CoChat
Sign Up
Cited by 77Cellular transport and secretionAutophagy in Disease and TherapyFungal and yeast genetics research

Maturation-driven transport and AP-1–dependent recycling of a secretory cargo in the Golgi

Open access
Casler, Jason C., Papanikou, Effrosyni, Barrero, Juan J., Glick, Benjamin S.·2019·Journal of Cell Biology
DOI 10.1083/jcb.201807195PMC PMC6504904
Open this paper in CoChat — free account

Abstract

Golgi cisternal maturation has been visualized by fluorescence imaging of individual cisternae in the yeast Saccharomyces cerevisiae, but those experiments did not track passage of a secretory cargo. The expectation is that a secretory cargo will be continuously present within maturing cisternae as resident Golgi proteins arrive and depart. We tested this idea using a regulatable fluorescent secretory cargo that forms ER-localized aggregates, which dissociate into tetramers upon addition of a ligand. The solubilized tetramers rapidly exit the ER and then transit through early and late Golgi compartments before being secreted. Early Golgi cisternae form near the ER and become loaded with the secretory cargo. As predicted, cisternae contain the secretory cargo throughout the maturation process. An unexpected finding is that a burst of intra-Golgi recycling delivers additional secretory cargo molecules to cisternae during the early-to-late Golgi transition. This recycling requires the AP-1 adaptor, suggesting that AP-1 can recycle secretory cargo proteins as well as resident Golgi proteins.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1083/jcb.201807195

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 103

  1. Appenzeller-Herzog C., Nyfeler B., Burkhard P., Santamaria I., Lopez-Otin C., and Hauri H.P. 2005 Carbohydrate- and conformation-dependent cargo capture for ER-exit. Mol. Biol. Cell. 16: 1258– 1267. 10.1091/mbc.e04-08-0708 15635097 PMC551490 · DOI
  2. Arlt H., Auffarth K., Kurre R., Lisse D., Piehler J., and Ungermann C. 2015 Spatiotemporal dynamics of membrane remodeling and fusion proteins during endocytic transport. Mol. Biol. Cell. 26: 1357– 1370. 10.1091/mbc.E14-08-1318 25657322 PMC4454181 · DOI
  3. Barfield R.M., Fromme J.C., and Schekman R. 2009 The exomer coat complex transports Fus1p to the plasma membrane via a novel plasma membrane sorting signal in yeast. Mol. Biol. Cell. 20: 4985– 4996. 10.1091/mbc.e09-04-0324 19812245 PMC2785741 · DOI
  4. Barlowe C., and Helenius A. 2016 Cargo capture and bulk flow in the early secretory pathway. Annu. Rev. Cell Dev. Biol. 32: 197– 222. 10.1146/annurev-cellbio-111315-125016 27298089 · DOI
  5. Barrero J.J., Papanikou E., Casler J.C., Day K.J., and Glick B.S. 2016 An improved reversibly dimerizing mutant of the FK506-binding protein FKBP. Cell. Logist. 6: e1204848 10.1080/21592799.2016.1204848 27738551 PMC5058350 · DOI
  6. Barrero J.J., Casler J.C., Valero F., Ferrer P., and Glick B.S. 2018 An improved secretion signal enhances the secretion of model proteins from Pichia pastoris. Microb. Cell Fact. 17: 161 10.1186/s12934-018-1009-5 30314480 PMC6182871 · DOI
  7. Bevis B.J., Hammond A.T., Reinke C.A., and Glick B.S. 2002 De novo formation of transitional ER sites and Golgi structures in Pichia pastoris. Nat. Cell Biol. 4: 750– 756. 10.1038/ncb852 12360285 · DOI
