Low dose effects of ionizing radiation on normal tissue stem cells

Mutation Research - Reviews in Mutation Research

Volumn 761, Issue , 2014, Pages 6-14

  Manda, Katrin ^a   Kavanagh, Joy N ^b   Buttler, Dajana ^a   Prise, Kevin M ^b   Hildebrandt, Guido ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Carcinogenesis; Irradiation; Low dose; Normal stem cells

Indexed keywords

CANCER STEM CELL; CELL PROLIFERATION; HUMAN; IONIZING RADIATION; NONHUMAN; PRIORITY JOURNAL; RADIATION CARCINOGENESIS; RADIATION DOSE; RADIATION EXPOSURE; RADIATION RESPONSE; RADIOBIOLOGY; RADIOSENSITIVITY; REVIEW; STEM CELL;

EID: 84921844288     PISSN: 13835742     EISSN: 13882139     Source Type: Journal    
DOI: 10.1016/j.mrrev.2014.02.003     Document Type: Review

References (121)

1. R.J.M. Fry, J.B. Storer, External radiation carcinogenesis. (Lett & JT, eds), New York, 1987, pp. 31-90.
2. Ozasa K., Shimizu Y., Suyama A., Kasagi F., Soda M., Grant E.J., Sakata R., Sugiyama H., Kodama K. Studies of the mortality of atomic bomb survivors, Report 14, 1950-2003: an overview of cancer and noncancer diseases. Radiat. Res. 2012, 177:229-243.
3. Shah D.J., Sachs R.K., Wilson D.J. Radiation-induced cancer: a modern view. Br. J. Radiol. 2012, 85:e1166-e1173.
4. Barcellos-Hoff M.H., Nguyen D.H. Radiation carcinogenesis in context: how do irradiated tissues become tumors?. Health Phys. 2009, 97:446-457.
5. Kadhim M., Salomaa S., Wright E., Hildebrandt G., Belyakov O.V., Prise K.M., Little M.P. Non-targeted effects of ionizing radiation-Implications for low dose risk. Mutat. Res. 2012, 752(2):84-98.
6. Nagasawa H., Little J.B. Induction of sister chromatid exchanges by extremely low doses of alpha-particles. Cancer Res. 1992, 52:6394-6396.
7. Kadhim M.A., Moore S.R., Goodwin E.H. Interrelationships amongst radiation-induced genomic instability, bystander effects, and the adaptive response. Mutat. Res. 2004, 568:21-32.
8. Morgan W.F. Non-targeted and delayed effects of exposure to ionizing radiation: I. Radiation-induced genomic instability and bystander effects in vitro. Radiat. Res. 2003, 159:567-580.
9. Lyng F.M., Seymour C.B., Mothersill C. Production of a signal by irradiated cells which leads to a response in unirradiated cells characteristic of initiation of apoptosis. Br. J. Cancer 2000, 83:1223-1230.
10. Sokolov M.V., Smilenov L.B., Hall E.J., Panyutin I.G., Bonner W.M., Sedelnikova O.A. Ionizing radiation induces DNA double-strand breaks in bystander primary human fibroblasts. Oncogene 2005, 24:7257-7265.
11. Yang H., Asaad N., Held K.D. Medium-mediated intercellular communication is involved in bystander responses of X-ray-irradiated normal human fibroblasts. Oncogene 2005, 24:2096-2103.
12. Shao C., Folkard M., Prise K.M. Role of TGF-beta1 and nitric oxide in the bystander response of irradiated glioma cells. Oncogene 2008, 27:434-440.
13. Belyakov O.V., Mitchell S.A., Parikh D., Randers-Pehrson G., Marino S.A., Amundson S.A., Geard C.R., Brenner D.J. Biological effects in unirradiated human tissue induced by radiation damage up to 1mm away. Proc. Natl. Acad. Sci. U.S.A 2005, 102:14203-14208.
14. Shao C., Furusawa Y., Aoki M., Matsumoto H., Ando K. Nitric oxide-mediated bystander effect induced by heavy-ions in human salivary gland tumour cells. Int. J. Radiat. Biol. 2002, 78:837-844.
