The chemokine receptor CCR7 expressed by dendritic cells: A key player in corneal and ocular surface inflammation

Ocular Surface

Volumn 12, Issue 2, 2014, Pages 87-99

  Saban, Daniel R ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Allergic conjunctivitis; CCR7; CD103; Conjunctivitis; Dendritic cells; Dry eye disease; Keratitis; Ocular allergy; Ocular surface; T cells

Indexed keywords

CHEMOKINE RECEPTOR CCR7; CCR7 PROTEIN, HUMAN; CCR7 PROTEIN, MOUSE;

CELL MIGRATION; DENDRITIC CELL; DRY EYE; GENE EXPRESSION; HUMAN; HYPERSENSITIVITY; IMMUNOPATHOGENESIS; NONHUMAN; OCULAR SURFACE DISEASE; OCULAR SURFACE INFLAMMATION; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE ACTIVATION; ANIMAL; CONJUNCTIVITIS; CORNEA; CYTOLOGY; IMMUNOLOGY; KERATITIS; PATHOLOGY;

ANIMALS; CONJUNCTIVITIS; CORNEA; DENDRITIC CELLS; HUMANS; KERATITIS; RECEPTORS, CCR7;

EID: 84901497806     PISSN: 15420124     EISSN: 19375913     Source Type: Journal    
DOI: 10.1016/j.jtos.2013.10.007     Document Type: Review

References (103)

