Apoptosis-linked gene-2 (ALG-2)/Sec31 interactions regulate endoplasmic reticulum (ER)-to-Golgi transport: A potential effector pathway for luminal calcium

Journal of Biological Chemistry

Volumn 289, Issue 34, 2014, Pages 23609-23628

  Helm, Jared R ^a   Bentley, Marvin ^a,c   Thorsen, Kevin D ^a   Wang, Ting ^a   Foltz, Lauren ^a   Oorschot, Viola ^b   Klumperman, Judith ^b   Hay, Jesse C ^a  

^a UNIVERSITY OF MONTANA   (United States)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; CELL MEMBRANES; GENES; MACHINERY; PROTEINS;

CALCIUM DEPLETION; ENDOPLASMIC RETICULUM; PROTEIN INTERACTION; SECRETORY PATHWAYS; TRANSPORT RATE; ULTRASTRUCTURAL ANALYSIS; VESICLE TRAFFICKING; VESICLE TRANSPORT;

CALCIUM;

APOPTOSIS LINKED GENE 2 PROTEIN; CALCIUM ION; COAT PROTEIN COMPLEX II; GAG PROTEIN; MEMBRANE PROTEIN; P115 PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; CALCIUM; CALCIUM BINDING PROTEIN; PDCD6 PROTEIN, HUMAN; PROTEIN BINDING; SEC31A PROTEIN, HUMAN; SMALL INTERFERING RNA; VESICULAR TRANSPORT PROTEIN;

ARTICLE; BINDING SITE; CALCIUM DEPLETION; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; INTRACELLULAR TRANSPORT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROLINE RICH PROTEIN DOMAIN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; CELL LINE; FLUORESCENCE MICROSCOPY; GENETICS; HUMAN; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

APOPTOSIS REGULATORY PROTEINS; BIOLOGICAL TRANSPORT; CALCIUM; CALCIUM-BINDING PROTEINS; CELL LINE; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HUMANS; MICROSCOPY, FLUORESCENCE; PROTEIN BINDING; RNA, SMALL INTERFERING; VESICULAR TRANSPORT PROTEINS;

EID: 84906544287     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.561829     Document Type: Article

References (75)

