56 Fe particle exposure results in a long-lasting increase in a cellular index of genomic instability and transiently suppresses adult hippocampal neurogenesis in vivo

Life Sciences in Space Research

Volumn 2, Issue , 2014, Pages 70-79

  Decarolis, Nathan A ^a   Rivera, Phillip D ^a   Ahn, Francisca ^b   Amaral, Wellington Z ^a   Leblanc, Junie A ^a   Malhotra, Shveta ^a   Shih, Hung Ying ^b   Petrik, David ^a   Melvin, Neal R ^a   Chen, Benjamin P C ^b   Eisch, Amelia J ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Adult neurogenesis; BrdU; Galactic cosmic radiation; Recovery; Subgranular zone; Transgenic mice

Indexed keywords

IRON; NESTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIVISION; CELL MATURATION; CELL PROLIFERATION; COGNITION; CONTROLLED STUDY; COSMIC RADIATION; DENTATE GYRUS; FEMALE; GENOMIC INSTABILITY; GLIA CELL; HIPPOCAMPUS; IN VIVO STUDY; LEARNING; MALE; MEMORY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; RADIATION EXPOSURE; RADIATION HAZARD; RADIATION INJURY; ADULT; ANIMAL MODEL; BRAIN INJURY; COSMONAUT; HEALTH HAZARD; IMMUNOHISTOCHEMISTRY; PROTEIN EXPRESSION; RADIATION DOSE DISTRIBUTION; WHOLE BODY RADIATION;

EID: 84904859894     PISSN: 22145524     EISSN: 22145532     Source Type: Journal    
DOI: 10.1016/j.lssr.2014.06.004     Document Type: Article

References (50)

