Regulation of mitochondrial poly(ADP-Ribose) polymerase activation by the β-adrenoceptor/cAMP/protein kinase A axis during oxidative stress

Molecular Pharmacology

Volumn 86, Issue 4, 2014, Pages 450-462

  Brunyanszki, Attila ^a   Olah, Gabor ^a   Coletta, Ciro ^a   Szczesny, Bartosz ^a   Szabo, Csaba ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; BETA ADRENERGIC RECEPTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROPRANOLOL; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CYCLIC AMP; LIPOPOLYSACCHARIDE; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

ARTICLE; CELL DAMAGE; CELL DEATH; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWNSTREAM PROCESSING; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LEUKOCYTE; MITOCHONDRIAL DNA DISORDER; MITOCHONDRION; OXIDATIVE STRESS; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; U937 CELL LINE; ANIMAL; APOPTOSIS; CELL LINE; DNA DAMAGE; DRUG EFFECT; INFLAMMATION; METABOLISM; MOUSE; PHOSPHORYLATION; TUMOR CELL LINE;

ADRENERGIC BETA-ANTAGONISTS; ANIMALS; APOPTOSIS; CELL LINE; CELL LINE, TUMOR; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA DAMAGE; DNA, MITOCHONDRIAL; HUMANS; INFLAMMATION; LEUKOCYTES; LIPOPOLYSACCHARIDES; MICE; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; PHOSPHORYLATION; POLY(ADP-RIBOSE) POLYMERASES; PROPRANOLOL; RECEPTORS, ADRENERGIC, BETA;

EID: 84907447200     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.114.094318     Document Type: Article

References (51)

