Safety paradigm: Genetic evaluation of therapeutic grade human embryonic stem cells

Journal of the Royal Society Interface

Volumn 7, Issue SUPPL. 6, 2010, Pages

  Stephenson, Emma ^a   Ogilvie, Caroline Mackie ^b   Patel, Heema ^b   Cornwell, Glenda ^a   Jacquet, Laureen ^a   Kadeva, Neli ^a   Braude, Peter ^a   Ilic, Dusko ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Array comparative genomic hybridization; Cell therapy; Chromosome instability; Copy number variations; Human embryonic stem cells; Karyotype; Single nucleotide polymorphism

Indexed keywords

GENES; INVESTMENTS; NUCLEOTIDES; POLYMORPHISM; STEM CELLS;

CELL THERAPY; COMPARATIVE GENOMIC HYBRIDIZATIONS; COPY NUMBER; HUMAN EMBRYONIC STEM CELLS; KARYOTYPE; SINGLE NUCLEOTIDE POLYMORPHISMS;

CYTOLOGY;

CHROMOSOMAL INSTABILITY; COMPARATIVE GENOMIC HYBRIDIZATION; COPY NUMBER VARIATION; CYTOGENETICS; DIAGNOSTIC TEST; EMBRYONIC STEM CELL; HETEROZYGOSITY LOSS; KARYOTYPING; REGENERATIVE MEDICINE; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; STEM CELL TRANSPLANTATION;

EID: 78649859839     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2010.0343.focus     Document Type: Review

References (79)

