Establishing and maintaining the Langerhans cell network

Seminars in Cell and Developmental Biology

Volumn 41, Issue , 2015, Pages 23-29

  Chopin, Michaël ^a,b   Nutt, Stephen L ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Dendritic cell; ID2; Langerhans cell; PU.1; RUNX3; Transcription factor

Indexed keywords

INHIBITOR OF DIFFERENTIATION 2; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; INTERFERON REGULATORY FACTOR 4; TRANSCRIPTION FACTOR PU 1; TRANSCRIPTION FACTOR RUNX3; TRANSCRIPTION FACTOR;

ANTIGEN PRESENTING CELL; CELL DIFFERENTIATION; DENDRITIC CELL; EMBRYO DEVELOPMENT; EPIDERMIS; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; INFLAMMATION; LANGERHANS CELL; ONTOGENY; REVIEW; SKIN; STEADY STATE; TRANSCRIPTION REGULATION; ANIMAL; BIOLOGICAL MODEL; BONE MARROW CELL; CYTOLOGY; GENE EXPRESSION; GENE REGULATORY NETWORK; GENETICS; IMMUNOLOGY; METABOLISM;

ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; EPIDERMIS; GENE EXPRESSION; GENE REGULATORY NETWORKS; HUMANS; LANGERHANS CELLS; MODELS, IMMUNOLOGICAL; TRANSCRIPTION FACTORS;

EID: 84931564853     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2014.02.001     Document Type: Review

References (88)

