<<

Arch. histol. jap., Vol. 33, No. 4 (1971) p. 283-299

Department of Anatomy (Prof. H. OUTI), Okayama University Medical School, Okayama, Japan

The Occurrence and Distribution of the Parafollicular Cells in the , Parathyroid IV and Thymus IV in Some Mammals

Yoko KAMEDA

Received August 6, 1971

Summary. The thyroid glands of eight rabbits, fifteen cats and eight mice of various ages and both sexes were made into serial sections, one lobe from each individual, and investigated by means of silver impregnation, pseudoisocyanin and lead-hematoxylin stainings. It was recognized that the parafollicular cells stained by these techniques were not restricted to the thyroid gland but were also distributed in the parathyroid IV and thymus IV. 1. In rabbits the parafollicular cells occurred in the parathyroid IV in six out of seven cases. Although the proportion of parafollicular cells to parathyroid cells differed from individual to individual, it reached 10% in the most numerous case. 2. In cats the parafollicular cells constantly occurred in the parathyroid IV. They were found also in the thymus IV of nine out of eleven cases. From forty to fifty para- follicular cells were generally counted in cat parathyroid IV. In two cases with numer- ous parafollicular cells, they were estimated as 1-3% of the parathyroid cells. In the thymus tissue their population was lower than in the . 3. No parafollicular cells were found in the parathyroid III and the thymus III. 4. The distribution of parafollicular cells in the thyroid of rabbits and mice was confined in a more or less restricted region of the gland around the parathyroid IV and thymus IV, or around ciliated cysts (vide infra). 5. In all three species a few ciliated cysts containing a foamy colloid-like substance constantly occurred in the thyroid grand. 6. These observations were discussed in relation to the ultimobranchial origin of the parafollicular cells. Experimental and immunohistochemical studies have supported that the para- follicular cells are the source of (MATSUZAWA, 1966; BUSSOLATI and PEARSE, 1967; ERICSON, 1968; KAMEDA, 1970). The existence of the parafollicular cells in the thyroid gland has been established in a variety of mammalian species since the dis- covery of the cells by BABER(1876) in the dog thyroid. The possibility that the para- follicular cells might occur also in other branchiogenic organs such as the parathyroid gland and thymus, however, seems to deserve systematic studies as the source organs of the hormone calcitonin have been much disputed (see Discussion). Some authors (DUBOISand DUMONT, 1966; WELSCH and PEARSE, 1969; KAMEDA,1971) noticed the occurrence of the parafollicular cells in the parathyroid gland, but our knowledge concerning this is only fragmental. The thymus has generally been thought free of parafollicular cells except for the report of the present author showing their occur- rence in the dog thymus (KAMEDA,1971). It should be further pointed out that even in the thyroid gland itself little has been investigated in detail on the distribution of the parafollicular cells. 283 284 Y. KAMEDA:

In the present study, the thyroid gland, parathyroid gland and thymus of cats, rabbits and mice were prepared in serial sections, and the occurrence and distribu- tion of the parafollicular cells in these organs were systematically investigated by light microscopy. Materials and Methods In the present study, 15 cats weighing from 0.5 to 3.7Kg (3 adults and 12 young animals from 1 to 7 months old), 8 rabbits from 0.5 to 3.5Kg (2 adults, 4 puberty animals and 2 juvenile animals) and 8 adult mice (R3) of both sexes were used. The thyroid glands were removed under pentobarbital anesthesia and fixed in GPA solu- tion (25% glutaraldehyde, 1 vol., saturated aqueous solution of picric acid, 3 vol. and acetic acid to give 1%, SOLCIAet al., 1968). One thyroid lobe from each animal was cut in longitudinal total serial sections 10μ thick and the other lobe was transversely (not serially) cut at 5-6μ. Besides the hematoxylin-eosin staining for general purposes, the silver impregnation (KAMEDA, 1968), pseudoisocyanin (SOLCIA et al., 1968) and lead-hematoxylin (SOLCIA et al., 1969) stainings were employed for the specific demonstration of the parafollicular cells. A female lion six years old was kindly provided by the Ritsurin Zoo, Takamatsu, and the thyroid and parathyroid glands were examined though not in serial sections.

