Action spectrum for photoperiodic control of thyroid-stimulating hormone in Japanese quail (Coturnix japonica)

English version

Autoři: Yusuke Nakane ^aff001; Ai Shinomiya ^aff003; Wataru Ota ^aff001; Keisuke Ikegami ^aff002; Tsuyoshi Shimmura ^aff003; Sho-Ichi Higashi ^aff006; Yasuhiro Kamei ^aff006; Takashi Yoshimura ^aff001
Působiště autorů: Institute of Transformative Bio-molecules (WPI-ITbM), Nagoya University, Nagoya, Japan ^aff001; Laboratory of Animal Integrative Physiology, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan ^aff002; Division of Seasonal Biology, National Institute for Basic Biology, Okazaki, Japan ^aff003; Department of Physiology, School of Medicine, Aichi Medical University, Nagakute, Japan ^aff004; Department of Agriculture, Tokyo University of Agriculture and Technology, Fuchu Japan ^aff005; Spectrography and Bioimaging Facility, National Institute for Basic Biology, Okazaki, Japan ^aff006; Avian Bioscience Research Center, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan ^aff007
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222106

Souhrn

At higher latitudes, vertebrates exhibit a seasonal cycle of reproduction in response to changes in day-length, referred to as photoperiodism. Extended day-length induces thyroid-stimulating hormone in the pars tuberalis of the pituitary gland. This hormone triggers the local activation of thyroid hormone in the mediobasal hypothalamus and eventually induces gonadal development. In avian species, light information associated with day-length is detected through photoreceptors located in deep-brain regions. Within these regions, the expressions of multiple photoreceptive molecules, opsins, have been observed. However, even though the Japanese quail is an excellent model for photoperiodism because of its robust and significant seasonal responses in reproduction, a comprehensive understanding of photoreceptors in the quail brain remains undeveloped. In this study, we initially analyzed an action spectrum using photoperiodically induced expression of the beta subunit genes of thyroid-stimulating hormone in quail. Among seven wavelengths examined, we detected maximum sensitivity of the action spectrum at 500 nm. The low value for goodness of fit in the alignment with a template of retinal1-based photopigment, assuming a spectrum associated with a single opsin, proposed the possible involvement of multiple opsins rather than a single opsin. Analysis of gene expression in the septal region and hypothalamus, regions hypothesized to be photosensitive in quail, revealed mRNA expression of a mammal-like melanopsin in the infundibular nucleus within the mediobasal hypothalamus. However, no significant diurnal changes were observed for genes in the infundibular nucleus. Xenopus-like melanopsin, a further isoform of melanopsin in birds, was detected in neither the septal region nor the infundibular nucleus. These results suggest that the mammal-like melanopsin expressed in the infundibular nucleus within the mediobasal hypothalamus could be candidate deep-brain photoreceptive molecule in Japanese quail. Investigation of the functional involvement of mammal-like melanopsin-expressing cells in photoperiodism will be required for further conclusions.

Klíčová slova:

Biology and life sciences – Cell biology – Biochemistry – Organisms – Eukaryota – Physical sciences – Research and analysis methods – Neuroscience – Psychology – Animals – Social sciences – Cellular types – Animal cells – Anatomy – Medicine and health sciences – Vertebrates – Amniotes – Mathematical and statistical techniques – Hormones – Physics – Peptide hormones – Brain – Electromagnetic radiation – Light – Cellular neuroscience – Neurons – Birds – Fowl – Gamefowl – Quails – Hypothalamus – Afferent neurons – Photoreceptors – Signal transduction – Sensory receptors – Sensory perception – Thyroid-stimulating hormone – Mathematical functions – Curve fitting

Zdroje

1. Nakao N, Ono H, Yamamura T, Anraku T, Takagi T, Higashi K, et al. Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature. 2008;452(7185):317. doi: 10.1038/nature06738 18354476

2. Yoshimura T, Yasuo S, Watanabe M, Iigo M, Yamamura T, Hirunagi K, et al. Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature. 2003 Nov;426(6963):178–81. 14614506

3. Yamamura T, Hirunagi K, Ebihara S, Yoshimura T. Seasonal morphological changes in the neuro-glial interaction between gonadotropin-releasing hormone nerve terminals and glial endfeet in Japanese quail. Endocrinology. 2004 Sep;145(9):4264–7. 15178649

