Paternal alcohol exposure in mice alters brain NGF and BDNF and increases ethanol-elicited preference in male offspring

Addiction Biology

Volumn 21, Issue 4, 2016, Pages 776-787

  Ceccanti, Mauro ^a   Coccurello, Roberto ^b   Carito, Valentina ^b   Ciafrè, Stefania ^c   Ferraguti, Giampiero ^a   Giacovazzo, Giacomo ^b   Mancinelli, Rosanna ^d   Tirassa, Paola ^b   Chaldakov, George N ^e   Pascale, Esterina ^a   Ceccanti, Marco ^a   Codazzo, Claudia ^a   Fiore, Marco ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b Institute of Cell Biology and Neurobiology (IBCN) IRCCS S Lucia Foundation   (Italy)

^c INSTITUTE OF TRANSLATIONAL PHARMACOLOGY   (Italy)

^d ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^e Trakia University Medical College   (Bulgaria)

Author keywords

Ethanol intake preference; neurotrophin; paternal alcohol exposure

Indexed keywords

ALCOHOL; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; DOPAMINE TRANSPORTER; NERVE GROWTH FACTOR; NEUROTROPHIN RECEPTOR P75; PROTEIN TYROSINE KINASE A; SUCROSE;

ALCOHOL TOLERANCE; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CHILD PARENT RELATION; CONTROLLED STUDY; CORPUS STRIATUM; DRINKING BEHAVIOR; ETHANOL ELICITED PREFERENCE; FEMALE; FRONTAL CORTEX; HIPPOCAMPUS; HYPOTHALAMUS; MALE; MOUSE; NONHUMAN; OLFACTORY BULB; PATERNAL ALCOHOL EXPOSURE; PATERNAL EXPOSURE; PLACE PREFERENCE; PRIORITY JOURNAL; PROGENY; REWARD;

EID: 84975068616     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/adb.12255     Document Type: Article

References (73)

