The nuclear phosphoinositide response to stress

References

• Hokin MR, Hokin LE. Enzyme secretion and the incorporation of P32 into phospholipides of pancreas slices. J Biol Chem. 1953;203:967–977.
   PubMed Web of Science ®Google Scholar
• Di Paolo G, De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature. 2006;443:651–657.
   PubMed Web of Science ®Google Scholar
• Rose HG, Frenster JH. Composition and metabolism of lipids within repressed and active chromatin of interphase lymphocytes. Biochim Biophys Acta. 1965;106:577–591.
   PubMedGoogle Scholar
• Manzoli FA, Maraldi NM, Cocco L, et al. Chromatin phospholipids in normal and chronic lymphocytic leukemia lymphocytes. Cancer Res. 1977;37:843–849.
   PubMed Web of Science ®Google Scholar
• Smith CD, Wells WW. Phosphorylation of rat liver nuclear envelopes. II. Characterization of in vitro lipid phosphorylation. J Biol Chem. 1983;258:9368–9373.
   PubMed Web of Science ®Google Scholar
• Cocco L, Gilmour RS, Ognibene A, et al. Synthesis of polyphosphoinositides in nuclei of friend cells. Evidence for polyphosphoinositide metabolism inside the nucleus which changes with cell differentiation. Biochem J. 1987;248:765–770.
   PubMed Web of Science ®Google Scholar
• Boronenkov IV, Loijens JC, Umeda M, et al. Phosphoinositide signaling pathways in nuclei are associated with nuclear speckles containing pre-mRNA processing factors. Mol Biol Cell. 1998;9:3547–3560.
   PubMed Web of Science ®Google Scholar
• Barlow CA, Laishram RS, Anderson RA. Nuclear phosphoinositides: a signaling enigma wrapped in a compartmental conundrum. Trends Cell Biol. 2010;20:25–35.
   PubMed Web of Science ®Google Scholar
• Sztacho M, Sobol M, Balaban C, et al. Nuclear phosphoinositides and phase separation: important players in nuclear compartmentalization. Adv Biol Regul. 2019;71:111–117.
   PubMedGoogle Scholar
• Castano E, Yildirim S, Faberova V, et al. Nuclear phosphoinositides-versatile regulators of genome functions. Cells. 2019;8(7):649.
   Web of Science ®Google Scholar
• Dickson EJ, Hille B. Understanding phosphoinositides: rare, dynamic, and essential membrane phospholipids. Biochem J. 2019;476:1–23.
   PubMed Web of Science ®Google Scholar
• Shisheva A. Regulating Glut4 vesicle dynamics by phosphoinositide kinases and phosphoinositide phosphatases. Front Biosci. 2003;8:s945–s946.
   PubMed Web of Science ®Google Scholar
• Rameh LE, Cantley LC. The role of phosphoinositide 3-kinase lipid products in cell function. J Biol Chem. 1999;274:8347–8350.
   PubMed Web of Science ®Google Scholar
• Liu Y, Bankaitis VA. Phosphoinositide phosphatases in cell biology and disease. Prog Lipid Res. 2010;49:201–217.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Bryant JM, Blind RD. Signaling through non-membrane nuclear phosphoinositide binding proteins in human health and disease. J Lipid Res. 2019;60:299–311.
   PubMed Web of Science ®Google Scholar
• Fu P, Ebenezer DL, Ha AW, et al. Nuclear lipid mediators: role of nuclear sphingolipids and sphingosine-1-phosphate signaling in epigenetic regulation of inflammation and gene expression. J Cell Biochem. 2018;119:6337–6353.
   PubMed Web of Science ®Google Scholar
• Poli A, Billi AM, Mongiorgi S, et al. Nuclear phosphatidylinositol signaling: focus on phosphatidylinositol phosphate kinases and phospholipases C. J Cell Physiol. 2016;231:1645–1655.
   PubMed Web of Science ®Google Scholar
• Hamann BL, Blind RD. Nuclear phosphoinositide regulation of chromatin. J Cell Physiol. 2018;233:107–123.
   PubMed Web of Science ®Google Scholar
• Jacobsen RG, Mazloumi Gavgani F, Edson AJ, et al. Polyphosphoinositides in the nucleus: roadmap of their effectors and mechanisms of interaction. Adv Biol Regul. 2019;72:7–21.
   PubMedGoogle Scholar
• Shah ZH, Jones DR, Sommer L, et al. Nuclear phosphoinositides and their impact on nuclear functions. Febs J. 2013;280:6295–6310.
   PubMed Web of Science ®Google Scholar
• Gillooly DJ, Morrow IC, Lindsay M, et al. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. Embo J. 2000;19:4577–4588.
   PubMed Web of Science ®Google Scholar
• Kalasova I, Faberova V, Kalendova A, et al. Tools for visualization of phosphoinositides in the cell nucleus. Histochem Cell Biol. 2016;145:485–496.
   PubMed Web of Science ®Google Scholar
• Sindic A, Aleksandrova A, Fields AP, et al. Presence and activation of nuclear phosphoinositide 3-kinase C2beta during compensatory liver growth. J Biol Chem. 2001;276:17754–17761.
