Cryo-electron tomography provides novel insights into nuclear pore architecture: Implications for nucleocytoplasmic transport

Journal of Molecular Biology

Volumn 328, Issue 1, 2003, Pages 119-130

  Stoffler, Daniel ^a,c   Feja, Bernhard ^a,d   Fahrenkrog, Birthe ^a   Walz, Jochen ^b,e   Typke, Dieter ^b   Aebi, Ueli ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d Tietz Video/Image Proc Systems GmbH   (Germany)

^e SIEMENS AG   (Germany)

Author keywords

3 D reconstruction; Cryo electron microscopy; Electron tomography; Nuclear pore complex; Nucleocytoplasmic transport

Indexed keywords

ANIMAL CELL; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CYTOPLASM; NONHUMAN; NUCLEAR PORE; NUCLEOCYTOPLASMIC TRANSPORT; OOCYTE; PRIORITY JOURNAL; TOMOGRAPHY; XENOPUS;

NES;

EID: 0037453221     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00266-3     Document Type: Article

References (50)

1. Görlich D., Kutay U. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 15:1999;607-660.
2. Reichelt R., Holzenburg A., Buhle E.L. Jr, Jarnik M., Engel A., Aebi U. Correlation between structure and mass distribution of the nuclear pore complex and of distinct pore complex components. J. Cell Biol. 110:1990;883-894.
3. Jarnik M., Aebi U. Towards a 3-D model of the nuclear pore complex. J. Struct. Biol. 107:1991;291-308.
4. Hinshaw J.E., Carragher B.O., Milligan R.A. Architecture and design of the nuclear pore complex. Cell. 69:1992;1133-1141.
5. Akey C.W., Radermacher M. Architecture of the Xenopus nuclear pore complex revealed by 3-dimensional cryo-electron microscopy. J. Cell Biol. 122:1993;1-19.
6. Goldberg M.W., Wiese C., Allen T.D., Wilson K.L. Dimples, pores, star-rings, and thin rings on growing nuclear envelopes: evidence for structural intermediates in nuclear pore complex assembly. J. Cell Sci. 110:1997;409-420.
7. Stoffler D., Fahrenkrog B., Aebi U. The nuclear pore complex: from molecular architecture to functional dynamics. Curr. Opin. Cell Biol. 11:1999;391-401.
8. Fahrenkrog B., Aebi U. The vertebrate nuclear pore complex: from structure to function. Res. Probl. Cell Diff. 35:2002;25-48.
9. Kiseleva E., Goldberg M.W., Allen T.D., Akey C.W. Active nuclear pore complexes in Chironomus: visualization of transporter configurations related to mRNP export. J. Cell Sci. 111:1998;223-236.
10. Stoffler D., Goldie K.N., Feja B., Aebi U. Calcium-mediated structural changes of native nuclear pore complexes monitored by time-lapse atomic force microscopy. J. Mol. Biol. 287:1999;741-752.
11. Yang Q., Rout M.P., Akey C.W. Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications. Mol. Cell. 1:1998;223-234.
12. Rout M.P., Blobel G. Isolation of the yeast nuclear pore complex. J. Cell Biol. 123:1993;771-783.
13. Fahrenkrog B., Hurt E.C., Aebi U., Panté N. Molecular architecture of the yeast nuclear pore complex: localization of Nsp1p subcomplexes. J. Cell Biol. 143:1998;577-588.
14. Akey C.W. Structural plasticity of the nuclear pore complex. J. Mol. Biol. 248:1995;273-293.
15. Panté N., Aebi U. Molecular dissection of the nuclear pore complex. Crit. Rev. Biochem. Mol. Biol. 31:1996;153-199.
16. Feja B., Aebi U. Determination of the inelastic mean free path of electrons in vitrified ice layers for on-line thickness measurements by zero loss imaging. J. Microsc. 193:1999;15-19.
17. Grimm R., Bärmann M., Hackl W., Typke D., Sackmann E., Baumeister W. Energy filtered electron tomography of ice-embedded actin and vesicles. Biophys. J. 72:1997;482-489.
18. Cordes V.C., Reidenbach S., Rackwitz H.R., Franke W.W. Identification of protein p270/Tpr as a constitutive component of the nuclear pore complex-attached intranuclear filaments. J. Cell Biol. 136:1997;515-529.
19. Panté N., Aebi U. Sequential binding of import ligands to distinct nucleopore regions during their nuclear import. Science. 273:1996;1729-1732.
20. Akey C.W. Interactions and structure of the nuclear pore complex revealed by cryo-electron microscopy. J. Cell Biol. 109:1989;955-970.
21. Greber U.F., Senior A., Gerace L. A major glycoprotein of the nuclear pore complex is a membrane-spanning polypeptide with a large lumenal domain and a small cytoplasmic tail. EMBO J. 9:1990;1495-1502.
22. Soullan B., Worman H.J. The amino-terminal domain of the lamin B receptor is a nuclear envelope targeting signal. J. Cell Biol. 120:1993;1093-1100.
23. Danker T., Schillers H., Storck J., Shahin V., Krämer B., Wilhelmi M., Oberleithner H. Nuclear hourglass technique: an approach that detects electrically open nuclear pores in Xenopus laevis oocyte. Proc. Natl Acad. Sci. USA. 96:1999;13530-13535.
