Anat. Embryol. 149, 155--171 (1976) 9 by Springer-Verlag 1976

Uhrastructure of the Surface Principal Cells of the Large Intestine in Postnatal Developing l~ats Kazuyuki Ono Department of Anatomy, School of medicine, Iwate medical University, Morioka, Japan Received January 21, 1976

Summary. The principal cells of the surface of the cecum, the ascending colon, and the descending colon in postnatal developing rats were investigated using both light and electron microscopy. In rats 1 to 14 days old the ultrastructure of the surface principal cells in the cecum and ascending colon were characterized by apical tubulo-vaeuolar systems and large supranuclear vacuoles similar to those in the absorbing cells of the neo-natal ileum as reported by Clark, 1959, and others. After about the 16th day, the special membrane system disappears from the principal cells of the proximal large intestine. On the other hand, in the descending colon, this special membrane system was absent from the cytoplasmic matrix of the epithelium. It is thought that the proximal portion of the large intestine together with the distal part of the small intestine actively participate in the absorption of protein molecules at least during the early postnatal period. Key words: Large intestinal epithelium--Postnatal development--Rat~Ultrastructure. Introduction

There are numerous reports of electron microscopic examination of the absorbing cells in the small intestine of the postnatal developing rat (Clark, 1959; Graney, 1968; Wissing and Graney, 1968; Cornell and Padykula, 1969; Worthington and Graney, 1973a). They state that during the suckling period the ileal epithelial cells contain the apical tubules and vacuoles and tubular invaginations between the microvilli (the tubulo-vacuolar system) along with the supranuelear large vacuole. Before now, the ultrastructure of the large intestine during the postnatal development has been the subject of only two reports, by Helander (1973, 1975). Although Itelander stated that the meconium corpuscles were most common in the newborn and 1-day-old rats, he did not take note of the apical tubulo-vacuolar system and the supranuclear vacuole in the surface principal cells of the transverse colon of the developing rats. I n a previous report, the author (1975a, in press) described the fine structure, the localization of the alkaline phosphatase activity, and absorption of horseradish peroxidase in different regions of the smallintestine, including the ileum, from postnatal developing and adult rats. In the present study, a report will be made on the apical tubulo-vacuolar system and the large supranuclear vacuole found for the first time in the surface principal cells of the cecum and the ascending colon of neonatal developing rats. In addition, the ultrastrueture of the principal cells of the descending colonic epithelium at electron microscopic levels will be assessed. 8 Anat.Embryol.

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Figs. i-4. Light micrograph of Epon sections of gut fixed in glutaraldehyde-OsO~. Stained with toluidine blue. • 800 Fig. 1. Epithelium of the ascending colon from a rat less 1 day old. Apical small vacuoles are found beneath the striated border in some epithelial cells Fig. 2. Epithelium of the ascending colon from a 4-day-old rat. The apical vacuoles and the supranuclear vacuoles are present in each surface principal cell Fig. 3. Epithelium of the descending colon from a 4-day-old rat. There are no vacuoles in the cytoplasm of the principal cells Fig. 4. Epithelium of the ascending colon from a 16-day-old rat. No apical vacuoles and the supranuclear vacuoles arc observed in the cytoplasm of the principal cells

Material and Methods About 90 neonatal albino rats of b o t h sexs aged 25 days or less were used in the present study. A t least 3 animals in each of the age groups were used. Also adult rats (250 grams) were used in the investigation. Newborn rats were obtained from the mother prior to suckling, a n d the other young rats a n d adult rats were fasted for a t least 15 h before killing. Small pieces were t a k e n from mid-part of the cecum, ascending colon, and descending colon. The samples were immediately immersed in 2 per cent phosphate-buffered glutaraldehyde and left there for 1 h, post-fixed in 1 per cent OsO~ with the same buffer for 1 h a t 4 ~ C, dehydrated, and embedded in Epon. U l t r a t h i n sections were stained with uranyl acet a t e and lead citrate, a n d examined in Hitachi H U 11A and H U Ds electron microscopes. For light microscopic investigation, thick sections (0.5 and 0.7/zm) were cut from the Epon blocks, m o u n t e d on glass slides a n d stained with toluidine blue. The numbers of surface principal cells with and without supranuclear vacuole were counted. The n u m b e r densities of the principal cells containing supranuclear vacuoles were expressed in percentages of the total n u m b e r of principal cells.

