Neurogenin 3 mediates sex chromosome effects on the generation of sex differences in hypothalamic neuronal development

Frontiers in Cellular Neuroscience

Volumn 8, Issue JULY, 2014, Pages

  Scerbo, María J ^a   Freire Regatillo, Alejandra ^b   Cisternas, Carla D ^a,c   Brunotto, Mabel ^c   Arevalo, Maria A ^b   Garcia Segura, Luis M ^b   Cambiasso, María J ^a,c  

^a INSTITUTO DE INVESTIGACIÓN MÉDICA MERCEDES Y MARTÍN FERREYRA   (Argentina)

^b INSTITUTO CAJAL   (Spain)

^c UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

Estradiol; Hypothalamic neurons; Neuritogenesis; Ngn3; Sex chromosomes; Sex differences

Indexed keywords

ESTRADIOL; MESSENGER RNA; NEUROGENIN 3; SMALL INTERFERING RNA; TESTOSTERONE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL MATURATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; EMBRYO; FEMALE; GENE EXPRESSION; GENE SILENCING; GENOTYPING TECHNIQUE; HYPOTHALAMUS; IMMUNOCYTOCHEMISTRY; MALE; MORPHOMETRICS; MOUSE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEUROSECRETORY CELL; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; SEX CHROMOSOME; SEX DIFFERENCE; SRY GENE; Y CHROMOSOME;

EID: 84904069953     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00188     Document Type: Article

References (59)