  8. Beznoussenko G.V., Parashuraman S., Rizzo R., Polishchuk R., Martella O., Di Giandomenico D., Fusella A., Spaar A., Sallese M., Capestrano M.G., 2014 Transport of soluble proteins through the Golgi occurs by diffusion via continuities across cisternae. eLife. 3: e02009 10.7554/eLife.02009 PMC4070021 24867214 · DOI
  9. Beznoussenko G.V., Ragnini-Wilson A., Wilson C., and Mironov A.A. 2016 Three-dimensional and immune electron microscopic analysis of the secretory pathway in Saccharomyces cerevisiae. Histochem. Cell Biol. 146: 515– 527. 10.1007/s00418-016-1483-y 27590193 · DOI
  10. Boncompain G., Divoux S., Gareil N., de Forges H., Lescure A., Latreche L., Mercanti V., Jollivet F., Raposo G., and Perez F. 2012 Synchronization of secretory protein traffic in populations of cells. Nat. Methods. 9: 493– 498. 10.1038/nmeth.1928 22406856 · DOI
  11. Bonfanti L., Mironov A.A. Jr., Martínez-Menárguez J.A., Martella O., Fusella A., Baldassarre M., Buccione R., Geuze H.J., Mironov A.A., and Luini A. 1998 Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation. Cell. 95: 993– 1003. 10.1016/S0092-8674(00)81723-7 9875853 · DOI
  12. Brigance W.T., Barlowe C., and Graham T.R. 2000 Organization of the yeast Golgi complex into at least four functionally distinct compartments. Mol. Biol. Cell. 11: 171– 182. 10.1091/mbc.11.1.171 10637300 PMC14766 · DOI
  13. Casler J.C., and Glick B.S. 2018 Visualizing secretory cargo transport in budding yeast. Curr. Protoc. Cell Biol. 10.1002/cpcb.80 PMC6506369 30414385 · DOI
  14. Castillon G.A., Watanabe R., Taylor M., Schwabe T.M., and Riezman H. 2009 Concentration of GPI-anchored proteins upon ER exit in yeast. Traffic. 10: 186– 200. 10.1111/j.1600-0854.2008.00857.x 19054390 · DOI
  15. Chen Y., Gershlick D.C., Park S.Y., and Bonifacino J.S. 2017 Segregation in the Golgi complex precedes export of endolysosomal proteins in distinct transport carriers. J. Cell Biol. 216: 4141– 4151. 10.1083/jcb.201707172 28978644 PMC5716290 · DOI · Paper page
  16. Coorey N.V.C., Matthews J.H., Bellows D.S., and Atkinson P.H. 2015 Pleiotropic drug-resistance attenuated genomic library improves elucidation of drug mechanisms. Mol. Biosyst. 11: 3129– 3136. 10.1039/C5MB00406C 26381459 · DOI
  17. Cox J.S., and Walter P. 1996 A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell. 87: 391– 404. 10.1016/S0092-8674(00)81360-4 8898193 · DOI
  18. Daboussi L., Costaguta G., and Payne G.S. 2012 Phosphoinositide-mediated clathrin adaptor progression at the trans-Golgi network. Nat. Cell Biol. 14: 239– 248. 10.1038/ncb2427 22344030 PMC4855891 · DOI
  19. Dancourt J., and Barlowe C. 2010 Protein sorting receptors in the early secretory pathway. Annu. Rev. Biochem. 79: 777– 802. 10.1146/annurev-biochem-061608-091319 20533886 · DOI
  20. Day K.J., Staehelin L.A., and Glick B.S. 2013 A three-stage model of Golgi structure and function. Histochem. Cell Biol. 140: 239– 249. 10.1007/s00418-013-1128-3 23881164 PMC3779436 · DOI
  21. Day K.J., Papanikou E., and Glick B.S. 2016 4D confocal imaging of yeast organelles. Methods Mol. Biol. 1496: 1– 11. 10.1007/978-1-4939-6463-5_1 27631997 PMC5086802 · DOI