15. Sawant S.G., Zheng W., Hopkins K.M., Randers-Pehrson G., Lieberman H.B., Hall E.J. The radiation-induced bystander effect for clonogenic survival. Radiat. Res. 2002, 157:361-364.
16. Schettino G., Folkard M., Prise K.M., Vojnovic B., Held K.D., Michael B.D. Low-dose studies of bystander cell killing with targeted soft X rays. Radiat. Res. 2003, 160:505-511.
17. Seymour C.B., Mothersill C. Relative contribution of bystander and targeted cell killing to the low-dose region of the radiation dose-response curve. Radiat. Res. 2000, 153:508-511.
18. Moore S.R., Marsden S., Macdonald D., Mitchell S., Folkard M., Michael B., Goodhead D.T., Prise K.M., Kadhim M.A. Genomic instability in human lymphocytes irradiated with individual charged particles: involvement of tumor necrosis factor alpha in irradiated cells but not bystander cells. Radiat. Res. 2005, 163:183-190.
19. Hall E.J., Hei T.K. Genomic instability and bystander effects induced by high-LET radiation. Oncogene 2003, 22:7034-7042.
20. Shuryak I., Brenner D.J., Ullrich R.L. Radiation-induced carcinogenesis: mechanistically based differences between gamma-rays and neutrons, and interactions with DMBA. PLoS. One 2011, 6:e28559.
21. Kundrát P., Friedland W. Non-linear response of cells to signals leads to revised characteristics of bystander effects inferred from their modelling. Int. J. Radiat. Biol. 2012, 10:743-750.
22. McMahon S.J., Butterworth K.T., Trainor C., McGarry C.K., O'Sullivan J.M., Schettino G., Hounsell A.R., Prise K.M. A kinetic-based model of radiation-induced intercellular signalling. PLoS One 2013, 8(1):e54526.
23. Butterworth K.T., McMahon S.J., Hounsell A.R., O'Sullivan J.M., Prise K.M. Bystander signalling: exploring clinical relevance through new approaches and new models. Clin. Oncol. (R Coll. Radiol.) 2013, 25(10):586-592.
24. Eidemüller M., Holmberg E., Jacob P., Lundell M., Karlsson P. Breast cancer risk after radiation treatment at infancy: potential consequences of radiation-induced genomic instability. Radiat. Prot. Dosimetry 2011, 143(2-4):375-379.
25. Jacob P., Meckbach R., Kaiser J.C., Sokolnikov M. Possible expressions of radiation-induced genomic instability, bystander effects or low-dose hypersensitivity in cancer epidemiology. Mutat. Res. 2010, 687(1-2):34-39.
26. Eidemüller M., Holmberg E., Jacob P., Lundell M., Karlsson P. Breast cancer risk among Swedish hemangioma patients and possible consequences of radiation-induced genomic instability. Mutat. Res. 2009, 669(1-2):48-55.
27. Prise K.M., Saran A. Stem cell effects in radiation risk. Stem Cells 2011, 29:1315-1321.
28. Fossett N. Signal transduction pathways, intrinsic regulators, and the control of cell fate choice. Biochim. Biophys. Acta 2013, 1830(2):2375-2384.
29. Pimanda J.E., Ottersbach K., Knezevic K., Kinston S., Chan W.Y., Wilson N.K., Landry J.R., Wood A.D., Kolb-Kokocinski A., Green A.R., Tannahill D., Lacaud G., Kouskoff V., Göttgens B. Gata2, Fli1, and Scl form a recursively wired gene-regulatory circuit during early hematopoietic development. Proc. Natl. Acad. Sci. U.S.A. 2007, 104(45):17692-17697.
30. Trompouki E., Bowman T.V., Lawton L.N., Fan Z.P., Wu D.C., DiBiase A., Martin C.S., Cech J.N., Sessa A.K., Leblanc J.L., Li P., Durand E.M., Mosimann C., Heffner G.C., Daley G.Q., Paulson R.F., Young R.A., Zon L.I. Lineage regulators direct BMP and Wnt pathways to cell-specific programs during differentiation and regeneration. Cell 2011, 147(3):577-589.