Results I n t h e p r e s e n t p a p e r , o n l y t h e s u r f a c e p r i n c i p a l ceils ( r e f e r e d t o b y s o m e a u t h o r s as b o u n d a r y cells or n o n - m u c o i d cells) of t h e l a r g e i n t e s t i n a l e p i t h e l i u m have been described.

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days after birth Fig. 5. Percentages of the principal cells containing supranuclear vacuoles in the rat large intestine at different stages of postnatal development

Light Microscopic Observations Cecum and Ascending Colon The cytological features of the cecal surface principal cells in early young and adult rats arc similar to the those in the ascending colon. The intestinal villi were observed in the intestinal epithelium from birth until the 8th day after birth. No villi could be seen in the cecum and ascending colon after the 9th day of neo-natal life even in the adult stage. On the day of birth the apical cytoplasm of some surface principal cells has some vacuoles which arc probably the apical tubulo-vacuolar system (Fig. 1), although the supranuclear vacuoles are absent in those cells. On the 1st day after birth the supranuclear vacuole appears in the principal cells. On the 4th day after birth, numerous principal cells possess the large supranuclear vacuoles and the apical vacuoles (Fig. 2). After the 16th day of neonatal life, the supranuclear vacuole and apical vacuole disappear from the surface principal cells (Fig. 4). The proportional number of surface principal cells containing supranuclear vacuoles in the postnatal developing rat is shown in figure 5. The percentage

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Fig. 6. The apical cytoplasm of the cecal principal cells from a rat less than 1 day old. The apical tubulo-v~cuolar system ~nd numerous free ribosomes ~re present in the apical cytoplasm. And the supranuclear part of the cytoplasm is occupied by a mass of glycogen particles. • 19,000

of t h e p r i n c i p a l cells of t h e cecum c o n t a i n i n g s u p r a n u c l e a r vacuoles in p o s t n a t a l d e v e l o p i n g r a t s is similar to t h a t of t h e p r i n c i p a l cells of t h e a s c e n d i n g colon. I n a r u t less t h a n 1 d a y old t h e p r i n c i p a l cells c o n t a i n i n g s u p r a n u c l e a r vacuoles c o n s t i t u t e o n l y 1% of t h e p r i n c i p a l cells of t h e cecum a n d ascending colon. H o w ever, on t h e 3rd d a y t h e p r o p o r t i o n of these cells i n c r e a s e d r a p i d l y . A n d on t h e 4 t h d a y a f t e r b i r t h t h e p e r c e n t a g e of t h e cells r e a c h e d a p e a k : 77 % in t h e cecum a n d 82% in t h e a s c e n d i n g colon. A f t e r t h e 8th d a y , t h e p r o p o r t i o n of

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Fig. 7. Apical cytoplasm of the surface principal cells of the ascending colon from a rat less than 1 day old. There are free ribosomes, glycogen granules, and some tiny vesicles with filamentous material resembling the surface coat substance in the apical cytoplasm. • 8,000 Fig. 8. Nuclear region of the principal cells of the ascending colon from a rat less than 1 day old. The large lysosome-like bodies are present in the cytoplasm. • 17,000

t h e p r i n c i p a l cells c o n t a i n i n g s u p r a n u c l e a r vacuoles d e c r e a s e d rapidly. These cells were n e v e r o b s e r v e d in t h e s e r a t s over 16 d a y s of age. D e s c e n d i n g Colon D u r i n g t h e p o s t n a t a l d e v e l o p i n g period, t h e apical vacuole a n d s u p r a n u e l e a r vacuole are n o t seen in t h e surface p r i n c i p a l cells of t h e descending colonic epit h e l i u m (Fig. 3).

