Response of normal stem cells to ionizing radiation: A balance between homeostasis and genomic stability

Mutation Research - Reviews in Mutation Research

Volumn 704, Issue 1-3, 2010, Pages 167-174

  Harfouche, Ghida ^a   Martin, Michèle T ^a  

^a Institute of Cellular and Molecular Radiobiology   (France)

Author keywords

Adult stem cells; Apoptosis; DNA repair; Embryonic stem cells; Genomic stability; Ionizing radiation

Indexed keywords

HISTONE H2AX;

CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; CELL SURVIVAL; DNA REPAIR; DOUBLE STRANDED DNA BREAK; EMBRYONIC STEM CELL; GENOMIC INSTABILITY; HEMATOPOIETIC STEM CELL; HOMEOSTASIS; HUMAN; INTESTINE; IONIZING RADIATION; KERATINOCYTE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RADIATION INJURY; RADIATION RESPONSE; RADIOBIOLOGY; RADIOSENSITIVITY; REVIEW; SIGNAL TRANSDUCTION; SKIN; STEM CELL; STRESS;

BONE MARROW CELLS; DNA DAMAGE; DNA REPAIR; EMBRYONIC STEM CELLS; GENOMIC INSTABILITY; HEMATOPOIETIC STEM CELLS; HOMEOSTASIS; HUMANS; INTESTINES; RADIATION TOLERANCE; RADIATION, IONIZING; SIGNAL TRANSDUCTION; SKIN; STEM CELLS; TIME;

EID: 77951977373     PISSN: 13835742     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrrev.2010.01.007     Document Type: Review

References (82)

