Clinical & Experimental Metastasis

, Volume 14, Issue 1, pp 3–11 | Cite as

Metastatic colorectal cancer cells induce matrix metalloproteinase release by human monocytes

  • Carol J. Swallow
  • Melissa P. Murray
  • José G. Guillem
Research Papers

Abstract

Matrix metalloproteinases-2 (MMP-2) and -9 (MMP-9) facilitate tumor invasion and metastasis via basement membrane degradation. In colorectal cancer (CRC) specimens, MMP production is largely stromal in origin, implicating monocytes (Mϕs) and fibroblasts. We hypothesize that CRC cells induce stromal cell MMP production. This study examines the differential effect of metastatic and non-metastatic CRC cells on Mϕ MMP production. The human Mϕ line THP-1 was co-cultured with either a non-metastatic human CRC cell line (SW620-P) or a metastatic clone (SW620-S5) established by serial cecal transplantation of SW620-P in nude mice. Conditioned medium MMP activity and cellular MMP mRNA expression were assessed by gelatinase zymography and Northern blot analysis, respectively. Neither CRC line released MMP-2 or MMP-9. Isolated THP-1 Mϕs produced basal levels of both MMP-2 and MMP-9. The level of MMP-9 activity was increased moderately by co-culture of Mϕs with the metastatic SW620-S5 clone, but decreased by the non-metastatic SW620-P cells. MMP-2 activity was greatly augmented by co-culturing Mϕs with SW620-S5 cells, but was not affected by SW620-P cells. The stimulatory effect of SW620-S5 cells on MMP-2 secretion was confirmed by Western blot analysis. Both isolated and co-cultured (Mϕs) expressed MMP-2 mRNA while SW620-S5 cells under similar conditions did not, implicating Mϕs as the source of increased MMP-2 activity. Since the induction of MMP-2 activity was not associated with a parallel increase in Mϕ MMP-2 mRNA, the modulation of Mϕ MMP-2 release appears to be post-transcriptionally regulated. Metastatic CRC cells are distinct from non-metastatic cells in their ability to induce Mϕ MMP release. This observation emphasizes the role of Mϕ-derived MMPs in facilitating CRC invasion and metastasis and suggests modulation of stromal cell MMP production by CRC cells in a paracrine fashion.

