Finding their niche: Chemokines directing cell migration in the thymus

Immunology and Cell Biology

Volumn 89, Issue 2, 2011, Pages 185-196

  Bunting, Mark D ^a   Comerford, Iain ^a   McColl, Shaun R ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

cell migration; chemokine; chemokine receptor; thymus

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCR8; CHEMOKINE RECEPTOR CXCR4; CXCL1 CHEMOKINE; CXCL11 CHEMOKINE; CXCL16 CHEMOKINE; CXCL2 CHEMOKINE; CXCL9 CHEMOKINE; EOTAXIN; FRACTALKINE; G PROTEIN COUPLED RECEPTOR; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HERMES ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA; MACROPHAGE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MONOCYTE CHEMOTACTIC PROTEIN 2; MONOCYTE CHEMOTACTIC PROTEIN 3; MONOCYTE CHEMOTACTIC PROTEIN 5; PERTUSSIS TOXIN; RANTES; SECONDARY LYMPHOID TISSUE CHEMOKINE; STEM CELL FACTOR RECEPTOR; T LYMPHOCYTE RECEPTOR; THYMUS AND ACTIVATION REGULATED CHEMOKINE; UNINDEXED DRUG;

ARTICLE; BRAIN CORTEX; CELL MIGRATION; CELL SELECTION; HUMAN; IN SITU HYBRIDIZATION; MEDULLA OBLONGATA; NATURAL KILLER T CELL; NONHUMAN; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THYMOCYTE; THYMUS; THYMUS FUNCTION;

ANIMALS; CELL MOVEMENT; CHEMOKINES; HUMANS; RECEPTORS, CHEMOKINE; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; THYMUS GLAND;

EID: 79951874005     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2010.142     Document Type: Article

References (129)

1. Petrie HT, Zuniga-Pflucker JC. Zoned out: functional mapping of stromal signaling microenvironments in the thymus. Annu Rev Immunol 2007; 25: 649-679. (Pubitemid 46697920)
2. Mori K, Itoi M, Tsukamoto N, Kubo H, Amagai T. The perivascular space as a path of hematopoietic progenitor cells and mature T cells between the blood circulation and the thymic parenchyma. Int Immunol 2007; 19: 745-753. (Pubitemid 47073264)
3. Lind EF, Prockop SE, Porritt HE, Petrie HT. Mapping precursor movement through the postnatal thymus reveals specific microenvironments supporting defined stages of early lymphoid development. J Exp Med 2001; 194: 127-134. (Pubitemid 32673345)
4. Anderson G, Jenkinson WE, Jones T, Parnell SM, Kinsella FA, White AJ et al. Establishment and functioning of intrathymic microenvironments. Immunol Rev 2006; 209: 10-27.
5. Godfrey DI, Kennedy J, Suda T, Zlotnik A. A developmental pathway involving four phenotypically and functionally distinct subsets of CD3-CD4-CD8- triple-negative adult mouse thymocytes defined by CD44 and CD25 expression. J Immunol 1993; 150: 4244-4252. (Pubitemid 23133699)
6. Godfrey DI, Kennedy J, Mombaerts P, Tonegawa S, Zlotnik A. Onset of TCR-beta gene rearrangement and role of TCR-beta expression during CD3-CD4-CD8- thymocyte differentiation. J Immunol 1994; 152: 4783-4792.
7. von Boehmer H, Fehling HJ. Structure and function of the pre-T cell receptor. Annu Rev Immunol 1997; 15: 433-452. (Pubitemid 27169288)
8. von Boehmer H. Unique features of the pre-T-cell receptor alpha-chain: not just a surrogate. Nat Rev Immunol 2005; 5: 571-577.
9. Porritt HE, Gordon K, Petrie HT. Kinetics of steady-state differentiation and mapping of intrathymic-signaling environments by stem cell transplantation in nonirradiated mice. J Exp Med 2003; 198: 957-962. (Pubitemid 37152932)
10. Petrie HT. Cell migration and the control of post-natal T-cell lymphopoiesis in the thymus. Nat Rev Immunol 2003; 3: 859-866. (Pubitemid 37411715)
11. Takahama Y. Journey through the thymus: stromal guides for T-cell development and selection. Nat Rev Immunol 2006; 6: 127-135. (Pubitemid 43361588)
12. Klein L, Hinterberger M, Wirnsberger G, Kyewski B. Antigen presentation in the thymus for positive selection and central tolerance induction. Nat Rev Immunol 2009; 9: 833-844.
