Universality and diversity in the signal transduction pathway that regulates seasonal reproduction in vertebrates

Frontiers in Neuroscience

Volumn , Issue 8 MAY, 2014, Pages

  Nakane, Yusuke ^a   Yoshimura, Takashi ^a,b  

^a NAGOYA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

Cerebrospinal fluid contacting neuron; Circadian rhythm; Coronet cell; Deep brain photoreceptor; Pars tuberalis; Saccus vasculosus; Thyroid hormone; Thyroid stimulating hormone

Indexed keywords

MELATONIN; MELATONIN RECEPTOR; OPSIN; THYROID HORMONE; THYROTROPIN; THYROXINE;

BIRD; BRAIN DEVELOPMENT; CEREBROSPINAL FLUID; CIRCADIAN RHYTHM; COTURNIX JAPONICA; FUNCTIONAL GENOMICS; HYPOPHYSIS; HYPOPHYSIS PARS TUBERALIS; MEDIOBASAL HYPOTHALAMUS; NONHUMAN; ONCORHYNCHUS MASOU; PHOTOPERIODICITY; PHOTORECEPTOR; PINEAL BODY; REPRODUCTION; REVIEW; SEASONAL REPRODUCTION; SEASONAL VARIATION; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS; VERTEBRATE;

EID: 84905050809     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2014.00115     Document Type: Review

References (76)

