Nuclear Phosphatidylinositol Signaling: Focus on Phosphatidylinositol Phosphate Kinases and Phospholipases C

Phosphatidylinositol (PI) metabolism represents the core of a network of signaling pathways which modulate many cellular functions including cell proliferation, cell differentiation, apoptosis, and membrane trafficking. An array of kinases, phosphatases, and lipases acts on PI creating an important number of second messengers involved in different cellular processes. Although, commonly, PI signaling was described to take place at the plasma membrane, many evidences indicated the existence of a PI cycle residing in the nuclear compartment of eukaryotic cells. The discovery of this mechanism shed new light on many nuclear functions, such as gene transcription, DNA modifications, and RNA expression. As these two PI cycles take place independently of one another, understanding how nuclear lipid signaling functions and modulates nuclear output is fundamental in the study of many cellular processes. J. Cell. Physiol. 231: 1645–1655, 2016. © 2015 Wiley Periodicals, Inc.

[1]  Z. Shah,et al.  PIP4K and the role of nuclear phosphoinositides in tumour suppression. , 2015, Biochimica et biophysica acta.

[2]  Z. Shah,et al.  The Basal Transcription Complex Component TAF3 Transduces Changes in Nuclear Phosphoinositides into Transcriptional Output , 2015, Molecular cell.

[3]  S. Jhanwar Genetic and epigenetic pathways in myelodysplastic syndromes: A brief overview. , 2015, Advances in biological regulation.

[4]  W. Blalock,et al.  PI‐PLCβ1b affects Akt activation, cyclin E expression, and caspase cleavage, promoting cell survival in pro‐B‐lymphoblastic cells exposed to oxidative stress , 2015, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[5]  W. Blalock,et al.  PLCβ1a and PLCβ1b Selective Regulation and Cyclin D3 Modulation Reduced by Kinamycin F During K562 Cell Differentiation , 2015, Journal of cellular physiology.

[6]  R. Irvine,et al.  Exploring phosphatidylinositol 5-phosphate 4-kinase function , 2015, Advances in biological regulation.

[7]  David R. Jones,et al.  A targeted knockdown screen of genes coding for phosphoinositide modulators identifies PIP4K2A as required for acute myeloid leukemia cell proliferation and survival , 2014, Oncogene.

[8]  Alessandro Poli,et al.  PLC and PI3K/Akt/mTOR signalling in disease and cancer. , 2015, Advances in biological regulation.

[9]  J. McCubrey,et al.  A novel DAG-dependent mechanism links PKCa and Cyclin B1 regulating cell cycle progression , 2014, Oncotarget.

[10]  L. Cocco,et al.  Protein kinase C involvement in cell cycle modulation. , 2014, Biochemical Society transactions.

[11]  O. Yersal,et al.  Biological subtypes of breast cancer: Prognostic and therapeutic implications. , 2014, World journal of clinical oncology.

[12]  J. McCubrey,et al.  PLC-beta 1 regulates the expression of miR-210 during mithramycin-mediated erythroid differentiation in K562 cells , 2014, Oncotarget.

[13]  A. Toker,et al.  Signaling specificity in the Akt pathway in biology and disease. , 2014, Advances in biological regulation.

[14]  Sharon Y. R. Dent,et al.  Chromatin modifiers and remodellers: regulators of cellular differentiation , 2013, Nature Reviews Genetics.

[15]  J. Chen,et al.  Alternative splicing in cancer: implications for biology and therapy , 2014, Oncogene.

[16]  Toshiaki Tanaka,et al.  DGKζ under stress conditions: “to be nuclear or cytoplasmic, that is the question”. , 2014, Advances in biological regulation.

[17]  J. McCubrey,et al.  Nuclear PI-PLCβ1: an appraisal on targets and pathology. , 2014, Advances in biological regulation.

[18]  Z. Shah,et al.  Nuclear phosphoinositides and their impact on nuclear functions , 2013, The FEBS journal.

[19]  K. Jirström,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. , 2013, Cancer research.

[20]  Thomas W. Mühleisen,et al.  Variation at 10p12.2 and 10p14 influences risk of childhood B-cell acute lymphoblastic leukemia and phenotype. , 2013, Blood.

[21]  John M. Asara,et al.  Depletion of a Putatively Druggable Class of Phosphatidylinositol Kinases Inhibits Growth of p53-Null Tumors , 2013, Cell.

