Age-dependent effect of prenatal stress on hippocampal cell proliferation in female rats

European Journal of Neuroscience

Volumn 29, Issue 3, 2009, Pages 635-640

  Koehl, Muriel ^a,b   Lemaire, Valerie ^a,b   Le Moal, Michel ^a,b   Abrous, Djoher N ^a,b  

^a INSTITUT FRANÇOIS MAGENDIE   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Aging; Hippocampus; Neurogenesis; Plasticity; Prenatal stress

Indexed keywords

ADRENAL GLAND; ADULTHOOD; AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; JUVENILE; MALE; NONHUMAN; ORGAN WEIGHT; PRENATAL STRESS; PRIORITY JOURNAL; RAT; SENESCENCE;

ADRENAL CORTEX HORMONES; ADRENAL GLANDS; AGE FACTORS; AGING; ANIMALS; CELL COUNT; CELL PROLIFERATION; CYTOPROTECTION; FEMALE; HIPPOCAMPUS; NEUROGENESIS; ORGAN SIZE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; STRESS, PHYSIOLOGICAL;

EID: 59149091914     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2009.06608.x     Document Type: Article

References (63)

1. Abrous, D.N., Adriani, W., Montaron, M.F., Aurousseau, C., Rougon, G., Le Moal, M. Piazza, P.V. (2002) Nicotine self-administration impairs hippocampal plasticity. J. Neurosci., 22, 3656 3662.
2. Abrous, D.N., Koehl, M. Le Moal, M. (2005) Adult neurogenesis: from precursors to network and physiology. Physiol. Rev., 85, 523 569.
3. Bergman, K., Sarkar, P., O'Connor, T.G., Modi, N. Glover, V. (2007) Maternal stress during pregnancy predicts cognitive ability and fearfulness in infancy. J. Am. Acad. Child Adolesc. Psychiatry, 46, 1454 1463.
4. Bland, S.T., Schmid, M.J., Greenwood, B.N., Watkins, L.R. Maier, S.F. (2006) Behavioral control of the stressor modulates stress-induced changes in neurogenesis and fibroblast growth factor-2. Neuroreport, 17, 593 597.
5. van der Borght, K. Brundin, P. (2007) Reduced expression of PSA-NCAM in the hippocampus and piriform cortex of the R6/1 and R6/2 mouse models of Huntington's disease. Exp. Neurol., 204, 473 478.
6. Bowman, R.E. (2005) Stress-induced changes in spatial memory are sexually differentiated and vary across the lifespan. J. Neuroendocrinol., 17, 526 535.
7. Brezun, J.M. Daszuta, A. (2000) Serotonin may stimulate granule cell proliferation in the adult hippocampus, as observed in rats grafted with foetal raphe neurons. Eur. J. Neurosci., 12, 391 396.
8. Brummelte, S., Pawluski, J.L. Galea, L.A. (2006) High post-partum levels of corticosterone given to dams influence postnatal hippocampal cell proliferation and behavior of offspring: A model of post-partum stress and possible depression. Horm. Behav., 50, 370 382.
9. Buitelaar, J.K., Huizink, A.C., Mulder, E.J., de Medina, P.G. Visser, G.H. (2003) Prenatal stress and cognitive development and temperament in infants. Neurobiol. Aging, 24 (Suppl 1 S53 S60. discussion S67-58.
10. Cabib, S., Orsini, C., Le Moal, M. Piazza, P.V. (2000) Abolition and reversal of strain differences in behavioral responses to drugs of abuse after a brief experience. Science, 289, 463 465.
11. Cameron, H.A. Gould, E. (1994) Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience, 61, 203 209.
12. Crabbe, J.C., Wahlsten, D. Dudek, B.C. (1999) Genetics of mouse behavior: interactions with laboratory environment. Science, 284, 1670 1672.
13. Drapeau, E. Abrous, D.N. (2008) Role of Neurogenesis in Age-Related Memory Disorders. Aging Cell, 7, 569 586.
14. Dupret, D., Revest, J.M., Koehl, M., Ichas, F., De Giorgi, F., Costet, P., Abrous, D.N. Piazza, P.V. (2008) Spatial relational memory requires hippocampal adult neurogenesis. PLoS ONE, 3, e1959.
15. Falconer, E.M. Galea, L.A. (2003) Sex differences in cell proliferation, cell death and defensive behavior following acute predator odor stress in adult rats. Brain Res., 975, 22 36.
16. Ferrini, M., Piroli, G., Frontera, M., Falbo, A., Lima, A. De Nicola, A.F. (1999) Estrogens normalize the hypothalamic-pituitary-adrenal axis response to stress and increase glucocorticoid receptor immuno-reactivity in hippocampus of aging male rats. Neuroendocrinology, 69, 129 137.
17. Galea, L.A.M. (2008) Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Res. Rev., 57, 332 341.
18. Galea, L.A., McEwen, B.S., Tanapat, P., Deak, T., Spencer, R.L. Dhabhar, F.S. (1997) Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience, 81, 689 697.
