Cited by 83Effects of Radiation ExposureSpaceflight effects on biologyRadiation Therapy and Dosimetry

Vive la radiorésistance!: converging research in radiobiology and biogerontology to enhance human radioresistance for deep space exploration and colonization

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Cortese, Franco, Klokov, Dmitry, Osipov, Andreyan, Stefaniak, Jakub, Moskalev, Alexey, Schastnaya, Jane, Cantor, Charles, Aliper, Alexander +22 more·2018·Oncotarget

Abstract

While many efforts have been made to pave the way toward human space colonization, little consideration has been given to the methods of protecting spacefarers against harsh cosmic and local radioactive environments and the high costs associated with protection from the deleterious physiological effects of exposure to high-Linear energy transfer (high-LET) radiation. Herein, we lay the foundations of a roadmap toward enhancing human radioresistance for the purposes of deep space colonization and exploration. We outline future research directions toward the goal of enhancing human radioresistance, including upregulation of endogenous repair and radioprotective mechanisms, possible leeways into gene therapy in order to enhance radioresistance via the translation of exogenous and engineered DNA repair and radioprotective mechanisms, the substitution of organic molecules with fortified isoforms, and methods of slowing metabolic activity while preserving cognitive function. We conclude by presenting the known associations between radioresistance and longevity, and articulating the position that enhancing human radioresistance is likely to extend the healthspan of human spacefarers as well.

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  • Promising strategies are the inducible expression of endogenous antioxidants, DNA repair genes or radioprotective transgenes resulting in controlled reduction in early and late-stage irradiation damage.

    “Promising strategies are the inducible expression of endogenous antioxidants, DNA repair genes or radioprotective transgenes resulting in controlled reduction in early and late-stage irradiation damage44.”

    From Towards sustainable human space exploration—priorities for radiation research to quantify and mitigate radiation risks (2023) · cites this paper as [44]

    The “Gene therapy for deep space exploration” section (page unavailable) recommends inducible expression for endogenous antioxidants and DNA repair genes, and identifies radioprotective transgenes as promising. But its reported reduction in early- and late-stage irradiation damage concerns MnSOD antioxidant transgenes specifically; the Dsup radioprotective transgene example used a constitutive promoter. It does not establish that inducible expression of all three strategies produces that outcome. (LLM, conf=0.88)

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  1. [2]Martinez R Goodliff KE Whitley RJ ISECG Global Exploration Roadmap: A Stepwise Approach to Deep Space Exploration AIAA SPACE 2013 Conference and Exposition 2013 10.2514/6.2013-5504 · DOI
  2. [4]Russo D Foley T Stroud K Connolly J Tillman B Pickett L NASA Space Flight Human System Standards PsycEXTRA Dataset 10.1037/e578052012-005 · DOI
  3. [5]Maalouf M Durante M Foray N Biological effects of space radiation on human cells: history, advances and outcomes J Radiat Res (Tokyo) 2011 52 126 46 10.1269/jrr.10128 21436608 · DOI · Paper page
  4. [6]Barratt MR PSL. Principles of clinical medicine for space flight Springer NY 2008
  5. [7]Zeitlin C The risky road to Mars—response Science 2013 341 1062 10.1126/science.341.6150.1062-b 24009375 · DOI
  6. [10]Geng C Tang X Gong C Guan F Johns J Shu D Chen D A Monte Carlo-based radiation safety assessment for astronauts in an environment with confined magnetic field shielding J Radiol Prot 2015 35 777 88 10.1088/0952-4746/35/4/777 26484984 · DOI
  7. [11]Washburn SA Blattnig SR Singleterry RC Westover SC Active magnetic radiation shielding system analysis and key technologies Life Sci Space Res (Amst) 2015 4 22 34 10.1016/j.lssr.2014.12.004 26177618 · DOI
  8. [12]Tubiana M Feinendegen LE Yang C Kaminski JM The linear no-threshold relationship is inconsistent with radiation biologic and experimental data Radiology 2009 251 13 22 10.1148/radiol.2511080671 19332842 PMC2663584 · DOI
  9. [14]Horikawa DD Sakashita T Katagiri C Watanabe M Kikawada T Nakahara Y Hamada N Wada S Funayama T Higashi S Kobayashi Y Okuda T Kuwabara M Radiation tolerance in the tardigrade Milnesium tardigradum Int J Radiat Biol 2006 82 843 48 10.1080/09553000600972956 17178624 · DOI
  10. [19]Wilson JW Shinn JL Tripathi RK Singleterry RC Clowdsley MS Thibeault SA Cheatwood FM Schimmerling W Cucinotta FA Badhwar GD Noor AK Kim MY Badavi FF Issues in deep space radiation protection Acta Astronaut 2001 49 289 312 10.1016/S0094-5765(01)00107-2 11669118 · DOI
  11. [20]Nelson GA Space Radiation and Human Exposures, A Primer Radiat Res 2016 185 349 58 10.1667/RR14311.1 27018778 · DOI
  12. [21]Thorne MC ICRP publication 60: 1990 recommendations of the international commission on radiological protection Ann Nucl Energy 1992 19 51 52 10.1016/0306-4549(92)90053-E · DOI
  13. [23]Cucinotta FA Cacao E Non-Targeted Effects Models Predict Significantly Higher Mars Mission Cancer Risk than Targeted Effects Models Sci Rep 2017 7 1832 10.1038/s41598-017-02087-3 28500351 PMC5431989 · DOI
  14. [24]Muller HJ ARTIFICIAL TRANSMUTATION OF THE GENE Science 1927 66 84 87 10.1126/science.66.1699.84 17802387 · DOI
  15. [25]Sankaranarayanan K Estimation of the genetic risks of exposure to ionizing radiation in humans: current status and emerging perspectives J Radiat Res 2006 Suppl B 47 B57 66 17019053
  16. [26]Ward JF The complexity of DNA damage: relevance to biological consequences Int J Radiat Biol 1994 66 427 32 10.1080/09553009414551401 7983426 · DOI · Paper page
  17. [27]Sutherland BM Bennett PV Sidorkina O Laval J Clustered damages and total lesions induced in DNA by ionizing radiation: oxidized bases and strand breaks Biochemistry 2000 39 8026 31 10.1021/bi9927989 10891084 · DOI
