Suprachiasmatic nucleus as the site of androgen action on circadian rhythms

Hormones and Behavior

Volumn 73, Issue , 2015, Pages 1-7

  Model, Zina ^a   Butler, Matthew P ^b   LeSauter, Joseph ^a,b   Silver, Rae ^a,b,c  

^a Program on US Russia Relations at Columbia s Harriman Institute   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c NewYork Presbyterian Hospital   (United States)

Author keywords

Androgen receptor; Brain clock; Free running period; Hypothalamus; Light; Locomotor activity; Sex difference; Sex steroid; Testosterone

Indexed keywords

ANDROGEN RECEPTOR; TESTOSTERONE PROPIONATE; ANDROGEN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CIRCADIAN RHYTHM; CONTROLLED STUDY; GONADECTOMY; HORMONE ACTION; HYPOTHALAMUS; LOCOMOTION; MALE; MAMMILLARY BODY; MOUSE; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RUNNING; STRIA TERMINALIS; SUPRACHIASMATIC NUCLEUS; ANIMAL; BRAIN; C57BL MOUSE; DRUG EFFECTS; METABOLISM; MOTOR ACTIVITY; ORCHIECTOMY; PHYSIOLOGY;

ANDROGENS; ANIMALS; BRAIN; CIRCADIAN RHYTHM; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; ORCHIECTOMY; RECEPTORS, ANDROGEN; RUNNING; SUPRACHIASMATIC NUCLEUS;

EID: 84930633813     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2015.05.007     Document Type: Article

References (56)

