Skip to main content
Log in

Chronic Alcohol Exposure Affects the Cell Components Involved in Membrane Traffic in Neuronal Dendrites

  • Original Article
  • Published:
Neurotoxicity Research Aims and scope Submit manuscript

Abstract

The specific traffic of the membrane components in neurons is a major requirement to establish and maintain neuronal domains—the axonal and the somatodendritic domains—and their polarized morphology. Unlike axons, dendrites contain membranous organelles, which are involved in the secretory pathway, including the endoplasmic reticulum, the Golgi apparatus and post-Golgi apparatus carriers, the cytoskeleton, and plasma membrane. A variety of molecules and factors are also involved in this process. Previous studies have shown that chronic alcohol exposure negatively affects several of these cell components, such as the Golgi apparatus or cytoskeleton in neurons. Yet very little information is available on the possible effects of this exposure on the remaining cell elements involved in intracellular trafficking in neurons, particularly in dendrites. By qualitative and quantitative electron microscopy, immunofluorescence and immunoblotting, we herein show that chronic exposure to moderate levels (30 mM) of ethanol in cultured neurons reduces the volume and surface density of the rough endoplasmic reticulum, and increases the levels of GRP78, a chaperone involved in endoplasmic reticulum stress. Ethanol also significantly diminishes the proportion of neurons that show an extension of Golgi into dendrites and dendritic Golgi outposts, a structure present exclusively in longer, thicker apical dendrites. Both Golgi apparatus types were also fragmented into a large number of cells. We also investigated the effect of alcohol on the levels of microtubule-based motor proteins KIF5, KIF17, KIFC2, dynein, and myosin IIb, responsible for transporting different cargoes in dendrites. Of these, alcohol differently affects several of them by lowering dynein and raising KIF5, KIFC2, and myosin IIb. These results, together with other previously published ones, suggest that practically all the protein trafficking steps in dendrites are altered to a greater or lesser extent by chronic alcohol exposure in neuronal cells, which may have negative repercussions for the development and maintenance of their polarized morphology and function.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • American Academy of Pediatrics Committee on Substance Abuse and Committee on Children with Disabilities (2000) Fetal alcohol syndrome and alcohol-related neurodevelopmental disorders. Pediatrics 106:358–361

    Article  Google Scholar 

  • Araki K, Nagata K (2012) Protein folding and quality control in the ER. Cold Spring Harb Perspect Biol 4:a015438

    Article  PubMed Central  PubMed  Google Scholar 

  • Bannai H, Inoue T, Nakayama T, Hattori M, Mikoshiba K (2004) Kinesin dependent, rapid, bi-directional transport of ER sub-compartment in dendrites of hippocampal neurons. J Cell Sci 117:163–175

    Article  CAS  PubMed  Google Scholar 

  • Beck R, Rawet M, Wieland FT, Cassel D (2009) The COPI system: molecular mechanisms and function. FEBS Lett 583:2701–2709

    Article  CAS  PubMed  Google Scholar 

  • Benyair R, Ron E, Lederkremer GZ (2011) Protein quality control, retention, and degradation at the endoplasmic reticulum. Int Rev Cell Mol Biol 292:197–280

    Article  CAS  PubMed  Google Scholar 

  • Berridge MJ (2012) Calcium signalling remodelling and disease. Biochem Soc Trans 40:297–309

    Article  CAS  PubMed  Google Scholar 

  • Binkhorst M, Wortmann SB, Funke S, Kozicz T, Wevers RA, Morava E (2012) Glycosylation defects underlying fetal alcohol spectrum disorder: a novel pathogenetic model. “When the wine goes in, strange things come out” ST Coleridge. The Piccolomini J Inherit Metab Dis 35:399–405

    Article  CAS  Google Scholar 

  • Boncompain G, Perez F (2013) The many routes of Golgi-dependent trafficking. Histochem Cell Biol. doi:10.1007/s00418-013-1124-7

  • Brewer GJ, Torricelli JR, Evege EK, Price PJ (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35:567–576

    Article  CAS  PubMed  Google Scholar 

  • Camarillo C, Miranda RC (2008) Ethanol exposure during neurogenesis induces persistent effects on neural maturation: evidence from an ex vivo model of fetal cerebral cortical neuroepithelial progenitor maturation. Gene Expr 14:159–171