13. Ehrlich LI, Oh DY, Weissman IL, Lewis RS. Differential contribution of chemotaxis and substrate restriction to segregation of immature and mature thymocytes. Immunity 2009; 31: 986-998.
14. Gale LM, McColl SR. Chemokines: extracellular messengers for all occasions? Bioessays 1999; 21: 17-28.
15. Sallusto F, Mackay CR. Chemoattractants and their receptors in homeostasis and inflammation. Curr Opin Immunol 2004; 16: 724-731. (Pubitemid 39423660)
16. Misslitz A, Bernhardt G, Forster R. Trafficking on serpentines: molecular insight on how maturating T cells find their winding paths in the thymus. Immunol Rev 2006; 209: 115-128.
17. Vianello F, Olszak IT, Poznansky MC. Fugetaxis: active movement of leukocytes away from a chemokinetic agent. J Mol Med 2005; 83: 752-763. (Pubitemid 41407859)
18. Alves NL, Richard-Le Goff O, Huntington ND, Sousa AP, Ribeiro VS, Bordack A et al. Characterization of the thymic IL-7 niche in vivo. Proc Natl Acad Sci USA 2009; 106: 1512-1517.
19. Jenkinson WE, Rossi SW, Parnell SM, Agace WW, Takahama Y, Jenkinson EJ et al. Chemokine receptor expression defines heterogeneity in the earliest thymic migrants. Eur J Immunol 2007; 37: 2090-2096. (Pubitemid 47250201)
20. Bleul CC, Boehm T. Chemokines define distinct microenvironments in the developing thymus. Eur J Immunol 2000; 30: 3371-3379. (Pubitemid 32005207)
21. Liu C, Saito F, Liu Z, Lei Y, Uehara S, Love P et al. Coordination between CCR7- and CCR9-mediated chemokine signals in prevascular fetal thymus colonization. Blood 2006; 108: 2531-2539.
22. Wilkinson B, Owen JJ, Jenkinson EJ. Factors regulating stem cell recruitment to the fetal thymus. J Immunol 1999; 162: 3873-3881. (Pubitemid 29314765)
23. Liu C, Ueno T, Kuse S, Saito F, Nitta T, Piali L et al. The role of CCL21 in recruitment of T-precursor cells to fetal thymi. Blood 2005; 105: 31-39. (Pubitemid 40053060)
24. Vicari AP, Figueroa DJ, Hedrick JA, Foster JS, Singh KP, Menon S et al. TECK: a novel CC chemokine specifically expressed by thymic dendritic cells and potentially involved in T cell development. Immunity 1997; 7: 291-301. (Pubitemid 27392020)
25. Plotkin J, Prockop SE, Lepique A, Petrie HT. Critical role for CXCR4 signaling in progenitor localization and T cell differentiation in the postnatal thymus. J Immunol 2003; 171: 4521-4527. (Pubitemid 37310567)
26. Trampont PC, Tosello-Trampont AC, Shen Y, Duley AK, Sutherland AE, Bender TP et al. CXCR4 acts as a costimulator during thymic beta-selection. Nat Immunol 2010; 11: 162-170.
27. Schabath R, Muller G, Schubel A, Kremmer E, Lipp M, Forster R. The murine chemokine receptor CXCR4 is tightly regulated during T cell development and activation. J Leukoc Biol 1999; 66: 996-1004. (Pubitemid 30010526)
28. Suzuki G, Sawa H, Kobayashi Y, Nakata Y, Nakagawa K, Uzawa A et al. Pertussis toxin-sensitive signal controls the trafficking of thymocytes across the corticomedullary junction in the thymus. J Immunol 1999; 162: 5981-5985. (Pubitemid 29314954)
29. Fu WX, Gong SY, Qian XP, Li Y, Zhu ML, Dong XY et al. Differential chemotactic potential of mouse platelet basic protein for thymocyte subsets. Cell Mol Life Sci 2004; 61: 1935-1945. (Pubitemid 39094800)
30. Germanov E, Veinotte L, Cullen R, Chamberlain E, Butcher EC, Johnston B. Critical role for the chemokine receptor CXCR6 in homeostasis and activation of CD1d-restricted NKT cells. J Immunol 2008; 181: 81-91.
