The clash of Langerhans cell homeostasis in skin: Should I stay or should I go?

Seminars in Cell and Developmental Biology

Volumn 41, Issue , 2015, Pages 30-38

  Hieronymus, Thomas ^a   Zenke, Martin ^a   Baek, Jea Hyun ^b   Seré, Kristin ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Dendritic cell; Epithelial to mesenchymal transition; Langerhans cell; Met signalling; Receptor tyrosine kinase; TGF signalling

Indexed keywords

CD135 ANTIGEN; COLONY STIMULATING FACTOR 1; PROTEIN TYROSINE KINASE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

CELL ADHESION; CELL MATURATION; CELL MIGRATION; EPITHELIAL MESENCHYMAL TRANSITION; HOMEOSTASIS; HUMAN; LANGERHANS CELL; LIFE CYCLE; NONHUMAN; ONTOGENY; REVIEW; SKIN; TUMOR INVASION; WOUND HEALING; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; HEMATOPOIETIC STEM CELL; IMMUNOLOGY; METABOLISM;

MUS;

CELL ADHESION; CELL DIFFERENTIATION; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; HEMATOPOIETIC STEM CELLS; HOMEOSTASIS; HUMANS; LANGERHANS CELLS; RECEPTOR PROTEIN-TYROSINE KINASES; SKIN;

EID: 84931564512     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2014.02.009     Document Type: Review

References (105)