1. Alamdary SZ, Digaleh H, and Khodagholi F (2013) Dual contradictory effect of H-89 on neuronal retraction, death and inflammation in differentiated PC12 cells subjected to oxidative stress. J Mol Neurosci 51:1030-1037.
2. Bürkle A and Virág L (2013) Poly(ADP-ribose): PARadigms and PARadoxes. Mol Aspects Med 34:1046-1065.
3. Carlucci A, Lignitto L, and Feliciello A (2008) Control of mitochondria dynamics and oxidative metabolism by cAMP, AKAPs and the proteasome. Trends Cell Biol 18: 604-613.
4. Chen G, Pekary AE, Sugawara M, and Hershman JM (1993) Effect of exogenous hydrogen peroxide on iodide transport and iodine organification in FRTL-5 rat thyroid cells. Acta Endocrinol (Copenh) 129:89-96.
5. Cho EA and Juhnn YS (2012) The cAMP signaling system inhibits the repair of g-ray-induced DNA damage by promoting Epac1-mediated proteasomal degradation of XRCC1 protein in human lung cancer cells. Biochem Biophys Res Commun 422:256-262.
6. Curtin NJ and Szabo C (2013) Therapeutic applications of PARP inhibitors: anticancer therapy and beyond. Mol Aspects Med 34:1217-1256.
7. De Vos M, Schreiber V, and Dantzer F (2012) The diverse roles and clinical relevance of PARPs in DNA damage repair: current state of the art. Biochem Pharmacol 84: 137-146.
8. Dorn GW, 2nd (2013) Molecular mechanisms that differentiate apoptosis from programmed necrosis. Toxicol Pathol 41:227-234.
9. Du L, Zhang X, Han YY, Burke NA, Kochanek PM, Watkins SC, Graham SH, Carcillo JA, Szabó C, and Clark RS (2003) Intra-mitochondrial poly(ADP-ribosylation) contributes to NAD1 depletion and cell death induced by oxidative stress. J Biol Chem 278:18426-18433.
10. Gagné JP, Moreel X, Gagné P, Labelle Y, Droit A, Chevalier-Paré M, Bourassa S, McDonald D, Hendzel MJ, and Prigent C et al. (2009) Proteomic investigation of phosphorylation sites in poly(ADP-ribose) polymerase-1 and poly(ADP-ribose) glycohydrolase. J Proteome Res 8:1014-1029.
11. Gancedo JM (2013) Biological roles of cAMP: variations on a theme in the different kingdoms of life. Biol Rev Camb Philos Soc 88:645-668.
12. Geraets L, Moonen HJ, Wouters EF, Bast A, and Hageman GJ (2006) Caffeine metabolites are inhibitors of the nuclear enzyme poly(ADP-ribose)polymerase-1 at physiological concentrations. Biochem Pharmacol 72:902-910.
13. Gerö D, Szoleczky P, Módis K, Pribis JP, Al-Abed Y, Yang H, Chevan S, Billiar TR, Tracey KJ, and Szabo C (2013a) Identification of pharmacological modulators of HMGB1-induced inflammatory response by cell-based screening. PLoS ONE 8: e65994.
14. Gerö D, Szoleczky P, Suzuki K, Módis K, Oláh G, oletta C, and Szabo C (2013b) Cellbased screening identifies paroxetine as an inhibitor of diabetic endothelial dysfunction. Diabetes 62:953-964.
15. Guicciardi ME, Malhi H, Mott JL, and Gores GJ (2013) Apoptosis and necrosis in the liver. Compr Physiol 3:977-1010.
16. Ha HC and Snyder SH (1999) Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci USA 96:13978-13982.
17. Hegedus C, Lakatos P, Oláh G, Tóth BI, Gergely S, Szabó E, Bíró T, Szabó C, and Virág L (2008) Protein kinase C protects from DNA damage-induced necrotic cell death by inhibiting poly(ADP-ribose) polymerase-1. FEBS Lett 582:1672-1678.
18. Hottiger MO, Boothby M, Koch-Nolte F, Lüscher B, Martin NM, Plummer R, Wang ZQ, and Ziegler M (2011) Progress in the function and regulation of ADP-Ribosylation. Sci Signal 4:mr5.
19. Jagtap P, Soriano FG, Virág L, Liaudet L, Mabley J, Szabó E, Haskó G, Marton A, Lorigados CB, and Gallyas F, Jr et al. (2002) Novel phenanthridinone inhibitors of poly (adenosine 59-diphosphate-ribose) synthetase: potent cytoprotective and antishock agents. Crit Care Med 30:1071-1082.
20. Jagtap P and Szabó C (2005) Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat Rev Drug Discov 4:421-440.
21. Kauppinen TM, Chan WY, Suh SW, Wiggins AK, Huang EJ, and Swanson RA (2006) Direct phosphorylation and regulation of poly(ADP-ribose) polymerase-1 by extracellular signal-regulated kinases 1/2. Proc Natl Acad Sci USA 103:7136-7141.
22. Leadsham JE and Gourlay CW (2010) cAMP/PKA signaling balances respiratory activity with mitochondria dependent apoptosis via transcriptional regulation. BMC Cell Biol 11:92.
23. Lefkimmiatis K, Leronni D, and Hofer AM (2013) The inner and outer compartments of mitochondria are sites of distinct cAMP/PKA signaling dynamics. J Cell Biol 202:453-462.
24. Lefkimmiatis K and Zaccolo M (2014) cAMP signaling in subcellular compartments. Pharmacol Ther DOI: 10.1016/j.pharmthera.2014.03.008 [published ahead of print].
25. Lopez-Hellin J, Garcia-Arumi E, and Schwartz S (1998) Oxidative stress induces agedependent changes in lymphocyte protein synthesis and second messenger levels. Life Sci 63:13-21.
26. Mabley JG, Horváth EM, Murthy KG, Zsengellér Z, Vaslin A, Benko R, Kollai M, and Szabó C (2005) Gender differences in the endotoxin-induced inflammatory and vascular responses: potential role of poly(ADP-ribose) polymerase activation. J Pharmacol Exp Ther 315:812-820.
