New knockout model confirms a role for androgen receptors in regulating anxiety-like behaviors and HPA response in mice

Hormones and Behavior

Volumn 65, Issue 3, 2014, Pages 211-218

  Chen, Chieh V ^a   Brummet, Jennifer L ^a   Lonstein, Joseph S ^a   Jordan, Cynthia L ^a   Breedlove, S Marc ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Androgen insensitivity; Androgen receptor; Anxiety; Corticosterone; Cre lox technology; HPA axis; Photoperiod; Testosterone

Indexed keywords

ANDROGEN RECEPTOR; TESTOSTERONE; CORTICOSTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; ELEVATED PLUS MAZE TEST; HORMONE ACTION; HYPOPHYSIS ADRENAL SYSTEM; KNOCKOUT MOUSE; MALE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN FUNCTION; WILD TYPE; ANDROGEN INSENSITIVITY SYNDROME; ANIMAL; ANIMAL BEHAVIOR; ANXIETY; BLOOD; C57BL MOUSE; DISEASE MODEL; FEMALE; GENETICS; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MENTAL STRESS; METABOLISM; PATHOPHYSIOLOGY; PHOTOPERIODICITY; PHYSIOLOGY;

ANDROGEN-INSENSITIVITY SYNDROME; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; CORTICOSTERONE; DISEASE MODELS, ANIMAL; FEMALE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, ANIMAL; PHOTOPERIOD; PITUITARY-ADRENAL SYSTEM; RECEPTORS, ANDROGEN; STRESS, PSYCHOLOGICAL; TESTOSTERONE;

EID: 84896873037     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2014.01.001     Document Type: Article

References (70)

