PGE1 Inhibits the Expression of PAI-1 mRNA Induced by TNF-α in Human Mesangial Cells

M. Kishida; M. Urakaze; M. Takata; Y. Nobata; N. Yamamoto; R. Temaru; A. Sato; K. Yamazaki; N. Nakamura; M. Kobayashi

doi:10.1055/s-2005-865681

Experimental and Clinical Endocrinology & Diabetes, Table of Contents

Exp Clin Endocrinol Diabetes 2005; 113(7): 365-371
DOI: 10.1055/s-2005-865681

Article

J. A. Barth Verlag in Georg Thieme Verlag KG Stuttgart · New York

PGE1 Inhibits the Expression of PAI-1 mRNA Induced by TNF-α in Human Mesangial Cells

M. Kishida¹ , M. Urakaze¹ , M. Takata¹ , Y. Nobata¹ , N. Yamamoto¹ , R. Temaru¹ , A. Sato¹ , K. Yamazaki¹ , N. Nakamura² , M. Kobayashi¹

¹Toyama Medical and Pharmaceutical University, Faculty of Medicine, the First Department of Internal Medicine, Toyama-shi, Toyama, Japan
²Second Department of Internal Medicine, Hirosaki University School of Medicine, Hirosaki, Japan

Abstract

We examined the effect of PGE1 on the expression of plasminogen activator inhibitor-1 (PAI-1) mRNA induced by tumor necrosis factor-α (TNF-α) in human mesangial cells, because PAI-1 is one of major factors for the progression of glomerulosclerosis. The expression of PAI-1 mRNA was increased after stimulation with TNF-α, and it was diminished by pre-incubation with PGE1. Next, we examined the effect of PGE1 on the phosphorylation of mitogen activated protein kinase (MAPK) family and Akt. TNF-α activated the phosphorylation of p44/42 MAPK, p38 MAPK, SAPK/JNK and Akt in mesangial cells. PGE1 inhibited the TNF-α induced phosphorylation of SAPK/JNK and Akt, but not p44/42 MAPK and p38 MAPK. The TNF-α induced expression of PAI-1 mRNA was not affected by PD98059, an inhibitor of MEK, SB203580, an inhibitor of p38 MAPK, nor LY294002, an inhibitor of PI3 K. However, DMAP, an inhibitor of SAPK/JNK, inhibited the expression of PAI-1 mRNA, suggesting that the TNF-α induced expression of PAI-1 mRNA is regulated by the SAPK/JNK dependent pathway in human mesangial cells. By the incubation with H8, an inhibitor of PKA, the inhibitory effect of PGE1 on the expression of PAI-1 mRNA was abolished, suggesting that PGE1 inhibited the PAI-1 mRNA expression via the PKA pathway. Our results suggest that the inhibition of PAI-1 synthesis by PGE1 in human mesangial cells may have therapeutic implications for glomerulosclerosis such as occurs in diabetic nephropathy.