  22. Day K.J., La Rivière P.J., Chandler T., Bindokas V.P., Ferrier N.J., and Glick B.S. 2017 Improved deconvolution of very weak confocal signals. F1000 Res. 6: 787 10.12688/f1000research.11773.1 PMC5553083 28868135 · DOI
  23. Day K.J., Casler J.C., and Glick B.S. 2018 Budding yeast has a minimal endomembrane system. Dev. Cell. 44: 56– 72.e4. 10.1016/j.devcel.2017.12.014 29316441 PMC5765772 · DOI
  24. De Matteis M.A., and Luini A. 2008 Exiting the Golgi complex. Nat. Rev. Mol. Cell Biol. 9: 273– 284. 10.1038/nrm2378 18354421 · DOI
  25. De Nobel J.G., Klis F.M., Munnik T., Priem J., and van den Ende H. 1990 An assay of relative cell wall porosity in Saccharomyces cerevisiae, Kluyveromyces lactis and Schizosaccharomyces pombe. Yeast. 6: 483– 490. 10.1002/yea.320060605 2080665 · DOI
  26. Di Santo R., Aboulhouda S., and Weinberg D.E. 2016 The fail-safe mechanism of post-transcriptional silencing of unspliced HAC1 mRNA. eLife. 5: e20069 10.7554/eLife.20069 27692069 PMC5114014 · DOI
  27. Dunlop M.H., Ernst A.M., Schroeder L.K., Toomre D.K., Lavieu G., and Rothman J.E. 2017 Land-locked mammalian Golgi reveals cargo transport between stable cisternae. Nat. Commun. 8: 432 10.1038/s41467-017-00570-z 28874656 PMC5585379 · DOI
  28. Dunphy W.G., and Rothman J.E. 1985 Compartmental organization of the Golgi stack. Cell. 42: 13– 21. 10.1016/S0092-8674(85)80097-0 3926324 · DOI
  29. Emr S., Glick B.S., Linstedt A.D., Lippincott-Schwartz J., Luini A., Malhotra V., Marsh B.J., Nakano A., Pfeffer S.R., Rabouille C., 2009 Journeys through the Golgi--taking stock in a new era. J. Cell Biol. 187: 449– 453. 10.1083/jcb.200909011 19948493 PMC2779233 · DOI
  30. Field C., and Schekman R. 1980 Localized secretion of acid phosphatase reflects the pattern of cell surface growth in Saccharomyces cerevisiae. J. Cell Biol. 86: 123– 128. 10.1083/jcb.86.1.123 6998984 PMC2110663 · DOI
  31. Finger F.P., and Novick P. 1998 Spatial regulation of exocytosis: lessons from yeast. J. Cell Biol. 142: 609– 612. 10.1083/jcb.142.3.609 9700152 PMC2148161 · DOI
  32. Fitzgerald I., and Glick B.S. 2014 Secretion of a foreign protein from budding yeasts is enhanced by cotranslational translocation and by suppression of vacuolar targeting. Microb. Cell Fact. 13: 125 10.1186/s12934-014-0125-0 25164324 PMC4176846 · DOI
  33. Galat A. 2008 Functional drift of sequence attributes in the FK506-binding proteins (FKBPs). J. Chem. Inf. Model. 48: 1118– 1130. 10.1021/ci700429n 18412331 · DOI
  34. Gaynor E.C., and Emr S.D. 1997 COPI-independent anterograde transport: cargo-selective ER to Golgi protein transport in yeast COPI mutants. J. Cell Biol. 136: 789– 802. 10.1083/jcb.136.4.789 9049245 PMC2132489 · DOI
  35. Glick B.S., and Luini A. 2011 Models for Golgi traffic: a critical assessment. Cold Spring Harb. Perspect. Biol. 3: a005215 10.1101/cshperspect.a005215 21875986 PMC3220355 · DOI
  36. Glick B.S., and Nakano A. 2009 Membrane traffic within the Golgi apparatus. Annu. Rev. Cell Dev. Biol. 25: 113– 132. 10.1146/annurev.cellbio.24.110707.175421 19575639 PMC2877624 · DOI
  37. Goldstein A.L., and McCusker J.H. 1999 Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast. 15: 1541– 1553. 10.1002/(SICI)1097-0061(199910)15:14<1541::AID-YEA476>3.0.CO;2-K 10514571 · DOI
