Revisiting the role of B cells in skin immune surveillance

Trends in Immunology

Volumn 36, Issue 2, 2015, Pages 102-111

  Egbuniwe, Isioma U ^a   Karagiannis, Sophia N ^a   Nestle, Frank O ^a   Lacy, Katie E ^a  

^a GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

B cell; Skin immune system; Skin pathology; Skin surveillance; Skin homing lymphocyte

Indexed keywords

ADOPTIVE TRANSFER; ANIMAL; ANTIINFLAMMATORY ACTIVITY; AUTOIMMUNITY; B LYMPHOCYTE; CELL GROWTH; CELL INFILTRATION; CELL MIGRATION; CELL MOTION; CELL POPULATION; DENDRITIC CELL; DERMATITIS; DERMOEPIDERMAL JUNCTION; GENETICS; HOMEOSTASIS; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOLOGY; IMMUNOSURVEILLANCE; MELANOMA; METABOLISM; NONHUMAN; PERIPHERAL CIRCULATION; PHENOTYPE; REVIEW; SKIN; SKIN TUMOR; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE;

ANIMALS; B-LYMPHOCYTES; CELL MOVEMENT; DERMATITIS; GENETICS; HUMANS; IMMUNOLOGIC SURVEILLANCE; IMMUNOLOGY; METABOLISM; SKIN; SKIN NEOPLASMS;

EID: 84954081087     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2014.12.006     Document Type: Review

References (110)

