Fetal and neonatal murine skin harbors Langerhans cell precursors

Journal of Leukocyte Biology

Volumn 77, Issue 3, 2005, Pages 352-360

  Chang Rodriguez, S ^a   Hoetzenecker, W ^a   Schwarzler C ^b   Biedermann, T ^c   Saeland, S ^d   Elbe Burger A ^a,e  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b Novartis Institutes for Biomed Res   (Austria)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d MERCK RESEARCH LABORATORIES   (United States)

^e Universitatsklinik fur Dermatologie   (Austria)

Author keywords

Apoptosis; Cell cycle; Cytokines; Epidermis; Grafts; Leukocytes; Transplantation

Indexed keywords

APYRASE; CD34 ANTIGEN; CYTOKINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL PROLIFERATION; CELL STRUCTURE; COMBINED IMMUNODEFICIENCY; CONTROLLED STUDY; DENDRITIC CELL; EPIDERMIS; EPIDERMIS CELL; FETUS; LANGERHANS CELL; LEUKOCYTE; MOUSE; NEWBORN; NICK END LABELING; NONHUMAN; PHENOTYPE; PRECURSOR; PRIORITY JOURNAL; SKIN GRAFT; SKIN TRANSPLANTATION;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CELL CYCLE; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; LANGERHANS CELLS; LEUKOCYTES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, SCID; PHENOTYPE; PREGNANCY; SKIN; STEM CELLS;

EID: 14244258925     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1004584     Document Type: Article

References (54)

