DNA damage response, redox status and hematopoiesis

Blood Cells, Molecules, and Diseases

Volumn 52, Issue 1, 2014, Pages 12-18

  Weiss, Cary N ^a   Ito, Keisuke ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Ataxia telangiectasia mutated; DNA damage; Hematopoietic stem cells; Reactive oxygen species

Indexed keywords

ATM PROTEIN; PROTEIN BID; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR FOXO;

ARTICLE; AUTOPHAGY; CELL DIFFERENTIATION; CELL FATE; CELL METABOLISM; CELL STRESS; DNA DAMAGE; DNA END JOINING REPAIR; DNA REPLICATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL;

ATAXIA TELANGIECTASIA;

ATAXIA-TELANGIECTASIA MUTATED; DNA DAMAGE; HEMATOPOIETIC STEM CELLS; REACTIVE OXYGEN SPECIES;

ANIMALS; ATAXIA TELANGIECTASIA; ATAXIA TELANGIECTASIA MUTATED PROTEINS; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CELL DIFFERENTIATION; CELL PROLIFERATION; DNA DAMAGE; GENE EXPRESSION REGULATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; OXIDATION-REDUCTION; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84888323327     PISSN: 10799796     EISSN: 10960961     Source Type: Journal    
DOI: 10.1016/j.bcmd.2013.08.002     Document Type: Article

References (101)

