Integrative genomic and proteomic analyses identifies glycerol-3-phosphate acyltransferase as a target of low-dose ionizing radiation in EBV infected-B cells

References

• Akiba S. 2012. Epidemiological studies of Fukushima residents exposed to ionising radiation from the Fukushima Daiichi Nuclear Power Plant prefecture – a preliminary review of current plans. J Radiol Prot 32:1–10.
   PubMed Web of Science ®Google Scholar
• Allan JM, Travis LB. 2005. Mechanisms of therapy-related carcinogenesis. Nat Rev Cancer 5:943–955.
   PubMed Web of Science ®Google Scholar
• Belyakov OV, Malcolmson AM, Folkard M, Prise KM, Michael BD. 2001. Direct evidence for a bystander effect of ionizing radiation in primary human fibroblasts. Br J Cancer 84:674–679.
   PubMed Web of Science ®Google Scholar
• Bennett KL, Plowman GD, Buckley SD, Skonier J, Purchio AF. 1992. Regulation of amphiregulin mRNA by TGF-beta in the human lung adenocarcinoma cell line A549. Growth Factors 7:207–213.
   PubMedGoogle Scholar
• Brockmöller SF, Bucher E, Müller BM, Budczies J, Hilvo M, Griffin JL, Orešič M, Kallioniemi O, Iljin K, Loibl S, Darb-Esfahani S, Sinn BV, Klauschen F, Prinzler J, Bangemann N, Ismaeel F, Fiehn O, Dietel M, Denkert C. 2012. Integration of metabolomics and expression of glycerol-3-phosphate acyltransferase (GPAM) in breast cancer-link to patient survival, hormone receptor status, and metabolic profiling. J Proteome Res 11:850–860.
   PubMed Web of Science ®Google Scholar
• Calderwood MA, Venkatesan K, Xing L, Chase MR, Vazquez A, Holthaus AM, Ewence AE, Li N, Hirozane-Kishikawa T, Hill DE, Vidal M, Kieff E, Johannsen E. 2007. Epstein-Barr virus and virus human protein interaction maps. Proc Natl Acad Sci USA 104:7606–7611.
   PubMed Web of Science ®Google Scholar
• Cha HJ, Seong KM, Bae S, Jung JH, Kim CS, Yang KH, Jin YW, An S. 2009. Identification of specific microRNAs responding to low and high dose gamma-irradiation in the human lymphoblast line IM9. Oncol Rep 22:863–868.
   PubMed Web of Science ®Google Scholar
• Chaudhry MA. 2008. Biomarkers for human radiation exposure. J Biomed Sci 15:557–563.
   PubMed Web of Science ®Google Scholar
• Chaudhry MA, Kreger B, Omaruddin RA. 2010a. Transcriptional modulation of micro-RNA in human cells differing in radiation sensitivity. Int J Radiat Biol 86:569–583.
   PubMed Web of Science ®Google Scholar
• Chaudhry MA, Sachdeva H, Omaruddin RA. 2010b. Radiation-induced micro-RNA modulation in glioblastoma cells differing in DNA-repair pathways. DNA Cell Biol 29:553–561.
   PubMed Web of Science ®Google Scholar
• Danjoh I, Sone H, Shirota R, Hiroyama T, Nakamura Y. 2012. Development of a robust method for establishing B cell lines using Epstein-Barr Virus. In Vitro Cell Dev Biol Anim 48:393–402.
   PubMed Web of Science ®Google Scholar
• Datta A, Park JE, Li X, Zhang H, Ho ZS, Heese K, Lim SK, Tam JP, Sze SK. 2010. Phenotyping of an in vitro model of ischemic penumbra by iTRAQ-based shotgun quantitative proteomics. J Proteome Res 9:472–484.
   PubMed Web of Science ®Google Scholar
• Du S, Barcellos-Hoff MH. 2013. Tumors as organs: biologically augmenting radiation therapy by inhibiting transforming growth factor β activity in carcinomas. Semin Radiat Oncol 23:242–251.
   PubMed Web of Science ®Google Scholar
• Ekins S, Bugrim A, Brovold L, Kirillov E, Nikolsky Y, Rakhmatulin E, Sorokina S, Ryabov A, Serebryiskaya T, Melnikov A, Metz J, Nikolskaya T. 2006. Algorithms for network analysis in systems-ADME/Tox using the MetaCore and MetaDrug platforms. Xenobiotica 36:877–901.
   PubMed Web of Science ®Google Scholar
• Epstein MA, Achong BG, Barr YM. 1964. Virus particles in cultured lymphoblast from Burkitt’s lymphoma. Lancet 1:702–703.
