Corticosterone treatment during adolescence induces down-regulation of reelin and NMDA receptor subunit GLUN2C expression only in male mice: Implications for schizophrenia

International Journal of Neuropsychopharmacology

Volumn 17, Issue 8, 2014, Pages 1221-1232

  Buret, Laetitia ^a   Van Den Buuse, Maarten ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

Author keywords

Corticosterone; Glutamate; NMDA; Reelin; Schizophrenia; Stress

Indexed keywords

CORTICOSTERONE; GLUCOCORTICOID RECEPTOR; GLUTAMATE DECARBOXYLASE 67; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2C; PARVALBUMIN; REELIN; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; NR2C NMDA RECEPTOR; PROTEIN SUBUNIT; REELIN PROTEIN; SCLEROPROTEIN; SERINE PROTEINASE;

ADOLESCENCE; ADOLESCENT; ADULTHOOD; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DORSAL HIPPOCAMPUS; DOWN REGULATION; FEMALE; FRONTAL CORTEX; MALE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN QUATERNARY STRUCTURE; SCHIZOPHRENIA; VENTRAL HIPPOCAMPUS; WESTERN BLOTTING; WILD TYPE MOUSE; ANIMAL; DRUG EFFECTS; FRONTAL LOBE; GENETICS; HETEROZYGOTE; HIPPOCAMPUS; METABOLISM; PROTEIN SUBUNIT; SEXUAL DEVELOPMENT;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CORTICOSTERONE; DOWN-REGULATION; EXTRACELLULAR MATRIX PROTEINS; FEMALE; FRONTAL LOBE; GLUTAMATE DECARBOXYLASE; HETEROZYGOTE; HIPPOCAMPUS; MALE; MICE; NERVE TISSUE PROTEINS; PARVALBUMINS; PROTEIN SUBUNITS; RECEPTORS, GLUCOCORTICOID; RECEPTORS, N-METHYL-D-ASPARTATE; SCHIZOPHRENIA; SERINE ENDOPEPTIDASES; SEX CHARACTERISTICS;

EID: 84927565412     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145714000121     Document Type: Article

References (90)

