@article{2-s2.0-85201060242,

title = {Breaking through the eggshell: embryonic development of the premaxillary dentition in Lacerta agilis (Squamata: Unidentata) with special emphasis on the egg tooth},

author = { P. Kaczmarek and B. Metscher and M. Kowalska and W. Rupik},

url = {https://www.scopus.com/inward/record.uri?eid=2-s2.0-85201060242&doi=10.1093%2fzoolinnean%2fzlae096&partnerID=40&md5=ea37b6681220f3eeb131d8f9ffd7d2bb},

doi = {10.1093/zoolinnean/zlae096},

year  = {2024},

date = {2024-01-01},

journal = {Zoological Journal of the Linnean Society},

volume = {201},

number = {4},

publisher = {Oxford University Press},

abstract = {The egg tooth of squamates is a true tooth that allows them to break, tear, or cut the eggshell during hatching. In this clade there are some uncertainties concerning the egg tooth implantation geometry, the number of germs, and their fates during embryonic development. Here, we used X-ray microtomography and light microscopy, focusing on the egg tooth and remaining premaxillary teeth of the sand lizard (Lacerta agilis; Squamata: Unidentata). The developing egg tooth of this species passes through all the classic stages of tooth development. We did not find any evidence that the large size of the egg tooth is related to the merging of two egg tooth germs, which has recently been suggested to occur in snakes. Instead, this feature can be attributed to the delayed formation of the neighbouring regular premaxillary teeth. This might provide more resources to the developing egg tooth. At the last developmental stage, the egg tooth is a large, midline structure, bent forward as in most oviparous Unidentata. It is characterized by pleurodont implantation, and its base is attached to the pleura and a peculiar ridge of the alveolar bone. The attachment tissue contains periodontal ligament-like tissue, acellular cementum-like tissue, and alveolar bone. © The Author(s) 2024.},

note = {0},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{2-s2.0-85189627626,

title = {Does the pancreas of gekkotans differentiate similarly? Developmental structural and 3D studies of the mourning gecko (Lepidodactylus lugubris) and the leopard gecko (Eublepharis macularius)},

author = { M. Kowalska and P. Kaczmarek and W. Rupik},

url = {https://www.scopus.com/inward/record.uri?eid=2-s2.0-85189627626&doi=10.1111%2fjoa.14038&partnerID=40&md5=723d9ff7efad541373c59ae09e28afdc},

doi = {10.1111/joa.14038},

year  = {2024},

date = {2024-01-01},

journal = {Journal of Anatomy},

volume = {245},

number = {2},

pages = {303-323},

publisher = {John Wiley and Sons Inc},

abstract = {This study investigated the pancreas differentiation of two species of gekkotan families—the mourning gecko Lepidodactylus lugubris (Gekkonidae) and the leopard gecko Eublepharis macularius (Eublepharidae)—based on two-dimensional (2D) histological samples and three-dimensional (3D) reconstructions of the position of the pancreatic buds and the surrounding organs. The results showed that at the moment of egg laying, the pancreas of L. lugubris is composed of three distinct primordia: one dorsal and two ventral. The dorsal primordium differentiates earlier than either ventral primordium. The right ventral primordium is more prominent and distinctive, starting to form earlier than the left one. Moreover, at this time, the pancreas of the leopard gecko is composed of the dorsal and right ventral primordium and the duct of the left ventral primordium. It means that the leopard gecko's left primordium is a transitional structure. These results indicate that the early development of the gekkotan pancreas is species specific. The pancreatic buds of the leopard and mourning gecko initially enter the duodenum by separate outlets, similar to the pancreas of other vertebrates. The pancreatic buds (3 of the mourning gecko and 2 of the leopard gecko) fuse quickly and form an embryonic pancreas. After that, the structure of this organ changes. After fusion, the pancreas of both gekkotans comprises four parts: the head of the pancreas (central region) and three lobes: upper, splenic, and lower. This organ develops gradually and is very well distinguished at hatching time. In both gekkotan species, cystic, hepatic, and pancreatic ducts enter the duodenum within the papilla. During gekkotan pancreas differentiation, the connection between the common bile duct and the dorsal pancreatic duct is associated with intestinal rotation, similar to other vertebrates. © 2024 Anatomical Society.},

note = {0},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{2-s2.0-85110091670,

title = {Architecture of the pancreatic islets and endocrine cell arrangement in the embryonic pancreas of the grass snake (Natrix natrix l.). immunocytochemical studies and 3d reconstructions},

