Abstract
Numerous macrophages were found aggregated in the lamina propria at the tips of villi in the small intestine of guinea pigs. These macrophages extended their pseudopodia into the epithelial lining and internalized fragments of effete enterocytes in their phagosomes. The epithelium of the villus tips was found to be infiltrated with numerous lymphocytes. They possessed electron-dense granules characteristic of natural killer cells, and actively interdigitated with the enterocytes. The latter were either fragmented or extensively lost in their basal cytoplasm, often leaving an attenuated apical cytoplasm of the cell. Immunohistochemical labeling using bromodeoxyuridine demonstrated that at 96 h after its administration, immunolabeled nuclei were encountered in the cytoplasm of macrophages in the lamina propria at the villus tips. These findings suggest that in the guinea pig, effete enterocytes are not simply exfoliated into the lumen, but are damaged by intraepithelial lymphocytes possessing a natural killer cytotoxicity, and subsequently phagocytosed by subepithelial macrophages.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Astaldi G, Meardi G, Lisino T (1966) The iron content of jejunal mucosa obtained by Crosby's biopsy in hemochromatosis and hemosiderosis. Blood 28: 70–82
Burnstone MS (1958) Histochemical demonstration of acid phosphatases with naphtol AS-phosphates. J Natl Cancer Inst 21: 523–539
Cerf-Bensussan N, Guy-Grand D, Griscelli C (1985) Intraepithelial lymphocytes of human gut: isolation, characterization and study of natural killer activity. Gut 26: 81–88
Cheng H, Leblond CP (1974a) Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. I. Columnar cell. Am J Anat 141: 461–480
Cheng H, Leblond CP (1974b) Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian theory of the origin of the four epithelial cell types. Am J Anat 141: 537–562
Cohn ZA (1968) The structure and function of monocytes and macrophages. Adv Immunol 9: 163–214
Deane HW (1964) Some electron microscopic observations on the lamina propria of the gut, with comments on the close association of macrophages, plasma cells, and cosinophils. Anat Rec 149: 453–474
Eastwood GL (1977) Gastrointestinal epithelial renewal. Gastroenterology 72: 962–975
Guy-Grand D, Griscelli C, Vassalli P (1978) The mouse gut lymphocyte, a novel type of T cell. Nature, origin, and traffic in normal and graft-versus-host conditions. J Exp Med 148: 1661–1677
Harmon B, Bell L, Williams L (1984) An ultrastructural study on the “meconium corpuscles” in rat foetal intestinal epithelium with particular reference to apoptosis. Anat Embryol 169: 119–124
Janeway CA, Jones B Jr, Hayday A (1988) Specificity and function of T cells bearing γσ receptors. Immunol Today 9: 73–76
Kaneda K (1989) Liver-associated large granular lymphocytes: morphological and functional aspects. Arch Histol Cytol 52: 447–459
Katunuma N, Kominami E (1983) Structures and functions of lysosomal thiol proteinases and their endogenous inhibitor. Curr Top Cell Regul 22: 71–101
Kerr JFR, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26: 239–257
Kominami E, Bando Y, Wakamatsu N, Katunuma N (1984) Different tissue distributions of two types of thiol proteinase inhibitors from rat liver and epidermis. J Biochem 96: 143–1443
Kominami E, Tsukahara T, Bando Y, Katunuma N (1985) Distribution of cathepsins B and H in rat tissues and peripheral blood cells. J Biochem 98: 87–95
Leblond CP (1981) The life history of cells in renewing systems. Am J Anat 160: 113–158
Leblond CP, Messier B (1958) Renewal of chief cells and goblet cells in the small intestine as shown by radioautography after injection of thymidine-3H into mice. Anat Rec 132: 247–259
