Dsl1p/Zw10: Common mechanisms behind tethering vesicles and microtubules

Trends in Cell Biology

Volumn 20, Issue 5, 2010, Pages 257-268

  Schmitt, Hans Dieter ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COAT PROTEIN; COAT PROTEIN 1; FUNGAL PROTEIN; PROTEIN DSL1P; PROTEIN ZW10; SNARE PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CELL COMPARTMENTALIZATION; CELL MATURATION; CELL MEMBRANE TRANSPORT; CELL VACUOLE; CENTROMERE; CHROMOSOME SEGREGATION; CYTOPLASM; ENDOPLASMIC RETICULUM; EUKARYOTE; GOLGI COMPLEX; HUMAN; MAMMAL CELL; MICROTUBULE; MITOSIS; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SEQUENCE HOMOLOGY; YEAST CELL;

ANIMALS; CELL CYCLE PROTEINS; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; MEMBRANE FUSION; MODELS, BIOLOGICAL; PROTEIN TRANSPORT; QA-SNARE PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

ANIMALIA; MAMMALIA; METAZOA;

EID: 77952554428     PISSN: 09628924     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tcb.2010.02.001     Document Type: Review

References (86)

1. Bonifacino J.S., Glick B.S. The mechanisms of vesicle budding and fusion. Cell 2004, 116:153-166.
2. Markgraf D.F., et al. Rab cascades and tethering factors in the endomembrane system. FEBS Lett. 2007, 581:2125-2130.
3. Jahn R., Scheller R.H. SNAREs - engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 2006, 7:631-643.
4. Sutton R.B., et al. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 1998, 395:347-353.
5. Pelham H.R. SNAREs and the specificity of membrane fusion. Trends Cell Biol. 2001, 11:99-101.
6. Tsui M.M., Banfield D.K. Yeast Golgi SNARE interactions are promiscuous. J. Cell. Sci. 2000, 113:145-152.
7. Cai H.Q., et al. Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev. Cell 2007, 12:671-682.
8. Kümmel D., Heinemann U. Diversity in structure and function of tethering complexes: evidence for different mechanisms in vesicular transport regulation. Curr. Protein Pept. Sci. 2008, 9:197-209.
9. Whyte J.R., Munro S. Vesicle tethering complexes in membrane traffic. J. Cell. Sci. 2002, 115:2627-2637.
10. Barinaga-Rementeria Ramirez I., Lowe M. Golgins and GRASPs: holding the Golgi together. Semin. Cell Dev. Biol. 2009, 20:770-779.
11. Sztul E., Lupashin V. Role of vesicle tethering factors in the ER-Golgi membrane traffic. FEBS Lett. 2009, 583:3770-3783.
12. Peplowska K., et al. The CORVET tethering complex interacts with the yeast Rab5 homolog Vps21 and is involved in endo-lysosomal biogenesis. Dev. Cell 2007, 12:739-750.
13. Sacher M., et al. Identification and characterization of five new subunits of TRAPP. Eur. J. Cell Biol. 2000, 79:71-80.
14. Kim Y.G., et al. The architecture of the multisubunit TRAPP I complex suggests a model for vesicle tethering. Cell 2006, 127:817-830.
15. Munson M., Novick P. The exocyst defrocked, a framework of rods revealed. Nat. Struct. Mol. Biol. 2006, 13:577-581.
16. Ren Y., et al. A structure-based mechanism for vesicle capture by the multisubunit tethering complex Dsl1. Cell 2009, 139:1119-1129.
17. Tripathi A., et al. Structural characterization of Tip20p and Dsl1p, subunits of the Dsl1p vesicle tethering complex. Nat. Struct. Mol. Biol. 2009, 16:114-123.
18. Cavanaugh L.F., et al. Structural analysis of conserved oligomeric Golgi complex subunit 2. J. Biol. Chem. 2007, 282:23418-23426.
