Hypoxia enhances the radioresistance of mouse mesenchymal stromal cells

Stem Cells

Volumn 32, Issue 8, 2014, Pages 2188-2200

  Sugrue, Tara ^a   Lowndes, Noel F ^a   Ceredig, Rhodri ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

DNA damage response; DNA repair; Hypoxia; Irradiation; Mesenchymal stromal cells

Indexed keywords

DNA LIGASE IV; HISTONE H2AX; HYPOXIA INDUCIBLE FACTOR 1ALPHA; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN KINASE C; RAD51 PROTEIN; UNCLASSIFIED DRUG; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL GROWTH; CELL HYPOXIA; CELL PROLIFERATION; CELL SIZE; CONTROLLED STUDY; DNA DAMAGE CHECKPOINT; DNA REPAIR; DOUBLE STRANDED DNA BREAK; G2 PHASE CELL CYCLE CHECKPOINT; GENOTOXICITY; HISTONE PHOSPHORYLATION; HYPOXIA; IN VITRO STUDY; LONG TERM SURVIVAL; MESENCHYMAL STROMA CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RADIOSENSITIVITY; RECEPTOR UPREGULATION; S PHASE CELL CYCLE CHECKPOINT; WHOLE BODY RADIATION; ANIMAL; C57BL MOUSE; DNA DAMAGE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; METABOLISM; PHYSIOLOGY; RADIATION DOSE; RADIATION RESPONSE; TUMOR MICROENVIRONMENT; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL HYPOXIA; DNA DAMAGE; DNA REPAIR; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE KNOCKDOWN TECHNIQUES; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; RADIATION TOLERANCE; RNA, SMALL INTERFERING; TUMOR MICROENVIRONMENT;

EID: 84904437150     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1683     Document Type: Article

References (87)

