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Cathepsin E in follicle associated epithelium of intestine and tonsils: localization to M cells and possible role in antigen processing

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Abstract

A specific rabbit anti-human serum was used selectively to localize the aspartic proteinase cathepsin E to follicle associated epithelium (FAE) of human and rat intestine, including jejunum, ileum, appendix, colon and rectum, as well as of human palatine, pharyngeal and lingual tonsils. Coexpression of class II histocompatibility antigen HLA-DR antigen has been observed in some of the cathepsin E-positive epithelial cells. In addition, cathepsin E has been detected in a few mononuclear cells of intestinal lymphoid structures and tonsils resembling interdigitating reticulum cells of lymph nodes. Another aspartic proteinase, cathepsin D, has been found to be poorly represented in FAE and intensely expressed by macrophages. Electron immunocytochemistry localized cathepsin E to endosomal vesicles and endoplasmic reticulum of M cells in rat and human ileum as well as of M-like cells in human palatine tonsil. The results suggest a possible role of endosomal cathepsin E in the processing of macromolecules and microorganisms transported by M cells and related epithelial cells to mucosal associated lymphoid tissue (MALT).

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References

  • Allan CH, Mendrick DL, Trier JS (1992) M cells contain acidic compartments and express class II MHC determinants. Gastroenterology 102:A589

  • Bendayan M, Zollinger M (1983) Ultrastructural localization of antigenic sites on osmium-fixed tissues applying the protein A-gold technique. J Histochem Cytochem 31:101–109

    Google Scholar 

  • Bennett K, Levine T, Ellis JS, Peanasky RJ, Samloff IM, Kay J, Chain BM (1992) Antigen processing for presentation by class II major histocompatibility complex requires cleavage by cathepsin E. Eur J Immunol 22:1519–1524

    Google Scholar 

  • Bjerke K, Brandtzaeg P (1988) Lack of relation between expression of HLA-DR and secretory component (SC) in follicle-associated epithelium of human Peyer's patches. Clin Exp Immunol 71:502–507

    Google Scholar 

  • Bjerke K, Brandtzaeg P, Fausa O (1988) T cell distribution is different in follicle-associated epithelium of human Peyer's patches and villous epithelium. Clin Exp Immunol 75:270–275

    Google Scholar 

  • Bockman DE, Cooper MD (1973) Pinocytosis by epithelium associated with lymphoid follicles in the bursa of Fabricius, appendix and Peyer's patches. An electron microscopy study. Am J Anat 136:455–478

    Google Scholar 

  • Bosi F, Silini E, Luisetti M, Romano AM, Prati U, Silvestri M, Tinelli C, Samloff IM, Fiocca R (1993) Identification and subcellular localization of aspartic proteinases in normal lung and interstitial pulmonary disease. Am J Respir Cell Mol Biol (in press)

  • Bye WA, Allan CH, Trier JS (1984) Structure, distribution and origin of M cells in Peyer's patches of mouse ileum. Gastroenterology 86:780–801

    Google Scholar 

  • Chain BM, Shaw MA (1988) Membranes proteases involved in antigen processing. J Cell Biochem 128:283

    Google Scholar 

  • Chain BM, Kaye PM, Shaw MA (1988) The biochemistry and cell biology of antigen processing. Immunol Rev 106:33–58

    Google Scholar 

  • Cornaggia M, Capella C, Riva C, Finzi G, Solcia E (1986) Electron immunocytochemical localization of pepsinogen I (PgI) in chief cells, mucous-neck cells and transitional mucous-neck/chief cells of the human fundic mucosa. Histochemistry 85:5–11

    Google Scholar 

  • Cornaggia M, Riva C, Capella C, Solcia E, Samloff IM (1987) Subcellular localization of pepsinogen II in stomach and duodenum by the immunogold technique. Gastroenterology 92:585–593

    Google Scholar 

  • Cornaggia M, Finzi G, Salvadore M, Cerati M, Capella C (1992) HLA-DR and cathepsin E expression in IBD. An immunohistochemical study. In: 3rd IGSC Joint Meeting of Surgeons and Gastroenterlogists: Abstracts. International Gastro-Surgical Club, Padua, p 316

    Google Scholar 

  • Diment S, Stahl P (1985) Macrophage endosomes contain proteases which degrade endocytosed protein ligands. J Biol Chem 260:15311–15317

    Google Scholar 

  • Diment S, Leech MS, Stahl PD (1988) Cathepsin D in membrane-associated macrophage endosomes. J Biol Chem 263:6901–6907

    Google Scholar 

  • Fiocca R, Villani L, Tenti P, Cornaggia M, Finzi G, Riva C, Capella C, Bara J, Samloff IM, Solcia E (1990) The foveolar cell component of gastric cancer. Hum Pathol 21:260–270

    Google Scholar 

  • Hirata I, Berrebi G, Austin LL, Keren DF, Dobbins WO (1986) Immunoelectron microscopic localization of HLA-DR antigen in control small intestine and colon and in inflammatory bowel disease. Dig Dsi Sci 31:1317

    Google Scholar 

  • Hsu SM, Raine L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques. J Histochem Cytochem 29:577–580

    Google Scholar 

  • Madara JL (1982) Cup cells: structure and distribution of a unique class of epithelial cells in guinea pig, rabbit and monkey small intestine. Gastroenterology 83:981–994

    Google Scholar 

  • Madara JL, Carlson SL (1985) Cup cells: further structural characterization of the brush border and the suggestion that they may serve as an attachment site for an unidentified bacillus in guinea pig ileum. Gastroenterology 89:1374–1386

    Google Scholar 

  • Marcial MA, Madara JL (1986) Cryptosporidium: cellular localization, structural analysis of absorptive cell parasite membrane-membrane interactions in guinea pigs and suggestion of protozoan transport by M cells. Gastroenterology 90:583–594