1. Absil P, Pinxten R, Balthazart J, Eens M (2003) Effects of testosterone on reelin expression in the brain of male European starlings. Cell Tiss Res 312:81-93.
2. Akbarian S, Sucher NJ, Bradley D, Tafazzoli A, Trinh D, Hetrick WP, Potkin SG, Sandman CA, Bunney WE Jr., Jones EG (1996) Selective alterations in gene expression for NMDA receptor subunits in prefrontal cortex of schizophrenics. J Neurosci 16:19-30.
3. Badea A, Nicholls PJ, Johnson GA, Wetsel WC (2007) Neuroanatomical phenotypes in the reeler mouse. NeuroImage 34:1363-1374.
4. Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, Bast T, Zhang WN, Pothuizen HH, Feldon J (2004) Regional dissociations within the hippocampus-memory and anxiety. Neurosci Biobehav Rev 28:273-283.
5. Bayer TA, Falkai P, Maier W (1999) Genetic and non-genetic vulnerability factors in schizophrenia: the basis of the "two hit hypothesis". J Psychiat Res 33:543-548.
6. Beffert U, Weeber EJ, Durudas A, Qiu S, Masiulis I, Sweatt JD, Li WP, Adelmann G, Frotscher M, Hammer RE, Herz J (2005) Modulation of synaptic plasticity and memory by reelin involves differential splicing of the lipoprotein receptor Apoer2. Neuron 47:567-579.
7. Bender RA, Zhou L, Wilkars W, Fester L, Lanowski JS, Paysen D, Konig A, Rune GM (2010) Roles of 17ss-estradiol involve regulation of reelin expression and synaptogenesis in the dentate gyrus. Cereb Cortex 20:2985-2995.
8. Beneyto M, Meador-Woodruff JH (2008) Lamina-specific abnormalities of NMDA receptor-associated postsynaptic protein transcripts in the prefrontal cortex in schizophrenia and bipolar disorder. Neuropsychopharmacology 33:2175-2186.
9. Biamonte F, Assenza G, Marino R, D'Amelio M, Panteri R, Caruso D, Scurati S, Yague JG, Garcia-Segura LM, Cesa R, Strata P, Melcangi RC, Keller F (2009) Interactions between neuroactive steroids and reelin haploinsufficiency in Purkinje cell survival. Neurobiol Dis 36:103-115.
10. Bock HH, Jossin Y, Liu P, Forster E, May P, Goffinet AM, Herz J (2003) Phosphatidylinositol 3-kinase interacts with the adaptor protein Dab1 in response to reelin signaling and is required for normal cortical lamination. J Biol Chem 278:38772-38779.
11. Botella-Lopez A, Burgaya F, Gavin R, Garcia-Ayllon MS, Gomez-Tortosa E, Pena-Casanova J, Urena JM, Del Rio JA, Blesa R, Soriano E, Saez-Valero J (2006) Reelin expression and glycosylation patterns are altered in Alzheimer's disease. Proc Natl Acad Sci USA 103:5573-5578.
12. Botella-Lopez A, Cuchillo-Ibanez I, Cotrufo T, Mok SS, Li QX, Barquero MS, Dierssen M, Soriano E, Saez-Valero J (2010) Beta-amyloid controls altered reelin expression and processing in Alzheimer's disease. Neurobiol Dis 37:682-691.
13. Bradley AJ, Dinan TG (2010) A systematic review of hypothalamic-pituitary-adrenal axis function in schizophrenia: implications for mortality. J Psychopharmacol 24:91-118.
14. Brown AS (2011) The environment and susceptibility to schizophrenia. Progr Neurobiol 93:23-58.
15. Burgess LH, Handa RJ (1992) Chronic estrogen-induced alterations in adrenocorticotropin and corticosterone secretion, and glucocorticoid receptor-mediated functions in female rats. Endocrinology 131:1261-1269.
16. Chen BS, Roche KW (2009) Growth factor-dependent trafficking of cerebellar NMDA receptors via protein kinase B/Akt phosphorylation of NR2C. Neuron 62:471-478.
17. Chen Y, Beffert U, Ertunc M, Tang TS, Kavalali ET, Bezprozvanny I, Herz J (2005) Reelin modulates NMDA receptor activity in cortical neurons. J Neurosci 25:8209-8216.
18. Cull-Candy SG, Leszkiewicz DN (2004) Role of distinct NMDA receptor subtypes at central synapses. Science's STKE 2004: re16.
19. Cvoro A, Yuan C, Paruthiyil S, Miller OH, Yamamoto KR, Leitman DC (2011) Cross talk between glucocorticoid and estrogen receptors occurs at a subset of proinflammatory genes. J Immunol 186:4354-4360.
20. D'Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374:719-723.
21. D'Arcangelo G, Homayouni R, Keshvara L, Rice DS, Sheldon M, Curran T (1999) Reelin is a ligand for lipoprotein receptors. Neuron 24:471-479.
22. de Bergeyck V, Nakajima K, Lambert de Rouvroit C, Naerhuyzen B, Goffinet AM, Miyata T, Ogawa M, Mikoshiba K (1997) A truncated reelin protein is produced but not secreted in the 'Orleans' reeler mutation (Reln[rl-Orl]). Brain Res Mol Brain Res 50:85-90.
