Hypothalamic control of seasonal changes in food intake and body weight

Frontiers in Neuroendocrinology

Volumn 37, Issue , 2015, Pages 97-107

  Ebling, Francis J P ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Appetite; Body weight; Food intake; Pars tuberalis; Photoperiod; Plasticity; Season; Tanycyte; Thyroid hormone

Indexed keywords

AGOUTI RELATED PROTEIN; COCAINE AND AMPHETAMINE REGULATED TRANSCRIPT PEPTIDE; MELANIN CONCENTRATING HORMONE; MELANOCORTIN; NEUROMEDIN U; NEUROPEPTIDE Y; PROTIRELIN; RETINOIC ACID; THYROID HORMONE;

BODY WEIGHT; CIRCADIAN RHYTHM; FEEDING BEHAVIOR; FOOD INTAKE; HORMONE ACTION; HYPOTHALAMUS FUNCTION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROENDOCRINE SYSTEM; NEUROMODULATION; NONHUMAN; PHOTOPERIODICITY; PHOTOSTIMULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REPRODUCTIVE BEHAVIOR; REVIEW; SEASONAL VARIATION; TANYCYTE; ANIMAL; EATING; HUMAN; HYPOTHALAMUS; NEUROSECRETION; PHYSIOLOGY; SEASON;

ANIMALS; APPETITE REGULATION; BODY WEIGHT; EATING; HUMANS; HYPOTHALAMUS; NEUROSECRETORY SYSTEMS; SEASONS; THYROID HORMONES;

EID: 84928685092     PISSN: 00913022     EISSN: 10956808     Source Type: Journal    
DOI: 10.1016/j.yfrne.2014.10.003     Document Type: Review

References (158)

1. Anderson G.M., Hardy S.L., Valent M., Billings H.J., Connors J.M., Goodman R.L. 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.
2. Arnold W., Ruf T., Frey-Roos F., Bruns U. Diet-independent remodeling of cellular membranes precedes seasonally changing body temperature in a hibernator. PLoS ONE 2011, 6:e18641. doi: 18610.11371/journal.pone.0018641.
3. Balland E., Dam J., Langlet F., Caron E., Steculorum S., Messina A., Rasika S., Falluel-Morel A., Anouar Y., Dehouck B., Trinquet E., Jockers R., Bouret S.G., Prévot V. Hypothalamic tanycytes are an ERK-gated conduit for leptin into the brain. Cell Metab. 2014, 19:293-301.
4. Bamshad M., Aoki V.T., Adkison M.G., Warren W.S., Bartness T.J. Central nervous system origins of the sympathetic nervous system outflow to white adipose tissue. Am. J. Physiol. 1998, 275:291-299.
5. Bamshad M., Song C.K., Bartness T.J. CNS origins of the sympathetic nervous system outflow to brown adipose tissue. Biol. Reprod. 1999, 290:R1569-R1578.
6. Barrett P., Ivanova E., Graham E.S., Ross A.W., Wilson D., Ple H., Mercer J.G., Ebling F.J.P., Schuhler S., Dupre S.M., Loudon A.S.I., Morgan P.J. Photoperiodic regulation of GPR50, Nestin and CRBP1 in tanycytes of the third ventricle ependymal layer of the Siberian hamster. J Endocrinol 2006, 191:687-698.
7. Barrett P., Ebling F.J.P., Schuhler S., Wilson D., Ross A.W., Warner A., Jethwa P.H., Boelen A., Visser T.J., Ozanne D.M., Archer Z.A., Mercer J.G., Morgan P.J. Hypothalamic thyroid hormone catabolism acts as a gatekeeper for the seasonal control of body weight and reproduction. Endocrinology 2007, 148:3608-3617.
8. Bartness T.J. Short day-induced depletion of lipid stores is fat pad- and gender-specific in Siberian hamsters. Physiol. Behav. 1995, 58:539-550.
9. Bartness T.J., Hamilton J.M., Wade G.N., Goldman B.D. Regional differences in fat pad responses to short days in Siberian hamsters. Am. J. Physiol. 1989, 257:R1533-R1540.
10. Bartness T.J., Powers J.B., Hastings M.H., Bittman E.L., Goldman B.D. The timed infusion paradigm for melatonin delivery: what has it taught us about the melatonin signal, its reception and the photoperiodic control of seasonal responses. J. Pineal Res. 1993, 15:161-190.
11. Bartness T.J., Demas G.E., Song C.K. Seasonal changes in adiposity: the roles of the photoperiod, melatonin and other hormones, and sympathetic nervous system. Exp. Biol. Med. 2002, 227:363-376.
12. Bartness T.J., Liu Y., Shrestha Y.B., Ryu V. Neural innervation of white adipose tissue and the control of lipolysis. Front. Neuroendocrinol. 2014, 35:473-493.
13. Batailler M., Droguerre M., Baroncini M., Fontaine C., Prevot V., Migaud M. DCX-expressing cells in the vicinity of the hypothalamic neurogenic niche: a comparative study between mouse, sheep, and human tissues. J. Comp. Neurol. 2014, 522:1966-1982.