    Google Scholar 

  • Mayorga LS, Diaz R, Stahl PD (1989) Reconstitution of endosomal proteolysis in a cell-free system. J Biol Chem 264:5392–5399

    Google Scholar 

  • Neutra MR, Phillips TL, Fishkind DJ (1987) Transport of membrane-bound macromolecules by M cells in follicle associated epithelium of rabbit Peyer's patch. Cell Tissue Res 247:537–546

    Google Scholar 

  • Owen RL (1977) Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer's patches in the normal unobstructed mouse intestine: an ultrastructural study. Gastroenterology 72:440–451

    Google Scholar 

  • Owen RL, Nemanic P (1978) Antigen processing structures of the mammalian intestinal tract: a SEM study of lymphoepithelial organs. Scan Electr Microsc 2:367–378

    Google Scholar 

  • Owen RL, Pierce NF, Apple RT, Cray WC Jr (1986) M cell transport of Vibrio cholerae from the intestinal lumen into Peyer's pathches: a mechanism for antigen sampling and for microbial transepithelial migration. J Infect Dis 153:1108–1118

    Google Scholar 

  • Reid WA, Valler MJ, Kay J (1986) Immunolocalisation of cathepsin D in normal and neoplastic human tissues. J Clin Pathol 39:1323–1330

    Google Scholar 

  • Roth J, Bendayan M, Carlemalm E, Villiger W, Garavito M (1981) Enhancement of structural preservation and immunocytochemical staining in low temperature embedded pancreatic tissue. J Histochem Cytochem 29:663–671

    Google Scholar 

  • Roy MJ, Varvayanis M (1987) Development of dome epithelium in gut-associated lymphoid tissues: association of IgA with M cells. Cell Tissue Res 248:645–651

    Google Scholar 

  • Samloff IM, Shiraishi T, Taggart RT, Lechago J, Porudiminsky R (1985) Colonic slow moving protease: a possible marker of dysplasia in ulcerative colitis. Gastroenterology (Abstract) 88:1567

    Google Scholar 

  • Samloff IM, Taggart RT, Shiraishi T, Branch T, Reid WA, Heath R, Lewis RW, Valler MJ, Kay J (1987) Slow moving proteinase. Isolation, characterization, and immunohistochemical localization in gastric mucosa. Gastroenterology 93:77–84

    Google Scholar 

  • Sessa F, Bonato M, Frigerio B, Capella C, Solcia E, Prat M, Bara J, Samloff IM (1990) Ductal cancers of the pancreas frequently express markers of gastrointestinal epithelial cells. Gastroenterology 98:1655–1665

    Google Scholar 

  • Sicinski P, Rowinski J, Warchol JB, Bem W (1986) Morphometric evidence against lymphocyte-induced differentiation of M cells from absorptive cells in mouse Peyer's patches. Gastroenterology 90:609–616

    Google Scholar 

  • Sicinski P, Rowinski J, Warchol JB, Jarzabek Z, Gut W, Szczygiel B, Bielecki K, Koch G (1990) Poliovirus Type 1 enters the human host through intestinal M cells. Gastroenterology 98:56–58

    Google Scholar 

  • Solcia E, Villani L, Luinetti O, Fiocca R (1992) Patogenesi dell'ulcera peptica: Ruolo della gastrite da Helicobacter pylori ed evoluzione in corso di trattamento antibiotico e/o antisecretorio. Minerva Gastroenterol Dietol 38:81–93

    Google Scholar 

  • Solcia E, Paulli M, Fiocca R, Silini E, Kindl S, Bosi F, Finzi G, Capella C (1993) Cathepsin E in antigen presenting cells: Langerhans cells of the epidermis and interdigitating reticulum cells of lymphoid tissues. Eur J Histochem 37:19–26

    Google Scholar 

  • Spencer J, Finn T, Isaacson PG (1986) Expression of HLA-DR antigens on epithelium associated with lymphoid tissue in the human gastrointestinal tract. Gut 27:153–157

    Google Scholar 

  • Van Noorden S, Stuart MC, Cheung A, Adams EF, Polak JM (1986) Localization of human pituitary hormones by multiple immunoenzyme staining procedures using monoclonal and polyclonal antibodies. J Histochem Cytochem 34:293–298

    Google Scholar 

  • Wolf J, Rubin DH, Finberg R, Kauffman RS, Sharpe AH, Trier JS, Fields BN (1981) Intestinal M cells: A pathway for entry of retrovirus into the host. Science 212:471–472

    Google Scholar 

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Authors and Affiliations

  1. Department of Human Pathology and Genetics, II Medical Faculty, University of Pavia at Varese and Varese Multizonal Hospital, I-21100, Varese, Italy

    Giovanna Finzi, Matteo Cornaggia & Carlo Capella

  2. Department of Human Pathology and Genetics, I Medical Faculty, University of Pavia and IRCCS Policlinico S. Matteo, I-27100, Pavia, Italy

    Roberto Fiocca, Federica Bosi & Enrico Solcia

  3. Veterans Administration Medical Center, Sepulveda, California, USA

    I. Michael Samloff

  4. UCLA School of Medicine, Los Angeles, California, USA

    I. Michael Samloff

Authors
  1. Giovanna Finzi
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  2. Matteo Cornaggia
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  3. Carlo Capella
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  4. Roberto Fiocca
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  5. Federica Bosi
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  6. Enrico Solcia
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  7. I. Michael Samloff
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Finzi, G., Cornaggia, M., Capella, C. et al. Cathepsin E in follicle associated epithelium of intestine and tonsils: localization to M cells and possible role in antigen processing. Histochemistry 99, 201–211 (1993). https://doi.org/10.1007/BF00269138

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