1. Adewumi, O. et al. 2007 Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat. Biotechnol. 25, 803-816. (doi:10.1038/nbt1318)
2. Ahn, J. W., Mann, K., Walsh, S., Shehab, M., Hoang, S., Docherty, Z., Mohammed, S. & Mackie Ogilvie, C. 2010 Validation and implementation of array comparative genomic hybridisation as a first line test in place of postnatal karyotyping for genome imbalance. Mol. Cytogenet. 3, 9. (doi:10.1186/1755-8166-3-9)
3. Aladjem, M. I., Spike, B. T., Rodewald, L. W., Hope, T. J., Klemm, M., Jaenisch, R. & Wahl, G. M. 1998 ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage. Curr. Biol. 8, 145-155. (doi:10.1016/S0960-9822(98)70061-2)
4. Allegrucci, C. & Young, L. E. 2007 Differences between human embryonic stem cell lines. Hum. Reprod. Update 13, 103-120. (doi:10.1093/humupd/ dml041)
5. Amariglio, N. et al. 2009 Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient. PLoS Med. 6, e1000029. (doi:10.1371/journal.pmed.1000029)
6. Ammann, A. J., Cowan, M. J., Wara, D. W., Weintrub, P., Dritz, S., Goldman, H. & Perkins, H. A. 1983 Acquired immunodeficiency in an infant: possible transmission by means of blood products. Lancet 321, 956-958. (doi:10.1016/S0140-6736(83)92082-2)
7. Baker, D. E., Harrison, N. J., Maltby, E., Smith, K., Moore, H. D., Shaw, P. J., Heath, P. R., Holden, H. & Andrews, P. W. 2007 Adaptation to culture of human embryonic stem cells and oncogenesis in vivo. Nat. Biotechnol. 25, 207-215. (doi:10.1038/nbt1285)
8. Ballif, B. C., Rorem, E. A., Sundin, K., Lincicum, M., Gaskin, S., Coppinger, J., Kashork, C. D., Shaffer, L. G. & Bejjani, B. A. 2006 Detection of low-level mosaicism by array CGH in routine diagnostic specimens. Am. J. Med. Genet. A 140, 2757-2767. (doi:10.1002/ajmg.a.31539)
9. Bongso, A., Fong, C. Y. & Gauthaman, K. 2008 Taking stem cells to the clinic: major challenges. J. Cell. Biochem. 105, 1352-1360. (doi:10.1002/jcb.21957)
10. Braude, P., Minger, S. L. & Warwick, R. M. 2005 Stem cell therapy: hope or hype? BMJ 330, 1159-1160. (doi:10.1136/bmj.330.7501.1159)
11. Brockes, J. P. 1997 Amphibian limb regeneration: rebuilding a complex structure. Science 276, 81-87. (doi:10.1126/science.276.5309.81)
12. Catalina, P., Montes, R., Ligero, G., Sanchez, L., de la Cueva, T., Bueno, C., Leone, P. E. & Menendez, P. 2008 Human ESCs predisposition to karyotypic instability: is a matter of culture adaptation or differential vulnerability among hESC lines due to inherent properties? Mol. Cancer 7, 76. (doi:10.1186/1476-4598-7-76)
13. Cervantes, R. B., Stringer, J. R., Shao, C., Tischfield, J. A. & Stambrook, P. J. 2002 Embryonic stem cells and somatic cells differ in mutation frequency and type. Proc. Natl Acad. Sci. USA 99, 3586-3590. (doi:10.1073/pnas.062527199)
14. Cho, Y. M., Kwon, S., Pak, Y. K., Seol, H. W., Choi, Y. M., Park, D. J., Park, K. S. & Lee, H. K. 2006 Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells. Biochem. Biophys. Res. Commun. 348, 1472-1478. (doi:10.1016/j.bbrc.2006.08.020)
15. Civin, C. I. & Rao, M. S. 2006 How many human embryonic stem cell lines are sufficient? A US perspective. Stem Cells 24, 800-803. (doi:10.1634/stemcells.2006-0084)
16. Crook, J. M. et al. 2007 The generation of six clinical-grade human embryonic stem cell lines. Cell Stem Cell 1, 490-494. (doi:10.1016/j.stem.2007. 10.004)
17. De Sousa, P. A., Galea, G. & Turner, M. 2006 The road to providing human embryo stem cells for therapeutic use: the UK experience. Reproduction 132, 681-689. (doi:10.1530/rep.1.01080) (Pubitemid 44782518)
18. Diaferia, G. R., Dessi, S. S., Deblasio, P. & Biunno, I. 2008 Is stem cell chromosomes stability affected by cryopreservation conditions? Cytotechnology 58, 11-16. (doi:10.1007/s10616-008-9163-y)
19. Draper, J. S. et al. 2004 Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat. Biotechnol. 22, 53-54. (doi:10.1038/nbt922)
20. Edelman, L. & Hirschhorn, K. 2009 Clinical utility of array CGH for the detection of chromosomal imbalances associated with mental retardation and multiple congenital anomalies. Ann. NY Acad. Sci. 1151, 157-166. (doi:10.1111/j.1749-6632.2008.03610.x)
