Home LiteratureArticle Details
PMID: 10758165 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Raf induces NF-kappaB by membrane shuttle kinase MEKK1, a signaling pathway critical for transformation.

Baumann B, Weber CK, Troppmair J, Whiteside S, Israel A, Rapp UR, Wirth T

Abstract

NF-kappaB is regulated by inhibitor proteins (IkappaBs), which retain NF-kappaB in the cytoplasm. Signal-induced phosphorylation by the IkappaB-kinase complex containing the IkappaB-kinases 1 and 2 (IKK-1/2 or IKK-alpha/beta) and subsequent degradation of the IkappaB proteins are prerequisites for NF-kappaB activation. Many signals induce NF-kappaB, one of them being oncogenic Raf kinase. We investigated whether NF-kappaB induction is critical for Raf-mediated transformation. Here, we demonstrate that inhibition of NF-kappaB interferes with transformation by the Raf-oncogene, and we characterized the mechanism of NF-kappaB induction by activated Raf kinase and the tumor promoter phorbol 12-myristate 13-acetate (PMA). NF-kappaB activation by PMA and Raf critically depends on the IkappaB-kinase complex, most notably on IKK-2. A major signaling pathway induced by Raf is the mitogenic cytoplasmic kinase cascade. However, different inhibitors of this cascade do not affect PMA- and Raf-mediated NF-kappaB activation. Raf does not phosphorylate the IkappaB-kinase proteins directly. Raf rather synergizes with another membrane shuttle kinase MEKK1, and Raf-mediated activation of NF-kappaB is blocked by a dominant negative form of MEKK1. These results suggest that Raf induction of NF-kappaB is relayed by MEKK1, but not by the classical mitogenic cytoplasmic kinase cascade.

MeSH Terms
Animals Cell Line Genes, Reporter I-kappa B Kinase NF-kappa B/metabolism Protein Serine-Threonine Kinases/metabolism Proto-Oncogene Proteins c-raf/metabolism Recombinant Fusion Proteins/metabolism Recombinant Proteins/metabolism Signal Transduction Spodoptera Tetradecanoylphorbol Acetate/pharmacology Transfection
Chemicals
NF-kappa B Recombinant Fusion Proteins Recombinant Proteins Protein Serine-Threonine Kinases Proto-Oncogene Proteins c-raf I-kappa B Kinase Tetradecanoylphorbol Acetate
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Baumann B
Institut für Medizinische Strahlenkunde und Zellforschung, Universität Würzburg Versbacher Strasse 5, 97078 Würzburg, Germany.
Weber C K
Troppmair J
Whiteside S
Israel A
Rapp U R
Wirth T
References (65)
65 references, click to expand
  1. I kappa B proteins: structure, function and regulation.
    Semin Cancer Biol. 1997 Apr;8(2):75-82 PMID: 9299585
  2. The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation.
    Cell. 1997 Oct 17;91(2):243-52 PMID: 9346241
  3. IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation.
    Science. 1997 Oct 31;278(5339):860-6 PMID: 9346484
  4. IkappaB kinase-beta: NF-kappaB activation and complex formation with IkappaB kinase-alpha and NIK.
    Science. 1997 Oct 31;278(5339):866-9 PMID: 9346485
  5. Requirement of NF-kappaB activation to suppress p53-independent apoptosis induced by oncogenic Ras.
    Science. 1997 Dec 5;278(5344):1812-5 PMID: 9388187
  6. TRAF2 is essential for JNK but not NF-kappaB activation and regulates lymphocyte proliferation and survival.
    Immunity. 1997 Nov;7(5):703-13 PMID: 9390693
  7. Early lethality, functional NF-kappaB activation, and increased sensitivity to TNF-induced cell death in TRAF2-deficient mice.
    Immunity. 1997 Nov;7(5):715-25 PMID: 9390694
  8. Plasma membrane-targeted Raf kinase activates NF-kappaB and human immunodeficiency virus type 1 replication in T lymphocytes.
    J Virol. 1998 Apr;72(4):2788-94 PMID: 9525598
  9. The death domain kinase RIP mediates the TNF-induced NF-kappaB signal.
    Immunity. 1998 Mar;8(3):297-303 PMID: 9529147
  10. NF-kappaB-inducing kinase activates IKK-alpha by phosphorylation of Ser-176.
    Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3792-7 PMID: 9520446
  11. The GABP-responsive element of the interleukin-2 enhancer is regulated by JNK/SAPK-activating pathways in T lymphocytes.
    J Biol Chem. 1998 Apr 24;273(17):10112-9 PMID: 9553058
  12. The mutant plasmacytoma cell line S107 allows the identification of distinct pathways leading to NF-kappaB activation.
    J Biol Chem. 1998 May 8;273(19):11448-55 PMID: 9565556
  13. Interleukin (IL)-1 receptor-associated kinase (IRAK) requirement for optimal induction of multiple IL-1 signaling pathways and IL-6 production.
