Melatonin-Dependent Timing of Seasonal Reproduction by the Pars Tuberalis: Pivotal Roles for Long Daylengths and Thyroid Hormones

Journal of Neuroendocrinology

Volumn 24, Issue 2, 2012, Pages 249-266

  Dardente, Hugues ^a  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

Author keywords

FSH; GnRH; Kisspeptin; LH; Melatonin; Oestrogens

Indexed keywords

DEIODINASE 2; FOLLITROPIN; GONADORELIN; IODIDE PEROXIDASE; LIOTHYRONINE; LUTEINIZING HORMONE; MELATONIN; MELATONIN RECEPTOR; PROGESTERONE; PROLACTIN; THYROID HORMONE; THYROTROPIN; THYROXINE; UNCLASSIFIED DRUG;

ANESTRUS; AUTUMN; BREEDING; CIRCADIAN RHYTHM; DAY LENGTH; DRUG DIFFUSION; DRUG EFFECT; DRUG INFUSION; EWE; GENETIC CODE; HORMONAL THERAPY; HORMONE INHIBITION; HORMONE RELEASE; HYPOPHYSIS PARS TUBERALIS; HYPOTHALAMUS; IMPLANT; LOW DRUG DOSE; MOLECULAR DYNAMICS; NEUROENDOCRINE SYSTEM; NONHUMAN; OVARY CYCLE; PARACRINE SIGNALING; PHOTOPERIODICITY; PRIORITY JOURNAL; PROLACTIN RELEASE; PROTEIN LOCALIZATION; RAM (SHEEP); REVIEW; SEASONAL REPRODUCTION; SEASONAL VARIATION; SHEEP; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; SPRING; SUMMER; SYRIAN HAMSTER; THYROTROPIN RELEASE; WINTER;

ANIMALS; CIRCADIAN RHYTHM; CRICETINAE; MELATONIN; MESOCRICETUS; PHOTOPERIOD; PITUITARY GLAND; REPRODUCTION; SEASONS; SHEEP; THYROID HORMONES; TIME FACTORS;

EID: 84855931783     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2011.02250.x     Document Type: Review

References (225)

1. Chemineau P, Guillaume D, Migaud M, Thiery JC, Pellicer-Rubio MT, Malpaux B. Seasonality of reproduction in mammals: intimate regulatory mechanisms and practical implications. Reprod Domest Anim 2008; 43: 40-47.
2. International Sheep Genomics Consortium, Archibald AL, Cockett NE, Dalrymple BP, Faraut T, Kijas JW, Maddox JF, McEwan JC, Hutton Oddy V, Raadsma HW, Wade C, Wang J, Wang W, Xun X. The sheep genome reference sequence: a work in progress. Anim Genet 2010; 41: 449-453.
3. Groeneveld LF, Lenstra JA, Eding H, Toro MA, Scherf B, Pilling D, Negrini R, Finlay EK, Jianlin H, Groeneveld E, Weigend S, GLOBALDIV Consortium. Genetic diversity in farm animals - a review. Anim Genet 2010; 41: 6-31.
4. Pelletier J, Garnier DH, de Reviers MM, Terqui M, Ortavant R. Seasonal variation in LH and testosterone release in rams of two breeds. J Reprod Fertil 1982; 64: 341-346.
5. D'Occhio MJ, Schanbacher BD, Kinder JE. Profiles of luteinizing hormone, follicle-stimulating hormone, testosterone and prolactin in rams of diverse breeds: effects of contrasting short (8L:16D) and long (16L:8D) photoperiods. Biol Reprod 1984; 30: 1039-1054.
6. Lincoln GA, Lincoln CE, McNeilly AS. Seasonal cycles in the blood plasma concentration of FSH, inhibin and testosterone, and testicular size in rams of wild, feral and domesticated breeds of sheep. J Reprod Fertil 1990; 88: 623-633.
7. Chemineau P, Bodin L, Migaud M, Thiery JC, Malpaux B. Neuroendocrine and genetic control of seasonal reproduction in sheep and goats. Reprod Domest Anim 2010; 45: 42-49.
8. Robinson JE, Karsch FJ. Refractoriness to inductive day lengths terminates the breeding season of the Suffolk ewe. Biol Reprod 1984; 31: 656-663.
9. Bittman EL, Karsch FJ, Hopkins JW. Role of the pineal gland in ovine photoperiodism: regulation of seasonal breeding and negative feedback effects of estradiol upon luteinizing hormone secretion. Endocrinology 1983; 30: 329-336.
10. Bittman EL, Karsch FJ. Nightly duration of pineal melatonin secretion determines the reproductive response to inhibitory day length in the ewe. Biol Reprod 1984; 43: 585-593.
11. Yellon SM, Bittman EL, Lehman MN, Olster DH, Robinson JE, Karsch FJ. Importance of duration of nocturnal melatonin secretion in determining the reproductive response to inductive photoperiod in the ewe. Biol Reprod 1985; 32: 523-529.
12. Simonneaux V, Ribelayga C. Generation of the melatonin endocrine message in mammals: a review of the complex regulation of melatonin synthesis by norepinephrine, peptides, and other pineal transmitters. Pharmacol Rev 2003; 55: 325-395.
13. Legan SJ, Karsch FJ. Photoperiodic control of seasonal breeding in ewes: modulation of the negative feedback action of estradiol. Biol Reprod 1980; 23: 1061-1068.
14. Webster GM, Haresign W. Seasonal changes in LH and prolactin concentrations in ewes of two breeds. J Reprod Fertil 1983; 67: 465-471.
15. Lincoln GA. Secretion of LH in rams exposed to two different photoperiods. J Reprod Fertil 1976; 47: 351-353.
16. Lincoln GA, Peet MJ. Photoperiodic control of gonadotrophin secretion in the ram: a detailed study of the temporal changes in plasma levels of follicle-stimulating hormone, luteinizing hormone and testosterone following an abrupt switch from long to short days. J Endocrinol 1977; 74: 355-367.
17. Mauléon P, Rougeot J. Régulation des saisons sexuelles chez des brebis de races différentes au moyen de divers rythmes lumineux. Ann Biol anim Bioch Biophys 1962; 2: 209-222.
18. Hauger RL, Karsch FJ, Foster DL. A new concept for control of the estrous cycle of the ewe based on the temporal relationships between luteinizing hormone, estradiol and progesterone in peripheral serum and evidence that progesterone inhibits tonic LH secretion. Endocrinology 1977; 101: 807-817.
