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Ann Huysseune - One of the best experts on this subject based on the ideXlab platform.
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Epithelial Label-Retaining Cells Are Absent during Tooth Cycling in Salmo salar and Polypterus senegalus.
PloS one, 2016Co-Authors: Sam Vandenplas, Maxime Willems, P. Eckhard Witten, Tom Hansen, Per Gunnar Fjelldal, Ann HuysseuneAbstract:The Atlantic salmon (Salmo salar) and African bichir (Polypterus senegalus) are both actinopterygian fish species that continuously replace their teeth without the involvement of a successional dental lamina. Instead, they share the presence of a middle dental epithelium: an epithelial tier enclosed by inner and outer dental epithelium. It has been hypothesized that this tier could functionally substitute for a successional dental lamina and might be a potential niche to house epithelial stem cells involved in tooth cycling. Therefore, in this study we performed a BrdU pulse chase experiment on both species to (1) determine the localization and extent of proliferating cells in the dental epithelial layers, (2) describe cell dynamics and (3) investigate if label-retaining cells are present, suggestive for the putative presence of stem cells. Cells proliferate in the middle dental epithelium, outer dental epithelium and cervical loop at the lingual side of the dental organ to form a new tooth germ. Using long chase times, both in S. salar (eight weeks) and P. senegalus (eight weeks and twelve weeks), we could not reveal the presence of label-retaining cells in the dental organ. Immunostaining of P. senegalus dental organs for the transcription factor Sox2, often used as a stem cell marker, labelled cells in the zone of outer dental epithelium which grades into the oral epithelium (ODE transition zone) and the inner dental epithelium of a successor only. The location of Sox2 distribution does not provide evidence for epithelial stem cells in the dental organ and, more specifically, in the middle dental epithelium. Comparison of S. salar and P. senegalus reveals shared traits in tooth cycling and thus advances our understanding of the developmental mechanism that ensures lifelong replacement.
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A comparison of the larval and juvenile dentition in Polypterus senegalus
Journal of Applied Ichthyology, 2014Co-Authors: A. De Clercq, Sam Vandenplas, Ann HuysseuneAbstract:Summary Polypterus senegalus is a freshwater fish belonging to the earliest diverged group of the actinopterygian lineage with currently living representatives. Its dentition has been well characterized in terms of distribution and shape of teeth in different life stages. Additionally, structural features of the first-generation teeth have been briefly described. However, at present it is not known how the primary dentition is patterned and if this pattern is similar to that found in juveniles. In this preliminary study, to answer this question we investigate the tooth pattern of a larval P. senegalus based on serial sections and 3D reconstructions, and compare dental features in larvae and juveniles. Polypterus senegalus passive apterolarvae possess a well developed primary dentition. Dentigerous bones develop either prior to the teeth (dentary, retroarticular), or as an attachment site concomitant with the expanding dentition (coronoid 1). Most teeth are attached and erupted, and thus considered functional, and their pulp houses a blood vessel, two features that contrast with earlier findings. The primary teeth do not display a level of maturation that could reflect a particular order of development. New teeth are added anteriorly, and likely also posteriorly, to allow the tooth row to grow to keep pace with the growing jaw. Replacement teeth are absent at this stage. Thus, the pattern observed in juveniles, with alternate (odd and even) positions displaying a different level of tooth maturation, is not present in the larva. Most strikingly, in the larva, considerable symmetry exists between apparently random patterns on both dentaries, eliciting intriguing questions on left-right control to be addressed in future studies.
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Tooth replacement without a dental lamina: The search for epithelial stem cells in Polypterus senegalus
Journal of experimental zoology. Part B Molecular and developmental evolution, 2014Co-Authors: Sam Vandenplas, Adelbert De Clercq, Ann HuysseuneAbstract:Most actinopterygians replace their teeth continuously throughout life. To address the question of where and how replacement teeth form in actinopterygians, it is advisable to investigate well-chosen representatives within the lineage. The African bichir, Polypterus senegalus, belongs to the earliest diverged group of the actinopterygian lineage with currently living representatives. Its well characterized dentition, together with its phylogenetic position, make this species an attractive model to answer following questions: (1) when and where does the replacement tooth form and how is it connected with the dental organ of the predecessor, and (2) is there any evidence for the presence of epithelial stem cells, hypothesized to play a role in replacement? Serial sections show that one tooth family can contain up to three members, which are all interconnected by dental epithelium. Replacement teeth develop without the presence of a successional dental lamina. We propose that this is the plesiomorphic condition for tooth replacement in actinopterygians. BrdU pulse-chase experiments reveal cells in the outer and middle dental epithelium, proliferating at the time of initiation of a new replacement tooth. It is tempting to assume that these cell layers provide a stem cell niche. The observed absence of label-retaining cells after long chase times (up to 8 weeks) is held against the light of divergent views on cell cycling properties of stem cells. At present, our data do not support, neither reject, the hypothesis on involvement of epithelial stem cells within the process of continuous tooth replacement. J. Exp. Zool. (Mol. Dev. Evol.) 322B: 281–293, 2014. © 2014 Wiley Periodicals, Inc.
