The Dlk1-Gtl2 Locus Preserves LT-HSC Function by Inhibiting the PI3K-mTOR Pathway to Restrict Mitochondrial Metabolism

Cell Stem Cell

Volumn 18, Issue 2, 2016, Pages 214-228

  Qian, Pengxu ^a   He, Xi C ^a   Paulson, Ariel ^a   Li, Zhenrui ^a,b   Tao, Fang ^a,b   Perry, John M ^a   Guo, Fengli ^a   Zhao, Meng ^a   Zhi, Lei ^c   Venkatraman, Aparna ^d   Haug, Jeffrey S ^a   Parmely, Tari ^a   Li, Hua ^a   Dobrowsky, Rick T ^e   Ding, Wen Xing ^b   Kono, Tomohiro ^f   Ferguson Smith, Anne C ^g   Li, Linheng ^a,b  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c TIANJIN MEDICAL UNIVERSITY   (China)

^d CHRISTIAN MEDICAL COLLEGE   (India)

^e UNIVERSITY OF KANSAS   (United States)

^f TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LONG UNTRANSLATED RNA; MAMMALIAN TARGET OF RAPAMYCIN; MICRORNA; PHOSPHATIDYLINOSITOL 3 KINASE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTOME; UNTRANSLATED RNA; ACETYLCYSTEINE; DLK1 PROTEIN, MOUSE; LEUKOCYTE ANTIGEN; MEG3 NON-CODING RNA, MOUSE; RAPAMYCIN; SIGNAL PEPTIDE; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ARTICLE; CELL LINEAGE; DLK1 GENE; FETUS LIVER; GENE; GENE CLUSTER; GENE LOCUS; GENOME IMPRINTING; GTL2 GENE; HEMATOPOIETIC STEM CELL; LONG TERM REPOPULATING HEMATOPOIETIC STEM CELL; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CYTOLOGY; EMBRYOLOGY; FETUS; GENETICS; HEK293 CELL LINE; HUMAN; LIVER; METABOLISM; MITOCHONDRION; MUTATION; ORGANELLE BIOGENESIS; SIGNAL TRANSDUCTION; ULTRASTRUCTURE;

ACETYLCYSTEINE; ANIMALS; ANTIGENS, CD; FETUS; GENETIC LOCI; GENOMIC IMPRINTING; HEK293 CELLS; HEMATOPOIETIC STEM CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER; MICE, INBRED C57BL; MICRORNAS; MITOCHONDRIA; MUTATION; ORGANELLE BIOGENESIS; PHOSPHATIDYLINOSITOL 3-KINASES; REACTIVE OXYGEN SPECIES; RNA, LONG NONCODING; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES;

EID: 84957839266     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2015.11.001     Document Type: Article

References (43)

