Milestones on steroids and the nervous system: 10 years of basic and translational research

Journal of Neuroendocrinology

Volumn 24, Issue 1, 2012, Pages 1-15

  Panzica, G C ^a   Balthazart, J ^b   Frye, C A ^c   Garcia Segura, L M ^d   Herbison, A E ^e   Mensah Nyagan, A G ^f   McCarthy, M M ^g   Melcangi, R C ^h  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c STATE UNIVERSITY OF NEW YORK   (United States)

^d INSTITUTO CAJAL   (Spain)

^e UNIVERSITY OF OTAGO   (New Zealand)

^f UNIVERSITÉ DE STRASBOURG   (France)

^g UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^h UNIVERSITY OF MILAN   (Italy)

Author keywords

Behaviour; Brain; GnRH; Kisspeptin; Neuroprotection; Neurosteroids; Peripheral nerve; Sex difference

Indexed keywords

20ALPHA DIHYDROPROGESTERONE; 4 AMINOBUTYRIC ACID; ARGIPRESTOCIN; BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; CONJUGATED ESTROGEN PLUS MEDROXYPROGESTERONE ACETATE; DIETHYLSTILBESTROL; ENDOCRINE DISRUPTOR; ENZYME; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR BETA; ETHINYLESTRADIOL; GLUTAMIC ACID; GONADORELIN; GROWTH FACTOR; NEUROACTIVE STEROID; NEUROSTEROID; NEUROTRANSMITTER; PHYTOESTROGEN; PROGESTERONE; PROSTAGLANDIN E2; SEX HORMONE; SOMATOSTATIN RECEPTOR; STEROID; STEROID HORMONE ANTAGONIST; STEROID RECEPTOR; TETRAHYDROPROGESTERONE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UNINDEXED DRUG;

BEHAVIOR; BRAIN; BRAIN DEVELOPMENT; CELLULAR DISTRIBUTION; CLINICAL TRIAL (TOPIC); DEMENTIA; DRUG EFFICACY; DRUG EXPOSURE; DRUG MECHANISM; DRUG SYNTHESIS; DRUG TARGETING; EDITORIAL; ENZYME LOCALIZATION; GABAERGIC TRANSMISSION; GENE EXPRESSION; GENOTYPE PHENOTYPE CORRELATION; GLIA CELL; GONAD; HORMONE SYNTHESIS; HUMAN; IN SITU HYBRIDIZATION; NEGATIVE FEEDBACK; NERVE CELL; NERVE CELL LESION; NERVE CELL NETWORK; NERVE DEGENERATION; NERVOUS SYSTEM; NERVOUS TISSUE; NEUROENDOCRINE SYSTEM; NEUROPROTECTION; NEUROSTEROIDOGENESIS; NEUROTRANSMITTER RELEASE; NONHUMAN; PATHOPHYSIOLOGY; POSITIVE FEEDBACK; PRIORITY JOURNAL; REPRODUCTION; SEX DIFFERENTIATION; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION; STEROIDOGENESIS; STROKE; TELEOST; TISSUE INJURY; TRANSLATIONAL RESEARCH;

ANIMALS; BRAIN; CONGRESSES AS TOPIC; HISTORY, 21ST CENTURY; HUMANS; NEUROBIOLOGY; NEUROLOGY; NEUROTRANSMITTER AGENTS; RESEARCH; STEROIDS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84055183055     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2011.02265.x     Document Type: Editorial

References (238)

