Chromosomal Abnormalities in Embryonic and Somatic Stem Cells

Cytogenetic and Genome Research

Volumn 147, Issue 1, 2015, Pages 1-9

  Rebuzzini, Paola ^a   Zuccotti, Maurizio ^c   Redi, Carlo A ^a,b   Garagna, Silvia ^a  

^a UNIVERSITY OF PAVIA   (Italy)

^b FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

^c UNIVERSITY OF PARMA   (Italy)

Author keywords

Aneuploidy; Chromosome instability; Stem cells

Indexed keywords

COMPLEMENT;

ANEUPLOIDY; CELLS BY BODY ANATOMY; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATION; EMBRYO CELL; EMBRYONIC STEM CELL; ENDOTHELIAL PROGENITOR CELL; GENOMIC INSTABILITY; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN EMBRYONIC STEM CELL; IN VITRO STUDY; KARYOTYPING; MESENCHYMAL STROMA CELL; MOUSE EMBRYONIC STEM CELL; NEURAL STEM CELL; NONHUMAN; PARTHENOGENETIC EMBRYONIC STEM CELL; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW; SOMATIC CELL; SOMATIC STEM CELL; SPECTRAL KARYOTYPING; STEM CELL; STEM CELL CULTURE; TRISOMY; UMBILICAL CORD BLOOD; ANIMAL; CELL LINE; CHROMOSOME BANDING PATTERN; COMPARATIVE GENOMIC HYBRIDIZATION; FLUORESCENCE IN SITU HYBRIDIZATION; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MOUSE; PATHOLOGY;

ANIMALS; CELL LINE; CHROMOSOME ABERRATIONS; CHROMOSOME BANDING; COMPARATIVE GENOMIC HYBRIDIZATION; EMBRYONIC STEM CELLS; ENDOTHELIAL PROGENITOR CELLS; HEMATOPOIETIC STEM CELLS; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; INDUCED PLURIPOTENT STEM CELLS; KARYOTYPING; MESENCHYMAL STROMAL CELLS; MICE; NEURAL STEM CELLS;

EID: 84947808134     PISSN: 14248581     EISSN: 1424859X     Source Type: Journal    
DOI: 10.1159/000441645     Document Type: Review

References (132)