14. Bechtold D.A., Loudon A.S.I. Hypothalamic thyroid hormones: mediators of seasonal physiology. Endocrinology 2007, 148:3605-3607.
15. Bechtold D.A., Sidibe A., Saer B.R., Hand L.E., Ivanova E., Darras V.M., Dam J., Jockers R., Luckman S.M., Loudon A.S.I. A role for the melatonin-related receptor GPR50 in leptin signaling, adaptive thermogenesis, and torpor. Curr. Biol. 2012, 22:70-77.
16. Bernal J. Thyroid hormone receptors in brain development and function. Nat. Clin. Practise Endocrinol. Metab. 2007, 3:249-259.
17. Bittman E.L. The sites and consequences of melatonin binding in mammals. Am. Zool. 1993, 33:200-211.
18. Bittman E.L., Weaver D.R. The distribution of melatonin binding sites in neuroendocrine tissues of the ewe. Biol. Reprod. 1990, 43:986-993.
19. Bockers T.M., Niklowitz P., Bockmann J., Fauteck J.D., Wittkowski W., Kreutz M.R. Daily melatonin injections induce cytological changes in pars tuberalis-specific cells similar to short photoperiod. J. Neuroendocrinol. 1995, 7:607-613.
20. Bockmann J., Bockers T.M., Vennemann B., Niklowitz P., Muller J., Wittkowski W., Sabel B.A., Kreutz M.R. Short photoperiod-dependent down-regulation of thyrotropin-α and -β in hamster pars tuberalis-specific cells is prevented by pinealectomy. Endocrinology 1996, 137:1804-1813.
21. Bolborea M., Laran-Chich M.P., Rasri K., Govitrapong P., Simmoneaux V., Pevet P., Steinlechner S., Klosen P. Melatonin controls photoperiodic changes in tanycyte vimentin and neural cell adhesion molecule expression in the Djungarian hamster (Phodopus sungorus). Endocrinology 2011, 152:3871-3883.
22. Bonnefond C., Monnerie R., Richard J.P., Martinet L. Melatonin and the circadian clock in mink: effects of daily injections of melatonin on circadian rhythm of locomotor activity and autoradiographic localization of melatonin binding sites. J. Neuroendocrinol. 1993, 5:241-246.
23. Brawer J.R., Gustafsson A.W. Changes in the fine structure of tanycytes during the annual reproductive cycle of the male little brown bat Myotis lucifugus lucifugus. Endocrinology 1979, 154:497-508.
24. Clarke I.J. Interface between Metabolic balance and Reproduction in Ruminants: focus on hypothalamus and pituitary. Horm. Behav. 2014, 66:15-40.
25. Clarke I.J., Rao A., Chilliard Y., Delavaud C., Lincoln G.A. Photoperiod effects on gene expression for hypothalamic appetite-regulating peptides and food intake in the ram. Am. J. Physiol. 2002, 284:R101-R115.
26. Coppola A., Liu Z.W., Andrews Z., Paradis E., Roy M.C., Friedman J.M., Ricquier D., Richard D., Horvath T.L., Gao X.B. A central thermogenic-like mechanism in feeding regulation: an interplay between arcuate nucleus T3 and UCP2. Cell Metab. 2007, 5:21-33.
27. Coskun T., Bina H.A., Schneider M.A., Dunbar J.D., Hu C.C., Chen Y., Moller D.E., Kharitonenkov A. Fibroblast growth factor 21 corrects obesity in mice. Endocrinology 2008, 149:6018-6027.
28. Dardente H., Wyse C.A., Birnie M.J., Dupre S.M., Loudon A.S.I., Lincoln G.A., Hazlerigg D.G. A molecular switch for photoperiod responsiveness in mammals. Curr. Biol. 2010, 20:2193-2198.
29. Duncan M.J., Goldman B.D. Hormonal regulation of the annual pelage color cycle in the Djungarian hamster, Phodopus sungorus sungorus. II: Role of prolactin. J. Exp. Zool. 1984, 230:97-103.
30. Dupre S., Burt D.W., Talbot R., Downing A., Mouzaki D., Waddington D., Malpaux B., Davis J.R., Lincoln G.A., Loudon A.S.I. Identification of melatonin-regulated genes in the ovine pituitary pars tuberalis, a target site for seasonal hormone control. Endocrinology 2008, 149:5527-5539.
31. Dupre S., Miedzinska K., Duval C.V., Yu L., Goodman R.L., Lincoln G.A., Davis J.R., McNeilly A.S., Burt D.W., Loudon A.S.I. Identification of Eya3 and TAC1 as long-day signals in the sheep pituitary. Curr. Biol. 2010, 20:829-835.
32. Ebling, F.J.P., 1984. Central mechanisms in the control of seasonal breeding n the Soay ram. PhD Thesis, University of Edinburgh.
33. Ebling F.J.P. The role of glutamate in the photic regulation of the suprachiasmatic nucleus. Prog. Neurobiol. 1996, 50:109-132.