1. Abel E (2004) Paternal contribution to fetal alcohol syndrome. Addict Biol 9:127–133, discussion 135–6.
2. Abel EL (1989) Paternal and maternal alcohol consumption: effects on offspring in two strains of rats. Alcohol Clin Exp Res 13:533–541.
3. Abel EL (1991) Paternal alcohol consumption affects grooming response in rat offspring. Alcohol Fayettev N 8:21–23.
4. Abel EL (1993) Rat offspring sired by males treated with alcohol. Alcohol Fayettev N 10:237–242.
5. Abel EL (1999) What really causes FAS? Teratology 59:4–6.
6. Abel EL (2009) Fetal alcohol syndrome: same old, same old. Addiction 104:1274–1275, discussion 1279–80.
7. Abel EL, Bilitzke P (1990) Paternal alcohol exposure: paradoxical effect in mice and rats. Psychopharmacology (Berl) 100:159–164.
8. Abel EL, Dintcheff BA (1986) Effects of prenatal alcohol exposure on behavior of aged rats. Drug Alcohol Depend 16:321–330.
9. Allen SJ, Dawbarn D (2006) Clinical relevance of the neurotrophins and their receptors. Clin Sci 110:175–191.
10. Alleva E, Aloe L, Bigi S (1993) An updated role for nerve growth factor in neurobehavioural regulation of adult vertebrates. Rev Neurosci 4:41–62.
11. Aloe L (2001) Nerve growth factor and neuroimmune responses: basic and clinical observations. Arch Physiol Biochem 109:354–356.
12. Aloe L (2006) Alcohol intake during prenatal life affects neuroimmune mediators and brain neurogenesis. Ann Ist Super Sanita 42:17–21.
13. Aloe L, Alleva E, Fiore M (2002) Stress and nerve growth factor: findings in animal models and humans. Pharmacol Biochem Behav 73:159–166.
14. Aloe L, Bracci-Laudiero L, Bonini S, Manni L (1997) The expanding role of nerve growth factor: from neurotrophic activity to immunologic diseases. Allergy 52:883–894.
15. Aloe L, Bracci-Laudiero L, Tirassa P (1993) The effect of chronic ethanol intake on brain NGF level and on NGF-target tissues of adult mice. Drug Alcohol Depend 31:159–167.
16. Aloe L, Tirassa P (1992) The effect of long-term alcohol intake on brain NGF-target cells of aged rats. Alcohol 9:299–304.
17. Astley S (2004) Diagnostic Guide for Fetal Alcohol Spectrum Disorders: The 4-Digit Diagnostic Code, Third—2004, Seattle, WA: FAS Diagnostic and Prevention Network University of Washington.
18. Astley SJ (2013) Validation of the fetal alcohol spectrum disorder (FASD) 4-Digit Diagnostic Code. J Popul Ther Clin Pharmacol J Thérapeutique Popul Pharamcologie Clin 20:e416–e467.
19. Bakoyiannis I, Gkioka E, Pergialiotis V, Mastroleon I, Prodromidou A, Vlachos GD, Perrea D (2014) Fetal alcohol spectrum disorders and cognitive functions of young children. Rev Neurosci 25:631–639.
20. Bekinschtein P, Cammarota M, Medina JH (2014) BDNF and memory processing. Neuropharmacology 76 (Pt C):677–683.
21. Bielawski DM, Abel EL (1997) Acute treatment of paternal alcohol exposure produces malformations in offspring. Alcohol Fayettev N 14:397–401.
22. Bonini S, Lambiase A, Lapucci G, Properzi F, Bresciani M, Bracci Laudiero ML, Mancini MJ, Procoli A, Micera A, Sacerdoti G, Bonini S, Levi-Schaffer F, Rasi G, Aloe L (2002) Nerve growth factor and asthma. Allergy 57 (Suppl. 72):13–15.
23. Bosse KE, Mathews TA (2011) Ethanol-induced increases in extracellular dopamine are blunted in brain-derived neurotrophic factor heterozygous mice. Neurosci Lett 489:172–176.
24. Cake H, Lenzer I (1985) On effects of paternal ethanol treatment on fetal outcome. Psychol Rep 57:51–57.
25. Ceccanti M, De Nicolo S, Mancinelli R, Chaldakov G, Carito V, Ceccanti M, Laviola G, Tirassa P, Fiore M (2013) NGF and BDNF long-term variations in the thyroid, testis and adrenal glands of a mouse model of fetal alcohol spectrum disorders. Ann Ist Super Sanita 49:383–390.
26. Ceccanti M, Mancinelli R, Tirassa P, Laviola G, Rossi S, Romeo M, Fiore M (2012) Early exposure to ethanol or red wine and longlasting effects in aged mice. A study on nerve growth factor, brain-derived neurotrophic factor, hepatocyte growth factor, and vascular endothelial growth factor. Neurobiol Aging 33:359–367.
