DHEA effects on brain and behavior: Insights from comparative studies of aggression

Journal of Steroid Biochemistry and Molecular Biology

Volumn 145, Issue , 2015, Pages 261-272

  Soma, Kiran K ^a   Rendon, Nikki M ^b   Boonstra, Rudy ^c   Albers, H Elliott ^d   Demas, Gregory E ^b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b INDIANA UNIVERSITY   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Aggressive behavior; Aromatase; Estradiol; Hamster; Intracrinology; Sex difference; Songbird; Stress

Indexed keywords

ANDROGEN; CHOLESTEROL; HORMONE PRECURSOR; MELATONIN; NEUROSTEROID; PRASTERONE; SEX HORMONE; TESTOSTERONE; AROMATASE; ESTRADIOL;

AGGRESSION; BIRD; BRAIN REGION; BREEDING; COMPARATIVE STUDY; ENDOCRINE FUNCTION; HORMONAL REGULATION; MAMMAL; NONHUMAN; REVIEW; SEASONAL VARIATION; STEROIDOGENESIS; TESTOSTERONE SYNTHESIS; ANIMAL; ANIMAL BEHAVIOR; BRAIN; FEMALE; HAMSTER; HUMAN; MALE; METABOLISM; PRIMATE; RAT; SOCIAL BEHAVIOR; SONGBIRD;

CRICETINAE; PASSERI;

AGGRESSION; ANDROGENS; ANIMALS; AROMATASE; BEHAVIOR, ANIMAL; BRAIN; CRICETINAE; DEHYDROEPIANDROSTERONE; ESTRADIOL; FEMALE; HUMANS; MALE; PRIMATES; RATS; SOCIAL BEHAVIOR; SONGBIRDS; TESTOSTERONE;

EID: 84915756716     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2014.05.011     Document Type: Review

References (156)

1. K.E. Moyer The Physiology of Hostility 1971 Markham Pub. Co. Chicago
2. D.C. Blanchard, and R.J. Blanchard Ethoexperimental approaches to the biology of emotion Annu. Rev. Psychol. 39 1988 43 68
3. H.E. Albers, K.L. Huhman, and R.L. Meisel Hormonal basis of social conflict and communication D.W. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, R.T. Rubin, Hormones, Brain and Behavior 2002 Academic Press New York 393 433
4. P. Brain, and A. Poole Some studies on use of standard opponents in intermale aggression testing in TT Albino Mice Behaviour 50 1974 100 110
5. V. Canoine, and E. Gwinner The hormonal response of female European stonechats to a territorial intrusion: the role of the male partner Horm. Behav. 47 2005 563 568
6. M.M. Landys, W. Goymann, M. Raess, and T. Slagsvold Hormonal responses to male-male social challenge in the blue tit Cyanistes caeruleus: single-broodedness as an explanatory variable Physiol. Biochem. Zool. 80 2007 228 240
7. J.C. Wingfield Short-term changes in plasma levels of hormones during establishment and defense of a breeding territory in male song sparrows, Melospiza Melodia Horm. Behav. 19 1985 174 187
8. B. Olivier, and D. Vandalen Social behavior in rats and mice: an ethologically based model for differentiating psychoactive drugs Aggressive Behav. 8 1982 163 168
9. H.E. Albers The regulation of social recognition, social communication and aggression: vasopressin in the social behavior neural network Horm. Behav. 61 2012 283 292
10. G.E. Demas, M.A. Cooper, H.E. Albers, and K.K. Soma Novel mechanisms underlying neuroendocrine regulation of aggression: a synthesis of rodent, avian, and primate studies A. Lajtha, J.D. Blaustein, Handbook of Neurochemistry and Molecular Neurobiology 2007 Springer US 337 372
11. K.K. Soma, K.A. Sullivan, A.D. Tramontin, C.J. Saldanha, B.A. Schlinger, and J.C. Wingfield Acute and chronic effects of an aromatase inhibitor on territorial aggression in breeding and nonbreeding male song sparrows J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 186 2000 759 769
12. K.K. Soma, A.D. Tramontin, and J.C. Wingfield Oestrogen regulates male aggression in the non-breeding season Proc. R. Soc. B: Biol. Sci. 267 2000 1089 1096
13. J.L. Do Rego, J.Y. Seong, D. Burel, J. Leprince, V. Luu-The, K. Tsutsui, M.-C. Tonon, G. Pelletier, and H. Vaudry Neurosteroid biosynthesis: enzymatic pathways and neuroendocrine regulation by neurotransmitters and neuropeptides Front. Neuroendocrinol. 30 2009 259 301