1. Arnold, A. P., and Burgoyne, P. S. (2004). Are XX and XY brain cells intrinsically different? TrendsEndocrinol.Metab. 15, 6-11. doi: 10.1016/j.tem.2003.11.001
2. Arnold, A. P., and Chen, X. (2009). What does the "four core genotypes" mouse model tell us about sex differences in the brain and other tissues? Front. Neuroendocrinol. 30:1-9. doi: 10.1016/j.yfrne.2008.11.001
3. Arnold, A. P., Chen, X., Link, J. C., Itoh, Y., and Reue, K. (2013). Cell- autonomous sex determination outside of the gonad. Dev. Dyn. 242, 371-379. doi: 10.1002/dvdy.23936
4. Arnold, A. P., and Gorski, R. A. (1984). Gonadal steroid induction of structural sex differences in the central nervous system. Annu. Rev. Neurosci. 7, 413-442. doi: 10.1146/annurev.ne.07.030184.002213
5. Ayoub, D. M., Greenough, W. T., and Juraska, J. M. (1983). Sex differences in dendritic structure in the preoptic area of the juvenile macaque monkey brain. Science 219, 197-198. doi: 10.1126/science.6849133
6. Beyer, C., Epp, B., Fassberg, J., Reisert, I., and Pilgrim, C. (1990). Region- and sex-related differences in maturation of astrocytes in dissociated cell cultures of embryonic rat brain. Glia 3, 55-64. doi: 10.1002/glia.440030108 Beyer
7. Kolbinger, W., Froehlich, U., Pilgrim, C., and Reisert, I. (1992). Sex differences of hypothalamic prolactin cells develop independently of the presence of sex steroids. Brain Res. 593, 253-256. doi: 10.1016/0006-8993(92) 91315-6
8. Caeiro, X. E., Mir, F. R., Vivas, L. M., Carrer, H. F., and Cambiasso, M. J. (2011). Sex chromosome complement contributes to sex differences in bradycardic baroreflex response. Hypertension 58, 505-511. doi: 10.1161/HYPERTENSI0N- AHA.111.175661
9. Cambiasso, M. J., Colombo, J. A., and Carrer, H. F. (2000). Differential effect of oestradiol and astroglia-conditioned media on the growth of hypothalamic neurons from male and female rat brains. Eur. J. Neurosci. 12, 2291-2298. doi: 10.1046/j.1460-9568.2000.00120.x
10. Cambiasso, M. J., Diaz, H., Caceres, A., and Carrer, H. F. (1995). Neurito- genic effect of estradiol on rat ventromedial hypothalamic neurons co-cultured with homotopic or heterotopic glia. J. Neurosci. Res. 42, 700-709. doi: 10.1002/jnr.490420513
11. Carruth, L. L., Reisert, I., and Arnold, A. P. (2002). Sex chromosome genes directly affect brain sexual differentiation. Nat. Neurosci. 5, 933-934. doi: 10.1038/nn922
12. Cubelos, B., Sebastian-Serrano, A., Beccari, L., Calcagnotto, M. E., Cisneros, E., Kim, S., et al. (2010). Cux1 and Cux2 regulate dendritic branching, spine morphology, and synapses of the upper layer neurons of the cortex. Neuron 66, 523-535. doi: 10.1016/j.neuron.2010.04.038
13. Dadam, F. M., Caeiro, X. E., Cisternas, C. D., Macchione, A. F., Cambiasso, M. J., andVivas, L. (2014). Effect of sex chromosome complement on sodium appetite and Fos-immunoreactivity induced by sodium depletion. Am. J. Physiol. Regul. Integr. Comp. Physiol. 306,R175-R184. doi: 10.1152/ajpregu.00447.2013
14. Davies, W., Isles, A. R., Burgoyne, P. S., and Wilkinson, L. S. (2006). X-linked imprinting: effects on brain and behaviour. Bioessays 28, 35-44. doi: 10.1002/bies.20341
15. DeVries, G. J., Rissman, E. F., Simerly, R.B.,Yang, L.-Y., Scordalakes, E.M., Auger, C. J., et al. (2002). A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J. Neurosci. 22, 9005-9014.
16. Diaz, H., Lorenzo, A., Carrer, H. F., and Caceres, A. (1992). Time lapse study of neurite growth in hypothalamic dissociated neurons in culture: sex differences and estrogen effects. J. Neurosci. Res. 33, 266-281. doi: 10.1002/jnr.4903 30210
17. Dotti, C. G., Sullivan, C.A., and Banker, G.A. (1988). The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8, 1454-1468.
18. Engele,J., Pilgrim, C., and Reisert, I. (1989). Sexual differentiation of mesencephalic neurons in vitro: effects of sex and gonadal hormones. Int. J. Dev. Neurosci. 7, 603-611. doi: 10.1016/0736-5748(89)90019-1
19. Ferreira, A., and Caceres, A. (1991). Estrogen-enhanced neurite growth: evidence fora selective induction ofTau and stable microtubules. J. Neurosci. 11, 392-400.
20. Flanagan-Cato, L. M. (2011). Sex differences in the neural circuit that mediates female sexual receptivity. Front. Neuroendocrinol. 32:124-136. doi: 10.1016/j.yfrne.2011.02.008
