Influence of amino acid metabolism on embryonic stem cell function and differentiation

Advances in Nutrition

Volumn 7, Issue 4, 2016, Pages 780S-789S

  Kilberg, Michael S ^a   Terada, Naohiro ^a   Shan, Jixiu ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Amino acids; Differentiation; Primary germ layers; Protein metabolism; Stem cells

Indexed keywords

AMINO ACID; METHIONINE; PROLINE; THREONINE;

ACETYLATION; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; EMBRYONIC STEM CELL; ENERGY METABOLISM; GENETIC EPIGENESIS; HUMAN; METABOLISM; METHYLATION; MOUSE; PHYSIOLOGY; PROCEDURES; REGENERATIVE MEDICINE;

ACETYLATION; AMINO ACIDS; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; ENERGY METABOLISM; EPIGENESIS, GENETIC; HUMANS; METHIONINE; METHYLATION; MICE; PROLINE; REGENERATIVE MEDICINE; THREONINE;

EID: 85015265776     PISSN: 21618313     EISSN: 21565376     Source Type: Journal    
DOI: 10.3945/an.115.011031     Document Type: Article

References (65)

1. Burton A, Torres-Padilla ME. Chromatin dynamics in the regulation of cell fate allocation during early embryogenesis. Nat Rev Mol Cell Biol 2014;15:723-34.
2. Keller G. Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev 2005;19:1129-55.
3. Tam PP, Loebel DA. Gene function in mouse embryogenesis: get set for gastrulation. Nat Rev Genet 2007;8:368-81.
4. Tan BS, Lonic A, Morris MB, Rathjen PD, Rathjen J. The amino acid transporter SNAT2 mediates L-proline-induced differentiation of ES cells. Am J Physiol Cell Physiol 2011;300:C1270-9.
5. Hackett JA, Surani MA. DNA methylation dynamics during the mammalian life cycle. Philos Trans R Soc Lond B Biol Sci 2013;368: 20110328.
6. Seisenberger S, Peat JR, Hore TA, Santos F, Dean W, Reik W. Reprogramming DNA methylation in the mammalian life cycle: building and breaking epigenetic barriers. Philos Trans R Soc Lond B Biol Sci 2013; 368:20110330.
7. Kraushaar DC, Zhao K. The epigenomics of embryonic stem cell differentiation. Int J Biol Sci 2013;9:1134-44.
8. Thiagarajan RD, Morey R, Laurent LC. The epigenome in pluripotency and differentiation. Epigenomics 2014;6:121-37.
9. Boland MJ, Nazor KL, Loring JF. Epigenetic regulation of pluripotency and differentiation. Circ Res 2014;115:311-24.
10. Li X, Li L, Pandey R, Byun JS, Gardner K, Qin Z, Dou Y. The histone acetyltransferase MOF is a key regulator of the embryonic stem cell core transcriptional network. Cell Stem Cell 2012;11:163-78.
11. Gifford CA, Ziller MJ, Gu H, Trapnell C, Donaghey J, Tsankov A, Shalek AK, Kelley DR, Shishkin AA, Issner R, et al. Transcriptional and epigenetic dynamics during specification of human embryonic stem cells. Cell 2013;153:1149-63.
12. Turinetto V, Giachino C. Histone variants as emerging regulators of embryonic stem cell identity. Epigenetics 2015;10:563-73.
13. Hu G, Cui K, Northrup D, Liu C, Wang C, Tang Q, Ge K, Levens D, Crane-Robinson C, Zhao K. H2A.Z facilitates access of active and repressive complexes to chromatin in embryonic stem cell self-renewal and differentiation. Cell Stem Cell 2013;12:180-92.
14. Banaszynski LA, Wen D, Dewell S, Whitcomb SJ, Lin M, Diaz N, Elsasser SJ, Chapgier A, Goldberg AD, Canaani E, et al. Hira-dependent histone H3.3 deposition facilitates PRC2 recruitment at developmental loci in ES cells. Cell 2013;155:107-20.
15. Wang J, Alexander P, Wu L, Hammer R, Cleaver O, McKnight SL. Dependence of mouse embryonic stem cells on threonine catabolism. Science 2009;325:435-9.
16. Wang J, Alexander P, McKnight SL. Metabolic specialization of mouse embryonic stem cells. Cold Spring Harb Symp Quant Biol 2011;76:183-93.
17. Chen G, Wang J. Threonine metabolism and embryonic stem cell self-renewal. Curr Opin Clin Nutr Metab Care 2014;17:80-5.
18. Amit M, Carpenter MK, Inokuma MS, Chiu CP, Harris CP, Waknitz MA, Itskovitz-Eldor J, Thomson JA. Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol 2000;227:271-8.
19. Gaspar JA, Doss MX, Hengstler JG, Cadenas C, Hescheler J, Sachinidis A. Unique metabolic features of stem cells, cardiomyocytes, and their progenitors. Circ Res 2014;114:1346-60.