14. J.L. Do Rego, J.Y. Seong, D. Burel, J. Leprince, D. Vaudry, V. Luu-The, M.-C. Tonon, K. Tsutsui, G. Pelletier, and H. Vaudry Regulation of neurosteroid biosynthesis by neurotransmitters and neuropeptides Front. Endocrinol. 4 2012 1 15
15. N.G. Simon Hormonal processes in the development and expression of aggressive behavior D.W. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, R.T. Rubin, Hormones, Brain and Behavior vol. 1 2002 Academic Press Waltham, MA 339 373
16. M.J. Benton, and P.C.J. Donoghue Paleontological evidence to date the tree of life Mol. Biol. Evol. 24 2007 26 53
17. M.J. Benton, P.C.J. Donoghue, and R.J. Asher Calibrating and constraining molecular clocks S.B. Hedges, S. Kumar, The Timetree of Life 2009 35 86
18. M.A. O'Leary, J.I. Bloch, J.J. Flynn, T.J. Gaudin, A. Giallombardo, N.P. Giannini, S.L. Goldberg, B.P. Kraatz, Z.-X. Luo, and J. Meng The placental mammal ancestor and the post-K-Pg radiation of placentals Science 339 2013 662 667
19. K.K. Soma, and J.C. Wingfield Endocrinology of aggression in the nonbreeding season N.J. Adams, R.H. Slotow, 22nd International Ornithological Congress 1999 Johannesburg BirdLife, South Africa 1606 1620
20. K.K. Soma, and J.C. Wingfield Dehydroepiandrosterone in songbird plasma: seasonal regulation and relationship to territorial aggression Gen. Comp. Endocrinol. 123 2001 144 155
21. J.C. Wingfield, and T.P. Hahn Testosterone and territorial behaviour in sedentary and migratory sparrows Anim. Behav. 47 1994 77 89
22. K.K. Soma Testosterone and aggression: Berthold, birds and beyond J. Neuroendocrinol. 18 2006 543 551
23. S.A. Heimovics, H.B. Fokidis, and K.K. Soma Brain aromatase and territorial aggression across the seasons in male song sparrows J. Balthazart, G.F. Ball, Brain, Aromatase, Estrogens and Behavior 2013 Oxford University Press Oxford 199 220
24. K.K. Soma, V.N. Hartman, J.C. Wingfield, and E.A. Brenowitz Seasonal changes in androgen receptor immunoreactivity in the song nucleus HVc of a wild bird J. Comp. Neurol. 409 1999 224 236
25. K.K. Soma, B.A. Schlinger, J.C. Wingfield, and C.J. Saldanha Brain aromatase, 5 alpha-reductase, and 5 beta-reductase change seasonally in wild male song sparrows: relationship to aggressive and sexual behavior J. Neurobiol. 56 2003 209 221
26. J.C. Wingfield Control of territorial aggression in a changing environment Psychoneuroendocrinology 19 1994 709 721
27. K.K. Soma, R.K. Bindra, J. Gee, J.C. Wingfield, and B.A. Schlinger Androgen-metabolizing enzymes show region-specific changes across the breeding season in the brain of a wild songbird J. Neurobiol. 41 1999 176 188
28. D.W. Wacker, J.C. Wingfield, J.E. Davis, and S.L. Meddle Seasonal changes in aromatase and androgen receptor, but not estrogen receptor mRNA expression in the brain of the free-living male song sparrow, Melospiza melodia morphna J. Comp. Neurol. 518 2010 3819 3835
29. J.L. Goodson, C.J. Saldanha, T.P. Hahn, and K.K. Soma Recent advances in behavioral neuroendocrinology: insights from studies on birds Horm. Behav. 48 2005 461 473
30. C.J. Maddison, R.C. Anderson, N.H. Prior, M.D. Taves, and K.K. Soma Soft song during aggressive interactions: seasonal changes and endocrine correlates in song sparrows Horm. Behav. 62 2012 455 463
31. A.E.M. Newman, S.A. MacDougall-Shackleton, Y.S. An, B. Kriengwatana, and K.K. Soma Corticosterone and dehydroepiandrosterone have opposing effects on adult neuroplasticity in the avian song control system J. Comp. Neurol. 518 2010 3662 3678
32. A.E.M. Newman, D.S. Pradhan, and K.K. Soma Dehydroepiandrosterone and corticosterone are regulated by season and acute stress in a wild songbird: jugular versus brachial plasma Endocrinology 149 2008 2537 2545
33. A.E.M. Newman, and K.K. Soma Corticosterone and dehydroepiandrosterone in songbird plasma and brain: effects of season and acute stress Eur. J. Neurosci. 29 2009 1905 1914