author = { M. Kowalska and W. Rupik},

url = {https://www.scopus.com/inward/record.uri?eid=2-s2.0-85110091670&doi=10.3390%2fijms22147601&partnerID=40&md5=27d914c871dc5ee2c5feab58737a688c},

doi = {10.3390/ijms22147601},

issn = {16616596},

year  = {2021},

date = {2021-01-01},

journal = {International Journal of Molecular Sciences},

volume = {22},

number = {14},

publisher = {MDPI},

abstract = {During the early developmental stages of grass snakes, within the differentiating pancreas, cords of endocrine cells are formed. They differentiate into agglomerates of large islets flanked throughout subsequent developmental stages by small groups of endocrine cells forming islets. The islets are located within the cephalic part of the dorsal pancreas. At the end of the embryonic period, the pancreatic islet agglomerates branch off, and as a result of their remodeling, surround the splenic “bulb”. The stage of pancreatic endocrine ring formation is the first step in formation of intrasplenic islets characteristics for the adult specimens of the grass snake. The arrangement of endocrine cells within islets changes during pancreas differentiation. Initially, the core of islets formed from B and D cells is surrounded by a cluster of A cells. Subsequently, A, B, and D endocrine cells are mixed throughout the islets. Before grass snake hatching, A and B endocrine cells are intermingled within the islets, but D cells are arranged centrally. Moreover, the pancreatic polypeptide (PP) cells are not found within the embryonic pancreas of the grass snake. Variation in the proportions of different cell types, depending on the part of the pancreas, may affect the islet function—a higher proportion of glucagon cells is beneficial for insulin secretion. © 2021 by the authors. Licensee MDPI, Basel, Switzerland.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{2-s2.0-85074968598,

title = {Development of pancreatic acini in embryos of the grass snake Natrix natrix (Lepidosauria, Serpentes)},

author = { M. Kowalska and W. Rupik},

url = {https://www.scopus.com/inward/record.uri?eid=2-s2.0-85074968598&doi=10.1002%2fjmor.21083&partnerID=40&md5=1f685f56b11f1dba13de3f9cc50cdd91},

doi = {10.1002/jmor.21083},

issn = {03622525},

year  = {2020},

date = {2020-01-01},

journal = {Journal of Morphology},

volume = {281},

number = {1},

pages = {110-121},

publisher = {John Wiley and Sons Inc.},

abstract = {This study report about the differentiation of pancreatic acinar tissue in grass snake, Natrix natrix, embryos using light microscopy, transmission electron microscopy, and immuno-gold labeling. Differentiation of acinar cells in the embryonic pancreas of the grass snake is similar to that of other amniotes. Pancreatic acini occurred for the first time at Stage VIII, which is the midpoint of embryonic development. Two pattern of acinar cell differentiation were observed. The first involved formation of zymogen granules followed by cell migration from ducts. In the second, one zymogen granule was formed at the end of acinar cell differentiation. During embryonic development in the pancreatic acini of N. natrix, five types of zymogen granules were established, which correlated with the degree of their maturation and condensation. Within differentiating acini of the studied species, three types of cells were present: acinar, centroacinar, and endocrine cells. The origin of acinar cells as well as centroacinar cells in the pancreas of the studied species was the pancreatic ducts, which is similar as in other vertebrates. In the differentiating pancreatic acini of N. natrix, intermediate cells were not present. It may be related to the lack of transdifferentiation activity of acinar cells in the studied species. Amylase activity of exocrine pancreas was detected only at the end of embryonic development, which may be related to animal feeding after hatching from external sources that are rich in carbohydrates and presence of digestive enzymes in the egg yolk. Mitotic division of acinar cells was the main mechanism of expansion of acinar tissue during pancreas differentiation in the grass snake embryos. © 2019 Wiley Periodicals, Inc.},

note = {4},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{2-s2.0-85057717468,

title = {Development of endocrine pancreatic islets in embryos of the grass snake Natrix natrix (Lepidosauria, Serpentes)},

author = { M. Kowalska and W. Rupik},

url = {https://www.scopus.com/inward/record.uri?eid=2-s2.0-85057717468&doi=10.1002%2fjmor.20921&partnerID=40&md5=dcc2083d3c63dc576cab6f20d320812b},

