Role of ALKBH1 in the Core Transcriptional Network of Embryonic Stem Cells

Cellular Physiology and Biochemistry

Volumn 38, Issue 1, 2016, Pages 173-184

  Ougland, Rune ^a   Jonson, Ida ^a   Moen, Marivi Nabong ^a   Nesse, Gaute ^a   Asker, Gry ^c   Klungland, Arne ^a,b   Larsen, Elisabeth ^a  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c ULLEVÅL UNIVERSITY HOSPITAL   (Norway)

Author keywords

AlkB; AlkB homologs; ALKBH1; Embryonic stem cells; Epigenetics; Histone demethylation; Histone H2A; NANOG; Pluripotency; SOX2

Indexed keywords

ALKBH1 PROTEIN; DIOXYGENASE; MICRORNA; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; 5' UNTRANSLATED REGION; ALKBH1 PROTEIN, MOUSE; ALKYLATED DNA REPAIR PROTEIN ALKB HOMOLOG 1; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; HOMEODOMAIN PROTEIN; NANOG PROTEIN, MOUSE; OCTAMER TRANSCRIPTION FACTOR 4; POU5F1 PROTEIN, MOUSE; RECOMBINANT PROTEIN; SOX2 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC TRANSCRIPTION; IMMUNOCYTOCHEMISTRY; INVESTIGATIVE PROCEDURES; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; REGENERATIVE MEDICINE; 5' UNTRANSLATED REGION; ANIMAL; BINDING SITE; CELL LINE; CHEMISTRY; CYTOLOGY; DEFICIENCY; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE REGULATORY NETWORK; GENETICS; HUMAN; METABOLISM; MOUSE EMBRYONIC STEM CELL; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN;

5' UNTRANSLATED REGIONS; ALKB HOMOLOG 1, HISTONE H2A DIOXYGENASE; ANIMALS; BASE SEQUENCE; BINDING SITES; CELL DIFFERENTIATION; CELL LINE; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKOUT TECHNIQUES; GENE REGULATORY NETWORKS; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICRORNAS; MOUSE EMBRYONIC STEM CELLS; NANOG HOMEOBOX PROTEIN; OCTAMER TRANSCRIPTION FACTOR-3; PROMOTER REGIONS, GENETIC; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT PROTEINS; SOXB1 TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS;

EID: 84954449781     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000438619     Document Type: Article

References (47)

