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Histochemistry and Cell Biology

, Volume 150, Issue 3, pp 245–253 | Cite as

Phospholipids and inositol phosphates linked to the epigenome

  • Lívia Uličná
  • Darina Paprčková
  • Veronika Fáberová
  • Pavel Hozák
Review

Abstract

Even though the majority of knowledge about phospholipids comes from their cytoplasmic functions, in the last decade, it has been shown that nuclear phospholipids and their building blocks, inositol phosphates, have many important roles in the cell nucleus. There are clear connections of phospholipids with the regulation of gene expression and chromatin biology, however, this review focuses on less known functions of nuclear phospholipids in connection with the epigenome regulation. In particular, we highlight the roles of nuclear phospholipids and inositol phosphates that involve histone modifications, such as acetylation or methylation, tightly connected with the cell physiology. This demonstrates the importance of nuclear phospholipids in the regulation of cellular processes, and should encourage further research of nuclear phospholipids and inositol phosphates.

Keywords

Phospholipids Phosphoinositide Inositol phosphate Acetylation Methylation 

Notes

Acknowledgements

This work was supported by the Grant Agency of the Czech Republic (Grant nos. 15-08738S; 16-03346S and 17-09103S); by the Czech Academy of Sciences (Grant no. JSPS-18-18) and the Institutional Research Concept of the Institute of Molecular Genetics (Grant no. RVO: 68378050). This work was supported by the project “BIOCEV—Biotechnology and Biomedicine Centre of the Academy of Sciences and Charles University” (CZ.1.05/1.1.00/02.0109), from the European Regional Development Fund. This work was supported by the Microscopy Centre; Light/Electron CF, IMG CAS supported by the MEYS CR (LM2015062 Czech-BioImaging). The work is supported from European Regional Development Fund-Project “Modernization and support of research activities of the national infrastructure for biological and medical imaging Czech-BioImaging” (no. CZ.02.1.01/0.0/0.0/16_013/0001775).

Compliance with ethical standards

Conflict of interest

The authors declare no competing or financial interests.