1. Steinman R.M., Hawiger D., Nussenzweig M.C. Tolerogenic dendritic cells. Annu Rev Immunol 2003, 21:685-711.
2. 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.
3. Romani N., Clausen B.E., Stoitzner P. Langerhans cells and more: langerin-expressing dendritic cell subsets in the skin. Immunol Rev 2010, 234:120-141.
4. Kaplan D.H. In vivo function of Langerhans cells and dermal dendritic cells. Trends Immunol 2010, 31:446-451.
5. Shortman K., Naik S.H. Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 2007, 7:19-30.
6. Merad M., Sathe P., Helft J., Miller J., Mortha A. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu Rev Immunol 2013, 31:563-604.
7. Schmid M.A., Kingston D., Boddupalli S., Manz M.G. Instructive cytokine signals in dendritic cell lineage commitment. Immunol Rev 2010, 234:32-44.
8. Fogg D.K., Sibon C., Miled C., Jung S., Aucouturier P., Littman D.R., et al. A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 2006, 311:83-87.
9. 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.
10. Auffray C., Fogg D.K., Narni-Mancinelli E., Senechal B., Trouillet C., Saederup N., et al. CX3CR1+ CD115+ CD135+ common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J Exp Med 2009, 206:595-606.
11. Liu K., Victora G.D., Schwickert T.A., Guermonprez P., Meredith M.M., Yao K., et al. In vivo analysis of dendritic cell development and homeostasis. Science 2009, 324:392-397.
12. Naik S.H., Sathe P., Park H.Y., Metcalf D., Proietto A.I., Dakic A., et al. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat Immunol 2007, 8:1217-1226.
13. Onai N., Obata-Onai A., Schmid M.A., Ohteki T., Jarrossay D., Manz M.G. Identification of clonogenic common Flt3+ M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat Immunol 2007, 8:1207-1216.
14. Zenke M., Hieronymus T. Towards an understanding of the transcription factor network of dendritic cell development. Trends Immunol 2006, 27:140-145.
15. Chorro L., Geissmann F. Development and homeostasis of 'resident' myeloid cells: the case of the Langerhans cell. Trends Immunol 2010, 31:438-445.
16. Belz G.T., Nutt S.L. Transcriptional programming of the dendritic cell network. Nat Rev Immunol 2012, 12:101-113.
17. Langerhans P. Über die Nerven der menschlichen Haut. Virchows Arch 1868, 44:325-337.
18. Katz S.I., Tamaki K., Sachs D.H. Epidermal Langerhans cells are derived from cells originating in bone marrow. Nature 1979, 282:324-326.
19. Frelinger J.G., Hood L., Hill S., Frelinger J.A. Mouse epidermal Ia molecules have a bone marrow origin. Nature 1979, 282:321-323.
20. Schuler G., Steinman R.M. Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J Exp Med 1985, 161:526-546.
21. Villadangos J.A., Schnorrer P. Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat Rev Immunol 2007, 7:543-555.
22. 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.
23. 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.
24. Chang-Rodriguez S., Hoetzenecker W., Schwarzler C., Biedermann T., Saeland S., Elbe-Burger A. Fetal and neonatal murine skin harbors Langerhans cell precursors. J Leukoc Biol 2005, 77:352-360.
25. 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.
26. Schuster C., Vaculik C., Fiala C., Meindl S., Brandt O., Imhof M., et al. HLA-DR+ leukocytes acquire CD1 antigens in embryonic and fetal human skin and contain functional antigen-presenting cells. J Exp Med 2009, 206:169-181.
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. Schulz C., Gomez Perdiguero E., Chorro L., Szabo-Rogers H., Cagnard N., Kierdorf K., et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 2012, 336:86-90.
29. 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.
30. 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.
31. 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.
32. 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. J Exp Med 2013, 210:2967-2980.
33. 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.
34. Metcalf D. Hematopoietic cytokines. Blood 2008, 111:485-491.
35. Karsunky H., Merad M., Cozzio A., Weissman I.L., Manz M.G. Flt3 ligand regulates dendritic cell development from Flt3+ lymphoid and myeloid-committed progenitors to Flt3+ dendritic cells in vivo. J Exp Med 2003, 198:305-313.
36. 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, 206:3115-3130.
37. Kingston D., Schmid M.A., Onai N., Obata-Onai A., Baumjohann D., Manz M.G. The concerted action of GM-CSF and Flt3-ligand on in vivo dendritic cell homeostasis. Blood 2009, 114:835-843.
38. Manning G., Whyte D.B., Martinez R., Hunter T., Sudarsanam S. The protein kinase complement of the human genome. Science 2002, 298:1912-1934.
39. Caenepeel S., Charydczak G., Sudarsanam S., Hunter T., Manning G. The mouse kinome: discovery and comparative genomics of all mouse protein kinases. Proc Natl Acad Sci USA 2004, 101:11707-11712.
40. Moustakas A., Heldin C.H. The regulation of TGFbeta signal transduction. Development 2009, 136:3699-3714.
41. Massague J. TGFbeta signalling in context. Nat Rev 2012, 13:616-630.
42. Fortunel N.O., Hatzfeld A., Hatzfeld J.A. Transforming growth factor-beta: pleiotropic role in the regulation of hematopoiesis. Blood 2000, 96:2022-2036.
43. Li M.O., Wan Y.Y., Sanjabi S., Robertson A.K., Flavell R.A. Transforming growth factor-beta regulation of immune responses. Annu Rev Immunol 2006, 24:99-146.
