Abstract
Melano-macrophages in the head-kidney, spleen and liver of sea bass and gilthead seabream have been investigated by means of light and electron microscopy, histochemistry and phagocytic assays. The results demonstrate the presence of both free and clustered melano-macrophages (melano-macrophage centres), with similar ultrastructural features. These large cells are PAS-, hemosiderin-and melanin-positive, and contain large, alkaline-and acid phosphatase-positive lysosomes, whose reaction intensity depends on the amount of accumulated pigment. The relationship between the cytochemical features of these lysosomes and the capacity of the melano-macrophages to phagocytose bacteria and latex beads, has been studied. The large melanomacrophage centres have a capsule of flattened cells, whose ultrastructural and cytochemical features are similar to fibroblast-like reticular cells. Melanin is the main accumulated pigment. A subpopulation of head-kidney mononuclear phagocytes engulfs melanin associated with cell debris. The relationship between the origin of the melano-macrophage pigment and the ability of monocytes/macrophages to phagocytise the melanin from melanocytes, is considered. The origin and possible function of melano-macrophage centres are discussed.
Similar content being viewed by others
References
Agius C (1979) The role of melano-macrophage centres in iron storge in normal and diseased fish. J Fish Dis 2:337–343
Agius C (1980) Phylogenetic development of melano-macrophage centres in fish. J Zool Lond 191:11–31
Agius C (1981 a) Preliminary studies on the ontogeny of the melano-macrophages of teleost haemopoietic tissues and age-related changes. Dev Comp Immunol 5:597–606
Agius C (1981 b) The effects of splenectomy and subsequent starvation on the storage of haemosiderin by the melano-macrophages of rainbow trout Salmo gairdneri Richardson. J Fish Biol 18:41–44
Agius C (1983) On the failure to detect haemosidenin in the melanomacrophages of the dogfish Scyliorhinus canicula (L.) after prolonged starvation. Experientia 39:64–67
Agius C (1985) The melano-macrophages centres of fish: a review. In: Manning MJ, Tatner MF (eds) Fish immunology. Academic Press, London, pp 85–105
Agius C, Agbede SA (1984) An electron microscopical study on the genesis of lipofuscin, melanin and haemosiderin in the haemopoietic tissues of fish. J Fish Biol 24:471–488
Agius C, Couchman W (1986) Induction of enhanced alkaline phosphatase activity in the melano-macrophage centres of Oreochromis aureus (Steindachner) through starvation and vaccination. J Fish Biol 28:87–92
Agius C, Roberts RJ (1981) Effects of starvation on the melanomacrophage centres of fish. J Fish Biol 19:161–169
Ardavin CF, Zapata A (1987) Ultrastructure and changes during metamorphosis of the lympho-hemopoietic tissue of the larval anadromous sea lamprey Petromyzon marinus. Dev Comp Immunol 11:79–93
Bach R, Chen PK, Chapman CB (1978) Changes in the spleen of the channel catfish, Ictalurus punctatus Rafinesque induced by infection with Aeromonas hydrophila. J Fish Dis 1:205–217
Bainton DF (1985) Bone marrow stromal cells, fibroblasts and macrophages. In Van Furth R (ed) Mononuclear phagocytes. Characteristics, physiology and function. Martinus Nijhoff, Dordrecht, pp 125–136
Braun-Mesje R, Bertheussen K, Kaplan G, Seljelid R (1981) Salmonid macrophages: separation, “in vitro” culture and characterization. J Fish Dis 4:141–151
Brown CL, George CJ (1985) Age-dependent accumulation of macrophage aggregates in the yellow perch Perca flavescens (Mitchill). J Fish Dis 8:135–138
Ellis AE (1977) The leucocytes of fish: a review. J Fish Biol 11:453–491
Ellis AE (1980) Antigen-trapping in the spleen and kidney of the plaice, Pleuronectes platessa L. J Fish Dis 3:413–426
Ellis AE (1981) Non-specific defence mechanisms in fish and their role in disease processes. Dev Biol Stand 49:337–352
Ellis AE, DeSousa M (1974) Phylogeny of the lymphoid system. I. A study of the fate of circulating lymphocytes in plaice. Eur J Immunol 4:338–343
Ellis AE, Munroe ALS, Roberts RJ (1976) Defence mechanisms in fish. 1. A study of the phagocytic system and the fate of intraperitoneally injected particulate material in the plaice (Pleuronectes platessa L.). J Fish Biol 8:67–78
Ellis AE, Roberts RJ, Tytler P (1978), The anatomy and physiology of teleosts. In: Roberts RJ (ed) Fish pathology. Baillière Tindall, London, pp 13–54
Ferguson HW (1976) The relationship between ellipsoids and melano-macrophages centres in the spleen of turbot (Scophthalmus maximus). J Comp Pathol 86:377–380
Fontana A (1912) Verfahren zur intensiven und raschen Färbung des Treponema pallidum und anderer Spirochäten. Dermatologische Wochenschrift 55:1003
