Endoplasmic reticulum: One continuous network compartmentalized by extrinsic cues

Current Opinion in Cell Biology

Volumn 17, Issue 4, 2005, Pages 362-368

  Levine, Tim ^a   Rabouille, Catherine ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA;

APOPTOSIS; CAENORHABDITIS ELEGANS; CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; CYTOSKELETON; ENDOPLASMIC RETICULUM; GENE MUTATION; GENETIC LINKAGE; GOLGI COMPLEX; INTRACELLULAR TRANSPORT; MEMBRANE BINDING; MITOCHONDRION; NONHUMAN; PICHIA; PRIORITY JOURNAL; REVIEW; SECRETORY VESICLE;

EID: 22044433038     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2005.06.005     Document Type: Review

References (65)

1. C. Barlowe, L. Orci, T. Yeung, M. Hosobuchi, S. Hamamoto, N. Salama, M.F. Rexach, M. Ravazzola, M. Amherdt, and R. Schekman COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum Cell 77 1994 895 907
2. G.K. Voeltz, M.M. Rolls, and T.A. Rapoport Structural organization of the endoplasmic reticulum EMBO Rep 3 2002 944 950
3. M.M. Rolls, D.H. Hall, M. Victor, E.H. Stelzer, and T.A. Rapoport Targeting of rough endoplasmic reticulum membrane proteins and ribosomes in invertebrate neurons Mol Biol Cell 13 2002 1778 1791
4. C.A. Farah, D. Liazoghli, S. Perreault, M. Desjardins, A. Guimont, A. Anton, M. Lauzon, G. Kreibich, J. Paiement, and N. Leclerc Interaction of microtubule-associated protein-2 and p63: a new link between microtubules and rough endoplasmic reticulum membranes in neurons J Biol Chem 280 2005 9439 9449
5. 2+-binding requirements Mol Biol Cell 15 2004 481 496
6. A.S. DePina, and G.M. Langford Vesicle transport: the role of actin filaments and myosin motors Microsc Res Tech 47 1999 93 106
7. Poteryaev D, Squirrell JM, Campbell JM, White JG, Spang A: Involvement of the actin cytoskeleton and homotypic membrane fusion in ER dynamics in C. elegans. Mol Biol Cell 2005, in press.
8. J. Soderholm, D. Bhattacharyya, D. Strongin, V. Markovitz, P.L. Connerly, C.A. Reinke, and B.S. Glick The transitional ER localization mechanism of Pichia pastoris Sec12 Dev Cell 6 2004 649 659 This elegant paper describes how sec12 is ruled out as the landmark protein specifying the localisation of the tER sites along the ER.
9. V. Kondylis, and C. Rabouille A novel role for dp115 in the organization of tER sites in Drosophila J Cell Biol 162 2003 185 198
10. B.J. Bevis, A.T. Hammond, C.A. Reinke, and B.S. Glick De novo formation of transitional ER sites and Golgi structures in Pichia pastoris Nat Cell Biol 4 2002 750 756
11. D.J. Stephens De novo formation, fusion and fission of mammalian COPII-coated endoplasmic reticulum exit sites EMBO Rep 4 2003 210 217
12. P. Watson, R. Forster, K.J. Palmer, R. Pepperkok, and D.J. Stephens Coupling of ER exit to microtubules through direct interaction of COPII with dynactin Nat Cell Biol 7 2005 48 55
13. R. Blum, D.J. Stephens, and I. Schulz Lumenal targeted GFP, used as a marker of soluble cargo, visualises rapid ERGIC to Golgi traffic by a tubulo-vesicular network J Cell Sci 113 2000 3151 3159
14. D.J. Stephens, and R. Pepperkok Imaging of procollagen transport reveals COPI-dependent cargo sorting during ER-to-Golgi transport in mammalian cells J Cell Sci 115 2002 1149 1160
15. A. Bashirullah, R.L. Cooperstock, and H.D. Lipshitz RNA localization in development Annu Rev Biochem 67 1998 335 394
16. •].
17. N. MacDougall, A. Clark, E. MacDougall, and I. Davis Drosophila gurken (TGFα) mRNA localizes as particles that move within the oocyte in two dynein-dependent steps Dev Cell 4 2003 307 319 This work gives an understanding of how interactions with the cytoskeleton localize Gurken mRNA at the dorsal anterior corner of the Drosophila oocyte.
18. Delanoue R, Davis I: Dynein anchors its mRNA cargo after apical transport in the Drosophila blastoderm embryo. Cell 2005, in press. For a long time, the anchoring of RNA at their restricted location within cells has been the object of intense research. This work shows that not only the movement of RNA (in the form of RNA particles) along the minus end of microtubules is mediated by dynein but that their anchoring uses the same molecular device.