[22]  A. Nakashima,et al.  Branched-Chain Amino Acids Enhance Premature Senescence through Mammalian Target of Rapamycin Complex I-Mediated Upregulation of p21 Protein , 2013, PloS one.

[23]  R. Irvine,et al.  Enzyme activity of the PIP4K2A gene product polymorphism that is implicated in schizophrenia , 2013, Psychopharmacology.

[24]  R. Devlin,et al.  Acute Physiological Stress Down-Regulates mRNA Expressions of Growth-Related Genes in Coho Salmon , 2013, PloS one.

[25]  T. Balla,et al.  Phosphoinositides: tiny lipids with giant impact on cell regulation. , 2013, Physiological reviews.

[26]  R. Irvine,et al.  Evolutionarily conserved structural changes in phosphatidylinositol 5-phosphate 4-kinase (PI5P4K) isoforms are responsible for differences in enzyme activity and localization , 2013, The Biochemical journal.

[27]  A. Chokkalingam,et al.  Novel childhood ALL susceptibility locus BMI1-PIP4K2A is specifically associated with the hyperdiploid subtype. , 2013, Blood.

[28]  R. Hasserjian Acute myeloid leukemia: advances in diagnosis and classification , 2013, International journal of laboratory hematology.

[29]  J. McCubrey,et al.  K562 cell proliferation is modulated by PLCβ1 through a PKCα-mediated pathway , 2013, Cell cycle.

[30]  N. Maraldi,et al.  Phosphoinositide-specific Phospholipase C β 1b (PI-PLCβ1b) Interactome: Affinity Purification-Mass Spectrometry Analysis of PI-PLCβ1b with Nuclear Protein* , 2013, Molecular & Cellular Proteomics.

[31]  E. Toska,et al.  Repression of transcription by WT1-BASP1 requires the myristoylation of BASP1 and the PIP2-dependent recruitment of histone deacetylase. , 2012, Cell reports.

[32]  S. Paolini,et al.  Activation of nuclear inositide signalling pathways during erythropoietin therapy in low-risk MDS patients , 2012, Leukemia.

[33]  P. Hawkins,et al.  PI3K signalling: the path to discovery and understanding , 2012, Nature Reviews Molecular Cell Biology.

[34]  Xu Gao,et al.  A microRNA “target pools” remains mysterious , 2012, Journal of cellular biochemistry.

[35]  M. Falasca,et al.  Phosphoinositides signalling in cancer: focus on PI3K and PLC. , 2012, Advances in biological regulation.

[36]  Kim Nasmyth,et al.  The cell cycle , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[37]  Ming-Ming Zhou,et al.  The PHD finger: a versatile epigenome reader. , 2011, Trends in biochemical sciences.

[38]  Frank B Gertler,et al.  The growth cone cytoskeleton in axon outgrowth and guidance. , 2011, Cold Spring Harbor perspectives in biology.

[39]  S. Paolini,et al.  Synergistic induction of PI-PLCβ1 signaling by azacitidine and valproic acid in high-risk myelodysplastic syndromes , 2011, Leukemia.

[40]  A. Lamond,et al.  Nuclear speckles. , 2011, Cold Spring Harbor perspectives in biology.

[41]  R. Reed,et al.  A role for TREX components in the release of spliced mRNA from nuclear speckle domains. , 2010, Nature communications.

[42]  Willem-Jan Keune,et al.  PIP4Kbeta interacts with and modulates nuclear localization of the high-activity PtdIns5P-4-kinase isoform PIP4Kalpha. , 2010, The Biochemical journal.

[43]  S. Minucci,et al.  Histone deacetylases and epigenetic therapies of hematological malignancies. , 2010, Pharmacological research.

[44]  O. Gavet,et al.  Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. , 2010, Developmental cell.

[45]  O. Gavet,et al.  Activation of cyclin B1–Cdk1 synchronizes events in the nucleus and the cytoplasm at mitosis , 2010, The Journal of cell biology.

[46]  A. Martelli,et al.  Nuclear inositide signaling in myelodysplastic syndromes , 2010, Journal of cellular biochemistry.

[47]  D. Reinberg,et al.  Chromatin structure and the inheritance of epigenetic information , 2010, Nature Reviews Genetics.

[48]  A. Newton,et al.  Protein kinase C: poised to signal. , 2010, American journal of physiology. Endocrinology and metabolism.

[49]  P. Zheng,et al.  CD24: from A to Z , 2010, Cellular and Molecular Immunology.

