Ethanol inhibits muscarinic receptor-induced axonal growth in rat hippocampal neurons

Alcoholism: Clinical and Experimental Research

Volumn 33, Issue 11, 2009, Pages 1945-1955

  Vandemark, Kathryn L ^a   Guizzetti, Marina ^a   Giordano, Gennaro ^a   Costa, Lucio G ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF PARMA MEDICAL SCHOOL   (Italy)

Author keywords

Ethanol; Hippocampus; Muscarinic Receptors; Neurite Outgrowth; Pyramidal Cells

Indexed keywords

ALCOHOL; BETA TUBULIN; CALCIUM; CARBACHOL; FLUORESCENT DYE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MUSCARINIC RECEPTOR; PROTEIN KINASE C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY LABELING; ARTICLE; ASSAY; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CONTROLLED STUDY; CYTOTOXICITY; DENSITOMETRY; ENZYME ACTIVATION; FEMALE; FETUS; HIPPOCAMPUS; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PYRAMIDAL NERVE CELL; RAT; SPECTROPHOTOMETRY; WESTERN BLOTTING;

RATTUS;

EID: 70350507390     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2009.01032.x     Document Type: Article

References (79)

1. Anagnostaras SG, Murphy GG, Hamilton SE, Mitchell SL, Rahnama NP, Nathanson NM, Silva AJ (2003) Selective cognitive dysfunction in acetylcholine M1 muscarinic receptor mutant mice. Nat Neurosci 6 : 51 58.
2. Balduini W, Costa LG (1989) Effects of ethanol on muscarinic receptor-stimulated phosphoinositide metabolism during brain development. J Pharmacol Exp Ther 250 : 541 547.
3. Balduini W, Reno F, Costa LG, Cattabeni F (1994) Developmental neurotoxicity of ethanol: further evidence for an involvement of muscarinic receptor-stimulated phosphoinositide hydrolysis. Eur J Pharmacol 266 : 283 289.
4. Bearer CF, Swick AR, O'Riordan MA, Cheng G (1999) Ethanol inhibits L1-mediated neurite outgrowth in postnatal rat cerebellar granule cells. J Biol Chem 274 : 13264 13270.
5. Berman RF, Hannigan JH (2000) Effects of prenatal alcohol exposure on the hippocampus: spatial behavior, electrophysiology, and neuroanatomy. Hippocampus 10 : 94 110.
6. Bertrand J, Floyd RL, Weber MK (2005) Guidelines for identifying and referring persons with fetal alcohol syndrome. MMWR Recomm Rep 54 : 1 14.
7. Bingham SM, Mudd LM, Lopez TF, Montague JR (2004) Effects of ethanol on cultured embryonic neurons from the cerebral cortex of the rat. Alcohol 32 : 129 135.
8. 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.
9. Bymaster FP, McKinzie DL, Felder CC, Wess J (2003) Use of M1-M5 muscarinic receptor knockout mice as novel tools to delineate the physiological roles of the muscarinic cholinergic system. Neurochem Res 28 : 437 442. (Pubitemid 36314830)
10. Catlin MC, Guizzetti M, Costa LG (2000) Effect of ethanol on muscarinic receptor-induced calcium responses in astroglia. J Neurosci Res 60 : 345 355.
11. Chaturvedi K, Sarkar DK (2005) Role of protein kinase C-Ras-MAPK p44/42 in ethanol and transforming growth factor-[beta]3-induced basic fibroblast growth factor release from folliculostellate cells. J Pharmacol Exp Ther 314 : 1346 1352.
12. Chen S, Charness ME (2008) Ethanol inhibits neuronal differentiation by disrupting activity-dependent neuroprotective protein signaling. Proc Natl Acad Sci U S A 105 : 19962 19967.
13. Clamp PA, Lindsley TA (1998) Early events in the development of neuronal polarity in vitro are altered by ethanol. Alcohol Clin Exp Res 22 : 1277 1284.
14. Costa LG (1993) Muscarinic receptors and the developing nervous system, in Receptors in the Developing Nervous System (Zagon IS, McLaughlin PJ eds), vol 2, pp. 21 62. Chapman & Hall, London.
15. Costa LG, Guizzetti M (1999) Muscarinic cholinergic receptor signal transduction as a potential target for the developmental neurotoxicity of ethanol. Biochem Pharmacol 57 : 721 726.
