CDK6 levels regulate quiescence exit in human hematopoietic stem cells

Cell Stem Cell

Volumn 16, Issue 3, 2015, Pages 302-313

  Laurenti, Elisa ^a   Frelin, Catherine ^a   Xie, Stephanie ^a   Ferrari, Robin ^a,c   Dunant, Cyrille F ^d   Zandi, Sasan ^a   Neumann, Andrea ^a   Plumb, Ian ^a   Doulatov, Sergei ^e   Chen, Jing ^f   April, Craig ^f   Fan, Jian Bing ^f   Iscove, Norman ^a,b   Dick, John E ^a,b  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d EPFL   (Switzerland)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f ILLUMINA INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; CYCLIN D3; CYCLIN DEPENDENT KINASE 6; GUANOSINE PHOSPHATE; MESSENGER RNA; RETINOBLASTOMA PROTEIN; CDK6 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE PHASE; CELL CYCLE REGULATION; CELL DIVISION; CELLULAR PARAMETERS; CONTROLLED STUDY; DNA CONTENT; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC SYSTEM; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; LATENT PERIOD; MITOGENICITY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUIESCENCE EXIT; REGULATORY MECHANISM; UPREGULATION; XENOTRANSPLANTATION; BIOLOGICAL MODEL; BIOSYNTHESIS; COMPUTER SIMULATION; CYTOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; PHYSIOLOGY;

CELL DIVISION; COMPUTER SIMULATION; CYCLIN-DEPENDENT KINASE 6; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; MODELS, BIOLOGICAL;

EID: 84924284076     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2015.01.017     Document Type: Article

References (41)