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cameron PL, Sudhof TC, Jahn R, De Camilli P (1991) Colocalization of synaptophysin with transferrin receptors: implications for synaptic vesicle biogenesis. J Cell Biol 115:151–164

    Article  CAS  PubMed  Google Scholar 

  • Cancino J, Luini A (2013) Signaling circuits on the Golgi complex. Traffic 14:121–134

    Article  CAS  PubMed  Google Scholar 

  • Capitani M, Sallese M (2009) The KDEL receptor: new functions for an old protein. FEBS Lett 583:3863–3871

    Article  CAS  PubMed  Google Scholar 

  • Chen G, Ma C, Bower KA, Shi X, Ke Z, Luo J (2008) Ethanol promotes endoplasmic reticulum stress induced neuronal death: involvement of oxidative stress. J Neurosci Res 86:937–946

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Conde C, Cáceres A (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10:319–332

    Article  CAS  PubMed  Google Scholar 

  • Cottam NP, Ungar D (2012) Retrograde vesicle transport in the Golgi. Protoplasma 249:943–955

    Article  CAS  PubMed  Google Scholar 

  • D’Addario C, Ming Y, Ogren SO, Terenius L (2008) The role of acetaldehyde in mediating effects of alcohol on expression of endogenous opioid system genes in a neuroblastoma cell line. FASEB J 22:662–670

    Article  PubMed  Google Scholar 

  • Day KJ, Staehelin LA, Glick BS (2013) A three-stage model of Golgi structure and function. Histochem Cell Biol 140:239–249

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Eckardt MJ, File SE, Gessa GL, Grant KA, Guerri C, Hoffman PL, Kalant H, Koob GF, Li TK, Tabakoff B (1998) Effects of moderate alcohol consumption on the central nervous system. Alcohol Clin Exp Res 22:998–1040

    Article  CAS  PubMed  Google Scholar 

  • English AR, Voeltz GK (2013) Rab10 GTPase regulates ER dynamics and morphology. Nat Cell Biol 15:169–178

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Esteban-Pretel G, Marín MP, Romero AM, Ponsoda X, Ballestin R, Canales JJ, Renau-Piqueras J (2011) Protein traffic is an intracellular target in alcohol toxicity. Pharmaceuticals 4:741–757

    Article  CAS  PubMed Central  Google Scholar 

  • Esteban-Pretel G, Marín MP, Romero AM, Timoneda J, Ponsoda X, Ballestín R, Renau-Piqueras J (2013) Polyphosphoinositide metabolism and Golgi complex morphology in hippocampal neurons in primary culture is altered by chronic ethanol exposure. Alcohol Alcohol 48:15–27

    Article  CAS  PubMed  Google Scholar 

  • Flynn KC, Sties M, Bradke F (2013) Role of the cytoskeleton and membrane trafficking in axon-dendrite morphogenesis. In: Rubenstein J, Rakic P (eds) Cellular migration and formation of neuronal connections: comprehensive developmental neuroscience, vol 2. Academic, London, pp 19–50

    Chapter  Google Scholar 

  • Galligan JJ, Smathers RL, Shearn CT, Fritz KS, Backos DS, Jiang H, Franklin CC, Orlicky DJ, Maclean KN, Petersen DR (2012) Oxidative stress and the ER stress response in a murine model for early-stage alcoholic liver disease. J Toxicol 2012:207594

    Article  PubMed Central  PubMed  Google Scholar 

  • González A, Salido GM (2009) Ethanol alters the physiology of neuron-glia communication. Int Rev Neurobiol 88:167–198

    Article  PubMed  Google Scholar 

  • Goodlett C, Horn K, Zhou F (2005) Alcohol teratogenesis: mechanisms of damage and strategies for intervention. Exp Biol Med 230:394–406

    CAS  Google Scholar 

  • Gorbatyuk MS, Gorbatyuk OS (2013) The molecular chaperone GRP78/BiP as a therapeutic target for neurodegenerative disorders: a mini review. J Genet Syndr Gene Ther 4(2):128

    PubMed Central  PubMed  Google Scholar 

  • Guerri C, Riley E, Strömland K (1999) Commentary on the recommendations of the Royal College of Obstetricians and Gynaecologists concerning alcohol consumption in pregnancy. Alcohol Alcohol 34:497–501

