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Karyorrhexis and Karyolysis of Mesenchymal Cells in the Intestinal Epithelium of Amphibians and Mammals

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Karyorrhexis and Karyolysis of Mesenchymal Cells in the Intestinal Epithelium of Amphibians and Mammals Okajimas Folia Anat. Jpn., 56(2-3) : 91-158, August 1979 Karyorrhexis and Karyolysis of Mesenchymal Cells in the Intestinal Epithelium of Amphibians and Mammals With Evidence for Successful Differentiation of Some Mesenchymal Cells into Epithelial Cells By WARREN ANDREW and NANCY V. ANDREW Department of Anatomy, Indiana University, 1100 West Michigan Street, Indianapolis, Indiana 46202, U.S.A. -Received for Publication, January 25, 1979- Key Words : Karyorrhexis, Karyolysis, Mesenchymal cells, Intestinal epithelium, Differentiation of cells. Summary : The nature of the migratory process and the role of the mesenchymal cells (primarily lymphocytes) have been studied by light and electron microscopy in the small and large intestines of the urodele amphibian, Ambystoma mexicanum, and in the mouse (C57 Black) and rat (Wistar Albino). In all three species the migration is intense and in all the large intestine shows a much higher proportion of mesenchymal cells in the apical position in the epithelium between the epithelial nuclei and the lumen. The mouse intestine was chosen for quantitative studies because of the genetic homogeneity of the material and the availability of animals of known age. A marked decrease in numbers of mesenchymal cells in epithelium is seen with ad- vaning age in our specimens. The total numbers. of migrating cells in the large intestine of the mouse do not seem to be greater than in the small intestine but the number in the apical position in the large intestine is approximately nine times that in the villi. It is in this apical position in all three species that degenerative change in the mesenchymal cells usually is seen. Degenerating mesenchymal cells (lymphocytes) are within epithelial cytoplasm. Condensation of nuclear chromatin is followed by nuclear breakdown (karyorrhexis) and solution of nuclear contents (karyolysis). The material of the lymphocyte nucleus seems either to be absorbed in the eyithelial cytoplasm or discharged to the intestinal lumen. The appearance of mesenchymal cells in the basal portion of the epithelium suggests strongly that some at least of them are undergoing a transformation, in all three species, in very much the way that Mori (1937) suggested as occurring in the intestine of the amphibian Megalobatrachus japonicus. Such transformation would appear to be occurring frequently enough to play a very significant role in replacement of epithelial cells. 91 92 W. Andrew and N. V. Andrew Introduction than those in the cores of the folds. Mitotic division was seldom seen in the Susumu Mori undertook the study of connective tissue cells close to the the mode of development of the goblet epithelial layer. cells in the amphibian intestine (Mori, Two characteristics of the subepithelial 1936) and was impressed with the dif- cells were especially noteworthy to culty of equating his findings with the Mori : (1) they are mobile, moving up generally accepted view that these to make their way between the epithelial mucus-secreting cells arise only by a cells and drawing a cytoplasmic "train" functional modification of the cylindrical (Schleppe) behind them, and (2) they are epithelial cells which form the lining of able to secrete mucus while still beneath that organ. As perhaps would seem only the epithelial layer. natural, he had confined his observations Mori speaks of an individual migratory to the region alove the membrana cell as a cell unit (Zelleinheit) and propria, since he believed that he was describes these units as coming from dealing with processes occurring only the plasmodia, each of which contains a within the epithelium. Failing to find number of such units. The cell or cell the looked-for changes from lining to unit, then, frees itself from the so-called secreting cell, however, he initiated a plasmodium and moves into the epithelial second study. Mori says (1937' p. 1) : layer. Secretion of mucus, however, has "Diesmal mein Au genmerk auf das begun either during its migration or subepitheliale Bindegewebe richtend, while it is still in the plasmodium. It begegnete ich eine merkwurdige Erschei- seems highly probable to Mori that the flung, welche, scheint mir, uber die cell moving out of the plasmodium does Becherzellenfrage einen neuen Aufchluss attain an independent existence, while geben durfte." (Turning my attention the plasmodium proceeds to produce new this time to the subepithelial connective cells. He found mitotic division as an tissue, I encountered a noteworthy evidence of new cell production in the phenomenon, which, it seems to me, may plasmodia. give a new explanation for the goblet In Gekko japonicus although "plasmodia" cell problem). are not described by Mori, and apparently The observations which Mori describes do not occur in the small intestine of in this second article were made on this reptile, he does affirm an origin