Conserved Oligomeric Golgi and Neuronal Vesicular Trafficking

  • Leslie K. Climer
  • Rachel D. Hendrix
  • Vladimir V. Lupashin
Part of the Handbook of Experimental Pharmacology book series (HEP, volume 245)


The conserved oligomeric Golgi (COG) complex is an evolutionary conserved multi-subunit vesicle tethering complex essential for the majority of Golgi apparatus functions: protein and lipid glycosylation and protein sorting. COG is present in neuronal cells, but the repertoire of COG function in different Golgi-like compartments is an enigma. Defects in COG subunits cause alteration of Golgi morphology, protein trafficking, and glycosylation resulting in human congenital disorders of glycosylation (CDG) type II. In this review we summarize and critically analyze recent advances in the function of Golgi and Golgi-like compartments in neuronal cells and functions and dysfunctions of the COG complex and its partner proteins.


COG Conserved oligomeric Golgi Glycosylation Golgi outpost Golgi satellite 



We are very grateful to Tanner E. Brackett for the creation and design of Fig. 1. This work was supported by the NIH grants GM083144 and U54 GM105814 and by the Pilot grant from the Arkansas Biosciences Institute.


  1. Abdul Rahman S et al (2014) Filter-aided N-glycan separation (FANGS): a convenient sample preparation method for mass spectrometric N-glycan profiling. J Proteome Res 13:1167–1176PubMedPubMedCentralCrossRefGoogle Scholar
  2. Arabidopsis Interactome Mapping Consortium (2011) Evidence for network evolution in an Arabidopsis interactome map. Science 333:601–607PubMedCentralCrossRefGoogle Scholar
  3. Arriagada C, Bustamante M, Atwater I, Rojas E, Caviedes R, Caviedes P (2010) Apoptosis is directly related to intracellular amyloid accumulation in a cell line derived from the cerebral cortex of a trisomy 16 mouse, an animal model of Down syndrome. Neurosci Lett 470:81–85PubMedCrossRefGoogle Scholar
  4. Bailey Blackburn J, Pokrovskaya I, Fisher P, Ungar D, Lupashin VV (2016) COG complex complexities: detailed characterization of a complete set of HEK293T cells lacking individual COG subunits. Front Cell Dev Biol 4:23PubMedPubMedCentralCrossRefGoogle Scholar
  5. Baker RW, Jeffrey PD, Zick M, Phillips BP, Wickner WT, Hughson FM (2015) A direct role for the Sec1/Munc18-family protein Vps33 as a template for SNARE assembly. Science 349:1111–1114PubMedPubMedCentralCrossRefGoogle Scholar
  6. Beznoussenko GV et al (2014) Transport of soluble proteins through the Golgi occurs by diffusion via continuities across cisternae. Elife 3.
  7. Blackburn JB, Lupashin VV (2016) Creating knockouts of conserved oligomeric Golgi complex subunits using CRISPR-mediated gene editing paired with a selection strategy based on glycosylation defects associated with impaired COG complex function. Methods Mol Biol 1496:145–161PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116:153–166PubMedCrossRefGoogle Scholar
  9. Brockhausen I, Schachter H, Stanley P (2009) O-GalNAc glycans. In: Varki A et al (eds) Essentials of glycobiology, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  10. Bunge MB (1973) Fine structure of nerve fibers and growth cones of isolated sympathetic neurons in culture. J Cell Biol 56:713–735PubMedPubMedCentralCrossRefGoogle Scholar
  11. Cajigas IJ, Tushev G, Will TJ, tom Dieck S, Fuerst N, Schuman EM (2012) The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron 74:453–466PubMedPubMedCentralCrossRefGoogle Scholar
  12. Castellano B, Gonzalez B, Palacios G (1989) Cytochemical demonstration of TPPase in myelinated fibers in the central and peripheral nervous system of the rat. Brain Res 492:203–210PubMedCrossRefGoogle Scholar
