Gender differences in animal models of posttraumatic stress disorder

Disease Markers

Volumn 30, Issue 2-3, 2011, Pages 141-150

  Cohen, Hagit ^a   Yehuda, Rachel ^b  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

animal model; corticosterone; estrogen; HPA Axis; Post traumatic stress disorder; resilience; sympathoadrenal system; vulnerability

Indexed keywords

AMITRIPTYLINE; ANDROGEN; CORTICOSTERONE; CORTICOTROPIN; ESTROGEN; NORTRIPTYLINE;

ACUTE STRESS; ADRENERGIC SYSTEM; ANIMAL BEHAVIOR; ANXIETY DISORDER; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CHRONIC STRESS; CIRCADIAN RHYTHM; COPING BEHAVIOR; CORTICOSTERONE BLOOD LEVEL; DRUG METABOLISM; HYPOPHYSIS ADRENAL SYSTEM; MENTAL STRESS; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; SEX DIFFERENCE; SIGNAL TRANSDUCTION; TRANQUILIZING ACTIVITY;

ANIMALIA;

EID: 79955105576     PISSN: 02780240     EISSN: 18758630     Source Type: Journal    
DOI: 10.3233/DMA-2011-0778     Document Type: Article

References (97)

1. M. Olff, W. Langeland, N. Draijer and B. Gersons, Gender differences in posttraumatic stress disorder, Psychol Bull 133 (2007), 183-204.
2. L. Pratchett, M. Pelcovitz and R. Yehuda, Trauma and Violence: Are Women The Weaker Sex? Psychiatric Clinics of North America 33 (2010), 465-474.
3. N. Breslau, H.D. Chilcoat, R.C. Kessler, E.L. Peterson and V.C. Lucia, Vulnerability to assaultive violence: further specification ofthe sex difference in post-traumatic stress disorder, Psychol Med29 (1999), 813-821. (Pubitemid 29381041)
4. R.W. Robin, B. Chester, J.K. Rasmussen, J.M. Jaranson andD. Goldman, Prevalence and characteristics of trauma and post-traumatic stress disorder in a southwestern American Indian community, Am J Psychiatry 154 (1997), 1582-1588. (Pubitemid 27471353)
5. C.R. Brewin, B. Andrews and J.D. Valentine, Meta-analysis of risk factors for posttraumatic stress disorder in trauma-exposed adults, J Consult Clin Psychol 68 (2000), 748-766.
6. S.A. Freedman, N. Gluck, R. Tuval-Mashiach, D. Brandes, T. Peri and A.Y. Shalev, Gender differences in responses to traumatic events: a prospective study, J Trauma Stress 15 (2002), 407-413.
7. A. Yasan, G. Saka, M. Ozkan and M. Ertem, Trauma type, gender, and risk ofPTSD in a region within an area ofconflict, J Trauma Stress 22 (2009), 663-666.
8. R.C. Kessler, A. Sonnega, E. Bromet, M. Hughes and CB. Nelson, Posttraumatic stress disorder in the National Comor-bidity Survey, Arch Gen Psychiatry 52 (1995), 1048-1060.
9. M. Stein, J. Walker and D. Forde, Gender differences in sus-ceptibility to posttraumatic stress disorder, Behav Res Ther38 (2000), 619-628. (Pubitemid 30151123)
10. B. Freidenberg, R. Gusmano, E. Hickling, E. Blanchard, J. Bremner and C. Frye, Women with PTSD have lower basal salivary levels later in the day than do men with PTSD: a preliminary study, Physiol Behav 99 (2010), 234-236.
11. V. Carrion, C. Weems, R. Ray, B. Glaser, D. Hessl and A. Reiss, Diurnal salivary cortisol in pediatric posttraumatic stress disorder, Biol Psychiatry 51 (2002), 575-582. (Pubitemid 34327332)
12. L. Hawk, A. Dougall, R. Ursano and A. Baum, Urinary cate-cholamines and recent-onset posttraumatic stress disorder af-ter motor vehicle accidents, Psychosom Med 62 (2000), 423-434. (Pubitemid 30347086)