19. Cumming IA, Buckmaster JM, Blockey MA, Goding JR, Winfield CG, Baxter RW. Constancy of interval between luteinizing hormone release and ovulation in the ewe. Biol Reprod 1973; 9: 24-29.
20. Lindsay DR, Cognié Y, Pelletier J, Signoret JP. Influence of the presence of rams on the timing of ovulation and discharge of LH in ewes. Physiol Behav 1975; 15: 423-426.
21. Yuthasastrakosol P, Palmer WM, Howland BE. Luteinizing hormone, oestrogen and progesterone levels in peripheral serum of anoestrous and cyclic ewes as determined by radioimmunoassay. J Reprod Fertil 1975; 43: 57-65.
22. Karsch FJ, Bowen JM, Caraty A, Evans NP, Moenter SM. Gonadotropin-releasing hormone requirements for ovulation. Biol Reprod 1997; 56: 303-309.
23. Goodman RL, Bittman EL, Foster DL, Karsch FJ. Alterations in the control of luteinizing hormone pulse frequency underlie the seasonal variation in estradiol negative feedback in the ewe. Biol Reprod 1982; 27: 580-589.
24. Robinson JE, Radford HM, Karsch FJ. Seasonal changes in pulsatile luteinizing hormone (LH) secretion in the ewe: relationship of frequency of LH pulses to day length and response to estradiol negative feedback. Biol Reprod 1985; 33: 324-334.
25. Barrell GK, Moenter SM, Caraty A, Karsch FJ. Seasonal changes of gonadotropin-releasing hormone secretion in the ewe. Biol Reprod 1992; 46: 1130-1135.
26. Karsch FJ, Dahl GE, Evans NP, Manning JM, Mayfield KP, Moenter SM, Foster DL. Seasonal changes in gonadotropin-releasing hormone secretion in the ewe: alteration in response to the negative feedback action of estradiol. Biol Reprod 1993; 49: 1377-1383.
27. Legan SJ, Karsch FJ. Neuroendocrine regulation of the estrous cycle and seasonal breeding in the ewe. Biol Reprod 1979; 20: 74-85.
28. Viguié C, Caraty A, Locatelli A, Malpaux B. Regulation of luteinizing hormone-releasing hormone (LHRH) secretion by melatonin in the ewe. I. Simultaneous delayed increase in LHRH and luteinizing hormone pulsatile secretion. Biol Reprod 1995; 52: 1114-1120.
29. Legan SJ, Karsch FJ, Foster DL. The endocrin control of seasonal reproductive function in the ewe: a marked change in response to the negative feedback action of estradiol on luteinizing hormone secretion. Endocrinology 1977; 101: 818-824.
30. Platt TE, Foster GS, Tarnavsky GK, Reeves JJ. Effects of photoperiod and estradiol on tonic gonadotropins in ovariectomized ewes. J Anim Sci 1983; 56: 1180-1185.
31. Pelletier J, Ortavant R. Photoperiodic control of LH release in the ram. I. Influence of increasing and decreasing light photoperiods. Acta Endocrinol (Copenh) 1975; 78: 435-441.
32. Pelletier J, Ortavant R. Photoperiodic control of LH release in the ram. II. Light-androgens interaction. Acta Endocrinol (Copenh) 1975; 78: 442-450.
33. Bittman EL, Kaynard AH, Olster DH, Robinson JE, Yellon SM, Karsch FJ. Pineal melatonin mediates photoperiodic control of pulsatile luteinizing hormone secretion in the ewe. Neuroendocrinology 1985; 40: 409-418.
34. Lubbers LS, Jackson GL. Neuroendocrine mechanisms that control seasonal changes of luteinizing hormone secretion in sheep are sexually differentiated. Biol Reprod 1993; 49: 1369-1376.
35. Kondo N, Sekijima T, Kondo J, Takamatsu N, Tohya K, Ohtsu T. Circannual control of hibernation by HP complex in the brain. Cell 2006; 125: 161-172.
36. Gwinner E. Circannual Rhythms. Berlin: Springer, 1986.
37. Zucker I. Circannual rhythms. In: Takahashi JS, Turek FW, Moore RY, eds. Handbook of Behavioural Neurobiology, Circadian Clocks. New York, NY: Kluwer/Plenum, 2001: 511-528.
38. Goldman BD. Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J Biol Rhythms 2001; 16: 283-301.
39. Lincoln GA, Hazlerigg DG. Mammalian circannual pacemakers. Soc Reprod Fertil Suppl 2010; 67: 171-186.
40. Wayne NL, Malpaux B, Karsch FJ. Photoperiodic requirements for timing onset and duration of the breeding season of the ewe: synchronization of an endogenous rhythm of reproduction. J Comp Physiol A 1990; 166: 835-842.
41. Woodfill CJ, Robinson JE, Malpaux B, Karsch FJ. Synchronization of the circannual reproductive rhythm of the ewe by discrete photoperiodic signals. Biol Reprod 1991; 45: 110-121.
42. Woodfill CJ, Wayne NL, Karsch FJ. Does seasonal reproductive state affect the neuroendocrine response of the ewe to a pattern of melatonin? J Biol Rhythms 1992; 7: 1-11.
43. Barrell GK, Thrun LA, Brown ME, Viguie C, Karsch FJ. Importance of photoperiodic signal quality to entrainment of the circannual reproductive rhythm of the ewe. Biol Reprod 2000; 80: 769-774.
44. Kennaway DJ, Dunstan EA, Gilmore TA, Seamark RF. Effects of pinealectomy, oestradiol and melatonin on plasma prolactin and LH secretion in ovariectomized sheep. J Endocrinol 1984; 102: 199-207.
45. Lincoln GA, Libre EA, Merriam GR. Long-term reproductive cycles in rams after pinealectomy or superior cervical ganglionectomy. J Reprod Fertil 1989; 85: 687-704.
46. Rosa HJD, Bryant MJ. The 'ram effect' as a way of modifying the reproductive activity in the ewe. Small Rum Res 2002; 45: 1-16.
47. Rosa HJD, Bryant MJ. Seasonality of reproduction in sheep. Small Rum Res 2003; 48: 155-171.
48. Gelez H, Fabre-Nys C. The 'male effect' in sheep and goats: a review of the respective roles of the two olfactory systems. Horm Behav 2004; 46: 257-271.
49. Wodzicka-Tomaszewska M, Hutchinson JCD, Bennett JW. Control of the annual rhythm of breeding in ewes: effect of an equatorial daylength with reversed thermal seasons. J Agric Sci 1967; 68: 61-67.
