The adaptation of human embryonic stem cells to different feeder-free culture conditions is accompanied by a mitochondrial response

Stem Cells and Development

Volumn 21, Issue 7, 2012, Pages 1145-1155

  Ramos Mejia, Verónica ^a   Bueno, Clara ^a   Roldan, Mar ^b,c   Sanchez, Laura ^a   Ligero, Gertrudis ^a   Menendez, Pablo ^a   Martin, Miguel ^b,c  

^a UNIVERSITY OF GRANADA   (Spain)

^b CABIMER Andalusian Center for Molecular Biology and Regenerative Medicine CSIC University of Seville UPO   (Spain)

^c Hospital University Carlos Haya de Málaga   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; MITOCHONDRIAL DNA; RNA;

ADAPTATION; ADIPOSE DERIVED STEM CELL; ARTICLE; CELL CULTURE; EMBRYO; EMBRYONIC STEM CELL; FEEDER FREE CULTURE; FIBROBLAST; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PLURIPOTENT STEM CELL; PREPUCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADAPTATION, PHYSIOLOGICAL; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; BIOLOGICAL MARKERS; CELL CULTURE TECHNIQUES; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; DNA REPLICATION; DNA, MITOCHONDRIAL; EMBRYONIC STEM CELLS; FIBROBLASTS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MESENCHYMAL STEM CELLS; MITOCHONDRIA; STAGE-SPECIFIC EMBRYONIC ANTIGENS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84860196837     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2011.0248     Document Type: Article

References (41)

