Advertisement

Histochemistry and Cell Biology

, Volume 140, Issue 3, pp 239–249 | Cite as

A three-stage model of Golgi structure and function

  • Kasey J. Day
  • L. Andrew Staehelin
  • Benjamin S. Glick
Review

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.

Keywords

Golgi Cisternal maturation COPI Clathrin Compartmentation Secretory pathway 

Notes

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.

References

  1. Anitei M, Hoflack B (2011) Exit from the trans-Golgi network: from molecules to mechanisms. Curr Opin Cell Biol 23:443–451PubMedCrossRefGoogle Scholar
  2. Appenzeller-Herzog C, Hauri HP (2006) The ER-Golgi intermediate compartment (ERGIC): in search of its identity and function. J Cell Sci 119:2173–2183PubMedCrossRefGoogle Scholar
  3. Atmodjo MA, Hao Z, Mohnen D (2013) Evolving views of pectin biosynthesis. Annu Rev Plant Biol 64:747–779PubMedCrossRefGoogle Scholar
  4. Banfield DK (2011) Mechanisms of protein retention in the Golgi. Cold Spring Harb Perspect Biol 3:a005264PubMedCrossRefGoogle Scholar
  5. Bankaitis VA, Garcia-Mata R, Mousley CJ (2012) Golgi membrane dynamics and lipid metabolism. Curr Biol 22:R414–R424PubMedCrossRefGoogle Scholar
  6. Bannykh SI, Balch WE (1997) Membrane dynamics at the endoplasmic reticulum-Golgi interface. J Cell Biol 138:1–4PubMedCrossRefGoogle Scholar
  7. Bard F, Malhotra V (2006) The formation of TGN-to-plasma membrane transport carriers. Annu Rev Cell Dev Biol 22:439–455PubMedCrossRefGoogle Scholar
  8. Barlowe CK, Miller EA (2013) Secretory protein biogenesis and traffic in the early secretory pathway. Genetics 193:383–410PubMedCrossRefGoogle Scholar
  9. Becker B, Melkonian M (1996) The secretory pathway of protists: spatial and functional organization and evolution. Microbiol Rev 60:697–721PubMedGoogle Scholar
  10. 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 176:255–261PubMedCrossRefGoogle Scholar
  11. 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 281:38825–38833PubMedCrossRefGoogle Scholar
  12. 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 4:750–756PubMedCrossRefGoogle Scholar
  13. Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116:153–166PubMedCrossRefGoogle Scholar
  14. Brigance WT, Barlowe C, Graham TR (2000) Organization of the yeast Golgi complex into at least four functionally distinct compartments. Mol Biol Cell 11:171–182PubMedCrossRefGoogle Scholar
  15. Chanat E, Huttner WB (1991) Milieu-induced, selective aggregation of regulated secretory proteins in the trans-Golgi network. J Cell Biol 115:1505–1519PubMedCrossRefGoogle Scholar
  16. 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 117:711–722PubMedCrossRefGoogle Scholar
  17. 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 99:12831–12834PubMedCrossRefGoogle Scholar
  18. Daboussi L, Costaguta G, Payne GS (2012) Phosphoinositide-mediated clathrin adaptor progression at the trans-Golgi network. Nat Cell Biol 14:239–248PubMedCrossRefGoogle Scholar
  19. De Matteis MA, Luini A (2008) Exiting the Golgi complex. Nat Rev Mol Cell Biol 9:273–284PubMedCrossRefGoogle Scholar
  20. 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 18:715–730PubMedCrossRefGoogle Scholar
  21. Dick G, Akslen-Hoel LK, Grøndahl F, Kjos I, Prydz K (2012) Proteoglycan synthesis and Golgi organization in polarized epithelial cells. J Histochem Cytochem 60:926–935PubMedCrossRefGoogle Scholar
  22. 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 104:163–168PubMedCrossRefGoogle Scholar
  23. 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 14:551–567PubMedCrossRefGoogle Scholar
  24. 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 275–301CrossRefGoogle Scholar
  25. 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 219–246CrossRefGoogle Scholar
  26. Dunphy WG, Rothman JE (1985) Compartmental organization of the Golgi stack. Cell 42:13–21PubMedCrossRefGoogle Scholar
  27. 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 63–129CrossRefGoogle Scholar
  28. Farquhar MG, Palade GE (1981) The Golgi apparatus (complex)—(1954–1981)—from artifact to center stage. J Cell Biol 91:77s–103sPubMedCrossRefGoogle Scholar
  29. Faso C, Boulaflous A, Brandizzi F (2009) The plant Golgi apparatus: last 10 years of answered and open questions. FEBS Lett 583:3752–3757PubMedCrossRefGoogle Scholar
