Posttranslational regulation of self-renewal capacity: Insights from proteome and phosphoproteome analyses of stem cell leukemia

Blood

Volumn 120, Issue 8, 2012, Pages

  Trost, Matthias ^a,b   Sauvageau, Martin ^a   Hèrault, Olivier ^a   Deleris, Paul ^a   Pomiès, Christelle ^a   Chagraoui, Jalila ^a   Mayotte, Nadine ^a   Meloche, Sylvain ^a,c   Sauvageau, Guy ^a,c,d   Thibault, Pierre ^a,c  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASM PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; NUCLEAR PROTEIN; PHOSPHOPROTEIN; POLYCOMB GROUP PROTEIN; TRANSCRIPTION FACTOR EZH2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FATE; CELL RENEWAL; CONTROLLED STUDY; LEUKEMIA STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEOMICS; STEM CELL;

EID: 84865444387     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-12-397844     Document Type: Article

References (65)

1. Lapidot T, Sirard C, Vormoor J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367(6464):645-648. (Pubitemid 24067706)
2. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3(7):730-737. (Pubitemid 27298715)
3. Taussig DC, Vargaftig J, Miraki-Moud F, et al. Leukemia-initiating cells from some acute myeloid leukemia patients with mutated nucleophosmin reside in the CD34(-) fraction. Blood. 2010;115(10):1976-1984.
4. McDermott SP, Eppert K, Lechman ER, Doedens M, Dick JE. Comparison of human cord blood engraftment between immunocompromised mouse strains. Blood. 2010;116(2):193-200.
5. Huntly BJ, Shigematsu H, Deguchi K, et al. MOZTIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell. 2004;6(6):587-596. (Pubitemid 40017702)
6. Somervaille TC, Cleary ML. Identification and characterization of leukemia stem cells in murine MLL-AF9 acute myeloid leukemia. Cancer Cell. 2006;10(4):257-268. (Pubitemid 44512188)
7. Thorsteinsdottir U, Krosl J, Kroon E, Haman A, Hoang T, Sauvageau G. The oncoprotein E2APbx1a collaborates with Hoxa9 to acutely transform primary bone marrow cells. Mol Cell Biol. 1999;19(9):6355-6366. (Pubitemid 29399340)
8. Wilhelm BT, Briau M, Austin P, et al. RNA-seq analysis of 2 closely related leukemia clones that differ in their self-renewal capacity. Blood. 2011;117(2):e27-e38.
9. Kroon E, Krosl J, Thorsteinsdottir U, Baban S, Buchberg AM, Sauvageau G. Hoxa9 transforms primary bone marrow cells through specific collaboration with Meis1a but not Pbx1b. EMBO J. 1998;17(13):3714-3725. (Pubitemid 28327389)
10. Milne TA, Martin ME, Brock HW, Slany RK, Hess JL. Leukemogenic MLL fusion proteins bind across a broad region of the Hox a9 locus, promoting transcription and multiple histone modifications. Cancer Res. 2005;65(24):11367-11374. (Pubitemid 41821694)
11. Wong P, Iwasaki M, Somervaille TC, So CW, Cleary ML. Meis1 is an essential and rate-limiting regulator of MLL leukemia stem cell potential. Genes Dev. 2007;21(21):2762-2774. (Pubitemid 350070722)
12. Trost M, English L, Lemieux S, Courcelles M, Desjardins M, Thibault P. The phagosomal proteome in interferon-gamma-activated macrophages. Immunity. 2009;30(1):143-154.
13. Thingholm TE, Jorgensen TJ, Jensen ON, Larsen MR. Highly selective enrichment of phosphorylated peptides using titanium dioxide. Nature Protoc. 2006;1(4):1929-1935. (Pubitemid 46773313)
14. Courcelles M, Lemieux S, Voisin L, Meloche S, Thibault P. ProteoConnections: a bioinformatics platform to facilitate proteome and phosphoproteome analyses. Proteomics. 2011;11(13):2654-2671.
15. Reya T, Duncan AW, Ailles L, et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature. 2003;423(6938):409-414. (Pubitemid 36626987)
16. Petropoulos K, Arseni N, Schessl C, et al. A novel role for Lef-1, a central transcription mediator of Wnt signaling, in leukemogenesis. J Exp Med. 2008;205(3):515-522. (Pubitemid 351439299)
17. Doyon Y, Cayrou C, Ullah M, et al. ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol Cell. 2006;21(1):51-64. (Pubitemid 43017848)
18. Shiseki M, Nagashima M, Pedeux RM, et al. p29ING4 and p28ING5 bind to p53 and p300, and enhance p53 activity. Cancer Res. 2003;63(10):2373-2378. (Pubitemid 36605171)
