Sex differences in NeuN- and androgen receptor-positive cells in the bed nucleus of the stria terminalis are due to Bax-dependent cell death

Neuroscience

Volumn 158, Issue 4, 2009, Pages 1251-1256

  Holmes, M M ^a   McCutcheon, J ^a   Forger, N G ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

apoptosis; cell death; differentiation; GFAP; sex difference; testosterone

Indexed keywords

ANDROGEN RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; NEURON SPECIFIC NUCLEAR PROTEIN; PROTEIN BAX; THIONINE;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; ASTROCYTE; BRAIN CELL; BRAIN NUCLEUS; BRAIN WEIGHT; CELL COUNT; CELL DEATH; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; FEMALE; GENE DELETION; HORMONE RESPONSE; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MALE; MOUSE; NERVE CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SEX DIFFERENCE; STEREOLOGY; STRIA TERMINALIS; TISSUE SECTION; WILD TYPE;

ANALYSIS OF VARIANCE; ANIMALS; BCL-2-ASSOCIATED X PROTEIN; CELL COUNT; CELL DEATH; FEMALE; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; MALE; MICE; MICE, KNOCKOUT; NEURONS; PHOSPHOPYRUVATE HYDRATASE; RECEPTORS, ANDROGEN; SEPTAL NUCLEI; SEX CHARACTERISTICS;

EID: 60149098169     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.11.020     Document Type: Article

References (36)

