Chromosomal stability of mesenchymal stromal cells during in vitro culture

Cytotherapy

Volumn 18, Issue 3, 2016, Pages 336-343

  Stultz, Brian G ^a   McGinnis, Kathleen ^a   Thompson, Elaine E ^a   Lo Surdo, Jessica L ^a   Bauer, Steven R ^a   Hursh, Deborah A ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

genomic stability; mesenchymal stromal cells; MSC; SKY; spectral karyotyping

Indexed keywords

ARTICLE; CELL EXPANSION; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATION; CLONAL CELL LINE; GENETIC STABILITY; HUMAN; HUMAN CELL; IN VITRO STUDY; KARYOTYPING; MESENCHYMAL STROMA CELL; METAPHASE; PRIORITY JOURNAL; SPECTRAL KARYOTYPING; ADULT; BIOLOGICAL THERAPY; BONE MARROW CELL; CELL CLONE; CELL CULTURE; CELL CULTURE TECHNIQUE; CYTOLOGY; FEMALE; MALE; METABOLISM; PHYSIOLOGY; YOUNG ADULT;

ADULT; BONE MARROW CELLS; CELL CULTURE TECHNIQUES; CELL- AND TISSUE-BASED THERAPY; CELLS, CULTURED; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATIONS; CLONE CELLS; FEMALE; HUMANS; KARYOTYPING; MALE; MESENCHYMAL STROMAL CELLS; YOUNG ADULT;

EID: 84954511057     PISSN: 14653249     EISSN: 14772566     Source Type: Journal    
DOI: 10.1016/j.jcyt.2015.11.017     Document Type: Article

References (43)

