Age- and sex-dependent effects of early life stress on hippocampal neurogenesis

Frontiers in Endocrinology

Volumn 5, Issue FEB, 2014, Pages

  Loi, Manila ^a   Koricka, Sylwia ^a   Lucassen, Paul J ^b   Joëls, Marian ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Adult neurogenesis; Dentate gyrus; Hippocampus; Maternal deprivation; Maternal separation; Proliferation; Rat; Stress

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLUCOCORTICOID RECEPTOR ANTAGONIST; HISTONE DEACETYLASE INHIBITOR; MIFEPRISTONE;

AGE; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; EARLY LIFE STRESS; EPIGENETICS; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INFANT DISEASE; META ANALYSIS (TOPIC); NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PERINATAL STRESS; POSTNATAL STRESS; PUBERTY; SEX; SPATIAL LEARNING;

EID: 84901005320     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2014.00013     Document Type: Article

References (87)

1. Kohman RA, Rhodes JS. Neurogenesis, inflammation and behavior. Brain Behav Immun (2013) 27:22-32. doi: 10.1016/j.bbi.2012.09.003.
2. Kempermann G. New neurons for 'survival of the fittest'. Nat Rev Neurosci (2012) 13:727-36. doi:10.1038/nrn3319.
3. Kolb B, Mychasiuk R, Muhammad A, Li Y, Frost DO, Gibb R. Experience and the developing prefrontal cortex. Proc Natl Acad Sci U S A (2012) 109(Suppl 2):17186-93. doi:10.1073/pnas.1121251109.
4. Brans RG, Kahn RS, Schnack HG, van Baal GC, Posthuma D, van Haren NE, et al. Brain plasticity and intellectual ability are influenced by shared genes. J Neurosci (2010) 30:5519-24. doi:10.1523/JNEUROSCI.5841-09.2010.
5. Sporns O. The human connectome: a complex network. Ann N Y Acad Sci (2011) 1224:109-25. doi:10.1111/j.1749-6632.2010.05888.x.
6. Raabe FJ, Spengler D. Epigenetic risk factors in PTSD and depression. Front Psychiatry (2013) 4:80. doi:10.3389/fpsyt.2013.00080.
7. Korosi A, Naninck EF, Oomen CA, Schouten M, Krugers H, Fitzsimons C, et al. Early-life stress mediated modulation of adult neurogenesis and behavior. Behav Brain Res (2012) 227:400-9. doi:10.1016/j.bbr.2011.07.037.
8. Jiang Z, Cowell RM, Nakazawa K. Convergence of genetic and environmental factors on parvalbumin-positive interneurons in schizophrenia. Front Behav Neurosci (2013) 7:116. doi:10.3389/fnbeh.2013.00116.
9. Schmahl CG, Vermetten E, Elzinga BM, Douglas BJ. Magnetic resonance imaging of hippocampal and amygdala volume in women with childhood abuse and borderline personality disorder. Psychiatry Res (2003) 122:193-8. doi:10.1016/S0925-4927(03)00023-4.
10. Heim C, NemeroffCB. The impact of early adverse experiences on brain systems involved in the pathophysiology of anxiety and affective disorders. Biol Psychiatry (1999) 46:1509-22. doi:10.1016/S0006-3223(99)00224-3.
11. Zimmermann P, Brückl T, Nocon A, Pfister H, Binder EB, Uhr M, et al. Interaction of FKBP5 gene variants and adverse life events in predicting depression onset: results from a 10-year prospective community study. Am J Psychiatry (2011) 168:1107-16. doi:10.1176/appi.ajp.2011.10111577.
12. Belsky DW, Caspi A, Arseneault L, Bleidorn W, Fonagy P, Goodman M, et al. Etiological features of borderline personality related characteristics in a birth cohort of 12-year-old children. Dev Psychopathol (2012) 24:251-65. doi:10.1017/S0954579411000812.
13. Breslau N, Koenen KC, Luo Z, Agnew-Blais J, Swanson S, Houts RM, et al. Childhood maltreatment, juvenile disorders and adult post-traumatic stress disorder: a prospective investigation. Psychol Med (2013) 29:1-9. doi:10.1017/S0033291713002651.
14. Pryce CR, Ruedi-Bettschen D, Dettling AC, Weston A, Russig H, Ferger B, et al. Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research. Neurosci Biobehav Rev (2005) 29:649-74. doi:10.1016/j.neubiorev.2005.03.011.
15. Schmidt MV, Wang XD, Meijer OC. Early life stress paradigms in rodents: potential animal models of depression? Psychopharmacology (Berl) (2011) 214:131-40. doi:10.1007/s00213-010-2096-0.