  38. Grimm J.B., English B.P., Chen J., Slaughter J.P., Zhang Z., Revyakin A., Patel R., Macklin J.J., Normanno D., Singer R.H., 2015 A general method to improve fluorophores for live-cell and single-molecule microscopy. Nat. Methods. 12: 244– 250. 10.1038/nmeth.3256 25599551 PMC4344395 · DOI
  39. Guo Y., Zanetti G., and Schekman R. 2013 A novel GTP-binding protein-adaptor protein complex responsible for export of Vangl2 from the trans Golgi network. eLife. 2: e00160 10.7554/eLife.00160 23326640 PMC3539332 · DOI
  40. Gut A., Kappeler F., Hyka N., Balda M.S., Hauri H.P., and Matter K. 1998 Carbohydrate-mediated Golgi to cell surface transport and apical targeting of membrane proteins. EMBO J. 17: 1919– 1929. 10.1093/emboj/17.7.1919 9524115 PMC1170538 · DOI
  41. Hammond A.T., and Glick B.S. 2000 Raising the speed limits for 4D fluorescence microscopy. Traffic. 1: 935– 940. 11208083
  42. Heitman J., Movva N.R., Hiestand P.C., and Hall M.N. 1991 FK 506-binding protein proline rotamase is a target for the immunosuppressive agent FK 506 in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 88: 1948– 1952. 10.1073/pnas.88.5.1948 1705713 PMC51143 · DOI
  43. Hirst J., Borner G.H., Antrobus R., Peden A.A., Hodson N.A., Sahlender D.A., and Robinson M.S. 2012 Distinct and overlapping roles for AP-1 and GGAs revealed by the “knocksideways” system. Curr. Biol. 22: 1711– 1716. 10.1016/j.cub.2012.07.012 22902756 PMC3485558 · DOI · Paper page
  44. Holt D.A., Luengo J.I., Yamashita D.S., Oh H.J., Konialian A.L., Yen H.K., Rozamus L.W., Brandt M., Bossard M.J., Levy M.A., 1993 Design, synthesis, and kinetic evaluation of high-affinity FKBP ligands and the X-ray crystal structures of their complexes with FKBP12. J. Am. Chem. Soc. 115: 9925– 9938. 10.1021/ja00075a008 · DOI
  45. Ishii M., Suda Y., Kurokawa K., and Nakano A. 2016 COPI is essential for Golgi cisternal maturation and dynamics. J. Cell Sci. 129: 3251– 3261. 10.1242/jcs.193367 27445311 PMC5047698 · DOI
  46. Jacobs C.W., Adams A.E.M., Szaniszlo P.J., and Pringle J.R. 1988 Functions of microtubules in the Saccharomyces cerevisiae cell cycle. J. Cell Biol. 107: 1409– 1426. 10.1083/jcb.107.4.1409 3049620 PMC2115239 · DOI
  47. Jørgensen M.U., Emr S.D., and Winther J.R. 1999 Ligand recognition and domain structure of Vps10p, a vacuolar protein sorting receptor in Saccharomyces cerevisiae. Eur. J. Biochem. 260: 461– 469. 10.1046/j.1432-1327.1999.00176.x 10095782 · DOI
  48. Kim J.J., Lipatova Z., Majumdar U., and Segev N. 2016 Regulation of Golgi cisternal progression by Ypt/Rab GTPases. Dev. Cell. 36: 440– 452. 10.1016/j.devcel.2016.01.016 26906739 PMC4768313 · DOI
  49. Kornfeld R., and Kornfeld S. 1985 Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54: 631– 664. 10.1146/annurev.bi.54.070185.003215 3896128 · DOI
  50. Koval M., Harley J.E., Hick E., and Steinberg T.H. 1997 Connexin46 is retained as monomers in a trans-Golgi compartment of osteoblastic cells. J. Cell Biol. 137: 847– 857. 10.1083/jcb.137.4.847 9151687 PMC2139843 · DOI
  51. Kurokawa K., Okamoto M., and Nakano A. 2014 Contact of cis-Golgi with ER exit sites executes cargo capture and delivery from the ER. Nat. Commun. 5: 3653 10.1038/ncomms4653 24728174 PMC3996532 · DOI