   PubMed Web of Science ®Google Scholar
• Evans C, Noirel J, Ow SY, Salim M, Pereira-Medrano AG, Couto N, Pandhal J, Smith D, Pham TK, Karunakaran E, Zou X, Biggs CA, Wright PC. 2012. An insight into iTRAQ: where do we stand now? Anal Bioanal Chem 404:1011–1027.
   PubMed Web of Science ®Google Scholar
• Glen A, Gan CS, Hamdy FC, Eaton CL, Cross SS, Catto JW, Wright PC, Rehman I. 2008. iTRAQ-facilitated proteomic analysis of human prostate cancer cells identifies proteins associated with progression. J Proteome Res 7:897–907.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Baró MR, Lewin TM, Coleman RA. 2007. Regulation of Triglyceride metabolism. II. Function of mitochondrial GPAT1 in the regulation of triacylglycerol biosynthesis and insulin action. Am J Physiol Gastrointest Liver Physiol. 292:G1195–1199.
   PubMed Web of Science ®Google Scholar
• Hammond LE, Gallagher PA, Wang S, Hiller S, Kluckman KD, Posey-Marcos EL, Maeda N, Coleman RA. 2002. Mitochondrial glycerol-3-phosphate acyltransferase-deficient mice have reduced weight and liver triacylglycerol content and altered glycerolipid fatty acid composition. Mol Cell Biol 22:8204–8214.
   PubMed Web of Science ®Google Scholar
• Hanto DW, Gajl-Peczalska KJ, Frizzera G, Arthur DC, Balfour HH, McClain K, Simmons RL, Najarian JS. 1983. Epstein-Barr virus (EBV) induced polyclonal and monoclonal B-cell lymphoproliferative diseases occurring after renal transplantation. Clinical, pathologic, and virologic findings and implications for therapy. Ann Surg 198:356–369.
   PubMed Web of Science ®Google Scholar
• Henderson S, Rowe M, Gregory C, Croom-Carter D, Wang F, Longnecker R, Kieff E, Rickinson A. 1991. Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell 65:1107–1115.
   PubMed Web of Science ®Google Scholar
• Herbrich SM, Cole RN, West KP, Schulze K, Yager JD, Groopman JD, Christian P, Wu L, O’Meally RN, May DH, McIntosh MW, Ruczinski I. 2013. Statistical inference from multiple iTRAQ experiments without using common reference standards. J Proteome Res 12:594–604.
   PubMed Web of Science ®Google Scholar
• Huang YS, Kan MC, Lin CL, Richter JD. 2006. CPEB3 and CPEB4 in neurons: analysis of RNA-binding specificity and translational control of AMPA receptor GluR2 mRNA. EMBO J 25:4865–4876.
   PubMed Web of Science ®Google Scholar
• Ishikawa K, Ishii H, Saito T. 2006. DNA damage-dependent cell cycle checkpoints and genomic stability. DNA Cell Biol 25:406–411.
   PubMed Web of Science ®Google Scholar
• Kadhim MA, Moore SR, Goodwin EH. 2004. Interrelationships amongst radiation-induced genomic instability, bystander effects, and the adaptive response. Mutat Res 568:21–32.
   PubMed Web of Science ®Google Scholar
• Kobayashi D, Kumagai J, Morikawa T, Wilson-Morifuji M, Wilson A, Irie A, Araki N. 2009. An integrated approach of differential mass spectrometry and gene ontology analysis identified novel proteins regulating neuronal differentiation and survival. Mol Cell Proteomics 8:2350–2367.
   PubMed Web of Science ®Google Scholar
• Lhakhang TW, Chaudhry MA. 2012. Interactome of radiation-induced microRNA-predicted target genes. Comp Funct Genomic 2012:569731.
   PubMedGoogle Scholar
• Liu H, Fu X, Ji W, Bao L, Yan Y, Wu M, Yang J, Su C. 2013. Human sulfatase-1 inhibits the migration and proliferation of SMMC-7721 hepatocellular carcinoma cells by downregulating the growth factor signalling. Hepatol Res 43: 516-525
   Google Scholar
• Maes OC, An J, Sarojini H, Wu H, Wang E. 2008. Changes in MicroRNA expression patterns in human fibroblasts after low-LET radiation. J Cell Biochem 105:824–834.
   PubMed Web of Science ®Google Scholar
• Marsit CJ, Eddy K, Kelsey KT. 2006. MicroRNA responses to cellular stress. Cancer Res 66:10843–10848.
   PubMed Web of Science ®Google Scholar
• Milella M, Kornblau SM, Estrov Z, Carter BZ, Lapillonne H, Harris D, Konopleva M, Zhao S, Estey E, Andreeff M. 2001. Therapeutic targeting of the MEK/MAPK signal transduction module in acute myeloid leukemia. J Clin Invest 108:851–859.
