Matrix metalloproteinases and tissue inhibitors of metalloproteinases in human gliomas

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✓ The gene expression of five matrix metalloproteinases (MMPs) and two tissue inhibitors of metalloproteinases (TIMPs) was studied in human gliomas in vivo and in vitro to evaluate their roles in glioma invasion. Simultaneous expression of one to four MMP genes and two TIMP genes was found in 17 surgical glioma specimens, and one MMP (gelatinase A) gene and two TIMP genes were simultaneously expressed in tissue of three brains. The concomitant overexpression of gelatinase A, gelatinase B, and occasional matrilysin genes was associated with the malignancy of gliomas and accompanied by overexpression of the TIMP-1 gene. In five human glioma cell lines, gelatinase A, TIMP-1, and TIMP-2 genes were constitutively expressed in all cell lines: the matrilysin gene in three cell lines; the stromelysin gene in two cell lines; and the interstitial collagenase gene in one cell line. There was a clear difference in the expression of gelatinase B and stromelysin genes between surgical glioma specimens and glioma cell lines: the gelatinase B gene was not expressed constitutively in vitro but was overexpressed in vivo, whereas the stromelysin gene was not expressed in vivo but was expressed in some cell lines. To find the cause of that difference in vivo and in vitro, the transcriptional regulations of MMP and TIMP genes by tumor promoter, growth factors, or cytokines were studied in vitro. Interstitial collagenase, gelatinase B, stromelysin, and TIMP-1 genes were upregulated in many cell lines by phorbol-12-myristate-13-acetate (PMA) and in some cell lines by epidermal growth factor, tumor necrosis factor-α, or interleukin-1β. Transforming growth factor-β1 (TGFβ1) upregulated gelatinase A and matrilysin genes in some cell lines, and there were no clear responses from any MMP and TIMP genes to interleukin-6. Thus, the transcriptional modulation of MMP genes by these growth factors and cytokines seemed insufficient to explain the difference in gelatinase B and stromelysin gene expressionsin vivo and in vitro and was suggestive of the genetic alteration of glioma cells in vitro, the heterogeneous cell population in glioma tissues, or both. Furthermore, the in vitro invasion of glioma cells through Matrigel in response to PMA, TGFβ1, or TIMP-1 was assessed by chemoinvasion assay. In most cell lines, invasion was significantly stimulated by PMA or TGFβ1 but suppressed by TIMP-1. These in vivo and in vitro studies are strongly suggestive of the important roles of some MMPs, especially gelatinase A, gelatinase B, and matrilysin, in the glioma invasion.

Article Information

Address reprint requests to: Eiichi Tani, M.D., Department of Neurosurgery, Hyogo College of Medicine, 1–1 Mukogawa-cho, Nishinomiya, Hyogo 663, Japan.

© AANS, except where prohibited by US copyright law.

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    Representative Northern blot analysis. Total cellular RNA was isolated from surgical specimens of three human brain tissues and 17 human gliomas (A) as well as from five human glioma cell lines (GB-1, U-373MG, A-172, T98G, and U-87MG) (B) and hybridized with 32P-labeled complementary DNA probes of interstitial collagenase (MMP-1), gelatinase A (MMP-2), gelatinase B (MMP-9), stromelysin (MMP-3), matrilysin (MMP-7), tissue inhibitor of metalloproteinases (TIMP)-1, and TIMP-2. Representative ethidium bromide-stained gels (ribosomal (r)RNA) are shown to allow comparison of the total amount of RNA per sample. Ribosomal RNA is used as the size standard. Arrowheads on TIMP-2 Northern blots show 3.5-, 2.3-, 1.5-, and 1.0-kb transcripts. A: Lanes 1 to 3 = brain tissues; Lanes 4 and 5 = primary astrocytomas; Lanes 6 to 8 = primary anaplastic astrocytomas; Lane 9 = recurrent anaplastic astrocytoma; Lanes 10 to 18 = primary glioblastomas; and Lanes 19 and 20 = recurrent glioblastomas. B: Lane 1 = GB-1; Lane 2 = U-373MG; Lane 3 = A-172; Lane 4 = T98G; and Lane 5 = U-87MG. MMP = matrix metalloproteinase.

