The Nucleoporin Nup358/RanBP2 Promotes Nuclear Import in a Cargo- and Transport Receptor-Specific Manner

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Volumn 13, Issue 2, 2012, Pages 218-233

  Wälde, Sarah ^a,b   Thakar, Ketan ^a   Hutten, Saskia ^a,c   Spillner, Christiane ^a   Nath, Annegret ^a   Rothbauer, Ulrich ^d   Wiemann, Stefan ^e   Kehlenbach, Ralph H ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d UNIVERSITY OF MUNICH   (Germany)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

DBC 1; DMAP 1; NPC; Nuclear import; Nuclear pore complex; Nup358

Indexed keywords

CARRIER PROTEIN; CELL PROTEIN; DNA METHYLTRANSFERASE 1; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; KARYOPHERIN ALPHA; NUCLEOPORIN; NUP358 PROTEIN; SMALL INTERFERING RNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FRACTIONATION; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; DELETION MUTANT; ENZYME ACTIVITY; HUMAN; IMMOBILIZED CELL; IMMUNOFLUORESCENCE; NONHUMAN; NUCLEAR IMPORT; NUCLEAR PORE COMPLEX; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RNA INTERFERENCE; STRUCTURE ANALYSIS;

ACTIVE TRANSPORT, CELL NUCLEUS; ALPHA KARYOPHERINS; BETA KARYOPHERINS; CELL NUCLEUS; CYTOPLASM; DEAD-BOX RNA HELICASES; HELA CELLS; HUMANS; KARYOPHERINS; MOLECULAR CHAPERONES; NEOPLASM PROTEINS; NUCLEAR ENVELOPE; NUCLEAR LOCALIZATION SIGNALS; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; PEPTIDE FRAGMENTS; POINT MUTATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; REV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; RNA, SMALL INTERFERING; SEQUENCE DELETION; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS; UPSTREAM STIMULATORY FACTORS;

EID: 84855913415     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2011.01302.x     Document Type: Article

References (63)

