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The Fine Structure of Blastema Cells and Differentiating Cartilage Cells in Regenerating Limbs of Amblysto~A Larvae*

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The Fine Structure of Blastema Cells and Differentiating Cartilage Cells in Regenerating Limbs of Amblysto~A Larvae* The Fine Structure of Blastema Cells and Differentiating Cartilage Cells in Regenerating Limbs of Amblysto~a Larvae* BY ELIZABETH D. HAY, M.D. (From the Department of Anatomy, CorneU University Medical College, New York) P~ATES 275 TO 281 (Received for publication, May 17, 1958) ABSTRACT Regenerating forelimbs of larval salamanders, Amblystoma punaatum, were fixed in OsO4 at various intervals after amputation and were sectioned for study with the electron microscope. The dedifferentiated cells comprising the early blas- tema were found to have a fine structure similar to that of other undifferentiated cells and to have lost all of the identifying morphological features of their tissues of origin. The cytoplasm of such cellsis characterized by numerous free ribonucleopro- tein granules and a discontinuous vesicular endoplasmic reticulum. The cells have more abundant cytoplasm and are in closer contact with each other than was previously realized. The layer of condensed ground substance investing most differentiated cell types is lacking. After a period of rapid cell division, the morphol- ogy of the blastema cell changes. Cytoplasm is now sparse and contains a high concentration of free ribonucleoprotein granules, but little endoplasmic reticulum. The differentiating cartilage cell, however, develops an extensive, highly organized endoplasmic reticulum and the Golgi apparatus also appears to become more highly differentiated and more extensive at this time. Small vesicles appear throughout the cytoplasm at the time the new cisternae originate and may con- tribute to their formation. These and other changes in the cytoplasmic organdies are discussed. INTRODUCTION Small particles of ribonucleoprotein are found The electron microscope has made it possible to either dispersed throughout the cytoplasm or extend the investigation of classical problems in closely associated with the surfaces of the mem- growth and differentiation to the level of the brane-limited system of vesicles and tubules now macromolecular organization of the cells in- commonly called the endoplasmic reticulum volved. It has revealed that the cytoplasm of (4, 5). The form of this system or organelle and differentiated cells exhibits a complexity of or- the abundance of the cytoplasmic nucleoprotein ganization not appreciated heretofore in studies granules have been shown to vary widely in with the light microscope and, furthermore, by different cells. Variations in the fine structure of means of correlated biochemical studies, it has mitochondria and of the Golgi apparatus in dif- added greatly to our knowledge of the functions of ferent functional states have also been reported. some of the cytoplasmic organelles depicted. Of The present study of the regenerating salamander particular interest to students of growth has been limb was undertaken with the object of describing the recent work (1-3) demonstrating the particu- the behavior of these cytoplasmic organelles in a late nature of the basophilic component of the biological system in which dedifferentiation, pro- cytoplasm and its relation to protein synthesis. liferative growth, and redifferentiation occur. The results of this study confirm and extend * Supported by grant C-3708 from the National previous descriptions, based on light microscopy, Institutes of Health, United States Public Health of the histology of the regenerating limb of Service. Amblystoma. The cells of the early blastema 583 J. BiOPHYStC. AND BIOCHEM. CYTOL , 1058, Vol. 4, No. 5 584 BLASTEMA AND CARTILAGE CELLS appear undifferentiated in all features of their at the tip of the limb of a group of undifferentiated submicroscopic morphology and a characteristic cells which will be referred to here as the early sequence of changes in the cytoplasmic organelles blastema. The next phase of regeneration is one of during the growth and differentiation of the rapid proliferation of blastema cells, bringing about regenerate has been demonstrated with the an increase in the length of the regenerate. The electron microscope. The observations reported first signs of cartilage and muscle redifferentiation here are mainly concerned with the cytomorphosis appear on about the 10th day. Two finger-buds of the cartilage cells. A future report will deal with are formed, soon to be followed by a third and the more complex changes that occur in muscle fourth. The process of regeneration is usually during regeneration of the salamander limb. completed 16 to 20 days after amputation. The electron microscope studies to be reported Materials and M~thods here will deal with the appearance of (a) the Amblystoma