Effects of microgravity on DNA damage response in Caenorhabditis elegans during Shenzhou-8 spaceflight

References

• Abbotts R, Thompson N, Madhusudan S. 2014. DNA repair in cancer: Emerging targets for personalized therapy. Cancer Manag Res 6:77–92.
   PubMed Web of Science ®Google Scholar
• Adachi R, Takaya T, Kuriyama K, Higashibata A, Ishioka N, Kagawa H. 2008. Spaceflight results in increase of thick filament but not thin filament proteins in the paramyosin mutant of Caenorhabditis elegans. Adv Space Res 41:816–823.
   Web of Science ®Google Scholar
• Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. 2000. Gene ontology: Tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29.
   PubMed Web of Science ®Google Scholar
• Aubert AE, Beckers F, Verheyden B. 2005. Cardiovascular function and basics of physiology in microgravity. Acta Cardiol 60:129–151.
   PubMed Web of Science ®Google Scholar
• Bartel DP. 2009. MicroRNAs: Target recognition and regulatory functions. Cell 136:215–233.
   PubMed Web of Science ®Google Scholar
• Betel D, Wilson M, Gabow A, Marks DS, Sander C. 2008. The microRNA.org resource: Targets and expression. Nucleic Acids Res 36:D149–153.
   PubMed Web of Science ®Google Scholar
• Blaise BJ, Giacomotto J, Elena B, Dumas ME, Toulhoat P, Segalat L, Emsley L. 2007. Metabotyping of Caenorhabditis elegans reveals latent phenotypes. Proc Natl Acad Sci USA 104:19808–19812.
   PubMed Web of Science ®Google Scholar
• Boule JB, Vega LR, Zakian VA. 2005. The yeast Pif1p helicase removes telomerase from telomeric DNA. Nature 438:57–61.
   PubMed Web of Science ®Google Scholar
• Burnell AM, Houthoofd K, O’Hanlon K, Vanfleteren JR. 2005. Alternate metabolism during the dauer stage of the nematode Caenorhabditis elegans. Exp Gerontol 40:850–856.
   Google Scholar
• Cucinotta FA, Durante M. 2006. Cancer risk from exposure to galactic cosmic rays: Implications for space exploration by human beings. Lancet Oncol 7:431–435.
   PubMed Web of Science ®Google Scholar
• Cucinotta FA, Manuel FK, Jones J, Iszard G, Murrey J, Djojonegro B, Wear M. 2001. Space radiation and cataracts in astronauts. Radiat Res 156:460–466.
   PubMed Web of Science ®Google Scholar
• Dallaire A, Garand C, Paquel ER, Mitchell SJ, de Cabo R, Simard MJ, Lebel M. 2012. Down regulation of miR-124 in both Werner syndrome DNA helicase mutant mice and mutant Caenorhabditis elegans wrn-1 reveals the importance of this microRNA in accelerated aging. Aging (Albany NY) 4:636–647.
   PubMedGoogle Scholar
• Degan P, Sancandi M, Zunino A, Ottaggio L, Viaggi S, Cesarone F, Pippia P, Galleri G, Abbondandolo A. 2005. Exposure of human lymphocytes and lymphoblastoid cells to simulated microgravity strongly affects energy metabolism and DNA repair. J Cell Biochem 94:460–469.
   PubMed Web of Science ®Google Scholar
• Deng X, Ma L, Wu M, Zhang G, Jin C, Guo Y, Liu R. 2013. miR-124 radiosensitizes human glioma cells by targeting CDK4. J Neurooncol 114:263–274.
   PubMed Web of Science ®Google Scholar
• Dziegielewski J, Goetz W, Baulch JE. 2010. Heavy ions, radioprotectors and genomic instability: Implications for human space exploration. Radiat Environ Biophys 49:303–316.
   PubMed Web of Science ®Google Scholar
• Eki T, Ishihara T, Katsura I, Hanaoka F. 2007. A genome-wide survey and systematic RNAi-based characterization of helicase-like genes in Caenorhabditis elegans. DNA Res 14:183–199.
   PubMed Web of Science ®Google Scholar
• Farshid AA, Tamaddonfard E, Simaee N, Mansouri S, Najafi S, Asri-Rezaee S, Alavi H. 2013. Effects of histidine and N-acetylcysteine on doxorubicin-induced cardiomyopathy in rats. Cardiovasc Toxicol 2:153–161.
