CCR10 and its ligands in regulation of epithelial immunity and diseases

Abstract

Epithelial tissues covering the external and internal surface of a body are constantly under physical, chemical or biological assaults. To protect the epithelial tissues and maintain their homeostasis, multiple layers of immune defense mechanisms are required. Besides the epithelial tissue-resident immune cells that provide the first line of defense, circulating immune cells are also recruited into the local tissues in response to challenges. Chemokines and chemokine receptors regulate tissue-specific migration, maintenance and functions of immune cells. Among them, chemokine receptor CCR10 and its ligands chemokines CCL27 and CCL28 are uniquely involved in the epithelial immunity. CCL27 is expressed predominantly in the skin by keratinocytes while CCL28 is expressed by epithelial cells of various mucosal tissues. CCR10 is expressed by various subsets of innate-like T cells that are programmed to localize to the skin during their developmental processes in the thymus. Circulating T cells might be imprinted by skin-associated antigen- presenting cells to express CCR10 for their recruitment to the skin during the local immune response. On the other hand, IgA antibody-producing B cells generated in mucosa-associated lymphoid tissues express CCR10 for their migration and maintenance at mucosal sites. Increasing evidence also found that CCR10/ligands are involved in regulation of other immune cells in epithelial immunity and are frequently exploited by epithelium-localizing or-originated cancer cells for their survival, proliferation and evasion from immune surveillance. Herein, we review current knowledge on roles of CCR10/ligands in regulation of epithelial immunity and diseases and speculate on related important questions worth further investigation.

Key words： CCR10; epithelial immunity; epithelial diseases

References

[1] Bowman, E.P., Kuklin, N.A., Youngman, K.R., Lazarus, N.H., Kunkel, E.J., Pan, J., Greenberg, H.B., and Butcher, E.C. (2002). The intestinal chemokine thymus-expressed chemokine (CCL25) attracts IgA antibody-secreting cells. J Exp Med 195, 269-275 .10.1084/jem.20010670
[2] Boyden, L.M., Lewis, J.M., Barbee, S.D., Bas, A., Girardi, M., Hayday, A.C., Tigelaar, R.E., and Lifton, R.P. (2008). Skint1, the prototype of a newly identified immunoglobulin superfamily gene cluster, positively selects epidermal gammadelta T cells. Nat Genet 40, 656-662 10.1038/ng.108
[3] Cerutti, A., and Rescigno, M. (2008). The biology of intestinal immunoglobulin A responses. Immunity 28, 740-750 .10.1016/j.immuni.2008.05.001
[4] Cha, H.R., Ko, H.J., Kim, E.D., Chang, S.Y., Seo, S.U., Cuburu, N., Ryu, S., Kim, S., and Kweon, M.N. (2011). Mucosa-associated epithelial chemokine/CCL28 expression in the uterus attracts CCR10+ IgA plasma cells following mucosal vaccination via estrogen control. J Immunol 187, 3044-3052 .10.4049/jimmunol.1100402
[5] Charo, I.F., and Ransohoff, R.M. (2006). The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 354, 610-621 .10.1056/NEJMra052723
[6] Chen, L., Lin, S.X., Agha-Majzoub, R., Overbergh, L., Mathieu, C., and Chan, L.S. (2006). CCL27 is a critical factor for the development of atopic dermatitis in the keratin-14 IL-4 transgenic mouse model. Int Immunol 18, 1233-1242 .10.1093/intimm/dxl054
[7] Corthésy, B. (2007). Roundtrip ticket for secretory IgA: role in mucosal homeostasis? J Immunol 178, 27-32 .
[8] De Creus, A., Van Beneden, K., Stevenaert, F., Debacker, V., Plum, J., and Leclercq, G. (2002). Developmental and functional defects of thymic and epidermal V gamma 3 cells in IL-15-deficient and IFN regulatory factor-1-deficient mice. J Immunol 168, 6486-6493 .
