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Golgi tubules: their structure, formation and role in intra-Golgi transport

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Abstract

Tubules are common Golgi elements that can form extensive networks associated with the cis-, lateral and trans-Golgi sides, but despite this, they have almost been forgotten for decades. The molecular mechanisms involved in their formation, elongation and fission are only just beginning to be understood. However, the role of these membranes is not well understood. In the present review, we analyze the mechanisms that induce Golgi tubulation or, conversely, disrupt tubules in order to throw some lights on the nature of these elements. The putative role of these elements in the framework of current models for intra-Golgi transport is also discussed.

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References

  • Antonny B, Huber I, Paris S, Chabre M, Cassel D (1997) Activation of ADP-ribosylation factor 1 GTPase-activating protein by phosphatidylcholine-derived diacylglycerols. J Biol Chem 272:30848–30851

    Article  PubMed  CAS  Google Scholar 

  • Asp L, Kartberg F, Fernandez-Rodriguez J, Smedh M, Elsner M, Laporte F, Bárcena M, Jansen KA, Valentijn JA, Koster AJ, Bergeron JJ, Nilsson T (2009) Early stages of Golgi vesicle and tubule formation require diacylglycerol. Mol Biol Cell 20:780–790

    Article  PubMed  CAS  Google Scholar 

  • Bechler ME, Doody AM, Racoosin E, Lin L, Lee KH, Brown WJ (2010) The phospholipase complex PAFAH Ib regulates the functional organization of the Golgi complex. J Cell Biol 190:45–53

    Article  PubMed  CAS  Google Scholar 

  • Ben-Tekaya H, Kahn RA, Hauri HP (2010) ADP ribosylation factors 1 and 4 and group VIA phospholipase A2 regulate morphology and intraorganellar traffic in the endoplasmic reticulum-Golgi intermediate compartment. Mol Biol Cell 21:4130–4140

    Article  PubMed  CAS  Google Scholar 

  • Beznoussenko GV, Dolgikh VV, Seliverstova EV, Semenov PB, Tokarev YS, Trucco A, Micaroni M, Di Giandomenico D, Auinger P, Senderskiy IV, Skarlato SO, Snigirevskaya ES, Komissarchik YY, Pavelka M, De Matteis MA, Luini A, Sokolova YY, Mironov AA (2007) Analogs of the Golgi complex in microsporidia: structure and avesicular mechanisms of function. J Cell Sci 120:1288–1298

    Article  PubMed  CAS  Google Scholar 

  • Bigay J, Gounon P, Robineau S, Antonny B (2003) Lipid packing sensed by ArfGAP1 couples COPI coat disassembly to membrane bilayer curvature. Nature 426:563–566

    Article  PubMed  CAS  Google Scholar 

  • Bonfanti L, Mironov AA Jr, Martínez-Menárguez JA, Martella O, Fusella A, Baldassarre M, Buccione R, Geuze HJ, Mironov AA, Luini A (1998) Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation. Cell 95:993–1003

    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 

  • Brown WJ, Chambers K, Doody A (2003) Phospholipase A2 (PLA2) enzymes in membrane trafficking: mediators of membrane shape and function. Traffic 4:214–221

    Article  PubMed  CAS  Google Scholar 

  • Campadelli G, Brandimarti R, Di Lazzaro C, Ward PL, Roizman B, Torrisi MR (1993) Fragmentation and dispersal of Golgi proteins and redistribution of glycoproteins and glycolipids processed through the Golgi apparatus after infection with herpes simplex virus 1. Proc Natl Acad Sci USA 90:2798–2802

    Article  PubMed  CAS  Google Scholar 

  • Clermont Y, Rambourg A, Hermo L (1994) Connections between the various elements of the cis- and mid-compartments of the Golgi apparatus of early rat spermatids. Anat Rec 240:469–480

    Article  PubMed  CAS  Google Scholar 

  • Clermont Y, Rambourg A, Hermo L (1995) Trans-Golgi network (TGN) of different cell types: three-dimensional structural characteristics and variability. Anat Rec 242:289–301

    Article  PubMed  CAS  Google Scholar 

  • Cluett EB, Wood SA, Banta M, Brown WJ (1993) Tubulation of Golgi membranes in vivo and in vitro in the absence of brefeldin A. J Cell Biol 120:15–24

    Article  PubMed  CAS  Google Scholar 

  • Cooper MS, Cornell-Bell AH, Chernjavsky A, Dani JW, Smith SJ (1990) Tubulovesicular processes emerge from trans-Golgi cisternae, extend along microtubules, and interlink adjacent trans-golgi elements into a reticulum. Cell 61:135–145

