X‑irradiation induces acute and early term inflammatory responses in atherosclerosis‑prone ApoE‑/‑ mice and in endothelial cells
- Authors:
- Raghda Ramadan
- Michaël Claessens
- Ellen Cocquyt
- Mohamed Mysara
- Elke Decrock
- Sarah Baatout
- An Aerts
- Luc Leybaert
-
Affiliations: Radiobiology Unit, Belgian Nuclear Research Centre, 2400 Mol, Belgium, Department of Basic and Applied Medical Sciences, Physiology Group, Ghent University, 9000 Ghent, Belgium, Microbiology Unit, Belgian Nuclear Research Centre (SCK CEN), 2400 Mol, Belgium - Published online on: March 25, 2021 https://doi.org/10.3892/mmr.2021.12038
- Article Number: 399
-
Copyright: © Ramadan et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Kong FM, Zhao L and Hayman JA: The role of radiation therapy in thoracic tumors. Hematol Oncol Clin North Am. 20:363–400. 2006. View Article : Google Scholar : PubMed/NCBI | |
Baskar R, Lee KA, Yeo R and Yeoh KW: Cancer and radiation therapy: Current advances and future directions. Int J Med Sci. 9:193–199. 2012. View Article : Google Scholar : PubMed/NCBI | |
Delaney G, Jacob S, Featherstone C and Barton M: The role of radiotherapy in cancer treatment: Estimating optimal utilization from a review of evidence-based clinical guidelines. Cancer. 104:1129–1137. 2005. View Article : Google Scholar : PubMed/NCBI | |
Miller KD, Siegel RL, Lin CC, Mariotto AB, Kramer JL, Rowland JH, Stein KD, Alteri R and Jemal A: Cancer treatment and survivorship statistics, 2016. CA Cancer J Clin. 66:271–289. 2016. View Article : Google Scholar : PubMed/NCBI | |
Darby S, McGale P, Peto R, Granath F, Hall P and Ekbom A: 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. 2003. View Article : Google Scholar : PubMed/NCBI | |
Darby SC, Ewertz M, McGale P, Bennet AM, Blom-Goldman U, Brønnum D, Correa C, Cutter D, Gagliardi G, Gigante B, et al: Risk of ischemic heart disease in women after radiotherapy for breast cancer. N Engl J Med. 368:987–998. 2013. View Article : Google Scholar : PubMed/NCBI | |
Baselet B, Rombouts C, Benotmane AM, Baatout S and Aerts A: Cardiovascular diseases related to ionizing radiation: The risk of low-dose exposure (review). Int J Mol Med. 38:1623–1641. 2016. View Article : Google Scholar : PubMed/NCBI | |
Yusuf SW, Sami S and Daher IN: Radiation-induced heart disease: A clinical update. Cardiol Res Pract. 2011:3176592011. View Article : Google Scholar : PubMed/NCBI | |
Authors on behalf of ICRP, ; Stewart FA, Akleyev AV, Hauer-Jensen M, Hendry JH, Kleiman NJ, Macvittie TJ, Aleman BM, Edgar AB, Mabuchi K, et al: 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. 2012. View Article : Google Scholar | |
Little MP: Radiation and circulatory disease. Mutat Res. 770:299–318. 2016. View Article : Google Scholar : PubMed/NCBI | |
Eftekhari M, Anbiaei R, Zamani H, Fallahi B, Beiki D, Ameri A, Emami-Ardekani A, Fard-Esfahani A, Gholamrezanezhad A, Seid Ratki KR and Roknabadi AM: Radiation-induced myocardial perfusion abnormalities in breast cancer patients following external beam radiation therapy. Asia Ocean J Nucl Med Biol. 3:3–9. 2015.PubMed/NCBI | |