1. Bendall SC, MH Stewart, P Menendez, D George, K Vijayaragavan, T Werbowetski-Ogilvie, V Ramos-Mejia, A Rouleau, J Yang, et al. (2007). IGF and FGF cooperatively establish the regulatory stem cell niche of pluripotent human cells in vitro. Nature 448:1015-1021.
2. Montes R, G Ligero, L Sanchez, P Catalina, T de la Cueva, A Nieto, GJ Melen, R Rubio, J Garcia-Castro, C Bueno and P Menendez. (2009). Feeder-free maintenance of hESCs in mesenchymal stem cell-conditioned media: distinct requirements for TGF-beta and IGF-II. Cell Res 19:698-709.
3. Cho YM, S Kwon, YK Pak, HW Seol, YM Choi, J Park do, KS Park and HK Lee. (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.
4. Prigione A, B Fauler, R Lurz, H Lehrach and J Adjaye. (2010). The senescence-related mitochondrial/oxidative stress pathway is repressed in human induced pluripotent stem cells. Stem Cells 28:721-733.
5. Saretzki G, T Walter, S Atkinson, JF Passos, B Bareth, WN Keith, R Stewart, S Hoare, M Stojkovic, et al. (2008). Downregulation of multiple stress defense mechanisms during differentiation of human embryonic stem cells. Stem Cells 26:455-464.
6. St John JC, J Ramalho-Santos, 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.
7. Armstrong L, K Tilgner, G Saretzki, SP Atkinson, M Stojkovic, R Moreno, S Przyborski and M Lako. (2010). Human induced pluripotent stem cell lines show stress defense mechanisms and mitochondrial regulation similar to those of human embryonic stem cells. Stem Cells 28:661-673.
8. Ramos-Mejia V, GJ Melen, L Sanchez, I Gutierrez-Aranda, G Ligero, JL Cortes, PJ Real, C Bueno and P Menendez. (2010). Nodal/Activin signaling predicts human pluripotent stem cell lines prone to differentiate toward the hematopoietic lineage. Mol Ther 18:2173-2181.
9. Cortes JL, L Sanchez, G Ligero, I Gutierrez-Aranda, P Catalina, C Elosua, PE Leone, R Montes, C Bueno, et al. (2009). Mesenchymal stem cells facilitate the derivation of human embryonic stem cells from cryopreserved poor-quality embryos. Hum Reprod 24:1844-1851.
10. Cobo F, JM Navarro, MI Herrera, A Vivo, D Porcel, C Hernandez, M Jurado, J Garcia-Castro and P Menendez. (2008). Electron microscopy reveals the presence of viruses in mouse embryonic fibroblasts but neither in human embryonic fibroblasts nor in human mesenchymal cells used for hESC maintenance: toward an implementation of microbiological quality assurance program in stem cell banks. Cloning Stem Cells 10:65-74.
11. Bueno C, P Catalina, GJ Melen, R Montes, L Sanchez, G Ligero, JL Garcia-Perez and P Menendez. (2009). Etoposide induces MLL rearrangements and other chromosomal abnormalities in human embryonic stem cells. Carcinogenesis 30:1628-1637.
12. Catalina P, R Montes, G Ligero, L Sanchez, T de la Cueva, C Bueno, PE Leone and P Menendez. (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.
13. Menendez P, L Wang, K Chadwick, L Li and M Bhatia. (2004). Retroviral transduction of hematopoietic cells differentiated from human embryonic stem cell-derived CD45(neg)PFV hemogenic precursors. Mol Ther 10:1109-1120.
14. Chin AC, J Padmanabhan, SK Oh and AB Choo. (2010). Defined and serum-free media support undifferentiated human embryonic stem cell growth. Stem Cells Dev 19: 753-761.
15. Wang L, L Li, P Menendez, C Cerdan and M Bhatia. (2005). Human embryonic stem cells maintained in the absence of mouse embryonic fibroblasts or conditioned media are capable of hematopoietic development. Blood 105:4598-4603.
16. Xu C, MS Inokuma, J Denham, K Golds, P Kundu, JD Gold and MK Carpenter. (2001). Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 19: 971-974.
17. Rodriguez R, R Rubio, I Gutierrez-Aranda, GJ Melen, C Elosua, J Garcia-Castro and P Menendez. (2011). Fus-chop fusion protein expression coupled to p53 deficiency induces liposarcoma in mouse but not human adipose-derived mesenchymal stem/stromal cells. Stem Cells 29:179-192.
18. Sanchez L, I Gutierrez-Aranda, G Ligero, R Rubio, M Munoz- Lopez, JL Garcia-Perez, V Ramos, PJ Real, C Bueno, et al. (2011). Enrichment of human ESC-derived multipotent mesenchymal stem cells with immunosuppressive and antiinflammatory properties capable to protect against experimental inflammatory bowel disease. Stem Cells 29:251-262.
19. Rubio R, J Garcia-Castro, I Gutierrez-Aranda, J Paramio, M Santos, P Catalina, PE Leone, P Menendez and R Rodriguez. (2010). Deficiency in p53 but not retinoblastoma induces the transformation of mesenchymal stem cells in vitro and initiates leiomyosarcoma in vivo. Cancer Res 70:4185-4194.
20. Menendez P, P Catalina, R Rodriguez, GJ Melen, C Bueno, M Arriero, F Garcia-Sanchez, A Lassaletta, R Garcia-Sanz and J Garcia-Castro. (2009). Bone marrow mesenchymal stem cells from infants with MLL-AF4 + acute leukemia harbor and express the MLL-AF4 fusion gene. J Exp Med 206:3131-3141.
21. Rodriguez R, R Rubio, M Masip, P Catalina, A Nieto, T de la Cueva, M Arriero, N San Martin, E de la Cueva, et al. (2009). Loss of p53 induces tumorigenesis in p21-deficient mesenchymal stem cells. Neoplasia 11:397-407.
22. Menendez P, C Bueno and L Wang. (2006). Human embryonic stem cells: a journey beyond cell replacement therapies. Cytotherapy 8:530-541.
23. Menendez P, C Bueno, L Wang and M Bhatia. (2005). Human embryonic stem cells: potential tool for achieving immunotolerance? Stem Cell Rev 1:151-158.
24. Menendez P, L Wang and M Bhatia. (2005). Genetic manipulation of human embryonic stem cells: a system to study early human development and potential therapeutic applications. Curr Gene Ther 5:375-385.
25. Wang L, P Menendez, C Cerdan and M Bhatia. (2005). Hematopoietic development from human embryonic stem cell lines. Exp Hematol 33:987-996.
26. Park Y, JH Kim, SJ Lee, IY Choi, SJ Park, SR Lee, HJ Sung, YD Yoo, DH Geum, et al. (2011). Human feeder cells can support the undifferentiated growth of human and mouse embryonic stem cells using their own basic fibroblast growth factors. Stem Cells Dev. [Epub ahead of print]; DOI:10.1089/scd.2010.0496
27. Bobyleva V, TL Pazienza, R Maseroli, A Tomasi, S Salvioli, A Cossarizza, C Franceschi and VP Skulachev. (1998). Decrease in mitochondrial energy coupling by thyroid hormones: a physiological effect rather than a pathological hyperthyroidism consequence. FEBS Lett 430:409-413.
28. Di Lisa F, PS Blank, R Colonna, G Gambassi, HS Silverman, MD Stern and RG Hansford. (1995). Mitochondrial membrane potential in single living adult rat cardiac myocytes exposed to anoxia or metabolic inhibition. J Physiol 486:1-13.
29. White RJ and IJ Reynolds. (1996). Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J Neurosci 16:5688-5697.
30. Kelly DP and RC Scarpulla. (2004). Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev 18:357-368.
31. Wu Z, P Puigserver, U Andersson, C Zhang, G Adelmant, V Mootha, A Troy, S Cinti, B Lowell, RC Scarpulla and BM Spiegelman. (1999). Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98:115-124.
32. Barroso-delJesus A, G Lucena-Aguilar, L Sanchez, G Ligero, I Gutierrez-Aranda and P Menendez. (2011). The Nodal inhibitor LEFTY is negatively modulated by the microRNA miR- 302 in human embryonic stem cells. FASEB J 25:1497-1508.
33. Bavister BD. (2006). The mitochondrial contribution to stem cell biology. Reprod Fertil Dev 18:829-838.
34. Lonergan T, B Bavister and C Brenner. (2007). Mitochondria in stem cells. Mitochondrion 7:289-296.
35. Pal R, A Mandal, HS Rao, MS Rao and A Khanna. (2007). A panel of tests to standardize the characterization of human embryonic stem cells. Regen Med 2:179-192.
36. Rehman J. (2010). Empowering self-renewal and differentiation: the role of mitochondria in stem cells. JMol Med 88:981-986.
37. Facucho-Oliveira JM and JC St John. (2009). The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Rev 5:140-158.
38. van den Bogert C, JN Spelbrink and HL Dekker. (1992). Relationship between culture conditions and the dependency on mitochondrial function of mammalian cell proliferation. J Cell Physiol 152:632-638.
39. Birket MJ, AL Orr, AA Gerencser, DT Madden, C Vitelli, A Swistowski, MD Brand and X Zeng. (2011).Areduction in ATP demand and mitochondrial activity with neural differentiation of human embryonic stem cells. J Cell Sci 124:348-358.
40. Blanco-Gelaz MA, B Suarez-Alvarez, G Ligero, L Sanchez, JR Vidal-Castineira, E Coto, H Moore, P Menendez and C Lopez- Larrea. (2010). Endoplasmic reticulum stress signals in defined human embryonic stem cell lines and culture conditions. Stem Cell Rev 6:462-472.
41. das Neves RP, NS Jones, L Andreu, R Gupta, T Enver and FJ Iborra. (2010). Connecting variability in global transcription rate to mitochondrial variability. PLoS Biol 8:e1000560.