Estrogen deficiency leads to apoptosis in dopaminergic neurons in the medial preoptic area and arcuate nucleus of male mice

Molecular and Cellular Neuroscience

Volumn 27, Issue 4, 2004, Pages 466-476

  Hill, Rachel A ^a,b   Pompolo, Sueli ^a   Jones, Margaret E E ^a   Simpson, Evan R ^a,b   Boon, Wah Chin ^b  

^a HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 8; DOPAMINE; ESTROGEN; PROTEIN BCL 2; RIBONUCLEASE; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; APOPTOSIS; ARCUATE NUCLEUS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DOWN REGULATION; ENZYMATIC ASSAY; ENZYME ACTIVITY; ESTROGEN DEFICIENCY; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; SEX DIFFERENTIATION; UPREGULATION; WILD TYPE;

EID: 9144268411     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2004.04.012     Document Type: Article

References (53)

1. D.M. Armstrong, C.A. Ross, V.M. Pickel, T.H. Joh, and D.J. Reis Distribution of dopamine-, noradrenaline-, and adrenaline-containing cell bodies in the rat medulla oblongata: demonstrated by the immunocytochemical localization of catecholamine biosynthetic enzymes J. Comp. Neurol. 212 1982 173 187
2. J. Balthazart, and P. Absil Identification of catecholaminergic inputs to and outputs from aromatase-containing brain areas of the Japanese quail by tract tracing combined with tyrosine hydroxylase immunocytochemistry J. Comp. Neurol. 382 1997 401 428
3. D. Bitran, and E.M. Hull Pharmacological analysis of male rat sexual behavior Neurosci. Biobehav. Rev. 11 1987 365 389
4. J.R. Blackburn, J.G. Pfaus, and A.G. Phillips Dopamine functions in appetitive and defensive behaviours Prog. Neurobiol. 39 1992 247 279
5. J. Brawer, J. Bertley, and A. Beaudet Testosterone inhibition of tyrosine hydroxylase expression in the hypothalamic arcuate nucleus Neurosci. Lett. 67 1986 313 318
6. L. Dong, W. Wang, F. Wang, M. Stoner, J.C. Reed, M. Harigai, I. Samudio, M.P. Kladde, C. Vyhlidal, and S. Safe Mechanisms of transcriptional activation of bcl-2 gene expression by 17beta-estradiol in breast cancer cells J. Biol. Chem. 274 1999 32099 32107
7. D.B. Dubal, M.L. Kashon, L.C. Pettigrew, J.M. Ren, S.P. Finklestein, S.W. Rau, and P.M. Wise Estradiol protects against ischemic injury J. Cereb. Blood Flow Metab. 18 1998 1253 1258
8. G. Emilien, K. Beyreuther, C.L. Masters, and J.M. Maloteaux Prospects for pharmacological intervention in Alzheimer disease Arch. Neurol. 57 2000 454 459
9. C.R. Fisher, K.H. Graves, A.F. Parlow, and E.R. Simpson Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene Proc. Natl. Acad. Sci. U. S. A. 95 1998 6965 6970
10. L.M. Garcia-Segura, P. Cardona-Gomez, F. Naftolin, and J.A. Chowen Estradiol upregulates Bcl-2 expression in adult brain neurons NeuroReport 9 1998 593 597
11. D.C. Gerardin, and O.C. Pereira Reproductive changes in male rats treated perinatally with an aromatase inhibitor Pharmacol. Biochem. Behav. 71 2002 301 305
12. F. Giuliano, and J. Allard Dopamine and male sexual function Eur. Urol. 40 2001 601 608
13. L. Grant, and W.E. Stumpf Hormone uptake sites in CNS biogenic amines systems Anat. Neuroendocrinol., Karger 1975 445 666
14. J.W. Gunnet, K.J. Lookingland, and K.E. Moore Comparison of the effects of castration and steroid replacement on incertohypothalamic dopaminergic neurons in male and female rats Neuroendocrinology 44 1986 269 275
15. S.D. Hall ED Gender differences in infarct size in mice after permanant focal ischaemia and in the protective effects of CuZu superoxide dismutase over expression-Soc Neuroscience 24 1998 1256
