Synaptic long-term potentiation and depression in the rat medial vestibular nuclei depend on neural activation of estrogenic and androgenic signals

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Scarduzio, Mariangela ^a   Panichi, Roberto ^a   Pettorossi, Vito Enrico ^a   Grassi, Silvarosa ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; ANDROSTANOLONE; AROMATASE; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; FINASTERIDE; FLUTAMIDE; FULVESTRANT; TESTOSTERONE;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; ESTROGEN SYNTHESIS; EXCITATORY POSTSYNAPTIC POTENTIAL; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MEDIAL VESTIBULAR NUCLEUS; NERVE CELL PLASTICITY; NONHUMAN; RAT; TESTOSTERONE SYNTHESIS; WHOLE CELL PATCH CLAMP;

ANDROGENS; ANIMALS; ELECTRIC STIMULATION; ESTROGENS; EVOKED POTENTIALS; GONADAL STEROID HORMONES; MALE; NEURONAL PLASTICITY; NEURONS; RATS; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; VESTIBULAR NUCLEI;

EID: 84892969150     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080792     Document Type: Article

References (51)

1. McEwen BS (2002) Estrogen actions throughout the brain. Recent Prog Horm Res 57: 357-384. doi:10.1210/rp.57.1.357. PubMed: 12017552.
2. Isgor C, Sengelaub DR (2003) Effects of gonadal steroids on adult CA3 pyramidal neuron dendritic morphology and spatial memory in rats. J Neurobiol 55: 179-190. doi:10.1002/neu.10200. PubMed: 12672016. (Pubitemid 36423157)
3. MacLusky NJ, Hajszan T, Prange-Kiel J, Leranth C (2006) Androgen modulation of hippocampal synaptic plasticity. Neurosci 138: 957-965. doi:10.1016/j.neuroscience.2005.12.054. PubMed: 16488544.
4. Hajszan T, MacLusky NJ, Leranth C (2008) Role of androgens and the androgen receptor in remodelling of spine synapses in limbic brain areas. Horm Behav 53: 638-646. doi:10.1016/j.yhbeh.2007.12.007. PubMed: 18262185.
5. Baulieu EE (1997) Neurosteroids: of the nervous system, by the nervous system, for the nervous system. Rec Prog Horm Res 52: 1-32. PubMed: 9238846.
6. Compagnone NA, Mellon SH (2000) Neurosteroids: biosynthesis and function of these novel neuromodulators. Front Neuroendocrinol 21: 1-56. doi:10.1006/frne.1999.0188. PubMed: 10662535. (Pubitemid 30105920)
7. Naftolin F, Ryan KJ, Davies IJ, Petro Z, Kuhn M (1975) The formation and metabolism of estrogens in brain tissues. Adv Biosci 15: 105-121. PubMed: 1164960.
8. Selmanoff MK, Brodkin LD, Weiner RI, Siiteri PK (1977) Aromatization and 5alpha-reduction of androgens in discrete hypothalamic and limbic regions of the male and female rat. Endocrinologist 101: 841-848. doi:10.1210/endo-101-3-841. PubMed: 891467. (Pubitemid 8191172)
9. Lephart ED (1993) A review of brain 5α-reductase: Cellular, enzymatic and molecular perspectives and implications for biological function. Mol Cell Neurosci 4: 473-484. doi:10.1006/mcne.1993.1059. PubMed: 19912954.
10. Simpson ER, Mahendroo MS, Means GD, Kilgore MW, Hinshelwood MM et al. (1994) Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev 15: 342-355. doi:10.1210/er.15.3.342. PubMed: 8076586. (Pubitemid 24180792)
11. Kimoto T, Tsurugizawa T, Ohta Y, Makino J, Tamura H et al. (2001) Neurosteroid synthesis by citochrome p450-containing systems localized in the rat brain. Endocrinologist 142: 3578-3589. doi:10.1210/en.142.8.3578.