1. Panzica GC, Ottinger MA. Action of environmental estrogens on neural circuits and behavior (Special Issue). Brain Res Bull 2005; 65: 185-273.
2. McCarthy MM, Todd BJ, Amateau SK. Estradiol modulation of astrocytes and the establishment of sex differences in the brain. Ann NY Acad Sci 2003; 1007: 283-297.
3. Arnold AP, Rissman EF, De Vries GJ. Two perspectives on the origin of sex differences in the brain. Ann NY Acad Sci 2003; 1007: 176-188.
4. Balthazart J, Cornil CA, Taziaux M, Charlier TD, Baillien M, Ball GF. Rapid changes in production and behavioral action of estrogens. Neuroscience 2006; 138: 783-791.
5. Kudwa AE, Michopoulos V, Gatewood JD, Rissman EF. Roles of estrogen receptors alpha and beta in differentiation of mouse sexual behavior. Neuroscience 2006; 138: 921-928.
6. Bao AM, Meynen G, Swaab DF. The stress system in depression and neurodegeneration: focus on the human hypothalamus. Brain Res Rev 2008; 57: 531-553.
7. Todd BJ, Merhi ZO, Shu J, Etgen AM, Neal-Perry GS. Hypothalamic insulin-like growth factor-I receptors are necessary for hormone-dependent luteinizing hormone surges: implications for female reproductive aging. Endocrinology 2010; 151: 1356-1366.
8. Schlinger BA, Remage-Healey L. Neurosteroidogenesis: insights from studies of songbirds. J Neuroendocrinol 2011; 24: 16-21.
9. Henderson VW, Brinton RD. Menopause and mitochondria: windows into estrogen effects on Alzheimer's disease risk and therapy. Prog Brain Res 2010; 182: 77-96.
10. Phoenix CH, Goy RW, Gerall AA, Young WC. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 1959; 65: 369-382.
11. Arnold AP, Chen X. What does the 'four core genotypes' mouse model tell us about sex differences in the brain and other tissues? Front Neuroendocrinol 2009; 30: 1-9.
12. Budefeld T, Tobet SA, Majdic G. Steroidogenic factor 1 and the central nervous system. J Neuroendocrinol 2011; 24: 225-235.
13. Pierman S, Sica M, Allieri F, Viglietti-Panzica C, Panzica GC, Bakker J. Activational effects of estradiol and dihydrotestosterone on social recognition and the arginine-vasopressin immunoreactive system in male mice lacking a functional aromatase gene. Horm Behav 2008; 54: 98-106.
14. Plumari L, Viglietti Panzica C, Allieri F, Honda S, Harada N, Absil P, Balthazar J, Panzica GC. Changes in the arginine-vasopressin immunoreactive systems in male mice lacking a functional aromatase gene. J Neuroendocrinol 2002; 14: 971-978.
15. Bodo C. A role for the androgen receptor in the sexual differentiation of the olfactory system in mice. Brain Res Rev 2008; 57: 321-331.
16. Martini M, Di Sante G, Collado P, Pinos H, Guillamon A, Panzica GC. Androgen receptors are required for full masculinization of nitric oxide synthase system in rat limbic-hypothalamic region. Horm Behav 2008; 54: 557-564.
17. Panzica GC, Allieri F, Bo E, Collado P, Bakker J, Viglietti-Panzica C. Androgens and development of the BST parvocellular vasopressin system. Trab Inst Cajal 2009; LXXXII: 78-79.
18. Ahmed EI, Zehr JL, Schulz KM, Lorenz BH, DonCarlos LL, Sisk CL. Pubertal hormones modulate the addition of new cells to sexually dimorphic brain regions. Nat Neurosci 2008; 11: 995-997.
19. Bodo C, Kudwa AE, Rissman EF. Both estrogen receptor-alpha and -beta are required for sexual differentiation of the anteroventral periventricular area in mice. Endocrinology 2006; 147: 415-420.
20. Juntti SA, Tollkuhn J, Wu MV, Fraser EJ, Soderborg T, Tan S, Honda S, Harada N, Shah NM. The androgen receptor governs the execution, but not programming, of male sexual and territorial behaviors. Neuron 2010; 66: 260-272.
21. Ogawa S, Chester AE, Hewitt SC, Walker VR, Gustafsson JÅ, Smithies O, Korach KS, Pfaff DW. Abolition of male sexual behaviors in mice lacking estrogen receptors alpha and beta (abERKO). Proc Natl Acad Sci USA 2000; 97: 14737-14741.
22. Kelly MJ, Qiu J, Ronnekleiv OK. Estrogen modulation of G-protein-coupled receptor activation of potassium channels in the central nervous system. Ann NY Acad Sci 2003; 1007: 6-16.
23. Kelly MJ, Ronnekleiv OK. Membrane-initiated estrogen signaling in hypothalamic neurons. Mol Cell Endocrinol 2008; 290: 14-23.
24. Balthazart J, Ball GF. Is brain estradiol a hormone or a neurotransmitter? Trends Neurosci 2006; 29: 241-249.
25. Schwarz JM, Liang SL, Thompson SM, McCarthy MM. Estradiol induces hypothalamic dendritic spines by enhancing glutamate release: a mechanism for organizational sex differences. Neuron 2008; 58: 584-598.
26. Kudwa AE, Bodo C, Gustafsson JA, Rissman EF. A previously uncharacterized role for estrogen receptor beta: defeminization of male brain and behavior. Proc Natl Acad Sci USA 2005; 102: 4608-4612.
27. Handa RJ, Ogawa S, Wang JM, Herbison AE. Roles for estrogen receptor beta in adult brain function. J Neuroendocrinol 2011; 24: 160-173.
28. Amateau SK, McCarthy MM. Induction of PGE2 by estradiol mediates developmental masculinization of sex behavior. Nat Neurosci 2004; 7: 643-650.
29. Todd BJ, Schwarz JM, McCarthy MM. Prostaglandin-E2: a point of divergence in estradiol-mediated sexual differentiation. Horm Behav 2005; 48: 512-521.
30. Bakker J, Honda S, Harada N, Balthazart J. The aromatase knockout (ArKO) mouse provides new evidence that estrogens are required for the development of the female brain. Ann NY Acad Sci 2003; 1007: 251-262.
31. Bakker J, Baum MJ. Role for estradiol in female-typical brain and behavioral sexual differentiation. Front Neuroendocrinol 2008; 29: 1-16.
32. Matsuda KI, Mori H, Nugent BM, Pfaff DW, McCarthy MM, Kawata M. Histone deacetylation during brain development is essential for permanent masculinization of sexual behavior. Endocrinology 2011; 152: 2760-2767.
33. Tsai HW, Grant PA, Rissman EF. Sex differences in histone modifications in the neonatal mouse brain. Epigenetics 2009; 4: 47-53.
34. McCarthy MM, Auger AP, Bale TL, De Vries GJ, Dunn GA, Forger NG, Murray EK, Nugent BM, Schwarz JM, Wilson ME. The epigenetics of sex differences in the brain. J Neurosci 2009; 29: 12815-12823.
