A genetically female brain is required for a regular reproductive cycle in chicken brain chimeras

Nature Communications

Volumn 4, Issue , 2013, Pages

  Maekawa, Fumihiko ^a,b   Sakurai, Miyano ^a,c   Yamashita, Yuki ^a   Tanaka, Kohichi ^a   Haraguchi, Shogo ^d   Yamamoto, Kazutoshi ^d   Tsutsui, Kazuyoshi ^d   Yoshioka, Hidefumi ^e   Murakami, Shizuko ^f   Tadano, Ryo ^g,h   Goto, Tatsuhiko ^g,i   Shiraishi, Jun Ichi ^g,j   Tomonari, Kohei ^g   Oka, Takao ^g   Ohara, Ken ^g   Maeda, Teruo ^g   Bungo, Takashi ^g   Tsudzuki, Masaoki ^g   Ohki Hamazaki, Hiroko ^a,c  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE FOR ENVIRONMENTAL STUDIES   (Japan)

^c KITASATO UNIVERSITY   (Japan)

^d WASEDA UNIVERSITY   (Japan)

^e HYOGO UNIVERSITY OF TEACHER EDUCATION   (Japan)

^f JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^g HIROSHIMA UNIVERSITY   (Japan)

^h GIFU UNIVERSITY   (Japan)

ⁱ NATIONAL INSTITUTE OF GENETICS   (Japan)

^j NIPPON VETERINARY AND LIFE SCIENCE UNIVERSITY   (Japan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN; LUTEINIZING HORMONE; SEX HORMONE; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; ESTRADIOL;

BRAIN; CHIMERA; FEMALE; OVIPOSITION; POULTRY; REPRODUCTIVE CYCLE; SECONDARY SEXUAL CHARACTERISTICS; SEX DETERMINATION; SEXUAL MATURITY; STEROID;

ARTICLE; BLOOD LEVEL; BRAIN; BRAIN CELL; CHICKEN; CHIMERA; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EGG LAYING; ESTRUS CYCLE; FEMALE; MALE; NONHUMAN; OVARY CYCLE; PERINATAL PERIOD; PHENOTYPE; REPRODUCTION; SEX DIFFERENTIATION; SEXUAL MATURATION; ANIMAL; ANIMAL BEHAVIOR; BLOOD; CHICK EMBRYO; CYTOLOGY; GENETICS; HISTOLOGY; METABOLISM; NERVE CELL; OVULATION; PHYSIOLOGY; PRENATAL DEVELOPMENT; SECRETION (PROCESS); SEXUAL DEVELOPMENT; SPERM; SPERMATOZOON;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CHICK EMBRYO; CHICKENS; CHIMERA; ESTRADIOL; FEMALE; GONADAL STEROID HORMONES; LUTEINIZING HORMONE; MALE; NEURONS; NEUROTRANSMITTER AGENTS; OVULATION; REPRODUCTION; SEMEN; SEX CHARACTERISTICS; SEX DIFFERENTIATION; SEXUAL MATURATION; SPERMATOZOA;

MLCS; MLOWN;

EID: 84879156382     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2372     Document Type: Article

References (59)