1. Khandelwal P, Blanco-Mezquita T, Emami P, et al. Ocular mucosal CD11b+ and CD103+ mouse dendritic cells under normal conditions and in allergic immune responses. PLoS One 2013;8:e64193
2. Schlereth S, Lee HS, Khandelwal P, Saban DR. Blocking CCR7 at the ocular surface impairs the pathogenic contribution of dendritic cells in allergic conjunctivitis. Am J Pathol 2012;180: 2351-60
3. Schaumburg CS, Siemasko KF, De Paiva CS, et al. Ocular surface APCs are necessary for autoreactive T cell-mediated experimental autoimmune lacrimal keratoconjunctivitis. J Immunol 2011;187: 3653-62
4. Chen Y, Chauhan SK, Soo Lee H, et al. Chronic dry eye disease is principally mediated by effector memory Th17 cells. Mucosal Immunol 2013 Apr 10. http://dx.doi.org/10.1038/mi.2013.20
5. Stern ME, Schaumburg CS, Pflugfelder SC. Dry eye as a mucosal autoimmune disease. Int Rev Immunol 2013;32: 19-41
6. Pflugfelder SC, Stern ME. Symposium Participants. Immunoregulation on the ocular surface: 2nd Cullen Symposium. Ocul Surf 2009;7: 67-77
7. Saban DR, Calder V, Kuo CH, et al. New twists to an old story: novel concepts in the pathogenesis of allergic eye disease. Curr Eye Res 2013;38: 317-30
8. Forster R, Schubel A, Breitfeld D, et al. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 1999;99: 23-33
9. Scandella E, Men Y, Gillessen S, et al. Prostaglandin E2 is a key factor for CCR7 surface expression and migration of monocyte-derived dendritic cells. Blood 2002;100: 1354-61
10. Saeki H, Moore AM, Brown MJ, Hwang ST. Cutting edge: secondary lymphoid-tissue chemokine (SLC) and CC chemokine receptor 7 (CCR7) participate in the emigration pathway of mature dendritic cells from the skin to regional lymph nodes. J Immunol 1999;162: 2472-5
11. Ohl L, Mohaupt M, Czeloth N, et al. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 2004;21: 279-88
12. Forster R, Davalos-Misslitz AC, Rot A. CCR7 and its ligands: balancing immunity and tolerance. Nat Rev Immunol 2008;8: 362-71
13. Yanagihara S, Komura E, Nagafune J, et al. EBI1/CCR7 is a new member of dendritic cell chemokine receptor that is up-regulated upon maturation. J Immunol 1998;161: 3096-102
14. Yu CR, Mahdi RM, Liu X, et al. SOCS1 regulates CCR7 expression and migration of CD4+ T cells into peripheral tissues. J Immunol 2008;181: 1190-8
15. Jin Y, Chauhan SK, Saban DR, Dana R. Role of CCR7 in facilitating direct allosensitization and regulatory T-cell function in high-risk corneal transplantation. Invest Ophthalmol Vis Sci 2010;51: 816-21
16. Irschick UM, Mayer WJ, Kranebitter N, et al. Active in vitro reduction of antigen presenting cells in human corneal grafts using different chemokines. Curr Eye Res 2010;35: 176-83
17. Jin Y, Shen L, Chong EM, et al. The chemokine receptor CCR7 mediates corneal antigen-presenting cell trafficking. Mol Vis 2007;13: 626-34
18. Ebihara N, Yamagami S, Yokoo S, et al. Involvement of C-C chemokine ligand 2-CCR2 interaction in monocyte-lineage cell recruitment of normal human corneal stroma. J Immunol 2007;178: 3288-92
19. Cook WJ, Kramer MF, Walker RM, et al. Persistent expression of chemokine and chemokine receptor RNAs at primary and latent sites of herpes simplex virus 1 infection. Virol J 2004;1: 5
20. Mackensen F, Metea CA, Planck SR, Rosenbaum JT. Endotoxin upregulates CCR7 and its ligands in the lymphatic-free mouse iris. Mol Vis 2007;13: 2209-13
21. Hua J, Stevenson W, Dohlman TH, et al. The CCR7-CCL19/CCL21 axis mediates enhanced antigen-presenting cell trafficking in highrisk corneal transplantation. Invest Ophthalmol Vis Sci 2013. 54 ARVO E-Abstract 1289
22. Mathew R, Mohd Zaki A, Galatowicz G, et al. CCR7 expression profiles in conjunctival biopsies from seasonal allergic conjunctivitis patients following challenge. Invest Ophthalmol Vis Sci 2013. 54 ARVO E-Abstract 2549
23. Saban DR, Bock F, Chauhan SK, et al. Thrombospondin-1 derived from APCs regulates their capacity for allosensitization. J Immunol 2010;185: 4691-7
24. Nagira M, Imai T, Hieshima K, et al. Molecular cloning of a novel human CC chemokine secondary lymphoid-tissue chemokine that is a potent chemoattractant for lymphocytes and mapped to chromosome 9p13. J Biol Chem 1997;272: 19518-24
25. Gunn MD, Tangemann K, Tam C, et al. A chemokine expressed in lymphoid high endothelial venules promotes the adhesion and chemotaxis of naive T lymphocytes. Proc Natl Acad Sci U S A 1998;95: 258-63
