Post transcriptional control of the epigenetic stem cell regulator PLZF by sirtuin and HDAC deacetylases

Epigenetics and Chromatin

Volumn 8, Issue 1, 2015, Pages

  McConnell, Melanie J ^a,f   Durand, Laetitia ^b   Langley, Emma ^c,g   Coste Sarguet, Lise ^b   Zelent, Arthur ^e   Chomienne, Christine ^b   Kouzarides, Tony ^c   Licht, Jonathan D ^d,f   Guidez, Fabien ^b  

^a MALAGHAN INSTITUTE OF MEDICAL RESEARCH   (New Zealand)

^b Hôpital Saint Louis   (France)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d NORTHWESTERN UNIVERSITY   (United States)

^e UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^f MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^g BIOGEN   (United States)

Author keywords

Deacetylation; DNA methylation; Epigenetic; Repression

Indexed keywords

HISTONE ACETYLTRANSFERASE PCAF; HISTONE DEACETYLASE 3; LYSINE; PROMYELOCYTIC LEUKEMIA ZINC FINGER PROTEIN; SIRTUIN 1; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ARTICLE; CARCINOGENESIS; CELL FUNCTION; CHROMATIN; CONTROLLED STUDY; DEACETYLATION; DNA BINDING; DNA METHYLATION; ENZYME ACTIVATION; EPIGENETICS; EUCHROMATIN; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE TARGETING; HETEROCHROMATIN; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; STEM CELL; TRANSCRIPTION REGULATION; TRANSCRIPTIONAL REPRESSION;

EID: 84960240996     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/s13072-015-0030-8     Document Type: Article

References (56)