Key words

PGE1 - PAI-1 - TNF-α - human mesangial cells - SAPK/JNK

Full Text

References

Reference

1 Andreasen P A, George B, Lund L R, Riccio A, Stacey S N. Plasminogen activator inhibitors: hormonally regulated serpins. Mol Cell Endocrinol. 1990; 68 1-19
2 Baricos W H, Cortez S L, El-Dahr S S, Schnaper H W. ECM degradation by cultured human mesangial cells is mediated by a PA/plasmin/MMP-2 cascade. Kidney Int. 1995; 47 1039-1047
3 Boulton T G, Nye S H, Robbins D J, Ip N Y, Radziejewska E, Morgenbesser S D, DePinho R A, Panayotatos N, Cobb M H, Yancopoulos G D. ERKs: A family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell. 1991; 65 663-675
4 Brenner B M, Cooper M E, de Zeeuw D. et al . Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N Engl J Med. 2001; 345 861-869
5 Dell K, Bohler T, Gaedeke J. et al . Impact of PGE1 on cyclosporine A induced up-regulation of TGF-beta1, its receptors, and related matrix production in cultured mesangial cells. Cytokine. 2003; 22 189-193
6 Denu J M, Zhou G, Wu L, Zhao R, Yuvaniyama J, Saper M A, Dixon J E. The purification and characterization of a human dual-specific protein tyrosine phosphatase. J Biol Chem. 1995; 270 3796-3803
7 Derijard B, Hibi M, Wu I H, Barrett T, Su B, Deng T, Karin M, Davis R J. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell. 1994; 76 1025-1037
8 Ding A H, Porteu F, Sanchez E, Nathan C F. Downregulation of tumor necrosis factor receptors on macrophages and endothelial cells by microtubule depolymerizing agents. J Exp Med. 1990; 171 715-727
9 Dzurik R, Spustova V, Janekova K. The prevalence of insulin resistance in kidney disease patients before the development of renal failure. Nephron. 1995; 69 281-285
10 EUCLID study group . Randomised placebo-controlled trial of lisinopril in normotensive patients with insulin-dependent diabetes and normoalbuminuria or microalbuminuria. Lancet. 1997; 349 1787-1791
11 Freshney N W, Rawlinson L, Guesdon F. et al . Interleukin-1 activates a novel protein kinase cascade that results in the phosphorylation of Hsp27. Cell. 1994; 78 1039-1049
12 Groop L, Ekstrand A, Forsblom C, Widen E, Groop P H, Eriksson J. Insulin resistance, hypertension and microalbuminuria in patients with type II (non insulin-dependent) diabetes mellitus. Diabetologia. 1993; 36 642-647
13 Han J, Lee J D, Bibbs L, Ulevitch R J. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science. 1994; 265 808-811
14 Hasegawa G, Nakano K, Sawada M, Uno K, Shibayama Y, Ienaga K, Kondo M. Possible role of tumor necrosis factor and interleukin-1 in the development of diabetic nephropathy. Kidney Int. 1991; 40 1007-1012
15 Hirano T, Kashiwazaki K, Morimoto Y, Nagano S, Adachi M. Albuminuria is directly associated with increased plasma PAI-1 and factor levels in NIDDM patients. Diabetes Res Clin Pract. 1997; 36 11-18
16 Hiraoka E, Kawashima S, Takahashi T, Rikitake Y, Kitamura T, Ogawa W, Yokoyama M. TNF-α induces protein synthesis through PI3-kinase-Akt/PKB pathway in cardiac myocytes. Am J Physiol Heart Circ Physiol. 2001; 280 H1861-1868
17 Hotamisligil G S. Molecular mechanisms of insulin resistance and the role of the adipocyte. Int J Obes Relat Metab Disord. 2000; 24 (Suppl 4) S23-27
18 Itoh Y, Yasui T, Kakizawa H, Makino M, Fujisawa K, Kato T, Imamura S, Yamamoto K, Hishida H, Nakai A, Itoh M, Nagasaka A. The therapeutic effect of lipo PGE1 on diabetic neuropathy-changes in endothelin and various angiopathic factors. Prostaglandins Other Lipid Mediat. 2001; 66 221-234
19 Iwata M, Haruta T, Usui I. et al . Pioglitazone ameliorates tumor necrosis factor-alpha-induced insulin resistance by a mechanism independent of adipogenic activity of peroxisome proliferator-activated receptor-γ. Diabetes. 2001; 50 1083-1092
20 Katsuki A, Sumida Y, Murata K, Furuta M, Araki-Sasaki R, Tsuchihashi K, Hori Y, Yano Y, Gabazza E C, Adachi Y. Troglitazone reduces plasma levels of tumour necrosis factor-alpha in obese patients with type 2 diabetes. Diabetes Obes Metab. 2000; 2 189-191
21 Kreisberg J I, Ayo S H. The glomerular mesangium in diabetes mellitus. Kidney Int. 1993; 43 109-113
22 Kruithof E K. Plasminogen activator inhibitors - a review. Enzyme. 1988; 40 113-121
23 Kyriakis J M, Banerjee P, Nikolakaki E, Dai T, Rubie E A, Ahmad M F, Avruch J, Woodgett J R. The stress-activated protein kinase subfamily of c-Jun kinases. Nature. 1994; 369 156-160
24 Lee J C, Laydon J T, McDonnell P C, Gallagher T F, Kumar S, Green D, McNulty D, Blumenthal M J, Heys J R, Landvatter S W. et al . A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature. 1994; 372 739-746
25 Lewis E J, Hunsicker L G, Bain R P. et al . The effect of angiotensin-converting-enzyme inhibition on diabetic nephropathy. The Collaborative Study Group. N Eng J Med. 1993; 329 1456-1462
