PKCα and HMGB1 antagonistically control hydrogen peroxide-induced poly-ADP-ribose formation

Nucleic Acids Research

Volumn 44, Issue 16, 2016, Pages 7630-7645

  Andersson, Anneli ^a   Bluwstein, Andrej ^a   Kumar, Nitin ^a   Teloni, Federico ^a   Traenkle, Jens ^b   Baudis, Michael ^a   Altmeyer, Matthias ^a   Hottiger, Michael O ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b BAYER AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; HIGH MOBILITY GROUP B1 PROTEIN; HYDROGEN PEROXIDE; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; PHOSPHOLIPASE C; POLY(ADENOSINE DIPHOSPHATE RIBOSE); PROTEIN KINASE C ALPHA; APEX1 PROTEIN, MOUSE; CHROMATIN; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DNA GLYCOSYLTRANSFERASE; HISTONE; INOSITOL 1,4,5 TRISPHOSPHATE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; OGG1 PROTEIN, MOUSE; PARP1 PROTEIN, MOUSE; PROTEOME;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME REGULATION; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; CALCIUM SIGNALING; CELL CYCLE; CELL LINE; CELL MEMBRANE; CHROMATIN; DNA STRAND BREAKAGE; DRUG EFFECTS; ENDOPLASMIC RETICULUM; ENZYMOLOGY; METABOLISM; NIH 3T3 CELL LINE; PHOSPHORYLATION;

ANIMALS; CALCIUM SIGNALING; CELL CYCLE; CELL LINE; CELL MEMBRANE; CELL NUCLEUS; CHROMATIN; DNA BREAKS; DNA GLYCOSYLASES; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; ENDOPLASMIC RETICULUM; HISTONES; HMGB1 PROTEIN; HUMANS; HYDROGEN PEROXIDE; INOSITOL 1,4,5-TRISPHOSPHATE; MICE; NIH 3T3 CELLS; PHOSPHORYLATION; POLY (ADP-RIBOSE) POLYMERASE-1; POLY ADENOSINE DIPHOSPHATE RIBOSE; PROTEIN KINASE C-ALPHA; PROTEOME; SIGNAL TRANSDUCTION; TYPE C PHOSPHOLIPASES;

EID: 84988979361     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw442     Document Type: Article

References (81)

1. Shokolenko, I., Venediktova, N., Bochkareva, A., Wilson, G.L. and Alexeyev, M.F. (2009) Oxidative stress induces degradation of mitochondrial DNA. Nucleic Acids Res., 37, 2539-2548.
2. Yoshida, H., Nishikawa, M., Kiyota, T., Toyota, H. and Takakura, Y. (2011) Increase in CpG DNA-induced inflammatory responses by DNA oxidation in macrophages and mice. Free Radic. Biol. Med., 51, 424-431.
3. Zhang, Q., Itagaki, K. and Hauser, C.J. (2010) Mitochondrial DNA is released by shock and activates neutrophils via P38 map kinase. Shock, 34, 55-59.
4. Brinkmann, V. and Zychlinsky, A. (2012) Neutrophil extracellular traps: is immunity the second function of chromatin? J. Cell Biol., 198, 773-783.
5. Collins, L.V., Hajizadeh, S., Holme, E., Jonsson, I.M. and Tarkowski, A. (2004) Endogenously oxidized mitochondrial DNA induces in vivo and in vitro inflammatory responses. J. Leukoc. Biol., 75, 995-1000.
6. Saxena, G., Chen, J.Q. and Shalev, A. (2010) Intracellular shuttling and mitochondrial function of thioredoxin-interacting protein. J. Biol. Chem., 285, 3997-4005.
7. Yoshihara, E., Chen, Z., Matsuo, Y., Masutani, H. and Yodoi, J. (2010) Thiol redox transitions by thioredoxin and thioredoxin-binding protein-2 in cell signaling. Method Enzymol., 474, 67-82.
8. Lane, T., Flam, B., Lockey, R. and Kolliputi, N. (2013) TXNIP shuttling: missing link between oxidative stress and inflannmasome activation. Front Physiol., 4, 50.
9. Kazak, L., Reyes, A. and Holt, I.J. (2012) Minimizing the damage: repair pathways keep mitochondrial DNA intact. Nat. Rev. Mol. Cell Biol., 13, 659-671.