1. Till J.E., and Mc C.E. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat. Res. 14 (1961) 213-222
2. Morrison S.J., Shah N.M., and Anderson D.J. Regulatory mechanisms in stem cell biology. Cell 88 (1997) 287-298
3. Potten C.S., and Grant H.K. The relationship between ionizing radiation-induced apoptosis and stem cells in the small and large intestine. Br. J. Cancer 78 (1998) 993-1003
4. Hall P.A., and Watt F.M. Stem cells: the generation and maintenance of cellular diversity. Development 106 (1989) 619-633
5. Knoblich J.A. Asymmetric cell division during animal development. Nat. Rev. Mol. Cell Biol. 2 (2001) 11-20
6. Lajtha L.G. Stem cell concepts. Nouv. Rev. Fr. Hematol. 21 (1979) 59-65
7. Clarke M.F., and Fuller M. Stem cells and cancer: two faces of eve. Cell 124 (2006) 1111-1115
8. Grichnik J.M. Genomic instability and tumor stem cells. J. Invest. Dermatol. 126 (2006) 1214-1216
9. Charames G.S., and Bapat B. Genomic instability and cancer. Curr. Mol. Med. 3 (2003) 589-596
10. Gilley D., Tanaka H., and Herbert B.S. Telomere dysfunction in aging and cancer. Int. J. Biochem. Cell Biol. 37 (2005) 1000-1013
11. Baumann M., Krause M., and Hill R. Exploring the role of cancer stem cells in radioresistance. Nat. Rev. Cancer 8 (2008) 545-554
12. Evans M.J., and Kaufman M.H. Establishment in culture of pluripotential cells from mouse embryos. Nature 292 (1981) 154-156
13. Martin G.R. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. U.S.A. 78 (1981) 7634-7638
14. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., and Jones J.M. Embryonic stem cell lines derived from human blastocysts. Science 282 (1998) 1145-1147
15. Banuelos C.A., Banath J.P., MacPhail S.H., Zhao J., Eaves C.A., O'Connor M.D., Lansdorp P.M., and Olive P.L. Mouse but not human embryonic stem cells are deficient in rejoining of ionizing radiation-induced DNA double-strand breaks. DNA Repair (Amst.) 7 (2008) 1471-1483
16. Solozobova V., Rolletschek A., and Blattner C. Nuclear accumulation and activation of p53 in embryonic stem cells after DNA damage. BMC Cell Biol. 10 (2009) 46
17. Lin T., Chao C., Saito S., Mazur S.J., Murphy M.E., Appella E., and Xu Y. p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat. Cell Biol. 7 (2005) 165-171
18. Hong Y., and 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. 101 (2004) 14443-14448
19. Saretzki G., Armstrong L., Leake A., Lako M., and von Zglinicki T. Stress defense in murine embryonic stem cells is superior to that of various differentiated murine cells. Stem Cells 22 (2004) 962-971
20. Banath J.P., Banuelos C.A., Klokov D., MacPhail S.M., Lansdorp P.M., and Olive P.L. Explanation for excessive DNA single-strand breaks and endogenous repair foci in pluripotent mouse embryonic stem cells. Exp. Cell Res. 315 (2009) 1505-1520
21. Tanaka T.S. Transcriptional heterogeneity in mouse embryonic stem cells. Reprod. Fertil. Dev. 21 (2009) 67-75
22. Kalmar T., Lim C., Hayward P., Munoz-Descalzo S., Nichols J., Garcia-Ojalvo J., and Martinez A. Aries regulated fluctuations in nanog expression mediate cell fate decisions in embryonic stem cells. PLoS Biol. 7 (2009) e1000149
23. Humpherys D., Eggan K., Akutsu H., Hochedlinger K., Rideout W.M., Biniszkiewicz III D., Yanagimachi R., and Jaenisch R. Epigenetic instability in ES cells and cloned mice. Science 293 (2001) 95-97
24. Filion T.M., Qiao M., Ghule P.N., Mandeville M., van Wijnen A.J., Stein J.L., Lian J.B., Altieri D.C., and Stein G.S. Survival responses of human embryonic stem cells to DNA damage. J. Cell. Physiol. 220 (2009) 586-592
25. Momcilovic O., Choi S., Varum S., Bakkenist C., Schatten G., and 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 27 (2009) 1822-1835
