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Repair of Ultraviolet Irradiation Damage to a Cytoplasmic Proc. Nat. Acad. Sci. USA Vol. 72, No. 4, pp. 1235-1239, April 1975 Repair of Ultraviolet Irradiation Damage to a Cytoplasmic Component Required for Neural Induction in the Amphibian Egg (cortex/vegetal hemisphere/gray crescent/dorsal lip/gastrulation) HAE-MOON CHUNG AND GEORGE M. MALACINSKI Department of Zoology, Indiana University, Bloomington, Ind. 47401 Communicated by Robert Briggs, January 2, 1975 ABSTRACT Localized ultraviolet irradiation of the am- In order to gain direct insight into whether an ultraviolet phibian egg destroys a cytoplasmic component that is sensitive component(s) localized in the egg cytoplasm prior required for neural induction. Destruction of that com- ponent severely diminishes the inducing capacity of the to first cleavage division is actually involved in neural dorsal lip at gastrulation, as determined by embryological induction, the following question was posed: Does regional assays. Repair of the ultraviolet lesion can be achieved by UV damage to the egg affect the subsequent inducing capacity replacing the dorsal lip of the irradiated embyro with a of the dorsal lip during gastrulation? By assaying for inducing lip from an unirradiated embryo. capacity of dorsal lips from irradiated embryos and replacing Various types of analyses have established that components the dorsal lips of irradiated embryos with normal lips it was of the amphibian egg cytoplasm influence the pattern of early possible to conclude that UV does indeed damage a localized morphogenesis (see ref. 1 for a review). One of the most component of the egg cytoplasm that is necessary for neural conveniently demonstrated, yet most incompletely under- morphogenesis. stood, cytoplasmic components in the amphibian egg is the MATERlALS AND METHODS gray crescent. It is located on the future dorsal side of the egg and is the site of formation of the dorsal lip. Experiments Source of Amphibians. Rana pipiens were obtained in both of Curtis (2), in which pieces of the cortex from the gray the spring and fall from Lake Champlain Frog Farm (Alburg, crescent were grafted onto the ventral side of another egg, Vt.). They were maintained at 5° for periods of up to 3-4 provided evidence that the cortex itself is the site of localiza- months and were induced to ovulate and were artificially tion of a component that influences embryonic axis forma- inseminated by standard procedures (10). tion. The interpretation received support from a series of UVIrradiation. Eggs were manually dejellied and irradiated cortical implantation experiments of Tompkins and Rodman within 90 min after fertilization with approximately 18,000 (3), in which a portion of the 8-cell stage cortex, when im- ergs/mm2 of 2537 A UV at the vegetal hemisphere, following planted into the blastocoel of another egg, was observed to procedures originally described by Grant (8). By carefully induce the formation of a secondary axis. The results of other dejellying the eggs, and selecting for grafting UV-irradiated experiments have, however, provided an alternative view of eggs which displayed a dorsal lip that was approximately the the process of secondary axis formation. Nieuwkoop's results same size and shape as lips on control (unirradiated) embryos, revealed that the gray crescent does not play a causal role in a uniform response to UV was achieved. Dorsal lip formation the establishment of the dorsal-ventral axis, but rather that in the irradiated embryos is usually delayed approximately the polarity established in the entire mass of the endoderm 8 hr. For each experiment, eggs from the same clutch were directs the formation of the embryonic axis (4, 5). employed as donors and recipients. The results of several investigations have demonstrated that ultraviolet (UV) irradiation of the vegetal hemisphere Dorsal Lip and Ventral Tissue Grafts. The method recently of the egg destroys the embryo's capacity for normal axis described by Hennen (11) was employed with the following formation and neural morphogenesis (6-8). Recent experi- modifications. Preliminary experiments revealed that the use ments from our laboratory confirmed that the target was of proteolytic enzyme treatment to weaken the vitelline mainly localized in the vegetal hemisphere. To avoid the membrane resulted in injury to large numbers of embryos, shielding effects of pigment, albino axolotl eggs were em- manifested most frequently by a variety of developmental ployed. Eggs which were UV irradiated in the animal hemi- abnormalities. The membrane was, therefore, manually re- sphere displayed only minor effects on neural morphogenesis, moved with watchmaker's forceps. Operations were performed while those irradiated in the vegetal hemisphere failed to in 100% Steinberg's solution containing 200 mg of penicillin neurulate. In addition, axolotl eggs which were irradiated on and 200 mg of streptomycin per liter. Within 30-60 min after the side of the egg containing the