31. Matloubian M, David A, Engel S, Ryan JE, Cyster JG. A transmembrane CXC chemokine is a ligand for HIV-coreceptor Bonzo. Nat Immunol 2000; 1: 298-304.
32. Baba T, Nakamoto Y, Mukaida N. Crucial contribution of thymic Sirp alpha+ conventional dendritic cells to central tolerance against blood-borne antigens in a CCR2-dependent manner. J Immunol 2009; 183: 3053-3063.
33. Laan M, Kisand K, Kont V, Moll K, Tserel L, Scott HS et al. Autoimmune regulator deficiency results in decreased expression of CCR4 and CCR7 ligands and in delayed migration of CD4+ thymocytes. J Immunol 2009; 183: 7682-7691.
34. Ueno T, Saito F, Gray DH, Kuse S, Hieshima K, Nakano H et al. CCR7 signals are essential for cortex-medulla migration of developing thymocytes. J Exp Med 2004; 200: 493-505. (Pubitemid 39121906)
35. Uehara S, Song K, Farber JM, Love PE. Characterization of CCR9 expression and CCL25/thymus-expressed chemokine responsiveness during T cell development: CD3(high)CD69+ thymocytes and gammadeltaTCR+ thymocytes preferentially respond to CCL25. J Immunol 2002; 168: 134-142. (Pubitemid 34014112)
36. Wurbel MA, Philippe JM, Nguyen C, Victorero G, Freeman T, Wooding P et al. The chemokine TECK is expressed by thymic and intestinal epithelial cells and attracts double- and single-positive thymocytes expressing the TECK receptor CCR9. Eur J Immunol 2000; 30: 262-271. (Pubitemid 30011788)
37. Alferink J, Lieberam I, Reindl W, Behrens A, Weiss S, Huser N et al. Compartmentalized production of CCL17 in vivo: strong inducibility in peripheral dendritic cells contrasts selective absence from the spleen. J Exp Med 2003; 197: 585-599. (Pubitemid 36314654)
38. Wurbel MA, Malissen B, Campbell JJ. Complex regulation of CCR9 at multiple discrete stages of T cell development. Eur J Immunol 2006; 36: 73-81. (Pubitemid 43116394)
39. Campbell JJ, Pan J, Butcher EC. Cutting edge: developmental switches in chemokine responses during T cell maturation. J Immunol 1999; 163: 2353-2357. (Pubitemid 29399149)
40. Drennan MB, Franki AS, Dewint P, Van Beneden K, Seeuws S, van de Pavert SA et al. Cutting edge: the chemokine receptor CXCR3 retains invariant NK T cells in the thymus. J Immunol 2009; 183: 2213-2216.
41. Kim CH, Pelus LM, White JR, Broxmeyer HE. Differential chemotactic behavior of developing T cells in response to thymic chemokines. Blood 1998; 91: 4434-4443. (Pubitemid 28270288)
42. Proietto AI, Lahoud MH, Wu L. Distinct functional capacities of mouse thymic and splenic dendritic cell populations. Immunol Cell Biol 2008; 86: 700-708.
