Erk signaling is indispensable for genomic stability and self-renewal of mouse embryonic stem cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 44, 2015, Pages E5936-E5943

  Chen, Haixia ^a   Guo, Renpeng ^a   Zhang, Qian ^a   Guo, Hongchao ^a   Yang, Meng ^a   Wu, Zhenfeng ^a   Gao, Shan ^a   Liu, Lin ^a   Chen, Lingyi ^a,b  

^a NANKAI UNIVERSITY   (China)

^b PEKING UNION MEDICAL COLLEGE   (China)

Author keywords

Embryonic stem cells; Erk; Genomic stability; Mek; Self renewal

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR NANOG; HOMEODOMAIN PROTEIN; NANOG PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; EMBRYONIC STEM CELL; G1 PHASE CELL CYCLE CHECKPOINT; GENOMIC INSTABILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING; ANIMAL; CELL CYCLE; CYTOLOGY; ENZYMOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; TELOMERE;

ANIMALS; CELL CYCLE; CELL DEATH; EMBRYONIC STEM CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENOMIC INSTABILITY; HOMEODOMAIN PROTEINS; MICE; MICE, KNOCKOUT; NANOG HOMEOBOX PROTEIN; SIGNAL TRANSDUCTION; TELOMERE;

EID: 84946550104     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1516319112     Document Type: Article

References (64)