50. Jackson GL, Jansen HT, Kuehl DE, Shanks RD. Time of the sidereal year affects responsiveness to the phase-resetting effects of photoperiod in the ewe. J Reprod Fertil 1989; 85: 221-227.
51. Kennaway DJ, Sanford LM, Godfrey B, Friesen HG. Patterns of progesterone, melatonin and prolactin secretion in ewes maintained in four different photoperiods. J Endocrinol 1983; 97: 229-242.
52. Lincoln GA, Ebling FJ. Effect of constant-release implants of melatonin on seasonal cycles in reproduction, prolactin secretion and moulting in rams. J Reprod Fertil 1985; 73: 241-253.
53. Thwaites CJ. Photoperiodic control of breeding activity in the southdown ewe with particular reference to the effects of an equatorial light regime. J Agric Sci 1965; 65: 57-64.
54. Jansen HT, Jackson GL. Circannual rhythms in the ewe: patterns of ovarian cycles and prolactin secretion under two different constant photoperiods. Biol Reprod 1993; 49: 627-634.
55. Barrell GK, Lapwood KR. Effects of pinealectomy on the secretion of luteinizing hormone, testosterone and prolactin in rams exposed to various lighting regimes. J Endocrinol 1979; 63: 397-405.
56. Jackson GL, Jansen HT. Persistence of a circannual rhythm of plasma prolactin concentrations in ewes exposed to a constant equatorial photoperiod. Biol Reprod 1991; 44: 469-475.
57. Williams HL. The reproductive performance of two British breeds of sheep in contrasting photoperiodic environments. J Agri Sci 1974; 82: 377-381.
58. Arroyo LJ, Gallegos-Sanchez J, Villa-Godoy A, Berruecos JM, Perera G, Valencia J. Reproductive activity of Pelibuey and Suffolk ewes at 19 degrees north latitude. Anim Reprod Sci 2007; 102: 24-30.
59. Malpaux B, Robinson JE, Wayne NL, Karsch FJ. Regulation of the onset of the breeding season of the ewe: importance of long days and of an endogenous reproductive rhythm. J Endocrinol 1989; 122: 269-278.
60. O'Callaghan D, Karsch FJ, Boland MP, Hanrahan JP, Roche JF. Variation in the timing of the reproductive season among breeds of sheep in relation to differences in photoperiodic synchronization of an endogenous rhythm. J Reprod Fertil 1992; 96: 443-452.
61. Sweeney T, Donovan A, Roche JF, O'Callaghan D. Variation in the ability of a long day followed by a short day photoperiod signal to initiate reproductive activity in ewes at different times of the year. J Reprod Fertil 1997; 109: 121-127.
62. Almeida OF, Lincoln GA. Reproductive photorefractoriness in rams and accompanying changes in the patterns of melatonin and prolactin secretion. Biol Reprod 1984; 30: 143-158.
63. Howles CM, Craigon J, Haynes NB. Long-term rhythms of testicular volume and plasma prolactin concentrations in rams reared for 3years in constant photoperiod. J Reprod Fertil 1982; 65: 439-446.
64. Langford GA, Ainsworth L, Marcus GJ, Shrestha JN. Photoperiod entrainment of testosterone, luteinizing hormone, follicle-stimulating hormone, and prolactin cycles in rams in relation to testis size and semen quality. Biol Reprod 1987; 37: 489-499.
65. Vidal A, Medigue C, Malpaux B, Clement F. Endogenous circannual rhythm in luteinizing hormone secretion: insight from signal analysis coupled with mathematical modelling. Philos Transact A Math Phys Eng Sci 2009; 367: 4759-4777.
66. Karsch FJ, Robinson JE, Woodfill CJ, Brown MB. Circannual cycles of luteinizing hormone and prolactin secretion in ewes during prolonged exposure to a fixed photoperiod: evidence for an endogenous reproductive rhythm. Biol Reprod 1989; 41: 1034-1046.
67. Thrun LA, Moenter SM, O'Callaghan D, Woodfill CJ, Karsch FJ. Circannual alterations in the circadian rhythm of melatonin secretion. J Biol Rhythms 1995; 10: 42-54.
68. Karsch FJ, Bittman EL, Robinson JE, Yellon SM, Wayne NL, Olster DH, Kaynard AH. Melatonin and photorefractoriness: loss of response to the melatonin signal leads to seasonal reproductive transitions in the ewe. Biol Reprod 1986; 34: 265-274.
69. Gomez-Brunet A, Santiago-Moreno J, del Campo A, Malpaux B, Chemineau P, Tortonese DJ, Gonzalez-Bulnes A, Lopez-Sebastian A. Endogenous circannual cycles of ovarian activity and changes in prolactin and melatonin secretion in wild and domestic female sheep maintained under a long-day photoperiod. Biol Reprod 2008; 78: 552-562.
70. Ebling FJ, Foster DL. Photoperiod requirements for puberty differ from those for the onset of the adult breeding season in female sheep. J Reprod Fertil 1988; 84: 283-293.
71. O'Callaghan D, Karsch FJ, Boland MP, Roche JF. Role of short days in timing the onset and duration of reproductive activity in ewes under artificial photoperiods. Biol Reprod 1991; 44: 23-28.
72. Foster DL, Ebling FJ, Claypool LE, Woodfill CJ. Cessation of long day melatonin rhythms time puberty in a short day breeder. Endocrinology 1988; 123: 1636-1641.
73. Foster DL, Yellon SM, Ebling FJ, Claypool LE. Are ambient short-day cues necessary for puberty in a short-day breeder? Biol Reprod 1988; 38: 821-829.
74. Chemineau P, Daveau A, Cognie Y, Aumont G, Chesneau D. Seasonal ovulatory activity exists in tropical Creole female goats and Black Belly ewes subjected to a temperate photoperiod. BMC Physiol 2004; 4: 12.
75. Robinson JE, Karsch FJ. Photoperiodic history and a changing melatonin pattern can determine the neuroendocrine response of the ewe to daylength. J Reprod Fertil 1987; 80: 159-165.
76. Ortavant R, Bocquier F, Pelletier J, Ravault JP, Thimonier J, Volland-Nail P. Seasonality of reproduction in sheep and its control by photoperiod. Aust J Biol Sci 1988; 41: 69-85.
77. Chemineau P, Pelletier J, Guerin Y, Colas G, Ravault JP, Toure G, Almeida G, Thimonier J, Ortavant R. Photoperiodic and melatonin treatments for the control of seasonal reproduction in sheep and goats. Reprod Nutr Dev 1988; 28: 409-422.
78. Chemineau P, Malpaux B, Delgadillo JA, Guérin Y, Ravault JP, Thimonier J, Pelletier J. Control of sheep and goat reproduction: use of light and melatonin. Anim Reprod Sci 1992; 30: 157-184.