gray crescent developed in- the grafting operation embryos were changed to dechlorinated complete neural structure, while eggs irradiated on the ven- tap water containing the above-mentioned antibiotics. This tral side were apparently unaffected, providing direct evi- procedure lowered substantially the incidence of exogastrula- dence that the UV-sensitive target is largely restricted to the tion. Small pieces of dorsal lip containing the entire blastopore dorsal (gray crescent) area of the egg (9). from UV-irradiated and nonirradiated embryos were grafted to the ventral marginal zone for secondary head induction. Abbreviation: UV, ultraviolet irradiation. For the reciprocal grafts, lips were directly exchanged be- 12345 Downloaded by guest on September 27, 2021 1236 Zoology: Chung and Malacinski Proc. Nat. Acad. Sci. USA 72 (1975) GRAFT a EXTENTof- ~~FATE OF NEURAl. i NO. EXTENT of SECONDARY |UCTION EXP. MQipHO_ N U IV GENESIS AE T7_ EST of DONOR DEV +wf*iatuain secondary UV n ga lp nduction o2 218 _14 4 0 0 =33es 10 _ Z7 21 0 ° 2? 5 14 UV o lisps cZZZ2173 9 5 0 0 ,225c~ (b)R2?~7 1 0 4 0 2 <00 10Z7,I 0 2 4 3 409 13 1 x2=22.7882 +l c4 (d) 13 4 () '379 1? 8 5 14P<oO UV excha ti FIG. 2. Extent of development of secondary axial structures fiertifzation in normal embryos onto which a dorsal lip from an irradiated embryo was grafted (Fig. la). In each experiment control grafts from normal donors to normal recipients were prepared (top normal ua line of each experiment). The extent of damage to external neural morphology for each batch of donor embryos is shown for FIG. 1. Design of grafting experiments. (a) Assay of the each experiment. In experiment (a), the donors received the inducing capacity of a dorsal lip from an irradiated embryo. highest dose of UV (24,000 ergs/mm2); in experiment (b) two At 75- to 90-min post-fertilization eggs were UV-irradiated at lower doses were employed (12,000 ergs/mm2 and 15,000 ergs/ the vegetal hemisphere. At the early gastrula stage their dorsal mm2); whereas in experiments (c), (d), and (e), an intermediate lips were grafted to the ventral surface of non-UV-irradiated dose was administered to the donors (18,000 ergs/mm2). Each recipient gastrulae. At the muscular response stage (Shumway experiment was performed with eggs from a single clutch. The stage 19) the extent of secondary induction was scored as shown dorsal lips from irradiated embryos always failed to promote de- in Fig. 2. (b) Assay of the ability of a normal (non-UV-irradiated) velopment of complete secondary axes. (I), Complete secondary dorsal lip to promote neural induction in irradiated embryos. axis; (II) partial, but recognizable secondary axis; (III), secon- Dorsal lips were exchanged between UV-irradiated and normal dary lump, but no visible external features of induction; (IV), no embryos. The extent of neural morphogenesis was later scored visible evidence for the presence of a graft. Photographs of these (see Fig. 4). (c) Determination of the effects of UV of the vegetal types of secondary inductions, including histological cross sec- hemisphere on the ability of the ventral marginal zone to affect tions, are displayed in Fig. 3. subsequent neural induction. lips are unmistakably capable of inducing a complete set of tween irradiated and nonirradiated embryos. Also, the site secondary axial structures (Fig. 3a). Conversely, only one opposite to the dorsal lip (in the ventral marginal zone) was embryo of the 64 successful grafts of lips from irradiated orthotopically exchanged between irradiated and nonirradi- embryos (2%) displayed at most a poor set of secondary axial ated embryos. All embryos were incubated at 20°. structures. Twenty-five percent of the dorsal lips from Hi8tological Analysi. Embryos were fixed in 5% neutralized irradiated embryos prompted development of a partial set of formalin solution, or Masui fixative, embedded and sectioned secondary axial structures, while the remainder displayed no in the standard manner, and stained with hematoxylin-eosin visible evidence of a secondary induction. In experiment (b) or Feulgen-fast green. of Fig. 2, two doses of UV were administered to the donor embryos. Embryos which received the higher dose, and de- RESULTS veloped more severe defects in neural morphogenesis, pro- Since UV-irradiated eggs failed to undergo normal morpho- vided dorsal lips with less inducing capacity than the genesis it was predicted that the inducing capacity of the embryos of that experimental series which received the lower dorsal lip of a UV-irradiated embryo would be drastically re- UV dose. duced. Grafting experiments were carried out in which a These data were analyzed by applying the chi-square test dorsal lip from a UV-irradiated embryo was grafted onto the of independence in contingency tables. The frequencies of ventral side of a normal embryo and later scored for its secondary induction were compared for the control (normal capacity to induce a secondary set of axial structures (Fig.
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