Isoform-selective oligomer formation of saccharomyces cerevisiae p24 family proteins

Journal of Biological Chemistry

Volumn 288, Issue 52, 2013, Pages 37057-37070

  Hirata, Ryogo ^a,b   Nihei, Coh Ichi ^a,d   Nakano, Akihiko ^a,c  

^a Japan   (Japan)

^b RIKEN   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d INSTITUTE OF MICROBIAL CHEMISTRY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ISOFORMS; OLIGOMER FORMATIONS; PHYSICAL INTERACTIONS; S.CEREVISIAE;

PROTEINS;

YEAST;

EMP24 PROTEIN; ERP1 PROTEIN; ERP2 PROTEIN; ERP3 PROTEIN; ERP4 PROTEIN; ERP5 PROTEIN; ERP6 PROTEIN; ERV25 PROTEIN; GLYCEROL; ISOPROTEIN; OLIGOMER; SACCHAROMYCES CEREVISIAE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FUNGAL CELL CULTURE; FUNGAL STRAIN; FUNGUS MUTATION; GENE INTERACTION; GOLGI COMPLEX; NONHUMAN; OLIGOMERIZATION; PHENOTYPE; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SECRETORY PATHWAY;

EID: 84891377648     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.518340     Document Type: Article

References (79)

1. Brandizzi, F., and Barlowe, C. (2013) Organization of the ER-Golgi interface for membrane traffic control. Nat. Rev. Mol. Cell Biol. 14, 382-392
2. Sato, K., and Nakano, A. (2007) Mechanisms of COPII vesicle formation and protein sorting. FEBS Lett. 581, 2076-2082
3. Popoff, V., Adolf, F., Brügger, B., and Wieland, F. (2011) COPI budding within the Golgi stack. Cold Spring Harb. Perspect. Biol. 3, a005231
4. Glick, B. S., and Nakano, A. (2009) Membrane traffic within the Golgi apparatus. Annu. Rev. Cell Dev. Biol. 25, 113-132
5. Losev, E., Reinke, C. A., Jellen, J., Strongin, D. E., Bevis, B. J., and Glick, B. S. (2006) Golgi maturation visualized in living yeast. Nature 441, 1002-1006
6. Matsuura-Tokita, K., Takeuchi, M., Ichihara, A., Mikuriya, K., and Nakano, A. (2006) Live imaging of yeast Golgi cisternal maturation. Nature 441, 1007-1010
7. Rizzo, R., Parashuraman, S., Mirabelli, P., Puri, C., Lucocq, J., and Luini, A. (2013) The dynamics of engineered resident proteins in the mammalian Golgi complex relies on cisternal maturation. J. Cell Biol. 201, 1027-1036
8. Lavieu, G., Zheng, H., and Rothman, J. E. (2013) Stapled Golgi cisternae remain in place as cargo passes through the stack. eLife 2, e00558
9. Yang, J.-S., Valente, C., Pollshchuk, R. S., Turacchio, G., Layre, E., Moody, D. B., Leslie, C. C., Gelb, M. H., Brown, W. J., Corda, D., Luini, A., and Hsu, V. W. (2011) COPI acts in both vesicular and tubular transport. Nat. Cell Biol. 13, 996-1003
10. 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
11. Michelsen, K., Yuan, H., and Schwappach, B. (2005) Hide and run. Arginine-based endoplasmic-reticulum-sorting motifs in the assembly of heteromultimeric membrane proteins. EMBO Rep. 6, 717-722
12. Sato, K., and Nakano, A. (2005) Dissection of COPII subunit-cargo assembly and disassembly kinetics during Sar1p-GTP hydrolysis. Nat. Struct. Mol. Biol. 12, 167-174
13. Ma, W., and Goldberg, J. (2013) Rules for the recognition of dilysine retrieval motifs by coatomer. EMBO J. 32, 926-937
14. Otte, S., and Barlowe, C. (2004) Sorting signals can direct receptor-mediated export of soluble proteins into COPII vesicles. Nat. Cell Biol. 6, 1189-1194
15. Semenza, J. C., Hardwick, K. G., Dean, N., and Pelham, H. R. (1990) ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway. Cell 61, 1349-1357
16. Lewis, M. J., and Pelham, H. R. (1990) A human homologue of the yeast HDEL receptor. Nature 348, 162-163
17. Zheng, C., Page, R. C., Das, V., Nix, J. C., Wigren, E., Misra, S., and Zhang, B. (2013) Structural characterization of carbohydrate binding by LMAN1 protein provides new insight into the endoplasmic reticulum export of factors V (FV) and VIII (FVIII). J. Biol. Chem. 288, 20499-20509