Results Thyroid parafollicular cells In hematoxylin-eosin staining, the parafollicular cells of rabbits, cats and mice may be distinguished from the follicular cells only by their relatively large and

Fig. 1. Parafollicular cells in the rabbit thyroid gland stained dark by lead-hematoxylin. The cells partly surround the follicles. Fixed in GPA. ×1,100 Parafollicular Cells in Parathyroid and Thymus 285 chromatin sparse nuclei and by the more or less weak stainability of the cytoplasm. By means of silver impregnation, pseudoisocyanin and lead-hematoxylin stainings,

Fig. 2. Parafollicular cells in the cat thyroid stained dark by lead-hematoxylin. The cells are grouped in the parafollicular position. Fixed in GPA. ×600 Fig. 3. Parafollicular cells in the cat thyroid stained by pseudoisocyanin. The granules of the cells and the content of the ciliated cyst shown in the upper left of the picture react metachromatically. Fixed in GPA. ×1,100 286 Y. KAMEDA:

however, the parafollicular cells of these animals are clearly demonstrated as cells containing numerous stained granules (Fig. 1-3, 12) The parafollicular cells of the rabbit were located either in the perifollicular position as a surrounding element of the follicles, or in parafollicular position in small cell groups (Fig. 1). The shape of rabbit parafollicular cells varied from oval to slender. There seemed to be an individual difference in the population of these forms: in six animals slender parafollicular cells exceeded oval ones in number, where- as in two cases oval parafollicular cells were more numerous. Those cells located in perifollicular positions, however, usually showed elongated forms. On the other hand, the shape of the parafollicular cells seemed unrelated to the age and sex. The cells measured 20-25μ in long diameter and rarely reached 30μ with elongated cyto- plasmic processes. Their nuclei were round and measured about 6.5μ in diameter. The parafollicular cells of the cat were found in parafollicular position and were mostly grouped in cell clusters (Fig. 2, 3). Although the boundary between the para- follicular cells was not very clear because of abundant stained granules, oval or round cells measuring about 13×9μ predominated. They contained a round nucleus of 6.5-7μ diameter. The parafollicular cell groups of the cat showed an oval or round outline and generally measured 20-30μ in long diameter, sometimes reaching 50μ. The parafollicular cells of the mouse were characterized by their solitary occur- rence in perifollicular position or between the follicular cells (Fig. 12). The cell and nucleus were oval or round and measured around 13×9μ and 6.5μ, respectively.

The distribution of the parafollicular cells within the thyroid gland In rabbits, mice and cats, the parafollicular cells were not evenly distributed in the thyroid gland. Certain parts of the thyroid parenchyme did not contain them at all, while they were conspicuously concentrated around the parathyroid IV and thymus IV (vide infra). Their distribution in the thyroid of a rabbit is diagrammatically shown in Figure 13. In seven of eight rabbits the distribution of the cells was limited to the middle of the thyroid gland covering one third to one half of it, which also included the para- thyroid IV. In the remaining one case in which the parathyroid IV was not situated in or beside the thyroid lobe, the parafollicular cells were more diffusely distributed in the thyroid parenchyme. The parafollicular cells of cats were more widely distributed within the thyroid lobes than in rabbits. The parathyroid IV and thymus IV usually were in the upper part of the thyroid lobes and the parafollicular cells were mostly restricted to the upper two thirds of the thyroid, although in three cases they were scattered through- out the gland. The parathyroid III of cats was usually located lower than the para- thyroid IV in the thyroid. In all eight mice the distribution of the parafollicular cells was limited to the middle one third of the thyroid parenchyme along the long axis of the organ and around the ciliated cyst which generally occupied the central region of the thyroid lobes (Fig. 12, 13). The distribution of the cells in one case is diagrammatically shown in Figure 13. Fig. 4. Parathyroid IV (internal parathyroid gland) in the rabbit thyroid stained by lead-hematoxylin. Note the numerous stained cells distributed among the parathyroid cells. The same cells also are shown in the cyst epithelium. Fixed in GPA. C cyst. ×150 Parafollicular Cells in Parathyroid and Thymus 287

Fig. 5. Higher magnification of the parathyroid IV in a neighbouring section of Figure 4. Oval or fusiform cells are stained dark by lead-hematoxylin. The round small profiles correspond to the cytoplasmic processes crossed in the section. ×600

Fig. 6. A neighbouring section to that of Figures 4 and 5 stained by silver impregnation. The cells corresponding to the lead-hematoxylin positive cells are filled with the argyrophil granules and provided with the elongated cytoplasmic processes. ×1,100 288 Y. KAMEDA:

