Divergence of Vascular Specification in Visceral Lymphoid Organs—Genetic Determinants and Differentiation Checkpoints

REFERENCES

• Gretz JE, Kaldjian EP, Anderson AO, Shaw S. Sophisticated strategies for information encounter in the lymph node: the reticular network as a conduit of soluble information and a highway for cell traffic. J Immunol 1996;157(2):495–499.
   PubMed Web of Science ®Google Scholar
• Sixt M, Kanazawa N, Selg M, The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity 2005;22(1):19–29.
   PubMed Web of Science ®Google Scholar
• Ahrendt M, Hammerschmidt SI, Pabst O, Stromal cells confer lymph node-specific properties by shaping a unique microenvironment influencing local immune responses. J Immunol 2008;181(3):1898–1907.
   PubMed Web of Science ®Google Scholar
• Tan JK, Watanabe T. Murine spleen tissue regeneration from neonatal spleen capsule requires lymphotoxin priming of stromal cells. J Immunol 2014;193(3):1194–1203.
   PubMed Web of Science ®Google Scholar
• Lu TT, Browning JL. Role of the lymphotoxin/LIGHT system in the development and maintenance of reticular networks and vasculature in lymphoid tissues. Front Immunol 2014;5:47.
   PubMed Web of Science ®Google Scholar
• Malhotra D, Fletcher AL, Turley SJ. Stromal and hematopoietic cells in secondary lymphoid organs: partners in immunity. Immunol Rev 2013;251(1):160–176.
   PubMed Web of Science ®Google Scholar
• den Haan JM, Mebius RE, Kraal G. Stromal cells of the mouse spleen. Front Immunol 2012;3:201.
   PubMed Web of Science ®Google Scholar
• Brendolan A, Ferretti E, Salsi V, et al. A Pbx1-dependent genetic and transcriptional network regulates spleen ontogeny. Development 2005;132(13):3113–3126.
   PubMed Web of Science ®Google Scholar
• Castagnaro L, Lenti E, Maruzzelli S, Nkx2–5(+)islet1(+) mesenchymal precursors generate distinct spleen stromal cell subsets and participate in restoring stromal network integrity. Immunity 2013;38(4):782–791.
   PubMed Web of Science ®Google Scholar
• Krautler NJ, Kana V, Kranich J, Follicular dendritic cells emerge from ubiquitous perivascular precursors. Cell 2012;150(1):194–206.
   PubMed Web of Science ®Google Scholar
• Zindl CL, Kim TH, Zeng M, et al. The lymphotoxin LTalpha(1)beta(2) controls postnatal and adult spleen marginal sinus vascular structure and function. Immunity 2009;30(3):408–420.
   PubMed Web of Science ®Google Scholar
• Vondenhoff MF, Desanti GE, Cupedo T, Separation of splenic red and white pulp occurs before birth in a LTalphabeta-independent manner. J Leukoc Biol 2008;84(1):152–161.
   PubMed Web of Science ®Google Scholar
• Balazs M, Horvath G, Grama L, Balogh P. Phenotypic identification and development of distinct microvascular compartments in the postnatal mouse spleen. Cell Immunol 2001;212(2):126–137.
   PubMed Web of Science ®Google Scholar
• Okada T, Ngo VN, Ekland EH, Chemokine requirements for B cell entry to lymph nodes and Peyer's patches. J Exp Med 2002;196(1):65–75.
   PubMed Web of Science ®Google Scholar
• Ebisuno Y, Tanaka T, Kanemitsu N, Cutting edge: the B cell chemokine CXC chemokine ligand 13/B lymphocyte chemoattractant is expressed in the high endothelial venules of lymph nodes and Peyer's patches and affects B cell trafficking across high endothelial venules. J Immunol 2003;171(4):1642–1646.
   PubMed Web of Science ®Google Scholar
• Warnock RA, Campbell JJ, Dorf ME, The role of chemokines in the microenvironmental control of T versus B cell arrest in Peyer's patch high endothelial venules. J Exp Med 2000;191(1):77–88.
   PubMed Web of Science ®Google Scholar
• Mebius RE, Streeter PR, Michie S, A developmental switch in lymphocyte homing receptor and endothelial vascular addressin expression regulates lymphocyte homing and permits CD4+ CD3- cells to colonize lymph nodes. Proc Natl Acad Sci U S A 1996;93(20):11019–11024.
