Pattern formation and growth in the regenerating limbs of urodelean amphibians

Development ◽  
1981 ◽  
Vol 65 (Supplement) ◽  
pp. 19-36
Author(s):  
Nigel Holder

The results of numerous types of grafting experiments involving the amputation of symmetrical limbs are described. These experiments were designed to test the tenets of the polar coordinate model. The analysis of the results of these grafts coupled with a quantitative analysis of blastemal shape strongly indicates that pattern regulation during amphibian limb regeneration can be understood in terms of the model.

Development ◽  
1988 ◽  
Vol 102 (1) ◽  
pp. 175-192
Author(s):  
V. French ◽  
T.F. Rowlands

We have studied pattern regulation in the medial-lateral axis of the insect segment by grafting legs of beetle larvae (Tenebrio molitor) in different orientations into different positions medial and lateral to the leg site. The Boundary Model and Polar Coordinate Model of the insect appendage predict various patterns of supernumerary leg regeneration, and these grafts were designed to test the predictions. When a larval leg is grafted with normal anterior-posterior orientation medial to the normal leg, larvae and subsequent adults bear the graft plus a supernumerary leg. This is located where the lateral edge of the grafted leg confronted medial thorax (from the leg base across to the midline) and is orientated as a mirror image of the graft. The tarsal structure of supernumeraries resulting from grafts of the mesothoracic leg onto the metathorax shows that the supernumeraries may be derived from the graft, the host site or from both sources. Similarly, when a leg is grafted lateral to the leg site, a supernumerary forms at the confrontation between the medial edge of the graft and lateral thorax (from leg base across to the dorsal tergite). These results agree with the predictions of both models and would indicate that the compartments or the positional values extend out from the leg to the midline and the edge of the tergite. The two models differ in their predictions for the number, position and orientation of supernumeraries following 180 degree rotation of the grafted leg. When the rotated graft is placed lateral to the leg, larvae and adults form a single supernumerary which, in accordance with the Polar Coordinate Model, is lateral to the graft and orientated as a mirror image of it. However, the results of the corresponding medial graft cannot be readily explained by either model. Larvae form a single supernumerary either posterior or medial to the graft, suggesting a modified model with unequally spaced positional values, but the subsequent adult supernumeraries are almost all located medially. Experiments involving a graft placed medial to the leg site frequently show duplication of the adult midline suture, an extra branch forming between the thorax and the graft or supernumerary leg. In this case, as in the regeneration of the dorsal midline, the extreme medial structure is formed between two more lateral regions, which need not come from opposite sides of the body, but must have opposite mediolateral polarities. At present, no model can adequately explain all the results of grafting and extirpation on the insect ventral thorax.


Development ◽  
1983 ◽  
Vol 76 (1) ◽  
pp. 115-137
Author(s):  
Hans Meinhardt

We postulate that positional information for secondary embryonic fields is generated by a cooperative interaction between two pairs of differently determined cell types. Positional information is thus generated at the boundaries between cells of different determination. The latter are assumed to result from the primary pattern formation in the embryo. The application of this model to vertebrate limbs accounts for the pairwise determination of limbs at a particular location, with a particular handedness and alignment to the main body axes of the embryo. It accounts further for the gross difference in the regeneration of double anterior and double posterior amphibian limbs as well as for the formation of supernumerary limbs after certain graft experiments including supernumeraries in which the dorsoventral polarity changes or which consist of two anterior or two posterior halves. Our model provides a feasible molecular basis for the polar coordinate model and successfully handles recently found violations, for instance formation of supernumerary limbs after ipsilateral grafting with 90° rotation. The most frequent types of developmental malformations become explicable. The models allow specific predictions which are fully supported by recent experiments (see the accompanying paper of M. Maden).


Development ◽  
1985 ◽  
Vol 90 (1) ◽  
pp. 57-78
Author(s):  
Hilary Anderson ◽  
Vernon French

In a series of grafting operations on cockroach legs, epidermal cells from different positions or from the same position on the circumference of the femur were placed together. Where cells from different positions were confronted, new cuticular structures corresponding to the positions which would normally have lain between them were formed during the following moults. At the control junctions, where cells from the same positions were placed together, no new structures were formed. Grafted legs were examined histologically at various times after the operation. The events following grafting fell into four phases: wound healing — when epidermal cells migrated over the wound to re-establish epidermal continuity and cells adjacent to the wound divided to compensate for cell emigration; intercalation — when cell divisions took place at the host-graft borders where there was a positional discrepancy; proliferation — when the general growth of the epidermis occurred by widespread cell division; cuticle secretion — when apolysis occurred, cell division ceased, and cuticle secretion began. The results show that intercalary regeneration is associated with local cell division at the graft-host borders, and that these divisions are not confined to the normal proliferative phase of the moult cycle, but begin much earlier in the cycle, as soon as wound healing is complete. These results support epimorphic models (such as the Polar Coordinate Model) of pattern regulation, where change of positional value is tied to cell division, but they do not discount the possibility of a limited initial morphallactic phase.