[9] Dent, A.L., Matis, L.A., Hooshmand, F., Widacki, S.M., Bluestone, J.A., and Hedrick, S.M. (1990). Self-reactive γ δ T cells are eliminated in the thymus. Nature 343, 714-719 .10.1038/343714a0
[10] Duhen, T., Geiger, R., Jarrossay, D., Lanzavecchia, A., and Sallusto, F. (2009). Production of interleukin 22 but not interleukin 17 by a subset of human skin-homing memory T cells. Nat Immunol 10, 857-863 .10.1038/ni.1767
[11] Eksteen, B., Miles, A., Curbishley, S.M., Tselepis, C., Grant, A.J., Walker, L.S., and Adams, D.H. (2006). Epithelial inflammation is associated with CCL28 production and the recruitment of regulatory T cells expressing CCR10. J Immunol 177, 593-603 .
[12] English, K., Brady, C., Corcoran, P., Cassidy, J.P., and Mahon, B.P. (2006). Inflammation of the respiratory tract is associated with CCL28 and CCR10 expression in a murine model of allergic asthma. Immunol Lett 103, 92-100 .10.1016/j.imlet.2005.09.011
[13] Eyerich, S., Eyerich, K., Pennino, D., Carbone, T., Nasorri, F., Pallotta, S., Cianfarani, F., Odorisio, T., Traidl-Hoffmann, C., Behrendt, H., . (2009). Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. J Clin Invest 119, 3573-3585 .
[14] Facciabene, A., Peng, X., Hagemann, I.S., Balint, K., Barchetti, A., Wang, L.P., Gimotty, P.A., Gilks, C.B., Lal, P., Zhang, L., . (2011). Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T(reg) cells. Nature 475, 226-230 .10.1038/nature10169
[15] Feng, N., Jaimes, M.C., Lazarus, N.H., Monak, D., Zhang, C., Butcher, E.C., and Greenberg, H.B. (2006). Redundant role of chemokines CCL25/TECK and CCL28/MEC in IgA+ plasmablast recruitment to the intestinal lamina propria after rotavirus infection. J Immunol 176, 5749-5759 .
[16] Fujita, Y., Abe, R., Sasaki, M., Honda, A., Furuichi, M., Asano, Y., Norisugi, O., Shimizu, T., and Shimizu, H. (2006). Presence of circulating CCR10+ T cells and elevated serum CTACK/CCL27 in the early stage of mycosis fungoides. Clin Cancer Res 12, 2670-2675 .10.1158/1078-0432.CCR-05-1513
[17] Girardi, M., Lewis, J., Glusac, E., Filler, R.B., Geng, L., Hayday, A.C., and Tigelaar, R.E. (2002). Resident skin-specific gammadelta T cells provide local, nonredundant regulation of cutaneous inflammation. J Exp Med 195, 855-867 .10.1084/jem.20012000
[18] Girardi, M., Oppenheim, D.E., Steele, C.R., Lewis, J.M., Glusac, E., Filler, R., Hobby, P., Sutton, B., Tigelaar, R.E., and Hayday, A.C. (2001). Regulation of cutaneous malignancy by gammadelta T cells. Science 294, 605-609 .10.1126/science.1063916
[19] Grayson, M.H., Cheung, D., Rohlfing, M.M., Kitchens, R., Spiegel, D.E., Tucker, J., Battaile, J.T., Alevy, Y., Yan, L., Agapov, E., . (2007). Induction of high-affinity IgE receptor on lung dendritic cells during viral infection leads to mucous cell metaplasia. J Exp Med 204, 2759-2769 .10.1084/jem.20070360
[20] Hayakawa, I., Hasegawa, M., Matsushita, T., Yanaba, K., Kodera, M., Komura, K., Takehara, K., and Sato, S. (2005). Increased cutaneous T-cell-attracting chemokine levels in sera from patients with systemic sclerosis. Rheumatology (Oxford) 44, 873-878 .10.1093/rheumatology/keh625
[21] Hayday, A.C. (2000). [gamma][delta] cells: a right time and a right place for a conserved third way of protection. Annu Rev Immunol 18, 975-1026 .10.1146/annurev.immunol.18.1.975
[22] Hieshima, K., Kawasaki, Y., Hanamoto, H., Nakayama, T., Nagakubo, D., Kanamaru, A., and Yoshie, O. (2004). CC chemokine ligands 25 and 28 play essential roles in intestinal extravasation of IgA antibody-secreting cells. J Immunol 173, 3668-3675 .