34. A.E.M. Newman, and K.K. Soma Aggressive interactions differentially modulate local and systemic levels of corticosterone and DHEA in a wild songbird Horm. Behav. 60 2011 389 396
35. D.S. Pradhan, A.E.M. Newman, D.W. Wacker, J.C. Wingfield, B.A. Schlinger, and K.K. Soma Aggressive interactions rapidly increase androgen synthesis in the brain during the non-breeding season Horm. Behav. 57 2010 381 389
36. L. Koren, E.S.M. Ng, K.K. Soma, and K.E. Wynne-Edwards Sample preparation and liquid chromatography-tandem mass spectrometry for multiple steroids in mammalian and avian circulation PLoS ONE 7 2012 e32496
37. M. Bauer, A.C. Hamm, M. Bonaus, A. Jacob, J. Jaekel, H. Schorle, M.J. Pankratz, and J.D. Katzenberger Starvation response in mouse liver shows strong correlation with life-span-prolonging processes Physiol. Genomics 17 2004 230 244
38. H.B. Fokidis, N.H. Prior, and K.K. Soma Fasting increases aggression and differentially modulates local and systemic steroid levels in male zebra finches Endocrinology 154 2013 4328 4339
39. L.L. Grasfeder, S. Gaillard, S.R. Hammes, O. Ilkayeva, C.B. Newgard, R.B. Hochberg, M.A. Dwyer, C.-y. Chang, and D.P. McDonnell Fasting-induced hepatic production of DHEA is regulated by PGC-1 alpha, ERR alpha, and HNF4 alpha Mol. Endocrinol. 23 2009 1171 1182
40. S.E. London, N.A. Alday, H. Tam, and B.A. Schlinger Enzymes necessary for de novo steroid synthesis are expressed along lateral ventricles in developing zebra finch brains Horm. Behav. 46 2004 95
41. B.A. Schlinger, and L. Remage-Healey Neurosteroidogenesis: insights from studies of songbirds J. Neuroendocrinol. 24 2012 16 21
42. K. Tsutsui, S. Haraguchi, M. Hatori, T. Hirota, and Y. Fukada Biosynthesis and biological actions of pineal neurosteroids in domestic birds Neuroendocrinology 98 2013 97 105
43. K. Tsutsui, M. Matsunaga, H. Miyabara, and K. Ukena Neurosteroid biosynthesis in the quail brain: a review J. Exp. Zool. A: Comp. Exp. Biol. 305A 2006 733 742
44. K.K. Soma, A.M. Wissman, E.A. Brenowitz, and J.C. Wingfield Dehydroepiandrosterone (DHEA) increases territorial song and the size of an associated brain region in a male songbird Horm. Behav. 41 2002 203 212
45. H. Wada, A.E.M. Newman, Z.J. Hall, K.K. Soma, and S.A. MacDougall-Shackleton Effects of corticosterone and DHEA on doublecortin immunoreactivity in the song control system and hippocampus of adult song sparrows Dev. Neurobiol. 74 2014 52 62
46. K.K. Soma, N.A. Alday, M. Hau, and B.A. Schlinger Dehydroepiandrosterone metabolism by 3β-hydroxysteroid dehydrogenase/Δ5-Δ4 isomerase in adult zebra finch brain: sex difference and rapid effect of stress Endocrinology 145 2004 1668 1677
47. N.T. Owen-Ashley, D. Hasselquist, and J.C. Wingfield Androgens and the immunocompetence handicap hypothesis: unraveling direct and indirect pathways of immunosuppression in song sparrows Am. Nat. 164 2004 490 505
48. D.S. Pradhan, Y. Yu, and K.K. Soma Rapid estrogen regulation of DHEA metabolism in the male and female songbird brain J. Neurochem. 104 2008 244 253
49. B.A. Schlinger, D.S. Pradhan, and K.K. Soma 3 beta-HSD activates DHEA in the songbird brain Neurochem. Int. 52 2008 611 620
50. S.A. Heimovics, N.H. Prior, C.J. Maddison, and K.K. Soma Rapid and widespread effects of 17 beta-estradiol on intracellular signaling in the male songbird brain: a seasonal comparison Endocrinology 153 2012 1364 1376
51. E.J. Filardo, and P. Thomas GPR30: a seven-transmembrane-spanning estrogen receptor that triggers EGF release Trends Endocrinol. Metab. 16 2005 362 367
52. M. Hau, S.T. Stoddard, and K.K. Soma Territorial aggression and hormones during the non-breeding season in a tropical bird Horm. Behav. 45 2004 40 49
53. M. Hau, M. Wikelski, K.K. Soma, and J.C. Wingfield Testosterone and year-round territorial aggression in a tropical bird Gen. Comp. Endocrinol. 117 2000 20 33
54. D.L. Duffy, G.E. Bentley, D.L. Drazen, and G.F. Ball Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European starlings Behav. Ecol. 11 2000 654 662
