Monoubiquitination of Syntaxin 5 Regulates Golgi Membrane Dynamics during the Cell Cycle

Developmental Cell

Volumn 38, Issue 1, 2016, Pages 73-85

  Huang, Shijiao ^a   Tang, Danming ^a   Wang, Yanzhuang ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; DEUBIQUITINASE; DEUBIQUITINASE VCIP135; LYSINE; PROTEIN P47; PROTEIN P97; SNARE PROTEIN; SYNTAXIN; SYNTAXIN 5; UBIQUITIN; UBIQUITIN LIGASE HACE1; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; PROTEIN BINDING; SMALL INTERFERING RNA;

ARTICLE; CELL CYCLE; CELL MUTANT; CONTROLLED STUDY; GOLGI COMPLEX; GOLGI MEMBRANE; HELA CELL LINE; MITOSIS; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; UBIQUITINATION; ANTAGONISTS AND INHIBITORS; GENETICS; HUMAN; MEMBRANE FUSION; METABOLISM; PHYSIOLOGY;

CELL CYCLE; GOLGI APPARATUS; HELA CELLS; HUMANS; MEMBRANE FUSION; MITOSIS; PROTEIN BINDING; QA-SNARE PROTEINS; RNA, SMALL INTERFERING; UBIQUITIN; UBIQUITINATION;

EID: 84979710789     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2016.06.001     Document Type: Article

References (33)