  18. [28]Sage E Shikazono N Radiation-induced clustered DNA lesions: repair and mutagenesis Free Radic Biol Med 2017 107 125 35 10.1016/j.freeradbiomed.2016.12.008 27939934 · DOI
  19. [29]Osipov AN Grekhova A Pustovalova M Ozerov IV Eremin P Vorobyeva N Lazareva N Pulin A Zhavoronkov A Roumiantsev S Klokov D Eremin I Activation of homologous recombination DNA repair in human skin fibroblasts continuously exposed to X-ray radiation Oncotarget 2015 6 26876 85 10.18632/oncotarget.4946 26337087 PMC4694959 · DOI
  20. [30]Osipov AN Pustovalova M Grekhova A Eremin P Vorobyova N Pulin A Zhavoronkov A Roumiantsev S Klokov DY Eremin I Low doses of X-rays induce prolonged and ATM-independent persistence of γH2AX foci in human gingival mesenchymal stem cells Oncotarget 2015 6 27275 87 10.18632/oncotarget.4739 26314960 PMC4694989 · DOI
  21. [31]Moynahan ME Jasin M Loss of heterozygosity induced by a chromosomal double-strand break Proc Natl Acad Sci USA 1997 94 8988 93 10.1073/pnas.94.17.8988 9256422 PMC22995 · DOI
  22. [32]Halazonetis TD Gorgoulis VG Bartek J An oncogene-induced DNA damage model for cancer development Science 2008 319 1352 55 10.1126/science.1140735 18323444 · DOI · Paper page
  23. [33]Mladenov E Magin S Soni A Iliakis G DNA double-strand break repair as determinant of cellular radiosensitivity to killing and target in radiation therapy Front Oncol 2013 3 113 10.3389/fonc.2013.00113 23675572 PMC3650303 · DOI
  24. [34]Mladenov E Magin S Soni A Iliakis G DNA double-strand-break repair in higher eukaryotes and its role in genomic instability and cancer: cell cycle and proliferation-dependent regulation Semin Cancer Biol 2016 37 38 51 64 10.1016/j.semcancer.2016.03.003 27016036 · DOI
  25. [35]Neumaier T Swenson J Pham C Polyzos A Lo AT Yang P Dyball J Asaithamby A Chen DJ Bissell MJ Thalhammer S Costes SV Evidence for formation of DNA repair centers and dose-response nonlinearity in human cells Proc Natl Acad Sci USA 2012 109 443 48 10.1073/pnas.1117849108 22184222 PMC3258602 · DOI
  26. [36]Costes SV Chiolo I Pluth JM Barcellos-Hoff MH Jakob B Spatiotemporal characterization of ionizing radiation induced DNA damage foci and their relation to chromatin organization Mutat Res 2010 704 78 87 10.1016/j.mrrev.2009.12.006 20060491 PMC3951968 · DOI
  27. [37]Metzger L Iliakis G Kinetics of DNA double-strand break repair throughout the cell cycle as assayed by pulsed field gel electrophoresis in CHO cells Int J Radiat Biol 1991 59 1325 39 10.1080/09553009114551201 1677379 · DOI
  28. [38]Kysela BP Michael BD Arrand JE Relative contributions of levels of initial DNA damage and repair of double strand breaks to the ionizing radiation-sensitive phenotype of the Chinese hamster cell mutant, XR-V15B. Part I. X-rays Int J Radiat Biol 1993 63 609 16 10.1080/09553009314450791 8099106 · DOI
  29. [41]Sies H Oxidative stress: oxidants and antioxidants Academic Pr 1991 650 9129943
  30. [42]Özben T Free Radicals, Oxidative Stress, and Antioxidants: Pathological and Physiological Significance Springer Science & Business Media 2013 395
  31. [43]Poljsak B Milisav I Aging, Oxidative Stress and Antioxidants. Oxidative Stress and Chronic Degenerative Diseases - A Role for Antioxidants 2013 10.5772/51609 · DOI
  32. [44]Santivasi WL Xia F Ionizing radiation-induced DNA damage, response, and repair Antioxid Redox Signal 2014 21 251 59 10.1089/ars.2013.5668 24180216 · DOI
  33. [45]Ward JF Ionizing Radiation Induced DNA Damage: Identities and DNA Repair Basic Life Sci 1986 38 135 8 3741327
  34. [46]Nelson SJ Models for DNA damage formation and repair in mammalian cells exposed to ionizing radiation Radiat Res 1982 92 120 45 10.2307/3575849 7134379 · DOI
  35. [47]Lehmann AR Repair processes for radiation-induced DNA damage Mol Biol Biochem Biophys 1978 27 312 34 10.1007/978-3-642-81196-8_15 349358 · DOI
  36. [48]Rahmanian S Taleei R Nikjoo H Radiation induced base excision repair (BER): a mechanistic mathematical approach DNA Repair (Amst) 2014 22 89 103 10.1016/j.dnarep.2014.07.011 25117268 · DOI
  37. [49]Chaudhry MA Base excision repair of ionizing radiation-induced DNA damage in G1 and G2 cell cycle phases Cancer Cell Int 2007 7 15 10.1186/1475-2867-7-15 17892593 PMC2063494 · DOI
  38. [50]Schötz U Heuer S Caldwell RB Zitzelsberger H Genetic and biochemical analysis of base excision repair complexes participating in radiation-induced ROS damage repair Radiat Prot Dosimetry 2011 143 284 88 10.1093/rpd/ncq400 21109544 · DOI
  39. [51]Huang H Claycamp HG DNA excision repair as a component of adaptation to low doses of ionizing radiation in Escherichia coli Int J Radiat Biol 1993 64 613 19 10.1080/09553009314551831 7902401 · DOI
  40. [52]Izumi T Mellon I Base Excision Repair and Nucleotide Excision Repair Genome Stability 2016 275 302 10.1016/B978-0-12-803309-8.00017-3 · DOI
  41. [54]Spivak G Nucleotide excision repair in humans DNA Repair (Amst) 2015 36 13 18 10.1016/j.dnarep.2015.09.003 26388429 PMC4688078 · DOI · Paper page
  42. [55]Bild W Stefanescu I Haulica I Lupuşoru C Titescu G Iliescu R Nastasa V Research concerning the radioprotective and immunostimulating effects of deuterium-depleted water Rom J Physiol 1999 36 205 18 11797936
  43. [56]Zavilgelsky GB Translesion synthesis, or molecular steeplechase Mol Biol 2000 34 175 82 10.1007/BF02759636 10779945 · DOI
  44. [57]Kai M Wang TS Checkpoint activation regulates mutagenic translesion synthesis Genes Dev 2003 17 64 76 10.1101/gad.1043203 12514100 PMC195967 · DOI
  45. [59]Almasan A Cellular commitment to radiation-induced apoptosis Radiat Res 2000 153 347 50 10.1667/0033-7587(2000)153[0347:CCTRIA]2.0.CO;2 10669558 · DOI
  46. [60]Langley RE Palayoor ST Coleman CN Bump EA Modifiers of radiation-induced apoptosis Radiat Res 1993 136 320 26 10.2307/3578543 8278572 · DOI
  47. [61]Jendrossek V Belka C Radiation Therapy and Apoptosis Apoptosis and Cancer Therapy 1049 86 10.1002/9783527619665.ch42 · DOI
  48. [62]Ferlini C Amelio RD Scambia G Apoptosis Induced by Ionizing Radiation Subcellular Biochemistry 171 86 10.1007/0-306-47931-1_9 12037980 · DOI
  49. [65]Crompton NE Telomeres, senescence and cellular radiation response Cell Mol Life Sci 1997 53 568 75 10.1007/s000180050073 9284959 PMC11147279 · DOI