    Article  PubMed  CAS  Google Scholar 

  • Corda D, Hidalgo Carcedo C, Bonazzi M, Luini A, Spanò S (2002) Molecular aspects of membrane fission in the secretory pathway. Cell Mol Life Sci 59:1819–1832

    Article  PubMed  CAS  Google Scholar 

  • Cosson P, Letourneur F (1994) Coatomer interaction with di-lysine endoplasmic reticulum retention motifs. Science 263:1629–1630

    Article  PubMed  CAS  Google Scholar 

  • Cruz-García D, Díaz-Ruiz A, Rabanal-Ruiz Y, Peinado JR, Gracia-Navarro F, Castaño JP, Montero-Hadjadje M, Tonon MC, Vaudry H, Anouar Y, Vázquez-Martínez R, Malagón MM (2012) The Golgi-associated long coiled-coil protein NECC1 participates in the control of the regulated secretory pathway in PC12 cells. Biochem J 443:387–396

    Article  PubMed  CAS  Google Scholar 

  • de Figueiredo P, Drecktrah D, Polizotto RS, Cole NB, Lippincott-Schwartz J, Brown WJ (2000) Phospholipase A2 antagonists inhibit constitutive retrograde membrane traffic to the endoplasmic reticulum. Traffic 1:504–511

    Article  PubMed  Google Scholar 

  • Diao A, Rahman D, Pappin DJC, Lucocq J, Lowe M (2003) The coiled-coil membrane protein golgin-84 is a novel rab effector required for Golgi ribbon formation. J Cell Biol 160:201–212

    Article  PubMed  CAS  Google Scholar 

  • Drecktrah D, Chambers K, Racoosin EL, Cluett EB, Gucwa A, Jackson B, Brown WJ (2003) Inhibition of a Golgi complex lysophospholipid acyltransferase induces membrane tubule formation and retrograde trafficking. Mol Biol Cell 14:3459–3469

    Article  PubMed  CAS  Google Scholar 

  • Fan JY, Roth J, Zuber C (2003) Ultrastructural analysis of transitional endoplasmic reticulum and pre-Golgi intermediates: a highway for cars and trucks. Histochem Cell Biol 120:455–463

    Article  PubMed  CAS  Google Scholar 

  • Fan JY, Roth J, Zuber C (2007) Expression of mutant Ins2C96Y results in enhanced tubule formation causing enlargement of pre-Golgi intermediates of CHO cells. Histochem Cell Biol 128:161–173

    Article  PubMed  CAS  Google Scholar 

  • Fan J, Hu Z, Zeng L, Lu W, Tang X, Zhang J, Li T (2008) Golgi apparatus and neurodegenerative diseases. Int J Dev Neuroscience 26:523–534

    Article  CAS  Google Scholar 

  • Feng Y, Yu S, Lasell TK, Jadhav AP, Macia E, Chardin P, Melancon P, Roth M, Mitchison T, Kirchhausen T (2003) Exo1: a new chemical inhibitor of the exocytic pathway. Proc Natl Acad Sci USA 100:6469–6474

    Article  PubMed  CAS  Google Scholar 

  • Fernandez-Ulibarri I, Vilella M, Lazaro-Dieguez F, Sarri E, Martinez SE, Jimenez N, Claro E, Merida I, Burger KN, Egea G (2007) Diacylglycerol is required for the formation of COPI vesicles in the Golgito-ER transport pathway. Mol Biol Cell 18:3250–3263

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Mata R, Szul T, Alvarez C, Sztul E (2003) ADP-ribosylation factor/COPI-dependent events at the endoplasmic reticulum—Golgi interface are regulated by the guanine nucleotide exchange factor GBF1. Mol Biol Cell 14:2250–2261

    Article  PubMed  CAS  Google Scholar 

  • Geuze HJ, Morré DJ (1991) Trans-Golgi reticulum. J Electron Microsc Tech 17:24–34

    Article  PubMed  CAS  Google Scholar 

  • Glick BS, Luini A (2011) Models for Golgi traffic: a critical assessment. Cold Spring Harb Perspect Biol 3(11):a005215

    Article  PubMed  CAS  Google Scholar 

  • Godi A, Di Campli A, Konstantakopoulos A, Di Tullio G, Alessi DR, Kular GS, Daniele T, Marra P, Lucocq JM, De Matteis MA (2004) FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P. Nat Cell Biol 6:393–404

    Article  PubMed  CAS  Google Scholar 

  • Goyal U, Blackstone C (2013) Untangling the web: mechanisms underlying ER network formation. Biochim Biophys Acta. doi:10.1016/j.bbamcr.2013.04.009

