COPI-mediated retrieval of SCAP is crucial for regulating lipogenesis under basal and sterol-deficient conditions

Journal of Cell Science

Volumn 128, Issue 15, 2015, Pages 2805-2815

  Takashima, Kouhei ^a   Saitoh, Akina ^a   Funabashi, Teruki ^a   Hirose, Shohei ^a   Yagi, Chikako ^a   Nozaki, Shohei ^a   Sato, Ryuichiro ^b   Shin, Hye Won ^a   Nakayama, Kazuhisa ^a  

^a KYOTO UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

COPI coated vesicles; Golgi complex; Lipogenesis; SCAP; SREBP

Indexed keywords

STEROL REGULATORY ELEMENT BINDING PROTEIN; MBTPS2 PROTEIN, HUMAN; MEMBRANE PROTEIN; MEMBRANE-BOUND TRANSCRIPTION FACTOR PEPTIDASE, SITE 1; METALLOPROTEINASE; SERINE PROTEINASE; SIGNAL PEPTIDE; SREBP CLEAVAGE-ACTIVATING PROTEIN; STEROL;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; COPI-COATED VESICLE; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN; HUMAN CELL; LIPOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN TRANSPORT; COP-COATED VESICLE; ENZYME ACTIVATION; ENZYMOLOGY; GENETICS; HELA CELL LINE; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; COP-COATED VESICLES; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; GOLGI APPARATUS; HELA CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOGENESIS; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; PROPROTEIN CONVERTASES; PROTEIN TRANSPORT; SERINE ENDOPEPTIDASES; STEROL REGULATORY ELEMENT BINDING PROTEINS; STEROLS;

EID: 84974577124     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.164137     Document Type: Article

References (33)

