The effect of early maternal separation on brain derived neurotrophic factor and monoamine levels in adult heterozygous reeler mice

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 32, Issue 5, 2008, Pages 1269-1276

  Ognibene, Elisa ^a,b   Adriani, Walter ^a   Caprioli, Antonio ^b   Ghirardi, Orlando ^b   Ali, Syed F ^c   Aloe, Luigi ^d   Laviola, Giovanni ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b Sigma Tau SpA   (Italy)

^c NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^d CNR   (Italy)

Author keywords

3,4 dihydroxyphenylacetic acid; 5 HIAA; 5 hydroxy tryptamine; 5 hydroxyindole acetic acid; 5HT; BDNF; Brain derived neurotrophic factor; DA; DOPAC; Dopamine; Early adversity; GDNF; Genetic vulnerability; Glial derived neurotrophic factor; H; Handled; Heterozygous (rl +); High performance liquid chromatography.; Homovanillic acid; HPLC; HVA; HZ; Mice; Olanzapine; OLZ; PND; Post natal day; Psychiatric disorder; Real time polymerase chain reaction; Reeler (rl rl); Reelin; RL; RT PCR; SAL; Saline; SEP; Separated; Social behavior; Wild Type (+ +); WT

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 5 HYDROXYINDOLEACETIC ACID; ATYPICAL ANTIPSYCHOTIC AGENT; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN MONOAMINE; DOPAMINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; HOMOVANILLIC ACID; OLANZAPINE; REELIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE BRAIN LEVEL; DRUG EFFECT; ENVIRONMENTAL FACTOR; GENOTYPE; HIPPOCAMPUS; MATERNAL DEPRIVATION; METABOLITE; MOUSE; MOUSE STRAIN; NERVE CELL PLASTICITY; NONHUMAN; OUTCOME ASSESSMENT; PERINATAL PERIOD; REELER HETEROZYGOUS MOUSE; SEROTONIN BRAIN LEVEL; STIMULUS; STRESS; WILD TYPE;

ANIMALS; ANTIPSYCHOTIC AGENTS; BEHAVIOR, ANIMAL; BENZODIAZEPINES; BIOGENIC MONOAMINES; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; EXPLORATORY BEHAVIOR; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; HETEROZYGOTE; MATERNAL DEPRIVATION; MICE; MICE, INBRED C57BL; MICE, NEUROLOGIC MUTANTS; MOTOR ACTIVITY; NAPHTHALENES; OXEPINS; SOCIAL BEHAVIOR;

EID: 50049104467     PISSN: 02785846     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2008.03.023     Document Type: Article

References (60)