  • Grassé PP (1957) Ultrastructure, polarity and reproduction of Golgi apparatus. C R de Acad Sci 245:1278–1281

    Google Scholar 

  • Griffiths G (2000) Gut thoughts on the Golgi complex. Traffic 1:738–745

    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 

  • Gutierrez-Martinez E, Fernandez-Ulibarri I, Lazaro-Dieguez F, Johannes L, Pyne S, Sarri E, Egea G (2013) Lipid phosphate phosphatase 3 participates in transport carrier formation and protein trafficking in the early secretory pathway. J Cell Sci. doi:10.1242/jcs.117705

    PubMed  Google Scholar 

  • Ha KD, Clarke BA, Brown WJ (2012) Regulation of the Golgi complex by phospholipid remodeling enzymes. Biochim Biophys Acta 1821:1078–1088

    Article  PubMed  CAS  Google Scholar 

  • Haas AK, Yoshimura S, Stephens DJ, Preisinger C, Fuchs E, Barr FA (2007) Analysis of GTPase-activating proteins: Rab1 and Rab43 are key Rabs required to maintain a functional Golgi complex in human cells. J Cell Sci 120:2997–3010

    Article  PubMed  CAS  Google Scholar 

  • Heuer D, Rejman Lipinski A, Machuy N, Karlas A, Wehrens A, Siedler F, Brinkmann V, Meyer TF (2009) Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature 457:731–735

    Article  PubMed  CAS  Google Scholar 

  • Holappa K, Muñoz MT, Egea G, Kellokumpu S (2004) The AE2 anion exchanger is necessary for the structural integrity of the Golgi apparatus in mammalian cells. FEBS Lett 564:97–103

    Article  PubMed  CAS  Google Scholar 

  • Hsu VW, Shah N, Klausner RD (1992) A brefeldin A-like phenotype is induced by the overexpression of a human ERD-2-like protein, ELP-1. Cell 69:625–635

    Article  PubMed  CAS  Google Scholar 

  • Jackson CL, Casanova JE (2000) Turning on ARF: the Sec7 family of guanine-nucleotide-exchange factors. Trends Cell Biol 10:60–67

    Article  PubMed  CAS  Google Scholar 

  • Jin L, Pahuja KB, Wickliffe KE, Gorur A, Baumgärtel C, Schekman R, Rape M (2012) Ubiquitin-dependent regulation of COPII coat size and function. Nature 482:495–500

    Article  PubMed  CAS  Google Scholar 

  • Judson BL, Brown WJ (2009) Assembly of an intact Golgi complex requires phospholipase A2 (PLA2) activity, membrane tubules, and dynein-mediated microtubule transport. Biochem Biophys Res Commun 389:473–477

    Article  PubMed  CAS  Google Scholar 

  • Kim HS, Takahashi M, Matsuo K, Ono Y (2007) Recruitment of CG-NAP to the Golgi apparatus through interaction with dynein-dynactin complex. Gen Cell 12:421–434

    Article  CAS  Google Scholar 

  • Kirchhausen T (2000) Clathrin. Annu Rev Biochem 69:699–727

    Article  PubMed  CAS  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. doi:10.1101/cshperspect.a005181

  • Koegler E, Bonnon C, Waldmeier L, Mitrovic S, Halbeisen R, Hauri HP (2010) p28, a novel ERGIC/cis Golgi protein, required for Golgi ribbon formation. Traffic 11:70–89

    Article  PubMed  CAS  Google Scholar 

  • Kooijman EE, Chupin V, Fuller NL, Kozlov MM, de Kruijff B, Burger KN, Rand PR (2005) Spontaneous curvature of phosphatidic acid and lysophosphatidic acid. Biochemistry 44:2097–2102

    Article  PubMed  CAS  Google Scholar 

  • Krauss M, Jia JY, Roux A, Beck R, Wieland FT, De Camilli P, Haucke V (2008) Arf1-GTP-induced tubule formation suggests a function of Arf family proteins in curvature acquisition at sites of vesicle budding. J Biol Chem 283:27717–27723

    Article  PubMed  CAS  Google Scholar 

  • Kreis TE (1992) Regulation of vesicular and tubular membrane traffic of the Golgi complex by coat proteins. Curr Opin Cell Biol 4:609–615

    Article  PubMed  CAS  Google Scholar 

  • Kudlyk T, Willett R, Pokrovskaya ID, Lupashin V (2013) COG6 interacts with a subset of the Golgi SNAREs and is important for the Golgi complex integrity. Traffic 14:194–204

    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 

  • Ladinsky MS, Wu CC, McIntosh S, McIntosh JR, Howell KE (2002) Structure of the Golgi and distribution of reporter molecules at 20 degrees C reveals the complexity of the exit compartments. Mol Biol Cell 13:2810–2825