1. Gubbay, J. et al. A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 346, 245-250 (1990).
2. Koopman, P., Gubbay, J., Vivian, N., Goodfellow, P. & Lovell-Badge, R. Male development of chromosomally female mice transgenic for Sry. Nature 351, 117-121 (1991). (Pubitemid 21896542)
3. Sinclair, A. H. et al. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346, 240-244 (1990).
4. Matsuda, M. et al. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417, 559-563 (2002). (Pubitemid 34595924)
5. Arnold, A. P. & Gorski, R. A. Gonadal steroid induction of structural sex differences in the central nervous system. Annu. Rev. Neurosci. 7, 413-442 (1984). (Pubitemid 14155304)
6. Phoenix, C. H., Goy, R. W., Gerall, A. A. & Young, W. C. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65, 369-382 (1959).
7. MacLusky, N. J. & Naftolin, F. Sexual differentiation of the central nervous system. Science 211, 1294-1302 (1981).
8. Smith, C. A. et al. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461, 267-271 (2009).
9. Zhao, D. et al. Somatic sex identity is cell autonomous in the chicken. Nature 464, 237-242 (2010).
10. Tanabe, Y., Saito, N. & Nakamura, T. Ontogenetic steroidogenesis by testes, ovary, and adrenals of embryonic and postembryonic chickens (Gallus domesticus). Gen. Comp. Endocrinol. 63, 456-463 (1986). (Pubitemid 16043795)
11. Woods, J. E. & Erton, L. H. The synthesis of estrogens in the gonads of the chick embryo. Gen. Comp. Endocrinol. 36, 360-370 (1978). (Pubitemid 9105048)
12. Wilson, J. A. & Glick, B. Ontogeny of mating behavior in the chicken. Am. J. Physiol. 218, 951-955 (1970).
13. Elbrecht, A. & Smith, R. G. Aromatase enzyme activity and sex determination in chickens. Science 255, 467-470 (1992).
14. Adkins-Regan, E. Sexual differentiation in birds. Trends Neurosci. 10, 517-522 (1987).
15. Balthazart, J. & Schumacher, M. Organization and activation of behavior in quail: role of testosterone metabolism. J. Exp. Zool. 232, 595-604 (1984). (Pubitemid 15193879)
16. Carruth, L. L., Reisert, I. & Arnold, A. P. Sex chromosome genes directly affect brain sexual differentiation. Nat. Neurosci. 5, 933-934 (2002).
17. Dewing, P. et al. Direct regulation of adult brain function by the male-specific factor SRY. Curr. Biol. 16, 415-420 (2006). (Pubitemid 43259353)
18. Agate, R. J. et al. Neural, not gonadal, origin of brain sex differences in a gynandromorphic finch. Proc. Natl Acad. Sci. USA 100, 4873-4878 (2003). (Pubitemid 36457821)
19. Balaban, E., Teillet, M. A. & Le Douarin, N. Application of the quail-chick chimera system to the study of brain development and behavior. Science 241, 1339-1342 (1988).
20. Teillet, M. A. et al. Transfer of genetic epilepsy by embryonic brain grafts in the chicken. Proc. Natl Acad. Sci. USA 88, 6966-6970 (1991).
21. Garcia-Lopez, R., Pombero, A. & Martinez, S. Fate map of the chick embryo neural tube. Dev. Growth Differ. 51, 145-165 (2009).
22. Nomura, O., Nakabayashi, O., Nishimori, K., Yasue, H. & Mizuno, S. Expression of five steroidogenic genes including aromatase gene at early developmental stages of chicken male and female embryos. J. Steroid Biochem. Mol. Biol. 71, 103-109 (1999). (Pubitemid 30001808)
23. Raymond, C. S., Kettlewell, J. R., Hirsch, B., Bardwell, V. J. & Zarkower, D. Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev. Biol. 215, 208-220 (1999).
24. Kent, J., Wheatley, S. C., Andrews, J. E., Sinclair, A. H. & Koopman, P. A male-specific role for SOX9 in vertebrate sex determination. Development 122, 2813-2822 (1996). (Pubitemid 26326513)
25. Morais da Silva, S. et al. Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat. Genet. 14, 62-68 (1996).
26. Jurkevich, A., Barth, S. W. & Grossmann, R. Sexual dimorphism of arg-vasotocin gene expressing neurons in the telencephalon and dorsal diencephalon of the domestic fowl. An immunocytochemical and in situ hybridization study. Cell Tissue Res. 287, 69-77 (1997).
27. Klein, S., Jurkevich, A. & Grossmann, R. Sexually dimorphic immunoreactivity of galanin and colocalization with arginine vasotocin in the chicken brain (Gallus gallus domesticus). J. Comp. Neurol. 499, 828-839 (2006). (Pubitemid 44730522)
28. Schlinger, B. A., Soma, K. K. & London, S. E. Neurosteroids and brain sexual differentiation. Trends Neurosci. 24, 429-431 (2001). (Pubitemid 32695347)
29. Tsutsui, K. Neurosteroid biosynthesis and function in the brain of domestic birds. Front. Endocrinol. 2, 371-14 (2011).
30. Kinutani, M. & Le Douarin, N. M. Avian spinal cord chimeras. I. Hatching ability and posthatching survival in homo-and heterospecific chimeras. Dev. Biol. 111, 243-255 (1985).
31. Gahr, M. Male Japanese quails with female brains do not show male sexual behaviors. Proc. Natl Acad. Sci. USA 100, 7959-7964 (2003). (Pubitemid 36760077)
32. Ohki, H., Martin, C., Corbel, C., Coltey, M. & Le Douarin, N. M. Tolerance induced by thymic epithelial grafts in birds. Science 237, 1032-1035 (1987). (Pubitemid 17124674)
33. Brown-Grant, K. & Raisman, G. Abnormalities in reproductive function associated with the destruction of the suprachiasmatic nuclei in female rats. Proc. R Soc. Lond. B Biol. Sci. 198, 279-296 (1977). (Pubitemid 8165162)
