A cascade of ER exit site assembly that is regulated by p125A and lipid signals

Journal of Cell Science

Volumn 127, Issue 8, 2014, Pages 1765-1778

  Klinkenberg, David ^a   Long, Kimberly R ^a   Shome, Kuntala ^a   Watkins, Simon C ^a   Aridor, Meir ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

COPII; ERES; p125A; Phosphatidylinositol 4 phosphate; Sec23ip

Indexed keywords

CARRIER PROTEIN; COAT PROTEIN COMPLEX II; LIPID; MEMBRANE PROTEIN; P125A PROTEIN; PHOSPHOLIPASE; POLYPHOSPHOINOSITIDE; UNCLASSIFIED DRUG; LIPOSOME; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; PHOSPHATIDYLINOSITOL 4-PHOSPHATE; PROTEIN BINDING; SAR1A PROTEIN, HUMAN; SEC13 PROTEIN, HUMAN; SEC16A PROTEIN, HUMAN; SEC23A PROTEIN, HUMAN; SEC23IP PROTEIN, HUMAN; SEC24A PROTEIN, HUMAN; SEC31A PROTEIN, HUMAN; VESICULAR TRANSPORT PROTEIN;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; IN VITRO STUDY; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; CHEMICAL PHENOMENA; CHEMISTRY; HELA CELL LINE; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

CARRIER PROTEINS; ENDOPLASMIC RETICULUM; HELA CELLS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPOSOMES; MONOMERIC GTP-BINDING PROTEINS; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; VESICULAR TRANSPORT PROTEINS;

EID: 84898860931     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.138784     Document Type: Article

References (49)