1. Arendt, D. (2008). The evolution of cell types in animals: emerging principles from molecular studies. Nat. Rev. Genet. 9, 868-882. doi: 10.1038/nrg2416.
2. Barrett, P., Ebling, F. J., Schuhler, S., Wilson, D., Ross, A. W., Warner, A., et al. (2007). Hypothalamic thyroid hormone catabolism acts as a gatekeeper for the seasonal control of body weight and reproduction. Endocrinology 148, 3608-3617. doi: 10.1210/en.2007-0316.
3. Benoit, J. (1935). Le role des yeux dans l'action stimulante de la lumiere sure le developpement testiulaire chez le canard. CR. Soc. Bio. (Paris.) 118, 669-671.
4. Bernal, J. (2005). Thyroid hormones and brain development. Vitam. Horm. 71, 95-122. doi: 10.1016/S0083-6729(05)71004-9.
5. Borg, B. (2010). "Photoperiodism in fishes," in Photoperiodism: The Biological Calendar, eds R. J. Nelson, D. L. Denlinger, and D. E. Somers (New York, NY: Oxford University Press), 371-398.
6. Chaurasia, S. S., Rollag, M. D., Jiang, G., Hayes, W. P., Haque, R., Natesan, A., et al. (2005). Molecular cloning, localization and circadian expression of chicken melanopsin (Opn4): differential regulation of expression in pineal and retinal cell types. J. Neurochem. 92, 158-170. doi: 10.1111/j.1471-4159.2004.02874.x.
7. Clarke, I. J., Sari, I. P., Qi, Y., Smith, J. T., Parkington, H. C., Ubuka, T., Iqbal, J., et al. (2008). Potent action of RFamide-related peptide-3 on pituitary gonadotropes indicative of a hypophysiotropic role in the negative regulation of gonadotropin secretion. Endocrinology 149, 5811-5821. doi: 10.1210/en.2008-0575.
8. Clements, M. K., McDonald, T. P., Wang, R., Xie, G., O'Dowd, B. F., George, S. R., et al. (2001). FMRFamide-related neuropeptides are agonists of the orphan G-protein-coupled receptor GPR54. Biochem. Biophys. Res. Commun. 284, 1189-1193. doi: 10.1006/bbrc.2001.5098.
9. Collins, S. (1685). A Systeme of Anatomy. London: Thomas Newcomb.
10. Dardente, H., Klosen, P., Pévet, P., and Masson-Pévet, M. (2003). MT1 melatonin receptor mRNA expressing cells in the pars tuberalis of the European hamster: effect of photoperiod. J. Neuroendocrinol. 15, 778-786. doi: 10.1046/j.1365-2826.2003.01060.x.
11. Davies, D. T., and Follett, B. K. (1975). Electrical stimulation of the hypothalamus and luteinizing hormone secretion in Japanese quail. J. Endocrinol. 67, 431-443. doi: 10.1677/joe.0.0670431.
12. Falcón, J., Besseau, L., Fuentès, M., Sauzet, S., Magnanou, E., and Boeuf, G. (2009). Structural and functional evolution of the pineal melatonin system in vertebrates. Ann. N. Y. Acad. Sci. 1163, 101-111. doi: 10.1111/j.1749-6632.2009.04435.x.
13. Foster, R. G., and Follett, B. K. (1985). The involvement of a rhodopsin-like photopigment in the photoperiodic response of the Japanese quail. J. Comp. Physiol. A 157, 519-528. doi: 10.1007/BF00615153.
14. Freeman, D. A., Teubner, B. J., Smith, C. D., and Prendergast, B. J. (2007). Exogenous T3 mimics long day lengths in Siberian hamsters. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, 2368-2372. doi: 10.1152/ajpregu.00713.2006.
15. Fukuhara, C., and Tosini, G. (2003). Induction of photosensitivity in cultured rat pineal affects Aa-nat regulation. Brain Res. Dev. Brain Res. 142, 219-221. doi: 10.1016/S0165-3806(03)00067-1.
16. Garg, S. K. (1989). Effect of pinealectomy, eye enucleation, and melatonin treatment on ovarian activity and vitellogenin levels in the catfish exposed to short photoperiod or long photoperiod. J. Pineal. Res. 7, 91-104. doi: 10.1111/j.1600-079X.1989.tb00658.x.
17. Halford, S., Pires, S. S., Turton, M., Zheng, L., González-Menéndez, I., Davies, W. L., et al. (2009). VA opsin-based photoreceptors in the hypothalamus of birds. Curr. Biol. 19, 1396-1402. doi: 10.1016/j.cub.2009.06.066.
18. Hanon, E. A., Lincoln, G. A., Fustin, J. M., Dardente, H., Masson-Pévet, M., Morgan, P. J., et al. (2008). Ancestral TSH mechanism signals summer in a photoperiodic mammal. Curr. Biol. 18, 1147-1152. doi: 10.1016/j.cub.2008.06.076.
19. Hartwig, H. G., and van Veen, T. (1979). Spectral characteristics of visible radiation penetrating into the brain and stimulating extraretinal photoreceptors. J. Comp. Physiol. 130, 277-282. doi: 10.1007/BF00614615.
