Multiple Aspects of PIP2 Involvement in C. elegans Gametogenesis

. 2018 Sep 10 ; 19 (9) : . [epub] 20180910

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid30201859

Grantová podpora
16-03346S Grantová Agentura České Republiky
17-09103S Grantová Agentura České Republiky
LTC17054 INTER COST
No. CZ.02.1.01/0.0/0.0/16_013/0001775 European Regional Development Fund
P40 OD010440 NIH HHS - United States
RVO: 68378050 The Long-term conceptual development of the scientific organization
LM2015062 MEYS CR
CZ.1.05/1.1.00/02.0109 European Regional Development Fund

One of the most studied phosphoinositides is phosphatidylinositol 4,5-bisphosphate (PIP2), which localizes to the plasma membrane, nuclear speckles, small foci in the nucleoplasm, and to the nucleolus in mammalian cells. Here, we show that PIP2 also localizes to the nucleus in prophase I, during the gametogenesis of C. elegans hermaphrodite. The depletion of PIP2 by type I PIP kinase (PPK-1) kinase RNA interference results in an altered chromosome structure and leads to various defects during meiotic progression. We observed a decreased brood size and aneuploidy in progeny, defects in synapsis, and crossover formation. The altered chromosome structure is reflected in the increased transcription activity of a tightly regulated process in prophase I. To elucidate the involvement of PIP2 in the processes during the C. elegans development, we identified the PIP2-binding partners, leucine-rich repeat (LRR-1) protein and proteasome subunit beta 4 (PBS-4), pointing to its involvement in the ubiquitin⁻proteasome pathway.

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MacQueen A.V., Villeneuve A.M. Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev. 2001;15:1674–1687. doi: 10.1101/gad.902601. PubMed DOI PMC

Nicklas B.R. Chromosome segregation mechanisms. Genetics. 1974;78:205–213. PubMed PMC

Ostergren G. The mechanism of co-orientation in bivalents and multivalents. Hereditas. 1951;37:85–156. doi: 10.1111/j.1601-5223.1951.tb02891.x. DOI

Bell O., Tiwari V.K., Thoma N.H., Schubeler D. Determinants and dynamics of genome accessibility. Nat. Rev. Genet. 2011;12:554–564. doi: 10.1038/nrg3017. PubMed DOI

Wang X., Zhao Y., Wong K., Ehlers P., Kohara Y., Jones S.J., Marra M.A., Holt R.A., Moerman D.G., Hansen D. Identification of genes expressed in the hermaphrodite germ line of C. elegans using SAGE. BMC Genom. 2009;10:213. doi: 10.1186/1471-2164-10-213. PubMed DOI PMC

Capitani S., Mazzotti G., Jovine R., Papa S., Maraldi N.M., Manzoli F.A. Effect of phosphatidylcholine vesicles on the activity of DNA polymerase-alpha. Mol. Cell. Biochem. 1979;27:135–138. doi: 10.1007/BF00215361. PubMed DOI

Capitani S., Caramelli E., Felaco M., Miscia S., Manzoli F.A. Effect of phospholipid vesicles on endogenous RNA polymerase activity of isolated rat liver nuclei. Physiol. Chem. Phys. 1981;13:153–158. PubMed

Manzoli F.A., Capitani S., Mazzotti G., Barnabei O., Maraldi N.M. Role of chromatin phospholipids on template availability and ultrastructure of isolated nuclei. Adv. Enzym. Regul. 1982;20:247–262. doi: 10.1016/0065-2571(82)90019-X. PubMed DOI

Maraldi N.M., Capitani S., Caramelli E., Cocco L., Barnabei O., Manzoli F.A. Conformational changes of nuclear chromatin related to phospholipid induced modifications of the template availability. Adv. Enzym. Regul. 1984;22:447–464. doi: 10.1016/0065-2571(84)90025-6. PubMed DOI

Cocco L., Gilmour R.S., Maraldi N.M., Martelli A.M., Papa S., Manzoli F.A. Increase of globin RNA synthesis induced by phosphatidylserine liposomes in isolated erythroleukemic cell nuclei. Morphological and functional features. Biol. Cell. 1985;54:49–56. doi: 10.1111/j.1768-322X.1985.tb00379.x. PubMed DOI

Capitani S., Cocco L., Maraldi N.M., Papa S., Manzoli F.A. Effect of phospholipids on transcription and ribonucleoprotein processing in isolated nuclei. Adv. Enzym. Regul. 1986;25:425–438. doi: 10.1016/0065-2571(86)90027-0. PubMed DOI

Kuvichkin V.V. DNA-lipid interactions in vitro and in vivo. Bioelectrochemistry. 2002;58:3–12. doi: 10.1016/S1567-5394(02)00123-8. PubMed DOI

