Phospholipids and inositol phosphates linked to the epigenome
- 80 Downloads
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.
KeywordsPhospholipids Phosphoinositide Inositol phosphate Acetylation Methylation
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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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 PubMedGoogle Scholar
- 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 PubMedPubMedCentralGoogle Scholar
- 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
- 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
- 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
- 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
- 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