[50]  Iman van den Bout,et al.  PIP5K-driven PtdIns(4,5)P2 synthesis: regulation and cellular functions , 2009, Journal of Cell Science.

[51]  M. Carroll,et al.  A Phase I Study of the Mammalian Target of Rapamycin Inhibitor Sirolimus and MEC Chemotherapy in Relapsed and Refractory Acute Myelogenous Leukemia , 2009, Clinical Cancer Research.

[52]  M. Baccarani,et al.  Reduction of phosphoinositide-phospholipase C beta1 methylation predicts the responsiveness to azacitidine in high-risk MDS , 2009, Proceedings of the National Academy of Sciences.

[53]  R. Gambari,et al.  Expression of miR-210 during erythroid differentiation and induction of γ-globin gene expression. , 2009 .

[54]  C. Bloomfield,et al.  The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. , 2009, Blood.

[55]  R. Anderson,et al.  Two novel phosphatidylinositol-4-phosphate 5-kinase type Iγ splice variants expressed in human cells display distinctive cellular targeting , 2009, The Biochemical journal.

[56]  M. Mitchell,et al.  Nuclear PLCbeta1 is required for 3T3-L1 adipocyte differentiation and regulates expression of the cyclin D3-cdk4 complex. , 2009, Cellular signalling.

[57]  Nicholas J. Wang,et al.  Characterization of a naturally occurring breast cancer subset enriched in epithelial-to-mesenchymal transition and stem cell characteristics. , 2009, Cancer research.

[58]  S. Armstrong,et al.  Chromatin maps, histone modifications and leukemia , 2009, Leukemia.

[59]  L. Cocco,et al.  Involvement of nuclear PLCβl in lamin B1 phosphorylation and G2/M cell cycle progression , 2009, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[60]  Valeria Santini,et al.  Efficacy of azacitidine compared with that of conventional care regimens in the treatment of higher-risk myelodysplastic syndromes: a randomised, open-label, phase III study. , 2009, The Lancet. Oncology.

[61]  M. Baccarani,et al.  Phosphoinositide-phospholipase C beta1 mono-allelic deletion is associated with myelodysplastic syndromes evolution into acute myeloid leukemia. , 2009, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[62]  A. Martelli,et al.  Nuclear inositides: PI-PLC signaling in cell growth, differentiation and pathology. , 2009, Advances in enzyme regulation.

[63]  A. Martelli,et al.  Catalytic activity of nuclear PLC-beta(1) is required for its signalling function during C2C12 differentiation. , 2008, Cellular signalling.

[64]  Razelle Kurzrock,et al.  Phase I Study of Epigenetic Modulation with 5-Azacytidine and Valproic Acid in Patients with Advanced Cancers , 2008, Clinical Cancer Research.

[65]  P. Emson,et al.  Localization of phosphatidylinositol phosphate kinase IIγ in kidney to a membrane trafficking compartment within specialized cells of the nephron , 2008, American journal of physiology. Renal physiology.

[66]  T. Kataoka,et al.  Multiple roles of phosphoinositide-specific phospholipase C isozymes. , 2008, BMB reports.

[67]  M. Okada,et al.  Akt phosphorylation and nuclear phosphoinositide association mediate mRNA export and cell proliferation activities by ALY , 2008, Proceedings of the National Academy of Sciences.

[68]  K. O’Malley,et al.  Activated Nuclear Metabotropic Glutamate Receptor mGlu5 Couples to Nuclear Gq/11 Proteins to Generate Inositol 1,4,5-Trisphosphate-mediated Nuclear Ca2+ Release* , 2008, Journal of Biological Chemistry.

[69]  Michael L. Gonzales,et al.  A PtdIns4,5P2-regulated nuclear poly(A) polymerase controls expression of select mRNAs , 2008, Nature.

[70]  G. Meer,et al.  Membrane lipids: where they are and how they behave , 2008, Nature Reviews Molecular Cell Biology.

[71]  R. Schneiter,et al.  Lipid signalling in disease , 2008, Nature Reviews Molecular Cell Biology.

[72]  M. Baccarani,et al.  PI-PLCβ-1 and activated Akt levels are linked to azacitidine responsiveness in high-risk myelodysplastic syndromes , 2008, Leukemia.