Mazzotti G., Zini N., Rizzi E., Rizzoli R., Galanzi A., Ognibene A., Santi S., Matteucci A., Martelli A.M., Maraldi N.M. Immunocytochemical detection of phosphatidylinositol 4,5-bisphosphate localization sites within the nucleus. J. Histochem. Cytochem. 1995;43:181–191. doi: 10.1177/43.2.7822774. PubMed DOI

Boronenkov I.V., Loijens J.C., Umeda M., Anderson R.A. Phosphoinositide signaling pathways in nuclei are associated with nuclear speckles containing pre-mRNA processing factors. Mol. Biol. Cell. 1998;9:3547–3560. doi: 10.1091/mbc.9.12.3547. PubMed DOI PMC

Osborne S.L., Thomas C.L., Gschmeissner S., Schiavo G. Nuclear PtdIns(4,5)P2 assembles in a mitotically regulated particle involved in pre-mRNA splicing. J. Cell Sci. 2001;114:2501–2511. PubMed

Yildirim S., Castano E., Sobol M., Philimonenko V.V., Dzijak R., Venit T., Hozák P. Involvement of phosphatidylinositol 4,5-bisphosphate in RNA polymerase I transcription. J. Cell Sci. 2013;126:2730–2739. doi: 10.1242/jcs.123661. PubMed DOI

Ulicna L., Kalendova A., Kalasova I., Vacik T., Hozák P. PIP2 epigenetically represses rRNA genes transcription interacting with PHF8. Biochim. Biophys. Acta. 2018;1863:266–275. doi: 10.1016/j.bbalip.2017.12.008. PubMed DOI

Sobol M., Krausová A., Yildirim S., Kalasová I., Fáberová V., Vrkoslav V., Philimonenko V., Marášek P., Pastorek L., Čapek M., et al. Nuclear phosphatidylinositol 4,5-bisphosphate islets contribute to efficient RNA polymerase II-dependent transcription. J. Cell Sci. 2018 doi: 10.1242/jcs.211094. PubMed DOI

Yu H.Y., Fukami K., Watanabe Y., Ozaki C., Takenawa T. Phosphatidylinositol 4,5-bisphosphate reverses the inhibition of RNA transcription caused by histone H1. Eur. J. Biochem. 1998;251:281–287. doi: 10.1046/j.1432-1327.1998.2510281.x. PubMed DOI

Toska E., Campbell H.A., Shandilya J., Goodfellow S.J., Shore P., Medler K.F., Roberts S.G.E. 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. doi: 10.1016/j.celrep.2012.08.005. PubMed DOI PMC

Loijens J.C., Anderson R.A. Type I phosphatidylinositol-4-phosphate 5-kinases are distinct members of this novel lipid kinase family. J. Biol. Chem. 1996;271:32937–32943. doi: 10.1074/jbc.271.51.32937. PubMed DOI

Ogg S.R., Ruvkun G. The C. elegans PTEN homolog, DAF-18, acts in the insulin receptor-like metabolic signaling pathway. Mol. Cell. 1998;2:887–893. doi: 10.1016/S1097-2765(00)80303-2. PubMed DOI

Blondeau F., Laporte J., Bodin S., Superti-Furga G., Payrastre B., Mandel J.L. Myotubularin, a phosphatase deficient in myotubular myopathy, acts on phosphatidylinositol 3-kinase and phosphatidylinositol 3-phosphate pathway. Hum. Mol. Genet. 2000;22:2223–2229. doi: 10.1093/oxfordjournals.hmg.a018913. PubMed DOI

Klopfenstein D.R., Tomishige M., Stuurman N., Vale R.D. Role of phosphatidylinositol (4,5)bisphosphate organization in membrane transport by the Unc104 kinesin motor. Cell. 2002;109:347–358. doi: 10.1016/S0092-8674(02)00708-0. PubMed DOI PMC

Nicot A.S., Fares H., Payrastre B., Chisholm A.D., Labouesse M., Laporte J. The phosphoinositide kinase PIKfyve/Fab1p regulates terminal lysosome maturation in Caenorhabditis elegans. Mol. Biol. Cell. 2006;17:3062–3074. doi: 10.1091/mbc.e05-12-1120. PubMed DOI PMC

Bae Y.K., Kim E., L’hernault S.W., Barr M.M. The CIL-1 PI 5-phosphatase localizes TRP Polycystins to cilia and activates sperm in C. elegans. Curr. Biol. 2009;19:1599–1607. doi: 10.1016/j.cub.2009.08.045. PubMed DOI PMC

Padmanabhan S., Mukhopadhyay A., Narasimhan S.D., Tesz G., Czech M.P., Tissenbaum H.A. A PP2A regulatory subunit regulates C. elegans insulin/IGF-1 signaling by modulating AKT-1 phosphorylation. Cell. 2009;136:939–951. doi: 10.1016/j.cell.2009.01.025. PubMed DOI PMC

