formed cells differentiate into goblet cells during this migration. This Florey [1956] show that these cells are included in the turnover.
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1 OBSERVATIONS ON THE SECRETORY CYCLE OF GOBLET CELLS. By D. J. C. SHEARMAN and A. R. MUIR. From the Department of Anatomy, University of Edinburgh. (Received for publication 18t April 1960) Goblet cells, from the large intestine of rats, have been studied by light and electron microscopy. The supranuclear area contains parallel lamelle of endoplasmic reticulum, whose intralamellar spaces are continuous with the mucous globules of the goblet. Continuity is shown between the globules, which communicate with the cavity of the crypt at the luminal surface of the cell. The observations suggest that mucus synthesis occurs in the supranuclear region and that the mucus is passed through the goblet before discharge. EPITHELIAL cells, which are modified for mucus secretion, often have their superficial parts expanded so that each cell resembles a goblet. In the colon these goblet cells, together with the principal cells, form the epithelium lining the intestinal crypts. Mitoses occur only near the base of the intestinal crypt, which suggests that the intestinal epithelium regenerates from here, and that the newly formed cells migrate towards, and are shed into, the lumen [Moe, 1955]. Bizzozero, cited by Moe [1955], suggests that some of the newly formed cells differentiate into goblet cells during this migration. This suggestion is based on the observation that the early stages of goblet formation are encountered in the mitotic area of the crypt, while mature cells are characteristic of the neck of the crypt, and cells on the surface of the colon have discharged their secretion. These early morphological studies are now supported by autoradiography, particularly with thymidine 14C [Walker and Leblond, 1958] and thymidine 3H [Leblond and Messier, 1959], which are incorporated into newly synthesized nucleic acids, retained during mitosis, and detected in the daughter cells. The use of these substances in the rodent, shows that the intestinal epithelium is completely renewed in periods ranging from 24 hr. in the duodenum to 72 hr. in the colon. Renewal times are also calculated by counting the percentage of cells in mitosis at a given time, and by estimating the duration of the mitotic cycle [Leblond and Stevens, 1948; Knowlton and Widner, 1950]. By autoradiography with 35S, which is incorporated into mucopolysaccharides of the goblet cells, Dziewiatkowski [1956] and Jennings and Florey [1956] show that these cells are included in the turnover. These results show that in a crypt, at any given time, it is possible to observe goblet cells at all stages of their secretory cycle. The electron microscopic structure of the goblet cells in the trachea is described by Rhodin and Dalhamn [1956]. In a review of the morphology of secretion, Palay [1958] refers to the goblet cell as an example of apocrine secretion. The arrangement of the intracellular membranes in the secreting goblet cell are reported in the present paper. VOL. xi^v, NO
2 338 Shearman and Muir MATERIAL AND METHODS Light Microscopy.-Adult rat colon was used; acetic-formol-alcohol was found to be the best fixative for the mucous containing cells, which were stained with the periodic-acid-schiff method [Hotchkiss, 1948]. The Schiff reagent was prepared as described by Barger and Delamater [1948]. The thionine-sulphur dioxide stain [Duijn, 1956] was used to demonstrate the nuclear chromatin and PAS-positive material. Electron Microscopy.-Portions of colon were rapidly removed from adult rats anaesthetized with chloroform; the tissue was cut into blocks, 1 mm. cubes, and fixed at 00 C. in 1 per cent potassium permanganate in 0 9 per cent sodium chloride -for 2 hr. After dehydration in alcohol, these blocks were embedded in Araldite [Glauert and Glauert, 1958]. Other blocks were fixed in 1 per cent osmium tetroxide -buffered with veronal-acetate to a ph 7-2 [Palade, 1952], and these were embedded in an 8: 1 mixture of butyl and methyl methacrylate. Sections, cut with a glass knife on a Servall microtome, were mounted on grids covered with carbon-collodion membranes. Sections about 1,u thick were mounted on glass slides and examined in the phase contrast microscope. The electron microscope was a Metropolitan- Vickers E.M. 6, which was operated at 40 Kv with a 50,u objective aperture. RESULTS Goblet cells are identified in the light microscope by their content of