26. Maynard S., Swistikowa A.M., Lee J.W., Liu Y., Liu S.T., Rao D.A.C.A.M., de Souza-Pinto N., Zeng X., and Bohr V.A. Human embryonic stem cells have enhanced repair of multiple forms of DNA damage. Stem Cells 26 (2008) 2266-2274
27. Moore M.A. Stem cell proliferation: ex vivo and in vivo observations. Stem Cells 15 Suppl. 1 (1997) 239-248 (discussion 248-251)
28. Zon L.I. Intrinsic and extrinsic control of haematopoietic stem-cell self-renewal. Nature 453 (2008) 306-313
29. Greenberger J.S., and Epperly M. Bone marrow-derived stem cells and radiation response. Semin. Radiat. Oncol. 19 (2009) 133-139
30. Cheng T., Rodrigues N., Shen H., Yang Y., Dombkowski D., Sykes M., and Scadden D.T. Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science 287 (2000) 1804-1808
31. Quesenberry P.J., Colvin G.A., Lambert J.F., Frimberger A.E., Dooner M.S., McAuliffe C.I., Miller C., Becker P., Badiavas E., Falanga V.J., Elfenbein G., and Lum L.G. The new stem cell biology. Trans. Am. Clin. Climatol. Assoc. 113 (2002) 182-206 (discussion 206-187)
32. Zipori D. The stem state: plasticity is essential, whereas self-renewal and hierarchy are optional. Stem Cells 23 (2005) 719-726
33. Glauche I., Moore K., Thielecke L., Horn K., Loeffler M., and Roeder I. Stem cell proliferation and quiescence-two sides of the same coin. PLoS Comput. Biol. 5 (2009) e1000447
34. Kreja L., Thoma S., Selig C., Lamping C., Ziegler B.L., and Nothdurft W. The effect of recombinant human stem cell factor and basic fibroblast growth factor on the in vitro radiosensitivity of CD34+ hematopoietic progenitors from human umbilical cord blood. Exp. Hematol. 21 (1993) 1436-1441
35. Zhao Y., Zhan Y., Burke K.A., and Anderson W.F. Soluble factor(s) from bone marrow cells can rescue lethally irradiated mice by protecting endogenous hematopoietic stem cells. Exp. Hematol. 33 (2005) 428-434
36. Meijne E.I., van der Winden-van Groenewegen R.J., Ploemacher R.E., Vos O., David J.A., and Huiskamp R. The effects of x-irradiation on hematopoietic stem cell compartments in the mouse. Exp. Hematol. 19 (1991) 617-623
37. Ploemacher R.E., van Os R., van Beurden C.A., and Down J.D. Murine haemopoietic stem cells with long-term engraftment and marrow repopulating ability are more resistant to gamma-radiation than are spleen colony forming cells. Int. J. Radiat. Biol. 61 (1992) 489-499
38. Tothova Z., and Gilliland D.G. FoxO transcription factors and stem cell homeostasis: insights from the hematopoietic system. Cell Stem Cell 1 (2007) 140-152
39. Wang Y., Schulte B.A., LaRue A.C., Ogawa M., and Zhou D. Total body irradiation selectively induces murine hematopoietic stem cell senescence. Blood 107 (2006) 358-366
40. Ban N., and Kai M. Implication of replicative stress-related stem cell ageing in radiation-induced murine leukaemia. Br. J. Cancer 101 (2009) 363-371
41. Simonnet A.J., Nehme J., Vaigot P., Barroca V., Leboulch P., and Tronik-Le Roux D. Phenotypic and functional changes induced in hematopoietic stem/progenitor cells after gamma-ray radiation exposure. Stem Cells 27 (2009) 1400-1409
42. Watson G.E., Lorimore S.A., Macdonald D.A., and Wright E.G. Chromosomal instability in unirradiated cells induced in vivo by a bystander effect of ionizing radiation. Cancer Res. 60 (2000) 5608-5611
43. Lorimore S.A., McIlrath J.M., Coates P.J., and Wright E.G. Chromosomal instability in unirradiated hemopoietic cells resulting from a delayed in vivo bystander effect of gamma radiation. Cancer Res. 65 (2005) 5668-5673
44. Nijnik A., Woodbine L., Marchetti C., Dawson S., Lambe T., Liu C., Rodrigues N.P., Crockford T.L., Cabuy E., Vindigni A., Enver T., Bell J.I., Slijepcevic P., Goodnow C.C., Jeggo P.A., and Cornall R.J. DNA repair is limiting for haematopoietic stem cells during ageing. Nature 447 (2007) 686-690
