Effect of arousing stimuli on circulating corticosterone and the circadian rhythms of luteinizing hormone (LH) surges and locomotor activity in estradiol-treated ovariectomized (ovx + EB) Syrian hamsters

Hormones and Behavior

Volumn 72, Issue , 2015, Pages 28-38

  Legan, S J ^a   Peng, X ^a   Yun, C ^a   Duncan, M J ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Arousal; Circadian rhythm; Corticosterone; Estradiol benzoate; Locomotor activity rhythm; Luteinizing hormone; Novel wheel; Ovariectomy; Phase advance; Syrian hamster

Indexed keywords

CORTICOSTERONE; ESTRADIOL BENZOATE; LUTEINIZING HORMONE; ESTRADIOL; ESTRADIOL 3-BENZOATE;

ADULT; ANIMAL EXPERIMENT; AROUSAL; ARTICLE; BLOOD SAMPLING; CIRCADIAN RHYTHM; CONTROLLED STUDY; DARKNESS; FEMALE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LOCOMOTION; MALE; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROESTRUS; SYRIAN HAMSTER; TREADMILL TEST; ZEITGEBER TIME; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; DRUG EFFECTS; HAMSTER; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MESOCRICETUS; METABOLISM; MOTOR ACTIVITY; PHYSIOLOGY; WAKEFULNESS;

ANIMALS; AROUSAL; CIRCADIAN RHYTHM; CORTICOSTERONE; CRICETINAE; ESTRADIOL; FEMALE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LUTEINIZING HORMONE; MALE; MESOCRICETUS; MOTOR ACTIVITY; OVARIECTOMY; PITUITARY-ADRENAL SYSTEM; WAKEFULNESS;

EID: 84929224007     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2015.04.020     Document Type: Article

References (70)

