Resorption and remodelling of skeletal tissues is required for development and growth, mechanical adaptation, repair, and mineral homeostasis of the vertebrate skeleton. Here we review for the first time the current knowledge about resorption and remodelling of the skeleton in teleost fish, the largest and most diverse group of extant vertebrates. Teleost species are increasingly used in aquaculture and as models in biomedical skeletal research. Thus, detailed knowledge is required to establish the differences and similarities between mammalian and teleost skeletal remodelling, and between distantly related species such as zebrafish (Danio rerio) and medaka (Oryzias latipes).



The cellular mechanisms of differentiation and activation of osteoclasts and the functions of teleost skeletal remodelling are described. Several characteristics, related to skeletal remodelling, distinguish teleosts from mammals. These characteristics include (a) the absence of osteocytes in most species; (b) the absence of haematopoietic bone marrow tissue; (c) the abundance of small mononucleated osteoclasts performing non-lacunar (smooth) bone resorption, in addition to or instead of multinucleated osteoclasts; and (d) a phosphorus- rather than calcium-driven mineral homeostasis (mainly affecting the postcranial dermal skeleton). Furthermore, (e) skeletal resorption is often absent from particular sites, due to sparse or lacking endochondral ossification.



Based on the mode of skeletal remodelling in early ontogeny of all teleosts and in later stages of development of teleosts with acellular bone we suggest a link between acellular bone and the predominance of mononucleated osteoclasts, on the one hand, and cellular bone and multinucleated osteoclasts on the other. The evolutionary origin of skeletal remodelling is discussed and whether mononucleated osteoclasts represent an ancestral type of resorbing cells. Revealing the differentiation and activation of teleost skeletal resorbing cells, in the absence of several factors that trigger mammalian osteoclast differentiation, is a current challenge. Understanding which characters of teleost bone remodelling are derived and which characters are conserved should enhance our understanding of the process in fish and may provide insights into alternative pathways of bone remodelling in mammals.

A comparative view on mechanisms and functions of skeletal remodelling in teleost fish, with special emphasis on osteoclasts and their function

Vertebrate organisms have evolved sophisticated immunological mechanisms for the recognition of self versus nonself. The immune system is functionally characterized by specificity, diversity, and memory but is based at the molecular level on highly diverse antigen receptors (T-cell receptor, TcR; immunoglobulin, Ig), which together with major histocompatibility complex (MHC) molecules allow the activation of the so-called immunocompetent cells (T- and B-lymphocytes) during the immune response. Development and functional activation of immune cells occur in specialized tissue microenvironments provided by the primary and/or secondary lymphoid organs. These lymphoid organs then, represent a higher-order morphological structure culminating from complex molecular, cellular and tissue interactions, and are an invariable feature of the vertebrate immune system.

Phylogeny of lower vertebrates and their immunological structures.

also occur together with the blood-forming state (e.g. in the hedgehog). Tischendorf (1969, pp. 128ff., 201ff., 374) in spite of fundamental objections to a far-tooinflexible handling of the terminology in general and the definition of the 'storage' spleen in particular does not wish to renounce the principle suggested by v. Herrath as a classification. Even if the type theory is not convincing in all its aspects, its combined quantitative and functional approach has permanently influenced spleen research and will especially in its more conciliatory last version (v. Herrath, 1963, 1965) keep its heuristical worth as a working hypothesis. The species-specific differences in the fine and coarse innervation of the mammalian spleen have unfortunately been neglected until now, and virtually nothing is known about the innervation of the non-mammalian spleen. Though many questions in the last analysis can be settled only by experiment, a specialized innervation or a favored kind of innervation allows us to draw conclusions about the functions of certain structures (Harting, 1952), because the nervous control (Hoff, 1931) is not less important than the humoral for the harmonious coordination of the numerous partial processes constituting the total function of the spleen. If the neuroarchitecture (Tischendorf, 1948, 1956, 1969, pp. 662ff.) of various spleens is considered in the light of v. Herrath's concepts, a considerable agreement results; i.e. the crucial points of innervation lie on the respective structural-functional key positions. But already the few innervation pictures known which, moreover, like the Experientia 41 (1985), Birkh~iuser Verlag, CH~010 Basel/Switzerland

The fish spleen: structure and function

Fish granulocytes: Morphology, distribution, and function

An understanding of several macroevolutionary trends has been greatly advanced in recent years by a focus on disparity (morphological variety) rather than taxic diversity. A seminal issue has been the nature of the Cambrian Radiation, and the question of whether problematical Cambrian fossils embody a range of anatomical design far exceeding that observed thereafter. Arthropods have hitherto furnished the only case study, revealing comparable levels of Cambrian and Recent disparity. The generality of this observation needs to be tested in other groups, and the priapulid worms provide a well-documented example. Cladistic analysis of morphological characters for priapulids reveals a paraphyletic series of Cambrian taxa below a crown-group of post-Cambrian genera. However, one extant family (the Tubiluchidae) may be more closely related to Cambrian forms or resolve basally. Character-based morphospace analysis demonstrates greater disparity amongst Recent taxa than amongst their Cambrian counterparts. There is relatively little overlap between the regions of morphospace occupied by Cambrian and Recent genera (contrasting with the situation in arthropods). The Tubiluchidae are morphologically intermediate between Cambrian and other Recent families using several measures of phenetic proximity, and they inhabit environments more comparable with their Cambrian cousins. This work confirms the extensive morphological diversification of major clades by the Cambrian but lends no support to models of a post-Cambrian “decimation” of disparity.

