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Generation of Biologically Active IL-1ß by Matrix Metalloproteinases: A Novel Caspase-1-Independent Pathway of IL-1ß Processing¹

Vascular Medicine and Atherosclerosis Unit, Cardiovascular Division, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115

Biologic activity of IL-1ß requires processing of the inactive precursor, a function generally ascribed to IL-1ß-converting enzyme (caspase-1). However, alternative mechanisms of IL-1ß activation have been postulated in local inflammatory reactions. Expression of IL-1ß and matrix metalloproteinases (MMPs) frequently occurs simultaneously at sites of inflammation. We describe here that stromelysin-1 (MMP-3), as well as the gelatinases A (MMP-2) and B (MMP-9), processes recombinant human IL-1ß precursor (pIL-1ß) into biologically active forms. Detection of both pIL-1ß processing and biologic IL-1ß activity demonstrated different processing capacities of the respective MMPs. Conversion of pIL-1ß by stromelysin-1 required coincubation for at least 1 h, and biologic activity faded after 8 h to 24 h. Gelatinase A was less effective in processing pIL-1ß, requiring at least 24 h of coincubation. In contrast, gelatinase B processed pIL-1ß within minutes, resulting in immunoreactive products as well as biologic activity stable for 72 h. In addition, prolonged incubation of mature IL-1ß with stromelysin-1, and to a lesser extent also with gelatinases, but not with interstitial collagenase, resulted in the degradation of mature IL-1ß. None of the MMPs processed the second isoform of IL-1, IL-1. The present study indicates a biphasic regulation of IL-1ß activity by MMPs: a caspase-1-independent pathway of IL-1ß activation and inhibition of IL-1ß activity by degrading the mature cytokine. The balance of the respective MMPs and pIL-1ß might regulate the long term appearance of IL-1ß activity at sites of acute or chronic inflammation.

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				G. Boulday, S. Coupel, F. Coulon, J.-P. Soulillou, and B. Charreau Antigraft Antibody-Mediated Expression of Metalloproteinases on Endothelial Cells : Differential Expression of TIMP-1 and ADAM-10 Depends on Antibody Specificity and Isotype Circ. Res., March 2, 2001; 88(4): 430 - 437. [Abstract] [Full Text] [PDF]

				P. E. Van den Steen, P. Proost, A. Wuyts, J. Van Damme, and G. Opdenakker Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-alpha and leaves RANTES and MCP-2 intact Blood, October 15, 2000; 96(8): 2673 - 2681. [Abstract] [Full Text] [PDF]

				T. H. Vu and Z. Werb Matrix metalloproteinases: effectors of development and normal physiology Genes & Dev., September 1, 2000; 14(17): 2123 - 2133. [Full Text]

				A. Solomon, M. Rosenblatt, D.-Q. Li, Z. Liu, D. Monroy, Z. Ji, B. L. Lokeshwar, and S. C. Pflugfelder Doxycycline Inhibition of Interleukin-1 in the Corneal Epithelium Invest. Ophthalmol. Vis. Sci., August 1, 2000; 41(9): 2544 - 2557. [Abstract] [Full Text]

				M. Kawasaki, K. Kuwano, N. Hagimoto, T. Matsuba, R. Kunitake, T. Tanaka, T. Maeyama, and N. Hara Protection from Lethal Apoptosis in Lipopolysaccharide-Induced Acute Lung Injury in Mice by a Caspase Inhibitor Am. J. Pathol., August 1, 2000; 157(2): 597 - 603. [Abstract] [Full Text] [PDF]

				A. Pagenstecher, A. K. Stalder, C. L. Kincaid, B. Volk, and I. L. Campbell Regulation of Matrix Metalloproteinases and Their Inhibitor Genes in Lipopolysaccharide-Induced Endotoxemia in Mice Am. J. Pathol., July 1, 2000; 157(1): 197 - 210. [Abstract] [Full Text] [PDF]

				S. Gardella, C. Andrei, S. Costigliolo, L. Olcese, M. R. Zocchi, and A. Rubartelli Secretion of bioactive interleukin-1beta by dendritic cells is modulated by interaction with antigen specific T cells Blood, June 15, 2000; 95(12): 3809 - 3815. [Abstract] [Full Text] [PDF]

				L. Sobrin, Z. Liu, D. C. Monroy, A. Solomon, M. G. Selzer, B. L. Lokeshwar, and S. C. Pflugfelder Regulation of MMP-9 Activity in Human Tear Fluid and Corneal Epithelial Culture Supernatant Invest. Ophthalmol. Vis. Sci., June 1, 2000; 41(7): 1703 - 1709. [Abstract] [Full Text]

				C S SETHI, T A BAILEY, P J LUTHERT, and N H V CHONG Matrix metalloproteinase biology applied to vitreoretinal disorders Br J Ophthalmol, June 1, 2000; 84(6): 654 - 666. [Full Text]

				M. P. Pereda, M. F. Ledda, V. Goldberg, A. Chervín, G. Carrizo, H. Molina, A. Müller, U. Renner, O. Podhajcer, E. Arzt, et al. High Levels of Matrix Metalloproteinases Regulate Proliferation and Hormone Secretion in Pituitary Cells J. Clin. Endocrinol. Metab., January 1, 2000; 85(1): 263 - 269. [Abstract] [Full Text]

				C.-R. Roh, W.-J. Oh, B.-K. Yoon, and J.-H. Lee Up-regulation of matrix metalloproteinase-9 in human myometrium during labour: a cytokine-mediated process in uterine smooth muscle cells Mol. Hum. Reprod., January 1, 2000; 6(1): 96 - 102. [Abstract] [Full Text] [PDF]

				J. Zhang, A. L. Hampton, G. Nie, and L. A. Salamonsen Progesterone Inhibits Activation of Latent Matrix Metalloproteinase (MMP)-2 by Membrane-Type 1 MMP: Enzymes Coordinately Expressed in Human Endometrium Biol Reprod, January 1, 2000; 62(1): 85 - 94. [Abstract] [Full Text]

				C. Coeshott, C. Ohnemus, A. Pilyavskaya, S. Ross, M. Wieczorek, H. Kroona, A. H. Leimer, and J. Cheronis Converting enzyme-independent release of tumor necrosis factor alpha  and IL-1beta from a stimulated human monocytic cell line in the presence of activated neutrophils or purified proteinase 3 PNAS, May 25, 1999; 96(11): 6261 - 6266. [Abstract] [Full Text] [PDF]

				R. Mohan, S. K. Chintala, J. C. Jung, W. V. L. Villar, F. McCabe, L. A. Russo, Y. Lee, B. E. McCarthy, K. R. Wollenberg, J. V. Jester, et al. Matrix Metalloproteinase Gelatinase B (MMP-9) Coordinates and Effects Epithelial Regeneration J. Biol. Chem., January 11, 2002; 277(3): 2065 - 2072. [Abstract] [Full Text] [PDF]