441
Views
13
CrossRef citations to date
0
Altmetric
Reviews

Radiation metabolomics in the quest of cardiotoxicity biomarkers: the review

ORCID Icon & ORCID Icon
Pages 349-359 | Received 15 Jul 2019, Accepted 04 Nov 2019, Published online: 24 Jan 2020

References

  • Adams MJ, Hardenbergh PH, Constine LS, Lipshultz SE. 2003. Radiation-associated cardiovascular disease. Crit Rev Oncol Hematol. 45:55–75.
  • Alawieh A, Kobaissy FH, Kurban M, Nemer G. 2013. Metabolomics in cardiovascular diseases: Biomarkers Quest. J Data Mining Genomics Proteomics. S2:e001.
  • Azimzadeh O, Azizova T, Merl-Pham J, Subramanian V, Bakshi MV, Moseeva M, Zubkova O, Hauck SM, Anastasov N, Atkinson MJ, et al. 2017. A dose-dependent perturbation in cardiac energy metabolism is linked to radiation-induced ischemic heart disease in Mayak nuclear workers. Oncotarget. 8:9067–9078.
  • Azimzadeh O, Scherthan H, Sarioglu H, Barjaktarovic Z, Conrad M, Vogt A, Calzada‐Wack J, Neff F, Aubele M, Buske C, et al. 2011. Rapid proteomic remodeling of cardiac tissue caused by total body ionizing radiation. Proteomics. 11:3299–3311.
  • Barba I, Garcia-Dorado D. 2012. Metabolomics in cardiovascular disease: towards clinical application. In: Squeri A. Coronary artery disease-new insights and novel approaches. Croatia: IntechOpen.
  • Barjaktarovic Z, Anastasov N, Azimzadeh O, Sriharshan A, Sarioglu H, Ueffing M, Tammio H, Hakanen A, Leszczynski D, Atkinson MJ, et al. 2013a. Integrative proteomic and microRNA analysis of primary human coronary artery endothelial cells exposed to low-dose gamma radiation. Radiat Environ Biophys. 52:87–98.
  • Barjaktarovic Z, Schmaltz D, Shyla A, Azimzadeh O, Schulz S, Haagen J, Dörr W, Sarioglu H, Schäfer A, Atkinson MJ, et al. 2011. Radiation–induced signaling results in mitochondrial impairment in mouse heart at 4 weeks after exposure to X-rays. PLoS One. 6:e27811.
  • Barjaktarovic Z, Shyla A, Azimzadeh O, Schulz S, Haagen J, Dörr W, Sarioglu H, Atkinson MJ, Zischka H, Tapio S. 2013b. Ionising radiation induces persistent alterations in the cardiac mitochondrial function of C57BL/6 mice 40 weeks after local heart exposure. Radiother Oncol. 106:404–410.
  • Baselet B, Belmans N, Coninx E, Lowe D, Janssen A, Michaux A, Tabury K, Raj K, Quintens R, Benotmane MA, et al. 2017. Functional gene analysis reveals cell cycle changes and inflammation in endothelial cells irradiated with a single X-ray dose. Front Pharmacol. 8:213.
  • Baselet B, Rombouts C, Benotmane AM, Baatout S, Aerts A. 2016. Cardiovascular diseases related to ionizing radiation: the risk of low-dose exposure (review). Int J Mol Med. 38:1623–1641.
  • Bhattacharya S, Asaithamby A. 2016. Ionizing radiation and heart risks. Semin Cell Dev Biol. 58:14–25.
  • Bingol K. 2018. Recent advances in targeted and untargeted metabolomics by NMR and MS/NMR methods. High Throughput. 7:9.
  • Boerma M, Sridharan V, Mao XW, Nelson GA, Cheema AK, Koturbash I, Singh SP, Tackett AJ, Hauer-Jensen M. 2016. Effects of ionizing radiation on the heart. Mutat Res. 770:319–327.