1. Birnberg T., Bar-On L., Sapoznikov A., Caton M.L., Cervantes-Barragan L., Makia D., et al. Lack of conventional dendritic cells is compatible with normal development and T cell homeostasis, but causes myeloid proliferative syndrome. Immunity 2008, 29:986-997.
2. Ohnmacht C., Pullner A., King S.B., Drexler I., Meier S., Brocker T., et al. Constitutive ablation of dendritic cells breaks self-tolerance of CD4 T cells and results in spontaneous fatal autoimmunity. J Exp Med 2009, 206:549-559.
3. Steinman R.M., Witmer M.D. Lymphoid dendritic cells are potent stimulators of the primary mixed leukocyte reaction in mice. Proc Natl Acad Sci U S A 1978, 75:5132-5136.
4. Belz G.T., Nutt S.L. Transcriptional programming of the dendritic cell network. Nat Rev Immunol 2012, 12:101-113.
5. Chopin M., Allan R.S., Belz G.T. Transcriptional regulation of dendritic cell diversity. Front Immunol 2012, 3:26.
6. Birbeck M.S., Breathnach A.S., Everall J.D. An electron microscope study of basal melanocytes and high-level clear cells (Langerhans cells) in vitiligo. J Invest Dermatol 1961, 37:51-63.
7. Wolff K. The fine structure of the Langerhans cell granule. J Cell Biol 1967, 35:468-473.
8. Kissenpfennig A., Ait-Yahia S., Clair-Moninot V., Stossel H., Badell E., Bordat Y., et al. Disruption of the langerin/CD207 gene abolishes Birbeck granules without a marked loss of Langerhans cell function. Mol Cell Biol 2005, 25:88-99.
9. Bennett C.L., van Rijn E., Jung S., Inaba K., Steinman R.M., Kapsenberg M.L., et al. Inducible ablation of mouse Langerhans cells diminishes but fails to abrogate contact hypersensitivity. J Cell Biol 2005, 169:569-576.
10. Kissenpfennig A., Henri S., Dubois B., Laplace-Builhe C., Perrin P., Romani N., et al. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 2005, 22:643-654.
11. Bursch L.S., Wang L., Igyarto B., Kissenpfennig A., Malissen B., Kaplan D.H., et al. Identification of a novel population of Langerin+ dendritic cells. J Exp Med 2007, 204:3147-3156.
12. Ginhoux F., Collin M.P., Bogunovic M., Abel M., Leboeuf M., Helft J., et al. Blood-derived dermal langerin+ dendritic cells survey the skin in the steady state. J Exp Med 2007, 204:3133-3146.
13. Poulin L.F., Henri S., de Bovis B., Devilard E., Kissenpfennig A., Malissen B. The dermis contains langerin+ dendritic cells that develop and function independently of epidermal Langerhans cells. J Exp Med 2007, 204:3119-3131.
14. Nagao K., Ginhoux F., Leitner W.W., Motegi S., Bennett C.L., Clausen B.E., et al. Murine epidermal Langerhans cells and langerin-expressing dermal dendritic cells are unrelated and exhibit distinct functions. Proc Natl Acad Sci U S A 2009, 106:3312-3317.
15. Borkowski T.A., Nelson A.J., Farr A.G., Udey M.C. Expression of gp40, the murine homologue of human epithelial cell adhesion molecule (Ep-CAM), by murine dendritic cells. Eur J Immunol 1996, 26:110-114.
16. Chikwava K., Jaffe R. Langerin (CD207) staining in normal pediatric tissues, reactive lymph nodes, and childhood histiocytic disorders. Pediatr Dev Pathol 2004, 7:607-614.
17. Kaser A., Ludwiczek O., Holzmann S., Moschen A.R., Weiss G., Enrich B., et al. Increased expression of CCL20 in human inflammatory bowel disease. J Clin Immunol 2004, 24:74-85.
18. Qiu C.H., Miyake Y., Kaise H., Kitamura H., Ohara O., Tanaka M. Novel subset of CD8{alpha}+ dendritic cells localized in the marginal zone is responsible for tolerance to cell-associated antigens. J Immunol 2009, 182:4127-4136.
19. Chorro L., Geissmann F. Development and homeostasis of 'resident' myeloid cells: the case of the Langerhans cell. Trends Immunol 2010, 31:438-445.
20. Ginhoux F., Merad M. Ontogeny and homeostasis of Langerhans cells. Immunol Cell Biol 2010, 88:387-392.
21. Frelinger J.G., Hood L., Hill S., Frelinger J.A. Mouse epidermal Ia molecules have a bone marrow origin. Nature 1979, 282:321-323.
22. Katz S.I., Tamaki K., Sachs D.H. Epidermal Langerhans cells are derived from cells originating in bone marrow. Nature 1979, 282:324-326.
23. Merad M., Ginhoux F., Collin M. Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat Rev Immunol 2008, 8:935-947.