   PubMed Web of Science ®Google Scholar
• Misra S, Heldin P, Hascall VC, Karamanos NK, Skandalis SS, Markwald RR, Ghatak S. 2011. Hyaluronan-CD44 interactions as potential targets for cancer therapy. FEBS J 278:1429–1443.
   PubMed Web of Science ®Google Scholar
• Morgan WF, Sowa MB. 2009. Non-targeted effects of ionizing radiation: implications for risk assessment and the radiation dose response profile. Health Phys 97:426–432.
   PubMed Web of Science ®Google Scholar
• Nilsen TW. 2007. Mechanisms of microRNA-mediated gene regulation in animal cells. Trends Genet 23:243–249.
   PubMed Web of Science ®Google Scholar
• Pant MC, Liao XY, Lu Q, Molloi S, Elmore E, Redpath JL. 2003. Mechanisms of suppression of neoplastic transformation in vitro by low doses of low LET radiation. Carcinogenesis 24:1961–1965.
   PubMed Web of Science ®Google Scholar
• Prise KM, Belyakov OV, Folkard M, Michael BD. 1998. Studies of bystander effects in human fibroblasts using a charged particle microbeam. Int J Radiat Biol 74:793–798.
   PubMed Web of Science ®Google Scholar
• Prise KM, O’Sullivan JM. 2009. Radiation-induced bystander signalling in cancer therapy. Nat Rev Cancer 9:351–360.
   PubMed Web of Science ®Google Scholar
• Purtilo DT, Sakamoto K, Barnabei V, Seeley J, Bechtold T, Rogers G, Yetz J, Harada S. 1982. Epstein-Barr virus-induced diseases in boys with the X-linked lymphoproliferative syndrome (XLP): update on studies of the registry. Am J Med 73:49–56.
   PubMed Web of Science ®Google Scholar
• Saenko V, Ivanov V, Tsyb A, Bogdanova T, Tronko M, Demidchik Y, Yamashita S. 2011. The Chernobyl accident and its consequences. Clin Oncol (R Coll Radiol) 23:234–243.
   PubMed Web of Science ®Google Scholar
• Sasai K, Shibamoto Y, Takahashi M, Zhou L, Hori H, Nagasawa H, Shibata T, Inayama S, Abe M. 1990. KIH-802, an acetohydroxamic acid derivative of 2-nitroimidazole, as a new potent hypoxic cell radiosensitizer: radiosensitizing activity, acute toxicity, and pharmacokinetics. Cancer Chemother Pharmacol 26:112–116.
   PubMed Web of Science ®Google Scholar
• Sasaki MS, Ejima Y, Tachibana A, Yamada T, Ishizaki K, Shimizu T, Nomura T. 2002. DNA damage response pathway in radioadaptive response. Mutat Res 504:101–118.
   PubMed Web of Science ®Google Scholar
• Sasaki MS, Tachibana A, Takeda S. 2014. Cancer risk at low doses of ionizing radiation: artificial neural networks inference from atomic bomb survivors. J Radiat Res 55:391–406.
   PubMed Web of Science ®Google Scholar
• Shao C, Furusawa Y, Aoki M, Matsumoto H, Ando K. 2002. Nitric oxide-mediated bystander effect induced by heavy-ions in human salivary gland tumour cells. Int J Radiat Biol 78:837–844.
   PubMed Web of Science ®Google Scholar
• Takayama S, Reed JC, Homma S. 2003. Heat-shock proteins as regulators of apoptosis. Oncogene 22:9041–9047.
   PubMed Web of Science ®Google Scholar
• Taki K, Wang B, Nakajima T, Wu J, Ono T, Uehara Y, Matsumoto T, Oghiso Y, Tanaka K, Ichinohe K, Nakamura S, Tanaka S, Magae J, Kakimoto A, Nenoi M. 2009. Microarray analysis of differentially expressed genes in the kidneys and testes of mice after long-term irradiation with low-dose-rate gamma-rays. J Radiat Res 50:241–252.