1. Kupper T.S., Fuhlbrigge R.C. Immune surveillance in the skin: mechanisms and clinical consequences. Nat. Rev. Immunol. 2004, 4:211-222.
2. Streilein J.W. Skin-associated lymphoid tissues (SALT): origins and functions. J. Invest. Dermatol. 1983, 120:12s-16s.
3. Bos J.D., Kapsenberg M.L. The skin immune system Its cellular constituents and their interactions. Immunol. Today 1986, 7:235-240.
4. Nestle F.O., et al. Skin immune sentinels in health and disease. Nat. Rev. Immunol. 2009, 9:679-691.
5. Pasparakis M., et al. Mechanisms regulating skin immunity and inflammation. Nat. Rev. Immunol. 2014, 14:289-301.
6. Chu C-C., et al. Harnessing dendritic cells in inflammatory skin diseases. Semin. Immunol. 2011, 23:28-41.
7. Clark R.A. Skin-resident T cells: the ups and downs of on site immunity. J. Invest. Dermatol. 2009, 130:362-370.
8. Gebhardt T., et al. Peripheral tissue surveillance and residency by memory T cells. Trends Immunol. 2013, 34:27-32.
9. McKee S.J., et al. Immunosuppressive roles of natural killer T (NKT) cells in the skin. J. Leukoc. Biol. 2014, 96:49-54.
10. Lacy K.E., et al. Advances in the treatment of melanoma. Clin. Med. J. R. Coll. Physicians 2012, 12:168-171.
11. Rivera A., et al. Role of B cells as antigen-presenting cells in vivo revisited: antigen-specific B cells are essential for T cell expansion in lymph nodes and for systemic T cell responses to low antigen concentrations. Int. Immunol. 2001, 13:1583-1593.
12. Rodríguez-Pinto D. B cells as antigen presenting cells. Cell. Immunol. 2005, 238:67-75.
13. Lund F.E. Cytokine-producing B lymphocytes-key regulators of immunity. Curr. Opin. Immunol. 2008, 20:332-338.
14. Duddy M.E., et al. Distinct profiles of human B cell effector cytokines: a role in immune regulation?. J. Immunol. 2004, 172:3422-3427.
15. Duddy M., et al. Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. J. Immunol. 2007, 178:6092-6099.
16. hi B Cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity 2010, 32:129-140.
17. Barr T.A., et al. B cell depletion therapy ameliorates autoimmune disease through ablation of IL-6-producing B cells. J. Exp. Med. 2012, 209:1001-1010.
18. Karagiannis P., et al. IgG4 subclass antibodies impair antitumor immunity in melanoma. J. Clin. Invest. 2013, 123:1457-1474.
19. Picker L.J., Butcher E.C. Physiological and molecular mechanisms of lymphocyte homing. Annu. Rev. Immunol. 1992, 10:561-591.
20. Kantele A., et al. Differential homing commitments of antigen-specific t cells after oral or parenteral immunization in humans. J. Immunol. 1999, 162:5173-5177.
21. + T cells activated in cutaneous or mucosal lymphoid tissues. J. Exp. Med. 2002, 195:135-141.
22. Sundström P., et al. Human IgA-secreting cells induced by intestinal, but not systemic, immunization respond to CCL25 (TECK) and CCL28 (MEC). Eur. J. Immunol. 2008, 38:3327-3338.
23. Mora J.R., et al. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 2003, 424:88-93.
24. Mora J.R., et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 2006, 314:1157-1160.
25. Sigmundsdottir H., et al. DCs metabolize sunlight-induced vitamin D3 to 'program' T cell attraction to the epidermal chemokine CCL27. Nat. Immunol. 2007, 8:285-293.
26. Sigmundsdottir H., Butcher E.C. Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking. Nat. Immunol. 2008, 9:981-987.
27. Salmi M., Jalkanen S. Lymphocyte homing to the gut: attraction, adhesion, and commitment. Immunol. Rev. 2005, 206:100-113.
28. von Andrian U.H., Mempel T.R. Homing and cellular traffic in lymph nodes. Nat. Rev. Immunol. 2003, 3:867-878.
29. Berg E.L., et al. The cutaneous lymphocyte antigen is a skin lymphocyte homing receptor for the vascular lectin endothelial cell-leukocyte adhesion molecule 1. J. Exp. Med. 1991, 174:1461-1466.
30. Bevilacqua M.P., et al. Endothelial leukocyte adhesion molecule 1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science 1989, 243:1160-1165.
31. Groves R.W., et al. Endothelial leucocyte adhesion molecule-1 (ELAM-1) expression in cutaneous inflammation. Br. J. Dermatol. 1991, 124:117-123.
32. Groves R.W., et al. Effect of in vivo interleukin-1 on adhesion molecule expression in normal human skin. J. Invest. Dermatol. 1992, 98:384-387.
33. Chong B.F., et al. E-Selectin, thymus- and activation-regulated chemokine/CCL17, and intercellular adhesion molecule-1 are constitutively coexpressed in dermal microvessels: a foundation for a cutaneous immunosurveillance system. J. Immunol. 2004, 172:1575-1581.
34. Postigo A.A., et al. B lymphocyte binding to E- and P-selectins is mediated through the de novo expression of carbohydrates on in vitro and in vivo activated human B cells. J. Clin. Invest. 1994, 94:1585-1596.
35. Rott L.S., et al. Expression of α4β7 and E-selectin ligand by circulating memory B cells: implications for targeted trafficking to mucosal and systemic sites. J. Leukoc. Biol. 2000, 68:807-814.
36. Yoshino T., et al. Cutaneous lymphocyte antigen is expressed on memory/effector B cells in the peripheral blood and monocytoid B cells in the lymphoid tissues. Cell. Immunol. 1999, 197:39-45.
37. Geherin S.A., et al. The skin, a novel niche for recirculating B cells. J. Immunol. 2012, 188:6027-6035.