1. Alberts B. Molecular Biology of the Cell 2002, Garland Science, New York.
2. Attar E.C., Scadden D.T. Regulation of hematopoietic stem cell growth. Leukemia 2004, 18:1760-1768.
3. Lemischka I.R., Raulet D.H., Mulligan R.C. Developmental potential and dynamic behavior of hematopoietic stem cells. Cell 1986, 45:917-927.
4. Osawa M., Hanada K., Hamada H., Nakauchi H. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 1996, 273:242-245.
5. Yilmaz O.H., Kiel M.J., Morrison S.J. SLAM family markers are conserved among hematopoietic stem cells from old and reconstituted mice and markedly increase their purity. Blood 2006, 107:924-930.
6. Kiel M.J., Yilmaz O.H., Iwashita T., et al. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 2005, 121:1109-1121.
7. Orkin S.H., Zon L.I. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 2008, 132:631-644.
8. Naka K., Hirao A. Maintenance of genomic integrity in hematopoietic stem cells. Int. J. Hematol. 2011, 93:434-439.
9. Cheshier S.H., Morrison S.J., Liao X., Weissman I.L. In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:3120-3125.
10. Kiel M.J., He S., Ashkenazi R., et al. Haematopoietic stem cells do not asymmetrically segregate chromosomes or retain BrdU. Nature 2007, 449:238-242.
11. Wilson A., Laurenti E., Oser G., et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 2008, 135:1118-1129.
12. Orford K.W., Scadden D.T. Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat. Rev. Genet. 2008, 9:115-128.
13. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
14. Lombard D.B., Chua K.F., Mostoslavsky R., et al. DNA repair, genome stability, and aging. Cell 2005, 120:497-512.
15. Bagby G.C., Alter B.P. Fanconi anemia. Semin. Hematol. 2006, 43:147-156.
16. Hoeijmakers J.H. DNA damage, aging, and cancer. N. Engl. J. Med. 2009, 361:1475-1485.
17. Branzei D., Foiani M. Regulation of DNA repair throughout the cell cycle. Nat. Rev. Mol. Cell Biol. 2008, 9:297-308.
18. Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993, 362:709-715.
19. Mandal P.K., Blanpain C., Rossi D.J. DNA damage response in adult stem cells: pathways and consequences. Nat. Rev. Mol. Cell Biol. 2011, 12:198-202.
20. Ciccia A., Elledge S.J. The DNA damage response: making it safe to play with knives. Mol. Cell 2010, 40:179-204.
21. Jackson S.P., Bartek J. The DNA-damage response in human biology and disease. Nature 2009, 461:1071-1078.
22. Rossi D.J., Jamieson C.H.M., Weissman I.L. Stems cells and the pathways to aging and cancer. Cell 2008, 132:681-696.
23. Parmar K., Kim J., Sykes S.M., et al. Hematopoietic stem cell defects in mice with deficiency of Fancd2 or Usp1. Stem Cells 2010, 28:1186-1195.
24. -/- mice have hematopoietic defects that can be partially corrected by resveratrol. Blood 2010, 116:5140-5148.
25. Clarke M.F., Fuller M. Stem cells and cancer: two faces of eve. Cell 2006, 124:1111-1115.
26. Jamieson C.H., Ailles L.E., Dylla S.J., et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N. Engl. J. Med. 2004, 351:657-667.
27. Kinzler K.W., Vogelstein B. Lessons from hereditary colorectal cancer. Cell 1996, 87:159-170.
28. Rossi D.J., Bryder D., Seita J., et al. Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 2007, 447:725-729.
29. Rube C.E., Fricke A., Widmann T.A., et al. Accumulation of DNA damage in hematopoietic stem and progenitor cells during human aging. PLoS One 2011, 6:e17487.
30. Wang J., Sun Q., Morita Y., et al. A differentiation checkpoint limits hematopoietic stem cell self-renewal in response to DNA damage. Cell 2012, 148:1001-1014.
31. Barzilai A., Rotman G., Shiloh Y. ATM deficiency and oxidative stress: a new dimension of defective response to DNA damage. DNA Repair (Amst) 2002, 1:3-25.
32. Meyn M.S. Ataxia-telangiectasia and cellular responses to DNA damage. Cancer Res. 1995, 55:5991-6001.
33. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 2003, 3:155-168.
34. Balaban R.S., Nemoto S., Finkel T. Mitochondria, oxidants, and aging. Cell 2005, 120:483-495.
35. Suda T., Takubo K., Semenza G.L. Metabolic regulation of hematopoietic stem cells in the hypoxic niche. Cell Stem Cell 2011, 9:298-310.
36. Bjelakovic G., Nikolova D., Gluud L.L., Simonetti R.G., Gluud C. Mortality in randomized trials of antioxidant supplements for primary and secondary prevention: systematic review and meta-analysis. JAMA 2007, 297:842-857.
37. Cipolleschi M.G., Dello Sbarba P., Olivotto M. The role of hypoxia in the maintenance of hematopoietic stem cells. Blood 1993, 82:2031-2037.
38. Mohyeldin A., Garzon-Muvdi T., Quinones-Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 2010, 7:150-161.