20. Henson, J. R., Carter, S. N., and Freeman, D. A. (2013). Exogenous T3 elicits long day-like alterations in testis size and the RFamides Kisspeptin and gonadotropin-inhibitory hormone in short-day Siberian hamsters. J. Biol. Rhythms 28, 193-200. doi: 10.1177/0748730413487974.
21. Homma, K., Ohta, M., and Sakakibara, Y. (1979). "Photoinducible phase of the Japanese quail detected by direct stimulation of the brain," in Biological Rhythms and their Central Mechanism, eds M. Suda, O. Hayaishi, and H. Nakagawa (Amsterdam: Elsevier, North-Holland Biomedical Press), 85-94.
22. Jansen, W. F., Burger, E. H., and Zandbergen, M. A. (1982). Subcellular localization of calcium in the coronet cells and tanycytes of the saccus vasculosus of the rainbow trout, Salmo gairdneri. Ann. N. Y. Acad. Sci. 117, 217-227..
23. Klosen, P., Bienvenu, C., Demarteau, O., Dardente, H., Guerrero, H., Pévet, P., et al. (2002). The mt1 melatonin receptor and RORb receptor are co-localized in specific TSH-immunoreactive cells in the pars tuberalis of the rat pituitary. J. Histochem. Cytochem. 50, 1647-1657. doi: 10.1177/002215540205001209.
24. Klosen, P., Sébert, M. E., Rasri, K., Laran-Chich, M. P., and Simonneaux, V. (2013). TSH restores a summer phenotype in photoinhibited mammals via the RF-amides RFRP3 and kisspeptin. FASEB J. 27, 2677-2686. doi: 10.1096/fj.13-229559.
25. Koger, C. S., Teh, S. J., and Hinton, D. E. (1999). Variations of light and temperature regimes and resulting effects on reproductive parameters in medaka (Oryzias latipes). Biol. Reprod. 61, 1287-1293. doi: 10.1095/biolreprod61.5.1287.
26. Konishi, H., Foster, R. G., and Follett, B. K. (1987). Evidence for a daily rhythmicity in the acute release of LH in response to electrical stimulation in the Japanese quail. J. Comp. Physiol. A 161, 315-319. doi: 10.1007/BF00615251.
27. Korf, H. W. (1994). The pineal organ as a component of the biological clock. Phylogenetic and ontogenetic considerations. Ann. N. Y. Acad. Sci. 31, 13-42. doi: 10.1111/j.1749-6632.1994.tb56818.x.
28. Kotani, M., Detheux, M., Vandenbogaerde, A., Communi, D., Vanderwinden, J. M., Le Poul, E., et al. (2001). The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J. Biol. Chem. 276, 34631-34636. doi: 10.1074/jbc.M104847200.
29. Masuda, T., Iigo, M., and Aida, K. (2005). Existence of an extra-retinal and extra-pineal photoreceptive organ that regulates photoperiodism in gonadal development of an Osmerid teleost, ayu (Plecoglossus altivelis). Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 140, 414-422. doi: 10.1016/j.cbpb.2005.01.004.
30. Meddle, S. L., and Follett, B. K. (1995). Photoperiodic activation of fos-like immunoreactive protein in neurones within the tuberal hypothalamus of Japanese quail. J. Comp. Physiol. A. 176, 79-89. doi: 10.1007/BF00197754.
31. Meddle, S. L., and Follett, B. K. (1997). Photoperiodically driven changes in Fos expression within the basal tuberal hypothalamus and median eminence of Japanese quail. J. Neurosci. 17, 8909-8918..
32. Menaker, M., Roberts, R., Elliott, J., and Underwood, H. (1970). Extraretinal light perception in the sparrow. III. The eyes do not participate in photoperiodic photoreception. Proc. Natl. Acad. Sci. U.S.A. 67, 320-325. doi: 10.1073/pnas.67.1.320.
33. Moenter, S. M., Woodfill, C. J., and Karsch, F. J. (1991). Role of the thyroid gland in seasonal reproduction: thyroidectomy blocks seasonal suppression of reproductive neuroendocrine activity in ewes. Endocrinology 128, 1337-1344. doi: 10.1210/endo-128-3-1337.
34. Muir, A. I., Chamberlain, L., Elshourbagy, N. A., Michalovich, D., Moore, D. J., Calamari, A., et al. (2001). AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J. Biol. Chem. 276, 28969-28975. doi: 10.1074/jbc.M102743200.
35. Nakane, Y., Ikegami, K., Iigo, M., Ono, H., Takeda, K., Takahashi, D., et al. (2013). The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nat. Commun. 4, 2108. doi: 10.1038/ncomms3108.
36. Nakane, Y., Ikegami, K., Ono, H., Yamamoto, N., Yoshida, S., Hirunagi, K., et al. (2010). A novel mammalian neural tissue opsin (Opsin5) is a deep brain photoreceptor in birds. Proc. Natl. Acad. Sci. U.S.A. 107, 15264-15268. doi: 10.1073/pnas.1006393107.
37. Nakao, N., Ono, H., Yamamura, T., Anraku, T., Takagi, T., Higashi, K., et al. (2008). Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature 452, 317-311. doi: 10.1038/nature06738.
