Chronic alcohol alters dendritic spine development in neurons in primary culture

Neurotoxicity Research

Volumn 24, Issue 4, 2013, Pages 532-548

  Romero, Ana M ^a   Renau Piqueras, Jaime ^a   Pilar Marin, M ^a   Timoneda, Joaquin ^b   Berciano, Maria T ^c   Lafarga, Miguel ^c   Esteban Pretel, Guillermo ^a  

^a HOSPITAL UNIVERSITARIO LA FE   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

^c UNIVERSITY OF CANTABRIA   (Spain)

Author keywords

Actin cytoskeleton; Chronic ethanol; Dendritic spines; Neurons; Synaptopodin

Indexed keywords

ACETYLCHOLINESTERASE; ACTIN BINDING PROTEIN; ALCOHOL; CHLORPHENIRAMINE MALEATE PLUS PHENYLEPHRINE; F ACTIN; G ACTIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SCAFFOLD PROTEIN; TUBULIN;

ANIMAL CELL; ARTICLE; CELL STRUCTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSKELETON; DENDRITIC SPINE; ENZYME ACTIVITY; FEMALE; FETUS; FLUORESCENCE MICROSCOPY; HIPPOCAMPUS; IN VITRO STUDY; LONG TERM EXPOSURE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIMARY CULTURE; PRIORITY JOURNAL; RAT; WESTERN BLOTTING;

ACETYLCHOLINESTERASE; ACTIN CYTOSKELETON; ACTINS; ANIMALS; CELLS, CULTURED; DENDRITIC SPINES; ETHANOL; FEMALE; HIPPOCAMPUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; NEURONS; RAS GTPASE-ACTIVATING PROTEINS; RATS; RATS, WISTAR; RECEPTORS, IONOTROPIC GLUTAMATE;

EID: 84885418879     PISSN: 10298428     EISSN: 14763524     Source Type: Journal    
DOI: 10.1007/s12640-013-9409-0     Document Type: Article

References (96)

