Abstract
The pars tuberalis is part of the pituitary stalk that sits at the interface between the median eminence of the hypothalamus and the anterior pituitary gland (pars distalis). It primarily comprises thyrotrophs that produce βTSH, and folliculostellate cells. In all mammals studied to date it expresses a high density of melatonin receptors, so it is the key interface between the circulation and the hypothalamus for transduction of nocturnal melatonin signals that convey photoperiodic information. This chapter explores the mechanisms by which the changing duration of nocturnal melatonin regulates circadian ‘clock genes’, including cry1 and a ‘developmental’ gene EYA3 in the pars tuberalis, resulting in differential production of βTSH and ‘tuberalins’ to regulate hypothalamic and anterior pituitary function, respectively.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Akimoto M et al (2010) Hes1 regulates formations of the hypophyseal pars tuberalis and the hypothalamus. Cell Tissue Res 340(3):509–521. https://doi.org/10.1007/s00441-010-0951-2
Anderson GM, Barrell GK (1998) Pulsatile luteinizing hormone secretion in the ovariectomized, thyroidectomized red deer hind following treatment with dopaminergic and opioidergic agonists and antagonists. Biol Reprod 59(4):960–968. http://www.ncbi.nlm.nih.gov/pubmed/9746749
Anderson G et al (2003) 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 144(7):2892–2901. https://doi.org/10.1210/en.2003-0322
Bank JHH et al (2017) Gene expression analysis and microdialysis suggest hypothalamic triiodothyronine (T3) gates daily torpor in Djungarian hamsters (Phodopus sungorus). J Comp Physiol B 187(5–6):857–868. https://doi.org/10.1007/s00360-017-1086-5
Barrett P et al (2006) Photoperiodic regulation of cellular retinoic acid-binding protein 1, GPR50 and nestin in tanycytes of the third ventricle ependymal layer of the Siberian hamster. J Endocrinol 191(3):687–698. https://doi.org/10.1677/joe.1.06929
Barrett P et al (2007) Hypothalamic thyroid hormone catabolism acts as a gatekeeper for the seasonal control of body weight and reproduction. Endocrinology 148(8):3608–3617. https://doi.org/10.1210/en.2007-0316
Bartness TJ et al (1993) 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 15(4):161–190. http://www.ncbi.nlm.nih.gov/pubmed/8120796
Bechtold DA et al (2012) A role for the melatonin-related receptor GPR50 in leptin signaling, adaptive thermogenesis, and torpor. Curr Biol 22(1):70–77. https://doi.org/10.1016/j.cub.2011.11.043
Benoit J (1936) Role de la thyroide dans la gonado-stimulation par lumiere artificielle chez le canard domestique. C R Soc Biol 123:243–246
Beymer M et al (2016) The role of kisspeptin and RFRP in the circadian control of female reproduction. Mol Cell Endocrinol 438:89–99. https://doi.org/10.1016/j.mce.2016.06.026
Billings HJ et al (2002) Temporal requirements of thyroid hormones for seasonal changes in LH secretion. Endocrinology 143(7):2618–2625. https://doi.org/10.1210/endo.143.7.8924
Bittman EL, Dempsey RJ, Karsch FJ (1983) Pineal melatonin secretion drives the reproductive response to daylength in the ewe. Endocrinology 113(6):2276–2283. https://doi.org/10.1210/endo-113-6-2276
Bockmann J et al (1997) Thyrotropin expression in hypophyseal pars tuberalis-specific cells is 3,5,3’-triiodothyronine, thyrotropin-releasing hormone, and pit-1 independent. Endocrinology 138(3):1019–1028. https://doi.org/10.1210/endo.138.3.5007
Bratincsák A et al (2007) Spatial and temporal activation of brain regions in hibernation: c-fos expression during the hibernation bout in thirteen-lined ground squirrel. J Comp Neurol 505(4):443–458. https://doi.org/10.1002/cne.21507