26. Hromas R, Kim CH, Klemsz M, et al. Isolation and characterization of Exodus-2, a novel C-C chemokine with a unique 37-amino acid carboxyl-terminal extension. J Immunol 1997;159: 2554-8
27. Hedrick JA, Zlotnik A. Identification and characterization of a novel beta chemokine containing six conserved cysteines. J Immunol 1997;159: 1589-93
28. Tanabe S, Lu Z, Luo Y, et al. Identification of a new mouse betachemokine, thymus-derived chemotactic agent 4, with activity on T lymphocytes and mesangial cells. J Immunol 1997;159: 5671-9
29. Yoshida R, Imai T, Hieshima K, 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: 13803-9
30. Rossi DL, Vicari AP, Franz-Bacon K, et al. Identification through bioinformatics of two new macrophage proinflammatory human chemokines: MIP-3a and MIP-3b. J Immunol 1997;158: 1033-6
31. Ngo VN, Tang HL, Cyster JG. Epstein-Barr viruseinduced molecule 1 ligand chemokine is expressed by dendritic cells in lymphoid tissues and strongly attracts naive T cells and activated B cells. J Exp Med 1998;188: 181-91
32. Yoshida R, Nagira M, Kitaura M, et al. Secondary lymphoid-tissue chemokine is a functional ligand for the CC chemokine receptor CCR7. J Biol Chem 1998;273: 7118-22
33. Burgstahler R, Kempkes B, Steube K, Lipp M. Expression of the chemokine receptor BLR2/EBI1 is specifically transactivated by Epstein-Barr virus nuclear antigen 2. Biochem Biophys Res Commun 1995;215: 737-43
34. Schweickart VL, Raport CJ, Godiska R, et al. Cloning of human and mouse EBI1, a lymphoid-specific G-protein-coupled receptor encoded on human chromosome 17q12-q21.2. Genomics 1994;23: 643-50
35. Birkenbach M, Josefsen K, Yalamanchili R, et al. Epstein-Barr virusinduced genes: first lymphocyte-specific G protein-coupled peptide receptors. J Virol 1993;67: 2209-20
36. Link A, Vogt TK, Favre S, et al. Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat Immunol 2007;8: 1255-65
37. Baekkevold ES, Yamanaka T, Palframan RT, et al. The CCR7 ligand elc (CCL19) is transcytosed in high endothelial venules and mediates T cell recruitment. J Exp Med 2001;193: 1105-12
38. Sallusto F, Palermo B, Lenig D, et al. Distinct patterns and kinetics of chemokine production regulate dendritic cell function. Eur J Immunol 1999;29: 1617-25
39. Gunn MD, Kyuwa S, Tam C, et al. Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization. J Exp Med 1999;189: 451-60
40. Vassileva G, Soto H, Zlotnik A, et al. The reduced expression of 6Ckine in the plt mouse results from the deletion of one of two 6Ckine genes. J Exp Med 1999;190: 1183-8
41. Carlsen HS, Haraldsen G, Brandtzaeg P, Baekkevold ES. Disparate lymphoid chemokine expression in mice and men: no evidence of CCL21 synthesis by human high endothelial venules. Blood 2005;106: 444-6
42. Luther SA, Tang HL, Hyman PL, et al. Coexpression of the chemokines ELC and SLC by T zone stromal cells and deletion of the ELC gene in the plt/plt mouse. Proc Natl Acad Sci U S A 2000;97: 12694-9
43. 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: 361-9
44. Martin-Fontecha A, Sebastiani S, Höpken UE, et al. Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J Exp Med 2003;198: 615-21
45. Stoll S, Delon J, Brotz TM, Germain RN. Dynamic imaging of T celldendritic cell interactions in lymph nodes. Science 2002;296(5574): 1873-6
46. Mori S, Nakano H, Aritomi K, et al. Mice lacking expression of the chemokines CCL21-ser and CCL19 (plt mice) demonstrate delayed but enhanced T cell immune responses. J Exp Med 2001;193: 207-18
47. Bajénoff M, Granjeaud S, Guerder S. The strategy of T cell antigenpresenting cell encounter in antigen-draining lymph nodes revealed by imaging of initial T cell activation. J Exp Med 2003;198: 715-24
48. Sallusto F, Lenig D, Förster R, et al. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999;401(6754): 708-12
49. Schneider MA, Meingassner JG, Lipp M, et al. CCR7 is required for the in vivo function of CD4+ CD25+ regulatory T cells. J Exp Med 2007;204: 735-45
50. Hattori T, Chauhan SK, Lee H, et al. Characterization of Langerinexpressing dendritic cell subsets in the normal cornea. Invest Ophthalmol Vis Sci 2011;52: 4598-604
51. Bursch LS, Wang L, Igyarto B, et al. Identification of a novel population of Langerin+ dendritic cells. J Exp Med 2007;204: 3147-56
