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Embryonic development of glial cells and myelin in the shark, Chiloscyllium punctatum.

ABSTRACT: Glial cells are responsible for a wide range of functions in the nervous system of vertebrates. The myelinated nervous systems of extant elasmobranchs have the longest independent history of all gnathostomes. Much is known about the development of glia in other jawed vertebrates, but research in elasmobranchs is just beginning to reveal the mechanisms guiding neurodevelopment. This study examines the development of glial cells in the bamboo shark, Chiloscyllium punctatum, by identifying the expression pattern of several classic glial and myelin proteins. We show for the first time that glial development in the bamboo shark (C. punctamum) embryo follows closely the one observed in other vertebrates and that neural development seems to proceed at a faster rate in the PNS than in the CNS. In addition, we observed more myelinated tracts in the PNS than in the CNS, and as early as stage 32, suggesting that the ontogeny of myelin in sharks is closer to osteichthyans than agnathans.

SUBMITTER: Rotenstein L

PROVIDER: S-EPMC2783534 | biostudies-literature | 2009 Dec

REPOSITORIES: biostudies-literature

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Embryonic development of glial cells and myelin in the shark, Chiloscyllium punctatum.

Rotenstein Lisa L Milanes Anthony A Juarez Marilyn M Reyes Michelle M de Bellard Maria Elena ME

Gene expression patterns : GEP 20090904 8

Glial cells are responsible for a wide range of functions in the nervous system of vertebrates. The myelinated nervous systems of extant elasmobranchs have the longest independent history of all gnathostomes. Much is known about the development of glia in other jawed vertebrates, but research in elasmobranchs is just beginning to reveal the mechanisms guiding neurodevelopment. This study examines the development of glial cells in the bamboo shark, Chiloscyllium punctatum, by identifying the expr ...[more]

PMID: 19733690

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Project description:There is currently a limited understanding of the morphological and functional organization of the olfactory system in cartilaginous fishes, particularly when compared to bony fishes and terrestrial vertebrates. In this fish group, there is a clear paucity of information on the characterization, density, and distribution of olfactory receptor neurons (ORNs) within the sensory olfactory epithelium lining the paired olfactory rosettes, and their functional implications with respect to the hydrodynamics of incurrent water flow into the nares. This imaging study examines the brownbanded bamboo shark Chiloscyllium punctatum (Elasmobranchii) and combines immunohistochemical labeling using antisera raised against five G-protein α-subunits (Gαs/olf, Gαq/ 11 / 14, Gαi- 1 / 2 / 3, Gαi- 3, Gα o ) with light and electron microscopy, to characterize the morphological ORN types present. Three main ORNs ("long", "microvillous" and "crypt-like") are confirmed and up to three additional microvilli-bearing types are also described; "Kappe-like" (potential or homologous "Kappe" as in teleosts), "pear-shaped" and "teardrop-shaped" cells. These morphotypes will need to be confirmed molecularly in the future. Using X-ray diffusible iodine-based contrast-enhanced computed tomography (diceCT), high-resolution scans of the olfactory rosettes, olfactory bulbs (OBs), peduncles, and telencephalon reveal a lateral segregation of primary olfactory inputs within the OBs, with distinct medial and lateral clusters of glomeruli, suggesting a potential somatotopic organization. However, most ORN morphotypes are found to be ubiquitously distributed within the medial and lateral regions of the olfactory rosette, with at least three microvilli-bearing ORNs labeled with anti-Gα o found in significantly higher densities in lateral lamellae [in lateral lamellae] and on the anterior portion of lamellae (facing the olfactory cavity). These microvilli-bearing ORN morphotypes (microvillous, "Kappe-like," "pear-shaped," and "teardrop-shaped") are the most abundant across the olfactory rosette of this species, while ciliated ORNs are less common and crypt cells are rare. Spatial simulations of the fluid dynamics of the incurrent water flow into the nares and within the olfactory cavities indicate that the high densities of microvilli-bearing ORNs located within the lateral region of the rosette are important for sampling incoming odorants during swimming and may determine subsequent tracking behavior.

Dataset Information

Embryonic development of glial cells and myelin in the shark, Chiloscyllium punctatum.

Publications

Embryonic development of glial cells and myelin in the shark, Chiloscyllium punctatum.

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