Prenatal ethanol exposure stimulates neurogenesis in hypothalamic and limbic peptide systems: Possible mechanism for offspring ethanol overconsumption

Neuroscience

Volumn 222, Issue , 2012, Pages 417-428

  Chang, G Q ^a   Karatayev, O ^a   Liang, S C ^a   Barson, J R ^a   Leibowitz, S F ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Hypothalamus; Neurogenesis; Nucleus accumbens; Orexigenic peptides; Prenatal ethanol

Indexed keywords

ALCOHOL; BROXURIDINE; CELL MARKER; ENKEPHALIN; GALANIN; NEURON SPECIFIC NUCLEAR PROTEIN; OREXIN;

ALCOHOL CONSUMPTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL LABELING; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; IN SITU HYBRIDIZATION; LATERAL HYPOTHALAMUS; LIMBIC SYSTEM; MALE; NERVE CELL NECROSIS; NERVE CELL STIMULATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEUS ACCUMBENS; PHENOTYPE; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REAL TIME POLYMERASE CHAIN REACTION;

ALCOHOLISM; ANIMALS; ANTIMETABOLITES; BRAIN; BROMODEOXYURIDINE; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DIGOXIGENIN; ENKEPHALINS; ETHANOL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GALANIN; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIMBIC SYSTEM; NEUROPEPTIDES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84865633695     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.05.066     Document Type: Article

References (57)