Kole TP, Aghayere O, Kwah J, Yorke ED and Goodman KA: Comparison of heart and coronary artery doses associated with intensity-modulated radiotherapy versus three-dimensional conformal radiotherapy for distal esophageal cancer. Int J Radiat Oncol Biol Phys. 83:1580–1586. 2012. View Article : Google Scholar : PubMed/NCBI | |
Tillman GF, Pawlicki T, Koong AC and Goodman KA: Preoperative versus postoperative radiotherapy for locally advanced gastroesophageal junction and proximal gastric cancers: A comparison of normal tissue radiation doses. Dis Esophagus. 21:437–444. 2008. View Article : Google Scholar : PubMed/NCBI | |
Hong JC, Rahimy E, Gross CP, Shafman T, Hu X, Yu JB, Ross R, Finkelstein SE, Dosoretz A, Park HS, et al: Radiation dose and cardiac risk in breast cancer treatment: An analysis of modern radiation therapy including community settings. Pract Radiat Oncol. 8:e79–e86. 2018. View Article : Google Scholar : PubMed/NCBI | |
Al-Kindi SG and Oliveira GH: Incidence and trends of cardiovascular mortality after common cancers in young adults: Analysis of surveillance, epidemiology and end-results program. World J Cardiol. 8:368–374. 2016. View Article : Google Scholar : PubMed/NCBI | |
Drost L, Yee C, Lam H, Zhang L, Wronski M, McCann C, Lee J, Vesprini D, Leung E and Chow E: A systematic review of heart dose in breast radiotherapy. Clin Breast Cancer. 18:e819–e824. 2018. View Article : Google Scholar : PubMed/NCBI | |
Hoving S, Heeneman S, Gijbels MJ, te Poele JA, Russell NS, Daemen MJ and Stewart FA: Single-dose and fractionated irradiation promote initiation and progression of atherosclerosis and induce an inflammatory plaque phenotype in ApoE(−/−) mice. Int J Radiat Oncol Biol Phys. 71:848–857. 2008. View Article : Google Scholar : PubMed/NCBI | |
Stewart FA, Heeneman S, Te Poele J, Kruse J, Russell NS, Gijbels M and Daemen M: Ionizing radiation accelerates the development of atherosclerotic lesions in ApoE−/− mice and predisposes to an inflammatory plaque phenotype prone to hemorrhage. Am J Pathol. 168:649–658. 2006. View Article : Google Scholar : PubMed/NCBI | |
Kreuzer M, Auvinen A, Cardis E, Hall J, Jourdain JR, Laurier D, Little MP, Peters A, Raj K, Russell NS, et al: Low-dose ionising radiation and cardiovascular diseases-strategies for molecular epidemiological studies in Europe. Mutat Res Rev Mutat Res. 764:90–100. 2015. View Article : Google Scholar : PubMed/NCBI | |
Shimizu Y, Kodama K, Nishi N, Kasagi F, Suyama A, Soda M, Grant EJ, Sugiyama H, Sakata R, Moriwaki H, et al: Radiation exposure and circulatory disease risk: Hiroshima and Nagasaki atomic bomb survivor data, 1950–2003. BMJ. 340:b53492010. View Article : Google Scholar : PubMed/NCBI | |
Yamada M, Naito K, Kasagi F, Masunari N and Suzuki G: Prevalence of atherosclerosis in relation to atomic bomb radiation exposure: An RERF adult health study. Int J Radiat Biol. 81:821–826. 2005. View Article : Google Scholar : PubMed/NCBI | |
Azizova TV, Grigoryeva ES, Haylock RG, Pikulina MV and Moseeva MB: Ischaemic heart disease incidence and mortality in an extended cohort of Mayak workers first employed in 1948–1982. Br J Radiol. 88:201501692015. View Article : Google Scholar : PubMed/NCBI | |
Kashcheev VV, Chekin SY, Karpenko SV, Maksioutov MA, Menyaylo AN, Tumanov KA, Kochergina EV, Kashcheeva PV, Gorsky AI, Shchukina NV, et al: Radiation risk of cardiovascular diseases in the cohort of Russian emergency workers of the chernobyl accident. Health Phys. 113:23–29. 2017. View Article : Google Scholar : PubMed/NCBI | |