19. Richardson B.C., et al. Structural basis for a human glycosylation disorder caused by mutation of the COG4 gene. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13329-13334.
20. Perez-Victoria F.J., Bonifacino J.S. Dual roles of the mammalian GARP complex in tethering and SNARE complex assembly at the trans-golgi network. Mol. Cell Biol. 2009, 29:5251-5263.
21. Shestakova A., et al. Interaction of the conserved oligomeric Golgi complex with t-SNARE Syntaxin5a/Sed5 enhances intra-Golgi SNARE complex stability. J. Cell. Biol. 2007, 179:1179-1192.
22. Starai V.J., et al. HOPS proofreads the trans-SNARE complex for yeast vacuole fusion. Mol. Biol. Cell 2008, 19:2500-2508.
23. Andag U., Schmitt H.D. Dsl1p, an essential component of the Golgi-endoplasmic reticulum retrieval system in yeast, uses the same sequence motif to interact with different subunits of the COPI vesicle coat. J. Biol. Chem. 2003, 278:51722-51734.
24. Cai H.Q., et al. TRAPPI tethers COPII vesicles by binding the coat subunit Sec23. Nature 2007, 445:941-944.
25. Zink S., et al. A link between ER tethering and COP-I vesicle uncoating. Dev. Cell 2009, 17:403-416.
26. Behnia R., et al. The yeast orthologue of GRASP65 forms a complex with a coiled-coil protein that contributes to ER to Golgi traffic. J. Cell Biol. 2007, 176:255-261.
27. Kraynack B.A., et al. Dsl1p, Tip20p, and the novel Dsl3(Sec39) protein are required for the stability of the Q/t-SNARE complex at the endoplasmic reticulum in yeast. Mol. Biol. Cell 2005, 16:3963-3977.
28. Collins K.M., et al. Sec17p and HOPS, in distinct SNARE complexes, mediate SNARE complex disruption or assembly for fusion. EMBO J. 2005, 24:1775-1786.
29. Sweet D.J., Pelham H.R.B. The Saccharomyces cerevisiae SEC20 gene encodes a membrane glycoprotein which is sorted by the hdel retrieval-system. EMBO J. 1992, 11:423-432.
30. Sweet D.J., Pelham H.R.B. The TIP1 gene of Saccharomyces cerevisiae encodes an 80 kda cytoplasmic protein that interacts with the cytoplasmic domain of Sec20p. EMBO J. 1993, 12:2831-2840.
31. Spang A. On vesicle formation and tethering in the ER-Golgi shuttle. Curr. Opin. Cell Biol. 2009, 21:531-536.
32. Hirose H., et al. Implication of ZW10 in membrane trafficking between the endoplasmic reticulum and Golgi. EMBO J. 2004, 23:1267-1278.
33. Aoki T., et al. Identification of the neuroblastoma-amplified gene (NAG) product as a component of the syntaxin 18 complex implicated in Golgi-to-endoplasmic reticulum retrograde transport. Mol. Biol. Cell 2009, 20:2639-2649.
34. Arasaki K., et al. RINT-1 regulates the localization and entry of ZW10 to the syntaxin 18 complex. Mol. Biol. Cell 2006, 17:2780-2788.
35. Nakajima K., et al. Involvement of BNIP1 in apoptosis and endoplasmic reticulum membrane fusion. EMBO J. 2004, 23:3216-3226.
36. Inoue M., et al. N-terminal region of ZW10 serves not only as a determinant for localization but also as a link with dynein function. Genes Cells 2008, 13:905-914.
37. Starr D.A., et al. Conservation of the centromere/kinetochore protein ZW10. J. Cell. Biol. 1997, 138:1289-1301.
38. Xiao J., et al. RINT-1, a novel Rad50-interacting protein, participates in radiation-induced G(2)/M checkpoint control. J. Biol. Chem. 2001, 276:6105-6111.
39. Lin X., et al. RINT-1 serves as a tumor suppressor and maintains Golgi dynamics and centrosome integrity for cell survival. Mol. Cell Biol. 2007, 27:4905-4916.