39. Jang Y.Y., Sharkis S.J. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 2007, 110:3056-3063.
40. Takao N., Kato H., Mori R., et al. Disruption of ATM in p53-null cells causes multiple functional abnormalities in cellular response to ionizing radiation. Oncogene 1999, 18:7002-7009.
41. Schubert R., Reichenbach J., Royer N., Pichler M., Zielen S. Spontaneous and oxidative stress-induced programmed cell death in lymphocytes from patients with ataxia telangiectasia (AT). Clin. Exp. Immunol. 2000, 119:140-147.
42. Takao N., Li Y., Yamamoto K. Protective roles for ATM in cellular response to oxidative stress. FEBS Lett. 2000, 472:133-136.
43. Kamsler A., Daily D., Hochman A., et al. Increased oxidative stress in ataxia telangiectasia evidenced by alterations in redox state of brains from Atm-deficient mice. Cancer Res. 2001, 61:1849-1854.
44. Guo Z., Deshpande R., Paull T.T. ATM activation in the presence of oxidative stress. Cell Cycle 2010, 9:4805-4811.
45. Guo Z., Kozlov S., Lavin M.F., Person M.D., Paull T.T. ATM activation by oxidative stress. Science 2010, 330:517-521.
46. Ito K., Hirao A., Arai F., et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 2004, 431:997-1002.
47. Oguro H., Iwama A., Morita Y., et al. Differential impact of Ink4a and Arf on hematopoietic stem cells and their bone marrow microenvironment in Bmi1-deficient mice. J. Exp. Med. 2006, 203:2247-2253.
48. Cheng T., Rodrigues N., Shen H., et al. Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science 2000, 287:1804-1808.
49. Allen D.M., van Praag H., Ray J., et al. Ataxia telangiectasia mutated is essential during adult neurogenesis. Genes Dev. 2001, 15:554-566.
50. Asai T., Liu Y., Bae N., Nimer S.D. The p53 tumor suppressor protein regulates hematopoietic stem cell fate. J. Cell. Physiol. 2011, 226:2215-2221.
51. Pant V., Quintas-Cardama A., Lozano G. The p53 pathway in hematopoiesis: lessons from mouse models, implications for humans. Blood 2012, 120:5118-5127.
52. Asai T., Liu Y., Di Giandomenico S., et al. Necdin, a p53 target gene, regulates the quiescence and response to genotoxic stress of hematopoietic stem/progenitor cells. Blood 2012, 120:1601-1612.
53. Fei P., El-Deiry W.S. P53 and radiation responses. Oncogene 2003, 22:5774-5783.
54. Vousden K.H., Prives C. Blinded by the light: the growing complexity of p53. Cell 2009, 137:413-431.
55. Vousden K.H., Lane D.P. p53 in health and disease. Nat. Rev. Mol. Cell Biol. 2007, 8:275-283.
56. Haupt Y., Maya R., Kazaz A., Oren M. Mdm2 promotes the rapid degradation of p53. Nature 1997, 387:296-299.
57. Collavin L., Lunardi A., Del Sal G. p53-family proteins and their regulators: hubs and spokes in tumor suppression. Cell Death Differ. 2010, 17:901-911.
58. Forsberg E.C., Prohaska S.S., Katzman S., et al. Differential expression of novel potential regulators in hematopoietic stem cells. PLoS Genet. 2005, 1:e28.
59. Liu Y., Elf S.E., Miyata Y., et al. p53 regulates hematopoietic stem cell quiescence. Cell Stem Cell 2009, 4:37-48.
60. -/- multipotent progenitors. Nature 2008, 453:228-232.
61. TeKippe M., Harrison D.E., Chen J. Expansion of hematopoietic stem cell phenotype and activity in Trp53-null mice. Exp. Hematol. 2003, 31:521-527.
62. Lacorazza H.D., Yamada T., Liu Y., et al. The transcription factor MEF/ELF4 regulates the quiescence of primitive hematopoietic cells. Cancer Cell 2006, 9:175-187.
63. Sablina A.A., Budanov A.V., Ilyinskaya G.V., et al. The antioxidant function of the p53 tumor suppressor. Nat. Med. 2005, 11:1306-1313.
64. Abbas H.A., Maccio D.R., Coskun S., et al. Mdm2 is required for survival of hematopoietic stem cells/progenitors via dampening of ROS-induced p53 activity. Cell Stem Cell 2010, 7:606-617.
65. Milyavsky M., Gan O.I., Trottier M., 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 2010, 7:186-197.
66. Molofsky A.V., Pardal R., Iwashita T., et al. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 2003, 425:962-967.
67. Park I.K., Qian D., Kiel M., et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 2003, 423:302-305.
68. Liu J., Cao L., Chen J., et al. Bmi1 regulates mitochondrial function and the DNA damage response pathway. Nature 2009, 459:387-392.
69. Smith J., Tho L.M., Xu N., Gillespie D.A. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv. Cancer Res. 2010, 108:73-112.
70. Ito K., Hirao A., Arai F., et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat. Med. 2006, 12:446-451.
71. Verma A., Deb D.K., Sassano A., et al. Cutting edge: activation of the p38 mitogen-activated protein kinase signaling pathway mediates cytokine-induced hemopoietic suppression in aplastic anemia. J. Immunol. 2002, 168:5984-5988.
