The actin family protein ARP6 contributes to the structure and the function of the nucleolus

. 2015 Aug 21 ; 464 (2) : 554-60. [epub] 20150709

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, Research Support, N.I.H., Intramural, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid26164235

Grantová podpora
Z99 AG999999 Intramural NIH HHS - United States
ZIA AG000511-19 Intramural NIH HHS - United States

Odkazy

PubMed 26164235
PubMed Central PMC5920680
DOI 10.1016/j.bbrc.2015.07.005
PII: S0006-291X(15)30236-9
Knihovny.cz E-zdroje

The actin family members, consisting of actin and actin-related proteins (ARPs), are essential components of chromatin remodeling complexes. ARP6, one of the nuclear ARPs, is part of the Snf-2-related CREB-binding protein activator protein (SRCAP) chromatin remodeling complex, which promotes the deposition of the histone variant H2A.Z into the chromatin. In this study, we showed that ARP6 influences the structure and the function of the nucleolus. ARP6 is localized in the central region of the nucleolus, and its knockdown induced a morphological change in the nucleolus. We also found that in the presence of high concentrations of glucose ARP6 contributed to the maintenance of active ribosomal DNA (rDNA) transcription by placing H2A.Z into the chromatin. In contrast, under starvation, ARP6 was required for cell survival through the repression of rDNA transcription independently of H2A.Z. These findings reveal novel pleiotropic roles for the actin family in nuclear organization and metabolic homeostasis.

Zobrazit více v PubMed

Oma Y, Harata M. Actin-related proteins localized in the nucleus: from discovery to novel roles in nuclear organization. Nucleus. 2011;2:38–46. PubMed PMC

Mizuguchi G, Shen X, Landry J, Wu WH, Sen S, Wu C. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science. 2004;303:343–348. PubMed

Matsuda R, Hori T, Kitamura H, Takeuchi K, Fukagawa T, Harata M. Identification and characterization of the two isoforms of the vertebrate H2A.Z histone variant. Nucleic Acids Res. 2010;38:4263–4273. PubMed PMC

Kumar SV, Wigge PA. H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell. 2010;140:136–147. PubMed

Hu G, Cui K, Northrup D, Liu C, Wang C, Tang Q, Ge K, Levens D, Crane-Robinson C, Zhao K. H2A.Z facilitates access of active and repressive complexes to chromatin in embryonic stem cell self-renewal and differentiation. Cell Stem Cell. 2013;12:180–192. PubMed PMC

Gallant-Behm CL, Ramsey MR, Bensard CL, Nojek I, Tran J, Liu M, Ellisen LW, Espinosa JM. DeltaNp63alpha represses anti-proliferative genes via H2A.Z deposition. Genes Dev. 2012;26:2325–2336. PubMed PMC

Simon DN, Zastrow MS, Wilson KL. Direct actin binding to A- and B-type lamin tails and actin filament bundling by the lamin A tail. Nucleus. 2010;1:264–272. PubMed PMC

Cibulka J, Fraiberk M, Forstova J. Nuclear actin and lamins in viral infections. Viruses. 2012;4:325–347. PubMed PMC

Verboon JM, Rincon-Arano H, Werwie TR, Delrow JJ, Scalzo D, Nandakumar V, Groudine M, Parkhurst SM. Wash interacts with lamin and affects global nuclear organization. Curr. Biol. 2015;25:804–810. PubMed PMC

Yoshida T, Shimada K, Oma Y, Kalck V, Akimura K, Taddei A, Iwahashi H, Kugou K, Ohta K, Gasser SM, Harata M. Actin-related protein Arp6 influences H2A.Z-dependent and -independent gene expression and links ribosomal protein genes to nuclear pores. PLoS Genet. 2010;6:e1000910. PubMed PMC

Maruyama EO, Hori T, Tanabe H, Kitamura H, Matsuda R, Tone S, Hozak P, Habermann FA, von Hase J, Cremer C, Fukagawa T, Harata M. The actin family member Arp6 and the histone variant H2A.Z are required for spatial positioning of chromatin in chicken cell nuclei. J. Cell Sci. 2012;125:3739–2743. PubMed

Moss T, Langlois F, Gagnon-Kugler T, Stefanovsky V. A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell. Mol. Life Sci. 2007;64:29–49. PubMed PMC

Drygin D, Rice WG, Grummt I. The RNA polymerase I transcription machinery: an emerging target for the treatment of cancer. Annu Rev. Pharmacol. Toxicol. 2010;50:131–156. PubMed

Grummt I. The nucleolus-guardian of cellular homeostasis and genome integrity. Chromosoma. 2013;122:487–497. PubMed

Grummt I, Voit R. Linking rDNA transcription to the cellular energy supply. Cell Cycle. 2010;9:225–226. PubMed