   PubMed Web of Science ®Google Scholar
• Choi S, Chen M, Cryns VL, et al. A nuclear phosphoinositide kinase complex regulates p53. Nat Cell Biol. 2019;21:462–475.
   PubMed Web of Science ®Google Scholar
• Clarke JH, Letcher AJ, D’Santos CS, et al. Inositol lipids are regulated during cell cycle progression in the nuclei of murine erythroleukaemia cells. Biochem J. 2001;357:905–910.
   PubMed Web of Science ®Google Scholar
• Zhang L, Malik S, Pang J, et al. Phospholipase Cepsilon hydrolyzes perinuclear phosphatidylinositol 4-phosphate to regulate cardiac hypertrophy. Cell. 2013;153:216–227.
   PubMed Web of Science ®Google Scholar
• Wang YH, Hariharan A, Bastianello G, et al. DNA damage causes rapid accumulation of phosphoinositides for ATR signaling. Nat Commun. 2017;8:2118.
   PubMed Web of Science ®Google Scholar
• Gozani O, Karuman P, Jones DR, et al. The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell. 2003;114:99–111.
   PubMed Web of Science ®Google Scholar
• Jones DR, Bultsma Y, Keune WJ, et al. Nuclear PtdIns5P as a transducer of stress signaling: an in vivo role for PIP4Kbeta. Mol Cell. 2006;23:685–695.
   PubMed Web of Science ®Google Scholar
• Bua DJ, Martin GM, Binda O, et al. Nuclear phosphatidylinositol-5-phosphate regulates ING2 stability at discrete chromatin targets in response to DNA damage. Sci Rep. 2013;3:2137.
   PubMed Web of Science ®Google Scholar
• Bunce MW, Boronenkov IV, Anderson RA. Coordinated activation of the nuclear ubiquitin ligase Cul3-SPOP by the generation of phosphatidylinositol 5-phosphate. J Biol Chem. 2008;283:8678–8686.
   PubMed Web of Science ®Google Scholar
• Poli A, Zaurito AE, Abdul-Hamid S, et al. Phosphatidylinositol 5 phosphate (PI5P): from behind the scenes to the front (nuclear) stage. Int J Mol Sci. 2019;20(9):2080.
   Web of Science ®Google Scholar
• Van der Kaay J, Beck M, Gray A, et al. Distinct phosphatidylinositol 3-kinase lipid products accumulate upon oxidative and osmotic stress and lead to different cellular responses. J Biol Chem. 1999;274:35963–35968.
   PubMed Web of Science ®Google Scholar
• Deleris P, Bacqueville D, Gayral S, et al. SHIP-2 and PTEN are expressed and active in vascular smooth muscle cell nuclei, but only SHIP-2 is associated with nuclear speckles. J Biol Chem. 2003;278:38884–38891.
   PubMed Web of Science ®Google Scholar
• Ehm P, Nalaskowski MM, Wundenberg T, et al. The tumor suppressor SHIP1 colocalizes in nucleolar cavities with p53 and components of PML nuclear bodies. Nucleus. 2015;6:154–164.
   PubMed Web of Science ®Google Scholar
• Yokogawa T, Nagata S, Nishio Y, et al. Evidence that 3 ‘-phosphorylated polyphosphoinositides are generated at the nuclear surface: use of immunostaining technique with monoclonal antibodies specific for PI 3,4-P-2. Febs Lett. 2000;473:222–226.
   PubMed Web of Science ®Google Scholar
• Osborne SL, Thomas CL, Gschmeissner S, et al. Nuclear PtdIns(4,5)P2 assembles in a mitotically regulated particle involved in pre-mRNA splicing. J Cell Sci. 2001;114:2501–2511.
   PubMed Web of Science ®Google Scholar
• Yoo SH, Huh YH, Huh SK, et al. Localization and projected role of phosphatidylinositol 4-kinases IIalpha and IIbeta in inositol 1,4,5-trisphosphate-sensitive nucleoplasmic Ca(2)(+) store vesicles. Nucleus. 2014;5:341–351.
   PubMed Web of Science ®Google Scholar
• Watt SA, Kular G, Fleming IN, et al. Subcellular localization of phosphatidylinositol 4,5-bisphosphate using the pleckstrin homology domain of phospholipase C delta1. Biochem J. 2002;363:657–666.
   PubMed Web of Science ®Google Scholar
• Sobol M, Krausova A, Yildirim S, et al. Nuclear phosphatidylinositol 4,5-bisphosphate islets contribute to efficient RNA polymerase II-dependent transcription. J Cell Sci. 2018;131:8.
   Web of Science ®Google Scholar
• Li W, Laishram RS, Ji Z, et al. Star-PAP control of BIK expression and apoptosis is regulated by nuclear PIPKIalpha and PKCdelta signaling. Mol Cell. 2012;45:25–37.