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Aspects of tooth replacement in a basal actinopterygian, Polypterus senegalus
2013Co-Authors: Sam Vandenplas, Adelbert De Clercq, Ann HuysseuneAbstract:Most actinopterygians replace their teeth continuously throughout life. Major differences are nevertheless observed in the spatial and temporal relationship between a developing replacement tooth and its predecessor. In this study we address the question of where and how replacement teeth form in the African bichir (Polypterus senegalus). Furthermore we test if there is any evidence for the presence of epithelial stem cells, hypothesized to play a role in replacement [1]. The bichirs’ well characterized dentition [2], together with its basal phylogenetic position, make this species an attractive model to answer these questions. We investigated stages of tooth development and replacement in juvenile bichirs of approx. 12 cm, using histological sections. A BrdU pulse-chase experiment was conducted on 20 juvenile Polypterus senegalus, to visualize label retaining cells. Dentary teeth are organized in one row. Each tooth family was observed to house three members: one functional tooth showing resorption, its successor in late cytodifferentiation, and a secondary successor in morphogenesis stage. Replacement teeth in cytodifferentiation stage showed proliferation in their cervical loop and the postero-lingual side of the outer dental epithelium. This is the site of the initiation of a new replacement tooth. No clear successional lamina was observed to connect the functional tooth and its successor. No label retaining cells were observed in the dental organ after 4 and 8-weeks chase time. A weak and mostly scattered BrdU signal was nevertheless observed in the basal layer of the oral epithelium. Together, our data suggest that a replacement tooth develops directly from the dental organ of the functional tooth. Furthermore, the lack of label retaining cells in the predecessor requires reconsideration of mechanisms of tooth replacement. Reference: [1] Huysseune et al. BioEssays (2004); [2] Wacker et al. Ann. anat. (2001)
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Identification of potential epithelial stem cells responsible for continuous tooth replacement in the African bichir (Polypterus senegalus), a basal Osteichtyan
2012Co-Authors: Adelbert De Clercq, Sam Vandenplas, Ann HuysseuneAbstract:In this thesis we wished to test the hypothesis that stem cells are involved in the process of continuous tooth replacement in the basal actinopterygian, Polypterus senegalus (African bichir). First, we studied the morphology of the dentition and the tooth replacement pattern on the premaxillary, maxillary and dentary, using cleared and alizarin red stained heads of juvenile Polypterus. Each of these bones bears one row of functional teeth. In addition, a replacement tooth develops at the lingual and posterior side of each single functional tooth. Functional teeth of a similar stage of maturation tended to be in alternate tooth positions. Two mechanisms are proposed to explain this alternate pattern. Using serially sectioned heads of juvenile fish, we could next reveal the cellular details of the replacement process. The anlage of the replacement tooth is first seen as a local differentiation of the outer dental epithelium of the predecessor, at its postero-lingual side. Throughout the development of the replacement tooth, an epithelial cell population, termed here the ‘middle dental epithelium’, connects the predecessor to the replacement tooth. The bulk of the cells of the ‘middle dental epithelium’ are irregular and separated by small intercellular spaces. In contrast, the cells closely opposed to the inner dental epithelium of the replacement tooth have a stellate reticulum phenotype. The mode of tooth replacement in Polypterus senegalus displays several characters highly similar to those observed in Atlantic salmon (Salmo salar). In the second part of this study we concentrated on the proliferation pattern and the identification of label retaining cells using PCNA (proliferating cell nuclear antigen) and BrdU (bromodeoxyuridine) immunostaining, resp. Proliferation was found in the preodontoblasts and dental organ of the replacement tooth. Strikingly, we found a focus of proliferating cells in the outer dental epithelium of the replacement tooth. This is the presumptive site of initiation of a third tooth family member. In addition, these proliferating cells could represent a transient amplifying cell population, suggesting the possible presence of putative stem cells in the outer dental epithelium of the replacement tooth. To identify label retaining cells we adapted a BrdU pulse-chase experiment for use on Polypterus senegalus. After two weeks of chase time we still observed a number of BrdU positive cells in the outer dental epithelium of the replacement tooth. In addition there were a few labeled cells in the ‘middle dental epithelium’ postero-lingual of the replacement tooth. After four weeks of chase time labeled cells were found in the basal layer of the oral epithelium only. In conclusion, we are tempted to speculate that putative dental stem cells could be localized in the outer dental epithelium of the replacement tooth, in the ‘middle dental epithelium’ or in the oral epithelium. The presence and exact location of dental stem cells in the process of continuous tooth replacement of Polypterus senegalus needs to be further explored.
