Rapid induction of hypothalamic iodothyronine deiodinase expression by photoperiod and melatonin in juvenile Siberian hamsters (Phodopus sungorus)

Endocrinology

Volumn 154, Issue 2, 2013, Pages 831-841

  Prendergast, Brian J ^a   Pyter, Leah M ^a   Kampf Lassin, August ^a   Patel, Priyesh N ^a   Stevenson, Tyler J ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIOTHYRONINE; MELATONIN; MESSENGER RNA; THYROXINE DEIODINASE; THYROXINE DEIODINASE 2; THYROXINE DEIODINASE 3; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; HORMONAL REGULATION; HORMONE RELEASE; HYPOPHYSIS GONAD SYSTEM; HYPOTHALAMUS; MALE; NONHUMAN; PERINATAL PERIOD; PHODOPUS; PHOTOPERIODICITY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; SIGNAL TRANSDUCTION; WEANING;

ANIMALS; CRICETINAE; ENZYME INDUCTION; FEMALE; HYPOTHALAMUS; IODIDE PEROXIDASE; MALE; MELATONIN; PHODOPUS; PHOTOPERIOD; RNA, MESSENGER; WEANING;

EID: 84872702823     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1990     Document Type: Article

References (66)

1. Goldman BD. Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurements. J Biol Rhythms. 2001;16(4):283-301. (Pubitemid 32706863)
2. Dawson A, King VM, Bentley GE, Ball GF. Photoperiodic control of seasonality in birds. J Biol Rhythms. 2001;16(4):365-380. (Pubitemid 32706869)
3. Stevenson TJ, Ball GF. Information theory and the neuropeptidergic regulation of seasonal reproduction in mammals and birds. Proc Biol Sci. 2011;278(1717):2477-2485.
4. Hoffman RA, Reiter RJ. Pineal gland: influence on gonads of male hamsters. Science. 1965;148(3677):1609-1611.
5. Reiter RJ. The pineal and its hormones in the control of reproduction in mammals. Endocr Rev. 1980;1(2):109-131.
6. Bartness TJ, Goldman BD. Peak duration of serum melatonin and short-day responses in adult Siberian hamsters. Am J Physiol. 1988;255(5 pt 2):812-822.
7. Illnerova H. The suprachiasmatic nucleus and rhythmic pineal melatonin production. In: Klein DC, Moore RY, Reppert SM, eds. Suprachiasmatic Nucleus: The Mind's Clock. New York, NY: Oxford University Press; 1991:157-176.
8. Badura LL, Goldman BD. Central sites mediating reproductive responses to melatonin in juvenile male Siberian hamsters. Brain Res. 1992;598(1-2):98-106. (Pubitemid 23013049)
9. Maywood ES, Hastings MH. Lesions of the iodomelatonin-binding sites of the mediobasal hypothalamus spare the lactotropic, but block the gonadotropic response of male Syrian hamsters to short photoperiod and to melatonin. Endocrinology. 1995;136(1):144-153.
10. Freeman DA, Zucker I. Refractoriness to melatonin occurs independently at multiple brain sites in Siberian hamsters. Proc Natl Acad Sci USA. 2001;98:6447-6452. (Pubitemid 32488257)
11. Murphy M, Jethwa PH, Warner A, Barrett P, Nilaweera KN, Brameld JM, Ebling FJ. Effects of manipulating hypothalamic triiodothyronine concentrations on seasonal body weight and torpor cycles in Siberian hamsters. Endocrinology. 2012;153(1):101-112.
12. Ono H, Hoshino Y, Yasuo S, Watanabe M, Nakane Y, Murai A, Ebihara S, Korf HW, Yoshimura T. Involvement of thyrotropin in photoperiodic signal transduction in mice. Proc Natl Acad Sci USA. 2008;105(47):18238-18242.
13. Hanon EA, Lincoln GA, Fustin JM, Dardente H, Masson-Pevet M, Morgan PJ, Hazlerigg DG. Ancestral TSH mechanism signals summer in a photoperiodic mammal. Curr Biol. 2008;18(15):1147-1152.