1. Dominici M, Le BK, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for CellularTherapy position statement. Cytotherapy 2006;8:315-17.
2. Casiraghi F, Remuzzi G, Abbate M, Perico N. Multipotent mesenchymal stromal cell therapy and risk of malignancies. Stem Cell Rev 2013;9:65-79.
3. Moon SH, Kim JS, Park SJ, Lim JJ, Lee HJ, Lee SM, et al. Effect of chromosome instability on the maintenance and differentiation of human embryonic stem cells in vitro and in vivo. Stem Cell Res 2011;6:50-9.
4. Sundaram S, One J, Siewert J, Teodosescu S, Zhao L, Dimitrievska S, et al. Tissue-engineered vascular grafts created from human induced pluripotent stem cells. Stem CellsTransl Med 2014;3:1535-43.
5. Wang Y, Zhang Z, Chi Y, Zhang Q, Xu F, Yang Z, et al. Long-term cultured mesenchymal stem cells frequently develop genomic mutations but do not undergo malignant transformation. Cell Death Dis 2013;4:e950.
6. Bellayr IH, Catalano JG, Lababidi S, Yang AX, Lo Surdo JL, Bauer SR, et al. Gene markers of cellular aging in human multipotent stromal cells in culture. Stem Cell Res Ther 2014;5:59.
7. Lo Surdo JL, Millis BA, Bauer SR. Automated microscopy as a quantitative method to measure differences in adipogenic differentiation in preparations of human mesenchymal stromal cells. Cytotherapy 2013;15:1527-40.
8. Lo Surdo JL, Bauer SR. Quantitative approaches to detect donor and passage differences in adipogenic potential and clonogenicity in human bone marrow-derived mesenchymal stem cells. Tissue Eng Part C Methods 2012;18:877-89.
9. Lynch PJ, Thompson EE, McGinnis K, Rovira Gonzalez YI, Lo Surdo JL, Bauer SR, et al. Chromatin changes at the PPAR-gamma2 promoter during bone marrow-derived multipotent stromal cell culture correlate with loss of gene activation potential. Stem Cells 2015;10.
10. Mindaye ST, Ra M, Lo Surdo JL, Bauer SR, Alterman MA. Global proteomic signature of undifferentiated human bone marrow stromal cells: evidence for donor-to-donor proteome heterogeneity. Stem Cell Res 2013;11:793-805.
11. Mindaye ST, Ra M, Lo Surdo JL, Bauer SR, Alterman MA. Improved proteomic profiling of the cell surface of cultureexpanded human bone marrow multipotent stromal cells. J Proteomics 2013;78:1-14.
12. Nazarov C, Lo Surdo J, Bauer SR, Wei CH. Assessment of immunosuppressive activity of human mesenchymal stem cells using murine antigen specific CD4 and CD8T cells in vitro. Stem Cell Res Ther 2013;4:128.
13. Foudah D, Redaelli S, Donzelli E, Bentivegna A, Miloso M, Dalpra L, et al. Monitoring the genomic stability of in vitro cultured rat bone-marrow-derived mesenchymal stem cells. Chromosome Res 2009;17:1025-39.
14. Miura M, Miura Y, Padilla-Nash HM, Molinolo AA, Fu B, Patel V, et al. Accumulated chromosomal instability in murine bone marrow mesenchymal stem cells leads to malignant transformation. Stem Cells 2006;24:1095-103.
15. Ben-David U, Mayshar Y, Benvenisty N. Large-scale analysis reveals acquisition of lineage-specific chromosomal aberrations in human adult stem cells. Cell Stem Cell 2011;9:97-102.
16. Capelli C, Pedrini O, Cassina G, Spinelli O, Salmoiraghi S, Golay J, et al. Frequent occurrence of non-malignant genetic alterations in clinical grade mesenchymal stromal cells expanded for cell therapy protocols. Haematologica 2014;99:e94-7.
17. Froelich K, Mickler J, Steusloff G, Technau A, Ramos TM, Scherzed A, et al. Chromosomal aberrations and deoxyribonucleic acid single-strand breaks in adipose-derived stem cells during long-term expansion in vitro. Cytotherapy 2013;15:767-81.
18. Nikitina VA, Chausheva AI, Zhanataev AK, Osipova EY, Durnev AD, Bochkov NP. Assessment of DNA damage in human bone marrow cells and multipotent mesenchymal stromal cells. Bull Exp Biol Med 2011;151:550-2.
19. Tarte K, Gaillard J, Lataillade JJ, Fouillard L, Becker M, Mossafa H, et al. Clinical-grade production of human mesenchymal stromal cells: occurrence of aneuploidy without transformation. Blood 2010;115:1549-53.
20. Bernardo ME, Zaffaroni N, Novara F, Cometa AM, Avanzini MA, Moretta A, et al. Human bone marrow derived mesenchymal stem cells do not undergo transformation after long-term in vitro culture and do not exhibit telomere maintenance mechanisms. Cancer Res 2007;67:9142-9.
21. Garcia S, Bernad A, Martin MC, Cigudosa JC, Garcia-Castro J, de la Fuente R. Pitfalls in spontaneous in vitro transformation of human mesenchymal stem cells. Exp Cell Res 2010;316: 1648-50.
