A cytoplasmic ATM-TRAF6-cIAP1 module links nuclear DNA damage signaling to ubiquitin-mediated NF-κB activation

Molecular Cell

Volumn 40, Issue 1, 2010, Pages 63-74

  Hinz, Michael ^a   Stilmann, Michael ^a   Arslan, Seda Çöl ^a,b   Khanna, Kum Kum ^c   Dittmar, Gunnar ^a   Scheidereit, Claus ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; CALCIUM; CELL NUCLEUS DNA; CYCLIN DEPENDENT KINASE 4; CYTOKINE; CYTOPLASM PROTEIN; I KAPPA B KINASE; I KAPPA B KINASE ALPHA; I KAPPA B KINASE GAMMA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN P50; TUBULIN; TUMOR NECROSIS FACTOR RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME 13; ATM PROTEIN, HUMAN; BIRC2 PROTEIN, HUMAN; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN; MAP KINASE KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PARP1 PROTEIN, HUMAN; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE; RECOMBINANT PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TAB2 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR ALPHA; TUMOR SUPPRESSOR PROTEIN; UBE2N PROTEIN, HUMAN; UBIQUITIN CONJUGATING ENZYME;

ARTICLE; CELL STRESS; CONTROLLED STUDY; CYTOSOL; DNA DAMAGE; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; GENOTOXICITY; HUMAN; HUMAN CELL; PROTEIN ASSEMBLY; PROTEIN DNA BINDING; PROTEIN MOTIF; SIGNAL TRANSDUCTION; SUMOYLATION; UBIQUITINATION; CELL NUCLEUS; DOUBLE STRANDED DNA BREAK; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; HELA CELL LINE; HEPG2 CELL LINE; METABOLISM; MUTATION; PHOSPHORYLATION; PROTEIN TRANSPORT; RNA INTERFERENCE; TIME;

ATAXIA TELANGIECTASIA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CALCIUM; CELL CYCLE PROTEINS; CELL NUCLEUS; CYTOSOL; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA-BINDING PROTEINS; HELA CELLS; HEP G2 CELLS; HUMANS; I-KAPPA B KINASE; INHIBITOR OF APOPTOSIS PROTEINS; MAP KINASE KINASE KINASES; MUTATION; NF-KAPPA B; PHOSPHORYLATION; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TNF RECEPTOR-ASSOCIATED FACTOR 6; TRANSFECTION; TUMOR NECROSIS FACTOR-ALPHA; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION;

EID: 77957333810     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2010.09.008     Document Type: Article

References (42)