14. Watanabe T, Yamamura T, Watanabe M, Yasuo S, Nakao N, Dawson A, Ebihara S, Yoshimura T. Hypothalamic expression of thyroid hormone-activating and -inactivating enzyme genes in relation to photorefractoriness in birds and mammals. Am J Physiol Regul Integr Comp Physiol. 2007;292:R568-R572. (Pubitemid 46089872)
15. Barrett P, Ebling FJ, Schuhler S, Wilson D, Ross AW, Warner A, Jethwa P, Boelen A, Visser TJ, Ozanne DM, Archer ZA, Mercer JG, Morgan PJ. Hypothalamic thyroid hormone catabolism acts as a gatekeeper for the seasonal control of body weight and reproduction. Endocrinology. 2007;148(8):3608-3617. (Pubitemid 47105856)
16. 3 mimics long day lengths in Siberian hamsters. Am J Physiol Regul Integr Comp Physiol. 2007;292(6):R2368-R2372.
17. Nakao N, Ono H, Yamamura T, Anraku T, Takagi T, Higashi K, Yasuo S, Katou Y, Kageyama S, Uno Y, Kasukawa T, Iigo M, Sharp PJ, Iwasawa A, Suzuki Y, Sugano S, Niimi T, Mizutani M, Namikawa T, Ebihara S, Ueda HR, Yoshimura T. Thyrotrophin in the pars tuberalis triggers photoperiodic responses. Nature. 2008;452(7185):317-322. (Pubitemid 351430794)
18. 3 regulates photoperiodic responses of gonads in birds. Nature. 2003;426(6963):178-181.
19. Yasuo S, Watanabe M, Nakao N, Takagi T, Follett BK, Ebihara S, Yoshimura T. The reciprocal switching of two thyroid hormone-activating and inactivating enzyme genes is involved in the photoperiodic gonadal response of Japanese quail. Endocrinology. 2005;146(6):2551-2554. (Pubitemid 40695557)
20. Wilson FE, Reinert BD. Thyroid hormone acts centrally to programme photostimulated male American tree sparrows for vernal and autumnal components of seasonality. J Neuroendocrinol. 2000;12(1):87-95. (Pubitemid 30098939)
21. Lechan RM, Fekete C. Role of thyroid hormone deiodination in the hypothalamus. Thyroid. 2005;15(8):883-897. (Pubitemid 41339267)
22. Revel FG, Saboureau M, Pevet P, Mikkelsen JD, Simoneaux V. Melatonin regulates type 2 deiodinase gene expression in the Syrian hamster. Endocrinology. 2006;147(10):4680-4687. (Pubitemid 44402175)
23. Yasuo S, Yoshimura T, Ebihara, S, Korf HW. Temporal dynamics of type 2 deiodinase expression after melatonin injections in Syrian hamsters. Endocrinology. 2007;148(9):4385-4392. (Pubitemid 47295692)
24. Herwig A, Petri I, Barrett P. Hypothalamic gene expression rapidly changes in response to photoperiod in juvenile Siberian hamsters (Phodopus sungorus). J Neuroendocrinol. 2012;24(7):991-998.
25. Hoffman K. Photoperiod, pineal, melatonin and reproduction in hamsters. Prog Brain Res. 1979;52:397-415.
26. Spears N, Finley CM, Whaling CS, Tuthill CR, Zucker I. Sustained reproductive responses in Djungarian hamsters exposed to a single long day. J Reprod Fertil. 1990;88(2):635-643. (Pubitemid 20109941)
27. Whaling CS. Kelly KK, Finley CM, Spears N, Licht P, Zucker I. Sustained hormonal responses of Siberian hamsters to a single longer day at weaning. Biol Reprod. 1993;49(3):555-560. (Pubitemid 23259679)
28. Prendergast BJ, Hotchkiss AK, Nelson RJ. Photoperiodic regulation of circulating leukocytes in juvenile Siberian hamsters: mediation by melatonin and testosterone. J Biol Rhythms. 2003;18(6):473-480. (Pubitemid 37463297)
29. Prendergast BJ, Hotchkiss AK, Bilbo SD, Nelson RJ. Peripubertal immune challenges attenuate reproductive development in male Siberian hamsters. Biol Reprod. 2004;70(3):813-820. (Pubitemid 38233721)
30. Prendergast BJ, Kelly KK, Zucker I, Gorman MR. Enhanced reproductive responses to melatonin in juvenile Siberian hamsters. Am J Physiol Regul Integr Comp Physiol. 1996;271(4 pt 2):R1041-R1046.