1. Bi, X., Mancias, J. D., and Goldberg, J. (2007) Insights into COPII coat nucleation from the structure of Sec23.Sar1 complexed with the active fragment of Sec31. Dev. Cell 13, 635-645
2. Hughes, H., and Stephens, D. J. (2008) Assembly, organization, and function of the COPII coat. Histochem. Cell Biol. 129, 129-151
3. Miller, E. A., and Barlowe, C. (2010) Regulation of coat assembly: sorting things out at the ER. Curr. Opin. Cell Biol. 22, 447-453
4. 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
5. Tabata, K. V., Sato, K., Ide, T., Nishizaka, T., Nakano, A., and Noji, H. (2009) Visualization of cargo concentration by COPII minimal machinery in a planar lipid membrane. EMBO J. 28, 3279-3289
6. Cai, H., Yu, S., Menon, S., Cai, Y., Lazarova, D., Fu, C., Reinisch, K., Hay, J. C., and Ferro-Novick, S. (2007) TRAPPI tethers COPII vesicles by binding the coat subunit Sec23. Nature 445, 941-944
7. Lord, C., Bhandari, D., Menon, S., Ghassemian, M., Nycz, D., Hay, J., Ghosh, P., and Ferro-Novick, S. (2011) Sequential interactions with Sec23 control the direction of vesicle traffic. Nature 473, 181-186
8. Trahey, M., and Hay, J. C. (2010) Transport vesicle uncoating: it's later than you think. F1000 Biol. Rep. 2, 47
9. Barlowe, C., Orci, L., Yeung, T., Hosobuchi, M., Hamamoto, S., Salama, N., Rexach, M. F., Ravazzola, M., Amherdt, M., and Schekman, R. (1994) COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77, 895-907
10. Bentley, M., Nycz, D. C., Joglekar, A., Fertschai, I., Malli, R., Graier, W. F., and Hay, J. C. (2010) Vesicular calcium regulates coat retention, fusogenicity, and size of pre-Golgi intermediates. Mol. Biol. Cell 21, 1033-1046
11. Angers, C. G., and Merz, A. J. (2011) New links between vesicle coats and Rab-mediated vesicle targeting. Semin. Cell Dev. Biol. 22, 18-26
12. Xu, D., and Hay, J. C. (2004) Reconstitution of COPII vesicle fusion to generate a pre-Golgi intermediate compartment. J. Cell Biol. 167, 997-1003
13. Yu, S., Satoh, A., Pypaert, M., Mullen, K., Hay, J. C., and Ferro-Novick, S. (2006) mBet3p is required for homotypic COPII vesicle tethering in mammalian cells. J. Cell Biol. 174, 359-368
14. Bentley, M., Liang, Y., Mullen, K., Xu, D., Sztul, E., and Hay, J. C. (2006) SNARE status regulates tether recruitment and function in homotypic COPII vesicle fusion. J. Biol. Chem. 281, 38825-38833
15. Allan, B. B., Moyer, B. D., and Balch, W. E. (2000) Rab1 recruitment of p115 into a cis-SNARE complex: programming budding COPII vesicles for fusion. Science 289, 444-448
16. Martínez-Menárguez, J. A., Geuze, H. J., Slot, J. W., and Klumperman, J. (1999) Vesicular tubular clusters between the ER and Golgi mediate concentration of soluble secretory proteins by exclusion from COPI-coated vesicles. Cell 98, 81-90
17. Beckers, C. J., and Balch, W. E. (1989) Calcium and GTP: essential components in vesicular trafficking between the endoplasmic reticulum and Golgi apparatus. J. Cell Biol. 108, 1245-1256
18. Porat, A., and Elazar, Z. (2000) Regulation of intra-Golgi membrane transport by calcium. J. Biol. Chem. 275, 29233-29237
19. Colombo, M. I., Beron, W., and Stahl, P. D. (1997) Calmodulin regulates endosome fusion. J. Biol. Chem. 272, 7707-7712
20. Peters, C., and Mayer, A. (1998) Ca2+/calmodulin signals the completion of docking and triggers a late step of vacuole fusion. Nature 396, 575-580
21. Pryor, P. R., Mullock, B. M., Bright, N. A., Gray, S. R., and Luzio, J. P. (2000) The role of intraorganellar Ca2+ in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J. Cell Biol. 149, 1053-1062
22. Burgoyne, R. D., and Clague, M. J. (2003) Calcium and calmodulin in membrane fusion. Biochim. Biophys. Acta 1641, 137-143
