Gene-environment interaction of reelin and stress in cognitive behaviours in mice: Implications for schizophrenia

Behavioural Brain Research

Volumn 287, Issue , 2015, Pages 304-314

  Schroeder, Anna ^a   Buret, Laetitia ^a,b   Hill, Rachel A ^a   van den Buuse, Maarten ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

Author keywords

Corticosterone; Prepulse inhibition; Reelin; Schizophrenia; Social interaction; Y maze

Indexed keywords

CORTICOSTERONE; REELIN; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; REELIN PROTEIN; SCLEROPROTEIN; SERINE PROTEINASE;

ADRENAL GLAND; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; COGNITION; CONTROLLED STUDY; FEMALE; GENOTYPE ENVIRONMENT INTERACTION; HABITUATION; HETEROZYGOSITY; HIPPOCAMPUS; MALE; MAZE TEST; MOUSE; NONHUMAN; ORGAN WEIGHT; PREFRONTAL CORTEX; PREPULSE INHIBITION; PRIORITY JOURNAL; PROTEIN INTERACTION; SCHIZOPHRENIA; SHORT TERM MEMORY; SIMULATION; SOCIAL INTERACTION; SPATIAL MEMORY; STRESS; VISUAL MEMORY; ANIMAL; ANIMAL BEHAVIOR; BRAIN; CHEMICALLY INDUCED; GENETICS; MENTAL STRESS; METABOLISM; PERCEPTION; PHYSIOLOGY; PSYCHOLOGY; SENSORY GATING; SEX DIFFERENCE;

ANIMALS; BEHAVIOR, ANIMAL; BODY WEIGHT; BRAIN; CELL ADHESION MOLECULES, NEURONAL; COGNITION; CORTICOSTERONE; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GENE-ENVIRONMENT INTERACTION; HIPPOCAMPUS; MALE; MEMORY, SHORT-TERM; MICE; NERVE TISSUE PROTEINS; SCHIZOPHRENIA; SENSORY GATING; SERINE ENDOPEPTIDASES; SEX FACTORS; SOCIAL PERCEPTION; SPATIAL MEMORY; STRESS, PSYCHOLOGICAL;

EID: 84927513862     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2015.03.063     Document Type: Article

References (71)

