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Research Article

RanBP1 controls the Ran pathway in mammalian cells through regulation of mitotic RCC1 dynamics

ORCID Icon, , , , ORCID Icon & ORCID Icon
Pages 1899-1916 | Received 12 Sep 2019, Accepted 05 May 2020, Published online: 28 Jun 2020

References

  • Dasso M. The Ran GTPase: theme and variations. Curr Biol. 2002;12(14):R502–508.
  • de Boor S, Knyphausen P, Kuhlmann N, et al. Small GTP-binding protein Ran is regulated by posttranslational lysine acetylation. Proc Natl Acad Sci U S A. 2015;112(28):E3679–3688.
  • Stewart M. Molecular mechanism of the nuclear protein import cycle. Nat Rev Mol Cell Biol. 2007;8(3):195–208.
  • Kalab P. Visualization of a Ran-GTP gradient in interphase and mitotic Xenopus egg extracts. Science. 2002;295(5564):2452–2456.
  • Cavazza T, Vernos I. The RanGTP pathway: from nucleo-cytoplasmic transport to spindle assembly and beyond. Front Cell Dev Biol. 2015;3:82.
  • Bischoff FR, Krebber H, Smirnova E, et al. Co-activation of RanGTPase and inhibition of GTP dissociation by Ran-GTP binding protein RanBP1. Embo J. 1995;14(4):705–715.
  • Bischoff FR, Gorlich D. RanBP1 is crucial for the release of RanGTP from importin beta-related nuclear transport factors. FEBS Lett. 1997;419:249–254.
  • Lounsbury KM, Macara IG. Ran-binding protein 1 (RanBP1) forms a ternary complex with Ran and karyopherin beta and reduces Ran GTPase-activating protein (RanGAP) inhibition by karyopherin beta. J Biol Chem. 1997;272:551–555.
  • Zhang MS, Arnaoutov A, Dasso M. RanBP1 governs spindle assembly by defining mitotic Ran-GTP production. Dev Cell. 2014;31(4):393–404.
  • Li HY, Ng WP, Wong CH, et al. Coordination of chromosome alignment and mitotic progression by the chromosome-based Ran signal. Cell cycle (Georgetown, Tex.). 2007;6(15):1886–1895..
  • Tedeschi A, Ciciarello M, Mangiacasale R, et al. RANBP1 localizes a subset of mitotic regulatory factors on spindle microtubules and regulates chromosome segregation in human cells. J Cell Sci. 2007;120(21):3748–3761.
  • Hutchins JRA, Moore WJ, Hood FE, et al. Phosphorylation regulates the dynamic interaction of RCC1 with chromosomes during mitosis. Curr Biol. 2004;14(12):1099–1104.
  • Cong L, Ran FA, Cox D, et al. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339(6121):819–823.
  • Holland AJ, Fachinetti D, Han JS, et al. Inducible, reversible system for the rapid and complete degradation of proteins in mammalian cells. Proc Natl Acad Sci U S A. 2012;109(49):E3350–3357.
  • Nishimura K, Kanemaki MT. Rapid depletion of budding yeast proteins via the fusion of an Auxin-Inducible Degron (AID). Curr Protoc Cell Biol. 2014;64:20.29.21–16.
  • Morawska M, Ulrich HD. An expanded tool kit for the auxin-inducible degron system in budding yeast. Yeast. 2013;30:341–351.
  • Blancher C, Jones A. SDS-PAGE and western blotting techniques. Methods Mol Med. 2001;57:145–162.
  • Niopek D, Wehler P, Roensch J, et al. Optogenetic control of nuclear protein export. Nat Commun. 2016;7:10624.
  • Li H-Y. Phosphorylation of RCC1 in mitosis is essential for producing a high RanGTP concentration on chromosomes and for spindle assembly in mammalian cells. Genes Dev. 2004;18(5):512–527.
  • Neumuller RA, Richter C, Fischer A, et al. Genome-wide analysis of self-renewal in Drosophila neural stem cells by transgenic RNAi. Cell Stem Cell. 2011;8(5):580–593.
  • Gray WM, Kepinski S, Rouse D, et al. Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature. 2001;414:271–276.
  • Nishimura K, Fukagawa T, Takisawa H, et al. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat Methods. 2009;6:917–922.
  • Plafker K, Macara IG. Facilitated nucleocytoplasmic shuttling of the Ran binding protein RanBP1. Mol Cell Biol. 2000;20(10):3510–3521.
  • Ciciarello M, Roscioli E, Di Fiore B, et al. Nuclear reformation after mitosis requires downregulation of the Ran GTPase effector RanBP1 in mammalian cells. Chromosoma. 2010;119:651–668.
  • Nagai M, Moriyama T, Mehmood R, et al. Mice lacking Ran binding protein 1 are viable and show male infertility. FEBS Lett. 2011;585:791–796.
  • Koffa MD, Casanova CM, Santarella R, et al. HURP is part of a Ran-dependent complex involved in spindle formation. Curr Biol. 2006;16(8):743–754.
  • Sillje HH, Nagel S, Korner R, et al. HURP is a Ran-importin beta-regulated protein that stabilizes kinetochore microtubules in the vicinity of chromosomes. Curr Biol. 2006;16:731–742.
  • Chen T, Muratore TL, Schaner-Tooley CE, et al. N-terminal alpha-methylation of RCC1 is necessary for stable chromatin association and normal mitosis. Nat Cell Biol. 2007;9:596–603.
  • Tooley CE, Petkowski JJ, Muratore-Schroeder TL, et al. NRMT is an alpha-N-methyltransferase that methylates RCC1 and retinoblastoma protein. Nature. 2010;466(7310):1125–1128.
  • van Hooff JJ, Tromer E, van Wijk LM, et al. Evolutionary dynamics of the kinetochore network in eukaryotes as revealed by comparative genomics. EMBO Rep. 2017;18(9):1559–1571.
  • Bushman DM, Chun J. The genomically mosaic brain: aneuploidy and more in neural diversity and disease. Semin Cell Dev Biol. 2013;24:357–369.
  • Sullivan AE, Silver RM, LaCoursiere DY, et al. Recurrent fetal aneuploidy and recurrent miscarriage. Obstet Gynecol. 2004;104(4):784–788.
  • Weaver BA, Cleveland DW. The aneuploidy paradox in cell growth and tumorigenesis. Cancer Cell. 2008;14(6):431–433.
  • Vaidyanathan S, Thangavelu PU, Duijf PH. Overexpression of Ran GTPase components regulating nuclear export, but not mitotic spindle assembly, marks chromosome instability and poor prognosis in breast cancer. Target Oncol. 2016;11:677–686.
  • Ly DH, Lockhart DJ, Lerner RA, et al. Mitotic misregulation and human aging. Science. 2000;287:2486–2492.
  • Pujol G, Soderqvist H, Radu A. Age-associated reduction of nuclear protein import in human fibroblasts. Biochem Biophys Res Commun. 2002;294(2):354–358.
  • Hasegawa K, Ryu SJ, Kalab P. Chromosomal gain promotes formation of a steep RanGTP gradient that drives mitosis in aneuploid cells. J Cell Biol. 2013;200(2):151–161.
  • Kalab P, Heald R. The RanGTP gradient - a GPS for the mitotic spindle. J Cell Sci. 2008;121(10):1577–1586.