23. Chen, J.-L., Ahluwalia, J. P., and Stamnes, M. (2002) Selective effects of calcium chelators on anterograde and retrograde protein transport in the cell. J. Biol. Chem. 277, 35682-35687
24. Hu, Z., Bonifas, J. M., Beech, J., Bench, G., Shigihara, T., Ogawa, H., Ikeda, S., Mauro, T., and Epstein, E. H. (2000) Mutations in ATP2C1, encoding a calcium pump, cause Hailey-Hailey disease. Nat. Genet. 24, 61-65
25. Sepúlveda, M. R., Vanoevelen, J., Raeymaekers, L., Mata, A. M., and Wuytack, F. (2009) Silencing the SPCA1 (secretory pathway Ca2+-ATPase isoform 1) impairs Ca2+ homeostasis in the Golgi and disturbs neural polarity. J. Neurosci. 29, 12174-12182
26. Micaroni, M., Perinetti, G., Berrie, C. P., and Mironov, A. A. (2010) The SPCA1 Ca2+ pump and intracellular membrane trafficking. Traffic 11, 1315-1333
27. von Blume, J., Alleaume, A.-M., Cantero-Recasens, G., Curwin, A., Carreras-Sureda, A., Zimmermann, T., van Galen, J., Wakana, Y., Valverde, M. A., and Malhotra, V. (2011) ADF/cofilin regulates secretory cargo sorting at the TGN via the Ca2+ ATPase SPCA1. Dev. Cell 20, 652-662
28. von Blume, J., Alleaume, A.-M., Kienzle, C., Carreras-Sureda, A., Valverde, M., and Malhotra, V. (2012) Cab45 is required for Ca2+-dependent secretory cargo sorting at the trans-Golgi network. J. Cell Biol. 199, 1057-1066
29. Micaroni, M. (2012) Calcium around the Golgi apparatus: implications for intracellular membrane trafficking. Adv. Exp. Med. Biol. 740, 439-460
30. Brown, W. J., Chambers, K., and Doody, A. (2003) Phospholipase A2 (PLA2) enzymes in membrane trafficking: mediators of membrane shape and function. Traffic 4, 214-221
31. Ahluwalia, J. P., Topp, J. D., Weirather, K., Zimmerman, M., and Stamnes, M. (2001) A role for calcium in stabilizing transport vesicle coats. J. Biol. Chem. 276, 34148-34155
32. Shibata, H., Inuzuka, T., Yoshida, H., Sugiura, H., Wada, I., and Maki, M. (2010) The ALG-2 binding site in Sec31A influences the retention kinetics of Sec31A at the endoplasmic reticulum exit sites as revealed by live-cell time-lapse imaging. Biosci. Biotechnol. Biochem. 74, 1819-1826
33. Shibata, H., Suzuki, H., Yoshida, H., and Maki, M. (2007) ALG-2 directly binds Sec31A and localizes at endoplasmic reticulum exit sites in a Ca2+- dependent manner. Biochem. Biophys. Res. Commun. 353, 756-763
34. la Cour, J. M., Mollerup, J., and Berchtold, M. W. (2007) ALG-2 oscillates in subcellular localization, unitemporally with calcium oscillations. Biochem. Biophys. Res. Commun. 353, 1063-1067
35. Yamasaki, A., Tani, K., Yamamoto, A., Kitamura, N., and Komada, M. (2006) The Ca2+-binding protein ALG-2 is recruited to endoplasmic reticulum exit sites by Sec31A and stabilizes the localization of Sec31A. Mol. Biol. Cell 17, 4876-4887
36. la Cour, J. M., Schindler, A. J., Berchtold, M. W., and Schekman, R. (2013) ALG-2 attenuates COPII budding in vitro and stabilizes the Sec23/Sec31A complex. PLoS One 8, e75309
37. Hay, J. C., Klumperman, J., Oorschot, V., Steegmaier, M., Kuo, C. S., and Scheller, R. H. (1998) Localization, dynamics, and protein interactions reveal distinct roles for ER and Golgi SNAREs. J. Cell Biol. 141, 1489-1502
38. Lefrancois, L., and Lyles, D. S. (1982) The interaction of antibody with the major surface glycoprotein of vesicular stomatitis virus. I. Analysis of neutralizing epitopes with monoclonal antibodies. Virology 121, 157-167
39. Thayanidhi, N., Helm, J. R., Nycz, D. C., Bentley, M., Liang, Y., and Hay, J. C. (2010) α-Synuclein delays endoplasmic reticulum (ER)-to-Golgi transport in mammalian cells by antagonizing ER/Golgi SNAREs. Mol. Biol. Cell 21, 1850-1863
40. Gordon, D. E., Bond, L. M., Sahlender, D. A., and Peden, A. A. (2010) A targeted siRNA screen to identify SNAREs required for constitutive secretion in mammalian cells. Traffic 11, 1191-1204
