The trials and tubule-ations of Rab6 involvement in Golgi-to-ER retrograde transport

Biochemical Society Transactions

Volumn 42, Issue 5, 2014, Pages 1453-1459

  Heffernan, Linda F ^a   Simpson, Jeremy C ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Golgi complex; Membrane traffic; Rab GTPase; Rab6; Retrograde transport

Indexed keywords

COAT PROTEIN COMPLEX I; DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN RAB6; UNCLASSIFIED DRUG; ISOENZYME; RAB PROTEIN; RAB6 PROTEIN;

ACTIN FILAMENT; COMPLEX FORMATION; ENDOPLASMIC RETICULUM; ENDOSOME; GOLGI COMPLEX; MEMBRANE STRUCTURE; MEMBRANE TRANSPORT; MICROTUBULE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SECRETORY PATHWAY; ALTERNATIVE RNA SPLICING; ANIMAL; BIOLOGICAL MODEL; ENZYMOLOGY; GENETICS; HUMAN; METABOLISM; ORGANELLE SIZE; PROTEIN TRANSPORT; TRANSPORT AT THE CELLULAR LEVEL;

ALTERNATIVE SPLICING; ANIMALS; BIOLOGICAL TRANSPORT; COAT PROTEIN COMPLEX I; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HUMANS; ISOENZYMES; MODELS, BIOLOGICAL; ORGANELLE SIZE; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS;

EID: 84907192657     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20140178     Document Type: Review

References (78)

