The Fine Structure of the Parathyroid Gland*
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The Fine Structure of the Parathyroid Gland* BY JERRY STEVEN TRIER, M.D. (From the Department of Anatomy, University of Washington School of Medicine, Seattle) PLATES 3 TO 10 (Received for publication, July 29, 1957) ABSTRACT The fine structure of the parathyroid of the macaque is described, and is cor- related with classical parathyroid cytology as seen in the light microscope. The two parenchymal cell types, the chief cells and the oxyphil cells, have been recognized in electron mierographs. The chief cells contain within their cyto- plasm mitochondria, endoplasmic reticulum, and Golgi bodies similar to those found in other endocrine tissues as well as frequent PAS-positive granules. The juxtanuclear body of the light microscopists is identified with stacks of parallel lamellar elements of the endoplasmic rcticulum of the ergastoplasmic or granular type. Oxyphll cells are characterized by juxtanuclear bodies and by numerous mito- chondria found throughout their cytoplasm. Puzzling lamellar whorls are described in the cytoplasm of some oxyphil cells. The endothelium of parathyroid capillaries is extremely thin in some areas and contains numerous fenestrations as well as an extensive system of vesicles. The possible significance of these structures is discussed. The connective tissue elements found in the perivascular spaces of macaque parathyroid are described. INTRODUCTION Other contributions to the present concepts con cerning the human parathyroid can be found in the It is the purpose of the present paper to report some observations on the fine structure of the reports of Bergstrand (7), Morgan (34), Pappen- parathyroid gland employing the electron micro- heimer and Wilens (45), Castleman and Mallory (10), and Gilmour (20). scope and the techniques of thin sectioning. Valuable contributions to the understanding of Throughout this study an attempt is made to cor- relate findings made with the electron microscope parathyroid structure of other mammals are con- with those based on light microscopy. tained in the descriptions of the parathyroids of the In 1880 Sandstr6m (32), in a classical paper, cat by Kohn (25), the horse by Bobeau (8), the described the constant presence of small epithelial rat by Rosof (51) and by De Robertis (15), the glandular organs in or near the thyroid of man and mouse by Foster (17), the dog by Bensley (5), and several other mammalian species. Since then many the macaque monkey by Cowdry and Scott (11) anatomists and cytologists have studied the and by Baker (3). An extensive review of the parathyroid glands of a variety of mammalian literature regarding parathyroid structure up to species. Welch in 1898 (55) outlined much of the 1939 can be found in the report of Bargmann (4). classical histology of human parathyroid as it is More recently Lever (29, 30), utilizing the elec- generally accepted today and was the first to tron microscope, has described some aspects of the recognize and describe accurately the oxyphil cells. fine structure of rat parathyroids. This present paper confirms many of the obser- * This study was supported in part by grants from the Life Insurance Medical Research Fund and from vations reported in papers mentioned above, and the United States Public Health Service, Department in addition presents some new findings not yet in- of Health, Education and Welfare (Grant H-2598.) cluded in the literature. 13 J. BIOPHYSIC. AlqV BIOCHEM. CYTOL., 1~58, Vol. 4, No. 1 14 FINE STRUCTURE OF PARATHYROID GLAND Materials and Methods of ribonucleaso prepared from a commercial prepara- tion 1 of crystalline salt-free ribonudease and distilled The macaque monkey was selected as the animal of water. The sections were flooded with the enzyme solu- choice for this study, since the parathyroids obtained tion and incubated at 37°C. for 3 hours. Control sections from the mature monkey possess both chief cells and were handled in exactly the same manner as the experi- oxyphil cells (11, 3). The parathyroids of the more mental sections, except that distilled water was substi- common laboratory animals are said to contain only tuted for the enzyme solution. Following the incubation chief cells. both experimental and control sections were simul- Mature male and female monkeys of the species, taneously stained with various dyes, including iron Macaca mulatta, were anesthetized by intravenous hematoxylin, gallocyanin-chromalum, and others injection of pentobarbital sodium. The thyroid gland known to stain intensively structures with a high con- was exposed with a minimum of trauma and the ex- tent of nucleic acids. ternal parathyroids were located on the lateral aspect of each thyroid lobe, embedded within the tissue of the OBSERVATIONS thyroid just below its surface. In most animals one external parathyroid was pre- The external parathyroid glands of the macaque pared for examination with the electron microscope monkey are composed of a compact parenchyma while the other was reserved for study by light micros- containing two basic cell types: chief cells and copy. oxyphil cells. A profuse network of vascular The parathyroids used for study with the electron channels, with associated perivaseular structures, microscope were removed while the animal was still traverses the dense stroma of the gland. alive and were fixed immediately in a 1 per cent solu- tion of osmic acid buffered with veronal acetate to pH 7.3-7.5 (35). The duration of the fixation was ~ to 1 Chief Cells: hour. General Features.