Home LiteratureArticle Details
PMID: 17728102 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

ROCK I-mediated activation of NF-kappaB by RhoB.

Cellular signalling ·Vol. 19 ·No. 11 ·2007-11-00 ·Pages 2361-9

Rodriguez PL, Sahay S, Olabisi OO, Whitehead IP

Abstract

RhoB is a short-lived protein whose expression is increased by a variety of extra-cellular stimuli including UV irradiation, epidermal growth factor (EGF) and transforming growth factor beta (TGF-beta). Whereas most Rho proteins are modified by the covalent attachment of a geranylgeranyl group, RhoB is unique in that it can exist in either a geranylgeranylated (RhoB-GG) or a farnesylated (RhoB-F) form. Although each form is proposed to have different cellular functions, the signaling events that underlie these differences are poorly understood. Here we show that RhoB can activate NF-kappaB signaling in multiple cell types. Whereas RhoB-F is a potent activator of NF-kappaB, much weaker activation is observed for RhoB-GG, RhoA, and RhoC. NF-kappaB activation by RhoB is not associated with increased nuclear translocation of RelA/p65, but rather, by modification of the RelA/p65 transactivation domain. Activation of NF-kappaB by RhoB is dependent upon ROCK I but not PRK I. Thus, ROCK I cooperates with RhoB to activate NF-kappaB, and suppression of ROCK I activity by genetic or pharmacological inhibitors blocks NF-kappaB activation. Suppression of RhoB activity by dominant-inhibitory mutants, or siRNA, blocks NF-kappaB activation by Bcr, and TSG101, but not by TNFalpha or oncogenic Ras. Collectively, these observations suggest the existence of an endosome-associated pathway for NF-kappaB activation that is preferentially regulated by the farnesylated form of RhoB.

