Cell division during intercalary regeneration in the cockroach leg

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.

Development ◽  
1985 ◽  
Vol 85 (1) ◽  
pp. 177-190
Author(s):  
Paul R. Truby

It has been shown that after a critical point in the moult cycle of a cockroach, wound healing can occur but regeneration of pattern does not take place until the following intermoult period. Leg removal after the critical point is used to separate the processes of wound healing and leg regeneration. This permits the study of patterns of cell division resulting from wound healing to be distinguished from those involved in leg regeneration. During wound healing, cell division occurs in the epidermal cells of approximately the distal half of the trochanter. The cells then return to the resting state until after the next ecdysis. Regeneration starts with cell division occurring in the distal half of the trochanter, and then spreading to include cells of the proximal trochanter and distal coxa. This spread and the following patterns of growth and redifferentiation appear to be the same as for regeneration following leg removal prior to the critical point, with the more distal structures completing early stages of regeneration first. Scanning electron micrographs of the cuticle of the trochanter after the ecdysis following leg removal support the evidence from the patterns of cell division in suggesting that the distal half of the trochanter is dedifferentiated during wound healing.


Development ◽  
1986 ◽  
Vol 92 (1) ◽  
pp. 115-131
Author(s):  
Paul R. Truby

When the anteroposterior axis of a cockroach leg is reversed at a graft by exchanging a left leg for a right leg at the mid-tibia level, regeneration occurs in the region of the graft/host junction. This results in the formation of a pair of lateral supernumerary legs. In these experiments the patterns of cell division which take place during supernumerary leg formation were observed in sections of regenerating legs of the cockroach Leucophaea maderae. Early patterns of cell division resemble those seen in control grafts in which no axial reversal had been carried out during grafting. These cell divisions are associated with the process of wound healing. Later, a large area of the epidermis proximal to the graft/host junction becomes activated and shows a rapid rate of cell division. This area forms two outgrowths which grow by cell division throughout their epidermis to form the epidermis of the supernumerary legs. The results are more consistent with the view that the formation of supernumerary legs involves dedifferentiation of the epidermis in the region of the graft/host junction to form a blastema, rather than being due to local cell division at the point of maximum pattern discontinuity. This conclusion is used to offer an explanation for the range of different types of outcome of left-right grafts that has been observed.


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 ◽  
1978 ◽  
Vol 47 (1) ◽  
pp. 53-84
Author(s):  
Vernon French

Epidermal cells from different circumferential positions around the femur of Blabera craniifer can interact to form an intercalary regenerate. Removal of a longitudinal strip of integument (cuticle plus epidermis) from any position around the circumference leads to thecut edges healing, localized growth and intercalary regeneration of the missing section ofthe circumference, so that the resulting femur is approximately normal in size and pattern of cuticular structures. Grafting a longitudinal strip of femur integument into a different circumferential position on the host femur confronts epidermal cells from different positions along both the inner and outer longitudinal graft/host junctions. In numerous different situations this results in local growth and intercalary regeneration of that section of the circumference normally separating graft and host positions, by the shorter route around the circumference. Confrontation of opposite positions results in the intercalation of either of the intervening half circumferences. In one opposite confrontation, between mid-anterior and mid-posterior, there was also a third result where graft and host healed together, provoking no intercalary regeneration. Grafts made with reversed proximal/distal polarity show that a confrontation between different circumferential positions gives the same result, regardless of the proximal/distal levels involved, hence circumferential position is an independent aspect of position on the femur. These results strongly suggest that epidermal position is not specified with respect to two transverse axes running through the epidermis and internal tissue of the leg, but that there is a continuous circular sequence of positional values running around the circumference, in the epidermis. This is analogous to but independent of the sequence previously shown by Bohn (1967) and Bulliere (1971) to run proximal/distal along a leg segment. Hence epidermal position on the femur is specified in two dimensions and can be represented in terms of the French, Bryant & Bryant (1976) polar co-ordinate model. Interactions along the edges of the strip-grafts conform to the Shortest Intercalation Rule (French et al. 1976). At the proximal and distal ends of strip-grafts intercalation restores normal sequences of positional values where possible. However, where the graft, together with the intercalary regenerates formed at the longitudinal graft/host junctions and the adjacent host tissue formed a complete sequence of circular values, then a supernumerary distal regenerate was formed, in agreement with the Complete Circle Rule of French et al. (1976). The problem of generating a continuous circular sequence of positional values by one or more circumferential gradients, is briefly discussed.


