Effect of oxygen tension on the amino acid utilisation of human embryonic stem cells

Cellular Physiology and Biochemistry

Volumn 33, Issue 1, 2014, Pages 237-246

  Christensen, David R ^a   Calder, Philip C ^a,b   Houghton, Franchesca D ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY HOSPITAL SOUTHAMPTON NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Amino acids; Embryonic stem cells; Hypoxia; Metabolism; Oxygen tension

Indexed keywords

AMINO ACID; FIBROBLAST GROWTH FACTOR 2; OXYGEN; SERINE; ALANINE; ARGININE; ASPARAGINE; GLUTAMIC ACID; GLUTAMINE; GLYCINE; HISTIDINE; ISOLEUCINE; LYSINE; METHIONINE; PHENYLALANINE; TYROSINE; VALINE;

AMINO ACID METABOLISM; AMINO ACID SYNTHESIS; AMINO ACID TRANSPORT; ARTICLE; CELL RENEWAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; OXYGEN TENSION; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN SECRETION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; TURNOVER TIME; ATMOSPHERIC PRESSURE; CARBOHYDRATE METABOLISM; CELL CULTURE; CELL DIFFERENTIATION; CELL FUNCTION; CELL ISOLATION; COMPARATIVE STUDY; ENERGY METABOLISM; ENVIRONMENTAL FACTOR; CYTOLOGY; DRUG EFFECTS; HUMAN EMBRYONIC STEM CELL; METABOLISM; METABOLOME; TIME FACTOR;

AMINO ACIDS; CELLS, CULTURED; FIBROBLAST GROWTH FACTOR 2; HUMAN EMBRYONIC STEM CELLS; HUMANS; METABOLOME; OXYGEN; TIME FACTORS;

EID: 84893650161     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000356665     Document Type: Article

References (52)