35. Nugent BM, Schwarz JM, McCarthy MM. Hormonally mediated epigenetic changes to steroid receptors in the developing brain: implications for sexual differentiation. Horm Behav 2011; 59: 338-344.
36. Schwarz JM, Nugent BM, McCarthy MM. Developmental and hormone-induced epigenetic changes to estrogen and progesterone receptor genes in brain are dynamic across the life span. Endocrinology 2010; 151: 4871-4881.
37. De Vries GJ. Minireview: sex differences in adult and developing brains: compensation, compensation, compensation. Endocrinology 2004; 145: 1063-1068.
38. Döhler KD, Hines M, Coquelin A, Davis FC, Shryne JE, Gorski RA. Pre- and postnatal influence of diethylstilboestrol on differentiation of the sexually dimorphic nucleus in the preoptic area of the female rat brain. Neuroendocrinol Lett 1982; 4: 361-365.
39. Bogic L, Gerlach JL, McEwen BS. The ontogeny of sex differences in estrogen-induced progesterone receptors in rat brain. Endocrinology 1988; 122: 2735-2741.
40. Colborn T, vom Saal FS, Soto AM. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect 1993; 101: 378-384.
41. Bern HA, Blair P, Brasseur S, Colborn T, Cunha GR, Davis W, Dohler KD, Fox G, Fry M, Gray E, Green R, Hines M, Kubiak TJ, McLachlan J, Myers JP, Peterson RE, Reijnders PJH, Soto AM, Van Der Kraak G, vom Saal FS, Whitten P. Statement from the work session on chemically-induced alterations in sexual development: the wildlife/human connection. In: Colborn T, Clement C, eds. Chemically-Induced Alterations in Sexual and Functional Development: The Wildlife/Human Connection. Princeton, NJ: Princeton Scientific Publishing Co., Inc, 1992: 1-8.
42. Lephart ED, Lund TD, Horvath TL. Brain androgen and progesterone metabolizing enzymes: biosynthesis, distribution and function. Brain Res Rev 2001; 37: 25-37.
43. Lephart ED, Adlercreutz H, Lund TD. Dietary soy phytoestrogen effects on brain structure and aromatase in Long-Evans rats. Neuroreport 2001; 12: 3451-3455.
44. Lephart ED, West TW, Weber KS, Rhees RW, Setchell KDR, Adlercreutz H, Lund TD. Neurobehavioral effects of dietary soy phytoestrogens. Neurotoxicol Teratol 2002; 24: 5-16.
45. McLachlan JA, Guillette LJ Jr, Iguchi T, Toscano WA Jr. Environmental Hormones: The Scientific Basis of Endocrine Disruption. New York, NY: NYAS, 2001.
46. Bauer R, Colborn T, Palanza P, Parmigiani S, Vom Saal FS. Endocrine disruptors. Environ Health Perspect (Special Issue) 2002; 110(Suppl. 3): 335-449.
47. Alò R, Facciolo RM, Madeo M, Giusi G, Carelli A, Canonaco M. Effects of the xenoestrogen bisphenol A in diencephalic regions of the teleost fish Coris julis occur preferentially via distinct somatostatin receptor subtypes. Brain Res Bull 2005; 65: 267-273.
48. Viglietti-Panzica C, Montoncello B, Mura E, Pessatti M, Panzica GC. Organizational effects of diethylstilbestrol on brain vasotocin and sexual behavior in male quail. Brain Res Bull 2005; 65: 225-233.
49. Panzica GC, Mura E, Pessatti M, Viglietti Panzica C. Early embryonic administration of xenoestrogens alters vasotocin system and male sexual behavior of the Japanese quail. Domest Anim Endocrinol 2005; 29: 436-445.
50. Ottinger MA, Wu JM, Hazelton JL, Abdelnabi MA, Thompson N, Quinn ML, Donoghue D, Schenck F, Ruscio M, Beavers J, Jaber M. Assessing the consequences of the pesticide methoxychlor: neuroendocrine and behavioral measures as indicators of biological impact of an estrogenic environmental chemical. Brain Res Bull 2005, 65: 199-210.
51. Halldin K, Axelsson J, Brunstrom B. Effects of endocrine modulators on sexual differentiation and reproductive function in male Japanese quail. Brain Res Bull 2005; 65: 211-218.
52. Laviola G, Gioiosa L, Adriani W, Palanza P. d-Amphetamine-related reinforcing effects are reduced in mice exposed prenatally to estrogenic endocrine disruptors. Brain Res Bull 2005; 65: 235-240.
53. Della Seta D, Minder I, Dessi-Fulgheri F, Farabollini F. Bisphenol-A exposure during pregnancy and lactation affects maternal behavior in rats. Brain Res Bull 2005; 65: 255-260.
54. Porrini S, Belloni V, Seta DD, Farabollini F, Giannelli G, Dessi-Fulgheri F. Early exposure to a low dose of bisphenol A affects socio-sexual behavior of juvenile female rats. Brain Res Bull 2005; 65: 261-266.
55. Razzoli M, Valsecchi P, Palanza P. Chronic exposure to low doses bisphenol A interferes with pair-bonding and exploration in female Mongolian gerbils. Brain Res Bull 2005; 65: 249-254.
56. Mussi P, Ciana P, Raviscioni M, Villa R, Regondi S, Agradi E, Maggi A, Lorenzo DD. Activation of brain estrogen receptors in mice lactating from mothers exposed to DDT. Brain Res Bull 2005; 65: 241-247.
57. Bu L-H, Lephart ED. Effects of dietary phytoestrogens on core body temperature during the estrous cycle and pregnancy. Brain Res Bull 2005; 65: 219-223.
58. Lephart ED, Setchell KDR, Lund TD. Phytoestrogens: hormonal action and brain plasticity. Brain Res Bull 2005; 65: 193-198.
59. Mukai H, Takata N, Ishii HT, Tanabe N, Hojo Y, Furukawa A, Kimoto T, Kawato S. Hippocampal synthesis of estrogens and androgens which are paracrine modulators of synaptic plasticity: synaptocrinology. Neuroscience 2006; 138: 757-764.
60. Gu Q, Korach KS, Moss RL. Rapid action of 17beta-estradiol on kainate-induced currents in hippocampal neurons lacking intracellular estrogen receptors. Endocrinology 1999; 140: 660-666.
61. Shibuya K, Takata N, Hojo Y, Furukawa A, Yasumatsu N, Kimoto T, Enami T, Suzuki K, Tanabe N, Ishii H, Mukai H, Takahashi T, Hattori TA, Kawato S. Hippocampal cytochrome P450s synthesize brain neurosteroids which are paracrine neuromodulators of synaptic signal transduction. Biochim Biophys Acta 2003; 1619: 301-316.
62. Kawato S. Endocrine disrupters as disrupters of brain function: a neurosteroid viewpoint. Environ Sci 2004; 11: 1-14.
63. Ogiue-Ikeda M, Tanabe N, Mukai H, Hojo Y, Murakami G, Tsurugizawa T, Takata N, Kimoto T, Kawato S. Rapid modulation of synaptic plasticity by estrogens as well as endocrine disrupters in hippocampal neurons. Brain Res Rev 2008; 57: 363-375.