Tanaka Y, Okamoto K, Teye K, Umata T, Yamagiwa N, Suto Y, Zhang Y, Tsuneoka M. JmjC enzyme KDM2A is a regulator of rRNA transcription in response to starvation. EMBO J. 2010;29:1510–1522. PubMed PMC

Hoppe S, Bierhoff H, Cado I, Weber A, Tiebe M, Grummt I, Voit R. AMP-activated protein kinase adapts rRNA synthesis to cellular energy supply. Proc. Natl. Acad. Sci. U. S. A. 2009;106:17781–17786. PubMed PMC

Boulon S, Westman BJ, Hutten S, Boisvert FM, Lamond AI. The nucleolus under stress. Mol. Cell. 2010;40:216–227. PubMed PMC

Kitayama K, Kamo M, Oma Y, Matsuda R, Uchida T, Ikura T, Tashiro S, Ohyama T, Winsor B, Harata M. The human actin-related protein hArp5: nucleo-cytoplasmic shuttling and involvement in DNA repair. Exp. Cell Res. 2009;315:206–217. PubMed

Ohfuchi E, Kato M, Sasaki M, Sugimoto K, Oma Y, Harata M. Vertebrate Arp6, a novel nuclear actin-related protein, interacts with heterochromatin protein 1. Eur. J. Cell. Biol. 2006;85:411–421. PubMed

Orlov N, Shamir L, Macura T, Johnston J, Eckley DM, Goldberg IG. WNDCHARM: multi-purpose image classification using compound image transforms. Pattern Recognit. Lett. 2008;29:1684–1693. PubMed PMC

Shamir L, Delaney JD, Orlov N, Eckley DM, Goldberg IG. Pattern recognition software and techniques for biological image analysis. PLoS Comput. Biol. 2010;6:e1000974. PubMed PMC

Eliceiri KW, Berthold MR, Goldberg IG, Ibanez L, Manjunath BS, Martone ME, Murphy RF, Peng H, Plant AL, Roysam B, Stuurman N, Swedlow JR, Tomancak P, Carpenter AE. Biological imaging software tools. Nat. Methods. 2012;9:697–710. PubMed PMC

Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods. 2012;9:671–675. PubMed PMC

Johnston J, Iser WB, Chow DK, Goldberg IG, Wolkow CA. Quantitative image analysis reveals distinct structural transitions during aging in caenorhabditis elegans tissues. PLoS One. 2008;3:e2821. PubMed PMC

Shav-Tal Y, Blechman J, Darzacq X, Montagna C, Dye BT, Patton JG, Singer RH, Zipori D. Dynamic sorting of nuclear components into distinct nucleolar caps during transcriptional inhibition. Mol. Biol. Cell. 2005;16:2395–2413. PubMed PMC

Shamir L, Orlov N, Eckley DM, Macura T, Johnston J, Goldberg IG. Wndchrm - an open source utility for biological image analysis. Source Code Biol. Med. 2008;3:13. PubMed PMC

van de Nobelen S, Rosa-Garrido M, Leers J, Heath H, Soochit W, Joosen L, Jonkers I, Demmers J, van der Reijden M, Torrano V, Grosveld F, Delgado MD, Renkawitz R, Galjart N, Sleutels F. CTCF regulates the local epigenetic state of ribosomal DNA repeats. Epigenetics Chromatin. 2010;3:19. PubMed PMC

Murayama A, Ohmori K, Fujimura A, Minami H, Yasuzawa-Tanaka K, Kuroda T, Oie S, Daitoku H, Okuwaki M, Nagata K, Fukamizu A, Kimura K, Shimizu T, Yanagisawa J. Epigenetic control of rDNA loci in response to intracellular energy status. Cell. 2008;133:627–639. PubMed

Boisvert FM, van Koningsbruggen S, Navascues J, Lamond AI. The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 2007;8:574–585. PubMed

Sloan KE, Bohnsack MT, Watkins NJ. The 5S RNP couples p53 homeostasis to ribosome biogenesis and nucleolar stress. Cell. Rep. 2013;5:237–247. PubMed PMC

Weber JD, Taylor LJ, Roussel MF, Sherr CJ, Bar-Sagi D. Nucleolar Arf sequesters Mdm2 and activates p53. Nat. Cell Biol. 1999;1:20–26. PubMed

Rubbi CP, Milner J. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J. 2003;22:6068–6077. PubMed PMC

Tsai RY, Pederson T. Connecting the nucleolus to the cell cycle and human disease. FASEB J. 2014;28:3290–3296. PubMed

Hetman M. Role of the nucleolus in human diseases. Preface. Biochim. Biophys. Acta. 2014;1842:757. PubMed

Hetman M, Pietrzak M. Emerging roles of the neuronal nucleolus. Trends Neurosci. 2012;35:305–314. PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...