40. Kong L.J., et al. The Rb-related p130 protein controls telomere lengthening through an interaction with a Rad50-interacting protein, RINT-1. Mol. Cell 2006, 22:63-71.
41. Uemura T., et al. p31 deficiency influences endoplasmic reticulum tubular morphology and cell survival. Mol. Cell Biol. 2009, 29:1869-1881.
42. Wimmer K., et al. Co-amplification of a novel gene, NAG, with the N-myc gene in neuroblastoma. Oncogene 1999, 18:233-238.
43. Karess R. Rod-Zw10-Zwilch: a key player in the spindle checkpoint. Trends Cell Biol. 2005, 15:386-392.
44. Vallee R.B., et al. ZW10 function in mitotic checkpoint control, dynein targeting and membrane trafficking: Is dynein the unifying theme?. Cell Cycle 2006, 5:2447-2451.
45. Wang H., et al. Human Zwint-1 specifies localization of Zeste White 10 to kinetochores and is essential for mitotic checkpoint signaling. J. Biol. Chem. 2004, 279:54590-54598.
46. Starr D.A., et al. HZwint-1, a novel human kinetochore component that interacts with HZW10. J. Cell. Sci. 2000, 113:1939-1950.
47. Famulski J.K., et al. Stable hZW10 kinetochore residency, mediated by hZwint-1 interaction, is essential for the mitotic checkpoint. J. Cell. Biol. 2008, 180:507-520.
48. Chan G.K., et al. Human Zw10 and ROD are mitotic checkpoint proteins that bind to kinetochores. Nat. Cell Biol. 2000, 2:944-947.
49. Williams B.C., et al. Zwilch, a new component of the ZW10/ROD complex required for kinetochore functions. Mol. Biol. Cell. 2003, 14:1379-1391.
50. Raikov I.B. The diversity of forms of mitosis in protozoa: a comparative review. Eur. J. Protistol. 1994, 30:253-269.
51. Scaërou F., et al. The ZW10 and Rough Deal checkpoint proteins function together in a large, evolutionarily conserved complex targeted to the kinetochore. J. Cell. Sci. 2001, 114:3103-3114.
52. Starr D.A., et al. ZW10 helps recruit dynactin and dynein to the kinetochore. J. Cell Biol. 1998, 142:763-774.
53. Gassmann R., et al. A new mechanism controlling kinetochore-microtubule interactions revealed by comparison of two dynein-targeting components: SPDL-1 and the Rod/Zwilch/Zw10 complex. Genes Dev. 2008, 22:2385-2399.
54. Basto R., et al. In vivo dynamics of the rough deal checkpoint protein during Drosophila mitosis. Curr. Biol. 2004, 14:56-61.
55. Kops G.J., et al. ZW10 links mitotic checkpoint signaling to the structural kinetochore. J. Cell Biol. 2005, 169:49-60.
56. Buffin E., et al. Recruitment of Mad2 to the kinetochore requires the Rod/Zw10 complex. Curr. Biol. 2005, 15:856-861.
57. Presley J.F., et al. ER-to-Golgi transport visualized in living cells. Nature 1997, 389:81-85.
58. Vaughan K.T. Microtubule plus ends, motors, and traffic of Golgi membranes. Biochim. Biophys. Acta. 2005, 1744:316-324.
59. Brownhill K., et al. Molecular motors and the Golgi complex: Staying put and moving through. Semin. Cell Dev. Biol. 2009, 20:784-792.
60. Sun Y., et al. Rab6 regulates both ZW10/RINT-1-and conserved oligomeric Golgi complex-dependent Golgi trafficking and homeostasis. Mol. Biol. Cell 2007, 18:4129-4142.
61. Varma D., et al. Role of the kinetochore/cell cycle checkpoint protein ZW10 in interphase cytoplasmic dynein function. J. Cell Biol. 2006, 172:655-662.
62. Iinuma T., et al. Role of syntaxin 18 in the organization of endoplasmic reticulum subdomains. J. Cell Sci. 2009, 122:1680-1690.