1. Aschoff J. Exogenous and endogenous components in circadian rhythms. Cold Spring Harb. Symp. Quant. Biol. 1960, 25:11-28.
2. Blattner M.S., Mahoney M.M. Circadian parameters are altered in two strains of mice with transgenic modifications of estrogen receptor subtype 1. Genes Brain Behav. 2012, 11:828-836.
3. Brockman R., Bunick D., Mahoney M.M. Estradiol deficiency during development modulates the expression of circadian and daily rhythms in male and female aromatase knockout mice. Horm. Behav. 2011, 60:439-447.
4. Butler M.P., Silver R. Divergent photic thresholds in the non-image-forming visual system: entrainment, masking and pupillary light reflex. Proc. Roy. Soc. B 2011, 278:745-750.
5. Butler M.P., Karatsoreos I.N., LeSauter J., Silver R. Dose-dependent effects of androgens on the circadian timing system and its response to light. Endocrinology 2012, 153:2344-2352.
6. Cain S.W., Dennison C.F., Zeitzer J.M., Guzik A.M., Khalsa S.B., Santhi N., Schoen M.W., Czeisler C.A., Duffy J.F. Sex differences in phase angle of entrainment and melatonin amplitude in humans. J. Biol. Rhythms 2010, 25:288-296.
7. Daan S., Damassa D., Pittendrigh C.S., Smith E.R. An effect of castration and testosterone replacement on a circadian pacemaker in mice (Mus musculus). Proc. Natl. Acad. Sci. U. S. A. 1975, 72:3744-3747.
8. Dart D.A., Waxman J., Aboagye E.O., Bevan C.L. Visualising androgen receptor activity in male and female mice. PLoS One 2013, 8:e71694.
9. Davis F.C., Darrow J.M., Menaker M. Sex differences in the circadian control of hamster wheel-running activity. Am. J. Physiol. 1983, 244:R93-R105.
10. De Vries G.J. Minireview: sex differences in adult and developing brains: compensation, compensation, compensation. Endocrinology 2004, 145:1063-1068.
11. Duffy J.F., Cain S.W., Chang A.M., Phillips A.J., Munch M.Y., Gronfier C., Wyatt J.K., Dijk D.J., Wright K.P., Czeisler C.A. Sex difference in the near-24-hour intrinsic period of the human circadian timing system. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(Suppl. 3):15602-15608.
12. Empson J.A., Purdie D.W. Effects of sex steroids on sleep. Ann. Med. 1999, 31:141-145.
13. Eskes G.A., Zucker I. Photoperiodic regulation of the hamster testis: dependence on circadian rhythms. Proc. Natl. Acad. Sci. U. S. A. 1978, 75:1034-1038.
14. Fernandez-Guasti A., Kruijver F.P., Fodor M., Swaab D.F. Sex differences in the distribution of androgen receptors in the human hypothalamus. J. Comp. Neurol. 2000, 425:422-435.
15. Franklin K., Paxinos G. The Mouse Brain in Stereotaxic Coordinates 1997, Academic Press, San Diego.
16. Gattermann R., Johnston R.E., Yigit N., Fritzsche P., Larimer S., Ozkurt S., Neumann K., Song Z., Colak E., Johnston J., McPhee M.E. Golden hamsters are nocturnal in captivity but diurnal in nature. Biol. Lett. 2008, 4:253-255.
17. Hagenauer M.H., Lee T.M. Time for testosterone: the suprachiasmatic nucleus gets sexy. Endocrinology 2011, 152:1727-1730.
18. Hagenauer M.H., King A.F., Possidente B., McGinnis M.Y., Lumia A.R., Peckham E.M., Lee T.M. Changes in circadian rhythms during puberty in Rattus norvegicus: developmental time course and gonadal dependency. Horm. Behav. 2011, 60:46-57.
19. Hagenauer M.H., Ku J.H., Lee T.M. Chronotype changes during puberty depend on gonadal hormones in the slow-developing rodent, Octodon degus. Horm. Behav. 2011, 60:37-45.
20. 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, 5alpha-androstane-3beta,17beta-diol. Horm. Behav. 2008, 53:741-752.
21. Harman S.M., Metter E.J., Tobin J.D., Pearson J., Blackman M.R., Baltimore Longitudinal Study of, A Longitudinal effects of aging on serum total and free testosterone levels in healthy men. Baltimore Longitudinal Study of Aging. J. Clin. Endocrinol. Metab. 2001, 86:724-731.
22. Hummer D.L., Peckham E.M., Lee T.M. Estradiol acts during a post-pubertal sensitive period to shorten free-running circadian period in male Octodon degus. Eur. J. Neurosci. 2012, 36:3051-3058.
23. Hut R.A., Kronfeld-Schor N., van der Vinne V., De la Iglesia H. In search of a temporal niche: environmental factors. Prog. Brain Res. 2012, 199:281-304.
24. Iwahana E., Karatsoreos I., Shibata S., Silver R. Gonadectomy reveals sex differences in circadian rhythms and suprachiasmatic nucleus androgen receptors in mice. Horm. Behav. 2008, 53:422-430.
25. Jahan M.R., Kokubu K., Islam M.N., Matsuo C., Yanai A., Wroblewski G., Fujinaga R., Shinoda K. Species differences in androgen receptor expression in the medial preoptic and anterior hypothalamic areas of adult male and female rodents. Neuroscience 2015, 284:943-961.
26. 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.
27. Karatsoreos I.N., Yan L., LeSauter J., Silver R. Phenotype matters: identification of light-responsive cells in the mouse suprachiasmatic nucleus. J. Neurosci. 2004, 24:68-75.
28. Karatsoreos I.N., Wang A., Sasanian J., Silver R. A role for androgens in regulating circadian behavior and the suprachiasmatic nucleus. Endocrinology 2007, 148:5487-5495.