1. 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
2. Berman RF, Hannigan JH (2000) Effects of prenatal alcohol exposure on the hippocampus: spatial behavior, electrophysiology, and neuroanatomy. Hippocampus 10:94-110
3. Berman RF, Hannigan JH, Sperry MA, Zajac CS (1996) Prenatal alcohol exposure and the effects of environmental enrichment on hippocampal dendritic spine density. Alcohol 13:209-216
4. Bhatt DH, Zhang S, Gan WB (2009) Dendritic spine dynamics. Annu Rev Physiol 71:261-282
5. 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
6. Bohlen Von, Halbach O (2009) Structure and function of dendritic spines within the hippocampus. Ann Anat 191:518-531
7. Bohlen Von, Halbach O (2010) Dendritic spine abnormalities in mental retardation. Cell Tissue Res 342:317-323
8. Bourne J, Harris KM (2007) Do thin spines learn to be mushroom spines that remember? Curr Opin Neurobiol 17:381-386
9. Bourne JN, Harris KM (2008) Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31:47-67
10. Boyer C, Schikorski T, Stevens CF (1998) Comparison of hippocampal dendritic spines in culture and in brain. J Neurosci 18:5294-5300
11. 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
12. Campoy FJ, Cabezas-Herrera J, Vidal CJ (1992) Interaction of AChE with Lens culinaris agglutinin reveals differences in glycosylation of molecular forms in sarcoplasmic reticulum membrane subfractions. J Neurosci Res 33:568-578
13. Carpenter-Hyland EP, Chandler LJ (2006) Homeostatic plasticity during alcohol exposure promotes enlargement of dendritic spines. Eur J Neurosci 24:3496-3506
14. Cingolani LA, Goda Y (2008) Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat Rev Neurosci 9:344-356
15. Condon KH, Ehlers MD (2007) Postsynaptic machinery for receptor trafficking. In: Beam AJ (ed) Protein trafficking in neurons. Academic Press, New York, pp 143-174
16. Cui Z, Zhao K, Zhao H, Yu D, Niu Y, Zhang J, Deng J (2010) Prenatal alcohol exposure induces long-term changes in dendritic spines and synapses in the mouse visual cortex. Alcohol Alcohol 45:312-319
17. Cullen CL, Burne TH, Lavidis NA, Moritz KM (2013) Low dose prenatal ethanol exposureinduces anxiety-like behaviour and alters dendritic morphology in the basolateralamygdala of rat offspring. PLoS One 8:e54924
18. 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
19. Deller T, Bas Orth C, Del Turco D, Vlachos A, Burbach GJ, Drakew A, Chabanis S, Korte M, Schwegler H, Haas CA, Frotscher M (2007) A role for synaptopodin and the spine apparatus in hippocampal synaptic plasticity. Ann Anat 189:5-16
20. 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
21. Esteban-Pretel G, Marín MP, Romero AM, Ponsoda X, Ballestín R, Canales JJ, Renau-Piqueras JJ (2011) Protein traffic is an intracellular target in alcohol toxicity. Pharmaceuticals 4:741-757
22. 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
23. Fiala JC, Spacek J, Harris KM (2007) Dendrite structure. In: Stuart G, Spruston N, Hausset (eds) Dendrites. Oxford University Press, Oxford, pp 1-41
24. Frost NA, Kerr JM, Lu HE, Blanpied TA (2010) A network of networks: cytoskeletal control of compartmentalized function within dendritic spines. Curr Opin Neurobiol 20:578-587
25. Galofré E, Ferrer I, Fábregues I, López-Tejero D (1987) Effects of prenatal ethanol exposure on dendritic spines of layer-V pyramidal neurons in the somatosensory cortex of the rat. J Neurol Sci 81:185-195
26. Gass JT, Olive MF (2012) Neurochemical and neurostructural plasticity in alcoholism. ACS Chem Neurosci 3:494-504
27. Gl Ellman, Callaway E (1961) Erythrocyte cholinesterase-levels in mental patients. Nature 23(192):1216
28. Gogolla N, Galimberti I, Deguchi Y, Caroni P (2009) Wnt signaling mediates experience-related regulation of synapse numbers and mossy fiber connectivities in the adult hippocampus. Neuron 62:510-525
29. González A, Salido GM (2009) Ethanol alters the physiology of neuron-glia communication. Int Rev Neurobiol 88:167-198
30. González-Billault C, Muñoz-Llancao P, Henriquez DR, Wojnacki J, Conde C, Caceres A (2012) The role of small GTPases in neuronal morphogenesis and polarity. Cytoskeleton 69:464-485
31. González-Burgos I, Alejandre-Gómez M, Olvera-Cortés ME, Pérez-Vega MI, Evans S, Feria-Velasco A (2006) Prenatal-through- postnatal exposure to moderate levels of ethanol leads to damage on the hippocampal CA1 field of juvenile rats: a stereology and Golgi study. Neurosci Res 56:400-408
32. Goodlett C, Horn K, Zhou F (2005) Alcohol teratogenesis: mechanisms of damage and strategies for intervention. Exp Biol Med 230:394-406