21. Gatewood, J. D., Wills, A., Shetty, S., Xu, J., Arnold, A. P., Burgoyne, P. S., et al. (2006). Sex chromosome complement and gonadal sex influence aggressive and parental behaviors in mice. J. Neurosci. 26, 2335-2342. doi: 10.1523/JNEUR0SCI.3743- 05.2006
22. Gioiosa, L., Chen, X., Watkins, R., Klanfer, N., Bryant, C. D., Evans, C. J., et al. (2008). Sex chromosome complement affects nociception in tests of acute and chronic exposure to morphine in mice. Horm. Behav. 53, 124-130. doi: 10.1016/j.yhbeh.2007.09.003
23. Griffin, G. D., and Flanagan-Cato, L. M. (2009). Sex differences in the dendritic arbor of hypothalamic ventromedial nucleus neurons. Physiol. Behav. 97, 151-156. doi: 10.1016/j.physbeh.2009.02.019
24. Gubbay, J., Collignon, J., Koopman, P., Capel, B., Economou, A., Münsterberg, A., et al. (1990). 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. doi: 10.1038/346245a0
25. Hojo, Y., Hattori, T.-A., Enami, T., Furukawa, A., Suzuki, K., Ishii, H.-T., et al. (2004). Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons. Proc. Natl. Acad. Sci. U.S.A. 101, 865-870. doi: 10.1073/pnas.2630225100
26. Huhtaniemi,I. (1994). Fetal testis-averyspecial endocrineorgan. Eur. J. Endocrinol. 130, 25-31. doi: 10.1530/eje.0.1300025
27. Iulianella, A., Sharma, M., Vanden Heuvel, G. B., and Trainor, P. A. (2009). Cux2 functions downstream of Notch signaling to regulate dorsal interneuron formation in the spinal cord. Development 136, 2329-2334. doi: 10.1242/dev. 032128
28. Iwase, S., Lan, F., Bayliss, P., de laTorre-Ubieta, L., Huarte, M., Qi, H. H., et al. (2007). The X-linked mental retardation gene SMCX/JARID1C defines a family ofhistone H3 lysine 4 demethylases. Cell 128,1077-1088. doi: 10.1016/j.cell.2007.02.017
29. Kopsida, E., Stergiakouli, E., Lynn, P.M., Wilkinson, L. S., and Davies, W. (2009). The role of the Y chromosome in brain function. Open Neuroendocrinol. J. 2, 20-30. doi: 10.2174/1876528900902010020
30. Lenz, K. M., and McCarthy, M. M. (2010). Organized for sex-steroid hormones and the developing hypothalamus. Eur. J. Neurosci. 32, 2096-2104. doi: 10.1111/j.1460-9568.2010.07511.x
31. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
32. Lovell-Badge, R., and Robertson, E. (1990). XY female mice resulting from a heritable mutation in the primary testis-determining gene, Tdy. Development 109, 635-646.
33. MacLusky, N. J., and Naftolin, F. (1981). Sexual differentiation of the centralnervous system. Science 211, 1294-1302. doi: 10.1126/science.6163211
34. Madeira, M. D., Leal, S., and Paula-Barbosa, M. M. (1999). Stereological evaluation and Golgi study of the sexual dimorphisms in the volume, cell numbers, and cell size in the medial preoptic nucleus of the rat. J. Neurocytol. 28, 131-148. doi: 10.1023/A:1007076206828
35. Mahadevaiah, S. K., Odorisio, T., Elliott, D. J., Rattigan, Ä., Szot, M., Laval, S. H., et al. (1998). Mouse homologues of the human AZF candidate gene RBM are expressed in spermatogonia and spermatids, and map to a Y chromosome deletion interval associated with a high incidence of sperm abnormalities. Hum. Mol. Genet. 1, US-121. doi: 10.1093/hmg/7.4.715
36. Matsumoto, A., and Arai, Y. (1986). Male-female difference in synaptic organization of the ventromedial nucleus of the hypothalamus in the rat. Neuroendocrinology 42, 232-236. doi: 10.1159/000124445
37. Naftolin, F., Ryan, K. J., and Petro, Z. (1972). Aromatization of androstenedione by the anterior hypothalamus of adult male and female rats. Endocrinology 90, 295-298. doi: 10.1210/endo-90-1-295
38. O'Shaughnessy, P. J., Baker, P. J., and Johnston, H. (2006). The foetal Leydig cell- differentiation, function and regulation. Int. J. Androl. 29, 90-95discussion 105-108. doi: 10.1111/j.1365-2605.2005.00555.x
39. O'Shaughnessy, P. J., Baker, P., Sohnius, U., Haavisto, A. M., Charlton, H. M., and Huhtaniemi, I. (1998). Fetal development of Leydig cell activity in the mouse is independent of pituitary gonadotroph function. Endocrinology 139, 1141-1146. doi: 10.1210/en.139.3.1141
40. Palaszynski, K. M., Smith, D. L., Kamrava, S., Burgoyne, P. S., Arnold, A. P., and Voskuhl, R. R. (2005). A yin-yang effect between sex chromosome complement and sex hormones on the immune response. Endocrinology 146, 3280-3285. doi: 10.1210/en.2005-0284