1. Falnes PO, Johansen RF, Seeberg E: AlkB-mediated oxidative demethylation reverses DNA damage in Escherichia coli. Nature 2002;419:178-182.
2. Trewick SC, Henshaw TF, Hausinger RP, Lindahl T, Sedgwick B: Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage. Nature 2002;419:174-178.
3. Li MM, Nilsen A, Shi Y, Fusser M, Ding YH, Fu Y, Liu B, Niu Y, Wu YS, Huang CM, Olofsson M, Jin KX, Lv Y, Xu XZ, He C, Dong MQ, Rendtlew Danielsen JM, Klungland A, Yang YG: ALKBH4-dependent demethylation of actin regulates actomyosin dynamics. Nat Commun 2013;4:1832.
4. Zheng G, Dahl JA, Niu Y, Fedorcsak P, Huang CM, Li CJ, Vagbo CB, Shi Y, Wang WL, Song SH, Lu Z, Bosmans RP, Dai Q, Hao YJ, Yang X, Zhao WM, Tong WM, Wang XJ, Bogdan F, Furu K, Fu Y, Jia G, Zhao X, Liu J, Krokan HE, Klungland A, Yang YG, He C: ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Mol Cell 2013;49:18-29.
5. Solberg A, Robertson AB, Aronsen JM, Rognmo O, Sjaastad I, Wisloff U, Klungland A: Deletion of mouse Alkbh7 leads to obesity. J Mol Cell Biol 2013;5:194-203.
6. Songe-Moller L, van den Born E, Leihne V, Vagbo CB, Kristoffersen T, Krokan HE, Kirpekar F, Falnes PO, Klungland A: Mammalian ALKBH8 possesses tRNA methyltransferase activity required for the biogenesis of multiple wobble uridine modifications implicated in translational decoding. Mol Cell Biol 2010;30:1814-1827.
7. van den Born E, Vagbo CB, Songe-Moller L, Leihne V, Lien GF, Leszczynska G, Malkiewicz A, Krokan HE, Kirpekar F, Klungland A, Falnes PO: ALKBH8-mediated formation of a novel diastereomeric pair of wobble nucleosides in mammalian tRNA. Nat Commun 2011;2:172.
8. Berulava T, Ziehe M, Klein-Hitpass L, Mladenov E, Thomale J, Ruther U, Horsthemke B: FTO levels affect RNA modification and the transcriptome. Eur J Hum Genet 2013;21:317-323.
9. Ougland R, Rognes T, Klungland A, Larsen E: Non-homologous functions of the AlkB homologs. J Mol Cell Biol 2015;7:494-504.
10. Ougland R, Lando D, Jonson I, Dahl JA, Moen MN, Nordstrand LM, Rognes T, Lee JT, Klungland A, Kouzarides T, Larsen E: ALKBH1 is a histone H2A dioxygenase involved in neural differentiation. Stem Cells 2012;30:2672-2682.
11. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R: Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 2003;17:126-140.
12. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A: Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003;113:643-655.
13. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Scholer H, Smith A: Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998;95:379-391.
14. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S: The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003;113:631-642.
15. Nakatake Y, Fukui N, Iwamatsu Y, Masui S, Takahashi K, Yagi R, Yagi K, Miyazaki J, Matoba R, Ko MS, Niwa H: Klf4 cooperates with Oct3/4 and Sox2 to activate the Lefty1 core promoter in embryonic stem cells. Mol Cell Biol 2006;26:7772-7782.
16. Adachi K, Suemori H, Yasuda SY, Nakatsuji N, Kawase E: Role of SOX2 in maintaining pluripotency of human embryonic stem cells. Genes Cells 2010;15:455-470.
17. Masui S, Nakatake Y, Toyooka Y, Shimosato D, Yagi R, Takahashi K, Okochi H, Okuda A, Matoba R, Sharov AA, Ko MS, Niwa H: Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat Cell Biol 2007;9:625-635.
18. Niwa H, Miyazaki J, Smith AG: Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 2000;24:372-376.
19. Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, Yagi R, Rossant J: Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 2005;123:917-929.
20. Fong H, Hohenstein KA, Donovan PJ: Regulation of self-renewal and pluripotency by Sox2 in human embryonic stem cells. Stem Cells 2008;26:1931-1938.
21. Zaehres H, Lensch MW, Daheron L, Stewart SA, Itskovitz-Eldor J, Daley GQ: High-efficiency RNA interference in human embryonic stem cells. Stem Cells 2005;23:299-305.
22. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, Gifford DK, Melton DA, Jaenisch R, Young RA: Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005;122:947-956.
23. Wong I, Lohman TM: A double-filter method for nitrocellulose-filter binding: application to protein-nucleic acid interactions. Proc Natl Acad Sci USA 1993;90:5428-5432.
24. Kunarso G, Chia NY, Jeyakani J, Hwang C, Lu X, Chan YS, Ng HH, Bourque G: Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet 2010;42:631-634.
25. Remenyi A, Lins K, Nissen LJ, Reinbold R, Scholer HR, Wilmanns M: Crystal structure of a POU/HMG/ DNA ternary complex suggests differential assembly of Oct4 and Sox2 on two enhancers. Genes Dev 2003;17:2048-2059.