Keywords

colorectal cancer metalloproteinase metastasis monocyte/macrophage 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Steele Jr G, 1995, Advances in the treatment of early- to late-stage colorectal cancer: 20 years of progress. Ann Surg Oncol, 2, 77–88;PubMedCrossRefGoogle Scholar
  2. 2.
    Mareel MM, De Bastelier P and Van Roy FM, 1991, Mechanisms of Invasion and Metastasis. Florida: CRC Press.Google Scholar
  3. 3.
    Matrisian LM, 1992, The matrix-degrading metalloproteinases. Bio Essays, 14, 455–63.Google Scholar
  4. 4.
    Cottam DW and Rees RC, 1993, Regulation of matrix metalloproteinases: their role in tumor invasion and metastasis (Review). Int J Surg Oncol,2, 861–72.Google Scholar
  5. 5.
    Murphy G, Reynolds JJ and Hembry RM, 1989, Metalloproteinases and cancer invasion and metastasis. Int J Cancer, 44, 757–60.PubMedGoogle Scholar
  6. 6.
    Liotta LA, Trypvasson K, Garbisa S, Hart IR, Folts CM and Shafie S, 1980, Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature, 284, 67–8.PubMedCrossRefGoogle Scholar
  7. 7.
    Nakajima M, Welch DR, Belloni PN and Nicholson GL, 1987, Degradation of basement membrane type IV collagen and lung subendothelial matrix by rat mammary adenocarcinoma cell clones of differing metastatic potentials. Cancer Res, 47, 4869–76.PubMedGoogle Scholar
  8. 8.
    Bernhard EJ, Gruber SB and Muschel RJ, 1994, Direct evidence linking expression of matrix metalloproteinase 9 (92-kDa gelatinase/collagenase) to the metastatic phenotype in transformed rat embryo cells. Proc Natl Acad Sci USA, 91, 4293–7.PubMedCrossRefGoogle Scholar
  9. 9.
    Baker T, Tickle S, Wasan H, Docherty A, Isenberg D and Waxman J, 1994, Serum metal Ioproteinases and their inhibitors: markers for malignant potential. Br J Cancer, 70, 506–12.PubMedGoogle Scholar
  10. 10.
    Van Der Stappen JWJ, Hendricks T and Wobbes T, 1990, Correlation between collagenolytic activity and grade of histological differentiation in colorectal tumors. Int J Cancer, 45, 1071–8.PubMedGoogle Scholar
  11. 11.
    Levy A, Cioce V, Sobel ME, et al. 1991, Increased expression of the 72,000 type IV collagenase in human colonic adenocarcinoma. Cancer Res, 51, 439–44.PubMedGoogle Scholar
  12. 12.
    Zucker S, Lysik RM, Zarrabi MH and Moll U, 1993, M r 92,000 type IV collagenase is increased in plasma of patients with colon cancer and breast cancer. Cancer Res, 53, 140–6.PubMedGoogle Scholar
  13. 13.
    Hyuga S, Nishikawa Y, Sakata K, et al. 1994, Autocrine factor enhancing the secretion of M r 95,000 gelatinase (matrix metalloproteinase 9) in serum-free medium conditioned with murine metastatic colon carcinoma cells. Cancer Res, 54, 3611–16.PubMedGoogle Scholar
  14. 14.
    Danø K, Oronsky A and Gjedde S, 1978, Proteases from cultured malignant cells. In: Magnusson S, Ottesen M, Foltmann B, Danø K, Neurath H, eds. Regulatory Proteolytic Enzymes and their Inhibitors. Oxford: Pergamon Press, pp. 113–25.Google Scholar
  15. 15.
    Monteagudo C, Merino MJ, San-Juan J, Liotta LA and Stetler-Steveson WG, 1990, Immunohistochemical distribution of type IV collagenase in normal, benign, and malignant breast tissue. Am J Pathol, 36, 585–92.Google Scholar
  16. 16.
    Pyke C, Ralfkiaer E, Tryggvason K and Danø K, 1993, Messenger RNA for two type IV collagenases is located in stromal cells in human colon cancer. Am J Pathol, 142, 359–65.PubMedGoogle Scholar
  17. 17.
    Kuranami M, Cohen AM and Guillem JG, 1994, Production of metalloproteinase-2 (MMP-2) in metastatic colorectal cancer (CRC) is stromal in origin. Surgical Forum, 45, 551–3.Google Scholar
  18. 18.
    Poulsom R, Pignatelli M, Stetler-Stevenson WG, et al. 1992, Stromal expression of 72 kDa type IV collagenase (MMP-2) and TIMP-2 mRNAs in colorectal neoplasia. Am J Pathol, 141, 389–96.PubMedGoogle Scholar
  19. 19.
    Zeng ZS and Guillem JG, 1995, Distinct pattern of matrix metalloproteinase-9 and tisssue inhibitor of metalloproteinase-1 mRNA expression in human colorectal cancer and liver metastases. Br J Cancer, 72, 575–82.PubMedGoogle Scholar
