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Seasonal Changes in the Fine Structure of the Basal J. Cell Set. 2, 401-410 (1967) 401 Printed in Great Britain SEASONAL CHANGES IN THE FINE STRUCTURE OF THE BASAL GRANULAR CELLS OF THE BAT THYROID E.A.NUNEZ Department of Radiology, Cornell University Medical School, New York City R. P. GOULD Department of Anatomy, The Middlesex Hospital Medical School, London D. W. HAMILTON Department of Anatomy, Harvard Medical School, Boston J. S. HAYWARD Department of Zoology, University of Alberta, Edmonton, Canada AND S. J. HOLT The Courtauld Institute of Biochemistry, The Middlesex Hospital Medical School, London SUMMARY The fine structure of the thyroid gland of non-hibernating, hibernating, and intermittently aroused hibernating bats was examined. It was found that in addition to the ordinary, follicular cell, another widespread thyroid cell type is present in all bats examined. This cell is situated in the basal region of the thyroid follicle and is characterized by a cytoplasm full of secretory- like granules. In the basal cells of bats captured in April and June the granules consist of an extremely dense core and are of a uniform size averaging from 0-1-0-5 /* i*1 diameter. In bats caught in August the solid dense granules vary greatly in size and large granules of diameters from 2 to 5 H are common. These large granules are often found concentrated in groups in the most basal region of the follicular epithelium. Hibernating bats are characterized by partly or totally degranulated basal thyroid cells. The cytoplasmic granules in the partly degranulated cell vary greatly in appearance, ranging from solid dense granules to empty vesicles. In totally degranulated basal cells, empty vesicles fill the cytoplasmic matrix. The granular endoplasmic reticulum of the basal thyroid cell also shows seasonal changes, while the Golgi complex remains a well-developed organelle throughout the year. These observations suggest that the thyroid basal granular cell is involved in secretory activities; its possible functional role is discussed. INTRODUCTION Animals that undergo hibernation are characterized by seasonal alterations in many physiological functions (Hoffman, 1965). One of the more striking changes occurs in the rate of oxygen consumption, which is elevated during the summer and greatly decreased during hibernation (Erikson, 1956; Popovic, 1955). Since cellular respiration is considered to be under thyroidal regulation (Tata, Ernster & Lindberg, 1962) there have been many investigations of the effect of seasonal changes on the thyroid gland of animals that undergo hibernation (Hoffman, 1965). During hibernation the thyroid gland involutes (Hoffman & Zarrow, 1958) and its capacity to concentrate circulating 402 E. A. Nunez, R. P. Gould, D. W. Hamilton, J. S. Hayward and S. J. Holt radioiodine is abolished (Vidovic & Popovic, 1954). It is therefore surprising that, although numerous electron-microscope studies of the thyroid have been made which have greatly contributed to our knowledge of this gland (Monroe, 1953; Ekholm & Sjostrand, 1957; Wissig, i960; Herman, i960; Irie, i960; Fujita, 1963; Muramoto, 1964; Fujita & Machino, 1965), none has dealt in any detail with the thyroid of hibernating animals. The present investigation is an electron-microscope study of the thyroid gland of bats collected in spring, summer and during hibernation, and after experimental arousal of hibernating animals. The fine structure, occurrence, and seasonal changes of the basal granular thyroid cells are reported and the significance of the findings is discussed. MATERIAL AND METHODS Adult normal bats of both sexes and of the species Myotis lucifugus (U.S.A.) and Nyctala noctula (England) were used in this study. Non-hibernating bats were cap- tured in their natural habitats in April (Nyctala), June (Myotis) and August (Nyctala). Hibernating bats (Nyctala) were collected in late November from a tree. The animals were killed by ether inhalation and the thyroid glands removed and placed into either Karnovsky's fixative (Karnovsky, 1965) for 6 h, or 6-25 % glutaraldehyde in o-o67M cacodylate buffer, pH 7-3, for 2 h. Following fixation, the tissues were washed in ice-cold 0-25 M sucrose buffered at pH 7-4 with 0-067M cacodylate. Thyroids were also removed from hibernating bats used in a study of the arousal process. The hibernating bats were kept in this state for 8 weeks at 4°-io °C, except that every third to fifth day they were aroused by removal from the cold room and fed mealworms (Tenebrio) to ensure their survival over the experimental period. During the feeding period and immediately after returning to the cold room, the bats exhibited considerable activity for an hour before their return to hibernating body temperature. At the end of the 8th week, the bats were killed, the thyroid glands removed, placed in Karnovsky's fixative for 6 h and then washed in the sucrose/cacodylate buffer. All tissues were post-fixed in phosphate-buffered 1 % osmium tetroxide, pH 7-4, for 1 h and