34. Ebling F.J.P., Arthurs O.J., Turney B.W., Cronin A.S. Seasonal neuroendocrine rhythms in the male Siberian hamster persist following monosodium glutamate-induced lesions of the arcuate nucleus in the neonatal period. J Neuroendocrinol 1998, 10:701-712.
35. Ebling F.J.P. Photoperiodic regulation of puberty in seasonal species. Mol. Cell. Endocrinol. 2010, 324:95-101.
36. Ebling F.J.P. On the value of seasonal mammals for identifying mechanisms underlying the control of food intake and body weight. Horm. Behav. 2014, 66:55-61.
37. Ebling F.J.P., Barrett P. The regulation of seasonal changes in food intake and body weight. J. Neuroendocrinol. 2008, 20:827-833.
38. Ebling F.J.P., Lincoln G.A. β-endorphin secretion in rams related to season and photoperiod. Endocrinology 1987, 120:809-818.
39. Ebling F.J.P., Wilson D., Wilson D., Wood J., Hughes D., Mercer J.G., Morgan P.J., Barrett P. Localisation of the TRH secretory system in the Siberian hamster. J. Neuroendocrinol. 2008, 20:576-586.
40. Follett B.K., Nicholls T.J. Influences of thyroidectomy and thyroxine replacement on photoperiodically controlled reproduction in quail. J. Endocrinol. 1985, 107:211-221.
41. Foster, R.G., Kreitzman, L., 2010. Seasons of Life: The Biological Rhythms That Enable Living Things to Thrive and Survive. Yale University Press.
42. Frayling C., Britton R., Dale N. ATP-mediated glucosensing by hypothalamic tanycytes. J. Physiol. 2011, 589:2275-2286.
43. Freeman D.A., Teubner B.J.W., Smith C.D., Prendergast B.J. Exogenous T3 mimics long day lengths in Siberian hamsters. Am. J. Physiol. 2007, 292:R2368-R2372.
44. Garcia M.A., Carrasco M., Godoy A., Reinicke K., Montecinos V.P., Aguayo L.G., Tapia J.C., Vera J.C., Nualart F. Elevated expression of glucose transporter-1 in hypothalamic ependymal cells not involved in the formation of the brain-cerebrospinal fluid barrier. J. Cell. Biochem. 2001, 80:491-503.
45. García M., Millán C., Balmaceda-Aguilera C., Castro T., Pastor P., Montecinos H., Reinicke K., Zúñiga F., Vera J.C., Oñate S.A., Nualart F. Hypothalamic ependymal-glial cells express the glucose transporter GLUT2, a protein involved in glucose sensing. J. Neurochem. 2003, 86:709-724.
46. Goldsmith A.R., Nicholls T.J. Thyroidectomy prevents the development of photorefractoriness and the associated rise in plasma prolactin in starlings. Gen. Comp. Endocrinol. 1984, 54:256-263.
47. Gooley J.J., Lu J., Chou T.C., Scammell T.E., Saper C.B. Melanopsin in cells of origin of the retinohypothalamic tract. Nat. Neurosci. 2001, 4. 1165-1165.
48. Graham E.S., Webster C.A., Hazlerigg D.G., Morgan P.J. Evidence for the biosynthesis of a prolactin-releasing factor from the ovine pars tuberalis, which is distinct from thyrotropin-releasing hormone. J. Neuroendocrinol. 2002, 14:945-954.
49. Graham E.S., Turnbull Y., Fotheringham P., Nilaweera K.N., Mercer J.G., Morgan P.J., Barrett P. Neuromedin U and Neuromedin U receptor-2 expression in the mouse and rat hypothalamus: effects of nutritional status. J. Neurochem. 2003, 87:1165-1173.
50. Grubb P., Jewell P.A. The rut and the occurrence of oestrus in the soay sheep on St Kilda. J. Reprod. Fertil. Suppl. 1973, 19:491-502.
51. Haan N., Goodman T., Najdi-Samiei A., Stratford C.M., Rice R., El Agha E., Bellusci S., Hajihosseini M.K. Fgf10-expressing tanycytes add new neurons to the appetite/energy-balance regulating centers of the postnatal and adult hypothalamus. J. Neurosci. 2013, 33:6170-6180.
52. Hanon E.A., Lincoln G.A., Fustin J.M., Dardente H., Masson-Pevet M., Morgan P.J., Hazlerigg D.G. Ancestral TSH mechanism signals summer in a photoperiodic mammal. Curr. Biol. 2008, 18:1147-1152.
53. Hanon E.A., Routledge K., Dardente H., Masson-Pevet M., Morgan P.J., Hazlerigg D.G. Effect of photoperiod on the thyroid-stimulating hormone neuroendocrine system in the European hamster (Cricetus cricetus). J Neuroendocrinol 2010, 22:51-55.
54. Hazlerigg D.G., Lincoln G.A. Hypothesis: cyclical histogenesis is the basis of circannual timing. J. Biol. Rhythms 2011, 26:471-485.
55. Hazlerigg D.G., Loudon A.S.I. Seasonal life timers: new insights into ancient mechanisms. Curr. Biol. 2008, 18:R795-R804.