Ramadan R, Vromans E, Anang DC, Decrock E, Mysara M, Monsieurs P, Baatout S, Leybaert L and Aerts A: Single and fractionated ionizing radiation induce alterations in endothelial connexin expression and channel function. Sci Rep. 9:46432019. View Article : Google Scholar : PubMed/NCBI | |
Mathias D, Mitchel RE, Barclay M, Wyatt H, Bugden M, Priest ND, Whitman SC, Scholz M, Hildebrandt G, Kamprad M and Glasow A: Low-dose irradiation affects expression of inflammatory markers in the heart of ApoE−/− mice. PLoS One. 10:e01196612015. View Article : Google Scholar : PubMed/NCBI | |
Sievert W, Trott KR, Azimzadeh O, Tapio S, Zitzelsberger H and Multhoff G: Late proliferating and inflammatory effects on murine microvascular heart and lung endothelial cells after irradiation. Radiother Oncol. 117:376–381. 2015. View Article : Google Scholar : PubMed/NCBI | |
Mitchel RE, Hasu M, Bugden M, Wyatt H, Little MP, Gola A, Hildebrandt G, Priest ND and Whitman SC: Low-dose radiation exposure and atherosclerosis in ApoE(−)/(−) mice. Radiat Res. 175:665–676. 2011. View Article : Google Scholar : PubMed/NCBI | |
Mancuso M, Pasquali E, Braga-Tanaka I III, Tanaka S, Pannicelli A, Giardullo P, Pazzaglia S, Tapio S, Atkinson MJ and Saran A: Acceleration of atherogenesis in ApoE−/− mice exposed to acute or low-dose-rate ionizing radiation. Oncotarget. 6:31263–31271. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kumarathasan P, Vincent R, Blais E, Saravanamuthu A, Gupta P, Wyatt H, Mitchel R, Hannan M, Trivedi A and Whitman S: Cardiovascular changes in atherosclerotic ApoE-deficient mice exposed to Co60 (ү) radiation. PLoS One. 8:e654862013. View Article : Google Scholar : PubMed/NCBI | |
Massberg S, Brand K, Gruner S, Page S, Müller E, Müller I, Bergmeier W, Richter T, Lorenz M, Konrad I, et al: A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J Exp Med. 196:887–896. 2002. View Article : Google Scholar : PubMed/NCBI | |
Heidenreich PA, Hancock SL, Lee BK, Mariscal CS and Schnittger I: Asymptomatic cardiac disease following mediastinal irradiation. J Am Coll Cardiol. 42:743–749. 2003. View Article : Google Scholar : PubMed/NCBI | |
Yusuf SW, Venkatesulu BP, Mahadevan LS and Krishnan S: Radiation-induced cardiovascular disease: A clinical perspective. Front Cardiovasc Med. 4:662017. View Article : Google Scholar : PubMed/NCBI | |
Corrado E, Rizzo M, Coppola G, Fattouch K, Novo G, Marturana I, Ferrara F and Novo S: An update on the role of markers of inflammation in atherosclerosis. J Atheroscler Thromb. 17:1–11. 2010. View Article : Google Scholar : PubMed/NCBI | |
Soeki T and Sata M: Inflammatory biomarkers and atherosclerosis. Int Heart J. 57:134–139. 2016. View Article : Google Scholar : PubMed/NCBI | |
Libby P: Inflammation in atherosclerosis. Arterioscler Thromb Vasc Biol. 32:2045–2051. 2012. View Article : Google Scholar : PubMed/NCBI | |
Murabito JM, Keyes MJ, Guo CY, Keaney JF Jr, Vasan RS, D'Agostino RB Sr and Benjamin EJ: Cross-sectional relations of multiple inflammatory biomarkers to peripheral arterial disease: The Framingham offspring study. Atherosclerosis. 203:509–514. 2009. View Article : Google Scholar : PubMed/NCBI | |