PAS-positive mucin, regardless of the shape of the cell. In the base of the crypt the cells are wedge-shaped (P1. I, fig. 1), and the mucus extends from the nucleus to the lumen (P1. I, fig. 3). While nearer the cavity of the gut the cells acquire a typical goblet shape and maintain this form to the mouth of the crypt. The lumen of the crypt contains a strand of PAS-positive material along its whole length. The epithelium which borders the lumen of the colon does not contain PAS-positive material (P1. I, fig. 2), and similar cells lining the crypt lumen may be regarded as principal cells. In electron micrographs of permanganate and osmium fixed material (P1. I, fig. 4; P1. II, fig. 5), the goblet cells can be recognized by their content of numerous, pale mucous globules, about 1-2 [t in diameter. With osmium fixation, the cytoplasm of the goblet cell is dense and is easily distinguished from the paler cytoplasm of the principal cells (P1. II, fig. 5; P1. III, fig. 6), This difference in density is not apparent after permanganate fixation (P1. I, fig. 4). The shape of the mature mucus-containing cell is that of a goblet, so that the part of the principal cells projecting between goblets consist of constricted strands of cytoplasm extending to the lumen (P1. II, fig. 5). But near the basement membrane, which separates the epithelium from the underlying connective tissue, the principal cells are not constricted, and the nuclei of all the cells lining the crypt are fairly evenly spaced. In the body of the goblet, the pale mucous globules are surrounded by membranes, and the interstices between globules are filled with dense cytoplasm similar to the cytoplasm of the rest of the cell. The considerable variation in size of these almost spherical globules could be due to sectioning, and there does not
3 Goblet Cells appear to be a significant increase in size as the luminal surface of the cell is approached. A striking feature of these globules is that they are continuous with one another. Most of the globules show this continuity with one or more of its neighbours, so that it is possible to trace various continuous pathways of mucus through the goblet from base to luminal surface. The endoplasmic reticulum, characteristically found in the basal part of the cell, is arranged in parallel lamella,. Of these membranes forming lamellse, those nearest the goblet are smooth and contain a clear material (E, P1. II, fig. 5), but they merge with membranes containing denser material and having a rough surface due to the presence of granules (EE, P1. II, fig. 5; P1. IV, fig. 8). Examination of the basal region of the goblet at a higher power shows that the mucous globules are in direct continuity with the clear material in the spaces between the parallel lamellke (P1. III, fig. 6; P1. IV, fig. 8). This description of mucous globules and endoplasmic reticulum is based on the examination of osmium-fixed material. After permanganate-fixation, the cytoplasmic matrix is less dense and non-granular, but the internal cytomembranes are clearly shown (P1. III, fig. 7). The size, shape and continuity of the mucous globules is the same as after osmium fixation, and there are similar groups of parallel lamellae (P1. III, figs. 6 and 7). The surface of the principal cell bordering the crypts of the large intestine has closely packed, regularly arranged microvilli (P1. IV, fig. 10). Goblet cells possess a few similar microvilli, though they are shorter and are distributed irregularly (P1. IV, fig. 9). In the central part of the internal surface of the goblet cell, the mucous globules are separated from the lumen of the crypt by a thin film of cytoplasm, which is perforated, in places, to give continuity between the mucous globules and the lumen (P1. IV, fig. 9). The lumen of the crypt contains an amorphous material (MM, P1. IV, fig. 10), with a similar density to that of the mucus in the globules, and also blocks of mucous globules (M) identical in appearance to those within the goblet cells, and retaining their separating membranes. DiscUSSION 339 In electron micrographs, it is only possible to study static pictures of a dynamic process such as secretion, and all observations are dependent on the preservation, by fixation, of an undistorted picture of the living cell. In the present study, two methods of fixation have been employed and although they produce different images of many components in the cell, the arrangement of internal cytomembranes is strikingly similar and may justify the following interpretations. At the basal part of the cell, the endoplasmic reticulum is of the ergastoplasmic type with ribonucleoprotein granules [Palade, 1955]. The formation of a substance within these lamellar cavities produces the clear parallel sacs seen at the base of the goblet. This material contained in the sacs has a density similar to that of mucus, and, in places, the lumen of a sac is continuous VOL. XLV, NO. 4., *
