Hypoxia Differentially Modulates the Genomic Stability of Clinical-Grade ADSCs and BM-MSCs in Long-Term Culture

Stem Cells

Volumn 33, Issue 12, 2015, Pages 3608-3620

  Bigot, Nicolas ^a,b,c   Mouche, Audrey ^a,b,c   Preti, Milena ^c,d,e   Loisel, Séverine ^a,b,c   Renoud, Marie Laure ^c,d,e   Le Guével, Rémy ^b,f   Sensebé, Luc ^c,d,e   Tarte, Karin ^a,b,c,g   Pedeux, Rémy ^a,b,c  

^a INSERM U917   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c ETABLISSEMENT FRANÇAIS DU SANG   (France)

^d UNIVERSITÉ PAUL SABATIER   (France)

^e INSERM   (France)

^f UNIVERSITÉ DE RENNES 1   (France)

^g PONTCHAILLOU UNIVERSITY HOSPITAL   (France)

Author keywords

Adipose derived stromal cell; Bone marrow mesenchymal stromal stem cell; DNA repair; Hypoxia; Long term culture

Indexed keywords

5' NUCLEOTIDASE; ADAPALENE; BRCA1 PROTEIN; CD200 ANTIGEN; DOXORUBICIN; FIBROBLAST GROWTH FACTOR 2; HISTONE H2AX; HISTONE H2AX GAMMA; KU80 PROTEIN; MITOCHONDRIAL DNA; RAD51 PROTEIN; THY 1 ANTIGEN; TP53BP1 PROTEIN; UNCLASSIFIED DRUG;

ADIPOSE DERIVED STEM CELL; ADULT; ARTICLE; BODY MASS; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CELL DIFFERENTIATION; CELL SURVIVAL; CHROMOSOME ABERRATION; CONTROLLED STUDY; DNA DAMAGE; DNA END JOINING REPAIR; DNA REPAIR; DNA REPLICATION; EX VIVO STUDY; FEMALE; GENE CONTROL; GENOMIC INSTABILITY; GENOTOXICITY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOFLUORESCENCE; OSTEOBLAST; OXYGEN TENSION; PLASTIC SURGERY; PROTEIN EXPRESSION; RECOMBINATION REPAIR; STEM CELL CULTURE; WEIGHT REDUCTION; YOUNG ADULT; ADIPOSE TISSUE; CELL CULTURE TECHNIQUE; CELL HYPOXIA; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; TIME FACTOR;

ADIPOSE TISSUE; ADULT; CELL CULTURE TECHNIQUES; CELL HYPOXIA; DNA DAMAGE; FEMALE; GENOMIC INSTABILITY; HUMANS; MESENCHYMAL STROMAL CELLS; RECOMBINATIONAL DNA REPAIR; TIME FACTORS;

EID: 84983112969     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2195     Document Type: Article

References (52)