72. Danial N.N., Korsmeyer S.J. Cell death: critical control points. Cell 2004, 116:205-219.
73. Kamer I., Sarig R., Zaltsman Y., et al. Proapoptotic BID is an ATM effector in the DNA-damage response. Cell 2005, 122:593-603.
74. Zinkel S.S., Hurov K.E., Ong C., et al. A role for proapoptotic BID in the DNA-damage response. Cell 2005, 122:579-591.
75. Oberkovitz G., Regev L., Gross A. Nucleocytoplasmic shuttling of BID is involved in regulating its activities in the DNA-damage response. Cell Death Differ. 2007, 14:1628-1634.
76. Maryanovich M., Oberkovitz G., Niv H., et al. The ATM-BID pathway regulates quiescence and survival of haematopoietic stem cells. Nat. Cell Biol. 2012, 14:535-541.
77. Yahata T., Takanashi T., Muguruma Y., et al. Accumulation of oxidative DNA damage restricts the self-renewal capacity of human hematopoietic stem cells. Blood 2011, 118:2941-2950.
78. Miyamoto K., Araki K.Y., Naka K., et al. Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 2007, 1:101-112.
79. Tothova Z., Kollipara R., Huntly B.J., et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 2007, 128:325-339.
80. Paik J.H., Kollipara R., Chu G., et al. FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 2007, 128:309-323.
81. Brunet A., Bonni A., Zigmond M.J., et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999, 96:857-868.
82. Dijkers P.F., Medema R.H., Lammers J.W., Koenderman L., Coffer P.J. Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr. Biol. 2000, 10:1201-1204.
83. Yamazaki S., Iwama A., Takayanagi S., et al. Cytokine signals modulated via lipid rafts mimic niche signals and induce hibernation in hematopoietic stem cells. EMBO J. 2006, 25:3515-3523.
84. Kops G.J., Dansen T.B., Polderman P.E., et al. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 2002, 419:316-321.
85. Yilmaz O.H., Valdez R., Theisen B.K., et al. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 2006, 441:475-482.
86. Zhang J., Grindley J.C., Yin T., et al. PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 2006, 441:518-522.
87. Maehama T., Dixon J.E. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 1998, 273:13375-13378.
88. Dahia P.L., Aguiar R.C., Alberta J., et al. PTEN is inversely correlated with the cell survival factor Akt/PKB and is inactivated via multiple mechanisms in haematological malignancies. Hum. Mol. Genet. 1999, 8:185-193.
89. Kharas M.G., Okabe R., Ganis J.J., et al. Constitutively active AKT depletes hematopoietic stem cells and induces leukemia in mice. Blood 2010, 115:1406-1415.
90. Juntilla M.M., Patil V.D., Calamito M., et al. AKT1 and AKT2 maintain hematopoietic stem cell function by regulating reactive oxygen species. Blood 2010, 115:4030-4038.
91. Warr M.R., Binnewies M., Flach J., et al. FOXO3A directs a protective autophagy program in haematopoietic stem cells. Nature 2013, 494:323-327.
92. Dasika G.K., Lin S.C., Zhao S., et al. DNA damage-induced cell cycle checkpoints and DNA strand break repair in development and tumorigenesis. Oncogene 1999, 18:7883-7899.
93. Sancar A., Lindsey-Boltz L.A., Unsal-Kacmaz K., Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 2004, 73:39-85.
94. Mao Z., Bozzella M., Seluanov A., Gorbunova V. Comparison of nonhomologous end joining and homologous recombination in human cells. DNA Repair (Amst) 2008, 7:1765-1771.
95. Elliott B., Jasin M. Double-strand breaks and translocations in cancer. Cell. Mol. Life Sci. 2002, 59:373-385.
96. Weinstock D.M., Elliott B., Jasin M. A model of oncogenic rearrangements: differences between chromosomal translocation mechanisms and simple double-strand break repair. Blood 2006, 107:777-780.
97. Weinstock D.M., Richardson C.A., Elliott B., Jasin M. Modeling oncogenic translocations: distinct roles for double-strand break repair pathways in translocation formation in mammalian cells. DNA Repair (Amst) 2006, 5:1065-1074.
98. Mohrin M., Bourke E., Alexander D., et al. Hematopoietic stem cell quiescence promotes error-prone DNA repair and mutagenesis. Cell Stem Cell 2010, 7:174-185.
99. Down J.D., Boudewijn A., van Os R., Thames H.D., Ploemacher R.E. Variations in radiation sensitivity and repair among different hematopoietic stem cell subsets following fractionated irradiation. Blood 1995, 86:122-127.
100. Passegue E., Wagers A.J., Giuriato S., Anderson W.C., Weissman I.L. Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J. Exp. Med. 2005, 202:1599-1611.
101. Seita J., Rossi D.J., Weissman I.L. Differential DNA damage response in stem and progenitor cells. Cell Stem Cell 2010, 7:145-147.