Nuclear distributions of NUP62 and NUP214 suggest architectural diversity and spatial patterning among nuclear pore complexes

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Kinoshita, Yayoi ^a   Kalir, Tamara ^a   Dottino, Peter ^a   Kohtz, D Stave ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOPORIN; NUCLEOPORIN 214; NUCLEOPORIN P62; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; NUCLEAR PORE PROTEIN P62; NUP214 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ANTIBODY LABELING; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CHROMATIN; CHROMOSOME; CONTROLLED STUDY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; INTERPHASE; NUCLEAR PORE COMPLEX; PROTEIN DOMAIN; PROTEIN LOCALIZATION; CELL COMPARTMENTALIZATION; CELL COUNT; FEMALE; FLUORESCENCE MICROSCOPY; GENE SILENCING; METABOLISM; NUCLEAR PORE; NUCLEAR SHAPE; OVARY TUMOR; PROTEIN TRANSPORT; STAINING; TUMOR CELL LINE;

CELL COMPARTMENTATION; CELL COUNT; CELL LINE, TUMOR; CELL NUCLEUS SHAPE; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; MEMBRANE GLYCOPROTEINS; MICROSCOPY, FLUORESCENCE; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; OVARIAN NEOPLASMS; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; STAINING AND LABELING; TRANSFECTION;

EID: 84860491229     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036137     Document Type: Article

References (64)