1. Aasen T, Raya A, Barrero MJ, Garreta E, Consiglio A, et al: Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat Biotechnol 26: 1276-1284 (2008).
2. Angelo PC, Ferreira AC, Fonseca VD, Frade SP, Ferreira CS, et al: Cryopreservation does not alter karyotype, multipotency, or NANOG/ SOX2 gene expression of amniotic fluid mesenchymal stem cells. Genet Mol Res 11: 1002-1012 (2012).
3. Bai Y, Hu Q, Li X, Wang Y, Lin C, et al: Telomerase immortalization of human neural progenitor cells. Neuroreport 15: 245-249 (2004).
4. Bajada S, Mazakova I, Richardson JB, Ashammakhi N: Updates on stem cells and their applications in regenerative medicine. J Tissue Eng Regen Med 2: 169-183 (2008).
5. Baker DE, Harrison NJ, Maltby E, Smith K, Moore HD, et al: Adaptation to culture of human embryonic stem cells and oncogenesis in vivo. Nat Biotechnol 25: 207-215 (2007).
6. Ben-David U, Benvenisty N: High prevalence of evolutionarily conserved and species-specific genomic aberrations in mouse pluripotent stem cells. Stem Cells 30: 612-622 (2012).
7. Ben-David U, Mayshar Y, Benvenisty N: Largescale analysis reveals acquisition of lineagespecific chromosomal aberrations in human adult stem cells. Cell Stem Cell 9: 97-102 (2011).
8. Ben-David U, Kopper O, Benvenisty N: Expanding the boundaries of embryonic stem cells. Cell Stem Cell 10: 666-677 (2012).
9. Bernardo ME, Zaffaroni N, Novara F, Cometa AM, Avanzini MA, 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 67: 9142-9149 (2007).
10. Blum B, Benvenisty N: The tumorigenicity of diploid and aneuploid human pluripotent stem cells. Cell Cycle 8: 3822-3830 (2009).
11. Boulting GL, Kiskinis E, Croft GF, Amoroso MW, Oakley DH, et al: A functionally characterized test set of human induced pluripotent stem cells. Nat Biotechnol 29: 279-286 (2011).
12. Brevini TA, Pennarossa G, Antonini S, Paffoni A, Tettamanti G, et al: Cell lines derived from human parthenogenetic embryos can display aberrant centriole distribution and altered expression levels of mitotic spindle check-point transcripts. Stem Cell Rev 5: 340-352 (2009).
13. Brevini TA, Pennarossa G, Maffei S, Tettamanti G, Vanelli A, et al: Centrosome amplification and chromosomal instability in human and animal parthenogenetic cell lines. Stem Cell Rev 8: 1076-1087 (2012).
14. Brimble SN, Zeng X, Weiler DA, Luo Y, Liu Y, et al: Karyotypic stability, genotyping, differentiation, feeder-free maintenance, and gene expression sampling in three human embryonic stem cell lines derived prior to August 9, 2001. Stem Cells Dev 13: 585-597 (2004).
15. Buehr M, Meek S, Blair K, Yang J, Ure J, et al: Capture of authentic embryonic stem cells from rat blastocysts. Cell 135: 1287-1298 (2008).
16. Buzzard JJ, Gough NM, Crook JM, Colman A: Karyotype of human ES cells during extended culture. Nat Biotechnol 22: 381-382 (2004).
17. Caldas C, Brenton JD: Sizing up miRNAs as cancer genes. Nat Med 11: 712-714 (2005).
18. Catalina P, Cobo F, Cortés JL, Nieto AI, Cabrera C, et al: Conventional and molecular cytogenetic diagnostic methods in stem cell research: A concise review. Cell Biol Int 31: 861-869 (2007).
19. Cibelli JB, Grant KA, Chapman KB, Cunniff K, Worst T, et al: Parthenogenetic stem cells in nonhuman primates. Science 295: 819 (2002).
20. Clark AT, Rodriguez RT, Bodnar MS, Abeyta MJ, Cedars MI, et al: Human STELLAR , NANOG , and GDF3 genes are expressed in pluripotent cells and map to chromosome 12p13, a hotspot for teratocarcinoma. Stem Cells 22: 169-179 (2004).
21. Cockburn K, Rossant J: Making the blastocyst: lessons from the mouse. J Clin Invest 120: 995-1003 (2010).
22. Corselli M, Parodi A, Mogni M, Sessarego N, Kunkl A, et al: Clinical scale ex vivo expansion of cord blood-derived outgrowth endothelial progenitor cells is associated with high incidence of karyotype aberrations. Exp Hematol 36: 340-349 (2008).