79. Pellicer-Rubio MT, Leboeuf B, Bernelas D, Forgerit Y, Pougnard JL, Bonne JL, Senty E, Chemineau P. Highly synchronous and fertile reproductive activity induced by the male effect during deep anoestrus in lactating goats subjected to treatment with artificially long days followed by a natural photoperiod. Anim Reprod Sci 2007; 98: 241-258.
80. Robinson JE, Wayne NL, Karsch FJ. Refractoriness to inhibitory day lengths initiates the breeding season of the Suffolk ewe. Biol Reprod 1985; 32: 1024-1030.
81. Wayne NL, Malpaux B, Karsch FJ. How does melatonin code for day length in the ewe: duration of nocturnal melatonin release or coincidence of melatonin with a light-entrained sensitive period? Biol Reprod 1988; 39: 66-75.
82. Woodfill CJ, Wayne NL, Moenter SM, Karsch FJ. Photoperiodic synchronization of a circannual reproductive rhythm in sheep: identification of season-specific time cues. Biol Reprod 1994; 50: 965-976.
83. Khalid M, Jackson GL. Exposure of ewes to long-day photoperiods before the winter solstice can disrupt refractoriness to short days. Anim Reprod Sci 1991; 25: 225-232.
84. Nett TM, Niswender GD. Influence of exogenous melatonin on seasonality of reproduction in sheep. Theriogenology 1982; 17: 645-653.
85. Arendt J, Symons AM, Laud CA, Pryde SJ. Melatonin can induce early onset of the breeding season in ewes. J Endocrinol 1983; 97: 395-400.
86. Robinson JJ, Wigzell S, Aitken RP, Wallace JM, Ireland S, Robertson IS. Daily oral administration of melatonin from March onwards advances by 4months the breeding season of ewes maintained under the ambient photoperiod at 57°N. Anim Reprod Sci 1992; 27: 141-160.
87. Ducker MJ, Thwaites CJ, Bowman JC. Photoperiodism in the ewe. 2. The effects of various patterns of decreasing daylength on the onset of oestrus in clun forest ewes. Anim Prod 1970; 12: 115-123.
88. Ducker MJ, Bowman JC. Photoperiodism in the ewe. 4. A note on the effect on onset of oestrus in clun forest ewes of applying the same decrease in daylength at two different times of the year. Anim Prod 1970; 12: 531-536.
89. Ducker MJ, Bowman JC. Photoperiodism in the ewe. 3. The effects of various patters of increasing daylength on the onset of anoestrus in clun forest ewes. Anim Prod 1970; 12: 465-471.
90. Worthy K, Haresign W. Evidence that the onset of seasonal anoestrus in the ewe may be independent of increasing prolactin concentrations and daylength. J Reprod Fertil 1983; 69: 41-48.
91. Lincoln GA, Clarke IJ, Hut RA, Hazlerigg DG. Characterizing a mammalian circannual pacemaker. Science 2006; 314: 1941-1944.
92. O'Callaghan D, Karsch FJ, Boland MP, Roche JF. What photoperiodic signal is provided by a continuous-release melatonin implant? Biol Reprod 1991; 45: 927-933.
93. Malpaux B, Wayne NL, Karsch FJ. Termination of the breeding season in the Suffolk ewe: involvement of an endogenous rhythm of reproduction. Biol Reprod 1988; 39: 254-263.
94. Malpaux B, Robinson JE, Brown MB, Karsch FJ. Importance of changing photoperiod and melatonin secretory pattern in determining the length of the breeding season in the Suffolk ewe. J Reprod Fertil 1988; 83: 461-470.
95. Nicholls TJ, Goldsmith AR, Dawson A. Photorefractoriness in birds and comparison with mammals. Physiol Rev 1988; 68: 133-176.
96. Bechtold DA, Loudon AS. Hypothalamic thyroid hormones: mediators of seasonal physiology. Endocrinology 2007; 148: 3605-3607.
97. Yoshimura T. Neuroendocrine mechanism of seasonal reproduction in birds and mammals. Anim Sci J 2010; 81: 403-410.
98. Nicholls TJ, Follett BK, Goldsmith AR, Pearson H. Possible homologies between photorefractoriness in sheep and birds: the effect of thyroidectomy on the length of the ewe's breeding season. Reprod Nutr Dev 1988; 28: 375-385.
99. Moenter SM, Woodfill CJ, Karsch FJ. Role of the thyroid gland in seasonal reproduction: thyroidectomy blocks seasonal suppression of reproductive neuroendocrine activity in ewes. Endocrinology 1991; 128: 1337-1344.
100. Dahl GE, Evans NP, Moenter SM, Karsch FJ. The thyroid gland is required for reproductive neuroendocrine responses to photoperiod in the ewe. Endocrinology 1994; 135: 10-15.
101. Billings HJ, Viguie C, Karsch FJ, Goodman RL, Connors JM, Anderson GM. Temporal requirements of thyroid hormones for seasonal changes in LH secretion. Endocrinology 2002; 143: 2618-2625.
102. Parkinson TJ, Follett BK. Effect of thyroidectomy upon seasonality in rams. J Reprod Fertil 1994; 101: 51-58.
103. Parkinson TJ, Follett BK. Thyroidectomy abolishes seasonal testicular cycles of Soay rams. Proc Biol Sci 1995; 259: 1-6.
104. Webster JR, Moenter SM, Woodfill CJ, Karsch FJ. Role of the thyroid gland in seasonal reproduction. II. Thyroxine allows a season-specific suppression of gonadotropin secretion in sheep. Endocrinology 1991; 129: 176-183.
105. O'Callaghan D, Wendling A, Karsch FJ, Roche JF. Effect of exogenous thyroxine on timing of seasonal reproductive transitions in ewes. Biol Reprod 1993; 49: 311-315.
106. Dahl GE, Evans NP, Thrun LA, Karsch FJ. Thyroxine is permissive to seasonal transitions in reproductive neuroendocrine activity in the ewe. Biol Reprod 1995; 52: 690-696.
107. Webster JR, Moenter SM, Barrell GK, Lehman MN, Karsch FJ. Role of the thyroid gland in seasonal reproduction. III. Thyroidectomy blocks seasonal suppression of gonadotropin-releasing hormone secretion in sheep. Endocrinology 1991; 129: 1635-1643.
108. Thrun LA, Dahl GE, Evans NP, Karsch FJ. Time-course of thyroid hormone involvement in the development of anestrus in the ewe. Biol Reprod 1996; 55: 833-837.