1. Friedenstein AJ, Deriglasova UF, Kulagina NN, et al. Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol 1974; 29: 83-92.
2. Bianco P, Riminucci M, Gronthos S, et al. Bone marrow stromal stem cells: Nature, biology, and potential applications. Stem Cells 2001; 19: 180-192.
3. Morikawa S, Mabuchi Y, Kubota Y, et al. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J Exp Med 2009; 206: 2483-2496.
4. Tolar J, Le Blanc K, Keating A, et al. Concise review: Hitting the right spot with mesenchymal stromal cells. Stem Cells 2010; 28: 1446-1455.
5. Wilson A, Trumpp A,. Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol 2006; 6: 93-106.
6. Celso CL, Scadden DT,. The hematopoietic stem cell niche at a glance. J Cell Sci 2011; 124: 3529-3535.
7. Wang LD, Wagers AJ,. Dynamic niches in the origination and differentiation of hematopoietic stem cells. Nat Rev Mol Cell Biol 2011; 12: 643-655.
8. Mercier FE, Ragu C, Scadden DT,. The bone marrow at the crossroads of blood and immunity. Nat Rev Immunol 2011; 12: 49-60.
9. Hanahan D, Coussens LM,. Accessories to the crime: Functions of cells recruited to the tumor microenvironment. Cancer Cell 2012; 21: 309-322.
10. Hanahan D, Weinberg RA,. Hallmarks of cancer: The next generation. Cell 2011; 144: 646-674.
11. Bergfeld SA, DeClerk YA,. Bone marrow-derived mesenchymal stem cells and the tumor microenvironment. Cancer Metastasis Rev 2010; 29: 249-261.
12. Kraman M, Bambrough PJ, Arnold JN, et al. Suppression of anti-tumor immunity by stromal cells expressing fibroblast activation protein-α. Science 2010; 330: 827-830.
13. Kidd S, Spaeth E, Watson K, et al. Origins of the tumor microenvironment: Quantitative assessment of adipose-derived and bone marrow-derived stroma. PLoS One 2012; 7: e30563.
14. Marigo I, Dazzi F,. The immunomodulatory properties of mesenchymal stem cells. Semin Immunopathol 2011; 33: 593-602.
15. Eliasson P, Jönsson JI,. The hematopoietic stem cell niche: Low in oxygen but a nice place to be. J Cell Physiol 2010; 222: 17-22.
16. Moyheldin A, Garzón-Muvdi T, Quiñones-Hinojosa A,. Oxygen in stem cell biology: A critical component of the stem cell niche. Cell Stem Cell 2010; 7: 150-161.
17. Vaupel P,. Tumor microenvironmental physiology and its implications for radiation oncology. Semin Radiat Oncol 2004; 14: 198-206.
18. Vaupel P, Mayer A, Höckel M,. Tumor hypoxia and malignant progression. Methods Enzymol 2004; 381: 335-354.
19. Ruan K, Song G, Ouyang G,. Role of hypoxia in the hallmarks of human cancer. J Cell Biochem 2009; 107: 1053-1062.
20. Heddleston JM, Li Z, Lathla JD, et al. Hypoxia inducible factors in cancer stem cells. Br J Cancer 2010; 102: 789-795.
21. Semenza GL,. HIF-1: Mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol 2000; 88: 1474-1480.
22. Ke Q, Costa M,. Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 2006; 70: 1469-1480.
23. Benizri E, Ginouvès A, Berra E,. The magic of the hypoxia-signaling cascade. Cell Mol Life Sci 2008; 65: 1133-1149.
24. Unruh A, Ressel A, Mohamed HG, et al. The hypoxia-inducible factor-1α is a negative factor for tumor therapy. Oncogene 2003; 22: 3213-3220.
25. Bertout JA, Patel SA, Simon MC,. The impact of O2 availability on human cancer. Nat Rev Cancer 2008; 8: 967-975.
26. Ward JF,. DNA damage produced by ionizing radiation in mammalian cells: Identities, mechanisms of formation, and reparability. Prog Nucleic Acid Res Mol Biol 1988; 35: 95-125.
27. Ciccia A, Elledge SJ,. The DNA Damage Response: Making it safe to play with knives. Mol Cell 2010; 40: 179-204.
28. Kastan MB, Bartek J,. Cell cycle checkpoints and cancer. Nature 2004; 432: 316-323.
29. Harper JW, Elledge SJ,. The DNA damage response: Ten years after. Mol Cell 2007; 28: 739-745.
30. Hammond EM, Denko NC, Dorie MJ, et al. Hypoxia links ATR and p53 through replication arrest. Mol Cell Biol 2002; 22: 1834-1843.
31. Hammond EM, Dorie MJ, Giaccia AJ,. ATR/ATM targets are phosphorylated by ATR in response to hypoxia and ATM in response to reoxygenation. J Biol Chem 2003; 278: 12207-12213.
32. Gibson SL, Bindra RS, Glazer PM,. Hypoxia-induced phosphorylation of Chk2 in an ataxia telangiectasia mutated-dependent manner. Cancer Res 2005; 65: 10734-10741.
33. Gibson SL, Bindra RS, Glazer PM,. CHK2-dependent phosphorylation of BRCA1 in hypoxia. Radiat Res 2006; 166: 646-651.
34. Bouquet F, Ousset M, Biard D, et al. A DNA-dependent stress response involving DNA-PK occurs in hypoxic cells and contributes to cellular adaptation to hypoxia. J Cell Sci 2011; 124: 1943-1951.
