Opposing Actions of Ethanol and Nicotine on MicroRNAs are Mediated by Nicotinic Acetylcholine Receptors in Fetal Cerebral Cortical-Derived Neural Progenitor Cells

Alcoholism: Clinical and Experimental Research

Volumn 36, Issue 10, 2012, Pages 1669-1677

  Balaraman, Sridevi ^a   Winzer Serhan, Ursula H ^a   Miranda, Rajesh C ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

Fetal alcohol spectrum disorders; miR 140 3p; miR 153; miR 21; miR 335; miR 9; Neural stem cells; Nicotinic acetylcholine receptors; Prenatal nicotine exposure

Indexed keywords

ALCOHOL; MECAMYLAMINE; MICRORNA; MICRORNA 140 3P; MICRORNA 153; MICRORNA 21; MICRORNA 335; MICRORNA 9; NICOTINE; NICOTINIC RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; FETUS; FETUS CELL; FETUS NEURAL STEM CELL; GENETIC TRANSCRIPTION; GESTATIONAL AGE; MOUSE; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOKING;

ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHANOL; FEMALE; FETAL STEM CELLS; MICE; MICE, INBRED C57BL; MICRORNAS; NEURAL STEM CELLS; NICOTINE; PREGNANCY; RECEPTORS, NICOTINIC;

MURINAE;

EID: 84866973222     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2012.01793.x     Document Type: Article

References (50)

