Involvement of a novel Rac/RhoA guanosine triphosphatase-nuclear factor-κB inducing kinase signaling pathway mediating angiotensin II-induced RelA transactivation

Molecular Endocrinology

Volumn 21, Issue 9, 2007, Pages 2203-2217

  Choudhary, Sanjeev ^a   Lu, Muping ^a   Cui, Ruwen ^a   Brasier, Allan R ^b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; RAC PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSCRIPTION FACTOR RELA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; GENE ACTIVATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SIGNAL TRANSDUCTION;

ANGIOTENSIN II; CELL LINE, TUMOR; CELL NUCLEUS; GTP PHOSPHOHYDROLASES; HUMANS; I-KAPPA B PROTEINS; PROTEIN-SERINE-THREONINE KINASES; RAC GTP-BINDING PROTEINS; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTOR RELA;

EID: 34548351303     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2006-0465     Document Type: Article

References (74)

1. Peach MJ 1977 Renin-angiotensin system: biochemistry and mechanisms of action. Physiol Rev 57:313-370
2. Jeunemaitre X, Soubrier F, Kotelevtsev YV, Lifton RP, Williams CS, Charru A, Hunt SC, Hopkins PN, Williams RR, Lalouel JM 1992 Molecular basis of human hypertension: role of angiotensinogen. Cell 71:169-180
3. Murphy TJ, Alexander RW, Griendling KK, Runge MS, Bernstein KE 1991 Isolation of a cDNA encoding the vascular type-1 angiotensin II receptor. Nature 351:233-236
4. Bataller R, Brenner DA 2005 Liver fibrosis. J Clin Invest 115:209-218
5. Brasier AR, Recinos AI, Eledrisi MS 2002 Vascular inflammation and the renin angiotensin system. Arterioscler Thromb Vasc Biol 22:1257-1266
6. Burns KD 2000 Angiotensin II and its receptors in the diabetic kidney. Am J Kidney Dis 36:449-467
7. Kim S, Iwao H 2000 Molecular and cellular mechanisms of angiotensin II mediated cardiovascular and renal diseases. Pharmacol Rev 52:11-34
8. Weiss D, Sorescu D, Taylor WR 2001 Angiotensin II and atherosclerosis. Am J Cardiol 87(Suppl):25C-32C
9. Bataller R, Gabele E, Schoonhoven R, Morris T, Lehnert M, Yang L, Brenner DA, Rippe RA 2003 Prolonged infusion of angiotensin II into normal rats induces stellate cell activation and proinflammatory events in liver. Am J Physiol Gastrointest Liver Physiol 285:G642-G651
10. Griendling KK, Lassegue B, Murphy TJ, Alexander DR 1994 Angiotensin II receptor pharmacology. Adv Pharmacol 28:269-306
11. Zhai P, Yamamoto M, Galeotti J, Liu J, Masurekar M, Thaisz J, Irie K, Holle E, Yu X, Kupershmidt S, Roden DM, Wagner T, Yatani A, Vatner DE, Vatner SF, Sadoshima J 2005 Cardiac-specific overexpression of AT1 receptor mutant lacking Gαq/Gαi coupling causes hypertrophy and bradycardia in transgenic mice. J Clin Invest 115:3045-3056
12. Naftilan A, Pratt RE, Eldridge CS, Lin HL, Dzau V 1989 Angiotensin II induces c-fos expression in smooth muscle via transcriptional control. Hypertension 13:706-711
13. Marrero MB, Schieffer B, Paxton WG, Heerdt L, Berk BC, Delafontaine P, Bernstein KE 1995 Direct stimulation of Jak/STAT pathway by the angiotensin II AT1 receptor. Nature 375:247-250
14. Han Y, Runge MS, Brasier AR 1999 Angiotensin II induces IL-6 transcription in vascular smooth muscle cells through pleiotropic activation of NF-kB transcription factors. Circ Res 84:695-703
15. Jamaluddin M, Meng T, Sun J, Boldogh I, Han Y, Brasier AR 2000 Angiotensin II induces nuclear factor (NF)-κB1 isoforms to bind the angiotensinogen gene acute-phase response element: a stimulus-specific pathway for NF-κB activation. Mol Endocrinol 14:99-113