4 340 Shearman and Muir with a fully formed mucous globule. This is akin to the continuity between the globules in the body of the goblet, which could likewise be produced by the accumulation of mucus within a series of parallel lamellke. However, apart from the limited area at the base of the cell in which the globules are all small and presumably increasing in size, the size of the globules appears to remain constant throughout the whole of the goblet. This suggests that the greater part of the goblet is an area of storage; synthesis of mucus in this part of the cell is unlikely as relatively little cytoplasm surrounds the globules. In the small intestinal goblet cell, Palay [1958] describes proliferation of ergastoplasm and agranular membranes at the onset of secretion. Later, the agranular membranes are arranged as parallel lamellke and small vesicles, to form a compact Golgi complex which is capped by ergastoplasmic cisternae. Palay considers that the vesicles of the Golgi complex pass between the ergastoplasmic cavities, to coalesce and form mucous globules in the goblet. The secretion product of the goblet cell is known to contain a PAS-positive material, mucopolysaceharide [Hotchkiss, 1948], but the amount of protein associated with this is uncertain. Nevertheless, the features of the goblet cell are very similar to those illustrated for the protein-secreting exocrine cells of the pancreas [Palade, 1956; Siekevitz and Palade, 1958 a, b and c]. These authors have related the chemical analysis of cell fractions to the cytological structure at various phases of the secretory cycle in the pancreatic cell. At first, the cytoplasm is dense with ribonucleoprotein granules, associated with membranes of the endoplasmic reticulum, later the reticulum consists of smooth membranes surrounding zymogen granules, which are finally seen to open into the lumen of the acinus. In the goblet cell the present observations suggest that all these phases of the secretory cycle are present in a single cell at one time. This interpretation of the structure of the goblet cell, having a limited area of mucus synthesis and a large goblet concerned with storage and transport to the lumen, is strongly supported by the autoradiographic studies on mucopolysaccharide synthesis in goblet cells of the mouse colon [Jennings and Florey, 1956]. Three hours after the administration of 35S radioactivity was present only at the base of the goblet, during the subsequent 12 hours this was present principally in the middle and luminal parts of the goblet, and all PLATE I Fio. 1. Light Micrograph: Longitudinal section of a crypt. The goblet cells at the base of the crypt contain only a small amount of mucus, whereas those near to the cavity of the gut have acquired the typical goblet shape. Stained P.A.S.: x 300. FIG. 2. Light Micrograph: Longitudinal section of the internal ends of two crypts. The epithelium of the crypts contains many goblet cells. There are no goblet cells in the epithelium which borders the cavity of the gut. Stained P.A.S.: x 450. FIG. 3. Light Micrograph: Transverse section of the bases of two crypts. The goblet cells are distinguished by their wedge-shaped area of mucus. Stained thionin-so2 reagent: x 600. FIG. 4. Electron Micrograph: The lumen of a crypt (L) is surrounded by principal cells (P) and goblet cells containing mucus (M). A few, short microvilli project from the luminal surface of the goblet and principal cells. Permanganate fixation: x 4,500.
5 as - PLATEI I [To face payc/( 340
6 PLATE II FIG. 5. A goblet cell, with (lark cytoplasm lies obliquiely across the field, surrounded by the paler cytoplasm of principal cells (P). The ntcleuis of the goblet cell is not seen, but the nuclei of two principal cells are present at the lower edge. The sturface of the goblet cell, which borders the lulmen (L), carries a few microvilli. In the basal part of the goblet cell, the endoplasmic reticulum (EE) is arranged in parallel lamelle, and at (E) its cavity contains a clear material. The goblet consists of large numbers of mtucouis globules which are in continuiity with one another (dotted line). Osmium fixation: x 9,800.