23. Cowan CA, Klimanskaya I, McMahon J, Atienza J, Witmyer J, et al: Derivation of embryonic stem-cell lines from human blastocysts. N Engl J Med 350: 1353-1356 (2004).
24. Diaferia GR, Conti L, Redaelli S, Cattaneo M, Mutti C, et al: Systematic chromosomal analysis of cultured mouse neural stem cell lines. Stem Cells Dev 20: 1411-1423 (2011).
25. Draper JS, Smith K, Gokhale P, Moore HD, Maltby E, et al: Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat Biotechnol 22: 53-54 (2004).
26. Duailibi MT, Kulikowski LD, Duailibi SE, Lipay MV, Melaragno MI, et al: Cytogenetic instability of dental pulp stem cell lines. J Mol Histol 43: 89-94 (2012).
27. Estrada JC, Albo C, Benguría A, Dopazo A, López-Romero P, et al: Culture of human mesenchymal stem cells at low oxygen tension improves growth and genetic stability by activating glycolysis. Cell Death Differ 19: 743-755 (2012).
28. Estrada JC, Torres Y, Benguría A, Dopazo A, Roche E, et al: Human mesenchymal stem cell-replicative senescence and oxidative stress are closely linked to aneuploidy. Cell Death Dis 4:e691 (2013).
29. Evans MJ, Kaufman MH: Establishment in culture of pluripotential cells from mouse embryos. Nature 292: 154-156 (1981).
30. Fan G, Wen L, Li M, Li C, Luo B, et al: Isolation of mouse mesenchymal stem cells with normal ploidy from bone marrows by reducing oxidative stress in combination with extracellular matrix. BMC Cell Biol 12: 30 (2011).
31. Fang ZF, Gai H, Huang YZ, Li SG, Chen XJ, et al: Rabbit embryonic stem cell lines derived from fertilized, parthenogenetic or somatic cell nuclear transfer embryos. Exp Cell Res 312: 3669-3682 (2006).
32. Forsyth NR, Musio A, Vezzoni P, Simpson AH, Noble BS, McWhir J: Physiologic oxygen enhances human embryonic stem cell clonal recovery and reduces chromosomal abnormalities. Cloning Stem Cells 8: 16-23 (2006).
33. Franco Lambert AP, Fraga Zandonai A, Bonatto D, Cantarelli Machado D, Pêgas Henriques JA: Differentiation of human adipose-derived adult stem cells into neuronal tissue: does it work? Differentiation 77: 221-228 (2009).
34. Gaztelumendi N, Nogués C: Chromosome instability in mouse embryonic stem cells. Sci Rep 4: 5324 (2014).
35. Ge J, Cai H, Tan WS: Chromosomal stability during ex vivo expansion of UCB CD34(+) cells. Cell Prolif 44: 550-557 (2011).
36. Gore A, Li Z, Fung HL, Young JE, Agarwal S, et al: Somatic coding mutations in human induced pluripotent stem cells. Nature 471: 63-67 (2011).
37. Grigorian AS, Kruglyakov PV, Taminkina UA, Efimova OA, Pendina AA, et al: Alterations of cytological and karyological profile of human mesenchymal stem cells during in vitro culturing. Bull Exp Biol Med 150: 125-130 (2010).
38. Grompe M: Tissue stem cells: new tools and functional diversity. Cell Stem Cell 10: 685-689 (2012).
39. Gronthos S, Mankani M, Brahim J, Robey PG, Shi S: Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci USA 97: 13625-13630 (2000).
40. Guo J, Jauch A, Heidi HG, Schoell B, Erz D, et al: Multicolor karyotype analyses of mouse embryonic stem cells. In Vitro Cell Dev Biol Anim 41: 278-283 (2005).
41. Hayes B, Fagerlie SR, Ramakrishnan A, Baran S, Harkey M, et al: Derivation, characterization, and in vitro differentiation of canine embryonic stem cells. Stem Cells 26: 465-473 (2008).
42. Holzwarth C, Vaegler M, Gieseke F, Pfister SM, Handgretinger R, et al: Low physiologic oxygen tensions reduce proliferation and differentiation of human multipotent mesenchymal stromal cells. BMC Cell Biol 11: 11 (2010).
43. Imreh MP, Gertow K, Cedervall J, Unger C, Holmberg K, et al: In vitro culture conditions favoring selection of chromosomal abnormalities in human ES cells. J Cell Biochem 99: 508-516 (2006).
44. International Stem Cell Initiative: Screening ethnically diverse human embryonic stem cells identifies a chromosome 20 minimal amplicon conferring growth advantage. Nat Biotechnol 29: 1132-1144 (2011).