1. Adriani W., Caprioli A., Granstrem O., Carli M., and Laviola G. The spontaneously hypertensive rat as an animal model of ADHD: evidence for impulsive and non-impulsive subpopulations. Neurosci Biobehav Rev 27 (2003) 639-651
2. Agid O., Shapira B., Zislin J., Ritsner M., Hanin B., Murad H., et al. Environment and vulnerability to major psychiatric illness - a case control study of early parental loss in major depression, biopolar disorder and schizophrenia. Mol Psychiatry 4 (1999) 163-172
3. Alcantara S., Pozas E., Ibanez C.F., and Soriano E. BDNF-modulated spatial organization of Cajal-Retzius and GABAergic neurons in the marginal zone plays a role in the development of cortical organization. Cereb Cortex 16 (2006) 487-499
4. Ali S.F., Newport G.D., Holson R.R., Slikker W., and Bowyer J.F. Low environmental temperatures or pharmacological agents which produce hypothermia decreases methamphetamine neurotoxicity in mice. Brain Res 658 (1994) 33-38
5. Aloe L., Iannitelli A., Angelucci F., Bersani G., and Fiore M. Studies in animal models and humans suggesting a role of nerve growth factor in schizophrenia-like disorders. Behav Pharmacol 11 (2000) 235-242
6. Andersen T.E., Finsen B., Goffinet A.M., Issinger O.G., and Boldyreff B. A reeler mutant mouse with a new, spontaneous mutation in the reelin gene. Mol Brain Res 105 (2002) 153-156
7. Bai O., Chlan-Fourney J., Bowen R., Keegan D., and Li X.M. Expression of brain-derived neurotrophic factor mRNA in rat hippocampus after treatment with antipsychotic drugs. J Neurosci Res 71 (2003) 127-131
8. Ballmaier M., Zoli M., Leo G., Agnati L.F., and Spano P. Preferential alterations in the mesolimbic dopamine pathway of heterozygous reeler mice: an emerging animal-based model of schizophrenia. Eur J Neurosci 15 (2002) 1197-1205
9. Bartlett C.W., Gharani N., Millonig J.H., and Brzustowicz L.M. Three autism candidate genes: a synthesis of human genetic analysis with other disciplines. Int J Dev Neurosci 23 (2005) 221-234
10. Berninger B., Marty S., Zafra F., da Penha Berzaghi M., Thoenen H., and Lindholm D. GABAergic stimulation switches from enhancing to repressing BDNF expression in rat hippocampal neurons during maturation in vitro. Development 121 (1995) 2327-2335
11. Bersani G., Garavini A., Iannitelli A., Quartini A., Nordio M., Di Biasi C., et al. Reduced pineal volume in male patients with schizophrenia: no relationship to clinical features of the illness. Neurosci Lett 329 (2002) 246-248
12. Biagini G., Merlo-Pich E., Carani C., Marrama P., and Agnati F.L. Postnatal maternal separation during the SHRP enhances the adrenocortical response to novelty in adult rats by affecting feedback regulation in the CA1 hippocampal field. Int J Dev Neurosci 16 (1997) 187-197
13. Caldji C., Diorio J., and Meaney M.J. Variations in maternal care in infancy regulate the development of stress reactivity. Biol Psychiatry 48 (2000) 1164-1174
14. Cirulli F., Berry A., and Alleva E. Early disruption of the mother-infant relationship: effects on brain plasticity and implications for psychopathology. Neurosci Biobehav Rev 27 (2003) 73-82
15. Costa E., Davis J., Grayson D.R., Guidotti A., Pappas G.D., and Pesold C. Dendritic spine hypoplasia and downregulation of reelin and GABAergic tone in schizophrenia vulnerability. Neurobiol Dis 8 (2001) 723-742
16. Dell'Omo G., Vannoni E., Vyssotski A.L., Di Bari M.A., Nonno R., Agrimi U., et al. Early behavioral changes in mice infected with BSE and scrapie: automated home cage monitoring reveals prion strain differences. Eur J Neurosci 16 (2002) 735-742
17. Dias B.G., Banerjee S.B., Duman R.S., and Vaidya V.A. Differential regulation of brain derived neurotrophic factor transcripts by antidepressant treatments in the adult rat brain. Neuropharmacology 45 (2003) 553-563
