Size-dependent leak of soluble and membrane proteins through the yeast nuclear pore complex

Molecular Biology of the Cell

Volumn 26, Issue 7, 2015, Pages 1386-1394

  Popken, Petra ^a,b,c   Ghavami, Ali ^b   Onck, Patrick R ^b   Poolman, Bert ^b,c   Veenhoff, Liesbeth M ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; IN VIVO STUDY; MOLECULAR DYNAMICS; MOLECULAR SIZE; NONHUMAN; NUCLEAR PORE COMPLEX; PERMEABILITY; PERMEABILITY BARRIER; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SIMULATION; SURFACE PROPERTY; YEAST CELL; DIFFUSION; METABOLISM; NUCLEAR PORE; PROTEIN TRANSPORT;

SACCHAROMYCES CEREVISIAE;

DIFFUSION; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MOLECULAR DYNAMICS SIMULATION; NUCLEAR PORE; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE;

EID: 84926443404     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-07-1175     Document Type: Article

References (55)

1. Adams R, Wente S (2013). Uncovering nuclear pore complexity with innovation. Cell 152, 1218-1221.
2. Aitchison J, Rout M (2012). The yeast nuclear pore complex and transport through it. Genetics 190, 855-883.
3. Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT, et al. (2007). The molecular architecture of the nuclear pore complex. Nature 450, 695-701.
4. Beetz C, Brodhun M, Moutzouris K, Kiehntopf M, Berndt A, Lehnert D, Deufel T, Bastmeyer M, Schickel J (2004). Identification of nuclear localisation sequences in spastin (SPG4) using a novel Tetra-GFP reporter system. Biochem Biophys Res Commun 318, 1079-1084.
5. Chatterjee S, Javier M, Stochaj U (1997). In vivo analysis of nuclear protein traffic in mammalian cells. Exp Cell Res 236, 346-350.
6. Chellappa R, Kandasamy P, Oh C, Jiang Y, Vemula M, Martin C (2001). The membrane proteins, Spt23p and Mga2p, play distinct roles in the activation of Saccharomyces cerevisiae OLE1 gene expression. Fatty acid-mediated regulation of Mga2p activity is independent of its proteolytic processing into a soluble transcription activator. J Biol Chem 276, 43548-43556.
7. Colwell L, Brenner M, Ribbeck K (2010). Charge as a selection criterion for translocation through the nuclear pore complex. PLoS Comput Biol 6, e1000747.
8. Corbett A, Koepp D, Schlenstedt G, Lee M, Hopper A, Silver P (1995). Rna1p, a Ran/TC4 GTPase activating protein, is required for nuclear import. J Cell Biol 130, 1017-1026.
9. D'Angelo M, Raices M, Panowski S, Hetzer M (2009). Age-dependent deterioration of nuclear pore complexes causes a loss of nuclear integrity in postmitotic cells. Cell 136, 284-295.
10. Deng M, Hochstrasser M (2006). Spatially regulated ubiquitin ligation by an ER/nuclear membrane ligase. Nature 443, 827-831.
11. Ellenberg J, Siggia E, Moreira J, Smith C, Presley J, Worman H, Lippincott-Schwartz J (1997). Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis. J Cell Biol 138, 1193-1206.
12. Fiserova J, Richards S, Wente S, Goldberg M (2010). Facilitated transport and diffusion take distinct spatial routes through the nuclear pore complex. J Cell Sci 123, 2773-2780.
13. Forrester W, Stutz F, Rosbash M, Wickens M (1992). Defects in mRNA 3′-end formation, transcription initiation, and mRNA transport associated with the yeast mutation prp20: possible coupling of mRNA processing and chromatin structure. Genes Dev 6, 1914-1926.
14. Frey S, Richter R, Görlich D (2006). FG-rich repeats of nuclear pore proteins form a three-dimensional meshwork with hydrogel-like properties. Science 314, 815-817.
15. Gardner J, Smoyer C, Stensrud E, Alexander R, Gogol M, Wiegraebe W, Jaspersen S (2011). Targeting of the SUN protein Mps3 to the inner nuclear membrane by the histone variant H2A.Z. J Cell Biol 193, 489-507.
16. Geertsma ER, Groeneveld M, Slotboom D, Poolman B (2008). Quality control of overexpressed membrane proteins. Proc Natl Acad Sci USA 105, 5722-5727.
17. Ghavami A, Veenhoff L, van der Giessen E, Onck P (2014). Probing the disordered domain of the nuclear pore complex through coarse-grained molecular dynamics simulations. Biophys J 107, 1393-1402.
18. Haruki H, Nishikawa J, Laemmli U (2008). The anchor-away technique: rapid, conditional establishment of yeast mutant phenotypes. Mol Cell 31, 925-932.
19. Heessen S, Fornerod M (2007). The inner nuclear envelope as a transcription factor resting place. EMBO Rep 8, 914-919.
20. Hinshaw J, Carragher B, Milligan R (1992). Architecture and design of the nuclear pore complex. Cell 69, 1133-1141.
21. Huh W, Falvo J, Gerke L, Carroll A, Howson R, Weissman J, O'Shea E (2003). Global analysis of protein localization in budding yeast. Nature 425, 686-691.
22. Hülsmann B, Labokha A, Görlich D (2012). The permeability of reconstituted nuclear pores provides direct evidence for the selective phase model. Cell 150, 738-751.
23. Iovine M, Wente S (1997). A nuclear export signal in Kap95p is required for both recycling the import factor and interaction with the nucleoporin GLFG repeat regions of Nup116p and Nup100p. J Cell Biol 137, 797-811.