1. Abel EL (1984) Prenatal effects of alcohol. Drug Alcohol Depend 14:1-10.
2. Adachi J, Mizoi Y, Fukunaga T, Ogawa Y, Ueno Y, Imamichi H (1991) Degrees of alcohol intoxication in 117 hospitalized cases. J Stud Alcohol 52:448-453.
3. Ambros V (2004) The functions of animal microRNAs. Nature 431:350-355.
4. Atluri P, Fleck MW, Shen Q, Mah SJ, Stadfelt D, Barnes W, Goderie SK, Temple S, Schneider AS (2001) Functional nicotinic acetylcholine receptor expression in stem and progenitor cells of the early embryonic mouse cerebral cortex. Dev Biol 240:143-156.
5. Bayer S, Altman J, Russo R, Zhang X (1993) Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14:83-144.
6. Blomqvist O, Engel JA, Nissbrandt H, Soderpalm B (1993) The mesolimbic dopamine-activating properties of ethanol are antagonized by mecamylamine. Eur J Pharmacol 249:207-213.
7. Bourguignon LY, Spevak CC, Wong G, Xia W, Gilad E (2009) Hyaluronan-CD44 interaction with protein kinase C(epsilon) promotes oncogenic signaling by the stem cell marker Nanog and the Production of microRNA-21, leading to down-regulation of the tumor suppressor protein PDCD4, anti-apoptosis, and chemotherapy resistance in breast tumor cells. J Biol Chem 284:26533-26546.
8. Broide RS, O'Connor LT, Smith MA, Smith JA, Leslie FM (1995) Developmental expression of alpha 7 neuronal nicotinic receptor messenger RNA in rat sensory cortex and thalamus. Neuroscience 67:83-94.
9. Buccafusco JJ, Beach JW, Terry AV Jr (2009) Desensitization of nicotinic acetylcholine receptors as a strategy for drug development. J Pharmacol Exp Ther 328:364-370.
10. Camarillo C, Kumar LS, Bake S, Sohrabji F, Miranda RC (2007) Ethanol regulates angiogenic cytokines during neural development: evidence from an in vitro model of mitogen-withdrawal-induced cerebral cortical neuroepithelial differentiation. Alcohol Clin Exp Res 31:324-335.
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. Chen WJ, Parnell SE, West JR (1998) Neonatal alcohol and nicotine exposure limits brain growth and depletes cerebellar Purkinje cells. Alcohol 15:33-41.
13. Chen WJ, Parnell SE, West JR (1999) Effects of alcohol and nicotine on developing olfactory bulb: loss of mitral cells and alterations in neurotransmitter levels. Alcohol Clin Exp Res 23:18-25.
14. Falugi C, Prestipino G (1989) Localization of putative nicotinic cholinoreceptors in the early development of Paracentrotus lividus. Cell Mol Biol 35:147-161.
15. Fenster CP, Rains MF, Noerager B, Quick MW, Lester RA (1997) Influence of subunit composition on desensitization of neuronal acetylcholine receptors at low concentrations of nicotine. J Neurosci 17:5747-5759.
16. Gottesfeld Z, Morgan B, Perez-Polo JR (1990) Prenatal alcohol exposure alters the development of sympathetic synaptic components and of nerve growth factor receptor expression selectivity in lymphoid organs. J Neurosci Res 26:308-316.
17. Guo Y, Chen Y, Carreon S, Qiang M (2011) Chronic intermittent ethanol exposure and its removal induce a different miRNA expression pattern in primary cortical neuronal cultures. Alcohol Clin Exp Res doi: 10.1111/j.1530-0277.2011.01689.x[Epub ahead of print].
18. Huang W, Li MD (2009) Nicotine modulates expression of miR-140*, which targets the 3′-untranslated region of dynamin 1 gene (Dnm1). Int J Neuropsychopharmacol 12:537-546.
19. Kotkoskie LA, Norton S (1989) Morphometric analysis of developing rat cerebral cortex following acute prenatal ethanol exposure. Exp Neurol 106:283-288.
20. Kuryatov A, Luo J, Cooper J, Lindstrom J (2005) Nicotine acts as a pharmacological chaperone to up-regulate human alpha4beta2 acetylcholine receptors. Mol Pharmacol 68:1839-1851.
21. Leucht C, Stigloher C, Wizenmann A, Klafke R, Folchert A, Bally-Cuif L(2008) MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nat Neurosci 11:641-648.
22. Lopez-Hernandez GY, Sanchez-Padilla J, Ortiz-Acevedo A, Lizardi-Ortiz J, Salas-Vincenty J, Rojas LV, Lasalde-Dominicci JA (2004) Nicotine-induced up-regulation and desensitization of alpha4beta2 neuronal nicotinic receptors depend on subunit ratio. J Biol Chem 279:38007-38015.
23. 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.
24. Miller M (1989) Effects of prenatal exposure to ethanol on neocortical development: II. Cell proliferation in the ventricular and subventricular zones of the rat. J Comp Neurol 287:326-338.
25. Miller MW (1993) Migration of cortical neurons is altered by gestational exposure to ethanol. Alcohol Clin Exp Res 17:304-314.
26. Miller MW (1996) Limited ethanol exposure selectively alters the proliferation of precursor cells in the cerebral cortex. Alcohol Clin Exp Res 20:139-143.
27. Miranda RC, Pietrzykowski AZ, Tang Y, Sathyan P, Mayfield D, Keshavarzian A, Sampson W, Hereld D (2010) MicroRNAs: master regulators of ethanol abuse and toxicity? Alcohol Clin Exp Res 34:575-587.
