Skip to main content
SpringerLink
Log in

A three-stage model of Golgi structure and function

  • Review
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

Scientific inquiry starts with observation. The more we can see, the more we can investigate.

Martin Chalfie

2008 Nobel Lecture

Abstract

The Golgi apparatus contains multiple classes of cisternae that differ in structure, composition, and function, but there is no consensus about the number and definition of these classes. A useful way to classify Golgi cisternae is according to the trafficking pathways by which the cisternae import and export components. By this criterion, we propose that Golgi cisternae can be divided into three classes that correspond to functional stages of maturation. First, cisternae at the cisternal assembly stage receive COPII vesicles from the ER and recycle components to the ER in COPI vesicles. At this stage, new cisternae are generated. Second, cisternae at the carbohydrate synthesis stage exchange material with one another via COPI vesicles. At this stage, most of the glycosylation and polysaccharide synthesis reactions occur. Third, cisternae at the carrier formation stage produce clathrin-coated vesicles and exchange material with endosomes. At this stage, biosynthetic cargo proteins are packaged into various transport carriers, and the cisternae ultimately disassemble. Discrete transitions occur as a cisterna matures from one stage to the next. Within each stage, the structure and composition of a cisterna can evolve, but the trafficking pathways remain unchanged. This model offers a unified framework for understanding the properties of the Golgi in diverse organisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Anitei M, Hoflack B (2011) Exit from the trans-Golgi network: from molecules to mechanisms. Curr Opin Cell Biol 23:443–451

    Article  PubMed  CAS  Google Scholar 

  • Appenzeller-Herzog C, Hauri HP (2006) The ER-Golgi intermediate compartment (ERGIC): in search of its identity and function. J Cell Sci 119:2173–2183

    Article  PubMed  CAS  Google Scholar 

  • Atmodjo MA, Hao Z, Mohnen D (2013) Evolving views of pectin biosynthesis. Annu Rev Plant Biol 64:747–779

    Article  PubMed  CAS  Google Scholar 

  • Banfield DK (2011) Mechanisms of protein retention in the Golgi. Cold Spring Harb Perspect Biol 3:a005264

    Article  PubMed  CAS  Google Scholar 

  • Bankaitis VA, Garcia-Mata R, Mousley CJ (2012) Golgi membrane dynamics and lipid metabolism. Curr Biol 22:R414–R424

    Article  PubMed  CAS  Google Scholar 

  • Bannykh SI, Balch WE (1997) Membrane dynamics at the endoplasmic reticulum-Golgi interface. J Cell Biol 138:1–4

    Article  PubMed  CAS  Google Scholar 

  • Bard F, Malhotra V (2006) The formation of TGN-to-plasma membrane transport carriers. Annu Rev Cell Dev Biol 22:439–455

    Article  PubMed  CAS  Google Scholar 

  • Barlowe CK, Miller EA (2013) Secretory protein biogenesis and traffic in the early secretory pathway. Genetics 193:383–410

    Article  PubMed  CAS  Google Scholar 

  • Becker B, Melkonian M (1996) The secretory pathway of protists: spatial and functional organization and evolution. Microbiol Rev 60:697–721

    PubMed  CAS  Google Scholar 

  • Behnia R, Barr FA, Flanagan JJ, Barlowe C, Munro S (2007) The yeast orthologue of GRASP65 forms a complex with a coiled-coil protein that contributes to ER to Golgi traffic. J Cell Biol 176:255–261

    Article  PubMed  CAS  Google Scholar 

  • Bentley M, Liang Y, Mullen K, Xu D, Sztul E, Hay JC (2006) SNARE status regulates tether recruitment and function in homotypic COPII vesicle fusion. J Biol Chem 281:38825–38833

    Article  PubMed  CAS  Google Scholar 

  • Bevis BJ, Hammond AT, Reinke CA, Glick BS (2002) De novo formation of transitional ER sites and Golgi structures in Pichia pastoris. Nat Cell Biol 4:750–756