   PubMed Web of Science ®Google Scholar
• Mellman DL, Gonzales ML, Song C, et al. A PtdIns4,5P2-regulated nuclear poly(A) polymerase controls expression of select mRNAs. Nature. 2008;451:1013–1017.
   PubMed Web of Science ®Google Scholar
• Mishkind M, Vermeer JE, Darwish E, et al. Heat stress activates phospholipase D and triggers PIP accumulation at the plasma membrane and nucleus. Plant J. 2009;60:10–21.
   PubMed Web of Science ®Google Scholar
• Lindsay Y, McCoull D, Davidson L, et al. Localization of agonist-sensitive PtdIns(3,4,5)P3 reveals a nuclear pool that is insensitive to PTEN expression. J Cell Sci. 2006;119:5160–5168.
   PubMed Web of Science ®Google Scholar
• Karlsson T, Altankhuyag A, Dobrovolska O, et al. A polybasic motif in ErbB3-binding protein 1 (EBP1) has key functions in nucleolar localization and polyphosphoinositide interaction. Biochem J. 2016;473:2033–2047.
   PubMed Web of Science ®Google Scholar
• Tanaka K, Horiguchi K, Yoshida T, et al. Evidence that a phosphatidylinositol 3,4,5-trisphosphate-binding protein can function in nucleus. J Biol Chem. 1999;274:3919–3922.
   PubMed Web of Science ®Google Scholar
• Kobayashi M, Muroyama A, Ohizumi Y. Phosphatidylinositol 4,5-bisphosphate enhances calcium release from sarcoplasmic reticulum of skeletal muscle. Biochem Biophys Res Commun. 1989;163:1487–1491.
   PubMed Web of Science ®Google Scholar
• Prole DL, Taylor CW. Structure and function of IP3 receptors. Cold Spring Harb Perspect Biol. 2019;11(4).
   Web of Science ®Google Scholar
• Romanauska A, Kohler A. The inner nuclear membrane is a metabolically active territory that generates nuclear lipid droplets. Cell. 2018;174:700-+.
   PubMed Web of Science ®Google Scholar
• Payrastre B, Nievers M, Boonstra J, et al. A differential location of phosphoinositide kinases, diacylglycerol kinase, and phospholipase-C in the nuclear matrix. J Biol Chem. 1992;267:5078–5084.
   PubMed Web of Science ®Google Scholar
• Zima AV, Bare DJ, Mignery GA, et al. IP3-dependent nuclear Ca2+ signalling in the mammalian heart. J Physiol. 2007;584:601–611.
   PubMed Web of Science ®Google Scholar
• Humbert JP, Matter N, Artault JC, et al. Inositol 1,4,5-trisphosphate receptor is located to the inner nuclear membrane vindicating regulation of nuclear calcium signaling by inositol 1,4,5-trisphosphate. Discrete distribution of inositol phosphate receptors to inner and outer nuclear membranes (vol 271, pg 478, 1996). J Biol Chem. 1996;271:5287.
   Web of Science ®Google Scholar
• Echevarria W, Leite MF, Guerra MT, et al. Regulation of calcium signals in the nucleus by a nucleoplasmic reticulum. Nat Cell Biol. 2003;5:440–446.
   PubMed Web of Science ®Google Scholar
• Tabellini G, Bortul R, Santi S, et al. Diacylglycerol kinase-theta is localized in the speckle domains of the nucleus. Exp Cell Res. 2003;287:143–154.
   PubMed Web of Science ®Google Scholar
• Neri LM, Bortul R, Borgatti P, et al. Proliferating or differentiating stimuli act on different lipid-dependent signaling pathways in nuclei of human leukemia cells. Mol Biol Cell. 2002;13:947–964.
   PubMed Web of Science ®Google Scholar
• Zhang H, Shao Z, Alibin CP, et al. Liganded peroxisome proliferator-activated receptors (PPARs) preserve nuclear histone deacetylase 5 levels in endothelin-treated Sprague-Dawley rat cardiac myocytes. PLoS One. 2014;9:e115258.
   PubMed Web of Science ®Google Scholar
• Arantes LAM, Aguiar CJ, Amaya MJ, et al. Nuclear inositol 1,4,5-trisphosphate is a necessary and conserved signal for the induction of both pathological and physiological cardiomyocyte hypertrophy. J Mol Cell Cardiol. 2012;53:475–486.
   PubMed Web of Science ®Google Scholar
• Balla A, Balla T. Phosphatidylinositol 4-kinases: old enzymes with emerging functions. Trends Cell Biol. 2006;16:351–361.
   PubMed Web of Science ®Google Scholar
• Boura E, Nencka R. Phosphatidylinositol 4-kinases: function, structure, and inhibition. Exp Cell Res. 2015;337:136–145.
   PubMed Web of Science ®Google Scholar
• Kakuk A, Friedlander E, Vereb G Jr., et al. Nucleolar localization of phosphatidylinositol 4-kinase PI4K230 in various mammalian cells. Cytometry A. 2006;69:1174–1183.
