Juvenile separation stress induces rapid region- and layer-specific changes in S100ß- and glial fibrillary acidic protein-immunoreactivity in astrocytes of the rodent medial prefrontal cortex

Neuroscience

Volumn 160, Issue 3, 2009, Pages 629-638

  Braun, K ^a   Antemano, R ^a   Helmeke, C ^a   Buchner M ^b   Poeggel, G ^b  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

cytoskeletal reorganization; development; glia; limbic cortex; Octodon degus

Indexed keywords

ACID CITRATE DEXTROSE; GLIAL FIBRILLARY ACIDIC PROTEIN; PROTEIN S100B;

ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CONTROLLED STUDY; GLIA CELL; IMMUNOREACTIVITY; JUVENILE; NONHUMAN; OCTODON; PLASTICITY; PREFRONTAL CORTEX; PRIORITY JOURNAL; REUNION; RODENT; SOMATOSENSORY CORTEX; STATISTICAL SIGNIFICANCE; STRESS; UPREGULATION;

ANALYSIS OF VARIANCE; ANIMALS; ASTROCYTES; CELL COUNT; FAMILY RELATIONS; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOENZYME TECHNIQUES; IMMUNOHISTOCHEMISTRY; LIMBIC SYSTEM; MALE; OCTODON; PREFRONTAL CORTEX; RATS; S100 PROTEINS; SOCIAL ISOLATION; SOMATOSENSORY CORTEX; STRESS, PSYCHOLOGICAL;

EID: 64449089015     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.02.074     Document Type: Article

References (56)