44. Chabanon A., Desterke C., Rodenburger E., Clay D., Guerton B., Boutin L., et al. A cross-talk between stromal cell-derived factor-1 and transforming growth factor-beta controls the quiescence/cycling switch of CD34(+) progenitors through FoxO3 and mammalian target of rapamycin. Stem Cells 2008, 26:3150-3161.
45. Karlsson G., Blank U., Moody J.L., Ehinger M., Singbrant S., Deng C.X., et al. Smad4 is critical for self-renewal of hematopoietic stem cells. J Exp Med 2007, 204:467-474.
46. Challen G.A., Boles N.C., Chambers S.M., Goodell M.A. Distinct hematopoietic stem cell subtypes are differentially regulated by TGF-beta1. Cell Stem Cell 2010, 6:265-278.
47. Kee B.L., Rivera R.R., Murre C. Id3 inhibits B lymphocyte progenitor growth and survival in response to TGF-beta. Nat Immunol 2001, 2:242-247.
48. Sere K.M., Lin Q., Felker P., Rehage N., Klisch T., Ortseifer I., et al. Dendritic cell lineage commitment is instructed by distinct cytokine signals. Eur J Cell Biol 2012, 91:515-523.
49. Felker P., Sere K., Lin Q., Becker C., Hristov M., Hieronymus T., et al. TGF-beta1 accelerates dendritic cell differentiation from common dendritic cell progenitors and directs subset specification toward conventional dendritic cells. J Immunol 2010, 185:5326-5335.
50. 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.
51. Kaplan D.H., Li M.O., Jenison M.C., Shlomchik W.D., Flavell R.A., Shlomchik M.J. Autocrine/paracrine TGFbeta1 is required for the development of epidermal Langerhans cells. J Exp Med 2007, 204:2545-2552.
52. Kel J.M., Girard-Madoux M.J., Reizis B., Clausen B.E. TGF-beta is required to maintain the pool of immature Langerhans cells in the epidermis. J Immunol 2010, 185:3248-3255.
53. Bobr A., Igyarto B.Z., Haley K.M., Li M.O., Flavell R.A., Kaplan D.H. Autocrine/paracrine TGF-beta1 inhibits Langerhans cell migration. Proc Natl Acad Sci USA 2012, 109:10492-10497.
54. Alvarez D., Vollmann E.H., von Andrian U.H. Mechanisms and consequences of dendritic cell migration. Immunity 2008, 29:325-342.
55. Yasmin N., Bauer T., Modak M., Wagner K., Schuster C., Koffel R., et al. Identification of bone morphogenetic protein 7 (BMP7) as an instructive factor for human epidermal Langerhans cell differentiation. J Exp Med 2013, 210:2597-2610.
56. Lemmon M.A., Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010, 141:1117-1134.
57. Hume D.A., MacDonald K.P. Therapeutic applications of macrophage colony-stimulating factor-1 (CSF-1) and antagonists of CSF-1 receptor (CSF-1R) signaling. Blood 2011, 119:1810-1820.
58. Lichanska A.M., Browne C.M., Henkel G.W., Murphy K.M., Ostrowski M.C., McKercher S.R., et al. Differentiation of the mononuclear phagocyte system during mouse embryogenesis: the role of transcription factor PU.1. Blood 1999, 94:127-138.
59. Mossadegh-Keller N., Sarrazin S., Kandalla P.K., Espinosa L., Stanley E.R., Nutt S.L., et al. M-CSF instructs myeloid lineage fate in single haematopoietic stem cells. Nature 2013, 497:239-243.
60. Lin H., Lee E., Hestir K., Leo C., Huang M., Bosch E., et al. Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science 2008, 320:807-811.
61. Wei S., Nandi S., Chitu V., Yeung Y.G., Yu W., Huang M., et al. Functional overlap but differential expression of CSF-1 and IL-34 in their CSF-1 receptor-mediated regulation of myeloid cells. J Leukoc Biol 2010, 88:495-505.
62. Chihara T., Suzu S., Hassan R., Chutiwitoonchai N., Hiyoshi M., Motoyoshi K., et al. IL-34 and M-CSF share the receptor Fms but are not identical in biological activity and signal activation. Cell Death Differ 2010, 17:1917-1927.
63. 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.
64. 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.
65. 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, 104:1021-1029.
66. Dai X.M., Ryan G.R., Hapel A.J., Dominguez M.G., Russell R.G., Kapp S., et al. Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 2002, 99:111-120.
67. 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.
68. Forsberg E.C., Serwold T., Kogan S., Weissman I.L., Passegue E. New evidence supporting megakaryocyte-erythrocyte potential of flk2/flt3+ multipotent hematopoietic progenitors. Cell 2006, 126:415-426.
69. MacDonald K.P., Rowe V., Bofinger H.M., Thomas R., Sasmono T., Hume D.A., et al. The colony-stimulating factor 1 receptor is expressed on dendritic cells during differentiation and regulates their expansion. J Immunol 2005, 175:1399-1405.
70. Fancke B., Suter M., Hochrein H., O'Keeffe M. M-CSF: a novel plasmacytoid and conventional dendritic cell poietin. Blood 2008, 111:150-159.
71. Adolfsson J., Mansson R., Buza-Vidas N., Hultquist A., Liuba K., Jensen C.T., et al. Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell 2005, 121:295-306.
72. D'Amico A., Wu L. The early progenitors of mouse dendritic cells and plasmacytoid predendritic cells are within the bone marrow hemopoietic precursors expressing Flt3. J Exp Med 2003, 198:293-303.
73. Bauer T., Zagorska A., Jurkin J., Yasmin N., Koffel R., Richter S., et al. Identification of Axl as a downstream effector of TGF-beta1 during Langerhans cell differentiation and epidermal homeostasis. J Exp Med 2012, 209:2033-2047.