MeSH Terms
Amino Acid Sequence Animals COS Cells Chlorocebus aethiops DNA-Binding Proteins/metabolism Endosomal Sorting Complexes Required for Transport HeLa Cells Humans Intracellular Signaling Peptides and Proteins/metabolism Mice NF-kappa B/metabolism NIH 3T3 Cells Protein Prenylation Protein Serine-Threonine Kinases/metabolism Protein Structure, Tertiary Proto-Oncogene Proteins c-bcr/metabolism Signal Transduction Transcription Factors/metabolism Tumor Necrosis Factor-alpha/metabolism ras Proteins/metabolism rho-Associated Kinases rhoB GTP-Binding Protein/metabolism
Chemicals
DNA-Binding Proteins Endosomal Sorting Complexes Required for Transport Intracellular Signaling Peptides and Proteins NF-kappa B Transcription Factors Tsg101 protein Tumor Necrosis Factor-alpha Protein Serine-Threonine Kinases Proto-Oncogene Proteins c-bcr rho-Associated Kinases ras Proteins rhoB GTP-Binding Protein
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Rodriguez Pedro L
Department of Microbiology and Molecular Genetics and New Jersey Medical School, University Hospital Cancer Center, University of Medicine and Dentistry of New Jersey, Newark, NJ 07101-1709, USA.
Sahay Sutapa
Olabisi Oyenike O
Whitehead Ian P
References (50)
50 references, click to expand
  1. Oncogenic Ras can induce transcriptional activation through a variety of promoter elements, including tandem c-Ets-2 binding sites.
    Oncogene. 1994 Oct;9(10):2913-21 PMID: 8084596
  2. Intracellular localization of the P21rho proteins.
    J Cell Biol. 1992 Nov;119(3):617-27 PMID: 1383236
  3. A novel signal transduction pathway from the endoplasmic reticulum to the nucleus is mediated by transcription factor NF-kappa B.
    EMBO J. 1995 Jun 1;14(11):2580-8 PMID: 7781611
  4. Expression cloning of lfc, a novel oncogene with structural similarities to guanine nucleotide exchange factors and to the regulatory region of protein kinase C.
    J Biol Chem. 1995 Aug 4;270(31):18388-95 PMID: 7629163
  5. Activation of Rac1, RhoA, and mitogen-activated protein kinases is required for Ras transformation.
    Mol Cell Biol. 1995 Nov;15(11):6443-53 PMID: 7565796
  6. Protein prenylation: molecular mechanisms and functional consequences.
    Annu Rev Biochem. 1996;65:241-69 PMID: 8811180
  7. Activation of the nuclear factor-kappaB by Rho, CDC42, and Rac-1 proteins.
    Genes Dev. 1997 Feb 15;11(4):463-75 PMID: 9042860
  8. rhoB encoding a UV-inducible Ras-related small GTP-binding protein is regulated by GTPases of the Rho family and independent of JNK, ERK, and p38 MAP kinase.
    J Biol Chem. 1997 Dec 5;272(49):30637-44 PMID: 9388198
  9. A requirement for NF-kappaB activation in Bcr-Abl-mediated transformation.
    Genes Dev. 1998 Apr 1;12(7):968-81 PMID: 9531535
  10. Cell growth inhibition by farnesyltransferase inhibitors is mediated by gain of geranylgeranylated RhoB.
    Mol Cell Biol. 1999 Mar;19(3):1831-40 PMID: 10022870
  11. Specific contributions of the small GTPases Rho, Rac, and Cdc42 to Dbl transformation.
    J Biol Chem. 1999 Aug 13;274(33):23633-41 PMID: 10438546
  12. Regulation of epidermal growth factor receptor traffic by the small GTPase rhoB.
    Curr Biol. 1999 Sep 9;9(17):955-8 PMID: 10508588
  13. IkappaB kinases phosphorylate NF-kappaB p65 subunit on serine 536 in the transactivation domain.
    J Biol Chem. 1999 Oct 22;274(43):30353-6 PMID: 10521409
  14. Dependence of Dbl and Dbs transformation on MEK and NF-kappaB activation.
    Mol Cell Biol. 1999 Nov;19(11):7759-70 PMID: 10523665
  15. Phosphorylation of serine 468 by GSK-3beta negatively regulates basal p65 NF-kappaB activity.
    J Biol Chem. 2004 Nov 26;279(48):49571-4 PMID: 15465828
  16. RhoA/Rho-associated kinase pathway selectively regulates thrombin-induced intercellular adhesion molecule-1 expression in endothelial cells via activation of I kappa B kinase beta and phosphorylation of RelA/p65.
    J Immunol. 2004 Dec 1;173(11):6965-72 PMID: 15557193
  17. A protein's final ESCRT.
    Traffic. 2005 Jan;6(1):2-9 PMID: 15569240
  18. Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation.
    Trends Biochem Sci. 2005 Jan;30(1):43-52 PMID: 15653325
  19. Geranylgeranylated, but not farnesylated, RhoB suppresses Ras transformation of NIH-3T3 cells.
    Exp Cell Res. 2005 Apr 1;304(2):354-64 PMID: 15748883
  20. Regulation of NF-kappaB and p53 through activation of ATR and Chk1 by the ARF tumour suppressor.
    EMBO J. 2005 Mar 23;24(6):1157-69 PMID: 15775976
  21. Farnesylated RhoB inhibits radiation-induced mitotic cell death and controls radiation-induced centrosome overduplication.
    Cell Death Differ. 2005 May;12(5):492-501 PMID: 15776002
  22. Bcr interacts with components of the endosomal sorting complex required for transport-I and is required for epidermal growth factor receptor turnover.
    Cancer Res. 2006 Jun 15;66(12):6250-7 PMID: 16778200
  23. Up-regulation of RhoB by glucocorticoids and its effects on the cell proliferation and NF-kappaB transcriptional activity.