[23] Hieshima, K., Ohtani, H., Shibano, M., Izawa, D., Nakayama, T., Kawasaki, Y., Shiba, F., Shiota, M., Katou, F., Saito, T., . (2003). CCL28 has dual roles in mucosal immunity as a chemokine with broad-spectrum antimicrobial activity. J Immunol 170, 1452-1461 .
[24] Hijnen, D., De Bruin-Weller, M., Oosting, B., Lebre, C., De Jong, E., Bruijnzeel-Koomen, C., and Knol, E. (2004). Serum thymus and activation-regulated chemokine (TARC) and cutaneous T cell- attracting chemokine (CTACK) levels in allergic diseases: TARC and CTACK are disease-specific markers for atopic dermatitis. J Allergy Clin Immunol 113, 334-340 .10.1016/j.jaci.2003.12.007
[25] Homey, B., Alenius, H., Müller, A., Soto, H., Bowman, E.P., Yuan, W., McEvoy, L., Lauerma, A.I., Assmann, T., Bünemann, E., . (2002). CCL27-CCR10 interactions regulate T cell-mediated skin inflammation. Nat Med 8, 157-165 .10.1038/nm0202-157
[26] Homey, B., Wang, W., Soto, H., Buchanan, M.E., Wiesenborn, A., Catron, D., Müller, A., McClanahan, T.K., Dieu-Nosjean, M.C., Orozco, R., . (2000). Cutting edge: the orphan chemokine receptor G protein-coupled receptor-2 (GPR-2, CCR10) binds the skin-associated chemokine CCL27 (CTACK/ALP/ILC). J Immunol 164, 3465-3470 .
[27] Hon, K.L., Leung, T.F., Ma, K.C., Li, A.M., Wong, Y., and Fok, T.F. (2004). Serum levels of cutaneous T-cell attracting chemokine (CTACK) as a laboratory marker of the severity of atopic dermatitis in children. Clin Exp Dermatol 29, 293-296 .10.1111/j.1365-2230.2004.01501.x
[28] Hu, S., Yang, K., Yang, J., Li, M., and Xiong, N. (2011). Critical roles of chemokine receptor CCR10 in regulating memory IgA responses in intestines. Proc Natl Acad Sci U S A 108, E1035-E1044 .10.1073/pnas.1100156108
[29] Ishida, I., Verbeek, S., Bonneville, M., Itohara, S., Berns, A., and Tonegawa, S. (1990). T-cell receptor γ δ and γ transgenic mice suggest a role of a γ gene silencer in the generation of α β T cells. Proc Natl Acad Sci U S A 87, 3067-3071 .10.1073/pnas.87.8.3067
[30] Ito, K., Van Kaer, L., Bonneville, M., Hsu, S., Murphy, D.B., and Tonegawa, S. (1990). Recognition of the product of a novel MHC TL region gene (27b) by a mouse gamma delta T cell receptor. Cell 62, 549-561 .10.1016/0092-8674(90)90019-B
[31] Jameson, J., Ugarte, K., Chen, N., Yachi, P., Fuchs, E., Boismenu, R., and Havran, W.L. (2002). A role for skin gammadelta T cells in wound repair. Science 296, 747-749 .10.1126/science.1069639
[32] Jarmin, D.I., Rits, M., Bota, D., Gerard, N.P., Graham, G.J., Clark-Lewis, I., and Gerard, C. (2000). Cutting edge: identification of the orphan receptor G-protein-coupled receptor 2 as CCR10, a specific receptor for the chemokine ESkine. J Immunol 164, 3460-3464 .