12. Hojo Y, Hattori TA, Enami T, Furukawa A, Suzuki K et al. (2004) Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P450 17alpha and P450 aromatase localized in neurons. Proc Natl Acad Sci USA 101: 865-870. doi:10.1073/pnas.2630225100. PubMed: 14694190. (Pubitemid 38121049)
13. Mukai H, Takata N, Ishii HT, Tanabe N, Hojo J et al. (2006) Hippocampal synthesis of estrogens and androgens which are paracrine modulators of synaptic plasticity: synaptocrinology. Neurosci 138: 757-764. doi:10.1016/j.neuroscience. 2005.09.010. PubMed: 16310315.
14. Hojo Y, Murakami G, Mukai H, Higo S, Hatanaka Y et al. (2008) Estrogen synthesis in the brain. Role on synaptic plasticity and memory. Mol Cell Endocrinol 290: 31-43. doi:10.1016/j.mce.2008.04.017. PubMed: 18541362.
15. Hojo Y, Higo S, Ishii H, Ooishi Y, Mukai H et al. (2009) Comparison between hippocampus-synthesized and circulation-derived sex steroids in the hippocampus. Endocrinologist 150: 5106-5112. doi:10.1210/en.2009-0305. PubMed: 19589866.
16. Wong M, Thompson TL, Moss RL (1996) Nongenomic actions of estrogen in the brain: Physiological significance and cellular mechanisms. Cr Rev Neurosci 10: 189-203. PubMed: 8971129. (Pubitemid 27033851)
17. Tabori NE, Stewart LS, Znamensky V, Romeo RD, Alves SE et al. (2005) Ultrastructural evidence that androgen receptors are located at extranuclear sites in the rat hippocampal formation. Neurosci 130: 151-163. doi:10.1016/j.neuroscience.2004.08.048. PubMed: 15561432. (Pubitemid 39550422)
18. Pedram A, Razandi M, Levi AR (2006) Nature of functional estrogen receptors at the plasma membrane. Mol Endocrinol 20: 1996-2009. doi:10.1210/me.2005-0525. PubMed: 16645038. (Pubitemid 44286700)
19. Foradori CD, Weiser MJ, Handa RJ (2008) Non-genomic actions of androgens. Front Neuroendocrinol 29: 169-181. doi:10.1016/j.yfrne.2007.10.005. PubMed: 18093638.
20. Morissette M, Le Saux M, D'Astous M, Jourdain S, Sweidi SA et al. (2008) Contribution of estrogen receptors alpha and beta to the effects of estradiol in the brain. J Steroid Biochem Mol Biol 108: 327-338. doi:10.1016/j.jsbmb.2007. 09.011. PubMed: 17936613. (Pubitemid 351179644)
21. Raz L, Khan MM, Mahesh VB, Vadlamudi RK, Brann DW (2008) Rapid estrogen signalling in the brain. Neurosignals 16: 140-153. doi:10.1159/000111559. PubMed: 18253054.
22. Levin ER (2009) Plasma membrane estrogen receptors. Trends Endocrinol Metab 20: 477-482. doi:10.1016/j.tem.2009.06.009. PubMed: 19783454.
23. Grassi S, Frondaroli A, Di Mauro M, Pettorossi VE (2010a) Influence of Testosterone on synaptic transmission in the rat medial vestibular nuclei: estrogenic and androgenic effects. Neurosci 171: 666-676. doi:10.1016/j. neuroscience.2010.09.035. PubMed: 20884332.
24. Grassi S, Frondaroli A, Scarduzio M, Dutia MB, Dieni C et al. (2010b) Effects of 17β-estradiol on glutamate synaptic transmission and neuronal excitability in the rat medial vestibular nuclei. Neurosci 165: 1100-1114. doi:10.1016/j.neuroscience.2009.11.039.
25. Grassi S, Scarduzio M, Panichi R, Dall'Aglio C, Boiti C et al. (2013) Opposite long-term synaptic effects of 17β-estradiol and 5α-dyidrotestosterone and localization of their receptors in the medial vestibular nucleus of rats. Brain. Res Bull 97: 1-7. doi:10.1016/j.brainresbull. 2013.05.006.
