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Article

Disruption of the Ran System by Cysteine Oxidation of the Nucleotide Exchange Factor RCC1

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Pages 566-581 | Received 05 Sep 2014, Accepted 19 Nov 2014, Published online: 20 Mar 2023

REFERENCES

  • Pemberton LF, Paschal BM. 2005. Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 6:187–198. http://dx.doi.org/10.1111/j.1600-0854.2005.00270.x.
  • Stewart M. 2007. Molecular mechanism of the nuclear protein import cycle. Nat Rev Mol Cell Biol 8:195–208. http://dx.doi.org/10.1038/nrm2114.
  • Ohtsubo M, Okazaki H, Nishimoto T. 1989. The RCC1 protein, a regulator for the onset of chromosome condensation locates in the nucleus and binds to DNA. J Cell Biol 109:1389–1397. http://dx.doi.org/10.1083/jcb.109.4.1389.
  • Bischoff FR, Ponstingl H. 1991. Catalysis of guanine nucleotide exchange factor on Ran by the mitotic regulator RCC1. Nature 354:80–82. http://dx.doi.org/10.1038/354080a0.
  • Bourne HR, Sanders DA, McCormick F. 1991. The GTPase superfamily: conserved structure and molecular mechanism. Nature 349:117–127. http://dx.doi.org/10.1038/349117a0.
  • Bischoff FR, Klebe C, Kretschmer J, Wittinghofer A, Ponstingl H. 1994. RanGAP1 induces GTPase activity of nuclear Ras-related Ran. Proc Natl Acad Sci U S A 91:2587–2591. http://dx.doi.org/10.1073/pnas.91.7.2587.
  • Paschal BM, Gerace L. 1995. Identification of NTF2, a cytosolic factor for nuclear import that interacts with nuclear pore complex protein p62. J Cell Biol 129:925–937. http://dx.doi.org/10.1083/jcb.129.4.925.
  • Paschal BM, Delphin C, Gerace L. 1996. Nucleotide-specific interaction of Ran/TC4 with nuclear transport factors NTF2 and p97. Proc Natl Acad Sci U S A 93:7679–7683. http://dx.doi.org/10.1073/pnas.93.15.7679.
  • Ribbeck KK, Lipowsky GG, Kent HMH, Stewart MM, Görlich DD. 1998. NTF2 mediates nuclear import of Ran. EMBO J 17:6587–6598. http://dx.doi.org/10.1093/emboj/17.22.6587.
  • Smith A, Brownawell A, Macara IG. 1998. Nuclear import of Ran is mediated by the transport factor NTF2. Curr Biol 8:1403–1406. http://dx.doi.org/10.1016/S0960-9822(98)00023-2.
  • Kelley JB, Paschal BM. 2007. Hyperosmotic stress signaling to the nucleus disrupts the Ran gradient and the production of RanGTP. Mol Biol Cell 18:4365–4376. http://dx.doi.org/10.1091/mbc.E07-01-0089.
  • Izaurralde E, Kutay U, von Kobbe C, Mattaj IW, Gorlich D. 1997. The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus. EMBO J 16:6535–6547. http://dx.doi.org/10.1093/emboj/16.21.6535.
  • Kelley JB, Datta S, Snow CJ, Chatterjee M, Ni L, Spencer A, Yang C-S, Cubeñas-Potts C, Matunis MJ, Paschal BM. 2011. The defective nuclear lamina in Hutchinson-Gilford progeria syndrome disrupts the nucleocytoplasmic Ran gradient and inhibits nuclear localization of Ubc9. Mol Cell Biol 31:3378–3395. http://dx.doi.org/10.1128/MCB.05087-11.
  • Clarkson W, Corbett AH, Paschal BM, Kent HM, McCoy AJ, Gerace L, Silver PA, Stewart M. 1997. Nuclear protein import is decreased by engineered mutants of nuclear transport factor 2 (NTF2) that do not bind GDP-Ran. J Mol Biol 272:716–730. http://dx.doi.org/10.1006/jmbi.1997.1255.
  • Tachibana T, Imamoto N, Seino H, Nishimoto T, Yoneda Y. 1994. Loss of Rcc1 leads to suppression of nuclear-protein import in living cells. J Biol Chem 269:24542–24545.
  • Renault L, Nassar N, Vetter I, Becker J, Klebe C, Roth M, Wittinghofer A. 1998. The 1.7A crystal structure of the regulator of chromosome condensation (RCC1) reveals a seven-bladed propeller. Nature 392:97–101. http://dx.doi.org/10.1038/32204.
