Langerhans Cells – The Macrophage in Dendritic Cell Clothing

Trends in Immunology

Volumn 38, Issue 11, 2017, Pages 817-828

  Doebel, Thomas ^a   Voisin, Benjamin ^a   Nagao, Keisuke ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Langerhans cell function; Langerhans cell ontogeny; Langerhans cells

Indexed keywords

ANTIGEN SPECIFICITY; ANTIGENICITY; CANDIDA ALBICANS; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL PROLIFERATION; DENDRITIC CELL; DERMOEPIDERMAL JUNCTION; HUMORAL IMMUNITY; LANGERHANS CELL; MACROPHAGE; NONHUMAN; ONTOGENY; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; T LYMPHOCYTE; ANIMAL; ANTIGEN PRESENTATION; CELL MOTION; CELL SELF-RENEWAL; HOMEOSTASIS; HUMAN; IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; PHYSIOLOGY; REGULATORY T LYMPHOCYTE; TH17 CELL;

ANIMALS; ANTIGEN PRESENTATION; CELL MOVEMENT; CELL SELF RENEWAL; DENDRITIC CELLS; HOMEOSTASIS; HUMANS; IMMUNITY; IMMUNITY, HUMORAL; LANGERHANS CELLS; MACROPHAGES; SELF TOLERANCE; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 85023605840     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2017.06.008     Document Type: Review

References (87)