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    Bar graph displaying the mean radioactivities of Northern blots of interstitial collagenase (MMP-1), gelatinase A (MMP-2), gelatinase B (MMP-9), stromelysin (MMP-3), matrilysin (MMP-7), tissue inhibitor of metalloproteinases (TIMP)-1, and TIMP-2 in three human brain tissues and 14 nonrecurrent human gliomas. Each bar shows mean ± standard deviation. MMP = matrix metalloproteinase. In each MMP and TIMP section, 1 = brain tissue; 2 = astrocytoma; 3 = anaplastic astrocytoma; 4 = glioblastoma. *p < 0.05 between brain tissue and anaplastic astrocytoma or glioblastoma; p < 0.05 between glioblastoma and astrocytoma or anaplastic astrocytoma.

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    Representative Northern blot responses of MMP and TIMP genes to agents. Total cellular RNA was isolated from five human glioma cell lines (GB-1, U-373MG, A-172, T98G, and U-87MG) and hybridized with 32P-labeled complementary DNA probe of interstitial collagenase (MMP-1) (A), gelatinase A (MMP-2) (B), gelatinase B (MMP-9) (C), stromelysin (MMP-3) (D), matrilysin (MMP-7) (E), tissue inhibitor of metalloproteinases (TIMP)-1 (F), or TIMP-2 (G). Northern blot analyses after treatment without and with phorbol-12-myristate-13-acetate (PMA) or transforming growth factor (TGF)-β1 were conducted together, whereas analyses after treatment without and with tumor necrosis factor (TNF)-α, epidermal growth factor (EGF), interleukin (IL)-1β or IL-6 were done separately from each other. Ribosomal RNA was used as the size standard. The upper thick bands (arrows) in B in Lanes TNFα, EGF, IL-1β, and IL-6 in the GB-1 and U-373MG cells show 28S ribosomal RNA. Representative ethidium bromide—stained gels (H) are shown to allow comparison of the total amount of RNA per sample. MMP = matrix metalloproteinase; Lane PMA • TGFβ1 (−) = no treatment with PMA or TGFβ1 for 24 hours; Lane PMA(+) = treatment with 10 ng/ml PMA for 24 hours; Lane TGFβ1 (+) = treatment with 5 ng/ml TGFβ1 for 24 hours; Lanes TNFα(−) and (+) = treatment without and with 10 ng/ml TNFα, respectively, for 24 hours; Lanes EGF(−) and (+) = treatment without and with 20 ng/ml EGF, respectively, for 16 hours; Lanes IL-1β(−) and (+) = treatment without and with 2.5 ng/ml IL-1β, respectively, for 10 hours; Lanes IL-6(−) and (+) in A, C, D, and E = treatment without and with 50 ng/ml IL-6, respectively, for 4 hours; Lanes IL-6(−) and (+) in B, F, and G = treatment without and with 50 ng/ml IL-6, respectively, for 24 hours; Lanes IL-6(−) 4h and IL-6(+) 4h in H = treatment without and with 50 ng/ml IL-6, respectively, for 4 hours; Lanes IL-6(−) 24h and IL-6(+) 24h in H = treatment without and with 50 ng/ml IL-6, respectively, for 24 hours.

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    Representative photomicrographs showing invading GB-1 glioma cells that were untreated (A) or treated with 10 ng/ml of phorbol-12-myristate-13-acetate (B) or 5 ng/ml of transforming growth factor-β1 (C) for 24 hours. The cells migrated through Matrigel were stained with Giemsa and shown to protrude from a porous filter(arrows). Original magnification × 100.

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    Bar graphs showing the effects of treatment with 10 ng/ml phorbol-12-myristate-13-acetate (PMA), 5 ng/ml of transforming growth factor (TGF)-β1, or 3 to 10 µg/ml tissue inhibitor of metalloproteinases (TIMP)-1, for 24 hours on the chemoinvasiveness of human glioma cell lines (GB-1, U-373MG, A-172, T98G and U-87MG). The migrated cells through the porous filter were stained with Giemsa and counted under a microscope. Each bar shows mean ± standard deviation cell numbers. A: Treatment with PMA or TGFβ1. B: Treatment with TIMP-1. *p < 0.001, **p < 0.005; p < 0.01; and ¶ ¶p < 0.05 compared to the no treatment group.

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