New insights into the development of lymphoid tissues (original) (raw)
De Togni, P. et al. Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin. Science264, 703–707 (1994). ArticleCASPubMed Google Scholar
Grabner, R. et al. Lymphotoxin β receptor signaling promotes tertiary lymphoid organogenesis in the aorta adventitia of aged _ApoE_−/− mice. J. Exp. Med.206, 233–248 (2009). ArticleCASPubMedPubMed Central Google Scholar
Wengner, A. M. et al. CXCR5- and CCR7-dependent lymphoid neogenesis in a murine model of chronic antigen-induced arthritis. Arthritis Rheum.56, 3271–3283 (2007). ArticleCASPubMed Google Scholar
Shields, J. D., Kourtis, I. C., Tomei, A. A., Roberts, J. M. & Swartz, M. A. Induction of lymphoidlike stroma and immune escape by tumors that express the chemokine CCL21. Science328, 749–752 (2010). ArticleCASPubMed Google Scholar
van de Pavert, S. A. et al. Chemokine CXCL13 is essential for lymph node initiation and is induced by retinoic acid and neuronal stimulation. Nature Immunol.10, 1193–1199 (2009). This manuscript documents the crucial role of retinoic acid, potentially derived from nerve fibres, for the development of peripheral lymph nodes through its capacity to induce CXCL13. ArticleCAS Google Scholar
Veiga-Fernandes, H. et al. Tyrosine kinase receptor RET is a key regulator of Peyer's patch organogenesis. Nature446, 547–551 (2007). This paper shows that RET-expressing CD11c+ cells initiate the formation of Peyer's patches on encountering RET ligands. ArticleCASPubMed Google Scholar
Mebius, R. E. Organogenesis of lymphoid tissues. Nature Rev. Immunol.3, 292–303 (2003). ArticleCAS Google Scholar
Yoshida, H. et al. Different cytokines induce surface lymphotoxin-αβ on IL-7 receptor-α cells that differentially engender lymph nodes and Peyer's patches. Immunity17, 823–833 (2002). ArticleCASPubMed Google Scholar
Vondenhoff, M. F. et al. LTβR signaling induces cytokine expression and up-regulates lymphangiogenic factors in lymph node anlagen. J. Immunol.182, 5439–5445 (2009). Here the authors propose that tight clustering of LTi cells is needed to allow TRANCER triggering on LTi cells, which is needed for the generation of the first LTα1β2-expressing LTi cells. ArticleCASPubMed Google Scholar
Eberl, G. et al. An essential function for the nuclear receptor RORγt in the generation of fetal lymphoid tissue inducer cells. Nature Immunol.5, 64–73 (2004). ArticleCAS Google Scholar
Coles, M. C. et al. Role of T and NK cells and IL7/IL7R interactions during neonatal maturation of lymph nodes. Proc. Natl Acad. Sci. USA103, 13457–13462 (2006). ArticleCASPubMedPubMed Central Google Scholar
Benezech, C. et al. Ontogeny of stromal organizer cells during lymph node development. J. Immunol.184, 4521–4530 (2010). ArticleCASPubMed Google Scholar
Mebius, R. E. et al. The fetal liver counterpart of adult common lymphoid progenitors gives rise to all lymphoid lineages, CD45+CD4+CD3− cells, as well as macrophages. J. Immunol.166, 6593–6601 (2001). ArticleCASPubMed Google Scholar
Yoshida, H. et al. Expression of α4β7 integrin defines a distinct pathway of lymphoid progenitors committed to T cells, fetal intestinal lymphotoxin producer, NK, and dendritic cells. J. Immunol.167, 2511–2521 (2001). ArticleCASPubMed Google Scholar
Boos, M. D., Yokota, Y., Eberl, G. & Kee, B. L. Mature natural killer cell and lymphoid tissue-inducing cell development requires Id2-mediated suppression of E protein activity. J. Exp. Med.204, 1119–1130 (2007). By combining ID2 deficiency, which is required for the generation of LTi cells, with deficiency of E2A-encoded proteins, which are required for differentiation towards the B cell lineage, this article shows that ID2 is needed to suppress the activity of E proteins, asId2−/−E2a−/−mice have LTi cells and form lymph nodes and Peyer's patches. ArticleCASPubMedPubMed Central Google Scholar