19. Li X, Nishida T, Noguchi A, et al. Decreased nuclear expression and increased cytoplasmic expression of ING5 may be linked to tumorigenesis and progression in human head and neck squamous cell carcinoma. J Cancer Res Clin Oncol. 2010;136(10):1573-1583.
20. Ohta H, Sekulovic S, Bakovic S, et al. Near-maximal expansions of hematopoietic stem cells in culture using NUP98-HOX fusions. Exp Hematol. 2007;35(5):817-830. (Pubitemid 46601757)
21. Osawa M, Hanada K, Hamada H, Nakauchi H. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science. 1996;273(5272):242-245. (Pubitemid 26285891)
22. Trowbridge JJ, Snow JW, Kim J, Orkin SH. DNA methyltransferase 1 is essential for and uniquely regulates hematopoietic stem and progenitor cells. Cell Stem Cell. 2009;5(4):442-449.
23. Weinreich MA, Lintmaer I, Wang L, Liggitt HD, Harkey MA, Blau CA. Growth factor receptors as regulators of hematopoiesis. Blood. 2006;108(12):3713-3721. (Pubitemid 44864549)
24. An JH, Kim JW, Jang SM, Kim CH, Kang EJ, Choi KH. Gelsolin negatively regulates the activity of tumor suppressor p53 through their physical interaction in hepatocarcinoma HepG2 cells. Biochem Biophys Res Commun. 2011;412(1):44-49.
25. Lukanidin E, Sleeman JP. Building the niche: the role of the S100 proteins in metastatic growth. Semin Cancer Biol. 2012;22(3):216-225.
26. Olsen JV, Blagoev B, Gnad F, et al. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell. 2006;127(3):635-648. (Pubitemid 44647421)
27. Ahn EY, Yan M, Malakhova OA, et al. Disruption of the NHR4 domain structure in AML1-ETO abrogates SON binding and promotes leukemogenesis. Proc Natl Acad Sci U S A. 2008;105(44):17103-17108.
28. Resar LM. The high mobility group A1 gene: transforming inflammatory signals into cancer? Cancer Res. 2010;70(2):436-439.
29. Deneault E, Cellot S, Faubert A, et al. A functional screen to identify novel effectors of hematopoietic stem cell activity. Cell. 2009;137(2):369-379.
30. Nishino J, Kim I, Chada K, Morrison SJ. Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf expression. Cell. 2008;135(2):227-239.
31. Kamminga LM, Bystrykh LV, de Boer A, et al. The Polycomb group gene Ezh2 prevents hematopoietic stem cell exhaustion. Blood. 2006;107(5):2170-2179. (Pubitemid 43289403)
32. Katsumoto T, Aikawa Y, Iwama A, et al. MOZ is essential for maintenance of hematopoietic stem cells. Genes Dev. 2006;20(10):1321-1330. (Pubitemid 43727592)
33. Tadokoro Y, Ema H, Okano M, Li E, Nakauchi H. De novo DNA methyltransferase is essential for self-renewal, but not for differentiation, in hematopoietic stem cells. J Exp Med. 2007;204(4):715-722. (Pubitemid 46631602)
34. Chi P, Allis CD, Wang GG. Covalent histone modifications: miswritten, misinterpreted and miserased in human cancers. Nat Rev Cancer. 2010;10(7):457-469.
35. Lessard JA, Crabtree GR. Chromatin regulatory mechanisms in pluripotency. Annu Rev Cell Dev Biol. 2010;26:503-532.
36. Dey A, Nishiyama A, Karpova T, McNally J, Ozato K. Brd4 marks select genes on mitotic chromatin and directs postmitotic transcription. Mol Biol Cell. 2009;20(23):4899-4909.
37. Probst AV, Dunleavy E, Almouzni G. Epigenetic inheritance during the cell cycle. Nat Rev Mol Cell Biol. 2009;10(3):192-206.
38. Gough SM, Slape CI, Aplan PD. NUP98 gene fusions and hematopoietic malignancies: common themes and new biologic insights. Blood. 2011;118(24):6247-6257.
39. Ito K, Hirao A, Arai F, et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med. 2006;12(4):446-451.
40. Palacios D, Mozzetta C, Consalvi S, et al. TNF/p38alpha/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration. Cell Stem Cell. 2010;7(4):455-469.
41. Wang Y, Kellner J, Liu L, Zhou D. Inhibition of p38 mitogen-activated protein kinase promotes ex vivo hematopoietic stem cell expansion. Stem Cells Dev. 2011;20(7):1143-1152.
42. Peng JC, Valouev A, Swigut T, et al. Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell. 2009;139(7):1290-1302.
43. Shen X, Kim W, Fujiwara Y, et al. Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell. 2009;139(7):1303-1314.