Halle M, Gabrielsen A, Paulsson-Berne G, Gahm C, Agardh HE, Farnebo F and Tornvall P: Sustained inflammation due to nuclear factor-kappa B activation in irradiated human arteries. J Am Coll Cardiol. 55:1227–1236. 2010. View Article : Google Scholar : PubMed/NCBI | |
Kiyohara H, Ishizaki Y, Suzuki Y, Katoh H, Hamada N, Ohno T, Takahashi T, Kobayashi Y and Nakano T: Radiation-induced ICAM-1 expression via TGF-β1 pathway on human umbilical vein endothelial cells; comparison between X-ray and carbon-ion beam irradiation. J Radiat Res. 52:287–292. 2011. View Article : Google Scholar : PubMed/NCBI | |
Hallahan D, Kuchibhotla J and Wyble C: Cell adhesion molecules mediate radiation-induced leukocyte adhesion to the vascular endothelium. Cancer Res. 56:5150–5155. 1996.PubMed/NCBI | |
Di Maggio FM, Minafra L, Forte GI, Cammarata FP, Lio D, Messa C, Gilardi MC and Bravatà V: Portrait of inflammatory response to ionizing radiation treatment. J Inflamm (Lond). 12:142015. View Article : Google Scholar : PubMed/NCBI | |
Baluna RG, Eng TY and Thomas CR: Adhesion molecules in radiotherapy. Radiat Res. 166:819–831. 2006. View Article : Google Scholar : PubMed/NCBI | |
Min X, Lu M, Tu S, Wang X, Zhou C, Wang S, Pang S, Qian J, Ge Y, Guo Y, et al: Serum cytokine profile in relation to the severity of coronary artery disease. Biomed Res Int. 2017:40136852017. View Article : Google Scholar : PubMed/NCBI | |
Peng J, Luo F, Ruan G, Peng R and Li X: Hypertriglyceridemia and atherosclerosis. Lipids Health Dis. 16:2332017. View Article : Google Scholar : PubMed/NCBI | |
Sloop GD: A critical analysis of the role of cholesterol in atherogenesis. Atherosclerosis. 142:265–268. 1999. View Article : Google Scholar : PubMed/NCBI | |
Lowe D and Raj K: Premature aging induced by radiation exhibits pro-atherosclerotic effects mediated by epigenetic activation of CD44 expression. Aging Cell. 13:900–910. 2014. View Article : Google Scholar : PubMed/NCBI | |
Lowe D, Horvath S and Raj K: Epigenetic clock analyses of cellular senescence and ageing. Oncotarget. 7:8524–8531. 2016. View Article : Google Scholar : PubMed/NCBI | |
Leligdowicz A, Conroy AL, Hawkes M, Zhong K, Lebovic G, Matthay MA and Kain KC: Validation of two multiplex platforms to quantify circulating markers of inflammation and endothelial injury in severe infection. PLoS One. 12:e01751302017. View Article : Google Scholar : PubMed/NCBI | |
Vitkova V, Panek M, Janec P, Šibíková M, Vobruba V, Haluzík M, Živný J and Janota J: Endothelial microvesicles and soluble markers of endothelial injury in critically Ill newborns. Mediators Inflamm. 2018:19750562018. View Article : Google Scholar : PubMed/NCBI | |
Bahlas S, Damiati L, Dandachi N, Sait H, Alsefri M and Pushparaj PN: Rapid immunoprofiling of cytokines, chemokines and growth factors in patients with active rheumatoid arthritis using luminex multiple analyte profiling technology for precision medicine. Clin Exp Rheumatol. 37:112–119. 2019.PubMed/NCBI | |
Reslova N, Michna V, Kasny M, Mikel P and Kralik P: xMAP technology: Applications in detection of pathogens. Front Microbiol. 8:552017. View Article : Google Scholar : PubMed/NCBI | |