    Article  PubMed  CAS  Google Scholar 

  • Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116:153–166

    Article  PubMed  CAS  Google Scholar 

  • Brigance WT, Barlowe C, Graham TR (2000) Organization of the yeast Golgi complex into at least four functionally distinct compartments. Mol Biol Cell 11:171–182

    Article  PubMed  CAS  Google Scholar 

  • Chanat E, Huttner WB (1991) Milieu-induced, selective aggregation of regulated secretory proteins in the trans-Golgi network. J Cell Biol 115:1505–1519

    Article  PubMed  CAS  Google Scholar 

  • Chantalat S, Park SK, Hua Z, Liu K, Gobin R, Peyroche A, Rambourg A, Graham TR, Jackson CL (2004) The Arf activator Gea2p and the P-type ATPase Drs2p interact at the Golgi in Saccharomyces cerevisiae. J Cell Sci 117:711–722

    Article  PubMed  CAS  Google Scholar 

  • Cosson P, Amherdt M, Rothman JE, Orci L (2002) A resident Golgi protein is excluded from peri-Golgi vesicles in NRK cells. Proc Natl Acad Sci USA 99:12831–12834

    Article  PubMed  CAS  Google Scholar 

  • Daboussi L, Costaguta G, Payne GS (2012) Phosphoinositide-mediated clathrin adaptor progression at the trans-Golgi network. Nat Cell Biol 14:239–248

    Article  PubMed  CAS  Google Scholar 

  • De Matteis MA, Luini A (2008) Exiting the Golgi complex. Nat Rev Mol Cell Biol 9:273–284

    Article  PubMed  CAS  Google Scholar 

  • Dettmer J, Hong-Hermesdorf A, Stierhof YD, Schumacher K (2006) Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18:715–730

    Article  PubMed  CAS  Google Scholar 

  • Dick G, Akslen-Hoel LK, Grøndahl F, Kjos I, Prydz K (2012) Proteoglycan synthesis and Golgi organization in polarized epithelial cells. J Histochem Cytochem 60:926–935

    Article  PubMed  CAS  Google Scholar 

  • Donohoe BS, Kang BH, Staehelin LA (2007) Identification and characterization of COPIa- and COPIb-type vesicle classes associated with plant and algal Golgi. Proc Natl Acad Sci USA 104:163–168

    Article  PubMed  CAS  Google Scholar 

  • Donohoe BS, Kang BH, Gerl MJ, Gergely ZR, McMichael CM, Bednarek SY, Staehelin LA (2013) cis-Golgi cisternal assembly and biosynthetic activation occur sequentially in plants and algae. Traffic 14:551–567

    Article  PubMed  CAS  Google Scholar 

  • Driouich A, Staehelin LA (1997) The plant Golgi apparatus: structural organization and functional properties. In: Berger EG, Roth J (eds) The Golgi apparatus. Birkhäuser, Basel, pp 275–301

    Chapter  Google Scholar 

  • Duden R, Schekman R (1997) Insights into Golgi function through mutants in yeast and animal cells. In: Berger EG, Roth J (eds) The Golgi apparatus. Birkhäuser Verlag, Basel, pp 219–246

    Chapter  Google Scholar 

  • Dunphy WG, Rothman JE (1985) Compartmental organization of the Golgi stack. Cell 42:13–21

    Article  PubMed  CAS  Google Scholar 

  • Farquhar MG, Hauri H-P (1997) Protein sorting and vesicular traffic in the Golgi apparatus. In: Berger EG, Roth J (eds) The Golgi apparatus. Birkhäuser Verlag, Basel, pp 63–129

    Chapter  Google Scholar 

  • Farquhar MG, Palade GE (1981) The Golgi apparatus (complex)—(1954–1981)—from artifact to center stage. J Cell Biol 91:77s–103s

    Article  PubMed  CAS  Google Scholar 

  • Faso C, Boulaflous A, Brandizzi F (2009) The plant Golgi apparatus: last 10 years of answered and open questions. FEBS Lett 583:3752–3757

    Article  PubMed  CAS  Google Scholar 

  • Gilchrist A, Au CE, Hiding J, Bell AW, Fernandez-Rodriguez J, Lesimple S, Nagaya H, Roy L, Gosline SJ, Hallett M, Paiement J, Kearney RE, Nilsson T, Bergeron JJ (2006) Quantitative proteomics analysis of the secretory pathway. Cell 127:1265–1281