16. Koenig JI, Walker CD, Romeo RD, Lupien SJ. Effects of stress across the lifespan. Stress (2011) 14:475-80. doi:10.3109/10253890.2011.604879.
17. Lemaire V, Koehl M, Le MM, Abrous DN. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci U S A (2000) 97:11032-7. doi:10.1073/pnas.97.20.11032.
18. Lemaire V, Lamarque S, Le MM, Piazza PV, Abrous DN. Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis. Biol Psychiatry (2006) 59:786-92. doi:10.1016/j.biopsych.2005.11.009.
19. van den Hove DL, Leibold NK, Strackx E, Martinez-Claros M, Lesch KP, Steinbusch HW, et al. Prenatal stress and subsequent exposure to chronic mild stress in rats; interdependent effects on emotional behavior and the serotonergic system. Eur Neuropsychopharmacol (2013) (in press). doi:10.1016/j.euroneuro.2013.09.006.
20. Welberg LA, Seckl JR. Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol (2001) 13:113-28. doi:10.1111/j.1365-2826.2001.00601.x.
21. Zhang TY, Labonte B, Wen XL, Turecki G, Meaney MJ. Epigenetic mechanisms for the early environmental regulation of hippocampal glucocorticoid receptor gene expression in rodents and humans. Neuropsychopharmacology (2013) 38:111-23. doi:10.1038/npp.2012.149.
22. Champagne FA. Maternal imprints and the origins of variation. Horm Behav (2011) 60:4-11. doi:10.1016/j.yhbeh.2011.02.016.
23. Holmes A, Le Guisquet AM, Vogel E, Millstein RA, Leman S, Belzung C. Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neurosci Biobehav Rev (2005) 29:1335-46. doi:10.1016/j.neubiorev.2005.04.012.
24. Baram TZ, Davis EP, Obenaus A, Sandman CA, Small SL, Solodkin A, et al. Fragmentation and unpredictability of early-life experience in mental disorders. Am J Psychiatry (2012) 169:907-15. doi:10.1176/appi.ajp.2012.11091347.
25. Francis DD, Diorio J, Plotsky PM, Meaney MJ. Environmental enrichment reverses the effects of maternal separation on stress reactivity. J Neurosci (2002) 22:7840-3.
26. de Kloet ER, Sibug RM, Helmerhorst FM, Schmidt MV. Stress, genes and the mechanism of programming the brain for later life. Neurosci Biobehav Rev (2005) 29:271-81. doi:10.1016/j.neubiorev.2004.10.008.
27. Bredy TW, Grant RJ, Champagne DL, Meaney MJ. Maternal care influences neuronal survival in the hippocampus of the rat. Eur J Neurosci (2003) 18:2903-9. doi:10.1111/j.1460-9568.2003.02965.x.
28. Cirulli F, Berry A, Bonsignore LT, Capone F, D'Andrea I, Aloe L, et al. Early life influences on emotional reactivity: evidence that social enrichment has greater effects than handling on anxiety-like behaviors, neuroendocrine responses to stress and central BDNF levels. Neurosci Biobehav Rev (2010) 34:808-20. doi:10.1016/j.neubiorev.2010.02.008.
29. de Kloet ER, Joëls M, Holsboer F. Stress and the brain: from adaptation to disease. Nat Rev Neurosci (2005) 6:463-75. doi:10.1038/nrn1683.
30. Handa RJ, Weiser MJ. Gonadal steroid hormones and the hypothalamo-pituitary-adrenal axis. Front Neuroendocrinol (2013) (in press). doi:10.1016/j.yfrne.2013.11.001.
31. Joels M, Sarabdjitsingh RA, Karst H. Unraveling the time domains of corticosteroid hormone influences on brain activity: rapid, slow, and chronic modes. Pharmacol Rev (2012) 64:901-38. doi:10.1124/pr.112.005892.
32. Oitzl MS, Champagne DL, van der Veen R, de Kloet ER. Brain development under stress: hypotheses of glucocorticoid actions revisited. Neurosci Biobehav Rev (2010) 34:853-66. doi:10.1016/j.neubiorev.2009.07.006.
33. Champagne FA. Early environments, glucocorticoid receptors, and behavioral epigenetics. Behav Neurosci (2013) 127:628-36. doi:10.1037/a0034186.
34. Lupien SJ, McEwen BS, Gunnar MR, Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci (2009) 10:434-45. doi:10.1038/nrn2639.