1. Merad, M., et al. Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat. Rev. Immunol. 8 (2008), 935–947.
2. Igyarto, B.Z., et al. Characterization of chicken epidermal dendritic cells. Immunology 119 (2006), 278–288.
3. Perez-Torres, A., et al. Epidermal Langerhans cells in the terrestrial turtle, Kinosternum integrum. Dev. Comp. Immunol. 19 (1995), 225–236.
4. Langerhans, P., Ueber die Nerven der menschlichen Haut. Archiv. Pathol. Anat. ​Physiol. Klin. Med. 44 (1868), 325–337.
5. Mass, E., et al. Specification of tissue-resident macrophages during organogenesis. Science, 353, 2016, aaf4238.
6. Gomez Perdiguero, E., et al. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 518 (2015), 547–551.
7. Schulz, C., et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336 (2012), 86–90.
8. Hoeffel, G., et al. C-Myb(+) erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity 42 (2015), 665–678.
9. Hoeffel, G., et al. Adult Langerhans cells derive predominantly from embryonic fetal liver monocytes with a minor contribution of yolk sac-derived macrophages. J. Exp. Med. 209 (2012), 1167–1181.
10. Sheng, J., et al. Most tissue-resident macrophages except microglia are derived from fetal hematopoietic stem cells. Immunity 43 (2015), 382–393.
11. Chorro, L., et al. Langerhans cell (LC) proliferation mediates neonatal development, homeostasis, and inflammation-associated expansion of the epidermal LC network. J. Exp. Med. 206 (2009), 3089–3100.
12. Gosselin, D., et al. Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell 159 (2014), 1327–1340.
13. Lavin, Y., et al. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159 (2014), 1312–1326.
14. Ghigo, C., et al. Multicolor fate mapping of Langerhans cell homeostasis. J. Exp. Med. 210 (2013), 1657–1664.
15. Soucie, E.L., et al. Lineage-specific enhancers activate self-renewal genes in macrophages and embryonic stem cells. Science, 351, 2016, aad5510.
16. Glick, A.B., et al. Loss of expression of transforming growth factor beta in skin and skin tumors is associated with hyperproliferation and a high risk for malignant conversion. Proc. Natl. Acad. Sci. U. S. A. 90 (1993), 6076–6080.
17. Kaplan, D.H., et al. Autocrine/paracrine TGFbeta1 is required for the development of epidermal Langerhans cells. J. Exp. Med. 204 (2007), 2545–2552.
18. Bobr, A., et al. Autocrine/paracrine TGF-beta1 inhibits Langerhans cell migration. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 10492–10497.
19. Kel, J.M., et al. TGF-beta is required to maintain the pool of immature Langerhans cells in the epidermis. J. Immunol. 185 (2010), 3248–3255.
20. Borkowski, T.A., et al. A role for endogenous transforming growth factor beta 1 in Langerhans cell biology: the skin of transforming growth factor beta 1 null mice is devoid of epidermal Langerhans cells. J. Exp. Med. 184 (1996), 2417–2422.
21. Travis, M.A., Sheppard, D., TGF-beta activation and function in immunity. Annu. Rev. Immunol. 32 (2014), 51–82.
22. Mohammed, J., et al. Stromal cells control the epithelial residence of DCs and memory T cells by regulated activation of TGF-beta. Nat. Immunol. 17 (2016), 414–421.
23. Fainaru, O., et al. Runx3 regulates mouse TGF-beta-mediated dendritic cell function and its absence results in airway inflammation. EMBO J. 23 (2004), 969–979.
24. Hacker, C., et al. Transcriptional profiling identifies Id2 function in dendritic cell development. Nat. Immunol. 4 (2003), 380–386.
25. Chopin, M., et al. Langerhans cells are generated by two distinct PU.1-dependent transcriptional networks. J. Exp. Med. 210 (2013), 2967–2980.
26. Sparber, F., et al. The late endosomal adaptor molecule p14 (LAMTOR2) represents a novel regulator of Langerhans cell homeostasis. Blood 123 (2014), 217–227.
27. Sparber, F., et al. The late endosomal adaptor molecule p14 (LAMTOR2) regulates TGFbeta1-mediated homeostasis of Langerhans cells. J. Invest. Dermatol. 135 (2015), 119–129.
28. Li, G., et al. TGF-beta1-Smad signaling pathways are not required for epidermal LC homeostasis. Oncotarget 7 (2016), 15290–15291.
29. Xu, Y.P., et al. TGFbeta/Smad3 signal pathway is not required for epidermal Langerhans cell development. J. Invest. Dermatol. 132 (2012), 2106–2109.
30. Zhang, Y.E., Non-Smad signaling pathways of the TGF-beta family. Cold Spring Harb. Perspect. Biol., 9, 2017, 10.1101/cshperspect.a022129.