  50. [66]Suzuki M Boothman DA Stress-induced premature senescence (SIPS)—influence of SIPS on radiotherapy J Radiat Res (Tokyo) 2008 49 105 12 10.1269/jrr.07081 18219184 · DOI
  51. [67]Plews M Simon SL Boreham DR Parchaliuk D Wyatt H Mantha R Frost K Lamoureux L Stobart M Czub S Mitchel RE Knox JD A radiation-induced adaptive response prolongs the survival of prion-infected mice Free Radic Biol Med 2010 49 1417 21 10.1016/j.freeradbiomed.2010.07.025 20692334 · DOI
  52. [68]Mitchel RE Jackson JS Morrison DP Carlisle SM Low doses of radiation increase the latency of spontaneous lymphomas and spinal osteosarcomas in cancer-prone, radiation-sensitive Trp53 heterozygous mice Radiat Res 2003 159 320 27 10.1667/0033-7587(2003)159[0320:LDORIT]2.0.CO;2 12600234 · DOI
  53. [69]Mitchel RE Adaption By Low Dose Radiation Exposure: A Look at Scope and Limitations for Radioprotection Dose Response 2015 13 dose-response.14-025.Mitchel. 10.2203/dose-response.14-025.Mitchel PMC4674178 26672725 · DOI
  54. [70]Tubiana M Dose-effect relationship and estimation of the carcinogenic effects of low doses of ionizing radiation: the joint report of the Académie des Sciences (Paris) and of the Académie Nationale de Médecine Int J Radiat Oncol Biol Phys 2005 63 317 19 10.1016/j.ijrobp.2005.06.013 16168825 · DOI
  55. [71]Matsumoto H Hamada N Takahashi A Kobayashi Y Ohnishi T Vanguards of paradigm shift in radiation biology: radiation-induced adaptive and bystander responses J Radiat Res (Tokyo) 2007 48 97 106 10.1269/jrr.06090 17327685 · DOI
  56. [72]Mitchel RE Jackson JS McCann RA Boreham DR The adaptive response modifies latency for radiation-induced myeloid leukemia in CBA/H mice Radiat Res 1999 152 273 79 10.2307/3580327 10453088 · DOI
  57. [73]ICRP ICRP Publication 99: Low-Dose Extrapolation of Radiation-related Cancer Risk SAGE Publications 2006 150 16782497
  58. [74]Morimoto S Gordon A Fukunishi N Yatagai F Cellular responses by exposure to heavy-ions Adv Space Res 2001 27 401 09 10.1016/S0273-1177(01)00008-4 11642302 · DOI
  59. [75]Varès G Wang B Tanaka K Kakimoto A Eguchi-Kasai K Nenoi M Mutagenic adaptive response to high-LET radiation in human lymphoblastoid cells exposed to X-rays Mutat Res 2011 706 46 52 10.1016/j.mrfmmm.2010.10.009 21055411 · DOI
  60. [76]Varès G Wang B Tanaka K Kakimoto A Eguchi-Kasai K Nenoi M Mutagenic adaptive response to high-LET radiation in human lymphoblastoid cells exposed to low doses of heavy-ion radiation Mutat Res 2011 712 49 54 10.1016/j.mrfmmm.2011.04.004 21540043 · DOI
  61. [77]Rithidech KN Scott BR Evidence for radiation hormesis after in vitro exposure of human lymphocytes to low doses of ionizing radiation Dose Response 2008 6 252 71 10.2203/dose-response.07-024.Rithidech 18846261 PMC2564764 · DOI
  62. [78]Scott BR It's time for a new low-dose-radiation risk assessment paradigm—one that acknowledges hormesis Dose Response 2008 6 333 51 10.2203/dose-response.07-005.Scott 19088900 PMC2592992 · DOI
  63. [79]Wang B Ninomiya Y Tanaka K Maruyama K Varès G Eguchi-Kasai K Nenoi M Adaptive response of low linear energy transfer X-rays for protection against high linear energy transfer accelerated heavy ion-induced teratogenesis Birth Defects Res B Dev Reprod Toxicol 2012 95 379 85 10.1002/bdrb.21027 23109298 · DOI
  64. [80]Buonanno M De Toledo SM Howell RW Azzam EI Low-dose energetic protons induce adaptive and bystander effects that protect human cells against DNA damage caused by a subsequent exposure to energetic iron ions J Radiat Res (Tokyo) 2015 56 502 08 10.1093/jrr/rrv005 25805407 PMC4426929 · DOI
  65. [81]Vijg J Suh Y Genome instability and aging Annu Rev Physiol 2013 75 645 68 10.1146/annurev-physiol-030212-183715 23398157 · DOI
  66. [82]Kirkwood TBL DNA, mutations and aging Mutat Res/DNAging 1989 219 1 7 10.1016/0921-8734(89)90035-0 2643028 · DOI
  67. [83]Singh KK Mitochondrial DNA Mutations in Aging, Disease and Cancer Springer 2013 412
  68. [84]Vijg J Aging of the Genome: The Dual Role of DNA in Life and Death Oxford University Press 2007 372 10.1093/acprof:oso/9780198569237.001.0001 · DOI · Paper page
  69. [85]López-Otín C Blasco MA Partridge L Serrano M Kroemer G The hallmarks of aging Cell 2013 153 1194 217 10.1016/j.cell.2013.05.039 23746838 PMC3836174 · DOI · Paper page
  70. [86]Freitas AA de Magalhães JP A review and appraisal of the DNA damage theory of ageing Mutat Res 2011 728 12 22 10.1016/j.mrrev.2011.05.001 21600302 · DOI
  71. [87]Azzam EI Little JB The radiation-induced bystander effect: evidence and significance Hum Exp Toxicol 2004 23 61 65 10.1191/0960327104ht418oa 15070061 · DOI
  72. [88]Cucinotta FA Chappell LJ Non-targeted effects and the dose response for heavy ion tumor induction Mutat Res 2010 687 49 53 10.1016/j.mrfmmm.2010.01.012 20085778 · DOI
  73. [89]Barcellos-Hoff MH Costes SV A systems biology approach to multicellular and multi-generational radiation responses Mutat Res 2006 597 32 38 10.1016/j.mrfmmm.2005.09.008 16417910 · DOI
  74. [90]Xu S Wang J Ding N Hu W Zhang X Wang B Hua J Wei W Zhu Q Exosome-mediated microRNA transfer plays a role in radiation-induced bystander effect RNA Biol 2015 12 1355 63 10.1080/15476286.2015.1100795 26488306 PMC4829325 · DOI
  75. [91]Yuan D Xu J Wang J Pan Y Fu J Bai Y Zhang J Shao C Extracellular miR-1246 promotes lung cancer cell proliferation and enhances radioresistance by directly targeting DR5 Oncotarget 2016 7 32707 22 10.18632/oncotarget.9017 27129166 PMC5078045 · DOI
  76. [92]Al-Mayah A Bright S Chapman K Irons S Luo P Carter D Goodwin E Kadhim M The non-targeted effects of radiation are perpetuated by exosomes Mutat Res 2015 772 38 45 10.1016/j.mrfmmm.2014.12.007 25772109 · DOI
  77. [93]Jella KK Rani S O’Driscoll L McClean B Byrne HJ Lyng FM Exosomes are involved in mediating radiation induced bystander signaling in human keratinocyte cells Radiat Res 2014 181 138 45 10.1667/RR13337.1 24502353 · DOI
  78. [94]Jelonek K Widlak P Pietrowska M The Influence of Ionizing Radiation on Exosome Composition, Secretion and Intercellular Communication Protein Pept Lett 2016 23 656 63 10.2174/0929866523666160427105138 27117741 PMC5029112 · DOI
