Regulation of NF-κB activation by protein phosphatase 2B and NO, via protein kinase A activity, in human monocytes

Nitric Oxide - Biology and Chemistry

Volumn 8, Issue 1, 2003, Pages 65-74

  Bengoechea Alonso, M Teresa ^a   Pelacho, Beatriz ^a   Osés Prieto, Juan A ^a   Santiago, Esteban ^a   López Moratalla, Natalia ^a   López Zabalza, María J ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

Author keywords

Endorphin; cAMP; Human monocytes; Immunomodulating peptide; Kinases; NF B; Nitric oxide; Phosphatases

Indexed keywords

6 ANILINO 5,8 QUINOLINEQUINONE; 9 (TETRAHYDRO 2 FURYL)ADENINE; BETA ENDORPHIN; CALCINEURIN; CALCINEURIN INHIBITOR; CALMODULIN INHIBITOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; CYCLOSPORIN A; GUANINE NUCLEOTIDE BINDING PROTEIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN RECEPTOR ANTAGONIST; LINSIDOMINE; N (6 AMINOHEXYL) 5 CHLORO 1 NAPHTHALENESULFONAMIDE; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; N METHYLARGININE; NF 499; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; PEPTIDE; RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG; NITRATE; PROTEIN SUBUNIT; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN;

ARTICLE; CELL STIMULATION; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; MOLECULAR BIOLOGY; MONOCYTE; NITRATION; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; WESTERN BLOTTING; AMINO ACID SEQUENCE; CELL CULTURE; ENZYME ACTIVATION; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; BETA-ENDORPHIN; BLOTTING, WESTERN; CALCINEURIN; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; GTP-BINDING PROTEIN ALPHA SUBUNITS, GS; HUMANS; MOLECULAR SEQUENCE DATA; MONOCYTES; NF-KAPPA B; NITRATES; NITRIC OXIDE; PROTEIN SUBUNITS; SIGNAL TRANSDUCTION;

EID: 0642276706     PISSN: 10898603     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1089-8603(02)00143-X     Document Type: Article

References (72)

