AMPKα2 exerts its anti-inflammatory effects through PARP-1 and Bcl-6

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 8, 2013, Pages 3161-3166

  Gongol, Brendan ^a,b   Marin, Traci ^a,b   Peng, I Chen ^b   Woo, Brian ^b   Martin, Marcy ^a   King, Stephanie ^b   Sun, Wei ^b   Johnson, David A ^b   Chien, Shu ^c   Shyy, John Y J ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Endothelium; Inflammatory co repressor; Monocyte adhesion; THP 1 cells; Vascular dysfunction

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; METFORMIN; MONOCYTE CHEMOTACTIC PROTEIN 3; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN BCL 6; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ATTENUATION; CONTROLLED STUDY; DISSOCIATION; DNA BINDING; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE INDUCTION; INTRON; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SHEAR STRESS;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELLS, CULTURED; INTRONS; MICE; PHOSPHORYLATION; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEINS C-BCL-6; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84874275609     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1222051110     Document Type: Article

References (44)

1. Marui N, et al. (1993) Vascular cell adhesion molecule-1 (VCAM-1) gene transcription and expression are regulated through an antioxidant-sensitive mechanism in human vascular endothelial cells. J Clin Invest 92 (4):1866-1874.
2. Murao K, et al. (2000) TNF-α stimulation of MCP-1 expression is mediated by the Akt/PKB signal transduction pathway in vascular endothelial cells. Biochem Biophys Res Commun 276 (2):791-796.
3. Kirii H, et al. (2003) Lack of interleukin-1β decreases the severity of atherosclerosis in ApoE-deficient mice. Arterioscler Thromb Vasc Biol 23 (4):656-660.
4. Ordás I, Mould DR, Feagan BG, Sandborn WJ (2012) Anti-TNF monoclonal antibodies in inflammatory bowel disease: pharmacokinetics-based dosing paradigms. Clin Pharmacol Ther 91 (4):635-646.
5. Feldmann M, Maini RN (2001) Anti-TNF alpha therapy of rheumatoid arthritis: What have we learned? Annu Rev Immunol 19:163-196.
6. Ewart MA, Kohlhass CF, Salt IP (2008) Inhibition of tumor necrosis factor alpha-stimulated monocyte adhesion to HAEC by AMPK. Arterioscler Thromb Vasc Biol 28:2255-2257.
7. Nerstedt A, et al. (2010) AMP-activated protein kinase inhibits IL-6-stimulated inflammatory response in human liver cells by suppressing phosphorylation of signal transducer and activator of transcription 3 (STAT3). Diabetologia 53 (11):2406-2416.
8. Salminen A, Hyttinen JMT, Kaarniranta K (2011) AMP-activated protein kinase inhibits NF-κB signaling and inflammation: Impact on healthspan and lifespan. J Mol Med (Berl) 89 (7):667-676.
9. Zhang Y, Qiu J, Wang X, Zhang Y, Xia M (2011) AMP-activated protein kinase suppresses endothelial cell inflammation through phosphorylation of transcriptional coactivator p300. Arterioscler Thromb Vasc Biol 31 (12):2897-2908.
10. Rouleau M, Patel A, Hendzel MJ, Kaufmann SH, Poirier GG (2010) PARP inhibition: PARP-1 and beyond. Nature 10 (4):293-301.
11. Ambrose HE, Papadopoulou V, Beswick RW, Wagner SD (2007) Poly-(ADP-ribose) polymerase-1 (Parp-1) binds in a sequence-specific manner at the Bcl-6 locus and contributes to the regulation of Bcl-6 transcription. Oncogene 26 (42):6244-6252.
12. Kong X, et al. (2011) Condensin I recruitment to base damage-enriched DNA lesions is modulated by PARP1. PLoS ONE 6 (8):e23548.
13. Kashima L, et al. (2012) CHFR protein regulates mitotic checkpoint by targeting PARP-1 protein for ubiquitination and degradation. J Biol Chem 287 (16):12975-12984.
14. Muñoz-Gámez JA, et al. (2009) PARP-1 is involved in autophagy induced by DNA damage. Autophagy 5 (1):61-74.
15. Hassa PO, Hottiger MO (2002) The functional role of poly (ADP-ribose) polymerase 1 as novel coactivator of NF-kappaB in inflammatory disorders. Cell Mol Life Sci 59 (9):1534-1553.
16. Racz B, et al. (2010) Regulation of MKP-1 expression and MAPK activation by PARP-1 in oxidative stress: A new mechanism for the cytoplasmic effect of PARP-1 activation. Free Radic Biol Med 49 (12):1978-1988.
17. Oliver FJ, et al. (1999) Resistance to endotoxic shock as a consequence of defective NF-κB activation in poly (ADP-ribose) polymerase-1 deficient mice. EMBO J 18:444-4454.
18. Garcia Soriano F, et al. (2001) Diabetic endothelial dysfunction: The role of poly (ADP-ribose) polymerase activation. Nat Med 7 (1):108-113.
19. von Lukowicz T, et al. (2008) PARP1 is required for adhesion molecule expression in atherogenesis. Cardiovasc Res 78 (1):158-166.