41. Slot, J. W., and Geuze, H. J. (2007) Cryosectioning and immunolabeling. Nat. Protoc. 2, 2480-2491
42. Flanagan, J. J., and Barlowe, C. (2006) Cysteine-disulfide cross-linking to monitor SNARE complex assembly during endoplasmic reticulum-Golgi transport. J. Biol. Chem. 281, 2281-2288
43. Mason, M. J., Garcia-Rodriguez, C., and Grinstein, S. (1991) Coupling between intracellular Ca2+ stores and the Ca2+ permeability of the plasma membrane. Comparison of the effects of thapsigargin, 2,5-di-(tert-butyl)-1,4- hydroquinone, and cyclopiazonic acid in rat thymic lymphocytes. J. Biol. Chem. 266, 20856-20862
44. Gallione, C. J., and Rose, J. K. (1985) A single amino acid substitution in a hydrophobic domain causes temperature-sensitive cell-surface transport of a mutant viral glycoprotein. J. Virol. 54, 374-382
45. Amodio, G., Renna, M., Paladino, S., Venturi, C., Tacchetti, C., Moltedo, O., Franceschelli, S., Mallardo, M., Bonatti, S., and Remondelli, P. (2009) Endoplasmic reticulum stress reduces the export from the ER and alters the architecture of post-ER compartments. Int. J. Biochem. Cell Biol. 41, 2511-2521
46. Hughes, H., Budnik, A., Schmidt, K., Palmer, K. J., Mantell, J., Noakes, C., Johnson, A., Carter, D. A., Verkade, P., Watson, P., and Stephens, D. J. (2009) Organisation of human ER-exit sites: requirements for the localisation of Sec16 to transitional ER. J. Cell Sci. 122, 2924-2934
47. Maki, M., and Shibata, H. (2007) The penta-EF-hand protein ALG-2 and its interacting proteins. Calcium Binding Proteins 2, 4-10
48. Shibata, H., Suzuki, H., Kakiuchi, T., Inuzuka, T., Yoshida, H., Mizuno, T., and Maki, M. (2008) Identification of Alix-type and non-Alix-type ALG-2-binding sites in human phospholipid scramblase 3: differential binding to an alternatively spliced isoform and amino acid-substituted mutants. J. Biol. Chem. 283, 9623-9632
49. Bonnon, C., Wendeler, M. W., Paccaud, J.-P., and Hauri, H.-P. (2010) Selective export of human GPI-Anchored proteins from the endoplasmic reticulum. J. Cell Sci. 123, 1705-1715
50. Strating, J. R. P. M., and Martens, G. J. M. (2009) The p24 family and selective transport processes at the ER-Golgi interface. Biol. Cell 101, 495-509
51. Aguilera-Romero, A., Kaminska, J., Spang, A., Riezman, H., and Muñiz, M. (2008) The yeast p24 complex is required for the formation of COPI retrograde transport vesicles from the Golgi apparatus. J. Cell Biol. 180, 713-720
52. Mukhopadhyay, S., Bachert, C., Smith, D. R., and Linstedt, A. D. (2010) Manganese-induced trafficking and turnover of the cis-Golgi glycoprotein GPP130. Mol. Biol. Cell 21, 1282-1292
53. Contreras, I., Yang, Y., Robinson, D. G., and Aniento, F. (2004) Sorting signals in the cytosolic tail of plant p24 proteins involved in the interaction with the COPII coat. Plant Cell Physiol. 45, 1779-1786
54. Dominguez, M., Dejgaard, K., Füllekrug, J., Dahan, S., Fazel, A., Paccaud, J. P., Thomas, D. Y., Bergeron, J. J., and Nilsson, T. (1998) gp25L/emp24/p24 protein family members of the cis-Golgi network bind bothCOPI and II coatomer. J. Cell Biol. 140, 751-765
55. Brandon, E., Szul, T., Alvarez, C., Grabski, R., Benjamin, R., Kawai, R., and Sztul, E. (2006) On and off membrane dynamics of the endoplasmic reticulum-Golgi tethering factor p115 in vivo. Mol. Biol. Cell 17, 2996-3008
56. Shaywitz, D. A., Espenshade, P. J., Gimeno, R. E., and Kaiser, C. A. (1997) COPII subunit interactions in the assembly of the vesicle coat. J. Biol. Chem. 272, 25413-25416
57. Higashio, H., and Kohno, K. (2002) A genetic link between the unfolded protein response and vesicle formation from the endoplasmic reticulum. Biochem. Biophys. Res. Commun. 296, 568-574