1. Abnet K., Fawcett J.W., and Dunnett S.B. Interactions between meningeal cells and astrocytes in vivo and in vitro. Brain Res Dev Brain Res 59 (1991) 187-196
2. Azmitia E.C. Cajal's hypotheses on neurobiones and neurotropic factor match properties of microtubules and S-100 beta. Prog Brain Res 136 (2002) 87-100
3. Barros V.G., Duhalde-Vega M., Caltana L., Brusco A., and Antonelli M.C. Astrocyte-neuron vulnerability to prenatal stress in the adult rat brain. J Neurosci Res 83 (2006) 787-800
4. Braun K., Lange E., Metzger M., and Poeggel G. Maternal separation followed by early social deprivation affects the development of monoaminergic fiber systems in the medial prefrontal cortex of Octodon degus. Neuroscience 95 (2000) 309-318
5. Bredy T.W., Grant R.J., Champagne D.L., and Meaney M.J. Maternal care influences neuronal survival in the hippocampus of the rat. Eur J Neurosci 18 (2003) 2903-2909
6. Bushong E.A., Martone M.E., and Ellisman M.H. Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development. Int J Dev Neurosci 22 (2004) 73-86
7. Chang M.S., Ariah L.M., Marks A., and Azmitia E.C. Chronic gliosis induced by loss of S-100B: knockout mice have enhanced GFAP-immunoreactivity but blunted response to a serotonin challenge. Brain Res 1031 (2005) 1-9
8. Corvetti L., Capsoni S., Cattaneo A., and Domenici L. Postnatal development of GFAP in mouse visual cortex is not affected by light deprivation. Glia 41 (2003) 404-414
9. Donato R. Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim Biophys Acta 1450 (1999) 191-231
10. Eng L.F., Ghirnikar R.S., and Lee Y.L. Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem Res 25 (2000) 1439-1451
11. Freeman M.R. Sculpting the nervous system: glial control of neuronal development. Curr Opin Neurobiol 16 (2006) 119-125
12. Garbuglia M., Verzini M., Sorci G., Bianchi R., Giambanco I., Agneletti A.L., and Donato R. The calcium-modulated proteins, S100A1 and S100B, as potential regulators of the dynamics of type III intermediate filaments. Braz J Med Biol Res 32 (1999) 1177-1185
13. Hafidi A., and Galifianakis D. Macroglia distribution in the developing and adult inferior colliculus. Brain Res Dev Brain Res 143 (2003) 167-177
14. Hawrylak N., Fleming J.C., and Salm A.K. Dehydration and rehydration selectively and reversibly alter glial fibrillary acidic protein immunoreactivity in the rat supraoptic nucleus and subjacent glial limitans. Glia 22 (1998) 260-271
15. Heizmann C.W. The multifunctional S100 protein family. Methods Mol Biol 172 (2002) 69-80
16. Heizmann C.W., Fritz G., and Schafer B.W. S100 proteins: structure, functions and pathology. Front Biosci 7 (2002) d1356-d1368
17. Helmeke C., Ovtscharoff Jr. W., Poeggel G., and Braun K. Juvenile emotional experience alters synaptic inputs on pyramidal neurons in the anterior cingulate cortex. Cereb Cortex 11 (2001) 717-727
18. Herrmann H., and Aebi U. Intermediate filaments: molecular structure, assembly mechanism, and integration into functionally distinct intracellular scaffolds. Annu Rev Biochem 73 (2004) 749-789
19. Horner P.J., Power A.E., Kempermann G., Kuhn H.G., Palmer T.D., Winkler J., Thal L.J., and Gage F.H. Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurol Sci 20 (2000) 2218-2228
20. Jones T.A., and Greenough W.T. Ultrastructural evidence for increased contact between astrocytes and synapses in rats reared in a complex environment. Neurobiol Learn Mem 65 (1996) 48-56
21. Jones T.A., Hawrylak N., and Greenough W.T. Rapid laminar-dependent changes in GFAP immunoreactive astrocytes in the visual cortex of rats reared in a complex environment. Psychoneuroendocrinology 21 (1996) 189-201
22. Kaplan M.S., and Hinds J.W. Gliogenesis of astrocytes and oligodendrocytes in the neocortical grey and white matter of the adult rat: electron microscopic analysis of light radioautographs. J Comp Neurol 193 (1980) 711-727
23. Landry C.F., Ivy G.O., and Brown I.R. Developmental expression of glial fibrillary acidic protein mRNA in the rat brain analyzed by in situ hybridization. J Neurosci Res 25 (1990) 194-203
24. Langle S.L., Poulain D.A., and Theodosis D.T. Neuronal-glial remodeling: a structural basis for neuronal-glial interactions in the adult hypothalamus. J Physiol Paris 96 (2002) 169-175
25. Laping N.J., Nichols N.R., Day J.R., Johnson S.A., and Finch C.E. Transcriptional control of glial fibrillary acidic protein and glutamine synthetase in vivo shows opposite responses to corticosterone in the hippocampus. Endocrinology 135 (1994) 1928-1933
26. Levitt P., and Rakic P. Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J Comp Neurol 193 (1980) 815-840
27. Lewis S.A., and Cowan N.J. Temporal expression of mouse glial fibrillary acidic protein mRNA studied by a rapid in situ hybridization procedure. J Neurochem 45 (1985) 913-919
28. Margis R., Zanatto V.C., Tramontina F., Vinade E., Lhullier F., Portela L.V., Souza D.O., Dalmaz C., Kapczinski F., and Goncalves C.A. Changes in S100B cerebrospinal fluid levels of rats subjected to predator stress. Brain Res 1028 (2004) 213-218
29. Matsutani S., and Leon M. Elaboration of glial cell processes in the rat olfactory bulb associated with early learning. Brain Res 613 (1993) 317-320
30. McAdory B.S., Van Eldik L.J., and Norden J.J. S100B, a neurotropic protein that modulates neuronal protein phosphorylation, is upregulated during lesion-induced collateral sprouting and reactive synaptogenesis. Brain Res 813 (1998) 211-217