   PubMed Web of Science ®Google Scholar
• Mebius RE. Organogenesis of lymphoid tissues. Nat Rev Immunol 2003;3(4):292–303.
   PubMed Web of Science ®Google Scholar
• van de Pavert SA, Mebius RE. Development of secondary lymphoid organs in relation to lymphatic vasculature. Adv Anat Embryol Cell Biol 2014;214:81–91.
   PubMed Web of Science ®Google Scholar
• Vondenhoff MF, van de Pavert SA, Dillard ME, Lymph sacs are not required for the initiation of lymph node formation. Development 2009;136(1):29–34.
   PubMed Web of Science ®Google Scholar
• Wigle JT, Harvey N, Detmar M, An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J 2002;21(7):1505–1513.
   PubMed Web of Science ®Google Scholar
• Srinivasan RS, Dillard ME, Lagutin OV, Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes Dev 2007;21(19):2422–2432.
   PubMed Web of Science ®Google Scholar
• Sabine A, Agalarov Y, Maby-El Hajjami H, Mechanotransduction, PROX1, and FOXC2 cooperate to control connexin37 and calcineurin during lymphatic-valve formation. Dev Cell 2012;22(2):430–445.
   PubMed Web of Science ®Google Scholar
• Hess PR, Rawnsley DR, Jakus Z, Platelets mediate lymphovenous hemostasis to maintain blood-lymphatic separation throughout life. J Clin Invest 2014;124(1):273–284.
   PubMed Web of Science ®Google Scholar
• Cupedo T, Jansen W, Kraal G, Mebius RE. Induction of secondary and tertiary lymphoid structures in the skin. Immunity 2004;21(5):655–667.
   PubMed Web of Science ®Google Scholar
• Hashi H, Yoshida H, Honda K, Compartmentalization of Peyer's patch anlagen before lymphocyte entry. J Immunol 2001;166(6):3702–3709.
   PubMed Web of Science ®Google Scholar
• Lacorre DA, Baekkevold ES, Garrido I, Plasticity of endothelial cells: rapid dedifferentiation of freshly isolated high endothelial venule endothelial cells outside the lymphoid tissue microenvironment. Blood 2004;103(11):4164–4172.
   PubMed Web of Science ®Google Scholar
• Mebius RE, Streeter PR, Breve J, The influence of afferent lymphatic vessel interruption on vascular addressin expression. J Cell Biol 1991;115(1):85–95.
   PubMed Web of Science ®Google Scholar
• Girard JP, Baekkevold ES, Yamanaka T, Heterogeneity of endothelial cells: the specialized phenotype of human high endothelial venules characterized by suppression subtractive hybridization. Am J Pathol 1999;155(6):2043–2055.
   PubMed Web of Science ®Google Scholar
• Hayasaka H, Taniguchi K, Fukai S, Miyasaka M. Neogenesis and development of the high endothelial venules that mediate lymphocyte trafficking. Cancer Sci 2010;101(11):2302–2308.
   PubMed Web of Science ®Google Scholar
• Lee M, Kiefel H, LaJevic MD, Transcriptional programs of lymphoid tissue capillary and high endothelium reveal control mechanisms for lymphocyte homing. Nat Immunol 2014;15(10):982–995.
   PubMed Web of Science ®Google Scholar
• Nitschke L. CD22 and Siglec-G: B-cell inhibitory receptors with distinct functions. Immunol Rev 2009;230(1):128–143.
   PubMed Web of Science ®Google Scholar
• Drayton DL, Bonizzi G, Ying X, I kappa B kinase complex alpha kinase activity controls chemokine and high endothelial venule gene expression in lymph nodes and nasal-associated lymphoid tissue. J Immunol 2004;173(10):6161–6168.
   PubMed Web of Science ®Google Scholar
• Browning JL, Allaire N, Ngam-Ek A, Lymphotoxin-beta receptor signaling is required for the homeostatic control of HEV differentiation and function. Immunity 2005;23(5):539–550.
   PubMed Web of Science ®Google Scholar
• Onder L, Danuser R, Scandella E, Endothelial cell-specific lymphotoxin-beta receptor signaling is critical for lymph node and high endothelial venule formation. J Exp Med 2013;210(3):465–473.
   PubMed Web of Science ®Google Scholar
• Picarella DE, Kratz A, Li CB, Insulitis in transgenic mice expressing tumor necrosis factor beta (lymphotoxin) in the pancreas. Proc Natl Acad Sci U S A 1992;89(21):10036–10040.
