Sec16 alternative splicing dynamically controls COPII transport efficiency

Nature Communications

Volumn 7, Issue , 2016, Pages

  Wilhelmi, Ilka ^a,c   Kanski, Regina ^a   Neumann, Alexander ^a   Herdt, Olga ^a   Hoff, Florian ^b   Jacob, Ralf ^b   Preußner, Marco ^a   Heyd, Florian ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COAT PROTEIN COMPLEX II; PEPTIDES AND PROTEINS; SEC16 PROTEIN; UNCLASSIFIED DRUG; ISOPROTEIN; SEC16A PROTEIN, HUMAN; VESICULAR TRANSPORT PROTEIN;

CELL ORGANELLE; GENE EXPRESSION; GENETIC ENGINEERING; GENOME; PROTEIN; SECRETION;

ALTERNATIVE RNA SPLICING; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FEMALE; GOLGI COMPLEX; HUMAN; HUMAN CELL; PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN TRANSPORT; T LYMPHOCYTE ACTIVATION; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; COP-COATED VESICLE; EXON; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; T LYMPHOCYTE; TRANSPORT AT THE CELLULAR LEVEL;

ALTERNATIVE SPLICING; BIOLOGICAL TRANSPORT; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; COP-COATED VESICLES; ENDOPLASMIC RETICULUM; EXONS; GOLGI APPARATUS; HEK293 CELLS; HELA CELLS; HUMANS; PROTEIN ISOFORMS; PROTEIN TRANSPORT; T-LYMPHOCYTES; VESICULAR TRANSPORT PROTEINS;

EID: 84981186394     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12347     Document Type: Article

References (43)