doi = {10.1002/jmor.20921},

issn = {03622525},

year  = {2019},

date = {2019-01-01},

journal = {Journal of Morphology},

volume = {280},

number = {1},

pages = {103-118},

publisher = {John Wiley and Sons Inc.},

abstract = {Differentiation of the pancreatic islets in grass snake Natrix natrix embryos, was analyzed using light, transmission electron microscopy, and immuno-gold labeling. The study focuses on the origin of islets, mode of islet formation, and cell arrangement within islets. Two waves of pancreatic islet formation in grass snake embryos were described. The first wave begins just after egg laying when precursors of endocrine cells located within large cell agglomerates in the dorsal pancreatic bud differentiate. The large cell agglomerates were divided by mesenchymal cells thus forming the first islets. This mode of islet formation is described as fission. During the second wave of pancreatic islet formation which is related to the formation of the duct mantle, we observed four phases of islet formation: (a) differentiation of individual endocrine cells from the progenitor layer of duct walls (budding) and their incomplete delamination; (b) formation of two types of small groups of endocrine cells (A/D and B) in the wall of pancreatic ducts; (c) joining groups of cells emerging from neighboring ducts (fusion) and rearrangement of cells within islets; (d) differentiated pancreatic islets with characteristic arrangement of endocrine cells. Mature pancreatic islets of the grass snake contained mainly A endocrine cells. Single B and D or PP–cells were present at the periphery of the islets. This arrangement of endocrine cells within pancreatic islets of the grass snake differs from that reported from most others vertebrate species. Endocrine cells in the pancreas of grass snake embryos were also present in the walls of intralobular and intercalated ducts. At hatching, some endocrine cells were in contact with the lumen of the pancreatic ducts. © 2018 Wiley Periodicals, Inc.},

note = {3},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{2-s2.0-85042195388,

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

author = { M. Kowalska and W. Rupik},

url = {https://www.scopus.com/inward/record.uri?eid=2-s2.0-85042195388&doi=10.1002%2fjmor.20806&partnerID=40&md5=e83d21d8301f76949b980279e6d18ab7},

doi = {10.1002/jmor.20806},

issn = {03622525},

year  = {2018},

date = {2018-01-01},

journal = {Journal of Morphology},

volume = {279},

number = {6},

pages = {724-746},

publisher = {John Wiley and Sons Inc.},

abstract = {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. © 2018 Wiley Periodicals, Inc.},

note = {4},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{2-s2.0-85034220441,

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

author = { M. Kowalska and W. Rupik},

url = {https://www.scopus.com/inward/record.uri?eid=2-s2.0-85034220441&doi=10.1002%2fjmor.20775&partnerID=40&md5=209b09e79fe0a39e8414e6373be3ca69},

doi = {10.1002/jmor.20775},

issn = {03622525},

year  = {2018},

date = {2018-01-01},

journal = {Journal of Morphology},

volume = {279},

number = {3},

pages = {330-348},

publisher = {John Wiley and Sons Inc.},

abstract = {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. © 2017 Wiley Periodicals, Inc.},

note = {3},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{2-s2.0-85007246649,

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

author = { M. Kowalska and M. Hermyt and W. Rupik},

url = {https://www.scopus.com/inward/record.uri?eid=2-s2.0-85007246649&doi=10.1016%2fj.zool.2016.11.001&partnerID=40&md5=52e8d777d89953be1011a672b2e37199},

doi = {10.1016/j.zool.2016.11.001},

issn = {09442006},

year  = {2017},

date = {2017-01-01},

journal = {Zoology},

volume = {121},

pages = {91-110},

publisher = {Elsevier GmbH},

abstract = {The aim of this study was to evaluate two research hypotheses: H0–the embryonic pancreas in grass snakes develops in the same manner as in all previously investigated amniotes (from three buds) and its topographical localization within the adult body has no relation to its development; H1–the pancreas develops in a different manner and is related to the different topography of internal organs in snakes. For the evaluation of these hypotheses we used histological methods and three-dimensional (3D) reconstructions of the position of the pancreatic buds and surrounding organs at particular developmental stages and of the final position and shape of the pancreatic gland. Our results indicate that the pancreas primordium in the grass snake is formed by only two buds – a dorsal and a ventral one – that are not connected until the end of stage II. This differs from the majority of vertebrates investigated so far. The gall bladder of the grass snake embryos is connected with the liver only by a thin cystic duct, which also differs from many other vertebrates. Our histological study also indicates a different distribution of the endocrine cells in the embryonic pancreas of the grass snake because the first endocrine cells appeared in the dorsal part of the pancreas in a region located close to the spleen. During the entire developmental period no evidence of these cells was found in the ventral part of the pancreas. The endocrine cells form elongated, large and irregular-shaped islets. They can also form structures resembling “inverted acini”. Such an arrangement is characteristic of snakes only. The differentiating pancreas penetrates the ventral part of the developing spleen and divides it into three separate parts at developmental stage IX. This is unique among vertebrates. At the end of the embryonic development (stage XI), the pancreas, the spleen and the gall bladder are located in close proximity and form the so-called triad. Our results suggest that the untypical topography of the organ systems in snakes may determine the unique development of the pancreas in these animals. © 2016 Elsevier GmbH},

