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. 1996 Apr;64(4):1426–1431. doi: 10.1128/iai.64.4.1426-1431.1996

Lipoteichoic acid and interleukin 1 stimulate synergistically production of hepatocyte growth factor (scatter factor) in human gingival fibroblasts in culture.

A Sugiyama 1, R Arakaki 1, T Ohnishi 1, N Arakaki 1, Y Daikuhara 1, H Takada 1
PMCID: PMC173936  PMID: 8606111

Abstract

Lipoteichoic acids (LTA) from various gram-positive bacteria, including oral streptococci such as Streptococcus sanguis, enhanced the production of hepatocyte growth factor (HGF) (scatter factor) by human gingival fibroblasts in culture, whereas lipopolysaccharides (LPS) from various gram-negative bacteria did not. In contrast, LPS induced interleukin 1 activity in human gingival epithelial cells in culture, while LTA had little effect. LTA and recombinant human interleukin 1 alpha enhanced synergistically the production of HGF/SF in human gingival fibroblast cultures. Recombinant human HGF, in turn, enhanced the proliferation of human gingival epithelial cells in culture.

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Selected References

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  1. Akira S., Isshiki H., Sugita T., Tanabe O., Kinoshita S., Nishio Y., Nakajima T., Hirano T., Kishimoto T. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J. 1990 Jun;9(6):1897–1906. doi: 10.1002/j.1460-2075.1990.tb08316.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BARTLETT G. R. Phosphorus assay in column chromatography. J Biol Chem. 1959 Mar;234(3):466–468. [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. De Kimpe S. J., Kengatharan M., Thiemermann C., Vane J. R. The cell wall components peptidoglycan and lipoteichoic acid from Staphylococcus aureus act in synergy to cause shock and multiple organ failure. Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10359–10363. doi: 10.1073/pnas.92.22.10359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dzink J. L., Socransky S. S., Haffajee A. D. The predominant cultivable microbiota of active and inactive lesions of destructive periodontal diseases. J Clin Periodontol. 1988 May;15(5):316–323. doi: 10.1111/j.1600-051x.1988.tb01590.x. [DOI] [PubMed] [Google Scholar]
  7. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  8. Fischer W., Koch H. U., Haas R. Improved preparation of lipoteichoic acids. Eur J Biochem. 1983 Jul 1;133(3):523–530. doi: 10.1111/j.1432-1033.1983.tb07495.x. [DOI] [PubMed] [Google Scholar]
  9. Fuller K., Owens J., Chambers T. J. The effect of hepatocyte growth factor on the behaviour of osteoclasts. Biochem Biophys Res Commun. 1995 Jul 17;212(2):334–340. doi: 10.1006/bbrc.1995.1974. [DOI] [PubMed] [Google Scholar]
  10. Furutani Y., Notake M., Yamayoshi M., Yamagishi J., Nomura H., Ohue M., Furuta R., Fukui T., Yamada M., Nakamura S. Cloning and characterization of the cDNAs for human and rabbit interleukin-1 precursor. Nucleic Acids Res. 1985 Aug 26;13(16):5869–5882. doi: 10.1093/nar/13.16.5869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Galanos C., Lüderitz O., Westphal O. A new method for the extraction of R lipopolysaccharides. Eur J Biochem. 1969 Jun;9(2):245–249. doi: 10.1111/j.1432-1033.1969.tb00601.x. [DOI] [PubMed] [Google Scholar]
  12. Galanos C., Lüderitz O., Westphal O. Preparation and properties of a standardized lipopolysaccharide from salmonella abortus equi (Novo-Pyrexal). Zentralbl Bakteriol Orig A. 1979 Apr;243(2-3):226–244. [PubMed] [Google Scholar]
  13. Gherardi E., Stoker M. Hepatocytes and scatter factor. Nature. 1990 Jul 19;346(6281):228–228. doi: 10.1038/346228b0. [DOI] [PubMed] [Google Scholar]