1. Lewis D.A., Hashimoto T., Volk D.W. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 2005, 6:312-324.
2. Davidson M., Galderisi S., Weiser M., Werbeloff N., Fleischhacker W.W., Keefe R.S., et al. Cognitive effects of antipsychotic drugs in first-episode schizophrenia and schizophreniform disorder: a randomized, open-label clinical trial (EUFEST). Am J Psychiatry 2009, 166:675-682.
3. Cannon M., Caspi A., Moffitt T.E., Harrington H., Taylor A., Murray R.M., et al. Evidence for early-childhood, pan-developmental impairment specific to schizophreniform disorder - results from a longitudinal birth cohort. Arch Gen Psychiatry 2002, 59:449-456.
4. Sitskoom M.M., Aleman A., Ebisch S.J.H., Appels M.C.M., Kahn R.S. Cognitive deficits in relatives of patients with schizophrenia: a meta-analysis. Schizophr Res 2004, 71:285-295.
5. Green M.F., Kern R.S., Heaton R.K. Longitudinal studies of cognition and functional outcome in schizophrenia: implications for MATRICS. Schizophr Res 2004, 72:41-51.
6. Maynard T.M., Sikich L., Lieberman J.A., LaMantia A.S. Neural development, cell-cell signaling, and the two-hit hypothesis of schizophrenia. Schizophr Bull 2001, 27:457-476.
7. McGrath J.J., Feron F.P., Burne T.H.J., Mackay-Sim A., Eyles D.W. The neurodevelopmental hypothesis of schizophrenia: a review of recent developments. Ann Med 2003, 35:86-93.
8. Freedman R. Schizophrenia. New Engl J Med 2003, 349:1738-1749.
9. Darcangelo G., Miao G.G., Chen S.C., Soares H.D., Morgan J.I., Curran T. A protein related to extracellular-matrix proteins deleted in the mouse mutant reeler. Nature 1995, 374:719-723.
10. Frotscher M., Chai X., Bock H.H., Haas C.A., Foerster E., Zhao S. Role of reelin in the development and maintenance of cortical lamination. J Neural Transm 2009, 116:1451-1455.
11. Campo C., Sinagra M., Verrier D., Manzoni O.J., Chavis P. Reelin secreted by GABAergic neurons regulates glutamate receptor homeostasis. PLoS ONE 2009, 4.
12. Ventruti A., Kazdoba T.M., Niu S., D'Arcangelo G. Reelin deficiency causes specific defects in the molecular composition of the synapses in the adult brain. Neuroscience 2011, 189:32-42.
13. Guidotti A., Auta J., Davis J.M., Gerevini V.D., Dwivedi Y., Grayson D.R., et al. Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder - a postmortem brain study. Arch Gen Psychiatry 2000, 57:1061-1069.
14. Impagnatiello F., Guidotti A.R., Pesold C., Dwivedi Y., Caruncho H., Pisu M.G., et al. A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proc Natl Acad Sci U S A 1998, 95:15718-15723.
15. Knable M.B., Barci B.M., Webster M.J., Meador-Woodruff J., Torrey E.F. Molecular abnormalities of the hippocampus in severe psychiatric illness: postmortem findings from the Stanley Neuropathology Consortium. Mol Psychiatry 2004, 9:609-620.
16. Brigman J.L., Padukiewicz K.E., Sutherland M.L., Rothblat L.A. Executive functions in the heterozygous reeler mouse model of schizophrenia. Behav Neurosci 2006, 120:984-988.
17. Larson J., Hoffman J.S., Guidotti A., Costa E. Olfactory discrimination learning deficit in heterozygous reeler mice. Brain Res 2003, 971:40-46.
18. Podhorna J., Didriksen M. The heterozygous reeler mouse: behavioural phenotype. Behav Brain Res 2004, 153:43-54.
19. Salinger W.L., Ladrow P., Wheeler C. Behavioral phenotype of the reeler mutant mouse: effects of Reln gene dosage and social isolation. Behav Neurosci 2003, 117:1257-1275.
20. Tueting P., Doueiri M., Guidotti A., Davis J.M., Costa E. Reelin down-regulation in mice and psychosis endo-phenotypes. Neurosci Biobehav Rev 2006, 30:1065-1077.
21. Tueting P., Costa E., Dwivedi Y., Guidotti A., Impagnatiello F., Manev R., et al. The phenotypic characteristics of heterozygous reeler mouse. Neuroreport 1999, 10:1329-1334.
22. van den Buuse M., Halley P., Hill R., Labots M., Martin S. Altered N-methyl-d-aspartate receptor function in reelin heterozygous mice: male-female differences and comparison with dopaminergic activity. Prog Neuro-Psychopharmacol Biol Psychiatry 2012, 37:237-246.
23. Howell K.R., Pillai A. Effects of prenatal hypoxia on schizophrenia-related phenotypes in heterozygous reeler mice: a gene×environment interaction study. Eur Neuropsychopharmacol 2014, 24:1324-1336.
24. Macri S., Biamonte F., Romano E., Marino R., Keller F., Laviola G. Perseverative responding and neuroanatomical alterations in adult heterozygous reeler mice are mitigated by neonatal estrogen administration. Psychoneuroendocrinology 2010, 35:1374-1387.
25. Qiu S., Korwek K.M., Pratt-Davis A.R., Peters M., Bergman M.Y., Weeber E.J. Cognitive disruption and altered hippocampus synaptic function in reelin haploinsufficient mice. Neurobiol Learn Mem 2006, 85:228-242.