    Article  PubMed  CAS  Google Scholar 

  • Lee TH, Linstedt AD (1999) Osmotically induced cell volume changes alter anterograde and retrograde transport, Golgi structure, and COPI dissociation. Mol Biol Cell 10:1445–1462

    Article  PubMed  CAS  Google Scholar 

  • Letourneur F, Gaynor EC, Hennecke S, Démollière C, Duden R, Emr SD, Riezman H, Cosson P (1994) Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79:1199–11207

    Article  PubMed  CAS  Google Scholar 

  • Liljedahl M, Maeda Y, Colanzi A, Ayala I, Van Lint J, Malhotra V (2001) Protein kinase D regulates the fission of cell surface destined transport carriers from the trans-Golgi network. Cell 104:409–420

    Article  PubMed  CAS  Google Scholar 

  • Lippincott-Schwartz J, Donaldson JG, Schweizer A, Berger EG, Hauri HP, Yuan LC, Klausner RD (1990) Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell 60:821–836

    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 

  • Losev E, Reinke CA, Jellen J, Strongin DE, Bevis BJ, Glick BS (2006) Golgi maturation visualized in living yeast. Nature 441:1002–1006

    Article  PubMed  CAS  Google Scholar 

  • Lowe M, Kreis TE (1998) Regulation of membrane traffic in animal cells by COPI. Biochim Biophys Acta 1404:53–66

    Article  PubMed  CAS  Google Scholar 

  • Lucocq J (1992) Mimicking mitotic Golgi disassembly using okadaic acid. J Cell Sci 103:875–880

    PubMed  CAS  Google Scholar 

  • Mardones GA, Snyder CM, Howell KE (2006) Cis-Golgi matrix proteins move directly to endoplasmic reticulum exit sites by association with tubules. Mol Biol Cell 17:525–538

    Article  PubMed  CAS  Google Scholar 

  • Marra P, Salvatore L, Mironov A Jr, Di Campli A, Di Tullio G, Trucco A, Beznoussenko G, Mironov A, De Matteis MA (2007) The biogenesis of the Golgi ribbon: the roles of membrane input from the ER and of GM130. Mol Biol Cell 18:1595–1608

    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 

  • Martinez-Alonso E, Ballesta J, Martinez-Menarguez JA (2007) Low-temperature- induced Golgi tubules are transient membranes enriched in molecules regulating intra-Golgi transport. Traffic 8:359–368

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Alonso E, Egea G, Ballesta J, Martínez-Menárguez JA (2005) Structure and dynamics of the Golgi complex at 15 degrees C: low temperature induces the formation of Golgi-derived tubules. Traffic 6:32–44

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Menárguez JA (2013) Intra-golgi transport: roles for vesicles, tubules, and cisternae. ISRN Cell Biol, vol 2013, Article ID 126731. doi:10.1155/2013/126731

  • Martinez-Menarguez JA, Geuze HJ, Slot JW, Klumperman J (1999) Vesicular tubular clusters between the ER and Golgi mediate concentration of soluble secretory proteins by exclusion from COPI-coated vesicles. Cell 98:81–90

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Menárguez JA, Prekeris R, Oorschot VM, 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 155:1213–1214

    Article  PubMed  Google Scholar 

  • Matsuura-Tokita K, Takeuchi M, Ichihara A, Mikuriya K, Nakano A (2006) Live imaging of yeast Golgi cisternal maturation. Nature 441:1007–1010

    Article  PubMed  CAS  Google Scholar 

  • Mironov AA, Beznoussenko GV (2011) Molecular mechanisms responsible for formation of Golgi ribbon. Histol Histopathol 26:117–133

    PubMed  CAS  Google Scholar 

  • Mironov AA, Beznoussenko GV (2012) The kiss-and-run model of intra-Golgi transport. Int J Mol Sci 13:6800–6819

    Article  PubMed  CAS  Google Scholar 

  • Mironov AA, Colanzi A, Polishchuk RS, Beznoussenko GV, Mironov AA Jr, Fusella A, Di Tullio G, Silletta MG, Corda D, De Matteis MA, Luini A (2004) Dicumarol, an inhibitor of ADP-ribosylation of CtBP3/BARS, fragments golgi non-compact tubular zones and inhibits intra-golgi transport. Eur J Cell Biol 83:263–279

    Article  PubMed  CAS  Google Scholar 

  • Mollenhauer HH, Morré DJ (1998) The tubular network of the Golgi apparatus. Histochem Cell Biol 109:533–543