18. Sato, K., and Nakano, A. (2002) Emp47p and its close homolog Emp46p have a tyrosine-containing endoplasmic reticulum exit signal and function in glycoprotein secretion in Saccharomyces cerevisiae. Mol. Biol. Cell 13, 2518-2532
19. Powers, J., and Barlowe, C. (1998) Transport of Axl2p depends on Erv14p, an ER-vesicle protein related to the Drosophila cornichon gene product. J. Cell Biol. 142, 1209-1222
20. Sato, K., Sato, M., and Nakano, A. (2003) Rer1p, a retrieval receptor for ER membrane proteins, recognizes transmembrane domains in multiple modes. Mol. Biol. Cell 14, 3605-3616
21. Bue, C. A., and Barlowe, C. (2009) Molecular dissection of Erv26p identifies separable cargo binding and coat protein sorting activities. J. Biol. Chem. 284, 24049-24060
22. Noda, Y., and Yoda, K. (2010) Svp26 facilitates endoplasmic reticulum to Golgi transport of a set of mannosyltransferases in Saccharomyces cerevisiae. J. Biol. Chem. 285, 15420-15429
23. Herzig, Y., Sharpe, H. J., Elbaz, Y., Munro, S., and Schuldiner, M. (2012) A systematic approach to pair secretory cargo receptors with their cargo suggests a mechanism for cargo selection by Erv14. PLoS Biol. 10, e1001329
24. 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
25. Castillon, G. A., Aguilera-Romero, A., Manzano-Lopez, J., Epstein, S., Kajiwara, K., Funato, K., Watanabe, R., Riezman, H., and Muñiz, M. (2011) The yeast p24 complex regulates GPI-anchored protein transport and quality control by monitoring anchor remodeling. Mol. Biol. Cell 22, 2924-2936
26. 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
27. Fujita, M., Watanabe, R., Jaensch, N., Romanova-Michaelides, M., Satoh, T., Kato, M., Riezman, H., Yamaguchi, Y., Maeda, Y., and Kinoshita, T. (2011) Sorting of GPI-anchored proteins into ER exit sites by p24 proteins is dependent on remodeled GPI. J. Cell Biol. 194, 61-75
28. 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
29. 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
30. Bouw, G., Van Huizen, R., Jansen, E. J., and Martens, G. J. (2004) A cellspecific transgenic approach in Xenopus reveals the importance of a functional p24 system for a secretory cell. Mol. Biol. Cell 15, 1244-1253
31. Zhang, L., and Volchuk, A. (2010) p24 family type 1 transmembrane proteins are required for insulin biosynthesis and secretion in pancreatic β-cells. FEBS Lett. 584, 2298-2304
32. Luo, W., Wang, Y., and Reiser, G. (2011) Proteinase-activated receptors, nucleotide P2Y receptors, andμ-opioid receptor-1B are under the control of the type I transmembrane proteins p23 and p24A in post-Golgi trafficking. J. Neurochem. 117, 71-81
33. Anantharaman, V., and Aravind, L. (2002) The GOLD domain, a novel protein module involved in Golgi function and secretion. Genome Biol. 3, research0023.1-research0023.7
34. Strating, J. R., van Bakel, N. H., Leunissen, J. A., and Martens, G. J. (2009) A comprehensive overview of the vertebrate p24 family. Identification of a novel tissue-specifically expressed member. Mol. Biol. Evol. 26, 1707-1714
35. Marzioch, M., Henthorn, D. C., Herrmann, J. M., Wilson, R., Thomas, D. Y., Bergeron, J. J., Solari, R. C., and Rowley, A. (1999) Erp1p and Erp2p, partners for Emp24p and Erv25p in a yeast p24 complex. Mol. Biol. Cell 10, 1923-1938
36. 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 both COP I and II coatomer. J. Cell Biol. 140, 751-765
37. Füllekrug, J., Suganuma, T., Tang, B. L., Hong, W., Storrie, B., and Nilsson, T. (1999) Localization and recycling of gp27 (hp24′3). Complex formation with other p24 family members. Mol. Biol. Cell 10, 1939-1955
38. 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
