Three-dimensional reconstruction of the embryonic pancreas in the grass snake Natrix natrix L. (Lepidosauria, Serpentes) based on histological studies

Kowalska, Magdalena; Hermyt, Mateusz; Rupik, Weronika

doi:10.1016/j.zool.2016.11.001

Cited by 11 publications

(26 citation statements)

References 92 publications

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“…It is worth mentioning that experimental data, such as histological images, provide only partial static information about the organogenesis of any organ [58]. That is why we applied tools that integrate these separate individual pieces of data into a 3D model.…”

Section: Introductionmentioning

confidence: 99%

Embryology of the VNO and associated structures in the grass snake Natrix natrix (Squamata: Natricinae): a 3D perspective

2017

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BackgroundSnakes are considered to be vomerolfaction specialists. They are members of one of the most diverse groups of vertebrates, Squamata. The vomeronasal organ and the associated structures (such as the lacrimal duct, choanal groove, lamina transversalis anterior and cupola Jacobsoni) of adult lizards and snakes have received much anatomical, histological, physiological and behavioural attention. However, only limited embryological investigation into these structures, constrained to some anatomical or cellular studies and brief surveys, has been carried out thus far. The purpose of this study was, first, to examine the embryonic development of the vomeronasal organ and the associated structures in the grass snake (Natrix natrix), using three-dimensional reconstructions based on histological studies, and, second, to compare the obtained results with those presented in known publications on other snakes and lizards.ResultsFive major developmental processes were taken into consideration in this study: separation of the vomeronasal organ from the nasal cavity and its specialization, development of the mushroom body, formation of the lacrimal duct, development of the cupola Jacobsoni and its relation to the vomeronasal nerve, and specialization of the sensory epithelium. Our visualizations showed the VNO in relation to the nasal cavity, choanal groove, lacrimal duct and cupola Jacobsoni at different embryonic stages. We confirmed that the choanal groove disappears gradually, which indicates that this structure is absent in adult grass snakes. On our histological sections, we observed a gradual growth in the height of the columns of the vomeronasal sensory epithelium and widening of the spaces between them.ConclusionsThe main ophidian taxa (Scolecophidia, Henophidia and Caenophidia), just like other squamate clades, seem to be evolutionarily conservative at some levels with respect to the VNO and associated structures morphology. Thus, it was possible to homologize certain embryonic levels of the anatomical and histological complexity, observed in the grass snake, with adult conditions of certain groups of Squamata. This may reflect evolutionary shift in Squamata from visually oriented predators to vomerolfaction specialists. Our descriptions offer material useful for future comparative studies of Squamata, both at their anatomical and histological levels.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-017-0188-y) contains supplementary material, which is available to authorized users.

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Section: Introductionmentioning

confidence: 99%

Embryology of the VNO and associated structures in the grass snake Natrix natrix (Squamata: Natricinae): a 3D perspective

2017

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“…Knowledge regarding the ultrastructure of endocrine cell differentiation in the pancreas of reptilian sauropsids is poor compared to other vertebrates. Only some hypotheses regarding their differentiation have been put forward, thus leading to certain generalizations being made about the evolutionary development of this organ in vertebrates in general (Kowalska et al, ). This study is the first to analyze the ultrastructural changes of the main endocrine pancreatic cells in the context of secretory granule differentiation in grass snake embryos at each developmental stage.…”

Section: Discussionmentioning

confidence: 99%

“…The pancreas is a glandular organ that is divided into an “exocrine” part, secreting digestive enzymes, and an “endocrine” part (Slack, ; Edlund, ; Pan & Wright, ). In reptilian sauropsids, the islets of the endocrine cells are not separated from the exocrine part of the pancreas by connective tissue (Miller, ; Kowalska, Hermyt, & Rupik, ), which is typical, for example, in mammals (Slack, ). The endocrine pancreas produces several hormones, including insulin, glucagon, somatostatin, and pancreatic polypeptide (Slack, ; Edlund, ).…”

Section: Introductionmentioning

confidence: 99%

Ultrastructure of endocrine pancreatic granules during pancreatic differentiation in the grass snake, Natrix natrix L. (Lepidosauria, Serpentes)

