Guide Aspects of Neural Ontogeny

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In vivo this leads to a striking absence of a well formed peripheral nervous system, as evidenced by lack of neurofilament and beta-III tubulin staining, suggesting an important function for beta-actin in peripheral nervous system development. This contrasts studies where conditional ablation of beta-actin is not required for motor neuron function or regeneration in vivo [49] or resulted in restricted morphological abnormalities in the central nervous system [9].

This however does not contradict our results since a complete downregulation of beta-actin during the early phases of development was never achieved with the conditional ablation setup. Cadherin expression during neural crest ontogeny is well studied in chick and Xenopus, however, details of cadherin expression during mouse neural crest ontogeny are lagging behind [19] , [48] , [50] , [51] , [52] , [53] , [54]. Cadherin expression patterns in mouse cranial neural crest cells were previously investigated [55].

Cadherin was localized in most mesenchymal cells in the head region and especially neural crest cells constituting the mandibular and maxillary arches expressed high levels. The developing cranial neural folds also expressed this cadherin. These authors additionally reported cadherin expression in the dorsal midline of the neural tube in the posterior trunk region. We can conclude that the cadherin expression pattern during the early phases of neural crest development is very similar in cranial and trunk regions of mouse embryos Figure 9 , left part.

Initial expression is seen in the pre-migratory neural crest territory: neural fold ridges in the cranial region and the dorsal part of the neural tube in the trunk region. Afterwards, expression of cadherin is retained in the migratory cell population, both in the cranial regions as the trunk regions. Similar cadherin expression was observed during rat development [56]. Neural crest cells in the dorsal neural tube express both N-cadherin and cadherin, migrating neural crest cells express high levels of cadherin while maintaining N-cadherin levels.

Ablation of beta-actin leads to decreased cadherin expression in the neural crest population, specifically in the pre-migratory neural crest cell population, and to impaired migration behavior. Figure 9 shows a schematic view of the E9. In addition, the neural crest cells show increased apoptosis, especially in the pre-migratory population, similar to the decreased cadherin staining. At this point, it is difficult to say which events are cause and which are consequence.

Based on our previous results [10] , [12] we assume that ablation of beta-actin causes altered cadherin expression, via genetic reprogramming or as part of a transcriptional complex instructing cadherin transcription. Data from many different cell types support the hypothesis that decreased cadherin signaling could elicit impaired migration [45] , [47] , [48] , [53] , [57] , [58] , [59] , [60] , [61].

Cadherin is a type II cadherin and indeed considered as a marker of mesenchymal, migratory phenotypes [55] , [56] , [62].

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On the other hand, altered cadherin expression in combination with apoptosis has frequently been reported in many different tissues as well [63] , [64] , [65] , [66]. N-cadherin was demonstrated to have important polarizing functions during neurulation and development of neurons [71] , [72] , [73] , [74] , [75]. Along similar lines it was recently reported that beta-actin is required for establishing apicobasal cell polarity in intestinal epithelial cells [76].

Moreover beta-actin seems important for the polarization of fibroblasts via cadherin [59]. Cells expressing a defective variant of cadherin revealed a more extensive cortical F-actin ring that correlated with significant higher levels of activated Rac1 and resulted in impaired intercellular motility and problems to rearrange in multicellular clusters.

Also in neural crest cells an important balance of Rac is necessary to define the front and rear of the cell [77]. A phenomenon which appears to be common to many species is the exchange of a type I cadherin for a type II cadherin prior to major mophological movement [67] , [68] , [69] , such as neural crest emigration [21] , [50] , [70]. We here demonstrate that emigrated neural crest cells retain N-cadherin expression, at least in the early stages of migration, suggesting the cadherin switch in mouse trunk is more subtle than previously described for other species such as chick and quail [55] , [68] , [69].

Several published observations support a regulatory role for ROCK in neural crest ontogeny [35] , [43].