1. Ahmed I.I., Shryne J.E., Gorski R.A., Branch B.J., Taylor A.N. Prenatal ethanol and the prepubertal sexually dimorphic nucleus of the preoptic area. Physiol Behav 1991, 49:427-432.
2. Alati R., Al Mamun A., Williams G.M., O'Callaghan M., Najman J.M., Bor W. In utero alcohol exposure and prediction of alcohol disorders in early adulthood: a birth cohort study. Arch Gen Psychiatry 2006, 63:1009-1016.
3. Altman J., Bayer S.A. Development of the diencephalon in the rat. I. Autoradiographic study of the time of origin and settling patterns of neurons of the hypothalamus. J Comp Neurol 1978, 182:945-971.
4. Arias C., Chotro M.G. Increased palatability of ethanol after prenatal ethanol exposure is mediated by the opioid system. Pharmacol Biochem Behav 2005, 82:434-442.
5. Barson JR, Fagan SE, Chang GQ, Leibowitz SF (2012) Neurochemical heterogeneity of rats predicted by different measures to be high ethanol consumers. Alcohol Clin Exp Res, [Epub ahead of print].
6. Barson J.R., Morganstern I., Leibowitz S.F. Galanin and consummatory behavior: special relationship with dietary fat, alcohol and circulating lipids. EXS 2010, 102:87-111.
7. Barson J.R., Morganstern I., Leibowitz S.F. Similarities in hypothalamic and mesocorticolimbic circuits regulating the overconsumption of food and alcohol. Physiol Behav 2011, 104:128-137.
8. Bayer S.A., Altman J., Russo R.J., Zhang X. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 1993, 14:83-144.
9. Bayerlein K., Kraus T., Leinonen I., Pilniok D., Rotter A., Hofner B., Schwitulla J., Sperling W., Kornhuber J., Biermann T. Orexin A expression and promoter methylation in patients with alcohol dependence comparing acute and protracted withdrawal. Alcohol (Fayetteville, NY) 2011, 45:541-547.
10. Boehme F., Gil-Mohapel J., Cox A., Patten A., Giles E., Brocardo P.S., Christie B.R. Voluntary exercise induces adult hippocampal neurogenesis and BDNF expression in a rodent model of fetal alcohol spectrum disorders. Eur J Neurosci 2011, 33:1799-1811.
11. Brocardo P.S., Boehme F., Patten A., Cox A., Gil-Mohapel J., Christie B.R. Anxiety- and depression-like behaviors are accompanied by an increase in oxidative stress in a rat model of fetal alcohol spectrum disorders: protective effects of voluntary physical exercise. Neuropharmacology 2011, 62:1607-1618.
12. Chang G.Q., Barson J.R., Karatayev O., Chang S.Y., Chen Y.W., Leibowitz S.F. Effect of chronic ethanol on enkephalin in the hypothalamus and extra-hypothalamic areas. Alcohol Clin Exp Res 2010, 34:761-770.
13. Chang G.Q., Gaysinskaya V., Karatayev O., Leibowitz S.F. Maternal high-fat diet and fetal programming: increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J Neurosci 2008, 28:12107-12119.
14. Chang G.Q., Karatayev O., Ahsan R., Gaysinskaya V., Marwil Z., Leibowitz S.F. Dietary fat stimulates endogenous enkephalin and dynorphin in the paraventricular nucleus: role of circulating triglycerides. Am J Physiol Endocrinol Metab 2007, 292:E561-E570.
15. Chotro M.G., Arias C., Laviola G. Increased ethanol intake after prenatal ethanol exposure: studies with animals. Neurosci Biobehav Rev 2007, 31:181-191.
16. de Gortari P., Mendez M., Rodriguez-Keller I., Perez-Martinez L., Joseph-Bravob P. Acute ethanol administration induces changes in TRH and proenkephalin expression in hypothalamic and limbic regions of rat brain. Neurochem Int 2000, 37:483-496.
17. De Witte P. The role of neurotransmitters in alcohol dependence. animal research. Alcohol Alcohol 1996, 1:13-16.
18. Dembele K., Yao X.H., Chen L., Nyomba B.L. Intrauterine ethanol exposure results in hypothalamic oxidative stress and neuroendocrine alterations in adult rat offspring. Am J Physiol 2006, 291:R796-R802.
19. Di Chiara G. Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res 2002, 137:75-114.
20. Druse M.J., Hao H.L., Eriksen J.L. In utero ethanol exposure increases proenkephalin, a precursor of a neuropeptide that is inhibitory to neuronal growth. Alcohol Clin Exp Res 1999, 23:1519-1527.
21. Emanuele N.V., LaPaglia N., Steiner J., Kirsteins L., Emanuele M.A. Effect of chronic ethanol exposure on female rat reproductive cyclicity and hormone secretion. Alcohol Clin Exp Res 2001, 25:1025-1029.
22. Fakoya F.A., Caxton-Martins E.A. Neocortical neurodegeneration in young adult Wistar rats prenatally exposed to ethanol. Neurotoxicol Teratol 2006, 28:229-237.
23. Fowler C.D., Liu Y., Wang Z. Estrogen and adult neurogenesis in the amygdala and hypothalamus. Brain Res Rev 2008, 57:342-351.
24. Gil-Mohapel J., Boehme F., Kainer L., Christie B.R. Hippocampal cell loss and neurogenesis after fetal alcohol exposure: insights from different rodent models. Brain Res Rev 2010, 64:283-303.
25. Gonzalez-Burgos I., Alejandre-Gomez M., Olvera-Cortes M.E., Perez-Vega M.I., Evans S., Feria-Velasco A. 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 2006, 56:400-408.
26. Heaton M.B., Paiva M., Madorsky I., Mayer J., Moore D.B. Effects of ethanol on neurotrophic factors, apoptosis-related proteins, endogenous antioxidants, and reactive oxygen species in neonatal striatum: relationship to periods of vulnerability. Brain Res 2003, 140:237-252.
27. Ifft J.D. An autoradiographic study of the time of final division of neurons in rat hypothalamic nuclei. J Comp Neurol 1972, 144:193-204.
28. Jamensky N.T., Gianoulakis C. Comparison of the proopiomelanocortin and proenkephalin opioid peptide systems in brain regions of the alcohol-preferring C57BL/6 and alcohol-avoiding DBA/2 mice. Alcohol (Fayetteville, NY) 1999, 18:177-187.
29. Lawrence R.C., Otero N.K., Kelly S.J. Selective effects of perinatal ethanol exposure in medial prefrontal cortex and nucleus accumbens. Neurotoxicol Teratol 2012, 34:128-135.