  13. Cataldo AM, Peterhoff CM, Troncoso JC, Gomez-Isla T, Hyman BT, Nixon RA (2000) Endocytic pathway abnormalities precede amyloid beta deposition in sporadic Alzheimer’s disease and Down syndrome: differential effects of APOE genotype and presenilin mutations. Am J Pathol 157:277–286PubMedPubMedCentralCrossRefGoogle Scholar
  14. Cavanaugh LF, Chen X, Richardson BC, Ungar D, Pelczer I, Rizo J, Hughson FM (2007) Structural analysis of conserved oligomeric Golgi complex subunit 2. J Biol Chem 282:23418–23426PubMedCrossRefGoogle Scholar
  15. Chatterton JE, Hirsch D, Schwartz JJ, Bickel PE, Rosenberg RD, Lodish HF, Krieger M (1999) Expression cloning of LDLB, a gene essential for normal Golgi function and assembly of the ldlCp complex. Proc Natl Acad Sci U S A 96:915–920PubMedPubMedCentralCrossRefGoogle Scholar
  16. Cheung PY, Pfeffer SR (2016) Transport vesicle tethering at the trans Golgi network: coiled coil proteins in action. Front Cell Dev Biol 4:18PubMedPubMedCentralCrossRefGoogle Scholar
  17. Chou HT, Dukovski D, Chambers MG, Reinisch KM, Walz T (2016) CATCHR, HOPS and CORVET tethering complexes share a similar architecture. Nat Struct Mol Biol 23:761–763PubMedPubMedCentralCrossRefGoogle Scholar
  18. Choudhury A, Sharma DK, Marks DL, Pagano RE (2004) Elevated endosomal cholesterol levels in Niemann-Pick cells inhibit rab4 and perturb membrane recycling. Mol Biol Cell 15:4500–4511PubMedPubMedCentralCrossRefGoogle Scholar
  19. Climer LK, Dobretsov M, Lupashin V (2015) Defects in the COG complex and COG-related trafficking regulators affect neuronal Golgi function. Front Neurosci 9:405PubMedPubMedCentralCrossRefGoogle Scholar
  20. Comstra HS et al (2017) The interactome of the copper transporter ATP7A belongs to a network of neurodevelopmental and neurodegeneration factors. Elife 6.
  21. Cooper AA et al (2006) Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson’s models. Science 313:324–328PubMedPubMedCentralCrossRefGoogle Scholar
  22. Corbett MA et al (2011) A mutation in the Golgi Qb-SNARE gene GOSR2 causes progressive myoclonus epilepsy with early ataxia. Am J Hum Genet 88:657–663PubMedPubMedCentralCrossRefGoogle Scholar
  23. Cottam NP, Ungar D (2012) Retrograde vesicle transport in the Golgi. Protoplasma 249:943–955PubMedCrossRefGoogle Scholar
  24. D’Arcangelo JG, Stahmer KR, Miller EA (2013) Vesicle-mediated export from the ER: COPII coat function and regulation. Biochim Biophys Acta 1833:2464–2472PubMedPubMedCentralCrossRefGoogle Scholar
  25. Dodonova SO et al (2015) Vesicular Transport. A structure of the COPI coat and the role of coat proteins in membrane vesicle assembly. Science 349:195–198PubMedCrossRefGoogle Scholar
  26. Dugan JM, deWit C, McConlogue L, Maltese WA (1995) The Ras-related GTP-binding protein, Rab1B, regulates early steps in exocytic transport and processing of beta-amyloid precursor protein. J Biol Chem 270:10982–10989PubMedCrossRefGoogle Scholar
  27. Fotso P, Koryakina Y, Pavliv O, Tsiomenko AB, Lupashin VV (2005) Cog1p plays a central role in the organization of the yeast conserved oligomeric Golgi complex. J Biol Chem 280:27613–27623PubMedCrossRefGoogle Scholar
  28. Foulquier F et al (2006) Conserved oligomeric Golgi complex subunit 1 deficiency reveals a previously uncharacterized congenital disorder of glycosylation type II. Proc Natl Acad Sci U S A 103:3764–3769PubMedPubMedCentralCrossRefGoogle Scholar
  29. Foulquier F et al (2007) A new inborn error of glycosylation due to a Cog8 deficiency reveals a critical role for the Cog1-Cog8 interaction in COG complex formation. Hum Mol Genet 16:717–730PubMedCrossRefGoogle Scholar
  30. Freeze HH, Chong JX, Bamshad MJ, Ng BG (2014) Solving glycosylation disorders: fundamental approaches reveal complicated pathways. Am J Hum Genet 94:161–175PubMedPubMedCentralCrossRefGoogle Scholar
  31. Fuchs-Telem D et al (2011) CEDNIK syndrome results from loss-of-function mutations in SNAP29. Br J Dermatol 164:610–616PubMedGoogle Scholar
