Glucocorticoid receptor exhibits sexually dimorphic expression in the medaka brain

General and Comparative Endocrinology

Volumn 223, Issue , 2015, Pages 47-53

  Kikuchi, Yukiko ^a   Hosono, Kohei ^a   Yamashita, Junpei ^a   Kawabata, Yukika ^a   Okubo, Kataaki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Brain; Glucocorticoid receptor (GR); Gonadotropin releasing hormone (GnRH); Sex differences; Teleost; Vasotocin

Indexed keywords

ARGIPRESTOCIN; GLUCOCORTICOID RECEPTOR; GONADORELIN; GONADOTROPIN RELEASING HORMONE 1; UNCLASSIFIED DRUG; MESSENGER RNA; NEUROPEPTIDE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR PARVOCELLULAR PREOPTIC NUCLEUS; ARTICLE; CONTROLLED STUDY; FEMALE; GENE; GR1 GENE; MALE; NERVE CELL; NONHUMAN; ORYZIAS LATIPES; PREOPTIC NUCLEUS; PRIORITY JOURNAL; SEX DIFFERENCE; SIGNAL TRANSDUCTION; STRESS; THALAMUS NUCLEUS; ANIMAL; BRAIN; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; IN SITU HYBRIDIZATION; METABOLISM; ORYZIAS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; BRAIN; FEMALE; IN SITU HYBRIDIZATION; MALE; NEURONS; NEUROPEPTIDES; ORYZIAS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, GLUCOCORTICOID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEX FACTORS;

EID: 84944232843     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2015.09.031     Document Type: Article

References (44)