References

  1. Albi E, Lazzarini R, Viola Magni M (2008) Phosphatidylcholine/sphingomyelin metabolism crosstalk inside the nucleus. Biochem J 1410(2):381–389CrossRefGoogle Scholar
  2. Alcázar-Román A, Wente S (2008) Inositol polyphosphates: a new frontier for regulating gene expression. Chromosoma 117(1):1–13.  https://doi.org/10.1007/s00412-007-0126-4 CrossRefPubMedGoogle Scholar
  3. Alessenko A, Burlakova E (2002) Functional role of phospholipids in the nuclear events. Bioelectrochemistry 58(1):13–21.  https://doi.org/10.1016/S1567-5394(02)00135-4 CrossRefPubMedGoogle Scholar
  4. Alvarez-Venegas R, Sadder M, Hlavacka A, Baluska F, Xia Y, Lu G, Firsov A, Sarath G, Moriyama H, Dubrovsky JG, Avramova Z (2006) The Arabidopsis homolog of trithorax, ATX1, binds phosphatidylinositol 5-phosphate, and the two regulate a common set of target genes. Proc Natl Acad Sci USA 103(15):6049–6054.  https://doi.org/10.1073/pnas.0600944103 CrossRefPubMedGoogle Scholar
  5. Bernstein B, Meissner A, Lander E (2007) The mammalian epigenome. Cell 128(4):669–681.  https://doi.org/10.1016/j.cell.2007.01.033 CrossRefPubMedGoogle Scholar
  6. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16(1):6–21.  https://doi.org/10.1101/gad.947102 CrossRefPubMedGoogle Scholar
  7. Boronenkov IV, Loijens JC, Umeda M, Anderson RA (1998) Phosphoinositide signaling pathways in nuclei are associated with nuclear speckles containing pre-mRNA processing factors. Mol Biol Cell 9(12):3547–3560CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bremer J, Greenberg D (1961) Methyl transferring enzyme system of microsomes in the biosynthesis of lecithin (phosphatidylcholine). Biochim Biophys Acta 46(2):205–216.  https://doi.org/10.1016/0006-3002(61)90745-4 CrossRefGoogle Scholar
  9. Brosnan J, Brosnan M (2006). The sulfur-containing amino acids: an overview. J Nutr 136(6 Suppl):1636S–1640S.  https://doi.org/10.1093/jn/136.6.1636S CrossRefPubMedGoogle Scholar
  10. Burton A, Azevedo C, Andreassi C, Riccio A, Saiardi A (2013) Inositol pyrophosphates regulate JMJD2C-dependent histone demethylation. Proc Natl Acad Sci USA 110(47):18970–18975CrossRefPubMedGoogle Scholar
  11. Chakraborty A, Kim S, Snyder S (2011) Inositol pyrophosphates as mammalian cell signals. Sci Signal 4(188):re1.  https://doi.org/10.1126/scisignal.2001958 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Clarke J, Letcher A, D’santos C, Halstead J, Irvine R, Divecha N (2001) Inositol lipids are regulated during cell cycle progression in the nuclei of murine erythroleukaemia cells. Biochem J 357:905–910.  https://doi.org/10.1042/0264-6021:3570905 CrossRefPubMedPubMedCentralGoogle Scholar
  13. D’Santos C, Clarke J, Divecha N (1998) Phospholipid signalling in the nucleus: Een DAG uit het leven van de inositide signalering in de nucleus. Biochim Biophys Acta 1436(1–2):201–232CrossRefPubMedGoogle Scholar
  14. Draskovic P, Saiardi A, Bhandari R, Burton A, Ilc G, Kovacevic M, Snyder S, Podobnik M (2008) Inositol hexakisphosphate kinase products contain diphosphate and triphosphate groups. Chem Biol 15(3):274–286.  https://doi.org/10.1016/j.chembiol.2008.01.011 CrossRefPubMedGoogle Scholar
  15. Essafi A, Webb A, Berry R, Sligh J, Burn S, Spraggon L, Velecela V, Martinez-Estrada O, Wiltshire J, Roberts S, Brownstein D, Davies J, Hastie N, Hohenstein P (2011) A wt1-controlled chromatin switching mechanism underpins tissue-specific wnt4 activation and repression. Dev Cell 21(3):559–574.  https://doi.org/10.1016/j.devcel.2011.07.014 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gelato KA, Tauber M, Ong MS, Winter S, Hiragami-Hamada K, Sindlinger J, Lemak A, Bultsma Y, Houliston S, Schwarzer D, Divecha N, Arrowsmith CH, Fischle W (2014) Accessibility of different histone H3-binding domains of UHRF1 is allosterically regulated by phosphatidylinositol 5-phosphate. Mol Cell 54(6):905–919.  https://doi.org/10.1016/j.molcel.2014.04.004 CrossRefPubMedGoogle Scholar