    Article  CAS  PubMed  Google Scholar 

  • Guerri C, Bazinet A, Riley EP (2009) Foetal alcohol spectrum disorders and alterations in brain and behaviour. Alcohol Alcohol 44:108–114

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hanus C, Ehlers MD (2008) Secretory outposts for the local processing of membrane cargo in neuronal dendrites. Traffic 9:1437–1445

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hetz C (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13:89–102

    CAS  PubMed  Google Scholar 

  • Hirokawa N (2011) From electron microscopy to molecular cell biology, molecular genetics and structural biology: intracellular transport and kinesin superfamily proteins, KIFs: genes, structure, dynamics and functions. J Electron Microsc (Tokyo) 60(Suppl 1):S63–S92

    CAS  Google Scholar 

  • Hirokawa N, Niwa S, Tanaka Y (2010) Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron 68:610–638

    Article  CAS  PubMed  Google Scholar 

  • Hodges JL, Newell-Litwa K, Asmussen H, Vicente-Manzanares M, Horwitz AR (2011) Myosin IIb activity and phosphorylation status determines dendritic spine and post-synaptic density morphology. PLoS ONE 6:e24149

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Horton AC, Ehlers MD (2004) Secretory trafficking in neuronal dendrites. Nat Cell Biol 6:585–591

    Article  CAS  PubMed  Google Scholar 

  • Horton AC, Rácz B, Monson EE, Lin AL, Weinberg RJ, Ehlers MD (2005) Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48:757–771

    Article  CAS  PubMed  Google Scholar 

  • Ji C (2012) Mechanisms of alcohol-induced endoplasmic reticulum stress and organ injuries. Biochem Res Int 2012:216450

    Article  PubMed Central  PubMed  Google Scholar 

  • Kapitein LC, Hoogenraad CC (2011) Which way to go? Cytoskeletal organization and polarized transport in neurons. Mol Cell Neurosci 46:9–20

    Article  CAS  PubMed  Google Scholar 

  • Kapitein LC, Schlager MA, Kuijpers M, Wulf PS, van Spronsen M, MacKintosh FC, Hoogenraad CC (2010) Mixed microtubules steer dynein-driven cargo transport into dendrites. Curr Biol 20:290–299

    Article  CAS  PubMed  Google Scholar 

  • Ke Z, Wang X, Liu Y, Fan Z, Chen G, Xu M, Bower KA, Frank JA, Li M, Fang S, Shi X, Luo J (2011) Ethanol induces endoplasmic reticulum stress in the developing brain. Alcohol Clin Exp Res 35:1574–1583

    CAS  PubMed  Google Scholar 

  • Kennedy MJ, Ehlers MD (2006) Organelles and trafficking machinery for postsynaptic plasticity. Annu Rev Neurosci 29:325–362

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kiebler MA, Bassell GJ (2006) Neuronal RNA granules: movers and makers. Neuron 51:685–690

    Article  CAS  PubMed  Google Scholar 

  • Kim KC, Go HS, Bak HR, Choi CS, Choi I, Kim P, Han SH, Han SM, Shin CY, Ko KH (2010) Prenatal exposure of ethanol induces increased glutamatergic neuronal differentiation of neural progenitor cells. J Biomed Sci 12:17–85

    Google Scholar 

  • Kollins KM, Bell RL, Butts M, Withers GS (2009) Dendrites differ from axons in patterns of microtubule stability and polymerization during development. Neural Dev 4:26

    Article  PubMed Central  PubMed  Google Scholar 

  • Kouzoukas DE, Li G, Takapoo M, Moninger T, Bhalla RC, Pantazis NJ (2013) Intracellular calcium plays a critical role in the alcohol-mediated death of cerebellar granule neurons. J Neurochem 124:323–335

    Article  CAS  PubMed  Google Scholar 

  • Lasiecka ZM, Yap CC, Vakulenko M, Winckler B (2009) Compartmentalizing the neuronal plasma membrane: from axon initial segments to synapses. Int Rev Cell Mol Biol 272:303–389

    Article  CAS  PubMed  Google Scholar 

  • Lee AS (2005) The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods 35:373–381