1. Steinman, R. M. (1991) The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9, 271-296.
2. Banchereau, J., Briere, F., Caux, C., Davoust, J., Lebecque, S., Liu, Y-J., Pulendran, B., Palucka, K. (2000) Immunobiology of dendritic cells. Annu. Rev. Immunol. 18, 767-811.
3. Stingl, G., Maurer, D., Hauser, C., Wolff, K. (2003) The skin: an immunologic barrier. In Fitzpatrick's Dermatology in General Medicine, vol. 1 (I. M. Freedberg, A. Z. Eisen, K. Wolff, K. F. G. L. A. Austen, S. I. Katz, eds.), New York, NY, McGraw Hill, 253-272.
4. Katz, S. I., Tamaki, K., Sachs, D. H. (1979) Epidermal Langerhans cells are derived from cells originating in bone marrow. Nature 282, 324-326.
5. Frelinger, J. G., Hood, L., Hill, S., Frelinger, J. A. (1979) Mouse epidermal Ia molecules have a bone marrow origin. Nature 282, 321-323.
6. Merad, M., Manz, M. G., Karsunky, H., Wagers, A., Peters, W., Charo, I., Weissman, I. L., Cyster, J. G., Engleman, E. G. (2002) Langerhans cells renew in the skin throughout life under steady-state conditions. Nat. Immunol. 3, 1135-1141.
7. Holzmann, S., Tripp, C. H., Schmuth, M., Janke, K., Koch, F., Saeland, S., Stoitzner, P., Romani, N. (2004) A model system using tape stripping for characterization of Langerhans cell-precursors in vivo. J. Invest. Dermatol. 122, 1165-1174.
8. Jakob, T., Ring, J., Udey, M. C. (2001) Multistep navigation of Langerhans/dendritic cells in and out of the skin. J. Allergy Clin. Immunol. 108, 688-696.
9. Hemmi, H., Yoshino, M., Yamazaki, H., Naito, M., Iyoda, T., Omatsu, Y., Shimoyama, S., Letterio, J. J., Nakabayashi, T., Tagaya, H., Yamane, T., Ogawa, M., Nishikawa, S., Ryoke, K., Inaba, K., Hayashi, S., Kunisada, T. (2001) Skin antigens in the steady state are trafficked to regional lymph nodes by transforming growth factor-β1-dependent cells. Int. Immunol. 13, 695-704.
10. + dendritic epidermal cells in the perinatal period. J. Immunol. 143, 2431-2438.
11. Romani, N., Schuler, G., Fritsch, P. (1986) Ontogeny of Ia-positive and Thy-1-positive leukocytes of murine epidermis. J. Invest. Dermatol. 86, 129-133.
12. Kobayashi, M., Asano, H., Fujita, Y., Hoshino, T. (1987) Development of ATPase-positive, immature Langerhans cells in the fetal mouse epidermis and their maturation during the early postnatal period. Cell Tissue Res. 248, 315-322.
13. Dewar, A. L., Doherty, K. V., Woods, G. M., Lyons, A. B., Muller, H. K. (2001) Acquisition of immune function during the development of the Langerhans cell network in neonatal mice. Immunology 103, 61-69.
14. Tripp, C. H., Chang-Rodriguez, S., Stoitzner, P., Holzmann, S., Stössel, H., Douillard, P., Saeland, S., Koch, F., Elbe-Bürger, A., Romani, N. (2004) Ontogeny of Langerin/CD207 expression in the epidermis of mice. J. Invest. Dermatol. 122, 670-672.
15. Chang-Rodriguez, S., Ecker, R., Stingl, G., Elbe-Bürger, A. (2004) Autocrine IL-10 partially prevents differentiation of neonatal dendritic epidermal leukocytes into Langerhans cells. J. Leukoc. Biol. 76, 657-666.
16. + fetal murine thymocytes home to the skin and give rise to proliferating dendritic epidermal T cells. J. Immunol. 146, 2536-2543.
17. Biedermann, T., Schwärzler, C., Lametschwandtner, G., Thoma, G., Carballido-Perrig, N., Kund, J., De Vries, J. E., Rot, A., Carballido, J. M. (2002) Targeting CLA/E-selectin interactions prevents CCR4-mediated recruitment of human Th2 memory cells to human skin in vivo. Eur. J. Immunol. 32, 3171-3180.
18. Hoetzenecker, W., Meingassner, J. G., Ecker, R., Stingl, G., Stuetz, A., Elbe-Bürger, A. (2004) Corticosteroids but not pimecrolimus affect viability, maturation and immune function of murine epidermal Langerhans cells. J. Invest. Dermatol. 122, 673-684.
19. Strobl, H., Bello-Fernandez, C., Riedl, E., Pickl, W. F., Majdic, O., Lyman, S. D., Knapp, W. (1997) Flt3 ligand in cooperation with transforming growth factor-β1 potentiates in vitro development of Langerhans-type dendritic cells and allows single-cell dendritic cell cluster formation under serum-free conditions. Blood 90, 1425-1434.
20. Valladeau, J., Clair-Moninot, V., Dezutter-Dambuyant, C., Pin, J. J., Kissenpfennig, A., Mattei, M. G., Ait-Yahia, S., Bates, E. E., Malissen, B., Koch, F., Fossiez, F., Romani, N., Lebecque, S., Saeland, S. (2002) Identification of mouse Langerin/CD207 in Langerhans cells and some dendritic cells of lymphoid tissues. J. Immunol. 168, 782-792.
21. Pines, J. (1999) Four-dimensional control of the cell cycle. Nat. Cell Biol. 1, E73-E79.
22. Bosma, G. C., Custer, R. P., Bosma, M. J. (1983) A severe combined immunodeficiency mutation in the mouse. Nature 301, 527-530.
23. Reams, W. M., Tompkins, S. P. (1973) A developmental study of murine epidermal Langerhans cells. Dev. Biol. 31, 114-123.
24. Schweizer, J., Marks, F. (1977) A developmental study of the distribution and frequency of Langerhans cells in relation to formation of patterning in mouse tail epidermis. J. Invest. Dermatol. 69, 198-204.
25. Schottelius, A. J., Moldawer, L. L., Dinarello, C. A., Asadullah, K., Sterry, W., Edwards III, C. K. (2004) Biology of tumor necrosis factor-α - implications for psoriasis. Exp. Dermatol. 13, 193-222.