1. Aikey J.L., Nyby J.G., Anmuth D.M., James P.J. Testosterone rapidly reduces anxiety in male house mice (Mus musculus). Horm. Behav. 2002, 42:448-460.
2. Almeida O.P., Waterreus A., Spry N., Flicker L., Martins R.N. One year follow-up study of the association between chemical castration, sex hormones, beta-amyloid, memory and depression in men. Psychoneuroendocrinology 2004, 29:1071-1081.
3. Amore M., Scarlatti F., Quarta A.L., Tagariello P. Partial androgen deficiency, depression and testosterone treatment in aging men. Aging Clin. Exp. Res. 2009, 21:1-8.
4. Bekker M.H., van Mens-Verhulst J. Anxiety disorders: sex differences in prevalence, degree, and background, but gender-neutral treatment. Gend. Med. 2007, 4(Suppl. B):S178-S193.
5. Bodo C., Rissman E.F. Androgen receptor is essential for sexual differentiation of responses to olfactory cues in mice. Eur. J. Neurosci. 2007, 25:2182-2190.
6. Charest N.J., Zhou Z.X., Lubahn D.B., Olsen K.L., Wilson E.M., French F.S. A frameshift mutation destabilizes androgen receptor messenger RNA in the Tfm mouse. Mol. Endocrinol. 1991, 5:573-581.
7. De Gendt K., Swinnen J.V., Saunders P.T., Schoonjans L., Dewerchin M., Devos A., Tan K., Atanassova N., Claessens F., Lecureuil C., Heyns W., Carmeliet P., Guillou F., Sharpe R.M., Verhoeven G. A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:1327-1332.
8. Dean C., Kendell R.E. The symptomatology of puerperal illnesses. Br. J. Psychiatry 1981, 139:128-133.
9. Decker D.A., Pettinga J.E., VanderVelde N., Huang R.R., Kestin L., Burdakin J.H. Estrogen replacement therapy in breast cancer survivors: a matched-controlled series. Menopause 2003, 10:277-285.
10. Demetrio F.N., Renno J., Gianfaldoni A., Goncalves M., Halbe H.W., Filho A.H.G.V., Gorenstein C. Effect of estrogen replacement therapy on symptoms of depression and anxiety in non-depressive menopausal women. Arch. Women Ment. Health 2011, 14:479-486.
11. Douma S.L., Husband C., O'Donnell M.E., Barwin B.N., Woodend A.K. Estrogen-related mood disorders: reproductive life cycle factors. ANS Adv. Nurs. Sci. 2005, 28:364-375.
12. Dugger B.N., Morris J.A., Jordan C.L., Breedlove S.M. Androgen receptors are required for full masculinization of the ventromedial hypothalamus (VMH) in rats. Horm. Behav. 2007, 51:195-201.
13. Durazzo A., Morris J.A., Breedlove S.M., Jordan C.L. Effects of the testicular feminization mutation (Tfm) of the androgen receptor gene on BSTMPM volume and morphology in rats. Neurosci. Lett. 2007, 419:168-171.
14. Edinger K.L., Frye C.A. Testosterone's analgesic, anxiolytic, and cognitive-enhancing effects may be due in part to actions of its 5 alpha-reduced metabolites in the hippocampus. Behav. Neurosci. 2004, 118:1352-1364.
15. Edinger K.L., Frye C.A. Intrahippocampal administration of an androgen receptor antagonist, flutamide, can increase anxiety-like behavior in intact and DHT-replaced male rats. Horm. Behav. 2006, 50:216-222.
16. Evuarherhe O., Leggett J.D., Waite E.J., Kershaw Y.M., Atkinson H.C., Lightman S.L. Organizational role for pubertal androgens on adult hypothalamic-pituitary-adrenal sensitivity to testosterone in the male rat. J. Physiol. (Lond.) 2009, 587:2977-2985.
17. Fernandez-Guasti A., Martinez-Mota L. Anxiolytic-like actions of testosterone in the burying behavior test: role of androgen and GABA-benzodiazepine receptors. Psychoneuroendocrinology 2005, 30:762-770.
18. Freeman E.W. Treatment of depression associated with the menstrual cycle: premenstrual dysphoria, postpartum depression, and the perimenopause. Dialogues Clin. Neurosci. 2002, 4:177-191.
19. Frye C.A. Steroids, reproductive endocrine function, and affect. A review. Minerva Ginecol. 2009, 61:541-562.
20. Frye C.A., Lacey E.H. Posttraining androgens' enhancement of cognitive performance is temporally distinct from androgens' increases in affective behavior. Cogn. Affect. Behav. Neurosci. 2001, 1:172-182.
21. Frye C.A., Edinger K., Sumida K. Androgen administration to aged male mice increases anti-anxiety behavior and enhances cognitive performance. Neuropsychopharm. 2008, 33:1049-1061.
22. Garcia-Falgueras A., Pinos H., Collado P., Pasaro E., Fernandez R., Jordan C.L., Segovia S., Guillamon A. The role of the androgen receptor in CNS masculinization. Brain Res. 2005, 1035:13-23.
23. Giltay E.J., Enter D., Zitman F.G., Penninx B.W.J.H., van Pelt J., Spinhoven P., Roelofs K. Salivary testosterone: associations with depression, anxiety disorders, and antidepressant use in a large cohort study. J. Psychosom. Res. 2012, 72:205-213.
24. Greenberg P.E., Sisitsky T., Kessler R.C., Finkelstein S.N., Berndt E.R., Davidson J.R., Ballenger J.C., Fyer A.J. The economic burden of anxiety disorders in the 1990s. J. Clin. Psychiatry 1999, 60:427-435.