1. Bartz, R., Sun, L.-P., Bisel, B., Wei, J.-H. and Seemann, J. (2008). Spatial separation of Golgi and ER during mitosis protects SREBP from unregulated activation. EMBO J. 27, 948-955.
2. Beller, M., Sztalryd, C., Southall, N., Bell, N., Jäckle, H., Auld, D.S. and Oliver, B. (2008). COPI complex is a regulator of lipid homeostasis. PLoS Biol. 6, e292.
3. DeBose-Boyd, R.A., Brown, M.S., Li, W.-P., Nohturfft, A., Goldstein, J.L. and Espenshade, P.J. (1999). Transport-dependent proteolysis of SREBP: relocation of site-1 protease from Golgi to ER obviates the need for SREBP transport to Golgi. Cell 99, 703-712.
4. Ellong, E.N., Soni, K.G., Bui, Q.-T., Sougrat, R., Golinelli-Cohen, M.-P. and Jackson, C.L. (2011). Interaction between the triglyceride lipase ATGL and the Arf1 activator GBF1. PLoS ONE 6, e21889.
5. Espenshade, P.J., Li, W.-P. and Yabe, D. (2002). Sterols block binding of COPII proteins to SCAP, thereby controlling SCAP sorting in ER. Proc. Natl. Acad. Sci. USA 99, 11694-11699.
6. Goldstein, J.L., DeBose-Boyd, R.A. and Brown, M.S. (2006). Protein sensors for membrane sterols. Cell 124, 35-46.
7. Griffiths, G., Fuller, S.D., Back, R., Hollinshead, M., Pfeiffer, S. and Simons, K. (1989). The dynamic nature of the Golgi complex. J. Cell Biol. 108, 277-297.
8. Guo, Y., Walther, T.C., Rao, M., Stuurman, N., Goshima, G., Terayama, K., Wong, J.S., Vale, R.D., Walter, P. and Farese, R.V., Jr. (2008). Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature 453, 657-661.
9. Harter, C. and Wieland, F. (1996). The secretory pathway: mechanisms of protein sorting and transport. Biochim. Biophys. Acta 1286, 75-93.
10. Horton, J.D., Goldstein, J.L. and Brown, M.S. (2002). SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Invest. 109, 1125-1131.
11. Hosaka, M., Toda, K., Takatsu, H., Torii, S., Murakami, K. and Nakayama, K. (1996). Structure and intracellular localization of mouse ADP-ribosylation factors type 1 to type 6 (ARF1-ARF6). J. Biochem. 120, 813-819.
12. Hua, X., Nohturfft, A., Goldstein, J.L. and Brown, M.S. (1996a). Sterol resistance in CHO cells traced to point mutation in SREBP cleavage-activating protein. Cell 87, 415-426.
13. Hua, X., Sakai, J., Brown, M.S. and Goldstein, J.L. (1996b). Regulated cleavage of sterol regulatory element binding proteins requires sequences on both sides of the endoplasmic reticulum membrane. J. Biol. Chem. 271, 10379-10384.
14. Irisawa, M., Inoue, J., Ozawa, N., Mori, K. and Sato, R. (2009). The sterol-sensing endoplasmic reticulum (ER) membrane protein TRC8 hampers ER to Golgi transport of sterol regulatory element-binding protein-2 (SREBP-2)/SREBP cleavage-activated protein and reduces SREBP-2 cleavage. J. Biol. Chem. 284, 28995-29004.
15. Jackson, C.L. (2000). Brefeldin A: revealing the fundamental principles governing membrane dynamics and protein transport. Subcell. Biochem. 34, 233-272.
16. Kitamura, T., Koshino, Y., Shibata, F., Oki, T., Nakajima, H., Nosaka, T. and Kumagai, H. (2003). Retrovirus-mediated gene transfer and expression cloning: powerful tools in functional genomics. Exp. Hematol. 31, 1007-1014.
17. Lowe, M. and Kreis, T.E. (1998). Regulation of membrane traffic in animal cells by COPI. Biochim. Biophys. Acta 1404, 53-66.
18. Makyio, H., Ohgi, M., Takei, T., Takahashi, S., Takatsu, H., Katoh, Y., Hanai, A., Ueda, T., Kanaho, Y., Xie, Y. et al. (2012). Structural basis for Arf6-MKLP1 complex formation on the Flemming body responsible for cytokinesis. EMBO J. 31, 2590-2603.
19. Nohturfft, A., Brown, M.S. and Goldstein, J.L. (1998). Sterols regulate processing of carbohydrate chains of wild-type SREBP cleavage-activating protein (SCAP), but not sterol-resistant mutants Y298C or D443N. Proc. Natl. Acad. Sci. USA 95, 12848-12853.
20. Nohturfft, A., DeBose-Boyd, R.A., Scheek, S., Goldstein, J.L. and Brown, M.S. (1999). Sterols regulate cycling of SREBP cleavage-activating protein (SCAP) between endoplasmic reticulum and Golgi. Proc. Natl. Acad. Sci. USA 96, 11235-11240.
21. Ohsaki, Y., Suzuki, M. and Fujimoto, T. (2014). Open questions in lipid droplet biology. Chem. Biol. 21, 86-96.
22. Saitoh, A., Shin, H.-W., Yamada, A., Waguri, S. and Nakayama, K. (2009). Three homologous ArfGAPs participate in coat protein I-mediated transport. J. Biol. Chem. 284, 13948-13957.
23. Sciaky,N., Presley, J., Smith,C., Zaal, K.J.M.,Cole, N.,Moreira, J.E., Terasaki,M., Siggia, E. and Lippincott-Schwartz, J. (1997). Golgi tubule traffic and the effects of brefeldin A visualized in living cells. J. Cell Biol. 139, 1137-1155.
24. Shao, W. and Espenshade, P.J. (2014). Sterol regulatory element-binding protein (SREBP) cleavage regulates Golgi-to-Endoplasmic Reticulum recycling of SREBP cleavage-activating protein (SCAP). J. Biol. Chem. 289, 7547-7557.
25. Shinotsuka, C., Yoshida, Y., Kawamoto, K., Takatsu, H. and Nakayama, K. (2002). Overexpression of an ADP-ribosylation factor-guanine nucleotide exchange factor, BIG2, uncouples brefeldin A-induced adaptor protein-1 coat dissociation and membrane tubulation. J. Biol. Chem. 277, 9468-9473.
26. Soni, K.G., Mardones, G.A., Sougrat, R., Smirnova, E., Jackson, C.L. and Bonifacino, J.S. (2009). Coatomer-dependent protein delivery to lipid droplets. J. Cell Sci. 122, 1834-1841.
27. Takashima,K., Saitoh,A., Hirose,S., Nakai,W.,Kondo,Y., Takasu, Y.,Kakeya,H., Shin, H.-W. and Nakayama, K. (2011). GBF1-Arf-COPI-ArfGAP-mediated Golgi-to-ER transport involved in regulation of lipid homeostasis. Cell Struct. Funct. 36, 223-235.
28. Thiam, A.R., Antonny, B., Wang, J., Delacotte, J., Wilfling, F., Walther, T.C., Beck, R., Rothman, J.E. and Pincet, F. (2013). COPI buds 60-nm lipid droplets from reconstituted water-phospholipid-triacylglyceride interfaces, suggesting a tension clamp function. Proc. Natl. Acad. Sci. USA 110, 13244-13249.
29. Tsuboi, H., Sugimoto, Y., Kainoh, T. and Ichikawa, A. (2004). Prostanoid EP4 receptor is involved in suppression of 3T3-L1 adipocyte differentiation. Biochem. Biophys. Res. Commun. 322, 1066-1072.
30. Watson, P. and Stephens, D.J. (2005). ER-to-Golgi transport: form and formation of vesicular and tubular carriers. Biochim. Biophys. Acta 1744, 304-315.
31. Wilfling, F., Haas, J.T., Walther, T.C. and Farese, R.V., Jr. (2014a). Lipid droplet biogenesis. Curr. Opin. Cell Biol. 29, 39-45.
32. Wilfling, F., Thiam, A.R., Olarte, M.-J.,Wang, J., Beck, R., Gould, T.J., Allgeyer, E.S., Pincet, F., Bewersdorf, J., Farese, R.V., Jr et al. (2014b). Arf1/COPI machinery acts directly on lipid droplets and enables their connection to the ER for protein targeting. Elife 3, e01607.
33. Yang, T., Espenshade, P.J., Wright, M.E., Yabe, D., Gong, Y., Aebersold, R., Goldstein, J.L. and Brown, M.S. (2002). Crucial step in cholesterol homeostasis: sterols promote binding of SCAP to INSIG-1, a membrane protein that facilitates retention of SREBPs in ER. Cell 110, 489-500.