HISTOCHEMICAL LOCALIZATION OF GASTRIC AND SMALL BOWEL MUCOSAL ENZYMES OF MAN, MONKEY, AND CHIMPANZEE

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1 GASTROENTEROLOGY Copyright 1967 by The Williams & Wilkins Co. Vol. 52, No.2, Part 1 Printed in U.S.A. HISTOCHEMICAL LOCALIZATION OF GASTRIC AND SMALL BOWEL MUCOSAL ENZYMES OF MAN, MONKEY, AND CHIMPANZEE MARTIN H. FLOCH, M.S., M.D., SUSAN VAN NOORDEN, M.A., AND HOWARD M. SPIRO, M.D. Department of Internal Medicine, Yale University School of Medicine, New Haven, Connecticut The interpretation and application of histochemical studies in gastrointestinal research has been hampered by some major differences in enzyme activity between smaller laboratory animals and man.!,2 Because the gastrointestinal function of a primate, the macaque, appears to be similar to that of man, we have studied the histochemical localization of a series of enzyme reactions of the upper gastrointestinal tract of man, the macaque, and the chimpanzee. Materials and Methods Five histologically normal gastric specimens and five histologically normal distal duodenal specimens were obtained by either the Crosby-Kugler capsule 3 or Brandborg tube' from patients studied for gastrointestinal disorders. Thirty gastric and 30 distal duodenal specimens were obtained from 5 chimpanzees (Papia papia) via a Brandborg tube 4 and 12 gastric and 24 small bowel specimens from monkeys (Macaca mulatta) killed for tissue culture purposes in another laboratory. Specimens were orientated on the vertical side of a supporting block of animal liver, quick frozen in liquid nitrogen, and stored at Received March 24, Accepted September 12, Address requests for reprints to: Martin Floch, M.D., Department of Medicine, Yale University School of Medicine, 333 Cedar Street, New Haven, Connecticut This investigation was supported in part by United States Army Research and Development Command Contracts DA MD-2732 and DA MD-2062 and by United States Public Health Service Grants AM and AM l. The authors express their appreciation to Dr. Robert McCollum for his cooperation in obtaining chimpanzee peroral small bowel biopsy and monkey autopsy specimens C sealed in plastic. Sections were cut at 4 fl in a cryostat at -20 C, picked up on a cover slip, and, according to the enzyme method to be used, either allowed to thaw and dry briefly at room temperature or fixed in cold neutral phosphate-buffered 10% formalin or cold acetone: Standard paraffin sections were stained with hematoxylin and eosin. Fresh specimens were observed under the dissecting microscope.' The following enzyme methods were employed. Nonspecific esterase: indoxyl method of Holt with 5-bromo-4-chloro-indoxyl acetate as the substrate, using sections fixed in formalin, with incubation at 37 C for 45 min." Leucine aminopeptidase: method of N achlas, Crawford, and Seligman using unfixed sections and 1 - l e u c y l - ~ - n aas p h the t h y l a m i d substrate 7 with incubation at 37 C for 15 min. Alkaline phosphatase: method of Burstone using naphthol AS-TR-phosphate as the substrate and fast red TR as the diazonium salt with sections fixed in cold acetones with incubation at room temperature for 20 min. Acid phosphatase: method of Burstone using naphthol AS-TR-phosphate as the substrate and fast dark blue R as the diazonium salt with sections fixed in cold formalin with incubation at 37 C for 90 min 9 and the method of Gomori using lead sulfide: Reduced nicotinamide adenine dinucleotide (NAD) and nicotinamide adenine dinucleotide phosphate (NADP) dehydrogenase: method of Scarpelli, Hess, and Pearse with incubation for 30 min at 37 C." O Succinate dehydrogenase: method of Pearse using 2, 5-diphenyltetrazoliumbromide (MTT) as the tetrazolium salt with incubation for 30 min at 37 Co" Cytochrome oxidase: method of Burstone using p-aminodiphenyl amine and variamine blue B base with incubation for 60 min at 37 C. 11 All reactions were recorded by two observers as 0, nonreactive; 1+, trace positive (fig. 1); 2+, definite positive (fig. 2); 3+ moderate reaction (fig. 2); or 4+, strong reaction (figs. 1 and 3). Comparisons of the