26. Ruckert, R., Lindner, G., Bulfone-Paus, S., Paus, R. (2000) High-dose proinflammatory cytokines induce apoptosis of hair bulb keratinocytes in vivo. Br. J. Dermatol. 143, 1036-1039.
27. Inaba, K., Inaba, M., Romani, N., Aya, H., Deguchi, M., Ikehara, S., Muramatsu, S., Steinman, R. M. (1992) Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176, 1693-1702.
28. + bone marrow progenitors that are expanded by c-kit-ligand and yield pure dendritic cell colonies in the presence of granulocyte/macrophage colony-stimulating factor and tumor necrosis factor α. J. Exp. Med. 182, 1111-1120.
29. Borkowski, T. A., Letterio, J. J., Mackall, C. L., Saitoh, A., Wang, X. J., Roop, D. R., Gress, R. E., Udey, M. C. (1997) A role for TGFβ1 in Langerhans cell biology. Further characterization of the epidermal Langerhans cell defect in TGFβ1 null mice. J. Clin. Invest. 100, 575-581.
30. + hemopoietic progenitors. J. Immunol. 157, 1499-1507.
31. + progenitors. J. Leukoc. Biol. 66, 781-791.
32. + hematopoietic progenitor cells into Langerhans cells under serum-free conditions without granulocyte-macrophage colony-stimulating factor. J. Invest. Dermatol. 120, 256-265.
33. + hematopoietic progenitor cells into dendritic cells with features of Langerhans cells. J. Invest. Dermatol. 121, 1397-1401.
34. + precursor cells develop into Langerhans cells in a TGF-β 1-dependent manner. J. Immunol. 163, 4869-4877.
35. Zhang, Y., Ogata, M., Chen, P., Harada, A., Hashimoto, S. I., Matsushima, K. (1999) Transforming growth factor-β1 polarizes murine hematopoietic progenitor cells to generate Langerhans cell-like dendritic cells through a monocyte/macrophage differentiation pathway. Blood 93, 1208-1220.
36. Geissmann, F., Prost, C., Monnet, J. P., Dy, M., Brousse, N., Hermine, O. (1998) Transforming growth factor β1, 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. 187, 961-966.
37. + subset of human blood dendritic cells is a direct precursor of Langerhans cells. J. Immunol. 163, 1409-1419.
38. + cells differentiate into Langerhans cells. Nat. Immunol. 2, 1151-1158.
39. + bone marrow precursors cultured with c-kit ligand, granulocyte-macrophage colony-stimulating factor, and TNF-α. J. Immunol. 154, 5851-5861.
40. + progenitors in bone marrow and cord blood. Br. J. Haematol. 93, 258-264.
41. Czernielewski, J., Vaigot, P., Prunieras, M. (1985) Epidermal Langerhans cell - a cycling cell population. J. Invest. Dermatol. 84, 424-426.
42. Czernielewski, J. M., Demarchez, M. (1987) Further evidence for the self-reproducing capacity of Langerhans cells in human skin. J. Invest. Dermatol. 88, 17-20.
43. Miyauchi, S., Hashimoto, K. (1987) Epidermal Langerhans cells undergo mitosis during the early recovery phase after ultraviolet-B irradiation. J. Invest. Dermatol. 88, 703-708.
44. Miyauchi, S., Hashimoto, K. (1989) Mitotic activities of normal epidermal Langerhans cells. J. Invest. Dermatol. 92, 120-121.
45. De Fraissinette, A., Staquet, M. J., Dezutter-Dambuyant, C., Schmitt, D., Thivolet, J. (1988) Langerhans cells in S-phase in normal skin detected by simultaneous analysis of cell surface antigen and BrdU incorporation. J. Invest. Dermatol. 91, 603-605.
46. Dunnwald, M., Chinnathambi, S., Alexandrunas, D., Bickenbach, J. R. (2003) Mouse epidermal stem cells proceed through the cell cycle. J. Cell. Physiol. 195, 194-201.
47. Streilein, J. W., Strome, P. G., Gruchalla, R. S., Wood, P. J. (1983) Analysis of neonatally induced tolerance of H-2 alloantigens. IV. Graft adaptation in long-term tolerated grafts. Transplantation 35, 474-478.
48. Krueger, G. G., Emam, M. (1983) Biology of Langerhans cells: selective migration of Langerhans cells into allogeneic and xenogeneic grafts on nude mice. Proc. Natl. Acad. Sci. USA 80, 1650-1654.
49. Krueger, G. G., Emam, M. (1984) Biology of Langerhans cells: analysis by experiments to deplete Langerhans cells from human skin. J. Invest. Dermatol. 82, 613-617.
50. Chen, H. D., Ma, C., Yuan, Y. T., Wang, Y. K., Silvers, W. K. (1986) Occurrence of donor Langerhans cells in mouse and rat chimeras and their replacement in skin grafts. J. Invest. Dermatol. 86, 630-633.
51. Demarchez, M., Asselineau, D., Czernielewski, J. (1993) Migration of Langerhans cells into human epidermis of "reconstructed" skin, normal skin, or healing skin, after grafting onto the nude mouse. J. Invest. Dermatol. 100, 648-652.
52. Cowin, A. J., Holmes, T. M., Brosnan, P., Ferguson, M. W. (2001) Expression of TGF-β and its receptors in murine fetal and adult dermal wounds. Eur. J. Dermatol. 11, 424-431.
53. Nolan, K. F., Strong, V., Soler, D., Fairchild, P. J., Cobbold, S. P., Croxton, R., Gonzalo, J. A., Rubio, A., Wells, M., Waldmann, H. (2004) IL-10-conditioned dendritic cells, decommissioned for recruitment of adaptive immunity, elicit innate inflammatory gene products in response to danger signals. J. Immunol. 172, 2201-2209.
54. Dorschner, R. A., Lin, K. H., Murakami, M., Gallo, R. L. (2003) Neonatal skin in mice and humans expresses increased levels of antimicrobial peptides: innate immunity during development of the adaptive response. Pediatr. Res. 53, 566-572.