13. M. De Bellis, M. Keshavan, D. Clark, B. Casey, J. Giedd, A. Boring, K. Frustaci and N. Ryan, A.E. Bennett Research Award. Developmental traumatology Part II: Brain develop-ment, Biol Psychiatry 45 (1999), 1271-1284.
14. M. De Bellis and M. Kehavan, Sex differences in brain mat-uration in maltreatment-related pediatric posttraumatic stress disorder, Neurosci Biobehav Rev 27 (2003), 103-117. (Pubitemid 36535393)
15. K. Felmingham, L. Williams, A. Kemp, B. Liddell, E. Falcon-er, A. Peduto and R. Bryant, Neural responses to masked fear faces: sex differences and trauma exposure in posttraumatic stress disorder, JAbnormal Psychol 119 (2010), 241-247.
16. A. Iwasaki-Sekin, A. Mano-Otagiri, H. Ohata, N. Yamauchi and T. Shibasaki, Gender differences in corticotrophin and cor-ticosterone secretion and corticotrophin-releasing factor mR-NA expression in the paraventricular nucleus of the hypotha-lamus and the central nucleus of the amygdale in response to footshock stress or psychological stress in rats, Psychoen-docrinology 34 (2009), 226-237.
17. V. Viau, B. Bingham, J. Davis, P. Lee and M. Wong, Gender and puberty interact on the stress-induced activation of parvo-cellular neurosecretory neurons and corticotrophin-releasing hormone mRMA expression in the rat, Endoctinology 146 (2005), 137-146. (Pubitemid 40051733)
18. M. Weinstock, M. Razin, D. Schorer-Apelbaum, D. Men and R. McCarty, Gender differences in sympathoadrenal activity in rats at rest and in response to footshock stress, Int J Dev Neurosci 16 (1998), 289-295. (Pubitemid 28427094)
19. B. Asia, R. Tordera, B. Lashers, J. Del Rio and R.M.J, Effects of maternal separation on hypothalamic-pituitary-adrenal re-sponses, cognition and vulnerability to stress in adult female rats, Neuroscience 154(2008), 1218-1226.
20. V. Luine, Sex differences in chronic stress effects on memory in rats, Stress 5 (2002), 205-216.
21. V. Critchlow, R.A. Liebelt, M. Bar-Sela, W. Mountcastle and H.S. Lipscomb, Sex difference in resting pituitary-adrenal function in the rat, Am JPhysiol 205 (1963), 807-815.
22. J.I. Kitay, Sex differences in adrenal cortical secretion in the rat, Endocrinol 68 (1961), 818-824.
23. L.H. Burgess and R.J. Handa, Chronic estrogen-induced al-terations in adrenocorticotropin and corticosterone secretion, and glucocorticoid receptor-mediated functions in female rats, Endocrinology 131 (1992), 1261-1269.
24. R.J. Handa, L.H. Burgess, J.E. Kerr and J.A. O'Keefe, Go-nadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis, Horm Behav 28 (1994), 464-476.
25. P. Palanza, Animal models of anxiety and depression: how are females different? Neurosci Biobehav Rev 25 (2001), 219-233. (Pubitemid 32506875)
26. M. Weinstock, Gender differences in the effects of prenatal stress on brain development and behaviour, Neurochem Res 32 (2007), 1730-1740. (Pubitemid 47428852)
27. R. Gorski, J. Gordon, J. Shryne and A. Southam, Evidence for a morphological sex difference within the medial preoptic area ofthe rat brain, Brain Res Bull 148 (1978), 333-346. (Pubitemid 8341403)
28. L.W. Christensen, D.M. Nance and G.R.A., Effects of hy-pothalamic and preoptic lesions on reproductive behavior in male rats, Brain Research Bulletin 2 (1977), 137-141. (Pubitemid 8109318)
29. E. Davis, P. Popper and R. Gorski, The role of apoptosis in sexual differentiation ofthe rat sexually dimorphic nucleus of the preoptic area, Brain Res Bull734 (1996), 10-18. (Pubitemid 26334024)