43. Carramolino L, Zaballos A, Kremer L, Villares R, Martin P, Ardavin C et al. Expression of CCR9 beta-chemokine receptor is modulated in thymocyte differentiation and is selectively maintained in CD8(+) T cells from secondary lymphoid organs. Blood 2001; 97: 850-857. (Pubitemid 32154264)
44. Franz-Bacon K, Dairaghi DJ, Boehme SA, Sullivan SK, Schall TJ, Conlon PJ et al. Human thymocytes express CCR-3 and are activated by eotaxin. Blood 1999; 93: 3233-3240. (Pubitemid 29220889)
45. Tanabe S, Lu Z, Luo Y, Quackenbush EJ, Berman MA, Collins-Racie LA et al. Identification of a new mouse beta-chemokine, thymus-derived chemotactic agent 4, with activity on T lymphocytes and mesangial cells. J Immunol 1997; 159: 5671-5679. (Pubitemid 127470098)
46. Romagnani P, Annunziato F, Lazzeri E, Cosmi L, Beltrame C, Lasagni L et al. Interferon-inducible protein 10, monokine induced by interferon gamma, and interferon-inducible T-cell alpha chemoattractant are produced by thymic epithelial cells and attract T-cell receptor (TCR) alphabeta+ CD8+ single-positive T cells, TCRgammadelta+ T cells, and natural killer-type cells in human thymus. Blood 2001; 97: 601-607. (Pubitemid 32114160)
47. Annunziato F, Romagnani P, Cosmi L, Beltrame C, Steiner BH, Lazzeri E et al. Macrophage-derived chemokine and EBI1-ligand chemokine attract human thymocytes in different stage of development and are produced by distinct subsets of medullary epithelial cells: possible implications for negative selection. J Immunol 2000; 165: 238-246. (Pubitemid 30429512)
48. Chantry D, Romagnani P, Raport CJ, Wood CL, Epp A, Romagnani S et al. Macrophage-derived chemokine is localized to thymic medullary epithelial cells and is a chemoattractant for CD3(+), CD4(+), CD8(low) thymocytes. Blood 1999; 94: 1890-1898. (Pubitemid 29430404)
49. Lieberam I, Forster I. The murine beta-chemokine TARC is expressed by subsets of dendritic cells and attracts primed CD4+ T cells. Eur J Immunol 1999; 29: 2684-2694. (Pubitemid 30098993)
50. Norment AM, Bogatzki LY, Gantner BN, Bevan MJ. Murine CCR9, a chemokine receptor for thymus-expressed chemokine that is up-regulated following pre-TCR signaling. J Immunol 2000; 164: 639-648. (Pubitemid 30043683)
51. Rothenberg ME, Luster AD, Leder P. Murine eotaxin: an eosinophil chemoattractant inducible in endothelial cells and in interleukin 4-induced tumor suppression. Proc Natl Acad Sci USA 1995; 92: 8960-8964.
52. Uehara S, Hayes SM, Li L, El-Khoury D, Canelles M, Fowlkes BJ et al. Premature expression of chemokine receptor CCR9 impairs Tcell development. J Immunol 2006; 176: 75-84. (Pubitemid 43023251)
53. Ueno T, Hara K, Willis MS, Malin MA, Hopken UE, Gray DH et al. Role for CCR7 ligands in the emigration of newly generated T lymphocytes from the neonatal thymus. Immunity 2002; 16: 205-218. (Pubitemid 34211961)
54. Misslitz A, Pabst O, Hintzen G, Ohl L, Kremmer E, Petrie HT et al. Thymic T cell development and progenitor localization depend on CCR7. J Exp Med 2004; 200: 481-491. (Pubitemid 39121905)
55. Ladi E, Schwickert TA, Chtanova T, Chen Y, Herzmark P, Yin X et al. Thymocyte-dendritic cell interactions near sources of CCR7 ligands in the thymic cortex. J Immunol 2008; 181: 7014-7023.
56. Gray DH, Tull D, Ueno T, Seach N, Classon BJ, Chidgey A et al. A unique thymic fibroblast population revealed by the monoclonal antibody MTS-15. J Immunol 2007; 178: 4956-4965. (Pubitemid 46595278)
57. Chaffin KE, Perlmutter RM. A pertussis toxin-sensitive process controls thymocyte emigration. Eur J Immunol 1991; 21: 2565-2573.
58. Person PL, Korngold R, Teuscher C. Pertussis toxin-induced lymphocytosis is associated with alterations in thymocyte subpopulations. J Immunol 1992; 148: 1506-1511.
59. Jin Y, Wu MX. Requirement of Galphai in thymic homing and early T cell development. Mol Immunol 2008; 45: 3401-3410.
60. Chensue SW, Lukacs NW, Yang TY, Shang X, Frait KA, Kunkel SL et al. Aberrant in vivo T helper type 2 cell response and impaired eosinophil recruitment in CC chemokine receptor 8 knockout mice. J Exp Med 2001; 193: 573-584. (Pubitemid 32539554)
61. Goya I, Villares R, Zaballos A, Gutierrez J, Kremer L, Gonzalo JA et al. Absence of CCR8 does not impair the response to ovalbumin-induced allergic airway disease. J Immunol 2003; 170: 2138-2146. (Pubitemid 36197437)
62. Krueger A, Willenzon S, Lyszkiewicz M, Kremmer E, Forster R. CC chemokine receptor 7 and 9 double-deficient hematopoietic progenitors are severely impaired in seeding the adult thymus. Blood 2010; 115: 1906-1912.