[33] Jensen, K.D., Shin, S., and Chien, Y.H. (2009). Cutting edge: Gammadelta intraepithelial lymphocytes of the small intestine are not biased toward thymic antigens. J Immunol 182, 7348-7351 .10.4049/jimmunol.0900465
[34] Jiang, X., Campbell, J.J., and Kupper, T.S. (2010). Embryonic trafficking of gammadelta T cells to skin is dependent on E/P selectin ligands and CCR4. Proc Natl Acad Sci U S A 107, 7443-7448 .10.1073/pnas.0912943107
[35] Jin, Y., Xia, M., Saylor, C.M., Narayan, K., Kang, J., Wiest, D.L., Wang, Y., and Xiong, N. (2010a). Cutting edge: Intrinsic programming of thymic γ δ T cells for specific peripheral tissue localization. J Immunol 185, 7156-7160 .10.4049/jimmunol.1002781
[36] Jin, Y., Xia, M., Sun, A., Saylor, C.M., and Xiong, N. (2010b). CCR10 is important for the development of skin-specific gammadeltaT cells by regulating their migration and location. J Immunol 185, 5723-5731 .10.4049/jimmunol.1001612
[37] John, A.E., Thomas, M.S., Berlin, A.A., and Lukacs, N.W. (2005). Temporal production of CCL28 corresponds to eosinophil accumulation and airway hyperreactivity in allergic airway inflammation. Am J Pathol 166, 345-353 .10.1016/S0002-9440(10)62258-4
[38] Kagami, S., Kakinuma, T., Saeki, H., Tsunemi, Y., Fujita, H., Sasaki, K., Nakamura, K., Takekoshi, T., Kishimoto, M., Mitsui, H., . (2005). Increased serum CCL28 levels in patients with atopic dermatitis, psoriasis vulgaris and bullous pemphigoid. J Invest Dermatol 124, 1088-1090 .10.1111/j.0022-202X.2005.23700.x
[39] Kagami, S., Saeki, H., Komine, M., Kakinuma, T., Nakamura, K., Tsunemi, Y., Sasaki, K., Asahina, A., and Tamaki, K. (2006). CCL28 production in HaCaT cells was mediated by different signal pathways from CCL27. Exp Dermatol 15, 95-100 .10.1111/j.1600-0625.2005.00390.x
[40] Kagami, S., Saeki, H., Tsunemi, Y., Nakamura, K., Kuwano, Y., Komine, M., Nakayama, T., Yoshie, O., and Tamaki, K. (2008). CCL27-transgenic mice show enhanced contact hypersensitivity to Th2, but not Th1 stimuli. Eur J Immunol 38, 647-657 .10.1002/eji.200737685
[41] Kai, H., Kadono, T., Kakinuma, T., Tomita, M., Ohmatsu, H., Asano, Y., Tada, Y., Sugaya, M., and Sato, S. (2011). CCR10 and CCL27 are overexpressed in cutaneous squamous cell carcinoma. Pathol Res Pract 207, 43-48 .10.1016/j.prp.2010.10.007
[42] Kakinuma, T., Saeki, H., Tsunemi, Y., Fujita, H., Asano, N., Mitsui, H., Tada, Y., Wakugawa, M., Watanabe, T., Torii, H., . (2003). Increased serum cutaneous T cell-attracting chemokine (CCL27) levels in patients with atopic dermatitis and psoriasis vulgaris. J Allergy Clin Immunol 111, 592-597 .10.1067/mai.2003.114
[43] Kanda, N., Koike, S., and Watanabe, S. (2005). IL-17 suppresses TNF-alpha-induced CCL27 production through induction of COX-2 in human keratinocytes. J Allergy Clin Immunol 116, 1144-1150 .10.1016/j.jaci.2005.08.014