   PubMedGoogle Scholar
• de Graaf P, Klapisz EE, Schulz TK, et al. Nuclear localization of phosphatidylinositol 4-kinase beta. J Cell Sci. 2002;115:1769–1775.
   PubMed Web of Science ®Google Scholar
• Szivak I, Lamb N, Heilmeyer LM. Subcellular localization and structural function of endogenous phosphorylated phosphatidylinositol 4-kinase (PI4K92). J Biol Chem. 2006;281:16740–16749.
   PubMed Web of Science ®Google Scholar
• Heilmeyer LM Jr., Vereb G Jr., Vereb G, et al. Mammalian phosphatidylinositol 4-kinases. IUBMB Life. 2003;55:59–65.
   PubMed Web of Science ®Google Scholar
• Schill NJ, Anderson RA. Two novel phosphatidylinositol-4-phosphate 5-kinase type Igamma splice variants expressed in human cells display distinctive cellular targeting. Biochem J. 2009;422:473–482.
   PubMed Web of Science ®Google Scholar
• Chakrabarti R, Sanyal S, Ghosh A, et al. Phosphatidylinositol-4-phosphate 5-kinase 1alpha modulates ribosomal RNA gene Silencing through its interaction with histone H3 lysine 9 trimethylation and heterochromatin protein HP1-alpha. J Biol Chem. 2015;290:20893–20903.
   PubMed Web of Science ®Google Scholar
• Ciruela A, Hinchliffe KA, Divecha N, et al. Nuclear targeting of the beta isoform of type II phosphatidylinositol phosphate kinase (phosphatidylinositol 5-phosphate 4-kinase) by its alpha-helix 7. Biochem J. 2000;346(Pt 3):587–591.
   PubMedGoogle Scholar
• Richardson JP, Wang MC, Clarke JH, et al. Genomic tagging of endogenous Type II beta phosphatidylinositol 5-phosphate 4-kinase in DT40 cells reveals a nuclear localisation. Cell Signal. 2007;19:1309–1314.
   PubMed Web of Science ®Google Scholar
• Kouchi Z, Fujiwara Y, Yamaguchi H, et al. Phosphatidylinositol 5-phosphate 4-kinase type II beta is required for vitamin D receptor-dependent E-cadherin expression in SW480 cells. Biochem Biophys Res Commun. 2011;408:523–529.
   PubMed Web of Science ®Google Scholar
• Stijf-Bultsma Y, Sommer L, Tauber M, et al. The basal transcription complex component TAF3 transduces changes in nuclear phosphoinositides into transcriptional output. Mol Cell. 2015;58:453–467.
   PubMed Web of Science ®Google Scholar
• Jean S, Kiger AA. Classes of phosphoinositide 3-kinases at a glance. J Cell Sci. 2014;127:923–928.
   PubMed Web of Science ®Google Scholar
• Kumar A, Redondo-Munoz J, Perez-Garcia V, et al. Nuclear but not cytosolic phosphoinositide 3-kinase beta has an essential function in cell survival. Mol Cell Biol. 2011;31:2122–2133.
   PubMed Web of Science ®Google Scholar
• Kumar A, Fernandez-Capetillo O, Carrera AC. Nuclear phosphoinositide 3-kinase beta controls double-strand break DNA repair. Proc Natl Acad Sci U S A. 2010;107:7491–7496.
   PubMed Web of Science ®Google Scholar
• Marques M, Kumar A, Poveda AM, et al. Specific function of phosphoinositide 3-kinase beta in the control of DNA replication. Proc Natl Acad Sci U S A. 2009;106:7525–7530.
   PubMed Web of Science ®Google Scholar
• Didichenko SA, Thelen M. Phosphatidylinositol 3-kinase c2alpha contains a nuclear localization sequence and associates with nuclear speckles. J Biol Chem. 2001;276:48135–48142.
   PubMed Web of Science ®Google Scholar
• Banfic H, Visnjic D, Mise N, et al. Epidermal growth factor stimulates translocation of the class II phosphoinositide 3-kinase PI3K-C2beta to the nucleus. Biochem J. 2009;422:53–60.
   PubMed Web of Science ®Google Scholar
• Resnick AC, Snowman AM, Kang BN, et al. Inositol polyphosphate multikinase is a nuclear P13-kinase with transcriptional regulatory activity. Proc Natl Acad Sci U S A. 2005;102:12783–12788.
   PubMed Web of Science ®Google Scholar
• Kim E, Beon J, Lee S, et al. IPMK: A versatile regulator of nuclear signaling events. Adv Biol Regul. 2016;61:25–32.
   PubMedGoogle Scholar
• Blind RD, Suzawa M, Ingraham HA. Direct modification and activation of a nuclear receptor-PIP(2) complex by the inositol lipid kinase IPMK. Sci Signal. 2012;5:ra44.
   PubMed Web of Science ®Google Scholar
• Xu R, Sen N, Paul BD, et al. Inositol polyphosphate multikinase is a coactivator of p53-mediated transcription and cell death. Sci Signal. 2013;6:ra22.