39. Jenne, N., Frey, K., Brugger, B., and Wieland, F. T. (2002) Oligomeric state and stoichiometry of p24 proteins in the early secretory pathway. J. Biol. Chem. 277, 46504-46511
40. Montesinos, J. C., Sturm, S., Langhans, M., Hillmer, S., Marcote, M. J., Robinson, D. G., and Aniento, F. (2012) Coupled transport of Arabidopsis p24 proteins at the ER-Golgi interface. J. Exp. Bot. 63, 4243-4261
41. Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E., Li, J., Hieter, P., and Boeke, J. D. (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C. A useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132
42. Rothstein, R. (1991) Targeting, disruption, replacement, and allele rescue. Integrative DNA transformation in yeast. Methods Enzymol. 194, 281-301
43. Janke, C., Magiera, M. M., Rathfelder, N., Taxis, C., Reber, S., Maekawa, H., Moreno-Borchart, A., Doenges, G., Schwob, E., Schiebel, E., and Knop, M. (2004) A versatile toolbox for PCR-based tagging of yeast genes. New fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21, 947-962
44. Burke, D., Dawson, D. S., Stearns, T., and Laboratory, C. S. H. (2000) Methods in Yeast Genetics 2000: A Cold Spring Harbor Laboratory Course Manual, pp. 171-181, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
45. Sikorski, R. S., and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27
46. Higuchi, R., Krummel, B., and Saiki, R. K. (1988) A general method of in vitro preparation and specific mutagenesis of DNA fragments. Study of protein and DNA interactions. Nucleic Acids Res. 16, 7351-7367
47. Sato, K., Sato, M., and Nakano, A. (2001) Rer1p, a retrieval receptor for endoplasmic reticulum membrane proteins, is dynamically localized to the Golgi apparatus by coatomer. J. Cell Biol. 152, 935-944
48. Nishikawa, S., and Nakano, A. (1993) Identification of a gene required for membrane protein retention in the early secretory pathway. Proc. Natl. Acad. Sci. U.S.A. 90, 8179-8183
49. Belden, W. J., and Barlowe, C. (2001) Distinct roles for the cytoplasmic tail sequences of Emp24p and Erv25p in transport between the endoplasmic reticulum and Golgi complex. J. Biol. Chem. 276, 43040-43048
50. Schimmöller, F., Singer-Krüger, B., Schröder, S., Krüger, U., Barlowe, C., and Riezman, H. (1995) The absence of Emp24p, a component of ERderived COPII-coated vesicles, causes a defect in transport of selected proteins to the Golgi. EMBO J. 14, 1329-1339
51. Elrod-Erickson, M. J., and Kaiser, C. A. (1996) Genes that control the fidelity of endoplasmic reticulum to Golgi transport identified as suppressors of vesicle budding mutations. Mol. Biol. Cell 7, 1043-1058
52. Belden, W. J., and Barlowe, C. (2001) Deletion of yeast p24 genes activates the unfolded protein response. Mol. Biol. Cell 12, 957-969
53. Čopič, A., Latham, C. F., Horlbeck, M. A., D'Arcangelo, J. G., and Miller, E. A. (2012) ER cargo properties specify a requirement for COPII coat rigidity mediated by Sec13p. Science 335, 1359-1362
54. Hontz, R. D., Niederer, R. O., Johnson, J. M., and Smith, J. S. (2009) Genetic identification of factors that modulate ribosomal DNA transcription in Saccharomyces cerevisiae. Genetics 182, 105-119
55. Punta, M., Coggill, P. C., Eberhardt, R. Y., Mistry, J., Tate, J., Boursnell, C., Pang, N., Forslund, K., Ceric, G., Clements, J., Heger, A., Holm, L., Sonnhammer, E. L., Eddy, S. R., Bateman, A., and Finn, R. D. (2012) The Pfam protein families database. Nucleic Acids Res. 40, D290-D301
56. Roberts, G. G., 3rd, and Hudson, A. P. (2009) Rsf1p is required for an efficient metabolic shift from fermentative to glycerol-based respiratory growth in S. cerevisiae. Yeast 26, 95-110
57. Jones, D. T. (1999) Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292, 195-202
