Functional Morphology of the White Bodies of the Cephalopod Mollusc Sepia officinalis

Abstract

Claes, M. F. 1996. Functional morphology of the white bodies of the cephalopod mollusc Sepia officinalis.-Acra Zoologica (Stockholm) 77: 173-190.The white bodies and blood cells of the cuttlefish, Sepia officinalis, were investigated using light microscopy and electron microscopy. Each white body is supplied with arterial blood by two branches of the ophthalmic artery. These two branches arborize into the tissue and form an extensive capillary network that appears to be confluent with a system of thin-walled venous channels in the white bodies. This vascular arrangement appears to allow maturing cells to leave the white body tissue and enter the general circulation. The putative hemopoietic cells are embedded in an internal connective tissue network. In addition to an extensive extracellular matrix system, this network contains many obliquely striated muscle fibers that probably aid in microcirculation. The white body cells were grouped into four categories that, ultrastructural evidence suggests, represent developmental stages of a single cell line. Morphological similarities between the putative final developmental stage of this cell line and circulating blood cells strongly support the hypothesis that white body cells are hemopoietic in function. Several lines of evidence indicate that proliferation within this cell line occurs at the first two stages of development. Thus a new developmental scheme is proposed. Quantitative analyses have shown that the white bodies are structurally and functionally uncompartmentalized. A comparison of developmental stages suggests that the physiology of the white bodies shifts from proliferation to differentiation as the animals mature. Blood cell densities decrease as the animals mature. Finally, cytological evidence indicates that the white bodies of Sepia ofJicinalis are involved in reticuloendothelial functions in addition to hemopoiesis.

Hemocyanin and the branchial heart complex of Sepia officinalis : are the hemocytes involved in hemocyanin metabolism of coleoid cephalopods?

“…The only difference between the two cell forms was the uptake rate of labeled Sepia hemocyanin (higher in adhesive and lower in circulating hemocytes), possibly due to the difference in exposure time to the tracer. This and the fact that the adhesive hemocytes exhibit similar ultrastructure and incorporation of xenobiotics as the predominant circulating blood cell type Beuerlein et al 2002) indicate that it is probably a question of different developmental stages of the same cell form, as proposed by Claes (1996). However, based on the present findings it cannot be excluded that there is more than one blood cell type in the hemolymph of cephalopods as described for other invertebrates (Hill and Welsh 1966;Stang-Voss 1970;Cheng 1975;Rowley and Ratcliffe 1981;Bayne 1983;Hine 1999;Cima et al 2000).…”

“…In coleoid cephalopods, hemopoietic stem cells are located in the so-called "white bodies" (Bolognari 1949(Bolognari , 1951Curtis 1974, 1981;Johnson 1987). Although the cell population of this hemopoietic organ is morphologically heterogeneous and appears to consist of distinct and unrelated cell types, the recent study by Claes (1996) indicates that the cytological differences represent developmental stages of one single cell lineage. The putative final developmental stage of this cell lineage corresponds to the predominant circulating blood cell type referred to as leukocytes (Bolognari 1951), amebocytes (Wells 1978) or hemocytes (Cowden and Curtis 1981).…”

Haematopoiesis in molluscs: A review of haemocyte development and function in gastropods, cephalopods and bivalves

“…They are found in the reticulum of the white body’s lobes, and give rise to leukoblasts, which are characterized by a reduced cytoplasmic volume and nuclear size compared to their progenitors [99]. With the use of transmission and scanning electron microscopy, Claes (1996) [100], found haemocytoblasts, leukoblasts, and mature haemocytes in the cuttlefish S. officianalis , and proposed a schematic of haemocyte development similar to that described for octopus and squid species [99]. He observed the number of each cell type undergoing mitosis, and proposed that haemocytoblasts undergo mitosis and differentiate to produce leukoblasts, and that the primary leukoblasts undergo another round of mitosis to produce secondary leukoblasts.…”

“…He observed the number of each cell type undergoing mitosis, and proposed that haemocytoblasts undergo mitosis and differentiate to produce leukoblasts, and that the primary leukoblasts undergo another round of mitosis to produce secondary leukoblasts. He did not observe mitosis in the secondary leukoblasts, suggesting that these cells differentiate into mature circulating haemocytes [100]. Mature haemocytes are larger and have a folded nucleus, and a well-developed Golgi apparatus [99].…”

Comparative immunogenomics of molluscs

“…Professional phagocytic cells termed hemocytes, dwelling in the tissues or circulating with the blood fluid of gastropods and bivalves, phagocytose or encapsulate pathogens, eliminating these with cell-mediated cytotoxicity involving lysosomal enzymes and production of reactive oxygen species (Adema et al, 1991; Granath and Yoshino, 1983; La Peyre et al, 1995; McKerrow et al, 1985; Mohandas et al, 1985; van der Knaap and Loker, 1990). Depending on the species, molluscs may have either a single type or several functionally different categories of hemocytes, and these cells may originate from connective tissue or specialized organs, termed the amoebocyte producing organ (APO) in gastropods (Jeong et al, 1983), or from the white body organ in cephalopods (Claes, 1996; Cowden, 1972). Recognition of nonself and subsequent immune activation is mediated through lectins, initially referred to as agglutinins or cytophilic receptors for foreignness, present as humoral factors or on the surface of hemocytes (Cheng et al, 1984; Michelson and Dubois, 1977; Mullainadhan and Renwrantz, 1986; Renwrantz and Cheng, 1977; Rögener et al, 1985; van der Knaap et al, 1983b).…”