16. C. Harms, M. Lautenschlager, and A. Bergk Differential mechanism of neuroprotection by 17 beta-estradiol in apoptotic versus necrotic neurodegeneration J. Neurosci. 21 2001 2600 2609
17. K.N. Hewitt, W.C. Boon, Y. Murata, M.E. Jones, and E.R. Simpson The aromatase knockout mouse presents with a sexually dimorphic disruption to cholesterol homeostasis Endocrinology 144 2003 3895 3903
18. T. Hokfelt Possible site of action of dopamine in the hypothalamic pituitary control Acta Physiol. Scand. 89 1973 606 608
19. T. Hokfelt, K. Fuxe, O. Johansson, and A. Ljungdahl Pharmaco- histochemical evidence of the existence of dopamine nerve terminals in the limbic cortex Eur. J. Pharmacol. 25 1974 108 112
20. T. Hokfelt, L. Skirboll, J.F. Rehfeld, M. Goldstein, K. Markey, and O. Dann A subpopulation of mesencephalic dopamine neurons projecting to limbic areas contains a cholecystokinin-like peptide: evidence from immunohistochemistry combined with retrograde tracing Neuroscience 5 1980 2093 2124
21. E.M. Hull, J. Du, D.S. Lorrain, and L. Matuszewich Extracellular dopamine in the medial preoptic area: implications for sexual motivation and hormonal control of copulation J. Neurosci. 15 1995 7465 7471
22. T. Ivanova, and C. Beyer Estrogen regulates tyrosine hydroxylase expression in the neonate mouse midbrain J. Neurobiol. 54 2003 638 647
23. T. Ivanova, E. Kuppers, J. Engele, and C. Beyer Estrogen stimulates brain-derived neurotrophic factor expression in embryonic mouse midbrain neurons through a membrane-mediated and calcium-dependent mechanism J. Neurosci. Res. 66 2001 221 230
24. M.E. Jones, A.W. Thorburn, K.L. Britt, K.N. Hewitt, N.G. Wreford, J. Proietto, O.K. Oz, B.J. Leury, K.M. Robertson, S. Yao, and E.R. Simpson Aromatase-deficient (ArKO) mice have a phenotype of increased adiposity Proc. Natl. Acad. Sci. U. S. A. 97 2000 12735 12740
25. S. Kawashima, and K. Takagi Role of sex steroids on the survival, neuritic outgrowth of neurons, and dopamine neurons in cultured preoptic area and hypothalamus Horm. Behav. 28 1994 305 312
26. E.J. Lee, W.R. Duan, M. Jakacka, B.D. Gehm, and J.L. Jameson Dominant negative ER induces apoptosis in GH(4) pituitary lactotrope cells and inhibits tumor growth in nude mice Endocrinology 142 2001 3756 3763
27. E.D. Lephart A review of brain aromatase cytochrome P450 Brain Res. Brain Res. Rev. 22 1996 1 26
28. M.P. Mattson, N. Robinson, and Q. Guo Estrogens stabilize mitochondrial function and protect neural cells against the pro-apoptotic action of mutant presenilin-1 NeuroReport 8 1997 3817 3821
29. L.D. McCullough, K. Blizzard, E.R. Simpson, O.K. Oz, and P.D. Hurn Aromatase cytochrome P450 and extragonadal estrogen play a role in ischemic neuroprotection J. Neurosci. 23 2003 8701 8705
30. J.L. McGrire, and R.D. Lisk Localization of estrogen receptors in the rat hypothalamus Neuroendocrinology 4 1969 289 295
31. F. Naftolin, and N.J. MacLusky Aromatase in the central nervous system Cancer Res. 42 1982 3274s 3276s
32. S. Ogawa, A.E. Chester, S.C. Hewitt, V.R. Walker, J.A. Gustafsson, O. Smithies, K.S. Korach, and D.W. Pfaff From the cover: abolition of male sexual behaviors in mice lacking estrogen receptors alpha and beta (alpha beta ERKO) Proc. Natl. Acad. Sci. U. S. A. 97 2000 14737 14741
33. B. Olivier, R. Olivier-Aardema, and P.R. Wiepkema Effect of anterior hypothalamic and mammillary area lesions on territorial aggressive behaviour in male rats Behav. Brain Res. 9 1983 59 81