25. Halberg F., Albrecht P.G., Bittner J.J. Corticosterone rhythm of mouse adrenal in relation to serum corticosterone and sampling. Am. J. Physiol. 1959, 197:1083-1085.
26. Handa R.J., Pak T.R., Kudwa A.E., Lund T.D., Hinds L. An alternate pathway for androgen regulation of brain function: activation of estrogen receptor beta by the metabolite of dihydrotestosterone, 5 alpha-androstane-3 beta,17 beta-diol. Horm. Behav. 2008, 53:741-752.
27. Hughes Z.A., Liu F., Platt B.J., Dwyer J.M., Pulicicchio C.M., Zhang G.M., Schechter L.E., Rosenzweig-Lipson S., Day M. WAY-200070, a selective agonist of estrogen receptor beta as a potential novel anxiolytic/antidepressant agent. Neuropharmacology 2008, 54:1136-1142.
28. Imwalle D.B., Gustafsson J.A., Rissman E.F. Lack of functional estrogen receptor beta influences anxiety behavior and serotonin content in female mice. Physiol. Behav. 2005, 84:157-163.
29. Jones B.A., Watson N.V. Spatial memory performance in androgen insensitive male rats. Physiol. Behav. 2005, 85:135-141.
30. Juntti S.A., Tollkuhn J., Wu M.V., Fraser E.J., Soderborg T., Tan S., Honda S., Harada N., Shah N.M. The androgen receptor governs the execution, but not programming, of male sexual and territorial behaviors. Neuron 2010, 66:260-272.
31. Karatsoreos I.N., Silver R. Minireview: the neuroendocrinology of the Suprachiasmatic nucleus as a conductor of body time in mammals. Endocrinology 2007, 148:5640-5647.
32. Kessler R.C., Chiu W.T., Demler O., Merikangas K.R., Walters E.E. Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Arch. Gen. Psychiatry 2005, 62:617-627.
33. Kiesner J. One woman's low is another woman's high: paradoxical effects of the menstrual cycle. Psychoneuroendocrinology 2011, 36:68-76.
34. Krezel W., Dupont S., Krust A., Chambon P., Chapman P.F. Increased anxiety and synaptic plasticity in estrogen receptor beta-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12278-12282.
35. Llaneza P., Garcia-Portilla M.P., Llaneza-Suarez D., Armott B., Perez-Lopez F.R. Depressive disorders and the menopause transition. Maturitas 2012, 71:120-130.
36. Lund T.D., Rovis T., Chung W.C.J., Handa R.J. Novel actions of estrogen receptor-beta on anxiety-related behaviors. Endocrinology 2005, 146:797-807.
37. Lydiard R.B. The role of GABA in anxiety disorders. J. Clin. Psychiatry 2003, 64:21-27.
38. Marcondes F.K., Miguel K.J., Melo L.L., Spadari-Bratfisch R.C. Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiol. Behav. 2001, 74:435-440.
39. McLean C.P., Asnaani A., Litz B.T., Hofmann S.G. Gender differences in anxiety disorders: prevalence, course of illness, comorbidity and burden of illness. J. Psychiatr. Res. 2011, 45:1027-1035.
40. Meaney M.J., Stewart J., Poulin P., Mcewen B.S. Sexual-differentiation of social play in rat pups is mediated by the neonatal androgen-receptor system. Neuroendocrinology 1983, 37:85-90.
41. Meng F.T., Ni R.J., Zhang Z., Zhao J., Liu Y.J., Zhou J.N. Inhibition of oestrogen biosynthesis induces mild anxiety in C57BL/6J ovariectomized female mice. Neurosci. Bull. 2011, 27:241-250.
42. Menger Y., Bettscheider M., Murgatroyd C., Spengler D. Sex differences in brain epigenetics. Epigenomics 2010, 2:807-821.
43. Morgan M.A., Pfaff D.W. Estrogen's effects on activity, anxiety, and fear in two mouse strains. Behavioural Brain Research 2002, 132:85-93.
44. Morris J.A., Jordan C.L., Dugger B.N., Breedlove S.M. Partial demasculinization of several brain regions in adult male (XY) rats with a dysfunctional androgen receptor gene. J. Comp. Neurol. 2005, 487:217-226.
45. Oliveira A.G., Coelho P.H., Guedes F.D., Mahecha G.A., Hess R.A., Oliveira C.A. 5alpha-Androstane-3beta,17beta-diol (3beta-diol), an estrogenic metabolite of 5alpha-dihydrotestosterone, is a potent modulator of estrogen receptor ERbeta expression in the ventral prostrate of adult rats. Steroids 2007, 72:914-922.
46. Olsen K.L., Whalen R.E. Hormonal-control of the development of sexual-behavior in androgen-insensitive (Tfm) rats. Physiol. Behav. 1981, 27:883-886.
47. Penatti C.A.A., Porter D.M., Henderson L.P. Chronic exposure to anabolic androgenic steroids alters neuronal function in the mammalian forebrain via androgen receptor- and estrogen receptor-mediated mechanisms. J. Neurosci. 2009, 29:12484-12496.
48. Rago L., Kiivet R.A., Harro J., Pold M. Behavioral-differences in an elevated plus-maze - correlation between anxiety and decreased number of GABA and benzodiazepine receptors in mouse cerebral-cortex. Naunyn Schmiedeberg's Arch. Pharmacol. 1988, 337:675-678.
