Sex Differences in Adolescent Depression: Do Sex Hormones Determine Vulnerability?

Journal of Neuroendocrinology

Volumn 23, Issue 5, 2011, Pages 383-392

  Naninck, E F G ^a,b   Lucassen, P J ^a   Bakker, J ^b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

Adolescence; Depression; HPA axis; Sex steroids; Sexual differentiation

Indexed keywords

ESTRADIOL; ESTROGEN; NEUROTRANSMITTER; SEX HORMONE;

ADOLESCENT DISEASE; BRAIN DEVELOPMENT; DEPRESSION; HIPPOCAMPUS POTENTIAL; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MENTAL STRESS; MOOD CHANGE; MORBIDITY; NERVE CELL PLASTICITY; NEUROENDOCRINOLOGY; NONHUMAN; PRIORITY JOURNAL; PSYCHOLOGICAL THEORY; REVIEW; SEX DIFFERENCE; SEX DIFFERENTIATION; SOCIAL STRESS; VULNERABLE POPULATION;

ADOLESCENT; ADOLESCENT PSYCHOLOGY; ANIMALS; BRAIN; DEPRESSION; FEMALE; GONADAL STEROID HORMONES; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; PITUITARY-ADRENAL SYSTEM; RISK FACTORS; SEX CHARACTERISTICS; SEX DIFFERENTIATION; STRESS, PSYCHOLOGICAL;

EID: 79954549944     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2011.02125.x     Document Type: Review

References (95)