56. Hazlerigg D.G., Wyse C.A., Dardente H., Hanon E.A., Lincoln G.A. Photoperiodic variation in CD45-positive cells and cell proliferation in the mediobasal hypothalamus of the soay sheep. Chronobiol. Int. 2013, 30:548-558.
57. Helfer G., Ross A.W., Russell L., Thomson L.M., Shearer K.D., Goodman T.H., McCaffery P.J., Morgan P.J. Photoperiod regulates vitamin A and Wnt/β-catenin signaling in F344 rats. Endocrinology 2012, 152:815-824.
58. Helfer G., Ross A.W., Morgan P.J. Neuromedin U partly mimics thyroid-stimulating hormone and triggers Wnt/β-catenin signalling in the photoperiodic response of F344 rats. J. Neuroendocrinol. 2013, 25:1264-1272.
59. 3 elicits long day-like alterations in testis size and the RFamides Kisspeptin and gonadotropin-inhibitory hormone in short-day Siberian hamsters. J. Biol. Rhythms 2013, 28:193-200.
60. Herbert J., Stacey P.M., Thorpe D.H. Recurrent breeding seasons in pinealectomized or optic-nerve-sectioned ferrets. J. Endocrinol. 1978, 78:389-397.
61. Herwig A., Wilson D., Logie T.J., Boelen A., Morgan P.J., Mercer J.G., Barrett P. Photoperiod and acute energy deficits interact on components of the thyroid hormone system in hypothalamic tanycytes of the Siberian hamster. Am J Physiol. 2009, 296:R1307-R1315.
62. Herwig A., de Vries E.M., Bolborea M., Wilson D., Mercer J.G., Ebling F.J.P., Morgan P.J., Barrett P. Hypothalamic ventricular ependymal thyroid hormone deiodinases are an important element of circannual timing in the siberian hamster (Phodopus sungorus). PLoS One 2013, 8:e62003. doi: 62010.61371/journal.pone.0062003.
63. Hoffmann K. The influence of photoperiod and melatonin on testis size, body weight, and pelage colour in the Djungarian hamster (Phodopus sungorus). J. Comp. Physiol. B. 1973, 85:267-282.
64. Hoffmann K. Effects of short photoperiods on puberty, growth and moult in the Djungarian hamster (Phodopus sungorus). J. Reprod. Fertil. 1978, 54:29-35.
65. Huang L., De Vries G.J., Bittman E.L. Photoperiod regulates neuronal bromodeoxyuridine labeling in the brain of a seasonally breeding mammal. J. Neurobiol. 1998, 36:410-420.
66. Jansen H.T., Cutter C., Hardy S., Lehman M.N., Goodman R.L. Seasonal plasticity within the gonadotropin-releasing hormone (GnRH) system of the ewe: changes in identified GnRH inputs and glial association. Endocrinology 2003, 144:119-122.
67. Ji H., Outterbridge L.V., Friedman M.I. Phenotype-based treatment of dietary obesity: differential effects of fenofibrate in obesity-prone and obesity-resistant rats. Metab. Clin. Exp. 2005, 54:421-429.
68. Johnston J.D., Tournier B.B., Andersson H., Masson-Pevet M., Lincoln G.A., Hazlerigg D.G. Multiple effects of melatonin on rhythmic clock gene expression in the mammalian pars tuberalis. Endocrinology 2006, 147:959-965.
69. Kameda Y., Arai Y., Nishimaki T. Ultrastructural localization of vimentin immunoreactivity and gene expression in tanycytes and their alterations in hamsters kept under different photoperiods. Cell Tissue Res. 2003, 314:251-262.
70. Kampf-Lassin A., Prendergast B.J. Photoperiod history-dependent responses to intermediate day lengths engage hypothalamic iodothyronine deiodinase type III mRNA expression. Am J Physiol. 2013, 304:R628-R635.
71. Karsch F.J., Bittman E.L., Foster D.L., Goodman R.L., Legan S.J., Robinson J.E. Neuroendocrine basis of seasonal reproduction. Recent Prog. Horm. Res. 1984, 40:185-231.
72. Klieverik L.P., Janssen S.F., van Riel A., Foppen E., Bisschop P.A., Serlie M.J., Boelen A., Ackerman M.T., Sauerwein H.P., Fliers E., Kalsbeek A. Thyroid hormone modulates glucose production via a sympathetic pathway from the hypothalamic paraventricular nucleus to the liver. Proc. Natl. Acad. Sci. USA 2009, 106:5966-5971.
73. Klingenspor M., Niggemann H., Heldmaier G. Modulation of leptin sensitivity by short photoperiod acclimation in the Djungarian hamster, Phodopus sungorus. J. Comp. Physiol. B. 2000, 170:37-43.
74. Klosen P., Sebert M.E., Rasri K., Laran-Chich M.P., Simonneaux V. TSH restores a summer phenotype in photoinhibited mammals via the RF-amides RFRP3 and kisspeptin. FASEB J. 2013, 27:2677-2686.
75. Knopper L.D., Boily P. The energy budget of captive Siberian hamsters, Phodopus sungorus, exposed to photoperiod changes: mass loss is caused by a voluntary decrease in food intake. Physiol. Biochem. Zool. 2000, 73:517-522.
