Sustained effects of developmental exposure to ethanol on Zebrafish anxiety-like behaviour

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Baiamonte, Matteo ^a   Parker, Matthew O ^b   Vinson, Gavin P ^a   Brennan, Caroline H ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF PORTSMOUTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; DIAZEPAM; HYDROCORTISONE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; BEHAVIOR ASSESSMENT; CONTROLLED STUDY; DISEASE SEVERITY; EMBRYO; ENVIRONMENTAL EXPOSURE; EXPLORATORY BEHAVIOR TEST; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LARVAL STAGE; NONHUMAN; NOVEL TANK DIVING TEST; OPEN FIELD TEST; SCOTOTAXIS TEST; STRESS; THIGMOTAXIS TEST; ZEBRA FISH; ANIMAL; ANIMAL BEHAVIOR; ANXIETY; BLOOD; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; EMBRYOLOGY; FEMALE; GROWTH, DEVELOPMENT AND AGING; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LARVA; LOCOMOTION; MALE; MOTOR ACTIVITY; NONMAMMALIAN EMBRYO; PHYSIOLOGICAL STRESS;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; DIAZEPAM; DISEASE MODELS, ANIMAL; EMBRYO, NONMAMMALIAN; ENVIRONMENTAL EXPOSURE; ETHANOL; FEMALE; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LARVA; LOCOMOTION; MALE; MOTOR ACTIVITY; PITUITARY-ADRENAL SYSTEM; STRESS, PHYSIOLOGICAL; ZEBRAFISH;

EID: 84959450649     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0148425     Document Type: Article

References (68)

1. Paintner A, Williams AD, Burd L (2012) Fetal alcohol spectrum disorders - implications for child neurology, part 1: prenatal exposure and dosimetry. Journal of child neurology 27: 258-263. doi: 10.1177/ 0883073811428376 PMID: 22351188
2. Colangelo W, Jones DG (1982) The fetal alcohol syndrome: a review and assessment of the syndrome and its neurological sequelae. Prog Neurobiol 19: 271-314. PMID: 6134303
3. Jones KL, Smith DW (1973) Recognition of the fetal alcohol syndrome in early infancy. Lancet 302: 999-1001. PMID: 4127281
4. O'Connor MJ, Paley B (2009) Psychiatric conditions associated with prenatal alcohol exposure. Dev Disabil Res Rev 15: 225-234. doi: 10.1002/ddrr.74 PMID: 19731386
5. Evrard SG (2010) Prenatal alcohol exposure as an etiological factor in neuropsychiatric diseases of childhood, adolescence and adulthood. Vertex 21: 260-265. PMID: 21188313
6. Uban KA, Comeau WL, Ellis LA, Galea LA, Weinberg J (2013) Basal regulation of HPA and dopamine systems is altered differentially in males and females by prenatal alcohol exposure and chronic variable stress. Psychoneuroendocrinology 38: 1953-1966. doi: 10.1016/j.psyneuen.2013.02.017 PMID: 23579081
7. Mead EA, Sarkar DK (2014) Fetal alcohol spectrum disorders and their transmission through genetic and epigenetic mechanisms. Front Genet 5: 154. doi: 10.3389/fgene.2014.00154 PMID: 24917878
8. Haley DW, Handmaker NS, Lowe J (2006) Infant stress reactivity and prenatal alcohol exposure. Alcoholism, clinical and experimental research 30: 2055-2064. PMID: 17117971
9. Weinberg J, Sliwowska JH, Lan N, Hellemans KG (2008) Prenatal alcohol exposure: foetal programming, the hypothalamic-pituitary-adrenal axis and sex differences in outcome. J Neuroendocrinol 20: 470-488. doi: 10.1111/j.1365-2826.2008.01669.x PMID: 18266938
10. Taylor AN, Branch BJ, Liu SH, Kokka N (1982) Long-term effects of fetal ethanol exposure on pituitaryadrenal response to stress. Pharmacol Biochem Behav 16: 585-589. PMID: 7071091
11. Taylor AN, Branch BJ, Liu SH, Wiechmann AF, Hill MA, Kokka N (1981) Fetal exposure to ethanol enhances pituitary-adrenal and temperature responses to ethanol in adult rats. Alcohol Clin Exp Res 5: 237-246. PMID: 7018304
12. Taylor AN, Branch BJ, Van Zuylen JE, Redei E (1988) Maternal alcohol consumption and stress responsiveness in offspring. Adv Exp Med Biol 245: 311-317. PMID: 3067559
13. Weinberg J (1988) Hyperresponsiveness to stress: differential effects of prenatal ethanol on males and females. Alcohol Clin Exp Res 12: 647-652. PMID: 3067609
14. Weinberg J (1992) Prenatal ethanol effects: sex differences in offspring stress responsiveness. Alcohol 9: 219-223. PMID: 1605890
15. Osborn JA, Kim CK, Yu W, Herbert L, Weinberg J (1996) Fetal ethanol exposure alters pituitary-adrenal sensitivity to dexamethasone suppression. Psychoneuroendocrinology 21: 127-143. PMID: 8774058