   Google Scholar
• Ferreira HC, Towbin BD, Jegou T, Gasser SM. 2013. The shelterin protein POT-1 anchors Caenorhabditis elegans telomeres through SUN-1 at the nuclear periphery. J Cell Biol 203:727–735.
   PubMed Web of Science ®Google Scholar
• Forrester HB, Li J, Hovan D, Ivashkevich AN, Sprung CN. 2012. DNA repair genes: Alternative transcription and gene expression at the exon level in response to the DNA damaging agent, ionizing radiation. PLoS One 7:e53358.
   PubMed Web of Science ®Google Scholar
• Girardi C, De Pitta C, Casara S, Sales G, Lanfranchi G, Celotti L, Mognato M. 2012. Analysis of miRNA and mRNA expression profiles highlights alterations in ionizing radiation response of human lymphocytes under modeled microgravity. PLoS One 7:e31293.
   PubMed Web of Science ®Google Scholar
• Greiss S, Schumacher B, Grandien K, Rothblatt J, Gartner A. 2008. Transcriptional profiling in C.elegans suggests DNA damage dependent apoptosis as an ancient function of the p53 family. BMC Genomics 9:1–10.
   PubMedGoogle Scholar
• Hada M, Georgakilas AG. 2008. Formation of clustered DNA damage after high-LET irradiation: A review. J Radiat Res 49:203–210.
   PubMed Web of Science ®Google Scholar
• Harper JW, Elledge SJ. 2007. The DNA damage response: Ten years after. Mol Cell 28:739–745.
   PubMed Web of Science ®Google Scholar
• Hartman PS, Hlavacek A, Wilde H, Lewicki D, Schubert W, Kern RG, Kazarians GA, Benton EV, Benton ER, Nelson GA. 2001. A comparison of mutations induced by accelerated iron particles versus those induced by low earth orbit space radiation in the FEM-3 gene of Caenorhabditis elegans. Mutat Res 474:47–55.
   PubMed Web of Science ®Google Scholar
• Hei TK, Zhao Y, Zhou H, Ivanov V. 2011. Mechanism of radiation carcinogenesis: Role of the TGFBI gene and the inflammatory signaling cascade. Adv Exp Med Biol 720:163–170.
   PubMed Web of Science ®Google Scholar
• Higashibata A, Higashitani A, Adachi R, Kagawa H, Honda S, Honda Y, Higashitani N, Sasagawa Y, Miyazawa Y, Szewczyk NJ, Conley CA, Fujimoto N, Fukui K, Shimazu T, Kuriyama K, Ishioka N. 2007. Biochemical and molecular biological analyses of space-flown nematodes in Japan, the First International Caenorhabditis elegans Experiment (ICE-First). Microgravity Sci Technol 19: 159–163.
   PubMed Web of Science ®Google Scholar
• Higashibata A, Szewczyk NJ, Conley CA, Imamizo-Sato M, Higashitani A, Ishioka N. 2006. Decreased expression of myogenic transcription factors and myosin heavy chains in Caenorhabditis elegans muscles developed during spaceflight. J Exp Biol 209:3209–3218.
   PubMed Web of Science ®Google Scholar
• Higashitani A, Higashibata A, Sasagawa Y, Sugimoto T, Miyazawa Y, Szewcyk NJ, Viso M, Gasset G, Eche B, Fukui K, Shimazu T, Fujimoto N, Kuriyama K, Ishioka N. 2005. Checkpoint and physiological apoptosis in germ cells proceeds normally in spaceflown Caenorhabditis elegans. Apoptosis 10:949–954.
   PubMed Web of Science ®Google Scholar
• Honda Y, Higashibata A, Matsunaga Y, Yonezawa Y, Kawano T, Higashitani A, Kuriyama K, Shimazu T, Tanaka M, Szewczyk NJ, Ishioka N, Honda S. 2012. Genes down-regulated in spaceflight are involved in the control of longevity in Caenorhabditis elegans. Sci Rep 2:487.
   Google Scholar
• Horneck G. 1999. Impact of microgravity on radiobiological processes and efficiency of DNA repair. Mutat Res 430:221–228.