63. Varona R, Villares R, Carramolino L, Goya I, Zaballos A, Gutierrez J et al. CCR6-deficient mice have impaired leukocyte homeostasis and altered contact hypersensitivity and delayed-type hypersensitivity responses. J Clin Invest 2001; 107: R37-R45. (Pubitemid 32225363)
64. Zlotoff DA, Sambandam A, Logan TD, Bell JJ, Schwarz BA, Bhandoola A. CCR7 and CCR9 together recruit hematopoietic progenitors to the adult thymus. Blood 2010; 115: 1897-1905.
65. Kurobe H, Liu C, Ueno T, Saito F, Ohigashi I, Seach N et al. CCR7-dependent cortex-to-medulla migration of positively selected thymocytes is essential for establishing central tolerance. Immunity 2006; 24: 165-177. (Pubitemid 43214586)
66. Nitta T, Nitta S, Lei Y, Lipp M, Takahama Y. CCR7-mediated migration of developing thymocytes to the medulla is essential for negative selection to tissue-restricted antigens. Proc Natl Acad Sci USA 2009; 106: 17129-17133.
67. Chung CD, Kuo F, Kumer J, Motani AS, Lawrence CE, Henderson Jr WR et al. CCR8 is not essential for the development of inflammation in a mouse model of allergic airway disease. J Immunol 2003; 170: 581-587. (Pubitemid 36026186)
68. Davalos-Misslitz AC, Rieckenberg J, Willenzon S, Worbs T, Kremmer E, Bernhardt G et al. Generalized multi-organ autoimmunity in CCR7-deficient mice. Eur J Immunol 2007; 37: 613-622. (Pubitemid 46916929)
69. Benz C, Heinzel K, Bleul CC. Homing of immature thymocytes to the subcapsular microenvironment within the thymus is not an absolute requirement for T cell development. Eur J Immunol 2004; 34: 3652-3663. (Pubitemid 40012183)
70. Davalos-Misslitz AC, Worbs T, Willenzon S, Bernhardt G, Forster R. Impaired responsiveness to T-cell receptor stimulation and defective negative selection of thymocytes in CCR7-deficient mice. Blood 2007; 110: 4351-4359. (Pubitemid 351377800)
71. Svensson M, Marsal J, Uronen-Hansson H, Cheng M, Jenkinson W, Cilio C et al. Involvement of CCR9 at multiple stages of adult T lymphopoiesis. J Leukoc Biol 2008; 83: 156-164.
72. Chvatchko Y, Hoogewerf AJ, Meyer A, Alouani S, Juillard P, Buser R et al. A key role for CC chemokine receptor 4 in lipopolysaccharide-induced endotoxic shock. J Exp Med 2000; 191: 1755-1764.
73. Wurbel MA, Malissen M, Guy-Grand D, Meffre E, Nussenzweig MC, Richelme M et al. 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.
74. Uehara S, Grinberg A, Farber JM, Love PE. A role for CCR9 in T lymphocyte development and migration. J Immunol 2002; 168: 2811-2819. (Pubitemid 34211660)
75. Schwarz BA, Sambandam A, Maillard I, Harman BC, Love PE, Bhandoola A. Selective thymus settling regulated by cytokine and chemokine receptors. J Immunol 2007; 178: 2008-2017. (Pubitemid 46233397)
76. Jotereau F, Heuze F, Salomon-Vie V, Gascan H. Cell kinetics in the fetal mouse thymus: precursor cell input, proliferation, and emigration. J Immunol 1987; 138: 1026-1030. (Pubitemid 17017879)
77. Yoshida R, Imai T, Hieshima K, Kusuda J, Baba M, Kitaura M et al. Molecular cloning of a novel human CC chemokine EBI1-ligand chemokine that is a specific functional ligand for EBI1, CCR7. J Biol Chem 1997; 272: 13803-13809. (Pubitemid 27224818)
78. Yoshida R, Nagira M, Kitaura M, Imagawa N, Imai T, Yoshie O. Secondary lymphoid-tissue chemokine is a functional ligand for the CC chemokine receptor CCR7. J Biol Chem 1998; 273: 7118-7122. (Pubitemid 28160383)
79. Nakano H, Gunn MD. 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 2001; 166: 361-369. (Pubitemid 32038453)
80. Zaballos A, Gutierrez J, Varona R, Ardavin C, Marquez G. Cutting edge: identification of the orphan chemokine receptor GPR-9-6 as CCR9, the receptor for the chemokine TECK. J Immunol 1999; 162: 5671-5675. (Pubitemid 29314915)
81. Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, Kitamura Y et al. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 1996; 382: 635-638. (Pubitemid 26268957)
82. Aiuti A, Tavian M, Cipponi A, Ficara F, Zappone E, Hoxie J et al. Expression of CXCR4, the receptor for stromal cell-derived factor-1 on fetal and adult human lymphohematopoietic progenitors. Eur J Immunol 1999; 29: 1823-1831. (Pubitemid 29265537)
83. Foster K, Sheridan J, Veiga-Fernandes H, Roderick K, Pachnis V, Adams R et al. Contribution of neural crest-derived cells in the embryonic and adult thymus. J Immunol 2008; 180: 3183-3189.