Liu Z., Klaavuniemi T., Ono S. Distinct roles of four gelsolin-like domains of Caenorhabditis elegans gelsolin-like protein-1 in actin filament severing, barbed end capping, and phosphoinositide binding. Biochemistry. 2010;49:4349–4360. doi: 10.1021/bi100215b. PubMed DOI PMC

Lu N., Shen Q., Mahoney T.R., Neukomm L.J., Wang Y., Zhou Z. Two PI 3-kinases and one PI 3-phosphatase together establish the cyclic waves of phagosomal PtdIns(3)P critical for the degradation of apoptotic cells. PLoS Biol. 2012;10:e1001245. doi: 10.1371/journal.pbio.1001245. PubMed DOI PMC

Cheng S., Wang K., Zou W., Miao R., Huang Y., Wang H., Wang X. PtdIns(4,5)P2 and PtdIns3P coordinate to regulate phagosomal sealing for apoptotic cell clearance. J. Cell Biol. 2015;210:485–502. doi: 10.1083/jcb.201501038. PubMed DOI PMC

Weinkove D., Bastiani M., Chessa T.A.M., Joshi D., Hauth L., Cooke F.T., Divecha N., Kim S. Overexpression of PPK-1, the C. elegans Type 1 PIP kinase, inhibits growth cone collapse in the developing nervous system and causes axonal degeneration in adults. Dev. Biol. 2008;313:384–397. doi: 10.1016/j.ydbio.2007.10.029. PubMed DOI PMC

Xu X., Guo H., Wycuff D.L., Lee M. Role of phosphatidylinositol-4-phosphate 5′ kinase (ppk-1) in ovulation of Caenorhabditis elegans. Exp. Cell Res. 2007;313:2465–2475. doi: 10.1016/j.yexcr.2007.03.017. PubMed DOI PMC

Sobol M., Yildirim S., Philimonenko V.V., Marasek P., Castano E., Hozak P. UBF complexes with phosphatidylinositol 4,5-bisphosphate in nucleolar organizer regions regardless of ongoing RNA polymerase I activity. Nucleus. 2013;4:478–486. doi: 10.4161/nucl.27154. PubMed DOI PMC

Mellman D.L., Gonzales M.L., Song C., Barlow C.A., Wang P., Kendziorski C., Anderson R.A. A PtdIns4,5P2-regulated nuclear poly(A) polymerase controls expression of select mRNAs. Nature. 2008;451:1013–1017. doi: 10.1038/nature06666. PubMed DOI

Kumsta C., Hansen M.C. Elegans rrf-1 mutations maintain RNAi efficiency in the soma in addition to the germline. PLoS ONE. 2012;7:e35428. doi: 10.1371/journal.pone.0035428. PubMed DOI PMC

Tang L., Machacek T., Mamnum Y.M., Penkner A., Gloggnitzer J., Wegrostek C., Konrat R., Jantsch M.F., Loidl J., Jantsch V. Mutations in Caenorhabditis elegans him-19 show meiotic defects that worsen with age. Mol. Biol. Cell. 2010;21:885–896. doi: 10.1091/mbc.e09-09-0811. PubMed DOI PMC

Cortes D.B., McNally K.L., Mains P.E., McNally F.J. The asymmetry of female meiosis reduces the frequency of inheritance of unpaired chromosomes. eLife. 2015;4:e06056. doi: 10.7554/eLife.06056. PubMed DOI PMC

Zhou Z., Hartwieg E., Horvitz H.R. CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell. 2001;104:43–56. doi: 10.1016/S0092-8674(01)00190-8. PubMed DOI

Colaiacovo M.P., MacQueen A.J., Martinez-Perez E., McDonald K., Adamo A., La Volpe A., Villeneuve A.M. Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev. Cell. 2003;5:463–474. doi: 10.1016/S1534-5807(03)00232-6. PubMed DOI

Kim H.M., Colaiacovo M.P. ZTF-8 interacts with the 9-1-1 complex and is required for DNA damage response and double-strand break repair in the C. elegans germline. PLoS Genet. 2014;10:e1004723. doi: 10.1371/journal.pgen.1004723. PubMed DOI PMC

Goodyer W., Kaitna S., Couteau F., Ward J.D., Boulton S.J., Zetka M. HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev. Cell. 2008;14:263–274. doi: 10.1016/j.devcel.2007.11.016. PubMed DOI

Yokoo R., Zawadzki K.A., Nabeshima K., Drake M., Arur S., Villeneuve A.M. COSA-1 Reveals Separable Licensing and Reinforcement Steps and Efficient Homeostasis Governing Meiotic Crossovers. Cell. 2012;149:75–87. doi: 10.1016/j.cell.2012.01.052. PubMed DOI PMC