then dehydrated through a graded series of ethanol solutions. The tissues were embedded in either Epon or Araldite. Thin sections were cut with glass or diamond knives on either a Porter-Blum MT-2 or Huxley ultramicrotome, mounted on copper grids and stained with 4% uranyl acetate (Watson, 1958) and/or lead citrate (Reynolds, 1963). The sections were studied in a Philips EM 200 or an AEI EM 6 electron microscope. For light microscopy, 1-2 fi sections were obtained from the embedded material and stained with a 1 % solution of toluidine blue. RESULTS Two varieties of follicle predominate in the bat thyroid gland. One is composed entirely of follicular cells (Fig. 1), while the other contains, in addition to the ordinary follicular cell, a widespread basal cell characterized by a cytoplasm filled with dense Seasonal changes in bat thyroid 403 granules (Fig. 3). The thyroid follicular cell of the active bat is cuboidal (Figs. 1, 3) and rests upon the follicular basement membrane (Fig. 1). It invariably possesses apical microvilli, which are short, irregular in shape, and unevenly spaced along the surface of the cells (Figs. 1, 2). Very rarely, cilia are seen projecting into the colloid (Fig. 2). The filaments of the cilia appear to arise from the apical region of the cyto- plasmic matrix. Terminal bars are prominent (Figs. 1, 3), and the apposed lateral plasma membranes of adjoining cells are approximately straight (Fig. 2). Nuclei are oval, centrally located, and have regular outlines. Oval to elongate mitochondria are found mainly in the basal half of the cell. They are usually in close contact with the granular endoplasmic reticulum and occasionally appear to be completely enfolded by its cisternae (Figs. 1-3). The baSally located endoplasmic reticulum consists of ribosome-dotted cisternae, characteristically widely dilated and containing a material of low electron density. The Golgi complex is relatively inconspicuous and usually situated in the apical half of the cell (Fig. 2). It consists of several dilated saccules and occasional vesicles. Beneath the apical surface are numerous small vesicles of light- to-medium density (Figs. 1, 2). Dense, lysosome-like bodies are present in the supra- nuclear half of the cell (Figs. 1-3). Colloid droplets are small and not abundant; when present they are found in the apical half of the cell (not shown in micrographs). The basal cell in the non-hibernating bat is an irregularly shaped granular epi- thelial cell, usually larger than the follicular cell. Such cells are usually found grouped together as irregular sheets and masses in the basal portion of the follicular epi- thelium (Fig. 3). They are separated from the luminal colloid by the cytoplasm of the follicular cells, and those most basally situated rest on the follicular basement mem- brane (Figs. 3-8). The salient feature of the basal epithelial cell are the numerous secretory-like granules that fill extensive areas of the cytoplasmic matrix (Figs. 3-8). The granules are characterized by an extremely dense core, sometimes surrounded by an outer light rim, and are individually bounded by a smooth membrane (Fig. 5, inset). They exhibit seasonal changes in size in the non-hibernating bat. In April and June the granules are fairly uniform in size, averaging from o-i to 0-5 ji in diameter (Figs. 3, 4). In the August animals the granules vary greatly in size (Fig. 5) and large, dense granules of 2-5 /i diameter are common (Fig. 6). Often, a group of very large, dense granules fills the entire cytoplasmic matrix of those cells situated in the most basal region of the follicle (Fig. 8). In basal cells of both spring and summer animals there is a well-developed Golgi complex, showing three to five groups of slightly dilated saccules that are often arranged in a roughly circular or horseshoe-like shape (Figs. 4, 5 and 7). In the centre of the Golgi complex are found numerous vesicles, vacuoles, and discrete granules. Some of the vacuoles contain dense material and granules similar in appearance to the granules distributed throughout the cell body (Figs. 4, 7). Long cilium-like structures (possibly centrioles) and multivesicular bodies are associated with the Golgi zone (Fig. 7). Large spherical vacuoles, which often contain flocculent material or small eccentrically placed dense granules are found distributed throughout the cytoplasmic matrix (Figs. 3, 4). The granular endoplasmic reticulum and clusters of free ribosomes are much more abundant in the basal cells of the summer animals (Figs. 5, 6) than in those of the spring animals (Figs. 3, 4). In 26 Cell Sci. 2 404 E. A. Nunez, R. P. Gould, D. W. Hamilton, J. S. Hayward and S. J. Holt the latter the granular endoplasmic reticulum consists mostly of numerous individual rod-like profiles. On the other hand, the prominent granular endoplasmic reticulum in the basal cell of the August animals consists of long tubular channels which are mostly arranged in parallel stacks or whorls of concentric lamellae (Figs.
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