[44] Kawai, K., Suzuki, H., Tomiyama, K., Minagawa, M., Mak, T.W., and Ohashi, P.S. (1998). Requirement of the IL-2 receptor beta chain for the development of Vgamma3 dendritic epidermal T cells. J Invest Dermatol 110, 961-965 .10.1046/j.1523-1747.1998.00214.x
[45] Kraynyak, K.A., Kutzler, M.A., Cisper, N.J., Khan, A.S., Draghia-Akli, R., Sardesal, N.Y., Lewis, M.G., Yan, J., and Weiner, D.B. (2010). Systemic immunization with CCL27/CTACK modulates immune responses at mucosal sites in mice and macaques. Vaccine 28, 1942-1951 .10.1016/j.vaccine.2009.10.095
[46] Kuhnelt-Leddihn, L., Muller, H., Eisendle, K., Zelger, B., and Weinlich, G. (2012). Overexpression of the chemokine receptors CXCR4, CCR7, CCR9, and CCR10 in human primary cutaneous melanoma: a potential prognostic value for CCR7 and CCR10? Arch Dermatol Res 304,185-193 .10.1007/s00403-012-1222-8
[47] Kunkel, E.J., Kim, C.H., Lazarus, N.H., Vierra, M.A., Soler, D., Bowman, E.P., and Butcher, E.C. (2003). CCR10 expression is a common feature of circulating and mucosal epithelial tissue IgA Ab-secreting cells. J Clin Invest 111, 1001-1010 .
[48] Lazarus, N.H., Kunkel, E.J., Johnston, B., Wilson, E., Youngman, K.R., and Butcher, E.C. (2003). A common mucosal chemokine (mucosae-associated epithelial chemokine/CCL28) selectively attracts IgA plasmablasts. J Immunol 170, 3799-3805 .
[49] Liu, B., and Wilson, E. (2010). The antimicrobial activity of CCL28 is dependent on C-terminal positively-charged amino acids. Eur J Immunol 40, 186-196 .10.1002/eji.200939819
[50] Lorenz, R.G., Chaplin, D.D., McDonald, K.G., McDonough, J.S., and Newberry, R.D. (2003). Isolated lymphoid follicle formation is inducible and dependent upon lymphotoxin-sufficient B lymphocytes, lymphotoxin beta receptor, and TNF receptor I function. J Immunol 170, 5475-5482 .
[51] Maeda, S., Ohno, K., Nakamura, K., Uchida, K., Nakashima, K., Fukushima, K., Tsukamoto, A., Goto-Koshino, Y., Fujino, Y., and Tsujimoto, H. (2011). Quantification of chemokine and chemokine receptor gene expression in duodenal mucosa of dogs with inflammatory bowel disease. Vet Immunol Immunopathol 144, 290-298 .10.1016/j.vetimm.2011.08.020
[52] Marchese, A., Docherty, J.M., Nguyen, T., Heiber, M., Cheng, R., Heng, H.H., Tsui, L.C., Shi, X., George, S.R., and O’Dowd, B.F. (1994). Cloning of human genes encoding novel G protein- coupled receptors. Genomics 23, 609-618 .10.1006/geno.1994.1549
[53] McDonald, K.G., and Newberry, R.D. (2007). Whole-mount techniques to evaluate subepithelial cellular populations in the adult mouse intestine. Biotechniques 43, 50, 52, 54 passim.10.2144/000112514
[54] Mei, H.E., Yoshida, T., Sime, W., Hiepe, F., Thiele, K., Manz, R.A., Radbruch, A., and D ?rner, T. (2009). Blood-borne human plasma cells in steady state are derived from mucosal immune responses. Blood 113, 2461-2469 .10.1182/blood-2008-04-153544
[55] Mirshahpanah, P., Li, Y.Y., Burkhardt, N., Asadullah, K., and Zollner, T.M. (2008). CCR4 and CCR10 ligands play additive roles in mouse contact hypersensitivity. Exp Dermatol 17, 30-34 .