16. Haley DW, Handmaker NS, Lowe J (2006) Infant stress reactivity and prenatal alcohol exposure. Alcohol Clin Exp Res 30: 2055-2064. PMID: 17117971
17. Hellemans KG, Sliwowska JH, Verma P, Weinberg J (2010) Prenatal alcohol exposure: fetal programming and later life vulnerability to stress, depression and anxiety disorders. Neurosci Biobehav Rev 34: 791-807. doi: 10.1016/j.neubiorev.2009.06.004 PMID: 19545588
18. Hellemans KG, Verma P, Yoon E, Yu WK, Young AH, Weinberg J (2010) Prenatal alcohol exposure and chronic mild stress differentially alter depressive-and anxiety-like behaviors in male and female offspring. Alcohol Clin Exp Res 34: 633-645. doi: 10.1111/j.1530-0277.2009.01132.x PMID: 20102562
19. Hellemans KGC, Verma P, Yoon E, Yu W, Weinberg J (2008) Prenatal Alcohol Exposure Increases Vulnerability to Stress and Anxiety-Like Disorders in Adulthood. Ann N Y Acad Sci 1144: 154-175. doi: 10.1196/annals.1418.016 PMID: 19076375
20. Carneiro LM, Diogenes JP, Vasconcelos SM, Aragao GF, Noronha EC, Gomes PB, et al. (2005) Behavioral and neurochemical effects on rat offspring after prenatal exposure to ethanol. Neurotoxicol Teratol 27: 585-592. PMID: 16039829
21. Slone JL, Redei EE (2002) Maternal alcohol and adrenalectomy: asynchrony of stress response and forced swim behavior. Neurotoxicol Teratol 24: 173-178. PMID: 11943505
22. Slattery DA, Cryan JF (2012) Using the rat forced swim test to assess antidepressant-like activity in rodents. Nat Protocols 7: 1009-1014. doi: 10.1038/nprot.2012.044 PMID: 22555240
23. Osborn JA, Kim CK, Steiger J, Weinberg J (1998) Prenatal ethanol exposure differentially alters behavior in males and females on the elevated plus maze. Alcohol Clin Exp Res 22: 685-696. PMID: 9622451
24. Gabriel KI, Yu CL, Osborn JA, Weinberg J (2006) Prenatal ethanol exposure alters sensitivity to the effects of corticotropin-releasing factor (CRF) on behavior in the elevated plus-maze. Psychoneuroendocrinology 31: 1046-1056. PMID: 16934947
25. Ellis FW (1966) Effect of ethanol on plasma corticosterone levels. J Pharmacol Exp Ther 153: 121-127. PMID: 4288396
26. Boyd KN, Kumar S, O'Buckley TK, Morrow AL (2010) Chronic ethanol exposure produces tolerance to elevations in neuroactive steroids: mechanisms and reversal by exogenous ACTH. Journal of neurochemistry 115: 142-152. doi: 10.1111/j.1471-4159.2010.06904.x PMID: 20633208
27. Richardson HN, Lee SY, O'Dell LE, Koob GF, Rivier CL (2008) Alcohol self-administration acutely stimulates the hypothalamic-pituitary-adrenal axis, but alcohol dependence leads to a dampened neuroendocrine state. Eur J Neurosci 28: 1641-1653. PMID: 18979677
28. Glavas MM, Ellis L, Yu WK, Weinberg J (2007) Effects of prenatal ethanol exposure on basal limbichypothalamic-pituitary-adrenal regulation: role of corticosterone. Alcoholism, clinical and experimental research 31: 1598-1610. PMID: 17760789
29. Hellemans KG, Verma P, Yoon E, Yu WK, Young AH, Weinberg J (2010) Prenatal alcohol exposure and chronic mild stress differentially alter depressive-and anxiety-like behaviors in male and female offspring. Alcoholism, clinical and experimental research 34: 633-645. doi: 10.1111/j.1530-0277.2009. 01132.x PMID: 20102562
30. Taylor AN, Branch BJ, Nelson LR, Lane LA, Poland RE (1986) Prenatal ethanol and ontogeny of pituitary-adrenal responses to ethanol and morphine. Alcohol 3: 255-259. PMID: 3755954
31. Weinberg J, Taylor AN, Gianoulakis C (1996) Fetal ethanol exposure: hypothalamic-pituitary-adrenal and beta-endorphin responses to repeated stress. Alcohol Clin Exp Res 20: 122-131. PMID: 8651441
32. Kim CK, Giberson PK, Yu W, Zoeller RT, Weinberg J (1999) Effects of prenatal ethanol exposure on hypothalamic-pituitary-adrenal responses to chronic cold stress in rats. Alcoholism, clinical and experimental research 23: 301-310. PMID: 10069560
33. Kily LJ, Cowe YC, Hussain O, Patel S, McElwaine S, Cotter FE, et al. (2008) Gene expression changes in a zebrafish model of drug dependency suggest conservation of neuro-adaptation pathways. J Exp Biol 211: 1623-1634. doi: 10.1242/jeb.014399 PMID: 18456890
34. Brennan CH, Parmar A, Kily LK, Ananthathevan A, Doshi A, Patel S (2010) Conditioned place preference models of drug-dependence and relapse to drug seeking: studies with nicotine and ethanol. In: Kalueff AV, editor. Zebrafish models in neurobehavioral research. Cambridge, UK: Cambridge University Press.
