Advertisement

Clinical & Experimental Metastasis

, Volume 15, Issue 6, pp 612–619 | Cite as

Increased matrix metalloproteinase-9 activity in human ovarian cancer cells cultured with conditioned medium from human peritoneal tissue

  • Kiyosumi Shibata
  • Fumitaka Kikkawa
  • Akihiko Nawa
  • Koji Tamakoshi
  • Nobuhiko Suganuma
  • Yutaka Tomoda
Article

Abstract

Ovarian cancer cells disseminate by attachment to the peritoneal mesothelial cell surface of the abdominal cavity. We therefore investigated the influence of conditioned medium (CM) from human peritoneal tissues and mesothelial cells on the secretion of matrix metalloproteinases (MMPs) by ovarian cancer cells. The molecular weights of MMPs stimulating factors derived from human peritoneal tissues and mesothelial cells were estimated using microconcentrators with various cut-off membranes. Human peritoneal tissues were obtained from 12 surgical patients, and mesothelial cells were isolated from three peritoneal specimens. Exposure to CM from peritoneal tissue caused a concentration-dependent increase of the MMP-2 and MMP-9 bands in CM from NOM1 ovarian cancer cells, as shown by zymography. There was a significant difference in the increase of MMP-2 and MMP-9 (2.46-fold and 7.14-fold, respectively, at 0.4mg/ml protein; P < 0.005). CM from mesothelial cells also significantly increased the secretion of MMP-9 by NOM1 cells. The molecular size of possible MMP-9-stimulating factors secreted by peritoneal tissues and mesothelial cells was above M 100000. Further, CM of peritoneal tissues and mesothelial cells also induced the invasiveness of NOM1 cells. These findings suggest that mesothelial cells may secrete some factors which predominantly induce the MMP-9 production and increase invading cell numbers.

