Stress experienced in utero reduces sexual dichotomies in neurogenesis, microenvironment, and cell death in the adult rat hippocampus

Developmental Neurobiology

Volumn 68, Issue 5, 2008, Pages 575-589

  Mandyam, Chitra D ^a   Crawford, Elena F ^a   Eisen, Amelia J ^c   Rivier, Catherine L ^b   Richardson, Heather N ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Doublecortin; Interleukin 1 beta; Ki 67; Restraint and random stress; Sex differences; Subgranular zone

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL PROLIFERATION; CHEMICAL STRESS; CONTROLLED STUDY; DIESTRUS; FEMALE; FOOTSHOCK; HIPPOCAMPUS; IMMOBILIZATION STRESS; MALE; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRENATAL STRESS; PRIORITY JOURNAL; RAT; RECEPTOR DENSITY; SEX DIFFERENCE;

ANIMALS; CELL COUNT; CELL DEATH; DATA INTERPRETATION, STATISTICAL; DENTATE GYRUS; ENVIRONMENT; FEMALE; FEMINIZATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-1BETA; MALE; NERVOUS SYSTEM; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL;

EID: 41549111127     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.20600     Document Type: Article

References (98)

1. Almeida OF, Conde GL, Crochemore C, Demeneix BA, Fischer D, Hassan AH, Meyer M, Holsboer F, Michaelidis TM. 2000. Subtle shifts in the ratio between pro- and antiapoptotic molecules after activation of corticosteroid receptors decide neuronal fate. FASEB J 14:779-790.
2. Altman D. 1991. Practical Statistics for Medical Research. London: Chapman and Hall.
3. Bacchi CE, Gown AM. 1993. Detection of cell proliferation in tissue sections. Braz J Med Biol Res 26:677-687.
4. Bethus I, Lemaire V, Lhomme M, Goodall G. 2005. Does prenatal stress affect latent inhibition? It depends on the gender. Behav Brain Res 158:331-338.
5. Bowman RE, MacLusky NJ, Sarmiento Y, Frankfurt M, Gordon M, Luine VN. 2004. Sexually dimorphic effects of prenatal stress on cognition, hormonal responses, and central neurotransmitters. Endocrinology 145:3778-3787.
6. 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.
7. 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.
8. Cooper-Kuhn CM, Kuhn HG. 2002. Is it all DNA repair? Methodological considerations for detecting neurogenesis in the adult brain. Brain Res Dev Brain Res 134(1-2):13-21.
9. Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, Bogdahn U, et al. 2005. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21:1-14.
10. Crochemore C, Michaelidis TM, Fischer D, Loeffler JP, Almeida OF. 2002. Enhancement of p53 activity and inhibition of neural cell proliferation by glucocorticoid receptor activation. FASEB J 16:761-770.
11. Cunningham C, Wilcockson DC, Campion S, Lunnon K, Perry VH. 2005. Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J Neurosci 25:9275-9284.
12. Donovan MH, Yazdani U, Norris RD, Games D, German DC, Eisch AJ. 2006. Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease. J Comp Neurol 495:70-83.
13. Einon D. 1980. Spatial memory and response strategies in rats: Age, sex and rearing differences in performance. Q J Exp Psychol 32:473-489.
14. Eisch AJ, Barrot M, Schad CA, Self DW, Nestler EJ. 2000. Opiates inhibit neurogenesis in the adult rat hippocampus. Proc Natl Acad Sci USA 97:7579-7584.
15. Endl E, Kausch I, Baack M, Knippers R, Gerdes J, Scholzen T. 2001. The expression of Ki-67, MCM3, and p27 defines distinct subsets of proliferating, resting, and differentiated cells. J Pathol 195:457-462.
16. Faherty CJ, Xanthoudakis S, Smeyne RJ. 1999. Caspase-3-dependent neuronal death in the hippocampus following kainic acid treatment. Brain Res Mol Brain Res 70:159-163.
17. Falconer EM, Galea LA. 2003. Sex differences in cell proliferation, cell death and defensive behavior following acute predator odor stress in adult rats. Brain Res 975 (1-2):22-36.
18. Franklin TB, Perrot-Sinal TS. 2006. Sex and ovarian steroids modulate brain-derived neurotrophic factor (BDNF) protein levels in rat hippocampus under stressful and non-stressful conditions. Psychoneuroendocrinology 31:38-48.
19. Fujioka A, Fujioka T, Ishida Y, Maekawa T, Nakamura S. 2006. Differential effects of prenatal stress on the morphological maturation of hippocampal neurons. Neuroscience 141:907-915.
