Abstract
The ontogeny and disease responses of Langerhans-like cells within lymphoid tissues of Atlantic salmon, Salmo salar, and rainbow trout, Oncorhynchus mykiss, were investigated. These cells were studied in situ with the use of two markers: the ultrastructural presence of Birbeck-like granules and immunohistochemistry with an antibody against human langerin/CD207 that cross-reacts with salmonid tissues. The appearance of Birbeck-like granules was observed in rainbow trout at 2 weeks post-hatch (PH) in the thymus and anterior kidney prior to the development of the spleen. Spleen first appeared at 3 weeks PH in both Atlantic salmon and rainbow trout, and Birbeck-like granules were observed within cells of the newly developed spleens. The cross-reactivity of langerin as seen by immunohistochemistry was not clearly observed in kidney and spleen until 9 weeks PH, when a strong cytoplasmic reaction was observed. To study langerin-positive cells in spleen and kidney during disease, microsporidial gill disease (MGD) in rainbow trout was used as a known disease model inducing a strong cell-mediated adaptive immune response. Langerin-positive cells in healthy fish were seen predominantly in the spleen, and only low numbers were present in the anterior kidney. During MGD, langerin-positive cell numbers were elevated in the anterior kidney and were significantly higher during 5, 6, and 10 weeks post-exposure (PE) compared with healthy control tissue. During MGD, the distribution of langerin-positive cells in the spleen and anterior kidney shifted from having significantly higher numbers of cells in the spleen than in the kidney in controls and at 1 and 4 weeks PE to having a similar distribution of the cells in the two organs at 2, 3, 5, and 6 weeks PE. By 10 weeks PE, significantly higher numbers of langerin-positive cells occurred in the anterior kidney compared with the spleen.
References
Chorro L, Sarde A, Li M, Woollard KJ, Chambon P, Malissen B, Kissenpfennig A, Barbaroux JP, Groves R, Geissmann F (2009) Langerhans cell (LC) proliferation mediates neonatal development, homeostasis, and inflammation-associated expansion of the epidermal LC network. J Exp Med 206:3089–3100
Lovy J, Savidant GP, Speare DJ, Wright GM (2009) Langerin/CD207 positive dendritic-like cells in the haemopoietic tissues of salmonids. Fish Shellfish Immunol 27:365–368
Lovy J, Speare DJ, Wright GM (2007) Ultrastructural examination of the host inflammatory response within gills of netpen reared chinook salmon (Oncorhynchus tshawytscha) with microsporidial gill disease. Fish Shellfish Immunol 22:131–149
Lovy J, Wright GM, Speare DJ (2008) Comparative cellular morphology suggesting the existence of resident dendritic cells within immune organs of salmonids. Anat Rec 291:456–462
Lovy J, Wright GM, Speare DJ, Tyml T, Dykova I (2010) Comparative ultrastructure of Langerhans-like cells in the spleens of ray-finned fishes (Actinopterygii). J Morphol 271:1229–1239
Passantino L, Cianciotta A, Jirillo F, Carrassi M, Jirillo E, Passantino GF (2005) Lymphoreticular system in fish: erythrocyte-mediated immunomodulation of macrophages contributes to the formation of melanomacrophage centers. Immunopharmacol Immunotoxicol 27:147–161
Rodriguez-Tovar LE, Wright GM, Wadowska DW, Speare DJ, Markham RJF (2002) Ultrastructural study of the early development and localization of Loma salmonae in the gills of experimentally infected rainbow trout. J Parasitol 88:244–253
Rodriguez-Tovar LE, Wright GM, Wadowska DW, Speare DJ, Markham RJF (2003) Ultrastructural study of the late stages of Loma salmonae development in the gills of experimentally infected rainbow trout. J Parasitol 89:464–474
Rodriguez-Tovar LE, Markham RJ, Speare DJ, Sheppard J (2006) Cellular immunity in salmonids infected with the microsporidial parasite Loma salmonae or exposed to non-viable spores. Vet Immunol Immunopathol 114:72–83
Sanchez JG, Speare DJ, Markham RJF, Wright GM, Kibenge FSB (2001) Localization of the initial developmental stages of Loma salmonae in rainbow trout (Oncorhynchus mykiss). Vet Pathol 38:540–546
Schuler G, Steinman RM (1985) Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J Exp Med 161:526–546
Speare DJ, Beaman HJ, Jones SRM, Markham RJF, Arsenault GJ (1998) Induced resistance in rainbow trout, Oncorhynchus mykiss (Walbaum), to gill disease associated with the microsporidian gill parasite Loma salmonae. J Fish Dis 21:93–100
Tatner MF, Manning MJ (1983) The ontogeny of cellular immunity in the rainbow trout in relation to the stage of development of the lymphoid organs. Dev Comp Immunol 7:69–75
Thepaut M, Valladeau J, Nurisso A, Kahn R, Arnou B, Vives C, Saeland S, Ebel C, Monnier C, Dezutter-Dambuyant C, Imberty A, Fieschi F (2009) Structural studies of langerin and Birbeck granule: a macromolecular organization model. Biochemistry 48:2684–2698
Tripp CH, Chang-Rodriguez S, Stoitzner P, Holzmann S, Stossel H, Douillard P, Saeland S, Koch F, Elbe-Burger A, Romani N (2004) Ontogeny of langerin/CD207 expression in the epidermis of mice. J Invest Dermatol 122:670–672
Valladeau J, Ravel O, Dezutter-Dambuyant C, Moore K, Kleijmeer M, Liu Y, Duvert-Frances V, Vincent C, Schmitt D, Davoust J, Caux C, Lebecque S, Saeland S (2000) Langerin, a novel C-type lectin specific to Langerhans cells, is an endocytic receptor that induces the formation of Birbeck granules. Immunity 12:71–81
Valladeau J, Clair-Moninot V, Dezutter-Dambuyant C, Pin JJ, Kissenpfennig A, Mattei MG, Ait-Yahia S, Bates EE, 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
Wolff K (1967) The fine structure of the Langerhans cell granule. J Cell Biol 35:468–473
Acknowledgements
We are grateful to Dr. David J. Speare for providing tank space and a source of Loma salmonae, to the Cardigan fish hatchery for providing Atlantic salmon, to Dorota Wadowska for assistance in the preparation of samples for transmission electron microscopy, and to Nicole Lewis for assistance with the statistical analysis.
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This research was funded by an AVC internal research grant.
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Lovy, J., Savidant, G.P. & Wright, G.M. Ontogeny and disease responses of Langerhans-like cells in lymphoid tissues of salmonid fish. Cell Tissue Res 346, 111–118 (2011). https://doi.org/10.1007/s00441-011-1244-0
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DOI: https://doi.org/10.1007/s00441-011-1244-0