1. Chadrin A, Hess B, San Roman M, Gatti X, Lombard B, Loew D, Barral Y, Palancade B, Doye V. Pom33, a novel transmembrane nucleoporin required for proper nuclear pore complex distribution. J Cell Biol 2010; 189: 795-811.
2. Gerace L, Ottaviano Y, Kondor-Koch C. Identification of a major polypeptide of the nuclear pore complex. J Cell Biol 1982; 95: 826-837.
3. Hallberg E, Wozniak RW, Blobel G. An integral membrane protein of the pore membrane domain of the nuclear envelope contains a nucleoporin-like region. J Cell Biol 1993; 122: 513-521.
4. Mansfeld J, Guttinger S, Hawryluk-Gara LA, Pante N, Mall M, Galy V, Haselmann U, Muhlhausser P, Wozniak RW, Mattaj IW, Kutay U, Antonin W. The conserved transmembrane nucleoporin NDC1 is required for nuclear pore complex assembly in vertebrate cells. Mol Cell 2006; 22: 93-103.
5. Stavru F, Hulsmann BB, Spang A, Hartmann E, Cordes VC, Görlich D. NDC1: a crucial membrane-integral nucleoporin of metazoan nuclear pore complexes. J Cell Biol 2006; 173: 509-519.
6. Brohawn SG, Partridge JR, Whittle JR, Schwartz TU. The nuclear pore complex has entered the atomic age. Structure 2009; 17: 1156-1168.
7. Terry LJ, Wente SR. Flexible gates: dynamic topologies and functions for FG nucleoporins in nucleocytoplasmic transport. Eukaryot Cell 2009; 8: 1814-1827.
8. Goldfarb DS. At loose ends: a guide to the translocation channel of the nuclear pore complex for dummies, In: Kehlenbach RH editor. Nuclear Transport. Austin, TX: Landes Bioscience; 2009:54-68.
9. Wälde S, Kehlenbach RH. The part and the whole: functions of nucleoporins in nucleocytoplasmic transport. Trends Cell Biol 2010; 20: 461-469.
10. Wente SR, Rout MP. The nuclear pore complex and nuclear transport. Cold Spring Harb Perspect Biol 2010; 2: a000562. doi: 10.1101/cshperspect.a000562. Epub 14 July 2010.
11. Rexach M, Blobel G. Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 1995; 83: 683-692.
12. Fried H, Kutay U. Nucleocytoplasmic transport: taking an inventory. Cell Mol Life Sci 2003; 60: 1659-1688.
13. Bernad R, Engelsma D, Sanderson H, Pickersgill H, Fornerod M. Nup214-Nup88 nucleoporin subcomplex is required for CRM1-mediated 60 S preribosomal nuclear export. J Biol Chem 2006; 281: 19378-19386.
14. Hutten S, Kehlenbach RH. Nup214 is required for CRM1-dependent nuclear protein export in vivo. Mol Cell Biol 2006; 26: 6772-6785.
15. Mahajan R, Delphin C, Guan T, Gerace L, Melchior F. A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 1997; 88: 97-107.
16. Matunis MJ, Wu J, Blobel G. SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex. J Cell Biol 1998; 140: 499-509.
17. Wu J, Matunis MJ, Kraemer D, Blobel G, Coutavas E. Nup358, a cytoplasmically exposed nucleoporin with peptide repeats, Ran-GTP binding sites, zinc fingers, a cyclophilin A homologous domain, and a leucine-rich region. J Biol Chem 1995; 270: 14209-14213.
18. Yokoyama N, Hayashi N, Seki T, Pante N, Ohba T, Nishii K, Kuma K, Hayashida T, Miyata T, Aebi U, Fukui M, Nishimoto T. A giant nucleopore protein that binds Ran/TC4. Nature 1995; 376: 184-188.
19. Pichler A, Gast A, Seeler JS, Dejean A, Melchior F. The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 2002; 108: 109-120.
20. Walther TC, Pickersgill HS, Cordes VC, Goldberg MW, Allen TD, Mattaj IW, Fornerod M. The cytoplasmic filaments of the nuclear pore complex are dispensable for selective nuclear protein import. J Cell Biol 2002; 158: 63-77.
21. Sabri N, Roth P, Xylourgidis N, Sadeghifar F, Adler J, Samakovlis C. Distinct functions of the Drosophila Nup153 and Nup214 FG domains in nuclear protein transport. J Cell Biol 2007; 178: 557-565.
22. Hutten S, Flotho A, Melchior F, Kehlenbach RH. The Nup358-RanGAP complex is required for efficient importin alpha/beta-dependent nuclear import. Mol Biol Cell 2008; 19: 2300-2310.