1. Antonny, B., Schekman, R. ER export: public transportation by the COPII coach. Curr. Opin. Cell Biol. 13, 438-443 (2001).
2. Gurkan, C., Stagg, S. M., Lapointe, P., Balch, W. E. The COPII cage: unifying principles of vesicle coat assembly. Nat. Rev. Mol. Cell Biol. 7, 727-738 (2006).
3. Sato, K., Nakano, A. Dissection of COPII subunit-cargo assembly and disassembly kinetics during Sar1p-GTP hydrolysis. Nat. Struct. Mol. Biol. 12, 167-174 (2005).
4. Supek, F., Madden, D. T., Hamamoto, S., Orci, L., Schekman, R. Sec16p potentiates the action of COPII proteins to bud transport vesicles. J. Cell Biol. 158, 1029-1038 (2002).
5. Kung, L. F. et al. Sec24p and Sec16p cooperate to regulate the GTP cycle of the COPII coat. EMBO J. 31, 1014-1027 (2012).
6. Adolf, F. et al. Scission of COPI and COPII vesicles is independent of GTP hydrolysis. Traffic 14, 922-932 (2013).
7. Budnik, A., Stephens, D. J. ER exit sites-localization and control of COPII vesicle formation. FEBS Lett. 583, 3796-3803 (2009).
8. Watson, P., Townley, A. K., Koka, P., Palmer, K. J., Stephens, D. J. Sec16 defines endoplasmic reticulum exit sites and is required for secretory cargo export in mammalian cells. Traffic 7, 1678-1687 (2006).
9. Ivan, V. et al. Drosophila Sec16 mediates the biogenesis of tER sites upstream of Sar1 through an arginine-rich motif. Mol. Biol. Cell 19, 4352-4365 (2008).
10. Hughes, H. et al. Organisation of human ER-exit sites: requirements for the localisation of Sec16 to transitional ER. J. Cell Sci. 122, 2924-2934 (2009).
11. Cho, H. J. et al. Leucine-rich repeat kinase 2 regulates Sec16A at ER exit sites to allow ER-Golgi export. EMBO J. 33, 2314-2331 (2014).
12. Espenshade, P., Gimeno, R. E., Holzmacher, E., Teung, P., Kaiser, C. A. Yeast SEC16 gene encodes a multidomain vesicle coat protein that interacts with Sec23p. J. Cell Biol. 131, 311-324 (1995).
13. Bhattacharyya, D., Glick, B. S. Two mammalian Sec16 homologues have nonredundant functions in endoplasmic reticulum (ER) export and transitional ER organization. Mol. Biol. Cell 18, 839-849 (2007).
14. Budnik, A., Heesom, K. J., Stephens, D. J. Characterization of human Sec16B: indications of specialized, non-redundant functions. Sci. Rep. 1, 77 (2011).
15. Yonekawa, S. et al. Sec16B is involved in the endoplasmic reticulum export of the peroxisomal membrane biogenesis factor peroxin 16 (Pex16) in mammalian cells. Proc. Natl Acad. Sci. USA 108, 12746-12751 (2011).
16. Montegna, E. A., Bhave, M., Liu, Y., Bhattacharyya, D., Glick, B. S. Sec12 binds to Sec16 at transitional ER sites. PLoS ONE 7, e31156 (2012).
17. Whittle, J. R., Schwartz, T. U. Structure of the Sec13-Sec16 edge element, a template for assembly of the COPII vesicle coat. J Cell Biol 190, 347-361 (2010).
18. Yorimitsu, T., Sato, K. Insights into structural and regulatory roles of Sec16 in COPII vesicle formation at ER exit sites. Mol. Biol. Cell 23, 2930-2942 (2012).
19. Bharucha, N. et al. Sec16 influences transitional ER sites by regulating rather than organizing COPII. Mol. Biol. Cell 24, 3406-3419 (2013).
20. Sprangers, J., Rabouille, C. SEC16 in COPII coat dynamics at ER exit sites. Biochem. Soc. Trans. 43, 97-103 (2015).
21. Huse, M., Lillemeier, B. F., Kuhns, M. S., Chen, D. S., Davis, M. M. T cells use two directionally distinct pathways for cytokine secretion. Nat. Immunol. 7, 247-255 (2006).
22. Huse, M., Quann, E. J., Davis, M. M. Shouts, whispers and the kiss of death: directional secretion in T cells. Nat. Immunol. 9, 1105-1111 (2008).
23. Farhan, H., Weiss, M., Tani, K., Kaufman, R. J., Hauri, H. P. Adaptation of endoplasmic reticulum exit sites to acute and chronic increases in cargo load. EMBO J. 27, 2043-2054 (2008).
24. Farhan, H. et al. MAPK signaling to the early secretory pathway revealed by kinase/phosphatase functional screening. J. Cell Biol. 189, 997-1011 (2010).
25. Zacharogianni, M. et al. ERK7 is a negative regulator of protein secretion in response to amino-acid starvation by modulating Sec16 membrane association. EMBO J. 30, 3684-3700 (2011).
26. Miller, E. A., Schekman, R. COPII-a flexible vesicle formation system. Curr. Opin. Cell Biol. 25, 420-427 (2013).
27. Tao, J. et al. SEC23B is required for the maintenance of murine professional secretory tissues. Proc. Natl Acad. Sci. USA 109, E2001-E2009 (2012).
28. Adams, E. J., Chen, X. W., O'Shea, K. S., Ginsburg, D. Mammalian COPII coat component SEC24C is required for embryonic development in mice. J. Biol. Chem. 289, 20858-20870 (2014).
29. Jensen, D., Schekman, R. COPII-mediated vesicle formation at a glance. J. Cell Sci. 124, 1-4 (2011).
30. Heyd, F., Lynch, K. W. Degrade, move, regroup: signaling control of splicing proteins. Trends Biochem. Sci. 36, 397-404 (2011).
31. Preussner, M. et al. Rhythmic U2af26 alternative splicing controls PERIOD1 stability and the circadian clock in mice. Mol. Cell 54, 651-662 (2014).
32. Martinez, N. M. et al. Alternative splicing networks regulated by signaling in human T cells. RNA 18, 1029-1040 (2012).
33. Michel, M., Wilhelmi, I., Schultz, A. S., Preussner, M., Heyd, F. Activationinduced tumor necrosis factor receptor-associated factor 3 (Traf3) alternative splicing controls the noncanonical nuclear factor kappaB pathway and chemokine expression in human T cells. J. Biol. Chem. 289, 13651-13660 (2014).
34. Tillmann, K. D. et al. Regulation of Sec16 levels and dynamics links proliferation and secretion. J. Cell. Sci. 128, 670-682 (2015).
35. Presley, J. F. et al. ER-to-Golgi transport visualized in living cells. Nature 389, 81-85 (1997).
36. Townley, A. K. et al. Efficient coupling of Sec23-Sec24 to Sec13-Sec31 drives COPII-dependent collagen secretion and is essential for normal craniofacial development. J. Cell Sci. 121, 3025-3034 (2008).
37. Fromme, J. C., Orci, L., Schekman, R. Coordination of COPII vesicle trafficking by Sec23. Trends Cell. Biol. 18, 330-336 (2008).
38. Jin, L. et al. Ubiquitin-dependent regulation of COPII coat size and function. Nature 482, 495-500 (2012).
39. Zeuschner, D. et al. Immuno-electron tomography of ER exit sites reveals the existence of free COPII-coated transport carriers. Nat. Cell Biol. 8, 377-383 (2006).
40. Zanetti, G., Pahuja, K. B., Studer, S., Shim, S., Schekman, R. COPII and the regulation of protein sorting in mammals. Nat. Cell Biol. 14, 20-28 (2012).
41. Ran, F. A. et al. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281-2308 (2013).
42. Heyd, F., Lynch, K. W. Phosphorylation-dependent regulation of PSF by GSK3 controls CD45 alternative splicing. Mol. Cell 40, 126-137 (2010).
43. Goodwin, J. S., Kenworthy, A. K. Photobleaching approaches to investigate diffusional mobility and trafficking of Ras in living cells. Methods 37, 154-164 (2005).