1. Pittenger MF, Mackay AM, Beck SC, et al., Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284: 143-147.
2. Ren G, Zhang L, Zhao X, et al., Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2008; 2: 141-150.
3. Ménard C, Pacelli L, Bassi G, et al., Clinical-grade mesenchymal stromal cells produced under various good manufacturing practice processes differ in their immunomodulatory properties: Standardization of immune quality controls. Stem Cells Dev 2013; 22: 1789-1801.
4. Wang Y, Chen X, Cao W, et al., Plasticity of mesenchymal stem cells in immunomodulation: Pathological and therapeutic implications. Nat Immunol 2014; 15: 1009-1016.
5. Tarte K, Gaillard J, Lataillade J-J, et al., Clinical-grade production of human mesenchymal stromal cells: Occurrence of aneuploidy without transformation. Blood 2010; 115: 1549-1553.
6. Sensebé L, Bourin P, Tarte K,. Good manufacturing practices production of mesenchymal stem/stromal cells. Hum Gene Ther 2011; 22: 19-26.
7. Chen Q, Fischer A, Reagan JD, et al., Oxidative DNA damage and senescence of human diploid fibroblast cells. Proc Natl Acad Sci USA 1995; 92: 4337-4341.
8. Wang Y, Zhang Z, Chi Y, et al., Long-term cultured mesenchymal stem cells frequently develop genomic mutations but do not undergo malignant transformation. Cell Death Dis 2013; 4: e950.
9. Estrada JC, Torres Y, Benguría A, et al., Human mesenchymal stem cell-replicative senescence and oxidative stress are closely linked to aneuploidy. Cell Death Dis 2013; 4: e691.
10. Li X-Y, Ding J, Zheng Z-H, et al., Long-term culture in vitro impairs the immunosuppressive activity of mesenchymal stem cells on T cells. Mol Med Report 2012; 6: 1183-1189.
11. Harding SM, Coackley C, Bristow RG,. ATM-dependent phosphorylation of 53BP1 in response to genomic stress in oxic and hypoxic cells. Radiother Oncol 2011; 99: 307-312.
12. Schuler N, Rübe CE,. Accumulation of DNA damage-induced chromatin alterations in tissue-specific stem cells: The driving force of aging? PLoS One 2013; 8: e63932.
13. Tang J, Cho NW, Cui G, et al., Acetylation limits 53BP1 association with damaged chromatin to promote homologous recombination. Nat Struct Mol Biol 2013; 20: 317-325
14. Jin Y, Kato T, Furu M, 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.
15. Tsai C-C, Chen Y-J, Yew T-L, 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.
16. Li T-S, Marbán E,. Physiological levels of reactive oxygen species are required to maintain genomic stability in stem cells. Stem Cells 2010; 28: 1178-1185.
17. Sugrue T, Lowndes NF, Ceredig R,. Hypoxia enhances the radio-resistance of mouse mesenchymal stromal cells. Stem Cells 2014; 32: 2188-2200.
18. Bindra RS, Schaffer PJ, Meng A, et al., Alterations in DNA repair gene expression under hypoxia: Elucidating the mechanisms of hypoxia-induced genetic instability. Ann N Y Acad Sci 2005; 1059: 184-195.
19. Bindra RS, Glazer PM,. Repression of RAD51 gene expression by E2F4/p130 complexes in hypoxia. Oncogene 2007; 26: 2048-2057.
20. Rodríguez-Jiménez FJ, Moreno-Manzano V, Lucas-Dominguez R, et al., Hypoxia causes downregulation of mismatch repair system and genomic instability in stem cells. Stem Cells 2008; 26: 2052-2062.
21. Bigot N, Guérillon C, Loisel S, et al., ING1b negatively regulates HIF1α protein levels in adipose-derived stromal cells by a SUMOylation-dependent mechanism. Cell Death Dis 2015; 6: e1612.
22. Ikura T, Tashiro S, Kakino A, et al., DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol Cell Biol 2007; 27: 7028-7040.
23. Zimmermann M, de Lange T,. 53BP1: Pro choice in DNA repair. Trends Cell Biol 2014; 24: 108-117.
24. Bonab MM, Alimoghaddam K, Talebian F, et al., Aging of mesenchymal stem cell in vitro. BMC Cell Biol 2006; 7: 14.
25. Grayson WL, Zhao F, Bunnell B, et al., Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun 2007; 358: 948-953.
