The concept of radiation-enhanced stem cell differentiation

1. Jones DL, Wagers AJ. No place like home: anatomy and function of the stem cell niche. Nat Rev Mol Cell Biol 2008; 9: 11-21.10.1038/nrm231918097443Search in Google Scholar

2. Tropepe V, Turksen K. The ontogeny of somatic stem cells. Stem Cell Rev 2012; 8: 548-50.10.1007/s12015-012-9370-y22529018Search in Google Scholar

3. Moore K A, Lemischka IR. Stem cells and their niches. Science 2006; 311: 1880-5.10.1126/science.111054216574858Search in Google Scholar

4. Turksen K. Adult stem cells and cardiac regeneration. Stem Cell Rev 2013; 9: 537-40.10.1007/s12015-013-9448-123775698Search in Google Scholar

5. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126: 663-76.10.1016/j.cell.2006.07.02416904174Search in Google Scholar

6. Shi Y, Kirwan P, Livesey FJ. Directed differentiation of human pluripotent stem cells to cerebral cortex neurons and neural networks. Nat Protoc 2012; 7: 1836-46.10.1038/nprot.2012.11622976355Search in Google Scholar

7. Lian X, Zhang J, Azarin SM, Zhu K, Hazeltine LB, Bao X, et al. Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/β-catenin signaling under fully defined conditions. Nat Protoc 2013; 8: 162-75.10.1038/nprot.2012.150361296823257984Search in Google Scholar

8. Bratt-Leal AM, Carpenedo RL, McDevitt TC. Engineering the embryoid body microenvironment to direct embryonic stem cell differentiation. Biotechnol Prog 2009; 25: 43-51.10.1002/btpr.139269301419198003Search in Google Scholar

9. Kurosawa H. Methods for inducing embryoid body formation: in vitro differentiation system of embryonic stem cells. J Biosci Bioeng 2007; 103: 389-98.10.1263/jbb.103.38917609152Search in Google Scholar

10. Detante O. Intravenous stem cells after ischemic stroke (ISIS). 2014. Available from: http://clinicaltrials.gov/ct2/show/NCT00875654. Accessed 8 March 2015.Search in Google Scholar

11. Vescovi AL. Human neural stem cell transplantation in amyotrophic lateral sclerosis (ALS) (hNSCALS). 2014. Available from: https://clinicaltrials.gov/ct2/show/NCT01640067. Accessed 8 March 2015.Search in Google Scholar

12. Lamo-Espinosa J, Prosper F, Blanco J. Treatment of knee osteoarthritis by intra-articular injection of bone marrow mesenchymal stem cells. 2014. Available from: https://clinicaltrials.gov/ct2/show/NCT02123368. Accessed 8 March 2015.Search in Google Scholar

13. Isa N. Evidence based radiation oncology with existing technology. Reports Pract Oncol Radiother 2014; 19: 259-66.10.1016/j.rpor.2013.09.002410401925061519Search in Google Scholar

14. Valerie K, Yacoub A, Hagan MP, Curiel DT, Fisher PB, Grant S, et al. Radiation-induced cell signaling: inside-out and outside-in. Mol Cancer Ther 2007; 6: 789-801.10.1158/1535-7163.MCT-06-059617363476Search in Google Scholar

15. Rodemann HP, Blaese MA. Responses of normal cells to ionizing radiation. Semin Radiat Oncol 2007; 17: 81-8.10.1016/j.semradonc.2006.11.00517395038Search in Google Scholar

16. Paulino AC, Constine LS, Rubin P, Williams JP. Normal tissue development, homeostasis, senescence, and the sensitivity to radiation injury across the age spectrum. Semin Radiat Oncol 2010; 20: 12-20.10.1016/j.semradonc.2009.08.00319959027Search in Google Scholar

17. Schwenke K, Peterson HP, von Wangenheim KH, Feinendegen LE. Radiation-enhanced differentiation of erythroid progenitor cells and its relation to reproductive cell death. Int J Radiat Biol 1996; 69: 309-17.10.1080/0955300961458698613680Search in Google Scholar

18. Von Wangenheim KH, Peterson HP, Schwenke K. Review: a major component of radiation action: interference with intracellular control of differentiation. Int J Radiat Biol 1995; 68: 369-88.10.1080/095530095145513217594962Search in Google Scholar

19. Fortini P, Ferretti C, Dogliotti E. The response to DNA damage during differentiation: pathways and consequences. Mutat Res 2013; 743-744: 160-8.10.1016/j.mrfmmm.2013.03.00423562804Search in Google Scholar

20. 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: 2345-53.10.1016/j.bbagen.2012.09.00122995214Search in Google Scholar