Sun, Z. et al. Requirement for RORγ in thymocyte survival and lymphoid organ development. Science288, 2369–2373 (2000). ArticleCASPubMed Google Scholar
Cupedo, T. et al. Human fetal lymphoid tissue-inducer cells are interleukin 17-producing precursors to RORC+ CD127+ natural killer-like cells. Nature Immunol.10, 66–74 (2009). Here the authors describe human LTi cells and show that they can produce IL-17 and IL-22. ArticleCAS Google Scholar
Luther, S. A., Ansel, K. M. & Cyster, J. G. Overlapping roles of CXCL13, interleukin 7 receptorα, and CCR7 ligands in lymph node development. J. Exp. Med.197, 1191–1198 (2003). ArticleCASPubMedPubMed Central Google Scholar
Ansel, K. M. et al. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature406, 309–314 (2000). ArticleCASPubMed Google Scholar
Ohl, L. et al. Cooperating mechanisms of CXCR5 and CCR7 in development and organization of secondary lymphoid organs. J. Exp. Med.197, 1199–1204 (2003). ArticleCASPubMedPubMed Central Google Scholar
Nakano, H. & Gunn, M. D. Gene duplications at the chemokine locus on mouse chromosome 4: multiple strain-specific haplotypes and the deletion of secondary lymphoid-organ chemokine and EBI-1 ligand chemokine genes in the Plt mutation. J. Immunol.166, 361–369 (2001). ArticleCASPubMed Google Scholar
Forster, R. et al. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell99, 23–33 (1999). ArticleCASPubMed Google Scholar
Vondenhoff, M. F. et al. Lymph sacs are not required for the initiation of lymph node formation. Development136, 29–34 (2009). ArticleCASPubMed Google Scholar
Niederreither, K. & Dolle, P. Retinoic acid in development: towards an integrated view. Nature Rev. Genet.9, 541–553 (2008). ArticleCASPubMed Google Scholar
Berggren, K., Ezerman, E. B., McCaffery, P. & Forehand, C. J. Expression and regulation of the retinoic acid synthetic enzyme RALDH-2 in the embryonic chicken wing. Dev. Dyn.222, 1–16 (2001). ArticleCASPubMed Google Scholar
Ji, S. J. et al. Mesodermal and neuronal retinoids regulate the induction and maintenance of limb innervating spinal motor neurons. Dev. Biol.297, 249–261 (2006). ArticleCASPubMed Google Scholar
Sockanathan, S. & Jessell, T. M. Motor neuron-derived retinoid signaling specifies the subtype identity of spinal motor neurons. Cell94, 503–514 (1998). ArticleCASPubMed Google Scholar
Bekker, M. N. et al. Increased NCAM expression and vascular development in trisomy 16 mouse embryos: relationship with nuchal translucency. Pediatr. Res.58, 1222–1227 (2005). ArticleCASPubMed Google Scholar
Bekker, M. N. et al. Nuchal edema and venous-lymphatic phenotype disturbance in human fetuses and mouse embryos with aneuploidy. J. Soc. Gynecol. Investig.13, 209–216 (2006). ArticlePubMed Google Scholar
Gittenberger-de Groot, A. C. et al. Abnormal lymphatic development in trisomy 16 mouse embryos precedes nuchal edema. Dev. Dyn.230, 378–384 (2004). ArticlePubMed Google Scholar
Niederreither, K. et al. The regional pattern of retinoic acid synthesis by RALDH2 is essential for the development of posterior pharyngeal arches and the enteric nervous system. Development130, 2525–2534 (2003). ArticleCASPubMed Google Scholar
Fu, M. et al. Vitamin A facilitates enteric nervous system precursor migration by reducing Pten accumulation. Development137, 631–640 (2010). ArticleCASPubMedPubMed Central Google Scholar