41. Pelling, M., Anthwal, N., McNay, D., Gradwohl, G., Leiter, A. B., Guillemot, F., etal. (2011). Differential requirements for neurogenin 3 in the development of POMC and NPY neurons in the hypothalamus. Dev. Biol. 349, 406-416. doi: 10.1016/j.ydbio.2010.11.007
42. Phoenix, C. H., Goy, R. W., Gerall, A. A., and Young, W. C. (1959). Organizing action of prenatallyadministered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65, 369-382. doi: 10.1210/endo-65-3-369
43. Quinn, J. J., Hitchcott, P. K., Umeda, E.A., Arnold, A. P., and Taylor, J. R. (2007). Sex chromosome complement regulates habit formation. Nat. Neurosci. 10, 1398-1400. doi: 10.1038/nn1994
44. Reinius, B., Shi, C., Hengshuo, L., Sandhu, K. S., Radomska, K. J., Rosen, G. D., etal. (2010). Female-biased expression of long non-coding RNAs in domains that escape X-inactivation in mouse. BMC Genomics 11:614. doi: 10.1186/14712164-11-614
45. Reisert, I., Engele, J., and Pilgrim, C. (1989). Early sexual differentiation of diencephalic dopaminergic neurons of the rat in vitro. Cell Tissue Res. 255, 411-417. doi: 10.1007/BF00224125
46. Reisert, I., and Pilgrim, C. (1991). Sexual differentiation of monoaminergic neurons-genetic or epigenetic? Trends Neurosci. 14,468-473. doi: 10.1016/0166- 2236(91)90047-X
47. Ruiz-Palmero, I., Simon-Areces, J., Garcia-Segura, L.M., and Arevalo, M.-A. (2011). Notch/neurogenin 3 signalling is involved in the neuritogenic actions of oestra- diol in developing hippocampal neurones. J. Neuroendocrinol. 23, 355-364. doi: 10.1111/j.1365-2826.2011.02110.x
48. Salama-Cohen, P., Arevalo, M.-A., Grantyn, R., and Rodriguez-Tebar, A. (2006). Notch and NGF/p75NTR control dendrite morphology and the balance of excitatory/inhibitory synaptic input to hippocampal neurones through Neurogenin 3. J. Neurochem. 97, 1269-1278. doi: 10.1111/j.1471-4159.2006. 03783.x
49. Scott, H. M., Mason, J. I., and Sharpe, R. M. (2009). Steroidogenesis in the fetal testis and its susceptibility to disruption by exogenous compounds. Endocr. Rev. 30, 883-925. doi: 10.1210/er.2009-2016
50. Semaan, S. J., and Kauffman, A. S. (2010). Sexual differentiation and development of forebrain reproductive circuits. Curr. Opin. Neurobiol. 20, 424-431. doi: 10.1016/j.conb.2010.04.004
51. Simon-Areces, J., Membrive, G., Garcia-Fernandez, C., Garcia-Segura, L. M., and Arevalo, M.-A. (2010). Neurogenin 3 cellular and subcellular localization in the developing and adult hippocampus. J. Comp. Neurol. 518, 1814-1824. doi: 10.1002/cne.22304
52. Smith-Bouvier, D. L., Divekar, A. A., Sasidhar, M., Du, S., Tiwari-Woodruff, S. K., King, J. K., et al. (2008). A role for sex chromosome complement in the female bias in autoimmune disease. J. Exp. Med. 205, 1099-1108. doi: 10.1084/jem. 20070850
53. Turner, J. M., Mahadevaiah, S. K., Benavente, R., Offenberg, H. H., Heyting, C., and Burgoyne, P. S. (2000). Analysis of male meiotic "sex body" proteins during XY female meiosis provides new insights into their functions. Chromosoma 109, 426-432. doi: 10.1007/s004120000097
54. Wijchers, P. J., and Festenstein, R. J. (2011). Epigenetic regulation of autosomal gene expression by sex chromosomes. Trends Genet. 27, 132-140. doi: 10.1016/j.tig.2011.01.004
55. Wittmann, W., Iulianella, A., and Gunhaga, L. (2014). Cux2 acts as a critical regulator for neurogenesis in the olfactoryepithelium of vertebrates. Dev. Biol. 388, 35-47. doi: 10.1016/j.ydbio.2014.01.026
56. Wolstenholme, J. T., Rissman, E. F., and Bekiranov, S. (2013). Sexual differentiation in the developing mouse brain: contributions of sex chromosome genes. Genes BrainBehav. 12, 166-180.doi: 10.1111/gbb.12010
57. Xu, J., Burgoyne, P. S., and Arnold, A. P. (2002). Sex differences in sex chromosome gene expression in mouse brain. Hum. Mol. Genet. 11, 1409-1419. doi: 10.1093/hmg/11.12.1409
58. Yang, F., Babak, T., Shendure, J., andDisteche, C. M. (2010). Global surveyof escape fromXinactivation byRNA-sequencinginmouse. GenomeRes. 20, 614-622. doi: 10.1101/gr.103200.109
59. Zwain, I. H., andYen, S. S. (1999). Neurosteroidogenesis in astrocytes, oligodendrocytes, and neurons of cerebral cortex of rat brain. Endocrinology 140, 3843-3852. doi: 10.1210/endo.140.8.6907