24. Merad M., Hoffmann P., Ranheim E., Slaymaker S., Manz M.G., Lira S.A., et al. Depletion of host Langerhans cells before transplantation of donor alloreactive T cells prevents skin graft-versus-host disease. Nat Med 2004, 10:510-517.
25. Merad M., Manz M.G., Karsunky H., Wagers A., Peters W., Charo I., et al. Langerhans cells renew in the skin throughout life under steady-state conditions. Nat Immunol 2002, 3:1135-1141.
26. Kanitakis J., Petruzzo P., Dubernard J.M. Turnover of epidermal Langerhans' cells. N Engl J Med 2004, 351:2661-2662.
27. Hoeffel G., Wang Y., Greter M., See P., Teo P., Malleret B., et al. Adult Langerhans cells derive predominantly from embryonic fetal liver monocytes with a minor contribution of yolk sac-derived macrophages. J Exp Med 2012, 209:1167-1181.
28. Chorro L., Sarde A., Li M., Woollard K.J., Chambon P., Malissen B., et al. Langerhans cell (LC) proliferation mediates neonatal development, homeostasis, and inflammation-associated expansion of the epidermal LC network. J Exp Med 2009, 206:3089-3100.
29. Tripp C.H., Chang-Rodriguez S., Stoitzner P., Holzmann S., Stossel H., Douillard P., et al. Ontogeny of Langerin/CD207 expression in the epidermis of mice. J Invest Dermatol 2004, 122:670-672.
30. Ghigo C., Mondor I., Jorquera A., Nowak J., Wienert S., Zahner S.P., et al. Multicolor fate mapping of Langerhans cell homeostasis. J Exp Med 2013, 210:1657-1664.
31. Geissmann F., Prost C., Monnet J.P., Dy M., Brousse N., Hermine O. Transforming growth factor beta1, in the presence of granulocyte/macrophage colony-stimulating factor and interleukin 4, induces differentiation of human peripheral blood monocytes into dendritic Langerhans cells. J Exp Med 1998, 187:961-966.
32. Ginhoux F., Tacke F., Angeli V., Bogunovic M., Loubeau M., Dai X.M., et al. Langerhans cells arise from monocytes in vivo. Nat Immunol 2006, 7:265-273.
33. Nagao K., Kobayashi T., Moro K., Ohyama M., Adachi T., Kitashima D.Y., et al. Stress-induced production of chemokines by hair follicles regulates the trafficking of dendritic cells in skin. Nat Immunol 2012, 13:744-752.
34. McKenna H.J., Stocking K.L., Miller R.E., Brasel K., De Smedt T., Maraskovsky E., et al. Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood 2000, 95:3489-3497.
35. Tussiwand R., Onai N., Mazzucchelli L., Manz M.G. Inhibition of natural type I IFN-producing and dendritic cell development by a small molecule receptor tyrosine kinase inhibitor with Flt3 affinity. J Immunol 2005, 175:3674-3680.
36. Waskow C., Liu K., Darrasse-Jeze G., Guermonprez P., Ginhoux F., Merad M., et al. The receptor tyrosine kinase Flt3 is required for dendritic cell development in peripheral lymphoid tissues. Nat Immunol 2008, 9:676-683.
37. Onai N., Obata-Onai A., Schmid M.A., Manz M.G. Flt3 in regulation of type I interferon-producing cell and dendritic cell development. Ann NY Acad Sci 2007, 1106:253-261.
38. Borkowski T.A., Letterio J.J., Farr A.G., Udey M.C. 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 1996, 184:2417-2422.
39. Witmer-Pack M.D., Hughes D.A., Schuler G., Lawson L., McWilliam A., Inaba K., et al. Identification of macrophages and dendritic cells in the osteopetrotic (op/op) mouse. J Cell Sci 1993, 104(Pt 4):1021-1029.
40. Greter M., Lelios I., Pelczar P., Hoeffel G., Price J., Leboeuf M., et al. Stroma-derived interleukin-34 controls the development and maintenance of Langerhans cells and the maintenance of microglia. Immunity 2012, 37:1050-1060.
41. Wang Y., Szretter K.J., Vermi W., Gilfillan S., Rossini C., Cella M., et al. IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat Immunol 2012, 13:753-760.
42. van Amerongen R., Nusse R. Towards an integrated view of Wnt signaling in development. Development 2009, 3205-3214.
43. Logan C.Y., Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 2004, 20:781-810.
44. Macdonald B.T., Semenov M.V., He X., SnapShot: 1. Wnt/beta-catenin signaling. Cell 2007, 131:1204.
45. Blauvelt A., Katz S.I., Udey M.C. Human Langerhans cells express E-cadherin. J Invest Dermatol 1995, 104:293-296.