1. Albers H.E., Yogev L., Todd R.B., Goldman B.D. Adrenal corticoids in hamsters: role in circadian timing. Am. J. Physiol. 1985, 248:R434-R438.
2. Antle M.C., Mistlberger R.E. Circadian clock resetting by sleep deprivation without exercise in the Syrian hamster. J. Neurosci. 2000, 20:9326-9332.
3. Antle M.C., Steen N.M., Mistlberger R.E. Adenosine and caffeine modulate circadian rhythms in the Syrian hamster. Neuroreport 2001, 12:2901-2905.
4. Atkinson H.C., Waddell B.J. Circadian variation in basal plasma corticosterone and adrenocorticotropin in the rat: sexual dimorphism and changes across the estrous cycle. Endocrinology 1997, 138:3842-3848.
5. Baldwin D.M. The effect of glucocorticoids on estrogen-dependent luteinizing hormone release in the ovariectomized rat and on gonadotropin secretin in the intact female rat. Endocrinology 1979, 105:120-128.
6. Baldwin D.M., Colombo J.A., Sawyer C.H. Plasma prolactin, LH, and corticosterone in rats exposed to a novel environment. Am. J. Physiol. 1974, 226:1366-1369.
7. Blake C.A., Elias K.A., Huffman L.J. Ovariectomy of young adult rats has a sparing effect on the ability of aged rats to release luteinizing hormone. Biol. Reprod. 1983, 28:575-585.
8. Briski K.P. Stimulatory vs. inhibitory effects of acute stress on plasma LH: differential effects of pretreatment with dexamethasone or the steroid receptor antagonist, RU 486. Pharmacol. Biochem. Behav. 1996, 55:19-26.
9. Buijs R.M., Wortel J., Van Heerikhuize J.J., Kalsbeek A. Novel environment induced inhibition of corticosterone secretion: physiological evidence for a suprachiasmatic nucleus mediated neuronal hypothalamo-adrenal cortex pathway. Brain Res. 1997, 758:229-236.
10. Castanon-Cervantes O., Wu M., Ehlen J.C., Paul K., Gamble K.L., Johnson R.L., Besing R.C., Menaker M., Gewirtz A.T., Davidson A.J. Dysregulation of inflammatory responses by chronic circadian disruption. J. Immunol. 2010, 185:5796-5805.
11. Christian C., Mobley J., Moenter S. Diurnal and estradiol-dependent changes in gonadotropin-releasing hormone neurone firing activity. Proc. Natl. Acad. Sci. U. S. A. 2005, 43:15682-15687.
12. Davidson A.J., Sellix M.T., Daniel J., Yamazaki S., Menaker M., Block G.D. Chronic jet-lag increases mortality in aged mice. Curr. Biol. 2006, 16:R914-R916.
13. Davidson A.J., Castanon-Cervantes O., Leise T.L., Molyneux P.C., Harrington M.E. Visualizing jet lag in the mouse suprachiasmatic nucleus and peripheral circadian timing system. Eur. J. Neurosci. 2009, 29:171-180.
14. Davis S., Mirick D.K. Circadian disruption, shift work and the risk of cancer: a summary of the evidence and studies in Seattle. Cancer Causes Control 2006, 17:539-545.
15. Donadio M.V., Kunrath A., Corezola K.L., Franci C.R., Anselmo-Franci J.A., Lucion A.B., Sanvitto G.L. Effects of acute stress on the day of proestrus on sexual behavior and ovulation in female rats: participation of the angiotensinergic system. Physiol. Behav. 2007, 92:591-600.
16. Duncan M.J., Franklin K.M., Peng X., Yun C., Legan S.J. Circadian rhythm disruption by a novel running wheel: roles of exercise and arousal in blockade of the luteinizing hormone surge. Physiol. Behav. 2014, 131:7-16.
17. Gamble K.L., Resuehr D., Johnson C.H. Shift work and circadian dysregulation of reproduction. Front. Endocrinol. (Lausanne.) 2013, 4:92.
18. Gaskin J.H., Kitay J.I. Adrenocortical function in the hamster. Sex differences and effects of gonadal hormones. Endocrinology 1970, 87:779-786.
19. Glass J.D., Guinn J., Kaur G., Francl J.M. On the intrinsic regulation of neuropeptide Y release in the mammalian suprachiasmatic nucleus circadian clock. Eur. J. Neurosci. 2010, 31:1117-1126.
20. Goldman B.D., Mahesh V.B. A possible role of acute FSH-release in ovulation in the hamster, as demonstrated by utilization of antibodies to LH and FSH. Endocrinology 1969, 84:236-243.
21. Goldman B.D., Mahesh V.B., Porter J.C. The role of the ovary in control of cyclic LH release in the hamster, Mesocricetus auratus. Biol. Reprod. 1971, 4:57-65.
22. Gore A.C., Attardi B., DeFranco D.B. Glucocorticoid repression of the reproductive axis: effects on GnRH and gonadotropin subunit mRNA levels. Mol. Cell. Endocrinol. 2006, 256:40-48.
23. Greenwald G.S. Preovulatory changes in ovulating hormone in the cyclic hamster. Endocrinology 1971, 88:671-677.