26 Marino M W, Dunbar J D, Wu L W, Ngaiza J R, Han H M, Guo D, Matsushita M, Nairn A C, Zhang Y, Kolesnick R, Jaffe E A, Donner D B. Inhibition of tumor necrosis factor signal transduction in endothelial cells by dimethylaminopurine. J Biol Chem. 1996; 271 28624-28629
27 Maschio G, Alberti D, Janin G. et al . Effect of the angiotensin-converting-enzyme inhibitor benazepril on the progression of chronic renal insufficiency. The Angiotensin-Converting-Enzyme Inhibition in Progressive Renal Insufficiency Study Group. N Eng J Med. 1996; 334 939-945
28 Mauer S M, Steffes M W, Ellis E N, Sutherland D ER, Brown D M, Goetz F C. Structural-functional relationships in diabetic nephropathy. J Clin Invest. 1984; 74 1143-1155
29 Meulders Q, He C J, Adida C, Peraldi M N, Schuleuning W D, Sraer J D, Rondeau E. Tumor necrosis factor α increases antifibrinolytic activity of cultured human mesangial cells. Kidney Int. 1992; 42 327-334
30 Mishima Y, Kuyama A, Tada A, Takahashi K, Ishioka T, Kibata M. Relationship between serum tumor necrosis factor-α and insulin resistance in obese men with Type 2 diabetes mellitus. Diabetes Res Clin Pract. 2001; 52 119-123
31 Nakamura T, Fukui M, Ebihara I, Osada S, Nagaoka I, Tomino Y, Koide H. mRNA expression of growth factors in glomeruli from diabetic rats. Diabetes. 1993; 42 450-456
32 Nicholas S B, Kawano Y, Wakino S, Collins A R, Hsueh W A. Expression and function of peroxisome proliferator-activated receptor-γ in mesangial cells. Hypertension. 2001; 37 722-727
33 Ninomiya Y, Arakawa M. Renal effects of prostaglandin E1 in type 2 (non-insulin-dependent) diabetic patients with subclinical nephropathy. Diabetes Res. 1989; 10 129-134
34 Niskanen L, Laakso M. Insulin resistance is related to albuminuria in patients with type II (non-insulin-dependent) diabetes mellitus. Metabolism. 1993; 42 1541-1545
35 Parving H H, Osterby R, Anderson P W, Hsueh W A. Brenner BM (ed) Brenner and Rector's The Kidney. 5th ed. Philadelphia; W. B. Saunders 1996: 1864-1883
36 Peraldi M N, Rondeau E, Medcalf R L, Hagege J, Lacave R, Delarue F, Schleuning W D, Sraer J D. Cell-specific regulation of plasminogen activator inhibitor 1 and tissue type plasminogen activator release by human kidney mesangial cells. Biochim Biophys Acta. 1992; 1134 189-196
37 Rerolle J P, Hertig A, Nguyen G. et al . Plasminogen activator inhibitor type 1 is a potential target in renal fibrogenesis. Kidney Int. 2000; 58 1841-1850
38 Pirart J. Why don't we teach and treat diabetic patients better?. Diabetes Care. 1978; 1 139-140
39 Rouse J, Cohen P, Trigon S, Morange M, Alonso-Llamazares A, Zamanillo D, Hunt T, Nebreda A R. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell. 1994; 78 1027-1037
40 Saksela O. Plasminogen activation and regulation of pericellular proteolysis. Biochim Biophys Acta. 1985; 823 35-65
41 Saksela O, Rifkin D B. Cell-associated plasminogen activation: regulation and physiological functions. Annu Rev Cell Biol. 1988; 4 93
42 Sraer J D, Kanfer A, Rondeau E, Lacave R. Glomerular hemostasis in normal and pathologic conditions. Adv Nephrol Necker Hosp. 1988; 17 27-55
43 Suzuki M, Kanazawa A, Shiba M, Kojima H, Harano Y. Insulin resistance in diabetic microangiopathies. J Diabetes Complications. 2000; 14 40-45
44 Takata M, Urakaze M, Temaru R, Yamazaki K, Nakamura N, Nobata Y, Kishida M, Sato A, Kobayashi M. Pravastatin suppresses the interleukin-8 production induced by thrombin in human aortic endothelial cells cultured with high glucose by inhibiting the p44/42 mitogen activated protein kinase. Br J Pharmcol. 2001; 134 753-762
45 Temaru R, Urakaze M, Sato A, Yamazaki K, Nakamura N, Kobayashi M. High glucose enhances the gene expression of interleukin-8 in human endothelial cells, but not in smooth muscle cells: possible role of interleukin-8 in diabetic macroangiopathy. Diabetologia. 1997; 40 610-613
46 Tomooka S, Border W A, Marshall B C, Noble N A. Glomerular matrix accumulation is linked to inhibition of the plasmin protease system. Kidney Int. 1992; 42 1462-1469
47 Tracey K J, Cerami A. Tumor necrosis factor, other cytokines and disease. Annu Rev Cell Biol. 1993; 9 317-343
48 Vassalli J D, Sappino A P, Belin D. The plasminogen activator/plasmin system. J Clin Invest. 1991; 88 1067-1072
49 Wahab N A, Mason R M. Modulation of neutral protease expression in human mesangial cells by hyperglycaemic culture. Biochem J. 1996; 320 777-783
50 Werb Z, Mainardi C L, Vater B A, Harris Jr E D. Endogenous activation of latent collagenase by rheumatoid synovial cells. N Engl J Med. 1977; 296 1017-1023
51 Wirta O R, Pasternack A I, Mustonen J T, Koivula T A, Harmoinen A. Urinary albumin excretion rate and its determinants after 6 years in non-insulin-dependent diabetic patients. Nephrol Dial Transplant. 1996; 11 449-456

MD, PhD Masaharu Urakaze

Toyama Medical and Pharmaceutical University
Faculty of Medicine
First Department of Internal Medicine

2630 Sugitani

Toyama-shi

Toyama, 930-0192

Japan

Phone: + 764347286

Fax: + 76 4 34 50 25

Email: murakaze@ms.toyama-mpu.ac.jp