1. Abbott D.W., Yang Y., Hutti J.E., Madhavarapu S., Kelliher M.A., Cantley L.C. Coordinated regulation of Toll-like receptor and NOD2 signaling by K63-linked polyubiquitin chains. Mol. Cell. Biol. 2007, 27:6012-6025.
2. Bakkenist C.J., Kastan M.B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003, 421:499-506.
3. Berchtold C.M., Wu Z.H., Huang T.T., Miyamoto S. Calcium-dependent regulation of NEMO nuclear export in response to genotoxic stimuli. Mol. Cell. Biol. 2007, 27:497-509.
4. Bhoj V.G., Chen Z.J. Ubiquitylation in innate and adaptive immunity. Nature 2009, 458:430-437.
5. Cohn M.A., D'Andrea A.D. Chromatin recruitment of DNA repair proteins: lessons from the fanconi anemia and double-strand break repair pathways. Mol. Cell 2008, 32:306-312.
6. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26:1367-1372.
7. D'Angelo M.A., Hetzer M.W. Structure, dynamics and function of nuclear pore complexes. Trends Cell Biol. 2008, 18:456-466.
8. de Godoy L.M., Olsen J.V., Cox J., Nielsen M.L., Hubner N.C., Frohlich F., Walther T.C., Mann M. Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 2008, 455:1251-1254.
9. Ea C.K., Deng L., Xia Z.P., Pineda G., Chen Z.J. Activation of IKK by TNFα requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol. Cell 2006, 22:245-257.
10. Garinis G.A., van der Horst G.T., Vijg J., Hoeijmakers J.H. DNA damage and ageing: new-age ideas for an age-old problem. Nat. Cell Biol. 2008, 10:1241-1247.
11. Gyrd-Hansen M., Darding M., Miasari M., Santoro M.M., Zender L., Xue W., Tenev T., da Fonseca P.C., Zvelebil M., Bujnicki J.M., et al. IAPs contain an evolutionarily conserved ubiquitin-binding domain that regulates NF-κB as well as cell survival and oncogenesis. Nat. Cell Biol. 2008, 10:1309-1317.
12. Hacker H., Karin M. Regulation and function of IKK and IKK-related kinases. Sci. STKE 2006, 2006:re13.
13. Harper J.W., Elledge S.J. The DNA damage response: ten years after. Mol. Cell 2007, 28:739-745.
14. Hayden M.S., Ghosh S. Shared principles in NF-κB signaling. Cell 2008, 132:344-362.
15. Hinz M., Broemer M., Arslan S.C., Otto A., Mueller E.C., Dettmer R., Scheidereit C. Signal responsiveness of IκB kinases is determined by Cdc37-assisted transient interaction with Hsp90. J. Biol. Chem. 2007, 282:32311-32319.
16. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature 2001, 411:366-374.
17. Huang T.T., Wuerzberger-Davis S.M., Wu Z.H., Miyamoto S. Sequential modification of NEMO/IKKγ by SUMO-1 and ubiquitin mediates NF-κB activation by genotoxic stress. Cell 2003, 115:565-576.
18. Hur G.M., Lewis J., Yang Q., Lin Y., Nakano H., Nedospasov S., Liu Z.G. The death domain kinase RIP has an essential role in DNA damage-induced NF-κB activation. Genes Dev. 2003, 17:873-882.
19. Jackson S.P., Bartek J. The DNA-damage response in human biology and disease. Nature 2009, 461:1071-1078.
20. Janssens S., Tschopp J. Signals from within: the DNA-damage-induced NF-κB response. Cell Death Differ. 2006, 13:773-784.
21. Jiang Z., Ninomiya-Tsuji J., Qian Y., Matsumoto K., Li X. Interleukin-1 (IL-1) receptor-associated kinase-dependent IL-1-induced signaling complexes phosphorylate TAK1 and TAB2 at the plasma membrane and activate TAK1 in the cytosol. Mol. Cell. Biol. 2002, 22:7158-7167.
22. Jin H.S., Lee D.H., Kim D.H., Chung J.H., Lee S.J., Lee T.H. cIAP1, cIAP2, and XIAP act cooperatively via nonredundant pathways to regulate genotoxic stress-induced nuclear factor-κB activation. Cancer Res. 2009, 69:1782-1791.
23. Kanayama A., Seth R.B., Sun L., Ea C.K., Hong M., Shaito A., Chiu Y.H., Deng L., Chen Z.J. TAB2 and TAB3 activate the NF-κB pathway through binding to polyubiquitin chains. Mol. Cell 2004, 15:535-548.
24. Kastan M.B., Bartek J. Cell-cycle checkpoints and cancer. Nature 2004, 432:316-323.
25. Khanna K.K., Keating K.E., Kozlov S., Scott S., Gatei M., Hobson K., Taya Y., Gabrielli B., Chan D., Lees-Miller S.P., Lavin M.F. ATM associates with and phosphorylates p53: mapping the region of interaction. Nat. Genet. 1998, 20:398-400.
26. Kim M.Y., Zhang T., Kraus W.L. Poly(ADP-ribosyl)ation by PARP-1: 'PAR-laying' NAD+ into a nuclear signal. Genes Dev. 2005, 19:1951-1967.
27. Lee J.H., Paull T.T. Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 2007, 26:7741-7748.
28. Li N., Banin S., Ouyang H., Li G.C., Courtois G., Shiloh Y., Karin M., Rotman G. ATM is required for IκB kinase (IKKk) activation in response to DNA double strand breaks. J. Biol. Chem. 2001, 276:8898-8903.
29. Mabb A.M., Wuerzberger-Davis S.M., Miyamoto S. PIASy mediates NEMO sumoylation and NF-κB activation in response to genotoxic stress. Nat. Cell Biol. 2006, 8:986-993.
30. Mortusewicz O., Ame J.C., Schreiber V., Leonhardt H. Feedback-regulated poly(ADP-ribosyl)ation by PARP-1 is required for rapid response to DNA damage in living cells. Nucleic Acids Res. 2007, 35:7665-7675.
31. Piret B., Schoonbroodt S., Piette J. The ATM protein is required for sustained activation of NF-κB following DNA damage. Oncogene 1999, 18:2261-2271.
32. Scheidereit C. IκB kinase complexes: gateways to NF-κB activation and transcription. Oncogene 2006, 25:6685-6705.
33. Schreiber E., Matthias 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. 1989, 17:6419.
34. Schreiber V., Dantzer F., Ame J.C., de Murcia G. Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol. 2006, 7:517-528.
35. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 2003, 3:155-168.
36. Stilmann M., Hinz M., Arslan S.C., Zimmer A., Schreiber V., Scheidereit C. A nuclear poly(ADP-ribose)-dependent signalosome confers DNA damage-induced IκB kinase activation. Mol. Cell 2009, 36:365-378.
37. Walsh M.C., Kim G.K., Maurizio P.L., Molnar E.E., Choi Y. TRAF6 autoubiquitination-independent activation of the NF-κB and MAPK pathways in response to IL-1 and RANKL. PLoS ONE 2008, 3:e4064. 10.1371/journal.pone.0004064.
38. Wu Z.H., Miyamoto S. Many faces of NF-κB signaling induced by genotoxic stress. J. Mol. Med. 2007, 85:1187-1202.
39. Wu C.J., Conze D.B., Li T., Srinivasula S.M., Ashwell J.D. Sensing of Lys 63-linked polyubiquitination by NEMO is a key event in NF-κB activation. Nat. Cell Biol. 2006, 8:398-406.
40. Wu Z.H., Shi Y., Tibbetts R.S., Miyamoto S. Molecular linkage between the kinase ATM and NF-κB signaling in response to genotoxic stimuli. Science 2006, 311:1141-1146.
41. Xia Z.P., Sun L., Chen X., Pineda G., Jiang X., Adhikari A., Zeng W., Chen Z.J. Direct activation of protein kinases by unanchored polyubiquitin chains. Nature 2009, 461:114-119.
42. Ye H., Arron J.R., Lamothe B., Cirilli M., Kobayashi T., Shevde N.K., Segal D., Dzivenu O.K., Vologodskaia M., Yim M., et al. Distinct molecular mechanism for initiating TRAF6 signalling. Nature 2002, 418:443-447.