No long-term effect two years after intrauterine exposure to dexamethasone on dentate gyrus volume, neuronal proliferation and differentiation in common marmoset monkeys

Brain Pathology

Volumn 18, Issue 4, 2008, Pages 497-503

  Tauber, Simone C ^a   Bunkowski, Stephanie ^a   Schlumbohm, Christina ^b   Rühlmann, Malte ^a   Fuchs, Eberhard ^b   Nau, Roland ^a   Gerber, Joachim ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b GERMAN PRIMATE CENTER   (Germany)

Author keywords

Dentate gyrus; Marmoset; Neurogenesis; Prenatal dexamethasone; Progenitor cell proliferation

Indexed keywords

CALRETININ; DEXAMETHASONE; MEMBRANE PROTEIN; TUC 4 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BODY WEIGHT; BRAIN WEIGHT; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; DRUG EFFECT; FETUS; FETUS LUNG MATURATION; GRANULE CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MARMOSET; MITOSIS; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEWBORN; NONHUMAN; PREGNANCY; PRENATAL DRUG EXPOSURE; PROTEIN EXPRESSION; STEROID THERAPY;

ABNORMALITIES, DRUG-INDUCED; ANIMALS; ANIMALS, NEWBORN; ANTI-INFLAMMATORY AGENTS; BIOLOGICAL MARKERS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CALLITHRIX; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; DENTATE GYRUS; DEXAMETHASONE; DISEASE MODELS, ANIMAL; FEMALE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KI-67 ANTIGEN; MALE; MICROTUBULE-ASSOCIATED PROTEINS; NERVE TISSUE PROTEINS; NERVOUS SYSTEM MALFORMATIONS; NEUROPEPTIDES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; TIME;

EID: 51249093013     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/j.1750-3639.2008.00149.x     Document Type: Article

References (48)