45. Inzunza J, Sahlén S, Holmberg K, Strömberg AM, Teerijoki H, et al: Comparative genomic hybridization and karyotyping of human embryonic stem cells reveals the occurrence of an isodicentric X chromosome after long-term cultivation. Mol Hum Reprod 10: 461-466 (2004).
46. Inzunza J, Gertow K, Strömberg MA, Matilainen E, Blennow E, et al: Derivation of human embryonic stem cell lines in serum replacement medium using postnatal human fibroblasts as feeder cells. Stem Cells 23: 544-549 (2005).
47. Jiang X, Xu R, Yang Z, Jin P, Xu Q, et al: Experimental study on trace marking and oncogenicity of neural stem cells derived from bone marrow. Cell Mol Neurobiol 28: 689-711 (2008).
48. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, et al: Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418: 41-49 (2002).
49. Josse C, Schoemans R, Niessen NA, Delgaudine M, Hellin AC, et al: Systematic chromosomal aberrations found in murine bone marrowderived mesenchymal stem cells. Stem Cells Dev 19: 1167-1173 (2010).
50. Ju JY, Park CY, Gupta MK, Uhm SJ, Paik EC, et al: Establishment of stem cell lines from nuclear transferred and parthenogenetically activated mouse oocytes for therapeutic cloning. Fertil Steril 89: 1314-1323 (2008).
51. Katari R, Peloso A, Orlando G: Tissue engineering and regenerative medicine: semantic considerations for an evolving paradigm. Front Bioeng Biotechnol 2: 57 (2015).
52. Kim K, Ng K, Rugg-Gunn PJ, Shieh JH, Kirak O, et al: Recombination signatures distinguish embryonic stem cells derived by parthenogenesis and somatic cell nuclear transfer. Cell Stem Cell 1: 346-352 (2007).
53. Kim YM, Lee JY, Xia L, Mulvihill JJ, Li S: Trisomy 8: A common finding in mouse embryonic stem (ES) cell lines. Mol Cytogenet 6: 3 (2013).
54. Lefort N, Feyeux M, Bas C, Féraud O, Bennaceur-Griscelli A, et al: Human embryonic stem cells reveal recurrent genomic instability at 20q11.21. Nat Biotechnol 26: 1364-1366 (2008).
55. Lefort N, Perrier AL, Laâbi Y, Varela C, Peschanski M: Human embryonic stem cells and genomic instability. Regen Med 4: 899-909 (2009).
56. Li P, Tong C, Mehrian-Shai R, Jia L, Wu N, et al: Germline competent embryonic stem cells derived from rat blastocysts. Cell 135: 1299-1310 (2008).
57. Li R, Chen B, Wang G, Yu B, Ren G, Ni G: Effects of mechanical strain on oxygen free radical system in bone marrow mesenchymal stem cells from children. Injury 42: 753-757 (2011).
58. Liang G, Zhang Y: Genetic and epigenetic variations in iPSCs: potential causes and implications for application. Cell Stem Cell 13: 149-159 (2013).
59. Lim HJ, Han J, Woo DH, Kim SE, Kim SK, et al: Biochemical and morphological effects of hypoxic environment on human embryonic stem cells in long-term culture and differentiating embryoid bodies. Mol Cells 31: 123-132 (2011).
60. Lin G, OuYang Q, Zhou X, Gu Y, Yuan D, et al: A highly homozygous and parthenogenetic human embryonic stem cell line derived from a one-pronuclear oocyte following in vitro fertilization procedure. Cell Res 17: 999-1007 (2007).
61. Liu LN, Wang G, Hendricks K, Lee K, Bohnlein E, et al: Comparison of drug and cell-based delivery: engineered adult mesenchymal stem cells expressing soluble tumor necrosis factor receptor II prevent arthritis in mouse and rat animal models. Stem Cells Transl Med 2: 362-375 (2013).
62. Liu W, Yin Y, Jiang Y, Kou C, Luo Y, et al: Genetic and epigenetic X-chromosome variations in a parthenogenetic human embryonic stem cell line. J Assist Reprod Genet 28: 303-313 (2011).
63. Liu X, Wu H, Loring J, Hormuzdi S, Disteche CM, et al: Trisomy eight in ES cells is a common potential problem in gene targeting and interferes with germ line transmission. Dev Dyn 209: 85-91 (1997).
64. Liyanage M, Coleman A, du Manoir S, Veldman T, McCormack S, et al: Multicolour spectral karyotyping of mouse chromosomes. Nat Genet 14: 312-315 (1996).
65. Ludwig TE, Levenstein ME, Jones JM, Berggren WT, Mitchen ER, et al: Derivation of human embryonic stem cells in defined conditions. Nat Biotechnol 24: 185-187 (2006).
