A targeted knockdown screen of genes coding for phosphoinositide modulators identifies PIP4K2A as required for acute myeloid leukemia cell proliferation and survival

Oncogene

Volumn 34, Issue 10, 2015, Pages 1253-1262

  Jude, J G ^a   Spencer, G J ^a   Huang, X ^a   Somerville, T D D ^a   Jones, D R ^a   Divecha, N ^a,b   Somervaille, T C P ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 5-PHOSPHATE; PHOSPHOTRANSFERASE; PIP4K2A PROTEIN, HUMAN; POLYPHOSPHOINOSITIDE; TARGET OF RAPAMYCIN KINASE;

ACUTE MYELOBLASTIC LEUKEMIA; ANIMAL; APOPTOSIS; CANCER STEM CELL; CELL PROLIFERATION; CELL SURVIVAL; CLUSTER ANALYSIS; DRUG SCREENING; ENZYME ACTIVATION; GENE EXPRESSION PROFILING; GENE SILENCING; GENETICS; HUMAN; INTRACELLULAR SPACE; METABOLISM; MOUSE; PATHOLOGY; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CLUSTER ANALYSIS; ENZYME ACTIVATION; GENE EXPRESSION PROFILING; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTRACELLULAR SPACE; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, TRANSGENIC; NEOPLASTIC STEM CELLS; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHATIDYLINOSITOLS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); TOR SERINE-THREONINE KINASES; TUMOR STEM CELL ASSAY;

EID: 84896691622     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.77     Document Type: Article

References (52)