23. Hutten S, Wälde S, Spillner C, Hauber J, Kehlenbach RH. The nuclear pore component Nup358 promotes transportin-dependent nuclear import. J Cell Sci 2009; 122: 1100-1110.
24. Hamaguchi M, Meth JL, von Klitzing C, Wei W, Esposito D, Rodgers L, Walsh T, Welcsh P, King MC, Wigler MH. DBC2, a candidate for a tumor suppressor gene involved in breast cancer. Proc Natl Acad Sci U S A 2002; 99: 13647-13652.
25. Richardson AL, Wang ZC, De Nicolo A, Lu X, Brown M, Miron A, Liao X, Iglehart JD, Livingston DM, Ganesan S. X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell 2006; 9: 121-132.
26. Kim JE, Chen J, Lou Z. DBC1 is a negative regulator of SIRT1. Nature 2008; 451: 583-586.
27. Zhao W, Kruse JP, Tang Y, Jung SY, Qin J, Gu W. Negative regulation of the deacetylase SIRT1 by DBC1. Nature 2008; 451: 587-590.
28. Sundararajan R, Chen G, Mukherjee C, White E. Caspase-dependent processing activates the proapoptotic activity of deleted in breast cancer-1 during tumor necrosis factor-alpha-mediated death signaling. Oncogene 2005; 24: 4908-4920.
29. Trauernicht AM, Kim SJ, Kim NH, Boyer TG. Modulation of estrogen receptor alpha protein level and survival function by DBC-1. Mol Endocrinol 2007; 21: 1526-1536.
30. Fu J, Jiang J, Li J, Wang S, Shi G, Feng Q, White E, Qin J, Wong J. Deleted in breast cancer 1, a novel androgen receptor (AR) coactivator that promotes AR DNA-binding activity. J Biol Chem 2009; 284: 6832-6840.
31. Li Z, Chen L, Kabra N, Wang C, Fang J, Chen J. Inhibition of SUV39H1 methyltransferase activity by DBC1. J Biol Chem 2009; 284: 10361-10366.
32. Rountree MR, Bachman KE, Baylin SB. DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat Genet 2000; 25: 269-277.
33. Bannasch D, Mehrle A, Glatting KH, Pepperkok R, Poustka A, Wiemann S. LIFEdb: a database for functional genomics experiments integrating information from external sources, and serving as a sample tracking system. Nucleic Acids Res 2004; 32: D505-D508.
34. Wiemann S, Arlt D, Huber W, Wellenreuther R, Schleeger S, Mehrle A, Bechtel S, Sauermann M, Korf U, Pepperkok R, Sultmann H, Poustka A. From ORFeome to biology: a functional genomics pipeline. Genome Res 2004; 14: 2136-2144.
35. Reverter D, Lima CD. Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature 2005; 435: 687-692.
36. Starr DA. Communication between the cytoskeleton and the nuclear envelope to position the nucleus. Mol Biosyst 2007; 3: 583-589.
37. Grady RM, Starr DA, Ackerman GL, Sanes JR, Han M. Syne proteins anchor muscle nuclei at the neuromuscular junction. Proc Natl Acad Sci U S A 2005; 102: 4359-4364.
38. Love DC, Sweitzer TD, Hanover JA. Reconstitution of HIV-1 rev nuclear export: independent requirements for nuclear import and export. Proc Natl Acad Sci U S A 1998; 95: 10608-10613.
39. Saitoh H, Sparrow DB, Shiomi T, Pu RT, Nishimoto T, Mohun TJ, Dasso M. Ubc9p and the conjugation of SUMO-1 to RanGAP1 and RanBP2. Curr Biol 1998; 8: 121-124.
40. Rothbauer U, Zolghadr K, Muyldermans S, Schepers A, Cardoso MC, Leonhardt H. A versatile nanotrap for biochemical and functional studies with fluorescent fusion proteins. Mol Cell Proteomics 2008; 7: 282-289.
41. Klebe C, Bischoff FR, Ponstingl H, Wittinghofer A. Interaction of the nuclear GTP-binding protein Ran with its regulatory proteins RCC1 and RanGAP1. Biochemistry 1995; 34: 639-647.
42. Bernad R, van der Velde H, Fornerod M, Pickersgill H. Nup358/RanBP2 attaches to the nuclear pore complex via association with Nup88 and Nup214/CAN and plays a supporting role in CRM1-mediated nuclear protein export. Mol Cell Biol 2004; 24: 2373-2384.
