Novel regulators of lymphocyte trafficking across high endothelial venules

Critical Reviews in Immunology

Volumn 31, Issue 2, 2011, Pages 147-169

  Umemoto, Eiji ^a,b   Hayasaka, Haruko ^a,b   Bai, Zhongbin ^a,b   Cai, Linjun ^a,b   Yonekura, Sari ^a,b   Peng, Xiaodong ^a,c   Takeda, Akira ^a,b   Tohya, Kazuo ^d   Miyasaka, Masayuki ^a,b  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c SICHUAN UNIVERSITY   (China)

^d KANSAI UNIVERSITY OF HEALTH SCIENCES   (Japan)

Author keywords

Adhesion molecule; Autotaxin; Chemokine; High endothelial venule; Lipid mediator; Lymphocyte traffcking; Nepmucin CD300g; Transendothelial migration (TEM)

Indexed keywords

AUTOTAXIN; CD300G; CELL ADHESION MOLECULE; CHEMOKINE; MEMBRANE PROTEIN; NEPMUCIN; UNCLASSIFIED DRUG;

ARTICLE; CELL INTERACTION; CELL MIGRATION; CELL MOTION; CELL TRANSPORT; EXTRAVASATION; HIGH ENDOTHELIAL VENULE; HOMEOSTASIS; HUMAN; IMMUNOPATHOLOGY; INTRACELLULAR TRANSPORT; LYMPHOCYTE; LYMPHOCYTE TRAFFICKING; LYMPHOID TISSUE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; SPLEEN; STRUCTURE ACTIVITY RELATION; TISSUE DISTRIBUTION; TRANSENDOTHELIAL MIGRATION; VENULE;

EID: 79955650645     PISSN: 10408401     EISSN: None     Source Type: Journal    
DOI: 10.1615/critrevimmunol.v31.i2.40     Document Type: Article

References (133)

1. von Andrian UH, Mempel TR. Homing and cellular traffc in lymph nodes. Nat Rev Immunol. 2003;3:867-78.
2. Miyasaka M, Tanaka T. Lymphocyte traffcking across high endothelial venules: dogmas and enigmas. Nat Rev Immunol. 2004;4:360-70.
3. Tanaka T, Ebisuno Y, Kanemitsu N, Umemoto E, Yang BG, Jang MH, Miyasaka M. Molecular determinants controlling homeostatic recirculation and tissue-specifc traffcking of lymphocytes. Int Arch Allergy Immunol. 2004;134:120-34.
4. Tohya K, Umemoto E, Miyasaka M. Microanatomy of lym-phocyte-endothelial interactions at the high endothelial venules of lymph nodes. Histol Histopathol. 2010;25:781-94.
5. Girard JP. Heterogeneity of endothelial cells: the specialized phenotype of human high endothelial venules characterized by suppression subtractive hybridization. Am J Pathol. 1999;155:2043-55.
6. Izawa D, Tanaka T, Saito K, Ogihara H, Usui T, Kawamoto S, Matsubara K, Okubo K, Miyasaka M. Expression pro-fle of active genes in mouse lymph node high endothelial cells. Int Immunol. 1999;11:1989-97.
7. Lacorre DA, Baekkevold ES, Garrido I, Brandtzaeg P, Hareldsen G, Amalric F, Girard JP. Plasticity of endothe-lial cells: rapid dedifferentiation of freshly isolated high endothelial venule endothelial cells outside the lymphoid tissue microenvironment. Blood 2004;103:4164-72.
8. Hayasaka H, Taniguchi K, Fukai S, Miyasaka M. Neo-genesis and development of the high endothelial venules that mediate lymphocyte traffcking. Cancer Sci. 2010;101:2302-8.
9. Miyasaka M, Trnka Z. Lymphocyte migration and differentiation in a large-animal model: the sheep. Immunol Rev. 1986;91:87-114.
10. Mora JR, Iwata M, von Andrian UH. Vitamin effects on the immune system: vitamins A and D take centre stage. Nature Rev Immunol. 2008;8:685-98.
11. Iwata M. Retinoic acid production by intestinal dendritic cells and its role in T-cell traffcking. Semin Immunol. 2009;21:8-13.
12. Marelli-Berg FM, Fu H, Vianello F, Tokoyoda K, Hamann A. Memory T-cell traffcking: new directions for busy commuters. Immunology. 2010;130:158-65.