64. Di Lorenzo D, Rando G, Ciana P, Maggi A. Molecular imaging, an innovative methodology for whole-body profiling of endocrine disrupter action. Toxicol Sci 2008; 106: 304-311.
65. Patisaul HB, Polston EK. Influence of endocrine active compounds on the developing rodent brain. Brain Res Rev 2008; 57: 352-362.
66. Ottinger MA, Lavoie E, Thompson N, Barton A, Whitehouse K, Abdelnabi M, Quinn MJ Jr, Panzica GC, Viglietti-Panzica C. Neuroendocrine and behavioral effects of embryonic exposure to endocrine disrupting chemicals in birds. Brain Res Rev 2008; 57: 376-385.
67. Tetel MJ. Modulation of steroid action in the central and peripheral nervous systems by nuclear receptor coactivators. Psychoneuroendocrinology 2009; 34(Suppl. 2): 9-19.
68. Palanza P, Gioiosa L, vom Saal FS, Parmigiani S. Effects of developmental exposure to bisphenol A on brain and behavior in mice. Environ Res 2008; 108: 150-157.
69. Frye CA, Bo E, Calamandrei G, Calza L, Dessi-Fulgheri F, Fernandez M, Fusani L, Kah O, Kajta M, Le Page Y, Patisaul HB, Venerosi A, Wojtowicz AK, Panzica GC. Endocrine disrupters: a review of some sources, effects, and mechanisms of actions on behavior and neuroendocrine systems. J Neuroendocrinol 2011; 24: 144-159.
70. Panzica GC, Viglietti-Panzica C, Mura E, Quinn MJ Jr, Palanza P, Ottinger MA. Effects of xenoestrogens on the differentiation of behaviorally relevant neural circuits. Front Neuroendocrinol 2007; 28: 179-200.
71. Panzica GC, Mura E, Miceli D, Martini M, Gotti S, Viglietti Panzica C. Effects of xenoestrogens on the differentiation of behaviorally-relevant neural circuits in higher vertebrates. In: Vaudry H, Rubois E, Coast GM, Vallarino M, eds. Trends in Comparative Endocrinology and Neurobiology. New York, NY: New York Academy of Sciences, 2009: 271-278.
72. Panzica GC, Bo E, Martini MA, Miceli D, Mura E, Viglietti-Panzica C, Gotti S. Neuropeptides and enzymes are targets for the action of endocrine disrupting chemicals in the vertebrate brain. J Toxicol Environ Health B Crit Rev 2011; 14: 449-472.
73. Bateman HL, Patisaul HB. Disrupted female reproductive physiology following neonatal exposure to phytoestrogens or estrogen specific ligands is associated with decreased GnRH activation and kisspeptin fiber density in the hypothalamus. Neurotoxicology 2008; 29: 988-997.
74. Bellingham M, Fowler PA, Amezaga MR, Rhind SM, Cotinot C, Mandon-Pepin B, Sharpe RM, Evans NP. Exposure to a complex cocktail of environmental endocrine-disrupting compounds disturbs the kisspeptin/GPR54 system in ovine hypothalamus and pituitary gland. Environ Health Perspect 2009; 117: 1556-1562.
75. Dickerson SM, Cunningham SL, Patisaul HB, Woller MJ, Gore AC. Endocrine disruption of brain sexual differentiation by developmental PCB exposure. Endocrinology 2011; 152: 581-594.
76. Miceli D, Bo E, Palanza P, Franceschini I, Panzica GC. Effects of bisphenol-A (BPA) in the hypothalamic nuclei that control puberty, reproduction and sexual behavior in a murine model. Trab Inst Cajal 2011; 83: 194-195.
77. Patisaul HB, Todd KL, Mickens JA, Adewale HB. Impact of neonatal exposure to the ERalpha agonist PPT, bisphenol-A or phytoestrogens on hypothalamic kisspeptin fiber density in male and female rats. Neurotoxicology 2009; 30: 350-357.
78. Mura E, Barale C, Quinn MJ Jr, Panzica GC, Ottinger MA, Viglietti Panzica C. Organizational effects of DDE on brain vasotocin system in male Japanese quail. Neurotoxicology 2009; 30: 479-484.
79. Viglietti-Panzica C, Mura E, Panzica GC. Effects of early embryonic exposure to genistein on male copulatory behavior and vasotocin system of Japanese quail. Horm Behav 2007; 51: 355-363.
80. Cheshenko K, Pakdel F, Segner H, Kah O, Eggen RI. Interference of endocrine disrupting chemicals with aromatase CYP19 expression or activity, and consequences for reproduction of teleost fish. Gen Comp Endocrinol 2008; 155: 31-62.
81. Le Page Y, Scholze M, Kah O, Pakdel F. Assessment of xenoestrogens using three distinct estrogen receptors and the zebrafish brain aromatase gene in a highly responsive glial cell system. Environ Health Perspect 2006; 114: 752-758.
82. Le Page Y, Vosges M, Servili A, Brion F, Kah O. Neuroendocrine effects of endocrine disruptors in teleost fish. J Toxicol Environ Health B Crit Rev 2011; 14: 370-386.
83. Curras-Collazo MC. Nitric oxide signaling as a common target of organohalogens and other neuroendocrine disruptors. J Toxicol Environ Health B Crit Rev 2011; 14: 495-536.
84. Martini M, Miceli D, Gotti S, Viglietti-Panzica C, Fissore E, Palanza P, Panzica GC. Effects of perinatal administration of bisphenol A on the neuronal nitric oxide synthase expressing system in the hypothalamus and limbic system of CD1 mice. J Neuroendocrinol 2010; 22: 1004-1012.
85. Vom Saal FS. Bisphenol a eliminates brain and behavior sex dimorphisms in mice: how low can you go? Endocrinology 2006; 147: 3679-3680.
86. Tena-Sempere M. Kisspeptin/GPR54 system as potential target for endocrine disruption of reproductive development and function. Int J Androl 2010; 33: 360-368.
87. Decherf S, Demeneix BA. The obesogen hypothesis: a shift of focus from the periphery to the hypothalamus. J Toxicol Environ Health B Crit Rev 2011; 14: 423-448.
88. MacLusky NJ, Hajszán T, Leranth C. The environmental estrogen bisphenol-A inhibits estradiol-induced hippocampal synaptogenesis. Environ Health Perspect 2005; 113: 675-679.
89. MacLusky NJ, Hajszan T, Prange-Kiel J, Leranth C. Androgen modulation of hippocampal synaptic plasticity. Neuroscience 2006; 138: 957-965.
90. Hajszan T, Leranth C. Bisphenol A interferes with synaptic remodeling. Front Neuroendocrinol 2010; 31: 519-530.
91. Xu XH, Zhang J, Wang YM, Ye YP, Luo QQ. Perinatal exposure to bisphenol-A impairs learning-memory by concomitant down-regulation of N-methyl-D-aspartate receptors of hippocampus in male offspring mice. Horm Behav 2010; 58: 326-333.