  • Cheema AK, Pathak R, Zandkarimi F, Kaur P, Alkhalil L, Singh R, Zhong X, Ghosh S, Aykin-Burns N, Hauer-Jensen M. 2014a. Liver metabolomics reveals increased oxidative stress and fibrogenic potential in GFRP transgenic mice in response to ionizing radiation. J Proteome Res. 13:3065–3074.
  • Cheema AK, Suman S, Kaur P, Singh R, Fornace AJ Jr, Datta K. 2014b. Long-term differential changes in mouse intestinal metabolomics after γ and heavy ion radiation exposure. PLoS One. 9:e87079.
  • Chen C, Brenner DJ, Brown TR. 2011. Identification of urinary biomarkers from X-irradiated mice using NMR spectroscopy. Radiat Res. 175:622–630.
  • Coleman MA, Sasi SP, Onufrak J, Natarajan M, Manickam K, Schwab J, Muralidharan S, Peterson LE, Alekseyev YO, Yan X, et al. 2015. Low-dose radiation affects cardiac physiology: gene networks and molecular signaling in cardiomyocytes. Am J Physiol Heart Circ Physiol. 309:H1947–63.
  • Constantinou MA, Tsantili-Kakoulidou A, Andreadou I, Iliodromitis EK, Kremastinos DT, Mikros E. 2007. Application of NMR-based metabonomics in the investigation of myocardial ischemia-reperfusion, ischemic preconditioning and antioxidant intervention in rabbits. Eur J Pharm Sci. 30:303–314.
  • Darby SC, Cutter DJ, Boerma M, Constine LS, Fajardo LF, Kodama K, Mabuchi K, Marks LB, Mettler FA, Pierce LJ, et al. 2010. Radiation-related heart disease: current knowledge and future prospects. Int J Radiat Oncol Biol Phys. 76:656–665.
  • Drake KJ, Sidorov VY, McGuinness OP, Wasserman DH, Wikswo JP. 2012. Amino acids as metabolic substrates during cardiac ischemia. Exp Biol Med (Maywood)). 237:1369–1378.
  • Dukan S, Farewell A, Ballesteros M, Taddei F, Radman M, Nyström T. 2000. Protein oxidation in response to increased transcriptional or translational errors. Proc Natl Acad Sci U S A. 97:5746–5749.
  • Emini Veseli B, Perrotta P, De Meyer GRA, Roth L, Van der Donckt C, Martinet W, De Meyer G. 2017. Animal models of atherosclerosis. Eur J Pharmacol. 816:3–13.
  • Feng Q, Liu Z, Zhong S, Li R, Xia H, Jie Z, Wen B, Chen X, Yan W, Fan Y, et al. 2016. Integrated metabolomics and metagenomics analysis of plasma and urine identified microbial metabolites associated with coronary heart disease. Sci Rep. 6:22525.
  • Gaya AM, Ashford RF. 2005. Cardiac complications of radiation therapy. Clin Oncol (R Coll Radiol). 17:153–159.
  • Golla S, Golla JP, Krausz KW, Manna SK, Simillion C, Beyoğlu D, Idle JR, Gonzalez FJ. 2017. Metabolomic analysis of mice exposed to gamma radiation reveals a systemic understanding of total-body exposure. Radiat Res. 187:612–629.
  • Goudarzi M, Mak TD, Chen C, Smilenov LB, Brenner DJ, Fornace AJ. 2014. The effect of low dose rate on metabolomic response to radiation in mice. Radiat Environ Biophys. 53:645–657.
  • Gramatyka M, Boguszewicz Ł, Ciszek M, Kulik R, Sokół M. 2019. Metabolic changes in mice cardiac tissue after low dose irradiation by means of 1H NMR spectroscopy. J Radiat Res. rrz079.
  • Gramatyka M, Skorupa A, Sokół M. 2018. Nuclear magnetic resonance spectroscopy reveals metabolic changes in living cardiomyocytes after low doses of ionizing radiation. Acta Biochim Pol. 65:309–318.
