GM130 Regulates Golgi-Derived Spindle Assembly by Activating TPX2 and Capturing Microtubules

Cell

Volumn 162, Issue 2, 2015, Pages 287-299

  Wei, Jen Hsuan ^a   Zhang, Zi Chao ^a   Wynn, R Max ^a   Seemann, Joachim ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA A KINASE; GM 130 PROTEIN; KARYOPHERIN ALPHA; MEMBRANE PROTEIN; TARGET PROTEIN FOR XENOPUS KINESIN LIKE PROTEIN 2; UNCLASSIFIED DRUG; AUTOANTIGEN; CELL CYCLE PROTEIN; GOLGIN SUBFAMILY A MEMBER 2; KARYOPHERIN; MICROTUBULE ASSOCIATED PROTEIN; NUCLEAR PROTEIN; PHOSPHOPROTEIN; TPX2 PROTEIN, MOUSE; TPX2 PROTEIN, XENOPUS; XENOPUS PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FEMALE; GOLGI MEMBRANE; HUMAN; HUMAN CELL; IN VITRO STUDY; MICROTUBULE; MICROTUBULE ASSEMBLY; MITOSIS SPINDLE; NONHUMAN; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; RAT; ANIMAL; GOLGI COMPLEX; HELA CELL LINE; METABOLISM; MITOSIS; MOUSE; SPINDLE APPARATUS; XENOPUS;

ANIMALS; AURORA KINASE A; AUTOANTIGENS; CELL CYCLE PROTEINS; GOLGI APPARATUS; HELA CELLS; HUMANS; KARYOPHERINS; MEMBRANE PROTEINS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOSIS; NUCLEAR PROTEINS; PHOSPHOPROTEINS; SPINDLE APPARATUS; XENOPUS; XENOPUS PROTEINS;

EID: 84937250948     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.06.014     Document Type: Article

References (54)