Emily M Standen - One of the best experts on this subject based on the ideXlab platform.
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Terrestrial acclimation and exercise lead to bone functional response in Polypterus senegalus pectoral fins.
The Journal of experimental biology, 2020Co-Authors: Emily M StandenAbstract:The ability of bones to sense and respond to mechanical loading is a central feature of vertebrate skeletons. However, the functional demands imposed on terrestrial and aquatic animals differ vastly. The pectoral girdle of the basal actinopterygian fish Polypterus senegalus was previously shown to exhibit plasticity following terrestrial acclimation, but the pectoral fin itself has yet to be examined. We investigated skeletal plasticity in the pectoral fins of P. senegalus after exposure to terrestrial loading. Juvenile fish were divided into three groups: a control group was kept under aquatic conditions without intervention, an exercised group was also kept in water but received daily exercise on land, and a terrestrial group was kept in a chronic semi-terrestrial condition. After 5 weeks, the pectoral fins were cleared and stained with Alcian Blue and Alizarin Red to visualize cartilage and bone, allowing measurements of bone length, bone width, ossification and curvature to be taken for the endochondral radial bones. Polypterus senegalus fin bones responded most strongly to chronic loading in the terrestrial condition. Fish that were reared in a terrestrial environment had significantly longer bones compared with those of aquatic controls, wider propterygia and metapterygia, and more ossified metapterygia and medial radials, and they showed changes in propterygial curvature. Exercised fish also had longer and more ossified medial radials compared with those of controls. Polypterus senegalus fin bones exhibit plasticity in response to novel terrestrial loading. Such plasticity could be relevant for transitions between water and land on evolutionary scales, but key differences between fish and tetrapod bone make direct comparisons challenging.
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Gill remodelling during terrestrial acclimation in the amphibious fish Polypterus senegalus.
Journal of morphology, 2019Co-Authors: Andy J. Turko, Priyam Maini, Patricia A. Wright, Emily M StandenAbstract:Fishes are effectively weightless in water due to the buoyant support of the environment, but amphibious fishes must cope with increased effective weight when on land. Delicate structures such as gills are especially vulnerable to collapse and loss of surface area out of water. We tested the 'structural support' hypothesis that amphibious Polypterus senegalus solve this problem using phenotypically plastic changes that provide mechanical support and increase stiffness at the level of the gill lamellae, the filaments, and the whole arches. After 7 d in terrestrial conditions, enlargement of an inter-lamellar cell mass filled the water channels between gill lamellae, possibly to provide structural support and/or reduce evaporative water loss. Similar gill remodelling has been described in several other actinopterygian fishes, suggesting this may be an ancestral trait. There was no change in the mechanical properties or collagen composition of filaments or arches after 7 days out of water, but 8 months of terrestrial acclimation caused a reduction in gill arch length and mineralized bone volume. Thus, rather than increasing the size and stiffness of the gill skeleton, P. senegalus may instead reduce investment in supportive gill tissue while on land. These results are strikingly similar to the evolutionary trend of gill loss that occurred during the tetrapod invasion of land, raising the possibility that genetic assimilation of gill plasticity was an underlying mechanism.
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Aerial and aquatic visual acuity of the grey bichir Polypterus senegalus, as estimated by optokinetic response.