2 February 1967 HISTOCHEMICAL 1,OCALIZATION OF MUCOSAL ENZYMES FIG. 1. Low power photomicrograph of monkey stomach. Cytochrome oxidase reaction (black granules ). Parietal cells are stained strongly (4+) and peripheral epithelium and chief cells give a trace reaction (1+). This is a black color stain and the ap pearance;is similar for all oxidative enzymes, succinate dehydrogenase, reduced nicotinamide adepine dinucleotide, and nicotinam ide a denine dinucleotide phosphate dehydrogenases (X 1(0). FIG. 2. Low power photomicrograph of monkey jejunum. Reduced nicotinamide adenine dinucleotide dehydrogenase reaction which is moderate (3+) in epithelium of villi and trace to definite (2+) reaction in crypts. The appearance of the reaction is similar, except for minor localization differences (see t ext) for all the oxidative enzymes, succinate dehydrogenase, cytochrome oxidase, and reduced nicotinamide adenine dinucleotide phosphate dehydrogenase. The liver tissue on which specimens are mounted is seen above the small bowel ( X 100). 231

3 232 FLOCH ET AL. Vol. 52, No. 2, Part 1 Enzyme TABLE 1. Mucosal enzyme activity in man, monkey, and chimpanzee' Epithelium Stomach Small bowel Parietal Chief cells Villous Crypt cells epithelium epithelium Lamina propria Alkaline phosphatase > 0->+ +-> Acid phosphatase > ++ -> ++ -> + -> c Esterase 0->+ ++ -> Succinate dehydrogenase > > Reduced nicotinamide ade- 0-> > nine dinucleotide dehydrogenase Reduced nicotinamide ade- + -> " +-> nine dinucleotide phosphate dehydrogenase Leucine aminopeptidase Cytochrome oxidase 0-> > ++++c See section on methods for interpretation of + ratings. Blood vessels. c Macrophages. d Brunner's glands. Differences in the chimpanzee are recorded in the text. three species were made only on specimens stained simultaneously (table 1). Results Dissecting Microscope Appearance of Small Bowel Both man and the chimpanzee had typical finger-like villi. The villi of the monkey appeared as either ridges or leafiike structures. Histology Gastric and small bowel architecture and cell structure were normal in all animals studied and resembled the typical human histology described in standard texts. 12, 13 The ratio of the length of small bowel villi to crypt area ranged between 3 and 4: 1. In a few of the duodenal specimens from the chimpanzee, a mild increase of lymphocytes and plasma cells was noted in the lamina propria. Enzymes The enzyme activities for the various mucosal elements are recorded in table 1. The description of individual enzyme distribution is as follows. Alkaline phosphatase. Stomach: except for activity in endothelial cells of blood vessels, no significant reaction was observed in the mucosa of any of the three species. Small intestine: no differences in activity were noted among the three speies. Activity was localized to the brush border and juxtaapical portion of the epithelial cells of the villi. There was heavy concentration of the azo dye in these areas as compared to the positive reaction in the endothelium of t he blood vessels (fig. 3A and B). Crypt cells reacted poorly. Acid phosphatase. Stomach: there was no appreciable difference between the results of the two techniques or among the three species. Activity was moderate to strong in chief cells and weak in surface epithelial and parietal cells. The azo dye was distributed evenly through the cytoplasm of reacting cells. Small intestine: activity was variable but the same in all three species. It was noted primarily along the apical portion and brush border of the

4 February 1967 HISTO CHEMICAL LOCALIZATION OF MUCOSAL ENZYMES 233 FIG. 3. Alkaline phosphatase reaction. A, low power photomicrograph of monkey jejunum. White arrow points to strong (4+) reaction in brush border which outlines the small bowel. The black arrow points to a positive (2+) reaction in blood vessel wall (X 100). B, oil immersion photomicrograph of same slide demonstrating activity in brush border (X 10(0). epithelial cells of the villi. So-called "lysosomal" distribution was also observed in the apical portion of these cells (fig. 4A). In the crypts, a heavy concentration of azo dye was noted in the area of Paneth cells, but the staining ' material could not be identified as Paneth granules (fig. 4B). Cytoplasm of macrophages in the lamina propria often had a strong reaction. Esterase. Stomach: most prominent indigo precipitates were noted in the area of greatest parietal cell concentration in all three species (fig. 5A). In this area, chief cells also reacted more strongly than in