55. S.A. Cavigelli, and M.E. Pereira Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta) Horm. Behav. 37 2000 246 255
56. D.A. Edwards Early androgen stimulation and aggressive behavior in male and female mice Physiol. Behav. 4 1969 333 338
57. M.J. Fuxjager, J.L. Montgomery, and C.A. Marler Species differences in the winner effect disappear in response to post-victory testosterone manipulations Proc. R. Soc. B: Biol. Sci. 278 2011 3497 3503
58. M.J. Fuxjager, T.O. Oyegbile, and C.A. Marler Independent and additive contributions of postvictory testosterone and social experience to the development of the winner effect Endocrinology 152 2011 3422 3429
59. J. Uhrich The social hierarchy in albino mice J. Comp. Psychol. 25 1938 373 413
60. G.E. Demas, K.K. Soma, and H.E. Albers DHEA and aggression R.R. Watson, DHEA in Human Health and Aging 2011 Taylor & Francis Group LLC London 415 431
61. K.K. Soma, M.-A.L. Scotti, A.E.M. Newman, T.D. Charlier, and G.E. Demas Novel mechanisms for neuroendocrine regulation of aggression Front. Neuroendocrinol. 29 2008 476 489
62. E.E. Baulieu Steroid hormones in the brain: several mechanisms? K. Fuxe, J.A. Gustafsson, L. Wetterberg, Steroid Hormone Regulation of the Brain 1981 Pergamon Oxford 3 14
63. E.E. Baulieu Neurosteroids: a new function in the brain Biol. Cell 71 1991 3 10
64. E.E. Baulieu Neurosteroids: of the nervous system, by the nervous system, for the nervous system P.M. Conn, Proceedings of the 1996 Conference Recent Progress in Hormone Research, vol. 52 1997 1 32
65. E.E. Baulieu, and P. Robel Dehydroepiandrosterone (DHEA) and dehydroepiandrosterone sulfate (DHEAS) as neuroactive neurosteroids Proc. Natl. Acad. Sci. U.S.A. 95 1998 4089 4091
66. C. Corpechot, P. Robel, M. Axelson, J. Sjovall, and E.E. Baulieu Characterization and measurement of dehydroepiandrosterone sulfate in rat brain Proc. Natl. Acad. Sci. U.S.A.: Biol. Sci. 78 1981 4704 4707
67. R. Boonstra, J.E. Lane, S. Boutin, A. Bradley, L. Desantis, A.E.M. Newman, and K.K. Soma Plasma DHEA levels in wild, territorial red squirrels: seasonal variation and effect of ACTH Gen. Comp. Endocrinol. 158 2008 61 67
68. H.K. Caldwell, D.A. Smith, and H.E. Albers Photoperiodic mechanisms controlling scent marking: interactions of vasopressin and gonadal steroids Eur. J. Neurosci. 27 2008 1189 1196
69. S.J. Gutzler, M. Karom, W.D. Erwin, and H.E. Albers Photoperiodic regulation of adrenal hormone secretion and aggression in female Syrian hamsters Horm. Behav. 56 2009 481 489
70. D.R. Pieper, and C.A. Lobocki Characterization of serum dehydroepiandrosterone secretion in golden hamsters Proc. Soc. Exp. Biol. Med. 224 2000 278 284
71. M.-A.L. Scotti, J. Belen, J.E. Jackson, and G.E. Demas The role of androgens in the mediation of seasonal territorial aggression in male Siberian hamsters (Phodopus sungorus) Physiol. Behav. 95 2008 633 640
72. M.-A.L. Scotti, K.L. Schmidt, A.E.M. Newman, T. Bonu, K.K. Soma, and G.E. Demas Aggressive encounters differentially affect serum dehydroepiandrosterone and testosterone concentrations in male Siberian hamsters (Phodopus sungorus) Horm. Behav. 56 2009 376 381
73. J. Balthazart, A. Foidart, C. Surlemont, and N. Harada Distribution of aromatase-immunoreactive cells in the mouse forebrain Cell Tissue Res. 263 1991 71 79
74. E. Dupont, J. Simard, V. Luuthe, F. Labrie, and G. Pelletier Localization of 3-beta-hydroxysteroid dehydrogenase in rat brain as studied by in situ hybridization Mol. Cell. Neurosci. 5 1994 119 123
75. C. Le goascogne, P. Robel, M. Gouezou, N. Sananes, E.E. Baulieu, and M. Waterman Neurosteroids: cytochrome p450scc in rat brain Science 237 1987 1212 1215
76. G. Pelletier, V. Luu-The, S. Li, G. Bujold, and F. Labrie Localization and glucocorticoid regulation of 11 beta-hydroxysteroid dehydrogenase type 1 mRNA in the male mouse forebrain Neuroscience 145 2007 110 115