18. Duman R.S. Novel therapeutic approaches beyond the serotonin receptor. Biol Psychiatry 44 (1998) 324-335
19. Fumagalli F., Molteni R., Roceri M., Bedogni F., Santero R., Fossati C., et al. Effect of antipsychotic drugs on brain-derived neurotrophic factor expression under reduced N-methyl-D-aspartate receptor activity. J Neurosci Res 72 (2003) 622-628
20. Fumagalli F., Bedogni F., Perez J., Racagni G., and Riva M.A. Corticostriatal brain-derived neurotrophic factor dysregulation in adult rats following prenatal stress. Eur J Neurosci 20 (2004) 1348-1354
21. Gottesman I.I., and Hanson D.R. Human development: biological and genetic processes. Annu Rev Psychol 2 (2005) 263-286
22. Greisen M.H., Altar C.A., Bolwig T.G., Whitehead R., and Wortwein G. Increased adult hippocampal brain-derived neurotrophic factor and normal levels of neurogenesis in maternal separation rats. J Neurosci Res 79 (2005) 772-778
23. Grootendorst J., De Kloet E.R., Dalm S., and Oitzl S. Reversal of cognitive deficit of ApoE knockout mice after repeated exposure to a common environmental experience. Neuroscience 108 (2001) 237-247
24. Huang E.J., and Reichardt L.F. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24 (2001) 677-736
25. Kaneko W.M., Riley E.P., and Elhers C.L. Behavioral and electrophysiological effects of early repeated maternal separation. Depression 2 (1994) 43-53
26. Kawano K., Morinobu S., Sawada T., Tsuji S., Erabi K., Fuchikami M., et al. Prior neonatal isolation reduces induction of NGF mRNA and decreases GDNF mRNA in the hippocampus of juvenile and adult rodents subjected to immobilization stress. Synapse 62 (2008) 259-267
27. Lasley S.M., Greenland R.D., Minnema D.J., and Michaelson I.A. Influence of chronic inorganic lead exposure on regional dopamine and 5-hydroxytryptamine turnover in rat brain. Neurochem Res 9 (1984) 1675-1688
28. Laviola G., and Terranova M.L. The developmental psychobiology of behavioral plasticity in mice: the role of social experiences in the family unit. Neurosci Biobehav Rev 23 (1998) 197-213
29. Laviola G., Sedowofia K., Innes J., Clayton R., and Manning A. Genetic differences in maternal behavior patterns in mice administered phenobarbital during pregnancy. Psychopharmacology 102 (1990) 383-390
30. Laviola G., Adriani W., Gaudino C., Marino R., and Keller F. Paradoxical effects of prenatal acetilcholinesterase blockade on neurobehavioral development and drug-induced stereotipies in reeler mice. Psychopharmacology 187 (2006) 331-344
31. Lehmann J., and Feldon J. Long-term bio-behavioral effects of maternal separation in the rat: consistent or confusing?. Rev Neurosci 11 (2000) 383-408
32. Lehmann J., Pryce C.R., Jongen-Relo A.L., Stöhr T., Pothuizen H.J., and Feldon J. Comparison of maternal separation and early handling in terms of neurobehavioral effects in aged rats. Neurobiol Aging 23 (2002) 457-466
33. Leriche L., Diaz J., and Sokoloff P. Dopamine and glutamate dysfunctions in schizophrenia: role of the dopamine D3 receptor. Neurotox Res 6 (2004) 63-71
34. Levine S. Infantile experience and resistance to physiological stress. Science 126 (1957) 405-406
35. Levine S., Huchton D.M., Wiener S.G., and Rosenfeld P. Time course of the effect of maternal deprivation on the hypothalamic-pituitary-adrenal axis in the infant rat. Dev Psychobiol 24 (1991) 547-558
36. Luo C., Xu H., and Li X.M. Post-stress changes in BDNF and Bcl-2 immunoreactivities in hippocampal neurons: effect of chronic administration of olanzapine. Brain Res 1025 (2004) 194-202
37. Marrone M.C., Marinelli S., Biamonte F., Keller F., Sgobio C.A., Ammassari-Teule M., et al. Altered cortico-striatal synaptic plasticity and related behavioral impairments in reeler mice. Eur J Neurosci 24 (2006) 2061-2070