    Article  CAS  PubMed  Google Scholar 

  • Lindke A, Tremper-Wells B, Miller MW (2008) Generation and use of primary rat cultures for studies of the effects of ethanol. In: Nagi LE (ed) Alcohol: methods and protocols. Humana, New York, pp 255–264

    Google Scholar 

  • Linstedt AD, Hauri HP (1993) Giantin, a novel conserved Golgi membrane protein containing a cytoplasmic domain of at least 350 kDa. Mol Biol Cell 4:679–693

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu Y, Xu XH, Chen Q, Wang T, Deng CY, Song BL, Du JL, Luo ZG (2005) Myosin Vb controls biogenesis of post-Golgi Rab10 carriers during axon development. Nat Commun 4:2005

    Google Scholar 

  • Lodish H, Berk A, Kaiser CA, Krieger M, Bretscher A, Ploegh H, Amon A, Scott MP (2012) Molecular cell biology, 7th edn. WH Freeman, New York

    Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Lucocq J (2008) Quantification of structures and gold labeling in Transmission Electron Microscopy. Methods Cell Biol 88:59–82

    Article  PubMed  Google Scholar 

  • Ma Y, Hendershot LM (2004) ER chaperone functions during normal and stress conditions. J Chem Neuroanat 28:51–65

    Article  CAS  PubMed  Google Scholar 

  • Marín MP, Tomás M, Esteban-Pretel G, Megías L, López-Iglesias C, Egea G, Renau-Piqueras J (2008) Chronic ethanol exposure induces alterations in the nucleocytoplasmic transport in growing astrocytes. J Neurochem 106:1914–1928

    Article  PubMed  Google Scholar 

  • Marín MP, Esteban-Pretel G, Ponsoda X, Romero AM, Ballestín R, López C, Megías L, Timoneda J, Molowny A, Canales JJ, Renau-Piqueras J (2010) Endocytosis in cultured neurons is altered by chronic alcohol exposure. Toxicol Sci 115:202–213

    Article  PubMed  Google Scholar 

  • Martínez SE, Egea G (2007) Novel molecular targets for the prevention of fetal alcohol syndrome. Recent Pat CNS Drug Discov 2:23–35

    Article  PubMed  Google Scholar 

  • Martínez-Menarguez JA (2013) Intra-Golgi transport: roles for vesicles, tubules, and cisternae. ISRN Cell Biol. Article ID126731, 15 p. doi:10.1155/2013/126731

  • Marzec M, Eletto D, Argon Y (2012) GRP94: An HSP90-like protein specialized for protein folding and quality control in the endoplasmic reticulum. Biochim Biophys Acta 1823:774–787

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • May PA, Gossage JP, Kalberg WO, Robinson LK, Buckley D, Manning M, Hoyme HE (2009) Prevalence and epidemiologic characteristics of FASD from various research methods with an emphasis on recent in-school studies. Dev Disabil Res Rev 15:176–192

    Article  PubMed  Google Scholar 

  • Mayhew TM (2011) Mapping the distributions and quantifying the labelling intensities of cell compartments by immunoelectron microscopy: progress towards a coherent set of methods. J Anat 219:647–660

    Article  PubMed Central  PubMed  Google Scholar 

  • Miller MW (1992) Effects of prenatal exposure to ethanol on cell proliferation and neuronal migration. In: Miller MW (ed) Development of the central nervous system: effects of alcohol and opiates. Wiley-Liss Inc, New York, NY, pp 47–69

  • Oyadomari S, Mori M (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11:381–389

    Article  CAS  PubMed  Google Scholar 

  • Powrozek TA, Olson EC (2012) Ethanol-induced disruption of Golgi apparatus morphology, primary neurite number and cellular orientation in developing cortical neurons. Alcohol 46:619–627

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Price PJ, Brewer GJ (2001) Serum-free media for neural cell cultures. Adult and embryonic. In: Fedoroff S, Richardson A (eds) Protocols for neural cell culture, 3rd edn. Humana Press Inc., Totowa, pp 255–264

    Chapter  Google Scholar 

  • Qian Y (2010) Heavy metal-regulated gene expression. In: McQueen CA (ed) Comprehensive toxicology: cellular and molecular toxicology, vol 2, 2nd edn. Elsevier Ltd, Oxford, pp 495–521