26. Balthazart J, Baillien M, Ball GF (2006) Rapid control of brain aromatase activity by glutamatergic inputs. Endocrinologist 147: 359-366. PubMed: 16195408. (Pubitemid 43004289)
27. Ooishi Y, Kawato S, Hojo Y, Hatanaka Y, Higo S et al. (2012) Modulation of synaptic plasticity in the hippocampus by hippocampus-derived estrogen and androgen. J Steroid Biochem Mol Biol 131: 37-51. doi:10.1016/j.jsbmb.2011.10. 004. PubMed: 22075082.
28. Grassi S, Frondaroli A, Dieni C, Scarduzio M, Pettorossi VE (2009) Long-term potentiation in the rat medial vestibular nuclei depends on locally synthesised 17β-Estradiol. J Neurosci 29: 10779-10783. doi:10.1523/ JNEUROSCI.1697-09.2009. PubMed: 19710328.
29. Grassi S, Tozzi A, Costa C, Tantucci M, Colcelli E et al. (2011b) Neural 17β-Estradiol facilitates long-term potentiation in the hippocampal CA1 region. Neurosci 192: 67-73. doi:10.1016/j.neuroscience.2011.06.078.
30. Scarduzio M, Panichi R, Pettorossi VE, Grassi S (2012) The repetition timing of high frequency afferent stimulation drives the bidirectional plasticity at central synapses in the rat medial vestibular nuclei. Neurosci 223: 1-11. doi:10.1016/j.neuroscience.2012.07.039. PubMed: 22863673.
31. Gittis AH, du Lac S (2006) Intrinsic and synaptic plasticity in the vestibular system. Curr Opin Neurobiol 16: 385-390. doi:10.1016/j.conb.2006.06. 012. PubMed: 16842990. (Pubitemid 44142274)
32. Pettorossi VE, Dutia M, Frondaroli A, Dieni C, Grassi S (2003) Long-term potentiation and depression after unilateral labyrinthectomy in the medial vestibular nuclei of rats. Acta Otolaryngol 123: 182-186. doi:10.1080/ 0036554021000028093. PubMed: 12701737. (Pubitemid 36359788)
33. Grassi S, Frondaroli A, Scarduzio M, Dieni CV, Brecchia G et al. (2011a) Influence of sex and estrous cycle on synaptic responses of the medial vestibular nuclei in rats: role of circulating 17β-estradiol. Brain. Res Bull 87: 319-327.
34. Pettorossi VE, Frondaroli A, Grassi S (2011a) Cyclic estrogenic fluctuation influences synaptic transmission of the medial vestibular nuclei in female rats. Acta Otolaryngol 131: 434-439. doi:10.3109/00016489.2010.536992. PubMed: 21189054.
35. Serafin M, de Waele C, Khateb A, Vidal PP, Mühlethaler M (1991) Medial vestibular nucleus in the guinea-pig. I. Intrinsic membrane properties in brainstem slices. Exp Brain Res 84: 417-425. doi:10.1007/BF00231464. PubMed: 2065749.
36. Johnston AR, MacLeod NK, Dutia MB (1994) Ionic conductances contributing to spike depolarization and after-potentials in rat medial vestibular nucleus neurons. J Physiol 481: 61-77. PubMed: 7531769. (Pubitemid 24361348)
37. Babalian A, Vibert N, Assie G, Serafin M, Mühlethaler M et al. (1997) Central vestibular networks in the guinea-pig: functional characterization in the isolated whole brain in vitro. Neurosci 81: 405-426. doi:10.1016/S0306-4522(97)00069-9. PubMed: 9300431. (Pubitemid 27381997)
38. McElvain LE, Bagnall MW, Sakatos A, du Lac S (2010) Bidirectional plasticity gated by hyperpolarization controls the gain of postsynaptic firing responses at central vestibular nerve synapses. Neuron 68: 763-775. doi:10.1016/j.neuron.2010.09.025. PubMed: 21092864.