45. Pontikoglou C., Delorme B., and Charbord P. Human bone marrow native mesenchymal stem cells. Regen. Med. 3 (2008) 731-741
46. Delorme B., Ringe J., Pontikoglou C., Gaillard J., Langonne A., Sensebe L., Noel D., Jorgensen C., Haupl T., and Charbord P. Specific lineage-priming of bone marrow mesenchymal stem cells provides the molecular framework for their plasticity. Stem Cells 27 (2009) 1142-1151
47. Friedenstein A.J., Chailakhyan R.K., Latsinik N.V., Panasyuk A.F., and Keiliss-Borok I.V. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 17 (1974) 331-340
48. Zipori D. The nature of stem cells: state rather than entity. Nat. Rev. Genet. 5 (2004) 873-878
49. Chen M.F., Lin C.T., Chen W.C., Yang C.T., Chen C.C., Liao S.K., Liu J.M., Lu C.H., and Lee K.D. The sensitivity of human mesenchymal stem cells to ionizing radiation. Int. J. Radiat. Oncol. Biol. Phys. 66 (2006) 244-253
50. Rieger K., Marinets O., Fietz T., Korper S., Sommer D., Mucke C., Reufi B., Blau W.I., Thiel E., and Knauf W.U. Mesenchymal stem cells remain of host origin even a long time after allogeneic peripheral blood stem cell or bone marrow transplantation. Exp. Hematol. 33 (2005) 605-611
51. Morikawa S., Mabuchi Y., Kubota Y., Nagai Y., Niibe K., Hiratsu E., Suzuki S., Miyauchi-Hara C., Nagoshi N., Sunabori T., Shimmura S., Miyawaki A., Nakagawa T., Suda T., Okano H., and Matsuzaki Y. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J. Exp. Med. 206 (2009) 2483-2496
52. Freedman G.M., Li T., Nicolaou N., Chen Y., Ma C.C., and Anderson P.R. Breast intensity-modulated radiation therapy reduces time spent with acute dermatitis for women of all breast sizes during radiation. Int. J. Radiat. Oncol. Biol. Phys. 74 (2009) 689-694
53. McQuestion M. Evidence-based skin care management in radiation therapy. Semin. Oncol. Nurs. 22 (2006) 163-173
54. Hymes S.R., Strom E.A., and Fife C. Radiation dermatitis: clinical presentation, pathophysiology, and treatment 2006. J. Am. Acad. Dermatol. 54 (2006) 28-46
55. Brouard M., and Barrandon Y. Controlling skin morphogenesis: hope and despair. Curr. Opin. Biotechnol. 14 (2003) 520-525
56. Rachidi W., Harfourche G., Lemaitre G., Amiot F., Vaigot P., and Martin M.T. Sensing radiosensitivity of human epidermal stem cells. Radiother. Oncol. 83 (2007) 267-276
57. Clayton E., Doupe D.P., Klein A.M., Winton D.J., Simons B.D., and Jones P.H. A single type of progenitor cell maintains normal epidermis. Nature 446 (2007) 185-189
58. Fuchs E. Skin stem cells: rising to the surface. J. Cell Biol. 180 (2008) 273-284
59. N.O. Fortunel, E. Cadio, P. Vaigot, L. Chadli, S. Moratille, S. Bouet, P.H. Roméo, M.T. Martin, Parallel clonal microcultures of keratinocytes: a new experimental system to explore the functional hierarchy of the basal layer of human epidermis, Exp. Dermatol. (2010), in press.
60. Li A., Simmons P.J., and Kaur P. Identification and isolation of candidate human keratinocyte stem cells based on cell surface phenotype. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 3902-3907
61. Terunuma A., Kapoor V., Yee C., Telford W.G., Udey M.C., and Vogel J.C. Stem cell activity of human side population and {alpha}6 integrin-bright keratinocytes defined by a quantitative in vivo assay. Stem Cells 25 (2007) 664-669
62. Tiberio R., Marconi A., Fila C., Fumelli C., Pignatti M., Krajewski S., Giannetti A., Reed J.C., and Pincelli C. Keratinocytes enriched for stem cells are protected from anoikis via an integrin signaling pathway in a Bcl-2 dependent manner. FEBS Lett. 524 (2002) 139-144
63. Sivan V., Vozenin-Brotons M.C., Tricaud Y., Lefaix J.L., Cosset J.M., Dubray B., and Martin M.T. Altered proliferation and differentiation of human epidermis in cases of skin fibrosis after radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 53 (2002) 385-393