Brinklow BR, Loudon AS (1993) Evidence for a circannual rhythm of reproduction and prolactin secretion in a seasonally breeding macropodid marsupial, the Bennett’s wallaby (Macropus rufogriseus rufogriseus). J Reprod Fertil 98(2):625–630. http://www.ncbi.nlm.nih.gov/pubmed/8410834
Bünning E (1936) Die endogene Tagesperiodik als Grundlage der photoperiodischen Reaktion. Ber Dtsch Bot Ges 54:590–608
Butler MP et al (2010) Seasonal regulation of reproduction: altered role of melatonin under naturalistic conditions in hamsters. Proc Biol Sci 277(1695):2867–2874. https://doi.org/10.1098/rspb.2010.0396
Carter DS, Goldman BD (1983) Antigonadal effects of timed melatonin infusion in pinealectomized male Djungarian hamsters (Phodopus sungorus sungorus): duration is the critical parameter. Endocrinology 113(4):1261–1267. https://doi.org/10.1210/endo-113-4-1261
Curlewis JD (1992) Seasonal prolactin secretion and its role in seasonal reproduction: a review. Reprod Fertil Dev 4(1):1–23. http://www.ncbi.nlm.nih.gov/pubmed/1585003
Dardente H (2012) Melatonin-dependent timing of seasonal reproduction by the pars tuberalis: pivotal roles for long daylengths and thyroid hormones. J Neuroendocrinol 24(2):249–266. https://doi.org/10.1111/j.1365-2826.2011.02250.x
Dardente H et al (2003) MT1 melatonin receptor mRNA expressing cells in the pars tuberalis of the European hamster: effect of photoperiod. J Neuroendocrinol 15(8):778–786. http://www.ncbi.nlm.nih.gov/pubmed/12834439
Dardente H et al (2010) A molecular switch for photoperiod responsiveness in mammals. Curr Biol 20(24):2193–2198. https://doi.org/10.1016/j.cub.2010.10.048
Dardente H, Hazlerigg DG, Ebling FJP (2014) Thyroid hormone and seasonal rhythmicity. Front Endocrinol 5:19. https://doi.org/10.3389/fendo.2014.00019
Dawson A (2015) Annual gonadal cycles in birds: modeling the effects of photoperiod on seasonal changes in GnRH-1 secretion. Front Neuroendocrinol 37:52–64. https://doi.org/10.1016/j.yfrne.2014.08.004
Dufourny L et al (2008) GPR50 is the mammalian ortholog of Mel1c: evidence of rapid evolution in mammals. BMC Evol Biol 8(1):105. https://doi.org/10.1186/1471-2148-8-105
Duncan MJ et al (1985) Testicular function and pelage color have different critical daylengths in the djungarian hamster, Phodopus sungorus sungorus. Endocrinology 116(1):424–430. https://doi.org/10.1210/endo-116-1-424
Dupré SM et al (2008) Identification of melatonin-regulated genes in the ovine pituitary pars tuberalis, a target site for seasonal hormone control. Endocrinology 149(11):5527–5539. https://doi.org/10.1210/en.2008-0834
Dupré SM et al (2010) Identification of Eya3 and TAC1 as long-day signals in the sheep pituitary. Curr Biol 20(9):829–835. https://doi.org/10.1016/j.cub.2010.02.066
Duston J, Bromage N (1991) Circannual rhythms of gonadal maturation in female rainbow trout (Oncorhynchus mykiss). J Biol Rhythm 6(1):49–53. https://doi.org/10.1177/074873049100600106
Falcón J et al (2010) Current knowledge on the melatonin system in teleost fish. Gen Comp Endocrinol 165(3):469–482. https://doi.org/10.1016/j.ygcen.2009.04.026
Follett BK, Nicholls TJ (1985) Influences of thyroidectomy and thyroxine replacement on photoperiodically controlled reproduction in quail. J Endocrinol 107(2):211–221. http://www.ncbi.nlm.nih.gov/pubmed/4067480
Frantzen M et al (2004) Effects of photoperiod on sex steroids and gonad maturation in Arctic charr. Aquaculture 240(1–4):561–574. https://doi.org/10.1016/j.aquaculture.2004.07.013
Freeman ME et al (2000) Prolactin: structure, function, and regulation of secretion. Physiol Rev 80(4):1523–1631. https://doi.org/10.1152/physrev.2000.80.4.1523
Fustin JM et al (2009) Egr1 involvement in evening gene regulation by melatonin. FASEB J 23(3):764–773. https://doi.org/10.1096/fj.08-121467
Goldman BD (2001) Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J Biol Rhythm 16(4): 283–301. http://www.ncbi.nlm.nih.gov/pubmed/11506375