   PubMed Web of Science ®Google Scholar
• Kratz A, Campos-Neto A, Hanson MS, Ruddle NH. Chronic inflammation caused by lymphotoxin is lymphoid neogenesis. J Exp Med 1996;183(4):1461–1472.
   PubMed Web of Science ®Google Scholar
• Drayton DL, Chan K, Lesslauer W, Lymphocyte traffic in lymphoid organ neogenesis: differential roles of Ltalpha and LTalphabeta. Adv Exp Med Biol 2002;512:43–48.
   PubMed Web of Science ®Google Scholar
• Drayton DL, Ying X, Lee J, Ectopic LT alpha beta directs lymphoid organ neogenesis with concomitant expression of peripheral node addressin and a HEV-restricted sulfotransferase. J Exp Med 2003;197(9):1153–1163.
   PubMed Web of Science ®Google Scholar
• Cuff CA, Sacca R, Ruddle NH. Differential induction of adhesion molecule and chemokine expression by LTalpha3 and LTalphabeta in inflammation elucidates potential mechanisms of mesenteric and peripheral lymph node development. J Immunol 1999;162(10):5965–5972.
   PubMed Web of Science ®Google Scholar
• Sacca R, Cuff CA, Lesslauer W, Ruddle NH. Differential activities of secreted lymphotoxin-alpha3 and membrane lymphotoxin-alpha1beta2 in lymphotoxin-induced inflammation: critical role of TNF receptor 1 signaling. J Immunol 1998;160(1):485–491.
   PubMed Web of Science ®Google Scholar
• Sikorski EE, Hallmann R, Berg EL, Butcher EC. The Peyer's patch high endothelial receptor for lymphocytes, the mucosal vascular addressin, is induced on a murine endothelial cell line by tumor necrosis factor-alpha and IL-1. J Immunol 1993;151(10):5239–5250.
   PubMed Web of Science ®Google Scholar
• Takeuchi M, Baichwal VR. Induction of the gene encoding mucosal vascular addressin cell adhesion molecule 1 by tumor necrosis factor alpha is mediated by NF-kappa B proteins. Proc Natl Acad Sci U S A 1995;92(8):3561–3565.
   PubMed Web of Science ®Google Scholar
• Cuff CA, Schwartz J, Bergman CM, Lymphotoxin alpha3 induces chemokines and adhesion molecules: insight into the role of LT alpha in inflammation and lymphoid organ development. J Immunol 1998;161(12):6853–6860.
   PubMed Web of Science ®Google Scholar
• Moussion C, Girard JP. Dendritic cells control lymphocyte entry to lymph nodes through high endothelial venules. Nature 2011;479(7374):542–546.
   PubMed Web of Science ®Google Scholar
• Tumanov AV, Koroleva EP, Guo X, Lymphotoxin controls the IL-22 protection pathway in gut innate lymphoid cells during mucosal pathogen challenge. Cell Host Microbe 2011;10(1):44–53.
   PubMed Web of Science ®Google Scholar
• Liao S, Ruddle NH. Synchrony of high endothelial venules and lymphatic vessels revealed by immunization. J Immunol 2006;177(5):3369–3379.
   PubMed Web of Science ®Google Scholar
• Schippers A, Leuker C, Pabst O, Mucosal addressin cell-adhesion molecule-1 controls plasma-cell migration and function in the small intestine of mice. Gastroenterology 2009;137(3):924–933.
   PubMed Web of Science ®Google Scholar
• Pabst O, Forster R, Lipp M, NKX2.3 is required for MAdCAM-1 expression and homing of lymphocytes in spleen and mucosa-associated lymphoid tissue. EMBO J 2000;19(9):2015–2023.
   PubMed Web of Science ®Google Scholar
• Wang CC, Biben C, Robb L, Homeodomain factor Nkx2–3 controls regional expression of leukocyte homing coreceptor MAdCAM-1 in specialized endothelial cells of the viscera. Dev Biol 2000;224(2):152–167.
   PubMed Web of Science ®Google Scholar
• Balogh P, Balazs M, Czompoly T, Distinct roles of lymphotoxin-beta signaling and the homeodomain transcription factor Nkx2.3 in the ontogeny of endothelial compartments in spleen. Cell Tissue Res 2007;328(3):473–486.