Maden, M. Retinoic acid in the development, regeneration and maintenance of the nervous system. Nature Rev. Neurosci.8, 755–765 (2007). ArticleCAS Google Scholar
Zhelyaznik, N. & Mey, J. Regulation of retinoic acid receptors α, β and retinoid X receptor α after sciatic nerve injury. Neuroscience141, 1761–1774 (2006). ArticleCASPubMed Google Scholar
Zhelyaznik, N., Schrage, K., McCaffery, P. & Mey, J. Activation of retinoic acid signalling after sciatic nerve injury: up-regulation of cellular retinoid binding proteins. Eur. J. Neurosci.18, 1033–1040 (2003). ArticlePubMed Google Scholar
Lu, X. et al. The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature432, 179–186 (2004). ArticleCASPubMed Google Scholar
Eichmann, A., Makinen, T. & Alitalo, K. Neural guidance molecules regulate vascular remodeling and vessel navigation. Genes Dev.19, 1013–1021 (2005). ArticleCASPubMed Google Scholar
Oliver, G. & Alitalo, K. The lymphatic vasculature: recent progress and paradigms. Annu. Rev. Cell Dev. Biol.21, 457–483 (2005). ArticleCASPubMed Google Scholar
Karpanen, T. & Alitalo, K. Molecular biology and pathology of lymphangiogenesis. Annu. Rev. Pathol.3, 367–397 (2008). ArticleCASPubMed Google Scholar
Le, B. B. et al. VEGF-C is a trophic factor for neural progenitors in the vertebrate embryonic brain. Nature Neurosci.9, 340–348 (2006). ArticleCAS Google Scholar
Wang, Y. et al. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature465, 483–486 (2010). ArticleCASPubMed Google Scholar
Sawamiphak, S. et al. Ephrin-B2 regulates VEGFR2 function in developmental and tumour angiogenesis. Nature465, 487–491 (2010). ArticleCASPubMed Google Scholar
Kim, D. et al. Regulation of peripheral lymph node genesis by the tumor necrosis factor family member TRANCE. J. Exp. Med.192, 1467–1478 (2000). ArticleCASPubMedPubMed Central Google Scholar
Honda, K. et al. Molecular basis for hematopoietic/mesenchymal interaction during initiation of Peyer's patch organogenesis. J. Exp. Med.193, 621–630 (2001). ArticleCASPubMedPubMed Central Google Scholar
Cupedo, T., Jansen, W., Kraal, G. & Mebius, R. E. Induction of secondary and tertiary lymphoid structures in the skin. Immunity21, 655–667 (2004). ArticleCASPubMed Google Scholar
Okamoto, N., Chihara, R., Shimizu, C., Nishimoto, S. & Watanabe, T. Artificial lymph nodes induce potent secondary immune responses in naive and immunodeficient mice. J. Clin. Invest.117, 997–1007 (2007). ArticleCASPubMedPubMed Central Google Scholar
Hashi, H. et al. Compartmentalization of Peyer's patch anlagen before lymphocyte entry. J. Immunol.166, 3702–3709 (2001). ArticleCASPubMed Google Scholar
Fukuyama, S. et al. Initiation of NALT organogenesis is independent of the IL-7R, LTβR, and NIK signaling pathways but requires the Id2 gene and CD3−CD4+CD45+ cells. Immunity17, 31–40 (2002). ArticleCASPubMed Google Scholar
Harmsen, A. et al. Cutting edge: organogenesis of nasal-associated lymphoid tissue (NALT) occurs independently of lymphotoxin-α (LTα) and retinoic acid receptor-related orphan receptor-γ, but the organization of NALT is LTα dependent. J. Immunol.168, 986–990 (2002). ArticleCASPubMed Google Scholar
Fukuyama, S. et al. Cutting edge: uniqueness of lymphoid chemokine requirement for the initiation and maturation of nasopharynx-associated lymphoid tissue organogenesis. J. Immunol.177, 4276–4280 (2006). ArticleCASPubMed Google Scholar
Rangel-Moreno, J. et al. Role of CXC chemokine ligand 13, CC chemokine ligand (CCL) 19, and CCL21 in the organization and function of nasal-associated lymphoid tissue. J. Immunol.175, 4904–4913 (2005). ArticleCASPubMed Google Scholar