84. Ara T, Itoi M, Kawabata K, Egawa T, Tokoyoda K, Sugiyama T et al. A role of CXC chemokine ligand 12/stromal cell-derived factor-1/pre-B cell growth stimulating factor and its receptor CXCR4 in fetal and adult T cell development in vivo. J Immunol 2003; 170: 4649-4655. (Pubitemid 36519971)
85. Bhandoola A, Sambandam A, Allman D, Meraz A, Schwarz B. Early T lineage progenitors: new insights, but old questions remain. J Immunol 2003; 171: 5653-5658. (Pubitemid 37467176)
86. Foss DL, Donskoy E, Goldschneider I. The importation of hematogenous precursors by the thymus is a gated phenomenon in normal adult mice. J Exp Med 2001; 193: 365-374. (Pubitemid 32524519)
87. Prockop SE, Petrie HT. Regulation of thymus size by competition for stromal niches among early T cell progenitors. J Immunol 2004; 173: 1604-1611. (Pubitemid 38971590)
88. Rossi FM, Corbel SY, Merzaban JS, Carlow DA, Gossens K, Duenas J et al. Recruitment of adult thymic progenitors is regulated by P-selectin and its ligand PSGL-1. Nat Immunol 2005; 6: 626-634. (Pubitemid 41710734)
89. Gossens K, Naus S, Corbel SY, Lin S, Rossi FM, Kast J et al. Thymic progenitor homing and lymphocyte homeostasis are linked via S1P-controlled expression of thymic P-selectin/CCL25. J Exp Med 2009; 206: 761-778.
90. Robertson P, Means TK, Luster AD, Scadden DT. CXCR4 and CCR5 mediate homing of primitive bone marrow-derived hematopoietic cells to the postnatal thymus. Exp Hematol 2006; 34: 308-319.
91. Lee PP, Fitzpatrick DR, Beard C, Jessup HK, Lehar S, Makar KW et al. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 2001; 15: 763-774. (Pubitemid 34008504)
92. Janas ML, Varano G, Gudmundsson K, Noda M, Nagasawa T, Turner M. Thymic development beyond beta-selection requires phosphatidylinositol 3-kinase activation by CXCR4. J Exp Med 2010; 207: 247-261.
93. Zingoni A, Soto H, Hedrick JA, Stoppacciaro A, Storlazzi CT, Sinigaglia F et al. The chemokine receptor CCR8 is preferentially expressed in Th2 but not Th1 cells. J Immunol 1998; 161: 547-551. (Pubitemid 28323513)
94. Suzuki G, Nakata Y, Dan Y, Uzawa A, Nakagawa K, Saito T et al. Loss of SDF-1 receptor expression during positive selection in the thymus. Int Immunol 1998; 10: 1049-1056. (Pubitemid 28362678)
95. Goya I, Gutierrez J, Varona R, Kremer L, Zaballos A, Marquez G. Identification of CCR8 as the specific receptor for the human beta-chemokine I-309: cloning and molecular characterization of murine CCR8 as the receptor for TCA-3. J Immunol 1998; 160: 1975-1981. (Pubitemid 28106488)
96. Kremer L, Carramolino L, Goya I, Zaballos A, Gutierrez J, Moreno-Ortiz MDC et al. The transient expression of C-C chemokine receptor 8 in thymus identifies a thymocyte subset committed to become CD4+ single-positive T cells. J Immunol 2001; 166: 218-225. (Pubitemid 32038435)
97. Yin X, Ladi E, Chan SW, Li O, Killeen N, Kappes DJ et al. CCR7 expression in developing thymocytes is linked to the CD4 versus CD8 lineage decision. J Immunol 2007; 179: 7358-7364.