20. Gardner DK. Changes in requirements and utilization of nutrients during mammalian preimplantation embryo development and their significance in embryo culture. Theriogenology 1998;49:83-102.
21. Washington JM, Rathjen J, Felquer F, Lonic A, Bettess MD, Hamra N, Semendric L, Tan BS, Lake JA, Keough RA, et al. L-Proline induces differentiation of ES cells: a novel role for an amino acid in the regulation of pluripotent cells in culture. Am J Physiol Cell Physiol 2010;298:C982-92.
22. Palii SS, Thiaville MM, Pan YX, Zhong C, Kilberg MS. Characterization of the amino acid response element within the human sodium-coupled neutral amino acid transporter 2 (SNAT2) system A transporter gene. Biochem J 2006;395:517-27.
23. Casalino L, Comes S, Lambazzi G, De Stefano B, Filosa S, De Falco S, De Cesare D, Minchiotti G, Patriarca EJ. Control of embryonic stem cell metastability by L-proline catabolism. J Mol Cell Biol 2011;3:108-22.
24. Comes S, Gagliardi M, Laprano N, Fico A, Cimmino A, Palamidessi A, De Cesare D, De Falco S, Angelini C, Scita G, et al. L-proline induces a mesenchymal-like invasive program in embryonic stem cells by remodeling H3K9 and H3K36 methylation. Stem Cell Reports 2013;1:307-21.
25. Phang JM, Liu W, Hancock C, Christian KJ. The proline regulatory axis and cancer. Front Oncol 2012;2:60.
26. Liu W, Le A, Hancock C, Lane AN, Dang CV, Fan TW, Phang JM. Reprogramming of proline and glutamine metabolism contributes to the proliferative and metabolic responses regulated by oncogenic transcription factor c-MYC. Proc Natl Acad Sci USA 2012;109:8983-8.
27. Simmons JM, Muller TA, Hausinger RP. Fe(II)/alpha-ketoglutarate hydroxylases involved in nucleobase, nucleoside, nucleotide, and chromatin metabolism. Dalton Trans 2008;5132-42.
28. Samavarchi-Tehrani P, Golipour A, David L, Sung HK, Beyer TA, Datti A, Woltjen K, Nagy A, Wrana JL. Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell 2010;7:64-77.
29. Li R, Liang J, Ni S, Zhou T, Qing X, Li H, He W, Chen J, Li F, Zhuang Q, et al. A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts. Cell Stem Cell 2010;7:51-63.
30. Wang T, Chen K, Zeng X, Yang J, Wu Y, Shi X, Qin B, Zeng L, Esteban MA, Pan G, et al. The histone demethylases Jhdm1a/1b enhance somatic cell reprogramming in a vitamin-C-dependent manner. Cell Stem Cell 2011;9:575-87.
31. Shan J, Lopez MC, Baker HV, Kilberg MS. Expression profiling after activation of the amino acid deprivation response in HepG2 human hepatoma cells. Physiol Genomics 2010;41:315-27.
32. Shan J, Fu L, Balasubramanian MN, Anthony T, Kilberg MS. ATF4-dependent regulation of the JMJD3 gene during amino acid deprivation can be rescued in Atf4-deficient cells by inhibition of deacetylation. J Biol Chem 2012;287:36393-403.
33. Miller SA, Mohn SE, Weinmann AS. Jmjd3 and UTX play a demethylase-independent role in chromatin remodeling to regulate T-box family member-dependent gene expression. Mol Cell 2010;40:594-605.
34. Date Y, Hasegawa S, Yamada T, Inoue Y, Mizutani H, Nakata S, Akamatsu H. Major amino acids in collagen hydrolysate regulate the differentiation of mouse embryoid bodies. J Biosci Bioeng 2013; 116:386-90.
35. Sato H, Takahashi M, Ise H, Yamada A, Hirose S, Tagawa Y, Morimoto H, Izawa A, Ikeda U. Collagen synthesis is required for ascorbic acid-enhanced differentiation of mouse embryonic stem cells into cardiomyocytes. Biochem Biophys Res Commun 2006;342:107-12.
36. Alexander PB, Wang J, McKnight SL. Targeted killing of a mammalian cell based upon its specialized metabolic state. Proc Natl Acad Sci USA 2011;108:15828-33.
37. Shyh-Chang N, Locasale JW, Lyssiotis CA, Zheng Y, Teo RY, Ratanasirintrawoot S, Zhang J, Onder T, Unternaehrer JJ, Zhu H, et al. Influence of threonine metabolism on S-adenosylmethionine and histone methylation. Science 2013;339:222-6.
38. Ryu JM, Han HJ. L-threonine regulates G1/S phase transition of mouse embryonic stem cells via PI3K/Akt, MAPKs, and mTORC pathways. J Biol Chem 2011;286:23667-78.
39. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006;125:315-26.