Electron Microscopic Observations Cecum a n d A s c e n d i n g Colon I n t h e p o s t n a t a l d e v e l o p i n g a n d a d u l t rats, t h e r e are no a p p a r e n t differences in fine s t r u c t u r e b e t w e e n t h e cecal p r i n c i p a l cells a n d t h e p r i n c i p a l cells of t h e a s c e n d i n g colon. On t h e d a y of birth, t h e t u b u l e s a n d vacuoles, t o g e t h e r with t h e t u b u l a r i n v a g i n a t i o n s b e t w e e n microvilli (apical t u b u l o - v a c u o l a r system) are p r e s e n t in some p r i n c i p a l cells of t h e cecum a n d a s c e n d i n g colon (Fig. 6). A n d also n u m e r o u s free ribosomes a n d a group of glycogen granules can be seen in t h e c y t o p l a s m of t h e m a n y p r i n c i p a l cells (Figs. 6 a n d 7). Usually, m i t o e h o n d r i a

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Fig. 9. The principal cells of the cecal epithelium from a 5-day-old rat. There are apical tubule-vacuolar systems and large supranuclear vacuoles containing an amorphous material or a finely fibrillar material in the apical cytoplasm. 3litoehondria are absent in the region of the tubule-vacuolar system of the apical cytoplasm. • 9,000

Fig. 10. The apical tubules of a cecal principal cell from a 5-day-old rat. The limiting membrane of the apical tubules is coated with bristles (arrows). • 154,000 Fig. 11. The rim of the supranuclear vacuole of a eecal principal cell from a 5-day-old rat. The limiting membrane of the supranuclear vacuole (S V) containing an electron dense material is smooth. • 175,000

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Fig. 12. A principal cell of the ascending colon from an 16-day-old rat. The apical tubulo-vacuolar system and the supranuclear vacuole are absent from the cytoplasm. Numerous free ribosomes, accumulations of glycogen, and tiny vesicles are present in the cytoplasm. • 13,000 Fig. 13. Apical part of the principal cell of the ascending colon from a 25-day-old rat. Many tiny vesicles are present, but accumulations of glycogen are absent from the cytoplasm. The cell in this case, has a poorly developed surface coat. • 24,500 a n d ergastoplasm are a b s e n t from the large glycogen bodies. Sometimes, the p r i n c i p a l cells c o n t a i n various lysosome-like bodies c o n t a i n i n g some cytoplasmic c o m p o n e n t s or dense m a t e r i a l in t h e s u p r a n n c l e a r region (Fig. 8). M a n y principal

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Fig. 14. Apical cytoplasm of principal cells of the ascending colon from an adult rat. The surface coat is best seen on the mierovilli. Some tiny vesicles with the substance resembling the surface coat are seen in the cytoplasm in addition to the usual organelles. • 27,000 l~ig. 15. Supranuclear region of a principal cell of the ascending colon from an adult rat. Large lysosome-like bodies containing the mitoehondrion-like material and multivesicular bodies are present in the cytoplasm. • 18,000

cells have well-developed microvilli with surface coats, although poorly developed microvilli are occasionally observed. I n some surface prineiFal cells, intraeellular, t i n y vesicles c o n t a i n filamentous material resembling the surface coat substance (Fig. 7). I n y o u n g animals, 1 to 14 d a y of age, the p r i n c i p a l cells of the eeeum a n d ascending eolon show a n u l t r a s t r u e t u r e similar to t h a t characteristic of the epithelial cells of the ileum d u r i n g the suckling period, as previously described b y

Clark (1959) and many others. Figure 9 shows the nltrastructure of the surface principal cells of the cecum of a 5-day-old rat. Below the well-developed micro-