The parafollicular cells in the parathyroid IV Cells selectively stained by silver impregnation, pseudoisocyanin and lead- hematoxylin were found in the parathyroid IV (internal parathyroid gland) of rabbits and cats (Fig 4-8). In the mouse the parathyroid IV was not present as has been confirmed by previous authors (See, BARGMANN, 1939). In rabbits, the parathyroid IV was not always included within the thyroid gland. It was detected in seven out of eight thyroid lobes cut in serial sections. The parafol- licular cells were found in six out of these seven parathyroids. They were oval or elongated cells containing a round nucleus and distributed among the parathyroid cells solitarily or in small groups (Fig. 4-6). Their size was the same as that of the thyroid parafollicular cells. With hematoxylin-eosin staining it was impossible to distinguish them from the parathyroid cells, because of the similar staining chara- cteristics and cell size. In two cases the parathyroid gland contained numerous parafollicular cells and a rough count reached 10% of the parathyroid cells, while in the other four parathyroids only several to fifty cells were found in the whole organ. Age difference in the population of the stained cells was not clear, because of the large individual differences. Although they were usually concentrated in the peri- phery of the parathyroid, a diffuse distribution was observed in the cases of their numerous occurrence. In cat parathyroid IV, the elements stained by silver impregnation, pseudo- isocyanin and lead-hematoxylin were round or oval cells with a round nucleus, and they were distributed among the parenchymal cells of the organ, forming small cell groups (Fig. 7, 8). Their size corresponded to that of the thyroid parafollicular cells. In hematoxylin-eosin staining, they were characterized by their more reddish cyto- plasm than found in the clear parathyroid cells, but a clear discrimination could not be made between them. The cell groups occurred rather diffusely in the parathyroid gland, though they tended to gather along larger blood vessels supplying parathyroid parenchyme. In all the fifteen cats examined, the parathyroid IV contained para- follicular cells (Table 1). The proportion of these cells to the parathyroid cells was low and only forty to fifty cells were counted in an entire gland. In two specimens containing relatively numerous stained cells, their ratio was roughly counted 1-3%. Although no clearcut result of age difference in population was obtained owing to individual differences, two cats with relatively numerous stained cells were both 6 months old.

The parathyroid III In four out of eight rabbits, the parathyroid III occurred adjacent to the thyroid lobes. The occurrence of the parathyroid III in or beside cat is indicated in Table 1. In mice, the parathyroid III was encountered in the caudal portion of five thyroid lobes. No stained cells were found in the parathyroid III in any species examined.

The parafollicular cells in the thymus IV The thymus IV of rabbits was found in none of the thyroid lobes cut in serial sections. Parafollicular Cells in Parathyroid and Thymus 289

In eleven out of fifteen thyroid lobes of cats, a thymus gland was recognized in connection with the parathyroid IV. Since it has been described that in the cat the

Fig. 7. Parathyroid IV of the cat stained by lead-hematoxylin. Note the darkely stained cell groups corresponding to the parafollicular cells. Fixed in GPA. T thymus, C cyst. ×150

Fig. 8. Parafollicular cell groups in the parathyroid IV of the cat stained by pseudoiso- cyanin, Fixed in GPA.×1,100 290 Y. KAMEDA:

Table 1. Relationship between the parafollicular cells and the parathyroid gland and thymus in the cat

+: Occurrence -: Non-occurrence Pfc: Parafollicular cells PT: Parathyroid gland

Fig. 9. Thymus IV of the cat stained by lead-hematoxylin. Darkly stained cells are shown among the thymic cells. Fixed in GPA. ×600 Parafollicular Cells in Parathyroid and Thymus 291

thymus IV develops from the pharyngeal pouch IV and becomes intimately connected with the parathyroid IV to enter into the thyroid gland together with it (see, BARGMANN, 1939), the thymus gland found adjacent to the parathyroid IV was con- sidered as the thymus IV. Cells stained by silver impregnation, pseudoisocyanin and lead-hematoxylin were found in nine of the eleven cat thymuses IV examined (Fig. 9, 10). The cells were round or oval with a round nucleus and corresponded to the thyroid parafollicular cells in size. They were diffusely distributed in medullary portions and rarely in the cortex of the thymic lobules, forming small cell groups. They could not be identified by hematoxylin-eosin. A few cysts which contained a colloid-like substance and cell debris and were covered with stratified epithelium sometimes occurred in the medullary portion of the thymus. The stained cells were often intercalated between the epithelial cells of the cysts or in contact with the basal side of the cyst epithelium. The population of these cells in the thymic parenchyme was lower than in the parathyroid. In the present study the thymus IV consisted of one to four lobules. The stained cells were distributed in two lobules in two out of the nine thymus glands, while they were restricted to one lobule in the other seven cases. In two mice a thymus gland occurred beside the ciliated cysts (vide infra) but no stained cells were found in them.