  • Hall EJ, Giaccia AJ. 2018. Radiobiology for the radiologist. 8th ed. Philadelphia (PA): LWW.
  • Hu JZ, Xiao X, Hu MY. 2016. NMR metabolomics in ionizing radiation. Clin Oncol (Belmont). 1:1080.
  • ICRP. 2012. ICRP publication 118: ICRP statement on tissue reactions and early and late effects of radiation in normal tissues and organs–threshold doses for tissue reactions in a radiation protection context. Ann ICRP. 41:1–322.
  • Ishikawa T, Takahara K, Hirabayashi T, Matsumura H, Fujisawa S, Terauchi R, Uchimiya H, Kawai-Yamada M. 2010. Metabolome analysis of response to oxidative stress in rice suspension cells overexpressing cell death suppressor Bax inhibitor-1. Plant Cell Physiol. 51:9–20.
  • Jacob S, Pathak A, Franck D, Latorzeff I, Jimenez G, Fondard O, Lapeyre M, Colombier D, Bruguiere E, Lairez O, et al. 2016. Early detection and prediction of cardiotoxicity after radiation therapy for breast cancer: the BACCARAT prospective cohort study. Radiat Oncol. 11:54.
  • Jang WG, Park JY, Lee J, Bang E, Kim SR, Lee EK, Yun HJ, Kang CM, Hwang GS. 2016. Investigation of relative metabolic changes in the organs and plasma of rats exposed to X-ray radiation using HR-MAS (1)H NMR and solution (1)H NMR. NMR Biomed. 29:507–518.
  • Kazama Y, Ishii K, Hirano T, Wakana T, Yamada M, Ohbu S, Abe T. 2017. Different mutational function of low- and high-linear energy transfer heavy-ion irradiation demonstrated by whole-genome resequencing of Arabidopsis mutants. Plant J. 92:1020–1030.
  • Khan AR, Rana P, Devi MM, Chaturvedi S, Javed S, Tripathi RP, Khushu S. 2011. Nuclear magnetic resonance spectroscopy-based metabonomic investigation of biochemical effects in serum of γ-irradiated mice. Int J Radiat Biol. 87:91–97.
  • Kreuzer M, Auvinen A, Cardis E, Hall J, Jourdain JR, Laurier D, Little MP, Peters A, Raj K, Russell NS, et al. 2015. Low-dose ionising radiation and cardiovascular diseases–Strategies for molecular epidemiological studies in Europe. Mutat Res Rev Mutat Res. 764:90–100.
  • Kwon YK, Ha IJ, Bae HW, Jang WG, Yun HJ, Kim SR, Lee EK, Kang CM, Hwang GS. 2014. Dose-dependent metabolic alterations in human cells exposed to gamma irradiation. PLoS One. 9:e113573.
  • Le Gallic C, Phalente Y, Manens L, Dublineau I, Benderitter M, Gueguen Y, Lehoux S, Ebrahimian TG. 2015. Chronic internal exposure to low dose 137Cs induces positive impact on the stability of atherosclerotic plaques by reducing inflammation in ApoE-/- Mice. PLoS One. 10:e0128539.
  • Lee WH, Nguyen PK, Fleischmann D, Wu JC. 2016. DNA damage-associated biomarkers in studying individual sensitivity to low-dose radiation from cardiovascular imaging. Eur Heart J. 37:3075–3080.
  • Lindsay DP, Camara AKS, Stowe DF, Lubbe R, Aldakkak MM. 2015. Differential effects of buffer pH on Ca(2+)-induced ROS emission with inhibited mitochondrial complexes I and III . Front Physiol. 6:58.
  • 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.
  • Little MP, Lipshultz SE. 2015. Low dose radiation and circulatory diseases: a brief narrative review. Cardio-Oncol. 1:4.
  • 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.
  • Markley JL, Brüschweiler R, Edison AS, Eghbalnia HR, Powers R, Raftery D, Wishart DS. 2017. The future of NMR-based metabolomics. Curr Opin Biotechnol. 43:34–40.