  17. Gozani O, Karuman P, Jones DR, Ivanov D, Cha J, Lugovskoy AA, Baird CL, Zhu H, Field SJ, Lessnick SL, Villasenor J, Mehrotra B, Chen J, Rao VR, Brugge JS, Ferguson CG, Payrastre B, Myszka DG, Cantley LC, Wagner G, Divecha N, Prestwich GD, Yuan J (2003) The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell 114(1):99–111CrossRefPubMedGoogle Scholar
  18. Hait N, Allegood J, Maceyka M, Strub G, Harikumar K, Singh S, Luo C, MArmorstein R, Kordula T, Milstien S, Spiegel S (2009) Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science 325(5945):1254–1257.  https://doi.org/10.1126/science.1176709 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hamann B, Blind R (2018) Nuclear phosphoinositide regulation of chromatin. J Cell Physiol 233(1):107–123.  https://doi.org/10.1002/jcp.25886 CrossRefPubMedGoogle Scholar
  20. Hickman M, Petti A, Ho-Shing O, Silverman S, McIsaac R, Lee T, Botstein D (2011) Coordinated regulation of sulfur and phospholipid metabolism reflects the importance of methylation in the growth of yeast. Mol Biol Cell 22(21):4192–4204.  https://doi.org/10.1091/mbc.E11-05-0467 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Irvine R, Divecha N (1992) Phospholipids in the nucleus-metabolism and possible functions. Semin Cell Biol 3(4):225–235CrossRefPubMedGoogle Scholar
  22. Jacob R, Stead L, Devlin C, Tabas I, Brosnan M, Brosnan J, Vance D (2005) Physiological regulation of phospholipid methylation alters plasma homocysteine in mice. J Biol Chem 280(31):28299–28305.  https://doi.org/10.1074/jbc.M501971200 CrossRefGoogle Scholar
  23. Jones DR, Bultsma Y, Keune WJ, Halstead JR, Elouarrat D, Mohammed S, Heck AJ, D’Santos CS, Divecha N (2006) Nuclear PtdIns5P as a transducer of stress signaling: an in vivo role for PIP4Kbeta. Mol Cell 23(5):685–695.  https://doi.org/10.1016/j.molcel.2006.07.014 CrossRefPubMedGoogle Scholar
  24. Jungmichel S, Sylvestersen KB, Choudhary C, Nguyen S, Mann M, Nielsen ML (2014) Specificity and commonality of the phosphoinositide-binding proteome analyzed by quantitative mass spectrometry. Cell Rep 6(3):578–591.  https://doi.org/10.1016/j.celrep.2013.12.038 CrossRefPubMedGoogle Scholar
  25. Kashihara M, Miyata S, Kumanogoh H, Funatsu N, Matsunaga W, Kiyohara T, Sokawa Y, Maekawa S (2000) Changes in the localization of NAP-22, a calmodulin binding membrane protein, during the development of neuronal polarity. Neurosci Res 37(4):315–325CrossRefPubMedGoogle Scholar
  26. Kutateladze T (2012) Histone deacetylation: IP4 is a epigenetic coregulator. Nat Chem Biol 8(3):230–231.  https://doi.org/10.1038/nchembio.795 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lemmon M (2007) Pleckstrin homology (PH) domains and phosphoinositides. Biochem Soc Symp 74:81–93.  https://doi.org/10.1042/BSS0740081 CrossRefGoogle Scholar
  28. Lewis AE, Sommer L, Arntzen M, Strahm Y, Morrice NA, Divecha N, D’Santos CS (2011). Identification of nuclear phosphatidylinositol 4,5-bisphosphate-interacting proteins by neomycin extraction. Mol Cell Proteomics.  https://doi.org/10.1074/mcp.M110.003376 PubMedCrossRefGoogle Scholar
  29. Lin H, Fridy P, Ribeiro A, Choi J, Barma D, Vogel G, Falck J, Shears S, York JD, Mayr G (2009) Structural analysis and detection of biological inositol pyrophosphates reveal that the family of VIP/diphosphoinositol pentakisphosphate kinases are 1/3-kinases. J Biol Chem 284(3):1863–1872.  https://doi.org/10.1074/jbc.M805686200 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Maceyka M, Sankala H, Hait N, Le Stunff H, Liu H, Toman R, Collier C, Zhang M, Satin L, Merrill AJ, Milstien S, Spiegel S (2005) SphK1 and SphK2, sphingosine kinase isoenzymes with opposing functions in sphingolipid metabolism. J Biol Chem 280(44):37118–37129.  https://doi.org/10.1074/jbc.M502207200 CrossRefPubMedGoogle Scholar