  79. [95]Arscott WT Camphausen KA Analysis of urinary exosomes to identify new markers of non-small-cell lung cancer Biomark Med 2011 5 822 22207914
  80. [96]Kaiser J Malignant messengers Science 2016 352 164 66 10.1126/science.352.6282.164 27124448 · DOI
  81. [97]Nilsson J Skog J Nordstrand A Baranov V Mincheva-Nilsson L Breakefield XO Widmark A Prostate cancer-derived urine exosomes: a novel approach to biomarkers for prostate cancer Br J Cancer 2009 100 1603 07 10.1038/sj.bjc.6605058 19401683 PMC2696767 · DOI
  82. [98]Jin H Wu Y Tan X The role of pancreatic cancer-derived exosomes in cancer progress and their potential application as biomarkers Clin Transl Oncol 2017 19 921 30 10.1007/s12094-017-1625-2 28168600 · DOI
  83. [99]Zhang Q Chen S Zeng L Chen Y Lian G Qian C Li J Xie R Huang KH New developments in the early diagnosis of pancreatic cancer Expert Rev Gastroenterol Hepatol 2017 11 149 56 10.1080/17474124.2017.1271323 27937041 · DOI
  84. [100]Gourlay J Morokoff AP Luwor RB Zhu HJ Kaye AH Stylli SS The emergent role of exosomes in glioma J Clin Neurosci 2017 35 13 23 10.1016/j.jocn.2016.09.021 27771233 · DOI
  85. [101]Bloomberg JJ Mulavara AP Changes in walking strategies after spaceflight IEEE Eng Med Biol Mag 2003 22 58 62 10.1109/MEMB.2003.1195697 12733460 · DOI
  86. [103]di Prampero PE Narici MV Muscles in microgravity: from fibres to human motion J Biomech 2003 36 403 12 10.1016/S0021-9290(02)00418-9 12594988 · DOI
  87. [104]Hopewell JW Models of CNS radiation damage during space flight Adv Space Res 1994 14 433 42 10.1016/0273-1177(94)90497-9 11539980 · DOI
  88. [105]Curtis SB Vazquez ME Wilson JW Atwell W Kim M Capala J Cosmic ray hit frequencies in critical sites in the central nervous system Adv Space Res 1998 22 197 207 10.1016/S0273-1177(98)80011-2 11541397 · DOI
  89. [106]Belov OV Batmunkh M Incerti S Lkhagva O Radiation damage to neuronal cells: simulating the energy deposition and water radiolysis in a small neural network Phys Med 2016 32 1510 20 10.1016/j.ejmp.2016.11.004 27865670 · DOI
  90. [107]Cucinotta FA Alp M Sulzman FM Wang M Space radiation risks to the central nervous system Life Sciences in Space Research 2014 2 54 69 10.1016/j.lssr.2014.06.003 · DOI · Paper page
  91. [108]Shtemberg AS Lebedeva-Georgievskaya KB Matveeva MI Kudrin VS Narkevich VB Klodt PM Bazyan AS Effect of space flight factors simulated in ground-based experiments on the behavior, discriminant learning, and exchange of monoamines in different brain structures of rats Biol Bull Russ Acad Sci 2014 41 161 67 25735169
  92. [109]Laack NN Brown PD Cognitive sequelae of brain radiation in adults Semin Oncol 2004 31 702 13 10.1053/j.seminoncol.2004.07.013 15497124 · DOI
  93. [111]Rabin BM Joseph JA Shukitt-Hale B Heavy particle irradiation, neurochemistry and behavior: thresholds, dose-response curves and recovery of function Adv Space Res 2004 33 1330 33 10.1016/j.asr.2003.09.051 15803623 · DOI · Paper page
  94. [112]Rabin BM Carrihill-Knoll KL Carey A Shukitt-Hale B Joseph JA Effect of diet on the disruption of operant responding at different ages following exposure to (56)Fe particles Age (Dordr) 2005 27 69 73 10.1007/s11357-005-4000-0 23598605 PMC3456091 · DOI
  95. [113]Higuchi Y Nashold BS Jr Sluijter M Cosman E Pearlstein RD Exposure of the dorsal root ganglion in rats to pulsed radiofrequency currents activates dorsal horn lamina I and II neurons Neurosurgery 2002 50 850 55 10.1097/00006123-200204000-00030 11904038 · DOI
  96. [114]Shukitt-Hale B Casadesus G McEwen JJ Rabin BM Joseph JA Spatial learning and memory deficits induced by exposure to iron-56-particle radiation Radiat Res 2000 154 28 33 10.1667/0033-7587(2000)154[0028:SLAMDI]2.0.CO;2 10856962 · DOI
  97. [115]Britten RA Jewell JS Davis LK Miller VD Hadley MM Semmes OJ Lonart G Dutta SM Changes in the Hippocampal Proteome Associated with Spatial Memory Impairment after Exposure to Low (20 cGy) Doses of 1 GeV/n56Fe Radiation Radiat Res 2017 187 287 97 10.1667/RR14067.1 28156212 · DOI
  98. [116]Rabin BM Hunt WA Joseph JA Dalton TK Kandasamy SB Relationship between linear energy transfer and behavioral toxicity in rats following exposure to protons and heavy particles Radiat Res 1991 128 216 21 10.2307/3578141 1658847 · DOI
  99. [117]Pecaut MJ Gridley DS Smith AL Nelson GA Dose and dose rate effects of whole-body proton-irradiation on lymphocyte blastogenesis and hematological variables: part II Immunol Lett 2002 80 67 73 10.1016/S0165-2478(01)00307-8 11716967 · DOI
  100. [118]Shtemberg AS Kokhan VS Kudrin VS Matveeva MI Lebedeva-Georgievskaya KD Timoshenko GN Molokanov AG Krasavin EA Narkevich VB Klodt PM Bazyan AS The effect of high-energy protons in the Bragg Peak on the behavior of rats and the exchange of monoamines in some brain structures Neurochem J 2015 9 66 72 10.1134/S1819712415010109 · DOI
  101. [119]Matveeva MI Shtemberg AS Timoshenko GN Krasavin EA Narkevich VB Klodt PM Kudrin VS Bazyan AS The effects of irradiation by 12C carbon ions on monoamine exchange in several rat brain structures Neurochem J 2013 7 303 07 10.1134/S1819712413040065 · DOI
  102. [120]Crocker LD Heller W Warren SL O’Hare AJ Infantolino ZP Miller GA Relationships among cognition, emotion, and motivation: implications for intervention and neuroplasticity in psychopathology Front Hum Neurosci 2013 7 261 10.3389/fnhum.2013.00261 23781184 PMC3678097 · DOI · Paper page
  103. [121]Frith C Dolan R The role of the prefrontal cortex in higher cognitive functions Brain Res Cogn Brain Res 1996 5 175 81 10.1016/S0926-6410(96)00054-7 9049084 · DOI · Paper page
  104. [123]Moffitt JA Foley CM Schadt JC Laughlin MH Hasser EM Attenuated baroreflex control of sympathetic nerve activity after cardiovascular deconditioning in rats Am J Physiol 1998 274 R1397 405 9612408
  105. [124]Mueller PJ Foley CM Hasser EM Hindlimb unloading alters nitric oxide and autonomic control of resting arterial pressure in conscious rats Am J Physiol Regul Integr Comp Physiol 2005 289 R140 47 10.1152/ajpregu.00820.2004 15761183 · DOI
  106. [125]Hargens AR Watenpaugh DE Cardiovascular adaptation to spaceflight Med Sci Sports Exerc 1996 28 977 82 10.1097/00005768-199608000-00007 8871907 · DOI
