Poly(ADP-ribose) polymerase-1-induced NAD+ depletion promotes nuclear factor-κB transcriptional activity by preventing p65 de-acetylation

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 8, 2013, Pages 1985-1991

  Kauppinen, Tiina M ^a   Gan, Li ^b   Swanson, Raymond A ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acetylation; Astrocyte; NAD+; NF B; PARP 1; SIRT1

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; METHYLNITRONITROSOGUANIDINE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; POLY(ADENOSINE DIPHOSPHATE RIBOSE); POLY(ADENOSINE DIPHOSPHATE RIBOSE)POLYMERASE 1; SIRTUIN 1; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG;

ALKYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CATALYSIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEACETYLATION; FEMALE; GENETIC TRANSCRIPTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; WILD TYPE;

ACETYLATION; ANIMALS; ASTROCYTES; CARBAZOLES; CELLS, CULTURED; EIF-2 KINASE; HUMANS; METHYLNITRONITROSOGUANIDINE; MICE; NAD; NF-KAPPA B; POLY(ADP-RIBOSE) POLYMERASES; SIRTUIN 1; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION;

EID: 84877795435     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.04.005     Document Type: Article

References (55)

1. McCool K.W., Miyamoto S. DNA damage-dependent NF-kappaB activation: NEMO turns nuclear signaling inside out. Immunological reviews 2012, 246:311-326.
2. Hoffmann A., Baltimore D. Circuitry of nuclear factor kappaB signaling. Immunol Rev 2006, 210:171-186.
3. Chen L.F., Mu Y., Greene W.C. Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kappaB. EMBO J 2002, 21:6539-6548.
4. Yeung F., Hoberg J.E., Ramsey C.S., Keller M.D., Jones D.R., Frye R.A., Mayo M.W. Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. Embo J 2004, 23:2369-2380.
5. Ashburner B.P., Westerheide S.D., Baldwin A.S. The p65 (RelA) subunit of NF-kappaB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol Cell Biol 2001, 21:7065-7077.
6. Chen L., Fischle W., Verdin E., Greene W.C. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 2001, 293:1653-1657.
7. Buck S.W., Gallo C.M., Smith J.S. Diversity in the Sir2 family of protein deacetylases. J Leukoc Biol 2004, 75:939-950.
8. Rothgiesser K.M., Erener S., Waibel S., Luscher B., Hottiger M.O. SIRT2 regulates NF-kappaB dependent gene expression through deacetylation of p65 Lys310. J Cell Sci 2010, 123:4251-4258.
9. D'Amours D., Desnoyers S., D'Silva I., Poirier G.G. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. The Biochemical journal 1999, 342(Pt 2):249-268.
10. Davidovic L., Vodenicharov M., Affar E.B., Poirier G.G. Importance of poly(ADP-ribose) glycohydrolase in the control of poly(ADP-ribose) metabolism. Experimental cell research 2001, 268:7-13.
11. Krishnakumar R., Kraus W.L. The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Molecular cell 2010, 39:8-24.
12. Ji Y., Tulin A.V. The roles of PARP1 in gene control and cell differentiation. Curr Opin Genet Dev 2010, 20:512-518.
13. Berger N.A. Poly(ADP-ribose) in the cellular response to DNA damage. Radiation research 1985, 101:4-15.
14. Alano C.C., Tran A., Tao R., Ying W., Karliner J.S., Swanson R.A. Differences among cell types in NAD(+) compartmentalization: a comparison of neurons, astrocytes, and cardiac myocytes. J Neurosci Res 2007, 85:3378-3385.
15. + depletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death. The Journal of neuroscience: the official journal of the Society for Neuroscience 2010, 30:2967-2978.
16. Zong W.X., Ditsworth D., Bauer D.E., Wang Z.Q., Thompson C.B. Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev 2004, 18:1272-1282.
17. Ha H.C., Hester L.D., Snyder S.H. Poly(ADP-ribose) polymerase-1 dependence of stress-induced transcription factors and associated gene expression in glia. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:3270-3275.