1. Allin S, Baris E, Farrington J, Guisset A, Jowett M, Koller T, Kutzin J, Lazarus J, Lear J, Loyola E, Mitis E, Nosikov A, Pellny M, Permanand G, Schiotz M, Sedgley M, Simpson S, Veillard J. The European Health Report 2009: Health and Health Systems (WHO). 2009; Online.
2. Nolen-Hoeksema S, Girgus JS. The emergence of gender differences in depression during adolescence. Psychol Bull 1994; 115: 424-443.
3. Frackiewicz EJ, Sramek JJ, Cutler NR. Gender differences in depression and antidepressant pharmacokinetics and adverse events. Ann Pharmacother 2000; 34: 80-88.
4. Solomon MB, Herman JP. Sex differences in psychopathology: of gonads, adrenals and mental illness. Physiol Behav 2009; 97: 250-258.
5. Joffe H, Cohen LS. Estrogen, serotonin, and mood disturbance: where is the therapeutic bridge? Biol Psychiatry 1998; 44: 798-811.
6. Kessler RC, McGonagle KA, Swartz M, Blazer DG, Nelson CB. Sex and depression in the National Comorbidity Survey. I: lifetime prevalence, chronicity and recurrence. J Affect Disord 1993; 29: 85-96.
7. Becker JB, Monteggia LM, Perrot-Sinal TS, Romeo RD, Taylor JR, Yehuda R, Bale TL. Stress and disease: is being female a predisposing factor? J Neurosci 2007; 27: 11851-11855.
8. Lenroot RK, Giedd JN. Sex differences in the adolescent brain. Brain Cogn 2010; 72: 46-55.
9. Greydanus DE, Bacopoulou F, Tsalamanios E. Suicide in adolescents: a worldwide preventable tragedy. Keio J Med 2009; 58: 95-102.
10. Hazell P. Depression in children and adolescents. Clin Evid (Online) 2009: 1-31.
11. Vitiello B. Treatment of adolescent depression: what we have come to know. Depress Anxiety 2009; 26: 393-395.
12. Leon AC. The revised warning for antidepressants and suicidality: unveiling the black box of statistical analyses. Am J Psychiatry 2007; 164: 1786-1789.
13. Ansorge MS, Zhou M, Lira A, Hen R, Gingrich JA. Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice. Science 2004; 306: 879-881.
14. Norcross M, Mathur P, Enoch AJ, Karlsson RM, Brigman JL, Cameron HA, Harvey-White J, Holmes A. Effects of adolescent fluoxetine treatment on fear-, anxiety- or stress-related behaviors in C57BL/6J or BALB/cJ mice. Psychopharmacology (Berl) 2008; 200: 413-424.
15. Hodes GE, Yang L, Van KJ, Santollo J, Shors TJ. Prozac during puberty: distinctive effects on neurogenesis as a function of age and sex. Neuroscience 2009; 163: 609-617.
16. Hodes GE, Hill-Smith TE, Suckow RF, Cooper TB, Lucki I. Sex-specific effects of chronic fluoxetine treatment on neuroplasticity and pharmacokinetics in mice. J Pharmacol Exp Ther 2010; 332: 266-273.
17. Bennett DS, Ambrosini PJ, Kudes D, Metz C, Rabinovich H. Gender differences in adolescent depression: do symptoms differ for boys and girls? J Affect Disord 2005; 89: 35-44.
18. Dahl RE. Adolescent brain development: a period of vulnerabilities and opportunities. Keynote address. Ann NY Acad Sci 2004; 1021: 1-22.
19. Neufang S, Specht K, Hausmann M, Gunturkun O, Herpertz-Dahlmann B, Fink GR, Konrad K. Sex differences and the impact of steroid hormones on the developing human brain. Cereb Cortex 2009; 19: 464-473.
20. Buchanan CM, Eccles JS, Becker JB. Are adolescents the victims of raging hormones: evidence for activational effects of hormones on moods and behavior at adolescence. Psychol Bull 1992; 111: 62-107.
21. Giedd JN, Clasen LS, Lenroot R, Greenstein D, Wallace GL, Ordaz S, Molloy EA, Blumenthal JD, Tossell JW, Stayer C, Samango-Sprouse CA, Shen D, Davatzikos C, Merke D, Chrousos GP. Puberty-related influences on brain development. Mol Cell Endocrinol 2006; 254-255: 154-162.
22. Peper JS, Brouwer RM, Schnack HG, van Baal GC, van LM, van den Berg SM, Delemarre-Van de Waal HA, Boomsma DI, Kahn RS, Hulshoff Pol HE. Sex steroids and brain structure in pubertal boys and girls. Psychoneuroendocrinology 2009; 34: 332-342.
23. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL. Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 1999; 2: 861-863.