109. Thrun LA, Dahl GE, Evans NP, Karsch FJ. Effect of thyroidectomy on maintenance of seasonal reproductive suppression in the ewe. Biol Reprod 1997; 56: 1035-1040.
110. Thrun LA, Dahl GE, Evans NP, Karsch FJ. A critical period for thyroid hormone action on seasonal changes in reproductive neuroendocrine function in the ewe. Endocrinology 1997; 138: 3402-3409.
111. Viguié C, Battaglia DF, Krasa HB, Thrun LA, Karsch FJ. Thyroid hormones act primarily within the brain to promote the seasonal inhibition of luteinizing hormone secretion in the ewe. Endocrinology 1999; 140: 1111-1117.
112. Anderson GM, Hardy SL, Valent M, Billings HJ, Connors JM, Goodman RL. Evidence that thyroid hormones act in the ventromedial preoptic area and the premammillary region of the brain to allow the termination of the breeding season in the ewe. Endocrinology 2003; 144: 2892-2901.
113. Bertrand F, Viguie C, Picard S, Malpaux B. Median eminence dopaminergic activation is critical for the early long-day inhibition of luteinizing hormone secretion in the ewe. Endocrinology 1998; 139: 5094-5102.
114. Thiéry JC, Gayrard V, Le Corre S, Viguié C, Martin GB, Chemineau P, Malpaux B. Dopaminergic control of LH secretion by the A15 nucleus in anoestrous ewes. J Reprod Fertil Suppl 1995; 49: 285-296.
115. Goodman RL, Jansen HT, Billings HJ, Coolen LM, Lehman MN. Neural systems mediating seasonal breeding in the ewe. J Neuroendocrinol 2010; 22: 674-681.
116. Lehman MN, Ladha Z, Coolen LM, Hileman SM, Connors JM, Goodman RL. Neuronal plasticity and seasonal reproduction in sheep. Eur J Neurosci 2010; 32: 2152-2164.
117. Tillet Y, Thibault J. Catecholamine-containing neurons in the sheep brainstem and diencephalon: immunohistochemical study with tyrosine hydroxylase (TH) and dopamine-beta-hydroxylase (DBH) antibodies. J Comp Neurol 1989; 290: 69-104.
118. Lincoln GA, Maeda KI. Reproductive effects of placing micro-implants of melatonin in the mediobasal hypothalamus and preoptic area in rams. J Endocrinol 1992; 132: 201-215.
119. Malpaux B, Daveau A, Maurice F, Gayrard V, Thiery JC. Short-day effects of melatonin on luteinizing hormone secretion in the ewe: evidence for central sites of action in the mediobasal hypothalamus. Biol Reprod 1993; 48: 752-760.
120. Lincoln GA, Maeda K. Effects of placing micro-implants of melatonin in the mediobasal hypothalamus and preoptic area on the secretion of prolactin and beta-endorphin in rams. J Endocrinol 1992; 134: 437-448.
121. Malpaux B, Skinner DC, Maurice F. The ovine pars tuberalis does not appear to be targeted by melatonin to modulate luteinizing hormone secretion, but may be important for prolactin release. J Neuroendocrinol 1995; 7: 199-206.
122. de Reviers MM, Ravault JP, Tillet Y, Pelletier J. Melatonin binding sites in the sheep pars tuberalis. Neurosci Lett 1989; 100: 89-93.
123. Bittman EL, Weaver DR. The distribution of melatonin binding sites in neuroendocrine tissues of the ewe. Biol Reprod 1990; 113: 986-993.
124. Helliwell RJA, Williams LM. Melatonin binding sites in the ovine brain and pituitary: characterization during the oestrous cycle. J Neuroendocrinol 1992; 4: 287-294.
125. Malpaux B, Daveau A, Maurice-Mandon F, Duarte G, Chemineau P. Evidence that melatonin acts in the premammillary hypothalamic area to control reproduction in the ewe: presence of binding sites and stimulation of luteinizing hormone secretion by in situ microimplant delivery. Endocrinology 1998; 139: 1508-1516.
126. Migaud M, Daveau A, Malpaux B. MTNR1A melatonin receptors in the ovine premammillary hypothalamus: day-night variation in the expression of the transcripts. Biol Reprod 2005; 72: 393-398.
127. Cogé F, Guenin SP, Fery I, Migaud M, Devavry S, Slugocki C, Legros C, Ouvry C, Cohen W, Renault N, Nosjean O, Malpaux B, Delagrange P, Boutin JA. The end of a myth: cloning and characterization of the ovine melatonin MT(2) receptor. Br J Pharmacol 2009; 158: 1248-1262.
128. Masson-Pevet M, George D, Kalsbeek A, Saboureau M, Lakhdar-Ghazal N, Pevet P. An attempt to correlate brain areas containing melatonin-binding sites with rhythmic functions: a study in five hibernator species. Cell Tissue Res 1994; 278: 97-106.
129. 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: 144-153.
130. Maywood ES, Bittman EL, Hastings MH. Lesions of the melatonin- and androgen-responsive tissue of the dorsomedial nucleus of the hypothalamus block the gonadal response of male Syrian hamsters to programmed infusions of melatonin. Biol Reprod 1996; 54: 470-477.
131. Weaver DR, Reppert SM. Melatonin receptors are present in the ferret pars tuberalis and pars distalis, but not in brain. Endocrinology 1990; 127: 2607-2609.
132. Lincoln GA, Clarke IJ. Photoperiodically-induced cycles in the secretion of prolactin in hypothalamo-pituitary disconnected rams: evidence for translation of the melatonin signal in the pituitary gland. J Neuroendocrinol 1994; 6: 251-260.
133. Lincoln GA, Clarke IJ. Evidence that melatonin acts in the pituitary gland through a dopamine-independent mechanism to mediate effects of daylength on the secretion of prolactin in the ram. J Neuroendocrinol 1995; 7: 637-643.
134. Lincoln GA, Clarke IJ. Refractoriness to a static melatonin signal develops in the pituitary gland for the control of prolactin secretion in the ram. Biol Reprod 1997; 57: 460-467.
135. Lincoln GA, Clarke IJ. Absence of photoperiodic modulation of gonadotrophin secretion in HPD rams following chronic pulsatile infusion of GnRH. J Neuroendocrinol 1998; 10: 461-471.
136. Lincoln GA. Neuroendocrine regulation of seasonal gonadotrophin and prolactin rhythms: lessons from the Soay ram model. Reprod Suppl 2002; 59: 131-147.