27. Chao MV (2000) Trophic factors: an evolutionary cul-de-sac or door into higher neuronal function? J Neurosci Res 59:353–355.
28. Chao MV, Hempstead BL (1995) p75 and Trk: a two-receptor system. Trends Neurosci 18:321–326.
29. Chao MV, Rajagopal R, Lee FS (2006) Neurotrophin signalling in health and disease. Clin Sci 110:167–173.
30. Cirulli F, Adriani W, Laviola G (1997) Sexual segregation in infant mice: behavioural and neuroendocrine responses to d-amphetamine administration. Psychopharmacol Berl. 134:140–152.
31. Cohen S, Levi-Montalcini R, Hamburger V (1954) A nerve growth-stimulating factor isolated from sarcomas 37 and 180. Proc Natl Acad Sci U S A 40:1014–1018.
32. Cuello AC (1983) Brain Microdissection Techniques, Chichester: Wiley.
33. De Nicolo S, Tarani L, Ceccanti M, Maldini M, Natella F, Vania A, Chaldakov GN, Fiore M (2013) Effects of olive polyphenols administration on nerve growth factor and brain-derived neurotrophic factor in the mouse brain. Nutrition 29:681–687.
34. Di Chiara G (1997) Alcohol and dopamine. Alcohol Health Res World 21:108–114.
35. Finegersh A, Homanics GE (2014) Paternal alcohol exposure reduces alcohol drinking and increases behavioral sensitivity to alcohol selectively in male offspring. PLoS ONE 9:e99078.
36. Fiore M, Chaldakov GN, Aloe L (2009a) Nerve growth factor as a signaling molecule for nerve cells and also for the neuroendocrine-immune systems. Rev Neurosci 20:133–145.
37. Fiore M, Laviola G, Aloe L, di Fausto V, Mancinelli R, Ceccanti M (2009b) Early exposure to ethanol but not red wine at the same alcohol concentration induces behavioral and brain neurotrophin alterations in young and adult mice. Neurotoxicology 30:59–71.
38. Fiore M, Mancinelli R, Aloe L, Laviola G, Sornelli F, Vitali M, Ceccanti M (2009c) Hepatocyte growth factor, vascular endothelial growth factor, glial cell-derived neurotrophic factor and nerve growth factor are differentially affected by early chronic ethanol or red wine intake. Toxicol Lett 188:208–213.
39. Freund-Michel V, Frossard N (2008) The nerve growth factor and its receptors in airway inflammatory diseases. Pharmacol Ther 117:52–76.
40. Getachew B, Hauser SR, Taylor RE, Tizabi Y (2010) Alcohol-induced depressive-like behavior is associated with cortical norepinephrine reduction. Pharmacol Biochem Behav 96:395–401.
41. Goodlett CR, Gilliam DM, Nichols JM, West JR (1989) Genetic influences on brain growth restriction induced by development exposure to alcohol. Neurotoxicology 10:321–334.
42. Goodlett CR, Horn KH (2001) Mechanisms of alcohol-induced damage to the developing nervous system. Alcohol Res Health 25:175–184.
43. He Y-Y, Zhang X-Y, Yung W-H, Zhu J-N, Wang J-J (2013) Role of BDNF in central motor structures and motor diseases. Mol Neurobiol 48:783–793.
44. Hegedus AM, Alterman AI, Tarter RE (1984) Learning achievement in sons of alcoholics. Alcohol Clin Exp Res 8:330–333.
45. Hellemans KG, Sliwowska JH, Verma P, Weinberg J (2009) Prenatal alcohol exposure: fetal programming and later life vulnerability to stress, depression and anxiety disorders. Neurosci Biobehav Rev 34:791–807.
46. Hellemans KG, Verma P, Yoon E, Yu W, Weinberg J (2008) Prenatal alcohol exposure increases vulnerability to stress and anxiety-like disorders in adulthood. Ann N Acad Sci 1144:154–175.
47. Hempstead BL (2014) Deciphering proneurotrophin actions. Handb Exp Pharmacol 220:17–32.
48. Huang EJ, Reichardt LF (2003) Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72:609–642.
49. Jamerson PA, Wulser MJ, Kimler BF (2004) Neurobehavioral effects in rat pups whose sires were exposed to alcohol. Brain Res Dev Brain Res 149:103–111.
50. Jones KL (1975) The fetal alcohol syndrome. Addict Dis 2:79–88.