1. López-Moratalla N., López-Zabalza M.J., Subirá M.L., Borras-Cuesta F., Pérez-Mediavilla L.A., Santiago E. Immunomodulation induced by synthetic peptides derived from Staphylococcus aureus protein A. Biochim. Biophys. Acta. 1221:1994;153-158.
2. López-Moratalla N., Calonge M.M., López-Zabalza M.J., Pérez-Mediavilla L.A., Subirá M.L., Santiago E. Activation of human lymphomononuclear cells by peptides derived from extracellular matrix proteins. Biochim. Biophys. Acta. 1265:1995;181-188.
3. López-Moratalla N., Ruiz E., López-Zabalza M.J., Santiago E. A common structural motif in immunopotentiating peptides with sequences present in human autoantigens, elicitation of a response mediated by monocytes and Th1 cells. Biochim. Biophys. Acta. 1317:1996;183-191.
4. Pérez-Mediavilla L.A., López-Zabalza M.J., Calonge M., Montuenga L., Lopez-Moratalla N., Santiago E. Inducible nitric oxide synthase in human lymphomononuclear cells activated by synthetic peptides derived from extracellular matrix proteins. FEBS Lett. 357:1995;121-124.
5. López-Moratalla N., González A., Aymerich M.S., López-Zabalza M.J., Pío R., de Castro P., Santiago E. Monocyte inducible nitric oxide synthase in multiple sclerosis: regulatory role of nitric oxide. Nitric Oxide. 1:1997;95-104.
6. López-Zabalza M.J., Martínez-Lausín S., Bengoechea-Alonso M.T., López-Moratalla N., González A., Santiago E. Signaling pathway triggered by a short immunomodulating peptide on human monocytes. Arch. Biochem. Biophys. 338:1997;136-142.
7. Aymerich M.S., Bengoechea-Alonso M.T., López-Zabalza M.J., Santiago E., López-Moratalla N. Inducible nitric oxide synthase (iNOS) expression in human monocytes triggered by β-endorphin through an increase in cAMP. Biochem. Biophys. Res. Commun. 245:1998;717-721.
8. Baeuerle P.A., Henkel T. Function and activation of NF-κB in the immune system. Annu. Rev. Immunol. 12:1994;141-179.
9. Kopp E., Ghosh S. NF-κB and rel proteins in innate immunity. Adv. Immunol. 58:1995;1-27.
10. Beg A.A., Baldwin A.S. Jr. The IκB proteins: multifunctional regulators of Rel/NF-κB transcription factors. Genes Dev. 7:1993;2064-2070.
11. Gilmore T.D., Morin P.J. The IκB proteins: members of a multifunctional family. Trends Genet. 9:1993;427-433.
12. Henkel T., Machleidt T., Alkalay Y., Kronke M., Ben-Neriah Y., Baeuerle P.A. Rapid proteolysis of IκBα is necessary for activation of transcription factor NF-κB. Nature. 365:1993;182-185.
13. Donald R., Ballard D.W., Hawiger J. Proteolytic processing of NF-κB/IκB in human monocytes, ATP-dependent induction by pro-inflammatory mediators. J. Biol. Chem. 270:1995;9-12.
14. Nishiya T., Uehara T., Nomura Y. Herbimycin A suppresses NF-κB activation and tyrosine phosphorylation of JAK2 and the subsequent induction of nitric oxide synthase in C6 glioma cells. FEBS Lett. 371:1995;333-336.
15. Alkalay I., Yaron A., Hatzubai A., Jung S., Avraham A., Gerlitz O., Pashut-Lavon Y., Ben-Neriah Y. In vivo stimulation of IκB phosphorylation is not sufficient to activate NF-κB. Mol. Cell. Biol. 15:1995;1294-1299.
16. DiDonato J.A., Mercurio F., Karin M. Phosphorylation of IκBα precedes but is not sufficient for its dissociation from NF-κB. Mol. Cell. Biol. 15:1995;1302-13011.
17. Thanos D., Maniatis T. NF-κB: a lesson in family values. Cell. 80:1995;529-532.
18. Baldwin A.S. Jr. The NF-κB and IκB proteins: new discoveries and insights. Annu. Rev. Immunol. 14:1996;649-681.
19. Ghosh S., Baltimore D. Activation in vitro of NF-κB by phosphorylation of its inhibitor IκB. Nature. 344:1990;678-682.
20. Zabel U., Baeuerle P.A. Purified human IκB can rapidly dissociate the complex of the NF-κB transcription factor with its cognate DNA. Cell. 61:1990;255-265.
21. Link E., Kerr L.D., Schreck R., Zabel U., Verma I.M., Baeuerle P.A. Purified IκB-β is inactivated upon dephosphorylation. J. Biol. Chem. 267:1992;239-246.
22. Baeuerle P.A., Baltimore D. IκB: a specific inhibitor of the NF-κB transcription factor. Science. 242:1988;540-546.
23. Brown K., Gerstberger S., Carlson L., Franzoso G., Siebenlist U. Control of IκBα proteolysis by site-specific, signal-induced phosphorylation. Science. 267:1995;1485-1488.
24. Traenckner E.B., Wilk S., Baeuerle P.A. A proteasome inhibitor prevents activation of NF-κB and stabilizes a newly phosphorylated form of IκBα that is still bound to NF-κB. EMBO J. 13:1994;5433-5441.
25. Thompson J.E., Phillips R.J., Erdjument-Bromage H., Tempst P., Ghosh S. IκBβ regulates the persistent response in a biphasic activation of NF-κB. Cell. 80:1995;573-582.