Ramadan R, Vromans E, Anang DC, Goetschalckx I, Hoorelbeke D, Decrock E, Baatout S, Leybaert L and Aerts A: Connexin43 hemichannel targeting with TAT-Gap19 alleviates radiation-induced endothelial cell damage. Front Pharmacol. 11:2122020. View Article : Google Scholar : PubMed/NCBI | |
Darby SC, Cutter DJ, Boerma M, Constine LS, Fajardo LF, Kodama K, Mabuchi K, Marks LB, Mettler FA, Pierce LJ, et al: Radiation-related heart disease: Current knowledge and future prospects. Int J Radiat Oncol Biol Phys. 76:656–665. 2010. View Article : Google Scholar : PubMed/NCBI | |
Aleman BM, Moser EC, Nuver J, Suter TM, Maraldo MV, Specht L, Vrieling C and Darby SC: Cardiovascular disease after cancer therapy. EJC Suppl. 12:18–28. 2014. View Article : Google Scholar : PubMed/NCBI | |
Monceau V, Meziani L, Strup-Perrot C, Morel E, Schmidt M, Haagen J, Escoubet B, Dörr W and Vozenin MC: 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:e570522013. View Article : Google Scholar : PubMed/NCBI | |
Brunner D, Altman S, Loebl K, Schwartz S and Levin S: Serum cholesterol and triglycerides in patients suffering from ischemic heart disease and in healthy subjects. Atherosclerosis. 28:197–204. 1977. View Article : Google Scholar : PubMed/NCBI | |
Sarwar N, Danesh J, Eiriksdottir G, Sigurdsson G, Wareham N, Bingham S, Boekholdt SM, Khaw KT and Gudnason V: Triglycerides and the risk of coronary heart disease: 10,158 incident cases among 262,525 participants in 29 Western prospective studies. Circulation. 115:450–458. 2007. View Article : Google Scholar : PubMed/NCBI | |
Ozmen HK, Erdemci B, Askin S and Sezen O: Carnitine and adiponectin levels in breast cancer after radiotherapy. Open Med (Wars). 12:189–194. 2017. View Article : Google Scholar : PubMed/NCBI | |
Park H, Kim CH, Jeong JH, Park M and Kim KS: GDF15 contributes to radiation-induced senescence through the ROS-mediated p16 pathway in human endothelial cells. Oncotarget. 7:9634–9644. 2016. View Article : Google Scholar : PubMed/NCBI | |
Hoving S, Heeneman S, Gijbels MJ, Te Poele JA, Visser N, Cleutjens J, Russell NS, Daemen MJ and Stewart FA: Irradiation induces different inflammatory and thrombotic responses in carotid arteries of wildtype C57BL/6J and atherosclerosis-prone ApoE(−/−) mice. Radiother Oncol. 105:365–370. 2012. View Article : Google Scholar : PubMed/NCBI | |
Bootcov MR, Bauskin AR, Valenzuela SM, Moore AG, Bansal M, He XY, Zhang HP, Donnellan M, Mahler S, Pryor K, et al: MIC-1, a novel macrophage inhibitory cytokine, is a divergent member of the TGF-beta superfamily. Proc Natl Acad Sci USA. 94:11514–11519. 1997. View Article : Google Scholar : PubMed/NCBI | |
Hsiao EC, Koniaris LG, Zimmers-Koniaris T, Sebald SM, Huynh TV and Lee SJ: Characterization of growth-differentiation factor 15, a transforming growth factor beta superfamily member induced following liver injury. Mol Cell Biol. 20:3742–3751. 2000. View Article : Google Scholar : PubMed/NCBI | |
Wollert KC and Kempf T: Growth differentiation factor 15 in heart failure: An update. Curr Heart Fail Rep. 9:337–345. 2012. View Article : Google Scholar : PubMed/NCBI | |
Chen J, Luo F, Fang Z and Zhang W: GDF-15 levels and atherosclerosis. Int J Cardiol. 257:362018. View Article : Google Scholar : PubMed/NCBI | |
