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Observations of Dependent Histogenesis in Salamander Limb Development

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Observations of Dependent Histogenesis in Salamander Limb Development /. Embryol. exp. Morph., Vol. 11, Part 2, pp. 325-338, June 1963 Printed in Great Britain Observations of Dependent Histogenesis in Salamander Limb Development by CYRIL V. FINNEGAN1 From the Department of Zoology, University of British Columbia INTRODUCTION PREVIOUS work in this laboratory (Finnegan, 1962) had suggested that limb development might be specifically enhanced by experimentally associated somite mesoderm tissue. Detwiler (1938), Swett (1945) and Nicholas (1958) called atten- tion to the influence of this mesoderm in the production of duplications when limb buds were transplanted heterotopically to the superficial somite region and, more recently, Amano (1960) stated that somite tissue was required, inductively and materially, for limb development. In an analysis of development it is assumed that a group of cells, whose histo- genesis has been determined by their previous experience, will evidence that histo- genesis if placed in an environment in which they continue to develop. Thus, after limb bud transplantation to the flank in urodeles, positive results (that is, histo- genesis, proximally, accompanied by growth, distally) have been interpreted as self-differentiation of the limb bud cell mass (see review by Nicholas, 1955). However, the possible synergistic role of the somite mesoderm in the histogenesis of the transplant has not been considered. It may be that greater histogenetic competence has been ascribed to the limb cell mass than it actually posesses. In this respect Wilde (1950) was able to show, by in vitro studies, a dependency of limb differentiation on donor developmental age. The more ventral region of the urodele flank has been considered an unfavour- able site for limb development (Nicholas, 1924; Takaya, 1938) since limb bud transplanted to that region does not continue its development. It seemed desir- able then to use this ventral flank as the transplantation site in order to disclose the actual histogenetic ability of the limb cell mass under environmental conditions which do not specifically assist its development. The same ventral environment was then used to obtain evidence of the possible supportive role of the epibrachial somite mesoderm in the histogenesis of the transplanted limb cell mass. Finally, results of an analysis of the relative supportive capacity of the dorsal somite and of the ventral somite tissue are included in this report. Author's address: Department of Zoology, University of British Columbia, Vancouver 8, Canada. 326 CYRIL V. FINNEGAN EXPERIMENTAL PROCEDURE The mesoderm and overlying ectoderm comprising the limb bud cell mass lying superficial to the somatic hypomere ventral to the pronephric kidney area (see Text-fig. 1) was excised from post-neurula stages of Ambystoma punctatum and Taricha torosa, Stages 25 to 38 inclusive. An incision was made in the ectoderm immediately ventral to this cell mass and the latter was then carefully lifted away from the underlying mesoderm by means of a finely sharpened steel needle. The ectodermal incision was continued around the mesodermal cell mass so that only the material in the cell mass at the time of operation, and not the entire limb disc of 3-4 somites (Nicholas, 1955), was included in the transplant. According to TEXT-FIG. 1. Lateral view of tail-bud embryo. The areas removed in the operation are indicated by cross-hatching. L = approximate limb area removed. S = approximate area of epibrachial somite removed. P = Pro- nephros. The boundary of the conventional limb disc is indicated by the dotted line. (Modified from Swett, 1945.) Schwind (1932), this cell mass comprises the limb tissue and contains little or no girdle tissue. A small incision was made in the ventral or ventrolateral ectoderm of the host animals, of approximately the same developmental age as the donors, and the excised limb material was placed in the incision so that the limb mesoderm cell mass was in contact with the hypomeric mesoderm of the host. The initial cut was made small since the wound tended to increase in size rendering subsequent contact of the host and donor ectoderm difficult to achieve. A glass bridge was used to hold the transplant in position until healing had occurred. In the series of experiments involving the addition of somite mesoderm, a por- tion of the donor's epibrachial somites (somites 3-5) ventral to the lateral line was removed (see Text-fig. 1). This material was placed beneath the host's ventral ecto- derm through the incision which subsequently received the donor limb cell mass, HISTOGENESIS OF LIMB 327 and the two transplants were finally placed so that the mesoderm of limb and somite were juxtaposed. These operations involving the ventral flank were difficult to conduct so that complete healing would result, and thus, while over sixty animals were prepared, the results are based on