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TRANSCRIPTIC PROFILE OF CHRONICLY IRRADIATED CELLS

Transcriptomic profiling suggests a role for IGFBP5 in premature senescence of endothelial cells after chronic low dose rate irradiation

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Pages 560-574 | Received 05 Nov 2013, Accepted 25 Feb 2014, Published online: 19 Mar 2014

References

  • Abengozar MA, de Frutos S, Ferreiro S, Soriano J, Perez-Martinez M, Olmeda D, Marenchino M, Canamero M, Ortega S, Megias D, Rodriguez A, Martinez-Torrecuadrada JL. 2012. Blocking ephrinB2 with highly specific antibodies inhibits angiogenesis, lymphangiogenesis, and tumor growth. Blood 119:4565–4576.
  • Aihara K. 2010. Heparin cofactor II attenuates vascular remodeling in humans and mice. Circulation J 74:1518–1523.
  • Amundson SA. 2008. Functional genomics in radiation biology: A gateway to cellular systems-level studies. Radiat Environ Biophys 47:25–31.
  • Ashmore JP, Krewski D, Zielinski JM, Jiang H, Semenciw R, Band PR. 1998. First analysis of mortality and occupational radiation exposure based on the National Dose Registry of Canada. Am J Epidemiol 148:564–574.
  • Azizova TV, Muirhead CR, Druzhinina MB, Grigoryeva ES, Vlasenko EV, Sumina MV, O’Hagan JA, Zhang W, Haylock RG, Hunter N. 2010. Cardiovascular diseases in the cohort of workers first employed at Mayak PA in 1948–1958. Radiat Res 174:155–168.
  • Baek JY, Jun DY, Taub D, Kim YH. 2003. Characterization of human phosphoserine aminotransferase involved in the phosphorylated pathway of L-serine biosynthesis. Biochem J 373:191–200.
  • Baker JE, Moulder JE, Hopewell JW. 2011. Radiation as a risk factor for cardiovascular disease. Antioxid Redox Signal 15:1945–1956.
  • Beattie J, Allan GJ, Lochrie JD, Flint DJ. 2006. Insulin-like growth factor-binding protein-5 (IGFBP-5): A critical member of the IGF axis. Biochem J 395:1–19.
  • Ben-Porath I, Weinberg RA. 2005. The signals and pathways activating cellular senescence. Int J Biochem Cell Biol 37:961–976.
  • Boothman DA, Wang M, Lee SW. 1991. Induction of tissue-type plasminogen activator by ionizing radiation in human malignant melanoma cells. Cancer Res 51:5587–5595.
  • Borghini A, Luca Gianicolo EA, Picano E, Andreassi MG. 2013. Ionizing radiation and atherosclerosis: Current knowledge and future challenges. Atherosclerosis 230:40–47.
  • Braun J, Hoffmann SC, Feldner A, Ludwig T, Henning R, Hecker M, Korff T. 2011. Endothelial cell ephrinB2-dependent activation of monocytes in arteriosclerosis. Arterioscler, Thromb Vasc Biol 31:297–305.
  • Buers I, Hofnagel O, Ruebel A, Severs NJ, Robenek H. 2011. Lipid droplet associated proteins: An emerging role in atherogenesis. Histol Histopathol 26:631–642.
  • Campisi J, d’Adda di Fagagna F. 2007. Cellular senescence: When bad things happen to good cells. Nature Rev Molec Cell Biol 8:729–740.
  • Chen Y, Johansson E, Fan Y, Shertzer HG, Vasiliou V, Nebert DW, Dalton TP. 2009. Early onset senescence occurs when fibroblasts lack the glutamate-cysteine ligase modifier subunit. Free Rad Biol Med 47:410–418.
  • Donninger H, Hesson L, Vos M, Beebe K, Gordon L, Sidransky D, Liu JW, Schlegel T, Payne S, Hartmann A, Latif F, Clark GJ. 2010. The Ras effector RASSF2 controls the PAR-4 tumor suppressor. Molec Cellular Biol 30:2608–2620.