26. Ognibene E., Adriani W., Macri S., Laviola G. Neurobehavioural disorders in the infant reeler mouse model: interaction of genetic vulnerability and consequences of maternal separation. Behav Brain Res 2007, 177:142-149.
27. Starkman M., Giordani B., Gebarski S., Schteingart D. Improvement in learning associated with increase in hippocampal formation volume. Biol Psychiatry 2003, 53:233-238.
28. Lupien S., Gillin C., Hauger R. Working memory is more sensitive than declarative memory to the acute effects of corticosteroids: a dose-response study in humans. Behav Neurosci 1999, 113:420-430.
29. Laviola G., Ognibene E., Romano E., Adriani W., Keller F. Gene-environment interaction during early development in the heterozygous reeler mouse: clues for modelling of major neurobehavioral syndromes. Neurosci Biobehav Rev 2009, 33:560-572.
30. Lussier A.L., Romay-Tallon R., Kalynchuk L.E., Caruncho H.J. Reelin as a putative vulnerability factor for depression: examining the depressogenic effects of repeated corticosterone in heterozygous reeler mice. Neuropharmacology 2011, 60:1064-1074.
31. Riecher-Rossler A., Kulkarni J. Estrogens and gonadal function in schizophrenia and related psychoses. Biological basis of sex differences in psychopharmacology 2011, 155-171. Springer-Verlag, Berlin. J.C. Neill, J. Kulkarni (Eds.).
32. Aleman A., Kahn R.S., Selten J.P. Sex differences in the risk of schizophrenia - evidence from meta-analysis. Arch Gen Psychiatry 2003, 60:565-571.
33. Broadbent N.J., Squire L.R., Clark R.E. Spatial memory, recognition memory, and the hippocampus. Proc Natl Acad Sci U S A 2004, 101:14515-14520.
34. Swerdlow N.R., Light G.A., Breier M.R., Shoemaker J.M., Saint Marie R.L., Neary A.C., et al. Sensory and sensorimotor gating deficits after neonatal ventral hippocampal lesions in rats. Dev Neurosci 2012, 34:240-249.
35. Koch M., Schnitzler H.U. The acoustic startle response in rats - circuits mediating evocation, inhibition and potentiation. Behav Brain Res 1997, 89:35-49.
36. Karatsoreos I.N., Bhagat S.M., Bowles N.P., Weil Z.M., Pfaff D.W., McEwen B.S. Endocrine and physiological changes in response to chronic corticosterone: a potential model of the metabolic syndrome in mouse. Endocrinology 2010, 151:2117-2127.
37. Klug M., Hill R.A., Choy K.H.C., Kyrios M., Hannan A.J., van den Buuse M. Long-term behavioral and NMDA receptor effects of young-adult corticosterone treatment in BDNF heterozygous mice. Neurobiol Dis 2012, 46:722-731.
38. Dellu F., Contarino A., Simon H., Koob G.F., Gold L.H. Genetic differences in response to novelty and spatial memory using a two-trial recognition task in mice. Neurobiol Learn Mem 2000, 73:31-48.
39. Ennaceur A., Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1. Behavioral data. Behav Brain Res 1988, 31:47-59.
40. Dere E., Huston J.P., De Souza Silva M.A. The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neurosci Biobehav Rev 2007, 31:673-704.
41. Yang M., Silverman J.L., Crawley J.N. Automated three-chambered social approach task for mice. Curr Protoc Neurosci 2011, 26. [chapter 8: unit 8].
42. van den Buuse M., Wischhof L., Lee R.X., Martin S., Karl T. Neuregulin 1 hypomorphic mutant mice: enhanced baseline locomotor activity but normal psychotropic drug-induced hyperlocomotion and prepulse inhibition regulation. Int J Neuropsychopharmacol 2009, 12:1383-1393.
43. van den Buuse M., Becker T., Kwek P., Martin S., Ruimschotel E., Risbrough V. Disruption of prepulse inhibition by 3,4-methylenedioxymethamphetamine (MDMA): comparison between male and female wild-type and 5-HT1A receptor knockout mice. Int J Neuropsychopharmacol 2011, 14:856-861.
44. Buret L., van den Buuse M. Corticosterone treatment during adolescence induces down-regulation of reelin and NMDA receptor subunit GLUN2C expression only in male mice: implications for schizophrenia. Int J Neuropsychopharmacol 2014, 21:1-12.
45. Wright R.L., Conrad C.D. Chronic stress leaves novelty-seeking behavior intact while impairing spatial recognition memory in the Y-maze. Stress 2005, 8:151-154.
46. Sapolsky R.M. Stress and plasticity in the limbic system. Neurochem Res 2003, 28:1735-1742.
47. Braff D.L., Geyer M.A., Swerdlow N.R. Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl) 2001, 156:234-258.
48. Swerdlow N.R., Weber M., Qu Y., Light G.A., Braff D.L. Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacology (Berl) 2008, 199:331-388.
49. Ingram N., Martin S., Wang J.H., van der Laan S., Loiacono R., van den Buuse M. Interaction of corticosterone and nicotine in regulation of prepulse inhibition in mice. Neuropharmacology 2005, 48:80-92.