    J Steroid Biochem Mol Biol. 2006 Nov;101(4-5):179-87 PMID: 17046241
  24. RhoB alteration is necessary for apoptotic and antineoplastic responses to farnesyltransferase inhibitors.
    Mol Cell Biol. 2000 Aug;20(16):6105-13 PMID: 10913192
  25. RhoB prenylation is driven by the three carboxyl-terminal amino acids of the protein: evidenced in vivo by an anti-farnesyl cysteine antibody.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11626-31 PMID: 11027361
  26. Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking.
    Traffic. 2000 Mar;1(3):248-58 PMID: 11208108
  27. I kappa B-independent control of NF-kappa B activity by modulatory phosphorylations.
    Trends Biochem Sci. 2001 Mar;26(3):186-90 PMID: 11246025
  28. Ras-related GTPase Rhob represses NF-kappaB signaling.
    J Biol Chem. 2001 Feb 2;276(5):3115-22 PMID: 11062238
  29. Akt stimulates the transactivation potential of the RelA/p65 Subunit of NF-kappa B through utilization of the Ikappa B kinase and activation of the mitogen-activated protein kinase p38.
    J Biol Chem. 2001 Jun 1;276(22):18934-40 PMID: 11259436
  30. RhoB is dispensable for mouse development, but it modifies susceptibility to tumor formation as well as cell adhesion and growth factor signaling in transformed cells.
    Mol Cell Biol. 2001 Oct;21(20):6906-12 PMID: 11564874
  31. The expression of rho proteins decreases with human brain tumor progression: potential tumor markers.
    Clin Exp Metastasis. 2002;19(1):9-15 PMID: 11918088
  32. p38 MAPK-mediated activation of NF-kappaB by the RhoGEF domain of Bcr.
    Oncogene. 2002 Jul 11;21(30):4601-12 PMID: 12096337
  33. Suppression of rho B expression in invasive carcinoma from head and neck cancer patients.
    Clin Cancer Res. 2002 Jul;8(7):2225-32 PMID: 12114424
  34. Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kappaB.
    EMBO J. 2002 Dec 2;21(23):6539-48 PMID: 12456660
  35. Receptor downregulation and multivesicular-body sorting.
    Nat Rev Mol Cell Biol. 2002 Dec;3(12):893-905 PMID: 12461556
  36. Reversion of RhoC GTPase-induced inflammatory breast cancer phenotype by treatment with a farnesyl transferase inhibitor.
    Mol Cancer Ther. 2002 Jun;1(8):575-83 PMID: 12479217
  37. Both farnesylated and geranylgeranylated RhoB inhibit malignant transformation and suppress human tumor growth in nude mice.
    J Biol Chem. 2000 Jun 16;275(24):17974-8 PMID: 10770919
  38. Transcriptional activation of the NF-kappaB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1).
    EMBO J. 2003 Mar 17;22(6):1313-24 PMID: 12628924
  39. Multifunctional roles for the PH domain of Dbs in regulating Rho GTPase activation.
    J Biol Chem. 2003 May 16;278(20):18393-400 PMID: 12637522
  40. Sertoli-germ cell adherens junction dynamics in the testis are regulated by RhoB GTPase via the ROCK/LIMK signaling pathway.
    Biol Reprod. 2003 Jun;68(6):2189-206 PMID: 12606349
  41. IKK beta plays an essential role in the phosphorylation of RelA/p65 on serine 536 induced by lipopolysaccharide.
    J Immunol. 2003 Jun 1;170(11):5630-5 PMID: 12759443
  42. Loss of RhoB expression in human lung cancer progression.
    Clin Cancer Res. 2004 Apr 15;10(8):2742-50 PMID: 15102679
  43. Suppression of MEK/ERK signaling pathway enhances cisplatin-induced NF-kappaB activation by protein phosphatase 4-mediated NF-kappaB p65 Thr dephosphorylation.
    J Biol Chem. 2004 Jun 18;279(25):26143-8 PMID: 15073167
  44. p53 induces NF-kappaB activation by an IkappaB kinase-independent mechanism involving phosphorylation of p65 by ribosomal S6 kinase 1.
    J Biol Chem. 2004 Jun 18;279(25):26115-25 PMID: 15073170
  45. The low molecular weight GTPase RhoA and atypical protein kinase Czeta are required for TLR2-mediated gene transcription.
    J Immunol. 2004 Jul 1;173(1):507-14 PMID: 15210811
  46. Farnesyltransferase inhibitors disrupt EGF receptor traffic through modulation of the RhoB GTPase.
    J Cell Sci. 2004 Jul 1;117(Pt 15):3221-31 PMID: 15226397
  47. Regulation at multiple levels of NF-kappaB-mediated transactivation by protein acetylation.
    Biochem Pharmacol. 2004 Sep 15;68(6):1221-9 PMID: 15313420
  48. Why three Rho proteins? RhoA, RhoB, RhoC, and cell motility.
    Exp Cell Res. 2004 Nov 15;301(1):43-9 PMID: 15501444
  49. The ras-related gene rhoB is an immediate-early gene inducible by v-Fps, epidermal growth factor, and platelet-derived growth factor in rat fibroblasts.
    Mol Cell Biol. 1991 Jul;11(7):3682-90 PMID: 1710770
  50. CAAX geranylgeranyl transferase transfers farnesyl as efficiently as geranylgeranyl to RhoB.
    J Biol Chem. 1995 Apr 7;270(14):7864-8 PMID: 7713879
Article Info
Journal
Cellular signalling
Abbr.
Cell Signal
ISSN
0898-6568
Published
2007-11-00
Epub
2007-00-08
Pages
2361-9
Language
English
Region
England
NLM ID
8904683
PMCID
PMC2084080
Subset
IM
Grants
NCI NIH HHS · F31 CA117049 · United States
NCI NIH HHS · R01 CA097066 · United States
NCI NIH HHS · R01 CA097066-04 · United States
NCI NIH HHS · CA097066 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com