Cambrian and recent disparity : the picture from priapulids

The lymphomyeloid system of nearly adult nurse sharks, Ginglymostoma cirratum, was investigated. Lymphomyeloid structures detectable by the naked eye at dissection are the epigonal organ and the spleen. Microscopic examination shows that the epigonal organ produces granulocytes and lymphocytes. The white pulp of the spleen is lymphoid, whereas the red pulp is mainly erythropoietic. Cells with the morphological characteristics of plasma cells occur in the epigonal organ and the spleen. Peroxidase-positive granulated cells are found in the epigonal organ. In contrast to many other elasmobranchs, the nurse shark lacks the Leydig organ, i.e. the lymphomyeloid structure of the esophagus; but the epigonal organ is well developed and averages 0.60% of the body weight. The spleen weighs about 0.26% of the body weight. The mode of life of the nurse shark in shallow tropical waters probably puts a considerable demand on its immune system. Cells produced by the epigonal organ may be important in immune responses and...

The lymphomyeloid (hemopoietic) system of the atlantic nurse shark, ginglymostoma cirratum

In Etmopterus spinax, a small deep water shark, the predominating lymphomyeloid tissue is the so called Leydig organ. This consists of bone marrow-like tissue situated between the muscularis and the mucosa of the esophagus. Examination by light and electron microscopy shows that the Leydig organ produces large numbers of granulocytes and lymphocytes. Two main types of granulocytes occur, tentatively called heterophilic and eosinophilic. The heterophilic cells may be subdivided into three types which differ in the ultrastructure of the granules. Cells structurally resembling mammalian plasma cells are common. The presence of these cells indicates that the tissue is part of the shark immune system.

The cellular structure of the leydig organ in the shark, etmopterus spinax (l.)

Studies on the physiology of the radula‐muscle of buccinum undatum

The muscle fibres of the marine invertebrate Priapulus caudatus (Priapulida) are obliquely striated. Thin and thick filaments and characteristic dyad structures were recognized. The ultrastructural organization shows more resemblances with that of arthropod muscles than with that of annelids or molluscs. Pharmacological studies show that the muscles are provided with “primitive” C 16 type of acetylcholine receptors. Tubocurarine, succinylcholine and decamethonium do not block the effect of acetylcholine but potentiate this. This remarkable response may be due to inhibition of choline esterase. No distinct structural or functional differences were observed between somatic and visceral muscles, but the rectum showed evidence of the presence of unspecific amine receptors. The pharmacological responses resemble in the main those known from various simply organized invertebrate phyla. The priapulids, as suggested by Lang in 1953, may te survivors of a very ancient animal group.

Light Microscopical and Ultrastructural Organization of Muscles of Priapulus caudatus (Priapulida) and Their Responses to Drugs, with Phylogenetic Remarks

The ultrastructure of the main lymphomyeloid organs of the holocephalan fish, Chimaera monstrosa, is presented. The thymus is well developed even in adults. It is densely packed with small and large lymphocytes, the former predominating. The ultrastructure of C. monstrosa's lymphocytes is similar to that of mammalian ones. The lymphocytes show intimate connections with large epithelial reticulocytes, which infiltrate the cytoplasm of the lymphocytes with long processes. The lymphomyeloid tissues around the orbit are mainly granulocytopoietic. Two types of granulocytes occur: eosinophilic and heterophilic. The latter is found in excess. The granulocytes are ultrastructurally similar to those of elasmobranchs such as Etmopterus spinax and have similar characteristic granules. In addition to granulocytes in various stages, lymphocytes, plasma cells, blast cells, and solitary macrophages are scattered throughout the tissue. The suprapalatal region also has a similar supply and variety of cells, but most heterophilic granulocytes have modified granules. In the spleen, erythrocytes in different developmental stages are common. This confirms earlier studies which suggested that the spleen functions primarily as an erythrocytopoietic organ.

https://www.jstor.org/stable/pdfplus/1541631.pdf

Artur Mattisson

Papers

The lymphomyeloid (hemopoietic) system of the atlantic nurse shark, ginglymostoma cirratum

The cellular structure of the leydig organ in the shark, etmopterus spinax (l.)

Studies on the physiology of the radula‐muscle of buccinum undatum

Light Microscopical and Ultrastructural Organization of Muscles of Priapulus caudatus (Priapulida) and Their Responses to Drugs, with Phylogenetic Remarks

The cellular structure of lymphomyeloid tissues in chimaera monstrosa (pisces, holocephali)