   PubMed Web of Science ®Google Scholar
• Lee YR, Chen M, Pandolfi PP. The functions and regulation of the PTEN tumour suppressor: new modes and prospects. Nat Rev Mol Cell Biol. 2018;19:547–562.
   PubMed Web of Science ®Google Scholar
• Li P, Wang D, Li H, et al. Identification of nucleolus-localized PTEN and its function in regulating ribosome biogenesis. Mol Biol Rep. 2014;41:6383–6390.
   PubMed Web of Science ®Google Scholar
• Shen WH, Balajee AS, Wang J, et al. Essential role for nuclear PTEN in maintaining chromosomal integrity. Cell. 2007;128:157–170.
   PubMed Web of Science ®Google Scholar
• Choi BH, Chen Y, Dai W. Chromatin PTEN is involved in DNA damage response partly through regulating Rad52 sumoylation. Cell Cycle. 2013;12:3442–3447.
   PubMed Web of Science ®Google Scholar
• Chang CJ, Mulholland DJ, Valamehr B, et al. PTEN nuclear localization is regulated by oxidative stress and mediates p53-dependent tumor suppression. Mol Cell Biol. 2008;28:3281–3289.
   PubMed Web of Science ®Google Scholar
• Trotman LC, Pandolfi PP. PTEN and p53: who will get the upper hand?. Cancer Cell. 2003;3:97–99.
   PubMed Web of Science ®Google Scholar
• Freeman DJ, Li AG, Wei G, et al. PTEN tumor suppressor regulates p53 protein levels and activity through phosphatase-dependent and -independent mechanisms. Cancer Cell. 2003;3:117–130.
   PubMed Web of Science ®Google Scholar
• Mayo LD, Donner DB. The PTEN, Mdm2, p53 tumor suppressor-oncoprotein network. Trends Biochem Sci. 2002;27:462–467.
   PubMed Web of Science ®Google Scholar
• Mayo LD, Dixon JE, Durden DL, et al. PTEN protects p53 from Mdm2 and sensitizes cancer cells to chemotherapy. J Biol Chem. 2002;277:5484–5489.
   PubMed Web of Science ®Google Scholar
• Stambolic V, MacPherson D, Sas D, et al. Regulation of PTEN transcription by p53. Mol Cell. 2001;8:317–325.
   PubMed Web of Science ®Google Scholar
• Elong Edimo W, Derua R, Janssens V, et al. Evidence of SHIP2 Ser132 phosphorylation, its nuclear localization and stability. Biochem J. 2011;439:391–401.
   PubMed Web of Science ®Google Scholar
• Zou J, Marjanovic J, Kisseleva MV, et al. Type I phosphatidylinositol-4, 5-bisphosphate 4-phosphatase regulates stress-induced apoptosis. Proc Natl Acad Sci U S A. 2007;104:16834–16839.
   PubMed Web of Science ®Google Scholar
• Cocco L, Rubbini S, Manzoli L, et al. Inositides in the nucleus: presence and characterisation of the isozymes of phospholipase beta family in NIH 3T3 cells. Biochim Biophys Acta. 1999;1438:295–299.
   PubMed Web of Science ®Google Scholar
• Lee YH, Kim SY, Kim JR, et al. Overexpression of phospholipase Cbeta-1 protects NIH3T3 cells from oxidative stress-induced cell death. Life Sci. 2000;67:827–837.
   PubMed Web of Science ®Google Scholar
• Stallings JD, Tall EG, Pentyala S, et al. Nuclear translocation of phospholipase C-delta(1) is linked to the cell cycle and nuclear phosphatidylinositol 4,5-bisphosphate. J Biol Chem. 2005;280:22060–22069.
   PubMed Web of Science ®Google Scholar
• Kunrath-Lima M, de Miranda MC, Ferreira ADF, et al. Phospholipase C delta 4 (PLCdelta4) is a nuclear protein involved in cell proliferation and senescence in mesenchymal stromal stem cells. Cell Signal. 2018;49:59–67.
   PubMed Web of Science ®Google Scholar
• Chi B, Wang Q, Wu G, et al. Aly and THO are required for assembly of the human TREX complex and association of TREX components with the spliced mRNA. Nucleic Acids Res. 2013;41:1294–1306.
   PubMed Web of Science ®Google Scholar
• Okada M, Jang SW, Ye K. Akt phosphorylation and nuclear phosphoinositide association mediate mRNA export and cell proliferation activities by ALY. Proc Natl Acad Sci U S A. 2008;105:8649–8654.
   PubMed Web of Science ®Google Scholar
• Wickramasinghe VO, Savill JM, Chavali S, et al. Human inositol polyphosphate multikinase regulates transcript-selective nuclear mRNA export to preserve genome integrity. Mol Cell. 2013;51:737–750.
   PubMed Web of Science ®Google Scholar
• Toska E, Campbell HA, Shandilya J, et al. Repression of transcription by WT1-BASP1 requires the myristoylation of BASP1 and the PIP2-dependent recruitment of histone deacetylase. Cell Rep. 2012;2:462–469.