33. Gu J, Firestein BL, Zheng JQ (2008) Microtubules in dendritic spine development. J Neurosc 28:12120-12124
34. Guasch R, Tomás M, Minambres R, Valles S, Renau-Piqueras J, Guerri C (2003) RhoA and lysophosphatidic acid are involved in the actin cytoskeleton reorganization of astrocytes exposed to ethanol. J Neurosci Res 72:487-502
35. 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
36. Guerri C, Bazinet A, Riley EP (2009) Foetal alcohol spectrum disorders and alterations in brain and behaviour. Alcohol Alcohol 44:108-114
37. Hamilton DA, Akers KG, Rice JP, Johnson TE, Candelaria-Cook FT, Maes LI, Rosenberg M, Valenzuela CF, Savage DD (2010a) Prenatal exposure to moderate levels of ethanol alters social behavior in adult rats: relationship to structural plasticity and immediate early gene expression in frontal cortex. Behav Brain Res 207:290-304
38. Hamilton GF, Whitcher LT, Klintsova AY (2010b) Postnatal binge-like alcohol exposure decreases dendritic complexity while increasing the density of mature spines in mPFC layer II/III pyramidal neurons. Synapse 64:127-135
39. Hering H, Sheng M (2001) Dendritic spines: structure, dynamics and regulation. Nat Rev Neurosci 2:880-888
40. Holcman D, Schuss Z (2011) Diffusion laws in dendritic spines. J Math Neurosci 1:10
41. Hotulainen P, Hoogenraad CC (2010) Actin in dendritic spines: connecting dynamics to function. J Cell Biol 189:619-629
42. Hugel S, Abegg M, de Paola V, Caroni P, Gähwiler BH, McKinney RA (2009) Dendritic spine morphology determines membrane-associated protein exchange between dendritic shafts and spine heads. Cereb Cortex 19:697-702
43. Kasai H, Matsuzaki M, Noguchi J, Yasumatsu N, Nakahara H (2003) Structure-stability-function relationships of dendritic spines. Trends Neurosci 26:360-368
44. Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, Noguchi J (2010) Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci 33:121-129
45. Kho CG (2006) Rho GTPases and their regulators in neuronal functions and development. Neurosignals 15:228-237
46. 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
47. Korobova F, Svitkina T (2010) Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Mol Biol Cell 21:165-176
48. Lin WH, Webb DJ (2009) Actin and Actin-binding proteins: masters of dendritic spine formation, morphology, and function. Open Neurosci J 3:54-66
49. Loureiro SO, Heimfarth L, Reis K, Wild L, Andrade C, Costa Rodrigues Guma FT, Goncalves CA, Pessoa-Pureur R (2011) Acute ethanol exposure disrupts actin cytoskeleton and generates reactive oxygen species in c6 cells. Toxicol In Vitro 25:28-36
50. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
51. 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
52. 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
53. Martínez SE, Egea G (2007) Novel molecular targets for the prevention of fetal alcohol syndrome. Recent Pat. CNS Drug Discov 2:23-35
54. Martínez SE, Lázaro-Dieguez F, Selva J, Calvo F, Piqueras J, Crespo P, Claro E, Egea G (2007) Lysophosphatidic acid rescues RhoA activation and phosphoinositides levels in astrocytes exposed to ethanol. J Neurochem 102:1044-1052
55. 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
56. Moore FB, Baleja JD (2012) Molecular remodeling mechanisms of the neural somatodendritic compartment. Biochim Biophys Acta 1283:1720-1730
57. Newey SE, Velamoor V, Govek EE, Van Aelst L (2005) Rho GTPases, dendritic structure, and mental retardation. J Neurobiol 64:58-74
58. Nwabuisi-Heath E, Ladu MJ, Yu C (2012) Simultaneous analysis of dendritic spine density, morphology and excitatory glutamate receptors during neuron maturation in vitro by quantitative immunocytochemistry. J Neurosci Methods 207:137-147
59. Okabe S (2007) Molecular anatomy of the postsynaptic density. Moll Cell Neurosci 34:503-518
60. Okamoto K, Hayashi Y (2006) Visualization of F-actin and G-actin equilibrium using fluorescence resonance energy transfer (FRET) in cultured cells and neurons in slices. Nat Protoc 21:911-919
61. Okamoto K, Nagai T, Miyawaki A, Hayashi Y (2004) Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat Neurosci 7:1104-1112
62. Okubo-Suzuki R, Okada D, Sekiguchi M, Inokuchi K (2008) Synaptopodin maintains the neural activity-dependent enlargement of dendritic spines in hippocampal neurons. Mol Cell Neurosci 38:266-276
63. Olivera S, Rodriguez-Ithurralde D, Henley JM (2003) Acetylcholinesterase promotes neurite elongation, synapse formation, and surface expression of AMPA receptors in hippocampal neurones. Mol Cell Neurosci 23:96-106
64. Papa M, Bundman MC, Greenberger V, Segal M (1995) Morphological analysis of dendritic spine development in primary cultures of hippocampal neurons. J Neurosci 15:1-11