observation of the smaller number (thirty-eight) in which the healing was such as to ensure the retention of the graft in the desired relation to the host's ventral hypomere or the grafted somite tissue. When the limb cell mass was transplanted to the host's somite mesoderm in the final series of experiments, the grafted limb tissue was placed so that the mesoderm of the transplant was in contact with the superficial area of the somite, either dorsal to or ventral to the lateral line. Ambystoma gracile embryos were used as donors in some of these cases and Taricha torosa embryos were used as donors in other cases. The latter species was used as the host animal in all of the seventeen pre- pared cases. Aseptic techniques were used throughout and the host animals reared in urodele growing medium (Rugh, 1962) at 18° C. Animals were prepared for histological examination by being fixed in Michaelis', sectioned at 8-10 /x and stained with haematoxylin and eosin. TABLE 1 Limb histogenesis in ventral sites Procedure Histogenesis Culture time Donor-host (weeks) Pronephros Cartilage Muscle Den I. T. torosa-T. torosa: (1) Limb bud (stages 25-35) 3 + _ _ + (2) Plus ectoderm (stage 35) 3 — + * — + (3) Plus epibrachial somite (stage 35) 2 — + +t + § + II. A. punctatum-T. torosa: (1) Limb bud (stage 35) 3 + + + + + III. A. punctatum-A. punctatum: (1) Limb bud (stages 30-35) 3 — + — + (2) Plus ectoderm (stage 35) 3+ — + — + (3) Plus epibrachial somite (stage 35) 2+ — + + +$ + + II + IV. T. torosa-A. punctatum: (1) Limb bud (a) Stage 25 8 — + + + — + (b) Stage 30 8 — + + + — + (c) Stage 35 8 — + + + ++ + * + Some concentric cell orientation was observed. t + + Definite cell orientation and a perichondrium were present. % + + + Definite cartilage (cells and matrix) observed. §+ Cell orientation and cytoplasmic acidophilia interpreted as possible myoblastic development. 11 + + A more definite muscle tissue was histologically identifiable. 328 CYRIL V. FINNEGAN RESULTS Heterotopic transplantation to a ventral (hypomere) site The results of both homoplastic and heteroplastic transplantation of limb bud are summarized in Table 1 and are considered further in the following. Limb bud alone as the transplant To facilitate description of the results the donors are grouped as representative of three developmental ages; a Stage 25 group, a Stage 30 group and a Stage 35 group. TSL&dBfr* TEXT-FIG. 2. A section through the ventral flank of a T. torosa host at 3 weeks after transplanta- tion of Stage 35 torosa limb cell mass. A prone- phric tissue (P) and mesentery (M) have differ- entiated internally and a reduced aggregation of basiphilic cells is present superficially (LBE-11). Triturus torosa transplant to Triturus torosa hosts (8 cases). During the first post-operative week the Stage 35 cases developed a projection nearly equal in size to that of the host's anterior limb but the other two donor stages exhibited only a small bump in the graft area. The graft appeared to regress relative to the growth of the host during the second week in all cases, so that, in the third week, the transplant was visible as a cell mass within the ventral body wall. The sectioned material fixed in the third week revealed that a pronephric unit had differentiated in the deeper portion of the graft area in all cases (see Text-fig. 2). This kidney tissue continued from the graft through the mesentery to the ven- tral wall of the host's gut. In some cases a short pronephric duct had developed HISTOGENESIS OF LIMB 329 either anteriorly or posteriorly from the kidney tissue and in contact with the host's somatic peritoneum. An aggregation of basiphilic cells was always found located immediately superficial to one end of the pronephric unit. The smallest such mass was present in the Stage 25 cases and the largest was in the Stage 35 cases, although this mass in all cases was obviously reduced as compared with the normal limb mesoderm cell mass. Ambystoma punctatum transplant to Ambystoma punctatum hosts (5 cases). The projections initially developed from the transplanted limb cell masses regressed, in the second week, to small mounds on the ventral flank which, when examined histologically, indicated early cartilage-like cell orientation. A thick *•:'•>, TEXT-FIG. 3. A section through the ventral flank of a T. torosa host at 3 weeks after transplantation of Stage 35 punctatum limb cell mass. A pronephric tissue (P) and mesentery (M) have developed internally and a girdle-like unit (G) with associated oriented cells lies more superficial (LBS-13). dermis, with dorso-ventrally oriented fibroblasts and much ground substance, was present superficial to the procartilage cell mass. In the third week, the graft area was visible macroscopically as a cell mass in the ventral body wall and sectioned material showed that the cartilage-like cell group had a definite peri- chondrium but little to no matrix production was evident. In some cases a mesentery was present from the graft to the host's gut wall, but no pronephric differentiation was observed.
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