1. Anglesio, M.S., Evdokimova, V., Melnyk, N., Zhang, L., Fernandez, C.V., Grundy, P.E., Leach, S., Marra, M.A., Brooks-Wilson, A.R., Penninger, J., et al. Differential expression of a novel ankyrin containing E3 ubiquitin-protein ligase, Hace1, in sporadic Wilms' tumor versus normal kidney. Hum. Mol. Genet. 13 (2004), 2061–2074.
2. Hardwick, K.G., Pelham, H.R., SED5 encodes a 39-kD integral membrane protein required for vesicular transport between the ER and the Golgi complex. J. Cell Biol. 119 (1992), 513–521.
3. Hay, J.C., Chao, D.S., Kuo, C.S., Scheller, R.H., Protein interactions regulating vesicle transport between the endoplasmic reticulum and Golgi apparatus in mammalian cells. Cell 89 (1997), 149–158.
4. Hong, W., Lev, S., Tethering the assembly of SNARE complexes. Trends Cell Biol. 24 (2014), 35–43.
5. Hui, N., Nakamura, N., Sonnichsen, B., Shima, D.T., Nilsson, T., Warren, G., An isoform of the Golgi t-SNARE, syntaxin 5, with an endoplasmic reticulum retrieval signal. Mol. Biol. Cell 8 (1997), 1777–1787.
6. Jahn, R., Scheller, R.H., SNAREs—engines for membrane fusion. Nat. Rev. 7 (2006), 631–643.
7. Lowe, M., Rabouille, C., Nakamura, N., Watson, R., Jackman, M., Jamsa, E., Rahman, D., Pappin, D.J., Warren, G., Cdc2 kinase directly phosphorylates the cis-Golgi matrix protein GM130 and is required for Golgi fragmentation in mitosis. Cell 94 (1998), 783–793.
8. Mallard, F., Tang, B.L., Galli, T., Tenza, D., Saint-Pol, A., Yue, X., Antony, C., Hong, W., Goud, B., Johannes, L., Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J. Cell Biol. 156 (2002), 653–664.
9. Meyer, H.H., Wang, Y., Warren, G., Direct binding of ubiquitin conjugates by the mammalian p97 adaptor complexes, p47 and Ufd1-Npl4. EMBO J. 21 (2002), 5645–5652.
10. Miyazaki, K., Wakana, Y., Noda, C., Arasaki, K., Furuno, A., Tagaya, M., Contribution of the long form of syntaxin 5 to the organization of the endoplasmic reticulum. J. Cell Sci. 125 (2012), 5658–5666.
11. Rabouille, C., Levine, T.P., Peters, J.M., Warren, G., An NSF-like ATPase, p97, and NSF mediate cisternal regrowth from mitotic Golgi fragments. Cell 82 (1995), 905–914.
12. Rabouille, C., Kondo, H., Newman, R., Hui, N., Freemont, P., Warren, G., Syntaxin 5 is a common component of the NSF- and p97-mediated reassembly pathways of Golgi cisternae from mitotic Golgi fragments in vitro. Cell 92 (1998), 603–610.
13. Sieber, J.J., Willig, K.I., Kutzner, C., Gerding-Reimers, C., Harke, B., Donnert, G., Rammner, B., Eggeling, C., Hell, S.W., Grubmuller, H., et al. Anatomy and dynamics of a supramolecular membrane protein cluster. Science 317 (2007), 1072–1076.
14. Tai, G., Lu, L., Wang, T.L., Tang, B.L., Goud, B., Johannes, L., Hong, W., Participation of the syntaxin 5/Ykt6/GS28/GS15 SNARE complex in transport from the early/recycling endosome to the trans-Golgi network. Mol. Biol. Cell 15 (2004), 4011–4022.
15. Takamori, S., Holt, M., Stenius, K., Lemke, E.A., Gronborg, M., Riedel, D., Urlaub, H., Schenck, S., Brugger, B., Ringler, P., et al. Molecular anatomy of a trafficking organelle. Cell 127 (2006), 831–846.
16. Tang, D., Wang, Y., Cell cycle regulation of Golgi membrane dynamics. Trends Cell Biol. 23 (2013), 296–304.
17. Tang, D., Wang, Y., Golgi isolation. Cold Spring Harb Protoc. 2015 (2015), 562–567.
18. Tang, D., Mar, K., Warren, G., Wang, Y., Molecular mechanism of mitotic Golgi disassembly and reassembly revealed by a defined reconstitution assay. J. Biol. Chem. 283 (2008), 6085–6094.
19. Tang, D., Xiang, Y., Wang, Y., Reconstitution of the cell cycle-regulated Golgi disassembly and reassembly in a cell-free system. Nat. Protoc. 5 (2010), 758–772.
20. Tang, D., Xiang, Y., De Renzis, S., Rink, J., Zheng, G., Zerial, M., Wang, Y., The ubiquitin ligase HACE1 regulates Golgi membrane dynamics during the cell cycle. Nat. Commun., 2, 2011, 501.
21. Torrino, S., Visvikis, O., Doye, A., Boyer, L., Stefani, C., Munro, P., Bertoglio, J., Gacon, G., Mettouchi, A., Lemichez, E., The E3 ubiquitin-ligase HACE1 catalyzes the ubiquitylation of active Rac1. Dev. Cell 21 (2011), 959–965.
22. Uchiyama, K., Jokitalo, E., Kano, F., Murata, M., Zhang, X., Canas, B., Newman, R., Rabouille, C., Pappin, D., Freemont, P., et al. VCIP135, a novel essential factor for p97/p47-mediated membrane fusion, is required for Golgi and ER assembly in vivo. J. Cell Biol. 159 (2002), 855–866.
23. Uchiyama, K., Totsukawa, G., Puhka, M., Kaneko, Y., Jokitalo, E., Dreveny, I., Beuron, F., Zhang, X., Freemont, P., Kondo, H., p37 is a p97 adaptor required for Golgi and ER biogenesis in interphase and at the end of mitosis. Dev. Cell 11 (2006), 803–816.
24. Wang, Y., Seemann, J., Golgi biogenesis. Cold Spring Harb Perspect. Biol., 3, 2011, a005330.
25. Wang, Y., Satoh, A., Warren, G., Meyer, H.H., VCIP135 acts as a deubiquitinating enzyme during p97-p47-mediated reassembly of mitotic Golgi fragments. J. Cell Biol. 164 (2004), 973–978.
26. Warren, G., Featherstone, C., Griffiths, G., Burke, B., Newly synthesized G protein of vesicular stomatitis virus is not transported to the cell surface during mitosis. J. Cell Biol. 97 (1983), 1623–1628.
27. Weber, T., Zemelman, B.V., McNew, J.A., Westermann, B., Gmachl, M., Parlati, F., Sollner, T.H., Rothman, J.E., SNAREpins: minimal machinery for membrane fusion. Cell 92 (1998), 759–772.
28. Xiang, Y., Wang, Y., GRASP55 and GRASP65 play complementary and essential roles in Golgi cisternal stacking. J. Cell Biol. 188 (2010), 237–251.
29. Xu, Y., Martin, S., James, D.E., Hong, W., GS15 forms a SNARE complex with syntaxin 5, GS28, and Ykt6 and is implicated in traffic in the early cisternae of the Golgi apparatus. Mol. Biol. Cell 13 (2002), 3493–3507.
30. Zhang, T., Hong, W., Ykt6 forms a SNARE complex with syntaxin 5, GS28, and Bet1 and participates in a late stage in endoplasmic reticulum-Golgi transport. J. Biol. Chem. 276 (2001), 27480–27487.
31. Zhang, X., Wang, Y., Cell cycle regulation of VCIP135 deubiquitinase activity and function in p97/p47-mediated Golgi reassembly. Mol. Biol. Cell 26 (2015), 2242–2251.
32. Zhang, X., Zhang, H., Wang, Y., Phosphorylation regulates VCIP135 function in Golgi membrane fusion during the cell cycle. J. Cell Sci. 127 (2014), 172–181.
33. Zhang, X., Gui, L., Zhang, X., Bulfer, S.L., Sanghez, V., Wong, D.E., Lee, Y., Lehmann, L., Lee, J.S., Shih, P.Y., et al. Altered cofactor regulation with disease-associated p97/VCP mutations. Proc. Natl. Acad. Sci. USA 112 (2015), E1705–E1714.