13. Uchimura K, Rosen SD. Sulfated L-selectin ligands as a therapeutic target in chronic infammation. Trends Immunol. 2006;27:559-65.
14. Hemmerich S, Leffer H, Rosen SD. Structure of the O-glycans in GlyCAM-1, an endothelial-derived ligand for L-selectin. J Biol Chem. 1995;270:12035-47.
15. Mitsuoka C, Sawada-Kasugai M, Ando-Furui K, Izawa M, Nakanishi H, Nakamura S, Ishida H, Kiso M, Kannagi R. Identifcation of a major carbohydrate capping group of the L-selectin ligand on high endothelial venules in human lymph nodes as 6-sulfo sialyl Lewis X. J Biol Chem. 1998;273:11225-33.
16. Harris H. The stimulation of lymphocyte motility by cultured high endothelial cells and its inhibition by pertussis toxin. Int Immunol. 1991;3:535-42.
17. Harris H, Miyasaka M. Reversible stimulation of lymphocyte motility by cultured high endothelial cells: mediation by L-selectin. Immunology. 1995;84:47-54.
18. Zarbock A, Ley K. Mechanisms and consequences of neu-trophil interaction with the endothelium. Am J Pathol. 2008;172:1-7.
19. Arbones ML. Lymphocyte homing and leukocyte rolling and migration are impaired in L-selectin-defcient mice. Immunity. 1994;1:247-60.
20. Gauguet JM, Rosen SD, Marth JD, von Andrian UH. Core 2 branching beta1,6-N-acetylglucosaminyltransferase and high endothelial cell N-acetylglucosamine-6-sulfotransferase exert differential control over B- and T-lymphocyte homing to peripheral lymph nodes. Blood. 2004;104:4104-12.
21. Yang BG, Tanaka T, Jang MH, Bai Z, Hayasaka H, Miya-saka M. Binding of lymphoid chemokines to collagen IV that accumulates in the basal lamina of high endothelial venules: Its implications in lymphocyte traffcking. J Immunol. 2 2007;179:4376-82.
22. Nagakubo D, Murai T, Tanaka T, Usui T, Matsumoto M, Sekiguchi K, Miyasaka M. A high endothelial venule secretory protein mac25/angiomodulin, interacts with multiple high endothelial venule-associated molecules including chemokines. J Immunol. 2003;171:553-61.
23. Ebisuno Y, Tanaka T, Kanemitsu N, Kanda H, Yamagu-chi K, Kaisho T, Akira S, Miyasaka M. 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 traffcking across high endothelial venules. J Immunol. 2003;171:1642-6.
24. Okada T, Ngo VN, Ekland EH, Forster R, Lipp M, Litt-man DR, Cyster, JG. Chemokine requirements for B cell entry to lymph nodes and Peyer's patches. J Exp Med. 2002;196:65-75.
25. Kanemitsu N, Ebisuno Y, Tanaka T, Otani K, Haya-saka H, Kaisho T, Akira S, Katagiri K, Kinashi T, Fu-jita N, Tsuruo T, Miyasaka M. CXCL13 is an arrest chemokine for B cells in high endothelial venules. Blood. 2005;106:2613-8.
26. Bai ZB, Hayasaka H, Kobayashi M, Li WZ, Guo ZJ, Jang MH, Kondo A, Choi B, Iwakura Y, Miyasaka M. CXC chemokine ligand 12 promotes CCR7-dependent naive T cell traffcking to lymph nodes and Peyer's patches. J Immunol. 2009;182:1287-95.
27. Bao X, Moseman EA, Saito H, Petryanik B, Thiriot A, Hatakeyama S, Ito Y, Kawashima H, Yamaguchi Y, Lowe JB, von Andrian UH, Fukuda M. Endothelial heparan sulfate controls chemokine presentation in recruitment of lymphocytes and dendritic cells to lymph nodes. Immunity. 2011;33:817-29.
28. Kashiwazaki M, Tanaka T, Kanda H, Ebisuno Y, Izawa D, Fukuma N, Akimitsu N, Sekimizu K, Monden M, Miya-saka M. A high endothelial venule-expressing promiscuous chemokine receptor DARC can bind infammatory, but not lymphoid, chemokines and is dispensable for lymphocyte homing under physiological conditions. Int Immunol. 2003;15:1219-27.