  31. Maceyka M, Harikumar K, Milstien S, Spiegel S (2012) Sphingosine-1-phosphate signaling and its role in disease. Trends Cell Biol 22(1):50–56é.  https://doi.org/10.1016/j.tcb.2011.09.003 CrossRefPubMedGoogle Scholar
  32. Maekawa S, Murofushi H, Nakamura S (1994) Inhibitory effect of calmodulin on phosphorylation of NAP-22 with protein kinase C. J Biol Chem 269(30):19462–19465PubMedGoogle Scholar
  33. Maraldi N, Santi S, Zini N, Ognibene A, Rizzoli R, Mazzotti G, Di Primio R, Bareggi R, Bertagnolo V, Pagliarini C (1993) Decrease in nuclear phospholipids associated with DNA replication. J Cell Sci 104(3):853–859PubMedGoogle Scholar
  34. Maraldi N., Zini N., Santi S. and Manzoli F. (1999). Topology of inositol lipid signal transduction in the nucleus. J Cell Physiol 181(2):203–217. https://doi.org/10.1002/(SICI)1097-4652(199911)181:2<203::AID-JCP3>3.0.CO;2-OCrossRefPubMedGoogle Scholar
  35. Margueron R, Trojer P, Reinberg D (2005) The key to development: interpreting the histone code? Curr Opin Genet Dev 15(2):163–176.  https://doi.org/10.1016/j.gde.2005.01.005 CrossRefPubMedGoogle Scholar
  36. Mazzotti G, Zini N, Rizzi E, Rizzoli R, Galanzi A, Ognibene A, Santi S, Matteucci A, Martelli AM, Maraldi NM (1995) Immunocytochemical detection of phosphatidylinositol 4,5-bisphosphate localization sites within the nucleus. J Histochem Cytochem 43(2):181–191CrossRefPubMedGoogle Scholar
  37. Mellman DL, Gonzales ML, Song CH, Barlow CA, Wang P, Kendziorski C, Anderson RA (2008) A PtdIns4,5P(2)-regulated nuclear poly(A) polymerase controls expression of select mRNAs. Nature 451(7181):U1013–U1019.  https://doi.org/10.1038/nature06666 CrossRefGoogle Scholar
  38. Millard C, Watson P, Celardo I, Gordiyenko Y, Cowley S, Robinson C, Fairall L, Schwabe J (2013) Class I HDACs share a common mechanism of regulation by inositol phosphates. Mol Cell 51(1):57–67.  https://doi.org/10.1016/j.molcel.2013.05.020 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Monserrate J, York J (2010) Inositol phospahte synthesis and the nuclear processes they affect. Curr Opin Cell Biol 22(3):365–373.  https://doi.org/10.1016/j.ceb.2010.03.006 CrossRefPubMedGoogle Scholar
  40. Mortier E, Wuytens G, Leenaerts I, Hannes F, Heung MY, Degeest G, David G, Zimmermann P (2005) Nuclear speckles and nucleoli targeting by PIP2–PDZ domain interactions. EMBO J 24(14):2556–2565CrossRefPubMedPubMedCentralGoogle Scholar
  41. Mosevitsky M, Capony J, Skladchikova G, Novitskaya V, Plekhanov A, Zakharov V (1997) The BASP1 family of myristoylated proteins abundant in axonal termini. Primary structure analysis and physico-chemical properties. Biochimie 79(6):373–384CrossRefPubMedGoogle Scholar
  42. Ndamukong I, Jones D, Lapko H, Divecha N, Avramova Z (2010) Phosphatidylinositol 5-phosphate links dehydration stress to the activity of Arabidopsis trithorax-like factor ATX1. PLoS One 5(10):e13396.  https://doi.org/10.1371/journal.pone.0013396 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Osborne SL, Thomas CL, Gschmeissner S, Schiavo G (2001) Nuclear PtdIns(4,5)P2 assembles in a mitotically regulated particle involved in pre-mRNA splicing. J Cell Sci 114(Pt 13):2501–2511PubMedGoogle Scholar
  44. Peitzsch R, McLaughlin S (1993) Binding of acylated peptides and fatty acids to phospholipid vesicles: pertinence to myristoylated proteins. Biochemistry 32(39):10436–10443CrossRefPubMedGoogle Scholar
  45. Rando O, Zhao K, Janmey P, Crabtree G (2002) Phosphatidylinositol-dependent actin filament binding by the SWI/SNF-like BAF chromatin remodeling complex. Proc Natl Acad Sci USA 99:2824–2829.  https://doi.org/10.1073/pnas.032662899 CrossRefPubMedGoogle Scholar
  46. Sadhu M, Moresco J, Zimmer A, Yates Jr, Rine J (2014) Multiple inputs control sulfur-containing amino acid synthesis in Saccharomyces cerevisiae. Mol Biol Cell 25(10):1653–1665.  https://doi.org/10.1091/mbc.E13-12-0755 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Sairadi A, Nagata E, Hongbo R, Sawa A, Luo X, Snowman A, Snyder S (2001) Mammalian inositol polyphosphate multikinase synthesizes inositol 1,4,5-trisphosphate and an inositol pyrophosphate. Proc Natl Acad Sci USA 98(5):2306–2311.  https://doi.org/10.1073/pnas.041614598 CrossRefGoogle Scholar