Fulop GMI, McMillan DB (1984) Phagocytosis in the spleen of the sunfish Lepomis spp. J Morphol 179:175–195
Goldberg RF, Barka T (1962) Acid phosphatase activity in human blood cells. Nature 195:297
Gomori G (1952) In. Microscopic histochemistry. Principles and practise. University of Chicago Press, Chicago, pp 134–136
Herraez MP, Zapata AG (1986) Structure and function of the melano-macrophage centres of the goldfish Carassius auratus. Vet Immunol Immunopathol 12:117–126
Herráez MP, Zapata AG (1991) Structural characterization of the melano-macrophage centres(MMC) of goldfish Carassius auratus. J Fish Biol 29:711–720
Kaplow LS (1955) A histochemical procedure for localizing and evaluated leucocyte alkaline phosphatase in smear of blood and bone marrow. Blood 10:1023–1029
Lamers CHJ (1985) The reaction of the immune system of fish, to vaccination. Ph. D. Thesis, Agricultural University of Wageningen, p 32
López-Ruiz A, Esteban MA, Meseguer J (1992) Blood cells of the gilthead seabream (Sparus aurata L.). Light and electron microscopic studies. Anat Rec 234:161–171
Masson P (1914) La glande endocrine de l'intestine chez l'homme. Comptes rendus hebdomadaires des séances de l'Academic des sciences 158:59
McManus JFA (1948) Histological demonstration of mucin after periodic acid. Nature 158:202
Meseguer J, Esteban MA, Agulleiro B (1991) Stromal cells, macrophages and lymphoid, cells in the head-kidney of sea bass (Dicentrarchus labrax L.). An ultrastructural study. Arch Histol Cytol 54:299–309
Meseguer J, Esteban MA, Muñoz J, López-Ruiz A (1993) Ultrastructure of the peritoneal exudate cells of seawater teleosts, seabream (Sparus aurata) and sea bass (Dicentrarchus labrax). Cell Tissue Res 273:301–307
Micale V, Perdichizzi F (1990) A quantitative and histochemical study on melano-macrophage centres in the spleen of the teleost fish Diplodus annularis L. J Fish Biol 37:191–197
Oguri M (1976) Histochemical observations on the dark brown pigment granules found in the kidney tissue of rainbow trout. Bull Jpn Sci Fish 42:1223–1227
Perls M (1867) Nachweis von Eisenoxyd in gewissen Pigmenten. Virchows Arch 39:42
Plytycz B, Flory CM, Galvan I, Bayne CJ (1989) Leukocytes of rainbow trout (Oncorhynchus mykiss) pronephros: cell types producing superoxide anion. Dev Comp Immunol 13:217–224
Quesada J, Villena MI, Agulleiro B (1990) Structure of the spleen of the sea bass (Dicentrarchus labrax): a light and electron microscopic study. J Morphol 206:273–281
Roberts RJ (1975) Melanin-containing cells of teleost fish and their relation to disease. In: Ribelin WE, Migaki G (eds) The pathology of fishes. University of Wisconsin Press, Madisson Wisconsin, USA, pp 399–428
Rowley AF, Page M (1985) Lamprey melano-macrophages: structure and function. In: Manning MJ, Tatner MF (eds) Fish immunology. Academic Press, London, pp 273–284
Scott JE, Dorling J (1965) Differential staining of acid glycosaminoglycans (mucopolysaccharides) by Alcian blue in salt solutions. Histochemie 5:221–233
Secombes CJ, Manning MJ (1982) Histological changes in lymphoid organs of carp following injection of soluble or particulate antigens. Dev Comp Immunol [Suppl] 2:53–58
Stenn KS (1988) The skin. In: Weiss L (ed) Cell and tissue biology. A textbook of histology. Urban and Schwarzenberg, Baltimore Munich, pp 539–572
Tokumaru M, Ferri AG (1970) Histochemistry of the pigments found in the liver, spleen and kidney of the fresh-water fish. Rev Bras Biol 30:163–171
Tsujii T, Seno S (1990) Melano-macrophage centres in the aglomerular kidney of the sea horse (teleosts): morphologic studies on its formation and possible function. Anat Rec 226:460–470
Vogelbein WK, Fournie JW, Overstreet RM (1987) Sequential development and morphology of experimentally induced hepatic melano-macrophage centres in Rivulus marmoratus. J Fish Biol 31:145–153
Yu ML, Kiley CW, Sarat DA, Perlmuter A (1971) Regulation of haemosiderin to erythropoiesis in the blue gourami Trichogaster tricopterus. J Fish Res Bd Can 28:47–48
Zapata A (1983) Phylogeny of the fish immune system. Bull Inst Pasteur 81:175–186
Zuasti A, Jara JR, Ferrer C, Solano F (1989) Occurrence of melanin granules and melanosynthesis in the kidney of Sparus auratus. Pigment Cell Res 2:93–99
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Meseguer, J., López-Ruiz, A. & Esteban, M.A. Melano-macrophages of the seawater teleosts, sea bass (Dicentrarchus labrax) and gilthead seabream (Sparus aurata): morphology, formation and possible function. Cell Tissue Res 277, 1–10 (1994). https://doi.org/10.1007/BF00303074
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00303074