58. Sato, M., Sato, K., and Nakano, A. (2002) Evidence for the intimate relationship between vesicle budding from the ER and the unfolded protein response. Biochem. Biophys. Res. Commun. 296, 560-567
59. Kitaura, Y., Matsumoto, S., Satoh, H., Hitomi, K., and Maki, M. (2001) Peflin and ALG-2, members of the penta-EF-hand protein family, form a heterodimer that dissociates in a Ca2+-dependent manner. J. Biol. Chem. 276, 14053-14058
60. Kung, L. F., Pagant, S., Futai, E., D'Arcangelo, J. G., Buchanan, R., Dittmar, J. C., Reid, R. J. D., Rothstein, R., Hamamoto, S., Snapp, E. L., Schekman, R., and Miller, E. A. (2012) Sec24p and Sec16p cooperate to regulate the GTP cycle of the COPII coat. EMBO J. 31, 1014-1027
61. Gillon, A. D., Latham, C. F., and Miller, E. A. (2012) Vesicle-mediated ER export of proteins and lipids. Biochim. Biophys. Acta 1821, 1040-1049
62. Appenzeller-Herzog, C., Roche, A.-C., Nufer, O., and Hauri, H.-P. (2004) pH-induced conversion of the transport lectin ERGIC-53 triggers glycoprotein release. J. Biol. Chem. 279, 12943-12950
63. Zhang, B., Kaufman, R. J., and Ginsburg, D. (2005) LMAN1 and MCFD2 form a cargo receptor complex and interact with coagulation factor VIII in the early secretory pathway. J. Biol. Chem. 280, 25881-25886
64. Mitrovic, S., Ben-Tekaya, H., Koegler, E., Gruenberg, J., and Hauri, H.-P. (2008) The cargo receptors Surf4, endoplasmic reticulum-Golgi intermediate compartment (ERGIC)-53, and p25 are required to maintain the architecture of ERGIC and Golgi. Mol. Biol. Cell 19, 1976-1990
65. Takida, S., Maeda, Y., and Kinoshita, T. (2008) Mammalian GPI-Anchored proteins require p24 proteins for their efficient transport from the ER to the plasma membrane. Biochem. J. 409, 555-562
66. Muñiz, M., Nuoffer, C., Hauri, H. P., and Riezman, H. (2000) The Emp24 complex recruits a specific cargo molecule into endoplasmic reticulumderived vesicles. J. Cell Biol. 148, 925-930
67. Bartoszewski, S., Luschnig, S., Desjeux, I., Grosshans, J., and Nüsslein- Volhard, C. (2004) Drosophila p24 homologues eclair and baiser are necessary for the activity of the maternally expressed Tkv receptor during early embryogenesis. Mech. Dev. 121, 1259-1273
68. Buechling, T., Chaudhary, V., Spirohn, K., Weiss, M., and Boutros, M. (2011) p24 proteins are required for secretion of Wnt ligands. EMBO Rep. 12, 1265-1272
69. Port, F., Hausmann, G., and Basler, K. (2011) A genome-wide RNA interference screen uncovers two p24 proteins as regulators of Wingless secretion. EMBO Rep. 12, 1144-1152
70. Béthune, J., Kol, M., Hoffmann, J., Reckmann, I., Brügger, B., and Wieland, F. (2006) Coatomer, the coat protein of COPI transport vesicles, discriminates endoplasmic reticulum residents from p24 proteins. Mol. Cell. Biol. 26, 8011-8021
71. Barr, F. A., Preisinger, C., Kopajtich, R., and Körner, R. (2001) Golgi matrix proteins interact with p24 cargo receptors and aid their efficient retention in the Golgi apparatus. J. Cell Biol. 155, 885-891
72. Füllekrug, J., Suganuma, T., Tang, B. L., Hong, W., Storrie, B., and Nilsson, T. (1999) Localization and recycling of gp27 (hp24γ3): complex formation with other p24 family members. Mol. Biol. Cell 10, 1939-1955
73. Belden, W. J., and Barlowe, C. (1996) Erv25p, a component of COPIIcoated vesicles, forms a complex with Emp24p that is required for efficient endoplasmic reticulum to Golgi transport. J. Biol. Chem. 271, 26939-26946
74. Denzel, A., Otto, F., Girod, A., Pepperkok, R., Watson, R., Rosewell, I., Bergeron, J. J., Solari, R. C., and Owen, M. J. (2000) The p24 family member p23 is required for early embryonic development. Curr. Biol. 10, 55-58
75. Rötter, J., Kuiper, R. P., Bouw, G., and Martens, G. J. M. (2002) Cell-typespecific and selectively induced expression of members of the p24 family of putative cargo receptors. J. Cell Sci. 115, 1049-1058