35. Kim JJ, Song EY, Kosten TA. Stress effects in the hippocampus: synaptic plasticity and memory. Stress (2006) 9:1-11. doi:10.1080/10253890600678004.
36. Fenoglio KA, Brunson KL, Baram TZ. Hippocampal neuroplasticity induced by early-life stress: functional and molecular aspects. Front Neuroendocrinol (2006) 27:180-92. doi:10.1016/j.yfrne.2006.02.001.
37. Champagne DL, Bagot RC, van Hasselt F, Ramakers G, Meaney MJ, de Kloet ER, et al. Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J Neurosci (2008) 28:6037-45. doi:10.1523/JNEUROSCI.0526-08.2008.
38. Bagot RC, van Hasselt FN, Champagne DL, Meaney MJ, Krugers HJ, Joels M. Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus. Neurobiol Learn Mem (2009) 92:292-300. doi:10.1016/j.nlm.2009.03.004.
39. Barha CK, Pawluski JL, Galea LA. Maternal care affects male and female offspring working memory and stress reactivity. Physiol Behav (2007) 92:939-50. doi:10.1016/j.physbeh.2007.06.022.
40. Oomen CA, Soeters H, Audureau N, Vermunt L, van Hasselt FN, Manders EM, et al. Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood. J Neurosci (2010) 30:6635-45. doi:10.1523/JNEUROSCI.0247-10.2010.
41. Baudin A, Blot K, Verney C, Estevez L, Santamaria J, Gressens P, et al. Maternal deprivation induces deficits in temporal memory and cognitive flexibility and exaggerates synaptic plasticity in the rat medial prefrontal cortex. Neurobiol Learn Mem (2012) 98:207-14. doi:10.1016/j.nlm.2012.08.004.
42. van Hasselt FN, de Visser L, Tieskens JM, Cornelisse S, Baars AM, Lavrijsen M, et al. Individual variations in maternal care early in life correlate with later life decision-making and c-fos expression in prefrontal subregions of rats. PLoS One (2012) 7:e37820. doi:10.1371/journal.pone.0037820.
43. Cao X, Huang S, Cao J, Chen T, Zhu P, Zhu R, et al. The timing of maternal separation affects morris water maze performance and long-term potentiation in male rats. Dev Psychobiol (2013) (in press). doi:10.1002/dev.21130.
44. Champagne FA, Curley JP. Epigenetic mechanisms mediating the long-term effects of maternal care on development. Neurosci Biobehav Rev (2009) 33:593-600. doi:10.1016/j.neubiorev.2007.10.009.
45. Claessens SE, Daskalakis NP, van der Veen R, Oitzl MS, de Kloet ER, Champagne DL. Development of individual differences in stress responsiveness: an overview of factors mediating the outcome of early life experiences. Psychopharmacology (Berl) (2011) 214:141-54. doi:10.1007/s00213-010-2118-y.
46. Nederhof E, Schmidt MV. Mismatch or cumulative stress: toward an integrated hypothesis of programming effects. Physiol Behav (2012) 106:691-700. doi:10.1016/j.physbeh.2011.12.008.
47. Karten YJ, Olariu A, Cameron HA. Stress in early life inhibits neurogenesis in adulthood. Trends Neurosci (2005) 28:171-2. doi:10.1016/j.tins.2005.01.009.
48. Lucassen PJ, Naninck EF, van Goudoever JB, Fitzsimons C, Joels M, Korosi A. Perinatal programming of adult hippocampal structure and function; emerging roles of stress, nutrition and epigenetics. Trends Neurosci (2013) 36:621-31. [Epub ahead of print]. doi:10.1016/j.tins.2013.08.002.
49. Sawada M, Sawamoto K. Mechanisms of neurogenesis in the normal and injured adult brain. Keio J Med (2013) 62:13-28. doi:10.2302/kjm.2012-0005-RE.
50. Kempermann G, Jessberger S, Steiner B, Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci (2004) 27:447-52. doi:10.1016/j.tins.2004.05.013.
51. von Bohlen und Halbach O. Immunohistological markers for proliferative events, gliogenesis, and neurogenesis within the adult hippocampus. Cell Tissue Res (2011) 345:1-19. doi:10.1007/s00441-011-1196-4.
52. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. Functional neurogenesis in the adult hippocampus. Nature (2002) 415:1030-4. doi:10.1038/4151030a.
53. Brown J, Cooper-Kuhn CM, Kempermann G, Van Praag H, Winkler J, Gage FH, et al. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci (2003) 17:2042-6. doi:10.1046/j.1460-9568.2003.02647.x.