23. De Kloet ER, Vreugdenhil E, Oitzl MS, Joels M (1998) Brain corticosteroid receptor balance in health and disease. Endocr Rev 19:269-301.
24. de Kloet ER, Joels M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nature Rev Neurosci 6:463-475.
25. Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7-19.
26. Fatemi SH (2001) Reelin mutations in mouse and man: from reeler mouse to schizophrenia, mood disorders, autism and lissencephaly. Mol Psychiat 6:129-133.
27. Fatemi SH, Earle JA, McMenomy T (2000) Reduction in reelin immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorder and major depression. Mol Psychiat 5:654-663, 571.
28. Fatemi SH, Kroll JL, Stary JM (2001) Altered levels of reelin and its isoforms in schizophrenia and mood disorders. Neuroreport 12:3209-3215.
29. Fatemi SH, Reutiman TJ, Folsom TD (2009) Chronic psychotropic drug treatment causes differential expression of reelin signaling system in frontal cortex of rats. Schizophr Res 111:138-152.
30. Feldman D, Mondon CE, Horner JA, Weiser JN (1979) Glucocorticoid and estrogen regulation of corticosteroidbinding globulin production by rat liver. Am J Physiol 237: E493-E499.
31. Fernandez-Real JM, Pugeat M, Grasa M, Broch M, Vendrell J, Brun J, Ricart W (2002) Serum corticosteroid-binding globulin concentration and insulin resistance syndrome: a population study. J Clin Endocr Metab 87:4686-4690.
32. Groc L, Choquet D, Stephenson FA, Verrier D, Manzoni OJ, Chavis P (2007) NMDA receptor surface trafficking and synaptic subunit composition are developmentally regulated by the extracellular matrix protein reelin. J Neurosci 27:10165-10175.
33. Gross CM, Flubacher A, Tinnes S, Heyer A, Scheller M, Herpfer I, Berger M, Frotscher M, Lieb K, Haas CA (2012) Early life stress stimulates hippocampal reelin gene expression in a sex-specific manner: evidence for corticosterone-mediated action. Hippocampus 22:409-420.
34. Guidotti A, Auta J, Davis JM, Di-Giorgi-Gerevini V, Dwivedi Y, Grayson DR, Impagnatiello F, Pandey G, Pesold C, Sharma R, Uzunov D, Costa E (2000) Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch Gen Psychiat 57:1061-1069.
35. Hammond V, So E, Gunnersen J, Valcanis H, Kalloniatis M, Tan SS (2006) Layer positioning of late-born cortical interneurons is dependent on reelin but not p35 signaling. J Neurosci 26:1646-1655.
36. Herz J, Chen Y (2006) Reelin, lipoprotein receptors and synaptic plasticity. Nature Rev Neurosci 7:850-859.
37. Hibi T, Hattori M (2009) The N-terminal fragment of reelin is generated after endocytosis and released through the pathway regulated by Rab11. FEBS Letters 583:1299-1303.
38. Hill RA, Wu YW, Kwek P, van den Buuse M (2012) Modulatory effects of sex steroid hormones on brain-derived neurotrophic factor-tyrosine kinase B expression during adolescent development in C57Bl/6 mice. J Neuroendocr 24:774-788.
39. Hillman BG, Gupta SC, Stairs DJ, Buonanno A, Dravid SM (2011) Behavioral analysis of NR2C knockout mouse reveals deficit in acquisition of conditioned fear and working memory. Neurobiol Learning Mem 95:404-414.
40. Impagnatiello F, Guidotti AR, Pesold C, Dwivedi Y, Caruncho H, Pisu MG, Uzunov DP, Smalheiser NR, Davis JM, Pandey GN, Pappas GD, Tueting P, Sharma RP, Costa E (1998) A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proc Natl Acad Sci USA 95:15718-15723.
41. Jafari M, Seese RR, Babayan AH, Gall CM, Lauterborn JC (2012) Glucocorticoid receptors are localized to dendritic spines and influence local actin signaling. Mol Neurobiol 46:304-315.
42. Joels M, Pu Z, Wiegert O, Oitzl MS, Krugers HJ (2006) Learning under stress: how does it work? Trends Cogn Sci 10:152-158.
43. Jones BC, Sarrieau A, Reed CL, Azar MR, Mormede P (1998) Contribution of sex and genetics to neuroendocrine adaptation to stress in mice. Psychoneuroendocrinol 23:505-517.
44. Jossin Y, Ignatova N, Hiesberger T, Herz J, Lambert de Rouvroit C, Goffinet AM (2004) The central fragment of reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. J Neurosci 24:514-521.
45. Jossin Y, Gui L, Goffinet AM (2007) Processing of reelin by embryonic neurons is important for function in tissue but not in dissociated cultured neurons. J Neurosci 27:4243-4252.