31. Massagué J. TGFβ signalling in context. Nat. Rev. Mol. Cell. Biol. 2012, 13(10):616-630.
32. Massagué J. TGFbeta in Cancer. Cell 2008, 134(2):215-230.
33. Hu X.L., Wang Y., Shen Q. Epigenetic control on cell fate choice in neural stem cells. Protein Cell. 2012, 3(4):278-290.
34. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
35. Upton A.C. Historical perspectives on radiation carcinogenesis. Radiation Carcinogenesis 1986, 1-10. Elsevier, New York. A.C. Upton, R.E. Albert, F.J. Burns, R.E. Shore (Eds.).
36. Nguyen L.V., Vanner R., Dirks P., Eaves C.J. Cancer stem cells: an evolving concept. Nat. Rev. Cancer 2012, 12:133-143.
37. Wicha M.S., Liu S., Dontu G. Cancer stem cells: an old idea--a paradigm shift. Cancer Res. 2006, 66:1883-1890.
38. Lapidot T., Sirard C., Vormoor J., Murdoch B., Hoang T., Caceres-Cortes J., Minden M., Paterson B., Caligiuri M.A., Dick J.E. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994, 367:645-648.
39. Sell S. On the stem cell origin of cancer. Am. J. Pathol. 2010, 176:2584-3494.
40. Park C.Y., Tseng D., Weissman I.L. Cancer stem cell-directed therapies: recent data from the laboratory and clinic. Mol. Ther. 2009, 17:219-230.
41. Lobo N.A., Shimono Y., Qian D., Clarke M.F. The biology of cancer stem cells. Annu. Rev. Cell Dev. Biol. 2007, 23:675-699.
42. Park C.H., Bergsagel D.E., McCulloch E.A. Mouse myeloma tumor stem cells: a primary cell culture assay. J. Natl. Cancer Inst. 1971, 46:411-422.
43. Bruce W.R., van der Gaag H. A quantitative assay for the number of murine lymphoma cells capable of proliferation in vivo. Nature 1963, 199:79-80.
44. Hamburger A.W., Salmon S.E. Primary bioassay of human tumor stem cells. Science 1977, 197:461-463.
45. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:3983-3988.
46. O'Brien C.A., Pollett A., Gallinger S., Dick J.E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007, 445:106-110.
47. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., Henkelman R.M., Cusimano M.D., Dirks P.B. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
48. Cheng L., Ramesh A.V., Flesken-Nikitin A., Choi J., Nikitin A.Y. Mouse models for cancer stem cell research. Toxicol. Pathol. 2010, 38:62-71.
49. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
50. Pardal R., Clarke M.F., Morrison S.J. Applying the principles of stem-cell biology to cancer. Nat. Rev. Cancer 2003, 3:895-902.
51. Morrison S.J., Kimble J. Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 2006, 441:1068-1074.
52. Dick J.E. Stem cell concepts renew cancer research. Blood 2008, 112:4793-4807.
53. Park S.Y., Lee H.E., Li H., Shipitsin M., Gelman R., Polyak K. Heterogeneity for stem cell-related markers according to tumor subtype and histologic stage in breast cancer. Clin. Cancer Res. 2010, 16:876-887.
54. Visvader J.E., Lindeman G.J. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nature Rev. Cancer 2008, 8:755-768.
55. Kelly P.N., Dakic A., Adams J.M., Nutt S.L., Strasser A. Tumor growth need not be driven by rare cancer stem cells. Science 2007, 317. 337-337.
56. Schwitalla S., Fingerle A.A., Cammareri P., Nebelsiek T., Göktuna S.I., Ziegler P.K., Canli O., Heijmans J., Huels D.J., Moreaux G., Rupec R.A., Gerhard M., Schmid R., Barker N., Clevers H., Lang R., Neumann J., Kirchner T., Taketo M.M., van den Brink G.R., Sansom O.J., Arkan M.C., Greten F.R. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 2013, 152(1-2):25-38.
57. Leder K., Holland E.C., Michor F. The Therapeutic Implications of Plasticity of the Cancer Stem Cell Phenotype. PLoS ONE 2010, 5(12):e14366.