  107. [126]Zipes DP Heart-brain interactions in cardiac arrhythmias: role of the autonomic nervous system Cleve Clin J Med 2008 Suppl 2 75 S94 96 10.3949/ccjm.75.Suppl_2.S94 18540155 · DOI
  108. [127]Lahiri MK Kannankeril PJ Goldberger JJ Assessment of autonomic function in cardiovascular disease: physiological basis and prognostic implications J Am Coll Cardiol 2008 51 1725 33 10.1016/j.jacc.2008.01.038 18452777 · DOI
  109. [128]Vaseghi M Shivkumar K The role of the autonomic nervous system in sudden cardiac death Prog Cardiovasc Dis 2008 50 404 19 10.1016/j.pcad.2008.01.003 18474284 PMC2752648 · DOI
  110. [129]Foster C Meyer K Georgakopoulos N Ellestad AJ Fitzgerald DJ Tilman K Weinstein H Young H Roskamm H Left ventricular function during interval and steady state exercise Med Sci Sports Exerc 1999 31 1157 62 10.1097/00005768-199908000-00012 10449018 · DOI
  111. [130]Delp MD Charvat JM Limoli CL Globus RK Ghosh P Apollo Lunar Astronauts Show Higher Cardiovascular Disease Mortality: Possible Deep Space Radiation Effects on the Vascular Endothelium Sci Rep 2016 6 29901 10.1038/srep29901 27467019 PMC4964660 · DOI
  112. [131]Cucinotta FA Hamada N Little MP No evidence for an increase in circulatory disease mortality in astronauts following space radiation exposures Life Sci Space Res (Amst) 2016 10 53 56 10.1016/j.lssr.2016.08.002 27662788 · DOI
  113. [132]Konstantinova IV Antropova EN Legen’kov VI Zazhireĭ VD [Reactivity of lymphoid blood cells in the crew of “Soiuz-6”, “Soiuz-7” and “Soiuz-8” spacecraft before and after flight]. [Article in Russian] Kosm Biol Med 1973 7 35 40 4779034
  114. [133]Grivennikov SI Greten FR Karin M Immunity, inflammation, and cancer Cell 2010 140 883 99 10.1016/j.cell.2010.01.025 20303878 PMC2866629 · DOI · Paper page
  115. [134]Crucian BE Zwart SR Mehta S Uchakin P Quiriarte HD Pierson D Sams CF Smith SM Plasma cytokine concentrations indicate that in vivo hormonal regulation of immunity is altered during long-duration spaceflight J Interferon Cytokine Res 2014 34 778 86 10.1089/jir.2013.0129 24702175 PMC4186776 · DOI · Paper page
  116. [135]Taylor PW Impact of space flight on bacterial virulence and antibiotic susceptibility Infect Drug Resist 2015 8 249 62 10.2147/IDR.S67275 26251622 PMC4524529 · DOI
  117. [136]Guéguinou N Huin-Schohn C Bascove M Bueb JL Tschirhart E Legrand-Frossi C Frippiat JP Could spaceflight-associated immune system weakening preclude the expansion of human presence beyond Earth's orbit? J Leukoc Biol 2009 86 1027 38 10.1189/jlb.0309167 19690292 · DOI · Paper page
  118. [137]Anderson RE Warner NL Ionizing radiation and the immune response Adv Immunol 1976 24 215 335 10.1016/S0065-2776(08)60331-4 14486 · DOI
  119. [138]George KA Hada M Cucinotta FA Biological Effectiveness of Accelerated Protons for Chromosome Exchanges Front Oncol 2015 5 226 10.3389/fonc.2015.00226 26539409 PMC4610205 · DOI
  120. [139]Schrek R Qualitative and quantitative reactions of lymphocytes to x rays Ann N Y Acad Sci 1961 95 839 48 10.1111/j.1749-6632.1961.tb50080.x 13909294 · DOI
  121. [140]Fernandez-Gonzalo R Baatout S Moreels M Impact of Particle Irradiation on the Immune System: From the Clinic to Mars Front Immunol 2017 8 177 10.3389/fimmu.2017.00177 28275377 PMC5319970 · DOI
  122. [141]Gridley DS Luo-Owen X Rizvi A Makinde A Pecaut M Mao XW Slater JM Low-dose photon and simulated solar particle event proton effects on Foxp3+ T regulatory cells and other leukocytes Technol Cancer Res Treat 2010 9 637 49 10.1177/153303461000900612 21070086 · DOI
  123. [142]Gridley DS Rizvi A Makinde AY Luo-Owen X Mao XW Tian J Slater JM Pecaut MJ Space-relevant radiation modifies cytokine profiles, signaling proteins and Foxp3+ T cells Int J Radiat Biol 2013 89 26 35 10.3109/09553002.2012.715792 22852758 · DOI
  124. [143]Rizvi A Pecaut MJ Gridley DS Low-dose gamma-rays and simulated solar particle event protons modify splenocyte gene and cytokine expression patterns J Radiat Res (Tokyo) 2011 52 701 11 10.1269/jrr.10107 21971034 · DOI
  125. [144]Rizvi A Pecaut MJ Slater JM Subramaniam S Gridley DS Low-dose γ-rays modify CD4(+) T cell signalling response to simulated solar particle event protons in a mouse model Int J Radiat Biol 2011 87 24 35 10.3109/09553002.2010.518206 21142612 · DOI
  126. [145]Stratton MR Campbell PJ Futreal PA The cancer genome Nature 2009 458 719 24 10.1038/nature07943 19360079 PMC2821689 · DOI
  127. [146]Preston DL Ron E Tokuoka S Funamoto S Nishi N Soda M Mabuchi K Kodama K Solid cancer incidence in atomic bomb survivors: 1958-1998 Radiat Res 2007 168 1 64 10.1667/RR0763.1 17722996 · DOI
  128. [147]de Magalhães JP How ageing processes influence cancer Nat Rev Cancer 2013 13 357 65 10.1038/nrc3497 23612461 · DOI · Paper page
  129. [148]Peto J Cancer epidemiology in the last century and the next decade Nature 2001 411 390 95 10.1038/35077256 11357148 · DOI
  130. [149]Baginska J Viry E Paggetti J Medves S Berchem G Moussay E Janji B The critical role of the tumor microenvironment in shaping natural killer cell-mediated anti-tumor immunity Front Immunol 2013 4 490 10.3389/fimmu.2013.00490 24400010 PMC3872331 · DOI
  131. [150]Howcroft TK Campisi J Louis GB Smith MT Wise B Wyss-Coray T Augustine AD McElhaney JE Kohanski R Sierra F The role of inflammation in age-related disease Aging (Albany NY) 2013 5 84 93 10.18632/aging.100531 23474627 PMC3616233 · DOI · Paper page
  132. [151]Cucinotta FA Durante M Cancer risk from exposure to galactic cosmic rays: implications for space exploration by human beings Lancet Oncol 2006 7 431 35 10.1016/S1470-2045(06)70695-7 16648048 · DOI
  133. [152]Anisimov VN Sikora E Pawelec G Relationships between cancer and aging: a multilevel approach Biogerontology 2009 10 323 38 10.1007/s10522-008-9209-8 19156531 · DOI
  134. [153]Baker DJ Dawlaty MM Wijshake T Jeganathan KB Malureanu L van Ree JH Crespo-Diaz R Reyes S Seaburg L Shapiro V Behfar A Terzic A van de Sluis B van Deursen JM Increased expression of BubR1 protects against aneuploidy and cancer and extends healthy lifespan Nat Cell Biol 2013 15 96 102 10.1038/ncb2643 23242215 PMC3707109 · DOI
