ISWI ATP-dependent remodeling of nucleoplasmic ω-speckles in the brain of Drosophila melanogaster

Luca Lo Piccolo; Andrea Attardi; Rosa Bonaccorso; Lorenzo Li Greci; Giorgio Giurato; Antonia Maria Rita Ingrassia; Maria Cristina Onorati

doi:10.1016/j.jgg.2016.12.002

Volume 44 Issue 2

Feb. 2017

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2017 > 44(2): 85-94

PDF( 1762 KB)

ISWI ATP-dependent remodeling of nucleoplasmic ω-speckles in the brain of Drosophila melanogaster

doi: 10.1016/j.jgg.2016.12.002

a
STEBICEF Department, University of Palermo, Palermo 90128, Italy
b
Genomix4Life Srl, University of Salerno, Baronissi Campus, Salerno 84081, Italy

More Information

Corresponding author: E-mail address: mconorati@dti.telethon.it (Maria Cristina Onorati)
Received Date: 2016-07-29
Accepted Date: 2016-12-18
Rev Recd Date: 2016-11-21

Available Online: 2016-12-22

Publish Date: 2017-02-20

Abstract

Abstract

Heterogeneous nuclear ribonucleoproteins (hnRNPs) belong to the RNA-binding proteins family. They are involved in processing heterogeneous nuclear RNAs (hnRNAs) into mature mRNAs. These proteins participate in every step of mRNA cycle, such as mRNA export, localization, translation, stability and alternative splicing. At least 14 major hnRNPs, which have structural and functional homologues in mammals, are expressed inDrosophila melanogaster. Until now, six of these hnRNPs are known to be nucleus-localized and associated with the long non-coding RNA (lncRNA) heat shock responsive ω (hsrω) in the omega speckle compartments (ω-speckles). The chromatin remodeler ISWI is the catalytic subunit of several ATP-dependent chromatin-remodeling complexes, and it is an essential factor for organization of ω-speckles. Indeed, in ISWI null mutant, severe defects in ω-speckles structure are detectable. Here, we clarify the role of ISWI in the hnRNPs‒hsrω interaction. Moreover, we describe how ISWI by its remodeling activity, controls hsrω and hnRNPs engagement in ω-speckles. Finally, we demonstrate that the sequestration of hnRNPs in ω-speckles nuclear compartment is a fundamental event in gene expression control and represents a key step in the regulation of several pathways.
- Omega speckles,
- hnRNPs,
- lncRNA,
- Nuclear body,
- Chromatin remodelers

Current address: Turku Center for Biotechnology, University of Turku, Turku FIN-20520, Finland.

FullText(HTML)

References(49)