    Article  PubMed  CAS  Google Scholar 

  • Glick BS, Luini A (2011) Models for Golgi traffic: a critical assessment. Cold Spring Harb Perspect Biol 3:a005215

    Article  PubMed  CAS  Google Scholar 

  • Glick BS, Malhotra V (1998) The curious status of the Golgi apparatus. Cell 95:883–889

    Article  PubMed  CAS  Google Scholar 

  • Glick BS, Nakano A (2009) Membrane traffic within the Golgi stack. Annu Rev Cell Dev Biol 25:113–132

    Article  PubMed  CAS  Google Scholar 

  • Glick BS, Elston T, Oster G (1997) A cisternal maturation mechanism can explain the asymmetry of the Golgi stack. FEBS Lett 414:177–181

    Article  PubMed  CAS  Google Scholar 

  • Goldberg DE, Kornfeld S (1983) Evidence for extensive subcellular organization of asparagine-linked oligosaccharide processing and lysosomal enzyme phosphorylation. J Biol Chem 258:3159–3165

    PubMed  CAS  Google Scholar 

  • Graham TR, Burd CG (2011) Coordination of Golgi functions by phosphatidylinositol 4-kinases. Trends Cell Biol 21:113–121

    Article  PubMed  CAS  Google Scholar 

  • Griffiths G, Simons K (1986) The trans Golgi network: sorting at the exit site of the Golgi complex. Science 234:438–443

    Article  PubMed  CAS  Google Scholar 

  • Hanada K, Kumagai K, Tomishige N, Yamaji T (2009) CERT-mediated trafficking of ceramide. Biochim Biophys Acta 1791:684–691

    Article  PubMed  CAS  Google Scholar 

  • Hawes C (2005) Cell biology of the plant Golgi apparatus. New Phytol 165:29–44

    Article  PubMed  Google Scholar 

  • Jedd G, Richardson CJ, Litt RJ, Segev N (1995) The Ypt1 GTPase is essential for the first two steps of the yeast secretory pathway. J Cell Biol 131:583–590

    Article  PubMed  CAS  Google Scholar 

  • Jedd G, Mulholland J, Segev N (1997) Two new Ypt GTPases are required for exit from the yeast trans-Golgi compartment. J Cell Biol 137:563–580

    Article  PubMed  CAS  Google Scholar 

  • Kang BH, Staehelin LA (2008) ER-to-Golgi transport by COPII vesicles in Arabidopsis involves a ribosome-excluding scaffold that is transferred with the vesicles to the Golgi matrix. Protoplasma 234:51–64

    Article  PubMed  CAS  Google Scholar 

  • Kang BH, Nielsen E, Preuss ML, Mastronarde D, Staehelin LA (2011) Electron tomography of RabA4b- and PI-4 Kβ1-labeled trans Golgi network compartments in Arabidopsis. Traffic 12:313–329

    Article  PubMed  CAS  Google Scholar 

  • Kinseth MA, Anjard C, Fuller D, Guizzunti G, Loomis WF, Malhotra V (2007) The Golgi associated protein GRASP is required for unconventional secretion during development. Cell 130:524–534

    Google Scholar 

  • Klausner RD, Donaldson JG, Lippincott-Schwartz J (1992) Brefeldin A: insights into the control of membrane traffic and organelle structure. J Cell Biol 116:1071–1080

    Article  PubMed  CAS  Google Scholar 

  • Klumperman J (2011) Architecture of the mammalian Golgi. Cold Spring Harb Perspect Biol 3:a005181

    Article  PubMed  CAS  Google Scholar 

  • Kornfeld R, Kornfeld S (1985) Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem 54:631–664

    Article  PubMed  CAS  Google Scholar 

  • Kweon HS, Beznoussenko GV, Micaroni M, Polishchuk RS, Trucco A, Martella O, Di Giandomenico D, Marra P, Fusella A, Di Pentima A, Berger EG, Geerts WJ, Koster AJ, Burger KN, Luini A, Mironov AA (2004) Golgi enzymes are enriched in perforated zones of Golgi cisternae but are depleted in COPI vesicles. Mol Biol Cell 15:4710–4724