Journal of fish biology, 2018Co-Authors: Katherine R Znotinas, Emily M StandenAbstract:The present study assessed the aerial and aquatic visual abilities of juvenile grey bichir Polypterus senegalus, fish capable of terrestrial locomotion, by measuring the optokinetic response to stimuli of varying speed and spatial frequency. In water, fish tracked slow-moving (2° s-1 ) stimuli moderately well and fast-moving stimuli very poorly. Spatial acuity was very low compared with many other species, with maximum response observed at 0.05-0.075 stimulus cycles per degree of visual arc; however, it should be noted that adult fish, with their larger eyes, are likely to have somewhat improved spatial acuity. Low spatial acuity and limited stimulus tracking ability might be expected in a nocturnal ambush predator such as P. senegalus, where gaze stabilization may be less crucial and other sensory inputs may have greater importance in perception of the environment. In air, spatial and temporal acuity were both poorer by every measure, but some visual ability persisted. As the eye shows no anatomical specialization for aerial vision, poor vision was expected; however, the large decrease in saccade velocity observed in air trials was unexpected. Stimulus parameters typically have little effect on the characteristics of the saccade, so this finding may suggest that the function of the reflex system itself could be compromised in the aerial vision of some fishes capable of terrestrial locomotion.
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Fin and body neuromuscular coordination changes during walking and swimming in Polypterus senegalus
The Journal of Experimental Biology, 2018Co-Authors: Kathleen L. Foster, Misha Dhuper, Emily M StandenAbstract:The ability to modulate the function of muscle is integral to an animal's ability to function effectively in the face of widely disparate challenges. This modulation of function can manifest through short-term changes in neuromuscular control, but also through long-term changes in force profiles, fatiguability and architecture. However, the relative extent to which shorter-term modulation and longer-term plasticity govern locomotor flexibility remains unclear. Here, we obtain simultaneously recorded kinematic and muscle activity data of fin and body musculature of an amphibious fish, Polypterus senegalus After examining swimming and walking behaviour in aquatically raised individuals, we show that walking behaviour is characterized by greater absolute duration of muscle activity in most muscles when compared with swimming, but that the magnitude of recruitment during walking is only increased in the secondary bursts of fin muscle and in the primary burst of the mid-body point. This localized increase in intensity suggests that walking in P. senegalus is powered in a few key locations on the fish, contrasting with the more distributed, low intensity muscle force that characterizes the stroke cycle during swimming. Finally, the increased intensity in secondary, but not primary, bursts of the fin muscles when walking probably underscores the importance of antagonistic muscle activity to prevent fin collapse, add stabilization and increase body support. Understanding the principles that underlie the flexibility of muscle function can provide key insights into the sources of animal functional and behavioural diversity.
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phenotypic plasticity of muscle fiber type in the pectoral fins of Polypterus senegalus reared in a terrestrial environment
The Journal of Experimental Biology, 2017Co-Authors: Trina Y Du, Emily M StandenAbstract:ABSTRACT Muscle fiber types in the pectoral fins of fishes have rarely been examined, despite their morphological and functional diversity. Here, we describe the distribution of fast and slow muscle fibers in the pectoral fins of Polypterus senegalus , an amphibious, basal actinopterygian. Each of the four muscle groups examined using mATPase staining showed distinct fiber-type regionalization. Comparison between fish raised in aquatic and terrestrial environments revealed terrestrially reared fish possess 28% more fast muscle compared with aquatically reared fish. The pattern of proximal–distal variation in the abductors differed, with a relative decrease in fast muscle fibers near the pectoral girdle in aquatic fish compared with an increase in terrestrial fish. Terrestrially reared fish also possess a greater proportion of very small diameter fibers, suggesting that they undergo more growth via hyperplasia. These observations may be a further example of adaptive plasticity in Polypterus , allowing for greater bursts of power during terrestrial locomotion.
Sam Vandenplas - One of the best experts on this subject based on the ideXlab platform.
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Epithelial Label-Retaining Cells Are Absent during Tooth Cycling in Salmo salar and Polypterus senegalus.
PloS one, 2016Co-Authors: Sam Vandenplas, Maxime Willems, P. Eckhard Witten, Tom Hansen, Per Gunnar Fjelldal, Ann HuysseuneAbstract:The Atlantic salmon (Salmo salar) and African bichir (Polypterus senegalus) are both actinopterygian fish species that continuously replace their teeth without the involvement of a successional dental lamina. Instead, they share the presence of a middle dental epithelium: an epithelial tier enclosed by inner and outer dental epithelium. It has been hypothesized that this tier could functionally substitute for a successional dental lamina and might be a potential niche to house epithelial stem cells involved in tooth cycling. Therefore, in this study we performed a BrdU pulse chase experiment on both species to (1) determine the localization and extent of proliferating cells in the dental epithelial layers, (2) describe cell dynamics and (3) investigate if label-retaining cells are present, suggestive for the putative presence of stem cells. Cells proliferate in the middle dental epithelium, outer dental epithelium and cervical loop at the lingual side of the dental organ to form a new tooth germ. Using long chase times, both in S. salar (eight weeks) and P. senegalus (eight weeks and twelve weeks), we could not reveal the presence of label-retaining cells in the dental organ. Immunostaining of P. senegalus dental organs for the transcription factor Sox2, often used as a stem cell marker, labelled cells in the zone of outer dental epithelium which grades into the oral epithelium (ODE transition zone) and the inner dental epithelium of a successor only. The location of Sox2 distribution does not provide evidence for epithelial stem cells in the dental organ and, more specifically, in the middle dental epithelium. Comparison of S. salar and P. senegalus reveals shared traits in tooth cycling and thus advances our understanding of the developmental mechanism that ensures lifelong replacement.