63. Okumura A.J., et al. Involvement of a novel Q-SNARE, D12, in quality control of the endomembrane system. J. Biol. Chem. 2006, 281:4495-4506.
64. Yang Z., et al. Kinetochore dynein is required for chromosome motion and congression independent of the spindle checkpoint. Curr. Biol. 2007, 17:973-980.
65. Thyberg J., Moskalewski S. Role of microtubules in the organization of the Golgi complex. Exp. Cell Res. 1999, 246:263-279.
66. Watson P., et al. Coupling of ER exit to microtubules through direct interaction of COPII with dynactin. Nat. Cell Biol. 2005, 7:48-55.
67. Kim H., et al. Microtubule binding by dynactin is required for microtubule organization but not cargo transport. J. Cell Biol. 2007, 176:641-651.
68. Watson P., Stephens D.J. Microtubule plus-end loading of p150(Glued) is mediated by EB1 and CLIP-170 but is not required for intracellular membrane traffic in mammalian cells. J. Cell Sci. 2006, 119:2758-2767.
69. Lomakin A.J., et al. CLIP-170-dependent capture of membrane organelles by microtubules initiates minus-end directed transport. Dev. Cell 2009, 17:323-333.
70. Tanaka T.U., Desai A. Kinetochore-microtubule interactions: the means to the end. Curr. Opin. Cell Biol. 2008, 20:53-63.
71. Arasaki K., et al. Correlation of Golgi localization of ZW10 and centrosomal accumulation of dynactin. Biochem. Biophys. Res. Commun. 2007, 359:811-816.
72. Wickstead B., Gull K. Dyneins across eukaryotes: a comparative genomic analysis. Traffic 2007, 8:1708-1721.
73. Sheeman B., et al. Determinants of S. cerevisiae dynein localization and activation: implications for the mechanism of spindle positioning. Curr. Biol. 2003, 13:364-372.
74. James T.Y., et al. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 2006, 443:818-822.
75. Boyd C., et al. Vesicles carry most exocyst subunits to exocytic sites marked by the remaining two subunits, Sec3p and Exo70p. J. Cell Biol. 2004, 167:889-901.
76. Pucadyil T.J., Schmid S.L. Conserved functions of membrane active GTPases in coated vesicle formation. Science 2009, 325:1217-1220.
77. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
78. Poirot O., et al. Tcoffee@igs: A web server for computing, evaluating and combining multiple sequence alignments. Nucleic Acids Res. 2003, 31:3503-3506.
79. Andag U., et al. The coatomer interacting protein Dsl1p is required for Golgi-to-ER retrieval in yeast. J. Biol. Chem. 2001, 276:39150-39160.
80. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983, 22:2577-2637.
81. Pei J., et al. Remote homology between Munc13 MUN domain and vesicle tethering complexes. J. Mol. Biol. 2009, 391:509-517.
82. Heath I.B. Variant mitoses in lower eukaryotes: indicators of the evolution of mitosis?. Int. Rev. Cytol. 1980, 64:1-80.
83. Burki F., et al. Phylogenomics reveals a new 'megagroup' including most photosynthetic eukaryotes. Biol. Lett. 2008, 4:366-369.
84. De Souza C.P., Osmani S.A. Double duty for nuclear proteins - the price of more open forms of mitosis. Trends Genet. 2009, 25:545-554.
85. Rawet, M. et al. (2010) ArfGAP1 interacts with coat proteins through tryptophan-based motifs. Biochem. Biophys. Res. Commun. doi:10.1016/j.bbrc.2010.03.017.
86. Çivril, F. et al. Structural analysis of the RZZ complex reveals common ancestry with multisubunit vesicle tethering machinery. Structure. In press. doi:10.1016/j.str.2010.02.014.