The thymus III In two rabbits and in five cats, the thymus III was found beside the parathyroid III (Table 1). No cell stained by silver impregnation, pseudoisocyanin and lead- hematoxylin was found in the thymus III of rabbits and cats.

The parafollicular cell complex found in cats Large parafollicular cell complexes, similar to those found in dogs (KAMEDA,1971), were found in three out of fifteen cats (Table 1). They consisted of numerous cells with granules stained by lead-hematoxylin, pseudoisocyanin and silver impregnation, another type of epithelial cell unstained by these staining methods, microfollicles with or without colloid droplets which are similar to the thyroid follicles, and small cysts lined by a simple or stratified epithelium. The proportions of these elements differed from complex to complex. In cat No. 12 a parafollicular cell complex occurred in the parathyroid IV (Fig. 10) and measured 220×180×120μin size. It contained a number of microfollicles in spite of the absence of connection with the thyroid parenchyme. In cat No. 14 there were found in the interlobular space of the thymus IV two large parafollicular cell complexes in which unstained and apparently immature epithelial cells were numer- ous (Fig.11). They measured 1300×220×700μ and 270×50×300μ in size, respec- tively. In animal No.4 a cell complex measuring 490×220×420μ in size was found beside the parathyroid IV-thymus IV complex. A portion of this complex was con- nected with the thyroid parenchyme. In rabbits and mice, no parafollicular cell complex was found.

The cysts in the thyroid, parathyroid and thymus Ciliated cysts were encountered in all the thyroid glands of rabbits, cats and mice 292 Y. KAMEDA:

Fig. 10. A special parafollicular cell complex consisting of numerous parafollicular cells and microfollicles found in the parathyroid IV of the cat. Note the darkly stained parafollicular cells distributed in the parathyroid, thyroid and thymus tissue. Fixed in GPA and stained by lead-hematoxylin. T thymus IV, C cyst, PT parathyroid IV, Th thyroid. ×150

Fig. 11. A special parafollicular cell complex found among the thymic lobules of the cat. It consists of darkly stained parafollicular cells and unstained epithelial cells. Fixation in GPA and staining in lead-hematoxylin. ×150 Parafollicular Cells in Parathyroid and Thymus 293 cut in serial sections. In the thyroid parenchyme of seven rabbits a few cysts were revealed around the parathyroid IV. Also in one case in which the thyroid lobe did not contain the parathyroid IV cysts were found in the thyroid. As shown in Figure 4, the cysts of rabbits were lined by a mixed single and stratified epithelium mingled with some ciliated cells. In four of these eight cases the pseudoisocyanin and lead-hematoxylin positive and silver-impregnated cells were encountered among the epithelial cells of the cysts. The cysts contained a foamy colloid-like substance weakly stained in eosin and sometimes cell debris, too. In all the thyroid lobes of fifteen cats, many ciliated cysts occurred arround the parathyroid IV and thymus IV (Table 1). In three cases a few cysts related neither to the parathyroid IV nor to the thymus IV were also recognized in the thyroid lobes. They were lined by a single cuboidal or squamous epithelium, partly furnished with cilia (Fig. 3, 7, 10). Rarely the lumen was divided by incomplete septa. The cysts contained a finely foamy granular substance and sometimes cell debris, both of which were sometimes stained by pseudoisocyanin (Fig. 3). Similar cysts were encountered in the parathyroid IV, parathyroid III and thymus IV (Table 1). The cysts found in the thymic lobes, on the other hand, were usually lined by a squamous stratified epithelium and had much cell debris in the lumen. These cysts often were continuous to the cyst covered by a single ciliated epithelium in the thyroid parenchyme. In spite of the absence of the parathyroid IV in the mouse, a few cysts were found in the central region of the thyroid lobes in all of the eight mice. They were lined

Fig. 12. Parafollicular cells of the mouse thyroid gland distributing around the ciliated cysts and thymus, T thymus, CE ciliated epithelium. ×375 294 Y. KAMEDA: by single cuboidal or squamous epithelial cells and some of the cells possessed cilia (Fig. 12). Stained cells were often located among the cyst epithelial cells. The lumen was filled with a foamy colloid-like substance.