26. Leonardo TR, Schultheisz HL, Loring JF, Laurent LC: The functions of microRNAs in pluripotency and reprogramming. Nat Cell Biol 2012;14:1114-1121.
27. Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, Johnstone S, Guenther MG, Johnston WK, Wernig M, Newman J, Calabrese JM, Dennis LM, Volkert TL, Gupta S, Love J, Hannett N, Sharp PA, Bartel DP, Jaenisch R, Young RA: Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 2008;134:521-533.
28. Chen Q, Xu J, Li L, Li H, Mao S, Zhang F, Zen K, Zhang CY, Zhang Q: MicroRNA-23a/b and microRNA-27a/b suppress Apaf-1 protein and alleviate hypoxia-induced neuronal apoptosis. Cell Death Dis 2014;5:e1132.
29. Tay Y, Zhang J, Thomson AM, Lim B, Rigoutsos I: MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 2008;455:1124-1128.
30. Nordstrand LM, Svard J, Larsen E, Nilsen A, Ougland R, Furu K, Lien GF, Rognes T, Namekawa SH, Lee JT, Klungland A: Mice lacking Alkbh1 display sex-ratio distortion and unilateral eye defects. PLoS One 2010;5:e13827.
31. Loh YH, Yang L, Yang JC, Li H, Collins JJ, Daley GQ: Genomic approaches to deconstruct pluripotency. Annu Rev Genomics Hum Genet 2011;12:165-185.
32. Loh YH, Zhang W, Chen X, George J, Ng HH: Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate selfrenewal in embryonic stem cells. Genes Dev 2007;21:2545-2557.
33. Liang G, Zhang Y: Embryonic stem cell and induced pluripotent stem cell: an epigenetic perspective. Cell Res 2013;23:49-69.
34. Ma Y, Li C, Gu J, Tang F, Li C, Li P, Ping P, Yang S, Li Z, Jin Y: Aberrant gene expression profiles in pluripotent stem cells induced from fibroblasts of a Klinefelter syndrome patient. J Biol Chem 2012;287:38970-38979.
35. Wang XM, Yik WY, Zhang P, Lu W, Dranchak PK, Shibata D, Steinberg SJ, Hacia JG: The gene expression profiles of induced pluripotent stem cells from individuals with childhood cerebral adrenoleukodystrophy are consistent with proposed mechanisms of pathogenesis. Stem Cell Res Ther 2012;3:39.
36. Liu GH, Qu J, Suzuki K, Nivet E, Li M, Montserrat N, Yi F, Xu X, Ruiz S, Zhang W, Wagner U, Kim A, Ren B, Li Y, Goebl A, Kim J, Soligalla RD, Dubova I, Thompson J, Yates J, III, Esteban CR, Sancho-Martinez I, Izpisua Belmonte JC: Progressive degeneration of human neural stem cells caused by pathogenic LRRK2. Nature 2012;491:603-607.
37. Guenther MG, Frampton GM, Soldner F, Hockemeyer D, Mitalipova M, Jaenisch R, Young RA: Chromatin structure and gene expression programs of human embryonic and induced pluripotent stem cells. Cell Stem Cell 2010;7:249-257.
38. Bar M, Wyman SK, Fritz BR, Qi J, Garg KS, Parkin RK, Kroh EM, Bendoraite A, Mitchell PS, Nelson AM, Ruzzo WL, Ware C, Radich JP, Gentleman R, Ruohola-Baker H, Tewari M: MicroRNA discovery and profiling in human embryonic stem cells by deep sequencing of small RNA libraries. Stem Cells 2008;26:2496-2505.
39. Kanellopoulou C, Muljo SA, Kung AL, Ganesan S, Drapkin R, Jenuwein T, Livingston DM, Rajewsky K: Dicerdeficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 2005;19:489-501.
40. Anokye-Danso F, Trivedi CM, Juhr D, Gupta M, Cui Z, Tian Y, Zhang Y, Yang W, Gruber PJ, Epstein JA, Morrisey EE: Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 2011;8:376-388.
41. Miyoshi N, Ishii H, Nagano H, Haraguchi N, Dewi DL, Kano Y, Nishikawa S, Tanemura M, Mimori K, Tanaka F, Saito T, Nishimura J, Takemasa I, Mizushima T, Ikeda M, Yamamoto H, Sekimoto M, Doki Y, Mori M: Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Cell Stem Cell 2011;8:633-638.
42. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A, Waldvogel B, Vannier C, Darling D, zur HA, Brunton VG, Morton J, Sansom O, Schuler J, Stemmler MP, Herzberger C, Hopt U, Keck T, Brabletz S, Brabletz T: The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 2009;11:1487-1495.
43. Woltering JM, Durston AJ: MiR-10 represses HoxB1a and HoxB3a in zebrafish. PLoS One 2008;3:e1396.
44. Liao X, Xue H, Wang YC, Nazor KL, Guo S, Trivedi N, Peterson SE, Liu Y, Loring JF, Laurent LC: Matched miRNA and mRNA signatures from an hESC-based in vitro model of pancreatic differentiation reveal novel regulatory interactions. J Cell Sci 2013;126:3848-3861.
45. Rogler CE, Levoci L, Ader T, Massimi A, Tchaikovskaya T, Norel R, Rogler LE: MicroRNA-23b cluster microRNAs regulate transforming growth factor-beta/bone morphogenetic protein signaling and liver stem cell differentiation by targeting Smads. Hepatology 2009;50:575-584.
46. McGinnis W, Krumlauf R: Homeobox genes and axial patterning. Cell 1992;68:283-302.
47. Muller TA, Yu K, Hausinger RP, Meek K: ALKBH1 is dispensable for abasic site cleavage during base excision repair and class switch recombination. PLoS One 2013;8:e67403.