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Phillips et al. At later stages, these mice exhibited neural crest deficiency and hypoplastic neural crest derived craniofacial structures, suggesting that ROCK activity is essential for neural crest cells to form the craniofacial region. Also in quail, a negative modulatory role for Rho and ROCK signaling in delamination of neural crest cells has been reported [35]. The inhibition of Rho-ROCK promotes premature and enhanced neural crest delamination, concomitant with the disruption of the F-actin cytoskeleton. The authors also reported an interaction between N-cadherin and Rho-ROCK via regulation of F-actin dynamics in quail neural crest cells.

N-cadherin expression is normally lost from delaminating cells due to intracellular cleavage which generates a C-terminal fragment CTF [35] , [78]. However, inhibition of ROCK results in neural crest cells devoid of N-cadherin and losing intercellular adhesions prematurely. A more direct connection between a cadherin and Rho was already described in Xenopus, where it was shown that cadherin acts upstream of RhoA [48].

In summary, we revealed a novel role for beta-actin during development. Absence of beta-actin severely hampers formation of the peripheral nervous system, due to defective neural crest migration. This suggests there might be a reciprocal connection between Rho-ROCK signaling and cadherin, since the influence of cadherins on this pathway in neural crest cells was already reported [35] , [48] , [79].

Conceived and designed the experiments: DT. Analyzed the data: DT RN. Wrote the paper: DT CA. Browse Subject Areas? Click through the PLOS taxonomy to find articles in your field. Abstract The mouse genome consists of six functional actin genes of which the expression patterns are temporally and spatially regulated during development and in the adult organism.

Introduction Actins are highly conserved proteins throughout evolution [1]. Trunk Neural Tube Explant Assay The method used to establish the neural crest outgrowth cultures were adapted from those described by Murphy et al. Immunohistochemistry Immunohistochemistry on whole mount embryos was performed as previously described [24]. Immunofluorescence For immunofluorescence on neural tube explants, the neural tube was first removed from the dish or slide. In situ Hybridization Whole mount in situ hybridization was carried out as described by Miyoshi et al.

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Figure 6. Figure 7. Figure 8. Discussion Our results reveal a role for beta-actin during neural crest ontogeny. A Role for Cadherin in Mouse Trunk Neural Crest Migration Cadherin expression during neural crest ontogeny is well studied in chick and Xenopus, however, details of cadherin expression during mouse neural crest ontogeny are lagging behind [19] , [48] , [50] , [51] , [52] , [53] , [54]. Figure 9. Author Contributions Conceived and designed the experiments: DT.

References 1. Vandekerckhove J, Weber K At least six different actins are expressed in a higher mammal: an analysis based on the amino acid sequence of the amino-terminal tryptic peptide. J Mol Biol 4 : — View Article Google Scholar 2. Pollard TD Genomics, the cytoskeleton and motility. Nature : — View Article Google Scholar 3.

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Dev Biol 2 : — View Article Google Scholar 4. Cell Motil Cytoskeleton 66 10 : — View Article Google Scholar 5. Nat Neurosci 9 10 : — View Article Google Scholar 6. View Article Google Scholar 7. J Cell Biol 2 : — View Article Google Scholar 8. J Cell Sci Pt 6 — PLoS One 7 3 : e View Article Google Scholar Mol Cell Proteomics 11 8 : — Genesis 42 4 : — PLoS One 8 6 : e Mayor R, Theveneau E The neural crest.

Development 11 : — Adv Exp Med Biol — Annu Rev Cell Dev Biol — Prog Mol Biol Transl Sci — Taneyhill LA To adhere or not to adhere: the role of Cadherins in neural crest development. Cell Adh Migr 2 4 : — More recently, Dalla Vecchia published several colored pictures of this specimen and thus its full description is not necessary here. This pterosaur skeleton is distributed into five slabs that were collected on different occasions Wellnhofer Several bones are preserved as impressions with bits of broken parts, probably due to the exposure of the material prior to collection.

Although the skeleton is disarticulated and scattered, there is no duplication of bones and all elements seem to be part of the same individual. So far, only two cranial elements could be recognized. A flattened bone with two distinct processes was previously identified as a sternum Wellnhofer , Dalla Vecchia , but is regarded as the fused frontals pers. The lack of a cristospine and the developed median ridge that marks the contact between opposite elements corroborate this reinterpretation.