39. Ahmadiani A, Mandgary A, Sayyah M (2003) Anticonvulsant effect of flutamide on seizures induced by pentylenetetrazole: involvement of benzodiazepine receptors. Epilepsia 44: 629-635. doi:10.1046/j.1528-1157.2003. 36402.x. PubMed: 12752460. (Pubitemid 36554629)
40. Wade CB, Robinson S, Shapiro RA, Dorsa DM (2001) Estrogen Receptor (ER)α and ERβ exhibit unique pharmacologic properties when coupled to activation of the mitogen-activated protein kinase pathway. Endocrinologist 142: 2336-2342. doi:10.1210/en.142.6.2336. (Pubitemid 32473088)
41. Zhou ZX, Lane MV, Kemppainen JA, French FS, Wilson EM (1995) Specificity of ligand-dependent androgen receptor stabilization: receptor domain interactions influence ligand dissociation and receptor stability. Mol Endocrinol 9: 208-218. doi:10.1210/me.9.2.208. PubMed: 7776971.
42. Reddy DS (2004) Anticonvulsant activity of the testosterone-derived neurosteroid 3alpha-androstanediol. Neuroreport 15: 515-518. doi:10.1097/00001756-200403010-00026. PubMed: 15094514.
43. Handa RJ, Pak TR, Kudwa AE, Lund TD, Hinds L (2008) An alternate pathway for androgen regulation of brain function: Activation of estrogen receptor beta by the metabolite of dihydrotestosterone, 5α-androstane-3β,17β- diol. Horm Behav 53: 741-752. doi:10.1016/j.yhbeh.2007.09.012. PubMed: 18067894.
44. Fang H, Tong W, Branham WS, Moland CL, Dial SL et al. (2003) Study of 202 natural, synthetic, and environmental chemicals for binding to the androgen receptor. Chem Res Toxicol 16: 1338-1358. doi:10.1021/tx030011g. PubMed: 14565775. (Pubitemid 37315223)
45. Bear MF, Malenka RC (1994) Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 4: 389-399. doi:10.1016/0959-4388(94)90101-5. PubMed: 7919934. (Pubitemid 24194277)
46. Micevych PE, Mermelstein PG (2008) Membrane estrogen receptors acting through metabotropic glutamate receptors: an emerging mechanism of estrogen action in brain. Mol Neurobiol 38: 66-77. doi:10.1007/s12035-008-8034-z. PubMed: 18670908.
47. Pouliot A, Handa RJ, Beck SG (1996) Androgen modulates N-methyl-D-aspartate-mediated depolarization in CA1 hippocampal pyramidal cells. Synapse 23: 10-19. doi:10.1002/(SICI)1098-2396(199605)23:1. PubMed: 8723131. (Pubitemid 26138643)
48. Foy MR, Xu J, Xie X, Brinton RD, Thompson RF et al. (1999) 17β-Estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J Neurophysiol 81: 925-929. PubMed: 10036289. (Pubitemid 29264535)
49. Smith CC, McMahon LL (2006) Estrogen-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors. J Neurosci 26: 8517-8522. doi:10.1523/JNEUROSCI.5279-05.2006. PubMed: 16914677. (Pubitemid 44316180)
50. Bi F, Foy M, Thompson M, Baudry M (2000) The tyrosine kinase and miogeno-activated protein kinase pathways mediate multiple effects of estrogen in hippocampus. Proc Natl Acad Sci USA 97: 3602-3607. doi:10.1073/pnas.97.7. 3602. PubMed: 10725383. (Pubitemid 30183349)
51. Garcia-Segura LM (2008) Aromatase in the brain: not just for reproduction anymore. J Neuroendocrinol 20: 705-712. doi:10.1111/j.1365-2826.2008.01713.x. PubMed: 18601693.