21. Edmonds, D. K., Lindsay, K. S., Miller, J. F., Williamson, E. & Wood, P. J. 1982 Early embryonic mortality in women. Fertil. Steril. 38, 447-453.
22. Elliott, A. M., Hohenstein Elliott, K. A. & Kammesheidt, A. In press. High resolution array-CGH characterization of human stem cells using a stem cell focused microarray. Mol. Biotechnol. (doi:10.1007/s12033-010-9294-1)
23. Engel, E. 1980 A new genetic concept: uniparental disomy and its potential effect, isodisomy. Am. J. Med. Genet. 6, 137-143. (doi:10.1002/ajmg. 1320060207)
24. Ezashi, T., Das, P. & Roberts, R. M. 2005 Low O2 tensions and the prevention of differentiation of hES cells. Proc. Natl Acad. Sci. USA 102, 4783-4788. (doi:10.1073/pnas.0501283102)
25. Feuk, L., Carson, A. R. & Scherer, S. W. 2006 Structural variation in the human genome. Nat. Rev. Genet. 7, 85-97. (doi:10.1038/nrg1767)
26. Forsyth, N. R., Musio, A., Vezzoni, P., Simpson, A. H., Noble, B. S. & McWhir, J. 2006 Physiologic oxygen enhances human embryonic stem cell clonal recovery and reduces chromosomal abnormalities. Cloning Stem Cells 8, 16-23. (doi:10.1089/clo.2006.8.16)
27. Franklin, S. B., Hunt, C., Cornwell, G., Peddie, V., Desousa, P., Livie, M., Stephenson, E. L. & Braude, P. R. 2008 hESCCO: development of good practice models for hES cell derivation. Regen. Med. 3, 105-116. (doi:10.2217/17460751.3.1.105)
28. Gianaroli, L., Magli, M. C., Ferraretti, A. P. & Munné, S. 1999 Preimplantation diagnosis for aneuploidies in patients undergoing in vitro fertilization with a poor prognosis: identification of the categories for which it should be proposed. Fertil. Steril. 72, 837-844. (doi:10.1016/S0015-0282(99) 00377-5)
29. Gruen, L. & Grabel, L. 2006 Concise review: scientific and ethical roadblocks to human embryonic stem cell therapy. Stem Cells 24, 2162-2169. (doi:10.1634/stemcells.2006-0105)
30. Hanson, C. & Caisander, G. 2005 Human embryonic stem cells and chromosome stability. APMIS 113, 751-755. (doi:10.1111/j.1600-0463.2005.apm-305. x)
31. Harper, J. C., Coonen, E., Handyside, A. H., Winston, R. M., Hopman, A. H. & Delhanty, J. D. 1995 Mosaicism of autosomes and sex chromosomes in morphologically normal, monospermic preimplantation human embryos. Prenat. Diagn. 15, 41-49. (doi:10.1002/pd.1970150109)
32. Hoffman, L. M. & Carpenter, M. K. 2005 Characterization and culture of human embryonic stem cells. Nat. Biotechnol. 23, 699-708. (doi:10.1038/nbt1102)
33. Hovatta, O. et al. 2010 A teratocarcinoma-like human embryonic stem cell (hESC) line and four hESC lines reveal potentially oncogenic genomic changes. PLoS ONE 5, e10263. (doi:10.1371/journal.pone.0010263)
34. Iafrate, A. J., Feuk, L., Rivera, M. N., Listewnik, M. L., Donahoe, P. K., Qi, Y., Scherer, S. W. & Lee, C. 2004 Detection of large-scale variation in the human genome. Nat. Genet. 36, 949-951. (doi:10.1038/ng1416)
35. Ilic, D. 2006 Culture of human embryonic stem cells and the extracellular matrix microenvironment. Regen. Med. 1, 95-101. (doi:10.2217/17460751.1.1.95)
36. Ilic, D., Caceres, E., Lu, S., Julian, P., Foulk, R. & Krtolica, A. 2010 Effect of karyotype on successful human embryonic stem cell derivation. Stem Cells Dev. 19, 39-46. (doi:10.1089/scd.2009.0136)
37. Imreh, M. P. et al. 2006 In vitro culture conditions favoring selection of chromosomal abnormalities in human ES cells. J. Cell. Biochem. 99, 508-516. (doi:10.1002/jcb.20897)
38. International HapMap Consortium. 2003 The International HapMap Project. Nature 426, 789-796. (doi:10.1038/nature02168)
39. International HapMap Consortium. 2005 A haplotype map of the human genome. Nature 437, 1299-1320. (doi:10.1038/nature04226)
40. International HapMap Consortium. 2007 A second generation human haplotype map of over 3.1 million SNPs. Nature 449, 851-861. (doi:10.1038/nature06258)