  52. Kurokawa K., Osakada O., Kodijani T., Waga M., Suda Y., Asakawa H., Haraguchi T., and Nakano A. 2019 Visualization of secretory cargo transport within the Golgi apparatus. J. Cell Biol. 10.1093/jcb.201807194. PMC6504898 30858192 · DOI
  53. Lavieu G., Zheng H., and Rothman J.E. 2013 Stapled Golgi cisternae remain in place as cargo passes through the stack. eLife. 2: e00558 10.7554/eLife.00558 23755362 PMC3673335 · DOI
  54. Levi S.K., Bhattacharyya D., Strack R.L., Austin J.R.I. II, and Glick B.S. 2010 The yeast GRASP Grh1 colocalizes with COPII and is dispensable for organizing the secretory pathway. Traffic. 11: 1168– 1179. 10.1111/j.1600-0854.2010.01089.x 20573068 PMC2919637 · DOI
  55. Lord C., Ferro-Novick S., and Miller E.A. 2013 The highly conserved COPII coat complex sorts cargo from the endoplasmic reticulum and targets it to the Golgi. Cold Spring Harb. Perspect. Biol. 5: a013367 10.1101/cshperspect.a013367 23378591 PMC3552504 · DOI
  56. 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. 10.1038/nature04717 16699524 · DOI
  57. Makarow M. 1988 Secretion of invertase in mitotic yeast cells. EMBO J. 7: 1475– 1482. 10.1002/j.1460-2075.1988.tb02965.x 3044781 PMC458398 · DOI
  58. Maley F., Trimble R.B., Tarentino A.L., and Plummer T.H. Jr 1989 Characterization of glycoproteins and their associated oligosaccharides through the use of endoglycosidases. Anal. Biochem. 180: 195– 204. 10.1016/0003-2697(89)90115-2 2510544 · DOI
  59. Matsuura-Tokita K., Takeuchi M., Ichihara A., Mikuriya K., and Nakano A. 2006 Live imaging of yeast Golgi cisternal maturation. Nature. 441: 1007– 1010. 10.1038/nature04737 16699523 · DOI
  60. Mironov A.A., Beznoussenko G.V., Nicoziani P., Martella O., Trucco A., Kweon H.S., Di Giandomenico D., Polishchuk R.S., Fusella A., Lupetti P., 2001 Small cargo proteins and large aggregates can traverse the Golgi by a common mechanism without leaving the lumen of cisternae. J. Cell Biol. 155: 1225– 1238. 10.1083/jcb.200108073 11756473 PMC2199327 · DOI
  61. 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. 10.1091/mbc.e07-10-0989 18287528 PMC2366877 · DOI
  62. Moscovici M., Chien W.Y., Abdelgawad M., and Sun Y. 2010 Electrical power free, low dead volume, pressure-driven pumping for microfluidic applications. Biomicrofluidics. 4: 46501 10.1063/1.3499939 21057609 PMC2973980 · DOI
  63. Myers M.D., and Payne G.S. 2013 Clathrin, adaptors and disease: insights from the yeast Saccharomyces cerevisiae. Front. Biosci. 18: 862– 891. 10.2741/4149 23747853 · DOI
  64. Nam A.S., Yin Y., von Marschall Z., and Fisher L.W. 2014 Efficient trafficking of acidic proteins out of the endoplasmic reticulum involves a conserved amino terminal IleProVal (IPV)-like tripeptide motif. Connect. Tissue Res. 55(Suppl 1): 138– 141. 10.3109/03008207.2014.923852 24844412 PMC4153534 · DOI
  65. Ng D.T., Brown J.D., and Walter P. 1996 Signal sequences specify the targeting route to the endoplasmic reticulum membrane. J. Cell Biol. 134: 269– 278. 10.1083/jcb.134.2.269 8707814 PMC2120870 · DOI
  66. Okamoto M., Kurokawa K., Matsuura-Tokita K., Saito C., Hirata R., and Nakano A. 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. 10.1242/jcs.100065 22467862 · DOI