1. J.R. Alvarez-Dominguez, W. Hu, B. Yuan, J. Shi, S.S. Park, A.A. Gromatzky, A. van Oudenaarden, and H.F. Lodish Global discovery of erythroid long noncoding RNAs reveals novel regulators of red cell maturation Blood 123 2014 570 581
2. D.P. Bartel MicroRNAs: target recognition and regulatory functions Cell 136 2009 215 233
3. M.S. Bartolomei Genomic imprinting: employing and avoiding epigenetic processes Genes Dev. 23 2009 2124 2133
4. I. Beerman, D. Bhattacharya, S. Zandi, M. Sigvardsson, I.L. Weissman, D. Bryder, and D.J. Rossi Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion Proc. Natl. Acad. Sci. USA 107 2010 5465 5470
5. P. Benveniste, C. Frelin, S. Janmohamed, M. Barbara, R. Herrington, D. Hyam, and N.N. Iscove Intermediate-term hematopoietic stem cells with extended but time-limited reconstitution potential Cell Stem Cell 6 2010 48 58
6. J.S. Berg, K.K. Lin, C. Sonnet, N.C. Boles, D.C. Weksberg, H. Nguyen, L.J. Holt, D. Rickwood, R.J. Daly, and M.A. Goodell Imprinted genes that regulate early mammalian growth are coexpressed in somatic stem cells PLoS ONE 6 2011 e26410
7. J. Cavaillé, M. Nicoloso, and J.P. Bachellerie Targeted ribose methylation of RNA in vivo directed by tailored antisense RNA guides Nature 383 1996 732 735
8. M. Charalambous, S.R. Ferron, S.T. da Rocha, A.J. Murray, T. Rowland, M. Ito, K. Schuster-Gossler, A. Hernandez, and A.C. Ferguson-Smith Imprinted gene dosage is critical for the transition to independent life Cell Metab. 15 2012 209 221
9. C. Chen, Y. Liu, R. Liu, T. Ikenoue, K.L. Guan, Y. Liu, and P. Zheng TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species J. Exp. Med. 205 2008 2397 2408
10. S.M. Cullen, A. Mayle, L. Rossi, and M.A. Goodell Hematopoietic stem cell development: an epigenetic journey Curr. Top. Dev. Biol. 107 2014 39 75
11. J.T. Cunningham, J.T. Rodgers, D.H. Arlow, F. Vazquez, V.K. Mootha, and P. Puigserver mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex Nature 450 2007 736 740
12. S.T. da Rocha, C.A. Edwards, M. Ito, T. Ogata, and A.C. Ferguson-Smith Genomic imprinting at the mammalian Dlk1-Dio3 domain Trends Genet. 24 2008 306 316
13. P.P. Das, D.A. Hendrix, E. Apostolou, A.H. Buchner, M.C. Canver, S. Beyaz, D. Ljuboja, R. Kuintzle, W. Kim, R. Karnik, and et al. PRC2 Is Required to Maintain Expression of the Maternal Gtl2-Rian-Mirg Locus by Preventing De Novo DNA Methylation in Mouse Embryonic Stem Cells Cell Rep. 12 2015 1456 1470
14. A.C. Ferguson-Smith Genomic imprinting: the emergence of an epigenetic paradigm Nat. Rev. Genet. 12 2011 565 575
15. A.R. Fernie, F. Carrari, and L.J. Sweetlove Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport Curr. Opin. Plant Biol. 7 2004 254 261
16. S.R. Ferrón, M. Charalambous, E. Radford, K. McEwen, H. Wildner, E. Hind, J.M. Morante-Redolat, J. Laborda, F. Guillemot, S.R. Bauer, and et al. Postnatal loss of Dlk1 imprinting in stem cells and niche astrocytes regulates neurogenesis Nature 475 2011 381 385
17. J.S. Haug, X.C. He, J.C. Grindley, J.P. Wunderlich, K. Gaudenz, J.T. Ross, A. Paulson, K.P. Wagner, Y. Xie, R. Zhu, and et al. N-cadherin expression level distinguishes reserved versus primed states of hematopoietic stem cells Cell Stem Cell 2 2008 367 379
18. A. Hirao, and T. Hoshii Mechanistic / mammalian target protein of rapamycin signaling in hematopoietic stem cells and leukemia Cancer Sci. 104 2013 977 982
19. Y.-Y. Jang, and S.J. Sharkis A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche Blood 110 2007 3056 3063
20. S. Labialle, V. Marty, M.L. Bortolin-Cavaillé, M. Hoareau-Osman, J.P. Pradère, P. Valet, P.G. Martin, and J. Cavaillé The miR-379/miR-410 cluster at the imprinted Dlk1-Dio3 domain controls neonatal metabolic adaptation EMBO J. 33 2014 2216 2230
21. M. Laplante, and D.M. Sabatini mTOR signaling in growth control and disease Cell 149 2012 274 293
22. J.Y. Lee, D. Nakada, O.H. Yilmaz, Z. Tothova, N.M. Joseph, M.S. Lim, D.G. Gilliland, and S.J. Morrison mTOR activation induces tumor suppressors that inhibit leukemogenesis and deplete hematopoietic stem cells after Pten deletion Cell Stem Cell 7 2010 593 605
23. L. Li, and H. Clevers Coexistence of quiescent and active adult stem cells in mammals Science 327 2010 542 545
24. S.P. Lin, N. Youngson, S. Takada, H. Seitz, W. Reik, M. Paulsen, J. Cavaille, and A.C. Ferguson-Smith Asymmetric regulation of imprinting on the maternal and paternal chromosomes at the Dlk1-Gtl2 imprinted cluster on mouse chromosome 12 Nat. Genet. 35 2003 97 102