26. DiDonato J.A., Hayakawa M., Rothwarf D.M., Zandi E., Karin M. A cytokine-responsive IκB kinase that activates the transcription factor NF-κB. Nature. 388:1997;548-554.
27. Régnier C.H., Song H.Y., Gao X., Goeddel D.V., Cao Z., Rothe M. Identification and characterization of an IκB kinase. Cell. 90:1997;373-383.
28. Zandi E., Rothwarf D.M., Delhase M., Hayakawa M., Karin M. The IκB kinase complex (IKK) contains two kinase subunits, IKKα and IKKβ, necessary for IκB phosphorylation and NF-κB activation. Cell. 91:1997;243-252.
29. Mercurio F., Zhu H., Murray B.W., Shevchenko A., Bennett B.L., Li J.W., Young D.B., Barbosa M., Mann M., Manning A., Rao A. IKK-1 and IKK-2: cytokine-activated IκB kinases essential for NF-κB activation. Science. 278:1997;860-866.
30. Woronicz J.D., Gao X., Cao Z., Rothe M., Goeddel D.V. IκB kinase-β: NF-κB activation and complex formation with IκB kinase-α and NIK. Science. 278:1997;866-869.
31. Diaz-Meco M.T., Dominguez Y., Sanz L., Dentm P., Lozano J., Municio M.M., Berra E., Hay R.T., Sturgill T.W., Moscat J. PKCζ induces phosphorylation and inactivation of IκBα in vitro. EMBO J. 13:1994;2842-2848.
32. Finco T., Baldwin A. κB site-dependent induction of gene expression by diverse inducers of nuclear factor κB requires Raf-1. J. Biol. Chem. 268:1993;17676-17679.
33. Kumar A., Haque J., Lacoste J., Hiscott J., Williams B.R. Double-stranded RNA-dependent protein kinase activates transcription factor NF-κB by phosphorylating IκB. Proc. Natl. Acad. Sci. USA. 91:1994;6288-6292.
34. Schouten G.J., Vertegaal A.C.O., Whiteside S.T., Israel A., Toebes M., Dorsman J.C., van der Eb A.J., Zantema A. IκBα is a target for the mitogen-activated 90. kDa ribosomal S6 kinase EMBO J. 16:1997;3133-3144.
35. Imbert V., Rupec R.A., Livolsi A., Phal H.L., Traenckner E.B., Mueller-Dieckmann C., Farahifar D., Rossi B., Auberger P., Baeuerle P.A., Peyron J. Tyrosine phosphorylation of IκBα activates NF-κB without proteolytic degradation of IκBα Cell. 86:1996;787-798.
36. Mukhopadhyay A., Manna S.K., Aggarwal B.B. Pervanadate-induced nuclear factor-κB activation requires tyrosine phosphorylation and degradation of IκBα, comparison with tumor necrosis factor-α J. Biol. Chem. 275:2000;8549-8555.
37. Merrifield R.B., Stewart J.M. Automated peptide synthesis. Nature. 207:1965;522-523.
38. Atherton E., Logan J.C., Sheppard C.R. Peptide synthesis. Part 2. Procedures for solid phase synthesis using N-fluorenil metoxicarbonyl amino acids on polyamide supports, synthesis of substance P and of acil carrier protein 65-74 decapeptide. J. Chem. Soc. Perkin. Trans. 1:1981;538-546.
39. Boyum A. Isolation of mononuclear cells and granulocytes from human blood, isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1g. Scand. J. Clin. Lab. Invest. Suppl. 97:1968;77-89.
40. Schreiber E., Mathias P., Muller M.M., Schaffner W. Rapid detection of octamer binding proteins with "mini-extracts," prepared from a small number of cells. Nucleic Acids Res. 17:1989;6419.
41. Lenardo M.J., Baltimore D. NF-κB: a pleiotropic mediator of inducible and tissue-specific gene control. Cell. 58:1989;227-229.
42. Perkins N.D., Schmid R.M., Duckett C.S., Leung K., Rice N.R., Nabel G.J. Distinct combinations of NF-κB subunits determine the specificity of transcriptional activation. Proc. Natl. Acad. Sci. USA. 89:1992;1529-1533.
43. Miyamoto S., Schmitt M.J., Verma I.M. Qualitative changes in the subunit composition of κB-binding complexes during B-cell differentation. Proc. Natl. Acad. Sci. USA. 91:1994;5056-5060.
44. Schreck R., Rieber P., Baeuerle P. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-κB transcription factor and HIV-1. EMBO J. 10:1991;2247-2258.
45. Sun S.C., Ganchi P.A., Ballard D.W., Greene W.C. NF-κB controls expression of inhibitor IκBα: evidence for an inducible autoregulatory pathway. Science. 259:1993;1912-1915.
46. Mohr S., Hallak H., de Boitte A., Lapetina E.G., Brune B. Nitric oxide-induced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydrogenase. J. Biol. Chem. 274:1999;9427-9430.
47. Ischiropoulos H. Biological tyrosine nitration: a pathophysiological function of nitric oxide and reactive oxygen species. Arch. Biochem. Biophys. 356:1998;1-11.
48. Collart M.A., Baeuerle P.A., Vassalli P. Regulation of tumor necrosis factor α transcription in macrophages: involvement of four κB-like motifs and of constitutive and inducible forms of NF-κB. Mol. Cell. Biol. 10:1990;1498-1506.