1. Schwartz TU, (2005) Modularity within the architecture of the nuclear pore complex. Curr Opin Struct Biol 15: 221-226.
2. Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, et al. (2007) The molecular architecture of the nuclear pore complex. Nature 450: 695-701.
3. Lim RY, Fahrenkrog B, (2006) The nuclear pore complex up close. Curr Opin Cell Biol 18: 342-347.
4. Lim RY, Ullman KS, Fahrenkrog B, (2008) Biology and biophysics of the nuclear pore complex and its components. Int Rev Cell Mol Biol 267: 299-342.
5. Gillespie PJ, Khoudoli GA, Stewart G, Swedlow JR, Blow JJ, (2007) ELYS/MEL-28 chromatin association coordinates nuclear pore complex assembly and replication licensing. Curr Biol 17: 1657-1662.
6. Rasala BA, Ramos C, Harel A, Forbes DJ, (2008) Capture of AT-rich chromatin by ELYS recruits POM121 and NDC1 to initiate nuclear pore assembly. Mol Biol Cell 19: 3982-3996.
7. Stavru F, Nautrup-Pedersen G, Cordes VC, Gorlich D, (2006) Nuclear pore complex assembly and maintenance in POM121- and gp210-deficient cells. J Cell Biol 173: 477-483.
8. Stavru F, Hulsmann BB, Spang A, Hartmann E, Cordes VC, et al. (2006) NDC1: a crucial membrane-integral nucleoporin of metazoan nuclear pore complexes. J Cell Biol 173: 509-519.
9. Rayala HJ, Kendirgi F, Barry DM, Majerus PW, Wente SR, (2004) The mRNA export factor human Gle1 interacts with the nuclear pore complex protein Nup155. Mol Cell Proteomics 3: 145-155.
10. Kendirgi F, Rexer DJ, Alcazar-Roman AR, Onishko HM, Wente SR, (2005) Interaction between the shuttling mRNA export factor Gle1 and the nucleoporin hCG1: a conserved mechanism in the export of Hsp70 mRNA. Mol Biol Cell 16: 4304-4315.
11. Hawryluk-Gara LA, Shibuya EK, Wozniak RW, (2005) Vertebrate Nup53 interacts with the nuclear lamina and is required for the assembly of a Nup93-containing complex. Mol Biol Cell 16: 2382-2394.
12. Fontoura BM, Blobel G, Matunis MJ, (1999) A conserved biogenesis pathway for nucleoporins: proteolytic processing of a 186-kilodalton precursor generates Nup98 and the novel nucleoporin, Nup96. J Cell Biol 144: 1097-1112.
13. Griffis ER, Xu S, Powers MA, (2003) Nup98 localizes to both nuclear and cytoplasmic sides of the nuclear pore and binds to two distinct nucleoporin subcomplexes. Mol Biol Cell 14: 600-610.
14. Krull S, Thyberg J, Bjorkroth B, Rackwitz HR, Cordes VC, (2004) Nucleoporins as components of the nuclear pore complex core structure and Tpr as the architectural element of the nuclear basket. Mol Biol Cell 15: 4261-4277.
15. Hu T, Guan T, Gerace L, (1996) Molecular and functional characterization of the p62 complex, an assembly of nuclear pore complex glycoproteins. J Cell Biol 134: 589-601.
16. Guan T, Muller S, Klier G, Pante N, Blevitt JM, et al. (1995) Structural analysis of the p62 complex, an assembly of O-linked glycoproteins that localizes near the central gated channel of the nuclear pore complex. Mol Biol Cell 6: 1591-1603.
17. Kraemer D, Wozniak RW, Blobel G, Radu A, (1994) The human CAN protein, a putative oncogene product associated with myeloid leukemogenesis, is a nuclear pore complex protein that faces the cytoplasm. Proc Natl Acad Sci U S A 91: 1519-1523.
18. Fornerod M, van Deursen J, van Baal S, Reynolds A, Davis D, et al. (1997) The human homologue of yeast CRM1 is in a dynamic subcomplex with CAN/Nup214 and a novel nuclear pore component Nup88. Embo J 16: 807-816.
19. Wu X, Kasper LH, Mantcheva RT, Mantchev GT, Springett MJ, et al. (2001) Disruption of the FG nucleoporin NUP98 causes selective changes in nuclear pore complex stoichiometry and function. Proc Natl Acad Sci U S A 98: 3191-3196.
20. Fahrenkrog B, Maco B, Fager AM, Koser J, Sauder U, et al. (2002) Domain-specific antibodies reveal multiple-site topology of Nup153 within the nuclear pore complex. J Struct Biol 140: 254-267.
21. Hutten S, Walde S, Spillner C, Hauber J, Kehlenbach RH, (2009) The nuclear pore component Nup358 promotes transportin-dependent nuclear import. J Cell Sci 122: 1100-1110.
22. Cole CN, Scarcelli JJ, (2006) Transport of messenger RNA from the nucleus to the cytoplasm. Curr Opin Cell Biol 18: 299-306.
23. Kelly SM, Corbett AH, (2009) Messenger RNA export from the nucleus: a series of molecular wardrobe changes. Traffic 10: 1199-1208.
24. Yasuhara N, Oka M, Yoneda Y, (2009) The role of the nuclear transport system in cell differentiation. Semin Cell Dev Biol 20: 590-599.
25. Terry LJ, Shows EB, Wente SR, (2007) Crossing the nuclear envelope: hierarchical regulation of nucleocytoplasmic transport. Science 318: 1412-1416.
26. Steggerda SM, Paschal BM, (2002) Regulation of nuclear import and export by the GTPase Ran. Int Rev Cytol 217: 41-91.
27. Braun IC, Herold A, Rode M, Izaurralde E, (2002) Nuclear export of mRNA by TAP/NXF1 requires two nucleoporin-binding sites but not p15. Mol Cell Biol 22: 5405-5418.
28. Terry LJ, Wente SR, (2007) Nuclear mRNA export requires specific FG nucleoporins for translocation through the nuclear pore complex. J Cell Biol 178: 1121-1132.
29. Sabri N, Roth P, Xylourgidis N, Sadeghifar F, Adler J, et al. (2007) Distinct functions of the Drosophila Nup153 and Nup214 FG domains in nuclear protein transport. J Cell Biol 178: 557-565.
30. Kalverda B, Pickersgill H, Shloma VV, Fornerod M, (2010) Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm. Cell 140: 360-371.
31. Capelson M, Liang Y, Schulte R, Mair W, Wagner U, et al. (2010) Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell 140: 372-383.
32. Paulillo SM, Phillips EM, Koser J, Sauder U, Ullman KS, et al. (2005) Nucleoporin domain topology is linked to the transport status of the nuclear pore complex. J Mol Biol 351: 784-798.