  48. Sato M, Ueda Y, Shibuya M, Umezawa Y (2005) Locating inositol 1,4,5-trisphosphate in the nucleus and neuronal dendrites with genetically encoded fluorescent indicators. Anal Chem 77(15):4751–4758CrossRefPubMedGoogle Scholar
  49. Seto E, Yoshida M (2014) Erasers of histone acetylation: the histone deacetylase enzymes. Cold Spring Harb Perspect Biol 6(4):a018713.  https://doi.org/10.1101/cshperspect.a018713 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Shears S (2015) Inositol pyrophosphates: why so many phosphates? Adv Biol Regul 57:203–216.  https://doi.org/10.1016/j.jbior.2014.09.015 CrossRefPubMedGoogle Scholar
  51. Sobol M, Yildirim S, Philimonenko VV, Marášek P, Castaño E, Hozák P (2013) UBF complexes with phosphatidylinositol 4,5-bisphosphate in nucleolar organizer regions regardless of ongoing RNA polymerase I activity. Nucleus 4(6):478–486.  https://doi.org/10.4161/nucl.27154 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Sobol M, Krausová A, Yildirim S, Kalasová I, Fáberová V, Vrkoslav V, Philimonenko V, Marášek P, Pastorek L, Čapek M, Lubovská Z, Uličná L, Tsuji T, Hozak P (2018) Nuclear phosphatidylinositol 4,5-bisphosphate islets contribute to efficient RNA polymerase II-dependent transcription. J Cell Sci.  https://doi.org/10.1242/jcs.211094 PubMedCrossRefGoogle Scholar
  53. Stefan C, Trimble W, Grinstein S, Drin G, Reinisch K, De Camilli P, Cohen S, Valm A, Lippincott-Schwartz J, Levine T, Iaea D, Maxfield F, Futter C, Eden E, Judith D, van Vliet A, Agostinis P, Tooze S, Sugiura A, McBride H (2017). Membrane dynamics and organelle biogenesis-lipid pipelines and vesicular carriers. BMC Biol.  https://doi.org/10.1186/s12915-017-0432-0 PubMedPubMedCentralCrossRefGoogle Scholar
  54. Stipanuk M (2004) Sulfur amino acid metabolism: pathways for production and removal of homocysteine and cysteine. Annu Rev Nutr 24:539–577CrossRefPubMedGoogle Scholar
  55. Strub G, Maceyka M, Hait N, Milstien S, Spiegel S (2010) Extracellular and intracellular actions of sphingosine-1-phosphate. Adv Exp Med Biol 688:141–155CrossRefPubMedPubMedCentralGoogle Scholar
  56. Sutter B, Wu X, Laxman S, Tu B (2013) Methionine inhibits autophagy and promotes growth by inducing the SAM-responsive methylation of PP2A. Cell 154(2):403–415.  https://doi.org/10.1016/j.cell.2013.06.041 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Takasaki A, Hayashi N, Matsubara M, Yamauchi E, Taniguchi H (1999) Identification of the calmodulin-binding domain of neuron-specific protein kinase C substrate protein CAP-22/NAP-22. Direct involvement of protein myristoylation in calmodulin-target protein interaction. J Biol Chem 274(17):11848–11853CrossRefPubMedGoogle Scholar
  58. Toska E, Campbell HA, Shandilya J, Goodfellow SJ, Shore P, Medler KF, Roberts SG (2012) Repression of transcription by WT1-BASP1 requires the myristoylation of BASP1 and the PIP2-dependent recruitment of histone deacetylase. Cell Rep 2(3):462–469.  https://doi.org/10.1016/j.celrep.2012.08.005 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Tran D, Gascard P, Berthon B, Fukami K, Takenawa T, Giraud F, Claret M (1993) Cellular distribution of polyphosphoinositides in rat hepatocytes. Cell Signal 5:565–581.  https://doi.org/10.1016/0898-6568(93)90052-N CrossRefPubMedGoogle Scholar
  60. Ulicna L, Kalendova A, Kalasova I, Vacik T, Hozák P (2018) PIP2 epigenetically represses rRNA genes transcription interacting with PHF8. Biochim Biophys Acta 1863(3):266–275.  https://doi.org/10.1016/j.bbalip.2017.12.008 CrossRefPubMedGoogle Scholar
  61. Ungewickell A, Hugge C, Kisseleva M, Chang S, Zou J, Feng Y, Galyov E, Wilson M, Majerus P (2005) The identification and characterization of two phosphatidylinositol-4,5-bisphosphate 4-phosphatases. Proc Natl Acad Sci USA 102:18854–18859.  https://doi.org/10.1073/pnas.0509740102 CrossRefPubMedGoogle Scholar