  • El-Saghire H, Thierens H, Monsieurs P, Michaux A, Vandevoorde C, Baatout S. 2013. Gene set enrichment analysis highlights different gene expression profiles in whole blood samples X-irradiated with low and high doses. Int J Radiat Biol 89:628–638.
  • El Assar M, Angulo J, Vallejo S, Peiro C, Sanchez-Ferrer CF, Rodriguez-Manas L. 2012. Mechanisms involved in the aging- induced vascular dysfunction. Frontiers in Physiol 3:132.
  • Erusalimsky JD. 2009. Vascular endothelial senescence: From mechanisms to pathophysiology. J Appl Physiol 106:326–332.
  • Favaro E, Bensaad K, Chong MG, Tennant DA, Ferguson DJ, Snell C, Steers G, Turley H, Li JL, Gunther UL, Buffa FM, McIntyre A, Harris AL. 2012. Glucose utilization via glycogen phosphorylase sustains proliferation and prevents premature senescence in cancer cells. Cell Metabol 16:751–764.
  • Fridman AL, Tainsky MA. 2008. Critical pathways in cellular senescence and immortalization revealed by gene expression profiling. Oncogene 27:5975–5987.
  • Fujita M, Momose A, Ohtomo T, Nishinosono A, Tanonaka K, Toyoda H, Morikawa M, Yamada J. 2011. Upregulation of fatty acyl-CoA thioesterases in the heart and skeletal muscle of rats fed a high-fat diet. Biolog Pharmaceut Bull 34:87–91.
  • Furuya S, Yoshida K, Kawakami Y, Yang JH, Sayano T, Azuma N, Tanaka H, Kuhara S, Hirabayashi Y. 2008. Inactivation of the 3-phosphoglycerate dehydrogenase gene in mice: Changes in gene expression and associated regulatory networks resulting from serine deficiency. Function Integrat Genom 8:235–249.
  • Grillari J, Hohenwarter O, Grabherr RM, Katinger H. 2000. Subtractive hybridization of mRNA from early passage and senescent endothelial cells. Experim Gerontol 35:187–197.
  • Hay N, Sonenberg N. 2004. Upstream and downstream of mTOR. Genes Develop 18:1926–1945.
  • Hayflick L. 1965. The limited in vitro lifetime of human diploid cell strains. Experim Cell Res 37:614–636.
  • Hendry JH, Simon SL, Wojcik A, Sohrabi M, Burkart W, Cardis E, Laurier D, Tirmarche M, Hayata I. 2009. Human exposure to high natural background radiation: What can it teach us about radiation risks?J Radiolog Protect 29:A29–42.
  • Hermanova I, Zaliova M, Trka J, Starkova J. 2012. Low expression of asparagine synthetase in lymphoid blasts precludes its role in sensitivity to L-asparaginase. Experim Hematol 40:657–665.
  • Ivanov VK, Maksioutov MA, Chekin SY, Petrov AV, Biryukov AP, Kruglova ZG, Matyash VA, Tsyb AF, Manton KG, Kravchenko JS. 2006. The risk of radiation-induced cerebrovascular disease in Chernobyl emergency workers. Health Phys 90:199–207.
  • Jackson SP, Bartek J. 2009. The DNA-damage response in human biology and disease. Nature 461:1071–1078.
  • Jiang Z, Gentleman R. 2007. Extensions to gene set enrichment. Bioinformatics 23:306–313.
  • Kamino H, Hiratsuka M, Toda T, Nishigaki R, Osaki M, Ito H, Inoue T, Oshimura M. 2003. Searching for genes involved in arteriosclerosis: Proteomic analysis of cultured human umbilical vein endothelial cells undergoing replicative senescence. Cell Struct Funct 28:495–503.