24. Bao AM, Swaab DF. Sex differences in the brain, behavior, and neuropsychiatric disorders. Neuroscientist 2010; 16: 550-565.
25. Schwarz JM, McCarthy MM. Steroid-induced sexual differentiation of the developing brain: multiple pathways, one goal. J Neurochem 2008; 105: 1561-1572.
26. Murakami S, Arai Y. Neuronal death in the developing sexually dimorphic periventricular nucleus of the preoptic area in the female rat: effect of neonatal androgen treatment. Neurosci Lett 1989; 102: 185-190.
27. Nordeen EJ, Nordeen KW, Sengelaub DR, Arnold AP. Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus. Science 1985; 229: 671-673.
28. Zhou JN, Hofman MA, Gooren LJ, Swaab DF. A sex difference in the human brain and its relation to transsexuality. Nature 1995; 378: 68-70.
29. Phoenix CH, Goy RW, Gerall AA, Young WC. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 1959; 65: 369-382.
30. Schulz KM, Molenda-Figueira HA, Sisk CL. Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence. Horm Behav 2009; 55: 597-604.
31. Manson JE. Prenatal exposure to sex steroid hormones and behavioral/cognitive outcomes. Metabolism 2008; 57(Suppl. 2): S16-S21.
32. Bakker J, Baum MJ. Role for estradiol in female-typical brain and behavioral sexual differentiation. Front Neuroendocrinol 2008; 29: 1-16.
33. Hines M, Allen LS, Gorski RA. Sex differences in subregions of the medial nucleus of the amygdala and the bed nucleus of the stria terminalis of the rat. Brain Res 1992; 579: 321-326.
34. Ahmed EI, Zehr JL, Schulz KM, Lorenz BH, DonCarlos LL, Sisk CL. Pubertal hormones modulate the addition of new cells to sexually dimorphic brain regions. Nat Neurosci 2008; 11: 995-997.
35. Schulz KM, Sisk CL. Pubertal hormones, the adolescent brain, and the maturation of social behaviors: lessons from the Syrian hamster. Mol Cell Endocrinol 2006; 254-255: 120-126.
36. Sisk CL, Zehr JL. Pubertal hormones organize the adolescent brain and behavior. Front Neuroendocrinol 2005; 26: 163-174.
37. Wallen K. Hormonal influences on sexually differentiated behavior in nonhuman primates. Front Neuroendocrinol 2005; 26: 7-26.
38. Tobet S, Knoll JG, Hartshorn C, Aurand E, Stratton M, Kumar P, Searcy B, McClellan K. Brain sex differences and hormone influences: a moving experience? J Neuroendocrinol 2009; 21: 387-392.
39. Zehr JL, Nichols LR, Schulz KM, Sisk CL. Adolescent development of neuron structure in dentate gyrus granule cells of male Syrian hamsters. Dev Neurobiol 2008; 68: 1517-1526.
40. Markham JA, Morris JR, Juraska JM. Neuron number decreases in the rat ventral, but not dorsal, medial prefrontal cortex between adolescence and adulthood. Neuroscience 2007; 144: 961-968.
41. Schildkraut JJ. The catecholamine hypothesis of affective disorders: a review of supporting evidence. Am J Psychiatry 1965; 122: 509-522.
42. Steiner M, Dunn E, Born L. Hormones and mood: from menarche to menopause and beyond. J Affect Disord 2003; 74: 67-83.
43. Hughes CW, Petty F, Sheikha S, Kramer GL. Whole-blood serotonin in children and adolescents with mood and behavior disorders. Psychiatry Res 1996; 65: 79-95.
44. Castren E. Is mood chemistry? Nat Rev Neurosci 2005; 6: 241-246.
45. 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: 250-260.
46. Lucassen PJ, Meerlo P, Naylor AS, van Dam AM, Dayer AG, Fuchs E, Oomen CA, Czeh B. Regulation of adult neurogenesis by stress, sleep disruption, exercise and inflammation: implications for depression and antidepressant action. Eur Neuropsychopharmacol 2010; 20: 1-17.
47. Romeo RD, McEwen BS. Stress and the adolescent brain. Ann NY Acad Sci 2006; 1094: 202-214.
48. Swaab DF, Bao AM, Lucassen PJ. The stress system in the human brain in depression and neurodegeneration. Ageing Res Rev 2005; 4: 141-194.