1. Antonny, B. and Schekman, R. (2001). ER export: public transportation by the COPII coach. Curr. Opin. Cell Biol. 13, 438-443.
2. Antonny, B., Madden, D., Hamamoto, S., Orci, L. and Schekman, R. (2001). Dynamics of the COPII coat with GTP and stable analogues. Nat. Cell Biol. 3, 531-537.
3. Aridor, M., Bannykh, S. I., Rowe, T. and Balch, W. E. (1995). Sequential coupling between COPII and COPI vesicle coats in endoplasmic reticulum to Golgi transport. J. Cell Biol. 131, 875-893.
4. Aridor, M., Weissman, J., Bannykh, S., Nuoffer, C. and Balch, W. E. (1998). Cargo selection by the COPII budding machinery during export from the ER. J. Cell Biol. 141, 61-70.
5. Aridor, M., Fish, K. N., Bannykh, S., Weissman, J., Roberts, T. H., Lippincott-Schwartz, J. and Balch, W. E. (2001). The Sar1 GTPase coordinates biosynthetic cargo selection with endoplasmic reticulum export site assembly. J. Cell Biol. 152, 213-230.
6. Arimitsu, N., Kogure, T., Baba, T., Nakao, K., Hamamoto, H., Sekimizu, K., Yamamoto, A., Nakanishi, H., Taguchi, R., Tagaya, M. et al. (2011). p125/Sec23-interacting protein (Sec23ip) is required for spermiogenesis. FEBS Lett. 585, 2171-2176.
7. Audhya, A., Foti, M. and Emr, S. D. (2000). Distinct roles for the yeast phosphatidylinositol 4-kinases, Stt4p and Pik1p, in secretion, cell growth, and organelle membrane dynamics. Mol. Biol. Cell 11, 2673-2689.
8. Bielli, A., Haney, C. J., Gabreski, G., Watkins, S. C., Bannykh, S. I. and Aridor, M. (2005). Regulation of Sar1 NH2 terminus by GTP binding and hydrolysis promotes membrane deformation to control COPII vesicle fission. J. Cell Biol. 171, 919-924.
9. Blumental-Perry, A., Haney, C. J., Weixel, K. M., Watkins, S. C., Weisz, O. A. and Aridor, M. (2006). Phosphatidylinositol 4-phosphate formation at ER exit sites regulates ER export. Dev. Cell 11, 671-682.
10. Farhan, H., Weiss, M., Tani, K., Kaufman, R. J. and Hauri, H. P. (2008). Adaptation of endoplasmic reticulum exit sites to acute and chronic increases in cargo load. EMBO J. 27, 2043-2054.
11. Fath, S., Mancias, J. D., Bi, X. and Goldberg, J. (2007). Structure and organization of coat proteins in the COPII cage. Cell 129, 1325-1336.
12. Forster, R., Weiss, M., Zimmermann, T., Reynaud, E. G., Verissimo, F., Stephens, D. J. and Pepperkok, R. (2006). Secretory cargo regulates the turnover of COPII subunits at single ER exit sites. Curr. Biol. 16, 173-179.
13. Frangioni, J. V. and Neel, B. G. (1993). Solubilization and purification of enzymatically active glutathione S-transferase (pGEX) fusion proteins. Anal. Biochem. 210, 179-187.
14. Fromme, J. C., Ravazzola, M., Hamamoto, S., Al-Balwi, M., Eyaid, W., Boyadjiev, S. A., Cosson, P., Schekman, R. and Orci, L. (2007). The genetic basis of a craniofacial disease provides insight into COPII coat assembly. Dev. Cell 13, 623-634.
15. Hughes, H., Budnik, A., Schmidt, K., Palmer, K. J., Mantell, J., Noakes, C., Johnson, A., Carter, D. A., Verkade, P., Watson, P. et al. (2009). Organisation of human ER-exit sites: requirements for the localisation of Sec16 to transitional ER. J. Cell Sci. 122, 2924-2934.
16. Iinuma, T., Shiga, A., Nakamoto, K., O'Brien, M. B., Aridor, M., Arimitsu, N., Tagaya, M. and Tani, K. (2007). Mammalian Sec16/p250 plays a role in membrane traffic from the endoplasmic reticulum. J. Biol. Chem. 282, 17632-17639.
17. Inoue, H., Baba, T., Sato, S., Ohtsuki, R., Takemori, A.,Watanabe, T., Tagaya, M. and Tani, K. (2012). Roles of SAM and DDHD domains in mammalian intracellular phospholipase A1 KIAA0725p. Biochim. Biophys. Acta 1823, 930-939.
18. Knight, M. J., Joubert, M. K., Plotkowski, M. L., Kropat, J., Gingery, M., Sakane, F., Merchant, S. S. and Bowie, J. U. (2010). Zinc binding drives sheet formation by the SAM domain of diacylglycerol kinase d. Biochemistry 49, 9667-9676.
19. Kuehn, M. J., Herrmann, J. M. and Schekman, R. (1998). COPII-cargo interactions direct protein sorting into ER-derived transport vesicles. Nature 391, 187-190.
20. Kung, L. F., Pagant, S., Futai, E., D'Arcangelo, J. G., Buchanan, R., Dittmar, J. C., Reid, R. J., Rothstein, R., Hamamoto, S., Snapp, E. L. et al. (2012). Sec24p and Sec16p cooperate to regulate the GTP cycle of the COPII coat. EMBO J. 31, 1014-1027.
21. Lee, M. C., Orci, L., Hamamoto, S., Futai, E., Ravazzola, M. and Schekman, R. (2005). Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell 122, 605-617.
22. Litvak, V., Dahan, N., Ramachandran, S., Sabanay, H. and Lev, S. (2005). Maintenance of the diacylglycerol level in the Golgi apparatus by the Nir2 protein is critical for Golgi secretory function. Nat. Cell Biol. 7, 225-234.
23. Long, K. R., Yamamoto, Y., Baker, A. L., Watkins, S. C., Coyne, C. B., Conway, J. F. and Aridor, M. (2010). Sar1 assembly regulates membrane constriction and ER export. J. Cell Biol. 190, 115-128.
24. Lorente-Rodríguez, A. and Barlowe, C. (2011). Requirement for Golgi-localized PI(4)P in fusion of COPII vesicles with Golgi compartments. Mol. Biol. Cell 22, 216-229.