24. Feldherr C., Akin D. The location of the transport gate in the nuclear pore complex. J. Cell Sci. 110:1997;3065-3070.
25. Keminer O., Siebrasse J.P., Zerf K., Peters R. Optical recording of signal-mediated protein transport through single nuclear pore complexes. Proc. Natl Acad. Sci. USA. 96:1999;11842-11847.
26. Rakowska A., Danker T., Schneider S.W., Oberleithner H. ATP-induced shape changes of nuclear pores visualized with the atomic force microscope. J. Membr. Biol. 163:1998;129-136.
27. Goldberg M.W., Allen T.D. High resolution scanning electron microscopy of the nuclear envelope: demonstration of a new, regular, fibrous lattice attached to the baskets of the nucleoplasmic face of the nuclear pores. J. Cell Biol. 119:1992;1429-1440.
28. Cordes V.C., Reidenbach S., Kohler A., Stuurman N., van Driel R., Franke W.W. Intranuclear filaments containing a nuclear pore complex protein. J. Cell Biol. 123:1993;1333-1344.
29. Rout M.P., Aitchison J.D., Suprapto A., Hjertaas K., Zhao Y., Chait B.T. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J. Cell Biol. 148:2000;635-651.
30. Panté N., Jarmolowski A., Baschong W., Sauder U., Izaurralde E., Mattaj I.W. Nuclear export of different types of RNA. RNA. 3:1997;498-513.
31. Kiseleva E., Visa N., Wurtz T., Daneholt B. Immunocytochemical evidence for a stepwise assembly of Balbiani ring premessenger ribonucleoprotein particles. Eur. J. Cell Biol. 74:1997;407-416.
32. Panté N., Kann M. The nuclear pore complex is able to transport macromolecules with diameters of about 39 nm. Mol. Biol. Cell. 13:2002;425-434.
33. Paine P.I., Moore L.C., Horwitz S.B. Nuclear envelope permeability. Nature. 254:1975;109-114.
34. Ribbeck K., Görlich D. Kinetic analysis of translocation through nuclear pore complexes. EMBO J. 20:2001;1320-1330.
35. Fahrenkrog B., Maco B., Fager A., Köser J., Sauder U., Ullman K.S., Aebi U. Domain specific antibodies reveal multiple-site topology of Nup153 within the nuclear pore complex. J. Struct. Biol. 140:2002;254-267.
36. Panté N., Bastos R., McMorrow I., Burke B., Aebi U. Interactions and three-dimensional localization of a group of nuclear pore complex proteins. J. Cell Biol. 126:1994;603-617.
37. Walther T.C., Fornerod M., Pickersgill H., Goldberg M., Allen T.D., Mattaj I.W. The nucleoporin Nup153 is required for nuclear pore basket formation, nuclear pore complex anchoring and import of a subset of nuclear proteins. EMBO J. 20:2001;5703-5714.
38. Shah S., Tugendreich S., Forbes D. Major binding sites for the nuclear import receptor are the internal nucleoporin Nup153 and the adjacent nuclear filament protein Tpr. J. Cell Biol. 141:1998;31-49.
39. Ben-Efraim I., Gerace L. Gradient of increasing affinity of importin beta for nucleoporins along the pathway of nuclear import. J. Cell Biol. 152:2001;411-418.
40. Fukami A., Adachi K. A new method of preparation of a self-perforated micro plastic grid and its application. J. Electron Microsc. 14:1965;112-118.
41. Malis T., Cheng S.C., Egerton R.F. EELS Log-Ratio technique for specimen-thickness measurement in the TEM. J. Electron Microsc. Tech. 8:1988;193-200.
42. Dierksen K., Typke D., Hegerl A., Koster A.J., Baumeister W. Toward automatic electron tomography. Ultramicroscopy. 40:1992;71-87.
43. Dierksen K., Typke D., Hegerl A., Baumeister W. Toward automatic electron tomography. II. Implementation of autofocus and low-dose procedures. Ultramicroscopy. 49:1993;109-120.
44. Koster A.J., Chen H., Sedat J.W., Agard D.A. Automated microscopy for electron tomography. Ultramicroscopy. 46:1992;207-227.
45. Koster A.J., Grimm R., Typke D., Hegerl R., Stoschek A., Walz J., Baumeister W. Perspectives of molecular and cellular electron tomography. J. Struct. Biol. 120:1997;276-308.
46. Grimm R., Sigh H., Rachel R., Typke D., Zillig W., Baumeister W. Energy filtered electron tomography of ice-embedded prokaryotic cells. Biophys. J. 74:1998;1031-1042.
47. Saxton W.O., Pitt T.J., Horner M. Digital image processing: the Semper system. Ultramicroscopy. 4:1979;343-354.
48. Hegerl R. The EM program package: a platform for image processing in biological electron microscopy. J. Struct. Biol. 116:1996;30-34.
49. Walz J., Typke D., Nitsch M., Koster A.J., Hegerl R., Baumeister W. Electron tomography of single ice-embedded macromolecules: three-dimensional alignment and classification. J. Struct. Biol. 120:1997;387-395.
50. Sheehan B., Fuller S.D., Pique M.E., Yeager M. AVS software for visualization in molecular microscopy. J. Struct. Biol. 116:1996;99-106.