4. Yasuo S, Watanabe M, Iigo M, Nakamura TJ, Watanabe T, Takagi T, et al. Differential response of type 2 deiodinase gene expression to photoperiod between photoperiodic Fischer 344 and nonphotoperiodic Wistar rats. Am J Physiol Regul Integr Comp Physiol. 2007 Mar;292(3):R1315–1319. 17110533

5. Hanon EA, Lincoln GA, Fustin J-M, Dardente H, Masson-Pévet M, Morgan PJ, et al. Ancestral TSH mechanism signals summer in a photoperiodic mammal. Curr Biol. 2008 Aug;18(15):1147–52. doi: 10.1016/j.cub.2008.06.076 18674911

6. Ono H, Hoshino Y, Yasuo S, Watanabe M, Nakane Y, Murai A, et al. Involvement of thyrotropin in photoperiodic signal transduction in mice. Proc Natl Acad Sci USA. 2008 Nov;105(47):18238–42. doi: 10.1073/pnas.0808952105 19015516

7. Nakane Y, Ikegami K, Iigo M, Ono H, Takeda K, Takahashi D, et al. The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nat Commun. 2013;4:2108. doi: 10.1038/ncomms3108 23820554

8. Menaker M, Roberts R, Elliott J, Underwood H. Extraretinal light perception in the sparrow. 3. The eyes do not participate in photoperiodic photoreception. Proc Natl Acad Sci USA. 1970 Sep;67(1):320–5. doi: 10.1073/pnas.67.1.320 5272320

9. Siopes TD, Wilson WO. Extraocular modification of photoreception in intact and pinealectomized coturnix. Poult Sci. 1974 Nov;53(6):2035–41. 4462102

10. von Frisch K. Beiträge zur Physiologie der Pigmentzellen in der Fischhaut. Pflüger’s, Arch. 1911 Feb 1;138(7):319–87.

11. Benoit J. Le role des yeux dans l’action stimulante de la lumiere sure le developpement testiulaire chez le canard. CR Soc Biol (Paris). 1935;118:669–671.

12. Yokoyama K, Oksche A, Darden TR, Farner DS. The sites of encephalic photoreception in photoperiodic induction of the growth of the testes in the White-crowned Sparrow, Zonotrichia leucophrys gambelii. Cell Tissue Res. 1978 Jun 1;189(3):441–67. 657255

13. Homma K M Ohta, Sakakibara Y. Photoinducible phase of the Japanese quail detected by direct stimulation of the brain. In: Suda M, Hayaishi O, Nakagawa H, editors. Biological Rhythms and their Central Mechanism. Amsterdam: Elsevier; 1979. p. 85–94.

14. Oliver J, Jallageas M, Baylé JD. Plasma testosterone and LH levels in male quail bearing hypothalamic lesions or radioluminous implants. Neuroendocrinology. 1979;28(2):114–22. 431774

15. Glass JD, Lauber JK. Sites and action spectra for encephalic photoreception in the Japanese quail. Am J Physiol. 1981 Mar;240(3):R220–228. 7212094

16. Silver R, Witkovsky P, Horvath P, Alones V, Barnstable CJ, Lehman MN. Coexpression of opsin- and VIP-like-immunoreactivity in CSF-contacting neurons of the avian brain. Cell Tissue Res. 1988 Jul;253(1):189–98. 2970894

17. Wada Y, Okano T, Fukada Y. Phototransduction molecules in the pigeon deep brain. J Comp Neurol. 2000 Dec;428(1):138–44. 11058228

18. Zhao H, Jiang J, Wang G, Le C, Wingfield JC. Daily, circadian and seasonal changes of rhodopsin-like encephalic photoreceptor and its involvement in mediating photoperiodic responses of Gambel’s white-crowned Sparrow, Zonotrichia leucophrys gambelii. Brain Res. 2018 15;1687:104–16. doi: 10.1016/j.brainres.2018.02.048 29510141

19. Halford S, Pires SS, Turton M, Zheng L, González-Menéndez I, Davies WL, et al. VA Opsin-Based Photoreceptors in the Hypothalamus of Birds. Current Biology. 2009 Aug;19(16):1396–402. doi: 10.1016/j.cub.2009.06.066 19664923

20. Chaurasia SS, Rollag MD, Jiang G, Hayes WP, Haque R, Natesan A, et al. Molecular cloning, localization and circadian expression of chicken melanopsin (Opn4): differential regulation of expression in pineal and retinal cell types. J Neurochem. 2005 Jan;92(1):158–70. 15606905