1. M.J. Aryee, J.A. Gutiérrez-Pabello, I. Kramnik, T. Maiti, and J. Quackenbush An improved empirical bayes approach to estimating differential gene expression in microarray time-course data: BETR (Bayesian Estimation of Temporal Regulation) BMC Bioinformatics 10 2009 409
2. 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
3. G.B. Bradford, B. Williams, R. Rossi, and I. Bertoncello Quiescence, cycling, and turnover in the primitive hematopoietic stem cell compartment Exp. Hematol. 25 1997 445 453
4. S.N. Catlin, L. Busque, R.E. Gale, P. Guttorp, and J.L. Abkowitz The replication rate of human hematopoietic stem cells in vivo Blood 117 2011 4460 4466
5. S.H. Cheshier, S.J. Morrison, X. Liao, and I.L. Weissman In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells Proc. Natl. Acad. Sci. USA 96 1999 3120 3125
6. M.R. Copley, P.A. Beer, and C.J. Eaves Hematopoietic stem cell heterogeneity takes center stage Cell Stem Cell 10 2012 690 697
7. A. Foudi, K. Hochedlinger, D. Van Buren, J.W. Schindler, R. Jaenisch, V. Carey, and H. Hock Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells Nat. Biotechnol. 27 2009 84 90
8. R. Gazit, B.S. Garrison, T.N. Rao, T. Shay, J. Costello, J. Ericson, F. Kim, J.J. Collins, A. Regev, A.J. Wagers, D.J. Rossi Immunological Genome Project Consortium Transcriptome analysis identifies regulators of hematopoietic stem and progenitor cells Stem Cell Reports 1 2013 266 280
9. I. Glauche, K. Moore, L. Thielecke, K. Horn, M. Loeffler, and I. Roeder Stem cell proliferation and quiescence - two sides of the same coin PLoS Comput. Biol. 5 2009 e1000447
10. M. Hoffmann, H.H. Chang, S. Huang, D.E. Ingber, M. Loeffler, and J. Galle Noise-driven stem cell and progenitor population dynamics PLoS ONE 3 2008 e2922
11. X. Huang, M. Di Liberto, D. Jayabalan, J. Liang, S. Ely, J. Bretz, A.L. Shaffer 3rd, T. Louie, I. Chen, and S. Randolph Prolonged early G(1) arrest by selective CDK4/CDK6 inhibition sensitizes myeloma cells to cytotoxic killing through cell cycle-coupled loss of IRF4 Blood 120 2012 1095 1106
12. V. Jankovic, A. Ciarrocchi, P. Boccuni, T. DeBlasio, R. Benezra, and S.D. Nimer Id1 restrains myeloid commitment, maintaining the self-renewal capacity of hematopoietic stem cells Proc. Natl. Acad. Sci. USA 104 2007 1260 1265
13. K. Kataoka, T. Sato, A. Yoshimi, S. Goyama, T. Tsuruta, H. Kobayashi, M. Shimabe, S. Arai, M. Nakagawa, and Y. Imai Evi1 is essential for hematopoietic stem cell self-renewal, and its expression marks hematopoietic cells with long-term multilineage repopulating activity J. Exp. Med. 208 2011 2403 2416
14. L.G. Lajtha On the concept of cell cycle J. Cell. Physiol. 62 1 1963 L1 143-145
15. E. Laurenti, B. Varnum-Finney, A. Wilson, I. Ferrero, W.E. Blanco-Bose, A. Ehninger, P.S. Knoepfler, P.-F. Cheng, H.R. MacDonald, and R.N. Eisenman Hematopoietic stem cell function and survival depend on c-Myc and N-Myc activity Cell Stem Cell 3 2008 611 624
16. E. Laurenti, S. Doulatov, S. Zandi, I. Plumb, J. Chen, C. April, J.-B. Fan, and J.E. Dick The transcriptional architecture of early human hematopoiesis identifies multilevel control of lymphoid commitment Nat. Immunol. 14 2013 756 763
17. E.R. Lechman, B. Gentner, P. van Galen, A. Giustacchini, M. Saini, F.E. Boccalatte, H. Hiramatsu, U. Restuccia, A. Bachi, and V. Voisin Attenuation of miR-126 activity expands HSC in vivo without exhaustion Cell Stem Cell 11 2012 799 811
18. H.S. Micklem, and D.A. Ogden Ageing of Haematopoietic Stem Cell Populations in the Mouse A.B. Cairnie, P.K. Lala, D.G. Osmond, Stem Cells of Renewing Cell Population 1976 Academic Press 331 341
19. M. Milyavsky, O.I. Gan, M. Trottier, M. Komosa, O. Tabach, F. Notta, E. Lechman, K.G. Hermans, K. Eppert, and Z. Konovalova A distinctive DNA damage response in human hematopoietic stem cells reveals an apoptosis-independent role for p53 in self-renewal Cell Stem Cell 7 2010 186 197
20. S.J. Morrison, and I.L. Weissman The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype Immunity 1 1994 661 673
21. F. Notta, S. Doulatov, E. Laurenti, A. Poeppl, I. Jurisica, and J.E. Dick Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment Science 333 2011 218 221
22. H. Oguro, L. Ding, and S.J. Morrison SLAM family markers resolve functionally distinct subpopulations of hematopoietic stem cells and multipotent progenitors Cell Stem Cell 13 2013 102 116
23. K.W. Orford, and D.T. Scadden Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation Nat. Rev. Genet. 9 2008 115 128
24. E. Passegué, A.J. Wagers, S. Giuriato, W.C. Anderson, and I.L. Weissman Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates J. Exp. Med. 202 2005 1599 1611
25. E.M. Pietras, M.R. Warr, and E. Passegué Cell cycle regulation in hematopoietic stem cells J. Cell Biol. 195 2011 709 720
26. M.E. Pietrzyk, G.V. Priestley, and N.S. Wolf Normal cycling patterns of hematopoietic stem cell subpopulations: an assay using long-term in vivo BrdU infusion Blood 66 1985 1460 1462
27. T. Placke, K. Faber, A. Nonami, S.L. Putwain, H.R. Salih, F.H. Heidel, A. Krämer, D.E. Root, D.A. Barbie, and A.V. Krivtsov Requirement for CDK6 in MLL-rearranged acute myeloid leukemia Blood 124 2014 13 23
28. J. Qiu, D. Papatsenko, X. Niu, C. Schaniel, and K. Moore Divisional History and Hematopoietic Stem Cell Function during Homeostasis Stem Cell Rep. 2 2014 473 490
29. S. Ren, and B.J. Rollins Cyclin C/cdk3 promotes Rb-dependent G0 exit Cell 117 2004 239 251
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, and C.-R. Tsai mTORC1 controls the adaptive transition of quiescent stem cells from G0 to G(Alert) Nature 510 2014 393 396
31. I. Roeder, and M. Loeffler A novel dynamic model of hematopoietic stem cell organization based on the concept of within-tissue plasticity Exp. Hematol. 30 2002 853 861
32. L. Rossi, K.K. Lin, N.C. Boles, L. Yang, K.Y. King, M. Jeong, A. Mayle, and M.A. Goodell Less is more: unveiling the functional core of hematopoietic stem cells through knockout mice Cell Stem Cell 11 2012 302 317
33. R. Scheicher, A. Hoelbl-Kovacic, F. Bellutti, A.-S. Tigan, M. Prchal-Murphy, G. Heller, C. Schneckenleithner, M. Salazar-Roa, S. Zöchbauer-Müller, and J. Zuber CDK6 as a key regulator of hematopoietic and leukemic stem cell activation Blood 125 2014 90 101
34. C.J. Sherr, and J.M. Roberts Living with or without cyclins and cyclin-dependent kinases Genes Dev. 18 2004 2699 2711
35. T. Suda, J. Suda, and M. Ogawa Proliferative kinetics and differentiation of murine blast cell colonies in culture: evidence for variable G0 periods and constant doubling rates of early pluripotent hemopoietic progenitors J. Cell. Physiol. 117 1983 308 318
36. H. Takizawa, R.R. Regoes, C.S. Boddupalli, S. Bonhoeffer, and M.G. Manz Dynamic variation in cycling of hematopoietic stem cells in steady state and inflammation J. Exp. Med. 208 2011 273 284
37. N. Uchida, B. Dykstra, K.J. Lyons, F.Y.K. Leung, and C.J. Eaves Different in vivo repopulating activities of purified hematopoietic stem cells before and after being stimulated to divide in vitro with the same kinetics Exp. Hematol. 31 2003 1338 1347
38. P. van Galen, A. Kreso, N. Mbong, D.G. Kent, T. Fitzmaurice, J.E. Chambers, S. Xie, E. Laurenti, K. Hermans, and K. Eppert The unfolded protein response governs integrity of the haematopoietic stem-cell pool during stress Nature 510 2014 268 272
39. H. Veiga-Fernandes, and B. Rocha High expression of active CDK6 in the cytoplasm of CD8 memory cells favors rapid division Nat. Immunol. 5 2004 31 37
40. A. Wilson, E. Laurenti, G. Oser, R.C. van der Wath, W. Blanco-Bose, M. Jaworski, S. Offner, C.F. Dunant, L. Eshkind, and E. Bockamp Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair Cell 135 2008 1118 1129
41. Y. Yuan, H. Shen, D.S. Franklin, D.T. Scadden, and T. Cheng In vivo self-renewing divisions of haematopoietic stem cells are increased in the absence of the early G1-phase inhibitor, p18INK4C Nat. Cell Biol. 6 2004 436 442