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Fig. 16. Some principal cells of the descending colon from a rat less than 1 day old. ~qumerous free ribosomes, accumulations of glycogen granules, and tiny vesicles are found in the cytoplasm. And also lysosome-like bodies can be seen in the cytoplasm, x 13,000

villi, t h e dense n e t w o r k s of t h e apical tubules, vacuoles, i n v a g i n a t i o n s of t h e apical cell m e m b r a n e , a n d t h e s u p r a n u c l e a r vacuole a r e seen in t h e apical cytoplasm. T h e large s u p r a n u c l e a r vacuole contains dense m a t e r i a l a n d clumps of a finely fibrillar m a t e r i a l . Sometimes, t h e y h a v e a bulge e x t e n d i n g into one of t h e smaller apical vacuoles in t h e p r i n c i p a l cells. The m i t o c h o n d r i a a n d e n d o p l a s m i c r e t i c u l u m are f o u n d in t h e p e r i p h e r a l c y t o p l a s m e x c e p t for t h e t e r m i n a l web. T h e Golgi a p p a r a t u s is o b s e r v e d on t h e p e r i p h e r y of t h e nucleus, often in association with t h e large s u p r a n u c l e a r vacuole. The l i m i t i n g m e m b r a n e of t h e smaller apical vacuoles a n d tubules, a n d of t h e i n v a g i n a t i o n b e t w e e n t h e microvilli is

Fig. 17. Apical part of a principal cell of the descending colon from a 5-day-old rat. Although some tiny vesicles and lysosome-like bodies are present on the cytoplasm, both the apical tubulo-vacuolar system and the supranuclear vacoule can not be seen in the principal cells. X 21,500 Fig. 18. A high magnification of the rectangular area outlined in Fig. 17. The intracellular, tiny vesicles possess the smooth-surfaced membrane with the substance resembling the surface coat. • 112,000

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coated with "bristles" which are evident when the membrane is cut normally (Fig. 10), although the peripheral limiting membrane of the large supranuclear vacuole is smooth (Fig. 11). During the same stage, some principal cells that do not have supranuclear vacuoles which contain numerous free ribosomes, accumulations of glycogen, apical tubulo-vaeuolar systems, or tiny vesicles like those of the principal cells from a rat less than 1 day old (see Figs. 6 and 7) are also found in the proximal large intestine. After the 8th day, the principal cells containing the supranuelear vacuoles plus tubulo-vaeuolar systems, and the principal cells containing only tubulo-vaeuolar systems decrease rapidly in number. By the 16th day of the postnatal period, the tubulo-vaeuolar system, and the supranuclear vacuole disappear from the cells of the cecum and the ascending colon, although numerous free ribosomes and accumulations of glycogen in addition to the other organelles and the tiny vesicles containing the surface coatlike substance remain (Fig. 12). At about the 25th day after birth, accumulations of glycogen and numerous free ribosomes are no longer seen in the surface principal cells. The apical cytoplasm of the principal cells contains the mierofilaments, free ribosomes, mitoehondria, rough-surfaced endoplasmie reticulum, and the tiny vesicles containing the surface coat-like substance (Fig. 13). This ultrastructural features closely resemble that of the adult animal mneosa (Fig. 14). Furthermore, in the cecum and the ascending colon the large lysosome-like bodies and the multivesicular bodies are occasionally seen in the principal cells not only in the postnatal developing rat but also in the adult rat (Fig. 15). Descending Colon In rats less than 1 day old the well-developed mierovilli covering the surface coat, microfilaments, mitoehondria, some multivesieular bodies, and tiny vesicles are found on the principal cells of the descending colon (Fig. 16). Although the apical cytoplasm contains also many glycogen granules and many free ribosomes, the apical tubulo-vacuolar system such as is in proximal portion of the large intestine during the postnatal developing period can not be seen in the descending colon. Also in a 5-day-old rat, the surface principal cells of the descending colon contain neither an apical tnbulo-vaeuolar system nor a large supranuelear vacuole although they contain some tiny vesicles (Fig. 17). The intracellular tiny vesicles (0.1-0.2 ~m in diameter) are smooth-surfaced and contain filamentous material resembling the surface coat substance (Fig. 18). This cytological features of the principal cells of the descending colon are essentially similar to those to in less than 1 day old rats, and does not greatly change during development until the 14th day after birth. In a 16-day-old rat, some glycogen particles are still present in the cytoplasm of the principal cells (Fig. 19), but it become very sparse at the weaning period (21 to 25 days after birth). The ultrastructural aspect of the principal cells at that time is almost identical to that in the adult rat (Fig. 20). Namely, there are microvilli with surface coats and tiny vesicles containing the surface coatdike substance in the cytoplasm of the surface epithelium of the descending colon in addition to the usual organelles.