    Article  PubMed  CAS  Google Scholar 

  • Ladinsky MS, Mastronarde DN, McIntosh JR, Howell KE, Staehelin LA (1999) Golgi structure in three dimensions: functional insights from the normal rat kidney cell. J Cell Biol 144:1135–1149

    Article  PubMed  CAS  Google Scholar 

  • Lanoix J, Ouwendijk J, Stark A, Szafer E, Cassel D, Dejgaard K, Weiss M, Nilsson T (2001) Sorting of Golgi resident proteins into different subpopulations of COPI vesicles: a role for ArfGAP1. J Cell Biol 155:1199–1212

    Article  PubMed  CAS  Google Scholar 

  • Lavieu G, Zheng H, Rothman JE (2013) Stapled Golgi cisternae remain in place as cargo passes through the stack. eLife 2:e00558

  • Lerich A, Hillmer S, Langhans M, Scheuring D, van Bentum P, Robinson DG (2012) ER import sites and their relationship to ER exit sites: a new model for bidirectional ER-Golgi transport in higher plants. Front Plant Sci 3:143

    Article  PubMed  Google Scholar 

  • Levi SK, Bhattacharyya D, Strack RL, Austin JRI, Glick BS (2010) The yeast GRASP Grh1 colocalizes with COPII and is dispensable for organizing the secretory pathway. Traffic 11:1168–1179

    Article  PubMed  CAS  Google Scholar 

  • Lippincott-Schwartz J, Roberts TH, Hirschberg K (2000) Secretory protein trafficking and organelle dynamics in living cells. Annu Rev Cell Dev Biol 16:557–589

    Article  PubMed  CAS  Google Scholar 

  • Liu S, Storrie B (2012) Are Rab proteins the link between Golgi organization and membrane trafficking? Cell Mol Life Sci 69:4093–4106

    Article  PubMed  CAS  Google Scholar 

  • Lord C, Ferro-Novick S, Miller EA (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

    Article  PubMed  CAS  Google Scholar 

  • Losev E, Reinke CA, Jellen J, Strongin DE, Bevis BJ, Glick BS (2006) Golgi maturation visualized in living yeast. Nature 22:1002–1006

    Article  CAS  Google Scholar 

  • Lowery J, Szul T, Styers M, Holloway Z, Oorschot V, Klumperman J, Sztul E (2013) The Sec7 guanine nucleotide exchange factor GBF1 regulates membrane recruitment of BIG1 and BIG2 guanine nucleotide exchange factors to the trans-Golgi network (TGN). J Biol Chem 288:11532–11545

    Article  PubMed  CAS  Google Scholar 

  • Machamer CE (1993) Targeting and retention of Golgi proteins. Curr Opin Cell Biol 5:606–612

    Article  PubMed  CAS  Google Scholar 

  • Malsam J, Söllner TH (2011) Organization of SNAREs within the Golgi stack. Cold Spring Harb Perspect Biol 3:a005249

    Article  PubMed  CAS  Google Scholar 

  • Malsam J, Satoh A, Pelletier L, Warren G (2005) Golgin tethers define subpopulations of COPI vesicles. Science 307:1095–1098

    Article  PubMed  CAS  Google Scholar 

  • Marra P, Maffucci T, Daniele T, Di Tullio G, Ikehara Y, Chan EKL, Luini A, Beznoussenko G, Mironov A, De Matteis MA (2001) The GM130 and GRASP65 Golgi proteins cycle through and define a subdomain of the intermediate compartment. Nat Cell Biol 3:1101–1113

    Article  PubMed  CAS  Google Scholar 

  • Marsh BJ, Mastronarde DN, Buttle KF, Howell KE, McIntosh JR (2001) Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography. Proc Natl Acad Sci USA 98:2399–2406

    Article  PubMed  CAS  Google Scholar 

  • Marsh BJ, Volkmann N, McIntosh JR, Howell KE (2004) Direct continuities between cisternae at different levels of the Golgi complex in glucose-stimulated mouse islet beta cells. Proc Natl Acad Sci USA 101:5565–5570

