The utility of zebrafish to study the mechanisms by which ethanol affects social behavior and anxiety during early brain development

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 55, Issue , 2014, Pages 94-100

  Parker, Matthew O ^a   Annan, Leonette V ^a,c   Kanellopoulos, Alexandros H ^a   Brock, Alistair J ^a   Combe, Fraser J ^a,d   Baiamonte, Matteo ^a   Teh, Muy Teck ^b   Brennan, Caroline H ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d MANCHESTER METROPOLITAN UNIVERSITY   (United Kingdom)

Author keywords

Moderate prenatal ethanol; Oxytocin; Serotonin; Social; Vasopressin; Zebrafish

Indexed keywords

ALCOHOL; MESSENGER RNA; OXYTOCIN; SEROTONIN; SEROTONIN 1A RECEPTOR; VASOPRESSIN; CENTRAL DEPRESSANT AGENT; ZEBRAFISH PROTEIN;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; FEMALE; GENE; GENE EXPRESSION; HRT1AA GENE; MALE; NONHUMAN; OXTR GENE; PRENATAL EXPOSURE; SLC6A4 GENE; SOCIAL BEHAVIOR; UPREGULATION; ZEBRA FISH; ANIMAL; BRAIN; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; MENTAL STRESS; METABOLISM; MOTOR ACTIVITY; PATHOPHYSIOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; ANXIETY; BRAIN; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ETHANOL; FEMALE; MALE; MOTOR ACTIVITY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, SEROTONIN, 5-HT1A; RNA, MESSENGER; SEROTONIN; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84908115946     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2014.03.011     Document Type: Article

References (61)