[73]  M. Cazzola,et al.  Time-dependent prognostic scoring system for predicting survival and leukemic evolution in myelodysplastic syndromes. , 2007, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[74]  G. Drin,et al.  Stimulation of phospholipase Cbeta by membrane interactions, interdomain movement, and G protein binding--how many ways can you activate an enzyme? , 2007, Cellular signalling.

[75]  P. Fenaux,et al.  Evolving trends in the treatment of low‐risk myelodysplastic syndromes: immunomodulation and beyond—9th European Hematology Association Congress Geneva, Switzerland, 10–13 June 2004 , 2007, Transfusion medicine.

[76]  G. Martinelli,et al.  The Akt/mammalian target of rapamycin signal transduction pathway is activated in high-risk myelodysplastic syndromes and influences cell survival and proliferation. , 2007, Cancer research.

[77]  M. Falasca,et al.  Role of class II phosphoinositide 3-kinase in cell signalling. , 2007, Biochemical Society transactions.

[78]  Frederick R. Cross,et al.  Multiple levels of cyclin specificity in cell-cycle control , 2007, Nature Reviews Molecular Cell Biology.

[79]  R. Irvine,et al.  The intracellular localisation and mobility of Type Iγ phosphatidylinositol 4P 5-kinase splice variants , 2006, FEBS letters.

[80]  Pietro De Camilli,et al.  Phosphoinositides in cell regulation and membrane dynamics , 2006, Nature.

[81]  C. Finelli,et al.  Real-time PCR as a tool for quantitative analysis of PI-PLCbeta1 gene expression in myelodysplastic syndrome. , 2006, International journal of molecular medicine.

[82]  T. Balla,et al.  Phosphatidylinositol 4-kinases: old enzymes with emerging functions. , 2006, Trends in cell biology.

[83]  L. Cocco,et al.  Phosphoinositide-specific phospholipase C (PI-PLC) beta1 and nuclear lipid-dependent signaling. , 2006, Biochimica et biophysica acta.

[84]  F. Baluška,et al.  The Arabidopsis homolog of trithorax, ATX1, binds phosphatidylinositol 5-phosphate, and the two regulate a common set of target genes. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[85]  P. Piccaluga,et al.  Frequent elevation of Akt kinase phosphorylation in blood marrow and peripheral blood mononuclear cells from high-risk myelodysplastic syndrome patients , 2006, Leukemia.

[86]  S. Minucci,et al.  Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer , 2006, Nature Reviews Cancer.

[87]  P. Zimmermann,et al.  Nuclear speckles and nucleoli targeting by PIP2–PDZ domain interactions , 2005, The EMBO journal.

[88]  A. Martelli,et al.  Nuclear Phospholipase C β1 (PLCβ1) Affects CD24 Expression in Murine Erythroleukemia Cells* , 2005, Journal of Biological Chemistry.

[89]  R. Pazdur,et al.  Approval Summary: Azacitidine for Treatment of Myelodysplastic Syndrome Subtypes , 2005, Clinical Cancer Research.

[90]  Vesna Lukinoviƈ-Škudar,et al.  Nuclear phospholipase C-beta1b activation during G2/M and late G1 phase in nocodazole-synchronized HL-60 cells. , 2005 .

[91]  H. Lane,et al.  The mTOR Inhibitor RAD001 Sensitizes Tumor Cells to DNA-Damaged Induced Apoptosis through Inhibition of p21 Translation , 2005, Cell.

[92]  A. Martelli,et al.  Nuclear phospholipase C beta1 (PLCbeta1) affects CD24 expression in murine erythroleukemia cells. , 2005, The Journal of biological chemistry.

[93]  H. Lane,et al.  The mTOR Inhibitor RAD 001 Sensitizes Tumor Cells to DNA-Damaged Induced Apoptosis through Inhibition of p 21 Translation , 2005 .

[94]  A. Shearn,et al.  The Direct Interaction Between ASH2, a Drosophila Trithorax Group Protein, and SKTL, a Nuclear Phosphatidylinositol 4-Phosphate 5-Kinase, Implies a Role for Phosphatidylinositol 4,5-Bisphosphate in Maintaining Transcriptionally Active Chromatin , 2004, Genetics.

[95]  S. Luoh,et al.  Overexpression of the amplified Pip4k2β gene from 17q11–12 in breast cancer cells confers proliferation advantage , 2004, Oncogene.

[96]  Voichita D. Marinescu,et al.  Expression profiling and identification of novel genes involved in myogenic differentiation , 2004, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[97]  Peter J Parker,et al.  PKC at a glance , 2004, Journal of Cell Science.