  20. 20.
    Campbell EJ, Cury JD, Shapiro SD, Goldberg GI and Welgus HG, 1991, Neutral proteinases of human mononuclear phagocytes. Cellular differentiation markedly alters cell phenotype for serine proteinases, metalloproteinases and tissue inhibitor of metalloproteinases. J Immunol, 146, 1286–93.PubMedGoogle Scholar
  21. 21.
    Welgus HG, Campbell EJ, Cury JD, et al. 1990, Neutral metalloproteinases produced by human mononuclear phagocytes. Enzyme profile, regulation, and expression during cellular development. J Clin Invest, 86, 1496–502.PubMedGoogle Scholar
  22. 22.
    Lacraz S, Isler P, Vey E, Welgus HG and Dayer J-M, 1994, Direct contact between T lymphocytes and monocytes is a major pathway for induction of metalloproteinase expression. J Biol Chem, 269, 22027–33.PubMedGoogle Scholar
  23. 23.
    Wahl SM, Allen JB, Weeks BS, Wong HL and Klotman PE, 1993, Transforming growth factor β enhances integrin expression and type IV collagenase secretion in human monocytes. Proc Natl Acad Sci USA, 90, 4577–81.PubMedCrossRefGoogle Scholar
  24. 24.
    Watanabe H, Nakanishi I, Yamashita K, Hayakawa T and Okada Y, 1993, Matrix metalloproteinase-9 (92 kDa gelatinase/type IV collagenase) from U937 monoblastoid cells: correlation with cellular invasion. J Cell Sci, 104, 991–9.PubMedGoogle Scholar
  25. 25.
    Kuranami M, Cohen AM and Guillem JG, 1995, Analyses of protein kinase C isoform expression in a colorectal cancer liver metastasis model. Am J Surg, 169, 57–64.PubMedCrossRefGoogle Scholar
  26. 26.
    Kleiner DE and Stetler-Stevenson WG, 1994, Quantitative zymography: detection of picogram quantities of gelatinases. Analyt Biochem, 218, 325–9.PubMedCrossRefGoogle Scholar
  27. 27.
    Laemmli UK, 1970, Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680–6.PubMedCrossRefGoogle Scholar
  28. 28.
    Chomczynski P and Saachi N, 1983, Single-step method of RNA isolation by acid guanidinium thiocyanatephenol-chloroform extraction. Analyt Biochem, 132, 6–10.CrossRefGoogle Scholar
  29. 29.
    Collier IE, Wilhelm SM, Eisen AZ, et al. 1988, H-ras oncogene-transformed human bronchial epithelial cells (TBE-1) secrete a single metalloprotease capable of degrading basement membrane collagen. J Biol Chem, 263, 6579–87.PubMedGoogle Scholar
  30. 30.
    Saarialho-Kere UK, Welgus HG and Parks WC, 1993, Distinct mechanisms regulate interstitial collagenase and 92-kDa gelatinase expression in human monocytec-like cells exposed to bacterial endotoxin. J Biol Chem, 268, 17354–61.PubMedGoogle Scholar
  31. 31.
    Lacraz S, Dayer J-M, Nicod L and Welgus HG, 1994, 1,25-Dihydroxyvitamin D3 dissociates production of interstitial collagenase and 92-kDa gelatinase in human mononuclear phagocytes. J Biol Chem, 269, 6485–90.PubMedGoogle Scholar
  32. 32.
    Himeltstein BP, Canete-Soler R, Bernhard EJ and Muschel RJ, 1994, Induction of fibroblast 92 kDa gelatinase/type IV collagenase expression by direct contact with metastasic tumor cells. J Cell Sci, 107, 477–86.Google Scholar
  33. 33.
    Hafez MM, Hsu S, Yan Z, Winawer S and Friedman E, 1992, Two roles for transforming growth factor β in colon enterocytic cell differentiation. Cell Growth Differen, 3, 753–62.Google Scholar
  34. 34.
    Lahm H, Wyniger J, Hertig S, et al. 1994, Secretion of bioactive granulocyte-macrophage colony-stimulating factor by human colorectal carcinoma cells. Cancer Res, 54, 3700–2.PubMedGoogle Scholar
  35. 35.
    Xie B, Bucana CD and Fidler IJ, 1994, Densitydependent induction of 92-kD type IV collagenase activity in cultures of A431 human epidermoid carcinoma cells. Am J Pathol, 144, 1058–67.PubMedGoogle Scholar

Copyright information

© Rapid Science Publishers 1996

Authors and Affiliations

  • Carol J. Swallow
    • 1
  • Melissa P. Murray
    • 1
  • José G. Guillem
    • 1
  1. 1.Department of SurgeryMemorial Sloan-Kettering Cancer CenterNew YorkUSA

Personalised recommendations