Skip to main content
NCBI home page
The American Journal of Pathology logoLink to The American Journal of Pathology
. 1991 Jun;138(6):1299–1305.

Interleukin-1 mRNA-expressing macrophages in human chronically inflamed gingival tissues.

Y Matsuki 1, T Yamamoto 1, K Hara 1
PMCID: PMC1886402  PMID: 2053589

Abstract

Interleukin-1 (IL-1)-producing cells in inflamed gingival tissues obtained from patients with periodontitis were examined by combined immunohistochemistry and in situ hybridization. Macrophages, T cells, B cells, and endothelial cells were visualized in the lesions by the immunoperoxidase method using specific antibodies to each cell type. Subsequent in situ hybridization using 35S-labeled synthetic oligonucleotide probes complementary to human IL-1 alpha and IL-1 beta mRNA showed IL-1 transcripts in macrophages predominantly but not in T cells or B cells. Neither fibroblasts nor keratinocytes contained the IL-1 message to any significant extent. Endothelial cells also were essentially negative for IL-1 messages. These findings indicate that IL-1 is produced principally by macrophages in inflamed gingival tissues of humans.

Full text

PDF
1299

Images in this article

1301Figure 1
on p.1301
1301Figure 2
on p.1301
1303Figure 3
on p.1303

Selected References

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

  1. Charon J. A., Luger T. A., Mergenhagen S. E., Oppenheim J. J. Increased thymocyte-activating factor in human gingival fluid during gingival inflammation. Infect Immun. 1982 Dec;38(3):1190–1195. doi: 10.1128/iai.38.3.1190-1195.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Deng G., Wu R. An improved procedure for utilizing terminal transferase to add homopolymers to the 3' termini of DNA. Nucleic Acids Res. 1981 Aug 25;9(16):4173–4188. doi: 10.1093/nar/9.16.4173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dinarello C. A. Interleukin-1 and its biologically related cytokines. Adv Immunol. 1989;44:153–205. doi: 10.1016/s0065-2776(08)60642-2. [DOI] [PubMed] [Google Scholar]
  4. Dower S. K., Kronheim S. R., Hopp T. P., Cantrell M., Deeley M., Gillis S., Henney C. S., Urdal D. L. The cell surface receptors for interleukin-1 alpha and interleukin-1 beta are identical. Nature. 1986 Nov 20;324(6094):266–268. doi: 10.1038/324266a0. [DOI] [PubMed] [Google Scholar]
  5. Furutani Y., Notake M., Fukui T., Ohue M., Nomura H., Yamada M., Nakamura S. Complete nucleotide sequence of the gene for human interleukin 1 alpha. Nucleic Acids Res. 1986 Apr 25;14(8):3167–3179. doi: 10.1093/nar/14.8.3167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hirano T., Yasukawa K., Harada H., Taga T., Watanabe Y., Matsuda T., Kashiwamura S., Nakajima K., Koyama K., Iwamatsu A. Complementary DNA for a novel human interleukin (BSF-2) that induces B lymphocytes to produce immunoglobulin. Nature. 1986 Nov 6;324(6092):73–76. doi: 10.1038/324073a0. [DOI] [PubMed] [Google Scholar]
  7. Iribe H., Koga T., Kotani S., Kusumoto S., Shiba T. Stimulating effect of MDP and its adjuvant-active analogues on guinea pig fibroblasts for the production of thymocyte-activating factor. J Exp Med. 1983 Jun 1;157(6):2190–2195. doi: 10.1084/jem.157.6.2190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Jandinski J. J., Stashenko P., Feder L. S., Leung C. C., Peros W. J., Rynar J. E., Deasy M. J. Localization of interleukin-1 beta in human periodontal tissue. J Periodontol. 1991 Jan;62(1):36–43. doi: 10.1902/jop.1991.62.1.36. [DOI] [PubMed] [Google Scholar]
  9. Kabashima H., Maeda K., Iwamoto Y., Hirofuji T., Yoneda M., Yamashita K., Aono M. Partial characterization of an interleukin-1-like factor in human gingival crevicular fluid from patients with chronic inflammatory periodontal disease. Infect Immun. 1990 Aug;58(8):2621–2627. doi: 10.1128/iai.58.8.2621-2627.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kupper T. S., Ballard D. W., Chua A. O., McGuire J. S., Flood P. M., Horowitz M. C., Langdon R., Lightfoot L., Gubler U. Human keratinocytes contain mRNA indistinguishable from monocyte interleukin 1 alpha and beta mRNA. Keratinocyte epidermal cell-derived thymocyte-activating factor is identical to interleukin 1. J Exp Med. 1986 Dec 1;164(6):2095–2100. doi: 10.1084/jem.164.6.2095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kurt-Jones E. A., Fiers W., Pober J. S. Membrane interleukin 1 induction on human endothelial cells and dermal fibroblasts. J Immunol. 1987 Oct 1;139(7):2317–2324. [PubMed] [Google Scholar]