  • Keppler D, Zhang J, Bihani T, Lin AW. 2011. Novel expression of CST1 as candidate senescence marker. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 66:723–731.
  • Kim KS, Kim JE, Choi KJ, Bae S, Kim DH. 2014. Characterization of DNA damage-induced cellular senescence by ionizing radiation in endothelial cells. Int J Radiat Biol 90:71–80.
  • Kim KS, Seu YB, Baek SH, Kim MJ, Kim KJ, Kim JH, Kim JR. 2007. Induction of cellular senescence by insulin-like growth factor binding protein-5 through a p53-dependent mechanism. Molec Biol Cell 18:4543–4552.
  • Kletsas D, Pratsinis H, Mariatos G, Zacharatos P, Gorgoulis VG. 2004. The proinflammatory phenotype of senescent cells: The p53-mediated ICAM-1 expression. Ann NY Acad Sci 1019:330–332.
  • Kong Y, Cui H, Zhang H. 2011. Smurf2-mediated ubiquitination and degradation of Id1 regulates p16 expression during senescence. Aging Cell 10:1038–1046.
  • Kortlever RM, Bernards R. 2006. Senescence, wound healing and cancer: The PAI-1 connection. Cell Cycle 5:2697–2703.
  • Kurz DJ, Decary S, Hong Y, Trivier E, Akhmedov A, Erusalimsky JD. 2004. Chronic oxidative stress compromises telomere integrity and accelerates the onset of senescence in human endothelial cells. J Cell Sci 117:2417–2426.
  • Ladenvall P, Nilsson S, Jood K, Rosengren A, Blomstrand C, Jern C. 2003. Genetic variation at the human tissue-type plasminogen activator (tPA) locus: Haplotypes and analysis of association to plasma levels of tPA. Eur J Human Genet 11:603–610.
  • Landmesser U, Hornig B, Drexler H. 2004. Endothelial function: A critical determinant in atherosclerosis?Circulation 109:II27–33.
  • Laplante M, Sabatini DM. 2012. mTOR signaling in growth control and disease. Cell 149:274–293.
  • Latini FR, Hemerly JP, Freitas BC, Oler G, Riggins GJ, Cerutti JM. 2011. ABI3 ectopic expression reduces in vitro and in vivo cell growth properties while inducing senescence. BMC Cancer 11:11.
  • Libby P. 2006. Inflammation and cardiovascular disease mechanisms. Am J Clin Nutrit 83:456S–460S.
  • Libby P, Ridker PM, Hansson GK. 2011. Progress and challenges in translating the biology of atherosclerosis. Nature 473:317–325.
  • Licciulli S, Luise C, Scafetta G, Capra M, Giardina G, Nuciforo P, Bosari S, Viale G, Mazzarol G, Tonelli C, Lanfrancone L, Alcalay M. 2011. Pirin inhibits cellular senescence in melanocytic cells. Am J Pathol 178:2397–2406.
  • Little MP, Azizova TV, Bazyka D, Bouffler SD, Cardis E, Chekin S, Chumak VV, Cucinotta FA, de Vathaire F, 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.
  • McGeoghegan D, Binks K, Gillies M, Jones S, Whaley S. 2008. The non-cancer mortality experience of male workers at British Nuclear Fuels plc, 1946–2005. Int J Epidemiol 37:506–518.
  • McMillan TJ, Bennett MR, Bridges BA, Hendry J, Jones B, Kanthou C, Little MP, Taylor A, Tzoulaki I, Bouffler SD, Zhang W, Walker H, Keep P. 2010. Circulatory disease risk. Report of the independentAdvisory Group on Ionising Radiation.
  • Merico D, Isserlin R, Stueker O, Emili A, Bader GD. 2010. Enrichment map: A network-based method for gene-set enrichment visualization and interpretation. PLoS One 5:e13984.
  • Michiels C. 2003. Endothelial cell functions. J Cellul Physiol 196:430–443.
