Low-dose radiation differentially regulates protein acetylation and histone deacetylase expression in human coronary artery endothelial cells

References

• Azimzadeh O, Barjaktarovic Z, Aubele M, Calzada-Wack J, Sarioglu H, Atkinson MJ, Tapio S. 2010. Formalin-fixed paraffin-embedded (FFPE) proteome analysis using gel-free and gel-based proteomics. J Proteome Res. 9:4710–4720.
   PubMed Web of Science ®Google Scholar
• Azimzadeh O, Scherthan H, Yentrapalli R, Barjaktarovic Z, Ueffing M, Conrad M, Neff F, Calzada-Wack J, Aubele M, Buske C, et al. 2012. Label-free protein profiling of formalin-fixed paraffin-embedded (FFPE) heart tissue reveals immediate mitochondrial impairment after ionising radiation. J Proteomics. 75:2384–2395.
   PubMed Web of Science ®Google Scholar
• Azimzadeh O, Sievert W, Sarioglu H, Merl-Pham J, Yentrapalli R, Bakshi MV, Janik D, Ueffing M, Atkinson MJ, Multhoff G, et al. 2015. Integrative proteomics and targeted transcriptomics analyses in cardiac endothelial cells unravel mechanisms of long-term radiation-induced vascular dysfunction. J Proteome Res. 14:1203–1219.
   PubMed Web of Science ®Google Scholar
• Barjaktarovic Z, Kempf SJ, Sriharshan A, Merl-Pham J, Atkinson MJ, Tapio S. 2015. Ionizing radiation induces immediate protein acetylation changes in human cardiac microvascular endothelial cells. J Radiat Res. 56:623–632.
   PubMed Web of Science ®Google Scholar
• Beli P, Lukashchuk N, Wagner SA, Weinert BT, Olsen JV, Baskcomb L, Mann M, Jackson SP, Choudhary C. 2012. Proteomic investigations reveal a role for RNA processing factor THRAP3 in the DNA damage response. Mol Cell. 46:212–225.
   PubMed Web of Science ®Google Scholar
• Boyault C, Sadoul K, Pabion M, Khochbin S. 2007. HDAC6, at the crossroads between cytoskeleton and cell signaling by acetylation and ubiquitination. Oncogene. 26:5468–5476.
   PubMed Web of Science ®Google Scholar
• Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M. 2009. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science. 325:834–840.
   PubMed Web of Science ®Google Scholar
• Coulton AT, East DA, Galinska-Rakoczy A, Lehman W, Mulvihill DP. 2010. The recruitment of acetylated and unacetylated tropomyosin to distinct actin polymers permits the discrete regulation of specific myosins in fission yeast. J Cell Sci. 123:3235–3243.
   PubMed Web of Science ®Google Scholar
• Cui C, Ren X, Liu D, Deng X, Qin X, Zhao X, Wang E, Yu B. 2014. 14-3-3 epsilon prevents G2/M transition of fertilized mouse eggs by binding with CDC25B. BMC Dev Biol. 14:33.
   PubMed Web of Science ®Google Scholar
• Darby S, McGale P, Peto R, Granath F, Hall P, Ekbom A. 2003. Mortality from cardiovascular disease more than 10 years after radiotherapy for breast cancer: nationwide cohort study of 90,000 Swedish women. BMJ. 326:256–257.
   PubMed Web of Science ®Google Scholar
• Darby SC, Ewertz M, McGale P, Bennet AM, Blom-Goldman U, Bronnum D, Correa C, Cutter D, Gagliardi G, Gigante B, et al. 2013. Risk of ischemic heart disease in women after radiotherapy for breast cancer. N Engl J Med. 368:987–998.
   PubMed Web of Science ®Google Scholar
• Delcuve GP, Khan DH, Davie JR. 2012. Roles of histone deacetylases in epigenetic regulation: emerging paradigms from studies with inhibitors. Clin Epigenetics. 4:5.
   PubMed Web of Science ®Google Scholar
• Fan LM, Douglas G, Bendall JK, McNeill E, Crabtree MJ, Hale AB, Mai A, Li JM, McAteer MA, Schneider JE, et al. 2014. Endothelial cell-specific reactive oxygen species production increases susceptibility to aortic dissection. Circulation. 129:2661–2672.