41. Iwatani, M., Ikegami, K., Kremenska, Y., Hattori, N., Tanaka, S., Yagi, S. & Shiota, K. 2006 Dimethyl sulfoxide has an impact on epigenetic profile in mouse embryoid body. Stem Cells 24, 2549-2556. (doi:10.1634/stemcells.2005- 0427)
42. Kahraman, S., Bahçe, M., Samli, H., Imirzalioǧlu, N., Yakisn, K., Cengiz, G. & Dönmez, E. 2000 Healthy births and ongoing pregnancies obtained by preimplantation genetic diagnosis in patients with advanced maternal age and recurrent implantation failure. Hum. Reprod. 15, 2003-2007. (doi:10.1093/humrep/15.9.2003)
43. Kopeika, J., Zhang, T., Rawson, D. M. & Elgar, G. 2005 Effect of cryopreservation on mitochondrial DNA of zebrafish (Danio rerio) blastomere cells. Mutat. Res. 570, 49-61. (doi:10.1016/j.mrfmmm.2004.09.007)
44. Krtolica, A. et al. 2007 Disruption of apical-basal polarity of human embryonic stem cells enhances hematoendothelial differentiation. Stem Cells 25, 2215-2223. (doi:10.1634/stemcells.2007-0230)
45. Laurent, L. C. et al. 2010 Restricted ethnic diversity in human embryonic stem cell lines. Nat. Methods 7, 6-7. (doi:10.1038/nmeth0110-06)
46. Lefort, N., Feyeux, M., Bas, C., Féraud, O., Bennaceur-Griscelli, A., Tachdjian, G., Peschanski, M. & Perrier, A. L. 2008 Human embryonic stem cells reveal recurrent genomic instability at 20q11.21. Nat. Biotechnol. 26, 1364-1366. (doi:doi:10.1038/nbt.1509)
47. Lefort, N., Perrier, A. L., Laâbi, Y., Varela, C. & Peschanski, M. 2009 Human embryonic stem cells and genomic instability. Regen. Med. 4, 899-909. (doi:10.2217/rme.09.63)
48. Llewelyn, C. A., Hewitt, P. E., Knight, R. S., Amar, K., Cousens, S., Mackenzie, J. & Will, R. G. 2004 Possible transmission of variant Creutzfeldt-Jakob disease by blood transfusion. Lancet 363, 417-421. (doi:10.1016/S0140-6736(04)15486-X)
49. Ludwig, T. E. et al. 2006 Derivation of human embryonic stem cells in defined conditions. Nat. Biotechnol. 24, 185-187. (doi:10.1038/nbt1177)
50. Maitra, A. et al. 2005 Genomic alterations in cultured human embryonic stem cells. Nat. Genet. 37, 1099-1103. (doi:10.1038/ng1631)
51. Marquez, C., Sandalinas, M., Bahçe, M., Alikani, M. & Munné, S. 2000 Chromosome abnormalities in 1255 cleavage-stage human embryos. Reprod. Biomed. Online 1, 17-26. (doi:10.1016/S1472-6483(10)61988-8)
52. Miller, G. 2009 Neurodegeneration. Could they all be prion diseases? Science 326, 1337-1339. (doi:10.1126/science.326.5958.1337)
53. Mitalipova, M. M., Rao, R. R., Hoyer, D. M., Johnson, J. A., Meisner, L. F., Jones, K. L., Dalton, S. & Stice, S. L. 2005 Preserving the genetic integrity of human embryonic stem cells. Nat. Biotechnol. 23, 19-20. (doi:10.1038/nbt0105-19)
54. Mosher, J. T., Pemberton, T. J., Harter, K., Wang, C., Buzbas, E. O., Dvorak, P., Simón, C., Morrison, S. J. & Rosenberg, N. A. 2010 Lack of population diversity in commonly used human embryonic stem-cell lines. N. Engl. J. Med. 362, 183-185. (doi:10.1056/NEJMc0910371)
55. Munné, S., Tang, Y. X., Grifo, J., Rosenwaks, Z. & Cohen, J. 1994 Sex determination of human embryos using the polymerase chain reaction and confirmation by fluorescence in situ hybridization. Fertil. Steril. 61, 111-117.
56. Nannya, Y. et al. 2005 A robust algorithm for copy number detection using high-density oligonucleotide single nucleotide polymorphism genotyping arrays. Cancer Res. 65, 6071-6079. (doi:10.1158/0008-5472.CAN-05-0465)
57. Närvä, E. et al. 2010 High-resolution DNA analysis of human embryonic stem cell lines reveals culture-induced copy number changes and loss of heterozygosity. Nat. Biotechnol. 28, 371-377. (doi:10.1038/nbt.1615)
58. Oh, S. K. et al. 2005 Derivation and characterization of new human embryonic stem cell lines: SNUhES1, SNUhES2, and SNUhES3. Stem Cells 23, 211-219. (doi:10.1634/stemcells.2004-0122)
59. Park, J., Hwang, S., Lee, Y. S., Kim, S. C. & Lee, D. 2007 SNP@Ethnos: a database of ethnically variant single-nucleotide polymorphisms. Nucleic Acids Res. 35, D711-D715. (doi:10.1093/nar/gkl962)
60. Robinson, W. P. 2000 Mechanisms leading to uniparental disomy and their clinical consequences. Bioessays 22, 452-459. (doi:10.1002/(SICI)1521- 1878(200005)22:5〈452::AID-BIES7〉3.0.CO;2-K)
