Skip to main content
PMC home page
Immunology logoLink to Immunology
. 1997 Oct;92(2):220–225. doi: 10.1046/j.1365-2567.1997.00341.x

The polymeric immunoglobulin receptor (secretory component) in a human intestinal epithelial cell line is up-regulated by interleukin-1.

M Hayashi 1, N Takenouchi 1, M Asano 1, M Kato 1, T Tsurumachi 1, T Saito 1, I Moro 1
PMCID: PMC1364062  PMID: 9415030

Abstract

Secretory component (SC or polymeric immunoglobulin receptor) on mucosal epithelial cells mediates transcytosis of polymeric immunoglobulin into external fluids and functions as a receptor for polymeric immunoglobulin. SC expression in a human colonic adenocarcinoma cell line, HT-29 has been reported to be up-regulated by various cytokines, such as interferon-gamma, tumour necrosis factor-alpha and interleukin-4 (IL-4). However, up-regulation of SC by IL-1 is controversial. In this study, we investigated the effect of human recombinant IL-1 alone on SC expression in HT-29 cells in detail. Immunocytochemistry and Northern blot analysis revealed that IL-1 beta increased both the number of SC-positive cells and SC mRNA expression. Enzyme-linked immunosorbent assay revealed that IL-1 beta enhanced secretion by HT-29 cells in both time- and dose-dependent manners. IL-1 alpha had the same effects on HT-29 cells. Northern blot analysis demonstrated that cycloheximide and actinomycin D abolished the effect of IL-1. Moreover, we detected IL-1 receptor (IL-1R) type I mRNA in HT-29 cells by polymerase chain reaction (PCR) and sequenced the PCR-amplified product. We think that it reflects the possibility of the presence of IL-1R in HT-29 cells. From these data, we concluded that IL-1 beta and IL-1 alpha play regulatory roles in SC expression, and their effects depend on de novo protein synthesis and transcription.

Full text

PDF
220

Images in this article

222Figure 1
on p.222
224Figure 3
on p.224
224Figure 4
on p.224
224Figure 5
on p.224