19. • ] illustrate very well how mRNAs can be anchored and how this restricted localisation is fundamental for basic cellular events.
20. K.A. Shepard, A.P. Gerber, A. Jambhekar, P.A. Takizawa, P.O. Brown, D. Herschlag, J.L. DeRisi, and R.D. Vale Widespread cytoplasmic mRNA transport in yeast: identification of 22 bud-localized transcripts using DNA microarray analysis Proc Natl Acad Sci USA 100 2003 11429 11434 Localised RNAs can also encode transmembrane/secreted proteins: in this study 5 out of 22 transcripts encode this type of protein, showing that this is not a rare phenomenon. This raises the issue of local transport, either through the classical exocytic pathway, as for Gurken, or via the novel ER/plasma membrane pathway, as is the case for Ist2.
21. J.O. Deshler, M.I. Highett, and B.J. Schnapp Localization of Xenopus Vg1 mRNA by Vera protein and the endoplasmic reticulum Science 276 1997 1128 1131
22. M. Kloc, and L.D. Etkin Apparent continuity between the messenger transport organizer and late RNA localization pathways during oogenesis in Xenopus Mech Dev 73 1998 95 106
23. S.B. Choi, C. Wang, D.G. Muench, K. Ozawa, V.R. Franceschi, Y. Wu, and T.W. Okita Messenger RNA targeting of rice seed storage proteins to specific ER subdomains Nature 407 2000 765 767
24. A.J. Crofts, H. Washida, T.W. Okita, M. Ogawa, T. Kumamaru, and H. Satoh Targeting of proteins to endoplasmic-reticulum-derived compartments in plants: the importance of RNA localization Plant Physiol 136 2004 3414 3419 This review discusses the direct anchoring of mRNAs on the ER in rice seeds, thus creating ER functional sub-domains. The associated paper [23] describes a powerful mRNA visualization method based on in situ fluorescent reverse transcriptase (RT) PCR.
25. S. Mogelsvang, N. Gomez-Ospina, J. Soderholm, B.S. Glick, and L.A. Staehelin Tomographic evidence for continuous turnover of Golgi cisternae in Pichia pastoris Mol Biol Cell 14 2003 2277 2291
26. B. Herpers, and C. Rabouille mRNA localization and ER-based protein sorting mechanisms dictate the use of tER-Golgi units involved in Gurken transport in Drosophila oocytes Mol Biol Cell 15 2004 5306 5317 This article shows that localized mRNA can create heterogeneity in the RER and in the usage of tER sites, thus creating a pre-translational mechanism for the localized deposition of secreted/transmembrane proteins. As a consequence, the tER sites are also shown to function independently.
27. F.S. Neuman-Silberberg, and T. Schupbach The Drosophila dorsoventral patterning gene Gurken produces a dorsally localized RNA and encodes a TGFα-like protein Cell 75 1993 165 174
28. W.J. Nelson, and C. Yeaman Protein trafficking in the exocytic pathway of polarized epithelial cells Trends Cell Biol 11 2001 483 486
29. A.J. Simmonds, G. dosSantos, I. Livne-Bar, and H.M. Krause Apical localization of wingless transcripts is required for wingless signaling Cell 105 2001 197 207
30. J.M. Lucocq, J.G. Pryde, E.G. Berger, and G. Warren A mitotic form of the Golgi apparatus in HeLa cells J Cell Biol 104 1987 865 874
31. A.C. Horton, and M.D. Ehlers Dual modes of endoplasmic-reticulum-to-Golgi transport in dendrites revealed by live-cell imaging J Neurosci 23 2003 6188 6199 This article shows unambiguously that dendrites contain ER and Golgi elements that might serve in the local synthesis and transport of transmembrane receptors.
32. W. Ju, W. Morishita, J. Tsui, G. Gaietta, T.J. Deerinck, S.R. Adams, C.C. Garner, R.Y. Tsien, M.H. Ellisman, and R.C. Malenka Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors Nat Neurosci 7 2004 244 253 This article and associated review [33] suggest strongly that mRNA for the AMPA receptor is translated and transported locally within dendrites. This pre-translational sorting mechanism is similar to that described in the Drosophila oocyte to ensure localized deposition of transmembrane proteins.