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 ◽  
1987 ◽  
Vol 101 (2) ◽  
pp. 221-235 ◽  
Author(s):  
G.L. Campbell ◽  
P.M.J. Shelton

The confrontation of cells from the anterior region of an abdominal segment of Oncopeltus with those from the posterior region of the same or the adjacent segment results in the generation of a segment border. The behaviour of epidermal cells during this regulation is described. It consists primarily of cell division and transverse elongation of cells at the site of confrontation. This behaviour can be separated from any associated purely with wound healing because a similar-sized wound to that used to ablate the segment border, performed within the segment, does not result in any cell division or elongation. The results are consistent with the view that there is a discontinuity in positional values at the segment border. The stability of such a discontinuity and the regeneration of segment borders are discussed in terms of there being a special population of cells at the segment border that have the property of isolating other cells with the maximum difference in positional values.


Development ◽  
1973 ◽  
Vol 30 (3) ◽  
pp. 681-699 ◽  
Author(s):  
Peter A. Lawrence

X-irradiation of eggs and larvae of Oncopeltus fasciatus results in the development of clonal patches of epidermal cells of unusual pigmentation. The frequency, size and distribution of these patches is dependent on the dose and timing of irradiation. Analysis of these clones in the abdomen has shown that the presumptive epidermis becomes effectively segmented during blastoderm formation and thereafter the clones are restricted to within a segment quadrant (dorsal or ventral, left or right). There are approximately 10 presumptive epidermal cells per segment quadrant. The shape of the clones and the orientation of mitoses in larvae suggest that both early and late cells of the anterior margin of the segments divide with a preferred orientation (cleavage plane parallel to the antero-posterior axis). Elsewhere in the larval segment the mitoses are randomly oriented, and the segment grows evenly all over. The number of mitoses/cell/moult cycle is not precisely determined, but the amount of cell division is perhaps under a general probabilistic control. It is suggested that the segmental gradient may be involved in this control.


Genetics ◽  
2000 ◽  
Vol 156 (4) ◽  
pp. 1817-1828 ◽  
Author(s):  
Wei Geng ◽  
Biao He ◽  
Mina Wang ◽  
Paul N Adler

Abstract During their differentiation epidermal cells of Drosophila form a rich variety of polarized structures. These include the epidermal hairs that decorate much of the adult cuticular surface, the shafts of the bristle sense organs, the lateral extensions of the arista, and the larval denticles. These cuticular structures are produced by cytoskeletal-mediated outgrowths of epidermal cells. Mutations in the tricornered gene result in the splitting or branching of all of these structures. Thus, tricornered function appears to be important for maintaining the integrity of the outgrowths. tricornered mutations however do not have major effects on the growth or shape of these cellular extensions. Inhibiting actin polymerization in differentiating cells by cytochalasin D or latrunculin A treatment also induces the splitting of hairs and bristles, suggesting that the actin cytoskeleton might be a target of tricornered. However, the drugs also result in short, fat, and occasionally malformed hairs and bristles. The data suggest that the function of the actin cytoskeleton is important for maintaining the integrity of cellular extensions as well as their growth and shape. Thus, if tricornered causes the splitting of cellular extensions by interacting with the actin cytoskeleton it likely does so in a subtle way. Consistent with this possibility we found that a weak tricornered mutant is hypersensitive to cytochalasin D. We have cloned the tricornered gene and found that it encodes the Drosophila NDR kinase. This is a conserved ser/thr protein kinase found in Caenorhabditis elegans and humans that is related to a number of kinases that have been found to be important in controlling cell structure and proliferation.


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.


Development ◽  
1997 ◽  
Vol 124 (18) ◽  
pp. 3555-3563 ◽  
Author(s):  
K. Weigmann ◽  
S.M. Cohen ◽  
C.F. Lehner

During larval development, Drosophila imaginal discs increase in size about 1000-fold and cells are instructed to acquire distinct fates as a function of their position. The secreted signaling molecules Wingless and Decapentaplegic have been implicated as sources of positional information that globally control growth and patterning. Evidence has also been presented that local cell interactions play an important role in controlling cell proliferation in imaginal discs. As a first step to understanding how patterning cues influence growth we investigated the effects of blocking cell division at different times and in spatially controlled manner by inactivation of the mitotic kinase Cdc2 in developing imaginal discs. We find that cell growth continues after inactivation of Cdc2, with little effect on overall patterning. The mechanisms that regulate size of the disc therefore do not function by regulating cell division, but appear to act primarily by regulating size in terms of physical distance or tissue volume.


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