  32. Fukuda M, Kanno E, Ishibashi K, Itoh T (2008) Large scale screening for novel rab effectors reveals unexpected broad Rab binding specificity. Mol Cell Proteomics 7:1031–1042PubMedCrossRefGoogle Scholar
  33. Fung CW et al (2012) COG5-CDG with a mild neurohepatic presentation. JIMD Rep 3:67–70PubMedCrossRefGoogle Scholar
  34. Gillingham AK, Munro S (2016) Finding the Golgi: Golgin coiled-coil proteins show the way. Trends Cell Biol 26:399–408PubMedCrossRefGoogle Scholar
  35. Ginsberg SD et al (2010) Microarray analysis of hippocampal CA1 neurons implicates early endosomal dysfunction during Alzheimer’s disease progression. Biol Psychiatry 68:885–893PubMedPubMedCentralCrossRefGoogle Scholar
  36. Giot L et al (2003) A protein interaction map of Drosophila melanogaster. Science 302:1727–1736PubMedCrossRefGoogle Scholar
  37. Gitler AD et al (2008) The Parkinson’s disease protein alpha-synuclein disrupts cellular Rab homeostasis. Proc Natl Acad Sci U S A 105:145–150PubMedCrossRefGoogle Scholar
  38. Giuditta A, Hunt T, Santella L (1986) Rapid important paper: messenger RNA in squid axoplasm. Neurochem Int 8:435–442PubMedCrossRefGoogle Scholar
  39. Glick BS, Luini A (2011) Models for Golgi traffic: a critical assessment. Cold Spring Harb Perspect Biol 3:a005215PubMedPubMedCentralCrossRefGoogle Scholar
  40. Glick BS, Nakano A (2009) Membrane traffic within the Golgi apparatus. Annu Rev Cell Dev Biol 25:113–132PubMedPubMedCentralCrossRefGoogle Scholar
  41. 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
  42. Gokhale A et al (2012) Quantitative proteomic and genetic analyses of the schizophrenia susceptibility factor dysbindin identify novel roles of the biogenesis of lysosome-related organelles complex 1. J Neurosci 32:3697–3711PubMedPubMedCentralCrossRefGoogle Scholar
  43. Goldfischer S (1982) The internal reticular apparatus of Camillo Golgi: a complex, heterogeneous organelle, enriched in acid, neutral, and alkaline phosphatases, and involved in glycosylation, secretion, membrane flow, lysosome formation, and intracellular digestion. J Histochem Cytochem 30:717–733PubMedCrossRefGoogle Scholar
  44. Golgi C (1989) On the structure of nerve cells. J Microsc 155:3–7PubMedCrossRefGoogle Scholar
  45. Gonatas NK, Stieber A, Gonatas JO (2006) Fragmentation of the Golgi apparatus in neurodegenerative diseases and cell death. J Neurol Sci 246:21–30PubMedCrossRefGoogle Scholar
  46. Griffith DL, Bondareff W (1973) Localization of thiamine pyrophosphatase in synaptic vesicles. Am J Anat 136:549–556PubMedCrossRefGoogle Scholar
  47. Ha JY et al (2014) Cog5-Cog7 crystal structure reveals interactions essential for the function of a multisubunit tethering complex. Proc Natl Acad Sci U S A 111:15762–15767PubMedPubMedCentralCrossRefGoogle Scholar
  48. Ha JY, Chou HT, Ungar D, Yip CK, Walz T, Hughson FM (2016) Molecular architecture of the complete COG tethering complex. Nat Struct Mol Biol 23:758–760PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hanus C, Ehlers MD (2016) Specialization of biosynthetic membrane trafficking for neuronal form and function. Curr Opin Neurobiol 39:8–16PubMedCrossRefGoogle Scholar
  50. Hanus C et al (2016) Unconventional secretory processing diversifies neuronal ion channel properties. Elife 5.
  51. Hasegawa H, Zinsser S, Rhee Y, Vik-Mo EO, Davanger S, Hay JC (2003) Mammalian ykt6 is a neuronal SNARE targeted to a specialized compartment by its profilin-like amino terminal domain. Mol Biol Cell 14:698–720PubMedPubMedCentralCrossRefGoogle Scholar
  52. Hasegawa H, Yang Z, Oltedal L, Davanger S, Hay JC (2004) Intramolecular protein-protein and protein-lipid interactions control the conformation and subcellular targeting of neuronal Ykt6. J Cell Sci 117:4495–4508PubMedCrossRefGoogle Scholar
  53. Horton AC, Ehlers MD (2003) Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging. J Neurosci 23:6188–6199PubMedCrossRefGoogle Scholar