    J Exp Med. 1998 Jun 15;187(12):2073-9 PMID: 9625767
  14. Complementation cloning of NEMO, a component of the IkappaB kinase complex essential for NF-kappaB activation.
    Cell. 1998 Jun 26;93(7):1231-40 PMID: 9657155
  15. MEKK1 activates both IkappaB kinase alpha and IkappaB kinase beta.
    Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9319-24 PMID: 9689078
  16. Activation of NF-kappa B by oncogenic Raf in HEK 293 cells occurs through autocrine recruitment of the stress kinase cascade.
    Oncogene. 1998 Aug 13;17(6):685-90 PMID: 9715269
  17. Direct phosphorylation of IkappaB by IKKalpha and IKKbeta: discrimination between free and NF-kappaB-bound substrate.
    Science. 1998 Aug 28;281(5381):1360-3 PMID: 9721103
  18. Sequential DNA damage-independent and -dependent activation of NF-kappaB by UV.
    EMBO J. 1998 Sep 1;17(17):5170-81 PMID: 9724653
  19. IKAP is a scaffold protein of the IkappaB kinase complex.
    Nature. 1998 Sep 17;395(6699):292-6 PMID: 9751059
  20. IKK-gamma is an essential regulatory subunit of the IkappaB kinase complex.
    Nature. 1998 Sep 17;395(6699):297-300 PMID: 9751060
  21. The RafC1 cysteine-rich domain contains multiple distinct regulatory epitopes which control Ras-dependent Raf activation.
    Mol Cell Biol. 1998 Nov;18(11):6698-710 PMID: 9774683
  22. Recombinant IkappaB kinases alpha and beta are direct kinases of Ikappa Balpha.
    J Biol Chem. 1998 Nov 13;273(46):30736-41 PMID: 9804849
  23. TPL-2 kinase regulates the proteolysis of the NF-kappaB-inhibitory protein NF-kappaB1 p105.
    Nature. 1999 Jan 28;397(6717):363-8 PMID: 9950430
  24. The proto-oncogene Cot kinase participates in CD3/CD28 induction of NF-kappaB acting through the NF-kappaB-inducing kinase and IkappaB kinases.
    Immunity. 1999 Feb;10(2):271-80 PMID: 10072079
  25. NF-kappaB function in growth control: regulation of cyclin D1 expression and G0/G1-to-S-phase transition.
    Mol Cell Biol. 1999 Apr;19(4):2690-8 PMID: 10082535
  26. Limb and skin abnormalities in mice lacking IKKalpha.
    Science. 1999 Apr 9;284(5412):313-6 PMID: 10195895
  27. Abnormal morphogenesis but intact IKK activation in mice lacking the IKKalpha subunit of IkappaB kinase.
    Science. 1999 Apr 9;284(5412):316-20 PMID: 10195896
  28. Severe liver degeneration in mice lacking the IkappaB kinase 2 gene.
    Science. 1999 Apr 9;284(5412):321-5 PMID: 10195897
  29. Genetic approaches to study Rel/NF-kappa B/I kappa B function in mice.
    Semin Cancer Biol. 1997 Apr;8(2):93-101 PMID: 9299587
  30. Efficient reversion of simian sarcoma virus-transformation and inhibition of growth factor-induced mitogenesis by suramin.
    Proc Natl Acad Sci U S A. 1986 Sep;83(17):6440-4 PMID: 3018732
  31. UV irradiation-induced interleukin-1 and basic fibroblast growth factor synthesis and release mediate part of the UV response.
    J Biol Chem. 1993 Mar 25;268(9):6734-41 PMID: 8454646
  32. The SRF accessory protein Elk-1 contains a growth factor-regulated transcriptional activation domain.
    Cell. 1993 Apr 23;73(2):381-93 PMID: 8386592
  33. Functional analysis of a growth factor-responsive transcription factor complex.
    Cell. 1993 Apr 23;73(2):395-406 PMID: 8477450
  34. Kappa B site-dependent induction of gene expression by diverse inducers of nuclear factor kappa B requires Raf-1.
    J Biol Chem. 1993 Aug 25;268(24):17676-9 PMID: 8349650
  35. Distinct NF-kappa B/Rel transcription factors are responsible for tissue-specific and inducible gene activation.
    Nature. 1993 Oct 21;365(6448):767-70 PMID: 7692309
  36. Oncogene activation of HIV-LTR-driven expression via the NF-kappa B binding sites.
    Nucleic Acids Res. 1993 Nov 11;21(22):5229-34 PMID: 8255780
  37. Activation of ternary complex factor Elk-1 by MAP kinases.
    EMBO J. 1993 Dec 15;12(13):5097-104 PMID: 8262053
  38. The MAP kinase Fus3 associates with and phosphorylates the upstream signaling component Ste5.
    Genes Dev. 1994 Feb 1;8(3):313-27 PMID: 8314085
  39. Mitogen-activated protein kinase/extracellular signal-regulated protein kinase activation by oncogenes, serum, and 12-O-tetradecanoylphorbol-13-acetate requires Raf and is necessary for transformation.