27. Mabley JG, Wallace R, Pacher P, Murphy K, and Szabó C (2007) Inhibition of poly (adenosine diphosphate-ribose) polymerase by the active form of vitamin D. Int J Mol Med 19:947-952.
28. Masmoudi A, Islam F, and Mandel P (1988) ADP-ribosylation of highly purified rat brain mitochondria. J Neurochem 51:188-193.
29. Módis K, Gero″ D, Erdélyi K, Szoleczky P, DeWitt D, and Szabo C (2012) Cellular bioenergetics is regulated by PARP1 under resting conditions and during oxidative stress. Biochem Pharmacol 83:633-643.
30. Módis K, Gero″ D, Stangl R, Rosero O, Szijártó A, Lotz G, Mohácsik P, Szoleczky P, Coletta C, and Szabó C (2013a) Adenosine and inosine exert cytoprotective effects in an in vitro model of liver ischemia-reperfusion injury. Int J Mol Med 31:437-446.
31. Módis K, Coletta C, Erdélyi K, Papapetropoulos A, and Szabo C (2013b) Intramitochondrial hydrogen sulfide production by 3-mercaptopyruvate sulfurtransferase maintains mitochondrial electron flow and supports cellular bioenergetics. FASEB J 27:601-611.
32. Oei SL, Keil C, and Ziegler M (2005) Poly(ADP-ribosylation) and genomic stability. Biochem Cell Biol 83:263-269.
33. Oláh G, Finnerty CC, Sbrana E, Elijah I, Gerö D, Herndon DN, and Szabó C (2011) Increased poly(ADP-ribosyl)ation in skeletal muscle tissue of pediatric patients with severe burn injury: prevention by propranolol treatment. Shock 36: 18-23.
34. Rossi MN, Carbone M, Mostocotto C, Mancone C, Tripodi M, Maione R, and Amati P (2009) Mitochondrial localization of PARP-1 requires interaction with mitofilin and is involved in the maintenance of mitochondrial DNA integrity. J Biol Chem 284: 31616-31624.
35. Srinivasan S, Spear J, Chandran K, Joseph J, Kalyanaraman B, and Avadhani NG (2013) Oxidative stress induced mitochondrial protein kinase A mediates cytochrome c oxidase dysfunction. PLoS ONE 8:e77129.
36. Suzuki K, Olah G, Modis K, Coletta C, Kulp G, Gerö D, Szoleczky P, Chang T, Zhou Z, and Wu L et al. (2011) Hydrogen sulfide replacement therapy protects the vascular endothelium in hyperglycemia by preserving mitochondrial function. Proc Natl Acad Sci USA 108:13829-13834.
37. Szabó C, Zingarelli B, O'Connor M, and Salzman AL (1996) DNA strand breakage, activation of poly (ADP-ribose) synthetase, and cellular energy depletion are involved in the cytotoxicity of macrophages and smooth muscle cells exposed to peroxynitrite. Proc Natl Acad Sci USA 93:1753-1758.
38. Szabo C, Pacher P, and Swanson RA (2006) Novel modulators of poly(ADP-ribose) polymerase. Trends Pharmacol Sci 27:626-630.
39. Szántó M, Brunyánszki A, Kiss B, Nagy L, Gergely P, Virág L, and Bai P (2012) Poly (ADP-ribose) polymerase-2: emerging transcriptional roles of a DNA-repair protein. Cell Mol Life Sci 69:4079-4092.
40. Szczesny B, Olah G, Walker DK, Volpi E, Rasmussen BB, Szabo C, and Mitra S (2013) Deficiency in repair of the mitochondrial genome sensitizes proliferating myoblasts to oxidative damage. PLoS ONE 8:e75201.
41. Tanaka Y, Koide SS, Yoshihara K, and Kamiya T (1987) Poly (ADP-ribose) synthetase is phosphorylated by protein kinase C in vitro. Biochem Biophys Res Commun 148:709-717.
42. Tann AW, Boldogh I, Meiss G, Qian W, Van Houten B, Mitra S, and Szczesny B (2011) Apoptosis induced by persistent single-strand breaks in mitochondrial genome: critical role of EXOG (59-exo/endonuclease) in their repair. J Biol Chem 286: 31975-31983.
43. Taylor SS, Zhang P, Steichen JM, Keshwani MM, and Kornev AP (2013) PKA: lessons learned after twenty years. Biochim Biophys Acta 1834:1271-1278.
44. Tulin A, Chinenov Y, and Spradling A (2003) Regulation of chromatin structure and gene activity by poly(ADP-ribose) polymerases. Curr Top Dev Biol 56:55-83.
45. Valsecchi F, Ramos-Espiritu LS, Buck J, Levin LR, and Manfredi G (2013) cAMP and mitochondria. Physiology (Bethesda) 28:199-209.
46. Virág L, Salzman AL, and Szabó C (1998) Poly(ADP-ribose) synthetase activation mediates mitochondrial injury during oxidant-induced cell death. J Immunol 161: 3753-3759.
47. Virág L and Szabó C (2001) Purines inhibit poly(ADP-ribose) polymerase activation and modulate oxidant-induced cell death. FASEB J 15:99-107.
48. Virág L, Robaszkiewicz A, Rodriguez-Vargas JM, and Oliver FJ (2013) Poly(ADP-ribose) signaling in cell death. Mol Aspects Med 34:1153-1167.
49. Wang Y, Dawson VL, and Dawson TM(2009) Poly(ADP-ribose) signals to mitochondrial AIF: a key event in parthanatos. Exp Neurol 218:193-202.
50. Yu SW, Andrabi SA, Wang H, Kim NS, Poirier GG, Dawson TM, and Dawson VL (2006) Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proc Natl Acad Sci USA 103:18314-18319.
51. Zhang J, Dawson VL, Dawson TM, and Snyder SH (1994) Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science 263:687-689.