98. Hikosaka Y, Nitta T, Ohigashi I, Yano K, Ishimaru N, Hayashi Y et al. The cytokine RANKL produced by positively selected thymocytes fosters medullary thymic epithelial cells that express autoimmune regulator. Immunity 2008; 29: 438-450.
99. Zubkova I, Mostowski H, Zaitseva M. Up-regulation of IL-7, stromal-derived factor-1 alpha, thymus-expressed chemokine, and secondary lymphoid tissue chemokine gene expression in the stromal cells in response to thymocyte depletion: implication for thymus reconstitution. J Immunol 2005; 175: 2321-2330. (Pubitemid 41113841)
100. Drennan MB, Elewaut D, Hogquist KA. Thymic emigration: sphingosine-1-phosphate receptor-1-dependent models and beyond. Eur J Immunol 2009; 39: 925-930.
101. DeKoning J, DiMolfetto L, Reilly C, Wei Q, Havran WL, Lo D. Thymic cortical epithelium is sufficient for the development of mature T cells in relB-deficient mice. J Immunol 1997; 158: 2558-2566. (Pubitemid 127470511)
102. Poznansky MC, Olszak IT, Evans RH, Wang Z, Foxall RB, Olson DP et al. Thymocyte emigration is mediated by active movement away from stroma-derived factors. J Clin Invest 2002; 109: 1101-1110. (Pubitemid 34408585)
103. Vianello F, Kraft P, Mok YT, Hart WK, White N, Poznansky MC. A CXCR4-dependent chemorepellent signal contributes to the emigration of mature single-positive CD4 cells from the fetal thymus. J Immunol 2005; 175: 5115-5125. (Pubitemid 41456395)
104. Ribot J, Enault G, Pilipenko S, Huchenq A, Calise M, Hudrisier D et al. Shaping of the autoreactive regulatory T cell repertoire by thymic cortical positive selection. J Immunol 2007; 179: 6741-6748.
105. Liston A, Nutsch KM, Farr AG, Lund JM, Rasmussen JP, Koni PA et al. Differentiation of regulatory Foxp3+ T cells in the thymic cortex. Proc Natl Acad Sci USA 2008; 105: 11903-11908.
106. Fontenot JD, Rasmussen JP, Williams LM, Dooley JL, Farr AG, Rudensky AY. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 2005; 22: 329-341. (Pubitemid 40387475)
107. Lee JH, Kang SG, Kim CH. FoxP3+ T cells undergo conventional first switch to lymphoid tissue homing receptors in thymus but accelerated second switch to nonlymphoid tissue homing receptors in secondary lymphoid tissues. J Immunol 2007; 178: 301-311.
108. Bonasio R, Scimone ML, Schaerli P, Grabie N, Lichtman AH, von Andrian UH. Clonal deletion of thymocytes by circulating dendritic cells homing to the thymus. Nat Immunol 2006; 7: 1092-1100. (Pubitemid 44420654)
109. Proietto AI, van Dommelen S, Wu L. The impact of circulating dendritic cells on the development and differentiation of thymocytes. Immunol Cell Biol 2009; 87: 39-45.
110. Li J, Park J, Foss D, Goldschneider I. Thymus-homing peripheral dendritic cells constitute two of the three major subsets of dendritic cells in the steady-state thymus. J Exp Med 2009; 206: 607-622.
111. Proietto AI, van Dommelen S, Zhou P, Rizzitelli A, D'Amico A, Steptoe RJ et al. Dendritic cells in the thymus contribute to T-regulatory cell induction. Proc Natl Acad Sci USA 2008; 105: 19869-19874.
