CK2 Phosphorylates Sec31 and Regulates ER-To-Golgi Trafficking

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2013 Jan 26

PMID 23349870

Citations 35

Authors

Mayuko Koreishi

Sidney Yu

Mayumi Oda

Yasuko Honjo

Ayano Satoh

Affiliations

Soon will be listed here.

Abstract

Protein export from the endoplasmic reticulum (ER) is an initial and rate-limiting step of molecular trafficking and secretion. This is mediated by coat protein II (COPII)-coated vesicles, whose formation requires small GTPase Sar1 and 6 Sec proteins including Sec23 and Sec31. Sec31 is a component of the outer layer of COPII coat and has been identified as a phosphoprotein. The initiation and promotion of COPII vesicle formation is regulated by Sar1; however, the mechanism regulating the completion of COPII vesicle formation followed by vesicle release is largely unknown. Hypothesizing that the Sec31 phosphorylation may be such a mechanism, we identified phosphorylation sites in the middle linker region of Sec31. Sec31 phosphorylation appeared to decrease its association with ER membranes and Sec23. Non-phosphorylatable mutant of Sec31 stayed longer at ER exit sites and bound more strongly to Sec23. We also found that CK2 is one of the kinases responsible for Sec31 phosphorylation because CK2 knockdown decreased Sec31 phosphorylation, whereas CK2 overexpression increased Sec31 phosphorylation. Furthermore, CK2 knockdown increased affinity of Sec31 for Sec23 and inhibited ER-to-Golgi trafficking. These results suggest that Sec31 phosphorylation by CK2 controls the duration of COPII vesicle formation, which regulates ER-to-Golgi trafficking.

Citing Articles

Loss of hepatic VMP1 trapped VLDL in the bilayer of endoplasmic reticulum membrane.

Ni H, Ding B, Chen A Liver Res. 2024; 7(2):161-163.

PMID: 38405163 PMC: 10888528. DOI: 10.1016/j.livres.2023.04.001.

Aromatic oil from lavender as an atopic dermatitis suppressant.

Sato H, Kato K, Koreishi M, Nakamura Y, Tsujino Y, Satoh A PLoS One. 2024; 19(1):e0296408.

PMID: 38181031 PMC: 10769034. DOI: 10.1371/journal.pone.0296408.

Nutrient deprivation alters the rate of COPII subunit recruitment at ER subdomains to tune secretory protein transport.

Kasberg W, Luong P, Swift K, Audhya A Nat Commun. 2023; 14(1):8140.

PMID: 38066006 PMC: 10709328. DOI: 10.1038/s41467-023-44002-7.

-GlcNAc Dynamics: The Sweet Side of Protein Trafficking Regulation in Mammalian Cells.

Ben Ahmed A, Lemaire Q, Scache J, Mariller C, Lefebvre T, Vercoutter-Edouart A Cells. 2023; 12(10).

PMID: 37408229 PMC: 10216988. DOI: 10.3390/cells12101396.

The C-terminus of the cargo receptor Erv14 affects COPII vesicle formation and cargo delivery.

Lagunas-Gomez D, Yanez-Dominguez C, Zavala-Padilla G, Barlowe C, Pantoja O J Cell Sci. 2023; 136(3).

PMID: 36651113 PMC: 10022740. DOI: 10.1242/jcs.260527.

References

Rutz C, Satoh A, Ronchi P, Brugger B, Warren G, Wieland F . Following the fate in vivo of COPI vesicles generated in vitro. Traffic. 2009; 10(8):994-1005. PMC: 4125364. DOI: 10.1111/j.1600-0854.2009.00934.x. View

Sohda M, Misumi Y, Yano A, Takami N, Ikehara Y . Phosphorylation of the vesicle docking protein p115 regulates its association with the Golgi membrane. J Biol Chem. 1998; 273(9):5385-8. DOI: 10.1074/jbc.273.9.5385. View

Yamasaki A, Tani K, Yamamoto A, Kitamura N, Komada M . The Ca2+-binding protein ALG-2 is recruited to endoplasmic reticulum exit sites by Sec31A and stabilizes the localization of Sec31A. Mol Biol Cell. 2006; 17(11):4876-87. PMC: 1635383. DOI: 10.1091/mbc.e06-05-0444. View

Lee M, Orci L, Hamamoto S, Futai E, Ravazzola M, Schekman R . Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell. 2005; 122(4):605-17. DOI: 10.1016/j.cell.2005.07.025. View