33. Paulillo SM, Powers MA, Ullman KS, Fahrenkrog B, (2006) Changes in nucleoporin domain topology in response to chemical effectors. J Mol Biol 363: 39-50.
34. Belgareh N, Snay-Hodge C, Pasteau F, Dagher S, Cole CN, et al. (1998) Functional characterization of a Nup159p-containing nuclear pore subcomplex. Mol Biol Cell 9: 3475-3492.
35. Bernad R, van der Velde H, Fornerod M, Pickersgill H, (2004) 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 24: 2373-2384.
36. Stochaj U, Banski P, Kodiha M, Matusiewicz N, (2006) The N-terminal domain of the mammalian nucleoporin p62 interacts with other nucleoporins of the FXFG family during interphase. Exp Cell Res 312: 2490-2499.
37. van Deursen J, Boer J, Kasper L, Grosveld G, (1996) G2 arrest and impaired nucleocytoplasmic transport in mouse embryos lacking the proto-oncogene CAN/Nup214. Embo J 15: 5574-5583.
38. Walther TC, Alves A, Pickersgill H, Loiodice I, Hetzer M, et al. (2003) The conserved Nup107-160 complex is critical for nuclear pore complex assembly. Cell 113: 195-206.
39. Liu HL, De Souza CP, Osmani AH, Osmani SA, (2009) The three fungal transmembrane nuclear pore complex proteins of Aspergillus nidulans are dispensable in the presence of an intact An-Nup84-120 complex. Mol Biol Cell 20: 616-630.
40. Kalverda B, Fornerod M, (2007) The nuclear life of nucleoporins. Dev Cell 13: 164-165.
41. Provencher DM, Lounis H, Champoux L, Tetrault M, Manderson EN, et al. (2000) Characterization of four novel epithelial ovarian cancer cell lines. In Vitro Cell Dev Biol Anim 36: 357-361.
42. Kinoshita Y, Kalir T, Rahaman J, Dottino P, Kohtz DS, (2012) Alterations in nuclear pore architecture allow cancer cell entry into or exit from drug-resistant dormancy. Am J Pathol 180: 375-389.
43. Suzuki K, Bose P, Leong-Quong RY, Fujita DJ, Riabowol K, (2010) REAP: A two minute cell fractionation method. BMC Res Notes 3: 294.
44. Onischenko EA, Gubanova NV, Kieselbach T, Kiseleva EV, Hallberg E, (2004) Annulate lamellae play only a minor role in the storage of excess nucleoporins in Drosophila embryos. Traffic 5: 152-164.
45. Napetschnig J, Kassube SA, Debler EW, Wong RW, Blobel G, et al. (2009) Structural and functional analysis of the interaction between the nucleoporin Nup214 and the DEAD-box helicase Ddx19. Proc Natl Acad Sci U S A 106: 3089-3094.
46. Pante N, Aebi U, (1996) Molecular dissection of the nuclear pore complex. Crit Rev Biochem Mol Biol 31: 153-199.
47. Lyman SK, Gerace L, (2001) Nuclear pore complexes: dynamics in unexpected places. J Cell Biol 154: 17-20.
48. Davis LI, Blobel G, (1987) Nuclear pore complex contains a family of glycoproteins that includes p62: glycosylation through a previously unidentified cellular pathway. Proc Natl Acad Sci U S A 84: 7552-7556.
49. Hanover JA, Cohen CK, Willingham MC, Park MK, (1987) O-linked N-acetylglucosamine is attached to proteins of the nuclear pore. Evidence for cytoplasmic and nucleoplasmic glycoproteins. J Biol Chem 262: 9887-9894.
50. Pante N, Bastos R, McMorrow I, Burke B, Aebi U, (1994) Interactions and three-dimensional localization of a group of nuclear pore complex proteins. J Cell Biol 126: 603-617.
51. Favreau C, Worman HJ, Wozniak RW, Frappier T, Courvalin JC, (1996) Cell cycle-dependent phosphorylation of nucleoporins and nuclear pore membrane protein Gp210. Biochemistry 35: 8035-8044.
52. Porter FW, Palmenberg AC, (2009) Leader-induced phosphorylation of nucleoporins correlates with nuclear trafficking inhibition by cardioviruses. J Virol 83: 1941-1951.
53. Porter FW, Brown B, Palmenberg AC, (2010) Nucleoporin phosphorylation triggered by the encephalomyocarditis virus leader protein is mediated by mitogen-activated protein kinases. J Virol 84: 12538-12548.
54. Schermelleh L, Carlton PM, Haase S, Shao L, Winoto L, et al. (2008) Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 320: 1332-1336.
55. Towbin BD, Meister P, Gasser SM, (2009) The nuclear envelope-a scaffold for silencing? Curr Opin Genet Dev 19: 180-186.
56. Meister P, Towbin BD, Pike BL, Ponti A, Gasser SM, (2010) The spatial dynamics of tissue-specific promoters during C. elegans development. Genes Dev 24: 766-782.
57. Roth P, Xylourgidis N, Sabri N, Uv A, Fornerod M, et al. (2003) The Drosophila nucleoporin DNup88 localizes DNup214 and CRM1 on the nuclear envelope and attenuates NES-mediated nuclear export. J Cell Biol 163: 701-706.
58. Xylourgidis N, Roth P, Sabri N, Tsarouhas V, Samakovlis C, (2006) The nucleoporin Nup214 sequesters CRM1 at the nuclear rim and modulates NFkappaB activation in Drosophila. J Cell Sci 119: 4409-4419.
59. Leng Y, Cao C, Ren J, Huang L, Chen D, et al. (2007) Nuclear import of the MUC1-C oncoprotein is mediated by nucleoporin Nup62. J Biol Chem 282: 19321-19330.
60. Echeverria PC, Mazaira G, Erlejman A, Gomez-Sanchez C, Piwien Pilipuk G, et al. (2009) Nuclear import of the glucocorticoid receptor-hsp90 complex through the nuclear pore complex is mediated by its interaction with Nup62 and importin beta. Mol Cell Biol 29: 4788-4797.
61. Ahmed S, Brickner JH, (2007) Regulation and epigenetic control of transcription at the nuclear periphery. Trends Genet 23: 396-402.
62. Bernad R, Engelsma D, Sanderson H, Pickersgill H, Fornerod M, (2006) Nup214-Nup88 nucleoporin subcomplex is required for CRM1-mediated 60 S preribosomal nuclear export. J Biol Chem 281: 19378-19386.
63. Biedler JL, Roffler-Tarlov S, Schachner M, Freedman LS, (1978) Multiple neurotransmitter synthesis by human neuroblastoma cell lines and clones. Cancer Res 38: 3751-3757.
64. Maeshima K, Yahata K, Sasaki Y, Nakatomi R, Tachibana T, et al. (2006) Cell-cycle-dependent dynamics of nuclear pores: pore-free islands and lamins. J Cell Sci 119: 4442-4451.