112. Johnston B, Kim CH, Soler D, Emoto M, Butcher EC. Differential chemokine responses and homing patterns of murine TCR alpha beta NKT cell subsets. J Immunol 2003; 171: 2960-2969. (Pubitemid 37093518)
113. Lee S, Tiffany HL, King L, Murphy PM, Golding H, Zaitseva MB. CCR8 on human thymocytes functions as a human immunodeficiency virus type 1 coreceptor. J Virol 2000; 74: 6946-6952. (Pubitemid 30470677)
114. Napolitano M, Zingoni A, Bernardini G, Spinetti G, Nista A, Storlazzi CT et al. Molecular cloning of TER1, a chemokine receptor-like gene expressed by lymphoid tissues. J Immunol 1996; 157: 2759-2763. (Pubitemid 126450027)
115. Rothenberg ME, MacLean JA, Pearlman E, Luster AD, Leder P. Targeted disruption of the chemokine eotaxin partially reduces antigen-induced tissue eosinophilia. J Exp Med 1997; 185: 785-790. (Pubitemid 27098162)
116. Varona R, Zaballos A, Gutierrez J, Martin P, Roncal F, Albar JP et al. Molecular cloning, functional characterization and mRNA expression analysis of the murine chemokine receptor CCR6 and its specific ligand MIP-3alpha. FEBS Lett 1998; 440: 188-194. (Pubitemid 28558762)
117. Jarmin DI, Rits M, Bota D, Gerard NP, Graham GJ, Clark-Lewis I et al. Cutting edge: identification of the orphan receptor G-protein-coupled receptor 2 as CCR10, a specific receptor for the chemokine ESkine. J Immunol 2000; 164: 3460-3464. (Pubitemid 30169793)
118. Fu W, Zhang Y, Zhang J, Chen WF. Cloning and characterization of mouse homolog of the CXC chemokine receptor CXCR1. Cytokine 2005; 31: 9-17. (Pubitemid 40828354)
119. Comerford I, Nibbs RJ. Post-translational control of chemokines: a role for decoy receptors? Immunol Lett 2005; 96: 163-174.
120. Mantovani A, Bonecchi R, Locati M. Tuning inflammation and immunity by chemokine sequestration: decoys and more. Nat Rev Immunol 2006; 6: 907-918. (Pubitemid 44851733)
121. Comerford I, Litchfield W, Harata-Lee Y, Nibbs RJ, McColl SR. Regulation of chemotactic networks by 'atypical' receptors. Bioessays 2007; 29: 237-247. (Pubitemid 46384163)
122. Comerford I, Nibbs RJ, Litchfield W, Bunting M, Harata-Lee Y, Haylock-Jacobs S et al. The atypical chemokine receptor CCX-CKR scavenges homeostatic chemokines in circulation and tissues and suppresses Th17 responses. Blood 2010 (in press).
123. Gosling J, Dairaghi DJ, Wang Y, Hanley M, Talbot D, Miao Z et al. Cutting edge: identification of a novel chemokine receptor that binds dendritic cell- and T cell-active chemokines including ELC, SLC, and TECK. J Immunol 2000; 164: 2851-2856. (Pubitemid 30148939)
124. Townson JR, Nibbs RJ. Characterization of mouse CCX-CKR, a receptor for the lymphocyte-attracting chemokines TECK/mCCL25, SLC/mCCL21 and MIP-3beta/mCCL19: comparison to human CCX-CKR. Eur J Immunol 2002; 32: 1230-1241. (Pubitemid 34546250)
125. Comerford I, Milasta S, Morrow V, Milligan G, Nibbs R. The chemokine receptor CCX-CKR mediates effective scavenging of CCL19 in vitro. Eur J Immunol 2006; 36: 1904-1916. (Pubitemid 44089056)
126. Heinzel K, Benz C, Bleul CC. A silent chemokine receptor regulates steady-state leukocyte homing in vivo. Proc Natl Acad Sci USA 2007; 104: 8421-8426. (Pubitemid 47175503)
127. Nibbs RJ, Wylie SM, Pragnell IB, Graham GJ. Cloning and characterization of a novel murine beta chemokine receptor, D6. Comparison to three other related macrophage inflammatory protein-1alpha receptors, CCR-1, CCR-3, and CCR-5. J Biol Chem 1997; 272: 12495-12504.
128. Graham GJ. D6 and the atypical chemokine receptor family: novel regulators of immune and inflammatory processes. Eur J Immunol 2009; 39: 342-351.
129. Migeotte I, Franssen JD, Goriely S, Willems F, Parmentier M. Distribution and regulation of expression of the putative human chemokine receptor HCR in leukocyte populations. Eur J Immunol 2002; 32: 494-501. (Pubitemid 34173341)