38. Matthews K., Hall S.F., Wilkinson L.S., and Robbins T.W. Retarded acquisition and reduced expression of conditioned locomotor activity in adult rats following repeated maternal separation: effects of prefeeding, d-amphetamine, dopamine antagonists and clonidine. Psychopharmacology 126 (1996) 75-84
39. McEwen B.S., Alves S.E., Bulloch K., and Weiland N.G. Clinically relevant basic science studies of gender differences and sex hormone effects. Psychopharmacol Bull 34 (1998) 251-259
40. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Ann Rev Neurosci 24 (2001) 1161-1192
41. Mizuno M., Yamada K., Olariu A., Nawa H., and Nabeshima T. Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J Neurosci 20 (2000) 7116-7121
42. Morisset S., Sahm U.G., Traiffort E., Tardivel-Lacombe J., Arrang J.M., and Schwartz J.C. Atypical neuroleptics enhance histamine turnover in brain via 5-Hydroxy-tryptamine 2A receptor blockade. J Pharmacol Exp Ther 288 (1999) 590-596
43. Nadler J.J., Moy S.S., Dold G., Trang D., Simmons N., Perez A., et al. Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav 3 (2004) 303-314
44. Ognibene E., Adriani W., Macrì S., and Laviola G. Neurobehavioral disorders in the infant reeler mouse model: interaction of genetic vulnerability and consequences of maternal separation. Behav Brain Res 177 (2007) 142-149
45. Ognibene E., Adriani W., Granstrem O., Pieretti S., and Laviola G. Impulsivity-anxiety-related behavior and profiles of morphine induced analgesia in heterozygous reeler mice. Brain Res 1131 (2007) 173-180
46. Persico A.M., and Keller F. The neurobiological context of autism. Mol Neurobiol 28 (2003) 1-22
47. Podhorna J., and Didriksen M. The heterozygous reeler mouse: behavioral phenotype. Behav Brain Res 153 (2003) 43-54
48. Poo M.M. Neurotrophins as synaptic modulators. Nat Rev Neurosci 2 (2001) 24-32
49. Ringstedt T., Linnarsson S., Wagner J., Lendahl U., Kokaia Z., Arenas E., et al. BDNF regulates reelin expression and Cajal-Retzius cell development in the cerebral cortex. Neuron 21 (1998) 305-315
50. Riva M.A., Molteni R., Bedogni F., Racagni G., and Fumagalli F. Emerging role of the FGF system in psychiatric disorders. Trends Pharmacol Sci 26 (2005) 228-231
51. Roceri M., Hendriks W., Racagni G., Ellenbroek B.A., and Riva M.A. Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol Psychiatry 7 (2002) 609-616
52. Roceri M., Cirulli F., Pessina C., Peretto P., Racagni G., and Riva M.A. Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions. Biol Psychiatry 55 (2004) 708-714
53. Romeo R., Mueller A., Sisti M., Ogawa S., McEwen B.S., and Brake W. Anxiety and fear behaviors in adult male and female C57BL/6 mice are modulated by maternal separation. Horm Behav 43 (2003) 561-567
54. Russo-Neustadt A. Brain-derived neurotrophic factor, behavior, and new directions for the treatment of mental disorders. Semin Clin Neuropsychiatry 8 (2003) 109-118
55. Salinger W.L., Ladrow P., and Wheeler C. Behavioral phenotype of the reeler mutant mouse: effects of reln gene dosage and social isolation. Behav Neurosci 6 (2003) 1257-1275
56. Shao Z., Dyck L.E., Wang H., and Li X.M. Antipsychotic drugs cause glial cell line-derived neurotrophic factor secretion from C6 glioma cells. J Psychiatry Neurosci 31 (2006) 32-37
57. Tirassa P., Manni L., Stenfors C., Lundeberg T., and Aloe L. RT-PCR ELISA method for the analysis of neurotrophin messenger-RNA expression in brain and peripheral tissues. J Biotechnol 84 (2000) 259-272
58. Tueting P., Costa E., Dwivedi Y., Guidotti A., Impagnatiello F., Manev R., et al. The phenotipic characteristics of heterozygous reeler mouse. Neuroreport 10 (1999) 1329-1334
59. Tueting P., Doueiri M.S., Guidotti A., Davis J.M., and Costa E. Reelin down-regulation in mice and psychosis endophenotypes. Neurosci Biobehav Rev 30 (2006) 1065-1077
60. Vaynman S., Ying Z., and Gomez-Pinilla F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 20 (2004) 2580-2590