The parafollicular cells in the lion The parafollicular cells in the lion thyroid gland were similar to those of cats in their form, size and filled with quantities of stained granules. They were mostly located in parafollicular position and were grouped in cell clusters. A few parafol- licular cells were also found in the parathyroid IV but the precise population of the cells is unknown as the tissue was not investigated in serial sections.

Discussion The parafollicular cells in the parathyroid IV and thymus IV The cells found in the parathyroid IV (internal parathyroid gland) of rabbits or in the parathyroid IV and thymus IV of cats are believed identical with the parafol- licular cells of the thyroid gland, because firstly they are stained by silver impregna- tion, pseudoisocyanin and lead-hematoxylin known as methods for the positive demonstration of parafollicular cells and secondly, their form, size and the nature of the granules are similar to the thyroid parafollicular cells of the same animals. In the case of the dog which also possesses these cells in the parathyroid IV and thymus IV, the cells have been shown to undergo degranulation and to show an increased mitotic activity after experimentally induced hypercalcemia, just as the thyroid parafollicular cells do (KAMEDA, 1971). It seems now fully evidenced that the thyroid parafollicular cells are responsible for the secretion of the serum calcium lowering hormone, calcitonin (for literature see KAMEDA,1970). At the time calcitonin was originally suggested by COPP et al. (1962), they con- sidered the parathyroid gland as its origin. A confirmatory view soon was published by KUMARet al. (1963). "The perfusion of the parathyroid" with calcium-rich blood which caused a rapid fall in the calcium level of the systemic blood in the studies of those researchers, however, could not distinguish between thyroid and parathyroid glands as the source of calcitonin, because both glands in dogs cannot be perfused separately. Later, HIRSCHet al. insisted that a hypocalcemic element, named anew as thyrocalcitonin by them, was extracted not from the parathyroid but from the thyroid gland in rats (1963) and in many mammalian species (1964). In goats (FOSTER et al., 1964), and pigs (CARE,1965) in which the external parathyroid glands have a blood supply separated from the thyroid gland, it was confirmed that the hypocalcemic substance was secreted not from the parathyroid but from the thyroid gland during hypercalcemic perfusion. Although additional evidence in favor of a parathyroid origin was given by COPP and HENZE(1964) and COPP (1965), it now seems generally accepted that calcitonin and thyrocalcitonin are identical substances (HIRSCHand MUNSON,1969) and that they are secreted from the thyroid gland in mammals. The parathyroid gland as the possible source of this hormone has become more and more ignored by most authors. Neither has attention been paid to the fact that the thymus tissue may occur in or adjacent to the thyroid gland nor to the possibility that the hormone in question may possibly be produced from there. Parafollicular Cells in Parathyroid and Thymus 295

