Splenic hemopoiesis of the platypus <i>(Ornithorhynchus anatinus)</i>: Evidence of primary hemopoiesis in the spleen of a primitive mammal

Tanaka, Yasukazu; Eishi, Yoshinobu; Morris, Bede

doi:10.1002/aja.1001810408

Cited by 11 publications

(11 citation statements)

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“…These observations suggest that the IZ may be a common morphological characteristic of the insectivore spleen. More recently, a similar tissue layer was found in the platypus spleen (Tanaka, 1986b), and it has been suggested that primary hemopoietic activity occurs in the spleen of this species (Tanaka, 198613;Tanaka et al, 1988). Monotremata (platypus) and Insectivora (mole, shrew) are phylogenetically primitive surviving mammals; thus, spleens with the IZ observed in these mammals may represent primitive mammalian spleens.…”

Section: Introductionmentioning

confidence: 94%

“Intermediate zone” of mammalian spleens: Light and electron microscopic study of three primitive mammalian species (platypus, shrew, and mole) with special reference to intrasplenic arteriovenous communication

Tanaka

1990

Am. J. Anat.

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The intermediate zone (IZ) of nonperfused and perfused spleens in three species of primitive mammals (shrew, mole, platypus) was studied morphologically. The IZ is a tissue zone consisting of plexiform vessels, probably venous capillaries, and is located transitionally between the white and red pulp. The IZ is separated from the white pulp by the arterial net (AN), in which the white pulp arteries terminate. Development of the IZ differs between the three species examined being distinctive in the platypus and shrew. The IZ is thin in the mole spleen. A closed type of arteriovenous (A-V) anastomosis was demonstrated in or around the IZ in the two Insectivora species examined. In the shrew spleen, peripheral arterial branches running within the IZ anastomose with the AN around the follicle. The AN anastomoses eventually with venous plexiform vessels of the IZ around the nonfollicular area of the white pulp to form a closed system. In the mole spleen, A-V anastomoses were noted between white pulp arteries (follicular and AN) and veins of the red pulp, either by direct communication or through fenestrated IZ vessels compatible with the plexiform vessels of the shrew spleen. A-V anastomosis in the IZ is probable, but not confirmed, in the platypus spleen, as analysis was limited to a nonperfused specimen. Well-developed ellipsoids were noted around arterial terminals of the IZ in the shrew spleen. Ellipsoids were also noted around all arterial terminals of the mole spleen directed to the red pulp. Most ellipsoids of the mole spleen appeared located within the IZ. No ellipsoids were present around arterial terminals of the IZ in the platypus spleen. Closed circulation was noted in terminals of the pulp artery in spleens of all three species. All pulp arteries of the mole spleen are postellipsoid segments of white pulp (AN and follicle) arteries. No ellipsoids were found around terminals of the pulp artery (penicillar artery) in shrew and platypus spleens. The IZ is probably homologous to the perilymphatic sinusoid (vein) of the lungfish spleen and may be regarded as part of the red pulp. The IZ may be representative of primitive mammalian spleens that have closed circulation. The marginal zone (MZ) of common mammalian spleens is probably a modified IZ by differentiation (remodelling) of the intrasplenic vein. In this process, withdrawal of venous vessels from the IZ occurred, leaving a lymphoreticular zone with open circulation (MZ). The marginal sinus reported in some mammalian spleens is probably a modified AN formed during this process. Possible morphological alterations of the spleen in vertebrate phylogeny are discussed.

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Section: Introductionmentioning

confidence: 94%

“Intermediate zone” of mammalian spleens: Light and electron microscopic study of three primitive mammalian species (platypus, shrew, and mole) with special reference to intrasplenic arteriovenous communication

Tanaka

1990

Am. J. Anat.

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“…Histological studies of these tissues in the platypus are limited but it has been reported that the parenchyma of the spleen is composed of red and white pulp supported by a capsule, trabeculae and reticular fibres (Tanaka et al 1988), that the thymus is composed of lobes divided into cortex and medulla and supported by a capsule and septa (Whittington, 1988) and that lymph nodules are single follicles scattered throughout loose connective tissue associated with blood vessels (Diener & Ealey, 1965 ;Whittington, 1988). Tonsillar tissue has not been reported in the platypus to date but has been reported in the pharynx of the echidna associated with the submandibular salivary glands (Diener & Ealey, 1965).…”