76. Kokoeva M.V., Yin H., Flier J.S. Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 2005, 310:679-683.
77. Kokoeva M.V., Yin H., Flier J.S. Evidence for constitutive neural cell proliferation in the adult murine hypothalamus. J. Comp. Neurol. 2007, 505:209-220.
78. 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.
79. Kong W.M., Martin N.M., Smith K.L., Gardiner J., Connoley I.P., Stephens D.A., Dhillo W.S., Ghatei M.A., Small C.J., Bloom S.R. Triiodothyronine stimulates food intake via the hypothalamic ventromedial nucleus independent of changes in energy expenditure. Endocrinology 2004, 145:5252-5258.
80. Król E., Douglas A., Dardente H., Birnie M.J., van der Vinne V., Eijer W.G., Gerkema M.P., Hazlerigg D.G., Hut R.A. Strong pituitary and hypothalamic responses to photoperiod but not to 6-methoxy-2-benzoxazolinone in female common voles (Microtus arvalis). Gen Comp Endocr 2012, 179:289-295.
81. Lechan R.M., Qi Y., Berrodin T.J., Davis K.D., Schwartz H.L., Strait K.A., Oppenheimer J.H., Lazar M.A. Immunocytochemical delineation of thyroid hormone receptor β2-like immunoreactivity in the rat central nervous system. Endocrinology 1993, 132:2461-2469.
82. Lee W., Watanabe M., Glass J.D. Photoperiod affects the expression of neural cell adhesion molecule and polysialic acid in the hypothalamus of the Siberian hamster. Brain Res. 1995, 690:64-72.
83. Lee D.A., Bedont J.L., Pak T., Wang H., Song J., Miranda-Angulo A., Takiar V., Charubhumi V., Balordi F., Takebayashi H., Aja S., Ford E., Fishell G., Blackshaw S. Tanycytes of the hypothalamic median eminence form a diet-responsive neurogenic niche. Nat. Neurosci. 2012, 15:700-702.
84. Legan S.J., Karsch F.J. Importance of retinal photoreceptors to the photoperiodic control of seasonal breeding in the ewe. Biol. Reprod. 1983, 29:316-325.
85. Lincoln G.A. Seasonal cycles in testicular activity in Mouflon, Soay sheep and domesticated breeds of sheep: breeding seasons modified by domestication. Zool. J. Linnean Soc. 1989, 95:137-147.
86. Lincoln G.A. Correlation with changes in horns and pelage, but not reproduction, of seasonal cycles in the secretion of prolactin in rams of wild, feral and domesticated breeds of sheep. J. Reprod. Fertil. 1990, 90:285-296.
87. Lincoln G.A. Reproductive seasonality and maturation throughout the complete life-cycle in the mouflon ram (Ovis musimon). Anim. Reprod. Sci. 1998, 53:87-105.
88. Lincoln G.A., Short R.V. Seasonal breeding: nature's contraceptive. Recent Prog. Horm. Res. 1980, 36:1-52.
89. Lincoln G.A., Fraser H.M., Fletcher T.J. Antler growth in male red deer (Cervus elaphus) after active immunization against LH-RH. J. Reprod. Fertil. 1982, 66:703-708.
90. López M., Varela L., Vázquez M.J., Rodríguez-Cuenca S., González C.R., Velagapudi V.R., Morgan D.A., Schoenmakers E., Agassandian K., Lage R., Martínez de Morentin P.B., Tovar S., Nogueiras R., Carling D., Lelliott C., Gallego R., Oresic M., Chatterjee K., Saha A.K., Rahmouni K., Diéguez C., Vidal-Puig A. Hypothalamic AMPK and fatty acid metabolism mediate thyroid regulation of energy balance. Nat. Med. 2010, 16:1001-1008.
91. Loudon A.S.I., Milne J.A., Curlewis J.D., McNeilly A.S. A comparison of the seasonal hormone changes and patterns of growth, voluntary food intake and reproduction in juvenile and adult red deer (Cervus elaphus) and Pere David's deer (Elaphurus davidianus) hinds. J. Endocrinol. 1989, 122:733-745.
92. Lucas R.J., Freedman M.S., Munoz M., Garciafernandez J.M., Foster R.G. Regulation of the mammalian pineal by non-rod, non-cone, ocular photoreceptors. Science 1999, 284:505-507.
93. Marshall F.H.A. On the change over in the oestrous cycle in animals after transference across the equator, with further observations on the incidence of the breeding seasons and the factors controlling sexual periodicity. Proc. Royal Soc. Lond. B 1937, 122:413-428.
94. Martin B., Ji S., Maudsley S., Mattson M.P. "Control" laboratory rodents are metabolically morbid: Why it matters. Proc. Natl. Acad. Sci. USA 2010, 107:6127-6133.
95. Martinet L., Mondain-Monval M., Monnerie R. Endogenous circannual rhythms and photorefractoriness of testis activity, moult and prolactin concentrations in mink (Mustela vison). J. Reprod. Fertil. 1992, 95:325-338.