16. Brasier AR, Jamaluddin M, Han Y, Patterson C, Runge MS 2001 Angiotensin II induces gene transcription through cell-type dependent effects on the nuclear factor-kB (NF-kB) transcription factor. Mol Cell Biochem 212:155-169
17. Siebenlist U, Franzoso G, Brown K 1994 Structure, regulation and function of NF-kB. Annu Rev Cell Biol 10:405-455
18. Ghosh S, May MJ, Kopp EB 1998 NF-κ B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 16:225-260
19. Pahl H 1999 Activators and target genes of Rel/NF-kB transcription factors. Oncogene 18:6853-6866
20. Tian B, Nowak D, Brasier AR 2005 A TNF induced gene expression program under oscillatory NF-κB control. BMC Genomics 6:137
21. Tian B, Nowak DE, Jamaluddin M, Wang S, Brasier AR 2005 Identification of direct genomic targets downstream of the NF-κ B transcription factor mediating TNF signaling. J Biol Chem 280:17435-17448
22. Karin M 1999 The beginning of the end: IkB kinase (IKK) and NF-kB activation. J Biol Chem 274:27342
23. Senftleben U, Cao Y, Xiao G, Greten FR, Krahn G, Bonizzi G, Chen Y, Hu Y, Fong A, Sun SC, Karin M 2001 Activation by IKKα of a second, evolutionary conserved, NF-κ B signaling pathway. Science 293:1495-1499
24. Beg AA, Baldwin ASJ 1993 The I κ B proteins: multifunctional regulators of Rel/NF-κ B transcription factors. Genes Dev 7:2064-2070
25. Maniatis T 1997 Catalysis by a multiprotein IkB kinase complex. Science 278:818-819
26. Karin M, Ben Neriah Y 2000 Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu Rev Immunol 18:621-663
27. Han Y, Weinman SA, Boldogh S, Brasier AR 1999 TNFα-Inducible IkBα proteolysis and NF-kB activation mediated by cytosolic m-Calpain. J Biol Chem 274:787-794
28. Sheppard KA, Rose DW, Haque ZK, Kurokawa R, McInerney E, Westin S, Thanos D, Rosenfeld MG, Glass CK, Collins T 1999 Transcriptional activation by NF-kB requires multiple coactivators. Mol Cell Biol 19:6367-6378
29. Bonizzi G, Karin M 2004 The two NF-kB activation pathways and their role in innate and adaptive immunity. Trends Immunol 25:280-288
30. Li J, Brasier AR 1996 Angiotensinogen gene activation by AII is mediated by the Rel A (NF-kB p65) transcription factor: one mechanism for the renin angiotensin system (RAS) positive feedback loop in hepatocytes. Mol Endocrinol 10:252-264
31. Ran J, Hirano T, Adachi M 2004 Angiotensin II type 1 receptor blocker ameliorates overproduction and accumulation of triglyceride in the liver of Zucker fatty rats. Am J Physiol Endocrinol Metab 287:E227-E232
32. Brasier AR, Spratt H, Wu Z, Boldogh I, Zhang Y, Garofalo RP, Casola A, Pashmi J, Haag A, Luxon B, Kurosky A 2004 Nuclear heat shock response and novel nuclear domain 10 reorganization in respiratory syncytial virus-infected A549 cells identified by high resolution 2D gel electrophoresis. J Virol 78:11461-11476
33. Han Y, Brasier AR 1997 Mechanism for biphasic Rel A:NF-kB1 nuclear translocation in tumor necrosis factor α-stimulated hepatocytes. J Biol Chem 272:9823-9830
34. Carlotti F, Dower SK, Qwarnstrom EE 2000 Dynamic shuttling of nuclear factor κ B between the nucleus and cytoplasm as a consequence of inhibitor dissociation. J Biol Chem 275:41028-41034
35. Birbach A, Gold P, Binder BR, Hofer E, de Martin R, Schmid JA 2002 Signaling molecules of the NF-κB pathway shuttle constitutively between cytoplasm and nucleus. J Biol Chem 277:10842-10851
36. Rice NR, Ernst MK 1993 In vivo control of NF-kB activation by IkB α. EMBO J 12:4685-4695