5 234 FLOCH ET.ilL. Vol. 52, No.2, Part 1 FIG. 4. Acid phosphatase reaction. A, high power photomicrograph of monkey jejunal epithelium. Note strong (4+) reaction in apical portion of cell, lysosomes (black arrow), and macro phages (white arrow) (X 400). B, oil immersion photomicrograph of crypt cells of chimpanzee jejunum. Note strong cytoplasm reactions. Arrow points to granules of Paneth cells which are not stained (X 1000). the base of the glands where they gave a weak reaction similar to that of surface epithelium. The indigo precipitate was localized to the cytoplasm of the gland cells. Small intestine: the distribution was the same in all three species. The indigo precipitate was distributed diffusely through the cytoplasm of the epithelial cells (fig. 5B). The reaction was strong in the villi and faint in the crypts. Occasionally the cytoplasm of round cells of the lamina also gave a faint reaction. Cytochrome oxidase. Stomach: in all three species, there was a marked precipitate of granules throughout the cytoplasm of the parietal cells, but superficial epi-

6 February 1967 HISTOCHEMICAL LOCALIZATION OF MUCOSAL ENZYMES 235 FIG. 5. Nonspecific esterase. A, low power photomicrograph of monkey stomach. Note heavy concentration of stain in parietal cell area (arrow) (X 100). B, oil immersion photomicrograph of monkey duodenal epithelium. Note the diffuse even distribution of indigo throughout the cytoplasm (X 1000). thelial and chief cells reacted poorly (fig. 1). Small intestine: in all three species, both the villi and crypt epithelial cell cytoplasm reacted moderately. At times, scattered particles of reactive material were noted in the lamina, probably representing enzyme activity within macrophages. Often round cells reacted strongly. Leucine aminopeptidase. Stomach: no activity was noted. Small intestine: a moderate reaction of epithelial cells of villi, but not crypts, was noted in all three species. Activity varied to some extent. In most specimens the reaction occurred evenly throughout the cytoplasm. Succinate dehydrogenase. Stomach: pa-

7 236 FLOCH ET AL. rietal cells reacted strongly, chief cells weakly, and superficial epithelial cells faintly in all three species. Formazan deposits were distributed diffusely through the cytoplasm (see description of cytochrome oxidase in legend to fig. 1). Small intestine: the columnar cells of both the villi and crypts reacted strongly in all three species. Formazan granules were spread evenly throughout the cytoplasm (fig. 2). Reduced N AD dehydrogenase. Stomach: formazan granules were deposited heavily and evenly through the cytoplasm of parietal cells. Chief and superficial epithelial cells either reacted faintly or not at all in all three species (see description of cytochrome oxidase in legend to fig. 1). Small intestine: the cytoplasm of epithelial cells had formazan granules distributed throughout in a strong reaction. The reaction was Vol. 52, No.2, Part 1 moderate in crypt epithelial cells. Findings were similar in all three species (fig. 2). Reduced N ADP dehydrogenase. Stomach: in all three species, the parietal cell cytoplasm reacted moderately, and the chief and surface epithelial cell cytoplasm weakly but definitely, except in man where the epithelial cell cytoplasm gave a moderate reaction. Formazan granules were distributed throughout the cytoplasm, being heaviest in parietal cells. Small intestine: in man and the monkey, the epithelial cell cytoplasm of the villi reacted strongly and the crypt cells weakly (fig. 6A). In the chimpanzee, the reactions varied from that of the other species to a "pattern" 14 where the major site of reaction was along the apical portion of the cell and the brush border (fig. 6B). This was noted in both villi and crypts. It occurred in all 5 of the chimpanzees in FIG. 6. Reduced nicotinamide adenine dinucleotide phosphate dehydrogenase. A, high power photomicrograph of human duodenal villi demonstrating moderate (3+) reaction throughout epithelial cells (X 400). B, high power photomicrograph of chimpanzee duodenum demonstrating localization of granules to apical border of epithelial cells (X 400).