18. Kraus W.L. Transcriptional control by PARP-1: chromatin modulation, enhancer-binding, coregulation, and insulation. Curr Opin Cell Biol 2008, 20:294-302.
19. Chang W.J., Alvarez-Gonzalez R. The sequence-specific DNA binding of NF-kappa B is reversibly regulated by the automodification reaction of poly (ADP-ribose) polymerase 1. The Journal of biological chemistry 2001, 276:47664-47670.
20. Chiarugi A., Moskowitz M.A. Poly(ADP-ribose) polymerase-1 activity promotes NF-kappaB-driven transcription and microglial activation: implication for neurodegenerative disorders. J Neurochem 2003, 85:306-317.
21. Hasko G., Mabley J.G., Nemeth Z.H., Pacher P., Deitch E.A., Szabo C. Poly(ADP-ribose) polymerase is a regulator of chemokine production: relevance for the pathogenesis of shock and inflammation. Mol Med 2002, 8:283-289.
22. Nakajima H., Nagaso H., Kakui N., Ishikawa M., Hiranuma T., Hoshiko S. Critical role of the automodification of poly(ADP-ribose) polymerase-1 in nuclear factor-kappaB-dependent gene expression in primary cultured mouse glial cells. The Journal of biological chemistry 2004, 279:42774-42786.
23. Kauppinen T.M., Swanson R.A. Poly(ADP-ribose) polymerase-1 promotes microglial activation, proliferation, and matrix metalloproteinase-9-mediated neuron death. Journal of immunology 2005, 174:2288-2296.
24. Chiarugi A. Inhibitors of poly(ADP-ribose) polymerase-1 suppress transcriptional activation in lymphocytes and ameliorate autoimmune encephalomyelitis in rats. Br J Pharmacol 2002, 137:761-770.
25. Hassa P.O., Hottiger M.O. The functional role of poly(ADP-ribose)polymerase 1 as novel coactivator of NF-kappaB in inflammatory disorders. Cell Mol Life Sci 2002, 59:1534-1553.
26. Hassa P.O., Covic M., Hasan S., Imhof R., Hottiger M.O. The enzymatic and DNA binding activity of PARP-1 are not required for NF-kappa B coactivator function. The Journal of biological chemistry 2001, 276:45588-45597.
27. Kraus W.L., Lis J.T. PARP goes transcription. Cell 2003, 113:677-683.
28. Zhang J. Are poly(ADP-ribosyl)ation by PARP-1 and deacetylation by Sir2 linked?. Bioessays 2003, 25:808-814.
29. Swanson R.A., Farrell K., Stein B.A. Astrocyte energetics, function, and death under conditions of incomplete ischemia: a mechanism of glial death in the penumbra. Glia 1997, 21:142-153.
30. Kauppinen T.M., Chan W.Y., Suh S.W., Wiggins A.K., Huang E.J., Swanson R.A. Direct phosphorylation and regulation of poly(ADP-ribose) polymerase-1 by extracellular signal-regulated kinases 1/2. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:7136-7141.
31. Chen J., Zhou Y., Mueller-Steiner S., Chen L.F., Kwon H., Yi S., Mucke L., Gan L. SIRT1 protects against microglia-dependent amyloid-beta toxicity through inhibiting NF-kappaB signaling. The Journal of biological chemistry 2005, 280:40364-40374.
32. + depletion and mitochondrial permeability transition. The Journal of biological chemistry 2004, 279:18895-18902.
33. Ying W., Sevigny M.B., Chen Y., Swanson R.A. Poly(ADP-ribose) glycohydrolase mediates oxidative and excitotoxic neuronal death. Proc Natl Acad Sci U S A 2001, 98:12227-12232.
34. Nagasawa K., Escartin C., Swanson R.A. Astrocyte cultures exhibit P2X7 receptor channel opening in the absence of exogenous ligands. Glia 2009, 57:622-633.
35. Napper A.D., Hixon J., McDonagh T., Keavey K., Pons J.F., Barker J., Yau W.T., Amouzegh P., Flegg A., Hamelin E., Thomas R.J., Kates M., Jones S., Navia M.A., Saunders J.O., DiStefano P.S., Curtis R. Discovery of indoles as potent and selective inhibitors of the deacetylase SIRT1. J Med Chem 2005, 48:8045-8054.
36. Peck B., Chen C.Y., Ho K.K., Di Fruscia P., Myatt S.S., Coombes R.C., Fuchter M.J., Hsiao C.D., Lam E.W. SIRT inhibitors induce cell death and p53 acetylation through targeting both SIRT1 and SIRT2. Mol Cancer Ther 2010, 9:844-855.
37. Smith B.C., Hallows W.C., Denu J.M. Mechanisms and molecular probes of sirtuins. Chem Biol 2008, 15:1002-1013.
38. + into a nuclear signal. Genes Dev 2005, 19:1951-1967.