Gross DS (1984) The mammalian hypophysial pars tuberalis: a comparative immunocytochemical study. Gen Comp Endocrinol 56(2):283–298. http://www.ncbi.nlm.nih.gov/pubmed/6510690. Accessed 27 Oct 2014
Gwinner E (1986) Circannual rhythms. Springer, Berlin
Hanon EA et al (2008) Ancestral TSH mechanism signals summer in a photoperiodic mammal. Curr Biol 18(15):1147–1152. https://doi.org/10.1016/j.cub.2008.06.076
Hanon EA et al (2010) Effect of photoperiod on the thyroid-stimulating hormone neuroendocrine system in the European hamster (Cricetus cricetus). J Neuroendocrinol 22(1):51–55. https://doi.org/10.1111/j.1365-2826.2009.01937.x
Hazlerigg D, Loudon A (2008) New insights into ancient seasonal life timers. Curr Biol 18(17):R795–R804. https://doi.org/10.1016/j.cub.2008.07.040
Hazlerigg D, Simonneaux V (2015) Seasonal reproduction in mammals. In: Plant T, Zeleznic A (eds) Knobil and Neill’s physiology and reproduction, 4th edn. Academic Press, London, pp 1575–1660
Hazlerigg DG et al (1993) Prolonged exposure to melatonin leads to time-dependent sensitization of adenylate cyclase and down-regulates melatonin receptors in pars tuberalis cells from ovine pituitary. Endocrinology 132(1):285–292. https://doi.org/10.1210/endo.132.1.7678217
Hazlerigg D, Blix AS, Stokkan K-A (2017) Waiting for the sun: the circannual program of reindeer is delayed by the recurrence of rhythmical melatonin secretion after the arctic night. J Exp Biol 220(Pt 21):jeb.163741. https://doi.org/10.1242/jeb.163741
Heyland A, Hodin J, Reitzel AM (2005) Hormone signaling in evolution and development: a non-model system approach. BioEssays 27(1):64–75. https://doi.org/10.1002/bies.20136
Hoffman RA, Reiter RJ (1965) Pineal gland: influence on gonads of male hamsters. Science (New York, NY) 148(3677):1609–1611.http://www.ncbi.nlm.nih.gov/pubmed/14287606
Inoue K et al (1999) The structure and function of folliculo-stellate cells in the anterior pituitary gland. Arch Histol Cytol 62(3):205–218. http://www.ncbi.nlm.nih.gov/pubmed/10495875
Inoue M et al (2013) Detailed morphogenetic analysis of the embryonic chicken pars tuberalis as glycoprotein alpha subunit positive region. J Mol Hist 44(4):401–409. https://doi.org/10.1007/s10735-012-9479-y
Ivanova EA et al (2008) Altered metabolism in the melatonin-related receptor (GPR50) knockout mouse. Am J Physiol Endocrinol Metab 294(1). http://ajpendo.physiology.org/content/294/1/E176
Johnston JD et al (2006) Regulation of MT melatonin receptor expression in the foetal rat pituitary. J Neuroendocrinol 18(1):50–56. https://doi.org/10.1111/j.1365-2826.2005.01389.x
Kameda Y, Miura M, Maruyama S (2002) Effect of pinealectomy on the photoperiod-dependent changes of the specific secretory cells and à-subunit mRNA level in the chicken pars tuberalis. Cell Tissue Res 308(1):121–130. https://doi.org/10.1007/s00441-002-0537-8
Klosen P et al (2002) 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 50(12):1647–1657. http://www.ncbi.nlm.nih.gov/pubmed/12486087
Klosen P et al (2013) TSH restores a summer phenotype in photoinhibited mammals via the RF-amides RFRP3 and kisspeptin. FASEB J 27(7):2677–2686. https://doi.org/10.1096/fj.13-229559
Korf H-W (2018) Signaling pathways to and from the hypophysial pars tuberalis, an important center for the control of seasonal rhythms. Gen Comp Endocrinol 258:236–243. https://doi.org/10.1016/j.ygcen.2017.05.011
Król E et al (2012) Strong pituitary and hypothalamic responses to photoperiod but not to 6-methoxy-2-benzoxazolinone in female common voles (Microtus arvalis). Gen Comp Endocrinol 179(2):289–295. https://doi.org/10.1016/j.ygcen.2012.09.004
Lechan RM, Fekete C (2005) Role of thyroid hormone deiodination in the hypothalamus. Thyroid 15(8):883–897. https://doi.org/10.1089/thy.2005.15.883