46. Karatsoreos IN, Bhagat SM, Bowles NP, Weil ZM, Pfaff DW, McEwen BS (2010) Endocrine and physiological changes in response to chronic corticosterone: a potential model of the metabolic syndrome in mouse. Endocrinology 151:2117-2127.
47. Karavanova I, Vasudevan K, Cheng J, Buonanno A (2007) Novel regional and developmental NMDA receptor expression patterns uncovered in NR2C subunit-beta-galactosidase knock-in mice. Mol Cell Neurosci 34:468-480.
48. Khashan AS, Abel KM, McNamee R, Pedersen MG, Webb RT, Baker PN, Kenny LC, Mortensen PB (2008) Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiat 65:146-152.
49. Klug M, van den Buuse M (2013) An investigation into "two hit" effects of BDNF deficiency and young-adult cannabinoid receptor stimulation on prepulse inhibition regulation and memory in mice. Front Behav Neurosci 7:149.
50. Klug M, Hill RA, Choy KH, Kyrios M, Hannan AJ, van den Buuse M (2012) Long-term behavioral and NMDA receptor effects of young-adult corticosterone treatment in BDNF heterozygous mice. Neurobiol Dis 46:722-731.
51. Kohno S, Kohno T, Nakano Y, Suzuki K, Ishii M, Tagami H, Baba A, Hattori M (2009) Mechanism and significance of specific proteolytic cleavage of reelin. Biochem Biophys Res Comm 380:93-97.
52. Krishnan AV, Swami S, Feldman D (2001) Estradiol inhibits glucocorticoid receptor expression and induces glucocorticoid resistance in MCF-7 human breast cancer cells. J Steroid Biochem Mol Biol 77:29-37.
53. Kubo K, Mikoshiba K, Nakajima K (2002) Secreted reelin molecules form homodimers. Neurosci Res 43:381-388.
54. Kutiyanawalla A, Promsote W, Terry A, Pillai A (2012) Cysteamine treatment ameliorates alterations in GAD67 expression and spatial memory in heterozygous reeler mice. Int J Neuropsychopharmacol 15:1073-1086.
55. Lambert de Rouvroit C, de Bergeyck V, Cortvrindt C, Bar I, Eeckhout Y, Goffinet AM (1999) Reelin, the extracellular matrix protein deficient in reeler mutant mice, is processed by a metalloproteinase. Exp Neurol 156:214-217.
56. Levenson JM, Qiu S, Weeber EJ (2008) The role of reelin in adult synaptic function and the genetic and epigenetic regulation of the reelin gene. Biochim Biophys Acta 1779:422-431.
57. Lewis JG, Bagley CJ, Elder PA, Bachmann AW, Torpy DJ (2005) Plasma free cortisol fraction reflects levels of functioning corticosteroid-binding globulin. Clinica Chimica Acta; Intern J Clin Chem 359:189-194.
58. Liu WS, Pesold C, Rodriguez MA, Carboni G, Auta J, Lacor P, Larson J, Condie BG, Guidotti A, Costa E (2001) Down-regulation of dendritic spine and glutamic acid decarboxylase 67 expressions in the reelin haploinsufficient heterozygous reeler mouse. Proc Natl Acad Sci USA 98:3477-3482.
59. Lussier AL, Romay-Tallon R, Kalynchuk LE, Caruncho HJ (2011) Reelin as a putative vulnerability factor for depression: examining the depressogenic effects of repeated corticosterone in heterozygous reeler mice. Neuropharmacology 60:1064-1074.
60. Maynard TM, Sikich L, Lieberman JA, LaMantia AS (2001) Neural development, cell-cell signaling, and the "two-hit" hypothesis of schizophrenia. Schizophr Bull 27:457-476.
61. McCormick CM, Mathews IZ (2007) HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol Biochem Behav 86:220-233.
62. Meyer U, Feldon J (2010) Epidemiology-driven neurodevelopmental animal models of schizophrenia. Progr Neurobiol 90:285-326.
63. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540.
64. Morimura T, Hattori M, Ogawa M, Mikoshiba K (2005) Disabled1 regulates the intracellular trafficking of reelin receptors. J Biol Chem 280:16901-16908.
65. Moser MB, Moser EI (1998) Functional differentiation in the hippocampus. Hippocampus 8:608-619.
66. Nakamura NH, McEwen BS (2005) Changes in interneuronal phenotypes regulated by estradiol in the adult rat hippocampus: a potential role for neuropeptide Y. Neuroscience 136:357-369.
67. Nakazawa K, Zsiros V, Jiang Z, Nakao K, Kolata S, Zhang S, Belforte JE (2012) GABAergic interneuron origin of schizophrenia pathophysiology. Neuropharmacology 62:1574-1583.
68. Nullmeier S, Panther P, Dobrowolny H, Frotscher M, Zhao S, Schwegler H, Wolf R (2011) Region-specific alteration of GABAergic markers in the brain of heterozygous reeler mice. Eur J Neurosci 33:689-698.
69. Paoletti P (2011) Molecular basis of NMDA receptor functional diversity. Eur J Neurosci 33:1351-1365.