1. Jaenisch R, Young R (2008) Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132(4):567-582.
2. Young RA (2011) Control of the embryonic stem cell state. Cell 144(6):940-954.
3. Boyer LA, et al. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122(6):947-956.
4. Loh YH, et al. (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38(4):431-440.
5. Raz R, Lee CK, Cannizzaro LA, d'Eustachio P, Levy DE (1999) Essential role of STAT3 for embryonic stem cell pluripotency. Proc Natl Acad Sci USA 96(6):2846-2851.
6. Niwa H, Burdon T, Chambers I, Smith A (1998) Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev 12(13): 2048-2060.
7. Ying QL, Nichols J, Chambers I, Smith A (2003) BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115(3):281-292.
8. Shaul YD, Seger R (2007) The MEK/ERK cascade: From signaling specificity to diverse functions. Biochim Biophys Acta 1773(8):1213-1226.
9. Pearson G, et al. (2001) Mitogen-activated protein (MAP) kinase pathways: Regulation and physiological functions. Endocr Rev 22(2):153-183.
10. Burdon T, Stracey C, Chambers I, Nichols J, Smith A (1999) Suppression of SHP-2 and ERK signalling promotes self-renewal of mouse embryonic stem cells. Dev Biol 210(1): 30-43.
11. Ying QL, et al. (2008) The ground state of embryonic stem cell self-renewal. Nature 453(7194):519-523.
12. Zhou H, et al. (2010) Conversion of mouse epiblast stem cells to an earlier pluripotency state by small molecules. J Biol Chem 285(39):29676-29680.
13. Gafni O, et al. (2013) Derivation of novel human ground state naive pluripotent stem cells. Nature 504(7479):282-286.
14. Chan YS, et al. (2013) Induction of a human pluripotent state with distinct regulatory circuitry that resembles preimplantation epiblast. Cell Stem Cell 13(6):663-675.
15. Takashima Y, et al. (2014) Resetting transcription factor control circuitry toward ground-state pluripotency in human. Cell 158(6):1254-1269.
16. Theunissen TW, et al. (2014) Systematic identification of culture conditions for induction and maintenance of naive human pluripotency. Cell Stem Cell 15(4):471-487.
17. Lu CW, et al. (2008) Ras-MAPK signaling promotes trophectoderm formation from embryonic stem cells and mouse embryos. Nat Genet 40(7):921-926.
18. Kunath T, et al. (2007) FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 134(16):2895-2902.
19. Stavridis MP, Lunn JS, Collins BJ, Storey KG (2007) A discrete period of FGF-induced Erk1/2 signalling is required for vertebrate neural specification. Development 134(16): 2889-2894.
20. Kim MO, et al. (2012) ERK1 and ERK2 regulate embryonic stem cell self-renewal through phosphorylation of Klf4. Nat Struct Mol Biol 19(3):283-290.
21. Brumbaugh J, et al. (2014) NANOG is multiply phosphorylated and directly modified by ERK2 and CDK1 in vitro. Stem Cell Rep 2(1):18-25.
22. Kim SH, et al. (2014) ERK1 phosphorylates Nanog to regulate protein stability and stem cell self-renewal. Stem Cell Res (Amst) 13(1):1-11.
23. Tee WW, Shen SS, Oksuz O, Narendra V, Reinberg D (2014) Erk1/2 activity promotes chromatin features and RNAPII phosphorylation at developmental promoters in mouse ESCs. Cell 156(4):678-690.
24. Thomson JA, et al. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282(5391):1145-1147.
25. Göke J, Chan YS, Yan J, Vingron M, Ng HH (2013) Genome-wide kinase-chromatin interactions reveal the regulatory network of ERK signaling in human embryonic stem cells. Mol Cell 50(6):844-855.
26. Brons IG, et al. (2007) Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448(7150):191-195.
27. Tesar PJ, et al. (2007) New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448(7150):196-199.
28. Tang Z, et al. (2015) MEK guards proteome stability and inhibits tumor-suppressive amyloidogenesis via HSF1. Cell 160(4):729-744.
29. Saba-El-Leil MK, et al. (2003) An essential function of the mitogen-activated protein kinase Erk2 in mouse trophoblast development. EMBO Rep 4(10):964-968.
30. Hamilton WB, Kaji K, Kunath T (2013) ERK2 suppresses self-renewal capacity of embryonic stem cells, but is not required for multi-lineage commitment. PLoS One 8(4): e60907.
31. Yao Y, et al. (2003) Extracellular signal-regulated kinase 2 is necessary for mesoderm differentiation. Proc Natl Acad Sci USA 100(22):12759-12764.
32. Pagès G, et al. (1999) Defective thymocyte maturation in p44 MAP kinase (Erk 1) knockout mice. Science 286(5443):1374-1377.
33. Silva J, et al. (2009) Nanog is the gateway to the pluripotent ground state. Cell 138(4): 722-737.
34. Frémin C, Saba-El-Leil MK, Lévesque K, Ang SL, Meloche S (2015) Functional redundancy of ERK1 and ERK2 MAP kinases during development. Cell Reports 12(6): 913-921.
35. Beard C, Hochedlinger K, Plath K, Wutz A, Jaenisch R (2006) Efficient method to generate single-copy transgenic mice by site-specific integration in embryonic stem cells. Genesis 44(1):23-28.