   PubMed Web of Science ®Google Scholar
• Wu C, Wang Y, Xia Y, et al. Wilms’ tumor 1 enhances Cisplatin-resistance of advanced NSCLC. Febs Lett. 2014;588:4566–4572.
   PubMed Web of Science ®Google Scholar
• Gadadhar S, Bora N, Tiwari V, et al. Sequestration of the abrin A chain to the nucleus by BASP1 increases the resistance of cells to abrin toxicity. Biochem J. 2014;458:375–385.
   PubMed Web of Science ®Google Scholar
• Kadoch C, Crabtree GR. Mammalian SWI/SNF chromatin remodeling complexes and cancer: mechanistic insights gained from human genomics. Sci Adv. 2015;1:e1500447.
   PubMed Web of Science ®Google Scholar
• Khan P, Drobic B, Perez-Cadahia B, et al. Mitogen- and stress-activated protein kinases 1 and 2 are required for maximal trefoil factor 1 induction. PLoS One. 2013;8:e63189.
   PubMed Web of Science ®Google Scholar
• Li F, Liang J, Tang D. Brahma-related gene 1 ameliorates the neuronal apoptosis and oxidative stress induced by oxygen-glucose deprivation/reoxygenation through activation of Nrf2/HO-1 signaling. Biomed Pharmacother. 2018;108:1216–1224.
   PubMed Web of Science ®Google Scholar
• Porter EG, Dhiman A, Chowdhury B, et al. PBRM1 regulates stress response in epithelial cells. iScience. 2019;15:196–210.
   PubMed Web of Science ®Google Scholar
• Zhao K, Wang W, Rando OJ, et al. Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell. 1998;95:625–636.
   PubMed Web of Science ®Google Scholar
• Rando OJ, Zhao K, Janmey P, et al. Phosphatidylinositol-dependent actin filament binding by the SWI/SNF-like BAF chromatin remodeling complex. Proc Natl Acad Sci U S A. 2002;99:2824–2829.
   PubMed Web of Science ®Google Scholar
• Shubina MY, Musinova YR, Sheval EV. Nucleolar methyltransferase fibrillarin: evolution of structure and functions. Biochemistry (Mosc). 2016;81:941–950.
   PubMed Web of Science ®Google Scholar
• Yildirim S, Castano E, Sobol M, et al. Involvement of phosphatidylinositol 4,5-bisphosphate in RNA polymerase I transcription. J Cell Sci. 2013;126:2730–2739.
   PubMed Web of Science ®Google Scholar
• Tiku V, Kew C, Mehrotra P, et al. Nucleolar fibrillarin is an evolutionarily conserved regulator of bacterial pathogen resistance. Nat Commun. 2018;9(1):3607.
   Web of Science ®Google Scholar
• Sobol M, Yildirim S, Philimonenko VV, et al. UBF complexes with phosphatidylinositol 4,5-bisphosphate in nucleolar organizer regions regardless of ongoing RNA polymerase I activity. Nucleus. 2013;4:478–486.
   PubMed Web of Science ®Google Scholar
• Kodiha M, Banski P, Stochaj U. Computer-based fluorescence quantification: a novel approach to study nucleolar biology. BMC Cell Biol. 2011;12:25.
   PubMedGoogle Scholar
• Nagashima M, Shiseki M, Miura K, et al. DNA damage-inducible gene p33ING2 negatively regulates cell proliferation through acetylation of p53. Proc Natl Acad Sci U S A. 2001;98:9671–9676.
   PubMed Web of Science ®Google Scholar
• Lindstrom MS. NPM1/B23: A multifunctional chaperone in ribosome biogenesis and chromatin remodeling. Biochem Res Int. 2011;2011:195209.
   PubMedGoogle Scholar
• Li J, Zhang X, Sejas DP, et al. Negative regulation of p53 by nucleophosmin antagonizes stress-induced apoptosis in human normal and malignant hematopoietic cells. Leuk Res. 2005;29:1415–1423.
   PubMed Web of Science ®Google Scholar
• Kurki S, Peltonen K, Latonen L, et al. Nucleolar protein NPM interacts with HDM2 and protects tumor suppressor protein p53 from HDM2-mediated degradation. Cancer Cell. 2004;5:465–475.
   PubMed Web of Science ®Google Scholar
• Borer RA, Lehner CF, Eppenberger HM, et al. Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell. 1989;56:379–390.
   PubMed Web of Science ®Google Scholar
• Ahn JY, Liu X, Cheng D, et al. Nucleophosmin/B23, a nuclear PI(3,4,5)P(3) receptor, mediates the antiapoptotic actions of NGF by inhibiting CAD. Mol Cell. 2005;18:435–445.
   PubMed Web of Science ®Google Scholar
• Feric M, Vaidya N, Harmon TS, et al. Coexisting liquid phases underlie nucleolar subcompartments. Cell. 2016;165:1686–1697.
   PubMed Web of Science ®Google Scholar
• Mitrea DM, Cika JA, Stanley CB, et al. Self-interaction of NPM1 modulates multiple mechanisms of liquid-liquid phase separation. Nat Commun. 2018;9:842.