38. Nicholls, T. J., Follett, B. K., Goldsmith, A. R., and Pearson, H. (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, 375-385. doi: 10.1051/rnd:19880304.
39. Nicholls, T. J., Follett, B. K., and Robinson, J. E. (1983). A photoperiodic response in gonadectomized Japanese quail exposed to a single long day. J. Endocrinol. 97, 121-126. doi: 10.1677/joe.0.0970121.
40. Nishikawa, K., Hirashima, T., Suzuki, S., and Suzuki, M. (1979). Changes in circulating L-thyroxine and L-triiodothyronine of the masu salmon, Oncorhynchus masou accompaning the smoltification, measured by radioimmunoassay. Endocrinol. Jpn. 26, 731-735. doi: 10.1507/endocrj1954.26.731.
41. Ohta, M., Wada, M., and Homma, K. (1984). Induction of rapid testicular growth in quail by phasic electrical stimulation of the hypothalamic photosensitive area. J. Comp. Physiol. A 154, 583-589. doi: 10.1007/BF00610171.
42. Ohtaki, T., Shintani, Y., Honda, S., Matsumoto, H., Hori, A., Kanehashi, K., et al. (2001). Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 411, 613-617. doi: 10.1038/35079135.
43. Oishi, T., and Ohashi, K. (1993). Effects of wavelengths of light on the photoperiodic gonadal response of blinded-pinealectomized Japanese quail. Zoolog. Sci. 10, 757-762.
44. Ono, H., Hoshino, Y., Yasuo, S., Watanabe, M., Nakane, Y., Murai, A., et al. (2008). Involvement of thyrotropin in photoperiodic signal transduction in mice. Proc. Natl. Acad. Sci. U.S.A. 105, 18238-18242. doi: 10.1073/pnas.0808952105.
45. Reiter, R. J. (1980). The pineal and its hormones in the control of reproduction in mammals. Endocr. Rev. 1, 109-131. doi: 10.1210/edrv-1-2-109.
46. Reppert, S. M., Weaver, D. R., and Ebisawa, T. (1994). Cloning and characterization of a mammalian melatonin receptor that mediates reproductive and circadian responses. Neuron 13, 1177-1185. doi: 10.1016/0896-6273(94)90055-8.
47. Revel, F. G., Saboureau, M., Pévet, P., Mikkelsen, J. D., and Simonneaux, V. (2006). Melatonin regulates type 2 deiodinase gene expression in the Syrian hamster. Endocrinology 147, 4680-4687. doi: 10.1210/en.2006-0606.
48. Revel, R. G., Saboureau, M., Pévet, P., Simonneaux, V., and Mikkelsen, J. D. (2008). RFamide-related peptide gene is a melatonin-driven photoperiodic gene. Endocrinology 149, 902-912. doi: 10.1210/en.2007-0848.
49. Robertson, O. H. (1949). Production of the silvery smolt stage in rainbow trout by intramuscular injection of mammalian thyroid extract and thyrotropic hormone. J. Exp. Zool. 110, 337-355 doi: 10.1002/jez.1401100303.
50. Schuster, C., Gauer, F., Guerrero, H., Lakhdar-Ghazal, N., Pévet, P., and Masson-Pévet, M. (2000). Photic regulation of mt1 melatonin receptors in the Siberian hamster pars tuberalis and suprachiasmatic nuclei: involvement of the circadian clock and intergeniculate leaflet. J. Neuroendocrinol. 12, 207-216. doi: 10.1046/j.1365-2826.2000.00039.x.
51. Sharp, P. J., and Follett, B. K. (1969). The effect of hypothalamic lesions on gonadotrophin release in Japanese quail (Coturnix coturnix japonica). Neuroendocrinology 5, 205-218. doi: 10.1159/000121861.
52. Silver, R., Witkovsky, P., Horvath, P., Alones, V., Barnstable, C. J., and Lehman, M. N. (1988). Coexpression of opsin- and VIP-like-immunoreactivity in CSF-contacting neurons of the avian brain. Cell Tissue Res. 253, 189-198. doi: 10.1007/BF00221754.
53. Siopes, T. D., and Wilson, W. O. (1974). Extraocular modification of photoreception in intact and pinealectomized coturnix. Poult. Sci. 53, 2035-2041. doi: 10.3382/ps.0532035.
54. Song, C. K., and Bartness, T. J. (2001). CNS sympathetic outflow neurons to white fat that express MEL receptors may mediate seasonal adiposity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281, R666-R672..
55. Sueiro, C., Carrera, I., Ferreiro, S., Molist, P., Adrio, F., Anadón, R., et al. (2007). New insights on saccus vasculosus evolution: a developmental and immunohistochemical study in Elasmobranchs. Brain Behav. Evol. 70, 187-204. doi: 10.1159/000104309.
56. Tosini, G., Doyle, S., Geusz, M., and Menaker, M. (2000). Induction of photosensitivity in neonatal rat pineal gland. Proc. Natl. Acad. Sci. U.S.A. 97, 11540-11544. doi: 10.1073/pnas.210248297.
57. Urasaki, H. (1976). The role of pineal and eyes in the photoperiodic effect on the gonad of the medaka, Oryzias latipes. Chronobiologia 3, 228-234..