Krege, J., Seth, S., Hardtke, S., Valos-Misslitz, A. C. & Forster, R. Antigen-dependent rescue of nose-associated lymphoid tissue (NALT) development independent of LTβR and CXCR5 signaling. Eur. J. Immunol.39, 2765–2778 (2009). ArticleCASPubMed Google Scholar
Nagatake, T. et al. Id2, RORγt, and LTβR-independent initiation of lymphoid organogenesis in ocular immunity. J. Exp. Med.206, 2351–2364 (2009). In this study, the authors show that the development of lymphoid structures associated with the tear ducts occurs independently of LTi cells. ArticleCASPubMedPubMed Central Google Scholar
Kanamori, Y. et al. Identification of novel lymphoid tissues in murine intestinal mucosa where clusters of c-kit+ IL-7R+ Thy1+ lympho-hemopoietic progenitors develop. J. Exp. Med.184, 1449–1459 (1996). ArticleCASPubMed Google Scholar
McDonald, K. G., McDonough, J. S., Dieckgraefe, B. K. & Newberry, R. D. Dendritic cells produce CXCL13 and participate in the development of murine small intestine lymphoid tissues. Am. J. Pathol.176, 2367–2377 (2010). ArticleCASPubMedPubMed Central Google Scholar
Tsuji, M. et al. Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity29, 261–271 (2008). ArticleCASPubMed Google Scholar
Hamada, H. et al. Identification of multiple isolated lymphoid follicles on the antimesenteric wall of the mouse small intestine. J. Immunol.168, 57–64 (2002). ArticleCASPubMed Google Scholar
Pabst, O. et al. Adaptation of solitary intestinal lymphoid tissue in response to microbiota and chemokine receptor CCR7 signaling. J. Immunol.177, 6824–6832 (2006). ArticleCASPubMed Google Scholar
Bouskra, D. et al. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature456, 507–510 (2008). ArticleCASPubMed Google Scholar
Salzman, N. H. et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nature Immunol.11, 76–83 (2010). ArticleCAS Google Scholar
McDonald, K. G. et al. CC chemokine receptor 6 expression by B lymphocytes is essential for the development of isolated lymphoid follicles. Am. J. Pathol.170, 1229–1240 (2007). ArticleCASPubMedPubMed Central Google Scholar
Eberl, G. & Littman, D. R. Thymic origin of intestinal αβ T cells revealed by fate mapping of RORγt+ cells. Science305, 248–251 (2004). ArticleCASPubMed Google Scholar
Moro, K. et al. Innate production of TH2 cytokines by adipose tissue-associated c-Kit+Sca-1+ lymphoid cells. Nature463, 540–544 (2010). ArticleCASPubMed Google Scholar
Rangel-Moreno, J. et al. Omental milky spots develop in the absence of lymphoid tissue-inducer cells and support B and T cell responses to peritoneal antigens. Immunity30, 731–743 (2009). ArticleCASPubMedPubMed Central Google Scholar
Aloisi, F. & Pujol-Borrell, R. Lymphoid neogenesis in chronic inflammatory diseases. Nature Rev. Immunol.6, 205–217 (2006). ArticleCAS Google Scholar
Moyron-Quiroz, J. E. et al. Role of inducible bronchus associated lymphoid tissue (iBALT) in respiratory immunity. Nature Med.10, 927–934 (2004). ArticleCASPubMed Google Scholar
GeurtsvanKessel, C. H. et al. Dendritic cells are crucial for maintenance of tertiary lymphoid structures in the lung of influenza virus-infected mice. J. Exp. Med.206, 2339–2349 (2009). ArticleCASPubMedPubMed Central Google Scholar
Rangel-Moreno, J., Moyron-Quiroz, J. E., Hartson, L., Kusser, K. & Randall, T. D. Pulmonary expression of CXC chemokine ligand 13, CC chemokine ligand 19, and CC chemokine ligand 21 is essential for local immunity to influenza. Proc. Natl Acad. Sci. USA104, 10577–10582 (2007). By depletion of all secondary lymphoid organs, the authors show the crucial role of the homeostatic chemokines CXCL13, CCL21 and CCL19 for local B and T cell responses in the lungs. ArticleCASPubMedPubMed Central Google Scholar