36. Ying QL, Stavridis M, Griffiths D, Li M, Smith A (2003) Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol 21(2): 183-186.
37. Fey D, Croucher DR, Kolch W, Kholodenko BN (2012) Crosstalk and signaling switches in mitogen-activated protein kinase cascades. Front Physiol 3:355.
38. Lee JH, et al. (2013) p38 MAP kinase and ERK play an important role in nitric oxideinduced apoptosis of the mouse embryonic stem cells. Toxicol In Vitro 27(1):492-498.
39. Weissbein U, Benvenisty N, Ben-David U (2014) Quality control: Genome maintenance in pluripotent stem cells. J Cell Biol 204(2):153-163.
40. Feldser DM, Hackett JA, Greider CW (2003) Telomere dysfunction and the initiation of genome instability. Nat Rev Cancer 3(8):623-627.
41. McEachern MJ, Krauskopf A, Blackburn EH (2000) Telomeres and their control. Annu Rev Genet 34:331-358.
42. Greider CW, Blackburn EH (1987) The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity. Cell 51(6):887-898.
43. Wang F, et al. (2012) Molecular insights into the heterogeneity of telomere reprogramming in induced pluripotent stem cells. Cell Res 22(4):757-768.
44. Niida H, et al. (1998) Severe growth defect in mouse cells lacking the telomerase RNA component. Nat Genet 19(2):203-206.
45. Savatier P, Lapillonne H, Jirmanova L, Vitelli L, Samarut J (2002) Analysis of the cell cycle in mouse embryonic stem cells. Methods Mol Biol 185:27-33.
46. Lavoie JN, L'Allemain G, Brunet A, Müller R, Pouysségur J (1996) Cyclin D1 expression is regulated positively by the p42/p44MAPK and negatively by the p38/HOGMAPK pathway. J Biol Chem 271(34):20608-20616.
47. Jirmanova L, Afanassieff M, Gobert-Gosse S, Markossian S, Savatier P (2002) Differential contributions of ERK and PI3-kinase to the regulation of cyclin D1 expression and to the control of the G1/S transition in mouse embryonic stem cells. Oncogene 21(36):5515-5528.
48. Savatier P, Lapillonne H, van Grunsven LA, Rudkin BB, Samarut J (1996) Withdrawal of differentiation inhibitory activity/leukemia inhibitory factor up-regulates D-type cyclins and cyclin-dependent kinase inhibitors in mouse embryonic stem cells. Oncogene 12(2):309-322.
49. Savatier P, Huang S, Szekely L, Wiman KG, Samarut J (1994) Contrasting patterns of retinoblastoma protein expression in mouse embryonic stem cells and embryonic fibroblasts. Oncogene 9(3):809-818.
50. Stead E, et al. (2002) Pluripotent cell division cycles are driven by ectopic Cdk2, cyclin A/E and E2F activities. Oncogene 21(54):8320-8333.
51. Burdon T, Smith A, Savatier P (2002) Signalling, cell cycle and pluripotency in embryonic stem cells. Trends Cell Biol 12(9):432-438.
52. Schneider RP, et al. (2013) TRF1 is a stem cell marker and is essential for the generation of induced pluripotent stem cells. Nat Commun 4:1946.
53. Allsopp RC, et al. (1992) Telomere length predicts replicative capacity of human fibroblasts. Proc Natl Acad Sci USA 89(21):10114-10118.
54. Iwano T, Tachibana M, Reth M, Shinkai Y (2004) Importance of TRF1 for functional telomere structure. J Biol Chem 279(2):1442-1448.
55. Martínez P, et al. (2009) Increased telomere fragility and fusions resulting from TRF1 deficiency lead to degenerative pathologies and increased cancer in mice. Genes Dev 23(17):2060-2075.
56. Marzec P, et al. (2015) Nuclear-receptor-mediated telomere insertion leads to genome instability in ALT cancers. Cell 160(5):913-927.
57. Niwa H, Ogawa K, Shimosato D, Adachi K (2009) A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells. Nature 460(7251):118-122.
58. Fritsche-Guenther R, et al. (2011) Strong negative feedback from Erk to Raf confers robustness to MAPK signalling. Mol Syst Biol 7:489.
59. Sturm OE, et al. (2010) The mammalian MAPK/ERK pathway exhibits properties of a negative feedback amplifier. Sci Signal 3(153):ra90.
60. Li Z, et al. (2012) BMP4 signaling acts via dual-specificity phosphatase 9 to control ERK activity in mouse embryonic stem cells. Cell Stem Cell 10(2):171-182.
61. Huang J, et al. (2011) Association of telomere length with authentic pluripotency of ES/iPS cells. Cell Res 21(5):779-792.
62. Levin-Salomon V, Kogan K, Ahn NG, Livnah O, Engelberg D (2008) Isolation of intrinsically active (MEK-independent) variants of the ERK family of mitogen-activated protein (MAP) kinases. J Biol Chem 283(50):34500-34510.
63. Schramek H, Feifel E, Healy E, Pollack V (1997) Constitutively active mutant of the mitogen-activated protein kinase kinase MEK1 induces epithelial dedifferentiation and growth inhibition in Madin-Darby canine kidney-C7 cells. J Biol Chem 272(17): 11426-11433.
64. Huang P, et al. (2011) Heritable gene targeting in zebrafish using customized TALENs. Nat Biotechnol 29(8):699-700.