16. Coulter CL, Leech RW, Schaefer GB, Scheithauer BW, Brumback RA (1993) Midline cerebral dysgenesis, dysfunction of the hypothalamic-pituitary axis, and fetal alcohol effects. Arch Neurol 50 : 771 775.
17. Davies DL, Smith DE (1981) A Golgi study of mouse hippocampal CA1 pyramidal neurons following perinatal ethanol exposure. Neurosci Lett 26 : 49 54.
18. Deitrich RA, Harris RA (1996) How much alcohol should I use in my experiments? Alcohol Clin Exp Res 20 : 1 2.
19. Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8 : 1454 1468.
20. Dunant Y, Israel M (2000) Neurotransmitter release at rapid synapses. Biochimie 82 : 289 302.
21. Fabregues I, Ferrer I, Gairi JM, Cahuana A, Giner P (1985) Effects of prenatal exposure to ethanol on the maturation of the pyramidal neurons in the cerebral cortex of the guinea-pig: a quantitative Golgi study. Neuropathol Appl Neurobiol 11 : 291 298.
22. Giordano G, White CC, Mohar I, Kavanagh TJ, Costa LG (2007) Glutathione levels modulate domoic acid induced apoptosis in mouse cerebellar granule cells. Toxicol Sci 100 : 433 444.
23. Guizzetti M, Chen J, Oram JF, Tsuji R, Dao K, Moller T, Costa LG (2007) Ethanol induces cholesterol efflux and up-regulates ATP-binding cassette cholesterol transporters in fetal astrocytes. J Biol Chem 282 : 18740 18749.
24. Guizzetti M, Costa LG (1996) Inhibition of muscarinic receptor-stimulated glial cell proliferation by ethanol. J Neurochem 67 : 2236 2245.
25. Guizzetti M, Costa LG (2000) Muscarinic receptors, protein kinase C isozymes and proliferation of astroglial cells: effects of ethanol. Neurotoxicology 21 : 1117 1121.
26. Guizzetti M, Costa LG (2002) Effect of ethanol on protein kinase C zeta and p70S6 kinase activation by carbachol: a possible mechanism for ethanol-induced inhibition of glial cell proliferation. J Neurochem 82 : 38 46.
27. Guizzetti M, Costa P, Peters J, Costa LG (1996) Acetylcholine as a mitogen: muscarinic receptor-mediated proliferation of rat astrocytes and human astrocytoma cells. Eur J Pharmacol 297 : 265 273. (Pubitemid 26066821)
28. Guizzetti M, Moller T, Costa LG (2003) Ethanol inhibits muscarinic receptor-mediated DNA synthesis and signal transduction in human fetal astrocytes. Neurosci Lett 344 : 68 70.
29. Guizzetti M, Moore NH, Giordano G, Costa LG (2008) Modulation of neuritogenesis by astrocyte muscarinic receptors. J Biol Chem 283 : 31884 31897.
30. Hammer RP, Scheibel AB (1981) Morphologic evidence for a delay of neuronal maturation in fetal alcohol exposure. Exp Neurol 74 : 587 596.
31. Heaton MB, Paiva M, Swanson DJ, Walker DW (1994) Responsiveness of cultured septal and hippocampal neurons to ethanol and neurotrophic substances. J Neurosci Res 39 : 305 318.
32. Hellmann J, Rommelspacher H, Wernicke C (2008) Long-term ethanol exposure impairs neuronal differentiation of human neuroblastoma cells involving neurotrophin-mediated intracellular signaling and in particular protein kinase C. Alcohol Clin Exp Res 33 : 1 13.
33. Hoffman EJ, Mintz CD, Wang S, McNickle DG, Salton SRJ, Benson DL (2008) Effects of ethanol on axon outgrowth and branching in developing rat cortical neurons. Neuroscience 157 : 556 565.
34. Jin K, Mao XO, Greenberg DA (2006) Vascular endothelial growth factor stimulates neurite outgrowth from cerebral cortical neurons via Rho kinase signaling. J Neurobiol 66 : 236 242.
35. Jones KL, Smith DW (1975) The fetal alcohol syndrome. Teratology 12 : 1 10.
36. Kovacs KA, Kavanagh TJ, Costa LG (1995) Ethanol inhibits muscarinic receptor-stimulated phosphoinositide metabolism and calcium mobilization in rat primary cortical cultures. Neurochem Res 20 : 939 949.