Anderson, M. S. & Bluestone, J. A. The NOD mouse: a model of immune dysregulation. Ann. Rev. Immunol.23, 447–485 (2005). ArticleCAS Google Scholar
Penaranda, C., Tang, Q., Ruddle, N. H. & Bluestone, J. A. Prevention of diabetes by FTY720-mediated stabilization of peri-islet tertiary lymphoid organs. Diabetes59, 1461–1468 (2010). ArticleCASPubMedPubMed Central Google Scholar
Lee, Y. et al. Recruitment and activation of naive T cells in the islets by lymphotoxin β receptor-dependent tertiary lymphoid structure. Immunity25, 499–509 (2006). ArticleCASPubMed Google Scholar
Wu, Q. et al. Reversal of spontaneous autoimmune insulitis in nonobese diabetic mice by soluble lymphotoxin receptor. J. Exp. Med.193, 1327–1332 (2001). ArticleCASPubMedPubMed Central Google Scholar
Drayton, D. L., Liao, S., Mounzer, R. H. & Ruddle, N. H. Lymphoid organ development: from ontogeny to neogenesis. Nature Immunol.7, 344–353 (2006). ArticleCAS Google Scholar
Perrier, P. et al. Distinct transcriptional programs activated by interleukin-10 with or without lipopolysaccharide in dendritic cells: induction of the B cell-activating chemokine, CXC chemokine ligand 13. J. Immunol.172, 7031–7042 (2004). ArticleCASPubMed Google Scholar
Carlsen, H. S., Baekkevold, E. S., Morton, H. C., Haraldsen, G. & Brandtzaeg, P. Monocyte-like and mature macrophages produce CXCL13 (B cell-attracting chemokine 1) in inflammatory lesions with lymphoid neogenesis. Blood104, 3021–3027 (2004). ArticleCASPubMed Google Scholar
Columba-Cabezas, S. et al. Suppression of established experimental autoimmune encephalomyelitis and formation of meningeal lymphoid follicles by lymphotoxin β receptor-Ig fusion protein. J. Neuroimmunol.179, 76–86 (2006). ArticleCASPubMed Google Scholar
Lotzer, K. et al. Mouse aorta smooth muscle cells differentiate into lymphoid tissue organizer-like cells on combined tumor necrosis factor receptor-1/lymphotoxin β-receptor NF-κB signaling. Arterioscler. Thromb. Vasc. Biol.30, 395–402 (2010). ArticleCASPubMedPubMed Central Google Scholar
Link, A. et al. Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nature Immunol.8, 1255–1265 (2007). CAS Google Scholar
Bajenoff, M. et al. Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity25, 989–1001 (2006). ArticleCASPubMedPubMed Central Google Scholar
Hammerschmidt, S. I. et al. Stromal mesenteric lymph node cells are essential for the generation of gut-homing T cells in vivo. J. Exp. Med.205, 2483–2490 (2008). ArticleCASPubMedPubMed Central Google Scholar
Molenaar, R. et al. Lymph node stromal cells support dendritic cell-induced gut-homing of T cells. J. Immunol.183, 6395–6402 (2009). ArticleCASPubMed Google Scholar
Gardner, J. M. et al. Deletional tolerance mediated by extrathymic Aire-expressing cells. Science321, 843–847 (2008). This paper shows that AIRE-expressing stromal cells in secondary lymphoid organs are involved in deleting autoreactive T cells through expression of self antigens. ArticleCASPubMedPubMed Central Google Scholar
Fletcher, A. L. et al. Lymph node fibroblastic reticular cells directly present peripheral tissue antigen under steady-state and inflammatory conditions. J. Exp. Med.207, 689–697 (2010). ArticleCASPubMedPubMed Central Google Scholar