7 0Asw-ia.r*>+eX,%P. Il 4 N*V 4 a.7. Am- Av at.4-; A%... I 4.'.! I3 *. > t -a w #} + <S. I 'IV 0.. fi C-W4.r.t Ifti. I 3 - I: e 't % 4 :, >' t'i -' s: ~ o' -> 4 - A W..- ll I A ' 4 V s - 1-i < 6,% a o - A i4k{to2i tf <3tw03;S - 0,,i, "..s,r,,. *.''' -',j:a,*, wx ^, - js >>As'^* y. ;xr X -r I', -E IV,s 'lp p a :1Z PLATE II W-+
8 PLATE III FIG. 6. The field shows the basal part of a goblet cell, with principal cell cytoplasmn at the lower right (P). Mucous globhules (M) anad lamellar endoplaslnic reticulum (E) are seen. The arrows show continuity between the muicouis globtules and the cavities of the endoplasmic reticuilum. Osmituml- fixation: x 24,800. FIG. 7. In this section of the basal part of a goblet cell, mucouis globuiles are in contintlity with one another (dotted line) an(l the endoplasmic retictlutm (E) is present in the saine formn as after osiniuimn fixation. Permanganate fixation: x 36,800.
9 PLATE 1l
10 PLATE IA
11 Goblet Cells 341 activity had disappeared after 24 hr. Earlier light microscope studies [Florey, 1955], showed that the probable site of mucus formation is immediately above the nucleus, because of the presence of supranuclear granules. The reformation of mucus after irritant stimuli have caused discharge, is also seen to occur irn the supranuclear area [Florey and Webb, 1931]. As the goblet cell moves towards the lumen of the intestine its content of mucus increases, because the amount synthesized exceeds the discharge of mucus into the lumen of the crypt. In the present study, the crypt lumen is seen to contain both free and membrane-enclosed mucus, the latter appearing to be the result of the discharge of an intact luminal part of a goblet. On reaching the mucosa which borders the intestinal lumen, the goblet cells must discharge all their mucus, as PAS-positive material is not found in the cells on this surface. ACKNOWLEDGMENTS We are grateful to Professor G. J. Romanes who made valuable suggestions during the preparation of this paper. The microscope, which is on permanent loan from the Wellcome Foundation, was maintained by Mr. G. Wilson. The photographs were prepared by Mr. H. Tully and part of the cost of their reproduction was borne by the Carnegie Trust. After this paper had been submitted, we were able to examine some aspects of the same subject in the paper by Florey in this issue. There is much agreement between the two accounts, the main discrepancy being in nomenclature. We consider the smooth, intracellular membranes without associated granules, to be a part of the endoplasmic reticulum, whereas Florey prefers to call these structures the Golgi complex. Sj6strand [1956] discusses the nomenclature of intracellular membranes, and according to his definitions, we consider that both the Golgi complex and the smooth endoplasmic reticulum would be equivalent to y-cytomembranes. PLATE IV FIG. 8.-Mucous globules (M) are present and are continuous with lamellar cavities of the endoplasmic reticulum (E) at the arrow. To the left, the endoplasmic reticulum (EE) contains more dense material and its surface is studded with granules. Osmium fixation: x 20,400. FIG. 9. Part of the luminal surface of a goblet cell shows microvilli (V) projecting into the lumen. The mucous globules are continuous with the mucus in the lumen (dotted line). Osmium fixation: x 19,200. FIG. 10. A longitudinal section of part of a crypt showing microvilli of principal cells (P) forming a brush border around the lulmen. The luminal part of a goblet cell borders the crypt at the upper right of the field. The lumen contains mucus (M) in the same form, as in the intact goblet cell (G), and as a diffuse material (MM). Osmium fixation: x 9,200.