24. Katta S, Smoyer C, Jaspersen S (2013). Destination: inner nuclear membrane. Trends Cell Biol 24, 221-229.
25. Kim S, Elbaum M (2013). A simple kinetic model with explicit predictions for nuclear transport. Biophys J 105, 565-569.
26. King M, Lusk C, Blobel G (2006). Karyopherin-mediated import of integral inner nuclear membrane proteins. Nature 442, 1003-1007.
27. Kopito RB, Elbaum M (2007). Reversibility in nucleocytoplasmic transport. Proc Natl Acad Sci USA 104, 12743-12748.
28. Laba J, Steen A, Veenhoff L (2014). Traffic to the inner membrane of the nuclear envelope. Curr Opin Cell Biol 28, 36-45.
29. Lénárt P, Ellenberg J (2006). Monitoring the permeability of the nuclear envelope during the cell cycle. Methods 38, 17-24.
30. Ma J, Goryaynov A, Sarma A, Yang W (2012). Self-regulated viscous channel in the nuclear pore complex. Proc Natl Acad Sci USA 109, 7326-7331.
31. Maimon T, Elad N, Dahan I, Medalia O (2012). The human nuclear pore complex as revealed by cryo-electron tomography. Structure 20, 998-1006.
32. Meinema A, Laba J, Hapsari R, Otten R, Mulder FA, Kralt A, van den Bogaart G, Lusk C, Poolman B, Veenhoff L (2011). Long unfolded linkers facilitate membrane protein import through the nuclear pore complex. Science 333, 90-93.
33. Meinema A, Poolman B, Veenhoff L (2013). Quantitative analysis of membrane protein transport across the nuclear pore complex. Traffic 14, 487-501.
34. Mohr D, Frey S, Fischer T, Güttler T, Görlich D (2009). Characterisation of the passive permeability barrier of nuclear pore complexes. EMBO J 28, 2541-2553.
35. Naim B, Zbaida D, Dagan S, Kapon R, Reich Z (2009). Cargo surface hydrophobicity is sufficient to overcome the nuclear pore complex selectivity barrier. EMBO J 28, 2697-2705.
36. Ohba T, Schirmer E, Nishimoto T, Gerace L (2004). Energy- and temperature-dependent transport of integral proteins to the inner nuclear membrane via the nuclear pore. J Cell Biol 167, 1051-1062.
37. Patel S, Belmont B, Sante J, Rexach M (2007). Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell 129, 83-96.
38. Radu A, Moore M, Blobel G (1995). The peptide repeat domain of nucleoporin Nup98 functions as a docking site in transport across the nuclear pore complex. Cell 81, 215-222.
39. Rexach M, Blobel G (1995). Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 83, 683-692.
40. Ribbeck K, Görlich D (2002). The permeability barrier of nuclear pore complexes appears to operate via hydrophobic exclusion. EMBO J 21, 2664-2671.
41. Rout M, Aitchison J, Suprapto A, Hjertaas K, Zhao Y, Chait B (2000). The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol 148, 635-651.
42. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat Methods 9, 676-682.
43. Schlenstedt G, Saavedra C, Loeb J, Cole C, Silver P (1995). The GTP-bound form of the yeast Ran/TC4 homologue blocks nuclear protein import and appearance of poly(A)+ RNA in the cytoplasm. Proc Natl Acad Sci USA 92, 225-229.
44. Seibel N, Eljouni J, Nalaskowski M, Hampe W (2007). Nuclear localization of enhanced green fluorescent protein homomultimers. Anal Biochem 368, 95-99.
45. Shulga N, Goldfarb D (2003). Binding dynamics of structural nucleoporins govern nuclear pore complex permeability and may mediate channel gating. Mol Cell Biol 23, 534-542.
46. Shulga N, Mosammaparast N, Wozniak R, Goldfarb DS (2000). Yeast nucleoporins involved in passive nuclear envelope permeability. J Cell Biol 149, 1027-1038.
47. Soullam B, Worman H (1995). Signals and structural features involved in integral membrane protein targeting to the inner nuclear membrane. J Cell Biol 130, 15-27.
48. Strawn L, Shen T, Shulga N, Goldfarb D, Wente S (2004). Minimal nuclear pore complexes define FG repeat domains essential for transport. Nat Cell Biol 6, 197-206.
49. Terry L, Wente S (2009). Flexible gates: dynamic topologies and functions for FG nucleoporins in nucleocytoplasmic transport. Eukaryotic Cell 8, 1814-1827.
50. Turgay Y, Ungricht R, Rothballer A, Kiss A, Csucs G, Horvath P, Kutay U (2010). A classical NLS and the SUN domain contribute to the targeting of SUN2 to the inner nuclear membrane. EMBO J 29, 2262-2275.
51. Wang R, Brattain M (2007). The maximal size of protein to diffuse through the nuclear pore is larger than 60kDa. FEBS Lett 581, 3164-3170.
52. Wei X, Henke VG, Strübing C, Brown EB, Clapham DE (2002). Real-time imaging of nuclear permeation by EGFP in single intact cells. Biophys J 84, 1317-1327.
53. Wu W, Lin F, Worman H (2002). Intracellular trafficking of MAN1, an integral protein of the nuclear envelope inner membrane. J Cell Sci 115, 1361-1371.
54. Yang W (2013). Distinct, but not completely separate spatial transport routes in the nuclear pore complex. Nucleus 4, 166-175.
55. Zuleger N, Kerr A, Schirmer E (2012). Many mechanisms, one entrance: membrane protein translocation into the nucleus. Cell Mol Life Sci 69, 2205-2216.