Cohen, J. N. et al. Lymph node-resident lymphatic endothelial cells mediate peripheral tolerance via Aire-independent direct antigen presentation. J. Exp. Med.207, 681–688 (2010). ArticleCASPubMedPubMed Central Google Scholar
Nichols, L. A. et al. Deletional self-tolerance to a melanocyte/melanoma antigen derived from tyrosinase is mediated by a radio-resistant cell in peripheral and mesenteric lymph nodes. J. Immunol.179, 993–1003 (2007). ArticleCASPubMed Google Scholar
Lee, J. W. et al. Peripheral antigen display by lymph node stroma promotes T cell tolerance to intestinal self. Nature Immunol.8, 181–190 (2007). This is the first paper to show the capacity of lymph node stromal cells to present peripheral tissue antigens to CD8+ T cells, leading to their activation and subsequent induction of tolerance. ArticleCAS Google Scholar
Katakai, T. et al. Organizer-like reticular stromal cell layer common to adult secondary lymphoid organs. J. Immunol.181, 6189–6200 (2008). ArticleCASPubMed Google Scholar
Cupedo, T. et al. Presumptive lymph node organizers are differentially represented in developing mesenteric and peripheral nodes. J. Immunol.173, 2968–2975 (2004). ArticleCASPubMed Google Scholar
White, A. et al. Lymphotoxin-α-dependent and -independent signals regulate stromal organiser cell homeostasis during lymph node organogenesis. Blood110, 1950–1959 (2007). ArticleCASPubMed Google Scholar
Scandella, E. et al. Restoration of lymphoid organ integrity through the interaction of lymphoid tissue-inducer cells with stroma of the T cell zone. Nature Immunol.9, 667–675 (2008). This paper shows a role for LTi cells in restoring the organization of the spleen after a viral infection. ArticleCAS Google Scholar
Kim, M. Y. et al. CD4+CD3− accessory cells costimulate primed CD4 T cells through OX40 and CD30 at sites where T cells collaborate with B cells. Immunity18, 643–654 (2003). ArticleCASPubMed Google Scholar
Luci, C. et al. Influence of the transcription factor RORγt on the development of NKp46+ cell populations in gut and skin. Nature Immunol.10, 75–82 (2009). ArticleCAS Google Scholar
Lochner, M. et al. In vivo equilibrium of proinflammatory IL-17+ and regulatory IL-10+ Foxp3+ RORγt+ T cells. J. Exp. Med.205, 1381–1393 (2008). ArticleCASPubMedPubMed Central Google Scholar
Sanos, S. L. et al. RORγt and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nature Immunol.10, 83–91 (2009). ArticleCAS Google Scholar
Marchesi, F. et al. CXCL13 expression in the gut promotes accumulation of IL-22-producing lymphoid tissue-inducer cells, and formation of isolated lymphoid follicles. Mucosal Immunol.2, 486–494 (2009). ArticleCASPubMed Google Scholar
Cella, M. et al. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature457, 722–725 (2009). ArticleCASPubMed Google Scholar
Satoh-Takayama, N. et al. IL-7 and IL-15 independently program the differentiation of intestinal CD3−NKp46+ cell subsets from Id2-dependent precursors. J. Exp. Med.207, 273–280 (2010). ArticleCASPubMedPubMed Central Google Scholar
Hughes, T. et al. Stage 3 immature human natural killer cells found in secondary lymphoid tissue constitutively and selectively express the TH17 cytokine interleukin-22. Blood113, 4008–4010 (2009). ArticleCASPubMedPubMed Central Google Scholar
Crellin, N. K., Trifari, S., Kaplan, C. D., Cupedo, T. & Spits, H. Human NKp44+IL-22+ cells and LTi-like cells constitute a stable RORC+ lineage distinct from conventional natural killer cells. J. Exp. Med.207, 281–290 (2010). ArticleCASPubMedPubMed Central Google Scholar
Vivier, E., Spits, H. & Cupedo, T. Interleukin-22-producing innate immune cells: new players in mucosal immunity and tissue repair? Nature Rev. Immunol.9, 229–234 (2009). ArticleCAS Google Scholar