note = {10},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{2-s2.0-85001013353,

title = {Development of the egg tooth – The tool facilitating hatching of squamates: Lessons from the grass snake Natrix natrix},

author = { M. Hermyt and P. Kaczmarek and M. Kowalska and W. Rupik},

url = {https://www.scopus.com/inward/record.uri?eid=2-s2.0-85001013353&doi=10.1016%2fj.jcz.2016.11.001&partnerID=40&md5=9b619f3b9c90ec4f8ccb6e7c204049ae},

doi = {10.1016/j.jcz.2016.11.001},

issn = {00445231},

year  = {2017},

date = {2017-01-01},

journal = {Zoologischer Anzeiger},

volume = {266},

pages = {61-70},

publisher = {Elsevier GmbH},

abstract = {Most embryos of squamates use their egg tooth to facilitate hatching when their development is completed. After they are out of the shell, this tooth is shed and, in the case, of the grass snake (Natrix natrix), not replaced by a successor teeth. The structure of this transient tooth resembles the development and histology of the regular teeth of vertebrates. Morphological, histological and scanning electron microscopic observations indicated that the egg tooth of the grass snake has four developmental phases. Like the teeth of other vertebrate species, it undergoes oral epithelium thickening as well as the bud, cap and bell phases. However, due to the specialised function it performs, the egg tooth differs significantly from the other teeth both in its morphology and development. The egg tooth of Natrix natrix embryos is an unpaired true tooth, as in most squamates. Our study indicated that the egg tooth started its development in the rostral part of the snout by the thickening of the oral epithelium and there was a condensation of mesenchyme underneath it. It formed very early, around developmental stage III, at approximately the same time as the null-generation teeth. After the thickening of the oral epithelium, only one tooth germ is formed, in contrast to lizards in which two germs can be observed during their embryonic life; however, in the course of development, one regressed and the other shifted into the midline position and developed into the functional egg tooth. The next step in the egg tooth development was the differentiation of the enamel organ and the dental papilla. Three layers of the enamel organ developed – the inner enamel epithelium, the stellate reticulum and the outer enamel epithelium, while a superficial layer of the dental papilla differentiated into the odontoblasts. The egg tooth was ready to erupt when its development ended at developmental stage XII, after the hard tissues developed. © 2016 Elsevier GmbH},

note = {15},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{2-s2.0-84959522869,

title = {Ultrastructural features of the differentiating thyroid primordium in the sand lizard (Lacerta agilis L.) from the differentiation of the cellular cords to the formation of the follicular lumen},

author = { W. Rupik and M. Kowalska and E. Swadźba and R. Maślak},

url = {https://www.scopus.com/inward/record.uri?eid=2-s2.0-84959522869&doi=10.1016%2fj.zool.2015.12.005&partnerID=40&md5=fa1c760500363c79738b246a51192d88},

doi = {10.1016/j.zool.2015.12.005},

issn = {09442006},

year  = {2016},

date = {2016-01-01},

journal = {Zoology},

volume = {119},

number = {2},

pages = {97-112},

publisher = {Elsevier GmbH},

abstract = {The differentiation of the thyroid primordium of lacertilian species is poorly understood. The present study reports on the ultrastructural analysis of the developing thyroid primordium in the sand lizard (Lacerta agilis) during the early stages of differentiation. The early thyroid primordium of sand lizard embryos was composed of cellular cords that contained single cells with a giant lipid droplet, which were eliminated by specific autophagy (lipophagy). The follicular lumens at the periphery of the primordium differentiated even before the division of the cellular cords. When the single cells within the cords started to die through paraptosis, the adjacent cells started to polarise and junctional complexes began to form around them. After polarisation and clearing up after the formation of the lumens, the cellular cords divided into definitive follicles. The cellular cords in the central part of the primordium started to differentiate later than those at the periphery. The cellular cords divided into presumptive follicles first and only later differentiated into definitive follicles. During this process, a population of centrally located cells was removed through apoptosis to form the lumen. Although the follicular lumen in sand lizard embryos is differentiated by cavitation similar to that in the grass snake, there were very important differences during the early stages of the differentiation of the cellular cords and the formation of the thyroid follicles. © 2016 Elsevier GmbH.},

note = {9},

keywords = {},

pubstate = {published},

tppubtype = {article}

}