Overexpression of Bcl-2 reduces sex differences in neuron number in the brain and spinal cord

Journal of Neuroscience

Volumn 23, Issue 6, 2003, Pages 2357-2362

  Zup, Susan L ^a   Carrier, Heather ^a   Waters, Elizabeth M ^b   Tabor, Abigail ^a   Bengston, Lynn ^a   Rosen, Greta J ^a   Simerly, Richard B ^b   Forger, Nancy G ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Anteroventral periventricular nucleus; Bcl 2; Cell death; Nervous system; Sex difference; Spinal nucleus of the bulbocavernosus

Indexed keywords

PROTEIN BCL 2; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL COUNT; CELL DEATH; CELL DENSITY; CELL SURVIVAL; GENE OVEREXPRESSION; GONADOTROPIN RELEASE; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IMMUNOREACTIVITY; MALE; MOTONEURON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SEX DIFFERENCE;

EID: 0037444449     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-06-02357.2003     Document Type: Article

References (58)

1. Alexander MJ, Kirly ZJ, Leeman SE (1991) Sexually dimorphic distribution of neurotensin/neuromedin N mRNA in the rat preoptic area. J Comp Neurol 311:84-96.
2. Alkayed NJ, Goto S, Sugo N, Joh HD, Klaus J, Crain BJ, Bernard O, Traystman RJ, Hurn PD (2001) Estrogen and Bcl-2: gene induction and effect of transgene in experimental stroke. J Neurosci 21:7543-7550.
3. Allsopp TE, Wyatt S, Paterson HF, Davies AM (1993) The proto-oncogene bcl-2 can selectively rescue neurotrophic factor-dependent neurons from apoptosis. Cell 73:295-307.
4. Arai Y, Sekine Y, Murakami S (1996) Estrogen and apoptosis in the developing sexually dimorphic preoptic area in female rats. Neurosci Res 25:403-407.
5. Bleier R, Byne W, Siggelkow I (1982) Cytoarchitectonic sexual dimorphisms of the medial preoptic and anterior hypothalamic areas in guinea pig, rat, hamster, and mouse. J Comp Neurol 212:118-130.
6. Bloch GJ, Kurth SM, Akesson TR, Micevych PE (1992) Estrogenconcentrating cells within cell groups of the medial preoptic area: sex differences and co-localization with galanin-immunoreactive cells. Brain Res 595:301-308.
7. Bonfanti L, Strettoi E, Chierzi S, Cenni MC, Liu XH, Martinou J-C, Maffei L, Rabacchi SA (1996) Protection of retinal ganglion cells from natural and axotomy-induced cell death in neonatal transgenic mice overexpressing bcl-2. J Neurosci 16:4186-4194.
8. Breedlove SM, Arnold AP (1980) Hormone accumulation in a sexually dimorphic motor nucleus of the rat spinal cord. Science 210:564-566.
9. Breedlove SM, Arnold AP (1983) Hormonal control of a developing neuromuscular system. I. Complete demasculinization of the male rat spinal nucleus of the bulbocavernosus using the anti-androgen flutamide. J Neurosci 3:417-423.
10. Cihak R, Gutmann E, Hanzlikova V (1970) Involution and hormone-induced persistence of the M. Sphincter (levator) ani in female rats. J Anat 106:93-110.
11. Coulpier M, Junier MP, Peschanski M, Dreyfus PS (1996) Bcl-2 sensitivity differentiates two pathways for motoneuronal death in wobbler mutant mouse. J Neurosci 16:5897-5904.
12. Deckwerth TL, Elliot JL, Knudson CM, Johnson EMJ, Snider WD, Korsmeyer SJ (1996) BAX is required for neuronal death after trophic factor deprivation and during development. Neuron 17:401-411.
13. Dubal DB, Shughrue PJ, Wilson ME, Merchenthaler I, Wise PM (1999) Estradiol modulates bcl-2 in cerebral ischemia: a potential role for estrogen receptors. J Neurosci 19:6385-6393.
14. Dubois-Dauphin M, Frankowski H, Tsujimoto Y, Huarte J, Martinou JC (1994) Neonatal motoneurons overexpressing the bcl-2 protooncogene in transgenic mice are protected from axotomy-induced cell death. Proc Natl Acad Sci USA 91:3309-3313.
15. Elliott JL, Snider WD (1996) Motor neuron growth factors. Neurol 47[Suppl 2]:S47-S53.