96. McNay D.E.G., Briançon N., Kokoeva M.V., Maratos-Flier E., Flier J.S. Remodeling of the arcuate nucleus energy balance circuit is inhibited in obese mice. J. Clin. Invest. 2012, 122:142-152.
97. Mercer J.G., Moar K.A., Ross A.W., Morgan P.J. Regulation of leptin receptor, POMC and AGRP gene expression by photoperiod and food deprivation in the hypothalamic arcuate nucleus of the male Siberian hamster (Phodopus sungorus). Appetite 2000, 34:109-111.
98. Merks T., Schulze-Bonhage A., Wittkowski W. Photoperiod-dependent changes in exocytotic activity in the hypophyseal pars tuberalis of the Djungarian hamster, Phodopus sungorus. Cell Tissue Res. 1993, 273:289-291.
99. Migaud M., Batailler M., Segura S., Duittoz A.H., 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.
100. Migaud M., Batailler M., Pillon D., Franceschini I., Malpaux B. Seasonal changes in cell proliferation in the adult sheep brain and pars tuberalis. J. Biol. Rhythms 2011, 26:486-496.
101. Millán C., Martínez F., Cortés-Campos C., Lizama I., Yañez M., Llanos P., Reinicke K., Rodríguez F., Peruzzo B., Nualart F., García M.A. Glial glucokinase expression in adult and post-natal development of the hypothalamic region. ASN Neuro 2010, 25:e00035. 00010.01042/AN20090059.
102. Moenter S.M., Woodfill C.J.I., Karsch F.J. Role of the thyroid gland in seasonal reproduction: thyroidectomy blocks seasonal suppression of reproductive neuroendocrine activity ewes. Endocrinology 1991, 128:1337-1344.
103. Moore R.Y. Neural control of the pineal gland. Behav. Brain Res. 1996, 73:125-130.
104. Morgan P.J., Hazlerigg D.G. Photoperiodic signalling through the melatonin receptor turns full circle. J. Neuroendocrinol. 2008, 20:820-826.
105. Morgan P.J., Barrett P., Howell H.E., Helliwell R. Melatonin receptors: localization, molecular pharmacology and physiological significance. Neurochem. Int. 1994, 24:101-146.
106. Morgan P.J., Ross A.W., Mercer J.G., Barrett P. What can we learn from seasonal animals about the regulation of energy balance?. Prog. Brain Res. 2006, 153:325-337.
107. Murphy M., Jethwa P.H., Warner A., Barrett P., Nilaweera K.N., Brameld J.M., Ebling F.J.P. Effects of manipulating hypothalamic tri-iodothyronine concentrations on seasonal body weight and torpor cycles in Siberian hamsters. Endocrinology 2012, 153:101-112.
108. Murphy M., Samms R., Warner A., Bolborea M., Barrett P., Fowler M.J., Brameld J.M., Kharitonenkov A., Adams A.C., Coskun T., Ebling F.J.P. Increased responses to the actions of fibroblast growth factor 21 on energy balance and body weight in a seasonal model of adiposity. J. Neuroendocrinol. 2013, 25:180-189.
109. Nakane, Y., Ikegami, K., Iigo, M., Ono, H., Takeda, K., Takahashi, D., Uesaka, M., Kimijima, M., Hashimoto, R., Arai, N., Suga, T., Kosuge, K., Abe, T., Maeda, R., Senga, T., Amiya, N., Azuma, T., Amano, M., Abe, H., Yamamoto, N., Yoshimura, T., 2013. The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nature Communications 4:2108 doi: 2110.1038/ncomms3108.
110. Nakao N., Ono H., Yamamura T., Anraku T., Takagi T., Higuchi K., Yasuo S., Katou Y., Kageyama S., Uno Y., Kasukama T., Iiog M., Sharp P.J., Iwasawa A., Suzuki Y., Sugano S., Niimi T., Mizutani M., Namikawa T., Ebihara S., Ueda H.R., Yoshimura T. Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature 2008, 452:317-322.
111. Ngarmukos C., Baur E.L., Kumagai A.K. Co-localization of GLUT1 and GLUT4 in the blood-brain barrier of the rat ventromedial hypothalamus. Brain Res. 2001, 900:1-8.
112. Nicholls T.J., Goldsmith A.R., Dawson A. Photorefractoriness in European starlings: associated hypothalamic changes and the involvement of thyroid hormones and prolactin. J. Exp. Zool. 1984, 232:567-572.
113. Nilaweera K.N., Herwig A., Bolborea M., Campbell G., Mayer C.D., Morgan P.J., Ebling F.J.P., Barrett P. Photoperiodic regulation of glycogen metabolism, glycolysis, and glutamine synthesis in tanycytes of the Siberian hamster suggests novel roles of tanycytes in hypothalamic function. Glia 2011, 59:1695-1705.
114. Nottebohm F. The road we travelled: discovery, choreography, and significance of brain replaceable neurons. Ann. N.Y. Acad. Sci. 2004, 1016:628-658.