21. Rocha CRR, Lerner LK, Okamoto OK, Marchetto MC, Menck CFM. The role of DNA repair in the pluripotency and differentiation of human stem cells. Mutat Res 2013; 752: 25-35.10.1016/j.mrrev.2012.09.00123010441Search in Google Scholar

22. Tichy ED, Pillai R, Deng L, Liang L, Tischfield J, Schwemberger SJ, et al. Mouse embryonic stem cells, but not somatic cells, predominantly use homologous recombination to repair double-strand DNA breaks. Stem Cells Dev 2010; 19: 1699-711.10.1089/scd.2010.0058312831120446816Search in Google Scholar

23. Liu JC, Guan X, Ryan JA, Rivera AG, Mock C, Agrawal V, et al. High mitochondrial priming sensitizes hESCs to DNA-damage-induced apoptosis. Cell Stem Cell 2013; 13: 483-91.10.1016/j.stem.2013.07.018410964723954752Search in Google Scholar

24. Sokolov M V, Neumann RD. Radiation-induced bystander effects in cultured human stem cells. PLoS One 2010; 5: e14195.10.1371/journal.pone.0014195299628021152027Search in Google Scholar

25. Lan ML, Acharya MM, Tran KK, Bahari-Kashani J, Patel NH, Strnadel J, et al. Characterizing the radioresponse of pluripotent and multipotent human stem cells. PLoS One 2012; 7: e50048.10.1371/journal.pone.0050048352268923272054Search in Google Scholar

26. Adams BR, Golding SE, Rao RR, 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: e10001.10.1371/journal.pone.0010001284885520368801Search in Google Scholar

27. Blanpain C, Mohrin M, Sotiropoulou PA, Passegué E. DNA-damage response in tissue-specific and cancer stem cells. Cell Stem Cell 2011; 8: 16-29.10.1016/j.stem.2010.12.01221211780Search in Google Scholar

28. Mandal PK, Blanpain C, Rossi DJ. DNA damage response in adult stem cells: pathways and consequences. Nat Rev Mol Cell Biol 2011; 12: 198-202.10.1038/nrm306021304553Search in Google Scholar

29. Latella L, Lukas J, Simone C, Puri PL, Bartek J. Differentiation-induced radioresistance in muscle cells. Mol Cell Biol 2004; 24: 6350-61.10.1128/MCB.24.14.6350-6361.200443424915226436Search in Google Scholar

30. Mohrin M, Bourke E, Alexander D, Warr MR, Barry-Holson K, Le Beau MM, et al. Hematopoietic stem cell quiescence promotes error-prone DNA repair and mutagenesis. Cell Stem Cell 2010; 7: 174-85.10.1016/j.stem.2010.06.014292490520619762Search in Google Scholar

31. Zheng H, Ying H, Yan H, Kimmelman AC, Hiller DJ, Chen AJ, et al. p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 2008; 455: 1129-33.10.1038/nature07443405143318948956Search in Google Scholar

32. Bonizzi G, Cicalese A, Insinga A, Pelicci PG. The emerging role of p53 in stem cells. Trends Mol Med 2014; 18: 6-12.10.1016/j.molmed.2011.08.00221907001Search in Google Scholar

33. Solozobova V, Blattner C. P53 in stem cells. World J Biol Chem 2011; 2: 202-14.10.4331/wjbc.v2.i9.202317875721949570Search in Google Scholar

34. Haupt S, Berger M, Goldberg Z, Haupt Y. Apoptosis - the p53 network. J Cell Sci 2003; 116: 4077-85.10.1242/jcs.0073912972501Search in Google Scholar

35. Yu J, Zhang L. The transcriptional targets of p53 in apoptosis control. Biochem Biophys Res Commun 2005; 331: 851-8.10.1016/j.bbrc.2005.03.18915865941Search in Google Scholar

36. Hong H, Takahashi K, Ichisaka T, Aoi T, Kanagawa O, Nakagawa M, et al. Suppression of induced pluripotent stem cell generation by the p53–p21 pathway. Nature 2009; 460: 1132-5.10.1038/nature08235291723519668191Search in Google Scholar

37. Menendez S, Camus S, Belmonte JCI. p53: Guardian of reprogramming. Cell Cycle 2010; 9: 3887-91.10.4161/cc.9.19.1330120948296Search in Google Scholar

38. Tapia N, Schöler HR. P53 connects tumorigenesis and reprogramming to pluripotency. J Exp Med 2010; 207: 2045-8.10.1084/jem.20101866294707120876313Search in Google Scholar

39. Zheng H, Ying H, Yan H, Kimmelman AC, Hiller DJ, Chen AJ, et al. p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 2008; 455: 1129-33.10.1038/nature07443405143318948956Search in Google Scholar