punctatum larvae, raised from eggs dedifferentiated cells of the early blastema, (b) collected near Baltimore, were used in the present the dividing and interphase cells of the proliferat- study. The animals were kept in finger-bowls (3 per ing blastema, and (c) the differentiating cartilage bowl) at 23°C. and were fed Tubifex worms. When cells. Although the major portion of the descrip- taken for study, larvae were about 18 mm. in length tion will be concerned with the appearance of the and the forelimbs possessed the fourth finger-bud. cytoplasmic organelles, reference to the general Limbs were amputated through the middle of the features of these cells will also be made. humerus and regenerating limbs were fixed at daily Fine Structure of the Dedifferentlated Cells of the intervals to the 10th postoperative day and every Early Blastema.--The cells that accumulate in the other day thereafter to the 20th day after amputation. early blastema, 3 to 6 days after amputation, are After being fixed for 2 hours in 1 per cent OsO4 buffered to pH 7.4 (6), the limbs were washed in distilled water, strikingly different from the cells in their tissues of dehydrated in alcohol or acetone and embedded in N- origin. Dedifferentiating cartilage and muscle cells butyl methacrylate, according to the techniques de- lose all of the morphological features which char- scribed by Borysko (7, 8). Longitudinal sections (0.05 acterized them in their previous state of dif- # or less in thickness) of whole limbs were cut with a ferentiation. As the cartilage cells are released into Servall microtome (9) and examined with an RCA the blastema by the dissolution of the cartilage EMU 2E or 3B electron microscope. Forty limbs were matrix, the character of their cytoplasm changes sectioned. Micrographs were taken at original magni- markedly. The relatively abundant cytoplasm fications of 1500 to 8000 and enlarged photographi- of the early blastema cell has an appreciable cally as desired. density compared to the extremely low electron Thicker (2 #) sections from the same blocks were cut with the same microtome and examined with a phase scattering properties of the cytoplasm in the contrast microscope. Some of these sections were mature cartilage cell. The cytoplasmic organelles stained, without removing the plastic, with thionine or change in appearance in a manner that will be by the periodic acid-Schiff reaction. described below. Nuclei have a fine granular karyoplasm which is less dense than that of the OBSERVATIONS differentiated cell types. There is little evidence of Course o] Regeneration as Revealed by Light organized extracellular material in the early Mieroscopy.--The histology of the regenerating blastema. The cells are in close contact with each limb of the larval Amblystama punctatum has other and are remarkably uniform in appearance been described in detail by Butler (10), Thornton (Figs. 1 and 4). This intimate association of (11, 12) and others and is summarized briefly here blastema cells has not been recognized heretofore as a background for the electron microscope ob- in studies with the light microscope. servations. After amputation through the hu- The cytoplasmic components that show the merus, epithelium migrates over the wound surface, greatest change during cell dedifferentiation are covering it completely within about 4 hours. the endoplasmic reticulum and its associated Beginning 2 to 3 days after amputation and ribonucleoprotein granules. In the differentiated continuing until about the 6th or 7th day, there is muscle or cartilage cell, the endoplasmic reticulum extensive dedifferentiatlon of the muscle, the is in the form of a highly organized, continuous cartilaginous humerus and other tissues of the network of membrane-bounded cavities. In the stump (11, 12). This results in the accumulation dedifferentiated cell of the early blastema, how- ELIZABETH D. HAY 585 ever, it becomes discontinuous, appearing in (14), rat and spider oocytes (15), and a green alga electron micrographs as round or oval vesicles and (16). occasional elongate profiles (Figs. 1 and 4). These In early blastema cells the nuclear envelope, vesicles are often rather large and dilated in ap- with its inner and outer membranes, contains pearance and their contents are of lower density many pores (p, Fig. 4), whereas in differentiated than the surrounding cytoplasm. The membranes cartilage cells nuclear pores are uncommon. Con- of the endoplasmic reticulum are sparsely covered tinuity of the cisternae of the endoplasmic retic- with delicate granules, which are seen best in ulum with the perinuclear cisterna, on the other tangential sections (gl, Figs. 3 and 4). Free hand, is frequent in the older cells and rarely seen granules of similar size (100 A) and density in- in early blastema cells. Nucleoli are prominent in crease in number in the cytoplasm during de- the young cells and consist
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