58. Charles N., Ozawa T., Squatrito M., Bleau A.M., Brennan C.W., Hambardzumyan D., Holland E.C. Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells. Cell Stem Cell 2010, 6:141-152.
59. Sharif A., Legendre P., Prévot V., Allet C., Romao L., Studler J.M., Chneiweiss H., Junier M.P. Transforming growth factor alpha promotes sequential conversion of mature astrocytes into neural progenitors and stem cells. Oncogene 2007, 26:2695-2706.
60. Vermeulen L., De Sousa E., Melo F., Van Der Heijden M., Cameron K., de Jong J.H., Borovski T., Tuynman J.B., Todaro M., Merz C., Rodermond H., Sprick M.R., Kemper K., Richel D.J., Stassi G., Medema J.P. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat. Cell Biol. 2010, 12:468-476.
61. Das B., Tsuchida R., Malkin D., Koren G., Baruchel S., Yeger H. Hypoxia enhances tumor stemness by increasing the invasive and tumorigenic side population fraction. Stem Cells 2008, 26:1818-1830.
62. Dontu G., Al-Hajj M., Abdallah W.M., Clarke M.F., Wicha M.S. Stem cells in normal breast development and breast cancer. Cell Prolif. 2003, 36(Suppl. 1):59-72.
63. Krantz S.B., Shields M.A., Dangi-Garimella S., Munshi H.G., Bentrem D.J. Contribution of epithelial-to-mesenchymal transition and cancer stem cells to pancreatic cancer progression. J. Surg. Res. 2012, 173:105-112.
64. May C.D., Sphyris N., Evans K.W., Werden S.J., Guo W., Mani S.A. Epithelial-mesenchymal transition and cancer stem cells: a dangerously dynamic duo in breast cancer progression. Breast Cancer Res. 2011, 13:202.
65. Wang Y., Liu L., Pazhanisamy S.K., Li H., Meng A., Zhou D. Total body irradiation causes residual bone marrow injury by induction of persistent oxidative stress in murine hematopoietic stem cells. Free Radic. Biol. Med. 2010, 48:348-356.
66. Wang Y., Liu L., Zhou D. Inhibition of p38 MAPK attenuates ionizing radiation-induced hematopoietic cell senescence and residual bone marrow injury. Radiat. Res. 2011, 176:743-752.
67. Cmielova J., Havelek R., Soukup T., Jiroutova A., Visek B., Suchanek J., Vavrova J., Mokry J., Muthna D., Bruckova L., Filip S., English D., Rezacova M. Gamma radiation induces senescence in human adult mesenchymal stem cells from bone marrow and periodontal ligaments. Int. J. Radiat. Biol. 2012, 88:393-404.
68. Filion T.M., Qiao M., Ghule P.N., Mandeville M., van Wijnen A.J., Stein J.L., Lian J.B., Altieri D.C., Stein G.S. Survival responses of human embryonic stem cells to DNA damage. J. Cell Physiol. 2009, 220:586-592.
69. Hong Y., Stambrook P.J. Restoration of an absent G1 arrest and protection from apoptosis in embryonic stem cells after ionizing radiation. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:14443-14448.
70. Denissova N.G., Tereshchenko I.V., Cui E., Stambrook P.J., Shao C., Tischfield J.A. Ionizing radiation is a potent inducer of mitotic recombination in mouse embryonic stem cells. Mutat. Res. 2011, 715:1-6.
71. Momcilovic O., Choi S., Varum S., Bakkenist C., Schatten G., Navara C. Ionizing radiation induces ataxia telangiectasia mutated-dependent checkpoint signaling and G(2) but not G(1) cell cycle arrest in pluripotent human embryonic stem cells. Stem Cells 2009, 27:1822-1835.
72. Sun K.D.N., Huang M., Zhang W.Y., Lee A.S., Li Z., Wang S.X., Wu J.C. Effects of ionizing radiation on self-renewal and pluripotency of human embryonic stem cells. Cancer Res. 2010, 70:5539-5548.
73. Sokolov M.V., Panyutin I.V., Neumann R.D. Unraveling the global microRNAome responses to ionizing radiation in human embryonic stem cells. PLoS One 2012, 7:e31028.