35. Wrann S, Kaufmann MR, Wirthner R, et al. HIF mediated and DNA damage independent histone H2AX phosphorylation in chronic hypoxia. Biol Chem 2013; 394: 519-528.
36. Bristow RG, Hill RP,. Hypoxia, DNA repair and genetic instability. Nat Rev Cancer 2008; 8: 180-192.
37. Rohwer N, Zasada C, Kempa S, et al. The growing complexity of HIF-1α's role in tumorigenesis: DNA repair and beyond. Oncogene 2013; 32: 3569-3576.
38. Anklesaria P, Kase K, Glowacki J, et al. Engraftment of a clonal bone marrow stromal cell line in vivo stimulates hematopoietic recovery from total body irradiation. PNAS 1987; 84: 7681-7685.
39. Dickhut A, Schwerdtfeger R, Kuklick L, et al. Mesenchymal stem cells obtained after bone marrow transplantation or peripheral blood stem cell transplantation originate from host tissue. Ann Hematol 2005; 84: 722-727.
40. Rieger K, Marinets O, Fietz T, et al. Mesenchymal stem cells remain of host origin even a long time after allogeneic peripheral blood stem cell or bone marrow transplantation. Exp Hematol 2005; 33: 605-611.
41. Chen MF, Lin CT, Chen WC, et al. The sensitivity of human mesenchymal stem cells to ionizing radiation. Int J Radiat Oncol Biol Phys 2006; 66: 244-253.
42. Mugurama Y, Yahata T, Miyatake H, et al. Reconstitution of the functional human hematopoietic microenvironment derived from human mesenchymal stem cells in the murine bone marrow compartment. Blood 2006; 107: 1878-1887.
43. Bartsch K, Al-Ali H, Reinhardt A, et al. Mesenchymal stem cells remain host-derived independent of the source of the stem-cell graft and conditioning regimen used. Transplantation 2009; 87: 217-221.
44. Sugrue T, Brown JAL, Lowndes NF, et al. Multiple facets of the DNA Damage Response contribute to the radio-resistance of mouse mesenchymal stromal cell lines. Stem Cells 2013; 31: 137-145.
45. Duffy MM, Pindjakova J, Hanley SA, et al. Mesenchymal stem cell inhibition of T-helper 17 cell-differentiation is triggered by cell-cell contact and mediated by prostaglandin E2 via the EP4 receptor. Eur J Immunol 2011; 41: 2840-2851.
46. Pierce AJ, Johnson RD, Thompson LH, et al. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev 1999; 13: 2633-2638.
47. Nakanishi K, Cavallo F, Brunet E, et al. Homologous recombination assay for interstrand cross-link repair. Methods Mol Biol 2011; 745: 283-291.
48. Sotiropoulou PA, Candi A, Mascré G, et al. Bcl-2 and accelerated DNA repair mediates resistance of hair follicle bulge stem cells to DNA-damage-induced cell death. Nat Cell Biol 2010; 12: 572-582.
49. Dos Santos F, Andrade PZ, Boura JS, et al. Ex vivo expansion of human mesenchymal stem cells: A more effective cell proliferation kinetics and metabolism under hypoxia. J Cell Physiol 2010; 223: 27-35.
50. Tsai CC, Chen YJ, Yew TL, et al. Hypoxia inhibits senescence and maintains mesenchymal stem cell properties through down-regulation of E2A-p21 by HIF-TWIST. Blood 2011; 117: 459-469.
51. Xu B, Kim S-T, Lim D-S, et al. Two molecularly distinct G2/M checkpoints are induced by ionizing irradiation. Mol Cell Biol 2002; 22: 1049-1059.
52. Bartek J, Lukas J,. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 2003; 3: 421-429.
53. Rogakou EP, Pilch DR, Orr AH, et al. DNA double-stranded breaks induce histone H2AX phosphorylation on Serine 139. J Biol Chem 1998; 273: 5858-5868.
54. Fernandez-Capetillo O, Lee A, Nussenzweig M, et al. H2AX: The histone guardian of the genome. DNA Repair 2004; 3: 959-967.
55. Bonner WM, Redon CE, Dickey JS, et al. γ H2AX and cancer. Nat Rev Cancer 2008; 8: 957-967.
56. Sugrue T, Lowndes NF, Ceredig Rh,. Mesenchymal stromal cells: Radio-resistant members of the bone marrow. Immunol Cell Biol 2013; 91: 5-11.
57. Tsai CC, Yew TL, Yang DC, et al. Benefits of hypoxic culture on bone marrow multipotent stromal cells. Am J Blood Res 2012; 2: 148-159.
58. Tsai CC, Su PF, Huang YF, et al. Oct4 and Nanog directly regulate Dnmt1 to maintain self-renewal and undifferentiated state in mesenchymal stem cells. Mol Cell 2012; 47: 169-182.
59. Liu L, Gao J, Yuan Y, et al. Hypoxia preconditioned human adipose derived mesenchymal stem cells enhance angiogenic potential via secretion of increased VEGF and bFGF. Cell Biol Int 2013; 37: 551-560.
60. Jin Y, Kato T, Furu N, et al. Mesenchymal stem cells cultured under hypoxia escape from senescence via down-regulation of p16 and extracellular signal regulated kinase. Biochem Biophys Res Commun 2010; 391: 1471-1476.