[56] Moed, H., Boorsma, D.M., Tensen, C.P., Flier, J., Jonker, M.J., Stoof, T.J., von Blomberg, B.M., Bruynzeel, D.P., Scheper, R.J., Rustemeyer, T., . (2004). Increased CCL27-CCR10 expression in allergic contact dermatitis: implications for local skin memory. J Pathol 204, 39-46 .10.1002/path.1619
[57] Mora, J.R., and von Andrian, U.H. (2008). Differentiation and homing of IgA-secreting cells. Mucosal Immunol 1, 96-109 .10.1038/mi.2007.14
[58] Morales, J., Homey, B., Vicari, A.P., Hudak, S., Oldham, E., Hedrick, J., Orozco, R., Copeland, N.G., Jenkins, N.A., McEvoy, L.M., . (1999). CTACK, a skin-associated chemokine that preferentially attracts skin-homing memory T cells. Proc Natl Acad Sci U S A 96, 14470-14475 .10.1073/pnas.96.25.14470
[59] Morteau, O., Gerard, C., Lu, B., Ghiran, S., Rits, M., Fujiwara, Y., Law, Y., Distelhorst, K., Nielsen, E.M., Hill, E.D., . (2008). An indispensable role for the chemokine receptor CCR10 in IgA antibody- secreting cell accumulation. J Immunol 181, 6309-6315 .
[60] Müller, A., Homey, B., Soto, H., Ge, N., Catron, D., Buchanan, M.E., McClanahan, T., Murphy, E., Yuan, W., Wagner, S.N., . (2001). Involvement of chemokine receptors in breast cancer metastasis. Nature 410, 50-56 .10.1038/35065016
[61] Murakami, T., Cardones, A.R., Finkelstein, S.E., Restifo, N.P., Klaunberg, B.A., Nestle, F.O., Castillo, S.S., Dennis, P.A., and Hwang, S.T. (2003). Immune evasion by murine melanoma mediated through CC chemokine receptor-10. J Exp Med 198, 1337-1347 .10.1084/jem.20030593
[62] Notohamiprodjo, M., Segerer, S., Huss, R., Hildebrandt, B., Soler, D., Djafarzadeh, R., Buck, W., Nelson, P.J., and von Luettichau, I. (2005). CCR10 is expressed in cutaneous T-cell lymphoma. Int J Cancer 115, 641-647 .10.1002/ijc.20922
[63] Ogawa, H., Iimura, M., Eckmann, L., and Kagnoff, M.F. (2004). Regulated production of the chemokine CCL28 in human colon epithelium. Am J Physiol Gastrointest Liver Physiol 287, G1062-G1069 .10.1152/ajpgi.00162.2004
[64] Pabst, O., Ohl, L., Wendland, M., Wurbel, M.A., Kremmer, E., Malissen, B., and F?rster, R. (2004). Chemokine receptor CCR9 contributes to the localization of plasma cells to the small intestine. J Exp Med 199, 411-416 .10.1084/jem.20030996
[65] Pan, J., Kunkel, E.J., Gosslar, U., Lazarus, N., Langdon, P., Broadwell, K., Vierra, M.A., Genovese, M.C., Butcher, E.C., and Soler, D. (2000). A novel chemokine ligand for CCR10 and CCR3 expressed by epithelial cells in mucosal tissues. J Immunol 165, 2943-2949 .