74. Sokolov M.V., Panyutin I.V., Panyutin I.G., Neumann R.D. Dynamics of the transcriptome response of cultured human embryonic stem cells to ionizing radiation exposure. Mutat. Res. 2011, 709-710:40-48.
75. Hayashi N., Monzen S., Ito K., Fujioka T., Nakamura Y., Kashiwakura I. Effects of ionizing radiation on proliferation and differentiation of mouse induced pluripotent stem cells. J. Radiat. Res. 2012, 53:195-201.
76. Monzen S., Tashiro E., Kashiwakura I. Megakaryocytopoiesis and thrombopoiesis in hematopoietic stem cells exposed to ionizing radiation. Radiat. Res. 2011, 176:716-724.
77. Rachidi W., Harfourche G., Lemaitre G., Amiot F., Vaigot P., Martin M.T. Sensing radiosensitivity of human epidermal stem cells. Radiother. Oncol. 2007, 83:267-276.
78. D'Andrea F.P., Horsman M.R., Kassem M., Overgaard J., Safwat A. Tumourigenicity and radiation resistance of mesenchymal stem cells. Acta Oncol. 2012, 51:669-679.
79. Inomata K., Aoto T., Binh N.T., Okamoto N., Tanimura S., Wakayama T., Iseki S., Hara E., Masunaga T., Shimizu H., Nishimura E.K. Genotoxic stress abrogates renewal of melanocyte stem cells by triggering their differentiation. Cell 2009, 137(6):1088-1099.
80. Aoki H., Hara A., Motohashi T. Protective effect of Kit signaling for melanocyte stem cells against radiation-induced genotoxic stress. J. Invest. Dermatol. 2011, 131(9):1906-1915.
81. Hachiva A., Sriwiriyanont P., Kobayashi T., Nagasawa A., Yoshida H., Ohuchi A., Kitahara T., Visscher M.O., Takema Y., Tsuboi R., Boissy R.E. Stem cell factor-KIT signalling plays a pivotal role in regulating pigmentation in mammalian hair. J. Pathol. 2009, 218(1):30-39.
82. H. Aoki, A. Hara, T., Motohashi, T. Kunisada, Keratinocyte stem cells but not melanocyte stem cells are the primary target for radiation-induced hair graying, J. Invest. Dermatol. (2013) doi:10.1038/jid.2013.155.
83. M.V. Sokolov, R.D. Neumann, Human embryonic stem cell responses to ionizing radiation exposures: current state of knowledge and future challenges, Stem Cells Int. (2012) doi:10.1155/2012/579104.
84. Bajinskis A., Lindegren H., Johansson L., Harms-Ringdahl M., Forsby A. Low-dose/dose-rate gamma radiation depresses neural differentiation and alters protein expression profiles in neuroblastoma SH-SY5Y cells and C17.2 neural stem cells. Radiat. Res. 2011, 175:185-192.
85. Liang X., So Y.H., Cui J., Ma K., Xu X., Zhao Y., Cai L., Li W. The low-dose ionizing radiation stimulates cell proliferation via activation of the MAPK/ERK pathway in rat cultured mesenchymal stem cells. J. Radiat. Res. 2011, 52:380-386.
86. Kern P., Keilholz L., Forster C., Seegenschmiedt M.H., Sauer R., Herrmann M. In vitro apoptosis in peripheral blood mononuclear cells induced by low-dose radiotherapy displays a discontinuous dose-dependence. Int. J. Radiat. Biol. 1999, 75:995-1003.
87. Rödel F., Keilholz L., Herrmann M., Sauer R., Hildebrandt G. Radiobiological mechanisms in inflammatory diseases of low-dose radiation therapy. Int. J. Radiat. Biol. 2007, 83:357-366.
88. Zaichkina S.I., Rozanova O.M., Aptikaeva G.F., Achmadieva A.Ch., Klokov D.Y. Low doses of gamma-radiation induce nonlinear dose responses in Mammalian and plant cells. Nonlinearity Biol. Toxicol. Med. 2004, 2:213-221.