29. Shulman Z, Shinder V, Klein E, Grabovsky V, Yeger O, Geron E, Montresor A, Bolomini-Vittori M, Feigelson SW, Kirchhausen T, Laudanna C, Shakhar G, Alon R. Lymphocyte Crawling and transendothelial migration require chemokine triggering of high-affnity LFA-1 integrin. Immunity. 2009;30:384-96.
30. Engelhardt B, Wolburg H. Mini-review: Transendothelial migration of leukocytes: through the front door or around the side of the house? Eur J Immunol. 2004;34:2955-63.
31. Vestweber D, Winderlich M, Cagna G, Nottebaum AF. Cell adhesion dynamics at endothelial junctions: VE-cadherin as a major player. Trends Cell Biol. 2009;19:8-15.
32. Marchesi VT, Gowans JL. The migration of lymphocytes through the endothelium of venules in lymph nodes: an electron microscope study. Proc R Soc Lond B Biol Sci. 1964;159:283-90.
33. Schoef GI. The migration of lymphocytes across the vascular endothelium in lymphoid tissue. a reexamination. J Exp Med. 1972;136:568-88.
34. Wenk EJ, Orlic D, Reith EJ, Rhodin JA. The ultrastructure of mouse lymph node venules and the passage of lymphocytes across their walls. J Ultrastruct Res. 1974;47:214-41.
35. Anderson AO, Anderson ND. Lymphocyte emigration from high endothelial venules in rat lymph nodes. Immunology. 1976;31:731-48.
36. Umetani Y. Postcapillary venule in rabbit tonsil and entry of lymphocytes into its endothelium: a scanning and transmission electron microscope study. Arch Histol Jpn. 1977;40:77-94.
37. Yamaguchi K, Schoef GI. Blood vessels of the Peyer's patch in the mouse: I. topographic studies. Anat Rec. 1983;206:391-401.
38. Yamaguchi K, Schoef GI. Blood vessels of the Peyer's patch in the mouse: II. in vivo observations. Anat Rec. 1983;206:403-17.
39. Yamaguchi K, Schoef GI. Blood vessels of the Peyer's patch in the mouse: III. high-endothelium venules. Anat Rec. 1983;206:419-38.
40. Nishi M, Hamada N, Nomura H, Mastueda M, Aiko T. The migration of lymphocytes across the vascular endothelium in lymph nodes: a scanning electron microscopic study. Lymphology. 1979;12:9-10.
41. Nieminen M, Hennttinen T, Merinen M, Marttila-Ichihara F, Eriksson JE, Jalkanen S. Vimentin function in lymphocyte adhesion and transcellular migration. Nat Cell Biol. 2006;8:156-62.
42. Carman CV, Sage PT, Sciuto TE, de la Fuente MA, Geha RS, Ochs HD, Dvorak HF, Dvorak AM, Springer TA. Tran-scellular diapedesis is initiated by invasive podosomes. Immunity. 2007;26:784-97.
43. Muller WA. Leukocyte-endothelial-cell interactions in leukocyte transmigration and the infammatory response. Trends Immunol. 2003;24:327-34.
44. Mamdouh Z, Chen X, Pierini LM, Maxfeld FR, Muller WA. Targeted recycling of PECAM from endothelial surface-connected compartments during diapedesis. Nature. 2003;421:748-53.
45. Mamdouh Z, Kreitzer GE, Muller WA. Leukocyte transmigration requires kinesin-mediated microtubule-dependent membrane traffcking from the lateral border recycling compartment. J Exp Med. 2008;205:951-66.
46. Mamdouh Z, Mikhailov A, Muller WA. Transcellu-lar migration of leukocytes is mediated by the endothe-lial lateral border recycling compartment. J Exp Med. 2009;206:2795-808.
47. Muller WA. Mechanisms of Leukocyte transendothelial migration. Annu Rev Pathol. 2010;6:323-44.
48. Seidman MA, Chew TW, Schenkel AR, Muller WA. PE-CAM-independent thioglycollate peritonitis is associated with a locus on murine chromosome 2. PLoS One. 2009;4:e4316.
49. Barreiro O. Dynamic interaction of VCAM-1 and ICAM-1 with moesin and ezrin in a novel endothelial docking structure for adherent leukocytes. J Cell Biol. 2002;157:1233-45.