Kowalska

Rupik

2017

Journal of Morphology

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We used transmission electron microscopy to study the pancreatic main endocrine cell types in the embryos of the grass snake Natrix natrix L. with focus on the morphology of their secretory granules. The embryonic endocrine part of the pancreas in the grass snake contains four main types of cells (A, B, D, and PP), which is similar to other vertebrates. The B granules contained a moderately electron-dense crystalline-like core that was polygonal in shape and an electron-dense outer zone. The A granules had a spherical electron-dense eccentrically located core and a moderately electron-dense outer zone. The D granules were filled with a moderately electron-dense non-homogeneous content. The PP granules had a spherical electron-dense core with an electron translucent outer zone. Within the main types of granules (A, B, D, PP), different morphological subtypes were recognized that indicated their maturity, which may be related to the different content of these granules during the process of maturation. The sequence of pancreatic endocrine cell differentiation in grass snake embryos differs from that in many vertebrates. In the grass snake embryos, the B and D cells differentiated earlier than A and PP cells. The different sequence of endocrine cell differentiation in snakes and other vertebrates has been related to phylogenetic position and nutrition during early developmental stages.

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“…Recent studies have indicated that the embryonic pancreas in most vertebrates, just after fusion of the pancreatic buds, can be divided into two compartments: the “trunk” central part (Zhou et al, ) that is formed by the primitive ducts (Pan & Wright, ) and the “tip” branching ends (Shih et al, ). The pancreatic duct system develops by fusion of the dorsal and ventral pancreatic bud ducts (Kamisawa, Takuma, Egawa, Tsuruta, & Sasaki, ; Kowalska, Hermyt, & Rupik, ). During morphogenesis, the epithelial cells forming the embryonic ducts differentiate into several cell categories, such as ductal and endocrine in embryos (Bouwens & De Blay, ; Teitelman, Alpert, Polak, Martinez, & Hanahan, ) or light, basal, goblet, endocrine, and brush in adults (Madden & Sarras, ).…”

Section: Introductionmentioning

confidence: 99%

“…All papers regarding the structure and ultrastructure of the exocrine pancreas in reptilian sauropsids were focused on adult specimens of the freshwater turtle Chrysemys picta (Thiruvathukal & Thiruvathukal, ), Varanus exanthematicus (Godet, Mattei, & Dupé‐Godet, ), and the snake Waglerophis merremii (Sottovia‐Filho & Taga, ). However, our earlier studies allowed to reconstruct in detail and describe the formation of the main pancreatic duct and their connections during pancreas differentiation in grass snake embryos (Kowalska et al, ). Therefore, the aim of this study was to investigate the structural and ultrastructural differentiation of the ducts during exocrine pancreas development in grass snake embryos.…”

Section: Introductionmentioning

confidence: 99%

Development of the duct system during exocrine pancreas differentiation in the grass snake Natrix natrix (Lepidosauria, Serpentes)

Kowalska

Rupik

2018

Journal of Morphology

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We analyzed the development of the pancreatic ducts in grass snake Natrix natrix L. embryos with special focus on the three-dimensional (3D)-structure of the duct network, ultrastructural differentiation of ducts with attention to cell types and lumen formation. Our results indicated that the system of ducts in the embryonic pancreas of the grass snake can be divided into extralobular, intralobular, and intercalated ducts, similarly as in other vertebrate species. However, the pattern of branching was different from that in other vertebrates, which was related to the specific topography of the snake's internal organs. The process of duct remodeling in Natrix embryos began when the duct walls started to change from multilayered to single-layered and ended together with tube formation. It began in the dorsal pancreatic bud and proceeded toward the caudal direction. The lumen of pancreatic ducts differentiated by cavitation because a population of centrally located cells was cleared through cell death resembling anoikis. During embryonic development in the pancreatic duct walls of the grass snake four types of cells were present, that is, principal, endocrine, goblet, and basal cells, which is different from other vertebrate species. The principal cells were electron-dense, contained indented nuclei with abundant heterochromatin, microvilli and cilia, and were connected by interdigitations of lateral membranes and junctional complexes. The endocrine cells were electron-translucent and some of them included endocrine granules. The goblet cells were filled with large granules with nonhomogeneous, moderately electron-dense material. The basal cells were small, electron-dense, and did not reach the duct lumen.

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Three-dimensional reconstruction of the embryonic pancreas in the grass snake Natrix natrix L. (Lepidosauria, Serpentes) based on histological studies

Cited by 11 publications

References 92 publications

Embryology of the VNO and associated structures in the grass snake Natrix natrix (Squamata: Natricinae): a 3D perspective

Embryology of the VNO and associated structures in the grass snake Natrix natrix (Squamata: Natricinae): a 3D perspective

Ultrastructure of endocrine pancreatic granules during pancreatic differentiation in the grass snake, Natrix natrix L. (Lepidosauria, Serpentes)

Development of the duct system during exocrine pancreas differentiation in the grass snake Natrix natrix (Lepidosauria, Serpentes)

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