20. Huynh KD, Bardwell VJ (1998) The BCL-6 POZ domain and other POZ domains interact with the co-repressors N-CoR and SMRT. Oncogene 17 (19):2473-2484.
21. Huynh KD, Fischle W, Verdin E, Bardwell VJ (2000) BCoR, a novel corepressor involved in BCL-6 repression. Genes Dev 14 (14):1810-1823.
22. Lee CH, et al. (2003) Transcriptional repression of atherogenic inflammation: Modulation by PPARdelta. Science 302 (5644):453-457.
23. Fan Y, et al. (2008) Suppression of pro-inflammatory adhesion molecules by PPAR-δ in human vascular endothelial cells. Arterioscler Thromb Vasc Biol 28 (2):315-321.
24. Toney LM, et al. (2000) BCL-6 regulates chemokine gene transcription in macro-phages. Nat Immunol 1 (3):214-220.
25. Zhang Y, et al. (2006) AMP-activated protein kinase is involved in endothelial NO synthase activation in response to shear stress. Arterioscler Thromb Vasc Biol 26 (6):1281-1287.
26. Mathews MT, Berk BC (2008) PARP-1 inhibition prevents oxidative and nitrosative stress-induced endothelial cell death via transactivation of the VEGF receptor 2. Ar-terioscler Thromb Vasc Biol 28 (4):711-717.
27. Los M, et al. (2002) Activation and caspase-mediated inhibition of PARP: A molecular switch between fibroblast necrosis and apoptosis in death receptor signaling. Mol Biol Cell 13 (3):978-988.
28. Zhu H, Jiang Z, Lei P, Huang W, Yu X (2011) Poly (ADP-ribose) polymerase-1 mediates angiotensin II-induced expression of plasminogen activator inhibitor-1 and fibro-nectin in rat mesangial cells. Kidney Blood Press Res 34 (5):320-327.
29. Takata Y, et al. (2008) PPARdelta-mediated antiinflammatory mechanisms inhibit angiotensin II-accelerated atherosclerosis. Proc Natl Acad Sci USA 105 (11):4277-4282.
30. Wang Q, et al. (2011) Activation of AMP-activated protein kinase is required for berberine-induced reduction of atherosclerosis in mice: The role of uncoupling protein 2. PLoS ONE 6 (9):e25436.
31. Wang S, et al. (2010) AMPKalpha2 deletion causes aberrant expression and activation of NAD (P) H oxidase and consequent endothelial dysfunction in vivo: Role of 26S proteasomes. Circ Res 106 (6):1117-1128.
32. Tang CH, Chiu YC, Tan TW, Yang RS, Fu WM (2007) Adiponectin enhances IL-6 production in human synovial fibroblast via an AdipoR1 receptor, AMPK, p38, and NF-κ B pathway. J Immunol 179 (8):5483-5492.
33. Liu C, Liang B, Wang Q, Wu J, Zou MH (2010) Activation of AMP-activated protein kinase alpha1 alleviates endothelial cell apoptosis by increasing the expression of anti-apoptotic proteins Bcl-2 and survivin. J Biol Chem 285 (20):15346-15355.
34. Perez-Rosado A, et al. (2008) Bcl-6 represses NF-κB activity in diffuse large B-cell lymphomas. J Pathol 214:489-507.
35. Luo X, Kraus WL (2012) On PAR with PARP: Cellular stress signaling through poly (ADP-ribose) and PARP-1. Genes Dev 26 (5):417-432.
36. Nagata D, et al. (2004) AMP-activated protein kinase inhibits angiotensin II-stimu-lated vascular smooth muscle cell proliferation. Circulation 110 (4):444-451.
37. Schulz E, et al. (2008) Suppression of the JNK pathway by induction of a metabolic stress response prevents vascular injury and dysfunction. Circulation 118 (13):1347-1357.
38. Caballero AE, et al. (2004) The differential effects of metformin on markers of en-dothelial activation and inflammation in subjects with impaired glucose tolerance: A placebo-controlled, randomized clinical trial. J Clin Endocrinol Metab 89 (8):3943-3948.
39. Bergheim I, et al. (2006) Metformin prevents endotoxin-induced liver injury after partial hepatectomy. J Pharmacol Exp Ther 316 (3):1053-1061.
40. Li D, et al. (2010) Adenosine monophosphate-activated protein kinase induces cholesterol efflux from macrophage-derived foam cells and alleviates atherosclerosis in apolipoprotein E-deficient mice. J Biol Chem 285 (43):33499-33509.
41. Hawley SA, Gadalla AE, Olsen GS, Hardie DG (2002) The antidiabetic drug metformin activates the AMP-activated protein kinase cascade via an adenine nucleotide-in-dependent mechanism. Diabetes 51 (8):2420-2425.
42. Li X, et al. (2008) AMP-activated protein kinase promotes the differentiation of en-dothelial progenitor cells. Arterioscler Thromb Vasc Biol 28 (10):1789-1795.
43. Sun W, et al. (2006) Statins activate AMP-activated protein kinase in vitro and in vivo. Circulation 114 (24):2655-2662.
44. Donato AJ, et al. (2012) TNF-α impairs endothelial function in adipose tissue resistance arteries of mice with diet-induced obesity. Am J Physiol Heart Circ Physiol 303 (6): H672-H679.