References

[1]	Anders, S., Pyl, P.T., Huber, W. HTSeq–a Python framework to work with high-throughput sequencing data Bioinformatics, 31 (2015),pp. 166-169
[2]	Babic, I., Anderson, E.S., Tanaka, K. et al. EGFR mutation-induced alternative splicing of max contributes to growth of glycolytic tumors in brain cancer Cell Metab., 17 (2013),pp. 1000-1008
[3]	Bhat, R., Axtell, R., Mitra, A. et al. Inhibitory role for GABA in autoimmune inflammation Proc. Natl. Acad. Sci. U. S. A., 107 (2010),pp. 2580-2585
[4]	Biamonti, G., Vourc'h, C. Nuclear stress bodies Cold Spring Harb. Perspect. Biol., 2 (2010),p. a000695
[5]	Burgio, G., La Rocca, G., Sala, A. et al. Genetic identification of a network of factors that functionally interact with the nucleosome remodeling ATPase ISWI PLoS Genet., 4 (2008),p. e1000089
[6]	Clemson, C.M., Hutchinson, J.N., Sara, S.A. et al. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles Mol. Cell, 33 (2009),pp. 717-726
[7]	Corona, D.F., Langst, G., Clapier, C.R. et al. ISWI is an ATP-dependent nucleosome remodeling factor Mol. Cell, 3 (1999),pp. 239-245
[8]	Corona, D.F., Siriaco, G., Armstrong, J.A. et al. PLoS Biol., 5 (2007),p. e232
[9]	David, C.J., Manley, J.L. Alternative pre-mRNA splicing regulation in cancer: pathways and programs unhinged Genes Dev., 24 (2010),pp. 2343-2364
[10]	Deuring, R., Fanti, L., Armstrong, J.A. et al. Mol. Cell, 5 (2000),pp. 355-365
[11]	Dobin, A., Davis, C.A., Schlesinger, F. et al. STAR: ultrafast universal RNA-seq aligner Bioinformatics, 29 (2013),pp. 15-21
[12]	Dreyfuss, G., Kim, V.N., Kataoka, N. Messenger-RNA-binding proteins and the messages they carry Nat. Rev. Mol. Cell Biol., 3 (2002),pp. 195-205
[13]	Dundr, M., Misteli, T. Biogenesis of nuclear bodies Cold Spring Harb. Perspect. Biol., 2 (2010),p. a000711
[14]	Gao, R., Yu, Y., Inoue, A. et al. Heterogeneous nuclear ribonucleoprotein K (hnRNP-K) promotes tumor metastasis by induction of genes involved in extracellular matrix, cell movement, and angiogenesis J. Biol. Chem., 288 (2013),pp. 15046-15056
[15]	Goodrich, J.S., Clouse, K.N., Schupbach, T. Development, 131 (2004),pp. 1949-1958
[16]	Grune, T., Brzeski, J., Eberharter, A. et al. Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI Mol. Cell, 12 (2003),pp. 449-460
[17]	Halliwell, B. Oxidative stress and neurodegeneration: where are we now? J. Neurochem., 97 (2006),pp. 1634-1658
[18]	Han, N., Li, W., Zhang, M. The function of the RNA-binding protein hnRNP in cancer metastasis J. Cancer Res. Ther., 9 (2013)
[19]	Hayes, J.D., Flanagan, J.U., Jowsey, I.R. Glutathione transferases Annu. Rev. Pharmacol. Toxicol., 45 (2005),pp. 51-88
[20]	Jean-Philippe, J., Paz, S., Caputi, M. hnRNP A1: the Swiss army knife of gene expression Int. J. Mol. Sci., 14 (2013),pp. 18999-19024
[21]	Jolly, C., Lakhotia, S.C. Nucleic Acids Res., 34 (2006),pp. 5508-5514
[22]	Kawaguchi, T., Hirose, T. Chromatin remodeling complexes in the assembly of long noncoding RNA-dependent nuclear bodies Nucleus, 6 (2015),pp. 462-467
[23]	Kawaguchi, T., Tanigawa, A., Naganuma, T. et al. SWI/SNF chromatin-remodeling complexes function in noncoding RNA-dependent assembly of nuclear bodies Proc. Natl. Acad. Sci. U. S. A., 112 (2015),pp. 4304-4309
[24]	Kim, H.J., Kim, N.C., Wang, Y.D. et al. Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS Nature, 495 (2013),pp. 467-473
[25]	Koga, M., Serritella, A.V., Sawa, A. et al. Implications for reactive oxygen species in schizophrenia pathogenesis Schizophr. Res., 176 (2015),pp. 52-71
[26]	Kore, R.A., Abraham, E.C. Inflammatory cytokines, interleukin-1 beta and tumor necrosis factor-alpha, upregulated in glioblastoma multiforme, raise the levels of CRYAB in exosomes secreted by U373 glioma cells Biochem. Biophys. Res. Commun., 453 (2014),pp. 326-331
[27]	Laborde, E. Glutathione transferases as mediators of signaling pathways involved in cell proliferation and cell death Cell Death Differ., 17 (2010),pp. 1373-1380
[28]	Lakhotia, A.K.S.S.C. Chromosoma, 124 (2015),pp. 367-383
[29]	Lakhotia, S.C. J. Biosci., 36 (2011),pp. 399-423
[30]	Lakhotia, S.C., Mallik, M., Singh, A.K. et al. Chromosoma, 121 (2012),pp. 49-70
[31]	Lakhotia, S.C., Sharma, A. Chromosome Res., 3 (1995),pp. 151-161
[32]	Lamond, A.I., Earnshaw, W.C. Structure and function in the nucleus Science, 280 (1998),pp. 547-553
[33]	Lo Piccolo, L., Bonaccorso, R., Onorati, M.C. Int. J. Mol. Sci., 16 (2015),pp. 12360-12367
[34]	Love, M.I., Huber, W., Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Genome Biol., 15 (2014),p. 550
[35]	Martin, M. Cutadapt removes adapter sequences from highthroughput sequencing reads EMBnet J., 17 (2011),pp. 10-12
[36]	Mallik, M., Lakhotia, S.C. J. Biosci., 36 (2011),pp. 265-280
[37]	Manning, B.J., Peterson, C.L. Releasing the brakes on a chromatin-remodeling enzyme Nat. Struct. Mol. Biol., 20 (2013),pp. 5-7
[38]	Marazziti, D., Baroni, S., Picchetti, M. et al. Psychiatric disorders and mitochondrial dysfunctions Eur. Rev. Med. Pharmacol. Sci., 16 (2012),pp. 270-275
[39]	Marques-Rocha, J.L., Samblas, M., Milagro, F.I. et al. Noncoding RNAs, cytokines, and inflammation-related diseases FASEB J., 29 (2015),pp. 3595-3611
[40]	McCloy, R.A., Rogers, S., Caldon, C.E. et al. Partial inhibition of Cdk1 in G 2 phase overrides the SAC and decouples mitotic events Cell Cycle, 13 (2014),pp. 1400-1412
[41]	Mueller-Planitz, F., Klinker, H., Ludwigsen, J. et al. The ATPase domain of ISWI is an autonomous nucleosome remodeling machine Nat. Struct. Mol. Biol., 20 (2013),pp. 82-89
[42]	Onorati, M.C., Lazzaro, S., Mallik, M. et al. The ISWI chromatin remodeler organizes the hsromega ncRNA-containing omega speckle nuclear compartments PLoS Genet., 7 (2011),p. e1002096
[43]	Piccolo, L.L., Corona, D., Onorati, M.C. Emerging roles for hnRNPs in post-transcriptional regulation: what can we learn from flies? Chromosoma, 123 (2014),pp. 515-527
[44]	Prasanth, K.V., Rajendra, T.K., Lal, A.K. et al. Omega speckles - a novel class of nuclear speckles containing hnRNPs associated with noncoding hsr-omega RNA in Drosophila J. Cell Sci., 113 (2000),pp. 3485-3497
[45]	Rochfort, K.D., Cummins, P.M. The blood-brain barrier endothelium: a target for pro-inflammatory cytokines Biochem. Soc. Trans., 43 (2015),pp. 702-706
[46]	Romano, M., Buratti, E. Targeting RNA binding proteins involved in neurodegeneration J. Biomol. Screen, 18 (2013),pp. 967-983
[47]	Singh, A.K., Lakhotia, S.C. Chromosoma, 124 (2015),pp. 367-383
[48]	Spector, D.L. SnapShot: cellular bodies Cell, 127 (2006),p. 1071
[49]	Zhao, R., Bodnar, M.S., Spector, D.L. Nuclear neighborhoods and gene expression Curr. Opin. Genet. Dev., 19 (2009),pp. 172-179