31. McCarthy G.F., and Leblond C.P. Radioautographic evidence for slow astrocyte turnover and modest oligodendrocyte production in the corpus callosum of adult mice infused with 3H-thymidine. J Comp Neurol 271 (1988) 589-603
32. McLendon R.E., and Bigner D.D. Immunohistochemistry of the glial fibrillary acidic protein: basic and applied considerations. Brain Pathol 4 (1994) 221-228
33. Missler M., Eins S., Bottcher H., and Wolff J.R. Postnatal development of glial fibrillary acidic protein, vimentin and S100 protein in monkey visual cortex: evidence for a transient reduction of GFAP immunoreactivity. Brain Res Dev Brain Res 82 (1994) 103-117
34. Musholt K., Cirillo G., Cavaliere C., Rosaria Bianco M., Bock J., Helmeke C., Braun K., and Papa M. Neonatal separation stress reduces glial fibrillary acidic protein- and S100beta-immunoreactive astrocytes in the rat medial precentral cortex. Dev Neurobiol 69 (2009) 203-211
35. Nadarajah B. Radial glia and somal translocation of radial neurons in the developing cerebral cortex. Glia 43 (2003) 33-36
36. Nichols N.R., Masters J.N., and Finch C.E. Changes in gene expression in hippocampus in response to glucocorticoids and stress. Brain Res Bull 24 (1990) 659-662
37. Nichols N.R., Osterburg H.H., Masters J.N., Millar S.L., and Finch C.E. Messenger RNA for glial fibrillary acidic protein is decreased in rat brain following acute and chronic corticosterone treatment. Brain Res Mol Brain Res 7 (1990) 1-7
38. O'Callaghan J.P., Brinton R.E., and McEwen B.S. Glucocorticoids regulate the synthesis of glial fibrillary acidic protein in intact and adrenalectomized rats but do not affect its expression following brain injury. J Neurochem 57 (1991) 860-869
39. Oliet S.H., Piet R., Poulain D.A., and Theodosis D.T. Glial modulation of synaptic transmission: insights from the supraoptic nucleus of the hypothalamus. Glia 47 (2004) 258-267
40. Oudega M., and Marani E. Expression of vimentin and glial fibrillary acidic protein in the developing rat spinal cord: an immunocytochemical study of the spinal cord glial system. J Anat 179 (1991) 97-114
41. Ovtscharoff W., and Braun K. Maternal separation and social isolation modulate the postnatal development of synaptic composition in the infralimbic cortex of Octodon degus. Neuroscience 104 (2001) 33-40
42. Pekny M., and Nilsson M. Astrocyte activation and reactive gliosis. Glia 50 (2005) 427-434
43. Pinto S.S., Gottfried C., Mendez A., Goncalves D., Karl J., Goncalves C.A., Wofchuk S., and Rodnight R. Immunocontent and secretion of S100B in astrocyte cultures from different brain regions in relation to morphology. FEBS Lett 486 (2000) 203-207
44. Poeggel G., Helmeke C., Abraham A., Schwabe T., Friedrich P., and Braun K. Juvenile emotional experience alters synaptic composition in the rodent cortex, hippocampus, and lateral amygdala. Proc Natl Acad Sci U S A 100 (2003) 16137-16142
45. Reynolds T.J., and Wright J.W. Early postnatal physical and behavioural development of degus (Octodon degus). Lab Anim 13 (1979) 93-100
46. Rothermundt M., Peters M., Prehn J.H., and Arolt V. S100B in brain damage and neurodegeneration. Microsc Res Tech 60 (2003) 614-632
47. Rozovsky I., Laping N.J., Krohn K., Teter B., O'Callaghan J.P., and Finch C.E. Transcriptional regulation of glial fibrillary acidic protein by corticosterone in rat astrocytes in vitro is influenced by the duration of time in culture and by astrocyte-neuron interactions. Endocrinology 136 (1995) 2066-2073
48. Scaccianoce S., Del Bianco P., Pannitteri G., and Passarelli F. Relationship between stress and circulating levels of S100B protein. Brain Res 1004 (2004) 208-211
49. Sirevaag A.M., and Greenough W.T. Plasticity of GFAP-immunoreactive astrocyte size and number in visual cortex of rats reared in complex environments [published erratum appears in brain Res 1991 Nov 22, 565(1):179]. Brain Res 540 (1991) 273-278
50. Stone D.J., Song Y., Anderson C.P., Krohn K.K., Finch C.E., and Rozovsky I. Bidirectional transcription regulation of glial fibrillary acidic protein by estradiol in vivo and in vitro. Endocrinology 139 (1998) 3202-3209
51. Theodosis D.T., Piet R., Poulain D.A., and Oliet S.H. Neuronal, glial and synaptic remodeling in the adult hypothalamus: functional consequences and role of cell surface and extracellular matrix adhesion molecules. Neurochem Int 45 (2004) 491-501
52. Theodosis D.T., Poulain D.A., and Vincent J.D. Neuronal-glial interactions and synaptic remodelling in the control of magnocellular neurosecretory activity. In: Imura H. (Ed). Neuroendocrine control of the hypothalamo-pituitary system (1988), Japan Scientific Society Press, S. Karger, Tokyo 183-200
53. Tiu S.C., Chan W.Y., Heizmann C.W., Schafer B.W., Shu S.Y., and Yew D.T. Differential expression of S100B and S100A6(1) in the human fetal and aged cerebral cortex. Brain Res Dev Brain Res 119 (2000) 159-168
54. Tsuneishi S., Takada S., Motoike T., Ohashi T., Sano K., and Nakamura H. Effects of dexamethasone on the expression of myelin basic protein, proteolipid protein, and glial fibrillary acidic protein genes in developing rat brain. Brain Res Dev Brain Res 61 (1991) 117-123
55. Volterra A., and Meldolesi J. Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6 (2005) 626-640
56. Ziegler D.R., Innocente C.E., Leal R.B., Rodnight R., and Goncalves C.A. The S100B protein inhibits phosphorylation of GFAP and vimentin in a cytoskeletal fraction from immature rat hippocampus. Neurochem Res 23 (1998) 1259-1263