44. Sauvageau M, Sauvageau G. Polycomb group proteins: multi-faceted regulators of somatic stem cells and cancer. Cell Stem Cell. 2010;7(3):299-313.
45. Kaneko S, Li G, Son J, et al. Phosphorylation of the PRC2 component Ezh2 is cell cycle-regulated and up-regulates its binding to ncRNA. Genes Dev. 2010;24(23):2615-2620.
46. Wei Y, Chen YH, Li LY, et al. CDK1-dependent phosphorylation of EZH2 suppresses methylation of H3K27 and promotes osteogenic differentiation of human mesenchymal stem cells. Nat Cell Biol. 2011;13(1):87-94.
47. Kuzmichev A, Jenuwein T, Tempst P, Reinberg D. Different EZH2-containing complexes target methylation of histone H1 or nucleosomal histone H3. Mol Cell. 2004;14(2):183-193. (Pubitemid 38515646)
48. Kuzmichev A, Margueron R, Vaquero A, et al. Composition and histone substrates of polycomb repressive group complexes change during cellular differentiation. Proc Natl Acad Sci U S A. 2005;102(6):1859-1864. (Pubitemid 40261977)
49. Brill LM, Xiong W, Lee KB, et al. Phosphoproteomic analysis of human embryonic stem cells. Cell Stem Cell. 2009;5(2):204-213.
50. Van Hoof D, Munoz J, Braam SR, et al. Phosphorylation dynamics during early differentiation of human embryonic stem cells. Cell Stem Cell. 2009;5(2):214-226.
51. Graumann J, Hubner NC, Kim JB, et al. Stable isotope labeling by amino acids in cell culture (SILAC) and proteome quantitation of mouse embryonic stem cells to a depth of 5111 proteins. Mol Cell Proteomics. 2008;7(4):672-683. (Pubitemid 351597479)
52. Voncken JW, Niessen H, Neufeld B, et al. MAPKAP kinase 3pK phosphorylates and regulates chromatin association of the polycomb group protein Bmi1. J Biol Chem. 2005;280(7):5178-5187. (Pubitemid 40279988)
53. Cha TL, Zhou BP, Xia W, et al. Akt-mediated phosphorylation of EZH2 suppresses methylation of lysine 27 in histone H3. Science. 2005;310(5746):306- 310. (Pubitemid 41457195)
54. Su IH, Dobenecker MW, Dickinson E, et al. Polycomb group protein ezh2 controls actin polymerization and cell signaling. Cell. 2005;121(3):425-436. (Pubitemid 40692302)
55. Philipp S, Puchert M, Adam-Klages S, et al. The Polycomb group protein EED couples TNF receptor 1 to neutral sphingomyelinase. Proc Natl Acad Sci U S A. 2010;107(3):1112-1117.
56. Rietzler M, Bittner M, Kolanus W, Schuster A, Holzmann B. The human WD repeat protein WAIT-1 specifically interacts with the cytoplasmic tails of beta7-integrins. J Biol Chem. 1998;273(42):27459-27466. (Pubitemid 28500464)
57. Witte V, Laffert B, Rosorius O, et al. HIV-1 Nef mimics an integrin receptor signal that recruits the polycomb group protein Eed to the plasma membrane. Mol Cell. 2004;13(2):179-190. (Pubitemid 38183265)
58. Pritsker M, Doniger TT, Kramer LC, Westcot SE, Lemischka IR. Diversification of stem cell molecular repertoire by alternative splicing. Proc Natl Acad Sci U S A. 2005;102(40):14290-14295. (Pubitemid 41429691)
59. Lupu F, Alves A, Anderson K, Doye V, Lacy E. Nuclear pore composition regulates neural stem/progenitor cell differentiation in the mouse embryo. Dev Cell. 2008;14(6):831-842. (Pubitemid 351757198)
60. Luco RF, Allo M, Schor IE, Kornblihtt AR, Misteli T. Epigenetics in alternative pre-mRNA splicing. Cell. 2011;144(1):16-26.
61. Dimaano C, Ullman KS. Nucleocytoplasmic transport: integrating mRNA production and turn-over with export through the nuclear pore. Mol Cell Biol. 2004;24(8):3069-3076. (Pubitemid 38452053)
62. Brown CR, Kennedy CJ, Delmar VA, Forbes DJ, Silver PA. Global histone acetylation induces functional genomic reorganization at mammalian nuclear pore complexes. Genes Dev. 2008;22(5):627-639. (Pubitemid 351342435)
63. Capelson M, Liang Y, Schulte R, Mair W, Wagner U, Hetzer MW. Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell. 2010;140(3):372-383.
64. Gruenbaum Y, Margalit A, Goldman RD, Shumaker DK, Wilson KL. The nuclear lamina comes of age. Nat Rev Mol Cell Biol. 2005;6(1):21-31. (Pubitemid 40064896)
65. Schneider R, Grosschedl R. Dynamics and interplay of nuclear architecture, genome organization, and gene expression. Genes Dev. 2007;21(23):3027-3043. (Pubitemid 350223521)