1. Palade, G. (1975) Intracellular aspects of the process of protein synthesis. Science 189, 347-358 CrossRef PubMed
2. Hoe, M.H., Slusarewicz, P., Misteli, T., Watson, R. and Warren, G. (1995) Evidence for recycling of the resident medial/trans Golgi enzyme, N-acetylglucosaminyltransferase I, in ldlD cells. J. Biol. Chem. 270, 25057-25063 CrossRef PubMed
3. Zaal, K.J., Smith, C.L., Polishchuk, R.S., Altan, N., Cole, N.B., Ellenberg, J., Hirschberg, K., Presley, J.F., Roberts, T.H., Siggia, E. et al. (1999) Golgi membranes are absorbed into and reemerge from the ER during mitosis. Cell 99, 589-601 CrossRef PubMed
4. Pelletier, L., Jokitalo, E. and Warren, G. (2000) The effect of Golgi depletion on exocytic transport. Nat. Cell Biol. 2, 840-846 CrossRef PubMed
5. Aoe, T., Cukierman, E., Lee, A., Cassel, D., Peters, P.J. and Hsu, V.W. (1997) The KDEL receptor, ERD2, regulates intracellular traffic by recruiting a GTPase-activating protein for ARF1. EMBO J. 16, 7305-7316 CrossRef PubMed
6. Orci, L., Glick, B.S. and Rothman, J.E. (1986) A new type of coated vesicular carrier that appears not to contain clathrin: its possible role in protein transport within the Golgi stack. Cell 46, 171-184 CrossRef PubMed
7. Pelham, H.R. (1991) Recycling of proteins between the endoplasmic reticulum and Golgi complex. Curr. Opin. Cell Biol. 3, 585-591 CrossRef PubMed
8. Nilsson, T., Jackson, M. and Peterson, P.A. (1989) Short cytoplasmic sequences serve as retention signals for transmembrane proteins in the endoplasmic reticulum. Cell 58, 707-718 CrossRef PubMed
9. Munro, S. and Pelham, H.R. (1987) A C-terminal signal prevents secretion of luminal ER proteins. Cell 48, 899-907 CrossRef PubMed
10. Pelham, H.R. (1988) Evidence that luminal ER proteins are sorted from secreted proteins in a post-ER compartment. EMBO J. 7, 913-918 PubMed
11. Pelham, H.R., Hardwick, K.G. and Lewis, M.J. (1988) Sorting of soluble ER proteins in yeast. EMBO J. 7, 1757-1762 PubMed
12. Girod, A., Storrie, B., Simpson, J.C., Johannes, L., Goud, B., Roberts, L.M., Lord, J.M., Nilsson, T. and Pepperkok, R. (1999) Evidence for a COP-I-independent transport route from the Golgi complex to the endoplasmic reticulum. Nat. Cell Biol. 1, 423-430 CrossRef PubMed
13. White, J., Johannes, L., Mallard, F., Girod, A., Grill, S., Reinsch, S., Keller, P., Tzschaschel, B., Echard, A., Goud, B. and Stelzer, E.H. (1999) Rab6 coordinates a novel Golgi to ER retrograde transport pathway in live cells. J. Cell Biol. 147, 743-760 CrossRef PubMed
14. Grosshans, B.L., Ortiz, D. and Novick, P. (2006) Rabs and their effectors: achieving specificity in membrane traffic. Proc. Natl. Acad. Sci. U.S.A.103, 11821-11827 CrossRef PubMed
15. Martinez, O. and Goud, B. (1998) Rab proteins. Biochim. Biophys. Acta 1404, 101-112 CrossRef PubMed
16. Chavrier, P. and Goud, B. (1999) The role of ARF and Rab GTPases in membrane transport. Curr. Opin. Cell Biol. 11, 466-475 CrossRef PubMed
17. Pfeffer, S.R. (2001) Rab GTPases: specifying and deciphering organelle identity and function. Trends Cell Biol. 11, 487-491 CrossRef PubMed
18. Goud, B., Salminen, A., Walworth, N.C. and Novick, P.J. (1988) A GTP-binding protein required for secretion rapidly associates with secretory vesicles and the plasma membrane in yeast. Cell 53, 753-768 CrossRef PubMed
19. Lee, M.T., Mishra, A. and Lambright, D.G. (2009) Structural mechanisms for regulation of membrane traffic by Rab GTPases. Traffic 10, 1377-1389 CrossRef PubMed
20. Pereira-Leal, J.B. and Seabra, M.C. (2001) Evolution of the Rab family of small GTP-binding proteins. J. Mol. Biol. 313, 889-901 CrossRef PubMed
21. Gilchrist, A., Au, C.E., Hiding, J., Bell, A.W., Fernandez-Rodriguez, J., Lesimple, S., Nagaya, H., Roy, L., Gosline, S.J., Hallett, M. et al. (2006) Quantitative proteomics analysis of the secretory pathway. Cell 127, 1265-1281 CrossRef PubMed