137. Williams LM, Lincoln GA, Mercer JG, Barrett P, Morgan PJ, Clarke IJ. Melatonin receptors in the brain and pituitary gland of hypothalamo-pituitary disconnected Soay rams. J Neuroendocrinol 1997; 9: 639-643.
138. Skinner DC, Evans NP, Delaleu B, Goodman RL, Bouchard P, Caraty A. The negative feedback actions of progesterone on gonadotropin-releasing hormone secretion are transduced by the classical progesterone receptor. Proc Natl Acad Sci USA 1998; 95: 10978-10983.
139. Caraty A, Skinner DC. Progesterone priming is essential for the full expression of the positive feedback effect of estradiol in inducing the preovulatory gonadotropin-releasing hormone surge in the ewe. Endocrinology 1999; 140: 165-170.
140. Smith JT. Sex steroid control of hypothalamic Kiss1 expression in sheep and rodents: comparative aspects. Peptides 2009; 30: 94-102.
141. Clarke IJ, Smith JT, Caraty A, Goodman RL, Lehman MN. Kisspeptin and seasonality in sheep. Peptides 2009; 30: 154-163.
142. Caraty A, Franceschini I, Hoffman GE. Kisspeptin and the preovulatory gonadotrophin-releasing hormone/luteinising hormone surge in the ewe: basic aspects and potential applications in the control of ovulation. J Neuroendocrinol 2010; 22: 710-715.
143. Goodman RL, Holaskova I, Nestor CC, Connors JM, Billings HJ, Valent M, Lehman MN, Hileman SM. Evidence that the arcuate nucleus is an important site of progesterone negative feedback in the ewe. Endocrinology 2011; 152: 3451-3460.
144. Tortonese DJ, Lincoln GA. Effects of melatonin in the mediobasal hypothalamus on the secretion of gonadotrophins in sheep: role of dopaminergic pathways. J Endocrinol 1995; 146: 543-552.
145. Lincoln GA. Effects of placing micro-implants of melatonin in the pars tuberalis, pars distalis and the lateral septum of the forebrain on the secretion of FSH and prolactin, and testicular size in rams. J Endocrinol 1994; 142: 267-276.
146. Malpaux B, Daveau A, Maurice F, Locatelli A, Thiery JC. Evidence that melatonin binding sites in the pars tuberalis do not mediate the photoperiodic actions of melatonin on LH and prolactin secretion in ewes. J Reprod Fertil 1994; 101: 625-632.
147. Malpaux B, Migaud M, Tricoire H, Chemineau P. Biology of mammalian photoperiodism and the critical role of the pineal gland and melatonin. J Biol Rhythms 2001; 16: 336-347.
148. Page RB. Pituitary blood flow. Am J Physiol Endocrinol Metab 1982; 243: E427-E442.
149. Ciofi P, Garret M, Lapirot O, Lafon P, Loyens A, Prevot V, Levine JE. Brain-endocrine interactions: a microvascular route in the mediobasal hypothalamus. Endocrinology 2009; 150: 5509-5519.
150. Rodriguez EM, Blazquez JL, Guerra M. The design of barriers in the hypothalamus allows the median eminence and the arcuate nucleus to enjoy private milieus: the former opens to the portal blood and the latter to the cerebrospinal fluid. Peptides 2010; 31: 757-776.
151. Guerra M, Blazquez JL, Peruzzo B, Pelaez B, Rodriguez S, Toranzo D, Pastor F, Rodriguez EM. Cell organization of the rat pars tuberalis. Evidence for open communication between pars tuberalis cells, cerebrospinal fluid and tanycytes. Cell Tissue Res 2010; 339: 359-381.
152. Mullier A, Bouret SG, Prevot V, Dehouck B. Differential distribution of tight junction proteins suggests a role for tanycytes in blood-hypothalamus barrier regulation in the adult mouse brain. J Comp Neurol 2010; 518: 943-962.
153. Morgan PJ, Hazlerigg DG. Photoperiodic signalling through the melatonin receptor turns full circle. J Neuroendocrinol 2008; 20: 820-826.
154. Hazlerigg DG, Andersson H, Johnston JD, Lincoln G. Molecular characterization of the long-day response in the Soay sheep, a seasonal mammal. Curr Biol 2004; 14: 334-339.
155. Dupré SM, Miedzinska K, Duval CV, Yu L, Goodman RL, Lincoln GA, Davis JR, McNeilly AS, Burt DD, Loudon AS. Identification of Eya3 and TAC1 as long-day signals in the sheep pituitary. Curr Biol 2010; 20: 829-835.
156. Dardente H. Does a melatonin-dependent circadian oscillator in the pars tuberalis drive prolactin seasonal rhythmicity? J Neuroendocrinol 2007; 19: 657-666.
157. Dupré SM. Encoding and decoding photoperiod in the mammalian pars tuberalis. Neuroendocrinology 2011; 94: 101-112.
158. 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: 1147-1152.
159. Yoshimura T, Yasuo S, Watanabe M, Iigo M, Yamamura T, Hirunagi K, Ebihara S. Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature 2003; 426: 178-181.
160. 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 response. Nature 2008; 452: 317-322.
161. Watanabe M, Yasuo S, Watanabe T, Yamamura T, Nakao N, Ebihara S, Yoshimura T. Photoperiodic regulation of type 2 deiodinase gene in Djungarian hamster: possible homologies between avian and mammalian photoperiodic regulation of reproduction. Endocrinology 2004; 145: 1546-1549.
162. Revel FG, Saboureau M, Pevet P, Mikkelsen JD, Simonneaux V. Melatonin regulates type 2 deiodinase gene expression in the Syrian hamster. Endocrinology 2006; 147: 4680-4687.
163. 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.
164. Yasuo S, Yoshimura T, Ebihara S, Korf HW. Melatonin transmits photoperiodic signals through the MT1 melatonin receptor. J Neurosci 2009; 29: 2885-2889.
165. Klosen P, Bienvenu C, Demarteau O, Dardente H, Guerrero H, Pevet P, Masson-Pevet M. The mt1 melatonin receptor and RORbeta receptor are co-localized in specific TSH-immunoreactive cells in the pars tuberalis of the rat pituitary. J Histochem Cytochem 2002; 50: 1647-1657.
166. Dardente H, Klosen P, Pevet P, Masson-Pevet M. MT1 melatonin receptor mRNA expressing cells in the pars tuberalis of the European hamster: effect of photoperiod. J Neuroendocrinol 2003; 15: 778-786.
167. 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: 18238-18242.