1. Collins T, Stone JR, Williams AJ. All in the family: the BTB/POZ, KRAB, and SCAN domains. Mol Cell Biol. 2001;21:3609.
2. Kelly KF, Daniel JM. POZ for effect - POZ-ZF transcription factors in cancer and development. Trends Cell Biol. 2006;16:578.
3. Chen Z, Brand NJ, Chen A, Chen SJ, Tong JH, Wang ZY, Waxman S, Zelent A. Fusion between a novel Krüppel-like zinc finger gene and the retinoic acid receptor-alpha locus due to a variant t(11; 17) translocation associated with acute promyelocytic leukaemia. EMBO J. 1993;12:1161.
4. Reid A, Gould A, Brand N, Cook M, Strutt P, Li J, Licht J, Waxman S, Krumlauf R, Zelent A. Leukemia translocation gene, PLZF, is expressed with a speckled nuclear pattern in early hematopoietic progenitors. Blood. 1995;86:4544.
5. Doulatov S, Notta F, Rice KL, Howell L, Zelent A, Licht JD, Dick JE. PLZF is a regulator of homeostatic and cytokine-induced myeloid development. Genes Dev. 2009;23:2076.
6. Puszyk W, Down T, Grimwade D, Chomienne C, Oakey RJ, Solomon E, Guidez F. The epigenetic regulator PLZF represses L1 retrotransposition in germ and progenitor cells. EMBO J. 2013;32:1941.
7. Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, Sukhwani M, Orwig KE, Wolgemuth DJ, Pandolfi PP. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet. 2004;36:653.
8. Buaas FW, Kirsh AL, Sharma M, McLean DJ, Morris JL, Griswold MD, de Rooij DG, Braun RE. Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet. 2004;36:647.
9. Constantinides MG, McDonald BD, Verhoef PA, Bendelac A. A committed precursor to innate lymphoid cells. Nature. 2014;508:397.
10. Constantinides MG, Gudjonson H, McDonald BD, Ishizuka IE, Verhoef PA, Dinner AR, Bendelac A. PLZF expression maps the early stages of ILC1 lineage development. Proc Natl Acad Sci USA. 2015;112:5123.
11. Suliman BA, Xu D, Williams BR. The promyelocytic leukemia zinc finger protein: two decades of molecular oncology. Front Oncol. 2012;2:74.
12. McConnell MJ, Licht JD. The PLZF gene of t(11; 17)-associated APL. Curr Top Microbiol Immunol. 2007;313:31.
13. Guidez F, Ivins S, Zhu J, Söderström M, Waxman S, Zelent A. Reduced retinoic acid-sensitivities of nuclear receptor corepressor binding to PML- and PLZF-RARalpha underlie molecular pathogenesis and treatment of acute promyelocytic leukemia. Blood. 1998;9:2634.
14. Melnick A, Fruchtman S, Zelent A, Liu M, Huang Q, Boczkowska B, Calasanz M, Fernandez A, Licht JD, Najfeld V. Identification of novel chromosomal rearrangements in acute myelogenous leukemia involving loci on chromosome 2p23, 15q22 and 17q21. Leukemia. 1999;13:1534.
15. Guidez F, Parks S, Wong H, Jovanovic JV, Mays A, Gilkes AF, Mills KI, Guillemin MC, Hobbs RM, Pandolfi PP, de Thé H, Solomon E, Grimwade D. RARalpha-PLZF overcomes PLZF-mediated repression of CRABPI, contributing to retinoid resistance in t(11; 17) acute promyelocytic leukemia. Proc Natl Acad Sci USA. 2007;104:18694.
16. Felicetti F, Errico MC, Bottero L, Segnalini P, Stoppacciaro A, Biffoni M, Felli N, Mattia G, Petrini M, Colombo MP, Peschle C, Carè A. The promyelocytic leukemia zinc finger-microRNA-221/-222 pathway controls melanoma progression through multiple oncogenic mechanisms. Cancer Res. 2008;68:2745.
17. Brooks CL, Gu W. The impact of acetylation and deacetylation on the p53 pathway. Protein Cell. 2011;2:456.
18. Bereshchenko OR, Gu W, Dalla-Favera R. Acetylation inactivates the transcriptional repressor BCL6. Nat Genet. 2002;32:606.
19. Guidez F, Howell L, Isalan M, Cebrat M, Alani RM, Ivins S, Hormaeche I, McConnell MJ, Pierce S, Cole PA, Licht J, Zelent A. Histone acetyltransferase activity of p300 is required for transcriptional repression by the promyelocytic leukemia zinc finger protein. Mol Cell Biol. 2005;25:5552.
20. Glozak MA, Sengupta N, Zhang X, Seto E. Acetylation and deacetylation of non-histone proteins. Gene. 2006;363:15.
21. Haberland M, Montgomery RL, Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet. 2009;10:32.
22. Melnick AM, Adelson K, Licht JD. The theoretical basis of transcriptional therapy of cancer: can it be put into practice? J Clin Oncol. 2005;23:3957.
23. Glozak MA, Seto E. Histone deacetylases and cancer. Oncogene. 2007;26:5420.
24. Roth M, Chen WY. Sorting out functions of sirtuins in cancer. Oncogene. 2014;33:1609.
25. Spange S, Wagner T, Heinzel T, Krämer OH. Acetylation of non-histone proteins modulates cellular signalling at multiple levels. Int J Biochem Cell Biol. 2009;41:185.
26. Brachmann CB, Sherman JM, Devine SE, Cameron EE, Pillus L, Boeke JD. The SIR2 gene family, conserved from bacteria to humans, functions in silencing, cell cycle progression, and chromosome stability. Genes Dev. 1995;9:2888.
27. Frye RA. Characterization of five human cDNAs with homology to the yeast SIR2 gene: sir2-like proteins (sirtuins) metabolize NAD and may have protein ADP-ribosyltransferase activity. Biochem Biophys Res Commun. 1999;260:273.
28. Houtkooper RH, Auwerx J. Exploring the therapeutic space around NAD+. J Cell Biol. 2012;199:205.
29. Saunders LR, Verdin E. Sirtuins: critical regulators at the crossroads between cancer and aging. Oncogene. 2007;26:5489.