  67. Orci L., Ravazzola M., Volchuk A., Engel T., Gmachl M., Amherdt M., Perrelet A., Söllner T.H., and Rothman J.E. 2000 Anterograde flow of cargo across the Golgi stack potentially mediated via bidirectional “percolating” COPI vesicles. Proc. Natl. Acad. Sci. USA. 97: 10400– 10405. 10.1073/pnas.190292497 10962035 PMC27036 · DOI
  68. 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. 10.1038/ncb1195 15516922 · DOI
  69. Paetzel M., Karla A., Strynadka N.C., and Dalbey R.E. 2002 Signal peptidases. Chem. Rev. 102: 4549– 4580. 10.1021/cr010166y 12475201 · DOI · Paper page
  70. Papanikou E., and Glick B.S. 2014 Golgi compartmentation and identity. Curr. Opin. Cell Biol. 29: 74– 81. 10.1016/j.ceb.2014.04.010 24840895 PMC4130901 · DOI
  71. Papanikou E., Day K.J., Austin J. II, and Glick B.S. 2015 COPI selectively drives maturation of the early Golgi. eLife. 4: e13232 10.7554/eLife.13232 26709839 PMC4758959 · DOI
  72. Patterson G.H., Hirschberg K., Polishchuk R.S., Gerlich D., Phair R.D., and Lippincott-Schwartz J. 2008 Transport through the Golgi apparatus by rapid partitioning within a two-phase membrane system. Cell. 133: 1055– 1067. 10.1016/j.cell.2008.04.044 18555781 PMC2481404 · DOI
  73. Pellett P.A., Dietrich F., Bewersdorf J., Rothman J.E., and Lavieu G. 2013 Inter-Golgi transport mediated by COPI-containing vesicles carrying small cargoes. eLife. 2: e01296 10.7554/eLife.01296 24137546 PMC3787390 · DOI
  74. Pfeffer S.R. 2010 How the Golgi works: a cisternal progenitor model. Proc. Natl. Acad. Sci. USA. 107: 19614– 19618. 10.1073/pnas.1011016107 21045128 PMC2993360 · DOI
  75. Presley J.F., Cole N.B., Schroer T.A., Hirschberg K., Zaal K.J.M., and Lippincott-Schwartz J. 1997 ER-to-Golgi transport visualized in living cells. Nature. 389: 81– 85. 10.1038/38001 9288971 · DOI
  76. Preuss D., Mulholland J., Franzusoff A., Segev N., and Botstein D. 1992 Characterization of the Saccharomyces Golgi complex through the cell cycle by immunoelectron microscopy. Mol. Biol. Cell. 3: 789– 803. 10.1091/mbc.3.7.789 1381247 PMC275635 · DOI
  77. Rivera V.M., Wang X., Wardwell S., Courage N.L., Volchuk A., Keenan T., Holt D.A., Gilman M., Orci L., Cerasoli F. Jr., 2000 Regulation of protein secretion through controlled aggregation in the endoplasmic reticulum. Science. 287: 826– 830. 10.1126/science.287.5454.826 10657290 · DOI
  78. Rivera-Molina F.E., and Novick P.J. 2009 A Rab GAP cascade defines the boundary between two Rab GTPases on the secretory pathway. Proc. Natl. Acad. Sci. USA. 106: 14408– 14413. 10.1073/pnas.0906536106 19666511 PMC2732877 · DOI
  79. Rockwell N.C., Krysan D.J., Komiyama T., and Fuller R.S. 2002 Precursor processing by Kex2/furin proteases. Chem. Rev. 102: 4525– 4548. 10.1021/cr010168i 12475200 · DOI
  80. Rogers B., Decottignies A., Kolaczkowski M., Carvajal E., Balzi E., and Goffeau A. 2001 The pleitropic drug ABC transporters from Saccharomyces cerevisiae. J. Mol. Microbiol. Biotechnol. 3: 207– 214. 11321575
  81. Rollins C.T., Rivera V.M., Woolfson D.N., Keenan T., Hatada M., Adams S.E., Andrade L.J., Yaeger D., van Schravendijk M.R., Holt D.A., 2000 A ligand-reversible dimerization system for controlling protein-protein interactions. Proc. Natl. Acad. Sci. USA. 97: 7096– 7101. 10.1073/pnas.100101997 10852943 PMC16505 · DOI