  30. 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 127:1265–1281PubMedCrossRefGoogle Scholar
  31. Glick BS, Luini A (2011) Models for Golgi traffic: a critical assessment. Cold Spring Harb Perspect Biol 3:a005215PubMedCrossRefGoogle Scholar
  32. Glick BS, Malhotra V (1998) The curious status of the Golgi apparatus. Cell 95:883–889PubMedCrossRefGoogle Scholar
  33. Glick BS, Nakano A (2009) Membrane traffic within the Golgi stack. Annu Rev Cell Dev Biol 25:113–132PubMedCrossRefGoogle Scholar
  34. Glick BS, Elston T, Oster G (1997) A cisternal maturation mechanism can explain the asymmetry of the Golgi stack. FEBS Lett 414:177–181PubMedCrossRefGoogle Scholar
  35. Goldberg DE, Kornfeld S (1983) Evidence for extensive subcellular organization of asparagine-linked oligosaccharide processing and lysosomal enzyme phosphorylation. J Biol Chem 258:3159–3165PubMedGoogle Scholar
  36. Graham TR, Burd CG (2011) Coordination of Golgi functions by phosphatidylinositol 4-kinases. Trends Cell Biol 21:113–121PubMedCrossRefGoogle Scholar
  37. Griffiths G, Simons K (1986) The trans Golgi network: sorting at the exit site of the Golgi complex. Science 234:438–443PubMedCrossRefGoogle Scholar
  38. Hanada K, Kumagai K, Tomishige N, Yamaji T (2009) CERT-mediated trafficking of ceramide. Biochim Biophys Acta 1791:684–691PubMedCrossRefGoogle Scholar
  39. Hawes C (2005) Cell biology of the plant Golgi apparatus. New Phytol 165:29–44PubMedCrossRefGoogle Scholar
  40. 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 131:583–590PubMedCrossRefGoogle Scholar
  41. Jedd G, Mulholland J, Segev N (1997) Two new Ypt GTPases are required for exit from the yeast trans-Golgi compartment. J Cell Biol 137:563–580PubMedCrossRefGoogle Scholar
  42. 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 234:51–64PubMedCrossRefGoogle Scholar
  43. 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 12:313–329PubMedCrossRefGoogle Scholar
  44. 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 130:524–534Google Scholar
  45. Klausner RD, Donaldson JG, Lippincott-Schwartz J (1992) Brefeldin A: insights into the control of membrane traffic and organelle structure. J Cell Biol 116:1071–1080PubMedCrossRefGoogle Scholar
  46. Klumperman J (2011) Architecture of the mammalian Golgi. Cold Spring Harb Perspect Biol 3:a005181PubMedCrossRefGoogle Scholar
  47. Kornfeld R, Kornfeld S (1985) Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem 54:631–664PubMedCrossRefGoogle Scholar
  48. 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 15:4710–4724PubMedCrossRefGoogle Scholar
  49. 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 144:1135–1149PubMedCrossRefGoogle Scholar
  50. 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 155:1199–1212PubMedCrossRefGoogle Scholar
  51. Lavieu G, Zheng H, Rothman JE (2013) Stapled Golgi cisternae remain in place as cargo passes through the stack. eLife 2:e00558Google Scholar
  52. 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 3:143PubMedCrossRefGoogle Scholar
  53. 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 11:1168–1179PubMedCrossRefGoogle Scholar
  54. Lippincott-Schwartz J, Roberts TH, Hirschberg K (2000) Secretory protein trafficking and organelle dynamics in living cells. Annu Rev Cell Dev Biol 16:557–589PubMedCrossRefGoogle Scholar
  55. Liu S, Storrie B (2012) Are Rab proteins the link between Golgi organization and membrane trafficking? Cell Mol Life Sci 69:4093–4106PubMedCrossRefGoogle Scholar
  56. 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:a013367PubMedCrossRefGoogle Scholar
  57. Losev E, Reinke CA, Jellen J, Strongin DE, Bevis BJ, Glick BS (2006) Golgi maturation visualized in living yeast. Nature 22:1002–1006CrossRefGoogle Scholar
  58. 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 288:11532–11545PubMedCrossRefGoogle Scholar
  59. Machamer CE (1993) Targeting and retention of Golgi proteins. Curr Opin Cell Biol 5:606–612PubMedCrossRefGoogle Scholar
  60. Malsam J, Söllner TH (2011) Organization of SNAREs within the Golgi stack. Cold Spring Harb Perspect Biol 3:a005249PubMedCrossRefGoogle Scholar