  54. Hutagalung AH, Novick PJ (2011) Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91:119–149PubMedPubMedCentralCrossRefGoogle Scholar
  55. Huybrechts S et al (2012) Deficiency of subunit 6 of the conserved oligomeric golgi complex (COG6-CDG): second patient, different phenotype. JIMD Rep 4:103–108PubMedCrossRefGoogle Scholar
  56. Jeyifous O et al (2009) SAP97 and CASK mediate sorting of NMDA receptors through a previously unknown secretory pathway. Nat Neurosci 12:1011–1019PubMedPubMedCentralCrossRefGoogle Scholar
  57. Kim DW, Sacher M, Scarpa A, Quinn AM, Ferro-Novick S (1999) High-copy suppressor analysis reveals a physical interaction between Sec34p and Sec35p, a protein implicated in vesicle docking. Mol Biol Cell 10:3317–3329PubMedPubMedCentralCrossRefGoogle Scholar
  58. Kingsley DM, Krieger M (1984) Receptor-mediated endocytosis of low density lipoprotein: somatic cell mutants define multiple genes required for expression of surface-receptor activity. Proc Natl Acad Sci U S A 81:5454–5458PubMedPubMedCentralCrossRefGoogle Scholar
  59. Klinger CM, Spang A, Dacks JB, Ettema TJ (2016) Tracing the archaeal origins of eukaryotic membrane-trafficking system building blocks. Mol Biol Evol 33:1528–1541PubMedCrossRefGoogle Scholar
  60. Kodera H et al (2015) Mutations in COG2 encoding a subunit of the conserved oligomeric golgi complex cause a congenital disorder of glycosylation. Clin Genet 87:455–460PubMedCrossRefGoogle Scholar
  61. Koenig E (1967) Synthetic mechanisms in the axon. IV. In vitro incorporation of [3H]precursors into axonal protein and RNA. J Neurochem 14:437–446PubMedCrossRefGoogle Scholar
  62. Koumandou VL, Dacks JB, Coulson RM, Field MC (2007) Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins. BMC Evol Biol 7:29PubMedPubMedCentralCrossRefGoogle Scholar
  63. Kozarsky KF, Brush HA, Krieger M (1986) Unusual forms of low density lipoprotein receptors in hamster cell mutants with defects in the receptor structural gene. J Cell Biol 102:1567–1575PubMedCrossRefGoogle Scholar
  64. Kranz C et al (2007) COG8 deficiency causes new congenital disorder of glycosylation type IIh. Hum Mol Genet 16:731–741PubMedCrossRefGoogle Scholar
  65. 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 14:194–204PubMedCrossRefGoogle Scholar
  66. Kunwar AJ et al (2011) Lack of the endosomal SNAREs vti1a and vti1b led to significant impairments in neuronal development. Proc Natl Acad Sci U S A 108:2575–2580PubMedPubMedCentralCrossRefGoogle Scholar
  67. Laufman O, Kedan A, Hong W, Lev S (2009) Direct interaction between the COG complex and the SM protein, Sly1, is required for Golgi SNARE pairing. EMBO J 28:2006–2017PubMedPubMedCentralCrossRefGoogle Scholar
  68. Laufman O, Hong W, Lev S (2011) The COG complex interacts directly with Syntaxin 6 and positively regulates endosome-to-TGN retrograde transport. J Cell Biol 194:459–472PubMedPubMedCentralCrossRefGoogle Scholar
  69. Laufman O, Hong W, Lev S (2013) The COG complex interacts with multiple Golgi SNAREs and enhances fusogenic assembly of SNARE complexes. J Cell Sci 126:1506–1516PubMedCrossRefGoogle Scholar
  70. Lees JA, Yip CK, Walz T, Hughson FM (2010) Molecular organization of the COG vesicle tethering complex. Nat Struct Mol Biol 17:1292–1297PubMedPubMedCentralCrossRefGoogle Scholar
  71. Lencer WI, Delp C, Neutra MR, Madara JL (1992) Mechanism of cholera toxin action on a polarized human intestinal epithelial cell line: role of vesicular traffic. J Cell Biol 117:1197–1209PubMedCrossRefGoogle Scholar
  72. Liu C et al (2017) Loss of the golgin GM130 causes Golgi disruption, Purkinje neuron loss, and ataxia in mice. Proc Natl Acad Sci U S A 114:346–351PubMedCrossRefGoogle Scholar