   PubMed Web of Science ®Google Scholar
• Ferguson BS, McKinsey TA. 2015. Non-sirtuin histone deacetylases in the control of cardiac aging. J Mol Cell Cardiol. 83:14–20.
   PubMed Web of Science ®Google Scholar
• Frye RA. 2000. Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem Biophys Res Commun. 273:793–798.
   PubMed Web of Science ®Google Scholar
• Gupta MP, Samant SA, Smith SH, Shroff SG. 2008. HDAC4 and PCAF bind to cardiac sarcomeres and play a role in regulating myofilament contractile activity. J Biol Chem. 283:10135–10146.
   PubMed Web of Science ®Google Scholar
• Hancock SL, Donaldson SS, Hoppe RT. 1993. Cardiac disease following treatment of Hodgkin's disease in children and adolescents. J Clin Oncol. 11:1208–1215.
   PubMed Web of Science ®Google Scholar
• Hauck SM, Dietter J, Kramer RL, Hofmaier F, Zipplies JK, Amann B, Feuchtinger A, Deeg CA, Ueffing M. 2010. Deciphering membrane-associated molecular processes in target tissue of autoimmune uveitis by label-free quantitative mass spectrometry. Mol Cell Proteomics. 9:2292–2305.
   PubMed Web of Science ®Google Scholar
• Hayes MJ, Rescher U, Gerke V, Moss SE. 2004. Annexin-actin interactions. Traffic. 5:571–576.
   PubMed Web of Science ®Google Scholar
• He W, Newman JC, Wang MZ, Ho L, Verdin E. 2012. Mitochondrial sirtuins: regulators of protein acylation and metabolism. Trends Endocrinol Metab. 23:467–476.
   PubMed Web of Science ®Google Scholar
• Hennenberg M, Biecker E, Trebicka J, Jochem K, Zhou Q, Schmidt M, Jakobs KH, Sauerbruch T, Heller J. 2006. Defective RhoA/Rho-kinase signaling contributes to vascular hypocontractility and vasodilation in cirrhotic rats. Gastroenterology. 130:838–854.
   PubMed Web of Science ®Google Scholar
• Heverin M, Brennan GP, Koehler CJ, Treumann A, Henshall DC. 2012. Proteomic analysis of 14-3-3 zeta binding proteins in the mouse hippocampus. Int J Physiol Pathophysiol Pharmacol. 4:74–83.
   PubMedGoogle Scholar
• Ishizuka Y, Shimizu H, Takagi E, Kato M, Yamagata H, Mikuni M, Shirao T. 2014. Histone deacetylase mediates the decrease in drebrin cluster density induced by amyloid beta oligomers. Neurochem Int. 76:114–121.
   PubMed Web of Science ®Google Scholar
• Jackson AE, Carraway KL 3rd, Payne ME, Means AR, Puett D, Brew K. 1987. Association of calmodulin and smooth muscle myosin light chain kinase: application of a label selection technique with trace acetylated calmodulin. Proteins. 2:202–209.
   PubMed Web of Science ®Google Scholar
• Jackson SE. 2013. Hsp90: structure and function. Top Curr Chem. 328:155–240.
   PubMed Web of Science ®Google Scholar
• Karve TM, Cheema AK. 2011. Small changes huge impact: the role of protein posttranslational modifications in cellular homeostasis and disease. J Amino Acids. 207691.
   PubMedGoogle Scholar
• Kawaguchi Y, Kovacs JJ, McLaurin A, Vance JM, Ito A, Yao TP. 2003. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell. 115:727–738.
   PubMed Web of Science ®Google Scholar
• Kekatpure VD, Dannenberg AJ, Subbaramaiah K. 2009. HDAC6 modulates Hsp90 chaperone activity and regulates activation of aryl hydrocarbon receptor signaling. J Biol Chem. 284:7436–7445.
   PubMed Web of Science ®Google Scholar
• Kovacs JJ, Murphy PJ, Gaillard S, Zhao X, Wu JT, Nicchitta CV, Yoshida M, Toft DO, Pratt WB, Yao TP. 2005. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol Cell. 18:601–607.
   PubMed Web of Science ®Google Scholar
• Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680–685.
   PubMed Web of Science ®Google Scholar
• Lee KK, Workman JL. 2007. Histone acetyltransferase complexes: one size doesn’t fit all. Nat Rev Mol Cell Biol. 8:284–295.