Weissman J, Plutner H, Balch W . The mammalian guanine nucleotide exchange factor mSec12 is essential for activation of the Sar1 GTPase directing endoplasmic reticulum export. Traffic. 2001; 2(7):465-75. DOI: 10.1034/j.1600-0854.2001.20704.x. View

Whittle J, Schwartz T . Structure of the Sec13-Sec16 edge element, a template for assembly of the COPII vesicle coat. J Cell Biol. 2010; 190(3):347-61. PMC: 2922654. DOI: 10.1083/jcb.201003092. View

Wendeler M, Paccaud J, Hauri H . Role of Sec24 isoforms in selective export of membrane proteins from the endoplasmic reticulum. EMBO Rep. 2007; 8(3):258-64. PMC: 1808030. DOI: 10.1038/sj.embor.7400893. View

Maday S, Anderson E, Chang H, Shorter J, Satoh A, Sfakianos J . A PDZ-binding motif controls basolateral targeting of syndecan-1 along the biosynthetic pathway in polarized epithelial cells. Traffic. 2008; 9(11):1915-24. PMC: 2820280. DOI: 10.1111/j.1600-0854.2008.00805.x. View

Bi X, Mancias J, Goldberg J . Insights into COPII coat nucleation from the structure of Sec23.Sar1 complexed with the active fragment of Sec31. Dev Cell. 2007; 13(5):635-645. PMC: 2686382. DOI: 10.1016/j.devcel.2007.10.006. View

10.

Lang M, Lapierre L, Frotscher M, Goldenring J, Knapik E . Secretory COPII coat component Sec23a is essential for craniofacial chondrocyte maturation. Nat Genet. 2006; 38(10):1198-203. DOI: 10.1038/ng1880. View

11.

Hanif I, Hanif I, Shazib M, Ahmad K, Pervaiz S . Casein Kinase II: an attractive target for anti-cancer drug design. Int J Biochem Cell Biol. 2010; 42(10):1602-5. DOI: 10.1016/j.biocel.2010.06.010. View

12.

Jin L, Pahuja K, Wickliffe K, Gorur A, Baumgartel C, Schekman R . Ubiquitin-dependent regulation of COPII coat size and function. Nature. 2012; 482(7386):495-500. PMC: 3292188. DOI: 10.1038/nature10822. View

13.

Montegna E, Bhave M, Liu Y, Bhattacharyya D, Glick B . Sec12 binds to Sec16 at transitional ER sites. PLoS One. 2012; 7(2):e31156. PMC: 3275590. DOI: 10.1371/journal.pone.0031156. View

14.

Lambert I, Hansen D . Regulation of taurine transport systems by protein kinase CK2 in mammalian cells. Cell Physiol Biochem. 2011; 28(6):1099-110. DOI: 10.1159/000335846. View

15.

Yorimitsu T, Sato K . Insights into structural and regulatory roles of Sec16 in COPII vesicle formation at ER exit sites. Mol Biol Cell. 2012; 23(15):2930-42. PMC: 3408419. DOI: 10.1091/mbc.E12-05-0356. View

16.

Gurkan C, Stagg S, LaPointe P, Balch W . The COPII cage: unifying principles of vesicle coat assembly. Nat Rev Mol Cell Biol. 2006; 7(10):727-38. DOI: 10.1038/nrm2025. View

17.

Kung L, Pagant S, Futai E, DArcangelo J, Buchanan R, Dittmar J . Sec24p and Sec16p cooperate to regulate the GTP cycle of the COPII coat. EMBO J. 2011; 31(4):1014-27. PMC: 3280547. DOI: 10.1038/emboj.2011.444. View

18.

Salama N, Chuang J, Schekman R . Sec31 encodes an essential component of the COPII coat required for transport vesicle budding from the endoplasmic reticulum. Mol Biol Cell. 1997; 8(2):205-17. PMC: 276074. DOI: 10.1091/mbc.8.2.205. View

19.

Sprague B, Pego R, Stavreva D, McNally J . Analysis of binding reactions by fluorescence recovery after photobleaching. Biophys J. 2004; 86(6):3473-95. PMC: 1304253. DOI: 10.1529/biophysj.103.026765. View

20.

Sucic S, El-Kasaby A, Kudlacek O, Sarker S, Sitte H, Marin P . The serotonin transporter is an exclusive client of the coat protein complex II (COPII) component SEC24C. J Biol Chem. 2011; 286(18):16482-90. PMC: 3091253. DOI: 10.1074/jbc.M111.230037. View