30. M. Diamond, R. Johnson, D. Young and S. Singh, Age-related morphologic differences in the rat cerebral cortex and hip-pocampus: male-female; right-left, Exp Neurol 81 (1983), 1-13. (Pubitemid 13025731)
31. D. Fleming, R. Anderson, R. Rhees, E. Kinghorn and J. Bakaitis, Effects of prenatal stress on sexually dimorphic asymmetries in the cerebral cortex of the male rat, Brain Res Bull 16 (1986), 395-398. (Pubitemid 16071498)
32. H.E. Jones, M.A. Ruscio, L.A. Keyser, C. Gonzalez, B. Bil-lack, R. Rowe, C. Hancock, K.G. Lambert and CH. Kinsley, Prenatal stress alters the size ofthe rostral anterior commissure in rats, Brain Res Bull 42 (1997), 341-346. (Pubitemid 27161551)
33. C. Isgor and D.R. Sengelaub, Prenatal gonadal steroids affect adult spatial behavior, CA1 and CA3 pyramidal cell morphology in rats, Hormones andBehavior 34 (1998), 183-198. (Pubitemid 28541759)
34. R.D. Romeo, E.M. Waters and B.S. McEwen, Steroid-induced hippocampal synaptic plasticity: sex differences and similarities, Neuron Glia Biol 1 (2004), 219-229.
35. N.M. Conejo, H. Gonzalez-Pardo, C. Pedraza, F.F. Navarro, G. Vallejo and J.L. Arias, Evidence for sexual difference in astrocytes of adult rat hippocampus, Neurosci Lett 339 (2003), 119-122. (Pubitemid 36258369)
36. J.A. Markham, K.P. McKian, T.S. Stroup and J.M. Juraska, Sexually dimorphic aging ofdendritic morphology in CA1 of hippocampus, Hippocampus 15 (2005), 97-103. (Pubitemid 40340245)
37. E. Gould, A. Westlind-Danielsson, M. Frankfurt and B.S. McEwen, Sex differences and thyroid hormone sensitivity of hippocampal pyramidal cells, Journal ofNeuroscience 10 (1990), 996-1003. (Pubitemid 20104795)
38. R.L. Roof, The dentate gyrus is sexually dimorphic in prepubescent rats: testosterone plays a significant role, Brain Research Bulletin 610 (1993), 148-151. (Pubitemid 23144435)
39. G. Tabibnia, B.M. Cooke and S.M. Breedlove, Sex difference and laterality in the volume of mouse dentate gyrus granule cell layer, Brain Research 827 (1999), 41-45. (Pubitemid 29222902)
40. A. Parducz and L.M. Garcia-Segura, Sexual differences in the synaptic connectivity in the rat dentate gyrus, Neuroscience Letters 161 (1993), 53-56. (Pubitemid 23311063)
41. J.P Andrade, M.D. Madeira and M.M. Paula-Barbosa, Sexual dimorphism in the subiculum of the rat hippocampal formation, Brain Research 875 (2000), 125-137.
42. T. J. Shors, C. Chua and J. Falduto, Sex differences and opposite effects ofstress on dendritic spine density inthe male versus female hippocampus, Journal ofNeuroscience 21 (2001), 6292-6297. (Pubitemid 32737760)
43. C. Woolley and B. McEwen, Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat, JNeurosci 12 (1992), 2549-2554.
44. E. Gould, C. Woolley, M. Frankfurt and B. McEwen, Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood, JNeurosci 10 (1990), 1286-1291.
45. C. Li, W. Brake, R. Romeo, J. Dunlop, M. Gordon, R. Buzescu, A. Magarinos, P. Allen, P. Greengard, V. Luine and B. McEwen, Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory infemale mice, Proc Natl Acad Sci USA 101 (2004), 2185-2190. (Pubitemid 38229036)
46. N. Mac Lusky, V. Luine, T. Hajszan and C. Leranth, The 17alpha and 17beta isomers of estradiol both induce rapid spine synapse formation in the CA1 hippocampal subfield of ovariectomized female rats, Endocrinology 146 (2005), 287-293. (Pubitemid 40051751)