Lewis JE, Ebling FJP (2017) tanycytes as regulators of seasonal cycles in neuroendocrine function. Front Neurol 8:79. https://doi.org/10.3389/fneur.2017.00079
Lincoln GA (2006) Melatonin entrainment of circannual rhythms. Chronobiol Int 23(1–2):301–306. https://doi.org/10.1080/07420520500464452
Lincoln GA, Clarke IJ (1994) Photoperiodically-lnduced cycles in the secretion of prolactin in hypothalamo-pituitary disconnected rams: evidence for translation of the melatonin signal in the pituitary gland. J Neuroendocrinol 6(3):251–260. https://doi.org/10.1111/j.1365-2826.1994.tb00580.x
Lincoln G et al (2002) 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 U S A 99(21):13890–13895. https://doi.org/10.1073/pnas.212517599
Lincoln GA et al (2005) Photorefractoriness in mammals: dissociating a seasonal timer from the circadian-based photoperiod response. Endocrinology 146(9):3782–3790. https://doi.org/10.1210/en.2005-0132
Lincoln GA et al (2006) Characterizing a mammalian circannual pacemaker. Science (New York, NY) 314(5807):1941–1944. https://doi.org/10.1126/science.1132009
Lorgen M et al (2015) Functional divergence of type 2 deiodinase paralogs in the Atlantic salmon. Curr Biol 25(7):936–941. https://doi.org/10.1016/j.cub.2015.01.074
Lu J et al (2012) The earliest known stem-tetrapod from the Lower Devonian of China. Nat Commun 3:1160–1167. https://doi.org/10.1038/ncomms2170
Maeda R et al (2015) Ontogeny of the saccus vasculosus, a seasonal sensor in fish. Endocrinology 156(11):4238–4243. https://doi.org/10.1210/en.2015-1415
Masumoto K et al (2010) Acute induction of eya3 by late-night light stimulation triggers TSHβ expression in photoperiodism. Curr Biol 20(24):2199–2206. https://doi.org/10.1016/j.cub.2010.11.038
Maywood ES, Hastings MH (1995) 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 136(1):144–153. https://doi.org/10.1210/en.136.1.144
Meijer JH et al (1999) Functional absence of extraocular photoreception in hamster circadian rhythm entrainment. Brain Res 831(1–2):337–339. http://www.ncbi.nlm.nih.gov/pubmed/10412017
Migaud H, Davie A, Taylor JF (2010) Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species. J Fish Biol 76(1):27–68. https://doi.org/10.1111/j.1095-8649.2009.02500.x
Morgan PJ, Williams LM (1996) The pars tuberalis of the pituitary: a gateway for neuroendocrine output. Rev Reprod 1(3):153–161. http://www.ncbi.nlm.nih.gov/pubmed/9414453
Morgan PJ et al (1994) Melatonin receptors: localization, molecular pharmacology and physiological significance. Neurochem Int 24(2):101–146. http://www.ncbi.nlm.nih.gov/pubmed/8161940. Accessed 19 Feb 2014
Morgan PJ et al (1996) The ovine pars tuberalis secretes a factor(s) that regulates gene expression in both lactotropic and nonlactotropic pituitary cells. Endocrinology 137(9):4018–4026. https://doi.org/10.1210/endo.137.9.8756579
Murphy M et al (2012) Effects of manipulating hypothalamic triiodothyronine concentrations on seasonal body weight and torpor cycles in Siberian hamsters. Endocrinology 153(1):101–112. https://doi.org/10.1210/en.2011-1249
Nakane Y, Yoshimura T (2010) Deep brain photoreceptors and a seasonal signal transduction cascade in birds. Cell Tissue Res 342(3):341–344. https://doi.org/10.1007/s00441-010-1073-6
Nakane Y, Yoshimura T (2014) Universality and diversity in the signal transduction pathway that regulates seasonal reproduction in vertebrates. Front Neurosci 8:115. https://doi.org/10.3389/fnins.2014.00115
Nakane Y et al (2010) A mammalian neural tissue opsin (Opsin 5) is a deep brain photoreceptor in birds. Proc Natl Acad Sci 107(34):15264–15268. https://doi.org/10.1073/pnas.1006393107
Nakane Y et al (2013) The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nat Commun 4:2108. https://doi.org/10.1038/ncomms3108
Nakao N et al (2008) Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature 452(7185):317–322. https://doi.org/10.1038/nature06738