54. Joels M, Karst H, Krugers HJ, Lucassen PJ. Chronic stress: implications for neuronal morphology, function and neurogenesis. Front Neuroendocrinol (2007) 28:72-96. doi:10.1016/j.yfrne.2007.04.001.
55. Czeh B, Lucassen PJ. What causes the hippocampal volume decrease in depression? Are neurogenesis, glial changes and apoptosis implicated? Eur Arch Psychiatry Clin Neurosci (2007) 257:250-60. doi:10.1007/s00406-007-0728-0.
56. Kempermann G, Krebs J, Fabel K. The contribution of failing adult hippocampal neurogenesis to psychiatric disorders. Curr Opin Psychiatry (2008) 21:290-5. doi:10.1097/YCO.0b013e3282fad375.
57. Sahay A, Hen R. Adult hippocampal neurogenesis in depression. Nat Neurosci (2007) 10:1110-5. doi:10.1038/nn1969.
58. Lucassen PJ, Fitzsimons CP, Korosi A, Joels M, Belzung C, Abrous DN. Stressing new neurons into depression? Mol Psychiatry (2013) 18:396-7. doi:10.1038/mp.2012.39.
59. Anacker C, Zunszain PA, Cattaneo A, Carvalho LA, Garabedian MJ, Thuret S, et al. Antidepressants increase human hippocampal neurogenesis by activating the glucocorticoid receptor. Mol Psychiatry (2011) 16:738-50. doi:10.1038/mp.2011.26.
60. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science (2003) 301:805-9. doi:10.1126/science.1083328.
61. Henn FA, Vollmayr B. Neurogenesis and depression: etiology or epiphenomenon? Biol Psychiatry (2004) 56:146-50. doi:10.1016/j.biopsych.2004.04.011.
62. Lucassen PJ, Stumpel MW, Wang Q, Aronica E. Decreased numbers of progenitor cells but no response to antidepressant drugs in the hippocampus of elderly depressed patients. Neuropharmacology (2010) 58:940-9. doi:10.1016/j.neuropharm.2010.01.012.
63. Lucassen PJ, Bosch OJ, Jousma E, Kromer SA, Andrew R, Seckl JR, et al. Prenatal stress reduces postnatal neurogenesis in rats selectively bred for high, but not low, anxiety: possible key role of placental 11beta-hydroxysteroid dehydrogenase type 2. Eur J Neurosci (2009) 29:97-103. doi:10.1111/j.1460-9568.2008.06543.x.
64. Belnoue L, Grosjean N, Ladeveze E, Abrous DN, Koehl M. Prenatal stress inhibits hippocampal neurogenesis but spares olfactory bulb neurogenesis. PLoS One (2013) 8:e72972. doi:10.1371/journal.pone.0072972.
65. Koehl M, Lemaire V, Mayo W, Abrous DN, Maccari S, Piazza PV, et al. Individual vulnerability to substance abuse and affective disorders: role of early environmental influences. Neurotox Res (2002) 4:281-96. doi:10.1080/1029842021000010866.
66. Mandyam CD, Crawford EF, Eisch AJ, Rivier CL, Richardson HN. Stress experienced in utero reduces sexual dichotomies in neurogenesis, microenvironment, and cell death in the adult rat hippocampus. Dev Neurobiol (2008) 68:575-89. doi:10.1002/dneu.20600.
67. Rayen I, van den Hove DL, Prickaerts J, Steinbusch HW, Pawluski JL. Fluoxetine during development reverses the effects of prenatal stress on depressive-like behavior and hippocampal neurogenesis in adolescence. PLoS One (2011) 6:e24003. doi:10.1371/journal.pone.0024003.
68. Madhyastha S, Sekhar S, Rao G. Resveratrol improves postnatal hippocampal neurogenesis and brain derived neurotrophic factor in prenatally stressed rats. Int J Dev Neurosci (2013) 31:580-5. doi:10.1016/j.ijdevneu.2013.06.010.
69. Wang H, Gondre-Lewis MC. Prenatal nicotine and maternal deprivation stress de-regulate the development of CA1, CA3, and dentate gyrus neurons in hippocampus of infant rats. PLoS One (2013) 8:e65517. doi:10.1371/journal.pone.0065517.
70. Oomen CA, Girardi CE, Cahyadi R, Verbeek EC, Krugers H, Joëls M, et al. Opposite effects of early maternal deprivation on neurogenesis in male versus female rats. PLoS One (2009) 4:e3675. doi:10.1371/journal.pone.0003675.