1. F. Baschieri, S. Confalonieri, G. Bertalot, P.P. Di Fiore, W. Dietmaier, M. Leist, P. Crespo, I.G. Macara, and H. Farhan Spatial control of Cdc42 signalling by a GM130-RasGRF complex regulates polarity and tumorigenesis Nat. Commun. 5 2014 4839
2. R. Basto, J. Lau, T. Vinogradova, A. Gardiol, C.G. Woods, A. Khodjakov, and J.W. Raff Flies without centrioles Cell 125 2006 1375 1386
3. R. Bayliss, T. Sardon, I. Vernos, and E. Conti Structural basis of Aurora-A activation by TPX2 at the mitotic spindle Mol. Cell 12 2003 851 862
4. H. Bazzi, and K.V. Anderson Acentriolar mitosis activates a p53-dependent apoptosis pathway in the mouse embryo Proc. Natl. Acad. Sci. USA 111 2014 E1491 E1500
5. R.E. Carazo-Salas, G. Guarguaglini, O.J. Gruss, A. Segref, E. Karsenti, and I.W. Mattaj Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation Nature 400 1999 178 181
6. K. Chabin-Brion, J. Marceiller, F. Perez, C. Settegrana, A. Drechou, G. Durand, and C. Poüs The Golgi complex is a microtubule-organizing organelle Mol. Biol. Cell 12 2001 2047 2060
7. P. Chang, M. Coughlin, and T.J. Mitchison Interaction between Poly(ADP-ribose) and NuMA contributes to mitotic spindle pole assembly Mol. Biol. Cell 20 2009 4575 4585
8. M.L. Cutress, H.C. Whitaker, I.G. Mills, M. Stewart, and D.E. Neal Structural basis for the nuclear import of the human androgen receptor J. Cell Sci. 121 2008 957 968
9. A. Diao, D. Rahman, D.J.C. Pappin, J. Lucocq, and M. Lowe The coiled-coil membrane protein golgin-84 is a novel rab effector required for Golgi ribbon formation J. Cell Biol. 160 2003 201 212
10. A. Efimov, A. Kharitonov, N. Efimova, J. Loncarek, P.M. Miller, N. Andreyeva, P. Gleeson, N. Galjart, A.R.R. Maia, I.X. McLeod, and et al. Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network Dev. Cell 12 2007 917 930
11. A. Giesecke, and M. Stewart Novel binding of the mitotic regulator TPX2 (target protein for Xenopus kinesin-like protein 2) to importin-alpha J. Biol. Chem. 285 2010 17628 17635
12. G. Goshima, M. Mayer, N. Zhang, N. Stuurman, and R.D. Vale Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle J. Cell Biol. 181 2008 421 429
13. O.J. Gruss, R.E. Carazo-Salas, C.A. Schatz, G. Guarguaglini, J. Kast, M. Wilm, N. Le Bot, I. Vernos, E. Karsenti, and I.W. Mattaj Ran induces spindle assembly by reversing the inhibitory effect of importin alpha on TPX2 activity Cell 104 2001 83 93
14. V. Hachet, T. Köcher, M. Wilm, and I.W. Mattaj Importin alpha associates with membranes and participates in nuclear envelope assembly in vitro EMBO J. 23 2004 1526 1535
15. H. Hehnly, and S. Doxsey Rab11 endosomes contribute to mitotic spindle organization and orientation Dev. Cell 28 2014 497 507
16. H.J. Heidebrecht, F. Buck, J. Steinmann, R. Sprenger, H.H. Wacker, and R. Parwaresch p100: a novel proliferation-associated nuclear protein specifically restricted to cell cycle phases S, G2, and M Blood 90 1997 226 233
17. R. Ishida, A. Yamamoto, K. Nakayama, M. Sohda, Y. Misumi, T. Yasunaga, and N. Nakamura GM130 is a parallel tetramer with a flexible rod-like structure and N-terminally open (Y-shaped) and closed (I-shaped) conformations FEBS J. 282 2015 2232 2244
18. S.A. Jesch, and A.D. Linstedt The Golgi and endoplasmic reticulum remain independent during mitosis in HeLa cells Mol. Biol. Cell 9 1998 623 635
19. E. Jokitalo, N. Cabrera-Poch, G. Warren, and D.T. Shima Golgi clusters and vesicles mediate mitotic inheritance independently of the endoplasmic reticulum J. Cell Biol. 154 2001 317 330
20. P. Kalab, and R. Heald The RanGTP gradient - a GPS for the mitotic spindle J. Cell Sci. 121 2008 1577 1586
21. P. Kalab, R.T. Pu, and M. Dasso The ran GTPase regulates mitotic spindle assembly Curr. Biol. 9 1999 481 484
22. P. Kaláb, A. Pralle, E.Y. Isacoff, R. Heald, and K. Weis Analysis of a RanGTP-regulated gradient in mitotic somatic cells Nature 440 2006 697 701
23. A. Khodjakov, R.W. Cole, B.R. Oakley, and C.L. Rieder Centrosome-independent mitotic spindle formation in vertebrates Curr. Biol. 10 2000 59 67
24. A. Kodani, and C. Sütterlin The Golgi protein GM130 regulates centrosome morphology and function Mol. Biol. Cell 19 2008 745 753
25. T.P. Levine, C. Rabouille, R.H. Kieckbusch, and G. Warren Binding of the vesicle docking protein p115 to Golgi membranes is inhibited under mitotic conditions J. Biol. Chem. 271 1996 17304 17311
26. M. Lowe, C. Rabouille, N. Nakamura, R. Watson, M. Jackman, E. Jämsä, D. Rahman, D.J. Pappin, and G. Warren Cdc2 kinase directly phosphorylates the cis-Golgi matrix protein GM130 and is required for Golgi fragmentation in mitosis Cell 94 1998 783 793
27. M. Lowe, N.K. Gonatas, and G. Warren The mitotic phosphorylation cycle of the cis-Golgi matrix protein GM130 J. Cell Biol. 149 2000 341 356
