Interleukin-1β inhibits ATP-induced protein kinase B activation in renal mesangial cells by two different mechanisms: The involvement of nitric oxide and ceramide

British Journal of Pharmacology

Volumn 138, Issue 3, 2003, Pages 461-468

  Rölz, Waltraud ^a   Xin, Cuiyan ^a   Ren, Shuyu ^a   Pfeilschifter, Josef ^a   Huwiler, Andrea ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

Ceramide; Interleukin 1; Mesangial cell; Nitric oxide; P2Y2 purinoceptor

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALYCULIN A; CERAMIDE; ENZYME INHIBITOR; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NOS2 PROTEIN, RAT; OKADAIC ACID; ONCOPROTEIN; OXAZOLE DERIVATIVE; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; 1 [(2 AMINOETHYL) N (2 AMMONIOETHYL)AMINO]DIAZEN 1 IUM 1,2 DIOLATE; 8 BROMO CYCLIC GMP; INTERLEUKIN 1BETA; N(G) METHYLARGININE; NITRIC OXIDE DONOR; NITRIC OXIDE SYNTHASE INHIBITOR; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; SPHINGOLIPID; UNCLASSIFIED DRUG;

ANIMAL; ARTICLE; BIOSYNTHESIS; CELL CULTURE; COMPARATIVE STUDY; CYTOLOGY; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ACTIVATION; ENZYME INDUCTION; MESANGIUM; METABOLISM; RAT; WESTERN BLOTTING; ANIMAL CELL; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; DRUG MECHANISM; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; INCUBATION TIME; KIDNEY CELL; MESANGIUM CELL; NONHUMAN; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CERAMIDES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME INHIBITORS; GLOMERULAR MESANGIUM; INTERLEUKIN-1; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; OKADAIC ACID; OXAZOLES; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RATS;

EID: 0037332044     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0705064     Document Type: Article

References (57)