  135. [154]Moolgavkar SH Venzon DJ Two-event models for carcinogenesis: incidence curves for childhood and adult tumors Math Biosci 1979 47 55 77 10.1016/0025-5564(79)90005-1 · DOI
  136. [155]Hoeijmakers JH DNA damage, aging, and cancer N Engl J Med 2009 361 1475 85 10.1056/NEJMra0804615 19812404 · DOI · Paper page
  137. [157]Sridharan DM Asaithamby A Bailey SM Costes SV Doetsch PW Dynan WS Kronenberg A Rithidech KN Saha J Snijders AM Werner E Wiese C Cucinotta FA Pluth JM Understanding cancer development processes after HZE-particle exposure: roles of ROS, DNA damage repair and inflammation Radiat Res 2015 183 1 26 10.1667/RR13804.1 25564719 · DOI · Paper page
  138. [158]Yang TC Craise LM Mei MT Tobias CA Neoplastic cell transformation by heavy charged particles Radiat Res Suppl 1985 8 S177 87 10.2307/3583525 3867082 · DOI
  139. [159]George K Durante M Wu H Willingham V Cucinotta FA In vivo and in vitro measurements of complex-type chromosomal exchanges induced by heavy ions Adv Space Res 2003 31 1525 35 10.1016/S0273-1177(03)00088-7 12971407 · DOI
  140. [160]George K Cucinotta FA The influence of shielding on the biological effectiveness of accelerated particles for the induction of chromosome damage Adv Space Res 2007 39 1076 81 10.1016/j.asr.2007.01.004 · DOI
  141. [161]Kiefer J Schreiber A Gutermuth F Koch S Schmidt P Mutation induction by different types of radiation at the Hprt locus Mutat Res 1999 431 429 48 10.1016/S0027-5107(99)00184-0 10636006 · DOI
  142. [163]Alpen EL Powers-Risius P Curtis SB DeGuzman R Fry RJ Fluence-based relative biological effectiveness for charged particle carcinogenesis in mouse Harderian gland Adv Space Res 1994 14 573 81 10.1016/0273-1177(94)90512-6 11539994 · DOI
  143. [165]Dicello JF Christian A Cucinotta FA Gridley DS Kathirithamby R Mann J Markham AR Moyers MF Novak GR Piantadosi S Ricart-Arbona R Simonson DM Strandberg JD In vivo mammary tumourigenesis in the Sprague-Dawley rat and microdosimetric correlates Phys Med Biol 2004 49 3817 30 10.1088/0031-9155/49/16/024 15446807 · DOI
  144. [166]Burns FJ Hosselet S Jin Y Dudas G Garte SJ Progression and multiple events in radiation carcinogenesis of rat skin J Radiat Res (Tokyo) 1991 Suppl 2 32 202 16 10.1269/jrr.32.SUPPLEMENT2_202 1823357 · DOI
  145. [167]Burns FJ Zhao P Xu G Roy N Loomis C Fibroma induction in rat skin following single or multiple doses of 1.0 GeV/nucleon 56Fe ions from the Brookhaven Alternating Gradient Synchrotron (AGS) Phys Med 2001 suppl 1 17 194 95 11776259
  146. [168]Ullrich RL Preston RJ Myeloid leukemia in male RFM mice following irradiation with fission spectrum neutrons or γ rays Radiat Res 1987 109 165 70 10.2307/3576877 3468555 · DOI
  147. [169]Boice JD Jr Leukemia risk in thorotrast patients Radiat Res 1993 136 301 02 10.2307/3578628 8248491 · DOI
  148. [170]Miousse IR Chalbot MC Aykin-Burns N Wang X Basnakian A Kavouras IG Koturbash I Epigenetic alterations induced by ambient particulate matter in mouse macrophages Environ Mol Mutagen 2014 55 428 35 10.1002/em.21855 24535919 PMC4162398 · DOI
  149. [171]Zheng X Zhang X Ding L Lee JR Weinberger PM Dynan WS Synergistic effect of high charge and energy particle radiation and chronological age on biomarkers of oxidative stress and tissue degeneration: a ground-based study using the vertebrate laboratory model organism Oryzias latipes PLoS One 2014 9 e111362 10.1371/journal.pone.0111362 25375139 PMC4222877 · DOI
  150. [172]George K Wu H Willingham V Cucinotta FA The effect of space radiation on the induction of chromosome damage Phys Med 2001 Suppl 1 17 222 25 11776981
  151. [173]George K Willingham V Cucinotta FA Stability of chromosome aberrations in the blood lymphocytes of astronauts measured after space flight by FISH chromosome painting Radiat Res 2005 164 474 80 10.1667/RR3323.1 16187752 · DOI
  152. [174]Jasinski-Bergner S Mandelboim O Seliger B The role of microRNAs in the control of innate immune response in cancer J Natl Cancer Inst 2014 106 dju257 10.1093/jnci/dju257 25217579 · DOI
  153. [175]Raisch J Darfeuille-Michaud A Nguyen HT Role of microRNAs in the immune system, inflammation and cancer World J Gastroenterol 2013 19 2985 96 10.3748/wjg.v19.i20.2985 23716978 PMC3662938 · DOI
  154. [176]Koturbash I Zemp FJ Kutanzi K Luzhna L Loree J Kolb B Kovalchuk O Sex-specific microRNAome deregulation in the shielded bystander spleen of cranially exposed mice Cell Cycle 2008 7 1658 67 10.4161/cc.7.11.5981 18560276 · DOI
  155. [177]Harries LW MicroRNAs as Mediators of the Ageing Process Genes (Basel) 2014 5 656 70 10.3390/genes5030656 25140888 PMC4198923 · DOI
  156. [178]Jima DD Zhang J Jacobs C Richards KL Dunphy CH Choi WW Au WY Srivastava G Czader MB Rizzieri DA Lagoo AS Lugar PL Mann KP Hematologic Malignancies Research Consortium Deep sequencing of the small RNA transcriptome of normal and malignant human B cells identifies hundreds of novel microRNAs Blood 2010 116 e118 27 10.1182/blood-2010-05-285403 20733160 PMC3012600 · DOI
  157. [179]Mazan-Mamczarz K Gartenhaus RB Role of microRNA deregulation in the pathogenesis of diffuse large B-cell lymphoma (DLBCL) Leuk Res 2013 37 1420 28 10.1016/j.leukres.2013.08.020 24054860 PMC3856880 · DOI
  158. [180]Lujambio A Lowe SW The microcosmos of cancer Nature 2012 482 347 55 10.1038/nature10888 22337054 PMC3509753 · DOI · Paper page
  159. [181]Yanaihara N Caplen N Bowman E Seike M Kumamoto K Yi M Stephens RM Okamoto A Yokota J Tanaka T Calin GA Liu CG Croce CM Harris CC Unique microRNA molecular profiles in lung cancer diagnosis and prognosis Cancer Cell 2006 9 189 98 10.1016/j.ccr.2006.01.025 16530703 · DOI · Paper page
  160. [182]Metheetrairut C Slack FJ MicroRNAs in the ionizing radiation response and in radiotherapy Curr Opin Genet Dev 2013 23 12 19 10.1016/j.gde.2013.01.002 23453900 PMC3617065 · DOI
  161. [183]Cucinotta FA Schimmerling W Wilson JW Peterson LE Badhwar GD Saganti PB Dicello JF Space radiation cancer risks and uncertainties for Mars missions Radiat Res 2001 156 682 88 10.1667/0033-7587(2001)156[0682:SRCRAU]2.0.CO;2 11604093 · DOI · Paper page
  162. [185]Doarn CR Medical policy development for human spaceflight at NASA: an evolution Aviat Space Environ Med 2011 82 1073 77 10.3357/ASEM.3103.2011 22097646 · DOI