31. Tamarkin L, Hollister CW, Lefebvre NG, Goldman BD. Melatonin induction of gonadal quiescence in pinealectomized Syrian hamsters. Science. 1977;198(4320):953-955. (Pubitemid 8225873)
32. Yellon SM, Goldman BD. Photoperiod control of reproductive development in male Djungarian hamster. Endocrinology. 1984;114(5):664-670. (Pubitemid 14183274)
33. Yellon SM, Tamarkin L, Goldman BD. Maturation of the pineal melatonin rhythm in long and short day reared Djungarian hamsters. Experientia. 1985;15(4):651-652. (Pubitemid 15001025)
34. Stetson MH, Elliott JA, Goldman BD. Maternal transfer of photoperiodic information influences the photoperiodic response of prepubertal Djungarian hamsters. Biol Reprod. 1986;34(4):664-669.
35. Carter DS, Goldman BD. Antigonadal effect of timed melatonin infusion in pinealectomized male Djungarian hamsters: duration is the critical parameter. Endocrinology. 1983;113(12):1261-1267. (Pubitemid 13009132)
36. Lehman MN, Ladha Z, Coolen LM, Hileman SM, Connors JM, Goodman RL. Neuronal plasticity and seasonal reproduction in sheep. Eur J Neurosci. 2010;32(2):2152-2164.
37. Clarke IJ, Smith JT. The role of kisspeptin and gonadotropin inhibitory hormone in the seasonality of reproduction in sheep. Soc Reprod Fertil Suppl. 2010;67(3):159-169.
38. Tsutsui K, Bentley GE, Bedecarrats G, Osugi T, Ubuka T, Kriegsfeld LJ. Gonadotropin-inhibitory hormone (GnIH) and its control of central and peripheral reproductive function. Front Neuroendocrinol. 2010;31(3):284-295.
39. Oakley AE, Clifton DK, Steiner RA. Kisspeptin signaling in the brain. Endocr Rev. 2009;30(6):713-743.
40. Simonneaux V, Ansel L, Revel FG, Klosen P, Pevet P, Mikkelsen JD. Kisspeptin and the seasonal control of reproduction in hamsters. Peptides. 2009;30(1):146-153.
41. Greives TJ, Kriegsfeld LJ, Bentley GE, Tsutsui K, Demas GE. Recent advances in reproductive neuroendocrinology: a role for RFamide peptides in seasonal reproduction. Proc Biol Sci. 2008;275(1646):1943-1951.
42. Greives TJ, Mason AO, Scotti MA, Levine J, Ketterson ED, Kriegsfeld LJ, Demas GE. Environmental control of kisspeptin: implications for seasonal reproduction. Endocrinology. 2007;148(3):1158-1166.
43. Paul MJ, Pyter LM, Freeman DA, Galang J, Prendergast BJ. Photic and nonphotic seasonal cues differentially engage hypothalamic kisspeptin and RFamide-related peptide mRNA expression in Siberian hamsters. J Neuroendocrinol. 2009;21(12):1007-1014.
44. Ubuka T, Inoue K, Fukuda Y, Mizuno T, Ukena K, Kriegsfeld LJ, Tsutsui K. Identification, expression and physiological functions of Siberian hamster gonadotropin-inhibitory hormone. Endocrinology. 2012;153(1):373-385.
45. Greives TJ, Long KL, Burns CM, Demas GE. Response to exogenous kisspeptin varies according to sex and reproductive conditions in Siberian hamsters. Gen Comp Endocrinol. 2011;170(1):172-179.
46. Prendergast BJ, Yellon SM, Tran LT, Nelson RJ. Photoperiod modulates the inhibitory effect of in vitro melatonin on lymphocyte proliferation in female Siberian hamsters. J Biol Rhythms. 2001;16(3):224-233. (Pubitemid 32516197)
47. Puchalski W, Lynch GR. Daily melatonin injections affect the expression of circadian rhythmicity in Djungarian hamsters kept under a long-day photoperiod. Neuroendocrinology. 1988;48(3):280-286.
48. Milette JJ, Turek FW. Circadian and photoperiodic effects of brief light pulses in male Djungarian hamsters. Biol Reprod. 1986;35(2):327-335.