89. Guo W.Y., Wang G.J., Wang P., Chen Q., Tan Y., Cai L. Acceleration of diabetic wound healing by low-dose radiation is associated with peripheral mobilization of bone marrow stem cells. Radiat. Res. 2010, 174:467-479.
90. Li W., Wang G., Cui J., Xue L., Cai L. Low-dose radiation (LDR) induces hematopoietic hormesis: LDR-induced mobilization of hematopoietic progenitor cells into peripheral blood circulation. Exp. Hematol. 2004, 32:1088-1096.
91. Jolly D., Meyer J. A brief review of radiation hormesis, Australas. Phys. Eng. Sci. Med. 2009, 32:180-187.
92. Bhattacharjee D., Ito A. Deceleration of carcinogenic potential by adaptation with low dose gamma irradiation. In Vivo 2001, 15:87-92.
93. Mitchel R.E. Low doses of radiation are protective in vitro and in vivo: evolutionary origins. Dose Resp. 2006, 4:5-90.
94. Wei L.C., Ding Y.X., Liu Y.H., Duan L., Bai Y., Shi M., Chen L.W. Low-dose radiation stimulates Wnt/beta-catenin signaling, neural stem cell proliferation and neurogenesis of the mouse hippocampus in vitro and in vivo. Curr. Alzheimer Res. 2012, 9:278-289.
95. Tian J., Zhao W., Tian S., Slater J.M., Deng Z., Gridley D.S. Expression of genes involved in mouse lung cell differentiation/regulation after acute exposure to photons and protons with or without low-dose preirradiation. Radiat. Res. 2011, 176:553-564.
96. Hughes K.R., Gandara R.M., Javkar T., Sablitzky F., Hock H., Potten C.S., Mahida Y.R. Heterogeneity in histone 2B-green fluorescent protein-retaining putative small intestinal stem cells at cell position 4 and their absence in the colon. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 303:G1188-G1201.
97. Harfouche G., Martin M.T. Response of normal stem cells to ionizing radiation: a balance between homeostasis and genomic stability. Mutat. Res. 2010, 704:167-174.
98. Pajonk F., Vlashi E. Characterization of the stem cell niche and its importance in radiobiological response. Semin. Radiat. Oncol. 2013, 23(4):237-241.
99. Khanna K.K., Jackson S.P. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 2001, 27(3):247-254.
100. Nagaria P., Robert C., Rassool F.V. DNA double-strand break response in stem cells: mechanisms to maintain genomic integrity. Biochim. Biophys. Acta 2013, 1830(2):2345-2353.
101. Kavanagh J.N., Redmond K.M., Schettino G., Prise K.M. DNA double strand break repair: a radiation perspective. Antioxid. Redox Signal. 2013, 18(18):2458-2472.
102. Niedernhofer L.J. DNA repair is crucial for maintaining hematopoietic stem cell function. DNA Repair (Amst.) 2008, 7(3):523-529.
103. Tichy E.D., Pillai R., Deng L., Liang L., Tischfield J., Schwemberger S.J., Babcock G.F., Stambrook P.J. Mouse embryonic stem cells, but not somatic cells, predominantly use homologous recombination to repair double-strand DNA breaks. Stem Cells Dev. 2010, 19(11):1699-1711.
104. Serrano L., Liang L., Chang Y., Deng L., Maulion C., Nguyen S., Tischfield J.A. Homologous recombination conserves DNA sequence integrity throughout the cell cycle in embryonic stem cells. Stem Cells Dev. 2011, 20(2):363-374.
105. Krutá M., Bálek L., Hejnová R., Dobšáková Z., Eiselleová L., Matulka K., Bárta T., Fojtík P., Fajkus J., Hampl A., Dvořák P., Rotrekl V. Decrease in abundance of apurinic/apyrimidinic endonuclease causes failure of base excision repair in culture-adapted human embryonic stem cells. Stem Cells 2012, 31(4):693-702.
106. Yang N., Galick H., Wallace S.S. Attempted base excision repair of ionizing radiation damage in human lymphoblastoid cells produces lethal and mutagenic double strand breaks. DNA Repair (Amst.) 2004, 3(10):1323-1334.