168. Yasuo S, Yoshimura T, Ebihara S, Korf HW. Photoperiodic control of TSH-beta expression in the mammalian pars tuberalis has different impacts on the induction and suppression of the hypothalamo-hypopysial gonadal axis. J Neuroendocrinol 2010; 22: 43-50.
169. Hanon EA, Routledge K, Dardente H, Masson-Pevet M, Morgan PJ, Hazlerigg DG. Effect of photoperiod on the thyroid-stimulating hormone neuroendocrine system in the European hamster (Cricetus cricetus). J Neuroendocrinol 2010; 22: 51-55.
170. Ross AW, Helfer G, Russell L, Darras VM, Morgan PJ. Thyroid hormone signalling genes are regulated by photoperiod in the hypothalamus of f344 rats. PLoS ONE 2011; 6: e21351.
171. Bockmann J, Bockers TM, Winter C, Wittkowski W, Winterhoff H, Deufel T, Kreutz MR. Thyrotropin expression in hypophyseal pars tuberalis-specific cells is 3, 5, 3'-triiodothyronine, thyrotropin-releasing hormone, and pit-1 independent. Endocrinology 1997; 138: 1019-1028.
172. Dupré SM, Burt DW, Talbot R, Downing A, Mouzaki D, Waddington D, Malpaux B, Davis JR, Lincoln GA, Loudon AS. Identification of melatonin-regulated genes in the ovine pituitary pars tuberalis, a target site for seasonal hormone control. Endocrinology 2008; 149: 5527-5539.
173. Dardente H, Menet JS, Poirel VJ, Streicher D, Gauer F, Vivien-Roels B, Klosen P, Pevet P, Masson-Pevet M. Melatonin induces Cry1 expression in the pars tuberalis of the rat. Mol Brain Res 2003; 114: 101-106.
174. Tournier BB, Dardente H, Simonneaux V, Vivien-Roels B, Pevet P, Masson-Pevet M, Vuillez P. Seasonal variations of clock gene expression in the suprachiasmatic nuclei and pars tuberalis of the European hamster (Cricetus cricetus). Eur J Neurosci 2007; 25: 1529-1536.
175. Unfried C, Burbach G, Korf HW, von Gall C. Melatonin receptor 1-dependent gene expression in the mouse pars tuberalis as revealed by cDNA microarray analysis and in situ hybridization. J Pineal Res 2010; 48: 148-156.
176. Lincoln G, Messager S, Andersson H, Hazlerigg D. Temporal expression of seven clock genes in the suprachiasmatic nucleus and the pars tuberalis of the sheep: evidence for an internal coincidence timer. Proc Natl Acad Sci USA 2002; 99: 13890-13895.
177. Hazlerigg D, Loudon A. New insights into ancient seasonal life timers. Curr Biol 2008; 18: R795-R804.
178. Fustin JM, Dardente H, Wagner GC, Carter DA, Johnston JD, Lincoln GA, Hazlerigg DG. Egr1 involvement in evening gene regulation by melatonin. FASEB J 2009; 23: 764-773.
179. Dardente H, Wyse CA, Birnie MJ, Dupré SM, Loudon AS, Lincoln GA, Hazlerigg DG. A molecular switch for photoperiod responsiveness in mammals. Curr Biol 2010; 20: 2193-2198.
180. Masumoto KH, Ukai-Tadenuma M, Kasukawa T, Nagano M, Uno KD, Tsujino K, Horikawa K, Shigeyoshi Y, Ueda HR. Acute induction of Eya3 by late-night light stimulation triggers TSHbeta expression in photoperiodism. Curr Biol 2010; 20: 2199-2206.
181. Bünning E. 'Die endonome tagesrhythmik als grundlage der photoperiodischen reaktion'. Ber Deut Bot Ges 1936; 54: 590-607.
182. Pittendrigh CS, Minis DH. The entrainment of circadian oscillations by light and their role as photoperiodic clocks. Am Nat 1964; 98: 261-299.
183. Pittendrigh CS. Circadian surfaces and the diversity of possible roles of circadian organization in photoperiodic induction. Proc Natl Acad Sci USA 1972; 69: 2734-2737.
184. Sato TK, Yamada RG, Ukai H, Baggs JE, Miraglia LJ, Kobayashi TJ, Welsh DK, Kay SA, Ueda HR, Hogenesch JB. Feedback repression is required for mammalian circadian clock function. Nat Genet 2006; 38: 312-319.
185. Fustin JM, O'Neill JS, Hastings MH, Hazlerigg DG, Dardente H. Cry1 circadian phase in vitro: wrapped up with an E-box. J Biol Rhythms 2009; 24: 16-24.
186. Ukai-Tadenuma M, Yamada RG, Xu H, Ripperger JA, Liu AC, Ueda HR. Delay in feedback repression by cryptochrome 1 is required for circadian clock function. Cell 2011; 144: 268-281.
187. Reiter RJ. Pineal control of a seasonal reproductive rhythm in male golden hamsters exposed to natural daylight and temperature. Endocrinology 1973; 92: 423-430.
188. Reiter RJ. Evidence for refractoriness of the pituitary-gonadal axis to the pineal gland in golden hamsters and its possible implications in annual reproductive rhythms. Anat Rec 1972; 173: 365-371.
189. Turek FW, Losee SH. Photoperiodic inhibition of the reproductive system: a prerequisite for the induction of the refractory period in hamsters. Biol Reprod 1979; 20: 611-616.
190. Turek FW, Elliott JA, Alvis JD, Menaker M. Effect of prolonged exposure to nonstimulatory photoperiods on the activity of the neuroendocrine-testicular axis of golden hamsters. Biol Reprod 1975; 13: 475-481.
191. Zucker I, Morin LP. Photoperiodic influences on testicular regression, recrudescence and the induction of scotorefractoriness in male golden hamsters. Biol Reprod 1977; 17: 493-498.
192. Czyba JC, Girod C, Durand N. On epiphyso-hypophysial antagonism and seasonal spermatogenesis variations in the gold hamster (Mesocricetus auratus). C R Seances Soc Biol Fil 1964; 158: 742-745.
193. Reiter RJ. Exogenous and endogenous control of the annual reproductive cycle in the male golden hamster: participation of the pineal gland. J Exp Zool 1975; 191: 111-120.
194. Stetson MH, Watson-Whitmyre M, Matt KS. Termination of photorefractoriness in golden hamsters-photoperiodic requirements. J Exp Zool 1977; 202: 81-88.
195. Bittman EL, Zucker I. Photoperiodic termination of hamster refractoriness: participation of the pineal gland. Biol Reprod 1981; 24: 568-572.
