Cis-Golgi Proteins Accumulate Near the ER Exit Sites and Act As the Scaffold for Golgi Regeneration After Brefeldin A Treatment in Tobacco BY-2 Cells

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2012 Jun 29

PMID 22740633

Citations 43

Authors

Yoko Ito

Tomohiro Uemura

Keiko Shoda

Masaru Fujimoto

Takashi Ueda

Akihiko Nakano

Affiliations

Soon will be listed here.

Abstract

The Golgi apparatus forms stacks of cisternae in many eukaryotic cells. However, little is known about how such a stacked structure is formed and maintained. To address this question, plant cells provide a system suitable for live-imaging approaches because individual Golgi stacks are well separated in the cytoplasm. We established tobacco BY-2 cell lines expressing multiple Golgi markers tagged by different fluorescent proteins and observed their responses to brefeldin A (BFA) treatment and BFA removal. BFA treatment disrupted cis, medial, and trans cisternae but caused distinct relocalization patterns depending on the proteins examined. Medial- and trans-Golgi proteins, as well as one cis-Golgi protein, were absorbed into the endoplasmic reticulum (ER), but two other cis-Golgi proteins formed small punctate structures. After BFA removal, these puncta coalesced first, and then the Golgi stacks regenerated from them in the cis-to-trans order. We suggest that these structures have a property similar to the ER-Golgi intermediate compartment and function as the scaffold of Golgi regeneration.

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References

An G . High efficiency transformation of cultured tobacco cells. Plant Physiol. 1985; 79(2):568-70. PMC: 1074928. DOI: 10.1104/pp.79.2.568. View

Losev E, Reinke C, Jellen J, Strongin D, Bevis B, Glick B . Golgi maturation visualized in living yeast. Nature. 2006; 441(7096):1002-6. DOI: 10.1038/nature04717. View

Sato K, Nishikawa S, Nakano A . Membrane protein retrieval from the Golgi apparatus to the endoplasmic reticulum (ER): characterization of the RER1 gene product as a component involved in ER localization of Sec12p. Mol Biol Cell. 1995; 6(11):1459-77. PMC: 301304. DOI: 10.1091/mbc.6.11.1459. View

Rossanese O, Soderholm J, Bevis B, Sears I, OConnor J, Williamson E . Golgi structure correlates with transitional endoplasmic reticulum organization in Pichia pastoris and Saccharomyces cerevisiae. J Cell Biol. 1999; 145(1):69-81. PMC: 2148216. DOI: 10.1083/jcb.145.1.69. View

Takeuchi M, Ueda T, Yahara N, Nakano A . Arf1 GTPase plays roles in the protein traffic between the endoplasmic reticulum and the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J. 2002; 31(4):499-515. DOI: 10.1046/j.1365-313x.2002.01372.x. View

Sato K, Ueda T, Nakano A . The Arabidopsis thaliana RER1 gene family: its potential role in the endoplasmic reticulum localization of membrane proteins. Plant Mol Biol. 2000; 41(6):815-24. DOI: 10.1023/a:1006329828395. View

Karimi M, Inze D, Depicker A . GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 2002; 7(5):193-5. DOI: 10.1016/s1360-1385(02)02251-3. View

Seemann J, Jokitalo E, Pypaert M, Warren G . Matrix proteins can generate the higher order architecture of the Golgi apparatus. Nature. 2000; 407(6807):1022-6. DOI: 10.1038/35039538. View

Lowe M . Structural organization of the Golgi apparatus. Curr Opin Cell Biol. 2010; 23(1):85-93. DOI: 10.1016/j.ceb.2010.10.004. View

10.

GAYNOR E, Emr S . COPI-independent anterograde transport: cargo-selective ER to Golgi protein transport in yeast COPI mutants. J Cell Biol. 1997; 136(4):789-802. PMC: 2132489. DOI: 10.1083/jcb.136.4.789. View

11.

Bevis B, Hammond A, Reinke C, Glick B . De novo formation of transitional ER sites and Golgi structures in Pichia pastoris. Nat Cell Biol. 2002; 4(10):750-6. DOI: 10.1038/ncb852. View

12.

Latijnhouwers M, Gillespie T, Boevink P, Kriechbaumer V, Hawes C, Carvalho C . Localization and domain characterization of Arabidopsis golgin candidates. J Exp Bot. 2008; 58(15-16):4373-86. DOI: 10.1093/jxb/erm304. View

13.

daSilva L, Snapp E, Denecke J, Lippincott-Schwartz J, Hawes C, Brandizzi F . Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells. Plant Cell. 2004; 16(7):1753-71. PMC: 514159. DOI: 10.1105/tpc.022673. View

14.

Nebenfuhr A, Frohlick J, Staehelin L . Redistribution of Golgi stacks and other organelles during mitosis and cytokinesis in plant cells. Plant Physiol. 2000; 124(1):135-51. PMC: 59129. DOI: 10.1104/pp.124.1.135. View

15.

McCloud T, Burns M, Majadly F, Muschik G, Miller D, Poole K . Production of brefeldin-A. J Ind Microbiol. 1995; 15(1):5-9. DOI: 10.1007/BF01570006. View

16.

Bubeck J, Scheuring D, Hummel E, Langhans M, Viotti C, Foresti O . The syntaxins SYP31 and SYP81 control ER-Golgi trafficking in the plant secretory pathway. Traffic. 2008; 9(10):1629-52. DOI: 10.1111/j.1600-0854.2008.00803.x. View

17.

Bonfanti L, Mironov Jr A, Martella O, Fusella A, Baldassarre M, Buccione R . Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation. Cell. 1999; 95(7):993-1003. DOI: 10.1016/s0092-8674(00)81723-7. View

18.

Nakano A, Luini A . Passage through the Golgi. Curr Opin Cell Biol. 2010; 22(4):471-8. DOI: 10.1016/j.ceb.2010.05.003. View

19.

Renna L, Hanton S, Stefano G, Bortolotti L, Misra V, Brandizzi F . Identification and characterization of AtCASP, a plant transmembrane Golgi matrix protein. Plant Mol Biol. 2005; 58(1):109-22. DOI: 10.1007/s11103-005-4618-4. View

20.

Fullekrug J, Sonnichsen B, Schafer U, Nguyen Van P, SOLING H, Mieskes G . Characterization of brefeldin A induced vesicular structures containing cycling proteins of the intermediate compartment/cis-Golgi network. FEBS Lett. 1997; 404(1):75-81. DOI: 10.1016/s0014-5793(97)00097-5. View