92. Baulieu EE, Robel P, Schumacher M. Neurosteroids. A New Regulatory Function in the Nervous System. Totowa, NJ: Humana Press, 1999.
93. Corpechot C, Robel P, Axelson M, Sjovall J, Baulieu EE. Characterization and measurement of dehydroepiandrosterone sulfate in rat brain. Proc Natl Acad Sci USA 1981; 78: 4704-4707.
94. Corpechot C, Synguelakis M, Talha S, Axelson M, Sjovall J, Vihko R, Baulieu EE, Robel P. Pregnenolone and its sulfate ester in the rat brain. Brain Res 1983; 270: 119-125.
95. Compagnone NA, Mellon SH. Neurosteroids: biosynthesis and function of these novel neuromodulators. Front Neuroendocrinol 2000; 21: 1-56.
96. Mensah-Nyagan AG, Do-Rego JL, Beaujean D, Luu-The V, Pelletier G, Vaudry H. Neurosteroids: expression of steroidogenic enzymes and regulation of steroid biosynthesis in the central nervous system. Pharmacol Rev 1999; 51: 63-81.
97. Schumacher M, Weill-Engerer S, Liere P, Robert F, Franklin RJ, Garcia-Segura LM, Lambert JJ, Mayo W, Melcangi RC, Parducz A, Suter U, Carelli C, Baulieu EE, Akwa Y. Steroid hormones and neurosteroids in normal and pathological aging of the nervous system. Prog Neurobiol 2003; 71: 3-29.
98. Mellon SH, Griffin LD, Compagnone NA. Biosynthesis and action of neurosteroids. Brain Res Rev 2001; 37: 3-12.
99. Mensah-Nyagan AG, Beaujean D, Luu-The V, Pelletier G, Vaudry H. Anatomical and biochemical evidence for the synthesis of unconjugated and sulfated neurosteroids in amphibians. Brain Res Rev 2001; 37: 13-24.
100. Stoffel-Wagner B. Neurosteroid biosynthesis in the human brain and its clinical implications. Ann NY Acad Sci 2003; 1007: 64-78.
101. Guarneri P, Cascio C, Russo D, D'Agostino S, Drago G, Galizzi G, De Leo G, Piccoli F, Guarneri M, Guarneri R. Neurosteroids in the retina: neurodegenerative and neuroprotective agents in retinal degeneration. Ann NY Acad Sci 2003; 1007: 117-128.
102. Melcangi RC, Mensah-Nyagan AG. Neuroprotective effects of neuroactive steroids in the spinal cord and peripheral nerves. J Mol Neurosci 2006; 28: 1-102.
103. Lavaque E, Sierra A, Azcoitia I, Garcia-Segura LM. Steroidogenic acute regulatory protein in the brain. Neuroscience 2006; 138: 741-747.
104. Papadopoulos V, Lecanu L, Brown RC, Han Z, Yao ZX. Peripheral-type benzodiazepine receptor in neurosteroid biosynthesis, neuropathology and neurological disorders. Neuroscience 2006; 138: 749-756.
105. Melcangi RC, Mensah-Nyagan AG. Neurosteroids: Measurements and pathophysiological relevance. Neurochem Int 2008; 52: 503-620.
106. Melcangi RC, Garcia-Segura LM, Panzica GC. Neuroactive steroids: focus on human brain. Neuroscience 2011; 191: 1-158.
107. Melcangi RC, Garcia-Segura LM, Mensah-Nyagan AG. Neuroactive steroids: state of the art and new perspectives. Cell Mol Life Sci 2008; 65: 777-797.
108. Schaeffer V, Meyer L, Patte-Mensah C, Mensah-Nyagan AG. Progress in dorsal root ganglion neurosteroidogenic activity: basic evidence and pathophysiological correlation. Prog Neurobiol 2010; 92: 33-41.
109. Zhu Y, Rice CD, Pang Y, Pace M, Thomas P. Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes. Proc Natl Acad Sci USA 2003; 100: 2231-2236.
110. Zhu Y, Bond J, Thomas P. Identification, classification, and partial characterization of genes in humans and other vertebrates homologous to a fish membrane progestin receptor. Proc Natl Acad Sci USA 2003; 100: 2237-2242.
111. Belelli D, Lambert JJ. Neurosteroids: endogenous regulators of the GABA(A) receptor. Nat Rev Neurosci 2005; 6: 565-575.
112. Hosie AM, Wilkins ME, da Silva HM, Smart TG. Endogenous neurosteroids regulate GABAA receptors through two discrete transmembrane sites. Nature 2006; 444: 486-489.
113. Majewska MD. Neurosteroids: endogenous bimodal modulators of the GABAA receptor. Mechanism of action and physiological significance. Prog Neurobiol 1992; 38: 379-395.
114. Pathirathna S, Brimelow BC, Jagodic MM, Krishnan K, Jiang X, Zorumski CF, Mennerick S, Covey DF, Todorovic SM, Jevtovic-Todorovic V. New evidence that both T-type calcium channels and GABAA channels are responsible for the potent peripheral analgesic effects of 5alpha-reduced neuroactive steroids. Pain 2005; 114: 429-443.
115. Bowlby MR. Pregnenolone sulfate potentiation of N-methyl-D-aspartate receptor channels in hippocampal neurons. Mol Pharmacol 1993; 43: 813-819.
116. Wu FS, Gibbs TT, Farb DH. Pregnenolone sulfate: a positive allosteric modulator at the N-methyl-D-aspartate receptor. Mol Pharmacol 1991; 40: 333-336.
117. De Roo M, Rodeau JL, Schlichter R. Dehydroepiandrosterone potentiates native ionotropic ATP receptors containing the P2X2 subunit in rat sensory neurones. J Physiol 2003; 552: 59-71.
118. Maurice T, Gregoire C, Espallergues J. Neuro(active)steroids actions at the neuromodulatory sigma1 (sigma1) receptor: biochemical and physiological evidences, consequences in neuroprotection. Pharmacol Biochem Behav 2006; 84: 581-597.
119. 3H]norepinephrine release evoked by N-methyl-D-aspartate in the rat hippocampus. Proc Natl Acad Sci USA 1995; 92: 3774-3778.
120. Gore AC. Gonadotropin-releasing hormone neurons, NMDA receptors, and their regulation by steroid hormones across the reproductive life cycle. Brain Res Rev 2001; 37: 235-248.
121. Melcangi RC, Cavarretta I, Magnaghi V, Martini L, Galbiati M. Interactions between growth factors and steroids in the control of LHRH-secreting neurons. Brain Res Rev 2001; 37: 223-234.
122. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 2003; 100: 10972-10976.
123. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS Jr, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, Zahn D, Dixon J, Kaiser UB, Slaugenhaupt SA, Gusella JF, O'Rahilly S, Carlton MB, Crowley WF Jr., Aparicio SA, Colledge WH. The GPR54 gene as a regulator of puberty. N Engl J Med 2003; 349: 1614-1627.
124. Herbison AE. Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: the case for the rostral periventricular area of the third ventricle (RP3V). Brain Res Rev 2008; 57: 277-287.