77. G. Pelletier, V. Luu-The, S. Li, L. Ren, and F. Labrie Sex-related expression of 20 alpha-hydroxysteroid dehydrogenase mRNA in the adult mouse J. Histochem. Cytochem. 51 2003 1425 1436
78. P. Robel, and E.E. Baulieu Neuro-steroids: 3beta-hydroxy-delta-5-derivatives in the rodent brain Neurochem. Int. 7 1985 953 958
79. N.A. Compagnone, and S.H. Mellon Neurosteroids: biosynthesis and function of these novel neuromodulators Front. Neuroendocrinol. 21 2000 1 56
80. S.H. Mellon, and H. Vaudry Biosynthesis of neurosteroids and regulation of their synthesis Neurosteroids Brain Funct. 46 2001 33 78
81. K. Tsutsui, K. Ukena, M. Usui, H. Sakamoto, and M. Takase Novel brain function: biosynthesis and actions of neurosteroids in neurons Neurosci. Res. 36 2000 261 273
82. G. Pinna, E. Costa, and A. Guidotti Changes in brain testosterone and allopregnanolone biosynthesis elicit aggressive behavior Proc. Natl. Acad. Sci. U.S.A. 102 2005 2135 2140
83. S. Higo, Y. Hojo, H. Ishii, T. Kominami, K. Nakajima, D. Poirier, T. Kimoto, and S. Kawato Comparison of sex-steroid synthesis between neonatal and adult rat hippocampus Biochem. Biophys. Res. Commun. 385 2009 62 66
84. Y. Hojo, T. Hattori, T. Enami, A. Furukawa, K. Suzuki, H.T. Ishii, H. Mukai, J.H. Morrison, W.G.M. Janssen, and S. Kominami Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017 alpha and P450 aromatase localized in neurons Proc. Natl. Acad. Sci. U.S.A. 101 2004 865 870
85. S. Kawato, Y. Hojo, H. Mukai, G. Murakami, M. Ogiue-Ikeda, H. Ishii, and T. Kimoto Local production of estrogen and its rapid modulatory action on synaptic plasticity M.S. Ritsner, A. Weizman, Neuroactive Steroids in Brain Function, Behavior and Neuropsychiatric Disorders 2008 Springer US 143 170
86. C. Cascio, R.C. Brown, Y. Liu, Z.Q. Han, D.B. Hales, and V. Papadopoulos Pathways of dehydroepiandrosterone formation in rat brain glia J. Steroid Biochem. Mol. Biol. 75 2000 177 186
87. C. Cascio, V.V.K. Prasad, Y.Y. Lin, S. Lieberman, and V. Papadopoulos Detection of P450c17-independent pathways for dehydroepiandrosterone (DHEA) biosynthesis in brain glial tumor cells Proc. Natl. Acad. Sci. U.S.A. 95 1998 2862 2867
88. L.B. Nicolas, W. Pinoteau, S. Papot, S. Routier, G. Guillaumet, and S. Mortaud Aggressive behavior induced by the steroid sulfatase inhibitor COUMATE and by DHEAS in CBA/H mice Brain Res. 922 2001 216 222
89. S. Mortaud, L. Nicolas, W. Pinoteau, S. Tordjman, M. Carlier, and P.L. Roubertoux Brain pathways mediating the pro-aggressive effect of the steroid sulfatase (Sts) gene Behav. Genet. 40 2010 211 219
90. S.J. Webb, T.E. Geoghegan, and R.A. Prough The biological actions of dehydroepiandrosterone involves multiple receptors Drug Metab. Rev. 38 2006 89 116
91. M.E. Baker Co-evolution of steroidogenic and steroid-inactivating enzymes and adrenal and sex steroid receptors Mol. Cell. Endocrinol. 215 2004 55 62
92. R.C. Agis-Balboa, G. Pinna, F. Pibiri, B. Kadriu, E. Costa, and A. Guidotti Down-regulation of neurosteroid biosynthesis in corticolimbic circuits mediates social isolation-induced behavior in mice Proc. Natl. Acad. Sci. U.S.A. 104 2007 18736 18741
93. R.C. Agis-Balboa, G. Pinna, A. Zhubi, E. Maloku, M. Veldic, E. Costa, and A. Guidotti Characterization of brain neurons that express enzymes mediating neurosteroid biosynthesis Proc. Natl. Acad. Sci. U.S.A. 103 2006 14602 14607
94. R. Berretti, F. Santoru, A. Locci, C. Sogliano, A. Calza, E. Choleris, P. Porcu, and A. Concas Neonatal exposure to estradiol decreases hypothalamic allopregnanolone concentrations and alters agonistic and sexual but not affective behavior in adult female rats Horm. Behav. 65 2014 142 153
95. K. Tsutsui, S. Haraguchi, Y. Fukada, and H. Vaudry Brain and pineal 7 alpha-hydroxypregnenolone stimulating locomotor activity: identification, mode of action and regulation of biosynthesis Front. Neuroendocrinol. 34 2013 179 189