38. Zarbock A., et al. Leukocyte ligands for endothelial selectins: specialized glycoconjugates that mediate rolling and signaling under flow. Blood 2011, 118:6743-6751.
39. Fuhlbrigge R.C., et al. Cutaneous lymphocyte antigen is a specialized form of PSGL-1 expressed on skin-homing T cells. Nature 1997, 389:978-981.
40. Kantele A., et al. Cutaneous lymphocyte antigen expression on human effector B cells depends on the site and on the nature of antigen encounter. Eur. J. Immunol. 2003, 33:3275-3283.
41. Nanki T., et al. Chemokine receptor expression and functional effects of chemokines on B cells: implication in the pathogenesis of rheumatoid arthritis. Arthritis Res. Ther. 2009, 11:R149.
42. Kunkel E.J., Butcher E.C. Plasma-cell homing. Nat. Rev. Immunol. 2003, 3:822-829.
43. Liao F., et al. Human B cells become highly responsive to macrophage-inflammatory protein-3α/CC chemokine ligand-20 after cellular activation without changes in CCR6 expression or ligand binding. J. Immunol. 2002, 168:4871-4880.
44. + T cells are resident in normal skin. J. Immunol. 2006, 176:4431-4439.
45. Fitzhugh D.J., et al. Cutting edge: 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.
46. Groom J.R., Luster A.D. CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunol. Cell Biol. 2011, 89:207-215.
47. Rottman J.B., et al. Potential role of the chemokine receptors CXCR3, CCR4, and the integrin alphaEbeta7 in the pathogenesis of psoriasis vulgaris. Lab. Invest. 2001, 81:335-347.
48. Villarroel V.A., et al. CXCR3-mediated skin homing of autoreactive CD8 T cells is a key determinant in murine graft-versus-host disease. J. Invest. Dermatol. 2014, 134:1552-1560.
49. Corcione A., et al. Phenotypic and functional characterization of switch memory B cells from patients with oligoarticular juvenile idiopathic arthritis. Arthritis Res. Ther. 2009, 11:R150.
50. Homey B., et al. Cutting edge: the orphan chemokine receptor G protein-coupled receptor-2 (GPR-2, CCR10) binds the skin-associated chemokine CCL27 (CTACK/ALP/ILC). J. Immunol. 2000, 164:3465-3470.
51. Homey B., et al. CCL27-CCR10 interactions regulate T cell-mediated skin inflammation. Nat. Med. 2002, 8:157-165.
52. Ferenczi K., et al. Increased CCR4 expression in cutaneous T cell lymphoma. J. Invest. Dermatol. 2002, 119:1405-1410.
53. + B cells. Clin. Exp. Immunol. 2005, 141:279-287.
54. Corcione A., et al. Chemotaxis of human tonsil B lymphocytes to CC chemokine receptor (CCR) 1, CCR2 and CCR4 ligands is restricted to non-germinal center cells. Int. Immunol. 2002, 14:883-892.
55. Shirakawa A-K., et al. 1,25-Dihydroxyvitamin D3 induces CCR10 expression in terminally differentiating human b cells. J. Immunol. 2008, 180:2786-2795.
56. +) over 'naive' T cells (CD4, CD45R) in both normal and diseased human skin. Arch. Dermatol. Res. 1989, 281:24-30.
57. Boyman O., et al. Spontaneous development of psoriasis in a new animal model shows an essential role for resident T cells and tumor necrosis factor-α. J. Exp. Med. 2004, 199:731-736.
58. + TRM cells providing global skin immunity. Nature 2012, 483:227-231.
59. + tissue-resident memory T cells of skin. Nat. Immunol. 2013, 14:1294-1301.
60. Nihal M., et al. Detection of clonally restricted immunoglobulin heavy chain gene rearrangements in normal and lesional skin: analysis of the B cell component of the skin-associated lymphoid tissue and implications for the molecular diagnosis of cutaneous B cell lymphomas. J. Mol. Diagn. 2000, 2:5-10.
61. Akbar A.N., et al. Investigation of the cutaneous response to recall antigen in humans in vivo. Clin. Exp. Immunol. 2013, 173:163-172.
62. Neeland M.R., et al. Afferent lymphatic cannulation as a model system to study innate immune responses to infection and vaccination. Vet. Immunol. Immunopathol. 2014, 158:86-97.
63. Hein W.R., Griebel P.J. A road less travelled: large animal models in immunological research. Nat. Rev. Immunol. 2003, 3:79-84.
64. Geiger B., et al. Resolving lesions in human cutaneous leishmaniasis predominantly harbour chemokine receptor CXCR3-positive T helper 1/T cytotoxic type 1 cells. Br. J. Dermatol. 2010, 162:870-874.
65. Lafyatis R., et al. B cell depletion with rituximab in patients with diffuse cutaneous systemic sclerosis. Arthritis Rheum. 2009, 60:578-583.
66. Simon D., et al. Anti-CD20 (rituximab) treatment improves atopic eczema. J. Allergy Clin. Immunol. 2008, 121:122-128.
67. Tsuji R.F., et al. B cell-dependent T cell responses: IgM antibodies are required to elicit contact sensitivity. J. Exp. Med. 2002, 196:1277-1290.
68. Szczepanik M., et al. B-1 B cells mediate required early T cell recruitment to elicit protein-induced delayed-type hypersensitivity. J. Immunol. 2003, 171:6225-6235.
69. Covens K., et al. Characterization of proposed human B-1 cells reveals pre-plasmablast phenotype. Blood 2013, 121:5176-5183.
70. Mabbott N.A., Gray D. Identification of co-expressed gene signatures in mouse B1, marginal zone and B2 B-cell populations. Immunology 2014, 141:79-95.
71. Tangye S.G. To B1 or not to B1: that really is still the question!. Blood 2013, 121:5109-5110.
72. Yanaba K., et al. CD19 Expression in B cells regulates atopic dermatitis in a mouse model. Am. J. Pathol. 2013, 182:2214-2222.