The present study indicates that the parafollicular cells are distributed not only in the thyroid gland but also very frequently in the parathyroid IV of rabbits and cats and in the thymus IV of cats. Their occurrence in the parathyroid IV and thymus IV of dogs has been reported elsewhere (KAMEDA,1971). The author proposes that the origin of calcitonin is not restricted to the thyroid gland, although it is generally the most significant source. Recently, DUBOIS and DUMONT (1966) by electron microscopy and SOLCIA and SAMPIETRO (1968) by light microscopy reported that cells with the same characteristics as the parafollicular cells of the thyroid gland existed in the internal parathyroid gland of the rabbit. CARVALHEIRA and PEARSE (1967) revealed that the thyroid para- follicular cells of the rabbit and dog showed a strong cholinesterase activity and that cells with the same enzyme activity occurred in the internal parathyroid gland. (As far as the photomicrograph by these authors indicates, the internal parathyroid of the dog described by them is not such but probably corresponds to the large parafol- licular cell complex containing microfollicles described in this paper.) By electron microscopy, WELSCH and PEARSE (1969) revealed the cholinesterase-positive cells in the internal parathyroid gland of the rabbit. Their simply qualitative observations on the existence of the parafollicular cells in the internal parathyroid gland of the rabbit are confirmed in the present study by a more quantitative methodology. The cell population and its individual variability is thus first elucidated. The occurrence of the parafollicular cells in the parathyroid IV of the cat has not been reported by previous investigators. It is distinctly indicated in the present study that the parathyroid IV of the cat constantly contains parafollicular cells. The occurrence of parafollicular cells in the thymus tissue has not been demon- strated in any species (except for the dog, KAMEDA,1971). In the cat in which the thymus IV in connection with the parathyroid IV is often encountered in the thyroid glands, the parafollicular cells occur in the thymus parenchyme. The finding by KOHN (1895) that the thymus IV is also found in the thyroid of the rabbit could not be confirmed in this study. It was previously generally accepted that the mammalian ultimobranchial body undergoes degeneration during postnatal life. GODWIN(1937), however, described that the ultimobranchial body of the dog, in the early embryonic development, becomes incorporated within the thyroid and gives origin to parafollicular cells. Recently, this opinion of GODWIN was confirmed in the rat by PEARSE and CARVALHEIRA (1967) using fluorescent amine technique after injection of 5-HTP and L-DOPA, and by ISHIKAWA (1965) and STOECKEL and Porte (1970) by electron microscopy. The distribution of the parafollicular cells in the parathyroid IV and thymus IV which are known to be in an intimate connection with the ultimobranchial body during embryonic development and not in the parathyroid III and thymus III favors the hypothesis that the parafollicular cells derive from the ultimobranchial body. The parafollicular cell complexes found in the cat without doubt correspond to those in the dog previously described by the author (KAMEDA,1971) which also were intimately related to the parathyroid IV and thymus IV. The occurrence, in cats and dogs, of the large parafollicular cell complexes seems to support the view that at least some parts of the ultimobranchial body may remain as cell masses of this type even in postnatal life. A detailed discussion has been made in this author's previous 296 Y. KAMEDA: paper on the nature and significance of the parafollicular cell complex (KAMEDA, 1971). GALANTE et al. (1968) extracted in man a calcitonin-like substance from the parathyroid tissue with hyperparathyroidism and from the thymus tissue, although they did not discriminate between the parathyroid III and IV. Although the exist- ence of the parafollicular cells in man was long disputed, SOLCIA et al. (1970) demon- strated that they occur concentrated in the posterior portions of the lateral thyroid lobes. The cells were not found in the parathyroid IV and thymus.

The distribution of the parafollicular cells in the thyroid In the present study, the parafollicular cells in the thyroid were concentrated around the parathyroid IV and the thymus IV (rabbits and cats) or around the ciliated cysts (mice). In rabbits and mice, the portion of the thyroid tissue containing none of those cells at all was conspicuous. This distinct distribution of the parafollicular elements near the parathyroid IV and thymus IV may eliminate the hypothesis that the parafollicular cells derive from the follicular cells suggested by some authors (SUGIYAMA, 1954; STUX et al., 1961). Similar distribution of the parafollicular cells in the thyroid was also reported by SOLCIA and SAMPIETRO (1968) in rabbits and by KAMEDA (1971) in dogs. In the papers of some other authors (SUGIYAMA, 1954, in guinea pigs; DUMONT, 1956, in rabbits; STUX et al., 1961, in rats) their relation to the parathyroid IV or to the thymus IV seems to have been overlooked.

The cysts in the thyroid, parathyroid and thymus In the present study a few ciliated cysts were constantly found in the thyroid gland of the rabbit, cat and mouse. The author supposed in the previous study (1971) that the ciliated cysts found in the dog thyroid may originated not only from the

Rabbit No. 1 Mouse No. 25

Fig. 13. Diagram indicating the distribution of the parafollicular cells in the thyroid lobes. The parafollicular cells are dotted. PT III parathyroid III, PT IV parathyroid IV, C cyst, T thymus. Parafollicular Cells in Parathyroid and Thymus 297 ultimobranchial body but also from the residual pharyngeal pouch IV and pharyngeal pouch III. This conclusion may applicable to the ciliated cysts of rabbits, cats and mice. The ciliated cysts have been recognized in the thyroid of a large variety of the mammalian species. They should be regarded as a regular constituent of the thyroid on the basis of their constant occurrence in rabbits, cats and mice as shown in the present paper. However, little is known about the function of these cysts. In the dog no changes were found in the frequency of their occurrence, quantity of colloid- like substances and cellular appearence after induced hypercalcemia or injection of thyroid inhibitors (KAMEDA, unpublished data).

Acknowledgment. The author wishes to express her cordial thanks to Prof. Hiromu OUTIof her department, and also to Prof. Tsuneo FUJITA, Department of Anatomy at Niigata University, for their kind advice and critical reading of the manuscript.