50. Fatemi S.H. Reelin glycoprotein: structure, biology and roles in health and disease 2008, 291-309. Springer, New York.
51. Teixeira C.M., Martin E.D., Sahun I., Masachs N., Pujadas L., Corvelo A., et al. Overexpression of reelin prevents the manifestation of behavioral phenotypes related to schizophrenia and bipolar disorder. Neuropsychopharmacology 2011, 36:2395-2405.
52. van den Buuse M. Modeling the positive symptoms of schizophrenia in genetically modified mice: pharmacology and methodology aspects. Schizophr Bull 2010, 36:246-270.
53. Mullen B.R., Khialeeva E., Hoffman D.B., Ghiani C.A., Carpenter E.M. Decreased reelin expression and organophosphate pesticide exposure alters mouse behaviour and brain morphology. ASN Neuro 2013, 5:27-42.
54. Tremolizzo L., Doueiri M.S., Dong E., Grayson D.R., Davis J., Pinna G., et al. Valproate corrects the schizophrenia-like epigenetic behavioral modifications induced by methionine in mice. Biol Psychiatry 2005, 57:500-509.
55. Winters B.D., Forwood S.E., Cowell R.A., Saksida L.M., Bussey T.J. Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: heterogeneity of function within the temporal lobe. J Neurosci 2004, 24:5901-5908.
56. Popovic N., Pajovic S.B. Lithium modulates the chronic stress-induced effect on blood glucose levels of male rats. Arch Biol Sci 2010, 62:289-295.
57. Ulrich-Lai Y.M., Figueiredo H.F., Ostrander M.M., Choi D.C., Engeland W.C., Herman J.P. Chronic stress induces adrenal hyperplasia and hypertrophy in a subregion-specific manner. Am J Physiol - Endocrinol Metab 2006, 291:E965-E973.
58. Donner N.C., Montoya C.D., Lukkes J.L., Lowry C.A. Chronic non-invasive corticosterone administration abolishes the diurnal pattern of tph2 expression. Psychoneuroendocrinology 2012, 37:645-661.
59. Enkel T., Koch M. Chronic corticosterone treatment impairs trace conditioning in rats with a neonatal medial prefrontal cortex lesion. Behav Brain Res 2009, 203:173-179.
60. Thanos P.K., Cavigelli S.A., Michaelides M., Olvet D.M., Patel U., Diep M.N., et al. A non-invasive method for detecting the metabolic stress response in rodents: characterization and disruption of the circadian corticosterone rhythm. Physiol Res 2009, 58:219-228.
61. Ninnes C.E., Waas J.R., Ling N., Nakagawa S., Banks J.C., Bell D.G., et al. Comparing plasma and faecal measures of steroid hormones in Adelie penguins Pygoscelis adeliae. J Comp Physiol B - Biochem Syst Environ Physiol 2010, 180:83-94.
62. Touma C., Palme R., Sachser N. Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones. Horm Behav 2004, 45:10-22.
63. Atkinson H.C., Waddell B.J. Circadian variation in basal plasma corticosterone and adrenocorticotropin in the rat: sexual dimorphism and changes across the estrous cycle. Endocrinology 1997, 138:3842-3848.
64. Critchlow V., Barsela M., Mountcastle W., Liebelt R.A., Lipscomb H.S. Sex difference in resting pituitary-adrenal function in the rat. Am J Physiol 1963, 205:807.
65. Doehner J., Genoud C., Imhof C., Krstic D., Knuesel I. Extrusion of misfolded and aggregated proteins - a protective strategy of aging neurons?. Eur J Neurosci 2012, 35:1938-1950.
66. Gonzalez M., Cabrera-Socorro A., Perez-Garcia C.G., Fraser J.D., Lopez F.J., Alonso R., et al. Distribution patterns of estrogen receptor alpha and beta in the human cortex and hippocampus during development and adulthood. J Comp Neurol 2007, 503:790-802.
67. Bender R.A., Zhou L.P., Wilkars W., Fester L., Lanowski J.S., Paysen D., et al. Roles of 17 beta-estradiol involve regulation of reelin expression and synaptogenesis in the dentate gyrus. Cereb Cortex 2010, 20:2985-2995.
68. Liu J., Hu P., Qi X.R., Meng F.T., Kalsbeek A., Zhou J.N. Acute restraint stress increases intrahypothalamic oestradiol concentrations in conjunction with increased hypothalamic oestrogen receptor beta and aromatase mRNA expression in female rats. J Neuroendocrinol 2011, 23:435-443.
69. Weeber E.J., Beffert U., Jones C., Christian J.M., Forster E., Sweatt J.D., et al. Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J Biol Chem 2002, 277:39944-39952.
70. Rogers J.T., Rusiana I., Trotter J., Zhao L., Donaldson E., Pak D.T.S., et al. Reelin supplementation enhances cognitive ability, synaptic plasticity, and dendritic spine density. Learn Mem 2011, 18:558-564.
71. Beffert U., Durudas A., Weeber E.J., Stolt P.C., Giehl K.M., Sweatt J.D., et al. Functional dissection of reelin signaling by site-directed disruption of disabled-1 adaptor binding to apolipoprotein E receptor 2: distinct roles in development and synaptic plasticity. J Neurosci 2006, 26:2041-2052.