    Article  PubMed  CAS  Google Scholar 

  • Mounier J, Boncompain G, Senerovic L, Lagache T, Chrétien F, Perez F, Kolbe M, Olivo-Marin JC, Sansonetti PJ, Sauvonnet N (2012) Shigella effector IpaB-induced cholesterol relocation disrupts the Golgi complex and recycling network to inhibit host cell secretion. Cell Host Microbe 12:381–389

    Article  PubMed  CAS  Google Scholar 

  • Muppirala M, Gupta V, Swarup G (2011) Syntaxin 17 cycles between the ER and ERGIC and is required to maintain the architecture of ERGIC and Golgi. Biol Cell 103:333–350

    Article  PubMed  CAS  Google Scholar 

  • Naydenov NG, Harris G, Brown B, Schaefer KL, Das SK, Fisher PB, Ivanov A (2012) Loss of soluble N-ethylmaleimide-sensitive factor attachment protein α (αSNAP) induces epithelial cell apoptosis via down-regulation of Bcl-2 expression and disruption of the Golgi. J Biol Chem 287:5928–5941

    Article  PubMed  CAS  Google Scholar 

  • Numata Y, Morimura T, Nakamura S, Hirano E, Kure S, Goto YI, Inoue K (2013) Depletion of molecular chaperones from the endoplasmic reticulum and fragmentation of the Golgi apparatus associated with pathogenesis in Pelizaeus-Merzbacher disease. J Biol Chem 288:7451–7466

    Article  PubMed  CAS  Google Scholar 

  • Orci L, Glick BS, Rothman JE (1986) A new type of coated vesicular carrier that appears not to contain clathrin: its possible role in protein transport within the Golgi stack. Cell 46:171–184

    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 

  • Palade G (1975) Intracellular aspects of the process of protein synthesis. Science 189:347–358

    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 HR, Rothman JE (2000) The debate about transport in the Golgi-two sides of the same coin? Cell 102:713–719

    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 

  • Polishchuk RS, Capestrano M, Polishchuk EV (2009) Shaping tubular carriers for intracellular membrane transport. FEBS Lett 583:3847–3856

    Article  PubMed  CAS  Google Scholar 

  • Polizotto RS, de Figueiredo P, Brown WL (1999) Stimulation of Golgi membrane tubulation and retrograde trafficking to the ER by phospholipase A(2) activating protein (PLAP) peptide. J Cell Biochem 74:670–683

    Article  PubMed  CAS  Google Scholar 

  • Presley JF, Cole NB, Schroer TA, Hirschberg K, Zaal KJ, Lippincott-Schwartz J (1997) ER-to-Golgi transport visualized in living cells. Nature 389:81–85

    Article  PubMed  CAS  Google Scholar 

  • Puthenveedu MA, Linstedt AD (2001) Evidence that Golgi structure depends on a p115 activity that is independent of the vesicle tether components giantin and GM130. J Cell Biol 155:227–238

    Article  PubMed  CAS  Google Scholar 

  • Puthenveedu MA, Bachert C, Puri S, Lanni F, Linstedt AD (2006) GM130 and GRASP65-dependent lateral cisternal fusion allows uniform Golgi-enzyme distribution. Nat Cell Biol 8:238–248

    Article  PubMed  CAS  Google Scholar 

  • Quiner CA, Jackson WT (2010) Fragmentation of the Golgi apparatus provides replication membranes for human rhinovirus 1A. Virology 407:185–195

    Article  PubMed  CAS  Google Scholar 

  • Rabouille C, Kondylis V (2007) Golgi ribbon unlinking: an organelle-based G2/M checkpoint. Cell Cycle 6:2723–2729

    Article  PubMed  CAS  Google Scholar 

  • Ramabhadran V, Korobova F, Rahme GJ, Higgs HN (2011) Splice variant-specific cellular function of the formin INF2 in maintenance of Golgi architecture. Mol Biol Cell 22:4822–4833

    Article  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, Switzerland, pp 37–61

    Chapter  Google Scholar 

  • Reddy JV, Burguete AS, Sridevi K, Ganley IG, Nottingham RM, Pfeffer SR (2006) A functional role for the GCC185 golgin in mannose 6-phosphate receptor recycling. Mol Biol Cell 17:4353–4363

    Article  PubMed  CAS  Google Scholar 

  • Rendón WO, Martínez-Alonso E, Tomás M, Martínez-Martínez N, Martínez-Menárguez JA (2013) Golgi fragmentation is Rab and SNARE dependent in cellular models of Parkinson’s disease. Histochem Cell Biol 139:671–684

    Article  PubMed  CAS  Google Scholar 

  • Ríos RM, Sanchís A, Tassin AM, Fedriani C, Bornens M (2004) GMAP-210 recruits γ-tubulin complexes to cis—Golgi membranes and is required for Golgi Gibbon formation. Cell 118:323–335