96. D. Belelli, M.B. Herd, E.A. Mitchell, D.R. Peden, A.W. Vardy, L. Gentet, and J.J. Lambert Neuroactive steroids and inhibitory neurotransmission: mechanisms of action and physiological relevance Neuroscience 138 2006 821 829
97. S.H. Mellon, and L.D. Griffin Neurosteroids: biochemistry and clinical significance Trends Endocrinol. Metab. 13 2002 35 43
98. K.A. Miczek, J.F. DeBold, A.M. van Erp, and W. Tornatzky Alcohol, GABAA-benzodiazepine receptor complex, and aggression Recent Dev. Alcohol. 13 1997 139 171
99. F.P. Monnet, V. Mahe, P. Robel, and E.E. Baulieu Neurosteroids, via sigma receptors, modulate the H-3 norepinephrine release evoked by N-methyl-d-aspartate in the rat hippocampus Proc. Natl. Acad. Sci. U.S.A. 92 1995 3774 3778
100. V. Anagnostopoulou, I. Pediaditakis, S. Alkahtani, S.A. Alarifi, E.-M. Schmidt, F. Lang, A. Gravanis, I. Charalampopoulos, and C. Stournaras Differential effects of dehydroepiandrosterone and testosterone in prostate and colon cancer cell apoptosis: the role of nerve growth factor (NGF) receptors Endocrinology 154 2013 2446 2456
101. L. Lazaridis, L. Charalampopoulos, V.-I. Alexaki, N. Avlonitis, I. Pediaditakis, P. Efstathopoulos, T. Calogeropoulou, E. Castanas, and A. Gravanis Neurosteroid dehydroepiandrosterone interacts with nerve growth factor (NGF) receptors, preventing neuronal apoptosis PLoS Biol. 9 2011 e1001051
102. A. Rahmani, A. Shoae-Hassani, P. Keyhanvar, D. Kheradmand, and A. Darbandi-Azar Dehydroepiandrosterone stimulates nerve growth factor and brain derived neurotrophic factor in cortical neurons Adv. Pharmacol. Sci. 2013 2013 7
103. S. Luchetti, I. Huitinga, and D.F. Swaab Neurosteroid and GABA-A receptor alterations in Alzheimer's disease, Parkinson's disease and multiple sclerosis Neuroscience 191 2011 6 21
104. T. Kasahara, K. Abe, K. Mekada, A. Yoshiki, and T. Kato Genetic variation of melatonin productivity in laboratory mice under domestication Proc. Natl. Acad. Sci. U.S.A. 107 2010 6412 6417
105. A.M. Lorincz, M.B. Shoemaker, and P.D. Heideman Genetic variation in photoperiodism among naturally photoperiodic rat strains Am. J. Physiol. - Regul. Integr. Comp. Physiol. 281 2001 R1817 R1824
106. R.J. Nelson Photoperiodic responsiveness in house mice Physiol. Behav. 48 1990 403 408
107. S.M. Yellon, and L.T. Tran Photoperiod, reproduction, and immunity in select strains of inbred mice J. Biol. Rhythms 17 2002 65 75
108. B.D. Goldman Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement J. Biol. Rhythms 16 2001 283 301
109. J.W. Garrett, and C.S. Campbell Changes in social behavior of the male golden hamster accompanying photoperiodic changes in reproduction Horm. Behav. 14 1980 303 318
110. A.M. Jasnow, K.L. Huhman, T.J. Bartness, and G.E. Demas Short days and exogenous melatonin increase aggression of male Syrian hamsters (Mesocricetus auratus) Horm. Behav. 42 2002 13 20
111. H.K. Caldwell, and H.E. Albers Short-photoperiod exposure reduces vasopressin (V-1a) receptor binding but not arginine-vasopressin-induced flank marking in male Syrian hamsters J. Neuroendocrinol. 15 2003 971 977
112. S.J. Gutzler, M. Karom, W.D. Erwin, and H.E. Albers Seasonal regulation of social communication by photoperiod and testosterone: effects of arginine-vasopressin, serotonin and galanin in the medial preoptic area-anterior hypothalamus Behav. Brain Res. 216 2011 214 219
113. A.M. Jasnow, K.L. Huhman, T.J. Bartness, and G.E. Demas Short-day increases in aggression are inversely related to circulating testosterone concentrations in male Siberian hamsters (Phodopus sungorus) Horm. Behav. 38 2000 102 110
114. J.C. Wen, A.K. Hotchkiss, G.E. Demas, and R.J. Nelson Photoperiod affects neuronal nitric oxide synthase and aggressive behaviour in male Siberian hamsters (Phodopus sungorus) J. Neuroendocrinol. 16 2004 916 921