16. Farlie PG, Dringen R, Rees SM, Kannourakis G, Bernard O (1995) bcl-2 transgene expression can protect neurons against developmental and induced cell death. Proc Natl Acad Sci USA 92:4397-4401.
17. Forger NG (2001) The development of sex differences in the nervous system. In: Developmental psychobiology, the handbook of behavioral neurobiology, Vol 13 (Blass E, ed), pp 153-208. New York: Plenum.
18. Forger NG, Hodges LL, Roberts SL, Breedlove SM (1992) Regulation of motoneuron death in the spinal nucleus of the bulbocavernosus. J Neurobiol 23:1192-1203.
19. Forger NG, Howell ML, Bengston L, MacKenzie L, DeChiara TM, Yancopoulos GD (1997) Sexual dimorphism in the spinal cord is absent in mice lacking the ciliary neurotrophic factor receptor. J Neurosci 17:9605-9612.
20. Garcia-Segura LM, Cardona-Gomez P, Naftolin F, Chowen JA (1998) Estradiol upregulates Bcl-2 expression in adult brain neurons. Neuro Report 9:593-597.
21. Green PS, Simpkins JW (2000) Neuroprotective effects of estrogens: potential mechanisms of action. Int J Dev Neurosci 18:347-358.
22. Hengartner MO (2000) The biochemistry of apoptosis. Nature 407:770-776.
23. Herbison AE, Dye S (1993) Perinatal and adult factors responsible for the sexually dimorphic calcitonin gene-related peptide-containing cell population in the rat preoptic area. Neuroscience 54:991-999.
24. Hollyday M, Hamburger V (1976) Reduction of the naturally occurring motor neuron loss by enlargement of the periphery. J Comp Neurol 170:311-320.
25. Hsu C, Hsieh Y-L, Yang R-C, Hsu H-K (2000) Blockage of N-methyl-D-aspartate receptors decreases testosterone levels and enhances postnatal neuronal apoptosis in the preoptic area of male rats. Neuroendocrinology 71:301-307.
26. Huang Y, Ray S, Reed JC, Ibrado AM, Tang C, Nawabi A, Bhalla K (1997) Estrogen increases intracellular p26Bcl-2 to p21Bax ratios and inhibits taxol-induced apoptosis of human breast cancer MCF-7 cells. Breast Cancer Res Treat 42:73-81.
27. Jordan CL, Breedlove SM, Arnold AP (1982) Sexual dimorphism and the influence of neonatal androgen in the dorsolateral motor nucleus of the rat lumbar spinal cord. Brain Res 249:309-314.
28. Kandouz M, Siromachkova M, Jacob D, Chretien Marquet B, Therwath A, Gompel A (1996) Antagonism between estradiol and progestin on Bcl-2 expression in breast-cancer cells. Int J Cancer 68:120-125.
29. Kandouz M, Lombet A, Perrot JY, Jacob D, Carvajal S, Kazem A, Rostene W, Therwath A, Gompel A (1999) Proapoptotic effects of antiestrogens, progestins and androgen in breast cancer cells. J Steroid Biochem Mol Biol 69:463-471.
30. Konigsmark BW (1970) Methods for the counting of neurons. In: Contemporary research methods in neuroanatomy (Nauta WJH, Ebbeson SOE, eds), pp 315-340. New York: Springer.
31. Lapointe J, Fournier A, Richard V, Labrie C (1999) Androgens downregulate bcl-2 protooncogene expression in ZR-75-1 human breast cancer cells. Endocrinology 140:416-421.
32. Leslie M, Forger NG, Breedlove SM (1991) Sexual dimorphism and androgen effects on spinal motoneurons innervating the rat flexor digitorum brevis. Brain Res 561:269-273.
33. Marangos PJ, Schmechel DE, Parma AM, Goodwin FK (1980) Developmental profile of neuron-specific (NSE) and non-neuronal (NNE) enolase. Brain Res 190:185-193.
34. Martin LJ (2001) Neuronal cell death in nervous system development, disease, and injury. Int J Mol Med 7:455-478.
35. Martinou JC, Dubois-Dauphin M, Staple JK, Rodriguez I, Frankowski H, Missotten M, Albertini P, Talabot D, Catsicas S, Pietra C (1994) Over-expression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron 13:1017-1030.
36. Murakami S, Arai Y (1989) Neuronal death in the developing sexually dimorphic periventricular nucleus of the preoptic area in the female rat: effect of neonatal androgen treatment. Neurosci Lett 102:185-190.