35. Collier AD, Khan KM, Caramillo EM, Mohn RS, Echevarria DJ (2014) Zebrafish and conditioned place preference: A translational model of drug reward. Progress in neuro-psychopharmacology & biological psychiatry 55: 16-25.
36. Tran S, Gerlai R (2014) Recent advances with a novel model organism: Alcohol tolerance and sensitization in zebrafish (Danio rerio). Progress in neuro-psychopharmacology & biological psychiatry 55: 87-93.
37. Parker MO, Annan LV, Kanellopoulos AH, Brock AJ, Combe FJ, Baiamonte M, et al. (2014) The utility of zebrafish to study the mechanisms by which ethanol affects social behavior and anxiety during early brain development. Prog Neuropsychopharmacol Biol Psychiatry 55: 94-100. doi: 10.1016/j.pnpbp. 2014.03.011 PMID: 24690524
38. Baiamonte M, Brennan CH, Vinson GP (2015) Sustained action of developmental ethanol exposure on the cortisol response to stress in zebrafish larvae and adults. PloS one.
39. Grossman L, Utterback E, Stewart A, Gaikwad S, Chung KM, Suciu C, et al. (2010) Characterization of behavioral and endocrine effects of LSD on zebrafish. Behavioural brain research 214: 277-284. doi: 10.1016/j.bbr.2010.05.039 PMID: 20561961
40. Maximino C, de Brito TM, da Silva Batista AW, Herculano AM, Morato S, Gouveia A Jr. (2010) Measuring anxiety in zebrafish: a critical review. Behav Brain Res 214: 157-171. doi: 10.1016/j.bbr.2010.05. 031 PMID: 20510300
41. Colwill RM, Creton R (2011) Imaging escape and avoidance behavior in zebrafish larvae. Rev Neurosci 22: 63-73. doi: 10.1515/RNS.2011.008 PMID: 21572576
42. Parker MO (2015) Adult vertebrate behavioural aquatic toxicology: reliability and validity. Aquat Toxicol.
43. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310. PMID: 8589427
44. Richendrfer H, Pelkowski SD, Colwill RM, Creton R (2012) On the edge: pharmacological evidence for anxiety-related behavior in zebrafish larvae. Behavioural brain research 228: 99-106. doi: 10.1016/j. bbr.2011.11.041 PMID: 22155488
45. Bencan Z, Sledge D, Levin ED (2009) Buspirone, chlordiazepoxide and diazepam effects in a zebrafish model of anxiety. Pharmacol Biochem Behav 94: 75-80. doi: 10.1016/j.pbb.2009.07.009 PMID: 19643124
46. Maximino C, Marques de Brito T, Dias CA, Gouveia A Jr., Morato S (2010) Scototaxis as anxiety-like behavior in fish. Nat Protoc 5: 209-216. doi: 10.1038/nprot.2009.225 PMID: 20134420
47. Lindstrom ML, Bates DM (1990) Nonlinear mixed effects models for repeated measures data. Biometrics 46: 673-687. PMID: 2242409
48. Sarnyai Z, Shaham Y, Heinrichs SC (2001) The role of corticotropin-releasing factor in drug addiction. Pharmacological reviews 53: 209-243. PMID: 11356984
49. Koob GF (2010) The role of CRF and CRF-related peptides in the dark side of addiction. Brain research 1314: 3-14. doi: 10.1016/j.brainres.2009.11.008 PMID: 19912996