Nelson RJ, Zucker I (1981) Photoperiodic control of reproduction in olfactory-bulbectomized rats. Neuroendocrinology 32(5):266–271. http://www.ncbi.nlm.nih.gov/pubmed/7242854
Nicholls TJ et al (1988) Possible homologies between photorefractoriness in sheep and birds: the effect of thyroidectomy on the length of the ewe’s breeding season. Reprod Nutr Dev 28(2B):375–385. http://www.ncbi.nlm.nih.gov/pubmed/3413338
O’Brien CS et al (2012) Conservation of the photoperiodic neuroendocrine axis among vertebrates: evidence from the teleost fish, Gasterosteus aculeatus. Gen Comp Endocrinol 178(1):19–27. https://doi.org/10.1016/j.ygcen.2012.03.010
Ono H et al (2008) Involvement of thyrotropin in photoperiodic signal transduction in mice. Proc Natl Acad Sci U S A 105(47):18238–18242. https://doi.org/10.1073/pnas.0808952105
Parkinson TJ, Follett BK (1994) Effect of thyroidectomy upon seasonality in rams. Reproduction 101(1):51–58. https://doi.org/10.1530/jrf.0.1010051
Pelletier J et al (1992) Localization of luteinizing hormone beta-mRNA by in situ hybridization in the sheep pars tuberalis. Cell Tissue Res 267(2):301–306.http://www.ncbi.nlm.nih.gov/pubmed/1600562
Pelletier J et al (1995) Changes in LHbeta-gene and FSHbeta-gene expression in the ram pars tuberalis according to season and castration. Cell Tissue Res 281(1):127–133. http://www.ncbi.nlm.nih.gov/pubmed/16358468
Pittendrigh CS, Minis DH (1964) The entrainment of circadian oscillations by light and their role as photoperiodic clocks. Am Nat 98:261–299
Reierth E, Van’t Hof TJ, Stokkan K-A (1999) Seasonal and daily variations in plasma melatonin in the high-arctic svalbard ptarmigan (Lagopus mutus hyperboreus). J Biol Rhythm 14(4):314–319. https://doi.org/10.1177/074873099129000731
Reiter RJ (1980) Photoperiod: its importance as an impeller of pineal and seasonal reproductive rhythms. Int J Biometeorol 24(1):57–63.http://www.ncbi.nlm.nih.gov/pubmed/7189183
Reppert SM (1997) Melatonin receptors: molecular biology of a new family of G protein-coupled receptors. J Biol Rhyth 12(6):528–31. http://www.ncbi.nlm.nih.gov/pubmed/9406026
Reppert SM et al (1996a) Cloning of a melatonin-related receptor from human pituitary. FEBS Lett 386(2–3):219–224. http://www.ncbi.nlm.nih.gov/pubmed/8647286
Reppert SM, Weaver DR, Godson C (1996b) Melatonin receptors step into the light: cloning and classification of subtypes. Trends Pharmacol Sci 17(3):100–102. https://doi.org/10.1016/0165-6147(96)10005-5
Revel FG et al (2006) Melatonin regulates type 2 deiodinase gene expression in the Syrian hamster. Endocrinology 147(10):4680–4687. https://doi.org/10.1210/en.2006-0606
Richter CP (1978) Evidence for existence of a yearly clock in surgically and self-blinded chipmunks. Proc Natl Acad Sci 75(7):3517–3521. https://doi.org/10.1073/pnas.75.7.3517
Rodríguez EM et al (2005) Hypothalamic tanycytes: a key component of brain-endocrine interaction. Int Rev Cytol 247:89–164. https://doi.org/10.1016/S0074-7696(05)47003-5
Ross AW et al (2011) Thyroid hormone signalling genes are regulated by photoperiod in the hypothalamus of F344 rats. In: Yamazaki S (ed) PLoS One 6(6):e21351. https://doi.org/10.1371/journal.pone.0021351
Sáenz de Miera C et al (2013) Circannual variation in thyroid hormone deiodinases in a short-day breeder. J Neuroendocrinol 25(4):412–421. https://doi.org/10.1111/jne.12013
Sáenz de Miera C et al (2014) A circannual clock drives expression of genes central for seasonal reproduction. Curr Biol 24(13):1500–1506. https://doi.org/10.1016/j.cub.2014.05.024
Sáenz de Miera C et al (2017) Maternal photoperiod programs hypothalamic thyroid status via the fetal pituitary gland. Proc Natl Acad Sci 114(31):8408–8413. https://doi.org/10.1073/pnas.1702943114