37. Gross S, Piwnica-Worms D 2005 Real-time imaging of ligand-induced IKK activation in intact cells and in living mice. Nat Meth 2:607-614
38. Harhaj EW, Sun S-C 1999 Regulation of RelA subcellular localization by a putative nuclear export signal and p50. Mol Cell Biol 19:7088-7095
39. Sasaki CY, Barberi TJ, Ghosh P, Longo DL 2005 Phosphorylation of RelA/p65 on serine 536 defines an IκBα-independent NF-κB pathway. J Biol Chem 280:34538-34547
40. Sakurai H, Chiba H, Miyoshi H, Sugita T, Toriumi W 1999 IκB kinases phosphorylate NF-κB p65 subunit on serine 536 in the transactivation domain. J Biol Chem 274:30353-30366
41. Jiang X, Takahashi N, Matsui N, Tetsuka T, Okamoto T 2003 The NF-κ B activation in lymphotoxin κ receptor signaling depends on the phosphorylation of p65 at serine 536. J Biol Chem 278:919-926
42. Yang CH, Murti A, Pfeffer LM 2005 Interferon induces NF-κB-inducing kinase/tumor necrosis factor receptor-associated factor-dependent NF-κB activation to promote cell survival. J Biol Chem 280:31530-31536
43. Schmitz ML, dos Santos Silva MA, Baeuerle PA 1995 Transactivation domain 2 (TA2) of p65 NF-kB: similarity to TA1 and phorbol ester-stimulated activity and phosphorylation in intact cells. J Biol Chem 270:15576-15584
44. Ling L, Cao Z, Goeddel DV 1998 NF-kB inducing kinase activates IKKα phosphorylation of Ser-176. Proc Natl Acad Sci USA 95:3792-3797
45. Funakoshi Y, Ichiki T, Shimokawa H, Egashira K, Takeda K, Kaibuchi K, Takeya M, Yoshimura T, Takeshita A 2001 Rho-kinase mediates angiotensin II-induced monocyte chemoattractant protein-1 expression in rat vascular smooth muscle cells. Hypertension 38:100-104
46. Aoki H, Izumo S, Sadoshima J 1998 Angiotensin II activates RhoA in cardiac myocytes. Circ Res 82:666-676
47. Matos P, Collard JG, Jordan P 2003 Tumor-related alternatively spliced Rac1b is not regulated by Rho-GDP dissociation inhibitors and exhibits selective downstream signaling. J Biol Chem 278:50442-50448
48. Sekine A, Fujiwara M, Narumiya S 1989 Asparagine residue in the rho gene product is the modification site for botulinum ADP ribosyltransferase. J Biol Chem 264:8602-8605
49. Daugherty A, Manning MW, Cassis LA 2001 Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J Clin Invest 105:1605-1612
50. Recinos III A, LeJeune W, Sun H, Lee C, Tieu B, Lu M, Hou T, Boldogh I, Tilton R, Brasier AR, 14 November 2006 Angiotensin II induces IL-6 expression and the Jak-STAT3 pathway in aortic adventitia of LDL receptor-deficient mice. Atherosclerosis, 10.1016/j.atherosclerosis.2006.10.013
51. Cui R, Tieu B, Recinos AI, Tilton RG, Brasier AR 2006 Rho A mediates angiotensin II-induced phospho-Ser536 NF-kB/RelA subunit exchange on the IL-6 promoter in VSMC. Circ Res 99:723-730
52. Douillette A, Bibeau-Poirier A, Gravel SP, Clement JF, Chenard V, Moreau P, Servant MJ 2006 The proinflammatory actions of angiotensin II are dependent on p65 phosphorylation by the IκB kinase complex. J Biol Chem 281:13275-13284
53. Zhang L, Ma Y, Zhang J, Cheng J, Du J 2005 A new cellular signaling mechanism for angiotensin II activation of NF-κB: an IκB- independent, RSK-mediated phosphorylation of p65. Arterioscler Thromb Vasc Biol 25:1148-1153
54. McAllister-Lucas LM, Ruland J, Siu K, Jin X, Gu S, Kim DSL, Kuffa P, Kohrt D, Mak TW, Nunez G, Lucas PC 2007 CARMA3/Bcl10/MALT1-dependent NF-κB activation mediates angiotensin II-responsive inflammatory signaling in nonimmune cells. Proc Natl Acad Sci USA 104:139-144