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Menárguez JA, Prekeris R, Oorschot VMJ, Scheller R, Slot JW, Geuze HJ, Klumperman J (2001) Peri-Golgi vesicles contain retrograde but not anterograde proteins consistent with the cisternal progression model of intra-Golgi transport. J Cell Biol 155:1213–1224

    Article  PubMed  Google Scholar 

  • Matsuura-Tokita K, Takeuchi M, Ichihara A, Mikuriya K, Nakano A (2006) Live imaging of yeast Golgi cisternal maturation. Nature 22:1007–1010

    Article  CAS  Google Scholar 

  • Mellman I, Simons K (1992) The Golgi complex: in vitro veritas? Cell 68:829–840

    Article  PubMed  CAS  Google Scholar 

  • Mizuno-Yamasaki E, Rivera-Molina F, Novick P (2012) GTPase networks in membrane traffic. Annu Rev Biochem 81:637–659

    Article  PubMed  CAS  Google Scholar 

  • Moelleken J, Malsam J, Betts MJ, Movafeghi A, Reckmann I, Meissner I, Hellwig A, Russell RB, Söllner T, Brügger B, Wieland FT (2007) Differential localization of coatomer complex isoforms within the Golgi apparatus. Proc Natl Acad Sci USA 104:4425–4430

    Article  PubMed  CAS  Google Scholar 

  • Mogelsvang S, Gomez-Ospina N, Soderholm J, Glick BS, Staehelin LA (2003) Tomographic evidence for continuous turnover of Golgi cisternae in Pichia pastoris. Mol Biol Cell 14:2277–2291

    Article  PubMed  CAS  Google Scholar 

  • Mogelsvang S, Marsh BJ, Ladinsky MS, Howell KE (2004) Predicting function from structure: 3D structure studies of the mammalian Golgi complex. Traffic 5:338–345

    Article  PubMed  CAS  Google Scholar 

  • Mollenhauer HH, Morré DJ (1991) Perspectives on Golgi apparatus form and function. J Electron Microsc Tech 17:2–14

    Article  PubMed  CAS  Google Scholar 

  • Mollenhauer HH, Whaley WG (1963) An observation on the functioning of the Golgi apparatus. J Cell Biol 17:222–225

    Article  PubMed  CAS  Google Scholar 

  • Mowbrey K, Dacks JB (2009) Evolution and diversity of the Golgi body. FEBS Lett 583:3738–3745

    Article  PubMed  CAS  Google Scholar 

  • Munro S (2011) The golgin coiled-coil proteins of the Golgi apparatus. Cold Spring Harb Perspect Biol 3:a005256

    Article  PubMed  CAS  Google Scholar 

  • Myers MD, Payne GS (2013) Clathrin, adaptors and disease: insights from the yeast Saccharomyces cerevisiae. Front Biosci 18:862–891

    Article  CAS  Google Scholar 

  • Nebenführ A, Ritzenthaler C, Robinson DG (2002) Brefeldin A: deciphering an enigmatic inhibitor of secretion. Plant Physiol 130:1102–1108

    Article  PubMed  CAS  Google Scholar 

  • Nilsson T, Pypaert M, Hoe MH, Slusarewicz P, Berger EG, Warren G (1993) Overlapping distribution of two glycosyltransferases in the Golgi apparatus of HeLa cells. J Cell Biol 120:5–13

    Article  PubMed  CAS  Google Scholar 

  • Orci L, Stamnes M, Ravazzola M, Amherdt M, Perrelet A, Söllner TH, Rothman JE (1997) Bidirectional transport by distinct populations of COPI-coated vesicles. Cell 90:335–349

    Article  PubMed  CAS  Google Scholar 

  • Orci L, Amherdt M, Ravazzola M, Perrelet A, Rothman JE (2000a) Exclusion of Golgi residents from transport vesicles budding from Golgi cisternae in intact cells. J Cell Biol 150:1263–1270