50. Yang L, Froio RM, Sciuto TE, Dvorak AM, Alon R, Lus-cinskas FW. ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-α-activated vascular en-dothelium under fow. Blood. 2005;106:584-92.
51. Tamatani T, Miyasaka M. Identifcation of monoclonal antibodies reactive with the rat homolog of ICAM-1, and evidence for a differential involvement of ICAM-1 in the adherence of resting versus activated lymphocytes to high endothelial cells. Int Immunol. 1990;2:165-71.
52. Perry ME, Brown KA, von Gaudecker B. Ultrastructural identifcation and distribution of the adhesion molecules ICAM-1 and LFA-1 in the vascular and extravascular compartments of the human palatine tonsil. Cell Tissue Res. 1992;268:317-26.
53. Tohya K, Kimura M. Ultrastructural evidence of distinctive behavior of L-selectin and LFA-1 (αLβ2 integrin) on lymphocytes adhering to the endothelial surface of high endothelial venules in peripheral lymph nodes. Histochem Cell Biol. 1998;110:407-16.
54. Carman CV, Springer TA. A transmigratory cup in leukocyte diapedesis both through individual vascular endotheli-al cells and between them. J Cell Biol. 2004;167:377-88.
55. Carman C V, Springer TA. Trans-cellular migration: cell-cell contacts get intimate. Curr Opin Cell Biol. 2008;20:533-40.
56. Millan J, Hewlett L, Glyn M, Toomre D, Clark P, Ridley AJ. Lymphocyte transcellular migration occurs through recruitment of endothelial ICAM-1 to caveola- and F-actin-rich domains. Nat Cell Biol. 2006;8:113-23.
57. Imhof BA, Aurrand-Lions M. Adhesion mechanisms regulating the migration of monocytes. Nat Rev Immunol. 2004;4:432-44.
58. Pfeiffer F, Kumar V, Butz S, Vestweber D, Imhof BA, Stein J V, Engelhardt B. Distinct molecular composition of blood and lymphatic vascular endothelial cell junctions establishes specifc functional barriers within the peripheral lymph node. Eur J Immunol. 2008;38:2142-55.
59. Weber C, Fraemohs L, Dejana E. The role of junctional adhesion molecules in vascular infammation. Nat Rev Immunol. 2007;7:467-77.
60. Cera MR, Del Prete A, Vecchi A, Corada M, Martin-Padu-ra I, Motoike T, Tonetti P, Bazzoni G, Vermi W, Gentili F, Bernasconi S, Sato TN, Mantovani A, Dejana E. Increased DC traffcking to lymph nodes and contact hypersensitivi-ty in junctional adhesion molecule-A-defcient mice. J Clin Invest. 2004;114:729-38.
61. Wegmann F. ESAM supports neutrophil extravasation, activation of Rho, and VEGF-induced vascular permeability. J Exp Med. 2006;203:1671-7.
62. Ishida T, Kundu RK, Yang E, Hirata K, Ho YD, Querter-mous T. Targeted disruption of endothelial cell-selective adhesion molecule inhibits angiogenic processes in vitro and in vivo. J Biol Chem. 2003;278:34598-604.
63. Bazzoni G. Endothelial tight junctions: permeable barriers of the vessel wall. Thromb Haemost. 2006;95:36-42.
64. Dejana E. Endothelial cell-cell junctions: happy together. Nature Rev Mol Cell Biol. 2004;5:261-70.
65. Shaw SK, Bamba PS, Perkins BN, Luscinskas FW. Realtime imaging of vascular endothelial-cadherin during leukocyte transmigration across endothelium. J Immunol. 2001;167:2323-30.
66. Turowski P, Martinelli R, Crawford R, Wateridge D, Papa-georgiou AP, Lampugnani MG, Gamp AC, Vestweber D, Adamson P, Dejana E, Greenwood J. Phosphorylation of vascular endothelial cadherin controls lymphocyte emigration. J Cell Sci. 2008;121:29-37.
67. Allingham MJ, van Buul JD, Burridge K. ICAM-1-mediat-ed, Src- and Pyk2-dependent vascular endothelial cadherin tyrosine phosphorylation is required for leukocyte transen-dothelial migration. J Immunol. 2007;179:4053-64.