   PubMed Web of Science ®Google Scholar
• Czompoly T, Labadi A, Kellermayer Z, Transcription factor Nkx2–3 controls the vascular identity and lymphocyte homing in the spleen. J Immunol 2011;186(12):6981–6989.
   PubMed Web of Science ®Google Scholar
• Kellermayer Z, Labadi A, Czompoly T, Absence of Nkx2–3 homeodomain transcription factor induces the formation of LYVE-1-positive endothelial cysts without lymphatic commitment in the spleen. J Histochem Cytochem 2011;59(7):690–700.
   PubMed Web of Science ®Google Scholar
• Kurusu M, Nagao T, Walldorf U, Genetic control of development of the mushroom bodies, the associative learning centers in the Drosophila brain, by the eyeless, twin of eyeless, and Dachshund genes. Proc Natl Acad Sci U S A 2000;97(5):2140–2144.
   PubMed Web of Science ®Google Scholar
• Pallafacchina G, Francois S, Regnault B, An adult tissue-specific stem cell in its niche: a gene profiling analysis of in vivo quiescent and activated muscle satellite cells. Stem Cell Res 2010;4(2):77–91.
   PubMed Web of Science ®Google Scholar
• Wu K, Jiao X, Li Z, Cell fate determination factor Dachshund reprograms breast cancer stem cell function. J Biol Chem 2011;286(3):2132–2142.
   PubMed Web of Science ®Google Scholar
• Yan W, Wu K, Herman JG, Epigenetic regulation of DACH1, a novel Wnt signaling component in colorectal cancer. Epigenetics 2013;8(12):1373–1383.
   PubMed Web of Science ®Google Scholar
• Chen K, Wu K, Cai S, Dachshund binds p53 to block the growth of lung adenocarcinoma cells. Cancer Res 2013;73(11):3262–3274.
   PubMed Web of Science ®Google Scholar
• Kellermayer Z, Mihalj M, Labadi A, Absence of Nkx2–3 homeodomain transcription factor reprograms the endothelial addressin preference for lymphocyte homing in Peyer's patches. J Immunol 2014;193(10):5284–5293.
   PubMed Web of Science ®Google Scholar
• Steiniger B, Stachniss V, Schwarzbach H, Barth PJ. Phenotypic differences between red pulp capillary and sinusoidal endothelia help localizing the open splenic circulation in humans. Histochem Cell Biol 2007;128(5):391–398.
   PubMed Web of Science ®Google Scholar
• Yu W, Hegarty JP, Berg A, PTPN2 is associated with Crohn's disease and its expression is regulated by NKX2–3. Dis Markers 2012;32(2):83–91.
   PubMed Web of Science ®Google Scholar
• Plevy S, Silverberg MS, Lockton S, Combined serological, genetic, and inflammatory markers differentiate non-IBD, Crohn's disease, and ulcerative colitis patients. Inflamm Bowel Dis 2013;19(6):1139–1148.
   PubMed Web of Science ®Google Scholar
• Fisher SA, Tremelling M, Anderson CA, Genetic determinants of ulcerative colitis include the ECM1 locus and five loci implicated in Crohn's disease. Nat Genet 2008;40(6):710–712.
   PubMed Web of Science ®Google Scholar
• Parkes M, Barrett JC, Prescott NJ, Sequence variants in the autophagy gene IRGM and multiple other replicating loci contribute to Crohn's disease susceptibility. Nat Genet 2007;39(7):830–832.
   PubMed Web of Science ®Google Scholar
• Yu W, Lin Z, Kelly AA, Association of a Nkx2–3 polymorphism with Crohn's disease and expression of Nkx2–3 is up-regulated in B cell lines and intestinal tissues with Crohn's disease. J Crohns Colitis 2009;3(3):189–195.
   PubMed Web of Science ®Google Scholar
• Yu W, Lin Z, Hegarty JP, Genes regulated by Nkx2–3 in siRNA-mediated knockdown B cells: implication of endothelin-1 in inflammatory bowel disease. Mol Genet Metab 2010;100(1):88–95.
   PubMed Web of Science ®Google Scholar
• Hemmerich S, Bistrup A, Singer MS, Sulfation of L-selectin ligands by an HEV-restricted sulfotransferase regulates lymphocyte homing to lymph nodes. Immunity 2001;15(2):237–247.
   PubMed Web of Science ®Google Scholar