LeFevre ME, Olivo R, Vanderhoff JW, Joel DD (1978) Accumulation of latex in Peyer's patches and its subsequent appearance in villi and mesenteric lymph nodes. Proc Soc Exp Biol Med 159: 298–302
LeFevre ME, Hammer R, Joel DD (1979) Macrophages of the mammalian small intestine: a review. J Reticuloendothel Soc 26: 553–573
MacDonald WC, Trier JS, Everett NB (1964) Cell proliferation and migration in stomach, duodenum and rectum of man. Gastroenterology 46: 405–417
Maximow A (1927) Bindegewebe and blutbildende Gewebe. In: Möllendorff W von (ed) Handbuch der mikroskopischen Anatomie des Menschen, vol. II/1. Springer, Berlin, pp 232–583
Möllendorff W von (1925) Beiträge zur Kenntnis der Stoffwanderung bei wachsenden Organismen. IV. Die Einschaltung des Farbstofftransportes in die Resorption bei Tieren verschiedenen Lebensalters. Histophysiologische Beiträge zum Resorptionsproblem. Z Zellforsch 2: 129–202
Moran R, Darzynkiewicz Z, Stainano-Coico L, Melamed MR (1985) Detection of 5-bromodeoxyuridine (BrdUrd) incorporation by monoclonal antibodies: Role of the DNA denaturation step. J Histochem Cytochem 33: 821–827
Nauss KM, Pavlina TM, Kumar V, Newberne P (1984) Functional characteristics of lymphocytes isolated from the rat large intestine. Response to T-cell mitogens and natural killer cell activity. Gastroenterology 86: 468–475
Pabst R (1987) The anatomical basis for the immune function of the gut. Anat Embryol 176: 135–144
Padykula HA (1962) Recent functional interpretations of intestinal morphology. Fed Proc 21: 873–879
Parker FG, Barnes EN, Kaye GI (1974) The pericryptal fibroblast sheath. IV. Replication, migration, and differentiation of the subepithelial fibroblasts of the crypt and villus of the rabbit jejunum. Gastroenterology 67: 607–621
Quastler H, Bensted JPM, Lamerton LF, Simpson SM (1959) Adaptation to continuous irradiation, observation on the rat intestine. Br J Radiol 32: 501–512
Reynolds CW, Timonen T, Herberman RB (1981) Natural killer (NK) cell activity in the rat. I. Isolation and characterization of the effector cells. J Immunol 127: 282–287
Saksela E, Timonen T, Ranki A, Häyry P (1979) Morphological and functional characterization of isolated effector cells responsible for human natural killer activity to fetal fibroblasts and to cultured cell line targets. Immunol Rev 44: 71–123
Sanderson CJ, Glauert AM (1979) The mechanism of T-cell mediated cytotoxicity. VI. T cell projections and their role in target cell killing. Immunology 36: 119–129
Sawicki W, Kucharczyk K, Szymanska K, Kujawa M (1977) Lamina propria macrophages of intestine of the guinea pig. Possible role in phagocytosis of migrating cells. Gastroenterology 73: 1340–1344
Searle J, Lawson TA, Abbott PJ, Harmon B, Kerr JFR (1975) An electron-microscope study of the mode of cell death induced by cancer-chemotherapeutic agents in populations of proliferating normal and neoplasmic cells. J Pathol 116: 129–138
Sugihara H, Hattori T, Fukuda M (1986) Immunohistochemical detection of bromodeoxyuridine in formalin-fixed tissues. Histochemistry 85: 193–195
Viney J, MacDonald TT, Spencer J (1990) Gamma/delta T cells in the gut epithelium. Gut 31: 841–844
Wyllie AH, Kerr JFR, Currie AR (1980) Cell death: the significance of apoptosis. Int Rev Cytol 68: 251–306
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Han, H., Iwanaga, T., Uchiyama, Y. et al. Aggregation of macrophages in the tips of intestinal villi in guinea pigs: their possible role in the phagocytosis of effete epithelial cells. Cell Tissue Res 271, 407–416 (1993). https://doi.org/10.1007/BF02913723
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02913723