[98]  A. Martelli,et al.  Nuclear protein kinase C isoforms: key players in multiple cell functions? , 2003, Histology and histopathology.

[99]  David L. Spector,et al.  Nuclear speckles: a model for nuclear organelles , 2003, Nature Reviews Molecular Cell Biology.

[100]  Junying Yuan,et al.  The PHD Finger of the Chromatin-Associated Protein ING2 Functions as a Nuclear Phosphoinositide Receptor , 2003, Cell.

[101]  A. Martelli,et al.  Up‐regulation of nuclear PLCβ1 in myogenic differentiation , 2003 .

[102]  K. Vermeulen,et al.  The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer , 2003, Cell proliferation.

[103]  R. Irvine Nuclear lipid signalling , 2003, Nature Reviews Molecular Cell Biology.

[104]  D. Steensma,et al.  The myelodysplastic syndrome(s): a perspective and review highlighting current controversies. , 2003, Leukemia research.

[105]  A. Martelli,et al.  Up-regulation of nuclear PLCbeta1 in myogenic differentiation. , 2003, Journal of cellular physiology.

[106]  A. Martelli,et al.  Nuclear PLCβ1 acts as a negative regulator of p45/NF-E2 expression levels in Friend erythroleukemia cells , 2002 .

[107]  C. Downes,et al.  Subcellular localization of phosphatidylinositol 4,5-bisphosphate using the pleckstrin homology domain of phospholipase C delta1. , 2002, The Biochemical journal.

[108]  Andrew J. Bannister,et al.  Type I PIPkinases Interact with and Are Regulated by the Retinoblastoma Susceptibility Gene Product—pRB , 2002, Current Biology.

[109]  P. Janmey,et al.  Phosphatidylinositol-dependent actin filament binding by the SWI/SNF-like BAF chromatin remodeling complex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[110]  J. Lord,et al.  Generation of diacylglycerol molecular species through the cell cycle: a role for 1-stearoyl, 2-arachidonyl glycerol in the activation of nuclear protein kinase C-betaII at G2/M. , 2002, Journal of cell science.

[111]  A. Martelli,et al.  Nuclear PLCbeta(1) acts as a negative regulator of p45/NF-E2 expression levels in Friend erythroleukemia cells. , 2002, Biochimica et biophysica acta.

[112]  H. Kantarjian,et al.  Acute myeloid leukemia , 2018, Methods in Molecular Biology.

[113]  J. Halstead,et al.  Inositol lipids are regulated during cell cycle progression in the nuclei of murine erythroleukaemia cells. , 2001, The Biochemical journal.

[114]  G. Schiavo,et al.  Nuclear PtdIns(4,5)P2 assembles in a mitotically regulated particle involved in pre-mRNA splicing. , 2001, Journal of cell science.

[115]  A. Newton,et al.  Protein kinase C: structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. , 2001, Chemical reviews.

[116]  A. Xu,et al.  Protein Kinase C α-mediated Negative Feedback Regulation Is Responsible for the Termination of Insulin-like Growth Factor I-induced Activation of Nuclear Phospholipase C β1 in Swiss 3T3 Cells* , 2001, The Journal of Biological Chemistry.

[117]  J. Harbour,et al.  The Rb/E2F pathway: expanding roles and emerging paradigms. , 2000, Genes & development.

[118]  M. Vitale,et al.  A Role for Nuclear Phospholipase Cβ1 in Cell Cycle Control* , 2000, The Journal of Biological Chemistry.

[119]  F. Gianfrancesco,et al.  Identification and chromosomal localisation by fluorescence in situ hybridisation of human gene of phosphoinositide-specific phospholipase C beta(1). , 2000, Biochimica et biophysica acta.

[120]  M. Vitale,et al.  A role for nuclear phospholipase Cbeta 1 in cell cycle control. , 2000, The Journal of biological chemistry.

[121]  A. Martelli,et al.  Insulin‐like growth factor‐I‐dependent stimulation of nuclear phospholipase C‐β1 activity in Swiss 3T3 cells requires an intact cytoskeleton and is paralleled by increased phosphorylation of the phospholipase , 1999, Journal of cellular biochemistry.

[122]  R. Anderson,et al.  Phosphoinositide signaling pathways in nuclei are associated with nuclear speckles containing pre-mRNA processing factors. , 1998, Molecular biology of the cell.