  14. Gohda E., Tsubouchi H., Nakayama H., Hirono S., Sakiyama O., Takahashi K., Miyazaki H., Hashimoto S., Daikuhara Y. Purification and partial characterization of hepatocyte growth factor from plasma of a patient with fulminant hepatic failure. J Clin Invest. 1988 Feb;81(2):414–419. doi: 10.1172/JCI113334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hardie J. M., Marsh P. D. Streptococci and the human oral flora. Soc Appl Bacteriol Symp Ser. 1978;7:157–206. [PubMed] [Google Scholar]
  16. Hattori M., Abraham L. J., Northemann W., Fey G. H. Acute-phase reaction induces a specific complex between hepatic nuclear proteins and the interleukin 6 response element of the rat alpha 2-macroglobulin gene. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2364–2368. doi: 10.1073/pnas.87.6.2364. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Igawa T., Kanda S., Kanetake H., Saitoh Y., Ichihara A., Tomita Y., Nakamura T. Hepatocyte growth factor is a potent mitogen for cultured rabbit renal tubular epithelial cells. Biochem Biophys Res Commun. 1991 Jan 31;174(2):831–838. doi: 10.1016/0006-291x(91)91493-v. [DOI] [PubMed] [Google Scholar]
  18. Inaba M., Koyama H., Hino M., Okuno S., Terada M., Nishizawa Y., Nishino T., Morii H. Regulation of release of hepatocyte growth factor from human promyelocytic leukemia cells, HL-60, by 1,25-dihydroxyvitamin D3, 12-O-tetradecanoylphorbol 13-acetate, and dibutyryl cyclic adenosine monophosphate. Blood. 1993 Jul 1;82(1):53–59. [PubMed] [Google Scholar]
  19. 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]
  20. Kan M., Zhang G. H., Zarnegar R., Michalopoulos G., Myoken Y., McKeehan W. L., Stevens J. I. Hepatocyte growth factor/hepatopoietin A stimulates the growth of rat kidney proximal tubule epithelial cells (RPTE), rat nonparenchymal liver cells, human melanoma cells, mouse keratinocytes and stimulates anchorage-independent growth of SV-40 transformed RPTE. Biochem Biophys Res Commun. 1991 Jan 15;174(1):331–337. doi: 10.1016/0006-291x(91)90524-b. [DOI] [PubMed] [Google Scholar]
  21. Le J., Vilcek J. Tumor necrosis factor and interleukin 1: cytokines with multiple overlapping biological activities. Lab Invest. 1987 Mar;56(3):234–248. [PubMed] [Google Scholar]
  22. Lenardo M. J., Baltimore D. NF-kappa B: a pleiotropic mediator of inducible and tissue-specific gene control. Cell. 1989 Jul 28;58(2):227–229. doi: 10.1016/0092-8674(89)90833-7. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Matsumoto K., Hashimoto K., Yoshikawa K., Nakamura T. Marked stimulation of growth and motility of human keratinocytes by hepatocyte growth factor. Exp Cell Res. 1991 Sep;196(1):114–120. doi: 10.1016/0014-4827(91)90462-4. [DOI] [PubMed] [Google Scholar]
  25. Miyazawa K., Kitamura A., Kitamura N. Structural organization and the transcription initiation site of the human hepatocyte growth factor gene. Biochemistry. 1991 Sep 24;30(38):9170–9176. doi: 10.1021/bi00102a007. [DOI] [PubMed] [Google Scholar]
  26. Miyazawa K., Tsubouchi H., Naka D., Takahashi K., Okigaki M., Arakaki N., Nakayama H., Hirono S., Sakiyama O., Takahashi K. Molecular cloning and sequence analysis of cDNA for human hepatocyte growth factor. Biochem Biophys Res Commun. 1989 Sep 15;163(2):967–973. doi: 10.1016/0006-291x(89)92316-4. [DOI] [PubMed] [Google Scholar]
  27. Montesano R., Matsumoto K., Nakamura T., Orci L. Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor. Cell. 1991 Nov 29;67(5):901–908. doi: 10.1016/0092-8674(91)90363-4. [DOI] [PubMed] [Google Scholar]
  28. Montesano R., Schaller G., Orci L. Induction of epithelial tubular morphogenesis in vitro by fibroblast-derived soluble factors. Cell. 1991 Aug 23;66(4):697–711. doi: 10.1016/0092-8674(91)90115-f. [DOI] [PubMed] [Google Scholar]
  29. Nakai S., Mizuno K., Kaneta M., Hirai Y. A simple, sensitive bioassay for the detection of interleukin-1 using human melanoma A375 cell line. Biochem Biophys Res Commun. 1988 Aug 15;154(3):1189–1196. doi: 10.1016/0006-291x(88)90266-5. [DOI] [PubMed] [Google Scholar]