8 February 1967 HISTOCHEMICAL LOCALIZATION OF MUCOSAL ENZYMES 237 varying degrees. In 2 animals, it was the predominant pattern, while in 1 it was noted only on one section. Discussion The significance of the histochemically identifiable intracellular mucosal enzymes in gastrointestinal physiology is poorly understood. However, their variation in activity and specific localization in gastric and small intestinal mucosal cells indicate that they may reflect some specific anatomy or function of these cells (e.g., alkaline phosphatase in the brush border of the small intestine and cytochrome oxidase in parietal cells). But the relation of histochemically identifiable enzymes to specific cellular function is still not clear. The enzymes studied here have a similar distribution in the mucosa of man, chimpanzee, and monkey. The degree of reaction observed was also about the same. Therefore, we can state that gastric and small bowel mucosal enzyme localization and integrity for the enzymes studied are similar for man, monkey, and the chimpanzee. This is of some importance since comparative studies have revealed discrepancies in cellular enzyme localization and activity between man and the laboratory animals commonly employed for gastric and small bowel studies.1, 2, 15 Since Schnitka's review in 1960, a number of histochemical studies of the gastrointestinal tract have been carried out in primates. Because there has been some disagreement about the distribution of acid phosphate and nonspecific esterase, a few comments are in order. We observed acid phosphatase activity to be most prominent in the chief cells with both the azo dye method and the lead sulfide technique. This confirms the observation of Planteydt and Willighagen,16 Correia et al.,17 and Ragins et al. 2 in man, but not of other workers who found the enzyme to be most prominent in the parietal cells. 18-2o We are unable to explain why our results with the acid phosphatase reaction in the small bowel demonstrate more activity in the apical portion and brush border than previously reported. 21,22 Padykula et al.,21 using the Gomori technique, and Spiro et al.,22 using the Burstone technique in another laboratory, observed the major dye deposition in the lysosomal areas. We used both techniques, repeatedly, at ph 5 and were able to demonstrate the dye in the apical area, as well as the lysosomal and Paneth cell distribution previously recorded (fig. 4). Results of histochemical localization of nonspecific esterase appear to vary with the substrate employed. Chessick,23 using,b-naphthyl acetate and naphthol AS acetate, found the parietal cells generally negative for esterase and the chief cells strongly positive. Nachlas and Seligman,24 using,b-naphthyl acetate as the substrate, and Planteydt and Willighagen,16 using both the,b-naphthyl acetate and the indoxyl acetate method, found that parietal cells stained more intensely than chief cells. Our results, using Holt's indoxyl method, agree with the latter observations. Except for these discrepancies in esterase distribution in the stomach and acid phosphatase in the stomach and small bowel, all reports concerning man agree with our observations on the localization of the other enzymes studied in the gastric and small bowel mucosa. The only difference that we detected among the three species was the abnormal distribution of reduced NADP dehydrogenase in the chimpanzee small bowel epithelium. This pattern of apical distribution has been noted in the rectal mucosa of ulcerative colitis patients,14 and in various parts of the bowel in man where an inflammatory response was present.25 The areas of the chimpanzee which showed this change had a mild inflammatory infiltrate, although the animals appeared healthy. Except for this variation, our data indicate that the mucosal enzymes of the stomach and small bowel are located in approximately the same areas with the same intensity of reaction in man, the monkey, and the chimpanzee. Summary Specimens of gastric and distal duodenal mucosa from the chimpanzee, man, and monkey were compared for activity of nonspecific esterase, alkaline phosphatase, acid

