CXCL12 and CCL20 Play a Significant Role in Mucosal T-Lymphocyte Adherence to Intestinal Microvessels in Mice

REFERENCES

• Agace W W, Amara A, Roberts A I, Pablos J L, Thelen S, Uguccioni M, Li X Y, Marsal J, Arenzana-Seisdedos F, Delaunay T, Ebert E C, Moser B, Parker C M. Constitutive expression of stromal derived factor-1 by mucosal epithelia and its role in HIV transmission and propagation. Curr Biol 2000; 10: 325–328
   PubMed Web of Science ®Google Scholar
• Agace W W, Roberts A I, Wu L, Greineder C, Ebert E C, Parker C M. Human intestinal lamina propria and intraepithelial lymphocytes express receptors specific for chemokines induced by inflammation. Eur J Immunol 2000; 30: 819–826
   PubMed Web of Science ®Google Scholar
• Ara T, Tokoyoda K, Okamoto R, Koni P A, Nagasawa T. The role of CXCL12 in the organ-specific process of artery formation. Blood 2005; 105: 3155–3161
   PubMed Web of Science ®Google Scholar
• Bargatze R F, Jutila M A, Butcher E C. Distinct roles of L-selectin and integrins alpha 4 beta 7 and LFA-1 in lymphocyte homing to Peyer's patch-HEV in situ: the multistep model confirmed and refined. Immunity 1995; 3: 99–108
   PubMed Web of Science ®Google Scholar
• Bleul C C, Fuhlbrigge R C, Casasnovas J M, Aiuti A, Springer T A. A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J Exp Med 1996; 184: 1101–1109
   PubMed Web of Science ®Google Scholar
• Briskin M, Winsor-Hines D, Shyjan A, Cochran N, Bloom S, Wilson J, McEvoy L M, Butcher E C, Kassam N, Mackay C R, Newman W, Ringler D J. Human mucosal addressin cell adhesion molecule-1 is preferentially expressed in intestinal tract and associated lymphoid tissue. Am J Pathol 1997; 151: 97–110
   PubMed Web of Science ®Google Scholar
• Campbell J J, Hedrick J, Zlotnik A, Siani M A, Thompson D A, Butcher E C. Chemokines and the arrest of lymphocytes rolling under flow conditions. Science 1998; 279: 381–384
   PubMed Web of Science ®Google Scholar
• Cook D N, Prosser D M, Forster R, Zhang J, Kuklin N A, Abbondanzo S J, Niu X D, Chen S C, Manfra D J, Wiekowski M T, Sullivan L M, Smith S R, Greenberg H B, Narula S K, Lipp M, Lira S A. CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity 2000; 12: 495–503
   PubMed Web of Science ®Google Scholar
• D'Apuzzo M, Rolink A, Loetscher M, Hoxie J A, Clark-Lewis I, Melchers F, Baggiolini M, Moser B. The chemokine SDF-1, stromal cell-derived factor 1, attracts early stage B cell precursors via the chemokine receptor CXCR4. Eur J Immunol 1997; 27: 1788–1793
   PubMed Web of Science ®Google Scholar
• Davies M D, Parrot D M. Preparation and purification of lymphocytes from the epithelium and lamina propria of murine small intestine. Gut 1981; 22: 481–488
   PubMed Web of Science ®Google Scholar
• Dieu M C, Vanbervliet B, Vicari A, Bridon J M, Oldham E, Ait-Yahia S, Briere F, Zlotnik A, Lebecque S, Caux C. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J Exp Med 1998; 188: 373–386
   PubMed Web of Science ®Google Scholar
• Dwinell M B, Lugering N, Eckmann L, Kagnoff M F. Regulated production of interferon-inducible T-cell chemoattractants by human intestinal epithelial cells. Gastroenterology 2001; 120: 49–59
   PubMed Web of Science ®Google Scholar
• Dwinell M B, Ogawa H, Barrett K E, Kagnoff M F. SDF-1/CXCL12 regulates cAMP production and ion transport in intestinal epithelial cells via CXCR4. Am J Physiol Gastrointest Liver Physiol 2004; 286: G844–G850
   Google Scholar
• Fitzhugh D J, Naik S, Caughman S W, Hwang S T. C-C chemokine receptor 6 is essential for arrest of a subset of memory T cells on activated dermal microvascular endothelial cells under physiologic flow conditions in vitro. J Immunol 2000; 165: 6677–6681
   PubMedGoogle Scholar
• Fujimori H, Miura S, Koseki S, Hokari R, Komoto S, Hara Y, Hachimura S, Kaminogawa S, Ishii H. Intravital observation of adhesion of lamina propria lymphocytes to microvessels of small intestine in mice. Gastroenterology 2002; 122: 734–744
   Google Scholar