25. S.P. Lin, P. Coan, S.T. da Rocha, H. Seitz, J. Cavaille, P.W. Teng, S. Takada, and A.C. Ferguson-Smith Differential regulation of imprinting in the murine embryo and placenta by the Dlk1-Dio3 imprinting control region Development 134 2007 417 426
26. M. Luo, M. Jeong, D. Sun, H.J. Park, B.A. Rodriguez, Z. Xia, L. Yang, X. Zhang, K. Sheng, G.J. Darlington, and et al. Long non-coding RNAs control hematopoietic stem cell function Cell Stem Cell 16 2015 426 438
27. M. Morita, S.P. Gravel, V. Chénard, K. Sikström, L. Zheng, T. Alain, V. Gandin, D. Avizonis, M. Arguello, C. Zakaria, and et al. mTORC1 controls mitochondrial activity and biogenesis through 4E-BP-dependent translational regulation Cell Metab. 18 2013 698 711
28. S.J. Morrison, H.D. Hemmati, A.M. Wandycz, and I.L. Weissman The purification and characterization of fetal liver hematopoietic stem cells Proc. Natl. Acad. Sci. USA 92 1995 10302 10306
29. T.D. Randall, F.E. Lund, M.C. Howard, and I.L. Weissman Expression of murine CD38 defines a population of long-term reconstituting hematopoietic stem cells Blood 87 1996 4057 4067
30. J.T. Rodgers, K.Y. King, J.O. Brett, M.J. Cromie, G.W. Charville, K.K. Maguire, C. Brunson, N. Mastey, L. Liu, C.R. Tsai, and et al. mTORC1 controls the adaptive transition of quiescent stem cells from G0 to G(Alert) Nature 510 2014 393 396
31. H. Seitz, H. Royo, M.L. Bortolin, S.P. Lin, A.C. Ferguson-Smith, and J. Cavaillé A large imprinted microRNA gene cluster at the mouse Dlk1-Gtl2 domain Genome Res. 14 2004 1741 1748
32. T. Simsek, F. Kocabas, J. Zheng, R.J. Deberardinis, A.I. Mahmoud, E.N. Olson, J.W. Schneider, C.C. Zhang, and H.A. Sadek The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche Cell Stem Cell 7 2010 380 390
33. C.M. Snyder, A.L. Rice, N.L. Estrella, A. Held, S.C. Kandarian, and F.J. Naya MEF2A regulates the Gtl2-Dio3 microRNA mega-cluster to modulate WNT signaling in skeletal muscle regeneration Development 140 2013 31 42
34. T. Suda, K. Takubo, and G.L. Semenza Metabolic regulation of hematopoietic stem cells in the hypoxic niche Cell Stem Cell 9 2011 298 310
35. N. Takahashi, A. Okamoto, R. Kobayashi, M. Shirai, Y. Obata, H. Ogawa, Y. Sotomaru, and T. Kono Deletion of Gtl2, imprinted non-coding RNA, with its differentially methylated region induces lethal parent-origin-dependent defects in mice Hum. Mol. Genet. 18 2009 1879 1888
36. K. Takubo, G. Nagamatsu, C.I. Kobayashi, A. Nakamura-Ishizu, H. Kobayashi, E. Ikeda, N. Goda, Y. Rahimi, R.S. Johnson, T. Soga, and et al. Regulation of glycolysis by Pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells Cell Stem Cell 12 2013 49 61
37. S. Tierling, S. Dalbert, S. Schoppenhorst, C.E. Tsai, S. Oliger, A.C. Ferguson-Smith, M. Paulsen, and J. Walter High-resolution map and imprinting analysis of the Gtl2-Dnchc1 domain on mouse chromosome 12 Genomics 87 2006 225 235
38. A. Venkatraman, X.C. He, J.L. Thorvaldsen, R. Sugimura, J.M. Perry, F. Tao, M. Zhao, M.K. Christenson, R. Sanchez, J.Y. Yu, and et al. Maternal imprinting at the H19-Igf2 locus maintains adult haematopoietic stem cell quiescence Nature 500 2013 345 349
39. A. Wilson, E. Laurenti, G. Oser, R.C. van der Wath, W. Blanco-Bose, M. Jaworski, S. Offner, C.F. Dunant, L. Eshkind, E. Bockamp, and et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair Cell 135 2008 1118 1129
40. L. Yang, D. Bryder, J. Adolfsson, J. Nygren, R. Månsson, M. Sigvardsson, and S.E. Jacobsen Identification of Lin(-)Sca1(+)kit(+)CD34(+)Flt3- short-term hematopoietic stem cells capable of rapidly reconstituting and rescuing myeloablated transplant recipients Blood 105 2005 2717 2723
41. S.J. Zacharek, C.M. Fillmore, A.N. Lau, D.W. Gludish, A. Chou, J.W. Ho, R. Zamponi, R. Gazit, C. Bock, N. Jäger, and et al. Lung stem cell self-renewal relies on BMI1-dependent control of expression at imprinted loci Cell Stem Cell 9 2011 272 281
42. J. Zhang, J.C. Grindley, T. Yin, S. Jayasinghe, X.C. He, J.T. Ross, J.S. Haug, D. Rupp, K.S. Porter-Westpfahl, L.M. Wiedemann, and et al. PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention Nature 441 2006 518 522
43. Y. Zhou, P. Cheunsuchon, Y. Nakayama, M.W. Lawlor, Y. Zhong, K.A. Rice, L. Zhang, X. Zhang, F.E. Gordon, H.G. Lidov, and et al. Activation of paternally expressed genes and perinatal death caused by deletion of the Gtl2 gene Development 137 2010 2643 2652