52. Ginhoux F, Liu K, Helft J, et al. The origin and development of nonlymphoid tissue CD103+ DCs. J Exp Med 2009;206: 3115-30
53. Bogunovic M, Ginhoux F, Helft J, et al. Origin of the lamina propria dendritic cell network. Immunity 2009;31: 513-25
54. Persson EK, Uronen-Hansson H, Semmrich M, et al. IRF4 transcription-factor-dependent CD103(+)CD11b(+) dendritic cells drive mucosal T helper 17 cell differentiation. Immunity 2013;38: 958-69
55. Schlitzer A, McGovern N, Teo P, et al. IRF4 transcription factordependent CD11b+ dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 2013;38: 970-83
56. Edelson BT, KC W, Juang R, et al. Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J Exp Med 2010;207: 823-36
57. Bedoui S, Whitney PG, Waithman J, et al. Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat Immunol 2009;10: 488-95
58. del Rio ML, Rodriguez-Barbosa JI, Kremmer E, Förster R. CD103- and CD103+ bronchial lymph node dendritic cells are specialized in presenting and cross-presenting innocuous antigen to CD4+ and CD8+ T cells. J Immunol 2007;178: 6861-6
59. Hamrah P, Liu Y, Zhang Q, Dana MR. The corneal stroma is endowed with a significant number of resident dendritic cells. Invest Ophthalmol Vis Sci 2003;44: 581-9
60. Hamrah P, Huq SO, Liu Y, et al. Corneal immunity is mediated by heterogeneous population of antigen-presenting cells. J Leukoc Biol 2003;74: 172-8
61. Brissette-Storkus CS, Reynolds SM, Lepisto AJ, Hendricks RL. Identification of a novel macrophage population in the normal mouse corneal stroma. Invest Ophthalmol Vis Sci 2002;43: 2264-71
62. Chinnery HR, Humphries T, Clare A, et al. Turnover of bone marrowderived cells in the irradiatedmouse cornea. Immunology 2008;125: 541-8
63. Mayer WJ, Mackert MJ, Kranebitter N, et al. Distribution of antigen presenting cells in the human cornea: correlation of in vivo confocal microscopy and immunohistochemistry in different pathologic entities. Curr Eye Res 2012;37: 1012-8
64. Mayer WJ, Irschick UM, Moser P, et al. Characterization of antigenpresenting cells in fresh and cultured human corneas using novel dendritic cell markers. Invest Ophthalmol Vis Sci 2007;48: 4459-67
65. Hamrah P, Zhang Q, Liu Y, Dana MR. Novel characterization of MHC class II-negative population of resident corneal Langerhans cell-type dendritic cells. Invest Ophthalmol Vis Sci 2002;43: 639-46
66. Merad M, Ginhoux F, Collin M. Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat Rev Immunol 2008;8: 935-47
67. Segura E, Amigorena S. Inflammatory dendritic cells in mice and humans. Trends Immunol 2013;34: 440-5
68. Leonardi A, Fregona IA, PlebaniM, et al. Th1- and Th2-type cytokines in chronic ocular allergy. Graefes Arch Clin Exp Ophthalmol 2006;244: 1240-5
69. Stern ME, Siemasko KF, Niederkorn JY. The Th1/Th2 paradigm in ocular allergy. Curr Opin Allergy Clin Immunol 2005;5: 446-50
70. Metz DP, Hingorani M, Calder VL, et al. T-cell cytokines in chronic allergic eye disease. J Allergy Clin Immunol 1997;100(6 Pt 1): 817-24
71. Paul W. Fundamental immunology. ed 6. Philadelphia, PA, Lippincott Williams & Wilkins, 2008
72. Niederkorn JY, Stern ME, Pflugfelder SC, et al. Desiccating stress induces T cell-mediated Sjögren's Syndrome like lacrimal keratoconjunctivitis. J Immunol 2006;176: 3950-7
73. Sall K, Stevenson OD, Mundorf TK, Reis BL. Two multicenter, randomized studies of the efficacy and safety of cyclosporine ophthalmic emulsion in moderate to severe dry eye disease. CsA Phase 3 Study Group. Ophthalmology 2000;107: 631-9
74. Stern ME, Schaumburg CS, Siemasko KF, et al. Autoantibodies contribute to the immunopathogenesis of experimental dry eye disease. Invest Ophthalmol Vis Sci 2012;53: 2062-75
75. Zhang X, Chen W, De Paiva CS, et al. Desiccating stress induces CD4+ T-cell-mediated Sjögren's syndrome-like corneal epithelial apoptosis via activation of the extrinsic apoptotic pathway by interferon- g. Am J Pathol 2011;179: 1807-14
76. Rahimy E, Pitcher 3rd JD, Pangelinan SB, et al. Spontaneous autoimmune dacryoadenitis in aged CD25KO mice. Am J Pathol 2010;177: 744-53
77. Stern ME, Gao J, Schwalb TA, et al. Conjunctival T-cell subpopulations in Sjögren's and non-Sjögren's patients with dry eye. Invest Ophthalmol Vis Sci 2002;43: 2609-14