21. Kang SW, Leclerc B, Kosonsiriluk S, Mauro LJ, Iwasawa A, El Halawani ME. Melanopsin expression in dopamine-melatonin neurons of the premammillary nucleus of the hypothalamus and seasonal reproduction in birds. Neuroscience. 2010 Sep;170(1):200–13. doi: 10.1016/j.neuroscience.2010.06.082 20620198

22. Nakane Y, Ikegami K, Ono H, Yamamoto N, Yoshida S, Hirunagi K, et al. A mammalian neural tissue opsin (Opsin 5) is a deep brain photoreceptor in birds. Proc Natl Acad Sci USA. 2010 Aug;107(34):15264–8. doi: 10.1073/pnas.1006393107 20679218

23. Yamashita T, Ohuchi H, Tomonari S, Ikeda K, Sakai K, Shichida Y. Opn5 is a UV-sensitive bistable pigment that couples with Gi subtype of G protein. Proc Natl Acad Sci USA. 2010 Dec;107(51):22084–9. doi: 10.1073/pnas.1012498107 21135214

24. Nakane Y, Shimmura T, Abe H, Yoshimura T. Intrinsic photosensitivity of a deep brain photoreceptor. Curr Biol. 2014 Jul;24(13):R596–597. doi: 10.1016/j.cub.2014.05.038 25004360

25. Kato M, Sugiyama T, Sakai K, Yamashita T, Fujita H, Sato K, et al. Two Opsin 3-Related Proteins in the Chicken Retina and Brain: A TMT-Type Opsin 3 Is a Blue-Light Sensor in Retinal Horizontal Cells, Hypothalamus, and Cerebellum. PLOS ONE. 2016 Nov 18;11(11):e0163925. doi: 10.1371/journal.pone.0163925 27861495

26. Kojima D, Mori S, Torii M, Wada A, Morishita R, Fukada Y. UV-sensitive photoreceptor protein OPN5 in humans and mice. PLOS ONE. 2011;6(10):e26388. doi: 10.1371/journal.pone.0026388 22043319

27. Soni BG, Foster RG. A novel and ancient vertebrate opsin. FEBS Lett. 1997 Apr;406(3):279–83. 9136902

28. Soni BG, Philp AR, Foster RG, Knox BE. Novel retinal photoreceptors. Nature. 1998 Jul;394(6688):27–8. 9665123

29. Philp AR, Bellingham J, Garcia-Fernandez J-M, Foster RG. A novel rod-like opsin isolated from the extra-retinal photoreceptors of teleost fish. FEBS Letters. 2000;468(2–3):181–8. 10692583

30. Kojima D, Mano H, Fukada Y. Vertebrate ancient-long opsin: a green-sensitive photoreceptive molecule present in zebrafish deep brain and retinal horizontal cells. J Neurosci. 2000 Apr;20(8):2845–51. 10751436

31. Davies WIL, Turton M, Peirson SN, Follett BK, Halford S, Garcia-Fernandez JM, et al. Vertebrate ancient opsin photopigment spectra and the avian photoperiodic response. Biol Lett. 2012 Apr;8(2):291–4. doi: 10.1098/rsbl.2011.0864 22031722

32. García-Fernández JM, Cernuda-Cernuda R, Davies WIL, Rodgers J, Turton M, Peirson SN, et al. The hypothalamic photoreceptors regulating seasonal reproduction in birds: A prime role for VA opsin. Frontiers in Neuroendocrinology. 2015 Apr;37:13–28. doi: 10.1016/j.yfrne.2014.11.001 25448788

33. Foster RG, Follett BK. The involvement of a rhodopsin-like photopigment in the photoperiodic response of the Japanese quail. Journal of comparative physiology A. 1985;157(4):519–528.

34. Foster RG, Follett BK, Lythgoe JN. Rhodopsin-like sensitivity of extra-retinal photoreceptors mediating the photoperiodic response in quail. Nature. 1985 Jan;313(5997):50–2. 3965970

35. Hartwig HG, Van Veen T. Spectral characteristics of visible radiation penetrating into the brain and stimulating extraretinal photoreceptors. Journal of comparative physiology. 1979;130(3):277–282.

36. Oishi T, Ohashi K. Effects of wavelengths of light on the photoperiodic gonadal response of blinded-pinealectomized Japanese quail. Zoological science. 1993;10(5):757–762.