  61. Malsam J, Satoh A, Pelletier L, Warren G (2005) Golgin tethers define subpopulations of COPI vesicles. Science 307:1095–1098PubMedCrossRefGoogle Scholar
  62. 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 3:1101–1113PubMedCrossRefGoogle Scholar
  63. 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 98:2399–2406PubMedCrossRefGoogle Scholar
  64. 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 101:5565–5570PubMedCrossRefGoogle Scholar
  65. 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 155:1213–1224PubMedCrossRefGoogle Scholar
  66. Matsuura-Tokita K, Takeuchi M, Ichihara A, Mikuriya K, Nakano A (2006) Live imaging of yeast Golgi cisternal maturation. Nature 22:1007–1010CrossRefGoogle Scholar
  67. Mellman I, Simons K (1992) The Golgi complex: in vitro veritas? Cell 68:829–840PubMedCrossRefGoogle Scholar
  68. Mizuno-Yamasaki E, Rivera-Molina F, Novick P (2012) GTPase networks in membrane traffic. Annu Rev Biochem 81:637–659PubMedCrossRefGoogle Scholar
  69. 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 104:4425–4430PubMedCrossRefGoogle Scholar
  70. 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 14:2277–2291PubMedCrossRefGoogle Scholar
  71. Mogelsvang S, Marsh BJ, Ladinsky MS, Howell KE (2004) Predicting function from structure: 3D structure studies of the mammalian Golgi complex. Traffic 5:338–345PubMedCrossRefGoogle Scholar
  72. Mollenhauer HH, Morré DJ (1991) Perspectives on Golgi apparatus form and function. J Electron Microsc Tech 17:2–14PubMedCrossRefGoogle Scholar
  73. Mollenhauer HH, Whaley WG (1963) An observation on the functioning of the Golgi apparatus. J Cell Biol 17:222–225PubMedCrossRefGoogle Scholar
  74. Mowbrey K, Dacks JB (2009) Evolution and diversity of the Golgi body. FEBS Lett 583:3738–3745PubMedCrossRefGoogle Scholar
  75. Munro S (2011) The golgin coiled-coil proteins of the Golgi apparatus. Cold Spring Harb Perspect Biol 3:a005256PubMedCrossRefGoogle Scholar
  76. Myers MD, Payne GS (2013) Clathrin, adaptors and disease: insights from the yeast Saccharomyces cerevisiae. Front Biosci 18:862–891CrossRefGoogle Scholar
  77. Nebenführ A, Ritzenthaler C, Robinson DG (2002) Brefeldin A: deciphering an enigmatic inhibitor of secretion. Plant Physiol 130:1102–1108PubMedCrossRefGoogle Scholar
  78. 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 120:5–13PubMedCrossRefGoogle Scholar
  79. 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 90:335–349PubMedCrossRefGoogle Scholar
  80. 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 150:1263–1270PubMedCrossRefGoogle Scholar
  81. 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 97:10400–10405PubMedCrossRefGoogle Scholar
  82. Papanikou E, Glick BS (2009) The yeast Golgi apparatus: insights and mysteries. FEBS Lett 583:3746–3751PubMedCrossRefGoogle Scholar
  83. 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 159:12–26PubMedCrossRefGoogle Scholar
  84. 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 133:1055–1067PubMedCrossRefGoogle Scholar
  85. Pelham HRB (1988) Evidence that luminal ER proteins are sorted from secreted proteins in a post-ER compartment. EMBO J 7:913–918PubMedGoogle Scholar
  86. Pelham HRB (1998) Getting through the Golgi complex. Trends Cell Biol 8:45–49PubMedCrossRefGoogle Scholar
  87. Pfeffer SR (2010) How the Golgi works: a cisternal progenitor model. Proc Natl Acad Sci USA 107:19614–19618PubMedCrossRefGoogle Scholar
  88. Pfeffer SR (2011) Entry at the trans-face of the Golgi. Cold Spring Harb Perspect Biol 3:a005272PubMedCrossRefGoogle Scholar
  89. 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 148:45–58PubMedCrossRefGoogle Scholar
  90. Popoff V, Adolf F, Brügger B, Wieland F (2011) COPI budding within the Golgi stack. Cold Spring Harb Perspect Biol 3:a005231PubMedCrossRefGoogle Scholar
  91. 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 3:789–803PubMedCrossRefGoogle Scholar
  92. Rabouille C, Klumperman J (2005) Opinion: the maturing role of COPI vesicles in intra-Golgi transport. Nat Rev Mol Cell Biol 6:812–817PubMedCrossRefGoogle Scholar
  93. 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 108:1617–1627PubMedGoogle Scholar
  94. 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 37–61CrossRefGoogle Scholar