1. ALESSI, D.R., ANDJELKOVIC, M., CAUDWELL, B., CRON, P., MORRICE, N., COHEN, P. & HEMMINGS, B.A. (1996). Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J., 15, 6541-6551.
2. ALESSI, D.R., JAMES, S.R., DOWNES, C.P., HOLMES, A.B., GAFFNEY, P.R., REESE, C.B. & COHEN, P. (1997). Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr. Biol., 7, 261-269.
3. ANDJELKOVIC, M., JAKUBOWICZ, T., CRON, P., MING, X.F., HAN, J.W. & HEMMINGS, B.A. (1996). Activation and phosphorylation of a pleckstrin homology domain containing protein kinase (RAC-PK/PKB) promoted by serum and protein phosphatase inhibitors. Proc. Natl. Acad. Sci. U.S.A., 93, 5699-5704.
4. BOARDER, M.R. & HOURANI, S.M. (1998). The regulation of vascular function by P2 receptors: multiple sites and multiple receptors. Trends Pharmacol. Sci., 19, 99-107.
5. BOURBON, N.A. SANDIRASEGARANE, L. & KESTER, M. (2002). Ceramide-induced inhibition of Akt is mediated through protein kinase Czeta: implications for growth arrest. J. Biol. Chem., 277, 3286-3292.
6. BRAZIL, D.P. & HEMMINGS, B.A. (2001). Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem. Sci., 26, 657-664.
7. BURGERING, B.M. & COFFER, P.J. (1995). Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature, 376, 599-602.
8. CALLSEN, D., SANDAU, K.B. & BRÜNE, B. (1999). Nitric oxide and superoxide inhibit platelet-derived growth factor receptor phosphotyrosine phosphatases. Free Radic. Biol. Med., 26, 1544-1553.
9. CASELLI, A., CAMICI, G., MANAO, G., MONETI, G., PAZZAGLI, L., CAPPUGI, G. & RAMPONI, G. (1994). Nitric oxide causes inactivation of the low molecular weight phosphotyrosine protein phosphatase. J. Biol. Chem., 269, 24878-24882.
10. CHAN, T.O., RITTENHOUSE, S.E. & TSICHLIS, P.N. (1999). AKT/ PKB and other D3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide-dependent phosphorylation. Annu. Rev. Biochem., 68, 965-1014.
11. COFFER, P.J. & WOODGETT, J.R. (1991). Molecular cloning and characterisation of a novel putative protein-serine kinase related to the cAMP-dependent and protein kinase C families. Eur. J. Bioehem., 201, 475-481.
12. DHAUNSI, G.S., MATTHEWS, C., KAUR, K. & HASSID, A. (1997). NO increases protein tyrosine phosphatase activity in smooth muscle cells: relationship to antimitogenesis. Am. J. Physiol., 272, H1342-H1349.
13. DINARELLO, C.A. (1998). Interleukin-1, interleukin-1 receptors and interleukin-1 receptor antagonist. Int. Rev. Immunol., 16, 457-499.
14. ESTRADA, C., GOMEZ, C., MARTIN-NIETO, J., DE FRUTOS, T., JIMENEZ, A. & VILLALOBO, A. (1997). Nitric oxide reversibly inhibits the epidermal growth factor receptor tyrosine kinase. Biochem. J., 326, 369-376.
15. FRANKE, T.F., YANG, S.I., CHAN, T.O., DATTA, K., KAZLAUSKAS, A., MORRISON, D.K., KAPLAN, D.R. & TSICHLIS, P.N. (1995). The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell, 81, 727-736.
16. FRANZEN, R., PAUTZ, A., BRÄUTIGAM, L-, GEISSLINGER, G., PFEILSCHIFTER, J. & HUWILER, A. (2001). Interleukin-1β induces chronic activation and de novo synthesis of neutral ceramidase in renal mesangial cells. J. Biol. Chem., 276, 35382-35389.
17. HONKANEN, R.E., CODISPOTI, B.A., TSE, K., BOYNTON, A.L. & HONKANEN, R. E. (1994). Characterization of natural toxins with inhibitory activity against serine/threonine protein phosphatases. Toxicon, 32, 339-350.
18. HUWILER, A. & PFEILSCHIFTER, J. (1994). Stimulation by extracellular ATP and UTP of the mitogen-activated protein kinase cascade and proliferation of rat renal mesangial cells. Br. J. Pharmacol., 113, 1455-1463.
19. HUWILER, A., BRUNNER, J., HUMMEL, R., VERVOORDELDONK, M., STABEL, S., VAN DEN BOSCH, H. & PFEILSCHIFTER, J. (1996). Ceramide-binding and activation defines protein kinase c-Raf as a ceramide-activated protein kinase. Proc. Natl. Acad. Sci. U.S.A., 93, 6959-6963.