115. Ono H., Hoshino Y., Yasuo S., Watanabe M., Nakane Y., Murai A., Ebihara S., Korf H.-W., Yoshimura T. Involvement of thyrotropin in photoperiodic signal transduction in mice. Proc. Natl. Acad. Sci. USA 2008, 105:18238-18242.
116. Parker J.A., Bloom S.R. Hypothalamic neuropeptides and the regulation of appetite. Neuropharmacology 2012, 63:18-30.
117. Parkinson T.J., Follett B.K. Effect of thyroidectomy upon seasonality in rams. J. Reprod. Fertil. 1994, 101:51-58.
118. Parkinson T.J., Follett B.K. Thyroidectomy abolishes seasonal testicular cycles of Soay rams. Proc. Royal Soc. Lond. B 1995, 259:1-6.
119. Petri I., Dumbell R., Scherbarth F., Steinlechner S., Barrett P. Effect of exercise on photoperiod-regulated hypothalamic gene expression and peripheral hormones in the seasonal dwarf hamster phodopus sungorus. PLoS ONE 2014, 9(3):e90253. 90210.91371/journal.pone.0090253.
120. Pierce A.A., Xu A.W. De novo neurogenesis in adult hypothalamus as a compensatory mechanism to regulate energy balance. J. Neurosci. 2010, 30:723-730.
121. Prendergast B.J., Pyter L.M., Kampf-Lassin A., Patel P.N., Stevenson T.J. Rapid induction of hypothalamic iodothyronine deiodinase expression by photoperiod and melatonin in juvenile Siberian hamsters (Phodopus sungorus). Endocrinology 2013, 154:831-841.
122. Randall V.A., Ebling F.J. Seasonal changes in human hair growth. Br. J. Dermatol. 1991, 124:146-151.
123. Reddy A.B., Cronin A.S., Ford H., Ebling F.J.P. Seasonal regulation of food intake and body weight in the male Siberian hamster: studies of hypothalamic orexin (hypocretin), neuropeptide Y (NPY) and pro-opiomelanocortin (POMC). Eur. J. Neurosci. 1999, 11:3255-3264.
124. Revel F.G., Saboureau M., Pevet P., Mikkelsen J.D., Simonneaux V. Melatonin regulates type 2 deiodinase gene expression in the Syrian hamster. Endocrinology 2006, 147:369-384.
125. Robinson J.E., Radford H.M., Karsch F.J. 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 feed back. Biol. Reprod. 1985, 33:324-334.
126. Robson A.J., Rousseau K., Loudon A.S.I., Ebling F.J.P. Cocaine and amphetamine-related transcript (CART) mRNA regulation in the hypothalamus in lean and obese rodents. J. Neuroendocrinol. 2002, 14:697-709.
127. Roenneberg T., Aschoff J. Annual rhythm of human reproduction: I. Biology, sociology, or both?. J. Biol. Rhythms 1990, 5:195-215.
128. Ross, A.W., Helfer, G., Russell, L., Darras, V.M., Morgan, P.J., 2011. Thyroid hormone signalling genes are regulated by photoperiod in the hypothalamus of F344 rats. PlosONE 6:e21351 doi: 21310.21371/journal.pone.0021351.
129. Rousseau K., Atcha Z., Cagampang F.R.A., Le Rouzic P., Stirland J.A., Ivanov T.R., Ebling F.J.P., Klingenspor M., Loudon A.S.I. Photoperiodic regulation of leptin resistance in the seasonally breeding Siberian hamster (Phodopus sungorus). Endocrinology 2002, 143:3083-3095.
130. Rousseau K., Atcha Z., Denton J., Cagampang F.R.A., Ennos E.R., Freemont A.J., Loudon A.S.I. Skeletal bone morphology is resistant to the high amplitude seasonal leptin cycle in the Siberian hamster. J. Endocrinol. 2005, 186:475-479.
131. Rowan W. Relation of light to bird migration and developmental changes. Nature 1925, 115:494-495.
132. Ruby N.F., Brennan T.J., Xie X., Cao V., Franken P., Heller H.C., O'Hara B.F. Role of melanopsin in circadian responses to light. Science 2002, 298:2211-2213.
133. Saaltink D.J., Håvik B., Verissimo C.S., Lucassen P.J., Vreugdenhil E. Doublecortin and doublecortin-like are expressed in overlapping and non-overlapping neuronal cell population: implications for neurogenesis. J. Comp. Neurol. 2012, 520:2805-2823.
134. Sáenz de Miera C., Hanon E.A., Dardente H., Birnie M.J., Simonneaux V., Lincoln G.A., Hazlerigg D.G. Circannual variation in thyroid hormone deiodinases in a short-day breeder. J. Neuroendocrinol. 2013, 25:412-421.
135. Sáenz de Miera C., Monecke S., Bartzen-Sprauer J., Laran-Chich M.P., Pevet P., Hazlerigg D.G., Simonneaux V. A circannual clock drives expression of genes central for seasonal reproduction. Curr. Biol. 2014, 24:1500-1506.
136. Samms R., Fowler M.J., Cooper S., Emmerson P.J., Coskun T., Adams A.C., Kharitonenkov A., Tsintzas K., Ebling F.J.P. Photoperiodic regulation of FGF21 production in the Siberian hamster. Horm. Behav. 2014, 66:180-185.