   PubMed Web of Science ®Google Scholar
• Ulicna L, Kalendova A, Kalasova I, et al. PIP2 epigenetically represses rRNA genes transcription interacting with PHF8. Biochim Biophys Acta Mol Cell Biol Lipids. 2018;1863:266–275.
   PubMed Web of Science ®Google Scholar
• Wang Q, Ma S, Song N, et al. Stabilization of histone demethylase PHF8 by USP7 promotes breast carcinogenesis. J Clin Invest. 2016;126:2205–2220.
   PubMed Web of Science ®Google Scholar
• Viiri KM, Janis J, Siggers T, et al. DNA-binding and -bending activities of SAP30L and SAP30 are mediated by a zinc-dependent module and monophosphoinositides. Mol Cell Biol. 2009;29:342–356.
   PubMed Web of Science ®Google Scholar
• Viiri KM, Korkeamaki H, Kukkonen MK, et al. SAP30L interacts with members of the Sin3A corepressor complex and targets Sin3A to the nucleolus. Nucleic Acids Res. 2006;34:3288–3298.
   PubMed Web of Science ®Google Scholar
• Krylova IN, Sablin EP, Moore J, et al. Structural analyses reveal phosphatidyl inositols as ligands for the NR5 orphan receptors SF-1 and LRH-1. Cell. 2005;120:343–355.
   PubMed Web of Science ®Google Scholar
• Blind RD, Sablin EP, Kuchenbecker KM, et al. The signaling phospholipid PIP3 creates a new interaction surface on the nuclear receptor SF-1. Proc Natl Acad Sci U S A. 2014;111:15054–15059.
   PubMed Web of Science ®Google Scholar
• Bland ML, Jamieson CA, Akana SF, et al. Haploinsufficiency of steroidogenic factor-1 in mice disrupts adrenal development leading to an impaired stress response. Proc Natl Acad Sci U S A. 2000;97:14488–14493.
   PubMed Web of Science ®Google Scholar
• Mortier E, Wuytens G, Leenaerts I, et al. Nuclear speckles and nucleoli targeting by PIP2-PDZ domain interactions. Embo J. 2005;24:2556–2565.
   PubMed Web of Science ®Google Scholar
• Liu XL, Gao QQ, Li PS, et al. UHRF1 targets DNMT1 for DNA methylation through cooperative binding of hemi-methylated DNA and methylated H3K9. Nat Commun. 2013;4:1563.
   Web of Science ®Google Scholar
• Bronner C, Fuhrmann G, Chedin FL, et al. UHRF1 links the histone code and DNA methylation to ensure faithful epigenetic memory inheritance. Genet Epigenet. 2010;2009:29–36.
   PubMedGoogle Scholar
• Wang F, Yang YZ, Shi CZ, et al. UHRF1 promotes cell growth and metastasis through repression of p16(ink4a) in colorectal cancer. Ann Surg Oncol. 2012;19:2753–2762.
   PubMed Web of Science ®Google Scholar
• Gelato KA, Tauber M, Ong MS, et al. Accessibility of different histone H3-binding domains of UHRF1 is allosterically regulated by phosphatidylinositol 5-phosphate. Mol Cell. 2014;54:905–919.
   PubMed Web of Science ®Google Scholar
• Tian YY, Paramasivam M, Ghosal G, et al. UHRF1 contributes to DNA damage repair as a lesion recognition factor and nuclease scaffold. Cell Rep. 2015;10:1957–1966.
   PubMed Web of Science ®Google Scholar
• Abu-Alainin W, Gana T, Liloglou T, et al. UHRF1 regulation of the Keap1-Nrf2 pathway in pancreatic cancer contributes to oncogenesis. J Pathol. 2016;238:423–433.
   PubMed Web of Science ®Google Scholar
• Bronner C, Achour M, Arima Y, et al. The UHRF family: oncogenes that are drugable targets for cancer therapy in the near future? Pharmacol Ther. 2007;115:419–434.
   PubMed Web of Science ®Google Scholar
• Unoki M, Brunet J, Mousli M. Drug discovery targeting epigenetic codes: the great potential of UHRF1, which links DNA methylation and histone modifications, as a drug target in cancers and toxoplasmosis. Biochem Pharmacol. 2009;78:1279–1288.
   PubMed Web of Science ®Google Scholar
• Trippe R, Guschina E, Hossbach M, et al. Identification, cloning, and functional analysis of the human U6 snRNA-specific terminal uridylyl transferase. RNA. 2006;12:1494–1504.
   PubMed Web of Science ®Google Scholar
• Li W, Li W, Laishram RS, et al. Distinct regulation of alternative polyadenylation and gene expression by nuclear poly(A) polymerases. Nucleic Acids Res. 2017;45:8930–8942.
   PubMed Web of Science ®Google Scholar
• Laishram RS, Anderson RA. The poly A polymerase star-PAP controls 3ʹ-end cleavage by promoting CPSF interaction and specificity toward the pre-mRNA. Embo J. 2010;29:4132–4145.