20. HUWILER, A., FABBRO, D. & PFEILSCHIFTER, J. (1998). Selective ceramide binding to protein kinase C-α and -δ isoenzymes in renal mesangial cells. Biochemistry, 37, 14556-14562.
21. HUWILER, A., KOLTER, T., PFEILSCHIFTER, J. & SANDHOFF, K. (2000b). Physiology and pathophysiology of sphingolipid metabolism and signaling. Biochim. Biophys. Acta, 1485, 63-99.
22. HUWILER, A., PFEILSCHIFTER, J. & VAN DEN BOSCH, H. (1999). Nitric oxide donors induce stress signaling via ceramide formation in renal mesangial cells. J. Biol. Chem., 274, 7190-7195.
23. 2 purinoceptor in renal mesangial cells. Br. J. Pharmacol., 136, 520-529.
24. HUWILER, A., STABEL, S., FABBRO, D. & PFEILSCHIFTER, J. (1995). Platelet-derived growth factor and angiotensin II stimulate the mitogen-activated protein kinase cascade in rat renal mesangial cells. Biochem. J., 305, 777-784.
25. HUWILER, A., VAN ROSSUM, G., WARTMANN, M. & PFEILSCHIFTER, J. (1997). Stimulation by extracellular ATP and UTP of the stress-activated protein kinase cascade in rat renal mesangial cells. Br. J. Pharmacol., 120, 807-812.
26. HUWILER, A., WARTMANN, M., VAN DEN BOSCH, H. & PFEILSCHIFTER, J. (2000a). Extracellular nucleotides activate the p38-stress-activated protein kinase cascade in glomerular mesangial cells. Br. J. Pharmacol., 129, 612-618.
27. KASHGARIAN, M. & STERZEL, R.B. (1992). The pathobiology of the mesangium. Kidney Int., 41, 524-529.
28. KASZKIN, M., HUWILER, A., SCHOLZ, K., VAN DEN BOSCH, H. & PFEILSCHIFTER, J. (1998). Negative regulation of interleukin-1β-activated neutral sphingomyelinase by protein kinase C in rat mesangial cells. FEBS Lett., 440, 163-166.
29. KAUR, K., YAO, J., PAN, X., MATTHEWS, C. & HASSID, A. (1998). NO decreases phosphorylation of focal adhesion proteins via reduction of Ca in rat aortic smooth muscle cells. Am. J. Physiol., 274, H1613-H1619.
30. KUNZ, D., MÜHL, H., WALKER, G. & PFEILSCHIFTER, J. (1994). Two distinct signaling pathways trigger the expression of inducible nitric oxide synthase in rat renal mesangial cells. Proc. Natl. Acad. Sci. U.S.A., 91, 5387-5391.
31. LANDER, H.M., SEHAJPAL, P., LEVINE, D.M. & NOVOGRODSKY, A. (1993). Activation of human peripheral blood mononuclear cells by nitric oxide-generating compounds. J. Immunol., 150, 1509-1516.
32. LEUNG-HAGESTEIJN, C., MAHENDRA, A., NARUSZEWICZ, I. & HANNIGAN, G.E (2001). Modulation of integrin signal transduction by ILKAP, a protein phosphatase 2C associating with the integrin-linked kinase, ILK 1. EMBO J., 20, 2160-2170.
33. MARQUIS, J.C. & DEMPLE, B. (1998). Complex genetic response of human cells to sublethal levels of pure nitric oxide. Cancer Res., 58, 3435-3440.
34. MÜHL, H., SANDAU, K., BRÜNE, B., BRINER, V.A. & PFEILSCHIFTER, J. (1996). Nitric oxide donors induce apoptosis in glomerular mesangial cells, epithelial cells and endothelial cells. Eur. J. Pharmacol., 317, 137-149.
35. PAVENSTÄDT, H., GLOY, J., LEIPZIGER, J., KLAER, B., PFEILSCHIFTER, J., SCHOLLMEYER, P. & GREGER, R. (1993). Effect of extracellular ATP on contraction, cytosolic calcium activity, membrane voltage and ion currents of rat mesangial cells in primary culture. Br. J. Pharmacol., 109, 953-959.
36. PERANOVICH, T.M., DA SILVA, A.M., FRIES, D.M., STERN, A. & MONTEIRO, H.P. (1995). Nitric oxide stimulates tyrosine phosphorylation in murine fibroblasts in the absence and presence of epidermal growth factor. Biochem. J., 305, 613-619.
37. PERSAD, S., ATTWELL, S., GRAY, V., MAWJI, N., DENG, J.T., LEUNG, D., YAN, J., SANGHERA, J., WALSH, M.P. & DEDHAR, S. (2001). Regulation of protein kinase B/Akt-serine 473 phosphorylation by integrin-linked kinase: critical roles for kinase activity and amino acids arginine 211 and serine 343. J. Biol. Chem., 276, 27462-27469.