115. J.W. Jahng, J.H. Lee, G.T. Kim, Y.M. Kim, T.A. Houpt, and D.G. Kim Adrenalectomy abolishes fasting-induced down-regulation of NADPH-diaphorase in the rat paraventricular nucleus Yonsei Med. J. 45 2004 123 128
116. G.E. Demas, K.M. Polacek, A. Durazzo, and A.M. Jasnow Adrenal hormones mediate melatonin-induced increases in aggression in male Siberian hamsters (Phodopus sungorus) Horm. Behav. 46 2004 582 591
117. T.A. Bedrosian, L.K. Fonken, G.E. Demas, and R.J. Nelson Photoperiod-dependent effects of neuronal nitric oxide synthase inhibition on aggression in Siberian hamsters Horm. Behav. 61 2012 176 180
118. L.A. Ciaccio, R.D. Lisk, and L.A. Reuter Prelordotic behavior in the hamster: hormonally modulated transition from aggression to sexual receptivity J. Comp. Physiol. Psychol. 93 1979 771 780
119. D.M. Marques, and E.S. Valenstein Individual differences in aggressiveness of female hamsters: response to intact and castrated males and to females Anim. Behav. 25 1977 131 139
120. L.L. Badura, and A.A. Nunez Photoperiodic modulation of sexual and aggressive behavior in female golden hamsters (Mesocricetus-Auratus): role of the pineal gland Horm. Behav. 23 1989 27 42
121. A.S. Fleming, A. Phillips, A. Rydall, and L. Levesque Effects of photoperiod, the pineal gland and the gonads on agonistic behavior in female golden hamsters (Mesocricetus auratus) Physiol. Behav. 44 1988 227 234
122. J. Haller, G.B. Makara, and M.R. Kruk Catecholaminergic involvement in the control of aggression: hormones, the peripheral sympathetic, and central noradrenergic systems Neurosci. Biobehav. Rev. 22 1998 85 97
123. A.T. Paterson, and C. Vickers Melatonin and the adrenal-cortex relationship to territorial aggression in mice Physiol. Behav. 27 1981 983 987
124. P.F. Brain, and N.W. Nowell Some behavioral and endocrine relationships in adult male laboratory mice subjected to open field and aggression tests Physiol. Behav. 4 1969 945 947
125. E.W. Fish, J.F. DeBold, and K.A. Miczek Escalated aggression as a reward: corticosterone and GABAA receptor positive modulators in mice Psychopharmacology (Berlin) 182 2005 116 127
126. J. Haller, and M.R. Kruk Neuroendocrine stress responses and aggression M.P. Mattson, Neurobiology of Aggression: Understanding and Preventing Violence 2003 Humana Press Inc. Totowa, NJ 93 118
127. M.L. Schlegel, J.F. Spetz, P. Robel, and M. Haug Studies on the effects of dehydroepiandrosterone and its metabolites on attack by castrated mice on lactating intruders Physiol. Behav. 34 1985 867 870
128. C.J. Reburn, and K.E. Wynne-Edwards Hormonal changes in males of a naturally biparental and a uniparental mammal Horm. Behav. 35 1999 163 176
129. P.D. Kroboth, F.S. Salek, A.L. Pittenger, T.J. Fabian, and R.F. Frye DHEA and DHEA-S: a review J. Clin. Pharmacol. 39 1999 327 348
130. E. Haus, G.Y. Nicolau, E. Ghinea, L. Dumitriu, E. Petrescu, and L. Sackett Lundeen Stimulation of the secretion of dehydroepiandrosterone by melatonin in mouse adrenals in vitro Life Sci. 58 1996 PL263 PL267
131. K.S. Rehman, and B.R. Carr Sex differences in adrenal androgens Semin. Reprod. Med. 22 2004 349 360
132. W. Goymann On the use of non-invasive hormone research in uncontrolled, natural environments: the problem with sex, diet, metabolic rate and the individual Methods Ecol. Evol. 3 2012 757 765
133. J.W. Lynch, T.E. Ziegler, and K.B. Strier Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted Capuchin monkeys, Cebus apella nigritus Horm. Behav. 41 2002 275 287
134. J. Ostner, P.M. Kappeler, and M. Heistermann Seasonal variation and social correlates of androgen excretion in male redfronted lemurs (Eulemur fulvus rufus) Behav. Ecol. Sociobiol. 52 2002 485 495
135. R.M. Sapolsky, J.H. Vogelman, N. Orentreich, and J. Altmann Senescent decline in serum dehydroepiandrosterone-sulfate concentrations in a population of wild baboons J. Gerontol. 48 1993 B196 B200