9 238 FLOCH ET AL. Vol. 52, No.2, Part 1 phosphatase, succinate dehydrogenase, reduced nicotinamide adenine dinucleotide and nicotinamide adenine dinucleotide phosphate dehydrogenases, and cytochrome oxidase. Except for an abnormal distribution of reduced nicotinamide adenine dinucleotide phosphate dehydrogenase in the chimpanzee small bowel, which may well have been the result of some chronic inflammatory response, all the enzymes studied in the three species of primates had essentially the same localization and intensity of reaction. REFERENCES 1. Schnitka, T. K Enzymatic histochemistry of gastrointestinal mucous membranes. Fed. Proc. 19: Ragins, H., M. Dittbrenner, and J. Diaz Comparative histochemistry of the gastric mucosa : a survey of the common laboratory animals and man. Anat. Rec. 150 : Crosby, W. H., and H. W. Kugler Intraluminal biopsy of small intestine. Amer. J. Dig. Dis. 2: Brandborg, L. L., C. E. Rubin, and W. E. Quinton Multipurpose instrument for suction biopsy of esophagus, stomach, small bowel and colon. Gastroenterology 37 : Pearse, A. G. E Histochemistry, theoretical and applied, Ed. 2. J. and A. Churchill, Ltd., London. 6. Holt, S. J lndigogenic staining methods for esterases, p In J. F. Danielli [ed.], General cytochemical methods, Vol. 1. Academic Press, New York. 7. Nachlas, M. M., D. T. Crawford, and A. M. Seligman The histochemical d emonstration of leucine aminopeptidase. J. Histochern. Cytochem. 5: Burstone, M. S Histochemical comparison of naphthol AS-phosphates for the demonstration of phosphatases. J. Nat. Cancer lnst. 20 : Burstone, M. S Histochemical demonstration of acid phosphatases with naphthol AS-phosphates. J. Nat. Cancer Inst. 21: Scarpelli, D. G., R. Hess, and A. G. E. Pearse The cytochemical localization of oxidative enzymes. J. Biophys. Biochem. Cytol. 4: Burstone, M. S Modification of histochemical techniques for the demonstration of cytochrome oxidase. J. Histochem. Cytochem. 9: Palmer, E Gastritis: a revaluation. Medicine (BaIt.) 33 : Sheehy, T., and M. H. Floch The small intestine: its function and diseases. Hoeber Medical Division, Harper and Row, Publishers, New York. 14. Mendeloff, A. I., and B. Morris Histochemical studies of three dehydrogenase systems in ulcerative colitis biopsy specimens. Gastroenteology 48: Jervis, H. R Enzymes in the mucosa of the small intestine of the rat, the guinea-pig and the rabbit. J. Histochem. Cytochem. 11: Planteydt, H. T., and R. G. J. Willighagen Enzyme histochemistry of the human stomach with special reference to intestinal metaplasia. J. Path. Bact. 80: Correia, J. P., M. I. Filipe, and J. C. Santos Histochemistry of the gastric mucosa. Gut 4: Rotenberg, A. M., B. Monis, and B. M. Banks Histochemical distribution of hydrolytic enzymes in the alimentary tract in man in health and disease. J. Histochem. Cytochem. 6: Roseman, D. M., D. Simon, and M. H. Sleisenger The concentration and distribution of acid phosphatase in the human stomach with particular reference to gastric carcinoma. Gastroenterology 36 : Dawson, I., and J. Pyrse-Davies The distribution of certain enzyme systems in the normal human gastrointestinal tract: Gastroenterology 44: Padykula, H. A., E. W. Strauss, A. J. Ladman, and F. H. Gardner A morphologic and histochemical analysis of the human jejunal epithelium in nontropical sprue. Gastroenterology 40 : Spiro, H. M., M. I. Filipe, J. S. Stewart, C. C. Booth, and A. G. E. Pearse Functional histochemistry of the small bowel mucosa in malabsorption syndrome. Gut 5: Chessick, R. D Histochemical study of the distribution of esterases. J. Histochem. Cytochem. 1 : Nachlas, M. M., and A. M. Seligman The comparative distribution of esterase in the tissues of five mammals by a histochemical technique. Anat. Rec. 105: Van Norden, S., W. Thayer, R. Yesner, and H. M. Spiro Some histochemical observations in ulcerative colitis. J. Path. Bact. In press.

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