34. Wiegand, S. J., Terasawa, E., Bridson, W. E. & Goy, R. W. Effects of discrete lesions of preoptic and suprachiasmatic structures in the female rat. Alterations in the feedback regulation of gonadotropin secretion. Neuroendocrinology 31, 147-157 (1980).
35. Miller, B. H. et al. Circadian clock mutation disrupts estrous cyclicity and maintenance of pregnancy. Curr. Biol. 14, 1367-1373 (2004). (Pubitemid 39081639)
36. Ratajczak, C. K., Boehle, K. L. & Muglia, L. J. Impaired steroidogenesis and implantation failure in Bmal1-/-mice. Endocrinology 150, 1879-1885 (2009).
37. Binkley, S., Hryshchyshyn, M. & Reilly, K. N-acetyltransferase activity responds to environmental lighting in the eye as well as in the pineal gland. Nature 281, 479-481 (1979). (Pubitemid 10244268)
38. Deguchi, T. Circadian rhythm of serotonin N-acetyltransferase activity in organ culture of chicken pineal gland. Science 203, 1245-1247 (1979). (Pubitemid 9149469)
39. Ebihara, S. & Kawamura, H. The role of the pineal organ and the suprachiasmatic nucleus in the control of circadian locomotor rhythms in the Java sparrow, Padda oryzivora. J. Comp. Physiol. A 141, 207-214 (1981).
40. Kasal, C. A., Menaker, M. & Perez-Polo, J. R. Circadian clock in culture: N-acetyltransferase activity of chick pineal glands oscillates in vitro. Science 203, 656-658 (1979). (Pubitemid 9149463)
41. Simpson, S. M. & Follett, B. K. Pineal and hypothalamic pacemakers: their role in regulating circadian rhythmicity in Japanese quail. J. Comp. Physiol. A 144, 381-389 (1981).
42. Akutsu, S., Takada, M., Ohki-Hamazaki, H., Murakami, S. & Arai, Y. Origin of luteinizing hormone-releasing hormone (LHRH) neurons in the chick embryo: effect of the olfactory placode ablation. Neurosci. Lett. 142, 241-244 (1992).
43. Yamamoto, N., Uchiyama, H., Ohki-Hamazaki, H., Tanaka, H. & Ito, H. Migration of GnRH-immunoreactive neurons from the olfactory placode to the brain: a study using avian embryonic chimeras. Dev. Brain Res. 95, 234-244 (1996). (Pubitemid 26273821)
44. Schlinger, B. A. & Arnold, A. P. Circulating estrogens in a male songbird originate in the brain. Proc. Natl Acad. Sci. USA 89, 7650-7653 (1992).
45. Tsutsui, K. et al. 7a-Hydroxypregnenolone mediates melatonin action underlying diurnal locomotor rhythms. J. Neurosci. 28, 2158-2167 (2008). (Pubitemid 351317628)
46. Holloway, C. C. & Clayton, D. F. Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nat. Neurosci. 4, 170-175 (2001). (Pubitemid 32125262)
47. Berga, S. & Naftolin, F. Neuroendocrine control of ovulation. Gynecol. Endocrinol. 28(Suppl 1): 9-13 (2012).
48. Deligeoroglou, E. et al. Evaluation and management of adolescent amenorrhea. Ann. N Y. Acad. Sci. 1205, 23-32 (2010).
49. Kovanen, L., Saarikoski, S. T., Aromaa, A., Lonnqvist, J. & Partonen, T. ARNTL (BMAL1) and NPAS2 gene variants contribute to fertility and seasonality. PLoS One 5, e10007 (2010).
50. Boden, M. J. & Kennaway, D. J. Circadian rhythms and reproduction. Reproduction 132, 379-392 (2006). (Pubitemid 44524502)
51. Widowski, T. M., Lo Fo Wong, D. M. & Duncan, I. J. Rearing with males accelerates onset of sexual maturity in female domestic fowl. Poult. Sci. 77, 150-155 (1998). (Pubitemid 128529252)
52. Krishnan, K. A., Proudman, J. A. & Bahr, J. M. Purification and partial characterization of isoforms of luteinizing hormone from the chicken pituitary gland. Comp. Biochem. Physiol. Biochem. Mol. Biol. 108, 253-264 (1994).
53. Chowdhury, V. S. et al. Melatonin stimulates the release of gonadotropin-inhibitory hormone by the avian hypothalamus. Endocrinology 151, 271-280 (2010).
54. Ubuka, T., Ukena, K., Sharp, P. J., Bentley, G. E. & Tsutsui, K. Gonadotropin-inhibitory hormone inhibits gonadal development and maintenance by decreasing gonadotropin synthesis and release in male quail. Endocrinology 147, 1187-1194 (2006). (Pubitemid 43244351)
55. Iwabuchi, M., Maekawa, F., Tanaka, K. & Ohki-Hamazaki, H. Overexpression of gastrin-releasing peptide receptor induced layer disorganization in brain. Neuroscience 138, 109-122 (2006). (Pubitemid 43222074)
56. Kanyinji, F. & Maeda, T. Additional dietary calcium fed to Barred Plymouth Rock roosters reduces blood cholesterol, elevates seminal calcium, and enhances sperm motility, thermo-tolerance and cryosurvivability. Anim. Reprod. Sci. 120, 158-165 (2010).
57. Haraguchi, S. et al. Acute stress increases the synthesis of 7a-hydroxypregnenolone, a new key neurosteroid stimulating locomotor activity, through corticosterone action in newts. Endocrinology 153, 794-805 (2012).
58. Matsunaga, M., Ukena, K., Baulieu, E. E. & Tsutsui, K. 7a-Hydroxypregnenolone acts as a neuronal activator to stimulate locomotor activity of breeding newts by means of the dopaminergic system. Proc. Natl Acad. Sci. USA 101, 17282-17287 (2004). (Pubitemid 39627811)
59. Meffre, D. et al. Steroid profiling in brain and plasma of male and pseudopregnant female rats after traumatic brain injury: analysis by gas chromatography/mass spectrometry. Endocrinology 148, 2505-2517 (2007). (Pubitemid 46997062)