24. Hastings M.H., Mead S.M., Vindlacheruvu R.R., Ebling F.J., Maywood E.S., Grosse J. Non-photic phase shifting of the circadian activity rhythm of Syrian hamsters: the relative potency of arousal and melatonin. Brain Res. 1992, 591:20-26.
25. Hastings M.H., Reddy A.B., Maywood E.S. A clockwork web: circadian timing in brain and periphery, in health and disease. Nat. Rev. Neurosci. 2003, 4:649-661.
26. Hauser U.E., Benson B. Rapid cessation of estrous cyclicity and depressed castration response in short photoperiod-treated, inbred LSH/SsLak hamsters. Biol. Reprod. 1986, 35:276-281.
27. Hueston C.M., Deak T. On the time course, generality, and regulation of plasma progesterone release in male rats by stress exposure. Endocrinology 2014, 155:3527-3537.
28. Huhman K.L., Albers H.E. Neuropeptide Y microinjected into the suprachiasmatic region phase shifts circadian rhythms in constant darkness. Peptides 1994, 15:1475-1478.
29. Janik D., Nest K.J., Janiga M.A. Exogenous corticosteroid and shifts of circadian rhythms in hamsters. Chronobiol. Int. 2001, 18:203-213.
30. Jorgenson K.L., Schwartz N.B. Effect of steroid treatment on tonic and surge secretion of LH and FSH in the female golden hamster: effect of photoperiod. Neuroendocrinology 1984, 39:549-554.
31. Kam K., Park Y., Cheon M., Son G.H., Kim K., Ryu K. Effects of immobilization stress on estrogen-induced surges of luteinizing hormone and prolactin in ovariectomized rats. Endocrine 2000, 12:279-287.
32. Legan S.J., Karsch F.J. A daily signal for the LH surge in the rat. Endocrinology 1975, 96:57-62.
33. Legan S.J., Coon G.A., Karsch F.J. Role of estrogen as initiator of daily LH surges in the ovariectomized rat. Endocrinology 1975, 96:50-56.
34. Legan S.J., Donoghue K.M., Franklin K.M., Duncan M.J. Phenobarbital blockade of the preovulatory luteinizing hormone surge: association with phase-advanced circadian clock and altered suprachiasmatic nucleus Period1 gene expression. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296:R1620-R1630.
35. Legan S.J., Franklin K.M., Peng X.L., Duncan M.J. Novel wheel running blocks the preovulatory luteinizing hormone surge and advances the hamster circadian pacemaker. J. Biol. Rhythms 2010, 25:450-459.
36. Mikkelsen J.D., Vrang N., Mrosovsky N. Expression of Fos in the circadian system following nonphotic stimulation. Brain Res. Bull. 1998, 47:367-376.
37. Mistlberger R.E., Antle M.C., Webb I.C., Jones M., Weinberg J., Pollock M.S. Circadian clock resetting by arousal in Syrian hamsters: the role of stress and activity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003, 285:R917-R925.
38. Moline M.L., Albers H.E., Moore-Ede M.C. Estrogen modifies the circadian timing and amplitude of the luteinizing hormone surge in female hamsters exposed to short photoperiods. Biol. Reprod. 1986, 35:516-523.
39. Moser M., Schaumberger K., Schernhammer E., Stevens R.G. Cancer and rhythm. Cancer Causes Control 2006, 17:483-487.
40. Mrosovsky N. Phase response curves for social entrainment. J. Comp. Physiol. A 1988, 162:35-46.
41. Mrosovsky N. Locomotor activity and non-photic influences on circadian clocks. Biol. Rev. Camb. Philos. Soc. 1996, 71:343-372.
42. Mrosovsky N., Salmon P.A. Triazolam and phase-shifting acceleration re-evaluated. Chronobiol. Int. 1990, 7:35-41.
43. Muscat L., Morin L.P. Intergeniculate leaflet: Contributions to photic and non-photic responsiveness of the hamster circadian system. Neuroscience 2006, 140:305-320.
44. Norman R.L., Spies H.G. Neural control of the estrogen-dependent twenty-four-hour periodicity of LH release in the golden hamster. Endocrinology 1974, 95:1367-1372.
45. Norman R.L., Blake C.A., Sawyer C.H. Estrogen-dependent twenty-four-hour periodicity in pituitary LH release in the female hamster. Endocrinology 1973, 93:965-970.
46. Orsini M.W. The external vaginal phenomena characterizing the stages of the estrous cycle, pregnancy, pseudopregnancy, lactation, and the anestrous hamster, Mesocricetus auratus waterhouse. Waterhouse Proc Anim Care Panel 1961, 11:193-206.
47. Reebs S.G., Mrosovsky N. Effects of induced wheel running on the circadian activity rhythms of Syrian hamsters: entrainment and phase response curve. J. Biol. Rhythms 1989, 4:39-48.