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allen D. C., Biggart J. D., Orchin J. C., Foster H. An immunoperoxidase study of epithelial marker antigens in ulcerative colitis with dysplasia and carcinoma. J Clin Pathol. 1985 Jan;38(1):18–29. doi: 10.1136/jcp.38.1.18. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Auron P. E., Webb A. C., Rosenwasser L. J., Mucci S. F., Rich A., Wolff S. M., Dinarello C. A. Nucleotide sequence of human monocyte interleukin 1 precursor cDNA. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7907–7911. doi: 10.1073/pnas.81.24.7907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brandtzaeg P., Prydz H. Direct evidence for an integrated function of J chain and secretory component in epithelial transport of immunoglobulins. Nature. 1984 Sep 6;311(5981):71–73. doi: 10.1038/311071a0. [DOI] [PubMed] [Google Scholar]
  4. Brandtzaeg P. Role of J chain and secretory component in receptor-mediated glandular and hepatic transport of immunoglobulins in man. Scand J Immunol. 1985 Aug;22(2):111–146. doi: 10.1111/j.1365-3083.1985.tb01866.x. [DOI] [PubMed] [Google Scholar]
  5. Chedid M., Mizel S. B. Involvement of cyclic AMP-dependent protein kinases in the signal transduction pathway for interleukin-1. Mol Cell Biol. 1990 Jul;10(7):3824–3827. doi: 10.1128/mcb.10.7.3824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  7. Curtis B. M., Widmer M. B., deRoos P., Qwarnstrom E. E. IL-1 and its receptor are translocated to the nucleus. J Immunol. 1990 Feb 15;144(4):1295–1303. [PubMed] [Google Scholar]
  8. Dinarello C. A. Biology of interleukin 1. FASEB J. 1988 Feb;2(2):108–115. [PubMed] [Google Scholar]
  9. Kelleher R. S., Hann L. E., Edwards J. A., Sullivan D. A. Endocrine, neural, and immune control of secretory component output by lacrimal gland acinar cells. J Immunol. 1991 May 15;146(10):3405–3412. [PubMed] [Google Scholar]
  10. Kilian P. L., Kaffka K. L., Stern A. S., Woehle D., Benjamin W. R., Dechiara T. M., Gubler U., Farrar J. J., Mizel S. B., Lomedico P. T. Interleukin 1 alpha and interleukin 1 beta bind to the same receptor on T cells. J Immunol. 1986 Jun 15;136(12):4509–4514. [PubMed] [Google Scholar]
  11. Kusama K., Takahashi T., Asano M., Iwase T., Saito T., Nagasaki Y., Moro I. Murine monoclonal antibody to secretory component. Shika Kiso Igakkai Zasshi. 1989 Aug;31(4):471–473. doi: 10.2330/joralbiosci1965.31.471. [DOI] [PubMed] [Google Scholar]
  12. Kvale D., Brandtzaeg P. Constitutive and cytokine induced expression of HLA molecules, secretory component, and intercellular adhesion molecule-1 is modulated by butyrate in the colonic epithelial cell line HT-29. Gut. 1995 May;36(5):737–742. doi: 10.1136/gut.36.5.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kvale D., Løvhaug D., Sollid L. M., Brandtzaeg P. Tumor necrosis factor-alpha up-regulates expression of secretory component, the epithelial receptor for polymeric Ig. J Immunol. 1988 May 1;140(9):3086–3089. [PubMed] [Google Scholar]
  14. Lambert R. W., Kelleher R. S., Wickham L. A., Vaerman J. P., Sullivan D. A. Neuroendocrinimmune modulation of secretory component production by rat lacrimal, salivary, and intestinal epithelial cells. Invest Ophthalmol Vis Sci. 1994 Mar;35(3):1192–1201. [PubMed] [Google Scholar]
  15. Mahida Y. R., Wu K., Jewell D. P. Enhanced production of interleukin 1-beta by mononuclear cells isolated from mucosa with active ulcerative colitis of Crohn's disease. Gut. 1989 Jun;30(6):835–838. doi: 10.1136/gut.30.6.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. March C. J., Mosley B., Larsen A., Cerretti D. P., Braedt G., Price V., Gillis S., Henney C. S., Kronheim S. R., Grabstein K. Cloning, sequence and expression of two distinct human interleukin-1 complementary DNAs. Nature. 1985 Jun 20;315(6021):641–647. doi: 10.1038/315641a0. [DOI] [PubMed] [Google Scholar]
  17. McMahan C. J., Slack J. L., Mosley B., Cosman D., Lupton S. D., Brunton L. L., Grubin C. E., Wignall J. M., Jenkins N. A., Brannan C. I. A novel IL-1 receptor, cloned from B cells by mammalian expression, is expressed in many cell types. EMBO J. 1991 Oct;10(10):2821–2832. doi: 10.1002/j.1460-2075.1991.tb07831.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mostov K. E., Kraehenbuhl J. P., Blobel G. Receptor-mediated transcellular transport of immunoglobulin: synthesis of secretory component as multiple and larger transmembrane forms. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7257–7261. doi: 10.1073/pnas.77.12.7257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Muñoz E., Beutner U., Zubiaga A., Huber B. T. IL-1 activates two separate signal transduction pathways in T helper type II cells. J Immunol. 1990 Feb 1;144(3):964–969. [PubMed] [Google Scholar]
  20. Phillips J. O., Everson M. P., Moldoveanu Z., Lue C., Mestecky J. Synergistic effect of IL-4 and IFN-gamma on the expression of polymeric Ig receptor (secretory component) and IgA binding by human epithelial cells. J Immunol. 1990 Sep 15;145(6):1740–1744. [PubMed] [Google Scholar]
  21. Qwarnstrom E. E., Page R. C., Gillis S., Dower S. K. Binding, internalization, and intracellular localization of interleukin-1 beta in human diploid fibroblasts. J Biol Chem. 1988 Jun 15;263(17):8261–8269. [PubMed] [Google Scholar]
  22. Radema S. A., van Deventer S. J., Cerami A. Interleukin 1 beta is expressed predominantly by enterocytes in experimental colitis. Gastroenterology. 1991 May;100(5 Pt 1):1180–1186. [PubMed] [Google Scholar]
  23. Rognum T. O., Elgjo K., Fausa O., Brandtzaeg P. Immunohistochemical evaluation of carcinoembryonic antigen, secretory component, and epithelial IgA in ulcerative colitis with dysplasia. Gut. 1982 Feb;23(2):123–133. doi: 10.1136/gut.23.2.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Shirakawa F., Chedid M., Suttles J., Pollok B. A., Mizel S. B. Interleukin 1 and cyclic AMP induce kappa immunoglobulin light-chain expression via activation of an NF-kappa B-like DNA-binding protein. Mol Cell Biol. 1989 Mar;9(3):959–964. doi: 10.1128/mcb.9.3.959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sims J. E., Acres R. B., Grubin C. E., McMahan C. J., Wignall J. M., March C. J., Dower S. K. Cloning the interleukin 1 receptor from human T cells. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8946–8950. doi: 10.1073/pnas.86.22.8946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sims J. E., Gayle M. A., Slack J. L., Alderson M. R., Bird T. A., Giri J. G., Colotta F., Re F., Mantovani A., Shanebeck K. Interleukin 1 signaling occurs exclusively via the type I receptor. Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):6155–6159. doi: 10.1073/pnas.90.13.6155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sollid L. M., Kvale D., Brandtzaeg P., Markussen G., Thorsby E. Interferon-gamma enhances expression of secretory component, the epithelial receptor for polymeric immunoglobulins. J Immunol. 1987 Jun 15;138(12):4303–4306. [PubMed] [Google Scholar]
  28. Thrane P. S., Sollid L. M., Haanes H. R., Brandtzaeg P. Clustering of IgA-producing immunocytes related to HLA-DR-positive ducts in normal and inflamed salivary glands. Scand J Immunol. 1992 Jan;35(1):43–51. doi: 10.1111/j.1365-3083.1992.tb02832.x. [DOI] [PubMed] [Google Scholar]
  29. Valnes K., Brandtzaeg P., Elgjo K., Stave R. Specific and nonspecific humoral defense factors in the epithelium of normal and inflamed gastric mucosa. Immunohistochemical localization of immunoglobulins, secretory component, lysozyme, and lactoferrin. Gastroenterology. 1984 Mar;86(3):402–412. [PubMed] [Google Scholar]
  30. Youngman K. R., Fiocchi C., Kaetzel C. S. Inhibition of IFN-gamma activity in supernatants from stimulated human intestinal mononuclear cells prevents up-regulation of the polymeric Ig receptor in an intestinal epithelial cell line. J Immunol. 1994 Jul 15;153(2):675–681. [PubMed] [Google Scholar]
  31. Youngman K. R., Simon P. L., West G. A., Cominelli F., Rachmilewitz D., Klein J. S., Fiocchi C. Localization of intestinal interleukin 1 activity and protein and gene expression to lamina propria cells. Gastroenterology. 1993 Mar;104(3):749–758. doi: 10.1016/0016-5085(93)91010-f. [DOI] [PubMed] [Google Scholar]

Articles from Immunology are provided here courtesy of British Society for Immunology

RESOURCES