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During Early Embryogenesis of the Chick, the Cells of the Primitive Streak Play a Key Role in the Development of the Primary Embryonic Structures

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During Early Embryogenesis of the Chick, the Cells of the Primitive Streak Play a Key Role in the Development of the Primary Embryonic Structures VOL. 55, 1966 ZOOLOGY: SANYAL AND NIU 743 10 Freese, E., in Brookhaven Symposia in Biology, No. 12 (1959), p. 63; Freese, E. B., these PROCEEDINGS, 47, 540 (1961). 11 Muller, H. J., in The Control of Hunman Heredity and Evolution, ed. T. M. Sonneborn (New York: Macmillan, 1965), p. 100. EFFECTS OF RNA ON THE DEVELOPMENTAL POTENTIALITY OF THE POSTERIOR PRIMITIVE STREAK OF THE CHICK BLASTODERM* BY SOMES SANYALt AND M. C. Niu DEPARTMENT OF BIOLOGY, TEMPLE UNIVERSITY, PHILADELPHIA Communicated by Victor C. Twitty, February 7, 1966 During early embryogenesis of the chick, the cells of the primitive streak play a key role in the development of the primary embryonic structures. However, the developmental potentiality of the streak at the different levels along its antero- posterior axis is not uniform. This is most striking when comparing the anterior regions including Hensen's node with the posterior portions under a variety of ex- perimental conditions.' Hensen's node has long been recognized as the center for the primary organization of the chick embryo. The regions more than 0.4-0.5 mm behind the node do not participate in the formation of central nervous tissue.2 When posterior portions of the primitive streak are transplanted to other embryos, we have noted that they do not differentiate into any histologically identifiable structure and in the majority of cases the implants become completely absorbed into the extraembryonic tissues of the host. If, however, they are combined with such tissue as Hensen's node, they are induced to undergo differentiation.' In view of the finding that RNA induces the formation of specific structure4 or specific protein,5 it was decided to treat the posterior segment of primitive streak with RNA and subsequently to study the effect of-the exogenous RNA on its developmental potency. The RNA used was extracted from brain, liver, kidney, heart, and com- mercial yeast. The purpose of this paper is to present data showing that freshly isolated RNA from the various tissues indeed affects the developmental potentiality of the posterior streak. The effect is specific and varied in accord with the kind of RNA employed. Material and Methods.-Material: All experiments reported in this study were performed on the definitive streak stage of chick embryos (Hamburger and Hamilton, stage 4).6 Fertilized eggs of the white Leghorn variety were obtained from Shaw's hatchery, W. Chester, Pa., and incubated in a forced-draft incubator for 16-18 hr at 380C. Experimental: The donor embryos were first explanted from the eggs. The portion of the primi- tive streak constituting one fourth of the total length of the streak, extending posteriorly from its middle, was dissected out under a binocular microscope. Since the length of the streak was about 1.4-1.8 mm, the anterior margin of the piece used was 0.7-0.9 mm posterior to the primitive pit. The RNA's used were separately dissolved in Pannet-Compton's saline at a concentration of 40-80 OD (optical density at 260 mu) per ml. Each OD is approximately equivalent to 50 jug of RNA. The isolates of posterior streak were transferred to the saline with and without RNA. Both were kept at 2-4oC for 6-8 hr before being transplanted to the host embryos. Embryos to serve as hosts were grown in vitro according to New's techniques The intact blastoderm after 16-18 hr of incubation was excised together with a large portion of the vitelline Downloaded by guest on October 1, 2021 744 ZOOLOGY: SANYAL AND NIU PROC. N. A. S. membrane and immediately transferred to a watch glass with the hypoblast facing up. A glass ring about an inch in diameter was so placed on the vitelline membrane that the blastoderm was located in the center, with the periphery of the membrane wrapping around the ring. Fluid albumen from the same eggs was added to the outside of the ring as nutrient. Both RNA-treated and untreated isolates were rinsed quickly in Pannet-Compton's saline and grafted onto the blastoderm (one in each host embryo) at the level of Hensen's node near the margin of the area pellucida. This was accomplished by making a very small slit on the hypoblast through which the isolate could be pushed into the space between the epiblast and the hypoblast. The microsurgery was performed with a pair of stainless steel needles. Sterile precautions were observed throughout the operation. After operation at room temperature (22-240C) the embryos were immediately returned to