Effects of long-term culture on human embryonic stem cell aging

Stem Cells and Development

Volumn 20, Issue 1, 2011, Pages 127-138

  Xie, Xiaoyan ^a,b   Hiona, Asimina ^a   Lee, Andrew Stephen ^a   Cao, Feng ^a   Huang, Mei ^a   Li, Zongjin ^a   Cherry, Athena ^a   Pei, Xuetao ^b   Wu, Joseph C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; REACTIVE OXYGEN METABOLITE; TELOMERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL AGING; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; GERM LAYER; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; TERATOMA;

ANIMALS; BIOLOGICAL MARKERS; CELL AGING; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CELL SHAPE; EMBRYONIC STEM CELLS; HUMANS; KARYOTYPING; MICE; MITOCHONDRIA; TELOMERASE; TERATOMA; TIME FACTORS;

EID: 78649854071     PISSN: 15473287     EISSN: None     Source Type: Journal    
DOI: 10.1089/scd.2009.0475     Document Type: Article

References (51)

1. Thomson JA, J Itskovitz-Eldor, SS Shapiro, MA Waknitz, JJ Swiergiel, VS Marshall and JM Jones. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147.
2. Laflamme MA, KY Chen, AV Naumova, V Muskheli, JA Fugate, SK Dupras, H Reinecke, C Xu, M Hassanipour, S Police, OSullivan C, L Collins, Y Chen, E Minami, EA Gill, S Ueno, C Yuan, J Gold and CE Murry. (2007). Cardiomyocytes derived from human embryonic stem cells in prosurvival factors enhance function of infarcted rat hearts. Nat Biotechnol 25:1015-1024.
3. Cao F, RA Wagner, KD Wilson, X Xie, Fu J-D, M Drukker, A Lee, RA Li, SS Gambhir, IL Weissman, RC Robbins and JC Wu. (2008). Transcriptional and functional profiling of human embryonic stem cell-derived cardiomyocytes. PLoS ONE 3:e3474.
4. Ben-Hur T, M Idelson, H Khaner, M Pera, E Reinhartz, A Itzik and BE Reubinoff. (2004). Transplantation of human embryonic stem cell-derived neural progenitors improves behavioral deficit in Parkinsonian rats. Stem Cells 22:1246-1255.
5. Kim JH, JM Auerbach, JA Rodriguez-Gomez, I Velasco, D Gavin, N Lumelsky, SH Lee, J Nguyen, R Sanchez-Pernaute, K Bankiewicz and R McKay. (2002). Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinsons disease. Nature 418:50-56.
6. Kroon E, LA Martinson, K Kadoya, AG Bang, OG Kelly, S Eliazer, H Young, M Richardson, NG Smart, J Cunningham, AD Agulnick, DAmour KA, MK Carpenter and EE Baetge. (2008). Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 26:443-452.
7. Soto-Gutierrez A, N Kobayashi, JD Rivas-Carrillo, N Navarro-Alvarez, D Zhao, T Okitsu, H Noguchi, H Basma, Y Tabata, Y Chen, K Tanaka, M Narushima, A Miki, T Ueda, HS Jun, JW Yoon, J Lebkowski, N Tanaka and IJ Fox. (2006). Reversal of mouse hepatic failure using an implanted liverassist device containing ES cell-derived hepatocytes. Nat Biotechnol 24:1412-1419.
8. Narayan AD, JL Chase, RL Lewis, X Tian, DS Kaufman, JA Thomson and ED Zanjani. (2006). Human embryonic stem cell-derived hematopoietic cells are capable of engrafting primary as well as secondary fetal sheep recipients. Blood 107:2180-2183.
9. Tian X, PS Woll, JK Morris, JL Linehan and DS Kaufman. (2006). Hematopoietic engraftment of human embryonic stem cell-derived cells is regulated by recipient innate immunity. Stem Cells 24:1370-1380. (Pubitemid 44464705)
10. Chen SL, WW Fang, F Ye, YH Liu, J Qian, SJ Shan, JJ Zhang, RZ Chunhua, LM Liao, S Lin and JP Sun. (2004). Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am J Cardiol 94:92-95. (Pubitemid 38813459)