61. Basciano L, Nemos C, Foliguet B, et al. Long term culture of mesenchymal stem cells in hypoxia promotes a genetic program maintaining their undifferentiated and multipotent status. BMC Cell Biol 2011; 12: 12.
62. Bindra RS, Crosby ME, Glazer PM,. Regulation of DNA repair in hypoxic cancer cells. Cancer Metastasis Rev 2007; 26: 249-260.
63. Koshiji M, Kageyama Y, Pete EA, et al. HIF-1 alpha induces cell cycle arrest by functionally counteracting Myc. EMBO J 2004; 23: 1949-1956.
64. Welford SM, Giaccia AJ,. Hypoxia and senescence: The impact of oxygenation on tumor suppression. Mol Cancer Res 2011; 9: 538-544.
65. Bindra RS, Schaffer PJ, Meng A, et al. Down-regulation of Rad51 and decreased homologous recombination in hypoxic cancer cells. Mol Cell Biol 2004; 24: 8504-8518.
66. Chan N, Koritzinsky M, Zhao H, et al. Chronic hypoxia decreases synthesis of homologous recombination proteins to offset chemoresistance and radioresistance. Cancer Res 2008; 68: 605-614.
67. Meng AX, Jalali F, Cuddihy A, et al. Hypoxia down-regulates DNA double strand break repair gene expression in prostate cancer cells. Radiother Oncol 2005; 76: 168-176.
68. Um JH, Kang CD, Bae JH, et al. Association of DNA-dependent protein kinase with hypoxia inducible factor-1 and its implication in resistance to anti-cancer drugs in hypoxic tumor cells. Exp Mol Med 2004; 36: 233-242.
69. Hall EJ, Giacci AJ,. Radiobiology for the Radiologist. 6th ed. Philadelphia, PA: Lippincott Williams & Wilkins, 2006: 1-546.
70. Sugiyama T, Kohara H, Noda M, et al. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 2006; 25: 977-988.
71. Méndez-Ferrer S, Michinura TV, Ferraro F, et al. Mesenchymal and hematopoietic stem cells form a unique bone marrow niche. Nature 2010; 466: 829-834.
72. Omatsu Y, Sugiyama T, Kohara H, et al. The essential functions of adipo-osteogenic progenitors as the hematopoietic stem and progenitor cell niche. Immunity 2010; 33: 387-399.
73. Park D, Spencer JA, Koh BI, et al. Endogenous bone marrow MSCs are dynamic, fate-restricted participants in bone maintenance and regeneration. Cell Stem Cell 2012; 10: 259-272.
74. Roberts EW, Deonarine A, Jones JO, et al. Depletion of stromal cells expressing fibroblast activation protein-α from skeletal muscle and bone marrow results in cachexia and anemia. J Exp Med 2013; 210: 1137-1151.
75. Mauch P, Constine L, Greenberger J, et al. Hematopoietic stem cell compartment: Acute and late effects of radiation therapy and chemotherapy. Int J Radiat Oncol Biol Phys 1995; 31: 1319-1339.
76. Copelan EA,. Hematopoietic stem-cell transplantation. N Engl J Med 2006; 354: 1813-1826.
77. Direkze NC, Hodivala-Dilke K, Jeffery R, et al. Bone marrow contribution to tumor-associated myofibroblasts and fibroblasts. Cancer Res 2004; 64: 8492-8495.
78. Kucerova L, Matuskova M, Pastorakova A, et al. Cytosine deaminase expressing human mesenchymal stem cells mediated tumor regression in melanoma bearing mice. J Gene Med 2008; 10: 1071-1082.
79. Wang H, Cao F, De A, et al. Trafficking mesenchymal stem cell engraftment and differentiation in tumor-bearing mice by bioluminescence imaging. Stem Cells 2009; 27: 1548-1558.
80. Quante M, Tu SP, Tomita H, et al. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 2011; 19: 257-272.
81. Jung Y, Kim JK, Shiozawa Y, et al. Recruitment of mesenchymal stem cells into prostate tumors promotes metastasis. Nat Commun 2013; 4: 1795.
82. Ramasamy R, Lam EW, Soeiro I, et al. Mesenchymal stem cells inhibit proliferation and apoptosis of tumor cells: Impact on in vivo tumor growth. Leukemia 2007; 21: 304-310.
83. Vianello F, Villanova F, Tisato V, et al. Bone marrow mesenchymal stromal cells non-selectively protect chronic myeloid leukemia cells from imatinib-induced apoptosis via the CXCR4/CXCL12 axis. Haematologica 2010; 95: 1081-1089.
84. Balakrishnan K, Burger JA, Quiroga MP, et al. Influence of bone marrow stromal microenvironment on forodesine-induced responses in CLL primary cells. Blood 2010; 116: 1083-1091.
85. Gammon L, Biddle A, Heywood HK, et al. Sub-sets of cancer stem cells differ intrinsically in their patterns of oxygen metabolism. PLoS One 2013; 8: e62493.
86. Sermeus A, Rebucci M, Fransolet M, et al. Differential effect of hypoxia on etoposide-induced DNA damage response and p53 regulation in different cell types. J Cell Physiol 2013; 228: 2365-2376.
87. Strese S, Fryknäs M, Larsson R, et al. Effects of hypoxia on cancer cell line chemosensitivity. BMC Cancer 2013; 13: 331.