  • Martinou M, Gaya A. 2013. Cardiac complications after radical radiotherapy. Semin Oncol. 40:178–185.
  • Mathias D, Mitchel RE, Barclay M, Wyatt H, Bugden M, Priest ND, Whitman SC, Scholz M, Hildebrandt G, Kamprad M, et al. 2015. Low-dose irradiation affects expression of inflammatory markers in the heart of ApoE -/- mice. PLoS One. 10:e0119661.
  • Monceau V, Meziani L, Strup-Perrot C, Morel E, Schmidt M, Haagen J, Escoubet B, Dörr W, Vozenin MC. 2013. Enhanced sensitivity to low dose irradiation of ApoE-/- mice mediated by early pro-inflammatory profile and delayed activation of the TGFβ1 cascade involved in fibrogenesis. PLoS One. 8:e57052.
  • Pannkuk EL, Laiakis EC, Girgis M, Dowd SE, Dhungana S, Nishita D, Bujold K, Bakke J, Gahagen J, Authier S, et al. 2019. Temporal effects on radiation responses in nonhuman primates: identification of biofluid small molecule signatures by gas chromatography mass spectrometry metabolomics. Metabolites. 9. DOI: 10.3390/metabo9050098.
  • Pfalzner PM. 1983. Sievert, gray and dose equivalent. J Can Assoc Radiol. 34:298–300.
  • Pluder F, Barjaktarovic Z, Azimzadeh O, Mörtl S, Krämer A, Steininger S, Sarioglu H, Leszczynski D, Nylund R, Hakanen A, et al. 2011. Low-dose irradiation causes rapid alterations to the proteome of the human endothelial cell line EA.hy926. Radiat Environ Biophys. 50:155–166.
  • Prosnitz RG, Hubbs JL, Evans ES, Zhou SM, Yu X, Blazing MA, Hollis DR, Tisch A, Wong TZ, Borges-Neto S, et al. 2007. Prospective assessment of radiotherapy associated cardiac toxicity in breast cancer patients: analysis of data 3 to 6 years after treatment. Cancer. 110:1840–1850.
  • Reed AB. 2011. The history of radiation use in medicine. J Vasc Surg. 53:3S–5S.
  • Rhee EP, Gerszten RE. 2012. Metabolomics and cardiovascular biomarker discovery. Clin Chem. 58:139–147.
  • Rombouts C, Aerts A, Beck M, De Vos WH, Van Oostveldt P, Benotmane MA, Baatout S. 2013. Differential response to acute low dose radiation in primary and immortalized endothelial cells. Int J Radiat Biol. 89:841–850.
  • Russo GL, Tedesco I, Russo M, Cioppa A, Andreassi MG, Picano E. 2012. Cellular adaptive response to chronic radiation exposure in interventional cardiologists. Eur Heart J. 33:408–414.
  • Rygiel K. 2017. Cardiotoxic effects of radiotherapy and strategies to reduce them in patients with breast cancer: an overview. J Can Res Ther. 13:186–192.
  • Sabatine MS, Morrow DA, de Lemos JA, Omland T, Sloan S, Jarolim P, Solomon SD, Pfeffer MA, Braunwald E. 2012. Evaluation of multiple biomarkers of cardiovascular stress for risk prediction and guiding medical therapy in patients with stable coronary disease. Circulation. 125:233–240.
  • Sag CM, Wolff HA, Neumann K, Opiela MK, Zhang J, Steuer F, Sowa T, Gupta S, Schirmer M, Hünlich M, et al. 2013. Ionizing radiation regulates cardiac CA handling via increased ROS and activated CaMKII. Basic Res Cardiol. 108:385.
  • Senn T, Hazen SL, Tang WH. 2012. Translating metabolomics to cardiovascular biomarkers. Prog Cardiovasc Dis. 55:70–76.
  • Sersa I, Kranjc S, Sersa G, Nemec-Svete A, Lozar B, Sepe A, Vidmar J, Sentjurc M. 2010. Study of radiation induced changes of phosphorus metabolism in mice by (31)P NMR spectroscopy. Radiol Oncol. 44:174–179.