78. Dohlman TH, Chauhan SK, Kodati S, et al. The CCR6/CCL20 axis mediates Th17 cell migration to the ocular surface in dry eye disease. Invest Ophthalmol Vis Sci 2013;54: 4081-91
79. El Annan J, Goyal S, Zhang Q, et al. Regulation of T-cell chemotaxis by programmed death-ligand 1 (PD-L1) in dry eye-associated corneal inflammation. Invest Ophthalmol Vis Sci 2010;51: 3418-23
80. El Annan J, Chauhan SK, Ecoiffier T, et al. Characterization of effector T cells in dry eye disease. Invest Ophthalmol Vis Sci 2009;50: 3802-7
81. Chauhan SK, El Annan J, Ecoiffier T, et al. Autoimmunity in dry eye is due to resistance of Th17 to Treg suppression. J Immunol 2009;182: 1247-52
82. Goyal S, Chauhan SK, Dana R. Blockade of prolymphangiogenic vascular endothelial growth factor C in dry eye disease. Arch Ophthalmol 2012;130: 84-9
83. Lee HS, Hattori T, Park EY, et al. Expression of Toll-like receptor 4 contributes to corneal inflammation in experimental dry eye disease. Invest Ophthalmol Vis Sci 2012;53: 5632-40
84. Koldati S, Chauhan SK, Chen Y, Dana R. Chemokine receptor expression on corneal CD11b+ cells in dry eye disease. Invest Ophthalmol Vis Sci 2011. 52 ARVO Abstract# 3762
85. Turpie B, Yoshimura T, Gulati A, et al. Sjögren's syndrome-like ocular surface disease in thrombospondin-1 deficient mice. Am J Pathol 2009;175: 1136-47
86. Contreras-Ruiz L, Regenfuss B, Mir FA, et al. Conjunctival inflammation in thrombospondin-1 deficient mouse model of Sjögren's syndrome. PLoS One 2013;8:e75937
87. Niederkorn JY. Corneal transplantation and immune privilege. Int Rev Immunol 2013;32: 57-67
88. Hattori T, Saban DR, Emami-Naeini P, et al. Donor-derived, tolerogenic dendritic cells suppress immune rejection in the indirect allosensitization- dominant setting of corneal transplantation. J Leukoc Biol 2012;91: 621-7
89. Huq S, Liu Y, Benichou G, Dana MR. Relevance of the direct pathway of sensitization in corneal transplantation is dictated by the graft bed microenvironment. J Immunol 2004;173: 4464-9
90. Chen L, Hamrah P, Cursiefen C, et al. Vascular endothelial growth factor receptor-3 mediates induction of corneal alloimmunity. Nat Med 2004;10: 813-5
91. Saito T, Shinagawa K, Takenaka K, et al. Ocular manifestation of acute graft-versus-host disease after allogeneic peripheral blood stem cell transplantation. Int J Hematol 2002;75: 332-4
92. Kawasaki S, Nishida K, Sotozono C, et al. Conjunctival inflammation in the chronic phase of Stevens-Johnson syndrome. Br J Ophthalmol 2000;84: 1191-3
93. Bernauer W, Wright P, Dart JK, et al. The conjunctiva in acute and chronic mucous membrane pemphigoid. An immunohistochemical analysis. Ophthalmology 1993;100: 339-46
94. Frank GM, Buela KA, Maker DM, et al. Early responding dendritic cells direct the local NK response to control herpes simplex virus 1infection within the cornea. J Immunol 2012;188: 1350-9
95. Gao Y, Li Z, Hassan N, et al. NK cells are necessary for recovery of corneal CD11c+ dendritic cells after epithelial abrasion injury. J Leukoc Biol 2013;94: 343-51
96. Gao N, Yin J, Yoon GS, et al. Dendritic cell-epithelium interplay is a determinant factor for corneal epithelial wound repair. Am J Pathol 2011;179: 2243-53
97. Steinman RM. Some active areas of DC research and their medical potential. Eur J Immunol 2010;40: 2085-8
98. Schieffer B, Luchtefeld M. Emerging role of chemokine receptor 7 in atherosclerosis. Trends Cardiovasc Med 2011;21: 211-6
99. Burman A, Haworth O, Hardie DL, et al. A chemokine-dependent stromal induction mechanism for aberrant lymphocyte accumulation and compromised lymphatic return in rheumatoid arthritis. J Immunol 2005;174: 1693-700
100. Kawashima D, Oshitani N, Jinno Y, et al. Augmented expression of secondary lymphoid tissue chemokine and EBI1 ligand chemokine in Crohn's disease. J Clin Pathol 2005;58: 1057-63
101. Ohbayashi M, Manzouri B, Flynn T, et al. Dynamic changes in conjunctival dendritic cell numbers, anatomical position and phenotype during experimental allergic conjunctivitis. Exp Mol Pathol 2007;83: 216-23
102. Dieu MC, Vanbervliet B, Vicari A, et al. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J Exp Med 1998;188: 373-86
103. Birke K, Lütjen-Drecoll E, Kerjaschki D, Birke MT. Expression of podoplanin and other lymphatic markers in the human anterior eye segment. Invest Ophthalmol Vis Sci 2010;51: 344-54