   PubMed Web of Science ®Google Scholar
• Horneck G, Klaus DM, Mancinelli RL. 2010. Space microbiology. Microbiol Mol Biol Rev 74:121–156.
   PubMed Web of Science ®Google Scholar
• Hu PJ. 2007. Dauer. WormBook: The online review of C. elegans biology. doi:10.1895/wormbook.1.144.1. Available from: http://www.ncbi.nlm.nih.gov/books/NBK116082/
   Google Scholar
• Jen KY, Cheung VG. 2003. Transcriptional response of lymphoblastoid cells to ionizing radiation. Genome Res 13:2092–2100.
   PubMed Web of Science ®Google Scholar
• Jeong PY, Na K, Jeong MJ, Chitwood D, Shim YH, Paik YK. 2009. Proteomic analysis of Caenorhabditis elegans. Methods Mol Biol 519:145–169.
   Google Scholar
• Kato M, Paranjape T, Muller RU, Nallur S, Gillespie E, Keane K, Esquela-Kerscher A, Weidhaas JB, Slack FJ. 2009. The mir-34 microRNA is required for the DNA damage response in vivo in C. elegans and in vitro in human breast cancer cells. Oncogene 28:2419–2424.
   PubMed Web of Science ®Google Scholar
• Kobayashi Y, Narumi I, Satoh K, Funayama T, Kikuchi M, Kitayama S, Watanabe H. 2004. Radiation response mechanisms of the extremely radioresistant bacterium Deinococcus radiodurans. Biol Sci Space 18:134–135.
   PubMedGoogle Scholar
• Kobayashi Y, Watanabe H, Kikuchi M, Narumi I. 2000. Effect of the space environment on the induction of DNA-repair related proteins and recovery from radiation damage. Adv Space Res 25:2103–2106.
   PubMed Web of Science ®Google Scholar
• Kumari R, Singh KP, Dumond JW Jr. 2009. Simulated microgravity decreases DNA repair capacity and induces DNA damage in human lymphocytes. J Cell Biochem 107:723–731.
   PubMed Web of Science ®Google Scholar
• Lemmens BB, Tijsterman M. 2011. DNA double-strand break repair in Caenorhabditis elegans. Chromosoma 120:1–21.
   PubMed Web of Science ®Google Scholar
• Lettre G, Hengartner MO. 2006. Developmental apoptosis in C. elegans: A complex CEDnario. Nat Rev Mol Cell Biol 7:97–108.
   Google Scholar
• Lim LP, Lau NC, Weinstein EG, Abdelhakim A, Yekta S, Rhoades MW, Burge CB, Bartel DP. 2003. The microRNAs of Caenorhabditis elegans. Genes Dev 17:991–1008.
   PubMed Web of Science ®Google Scholar
• Lin YX, Yu F, Gao N, Sheng JP, Qiu JZ, Hu BC. 2011. microRNA-143 protects cells from DNA damage-induced killing by downregulating FHIT expression. Cancer Biother Radio 26:365–372.
   PubMed Web of Science ®Google Scholar
• Lord CE, Gunawardena AH. 2012. Programmed cell death in C. elegans, mammals and plants. Eur J Cell Biol 91:603–613.
   Google Scholar
• Maalouf M, Durante M, Foray N. 2011. Biological effects of space radiation on human cells: history, advances and outcomes. J Radiat Res 52:126–146.
   PubMed Web of Science ®Google Scholar
• Mangala LS, Zhang Y, He Z, Emami K, Ramesh GT, Story M, Rohde LH, Wu H. 2011. Effects of simulated microgravity on expression profile of microRNA in human lymphoblastoid cells. J Biol Chem 286:32483–32490.
   PubMed Web of Science ®Google Scholar
• Manti L. 2006. Does reduced gravity alter cellular response to ionizing radiation? Radiat Environ Biophys 45:1–8.
   PubMed Web of Science ®Google Scholar
• Mao XW, Pecaut MJ, Stodieck LS, Ferguson VL, Bateman TA, Bouxsein ML, Gridley DS. 2014. Biological and metabolic response in STS-135 space-flown mouse skin. Free Radic Res 48:890–897.
   PubMed Web of Science ®Google Scholar
• Mognato M, Celotti L. 2005. Modeled microgravity affects cell survival and HPRT mutant frequency, but not the expression of DNA repair genes in human lymphocytes irradiated with ionising radiation. Mutat Res 578:417–429.