1. Evans MJ, Kaufman MH: Establishment in culture of pluripotential cells from mouse embryos. Nature 1981;292:154-156.
2. 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 1981;78:7634-638.
3. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM: Embryonic stem cell lines derived from human blastocysts. Science 1998;282:1145-1147.
4. Thomson JA, Marshall VS: Primate embryonic stem cells. Curr Top Dev Biol 1998;38:133-165.
5. Ezashi T, Das P, Roberts RM: Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci USA 2005;102:4783-4788.
6. Westfall SD, Sachdev S, Das P, Hearne LB, Hannink M, Roberts RM, Ezashi T: Identification of oxygen-sensitive transcriptional programs in human embryonic stem cells. Stem Cells Dev 2008;17:869-881.
7. Prasad SM, Czepiel M, Cetinkaya C, Smigielska K, Weli SC, Lysdahl H, Gabrielsen A, Petersen K, Ehlers N, Fink T, Minger SL, Zachar V: Continuous hypoxic culturing maintains activation of Notch and allows long-term propagation of human embryonic stem cells without spontaneous differentiation. Cell Prolif 2009;42:63-74.
8. Chen H-F, Kuo H-C, Lin S-P, Chien C-L, Chiang M-S, Ho H-N: Hypoxic culture maintains self-renewal and enhances embryoid body formation of human embryonic stem cells. Tissue Eng Part A 2010;16:2901-2913.
9. Forristal CE, Wright KL, Hanley NA, Oreffo RO, Houghton FD: Hypoxia inducible factors regulate pluripotency and proliferation in human embryonic stem cells cultured at reduced oxygen tensions. Reproduction 2010;139:85-97.
10. Forristal CE, Christensen DR, Chinnery FE, Petruzzelli R, Parry KL, Sanchez-Elsner T, Houghton FD: Environmental oxygen tension regulates the energy metabolism and self-renewal of human embryonic stem cells. PLoS One 2013;8:e62507.
11. Meijer AJ, Baquet A, Gustafson L, van Woerkom GM, Hue L: Mechanism of activation of liver glycogen synthase by swelling. J Biol Chem 1992;267:5823-5828.
12. Bredt DS, Snyder SH: Nitric oxide: a physiologic messenger molecule. Annu Rev Biochem 1994;63:175-195.
13. Häussinger D: The role of cellular hydration in the regulation of cell function. Biochem J 1996;313:697-710.
14. Dawson KM, Collins JL, Baltz JM: Osmolarity-dependent glycine accumulation indicates a role for glycine as an organic osmolyte in early preimplantation mouse embryos. Biol Reprod 1998;59:225-232.
15. Lane M, Gardner DK: Amino acids and vitamins prevent culture-induced metabolic perturbations and associated loss of viability of mouse blastocysts. Hum Reprod 1998;13:991-997.
16. Wu G, Morris SM: Arginine metabolism: nitric oxide and beyond. Biochem J 1998;336:1-17.
17. Wu G, Meininger CJ: Regulation of nitric oxide synthesis by dietary factors. Annu Rev Nutr 2002;22:61-86.
18. Meijer AJ, Dubbelhuis PF: Amino acid signalling and the integration of metabolism. Biochem Biophys Res Commun 2004;313:397-403.
19. Morris SM: Arginine: beyond protein. Am J Clin Nutr 2006;83:508S-512S.
20. Chang L, Geng B, Yu F, Zhao J, Jiang H, Du J, Tang C: Hydrogen sulfide inhibits myocardial injury induced by homocysteine in rats. Amino Acids 2008;34:573-585.
21. Wu G: Amino acids: metabolism, functions, and nutrition. Amino Acids 2009;37:1-17.
22. Devreker F, Hardy K, Van den Bergh M, Vannin AS, Emiliani S, Englert Y: Amino acids promote human blastocyst development in vitro. Hum Reprod 2001;16:749-756.
23. Houghton FD, Hawkhead JA, Humpherson PG, Hogg JE, Balen AH, Rutherford AJ, Leese HJ: Non-invasive amino acid turnover predicts human embryo developmental capacity. Hum Reprod 2002;17:999-1005.
24. Brison DR, Houghton FD, Falconer D, Roberts SA, Hawkhead J, Humpherson PG, Lieberman BA, Leese HJ: Identification of viable embryos in IVF by non-invasive measurement of amino acid turnover. Hum Reprod 2004;19:2319-2324.
25. Stokes PJ, Hawkhead JA, Fawthrop RK, Picton HM, Sharma V, Leese HJ, Houghton FD: Metabolism of human embryos following cryopreservation: Implications for the safety and selection of embryos for transfer in clinical IVF. Hum Reprod 2007;22:829-835.
26. Higuera GA, Schop D, Spitters TWGM, van Dijkhuizen-Radersma R, Bracke M, de Bruijn JD, Martens D, Karperien M, van Boxtel A, van Blitterswijk CA: Patterns of amino acid metabolism by proliferating human mesenchymal stem cells. Tissue Eng Part A 2012;18:654-664.
27. Rathjen J, Yeo C, Yap C, Tan BSN, Rathjen PD, Gardner DK: Culture environment regulates amino acid turnover and glucose utilisation in human ES cells. Reprod Fertil Dev 2013; DOI: 10.1071/rd12276.
28. Soh H, Wasa M, Fukuzawa M: Hypoxia upregulates amino acid transport in a human neuroblastoma cell line. J Pediatr Surg 2007;42:608-612.
29. Gleason JE, Corrigan DJ, Cox JE, Reddi AR, McGinnis LA, Culotta VC: Analysis of hypoxia and hypoxia-like states through metabolite profiling. PLoS One 2011;6:e24741.
30. King N, Lin H, Suleiman MS: Oxidative stress increases SNAT1 expression and stimulates cysteine uptake in freshly isolated rat cardiomyocytes. Amino Acids 2011;40:517-526.
