Taeseung Lee, MD, Nowokere Esemuede, MD, Bauer E

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Thrombospondin-1 induces matrix metalloproteinase-2 activation in vascular smooth muscle cells1 Taeseung Lee, MD, Nowokere Esemuede, MD, Bauer E. Sumpio, MD, PhD, Vivian Gahtan, MD Journal of Vascular Surgery Volume 38, Issue 1, Pages 147-154 (July 2003) DOI: 10.1016/S0741-5214(02)75468-2

Fig 1 TSP-1 upregulates pro-MMP2. VSMCs were seeded in plates and cultured in 10% FBS for 48 hours, then incubated for 24 hours in SFM. Subsequently, the medium was changed with SFM with or without TSP-1 (20 μg/mL). At indicated time points (1, 4, 24 hours), 30 μL aliquots were collected and analyzed with gelatin zymography. TSP-1 induced more pro-MMP2 activation at 1 and 4 hours compared with their respective negative controls. Journal of Vascular Surgery 2003 38, 147-154DOI: (10.1016/S0741-5214(02)75468-2)

Fig 2 TSP-1 increases MMP2 activation during VSMC invasion. A, A modified Boyden chamber was used. The porous membrane separating the two chambers was coated with Matrigel. VSMCs were stimulated with TSP-1 (20 μg/mL) or TSP-1 with TNF-α (10 ng/mL) in the upper well (18 hours) and 10% FBS in the lower well (chemoattractant). Zymography demonstrated gelatinolytic activity of MMP2 in media obtained from the upper well in the TSP-1 with or without TNF-α groups. B, Findings are summarized for a representative invasion assay (N = 3). TSP-1 with or without TNF-α induced more invasion than SFM alone (P < .05). No significant difference was noted between TSP-1 and TSP-1 with TNF-α. ∗P< .05 in comparison with negative control (SFM). Journal of Vascular Surgery 2003 38, 147-154DOI: (10.1016/S0741-5214(02)75468-2)

Fig 3 TSP-1 increases MMP2 mRNA levels. A, Representative Northern blot demonstrates that after 1 hour of exposure TSP-1 (10 and 20 μg/mL) and PDGF-BB (10 ng/mL) induce upregulation of MMP2 steady-state mRNA. B, Densitometric analysis of three independent experiments demonstrates that upregulation of MMP2 steady-state mRNA occurred in groups exposed to TSP-1 (10 or 20 μg/mL) or PDGF-BB (10 ng/mL). There was no significant difference for degree of upregulation by the three groups in comparison with SFM alone. ∗P < .05 in comparison with negative control (SFM). C, Representative Northern blot indicates that TSP-1-induced upregulation of MMP2 mRNA increases over the times measured (1, 4, 24 hours). Journal of Vascular Surgery 2003 38, 147-154DOI: (10.1016/S0741-5214(02)75468-2)

Fig 4 GM6001 inhibits TSP-1-induced VSMC invasion of membrane. A, TSP-1-stimulated VSMCs (5×; 105), suspended in DMEM containing 0.1% BSA, were added to upper chamber. Migrated VSMCs through Matrigel were stained with hematoxylin (200×). B, GM6001 (MMP inhibitor)-pretreated VSMCs were used instead in upper chamber. Fewer cells migrated in the GM 6001-pretreated group. Journal of Vascular Surgery 2003 38, 147-154DOI: (10.1016/S0741-5214(02)75468-2)

Fig 5 MMPs are required for TSP-1-induced chemoinvasiveness, not chemotaxis. Bar graphs show effect of GM6001 on chemoinvasion and chemotaxis of TSP-1-stimulated VSMCs. A, VSMCs with or without GM6001 were placed in top chamber containing TSP-1. Bottom chamber contained 10% FBS with 0.1% BSA. Membrane separating the two chambers was coated with Matrigel. Presence of GM6001 in the upper well prevented invasion of TSP-1-stimulated VSMCs. GM6001 in the bottom chamber had no significant effect on invasion. ∗P < .05 in comparison with respective negative controls. B, Chemotaxis was measured in absence of a matrix barrier. MMP inhibition (GM6001) did not affect VSMC chemotaxis. Journal of Vascular Surgery 2003 38, 147-154DOI: (10.1016/S0741-5214(02)75468-2)

Fig 6 TSP-1 binds MMP2. MMP2 (50 nmol/L) was pretreated with amino-phenylmercuric acetate and incubated overnight (4°C) in wells coated with BSA, TSP-1, or type I collagen (positive control, 50 μg). Soluble enzyme was removed (designated “soluble”). After washing wells with assay buffer, bound enzyme was eluted with two different techniques: bound enzyme was eluted with nonreducing Laemmli sample buffer (50 μg, designated “bound”) and analyzed with gelatin zymography; and bound enzyme was eluted with reducing Laemmli sample buffer (50 μg, designated “bound”) and analyzed with Western blot. Both techniques demonstrated that TSP-1 binds MMP2. BSA, TSP-1, and type I collagen upregulated pro-MMP2 and MMP2 when analyzing the soluble forms. Journal of Vascular Surgery 2003 38, 147-154DOI: (10.1016/S0741-5214(02)75468-2)

Fig 7 TSP-1 preferentially binds MMP2. To quantify activity of MMP2 bound to ECM proteins, MMP2 (10 nmol/L) was incubated overnight (4°C) in wells coated with BSA, TSP-1, elastin, type 1 collagen, or fibronectin. After analysis, MMP2 was eluted with reducing Laemmli sample buffer (50 μg, designated “bound”) and analyzed with gelatin zymography. TSP-1 had a stronger binding affinity for MMP2 than did other ECM proteins studied. Journal of Vascular Surgery 2003 38, 147-154DOI: (10.1016/S0741-5214(02)75468-2)