  82. Rossanese O.W., Soderholm J., Bevis B.J., Sears I.B., O’Connor J., Williamson E.K., and Glick B.S. 1999 Golgi structure correlates with transitional endoplasmic reticulum organization in Pichia pastoris and Saccharomyces cerevisiae. J. Cell Biol. 145: 69– 81. 10.1083/jcb.145.1.69 10189369 PMC2148216 · DOI
  83. Saegusa K., Sato M., Morooka N., Hara T., and Sato K. 2018 SFT-4/Surf4 control ER export of soluble cargo proteins and participate in ER exit site organization. J. Cell Biol. 217: 2073– 2085. 10.1083/jcb.201708115 29643117 PMC5987718 · DOI
  84. 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. 10.1091/mbc.e02-01-0027 12134087 PMC117331 · DOI
  85. Schüller C., Mamnun Y.M., Wolfger H., Rockwell N., Thorner J., and Kuchler K. 2007 Membrane-active compounds activate the transcription factors Pdr1 and Pdr3 connecting pleiotropic drug resistance and membrane lipid homeostasis in Saccharomyces cerevisiae. Mol. Biol. Cell. 18: 4932– 4944. 10.1091/mbc.e07-06-0610 17881724 PMC2096591 · DOI
  86. Shakoury-Elizeh M., Protchenko O., Berger A., Cox J., Gable K., Dunn T.M., Prinz W.A., Bard M., and Philpott C.C. 2010 Metabolic response to iron deficiency in Saccharomyces cerevisiae. J. Biol. Chem. 285: 14823– 14833. 10.1074/jbc.M109.091710 20231268 PMC2863190 · DOI · Paper page
  87. Spang A. 2015 The road not taken: less traveled roads from the TGN to the plasma membrane. Membranes (Basel). 5: 84– 98. 10.3390/membranes5010084 25764365 PMC4384092 · DOI
  88. Strack R.L., Strongin D.E., Bhattacharyya D., Tao W., Berman A., Broxmeyer H.E., Keenan R.J., and Glick B.S. 2008 A noncytotoxic DsRed variant for whole-cell labeling. Nat. Methods. 5: 955– 957. 10.1038/nmeth.1264 18953349 PMC4107390 · DOI
  89. Strack R.L., Bhattacharyya D., Glick B.S., and Keenan R.J. 2009 a Noncytotoxic orange and red/green derivatives of DsRed-Express2 for whole-cell labeling. BMC Biotechnol. 9: 32 10.1186/1472-6750-9-32 19344508 PMC2678115 · DOI
  90. Strack R.L., Hein B., Bhattacharyya D., Hell S.W., Keenan R.J., and Glick B.S. 2009 b A rapidly maturing far-red derivative of DsRed-Express2 for whole-cell labeling. Biochemistry. 48: 8279– 8281. 10.1021/bi900870u 19658435 PMC2861903 · DOI
  91. Tie H.C., Mahajan D., Chen B., Cheng L., VanDongen A.M., and Lu L. 2016 A novel imaging method for quantitative Golgi localization reveals differential intra-Golgi trafficking of secretory cargoes. Mol. Biol. Cell. 27: 848– 861. 10.1091/mbc.E15-09-0664 26764092 PMC4803310 · DOI
  92. Toshima J.Y., Nishinoaki S., Sato Y., Yamamoto W., Furukawa D., Siekhaus D.E., Sawaguchi A., and Toshima J. 2014 Bifurcation of the endocytic pathway into Rab5-dependent and -independent transport to the vacuole. Nat. Commun. 5: 3498 10.1038/ncomms4498 24667230 · DOI
  93. Trimble R.B., Maley F., and Chu F.K. 1983 Glycoprotein biosynthesis in yeast. protein conformation affects processing of high mannose oligosaccharides on carboxypeptidase Y and invertase. J. Biol. Chem. 258: 2562– 2567. 6401737
  94. Trucco A., Polishchuk R.S., Martella O., Di Pentima A., Fusella A., Di Giandomenico D., San Pietro E., Beznoussenko G.V., Polishchuk E.V., Baldassarre M., 2004 Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments. Nat. Cell Biol. 6: 1071– 1081. 10.1038/ncb1180 15502824 · DOI