22. Antony, C., Cibert, C., Geraud, G., Santa Maria, A., Maro, B., Mayau, V. and Goud, B. (1992) The small GTP-binding protein Rab6p is distributed from medial Golgi to the trans-Golgi network as determined by a confocal microscopic approach. J. Cell Sci. 103, 785-796 PubMed
23. Dejgaard, S.Y., Murshid, A., Erman, A., Kizilay, O., Verbich, D., Lodge, R., Dejgaard, K., Ly-Hartig, T.B., Pepperkok, R., Simpson, J.C. and Presley, J.F. (2008) Rab18 and Rab43 have key roles in ER-Golgi trafficking. J. Cell Sci. 121, 2768-2781 CrossRef PubMed
24. Beranger, F., Paterson, H., Powers, S., de Gunzburg, J. and Hancock, J.F. (1994) The effector domain of Rab6, plus a highly hydrophobic C terminus, is required for Golgi apparatus localization. Mol. Cell. Biol. 14, 744-758 PubMed
25. Schimmoller, F., Simon, I. and Pfeffer, S.R. (1998) Rab GTPases, directors of vesicle docking. J. Biol. Chem. 273, 22161-22164 CrossRef PubMed
26. Bock, J.B., Matern, H.T., Peden, A.A. and Scheller, R.H. (2001) A genomic perspective on membrane compartment organization. Nature 409, 839-841 CrossRef PubMed
27. Echard, A., Opdam, F.J., de Leeuw, H.J., Jollivet, F., Savelkoul, P., Hendriks, W., Voorberg, J., Goud, B. and Fransen, J.A. (2000) Alternative splicing of the human Rab6A gene generates two close but functionally different isoforms. Mol. Biol. Cell 11, 3819-3833 CrossRef PubMed
28. Opdam, F.J., Echard, A., Croes, H.J., van den Hurk, J.A., van de Vorstenbosch, R.A., Ginsel, L.A., Goud, B. and Fransen, J.A. (2000) The small GTPase Rab6B, a novel Rab6 subfamily member, is cell-type specifically expressed and localised to the Golgi apparatus. J. Cell Sci. 113, 2725-2735 PubMed
29. Simpson, J.C., Wellenreuther, R., Poustka, A., Pepperkok, R. and Wiemann, S. (2000) Systematic subcellular localization of novel proteins identified by large-scale cDNA sequencing. EMBO Rep. 1, 287-292 CrossRef PubMed
30. Shan, J., Yuan, L., Budman, D.R. and Xu, H.P. (2002) WTH3, a new member of the Rab6 gene family, and multidrug resistance. Biochim. Biophys. Acta 1589, 112-123 CrossRef PubMed
31. Young, J., Menetrey, J. and Goud, B. (2010) RAB6C is a retrogene that encodes a centrosomal protein involved in cell cycle progression. J. Mol. Biol. 397, 69-88 CrossRef PubMed
32. Valencia, A., Chardin, P., Wittinghofer, A. and Sander, C. (1991) The Ras protein family: evolutionary tree and role of conserved amino acids. Biochemistry 30, 4637-4648 CrossRef PubMed
33. Hardie, D.G. (1993) Protein Phosphorylation: a Practical Approach, IRL Press, Oxford
34. Miserey-Lenkei, S., Couedel-Courteille, A., Del Nery, E., Bardin, S., Piel, M., Racine, V., Sibarita, J.B., Perez, F., Bornens, M. and Goud, B. (2006) A role for the Rab6A′ GTPase in the inactivation of the Mad2-spindle checkpoint. EMBO J. 25, 278-289 CrossRef PubMed
35. Mallard, F., Tang, B.L., Galli, T., Tenza, D., Saint-Pol, A., Yue, X., Antony, C., Hong, W., Goud, B. and Johannes, L. (2002) Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J. Cell Biol. 156, 653-664 CrossRef PubMed
36. Martinez, O., Antony, C., Pehau-Arnaudet, G., Berger, E.G., Salamero, J. and Goud, B. (1997) GTP-bound forms of Rab6 induce the redistribution of Golgi proteins into the endoplasmic reticulum. Proc. Natl. Acad. Sci. U.S.A. 94, 1828-1833 CrossRef PubMed
37. Martinez, O., Schmidt, A., Salamero, J., Hoflack, B., Roa, M. and Goud, B. (1994) The small GTP-binding protein Rab6 functions in intra-Golgi transport. J. Cell Biol. 127, 1575-1588 CrossRef PubMed
38. Young, J., Stauber, T., del Nery, E., Vernos, I., Pepperkok, R. and Nilsson, T. (2005) Regulation of microtubule-dependent recycling at the trans-Golgi network by Rab6A and Rab6A′. Mol. Biol. Cell 16, 162-177 CrossRef PubMed
39. Jiang, S. and Storrie, B. (2005) Cisternal Rab proteins regulate Golgi apparatus redistribution in response to hypotonic stress. Mol. Biol. Cell 16, 2586-2596 CrossRef PubMed