  163. [186]Mortazavi SM Cameron JR Niroomand-rad A Adaptive response studies may help choose astronauts for long-term space travel Adv Space Res 2003 31 1543 51 10.1016/S0273-1177(03)00089-9 12971409 · DOI
  164. [187]Ushakov IB Shtemberg AS [The organism tolerance to extreme factors: physiological basis, regulation, prediction] [Article in Russian] Usp Fiziol Nauk 2011 42 26 45 21950007
  165. [188]Mortazavi S How Does Biological Protection Help Astronauts Tolerate High Levels of Radiation During Deep Space Manned Missions 2017 Available from: https://www.researchgate.net/profile/SMJ_Mortazavi/publication/316917673_How_Does_Biological_Protection_Help_Astronauts_Tolerate_High_Levels_of_Radiation_-_City_College_of_New_York-_New_York_-_May_11_2017/links/59184d40a6fdcc963e867e85/How-Does-Biological-Protection-Help-Astronauts-Tolerate-High-Levels-of-Radiation-City-College-of-New-York-New-York-May-11-2017.pdf
  166. [190]Asaithamby A Hu B Chen DJ Unrepaired clustered DNA lesions induce chromosome breakage in human cells Proc Natl Acad Sci USA 2011 108 8293 98 10.1073/pnas.1016045108 21527720 PMC3100920 · DOI
  167. [191]Pustovalova M Grekhova A Astrelina T Nikitina V Dobrovolskaya E Suchkova Y Kobzeva I Usupzhanova D Vorobyeva N Samoylov A Bushmanov A Ozerov IV Zhavoronkov A Accumulation of spontaneous γH2AX foci in long-term cultured mesenchymal stromal cells Aging (Albany NY) 2016 8 3498 506 10.18632/aging.101142 27959319 PMC5270682 · DOI
  168. [192]Marcon F Andreoli C Rossi S Verdina A Galati R Crebelli R Assessment of individual sensitivity to ionizing radiation and DNA repair efficiency in a healthy population Mutat Res 2003 541 1 8 10.1016/S1383-5718(03)00171-2 14568289 · DOI
  169. [193]Bosi A Olivieri G Variability of the adaptive response to ionizing radiations in humans Mutat Res 1989 211 13 17 10.1016/0027-5107(89)90102-4 2921997 · DOI
  170. [194]Zorin V Zorina A Smetanina N Kopnin P Ozerov IV Leonov S Isaev A Klokov D Osipov AN Diffuse colonies of human skin fibroblasts in relation to cellular senescence and proliferation Aging (Albany NY) 2017 9 1404 13 10.18632/aging.101240 28522793 PMC5472740 · DOI
  171. [195]Desai N Davis E O’Neill P Durante M Cucinotta FA Wu H Immunofluorescence detection of clustered gamma-H2AX foci induced by HZE-particle radiation Radiat Res 2005 164 518 22 10.1667/RR3431.1 16187760 · DOI
  172. [196]Groesser T Fontenay GV Han J Chang H Pluth J Parvin B Quantification of the Dynamics of DNA Repair to Ionizing Radiation via Colocalization of 53BP1 and ɣH2AX Video Bioinformatics Cham Springer 2015 253 63
  173. [197]Torudd J Protopopova M Sarimov R Nygren J Eriksson S Markova E Chovanec M Selivanova G Belyaev IY Dose-response for radiation-induced apoptosis, residual 53BP1 foci and DNA-loop relaxation in human lymphocytes. IInt J Radiat Biol 2005 81 125 38 10.1080/09553000500077211 16019922 · DOI
  174. [198]Lobachevsky P Leong T Daly P Smith J Best N Tomaszewski J Thompson ER Li N Campbell IG Martin RF Martin OA Compromized DNA repair as a basis for identification of cancer radiotherapy patients with extreme radiosensitivity Cancer Lett 2016 383 212 19 10.1016/j.canlet.2016.09.010 27693457 PMC5159273 · DOI
  175. [199]Grekhova AK Eremin PS Osipov AN Eremin II Pustovalova MV Ozerov IV Smetanina NM Lazareva NL Vorobyeva NY Pulin AA Maksimova OA Gordeev AV Bushmanov AY Kotenko KV [Slow Formation and Degradation of γH2AX Foci in Human Skin Fibroblasts Exposed to Low-Dose X-Ray Radiation]. [Article in Russian] Radiats Biol Radioecol 2015 55 395 401 26601539
  176. [200]Saha J Wang M Cucinotta FA Investigation of switch from ATM to ATR signaling at the sites of DNA damage induced by low and high LET radiation DNA Repair (Amst) 2013 12 1143 51 10.1016/j.dnarep.2013.10.004 24238855 · DOI
  177. [201]Tsvetkova A Ozerov IV Pustovalova M Grekhova A Eremin P Vorobyeva N Eremin I Pulin A Zorin V Kopnin P Leonov S Zhavoronkov A Klokov D Osipov AN γH2AX, 53BP1 and Rad51 protein foci changes in mesenchymal stem cells during prolonged X-ray irradiation Oncotarget 2017 8 64317 29 10.18632/oncotarget.19203 28969073 PMC5610005 · DOI
  178. [202]Pustovalova M Astrelina TA Grekhova A Vorobyeva N Tsvetkova A Blokhina T Nikitina V Suchkova Y Usupzhanova D Brunchukov V Kobzeva I Karaseva T Ozerov IV Residual γH2AX foci induced by low dose x-ray radiation in bone marrow mesenchymal stem cells do not cause accelerated senescence in the progeny of irradiated cells Aging (Albany NY) 2017 9 2397 410 10.18632/aging.101327 29165316 PMC5723693 · DOI
  179. [203]Belli M Sapora O Tabocchini MA Molecular targets in cellular response to ionizing radiation and implications in space radiation protection J Radiat Res (Tokyo) 2002 Suppl 43 S13 19 10.1269/jrr.43.S13 12793724 · DOI
  180. [204]Durante M Kronenberg A Ground-based research with heavy ions for space radiation protection Adv Space Res 2005 35 180 84 10.1016/j.asr.2004.12.034 15934192 · DOI
  181. [205]Rashi-Elkeles S Warnatz HJ Elkon R Kupershtein A Chobod Y Paz A Amstislavskiy V Sultan M Safer H Nietfeld W Lehrach H Shamir R Yaspo ML Shiloh Y Parallel profiling of the transcriptome, cistrome, and epigenome in the cellular response to ionizing radiation Sci Signal 2014 7 rs3 10.1126/scisignal.2005032 24825921 · DOI
  182. [206]Ozerov IV Lezhnina KV Izumchenko E Artemov AV Medintsev S Vanhaelen Q Aliper A Vijg J Osipov AN Labat I West MD Buzdin A Cantor CR In silico Pathway Activation Network Decomposition Analysis (iPANDA) as a method for biomarker development Nat Commun 2016 7 13427 10.1038/ncomms13427 27848968 PMC5116087 · DOI
  183. [207]Mettler FA Jr Brenner D Coleman CN Kaminski JM Kennedy AR Wagner LK Can radiation risks to patients be reduced without reducing radiation exposure? The status of chemical radioprotectants AJR Am J Roentgenol 2011 196 616 18 10.2214/AJR.10.4959 21343505 · DOI
  184. [208]Maier P Hartmann L Wenz F Herskind C Cellular Pathways in Response to Ionizing Radiation and Their Targetability for Tumor Radiosensitization Int J Mol Sci 2016 17 E102 10.3390/ijms17010102 26784176 PMC4730344 · DOI