66. Luft S, Pignalosa D, Nasonova E, Arrizabalaga O, Helm A, et al: Fate of D3 mouse embryonic stem cells exposed to X-rays or carbon ions. Mutat Res Genet Toxicol Environ Mutagen 760: 56-63 (2014).
67. Mai Q, Yu Y, Li T, Wang L, Chen MJ, et al: Derivation of human embryonic stem cell lines from parthenogenetic blastocysts. Cell Res 17: 1008-1019 (2007).
68. Maitra A, Arking DE, Shivapurkar N, Ikeda M, Stastny V, et al: Genomic alterations in cultured human embryonic stem cells. Nat Genet 37: 1099-1103 (2005).
69. Martin GR: Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 78: 7634-7638 (1981).
70. Martins-Taylor K, Xu RH: Concise review: genomic stability of human induced pluripotent stem cells. Stem Cells 30: 22-27 (2012).
71. Martins-Taylor K, Nisler BS, Taapken SM, Compton T, Crandall L, et al: Recurrent copy number variations in human induced pluripotent stem cells. Nat Biotechnol 29: 488-491 (2011).
72. Mayshar Y, Ben-David U, Lavon N, Biancotti JC, Yakir B, et al: Identification and classification of chromosomal aberrations in human induced pluripotent stem cells. Cell Stem Cell 7: 521-531 (2010).
73. Merkle FT, Eggan K: Modeling human disease with pluripotent stem cells: from genome association to function. Cell Stem Cell 12: 656-668 (2013).
74. 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 12: 553-563 (2008).
75. Mitalipova MM, Rao RR, Hoyer DM, Johnson JA, Meisner LF, et al: Preserving the genetic integrity of human embryonic stem cells. Nat Biotechnol 23: 19-20 (2005).
76. Miura M, Miura Y, Padilla-Nash HM, Molinolo AA, Fu B, et al: Accumulated chromosomal instability in murine bone marrow mesenchymal stem cells leads to malignant transformation. Stem Cells 24: 1095-1103 (2006).
77. Navarro P, Chambers I, Karwacki-Neisius V, Chureau C, Morey C, et al: Molecular coupling of Xist regulation and pluripotency. Science 321: 1693-1695 (2008).
78. Neri T, Merico V, Fiordaliso F, Salio M, Rebuzzini P, et al: The differentiation of cardiomyocytes from mouse embryonic stem cells is altered by dioxin. Toxicol Lett 202: 226-236 (2011).
79. Nikitina VA, Osipova EY, Katosova LD, Rumyantsev SA, Skorobogatova EV, et al: Study of genetic stability of human bone marrow multipotent mesenchymal stromal cells. Bull Exp Biol Med 150: 627-631 (2011).
80. Okita K, Ichisaka T, Yamanaka S: Generation of germline-competent induced pluripotent stem cells. Nature 448: 313-317 (2007).
81. Oliveira PH, Boura JS, Abecasis MM, Gimble JM, da Silva CL, Cabral JM: 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 9: 225-236 (2012).
82. Oliveira PH, da Silva CL, Cabral JM: Concise review: Genomic instability in human stem cells: current status and future challenges. Stem Cells 32: 2824-2832 (2014).
83. Peiffer DA, Le JM, Steemers FJ, Chang W, Jenniges T, et al: High-resolution genomic profiling of chromosomal aberrations using Infinium whole-genome genotyping. Genome Res 16: 1136-1148 (2006).
84. Peterson SE, Loring JF: Genomic instability in pluripotent stem cells: implications for clinical applications. J Biol Chem 289: 4578-4584 (2014).
85. Pittenger MF, Martin BJ: Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res 95: 9-20 (2004).
86. Poloni A, Maurizi G, Babini L, Serrani F, Berardinelli E, et al: Human mesenchymal stem cells from chorionic villi and amniotic fluid are not susceptible to transformation after extensive in vitro expansion. Cell Transplant 20: 643-654 (2011).
87. Porada CD, Atala AJ, Almeida-Porada G: The hematopoietic system in the context of regenerative medicine. Methods S1046-2023: 30057-30058 (2015).
88. Ra JC, Shin IS, Kim SH, Kang SK, Kang BC, et al: Safety of intravenous infusion of human adipose tissue-derived mesenchymal stem cells in animals and humans. Stem Cells Dev 20: 1297-1308 (2011).