of small intestine from two species, one the goblet cells as from a kind of wandering urodele amphibian, Megalobatrachus cell which again makes its way between jaPonicus and the other the reptile, the ordinary epithelial cells. These, he Gekko japonicus. They were made with says, probably are the so-called "replace- the light microscope on sections 4-5 ment cells" which many earlier authors micra (micrometers) thick, stained with had described as occurring between the hemalum or iron hematoxylin (Regaud) basal parts of the cylindrical cells. and with mucicarmine. While commendably cautious on this In the interior of the mucosal folds of point, he states (p. 270) : "Deshalb neige Megalobatrachus japonicus, certain cells ich vielleicht zu denken, dass die were seen with deeply stained nuclei sogenannte Ersatzzelle nichts anderes als and with scanty cytoplasm, The more eine bindegewebige Zelle ist, welche aus deeply situated free cells in the loose dem Darmstroma in die Epithelschicht connective tissue had nuclei more rounded einwandert." (Therefore, I incline perhaps Karyorrhexis and Karyolytis of Mesenchymal Cellt 93 to think that the so-called replacement the blood of invertebrates (Andrew, cell is nothing other than a connective 1961, 1962), as well as the review of the tissue cell which migrates from the work of many authors on the blood, intestinal stroma into the epithelial lymph, and tissue fluid of lower verteb- layer). Settled between the epithelial rates which we carried out in the pre- cells, such a cell gradually changes paration of a book on "Comparative from its rounded form, pushing forward Hematology" (Andrew, 1965a) have shown a cytoplasmic extension toward the us the importance of the lymphocyte in surface to become at first an immature its multipotential characteristics. It is "goblet cell" without secretion , then this evidence, together with the results attaining to the lumen with its apical of the most recent work by a number end and actively producing mucus. of investigators in the fields of ultra- We have described the work of Mori structure, immunology, and tissue repair at some length here because, although it which we have brought together in the has not served as a basis for our monograph (Andrew, 1978). The broad research on the intestinal epithelium, we outlook on cell transformation and its have been impressed by the increasing role in the body economy has stimulated significance to some fundamental bio- us to re-investigate the phenomena in logical problems which it has presented the intestine of the urodele amphibians, in the development of our own concepts. especially in relation to the early work In the preparation of a monograph on of Mori. "The Lymphocyte in Evolution : New Light on its Role as a Transforming Materials and Methods Cell in Blood and Tissues" (Andrew, 1978), we have found it necessary to In the present study observations have review a large amount of literature on been made on the relation between the relation between wandering cells migrating mesenchymal cells (largely and "stable" epithelial cells. We have classifiable as lymphocytes) and the found that the observations and con. intestinal epithelium in one species of clusions of Mori on the phenomena as amphibian and in several species of seen in urodele amphibians and in reptiles mammals. The amphibian species is the have received markably little attention Axolotl, Ambystoma mexicanum, which in the literature. has been much used in experimental It is true that Mori newhere uses the studies. An analysis of the literature term "lymphocyte", speaking of the on the viscera and lymphatic system of wandering cell as "eine bindegewebige this species has been made (Smith, R.B., Zelle" (connective tissue cell) which and H.M. Smith, 1969) and has been wanders out from the intestinal stroma useful to us. into the epithelium. There may indeed We have used 33 individuals of the be some room for discussion as to Axolotl, all of which came originally which term is preferable in describing from the laboratory of Rufus Richard the migrating cells. It seems to us, Humphrey in the Department of Zoology however, that Mori, intent on describing of Indiana University. On all of these the intestine, was not likely to have animals the time between spawning and been concerned about a more specific sacrifice is indicated as the age of the designation of such cells. The individual individual, which ranges from nine research studies which we have made on months to over eight years. 94 W. Andrew and N. V. Andrew In the study of the intestinal epithe- the intestine of Ambystoma mexicanum lium of mammals, we have used chiefly (Andrew, 1972, 1975) we have discussed the C57 Black mouse and the Albino rat briefly the general histological structure of the Wistar Institute. The ages of of that organ. The cells have diameters all of the rodents were known and several times greater than those in the recorded. The mice are of both sexes mouse and rat. The greatest difference, and range in age from 88 to 849 days. however, is seen in the presence in this The rats all are 100 days of age.
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