Kempf T and Wollert KC: Growth differentiation factor-15: A new biomarker in cardiovascular disease. Herz. 34:594–599. 2009. View Article : Google Scholar : PubMed/NCBI | |
Xu X, Li Z and Gao W: Growth differentiation factor 15 in cardiovascular diseases: From bench to bedside. Biomarkers. 16:466–475. 2011. View Article : Google Scholar : PubMed/NCBI | |
Bonaterra GA, Zugel S, Thogersen J, Walter SA, Haberkorn U, Strelau J and Kinscherf R: Growth differentiation factor-15 deficiency inhibits atherosclerosis progression by regulating interleukin-6-dependent inflammatory response to vascular injury. J Am Heart Assoc. 1:e0025502012. View Article : Google Scholar : PubMed/NCBI | |
de Jager SC, Bermudez B, Bot I, Koenen RR, Bot M, Kavelaars A, de Waard V, Heijnen CJ, Muriana FJ, Weber C, et al: Growth differentiation factor 15 deficiency protects against atherosclerosis by attenuating CCR2-mediated macrophage chemotaxis. J Exp Med. 208:217–225. 2011. View Article : Google Scholar : PubMed/NCBI | |
Heller EA, Liu E, Tager AM, Yuan Q, Lin AY, Ahluwalia N, Jones K, Koehn SL, Lok VM, Aikawa E, et al: Chemokine CXCL10 promotes atherogenesis by modulating the local balance of effector and regulatory T cells. Circulation. 113:2301–2312. 2006. View Article : Google Scholar : PubMed/NCBI | |
Mach F, Sauty A, Iarossi AS, Sukhova GK, Neote K, Libby P and Luster AD: Differential expression of three T lymphocyte-activating CXC chemokines by human atheroma-associated cells. J Clin Invest. 104:1041–1050. 1999. View Article : Google Scholar : PubMed/NCBI | |
van den Borne P, Quax PH, Hoefer IE and Pasterkamp G: The multifaceted functions of CXCL10 in cardiovascular disease. Biomed Res Int. 2014:8931062014. View Article : Google Scholar : PubMed/NCBI | |
Ardigo D, Assimes TL, Fortmann SP, Go AS, Hlatky M, Hytopoulos E, Iribarren C, Tsao PS, Tabibiazar R and Quertermous T; ADVANCE Investigators, : Circulating chemokines accurately identify individuals with clinically significant atherosclerotic heart disease. Physiol Genomics. 31:402–409. 2007. View Article : Google Scholar : PubMed/NCBI | |
Orn S, Breland UM, Mollnes TE, Manhenke C, Dickstein K, Aukrust P and Ueland T: The chemokine network in relation to infarct size and left ventricular remodeling following acute myocardial infarction. Am J Cardiol. 104:1179–1183. 2009. View Article : Google Scholar : PubMed/NCBI | |
Tavakolian Ferdousie V, Mohammadi M, Hassanshahi G, Khorramdelazad H, Khanamani Falahati-Pour S, Mirzaei M, Allah Tavakoli M, Kamiab Z, Ahmadi Z, Vazirinejad R, et al: Serum CXCL10 and CXCL12 chemokine levels are associated with the severity of coronary artery disease and coronary artery occlusion. Int J Cardiol. 233:23–28. 2017. View Article : Google Scholar : PubMed/NCBI | |
Palayoor ST, John-Aryankalayil M, Makinde AY, Falduto MT, Magnuson SR and Coleman CN: Differential expression of stress and immune response pathway transcripts and miRNAs in normal human endothelial cells subjected to fractionated or single-dose radiation. Mol Cancer Res. 12:1002–1015. 2014. View Article : Google Scholar : PubMed/NCBI | |