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Tooth replacement in an evo-devo context : the dental lamina as a possible source of stem cells
2016Co-Authors: Sam VandenplasAbstract:The enthralling ability to continuously replace teeth throughout life has fascinated scientists for decades. This ability (polyphyodonty) is maintained in almost all tooth-bearing non-mammalian vertebrates. Teeth are organised in tooth families, i.e. a functional tooth and all of its successors (Reif, 1982). In general, first and later generation teeth develop within an epithelial dental lamina as result of interaction of the epithelial cells with the underlying neural crest derived mesenchyme. Many aspects of tooth development and tooth evolution have been intensively studied over the past century; however the mechanism that drives lifelong tooth renewal remains largely unknown. Huysseune and Thesleff (2004) were the first to hypothesise that epithelial stem cells might be involved in this process, and suggested the dental lamina as a putative stem cell niche. In this thesis, we wished to test this hypothesis using a selection of polyphyodont species. In each of the species examined, we focussed on the lower jaw, and addressed three key issues: (1) the morphology and architecture of the dental tissues, with a particular interest for the dental lamina, (2) the spatiotemporal pattern of cell proliferation within the different layers of the dental lamina, and (3) the potential presence of epithelial stem cells. We selected three polyphyodont species that are interesting from a comparative, evo-devo perspective: a chondrichthyan (Scyliorhinus canicula) and two actinopterygian osteichthyans (Polypterus senegalus as a member of a basal clade within the Actinopterygii and Salmo salar as a basal protacanthopterygian). (1) Scyliorhinus canicula has many successor teeth, which are prefabricated before the functional tooth is shed (CHAPTER 3). This results in tooth family sizes of seven to eight members. All tooth families are interconnected by a continuous and permanent dental lamina and are organised in an alternating pattern of developmental stages along the jaw margin. Three to four members of each family reside in the dental lamina. Polypterus senegalus and Salmo salar have their teeth organised in tooth families with two to three members; however, neither for the establishment of the first-generation tooth, nor for the development of its successors, a distinct dental lamina could be determined (CHAPTER 5,7). The maturation stage of functional teeth in Polypterus senegalus showed an alternating pattern, similar on both jaw halves (CHAPTER 4), while in Salmo salar a pattern with tooth families in similar developmental stages occurred every third position (CHAPTER 6). We propose to define the dental lamina in broad terms as ‘all epithelial cells that enclose a tooth family’. This allows us to interpret the dental lamina in Polypterus senegalus (CHAPTER 5) and Salmo salar (CHAPTER 7) as being extremely small or spatially compressed rather than being absent, and morphologically indistinguishable from the superficial epithelium. In conclusion of our morphological observations, we have constructed a hypothetical evolutionary model that generalises the dental lamina as a homologous modular structure in dental development (CHAPTER 8). (2) BrdU proliferation studies showed dividing cells during the development of the youngest tooth germs in all three species (CHAPTERS 3,5,7). These tooth germs arise at the distal end of the dental lamina in Scyliorhinus canicula and the lingual side of the dental lamina in Polypterus senegalus and Salmo salar. In all three species, the middle dental epithelium (MDE) and outer dental epithelium (ODE) in the lingualmost part (i.e. most distal) of the dental lamina showed intensive proliferation, while the transition zone of the outer dental epithelium towards the oral epithelium was not proliferating in any of the three species. Further similarities were obvious from BrdU chase experiments (CHAPTERS 3,5,7). All three species showed a shift in position of proliferative areas in the epithelium from the lingual side of the dental lamina towards a labial and oral position. This is consistent with a shift that developing successor teeth undergo towards the superficial epithelium, i.e. the location where they replace functional teeth. (3) BrdU pulse-chase experiments were conducted in all three species, with the intention to detect label-retaining cells (LRCs) in the dental lamina as a possible indication for the presence of stem cells. In Scyliorhinus canicula, LRCs were found in the lingualmost part of the dental lamina both within the dental and interdental region (CHAPTER 3). Our experiments on Salmo salar and Polypterus senegalus did not reveal any of such cells in the epithelial tissues surrounding a tooth family (CHAPTERS 5,7). Immunohistological staining for Sox2, used on all three species as proxy for the potential presence of stem cells, yielded consistent results, with positive staining in the oral epithelium, taste buds and ODE transition zone but absent in the dental lamina (CHAPTERS 3,7). The Sox2+ cells in Scyliorhinus canicula did not coincide with the LRCs in the MDE. The combination of these conflicting results obtained for the three species studied, provided arguments for either of two scenarios: one supporting the presence, and one, conversely, in support of the absence of stem cells in the dental lamina. While only limited support for the presence of epithelial stem cells could be collected using the commonly proposed character of label retention, we consider the presence of cells with stem cell like characteristics likely. At the same time we emphasise that the concept of what ‘true’ stem cells are, needs to be critically re-evaluated. In the species examined, the lingualmost part of the MDE could serve as a site within the dental lamina to maintain a population of such potential stem cells. Continued experimental research on the proposed candidate area for stem cells should be pursued.
