An Apela RNA-Containing Negative Feedback Loop Regulates p53-Mediated Apoptosis in Embryonic Stem Cells

Cell Stem Cell

Volumn 16, Issue 6, 2015, Pages 669-683

  Li, Mangmang ^a   Gou, Hongfeng ^a   Tripathi, Brajendra K ^a   Huang, Jing ^a,b   Jiang, Shunlin ^a   Dubois, Wendy ^a   Waybright, Tim ^c   Lei, Ming ^b   Shi, Jianxin ^a   Zhou, Ming ^c  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APELIN RECEPTOR EARLY ENDOGENOUS LIGAND; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN L; PEPTIDES AND PROTEINS; PROTEIN P53; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; PROTEIN BINDING; RNA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA DAMAGE INDUCED APOPTOSIS; EMBRYO; EMBRYONIC STEM CELL; ENHANCER REGION; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; 3' UNTRANSLATED REGION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CYTOLOGY; DNA DAMAGE; FEEDBACK SYSTEM; GENE LOCUS; GENETICS; METABOLISM; MITOCHONDRION; MOLECULAR GENETICS; MOUSE EMBRYONIC STEM CELL; NUCLEOTIDE SEQUENCE; OPEN READING FRAME;

3' UNTRANSLATED REGIONS; AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BASE SEQUENCE; DNA DAMAGE; ENHANCER ELEMENTS, GENETIC; FEEDBACK, PHYSIOLOGICAL; GENETIC LOCI; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; MICE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MOUSE EMBRYONIC STEM CELLS; OPEN READING FRAMES; PROTEIN BINDING; RNA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84931285961     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2015.04.002     Document Type: Article

References (36)