1. Bunney TD, Katan M. Phosphoinositide signalling in cancer: beyond PI3K and PTEN. Nat Rev Cancer 2010; 10: 342-352.
2. Di Paolo G, De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature 2006; 443: 651-657.
3. Lemmon MA. Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 2008; 9: 99-111.
4. Martelli AM, Nyakern M, Tabellini G, Bortul R, Tazzari PL, Evangelisti C et al. Phosphoinositide 3-kinase/Akt signaling pathway and its therapeutical implications for human acute myeloid leukemia. Leukemia 2006; 20: 911-928.
5. Polak R, Buitenhuis M. The PI3K/PKB signaling module as key regulator of hematopoiesis: implications for therapeutic strategies in leukemia. Blood 2012; 119: 911-923.
6. Vergez F, Recher C, Payrastre B. Class I phosphoinositide 3-kinases in normal and pathologic hematopoietic cells. Curr Top Microbiol Immunol 2012; 362: 163-184.
7. Yilmaz OH, Valdez R, Theisen BK, Guo W, Ferguson DO, Wu H et al. Pten dependence distinguishes haematopoietic stem cells from leukaemiainitiating cells. Nature 2006; 441: 475-482.
8. Zhang J, Grindley JC, Yin T, Jayasinghe S, He XC, Ross JT et al. PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 2006; 441: 518-522.
9. Helgason CD, Damen JE, Rosten P, Grewal R, Sorensen P, Chappel SM et al. Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev 1998; 12: 1610-1620.
10. Xu Q, Simpson SE, Scialla TJ, Bagg A, Carroll M. Survival of acute myeloid leukemia cells requires PI3 kinase activation. Blood 2003; 102: 972-980.
11. Min YH, Eom JI, Cheong JW, Maeng HO, Kim JY, Jeung HK et al. Constitutive phosphorylation of Akt/PKB protein in acute myeloid leukemia: its significance as a prognostic variable. Leukemia 2003; 17: 995-997.
12. Kubota Y, Ohnishi H, Kitanaka A, Ishida T, Tanaka T. Constitutive activation of PI3K is involved in the spontaneous proliferation of primary acute myeloid leukemia cells: direct evidence of PI3K activation. Leukemia 2004; 18: 1438-1440.
13. Zhao S, Konopleva M, Cabreira-Hansen M, Xie Z, Hu W, Milella M et al. Inhibition of phosphatidylinositol 3-kinase dephosphorylates BAD and promotes apoptosis in myeloid leukemias. Leukemia 2004; 18: 267-275.
14. Sykes SM, Lane SW, Bullinger L, Kalaitzidis D, Yusuf R, Saez B et al. AKT/FOXO signaling enforces reversible differentiation blockade in myeloid leukemias. Cell 2011; 146: 697-708.
15. Myhre S, Mohammed H, Tramm T, Alsner J, Finak G, Park M et al. In silico ascription of gene expression differences to tumor and stromal cells in a model to study impact on breast cancer outcome. PLoS One 2010; 5: e14002.
16. Luo J, Emanuele MJ, Li D, Creighton CJ, Schlabach MR, Westbrook TF et al. A genome-wide RNAi screen identifi es multiple synthetic lethal interactions with the Ras oncogene. Cell 2009; 137: 835-848.
17. Grimwade D, Hills RK, Moorman AV, Walker H, Chatters S, Goldstone AH et al. Refinement of cytogenetic classification in acute myeloid leukemia: determination of prognostic significance of rare recurring chromosomal abnormalities among 5876 younger adult patients treated in the United Kingdom Medical Research Council trials. Blood 2010; 116: 354-365.
18. Zhang L, Huang J, Yang N, Greshock J, Liang S, Hasegawa K et al. Integrative genomic analysis of phosphatidylinositol 3'-kinase family identifi es PIK3R3 as a potential therapeutic target in epithelial ovarian cancer. Clin Cancer Res 2007; 13: 5314-5321.
19. Bertagnolo V, Benedusi M, Querzoli P, Pedriali M, Magri E, Brugnoli F et al. PLC-beta2 is highly expressed in breast cancer and is associated with a poor outcome: a study on tissue microarrays. Int J Oncol 2006; 28: 863-872.
20. Bertagnolo V, Benedusi M, Brugnoli F, Lanuti P, Marchisio M, Querzoli P et al. Phospholipase C-beta 2 promotes mitosis and migration of human breast cancer-derived cells. Carcinogenesis 2007; 28: 1638-1645.
21. Emerling BM, Hurov JB, Poulogiannis G, Tsukazawa KS, Choo-Wing R, Wulf GM et al. Depletion of a putatively druggable class of phosphatidylinositol kinases inhibits growth of p53-null tumors. Cell 2013; 155: 844-857.
22. Barretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S et al. The Cancer Cell Line Encyclopedia enables predictive mode of anticancer drug sensitivity. Nature 2012; 483: 603-607.
23. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, Beare D et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res 2011; 39: D945-D950.
24. Rhodes DR, Kalyana-Sundaram S, Mahavisno V, Varambally R, Yu J, Briggs BB et al. Oncomine 3.0: genes, pathways, and networks in a collection of 18,000 cancer gene expression profiles. Neoplasia 2007; 9: 166-180.
25. Wouters BJ, Louwers I, Valk PJ, Lowenberg B, Delwel R. A recurrent in-frame insertion in a CEBPA transactivation domain is a polymorphism rather than a mutation that does not affect gene expression profiling-based clustering of AML. Blood 2007; 109: 389-390.
26. Szczepanek J, Jarzab M, Oczko-Wojciechowska M, Kowalska M, Tretyn A, Haus O et al. Gene expression signatures and ex vivo drug sensitivity profiles in children with acute lymphoblastic leukemia. J Appl Genet 2012; 53: 83-91.