• Grabovsky V, Feigelson S, Chen C, Bleijs D A, Peled A, Cinamon G, Baleux F, Arenzana-Seisdedos F, Lapidot T, van Kooyk Y, Lobb R R, Alon R. Subsecond induction of alpha4 integrin clustering by immobilized chemokines stimulates leukocyte tethering and rolling on endothelial vascular cell adhesion molecule 1 under flow conditions. J Exp Med 2000; 192: 495–506
   PubMed Web of Science ®Google Scholar
• Heidemann J, Ogawa H, Rafiee P, Lugering N, Maaser C, Domschke W, Binion D G, Dwinell M B. Mucosal angiogenesis regulation by CXCR4 and its ligand CXCL12 expressed by human intestinal microvascular endothelial cells. Am J Physiol Gastrointest Liver Physiol 2004; 286: G1059–G1068
   Google Scholar
• Hidalgo A, Sanz-Rodriguez F, Rodriguez-Fernandez J L, Albella B, Blaya C, Wright N, Cabanas C, Prosper F, Gutierrez-Ramos J C, Teixido J. Chemokine stromal cell-derived factor-1alpha modulates VLA-4 integrin-dependent adhesion to fibronectin and VCAM-1 on bone marrow hematopoietic progenitor cells. Exp Hematol 2001; 29: 345–355
   Google Scholar
• Hosoe N, Miura S, Watanabe C, Tsuzuki Y, Hokari R, Oyama T, Fujiyama Y, Nagata H, Ishii H. Demonstration of functional role of TECK/CCL25 in T lymphocyte-endothelium interaction in inflamed and uninflamed intestinal mucosa. Am J Physiol Gastrointest Liver Physiol 2004; 286: G458–G466
   PubMed Web of Science ®Google Scholar
• Iwasaki A, Kelsall B L. Localization of distinct Peyer's patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3alpha, MIP-3beta, and secondary lymphoid organ chemokine. J Exp Med 2000; 191: 1381–1394
   PubMed Web of Science ®Google Scholar
• Izadpanah A, Dwinell M B, Eckmann L, Varki N M, Kagnoff M F. Regulated MIP-3alpha/CCL20 production by human intestinal epithelium: mechanism for modulating mucosal immunity. Am J Physiol Gastrointest Liver Physiol 2001; 280: G710–G719
   PubMed Web of Science ®Google Scholar
• Katayama Y, Hidalgo A, Peired A, Frenette P S. Integrin alpha4beta7 and its counterreceptor MAdCAM-1 contribute to hematopoietic progenitor recruitment into bone marrow following transplantation. Blood 2004; 104: 2020–2026
   Google Scholar
• Kriehuber E, Breiteneder-Geleff S, Groeger M, Soleiman A, Schoppmann S F, Stingl G, Kerjaschki D, Maurer D. Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J Exp Med 2001; 194: 797–808
   PubMed Web of Science ®Google Scholar
• Kunkel E J, Campbell D J, Butcher E C. Chemokines in lymphocyte trafficking and intestinal immunity. Microcirculation 2003; 10: 313–323
   PubMed Web of Science ®Google Scholar
• Kunkel E J, Campbell J J, Haraldsen G, Pan J, Boisvert J, Roberts A I, Ebert E C, Vierra M A, Goodman S B, Genovese M C, Wardlaw A J, Greenberg H B, Parker C M, Butcher E C, Andrew D P, Agace W W. Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: Epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. J Exp Med 2000; 192: 761–768
   PubMed Web of Science ®Google Scholar
• Kwon J H, Keates S, Bassani L, Mayer L F, Keates A C. Colonic epithelial cells are a major site of macrophage inflammatory protein 3alpha (MIP-3alpha) production in normal colon and inflammatory bowel disease. Gut 2002; 51: 818–826
   PubMed Web of Science ®Google Scholar
• Liao F, Rabin R L, Smith C S, Sharma G, Nutman T B, Farber J M. CC-chemokine receptor 6 is expressed on diverse memory subsets of T cells and determines responsiveness to macrophage inflammatory protein 3 alpha. J Immunol 1999; 162: 186–194
   PubMed Web of Science ®Google Scholar
• Luster A D. Chemokines regulate lymphocyte homing to the intestinal mucosa. Gastroenterology 2001; 120: 291–294
   Google Scholar
• Miura S, Tsuzuki Y, Kurose I, Suematsu M, Shigematsu T, Kimura H, Higuchi H, Serizawa H, Yagita H, Okumura K, Granger D N, Ishii H. Endotoxin stimulates lymphocyte-endothelial interactions in rat intestinal Peyer's patches and villus mucosa. Am J Physiol 1996; 271: G282–G292
   Google Scholar
• Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, Kitamura Y, Yoshida N, Kikutani H, Kishimoto T. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 1996; 382: 635–638