The anterior processes of the frontals are shorter than in Eudimorphodon ranzii , and apparently also than that of Bergamodactylus MPUM The notch between them enclosed the posterior processes of the premaxillae. Except for a small bony portion that forms part of the ventral margin of the orbit and the posterior tip of the quadratojugal process, the jugal is preserved as an impression. The postorbital process is thin and long, subequal in length with the ventral margin of this bone, being therefore proportionally longer than in any other pterosaur.

Several thin and flat bones are preserved ventral to the jugal and can be identified as part of the sclerotic ring. The most interesting element of BSP I 51 is the lower jaw. As Nesbitt and Hone pointed out, this bone belongs to the right side and is exposed in lateral view contrary to the original description Wellnhofer This interpretation is corroborated by several anatomical observations such as the presence of foraminae and the slightly rugose texture of the bone surface, which is characteristic of the lateral portion of reptilian dentaries.

The mandibular rami are preserved with the right one being more complete and both lacking the symphyseal region. Therefore, the observed elevation can be interpreted as a dorsal extension or process of the surangular. In any case, the surangular dorsal process is not pointed or developed in BSP I 51, but rather low and rounded. The right mandibular ramus clearly shows an external mandibular fenestra, bordered by the dentary, surangular and angular.

It has an oval shape and is reduced. The left mandibular ramus is incomplete and also has the anterior margin of an opening that looks like the external mandibular fenestra. However, this opening is significantly larger than the one on the right side. The anterior part of this bone is not preserved but left an impression on the matrix close to the left scapulocoracoid.

The right lower jaw shows 12 multicuspid teeth in place and two additional alveoli, totalizing 14 teeth. The preserved portion of the left lower jaw only has the last 10 teeth. There are some differences in the opposite teeth from the left and right side, which were interpreted by Wellnhofer as ontogenetic or individual variation. The dentary of both sides is shallow compared to other Triassic taxa, similar to that of Carniadactylus rosenfeldi. In the preserved portion of the mandible there is a thick anteroposteriorly oriented ridge that is also observed in Bergamodactylus MPUM Regarding the postcranial skeleton, it is inte resting to mention that one cervical vertebra shows at least one lateral opening in the contact region of the centrum and the neural arch.

This opening was correctly interpreted as a pneumatic foramen by Wellnhofer and is rather rare in the neck of other Triassic pterosaur species Butler et al. Pre- and postzygapophyses of the caudal vertebrae are not elongated and do not form rod-like structures.

The haemapophyses are long but not to the same degree as in other long-tailed non-pterodactyloid pterosaurs. Scapula and coracoid are fused, with the scapula being a much longer bone.

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The coracoid is broad and has an expanded proximal end. On the anterior margin of the coracoid a developed ridge runs from the medial opposite portion to the ventral margin of the bone. The articulation of the coracoid with the sternum is dorsoventrally flattened and only slightly concave. The coracoid of BSP I 51 differs from the more straighter one of Eudimorphodon ranzii and shows a more constricted shaft compared to Carniadactlylus rosenfeldi and MPUM which is referred to a new species Bergamodactyluswildi , see below.

Both humeri are preserved, albeit the right one only as an impression. The deltopectoral crest is subrectangular and similar to Bergamodactylus MPUM , but the medial crest is less developed. The left humerus shows a distinct rugose oval depression separated from the remaining part of the deltopectoral crest by a marked diagonal bony ridge. It is not clear if this feature, never observed in pterosaur humeri before, constitute a taphonomic artifact. No evidence of a pneumatic foramen was observed in both humeri.


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The right first wing phalanx is preserved and has the extensor tendon process fused. The pelvis shows the ilium, pubis and ischium fused, being much deeper than in Eudimorphodon ranzii. The ischium presents a developed process on the posterior margin. Tibia and fibula are not fused, with the fibula reaching the distal end of the tibia and contacting the proximal tarsals. However, tarsals are fused with the tibia forming a tibiotarsus.

