Implication of ZW10 in Membrane Trafficking Between the Endoplasmic Reticulum and Golgi

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 2004 Mar 19

PMID 15029241

Citations 102

Authors

Hidenori Hirose

Kohei Arasaki

Naoshi Dohmae

Koji Takio

Kiyotaka Hatsuzawa

Masami Nagahama

Katsuko Tani

Akitsugu Yamamoto

Masaya Tohyama

Mitsuo Tagaya

Affiliations

Soon will be listed here.

Abstract

ZW10, a dynamitin-interacting protein associated with kinetochores, is known to participate directly in turning off of the spindle checkpoint. In the present study, we show that ZW10 is located in the endoplasmic reticulum as well as in the cytosol during interphase, and forms a subcomplex with RINT-1 (Rad50-interacting protein) and p31 in a large complex comprising syntaxin 18, an endoplasmic reticulum-localized t-SNARE implicated in membrane trafficking. Like conventional syntaxin-binding proteins, ZW10, RINT-1 and p31 dissociated from syntaxin 18 upon Mg(2+)-ATP treatment in the presence of NSF and alpha-SNAP, whereas the subcomplex was not disassembled. Overexpression, microinjection and knockdown experiments revealed that ZW10 is involved in membrane trafficking between the endoplasmic reticulum and Golgi. The present results disclose an unexpected role for a spindle checkpoint protein, ZW10, during interphase.

Citing Articles

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References

STARR D, Williams B, Li Z, Etemad-Moghadam B, Dawe R, Goldberg M . Conservation of the centromere/kinetochore protein ZW10. J Cell Biol. 1997; 138(6):1289-301. PMC: 2132553. DOI: 10.1083/jcb.138.6.1289. View

Yamaguchi T, Yamamoto A, Furuno A, Hatsuzawa K, Tani K, Himeno M . Possible involvement of heterotrimeric G proteins in the organization of the Golgi apparatus. J Biol Chem. 1997; 272(40):25260-6. DOI: 10.1074/jbc.272.40.25260. View

Burkhardt J, Echeverri C, Nilsson T, Vallee R . Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J Cell Biol. 1997; 139(2):469-84. PMC: 2139801. DOI: 10.1083/jcb.139.2.469. View

Patel S, Indig F, Olivieri N, Levine N, Latterich M . Organelle membrane fusion: a novel function for the syntaxin homolog Ufe1p in ER membrane fusion. Cell. 1998; 92(5):611-20. DOI: 10.1016/s0092-8674(00)81129-0. View

STARR D, Williams B, Hays T, Goldberg M . ZW10 helps recruit dynactin and dynein to the kinetochore. J Cell Biol. 1998; 142(3):763-74. PMC: 2148168. DOI: 10.1083/jcb.142.3.763. View

Fukunaga T, Furuno A, Hatsuzawa K, Tani K, Yamamoto A, Tagaya M . NSF is required for the brefeldin A-promoted disassembly of the Golgi apparatus. FEBS Lett. 1998; 435(2-3):237-40. DOI: 10.1016/s0014-5793(98)01081-3. View

Storrie B, White J, Rottger S, Stelzer E, Suganuma T, Nilsson T . Recycling of golgi-resident glycosyltransferases through the ER reveals a novel pathway and provides an explanation for nocodazole-induced Golgi scattering. J Cell Biol. 1998; 143(6):1505-21. PMC: 2132995. DOI: 10.1083/jcb.143.6.1505. View

Alvarez C, Fujita H, Hubbard A, Sztul E . ER to Golgi transport: Requirement for p115 at a pre-Golgi VTC stage. J Cell Biol. 1999; 147(6):1205-22. PMC: 2168100. DOI: 10.1083/jcb.147.6.1205. View

Zaal K, Smith C, Polishchuk R, Altan N, Cole N, Ellenberg J . Golgi membranes are absorbed into and reemerge from the ER during mitosis. Cell. 1999; 99(6):589-601. DOI: 10.1016/s0092-8674(00)81548-2. View

10.

Tang B, Zhang T, Low D, Wong E, Horstmann H, Hong W . Mammalian homologues of yeast sec31p. An ubiquitously expressed form is localized to endoplasmic reticulum (ER) exit sites and is essential for ER-Golgi transport. J Biol Chem. 2000; 275(18):13597-604. DOI: 10.1074/jbc.275.18.13597. View

11.

Hatsuzawa K, Hirose H, Tani K, Yamamoto A, Scheller R, Tagaya M . Syntaxin 18, a SNAP receptor that functions in the endoplasmic reticulum, intermediate compartment, and cis-Golgi vesicle trafficking. J Biol Chem. 2000; 275(18):13713-20. DOI: 10.1074/jbc.275.18.13713. View

12.

STARR D, Saffery R, Li Z, Simpson A, Choo K, Yen T . HZwint-1, a novel human kinetochore component that interacts with HZW10. J Cell Sci. 2000; 113 ( Pt 11):1939-50. DOI: 10.1242/jcs.113.11.1939. View

13.

Fukunaga T, Nagahama M, Hatsuzawa K, Tani K, Yamamoto A, Tagaya M . Implication of sphingolipid metabolism in the stability of the Golgi apparatus. J Cell Sci. 2000; 113 ( Pt 18):3299-307. DOI: 10.1242/jcs.113.18.3299. View

14.

Wickner W, Haas A . Yeast homotypic vacuole fusion: a window on organelle trafficking mechanisms. Annu Rev Biochem. 2000; 69:247-75. DOI: 10.1146/annurev.biochem.69.1.247. View

15.

Lin R, Scheller R . Mechanisms of synaptic vesicle exocytosis. Annu Rev Cell Dev Biol. 2000; 16:19-49. DOI: 10.1146/annurev.cellbio.16.1.19. View

16.

Chan G, Jablonski S, STARR D, Goldberg M, Yen T . Human Zw10 and ROD are mitotic checkpoint proteins that bind to kinetochores. Nat Cell Biol. 2001; 2(12):944-7. DOI: 10.1038/35046598. View

17.

Savoian M, Goldberg M, Rieder C . The rate of poleward chromosome motion is attenuated in Drosophila zw10 and rod mutants. Nat Cell Biol. 2001; 2(12):948-52. DOI: 10.1038/35046605. View

18.

Xiao J, Liu C, Chen P, Lee W . RINT-1, a novel Rad50-interacting protein, participates in radiation-induced G(2)/M checkpoint control. J Biol Chem. 2000; 276(9):6105-11. DOI: 10.1074/jbc.M008893200. View

19.

Ito T, Chiba T, Ozawa R, Yoshida M, Hattori M, Sakaki Y . A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci U S A. 2001; 98(8):4569-74. PMC: 31875. DOI: 10.1073/pnas.061034498. View

20.

Elbashir S, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T . Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature. 2001; 411(6836):494-8. DOI: 10.1038/35078107. View