46. Tang A., Amagai M., Granger L.G., Stanley J.R., Udey M.C. Adhesion of epidermal Langerhans cells to keratinocytes mediated by E-cadherin. Nature 1993, 361:82-85.
47. Riedl E., Stockl J., Majdic O., Scheinecker C., Rappersberger K., Knapp W., et al. Functional involvement of E-cadherin in TGF-beta 1-induced cell cluster formation of in vitro developing human Langerhans-type dendritic cells. J Immunol 2000, 165:1381-1386.
48. Yasmin N., Konradi S., Eisenwort G., Schichl Y.M., Seyerl M., Bauer T., et al. beta-Catenin promotes the differentiation of epidermal Langerhans dendritic cells. J Invest Dermatol 2013, 133:1250-1259.
49. Yamashita T., Budhu A., Forgues M., Wang X.W. Activation of hepatic stem cell marker EpCAM by Wnt-beta-catenin signaling in hepatocellular carcinoma. Cancer Res 2007, 67:10831-10839.
50. Becker M.R., Choi Y.S., Millar S.E., Udey M.C. Wnt signaling influences the development of murine epidermal Langerhans cells. J Invest Dermatol 2011, 131:1861-1868.
51. Engel I., Murre C. The function of E- and Id proteins in lymphocyte development. Nat Rev Immunol 2001, 1:193-199.
52. Ginhoux F., Liu K., Helft J., Bogunovic M., Greter M., Hashimoto D., et al. The origin and development of nonlymphoid tissue CD103+ DCs. J Exp Med 2009, 206:2115-2130.
53. Hacker C., Kirsch R.D., Ju X.S., Hieronymus T., Gust T.C., Kuhl C., et al. Transcriptional profiling identifies Id2 function in dendritic cell development. Nat Immunol 2003, 4:380-386.
54. Sere K., Baek J.H., Ober-Blobaum J., Muller-Newen G., Tacke F., Yokota Y., et al. Two distinct types of Langerhans cells populate the skin during steady state and inflammation. Immunity 2012, 37:905-916.
55. Chopin M., Seillet C., Chevrier S., Wu L., Wang H., Morse H.C., et al. Langerhans cells are generated by two distinct PU. 1-dependent transcriptional networks. Journal of Experimental Medicine 2013, 210:2967-2980.
56. Collins A., Littman D.R., Taniuchi I. RUNX proteins in transcription factor networks that regulate T-cell lineage choice. Nat Rev Immunol 2009, 9:106-115.
57. Fainaru O., Woolf E., Lotem J., Yarmus M., Brenner O., Goldenberg D., et al. Runx3 regulates mouse TGF-beta-mediated dendritic cell function and its absence results in airway inflammation. EMBO J 2004, 23:969-979.
58. Holtschke T., Lohler J., Kanno Y., Fehr T., Giese N., Rosenbauer F., et al. Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene. Cell 1996, 87:307-317.
59. Schiavoni G., Mattei F., Sestili P., Borghi P., Venditti M., Morse H.C., et al. ICSBP is essential for the development of mouse type I interferon-producing cells and for the generation and activation of CD8alpha(+) dendritic cells. J Exp Med 2002, 196:1415-1425.
60. Schiavoni G., Mattei F., Borghi P., Sestili P., Venditti M., Morse H.C., et al. ICSBP is critically involved in the normal development and trafficking of Langerhans cells and dermal dendritic cells. Blood 2004, 103:2221-2228.
61. Hashimoto D., Miller J., Merad M. Dendritic cell and macrophage heterogeneity in vivo. Immunity 2011, 35:323-335.
62. Hambleton S., Salem S., Bustamante J., Bigley V., Boisson-Dupuis S., Azevedo J., et al. IRF8 mutations and human dendritic-cell immunodeficiency. N Engl J Med 2011, 365:127-138.
63. Shaffer A.L., Emre N.C., Romesser P.B., Staudt L.M. IRF4: immunity. malignancy! Therapy?. Clin Cancer Res 2009, 15:2954-2961.
64. Bajana S., Roach K., Turner S., Paul J., Kovats S. IRF4 promotes cutaneous dendritic cell migration to lymph nodes during homeostasis and inflammation. J Immunol 2012, 189:3368-3377.
65. Suzuki S., Honma K., Matsuyama T., Suzuki K., Toriyama K., Akitoyo I., et al. Critical roles of interferon regulatory factor 4 in CD11bhighCD8alpha-dendritic cell development. Proc Natl Acad Sci U S A 2004, 101:8981-8986.
66. Dakic A., Wu L., Nutt S.L. Is PU.1 a dosage-sensitive regulator of haemopoietic lineage commitment and leukaemogenesis?. Trends Immunol 2007, 28:108-114.
67. Carotta S., Dakic A., D'Amico A., Pang S.H., Greig K.T., Nutt S.L., et al. The transcription factor PU.1 controls dendritic cell development and Flt3 cytokine receptor expression in a dose-dependent manner. Immunity 2010, 32:628-641.
