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PMID: 15798218 Published · ppublish English Journal Article

Posttranscriptional downregulation of c-IAP2 by the ubiquitin protein ligase c-IAP1 in vivo.

Molecular and cellular biology ·Vol. 25 ·No. 8 ·2005-04-00 ·Pages 3348-56

Conze DB, Albert L, Ferrick DA, Goeddel DV, Yeh WC, Mak T, Ashwell JD

Abstract

Inhibitor of apoptosis proteins (IAPs) c-IAP1 and c-IAP2 were identified as part of the tumor necrosis factor receptor 2 (TNFR2) signaling complex and have been implicated as intermediaries in tumor necrosis factor alpha signaling. Like all RING domain-containing IAPs, c-IAP1 and c-IAP2 have ubiquitin protein ligase (E3) activity. To explore the function of c-IAP1 in a physiologic setting, c-IAP1-deficient mice were generated by homologous gene recombination. These animals are viable and have no obvious sensitization to proapoptotic stimuli. Cells from c-IAP1(-/-) mice do, however, express markedly elevated levels of c-IAP2 protein in the absence of increased c-IAP2 mRNA. In contrast to reports implicating c-IAPs in the activation of NF-kappaB, resting and cytokine-induced NF-kappaB activation was not impaired in c-IAP1-deficient cells. Transient transfection studies with wild-type and E3-defective c-IAP1 revealed that c-IAP2 is a direct target for c-IAP1-mediated ubiquitination and subsequent degradation, which are potentiated by the adaptor function of TRAF2. Thus, the c-IAPs represent a pair of TNFR-associated ubiquitin protein ligases in which one regulates the expression of the other by a posttranscriptional and E3-dependent mechanism.