1. Antonow-Schlorke I, Schwab M, Li C, Nathanielsz PW (2003) Glucocorticoid exposure at the dose used clinically alters cytoskeletal proteins and presynaptic terminals in the fetal baboon brain. J Physiol 547 : 117 123.
2. Bick-Sander A, Steiner B, Wolf SA, Babu H, Kempermann G (2006) Running in pregnancy transiently increases postnatal hippocampal neurogenesis in the offspring. Proc Natl Acad Sci USA 103 : 3852 3857.
3. Brabham T, Phelka A, Zimmer C, Nash A, Lopez JF, Vazquez DM (2000) Effects of prenatal dexamethasone on spatial learning and response to stress is influenced by maternal factors. Am J Physiol Regul Integr Comp Physiol 279 : R1899 R1909.
4. Brandt MD, Jessberger S, Steiner B, Kronenberg G, Reuter K, Bick-Sander A et al (2003) Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci 24 : 603 613.
5. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467 : 1 10.
6. Coe CL, Kramer M, Czeh B, Gould E, Reeves AJ, Kirschbaum C, Fuchs E (2003) Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry 54 : 1025 1034.
7. Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N et al (2005) Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21 : 1 14.
8. Czeh B, Lucassen PJ (2007) What causes the hippocampal volume decrease in depression? Are neurogenesis, glial changes and apoptosis implicated? Eur Arch Psychiatry Clin Neurosci 257 : 250 260.
9. Czeh B, Michaelis T, Watanabe T, Frahm J, de Biurrun G, van Kampen M et al (2001) Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc Natl Acad Sci USA 98 : 12796 12801.
10. Czeh B, Welt T, Fischer AK, Erhardt A, Schmitt W, Muller MB et al (2002) Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol Psychiatry 52 : 1057 1065.
11. Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza PV, Abrous DN (2003) Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci USA 100 : 14385 14390.
12. Ferguson SA, Paule MG, Holson RR (2001) Neonatal dexamethasone on day 7 in rats causes behavioral alterations reflective of hippocampal, but not cerebellar, deficits. Neurotoxicol Teratol 23 : 57 69.
13. Flagel SB, Vazquez DM, Watson SJ Jr., Neal, CR Jr. (2002) Effects of tapering neonatal dexamethasone on rat growth, neurodevelopment, and stress response. Am J Physiol Regul Integr Comp Physiol 282 : R55 R63.
14. Gaetano C, Matsuo T, Thiele CJ (1997) Identification and characterization of a retinoic acid-regulated human homologue of the unc-33-like phosphoprotein gene (hUlip) from neuroblastoma cells. J Biol Chem 272 : 12195 12201.
15. Gerber J, Raivich G, Wellmer A, Noeske C, Kunst T, Werner A et al (2001) A mouse model of Streptococcus pneumoniae meningitis mimicking several features of human disease. Acta Neuropathol (Berl) 101 : 499 508.
16. Gerdes J (1990) Ki-67 and other proliferation markers useful for immunohistological diagnostic and prognostic evaluations in human malignancies. Semin Cancer Biol 1 : 199 206.
17. Gold R, Schmied M, Giegerich G, Breitschopf H, Hartung HP, Toyka KV, Lassmann H (1994) Differentiation between cellular apoptosis and necrosis by the combined use of in situ tailing and nick translation techniques. Lab Invest 71 : 219 225.
18. Hassan AH, von Rosenstiel P, Patchev VK, Holsboer F, Almeida OF (1996) Exacerbation of apoptosis in the dentate gyrus of the aged rat by dexamethasone and the protective role of corticosterone. Exp Neurol 140 : 43 52.
19. Haynes LE, Griffiths MR, Hyde RE, Barber DJ, Mitchell IJ (2001) Dexamethasone induces limited apoptosis and extensive sublethal damage to specific subregions of the striatum and hippocampus: implications for mood disorders. Neuroscience 104 : 57 69.
20. Heine VM, Maslam S, Zareno J, Joels M, Lucassen PJ (2004) Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur J Neurosci 19 : 131 144.
21. Joelving FC, Billeskov R, Christensen JR, West M, Pakkenberg B (2006) Hippocampal neuron and glial cell numbers in Parkinson's disease - a stereological study. Hippocampus 16 : 826 833.
22. Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386 : 493 495.
23. Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27 : 447 452.
24. Kronenberg G, Bick-Sander A, Bunk E, Wolf C, Ehninger D, Kempermann G (2006) Physical exercise prevents age-related decline in precursor cell activity in the mouse dentate gyrus. Neurobiol Aging 27 : 1505 1513.
25. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16 : 2027 2033.
26. Lagace DC, Fischer SJ, Eisch AJ (2007) Gender and endogenous levels of estradiol do not influence adult hippocampal neurogenesis in mice. Hippocampus 17 : 175 180.
27. Leuner B, Mirescu C, Noiman L, Gould E (2007) Maternal experience inhibits the production of immature neurons in the hippocampus during the postpartum period through elevations in adrenal steroids. Hippocampus 17 : 434 442.
28. Magarinos AM, McEwen BS, Flugge G, Fuchs E (1996) Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci 16 : 3534 3540.
29. Malberg JE, Duman RS (2003) Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 28 : 1562 1571.
30. Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20 : 9104 9110.
31. Meaney MJ, Diorio J, Francis D, Widdowson J, LaPlante P, Caldji C et al (1996) Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev Neurosci 18 : 49 72.
32. Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28 : 223 250.
33. Minturn JE, Geschwind DH, Fryer HJ, Hockfield S (1995) Early postmitotic neurons transiently express toad-64, a neural specific protein. J Comp Neurol 355 : 369 379.
34. Morimoto M, Morita N, Ozawa H, Yokoyama K, Kawata M (1996) Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study. Neurosci Res 26 : 235 269.
35. Muneoka K, Mikuni M, Ogawa T, Kitera K, Kamei K, Takigawa M, Takahashi K (1997) Prenatal dexamethasone exposure alters brain monoamine metabolism and adrenocortical response in rat offspring. Am J Physiol 273 : R1669 R1675.
36. Naylor AS, Persson AI, Eriksson PS, Jonsdottir IH, Thorlin T (2005) Extended voluntary running inhibits exercise-induced adult hippocampal progenitor proliferation in the spontaneously hypertensive rat. J Neurophysiol 93 : 2406 2414.
37. Pryce CR, Feldon J, Fuchs E, Knuesel I, Oertle T, Sengstag C, Spengler M, Weber E, Weston A, Jongen-Relo A (2005) Postnatal ontogeny of hippocampal expression of the mineralocorticoid and glucocorticoid receptors in the common marmoset monkey. Eur J Neurosci 21 : 1521 1535.
38. Quinn CC, Gray GE, Hockfield S (1999) A family of proteins implicated in axon guidance and outgrowth. J Neurobiol 41 : 158 164.
39. Seckl JR, Dickson KL, Yates C, Fink G (1991) Distribution of glucocorticoid and mineralocorticoid receptor messenger RNA expression in human postmortem hippocampus. Brain Res 561 : 332 337.
40. Slotkin TA, Zhang J, McCook EC, Seidler FJ (1998) Glucocorticoid administration alters nuclear transcription factors in fetal rat brain: implications for the use of antenatal steroids. Brain Res Dev Brain Res 111 : 11 24.
41. Speirs HJ, Seckl JR, Brown RW (2004) Ontogeny of glucocorticoid receptor and 11beta-hydroxysteroid dehydrogenase type-1 gene expression identifies potential critical periods of glucocorticoid susceptibility during development. J Endocrinol 181 : 105 116.
42. Starkman MN, Giordani B, Gebarski SS, Berent S, Schork MA, Schteingart DE (1999) Decrease in cortisol reverses human hippocampal atrophy following treatment of Cushing's disease. Biol Psychiatry 46 : 1595 1602.
43. Tanapat P, Hastings NB, Reeves AJ, Gould E (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19 : 5792 5801.
44. Tauber SC, Schlumbohm C, Schilg L, Fuchs E, Nau R, Gerber J (2006) Intrauterine exposure to dexamethasone impairs proliferation but not neuronal differentiation in the dentate gyrus of newborn common marmoset monkeys. Brain Pathol 16 : 209 217.
45. Uno H, Eisele S, Sakai A, Shelton S, Baker E, DeJesus O, Holden J (1994) Neurotoxicity of glucocorticoids in the primate brain. Horm Behav 28 : 336 348.
46. van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96 : 13427 13431.
47. van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2 : 266 270.
48. Yu IT, Lee SH, Lee YS, Son H (2004) Differential effects of corticosterone and dexamethasone on hippocampal neurogenesis in vitro. Biochem Biophys Res Commun 317 : 484 490.