19. Garcia-Segura, L.M., Azcoitia, I. DonCarlos, L.L. (2001) Neuroprotection by estradiol. Prog. Neurobiol., 63, 29 60.
20. Gluckman, P.D., Hanson, M.A., Cooper, C. Thornburg, K.L. (2008) Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med., 359, 61 73.
21. Gomez, F., Lahmame, A., de Kloet, E.R. Armario, A. (1996) Hypothalamic-pituitary-adrenal response to chronic stress in five inbred rat strains: differential responses are mainly located at the adrenocortical level. Neuroendocrinology, 63, 327 337.
22. Gould, E., Cameron, H.A., Daniels, D.C., Woolley, C.S. McEwen, B.S. (1992) Adrenal hormones suppress cell division in the adult rat dentate gyrus. J. Neurosci., 12, 3642 3650.
23. Heine, V.M., Maslam, S., Zareno, J., Joels, M. Lucassen, P.J. (2004) Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur.J Neurosci., 19, 131 144.
24. Kempermann, G., Jessberger, S., Steiner, B. Kronenberg, G. (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci., 27, 447 452.
25. Kesner, R.P. Helen, E.S. (2007) A behavioral analysis of dentate gyrus function Progress in Brain Research. Elsevier, Amsterdam, The Netherlands, pp. 567 576.
26. Koehl, M., Lemaire, V., Vallee, M., Abrous, N., Piazza, P.V., Mayo, W., Maccari, S. Le Moal, M. (2001) Long term neurodevelopmental and behavioral effects of perinatal life events in rats. Neurotox. Res., 3, 65 83.
27. Koehl, M., Lemaire, V., Mayo, W., Abrous, D.N., Maccari, S., Piazza, P.V., Le Moal, M. Vallee, M. (2002) Individual vulnerability to substance abuse and affective disorders: role of early environmental influences. Neurotox. Res., 4, 281 296.
28. Lemaire, V., Aurousseau, C., Le Moal, M. Abrous, D.N. (1999) Behavioural trait of reactivity to novelty is related to hippocampal neurogenesis. Eur. J. Neurosci., 11, 4006 4014.
29. Lemaire, V., Koehl, M., Le Moal, M. Abrous, D.N. (2000) Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc. Natl Acad. Sci. USA, 97, 11032 11037.
30. Lemaire, V., Lamarque, S., Moal, M.L., Piazza, P.V. Abrous, D.N. (2006) Postnatal Stimulation of the Pups Counteracts Prenatal Stress-Induced Deficits in Hippocampal Neurogenesis. Biol. Psychiatry, 59, 786 792.
31. Maccari, S. Morley-Fletcher, S. (2007) Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology, 32 (Suppl 1 S10 S15.
32. Malberg, J.E. Duman, R.S. (2003) Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology, 28, 1562 1571.
33. Mandyam, C.D., Crawford, E.F., Eisch, A.J., Rivier, C.L. Richardson, H.N. (2008) Stress experienced in utero reduces sexual dichotomies in neurogenesis, microenvironment, and cell death in the adult rat hippocampus. Dev. Neurobiol., 68, 575 589.
34. Mayer, J.L., Klumpers, L., Maslam, S., de Kloet, E.R., Joels, M. Lucassen, P.J. (2006) Brief treatment with the glucocorticoid receptor antagonist mifepristone normalises the corticosterone-induced reduction of adult hippocampal neurogenesis. J. Neuroendocrinol., 18, 629 631.
35. Montaron, M.F., Petry, K.G., Rodriguez, J.J., Marinelli, M., Aurousseau, C., Rougon, G., Le Moal, M. Abrous, D.N. (1999) Adrenalectomy increases neurogenesis but not PSA-NCAM expression in aged dentate gyrus. Eur. J. Neurosci., 11, 1479 1485.
36. Montaron, M.F., Drapeau, E., Dupret, D., Kitchener, P., Aurousseau, C., Le Moal, M., Piazza, P.V. Abrous, D.N. (2006) Lifelong corticosterone level determines age-related decline in neurogenesis and memory. Neurobiol. Aging, 27, 645 654.
37. Nacher, J., Rosell, D.R., Alonso-Llosa, G. McEwen, B.S. (2001) NMDA receptor antagonist treatment induces a long-lasting increase in the number of proliferating cells, PSA-NCAM-immunoreactive granule neurons and radial glia in the adult rat dentate gyrus. Eur. J. Neurosci., 13, 512 520.
38. Oomen, C.A., Mayer, J.L., de Kloet, E.R., Joels, M. Lucassen, P.J. (2007) Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur. J. Neurosci., 26, 3395 3401.
39. van Os, J. Selten, J.P. (1998) Prenatal exposure to maternal stress and subsequent schizophrenia. The May 1940 invasion of The Netherlands. Br. J. Psychiatry, 172, 324 326.
40. Pham, K., Nacher, J., Hof, P.R. McEwen, B.S. (2003) Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur. J. Neurosci., 17, 879 886.
