Differential subcellular localization of the glucocorticoid receptor in distinct neural stem and progenitor populations of the mouse telencephalon in vivo

Brain Research

Volumn 1523, Issue , 2013, Pages 10-27

  Tsiarli, Maria A ^a,b   Paula Monaghan, A ^a   Defranco, Donald B ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Cortex; Embryo; Glucocorticoid receptor; Neural stem progenitor cells; Neurodevelopment

Indexed keywords

GLUCOCORTICOID RECEPTOR;

ANIMAL CELL; ARTICLE; CELL POPULATION; CELLULAR DISTRIBUTION; CYTOPLASM; FEMALE; GLIA CELL; HIPPOCAMPUS; MOUSE; NEURAL STEM CELL; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUBVENTRICULAR ZONE; TELENCEPHALON;

4′,6-DIAMIDINO-2-PHENYLINDOLE; APICAL VENTRICULAR ZONE; AVZ; BASAL VENTRICULAR ZONE; BVZ; CORTEX; DAPI; E11.5; EMBRYO; EMBRYONIC DAY 11.5; GCS; GLUCOCORTICOID RECEPTOR; GLUCOCORTICOIDS; GR; IIF; INDIRECT IMMUNOFLUORESCENCE; INTERMEDIATE PROGENITOR CELLS; IPCS; NEURAL STEM/PROGENITOR CELLS; NEURODEVELOPMENT; NEURON-SPECIFIC CLASS III BETA-TUBULIN; NSPCS; PAIRED BOX PROTEIN 6; PAX6; RADIAL GLIAL CELLS; RGCS; T-BOX BRAIN PROTEIN 2 (EOMESODERMIN); TBR2; TUJ1;

ANIMALS; CEREBRAL CORTEX; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICE; NEURAL STEM CELLS; NEUROGLIA; PREGNANCY; RECEPTORS, GLUCOCORTICOID; STEM CELLS; SUBCELLULAR FRACTIONS; TELENCEPHALON;

EID: 84879838840     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.06.001     Document Type: Article

References (68)