   PubMed Web of Science ®Google Scholar
• Morey-Holton ER, Hill EL, Souza KA. 2007. Animals and spaceflight: From survival to understanding. J Musculoskelet Neuronal Interact 7:17–25.
   PubMedGoogle Scholar
• Morrison DR. 1994. Cellular changes in microgravity and the design of space radiation experiments. Adv Space Res 14:1005–1019.
   PubMed Web of Science ®Google Scholar
• Murphy JT, Bruinsma JJ, Schneider DL, Collier S, Guthrie J, Chinwalla A, Robertson JD, Mardis ER, Kornfeld K. 2011. Histidine protects against zinc and nickel toxicity in Caenorhabditis elegans. PLoS Genet 7:e1002013.
   PubMed Web of Science ®Google Scholar
• Ng EKO, Li R, Shin VY, Siu JM, Ma ESK, Kwong A. 2014. MicroRNA-143 is downregulated in breast cancer and regulates DNA methyltransferases 3A in breast cancer cells. Tumor Biol 35:2591–2598.
   PubMed Web of Science ®Google Scholar
• O’Neil N, Rose A. 2006. DNA repair. WormBook: The online review of C. elegans biology. doi/10.1895/wormbook.1.54.1. Available from: http://www.ncbi.nlm.nih.gov/books/NBK19702/
   Google Scholar
• Oczypok EA, Etheridge T, Freeman J, Stodieck L, Johnsen R, Baillie D, Szewczyk NJ. 2012. Remote automated multi-generational growth and observation of an animal in low Earth orbit. J R Soc Interface 9:596–599.
   PubMed Web of Science ®Google Scholar
• Ohnishi T, Takahashi A, Ohnishi K. 2002. Studies about space radiation promote new fields in radiation biology. J Radiat Res 43:S7–12.
   Web of Science ®Google Scholar
• Pagliuca A, Valvo C, Fabrizi E, di Martino S, Biffoni M, Runci D, Forte S, De Maria R, Ricci-Vitiani L. 2013. Analysis of the combined action of miR-143 and miR-145 on oncogenic pathways in colorectal cancer cells reveals a coordinate program of gene repression. Oncogene 32:4806–4813.
   PubMed Web of Science ®Google Scholar
• Perrin AJ, Gunda M, Yu B, Yen K, Ito S, Forster S, Tissenbaum HA, Derry WB. 2013. Noncanonical control of C. elegans germline apoptosis by the insulin/IGF-1 and Ras/MAPK signaling pathways. Cell Death Differ 20:97–107.
   PubMed Web of Science ®Google Scholar
• Pross HD, Casares A, Kiefer J. 2000. Induction and repair of DNA double-strand breaks under irradiation and microgravity. Radiat Res 153:521–525.
   PubMed Web of Science ®Google Scholar
• Ruzanov P, Riddle DL, Marra MA, McKay SJ, Jones SM. 2007. Genes that may modulate longevity in C. elegans in both dauer larvae and long-lived daf-2 adults. Exp Gerontol 42:825–839.
   PubMed Web of Science ®Google Scholar
• Salinas LS, Maldonado E, Navarro RE. 2006. Stress-induced germ cell apoptosis by a p53 independent pathway in Caenorhabditis elegans. Cell Death Differ 13:2129–2139.
   PubMed Web of Science ®Google Scholar
• Schenten V, Gueguinou N, Baatout S, Frippiat JP. 2013. Modulation of Pleurodeles waltl DNA polymerase mu expression by extreme conditions encountered during spaceflight. PLoS One 8:e69647.
   PubMedGoogle Scholar
• Selch F, Higashibata A, Imamizo-Sato M, Higashitani A, Ishioka N, Szewczyk NJ, Conley CA. 2008. Genomic response of the nematode Caenorhabditis elegans to spaceflight. Adv Space Res 41:807–815.
   PubMed Web of Science ®Google Scholar
• Shtifman A, Pezone MJ, Sasi SP, Agarwal A, Gee H, Song J, Perepletchikov A, Yan X, Kishore R, Goukassian DA. 2013. Divergent modification of low-dose 56Fe-particle and proton radiation on skeletal muscle. Radiat Res 180:455–464.