Merlet J., Burger J., Tavernier N., Richaudeau B., Gomes J.E., Pintard L. The CRL2LRR-1 ubiquitin ligase regulates cell cycle progression during C. elegans development. Development. 2010;137:3857–3866. doi: 10.1242/dev.054866. PubMed DOI PMC

Burger J., Merlet J., Tavernier N., Richaudeau B., Arnold A., Ciosk R., Bowerman B., Pintard L. CRL2(LRR-1) E3-ligase regulates proliferation and progression through meiosis in the Caenorhabditis elegans germline. PLoS Genet. 2013;9:e1003375. doi: 10.1371/journal.pgen.1003375. PubMed DOI PMC

Panbianco C., Weinkove D., Zanin E., Jones D., Divecha N., Gotta M., Ahringer J. A casein kinase 1 and PAR proteins regulate asymmetry of a PIP(2) synthesis enzyme for asymmetric spindle positioning. Dev. Cell. 2008;15:198–208. doi: 10.1016/j.devcel.2008.06.002. PubMed DOI PMC

Chakrabarti R., Sanyal S., Ghosh A., Bhar K., Das C., Siddhanta A. Phosphatidylinositol-4-phosphate 5-Kinase 1α Modulates Ribosomal RNA Gene Silencing through Its Interaction with Histone H3 Lysine 9 Trimethylation and Heterochromatin Protein HP1-α. J. Biol. Chem. 2015;290:20893–20903. doi: 10.1074/jbc.M114.633727. PubMed DOI PMC

Hodgkin J., Horovitz H.R., Brenner S. Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics. 1979;91:67–94. PubMed PMC

Sullivan T., Escalante-Alcalde D., Bhatt H., Anver M., Bhat N., Nagashima K., Stewart C.L., Burke B. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J. Cell Biol. 1999;147:913–920. doi: 10.1083/jcb.147.5.913. PubMed DOI PMC

Starr D.A. A nuclear-envelope bridge positions nuclei and moves chromosomes. J. Cell Biol. 2009;122:577–586. doi: 10.1242/jcs.037622. PubMed DOI PMC

Penkner A., Tang L., Novatchkova M., Ladurner M., Fridkin A., Gruenbaum Y., Schweizer D., Loidl J., Jantsch V. The nuclear envelope protein Matefin/SUN-1 is required for homologous pairing in C. elegans meiosis. Dev. Cell. 2007;12:873–886. doi: 10.1016/j.devcel.2007.05.004. PubMed DOI

Jungmichel S., Sylvestersen K.B., Choudhary C., Nguyen S., Mann M., Nielsen M.L. Specificity and commonality of the phosphoinositide-binding proteome analyzed by quantitative mass spectrometry. Cell Rep. 2014;6:578–591. doi: 10.1016/j.celrep.2013.12.038. PubMed DOI

Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974;77:71–94. PubMed PMC

Timmons L., Fire A. Specific interference by ingested dsRNA. Nature. 1998;395:854. doi: 10.1038/27579. PubMed DOI

Martinez-Perez E., Villeneuve A.M. HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev. 2005;19:2727–2743. doi: 10.1101/gad.1338505. PubMed DOI PMC

Singh V.A., Aballay A. Regulation of DAF-16-mediated Innate Immunity in Caenorhabditis elegans. J. Biol. Chem. 2009;284:35580–35587. doi: 10.1074/jbc.M109.060905. PubMed DOI PMC

Masuda T., Tomita M., Ishihama Y. Phase Transfer Surfactant-Aided Trypsin Digestion for Membrane Proteome Analysis. J. Proteome Res. 2008;7:731–740. doi: 10.1021/pr700658q. PubMed DOI

Hebert A., Richards A.L., Bailey D.J., Ulbrich A., Coughlin E.E., Westphall M.S., Coon J.J. The one hour yeast proteome. Mol. Cell. Proteom. 2014;13:339–347. doi: 10.1074/mcp.M113.034769. PubMed DOI PMC

Cox J., Hein M.Y., Luber C.A., Paron I., Nagaraj N., Mann M. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol. Cell. Proteom. 2014;13:2513–2526. doi: 10.1074/mcp.M113.031591. PubMed DOI PMC

Harper N., Rillo R., Jover-Gil S., Assaf Z.J., Bhalla N., Dernburg A.F. Pairing centers recruit a Polo-like kinase to orchestrate meiotic chromosome dynamics in C. elegans. Dev. Cell. 2011;21:934–947. doi: 10.1016/j.devcel.2011.09.001. PubMed DOI PMC

Villeneuve A. A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Genetics. 1994;136:887–902. PubMed PMC

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