Abstract
Photoperiodically generated triiodothyronin (T3) in the mediobasal hypothalamus (MBH) has critical roles in the photoperiodic response of the gonads in Japanese quail. In a previous study, we demonstrated seasonal morphological changes in the neuro-glial interaction between gonadotrophin-releasing hormone (GnRH) nerve terminals and glial endfeet in the median eminence (ME). However, a direct relationship between photoperiodically generated T3 and seasonal neuro-glial plasticity in the ME remained unclear. In the present study, we examined the effect of T3 implantation into the MBH on the neuro-glial interaction in the ME. T3 implantation caused testicular growth and reduced encasement of nerve terminals in the external zone of the ME. In contrast, no morphological changes were observed in birds given an excessive dose of T3, which did not cause testicular growth. These results support the hypothesis that thyroid hormone regulates photoperiodic GnRH secretion via neuro-glial plasticity in the ME.
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References
Baylé JD, Ramade F, Oliver J (1974) Stereotaxic topography of the brain of the quail (Coturnix coturnix japonica). J Physiol (Lond) 68:219–241
Bernal J (2002) Action of thyroid hormone in brain. J Endocrinol Invest 25:268–288
Davies DT, Follett BK (1975) The neuroendocrine control of gonadotrophin release in Japanese quail. I. The role of the tuberal hypothalamus. Proc R Soc Lond (Biol) 191:303–315
Dawson A, King VM, Bentley GE, Ball GF (2001) Photoperiodic control of seasonality in birds. J Biol Rhythms 16:365–380
Dawson A, Thapliyal JP (2001) The thyroid and photoperiodism. In: Dawson A, Chatruvedi CM (eds) Avian endocrinology. Narosa, New Delhi, pp 141–151
Dhandapani KM, Mahesh VB, Brann DW (2003) Minireview: astrocytes and brain function: implications for reproduction. Exp Biol Med 228:253–260
Garcia-Segura LM, McCarthy MM (2004) Minireview: role of glia in neuroendocrine function. Endocrinology 145:1082–1086
Gould E, Allan MD, McEwen BS (1990) Dendritic spine density of adult hippocampal pyramidal cells is sensitive to thyroid hormone. Brain Res 525:327–329
Granholm AC (1985) Effects of thyroid hormone deficiency on glial constituents in developing cerebellum of the rat. Exp Brain Res 59:451–456
Hökfelt T (1973) Possible site of action of dopamine in the hypothalamic pituitary control. Acta Physiol Scand 89:606–608
Hökfelt T, Everitt B, Meister B, Melander T, Schalling M, Johansson O, Lundberg JM, Hulting AL, Werner S, Cuello C, Hemmings H, Ouimet C, Walaas I, Greengard P, Goldstein M (1986) Neurons with multiple messengers with special reference in neuroendocrine systems. Recent Prog Horm Res 42:1–70
Juss TS (1993) Neuroendocrine and neural changes associated with the photoperiodic control of reproduction. In: Sharp PJ (ed) Avian endocrinology. Society for Endocrinology, Bristol, pp 47–60
King JC, Letourneau RJ (1994) Luteinizing hormone-releasing hormone terminals in the median eminence of rats undergo dramatic changes after gonadectomy, as revealed by electron microscopic image analysis. Endocrinology 134:1340–1351
King JC, Rubin BS (1994) Dynamic changes in LHRH neurovascular terminals with various endocrine conditions in adults. Horm Behav 28:349–356
King JC, Rubin BS (1995) Dynamic alterations in luteinizing hormone-releasing hormone (LHRH) neuronal cell bodies and terminals of adult rats. Cell Mol Neurobiol 15:89–106
Kozlowski GP, Coates PW (1985) Ependymoneuronal specializations between LHRH fibers and cells of the cerebroventricular system. Cell Tissue Res 242:301–311
Krisch B (1986) Ultrastructure of regulatory neuroendocrine neurons and functionally related structure. In: Ganten D, Pfaff D (eds) Current topics in neuroendocrinology. Springer, Berlin Heidelberg New York, pp 251–290