10. Alexeyev, M., Shokolenko, I., Wilson, G. and LeDoux, S. (2013) The maintenance of mitochondrial DNA integrity-critical analysis and update. Csh Perspect. Biol., 5, a012641.
11. Suzuki, N., Kamataki, A., Yamaki, J. and Homma, Y. (2008) Characterization of circulating DNA in healthy human plasma. Clin. Chim. Acta, 387, 55-58.
12. Hassa, P.O., Haenni, S., Elser, M. and Hottiger, M.O. (2006) Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going? Microbiol. Mol. Biol. Rev., 70, 789-829.
13. Hottiger, M.O., Hassa, P.O., Luscher, B., Schuler, H. and Koch-Nolte, F. (2010) Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem. Sci., 35, 208-219.
14. Luo, X. and Kraus, W.L. (2012) On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev., 26, 417-432.
15. Altmeyer, M., Messner, S., Hassa, P.O., Fey, M. and Hottiger, M.O. (2009) Molecular mechanism of poly(ADP-ribosyl)ation by PARP1 and identification of lysine residues as ADP-ribose acceptor sites. Nucleic Acids Res., 37, 3723-3738.
16. Krishnakumar, R. and Kraus, W. (2010) The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol. Cell, 39, 8-24.
17. Schiewer, M.J., Goodwin, J.F., Han, S., Brenner, J.C., Augello, M.A., Dean, J.L., Liu, F., Planck, J.L., Ravindranathan, P., Chinnaiyan, A.M. et al. (2012) Dual roles of PARP-1 promote cancer growth and progression. Cancer Discov., 2, 1134-1149.
18. Kraus, W.L. and Hottiger, M.O. (2013) PARP-1 and gene regulation: progress and puzzles. Mol. Aspects Med., 34, 1109-1123.
19. David, K.K., Andrabi, S.A., Dawson, T.M. and Dawson, V.L. (2009) Parthanatos, a messenger of death. Front. Biosci., 14, 1116-1128.
20. Lonskaya, I., Potaman, V.N., Shlyakhtenko, L.S., Oussatcheva, E.A., Lyubchenko, Y.L. and Soldatenkov, V.A. (2005) Regulation of poly(ADP-ribose) polymerase-1 by DNA structure-specific binding. J. Biol. Chem., 280, 17076-17083.
21. Kun, E., Kirsten, E., Mendeleyev, J. and Ordahl, C. (2004) Regulation of the enzymatic catalysis of poly(ADP-ribose) polymerase by dsDNA, polyamines, Mg2+, Ca2+, histones H1 and H3, and ATP. Biochemistry, 43, 210-216.
22. Thomas, C.J., Kotova, E., Andrake, M., Adolf-Bryfogle, J., Glaser, R., Regnard, C. and Tulin, A.V. (2014) Kinase-mediated changes in nucleosome conformation trigger chromatin decondensation via poly(ADP-Ribosyl)ation. Mol. Cell, 53, 831-842.
23. Osmanov, T., Ugrinova, I. and Pasheva, E. (2013) The chaperone like function of the nonhistone protein HMGB1. Biochem. Bioph. Res. Co., 432, 231-235.
24. Joshi, S.R., Sarpong, Y.C., Peterson, R.C. and Scovell, W.M. (2012) Nucleosome dynamics: HMGB1 relaxes canonical nucleosome structure to facilitate estrogen receptor binding. Nucleic Acids Res., 40, 10161-10171.
25. Bonaldi, T., Langst, G., Strohner, R., Becker, P.B. and Bianchi, M.E. (2002) The DNA chaperone HMGB1 facilitates ACF/CHRAC-dependent nucleosome sliding. EMBO J., 21, 6865-6873.
26. Watson, M., Stott, K., Fischl, H., Cato, L. and Thomas, J.O. (2014) Characterization of the interaction between HMGB1 and H3-a possible means of positioning HMGB1 in chromatin. Nucleic Acids Res., 42, 848-859.
27. Celona, B., Weiner, A., Di Felice, F., Mancuso, F.M., Cesarini, E., Rossi, R.L., Gregory, L., Baban, D., Rossetti, G., Grianti, P., et al. (2011) Substantial histone reduction modulates genomewide nucleosomal occupancy and global transcriptional output. PLoS Biol., 9, e1001086.