  • 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–b5349.
  • Slezak J, Kura B, Babal P, Barancik M, Ferko M, Frimmel K, Kalocayova B, Kukreja RC, Lazou A, Mezesova L, et al. 2017. Potential markers and metabolic processes involved in the mechanism of radiation-induced heart injury. Can J Physiol Pharmacol. 95:1190–1203.
  • Sridharan V, Aykin-Burns N, Tripathi P, Krager KJ, Sharma SK, Moros EG, Corry PM, Nowak G, Hauer-Jensen M, Boerma M. 2014. Radiation-induced alterations in mitochondria of the rat heart. Radiat Res. 181:324–334.
  • Tai Y, Inoue H, Sakurai T, Yamada H, Morito M, Ide F, Mishima K, Saito I. 2009. Protective effect of lecithinized SOD on reactive oxygen species-induced xerostomia. Radiat Res. 172:331–338.
  • Tapio S. 2016. Pathology and biology of radiation-induced cardiac disease. J Radiat Res. 57:439–448.
  • Tapio S. 2017. Using proteomics to explore the effects of radiation on the heart - impacts for medicine. Expert Rev Proteomics. 14:277–279.
  • Taunk NK, Haffty BG, Kostis JB, Goyal S. 2015. Radiation-induced heart disease: pathologic abnormalities and putative mechanisms. Front Oncol. 5:39.
  • Tian S, Hirshfield KM, Jabbour SK, Toppmeyer D, Haffty BG, Khan AJ, Goyal S. 2014. Serum biomarkers for the detection of cardiac toxicity after chemotherapy and radiation therapy in breast cancer patients. Front Oncol. 4:277.
  • Tsuyama N, Mizuno H, Katafuchi A, Abe Y, Kurosu Y, Yoshida M, Kamiya K, Sakai A. 2015. Identification of low-dose responsive metabolites in X-irradiated human B lymphoblastoid cells and fibroblasts. J Radiat Res. 56:46–58.
  • Turer AT. 2013. Using metabolomics to assess myocardial metabolism and energetics in heart failure. J Mol Cell Cardiol. 55:12–18.
  • Ussher JR, Elmariah S, Gerszten RE, Dyck JR. 2016. The emerging role of metabolomics in the diagnosis and prognosis of cardiovascular disease. J Am Coll Cardiol. 68:2850–2870.
  • Ventura-Clapier R, Garnier A, Veksler V, Joubert F. 2011. Bioenergetics of the failing heart. Biochim Biophys Acta. 1813:1360–1372.
  • Wang J, Boerma M, Fu Q, Hauer-Jensen M. 2007. Significance of endothelial dysfunction in the pathogenesis of early and delayed radiation enteropathy. World J Gastroenterol. 13:3047–3055.
  • Wang J, Zheng H, Ou X, Fink LM, Hauer-Jensen M. 2002. Deficiency of microvascular thrombomodulin and up-regulation of protease-activated receptor-1 in irradiated rat intestine: possible link between endothelial dysfunction and chronic radiation fibrosis. Am J Pathol. 160:2063–2072.
  • Xiao X, Hu M, Zhang X, Hu JZ. 2017. NMR-based metabolomics analysis of liver from C57BL/6 mouse exposed to ionizing radiation. Radiat Res. 188:44–55.
  • Yoshida T, Goto S, Kawakatsu M, Urata Y, Li TS. 2012. Mitochondrial dysfunction, a probable cause of persistent oxidative stress after exposure to ionizing radiation. Free Radic Res. 46:147–153.
  • Ziółkowska E, Woźniak-Wiśniewska A, Wiśniewski T, Makarewicz R, Sinkiewicz W. 2009. Wpływ radioterapii na zaburzenia pracy serca [The influence of radiotherapy on cardiac disorders]. Contemp Oncol/Współczesna Onkologia. 13:16–21. Polish.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.