27. van den Bout I, Divecha N. PIP5K-driven PtdIns(4,5)P2 synthesis: regulation and cellular functions. J Cell Sci 2009; 122: 3837-3850.
28. Ling LE, Schulz JT, Cantley LC. Characterization and purification of membraneassociated phosphatidylinositol-4-phosphate kinase from human red blood cells. J Biol Chem 1989; 264: 5080-5088.
29. Schulze H, Korpal M, Hurov J, Kim SW, Zhang J, Cantley LC et al. Characterization of the megakaryocyte demarcation membrane system and its role in thrombopoiesis. Blood 2006; 107: 3868-3875.
30. Jones DR, Foulger R, Keune WJ, Bultsma Y, Divecha N. PtdIns5P is an oxidative stress-induced second messenger that regulated PKB activation. FASEB J 2013; 27: 1644-1656.
31. Viale A, De Franco F, Orleth A, Cambiaghi V, Giuliani V, Bossi D et al. Cell-cycle restriction limits DNA damage and maintains self-renewal of leukaemia stem cells. Nature 2009; 457: 51-56.
32. Saito Y, Uchida N, Tanaka S, Suzuki N, Tomizawa-Murasawa M, Sone A et al. Induction of cell cycle entry eliminates human leukemia stem cells in a mouse model of AML. Nat Biotechnol 2010; 28: 275-280.
33. Goardon N, Marchi E, Atzberger A, Quek L, Schuh A, Soneji S et al. Coexistence of LMPP-like and GMP-like leukemia stem cells in acute myeloid leukemia. Cancer Cell 2011; 19: 138-152.
34. Harris WJ, Huang X, Lynch JT, Spencer GJ, Hitchin JR, Li Y et al. The histone demethylase KDM1A sustains the oncogenic potential of MLL-AF9 leukemia stem cells. Cancer Cell 2012; 21: 473-487.
35. Somervaille TC, Cleary ML. Identification and characterization of leukemia stem cells in murine MLL-AF9 acute myeloid leukemia. Cancer Cell 2006; 10: 257-268.
36. Somervaille TC, Matheny CJ, Spencer GJ, Iwasaki M, Rinn JL, Witten DM et al. Hierarchical maintenance of MLL myeloid leukemia stem cells employs a transcriptional program shared with embryonic rather than adult stem cells. Cell Stem Cell 2009; 4: 129-140.
37. Wiseman D, Greystoke BF, Somervaille TC. The variety of leukemic stem cells in myeloid malignancy. Oncogene 2014; 33: 3091-3098.
38. Migliorini G, Fiege B, Hosking FJ, Ma Y, Kumar R, Sherborne AL et al. Variation at 10p12.2 and 10p14 influences risk of childhood B-cell acute lymphoblastic leukemia and phenotype. Blood 2013; 122 : 3298-3307.
39. Xu H, Yang W, Perez-Andreu V, Devidas M, Fan Y, Cheng S et al. Novel susceptibility variants at 10p12.31-12.2 for childhood acute lymphoblastic leukemia in ethnically diverse populations. J Natl Cancer Inst 2013; 105 : 733-742.
40. Davis MI, Sasaki AT, Shen M, Emerling BM, Thorne N, Michael S et al. A homogeneous, high-throughput assay for phosphatidylinositol 5-phosphate 4-kinase with a novel, rapid substrate preparation. PLoS One 2013; 8: e54127.
41. Beuvink I, Boulay B, Fumagalli S, Zilbermann F, Ruetz S, O'Reilly T et al. The mTOR inhibitor RAD001 sensitizes tumor cells to DNA-damaged induced apoptosis through inhibition of p21 translation. Cell 2005; 120: 747-759.
42. Wilcox A, Hinchliffe KA. Regulation of extranuclear PtdIns5P production by phosphatidylinositol phosphate 4-kinase 2alpha. FEBS Lett 2008; 582: 1391-1394.
43. Keune WJ, Jones DR, Bultsma Y, Sommer L, Zhou XZ, Lu KP et al. Regulation of phosphatidylinositol-5-phosphate signaling by Pin1 determines sensitivity to oxidative stress. Sci Signal 2012; 5: ra86.
44. Sarkes D, Rameh LE. A novel HPLC-based approach makes possible the spatial characterization of cellular PtdIns5P and other phosphoinositides. Biochem J 2010; 428: 375-384.
45. Jones DR, Bultsma Y, Keune WJ, Halstead JR, Elouarrat D, Mohammed S et al. Nuclear PtdIns5P as a transducer of stress signaling: an in vivo role for PIP4Kbeta. Mol Cell 2006; 23: 685-695.
46. Ndamukong I, Jones DR, Lapko H, Divecha N, Avramova Z. Phosphatidylinositol 5-phosphate links dehydration stress to the activity of ARABIDOPSIS TRITHORAXLIKE factor ATX1. PLoS One 2010; 5: e13396.
47. Keune WJ, Sims AH, Jones DR, Bultsma Y, Lynch JT, Jirstrom K et al. Low PIP4K2B expression in human breast tumors correlates with reduced patient survival: a role for PIP4K2B in the regulation of E-cadherin expression. Cancer Res 2013; 73: 6913-6925.
48. Jones DR, Foulger R, Keune WJ, Bultsma Y, Divecha N. PtdIns5P is an oxidative stress-induced second messenger that regulates PKB activation. FASEB J 2012; 27: 1644-1656.
49. Huang X, Spencer GJ, Lynch JT, Ciceri F, Somerville TD, Somervaille TC. Enhancers of Polycomb EPC1 and EPC2 sustain the oncogenic potential of MLL leukemia stem cells. Leukemia 2014; 28: 1081-1091.
50. Somervaille TC, Linch DC, Khwaja A. Different levels of p38 MAP kinase activity mediate distinct biological effects in primary human erythroid progenitors. Br J Haematol 2003; 120: 876-886.
51. Jones DR, Ramirez IB, Lowe M, Divecha N. Measurement of phosphoinositides in the zebrafish Danio rerio. Nat Protoc 2013; 8: 1058-1072.
52. Halstead JR, Roefs M, Ellson CD, D'Andrea S, Chen C, D'Santos CS et al. A novel pathway of cellular phosphatidylinositol(3,4,5)-trisphosphate synthesis is regulated by oxidative stress. Curr Biol 2001; 11: 386-395.