71. Oomen CA, Soeters H, Audureau N, Vermunt L, van Hasselt FN, Manders EM, et al. Early maternal deprivation affects dentate gyrus structure and emotional learning in adult female rats. Psychopharmacology (Berl) (2011) 214:249-60. doi:10.1007/s00213-010-1922-8.
72. Mirescu C, Peters JD, Gould E. Early life experience alters response of adult neurogenesis to stress. Nat Neurosci (2004) 7:841-6. doi:10.1038/nn1290.
73. Kumar G, Jones NC, Morris MJ, Rees S, O'Brien TJ, Salzberg MR. Early life stress enhancement of limbic epileptogenesis in adult rats: mechanistic insights. PLoS One (2011) 6:e24033. doi:10.1371/journal.pone.0024033.
74. Hulshof HJ, Novati A, Sgoifo A, Luiten PG, den Boer JA, Meerlo P. Maternal separation decreases adult hippocampal cell proliferation and impairs cognitive performance but has little effect on stress sensitivity and anxiety in adult Wistar rats. Behav Brain Res (2011) 216:552-60. doi:10.1016/j.bbr.2010.08.038.
75. Suri D, Veenit V, Sarkar A, Thiagarajan D, Kumar A, Nestler EJ, et al. Early stress evokes age-dependent biphasic changes in hippocampal neurogenesis, BDNF expression, and cognition. Biol Psychiatry (2013) 73:658-66. doi:10.1016/j.biopsych.2012.10.023.
76. Buwalda B, StubbendorffC, Zickert N, Koolhaas JM. Adolescent social stress does not necessarily lead to a compromised adaptive capacity during adulthood: a study on the consequences of social stress in rats. Neuroscience (2013) 249:258-70. doi:10.1016/j.neuroscience.2012.12.050.
77. Hu P, Oomen C, van Dam AM, Wester J, Zhou JN, Joels M, et al. A single-day treatment with mifepristone is sufficient to normalize chronic glucocorticoid induced suppression of hippocampal cell proliferation. PLoS One (2012) 7:e46224. doi:10.1371/journal.pone.0046224.
78. McClelland S, Korosi A, Cope J, Ivy A, Baram TZ. Emerging roles of epigenetic mechanisms in the enduring effects of early-life stress and experience on learning and memory. Neurobiol Learn Mem (2011) 96:79-88. doi:10.1016/j.nlm.2011.02.008.
79. Koo JW, Russo SJ, Ferguson D, Nestler EJ, Duman RS. Nuclear factor-kappaB is a critical mediator of stress-impaired neurogenesis and depressive behavior. Proc Natl Acad Sci U S A (2010) 107:2669-74. doi:10.1073/pnas.0910658107.
80. Anacker C, Cattaneo A, Musaelyan K, Zunszain PA, Horowitz M, Molteni R, et al. Role for the kinase SGK1 in stress, depression, and glucocorticoid effects on hippocampal neurogenesis. Proc Natl Acad Sci U S A (2013) 110:8708-13. doi:10.1073/pnas.1300886110.
81. Bagot RC, Tse YC, Nguyen HB, Wong AS, Meaney MJ, Wong TP. Maternal care influences hippocampal N-methyl-D-aspartate receptor function and dynamic regulation by corticosterone in adulthood. Biol Psychiatry (2012) 72:491-8. doi:10.1016/j.biopsych.2012.03.016.
82. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, et al. Epigenetic programming by maternal behavior. Nat Neurosci (2004) 7:847-54. doi:10.1038/nn1276.
83. Weaver IC. Epigenetic effects of glucocorticoids. Semin Fetal Neonatal Med (2009) 14:143-50. doi:10.1016/j.siny.2008.12.002.
84. Jacobson-Pick S, Richter-Levin G. Differential impact of juvenile stress and corticosterone in juvenility and in adulthood, in male and female rats. Behav Brain Res (2010) 214:268-76. doi:10.1016/j.bbr.2010.05.036.
85. Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, et al. Dynamics of hippocampal neurogenesis in adult humans. Cell (2013) 153:1219-27. doi:10.1016/j.cell.2013.05.002.
86. Knoth R, Singec I, Ditter M, Pantazis G, Capetian P, Meyer RP, et al. Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS One (2010) 5:e8809. doi:10.1371/journal.pone.0008809.
87. Boldrini M, Hen R, Underwood MD, Rosoklija GB, Dwork AJ, Mann JJ, et al. Hippocampal angiogenesis and progenitor cell proliferation are increased with antidepressant use in major depression. Biol Psychiatry (2012) 72:562-71. doi:10.1016/j.biopsych.2012.04.024.