TANGO1 recruits Sec 16 to coordinately organize ER exit sites for efficient secretion

Journal of Cell Biology

Volumn 216, Issue 6, 2017, Pages 1731-1743

  Maeda, Miharu ^a   Katada, Toshiaki ^a,b   Saito, Kota ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b MUSASHINO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COAT PROTEIN COMPLEX II; COLLAGEN RECEPTOR; CTAGE5 PROTEIN; FK 506 BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; RECOMBINANT PROTEIN; SEC16 PROTEIN; SMALL INTERFERING RNA; TANGO1 PROTEIN; TANGO1L PROTEIN; TANGO1S PROTEIN; UNCLASSIFIED DRUG; ARNT PROTEIN, HUMAN; COATOMER PROTEIN; CTAGE5 PROTEIN, HUMAN; DNA BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; HYPOXIA INDUCIBLE FACTOR 1BETA; PREB PROTEIN, HUMAN; PROTEIN BINDING; SEC16A PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TUMOR ANTIGEN; TUMOR PROTEIN; VESICULAR TRANSPORT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING ASSAY; CARBOXY TERMINAL SEQUENCE; CELL LYSATE; CONTROLLED STUDY; CYTOPLASM; ENDOPLASMIC RETICULUM; FEMALE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; IN VITRO STUDY; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; RAT; WESTERN BLOTTING; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PROTEIN DOMAIN; RNA INTERFERENCE; SECRETION (PROCESS); SIGNAL TRANSDUCTION; TIME FACTOR;

ANTIGENS, NEOPLASM; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; COATOMER PROTEIN; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HELA CELLS; HUMANS; NEOPLASM PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSFECTION; VESICULAR TRANSPORT PROTEINS;

EID: 85021838626     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201703084     Document Type: Article

References (67)

1. Aguilera-Gomez, A., M.M. van Oorschot, T. Veenendaal, and C. Rabouille. 2016. In vivo vizualisation of mono-ADP-ribosylation by dPARP16 upon amino-acid starvation. eLife. 5:e21475. http://dx.doi.org/10.7554/eLife.21475
2. Antonny, B., D. Madden, S. Hamamoto, L. Orci, and R. Schekman. 2001. Dynamics of the COP II coat with GTP and stable analogues. Nat. Cell Biol. 3:531-537. http://dx.doi.org/10.1038/35078500
3. Aridor, M., J. Weissman, S. Bannykh, C. Nuoffer, and W.E. Balch. 1998. Cargo selection by the COP II budding machinery during export from the ER. J. Cell Biol. 141:61-70. http://dx.doi.org/10.1083/jcb.141.1.61
4. Bannykh, S.I., T. Rowe, and W.E. Balch. 1996. The organization of endoplasmic reticulum export complexes. J. Cell Biol. 135:19-35. http://dx.doi.org/10..1083/jcb.135.1.19
5. Bard, F., L. Casano, A. Mallabiabarrena, E. Wallace, K. Saito, H. Kitayama, G. Guizzunti, Y. Hu, F. Wendler, R. Dasgupta, et al. 2006. Functional genomics reveals genes involved in protein secretion and Golgi organization. Nature. 439:604-607. http://dx.doi.org/10.1038/nature04377
6. Barlowe, C., and R. Schekman. 1993. SEC12 encodes a guanine-nucleotideexchange factor essential for transport vesicle budding from the ER. Nature. 365:347-349. http://dx.doi.org/10.1038/365347a0
7. Bharucha, N., Y. Liu, E. Papanikou, C. McMahon, M. Esaki, P.D. Jeffrey, F.M. Hughson, and B.S. Glick. 2013. Sec16 influences transitional ER sites by regulating rather than organizing COP II. Mol. Biol. Cell. 24:3406-3419. http://dx.doi.org/10.1091/mbc.E13-04-0185
8. Bhattacharyya, D., and B.S. Glick. 2007. Two mammalian Sec16 homologues have nonredundant functions in endoplasmic reticulum (ER) export and transitional ER organization. Mol. Biol. Cell. 18:839-849. http://dx.doi.org/10.1091/mbc.E06-08-0707