[66] Pivarcsi, A., Müller, A., Hippe, A., Rieker, J., van Lierop, A., Steinhoff, M., Seeliger, S., Kubitza, R., Pippirs, U., Meller, S., . (2007). Tumor immune escape by the loss of homeostatic chemokine expression. Proc Natl Acad Sci U S A 104, 19055-19060 .10.1073/pnas.0705673104
[67] Rainone, V., Dubois, G., Temchura, V., überla, K., Clivio, A., Nebuloni, M., Lauri, E., Trabattoni, D., Veas, F., and Clerici, M. (2011). CCL28 induces mucosal homing of HIV-1-specific IgA-secreting plasma cells in mice immunized with HIV-1 virus-like particles. PLoS One 6, e26979.10.1371/journal.pone.0026979
[68] Reiss, Y., Proudfoot, A.E., Power, C.A., Campbell, J.J., and Butcher, E.C. (2001). CC chemokine receptor (CCR)4 and the CCR10 ligand cutaneous T cell-attracting chemokine (CTACK) in lymphocyte trafficking to inflamed skin. J Exp Med 194, 1541-1547 .10.1084/jem.194.10.1541
[69] Riis, J.L., Johansen, C., Vestergaard, C., Bech, R., Kragballe, K., and Iversen, L. (2011a). Kinetics and differential expression of the skin-related chemokines CCL27 and CCL17 in psoriasis, atopic dermatitis and allergic contact dermatitis. Exp Dermatol 20, 789-794 .10.1111/j.1600-0625.2011.01323.x
[70] Riis, J.L., Johansen, C., Vestergaard, C., Otkjaer, K., Kragballe, K., and Iversen, L. (2011b). CCL27 expression is regulated by both p38 MAPK and IKKβ signalling pathways. Cytokine 56, 699-707 .10.1016/j.cyto.2011.09.007
[71] Scanlon, K.M., Hawksworth, R.J., Lane, S.J., and Mahon, B.P. (2011). IL-17A induces CCL28, supporting the chemotaxis of IgE-secreting B cells. Int Arch Allergy Immunol 156, 51-61 .10.1159/000322178
[72] Shirakawa, A.K., Nagakubo, D., Hieshima, K., Nakayama, T., Jin, Z., and Yoshie, O. (2008). 1,25-dihydroxyvitamin D3 induces CCR10 expression in terminally differentiating human B cells. J Immunol 180, 2786-2795 .
[73] Sigmundsdottir, H., Pan, J., Debes, G.F., Alt, C., Habtezion, A., Soler, D., and Butcher, E.C. (2007). DCs metabolize sunlight-induced vitamin D3 to ‘program’ T cell attraction to the epidermal chemokine CCL27. Nat Immunol 8, 285-293 .10.1038/ni1433
[74] Simonetti, O., Goteri, G., Lucarini, G., Filosa, A., Pieramici, T., Rubini, C., Biagini, G., and Offidani, A. (2006). Potential role of CCL27 and CCR10 expression in melanoma progression and immune escape. Eur J Cancer 42, 1181-1187 .10.1016/j.ejca.2006.01.043
[75] Sisirak, V., Vey, N., Vanbervliet, B., Duhen, T., Puisieux, I., Homey, B., Bowman, E.P., Trinchieri, G., Dubois, B., Kaiserlian, D., . (2011). CCR6/CCR10-mediated plasmacytoid dendritic cell recruitment to inflamed epithelia after instruction in lymphoid tissues. Blood 118, 5130-5140 .10.1182/blood-2010-07-295626
[76] Soler, D., Humphreys, T.L., Spinola, S.M., and Campbell, J.J. (2003). CCR4 versus CCR10 in human cutaneous TH lymphocyte trafficking. Blood 101, 1677-1682 .10.1182/blood-2002-07-2348
[77] Song, T.W., Sohn, M.H., Kim, E.S., Kim, K.W., and Kim, K.E. (2006). Increased serum thymus and activation-regulated chemokine and cutaneous T cell-attracting chemokine levels in children with atopic dermatitis. Clin Exp Allergy 36, 346-351 .10.1111/j.1365-2222.2006.02430.x
[78] Staton, T.L., Habtezion, A., Winslow, M.M., Sato, T., Love, P.E., and Butcher, E.C. (2006). CD8+ recent thymic emigrants home to and efficiently repopulate the small intestine epithelium. Nat Immuno l7, 482-488 .10.1038/ni1319