  95. Valdivia R.H., Baggott D., Chuang J.S., and Schekman R.W. 2002 The yeast clathrin adaptor protein complex 1 is required for the efficient retention of a subset of late Golgi membrane proteins. Dev. Cell. 2: 283– 294. 10.1016/S1534-5807(02)00127-2 11879634 · DOI
  96. Vater C.A., Raymond C.K., Ekena K., Howald-Stevenson I., and Stevens T.H. 1992 The VPS1 protein, a homolog of dynamin required for vacuolar protein sorting in Saccharomyces cerevisiae, is a GTPase with two functionally separable domains. J. Cell Biol. 119: 773– 786. 10.1083/jcb.119.4.773 1429836 PMC2289700 · DOI
  97. 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. 10.1083/jcb.201207180 23266954 PMC3529532 · DOI
  98. Wach A., Brachat A., Pöhlmann R., and Philippsen P. 1994 New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast. 10: 1793– 1808. 10.1002/yea.320101310 7747518 · DOI
  99. Whitfield S.T., Burston H.E., Bean B.D., Raghuram N., Maldonado-Báez L., Davey M., Wendland B., and Conibear E. 2016 The alternate AP-1 adaptor subunit Apm2 interacts with the Mil1 regulatory protein and confers differential cargo sorting. Mol. Biol. Cell. 27: 588– 598. 10.1091/mbc.e15-09-0621 26658609 PMC4751606 · DOI
  100. Willer M., Forte G.M., and Stirling C.J. 2008 Sec61p is required for ERAD-L: genetic dissection of the translocation and ERAD-L functions of Sec61P using novel derivatives of CPY. J. Biol. Chem. 283: 33883– 33888. 10.1074/jbc.M803054200 18819915 PMC2590686 · DOI
  101. Wooding S., and Pelham H.R.B. 1998 The dynamics of Golgi protein traffic visualized in living yeast cells. Mol. Biol. Cell. 9: 2667– 2680. 10.1091/mbc.9.9.2667 9725919 PMC25539 · DOI
  102. Wu H., Ng B.S., and Thibault G. 2014 Endoplasmic reticulum stress response in yeast and humans. Biosci. Rep. 34: e00118 10.1042/BSR20140058 24909749 PMC4076835 · DOI
  103. Yin Y., Garcia M.R., Novak A.J., Saunders A.M., Ank R.S., Nam A.S., and Fisher L.W. 2018 Surf4 (Erv29p) binds amino-terminal tripeptide motifs of soluble cargo proteins with different affinities, enabling prioritization of their exit from the endoplasmic reticulum. PLoS Biol. 16: e2005140 10.1371/journal.pbio.2005140 30086131 PMC6097701 · DOI

Cited by

Sorted by citations

Authors
Casler, J. C., Papanikou, E., Barrero, J. J., & Glick, B. S.
Affiliations
University of Chicago (US)
Corresponding author
Glick, Benjamin S.
ORCID
Venue
Journal of Cell Biology
Publisher
Rockefeller University Press
Published
2019-03-11
Volume
218
Issue
5
Pages
1582-1601
ISSN
  • 0021-9525 (ISSN-L)
  • 1540-8140
DOI
10.1083/jcb.201807195
PMC
PMC6504904
OpenAlex
W2921054355
Cited by
77
References
0
Citations by year
2026: 11 · 2025: 7 · 2024: 11 · 2023: 6 · 2022: 12 · 2021: 7 · 2020: 13 · 2019: 10
FWCI
5.51
Type
journal article
Language
en
Open access
Licence
Locations
  • The Journal of Cell Biology (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health (R01 GM104010)
  • NIH (T32 GM007183, P30 CA014599)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Keywords
Golgi maturation, Golgi cisternae, ER exit
MeSH terms
Biological Transport, Endoplasmic Reticulum, Golgi Apparatus, Intracellular Membranes, Microscopy, Fluorescence, Saccharomyces cerevisiae, Transcription Factor AP-1, Saccharomyces cerevisiae Proteins

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review