9. Bi, X., R.A. Corpina, and J. Goldberg. 2002. Structure of the Sec23/24-Sar1. pre-budding complex of the COP II vesicle coat. Nature. 419:271-277. http://dx.doi.org/10.1038/nature01040
10. Bi, X., J.D. Mancias, and J. Goldberg. 2007. Insights into COP II coat nucleation from the structure of Sec23.Sar1 complexed with the active fragment of Sec31. Dev. Cell. 13:635-645. http://dx.doi.org/10.1016/j.devcel.2007..10.006
11. Bruno, J., A. Brumfield, N. Chaudhary, D. Iaea, and T.E. McGraw. 2016. SEC16A is a RAB10 effector required for insulin-stimulated GLUT4. trafficking in adipocytes. J. Cell Biol. 214:61-76. http://dx.doi.org/10..1083/jcb.201509052
12. Cho, H.J., J. Yu, C. Xie, P. Rudrabhatla, X. Chen, J. Wu, L. Parisiadou, G. Liu, L. Sun, B. Ma, et al. 2014. Leucine-rich repeat kinase 2 regulates Sec16A at ER exit sites to allow ER-Golgi export. EMBO J. 33:2314-2331. http://dx.doi.org/10.15252/embj.201487807
13. Connerly, P.L., M. Esaki, E.A. Montegna, D.E. Strongin, S. Levi, J. Soderholm, and B.S. Glick. 2005. Sec16 is a determinant of transitional ER organization. Curr. Biol. 15:1439-1447. http://dx.doi.org/10.1016/j.cub.2005.06.065
14. Espenshade, P., R.E. Gimeno, E. Holzmacher, P. Teung, and C.A. Kaiser. 1995. Yeast SEC16 gene encodes a multidomain vesicle coat protein that interacts with Sec23p. J. Cell Biol. 131:311-324. http://dx.doi.org/10..1083/jcb.131.2.311
15. Farhan, H., M. Weiss, K. Tani, R.J. Kaufman, and H.P. Hauri. 2008. Adaptation of endoplasmic reticulum exit sites to acute and chronic increases in cargo load. EMBO J. 27:2043-2054. http://dx.doi.org/10.1038/emboj.2008.136
16. Farhan, H., M.W. Wendeler, S. Mitrovic, E. Fava, Y. Silberberg, R. Sharan, M. Zerial, and H.P. Hauri. 2010. MAPK signaling to the early secretory pathway revealed by kinase/phosphatase functional screening. J. Cell Biol. 189:997-1011. http://dx.doi.org/10.1083/jcb.200912082
17. Gimeno, R.E., P. Espenshade, and C.A. Kaiser. 1996. COP II coat subunit interactions: Sec24p and Sec23p bind to adjacent regions of Sec16p. Mol. Biol. Cell. 7:1815-1823. http://dx.doi.org/10.1091/mbc.7.11.1815
18. Glick, B.S. 2014. Integrated self-organization of transitional ER and early Golgi compartments. BioEssays. 36:129-133. http://dx.doi.org/10.1002/bies.201300131
19. Hughes, H., A. Budnik, K. Schmidt, K.J. Palmer, J. Mantell, C. Noakes, A. Johnson, D.A. Carter, P. Verkade, P. Watson, and D.J. Stephens. 2009. Organisation of human ER-exit sites: Requirements for the localisation of Sec16 to transitional ER. J. Cell Sci. 122:2924-2934. http://dx.doi.org/10.1242/jcs.044032
20. Iinuma, T., A. Shiga, K. Nakamoto, M.B. O'Brien, M. Aridor, N. Arimitsu, M. Tagaya, and K. Tani. 2007. Mammalian Sec16/p250 plays a role in membrane traffic from the endoplasmic reticulum. J. Biol. Chem. 282:17632-17639. http://dx.doi.org/10.1074/jbc.M611237200
21. Ishikawa, Y., S. Ito, K. Nagata, L.Y. Sakai, and H.P. Bächinger. 2016. Intracellular mechanisms of molecular recognition and sorting for transport of large extracellular matrix molecules. Proc. Natl. Acad. Sci. USA. 113:E6036-E6044. http://dx.doi.org/10.1073/pnas.1609571113
22. Ivan, V., G. de Voer, D. Xanthakis, K.M. Spoorendonk, V. Kondylis, and C. Rabouille. 2008. Drosophila Sec16 mediates the biogenesis of tER sites upstream of Sar1 through an arginine-rich motif. Mol. Biol. Cell. 19:4352-4365. http://dx.doi.org/10.1091/mbc.E08-03-0246