107. de Souza-Pinto N.C., Maynard S., Hashiguchi K., Hu J., Muftuoglu M., Bohr V.A. The recombination protein RAD52 cooperates with the excision repair protein OGG1 for the repair of oxidative lesions in mammalian cells. Mol. Cell Biol. 2009, 29(16):4441-4454.
108. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 1998, 273(10):5858-5868.
109. Adams B.R., Golding S.E., Rao R.R., Valerie K. Dynamic dependence on ATR and ATM for double-strand break repair in human embryonic stem cells and neural descendants. PLoS One 2010, 5(4). 10.1371/journal.pone.0010001.
110. Sokolov M.V., Neumann R.D. Radiation-induced bystander effects in cultured human stem cells. PLoS One 2010, 5. doi: 10.1371/journal.pone.0014195.
111. J. Tang, I. Fernandez-Garcia, S. Vijayakumar, H. Martinez-Ruiz, I. Illa- Bochaca, D.H. Nguyen, J.H. Mao, S.V. Costes, M.H. Barcellos-Hoff, Irradiation of juvenile, but not adult, mammary gland increases stem cell self- renewal and estrogen receptor negative tumors, Stem Cells. (2013) doi:10.1002/stem.1533.
112. Sokolov M.V., Panyutin I.V., Onyshchenko M.I., Panyutin I.G., Neumann R.D. Expression of pluripotency-associated genes in the surviving fraction of cultured human embryonic stem cells is not significantly affected by ionizing radiation. Gene 2010, 455:8-15.
113. Becker D., Elsasser T., Tonn T., Seifried E., Durante M., Ritter S., Fournier C. Response of human hematopoietic stem and progenitor cells to energetic carbon ions. Int. J. Radiat. Biol. 2009, 85:1051-1059.
114. Bi X., Feng D., Korczeniewska J., Alper N., Hu G., Barnes B.J. Deletion of Irf5 protects hematopoietic stem cells from DNA damage-induced apoptosis and suppresses (-irradiation-induced thymic lymphomagenesis. Oncogene 2013, 10.1038/onc.2013.295.
115. Kato K., Omori A., Kashiwakura I. Radiosensitivity of human haematopoietic stem/progenitor cells. J. Radiol. Prot. 2013, 33(1):71-80.
116. Furlong H., Mothersill C., Lyng F.M., Howe O. Apoptosis is signalled early by low doses of ionising radiation in a radiation-induced bystander effect. Mutat. Res. 2013, 741-742:35-43.
117. Otsuka K., Hamada N., Magae J., Matsumoto H., Hoshi Y., Iwasaki T. Ionizing radiation leads to the replacement and de novo production of colonic Lgr5(+) stem cells. Radiat. Res. 2013, 179(6):637-646.
118. Tseng B.P., Lan M.L., Tran K.K., Acharya M.M., Giedzinski E., Limoli C.L. Characterizing low dose and dose rate effects in rodent and human neural stem cells exposed to proton and gamma irradiation. Redox Biol. 2013, 1(1):153-162.
119. Tanori M., Pasquali E., Leonardi S., Casciati A., Giardullo P., De Stefano I., Mancuso M., Saran A., Pazzaglia S. Developmental and oncogenic radiation effects on neural stem cells and their differentiating progeny in mouse cerebellum. Stem Cells 2013, 31(11):2506-2516.
120. Acharya M.M., Lan M.L., Kan V.H., Patel N.H., Giedzinski E., Tseng B.P., Limoli C.L. Consequences of ionizing radiation-induced damage in human neural stem cells. Free Radic. Biol. Med. 2010, 49(12):1846-1855.
121. B.P. Tseng, E. Giedzinski, A. Izadi, T. Suarez, M.L. Lan, K.K. Tran, M.M. Acharya, G.A. Nelson, J. Raber, V.K. Parihar, C.L. Limoli, Functional Consequences of Radiation-Induced Oxidative Stress in Cultured Neural Stem Cells and the Brain Exposed to Charged Particle Irradiation, Antioxid. Redox Signal. (2013) [Epub ahead of print] PMID:23802883.