125. Smith JT. Kisspeptin signalling in the brain: steroid regulation in the rodent and ewe. Brain Res Rev 2008; 57: 288-298.
126. Garcia-Galiano D, Pinilla L, Tena-Sempere M. Sex steroids and the control of the kiss1 system: developmental roles and major regulatory actions. J Neuroendocrinol 2011; 24: 22-34.
127. El-Etr M, Akwa Y, Baulieu EE, Schumacher M. The neuroactive steroid pregnenolone sulfate stimulates the release of gonadotropin-releasing hormone from GT1-7 hypothalamic neurons, through N-methyl-D-aspartate receptors. Endocrinology 2006; 147: 2737-2743.
128. Sim JA, Skynner MJ, Herbison AE. Direct regulation of postnatal GnRH neurons by the progesterone derivative allopregnanolone in the mouse. Endocrinology 2001; 142: 4448-4453.
129. Abraham IM, Han SK, Todman MG, Korach KS, Herbison AE. Estrogen receptor beta mediates rapid estrogen actions on gonadotropin-releasing hormone neurons in vivo. J Neurosci 2003; 23: 5771-5777.
130. Romano N, Lee K, Abraham IM, Jasoni CL, Herbison AE. Nonclassical estrogen modulation of presynaptic GABA terminals modulates calcium dynamics in gonadotropin-releasing hormone neurons. Endocrinology 2008; 149: 5335-5344.
131. Moenter SM, Chu Z. Rapid non-genomic effects of oestradiol on GnRH neurons. J Neuroendocrinol 2011; 24: 117-121.
132. Chu Z, Andrade J, Shupnik MA, Moenter SM. Differential regulation of gonadotropin-releasing hormone neuron activity and membrane properties by acutely applied estradiol: dependence on dose and estrogen receptor subtype. J Neurosci 2009; 29: 5616-5627.
133. Oberlander JG, Porter DM, Penatti CA, Henderson LP. Anabolic androgenic steroid abuse: multiple mechanisms of regulation of gabaergic synapses in neuroendocrine control regions of the rodent forebrain. J Neuroendocrinol 2011; 24: 202-214.
134. Penatti CA, Davis MC, Porter DM, Henderson LP. Altered GABAA receptor-mediated synaptic transmission disrupts the firing of gonadotropin-releasing hormone neurons in male mice under conditions that mimic steroid abuse. J Neurosci 2010; 30: 6497-6506.
135. Herbison AE. Rapid actions of oestrogen on gonadotropin-releasing hormone neurons; from fantasy to physiology? J Physiol 2009; 587: 5025-5030.
136. Galbiati M, Saredi S, Melcangi RC. Steroid hormones and growth factors act in an integrated manner at the levels of hypothalamic astrocytes: a role in the neuroendocrine control of reproduction. Ann NY Acad Sci 2003; 1007: 162-168.
137. Etgen AM. Ovarian steroid and growth factor regulation of female reproductive function involves modification of hypothalamic alpha 1-adrenoceptor signaling. Ann NY Acad Sci 2003; 1007: 153-161.
138. Micevych P, Soma KK, Sinchak K. Neuroprogesterone: key to estrogen positive feedback? Brain Res Rev 2008; 57: 470-480.
139. Thanky NR, Slater R, Herbison AE. Sex differences in estrogen-dependent transcription of gonadotropin-releasing hormone (GnRH) gene revealed in GnRH transgenic mice. Endocrinology 2003; 144: 3351-3358.
140. Moenter SM, Defazio RA, Straume M, Nunemaker CS. Steroid regulation of GnRH neurons. Ann NY Acad Sci 2003; 1007: 143-152.
141. Ronnekleiv OK, Bosch MA, Zhang C. Regulation of endogenous conductances in GnRH neurons by estrogens. Brain Res 2010; 1364: 25-34.
142. Ronnekleiv OK, Bosch MA, Zhang C. 17beta-estradiol regulation of GnRH neuronal excitability. J Neuroendocrinol 2011; 24: 122-130.
143. Matagne V, Lebrethon MC, Gerard A, Bourguignon JP. In vitro paradigms for the study of GnRH neuron function and estrogen effects. Ann NY Acad Sci 2003; 1007: 129-142.
144. Roa J, Vigo E, Castellano JM, Gaytan F, Navarro VM, Aguilar E, Dijcks FA, Ederveen AG, Pinilla L, van Noort PI, Tena-Sempere M. Opposite roles of estrogen receptor (ER)-alpha and ERbeta in the modulation of luteinizing hormone responses to kisspeptin in the female rat: implications for the generation of the preovulatory surge. Endocrinology 2008; 149: 1627-1637.
145. Wintermantel TM, Campbell RE, Porteous R, Bock D, Grone HJ, Todman MG, Korach KS, Greiner E, Perez CA, Schutz G, Herbison AE. Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 2006; 52: 271-280.
146. Clarkson J, Herbison AE. Dual phenotype kisspeptin-dopamine neurones of the rostral periventricular area of the third ventricle project to gonadotrophin-releasing hormone neurones. J Neuroendocrinol 2011; 23: 293-301.
147. Khan AR, Kauffman AS. The role of kisspeptin and RFRP-3 neurons in the circadian-timed preovulatory luteinizing hormone surge. J Neuroendocrinol 2011; 24: 131-143.
148. Jensen EV, Jacobson HI, Walf AA, Frye CA. Estrogen action: a historic perspective on the implications of considering alternative approaches. Physiol Behav 2010; 99: 151-162.
149. Prange-Kiel J, Rune GM. Direct and indirect effects of estrogen on rat hippocampus. Neuroscience 2006; 138: 765-772.
150. Weiser MJ, Foradori CD, Handa RJ. Estrogen receptor beta in the brain: from form to function. Brain Res Rev 2008; 57: 309-320.
151. Blaustein JD. Progestin receptors: neuronal integrators of hormonal and environmental stimulation. Ann NY Acad Sci 2003; 1007: 238-250.
152. Guerriero G, Ciarcia G. Progesterone receptor: some viewpoints on hypothalamic seasonal fluctuations in a lower vertebrate. Brain Res Rev 2001; 37: 172-177.
153. Mani SK. Signaling mechanisms in progesterone-neurotransmitter interactions. Neuroscience 2006; 138: 773-781.
154. Adkins Regan EK, Mansukhani V, Thompson R, Yang S. Organizational action of sex hormones on sexual partner preference. Brain Res Bull 1997; 44: 497-502.
155. DonCarlos LL, Sarkey S, Lorenz B, Azcoitia I, Garcia-Ovejero D, Huppenbauer C, Garcia-Segura LM. Novel cellular phenotypes and subcellular sites for androgen action in the forebrain. Neuroscience 2006; 138: 801-807.
156. Gahr M, Metzdorf R. Distribution and dynamics in the expression of androgen and estrogen receptors in vocal control systems of songbirds. Brain Res Bull 1997; 44: 509-517.
