Environmental Oxygen Tension Regulates the Energy Metabolism and Self-Renewal of Human Embryonic Stem Cells

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Forristal, Catherine E ^a   Christensen, David R ^a   Chinnery, Fay E ^a   Petruzzelli, Raffaella ^a   Parry, Kate L ^a   Sanchez Elsner, Tilman ^a   Houghton, Franchesca D ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; GLUCOSE; GLUCOSE TRANSPORTER 1; HYPOXIA INDUCIBLE FACTOR 2ALPHA; LACTIC ACID; MESSENGER RNA; OCTAMER TRANSCRIPTION FACTOR 4; OXYGEN; PYRUVIC ACID; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

ARTICLE; CARBOHYDRATE METABOLISM; CELL CULTURE; CELL HYPOXIA; CELL RENEWAL; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENERGY METABOLISM; ENVIRONMENTAL FACTOR; GENE EXPRESSION; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; INCUBATION TIME; METABOLIC REGULATION; OXIDATION; OXYGEN TENSION; PLURIPOTENT STEM CELL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL HYPOXIA; CELL PROLIFERATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; ENERGY METABOLISM; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION; GENE EXPRESSION REGULATION; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; HOMEODOMAIN PROTEINS; HUMANS; OXYGEN; OXYGEN CONSUMPTION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SOXB1 TRANSCRIPTION FACTORS;

EID: 84877090090     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062507     Document Type: Article

References (41)

1. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, et al. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147.
2. Ludwig TE, Levenstein ME, Jones JM, Berggren WT, Mitchen ER, et al. (2006) Derivation of human embryonic stem cells in defined conditions. Nat Biotechnol 24: 185-187.
3. Ezashi T, Das P, Roberts RM, (2005) Low O2 tensions and the prevention of differentiation of hES cells. Proceedings of the National Academy of Sciences of the United States of America 102: 4783-4788.
4. Westfall SD, Sachdev S, Das P, Hearne LB, Hannink M, et al. (2008) Identification of oxygen-sensitive transcriptional programs in human embryonic stem cells. Stem cells and development 17: 869-881.
5. Forristal CE, Wright KL, Hanley NA, Oreffo RO, Houghton FD, (2010) Hypoxia inducible factors regulate pluripotency and proliferation in human embryonic stem cells cultured at reduced oxygen tensions. Reproduction 139: 85-97.
6. Lofstedt T, Fredlund E, Holmquist-Mengelbier L, Pietras A, Ovenberger M, et al. (2007) Hypoxia inducible factor-2alpha in cancer. Cell Cycle 6: 919-926.
7. Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC, (2003) Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol 23: 9361-9374.
8. Houghton FD, Hawkhead JA, Humpherson PG, Hogg JE, Balen AH, et al. (2002) Non-invasive amino acid turnover predicts human embryo developmental capacity. Hum Reprod 17: 999-1005.
9. Brison DR, Houghton FD, Falconer D, Roberts SA, Hawkhead J, et al. (2004) Identification of viable embryos in IVF by non-invasive measurement of amino acid turnover. Hum Reprod 19: 2319-2324.
10. Sathananthan H, Pera M, Trounson A, (2002) The fine structure of human embryonic stem cells. Reproductive biomedicine online 4: 56-61.
11. Van Blerkom J, Davis P, Mathwig V, Alexander S, (2002) Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos. Hum Reprod 17: 393-406.
12. Henderson JK, Draper JS, Baillie HS, Fishel S, Thomson JA, et al. (2002) Preimplantation human embryos and embryonic stem cells show comparable expression of stage-specific embryonic antigens. Stem Cells 20: 329-337.
13. Draper JS, Fox V, (2003) Human embryonic stem cells: multilineage differentiation and mechanisms of self-renewal. Arch Med Res 34: 558-564.
14. Hewitson LC, Leese HJ, (1993) Energy metabolism of the trophectoderm and inner cell mass of the mouse blastocyst. J Exp Zool 267: 337-343.
15. Houghton FD, (2006) Energy metabolism of the inner cell mass and trophectoderm of the mouse blastocyst. Differentiation 74: 11-18.
16. Varum S, Momcilovic O, Castro C, Ben-Yehudah A, Ramalho-Santos J, et al. (2009) Enhancement of human embryonic stem cell pluripotency through inhibition of the mitochondrial respiratory chain. Stem cell research 3: 142-156.
17. Varum S, Rodrigues AS, Moura MB, Momcilovic O, Easley CA, et al. (2011) Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS One 6: e20914.
18. Folmes CD, Nelson TJ, Martinez-Fernandez A, Arrell DK, Lindor JZ, et al. (2011) Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metab 14: 264-271.
19. Tay JI, Rutherford AJ, Killick SR, Maguiness SD, Partridge RJ, et al. (1997) Human tubal fluid: production, nutrient composition and response to adrenergic agents. Hum Reprod 12: 2451-2456.
20. Petruzzelli R, Gaudino S, Amendola G, Sessa R, Puzone S, et al. (2010) Role of the cold shock domain protein A in the transcriptional regulation of HBG expression. Br J Haematol 150: 689-699.
21. Weinmann AS, Farnham PJ, (2002) Identification of unknown target genes of human transcription factors using chromatin immunoprecipitation. Methods 26: 37-47.
22. Forsyth NR, Musio A, Vezzoni P, Simpson AH, Noble BS, et al. (2006) Physiologic oxygen enhances human embryonic stem cell clonal recovery and reduces chromosomal abnormalities. Cloning Stem Cells 8: 16-23.
23. Amit M, Margulets V, Segev H, Shariki K, Laevsky I, et al. (2003) Human feeder layers for human embryonic stem cells. Biology of reproduction 68: 2150-2156.
24. Xu C, Inokuma MS, Denham J, Golds K, Kundu P, et al. (2001) Feeder-free growth of undifferentiated human embryonic stem cells. Nature biotechnology 19: 971-974.
25. Kihira Y, Yamano N, Izawa-Ishizawa Y, Ishizawa K, Ikeda Y, et al. (2011) Basic fibroblast growth factor regulates glucose metabolism through glucose transporter 1 induced by hypoxia-inducible factor-1alpha in adipocytes. Int J Biochem Cell Biol 43: 1602-1611.
26. Kondoh H, Lleonart ME, Nakashima Y, Yokode M, Tanaka M, et al. (2007) A high glycolytic flux supports the proliferative potential of murine embryonic stem cells. Antioxid Redox Signal 9: 293-299.
27. Chen CT, Shih YR, Kuo TK, Lee OK, Wei YH, (2008) Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells. Stem Cells 26: 960-968.
28. Flier JS, Mueckler M, McCall AL, Lodish HF, (1987) Distribution of glucose transporter messenger RNA transcripts in tissues of rat and man. J Clin Invest 79: 657-661.
29. Froehner SC, Davies A, Baldwin SA, Lienhard GE, (1988) The blood-nerve barrier is rich in glucose transporter. J Neurocytol 17: 173-178.
30. Kahn BB, Flier JS, (1990) Regulation of glucose-transporter gene expression in vitro and in vivo. Diabetes Care 13: 548-564.
31. Lee SH, Heo JS, Han HJ, (2007) Effect of hypoxia on 2-deoxyglucose uptake and cell cycle regulatory protein expression of mouse embryonic stem cells: involvement of Ca2+/PKC, MAPKs and HIF-1alpha. Cell Physiol Biochem 19: 269-282.
32. Hayashi M, Sakata M, Takeda T, Yamamoto T, Okamoto Y, et al. (2004) Induction of glucose transporter 1 expression through hypoxia-inducible factor 1alpha under hypoxic conditions in trophoblast-derived cells. J Endocrinol 183: 145-154.
33. Zelzer E, Levy Y, Kahana C, Shilo BZ, Rubinstein M, et al. (1998) Insulin induces transcription of target genes through the hypoxia-inducible factor HIF-1alpha/ARNT. The EMBO journal 17: 5085-5094.
34. Iyer NV, Kotch LE, Agani F, Leung SW, Laughner E, et al. (1998) Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 12: 149-162.
35. Seagroves TN, Ryan HE, Lu H, Wouters BG, Knapp M, et al. (2001) Transcription factor HIF-1 is a necessary mediator of the pasteur effect in mammalian cells. Mol Cell Biol 21: 3436-3444.
36. Wright G, Higgin JJ, Raines RT, Steenbergen C, Murphy E, (2003) Activation of the prolyl hydroxylase oxygen-sensor results in induction of GLUT1, heme oxygenase-1, and nitric-oxide synthase proteins and confers protection from metabolic inhibition to cardiomyocytes. J Biol Chem 278: 20235-20239.
37. Ryan HE, Lo J, Johnson RS, (1998) HIF-1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J 17: 3005-3015.
38. Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet JP, et al. (1996) Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J Biol Chem 271: 32529-32537.
39. Panopoulos AD, Yanes O, Ruiz S, Kida YS, Diep D, et al. (2012) The metabolome of induced pluripotent stem cells reveals metabolic changes occurring in somatic cell reprogramming. Cell Res 22: 168-177.
40. Prigione A, Fauler B, Lurz R, Lehrach H, Adjaye J, (2010) The senescence-related mitochondrial/oxidative stress pathway is repressed in human induced pluripotent stem cells. Stem Cells 28: 721-733.
41. Cowan CA, Klimanskaya I, McMahon J, Atienza J, Witmyer J, et al. (2004) Derivation of embryonic stem-cell lines from human blastocysts. N Engl J Med 350: 1353-1356.