the incubator and allowed to develop for 24-26 hr. They were fixed in Bouin's fluid, sectioned at 8 ,u, and stained with hematoxylin and eosin. Preparation of RNA: RNA was extracted from chick brain, chick liver, calf brain, calf liver, calf kidney, and calf heart. Brains and livers of 10-12-day chick embryos were pooled and im- mediately frozen on dry ice. The calf tissues were brought from the slaughterhouse in ice-cold sucrose solution (0.25 M) and used immediately for RNA isolation or stored frozen in dry ice no more than 10 days before use. The RNA's were prepared by a modifications of Kirby's8 procedure. The tissue homogenates were deproteinized twice with water-saturated phenol. Polysaccharides and other particles were removed by centrifugation at 20C (Spinco-30,000 rpm for 45 min). The supernatant was precipitated by alcohol and redissolved in saline. This was repeated three times. The last alcohol precipitate was dissolved in Pannet-Compton's saline. The yeast RNA, pur- chased from Schwarz BioResearch, Inc., was reprecipitated by 2 vol of alcohol. All of our RNA preparations gave a positive orcinol reaction and a maximum UV absorption at 258-260 mM and a minimum at 230 my. The ratio between 230 and 260 was over 2 and that of 260 and 280 was above 0.45 but less than 0.5. It should be emphasized that the RNA was either freshly prepared or quickly frozen in acetone-dry ice mixture and subsequently stored in a deep freezer for 3-5 days. In experiments with ribonuclease, the liver RNA and crystallized ribonuclease (Worthington Biochemical Co.) were dissolved separately in Pannet-Compton's saline and mixed to make up the final concentration of 80 OD units of RNA and 1 mg of ribonuclease per ml of the RNA solution. This mixture was incubated at 37CC, pH 7, for 1 hr and cooled to 20C before use. RNase activity was inactivated by the rabbit antiserum against RNase. However, there was practically no difference observed in experiments with and without the presence of added RNase. Results.-Development of untreated fragments of the primitive streak: A total of 39 cases were studied in which the posterior isolates of the definitive streak were kept in the saline solution for 6-8 hr. After grafting to the host embryos, 24-26 hr were allowed for further development. Of the 39 grafts, 28 showed no trace of the implanted cells in serial sections of the host embryos. Thickened ectoderm re- sembling a neural plate developed in one case. Persistent grafts were found in ten embryos. A typical example is shown in Figure 1, where it can be seen that the ec- toderm is slightly thicker than the adjoining extraembryonic ectoderm overlying a mass of very loosely scattered mesenchymal cells. No definite structure or pattern was noted in any of these ten grafts. Thus, the posterior portions of the primi- tive streak under the experimental condition employed here can develop at best into mesenchyme cells. FIG. 1.-Cross section of a trans- _ from the posterior primitive _ __plant AT streak of chick blastoderm. (control). ~~~~~~Itwas allowed to develop in the ex- traembryonic area for 24 hr. Note layer of ectoderm cells overlying a mass of mesodermal cells and absence of any definite histological structure. X 50. Downloaded by guest on October 1, 2021 VOL. 55, 1966 ZOOLOGY: SANYAL AND NIU 745 Hi~~~~~A '... FIG. 2.-Cross section of two transplants treated with chick brain RNA. Note the development of neuralAtissue which*~~~~~~~~~~~~~~~~~~~Aroverlies a mass of loose mesodermal cells. X 50. A FIG. 3.-Cross section of two transplants treated with liver RNA. (A) Calf liver RNA. Note the presence of neural tissue and the enhanced development of mesodermal cells (arrow). X100. (B) Chick liver RNA. X50. Effects of RNA isolated from different tissueson development of the posterior primi- tive streak: Pretreatment with various RNA's evoked a distinct shift in the de- velopmental potentiality of the posterior portion of the primitive streak. Table 1 shows the frequency of occurrence of neural structures, nonneural tissues, and ab- sorption in the various series. Brain RNA: Isolates of the posterior portion of the streak were exposed to RNA Downloaded by guest on October 1, 2021 746 ZOOLOGY: SANYAL AND NIU PROC. N. A. S. TABLE 1 NUMBERS AND PERCENTAGES* OF GRAFTS SHOWING DIFFERENTIATION IN CONTROL AND 1ANA-T'REATED SERIES No. of No. of No. of neural nonneural No. of cases RNA source cases tissue tissue absorbed Control 39 1(2.6) 10(25.6) 28(71.8) Chick brain 29 10(34.5) 9(31.0) 10(34.5) Chick liver 28 10(35.7) 10(35.7) 8(28.6) Calf liver 35 18(51.4) 6(31.4) 11(31.4) Calf kidney 35 2(5.7) 12(34.3) 21(60.0) Calf heart 30 1(3.4) 14(46.6) 15(50.0) Commercial yeast 22 0(0) 3(13.6) 19(86.4) Calf liver RNA plus RNase 26 4(15.3) 8(30.9) 14(53.8) * Percentages in parentheses.
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