  • Minamino T, Komuro I. 2007. Vascular cell senescence: Contribution to atherosclerosis. Circulat Res 100:15–26.
  • Minamino T, Miyauchi H, Yoshida T, Ishida Y, Yoshida H, Komuro I. 2002. Endothelial cell senescence in human atherosclerosis: Role of telomere in endothelial dysfunction. Circulation 105: 1541–1544.
  • Mittal S, Aslam A, Doidge R, Medica R, Winkler GS. 2011. The Ccr4a (CNOT6) and Ccr4b (CNOT6L) deadenylase subunits of the human Ccr4-Not complex contribute to the prevention of cell death and senescence. Molec Biol Cell 22:748–758.
  • Molenaar TJ, Twisk J, de Haas SA, Peterse N, Vogelaar BJ, van Leeuwen SH, Michon IN, van Berkel TJ, Kuiper J, Biessen EA. 2003. P-selectin as a candidate target in atherosclerosis. Biochem Pharmacol 66:859–866.
  • Moser M, Bauer M, Schmid S, Ruppert R, Schmidt S, Sixt M, Wang HV, Sperandio M, Fassler R. 2009. Kindlin-3 is required for beta2 integrin-mediated leukocyte adhesion to endothelial cells. Nature Med 15:300v305.
  • Ogami M, Ikura Y, Ohsawa M, Matsuo T, Kayo S, Yoshimi N, Hai E, Shirai N, Ehara S, Komatsu R, Naruko T, Ueda M. 2004. Telomere shortening in human coronary artery diseases. Arterioscler, Thromb Vasc Biol 24:546–550.
  • Pernot E, Hall J, Baatout S, Benotmane MA, Blanchardon E, Bouffler S, El Saghire H, Gomolka M, Guertler A, et al. 2012. Ionizing radiation biomarkers for potential use in epidemiological studies. Mutat Res 751:258–286.
  • Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:6.
  • Robert P, Canault M, Farnarier C, Nurden A, Grosdidier C, Barlogis V, Bongrand P, Pierres A, Chambost H, Alessi MC, 2011. A novel leukocyte adhesion deficiency III variant: Kindlin-3 deficiency results in integrin- and nonintegrin-related defects in different steps of leukocyte adhesion. J Immunol 186:5273–5283.
  • Schneider LP, Pellegatta S, Favaro R, Pisata F, Roncaglia P, Testa G, Nicolis SK, Finocchiaro G, d’Adda di Fagagna F. 2013. DNA damage in mammalian neural stem cells leads to astrocytic differentiation mediated by BMP2 signaling through JAK-STAT. Stem Cell Rep 1:123–138.
  • Schollnberger H, Kaiser JC, Jacob P, Walsh L. 2012. Dose-responses from multi-model inference for the non-cancer disease mortality of atomic bomb survivors. Radiat Environ Biophys 51:165–178.
  • Shackelford RE, Kaufmann WK, Paules RS. 1999. Cell cycle control, checkpoint mechanisms, and genotoxic stress. Environ Health Perspect 107(Suppl. 1):5–24.
  • Shelton DN, Chang E, Whittier PS, Choi D, Funk WD. 1999. Microarray analysis of replicative senescence. Curr Biol 9:939–945.
  • Shimizu Y, Kodama K, Nishi N, Kasagi F, Suyama A, Soda M, Grant EJ, Sugiyama H, Sakata R, Moriwaki H, Hayashi M, Konda M, Shore RE. 2010. Radiation exposure and circulatory disease risk: Hiroshima and Nagasaki atomic bomb survivor data, 1950–2003. BMJ 340:b5349.
  • Sies H. 1999. Glutathione and its role in cellular functions. Free Rad Biol Med 27:916–921.
  • Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. 2005. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Nat Acad Sci USA 102:15545–15550.
  • Uchida N, Takahashi K, Kasai T, Ishida T, Kwaan HC. 1994. The concomitant augmentation of urokinase-type plasminogen activator and collagenase-like proteinase activities in X-ray irradiated cells of a human metastatic carcinomatous line. Thrombosis Res 74:565–576.