49. Raskin K., de Gendt K., Duittoz A., Liere P., Verhoeven G., Tronche F., Mhaouty-Kodja S. Conditional inactivation of androgen receptor gene in the nervous system: effects on male behavioral and neuroendocrine responses. J. Neurosci. Off. J. Soc. Neurosci. 2009, 29:4461-4470.
50. Reynolds D.S. The value of genetic and pharmacological approaches to understanding the complexities of GABA(A) receptor subtype functions: the anxiolytic effects of benzodiazepines. Pharmacol. Biochem. Behav. 2008, 90:37-42.
51. Rizk A., Robertson J., Raber J. Behavioral performance of Tfm mice supports the beneficial role of androgen receptors in spatial learning and memory. Brain Res. 2005, 1034:132-138.
52. Rocha B.A., Fleischer R., Schaeffer J.M., Rohrer S.P., Hickey G.J. 17 beta-Estradiol-induced antidepressant-like effect in the Forced Swim Test is absent in estrogen receptor-beta knockout (BERKO) mice. Psychopharmacology (Berl) 2005, 179:637-643.
53. Shifren J.L., Braunstein G.D., Simon J.A., Casson P.R., Buster J.E., Redmond G.P., Burki R.E., Ginsburg E.S., Rosen R.C., Leiblum S.R., Caramelli K.E., Mazer N.A. Transdermal testosterone treatment in women with impaired sexual function after oophorectomy. N. Engl. J. Med. 2000, 343:682-688.
54. Sternbach H. Age-associated testosterone decline in men: clinical issues for psychiatry. Am. J. Psychiatry 1998, 155:1310-1318.
55. Sullivan S.D., Moenter S.M. Prenatal androgens alter GABAergic drive to gonadotropin-releasing hormone neurons: implications for a common fertility disorder. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:7129-7134.
56. Tangen T., Mykletun A. Depression and anxiety through the climacteric period: an epidemiological study (HUNT-II). J. Psychosom. Obstet. Gynaecol. 2008, 29:125-131.
57. Thomson J., Oswald I. Effect of oestrogen on the sleep, mood, and anxiety of menopausal women. Br. Med. J. 1977, 2:1317-1319.
58. Walf A.A., Frye C.A. ERbeta-selective estrogen receptor modulators produce antianxiety behavior when administered systemically to ovariectomized rats. Neuropsychopharm. 2005, 30:1598-1609.
59. Walf A.A., Frye C.A. Estradiol reduces anxiety- and depression-like behavior of aged female mice. Physiol. Behav. 2010, 99:169-174.
60. Walf A.A., Koonce C.J., Frye C.A. Estradiol or diarylpropionitrile decrease anxiety-like behavior of wildtype, but not estrogen receptor beta knockout, mice. Behav. Neurosci. 2008, 122:974-981.
61. Walf A.A., Koonce C., Manley K., Frye C.A. Proestrous compared to diestrous wildtype, but not estrogen receptor beta knockout, mice have better performance in the spontaneous alternation and object recognition tasks and reduced anxiety-like behavior in the elevated plus and mirror maze. Behav. Brain Res. 2009, 196:254-260.
62. Wang C., Alexander G., Berman N., Salehian B., Davidson T., McDonald V., Steiner B., Hull L., Callegari C., Swerdloff R.S. Testosterone replacement therapy improves mood in hypogonadal men - a clinical research center study. J. Clin. Endocrinol. Metab. 1996, 81:3578-3583.
63. Wu M.V., Shah N.M. Control of masculinization of the brain and behavior. Curr. Opin. Neurobiol. 2011, 21:116-123.
64. Yazici K., Pata O., Yazici A., Aktas A., Tot S., Kanik A. The effects of hormone replacement therapy in menopause on symptoms of anxiety and depression. Turk. J. Psychiatry 2003, 14:101-105.
65. Zahn-Waxler C., Shirtcliff E.A., Marceau K. Disorders of childhood and adolescence: gender and psychopathology. Annu. Rev. Clin. Psychol. 2008, 4:275-303.
66. Zhou L., Blaustein J.D., Devries G.J. Distribution of androgen receptor immunoreactivity in vasopressin-immunoreactive and oxytocin-immunoreactive neurons in the male-rat brain. Endocrinology 1994, 134:2622-2627.
67. Zuloaga D.G., Morris J.A., Jordan C.L., Breedlove S.M. Mice with the testicular feminization mutation demonstrate a role for androgen receptors in the regulation of anxiety-related behaviors and the hypothalamic-pituitary-adrenal axis. Horm. Behav. 2008, 54:758-766.
68. Zuloaga D.G., Puts D.A., Jordan C.L., Breedlove S.M. The role of androgen receptors in the masculinization of brain and behavior: what we've learned from the testicular feminization mutation. Horm. Behav. 2008, 53:613-626.
69. Zuloaga D.G., Carbone D.L., Hiroi R., Chong D.L., Handa R.J. Dexamethasone induces apoptosis in the developing rat amygdala in an age-, region-, and sex-specific manner. Neuroscience 2011, 199:535-547.
70. Zuloaga D.G., Poort J.E., Jordan C.L., Breedlove S.M. Male rats with the testicular feminization mutation of the androgen receptor display elevated anxiety-related behavior and corticosterone response to mild stress. Horm. Behav. 2011, 60:380-388.