    Chapter  Google Scholar 

  • Ramírez OA, Couve A (2011) The endoplasmic reticulum and protein trafficking in dendrites and axons. Trends Cell Biol 21:2192–2227

    Article  Google Scholar 

  • Renau-Piqueras J, Cervera J (1983) Chromatin pattern of isolated human small thymocytes. A morphometric and stereologic study. Virchows Arch B Cell Pathol Incl Mol Pathol 42:315–325

    CAS  PubMed  Google Scholar 

  • Renau-Piqueras J, Gómez-Perretta C, Guerri C, Sanchís R (1985) Qualitative and quantitative ultrastructural alterations in hepatocytes of rats prenatally exposed to ethanol with special reference to mitochondria, Golgi apparatus and peroxisomes. Virchows Arch A Pathol Anat 405:237–251

    Article  CAS  Google Scholar 

  • Renau-Piqueras J, Miragall F, Marques A, Baguena-Cervellera R, Guerri C (1987) Chronic ethanol consumption affects filipin-cholesterol complexes and intramembranous particles of synaptosomes of rat brain cortex. Alcohol Clin Exp Res 11:486–493

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez FD, Simonsson P, Alling C (1992) A method for maintaining constant ethanol concentrations in cell culture media. Alcohol Alcohol 27:309–313

    PubMed  Google Scholar 

  • Romero AM, Esteban-Pretel G, Marín MP, Ponsoda X, Ballestín R, Canales JJ, Renau-Piqueras J (2010) Chronic ethanol exposure alters the levels, assembly, and cellular organization of the actin cytoskeleton and microtubules in hippocampal neurons in primary culture. Toxicol Sci 118:602–612

    Article  CAS  PubMed  Google Scholar 

  • Romero AM, Renau-Piqueras J, PilarMarín M, Timoneda J, Berciano MT, Lafarga M, Esteban-Pretel G (2013) Chronic alcohol alters dendritic spine development in neurons in primary culture. Neurotox Res 24:532–548

    Article  CAS  PubMed  Google Scholar 

  • Ruela C, Sousa N, Madeira MD, Paula-Barbosa MM (1994) Stereological study of the ultrastructural changes induced by chronic alcohol consumption and dehydration in the supraoptic nucleus of the rat hypothalamus. J Neurocytol 23:410–421

    Article  CAS  PubMed  Google Scholar 

  • Saito M, Chakraborty G, Mao RF, Wang R, Cooper TB, Vadasz C, Saito M (2007) Ethanol alters lipid profiles and phosphorylation status of AMP activated protein kinase in the neonatal mouse brain. J Neurochem 103:1208–1218

    Article  CAS  PubMed  Google Scholar 

  • Sampson PD, Streissguth AP, Bookstein FL, Little RE, Clarren SK, Dehaene P, Hanson JW, Graham JM Jr (1997) Incidence of fetal alcohol syndrome and prevalence of alcohol-related neurodevelopmental disorder. Teratology 56:317–326

    Article  CAS  PubMed  Google Scholar 

  • Schaub BE, Berger B, Berger EG, Rohrer J (2006) Transition of galactosyltransferase 1 from trans-Golgi cisterna to the trans-Golgi network is signal mediated. Mol Biol Cell 17:5153–5162

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sokol RJ, Delaney-Black V, Nordstrom B (2003) Fetal alcohol spectrum disorder. JAMA 290:2996–2999

    Article  CAS  PubMed  Google Scholar 

  • Sowell ER, Thompson PM, Mattson SN, Tessner KD, Jernigan TL, Riley EP, Toga AW (2002) Regional brain shape abnormalities persist into adolescence after heavy prenatal alcohol exposure. Cereb Cortex 12:856–865

    Article  PubMed  Google Scholar 

  • Srivastava DP, Woolfrey KM, Jones KA, Anderson CT, Smith KR, Russell TA, Lee H, Yasvoina MV, Wokosin DL, Ozdinler PH, Shepherd GM, Penzes P (2012) An autism-associated variant of Epac2 reveals a role for Ras/Epac2 signaling in controlling basal dendrite maintenance in mice. PLoS Biol 10:e1001350