11. Wollert KC, GP Meyer, J Lotz, S Ringes-Lichtenberg, P Lippolt, C Breidenbach, S Fichtner, T Korte, B Hornig, D Messinger, L Arseniev, B Hertenstein, A Ganser and H Drexler. (2004). Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet. 364:141-148.
12. Goldstein S. (1990). Replicative senescence: the human fibroblast comes of age. Science 249:1129-1133.
13. Finkel T and NJ Holbrook. (2000). Oxidants, oxidative stress and the biology of ageing. Nature 408:239-247.
14. Kamminga LM and GD Haan. (2006). Cellular memory and hematopoietic stem cell aging. Stem Cells 24:1143-1149.
15. Cervantes RB, JR Stringer, C Shao, JA Tischfield and PJ Stambrook. (2002). Embryonic stem cells and somatic cells differ in mutation frequency and type. Proc Natl Acad Sci USA 99:3586-3590.
16. Amit M, MK Carpenter, MS Inokuma, C-P Chiu, CP Harris, MA Waknitz, J Itskovitz-Eldor and JA Thomson. (2000). Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol 227:271-278.
17. Rosler ES, GJ Fisk, X Ares, J Irving, T Miura, MS Rao and MK Carpenter. (2004). Long-term culture of human embryonic stem cells in feeder-free conditions. Dev Dyn 229: 259-274. (Pubitemid 38140465)
18. Brimble SN, X Zeng, DA Weiler, Y Luo, Y Liu, IG Lyons, WJ Freed, AJ Robins, MS Rao and TC Schulz. (2004). 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.
19. Buzzard JJ, NM Gough, JM Crook and A Colman. (2004). Karyotype of human ES cells during extended culture. Nat Biotech 22:381-382.
20. Rugg-Gunn PJ, AC Ferguson-Smith and RA Pedersen. (2005). Epigenetic status of human embryonic stem cells. Nat Genet 37:585-587.
21. Mitalipov SM. (2006). Genomic imprinting in primate embryos and embryonic stem cells. Reprod Fertil Dev 18: 817-821.
22. Sun BW, AC Yang, Y Feng, YJ Sun, Y Zhu, Y Zhang, H Jiang, CL Li, FR Gao, ZH Zhang, WC Wang, XY Kong, G Jin, SJ Fu and Jin Y. (2006). Temporal and parental-specific expression of imprinted genes in a newly derived Chinese human embryonic stem cell line and embryoid bodies. Hum Mol Genet 15:65-75.
23. Draper JS, K Smith, P Gokhale, HD Moore, E Maltby, J Johnson, L Meisner, TP Zwaka, JA Thomson and PW Andrews. (2004). Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat Biotechnol 22:53-54.
24. Maitra A, DE Arking, N Shivapurkar, M Ikeda, V Stastny, K Kassauei, G Sui, DJ Cutler, Y Liu, SN Brimble, K Noaksson, J Hyllner, TC Schulz, X Zeng, WJ Freed, J Crook, S Abraham, A Colman, P Sartipy, S Matsui, M Carpenter, AF Gazdar, M Rao and Chakravarti A. (2005). Genomic alterations in cultured human embryonic stem cells. Nat Genet 37:1099-1103. (Pubitemid 41486662)
25. Pannetier M and Feil R. (2007). Epigenetic stability of embryonic stem cells and developmental potential. Trends Biotechnol 25:556-562.
26. Peng H-m and G-a Chen. (2006). Serum-free medium cultivation to improve efficacy in establishment of human embryonic stem cell lines. Hum Reprod 21:217-222.
27. Li Z, Y Suzuki, M Huang, F Cao, X Xie, AJ Connolly, PC Yang and JC Wu. (2008). Comparison of reporter gene and iron particle labeling for tracking fate of human embryonic stem cells and differentiated endothelial cells in living subjects. Stem Cells 26:864-873.
28. Sun N, A Lee and JC Wu. (2009). Long term non-invasive imaging of embryonic stem cells using reporter genes. Nature protocols 4:1192-1201.
29. Barch MJ, T Knutsen and JL Spurbeck. (1997). The AGT Cytogenetics Laboratory Manual. Chapter 4 (3rd Edition). Lippincott-Raven, New York.