  12. Le J. M., Vilcek J. Interleukin 6: a multifunctional cytokine regulating immune reactions and the acute phase protein response. Lab Invest. 1989 Dec;61(6):588–602. [PubMed] [Google Scholar]
  13. Libby P., Ordovas J. M., Auger K. R., Robbins A. H., Birinyi L. K., Dinarello C. A. Endotoxin and tumor necrosis factor induce interleukin-1 gene expression in adult human vascular endothelial cells. Am J Pathol. 1986 Aug;124(2):179–185. [PMC free article] [PubMed] [Google Scholar]
  14. Lindemann R. A., Economou J. S., Rothermel H. Production of interleukin-1 and tumor necrosis factor by human peripheral monocytes activated by periodontal bacteria and extracted lipopolysaccharides. J Dent Res. 1988 Aug;67(8):1131–1135. doi: 10.1177/00220345880670081401. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Masada M. P., Persson R., Kenney J. S., Lee S. W., Page R. C., Allison A. C. Measurement of interleukin-1 alpha and -1 beta in gingival crevicular fluid: implications for the pathogenesis of periodontal disease. J Periodontal Res. 1990 May;25(3):156–163. doi: 10.1111/j.1600-0765.1990.tb01038.x. [DOI] [PubMed] [Google Scholar]
  17. Mason D. Y., Comans-Bitter W. M., Cordell J. L., Verhoeven M. A., van Dongen J. J. Antibody L26 recognizes an intracellular epitope on the B-cell-associated CD20 antigen. Am J Pathol. 1990 Jun;136(6):1215–1222. [PMC free article] [PubMed] [Google Scholar]
  18. Mergenhagen S. E. Thymocyte activating factor(s) in human gingival fluids. J Dent Res. 1984 Mar;63(3):461–464. doi: 10.1177/00220345840630031901. [DOI] [PubMed] [Google Scholar]
  19. Muraguchi A., Hirano T., Tang B., Matsuda T., Horii Y., Nakajima K., Kishimoto T. The essential role of B cell stimulatory factor 2 (BSF-2/IL-6) for the terminal differentiation of B cells. J Exp Med. 1988 Feb 1;167(2):332–344. doi: 10.1084/jem.167.2.332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nelson J. A., Reynolds-Kohler C., Oldstone M. B., Wiley C. A. HIV and HCMV coinfect brain cells in patients with AIDS. Virology. 1988 Jul;165(1):286–290. doi: 10.1016/0042-6822(88)90685-x. [DOI] [PubMed] [Google Scholar]
  21. Norton A. J., Isaacson P. G. Monoclonal antibody L26: an antibody that is reactive with normal and neoplastic B lymphocytes in routinely fixed and paraffin wax embedded tissues. J Clin Pathol. 1987 Dec;40(12):1405–1412. doi: 10.1136/jcp.40.12.1405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Norton A. J., Ramsay A. D., Smith S. H., Beverley P. C., Isaacson P. G. Monoclonal antibody (UCHL1) that recognises normal and neoplastic T cells in routinely fixed tissues. J Clin Pathol. 1986 Apr;39(4):399–405. doi: 10.1136/jcp.39.4.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ohmori Y., Hanazawa S., Amano S., Miyoshi T., Hirose K., Kitano S. Spontaneous production of thymocyte-activating factor by human gingival fibroblasts and its autoregulatory effect on their proliferation. Infect Immun. 1987 Apr;55(4):947–954. doi: 10.1128/iai.55.4.947-954.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pulford K. A., Rigney E. M., Micklem K. J., Jones M., Stross W. P., Gatter K. C., Mason D. Y. KP1: a new monoclonal antibody that detects a monocyte/macrophage associated antigen in routinely processed tissue sections. J Clin Pathol. 1989 Apr;42(4):414–421. doi: 10.1136/jcp.42.4.414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Richards D., Rutherford R. B. The effects of interleukin 1 on collagenolytic activity and prostaglandin-E secretion by human periodontal-ligament and gingival fibroblast. Arch Oral Biol. 1988;33(4):237–243. doi: 10.1016/0003-9969(88)90184-7. [DOI] [PubMed] [Google Scholar]
  27. Seymour G. J., Greenspan J. S. The phenotypic characterization of lymphocyte subpopulations in established human periodontal disease. J Periodontal Res. 1979 Jan;14(1):39–46. doi: 10.1111/j.1600-0765.1979.tb00216.x. [DOI] [PubMed] [Google Scholar]
  28. Turner M., Chantry D., Buchan G., Barrett K., Feldmann M. Regulation of expression of human IL-1 alpha and IL-1 beta genes. J Immunol. 1989 Dec 1;143(11):3556–3561. [PubMed] [Google Scholar]
  29. di Giovine F. S., Duff G. W. Interleukin 1: the first interleukin. Immunol Today. 1990 Jan;11(1):13–20. doi: 10.1016/0167-5699(90)90005-t. [DOI] [PubMed] [Google Scholar]

Articles from The American Journal of Pathology are provided here courtesy of American Society for Investigative Pathology

RESOURCES