137. Schafer E.A. On the incidence of daylight as a determining factor in bird migration. Nature 1907, 77:159-163.
138. Schneider J.E., Klingerman C.M., Abdulhay A. Sense and nonsense in metabolic control of reproduction. Front. Endocrinol. 2012, 3:26. 10.3389/fendo.2012.00026.
139. Schneider J.E., Wise J.D., Benton N.A., Brozek J.M., Keen-Rhinehart E. When do we eat? Ingestive behavior, survival, and reproductive success. Horm. Behav. 2013, 64:702-728.
140. Shearer K.D., Goodman T.H., Ross A.W., Reilly L., Morgan P.J., McCaffery P.J. Photoperiodic regulation of retinoic acid signaling in the hypothalamus. J. Neurochem. 2010, 112:246-257.
141. Shearer K.D., Stoney P.N., Morgan P.J., McCaffery P.J. A vitamin for the brain. Trends Neurosci. 2012, 35:733-741.
142. Tups A., Ellis C., Moar K.A., Logie T.J., Adam C., Mercer J.G., Klingenspor M. Photoperiodic regulation of leptin sensitivity in the siberian hamster, phodopus sungorus, is reflected in arcuate nucleus SOCS-3 (suppressor of cytokine signaling) gene expression. Endocrinology 2004, 145:1185-1193.
143. Viguie C., Battaglia D.F., Krasa H.B., Thrun L.A., Karsch F.J. Thyroid hormones act primarily within the brain to promote the seasonal inhibition of luteinizing hormone secretion in the ewe. Endocrinology 1999, 140:1111-1117.
144. Wade G.N., Bartness T.J. Effects of photoperiod and gonadectomy on food intake, body weight, and body composition in Siberian hamsters. Am. J. Physiol. 1984, 246:R26-R30.
145. Wagner G.C., Johnston J.D., Tournier B.B., Ebling F.J.P., Hazlerigg D.G. Melatonin induces gene-specific effects on rhythmic mRNA expression in the pars tuberalis of the Siberian Hamster (Phodopus sungorus). Eur. J. Neurosci. 2007, 25:485-490.
146. Warner A., Mittag J. Thyroid hormone and the central control of homeostasis. J. Mol. Endocrinol. 2012, 49:29-36.
147. Warner A., Jethwa P.H., Wyse C.A., I'Anson H., Brameld J.M., Ebling F.J.P. Effects of photoperiod on daily locomotor activity, energy expenditure and feeding behavior in a seasonal mammal. Am. J. Physiol. 2010, 298:R1409-R1416.
148. Weaver D.R., Reppert S.M. Melatonin receptors are present in the ferret pars tuberalis and pars distalis, but not in brain. Endocrinology 1990, 127:2607-2609.
149. Webster J.R., Moenter S.M., Barrell G.K., Lehman M.N., Karsch F.J. Role of the thyroid gland in seasonal reproduction. III. Thyroidectomy blocks seasonal suppression of Gonadotropin-Releasing hormone secretion in sheep. Endocrinology 1991, 123:1635-1643.
150. Webster J.R., Moenter S.M., Woodfill C.J.I., Karsch F.J. 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.
151. Williams L.M., Morgan P.J. Demonstration of melatonin-binding sites on the pars tuberalis of the rat. Exp. Brain Res. 1988, 72:443-449.
152. Wittkowski W., Hewing M., Hoffmann K., Bergmann M., Fechner J. Influence of photoperiod on the ultrastructure of the hypophysial pars tuberalis of the Djungarian hamster, Phodopus sungorus. Cell Tissue Res. 1984, 238:213-216.
153. Wittkowski W., Bergmann M., Hoffmann K., Pera F. Photoperiod-dependent changes in TSH-like immunoreactivity of cells in the hypophysical pars tuberalis of the Djungarian hamster, Phodopus sungorus. Cell Tissue Res. 1988, 251:183-187.
154. Xiong J.J., Karsch F.J., Lehman M.N. Evidence for seasonal plasticity in the gonadotrophin-releasing hormone (GnRH) system of the ewe: changes in synaptic inputs onto GnRH neurons. Endocrinology 1997, 138:1240-1250.
155. Xu Y., Tamamaki N., Noda T., Kimura K., Itokazu Y., Matsumoto S., Dezawa M., Ide C. Neurogenesis in the ependymal layer of the adult rat 3rd ventricle. Exp. Neurol. 2005, 192:251-264.
156. Yasuo S., Watanabe M., Ligo M., Nakamura T., Watanabe T., Takagi T., Ono H., Ebihara S., Yoshimura T. Differential response of type 2 deiodinase gene expression to photoperiod between photoperiodic Fischer 344 and nonphotoperiodic Wistar rats. Am J Physiol. 2007, 292:R1315-R1319.
157. Yeo G.S.H., Heisler L.K. Unraveling the brain regulation of appetite: lessons from genetics. Nat. Neurosci. 2012, 15:1343-1349.
158. 3 regulates photoperiodic response of gonads in birds. Nature 2003, 426:178-181.