12 342 Shearman and Muir REFERENCES BARGER, J. D. and DELAMATER, E. D. (1948). "The use of Thionyl Chloride in the preparation of Schiff's reagent", Science, 108, DuIJN, P. VAN (1956). "A histochemical specific thionine-so2 reagent, and its use in a bicolor method for deoxyribonucleic acid and periodic acid Schiff positive substances", J. Histochem. Cytochem. 4, DZIEWIATKowsKI, D. D. (1956). "Turnover of S35 sulfate on the mucosa of the gastrointestinal tract of rats as seen in autoradiograms ", J. biophys. biochem. Cytol. 2, FLOREY, H. W. and WEBB, R. A. (1931). "Mucus secretion in acute experimental inflammation of the colon, and other mucous membranes of the cat; histological changes", Brit. J. exp. Path. 12, FLOREY, H. W. (1955). "Mucin and the protection of the body", Proc. Roy. Soc. B, 143, GLAUERT, A. M. and GLAUERT, R. H. (1958). "Araldite as an embedding medium for electron microscopy", J. biophys. biochem. Cytol. 4, HOTCHKISS, R. D. (1948). "A microchemical reaction resulting in the staining of polysaccharide structures in fixed tissue preparations", Arch. Biochem. 16, JENNINGS, M. A. and FLOREY, H. W. (1956). "Autoradiographic observations on the mucous cells of the stomach and intestine", Quart. J. exp. Physiol. 41, KNOWLTON, N. P. and WIDNER, W. R. (1950). "The use of X-rays to determine the mitotic and intermitotic time of various mouse tissues ", Cancer Res. 10, LEBLOND, C. P. and STEVENS, C. E. (1948). "The constant renewal of the intestinal epithelium in the albino rat", Anat. Rec. 100, LEBLOND, C. P. and MESSIER, B. (1959). "Renewal of chief cells and goblet cells in the small intestine as shown by radioautography after injection of Thymidine H3 into mice", Anat. Rec. 132, MOE, H. (1955). "On goblet cells, especially of the intestine of some mammalian species", Int. Rev. Cytol. 4, PALADE, G. E. (1952). "A study of fixation for electron microscopy", J. exp. Med. 95, PALADE, G. E. (1955). "A small particulate component of the cytoplasm", J. biophys. biochem. Cytol. 1, PALADE, G. E. (1956). "Intracisternal granules in the exocrine cells of the pancreas", J. biophys. biochem. Cytol. 2, PALAY, S. L. (1958). "The morphology of secretion" pp in Frontiers in Cytology. Ed. S. L. Palay. New Haven: Yale University Press. RHODIN, J. and DALHAMN, T. (1956). "Electron microscopy of the tracheal ciliated mucosa in rat", Z. Zellforsch. 44, SIEKEVITZ, P. and PALADE, G. E. (1958 a). "A cytochemical study on the pancreas of the guinea pig. I. Isolation and enzymatic activities of cell fractions", J. biophys. biochem. Cytol. 4, SIEEEVITZ, P. and PALADE, G. E. (1958 b). "A cytochemical study on the pancreas of the guinea pig. II. Functional variations in the enzymatic activity of microsomes ", J. biophys. biochem. Cytol. 4, SIEKEVITZ, P. and PALADE, G. E. (1958 c). "A cytochemical study on the pancreas of the guinea pig. III. In vivo incorporation of leucine-l-c14 into the proteins of cell fractions", J. biophys. biochemn. Cytol. 4, SJ6STRAND, F.S. (1956). "Electron microscopy of cells and tissues". In Physical Techniques in Biological Research, Vol III. Ed. G. Oster and A. W. Pollister. New York: Academic Press Inc. WALKER, B. E. and LEBLOND, C. P. (1958). "Sites of nucleic acid synthesis in the mouse, visualized by radioautography after administration of C'4-labelled adenine and thymidine", Exp. Cell. Res. 14,
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