1. S. Assimacopoulos, E.A. Grove, and C.W. Ragsdale Identification of a Pax6-dependent epidermal growth factor family signaling source at the lateral edge of the embryonic cerebral cortex J. Neurosci. 23 2003 6399 6403
2. I. Bombin Neuropsychological evidence for abnormal neurodevelopment associated with early-onset psychoses Psychol. Med. 2012 1 12
3. V.S. Caviness Jr.; R.S. Nowakowski, and P.G. Bhide Neocortical neurogenesis: morphogenetic gradients and beyond Trends Neurosci. 32 2009 443 450
4. A. Cintra Prenatal development of glucocorticoid receptor gene expression and immunoreactivity in the rat brain and pituitary gland: a combined in situ hybridization and immunocytochemical analysis Neuroendocrinology 57 1993 1133 1147
5. B. Czeh Chronic stress decreases the number of parvalbumin-immunoreactive interneurons in the hippocampus: prevention by treatment with a substance P receptor (NK1) antagonist Neuropsychopharmacology 30 2005 67 79
6. J. Dahlstrand, M. Lardelli, and U. Lendahl Nestin mRNA expression correlates with the central nervous system progenitor cell state in many, but not all, regions of developing central nervous system Brain Res. Dev. Brain Res. 84 1995 109 129
7. D. Duan Spatiotemporal expression patterns of Pax6 in the brain of embryonic, newborn, and adult mice Brain Struct. Funct. 218 2013 353 372
8. C. Englund Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex J. Neurosci. 25 2005 247 251
9. C.P. Fitzsimons The microtubule-associated protein doublecortin-like regulates the transport of the glucocorticoid receptor in neuronal progenitor cells Mol. Endocrinol. 22 2008 248 262
10. K. Fukumoto Detrimental effects of glucocorticoids on neuronal migration during brain development Mol. Psychiatry 14 2009 1119 1131
11. A.J. Galliher-Beckley, and J.A. Cidlowski Emerging roles of glucocorticoid receptor phosphorylation in modulating glucocorticoid hormone action in health and disease IUBMB Life 61 2009 979 986
12. A.J. Galliher-Beckley, J.G. Williams, and J.A. Cidlowski Ligand-independent phosphorylation of the glucocorticoid receptor integrates cellular stress pathways with nuclear receptor signaling Mol. Cell. Biol. 31 2011 4663 4675
13. B. Gametchu, and R.W. Harrison Characterization of a monoclonal antibody to the rat liver glucocorticoid receptor Endocrinology 114 1984 274 279
14. J.C. Garza Leptin restores adult hippocampal neurogenesis in a chronic unpredictable stress model of depression and reverses glucocorticoid-induced inhibition of GSK-3beta/beta-catenin signaling Mol. Psychiatry 17 2011 790 808
15. S. Gong A gene expression atlas of the central nervous system based on bacterial artificial chromosomes Nature 425 2003 917 925
16. M. Gotz, and W.B. Huttner The cell biology of neurogenesis Nat. Rev. Mol. Cell. Biol. 6 2005 777 788
17. E. Gould Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation J. Neurosci. 17 1997 2492 2498
18. S.J. Harrison, R. Nishinakamura, and A.P. Monaghan Sall1regulates mitral cell development and olfactory nerve extension in the developing olfactory bulb Cereb. Cortex 18 2008 1604 1617
19. V.M. Heine, and D.H. Rowitch Hedgehog signaling has a protective effect in glucocorticoid-induced mouse neonatal brain injury through an 11βHSD2-dependent mechanism J. Clin. Invest. 119 2009 267 277
20. V.M. Heine Dexamethasone destabilizes Nmyc to inhibit the growth of hedgehog-associated medulloblastoma Cancer Res. 70 2010 5220 5225
21. N. Heintz Gene expression nervous system atlas (GENSAT) Nat. Neurosci. 7 2004 483
22. J.W. Hinds Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia J. Comp. Neurol. 134 1968 287 304
23. J.W. Hinds Early neuron differentiation in the mouse of olfactory bulb. I. Light microscopy J. Comp. Neurol. 146 1972 233 252
24. S. Hirai MAPK-upstream protein kinase (MUK) regulates the radial migration of immature neurons in telencephalon of mouse embryo Development 129 2002 4483 4495
25. L.-T. Huang The link between perinatal glucocorticoids exposure and psychiatric disorders Pediatr. Res. 69 2011 19R 25R
26. L. Khozhai, and V. Otellin Formation of neocortex and hippocampal structures after single action of dexamethasone during prenatal period of rat development J. Evol. Biochem. Physiol. 44 2008 528 531
27. J.B. Kim Dexamethasone inhibits proliferation of adult hippocampal neurogenesis in vivo and in vitro Brain Res. 1027 2004 1 10
28. E. Kitraki Glucocorticoid receptor gene expression in the embryonic rat brain Neuroendocrinology 63 1996 305 317
29. A. Kriegstein, and A. Alvarez-Buylla The glial nature of embryonic and adult neural stem cells Annu. Rev. Neurosci. 32 2009 149 184
30. K.Y. Kwan, N. Sestan, and E.S. Anton Transcriptional co-regulation of neuronal migration and laminar identity in the neocortex Development 139 2012 1535 1546
31. G.C. Liggins Premature delivery of foetal lambs infused with glucocorticoids J. Endocrinol. 45 1969 515 523
32. G.C. Liggins, and R.N. Howie A controlled trial of antepartum glucocorticoid treatment for prevention of the respiratory distress syndrome in premature infants Pediatrics 50 1972 515 525
33. S.J. Lupien Effects of stress throughout the lifespan on the brain, behaviour and cognition Nat. Rev. Neurosci. 10 2009 434 445