26. Chacko SM, Ahmed S, Selvendiran K, et al., Hypoxic preconditioning induces the expression of prosurvival and proangiogenic markers in mesenchymal stem cells. Am J Physiol Cell Physiol 2010; 299: C1562-C1570.
27. Oliver L, Hue E, Séry Q, et al., Differentiation related response to DNA breaks in human mesenchymal stem cells. Stem Cells 2013; 31: 800-807.
28. Torsvik A, Røsland GV, Svendsen A, et al., Spontaneous malignant transformation of human mesenchymal stem cells reflects cross-contamination: Putting the research field on track-Letter. Cancer Res 2010; 70: 6393-6396.
29. Oliveira PH, Boura JS, Abecasis MM, et al., Impact of hypoxia and long-term cultivation on the genomic stability and mitochondrial performance of ex vivo expanded human stem/stromal cells. Stem Cell Res 2012; 9: 225-236.
30. Nunes-Alves C,. Viral infection: Manipulation of DNA repair pathways. Nat Rev Microbiol 2014; 12: 530-530.
31. Doucet C, Ernou I, Zhang Y, et al., Platelet lysates promote mesenchymal stem cell expansion: A safety substitute for animal serum in cell-based therapy applications. J Cell Physiol 2005; 205: 228-236.
32. Bura A, Planat-Benard V, Bourin P, et al., Phase I trial: The use of autologous cultured adipose-derived stroma/stem cells to treat patients with non-revascularizable critical limb ischemia. Cytotherapy 2014; 16: 245-257.
33. Kumareswaran R, Ludkovski O, Meng A, et al., Chronic hypoxia compromises repair of DNA double-strand breaks to drive genetic instability. J Cell Sci 2012; 125: 189-199.
34. Bencokova Z, Kaufmann MR, Pires IM, et al., ATM activation and signaling under hypoxic conditions. Mol Cell Biol 2009; 29: 526-537.
35. Doil C, Mailand N, Bekker-Jensen S, et al., RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 2009; 136: 435-446.
36. Mallette FA, Mattiroli F, Cui G, et al., RNF8- and RNF168-dependent degradation of KDM4A/JMJD2A triggers 53BP1 recruitment to DNA damage sites. EMBO J 2012; 31: 1865-1878.
37. Perez-Oliva AB, Lachaud C, Szyniarowski P, et al., USP45 deubiquitylase controls ERCC1-XPF endonuclease-mediated DNA damage responses. EMBO J 2015; 34: 326-343.
38. Sharma N, Zhu Q, Wani G, et al., USP3 counteracts RNF168 via deubiquitinating H2A and γH2AX at lysine 13 and 15. Cell Cycle 2013; 13: 106-114.
39. Gudjonsson T, Altmeyer M, Savic V, et al., TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes. Cell 2012; 150: 697-709.
40. Stiff T, O'Driscoll M, Rief N, et al., ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res 2004; 64: 2390-2396.
41. 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.
42. Harding SM, Bristow RG,. Discordance between phosphorylation and recruitment of 53BP1 in response to DNA double-strand breaks. Cell Cycle 2012; 11: 1432-1444.
43. Galanty Y, Belotserkovskaya R, Coates J, et al., Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 2009; 462: 935-939.
44. Huyen Y, Zgheib O, Ditullio RA, et al., Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 2004; 432: 406-411.
45. 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.
46. Bindra RS, Gibson SL, Meng A, et al., Hypoxia-induced down-regulation of BRCA1 expression by E2Fs. Cancer Res 2005; 65: 11597-11604.
47. Koshiji M, To KK-W, Hammer S, et al., HIF-1alpha induces genetic instability by transcriptionally downregulating MutSalpha expression. Mol Cell 2005; 17: 793-803.
48. Santos Dos 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.
49. Zheng W, Khrapko K, Coller HA, et al., Origins of human mitochondrial point mutations as DNA polymerase gamma-mediated errors. Mutat Res 2006; 599: 11-20.
50. Alison MR, McDonald SAC, Lin WR, et al., Protection of mitochondrial genome integrity: A new stem cell property? Hepatology 2010; 51: 354-354.
51. Cho YM, Kim JH, Kim M, et al., Mesenchymal stem cells transfer mitochondria to the cells with virtually no mitochondrial function but not with pathogenic mtDNA mutations. PLoS One 2012; 7: e32778.
52. Baines HL, Turnbull DM, Greaves LC,. Human stem cell aging: Do mitochondrial DNA mutations have a causal role? Aging Cell 2014; 13: 201-205.