25. Matsuoka, K., Orci, L., Amherdt, M., Bednarek, S. Y., Hamamoto, S., Schekman, R. and Yeung, T. (1998). COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes. Cell 93, 263-275.
26. McGary, K. L., Park, T. J., Woods, J. O., Cha, H. J., Wallingford, J. B. and Marcotte, E. M. (2010). Systematic discovery of nonobvious human disease models through orthologous phenotypes. Proc. Natl. Acad. Sci. USA 107, 6544-6549.
27. Mezzacasa, A. and Helenius, A. (2002). The transitional ER defines a boundary for quality control in the secretion of tsO45 VSV glycoprotein. Traffic 3, 833-849.
28. Miller, E. A., Beilharz, T. H., Malkus, P. N., Lee, M. C., Hamamoto, S., Orci, L. and Schekman, R. (2003). Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell 114, 497-509.
29. Mizoguchi, T., Nakajima, K., Hatsuzawa, K., Nagahama, M., Hauri, H. P., Tagaya, M. and Tani, K. (2000). Determination of functional regions of p125, a novel mammalian Sec23p-interacting protein. Biochem. Biophys. Res. Commun. 279, 144-149.
30. Nagaya, H., Wada, I., Jia, Y. J. and Kanoh, H. (2002). Diacylglycerol kinase delta suppresses ER-to-Golgi traffic via its SAM and PH domains. Mol. Biol. Cell 13, 302-316.
31. Nakajima, K., Sonoda, H., Mizoguchi, T., Aoki, J., Arai, H., Nagahama, M., Tagaya, M. and Tani, K. (2002). A novel phospholipase A1 with sequence homology to a mammalian Sec23p-interacting protein, p125. J. Biol. Chem. 277, 11329-11335.
32. Nakatsu, F., Perera, R. M., Lucast, L., Zoncu, R., Domin, J., Gertler, F. B., Toomre, D. and De Camilli, P. (2010). The inositol 5-phosphatase SHIP2 regulates endocytic clathrin-coated pit dynamics. J. Cell Biol. 190, 307-315.
33. Ong, Y. S., Tang, B. L., Loo, L. S. and Hong, W. (2010). p125A exists as part of the mammalian Sec13/Sec31 COPII subcomplex to facilitate ER-Golgi transport. J. Cell Biol. 190, 331-345.
34. Pathre, P., Shome, K., Blumental-Perry, A., Bielli, A., Haney, C. J., Alber, S., Watkins, S. C., Romero, G. and Aridor, M. (2003). Activation of phospholipase D by the small GTPase Sar1p is required to support COPII assembly and ER export. EMBO J. 22, 4059-4069.
35. Qiao, F. and Bowie, J. U. (2005). The many faces of SAM. Sci. STKE 2005, re7.
36. Raaijmakers, J. H., Deneubourg, L., Rehmann, H., de Koning, J., Zhang, Z., Krugmann, S., Erneux, C. and Bos, J. L. (2007). The PI3K effector Arap3 interacts with the PI(3,4,5)P3 phosphatase SHIP2 in a SAM domain-dependent manner. Cell. Signal. 19, 1249-1257.
37. Rowe, T. and Balch,W. E. (1995). Expression and purification of mammalian Sarl. Methods Enzymol. 257, 49-53.
38. Rowe, T., Aridor, M., McCaffery, J. M., Plutner, H., Nuoffer, C. and Balch, W. E. (1996). COPII vesicles derived from mammalian endoplasmic reticulum microsomes recruit COPI. J. Cell Biol. 135, 895-911.
39. Saraste, J. and Svensson, K. (1991). Distribution of the intermediate elements operating in ER to Golgi transport. J. Cell Sci. 100, 415-430.
40. Sato, S., Inoue, H., Kogure, T., Tagaya, M. and Tani, K. (2010). Golgi-localized KIAA0725p regulates membrane trafficking from the Golgi apparatus to the plasma membrane in mammalian cells. FEBS Lett. 584, 4389-4395.
41. Shimoi, W., Ezawa, I., Nakamoto, K., Uesaki, S., Gabreski, G., Aridor, M., Yamamoto, A., Nagahama, M., Tagaya, M. and Tani, K. (2005). p125 is localized in endoplasmic reticulum exit sites and involved in their organization. J. Biol. Chem. 280, 10141-10148.
42. Stagg, S. M., LaPointe, P., Razvi, A., Gürkan, C., Potter, C. S., Carragher, B. and Balch, W. E. (2008). Structural basis for cargo regulation of COPII coat assembly. Cell 134, 474-484.
43. Supek, F., Madden, D. T., Hamamoto, S., Orci, L. and Schekman, R. (2002). Sec16p potentiates the action of COPII proteins to bud transport vesicles. J. Cell Biol. 158, 1029-1038.
44. Tani, K., Mizoguchi, T., Iwamatsu, A., Hatsuzawa, K. and Tagaya, M. (1999). p125 is a novel mammalian Sec23p-interacting protein with structural similarity to phospholipid-modifying proteins. J. Biol. Chem. 274, 20505-20512.
45. Weixel, K. M., Blumental-Perry, A., Watkins, S. C., Aridor, M. and Weisz, O. A. (2005). Distinct Golgi populations of phosphatidylinositol 4-phosphate regulated by phosphatidylinositol 4-kinases. J. Biol. Chem. 280, 10501-10508.
46. Whittle, J. R. and Schwartz, T. U. (2010). Structure of the Sec13-Sec16 edge element, a template for assembly of the COPII vesicle coat. J. Cell Biol. 190, 347-361.
47. Yamashita, A., Kumazawa, T., Koga, H., Suzuki, N., Oka, S. and Sugiura, T. (2010). Generation of lysophosphatidylinositol by DDHD domain containing 1 (DDHD1): Possible involvement of phospholipase D/phosphatidic acid in the activation of DDHD1. Biochim. Biophys. Acta 1801, 711-720.
48. Yorimitsu, T. and Sato, K. (2012). Insights into structural and regulatory roles of Sec16 in COPII vesicle formation at ER exit sites. Mol. Biol. Cell 23, 2930-2942.
49. Zanetti, G., Pahuja, K. B., Studer, S., Shim, S. and Schekman, R. (2011). COPII and the regulation of protein sorting in mammals. Nat. Cell Biol. 14, 20-28.