68. Heinz L.X., Platzer B., Reisner P.M., Jorgl A., Taschner S., Gobel F., et al. Differential involvement of PU.1 and Id2 downstream of TGF-beta1 during Langerhans-cell commitment. Blood 2006, 107:1445-1453.
69. Iwama A., Osawa M., Hirasawa R., Uchiyama N., Kaneko S., Onodera M., et al. Reciprocal roles for CCAAT/enhancer binding protein (C/EBP) and PU.1 transcription factors in Langerhans cell commitment. J Exp Med 2002, 195:547-558.
70. Mullen A.C., Orlando D.A., Newman J.J., Loven J., Kumar R.M., Bilodeau S., et al. Master transcription factors determine cell-type-specific responses to TGF-beta signaling. Cell 2011, 147:565-576.
71. Romani N., Brunner P.M., Stingl G. Changing views of the role of Langerhans cells. J Invest Dermatol 2012, 132:872-881.
72. Steinman R.M., Gutchinov B., Witmer M.D., Nussenzweig M.C. Dendritic cells are the principal stimulators of the primary mixed leukocyte reaction in mice. J Exp Med 1983, 157:613-627.
73. Schuler G., Steinman R.M. Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J Exp Med 1985, 161:526-546.
74. Allan R.S., Smith C.M., Belz G.T., van Lint A.L., Wakim L.M., Heath W.R., et al. Epidermal viral immunity induced by CD8alpha+ dendritic cells but not by Langerhans cells. Science 2003, 301:1925-1928.
75. Zhao X., Deak E., Soderberg K., Linehan M., Spezzano D., Zhu J., et al. Vaginal submucosal dendritic cells, but not Langerhans cells, induce protective Th1 responses to herpes simplex virus-2. J Exp Med 2003, 197:153-162.
76. He Y., Zhang J., Donahue C., Falo L.D. Skin-derived dendritic cells induce potent CD8(+) T cell immunity in recombinant lentivector-mediated genetic immunization. Immunity 2006, 24:643-656.
77. Bursch L.S., Rich B.E., Hogquist K.A. Langerhans cells are not required for the CD8 T cell response to epidermal self-antigens. J Immunol 2009, 182:4657-4664.
78. Bedoui S., Whitney P.G., Waithman J., Eidsmo L., Wakim L., Caminschi I., et al. Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat Immunol 2009, 10:488-495.
79. Henri S., Poulin L.F., Tamoutounour S., Ardouin L., Guilliams M., de Bovis B., et al. CD207+ CD103+ dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells. J Exp Med 2010, 207:189-206.
80. Obhrai J.S., Oberbarnscheidt M., Zhang N., Mueller D.L., Shlomchik W.D., Lakkis F.G., et al. Langerhans cells are not required for efficient skin graft rejection. J Invest Dermatol 2008, 128:1950-1955.
81. Kaplan D.H., Jenison M.C., Saeland S., Shlomchik W.D., Shlomchik M.J. Epidermal langerhans cell-deficient mice develop enhanced contact hypersensitivity. Immunity 2005, 23:611-620.
82. Igyarto B.Z., Haley K., Ortner D., Bobr A., Gerami-Nejad M., Edelson B.T., et al. Skin-resident murine dendritic cell subsets promote distinct and opposing antigen-specific T helper cell responses. Immunity 2011, 35:260-272.
83. van der Aar A.M., Picavet D.I., Muller F.J., de Boer L., van Capel T.M., Zaat S.A., et al. Langerhans cells favor skin flora tolerance through limited presentation of bacterial antigens and induction of regulatory T cells. J Invest Dermatol 2013, 133:1240-1249.
84. Bobr A., Olvera-Gomez I., Igyarto B.Z., Haley K.M., Hogquist K.A., Kaplan D.H. Acute ablation of Langerhans cells enhances skin immune responses. J Immunol 2010, 185:4724-4728.
85. Shklovskaya E., Roediger B. Fazekas de St Groth B. Epidermal and dermal dendritic cells display differential activation and migratory behavior while sharing the ability to stimulate CD4+ T cell proliferation in vivo. J Immunol 2008, 181:418-430.
86. Shklovskaya E., O'Sullivan B.J., Ng L.G., Roediger B., Thomas R., Weninger W., et al. Langerhans cells are precommitted to immune tolerance induction. Proc Natl Acad Sci U S A 2011, 108:18049-18054.
87. Ouchi T., Kubo A., Yokouchi M., Adachi T., Kobayashi T., Kitashima D.Y., et al. Langerhans cell antigen capture through tight junctions confers preemptive immunity in experimental staphylococcal scalded skin syndrome. J Exp Med 2011, 208:2607-2613.
88. Seneschal J., Clark R.A., Gehad A., Baecher-Allan C.M., Kupper T.S. Human epidermal Langerhans cells maintain immune homeostasis in skin by activating skin resident regulatory T cells. Immunity 2012, 36:873-884.