31. Yasmin, N., et al. Identification of bone morphogenetic protein 7 (BMP7) as an instructive factor for human epidermal Langerhans cell differentiation. J. Exp. Med. 210 (2013), 2597–2610.
32. Wang, Y., et al. IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat. Immunol. 13 (2012), 753–760.
33. Wang, Y., et al. Nonredundant roles of keratinocyte-derived IL-34 and neutrophil-derived CSF1 in Langerhans cell renewal in the steady state and during inflammation. Eur. J. Immunol. 46 (2016), 552–559.
34. Sere, K., et al. Two distinct types of Langerhans cells populate the skin during steady state and inflammation. Immunity 37 (2012), 905–916.
35. Ginhoux, F., et al. Langerhans cells arise from monocytes in vivo. Nat. Immunol. 7 (2006), 265–273.
36. Nagao, K., et al. Stress-induced production of chemokines by hair follicles regulates the trafficking of dendritic cells in skin. Nat. Immunol. 13 (2012), 744–752.
37. van de Laar, L., et al. Yolk sac macrophages, fetal liver, and adult monocytes can colonize an empty niche and develop into functional tissue-resident macrophages. Immunity 44 (2016), 755–768.
38. Capucha, T., et al. Distinct murine mucosal Langerhans cell subsets develop from pre-dendritic cells and monocytes. Immunity 43 (2015), 369–381.
39. + blood dendritic cells have Langerhans cell potential. Blood 125 (2015), 470–473.
40. Martinez-Cingolani, C., et al. Human blood BDCA-1 dendritic cells differentiate into Langerhans-like cells with thymic stromal lymphopoietin and TGF-beta. Blood 124 (2014), 2411–2420.
41. Tang, A., et al. Adhesion of epidermal Langerhans cells to keratinocytes mediated by E-cadherin. Nature 361 (1993), 82–85.
42. Schuler, G., Steinman, R.M., Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J. Exp. Med. 161 (1985), 526–546.
43. Ratzinger, G., et al. Matrix metalloproteinases 9 and 2 are necessary for the migration of Langerhans cells and dermal dendritic cells from human and murine skin. J. Immunol. 168 (2002), 4361–4371.
44. Kabashima, K., et al. CXCL12-CXCR4 engagement is required for migration of cutaneous dendritic cells. Am. J. Pathol. 171 (2007), 1249–1257.
45. Tal, O., et al. DC mobilization from the skin requires docking to immobilized CCL21 on lymphatic endothelium and intralymphatic crawling. J. Exp. Med. 208 (2011), 2141–2153.
46. Ohl, L., et al. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21 (2004), 279–288.
47. Kissenpfennig, A., et al. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 22 (2005), 643–654.
48. Tomura, M., et al. Tracking and quantification of dendritic cell migration and antigen trafficking between the skin and lymph nodes. Sci. Rep., 4, 2014, 6030.
49. Shih, V.F., et al. Control of RelB during dendritic cell activation integrates canonical and noncanonical NF-kappaB pathways. Nat. Immunol. 13 (2012), 1162–1170.
50. Baratin, M., et al. Homeostatic NF-kappaB signaling in steady-state migratory dendritic cells regulates immune homeostasis and tolerance. Immunity 42 (2015), 627–639.
51. Shklovskaya, E., et al. Langerhans cells are precommitted to immune tolerance induction. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 18049–18054.
52. Cumberbatch, M., et al. Langerhans cells require signals from both tumour necrosis factor-alpha and interleukin-1 beta for migration. Immunology 92 (1997), 388–395.
53. Cumberbatch, M., et al. Interleukin (IL)-18 induces Langerhans cell migration by a tumour necrosis factor-alpha- and IL-1beta-dependent mechanism. Immunology 102 (2001), 323–330.
54. Cumberbatch, M., et al. Differential regulation of epidermal Langerhans ​cell migration by interleukins (IL)-1alpha and IL-1beta during irritant- and allergen-induced cutaneous immune responses. Toxicol. Appl. Pharmacol. 182 (2002), 126–135.
55. Haley, K., et al. Langerhans cells require MyD88-dependent signals for Candida albicans response but not for contact hypersensitivity or migration. J. Immunol. 188 (2012), 4334–4339.
56. Wilson, N.S., Villadangos, J.A., Lymphoid organ dendritic cells: beyond the Langerhans cells paradigm. Immunol. Cell Biol. 82 (2004), 91–98.
57. + dendritic cells. Nat. Immunol. 10 (2009), 488–495.
58. Kaplan, D.H., et al. Epidermal Langerhans ​cell-deficient mice develop enhanced contact hypersensitivity. Immunity 23 (2005), 611–620.
59. Bennett, C.L., et al. Inducible ablation of mouse Langerhans cells diminishes but fails to abrogate contact hypersensitivity. J. Cell Biol. 169 (2005), 569–576.