1. Alsop D., Vijayan M. The zebrafish stress axis: molecular fallout from the teleost-specific genome duplication event. Gen. Comp. Endocrinol. 2009, 161:62-66.
2. Anken R., Bourrat F. Brain Atlas of the Medakafish 1998, INRA Editions, Paris.
3. Bangasser D.A., Valentino R.J. Sex differences in stress-related psychiatric disorders: neurobiological perspectives. Front. Neuroendocrinol. 2014, 35:303-319.
4. Bond H., Warne J.M., Balment R.J. Effect of acute restraint on hypothalamic pro-vasotocin mRNA expression in flounder, Platichthys flesus. Gen. Comp. Endocrinol. 2007, 153:221-227.
5. Bourke C.H., Harrell C.S., Neigh G.N. Stress-induced sex differences: adaptations mediated by the glucocorticoid receptor. Horm. Behav. 2012, 62:210-218.
6. Chandran U.R., DeFranco D.B. Regulation of gonadotropin-releasing hormone gene transcription. Behav. Brain Res. 1999, 105:29-36.
7. Dewan A.K., Tricas T.C. Arginine vasotocin neuronal phenotypes and their relationship to aggressive behavior in the territorial monogamous multiband butterflyfish, Chaetodon multicinctus. Brain Res. 2011, 1401:74-84.
8. Farmer M.A., Leja A., Foxen-Craft E., Chan L., MacIntyre L.C., Niaki T., Chen M., Mapplebeck J.C., Tabry V., Topham L., Sukosd M., Binik Y.M., Pfaus J.G., Mogil J.S. Pain reduces sexual motivation in female but not male mice. J. Neurosci. 2014, 34:5747-5753.
9. Fernandino J.I., Hattori R.S., Kishii A., Strüssmann C.A., Somoza G.M. The cortisol and androgen pathways cross talk in high temperature-induced masculinization: the 11β-hydroxysteroid dehydrogenase as a key enzyme. Endocrinology 2012, 153:6003-6011.
10. Forlano P.M., Bass A.H. Neural and hormonal mechanisms of reproductive-related arousal in fishes. Horm. Behav. 2011, 59:616-629.
11. Gilchriest B.J., Tipping D.R., Hake L., Levy A., Baker B.I. The effects of acute and chronic stresses on vasotocin gene transcripts in the brain of the rainbow trout (Oncorhynchus mykiss). J. Neuroendocrinol. 2000, 12:795-801.
12. Godwin J. Neuroendocrinology of sexual plasticity in teleost fishes. Front. Neuroendocrinol. 2010, 31:203-216.
13. Goel N., Bale T.L. Sex differences in the serotonergic influence on the hypothalamic-pituitary-adrenal stress axis. Endocrinology 2010, 151:1784-1794.
14. Greenwood A.K., Wark A.R., Fernald R.D., Hofmann H.A. Expression of arginine vasotocin in distinct preoptic regions is associated with dominant and subordinate behaviour in an African cichlid fish. Proc. Biol. Sci. 2008, 275:2393-2402.
15. Handa R.J., Weiser M.J. Gonadal steroid hormones and the hypothalamo-pituitary-adrenal axis. Front. Neuroendocrinol. 2014, 35:197-220.
16. Hattori R.S., Fernandino J.I., Kishii A., Kimura H., Kinno T., Oura M., Somoza G.M., Yokota M., Strüssmann C.A., Watanabe S. Cortisol-induced masculinization: does thermal stress affect gonadal fate in pejerrey, a teleost fish with temperature-dependent sex determination?. PLoS One 2009, 4:e6548.
17. Hayashi Y., Kobira H., Yamaguchi T., Shiraishi E., Yazawa T., Hirai T., Kamei Y., Kitano T. High temperature causes masculinization of genetically female medaka by elevation of cortisol. Mol. Reprod. Dev. 2010, 77:679-686.
18. Hiraki T., Takeuchi A., Tsumaki T., Zempo B., Kanda S., Oka Y., Nagahama Y., Okubo K. Female-specific target sites for both oestrogen and androgen in the teleost brain. Proc. Biol. Sci. 2012, 279:5014-5023.
19. Ishikawa Y., Yoshimoto M., Ito H. A brain atlas of a wild-type inbred strain of the medaka, Oryzias latipes. Fish Biol. J. Medaka 1999, 10:1-26.
20. Iwata E., Mikami K., Manbo J., Moriya-Ito K., Sasaki H. Social interaction influences blood cortisol values and brain aromatase genes in the protandrous false clown anemonefish, Amphiprion ocellaris. Zool. Sci. 2012, 29:849-855.
21. Karigo T., Kanda S., Takahashi A., Abe H., Okubo K., Oka Y. Time-of-day-dependent changes in GnRH1 neuronal activities and gonadotropin mRNA expression in a daily spawning fish, medaka. Endocrinology 2012, 153:3394-3404.
22. Karigo T., Oka Y. Neurobiological study of fish brains gives insights into the nature of gonadotropin-releasing hormone 1-3 neurons. Front. Endocrinol. 2013, 4:177.
23. Kawabata Y., Hiraki T., Takeuchi A., Okubo K. Sex differences in the expression of vasotocin/isotocin, gonadotropin-releasing hormone, and tyrosine and tryptophan hydroxylase family genes in the medaka brain. Neuroscience 2012, 218:65-77.