二三 の哺乳動物 の甲状腺, 上皮小体IV, 胸腺IVに おけ る旁濾胞細胞の 存在 と分布 について

亀 田 芙 子

ウサ ギ (8匹), ネ コ (15匹) お よびマ ウス (8匹) の 甲状腺 を1個 体 よ り1葉 を と り, 連続切 片に して, 渡銀, プソイ ドイ ソチアニ ンお よび鉛 ヘマ トキシ リンに よる染色 法 に よ って しらべ た. これ らの方法 で染 まる旁濾胞細 胞は 甲状 腺だ けに限 らず, 上皮 小 体IVと 胸 腺IVに も分布す ることが明 らか にな った. 1. ウサ ギで 旁濾胞細胞 は7例 中6例 の上皮小体IVに 存 在 した. 上皮小体 内の旁濾 胞細胞 の数 は個体差が著 しいが, 最 も多 い例 では全 上皮細胞 の10%に 達 した. 2. ネ コでは 上皮小 体IVの 中に 旁濾胞細 胞は常 に存在 した. それ らは11例 中9例 の 胸腺IVの 中に も見 いだされた. 一般に ネ コの上皮小 体IVに は40~50個 の旁濾胞 細胞が 数 え られたが, 細胞数 の多い2例 では1~3%の 割合 であ った. 胸腺IVに おけ る旁濾胞 細胞 の数は 上皮小 体IVに おけ るよ り少なか った. 3. 上 皮小体IIIと胸 腺IIIには 旁濾胞細胞 はみ とめ られなか った. 4. ウサ ギ とマ ウスの 甲状腺 内の旁濾 胞細 胞 の分布 は 上皮小体IVと 胸 腺IV, あるいは 繊毛 を もつ嚢胞 の周 囲の領域に局在 していた. 5. これ ら3種 の動 物の全 例 の甲状腺 内に, 泡状 の コロイ ド様物質 を含 み繊毛 をもつ 嚢胞 が常に存在 した. 6. これ らの観察 か ら旁濾 胞細胞 の鰓 後体 起源が考察 され た. 298 Y. KAMEDA:

References Baber, E. C.: Contributions to the minute anatomy of the thyroid gland of the dog (abstract). Proc. Roy. Soc. 24: 240-241 (1876). Bargmann, W.: Die Epithelkorperchen. In: Mollendorff's Handbuch der mikroskopischen Anatomie des Menschen. VI/2, Berlin, Springer Verlag, 1939. (p. 137-196). Bussolati, G. and A. G. E. Pearse: Immunofluorescent localization of calcitonin in the ‘C’ cells of pig and dog thyroid. J. Endocrinol. 37: 205-209 (1967). Care, A. D.: Secretion of thyrocalcitonin. Nature 205: 1289-1291 (1965). Carvalheira, A. F. and A. G. E. Pearse: Comparative cytochemistry of C cell esterases in the mammalian thyroid-parathyroid complex. Histochemie 8: 175-182 (1967). Copp, D. H.: The hormones of the parathyroid and calcium . In: (ed. by) P. J. Gaillard, R. V. Talmage and A. M. Budy: The parathyroid gland. Chicago, University of Chicago Press, 1965. (p. 73-87). Copp, D. H., E. C. Cameron, B. A. Cheney, A. G. F. Davidson and K. G. Henze: Evidence for calcitonin-a new hormone from the parathyroid that lowers blood calcium. 70: 638-649 (1962). Copp, D. H. and K. G. Henze: Parathyroid origin of calcitonin-evidence from perfusion of sheep glands. Endocrinology 75: 49-55 (1964). Dubois, P. et L. Dumont: Aspects ultrastructuraux des cellules parafolliculaires de la thyroide du lapin en fonction de la nature du fixateur. C. r. Soc. Biol. 160: 2331-2334 (1966). Dumont, L.: Les cellules parafolliculaires de la thyroide du lapin leur rapport avec le canal thyreoglosse. Ann. Endocrinol. 17: 700-712 (1956). Ericson, L. E.: Degranulation of the parafollicular cells of the rat thyroid by vitamine D2-induced hypercalcemia. J. Ultrastr. Res. 24: 145-149 (1968). Foster, G. V., A. Baghdiantz, M. A. Kumar, E. Slack, H. A. Soliman and I. MacIntyre: Thyroid origin of calcitonin. Nature 202: 1303-1305 (1964). Galante, L., T. V. Gudmundsson, E. W. Matthews, A. Tse, E. D. Williams, N. J. Y. Woodhouse and I. MacIntyre: Thymic and parathyroid origin of calcitonin in man. Lancet 2: 537-538 (1968). Godwin, M. C.: Complex IV in the dog with special emphasis on the relation of the ultimobranchial body to interfollicular cells in the postnatal thyroid gland. Amer. J. Anat. 60: 299-339 (1937). Hirsch, P. F., G. F. Gauthier and P. L. Munson: Thyroid hypocalcemic principle and recurrent laryngeal nerve injury as factors affecting the response to parathyroidectomy in rats. Endo- crinology 73: 244-252 (1963). Hirsch, P. F., and P. L. Munson: Thyrocalcitonin. Physiol. Rev. 49: 548-622 (1969). Hirsch, P. F., E. F. Voelkel, A. Savery and P. L. Munson: Partial purification of thyrocalcitonin (abstract). Fed. Proc. 23: 204 (1964). Ishikawa, K.: Electron microscopical studies of the ultimobranchial body of the rat in embryonic life, with special emphasis on its fate-the relation to the thyroid tissue and parafollicular cells. Fol. anat. jap. 41: 313-335 (1965). Kameda, Y.: Parafollicular cells of the thyroid as studied with Davenport's silver impregnation. Arch. histol. jap. 30: 83-94 (1968). -: Increased mitotic activity of the parafollicular cells of the dog thyroid in experimentally induced hypercalcemia. Arch. histol. jap. 32: 179-192 (1970). -: The occurrence of a special parafollicular cell complex in and beside the dog thyroid gland. Arch. histol. jap. 33: 115-132 (1971). Kohn, A.: Cited from W. Bargmann: Der Thymus. In: Mollendorff's Handbuch der mikrosko- pischen Anatomie des Menschen. VI/4. Berlin, Springer Verlag, 1943. (p. 1-172). Kumar, M. A., G. V. Foster and I. MacIntyre: Further evidence for calcitonin. A rapid-acting hormone which lowers plasma-calcium. Lancet 2: 480-482 (1963). Matsuzawa, T.: Experimental morphological studies on the parafollicular cells of the rat thyroid Parafollicular Cells in Parathyroid and Thymus 299