    Article  PubMed  Google Scholar 

  • Rohde J, Emschermann F, Knittler MR, Rziha HJ (2012) Orf virus interferes with MHC class I surface expression by targeting vesicular transport and Golgi. BMC Vet Res 8:114

    Article  PubMed  CAS  Google Scholar 

  • Romano JD, Sonda S, Bergbower E, Smith ME, Coppens I (2013) Toxoplasma gondii salvages sphingolipids from the host Golgi through the rerouting of selected Rab vesicles to the parasitophorous vacuole. Mol Biol Cell 24:1974–1995

    Google Scholar 

  • Roth J, Taatjes DJ, Lucocq JM, Weinstein J, Paulson JC (1985) Demonstration of an extensive trans-tubular network continuous with the Golgi apparatus stack that may function in glycosylation. Cell 43:287–295

    Article  PubMed  CAS  Google Scholar 

  • Roux A, Cappello G, Cartaud J, Prost J, Goud B, Bassereau P (2002) A minimal system allowing tubulation with molecular motors pulling on giant liposomes. Proc Natl Acad Sci USA 99:5394–5539

    Article  PubMed  CAS  Google Scholar 

  • Saito K, Chen M, Bard F, Chen S, Zhou H, Woodley D, Polischuk R, Schekman R, Malhotra V (2009) TANGO1 facilitates cargo loading at endoplasmic reticulum exit sites. Cell 136:891–902

    Article  PubMed  CAS  Google Scholar 

  • Saito K, Yamashiro K, Ichikawa Y, Erlmann P, Kontani K, Malhotra V, Katada T (2011) cTAGE5 mediates collagen secretion through interaction with TANGO1 at endoplasmic reticulum exit sites. Mol Biol Cell 22:2301–2308

    Article  PubMed  CAS  Google Scholar 

  • Saka HA, Valdivia RH (2010) Acquisition of nutrients by Chlamydiae: unique challenges of living in an intracellular compartment. Curr Opin Microbiol 13:4–10

    Article  PubMed  CAS  Google Scholar 

  • Salcedo-Sicilia L, Granell S, Jovic M, Sicart A, Mato E, Johannes L, Balla T, Egea G (2013) βIII spectrin regulates the structural integrity and the secretory protein transport of the Golgi complex. J Biol Chem 288:2157–2166

    Article  PubMed  CAS  Google Scholar 

  • San Pietro E, Capestrano M, Polishchuk EV, DiPentima A, Trucco A, Zizza P, Mariggiò S, Pulvirenti T, Sallese M, Tete S, Mironov AA, Leslie CC, Corda D, Luini A, Polishchuk RS (2009) Group IV phospholipase A(2)alpha controls the formation of inter-cisternal continuities involved in intra-Golgi transport. PLoS Biol 7:e1000194

    Article  PubMed  CAS  Google Scholar 

  • Schecterson LC, Hudson MP, Ko M, Philippidou P, Akmentin W, Wiley J, Rosenblum E, Chao MV, Halegoua S, Bothwell M (2010) Trk activation in the secretory pathway promotes Golgi fragmentation. Mol Cell Neurosci 43:403–413

    Article  PubMed  CAS  Google Scholar 

  • Schmidt JA, Kalkofen DN, Donovan KW, Brown WJ (2010) A role for phospholipase A2 activity in membrane tubule formation and TGN trafficking. Traffic 11:1530–1536

    Article  PubMed  CAS  Google Scholar 

  • Sciaky N, Presley J, Smith C, Zaal KJ, Cole N, Moreira JE, Terasaki M, Siggia E, Lippincott-Schwartz J (1997) Golgi tubule traffic and the effects of brefeldin A visualized in living cells. J Cell Biol 139:1137–1155

    Article  PubMed  CAS  Google Scholar 

  • Seifert W, Kühnisch J, Maritzen T, Horn D, Haucke V, Hennies HC (2011) Cohen syndrome-associated protein, COH1, is a novel, giant Golgi matrix protein required for Golgi integrity. J Biol Chem 286:37665–37675

    Article  PubMed  CAS  Google Scholar 

  • Serafini T, Orci L, Amherdt M, Brunner M, Kahn RA, Rothman JE (1991) ADP-ribosylation factor is a subunit of the coat of Golgi-derived COP-coated vesicles: a novel role for a GTP-binding protein. Cell 67:239–253

    Article  PubMed  CAS  Google Scholar 

  • Sesso A, de Faria FP, Iwamura ES, Corrêa H (1994) A three-dimensional reconstruction study of the rough ER-Golgi interface in serial thin sections of the pancreatic acinar cell of the rat. J Cell Sci 107:517–528