    J Biol Chem. 1994 Mar 4;269(9):7030-5 PMID: 8120067
  40. Differential transactivation potential of Oct1 and Oct2 is determined by additional B cell-specific activities.
    EMBO J. 1994 Apr 1;13(7):1654-63 PMID: 8157005
  41. Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells.
    Cell. 1994 Jun 17;77(6):841-52 PMID: 7911739
  42. Complexes between STE5 and components of the pheromone-responsive mitogen-activated protein kinase module.
    Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7762-6 PMID: 8052657
  43. Transformation of mammalian cells by constitutively active MAP kinase kinase.
    Science. 1994 Aug 12;265(5174):966-70 PMID: 8052857
  44. Ste5 tethers multiple protein kinases in the MAP kinase cascade required for mating in S. cerevisiae.
    Cell. 1994 Aug 12;78(3):499-512 PMID: 8062390
  45. Functional differences between the Oct2 transactivation domains determine the transactivation potential of individual Oct2 isoforms.
    Nucleic Acids Res. 1994 Oct 11;22(20):4250-8 PMID: 7937153
  46. The ins and outs of Raf kinases.
    Trends Biochem Sci. 1994 Nov;19(11):474-80 PMID: 7855890
  47. A synthetic inhibitor of the mitogen-activated protein kinase cascade.
    Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7686-9 PMID: 7644477
  48. Rapid induction of heparin-binding epidermal growth factor/diphtheria toxin receptor expression by Raf and Ras oncogenes.
    Genes Dev. 1995 Aug 15;9(16):1953-64 PMID: 7649477
  49. The NF-kappa B and I kappa B proteins: new discoveries and insights.
    Annu Rev Immunol. 1996;14:649-83 PMID: 8717528
  50. A role for nuclear NF-kappaB in B-cell-specific demethylation of the Igkappa locus.
    Nat Genet. 1996 Aug;13(4):435-41 PMID: 8696338
  51. Anatomy of TRAF2. Distinct domains for nuclear factor-kappaB activation and association with tumor necrosis factor signaling proteins.
    J Biol Chem. 1996 Aug 16;271(33):19935-42 PMID: 8702708
  52. TRAF6 is a signal transducer for interleukin-1.
    Nature. 1996 Oct 3;383(6599):443-6 PMID: 8837778
  53. Oncogenic Ha-Ras-induced signaling activates NF-kappaB transcriptional activity, which is required for cellular transformation.
    J Biol Chem. 1997 Sep 26;272(39):24113-6 PMID: 9305854
  54. NF-kappaB to the rescue: RELs, apoptosis and cellular transformation.
    Trends Genet. 1999 Jun;15(6):229-35 PMID: 10354583
  55. The IKKbeta subunit of IkappaB kinase (IKK) is essential for nuclear factor kappaB activation and prevention of apoptosis.
    J Exp Med. 1999 Jun 7;189(11):1839-45 PMID: 10359587
  56. Bridging the gap: composition, regulation, and physiological function of the IkappaB kinase complex.
    Mol Cell Biol. 1999 Jul;19(7):4547-51 PMID: 10373503
  57. NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1.
    Mol Cell Biol. 1999 Aug;19(8):5785-99 PMID: 10409765
  58. The beginning of the end: IkappaB kinase (IKK) and NF-kappaB activation.
    J Biol Chem. 1999 Sep 24;274(39):27339-42 PMID: 10488062
  59. Differential regulation of IkappaB kinase alpha and beta by two upstream kinases, NF-kappaB-inducing kinase and mitogen-activated protein kinase/ERK kinase kinase-1.
    Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3537-42 PMID: 9520401
  60. MAP3K-related kinase involved in NF-kappaB induction by TNF, CD95 and IL-1.
    Nature. 1997 Feb 6;385(6616):540-4 PMID: 9020361
  61. Induction of cell proliferation in quiescent NIH 3T3 cells by oncogenic c-Raf-1.
    Mol Cell Biol. 1997 May;17(5):2576-86 PMID: 9111327
  62. IkappaB alpha is a target for the mitogen-activated 90 kDa ribosomal S6 kinase.
    EMBO J. 1997 Jun 2;16(11):3133-44 PMID: 9214631
  63. Identification and characterization of an IkappaB kinase.
    Cell. 1997 Jul 25;90(2):373-83 PMID: 9244310
  64. A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB.
    Nature. 1997 Aug 7;388(6642):548-54 PMID: 9252186
  65. The 90-kDa ribosomal S6 kinase (pp90rsk) phosphorylates the N-terminal regulatory domain of IkappaBalpha and stimulates its degradation in vitro.
    J Biol Chem. 1997 Aug 22;272(34):21281-8 PMID: 9261139
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2000-04-25
Pages
4615-20
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC18281
Subset
IM
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: [email protected]