    Article  PubMed  CAS  Google Scholar 

  • Orci L, Ravazzola M, Volchuk A, Engel T, Gmachl M, Amherdt M, Perrelet A, Söllner TH, Rothman JE (2000b) Anterograde flow of cargo across the Golgi stack potentially mediated via bidirectional “percolating” COPI vesicles. Proc Natl Acad Sci USA 97:10400–10405

    Article  PubMed  CAS  Google Scholar 

  • Papanikou E, Glick BS (2009) The yeast Golgi apparatus: insights and mysteries. FEBS Lett 583:3746–3751

    Article  PubMed  CAS  Google Scholar 

  • Parsons HT, Christiansen K, Knierim B, Carroll A, Ito J, Batth TS, Smith-Moritz AM, Morrison S, McInerney P, Hadi MZ, Auer M, Mukhopadhyay A, Petzold CJ, Scheller HV, Loqué D, Heazlewood JL (2012) Isolation and proteomic characterization of the Arabidopsis Golgi defines functional and novel components involved in plant cell wall biosynthesis. Plant Physiol 159:12–26

    Article  PubMed  CAS  Google Scholar 

  • Patterson GH, Hirschberg K, Polishchuk RS, Gerlich D, Phair RD, Lippincott-Schwartz J (2008) Transport through the Golgi apparatus by rapid partitioning within a two-phase membrane system. Cell 133:1055–1067

    Article  PubMed  CAS  Google Scholar 

  • Pelham HRB (1988) Evidence that luminal ER proteins are sorted from secreted proteins in a post-ER compartment. EMBO J 7:913–918

    PubMed  CAS  Google Scholar 

  • Pelham HRB (1998) Getting through the Golgi complex. Trends Cell Biol 8:45–49

    Article  PubMed  CAS  Google Scholar 

  • Pfeffer SR (2010) How the Golgi works: a cisternal progenitor model. Proc Natl Acad Sci USA 107:19614–19618

    Article  PubMed  CAS  Google Scholar 

  • Pfeffer SR (2011) Entry at the trans-face of the Golgi. Cold Spring Harb Perspect Biol 3:a005272

    Article  PubMed  CAS  Google Scholar 

  • Polishchuk RS, Polishchuk EV, Marra P, Alberti S, Buccione R, Luini A, Mironov AA (2000) Correlative light-electron microscopy reveals the tubular-saccular ultrastructure of carriers operating between the Golgi apparatus and plasma membrane. J Cell Biol 148:45–58

    Article  PubMed  CAS  Google Scholar 

  • Popoff V, Adolf F, Brügger B, Wieland F (2011) COPI budding within the Golgi stack. Cold Spring Harb Perspect Biol 3:a005231

    Article  PubMed  CAS  Google Scholar 

  • Preuss D, Mulholland J, Franzusoff A, Segev N, Botstein D (1992) Characterization of the Saccharomyces Golgi complex through the cell cycle by immunoelectron microscopy. Mol Biol Cell 3:789–803

    Article  PubMed  CAS  Google Scholar 

  • Rabouille C, Klumperman J (2005) Opinion: the maturing role of COPI vesicles in intra-Golgi transport. Nat Rev Mol Cell Biol 6:812–817

    Article  PubMed  CAS  Google Scholar 

  • Rabouille C, Hui N, Hunte F, Kieckbusch R, Berger EG, Warren G, Nilsson T (1995) Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides. J Cell Sci 108:1617–1627

    PubMed  CAS  Google Scholar 

  • Rambourg A, Clermont Y (1997) Three-dimensional structure of the Golgi apparatus in mammalian cells. In: Berger EG, Roth J (eds) The Golgi apparatus. Birkhäuser Verlag, Basel, pp 37–61

    Chapter  Google Scholar 

  • Ren Y, Yip CK, Tripathi A, Huie D, Jeffrey PD, Walz T, Hughson FM (2009) A structure-based mechanism for vesicle capture by the multisubunit tethering complex Dsl1. Cell 139:1119–1129

    Article  PubMed  CAS  Google Scholar 

  • Richardson BC, McDonold CM, Fromme JC (2012) The Sec7 Arf-GEF is recruited to the trans-Golgi network by positive feedback. Dev Cell 22:799–810