196. Reiter RJ, Petterborg LJ, Philo RC. Refractoriness to the antigonadotrophic effects of melatonin in male hamsters and its interruption by exposure of the animals to long daily photoperiods. Life Sci 1979; 25: 1571-1576.
197. Gaston S, Menaker M. Photoperiodic control of hamster testis. Science 1967; 158: 925-928.
198. Elliott JA. Circadian rhythms and photoperiodic time measurement in mammals. Fed Proc 1976; 35: 2339-2346.
199. Vitaterna MH, Turek FW. Photoperiodic responses differ among inbred strains of golden hamsters (Mesocricetus auratus). Biol Reprod 1993; 49: 496-501.
200. Hoffmann K. Effects of short photoperiods on puberty, growth and moult in the Djungarian hamster (Phodopus sungorus). J Reprod Fertil 1978; 54: 29-35.
201. Hoffmann K, Kuderling I. Pinealectomy inhibits stimulation of testicular development by long photoperiods in a hamster (Phodopus sungorus). Experientia 1975; 31: 122-123.
202. Niklowitz P, Lerchl A, Nieschlag E. Photoperiodic responses in Djungarian hamsters (Phodopus sungorus): importance of light history for pineal and serum melatonin profiles. Biol Reprod 1994; 51: 714-724.
203. Kauffman AS, Freeman DA, Zucker I. Termination of neuroendocrine refractoriness to melatonin in Siberian hamsters (Phodopus sungorus). J Neuroendocrinol 2003; 15: 191-196.
204. 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: 3608-3617.
205. Freeman DA, Teubner BJ, Smith CD, Prendergast BJ. Exogenous T3 mimics long day lengths in Siberian hamsters. Am J Physiol Regul Integr Comp Physiol 2007; 292: R2368-R2372.
206. Murphy M, Jethwa PH, Warner A, Barrett PN, Nilaweera KN, Brameld JM, Ebling FJP. Effects of manipulating hypothalamic tri-iodothyronine concentrations on seasonal body weight and torpor cycles in Siberian hamsters. Endocrinology, in press.
207. Lincoln GA, Johnston JD, Andersson H, Wagner G, Hazlerigg DG. Photorefractoriness in mammals: dissociating a seasonal timer from the circadian-based photoperiod response. Endocrinology 2005; 146: 3782-3790.
208. Bockers TM, Bockmann J, Salem A, Niklowitz P, Lerchl A, Huppertz M, Wittkowski W, Kreutz MR. Initial expression of the common alpha-chain in hypophyseal pars tuberalis-specific cells in spontaneous recrudescent hamsters. Endocrinology 1997; 138: 4101-4108.
209. Visser WE, Friesema EC, Visser TJ. Minireview: thyroid hormone transporters: the knowns and the unknowns. Mol Endocrinol 2011; 25: 1-14.
210. Kokoeva MV, Yin H, Flier JS. Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 2005; 310: 679-683.
211. Bennett L, Yang M, Enikolopov G, Iacovitti L. Circumventricular organs: a novel site of neural stem cells in the adult brain. Mol Cell Neurosci 2009; 41: 337-347.
212. Hazlerigg DG, Lincoln GA. Hypothesis: cyclical histogenesis is the basis of circannual timing. J Biol Rhythms 2011; 26: 471-485.
213. Migaud M, Batailler M, Segura S, Duittoz A, Franceschini I, Pillon D. Emerging new sites for adult neurogenesis in the mammalian brain: a comparative study between the hypothalamus and the classical neurogenic zones. Eur J Neurosci 2010; 32: 2042-2052.
214. Ebling FJ, Barrett P. The regulation of seasonal changes in food intake and body weight. J Neuroendocrinol 2008; 20: 827-833.
215. Nakao N, Ono H, Yoshimura T. Thyroid hormones and seasonal reproductive neuroendocrine interactions. Reproduction 2008; 136: 1-8.
216. Chalivoix S, Malpaux B, Dufourny L. Relationship between polysialylated neural cell adhesion molecule and beta-endorphin- or gonadotropin releasing hormone-containing neurons during activation of the gonadotrope axis in short daylength in the ewe. Neuroscience 2010; 169: 1326-1336.
217. Clarkson J, Herbison AE. Oestrogen, kisspeptin, GPR54 and the pre-ovulatory luteinising hormone surge. J Neuroendocrinol 2009; 21: 305-311.
218. Kauffman AS. Gonadal and nongonadal regulation of sex differences in hypothalamic Kiss1 neurones. J Neuroendocrinol 2010; 22: 682-691.
219. Revel FG, Saboureau M, Masson-Pevet M, Pevet P, Mikkelsen JD, Simonneaux V. Kisspeptin mediates the photoperiodic control of reproduction in hamsters. Curr Biol 2006; 16: 1730-1735.
220. Smith JT, Clay CM, Caraty A, Clarke IJ. KiSS-1 messenger ribonucleic acid expression in the hypothalamus of the ewe is regulated by sex steroids and season. Endocrinology 2007; 148: 1150-1157.
221. Smith JT, Coolen LM, Kriegsfeld LJ, Sari IP, Jaafarzadehshirazi MR, Maltby M, Bateman K, Goodman RL, Tilbrook AJ, Ubuka T, Bentley GE, Clarke IJ, Lehman MN. Variation in kisspeptin and RFamide-related peptide (RFRP) expression and terminal connections to gonadotropin-releasing hormone neurons in the brain: a novel medium for seasonal breeding in the sheep. Endocrinology 2008; 149: 5770-5782.
222. Li D, Mitchell D, Luo J, Yi Z, Cho SG, Guo J, Li X, Ning G, Wu X, Liu M. Estrogen regulates KiSS1 gene expression through estrogen receptor alpha and SP protein complexes. Endocrinology 2007; 148: 4821-4828.
223. Naar AM, Boutin JM, Lipkin SM, Yu VC, Holloway JM, Glass CK, Rosenfeld MG. The orientation and spacing of core DNA-binding motifs dictate selective transcriptional responses to three nuclear receptors. Cell 1991; 65: 1267-1279.
224. Vasudevan N, Davidkova G, Zhu YS, Koibuchi N, Chin WW, Pfaff D. Differential interaction of estrogen receptor and thyroid hormone receptor isoforms on the rat oxytocin receptor promoter leads to differences in transcriptional regulation. Neuroendocrinology 2001; 74: 309-324.
225. Yamamura T, Yasuo S, Hirunagi K, Ebihara S, Yoshimura T. T3 implantation mimics photoperiodically reduced encasement of nerve terminals by glial processes in the median eminence of Japanese quail. Cell Tissue Res 2006; 324: 175-179.