   PubMed Web of Science ®Google Scholar
• Nanki T, Hayashida K, El-Gabalawy H S, Suson S, Shi K, Girschick H J, Yavuz S, Lipsky P E. Stromal cell-derived factor-1-CXC chemokine receptor 4 interactions play a central role in CD4+ T cell accumulation in rheumatoid arthritis synovium. J Immunol 2000; 165: 6590–6598
   PubMed Web of Science ®Google Scholar
• Papadakis K A, Prehn J, Moreno S T, Cheng L, Kouroumalis E A, Deem R, Breaverman T, Ponath P D, Andrew D P, Green P H, Hodge M R, Binder S W, Targan S R. CCR9-positive lymphocytes and thymus-expressed chemokine distinguish small bowel from colonic Crohn's disease. Gastroenterology 2001; 121: 246–254
   PubMed Web of Science ®Google Scholar
• Papadakis K A, Prehn J, Nelson V, Cheng L, Binder S W, Ponath P D, Andrew D P, Targan S R. The role of thymus-expressed chemokine and its receptor CCR9 on lymphocytes in the regional specialization of the mucosal immune system. J Immunol 2000; 165: 5069–5076
   PubMed Web of Science ®Google Scholar
• Peled A, Grabovsky V, Habler L, Sandbank J, Arenzana-Seisdedos F, Petit I, Ben-Hur H, Lapidot T, Alon R. The chemokine SDF-1 stimulates integrin-mediated arrest of CD34(+) cells on vascular endothelium under shear flow. J Clin Invest 1999; 104: 1199–1211
   PubMed Web of Science ®Google Scholar
• Sanz-Rodriguez F, Hidalgo A, Teixido J. Chemokine stromal cell-derived factor-1alpha modulates VLA-4 integrin-mediated multiple myeloma cell adhesion to CS-1/fibronectin and VCAM-1. Blood 2001; 97: 346–351
   PubMed Web of Science ®Google Scholar
• Sotnikov I, Hershkoviz R, Grabovsky V, Ilan N, Cahalon L, Vlodavsky I, Alon R, Lider O. Enzymatically quiescent heparanase augments T cell interactions with VCAM-1 and extracellular matrix components under versatile dynamic contexts. J Immunol 2004; 172: 5185–5193
   Google Scholar
• Tachibana K, Hirota S, Iizasa H, Yoshida H, Kawabata K, Kataoka Y, Kitamura Y, Matsushima K, Yoshida N, Nishikawa S, Kishimoto T, Nagasawa T. The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 1998; 393: 591–594
   PubMed Web of Science ®Google Scholar
• Tanaka Y, Imai T, Baba M, Ishikawa I, Uehira M, Nomiyama H, Yoshie O. Selective expression of liver and activation-regulated chemokine (LARC) in intestinal epithelium in mice and humans. Eur J Immunol 1999; 29: 633–642
   PubMedGoogle Scholar
• Teramoto K, Miura S, Tsuzuki Y, Hokari R, Watanabe C, Inamura T, Ogawa T, Hosoe N, Nagata H, Ishii H, Hibi T. Increased lymphocyte trafficking to colonic microvessels is dependent on MAdCAM-1 and C-C chemokine mLARC/CCL20 in DSS-induced mice colitis. Clin Exp Immunol 2005; 139: 421–428
   Google Scholar
• Uehara S, Grinberg A, Farber J M, Love P E. A role for CCR9 in T lymphocyte development and migration. J Immunol 2002; 168: 2811–2819
   PubMed Web of Science ®Google Scholar
• Watanabe C, Miura S, Hokari R, Teramoto K, Ogino T, Komoto S, Hara Y, Koseki S, Tsuzuki Y, Nagata H, Granger D N, Ishii H. Spatial heterogeneity of TNF-alpha-induced T cell migration to colonic mucosa is mediated by MAdCAM-1 and VCAM-1. Am J Physiol Gastrointest Liver Physiol 2002; 283: G1379–G1387
   Google Scholar
• Wright N, Hidalgo A, Rodriguez-Frade J M, Soriano S F, Mellado M, Parmo-Cabanas M, Briskin M J, Teixido J. The chemokine stromal cell-derived factor-1 alpha modulates alpha 4 beta 7 integrin-mediated lymphocyte adhesion to mucosal addressin cell adhesion molecule-1 and fibronectin. J Immunol 2002; 168: 5268–5277
   Google Scholar
• Wurbel M-A, Malissen M, Guy-Grand D, Meffre E, Nussenzweig M C, Richelme M, Carrier A, Malissen B. Mice lacking the CCR9 CC-chemokine receptor show a mild impairment of early T- and B-cell development and a reduction in T-cell receptor gammadelta(+) gut intraepithelial lymphocytes. Blood 2001; 98: 2626–2632
   PubMed Web of Science ®Google Scholar
• Yang S K, Eckmann L, Panja A, Kagnoff M F. Differential and regulated expression of C-X-C, C-C, and C-chemokines by human colon epithelial cells. Gastroenterology 1997; 113: 1214–1223
   PubMed Web of Science ®Google Scholar