    Article  PubMed  CAS  Google Scholar 

  • Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122:735–749

    Article  PubMed  CAS  Google Scholar 

  • Rizzo R, Parashuraman S, Mirabelli P, Puri C, Lucocq J, Luini A (2013) The dynamics of engineered resident proteins in the mammalian Golgi complex relies on cisternal maturation. J Cell Biol 201:1027–1036

    Article  PubMed  CAS  Google Scholar 

  • Rockwell NC, Krysan DJ, Komiyama T, Fuller RS (2002) Precursor processing by Kex2/furin proteases. Chem Rev 102:4525–4548

    Article  PubMed  CAS  Google Scholar 

  • Rothman JE (1981) The Golgi apparatus: two organelles in tandem. Science 213:1212–1219

    Article  PubMed  CAS  Google Scholar 

  • Rothman JE, Wieland FT (1996) Protein sorting by transport vesicles. Science 272:227–234

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-May E, Kim SJ, Brandizzi F, Rose JK (2012) The secreted plant N-glycoproteome and associated secretory pathways. Front Plant Sci 3:117

    PubMed  CAS  Google Scholar 

  • Schmidt WK, Moore HP (1995) Ionic milieu controls the compartment-specific activation of pro-opiomelanocortin processing in AtT-20 cells. Mol Biol Cell 6:1271–1285

    Article  PubMed  CAS  Google Scholar 

  • Sharpe HJ, Stevens TJ, Munro S (2010) A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 142:158–169

    Article  PubMed  CAS  Google Scholar 

  • Smith RD, Lupashin VV (2008) Role of the conserved oligomeric Golgi (COG) complex in protein glycosylation. Carbohydr Res 343:2024–2031

    Article  PubMed  CAS  Google Scholar 

  • Sönnichsen B, Lowe M, Levine T, Jämsä E, Dirac-Svejstrup B, Warren G (1998) A role for giantin in docking COPI vesicles to Golgi membranes. J Cell Biol 140:1013–1021

    Article  PubMed  Google Scholar 

  • Spang A (2012) The DSL1 complex: the smallest but not the least CATCHR. Traffic 13:908–913

    Article  PubMed  CAS  Google Scholar 

  • Spang A, Herrmann JM, Hamamoto S, Schekman R (2001) The ADP ribosylation factor-nucleotide exchange factors Gea1p and Gea2p have overlapping, but not redundant functions in retrograde transport from the Golgi to the endoplasmic reticulum. Mol Biol Cell 12:1035–1045

    Article  PubMed  CAS  Google Scholar 

  • Staehelin LA, Kang BH (2008) Nanoscale architecture of endoplasmic reticulum export sites and of Golgi membranes as determined by electron tomography. Plant Physiol 147:1454–1468

    Article  PubMed  CAS  Google Scholar 

  • Stalder D, Antonny B (2013) Arf GTPase regulation through cascade mechanisms and positive feedback loops. FEBS Lett 587:2028–2035

    Article  PubMed  CAS  Google Scholar 

  • Stanley P (2011) Golgi glycosylation. Cold Spring Harb Perspect Biol 3:a005199

    Article  PubMed  CAS  Google Scholar 

  • Storrie B, Micaroni M, Morgan GP, Jones N, Kamykowski JA, Wilkins N, Pan TH, Marsh BJ (2012) Electron tomography reveals Rab6 is essential to the trafficking of trans-Golgi clathrin and COPI-coated vesicles and the maintenance of Golgi cisternal number. Traffic 13:727–744

    Article  PubMed  CAS  Google Scholar 

  • Suvorova ES, Duden R, Lupashin VV (2002) The Sec34/Sec35p complex, a Ypt1p effector required for retrograde intra-Golgi trafficking, interacts with Golgi SNAREs and COPI vesicle coat proteins. J Cell Biol 157:631–643

    Article  PubMed  CAS  Google Scholar 

  • Trucco A, Polishchuk RS, Martella O, Pentima AD, Fusella A, Giandomenico DD, Pietro ES, Beznoussenko GV, Polishchuk EV, Baldassarre M, Buccione R, Geerts WJ, Koster AJ, Burger KN, Mironov AA, Luini A (2004) Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments. Nat Cell Biol 6:1071–1081