31. Fike CD, Sidoryk-Wegrzynowicz M, Aschner M, Summar M, Prince LS, Cunningham G, Kaplowitz M, Zhang Y, Aschner JL: Prolonged hypoxia augments L-citrulline transport by system A in the newborn piglet pulmonary circulation. Cardiovasc Res 2012;95:375-384.
32. Aflatoonian B, Ruban L, Shamsuddin S, Baker D, Andrews P, Moore H: Generation of Sheffield (Shef) human embryonic stem cell lines using a microdrop culture system. In Vitro Cell Dev Biol Anim 2010;46:236-241.
33. Cowan CA, Klimanskaya I, McMahon J, Atienza J, Witmyer J, Zucker JP, Wang S, Morton CC, McMahon AP, Powers D, Melton DA: Derivation of embryonic stem-cell lines from human blastocysts. New Engl J Med 2004;350:1353-1356.
34. Tay JI, Rutherford AJ, Killick SR, Maguiness SD, Partridge RJ, Leese HJ: Human tubal fluid: production, nutrient composition and response to adrenergic agents. Hum Reprod 1997;12:2451-2456.
35. Forsyth NR, Musio A, Vezzoni P, Simpson AHRW, Noble BS, McWhir J: Physiologic oxygen enhances human embryonic stem cell clonal recovery and reduces chromosomal abnormalities. Cloning Stem Cells 2006;8:16-23.
36. Mitchell JA, Yochim JM: Measurement of intrauterine oxygen tension in the rat and its regulation by ovarian steroid hormones. Endocrinology 1968;83:691-700.
37. Rodesch F, Simon P, Donner C, Jauniaux E: Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol 1992;80:283-285.
38. Fischer B, Bavister BD: Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil 1993;99:673-679.
39. Vander Heiden MG, Cantley LC, Thompson CB: Understanding the Warburg effect: The metabolic requirements of cell proliferation. Science 2009;324:1029-1033.
40. Locasale JW, Grassian AR, Melman T, Lyssiotis CA, Mattaini KR, Bass AJ, Heffron G, Metallo CM, Muranen T, Sharfi H, Sasaki AT, Anastasiou D, Mullarky E, Vokes NI, Sasaki M, Beroukhim R, Stephanopoulos G, Ligon AH, Meyerson M, Richardson AL, Chin L, Wagner G, Asara JM, Brugge JS, Cantley LC, Vander Heiden MG: Phosphoglycerate dehydrogenase diverts glycolytic flux and contributes to oncogenesis. Nat Genet 2011;43:869-874.
41. Possemato R, Marks KM, Shaul YD, Pacold ME, Kim D, Birsoy K, Sethumadhavan S, Woo H-K, Jang HG, Jha AK, Chen WW, Barrett FG, Stransky N, Tsun Z-Y, Cowley GS, Barretina J, Kalaany NY, Hsu PP, Ottina K, Chan AM, Yuan B, Garraway LA, Root DE, Mino-Kenudson M, Brachtel EF, Driggers EM, Sabatini DM: Functional genomics reveal that the serine synthesis pathway is essential in breast cancer. Nature 2011;476:346-350.
42. Zhang WC, Shyh-Chang N, Yang H, Rai A, Umashankar S, Ma S, Soh BS, Sun LL, Tai BC, Nga ME, Bhakoo KK, Jayapal SR, Nichane M, Yu Q, Ahmed DA, Tan C, Sing WP, Tam J, Thirugananam A, Noghabi MS, Pang YH, Ang HS, Mitchell W, Robson P, Kaldis P, Soo RA, Swarup S, Lim EH, Lim B: Glycine decarboxylase activity drives non-small cell lung cancer tumor-initiating cells and tumorigenesis. Cell 2012;148:259-272.
43. Maddocks ODK, Berkers CR, Mason SM, Zheng L, Blyth K, Gottlieb E, Vousden KH: Serine starvation induces stress and p53-dependent metabolic remodelling in cancer cells. Nature 2013;493:542-546.
44. Vacanti NM, Metallo CM: Exploring metabolic pathways that contribute to the stem cell phenotype. Biochim Biophys Acta 2013;1830:2361-2369.
45. Gwatkin RBL, Haidri AA: Requirements for the maturation of hamster oocytes in vitro. Exp Cell Res 1973;76:1-7.
46. Bavister BD, McKiernan SH: Regulation of Hamster Embryo Development In Vitro by Amino Acids; in Bavister BD, (ed): Preimplantation Embryo Development. New York, Springer, 1993, pp 57-72.
47. Broome JD: Studies on the mechanism of tumor inhibition by L-asparaginase. Effects of the enzyme on asparagine levels in the blood, normal tissues, and 6C3HED lymphomas of mice: differences in asparagine formation and utilization in asparaginase-sensitive and-resistant lymphoma cells. J Exp Med 1968;127:1055-1072.
48. Aslanian AM, Fletcher BS, Kilberg MS: Asparagine synthetase expression alone is sufficient to induce L-asparaginase resistance in MOLT-4 human leukaemia cells. Biochem J 2001;357:321-328.
49. Ameri K, Luong R, Zhang H, Powell AA, Montgomery KD, Espinosa I, Bouley DM, Harris AL, Jeffrey SS: Circulating tumour cells demonstrate an altered response to hypoxia and an aggressive phenotype. Br J Cancer 2010;102:561-569.
50. Balasubramanian M, Butterworth E, Kilberg M: Asparagine synthetase: regulation by cell stress and involvement in tumor biology. Am J Physiol-Endocrinol Metab 2013;304:E789-E799.
51. Xu C, Inokuma MS, Denham J, Golds K, Kundu P, Gold JD, Carpenter MK: Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 2001;19:971-974.
52. Amit M, Margulets V, Segev H, Shariki K, Laevsky I, Coleman R, Itskovitz-Eldor J: Human feeder layers for human embryonic stem cells. Biol Reprod 2003;68:2150-2156.