38. PFEILSCHIFTER, J. (1989). Cross-talk between transmembrane signalling systems: a prerequisite for the delicate regulation of glomerular haemodynamics by mesangial cells. Eur. J. Clin. Invest., 19, 347-361.
39. PFEILSCHIFTER, J. (1990a). Extracellular ATP stimulates polyphosphoinositide hydrolysis and prostaglandin synthesis in rat renal mesangial cells. Involvement of a pertussis toxin-sensitive guanine nucleotide binding protein and feedback inhibition by protein kinase C. Cell. Signal., 2, 129-138.
40. PFEILSCHIFTER, J. (1990b). Comparison of extracellular ATP and UTP signalling in rat renal mesangial cells. No indications for the involvement of separate purino- and pyrimidino-ceptors. Biochem. J., 272, 469-472.
41. PFEILSCHIFTER, J. (1994). Mesangial cells orchestrate inflammation in the renal glomerulus. News Physiol. Sci., 9, 271-276.
42. PFEILSCHIFTER, J. & HUWILER, A. (1996a). Regulatory functions of protein kinase C isoenzymes in purinoceptor signalling in mesangial cells. J. Auton. Pharmacol., 16, 315-318.
43. PFEILSCHIFTER, J. & HUWILER, A. (1996b). Nitric oxide stimulates stress-activated protein kinases in glomerular endothelial and mesangial cells. FEBS Lett., 396, 67-70.
44. PFEILSCHIFTER, J. & SCHWARZENBACH, H. (1990). Interleukin 1 and tumor necrosis factor stimulate cGMP formation in rat renal mesangial cells. FEBS Lett., 273, 185-187.
45. PFEILSCHIFTER. J., EBERHARDT, W. & HUWILER, A. (2001). Nitric oxide and mechanisms of redox signalling: matix and matrix-metabolizing enzymes as prime nitric oxide targets. Eur. J. Pharmacol. 429, 279-286.
46. PFEILSCHIFTER, J., ROB, P., MÜLSCH. A., FANDREY, J., VOSBECK, K. & BUSSE, R. (1992). Interleukin 1β and tumour necrosis factor α induce a macrophage-type of nitric oxide synthase in rat renal mesangial cells. Eur. J. Biochem., 203, 251-255.
47. RALEVIC, V. & BURNSTOCK, G. (1998). Receptors for purines and pyrimidines. Pharmacol Rev., 50, 413-492.
48. SALINAS, M., LOPEZ-VALDALISO, R., MARTIN, D., ALVAREZ, A. & CUADRADO, A. (2000). Inhibition of PKB/Aktl by C2-ceramide involves activation of ceramide-activated protein phosphatase in PC12 cells. Mol. Cell Neurosci., 15, 156-169.
49. SCHUBERT, K.M., SCHEID, M.P. & DURONIO, V. (2000). Ceramide inhibits protein kinase B/Akt by promoting dephosphorylation of serine 473. J. Biol. Chem., 275, 13330-13335.
50. SCHULZE-LOHOFF, E., ZANNER, S., OGILVIE. A. & STERZEL R.B. (1992). Extracellular ATP stimulates proliferation of cultured mesangial cells via P2-purinergic receptors. Am. J. Physiol., 263, F374-F383.
51. SIMPSON, L. & PARSONS, R. (2001). PTEN: life as a tumor suppressor. Exp. Cell. Res., 264, 29-41.
52. STAAL, S.P. (1987). Molecular cloning of the akt oncogene and its human homologues AKT1 and AKT2: amplification of AKT1 in a primary human gastric adenocarcinoma. Proc. Natl. Acad. Sci. U.S.A., 84, 5034-5037.
53. TOKER, A. & NEWTON, A.C. (2000). Akt/protein kinase B is regulated by autophosphorylation at the hypothetical PDK-2 site. J. Biol. Chem., 275, 8271-8274.
54. TRAVO, P., WEBER, K. & OSBORN, M. (1982). Co-existence of vimentin and desmin type intermediate filaments in a subpopulation of adult rat vascular smooth muscle cells growing in primary culture. Exp. Cell Res., 139, 87-94.
55. ZINDA, M.J., VLAHOS, C.J. & LAI, M.T. (2001). Ceramide induces the dephosphorylation and inhibition of constitutively activated Akt in PTEN negative U87mg cells. Biochem. Biophys. Res. Commun., 280, 1107-1115.
56. ZHOU, H., SUMMERS, S.A., BIRNBAUM, M.J. & PITTMAN, R.N. (1998). Inhibition of Akt kinase by cell-permeable ceramide and its implications for ceramide-induced apoptosis. J. Biol. Chem., 273, 16568-16575.
57. ZUNDEL, W. & GIACCIA, A. (1998). Inhibition of the anti-apoptotic PI(3)K/Akt/Bad pathway by stress. Genes Dev., 12, 1941-1946.