39. Miyamoto S. Nuclear initiated NF-kappaB signaling: NEMO and ATM take center stage. Cell Res 2011, 21:116-130.
40. Mabb A.M., Wuerzberger-Davis S.M., Miyamoto S. PIASy mediates NEMO sumoylation and NF-kappaB activation in response to genotoxic stress. Nat Cell Biol 2006, 8:986-993.
41. Wu Z.H., Shi Y., Tibbetts R.S., Miyamoto S. Molecular linkage between the kinase ATM and NF-kappaB signaling in response to genotoxic stimuli. Science 2006, 311:1141-1146.
42. Hassa P.O., Buerki C., Lombardi C., Imhof R., Hottiger M.O. Transcriptional coactivation of nuclear factor-kappaB-dependent gene expression by p300 is regulated by poly(ADP)-ribose polymerase-1. The Journal of biological chemistry 2003, 278:45145-45153.
43. Stilmann M., Hinz M., Arslan S.C., Zimmer A., Schreiber V., Scheidereit C. A nuclear poly(ADP-ribose)-dependent signalosome confers DNA damage-induced IkappaB kinase activation. Molecular cell 2009, 36:365-378.
44. Oumouna-Benachour K., Hans C.P., Suzuki Y., Naura A., Datta R., Belmadani S., Fallon K., Woods C., Boulares A.H. Poly(ADP-ribose) polymerase inhibition reduces atherosclerotic plaque size and promotes factors of plaque stability in apolipoprotein E-deficient mice: effects on macrophage recruitment, nuclear factor-kappaB nuclear translocation, and foam cell death. Circulation 2007, 115:2442-2450.
45. Zerfaoui M., Errami Y., Naura A.S., Suzuki Y., Kim H., Ju J., Liu T., Hans C.P., Kim J.G., Abd Elmageed Z.Y., Koochekpour S., Catling A., Boulares A.H. Poly(ADP-ribose) polymerase-1 is a determining factor in Crm1-mediated nuclear export and retention of p65 NF-kappa B upon TLR4 stimulation. Journal of immunology 2010, 185:1894-1902.
46. Zerfaoui M., Suzuki Y., Naura A.S., Hans C.P., Nichols C., Boulares A.H. Nuclear translocation of p65 NF-kappaB is sufficient for VCAM-1, but not ICAM-1, expression in TNF-stimulated smooth muscle cells: differential requirement for PARP-1 expression and interaction. Cellular signalling 2008, 20:186-194.
47. Kauppinen T.M., Higashi Y., Suh S.W., Escartin C., Nagasawa K., Swanson R.A. Zinc triggers microglial activation. The Journal of neuroscience : the official journal of the Society for Neuroscience 2008, 28:5827-5835.
48. Kauppinen T.M., Suh S.W., Higashi Y., Berman A.E., Escartin C., Won S.J., Wang C., Cho S.H., Gan L., Swanson R.A. Poly(ADP-ribose)polymerase-1 modulates microglial responses to amyloid beta. Journal of neuroinflammation 2011, 8:152.
49. McCourtie A.S., Farivar A.S., Woolley S.M., Merry H.E., Wolf P.S., Szabo C., Mulligan M.S. Poly (ADP) ribose synthetase inhibition in alveolar macrophages undergoing hypoxia and reoxygenation. Experimental and molecular pathology 2008, 84:141-144.
50. Ullrich O., Diestel A., Eyupoglu I.Y., Nitsch R. Regulation of microglial expression of integrins by poly(ADP-ribose) polymerase-1. Nature cell biology 2001, 3:1035-1042.
51. Veuger S.J., Hunter J.E., Durkacz B.W. Ionizing radiation-induced NF-kappaB activation requires PARP-1 function to confer radioresistance. Oncogene 2009, 28:832-842.
52. Hassa P.O., Haenni S.S., Buerki C., Meier N.I., Lane W.S., Owen H., Gersbach M., Imhof R., Hottiger M.O. Acetylation of poly(ADP-ribose) polymerase-1 by p300/CREB-binding protein regulates coactivation of NF-kappaB-dependent transcription. J Biol Chem 2005, 280:40450-40464.
53. Kanai M., Hanashiro K., Kim S.H., Hanai S., Boulares A.H., Miwa M., Fukasawa K. Inhibition of Crm1-p53 interaction and nuclear export of p53 by poly(ADP-ribosyl)ation. Nature cell biology 2007, 9:1175-1183.
54. +: an old metabolite controlling new metabolic signaling pathways. Endocr Rev 2010, 31:194-223.
55. Bai P., Canto C., Oudart H., Brunyanszki A., Cen Y., Thomas C., Yamamoto H., Huber A., Kiss B., Houtkooper R.H., Schoonjans K., Schreiber V., Sauve A.A., Menissier-de Murcia J., Auwerx J. PARP-1 inhibition increases mitochondrial metabolism through SIRT1 activation. Cell Metab 2011, 13:461-468.