74. Eisenwort G., Jurkin J., Yasmin N., Bauer T., Gesslbauer B., Strobl H. Identification of TROP2 (TACSTD2), an EpCAM-like molecule, as a specific marker for TGF-beta1-dependent human epidermal Langerhans cells. J Invest Dermatol 2011, 131:2049-2057.
75. Konradi S., Yasmin N., Haslwanter D., Weber M., Gesslbauer B., Sixt M., et al. Langerhans cell maturation is accompanied by induction of N-cadherin and the transcriptional regulators of epithelial-mesenchymal transition ZEB1/2. Eur J Immunol 2013, 44:553-560.
76. 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.
77. Trusolino L., Comoglio P.M. Scatter-factor and semaphorin receptors: cell signalling for invasive growth. Nat Rev Cancer 2002, 2:289-300.
78. Birchmeier C., Birchmeier W., Gherardi E., Vande Woude G.F. Met, metastasis, motility and more. Nat Rev 2003, 4:915-925.
79. Kmiecik T.E., Keller J.R., Rosen E., Vande Woude G.F. Hepatocyte growth factor is a synergistic factor for the growth of hematopoietic progenitor cells. Blood 1992, 80:2454-2457.
80. Tesio M., Golan K., Corso S., Giordano S., Schajnovitz A., Vagima Y., et al. Enhanced c-Met activity promotes G-CSF-induced mobilization of hematopoietic progenitor cells via ROS signaling. Blood 2011, 117:419-428.
81. van der Voort R., Taher T.E., Keehnen R.M., Smit L., Groenink M., Pals S.T. Paracrine regulation of germinal center B cell adhesion through the c-met-hepatocyte growth factor/scatter factor pathway. J Exp Med 1997, 185:2121-2131.
82. Gordin M., Tesio M., Cohen S., Gore Y., Lantner F., Leng L., et al. c-Met and its ligand hepatocyte growth factor/scatter factor regulate mature B cell survival in a pathway induced by CD74. J Immunol 2010, 185:2020-2031.
83. Beilmann M., Odenthal M., Jung W., Vande Woude G.F., Dienes H.P., Schirmacher P. Neoexpression of the c-met/hepatocyte growth factor-scatter factor receptor gene in activated monocytes. Blood 1997, 90:4450-4458.
84. Benkhoucha M., Santiago-Raber M.L., Schneiter G., Chofflon M., Funakoshi H., Nakamura T., et al. Hepatocyte growth factor inhibits CNS autoimmunity by inducing tolerogenic dendritic cells and CD25+ Foxp3+ regulatory T cells. Proc Natl Acad Sci USA 2010, 107:6424-6429.
85. Baek J.H., Birchmeier C., Zenke M., Hieronymus T. The HGF receptor/Met tyrosine kinase is a key regulator of dendritic cell migration in skin immunity. J Immunol 2012, 189:1699-1707.
86. Kurz S.M., Diebold S.S., Hieronymus T., Gust T.C., Bartunek P., Sachs M., et al. The impact of c-met/scatter factor receptor on dendritic cell migration. Eur J Immunol 2002, 32:1832-1838.
87. Trusolino L., Bertotti A., Comoglio P.M. MET signalling: principles and functions in development, organ regeneration and cancer. Nat Rev 2010, 11:834-848.
88. Price A.A., Cumberbatch M., Kimber I., Ager A. Alpha 6 integrins are required for Langerhans cell migration from the epidermis. J Exp Med 1997, 186:1725-1735.
89. Ratzinger G., Stoitzner P., Ebner S., Lutz M.B., Layton G.T., Rainer C., 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 2002, 168:4361-4371.
90. Yen J.H., Khayrullina T., Ganea D. PGE2-induced metalloproteinase-9 is essential for dendritic cell migration. Blood 2008, 111:260-270.
91. Lemke G., Rothlin C.V. Immunobiology of the TAM receptors. Nat Rev Immunol 2008, 8:327-336.
92. Linger R.M., Keating A.K., Earp H.S., Graham D.K. TAM receptor tyrosine kinases: biologic functions, signaling, and potential therapeutic targeting in human cancer. Adv Cancer Res 2008, 100:35-83.
93. Gujral T.S., Karp R.L., Finski A., Chan M., Schwartz P.E., MacBeath G., et al. Profiling phospho-signaling networks in breast cancer using reverse-phase protein arrays. Oncogene 2013, 32:3470-3476.
94. Salian-Mehta S., Xu M., Wierman M.E. AXL and MET crosstalk to promote gonadotropin releasing hormone (GnRH) neuronal cell migration and survival. Mol Cell Endocrinol 2013, 374:92-100.
95. Sharif M.N., Sosic D., Rothlin C.V., Kelly E., Lemke G., Olson E.N., et al. Twist mediates suppression of inflammation by type I IFNs and Axl. J Exp Med 2006, 203:1891-1901.
96. Rothlin C.V., Ghosh S., Zuniga E.I., Oldstone M.B., Lemke G. TAM receptors are pleiotropic inhibitors of the innate immune response. Cell 2007, 131:1124-1136.
97. Lemke G., Burstyn-Cohen T. TAM receptors and the clearance of apoptotic cells. Ann N Y Acad Sci 2010, 1209:23-29.
98. Christofori G. New signals from the invasive front. Nature 2006, 441:444-450.
99. Peinado H., Olmeda D., Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?. Nat Rev Cancer 2007, 7:415-428.
100. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
101. Lamouille S., Subramanyam D., Blelloch R., Derynck R. Regulation of epithelial-mesenchymal and mesenchymal-epithelial transitions by microRNAs. Curr Opin Cell Biol 2013, 25:200-207.
102. Goumans M.J., Valdimarsdottir G., Itoh S., Lebrin F., Larsson J., Mummery C., et al. Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFbeta/ALK5 signaling. Mol Cell 2003, 12:817-828.
103. 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.
104. Kubo A., Nagao K., Yokouchi M., Sasaki H., Amagai M. External antigen uptake by Langerhans cells with reorganization of epidermal tight junction barriers. J Exp Med 2009, 206:2937-2946.
105. Weinlich G., Heine M., Stössel H., Zanella M., Stoitzner P., Ortner U., et al. Entry into afferent lymphatics and maturation in situ of migrating murine cutaneous dendritic cells. J Invest Dermatol 1998, 110:441-448.