51. Kim P, Choi CS, Park JH, Joo SH, Kim SY, Ko HM, Kim KC, Jeon SJ, Park SH, Han SH, Ryu JH, Cheong JH, Han JY, Ko KN, Shin CY (2014) Chronic exposure to ethanol of male mice before mating produces attention deficit hyperactivity disorder-like phenotype along with epigenetic dysregulation of dopamine transporter expression in mouse offspring. J Neurosci Res 92:658–670.
52. Koob GF (2014) Neurocircuitry of alcohol addiction: synthesis from animal models. Handb Clin Neurol. 125:33–54.
53. Levi-Montalcini R (1987) The nerve growth factor 35 years later. Science 237:1154–1162.
54. Little RE, Sing CF (1987) Father's drinking and infant birth weight: report of an association. Teratology 36:59–65.
55. Macchia T, Mancinelli R, Gentili S, Lugaresi EC, Raponi A, Taggi F (1995) Ethanol in biological fluids: headspace GC measurement. J Anal Toxicol 19:241–246.
56. Mead EA, Sarkar DK (2014) Fetal alcohol spectrum disorders and their transmission through genetic and epigenetic mechanisms. Front Genet 5:154.
57. Naassila M, Pierrefiche O, Beauge FJ, Sebire N, Daoust M (2003) Chronic ethanol exposure differentially regulates NOS1 mRNA levels depending on rat brain area. Neurosci Lett 338:221–224.
58. O'Malley KD, Nanson J (2002) Clinical implications of a link between fetal alcohol spectrum disorder and attention-deficit hyperactivity disorder. Can J Psychiatry 47:349–354.
59. Passaro KT, Little RE, Savitz DA, Noss J (1998) Effect of paternal alcohol consumption before conception on infant birth weight. ALSPAC Study Team. Avon Longitudinal Study of Pregnancy and Childhood. Teratology 57:294–301.
60. Raivio N, Miettinen P, Kiianmaa K (2014) Innate BDNF expression is associated with ethanol intake in alcohol-preferring AA and alcohol-avoiding ANA rats. Brain Res 1579:74–83.
61. Randall CL, Burling TA, Lochry EA, Sutker PB (1982) The effect of paternal alcohol consumption on fetal development in mice. Drug Alcohol Depend 9:89–95.
62. Servais L, Hourez R, Bearzatto B, Gall D, Schiffmann SN, Cheron G (2007) Purkinje cell dysfunction and alteration of long-term synaptic plasticity in fetal alcohol syndrome. Proc Natl Acad Sci USA 104:9858–9863.
63. Sofroniew MV, Howe CL, Mobley WC (2001) Nerve growth factor signaling, neuroprotection, and neural repair. Annu Rev Neurosci 24:1217–1281.
64. Söderpalm B, Ericson M (2013) Neurocircuitry involved in the development of alcohol addiction: the dopamine system and its access points. Curr Top Behav Neurosci. 13:127–161.
65. Streissguth AP, O'Malley K (2000) Neuropsychiatric implications and long-term consequences of fetal alcohol spectrum disorders. Semin Clin Neuropsychiatry 5:177–190.
66. Tabakoff B, Hoffman PL (2013) The neurobiology of alcohol consumption and alcoholism: an integrative history. Pharmacol Biochem Behav 113:20–37.
67. Tanaka H, Suzuki N, Arima M (1982) Experimental studies on the influence of male alcoholism on fetal development. Brain Dev 4:1–6.
68. Tarter RE, Jacob T, Bremer DL (1989) Specific cognitive impairment in sons of early onset alcoholics. Alcohol Clin Exp Res 13:786–789.
69. Tsai G, Gastfriend DR, Coyle JT (1995) The glutamatergic basis of human alcoholism. Am J Psychiatry 152:332–340.
70. Van der Kooij MA, Glennon JC (2007) Animal models concerning the role of dopamine in attention-deficit hyperactivity disorder. Neurosci Biobehav Rev 31:597–618.
71. Ventura R, Coccurello R, Andolina D, Latagliata EC, Zanettini C, Lampis V, Battaglia M, D'Amato FR, Moles A (2013) Postnatal aversive experience impairs sensitivity to natural rewards and increases susceptibility to negative events in adult life. Cereb Cortex 23:1606–1617.
72. Wozniak DF, Cicero TJ, Kettinger L, Meyer ER (1991) Paternal alcohol consumption in the rat impairs spatial learning performance in male offspring. Psychopharmacology (Berl) 105:289–302.
73. Yanev S, Aloe L, Fiore F, Chaldakov GN (2013) Neurotrophic and metabotrophic potential of nerve growth factor and brain-derived neurotrophic factor: linking cardiometabolic and neuropsychiatric diseases. World J Pharmacol 2:92–99.