64. Shore R.E., Moseson M., Xue X., Tse Y., Harley N., and Pasternack B.S. Skin cancer after X-ray treatment for scalp ringworm. Radiat. Res. 157 (2002) 410-418
65. Inomata K., Aoto T., Binh N.T., Okamoto N., Tanimura S., Wakayama T., Iseki S., Hara E., Masunaga T., Shimizu H., and Nishimura E.K. Genotoxic stress abrogates renewal of melanocyte stem cells by triggering their differentiation. Cell 137 (2009) 1088-1099
66. Potten C.S., Owen G., and Roberts S.A. The temporal and spatial changes in cell proliferation within the irradiated crypts of the murine small intestine. Int. J. Radiat. Biol. 57 (1990) 185-199
67. Potten C.S. Radiation, the ideal cytotoxic agent for studying the cell biology of tissues such as the small intestine. Radiat. Res. 161 (2004) 123-136
68. Hendry J.H., Dorr W., Hill R.P., and Potten C.S. No apoptotic endothelial cells in irradiated intestine: regarding Schuller et al. (Int. J. Radiat. Oncol. Biol. Phys. 2007;68:205-210). Int. J. Radiat. Oncol. Biol. Phys. 70 (2008) 801-802 (author reply 803)
69. Barker N., van Es J.H., Kuipers J., Kujala P., van den Born M., Cozijnsen M., Haegebarth A., Korving J., Begthel H., Peters P.J., and Clevers H. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449 (2007) 1003-1007
70. Ch'ang H.J., Maj J.G., Paris F., Xing H.R., Zhang J., Truman J.P., Cardon-Cardo C., Haimovitz-Friedman A., Kolesnick R., and Fuks Z. ATM regulates target switching to escalating doses of radiation in the intestines. Nat. Med. 11 (2005) 484-490
71. Qiu W., Carson-Walter E.B., Liu H., Epperly M., Greenberger J.S., Zambetti G.P., Zhang L., and Yu J. PUMA regulates intestinal progenitor cell radiosensitivity and gastrointestinal syndrome. Cell Stem Cell 2 (2008) 576-583
72. Pritchard D.M., Print C., O'Reilly L., Adams J.M., Potten C.S., and Hickman J.A. Bcl-w is an important determinant of damage-induced apoptosis in epithelia of small and large intestine. Oncogene 19 (2000) 3955-3959
73. Tucker S.L., Withers H.R., Mason K.A., and Thames Jr. H.D. A dose-surviving fraction curve for mouse colonic mucosa. Eur. J. Cancer Clin. Oncol. 19 (1983) 433-437
74. Hendry J.H. A new derivation, from split-dose data, of the complete survival curve for clonogenic normal cells in vivo. Radiat. Res. 78 (1979) 404-414
75. Hendry J.H., Cai W.B., Roberts S.A., and Potten C.S. p53 deficiency sensitizes clonogenic cells to irradiation in the large but not the small intestine. Radiat. Res. 148 (1997) 254-259
76. Merritt A.J., Potten C.S., Watson A.J., Loh D.Y., Nakayama K., and Hickman J.A. Differential expression of bcl-2 in intestinal epithelia. Correlation with attenuation of apoptosis in colonic crypts and the incidence of colonic neoplasia. J. Cell Sci. 108 Pt 6 (1995) 2261-2271
77. Cairns J. Mutation selection and the natural history of cancer. Nature 255 (1975) 197-200
78. Potten C.S., Owen G., and Booth D. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J. Cell Sci. 115 (2002) 2381-2388
79. Sato T., Vries R.G., Snippert H.J., van de Wetering M., Barker N., Stange D.E., van Es J.H., Abo A., Kujala P., Peters P.J., and Clevers H. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459 (2009) 262-265
80. Potten C.S. Keratinocyte stem cells, label-retaining cells and possible genome protection mechanisms. J. Investig. Dermatol. Symp. Proc. 9 (2004) 183-195
81. Barroca V., Lassalle B., Coureuil M., Louis J.P., Le Page F., Testart J., Allemand I., Riou L., and Fouchet P. Mouse differentiating spermatogonia can generate germinal stem cells in vivo. Nat. Cell Biol. 11 (2009) 190-196
82. Meshorer E., Yellajoshula D., George E., Scambler P.J., Brown D.T., and Misteli T. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev. Cell 10 (2006) 105-116