Wellnhofer considered BSP I 51 an immature individual mainly due to the slenderness of some bones, including the jugal and the sternum. However, the scapula and coracoid are firmly fused, as is the extensor tendon process of the first wing phalanx, the pelvic bones ilium, pubis and ischium , and the proximal tarsals with the tibia, suggesting that this specimen represents an adult individual instead.

The marked differences in the anatomy observed in BSP I 51 justify the establishment of a new taxon, designated here as Austriadraco dallavecchiai. Etymology: In allusion to the Bergamo Province, in Italy and dactylus , from the Greek meaning finger, a common epithet for pterosaur species.

The new species can be further distinguished from other campylognathoidids by the following combination of characters: surangular dorsal process of moderate size smaller than in Carniadactylus rosenfeldi but larger than in Eudimorphodon ranzii ; mandibular rami deeper than in Carniadactylus ; pteroid rod-like with a marked bend, having the proximal part shorter than in Carniadactylus ; lack of enlarged maxillary teeth on the middle region of the maxillae unknown in Carniadactylus ; dentition of the lower jaw extending more posteriorly than in Carniadactylus ; 18 and 17 teeth on each side of the upper and lower jaw, respectively.

Remarks: The holotype of Bergamodactyuswildi has been described and was illustrated several times in the literature. The first report of MPUM was done by Wild in an extensive monograph on the Triassic pterosaurs recovered from Cene Italy and most recently by Dalla Vecchia , who presented several colored illustrations of this material.

He observed several anatomical differences between this material and the holotype of Eudimorphodon ranzii MCSNB , including dissimilarities in the dentition, but interpreted them as a result of its purported young ontogenetic stage. However, despite this difference, there is no indication that MPUM is a juvenile. Quite the contrary, size-independent characters commonly used in pterosaur material to assess their ontogenetic stage e.

Despite the compressed nature of the specimen, there is also no sign that the carpal elements are unfused, which has also been observed by Dalla Vecchia This included the shorter skull of MPUM and a more gracile postorbital, particularly the postorbital frontal process that lacked the dorsal expansion present in the holotype of Eudimorphodon ranzii MCSNB Furthermore, Wild recognized that MPUM had fewer teeth, with 18 in the upper and 17 in the lower jaw, as opposed to 29 and 28 found in the holotype of Eudimorphodon ranzii MCSNB , respectively.

As pointed out before, there is no indication in MPUM that suggests that it was a juvenile. Quite the contrary, the fused scapula and coracoid, elements of the syncarpal and the extensor tendon process strongly indicate that this specimen represents an adult individual and therefore the differences registered above cannot be attributed to ontogeny. Although it is conceivable that the skull and lower jaw might indeed get longer in ontogenetically older individuals e. In the bone-bed of one pterodactyloid pterosaur from Lower Cretaceous deposits of China, where ontogenetically younger and older individuals were recovered, the number of teeth is constant Wang et al.

In recent reptiles there might be some changes regarding the number of teeth due to ontogeny Edmund , but not as significant as in these pterosaur specimens. Those teeth were interpreted by Wild as a result of sexual dimorphism, a hypothesis that cannot be tested on the little number of specimens available. Another significant difference between MPUM and Eudimorphodon ranzii MCSNB is the broad posterior part of the jugal process of the maxillae, which is similar to the condition observed in Campylognathoides e.

Moreover, the nasal does not send a thin anterior process to form the dorsoanterior margin of the external nares that is very well developed in MCSNB Wild : Fig. The antorbital fenestra of Eudimorphodon ranzii MCSNB shows the same subtriangular shape than that of MPUM , although being higher, with the dorsal margin surpassing that of the external naris.