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A comparison of the larval and juvenile dentition in Polypterus senegalus
Journal of Applied Ichthyology, 2014Co-Authors: A. De Clercq, Sam Vandenplas, Ann HuysseuneAbstract:Summary Polypterus senegalus is a freshwater fish belonging to the earliest diverged group of the actinopterygian lineage with currently living representatives. Its dentition has been well characterized in terms of distribution and shape of teeth in different life stages. Additionally, structural features of the first-generation teeth have been briefly described. However, at present it is not known how the primary dentition is patterned and if this pattern is similar to that found in juveniles. In this preliminary study, to answer this question we investigate the tooth pattern of a larval P. senegalus based on serial sections and 3D reconstructions, and compare dental features in larvae and juveniles. Polypterus senegalus passive apterolarvae possess a well developed primary dentition. Dentigerous bones develop either prior to the teeth (dentary, retroarticular), or as an attachment site concomitant with the expanding dentition (coronoid 1). Most teeth are attached and erupted, and thus considered functional, and their pulp houses a blood vessel, two features that contrast with earlier findings. The primary teeth do not display a level of maturation that could reflect a particular order of development. New teeth are added anteriorly, and likely also posteriorly, to allow the tooth row to grow to keep pace with the growing jaw. Replacement teeth are absent at this stage. Thus, the pattern observed in juveniles, with alternate (odd and even) positions displaying a different level of tooth maturation, is not present in the larva. Most strikingly, in the larva, considerable symmetry exists between apparently random patterns on both dentaries, eliciting intriguing questions on left-right control to be addressed in future studies.
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Tooth replacement without a dental lamina: The search for epithelial stem cells in Polypterus senegalus
Journal of experimental zoology. Part B Molecular and developmental evolution, 2014Co-Authors: Sam Vandenplas, Adelbert De Clercq, Ann HuysseuneAbstract:Most actinopterygians replace their teeth continuously throughout life. To address the question of where and how replacement teeth form in actinopterygians, it is advisable to investigate well-chosen representatives within the lineage. The African bichir, Polypterus senegalus, belongs to the earliest diverged group of the actinopterygian lineage with currently living representatives. Its well characterized dentition, together with its phylogenetic position, make this species an attractive model to answer following questions: (1) when and where does the replacement tooth form and how is it connected with the dental organ of the predecessor, and (2) is there any evidence for the presence of epithelial stem cells, hypothesized to play a role in replacement? Serial sections show that one tooth family can contain up to three members, which are all interconnected by dental epithelium. Replacement teeth develop without the presence of a successional dental lamina. We propose that this is the plesiomorphic condition for tooth replacement in actinopterygians. BrdU pulse-chase experiments reveal cells in the outer and middle dental epithelium, proliferating at the time of initiation of a new replacement tooth. It is tempting to assume that these cell layers provide a stem cell niche. The observed absence of label-retaining cells after long chase times (up to 8 weeks) is held against the light of divergent views on cell cycling properties of stem cells. At present, our data do not support, neither reject, the hypothesis on involvement of epithelial stem cells within the process of continuous tooth replacement. J. Exp. Zool. (Mol. Dev. Evol.) 322B: 281–293, 2014. © 2014 Wiley Periodicals, Inc.