68. Taddei A, Giampietro C, Conti A, Orsenigo F, Breviario F, Pirazzoli V, Potente M, Daly C, Dimmeler S, Dejana E. Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5. Nat Cell Biol. 2008;10:923-34.
69. Umemoto E, Tanaka T, Kanda H, Jin S, Tohya K, Otani K, Matsutani T, Matsumoto M, Ebisuno Y, Jang MH, Fukuda M, Hirata T, Miyasaka M. Nepmucin, a novel HEV sia-lomucin, mediates L-selectin-dependent lymphocyte rolling and promotes lymphocyte adhesion under fow. J Exp Med. 2006;203:1603-14.
70. Clark GJ, Ju X, Azlan M, Tate C, Ding Y, Hart DN. The CD300 molecules regulate monocyte and dendritic cell functions. Immunobiol. 2009;214:730-6.
71. Takatsu H, Hase K, Ohmae M, Ohshima S, Hashimoto K, Taniura N, Yamamoto A, Ohno H. CD300 antigen like family member G: A novel Ig receptor like protein exclusively expressed on capillary endothelium. Biochem Bio-phys Res Commun. 2006;348:183-91.
72. Jin S, Umemoto E, Tanaka T, Shimomura Y, Tohya K, Kunizawa K, Yang BG, Jang MH, Hirata T, Miyasaka M. Nepmucin/CLM-9, an Ig domain-containing sialomucin in vascular endothelial cells, promotes lymphocyte transend-othelial migration in vitro. FEBS Lett. 2008;582:3018-24.
73. Nourshargh S, Krombach F, Dejana E. The role of JAM-A and PECAM-1 in modulating leukocyte infltration in in-famed and ischemic tissues. J Leukoc Biol. 2006;80:714-8.
74. Nourshargh S, Marelli-Berg FM. Transmigration through venular walls: a key regulator of leukocyte phenotype and function. Trends Immunol. 2005;26:157-65.
75. Daro E, van der Sluijs P, Galli T, Mellman I. Rab4 and cellubrevin defne different early endosome populations on the pathway of transferrin receptor recycling. Proc Natl Acad Scie U S A. 1996;93:9559-64.
76. Humphries IV WH, Fay NC, Payne CK. Intracellular degradation of low-density lipoprotein probed with two-color fuorescence microscopy. Integr Biol. 2010;2:536-44.
77. Shaw SK. Coordinated redistribution of leukocyte LFA-1 and endothelial cell ICAM-1 accompany neutrophil transmigration. J Exp Med. 2004;200:1571-80.
78. Dejana E. The transcellular railway: insights into leukocyte diapedesis. Nat Cell Biol. 2006;8:105-7.
79. Keuschnigg J, Henttinen T, Auvinen K, Karikoski M, Salmi M, Jalkanen S. The prototype endothelial marker PAL-E is a leukocyte traffcking molecule. Blood. 2009;114:478-84.
80. Muller WA. Mechanisms of transendothelial migration of leukocytes. Circ Res. 2009;105:223-30.
81. Miyanishi M, Tada K, Koike M, Uchiyama Y, Kitamura T, Nagata S. Identifcation of Tim4 as a phosphatidylserine receptor. Nature. 2007;450:435-9.
82. Kanda H, Newton R, Klein R, Morita Y, Gunn MD, Rosen SD. Autotaxin, an ectoenzyme that produces lysophospha-tidic acid, promotes the entry of lymphocytes into secondary lymphoid organs. Nat Immunol. 2008;9:415-23.
83. Nakasaki T, Tanaka T, Okudaira S, Hirosawa M, Umemoto E, Otani K, Jin S, Bai Z, Hayasaka H, Fukui Y, Aozasa K, Fujita N, Tsuruo T, Ozono K, Aoki J, Miyasaka M. Involvement of the lysophosphatidic scid-generating enzyme autotaxin in lymphocyte-endothelial cell interactions. Am J Pathol. 2008;173:1566-76.
84. van Meeteren LA, Moolenaar WH. Regulation and biological activities of the autotaxin-LPA axis. Prog Lipid Res. 2007;46:145-60.
85. Jansen S, Stefan C, Creemers JW, Waelkens E, Van Eynde A, Stalmans W, Bollen M. Proteolytic maturation and activation of autotaxin (NPP2), a secreted metastasis-enhancing lysophospholipase D. J Cell Sci. 2005;118:3081-9.