40. Del Nery, E., Miserey-Lenkei, S., Falguieres, T., Nizak, C., Johannes, L., Perez, F. and Goud, B. (2006) Rab6A and Rab6A′ GTPases play non-overlapping roles in membrane trafficking. Traffic 7, 394-407 CrossRef PubMed
41. Barr, F.A. (1999) A novel Rab6-interacting domain defines a family of Golgi-targeted coiled-coil proteins. Curr. Biol. 9, 381-384 CrossRef PubMed
42. Mollenhauer, H.H. and Morre, D.J. (1998) The tubular network of the Golgi apparatus. Histochem. Cell Biol. 109, 533-543 CrossRef PubMed
43. Klausner, R.D., Donaldson, J.G. and Lippincott-Schwartz, J. (1992) Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116, 1071-1080 CrossRef PubMed
44. Jackson, C.L. and Casanova, J.E. (2000) Turning on ARF: the Sec7 family of guanine-nucleotide-exchange factors. Trends Cell Biol. 10, 60-67 CrossRef PubMed
45. Martinez-Alonso, E., Egea, G., Ballesta, J. and Martinez-Menarguez, J.A. (2005) Structure and dynamics of the Golgi complex at 15°C: low temperature induces the formation of Golgi-derived tubules. Traffic 6, 32-44 CrossRef PubMed
46. Judson, B.L. and Brown, W.J. (2009) Assembly of an intact Golgi complex requires phospholipase A2 (PLA2) activity, membrane tubules, and dynein-mediated microtubule transport. Biochem. Biophys. Res. Commun. 389, 473-477 CrossRef PubMed
47. Voeltz, G.K., Prinz, W.A., Shibata, Y., Rist, J.M. and Rapoport, T.A. (2006) A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124, 573-586 CrossRef PubMed
48. Hu, J., Shibata, Y., Zhu, P.P., Voss, C., Rismanchi, N., Prinz, W.A., Rapoport, T.A. and Blackstone, C. (2009) A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell 138, 549-561 CrossRef PubMed
49. Weidman, P.J. (1995) Anterograde transport through the Golgi complex: do Golgi tubules hold the key? Trends Cell Biol. 5, 302-305 CrossRef PubMed
50. Simpson, J.C., Nilsson, T. and Pepperkok, R. (2006) Biogenesis of tubular ER-to-Golgi transport intermediates. Mol. Biol. Cell 17, 723-737 CrossRef PubMed
51. Spang, A., Matsuoka, K., Hamamoto, S., Schekman, R. and Orci, L. (1998) Coatomer, Arf1p, and nucleotide are required to bud coat protein complex I-coated vesicles from large synthetic liposomes. Proc. Natl. Acad. Sci. U.S.A. 95, 11199-11204 CrossRef PubMed
52. Yang, J.S., Valente, C., Polishchuk, R.S., Turacchio, G., Layre, E., Moody, D.B., Leslie, C.C., Gelb, M.H., Brown, W.J., Corda, D. et al. (2011) COPI acts in both vesicular and tubular transport. Nat. Cell Biol. 13, 996-1003 CrossRef PubMed
53. de Figueiredo, P., Drecktrah, D., Katzenellenbogen, J.A., Strang, M. and Brown, W.J. (1998) Evidence that phospholipase A2 activity is required for Golgi complex and trans Golgi network membrane tubulation. Proc. Natl. Acad. Sci. U.S.A. 95, 8642-8647 CrossRef PubMed
54. de Figueiredo, P., Polizotto, R.S., Drecktrah, D. and Brown, W.J. (1999) Membrane tubule-mediated reassembly and maintenance of the Golgi complex is disrupted by phospholipase A2 antagonists. Mol. Biol. Cell 10, 1763-1782 CrossRef PubMed
55. Corda, D., Hidalgo Carcedo, C., Bonazzi, M., Luini, A. and Spano, S. (2002) Molecular aspects of membrane fission in the secretory pathway. Cell. Mol. Life Sci. 59, 1819-1832 CrossRef PubMed
56. Shindou, H. and Shimizu, T. (2009) Acyl-CoA:lysophospholipid acyltransferases. J. Biol. Chem. 284, 1-5 CrossRef PubMed
57. Schmidt, J.A. and Brown, W.J. (2009) Lysophosphatidic acid acyltransferase 3 regulates Golgi complex structure and function. J. Cell Biol. 186, 211-218 CrossRef PubMed
58. Echard, A., Jollivet, F., Martinez, O., Lacapere, J.J., Rousselet, A., Janoueix-Lerosey, I. and Goud, B. (1998) Interaction of a Golgi-associated kinesin-like protein with Rab6. Science 279, 580-585 CrossRef PubMed
59. Hill, E., Clarke, M. and Barr, F.A. (2000) The Rab6-binding kinesin, Rab6-KIFL, is required for cytokinesis. EMBO J. 19, 5711-5719 CrossRef PubMed
60. Fontijn, R.D., Goud, B., Echard, A., Jollivet, F., van Marle, J., Pannekoek, H. and Horrevoets, A.J. (2001) The human kinesin-like protein RB6K is under tight cell cycle control and is essential for cytokinesis. Mol. Cell. Biol. 21, 2944-2955 CrossRef PubMed