22. Torsvik A, Rosland GV, Svendsen A, Molven A, Immervoll H, McCormack E, et al. Spontaneous malignant transformation of human mesenchymal stem cells reflects cross-contamination: putting the research field on track [letter]. Cancer Res 2010;70:6393-6.
23. Pan Q, Fouraschen SM, de Ruiter PE, Dinjens WN, Kwekkeboom J, Tilanus HW, et al. Detection of spontaneous tumorigenic transformation during culture expansion of human mesenchymal stromal cells. Exp Biol Med (Maywood) 2014;239:105-15.
24. Schrock E, du Manoir S, Veldman T, Schoell B, Wienberg J, Ferguson-Smith MA, et al. Multicolor spectral karyotyping of human chromosomes. Science 1996;273:494-7.
25. McNeil N, Ried T. Novel molecular cytogenetic techniques for identifying complex chromosomal rearrangements: technology and applications in molecular medicine. Expert Rev Mol Med 2000;1-14:2000.
26. Shaffer LG, Slovak ML, Campbell LJ. ISCN 2009 An international system for human cytogenetic nomenclature. Springer-Verlag: Human Genetics; 2009. p. 603-4.
27. Barkholt L, Flory E, Jekerle V, Lucas-Samuel S, Ahnert P, Bisset L, et al. Risk of tumorigenicity in mesenchymal stromal cell-based therapies-bridging scientific observations and regulatory viewpoints. Cytotherapy 2013;15:753-9.
28. Nestor CE, Ottaviano R, Reinhardt D, Cruickshanks HA, Mjoseng HK, McPherson RC, et al. Rapid reprogramming of epigenetic and transcriptional profiles in mammalian culture systems. Genome Biol 2015;16:11.
29. Baker DE, Harrison NJ, Maltby E, Smith K, Moore HD, Shaw PJ, et al. Adaptation to culture of human embryonic stem cells and oncogenesis in vivo. Nat Biotechnol 2007;25:207-15.
30. Enver T, Soneji S, Joshi C, Brown J, Iborra F, Orntoft T, et al. Cellular differentiation hierarchies in normal and cultureadapted human embryonic stem cells. Hum Mol Genet 2005;14:3129-40.
31. Binato R, de Souza FT, Lazzarotto-Silva C, Du RB, Mencalha A, Pizzatti L, et al. Stability of human mesenchymal stem cells during in vitro culture: considerations for cell therapy. Cell Prolif 2013;46:10-22.
32. Redaelli S, Bentivegna A, Foudah D, Miloso M, Redondo J, Riva G, et al. From cytogenomic to epigenomic profiles: Monitoring the biologic behavior of in vitro cultured human bone marrow mesenchymal stem cells. Stem Cell Res Ther 2012;3:47.
33. Dahl JA, Duggal S, Coulston N, Millar D, Melki J, Shahdadfar A, et al. Genetic and epigenetic instability of human bone marrow mesenchymal stem cells expanded in autologous serum or fetal bovine serum. Int J Dev Biol 2008;52:1033-42.
34. Estrada JC, Torres Y, Benguria A, Dopazo A, Roche E, Carrera-Quintanar L, et al. Human mesenchymal stem cell-replicative senescence and oxidative stress are closely linked to aneuploidy. Cell Death Dis 2013;4:e691.
35. Ganguly BB. Cell division, chromosomal damage and micronucleus formation in peripheral lymphocytes of healthy donors: related to donor's age. Mutat Res 1993;295:135-48.
36. Wojda A, Zietkiewicz E, Mossakowska M, Pawlowski W, Skrzypczak K, Witt M. Correlation between the level of cytogenetic aberrations in cultured human lymphocytes and the age and gender of donors. J Gerontol A Biol Sci Med Sci 2006;61:763-72.
37. Fan YS, Siu VM, Jung JH, Xu J. Sensitivity of multiple color spectral karyotyping in detecting small interchromosomal rearrangements. GenetTest 2000;4:9-14.
38. Nordgren A, Heyman M, Sahlen S, Schoumans J, Soderhall S, Nordenskjold M, et al. Spectral karyotyping and interphase FISH reveal abnormalities not detected by conventional G-banding. Implications for treatment stratification of childhood acute lymphoblastic leukaemia: detailed analysis of 70 cases. Eur J Haematol 2002;68:31-41.
39. Imataka G, Arisaka O. Chromosome analysis using spectral karyotyping (SKY). Cell Biochem Biophys 2012;62:13-17.
40. Lee C, Gisselsson D, Jin C, Nordgren A, Ferguson DO, Blennow E, et al. Limitations of chromosome classification by multicolor karyotyping. Am J Hum Genet 2001;68:1043-7.
41. Muntion S, Sanchez-Guijo FM, Carrancio S, Villaron E, Lopez O, Diez-Campelo M, et al. Optimisation of mesenchymal stromal cells karyotyping analysis: implications for clinical use. Transfus Med 2012;22:122-7.
42. Meza-Zepeda LA, Noer A, Dahl JA, Micci F, Myklebost O, Collas P. High-resolution analysis of genetic stability of human adipose tissue stem cells cultured to senescence. J Cell Mol Med 2008;12:553-63.
43. Sensebe L, Tarte K, Galipeau J, Krampera M, Martin I, Phinney DG, et al. Limited acquisition of chromosomal aberrations in human adult mesenchymal stromal cells. Cell Stem Cell 2012;10:9-10.