  • Seino H, Hisamoto N, Uzawa S, Sekiguchi T, Nishimoto T. 1992. DNA-binding domain of RCC1 protein is not essential for coupling mitosis with DNA replication. J Cell Sci 102(Pt 3):393–400.
  • Nemergut ME, Mizzen CA, Stukenberg T, Allis CD, Macara IG. 2001. Chromatin docking and exchange activity enhancement of RCC1 by histones H2A and H2B. Science 292:1540–1543. http://dx.doi.org/10.1126/science.292.5521.1540.
  • Li H-Y, Wirtz D, Zheng Y. 2003. A mechanism of coupling RCC1 mobility to RanGTP production on the chromatin in vivo. J Cell Biol 160:635–644. http://dx.doi.org/10.1083/jcb.200211004.
  • England JR, Huang J, Jennings MJ, Makde RD, Tan S. 2010. RCC1 uses a conformationally diverse loop region to interact with the nucleosome: a model for the RCC1-nucleosome complex. J Mol Biol 398:518–529. http://dx.doi.org/10.1016/j.jmb.2010.03.037.
  • Makde RD, England JR, Yennawar HP, Tan S. 2010. Structure of RCC1 chromatin factor bound to the nucleosome core particle. Nature 467:562–566. http://dx.doi.org/10.1038/nature09321.
  • Chen T, Muratore TL, Schaner-Tooley CE, Shabanowitz J, Hunt DF, Macara IG. 2007. N-terminal alpha-methylation of RCC1 is necessary for stable chromatin association and normal mitosis. Nat Cell Biol 9:596–603. http://dx.doi.org/10.1038/ncb1572.
  • Hao Y, Macara IG. 2008. Regulation of chromatin binding by a conformational switch in the tail of the Ran exchange factor RCC1. J Cell Biol 182:827–836. http://dx.doi.org/10.1083/jcb.200803110.
  • Li H-Y, Zheng Y. 2004. Phosphorylation of RCC1 in mitosis is essential for producing a high RanGTP concentration on chromosomes and for spindle assembly in mammalian cells. Genes Dev 18:512–527. http://dx.doi.org/10.1101/gad.1177304.
  • Geiszt M, Leto TL. 2004. The Nox family of NAD(P)H oxidases: host defense and beyond. J Biol Chem 279:51715–51718. http://dx.doi.org/10.1074/jbc.R400024200.
  • Li J, Stouffs M, Serrander L, Banfi B, Bettiol E, Charnay Y, Steger K, Krause K-H, Jaconi ME. 2006. The NADPH oxidase NOX4 drives cardiac differentiation: role in regulating cardiac transcription factors and MAP kinase activation. Mol Biol Cell 17:3978–3988. http://dx.doi.org/10.1091/mbc.E05-06-0532.
  • Sauer H, Rahimi C, Hescheler J, Wartenberg M. 2000. Role of reactive oxygen species and phosphatidylinositol 3-kinase in cardiomyocyte differentiation of embryonic stem cells. FEBS Lett 476:218–223. http://dx.doi.org/10.1016/S0014-5793(00)01747-6.
  • Cai H. 2005. Hydrogen peroxide regulation of endothelial function: origins, mechanisms, and consequences. Cardiovasc Res 68:26–36. http://dx.doi.org/10.1016/j.cardiores.2005.06.021.
  • Veal EA, Day AM, Morgan BA. 2007. Hydrogen peroxide sensing and signaling. Mol Cell 26:1–14. http://dx.doi.org/10.1016/j.molcel.2007.03.016.
  • Finkel T, Holbrook NJ. 2000. Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247. http://dx.doi.org/10.1038/35040709.
  • Chen D, Toone WM, Mata J, Lyne R, Burns G, Kivinen K, Brazma A, Jones N, Bähler J. 2003. Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 14:214–229. http://dx.doi.org/10.1091/mbc.E02-08-0499.
  • Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257. http://dx.doi.org/10.1091/mbc.11.12.4241.
  • Stochaj U, Rassadi R, Chiu J. 2000. Stress-mediated inhibition of the classical nuclear protein import pathway and nuclear accumulation of the small GTPase Gsp1p. FASEB J 14:2130–2132. http://dx.doi.org/10.1096/fj.99-0751fje.
  • Kodiha M, Chu A, Matusiewicz N, Stochaj U. 2004. Multiple mechanisms promote the inhibition of classical nuclear import upon exposure to severe oxidative stress. Cell Death Differ 11:862–874. http://dx.doi.org/10.1038/sj.cdd.4401432.