55. Naumann M, Scheidereit C 1994 Activation of NF-kB in vivo is regulated by multiple phosphorylations. EMBO J 13:4597-4607
56. Zhong H, Voll RE, Ghosh S 1998 Phosphorylation of NF-kB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol Cell 1:661-671
57. Vermeulen L, De Wilde G, Van Damme P, Vanden Berghe W, Haegeman G 2003 Transcriptional activation of the NF-κB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J 22:1313-1324
58. Folgueira L, McElhinny JA, Bren GD, MacMorran WS, Diaz-Meco MT, Moscat J, Paya CV 1996 Protein Kinase C-zeta mediates NF-kB activation in human immunodeficiency virus-infect monocytes. J Virol 70:223-231
59. Wang D, Westerheide SD, Hanson JL, Baldwin ASJ 2000 TNFα-induced phosphorylation of RelA/p65 on Ser529 is controlled by casein kinase II. J Biol Chem 275:32592-32597
60. Brasier AR, Lu M, Hai T, Lu Y, Boldogh I 2001 NF-kB inducible BCL-3 expression is an autoregulatory loop controlling nuclear p50/NF-kB1 residence. J Biol Chem 276:32080-32093
61. Zhang L, Cheng J, Ma Y, Thomas W, Zhang J, Du J 2005 Dual pathways for nuclear factor κB activation by angiotensin II in vascular smooth muscle: phosphorylation of p65 by IκB kinase and ribosomal kinase. Circ Res 97:975-982
62. Han Y, Meng T, Murray NR, Fields AP, Brasier AR 1999 IL-1 induced NF-κB-IκBα autoregulatory feedback loop in hepatocytes: a role for PKCα in post-transcriptional regulation of IkBa resynthesis. J Biol Chem 274:939-947
63. Malanin NL, Boldin MP, Kovalenko AV, Wallach D 1997 MAP3K-related kinase involved in NF-kB induction by TNF, CD95 and IL-1. Nature 385:540-544
64. Bonizzi G, Bebien M, Otero DC, Johnson-Vroom K, Cao Y, Vu D, Jegga AG, Aronow B, Ghosh G, Rickert R, Karin M 2004 Activation of IKKα target genes depends on recognition of specific κB binding sites by RelB:p52 dimers. EMBO J 23:4202-4210
65. Lin X, Mu Y, cunningham ET, Marcu KB, Geleziunas R, Greene WG 1998 Molecular determinants of NF-kB inducing kinase action. Mol Cell Biol 18:5899-5907
66. Neumann M, Foryst-Ludwig A, Klar S, Schweitzer K, Naumann M 2006 The PAK1 autoregulatory domain is required for interaction with NIK in Helicobacter pylori-induced NF-κB activation. Biol Chem 387:79-86
67. Lawrence T, Bebien M, Liu GY, Nizet V, Karin M 2005 IKKα limits macrophage NF-κB activation and contributes to the resolution of inflammation. Nature 434:1138-1143
68. Bosisio D, Marazzi I, Agresti A, Shimizu N, Bianchi ME, Natoli G 2006 A hyper-dynamic equilibrium between promoter-bound and nucleoplasmic dimers controls NF-κB-dependent gene activity. EMBO J 25:798-810
69. Van Aelst L, D'Souza-Schorey C 1997 Rho GTPases and signaling networks. Genes Dev 11:2295-2322
70. Ren X-D, Kiosses WB, Schwartz MA 1999 Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J 18:578-585
71. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW 1994 Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 74:1141-1148
72. Woronicz J, Gao X., Cao Z, Rothe M, Goeddel DV 1997 IkB kinase-β: NF-kB activation and complex formation with IkB kinase α and NIK. Science 866-869
73. Casola A, Garofalo RP, Haeberle H, Elliott T, Lin R, Jamaluddin M, Brasier AR 2000 Multiple inducible cis elements control RANTES promoter activation in alveolar epithelial cells infected with RSV. J Virol 75:6428-6439
74. Hai T, Yeung ML, Wood TG, Wei Y, Yamaoaka S, Gatalica Z, Jeang K-T, Brasier AR 2006 An alternative splice product of IκB kinase (IKK)-γ, IKK γ-Δ, differentially mediates cytokine and HTLV-I tax induced NF-κB activation. J Virol 80:4227-4241