43. Hamada M, Haeger A, Jeganathan KB, van Ree JH, Malureanu L, Wälde S, Joseph J, Kehlenbach RH, van Deursen JM. Ran-dependent docking of importin-{beta} to RanBP2/Nup358 filaments is essential for protein import and cell viability. J Cell Biol 2011; 194: 597-612.
44. Arnold M, Nath A, Hauber J, Kehlenbach RH. Multiple importins function as nuclear transport receptors for the Rev protein of human immunodeficiency virus type 1. J Biol Chem 2006; 281: 20883-20890.
45. Arnold M, Nath A, Wohlwend D, Kehlenbach RH. Transportin is a major nuclear import receptor for c-Fos: a novel mode of cargo interaction. J Biol Chem 2006; 281: 5492-5499.
46. Joseph J, Dasso M. The nucleoporin Nup358 associates with and regulates interphase microtubules. FEBS Lett 2008; 582: 190-196.
47. Melchior F, Schergaut M, Pichler A. SUMO: ligases, isopeptidases and nuclear pores. Trends Biochem Sci 2003; 28: 612-618.
48. Zhang X, Chen S, Yoo S, Chakrabarti S, Zhang T, Ke T, Oberti C, Yong SL, Fang F, Li L, de la Fuente R, Wang L, Chen Q, Wang QK. Mutation in nuclear pore component NUP155 leads to atrial fibrillation and early sudden cardiac death. Cell 2008; 135: 1017-1027.
49. Marg A, Shan Y, Meyer T, Meissner T, Brandenburg M, Vinkemeier U. Nucleocytoplasmic shuttling by nucleoporins Nup153 and Nup214 and CRM1-dependent nuclear export control the subcellular distribution of latent Stat1. J Cell Biol 2004; 165: 823-833.
50. Charneau P, Mirambeau G, Roux P, Paulous S, Buc H, Clavel F. HIV-1 reverse transcription. A termination step at the center of the genome. J Mol Biol 1994; 241: 651-662.
51. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. Current Protocols in Molecular Biology. New York: Greene Publishing Associates and Wiley-Interscience; 1994.
52. Gasteier JE, Madrid R, Krautkramer E, Schroder S, Muranyi W, Benichou S, Fackler OT. Activation of the Rac-binding partner FHOD1 induces actin stress fibers via a ROCK-dependent mechanism. J Biol Chem 2003; 278: 38902-38912.
53. Hu T, Guan T, Gerace L. Molecular and functional characterization of the p62 complex, an assembly of nuclear pore complex glycoproteins. J Cell Biol 1996; 134: 589-601.
54. Chi NC, Adam SA. Functional domains in nuclear import factor p97 for binding the nuclear localization sequence receptor and the nuclear pore. Mol Biol Cell 1997; 8: 945-956.
55. Baake M, Bauerle M, Doenecke D, Albig W. Core histones and linker histones are imported into the nucleus by different pathways. Eur J Cell Biol 2001; 80: 669-677.
56. Jäkel S, Görlich D. Importin beta, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J 1998; 17: 4491-4502.
57. Wohlwend D, Strasser A, Dickmanns A, Doenecke D, Ficner R. Thermodynamic analysis of H1 nuclear import: receptor tuning of importin beta/importin 7. J Biol Chem 2007; 282: 10707-10719.
58. Mühlhäusser P, Müller EC, Otto A, Kutay U. Multiple pathways contribute to nuclear import of core histones. EMBO Rep 2001; 2: 690-696.
59. Mingot JM, Kostka S, Kraft R, Hartmann E, Görlich D. Importin 13: a novel mediator of nuclear import and export. EMBO J 2001; 20: 3685-3694.
60. Melchior F, Sweet DJ, Gerace L. Analysis of Ran/TC4 function in nuclear protein import. Methods Enzymol 1995; 257: 279-291.
61. Holden P, Horton WA. Crude subcellular fractionation of cultured mammalian cell lines. BMC Res Notes 2009; 2: 243.
62. Kehlenbach RH, Dickmanns A, Kehlenbach A, Guan T, Gerace L. A role for RanBP1 in the release of CRM1 from the nuclear pore complex in a terminal step of nuclear export. J Cell Biol 1999; 145: 645-657.
63. Koizumi T, Negishi M, Nakamura S, Oguro H, Satoh K, Ichinose M, Iwama A. Depletion of Dnmt1-associated protein 1 triggers DNA damage and compromises the proliferative capacity of hematopoietic stem cells. Int J Hematol 2010; 91: 611-619.