41. Rice, F., Jones, I. Thapar, A. (2007) The impact of gestational stress and prenatal growth on emotional problems in offspring: a review. Acta Psychiatr. Scand., 115, 171 183.
42. Rougon, G., Dubois, C., Buckley, N., Magnani, J.L. Zollinger, W. (1986) A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM. J. Cell Biol., 103, 2429 2437.
43. Seki, T. (2002a) Expression patterns of immature neuronal markers PSA-NCAM, CRMP-4 and NeuroD in the hippocampus of young adult and aged rodents. J Neurosci.Res., 70, 327 334.
44. Seki, T. (2002b) Hippocampal adult neurogenesis occurs in a microenvironment provided by PSA-NCAM-expressing immature neurons. J. Neurosci. Res., 69, 772 783.
45. Seki, T. Arai, Y. (1993) Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J. Neurosci., 13, 2351 2358.
46. Seri, B., Garcia-Verdugo, J.M., Collado-Morente, L., McEwen, B.S. Alvarez-Buylla, A. (2004) Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J. Comp. Neurol., 478, 359 378.
47. Shors, T.J., Mathew, J., Sisti, H.M., Edgecomb, C., Beckoff, S. Dalla, C. (2007) Neurogenesis and helplessness are mediated by controllability in males but not in females. Biol. Psychiatry, 62, 487 495.
48. Stranahan, A.M., Khalil, D. Gould, E. (2006) Social isolation delays the positive effects of running on adult neurogenesis. Nat. Neurosci., 9, 526 533.
49. Szuran, T.F., Pliska, V., Pokorny, J. Welzl, H. (2000) Prenatal stress in rats: effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance. Physiol. Behav., 71, 353 362.
50. Tanapat, P., Galea, L.A. Gould, E. (1998) Stress inhibits the proliferation of granule cell precursors in the developing dentate gyrus. Int. J. Dev. Neurosci., 16, 235 239.
51. Tanapat, P., Hastings, N.B., Rydel, T.A., Galea, L.A. Gould, E. (2001) Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J. Comp. Neurol., 437, 496 504.
52. Thomas, R.M., Urban, J.H. Peterson, D.A. (2006) Acute exposure to predator odor elicits a robust increase in corticosterone and a decrease in activity without altering proliferation in the adult rat hippocampus. Exp. Neurol., 201, 308 315.
53. Thomas, R.M., Hotsenpiller, G. Peterson, D.A. (2007) Acute psychosocial stress reduces cell survival in adult hippocampal neurogenesis without altering proliferation. J. Neurosci., 27, 2734 2743.
54. Toran-Allerand, C.D., Singh, M. Setalo, G. Jr. (1999) Novel mechanisms of estrogen action in the brain: new players in an old story. Front. Neuroendocrinol., 20, 97 121.
55. Vallee, M., MacCari, S., Dellu, F., Simon, H., Le Moal, M. Mayo, W. (1999) Long-term effects of prenatal stress and postnatal handling on age- related glucocorticoid secretion and cognitive performance: a longitudinal study in the rat. Eur. J. Neurosci., 11, 2906 2916.
56. Weinstock, M. (2007) Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem. Res., 32, 1730 1740.
57. Weinstock, M. (2008) The long-term behavioural consequences of prenatal stress. Neurosci. Biobehav. Rev., 32, 1073 1086.
58. Westenbroek, C., Den Boer, J.A., Veenhuis, M. Ter Horst, G.J. (2004) Chronic stress and social housing differentially affect neurogenesis in male and female rats. Brain Res. Bull., 64, 303 308.
59. Wise, P.M., Dubal, D.B., Wilson, M.E., Rau, S.W. Bottner, M. (2001) Minireview: neuroprotective effects of estrogen-new insights into mechanisms of action. Endocrinology, 142, 969 973.
60. Wong, E.Y. Herbert, J. (2004) The corticoid environment: a determining factor for neural progenitors' survival in the adult hippocampus. Eur. J. Neurosci., 20, 2491 2498.
61. Zagron, G. Weinstock, M. (2006) Maternal adrenal hormone secretion mediates behavioural alterations induced by prenatal stress in male and female rats. Behav. Brain Res., 175, 323 328.
62. Zhang, C.L., Zou, Y., He, W., Gage, F.H. Evans, R.M. (2008) A role for adult TLX-positive neural stem cells in learning and behaviour. Nature, 451, 1004 1007.
63. Zuena, A.R., Mairesse, J., Casolini, P., Cinque, C., Alema, G.S., Morley-Fletcher, S., Chiodi, V., Spagnoli, L.G., Gradini, R., Catalani, A., Nicoletti, F. Maccari, S. (2008) Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLoS ONE, 3, e2170.