28. S. Meunier, and I. Vernos Microtubule assembly during mitosis - from distinct origins to distinct functions? J. Cell Sci. 125 2012 2805 2814
29. N. Nakamura, M. Lowe, T.P. Levine, C. Rabouille, and G. Warren The vesicle docking protein p115 binds GM130, a cis-Golgi matrix protein, in a mitotically regulated manner Cell 89 1997 445 455
30. J. Niclas, V.J. Allan, and R.D. Vale Cell cycle regulation of dynein association with membranes modulates microtubule-based organelle transport J. Cell Biol. 133 1996 585 593
31. S. Oddoux, K.J. Zaal, V. Tate, A. Kenea, S.A. Nandkeolyar, E. Reid, W. Liu, and E. Ralston Microtubules that form the stationary lattice of muscle fibers are dynamic and nucleated at Golgi elements J. Cell Biol. 203 2013 205 213
32. T. Ohba, M. Nakamura, H. Nishitani, and T. Nishimoto Self-organization of microtubule asters induced in Xenopus egg extracts by GTP-bound Ran Science 284 1999 1356 1358
33. K.M. Ori-McKenney, L.Y. Jan, and Y.-N. Jan Golgi outposts shape dendrite morphology by functioning as sites of acentrosomal microtubule nucleation in neurons Neuron 76 2012 921 930
34. S. Petry, A.C. Groen, K. Ishihara, T.J. Mitchison, and R.D. Vale Branching microtubule nucleation in Xenopus egg extracts mediated by augmin and TPX2 Cell 152 2013 768 777
35. V.W. Pollard, W.M. Michael, S. Nakielny, M.C. Siomi, F. Wang, and G. Dreyfuss A novel receptor-mediated nuclear protein import pathway Cell 86 1996 985 994
36. C. Preisinger, B. Short, V. De Corte, E. Bruyneel, A. Haas, R. Kopajtich, J. Gettemans, and F.A. Barr YSK1 is activated by the Golgi matrix protein GM130 and plays a role in cell migration through its substrate 14-3-3zeta J. Cell Biol. 164 2004 1009 1020
37. S. Rivero, J. Cardenas, M. Bornens, and R.M. Rios Microtubule nucleation at the cis-side of the Golgi apparatus requires AKAP450 and GM130 EMBO J. 28 2009 1016 1028
38. T. Sardon, I. Peset, B. Petrova, and I. Vernos Dissecting the role of Aurora A during spindle assembly EMBO J. 27 2008 2567 2579
39. G. Sauer, R. Körner, A. Hanisch, A. Ries, E.A. Nigg, and H.H.W. Silljé Proteome analysis of the human mitotic spindle Mol. Cell. Proteomics 4 2005 35 43
40. C.A. Schatz, R. Santarella, A. Hoenger, E. Karsenti, I.W. Mattaj, O.J. Gruss, and R.E. Carazo-Salas Importin alpha-regulated nucleation of microtubules by TPX2 EMBO J. 22 2003 2060 2070
41. J. Seemann, E.J. Jokitalo, and G. Warren The role of the tethering proteins p115 and GM130 in transport through the Golgi apparatus in vivo Mol. Biol. Cell 11 2000 635 645
42. J. Seemann, M. Pypaert, T. Taguchi, J. Malsam, and G. Warren Partitioning of the matrix fraction of the Golgi apparatus during mitosis in animal cells Science 295 2002 848 851
43. D.T. Shima, K. Haldar, R. Pepperkok, R. Watson, and G. Warren Partitioning of the Golgi apparatus during mitosis in living HeLa cells J. Cell Biol. 137 1997 1211 1228
44. D.T. Shima, N. Cabrera-Poch, R. Pepperkok, and G. Warren An ordered inheritance strategy for the Golgi apparatus: visualization of mitotic disassembly reveals a role for the mitotic spindle J. Cell Biol. 141 1998 955 966
45. D. Tang, Y. Xiang, and Y. Wang Reconstitution of the cell cycle-regulated Golgi disassembly and reassembly in a cell-free system Nat. Protoc. 5 2010 758 772
46. R.S. Taylor, S.M. Jones, R.H. Dahl, M.H. Nordeen, and K.E. Howell Characterization of the Golgi complex cleared of proteins in transit and examination of calcium uptake activities Mol. Biol. Cell 8 1997 1911 1931
47. M.-Y. Tsai, C. Wiese, K. Cao, O. Martin, P. Donovan, J. Ruderman, C. Prigent, and Y. Zheng A Ran signalling pathway mediated by the mitotic kinase Aurora A in spindle assembly Nat. Cell Biol. 5 2003 242 248
48. J.-H. Wei, and J. Seemann Mitotic division of the mammalian Golgi apparatus Semin. Cell Dev. Biol. 20 2009 810 816
49. J.-H. Wei, and J. Seemann The mitotic spindle mediates inheritance of the Golgi ribbon structure J. Cell Biol. 184 2009 391 397
50. C. Wiese, A. Wilde, M.S. Moore, S.A. Adam, A. Merdes, and Y. Zheng Role of importin-beta in coupling Ran to downstream targets in microtubule assembly Science 291 2001 653 656
51. J.D. Wilbur, and R. Heald Mitotic spindle scaling during Xenopus development by kif2a and importin α eLife 2 2013 e00290
52. A. Wilde, and Y. Zheng Stimulation of microtubule aster formation and spindle assembly by the small GTPase Ran Science 284 1999 1359 1362
53. C.-H. Zhang, Z.-B. Wang, S. Quan, X. Huang, J.-S. Tong, J.-Y. Ma, L. Guo, Y.-C. Wei, Y.-C. Ouyang, Y. Hou, and et al. GM130, a cis-Golgi protein, regulates meiotic spindle assembly and asymmetric division in mouse oocyte Cell Cycle 10 2011 1861 1870
54. Y. Zheng A membranous spindle matrix orchestrates cell division Nat. Rev. Mol. Cell Biol. 11 2010 529 535