23. Johnson, A., N. Bhattacharya, M. Hanna, J.G. Pennington, A.L. Schuh, L. Wang, M.S. Otegui, S.M. Stagg, and A. Audhya. 2015. TFG clusters COP II-coated transport carriers and promotes early secretory pathway organization. EMBO J. 34:811-827. http://dx.doi.org/10.15252/embj.201489032
24. Komatsu, T., I. Kukelyansky, J.M. McCaffery, T. Ueno, L.C. Varela, and T. Inoue. 2010. Organelle-specific, rapid induction of molecular activities and membrane tethering. Nat. Methods. 7:206-208. http://dx.doi.org/10..1038/nmeth.1428
25. Kuehn, M.J., J.M. Herrmann, and R. Schekman. 1998. COP II-cargo interactions direct protein sorting into ER-derived transport vesicles. Nature. 391:187-190. http://dx.doi.org/10.1038/34438
26. Kung, L.F., S. Pagant, E. Futai, J.G. D'Arcangelo, R. Buchanan, J.C. Dittmar, R.J. Reid, R. Rothstein, S. Hamamoto, E.L. Snapp, et al. 2012. Sec24p and Sec16p cooperate to regulate the GTP cycle of the COP II coat. EMBO J. 31:1014-1027. http://dx.doi.org/10.1038/emboj.2011.444
27. Kurokawa, K., Y. Suda, and A. Nakano. 2016. Sar1 localizes at the rims of COP II-coated membranes in vivo. J. Cell Sci. 129:3231-3237. http://dx.doi.org/10.1242/jcs.189423
28. Liu, M., Z. Feng, H. Ke, Y. Liu, T. Sun, J. Dai, W. Cui, and J.C. Pastor-Pareja. 2017. Tango1 spatially organizes ER exit sites to control ER export. J. Cell Biol. 216:1035-1049. http://dx.doi.org/10.1083/jcb.201611088
29. Ma, W., and J. Goldberg. 2016. TAN GO1/cTAGE5 receptor as a polyvalent template for assembly of large COP II coats. Proc. Natl. Acad. Sci. USA. 113:10061-10066. http://dx.doi.org/10.1073/pnas.1605916113
30. Maeda, M., K. Saito, and T. Katada. 2016. Distinct isoform-specific complexes of TAN GO1 cooperatively facilitate collagen secretion from the endoplasmic reticulum. Mol. Biol. Cell. 27:2688-2696. http://dx.doi.org/10.1091/mbc.E16-03-0196
31. Malhotra, V., and P. Erlmann. 2015. The pathway of collagen secretion. Annu. Rev. Cell Dev. Biol. 31:109-124. http://dx.doi.org/10.1146/annurev-cellbio-100913-013002
32. Matsuoka, K., L. Orci, M. Amherdt, S.Y. Bednarek, S. Hamamoto, R. Schekman, and T. Yeung. 1998. COP II-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes. Cell. 93:263-275. http://dx.doi.org/10.1016/S0092-8674(00)81577-9
33. McCaughey, J., V.J. Miller, N.L. Stevenson, A.K. Brown, A. Budnik, K.J. Heesom, D. Alibhai, and D.J. Stephens. 2016. TFG promotes organization of transitional ER and efficient collagen secretion. Cell Reports. 15:1648-1659. http://dx.doi.org/10.1016/j.celrep.2016.04.062
34. Miller, E.A., and R. Schekman. 2013. COP II: A flexible vesicle formation system. Curr. Opin. Cell Biol. 25:420-427. http://dx.doi.org/10.1016/j.ceb.2013.04.005
35. Miller, E., B. Antonny, S. Hamamoto, and R. Schekman. 2002. Cargo selection into COP II vesicles is driven by the Sec24p subunit. EMBO J. 21:6105-6113. http://dx.doi.org/10.1093/emboj/cdf605
36. Miller, E.A., T.H. Beilharz, P.N. Malkus, M.C. Lee, S. Hamamoto, L. Orci, and R. Schekman. 2003. Multiple cargo binding sites on the COP II subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell. 114:497-509. http://dx.doi.org/10.1016/S0092.-8674(03)00609-3
37. Montegna, E.A., M. Bhave, Y. Liu, D. Bhattacharyya, and B.S. Glick. 2012. Sec12 binds to Sec16 at transitional ER sites. PLoS One. 7:e31156. http://dx.doi.org/10.1371/journal.pone.0031156
38. Nakano, A., and M. Muramatsu. 1989. A novel GTP-binding protein, Sar1p, is involved in transport from the endoplasmic reticulum to the Golgi apparatus. J. Cell Biol. 109:2677-2691. http://dx.doi.org/10.1083/jcb.109.6.2677