47. C. Smith and L. McMahon, Estrogen-induced increase in the magnitude of long-term potentiation occurs only when the ratio ofNMDAtransmissionto AMPAtransmission is increased, JNeurosci 25 (2005), 7780-7791. (Pubitemid 41208649)
48. C. Woolley, H. Wenzel and P. Schwartzkroin, Estradiol increases the frequency of multiple synapse boutons in the hippocampal CA1 region ofthe adult female rat, J Comp Neurol 373(1996), 108-117. (Pubitemid 26292122)
49. M. Yankova, S. Hart and C. Woolley, From the cover: estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: a serial electronmicroscopic study, Proc Natl Acad Sci USA 98 (2001), 3525-32530.
50. E.A. Nimchinsky, B.L. Sabatini and K. Svoboda, Structure and function ofdendritic spines, Annual Review ofPhysiology 64 (2002), 313-353.
51. B. McEwen, Estrogen actions throughout the brain, Recent Prog Horm Res 57 (2002), 357-384.
52. C. Leranth, O. Petnehazy and N.J. Mac Lusky, Gonadal hor-mones affect spine synaptic density in the CA1 hippocam-pal subfield of male rats, Journal ofNeuroscience 23 (2003), 1588-1592. (Pubitemid 36314713)
53. C. Lewis, B.S. McEwen and M. Frankfurt, Estrogen-induction of dendritic spines in ventromedial hypothalamus and hip-pocampus: effects ofneonatal aromatase blockade and adult GDX, Developmental Brain Research 87 (1995), 91-95.
54. J.M. Daniel and G.P Dohanich, Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 ofthe hippocampus and the associated improvement in work-ing memory, Journal ofNeuroscience 21 (2001), 6949-6956. (Pubitemid 32781137)
55. N. Weiland, Estradiol selectively regulates agonist binding sites on the N-methyl-D-aspartate receptor complex in the CA1 region ofthe hippocampus, Endocrinology 131 (1992), 662-668.
56. CS. Woolley and B.S. McEwen, Estradiol regulates hip-pocampal dendritic spine density via an N-methyl-D-aspartate receptordependent mechanism, Journal ofNeuroscience 14 (1994), 7680-7687.
57. B.S. McEwen and R.E. Brinton, Neuroendocrine aspects of adaptation, Prog. Brain Res 72 (1987), 11-26.
58. A. Mazor, M.A. Matar, Z. Kaplan, N. Kozlovsky, J. Zohar and H. Cohen, Gender-related qualitative differences in baseline and post-stress anxiety responses are not reflected in the inci-dence of criterion-based PTSD-like behaviour patterns, World JBiol Psychiatry 10 (2009), 856-869.
59. H. Louvart, S. Maccari, J. Lesage, M. Leonhardt, A. Dickes-Coopman and M. Darnaudéry, Effects of a single footshock followed by situational reminders on HPA axis and behaviour in the aversive context in male and female rats, Psychoneu-roendocrinology 31 (2006), 92-99. (Pubitemid 41668897)
60. D.D. Rasmussen, NJ. Crites and B.L. Burke, Acoustic star-tle amplitude predicts vulnerability to develop post-traumatic stress hyper-responsivity and associated plasma corticosterone changes in rats, Psychoneuroendocrinology 33 (2008), 282-291.
61. V. Viau and MJ. Meaney, Testosterone-dependent variations in plasma and intrapituitary corticosteroid binding globulin and stress hypothalamic- pituitary-adrenal activity in the male rat, J Endocrinol 181 (2004), 223-231. (Pubitemid 38744672)
62. J. Le Mevel, S. Abitbol, G. Beraud and J. Maniey, Temporal changes in plasma adrenocorticotropin concentration after re-peated neurotropic stress in male and female rats, Endocrinol-ogy 105 (1979), 812-817. (Pubitemid 9257476)