30. Li Y., van den Pol A.N. Direct and indirect inhibition by catecholamines of hypocretin/orexin neurons. J Neurosci 2005, 25:173-183.
31. Livy D.J., Maier Se., West J.R. Fetal alcohol exposure and temporal vulnerability: effects of binge-like alcohol exposure on the ventrolateral nucleus of the thalamus. Alcohol Clin Exp Res 2001, 25:774-780.
32. Livy D.J., Miller E.K., Maier S.E., West J.R. Fetal alcohol exposure and temporal vulnerability: effects of binge-like alcohol exposure on the developing rat hippocampus. Neurotoxicol Teratol 2003, 25:447-458.
33. Lugo J.N., Wilson M.A., Kelly S.J. Perinatal ethanol exposure alters met-enkephalin levels of male and female rats. Neurotoxicol Teratol 2006, 28:238-244.
34. Maekawa M., Takashima N., Matsumata M., Ikegami S., Kontani M., Hara Y., Kawashima H., Owada Y., Kiso Y., Yoshikawa T., Inokuchi K., Osumi N. Arachidonic acid drives postnatal neurogenesis and elicits a beneficial effect on prepulse inhibition, a biological trait of psychiatric illnesses. PLoS One 2009, 4:e5085.
35. Maier S.E., West J.R. Regional differences in cell loss associated with binge-like alcohol exposure during the first two trimesters equivalent in the rat. Alcohol (Fayetteville, NY) 2001, 23:49-57.
36. Marinelli P.W., Kiianmaa K., Gianoulakis C. Opioid propeptide mRNA content and receptor density in the brains of AA and ANA rats. Life Sci 2000, 66:1915-1927.
37. McGivern R.F., Ervin M.G., McGeary J., Somes C., Handa R.J. Prenatal ethanol exposure induces a sexually dimorphic effect on daily water consumption in prepubertal and adult rats. Alcohol Clin Exp Res 1998, 22:868-875.
38. Miller M.W. Effect of pre- or postnatal exposure to ethanol on the total number of neurons in the principal sensory nucleus of the trigeminal nerve: cell proliferation and neuronal death. Alcohol Clin Exp Res 1995, 19:1359-1363.
39. Miller M.W. Generation of neurons in the rat dentate gyrus and hippocampus: effects of prenatal and postnatal treatment with ethanol. Alcohol Clin Exp Res 1995, 19:1500-1509.
40. Mooney S.M., Miller M.W. Prenatal exposure to ethanol affects postnatal neurogenesis in thalamus. Exp Neurol 2010, 223:566-573.
41. Morganstern I., Barson J.R., Leibowitz S.F. Regulation of drug and palatable food overconsumption by similar Peptide systems. Curr Drug Abuse Rev 2011, 4:163-173.
42. Morganstern I., Chang G.Q., Barson J.R., Ye Z., Karatayev O., Leibowitz S.F. Differential effects of acute and chronic ethanol exposure on orexin expression in the perifornical lateral hypothalamus. Alcohol Clin Exp Res 2010, 34:886-896.
43. Morganstern I., Chang G.Q., Karatayev O., Leibowitz S.F. Increased orexin and melanin-concentrating hormone expression in the perifornical lateral hypothalamus of rats prone to overconsuming a fat-rich diet. Pharmacol Biochem Behav 2010, 96:413-422.
44. Oliva J.M., Manzanares J. Gene transcription alterations associated with decrease of ethanol intake induced by naltrexone in the brain of Wistar rats. Neuropsychopharmacology 2007, 32:1358-1369.
45. Parab S., Nankova B.B., La Gamma E.F. Differential regulation of the tyrosine hydroxylase and enkephalin neuropeptide transmitter genes in rat PC12 cells by short chain fatty acids: concentration-dependent effects on transcription and RNA stability. Brain Res 2007, 1132:42-50.
46. Qiang M., Wang M.W., Elberger A.J. Second trimester prenatal alcohol exposure alters development of rat corpus callosum. Neurotoxicol Teratol 2002, 24:719-732.
47. Ramos A.J., Evrard S.G., Tagliaferro P., Tricarico M.V., Brusco A. Effects of chronic maternal ethanol exposure on hippocampal and striatal morphology in offspring. Ann N Y Acad Sci 2002, 965:343-353.
48. Reagan L.P., Rosell D.R., Wood G.E., Spedding M., Munoz C., Rothstein J., McEwen B.S. Chronic restraint stress up-regulates GLT-1 mRNA and protein expression in the rat hippocampus: reversal by tianeptine. Proc Natl Acad Sci U S A 2004, 101:2179-2184.
49. Rubert G., Minana R., Pascual M., Guerri C. Ethanol exposure during embryogenesis decreases the radial glial progenitorpool and affects the generation of neurons and astrocytes. J Neurosci Res 2006, 84:483-496.
50. Rudeen P.K. Reduction of the volume of the sexually dimorphic nucleus of the preoptic area by in utero ethanol exposure in male rats. Neurosci Lett 1986, 72:363-368.
51. Schaffer D.V., Gage F.H. Neurogenesis and neuroadaptation. NeuroMol Med 2004, 5:1-9.
52. Sherwood N.M., Timiras P.S. A sterotaxic atlas of the developing rat brain 1970, University of California, Los Angeles.
53. Steinberg G.R., Watt M.J., Fam B.C., Proietto J., Andrikopoulos S., Allen A.M., Febbraio M.A., Kemp B.E. Ciliary neurotrophic factor suppresses hypothalamic AMP-kinase signaling in leptin-resistant obese mice. Endocrinology 2006, 147:3906-3914.
54. Tabakoff B., Saba L., Printz M., Flodman P., Hodgkinson C., Goldman D., Koob G., Richardson H.N., Kechris K., Bell R.L., Hubner N., Heinig M., Pravenec M., Mangion J., Legault L., Dongier M., Conigrave K.M., Whitfield J.B., Saunders J., Grant B., Hoffman P.L., State WISo, Trait Markers of A Genetical genomic determinants of alcohol consumption in rats and humans. BMC Biol 2009, 7:70.
55. Uban K.A., Sliwowska J.H., Lieblich S., Ellis L.A., Yu W.K., Weinberg J., Galea L.A. Prenatal alcohol exposure reduces the proportion of newly produced neurons and glia in the dentate gyrus of the hippocampus in female rats. Horm Behav 2010, 58:835-843.
56. Vengeliene V., Bilbao A., Molander A., Spanagel R. Neuropharmacology of alcohol addiction. Br J Pharmacol 2008, 154:299-315.
57. Xie X., Crowder T.L., Yamanaka A., Morairty S.R., Lewinter R.D., Sakurai T., Kilduff T.S. GABA(B) receptor-mediated modulation of hypocretin/orexin neurones in mouse hypothalamus. J Physiol 2006, 574:399-414.