    PubMed  Google Scholar 

  • Simpson JC, Nilsson T, Pepperkok R (2006) Biogenesis of tubular ER-to-Golgi transport intermediates. Mol Biol Cell 17:723–737

    Article  PubMed  CAS  Google Scholar 

  • Stagg SM, LaPointe P, Razvi A, Gürkan C, Potter CS, Carragher B, Balch WE (2008) Structural basis for cargo regulation of COPII coat assembly. Cell 134:474–484

    Article  PubMed  CAS  Google Scholar 

  • Stauber T, Simpson JC, Pepperkok R, Vernos I (2006) A role for kinesin-2 in COPI-dependent recycling between the ER and the Golgi complex. Curr Biol 16:2245–2251

    Article  PubMed  CAS  Google Scholar 

  • Stieber A, Chen Y, Wei S, Mourelatos Z, Gonatas J, Okamoto K, Gonatas NK (1998) The fragmented neuronal Golgi apparatus in amyotrophic lateral sclerosis includes the trans-Golgi-network: functional implications. Acta Neuropathol 5:245–253

    Article  Google Scholar 

  • Storrie B, White J, Röttger S, Stelzer EH, Suganuma T, Nilsson T (1998) Recycling of golgi-resident glycosyltransferases through the ER reveals a novel pathway and provides an explanation for nocodazole-induced Golgi scattering. J Cell Biol 143:1505–1521

    Article  PubMed  CAS  Google Scholar 

  • Suga K, Hattori H, Saito A, Akagawa K (2005) RNA interference-mediated silencing of the syntaxin 5 gene induces Golgi fragmentation but capable of transporting vesicles. FEBS Lett 579:4226–4234

    Article  PubMed  CAS  Google Scholar 

  • Szul T, Sztul E (2011) COPII and COPI traffic at the ER-Golgi interface. Physiology 26:348–364

    Article  PubMed  CAS  Google Scholar 

  • Szul T, Grabski R, Lyons S, Morohashi Y, Shestopal S, Lowe M, Sztul E (2007) Dissecting the role of the ARF guanine nucleotide exchange factor GBF1 in Golgi biogenesis and protein trafficking. J Cell Sci 120:3929–3940

    Article  PubMed  CAS  Google Scholar 

  • Taatjes DJ, Roth J (1986) The trans-tubular network of the hepatocyte Golgi apparatus is part of the secretory pathway. Eur J Cell Biol 42:344–350

    Google Scholar 

  • Tanaka K, Fukudome H (1991) Three-dimensional organization of the Golgi complex observed by scanning electron microscopy. J Electron Microsc Tech 17:15–23

    Article  PubMed  CAS  Google Scholar 

  • Tomás M, Martínez-Alonso E, Ballesta J, Martínez-Menárguez JA (2010) Regulation of ER-Golgi intermediate compartment tubulation and mobility by COPI coats, motor proteins and microtubules. Traffic 11:616–625

    Article  PubMed  CAS  Google Scholar 

  • Tomás M, Marín MP, Martínez-Alonso E, Esteban-Pretel G, Díaz-Ruiz A, Vázquez-Martínez R, Malagón MM, Renau-Piqueras J, Martínez-Menárguez JA (2012) Alcohol induces Golgi fragmentation in differentiated PC12 cells by deregulating Rab1-dependent ER-to-Golgi transport. Histochem Cell Biol 138:489–501

    Article  PubMed  CAS  Google Scholar 

  • Trucco A, Polishchuk RS, Martella O, Di Pentima A, Fusella A, Di Giandomenico D, San Pietro E, 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 

  • Venditti R, Scanu T, Santoro M, Di Tullio G, Spaar A, Gaibisso R, Beznoussenko GV, Mironov AA, Mironov A Jr, Zelante L, Piemontese MR, Notarangelo A, Malhotra V, Vertel BM, Wilson C, De Matteis MA (2012) Sedlin controls the ER export of procollagen by regulating the Sar1 cycle. Science 337:1668–1672

    Article  PubMed  CAS  Google Scholar 

  • Vivero-Salmerón G, Ballesta J, Martínez-Menárguez JA (2008) Heterotypic tubular connections at the endoplasmic reticulum-Golgi complex interface. Histochem Cell Biol 130:709–717

    Article  PubMed  CAS  Google Scholar 

  • Volchuk A, Amherdt M, Ravazzola M, Brügger B, Rivera VM, Clackson T, Perrelet A, Söllner TH, Rothman JE, Orci L (2000) Megavesicles implicated in the rapid transport of intracisternal aggregates across the Golgi stack. Cell 102:335–348