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Streissguth AP, Bookstein FL, Barr HM, Sampson PD, O’Malley K, Young JK (2004) Risk factors for adverse life outcomes in fetal alcohol syndrome and fetal alcohol effects. J Dev Behav Pediatr 25:228–238

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tang BL (2008) Emerging aspects of membrane traffic in neuronal dendrite growth. Biochim Biophys Acta 1783:169–176

    Article  CAS  PubMed  Google Scholar 

  • Tang BL, Wang Y, Ong YS, Hong W (2005) COPII and exit from the endoplasmic reticulum. Biochim Biophys Acta 1744:293–303

    Article  CAS  PubMed  Google Scholar 

  • Tomás M, Marín P, Megías L, Egea G, Renau-Piqueras J (2005) Ethanol perturbs the secretory pathway in astrocytes. Neurobiol Dis 20:773–784

    Article  PubMed  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  Google Scholar 

  • Tomomura M, Hasegawa Y, Hashikawa T, Tomomura A, Yuzaki M, Furuichi T, Yano R (2003) Differential expression and function of apoptosis-associated tyrosine kinase (AATYK) in the developing mouse brain. Brain Res Mol Brain Res 112:103–112

    Article  CAS  PubMed  Google Scholar 

  • Valderrama F, Durán JM, Babià T, Barth H, Renau-Piqueras J, Egea G (2001) Actin microfilaments facilitate the retrograde transport from the Golgi complex to the endoplasmic reticulum in mammalian cells. Traffic 2:717–726

    Article  CAS  PubMed  Google Scholar 

  • Valenzuela CF (1997) Alcohol and neurotransmitter interactions. Alcohol Health Res World 21:144–148

    CAS  PubMed  Google Scholar 

  • Valenzuela JI, Jaureguiberry-Bravo M, Couve A (2011) Neuronal protein trafficking: emerging consequences of endoplasmic reticulum dynamics. Mol Cell Neurosci 48:269–277

    Article  CAS  PubMed  Google Scholar 

  • Verissimo F, Pepperkok R (2008) ER-to-Golgi transport. In: Minorov A, Pavelka M (eds) The Golgi apparatus. State of the art 110 years after Camilo Golgi’s discovery. Springer, New York, pp 333–341

    Google Scholar 

  • Wang T, Liu Y, Xu XH, Deng CY, Wu KY, Zhu J, Fu XQ, He M, Luo ZG (2011) Lgl1 activation of rab10 promotes axonal membrane trafficking underlying neuronal polarization. Dev Cell 21:431–444

    Article  CAS  PubMed  Google Scholar 

  • Webb B, Walker DW, Heaton MB (2003) Nerve growth factor and chronic ethanol treatment alter calcium homeostasis in developing rat septal neurons. Brain Res Dev Brain Res 143:57–71

    Article  CAS  PubMed  Google Scholar 

  • Weibel ER (1979) Stereological methods. Practical methods for biological morphometry, vol 1. Academic Press, London

    Google Scholar 

  • Williams M (1977) Stereological techniques. In: Glauert AM (ed) Practical methods in electron microscopy, vol 6, part 2, chap 2. North Holland/American Elsevier, Amsterdam, pp 1–84

    Google Scholar 

  • Xiao S, Jan LY (2009) A gate keeper for axonal transport. Cell 136:996–998

    Article  CAS  PubMed  Google Scholar 

  • 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 130:717–729

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zanetti G, Pahuja KB, Studer S, Shim S, Schekman R (2011) COPII and the regulation of protein sorting in mammals. Nat Cell Biol 14:20–28

    Article  PubMed  Google Scholar 

  • Zhou FC, Sari Y, Powrozek T, Goodlett CR, Li TK (2003) Moderate alcohol exposure compromises neural tube midline development in prenatal brain. Brain Res Dev Brain Res 144:43–55

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are very grateful to I. Monserrat for her technical help, A. Fuentes for helping us with the figures and to H. L. Warburton for linguistic assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guillermo Esteban-Pretel.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (TIFF 7431 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Romero, A.M., Renau-Piqueras, J., Marín, M.P. et al. Chronic Alcohol Exposure Affects the Cell Components Involved in Membrane Traffic in Neuronal Dendrites. Neurotox Res 27, 43–54 (2015). https://doi.org/10.1007/s12640-014-9484-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12640-014-9484-x

Keywords

Navigation