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Aspects of tooth replacement in a basal actinopterygian, Polypterus senegalus
2013Co-Authors: Sam Vandenplas, Adelbert De Clercq, Ann HuysseuneAbstract:Most actinopterygians replace their teeth continuously throughout life. Major differences are nevertheless observed in the spatial and temporal relationship between a developing replacement tooth and its predecessor. In this study we address the question of where and how replacement teeth form in the African bichir (Polypterus senegalus). Furthermore we test if there is any evidence for the presence of epithelial stem cells, hypothesized to play a role in replacement [1]. The bichirs’ well characterized dentition [2], together with its basal phylogenetic position, make this species an attractive model to answer these questions. We investigated stages of tooth development and replacement in juvenile bichirs of approx. 12 cm, using histological sections. A BrdU pulse-chase experiment was conducted on 20 juvenile Polypterus senegalus, to visualize label retaining cells. Dentary teeth are organized in one row. Each tooth family was observed to house three members: one functional tooth showing resorption, its successor in late cytodifferentiation, and a secondary successor in morphogenesis stage. Replacement teeth in cytodifferentiation stage showed proliferation in their cervical loop and the postero-lingual side of the outer dental epithelium. This is the site of the initiation of a new replacement tooth. No clear successional lamina was observed to connect the functional tooth and its successor. No label retaining cells were observed in the dental organ after 4 and 8-weeks chase time. A weak and mostly scattered BrdU signal was nevertheless observed in the basal layer of the oral epithelium. Together, our data suggest that a replacement tooth develops directly from the dental organ of the functional tooth. Furthermore, the lack of label retaining cells in the predecessor requires reconsideration of mechanisms of tooth replacement. Reference: [1] Huysseune et al. BioEssays (2004); [2] Wacker et al. Ann. anat. (2001)
R. Glenn Northcutt - One of the best experts on this subject based on the ideXlab platform.
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The cranial nerves of the Senegal bichir, Polypterus senegalus [osteichthyes: actinopterygii: cladistia].
Brain behavior and evolution, 1996Co-Authors: Tatjana Piotrowski, R. Glenn NorthcuttAbstract:The organization of the roots, ganglia and peripheral distribution of the rami of the cranial nerves of larval and juvenile Senegal bichirs was examined with a wide range of techniques, including gros
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An immunohistochemical study of the telencephalon of the senegal bichir (Polypterus senegalus).
The Journal of comparative neurology, 1992Co-Authors: Anton Reiner, R. Glenn NorthcuttAbstract:The telencephalon in ray-finned fish (actinopterygians) is everted, in contrast to the evaginated telencephalic hemispheres in all other vertebrates. In the more derived ray-finned fish, the teleosts, proliferation of neurons and their migration from the ependymal zone of the pallium renders comparisons between telencephalic cell groups of the teleosts and members of other vertebrate groups extremely difficult. The telencephalon of Polypterus (a primitive living ray-finned fish), although everted, is cytoarchitecturally much simpler than that of teleosts. We have thus applied immunohistochemical techniques to the study of the telencephalon of Polypterus to help clarify the evolution of the telencephalon in teleosts and facilitate comparisons between the telencephalon in ray-finned fish and other vertebrates. Antisera against the following neuroactive substances were used: 1) serotonin (5HT), 2) tyrosine hydroxylase (TH), 3) substance P (SP), 4) leucine-enkephalin (ENK), 5) neuropeptide Y (NPY), and 6) the neurotensin-related hexapeptide LANT6. Several features of the labeling patterns obtained suggested that the dorsal and ventral subdivisions of the area ventralis are homologous as a field to the basal ganglia and septum plus other basal telencephalic regions of land vertebrates, sharks and lungfish: 1) an abundance of SP +, NPY +, and ENK+ fibers; 2) an abundance of TH+ fibers, possibly of posterior tubercle/tegmental origin; 3) the presence of an SP + fiber bundle that appeared to descend from basal telencephalic levels and terminate in the posterior tubercle/tegmentum, which contain TH + (possibly dopaminergic) neurons; and 4) an abundance of 5HT+ fibers, presumably of posterior tubercle/tegmental origin. It was not possible, however, to recognize distinct pallidal and striatal subdivisions within the area ventralis of Polypterus. The olfactory pallium (Pl) was generally poor in most of the substances examined, except for the presence of LANT6+ fibers. The P3 pallid field was conspicuously rich in SP+ and ENK+ fibers throughout its extent, and the caudal and lateral parts of the P2 field were rich in SP+ fibers and ENK+ fibers. Since this is characteristic of the medial pallial and/or dorsomedial pallial walls of the telencephalon in lungfish, sharks, frogs, and reptiles, the P3 field and caudolateral part of the P2 field may be homologous to these portions of the telencephalon in other vertebrates. More rostromedial parts of P2 may correspond to those parts of the pallium in land vertebrates that are in receipt of specific sensory input from the thalamus, since low neuropeptide levels are characteristic of these regions. These results indicate that the dorsal part of the ventral area of the telencephalon in ray-finned fish may be homologous to the basal ganglia in other vertebrates. These results also suggest that the pallial portions of the telencephalon in Polypterus may include a region comparable to part of the isocortex or its homologues in amniotes. o 1992 Wiley-Liss, Inc.