  62. Vance D (2014) Phospholipid methylation in mammals: from biochemistry to physiological function. Biochim Biophys Acta 1838(6):1477–1487.  https://doi.org/10.1016/j.bbamem.2013.10.018 CrossRefPubMedGoogle Scholar
  63. Vance J, Tasseva G (2013) Formation and function of phosphatidylserine and phosphatidylethanolamine in mammalian cells. Biochim Biophys Acta 1831(3):543–554.  https://doi.org/10.1016/j.bbalip.2012.08.016 CrossRefPubMedGoogle Scholar
  64. Vann L, Wooding F, Irvine R, Divecha N (1997) Metabolism and possible compartmentalization of inositol lipids in isolated rat-liver nuclei. Biochem J 327(2):569–576.  https://doi.org/10.1042/bj3270569 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Viiri K, Maki M, Lohi O (2012). Phosphoinositides as regulators of protein–chromatin interactions. Sci Signal.  https://doi.org/10.1126/scisignal.2002917 PubMedCrossRefGoogle Scholar
  66. Watson P, Fairall L, Santos G, Schwabe J (2012) Structure of HDAC3 bound to co-repressor and inositol tetraphosphate. Nature 481(7381):335–340CrossRefPubMedPubMedCentralGoogle Scholar
  67. Watson P, Millard C, Riley A, Robertson N, Wright L, Godage H, Cowley S, Jamieson A, Potter B, Schwabe J (2016). Insights into the activation mechanism of class I HDAC complexes by inositol phosphates. Nat Commun.  https://doi.org/10.1038/ncomms11262 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Watt SA, Kular G, Fleming IN, Downes CP, Lucocq JM (2002) Subcellular localization of phosphatidylinositol 4,5-bisphosphate using the pleckstrin homology domain of phospholipase C delta1. Biochem J 363(Pt 3):657–666CrossRefPubMedPubMedCentralGoogle Scholar
  69. Wilson M, Livermore T, Saiardi A (2013) Inositol pyrophosphates: between signalling and metabolism. Biochem J 452(3):369–379.  https://doi.org/10.1042/BJ20130118 CrossRefPubMedGoogle Scholar
  70. Ye C, Sutter B, Wang Y, Kuang Z, Tu B (2017) A metabolic function for phospholipid and histone methylation. Mol Cell 66(2):180–193.  https://doi.org/10.1016/j.molcel.2017.02.026 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Yildirim S, Castano E, Sobol M, Philimonenko VV, Dzijak R, Venit T, Hozák P (2013) Involvement of PIP2 in RNA polymerase I transcription. J Cell Sci 126(Pt 12):2730–2739.  https://doi.org/10.1242/jcs.123661 CrossRefPubMedGoogle Scholar
  72. York J, Majerus P (1994) Nuclear phosphatidylinositols decrease during S-phase of the cell cycle in HeLa cells. J Biol Chem 269(11):7847–7850PubMedGoogle Scholar
  73. Yu HY, Fukami K, Watanabe Y, Ozaki C, Takenawa T (1998) Phosphatidylinositol 4,5-bisphosphate reverses the inhibition of RNA transcription caused by histone H1. Eur J Biochem 251(1–2):281–287.  https://doi.org/10.1046/j.1432-1327.1998.2510281.x CrossRefPubMedGoogle Scholar
  74. Zhao K, Wang W, Rando O, Xue Y, Swiderek K, Kuo A, Crabtree G (1998) Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 95(5):625–636CrossRefPubMedGoogle Scholar
  75. Zolov SN, Bridges D, Zhang Y, Lee WW, Riehle E, Verma R, Lenk GM, Converso-Baran K, Weide T, Albin RL, Saltiel AR, Meisler MH, Russell MW, Weisman LS (2012) In vivo, Pikfyve generates PI(3,5)P2, which serves as both a signaling lipid and the major precursor for PI5P. Proc Natl Acad Sci USA 109(43):17472–17477.  https://doi.org/10.1073/pnas.1203106109 CrossRefPubMedGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biology of the Cell NucleusInstitute of Molecular Genetics of the Czech Academy of SciencesPragueCzech Republic
  2. 2.Department of Epigenetics of the Cell NucleusInstitute of Molecular Genetics of the Czech Academy of SciencesVestecCzech Republic
  3. 3.Microscopy CentreInstitute of Molecular Genetics of the Czech Academy of SciencesPragueCzech Republic

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