49. Raadsheer FC, van Heerikhuize JJ, Lucassen PJ, Hoogendijk WJ, Tilders FJ, Swaab DF. Corticotropin-releasing hormone mRNA levels in the paraventricular nucleus of patients with Alzheimer's disease and depression. Am J Psychiatry 1995; 152: 1372-1376.
50. Lucassen PJ, Muller MB, Holsboer F, Bauer J, Holtrop A, Wouda J, Hoogendijk WJ, De Kloet ER, Swaab DF. Hippocampal apoptosis in major depression is a minor event and absent from subareas at risk for glucocorticoid overexposure. Am J Pathol 2001; 158: 453-468.
51. Muller MB, Lucassen PJ, Yassouridis A, Hoogendijk WJ, Holsboer F, Swaab DF. Neither major depression nor glucocorticoid treatment affects the cellular integrity of the human hippocampus. Eur J Neurosci 2001; 14: 1603-1612.
52. Boldrini M, Underwood MD, Hen R, Rosoklija GB, Dwork AJ, John MJ, Arango V. Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology 2009; 34: 2376-2389.
53. 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: 940-949.
54. Campbell S, Marriott M, Nahmias C, MacQueen GM. Lower hippocampal volume in patients suffering from depression: a meta-analysis. Am J Psychiatry 2004; 161: 598-607.
55. Axelson DA, Doraiswamy PM, McDonald WM, Boyko OB, Tupler LA, Patterson LJ, Nemeroff CB, Ellinwood EH Jr, Krishnan KR. Hypercortisolemia and hippocampal changes in depression. Psychiatry Res 1993; 47: 163-173.
56. Bremner JD, Narayan M, Anderson ER, Staib LH, Miller HL, Charney DS. Hippocampal volume reduction in major depression. Am J Psychiatry 2000; 157: 115-118.
57. Janssen J, Hulshoff Pol HE, Lampe IK, Schnack HG, de Leeuw FE, Kahn RS, Heeren TJ. Hippocampal changes and white matter lesions in early-onset depression. Biol Psychiatry 2004; 56: 825-831.
58. Videbech P, Ravnkilde B. Hippocampal volume and depression: a meta-analysis of MRI studies. Am J Psychiatry 2004; 161: 1957-1966.
59. Chen MC, Hamilton JP, Gotlib IH. Decreased hippocampal volume in healthy girls at risk of depression. Arch Gen Psychiatry 2010; 67: 270-276.
60. Oomen CA, Soeters H, Audureau N, Vermunt L, van Hasselt FN, Manders EM, Joels M, Lucassen PJ, Krugers H. 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: 6635-6645.
61. Oomen CA, Soeters H, Audureau N, Vermunt L, van Hasselt FN, Manders EMM, Joëls M, Krugers H, Lucassen PJ. Early maternal deprivation affects dentate gyrus structure and emotional learning in adult females. Psychopharmacology 2011; 214: 249-260.
62. Vythilingam M, Heim C, Newport J, Miller AH, Anderson E, Bronen R, Brummer M, Staib L, Vermetten E, Charney DS, Nemeroff CB, Bremner JD. Childhood trauma associated with smaller hippocampal volume in women with major depression. Am J Psychiatry 2002; 159: 2072-2080.
63. Heine VM, Maslam S, Zareno J, Joels M, Lucassen PJ. Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur J Neurosci 2004; 19: 131-144.
64. Leventopoulos M, Ruedi-Bettschen D, Knuesel I, Feldon J, Pryce CR, Opacka-Juffry J. Long-term effects of early life deprivation on brain glia in Fischer rats. Brain Res 2007; 1142: 119-126.
65. Fabricius K, Wortwein G, Pakkenberg B. The impact of maternal separation on adult mouse behaviour and on the total neuron number in the mouse hippocampus. Brain Struct Funct 2008; 212: 403-416.
66. Huot RL, Plotsky PM, Lenox RH, McNamara RK. Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Res 2002; 950: 52-63.
67. Aisa B, Elizalde N, Tordera R, Lasheras B, Del RJ, Ramirez MJ. Effects of neonatal stress on markers of synaptic plasticity in the hippocampus: implications for spatial memory. Hippocampus 2009; 19: 1222-1231.
68. Mirescu C, Peters JD, Gould E. Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 2004; 7: 841-846.
69. Oomen CA, Girardi CE, Cahyadi R, Verbeek EC, Krugers H, Joels M, Lucassen PJ. Opposite effects of early maternal deprivation on neurogenesis in male versus female rats. PLoS ONE 2009; 4: e3675.