37. Lauder JM, Schambra UB (1999) Morphogenetic roles of acetylcholine. Environ Health Perspect 107 : 65 69.
38. Liesi P (1997) Ethanol-exposed central neurons fail to migrate and undergo apoptosis. J Neurosci Res 48 : 439 448.
39. Lindsley TA (2006) Effects of ethanol on mechanisms regulating neuronal process outgrowth, in Brain Development: Normal Processes and the Effects of Alcohol and Nicotine (Miller MW ed), pp. 230 244. Oxford University Press, New York.
40. Lindsley TA, Kerlin AM, Rising LJ (2003) Time-lapse analysis of ethanol's effects on axon growth in vitro. Dev Brain Res 147 : 191 199.
41. Livy DJ, Elberger AJ (2001) Effect of prenatal alcohol exposure on midsagittal commissure size in rats. Teratology 63 : 15 22.
42. 2+, Cl-, pH and membrane potential in cultured astrocytes using a fluorescence plate reader. J Neurosci Methods 91 : 73 81.
43. Mendelson B, Driskill A (1996) Ethanol exposure alters the development of serotonergic neurons in chick spinal cord. Alcohol 13 : 431 441.
44. Messing RO, Henteleff M, Park JJ (1991a) Ethanol enhances growth factor-induced neurite formation in PC12 cells. Brain Res 565 : 301 311.
45. Messing RO, Petersen PJ, Henrich CJ (1991b) Chronic ethanol exposure increases levels of protein kinase C delta and epsilon and protein kinase C-mediated phosphorylation in cultured neural cells. J Biol Chem 266 : 23428 23432.
46. Miller MW (1987) Effect of prenatal exposure to alcohol on the distribution and time of origin of corticospinal neurons in the rat. J Comp Neurol 257 : 372 382.
47. Miller MW (1997) Effects of prenatal exposure to ethanol on callosal projection neurons in rat somatosensory cortex. Brain Res 766 : 121 128.
48. Miller MW, al-Rabiai S (1994) Effects of prenatal exposure to ethanol on the number of axons in the pyramidal tract of the rat. Alcohol Clin Exp Res 18 : 346 354.
49. Miller MW, Astley SJ, Clarren SK (1999) Number of axons in the corpus callosum of the mature macaca nemestrina: increases caused by prenatal exposure to ethanol. J Comp Neurol 412 : 123 131.
50. Moreland N, La Grange L, Montoya R (2002) Impact of in utero exposure to EtOH on corpus callosum development and paw preference in rats: protective effects of silymarin. BMC Complement Altern Med 2 : 10.
51. Mount HTJ, Dreyfus CF, Black IB (1994) Muscarinic stimulation promotes cultured Purkinje cell survival: a role for acetylcholine in cerebellar development? J Neurochem 63 : 2065 2073.
52. Owen A, Bird M (1995) Acetylcholine as a regulator of neurite outgrowth and motility in cultured embryonic mouse spinal cord. Neuroreport 6 : 2269 2272.
53. Parson SH, Sojitra NM (1995) Loss of myelinated axons is specific to the central nervous system in a mouse model of the fetal alcohol syndrome. J Anat 187 (Pt 3 739 748.
54. Pascual M, Guerri C (2007) The peptide NAP promotes neuronal growth and differentiation through extracellular signal-regulated protein kinase and Akt pathways, and protects neurons co-cultured with astrocytes damaged by ethanol. J Neurochem 103 : 557 568.
55. Phillips DE (1989) Effects of limited postnatal ethanol exposure on the development of myelin and nerve fibers in rat optic nerve. Exp Neurol 103 : 90 100.
56. Pinazo-Duran MD, Renau-Piqueras J, Guerri C, Stromland K (1997) Optic nerve hypoplasia in fetal alcohol syndrome: an update. Eur J Ophthalmol 7 : 262 270.
57. Pratt OE, Doshi R (1984) Range of alcohol-induced damage in the developing central nervous system. Ciba Found Symp 105 : 142 156.
58. al-Rabiai S, Miller MW (1989) Effect of prenatal exposure to ethanol on the ultrastructure of layer V of mature rat somatosensory cortex. J Neurocytol 18 : 711 729.