70. Pillai A, Mahadik SP (2008) Increased truncated TrkB receptor expression and decreased BDNF/TrkB signaling in the frontal cortex of reeler mouse model of schizophrenia. Schizophr Res 100:325-333.
71. Robertson DA, Beattie JE, Reid IC, Balfour DJ (2005) Regulation of corticosteroid receptors in the rat brain: the role of serotonin and stress. Eur J Neurosci 21:1511-1520.
72. Rodriguez MA, Pesold C, Liu WS, Kriho V, Guidotti A, Pappas GD, Costa E (2000) Colocalization of integrin receptors and reelin in dendritic spine postsynaptic densities of adult nonhuman primate cortex. Proc Natl Acad Sci USA 97:3550-3555.
73. Romeo RD, Kaplowitz ET, Ho A, Franco D (2012) The influence of puberty on stress reactivity and forebrain glucocorticoid receptor levels in inbred and outbred strains of male and female mice. Psychoneuroendocrinology 38:592-596.
74. Romero Mdel M, Holmgren-Holm F, Grasa Mdel M, Esteve M, Remesar X, Fernandez-Lopez JA, Alemany M (2013) Modulation in Wistar rats of blood corticosterone compartmentation by sex and a cafeteria diet. PloS ONE 8:e57342.
75. Schlosser DA, Pearson R, Perez VB, Loewy RL (2012) Environmental risk and protective factors and their influence on the emergence of psychosis. Adol Psychiat 2:163-171.
76. Schmitt A, Koschel J, Zink M, Bauer M, Sommer C, Frank J, Treutlein J, Schulze T, Schneider-Axmann T, Parlapani E, Rietschel M, Falkai P, Henn FA (2010) Gene expression of NMDA receptor subunits in the cerebellum of elderly patients with schizophrenia. Eur Arch Psychiat Clin Neurosci 260:101-111.
77. Sinagra M, Verrier D, Frankova D, Korwek KM, Blahos J, Weeber EJ, Manzoni OJ, Chavis P (2005) Reelin, very-low-density lipoprotein receptor, and apolipoprotein E receptor 2 control somatic NMDA receptor composition during hippocampal maturation in vitro. J Neurosci 25:6127-6136.
78. Stranahan AM, Erion JR, Wosiski-Kuhn M (2013) Reelin signaling in development, maintenance, and plasticity of neural networks. Ageing Res Rev 12:815-822.
79. Tamminga CA, Holcomb HH (2005) Phenotype of schizophrenia: a review and formulation. Mol Psychiat 10:27-39.
80. Tse YC, Bagot RC, Wong TP (2012) Dynamic regulation of NMDAR function in the adult brain by the stress hormone corticosterone. Front Cell Neurosci 6:9.
81. Tueting P, Costa E, Dwivedi Y, Guidotti A, Impagnatiello F, Manev R, Pesold C (1999) The phenotypic characteristics of heterozygous reeler mouse. Neuroreport 10:1329-1334.
82. Tueting P, Doueiri MS, Guidotti A, Davis JM, Costa E (2006) Reelin down-regulation in mice and psychosis endophenotypes. Neurosci Biobehav Rev 30:1065-1077.
83. Utsunomiya-Tate N, Kubo K, Tate S, Kainosho M, Katayama E, Nakajima K, Mikoshiba K (2000) Reelin molecules assemble together to form a large protein complex, which is inhibited by the function-blocking CR-50 antibody. Proc Natl Acad Sci USA 97:9729-9734.
84. van den Buuse M, Morris M, Chavez C, Martin S, Wang J (2004) Effect of adrenalectomy and corticosterone replacement on prepulse inhibition and locomotor activity in mice. Brit J Pharmacol 142:543-550.
85. van den Buuse M, Halley P, Hill R, Labots M, Martin S (2012) Altered N-methyl-D-aspartate receptor function in reelin heterozygous mice: male-female differences and comparison with dopaminergic activity. Progr Neuro-psychopharmacol Biol Psychiat 37:237-246.
86. Ventruti A, Kazdoba TM, Niu S, D'Arcangelo G (2011) Reelin deficiency causes specific defects in the molecular composition of the synapses in the adult brain. Neuroscience 189:32-42.
87. Viau V, Sharma S, Meaney MJ (1996) Changes in plasma adrenocorticotropin, corticosterone, corticosteroid-binding globulin, and hippocampal glucocorticoid receptor occupancy/translocation in rat pups in response to stress. J Neuroendocrinol 8:1-8.
88. Walder DJ, Walker EF, Lewine RJ (2000) Cognitive functioning, cortisol release, and symptom severity in patients with schizophrenia. Biol Psychiat 48:1121-1132.
89. Webster MJ, Knable MB, O'Grady J, Orthmann J, Weickert CS (2002) Regional specificity of brain glucocorticoid receptor mRNA alterations in subjects with schizophrenia and mood disorders. Mol Psychiat 7:985-994, 924.
90. Xi D, Keeler B, Zhang W, Houle JD, Gao WJ (2009) NMDA receptor subunit expression in GABAergic interneurons in the prefrontal cortex: application of laser microdissection technique. J Neurosci Meth 176:172-181.