1. Bell R., Hobson H. Effects of pindobind 5-hydroxytryptamine1A (5-HT1A), a novel and potent 5-HT1A antagonist, on social and agonistic behaviour in male albino mice. Pharmacol Biochem Behav 1993, 46:67-72.
2. Blakely R.D., Berson H.E., Fremeau R.T., Caron M.G., Peek M.M., Prince H.K., et al. Cloning and expression of a functional serotonin transporter from rat brain. Nature 1991, 354:66-70.
3. Buske C., Gerlai R. Early embryonic ethanol exposure impairs shoaling and the dopaminergic and serotoninergic systems in adult zebrafish. Neurotoxicol Teratol 2011, 33:698-707.
4. Canli T., Lesch K.P. Long story short: the serotonin transporter in emotion regulation and social cognition. Nat Neurosci 2007, 10:1103-1109.
5. 1A agonist 8-OH-DPAT in the social interaction test in gerbils. Brain Res 2001, 915:170-175.
6. Collins L.M., Asher L., Pfeiffer D.U., Browne W.J., Nicol C.J. Clustering and synchrony in laying hens: the effect of environmental resources on social dynamics. Appl Anim Behav Sci 2011, 129:43-53.
7. Dlugos C.A., Rabin R.A. Ethanol effects on three strains of zebrafish: model system for genetic investigations. Pharmacol Biochem Behav 2003, 74:471-480.
8. Eisenhofer G., Johnson R.H. Effect of ethanol ingestion on plasma vasopressin and water balance in humans. Am J Physiol Regul Integr Comp Physiol 1982, 242:R522-R527.
9. Emiliano A.B., Cruz T., Pannoni V., Fudge J.L. The interface of oxytocin-labeled cells and serotonin transporter-containing fibers in the primate hypothalamus: a substrate for SSRIs therapeutic effects?. Neuropsychopharmacology 2007, 32:977-988.
10. Fernandes Y., Gerlai R. Long-term behavioral changes in response to early developmental exposure to ethanol in zebrafish. Alcohol Clin Exp Res 2009, 33:601-609.
11. Fuchs A.R., Wagner G. Effect of alcohol on release of oxytocin. Nature. 1963, 198:92-94.
12. Gemenetzidis E., Elena-Costea D., Parkinson E.K., Waseem A., Wan H., Teh M.-T. Induction of human epithelial stem/progenitor expansion by FOXM1. Cancer Res 2010, 70:9515-9526.
13. Giberson P.K., Weinberg J. Effects of prenatal ethanol exposure and stress in adulthood on lymphocyte populations in rats. Alcohol Clin Exp Res 1995, 19:1286-1294.
14. Guo S. Linking genes to brain, behavior and neurological diseases: what can we learn from zebrafish?. Genes Brain Behav 2004, 3:63-74.
15. Guo S., Brush J., Teraoka H., Goddard A., Wilson S.W., Mullins M.C., et al. Development of noradrenergic neurons in the zebrafish hindbrain requires BMP, FGF8, and the homeodomain protein soulless/Phox2a. Neuron 1999, 24:555-566.
16. Hamilton D.A., Akers K.G., Rice J.P., Johnson T.E., Candelaria-Cook F.T., Maes L.I., et al. Prenatal exposure to moderate levels of ethanol alters social behavior in adult rats: relationship to structural plasticity and immediate early gene expression in frontal cortex. Behav Brain Res 2010, 207:290-304.
17. Hanson J.W., Jones K.L., Smith D.W. Fetal alcohol syndrome. JAMA 1976, 235:1458.
18. Heinrichs M., Von Dawans B., Domes G. Oxytocin, vasopressin, and human social behavior. Front Neuroendocrinol 2009, 30:548-557.
19. Heisler L.K., Chu H.-M., Brennan T.J., Danao J.A., Bajwa P., Parsons L.H., et al. Elevated anxiety and antidepressant-like responses in serotonin 5-HT1A receptor mutant mice. Proc Natl Acad Sci 1998, 95:15049-15054.
20. Hellemans K.G., Verma P., Yoon E., Yu W., Weinberg J. Prenatal alcohol exposure increases vulnerability to stress and anxiety-like disorders in adulthood. Ann N Y Acad Sci 2008, 1144:154-175.
21. Hofmann C.E., Ellis L., Yu W.K., Weinberg J. Hypothalamic-pituitary-adrenal responses to 5-HT1A and 5-HT2A/C agonists are differentially altered in female and male rats prenatally exposed to ethanol. Alcohol Clin Exp Res 2007, 31:345-355.
22. Kalant H. Direct effects of ethanol on the nervous system. Fed Proc 1930-1941, 34:1975.
23. Keil V., Paley B., Frankel F., O'connor M.J. Impact of a social skills intervention on the hostile attributions of children with prenatal alcohol exposure. Alcohol Clin Exp Res 2010, 34:231-241.
24. Kelly S.J., Day N., Streissguth A.P. Effects of prenatal alcohol exposure on social behavior in humans and other species. Neurotoxicol Teratol 2000, 22:143-149.
25. Kim J., Gillespie R.A., Druse M.J. Effects of maternal ethanol consumption and buspirone treatment on 5-HT1A and 5-HT2A receptors in offspring. Alcohol Clin Exp Res 1997, 21:1169-1178.
26. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev Dyn 1995, 203:253-310.
27. Mathur P., Berberoglu M.A., Guo S. Preference for ethanol in zebrafish following a single exposure. Behav Brain Res 2011, 217:128-133.
28. May P.A., Gossage J.P., Kalberg W.O., Robinson L.K., Buckley D., Manning M., et al. Prevalence and epidemiologic characteristics of FASD from various research methods with an emphasis on recent in-school studies. Dev Disabil Res Rev 2009, 15:176-192.
29. Mcgee C.L., Fryer S.L., Bjorkquist O.A., Mattson S.N., Riley E.P. Deficits in social problem solving in adolescents with prenatal exposure to alcohol. Am J Drug Alcohol Abuse 2008, 34:423-431.
30. Moore K.A., Kunsman G.W., Levine B.S., Herman M.M., Cervenak J., Hyde T.M. A comparison of ethanol concentrations in the occipital lobe and cerebellum. Forensic Sci Int 1997, 86:127-134.
31. O'connor M.J., Kogan N., Findlay R. Prenatal alcohol exposure and attachment behavior in children. Alcohol Clin Exp Res 2002, 26:1592-1602.
32. Oliveira R.F. Mind the fish: zebrafish as a model in cognitive social neuroscience. Front Neural Circ 2013, 7.
