu, Q. (2016). Regional immunity in tissue homeostasis and diseases. Sci China Life Sci 59, 1205–1209.
Turnquist, H.R., Zhao, Z., Rosborough, B.R., Liu, Q., Castellaneta, A., Isse, K., Wang, Z., Lang, M., Beer Stolz, D., Zheng, X.X., Demetris, A.J., Liew, F.Y., Wood, K.J., and Thomson, A.W. (2011). IL-33 expands suppressive CD11b+ Gr-1int and regulatory T cells, including ST2L+ Foxp3+ cells, and mediates regulatory T cell-dependent promotion of cardiac allograft survival. J Immunol 187, 4598–4610.
Varol, C., Mildner, A., and Jung, S. (2015). Macrophages: development and tissue specialization. Annu Rev Immunol 33, 643–675.
Villalta, S.A., Rosenthal, W., Martinez, L., Kaur, A., Sparwasser, T., Tidball, J.G., Margeta, M., Spencer, M.J., and Bluestone, J.A. (2014). Regulatory T cells suppress muscle inflammation and injury in muscular dystrophy. Sci Transl Med 6, 258ra142.
Waisman, A., Liblau, R.S., and Becher, B. (2015). Innate and adaptive immune responses in the CNS. Lancet Neurol 14, 945–955.
Weirather, J., Hofmann, U.D.W., Beyersdorf, N., Ramos, G.C., Vogel, B., Frey, A., Ertl, G., Kerkau, T., and Frantz, S. (2014). Foxp3+ CD4+ T cells improve healing after myocardial infarction by modulating monocyte/macrophage differentiation. Circulation Res 115, 55–67.
Westfall, S., Lomis, N., Kahouli, I., Dia, S.Y., Singh, S.P., and Prakash, S. (2017). Microbiome, probiotics and neurodegenerative diseases: deciphering the gut brain axis. Cell Mol Life Sci, doi: 10.1007/s00018-017-2550-9.
Xie, D., Zhu, S., and Bai, L. (2016). Lactic acid in tumor microenvironments causes dysfunction of NKT cells by interfering with mTOR signaling. Sci China Life Sci 59, 1290–1296.
Yamasaki, R., Lu, H., Butovsky, O., Ohno, N., Rietsch, A.M., Cialic, R., Wu, P.M., Doykan, C.E., Lin, J., Cotleur, A.C., Kidd, G., Zorlu, M.M., Sun, N., Hu, W., Liu, L.P., Lee, J.C., Taylor, S.E., Uehlein, L., Dixon, D., Gu, J., Floruta, C.M., Zhu, M., Charo, I.F., Weiner, H.L., and Ransohoff, R.M. (2014). Differential roles of microglia and monocytes in the inflamed central nervous system. J Exp Med 211, 1533–1549.
Yan, X., Shichita, T., Katsumata, Y., Matsuhashi, T., Ito, H., Ito, K., Anzai, A., Endo, J., Tamura, Y., Kimura, K., Fujita, J., Shinmura, K., Shen, W., Yoshimura, A., Fukuda, K., and Sano, M. (2012). Deleterious effect of the IL-23/IL-17A axis and gammadeltaT cells on left ventricular remodeling after myocardial infarction. J Am Heart Assoc 1, e004408.
Yan, Y., Li, Y., Fu, Y., Yang, L., Su, L., Shi, K., Li, M., Liu, Q., Borazanci, A., Liu, Y., He, Y., Bennett, J.L., Vollmer, T.L., and Shi, F.D. (2016). Autoantibody to MOG suggests two distinct clinical subtypes of NMOSD. Sci China Life Sci 59, 1270–1281.
Yung, S., Cheung, K.F., Zhang, Q., and Chan, T.M. (2010). Anti-dsDNA antibodies bind to mesangial annexin II in lupus nephritis. J Am Soc Nephrol 21, 1912–1927.
Zárate-Bladés, C.R., Horai, R., Mattapallil, M.J., Ajami, N.J., Wong, M., Petrosino, J.F., Itoh, K., Chan, C.C., and Caspi, R.R. (2017). Gut microbiota as a source of a surrogate antigen that triggers autoimmunity in an immune privileged site. Gut Microbes 8, 59–66.
Zhang, N., and Bevan, M.J. (2013). Transforming growth factor-β signaling controls the formation and maintenance of gut-resident memory T cells by regulating migration and retention. Immunity 39, 687–696.
Zhang, X., Jiang, Z., Gu, Y., Liu, Y., Cao, X., and Han, Y. (2016). Inflammation-induced CD69+ Kupffer cell feedback inhibits T cell proliferation via membrane-bound TGF-β1. Sci China Life Sci 59, 1259–1269.
Zhang, Y., and Liang, C. (2016). Innate recognition of microbial-derived signals in immunity and inflammation. Sci China Life Sci 59, 1210–1217.
Zhao, L., Huang, L., and Zhang, X. (2016). Osteoimmunology: memorandum for rheumatologists. Sci China Life Sci 59, 1241–1258.
Zhou, G., and Levitsky, H.I. (2007). Natural regulatory T cells and de novo-induced regulatory T cells contribute independently to tumor-specific tolerance. J Immunol 178, 2155–2162.
Zouggari, Y., Ait-Oufella, H., Bonnin, P., Simon, T., Sage, A.P., Guérin, C., Vilar, J., Caligiuri, G., Tsiantoulas, D., Laurans, L., Dumeau, E., Kotti, S., Bruneval, P., Charo, I.F., Binder, C.J., Danchin, N., Tedgui, A., Tedder, T.F., Silvestre, J.S., and Mallat, Z. (2013). B lymphocytes trigger monocyte mobilization and impair heart function after acute myocardial infarction. Nat Med 19, 1273–1280.
Acknowledgements
This work was supported by grants from the National Natural Science Foundation of China (81788104, 81630044, 81601432, 81550023, 81771763), the National Science Fund for Distinguished Young Scholars of China (81325019), National Key Research and Development Program: “Precise Medical Research” (2016YFC0903900), and Chinese Academy of Medical Science Innovation Fund for Medical Sciences (CIFM2016-12M-1-003, 2017-12M-1-008, 2016-12M-1-008), and 2016 Peking Union Medical College Hospital Fund for Junior Faculty (pumch-2016-2.1).
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Zhou, C., Sun, L., Zhao, L. et al. Advancement in regional immunity and its clinical implication. Sci. China Life Sci. 60, 1178–1190 (2017). https://doi.org/10.1007/s11427-017-9224-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-017-9224-6