  73. Lubbehusen J et al (2010) Fatal outcome due to deficiency of subunit 6 of the conserved oligomeric Golgi complex leading to a new type of congenital disorders of glycosylation. Hum Mol Genet 19:3623–3633PubMedCrossRefGoogle Scholar
  74. Marshall RD (1974) The nature and metabolism of the carbohydrate-peptide linkages of glycoproteins. Biochem Soc Symp 40:17–26Google Scholar
  75. McConlogue L, Castellano F, de Wit C, Schenk D, Maltese WA (1996) Differential effects of a Rab6 mutant on secretory versus amyloidogenic processing of Alzheimer’s beta-amyloid precursor protein. J Biol Chem 271:1343–1348PubMedCrossRefGoogle Scholar
  76. Merianda TT et al (2009) A functional equivalent of endoplasmic reticulum and Golgi in axons for secretion of locally synthesized proteins. Mol Cell Neurosci 40:128–142PubMedCrossRefGoogle Scholar
  77. Mikhaylova M, Bera S, Kobler O, Frischknecht R, Kreutz MR (2016) A dendritic Golgi satellite between ERGIC and retromer. Cell Rep 14:189–199PubMedCrossRefGoogle Scholar
  78. Miller VJ et al (2013) Molecular insights into vesicle tethering at the Golgi by the conserved oligomeric Golgi (COG) complex and the golgin TATA element modulatory factor (TMF). J Biol Chem 288:4229–4240PubMedCrossRefGoogle Scholar
  79. Mironov AA, Weidman P, Luini A (1997) Variations on the intracellular transport theme: maturing cisternae and trafficking tubules. J Cell Biol 138:481–484PubMedPubMedCentralCrossRefGoogle Scholar
  80. Mironov AA, Sesorova IS, Seliverstova EV, Beznoussenko GV (2017) Different Golgi ultrastructure across species and tissues: implications under functional and pathological conditions, and an attempt at classification. Tissue Cell 49:186–201PubMedCrossRefGoogle Scholar
  81. 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 14:2277–2291PubMedPubMedCentralCrossRefGoogle Scholar
  82. Mollenhauer HH, Morre DJ (1978) Structural differences contrast higher plant and animal Golgi apparatus. J Cell Sci 32:357–362PubMedGoogle Scholar
  83. Morava E et al (2007) A common mutation in the COG7 gene with a consistent phenotype including microcephaly, adducted thumbs, growth retardation, VSD and episodes of hyperthermia. Eur J Hum Genet 15:638–645PubMedCrossRefGoogle Scholar
  84. Morelle W et al (2017) Galactose supplementation in patients with TMEM165-CDG rescues the glycosylation defects. J Clin Endocrinol Metab 102:1375–1386PubMedCrossRefGoogle Scholar
  85. Moremen KW, Tiemeyer M, Nairn AV (2012) Vertebrate protein glycosylation: diversity, synthesis and function. Nat Rev Mol Cell Biol 13:448–462PubMedPubMedCentralCrossRefGoogle Scholar
  86. Mullin AP, Gokhale A, Larimore J, Faundez V (2011) Cell biology of the BLOC-1 complex subunit dysbindin, a schizophrenia susceptibility gene. Mol Neurobiol 44:53–64PubMedPubMedCentralCrossRefGoogle Scholar
  87. Ng BG et al (2007) Molecular and clinical characterization of a Moroccan Cog7 deficient patient. Mol Genet Metab 91:201–204PubMedPubMedCentralCrossRefGoogle Scholar
  88. Ng BG, Sharma V, Sun L, Loh E, Hong W, Tay SK, Freeze HH (2011) Identification of the first COG-CDG patient of Indian origin. Mol Genet Metab 102:364–367PubMedCrossRefGoogle Scholar
  89. Ngamukote S, Yanagisawa M, Ariga T, Ando S, RK Y (2007) Developmental changes of glycosphingolipids and expression of glycogenes in mouse brains. J Neurochem 103:2327–2341PubMedCrossRefGoogle Scholar
  90. Ortiz D, Medkova M, Walch-Solimena C, Novick P (2002) Ypt32 recruits the Sec4p guanine nucleotide exchange factor, Sec2p, to secretory vesicles; evidence for a Rab cascade in yeast. J Cell Biol 157:1005–1016PubMedPubMedCentralCrossRefGoogle Scholar
  91. Paesold-Burda P et al (2009) Deficiency in COG5 causes a moderate form of congenital disorders of glycosylation. Hum Mol Genet 18:4350–4356PubMedCrossRefGoogle Scholar
  92. Palmigiano A et al (2017) MALDI-MS profiling of serum O-glycosylation and N-glycosylation in COG5-CDG. J Mass Spectrom 52:372–377PubMedCrossRefGoogle Scholar