34. A. Pecci, A. Scholz, D. Pelster, and M. Beato Progestins prevent apoptosis in a rat endometrial cell line and increase the ratio of bcl-XL to bcl-XS J. Biol. Chem. 272 1997 11791 11798
35. C. Pike Estrogen modulates neuronal Bcl-xL expression and beta-amyloid-induced apoptosis: relevance to Alzheimer's Disease J. Neurochem. 72 1999 1552 1563
36. K.M. Robertson, E.R. Simpson, O. Lacham-Kaplan, and M.E. Jones Characterization of the fertility of male aromatase knockout mice J. Androl. 22 2001 825 830
37. A. Sainsbury, G.J. Cooney, and H. Herzog Hypothalamic regulation of energy homeostasis Best Pract. Res. Clin. Endocrinol. Metab. 16 2002 623 637
38. M. Sar Estradiol is concentrated in tyrosine hydroxylase-containing neurons of the hypothalamus Science 223 1984 938 940
39. H. Sawada, M. Ibi, T. Kihara, K. Honda, T. Nakamizo, R. Kanki, M. Nakanishi, N. Sakka, A. Akaike, and S. Shimohama Estradiol protects dopaminergic neurons in a MPP+Parkinson's disease model Neuropharmacology 42 2002 1056 1064
40. M.K. Selmanoff, L.D. Brodkin, R.I. Weiner, and P.K. Siiteri Aromatization and 5alpha-reduction of androgens in discrete hypothalamic and limbic regions of the male and female rat Endocrinology 101 1977 841 848
41. R.B. Simerly, C. Chang, M. Muramatsu, and L.W. Swanson 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
42. R.B. Simerly, M.C. Zee, J.W. Pendleton, D.B. Lubahn, and K.S. Korach 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
43. W.E. Stumpf Probable sites for estrogen receptors in brain and pituitary J. Neuro-Visc. Relat. 0 Suppl 10 1971 51 64
44. M.X. Tang, D. Jacobs, Y. Stern, K. Marder, P. Schofield, B. Gurland, H. Andrews, and R. Mayeux Effect of oestrogen during menopause on risk and age at onset of Alzheimer's disease Lancet 348 1996 429 432
45. K. Toda, T. Saibara, T. Okada, S. Onishi, and Y. Shizuta A loss of aggressive behaviour and its reinstatement by oestrogen in mice lacking the aromatase gene (Cyp19) J. Endocrinol. 168 2001 217 220
46. S.B. Wade, P. Oommen, W.C. Conner, D.J. Earnest, and R.C. Miranda Overlapping and divergent actions of estrogen and the neurotrophins on cell fate and p53-dependent signal transduction in conditionally immortalized cerebral cortical neuroblasts J. Neurosci. 19 1999 6994 7006
47. A.S. Wang, M. Warner, and J. Gustafsson Morphological abnormalities in the brains of estrogen receptor beta knockout mice Proc. Natl. Acad. Sci. 98 2001 2792 2796
48. S.R. Wersinger, and E.F. Rissman Dopamine activates masculine sexual behavior independent of the estrogen receptor alpha J. Neurosci. 20 2000 4248 4254
49. B. Wiedenmann, and W.W. Franke Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles Cell 41 1985 1017 1028
50. H. Xu, G.K. Gouras, and J.P. Greenfield Estrogen reduces neuronal generation of Alzheimer beta-amyloid peptides Nat. Med. 4 1998 447 451
51. K. Yuri, and M. Kawata Region-specific changes of tyrosine hydroxylase-immunoreactivity by estrogen treatment in female rat hypothalamus Brain Res. 645 1994 278 284
52. H. Zha, C. Aime-Sempe, T. Sato, and J.C. Reed Proapoptotic protein Bax heterodimerizes with Bcl-2 and homodimerizes with Bax via a novel domain (BH3) distinct from BH1 and BH2 J. Biol. Chem. 271 1996 7440 7444
53. H. Zhang, B. Saeed, and S.C. Ng Combinatorial interaction of human bcl-2 related proteins: mapping of regions important for bcl-2/bcl-x-s interaction Biochem. Biophys. Res. Commun. 208 1995 950 956