Regarding the postcranial skeleton, the main differences observed by Wild were seen in the pteroid, which is rod-like in MPUM and lacks the marked proximal expansion observed in the holotype of Eudimorphodon ranzii MCSNB To my knowledge, no pterosaur species shows such marked differences in the configuration of the pteroid from ontogenetically younger or smaller to older or larger individuals e. Although the variation in the humeri of younger and older pterosaur individuals is still not known in detail, particularly in non-pterodactyloid pterosaurs, a similar change in morphology was observed comparing two humeri of very different sizes of one toothless pterodactyloid species Manzig et al.

However, when humeri about half the size are compared, there is no difference at all Manzig et al. Dalla Vecchia agreed with the observation of Kellner that MPUM was not a juvenile, having several bones fused, albeit being much smaller see comments below. Unfortunately, the holotype of Carniadactylus rosenfeldi MFSN lacks most of the anterior region of the skull, which limits comparisons. Since there is no evidence of any tooth in this region in MFSN , this difference does not seem to be an artifact of preservation. This author also pointed out the similarities of the pteroid in both specimens that are rod-like and bended.

In MPUM however, the proximal part before the bend is proportionally shorter. There are also differences in the humerus, with Carniadactylus rosenfeldi MFSN having the deltopectoral crest comparatively less extended down the humerus shaft. This is not expected in individuals of similar ontogenetic stages see Manzig et al.

The proportions of the lengths of several postcranial elements Tabs. I , II , with the ratios of MPUM substantially different from the holotype of Carniadactylus rosenfeldi MFSN and being actually more similar to Raeticodactylus see tables in Dalla Vecchia , also strike as being quite distinct between these two specimens.

Overall, the femur in MPUM is much smaller relative to the humers, ulna and the first wing phalanx. The same is true for the metacarpal, which is also proportionally shorter relative to several bones in MPUM compared to other Triassic pterosaurs, including the holotype of Carniadactylus rosenfeldi MFSN Most interestingly, ph1d4 is larger than ph2d4, which is rather derived within pterosaurs e.

The ratio between ph3d4 and ph1d4 of both specimens also differ from most other Triassic and Jurassic taxa, where ph3d4 is larger than ph1d4. As pointed out by Dalla Vecchia , MFSN has several bones fused, like the scapula and coracoid, the proximal carpal elements, and the extensor tendon process of the first wing phalanx.

Fibula and tibia might also be fused. The sole potential indications that the individual represented by MFSN might not have reached a full ontogenetic maturity at time of death lies on the unfused distal syncarpals formed by three elements, Dalla Vecchia and the presence of a narrow region with a slightly distinct texture between the proximal tarsals and the tibia, indicating that they might not have completely fused despite being otherwise strongly connected. Regarding the ontogenetic stage of MPUM , this individual has basically the same fused elements as observed in the holotype of Carniadactylus rosenfeldi MFSN : scapula and coracoid, proximal carpal series and the extensor tendon process of the first wing phalanx.

The distal portion of the tibia and tarsal elements are not preserved in MPUM There is no feature that suggests that both specimens represent individuals of very distinct if at all ontogenetic stages see Discussion. Yet regarding size, the maximized wingspan maxws sensu Kellner et al. The differences in anatomical features and size between the holotype of Carniadactylus rosenfeldi MFSN and MPUM , combined with the developed ontogenetic stage of the latter, indicate that both specimens are not conspecific.

It should also be noted that Carniadactylus rosenfeldi comes from a distinct formation, the Dolomia di Forni Formation, that outcrops in the Friuli region and is slightly older than the Calcari di Zorzino Formation see Dalla Vecchia a: Fig. An adequate evaluation of the anatomical dif ferences concerning taxonomy is a difficult challenge. Besides the usual variation in anatomy due to intrinsic characteristics of organisms e. The nature of the fossil record that dictates a general low number of specimens preserved in different grades of incompleteness, further introduces distortions of variable effects and causes.

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Felleman b Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys. Middlebrooks a Observations and hypotheses on special organizational features of the central auditory nervous system. Zook b Somatosensory cortical map changes following digital amputation in adult monkey. Cynader, M. Schoppmann Variability in hand surface representations in areas 3b and 1 in adult owl and squirrel monkeys.

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