37. Nilsen J, Mor G, Naftolin F (2000) Estrogen-regulated developmental neuronal apoptosis is determined by estrogen receptor subtype and the Fas/Fas ligand system. J Neurobiol 43:64-78.
38. Nishizuka M, Sumida H, Kano Y, Arai Y (1993) Formation of neurons in the sexually dimorphic anteroventral periventricular nucleus of the preoptic area of the rat: effects of prenatal treatment with testosterone propionate. J Neuroendocrinol 5:569-573.
39. Nordeen EJ, Nordeen KW, Sengelaub DR, Arnold AP (1985) Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus. Science 229:671-673.
40. Oppenheim RW (1991) Cell death during development of the nervous system. Annu Rev Neurosci 14:453-501.
41. Park JJ, Howell M, Winseck A, Forger NG (1999) Effects of testosterone on the development of a sexually dimorphic neuromuscular system in ciliary neurotrophic factor receptor knockout mice. J Neurobiol 41:317-325.
42. Park JJ, Zup SL, Verhovshek T, Sengelaub DR, Forger NG (2002) Castration reduces motoneuron soma size but not dendritic length in the spinal nucleus of the bulbocavernosus of wild-type and BCL-2 overexpressing mice. J Neurobiol 53:403-412.
43. Raoul C, Henderson CE, Pettmann B (1999) Programmed cell death of embryonic motoneurons triggered through the Fas death receptor. J Cell Biol 147:1049-1062.
44. Schroder HD (1980) Organization of the motoneurons innervating the pelvic muscles of the male rats. J Comp Neurol 192:567-587.
45. Simerly RB (1991) Prodynorphin and proenkephalin gene expression in the anteroventral periventricular nucleus of the rat: sexual differentiation and hormonal regulation. Mol Cell Neurosci 2:473-484.
46. Simerly RB (1998) Organization and regulation of sexually dimorphic neuroendocrine pathways. Behav Brain Res 92:195-203.
47. Simerly RB, Swanson LW, Handa RJ, Gorski RA (1985) Influence of perinatal androgen on the sexually dimorphic distribution of tyrosine hydroxylase-immunoreactive cells and fibers in the anteroventral periventricular nucleus of the rat. Neuroendocrinology 40:501-510.
48. Simerly RB, Zee MC, Pendleton JW, Lubahn DB, Korach KS (1997) Estrogen receptor-dependent sexual differentiation of dopaminergic neurons in the preoptic region of the mouse. Proc Natl Acad Sci USA 94:14077-14082.
49. Sumida H, Nishizuka M, Kano Y, Arai Y (1993) Sex differences in the anteroventral periventricular nucleus of the preoptic area and in the related effects of androgen in prenatal rats. Neurosci Lett 151:41-44.
50. Tobet SA, Hanna IK (1997) Ontogeny of sex differences in the mammalian hypothalamus and preoptic area. Cell Mol Neurobiol 17:565-601.
51. Tobin C, Joubert Y (1991) Testosterone-induced development of the rat levator ani muscle. Dev Biol 146:131-138.
52. Wagner CK, Clemens LG (1989) Perinatal modification of a sexually dimorphic motor nucleus in the spinal cord of the B6D2F1 house mouse. Physiol Behav 45:831-835.
53. Wang TT, Phang JM (1995) Effects of estrogen on apoptotic pathways in human breast cancer cell line MCF-7. Cancer Res 55:2487-2489.
54. Waters EM, Simerly RB (2002) Estrogen-mediated programmed cell death during development of a sexually dimorphic hypothalamic nucleus. Soc Neurosci Abstr 28:33.5.
55. Wee B, Clemens LG (1987) Characteristics of the spinal nucleus of the bulbocavernosus are influenced by genotype in the house mouse. Brain Res 424:305-310.
56. Yang E, Korsmeyer SJ (1996) Molecular thanatopsis: a discourse on the BCL2 family and cell death. Blood 88:386-401.
57. Zup SL (2002) The role of Bcl-2 family members in sexual differentiation and adult neural plasticity. PhD thesis, University of Massachusetts.
58. Zup SL, Forger NG (2002) Testosterone regulates BCL-2 immunoreactivity in a sexually dimorphic motor pool of adult rats. Brain Res 950:312-316.