MeSH Terms
Animals B-Lymphocytes/physiology Baculoviral IAP Repeat-Containing 3 Protein Down-Regulation Inhibitor of Apoptosis Proteins Mice Mice, Mutant Strains NF-kappa B/metabolism Proteins/genetics,metabolism RNA, Messenger/analysis,metabolism Sequence Deletion/genetics Signal Transduction Spleen/cytology,metabolism T-Lymphocytes/physiology TNF Receptor-Associated Factor 2/metabolism,physiology Thymus Gland/cytology,metabolism Transcription, Genetic Ubiquitin-Protein Ligases/genetics,metabolism,physiology Up-Regulation
Chemicals
Inhibitor of Apoptosis Proteins NF-kappa B Proteins RNA, Messenger TNF Receptor-Associated Factor 2 Baculoviral IAP Repeat-Containing 3 Protein Birc2 protein, mouse Birc3 protein, mouse Ubiquitin-Protein Ligases
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Conze Dietrich B
Laboratory of Immune Cell Biology, National Cancer Institute, National Institutes of Health, 9000 Rockville Pike, Building 37, Room 3002, Bethesda, MD 20892, USA.
Albert Lori
Ferrick David A
Goeddel David V
Yeh Wen-Chen
Mak Tak
Ashwell Jonathan D
References (46)
46 references, click to expand
  1. Derivation of embryonic stem cell lines.
    Methods Enzymol. 1993;225:803-23 PMID: 8231888
  2. The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases.
    EMBO J. 1997 Dec 1;16(23):6914-25 PMID: 9384571
  3. The NF-kappa B activation pathway: a paradigm in information transfer from membrane to nucleus.
    Sci STKE. 1999 Oct 26;1999(5):RE1 PMID: 11865184
  4. Inhibition of NF-kappaB activity and enhancement of apoptosis by the neuropeptide calcitonin gene-related peptide.
    J Biol Chem. 2000 May 19;275(20):15114-21 PMID: 10809748
  5. c-IAP1 is cleaved by caspases to produce a proapoptotic C-terminal fragment.
    J Biol Chem. 2001 Mar 9;276(10):7602-8 PMID: 11106668
  6. Genomic characterization of the mouse inhibitor of apoptosis protein 1 and 2 genes.
    Genomics. 1997 Dec 15;46(3):495-503 PMID: 9441758
  7. Cloning and characterization of the rat homologues of the Inhibitor of Apoptosis protein 1, 2, and 3 genes.
    BMC Genomics. 2002;3:5 PMID: 11860601
  8. Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli.
    Science. 2000 May 5;288(5467):874-7 PMID: 10797013
  9. Severe liver degeneration and lack of NF-kappaB activation in NEMO/IKKgamma-deficient mice.
    Genes Dev. 2000 Apr 1;14(7):854-62 PMID: 10766741
  10. Human T cell activation through the activation-inducer molecule/CD69 enhances the activity of transcription factor AP-1.
    J Immunol. 1992 Apr 1;148(7):2300-6 PMID: 1545132
  11. Regulation of activator protein-1 and NF-kappa B in CD8+ T cells exposed to peripheral self-antigens.
    J Immunol. 2001 Apr 1;166(7):4399-407 PMID: 11254694
  12. Cloning and expression of apoptosis inhibitory protein homologs that function to inhibit apoptosis and/or bind tumor necrosis factor receptor-associated factors.
    Proc Natl Acad Sci U S A. 1996 May 14;93(10):4974-8 PMID: 8643514
  13. JunD mediates survival signaling by the JNK signal transduction pathway.
    Mol Cell. 2003 Jun;11(6):1479-89 PMID: 12820962
  14. Suppression of tumor necrosis factor-induced cell death by inhibitor of apoptosis c-IAP2 is under NF-kappaB control.
    Proc Natl Acad Sci U S A. 1997 Sep 16;94(19):10057-62 PMID: 9294162
  15. Disruption of glucocorticoid receptor exon 2 yields a ligand-responsive C-terminal fragment that regulates gene expression.
    Mol Endocrinol. 2003 Aug;17(8):1534-42 PMID: 12750452
  16. NEMO/IKK gamma-deficient mice model incontinentia pigmenti.
    Mol Cell. 2000 Jun;5(6):981-92 PMID: 10911992
  17. Activation of interleukin-6 gene expression through the NF-kappa B transcription factor.
    Mol Cell Biol. 1990 May;10(5):2327-34 PMID: 2183031
  18. Critical function of endogenous XIAP in regulating caspase activation during sympathetic neuronal apoptosis.
    J Cell Biol. 2003 Nov 24;163(4):789-99 PMID: 14623868
  19. 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
  20. Natural cellular inhibitors of caspases.
    Prog Neuropsychopharmacol Biol Psychiatry. 2003 Apr;27(2):215-29 PMID: 12657361
  21. Thymocyte-targeted overexpression of xiap transgene disrupts T lymphoid apoptosis and maturation.
    Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):5049-54 PMID: 11309492
  22. Characterization of XIAP-deficient mice.
    Mol Cell Biol. 2001 May;21(10):3604-8 PMID: 11313486
  23. IAP proteins: blocking the road to death's door.
    Nat Rev Mol Cell Biol. 2002 Jun;3(6):401-10 PMID: 12042762
  24. A comprehensive search for DNA amplification in lung cancer identifies inhibitors of apoptosis cIAP1 and cIAP2 as candidate oncogenes.
    Hum Mol Genet. 2003 Apr 1;12(7):791-801 PMID: 12651874
  25. TNF-RII and c-IAP1 mediate ubiquitination and degradation of TRAF2.
    Nature. 2002 Mar 21;416(6878):345-7 PMID: 11907583
  26. NF-kappa B activation by the pre-T cell receptor serves as a selective survival signal in T lymphocyte development.
    Immunity. 2000 Nov;13(5):677-89 PMID: 11114380
  27. Cytokine regulation of pro- and anti-apoptotic genes in rat hepatocytes: NF-kappaB-regulated inhibitor of apoptosis protein 2 (cIAP2) prevents apoptosis.
    J Hepatol. 2002 Jun;36(6):742-50 PMID: 12044523
  28. Prostaglandin E2 and the increase of intracellular cAMP inhibit the expression of interleukin 2 receptors in human T cells.
    Eur J Immunol. 1988 Nov;18(11):1791-6 PMID: 2849551
  29. Dominant negative mutant of c-Jun inhibits NF-AT transcriptional activity and prevents IL-2 gene transcription.
    J Immunol. 1994 Sep 1;153(5):2046-51 PMID: 8051409
  30. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif.
    J Virol. 1993 Apr;67(4):2168-74 PMID: 8445726
  31. Reprogramming the signalling requirement for AP-1 (activator protein-1) activation during differentiation of precursor CD4+ T-cells into effector Th1 and Th2 cells.
    Genes Funct. 1997 Feb;1(1):51-68 PMID: 9680328
  32. The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins.
    Cell. 1995 Dec 29;83(7):1243-52 PMID: 8548810
  33. Cellular inhibitor of apoptosis 1 and 2 are ubiquitin ligases for the apoptosis inducer Smac/DIABLO.
    J Biol Chem. 2003 Mar 21;278(12):10055-60 PMID: 12525502
  34. A novel p75TNF receptor isoform mediating NFkappa B activation.
    J Biol Chem. 2001 Jun 1;276(22):19390-5 PMID: 11279196
  35. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells.
    Nucleic Acids Res. 1989 Aug 11;17(15):6419 PMID: 2771659
  36. RING domains: master builders of molecular scaffolds?
    J Mol Biol. 2000 Feb 4;295(5):1103-12 PMID: 10653689
  37. RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination.
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11364-9 PMID: 10500182
  38. The inhibitor of apoptosis, cIAP2, functions as a ubiquitin-protein ligase and promotes in vitro monoubiquitination of caspases 3 and 7.
    J Biol Chem. 2000 Sep 1;275(35):26661-4 PMID: 10862606
  39. Phosphorylation of serine 276 is essential for p65 NF-kappaB subunit-dependent cellular responses.
    Biochem Biophys Res Commun. 2003 Jan 24;300(4):807-12 PMID: 12559944
  40. A novel role for XIAP in copper homeostasis through regulation of MURR1.
    EMBO J. 2004 Jan 14;23(1):244-54 PMID: 14685266
  41. Nuclear factor (NF)-kappaB-regulated X-chromosome-linked iap gene expression protects endothelial cells from tumor necrosis factor alpha-induced apoptosis.
    J Exp Med. 1998 Jul 6;188(1):211-6 PMID: 9653098
  42. c-Jun NH(2)-terminal kinase (JNK)1 and JNK2 have distinct roles in CD8(+) T cell activation.
    J Exp Med. 2002 Apr 1;195(7):811-23 PMID: 11927626
  43. IL-6 and NF-IL6 in acute-phase response and viral infection.
    Immunol Rev. 1992 Jun;127:25-50 PMID: 1380488
  44. A role for NF-kappaB essential modifier/IkappaB kinase-gamma (NEMO/IKKgamma) ubiquitination in the activation of the IkappaB kinase complex by tumor necrosis factor-alpha.
    J Biol Chem. 2003 Sep 26;278(39):37297-305 PMID: 12867425
  45. NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation.
    Science. 1998 Sep 11;281(5383):1680-3 PMID: 9733516
  46. Identification of cIAP1 as a candidate target gene within an amplicon at 11q22 in esophageal squamous cell carcinomas.
    Cancer Res. 2001 Sep 15;61(18):6629-34 PMID: 11559525
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2005-04-00
Pages
3348-56
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC1069614
Subset
IM
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