34. A.P. Madan, and D.B. DeFranco Bidirectional transport of glucocorticoid receptors across the nuclear envelope Proc. Natl. Acad. Sci. U. S. A. 90 1993 3588 3592
35. B.S. McEwen Glucocorticoids, depression, and mood disorders: structural remodeling in the brain Metabolism 54 2005 20 23
36. W.L. McKenna Tbr1 and Fezf2 regulate alternate corticofugal neuronal identities during neocortical development J. Neurosci. 31 2011 549 564
37. A.R. Mesquita Glucocorticoids and neuro- and behavioural development Semin. Fetal. Neonatal. Med. 14 2009 130 135
38. N. Modi The effects of repeated antenatal glucocorticoid therapy on the developing brain Pediatr. Res. 50 2001 581 585
39. A. Patel, and K. Bulloch Type II glucocorticoid receptor immunoreactivity in the mossy cells of the rat and the mouse hippocampus Hippocampus 13 2003 59 66
40. A. Pekki Subcellular location of unoccupied and occupied glucocorticoid receptor by a new immunohistochemical technique J. Steroid Biochem. Mol. Biol. 41 1992 753 756
41. A. Pontious Role of intermediate progenitor cells in cerebral cortex development Dev. Neurosci. 30 2008 24 32
42. J.N. Pulvers, and W.B. Huttner Brca1 is required for embryonic development of the mouse cerebral cortex to normal size by preventing apoptosis of early neural progenitors Development 136 2009 1859 1868
43. I.B. Purdy Cumulative perinatal steroids: child development of preterm infants J. Pediatr. Nurs. 23 2008 201 214
44. M. Qi, B.J. Hamilton, and D. DeFranco v-mos oncoproteins affect the nuclear retention and reutilization of glucocorticoid receptors Mol. Endocrinol. 3 1989 1279 1288
45. P. Rakic Specification of cerebral cortical areas Science 241 1988 170 176
46. H.M. Reichardt, and G. Schutz Feedback control of glucocorticoid production is established during fetal development Mol. Med. 2 1996 735 744
47. R. Reimer Nestin modulates glucocorticoid receptor function by cytoplasmic anchoring PLoS One 4 2009 e6084
48. R.M. Reynolds, and J.R. Seckl Antenatal glucocorticoid treatment: are we doing harm to term babies? J. Clin. Endocrinol. Metab. 97 2012 3457 3459
49. H.D. Ritter, L. Antonova, and C.R. Mueller The unliganded glucocorticoid receptor positively regulates the tumor suppressor gene BRCA1 through GABP beta Mol. Cancer Res. 10 2012 558 569
50. S.A. Rivkees, and J.D. Crawford Dexamethasone treatment of virilizing congenital adrenal hyperplasia: the ability to achieve normal growth Pediatrics 106 2000 767 773
51. D. Roberts, and S. Dalziel Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth Cochrane Database Syst. Rev. CD004454 2006
52. R.A. Samarasinghe Nongenomic glucocorticoid receptor action regulates gap junction intercellular communication and neural progenitor cell proliferation Proc. Natl. Acad. Sci. U. S. A. 108 2011 16657 16662
53. R.A. Sarabdjitsingh, O.C. Meijer, and E.R. de Kloet Specificity of glucocorticoid receptor primary antibodies for analysis of receptor localization patterns in cultured cells and rat hippocampus Brain Res. 1331 2010 1 11
54. C.A. Schneider, W.S. Rasband, and K.W. Eliceiri NIH Image to ImageJ: 25 years of image analysis Nat. Methods 9 2012 671 675
55. M. Shimada, and J. Langman Cell proliferation, migration and differentiation in the cerebral cortex of the golden hamster J. Comp. Neurol. 139 1970 227 244
56. E. Soriano, A. Cobas, and A. Fairen Neurogenesis of glutamic acid decarboxylase immunoreactive cells in the hippocampus of the mouse. II: area dentata J. Comp. Neurol. 281 1989 603 611
57. E. Soriano, A. Cobas, and A. Fairen Neurogenesis of glutamic acid decarboxylase immunoreactive cells in the hippocampus of the mouse. I: regio superior and regio inferior J. Comp. Neurol. 281 1989 586 602
58. H.J. Speirs, J.R. Seckl, and R.W. Brown Ontogeny of glucocorticoid receptor and 11beta-hydroxysteroid dehydrogenase type-1 gene expression identifies potential critical periods of glucocorticoid susceptibility during development J. Endocrinol. 181 2004 105 116
59. E.K. Stancik Heterogeneity in ventricular zone neural precursors contributes to neuronal fate diversity in the postnatal neocortex J. Neurosci. 30 2010 7028 7036
60. Q. Tang A comprehensive view of nuclear receptor cancer cistromes Cancer Res. 71 2011 6940 6947
61. S. Tekin, and J.L. Cummings Frontal-subcortical neuronal circuits and clinical neuropsychiatry: an update J. Psychosom. Res. 53 2002 647 654
62. J.A. Thorp Does antenatal corticosteroid therapy affect birth weight and head circumference? Obstet. Gynecol. 99 2002 101 108
63. H. Uno Brain damage induced by prenatal exposure to dexamethasone in fetal rhesus macaques. I. Hippocampus Brain Res. Dev. Brain Res. 53 1990 157 167
64. H. Uno Neurotoxicity of glucocorticoids in the primate brain Horm. Behav. 28 1994 336 348
65. T. Usuku Visualization of glucocorticoid receptor in the brain of green fluorescent protein-glucocorticoid receptor knockin mice Neuroscience 135 2005 1119 1128
66. S. Vandevyver, L. Dejager, and C. Libert On the trail of the glucocorticoid receptor: into the nucleus and back Traffic 13 2011 364 374
67. M. Venihaki Circadian rise in maternal glucocorticoid prevents pulmonary dysplasia in fetal mice with adrenal insufficiency Proc. Natl. Acad. Sci. U. S. A. 97 2000 7336 7341
68. L.A. Welberg, and J.R. Seckl Prenatal stress, glucocorticoids and the programming of the brain J. Neuroendocrinol. 13 2001 113 128