39. Nogueira, C., P. Erlmann, J. Villeneuve, A.J. Santos, E. Martínez-Alonso, J.A. Martínez-Menárguez, and V. Malhotra. 2014. SLY1 and Syntaxin 18. specify a distinct pathway for procollagen VII export from the endoplasmic reticulum. eLife. 3:e02784. http://dx.doi.org/10.7554/eLife.02784
40. Okamoto, M., K. Kurokawa, K. Matsuura-Tokita, C. Saito, R. Hirata, and A. Nakano. 2012. High-curvature domains of the ER are important for the organization of ER exit sites in Saccharomyces cerevisiae. J. Cell Sci. 125:3412-3420. http://dx.doi.org/10.1242/jcs.100065
41. Orci, L., M. Ravazzola, P. Meda, C. Holcomb, H.P. Moore, L. Hicke, and R. Schekman. 1991. Mammalian Sec23p homologue is restricted to the endoplasmic reticulum transitional cytoplasm. Proc. Natl. Acad. Sci. USA. 88:8611-8615. http://dx.doi.org/10.1073/pnas.88.19.8611
42. Pagant, S., A. Wu, S. Edwards, F. Diehl, and E.A. Miller. 2015. Sec24 is a coincidence detector that simultaneously binds two signals to drive ER export. Curr. Biol. 25:403-412. http://dx.doi.org/10.1016/j.cub.2014.11..070
43. Palade, G. 1975. Intracellular aspects of the process of protein synthesis. Science. 189:347-358. http://dx.doi.org/10.1126/science.1096303
44. Raote, I., M. Ortega Bellido, M. Pirozzi, C. Zhang, D. Melville, S. Parashuraman, T. Zimmermann, and V. Malhotra. 2017. TAN GO1 assembles into rings around COP II coats at ER exit sites. J. Cell Biol. 216:901-909. http://dx.doi.org/10.1083/jcb.201608080
45. Saito, K., and T. Katada. 2015. Mechanisms for exporting large-sized cargoes from the endoplasmic reticulum. Cell. Mol. Life Sci. 72:3709-3720. http://dx.doi.org/10.1007/s00018-015-1952-9
46. Saito, K., M. Chen, F. Bard, S. Chen, H. Zhou, D. Woodley, R. Polischuk, R. Schekman, and V. Malhotra. 2009. TAN GO1 facilitates cargo loading at endoplasmic reticulum exit sites. Cell. 136:891-902. http://dx.doi.org/10.1016/j.cell.2008.12.025
47. Saito, K., K. Yamashiro, Y. Ichikawa, P. Erlmann, K. Kontani, V. Malhotra, and T. Katada. 2011. cTAGE5 mediates collagen secretion through interaction with TAN GO1 at endoplasmic reticulum exit sites. Mol. Biol. Cell. 22:2301-2308. http://dx.doi.org/10.1091/mbc.E11-02-0143
48. Saito, K., K. Yamashiro, N. Shimazu, T. Tanabe, K. Kontani, and T. Katada. 2014. Concentration of Sec12 at ER exit sites via interaction with cTAGE5 is required for collagen export. J. Cell Biol. 206:751-762. http://dx.doi.org/10.1083/jcb.201312062
49. Santos, A.J., I. Raote, M. Scarpa, N. Brouwers, and V. Malhotra. 2015. TAN GO1. recruits ERG IC membranes to the endoplasmic reticulum for procollagen export. eLife. 4:e10982. http://dx.doi.org/10.7554/eLife.10982
50. Schindelin, J., I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, et al. 2012. Fiji: An opensource platform for biological-image analysis. Nat. Methods. 9:676-682. http://dx.doi.org/10.1038/nmeth.2019
51. Shaywitz, D.A., P.J. Espenshade, R.E. Gimeno, and C.A. Kaiser. 1997. COP II subunit interactions in the assembly of the vesicle coat. J. Biol. Chem. 272:25413-25416. http://dx.doi.org/10.1074/jbc.272.41.25413
52. Shin, K.J., E.A. Wall, J.R. Zavzavadjian, L.A. Santat, J. Liu, J.I. Hwang, R. Rebres, T. Roach, W. Seaman, M.I. Simon, and I.D. Fraser. 2006. A single lentiviral vector platform for microRNA-based conditional RNA interference and coordinated transgene expression. Proc. Natl. Acad. Sci. USA. 103:13759-13764. http://dx.doi.org/10.1073/pnas.0606179103