20. Galea LA. 2007. Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Res Rev. Epub ahead of print.
21. Galea LA, Kavaliers M, Ossenkopp KP. 1996. Sexually dimorphic spatial learning in meadow voles Microtus pennsylvanicus and deer mice Peromyscus maniculatus. J Exp Biol 199(Part 1):195-200.
22. Galea LA, McEwen BS. 1999. Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Neuroscience 89:955-964.
23. Galea LA, Spritzer MD, Barker JM, Pawluski JL. 2006. Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 16:225-232.
24. Garcia A, Steiner B, Kronenberg G, Bick-Sander A, Kempermann G. 2004. Age-dependent expression of glucocorticoid- and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus. Aging Cell 3:363-371.
25. Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, Stein H. 1984. Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol 133:1710-1715.
26. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. 1999. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265.
27. Gould E, Cameron HA, Daniels DC, Woolley CS, McEwen BS. 1992. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 12:3642-3650.
28. Hajszan T, Milner TA, Leranth C. 2007. Sex steroids and the dentate gyrus. Prog Brain Res 163:399-816.
29. Harburg GC, Hall FS, Harrist AV, Sora I, Uhl GR, Eisch AJ. 2007. Knockout of the mu opioid receptor enhances the survival of adult-generated hippocampal granule cell neurons. Neuroscience 144:77-87.
30. 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.
31. Hastings NB, Gould E. 2003. Neurons inhibit neurogenesis. Nat Med 9:264-266.
32. Heine VM, Maslam S, Joels M, Lucassen PJ. 2004. Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation. Neurobiol Aging 25:361-375.
33. Holmes MC, Abrahamsen CT, French KL, Paterson JM, Mullins JJ, Seckl JR. 2006. The mother or the fetus? 11beta-hydroxysteroid dehydrogenase type 2 null mice provide evidence for direct fetal programming of behavior by endogenous glucocorticoids. J Neurosci 26:3840-3844.
34. Jessberger S, Nakashima K, Clemenson GD Jr, Mejia E, Mathews E, Ure K, Ogawa S, et al. 2007. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci 27:5967-5975.
35. Jessberger S, Romer B, Babu H, Kempermann G. 2005. Seizures induce proliferation and dispersion of double-cortin-positive hippocampal progenitor cells. Exp Neurol 196:342-351.
36. Jortner BS. 2006. The return of the dark neuron. A histological artifact complicating contemporary neurotoxicologic evaluation. Neuro toxicology 27:628-634.
37. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM. 2002. The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115:97-105.
38. Kempermann G, Gage FH. 1999. Experience-dependent regulation of adult hippocampal neurogenesis: Effects of long-term stimulation and stimulus withdrawal. Hippocampus 9:321-332.
39. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH. 2003. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130:391-399.
40. Krasnoff A, Weston LM. 1976. Puberal status and sex differences: activity and maze behavior in rats. Dev Psychobiol 9:261-269.
41. Kuhn HG, Biebl M, Wilhelm D, Li M, Friedlander RM, Winkler J. 2005. Increased generation of granule cells in adult Bcl-2-overexpressing mice: A role for cell death during continued hippocampal neurogenesis. Eur J Neurosci 22:1907-1915.
42. Lee SJ, McEwen BS. 2001. Neurotrophic and neuroprotective actions of estrogens and their therapeutic implications. Annu Rev Pharmacol Toxicol 41:569-591.
43. Lemaire V, Koehl M, Le Moal M, Abrous DN. 2000. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 97:11032-11037.
44. Lemaire V, Lamarque S, Le Moal M, Piazza PV, Abrous DN. 2006. Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis. Biol Psychiatry 59:786-792.
45. Li H, Pin S, Zeng Z, Wang MM, Andreasson KA, McCullough LD. 2005. Sex differences in cell death. Ann Neurol 58:317-321.
46. Li H, Zhu ZL, Jia N, Bai ZL, Cai Q, Chen R, Song TB, et al. 2006. [Gender-dependent difference of NF-kappaB expression in the hippocampus of prenatally stressed offspring rats.]. Sheng Li Xue Bao 58:577-583.