33. Olson H.C., Feldman J.J., Streissguth A.P., Sampson P.D., Bookstein F.L. Neuropsychological deficits in adolescents with fetal alcohol syndrome: clinical findings. Alcohol Clin Exp Res 1998, 22:1998-2012.
34. Osborn J.A., Kim C.K., Steiger J., Weinberg J. Prenatal ethanol exposure differentially alters behavior in males and females on the elevated plus maze. Alcohol Clin Exp Res 1998, 22:685-696.
35. Paaver M., Nordquist N., Parik J., Harro M., Oreland L., Harro J. Platelet MAO activity and the 5-HTT gene promoter polymorphism are associated with impulsivity and cognitive style in visual information processing. Psychopharmacology (Berl) 2007, 194:545-554.
36. Paintner A., Williams A.D., Burd L. Fetal alcohol spectrum disorders-implications for child neurology, part 1: prenatal exposure and dosimetry. J Child Neurol 2012, 27:258-263.
37. Parker M.O., Brock A.J., Millington M.E., Brennan C.H. Behavioral phenotyping of casper mutant and 1-pheny-2-thiourea treated adult zebrafish. Zebrafish 2013, 10:466-471.
38. Parker M.O., Millington M.E., Combe F.J., Brennan C.H. Housing conditions differentially affect physiological and behavioural stress responses of zebrafish, as well as the response to anxiolytics. PLoS ONE 2012, 7:e34992.
39. Pham M., Raymond J., Hester J., Kyzar E., Gaikwad S., Bruce I., et al. Assessing social behavior phenotypes in adult zebrafish: shoaling, social preference, and mirror biting tests. Zebrafish protocols for neurobehavioral research 2012, 231-246. Springer.
40. Rasmussen C., Becker M., Mclennan J., Urichuk L., Andrew G. An evaluation of social skills in children with and without prenatal alcohol exposure. Child Care Health Dev 2011, 37:711-718.
41. Reimers M.J., Flockton A.R., Tanguay R.L. Ethanol-and acetaldehyde-mediated developmental toxicity in zebrafish. Neurotoxicol Teratol 2004, 26:769-781.
42. Retz W., Retz-Junginger P., Supprian T., Thome J., Rösler M. Association of serotonin transporter promoter gene polymorphism with violence: relation with personality disorders, impulsivity, and childhood ADHD psychopathology. Behav Sci Law 2004, 22:415-425.
43. Risch N., Herrell R., Lehner T., Liang K.Y., Eaves L., Hoh J., et al. Interaction between the serotonin transporter gene (5-HTTLPR), stressful life events, and risk of depression. JAMA 2009, 301:2462.
44. Roebuck T.M., Mattson S.N., Riley E.P. Behavioral and psychosocial profiles of alcohol-exposed children. Alcohol Clin Exp Res 1999, 23:1070-1076.
45. Sood B., Delaney-Black V., Covington C., Nordstrom-Klee B., Ager J., Templin T., et al. Prenatal alcohol exposure and childhood behavior at age 6 to 7years: I. dose-response effect. Pediatrics 2001, 108:E34.
46. Stewart A., Gaikwad S., Kyzar E., Green J., Roth A., Kalueff A.V. Modeling anxiety using adult zebrafish: a conceptual review. Neuropharmacology 2012, 62:135-143.
47. Streissguth A.P., Bookstein F.L., Sampson P.D., Barr H.M. Neurobehavioral effects of prenatal alcohol: Part III. PLS analyses of neuropsychologic tests. Neurotoxicol Teratol 1989, 11:493-507.
48. Strobel A., Gutknecht L., Rothe C., Reif A., Mössner R., Zeng Y., et al. Allelic variation in 5-HT1A receptor expression is associated with anxiety-and depression-related personality traits. J Neural Transm 2003, 110:1445-1453.
49. Suess P.E., Newlin D.B., Porges S.W. Motivation, sustained attention, and autonomic regulation in school-age boys exposed in utero to opiates and alcohol. Exp Clin Psychopharmacol 1997, 5:375-387.
50. Swanson K., Beckwith L., Howard J. Intrusive caregiving and quality of attachment in prenatally drug-exposed toddlers and their primary caregivers. Attach Hum Dev 2000, 2:130-148.
51. Tang R., Dodd A., Lai D., Mcnabb W.C., Love D.R. Validation of zebrafish (Danio rerio) reference genes for quantitative real-time RT-PCR normalization. Acta Biochim Biophys Sin 2007, 39:384-390.
52. Teh M.T., Hutchison I.L., Costea D.E., Neppelberg E., Liavaag P.G., Purdie K., et al. Exploiting FOXM1-orchestrated molecular network for early squamous cell carcinoma diagnosis and prognosis. Int J Cancer 2012, 2012.
53. Thomas S.E., Kelly S.J., Mattson S.N., Riley E.P. Comparison of social abilities of children with fetal alcohol syndrome to those of children with similar IQ scores and normal controls. Alcohol Clin Exp Res 1998, 22:528-533.
54. Valenzuela C.F., Morton R.A., Diaz M.R., Topper L. Does moderate drinking harm the fetal brain? Insights from animal models. Trends Neurosci 2012, 35:284-292.
55. Weinberg J. Neuroendocrine effects of prenatal alcohol exposure. Ann N Y Acad Sci 1993, 697:86-96.
56. Weinberg J., Kim C.K., Yu W. Early handling can attenuate adverse effects of fetal ethanol exposure. Alcohol 1995, 12:317-327.
57. Weinberg J., Taylor A.N., Gianoulakis C. Fetal ethanol exposure: hypothalamic-pituitary-adrenal and beta-endorphin responses to repeated stress. Alcohol Clin Exp Res 1996, 20:122-131.
58. Wendland J.R., Lesch K.P., Newman T.K., Timme A., Gachot-Neveu H., Thierry B., et al. Differential functional variability of serotonin transporter and monoamine oxidase a genes in macaque species displaying contrasting levels of aggression-related behavior. Behav Genet 2006, 36:163-172.
59. Winslow J.T., Shapiro L., Carter C.S., Insel T.R. Oxytocin and complex social behavior: species comparisons. Psychopharmacol Bull 1993, 29:409-414.
60. Yoshida M., Takayanagi Y., Inoue K., Kimura T., Young L.J., Onaka T., et al. Evidence that oxytocin exerts anxiolytic effects via oxytocin receptor expressed in serotonergic neurons in mice. J Neurosci 2009, 29:2259-2271.
61. Zafar H., Shelat S.G., Redei E., Tejani-Butt S. Fetal alcohol exposure alters serotonin transporter sites in rat brain. Brain Res 2000, 856:184-192.