28. Ugrinova, I., Pasheva, E.A., Armengaud, J. and Pashev, I.G. (2001) In vivo acetylation of HMG1 protein enhances its binding affinity to distorted DNA structures. Biochemistry, 40, 14655-14660.
29. Youn, J.H. and Shin, J.S. (2006) Nucleocytoplasmic shuttling of HMGB1 is regulated by phosphorylation that redirects it toward secretion. J. Immunol., 177, 7889-7897.
30. Zhang, Q. and Wang, Y. (2008) High mobility group proteins and their post-translational modifications. Biochim. Biophys. Acta, 1784, 1159-1166.
31. Paull, T.T., Haykinson, M.J. and Johnson, R.C. (1993) The nonspecific DNA-binding and -bending proteins HMG1 and HMG2 promote the assembly of complex nucleoprotein structures. Genes Dev., 7, 1521-1534.
32. Cohen-Armon, M. (2007) PARP-1 activation in the ERK signaling pathway. Trends Pharmacol. Sci., 28, 556-560.
33. Cohen-Armon, M., Visochek, L., Rozensal, D., Kalal, A., Geistrikh, I., Klein, R., Bendetz-Nezer, S., Yao, Z. and Seger, R. (2007) DNA-independent PARP-1 activation by phosphorylated ERK2 increases Elk1 activity: a link to histone acetylation. Mol. Cell, 25, 297-308.
34. Kauppinen, T., Chan, W., Suh, S., Wiggins, A., Huang, E. and Swanson, R. (2006) Direct phosphorylation and regulation of poly(ADP-ribose) polymerase-1 by extracellular signal-regulated kinases 1/2. Proc. Natl. Acad. Sci. U.S.A., 103, 7136-7141.
35. Zhang, S., Lin, Y., Kim, Y.S., Hande, M.P., Liu, Z.G. and Shen, H.M. (2007) c-Jun N-terminal kinase mediates hydrogen peroxide-induced cell death via sustained poly(ADP-ribose) polymerase-1 activation. Cell Death Differ., 14, 1001-1010.
36. Bauer, P.I., Farkas, G., Buday, L., Mikala, G., Meszaros, G., Kun, E. and Farago, A. (1992) Inhibition of DNA binding by the phosphorylation of poly ADP-ribose polymerase protein catalysed by protein kinase C. Biochem. Biophys. Res. Commun., 187, 730-736.
37. Hegedus, C., Lakatos, P., Olah, G., Toth, B.I., Gergely, S., Szabo, E., Biro, T., Szabo, C. and Virag, 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.
38. Tanaka, Y., Koide, S.S., 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.
39. Mizuguchi, H., Terao, T., Kitai, M., Ikeda, M., Yoshimura, Y., Das, A.K., Kitamura, Y., Takeda, N. and Fukui, H. (2011) Involvement of protein kinase Cdelta/extracellular signal-regulated kinase/poly(ADP-ribose) polymerase-1 (PARP-1) signaling pathway in histamine-induced up-regulation of histamine H1 receptor gene expression in HeLa cells. J. Biol. Chem., 286, 30542-30551.
40. Jacobs, J.P., Jones, C.M. and Baille, J.P. (1970) Characteristics of a human diploid cell designated MRC-5. Nature, 227, 168-170.
41. Nichols, W.W., Murphy, D.G., Cristofalo, V.J., Toji, L.H., Greene, A.E. and Dwight, S.A. (1977) Characterization of a new human diploid cell strain, IMR-90. Science, 196, 60-63.
42. Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem., 193, 265-275.
43. Dignam, J.D., Lebovitz, R.M. and Roeder, R.G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res., 11, 1475-1489.
44. Pawlak, M., Schick, E., Bopp, M.A., Schneider, M.J., Oroszlan, P. and Ehrat, M. (2002) Zeptosens protein microarrays: a novel high performance microarray platform for low abundance protein analysis. Proteomics, 2, 383-393.
45. Bluwstein, A., Kumar, N., Leger, K., Traenkle, J., Oostrum, J., Rehrauer, H., Baudis, M. and Hottiger, M.O. (2013) PKC signaling prevents irradiation-induced apoptosis of primary human fibroblasts. Cell Death Dis., 4, e498.