Heinonen M, Milliat F, Benadjaoud MA, François A, Buard V, Tarlet G, d'Alché-Buc F and Guipaud O: Temporal clustering analysis of endothelial cell gene expression following exposure to a conventional radiotherapy dose fraction using Gaussian process clustering. PLoS One. 13:e02049602018. View Article : Google Scholar : PubMed/NCBI | |
Libby P, Ridker PM and Maseri A: Inflammation and atherosclerosis. Circulation. 105:1135–1143. 2002. View Article : Google Scholar : PubMed/NCBI | |
Lusis AJ: Atherosclerosis. Nature. 407:233–241. 2000. View Article : Google Scholar : PubMed/NCBI | |
Hallahan DE and Virudachalam S: Accumulation of P-selectin in the lumen of irradiated blood vessels. Radiat Res. 152:6–13. 1999. View Article : Google Scholar : PubMed/NCBI | |
Tu J, Hu Z and Chen Z: Endothelial gene expression and molecular changes in response to radiosurgery in in vitro and in vivo models of cerebral arteriovenous malformations. Biomed Res Int. 2013:4082532013. View Article : Google Scholar : PubMed/NCBI | |
Hallahan DE and Virudachalam S: Ionizing radiation mediates expression of cell adhesion molecules in distinct histological patterns within the lung. Cancer Res. 57:2096–2099. 1997.PubMed/NCBI | |
Gaugler MH, Squiban C, van der Meeren A, Bertho JM, Vandamme M and Mouthon MA: Late and persistent up-regulation of intercellular adhesion molecule-1 (ICAM-1) expression by ionizing radiation in human endothelial cells in vitro. Int J Radiat Biol. 72:201–209. 1997. View Article : Google Scholar : PubMed/NCBI | |
Haubner F, Leyh M, Ohmann E, Pohl F, Prantl L and Gassner HG: Effects of external radiation in a co-culture model of endothelial cells and adipose-derived stem cells. Radiat Oncol. 8:662013. View Article : Google Scholar : PubMed/NCBI | |
Azimzadeh O, Sievert W, Sarioglu H, Merl-Pham J, Yentrapalli R, Bakshi MV, Janik D, Ueffing M, Atkinson MJ, Multhoff G and Tapio S: 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. 2015. View Article : Google Scholar : PubMed/NCBI | |
Cervelli T, Panetta D, Navarra T, Andreassi MG, Basta G, Galli A, Salvadori PA, Picano E and Del Turco S: Effects of single and fractionated low-dose irradiation on vascular endothelial cells. Atherosclerosis. 235:510–518. 2014. View Article : Google Scholar : PubMed/NCBI | |
Ria R, Cirulli T, Giannini T, Bambace S, Serio G, Portaluri M, Ribatti D, Vacca A and Dammacco F: Serum levels of angiogenic cytokines decrease after radiotherapy in non-Hodgkin lymphomas. Clin Exp Med. 8:141–145. 2008. View Article : Google Scholar : PubMed/NCBI | |
Ria R, Portaluri M, Russo F, Cirulli T, Di Pietro G, Bambace S, Cucci F, Romano T, Vacca A and Dammacco F: Serum levels of angiogenic cytokines decrease after antineoplastic radiotherapy. Cancer Lett. 216:103–107. 2004. View Article : Google Scholar : PubMed/NCBI | |
Yang X, Liaw L, Prudovsky I, Brooks PC, Vary C, Oxburgh L and Friesel R: Fibroblast growth factor signaling in the vasculature. Curr Atheroscler Rep. 17:5092015. View Article : Google Scholar : PubMed/NCBI | |
Fuks Z, Persaud RS, Alfieri A, McLoughlin M, Ehleiter D, Schwartz JL, Seddon AP, Cordon-Cardo C and Haimovitz-Friedman A: Basic fibroblast growth factor protects endothelial cells against radiation-induced programmed cell death in vitro and in vivo. Cancer Res. 54:2582–2590. 1994.PubMed/NCBI | |