   PubMed Web of Science ®Google Scholar
• Li J, Buchner J. 2013. Structure, function and regulation of the hsp90 machinery. Biomed J. 36:106–117.
   PubMedGoogle Scholar
• Little MP, Azizova TV, Bazyka D, Bouffler SD, Cardis E, Chekin S, Chumak VV, Cucinotta FA, de Vathaire F, Hall P, et al. 2012. Systematic review and meta-analysis of circulatory disease from exposure to low-level ionizing radiation and estimates of potential population mortality risks. Environ Health Perspect. 120:1503–1511.
   PubMed Web of Science ®Google Scholar
• Little MP, Tawn EJ, Tzoulaki I, Wakeford R, Hildebrandt G, Paris F, Tapio S, Elliott P. 2008. A systematic review of epidemiological associations between low and moderate doses of ionizing radiation and late cardiovascular effects, and their possible mechanisms. Radiat Res. 169:99–109.
   PubMed Web of Science ®Google Scholar
• Little MP, Tawn EJ, Tzoulaki I, Wakeford R, Hildebrandt G, Paris F, Tapio S, Elliott P. 2010. Review and meta-analysis of epidemiological associations between low/moderate doses of ionizing radiation and circulatory disease risks, and their possible mechanisms. Radiat Environ Biophys. 49:139–153.
   PubMed Web of Science ®Google Scholar
• Lowe D, Raj K. 2014. Premature aging induced by radiation exhibits pro-atherosclerotic effects mediated by epigenetic activation of CD44 expression. Aging Cell. 13:900–910.
   PubMed Web of Science ®Google Scholar
• Maekawa M, Ishizaki T, Boku S, Watanabe N, Fujita A, Iwamatsu A, Obinata T, Ohashi K, Mizuno K, Narumiya S. 1999. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science. 285:895–898.
   PubMed Web of Science ®Google Scholar
• Marcu MG, Doyle M, Bertolotti A, Ron D, Hendershot L, Neckers L. 2002. Heat shock protein 90 modulates the unfolded protein response by stabilizing IRE1alpha. Mol Cell Biol. 22:8506–8513.
   PubMed Web of Science ®Google Scholar
• Masiero L, Lapidos KA, Ambudkar I, Kohn EC. 1999. Regulation of the RhoA pathway in human endothelial cell spreading on type IV collagen: role of calcium influx. J Cell Sci. 112(Pt 19):3205–3213.
   PubMed Web of Science ®Google Scholar
• Menendez JC, Casanova D, Amado JA, Salas E, Garcia-Unzueta MT, Fernandez F, de la Lastra LP, Berrazueta JR. 1998. Effects of radiation on endothelial function. Int J Radiat Oncol Biol Phys. 41:905–913.
   PubMed Web of Science ®Google Scholar
• Morris BJ. 2013. Seven sirtuins for seven deadly diseases of aging. Free Radic Biol Med. 56:133–171.
   PubMed Web of Science ®Google Scholar
• Niemantsverdriet M, Wagner K, Visser M, Backendorf C. 2008. Cellular functions of 14-3-3 zeta in apoptosis and cell adhesion emphasize its oncogenic character. Oncogene. 27:1315–1319.
   PubMed Web of Science ®Google Scholar
• Onyango P, Celic I, McCaffery JM, Boeke JD, Feinberg AP. 2002. SIRT3, a human SIR2 homologue, is an NAD-dependent deacetylase localized to mitochondria. Proc Natl Acad Sci USA. 99:13653–13658.
   PubMed Web of Science ®Google Scholar
• Popoff MR, Geny B. 2009. Multifaceted role of Rho, Rac, Cdc42 and Ras in intercellular junctions, lessons from toxins. Biochim Biophys Acta. 1788:797–812.
   PubMed Web of Science ®Google Scholar
• Priviero FB, Jin LM, Ying Z, Teixeira CE, Webb RC. 2010. Up-regulation of the RhoA/Rho-kinase signaling pathway in corpus cavernosum from endothelial nitric-oxide synthase (NOS), but not neuronal NOS, null mice. J Pharmacol Exp Ther. 333:184–192.
   PubMed Web of Science ®Google Scholar
• Psatha MI, Razi M, Koffer A, Moss SE, Sacks DB, Bolsover SR. 2007. Targeting of calcium:calmodulin signals to the cytoskeleton by IQGAP1. Cell Calcium. 41:593–605.