    Article  PubMed  CAS  Google Scholar 

  • Tsai PC, Hsu JW, Liu YW, Chen KY, Lee FJ (2013) Arl1p regulates spatial membrane organization at the trans-Golgi network through interaction with Arf-GEF Gea2p and flippase Drs2p. Proc Natl Acad Sci USA 110:E668–E677

    Article  PubMed  CAS  Google Scholar 

  • Tu L, Tai WC, Chen L, Banfield DK (2008) Signal-mediated dynamic retention of glycosyltransferases in the Golgi. Science 321:404–407

    Article  PubMed  CAS  Google Scholar 

  • Ungar D, Oka T, Krieger M, Hughson FM (2006) Retrograde transport on the COG railway. Trends Cell Biol 16:113–120

    Article  PubMed  CAS  Google Scholar 

  • Valdivia RH, Baggott D, Chuang JS, Schekman R (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

    Article  PubMed  CAS  Google Scholar 

  • Velasco A, Hendricks L, Moremen KW, Tulsiani DRP, Touster O, Farquhar MG (1993) Cell type-dependent variations in the subcellular distribution of α-mannosidase I and II. J Cell Biol 122:39–51

    Article  PubMed  CAS  Google Scholar 

  • Viotti C, Bubeck J, Stierhof YD, Krebs M, Langhans M, van den Berg W, van Dongen W, Richter S, Geldner N, Takano J, Jürgens G, de Vries SC, Robinson DG, Schumacher K (2010) Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 22:1344–1357

    Article  PubMed  CAS  Google Scholar 

  • von Blume J, Alleaume AM, Kienzle C, Carreras-Sureda A, Valverde M, Malhotra V (2012) Cab45 is required for Ca2+-dependent secretory cargo sorting at the trans-Golgi network. J Cell Biol 199:1057–1066

    Article  CAS  Google Scholar 

  • Wakana Y, van Galen J, Meissner F, Scarpa M, Polishchuk RS, Mann M, Malhotra V (2012) A new class of carriers that transport selective cargo from the trans Golgi network to the cell surface. EMBO J 31:3976–3990

    Article  PubMed  CAS  Google Scholar 

  • Woollard AA, Moore I (2008) The functions of Rab GTPases in plant membrane traffic. Curr Opin Plant Biol 11:610–619

    Article  PubMed  CAS  Google Scholar 

  • Zeuschner D, Geerts WJ, van Donselaar E, Humbel BM, Slot JW, Koster AJ, Klumperman J (2006) Immuno-electron tomography of ER exit sites reveals the existence of free COPII-coated transport carriers. Nat Cell Biol 8:377–383

    Article  PubMed  CAS  Google Scholar 

  • Zhang GF, Staehelin LA (1992) Functional compartmentation of the Golgi apparatus of plant cells: immunocytochemical analysis of high-pressure frozen and freeze-substituted sycamore maple suspension culture cells. Plant Physiol 99:1070–1083

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Thanks to Vivek Malhotra and members of the Glick lab for helpful discussion. This work was supported by U.S. National Institutes of Health grants T32 GM007183 to K.J.D. and R01 GM061156 to B.S.G.

Author information

Authors and Affiliations

  1. Department of Molecular Genetics and Cell Biology, The University of Chicago, 920 East 58th Street, Chicago, IL, 60615, USA

    Kasey J. Day & Benjamin S. Glick

  2. Molecular, Cellular, and Developmental Biology, University of Colorado at Boulder, Boulder, CO, 80309-0347, USA

    L. Andrew Staehelin

Authors
  1. Kasey J. Day
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. Andrew Staehelin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Benjamin S. Glick
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Benjamin S. Glick.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Day, K.J., Staehelin, L.A. & Glick, B.S. A three-stage model of Golgi structure and function. Histochem Cell Biol 140, 239–249 (2013). https://doi.org/10.1007/s00418-013-1128-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-013-1128-3

Keywords

Search

Navigation