   PubMed Web of Science ®Google Scholar
• Teslovich TM, Musunuru K, Smith AV, Edmondson AC, Stylianou IM, Koseki M, Pirruccello JP, Ripatti S, Chasman DI, Willer CJ, Johansen CT, Fouchier SW, Isaacs A, Peloso GM, Barbalic M, Ricketts SL, Bis JC, Aulchenko YS, Thorleifsson G, Feitosa MF, Chambers J, Orho-Melander M, Melander O, Johnson T, Li X, Guo X, Li M, Shin Cho Y, Jin Go M, Jin Kim Y, Lee JY, Park T, Kim K, Sim X, Twee-Hee Ong R, Croteau-Chonka DC, Lange LA, Smith JD, Song K, Hua Zhao J, Yuan X, Luan J, Lamina C, Ziegler A, Zhang W, Zee RY, Wright AF, Witteman JC, Wilson JF, Willemsen G, Wichmann HE, Whitfield JB, Waterworth DM, Wareham NJ, Waeber G, Vollenweider P, Voight BF, Vitart V, Uitterlinden AG, Uda M, Tuomilehto J, Thompson JR, Tanaka T, Surakka I, Stringham HM, Spector TD, Soranzo N, Smit JH, Sinisalo J, Silander K, Sijbrands EJ, Scuteri A, Scott J, Schlessinger D, Sanna S, Salomaa V, Saharinen J, Sabatti C, Ruokonen A, Rudan I, Rose LM, Roberts R, Rieder M, Psaty BM, Pramstaller PP, Pichler I, Perola M, Penninx BW, Pedersen NL, Pattaro C, Parker AN, Pare G, Oostra BA, O’Donnell CJ, Nieminen MS, Nickerson DA, Montgomery GW, Meitinger T, McPherson R, McCarthy MI, McArdle W, Masson D, Martin NG, Marroni F, Mangino M, Magnusson PK, Lucas G, Luben R, Loos RJ, Lokki ML, Lettre G, Langenberg C, Launer LJ, Lakatta EG, Laaksonen R, Kyvik KO, Kronenberg F, König IR, Khaw KT, Kaprio J, Kaplan LM, Johansson A, Jarvelin MR, Janssens AC, Ingelsson E, Igl W, Kees Hovingh G, Hottenga JJ, Hofman A, Hicks AA, Hengstenberg C, Heid IM, Hayward C, Havulinna AS, Hastie ND, Harris TB, Haritunians T, Hall AS, Gyllensten U, Guiducci C, Groop LC, Gonzalez E, Gieger C, Freimer NB, Ferrucci L, Erdmann J, Elliott P, Ejebe KG, Döring A, Dominiczak AF, Demissie S, Deloukas P, de Geus EJ, de Faire U, Crawford G, Collins FS, Chen YD, Caulfield MJ, Campbell H, Burtt NP, Bonnycastle LL, Boomsma DI, Boekholdt SM, Bergman RN, Barroso I, Bandinelli S, Ballantyne CM, Assimes TL, Quertermous T, Altshuler D, Seielstad M, Wong TY, Tai ES, Feranil AB, Kuzawa CW, Adair LS, Taylor HA, Borecki IB, Gabriel SB, Wilson JG, Holm H, Thorsteinsdottir U, Gudnason V, Krauss RM, Mohlke KL, Ordovas JM, Munroe PB, Kooner JS, Tall AR, Hegele RA, Kastelein JJ, Schadt EE, Rotter JI, Boerwinkle E, Strachan DP, Mooser V, Stefansson K, Reilly MP, Samani NJ, Schunkert H, Cupples LA, Sandhu MS, Ridker PM, Rader DJ, van Duijn CM, Peltonen L, Abecasis GR, Boehnke M, Kathiresan S. 2010. Biological, clinical and population relevance of 95 loci for blood lipids. Nature 466:707–713.
   PubMed Web of Science ®Google Scholar
• Vickers KC, Shoucri BM, Levin MG, Wu H, Pearson DS, Osei-Hwedieh D, Collins FS, Remaley AT, Sethupathy P. 2013. MicroRNA-27b is a regulatory hub in lipid metabolism and is altered in dyslipidemia. Hepatology 57:533–542.
   PubMed Web of Science ®Google Scholar
• Wendel AA, Cooper DE, Ilkayeva OR, Muoio DM, Coleman RA. 2013. Glycerol-3-phosphate acyltransferase (GPAT)-1, but not GPAT4, incorporates newly synthesized fatty acids into triacylglycerol and diminishes fatty acid oxidation. J Biol Chem 288:27299–27306.
   PubMed Web of Science ®Google Scholar
• Wolff S, Afzal V, Wiencke JK, Olivieri G, Michaeli A. 1988. Human lymphocytes exposed to low doses of ionizing radiations become refractory to high doses of radiation as well as to chemical mutagens that induce double-strand breaks in DNA. Int J Radiat Biol Relat Stud Phys Chem Med 53:39–47.
   PubMedGoogle Scholar
• Yue J, Wang Q, Lu H, Brenneman M, Fan F, Shen Z. 2009. The cytoskeleton protein filamin-A is required for an efficient recombinational DNA double strand break repair. Cancer Res 69:7978–7985.
   PubMed Web of Science ®Google Scholar