   PubMed Web of Science ®Google Scholar
• Rao R, Fiskus W, Yang Y, Lee P, Joshi R, Fernandez P, Mandawat A, Atadja P, Bradner JE, Bhalla K. 2008. HDAC6 inhibition enhances 17-AAG–mediated abrogation of hsp90 chaperone function in human leukemia cells. Blood. 112:1886–1893.
   PubMed Web of Science ®Google Scholar
• Samant SA, Courson DS, Sundaresan NR, Pillai VB, Tan M, Zhao Y, Shroff SG, Rock RS, Gupta MP. 2011. HDAC3-dependent reversible lysine acetylation of cardiac myosin heavy chain isoforms modulates their enzymatic and motor activity. J Biol Chem. 286:5567–5577.
   PubMed Web of Science ®Google Scholar
• Shahbazian MD, Grunstein M. 2007. Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem. 76:75–100.
   PubMed Web of Science ®Google Scholar
• Shimizu Y, Kodama K, Nishi N, Kasagi F, Suyama A, Soda M, Grant EJ, Sugiyama H, Sakata R, Moriwaki H, et al. 2010. Radiation exposure and circulatory disease risk: Hiroshima and Nagasaki atomic bomb survivor data, 1950–2003. BMJ. 340:b5349.
   PubMed Web of Science ®Google Scholar
• Soe NN, Sowden M, Baskaran P, Kim Y, Nigro P, Smolock EM, Berk BC. 2014. Acetylation of cyclophilin A is required for its secretion and vascular cell activation. Cardiovasc Res. 101:444–453.
   PubMed Web of Science ®Google Scholar
• Soloviev AI, Tishkin SM, Parshikov AV, Ivanova IV, Goncharov EV, Gurney AM. 2003. Mechanisms of endothelial dysfunction after ionized radiation: selective impairment of the nitric oxide component of endothelium-dependent vasodilation. Br J Pharmacol. 138:837–844.
   PubMed Web of Science ®Google Scholar
• Sriharshan A, Boldt K, Sarioglu H, Barjaktarovic Z, Azimzadeh O, Hieber L, Zitzelsberger H, Ueffing M, Atkinson MJ, Tapio S. 2012. Proteomic analysis by SILAC and 2D-DIGE reveals radiation-induced endothelial response: Four key pathways. J Proteomics. 75:2319–2330.
   PubMed Web of Science ®Google Scholar
• Sugihara T, Hattori Y, Yamamoto Y, Qi F, Ichikawa R, Sato A, Liu MY, Abe K, Kanno M. 1999. Preferential impairment of nitric oxide-mediated endothelium-dependent relaxation in human cervical arteries after irradiation. Circulation. 100:635–641.
   PubMed Web of Science ®Google Scholar
• Tsai YC, Greco TM, Cristea IM. 2014. Sirtuin 7 plays a role in ribosome biogenesis and protein synthesis. Mol Cell Proteomics. 13:73–83.
   PubMed Web of Science ®Google Scholar
• Uehara K, Uehara A. 2010. Vimentin intermediate filaments: the central base in sinus endothelial cells of the rat spleen. Anat Rec (Hoboken). 293:2034–2043.
   PubMedGoogle Scholar
• Valencia RG, Walko G, Janda L, Novacek J, Mihailovska E, Reipert S, Andra-Marobela K, Wiche G. 2013. Intermediate filament-associated cytolinker plectin 1c destabilizes microtubules in keratinocytes. Mol Biol Cell. 24:768–784.
   PubMed Web of Science ®Google Scholar
• van Nieuw Amerongen GP, van Delft S, Vermeer MA, Collard JG, van Hinsbergh VW. 2000. Activation of RhoA by thrombin in endothelial hyperpermeability: role of Rho kinase and protein tyrosine kinases. Circ Res. 87:335–340.
   PubMed Web of Science ®Google Scholar
• Vijg J, Maslov AY, Suh Y. 2008. Aging: a sirtuin shake-up? Cell. 135:797–798.
   PubMed Web of Science ®Google Scholar
• Zuo S, Xue Y, Tang S, Yao J, Du R, Yang P, Chen X. 2010. 14-3-3 epsilon dynamically interacts with key components of mitogen-activated protein kinase signal module for selective modulation of the TNF-alpha-induced time course-dependent NF-kappaB activity. J Proteome Res. 9:3465–3478.
   PubMed Web of Science ®Google Scholar