  • Ungvari Z, Kaley G, de Cabo R, Sonntag WE, Csiszar A. 2010. Mechanisms of vascular aging: New perspectives. J Gerontol A, Biolog Sci Med Sci 65:1028–1041.
  • Vasile E, Tomita Y, Brown LF, Kocher O, Dvorak HF. 2001. Differential expression of thymosin beta-10 by early passage and senescent vascular endothelium is modulated by VPF/VEGF: Evidence for senescent endothelial cells in vivo at sites of atherosclerosis. FASEB J 15:458–466.
  • Vavrova J, Rezacova M. 2011. The importance of senescence in ionizing radiation-induced tumour suppression. Folia Biolog 57:41–46.
  • Vicente CP, He L, Tollefsen DM. 2007. Accelerated atherogenesis and neointima formation in heparin cofactor II deficient mice. Blood 110:4261–4267.
  • Voghel G, Thorin-Trescases N, Farhat N, Nguyen A, Villeneuve L, Mamarbachi AM, Fortier A, Perrault LP, Carrier M, Thorin E. 2007. Cellular senescence in endothelial cells from atherosclerotic patients is accelerated by oxidative stress associated with cardiovascular risk factors. Mechan Ageing Develop 128:662–671.
  • Volcik KA, Catellier D, Folsom AR, Matijevic N, Wasserman B, Boerwinkle E. 2009. SELP and SELPLG genetic variation is associated with cell surface measures of SELP and SELPLG: The Atherosclerosis Risk in Communities Carotid MRI Study. Clin Chem 55:1076–1082.
  • Vos MD, Ellis CA, Elam C, Ulku AS, Taylor BJ, Clark GJ. 2003. RASSF2 is a novel K-Ras-specific effector and potential tumor suppressor. J Biolog Chem 278:28045–28051.
  • Wang JC, Bennett M. 2012. Aging and atherosclerosis: Mechanisms, functional consequences, and potential therapeutics for cellular senescence. Circulat Res 111:245–259.
  • West MD, Shay JW, Wright WE, Linskens MH. 1996. Altered expression of plasminogen activator and plasminogen activator inhibitor during cellular senescence. Experim Gerontol 31:175–193.
  • Wu MC, Lin X. 2009. Prior biological knowledge-based approaches for the analysis of genome-wide expression profiles using gene sets and pathways. Statist Meth Med Res 18:577–593.
  • Yan X, Baxter RC, Firth SM. 2010. Involvement of pregnancy- associated plasma protein-A2 in insulin-like growth factor (IGF) binding protein-5 proteolysis during pregnancy: A potential mechanism for increasing IGF bioavailability. J Clin Endocrinol Metabol 95:1412–1420.
  • Yentrapalli R, Azimzadeh O, Barjaktarovic Z, Sarioglu H, Wojcik A, Harms-Ringdahl M, Atkinson MJ, Haghdoost S, Tapio S. 2013a. Quantitative proteomic analysis reveals induction of premature senescence in human umbilical vein endothelial cells exposed to chronic low-dose rate gamma-radiation. Proteomics 13:1096–1107.
  • Yentrapalli R, Azimzadeh O, Sriharshan A, Malinowsky K, Merl J, Wojcik A, Harms-Ringdahl M, Atkinson MJ, Becker K-F, Haghdoost S, Tapio S. 2013b. The PI3K/Akt/mTOR pathway is implicated in the premature senescence of primary human endothelial cells exposed to chronic radiation. PLoS One8:e70024.
  • Zhan M, Han ZC. 2004. Phosphatidylinositide 3-kinase/AKT in radiation responses. Histol Histopathol 19:915–923.
  • Zhang H, Cohen SN. 2004. Smurf2 up-regulation activates telomere-dependent senescence. Genes Develop 18:3028–3040.

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