Meddle SL, Follett BK (1995) Photoperiodic activation of Fos-like immunoreactive protein in neurons within the tuberal hypothalamus of Japanese quail. J Comp Physiol [A] 176:79–89
Meddle SL, Follett BK (1997) Photoperiodically driven changes in Fos expression within the basal tuberal hypothalamus and median eminence of Japanese quail. J Neurosci 17:8909–8918
Prevot V (2002) Glial-neuronal-endothelial interactions are involved in the control of GnRH secretion. J Neuroendocrinol 14:247–255
Prevot V, Croix D, Bouret S, Dutoit S, Tramu G, Stefano GB, Beauvillain JC (1999) Definitive evidence for the existence of morphological plasticity in the external zone of the median eminence during the rat estrous cycle: implication of neuro-glio-endothelial interactions in gonadotropin-releasing hormone release. Neuroscience 94:809–819
Ruiz-Marcos A, Cartagena Abella P, García García A, Escobar del Rey F, Morreale de Escobar G (1988) Rapid effects of adult-onset hypothyroidism on dendritic spines of pyramidal cells of the rat cerebral cortex. Exp Brain Res 73:583–588
Sharp PJ, Follett BK (1969) The effect of hypothalamic lesions on gonadotrophin release in Japanese quail (Coturnix coturnix japonica). Neuroendocrinology 5:205–218
Silver R, Witkovsky P, Horvath P, Alones V, Barnstable CJ, Lehman MN (1988) Coexpression of opsin- and VIP-like-immunoreactivity in CSF-contacting neurons of the avian brain. Cell Tissue Res 253:189–198
Slotkin TA, Slepetis RJ (1984) Obligatory role of thyroid hormones in development of peripheral sympathetic and central nervous system catecholaminergic neurons: effect of propylthiouracil-induced hypothyroidism on transmitter levels, turnover and release. J Pharmacol Exp Ther 230:53–61
Tekumalla PK, Tontonoz M, Hesla MA, Kim JR (2002) Effect of excess thyroid hormone on cell death, cell proliferation, and new neuron incorporation in the adult zebra finch telencephalon. J Neurobiol 51:323–341
Wilson FE, Reinert BD (2000) Thyroid hormone acts centrally to programme photostimulated male American tree sparrows (Spizella arborea) for vernal and autumnal components of seasonality. J Neuroendocrinol 12:87–95
Wittkowski W (1998) Tanycytes and pituicytes: morphological and functional aspects of neuroglial interaction. Microsc Res Tech 41:29–42
Yamamura T, Hirunagi K, Ebihara S, Yoshimura T (2004) Seasonal morphological changes in the neuro-glial interaction between gonadotropin-releasing hormone nerve terminals and glial endfeet in Japanese quail. Endocrinology 145:4264–4267
Yasuo S, Watanabe M, Okabayashi N, Ebihara S, Yoshimura T (2003) Circadian clock genes and photoperiodism: comprehensive analysis of clock genes expression in the mediobasal hypothalamus, the suprachiasmatic nucleus and the pineal gland of Japanese quail under various light schedules. Endocrinology 144:3742–3748
Yoshimura T, Yasuo S, Watanabe M, Iigo M, Yamamura T, Hirunagi K, Ebihara S (2003) Light induced T4-to-T3 conversion regulates photoperiodic response of gonads in birds. Nature 426:178–181
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T. Yoshimura was supported by the Program for Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN) and a Grant-in-Aid for Encouragement of Young Scientists from the Ministry of Education, Science, Sports, and Culture, Japan.
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Yamamura, T., Yasuo, S., Hirunagi, K. et al. T3 implantation mimics photoperiodically reduced encasement of nerve terminals by glial processes in the median eminence of Japanese quail. Cell Tissue Res 324, 175–179 (2006). https://doi.org/10.1007/s00441-005-0126-8
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DOI: https://doi.org/10.1007/s00441-005-0126-8