46. Voshol, H., Ehrat, M., Traenkle, J., Bertrand, E. and van Oostrum, J. (2009) Antibody-based proteomics: analysis of signaling networks using reverse protein arrays. FEBS J., 276, 6871-6879.
47. Lloyd, S.P. (1982) Least squares quantization in PCM. IEEE Trans. Inf. Theory, 28, 128-137.
48. Bevington, P.R. (2002) Data Reduction and Error Analysis for the Physical Sciences. 3rd edn, McGraw-Hill, NY.
49. Saeed, A.I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T., Thiagarajan, M., et al. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques, 34, 374-378.
50. Zar, J.H. (2009) Biostatistical Analysis, 5th edn, Prentice Hall, Upper Saddle River, NJ.
51. Schaefer, C.F., Anthony, K., Krupa, S., Buchoff, J., Day, M., Hannay, T. and Buetow, K.H. (2009) PID: the pathway interaction database. Nucleic Acids Res., 37, D674-D679.
52. Kanehisa, M., Goto, S., Furumichi, M., Tanabe, M. and Hirakawa, M. (2010) KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res., 38, D355-D360.
53. Ihaka, R. and Genleman, R. (1996) R. A language for data analysis and graphics. J. Comput. Graph. Stat., 5, 299-314.
54. Reiner, A., Yekutieli, D. and Benjamini, Y. (2003) Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics, 19, 368-375.
55. Szklarczyk, D., Franceschini, A., Kuhn, M., Simonovic, M., Roth, A., Minguez, P., Doerks, T., Stark, M., Muller, J., Bork, P., et al. (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res., 39, D561-D568.
56. Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B. and Ideker, T. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res., 13, 2498-2504.
57. Altmeyer, M., Toledo, L., Gudjonsson, T., Grofte, M., Rask, M.B., Lukas, C., Akimov, V., Blagoev, B., Bartek, J. and Lukas, J. (2013) The chromatin scaffold protein SAFB1 renders chromatin permissive for DNA damage signaling. Mol. Cell, 52, 206-220.
58. Toledo, L.I., Altmeyer, M., Rask, M.B., Lukas, C., Larsen, D.H., Povlsen, L.K., Bekker-Jensen, S., Mailand, N., Bartek, J. and Lukas, J. (2013) ATR prohibits replication catastrophe by preventing global exhaustion of RPA. Cell, 155, 1088-1103.
59. Newton, A.C. (2010) Protein kinase C: poised to signal. Am. J. Physiol. Endocrinol. Metab., 298, E395-E402.
60. Ali, A.A., Timinszky, G., Arribas-Bosacoma, R., Kozlowski, M., Hassa, P.O., Hassler, M., Ladurner, A.G., Pearl, L.H. and Oliver, A.W. (2012) The zinc-finger domains of PARP1 cooperate to recognize DNA strand breaks. Nat. Struct. Mol. Biol., 19, 685-692.
61. Tokui, T., Inagaki, M., Nishizawa, K., Yatani, R., Kusagawa, M., Ajiro, K., Nishimoto, Y., Date, T. and Matsukage, A. (1991) Inactivation of DNA-Polymerase Beta by Invitro Phosphorylation with Protein-Kinase-C. J. Biol. Chem., 266, 10820-10824.
62. Ugrinova, I., Zlateva, S. and Pasheva, E. (2012) The effect of PKC phosphorylation on the "architectural" properties of HMGB1 protein. Mol. Biol. Rep., 39, 9947-9953.
63. Oh, Y.J., Youn, J.H., Ji, Y., Lee, S.E., Lim, K.J., Choi, J.E. and Shin, J.S. (2009) HMGB1 is phosphorylated by classical protein kinase C and is secreted by a calcium-dependent mechanism. J. Immunol., 182, 5800-5809.
64. Ditsworth, D., Zong, W.X. and Thompson, C.B. (2007) Activation of poly(ADP)-ribose polymerase (PARP-1) induces release of the pro-inflammatory mediator HMGB1 from the nucleus. J. Biol. Chem., 282, 17845-17854.
65. Yang, M., Liu, L., Xie, M., Sun, X., Yu, Y., Kang, R., Yang, L., Zhu, S., Cao, L. and Tang, D. (2015) Poly-ADP-ribosylation of HMGB1 regulates TNFSF10/TRAIL resistance through autophagy. Autophagy, 11, 214-224.