37. Lamb TD. Photoreceptor spectral sensitivities: common shape in the long-wavelength region. Vision Res. 1995 Nov;35(22):3083–91. 8533344

38. Yoshimura T, Ebihara S. Spectral sensitivity of photoreceptors mediating phase-shifts of circadian rhythms in retinally degenerate CBA/J (rd/rd) and normal CBA/N (+/+)mice. J Comp Physiol A. 1996 Jun;178(6):797–802. 8667293

39. Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH, Hankins MW, et al. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature. 2003 Jul;424(6944):76–81. doi: 10.1038/nature01761 12808468

40. Altimus CM, Güler AD, Alam NM, Arman AC, Prusky GT, Sampath AP, et al. Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities. Nat Neurosci. 2010 Sep;13(9):1107–12. doi: 10.1038/nn.2617 20711184

41. Bellingham J, Chaurasia SS, Melyan Z, Liu C, Cameron MA, Tarttelin EE, et al. Evolution of melanopsin photoreceptors: discovery and characterization of a new melanopsin in nonmammalian vertebrates. PLoS Biol. 2006 Jul;4(8):e254. doi: 10.1371/journal.pbio.0040254 16856781

42. Torii M, Kojima D, Okano T, Nakamura A, Terakita A, Shichida Y, et al. Two isoforms of chicken melanopsins show blue light sensitivity. FEBS Lett. 2007 Nov;581(27):5327–31. 17977531

43. Wang F, Flanagan J, Su N, Wang L-C, Bui S, Nielson A, et al. RNAscope: a novel in situ RNA analysis platform for formalin-fixed, paraffin-embedded tissues. J Mol Diagn. 2012 Jan;14(1):22–9. doi: 10.1016/j.jmoldx.2011.08.002 22166544

44. Hughes ME, Hogenesch JB, Kornacker K. JTK_CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J Biol Rhythms. 2010 Oct;25(5):372–80. doi: 10.1177/0748730410379711 20876817

45. Bailey MJ, Cassone VM. Melanopsin expression in the chick retina and pineal gland. Brain Res Mol Brain Res. 2005 Apr;134(2):345–8. 15836930

46. Vigh-Teichmann I, Röhlich P, Vigh B, Aros B. Comparison of the pineal complex, retina and cerebrospinal fluid contacting neurons by immunocytochemical antirhodopsin reaction. Z Mikrosk Anat Forsch. 1980;94(4):623–40. 7456628

47. Franzoni MF, Viglietti-Panzica C, Ramieri G, Panzica GC. A Golgi study on the neuronal morphology in the hypothalamus of the Japanese quail (Coturnix coturnix japonica). I. Tuberal and mammillary regions. Cell Tissue Res. 1984;236(2):357–64. 6203645

48. Haida Y, Ubuka T, Ukena K, Tsutsui K, Oishi T, Tamotsu S. Photoperiodic response of serotonin- and galanin-immunoreactive neurons of the paraventricular organ and infundibular nucleus in Japanese quail, Coturnix coturnix japonica. Zool Sci. 2004 May;21(5):575–82. 15170061

49. Moore AF, Cassone VM, Alloway KD, Bartell PA. The premammillary nucleus of the hypothalamus is not necessary for photoperiodic timekeeping in female turkeys (Meleagris gallopavo). PLOS ONE. 2018 Feb 20;13(2):e0190274. doi: 10.1371/journal.pone.0190274 29462137

50. Shimmura T, Nakayama T, Shinomiya A, Fukamachi S, Yasugi M, Watanabe E, et al. Dynamic plasticity in phototransduction regulates seasonal changes in color perception. Nature Communications. 2017 Sep 4;8(1):412. doi: 10.1038/s41467-017-00432-8 28871081

51. Foster RG, Korf H-W, Schalken JJ. Immunocytochemical markers revealing retinal and pineal but not hypothalamic photoreceptor systems in the Japanese quail. Cell Tissue Res. 1987 Apr 1;248(1):161–7. 2952278

52. Yoshikawa T, Oishi T. Extraretinal Photoreception and Circadian Systems in Nonmammalian Vertebrates. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology. 1998 Jan;119(1):65–72.

53. Yoshimura T, Suzuki Y, Makino E, Suzuki T, Kuroiwa A, Matsuda Y, et al. Molecular analysis of avian circadian clock genes. Brain Res Mol Brain Res. 2000 May;78(1–2):207–15. 10891604

Action spectrum for photoperiodic control of thyroid-stimulating hormone in Japanese quail (Coturnix japonica)

Souhrn

Klíčová slova:

Zdroje

PLOS One

Získaná hemofilie - Povědomí o nemoci a její diagnostika

Eozinofilní granulomatóza s polyangiitidou