Abstract
A polymerase chain reaction (PCR)-based homology cloning strategy was used to define the spectrum of stromelysin-like matrix metalloproteinases (MMPs) synthesized by cultured glomerular mesangial cells (MC). Using this technique, cDNAs encoding an unusual, truncated member of the MMP family, punctuated (putative) metalloproteinase (PUMP-1), were exclusively isolated. Incubation with the cytokines interleukin 1 and tumour necrosis factor increased the abundance of PUMP-1 mRNA in mesangial cells. The mesangial PUMP-1 mRNA is processed in a tissue-specific manner, yielding a transcript containing repeated 3'-untranslated region ATTTA motifs commonly found in cytokines with limited mRNA stability. Polyclonal antibodies prepared against the C-terminal region of the PUMP-1 protein documented release of this enzyme by cultures of cytokine-stimulated MC and permitted identification of PUMP-1-expressing mesangial cells within clinical biopsy specimens of acute glomerulonephritis. These findings represent new molecular and clinical evidence that non-malignant cells process and secrete this unusual member of the MMP family in a cytokine-mediated, tissue-specific manner. Mesangial synthesis of PUMP-1 may contribute to the progression of injury during glomerular inflammatory states.
Full text
PDF






Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Abrass C. K., Peterson C. V., Raugi G. J. Phenotypic expression of collagen types in mesangial matrix of diabetic and nondiabetic rats. Diabetes. 1988 Dec;37(12):1695–1702. doi: 10.2337/diab.37.12.1695. [DOI] [PubMed] [Google Scholar]
- Adler S., Striker L. J., Striker G. E., Perkinson D. T., Hibbert J., Couser W. G. Studies of progressive glomerular sclerosis in the rat. Am J Pathol. 1986 Jun;123(3):553–562. [PMC free article] [PubMed] [Google Scholar]
- Baricos W. H., Shah S. V. Proteolytic enzymes as mediators of glomerular injury. Kidney Int. 1991 Aug;40(2):161–173. doi: 10.1038/ki.1991.196. [DOI] [PubMed] [Google Scholar]
- Basset P., Bellocq J. P., Wolf C., Stoll I., Hutin P., Limacher J. M., Podhajcer O. L., Chenard M. P., Rio M. C., Chambon P. A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas. Nature. 1990 Dec 20;348(6303):699–704. doi: 10.1038/348699a0. [DOI] [PubMed] [Google Scholar]
- Boswell J. M., Yui M. A., Burt D. W., Kelley V. E. Increased tumor necrosis factor and IL-1 beta gene expression in the kidneys of mice with lupus nephritis. J Immunol. 1988 Nov 1;141(9):3050–3054. [PubMed] [Google Scholar]
- Bulman A. S., Heyderman E. Alkaline phosphatase for immunocytochemical labelling: problems with endogenous enzyme activity. J Clin Pathol. 1981 Dec;34(12):1349–1351. doi: 10.1136/jcp.34.12.1349. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Caput D., Beutler B., Hartog K., Thayer R., Brown-Shimer S., Cerami A. Identification of a common nucleotide sequence in the 3'-untranslated region of mRNA molecules specifying inflammatory mediators. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1670–1674. doi: 10.1073/pnas.83.6.1670. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chin J. R., Murphy G., Werb Z. Stromelysin, a connective tissue-degrading metalloendopeptidase secreted by stimulated rabbit synovial fibroblasts in parallel with collagenase. Biosynthesis, isolation, characterization, and substrates. J Biol Chem. 1985 Oct 5;260(22):12367–12376. [PubMed] [Google Scholar]