89. Rebuzzini P, Neri T, Mazzini G, Zuccotti M, Redi CA, Garagna S: Karyotype analysis of the euploid cell population of a mouse embryonic stem cell line revealed a high incidence of chromosome abnormalities that varied during culture. Cytogenet Genome Res 121: 18-24 (2008a).
90. Rebuzzini P, Neri T, Zuccotti M, Redi CA, Garagna S: Chromosome number variation in three mouse embryonic stem cell lines during culture. Cytotechnology 58: 17-23 (2008b).
91. Rebuzzini P, Zuccotti M, Redi CA, Garagna S: Genome stability in embryonic stem cells, in Atwood CS (ed): Embryonic Stem Cells-Recent Advantages in Pluripotent Stem Cell-Based Regenerative Medicine, pp 399-410 (InTech, Rijeka 2011).
92. Rebuzzini P, Pignalosa D, Mazzini G, Di Liberto R, Coppola A, et al: Mouse embryonic stem cells that survive γ-rays exposure maintain pluripotent differentiation potential and genome stability. J Cell Physiol 227: 1242-1249 (2012).
93. Rebuzzini P, Fassina L, Mulas F, Bellazzi R, Redi CA, et al: Mouse embryonic stem cells irradiated with γ-rays differentiate into cardiomyocytes but with altered contractile properties. Mutat Res 756: 37-45 (2013).
94. Revazova ES, Turovets NA, Kochetkova OD, Kindarova LB, Kuzmichev LN, et al: Patientspecific stem cell lines derived from human parthenogenetic blastocysts. Cloning Stem Cells 9: 432-449 (2007).
95. Rosler ES, Fisk GJ, Ares X, Irving J, Miura T, et al: Long-term culture of human embryonic stem cells in feeder-free conditions. Dev Dyn 229: 259-274 (2004).
96. Rossant J: Stem cells from the mammalian blastocyst. Stem Cells 19: 477-482 (2001).
97. Ruan ZB, Zhu L, Yin YG, Chen GC: Karyotype stability of human umbilical cord-derived mesenchymal stem cells during in vitro culture. Exp Ther Med 8: 1508-1512 (2014).
98. Sanlaville D, Lapierre JM, Turleau C, Coquin A, Borck G, et al: Molecular karyotyping in human constitutional cytogenetics. Eur J Med Genet 48: 214-231 (2005).
99. Sareen D, McMillan E, Ebert AD, Shelley BC, Johnson JA, et al: Chromosome 7 and 19 trisomy in cultured human neural progenitor cells. PLoS One 4:e7630 (2009).
100. Schröck E, Blume C, Meffert MC, du Manoir S, Bersch W, et al: Recurrent gain of chromosome arm 7q in low-grade astrocytic tumors studied by comparative genomic hybridization. Genes Chromosomes Cancer 15: 199-205 (1996).
101. Seiler AE, Spielmann H: The validated embryonic stem cell test to predict embryotoxicity in vitro. Nat Protoc 6: 961-978 (2011).
102. Sensebé L, Tarte K, Galipeau J, Krampera M, Martin I, et al: Limited acquisition of chromosomal aberrations in human adult mesenchymal stromal cells. Cell Stem Cell 10: 9-10 (2012).
103. Shan ZY, Wu YS, Shen XH, Li X, Xue Y, et al: Aggregation of pre-implantation embryos improves establishment of parthenogenetic stem cells and expression of imprinted genes. Dev Growth Differ 54: 481-488 (2012).
104. Shao H, Wei Z, Wang L, Wen L, Duan B, et al: Generation and characterization of mouse parthenogenetic embryonic stem cells containing genomes from non-growing and fully grown oocytes. Cell Biol Int 31: 1336-1344 (2007).
105. Smith AG: Embryo-derived stem cells: of mice and men. Annu Rev Cell Dev Biol 17: 435-462 (2001).
106. Soukup T, Mokrý J, Karbanová J, Pytlík R, Suchomel P, Kucerová L: Mesenchymal stem cells isolated from the human bone marrow: cultivation, phenotypic analysis and changes in proliferation kinetics. Acta Medica (Hradec Kralove) 49: 27-33 (2006).
107. Spits C, Mateizel I, Geens M, Mertzanidou A, Staessen C, et al: Recurrent chromosomal abnormalities in human embryonic stem cells. Nat Biotechnol 26: 1361-1363 (2008).
108. Suchánek J, Soukup T, Ivancaková R, Karbanová J, Hubková V, et al: Human dental pulp stem cells-isolation and long term cultivation. Acta Medica (Hradec Kralove) 50: 195-201 (2007).
109. Suemori H, Yasuchika K, Hasegawa K, Fujioka T, Tsuneyoshi N, Nakatsuji N: Efficient establishment of human embryonic stem cell lines and long-term maintenance with stable karyotype by enzymatic bulk passage. Biochem Biophys Res Commun 345: 926-932 (2006).