61. Sherry, S. T., Ward, M. H., Kholodov, M., Baker, J., Phan, L., Smigielski, E. M. & Sirotkin, K. 2001 dbSNP: the NCBI database of genetic variation. Nucleic Acids Res. 29, 308-311. (doi:10.1093/nar/29.1.308)
62. Skottman, H. & Hovatta, O. 2006 Culture conditions for human embryonic stem cells. Reproduction 132, 691-698. (doi:10.1530/rep.1.01079)
63. Song, H., Chung, S. K. & Xu, Y. 2010 Modeling disease in human ESCs using an efficient BAC-based homologous recombination system. Cell Stem Cell 6, 80-89. (doi:10.1016/j.stem.2009.11.016)
64. Spits, C., Mateizel, I., Geens, M., Mertzanidou, A., Staessen, C., Vandeskelde, Y., Van der Elst, J., Liebaers, I. & Sermon, K. 2008 Recurrent chromosomal abnormalities in human embryonic stem cells. Nat. Biotechnol. 26, 1361-1363. (doi:10.1038/nbt.1510)
65. St John, J. C., Ramalho-Santos, J., Gray, H. L., Petrosko, P., Rawe, V. Y., Navara, C. S., Simerly, C. R. & Schatten, G. P. 2005 The expression of mitochondrial DNA transcription factors during early cardiomyocyte in vitro differentiation from human embryonic stem cells. Cloning Stem Cells 7, 141-153. (doi:10.1089/clo.2005.7.141)
66. Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S. & Jones, J. M. 1998 Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147. (doi:10.1126/science.282.5391.1145)
67. Tlsty, T. D. 1998 Cell-adhesion-dependent influences on genomic instability and carcinogenesis. Curr. Opin. Cell Biol. 10, 647-653. (doi:10.1016/S0955-0674(98)80041-0)
68. Unger, C., Skottman, H., Blomberg, P., Dilber, M. S. & Hovatta, O. 2008 Good manufacturing practice and clinical-grade human embryonic stem cell lines. Hum. Mol. Genet. 17, R48-R53. (doi:10.1093/hmg/ddn079)
69. Van Hoof, D., Braam, S. R., Dormeyer, W., Ward-van Oostwaard, D., Heck, A. J., Krijgsveld, J. & Mummery, C. L. 2008 Feeder-free monolayer cultures of human embryonic stem cells express an epithelial plasma membrane protein profile. Stem Cells 26, 2777-2781. (doi:10.1634/stemcells.2008-0365)
70. Venter, J. C. et al. 2001 The sequence of the human genome. Science 291, 1304-1351. (doi:10.1126/science.1058040)
71. Voullaire, L., Collins, V., Callaghan, T., McBain, J., Williamson, R. & Wilton, L. 2007 High incidence of complex chromosome abnormality in cleavage embryos from patients with repeated implantation failure. Fertil. Steril. 87, 1053-1058. (doi:10.1016/j.fertnstert.2006.11.043)
72. Wells, D., Bermudez, M. G., Steuerwald, N., Malter, H. E., Thornhill, A. R. & Cohen, J. 2005 Association of abnormal morphology and altered gene expression in human preimplantation embryos. Fertil. Steril. 84, 343-355. (doi:10.1016/j.fertnstert.2005.01.143)
73. Werbowetski-Ogilvie, T. E. et al. 2009 Characterization of human embryonic stem cells with features of neoplastic progression. Nat. Biotechnol. 27, 91-97. (doi:10.1038/nbt.1516)
74. Wu, H. et al. 2008 Copy number variant analysis of human embryonic stem cells. Stem Cells 26, 1484-1489. (doi:10.1634/stemcells.2007-0993)
75. Xu, C., Inokuma, M. S., Denham, J., Golds, K., Kundu, P., Gold, J. D. & Carpenter, M. K. 2001 Feeder-free growth of undifferentiated human embryonic stem cells. Nat. Biotechnol. 19, 971-974. (doi:10.1038/nbt1001-971)
76. Ylstra, B., van den Ijssel, P., Carvalho, B., Brakenhoff, R. H. & Meijer, G. A. 2006 BAC to the future! or oligonucleotides: a perspective for micro array comparative genomic hybridization (array CGH). Nucleic Acids Res. 34, 445-450. (doi:10.1093/nar/gkj456)
77. Yunis, J. J. 1976 High resolution of human chromosomes. Science 191, 1268-1270. (doi:10.1126/science.1257746)
78. Zhao, T. & Xu, Y. 2010 p53 and stem cells: new developments and new concerns. Trends Cell Biol. 20, 170-175. (doi:10.1016/j.tcb.2009.12.004)
79. Zhao, X. et al. 2004 An integrated view of copy number and allelic alterations in the cancer genome using single nucleotide polymorphism arrays. Cancer Res. 64, 3060-3071. (doi:10.1158/0008-5472.CAN-03-3308)