47. Liu L, Li A, Matthews SG. 2001. Maternal glucocorticoid treatment programs HPA regulation in adult offspring: sex-specific effects. Am J Physiol Endocrinol Metab 280:E729-E739.
48. Lucassen PJ, Heine VM, Muller MB, van der Beek EM, Wiegant VM, De Kloet ER, et al. 2006. Stress, depression and hippocampal apoptosis. CNS Neurol Disord Drug Targets 5:531-546.
49. Maccari S, Piazza PV, Kabbaj M, Barbazanges A, Simon H, Le Moal M. 1995. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci 15(Part 1):110-116.
50. MacPherson A, Dinkel K, Sapolsky R. 2005. Glucocorticoids worsen excitotoxin-induced expression of pro-inflammatory cytokines in hippocampal cultures. Exp Neurol 194:376-383.
51. Mandyam CD, Harburg GC, Eisch AJ. 2007. Determination of key aspects of precursor cell proliferation, cell cycle length and kinetics in the adult mouse subgranular zone. Neuroscience 146:108-122.
52. Mandyam CD, Norris RD, Eisch AJ. 2004. Chronic morphine induces premature mitosis of proliferating cells in the adult mouse subgranular zone. J Neurosci Res 76:783-794.
53. Mandyam CD, Wee S, Eisch AJ, Richardson HN, Koob GF. 2007. Methamphetamine self-administration and voluntary exercise have opposing effects on medial prefrontal cortex gliogenesis. J Neurosci 27:11442-11450.
54. Markakis EA, Palmer TD, Randolph-Moore L, Rakic P, Gage FH. 2004. Novel neuronal phenotypes from neural progenitor cells. J Neurosci 24:2886-2897.
55. McCormick CM, Smythe JW, Sharma S, Meaney MJ. 1995. Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Brain Res Dev Brain Res 84:55-61.
56. McEwen BS. 2002. Sex, stress and the hippocampus: Allostasis, allostatic load and the aging process. Neurobiol Aging 23:921-939.
57. McEwen BS, Lieberburg I, Chaptal C, Krey LC. 1977. Aromatization: Important for sexual differentiation of the neonatal rat brain. Horm Behav 9:249-263.
58. Monje ML, Mizumatsu S, Fike JR, Palmer TD. 2002. Irradiation induces neural precursor-cell dysfunction. Nat Med 8:955-962.
59. Montano MM, Wang MH, Even MD, vom Saal FS. 1991. Serum corticosterone in fetal mice: Sex differences, circadian changes, and effect of maternal stress. Physiol Behav 50:323-329.
60. Montaron MF, Piazza PV, Aurousseau C, Urani A, Le Moal M, Abrous DN. 2003. Implication of corticosteroid receptors in the regulation of hippocampal structural plasticity. Eur J Neurosci 18:3105-3111.
61. Moore CL, Power KL. 1986. Prenatal stress affects mother-infant interaction in Norway rats. Dev Psychobiol 19:235-245.
62. Olney JW, Tenkova T, Dikranian K, Muglia LJ, Jermakowicz WJ, D'Sa C, Roth KA. 2002. Ethanol-induced caspase-3 activation in the in vivo developing mouse brain. Neurobiol Dis 9:205-219.
63. Palanza P. 2001. Animal models of anxiety and depression: How are females different? Neurosci Biobehav Rev 25:219-233.
64. Paxinos G, Watson C. 1997. The Rat Brain in Stereotaxic Coordinates. San Diego: Academic Press.
65. Peissner W, Kocher M, Treuer H, Gillardon F. 1999. Ionizing radiation-induced apoptosis of proliferating stem cells in the dentate gyrus of the adult rat hippocampus. Brain Res Mol Brain Res 71:61-68.
66. Perfilieva E, Risedal A, Nyberg J, Johansson BB, Eriksson PS. 2001. Gender and strain influence on neurogenesis in dentate gyrus of young rats. J Cereb Blood Flow Metab 21:211-217.
67. Rao MS, Shetty AK. 2004. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 19:234-246.
68. Richardson HN, Zorrilla EP, Mandyam CD, Rivier CL. 2006. Exposure to repetitive versus varied stress during prenatal development generates two distinct anxiogenic and neuroendocrine profiles in adulthood. Endocrinology 147:2506-2517.
69. Rivier C, Vale W. 1990. Cytokines act within the brain to inhibit luteinizing hormone secretion and ovulation in the rat. Endocrinology 127:849-856.
70. Rivier J, Amoss M, Rivier C, Vale W. 1974. Synthetic luteinizing hormone releasing factor. Short chain analogs. J Med Chem 17(2):230-233.
71. Rodriguez JJ, Montaron MF, Petry KG, Aurousseau C, Marinelli M, Premier S, Rougon G, et al. 1998. Complex regulation of the expression of the polysialylated form of the neuronal cell adhesion molecule by glucocorticoids in the rat hippocampus. Eur J Neurosci 10:2994-3006.