53. Soderholm, J., D. Bhattacharyya, D. Strongin, V. Markovitz, P.L. Connerly, C.A. Reinke, and B.S. Glick. 2004. The transitional ER localization mechanism of Pichia pastoris Sec12. Dev. Cell. 6:649-659. http://dx.doi.org/10.1016/S1534-5807(04)00129-7
54. Sprangers, J., and C. Rabouille. 2015. SEC16 in COP II coat dynamics at ER exit sites. Biochem. Soc. Trans. 43:97-103. http://dx.doi.org/10.1042/BST20140283
55. Supek, F., D.T. Madden, S. Hamamoto, L. Orci, and R. Schekman. 2002. Sec16p potentiates the action of COP II proteins to bud transport vesicles. J. Cell Biol. 158:1029-1038. http://dx.doi.org/10.1083/jcb.200207053
56. Tabata, K.V., K. Sato, T. Ide, T. Nishizaka, A. Nakano, and H. Noji. 2009. Visualization of cargo concentration by COP II minimal machinery in a planar lipid membrane. EMBO J. 28:3279-3289. http://dx.doi.org/10..1038/emboj.2009.269
57. Tanabe, T., M. Maeda, K. Saito, and T. Katada. 2016. Dual function of cTAGE5. in collagen export from the endoplasmic reticulum. Mol. Biol. Cell. 27:2008-2013. http://dx.doi.org/10.1091/mbc.E16-03-0180
58. Tillmann, K.D., V. Reiterer, F. Baschieri, J. Hoffmann, V. Millarte, M.A. Hauser, A. Mazza, N. Atias, D.F. Legler, R. Sharan, et al. 2015. Regulation of Sec16 levels and dynamics links proliferation and secretion. J. Cell Sci. 128:670-682. http://dx.doi.org/10.1242/jcs.157115
59. Venditti, R., T. Scanu, M. Santoro, G. Di Tullio, A. Spaar, R. Gaibisso, G.V. Beznoussenko, A.A. Mironov, A. Mironov Jr., L. Zelante, et al. 2012. Sedlin controls the ER export of procollagen by regulating the Sar1 cycle. Science. 337:1668-1672. http://dx.doi.org/10.1126/science.1224947
60. Watson, P., A.K. Townley, P. Koka, K.J. Palmer, and D.J. Stephens. 2006. Sec16. defines endoplasmic reticulum exit sites and is required for secretory cargo export in mammalian cells. Traffic. 7:1678-1687. http://dx.doi.org/10.1111/j.1600-0854.2006.00493.x
61. Whittle, J.R., and T.U. Schwartz. 2010. Structure of the Sec13-Sec16 edge element, a template for assembly of the COP II vesicle coat. J. Cell Biol. 190:347-361. http://dx.doi.org/10.1083/jcb.201003092
62. Wilhelmi, I., R. Kanski, A. Neumann, O. Herdt, F. Hoff, R. Jacob, M. Preußner, and F. Heyd. 2016. Sec16 alternative splicing dynamically controls COP II transport efficiency. Nat. Commun. 7:12347. http://dx.doi.org/10.1038./ncomms12347
63. Wilson, D.G., K. Phamluong, L. Li, M. Sun, T.C. Cao, P.S. Liu, Z. Modrusan, W.N. Sandoval, L. Rangell, R.A. Carano, et al. 2011. Global defects in collagen secretion in a Mia3/TAN GO1 knockout mouse. J. Cell Biol. 193:935-951. http://dx.doi.org/10.1083/jcb.201007162
64. Witte, K., A.L. Schuh, J. Hegermann, A. Sarkeshik, J.R. Mayers, K. Schwarze, J.R. Yates III, S. Eimer, and A. Audhya. 2011. TFG-1 function in protein secretion and oncogenesis. Nat. Cell Biol. 13:550-558. http://dx.doi.org/10.1038/ncb2225
65. Yorimitsu, T., and K. Sato. 2012. Insights into structural and regulatory roles of Sec16 in COP II vesicle formation at ER exit sites. Mol. Biol. Cell. 23:2930-2942. http://dx.doi.org/10.1091/mbc.E12-05-0356
66. Yoshihisa, T., C. Barlowe, and R. Schekman. 1993. Requirement for a GTPaseactivating protein in vesicle budding from the endoplasmic reticulum. Science. 259:1466-1468. http://dx.doi.org/10.1126/science.8451644
67. Zacharogianni, M., V. Kondylis, Y. Tang, H. Farhan, D. Xanthakis, F. Fuchs, M. Boutros, and C. Rabouille. 2011. ERK7 is a negative regulator of protein secretion in response to amino-acid starvation by modulating Sec16 membrane association. EMBO J. 30:3684-3700. http://dx.doi.org/10.1038/emboj.2011.253