Chihua Chiu - One of the best experts on this subject based on the ideXlab platform.
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hox clusters of the bichir actinopterygii Polypterus senegalus highlight unique patterns of sequence evolution in gnathostome phylogeny
Journal of Experimental Zoology, 2011Co-Authors: Jeremy Raincrow, Ken Dewar, Claudia Stocsits, Sonja J Prohaska, Chris T Amemiya, Peter F Stadler, Chihua ChiuAbstract:Teleost fishes have extra Hox gene clusters owing to shared or lineage-specific genome duplication events in rayfinned fish (actinopterygian) phylogeny. Hence, extrapolating between genome function of teleosts and human or even between different fish species is difficult. We have sequenced and analyzed Hox gene clusters of the Senegal bichir (Polypterus senegalus), an extant representative of the most basal actinopterygian lineage. Bichir possesses four Hox gene clusters (A, B, C, D); phylogenetic analysis supports their orthology to the four Hox gene clusters of the gnathostome ancestor. We have generated a comprehensive database of conserved Hox noncoding sequences that include cartilaginous, lobe-finned, and ray-finned fishes (bichir and teleosts). Our analysis identified putative and known Hox cis-regulatory sequences with differing depths of conservation in Gnathostoma. We found that although bichir possesses four Hox gene clusters, its pattern of conservation of noncoding sequences is mosaic between outgroups, such as human, coelacanth, and shark, with four Hox gene clusters and teleosts, such as zebrafish and pufferfish, with seven or eight Hox gene clusters. Notably, bichir Hox gene clusters have been invaded by DNA transposons and this trend is further exemplified in teleosts, suggesting an as yet unrecognized mechanism of genome evolution that may explain Hox cluster plasticity in actinopterygians. Taken together, our results suggest that actinopterygian Hox gene clusters experienced a reduction in selective constraints that surprisingly predates the teleost-specific genome duplication. J. Exp. Zool. (Mol. Dev. Evol.) 316:451–464, 2011. © 2011 Wiley-Liss, Inc.
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Hox clusters of the bichir (Actinopterygii, Polypterus senegalus) highlight unique patterns of sequence evolution in gnathostome phylogeny
Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 2011Co-Authors: Jeremy Raincrow, Ken Dewar, Claudia Stocsits, Sonja J Prohaska, Chris T Amemiya, Peter F Stadler, Chihua ChiuAbstract:Teleost fishes have extra Hox gene clusters owing to shared or lineage-specific genome duplication events in rayfinned fish (actinopterygian) phylogeny. Hence, extrapolating between genome function of teleosts and human or even between different fish species is difficult. We have sequenced and analyzed Hox gene clusters of the Senegal bichir (Polypterus senegalus), an extant representative of the most basal actinopterygian lineage. Bichir possesses four Hox gene clusters (A, B, C, D); phylogenetic analysis supports their orthology to the four Hox gene clusters of the gnathostome ancestor. We have generated a comprehensive database of conserved Hox noncoding sequences that include cartilaginous, lobe-finned, and ray-finned fishes (bichir and teleosts). Our analysis identified putative and known Hox cis-regulatory sequences with differing depths of conservation in Gnathostoma. We found that although bichir possesses four Hox gene clusters, its pattern of conservation of n oncoding sequences is mosaic between outgroups, such as human, coelacanth, and shark, with four Hox gene clusters and teleosts, such as zebrafish and pufferfish, with seven or eight Hox gene clusters. Notably, bichir Hox gene clusters have been invaded by DNA transposons and this trend is further exemplified in teleosts, suggesting an as yet unrecognized mechanism of genome evolution that may explain Hox cluster plasticity in actinopterygians. Taken together, our results suggest that actinopterygian Hox gene clusters experienced a reduction in selective constraints that surprisingly predates the teleost-specific genome duplication