40. Han C, Gu H, Wang J, Lu W, Mei Y, Wu M. Regulation of L-threonine dehydrogenase in somatic cell reprogramming. Stem Cells 2013;31:953-65.
41. Edgar AJ. The human L-threonine 3-dehydrogenase gene is an expressed pseudogene. BMC Genet 2002;3:18.
42. Shiraki N, Shiraki Y, Tsuyama T, Obata F, Miura M, Nagae G, Aburatani H, Kume K, Endo F, Kume S. Methionine metabolism regulates maintenance and differentiation of human pluripotent stem cells. Cell Metab 2014;19:780-94.
43. Figueras F, Gardosi J. Intrauterine growth restriction: new concepts in antenatal surveillance, diagnosis, and management. Am J Obstet Gynecol 2011;204:288-300.
44. Brown LD, Green AS, Limesand SW, Rozance PJ. Maternal amino acid supplementation for intrauterine growth restriction. Front Biosci (Schol Ed) 2011;3:428-44.
45. Yung HW, Calabrese S, Hynx D, Hemmings BA, Cetin I, Charnock-Jones DS, Burton GJ. Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human intrauterine growth restriction. Am J Pathol 2008;173:451-62.
46. Kilberg MS, Balasubramanian M, Fu L, Shan J. The transcription factor network associated with the amino acid response in mammalian cells. Adv Nutr 2012;3:295-306.
47. Kilberg MS, Shan J, Su N. ATF4-dependent transcription mediates signaling of amino acid limitation. Trends Endocrinol Metab 2009; 20:436-43.
48. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 2000;6:1099-108.
49. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 2005;135:1382-6.
50. Barker DJ. The origins of the developmental origins theory. J Intern Med 2007;261:412-7.
51. Shi L, Wu J. Epigenetic regulation in mammalian preimplantation embryo development. Reprod Biol Endocrinol 2009;7:59.
52. Christophersen NS, Helin K. Epigenetic control of embryonic stem cell fate. J Exp Med 2010;207:2287-95.
53. Shan J, Hamazaki T, Tang TA, Terada N, Kilberg MS. Activation of the amino acid response modulates lineage specification during differentiation of murine embryonic stem cells. Am J Physiol Endocrinol Metab 2013;305:E325-35.
54. Kimball SR. Regulation of global and specific mRNA translation by amino acids. J Nutr 2002;132:883-6.
55. Pfister S, Steiner KA, Tam PP. Gene expression pattern and progression of embryogenesis in the immediate post-implantation period of mouse development. Gene Expr Patterns 2007;7:558-73.
56. Wek RC, Cavener DR. Translational control and the unfolded protein response. Antioxid Redox Signal 2007;9:2357-71.
57. Dang Do AN, Kimball SR, Cavener DR, Jefferson LS. eIF2alpha kinases GCN2 and PERK modulate transcription and translation of distinct sets of mRNAs in mouse liver. Physiol Genomics 2009;38:328-41.
58. Xu H, Tsang KS, Wang Y, Chan JC, Xu G, Gao WQ. Unfolded protein response is required for the definitive endodermal specification of mouse embryonic stem cells via Smad2 and beta-catenin signaling. J Biol Chem 2014;289:26290-301.
59. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 2000;5:897-904.
60. Werner JC, Sicard RE. Lactate metabolism of isolated, perfused fetal, and newborn pig hearts. Pediatr Res 1987;22:552-6.
61. Tohyama S, Hattori F, Sano M, Hishiki T, Nagahata Y, Matsuura T, Hashimoto H, Suzuki T, Yamashita H, Satoh Y, et al. Distinct metabolic flow enables large-scale purification of mouse and human pluripotent stem cell-derived cardiomyocytes. Cell Stem Cell 2013;12:127-37.
62. Tomizawa M, Toyama Y, Ito C, Toshimori K, Iwase K, Takiguchi M, Saisho H, Yokosuka O. Hepatoblast-like cells enriched from mouse embryonic stem cells in medium without glucose, pyruvate, arginine, and tyrosine. Cell Tissue Res 2008;333:17-27.
63. Rachdi L, Aiello V, Duvillie B, Scharfmann R. L-leucine alters pancreatic beta-cell differentiation and function via the mTor signaling pathway. Diabetes 2012;61:409-17.
64. Oburoglu L, Tardito S, Fritz V, de Barros SC, Merida P, Craveiro M, Mamede J, Cretenet G, Mongellaz C, An X, et al. Glucose and glutamine metabolism regulate human hematopoietic stem cell lineage specification. Cell Stem Cell 2014;15:169-84.
65. Shyh-Chang N, Daley GQ, Cantley LC. Stem cell metabolism in tissue development and aging. Development 2013;140:2535-47.