48. Reul J.M., Stec I., Söder M., Holsboer F. Chronic treatment of rats with the antidepressant amitriptyline attenuates the activity of the hypothalamic-pituitary-adrenocortical system. Endocrinology 1993, 133:312-320.
49. Rivier C., Rivest S. Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: peripheral and central mechanisms. Biol. Reprod. 1991, 45:523-532.
50. Roozendaal M.M., Swarts H.J.M., Wiegant V.M., Mattheij J.A.M. Effect of restraint stress on the preovulatory luteinizing hormone profile and ovulation in the rat. Eur. J. Endocrinol. 1995, 133:347-353.
51. Salgado-Delgado R.C., Saderi N., Basualdo M.C., Guerrero-Vargas N.N., Escobar C., Buijs R.M. Shift work or food intake during the rest phase promotes metabolic disruption and desynchrony of liver genes in male rats. PLoS One 2013, 8:e60052.
52. Seegal R.F., Goldman B.D. Effects of photoperiod on cyclicity and serum gonadotropins in the Syrian hamster. Biol. Reprod. 1975, 12:223-231.
53. Seggie J.A., Brown G.M. Stress response patterns of plasma corticosterone, prolactin, and growth hormone in the rat, following handling or exposure to novel environment. Can. J. Physiol. Pharmacol. 1975, 53:629-637.
54. Shander D., Goldman B. Ovarian steroid modulation of gonadotropin secretion and pituitary responsiveness to luteinizing hormone-releasing hormone in the female hamster. Endocrinology 1978, 103:1383-1393.
55. Spiegel K., Tasali E., Leproult R., Van Cauter E. Effects of poor and short sleep on glucose metabolism and obesity risk. Nat. Rev. Endocrinol. 2009, 5:253-261.
56. Stetson M.H., Watson-Whitmyre M. The neural clock regulating estrous cyclicity in hamsters: gonadotropin release following barbiturate blockade. Biol. Reprod. 1977, 16:536-542.
57. Stetson M.H., Watson-Whitmyre M., Matt K.S. Cyclic gonadotropin release in the presence and absence of estrogenic feedback in ovariectomized golden hamsters. Biol. Reprod. 1978, 19:40-50.
58. Stetson M.H., Watson-Whitmyre M., Dipinto M.N., Smith S.G. Daily luteinizing hormone release in ovariectomized hamsters: effect of barbiturate blockade. Biol. Reprod. 1981, 24:139-144.
59. Swann J., Turek F.W. Multiple circadian oscillators regulate the timing of behavioral and endocrine rhythms in female golden hamsters. Science 1985, 228:898-899.
60. Traslavina G.A., Franci C.R. The CRH-R(1) receptor mediates luteinizing hormone, prolactin, corticosterone and progesterone secretion induced by restraint stress in estrogen-primed rats. Brain Res. 2011, 1421:11-19.
61. Tsai H.-W., Legan S.J. Chronic elevation of estradiol in young ovariectomized rats causes aging-like loss of steroid-induced luteinizing hormone surges. Biol. Reprod. 2001, 64:691-695.
62. Turek F.W. From circadian rhythms to clock genes in depression. Int. Clin. Psychopharmacol. 2007, 22(Suppl. 2):S1-S8.
63. Turek F.W., Van R.O. Use of benzodiazepines to manipulate the circadian clock regulating behavioral and endocrine rhythms. Horm. Res. 1989, 31:59-65.
64. Van Reeth O., Turek F.W. Stimulated activity mediates phase shifts in the hamster circadian clock induced by dark pulses or benzodiazepines. Nature 1989, 339:49-51.
65. Viau V., Bingham B., Davis J., Lee P., Wong M. Gender and puberty interact on the stress-induced activation of parvocellular neurosecretory neurons and corticotropin-releasing hormone messenger ribonucleic acid expression in the rat. Endocrinology 2005, 146:137-146.
66. Webb I.C., Pollock M.S., Mistlberger R.E. Modafinil [2-[(diphenylmethyl)sulfinyl]acetamide] and circadian rhythms in Syrian hamsters: assessment of the chronobiotic potential of a novel alerting compound. J. Pharmacol. Exp. Ther. 2006, 317:882-889.
67. Webb I.C., Patton D.F., Hamson D.K., Mistlberger R.E. Neural correlates of arousal-induced circadian clock resetting: hypocretin/orexin and the intergeniculate leaflet. Eur. J. Neurosci. 2008, 27:828-835.
68. Weinberg J., Wong R. Adrenocortical responsiveness to novelty in the hamster. Physiol. Behav. 1986, 37:669-672.
69. Wickland C.R., Turek F.W. Phase-shifting effects of acute increases in activity on circadian locomotor rhythms in hamsters. Am. J. Physiol. 1991, 261:R1109-R1117.
70. Wolff G., Duncan M.J., Esser K.A. Chronic phase advance alters circadian physiological rhythms and peripheral molecular clocks. J. Appl. Physiol. (1985) 2013, 115:373-382.