86. Koike S, Keino-Masu K, Ohto T, Masu M. The N-terminal hydrophobic sequence of autotaxin (ENPP2) functions as a signal peptide. Genes Cells. 2006;11:133-42.
87. Tokumura A, Majima E, Kariya Y, Tominaga K, Kogure K, Yasuda K, Fukuzawa K. Identifcation of human plasma lysophospholipase D, a lysophosphatidic acid-producing enzyme, as autotaxin, a multifunctional phosphodiesterase. J Biol Chem. 2002;277:39436-42.
88. Umezu-Goto M, Kishi Y, Taira A, Hama K, Dohmae N, Takio K, Yamori T, Mills GB, Inoue K, Aoki J, Arai H. Au-totaxin has lysophospholipase D activity leading to tumor cell growth and motility by lysophosphatidic acid production. J Cell Biol. 2002;158:227-33.
89. Ferry G, Giganti A, Coge F, Bertaux F, Thiam K, Boutin JA. Functional invalidation of the autotaxin gene by a single amino acid mutation in mouse is lethal. FEBS Lett. 2007;581:3572-8.
90. Stefan C, Jansen S, Bollen M. NPP-type ectophospho-diesterases: unity in diversity. Trends Biochem Sci. 2005;30:542-50.
91. Hausmann J, Kamtekar S, Christodouloou F, Day JE, Wu T, Fulkerson Z, Albers HMHG, van Meeteren LA, Houben AJS, van Zeijl L, Jansen S, Andries M, Hall T, Pegg LE, Benson TE, Kaseim M, Harlos K, Kooi CWV, Smyth SS, Ovaa H, Bollen M, Morris AJ, Moolenaar WH, Perrakis A. Structural basis of substrate discrimination and integrin binding by autotaxin. Nature Struct Mol Biol. 2011 Jan 16. [Epub ahead of print].
92. Nishimasu H, Okudaira S, Hama K, Mihara E, Dohmae N, Inoue A, Ishitani R, Takagi J, Aoki J, Nureki O. Crystal structure of autotaxin and insight into GPCR activation by lipid mediators. Nature Struct Mol Biol. 2011 Jan 16. [Epub ahead of print].
93. Clair T, Aoki J, Koh E, Bandle RW, Nam SW, Ptaszynska MM, Mills GB, Schiffmann E, Liotta LA, Stracke ML. Au-totaxin hydrolyzes sphingosylphosphorylcholine to produce the regulator of migration, sphingosine-1-phosphate. Cancer Res. 2003;63:5446-53.
94. Liliom K, Sun G, Bunemann M, Virag T, Nusser N, Baker DL, Wang DA, Fabian MJ, Brandts B, Bender K, Eickel A, Malik KU, Miller DD, Desiderio DM, Tigyi G, Pott L. Sphingosylphosphocholine is a naturally occurring lipid mediator in blood plasma: a possible role in regulating cardiac function via sphingolipid receptors. Biochem J. 2001;355:189-97.
95. Tanaka M, Okudaira S, Kishi Y, Ohkawa R, Iseki S, Ota M, Noji S, Yatomi Y, Aoki J, Arai H. Autotaxin stabilizes blood vessels and is required for embryonic vascula- ture by producing lysophosphatidic acid. J Biol Chem. 2006;281:25822-30.
96. Tsuda S, Okudaira S, Moriya-Ito K, Shimamoto C, Tanaka M, Aoki J, Arai H, Murakami-Murofushi K, Kobayashi T. Cyclic phosphatidic acid is produced by autotaxin in blood. J Biol Chem. 2006;281:26081-8.
97. Mizugishi K, Yamashita T, Olivera A, Miller GF, Spiegel S, Proia RL. Essential role for sphingosine kinases in neural and vascular development. Mol Cell Biol. 2005;25:11113-21.
98. Mills GB, Moolenaar WH. The emerging role of lysophos-phatidic acid in cancer. Nat Rev Cancer. 2003;3:582-91.
99. Okudaira S, Yukiura H, Aoki J. Biological roles of lyso-phosphatidic acid signaling through its production by au-totaxin. Biochimie. 2010;92:698-706.
100. Hosogaya S, Yatomi Y, Nakamura K, Ohkawa R, Okubo S, Yokota H, Ohta M, Yamazaki H, Koike T, Ozaki Y. Measurement of plasma lysophosphatidic acid concentration in healthy subjects: strong correlation with lysophospholi-pase D activity. Ann Clin Biochem. 2008;45:364-8.