- Collier I. E., Wilhelm S. M., Eisen A. Z., Marmer B. L., Grant G. A., Seltzer J. L., Kronberger A., He C. S., Bauer E. A., Goldberg G. I. H-ras oncogene-transformed human bronchial epithelial cells (TBE-1) secrete a single metalloprotease capable of degrading basement membrane collagen. J Biol Chem. 1988 May 15;263(14):6579–6587. [PubMed] [Google Scholar]
- Davies M., Coles G. A., Thomas G. J., Martin J., Lovett D. H. Proteinases and the glomerulus: their role in glomerular diseases. Klin Wochenschr. 1990 Nov 16;68(22):1145–1149. doi: 10.1007/BF01798066. [DOI] [PubMed] [Google Scholar]
- Davies M., Thomas G. J., Martin J., Lovett D. H. The purification and characterization of a glomerular-basement-membrane-degrading neutral proteinase from rat mesangial cells. Biochem J. 1988 Apr 15;251(2):419–425. doi: 10.1042/bj2510419. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Falk R. J., Scheinman J. I., Mauer S. M., Michael A. F. Polyantigenic expansion of basement membrane constituents in diabetic nephropathy. Diabetes. 1983 May;32 (Suppl 2):34–39. doi: 10.2337/diab.32.2.s34. [DOI] [PubMed] [Google Scholar]
- Fini M. E., Girard M. T. The pattern of metalloproteinase expression by corneal fibroblasts is altered by passage in cell culture. J Cell Sci. 1990 Oct;97(Pt 2):373–383. doi: 10.1242/jcs.97.2.373. [DOI] [PubMed] [Google Scholar]
- Green N., Alexander H., Olson A., Alexander S., Shinnick T. M., Sutcliffe J. G., Lerner R. A. Immunogenic structure of the influenza virus hemagglutinin. Cell. 1982 Mar;28(3):477–487. doi: 10.1016/0092-8674(82)90202-1. [DOI] [PubMed] [Google Scholar]
- Hopp T. P. Protein surface analysis. Methods for identifying antigenic determinants and other interaction sites. J Immunol Methods. 1986 Apr 3;88(1):1–18. doi: 10.1016/0022-1759(86)90045-1. [DOI] [PubMed] [Google Scholar]
- Hughes K. T., Coles G. A., Harry T. R., Davies M. Some properties of human blood monocyte cell lysate neutral proteinase(s). Biochim Biophys Acta. 1981 Nov 13;662(1):111–118. doi: 10.1016/0005-2744(81)90230-8. [DOI] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Lovett D. H., Sterzel R. B., Kashgarian M., Ryan J. L. Neutral proteinase activity produced in vitro by cells of the glomerular mesangium. Kidney Int. 1983 Feb;23(2):342–349. doi: 10.1038/ki.1983.25. [DOI] [PubMed] [Google Scholar]
- MacNaul K. L., Chartrain N., Lark M., Tocci M. J., Hutchinson N. I. Discoordinate expression of stromelysin, collagenase, and tissue inhibitor of metalloproteinases-1 in rheumatoid human synovial fibroblasts. Synergistic effects of interleukin-1 and tumor necrosis factor-alpha on stromelysin expression. J Biol Chem. 1990 Oct 5;265(28):17238–17245. [PubMed] [Google Scholar]
- Martin J., Davies M., Thomas G., Lovett D. H. Human mesangial cells secrete a GBM-degrading neutral proteinase and a specific inhibitor. Kidney Int. 1989 Nov;36(5):790–801. doi: 10.1038/ki.1989.264. [DOI] [PubMed] [Google Scholar]
- Matsumoto K., Dowling J., Atkins R. C. Production of interleukin 1 in glomerular cell cultures from patients with rapidly progressive crescentic glomerulonephritis. Am J Nephrol. 1988;8(6):463–470. doi: 10.1159/000167656. [DOI] [PubMed] [Google Scholar]
- Mené P., Simonson M. S., Dunn M. J. Physiology of the mesangial cell. Physiol Rev. 1989 Oct;69(4):1347–1424. doi: 10.1152/physrev.1989.69.4.1347. [DOI] [PubMed] [Google Scholar]