59. Riley EP, Mattson SN, Sowell ER, Jernigan TL, Sobel DF, Jones KL (1995) Abnormalities of the corpus callosum in children prenatally exposed to alcohol. Alcohol Clin Exp Res 19 : 1198 1202.
60. Roivainen R, McMahon T, Messing RO (1993) Protein kinase C isozymes that mediate enhancement of neurite outgrowth by ethanol and phorbol esters in PC12 cells. Brain Res 624 : 85 93.
61. Ryan SH, Williams JK, Thomas JD (2008) Choline supplementation attenuates learning deficits associated with neonatal alcohol exposure in the rat: Effects of varying the timing of choline administration. Brain Res 1237 : 91 100.
62. Saunders DE, DiCerbo JA, Williams JR, Hannigan JH (1997) Alcohol reduces neurofilament protein levels in primary cultured hippocampal neurons. Alcohol 14 : 519 526.
63. Saunders DE, Zajac CS, Wappler NL (1995) Alcohol inhibits neurite extension and increases N-Myc and c-Myc proteins. Alcohol 12 : 475 483.
64. Sawada K, Sakata-Haga H, Komatsu S, Ohta K, Jeong YG, Fukui Y (2002) A selective loss of small-diameter myelinated optic nerve axons in rats prenatally exposed to ethanol. Congenit Anom (Kyoto) 42 : 125 129.
65. Shetty AK, Burrows RC, Phillips DE (1993) Alterations in neuronal development in the substantia nigra pars compacta following in utero ethanol exposure: immunohistochemical and Golgi studies. Neuroscience 52 : 311 322.
66. Smit M, Leng J, Klemke RL (2003) Assay for neurite outgrowth quantification. BioTechniques 35 : 254 256.
67. Smith DE, Davies DL (1990) Effect of perinatal administration of ethanol on the CA1 pyramidal cell of the hippocampus and Purkinje cell of the cerebellum: an ultrastructural survey. J Neurocytol 19 : 708 717.
68. Smith DE, Foundas A, Canale J (1986) Effect of perinatally administered ethanol on the development of the cerebellar granule cell. Exp Neurol 92 : 491 501.
69. Sowell ER, Mattson SN, Thompson PM, Jernigan TL, Riley EP, Toga AW (2001) Mapping callosal morphology and cognitive correlates: effects of heavy prenatal alcohol exposure. Neurology 57 : 235 244.
70. Stromland K (1987) Ocular involvement in the fetal alcohol syndrome. Surv Ophthalmol 31 : 277 284.
71. Swayze VW II., Johnson VP, Hanson JW, Piven J, Sato Y, Giedd JN, Mosnik D, Andreasen NC (1997) Magnetic resonance imaging of brain anomalies in fetal alcohol syndrome. Pediatrics 99 : 232 240.
72. Tang N, He M, O'Riordan MA, Farkas C, Buck K, Lemmon V, Bearer CF (2006) Ethanol inhibits L1 cell adhesion molecule activation of mitogen-activated protein kinases. J Neurochem 96 : 1480 1490.
73. VanDeMark KL, Guizzetti M, Giordano G, Costa LG (2009) The activation of M1 muscarinic receptor signaling induces neuronal differentiation in pyramidal hippocampal neurons. J Pharmacol Exp Ther 329 : 532 542.
74. Wattendorf DJ, Muenke M (2005) Fetal alcohol spectrum disorders. Am Fam Physician 72 : 279 282.
75. West JR, Hodges CA, Black AC Jr. (1981) Prenatal exposure to ethanol alters the organization of hippocampal mossy fibers in rats. Science 211 : 957 959.
76. Yanni PA, Lindsley TA (2000) Ethanol inhibits development of dendrites and synapses in rat hippocampal pyramidal neuron cultures. Brain Res Dev Brain Res 120 : 233 243.
77. Yao W-D, Rusch J, Poo M-M, Wu C-F (2000) Spontaneous acetylcholine secretion from developing growth cones of drosophila central neurons in culture: effects of cAMP-pathway mutations. J Neurosci 20 : 2626 2637.
78. Zimmerberg B, Mickus LA (1990) Sex differences in corpus callosum: influence of prenatal alcohol exposure and maternal undernutrition. Brain Res 537 : 115 122.
79. Zou J-Y, Rabin RA, Pentney RJ (1993) Ethanol enhances neurite outgrowth in primary cultures of rat cerebellar macroneurons. Brain Res Dev Brain Res 72 : 75 84.