61. Karki, S. and Holzbaur, E.L. (1999) Cytoplasmic dynein and dynactin in cell division and intracellular transport. Curr. Opin. Cell Biol. 11, 45-53 CrossRef PubMed
62. Allan, V. (2000) Dynactin. Curr. Biol. 10, R432 CrossRef PubMed
63. King, S.J. and Schroer, T.A. (2000) Dynactin increases the processivity of the cytoplasmic dynein motor. Nat. Cell Biol. 2, 20-24 CrossRef PubMed
64. Helfand, B.T., Mikami, A., Vallee, R.B. and Goldman, R.D. (2002) A requirement for cytoplasmic dynein and dynactin in intermediate filament network assembly and organization. J. Cell Biol. 157, 795-806 CrossRef PubMed
65. Wanschers, B., van de Vorstenbosch, R., Wijers, M., Wieringa, B., King, S.M. and Fransen, J. (2008) Rab6 family proteins interact with the dynein light chain protein DYNLRB1. Cell Motil. Cytoskeleton 65, 183-196 CrossRef PubMed
66. Short, B., Preisinger, C., Schaletzky, J., Kopajtich, R. and Barr, F.A. (2002) The Rab6 GTPase regulates recruitment of the dynactin complex to Golgi membranes. Curr. Biol. 12, 1792-1795 CrossRef PubMed
67. Hoogenraad, C.C., Akhmanova, A., Howell, S.A., Dortland, B.R., De Zeeuw, C.I., Willemsen, R., Visser, P., Grosveld, F. and Galjart, N. (2001) Mammalian Golgi-associated Bicaudal-D2 functions in the dynein-dynactin pathway by interacting with these complexes. EMBO J. 20, 4041-4054 CrossRef PubMed
68. Matanis, T., Akhmanova, A., Wulf, P., Del Nery, E., Weide, T., Stepanova, T., Galjart, N., Grosveld, F., Goud, B., De Zeeuw, C.I. et al. (2002) Bicaudal-D regulates COPI-independent Golgi-ER transport by recruiting the dynein-dynactin motor complex. Nat. Cell Biol. 4, 986-992 CrossRef PubMed
69. Januschke, J., Nicolas, E., Compagnon, J., Formstecher, E., Goud, B. and Guichet, A. (2007) Rab6 and the secretory pathway affect oocyte polarity in Drosophila. Development 134, 3419-3425 CrossRef PubMed
70. Mallik, R., Petrov, D., Lex, S.A., King, S.J. and Gross, S.P. (2005) Building complexity: an in vitro study of cytoplasmic dynein with in vivo implications. Curr. Biol. 15, 2075-2085 CrossRef PubMed
71. Yamada, M., Kumamoto, K., Mikuni, S., Arai, Y., Kinjo, M., Nagai, T., Tsukasaki, Y., Watanabe, T.M., Fukui, M., Jin, M. et al. (2013) Rab6a releases LIS1 from a dynein idling complex and activates dynein for retrograde movement. Nat. Commun. 4, 2033 CrossRef PubMed
72. Valderrama, F., Duran, J.M., Babia, T., Barth, H., Renau-Piqueras, J. and Egea, G. (2001) Actin microfilaments facilitate the retrograde transport from the Golgi complex to the endoplasmic reticulum in mammalian cells. Traffic 2, 717-726 CrossRef PubMed
73. Musch, A., Cohen, D. and Rodriguez-Boulan, E. (1997) Myosin II is involved in the production of constitutive transport vesicles from the TGN. J. Cell Biol. 138, 291-306 CrossRef PubMed
74. Stow, J.L., Fath, K.R. and Burgess, D.R. (1998) Budding roles for myosin II on the Golgi. Trends Cell Biol. 8, 138-141 CrossRef PubMed
75. Duran, J.M., Valderrama, F., Castel, S., Magdalena, J., Tomas, M., Hosoya, H., Renau-Piqueras, J., Malhotra, V. and Egea, G. (2003) Myosin motors and not actin comets are mediators of the actin-based Golgi-to-endoplasmic reticulum protein transport. Mol. Biol. Cell 14, 445-459 CrossRef PubMed
76. Narula, N., McMorrow, I., Plopper, G., Doherty, J., Matlin, K.S., Burke, B. and Stow, J.L. (1992) Identification of a 200-kD, brefeldin-sensitive protein on Golgi membranes. J. Cell Biol. 117, 27-38 CrossRef PubMed
77. Miserey-Lenkei, S., Chalancon, G., Bardin, S., Formstecher, E., Goud, B. and Echard, A. (2010) Rab and actomyosin-dependent fission of transport vesicles at the Golgi complex. Nat. Cell Biol. 12, 645-654 CrossRef PubMed
78. Valente, C., Polishchuk, R. and De Matteis, M.A. (2010) Rab6 and myosin II at the cutting edge of membrane fission. Nat. Cell Biol. 12, 635-638 CrossRef PubMed