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Fig. 19. Apical part of the principal cells of the descending colon from a 16-day-old rat. Some glycogen particles, free ribosomes, and tiny vesicles are present on the epithelial cells. • 19,000 Fig. 20. A principal cell of the descending colon from a n adult rat. Some tiny vesicles containing the filamentous substance are found in the cytoplasm. No accumulations of glycogen granules can be seen in the colonic cells. •

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In adult mammals, the ultrastructural appearance of the surface principal cells of the various parts of the large intestine (Hampton, 1960; Hayward and Johnston, 1961; Henrikson, 1973; Hollmann, 1965) is very similar to that observed in the absorptive cells of the small intestinal epithelium as described by many authors (see review by Trier, 1968). At the electron microscopic level, the prominent enteric surface coat was observed on the small intestinal microvilli by Ito (1965, eat, bat), and by Mukherjee and Williams (1967, mouse). Also in the surface principal cells of the large intestine, the surface coat was found on the mierovilli by Ito (1965, eat, bat), Rifaat et al. (1965, human), Pittman and Pittman (1966, human), Wetzel et al. (1966, mouse), and Mukherjee and Williams (1967, mouse). Numerous tiny vesicles containing tile surface coat-like substance were seen in the cytoplasm, particularly in the apical part of the principal cells of the colon by Pittman and Pittman (1966). That this substance was composed of acid mueosubstanee was histoehemieally demonstrated by Ito (1965) and Wetzel et al. (1966). Moreover, large lysosome-like bodies (meconinm bodies or cytoplasmic bodies) containing myelinlike material or mitoehondrion-like structure were observed in the cecal principal cells of adult mammals by Gustafsson and Maunsbaeh (1971). In the present investigation, the nltrastruetural features of adult rats were essentially in accordance with the findings of the above mentioned authors. There are no significant differences between the ultrastrnctures of the principal cells of the cecum, the ascending colon, and the descending colon. The surface principal cells often have large lysosome-like bodies and multivesicle bodies, the relatively well-developed surface coat, and numerous tiny vesicles containing the surface coat-like substance. Accordingly, these tiny vesicles may arise from the principal cells of the large intestinal epithelium, and discharge their contents into the lumen at the base of the mierovilli as previously described by Pittman and Pittman (1966), and by Wetzel et al. (1966). At present, in the postnatal developing rats, the mierovilli with well-developed surface coats, and numerous tiny vesicles containing the surface coat-like substance are observed on the principal cells of the descending colon. Moreover, numerous ribosomes and aecumulations of glycogen which may act as energy sources for cellular metabolism, are also present in the cytoplasm of the principal cells. The accumulation of glycogen in the fetal small intestinal epithelium (Bierring etal., 1964; Deren etal., 1965; Merrill et al., 1967; ttugon and Borgcrs, 1969; Vollrath, 1969) and in the fetal large intestinal epithelium (I-telander, 1973) has previously been noted in many species. In the principal cells of the large intestinal epithelimn, accumulation of numerous free ribosomes has also been reported in the rat fetus by tIelander (1973). By the 21st to the 25th day after birth, glycogen particles and free ribosomes in the principal cells of the descending colon become very sparse, and the ultrastructure of the principal cells at that time does not seem to differ greatly from that of the colon mucosa in the adult rat. In early postnatal developing rats, the ultrastrueture of some principal cells of the cecum and of the ascending colon closely resembles that of those in the