--The chief cell is by far the Attempts were made to perfuso the parathyroids of predominant cellular element in the parathyroid of three animals with the fixative, but there was some the monkey. Only one distinct type, the pale chief doubt as to the success of the perfusions, since, although cell, can be identified in these preparations, the thyroid gland darkened immediately on completion of the pedusion, rapid blackening of the external although Baker (3), it should be noted, has de- parathyroids was not observed. The parathyroids were scribed pale and dark chief cells in this same removed immediately following the perfusion and were species. The appearance of the pale chief cell as then handled in the same manner as described above for observed here confirms, in general, the descrip- tissue prepared by immersion fixation only. Little dif- tion of this cell by Baker (3). Certain cytoplasmic ference was noted in the quality of fixation between the structures can be identified in virtually each chief per[used tissue and the tissue exposed only to immersion cell ~ollowing adequate preparation of the tissue. fixation. Numerous small, rod-shaped and filamentous Following fi afion, the tissue was washed, dehy- mitochondria are seen which, though distributed drated in alcohol, embedded in methacrylate, and diffusely throughout the cytoplasm, have a sectioned in the usual manner on a Servall microtome originally designed by Porter and Blum (49), with glass tendency to be congregated at the vascular pole of knives similar to those described by Latta and Hart- the cell (Fig. 1). A distinctive, compact, relatively mann (28). The sections were examined with an RCA large, dense, deeply basophilic structure, pre- EMU 2C electron microscope equipped with a com- viously described in the parathyroids of man and pensated objective. Either 50 or 100 ~ objective aper- the macaque monkey (45, 11, 3) and designated by tures were used. Original magnifications of the electron Pappenheimer and Wilens as the "juxtanuclear micrographs ranged from 1500 to 7500 diameters, as body," is present in each chief cell. Several pro- calibrated with polystyrene latex (2, 19). Further files of juxtanuclear body material are frequently magnification was achieved photographically. present in a single chief cell (Figs. 2 to 4). The parathyroids used for study with the light When tissue sections of macaque parathyroid are microscope were fixed immediately after extirpation in either Bouin's or Helly's solution. The glands were subjected to hydrolysis with a ribonuclease solu- sectioned at 4/~ and a variety of staining techniques tion and subsequently stained with basic stains as were employed, including the Altmann-Kull method described above, the juxtanuclear bodies still stain for mitochondria (9), the periodic acid Schiff technique lightly and can be identified, but the basophilia is (23), toluidine blue, hematoxylin and eosin, and others. In addition, mounted sections from 2 parathyroids 1 The ribonuclease enzyme preparation was obtained were subjected to hydrolysis by a 0.15 per cent solution from General Biochemicals, Inc., Chagrin Fails, Ohio. JERRY STEVEN TRIER 15 strikingly less intense when compared with those in length. The submicroscopic structure of the mito- control sections which have not been treated with chondria present in parathyroid chief cells is consistent ribonuclease solution (compare Fig. 4 with Fig. 5). with Palade's description of mitochondrial structure in The background basophilia of the cytoplasm is other mammalian tissues (36, 37). reduced only slightly following hydrolysis with Endoplasmic Ret~dum.--The endoplasmic reticulum as seen in a variety of cells has been well described by ribonuclease. Porter (47, 48), Palade and Porter (41) and Palade (38, In many of the chief cells one can see discrete 39). Its presence in the chief cells of the rat parathyroid small granules which stain brightly with the has already been noted by Lever (30). It has also been periodic acid Schiff technique (23). These granules found to be a component of the cytoplasm of the chief are scattered throughout the cytoplasm, often in cells of the macaque (Figs. 6 to 8), where it is disposed close relation to the juxtanuclear bodies (Fig. 3). both diffusely and in well organized masses of oriented They are here designated the PAS-positive lamellae resembling some of the Nissl bodies described granules. in nerve ceils by Palay and Palade (42). The dark chief cell described by Baker (3) could The distribution and size of the masses of not be identified in this study with either the light oriented lamellae as seen with the electron micro- or electron microscope.