    Article  PubMed  CAS  Google Scholar 

  • Volpicelli-Daley LA, Li Y, Zhang CJ, Kahn RA (2005) Isoform-selective effects of the depletion of ADP-ribosylation factors 1–5 on membrane traffic. Mol Biol Cell 16:4495–4508

    Article  PubMed  CAS  Google Scholar 

  • Waters MG, Serafini T, Rothman JE (1991) ‘Coatomer’: a cytosolic protein complex containing subunits of non-clathrin-coated Golgi transport vesicles. Nature 349:248–251

    Article  PubMed  CAS  Google Scholar 

  • Wehland J, Henkart M, Klausner R, Sandoval IV (1983) Role of microtubules in the distribution of the Golgi apparatus: effect of taxol and microinjected anti-alpha-tubulin antibodies. Proc Natl Acad Sci USA 80:4286–4290

    Article  PubMed  CAS  Google Scholar 

  • Wei JH, Seemann J (2010) Unraveling the Golgi ribbon. Traffic 11:1391–1400

    Article  PubMed  Google Scholar 

  • Weidman P, Roth R, Heuser J (1993) Golgi membrane dynamics imaged by freeze-etch electron microscopy: views of different membrane coatings involved in tubulation versus vesiculation. Cell 75:123–133

    PubMed  CAS  Google Scholar 

  • White J, Johannes L, Mallard F, Girod A, Grill S, Reinsch S, Keller P, Tzschaschel B, Echard A, Goud B, Stelzer EH (1999) Rab6 coordinates a novel Golgi to ER retrograde transport pathway in live cells. J Cell Biol 147:743–760

    Article  PubMed  CAS  Google Scholar 

  • Wilson BS, Nuoffer C, Meinkoth JL, McCaffery M, Feramisco JR, Balch WE, Farquhar MG (1994) A Rab1 mutant affecting guanine nucleotide exchange promotes disassembly of the Golgi apparatus. J Cell Biol 125:557–571

    Article  PubMed  CAS  Google Scholar 

  • Yang JS, Gad H, Lee SY, Mironov A, Zhang L, Beznoussenko GV, Valente C, Turacchio G, Bonsra AN, Du G, Baldanzi G, Graziani A, Bourgoin S, Frohman MA, Luini A, Hsu VW (2008) A role for phosphatidic acid in COPI vesicle fission yields insights into Golgi maintenance. Nat Cell Biol 10:1146–1153

    Article  PubMed  CAS  Google Scholar 

  • Yang JS, Valente C, Polishchuk RS, Turacchio G, Layre E, Moody DB, Leslie CC, Gelb MH, Brown WJ, Corda D, Luini A, Hsu VW (2011) COPI acts in both vesicular and tubular transport. Nat Cell Biol 13:996–1003

    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 

  • Zimmerberg J, Kozlov MM (2006) How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7:9–19

    Article  PubMed  CAS  Google Scholar 

  • Zolov SN, Lupashin VV (2005) Cog3p depletion blocks vesicle-mediated Golgi retrograde trafficking in HeLa cells. J Cell Biol 168:747–759

    Article  PubMed  CAS  Google Scholar 

  • Zuber C, Fan JY, Guhl B, Roth J (2004) Misfolded proinsulin accumulates in expanded pre-Golgi intermediates and endoplasmic reticulum subdomains in pancreatic beta cells of Akita mice. FASEB J 18:917–919

    PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr Vivero-Salmerón for some of the images of Fig. 1. This work has been supported by grants from the Ministerio de Ciencia e Innovación (Spain) Consolider COAT CSD2009-00016) and Fundación Séneca de la Comunidad Autónoma de la Región de Murcia (04542/GERM/06) to JAM-M.

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Authors and Affiliations

  1. Department of Cell Biology and Histology, Medical School, University of Murcia, 30100, Murcia, Spain

    Emma Martínez-Alonso & José A. Martínez-Menárguez

  2. Department of Human Anatomy and Embryology, Medical School, Valencia University, 46010, Valencia, Spain

    Mónica Tomás

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  1. Emma Martínez-Alonso
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  2. Mónica Tomás
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  3. José A. Martínez-Menárguez
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Correspondence to José A. Martínez-Menárguez.

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Emma Martínez-Alonso and Mónica Tomás contributed equally to this publication.

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Martínez-Alonso, E., Tomás, M. & Martínez-Menárguez, J.A. Golgi tubules: their structure, formation and role in intra-Golgi transport. Histochem Cell Biol 140, 327–339 (2013). https://doi.org/10.1007/s00418-013-1114-9

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