1. S.L. Berger The complex language of chromatin regulation during transcription Nature 447 2007 407 412
2. R.B. Cervantes, J.R. Stringer, C. Shao, J.A. Tischfield, and P.J. Stambrook Embryonic stem cells and somatic cells differ in mutation frequency and type Proc. Natl. Acad. Sci. USA 99 2002 3586 3590
3. A. Chaudhury, P. Chander, and P.H. Howe Heterogeneous nuclear ribonucleoproteins (hnRNPs) in cellular processes: Focus on hnRNP E1's multifunctional regulatory roles RNA 16 2010 1449 1462
4. X. Chen, H. Xu, P. Yuan, F. Fang, M. Huss, V.B. Vega, E. Wong, Y.L. Orlov, W. Zhang, J. Jiang, and et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells Cell 133 2008 1106 1117
5. S.C. Chng, L. Ho, J. Tian, and B. Reversade ELABELA: a hormone essential for heart development signals via the apelin receptor Dev. Cell 27 2013 672 680
6. S. Cinghu, S. Yellaboina, J.M. Freudenberg, S. Ghosh, X. Zheng, A.J. Oldfield, B.L. Lackford, D.V. Zaykin, G. Hu, and R. Jothi Integrative framework for identification of key cell identity genes uncovers determinants of ES cell identity and homeostasis Proc. Natl. Acad. Sci. USA 111 2014 E1581 E1590
7. L.A. Donehower, M. Harvey, B.L. Slagle, M.J. McArthur, C.A. Montgomery Jr., J.S. Butel, and A. Bradley Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours Nature 356 1992 215 221
8. R. Dumitru, V. Gama, B.M. Fagan, J.J. Bower, V. Swahari, L.H. Pevny, and M. Deshmukh Human embryonic stem cells have constitutively active Bax at the Golgi and are primed to undergo rapid apoptosis Mol. Cell 46 2012 573 583
9. A.M. Goh, C.Y. Lim, P.C. Chiam, L. Li, M.B. Mann, K.M. Mann, S. Menendez, and D.P. Lane Using targeted transgenic reporter mice to study promoter-specific p53 transcriptional activity Proc. Natl. Acad. Sci. USA 109 2012 1685 1690
10. M.K. Han, E.K. Song, Y. Guo, X. Ou, C. Mantel, and H.E. Broxmeyer SIRT1 regulates apoptosis and Nanog expression in mouse embryonic stem cells by controlling p53 subcellular localization Cell Stem Cell 2 2008 241 251
11. N.D. Heintzman, R.K. Stuart, G. Hon, Y. Fu, C.W. Ching, R.D. Hawkins, L.O. Barrera, S. Van Calcar, C. Qu, K.A. Ching, and et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome Nat. Genet. 39 2007 311 318
12. Y. Hong, and P.J. Stambrook Restoration of an absent G1 arrest and protection from apoptosis in embryonic stem cells after ionizing radiation Proc. Natl. Acad. Sci. USA 101 2004 14443 14448
13. M. Huarte, M. Guttman, D. Feldser, M. Garber, M.J. Koziol, D. Kenzelmann-Broz, A.M. Khalil, O. Zuk, I. Amit, M. Rabani, and et al. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response Cell 142 2010 409 419
14. J. Hui, L.H. Hung, M. Heiner, S. Schreiner, N. Neumüller, G. Reither, S.A. Haas, and A. Bindereif Intronic CA-repeat and CA-rich elements: a new class of regulators of mammalian alternative splicing EMBO J. 24 2005 1988 1998
15. T. Hung, Y. Wang, M.F. Lin, A.K. Koegel, Y. Kotake, G.D. Grant, H.M. Horlings, N. Shah, C. Umbricht, P. Wang, and et al. Extensive and coordinated transcription of noncoding RNAs within cell-cycle promoters Nat. Genet. 43 2011 621 629
16. N.T. Ingolia, L.F. Lareau, and J.S. Weissman Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes Cell 147 2011 789 802
17. S.N. Jones, A.E. Roe, L.A. Donehower, and A. Bradley Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53 Nature 378 1995 206 208
18. M.H. Kagey, J.J. Newman, S. Bilodeau, Y. Zhan, D.A. Orlando, N.L. van Berkum, C.C. Ebmeier, J. Goossens, P.B. Rahl, S.S. Levine, and et al. Mediator and cohesin connect gene expression and chromatin architecture Nature 467 2010 430 435
19. C.A. Klattenhoff, J.C. Scheuermann, L.E. Surface, R.K. Bradley, P.A. Fields, M.L. Steinhauser, H. Ding, V.L. Butty, L. Torrey, S. Haas, and et al. Braveheart, a long noncoding RNA required for cardiovascular lineage commitment Cell 152 2013 570 583
20. J.P. Kruse, and W. Gu Modes of p53 regulation Cell 137 2009 609 622
21. K.H. Lee, M. Li, A.M. Michalowski, X. Zhang, H. Liao, L. Chen, Y. Xu, X. Wu, and J. Huang A genomewide study identifies the Wnt signaling pathway as a major target of p53 in murine embryonic stem cells Proc. Natl. Acad. Sci. USA 107 2010 69 74
22. D.F. Lee, J. Su, Y.S. Ang, X. Carvajal-Vergara, S. Mulero-Navarro, C.F. Pereira, J. Gingold, H.L. Wang, R. Zhao, A. Sevilla, and et al. Regulation of embryonic and induced pluripotency by aurora kinase-p53 signaling Cell Stem Cell 11 2012 179 194
23. M. Li, Y. He, W. Dubois, X. Wu, J. Shi, and J. Huang Distinct regulatory mechanisms and functions for p53-activated and p53-repressed DNA damage response genes in embryonic stem cells Mol. Cell 46 2012 30 42
24. T. Lin, C. Chao, S. Saito, S.J. Mazur, M.E. Murphy, E. Appella, and Y. Xu p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression Nat. Cell Biol. 7 2005 165 171
25. J.C. Liu, X. Guan, J.A. Ryan, A.G. Rivera, C. Mock, V. Agrawal, A. Letai, P.H. Lerou, and G. Lahav High mitochondrial priming sensitizes hESCs to DNA-damage-induced apoptosis Cell Stem Cell 13 2013 483 491
26. R. Montes de Oca Luna, D.S. Wagner, and G. Lozano Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53 Nature 378 1995 203 206
27. L.B. Motta-Mena, F. Heyd, and K.W. Lynch Context-dependent regulatory mechanism of the splicing factor hnRNP L Mol. Cell 37 2010 223 234
28. A. Moumen, P. Masterson, M.J. O'Connor, and S.P. Jackson hnRNP K: an HDM2 target and transcriptional coactivator of p53 in response to DNA damage Cell 123 2005 1065 1078
29. J. Parant, A. Chavez-Reyes, N.A. Little, W. Yan, V. Reinke, A.G. Jochemsen, and G. Lozano Rescue of embryonic lethality in Mdm4-null mice by loss of Trp53 suggests a nonoverlapping pathway with MDM2 to regulate p53 Nat. Genet. 29 2001 92 95
30. A. Pauli, M.L. Norris, E. Valen, G.L. Chew, J.A. Gagnon, S. Zimmerman, A. Mitchell, J. Ma, J. Dubrulle, D. Reyon, and et al. Toddler: an embryonic signal that promotes cell movement via Apelin receptors Science 343 2014 1248636
31. P.B. Rahl, C.Y. Lin, A.C. Seila, R.A. Flynn, S. McCuine, C.B. Burge, P.A. Sharp, and R.A. Young c-Myc regulates transcriptional pause release Cell 141 2010 432 445
32. P.S. Ray, J. Jia, P. Yao, M. Majumder, M. Hatzoglou, and P.L. Fox A stress-responsive RNA switch regulates VEGFA expression Nature 457 2009 915 919
33. J.L. Rinn, M. Kertesz, J.K. Wang, S.L. Squazzo, X. Xu, S.A. Brugmann, L.H. Goodnough, J.A. Helms, P.J. Farnham, E. Segal, and H.Y. Chang Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs Cell 129 2007 1311 1323
34. M.C. Tsai, O. Manor, Y. Wan, N. Mosammaparast, J.K. Wang, F. Lan, Y. Shi, E. Segal, and H.Y. Chang Long noncoding RNA as modular scaffold of histone modification complexes Science 329 2010 689 693
35. R.A. Young Control of the embryonic stem cell state Cell 144 2011 940 954
36. X. Zhang, Y. He, K.H. Lee, W. Dubois, Z. Li, X. Wu, A. Kovalchuk, W. Zhang, and J. Huang Rap2b, a novel p53 target, regulates p53-mediated pro-survival function Cell Cycle 12 2013 1279 1291