66. Vogel, C., Silva, G.M. and Marcotte, E.M. (2011) Protein expression regulation under oxidative stress. Mol. Cell Proteomics, 10, M111 009217.
67. Ju, B.-G., Solum, D., Song, E., Lee, K.-J., Rose, D., Glass, C. and Rosenfeld, M. (2004) Activating the PARP-1 sensor component of the groucho/ TLE1 corepressor complex mediates a CaMKinase IIdelta-dependent neurogenic gene activation pathway. Cell, 119, 815-829.
68. Midorikawa, R., Takei, Y. and Hirokawa, N. (2006) KIF4 motor regulates activity-dependent neuronal survival by suppressing PARP-1 enzymatic activity. Cell, 125, 371-383.
69. Bentle, M., Reinicke, K., Bey, E., Spitz, D. and Boothman, D. (2006) Calcium-dependent modulation of poly(ADP-ribose) polymerase-1 alters cellular metabolism and DNA repair. J. Biol. Chem., 281, 33684-33696.
70. Sato, H., Takeo, T., Liu, Q., Nakano, K., Osanai, T., Suga, S., Wakui, M. and Wu, J. (2009) Hydrogen peroxide mobilizes Ca2+ through two distinct mechanisms in rat hepatocytes. Acta Pharmacol. Sinica, 30, 78-89.
71. Hong, J.H., Moon, S.J., Byun, H.M., Kim, M.S., Jo, H., Bae, Y.S., Lee, S.I., Bootman, M.D., Roderick, H.L., Shin, D.M., et al. (2006) Critical role of phospholipase Cgamma1 in the generation of H2O2-evoked [Ca2+]i oscillations in cultured rat cortical astrocytes. J. Biol. Chem., 281, 13057-13067.
72. Lee, S.R., Yang, K.S., Kwon, J., Lee, C., Jeong, W. and Rhee, S.G. (2002) Reversible inactivation of the tumor suppressor PTEN by H2O2. J. Biol. Chem., 277, 20336-20342.
73. Bartha, E., Solti, I., Kereskai, L., Lantos, J., Plozer, E., Magyar, K., Szabados, E., Kalai, T., Hideg, K., Halmosi, R., et al. (2009) PARP inhibition delays transition of hypertensive cardiopathy to heart failure in spontaneously hypertensive rats. Cardiovasc. Res., 83, 501-510.
74. Gagne, J.P., Moreel, X., Gagne, P., Labelle, Y., Droit, A., Chevalier-Pare, M., Bourassa, S., McDonald, D., Hendzel, M.J., 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.
75. Mizuguchi, H., Miyagi, K., Terao, T., Sakamoto, N., Yamawaki, Y., Adachi, T., Ono, S., Sasaki, Y., Yoshimura, Y., Kitamura, Y., et al. (2012) PMA-induced dissociation of Ku86 from the promoter causes transcriptional up-regulation of histamine H(1) receptor. Sci. Rep., 2, 916.
76. Konat, G.W. (2003) H2O2-induced higher order chromatin degradation: a novel mechanism of oxidative genotoxicity. J. Biosci., 28, 57-60.
77. Shin, J.H., Lee, H.K., Lee, H.B., Jin, Y. and Lee, J.K. (2014) Ethyl pyruvate inhibits HMGB1 phosphorylation and secretion in activated microglia and in the postischemic brain. Neurosci. Lett., 558, 159-163.
78. Burkle, A. and Virag, L. (2013) Poly(ADP-ribose): PARadigms and PARadoxes. Mol. Aspects Med., 34, 1046-1065.
79. Scaffidi, P., Misteli, T. and Bianchi, M.E. (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature, 418, 191-195.
80. Klune, J.R., Dhupar, R., Cardinal, J., Billiar, T.R. and Tsung, A. (2008) HMGB1: endogenous danger signaling. Mol. Med., 14, 476-484.
81. Davis, K., Banerjee, S., Friggeri, A., Bell, C., Abraham, E. and Zerfaoui, M. (2012) Poly(ADP-ribosyl)ation of high mobility group box 1 (HMGB1) protein enhances inhibition of efferocytosis. Mol. Med., 18, 359-369.