33. R.C. Malenka Synaptic plasticity and AMPA receptor trafficking Ann N Y Acad Sci 1003 2003 1 11
34. P.A. Brittis, Q. Lu, and J.G. Flanagan Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target Cell 110 2002 223 235
35. ••] are all shown to be translated and inserted in the plasma membrane independently from the cell body.
36. G.E. Spencer, N.I. Syed, E. van Kesteren, K. Lukowiak, W.P. Geraerts, and J. van Minnen Synthesis and functional integration of a neurotransmitter receptor in isolated invertebrate axons J Neurobiol 44 2000 72 81
37. M.S. Ladinsky, D.N. Mastronarde, J.R. McIntosh, K.E. Howell, and L.A. Staehelin Golgi structure in three dimensions: functional insights from the normal rat kidney cell J Cell Biol 144 1999 1135 1149
38. F.G. Haj, P.J. Verveer, A. Squire, B.G. Neel, and P.I. Bastiaens Imaging sites of receptor dephosphorylation by PTP1B on the surface of the endoplasmic reticulum Science 295 2002 1708 1711
39. C. Xu, J. Fan, W. Riekhof, J.E. Froehlich, and C. Benning A permease-like protein involved in ER to thylakoid lipid transfer in Arabidopsis EMBO J 22 2003 2370 2379
40. H.J. Geuze, J.L. Murk, A.K. Stroobants, J.M. Griffith, M.J. Kleijmeer, A.J. Koster, A.J. Verkleij, B. Distel, and H.F. Tabak Involvement of the endoplasmic reticulum in peroxisome formation Mol Biol Cell 14 2003 2900 2907
41. Y. Li, and W.A. Prinz ATP-binding cassette (ABC) transporters mediate nonvesicular, raft-modulated sterol movement from the plasma membrane to the endoplasmic reticulum J Biol Chem 279 2004 45226 45234 The traffic of sterol in yeast is independent of the classical secretory pathway, even though the sterol studied here is cholesterol rather than endogenous ergosterol. Also, as found in the study by Baumann et al. [42••], the propensity for sterol to escape the ER is correlated with its ability to form complexes.
42. Baumann N, Sullivan D, Ohvo-Rekilä H, Simonot C, Pottekat A, Klaassen Z, Beh C, Menon A: Transport of newly synthesized sterol to the sterol-enriched plasma membrane occurs via non-vesicular equilibration. Biochemistry 2005, in press. The kinetics of sterol traffic to the plasma membrane in yeast are not affected by blocking all SNARE-mediated traffic, suggesting that sterol traffics by a non-vesicular route. Furthermore, sphingolipids in the plasma membrane act as a sink for sterol, as together these lipids form high-affinity complexes, so that the total sterol concentration in the plasma membrane is far higher in than in the ER, although the concentration of free sterol is the same in both compartments.
43. H. Pichler, B. Gaigg, C. Hrastnik, G. Achleitner, S.D. Kohlwein, G. Zellnig, A. Perktold, and G. Daum A subfraction of the yeast endoplasmic reticulum associates with the plasma membrane and has a high capacity to synthesize lipids Eur J Biochem 268 2001 2351 2361
44. W. Guo, and P. Novick The exocyst meets the translocon: a regulatory circuit for secretion and protein synthesis? Trends Cell Biol 14 2004 61 63
45. A. Wiederkehr, Y. Du, M. Pypaert, S. Ferro-Novick, and P. Novick Sec3p is needed for the spatial regulation of secretion and for the inheritance of the cortical endoplasmic reticulum Mol Biol Cell 14 2003 4770 4782
46. C.J. Loewen, A. Roy, and T.P. Levine A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP EMBO J 22 2003 2025 2035
47. T. Becker, A. Volchuk, and J.E. Rothman Differential use of endoplasmic reticulum membrane for phagocytosis in J774 macrophages Proc Natl Acad Sci USA 102 2005 4022 4026
48. 2+ release triggers translocation of membrane marker FM1-43 from the extracellular leaflet of the plasma membrane into endoplasmic reticulum in T lymphocytes. J Biol Chem 2005, in press.