24. Kovács K.J., Földes A., Sawchenko P.E. Glucocorticoid negative feedback selectively targets vasopressin transcription in parvocellular neurosecretory neurons. J. Neurosci. 2000, 20:3843-3852.
25. Kudielka B.M., Kirschbaum C. Sex differences in HPA axis responses to stress: a review. Biol. Psychol. 2005, 69:113-132.
26. Miyagawa S., Lange A., Tohyama S., Ogino Y., Mizutani T., Kobayashi T., Tatarazako N., Tyler C.R., Iguchi T. Characterization of Oryzias latipes glucocorticoid receptors and their unique response to progestins. J. Appl. Toxicol. 2015, 35:302-309.
27. Moss R.L., McCann S.M. Induction of mating behavior in rats by luteinizing hormone releasing factor. Science 1973, 181:177-179.
28. Myers B., McKlveen J.M., Herman J.P. Glucocorticoid actions on synapses, circuits, and behavior: implications for the energetics of stress. Front. Neuroendocrinol. 2014, 35:180-196.
29. Okubo K., Sakai F., Lau E.L., Yoshizaki G., Takeuchi Y., Naruse K., Aida K., Nagahama Y. Forebrain gonadotropin-releasing hormone neuronal development: insights from transgenic medaka and the relevance to X-linked Kallmann syndrome. Endocrinology 2006, 147:1076-1084.
30. Okubo K., Nagahama Y. Structural and functional evolution of gonadotropin-releasing hormone in vertebrates. Acta Physiol. 2008, 193:3-15.
31. Olivereau M., Olivereau J. Effect of pharmacological adrenalectomy on corticotropin-releasing factor-like and arginine vasotocin immunoreactivities in the brain and pituitary of the eel: immunocytochemical study. Gen. Comp. Endocrinol. 1990, 80:199-215.
32. Pfaff D.W. Luteinizing hormone-releasing factor potentiates lordosis behavior in hypophysectomized ovariectomized female rats. Science 1973, 182:1148-1149.
33. Sakamoto N., Ito H. Fiber connections of the corpus glomerulosum in a teleost, Navodon modestus. J. Comp. Neurol. 1982, 205:291-298.
34. Sapolsky R.M., Romero L.M., Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 2000, 21:55-89.
35. Seale J.V., Wood S.A., Atkinson H.C., Bate E., Lightman S.L., Ingram C.D., Jessop D.S., Harbuz M.S. Gonadectomy reverses the sexually diergic patterns of circadian and stress-induced hypothalamic-pituitary-adrenal axis activity in male and female rats. J. Neuroendocrinol. 2004, 16:516-524.
36. Seale J.V., Wood S.A., Atkinson H.C., Harbuz M.S., Lightman S.L. Gonadal steroid replacement reverses gonadectomy-induced changes in the corticosterone pulse profile and stress-induced hypothalamic-pituitary-adrenal axis activity of male and female rats. J. Neuroendocrinol. 2004, 16:989-998.
37. Takeuchi A., Okubo K. Post-proliferative immature radial glial cells female-specifically express aromatase in the medaka optic tectum. PLoS One 2013, 8:e73663.
38. Teitsma C.A., Anglade I., Toutirais G., Muñoz-Cueto J.A., Saligaut D., Ducouret B., Kah O. Immunohistochemical localization of glucocorticoid receptors in the forebrain of the rainbow trout (Oncorhynchus mykiss). J. Comp. Neurol. 1998, 401:395-410.
39. Teitsma C.A., Anglade I., Lethimonier C., Le Dréan G., Saligaut D., Ducouret B., Kah O. Glucocorticoid receptor immunoreactivity in neurons and pituitary cells implicated in reproductive functions in rainbow trout: a double immunohistochemical study. Biol. Reprod. 1999, 60:642-650.
40. Trayer V., Hwang P.P., Prunet P., Thermes V. Assessment of the role of cortisol and corticosteroid receptors in epidermal ionocyte development in the medaka (Oryzias latipes) embryos. Gen. Comp. Endocrinol. 2013, 194:152-161.
41. Whirledge S., Cidlowski J.A. A role for glucocorticoids in stress-impaired reproduction: beyond the hypothalamus and pituitary. Endocrinology 2013, 154:4450-4468.
42. Yamaguchi T., Yoshinaga N., Yazawa T., Gen K., Kitano T. Cortisol is involved in temperature-dependent sex determination in the Japanese flounder. Endocrinology 2010, 151:3900-3908.
43. Yamaguchi T., Kitano T. High temperature induces cyp26b1 mRNA expression and delays meiotic initiation of germ cells by increasing cortisol levels during gonadal sex differentiation in Japanese flounder. Biochem. Biophys. Res. Commun. 2012, 419:287-292.
44. Yokoi S., Okuyama T., Kamei Y., Naruse K., Taniguchi Y., Ansai S., Kinoshita M., Young L.J., Takemori N., Kubo T., Takeuchi H. An essential role of the arginine vasotocin system in mate-guarding behaviors in triadic relationships of medaka fish (Oryzias latipes). PLoS Genet. 2015, 11:e1005009.