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

Abstract

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.

Heavy Chain V Region Diversity in the Duck-Billed Platypus (Ornithorhynchus anatinus): Long and Highly Variable Complementarity-Determining Region 3 Compensates for Limited Germline Diversity

“…Histological studies show that the spleen-, thymus-, and gut-associated lymphoid tissues in the platypus are well developed and comparable in histological structure to those of therian mammals (25). However, in sites where lymph nodes would be expected in marsupials and placental mammals, monotremes were found to have lymphoid nodules that resemble the jugular bodies of the amphibians, which indicate that monotremes have a somewhat more primitive immune system (25). (27).…”

“…The monotremes are egg-laying mammals and were therefore regarded as reptile-like or primitive mammals; however, they posses almost all major mammalian features, including a well-developed fur coat, a single bone in the lower jaw, three bones in the middle ear, and mammary glands. Histological studies show that the spleen-, thymus-, and gut-associated lymphoid tissues in the platypus are well developed and comparable in histological structure to those of therian mammals (25). However, in sites where lymph nodes would be expected in marsupials and placental mammals, monotremes were found to have lymphoid nodules that resemble the jugular bodies of the amphibians, which indicate that monotremes have a somewhat more primitive immune system (25).…”

Comparative Phylogeny of the Mucosa-Associated Lymphoid Tissue

“…Furthermore, lymph nodes, when present, are less complex and resemble lymph nodules that contain only single follicles (Connolly et al, 1999). Monotremes have no obvious macroscopic GALT, although histology reveals that they have PP and cecal lymphoid follicles (Connolly et al, 1999). Success in breeding monotremes in captivity has been limited and likewise so are immunological studies of these enigmatic animals.…”

“…Their TCR gene organization and content, for example, have characteristics found in birds and amphibians but absent in marsupials and placentals (Parra et al, 2012). Furthermore, lymph nodes, when present, are less complex and resemble lymph nodules that contain only single follicles (Connolly et al, 1999). Monotremes have no obvious macroscopic GALT, although histology reveals that they have PP and cecal lymphoid follicles (Connolly et al, 1999).…”

Storage of Blood in the Mammalian Spleen: an Evolutionary Perspective

“…Table 2 (which is a synthesis of the 187 species for which data are collected in the Appendix) compiles data on relative splenic weight, characteristics indicating storage ability (capsule layers and muscularization) and presence of erythropoiesis. It can be seen that mammals displaying splenic erythropoiesis have large spleens that, nevertheless, do not belong to the Bstorage type.T he highest relative splenic weight among mammals is seen in Ornithorhynchus anatinus, in which the spleen is the main erythropoietic organ (Tanaka 1986); but, because of its relative scarceness of smooth muscle cells, the spleen of the platypus is not classified as a storing one (Connolly et al 1999). Similarly, in opossums and Lipotyphla, the spleen is an important site of erythropoiesis (although not the main one as in platypus) and displays a high relative weight accompanied by poor muscularization.…”