- Michael A. F., Falk R. J., Platt J. L., Melvin T., Yang J. Y. Antigens of the human glomerulus. Adv Nephrol Necker Hosp. 1984;13:203–218. [PubMed] [Google Scholar]
- Miyazaki K., Hattori Y., Umenishi F., Yasumitsu H., Umeda M. Purification and characterization of extracellular matrix-degrading metalloproteinase, matrin (pump-1), secreted from human rectal carcinoma cell line. Cancer Res. 1990 Dec 15;50(24):7758–7764. [PubMed] [Google Scholar]
- Monga G., Mazzucco G., di Belgiojoso G. B., Busnach G. The presence and possible role of monocyte infiltration in human chronic proliferative glomerulonephritides. Light microscopic, immunofluorescence, and histochemical correlations. Am J Pathol. 1979 Feb;94(2):271–284. [PMC free article] [PubMed] [Google Scholar]
- Morel-Maroger Striker L., Killen P. D., Chi E., Striker G. E. The composition of glomerulosclerosis. I. Studies in focal sclerosis, crescentic glomerulonephritis, and membranoproliferative glomerulonephritis. Lab Invest. 1984 Aug;51(2):181–192. [PubMed] [Google Scholar]
- Muller D., Quantin B., Gesnel M. C., Millon-Collard R., Abecassis J., Breathnach R. The collagenase gene family in humans consists of at least four members. Biochem J. 1988 Jul 1;253(1):187–192. doi: 10.1042/bj2530187. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Murphy G., Cockett M. I., Ward R. V., Docherty A. J. Matrix metalloproteinase degradation of elastin, type IV collagen and proteoglycan. A quantitative comparison of the activities of 95 kDa and 72 kDa gelatinases, stromelysins-1 and -2 and punctuated metalloproteinase (PUMP). Biochem J. 1991 Jul 1;277(Pt 1):277–279. doi: 10.1042/bj2770277. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Quantin B., Murphy G., Breathnach R. Pump-1 cDNA codes for a protein with characteristics similar to those of classical collagenase family members. Biochemistry. 1989 Jun 27;28(13):5327–5334. doi: 10.1021/bi00439a004. [DOI] [PubMed] [Google Scholar]
- Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shaw G., Kamen R. A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell. 1986 Aug 29;46(5):659–667. doi: 10.1016/0092-8674(86)90341-7. [DOI] [PubMed] [Google Scholar]
- Sirum K. L., Brinckerhoff C. E. Cloning of the genes for human stromelysin and stromelysin 2: differential expression in rheumatoid synovial fibroblasts. Biochemistry. 1989 Oct 31;28(22):8691–8698. doi: 10.1021/bi00448a004. [DOI] [PubMed] [Google Scholar]
- Thomas G. J., Mason R. M., Davies M. Characterization of proteoglycans synthesized by human adult glomerular mesangial cells in culture. Biochem J. 1991 Jul 1;277(Pt 1):81–88. doi: 10.1042/bj2770081. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Welling G. W., Weijer W. J., van der Zee R., Welling-Wester S. Prediction of sequential antigenic regions in proteins. FEBS Lett. 1985 Sep 2;188(2):215–218. doi: 10.1016/0014-5793(85)80374-4. [DOI] [PubMed] [Google Scholar]
- Wilhelm S. M., Collier I. E., Kronberger A., Eisen A. Z., Marmer B. L., Grant G. A., Bauer E. A., Goldberg G. I. Human skin fibroblast stromelysin: structure, glycosylation, substrate specificity, and differential expression in normal and tumorigenic cells. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6725–6729. doi: 10.1073/pnas.84.19.6725. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Woessner J. F., Jr, Taplin C. J. Purification and properties of a small latent matrix metalloproteinase of the rat uterus. J Biol Chem. 1988 Nov 15;263(32):16918–16925. [PubMed] [Google Scholar]