60. Kaplan, D.H., et al. Insights into Langerhans cell function from Langerhans cell ablation models. Eur. J. Immunol. 38 (2008), 2369–2376.
61. Nakajima, S., et al. Langerhans cells are critical in epicutaneous sensitization with protein antigen via thymic stromal lymphopoietin receptor signaling. J. Allergy Clin. Immunol., 129, 2012 1048–1055 e1046.
62. Kaplan, D.H., In vivo function of Langerhans cells and dermal dendritic cells. Trends Immunol. 31 (2010), 446–451.
63. Kumamoto, Y., et al. MGL2 Dermal dendritic cells are sufficient to initiate contact hypersensitivity in vivo. PLoS One, 4, 2009, e5619.
64. Elias, P.M., Stratum corneum defensive functions: an integrated view. J. Invest. Dermatol. 125 (2005), 183–200.
65. Furuse, M., et al. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J. Cell Biol. 156 (2002), 1099–1111.
66. Kubo, A., et al. The stratum corneum comprises three layers with distinct metal-ion barrier properties. Sci. Rep., 3, 2013, 1731.
67. Kubo, A., et al. External antigen uptake by Langerhans cells with reorganization of epidermal tight junction barriers. J. Exp. Med. 206 (2009), 2937–2946.
68. Ouchi, T., et al. Langerhans cell antigen capture through tight junctions confers preemptive immunity in experimental staphylococcal scalded skin syndrome. J. Exp. Med. 208 (2011), 2607–2613.
69. Nishioka, K., et al. Staphylococcal scalded skin syndrome. II. Serum level of anti exfoliatin and anti alpha-toxin in patients with staphylococcal scalded skin syndrome or bullous impetigo. J. Dermatol. 4 (1977), 65–68.
70. Yao, C., et al. Skin dendritic cells induce follicular helper T cells and protective humoral immune responses. J. Allergy Clin. Immunol., 136, 2015 1387–1397.e1–7.
71. Kawasaki, H., et al. Altered stratum corneum barrier and enhanced percutaneous immune responses in filaggrin-null mice. J. Allergy Clin. Immunol., 129, 2012 1538–1546.e6.
72. Kobayashi, T., et al. Dysbiosis and Staphylococcus aureus colonization drives inflammation in atopic dermatitis. Immunity 42 (2015), 756–766.
73. Kashem, S.W., Kaplan, D.H., Skin immunity to Candida albicans. Trends Immunol. 37 (2016), 440–450.
74. Igyarto, B.Z., et al. Skin-resident murine dendritic cell subsets promote distinct and opposing antigen-specific T helper cell responses. Immunity 35 (2011), 260–272.
75. Kashem, S.W., et al. Candida albicans morphology and dendritic cell subsets determine T helper cell differentiation. Immunity 42 (2015), 356–366.
76. Singh, T.P., et al. Monocyte-derived inflammatory Langerhans cells and dermal dendritic cells mediate psoriasis-like inflammation. Nat. Commun., 7, 2016, 13581.
77. Yoshiki, R., et al. IL-23 from Langerhans cells is required for the development of imiquimod-induced psoriasis-like dermatitis by induction of IL-17A-producing gammadelta T cells. J. Invest. Dermatol. 134 (2014), 1912–1921.
78. Kautz-Neu, K., et al. Langerhans cells are negative regulators of the anti-Leishmania response. J. Exp. Med. 208 (2011), 885–891.
79. Gomez de Aguero, M., et al. Langerhans cells protect from allergic contact dermatitis in mice by tolerizing CD8(+) T cells and activating Foxp3(+) regulatory T cells. J. Clin. Invest. 122 (2012), 1700–1711.
80. + T cells while Langerhans cells induce cross-tolerance. EMBO Mol. Med. 6 (2014), 1191–1204.
81. Price, J.G., et al. CDKN1A regulates Langerhans cell survival and promotes Treg cell generation upon exposure to ionizing irradiation. Nat. Immunol. 16 (2015), 1060–1068.
82. Idoyaga, J., et al. Specialized role of migratory dendritic cells in peripheral tolerance induction. J. Clin. Invest. 123 (2013), 844–854.
83. Tobin, D.J., A possible role for Langerhans cells in the removal of melanin from early catagen hair follicles. Br. J. Dermatol. 138 (1998), 795–798.
84. Kawamura, T., et al. Severe dermatitis with loss of epidermal Langerhans cells in human and mouse zinc deficiency. J. Clin. Invest. 122 (2012), 722–732.
85. + macrophages or monocyte-derived dendritic cells. Immunity 45 (2016), 1205–1218.
86. Wu, X., et al. Mafb lineage tracing to distinguish macrophages from other immune lineages reveals dual identity of Langerhans cells. J. Exp. Med. 213 (2016), 2553–2565.
87. Ribeiro, C.M., et al. Receptor usage dictates HIV-1 restriction by human TRIM5alpha in dendritic cell subsets. Nature 540 (2016), 448–452.