110. Sugawara A, Goto K, Sotomaru Y, Sofuni T, Ito T: Current status of chromosomal abnormalities in mouse embryonic stem cell lines used in Japan. Comp Med 56: 31-34 (2006).
111. Takahashi K, Yamanaka S: Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676 (2006).
112. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, et al: Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872 (2007).
113. Tamaki Y, Nakahara T, Ishikawa H, Sato S: In vitro analysis of mesenchymal stem cells derived from human teeth and bone marrow. Odontology 101: 121-132 (2013).
114. Tarte K, Gaillard J, Lataillade JJ, Fouillard L, Becker M, et al: Clinical-grade production of human mesenchymal stromal cells: occurrence of aneuploidy without transformation. Blood 115: 1549-1553 (2010).
115. Thomsen GM, Gowing G, Svendsen S, Svendsen CN: The past, present and future of stem cell clinical trials for ALS. Exp Neurol 262: 127-137 (2014).
116. Thomson JA, Kalishman J, Golos TG, Durning M, Harris CP, et al: Isolation of a primate embryonic stem cell line. Proc Natl Acad Sci USA 92: 7844-7848 (1995).
117. Thomson JA, Kalishman J, Golos TG, Durning M, Harris CP, Hearn JP: Pluripotent cell lines derived from common marmoset (Callithrix jacchus) blastocysts. Biol Reprod 55: 254-259 (1996).
118. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, et al: Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147 (1998).
119. Tian H, Huang S, Gong F, Tian L, Chen Z: Karyotyping, immunophenotyping, and apoptosis analyses on human hematopoietic precursor cells derived from umbilical cord blood following long-term ex vivo expansion. Cancer Genet Cytogenet 157: 33-36 (2005).
120. Till JE, McCullough EA: A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res 14: 213-222 (1961).
121. Tsai CC, Chen YJ, Yew TL, Chen LL, Wang JY, et al: Hypoxia inhibits senescence and maintains mesenchymal stem cell properties through down-regulation of E2A-p21 by HIF-TWIST. Blood 117: 459-469 (2011).
122. Ueyama H, Horibe T, Hinotsu S, Tanaka T, Inoue T, et al: Chromosomal variability of human mesenchymal stem cells cultured under hypoxic conditions. J Cell Mol Med 16: 72-82 (2012).
123. Untergasser G, Koeck R, Wolf D, Rumpold H, Ott H, et al: CD34+/CD133-circulating endothelial precursor cells (CEP): characterization, senescence and in vivo application. Exp Gerontol 41: 600-608 (2006).
124. Vrana KE, Hipp JD, Goss AM, McCool BA, Riddle DR, et al: Nonhuman primate parthenogenetic stem cells. Proc Natl Acad Sci USA 100 Suppl 1: 11911-11916 (2003).
125. Wang S, Tang X, Niu Y, Chen H, Li B, et al: Generation and characterization of rabbit embryonic stem cells. Stem Cells 25: 481-489 (2007).
126. Wang Y, Zhang Z, Chi Y, Zhang Q, Xu F, et al: Long-term cultured mesenchymal stem cells frequently develop genomic mutations but do not undergo malignant transformation. Cell Death Dis 4:e950 (2013).
127. Wei Q, Sun Z, He X, Tan T, Lu B, et al: Derivation of rhesus monkey parthenogenetic embryonic stem cells and its microRNA signature. PLoS One 6:e25052 (2011).
128. Werbowetski-Ogilvie TE, Bossé M, Stewart M, Schnerch A, Ramos-Mejia V, et al: Characterization of human embryonic stem cells with features of neoplastic progression. Nat Biotechnol 27: 91-97 (2009).
129. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, et al: In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448: 318-324 (2007).
130. Wu W, He Q, Li X, Zhang X, Lu A, et al: Longterm cultured human neural stem cells undergo spontaneous transformation to tumor-initiating cells. Int J Biol Sci 7: 892-901 (2011).
131. Yang XF, He X, He J, Zhang LH, Su XJ, et al: High efficient isolation and systematic identification of human adipose-derived mesenchymal stem cells. J Biomed Sci 18: 59 (2011).
132. Zhang ZX, Guan LX, Zhang K, Wang S, Cao PC, et al: Cytogenetic analysis of human bone marrow-derived mesenchymal stem cells passaged in vitro. Cell Biol Int 31: 645-648 (2007).