28. Miranda RC, Santillano DR, Camarillo C, Dohrman D (2008) Modeling the impact of alcohol on cortical development in a dish: strategies from mapping neural stem cell fate. Methods Mol Biol 447:151-168.
29. Mooney SM, Siegenthaler JA, Miller MW (2004) Ethanol induces heterotopias in organotypic cultures of rat cerebral cortex. Cereb Cortex 14:1071-1080.
30. Ostenfeld T, Svendsen CN (2004) Requirement for neurogenesis to proceed through the division of neuronal progenitors following differentiation of epidermal growth factor and fibroblast growth factor-2-responsive human neural stem cells. Stem Cells 22:798-811.
31. Perera RJ, Ray A (2007) MicroRNAs in the search for understanding human diseases. BioDrugs 21:97-104.
32. Pietrzykowski AZ, Friesen RM, Martin GE, Puig SI, Nowak CL, Wynne PM, Siegelmann HT, Treistman SN (2008) Posttranscriptional regulation of BK channel splice variant stability by miR-9 underlies neuroadaptation to alcohol. Neuron 59:274-287.
33. Prock TL, Miranda RC (2007) Embryonic cerebral cortical progenitors are resistant to apoptosis, but increase expression of suicide receptor DISC-complex genes and suppress autophagy following ethanol exposure. Alcohol Clin Exp Res 31:694-703.
34. Quick MW, Lester RA (2002) Desensitization of neuronal nicotinic receptors. J Neurobiol 53:457-478.
35. Richards CI, Srinivasan R, Xiao C, Mackey ED, Miwa JM, Lester HA (2011) Trafficking of alpha4* nicotinic receptors revealed by superecliptic phluorin: effects of a beta4 amyotrophic lateral sclerosis-associated mutation and chronic exposure to nicotine. J Biol Chem 286:31241-31249.
36. Robles N, Sabria J (2008) Effects of moderate chronic ethanol consumption on hippocampal nicotinic receptors and associative learning. Neurobiol Learn Mem 89:497-503.
37. Russell MA, Jarvis M, Iyer R, Feyerabend C (1980) Relation of nicotine yield of cigarettes to blood nicotine concentrations in smokers. Br Med J 280:972-976.
38. Sallette J, Bohler S, Benoit P, Soudant M, Pons S, Le Novère N, Changeux JP, Corringer PJ (2004) An extracellular protein microdomain controls up-regulation of neuronal nicotinic acetylcholine receptors by nicotine. J Biol Chem 279:18767-18775.
39. SAMHSA (2009) The NSDUH Report: Substance Use among Women During Pregnancy and Following Childbirth, vol NSDUH09-0521. Substance Abuse and Mental Health Services Administration, Office of Applied Studies, Rockville, MD.
40. Santillano DR, Kumar LS, Prock TL, Camarillo C, Tingling JD, Miranda RC (2005) Ethanol induces cell-cycle activity and reduces stem cell diversity to alter both regenerative capacity and differentiation potential of cerebral cortical neuroepithelial precursors. BMC Neurosci 6:59.
41. Sathyan P, Golden HB, Miranda RC (2007) Competing interactions between micro-RNAs determine neural progenitor survival and proliferation after ethanol exposure: evidence from an ex vivo model of the fetal cerebral cortical neuroepithelium. J Neurosci 27:8546-8557.
42. Schraivogel D, Weinmann L, Beier D, Tabatabai G, Eichner A, Zhu JY, Anton M, Sixt M, Weller M, Beier CP, Meister G (2011) CAMTA1 is a novel tumour suppressor regulated by miR-9/9(*) in glioblastoma stem cells. EMBO J 30:4309-4322.
43. Shoaib M, Stolerman IP (1999) Plasma nicotine and cotinine levels following intravenous nicotine self-administration in rats. Psychopharmacology 143:318-321.
44. Takahashi T, Goto T, Miyama S, Nowakowski R, Caviness VJ (1999) Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J Neurosci 19:10357-10371.
45. Wang H, Sun X (2005) Desensitized nicotinic receptors in brain. Brain Res Brain Res Rev 48:420-437.
46. Wang J, Gutala R, Sun D, Ma JZ, Sheela RC, Ticku MK, Li MD (2007) Regulation of platelet-derived growth factor signaling pathway by ethanol, nicotine, or both in mouse cortical neurons. Alcohol Clin Exp Res 31:357-375.
47. Williams JM, Gandhi KK, Lu SE, Kumar S, Shen J, Foulds J, Kipen H, Benowitz NL (2010) Higher nicotine levels in schizophrenia compared with controls after smoking a single cigarette. Nicotine Tob Res 12:855-859.
48. Williams SK, Cox ET, McMurray MS, Fay EE, Jarrett TM, Walker CH, Overstreet DH, Johns JM (2009) Simultaneous prenatal ethanol and nicotine exposure affect ethanol consumption, ethanol preference and oxytocin receptor binding in adolescent and adult rats. Neurotoxicol Teratol 31:291-302.
49. Winzer-Serhan UH (2008) Long-term consequences of maternal smoking and developmental chronic nicotine exposure. Front Biosci 13:636-649.
50. Zoli M, Le Novere N, Hill JA Jr, Changeux JP (1995) Developmental regulation of nicotinic ACh receptor subunit mRNAs in the rat central and peripheral nervous systems. J Neurosci 15(3 Pt 1):1912-1939.