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developing descending colon. The large lysosome-like bodies, moreover, were common in the principal cells of the proximal part of the large intestine. Since these large bodies include various cytoplasmic elements, they are thought to play a role in physiological intraeellular autolysis (Moe and Behnke, 1962 ; Bierring et al., 1964). The presence of the lysosome-like bodies in the epithelial cells has already been described in the colon of fetal and newborn rats (Helander, 1973, 1975), and in the small intestine of human fetus and fetal and newborn rats (Moe and Behnke, 1962 ; Behnke, 1963 ; Bierring et al., 1964). In the present study, in addition to accumulations of glycogen and numerous free ribosomes such as those in principal eells of the descending colon as described above, an apical tubulo-vacuolar system was found in the surface principal cells of the cecum and the ascending colon from rats less than 1 day old. This tubulo-vacuolar system of the principal cells is strikingly similar to that of the columnar absorbing cells of the duodenum and the jejunum during early postnatal development, as described by previous authors (Clark, 1959; Kraehenbuhl et al., 1966; Kraehenbuhl and Capiehe, 1969; Mfllington and Brown, 1967; Staley et al., 1968; ttugon, 1970; godewald, 1970; Worthington and Graney, 1973b; Ono, 1975a). One of the most important features of this study has been the observation of the apical tubulo-vaeuolar system and the supranuelear vacuole of the surface principal cells of the cecum and the ascending colon in the postnatal developing rats (lst to 16th day). The results of the present investigation were in accordance with those previously done on the small intestine during the suckling period by many authors (Clark, 1959; Graney, 1968; Wissing and Graney, 1968 ; Cornell and Padyknla, 1969 ; Krause, 1972 ; Worthington and Graney, 1973 a; Ono, 1975a). As shown in the figure 5, the principal cells containing the large supranuelear vacuoles and the tubulo-vaeuolar systems do not include all of the principal cells of the proximal part of the large intestinal epithelium. On the 4th day after birth, a characteristic principal cell in the cecum or the ascending colon has a peak in the number of these features. The membranes of the apical tubules and the vacuoles in the surface principal cells before the 16th day were occasionally coated with bristles. This observation was also consistent with those previously done on the small intestine of neonatal developing animals by Staley et al. (1968), Wissig and Graney (1968), Worthington and Graney (1973a), and Ono (1975a). I t seems that during early postnatal development the absorption of protein molecules by the small intestine is particularly concentrated in its distal part (see Clark, 1959; Kraehenbuhl et al., 1967; Graney, 1968; Cornell and Padykula, 1969; Worthington and Graney, 1973a; Ono, in press) and also in the cecum and the ascending colon, and this is perhaps related to the presence of the "bristlecoated" membrane system as well as of the supranuelear vacuoles within the surface principal cells. The details of the uptake of exogenous protein and the localization of the alkaline phosphatase activity in large intestine of postnatal developing rats (Ono, 1975b) will be reported in later papers.

Acknowledgments. The author is greatly indebted to Professor A. Yamauchi for his critical reading of the manuscript, to Mr. K. Kumagai for his skillful technical assistance.