70. Schmitz C, Rhodes ME, Bludau M, Kaplan S, Ong P, Ueffing I, Vehoff J, Korr H, Frye CA. Depression: reduced number of granule cells in the hippocampus of female, but not male, rats due to prenatal restraint stress. Mol Psychiatry 2002; 7: 810-813.
71. Weinstock M. Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 2007; 32: 1730-1740.
72. Levine S, Chevalier JA, Korchin SJ. The effects of early shock and handling on later avoidance learning. J Pers 1956; 24: 475-493.
73. Lehmann J, Russig H, Feldon J, Pryce CR. Effect of a single maternal separation at different pup ages on the corticosterone stress response in adult and aged rats. Pharmacol Biochem Behav 2002; 73: 141-145.
74. Plotsky PM, Meaney MJ. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res Mol Brain Res 1993; 18: 195-200.
75. Pryce CR, Feldon J. Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms. Neurosci Biobehav Rev 2003; 27: 57-71.
76. Rao U, Chen LA, Bidesi AS, Shad MU, Thomas MA, Hammen CL. Hippocampal changes associated with early-life adversity and vulnerability to depression. Biol Psychiatry 2010; 67: 357-364.
77. McEwen BS. Early life influences on life-long patterns of behavior and health. Ment Retard Dev Disabil Res Rev 2003; 9: 149-154.
78. Heim C, Nemeroff CB. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 2001; 49: 1023-1039.
79. Seeman MV. Psychopathology in women and men: focus on female hormones. Am J Psychiatry 1997; 154: 1641-1647.
80. Romeo RD. Adolescence: a central event in shaping stress reactivity. Dev Psychobiol 2010; 52: 244-253.
81. Sapolsky RM, Meaney MJ. Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res 1986; 396: 64-76.
82. Romeo RD, Lee SJ, McEwen BS. Differential stress reactivity in intact and ovariectomized prepubertal and adult female rats. Neuroendocrinology 2004; 80: 387-393.
83. Romeo RD, Lee SJ, Chhua N, McPherson CR, McEwen BS. Testosterone cannot activate an adult-like stress response in prepubertal male rats. Neuroendocrinology 2004; 79: 125-132.
84. Doremus-Fitzwater TL, Varlinskaya EI, Spear LP. Social and non-social anxiety in adolescent and adult rats after repeated restraint. Physiol Behav 2009; 97: 484-494.
85. Tsoory M, Richter-Levin G. Learning under stress in the adult rat is differentially affected by 'juvenile' or 'adolescent' stress. Int J Neuropsychopharmacol 2006; 9: 713-728.
86. Barha CK, Brummelte S, Lieblich SE, Galea LA. Chronic restraint stress in adolescence differentially influences hypothalamic-pituitary-adrenal axis function and adult hippocampal neurogenesis in male and female rats. Hippocampus 2010; [Epub ahead of print] doi:10.1002/hipo.20829.
87. McCormick CM, Mathews IZ. HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol Biochem Behav 2007; 86: 220-233.
88. Shors TJ, Chua C, Falduto J. Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J Neurosci 2001; 21: 6292-6297.
89. Dalla C, Whetstone AS, Hodes GE, Shors TJ. Stressful experience has opposite effects on dendritic spines in the hippocampus of cycling versus masculinized females. Neurosci Lett 2009; 449: 52-56.
90. Rubinow DR, Schmidt PJ, Roca CA. Estrogen-serotonin interactions: implications for affective regulation. Biol Psychiatry 1998; 44: 839-850.
91. Toufexis D. Region- and sex-specific modulation of anxiety behaviours in the rat. J Neuroendocrinol 2007; 19: 461-473.
92. Warren MP, Brooks-Gunn J. Mood and behavior at adolescence: evidence for hormonal factors. J Clin Endocrinol Metab 1989; 69: 77-83.
93. Dalla C, Edgecomb C, Whetstone AS, Shors TJ. Females do not express learned helplessness like males do. Neuropsychopharmacology 2008; 33: 1559-1569.
94. Shors TJ, Mathew J, Sisti HM, Edgecomb C, Beckoff S, Dalla C. Neurogenesis and helplessness are mediated by controllability in males but not in females. Biol Psychiatry 2007; 62: 487-495.
95. Dalla C, Antoniou K, Drossopoulou G, Xagoraris M, Kokras N, Sfikakis A, Papadopoulou-Daifoti Z. Chronic mild stress impact: are females more vulnerable? Neuroscience 2005; 135: 703-714.