   PubMed Web of Science ®Google Scholar
• Stiernagle T. 2006. Maintenance of C. elegans. WormBook: The online review of C. elegans biology. doi/10.1895/wormbook.1.101.1. Available from: http://www.ncbi.nlm.nih.gov/books/NBK19649/
   Google Scholar
• Szewczyk NJ, Tillman J, Conley CA, Granger L, Segalat L, Higashitani A, Honda S, Honda Y, Kagawa H, Adachi R, Higashibata A, Fujimoto N, Kuriyama K, Ishioka N, Fukui K, Baillie D, Rose A, Gasset G, Eche B, Chaput D, Viso M. 2008. Description of International Caenorhabditis elegans Experiment first flight (ICE-FIRST). Adv Space Res 42: 1072–1079.
   PubMed Web of Science ®Google Scholar
• Takahashi A, Suzuki H, Omori K, Seki M, Hashizume T, Shimazu T, Ishioka N, Ohnishi T. 2012. Expression of p53-regulated proteins in human cultured lymphoblastoid TSCE5 and WTK1 cell lines during spaceflight. J Radiat Res 53:168–175.
   Web of Science ®Google Scholar
• Tauber S, Hauschild S, Crescio C, Secchi C, Paulsen K, Pantaleo A, Saba A, Buttron I, Thiel CS, Cogoli A, Pippia P, Ullrich O. 2013. Signal transduction in primary human T lymphocytes in altered gravity – results of the MASER-12 suborbital space flight mission. Cell Commun Signal 11:32.
   PubMedGoogle Scholar
• Trivigno D, Bornes L, Huber SM, Rudner J. 2013. Regulation of protein translation initiation in response to ionizing radiation. Radiat Oncol 8:35.
   PubMed Web of Science ®Google Scholar
• Versari S, Longinotti G, Barenghi L, Maier JA, Bradamante S. 2013. The challenging environment on board the International Space Station affects endothelial cell function by triggering oxidative stress through thioredoxin interacting protein overexpression: The ESA-SPHINX experiment. FASEB J 27:4466–4475.
   PubMed Web of Science ®Google Scholar
• Wang J, Kim SK. 2003. Global analysis of dauer gene expression in Caenorhabditis elegans. Development 130:1621–1634.
   PubMed Web of Science ®Google Scholar
• Wang Y, An L, Jiang Y, Hang H. 2011. Effects of simulated microgravity on embryonic stem cells. PLoS One 6:e29214.
   PubMedGoogle Scholar
• Wouters MD, van Gent DC, Hoeijmakers JH, Pothof J. 2011. MicroRNAs, the DNA damage response and cancer. Mutat Res 717:54–66.
   PubMed Web of Science ®Google Scholar
• Wu XL, Cheng B, Li PY, Huang HJ, Zhao Q, Dan ZL, Tian DA, Zhang P. 2013. MicroRNA-143 suppresses gastric cancer cell growth and induces apoptosis by targeting COX-2. World J Gastroenterol 19:7758–7765.
   PubMed Web of Science ®Google Scholar
• Xu D, Gao Y, Huang L, Sun Y. 2014. Changes in miRNA expression profile of space-flown Caenorhabditis elegans during Shenzhou-8 mission. Life Sci Space Res 1:44–52.
   Google Scholar
• Yatagai F, Honma M, Takahashi A, Omori K, Suzuki H, Shimazu T, Seki M, Hashizume T, Ukai A, Sugasawa K, Abe T, Dohmae N, Enomoto S, Ohnishi T, Gordon A, Ishioka N. 2011. Frozen human cells can record radiation damage accumulated during space flight: Mutation induction and radioadaptation. Radiat Environ Biophys 50:125–134.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Lai K, Cheung I, Youds J, Tarailo M, Tarailo S, Rose A. 2006. A mutational analysis of Caenorhabditis elegans in space. Mutat Res 601:19–29.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Johnsen R, Bailie D, Rose A. 2005. Worm in space? A model biological dosimeter. Gravit Space Biol Bull 18:11–16.
   PubMedGoogle Scholar
• Zhu F, Liu JL, Li JP, Xiao F, Zhang ZX, Zhang L. 2013. MicroRNA-124 (miR-124) regulates Ku70 expression and is correlated with neuronal death induced by ischemia/reperfusion. J Mol Neurosci 52:148–155.
   PubMed Web of Science ®Google Scholar