   PubMed Web of Science ®Google Scholar
• Laishram RS, Barlow CA, Anderson RA. CKI isoforms α and ε regulate star-PAP target messages by controlling star-PAP poly(A) polymerase activity and phosphoinositide stimulation. Nucleic Acids Res. 2011;39:7961–7973.
   PubMed Web of Science ®Google Scholar
• Dai C, Gu W. p53 post-translational modification: deregulated in tumorigenesis. Trends Mol Med. 2010;16:528–536.
   PubMed Web of Science ®Google Scholar
• Bieging KT, Mello SS, Attardi LD. Unravelling mechanisms of p53-mediated tumour suppression. Nat Rev Cancer. 2014;14:359–370.
   PubMed Web of Science ®Google Scholar
• Kruiswijk F, Labuschagne CF, Vousden KH. p53 in survival, death and metabolic health: a lifeguard with a licence to kill. Nat Rev Mol Cell Biol. 2015;16:393–405.
   PubMed Web of Science ®Google Scholar
• Freed-Pastor WA, Prives C. Mutant p53: one name, many proteins. Genes Dev. 2012;26:1268–1286.
   PubMed Web of Science ®Google Scholar
• Muller PA, Vousden KH. Mutant p53 in cancer: new functions and therapeutic opportunities. Cancer Cell. 2014;25:304–317.
   PubMed Web of Science ®Google Scholar
• Weibrecht I, Leuchowius KJ, Clausson CM, et al. Proximity ligation assays: a recent addition to the proteomics toolbox. Expert Rev Proteomics. 2010;7:401–409.
   PubMed Web of Science ®Google Scholar
• Sehat B, Tofigh A, Lin Y, et al. SUMOylation mediates the nuclear translocation and signaling of the IGF-1 receptor. Sci Signal. 2010;3:ra10.
   PubMed Web of Science ®Google Scholar
• Chen M, Qiu T, Wu J, et al. Extracellular anti-angiogenic proteins augment an endosomal protein trafficking pathway to reach mitochondria and execute apoptosis in HUVECs. Cell Death Differ. 2018;25:1905–1920.
   PubMed Web of Science ®Google Scholar
• Chen M, Zhang Y, Yu VC, et al. Isthmin targets cell-surface GRP78 and triggers apoptosis via induction of mitochondrial dysfunction. Cell Death Differ. 2014;21:797–810.
   PubMed Web of Science ®Google Scholar
• Semenas J, Hedblom A, Miftakhova RR, et al. The role of PI3K/AKT-related PIP5K1alpha and the discovery of its selective inhibitor for treatment of advanced prostate cancer. Proc Natl Acad Sci U S A. 2014;111:E3689–E3698.
   PubMed Web of Science ®Google Scholar
• Arrigo AP, Gibert B. HspB1, HspB5 and HspB4 in human cancers: potent oncogenic role of some of their client proteins. Cancers (Basel). 2014;6:333–365.
   PubMed Web of Science ®Google Scholar
• Malin D, Petrovic V, Strekalova E, et al. alphaB-crystallin: portrait of a malignant chaperone as a cancer therapeutic target. Pharmacol Ther. 2016;160:1–10.
   PubMed Web of Science ®Google Scholar
• Fiume R, Faenza I, Sheth B, et al. Nuclear phosphoinositides: their regulation and roles in nuclear functions. Int J Mol Sci. 2019;20:2991.
   Web of Science ®Google Scholar
• Choi S, Hedman AC, Sayedyahossein S, et al. Agonist-stimulated phosphatidylinositol-3,4,5-trisphosphate generation by scaffolded phosphoinositide kinases. Nat Cell Biol. 2016;18:1324–1335.
   PubMed Web of Science ®Google Scholar
• Chen M, Choi S, Jung O, et al. The specificity of EGF-stimulated IQGAP1 scaffold towards the PI3K-Akt pathway is defined by the IQ3 motif. Sci Rep. 2019;9:9126.
   PubMed Web of Science ®Google Scholar
• Kakuk A, Friedlander E, Vereb G Jr., et al. Nuclear and nucleolar localization signals and their targeting function in phosphatidylinositol 4-kinase PI4K230. Exp Cell Res. 2008;314:2376–2388.
   PubMed Web of Science ®Google Scholar
• Visnjic D, Crljen V, Curic J, et al. The activation of nuclear phosphoinositide 3-kinase C2beta in all-trans-retinoic acid-differentiated HL-60 cells. Febs Lett. 2002;529:268–274.
   PubMed Web of Science ®Google Scholar
• Oh SM, Liu Z, Okada M, et al. Ebp1 sumoylation, regulated by TLS/FUS E3 ligase, is required for its anti-proliferative activity. Oncogene. 2010;29:1017–1030.
   PubMed Web of Science ®Google Scholar
• Geeraerts A, Hsiu-Fang F, Zimmermann P, et al. The characterization of the nuclear dynamics of syntenin-2, a PIP2 binding PDZ protein. Cytometry A. 2013;83:866–875.
   PubMed Web of Science ®Google Scholar