  • Miyamoto Y, Saiwaki T, Yamashita J, Yasuda Y, Kotera I, Shibata S, Shigeta M, Hiraoka Y, Haraguchi T, Yoneda Y. 2004. Cellular stresses induce the nuclear accumulation of importin alpha and cause a conventional nuclear import block. J Cell Biol 165:617–623. http://dx.doi.org/10.1083/jcb.200312008.
  • Kodiha M, Tran D, Qian C, Morogan A, Presley JF, Brown CM, Stochaj U. 2008. Oxidative stress mislocalizes and retains transport factor importin-alpha and nucleoporins Nup153 and Nup88 in nuclei where they generate high molecular mass complexes. Biochim Biophys Acta 1783:405–418. http://dx.doi.org/10.1016/j.bbamcr.2007.10.022.
  • Crampton N, Kodiha M, Shrivastava S, Umar R, Stochaj U. 2009. Oxidative stress inhibits nuclear protein export by multiple mechanisms that target FG nucleoporins and Crm1. Mol Biol Cell 20:5106–5116. http://dx.doi.org/10.1091/mbc.E09-05-0397.
  • Yasuda Y, Miyamoto Y, Saiwaki T, Yoneda Y. 2006. Mechanism of the stress-induced collapse of the Ran distribution. Exp Cell Res 312:512–520. http://dx.doi.org/10.1016/j.yexcr.2005.11.017.
  • Viteri G, Chung YW, Stadtman ER. 2010. Effect of progerin on the accumulation of oxidized proteins in fibroblasts from Hutchinson Gilford progeria patients. Mech Ageing Dev 131:2–8. http://dx.doi.org/10.1016/j.mad.2009.11.006.
  • Datta S, Snow CJ, Paschal BM. 2014. A pathway linking oxidative stress and the Ran GTPase system in progeria. Mol Biol Cell 25:1202–1215. http://dx.doi.org/10.1091/mbc.E13-07-0430.
  • Eisinger-Mathason TK, Andrade J, Groehler AL, Clark DE, Muratore-Schroeder TL, Pasic L, Smith JA, Shabanowitz J, Hunt DF, Macara IG, Lannigan DA. 2008. Codependent functions of RSK2 and the apoptosis-promoting factor TIA-1 in stress granule assembly and cell survival. Mol Cell 31:722–736. http://dx.doi.org/10.1016/j.molcel.2008.06.025.
  • Toone WM, Kuge S, Samuels M, Morgan BA, Toda T, Jones N. 1998. Regulation of the fission yeast transcription factor Pap1 by oxidative stress: requirement for the nuclear export factor Crm1 (exportin) and the stress-activated MAP kinase StyI/Spc1. Genes Dev 12:1453–1463. http://dx.doi.org/10.1101/gad.12.10.1453.
  • Steggerda SM, Paschal BM. 2000. The mammalian Mog1 protein is a guanine nucleotide release factor for Ran. J Biol Chem 275:23175–23180. http://dx.doi.org/10.1074/jbc.C000252200.
  • Welch K, Franke J, Kohler M, Macara IG. 1999. RanBP3 contains an unusual nuclear localization signal that is imported preferentially by importin-alpha3. Mol Cell Biol 19:8400–8411.
  • Kosower NS, Kosower EM. 1995. Diamide: an oxidant probe for thiols. Methods Enzymol 251:123–133. http://dx.doi.org/10.1016/0076-6879(95)51116-4.
  • Ohtsubo M, Kai R, Furuno N, Sekiguchi T, Sekiguchi M, Hayashida H, Kuma K, Miyata T, Fukushige S, Murotsu T. 1987. Isolation and characterization of the active cDNA of the human cell cycle gene (RCC1) involved in the regulation of onset of chromosome condensation. Genes Dev 1:585–593. http://dx.doi.org/10.1101/gad.1.6.585.
  • Uchida S, Sekiguchi T, Nishitani H, Miyauchi K, Ohtsubo M, Nishimoto T. 1990. Premature chromosome condensation is induced by a point mutation in the hamster RCC1 gene. Mol Cell Biol 10:577–584.
  • Seki T, Hayashi N, Nishimoto T. 1996. RCC1 in the Ran pathway. J Biochem 120:207–214. http://dx.doi.org/10.1093/oxfordjournals.jbchem.a021400.
  • Schwoebel ED. 1998. Ran-dependent signal-mediated nuclear import does not require GTP hydrolysis by Ran. J Biol Chem 273:35170–35175. http://dx.doi.org/10.1074/jbc.273.52.35170.
  • Ren M, Drivas G, D'Eustachio P, Rush MG. 1993. Ran/TC4: a small nuclear GTP-binding protein that regulates DNA synthesis. J Cell Biol 120:313–323. http://dx.doi.org/10.1083/jcb.120.2.313.