30. Seabright M. (1971). A rapid banding technique for human chromosomes. Lancet 2:971-972.
31. Vermulst M, J Wanagat, GC Kujoth, JH Bielas, PS Rabinovitch, TA Prolla and LA Loeb. (2008). DNA deletions and clonal mutations drive premature aging in mitochondrial mutator mice. Nat Genet 40:392-394.
32. Balaban RS, S Nemoto and T Finkel. (2005). Mitochondria, oxidants, and aging. Cell 120:483-495.
33. Smiley ST, M Reers, Mottola-Hartshorn C, M Lin, A Chen, TW Smith, GD Steele, Jr., and LB Chen. (1991). Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc Natl Acad Sci USA 88:3671-3675.
34. Mamaeva SE. (1998). Karyotyptic evolution of cells in culture: a new concept. Int Rev Cytol 178:1-40.
35. Hiyama E and Hiyama K. (2007). Telomere and telomerase in stem cells. Br J Cancer 96:1020-1024.
36. Collins K and JR Mitchell. (2002). Telomerase in the human organism. Oncogene 21:564-579.
37. Blasco MA. (2005). Telomeres and human disease: ageing, cancer and beyond. Nat Rev Genet 6:611-622.
38. Wright WE and JW Shay. (2005). Telomere biology in aging and cancer. J Am Geriatr Soc 53(9 Suppl):S292-S294.
39. Park YB, YY Kim, SK Oh, SG Chung, SY Ku, SH Kim, YM Choi and SY Moon. (2008). Alterations of proliferative and differentiation potentials of human embryonic stem cells during long-term culture. Exp Mol Med 40:98-108.
40. Park S, KS Lee, YJ Lee, HA Shin, HY Cho, KC Wang, YS Kim, HT Lee, KS Chung, EY Kim and J Lim. (2004). Generation of dopaminergic neurons in vitro from human embryonic stem cells treated with neurotrophic factors. Neurosci Lett 359:99-103.
41. Harman D. (1956). Aging: a theory based on free radical and radiation chemistry. J Gerontol 11:298-300.
42. Trifunovic A, A Wredenberg, M Falkenberg, JN Spelbrink, AT Rovio, CE Bruder, YM Bohlooly, S Gidlof, A Oldfors, R Wibom, J Tornell, HT Jacobs and NG Larsson. (2004). Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429:417-423.
43. Linnane AW, S Marzuki, T Ozawa, et al. (1989). Mitochondrial DNA mutations as an important contributor to ageing and degenerative diseases. Lancet 1:642-645.
44. Brenner CA, HM Kubisch and KE Pierce. (2004). Role of the mitochondrial genome in assisted reproductive technologies and embryonic stem cell-based therapeutic cloning. Reprod Fertil Dev 16:743-751.
45. Schieke SM, M Ma, L Cao, McCoy JP, C Liu, NF Hensel, AJ Barrett, M Boehm and T Finkel. (2008). Mitochondrial metabolism modulates differentiation and teratoma formation capacity in mouse embryonic stem cells. J Biol Chem 283: 28506-28512.
46. Nesti C, L Pasquali, F Vaglini, G Siciliano and L Murri. (2007). The role of mitochondria in stem cell biology. Bioscience reports. 27:165-171.
47. St. John JC, Ramalho-Santos J, HL Gray, P Petrosko, VY Rawe, CS Navara, CR Simerly and GP Schatten. (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.
48. St. John J and R Lovell-Badge. (2007). Human-animal cytoplasmic hybrid embryos, mitochondria, and an energetic debate. Nat Cell Biol 9:988-992.
49. Rivolta MN and MC Holley. (2002). Asymmetric segregation of mitochondria and mortalin correlates with the multi-lineage potential of inner ear sensory cell progenitors in vitro. BrainRes Dev Brain Res 133:49-56.
50. Ezashi T, P Das and RM Roberts. (2005). Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci USA 102:4783-4788.
51. Sergey SK, PS Vladimir and AS Anatoly. (1997). High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416:15-18.