  30. Obayashi T., Tamura H., Tanaka S., Ohki M., Takahashi S., Arai M., Masuda M., Kawai T. A new chromogenic endotoxin-specific assay using recombined limulus coagulation enzymes and its clinical applications. Clin Chim Acta. 1985 Jun 30;149(1):55–65. doi: 10.1016/0009-8981(85)90273-6. [DOI] [PubMed] [Google Scholar]
  31. Plaschke-Schlütter A., Behrens J., Gherardi E., Birchmeier W. Characterization of the scatter factor/hepatocyte growth factor gene promoter. Positive and negative regulatory elements direct gene expression to mesenchymal cells. J Biol Chem. 1995 Jan 13;270(2):830–836. doi: 10.1074/jbc.270.2.830. [DOI] [PubMed] [Google Scholar]
  32. Shima N., Nagao M., Ogaki F., Tsuda E., Murakami A., Higashio K. Tumor cytotoxic factor/hepatocyte growth factor from human fibroblasts: cloning of its cDNA, purification and characterization of recombinant protein. Biochem Biophys Res Commun. 1991 Oct 31;180(2):1151–1158. doi: 10.1016/s0006-291x(05)81187-8. [DOI] [PubMed] [Google Scholar]
  33. Stoker M., Gherardi E., Perryman M., Gray J. Scatter factor is a fibroblast-derived modulator of epithelial cell mobility. Nature. 1987 May 21;327(6119):239–242. doi: 10.1038/327239a0. [DOI] [PubMed] [Google Scholar]
  34. Strain A. J., Ismail T., Tsubouchi H., Arakaki N., Hishida T., Kitamura N., Daikuhara Y., McMaster P. Native and recombinant human hepatocyte growth factors are highly potent promoters of DNA synthesis in both human and rat hepatocytes. J Clin Invest. 1991 May;87(5):1853–1857. doi: 10.1172/JCI115207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Takada H., Iki K., Sakuta T., Sugiyama A., Sawamura S., Hamada S. Lipopolysaccharides of oral black pigmented bacteria and periodontal diseases. A novel immunomodulator different from endotoxin was extracted from Prevotella intermedia ATCC 25611 with hot phenol-water. Prog Clin Biol Res. 1995;392:59–68. [PubMed] [Google Scholar]
  36. Takada H., Mihara J., Morisaki I., Hamada S. Induction of interleukin-1 and -6 in human gingival fibroblast cultures stimulated with Bacteroides lipopolysaccharides. Infect Immun. 1991 Jan;59(1):295–301. doi: 10.1128/iai.59.1.295-301.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Tamura M., Arakaki N., Tsubouchi H., Takada H., Daikuhara Y. Enhancement of human hepatocyte growth factor production by interleukin-1 alpha and -1 beta and tumor necrosis factor-alpha by fibroblasts in culture. J Biol Chem. 1993 Apr 15;268(11):8140–8145. [PubMed] [Google Scholar]
  38. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tokunaga K., Nakamura Y., Sakata K., Fujimori K., Ohkubo M., Sawada K., Sakiyama S. Enhanced expression of a glyceraldehyde-3-phosphate dehydrogenase gene in human lung cancers. Cancer Res. 1987 Nov 1;47(21):5616–5619. [PubMed] [Google Scholar]
  40. Tsubouchi H., Niitani Y., Hirono S., Nakayama H., Gohda E., Arakaki N., Sakiyama O., Takahashi K., Kimoto M., Kawakami S. Levels of the human hepatocyte growth factor in serum of patients with various liver diseases determined by an enzyme-linked immunosorbent assay. Hepatology. 1991 Jan;13(1):1–5. [PubMed] [Google Scholar]
  41. Weidner K. M., Arakaki N., Hartmann G., Vandekerckhove J., Weingart S., Rieder H., Fonatsch C., Tsubouchi H., Hishida T., Daikuhara Y. Evidence for the identity of human scatter factor and human hepatocyte growth factor. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7001–7005. doi: 10.1073/pnas.88.16.7001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Yoshiyama Y., Arakaki N., Naka D., Takahashi K., Hirono S., Kondo J., Nakayama H., Gohda E., Kitamura N., Tsubouchi H. Identification of the N-terminal residue of the heavy chain of both native and recombinant human hepatocyte growth factor. Biochem Biophys Res Commun. 1991 Mar 15;175(2):660–667. doi: 10.1016/0006-291x(91)91616-k. [DOI] [PubMed] [Google Scholar]

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