101. Brindley DN, Pilquil C. Lipid phosphate phosphatases and signaling. J Lipid Res. 2009;50 Suppl:S225-30.
102. Albers HM, Dong A, van Meeteren LA, Egan DA, Sunk-ara M, van Tilburg EW, Schuurman K, van Tellingen O, Morris AJ, Smyth SS, Moolenaar WH, Ovaa H. Boronic acid-based inhibitor of autotaxin reveals rapid turnover of LPA in the circulation. Proc Natl Acad Sci U S A. 2010;107:7257-62.
103. Ishii S, Noguchi K, Yanagida K. Non-Edg family lyso-phosphatidic acid (LPA) receptors. Prostaglandins Other Lipid Mediat. 2009;89:57-65.
104. Tigyi G. Aiming drug discovery at lysophosphatidic acid targets. Br J Pharmacol. 2010;161:241-70.
105. Nakanaga K, Hama K, Aoki J. Autotaxin - an LPA producing enzyme with diverse functions. J Biochem. 2010;148:13-24.
106. Ruppel KM, Willison D, Kataoka H, Wang A, Zheng YW, Cornelissen I, Yin L, Xu SM, Coughlin SR. Essential role for Gα13 in endothelial cells during embryonic development. Proc Natl Acad Sci U S A. 2005;102:8281-6.
107. Sumida H, Noguchi K, Kihara Y, Abe M, Yanagida K, Ha-mano F, Sato S, Tamaki K, Morishita Y, Kano MR, Iwata C, Miyazono K, Sakimura K, Shimizu T, Ishii S. LPA4 regulates blood and lymphatic vessel formation during mouse embryogenesis. Blood. 2010;116:5060-70.
108. Yanagida K, Masago K, Nakanishi H, Kihara Y, Hamano F, Tajima Y, Taguchi R, Shimizu T, Ishii S. Identifcation and characterization of a novel lysophosphatidic acid receptor, p2y5/LPA6. J Biol Chem. 2009;284:17731-41.
109. Rizza C, Leitinger N, Yue J, Fischer DJ, Wang DA, Shih PT, Lee H, Tigyi G, Berliner JA. Lysophosphatidic acid as a regulator of endothelial/leukocyte interaction. Lab Invest. 1999;79:1227-35.
110. van Nieuw Amerongen GP, Vermeer MA, van Hinsbergh VW. Role of RhoA and Rho kinase in lysophosphatidic acid-induced endothelial barrier dysfunction. Arterioscler Thromb Vasc Biol. 2000;20:E127-33.
111. Baker DL, Fujiwara Y, Pigg KR, Tsukahara R, Kobayashi S, Murofushi H, Uchiyama A, Murakami-Murofushi K, Koh E, Bandle RW, Byun HS, Bittman R, Fan D, Murph M, Mills GB, Tigyi G. Carba analogs of cyclic phosphatidic acid are selective inhibitors of autotaxin and cancer cell invasion and metastasis. J Biol Chem. 2006;281:22786-93.
112. Xu X, Prestwich GD. Inhibition of tumor growth and an-giogenesis by a lysophosphatidic acid antagonist in an engineered three-dimensional lung cancer xenograft model. Cancer. 2010;116:1739-50.
113. Vestweber D, Wild MK. A new player in lymphocyte homing. Nat Immunol. 2008;9:347-8.
114. Wu JM, Xu Y, Skill NJ, Sheng H, Zhao Z, Yu M, Saxena R, Maluccio MA. Autotaxin expression and its connection with the TNF-α-NF-κB axis in human hepatocellular carcinoma. Mol Cancer. 2010;9:71-85.
115. Drayton DL, Bonizzi G, Ying X, Liao S, Karin M, Ruddle NH. IκB kinase complex α kinase activity controls chemokine and high endothelial venule gene expression in lymph nodes and nasal-associated lymphoid tissue. J Immunol. 2004;173:6161-8.
116. Drayton DL, Liao S, Mounzer RH, Ruddle NH. Lymphoid organ development: from ontogeny to neogenesis. Nat Immunol. 2006;7:344-53.