  • Renault L, Kuhlmann J, Henkel A, Wittinghofer A. 2001. Structural basis for guanine nucleotide exchange on Ran by the regulator of chromosome condensation (RCC1). Cell 105:245–255. http://dx.doi.org/10.1016/S0092-8674(01)00315-4.
  • Azuma Y, Renault L, Garcia-Ranea JA, Valencia A, Nishimoto T, Wittinghofer A. 1999. Model of the Ran-RCC1 interaction using biochemical and docking experiments. J Mol Biol 289:1119–1130. http://dx.doi.org/10.1006/jmbi.1999.2820.
  • Cushman I, Stenoien D, Moore MS. 2004. The dynamic association of RCC1 with chromatin is modulated by Ran-dependent nuclear transport. Mol Biol Cell 15:245–255. http://dx.doi.org/10.1091/mbc.E03-06-0409.
  • Görlich DD, Kutay UU. 1999. Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol 15:607–660. http://dx.doi.org/10.1146/annurev.cellbio.15.1.607.
  • Czubryt MP, Austria JA, Pierce GN. 2000. Hydrogen peroxide inhibition of nuclear protein import is mediated by the mitogen-activated protein kinase, ERK2. J Cell Biol 148:7–16. http://dx.doi.org/10.1083/jcb.148.1.7.
  • Kodiha M, Bański P, Stochaj U. 2009. Interplay between MEK and PI3 kinase signaling regulates the subcellular localization of protein kinases ERK1/2 and Akt upon oxidative stress. FEBS Lett 583:1987–1993. http://dx.doi.org/10.1016/j.febslet.2009.05.011.
  • Kosako H, Yamaguchi N, Aranami C, Ushiyama M, Kose S, Imamoto N, Taniguchi H, Nishida E, Hattori S. 2009. Phosphoproteomics reveals new ERK MAP kinase targets and links ERK to nucleoporin-mediated nuclear transport. Nat Struct Mol Biol 16:1026–1035. http://dx.doi.org/10.1038/nsmb.1656.
  • Tao G-Z, Zhou Q, Strnad P, Salemi MR, Lee YM, Omary MB. 2005. Human Ran cysteine 112 oxidation by pervanadate regulates its binding to keratins. J Biol Chem 280:12162–12167. http://dx.doi.org/10.1074/jbc.M412505200.
  • Ckless K, Reynaert NL, Taatjes DJ, Lounsbury KM. 2004. In situ detection and visualization of S-nitrosylated proteins following chemical derivatization: identification of Ran GTPase as a target for S-nitrosylation. Nitric Oxide 11:216–227. http://dx.doi.org/10.1016/j.niox.2004.06.002.
  • Reddie KG, Carroll KS. 2008. Expanding the functional diversity of proteins through cysteine oxidation. Curr Opin Chem Biol 12:746–754. http://dx.doi.org/10.1016/j.cbpa.2008.07.028.
  • Poole LB, Nelson KJ. 2008. Discovering mechanisms of signaling-mediated cysteine oxidation. Curr Opin Chem Biol 12:18–24. http://dx.doi.org/10.1016/j.cbpa.2008.01.021.
  • Hutchins J, Moore WJ, Hood FE, Wilson J, Andrews PD, Swedlow JR, Clarke PR. 2004. Phosphorylation regulates the dynamic interaction of RCC1 with chromosomes during mitosis. Curr Biol 14:1099–1104. http://dx.doi.org/10.1016/j.cub.2004.05.021.
  • Hood FE, Clarke PR. 2007. RCC1 isoforms differ in their affinity for chromatin, molecular interactions and regulation by phosphorylation. J Cell Sci 120:3436–3445. http://dx.doi.org/10.1242/jcs.009092.
  • Kodiha M, Rassi JG, Brown CM, Stochaj U. 2007. Localization of AMP kinase is regulated by stress, cell density, and signaling through the MEK→ERK1/2 pathway. Am J Physiol Cell Physiol 293:C1427–C1436. http://dx.doi.org/10.1152/ajpcell.00176.2007.
  • D'Angelo MA, Raices M, Panowski SH, Hetzer MW. 2009. Age-dependent deterioration of nuclear pore complexes causes a loss of nuclear integrity in postmitotic cells. Cell 136:284–295. http://dx.doi.org/10.1016/j.cell.2008.11.037.
  • Snow CJ, Dar A, Dutta A, Kehlenbach RH, Paschal BM. 2013. Defective nuclear import of Tpr in progeria reflects the Ran sensitivity of large cargo transport. J Cell Biol 201:541–557. http://dx.doi.org/10.1083/jcb.201212117.

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