30. Guarente L. Sir2 links chromatin silencing, metabolism, and aging. Genes Dev. 2000;14:1021.
31. Houtkooper RH, Pirinen E, Auwerx J. Sirtuins as regulators of metabolism and healthspan. Nat Rev Mol Cell Biol. 2012;13:225.
32. Bradbury CA, Khanim FL, Hayden R, Bunce CM, White DA, Drayson MT, Craddock C, Turner BM. Histone deacetylases in acute myeloid leukaemia show a distinctive pattern of expression that changes selectively in response to deacetylase inhibitors. Leukemia. 2005;19:1751.
33. Chen W, Bhatia R. Roles of SIRT1 in leukemogenesis. Curr Opin Hematol. 2013;20:308.
34. Yuan H, Wang Z, Li L, Zhang H, Modi H, Horne D, Bhatia R, Chen W. Activation of stress response gene SIRT1 by BCR-ABL promotes leukemogenesis. Blood. 2012;119:1904.
35. Li L, Wang L, Wang Z, Ho Y, McDonald T, Holyoake TL, Chen W, Bhatia R. Activation of p53 by SIRT1 inhibition enhances elimination of CML leukemia stem cells in combination with imatinib. Cancer Cell. 2012;21:266.
36. Chauchereau A, Mathieu M, de Saintignon J, Ferreira R, Pritchard LL, Mishal Z, Dejean A, Harel-Bellan A. HDAC4 mediates transcriptional repression by the acute promyelocytic leukaemia-associated protein PLZF. Oncogene. 2004;23:8777.
37. Petrie K, Guidez F, Howell L, Healy L, Waxman S, Greaves M, Zelent A. The histone deacetylase 9 gene encodes multiple protein isoforms. J Biol Chem. 2003;278:16059.
38. Lin RJ, Nagy L, Inoue S, Shao W, Miller WH, Evans RM. Role of the histone deacetylase complex in acute promyelocytic leukaemia. Nature. 1998;391:811.
39. Melnick A, Carlile G, Ahmad KF, Kiang CL, Corcoran C, Bardwell V, Prive GG, Licht JD. Critical residues within the BTB domain of PLZF and Bcl-6 modulate interaction with corepressors. Mol Cell Biol. 2002;22:1804.
40. Sadler AJ, Rossello FJ, Yu L, Deane JA, Yuan X, Wang D, Irving AT, Kaparakis-Liaskos M, Gantier MP, Ying H, Yim HC, Hartland EL, Notini AJ, de Boer S, White SJ, Mansell A, Liu JP, Watkins DN, Gerondakis S, Williams BR, Xu D. BTB-ZF transcriptional regulator PLZF modifies chromatin to restrain inflammatory signalling programs. Proc Natl Acad Sci USA. 2015;112:1535.
41. Sadler AJ, Suliman BA, Yu L, Yuan X, Wang D, Irving AT, Sarvestani ST, Banerjee A, Mansell AS, Liu JP, Gerondakis S, Williams BR, Xu D. The acetyltransferase HAT1 moderates the NK-kB response by regulating the transcription factor PLZF. Nat Commun. 2015;6:6795.
42. Langley E, Pearson M, Faretta M, Bauer UM, Frye RA, Minucci S, Pelicci PG, Kouzarides T. Human SIR2 deacetylates p53 and antagonizes PML/p53-induced cellular senescence. EMBO J. 2002;21:2383.
43. Li JY, English MA, Ball HJ, Yeyati PL, Waxman S, Licht JD. Sequence-specific DNA binding and transcriptional regulation by the promyelocytic leukemia zinc finger protein. J Biol Chem. 1997;272:22447.
44. Bitterman KJ, Anderson RM, Cohen HY, Latorre-Esteves M, Sinclair DA. Inhibition of silencing and accelerated aging by nicotinamide, a putative negative regulator of yeast sir2 and human SIRT1. J Biol Chem. 2002;277:45099.
45. Kouzarides T. Acetylation: a regulatory modification to rival phosphorylation? EMBO J. 2000;19:1176.
46. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science. 2009;325:834.
47. Zhao S, Xu W, Jiang W, Yu W, Lin Y, Zhang T, Yao J, Zhou L, Zeng Y, Li H, Li Y, Shi J, An W, Hancock SM, He F, Qin L, Chin J, Yang P, Chen X, Lei Q, Xiong Y, Guan KL. Regulation of cellular metabolism by protein lysine acetylation. Science. 2010;327:1000.
48. McConnell MJ, Chevallier N, Berkofsky-Fessler W, Giltnane JM, Malani RB, Staudt LM, Licht JD. Growth suppression by acute promyelocytic leukemia-associated protein PLZF is mediated by repression of c-myc expression. Mol Cell Biol. 2003;23:9375.
49. Elizalde C, Fernández-Rueda J, Salcedo JM, Dorronsoro A, Ferrin I, Jakobsson E, Trigueros C. Histone deacetylase 3 modulates the expansion of human hematopoietic stem cells. Stem Cells Dev. 2012;21:2581.
50. Leko V, Varnum-Finney B, Li H, Gu Y, Flowers D, Nourigat C, Bernstein ID, Bedalov A. SIRT1 is dispensable for function of hematopoietic stem cells in adult mice. Blood. 2012;119:1856.
51. Dadoune JP. New insights into male gametogenesis: what about the spermatogonial stem cell niche? Folia Histochem Cytobiol. 2007;45:141.
52. Bell EL, Nagamori I, Williams EO, Del Rosario AM, Bryson BD, Watson N, White FM, Sassone-Corsi P, Guarente L. SirT1 is required in the male germ cell for differentiation and fecundity in mice. Development. 2014;141:3495.
53. Yao YL, Yang WM. Beyond histone and deacetylase: an overview of cytoplasmic histone deacetylases and their nonhistone substrates. J Biomed Biotechnol. 2011;2011:146493.
54. Gabay M, Li Y, Felsher DW. MYC activation is a hallmark of cancer initiation and maintenance. Cold Spring Harb Perspect Med. 2014;4:a014241.
55. Carreira PE, Richardson SR, Faulkner GJ. L1 retrotransposons, cancer stem cells and oncogenesis. FEBS J. 2014;281:63.
56. Matsuzawa K, Izawa S, Ohkura T, Ohkura H, Ishiguro K, Yoshida A, Takiyama Y, Haneda M, Shigemasa C, Yamamoto K, Taniguchi S. Implication of intracellular localization of transcriptional repressor PLZF in thyroid neoplasms. BMC Endocr Disord. 2014;14:52.