117. Huber C, Thielen C, Seeger H, Schwarz P, Montrasio F, Wilson MR, Heinen E, Fu YX, Miele G, Aguzzi A. Lymphotoxin-β receptor-dependent genes in lymph node and follicular dendritic cell transcriptomes. J Immunol. 2005;174:5526-36.
118. Browning JL. Lymphotoxin-β receptor signaling is required for the homeostatic control of HEV differentiation and function. Immunity. 2005;23:539-50.
119. van Meeteren LA, Ruurs P, Christodoulou E, Goding JW, Takakusa H, Kikuchi K, Perrakis A, Nagano T, Moolenaar WH. Inhibition of autotaxin by lysophosphatidic acid and sphingosine 1-phosphate. J Biol Chem. 2005:21155-61.
120. Leppert D, Waubant E, Galardy R, Bunnett NW, Hauser SL. T cell gelatinases mediate basement membrane transmigration in vitro. J Immunol. 1995;154:4379-89.
121. Faveeuw C, Preece G, Ager A. Transendothelial migration of lymphocytes across high endothelial venules into lymph nodes is affected by metalloproteinases. Blood. 2001;98:688-95.
122. Bajenoff M, Egen JG, Koo LY, Laugier JP, Brau F, Gla-ichenhaus N, Germain RN. Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity. 2006;25:989-1001.
123. Ohtani O, Kikuta A, Ohtsuka A, Murakami T. Organization of the reticular network of rabbit Peyer's patches. Anat Rec. 1991;229:251-8.
124. Wang S, Voisin MB, Larbi KY, Dangerfeld J, Scheiermann C, Tran M, Maxwell PH, Sorokin L, Nourshargh S. Venu-lar basement membranes contain specifc matrix protein low expression regions that act as exit points for emigrating neutrophils. J Exp Med. 2006;203:1519-32.
125. Poznansky MC, Olszak IT, Foxall R, Evans RH, Luster AD, Scadden DT. Active movement of T cells away from a chemokine. Nat Med. 2000;6:543-8.
126. Lämmermann T, Bader BL, Monkley SJ, Worbs T, Wedlich-Soldner R, Hirsch K, Keller M, Forster R, Critchley DR, Fassler R, Sixt M. Rapid leukocyte migration by integrin-in-dependent fowing and squeezing. Nature. 2008;453:51-5.
127. Schumann K, Lämmermann T, Bruckner M, Legler DF, Polleux J, Spatz JP, Schuler G, Förster R, Lutz MB, So-rokin L, Sixt M. Immobilized chemokine felds and soluble chemokine gradients cooperatively shape migration patterns of cendritic cells. Immunity. 2010;32:703-13.
128. Baekkevold ES, Yamanaka T, Palframan RT, Carlsen HS, Reinholt FP, Von Andrian UH, Brandtzaeg P, Haraldsen G. The CCR7 ligand ELC (CCL19) is transcytosed in high endothelial venules and mediates T cell recruitment. J Exp Med. 2001;193:1105-12.
129. Gretz JE, Anderson AO, Shaw S. Cords, channels, corridors and conduits: critical architectural elements facilitating cell interactions in the lymph node cortex. Immunol Rev. 1997;156:11-24.
130. Gretz JE, Norbury CC, Anderson AO, Proudfoot AE, Shaw S. Lymph-borne chemokines and other low molecular weight molecules reach high endothelial venules via specialized conduits while a functional barrier limits access to the lymphocyte microenvironments in lymph node cortex. J Exp Med. 2000;192:1425-40.
131. Lindquist RL, Shakhar G, Dudziak D, Wardemann H, Eisenreich T, Dustin ML, Nussenzweig MC. Visualizing dendritic cell networks in vivo. Nat Immunol. 2004;5:1243-50.
132. Takedachi M, Qu D, Ebisuno Y, Oohara H, Joachims ML, McGee ST, Maeda E, McEver RP, Tanaka T, Miyasaka M, Murakami S, Krahn T, Blackburn MR, Thompson LF. CD73-generated adenosine restricts lymphocyte migration into draining lymph nodes. J Immunol. 2008;180:6288-96.
133. Thompson LF, Takedachi M, Ebisuno Y, Tanaka T, Mi-yasaka M, Mills JH, Bynoe MS. Regulation of leukocyte migration across endothelial barriers by ECTO-5'-nucle-otidase-generated adenosine. Nucleosides Nucleotides Nucleic Acids. 2008;27:755-60.