Satoh-Takayama, N. et al. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity29, 958–970 (2008). ArticleCASPubMed Google Scholar
Colonna, M. Interleukin-22-producing natural killer cells and lymphoid tissue inducer-like cells in mucosal immunity. Immunity31, 15–23 (2009). ArticleCASPubMed Google Scholar
Ouyang, W., Kolls, J. K. & Zheng, Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity28, 454–467 (2008). ArticleCASPubMedPubMed Central Google Scholar
Zheng, Y. et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nature Med.14, 282–289 (2008). ArticleCASPubMed Google Scholar
Mora, J. R., Iwata, M. & von Andrian, U. H. Vitamin effects on the immune system: vitamins A and D take centre stage. Nature Rev. Immunol.8, 685–698 (2008). ArticleCAS Google Scholar
Schug, T. T., Berry, D. C., Shaw, N. S., Travis, S. N. & Noy, N. Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell129, 723–733 (2007). ArticleCASPubMedPubMed Central Google Scholar
Niederreither, K., Fraulob, V., Garnier, J. M., Chambon, P. & Dolle, P. Differential expression of retinoic acid-synthesizing (RALDH) enzymes during fetal development and organ differentiation in the mouse. Mech. Dev.110, 165–171 (2002). ArticleCASPubMed Google Scholar
Iwata, M. et al. Retinoic acid imprints gut-homing specificity on T cells. Immunity21, 527–538 (2004). ArticleCASPubMed Google Scholar
Mucida, D. et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science317, 256–260 (2007). ArticleCASPubMed Google Scholar
Mora, J. R. et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science314, 1157–1160 (2006). ArticleCASPubMed Google Scholar
Sauka-Spengler, T. & Bronner-Fraser, M. A gene regulatory network orchestrates neural crest formation. Nature Rev. Mol. Cell Biol.9, 557–568 (2008). ArticleCAS Google Scholar
Young, H. M. & Newgreen, D. Enteric neural crest-derived cells: origin, identification, migration, and differentiation. Anat. Rec.262, 1–15 (2001). ArticleCASPubMed Google Scholar
Young, H. M., Jones, B. R. & McKeown, S. J. The projections of early enteric neurons are influenced by the direction of neural crest cell migration. J. Neurosci.22, 6005–6018 (2002). ArticleCASPubMedPubMed Central Google Scholar
Borovikova, L. V. et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature405, 458–462 (2000). ArticleCASPubMed Google Scholar
Tracey, K. J. Reflex control of immunity. Nature Rev. Immunol.9, 418–428 (2009). ArticleCAS Google Scholar
de Jonge, W. J. et al. Stimulation of the vagus nerve attenuates macrophage activation by activating the Jak2–STAT3 signaling pathway. Nature Immunol.6, 844–851 (2005). ArticleCAS Google Scholar
Van Der Zanden, E. P., Boeckxstaens, G. E. & de Jonge, W. J. The vagus nerve as a modulator of intestinal inflammation. Neurogastroenterol. Motil.21, 6–17 (2009). ArticleCASPubMed Google Scholar
Wang, H. et al. Nicotinic acetylcholine receptor α7 subunit is an essential regulator of inflammation. Nature421, 384–388 (2003). ArticleCASPubMed Google Scholar
Ying, X., Chan, K., Shenoy, P., Hill, M. & Ruddle, N. H. Lymphotoxin plays a crucial role in the development and function of nasal-associated lymphoid tissue through regulation of chemokines and peripheral node addressin. Am. J. Pathol.166, 135–146 (2005). ArticleCASPubMedPubMed Central Google Scholar
Velaga, S. et al. Chemokine receptor CXCR5 supports solitary intestinal lymphoid tissue formation, B cell homing, and induction of intestinal IgA responses. J. Immunol.182, 2610–2619 (2009). ArticleCASPubMed Google Scholar