58. Ciufo, L. F., and Boyd, A. (2000) Identification of a lumenal sequence specifying the assembly of Emp24p into p24 complexes in the yeast secretory pathway. J. Biol. Chem. 275, 8382-8388
59. Weidler, M., Reinhard, C., Friedrich, G., Wieland, F. T., and Rösch, P. (2000) Structure of the cytoplasmic domain of p23 in solution. Implications for the formation of COPI vesicles. Biochem. Biophys. Res. Commun. 271, 401-408
60. 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
61. Nakamura, N., Yamazaki, S., Sato, K., Nakano, A., Sakaguchi, M., and Mihara, K. (1998) Identification of potential regulatory elements for the transport of Emp24p. Mol. Biol. Cell 9, 3493-3503
62. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0. Discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786
63. +-ATPase occurs in the endoplasmic reticulum and requires a Vma12p/Vma22p assembly complex. J. Cell Biol. 142, 39-49
64. Sacher, M., Stone, S., and Ferro-Novick, S. (1997) The synaptobrevinrelated domains of Bos1p and Sec22p bind to the syntaxin-like region of Sed5p. J. Biol. Chem. 272, 17134-17138
65. Nakano, A., Brada, D., and Schekman, R. (1988) A membrane glycoprotein, Sec12p, required for protein transport from the endoplasmic reticulum to the Golgi apparatus in yeast. J. Cell Biol. 107, 851-863
66. Harris, S. L., and Waters, M. G. (1996) Localization of a yeast early Golgi mannosyltransferase, Och1p, involves retrograde transport. J. Cell Biol. 132, 985-998
67. Finnigan, G. C., Hanson-Smith, V., Houser, B. D., Park, H. J., and Stevens, T. H. (2011) The reconstructed ancestral subunit a functions as both VATPase isoforms Vph1p and Stv1p in Saccharomyces cerevisiae. Mol. Biol. Cell 22, 3176-3191
68. 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
69. Chen, S., Zhang, Y. E., and Long, M. (2010) New genes in Drosophila quickly become essential. Science 330, 1682-1685
70. Kellis, M., Birren, B. W., and Lander, E. S. (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428, 617-624
71. Strating, J. R., Bouw, G., Hafmans, T. G., and Martens, G. J. (2007) Disparate effects of p24α and p24δ on secretory protein transport and processing. PLoS ONE 2, e704
72. Strating, J. R., Hafmans, T. G., and Martens, G. J. (2009) Functional diversity among p24 subfamily members. Biol. Cell 101, 207-219
73. Strating, J. R., and Martens, G. J. (2009) The p24 family and selective transport processes at the ER-Golgi interface. Biol. Cell 101, 495-509
74. Rötter, J., Kuiper, R. P., Bouw, G., and Martens, G. J. (2002) Cell-typespecific and selectively induced expression of members of the p24 family of putative cargo receptors. J. Cell Sci. 115, 1049-1058
75. Li, S., Spooner, R. A., Allen, S. C., Guise, C. P., Ladds, G., Schnöder, T., Schmitt, M. J., Lord, J. M., and Roberts, L. M. (2010) Folding-competent and folding-defective forms of ricin A chain have different fates after retrotranslocation from the endoplasmic reticulum. Mol. Biol. Cell 21, 2543-2554
76. Haynes, C. M., Caldwell, S., and Cooper, A. A. (2002) An HRD/DER independent ER quality control mechanism involves Rsp5p-dependent ubiquitination and ER-Golgi transport. J. Cell Biol. 158, 91-101
77. Vashist, S., and Ng, D. T. (2004) Misfolded proteins are sorted by a sequential checkpoint mechanism of ER quality control. J. Cell Biol. 165, 41-52
78. Shi, Y., Stefan, C. J., Rue, S. M., Teis, D., and Emr, S. D. (2011) Two novel WD40 domain-containing proteins, Ere1 and Ere2, function in the retromer-mediated endosomal recycling pathway. Mol. Biol. Cell 22, 4093-4107
79. Ishihama, Y., Oda, Y., Tabata, T., Sato, T., Nagasu, T., Rappsilber, J., and Mann, M. (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol. Cell. Proteomics 4, 1265-1272