[123]  Keji Zhao,et al.  Rapid and Phosphoinositol-Dependent Binding of the SWI/SNF-like BAF Complex to Chromatin after T Lymphocyte Receptor Signaling , 1998, Cell.

[124]  S. Rhee,et al.  Nuclear but not cytoplasmic phospholipase C beta 1 inhibits differentiation of erythroleukemia cells. , 1998, Cancer research.

[125]  F. Hucho,et al.  Nuclear import of protein kinase C occurs by a mechanism distinct from the mechanism used by proteins with a classical nuclear localization signal. , 1998, Journal of cell science.

[126]  Roger L. Williams,et al.  Catalytic Domain of Phosphoinositide-specific Phospholipase C (PLC) , 1998, The Journal of Biological Chemistry.

[127]  S. Ryu,et al.  Localization of two forms of phospholipase C-beta1, a and b, in C6Bu-1 cells. , 1998, Biochimica et biophysica acta.

[128]  L. Cantley,et al.  A new pathway for synthesis of phosphatidylinositol-4,5-bisphosphate , 1997, Nature.

[129]  A. Fields,et al.  A Role for Nuclear Phosphatidylinositol-specific Phospholipase C in the G2/M Phase Transition* , 1997, The Journal of Biological Chemistry.

[130]  N. Divecha,et al.  Metabolism and possible compartmentalization of inositol lipids in isolated rat-liver nuclei. , 1997, The Biochemical journal.

[131]  H. Perlman,et al.  Cell cycle exit upon myogenic differentiation. , 1997, Current opinion in genetics & development.

[132]  T Hamblin,et al.  International scoring system for evaluating prognosis in myelodysplastic syndromes. , 1997, Blood.

[133]  J. Loijens,et al.  Type I Phosphatidylinositol-4-phosphate 5-Kinases Are Distinct Members of This Novel Lipid Kinase Family* , 1996, The Journal of Biological Chemistry.

[134]  Y. Yazaki,et al.  Cloning of cDNAs Encoding Two Isoforms of 68-kDa Type I Phosphatidylinositol4-phosphate 5-Kinase* , 1996, The Journal of Biological Chemistry.

[135]  S. Rhee,et al.  The Role of Carboxyl-terminal Basic Amino Acids in Gqα-dependent Activation, Particulate Association, and Nuclear Localization of Phospholipase C-β1* , 1996, The Journal of Biological Chemistry.

[136]  K. Walsh,et al.  Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis , 1996, The Journal of cell biology.

[137]  Gregory J. Parker,et al.  The phosphatidylinositol 4-phosphate 5-kinase family. , 1996, Advances in enzyme regulation.

[138]  M. Katan,et al.  Mutations within a highly conserved sequence present in the X region of phosphoinositide-specific phospholipase C-delta 1. , 1995, The Biochemical journal.

[139]  M. Vidal,et al.  The retinoblastoma protein binds to a family of E2F transcription factors , 1993, Molecular and cellular biology.

[140]  N. Divecha,et al.  Nuclear diacylglycerol is increased during cell proliferation in vivo. , 1993, The Biochemical journal.

[141]  A. Martelli,et al.  Nuclear localization and signalling activity of phosphoinositidase Cβ in Swiss 3T3 cells , 1992, Nature.

[142]  J. Boonstra,et al.  A differential location of phosphoinositide kinases, diacylglycerol kinase, and phospholipase C in the nuclear matrix. , 1992, The Journal of biological chemistry.

[143]  Michael J. Berridge,et al.  Inositol phosphates and cell signalling , 1989, Nature.

[144]  A. Martelli,et al.  Rapid changes in phospholipid metabolism in the nuclei of Swiss 3T3 cells induced by treatment of the cells with insulin-like growth factor I. , 1988, Biochemical and biophysical research communications.

[145]  L. Cocco,et al.  Synthesis of polyphosphoinositides in nuclei of Friend cells. Evidence for polyphosphoinositide metabolism inside the nucleus which changes with cell differentiation. , 1987, The Biochemical journal.

[146]  C. Smith,et al.  Characterization of a phosphatidylinositol 4-phosphate-specific phosphomonoesterase in rat liver nuclear envelopes. , 1984, Archives of biochemistry and biophysics.

[147]  L. Cioé,et al.  Differential expression of the globin genes in human leukemia K562(S) cells induced to differentiate by hemin or butyric acid. , 1981, Cancer research.