49. Gardiner E, Beveridge NJ, Wu JQ, Carr V, Scott RJ, Tooney PA, Cairns MJ. Imprinted DLK1-DIO3 region of 14q32 defines a schizophrenia-associated miRNA signature in peripheral blood mononuclear cells. Mol Psychiatry. 2012;17(8):827-840.
50. Elliott JA, Bartness TJ, Goldman BD. Effect of melatonin infusion duration and frequency on gonad, lipid, and body mass in pinealectomized male Siberian hamsters. J Biol Rhythms. 1989;4(4):439-455.
51. Prendergast BJ, Zucker I, Yellon SM, Ringold DA, Gorman MR. Melatonin chimeras alter reproductive development and photorefractoriness in Siberian hamsters. J Biol Rhythms. 1998;13(6):518-531. (Pubitemid 128477535)
52. Yamamura T, Hirunagi K, Ebihara S, Yoshimura T. Seasonal morphological changes in the neuro-glial interaction between gonadotropin-releasing hormone nerve terminals and glial endfeet in Japanese quail. Endocrinology. 2004;145(9):4264-4267. (Pubitemid 39120575)
53. Isorna E, Obregon MJ, Calvo RM, Vázquez R, Pendón C, Falcón J, Muñoz-Cueto JA. Iodothyronine deiodinases and thyroid hormone receptors regulation during flatfish (Solea senegalensis) metamorphosis. J Exp Zool B Mol Dev Evol. 2009;312B(3):231-246.
54. Itoh K, Watanabe K, Wu X, Suzuki T. Three members of the iodothyronine deiodinase family, dio1, dio2 and dio3, are expressed in spatially and temporally specific patterns during metamorphosis of the flounder, Paralichthys olivaceus. Zoolog Sci. 2010;27(7):574-580.
55. 3 regulation of thyroid hormone- and sex steroid-related genes during Silurana (Xenopus) tropicalis early development. Gen Comp Endocrinol. 2010;166(2):428-435.
56. Duarte-Guterman P, Trudeau VL. Regulation of thyroid hormone-, oestrogen- and androgen-related genes by triiodothyronine in the brain of Silurana tropicalis. J Neuroendocrinol. 2010;22(9):1023-1031.
57. Duarte-Guterman P, Ryan MJ, Hogan NS, Trudeau VL. Developmental profiles and thyroid hormone regulation of brain transcripts in frogs: a species comparison with emphasis on Physalaemus pustulosus. Brain Behav Evol. 2012;79(2):98-112.
58. Ball GF, Ketterson ED. Sex differences in the response to environmental cues regulating seasonal reproduction in birds. Philos Trans R Soc Lond B Biol Sci. 2008;363(1490):231-246. (Pubitemid 350249338)
59. Shaw D, Goldman BD. Gender differences in influence of prenatal photoperiods on postnatal pineal melatonin rhythms and serum prolactin and follicle-stimulating hormone in the Siberian hamster. Endocrinology. 1995;136(10):4237-4246.
60. Beery AK, Zucker I. Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev. 2011;565(3):572.
61. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS Jr, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG. The GPR54 gene as a regulator of puberty. New Eng J Med. 2003;349(17):1614-1627. (Pubitemid 37303886)
62. Pinilla L, Aguilar E, Dieguez C, Millar RP, Tena-Sempere M. Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiol Rev. 2012;92(3):1235-1316.
63. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci. 2005;25(49):11349-11356. (Pubitemid 43083709)
64. Clarkson J, Herbison AE. Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin releasing hormone neurons. Endocrinology. 2006;147(12):5817-5825. (Pubitemid 44833498)
65. Butler MP, Turner KW, Zucker I. A melatonin-independent seasonal timer induces neuroendocrine refractoriness to short day lengths. J Biol Rhythms. 2008;23(3):242-251. (Pubitemid 351652374)
66. Dooley JC, Prendergast BJ. Photorefractoriness and energy availability interact to permit facultative timing of spring breeding. Behav Ecol. 2012;23(5):1049-1058.