invasion matrix metalloproteinase mesothelial cells ovarian cancer cells peritoneal tissue 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Mareel MM, De Baetselier P and Van Roy FM, 1991, Cellular activities implicated in invasion and metastasis. In: Mareel MM, De Baetselier P and Van Roy FM, eds. Mechanisms of Invasion and Metastasis. Boca Raton, FL: CRC Press, 73–219.Google Scholar
  2. 2.
    Liotta LA, Steeg PS and Stetler-Stevenson WG, 1991, Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell, 64, 327–36.Google Scholar
  3. 3.
    Lyons JG, Hansen BB, Pierson MC, Whitelock JM and Hansen HB, 1993, Interleukin-1β and transforming growth factor-α/epidermal growth factor induce expression of Mr 95 000 type IV collagenase/gelatinase and interstitial fibroblast-type collagenase by rat mucosal keratinocytes. J Biol Chem, 25, 19143–51.Google Scholar
  4. 4.
    Fabunmi RP, Baker AH, Murray EJ, Booth RF and Newby AC, 1996, Divergent regulation by growth factors and cytokines of 95 kDa and 72 kDa gelatinases and tissue inhibitors or metalloproteinase-1,-2,-3 in rabbit aortic smooth muscle cells. Biochem J, 315, 335–42.Google Scholar
  5. 5.
    Lengyel ER, Rebewcca GU, Juarez JO, et al.1995, Induction of Mr 92,000 type IV collagenase expression in a squamous cell carcinoma cell line by fibroblasts. Cancer Res, 55, 963–7.Google Scholar
  6. 6.
    Goldberg GI, Strongin A, Collier IE, Genrich LT and Marmer BL, 1992, Interaction of 92-kDa type IV collagenase with the tissue inhibitor of metalloproteinases prevents dimerization, complex formation with interstitial collagenase, and activation of the proenzyme with stromelysin. J Biol Chem, 267, 4583–91.Google Scholar
  7. 7.
    Kurogi T, Nabeshima K, Kataoka H, Okada Y and Koono M, 1996, Stimulation of gelatinase B and tissue inhibitors of metalloproteinase (TIMP) production in co-culture of human osteosarcoma cells and human fibroblasts: gelatinase B production was stimulated via up-regulation of fibroblast growth factor (FGF) receptor. Int J Cancer, 66, 82–90.Google Scholar
  8. 8.
    Himelstein BP and Muschel RJ, 1996, Induction of matrix metalloproteinase 9 expression in breast carcinoma cells by soluble factor from fibroblast. Clin Exp Metastasis, 14, 197–208.Google Scholar
  9. 9.
    Nakajima M and Chop AM, 1991, Tumor invasion and extracellular matrix degradative enzymes: regulation of activity by organ factors. Sem Cancer Biol, 2, 115–27.Google Scholar
  10. 10.
    Nakajima M, Morikawa K, Fabra A, Bucana CD and Fidler IJ, 1990, Influence of organ environment on extracellular matrix degradative activity and metastasis of human colon carcinoma cells. J Natl Cancer Inst, 82, 1890–8.Google Scholar
  11. 11.
    Fabra A, Nakajima M, Bucana CD and Fidler IJ, 1992, Modulation of the invasive phenotype of human colon carcinoma cells by organ specific fibroblasts of nude mice. Differentiation, 52, 101–10.Google Scholar
  12. 12.
    Gohji K, Nakajima M, Fabra A, et al.1994, Regulation of gelatinase production in metastatic renal cell carcinoma by organ-specific fibroblasts. Jpn J Cancer Res, 85, 152–60.Google Scholar
  13. 13.
    Gohji K, Fidler IJ, Tsan R, et al.1994, Human recombinant interferons-beta and-gamma decrease gelatinase production and invasion by human KG-2 renal-carcinoma cells. Int J Cancer, 58, 380–4.Google Scholar
  14. 14.
    Kikkawa F, Ishikawa H, Tamakoshi K, et al.1995, Prognostic evaluation of lymphadenectomy for epithelial ovarian cancer. J Surg Oncol, 60, 227–31.Google Scholar
  15. 15.
    Nicholson LJ, Clarke JM, Pittilo RM, Machin SJ and Woolf N, 1984, The mesothelial cell as a non-thrombotic surface. Tromb Haemostas, 37, 108–14.Google Scholar
  16. 16.
    Wu YU, Parker LM, Binder NE, et al.1982, The mesothelial keratins: a new family of cytoskeletal proteins identified in cultured mesothelial cells and nonkeratinizing epithelia. Cell, 31, 693–8.Google Scholar
  17. 17.
    Tamakoshi K, Kikkawa F, Nawa A, et al.1994, Different pattern of zymography between human gynecologic normal and malignant tissues. Am J Obstet Gynecol, 171, 478–84.Google Scholar
  18. 18.
    Tamakoshi K, Kikkawa F, Nawa A, et al.1995, Characterization of extracellular matrix degrading proteinases and its inhibitor in gynecologic cancer tissues with clinically different metastatic form. Cancer, 76, 2565–71.Google Scholar
  19. 19.
    Tryggvasion K, Hoyhtya M and Salo T, 1987, Proteolytic degradation of extracellular matrix in tumor invasion. Biochim Biophys Acta, 907, 191–217.Google Scholar
  20. 20.
    Murphy G, Cockett MI, Ward RV and Docherty AJ, 1991, Matrix metalloproteinase degradation of elastin, type IV collagen and proteoglycan. Biochem J, 277, 277–9.Google Scholar
  21. 21.
    Fabumi R, Baker A, Murray E, Booth R and Newby A, 1996, Divergent regulation by growth factors and cytokines of 95 kDa and 72 kDa gelatinase and tissue inhibitors or metalloproteinase-1,-2, and-3 in rabbit aortic smooth muscle cells. Biochem J, 315, 335–42.Google Scholar
  22. 22.
    Shimada I, Sasaguri Y, Kusukawa J, et al.1993, Production of matrix metalloproteinase 9 (92-kDa gelatinase) by human oesophageal squamous cell carcinoma in response to epidermal growth factor. Br J Cancer, 67, 721–7.Google Scholar
  23. 23.
    Overall CM, Wanda JL and Sodek J, 1991, Transcriptional and post-transcriptional regulation of 72-kDa gelatinase/type IV collagenase by transforming growth factor-b1 in human fibroblasts. J Biol Chem, 21, 14064–71.Google Scholar
  24. 24.
    Ito A, Nakajima S, Sasaguri Y, Nagase H and Mori Y, 1995, Co-culture of human breast adenocarcinoma MCF-7 cells and human dermal fibroblasts enhances the production of matrix metalloproteinases 1, 2 and 3 in fibroblasts. Br J Cancer, 71, 1039–45.Google Scholar
  25. 25.
    Morikawa K, Walker SM, Nakajima M, et al.1988, Influence of organ environment on the growth, selection, and metastasis of human colon carcinoma cells in nude mice. Cancer Res, 48, 6863–71.Google Scholar
  26. 26.
    Offner F, Obrist P, Stadlmann S, et al.1995, IL-6 secretion by human peritoneal and ovarian cancer cells. Cytokine, 7, 542–7.Google Scholar
  27. 27.
    Zeillermarker AM, Mul FP, Hoynck van papendrecht AA, et al.1995, Polarized secretion of interleukin-8 by human mesothelial cells: a role in neutrophile migration. Immunology, 84, 227–32.Google Scholar
  28. 28.
    Langerak AW, van-der-Linden-van-Beurden CM and Versnel MA, 1996, Regulation of differential expression of platelet-derived growth factor alpha-and betareceptor mRNA in normal and malignant human mesothelial cell lines. Biochim Biophys Acta, 1305, 63–70.Google Scholar
  29. 29.
    Cannistra SA, Ottensmeier C, Niloff J, Orta B and Dicarlo J, 1995, Expression and function of beta 1 and alpha v beta 3 integrins in ovarian cancer. Gynecol Oncol, 58, 216–25.Google Scholar
  30. 30.
    Jones LM, Gardner MJ, Catterall JB and Turner GA, 1995, Hyaluronic acid secreted by mesothelial cells: a natural barrier to ovarian cancer cell adhesion. Clin Exp Metastasis, 13, 373–80.Google Scholar
  31. 31.
    Engebraaten O, Bjerkvig R, Pedersen PH and Laerum OD, 1993, Effects of EGF, bFGF, NGF and PDGF(bb) on cell proliferative, migratory and invasive capacities of human brain-tumor biopsies in vitro. Int J Cancer, 53, 209–14.Google Scholar
  32. 32.
    Moriyama T, Kataoka H, Seguchi K, Tsubouchi H and Koono M, 1996, Effects of hepatocyte growth factor (HGF) on human glioma cells in vitro: HGF acts as a motility factor in glioma cells. Int J Cancer, 66, 678–85.Google Scholar

Copyright information

© Chapman and Hall 1997

Authors and Affiliations

  • Kiyosumi Shibata
    • 1
  • Fumitaka Kikkawa
    • 1
  • Akihiko Nawa
    • 1
  • Koji Tamakoshi
    • 1
  • Nobuhiko Suganuma
    • 1
  • Yutaka Tomoda
    • 1
  1. 1.Department of Obstetrics and GynecologyNagoya University School of MedicineNagoyaJapan

Personalised recommendations