  185. [209]Braunstein S Badura ML Xi Q Formenti SC Schneider RJ Regulation of protein synthesis by ionizing radiation Mol Cell Biol 2009 29 5645 56 10.1128/MCB.00711-09 19704005 PMC2772731 · DOI
  186. [210]Magné N Toillon RA Bottero V Didelot C Houtte PV Gérard JP Peyron JF NF-kappaB modulation and ionizing radiation: mechanisms and future directions for cancer treatment Cancer Lett 2006 231 158 68 10.1016/j.canlet.2005.01.022 16399220 · DOI
  187. [211]Venkata Narayanan I Paulsen MT Bedi K Berg N Ljungman EA Francia S Veloso A Magnuson B di Fagagna FD Wilson TE Ljungman M Transcriptional and post-transcriptional regulation of the ionizing radiation response by ATM and p53 Sci Rep 2017 7 43598 10.1038/srep43598 28256581 PMC5335570 · DOI
  188. [212]Moskalev AA Plyusnina EN Shaposhnikov MV Radiation hormesis and radioadaptive response in Drosophila melanogaster flies with different genetic backgrounds: the role of cellular stress-resistance mechanisms Biogerontology 2011 12 253 63 10.1007/s10522-011-9320-0 21234801 · DOI
  189. [213]Munshi A Ramesh R Mitogen-activated protein kinases and their role in radiation response Genes Cancer 2013 4 401 08 10.1177/1947601913485414 24349638 PMC3863336 · DOI
  190. [214]Williams K Christensen J Rappsilber J Nielsen AL Johansen JV Helin K The histone lysine demethylase JMJD3/KDM6B is recruited to p53 bound promoters and enhancer elements in a p53 dependent manner PLoS One 2014 9 e96545 10.1371/journal.pone.0096545 24797517 PMC4010471 · DOI
  191. [215]Kim AH Lebman DA Dietz CM Snyder SR Eley KW Chung TD Transforming growth factor-beta is an endogenous radioresistance factor in the esophageal adenocarcinoma cell line OE-33 Int J Oncol 2003 23 1593 99 14612931
  192. [216]Matusiewicz R Stempniak M Lebiedowski K Czajkowski M [The most frequent complications during long-term corticotherapy] [Article in Polish] Wiad Lek 1989 42 273 77 2815743
  193. [217]Seong KM Yu M Lee KS Park S Jin YW Min KJ Curcumin mitigates accelerated aging after irradiation in Drosophila by reducing oxidative stress BioMed Res Int 2015 2015 425380 10.1155/2015/425380 25815315 PMC4359819 · DOI
  194. [218]Proshkina E Lashmanova E Dobrovolskaya E Zemskaya N Kudryavtseva A Shaposhnikov M Moskalev A Geroprotective and Radioprotective Activity of Quercetin, (−)-Epicatechin, and Ibuprofen in Drosophila melanogaster Front Pharmacol 2016 7 505 10.3389/fphar.2016.00505 28066251 PMC5179547 · DOI
  195. [219]Moskalev A Chernyagina E de Magalhães JP Barardo D Thoppil H Shaposhnikov M Budovsky A Fraifeld VE Garazha A Tsvetkov V Bronovitsky E Bogomolov V Scerbacov A Geroprotectors.org: a new, structured and curated database of current therapeutic interventions in aging and age-related disease Aging (Albany NY) 2015 7 616 28 10.18632/aging.100799 26342919 PMC4600621 · DOI
  196. [220]Barardo D Thornton D Thoppil H Walsh M Sharifi S Ferreira S Anžič A Fernandes M Monteiro P Grum T Cordeiro R De-Souza EA Budovsky A The DrugAge database of aging-related drugs Aging Cell 2017 16 594 97 10.1111/acel.12585 28299908 PMC5418190 · DOI · Paper page
  197. [223]Badiello R Ceschel GC Esposito B Radioprotective effects of glutathione on molecular systems J Radioanal Nucl Chem 1998 229 149 52 10.1007/BF02389464 · DOI
  198. [224]Jensen GL Meister A Radioprotection of human lymphoid cells by exogenously supplied glutathione is mediated by gamma-glutamyl transpeptidase Proc Natl Acad Sci USA 1983 80 4714 17 10.1073/pnas.80.15.4714 6136037 PMC384114 · DOI
  199. [225]Hashimoto K Takasaki W Yamoto T Manabe S Sato I Tsuda S Effect of glutathione (GSH) depletion on DNA damage and blood chemistry in aged and young rats J Toxicol Sci 2008 33 421 29 10.2131/jts.33.421 18827442 · DOI
  200. [226]Raghuraman M Verma P Kunwar A Phadnis PP Jain VK Priyadarsini KI Cellular evaluation of diselenonicotinamide (DSNA) as a radioprotector against cell death and DNA damage Metallomics 2017 9 715 25 10.1039/C7MT00034K 28503683 · DOI

200 of 257 shown

Authors
Cortese, F., Klokov, D., Osipov, A., Stefaniak, J., Moskalev, A., Schastnaya, J., Cantor, C., Aliper, A., Mamoshina, P., Ushakov, I., Sapetsky, A., Vanhaelen, Q., Alchinova, I., Karganov, M., Kovalchuk, O., Wilkins, R., Shtemberg, A., Moreels, M., Baatout, S., Izumchenko, E., de Magalhães, J. P., Artemov, A. V., Costes, S. V., Beheshti, A., Mao, X. W., Pecaut, M. J., Kaminskiy, D., Ozerov, I. V., Scheibye-Knudsen, M., & Zhavoronkov, A.
Affiliations
  • Queen's University (CA)
  • University of Ottawa (CA)
  • Johns Hopkins University (US)
  • University of Oxford (GB)
  • Engelhardt Institute of Molecular Biology (RU)
  • Boston University (US)
  • State Research Center - Burnasyan Federal Medical Biophysical Center of Federal Medical Biological Agency, Moscow, Russia
  • Research Institute of General Pathology and Pathophysiology, the Russian Academy of Medical Sciences (RU)
  • University of Lethbridge (CA)
  • Health Canada (CA)
  • Russian Academy of Sciences (RU)
  • Belgian Nuclear Research Centre (BE)
  • Ghent University (BE)
  • Biogerontology Research Foundation, London, UK
  • Ames Research Center (US)
  • Loma Linda University (US)
  • Center for Healthy Aging, University of Copenhagen, Copenhagen, Denmark
Venue
Oncotarget
Published
2018-02-12
Volume
9
Issue
18
Pages
14692-14722
ISSN
1949-2553 (ISSN-L)
OpenAlex
W2792124893
Cited by
83
References
288
Citations by year
2026: 4 · 2025: 5 · 2024: 10 · 2023: 13 · 2022: 8 · 2021: 12 · 2020: 11 · 2019: 17 · 2018: 3
FWCI
1.68
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Oncotarget (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by)
  • Ghent University Academic Bibliography (Ghent University) (submittedVersion, cc-by)
Funders
Russian Foundation for Basic Research (17–29–01002)
Topics
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
  • Health Sciences › Medicine › Physiology › Spaceflight effects on biology
  • Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Radiation Therapy and Dosimetry
Keywords
radioresistance (biology), deep space exploration, space colonization, high-LET radiation, cosmic rays, DNA repair, radiation protection, gene therapy, metabolic rate reduction, cognitive function, longevity, healthspan

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