29. Karatsoreos I.N., Butler M.P., Lesauter J., Silver R. Androgens modulate structure and function of the suprachiasmatic nucleus brain clock. Endocrinology 2011, 152:1970-1978.
30. Kashon M.L., Arbogast J.A., Sisk C.L. Distribution and hormonal regulation of androgen receptor immunoreactivity in the forebrain of the male European ferret. J. Comp. Neurol. 1996, 376:567-586.
31. Kavanau J.L. Influences of light on activity of the small mammals, Peromyscus spp., Tamias striatus, and Mustela rixosa. Experientia 1969, 25:208-209.
32. Klein D.C., Moore R.Y., Reppert S.M. Suprachiasmatic Nucleus. The Mind's Clock 1991, 467. Oxford University Press, New York.
33. Koteja P., Swallow J.G., Carter P.A., Garland T. Different effects of intensity and duration of locomotor activity on circadian period. J. Biol. Rhythms 2003, 18:491-501.
34. Levy O., Dayan T., Kronfeld-Schor N. The relationship between the golden spiny mouse circadian system and its diurnal activity: an experimental field enclosures and laboratory study. Chronobiol. Int. 2007, 24:599-613.
35. Lu S.F., McKenna S.E., Cologer-Clifford A., Nau E.A., Simon N.G. Androgen receptor in mouse brain: sex differences and similarities in autoregulation. Endocrinology 1998, 139:1594-1601.
36. Lund T.D., Hinds L.R., Handa R.J. The androgen 5alpha-dihydrotestosterone and its metabolite 5alpha-androstan-3beta, 17beta-diol inhibit the hypothalamo-pituitary-adrenal response to stress by acting through estrogen receptor beta-expressing neurons in the hypothalamus. J. Neurosci. 2006, 26:1448-1456.
37. Manber R., Armitage R. Sex, steroids, and sleep: a review. Sleep 1999, 22:540-555.
38. Manber R., Bootzin R.R. Sleep and the menstrual cycle. Health Psychol. 1997, 16:209-214.
39. Melo P.R., Belisio A.S., Menezes A.A., Azevedo C.V. Influence of seasonality on circadian motor activity rhythm in common marmosets during puberty. Chronobiol. Int. 2010, 27:1420-1437.
40. Mong J.A., Baker F.C., Mahoney M.M., Paul K.N., Schwartz M.D., Semba K., Silver R. Sleep, rhythms, and the endocrine brain: influence of sex and gonadal hormones. J. Neurosci. 2011, 31:16107-16116.
41. Monk T.H. Aging human circadian rhythms: conventional wisdom may not always be right. J. Biol. Rhythms 2005, 20:366-374.
42. Morin L.P., Allen C.N. The circadian visual system, 2005. Brain Res. Rev. 2006, 51:1-60.
43. Morin L.P., Fitzgerald K.M., Rusak B., Zucker I. Circadian organization and neural mediation of hamster reproductive rhythms. Psychoneuroendocrinology 1977, 2:73-98.
44. Purdie D.W., Empson J.A., Crichton C., Macdonald L. Hormone replacement therapy, sleep quality and psychological wellbeing. Br. J. Obstet. Gynaecol. 1995, 102:735-739.
45. Roenneberg T., Kuehnle T., Pramstaller P.P., Ricken J., Havel M., Guth A., Merrow M. A marker for the end of adolescence. Curr. Biol. 2004, 14:R1038-R1039.
46. Schull J., Walker J., Fitzgerald K., Hiilivirta L., Ruckdeschel J., Schumacher D., Stanger D., McEachron D.L. Effects of sex, thyro-parathyroidectomy, and light regime on levels and circadian rhythms of wheel-running in rats. Physiol. Behav. 1989, 46:341-346.
47. Sellix M.T., Murphy Z.C., Menaker M. Excess androgen during puberty disrupts circadian organization in female rats. Endocrinology 2013, 154:1636-1647.
48. Sharma U.R., Rissman E.F. Testosterone implants in specific neural sites activate female sexual behaviour. J. Neuroendocrinol. 1994, 6:423-432.
49. Smale L., Lee T., Nunez A.A. Mammalian diurnality: some facts and gaps. J Biol Rhythms 2003, 18:356-366.
50. Veney S.L., Rissman E.F. Steroid implants in the medial preoptic area or ventromedial nucleus of the hypothalamus activate female sexual behaviour in the musk shrew. J. Neuroendocrinol. 2000, 12:1124-1132.
51. Vida B., Hrabovszky E., Kalamatianos T., Coen C.W., Liposits Z., Kallo I. Oestrogen receptor alpha and beta immunoreactive cells in the suprachiasmatic nucleus of mice: distribution, sex differences and regulation by gonadal hormones. J. Neuroendocrinol. 2008, 20:1270-1277.
52. Weisgerber D., Redlin U., Mrosovsky N. Lengthening of circadian period in hamsters by novelty-induced wheel running. Physiol. Behav. 1997, 62:759-765.
53. Welsh D.K., Takahashi J.S., Kay S.A. Suprachiasmatic nucleus: cell autonomy and network properties. Annu. Rev. Physiol. 2010, 72:551-577.
54. Williamson M., Bingham B., Gray M., Innala L., Viau V. The medial preoptic nucleus integrates the central influences of testosterone on the paraventricular nucleus of the hypothalamus and its extended circuitries. J. Neurosci. 2010, 30:11762-11770.
55. Yan L., Karatsoreos I., LeSauter J., Welsh D.K., Kay S.A., Foley D.K., Silver R. Exploring spatiotemporal organizatio of the SCN circuits. Clocks and Rhythms 2007, Cold Spring Harbor Laboratory Press.
56. Zucker I., Fitzgerald K.M., Morin L.P. Sex differentiation of the circadian system in the golden hamster. Am. J. Physiol. 1980, 238:R97-R101.