Zhang S, Qiu X, Zhang Y, Fu K, Zhao X, Wu J, Hu Y, Zhu W and Guo H: Basic fibroblast growth factor ameliorates endothelial dysfunction in radiation-induced bladder injury. Biomed Res Int. 2015:9676802015.PubMed/NCBI | |
Six I, Mouquet F, Corseaux D, Bordet R, Letourneau T, Vallet B, Dosquet CC, Dupuis B, Jude B, Bertrand ME, et al: Protective effects of basic fibroblast growth factor in early atherosclerosis. Growth Factors. 22:157–167. 2004. View Article : Google Scholar : PubMed/NCBI | |
Aiello RJ, Bourassa PA, Lindsey S, Weng W, Natoli E, Rollins BJ and Milos PM: Monocyte chemoattractant protein-1 accelerates atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 19:1518–1525. 1999. View Article : Google Scholar : PubMed/NCBI | |
Harrington JR: The role of MCP-1 in atherosclerosis. Stem Cells. 18:65–66. 2000. View Article : Google Scholar : PubMed/NCBI | |
Nalla AK, Gogineni VR, Gupta R, Dinh DH and Rao JS: Suppression of uPA and uPAR blocks radiation-induced MCP-1 mediated recruitment of endothelial cells in meningioma. Cell Signal. 23:1299–1310. 2011. View Article : Google Scholar : PubMed/NCBI | |
Farris SD, Hu JH, Krishnan R, Emery I, Chu T, Du L, Kremen M, Dichek HL, Gold E, Ramsey SA and Dichek DA: Mechanisms of urokinase plasminogen activator (uPA)-mediated atherosclerosis: Role of the uPA receptor and S100A8/A9 proteins. J Biol Chem. 286:22665–22677. 2011. View Article : Google Scholar : PubMed/NCBI | |
Kimura M, Sudhir K, Jones M, Simpson E, Jefferis AM and Chin-Dusting JP: Impaired acetylcholine-induced release of nitric oxide in the aorta of male aromatase-knockout mice: Regulation of nitric oxide production by endogenous sex hormones in males. Circ Res. 93:1267–1271. 2003. View Article : Google Scholar : PubMed/NCBI | |
Adams MR, Golden DL, Register TC, Anthony MS, Hodgin JB, Maeda N and Williams JK: The atheroprotective effect of dietary soy isoflavones in apolipoprotein E−/− mice requires the presence of estrogen receptor-alpha. Arterioscler Thromb Vasc Biol. 22:1859–1864. 2002. View Article : Google Scholar : PubMed/NCBI | |
Zhu Y, Bian Z, Lu P, Karas RH, Bao L, Cox D, Hodgin J, Shaul PW, Thoren P, Smithies O, et al: Abnormal vascular function and hypertension in mice deficient in estrogen receptor beta. Science. 295:505–508. 2002. View Article : Google Scholar : PubMed/NCBI | |
Hodgin JB, Krege JH, Reddick RL, Korach KS, Smithies O and Maeda N: Estrogen receptor alpha is a major mediator of 17beta-estradiol's atheroprotective effects on lesion size in Apoe−/− mice. J Clin Invest. 107:333–340. 2001. View Article : Google Scholar : PubMed/NCBI | |
Hurtado R, Celani M and Geber S: Effect of short-term estrogen therapy on endothelial function: A double-blinded, randomized, controlled trial. Climacteric. 19:448–451. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zheng S, Chen X, Hong S, Long L, Xu Y, Simoncini T and Fu X: 17β-Estradiol inhibits vascular smooth muscle cell migration via up-regulation of striatin protein. Gynecol Endocrinol. 31:618–624. 2015. View Article : Google Scholar : PubMed/NCBI | |
Zhang G, Li C, Zhu N, Chen Y, Yu Q, Liu E and Wang R: Sex differences in the formation of atherosclerosis lesion in apoE−/−mice and the effect of 17β-estrodiol on protein S-nitrosylation. Biomed Pharmacother. 99:1014–1021. 2018. View Article : Google Scholar : PubMed/NCBI |