with special reference to the source of thyrocalcitonin. Arch. histol. jap. 27: 521-544 (1966). Pearse, A. G. E. and A. F. Carvalheira: Cytochemical evidence for an ultimobranchial origin of rodent thyroid C cells Nature 214: 929-930 (1967). Solcia, E., C. Capella, R. Sampietro and G. Vassallo: The distribution of human C cells and their relationship to osteopetrosis and medullary carcinoma of the thyroid. In: (ed. by) S. Taylor: Calcitonin. 1969 Proceedings of the second international symposium. London, Heinemann, 1970. (p. 220-226). Solcia, E., C. Capella and G. Vassallo: Lead-haematoxylin as a stain for endocrine cells. Histo- chemie 20: 116-126 (1969). Solcia, E. and R. Sampietro: New methods for staining secretory granules and 5-hydroxytrypt- amine in the thyroid C cells. In: (ed. by) S. Taylor: Calcitonin. Proceedings of the symposium on thyrocalcitonin and the C cells. London, Heinemann, 1968. (p. 127-132). Solcia, E., G. Vassallo and C. Capella: Selective staining of endocrine cells by basic dyes after acid hydrolysis. Stain Technol. 43: 257-263 (1968). Stoeckel, M. E. et A. Porte: Origine embryonnaire et differenciation secretoire des cellules a calcitonine (cellules C) dans la thyroide foetale du rat. Z. Zellforsch. 106: 251-268 (1970). Stux, M., B. Thompson, H. Isler and C. P. Leblond: The “light cells” of the thyroid gland in the rat. Endocrinology 68: 292-308 (1961). Sugiyama, S.: Studyies of the histogenesis of the thyroid gland of the guinea pig. Anat. Rec. 120: 363-377 (1954). Welsch, U. and A. G. E. Pearse: Electron cytochemistry of BuchE and AchE in thyroid and para- thyroid C cells, under normal and experimental conditions. Histochemie 17: 1-10 (1969).

亀 田 芙 子 Miss Yoko KAMEDA 〒700岡 山市鹿田町 Department of Anatomy 岡山大学医学部 Okayama University Medical School 第二解剖学教室 700 Okayama, Japan