50. Vinson GP, Brennan CH (2013) Addiction and the adrenal cortex. Endocr Connect 2: R1-R14.
51. Vinson GP (2009) The adrenal cortex and life. Mol Cell Endocrinol 300: 2-6. doi: 10.1016/j.mce.2008. 09.008 PMID: 18840500
52. Egan RJ, Bergner CL, Hart PC, Cachat JM, Canavello PR, Elegante MF, et al. (2009) Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav Brain Res 205: 38-44. doi: 10.1016/j.bbr.2009.06.022 PMID: 19540270
53. Grossman L, Utterback E, Stewart A, Gaikwad S, Chung KM, Suciu C, et al. (2010) Characterization of behavioral and endocrine effects of LSD on zebrafish. Behav Brain Res 214: 277-284. doi: 10.1016/j. bbr.2010.05.039 PMID: 20561961
54. Stewart A, Wu N, Cachat J, Hart P, Gaikwad S, Wong K, et al. (2011) Pharmacological modulation of anxiety-like phenotypes in adult zebrafish behavioral models. Prog Neuropsychopharmacol Biol Psychiatry 35: 1421-1431. doi: 10.1016/j.pnpbp.2010.11.035 PMID: 21122812
55. Cachat J, Stewart A, Grossman L, Gaikwad S, Kadri F, Chung KM, et al. (2010) Measuring behavioral and endocrine responses to novelty stress in adult zebrafish. Nat Protoc 5: 1786-1799. doi: 10.1038/ nprot.2010.140 PMID: 21030954
56. Abreu MS, Koakoski G, Ferreira D, Oliveira TA, Rosa JG, Gusso D, et al. (2014) Diazepam and fluoxetine decrease the stress response in zebrafish. PLoS One 9: e103232. doi: 10.1371/journal.pone. 0103232 PMID: 25054216
57. Boyd KN, Kumar S, O'Buckley TK, Porcu P, Morrow AL (2010) Ethanol induction of steroidogenesis in rat adrenal and brain is dependent upon pituitary ACTH release and de novo adrenal StAR synthesis. Journal of neurochemistry 112: 784-796. doi: 10.1111/j.1471-4159.2009.06509.x PMID: 20021565
58. Marchesi C, Chiodera P, Ampollini P, Volpi R, Coiro V (1997) Beta-endorphin, adrenocorticotropic hormone and cortisol secretion in abstinent alcoholics. Psychiatry Res 72: 187-194. PMID: 9406908
59. Keedwell PA, Poon L, Papadopoulos AS, Marshall EJ, Checkley SA (2001) Salivary cortisol measurements during a medically assisted alcohol withdrawal. Addict Biol 6: 247-256. PMID: 11900603
60. Adinoff B, Ruether K, Krebaum S, Iranmanesh A, Williams MJ (2003) Increased salivary cortisol concentrations during chronic alcohol intoxication in a naturalistic clinical sample of men. Alcoholism, clinical and experimental research 27: 1420-1427. PMID: 14506402
61. Rose AK, Shaw SG, Prendergast MA, Little HJ (2010) The importance of glucocorticoids in alcohol dependence and neurotoxicity. Alcohol Clin Exp Res 34: 2011-2018. doi: 10.1111/j.1530-0277.2010. 01298.x PMID: 21087289
62. Cachat J, Canavello P, Elegante M, Bartels B, Hart P, Bergner C, et al. (2010) Modeling withdrawal syndrome in zebrafish. Behav Brain Res 208: 371-376. doi: 10.1016/j.bbr.2009.12.004 PMID: 20006651
63. Gangisetty O, Bekdash R, Maglakelidze G, Sarkar DK (2014) Fetal alcohol exposure alters proopiomelanocortin gene expression and hypothalamic-pituitary-adrenal axis function via increasing MeCP2 expression in the hypothalamus. PloS one 9: e113228. doi: 10.1371/journal.pone.0113228 PMID: 25409090
64. Fernandes Y, Gerlai R (2009) Long-term behavioral changes in response to early developmental exposure to ethanol in zebrafish. Alcohol Clin Exp Res 33: 601-609. doi: 10.1111/j.1530-0277.2008.00874. x PMID: 19183139
65. Bailey JM, Oliveri AN, Zhang C, Frazier JM, Mackinnon S, Cole GJ, et al. (2015) Long-term behavioral impairment following acute embryonic ethanol exposure in zebrafish. Neurotoxicol Teratol 48C: 1-8.
66. Hellemans KG, Verma P, Yoon E, Yu W, Weinberg J (2008) Prenatal alcohol exposure increases vulnerability to stress and anxiety-like disorders in adulthood. Annals of the New York Academy of Sciences 1144: 154-175. doi: 10.1196/annals.1418.016 PMID: 19076375
67. Schambra UB, Goldsmith J, Nunley K, Liu Y, Harirforoosh S, Schambra HM (2015) Low and moderate prenatal ethanol exposures of mice during gastrulation or neurulation delays neurobehavioral development. Neurotoxicol Teratol 51: 1-11. doi: 10.1016/j.ntt.2015.07.003 PMID: 26171567
68. Carvan MJ 3rd, Loucks E, Weber DN, Williams FE (2004) Ethanol effects on the developing zebrafish: neurobehavior and skeletal morphogenesis. Neurotoxicol Teratol 26: 757-768. PMID: 15451040