136. N.D. Goncharova, V.Y. Marenin, and T.E. Oganyan Aging of the hypothalamic-pituitary-adrenal axis in nonhuman primates with depression-like and aggressive behavior Aging-Us 2 2010 854 866
137. K.G. Sorwell, S.G. Kohama, and H.F. Urbanski Perimenopausal regulation of steroidogenesis in the nonhuman primate Neurobiol. Aging 33 2012 1487.e1 1487.e13
138. K.G. Sorwell, and H.F. Urbanski Causes and consequences of age-related steroid hormone changes: insights gained from nonhuman primates J. Neuroendocrinol. 25 2013 1062 1069
139. N. Maninger, O.M. Wolkowitz, V.I. Reus, E.S. Epel, and S.H. Mellon Neurobiological and neuropsychiatric effects of dehydroepiandrosterone (DHEA) and DHEA sulfate (DHEAS) Front. Neuroendocrinol. 30 2009 65 91
140. F. Labrie, V. Luu-The, A. Belanger, S.X. Lin, J. Simard, G. Pelletier, and C. Labrie Is dehydroepiandrosterone a hormone? J. Endocrinol. 187 2005 169 196
141. D.H. Barzman, A. Patel, L. Sonnier, and J.R. Strawn Neuroendocrine aspects of pediatric aggression: can hormone measures be clinically useful? Neuropsychiatr. Dis. Treat. 6 2010 691 697
142. S.H.M. van Goozen, W. Matthys, P.T. Cohen-Kettenis, J.H.H. Thijssen, and H. van Engeland Adrenal androgens and aggression in conduct disorder prepubertal boys and normal controls Biol. Psychiatry 43 1998 156 158
143. J.N. Constantino, D. Grosz, P. Saenger, D.W. Chandler, R. Nandi, and F.J. Earls Testosterone and aggression in children J. Am. Acad. Child Adolesc. Psychiatry 32 1993 1217 1222
144. S.H.M. van Goozen, E. van den Ban, W. Matthys, P.T. Cohen-Kettenis, J.H.H. Thijssen, and H. van Engeland Increased adrenal androgen functioning in children with oppositional defiant disorder: a comparison with psychiatric and normal controls J. Am. Acad. Child Adolesc. Psychiatry 39 2000 1446 1451
145. D.H. Barzman, D. Mossman, K. Appel, T.J. Blom, J.R. Strawn, N.N. Ekhator, B. Patel, M.P. DelBello, M. Sorter, and D. Klein The association between salivary hormone levels and children's inpatient aggression: a pilot study Psychiatr. Q. 84 2013 475 484
146. P. Golubchik, T. Mozes, R. Maayan, and A. Weizman Neurosteroid blood levels in delinquent adolescent boys with conduct disorder Eur. Neuropsychopharmacol. 19 2009 49 52
147. S.A. Berenbaum, and S.M. Resnick Early androgen effects on aggression in children and adults with congenital adrenal hyperplasia Psychoneuroendocrinology 22 1997 505 515
148. K. Pajer, R. Tabbah, W. Gardner, R.T. Rubin, R.K. Czambel, and Y. Wang Adrenal androgen and gonadal hormone levels in adolescent girls with conduct disorder Psychoneuroendocrinology 31 2006 1245 1256
149. J.R. Sánchez-Martín, A.A. Imaz, E.F. Ardanaz, F.B. Lloret, J.M.M. Sánchez, and M.R.C. de Alba Niveles de andrógenos, estilos parentales y conducta agresiva en niños y niñas de 5-6 años de edad Psicothema 21 2009 57 62
150. V.A. Gavrilova, S.A. Ivanova, S.I. Gusev, M.V. Trofimova, and N.A. Bokhan Neurosteroids dehydroepiandrosterone and its sulfate in individuals with personality disorders convicted of serious violent crimes Bull. Exp. Biol. Med. 154 2012 89 91
151. G. Lac, F. Dutheil, G. Brousse, C. Triboulet-Kelly, and A. Chamoux Saliva DHEAS changes in patients suffering from psychopathological disorders arising from bullying at work Brain Cogn. 80 2012 277 281
152. D.S. Reddy Neurosteroids: endogenous role in the human brain and therapeutic potentials Prog. Brain Res. 186 2010 113
153. B. Stoffel-Wagner Neurosteroid metabolism in the human brain Eur. J. Endocrinol. 145 2001 669 679
154. R.J. Barfield Activation of sexual and aggressive behavior by androgen implanted into male ring dove brain Endocrinology 89 1971 1470 1477
155. D.A. Edwards Post-neonatal androgenization and adult aggressive behavior in female mice Physiol. Behav. 5 1970 465 466
156. J.C. Wingfield, G.F. Ball, A.M. Dufty, R.E. Hegner, and M. Ramenofsky Testosterone and aggression in birds Am. Sci. 75 1987 602 608