  93. Papanikou E, Day KJ, Austin J, Glick BS (2015) COPI selectively drives maturation of the early Golgi. Elife 4.
  94. Pelham HR (2001) Traffic through the Golgi apparatus. J Cell Biol 155:1099–1101PubMedPubMedCentralCrossRefGoogle Scholar
  95. Pelham HR, Rothman JE (2000) The debate about transport in the Golgi – two sides of the same coin? Cell 102:713–719PubMedCrossRefGoogle Scholar
  96. Pfeffer SR (2010) How the Golgi works: a cisternal progenitor model. Proc Natl Acad Sci U S A 107:19614–19618PubMedPubMedCentralCrossRefGoogle Scholar
  97. Pierce JP, Mayer T, McCarthy JB (2001) Evidence for a satellite secretory pathway in neuronal dendritic spines. Curr Biol 11:351–355PubMedCrossRefGoogle Scholar
  98. Pokrovskaya ID, Willett R, Smith RD, Morelle W, Kudlyk T, Lupashin VV (2011) Conserved oligomeric Golgi complex specifically regulates the maintenance of Golgi glycosylation machinery. Glycobiology 21:1554–1569PubMedPubMedCentralCrossRefGoogle Scholar
  99. Potelle S et al (2017) Manganese-induced turnover of TMEM165. Biochem J 474:1481–1493PubMedPubMedCentralCrossRefGoogle Scholar
  100. Quassollo G et al (2015) A RhoA signaling pathway regulates dendritic Golgi outpost formation. Curr Biol 25:971–982PubMedCrossRefGoogle Scholar
  101. Ram RJ, Li B, Kaiser CA (2002) Identification of Sec36p, Sec37p, and Sec38p: components of yeast complex that contains Sec34p and Sec35p. Mol Biol Cell 13:1484–1500PubMedPubMedCentralCrossRefGoogle Scholar
  102. Rendon WO, Martinez-Alonso E, Tomas M, Martinez-Martinez N, Martinez-Menarguez JA (2013) Golgi fragmentation is Rab and SNARE dependent in cellular models of Parkinson’s disease. Histochem Cell Biol 139:671–684PubMedCrossRefGoogle Scholar
  103. Reynders E et al (2009) Golgi function and dysfunction in the first COG4-deficient CDG type II patient. Hum Mol Genet 18:3244–3256PubMedPubMedCentralCrossRefGoogle Scholar
  104. Richardson BC, Smith RD, Ungar D, Nakamura A, Jeffrey PD, Lupashin VV, Hughson FM (2009) Structural basis for a human glycosylation disorder caused by mutation of the COG4 gene. Proc Natl Acad Sci U S A 106:13329–13334PubMedPubMedCentralCrossRefGoogle Scholar
  105. Rizo J, Sudhof TC (2012) The membrane fusion enigma: SNAREs, Sec1/Munc18 proteins, and their accomplices – guilty as charged? Annu Rev Cell Dev Biol 28:279–308PubMedCrossRefGoogle Scholar
  106. Robinson MS (2015) Forty years of Clathrin-coated vesicles. Traffic 16:1210–1238PubMedCrossRefGoogle Scholar
  107. Rosenbaum EE, Vasiljevic E, Cleland SC, Flores C, Colley NJ (2014) The Gos28 SNARE protein mediates intra-Golgi transport of rhodopsin and is required for photoreceptor survival. J Biol Chem 289:32392–32409PubMedPubMedCentralCrossRefGoogle Scholar
  108. Rossanese OW, Soderholm J, Bevis BJ, Sears IB, O’Connor J, Williamson EK, Glick BS (1999) Golgi structure correlates with transitional endoplasmic reticulum organization in Pichia pastoris and Saccharomyces cerevisiae. J Cell Biol 145:69–81PubMedPubMedCentralCrossRefGoogle Scholar
  109. Rothman JE (2002) Lasker basic medical research award. The machinery and principles of vesicle transport in the cell. Nat Med 8:1059–1062PubMedCrossRefGoogle Scholar
  110. Rout MP, Field MC (2017) The evolution of organellar coat complexes and organization of the eukaryotic cell. Annu Rev Biochem 86:637–657PubMedCrossRefGoogle Scholar
  111. Rush JS, Panneerselvam K, Waechter CJ, Freeze HH (2000) Mannose supplementation corrects GDP-mannose deficiency in cultured fibroblasts from some patients with Congenital Disorders of Glycosylation (CDG). Glycobiology 10:829–835PubMedCrossRefGoogle Scholar
  112. Rymen D et al (2012) COG5-CDG: expanding the clinical spectrum. Orphanet J Rare Dis 7:94PubMedPubMedCentralCrossRefGoogle Scholar
  113. Rymen D et al (2015) Key features and clinical variability of COG6-CDG. Mol Genet Metab 116(3):163–170PubMedCrossRefGoogle Scholar
  114. Satoh T, Nakamura Y, Satoh AK (2016) The roles of Syx5 in Golgi morphology and Rhodopsin transport in Drosophila photoreceptors. Biol Open 5:1420–1430PubMedPubMedCentralCrossRefGoogle Scholar