  95. 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 139:1119–1129PubMedCrossRefGoogle Scholar
  96. Richardson BC, McDonold CM, Fromme JC (2012) The Sec7 Arf-GEF is recruited to the trans-Golgi network by positive feedback. Dev Cell 22:799–810PubMedCrossRefGoogle Scholar
  97. Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122:735–749PubMedCrossRefGoogle Scholar
  98. 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 201:1027–1036PubMedCrossRefGoogle Scholar
  99. Rockwell NC, Krysan DJ, Komiyama T, Fuller RS (2002) Precursor processing by Kex2/furin proteases. Chem Rev 102:4525–4548PubMedCrossRefGoogle Scholar
  100. Rothman JE (1981) The Golgi apparatus: two organelles in tandem. Science 213:1212–1219PubMedCrossRefGoogle Scholar
  101. Rothman JE, Wieland FT (1996) Protein sorting by transport vesicles. Science 272:227–234PubMedCrossRefGoogle Scholar
  102. Ruiz-May E, Kim SJ, Brandizzi F, Rose JK (2012) The secreted plant N-glycoproteome and associated secretory pathways. Front Plant Sci 3:117PubMedGoogle Scholar
  103. Schmidt WK, Moore HP (1995) Ionic milieu controls the compartment-specific activation of pro-opiomelanocortin processing in AtT-20 cells. Mol Biol Cell 6:1271–1285PubMedCrossRefGoogle Scholar
  104. Sharpe HJ, Stevens TJ, Munro S (2010) A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 142:158–169PubMedCrossRefGoogle Scholar
  105. Smith RD, Lupashin VV (2008) Role of the conserved oligomeric Golgi (COG) complex in protein glycosylation. Carbohydr Res 343:2024–2031PubMedCrossRefGoogle Scholar
  106. 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 140:1013–1021PubMedCrossRefGoogle Scholar
  107. Spang A (2012) The DSL1 complex: the smallest but not the least CATCHR. Traffic 13:908–913PubMedCrossRefGoogle Scholar
  108. 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 12:1035–1045PubMedCrossRefGoogle Scholar
  109. Staehelin LA, Kang BH (2008) Nanoscale architecture of endoplasmic reticulum export sites and of Golgi membranes as determined by electron tomography. Plant Physiol 147:1454–1468PubMedCrossRefGoogle Scholar
  110. Stalder D, Antonny B (2013) Arf GTPase regulation through cascade mechanisms and positive feedback loops. FEBS Lett 587:2028–2035PubMedCrossRefGoogle Scholar
  111. Stanley P (2011) Golgi glycosylation. Cold Spring Harb Perspect Biol 3:a005199PubMedCrossRefGoogle Scholar
  112. 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 13:727–744PubMedCrossRefGoogle Scholar
  113. 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 157:631–643PubMedCrossRefGoogle Scholar
  114. 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 6:1071–1081PubMedCrossRefGoogle Scholar
  115. 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–E677PubMedCrossRefGoogle Scholar
  116. Tu L, Tai WC, Chen L, Banfield DK (2008) Signal-mediated dynamic retention of glycosyltransferases in the Golgi. Science 321:404–407PubMedCrossRefGoogle Scholar
  117. Ungar D, Oka T, Krieger M, Hughson FM (2006) Retrograde transport on the COG railway. Trends Cell Biol 16:113–120PubMedCrossRefGoogle Scholar
  118. 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 2:283–294PubMedCrossRefGoogle Scholar
  119. 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 122:39–51PubMedCrossRefGoogle Scholar
  120. 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 22:1344–1357PubMedCrossRefGoogle Scholar
  121. 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 199:1057–1066CrossRefGoogle Scholar
  122. 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 31:3976–3990PubMedCrossRefGoogle Scholar
  123. Woollard AA, Moore I (2008) The functions of Rab GTPases in plant membrane traffic. Curr Opin Plant Biol 11:610–619PubMedCrossRefGoogle Scholar
  124. 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 8:377–383PubMedCrossRefGoogle Scholar
  125. 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 99:1070–1083PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Kasey J. Day
    • 1
  • L. Andrew Staehelin
    • 2
  • Benjamin S. Glick
    • 1
  1. 1.Department of Molecular Genetics and Cell BiologyThe University of ChicagoChicagoUSA
  2. 2.Molecular, Cellular, and Developmental BiologyUniversity of Colorado at BoulderBoulderUSA

Personalised recommendations