40. Dosch J, Lee CJ, Simeone DM. Cancer stem cells: pancreatic cancer. Stem Cells Cancer 2009; 414: 105-11.10.1007/978-1-60327-933-8_15Search in Google Scholar

41. Marión RM, Strati K, Li H, Murga M, Blanco R, Ortega S, et al. A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 2009; 460: 1149-53.10.1038/nature08287362408919668189Search in Google Scholar

42. Dolezalova D, Mraz M, Barta T, Plevova K, Vinarsky V, Holubcova Z, et al. MicroRNAs regulate p21(Waf1/Cip1) protein expression and the DNA damage response in human embryonic stem cells. Stem Cells 2012; 30: 1362-72.10.1002/stem.110822511267Search in Google Scholar

43. Maimets T, Neganova I, Armstrong L, Lako M. Activation of p53 by nutlin leads to rapid differentiation of human embryonic stem cells. Oncogene 2008; 27: 5277-87.10.1038/onc.2008.16618521083Search in Google Scholar

44. Sabapathy K, Klemm M, Jaenisch R, Wagner EF. Regulation of ES cell differentiation by functional and conformational modulation of p53. EMBO J 1997; 16: 6217-29.10.1093/emboj/16.20.621713263069321401Search in Google Scholar

45. Jain AK, Allton K, Iacovino M, Mahen E, Milczarek RJ, Zwaka TP, et al. p53 regulates cell cycle and microRNAs to promote differentiation of human embryonic stem cells. PLoS Biol 2012; 10: e1001268.10.1371/journal.pbio.1001268328960022389628Search in Google Scholar

46. Okada Y, Shimazaki T, Sobue G, Okano H. Retinoic-acid-concentration-dependent acquisition of neural cell identity during in vitro differentiation of mouse embryonic stem cells. Dev Biol 2004; 275: 124-42.10.1016/j.ydbio.2004.07.03815464577Search in Google Scholar

47. Burridge PW, Keller G, Gold JD, Wu JC. Production of de novo cardiomyocytes: human pluripotent stem cell differentiation and direct reprogramming. Cell Stem Cell 2012; 10: 16-28.10.1016/j.stem.2011.12.013325507822226352Search in Google Scholar

48. Kawaguchi J, Mee PJ, Smith AG. Osteogenic and chondrogenic differentiation of embryonic stem cells in response to specific growth factors. Bone 2005; 36: 758-69.10.1016/j.bone.2004.07.01915794925Search in Google Scholar

49. Lin T, Chao C, Saito S, Mazur SJ, Murphy ME, Appella E, et al. p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat Cell Biol 2005; 7: 165-71.10.1038/ncb121115619621Search in Google Scholar

50. Dravid G, Ye Z, Hammond H, Chen G, Pyle A, Donovan P, et al. Defining the role of Wnt/β-catenin signaling in the survival, proliferation, and self-renewal of human embryonic stem cells. Stem Cells 2005; 23: 1489-501.10.1634/stemcells.2005-003416002782Search in Google Scholar

51. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou AH. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 2004; 10: 55-63.10.1038/nm97914702635Search in Google Scholar

52. Taupin P, Gage FH. Adult neurogenesis and neural stem cells of the central nervous system in mammals. J Neurosci Res 2002; 69: 745-9.10.1002/jnr.1037812205667Search in Google Scholar

53. Galli R, Gritti A, Bonfanti L, Vescovi AL. Neural stem cells: an overview. Circ Res 2003; 92: 598-608.10.1161/01.RES.0000065580.02404.F412676811Search in Google Scholar

54. Armesilla-Diaz A, Bragado P, Del Valle I, Cuevas E, Lazaro I, Martin C, et al. p53 regulates the self-renewal and differentiation of neural precursors. Neuroscience 2009; 158: 1378-89.10.1016/j.neuroscience.2008.10.05219038313Search in Google Scholar

55. Monje ML, Mizumatsu S, Fike JR, Palmer TD. Irradiation induces neural precursor-cell dysfunction. Nat Med 2002; 8: 955-62.10.1038/nm74912161748Search in Google Scholar

56. Wei L-C, Ding Y-X, Liu Y-H, Duan L, Bai Y, Shi M, et al. Low-dose radiation stimulates Wnt/β-catenin signaling, neural stem cell proliferation and neurogenesis of the mouse hippocampus in vitro and in vivo. Curr Alzheimer Res 2012; 9: 278-89.10.2174/15672051280010762722272614Search in Google Scholar

57. Visvader JE, Stingl J, Genes D. Mammary stem cells and the differentiation hierarchy: current status and perspectives. Genes Dev 2014; 28: 1143-58.10.1101/gad.242511.114405276124888586Search in Google Scholar

58. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, et al. Generation of a functional mammary gland from a single stem cell. Nature 2006; 439: 84-8.10.1038/nature0437216397499Search in Google Scholar

59. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003; 17: 1253-70.10.1101/gad.106180319605612756227Search in Google Scholar

60. Cicalese A, Bonizzi G, Pasi CE, Faretta M, Ronzoni S, Giulini B, et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 2014; 138: 1083-95.10.1016/j.cell.2009.06.04819766563Search in Google Scholar

61. Ziyaie D, Hupp TR, Thompson AM. P53 and breast cancer. Breast 2000; 9: 239-46.10.1054/brst.2000.019914732173Search in Google Scholar

62. Insinga a, Cicalese a, Faretta M, Gallo B, Albano L, Ronzoni S, et al. DNA damage in stem cells activates p21, inhibits p53, and induces symmetric self-renewing divisions. Proc Natl Acad Sci U S A 2013; 110: 3931-6.10.1073/pnas.1213394110359390123417300Search in Google Scholar

63. Kondo M, Wagers AJ, Manz MG, Prohaska SS, Scherer DC, Beilhack GF, et al. Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annu Rev Immunol 2003; 21: 759-806.10.1146/annurev.immunol.21.120601.14100712615892Search in Google Scholar

64. Milyavsky M, Gan OI, Trottier M, Komosa M, Tabach O, Notta F, et al. A distinctive DNA damage response in human hematopoietic stem cells reveals an apoptosis-independent role for p53 in self-renewal. Cell Stem Cell 2014; 7: 186-97.10.1016/j.stem.2010.05.01620619763Search in Google Scholar

65. Mitra K. Mitochondrial fission-fusion as an emerging key regulator of cell proliferation and differentiation. Bioessays 2013; 35: 955-64.10.1002/bies.20130001123943303Search in Google Scholar

66. Yakes FM, Van Houten B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci 1997; 94: 514-9.10.1073/pnas.94.2.514195449012815Search in Google Scholar

67. Kam WW-Y, Banati RB. Effects of ionizing radiation on mitochondria. Free Radic Biol Med 2013; 65: 607-19.10.1016/j.freeradbiomed.2013.07.02423892359Search in Google Scholar

68. Azzam EI, Jay-Gerin JP, Pain D. Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury. Cancer Lett 2012; 327: 48-60.10.1016/j.canlet.2011.12.012398044422182453Search in Google Scholar

69. Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science 2012; 337: 1062-5.10.1126/science.1219855476202822936770Search in Google Scholar

70. Nugent SME, Mothersill CE, Seymour C, McClean B, Lyng FM, Murphy JEJ. Increased mitochondrial mass in cells with functionally compromised mitochondria after exposure to both direct γ radiation and bystander factors. Radiat Res 2007; 168: 134-42.10.1667/RR0769.117722997Search in Google Scholar

71. Bañuelos CA, Banáth JP, MacPhail SH, Zhao J, Eaves CA, O’Connor MD, et al. Mouse but not human embryonic stem cells are deficient in rejoining of ionizing radiation-induced DNA double-strand breaks. DNA Repair (Amst) 2008; 7: 1471-83.10.1016/j.dnarep.2008.05.00518602349Search in Google Scholar

72. Hanawalt P. Functional characterization of global genomic DNA repair and its implications for cancer. Mutat Res Mutat Res 2003; 544: 107-14.10.1016/j.mrrev.2003.06.00214644313Search in Google Scholar

73. Purschke M, Kasten-Pisula U, Brammer I, Dikomey E. Human and rodent cell lines showing no differences in the induction but differing in the repair kinetics of radiation-induced DNA base damage. Int J Radiat Biol 2004; 80: 29-38.10.1080/0955300031000164288514761848Search in Google Scholar

74. Parrinello S, Samper E, Krtolica A, Goldstein J, Melov S, Campisi J. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat Cell Biol 2003; 5: 741-7.10.1038/ncb1024Search in Google Scholar

75. Hornsby PJ. Mouse and human cells versus oxygen. Sci Aging Knowl Environ 2003; 2003: PE21.10.1126/sageke.2003.30.pe21Search in Google Scholar

76. Wright WE, Shay JW. Telomere dynamics in cancer progression and prevention: fundamental differences in human and mouse telomere biology. Nat Med 2000; 6: 849-51.10.1038/78592Search in Google Scholar

77. Hornsby PJ. Replicative senescence of human and mouse cells in culture: significance for aging research. Mech Ageing Dev 2003; 124: 853-5.10.1016/S0047-6374(03)00173-8Search in Google Scholar