  115. Shaheen R, Ansari S, Alshammari MJ, Alkhalidi H, Alrukban H, Eyaid W, Alkuraya FS (2013) A novel syndrome of hypohidrosis and intellectual disability is linked to COG6 deficiency. J Med Genet 50:431–436PubMedCrossRefGoogle Scholar
  116. Shestakova A, Zolov S, Lupashin V (2006) COG complex-mediated recycling of Golgi glycosyltransferases is essential for normal protein glycosylation. Traffic 7:191–204PubMedCrossRefGoogle Scholar
  117. Shestakova A, Suvorova E, Pavliv O, Khaidakova G, Lupashin V (2007) Interaction of the conserved oligomeric Golgi complex with t-SNARE Syntaxin5a/Sed5 enhances intra-Golgi SNARE complex stability. J Cell Biol 179:1179–1192PubMedPubMedCentralCrossRefGoogle Scholar
  118. Simpson MA et al (2004) Infantile-onset symptomatic epilepsy syndrome caused by a homozygous loss-of-function mutation of GM3 synthase. Nat Genet 36:1225–1229PubMedCrossRefGoogle Scholar
  119. Smith RD, Willett R, Kudlyk T, Pokrovskaya I, Paton AW, Paton JC, Lupashin VV (2009) The COG complex, Rab6 and COPI define a novel Golgi retrograde trafficking pathway that is exploited by SubAB toxin. Traffic 10:1502–1517PubMedPubMedCentralCrossRefGoogle Scholar
  120. Sohda M et al (2007) The interaction of two tethering factors, p115 and COG complex, is required for Golgi integrity. Traffic 8:270–284PubMedCrossRefGoogle Scholar
  121. Sohda M et al (2010) Interaction of Golgin-84 with the COG complex mediates the intra-Golgi retrograde transport. Traffic 11:1552–1566PubMedCrossRefGoogle Scholar
  122. Soo KY et al (2015) Rab1-dependent ER-Golgi transport dysfunction is a common pathogenic mechanism in SOD1, TDP-43 and FUS-associated ALS. Acta Neuropathol 130:679–697PubMedCrossRefGoogle Scholar
  123. Sprecher E et al (2005) A mutation in SNAP29, coding for a SNARE protein involved in intracellular trafficking, causes a novel neurocutaneous syndrome characterized by cerebral dysgenesis, neuropathy, ichthyosis, and palmoplantar keratoderma. Am J Hum Genet 77:242–251PubMedPubMedCentralCrossRefGoogle Scholar
  124. Stanley P, Schachter H, Taniguchi N (2009) N-Glycans. In: Varki A et al (eds) Essentials of glycobiology, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  125. Suga K, Saito A, Tomiyama T, Mori H, Akagawa K (2005) Syntaxin 5 interacts specifically with presenilin holoproteins and affects processing of betaAPP in neuronal cells. J Neurochem 94:425–439PubMedCrossRefGoogle Scholar
  126. Suga K, Saito A, Akagawa K (2015) ER stress response in NG108-15 cells involves upregulation of syntaxin 5 expression and reduced amyloid beta peptide secretion. Exp Cell Res 332:11–23PubMedCrossRefGoogle Scholar
  127. 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 157:631–643PubMedPubMedCentralCrossRefGoogle Scholar
  128. Tarassov K et al (2008) An in vivo map of the yeast protein interactome. Science 320:1465–1470PubMedCrossRefGoogle Scholar
  129. Tennyson VM (1970) The fine structure of the axon and growth cone of the dorsal root neuroblast of the rabbit embryo. J Cell Biol 44:62–79PubMedPubMedCentralCrossRefGoogle Scholar
  130. Thayanidhi N, Helm JR, Nycz DC, Bentley M, Liang Y, Hay JC (2010) Alpha-synuclein delays endoplasmic reticulum (ER)-to-Golgi transport in mammalian cells by antagonizing ER/Golgi SNAREs. Mol Biol Cell 21:1850–1863PubMedPubMedCentralCrossRefGoogle Scholar
  131. Tripathi A, Ren Y, Jeffrey PD, Hughson FM (2009) Structural characterization of Tip20p and Dsl1p, subunits of the Dsl1p vesicle tethering complex. Nat Struct Mol Biol 16:114–123PubMedPubMedCentralCrossRefGoogle Scholar
  132. Uetz P et al (2000) A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403:623–627PubMedCrossRefGoogle Scholar
  133. Ungar D et al (2002) Characterization of a mammalian Golgi-localized protein complex, COG, that is required for normal Golgi morphology and function. J Cell Biol 157:405–415PubMedPubMedCentralCrossRefGoogle Scholar
  134. Van Rheenen SM, Cao X, Lupashin VV, Barlowe C, Waters MG (1998) Sec35p, a novel peripheral membrane protein, is required for ER to Golgi vesicle docking. J Cell Biol 141:1107–1119CrossRefGoogle Scholar