1. J.L. Ables et al. Notch1 is required for maintenance of the reservoir of adult hippocampal stem cells J. Neurosci. 30 31 2010 10484 10492
2. A. Asaithamby, and D.J. Chen Mechanism of cluster DNA damage repair in response to high-atomic number and energy particles radiation Mutat. Res. 711 1-2 2011 87 99
3. J. Bartkova et al. Replication stress and oxidative damage contribute to aberrant constitutive activation of DNA damage signalling in human gliomas Oncogene 29 36 2010 5095 5102
4. J. Battiste et al. Ascl1 defines sequentially generated lineage-restricted neuronal and oligodendrocyte precursor cells in the spinal cord Development 134 2 2007 285 293
5. 56 Fe- particle radiation lead to a persistent reduction in the spatial learning ability of rats Radiat. Res. 177 2 2012 146 151
6. 56 Fe particles mimics that seen during aging in rats Exp. Gerontol. 40 3 2005 249 254
7. J.D. Cherry et al. Galactic cosmic radiation leads to cognitive impairment and increased abeta plaque accumulation in a mouse model of Alzheimer's disease PLoS ONE 7 12 2012 e53275
8. C. Contet et al. μ-Opioid receptors mediate the effects of chronic ethanol binge drinking on the hippocampal neurogenic niche Addict. Biol 2014 10.1111/adb.12040
9. F.A. Cucinotta Space radiation risks for astronauts on multiple international space station missions PLoS ONE 9 4 2014 e96099
10. F.A. Cucinotta, H. Wang, and J.L. Huff Risk of acute or late central nervous system effects from radiation exposure J.C. McPhee, J.B. Charles, Human Health and Performance Risks of Space Exploration Missions: Evidence Reviewed by the NASA Human Research Program 2009 National Aeronautics and Space Administration, Lyndon B. Johnson Space Center Houston, TX 191 212 Chapter 6
11. N.A. DeCarolis et al. In vivo contribution of nestin- and GLAST-lineage cells to adult hippocampal neurogenesis Hippocampus 23 8 2013 708 719
12. F. Doetsch, J.M. Garcia-Verdugo, and A. Alvarez-Buylla Regeneration of a germinal layer in the adult mammalian brain Proc. Natl. Acad. Sci. USA 96 20 1999 11619 11624
13. A.J. Eisch Adult neurogenesis: implications for psychiatry Prog. Brain Res. 138 2002 315 342
14. J.M. Encinas et al. Quiescent adult neural stem cells are exceptionally sensitive to cosmic radiation Exp. Neurol. 210 1 2008 274 279
15. J.M. Encinas et al. Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus Cell Stem Cell 8 5 2011 566 579
16. K. Flurkey, J.M. Currie, and D.E. Harrison Mouse models in aging research J.G. Fox, The Mouse in Biomedical Research: Normative Biology, Husbandry, and Models 2007 Elsevier
17. D. Grahn HZE Particle Effects in Manned Spaceflight 1973 National Academy of Sciences Washington, DC
18. T. Groesser et al. Persistence of gamma-H2AX and 53BP1 foci in proliferating and non-proliferating human mammary epithelial cells after exposure to gamma-rays or iron ions Int. J. Radiat. Biol. 87 7 2011 696 710
19. G.C. Harburg et al. Knockout of the mu opioid receptor enhances the survival of adult-generated hippocampal granule cell neurons Neuroscience 144 1 2007 77 87
20. D.M. Hassler et al. Mars' surface radiation environment measured with the Mars Science Laboratory's Curiosity rover Science 343 6169 2014 1244797
21. T. Ikrar et al. Adult neurogenesis modifies excitability of the dentate gyrus Front Neural Circuits 7 2013 204
22. S. Jinno Topographic differences in adult neurogenesis in the mouse hippocampus: a stereology-based study using endogenous markers Hippocampus 21 5 2011 467 480
23. G. Kempermann Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice Development 130 2 2003 391 399
24. D.C. Lagace et al. Dynamic contribution of nestin-expressing stem cells to adult neurogenesis J. Neurosci. 27 46 2007 12623 12629
25. D.C. Lagace et al. Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance Proc. Natl. Acad. Sci. USA 107 2010 4436 4441
26. C.L. Limoli et al. Redox changes induced in hippocampal precursor cells by heavy ion irradiation Radiat. Environ. Biophys. 46 2 2007 167 172
27. J.L. Liu et al. Tamoxifen alleviates irradiation-induced brain injury by attenuating microglial inflammatory response in vitro and in vivo Brain Res. 1316 2010 101 111
28. K. Manda, M. Ueno, and K. Anzai Space radiation-induced inhibition of neurogenesis in the hippocampal dentate gyrus and memory impairment in mice: ameliorative potential of the melatonin metabolite, AFMK J. Pineal Res. 45 4 2008 430 438
29. C.D. Mandyam, G.C. Harburg, and A.J. Eisch Determination of key aspects of precursor cell proliferation, cell cycle length and kinetics in the adult mouse subgranular zone Neuroscience 146 1 2007 108 122
30. C.D. Mandyam, R.D. Norris, and A.J. Eisch Chronic morphine induces premature mitosis of proliferating cells in the adult mouse subgranular zone J. Neurosci. Res. 76 6 2004 783 794
31. N.R. Melvin, D. Poda, and R.J. Sutherland A simple and efficient alternative to implementing systematic random sampling in stereological designs without a motorized microscope stage J. Microsc. 228 Pt. 1 2007 103 106
32. G.L. Ming, and H. Song Adult neurogenesis in the mammalian central nervous system Annu. Rev. Neurosci. 28 2005 223 250
33. P.R. Mouton Principles and Practices of Unbiased Stereology: An Introduction for Bioscientists 2002 The Johns Hopkins University Press Baltimore, MD
34. Y. Naruke et al. Genomic instability in the epidermis induced by atomic bomb (A-bomb) radiation: a long-lasting health effect in A-bomb survivors Cancer 115 16 2009 3782 3790
35. D. Petrik et al. Functional and mechanistic exploration of an adult neurogenesis-promoting small molecule FASEB J. 26 8 2012 3148 3162
36. D. Petrik, D.C. Lagace, and A.J. Eisch The neurogenesis hypothesis of affective and anxiety disorders: are we mistaking the scaffolding for the building? Neuropharmacology 62 1 2012 21 34
37. 56 Fe HZE-particle radiation both result in similar long-term deficits in adult hippocampal neurogenesis Radiat. Res. 180 6 2013 658 667
38. 56 Fe-particle irradiation in a dose-dependent manner Radiat. Res. 162 4 2004 442 446
39. R. Rola et al. High-LET radiation induces inflammation and persistent changes in markers of hippocampal neurogenesis Radiat. Res. 164 4 Pt. 2 2005 556 560
40. 56 Fe particles Radiat. Res. 169 6 2008 626 632
41. 56 Fe irradiation Hippocampus 22 3 2012 544 554
42. A. Sahay et al. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation Nature 472 7344 2011 466 470
43. B. Shukitt-Hale, G. Casadesus, J.J. McEwen, B.M. Rabin, and J.A. Joseph Spatial learning and memory deficits induced by exposure to iron-56-particle radiation Radiat. Res. 154 1 2000 28 33
44. 56 Fe radiation exposure Adv. Space Res. 31 1 2003 119 126
45. J.S. Snyder et al. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour Nature 476 7361 2011 458 461
46. 56 Fe irradiation on contextual fear conditioning in C57BL/6J mice Hippocampus 20 1 2010 19 23
47. A.K. Walker et al. The P7C3 class of neuroprotective compounds exerts antidepressant efficacy in mice by increasing hippocampal neurogenesis Mol. Psychiatry 2014 10.1038/mp.2014.34
48. M. Yamaguchi et al. Visualization of neurogenesis in the central nervous system using nestin promoter-GFP transgenic mice NeuroReport 11 9 2000 1991 1996
49. C. Zeitlin et al. Measurements of energetic particle radiation in transit to mars on the mars science laboratory Science 340 2013 1080 1084
50. M. Zimmermann et al. 53BP1 regulates DSB repair using Rif1 to control 5′ end resection Science 339 6120 2013 700 704