157. Guillamon A, Segovia S. Sex differences in the vomeronasal system. Brain Res Bull 1997; 44: 377-382.
158. Walf AA. Oestrogen receptor beta is involved in the actions of oestrogens in the brain for affective behaviour, but not trophic effects in peripheral tissues. J Neuroendocrinol 2010; 22: 141-151.
159. Charlier TD. Importance of steroid receptor coactivators in the modulation of steroid action on brain and behavior. Psychoneuroendocrinology 2009; 34(Suppl. 1): 520-529.
160. Auger AP, Jessen HM. Corepressors, nuclear receptors, and epigenetic factors on DNA: a tail of repression. Psychoneuroendocrinology 2009; 34(Suppl. 1): 39-47.
161. Belcher SM. Rapid signaling mechanisms of estrogens in the developing cerebellum. Brain Res Rev 2008; 57: 481-492.
162. Wandosell F, Varea O, Arevalo MA, Garcia-Segura LM. Oestradiol regulates beta-catenin-mediated transcription in neurones. J Neuroendocrinol 2011; 24: 191-194.
163. Guennoun R, Meffre D, Labombarda F, Gonzalez SL, Deniselle MC, Stein DG, De Nicola AF, Schumacher M. The membrane-associated progesterone-binding protein 25-Dx: expression, cellular localization and up-regulation after brain and spinal cord injuries. Brain Res Rev 2008; 57: 493-505.
164. Mhyre AJ, Dorsa DM. Estrogen activates rapid signaling in the brain: role of estrogen receptor alpha and estrogen receptor beta in neurons and glia. Neuroscience 2006; 138: 851-858.
165. Ramirez VD, Kipp JL, Joe I. Estradiol, in the CNS, targets several physiologically relevant membrane-associated proteins. Brain Res Rev 2001; 37: 141-152.
166. Akk G, Covey DF, Evers AS, Steinbach JH, Zorumski CF, Mennerick S. The influence of the membrane on neurosteroid actions at GABA(A) receptors. Psychoneuroendocrinology 2009; 34(Suppl. 1): 59-66.
167. Covey DF, Evers AS, Mennerick S, Zorumski CF, Purdy RH. Recent developments in structure-activity relationships for steroid modulators of GABA(A) receptors. Brain Res Rev 2001; 37: 91-97.
168. Follesa P, Concas A, Porcu P, Sanna E, Serra M, Mostallino MC, Purdy RH, Biggio G. Role of allopregnanolone in regulation of GABA(A) receptor plasticity during long-term exposure to and withdrawal from progesterone. Brain Res Rev 2001; 37: 81-90.
169. Lambert JJ, Belelli D, Harney SC, Peters JA, Frenguelli BG. Modulation of native and recombinant GABA(A) receptors by endogenous and synthetic neuroactive steroids. Brain Res Rev 2001; 37: 68-80.
170. Lambert JJ, Cooper MA, Simmons RD, Weir CJ, Belelli D. Neurosteroids: endogenous allosteric modulators of GABA(A) receptors. Psychoneuroendocrinology 2009; 34(Suppl. 1): 48-58.
171. Maguire J, Mody I. Steroid hormone fluctuations and GABA(A)R plasticity. Psychoneuroendocrinology 2009; 34(Suppl. 1): 84-90.
172. McCarthy MM, Davis AM, Mong JA. Excitatory neurotransmission and sexual differentiation of the brain. Brain Res Bull 1997; 44: 487-495.
173. Smith CC, Vedder LC, McMahon LL. Estradiol and the relationship between dendritic spines, NR2B containing NMDA receptors, and the magnitude of long-term potentiation at hippocampal CA3-CA1 synapses. Psychoneuroendocrinology 2009; 34(Suppl. 1): 130-142.
174. Cyr M, Ghribi O, Thibault C, Morissette M, Landry M, Di Paolo T. Ovarian steroids and selective estrogen receptor modulators activity on rat brain NMDA and AMPA receptors. Brain Res Rev 2001; 37: 153-161.
175. Hull EM, Du J, Lorrain DS, Matuszewich L. Testosterone, preoptic dopamine, and copulation in male rats. Brain Res Bull 1997; 44: 327-333.
176. Etgen AM, Gonzalez-Flores O, Todd BJ. The role of insulin-like growth factor-I and growth factor-associated signal transduction pathways in estradiol and progesterone facilitation of female reproductive behaviors. Front Neuroendocrinol 2006; 27: 363-375.
177. Herbison AE. Estrogen regulation of GABA transmission in rat preoptic area. Brain Res Bull 1997; 44: 321-326.
178. Micevych PE, Eckersell CB, Brecha N, Holland KL. Estrogen modulation of opioid and cholecystokinin systems in the limbic-hypothalamic circuit. Brain Res Bull 1997; 44: 335-343.
179. Maurice T, Urani A, Phan VL, Romieu P. The interaction between neuroactive steroids and the sigma(1) receptor function: behavioral consequences and therapeutic opportunities. Brain Res Rev 2001; 37: 116-132.
180. Dewing P, Christensen A, Bondar G, Micevych P. Protein kinase C signaling in the hypothalamic arcuate nucleus regulates sexual receptivity in female rats. Endocrinology 2008; 149: 5934-5942.
181. Frye CA. Neurosteroids' effects and mechanisms for social, cognitive, emotional, and physical functions. Psychoneuroendocrinology 2009; 34(Suppl. 1): 143-161.
182. Simpkins JW, Dykens JA. Mitochondrial mechanisms of estrogen neuroprotection. Brain Res Rev 2008; 57: 421-430.
183. Micevych PE, Mermelstein PG. Membrane estrogen receptors acting through metabotropic glutamate receptors: an emerging mechanism of estrogen action in brain. Mol Neurobiol 2008; 38: 66-77.
184. Meitzen J, Mermelstein PG. Estrogen receptors stimulate brain region specific metabotropic glutamate receptors to rapidly initiate signal transduction pathways. J Chem Neuroanat 2011; 42: 236-241.
185. Rapp SR, Espeland MA, Shumaker SA, Henderson VW, Brunner RL, Manson JE, Gass ML, Stefanick ML, Lane DS, Hays J, Johnson KC, Coker LH, Dailey M, Bowen D. Effect of estrogen plus progestin on global cognitive function in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 2003; 289: 2663-2672.
186. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA 2002; 288: 321-333.
187. Maki PM. Hormone therapy and cognitive function: is there a critical period for benefit? Neuroscience 2006; 138: 1027-1030.
188. Brann D, Raz L, Wang R, Vadlamudi R, Zhang Q. Oestrogen signaling and neuroprotection in cerebral ischemia. J Neuroendocrinol 2011; 24: 34-47.
189. Azcoitia I, Arevalo MA, De Nicola AF, Garcia-Segura LM. Neuroprotective actions of estradiol revisited. Trends Endocrinol Metab 2011; 24: 467-473.