  135. Van Rheenen SM, Cao X, Sapperstein SK, Chiang EC, Lupashin VV, Barlowe C, Waters MG (1999) Sec34p, a protein required for vesicle tethering to the yeast Golgi apparatus, is in a complex with Sec35p. J Cell Biol 147:729–742CrossRefGoogle Scholar
  136. Walter DM, Paul KS, Waters MG (1998) Purification and characterization of a novel 13 S hetero-oligomeric protein complex that stimulates in vitro Golgi transport. J Biol Chem 273:29565–29576PubMedCrossRefGoogle Scholar
  137. Walter AM et al (2014) The SNARE protein vti1a functions in dense-core vesicle biogenesis. EMBO J 33:1681–1697PubMedPubMedCentralCrossRefGoogle Scholar
  138. Weber T et al (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92:759–772PubMedCrossRefGoogle Scholar
  139. Whyte JR, Munro S (2001) The Sec34/35 Golgi transport complex is related to the exocyst, defining a family of complexes involved in multiple steps of membrane traffic. Dev Cell 1:527–537PubMedCrossRefGoogle Scholar
  140. Whyte JR, Munro S (2002) Vesicle tethering complexes in membrane traffic. J Cell Sci 115:2627–2637PubMedGoogle Scholar
  141. Willett R, Kudlyk T, Pokrovskaya I, Schonherr R, Ungar D, Duden R, Lupashin V (2013a) COG complexes form spatial landmarks for distinct SNARE complexes. Nat Commun 4:1553PubMedPubMedCentralCrossRefGoogle Scholar
  142. Willett R, Ungar D, Lupashin V (2013b) The Golgi puppet master: COG complex at center stage of membrane trafficking interactions. Histochem Cell Biol 140:271–283PubMedPubMedCentralCrossRefGoogle Scholar
  143. Willett R, Pokrovskaya I, Kudlyk T, Lupashin V (2014) Multipronged interaction of the COG complex with intracellular membranes. Cell Logist 4:e27888PubMedPubMedCentralCrossRefGoogle Scholar
  144. Willett R, Blackburn JB, Climer L, Pokrovskaya I, Kudlyk T, Wang W, Lupashin V (2016) COG lobe B sub-complex engages v-SNARE GS15 and functions via regulated interaction with lobe a sub-complex. Sci Rep 6:29139PubMedPubMedCentralCrossRefGoogle Scholar
  145. Witkos TM, Lowe M (2017) Recognition and tethering of transport vesicles at the Golgi apparatus. Curr Opin Cell Biol 47:16–23PubMedCrossRefGoogle Scholar
  146. Wu X et al (2004) Mutation of the COG complex subunit gene COG7 causes a lethal congenital disorder. Nat Med 10:518–523PubMedCrossRefGoogle Scholar
  147. Yang A et al (2017) Further delineation of COG8-CDG: a case with novel compound heterozygous mutations diagnosed by targeted exome sequencing. Clin Chim Acta 471:191–195PubMedCrossRefGoogle Scholar
  148. Ye B, Zhang Y, Song W, Younger SH, Jan LY, Jan YN (2007) Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130:717–729PubMedPubMedCentralCrossRefGoogle Scholar
  149. Yu IM, Hughson FM (2010) Tethering factors as organizers of intracellular vesicular traffic. Annu Rev Cell Dev Biol 26:137–156PubMedCrossRefGoogle Scholar
  150. Yu RK, Macala LJ, Taki T, Weinfield HM, FS Y (1988) Developmental changes in ganglioside composition and synthesis in embryonic rat brain. J Neurochem 50:1825–1829PubMedCrossRefGoogle Scholar
  151. Zeevaert R et al (2009) A new mutation in COG7 extends the spectrum of COG subunit deficiencies. Eur J Med Genet 52:303–305PubMedCrossRefGoogle Scholar
  152. Zhou W, Chang J, Wang X, Savelieff MG, Zhao Y, Ke S, Ye B (2014) GM130 is required for compartmental organization of dendritic golgi outposts. Curr Biol 24:1227–1233PubMedPubMedCentralCrossRefGoogle Scholar
  153. Zlatic S, Comstra HS, Gokhale A, Petris MJ, Faundez V (2015) Molecular basis of neurodegeneration and neurodevelopmental defects in Menkes disease. Neurobiol Dis 81:154–161PubMedPubMedCentralCrossRefGoogle Scholar
  154. Zolov SN, Lupashin VV (2005) Cog3p depletion blocks vesicle-mediated Golgi retrograde trafficking in HeLa cells. J Cell Biol 168:747–759PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Leslie K. Climer
    • 1
  • Rachel D. Hendrix
    • 2
  • Vladimir V. Lupashin
    • 1
  1. 1.College of Medicine, Physiology and BiophysicsUAMSLittle RockUSA
  2. 2.College of Medicine, Neurobiology and Developmental SciencesUAMSLittle RockUSA

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