Simonneaux V et al (2013) Kisspeptins and RFRP-3 act in concert to synchronize rodent reproduction with seasons. Front Neurosci 7:22. https://doi.org/10.3389/fnins.2013.00022
Stirland JA et al (2001) Photoperiodic regulation of prolactin gene expression in the Syrian hamster by a pars tuberalis-derived factor. J Neuroendocrinol 13(2):147–157. http://www.ncbi.nlm.nih.gov/pubmed/11168840
Stoeckel E et al (1993) Early expression of the glycoprotein hormone alpha-subunit in the pars tuberalis of the rat pituitary gland during ontogenesis. Neuroendocrinology 58(6):616–624. https://doi.org/10.1159/000126600
Stokkan K-A, Tyler NJC, Reiter RJ (1994) The pineal gland signals autumn to reindeer (Rangifer tarandus tarandus) exposed to the continuous daylight of the Arctic summer. Can J Zool 72(5):904–909. https://doi.org/10.1139/z94-123
Stokkan K-A et al (2007) Adaptations for life in the arctic: evidence that melatonin rhythms in reindeer are not driven by a circadian oscillator but remain acutely sensitive to environmental photoperiod. J Pineal Res 43(3):289–293. https://doi.org/10.1111/j.1600-079X.2007.00476.x
Strand JET et al (2008) Keeping track of time under ice and snow in a sub-arctic lake: plasma melatonin rhythms in Arctic charr overwintering under natural conditions. J Pineal Res 44(3):227–233. https://doi.org/10.1111/j.1600-079X.2007.00511.x
Tsutsui K et al (2013) Review: regulatory mechanisms of gonadotropin-inhibitory hormone (GnIH) synthesis and release in photoperiodic animals. Front Neurosci 7:60. https://doi.org/10.3389/fnins.2013.00060
Ubuka T, Bentley GE, Tsutsui K (2013) Neuroendocrine regulation of gonadotropin secretion in seasonally breeding birds. Front Neurosci 7:38. https://doi.org/10.3389/fnins.2013.00038
Unfried C et al (2009) Impact of melatonin and molecular clockwork components on the expression of thyrotropin β-chain (Tshb) and the Tsh receptor in the mouse pars tuberalis. Endocrinology 150(10):4653–4662. https://doi.org/10.1210/en.2009-0609
Viguie C (1999) Thyroid hormones act primarily within the brain to promote the seasonal inhibition of luteinizing hormone secretion in the ewe. Endocrinology 140(3):1111–1117. https://doi.org/10.1210/en.140.3.1111
Watanabe M et al (2004) Photoperiodic regulation of type 2 deiodinase gene in djungarian hamster: possible homologies between avian and mammalian photoperiodic regulation of reproduction. Endocrinology 145(4):1546–1549. https://doi.org/10.1210/en.2003-1593
Watanabe T et al (2007) Hypothalamic expression of thyroid hormone-activating and -inactivating enzyme genes in relation to photorefractoriness in birds and mammals. Am J Phys Regul Integr Comp Phys 292(1):R568–R572. https://doi.org/10.1152/ajpregu.00521.2006
Webster JR, Moenter SM, Woodfill CJ et al (1991a) Role of the thyroid gland in seasonal reproduction. II. Thyroxine allows a season-specific suppression of gonadotropin secretion in sheep. Endocrinology 129(1):176–183. https://doi.org/10.1210/endo-129-1-176
Webster JR, Moenter SM, Barrell GK et al (1991b) Role of the thyroid gland in seasonal reproduction. III. Thyroidectomy blocks seasonal suppression of gonadotropin-releasing hormone secretion in sheep. Endocrinology 129(3):1635–1643. https://doi.org/10.1210/endo-129-3-1635
West AC, Wood SH (2018) Seasonal physiology: making the future a thing of the past. Curr Opin Physiol 5:1–8. https://doi.org/10.1016/j.cophys.2018.04.006
West A et al (2013) Npas4 is activated by melatonin, and drives the clock gene Cry1 in the ovine pars tuberalis. Mol Endocrinol 27(6):979–989. https://doi.org/10.1210/me.2012-1366
Woitkewitsch A (1940) Dependence of seasonal periodicity in gonadal changes on the thyroid gland. C R Dokl Acad Sci URSS 27:741–745
Wood S, Loudon A (2014) Clocks for all seasons: unwinding the roles and mechanisms of circadian and interval timers in the hypothalamus and pituitary. J Endocrinol 222(2):R39–R59. https://doi.org/10.1530/JOE-14-0141