49. Taylor B.S., de Vera M.E., Ganster R.W., Wang Q., Shapiro R.A., Morris S.M. Jr., Billiar T.R., Geller D.A. Multiple NF-κB enhancer elements regulate cytokine induction of the human inducible nitric oxide synthase gene. J. Biol. Chem. 273:1998;15148-15156.
50. Natarajan K., Manna S.K., Chaturvedi M.M., Aggarwal B.B. Protein tyrosine kinase inhibitors block tumor necrosis factor-induced activation of nuclear factor-κB, degradation of IκBα, nuclear translocation of p65, and subsequent gene expression. Arch. Biochem. Biophys. 352:1998;59-70.
51. Chen Z.J., Hagler J., Palombella V.J., Melandri F., Scherer D., Ballard D., Maniatis T. Signal-induced site-specific phosphorylation targets IκBα to the ubiquitin-proteasome pathway. Genes Dev. 9:1995;1586-1597.
52. Chen Z.J., Parent L., Maniatis T. Site-specific phosphorylation of IκBα by a novel ubiquitination-dependent protein kinase activity. Cell. 84:1996;853-862.
53. Peters R.T., Liao S.M., Maniatis T. IKK. ε is part of a novel PMA-inducible IκB kinase complex Cell. 5:2000;513-522.
54. Tojima Y., Fujimoto A., Delhase M., Chen Y., Hatakeyama S., Nakayama K., Kaneko Y., Nimura Y., Motoyama M., Ikeda K., Karin M., Nakanishi M. NAK is an IκB kinase-activating kinase. Nature. 404:2000;778-782.
55. 2+ -dependent signal transduction pathways J. Immunol. 155:1955;4685-4691.
56. Frantz B., Nordby E.C., Bren G., Steffan N., Paya C.V., Kincaid R.L., Tocci M.J., O'Keefe S.J., O'Neill E.A. Calcineurin acts in synergy with PMA to inactivate kappa/B MAD3, an inhibitor of NF-κB. EMBO J. 13:1994;861-870.
57. Petro J.B., Khan W.N. Phospholipase C-γ2 couples Bruton's tyrosine kinase to the NF-κB signaling pathways in B lymphocytes. J. Biol. Chem. 276:2001;1715-1719.
58. Neumann M., Grieshammer T., Chuvpilo S., Kneitz B., Lohoff M., Schimpl A., Franza B.R. Jr., Serfling E. RelA/p65 is a molecular target for the immunosuppressive action of protein kinase A. EMBO J. 14:1995;1991-2004.
59. Shirakawa F., Mizel S.B. In vitro activation and nuclear translocation of NF-κB catalyzed by cyclic AMP-dependent and protein kinase C. Mol. Cell. Biol. 9:1989;2424-2430.
60. Sakurai H., Chiba H., Miyoshi H., Sugita T., Toriumi W. IκB kinases phosphorylate NF-κB p65 subunit on serine 536 in the transactivation domain. J. Biol. Chem. 274:1999;30353-30356.
61. Ghosh S., Baltimore D. Activation in vitro of NF-κB by phosphorylation of its inhibitor IκB. Nature. 344:1990;678-682.
62. Lee F.S., Hagler J., Chen Z.J., Maniatis T. Activation of the IκBα kinase complex by MEKK1, a kinase of the JNK pathway. Cell. 88:1997;213-222.
63. Baumann B., Kistler B., Kirillov A., Bergman Y., Wirth T. The mutant Plastocytoma cell line S107 allows the identification of distinct pathways leading to NF-κB activation. J. Biol. Chem. 273:1998;11448-11455.
64. Christopherson K.S., Bredt D.S. Nitric oxide in excitable tissues: physiological roles and disease. J. Clin. Invest. 100:1997;2424-2429.
65. Umansky V., Hehner S.P., Dumont A., Hofmann T.G., Schirrmacher V., Droge W., Schmitz M.L. Co-stimulatory effect of nitric oxide on endothelial NF-κB implies a physiological self-amplifying mechanism. Eur. J. Immunol. 28:1998;2276-2288.
66. de la Torre A., Schroeder R.A., Punzalan C., Kuo P.C. Endotoxin-mediated S-nitrosylation of p50 alters NF-κB-dependent gene transcription in ANA-1 murine macrophages. J. Immunol. 162:1999;4101-4108.
67. Roman V., Dugas N., Abadie A., Amirand C., Zhao H., Dugas B., Colb J.P. Characterization of a constitutive type III nitric oxide synthase in human U937 monocytic cells: stimulation by soluble CD23. Immunology. 91:1997;643-648.
68. López-Moratalla N., González A., Aymerich M.S., López-Zabalza M.J., Pío R., de Castro P., Santiago E. Monocyte inducible nitric oxide synthase in multiple esclerosis: regulatory role of nitric oxide. Nitric Oxide. 1:1997;95-104.
69. Duhe R.J., Nielsen D.M., Dittman A.H., Villacres E.C., Choi E.J., Storm R.D. Oxidation of critical cysteine residues of type I adenylyl cyclase by o-iodosobenzoate or nitric oxide reversibly inhibits stimulation by calcium and calmodulin. J. Biol. Chem. 269:1994;7290-7296.
70. Zou M.H., Leist M., Ullrich V. Selective nitration of prostacyclin synthase and defective vasorelaxation in atherosclerotic bovine coronary arteries. Am. J. Pathol. 154:1999;1359-1365.
71. Sozzani P., Cambon C., Vita N., Séguelas M., Caput D., Ferrara P., Pipy B. Interleukin-13 inhibits protein kinase C-triggered respiratory burst in human monocytes, role of calcium and cyclic AMP. J. Biol. Chem. 270:1995;319-326.
72. Beavo J.A. Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol. Rev. 75:1995;725-748.