Section: mentioning

confidence: 99%

Histological and immunohistological investigation of lymphoid tissue in the platypus (Ornithorhynchus anatinus)

et al. 1999

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The gross and histological appearance and the distribution of T and B lymphocytes and plasma cells are described for lymphoid tissues obtained from 15 platypuses. The spleen was bilobed and surrounded by a thick capsule of collagen, elastic fibres and little smooth muscle. White pulp was prominent and included germinal centres and periarterial lymphoid sheaths. Red pulp contained haematopoietic tissue. A thin lobulated thymus was located within the mediastinum overlying the heart. The cortex of lobules consisted of dense aggregates of small and medium lymphocytes, scattered macrophages and few reticular epithelial cells. In the medulla, Hassall's corpuscles were numerous, lymphocytes were small and less abundant, and reticular cells were more abundant than in the cortex. Lymphoid nodules scattered throughout loose connective tissue in cervical, pharyngeal, thoracic, mesenteric and pelvic sites measured 790p370 µm (meanp.., n l 39) in diameter, the larger of which could be observed macroscopically. These consisted of single primary or secondary follicles supported by a framework of reticular fibres. Macrophages were common in the germinal centres. The platypus had a full range of gut-associated lymphoid tissue. No tonsils were observed macroscopically but histologically they consisted of submucosal follicles and intraepithelial lymphocytes. Peyer's patches were not observed macroscopically but histologically they consisted of several prominent submucosal secondary follicles in the antimesenteric wall of the intestine. Caecal lymphoid tissue consisted of numerous secondary follicles in the submucosa and densely packed lymphocytes in the lamina propria. Bronchus-associated lymphoid tissue was not observed macroscopically but was identified in 7 of 11 platypus lungs assessed histologically. Lymphoid cells were present as primary follicles associated with bronchi, as aggregates adjacent to blood vessels and as intraepithelial lymphocytes. The distribution of T lymphocytes, identified with antihuman CD3 and CD5, and B lymphocytes and plasma cells, identified with antihuman CD79a and CD79b and antiplatypus immunoglobulin, within lymphoid tissues in the platypus was similar to that described in therian mammals except for an apparent relative paucity of B lymphocytes. This study establishes that the platypus has a well-developed lymphoid system which is comparable in histological structure to that in therian mammals. It also confirms the distinctiveness of its peripheral lymphoid tissue, namely lymphoid nodules. Platypus lymphoid tissue has all the essential cell types, namely T and B lymphocytes and plasma cells, to mount an effective immune response against foreign antigens.

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“…Classically, ancient mammals as monotrems (Tanaka, 1986a;Tanaka et al, 1988) and insectivores (Tanaka, 1986b(Tanaka, , 1987 have a myeloid spleen similar to those present in lower vertebrates as elasmobranchs (Galíndez and Aggio, 1998) and lungfishes .…”

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confidence: 99%

“…Brief reports exist about Dasypus hybridus (Cuba Caparo, 1979), Dasypus sexcinctus and Tolypeutes tricinctus (Oria, 1941). Apparently the armadillo's spleen have characteristics of storage structures (Weiss, 1989), together with most primitive features such as persistence of myelopoiesis (Tanaka et al, 1988).…”

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confidence: 99%

Spleen of Dasypus hybridus (Mammalia, Dasypodidae): A light and electron microscopic study

2000

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Armadillos are relictual mammals important as models for biomedical studies. They contain adaptative and primitive characteristics in both anatomical and physiological aspects. In this study we describe the splenic histology and cytology of the "mulita," Dasypus hybridus. Organ samples were processed for light and electron microscopy study. The microanatomy of the organ samples as well as their different cell types are described. The spleen is non-sinusoidal, with the typical arrangement for storage functions. White pulp is lightly diffuse. Red pulp is a meshwork of circulating, immunocompetent and hemopoietic cells. Differences with other studied members of the group are discussed. The general structure of the organ agrees with the semi-fossorial habit of the species. Persistence of myeloid activity in the adult suggests the existence of specific inductive functions of the stroma. Better knowledge of this fact may give further insight on the phylogeny of hemopoiesis. Anat Rec 258:286 -291, 2000.

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Splenic hemopoiesis of the platypus (Ornithorhynchus anatinus): Evidence of primary hemopoiesis in the spleen of a primitive mammal

Cited by 11 publications

References 7 publications

“Intermediate zone” of mammalian spleens: Light and electron microscopic study of three primitive mammalian species (platypus, shrew, and mole) with special reference to intrasplenic arteriovenous communication

“Intermediate zone” of mammalian spleens: Light and electron microscopic study of three primitive mammalian species (platypus, shrew, and mole) with special reference to intrasplenic arteriovenous communication

Histological and immunohistological investigation of lymphoid tissue in the platypus (Ornithorhynchus anatinus)

Spleen of Dasypus hybridus (Mammalia, Dasypodidae): A light and electron microscopic study

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