Wood S, Loudon A (2017) The pars tuberalis: the site of the circannual clock in mammals. Gen Comp Endocrinol 258:222–235. https://doi.org/10.1016/j.ygcen.2017.06.029
Wood SH et al (2015) Binary switching of calender cells in the pituitary defines the phase of the circannual cycle in mammals. Curr Biol 25(20). https://doi.org/10.1016/j.cub.2015.09.014
Woodfill CJ et al (1994) Photoperiodic synchronization of a circannual reproductive rhythm in sheep: identification of season-specific time cues. Biol Reprod 50(4):965–76. http://www.ncbi.nlm.nih.gov/pubmed/8199277
Yasuo S, Korf H-W (2011) The hypophysial pars tuberalis transduces photoperiodic signals via multiple pathways and messenger molecules. Gen Comp Endocrinol 172(1):15–22. https://doi.org/10.1016/j.ygcen.2010.11.006
Yasuo S et al (2009) Melatonin transmits photoperiodic signals through the MT1 melatonin receptor. J Neurosci 29(9):2885–2889. https://doi.org/10.1523/JNEUROSCI.0145-09.2009
Yasuo S et al (2014) 2-Arachidonoyl glycerol sensitizes the pars distalis and enhances forskolin-stimulated prolactin secretion in Syrian hamsters. Chronobiol Int 31(3):337–342. https://doi.org/10.3109/07420528.2013.852104
Yoshimura T (2010) Neuroendocrine mechanism of seasonal reproduction in birds and mammals. Anim Sci J 81(4):403–410. https://doi.org/10.1111/j.1740-0929.2010.00777.x
Yoshimura T (2013) Thyroid hormone and seasonal regulation of reproduction. Front Neuroendocrinol 34(3):157–166. https://doi.org/10.1016/j.yfrne.2013.04.002
Yoshimura T et al (2003) Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature 426(6963):178–181. https://doi.org/10.1038/nature02117
Zucker I (1985) Pineal gland influences period of circannual rhythms of ground squirrels. Am J Physiol 249(1 Pt 2):R111–R115. http://www.ncbi.nlm.nih.gov/pubmed/4014491
Recommended Further Reading
Dardente H, Wood S, Ebling FJ, Sáenz de Miera C (2019) An integrative view of mammalian seasonal neuroendocrinology. J Neuroendocrinol 31(5):e12729. https://doi.org/10.1111/jne.12729. A very recent detailed open access review of the pars tuberalis and associated mechanisms underlying seasonality in mammals.
David A. Freeman, Brett J. W. Teubner, Carlesia D. Smith, Brian J. Prendergast, (2007) Exogenous Tmimics long day lengths in Siberian hamsters. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 292 (6):R2368-R2372
Hazlerigg DG, Lincoln GA (2011) Hypothesis: cyclical histogenesis is the basis of circannual timing. J Biol Rhythms 26:471–485. https://doi.org/10.1177/0748730411420812. An influential review proposing the hypothesis that circannual rhythm generation depends on tissue-autonomous, reiterated cycles of cell division, functional differentiation, and cell death, using the pars tuberalis in mammals as a prime example.
Wood SH, Christian HC, Miedzinska K, Saer BR, Johnson M, Paton B, Yu L, McNeilly J, Davis JR, McNeilly AS, Burt DW, Loudon AS (2015) Binary switching of calendar cells in the pituitary defines the phase of the circannual cycle in mammals. Curr Biol 25: 2651–2662. https://doi.org/10.1016/j.cub.2015.09.014. A primary research paper providing substantial evidence that thyrotrophs in the sheep pars tuberalis transition between two states, resulting in a morphological plasticity that underpins circannual rhythmicity.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Wood, S.H. (2020). The Pars Tuberalis and Seasonal Timing. In: Ebling, F.J.P., Piggins, H.D. (eds) Neuroendocrine Clocks and Calendars. Masterclass in Neuroendocrinology, vol 10. Springer, Cham. https://doi.org/10.1007/978-3-030-55643-3_2
Download citation
DOI: https://doi.org/10.1007/978-3-030-55643-3_2
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-55642-6
Online ISBN: 978-3-030-55643-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)