63. A.L. Herbst, F.E. Yates, D.W. Glenister and J. Urquhart, Vari-ations in hepatic inactivation of corticosterone with changes in food intake: an explanation of impaired corticosteroid metabolism following noxious stimuli, Endocrinology 67 (1960), 222-238.
64. A. A. Hagen and R.C. Troop, Influence of age, sex and adreno-cortical status on hepatic reduction of cortisone in vitro, En-docrinology 67 (1960), 194-203.
65. R.C. Troop, Influence of gonadal hormones onthe metabolism ofcortisone, Endocrinology 64 (1959), 671-675.
66. J. Urquhart, F.E. Yates and A.L. Herbst, Hepatic regulation of adrenal cortical function, Endocrinology 64 (1959), 816-830.
67. C. Rivier, Gender, sex steroids, corticotrophin-releasing factor, and HPA response to stress, Biochem Behv (1999), 739-751.
68. CA. Gemzell, [Increase in the formation and the secre-tion of ACTH in rats following administration of oestradiol-monobenzoate.], Acta Endocrinol (Copenh) 11 (1952), 221-228.
69. D. Gompertz, The effect ofsex hormones on the adrenal gland ofthe male rat, JEndocrinol 17 (1958), 107-113.
70. L.H. Burgess and RJ. Handa, Hormonal regulation of andro-gen receptor mRNA in the brain and anterior pituitary gland ofthe male rat, Brain Res Mol Brain Res 19 (1993), 31-38.
71. M.P. Carey, CH. Deterd, J. de Koning, F. Helmerhorst and E.R. de Kloet, The influence of ovarian steroids on hypothalamic-pituitary-adrenal regulation inthe female rat, J. Endocrinol 144 (1995), 311-321.
72. A. Peiffer and N. Barden, Estrogen-induced decrease of glu-cocorticoid receptor messenger ribonucleic acid concentration in rat anterior pituitary gland, Mol Endocrinol 1 (1987), 435-440. (Pubitemid 17165982)
73. B.B. Turner, Sex difference in glucocorticoid binding in rat pituitary is estrogen dependent, Life Sci 46(1990), 1399-1406. (Pubitemid 20169724)
74. V.K. Patchev, S. Hayashi, C. Orikasa and O.F. Almeida, Im-plications of estrogen-dependent brain organization for gen-der differences in hypothalamo-pituitary-adrenal regulation, FASEBJ9(1995), 419-423.
75. MJ. Weiser and RJ. Handa, Estrogen impairs glucocorticoid dependent negative feedback on the hypothalamic-pituitary-adrenal axis via estrogen receptor alpha within the hypothala-mus, Neuroscience 159 (2009), 883-895.
76. V.K. Patchev and O.F. Almeida, Gender specificity in the neu-ral regulation ofthe response to stress: new leads from classi-cal paradigms, Mol Neurobiol 16 (1998), 63-77. (Pubitemid 28372725)
77. CM. McCormick, W. Linkroum, BJ. Sallinen and N.W. Miller, Peripheral and central sex steroids have differential ef-fects on the HPA axis of male and female rats, Stress 5 (2002), 235-247. (Pubitemid 36019509)
78. M. Baum, Activational and organizational effects ofestradiol on male behavioral neuroendocrine function, Scand JPsychol 44 (2003), 213-220. (Pubitemid 37256449)
79. B. McEwen, Steroid hormones: effect on brain development and function, Horm Res 37 (1992), 1-10.
80. J.H. Gaskin and J.I. Kitay, Hypothalamic and pituitary regu-lation of adrenocortical function inthe hamster: effects of go-nadectomy and gonadal hormone replacement, Endocrinology 89 (1971), 1047-1053.
81. RJ. Handa, K.M. Nunley, S.A. Lorens, J.P Louie, R.F. Mc-Givern and M.R. Bollnow, Androgen regulation of adrenocor-ticotropin and corticosterone secretion in the male rat follow-ing novelty and foot shock stressors, Physiol Behav 55 (1994), 117-124.