58. Vigh, B., and Vigh-Teichmann, I. (1998). Actual problems of the cerebrospinal fluid-contacting neurons. Microsc. Res. Tech. 41, 57-83.
59. Vigh-Teichmann, I., Röhlich, P., Vigh, B., and Aros, B. (1980). Comparison of the pineal complex, retina and cerebrospinal fluid contacting neurons by immunocytochemical antirhodopsin reaction. Z. Mikrosk. Anat. Forsch. 94, 623-640..
60. von Frisch, K. (1911). Beitrage zur physiologie der pigmentzellen in der fischhaut. Pflü. Arch. Gesammte. Physiol. Menschen. Tiere. 138, 319-387. doi: 10.1007/BF01680752.
61. Wada, Y., Okano, T., Adachi, A., Ebihara, S., and Fukada, Y. (1998). Identification of rhodopsin in the pigeon deep brain. FEBS Lett. 424, 53-56. doi: 10.1016/S0014-5793(98)00138-0.
62. Watanabe, M., Yasuo, S., Watanabe, T., Yamamura, T., Nakao, N., Ebihara, S., 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, 1546-1549. doi: 10.1210/en.2003-1593.
63. Watanabe, T., Yamamura, T., Watanabe, M., Yasuo, S., Nakao, N., Dawson, A., et al. (2007). 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. 292, 568-572. doi: 10.1152/ajpregu.00521.2006.
64. Williams, L. M., and Morgan, P. J. (1988). Demonstration of melatonin-binding sites on the pars tuberalis of the rat. J. Endocrinol. 119, 1-3. doi: 10.1677/joe.0.119R001.
65. Wittkowski, W., Bergmann, M., Hoffmann, K., and Pera, F. (1988). Photoperiod-dependent changes in TSH-like immunoreactivity of cells in the hypophysial pars tuberalis of the Djungarian hamster, Phodopus sungorus. Cell Tissue Res. 251, 183-187. doi: 10.1007/BF00215463.
66. Yamamura, T., Yasuo, S., Hirunagi, K., Ebihara, S., and Yoshimura, T. (2006). 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. doi: 10.1007/s00441-005-0126-8.
67. Yamashita, T., Ohuchi, H., Tomonari, S., Ikeda, K., Sakai, K., and Shichida, Y. (2010). Opn5 is a UV-sensitive bistable pigment that couples with Gi subtype of G protein. Proc. Natl. Acad. Sci. U.S.A. 107, 22084-22089. doi: 10.1073/pnas.1012498107.
68. Yamazaki, S., Goto, M., and Menaker, M. (1999). No evidence for extraocular photoreceptors in the circadian system of the Syrian hamster. J. Biol. Rhythms 14, 197-201. doi: 10.1177/074873099129000605.
69. Yasuo, S., Nakao, N., Ohkura, S., Iigo, M., Hagiwara, S., Goto, A., et al. (2006). Long-day suppressed expression of type 2 deiodinase gene in the mediobasal hypothalamus of the Saanen goat, a short-day breeder: Implication for seasonal window of thyroid hormone action on reproductive neuroendocrine axis. Endocrinology 147, 432-440. doi: 10.1210/en.2005-0507.
70. Yasuo, S., Watanabe, M., Iigo, M., Nakamura, T. J., Watanabe, T., Takagi, T., et al. (2007b). Differential response of type 2 deiodinase gene expression tophotoperiod between photoperiodic Fischer 344 and nonphotoperiodic Wistar rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, 1315-1319. doi: 10.1152/ajpregu.00396.2006.
71. Yasuo, S., Watanabe, M., Nakao, N., Takagi, T., Follett, B. K., Ebihara, S., et al. (2005). The reciprocal switching of two thyroid hormone-activating and -inactivating enzyme genes is involved in the photoperiodic gonadal response of Japanese quail. Endocrinology 146, 2551-2554. doi: 10.1210/en.2005-0057.
72. Yasuo, S., Yoshimura, T., Ebihara, S., and Kolf, H. W. (2009). Melatonin transmits photoperiodic signals through the MT1 melatonin receptor. J. Neurosci. 29, 2885-2889. doi: 10.1523/JNEUROSCI.0145-09.2009.
73. Yasuo, S., Yoshimura, T., Ebihara, S., and Korf, H. W. (2007a). Temporal dynamics of type 2 deiodinase expression after melatonin injections in Syrian hamsters. Endocrinology 148, 3608-3617. doi: 10.1210/en.2007-0497.
74. Yokoyama, K., Oksche, A., Darden, T. R., and Farner, D. S. (1978). The sites of encephalic photoreception in phosoperiodic induction of the growth of the testes in the white-crowned sparrow. Zonotrichia leucophrys gambelii. Cell Tissue Res. 189, 441-467. doi: 10.1007/BF00209132.
75. Yoshimura, T., Yasuo, S., Watanabe, M., Iigo, M., Yamamura, T., Hirunagi, K., et al. (2003). Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature 426, 178-181. doi: 10.1038/nature02117.
76. Zweig, M., Snyder, S. H., and Axelrod, J. (1966). Evidence for a nonretinal pathway of light to the pineal gland of newborn rats. Proc. Natl. Acad. Sci. U.S.A. 56, 515-520. doi: 10.1073/pnas.56.2.515