1. Allen L.S., and Gorski R.A. Sex difference in the bed nucleus of the stria terminalis of the human brain. J Comp Neurol 302 (1990) 697-706
2. Burne J.F., Staple J.K., and Raff M.C. Glial cells are increased proportionally in transgenic optic nerves with increased numbers of axons. J Neurosci 16 (1996) 2064-2073
3. Buss R.R., Gould T.W., Ma J., Vinsant S., Prevette D., Winseck A., Toops K.A., Hammarback J.A., Smith T.L., and Oppenheim R.W. Neuromuscular development in the absence of programmed cell death: phenotypic alteration of motoneurons and muscle. J Neurosci 26 (2006) 13413-13427
4. Degenhardt K., Sundararajan R., Lindsten T., Thompson C., and White E. Bax and Bak independently promote cytochrome C release from mitochondria. J Biol Chem 277 (2002) 14127-14134
5. De Vries G.J., and al-Shamma H.A. Sex differences in hormonal responses of vasopressin pathways in the rat brain. J Neurobiol 21 (1990) 686-693
6. del Abril A., Segovia S., and Guillamon A. The bed nucleus of the stria terminalis in the rat: regional sex differences controlled by gonadal steroids early after birth. Brain Res 429 (1987) 295-300
7. De Vries G.J., Jardon M., Reza M., Rosen G.J., Immerman E., and Forger N.G. Sexual differentiation of vasopressin innervations of the brain: cell death versus phenotypic differentiation. Endocrinology 149 (2008) 4632-4637
8. Fan H., Favero M., and Vogel M.W. Elimination of Bax expression in mice increases cerebellar Purkinje cell numbers but not the number of granule cells. J Comp Neurol 436 (2001) 82-91
9. Forger N.G. Cell death and sexual differentiation of the nervous system. Neuroscience 138 (2006) 929-938
10. Forger N.G., Rosen G.J., Waters E.M., Jacob D., Simerly R.B., and de Vries G.J. Deletion of Bax eliminates sex differences in the mouse forebrain. Proc Natl Acad Sci U S A 101 (2004) 13666-13671
11. Greco B., Allegretto E.A., Tetel M.J., and Blaustein J.D. Coexpression of ER beta with ER alpha and progestin receptor proteins in the female rat forebrain: effects of estradiol treatment. Endocrinology 142 (2001) 5172-5181
12. Guillamon A., Segovia S., and del Abril A. Early effects of gonadal steroids on the neuron number in the medial posterior region and the lateral division of the bed nucleus of the stria terminalis in the rat. Brain Res Dev Brain Res 44 (1988) 281-290
13. Han T.M., and De Vries G.J. Neurogenesis of galanin cells in the bed nucleus of the stria terminalis and centromedial amygdala in rats: a model for sexual differentiation of neuronal phenotype. J Neurobiol 38 (1999) 491-498
14. Hines M., Davis F.C., Coquelin A., Goy R.W., and Gorski R.A. Sexually dimorphic regions in the medial preoptic area and the bed nucleus of the stria terminalis of the guinea pig brain: a description and an investigation of their relationship to gonadal steroids in adulthood. J Neurosci 5 (1985) 40-47
15. Itoh T., Itoh A., and Pleasure D. Bcl-2-related protein family gene expression during oligodendroglial differentiation. J Neurochem 85 (2003) 1500-1512
16. Jacob D.A., Bengston C.L., and Forger N.G. Effects of Bax gene deletion on muscle and motoneuron degeneration in a sexually dimorphic neuromuscular system. J Neurosci 25 (2005) 5638-5644
17. Jung A.R., Kim T.W., Rhyu I.J., Kim H., Lee Y.D., Vinsant S., Oppenheim R.W., and Sun W. Misplacement of Purkinje cells during postnatal development in Bax knock-out mice: a novel role for programmed cell death in the nervous system?. J Neurosci 28 (2008) 2941-2948
18. Jyotika J., McCutcheon J., Laroche J., Blaustein J.D., and Forger N.G. Deletion of Bax gene disrupts sexual behavior and modestly impairs motor function in mice. Dev Neurobiol 67 (2007) 1511-1519
19. Lindsten T., Ross A.J., King A., Zong W.X., Rathmell J.C., Shiels H.A., Ulrich E., Waymire K.G., Mahar P., Frauwirth K., Chen Y., Wei M., Eng V.M., Adelman D.M., Simon M.C., Ma A., Golden J.A., Evan G., Korsmeyer S.J., MacGregor G.R., and Thompson C.B. The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol Cell 6 (2000) 1389-1399
20. Malsbury C.W., and McKay K. A sex difference in the pattern of substance P-like immunoreactivity in the bed nucleus of the stria terminalis. Brain Res 420 (1987) 365-370
21. Merry D.E., and Korsmeyer S.J. Bcl-2 gene family in the nervous system. Annu Rev Neurosci 20 (1997) 245-267
22. Micevych P.E., Matt D.W., and Go V.L. Concentrations of cholecystokinin, substance P, and bombesin in discrete regions of male and female rat brain: sex differences and estrogen effects. Exp Neurol 100 (1988) 416-425
23. Mitra S.W., Hoskin E., Yudkovitz J., Pear L., Wilkinson H.A., Hayashi S., Pfaff D.W., Ogawa S., Rohrer S.P., Schaeffer J.M., McEwen B.S., and Alves S.E. Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 144 (2003) 2055-2067
24. Shah N.M., Pisapia D.J., Maniatis S., Mendelsohn M.M., Nemes A., and Axel R. Visualizing sexual dimorphism in the brain. Neuron 43 (2004) 313-319
25. Simerly R.B. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 25 (2002) 507-536
26. Simerly R.B., Chang C., Muramatsu M., and Swanson L.W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 294 (1990) 76-95
27. Simerly R.B., Zee M.C., Pendleton J.W., Lubahn D.B., and Korach K.S. Estrogen receptor-dependent sexual differentiation of dopaminergic neurons in the preoptic region of the mouse. Proc Natl Acad Sci U S A 94 (1997) 14077-14082
28. Sun W., Gould T.W., Vinsant S., Prevette D., and Oppenheim R.W. Neuromuscular development after the prevention of naturally occurring neuronal death by Bax deletion. J Neurosci 23 (2003) 7298-7310
29. Sun W., Winseck A., Vinsant S., Park O.H., Kim H., and Oppenheim R.W. Programmed cell death of adult-generated hippocampal neurons is mediated by the proapoptotic gene Bax. J Neurosci 24 (2004) 11205-11213
30. Uo T., Kinoshita Y., and Morrison R.S. Neurons exclusively express N-Bak, a BH3 domain-only Bak isoform that promotes neuronal apoptosis. J Biol Chem 280 (2005) 9065-9073
31. Wei M.C., Zong W.X., Cheng E.H., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacGregor G.R., Thompson C.B., and Korsmeyer S.J. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292 (2001) 727-730
32. Wersinger S.R., Sannen K., Villalba C., Lubahn D.B., Rissman E.F., and De Vries G.J. Masculine sexual behavior is disrupted in male and female mice lacking a functional estrogen receptor alpha gene. Horm Behav 32 (1997) 176-183
33. White F.A., Keller-Peck C.R., Knudson C.M., Korsmeyer S.J., and Snider W.D. Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J Neurosci 18 (1998) 1428-1439
34. Winseck A.K., Caldero J., Ciutat D., Prevette D., Scott S.A., Wang G., Esquerda J.E., and Oppenheim R.W. In vivo analysis of Schwann cell programmed cell death in the embryonic chick: regulation by axons and glial growth factor. J Neurosci 22 (2002) 4509-4521
35. Yu L.Y., Saarma M., and Arumae U. Death receptors and caspases but not mitochondria are activated in the GDNF- or BDNF-deprived dopaminergic neurons. J Neurosci 28 (2008) 7467-7475
36. Zhou L., Blaustein J.D., and De Vries G.J. Distribution of androgen receptor immunoreactivity in vasopressin- and oxytocin-immunoreactive neurons in the male rat brain. Endocrinology 134 (1994) 2622-2627