1999 ◽  
Vol 77 (11) ◽  
pp. 1835-1837 ◽  
Author(s):  
Steven R Scadding

While the effects of exogenous retinoids on amphibian limb regeneration have been studied extensively, the role of endogenous retinoids is not clear. Hence, I wished to investigate the role of endogenous retinoic acid during axolotl limb regeneration. Citral is a known inhibitor of retinoic acid synthesis. Thus, I treated regenerating limbs of the larval axolotl Ambystoma mexicanum with citral. The result of this inhibition of retinoic acid synthesis was that limb regeneration became extremely irregular and hypomorphic, with serious pattern defects, or was inhibited altogether. I conclude that endogenous retinoic acid plays an important role in pattern formation during limb regeneration.


1998 ◽  
Vol 76 (9) ◽  
pp. 1795-1796 ◽  
Author(s):  
Steven R Scadding ◽  
Andrew Burns

The purpose of this investigation was to determine whether there were any asymmetries in the vascularization of the limb-regeneration blastema in the axolotl, Ambystoma mexicanum, that might be related to pattern formation, and to determine if retinoic acid could modify the vascular patterns of the blastema. We used acrylic casts of the vascular system of the limbs to assess the pattern of vascularization. We observed a very regular symmetrical arrangement of capillaries in the limb-regeneration blastema that did not appear to be modified by doses of retinoic acid sufficient to modify the limb pattern.


Development ◽  
1981 ◽  
Vol 66 (1) ◽  
pp. 117-126
Author(s):  
Jane Karlsson ◽  
R. J. Smith

It is a general rule that of two complementary Drosophila imaginal disc fragments, one regenerates and the other duplicates. This paper reports an investigation of an exception to this rule. Duplicating fragments from the periphery of the wing disc which lacked presumptive notum were found to regenerate notum structures during and after duplication. The propensity for this was greatest in fragments lying close to the presumptive notum, with the exception of a fragment confined to the posterior compartment, which did not regenerate notum. Structures were added sequentially, and regeneration stopped once most of the notum was present. These results are not easily explained by the polar coordinate model, which states that regeneration cannot occur from duplicating fragments. Since compartments appear to be involved in this type of regeneration as in others, it is suggested that a new type of model is required, one which permits simultaneous regeneration and duplication, and assigns a major role to compartments.


2018 ◽  
Vol 62 (9-10) ◽  
pp. 605-612 ◽  
Author(s):  
Akira Satoh ◽  
Kazumasa Mitogawa ◽  
Aki Makanae

Development ◽  
1984 ◽  
Vol 79 (1) ◽  
pp. 165-181
Author(s):  
Nigel Holder ◽  
Susan Reynolds

A relationship between pattern formation and field shape is established following the formation of rounded blastemas on lower arm limb stumps after treatment with vitamin A. Pattern formation is not affected by alteration in blastemal shape caused by removal of the dermis from the thigh region of the leg. We conclude, therefore, that blastemal shape does not play a causal role in establishing limb pattern. Data relating the number of cells present between the cardinal axial poles of blastemas and the size of blastemas is discussed in terms of short arc intercalation and short range cell—cell interactions during pattern regulation.


Development ◽  
1986 ◽  
Vol 98 (1) ◽  
pp. 137-165
Author(s):  
Vernon French ◽  
Tamara F. Rowlands

After removal of a transverse strip of ventral thorax from the beetle, Tenebrio molitor, interaction occurred between epidermis posterior to the mesothoracic leg and that anterior to the metathoracic leg. Depending on the size and position of the excision, this interaction resulted in either the regeneration of the extirpated tissue or its replacement by an A/P reversed pattern of sclerites and supernumerary leg. By either route, local pattern continuity was restored between the normal meso- and metathoracic legs. Similarly, when a leg plus adjacent tissue was extirpated, continuity was restored by leg regeneration or by formation of an A/P reversed duplication of sclerites. The results of these strip excisions can be understood in terms of two current models of the ventral thorax (the Boundary Model and the Polar Coordinate Model), each of which postulates a distinct compartment or region intervening between the epidermis surrounding the bases of successive legs. However, the models do not explain the large differences in the frequency of formation of the duplication/deletion pattern after excisions of different widths. The results are also compatible with a different model, involving an A–P sequence of positional values similar to that proposed for the abdominal segment. Regeneration would restore continuity within the sequence by the shortest route, forming either the midsegment (including the leg) or the intersegmental region. The meso- and metathorax differ in the structure of the ventral sclerites and in the segmentation of the tarsus of the leg. The structures regenerated after the various excisions show that the segment border is not crossed during regeneration and indicate that an A/P compartment border running through the leg is usually also respected. There is no sign, however, of a third line of lineage restriction that would indicate a subdivision of the segment into three compartments (as proposed in the Boundary Model).


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