72. Roof RL, Stein DG. 1999. Gender differences in Morris water maze performance depend on task parameters. Physiol Behav 68(1-2):81-86.
73. Roussel S, Boissy A, Montigny D, Hemsworth PH, Duvaux-Ponter C. 2005. Gender-specific effects of prenatal stress on emotional reactivity and stress physiology of goat kids. Horm Behav 47:256-266.
74. Schmidt M, Pauels HG, Lugering N, Lugering A, Domschke W, Kucharzik T. 1999. Glucocorticoids induce apoptosis in human monocytes: Potential role of IL-1 beta. J Immunol 163:3484-3490.
75. Schmitz C, Rhodes ME, Bludau M, Kaplan S, Ong P, Ueffing I, Vehoff J, Korr H, Frye CA. 2002. Depression: Reduced number of granule cells in the hippocampus of female, but not male, rats due to prenatal restraint stress. Mol Psychiatry 7:810-813.
76. Seri B, Garcia-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A. 2004. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 478:359-378.
77. Sisk CL, Richardson HN, Chappell PE, Levine JE. 2001. In vivo gonadotropin-releasing hormone secretion in female rats during peripubertal development and on proestrus. Endocrinology 142:2929-2936.
78. Sutcliffe JS, Marshall KM, Neill JC. 2007. Influence of gender on working and spatial memory in the novel object recognition task in the rat. Behav Brain Res 177:117-125.
79. Szuran TF, Pliska V, Pokorny J, Welzl H. 2000. Prenatal stress in rats: Effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance. Physiol Behav 71(3-4):353-362.
80. Tanapat P, Galea LA, Gould E. 1998. Stress inhibits the proliferation of granule cell precursors in the developing dentate gyrus. Int J Dev Neurosci 16(3-4):235-239.
81. 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.
82. Van den Hove DL, Blanco CE, Aendekerk B, Desbonnet L, Bruschettini M, Steinbusch HP, Prickaerts J, et al. 2005. Prenatal restraint stress and long-term affective consequences. Dev Neurosci 27:313-320.
83. Van den Hove DL, Steinbusch HW, Scheepens A, Van de Berg WD, Kooiman LA, Boosten BJ, Prickaerts J, et al. 2006. Prenatal stress and neonatal rat brain development. Neuroscience 137:145-155.
84. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
85. Wang Z, Garabedian MJ. 2003. Modulation of glucocorticoid receptor transcriptional activation, phosphorylation, and growth inhibition by p27Kip1. J Biol Chem 278:50897-50901.
86. Ward IL, Weisz J. 1980. Maternal stress alters plasma testosterone in fetal males. Science 207:328-329.
87. Ward IL, Weisz J. 1984. Differential effects of maternal stress on circulating levels of corticosterone, progesterone, and testosterone in male and female rat fetuses and their mothers. Endocrinology 114:1635-1644.
88. Weinstock M. 2007. Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 32:1730-1740.
89. Weinstock M, Matlina E, Maor GI, Rosen H, McEwen BS. 1992. Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary adrenal system in the female rat. Brain Res 595:195-200.
90. Welberg LA, Seckl JR, Holmes MC. 2000. Inhibition of 11beta- hydroxysteroid dehydrogenase, the foeto-placental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxiety-like behaviour in the offspring. Eur J Neurosci 12:1047-1054.
91. West MJ, Andersen AH. 1980. An allometric study of the area dentata in the rat and mouse. Brain Res 2:317-348.
92. West MJ, Gundersen HJ. 1990. Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 296:1-22.
93. West MJ, Slomianka L, Gundersen HJ. 1991. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
94. Westenbroek C, Den Boer JA, Veenhuis M, Ter Horst GJ. 2004. Chronic stress and social housing differentially affect neurogenesis in male and female rats. Brain Res Bull 64:303-308.
95. Williams CL, Barnett AM, Meek WH. 1990. Organizational effects of early gonadal secretions on sexual differentiation in spatial memory. Behav Neurosci 104:84-97.
96. 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.
97. Zhu Z, Li X, Chen W, Zhao Y, Li H, Qing C, Jia N, et al. 2004. Prenatal stress causes gender-dependent neuronal loss and oxidative stress in rat hippocampus. J Neurosci Res 78:837-844.
98. Zorrilla EP. 1997. Multiparous species present problems (and possibilities) to developmentalists. Dev Psychobiol 30:141-150.