73. Ponte P., Lopes M.J.P. Apparent safe use of single dose rituximab for recalcitrant atopic dermatitis in the first trimester of a twin pregnancy. J. Am. Acad. Dermatol. 2010, 63:355-356.
74. Baum S., et al. Diagnosis and classification of autoimmune blistering diseases. Autoimmun. Rev. 2014, 13:482-489.
75. Schmidt E., et al. Rituximab in treatment-resistant autoimmune blistering skin disorders. Clin. Rev. Allergy Immunol. 2008, 34:56-64.
76. Schmidt E., et al. Rituximab in autoimmune bullous diseases: mixed responses and adverse effects. Br. J. Dermatol. 2007, 156:352-356.
77. Schulze J., et al. Severe bullous pemphigoid in an infant - successful treatment with rituximab. Pediatr. Dermatol. 2008, 25:462-465.
78. Saouli Z., et al. A new approach on bullous pemphigoid therapy. Ann. Oncol. 2008, 825-826.
79. Reguiai Z., et al. Efficacy of rituximab in a case of refractory bullous pemphigoid. Ann. Dermatol. Venereol. 2009, 136:431-434. (article in French).
80. Lourari S., et al. Bullous and mucous membrane pemphigoid show a mixed response to rituximab: experience in seven patients. J. Eur. Acad. Dermatol. Venereol. 2011, 25:1238-1240.
81. Kasperkiewicz M., et al. Rituximab for treatment-refractory pemphigus and pemphigoid: a case series of 17 patients. J. Am. Acad. Dermatol. 2011, 65:552-558.
82. Neta R., Salvin S.B. Specific suppression of delayed hypersensitivity: the possible presence of a suppressor B cell in the regulation of delayed hypersensitivity. J. Immunol. 1974, 113:1716-1725.
83. Mauri C., Bosma A. Immune regulatory function of B cells. Annu. Rev. Immunol. 2012, 30:221-241.
84. Candando K.M., et al. B10 cell regulation of health and disease. Immunol. Rev. 2014, 259:259-272.
85. Yanaba K., et al. Regulatory B cells suppress imiquimod-induced, psoriasis-like skin inflammation. J. Leukoc. Biol. 2013, 94:563-573.
86. + phenotype controls T cell-dependent inflammatory responses. Immunity 2008, 28:639-650.
87. Iwata Y., et al. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 2011, 117:530-541.
88. Dass S., et al. Development of psoriasis after B cell depletion with rituximab. Arthritis Rheum. 2007, 56:2715-2718.
89. Mielke F., et al. Onset of psoriasis with psoriatic arthropathy during rituximab treatment of non-Hodgkin lymphoma. Ann. Rheum. Dis. 2008, 67:1056-1057.
90. Affara NesrineI., et al. B cells regulate macrophage phenotype and response to chemotherapy in squamous carcinomas. Cancer Cell 2014, 25:809-821.
91. Ladányi A., et al. Prognostic impact of B-cell density in cutaneous melanoma. Cancer Immunol. Immunother. 2011, 60:1729-1738.
92. de Visser K.E., et al. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 2005, 7:411-423.
93. Andreu P., et al. FcRγ activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell 2010, 17:121-134.
94. Schioppa T., et al. B regulatory cells and the tumor-promoting actions of TNF-α during squamous carcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:10662-10667.
95. Ruddell A., et al. B lymphocytes promote lymphogenous metastasis of lymphoma and melanoma. Neoplasia 2011, 13:748-757.
96. Yang C., et al. B cells promote tumor progression via STAT3 regulated-angiogenesis. PLoS ONE 2013, 8:e64159.
97. Ladányi A., et al. Ectopic lymphoid structures in primary cutaneous melanoma. Pathol. Oncol. Res. 2014, 1-5.
98. Cipponi A., et al. Neogenesis of lymphoid structures and antibody responses occur in human melanoma metastases. Cancer Res. 2012, 72:3997-4007.
99. Erdag G., et al. Immunotype and immunohistologic characteristics of tumor-infiltrating immune cells are associated with clinical outcome in metastatic melanoma. Cancer Res. 2012, 72:1070-1080.
100. Gilbert A.E., et al. Monitoring the systemic human memory b cell compartment of melanoma patients for anti-tumor IgG antibodies. PLoS ONE 2011, 6:e19330.
101. Egbuniwe I., et al. Interleukin-10-producing B-cell populations in melanoma. Br. J. Dermatol. 2012, 166:e35.
102. Egawa G., Kabashima K. Skin as a peripheral lymphoid organ: revisiting the concept of skin-associated lymphoid tissues. J. Invest. Dermatol. 2011, 131:2178-2185.
103. Shimizu Y., et al. Lymphocyte interactions with endothelial cells. Immunol. Today 1992, 13:106-112.
104. Arbonés M.L., et al. Lymphocyte homing and leukocyte rolling and migration are impaired in L-selectin-deficient mice. Immunity 1994, 1:247-260.
105. Stein J.V., Nombela-Arrieta C. Chemokine control of lymphocyte trafficking: a general overview. Immunology 2005, 116:1-12.
106. Okada T., et al. Chemokine requirements for B cell entry to lymph nodes and Peyer's patches. J. Exp. Med. 2002, 196:65-75.
107. Ebisuno Y., et al. 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, 171:1642-1646.
108. Rao R.M., et al. Endothelial-dependent mechanisms of leukocyte recruitment to the vascular wall. Circ. Res. 2007, 101:234-247.
109. Stefanidakis M., et al. Endothelial CD47 interaction with SIRPgamma is required for human T-cell transendothelial migration under shear flow conditions in vitro. Blood 2008, 112:1280-1289.
110. Watanabe R., et al. CD19 expression in B cells is important for suppression of contact hypersensitivity. Am. J. Pathol. 2007, 171:560-570.