82. E.W. Bingaman, DJ. Magnuson, T.S. Gray and RJ. Handa, Androgen inhibits the increases in hypothalamic corticotropin-releasing hormone (CRH) and CRH-immunoreactivity follow-ing gonadectomy, Neuroendocrinology 59 (1994), 228-234. (Pubitemid 24053258)
83. Y. Lin, C. Wesrenbroek, P. Bakker, J. Termeer, A. Liu, X. Li and G. Ter Horst, Effects of long-term stress and recovery on the prefrontal cortex and dentate gyrus in male and female rats, Cerebral Cortex 18 (2008), 2762-2774.
84. R.M. Shansky, G. Bender and A. F. Arnsten, Estrogen prevents norepinephrine alpha-2a receptor reversal of stress-induced working memory impairment, Stress 12 (2009), 457-463.
85. T. Poltyrev and M. Weinstock, Genderdifferenceinthepreven-tion ofhyperanxiety in adult prenatally stressed rats by chron-ic treatment with amitriptyline, Psychopharmacology (Berl) 171 (2004), 270-276. (Pubitemid 38200065)
86. Y. Masubuchi, T. Iwasa, S. Fujita, T. Suzuki, T. Horie and S. Narimatsu, Regioselectivity and substrate concentration-dependency of involvement ofthe CYP2D subfamily in oxida-tive metabolism of amitriptyline and nortriptyline in rat liver microsomes, JPharm Pharmacol 48 (1996), 925-929. (Pubitemid 26364895)
87. H. Cohen, Z. Joseph and M. Matar, The relevance of differen-tial response to trauma in an animal model of post-traumatic stress disorder, Biol Psychiatry 53 (2003), 463-473. (Pubitemid 36331885)
88. H. Cohen and J. Zohar, Animal models ofpost traumatic stress disorder: The use of cut off behavioral criteria, The Annals New-York Academy ofSciences 1032 (2004), 167-178. (Pubitemid 40298469)
89. H. Cohen, J. Zohar, M.A. Matar, Z. Kaplan and A.B. Ge-va, Unsupervised fuzzy clustering analysis supports behav-ioral cutoff criteria in an animal model ofposttraumatic stress disorder, Biol Psychiatry 58 (2005), 640-650. (Pubitemid 41565579)
90. H. Cohen, J. Zohar, M.A. Matar, K. Zeev, U. Loewenthal and G. Richter-Levin, Setting apart the affected: the use of behavioral criteria in animal models of post traumatic stress disorder, Neuropsychopharmacology 29 (2004), 1962-1970. (Pubitemid 39486547)
91. R. Andrew, D.I. Phillips and B.R. Walker, Obesity and gender influence cortisol secretion and metabolism in man, J Clin Endocrinol Metab 83 (1998), 1806-1809. (Pubitemid 28501063)
92. M. Balbo, R. Leproult and E. Van Cauter, Impact of sleep and its disturbances on hypothalamo-pituitary-adrenal axis activi-ty, Int J Endocrinol 2010 (2010), 759234.
93. T. Smeets, I. Dziobek and O.T. Wolf, Social cognition under stress: differential effects ofstress-induced cortisol elevations in healthy young men and women, Horm Behav 55 (2009), 507-513.
94. N. Takai, M. Yamaguchi, T. Aragaki, K. Eto, K. Uchihashi and Y. Nishikawa, Gender-specific differences in salivary biomarker responses to acute psychological stress, Ann N Y Acad Sci 1098 (2007), 510-515. (Pubitemid 47092535)
95. H. Vierhapper, P. Nowotny and W. Waldhausl, Sex-specific differences in cortisol production rates in humans, Metabolism 47 (1998), 974-976. (Pubitemid 28364616)
96. R. Yehuda, A. McFarlane and A. Shalev, Predicting the de-velopment of posttraumatic stress disorder from the acute re-sponse to a traumatic event, Biological Psychiatry 44 (1998), 1305-1313. (Pubitemid 29015868)
97. R. Yehuda, J. Flory, L. Pratchett, J. Buxbaum, M. Ising and F. Holsboer, Putative Biological Mechanisms for the Associ-ation between Early Life Adversity and the Subsequent De-velopment ofPTSD, Psychopharmacology (Berl) 212 (2010), 405-417.