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Behnke, O.: Demonstration of acid phosphatase-containing granules and cytoplasmic bodies in the epithelium of foetal rat duodenum during certain stages of differentiation. J. Cell Biol. 18, 251-265 (1963) Bierring, F., Anderson, H., Egeberg, J., Bro-t~asmussen, F., Matthiessen, M. : On the nature of the meeonium corpuscles in human foetal intestinal epithelium. I. Electron microstopic studies. Acta path. mierobiol, seand. 61, 365-376 (1964) Clark, S. L. : The ingestion of proteins and colloidal materials by columnar absorptive cells of the small intestine in suckling rats and mice. J. biophys, biochem. Cytol. 5, 41-50 (1959) Cornell, It., Padykula, It. A. : A cytological study of intestinal absorption in the suckling rat. Amer. J. Anat. 125, 291-316 (1969) Deren, J. J., Strauss, E . W . , Wilson, T . g . : The development of structure and transport systems of the fetal rabbit intestine. Develop. Biol. 12,467 486 (1965) Graney, D. 0. : The uptake of ferritin by ileal absorptive cells in suckling rats. An electron microscope study. Amer. J. Anat. 123, 227-254 (1968) Gustafsson, B. E., Maunsbach, A. B. : Ultrastructure of the enlarged cecum in germfree rats. Z. Zellforsch. 120, 555-578 (1971) Hampton, J. C. : An electron microscopic study of mouse colon. Dis. Colon t~ect. 3, 423~140 (1960) I-Iayward, A. F., Johnston, H. S. : The fine structure of the epithelium of the colon in the mouse. Scot. reed. J. 6, 416 425 (1961) Helander, H. F. : Morphological studies on ~he development of the rat colonic mucosa. Acta anat. (Basel) 85, 153-176 (1973) tIelander, H. F. : Enzyme patterns and protein absorption in rat colon during development. Acta anat. (Basel) 91, 330-349 (1975) Henrikson, R . C . : Ultrastructural aspects of mouse cecal epithelium. Z. Zellforsch. 140, 445~t49 (1973) ttollmann, K. H. : Uber den Feinbau des Rectumepithels. Z. Zellforseh. 68, 502-542 (1965). Hugon, J. S. : Ultrastructural differentiation and enzymatic localization of phosphatases in the developing duodenal epithelium of the mouse. II. The newborn mouse, ttistochemie 22, 109-124 (1970) Itugon, J . S . , Borgers, M.: Ultrastructural differentiation and enzymatic localization of phosphatases in the developing duodenal epithelium of the mouse. I. The foetal mouse. Histochemie 19, 13-30 (1969) Ito, S.: The enteric surface coat on cat intestinal microvilli. J. Cell Biol. 27, 475-491 (1965) Kraehenbuhl, J . P . , Capiche, M.A.: Early stages of intestinal absorption of specific antibodies in the newborn. An ultrstruetural, eytochemical, and immunological study in the pig, rat, and rabbit. J. Cell Biol. 42, 345-365 (1969) Kraehenbuhl, J. P., Gloor, E., Blanc, B. : Morphologie comparge de la muqueuse intestinale de deux esp~ces animales aux possibilit6s d'absorption prot6que n6onatale diffgrentes. Z. Zellforsch. 70,209-219 (1966) Kraehenbuhl, J . P . , Gloor, E., Blanc, B. : l~sorption intestinale de la ferritine chez deux esp~ces animales aux possibilit~s d'absorption prot4ique n6onatale diff6renties. Z. Zellforsch. 76, 170-186 (1967) Krause, W. J. : Light and electron microscopic studies on the gastrointestinal tract of the suckling Echidna (Tachyglossus aculeatus). Anat. Rec. 172, 603-622 (1972) Merrill, T. G., Sprinz, H., Tousimis, A . J . : Changes of intestinal absorptive cells during maturation: an electron microscopic study of prenatal, postnatal, and adult guinea pig ileum. J. Ultrastruct. Res. 19, 304-326 (1967) Millington, P. F., Brown, A. C. : Electron microscope studies of the distribution of phosphatase in rat intestinal epithelium from birth to ten days after weaning. I-Iistochemie 8, 109-121 (1967) Moe, H., Behnke, O. : Cytoplasmic bodies containing mitoehondria, ribosomes, and rough surfaced endoplasmic membranes in the epithelium of the small intestine of newborn rats. J. Cell Biol. 13, 168-171 (1962)

Ultrastrueture of Large Intestinal Principal Cells

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Dr. X. Ono I)epartment of Anatomy School of Medicine Iwate Medical University Morioka 020, Japan

4 Anat. Embryol.

Ultrastructure of the surface principal cells of the large intestine in postnatal developing rats.

Anat. Embryol. 149, 155--171 (1976) 9 by Springer-Verlag 1976 Uhrastructure of the Surface Principal Cells of the Large Intestine in Postnatal Develo...
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