[79] Sundstr?m, P., Lundin, S.B., Nilsson, L.A., and Quiding-J?rbrink, M. (2008). Human IgA-secreting cells induced by intestinal, but not systemic, immunization respond to CCL25 (TECK) and CCL28 (MEC). Eur J Immunol 38, 3327-3338 .10.1002/eji.200838506
[80] Suzuki, K., and Fagarasan, S. (2009). Diverse regulatory pathways for IgA synthesis in the gut. Mucosal Immunol 2, 468-471 .10.1038/mi.2009.107
[81] Tilloy, F., Treiner, E., Park, S.H., Garcia, C., Lemonnier, F., de la Salle, H., Bendelac, A., Bonneville, M., and Lantz, O. (1999). An invariant T cell receptor alpha chain defines a novel TAP-independent major histocompatibility complex class Ib-restricted alpha/beta T cell subpopulation in mammals. J Exp Med 189, 1907-1921 .10.1084/jem.189.12.1907
[82] Treiner, E., Duban, L., Bahram, S., Radosavljevic, M., Wanner, V., Tilloy, F., Affaticati, P., Gilfillan, S., and Lantz, O. (2003). Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 422, 164-169 .10.1038/nature01433
[83] Trifari, S., Kaplan, C.D., Tran, E.H., Crellin, N.K., and Spits, H. (2009). Identification of a human helper T cell population that has abundant production of interleukin 22 and is distinct from T(H)-17, T(H)1 and T(H)2 cells. Nat Immunol 10, 864-871 .10.1038/ni.1770
[84] Tubo, N.J., McLachlan, J.B., and Campbell, J.J. (2011). Chemokine receptor requirements for epidermal T-cell trafficking. Am J Pathol 178, 2496-2503 .10.1016/j.ajpath.2011.02.031
[85] Turchinovich, G., and Hayday, A.C. (2011). Skint-1 identifies a common molecular mechanism for the development of interferon-γ-secreting versus interleukin-17-secreting γ δ T cells. Immunity 35, 59-68 .10.1016/j.immuni.2011.04.018
[86] Vestergaard, C., Deleuran, M., Gesser, B., and Gr?nh ?j Larsen, C. ( 2003). Expression of the T-helper 2-specific chemokine receptor CCR4 on CCR10-positive lymphocytes in atopic dermatitis skin but not in psoriasis skin. Br J Dermatol 149, 457-463 .10.1046/j.1365-2133.2003.05505.x
[87] Vestergaard, C., Johansen, C., Otkjaer, K., Deleuran, M., and Iversen, L. (2005). Tumor necrosis factor-alpha-induced CTACK/CCL27 (cutaneous T-cell-attracting chemokine) production in keratinocytes is controlled by nuclear factor kappaB. Cytokine 29, 49-55 .10.1016/j.cyto.2004.09.008
[88] Wang, W., Soto, H., Oldham, E.R., Buchanan, M.E., Homey, B., Catron, D., Jenkins, N., Copeland, N.G., Gilbert, D.J., Nguyen, N., . (2000). Identification of a novel chemokine (CCL28), which binds CCR10 (GPR2). J Biol Chem 275, 22313-22323 .10.1074/jbc.M001461200
[89] Watkins, H.R., Lapp, C.A., Hanes, P.J., Dickinson, D.P., Volkmann, K.R., Newman, C.L., and Konzelman, J.L. (2007). CCL28 effects on periodontal pathogens. J Periodontol 78, 2356-2363 .10.1902/jop.2007.060504
[90] Wilson, E., and Butcher, E.C. (2004). CCL28 controls immunoglobulin (Ig)A plasma cell accumulation in the lactating mammary gland and IgA antibody transfer to the neonate. J Exp Med 200, 805-809 .10.1084/jem.20041069
[91] Xiong, N., Kang, C., and Raulet, D.H. (2004). Positive selection of dendritic epidermal gammadelta T cell precursors in the fetal thymus determines expression of skin-homing receptors. Immunity 21, 121-131 .10.1016/j.immuni.2004.06.008
[92] Yamagata, T., Mathis, D., and Benoist, C. (2004). Self-reactivity in thymic double-positive cells commits cells to a CD8 alpha alpha lineage with characteristics of innate immune cells. Nat Immunol 5, 597-605 .10.1038/ni1070