49. C. Juschke, D. Ferring, R.P. Jansen, and M. Seedorf A novel transport pathway for a yeast plasma membrane protein encoded by a localized mRNA Curr Biol 14 2004 406 411 Transport of the integral membrane protein Ist2 to the plasma membrane is unaffected by various sec mutations inactivating the classical secretory pathway at different points, and appears to rely instead on direct transport from the ER to the plasma membrane. In addition, Ist2 mRNA is one of very few mRNAs localized to the bud-tip that code for a membrane protein, although the relationship between this and the means of exocytosis has not been examined.
50. Juschke C, Wachter A, Schwappach B, Seedorf M: SEC18/NSF-independent, protein-sorting pathway from the yeast cortical ER to the plasma membrane. J Cell Biol 2005, in press.
51. W. Nickel The mystery of nonclassical protein secretion: a current view on cargo proteins and potential export routes Eur J Biochem 270 2003 2109 2119 This review describes protein insertion in the plasma membrane that is independent of the ER. This differs from the novel membrane trafficking pathway suggested for Ist2 from the ER to the plasma membrane.
52. M. Schnabl, G. Daum, and H. Pichler Multiple lipid transport pathways to the plasma membrane in yeast Biochim Biophys Acta 1687 2005 130 140
53. T. Levine Short-range intracellular trafficking of small molecules across endoplasmic reticulum junctions Trends Cell Biol 14 2004 483 490
54. H.J. Wang, G. Guay, L. Pogan, R. Sauve, and I.R. Nabi Calcium regulates the association between mitochondria and a smooth subdomain of the endoplasmic reticulum J Cell Biol 150 2000 1489 1498
55. J.E. Vance Phospholipid synthesis in a membrane fraction associated with mitochondria J Biol Chem 265 1990 7248 7256
56. 2+ traffic occurs at stable structures similar to MAM.
57. S. Colombo, R. Longhi, S. Alcaro, F. Ortuso, T. Sprocati, A. Flora, and N. Borgese N-myristoylation determines dual targeting of mammalian NADH-Cytochrome b(5) reductase to ER and mitochondrial outer membranes by a mechanism of kinetic partitioning J Cell Biol 168 2005 735 745
58. Miyazaki E, Kida Y, Mihara K, Sakaguchi M: Switching the sorting mode of membrane proteins from co-translational ER targeting to post-translational mitochondrial import. Mol Biol Cell 2005, in press.
59. R.E. van Herpen, R.J. Oude Ophuis, M. Wijers, M.B. Bennink, F.A. van de Loo, J. Fransen, B. Wieringa, and D.G. Wansink Divergent mitochondrial and endoplasmic reticulum association of DMPK splice isoforms depends on unique sequence arrangements in tail anchors Mol Cell Biol 25 2005 1402 1414
60. V. Shoshan-Barmatz, R. Zalk, D. Gincel, and N. Vardi Subcellular localization of VDAC in mitochondria and ER in the cerebellum Biochim Biophys Acta 1657 2004 105 114
61. D.G. Breckenridge, M. Stojanovic, R.C. Marcellus, and G.C. Shore Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol J Cell Biol 160 2003 1115 1127
62. D. Chandra, G. Choy, X. Deng, B. Bhatia, P. Daniel, and D.G. Tang Association of active caspase 8 with the mitochondrial membrane during apoptosis: potential roles in cleaving BAP31 and caspase 3 and mediating mitochondrion-endoplasmic-reticulum cross talk in etoposide-induced cell death Mol Cell Biol 24 2004 6592 6607
63. T. Simmen, J.E. Aslan, A.D. Blagoveshchenskaya, L. Thomas, L. Wan, Y. Xiang, S.F. Feliciangeli, C.H. Hung, C.M. Crump, and G. Thomas PACS-2 controls endoplasmic reticulum-mitochondria communication and Bid-mediated apoptosis EMBO J 24 2005 717 729 PACS-2, like PACS-1, is shown to be a cargo sorting protein, but unlike PACS-1, which targets cargo within the late secretory pathway, PACS-2 targets Bid to mitochondria. Furthermore, PACS-2 is among the first proteins identified that are essential for normal architecture of ER-mitochondrial- membrane contact sites.
64. L.A. Staehelin The plant ER: a dynamic organelle composed of a large number of discrete functional domains Plant J 11 1997 1151 1165
65. X. Pan, P. Roberts, Y. Chen, E. Kvam, N. Shulga, K. Huang, S. Lemmon, and D.S. Goldfarb Nucleus-vacuole junctions in Saccharomyces cerevisiae are formed through the direct interaction of Vac8p with Nvj1p Mol Biol Cell 11 2000 2445 2457