65. Peebles CL, Yoo J, Thwin MT, Palop JJ, Noebels JL, Finkbeiner S (2010) Arc regulates spine morphology and maintains network stability in vivo. Proc Natl Acad Sci USA 107:18173-18178
66. Penzes P, Cahill ME (2012) Deconstructing signal transduction pathways that regulate the actin cytoskeleton in dendritic spines. Cytoskeleton 69:426-441
67. Penzes P, Jones KA (2008) Dendritic spine dynamics: a key role for kalirin-7. Trends Neurosci 31:419-427
68. Penzes P, Cahill ME, Jones KA, Van Leeuwen JE, Woolfrey KM (2011) Dendritic spine pathology in neuropsychiatric disorders. Nat Neurosci 14:285-293
69. Pontrello CG, Ethell IM (2009) Accelerators, brakes, and gears of actin dynamics in dendritic spines. Open Neurosci J 3:67-86
70. Renner M, Specht CG, Triller A (2008) Molecular dynamics of postsynaptic receptors and scaffold proteins. Curr Opin Neurobiol 18:532-540
71. Rice JP, Suggs LE, Lusk AV, Parker MO, Candelaria-Cook FT, Akers KG, Savage DD, Hamilton DA (2012) Effects of exposure to moderate levels of ethanol during prenatal brain development on dendritic length, branching, and spine density in the nucleus accumbens and dorsal striatum of adult rats. Alcohol 46:577-584
72. Robinson TE, Kolb B (2004) Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology Suppl 1:33-46
73. Rochefort NL, Konnerth A (2012) Dendritic spines: from structure to in vivo function. EMBO Rep 13:699-708
74. 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
75. Sala C, Cambianica I, Rossi F (2008) Molecular mechanisms of dendritic spine development and maintenance. Acta Neurobiol Exp 68:289-304
76. Segal M, Vlachos A, Korkotian E (2010) The spine apparatus, synaptopodin, and dendritic spine plasticity. Neuroscientist 16:125-131
77. Sekino Y, Kojima N, Shirao T (2007) Role of actin cytoskeleton in dendritic spine morphogenesis. Neurochem Int 51:92-104
78. Shen HW, Toda S, Moussawi K, Bouknight A, Zahm DS, Kalivas PW (2009) Altered dendritic spine plasticity in cocaine-withdrawn rats. J Neurosci 29:2876-2884
79. Sheng M, Hoogenraad CC (2007) The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu Rev Biochem 76:823-847
80. Sordella R, Van Aelst L (2006) Driving actin dynamics under the influence of alcohol. Cell 127:37-39
81. Soreq H, Seidman S (2001) Acetylcholinesterase new roles for an old actor. Nat Rev Neurosci 2:294-302
82. Star EN, Kwiatkowski DJ, Murthy VN (2002) Rapid turnover of actin in dendritic spines and its regulation by activity. Nat Neurosci 5:239-246
83. Tada T, Sheng M (2006) Molecular mechanisms of dendritic spine morphogenesis. Curr Opin Neurobiol 16:95-101
84. Tarelo-Acuña L, Olvera-Cortes E, Gonzalez-Burgos I (2000) Prenatal and postnatal exposure to ethanol induces changes in the shape of the dendritic spines from hippocampal CA1 pyramidal neurons of the rat. Neurosci Lett 286:13-16
85. Tcherkezian J, Lamarche-Vane N (2007) Current knowledge of the large RhoGAP family of proteins. Biol Cell 99:67-86
86. Tomás M, Lázaro-Diéguez F, Durán JM, Marín P, Renau-Piqueras J, Egea G (2003) Protective effects of lysophosphatidic acid (LPA) on chronic ethanol-induced injuries to the cytoskeleton and on glucose uptake in rat astrocytes. J Neurochem 87:220-229
87. Tomás M, Marín P, Megías L, Egea G, Renau-Piqueras J (2005) Ethanol perturbs the secretory pathway in astrocytes. Neurobiol Dis 20:773-784
88. 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
89. Urbanska M, Swiech L, Jaworski J (2012) Developmental plasticity of the dendritic compartment: focus on the cytoskeleton. Adv Exp Med Biol 970:265-284. doi: 10.1007/978-3-7091-0932-8-12
90. Valenzuela CF, Puglia MP, Zucca S (2011) Focus on: neurotransmitter systems. Alcohol Res Health 34:106-120
91. Vlachos A (2012) Synaptopodin and the spine apparatus organelle-regulators of different forms of synaptic plasticity? Ann Anat 194:317-320
92. Vlachos A, Korkotian E, Schonfeld E, Copanaki E, Deller T, Segal M (2009) Synaptopodin regulates plasticity of dendritic spines in hippocampal neurons. J Neurosci 29:1017-1033
93. Yuste R, Bonhoeffer T (2004) Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat Rev Neurosci 5:24-34
94. Zhang H, Webb DJ, Asmussen H, Niu S, Horwitz AF (2005) A GIT1/PIX/Rac/PAK signaling module regulates spine morphogenesis and synapse formation through MLC. J Neurosci 25:3379-3388
95. 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
96. Zhou FC, Anthony B, Dunn KW, Lindquist WB, Xu ZC, Deng P (2007) Chronic alcohol drinking alters neuronal dendritic spines in the brain reward center nucleus accumbens. Brain Res 1134:148-161