190. Ciriza I, Carrero P, Frye CA, Garcia-Segura LM. Reduced metabolites mediate neuroprotective effects of progesterone in the adult rat hippocampus. The synthetic progestin medroxyprogesterone acetate (Provera) is not neuroprotective. J Neurobiol 2006; 66: 916-928.
191. De Nicola AF, Labombarda F, Deniselle MC, Gonzalez SL, Garay L, Meyer M, Gargiulo G, Guennoun R, Schumacher M. Progesterone neuroprotection in traumatic CNS injury and motoneuron degeneration. Front Neuroendocrinol 2009; 30: 173-187.
192. Sayeed I, Stein DG. Progesterone as a neuroprotective factor in traumatic and ischemic brain injury. Prog Brain Res 2009; 175: 219-237.
193. Ibanez C, Shields SA, El-Etr M, Leonelli E, Magnaghi V, Li WW, Sim FJ, Baulieu EE, Melcangi RC, Schumacher M, Franklin RJ. Steroids and the reversal of age-associated changes in myelination and remyelination. Prog Neurobiol 2003; 71: 49-56.
194. Schumacher M, Sitruk-Ware R, De Nicola AF. Progesterone and progestins: neuroprotection and myelin repair. Curr Opin Pharmacol 2008; 8: 740-746.
195. Melcangi RC, Azcoitia I, Ballabio M, Cavarretta I, Gonzalez LC, Leonelli E, Magnaghi V, Veiga S, Garcia-Segura LM. Neuroactive steroids influence peripheral myelination: a promising opportunity for preventing or treating age-dependent dysfunctions of peripheral nerves. Prog Neurobiol 2003; 71: 57-66.
196. Melcangi RC, Cavarretta IT, Ballabio M, Leonelli E, Schenone A, Azcoitia I, Miguel Garcia-Segura L, Magnaghi V. Peripheral nerves: a target for the action of neuroactive steroids. Brain Res Brain Res Rev 2005; 48: 328-338.
197. Roglio I, Bianchi R, Gotti S, Scurati S, Giatti S, Pesaresi M, Caruso D, Panzica GC, Melcangi RC. Neuroprotective effects of dihydroprogesterone and progesterone in an experimental model of nerve crush injury. Neuroscience 2008; 155: 673-685.
198. Garay L, Deniselle MC, Lima A, Roig P, De Nicola AF. Effects of progesterone in the spinal cord of a mouse model of multiple sclerosis. J Steroid Biochem Mol Biol 2007; 107: 228-237.
199. Garay L, Deniselle MC, Meyer M, Costa JJ, Lima A, Roig P, De Nicola AF. Protective effects of progesterone administration on axonal pathology in mice with experimental autoimmune encephalomyelitis. Brain Res 2009; 1283: 177-185.
200. Kipp M, Beyer C. Impact of sex steroids on neuroinflammatory processes and experimental multiple sclerosis. Front Neuroendocrinol 2009; 30: 188-200.
201. Kipp M, Berger K, Clarner T, Dang J, Beyer C. Sex steroids control neuroinflammatory processes in the brain: relevance for acute ischemia and degenerative demyelination. J Neuroendocrinol 2011; 24: 62-70.
202. Leonelli E, Bianchi R, Cavaletti G, Caruso D, Crippa D, Garcia-Segura LM, Lauria G, Magnaghi V, Roglio I, Melcangi RC. Progesterone and its derivatives are neuroprotective agents in experimental diabetic neuropathy: a multimodal analysis. Neuroscience 2007; 144: 1293-1304.
203. Stein DG. Progesterone in the treatment of acute traumatic brain injury: a clinical perspective and update. Neuroscience 2011; 191: 101-106.
204. Griffin LD, Gong W, Verot L, Mellon SH. Niemann-Pick type C disease involves disrupted neurosteroidogenesis and responds to allopregnanolone. Nat Med 2004; 10: 704-711.
205. Fiore C, Inman DM, Hirose S, Noble LJ, Igarashi T, Compagnone NA. Treatment with the neurosteroid dehydroepiandrosterone promotes recovery of motor behavior after moderate contusive spinal cord injury in the mouse. J Neurosci Res 2004; 75: 391-400.
206. Pesaresi M, Giatti S, Cavaletti G, Abbiati F, Calabrese D, Lombardi R, Bianchi R, Lauria G, Caruso D, Garcia-Segura LM, Melcangi RC. Sex-dimorphic effects of dehydroepiandrosterone in diabetic neuropathy. Neuroscience 2011; Sep 16. [Epub ahead of print]. doi:10.1016/j.neuroscience.2011.09.013.
207. Schule C, Eser D, Baghai TC, Nothdurfter C, Kessler JS, Rupprecht R. Neuroactive steroids in affective disorders: target for novel antidepressant or anxiolytic drugs? Neuroscience 2011; 191: 55-77.
208. Marx CE, Bradford DW, Hamer RM, Naylor JC, Allen TB, Lieberman JA, Strauss JL, Kilts JD. Pregnenolone as a novel therapeutic candidate in schizophrenia: emerging preclinical and clinical evidence. Neuroscience 2011; 191: 78-90.
209. Ritsner MS. The clinical and therapeutic potentials of dehydroepiandrosterone and pregnenolone in schizophrenia. Neuroscience 2011; 191: 91-100.
210. Arevalo MA, Diz-Chaves Y, Santos-Galindo M, Bellini MJ, Garcia-Segura LM. Selective oestrogen receptor modulators decrease the inflammatory response of glial cells. J Neuroendocrinol 2011; 24: 183-190.
211. Pinna G, Rasmusson AM. Upregulation of neurosteroid biosynthesis as a pharmacological strategy to improve behavioral deficits in a putative mouse model of PTSD. J Neuroendocrinol 2011; 24: 102-116.
212. Papadopoulos V, Lecanu L. Caprospinol: discovery of a steroid drug candidate to treat Alzheimer's disease based on 22r-hydroxycholesterol structure and properties. J Neuroendocrinol 2011; 24: 93-101.
213. Girard C, Liu S, Adams D, Lacroix C, Sineus M, Boucher C, Papadopoulos V, Rupprecht R, Schumacher M, Groyer G. Axonal regeneration and neuroinflammation: roles for the translocator protein 18kDa (TSPO). J Neuroendocrinol 2011; 24: 71-81.
214. Nothdurfter C, Rammes G, Baghai TC, Schule C, Schumacher M, Papadopoulos V, Rupprecht R. TSPO (18kDa) as a target for novel anxiolytics with a favourable side-effect profile. J Neuroendocrinol 2011; 24: 82-92.
215. Leonelli E, Yague JG, Ballabio M, Azcoitia I, Magnaghi V, Schumacher M, Garcia-Segura LM, Melcangi RC. Ro5-4864, a synthetic ligand of peripheral benzodiazepine receptor, reduces aging-associated myelin degeneration in the sciatic nerve of male rats. Mech Ageing Dev 2005; 126: 1159-1163.
216. Giatti S, Pesaresi M, Cavaletti G, Bianchi R, Carozzi V, Lombardi R, Maschi O, Lauria G, Garcia-Segura LM, Caruso D, Melcangi RC. Neuroprotective effects of a ligand of translocator protein-18kDa (Ro5-4864) in experimental diabetic neuropathy. Neuroscience 2009; 164: 520-529.
217. Veiga S, Azcoitia I, Garcia-Segura LM. Ro5-4864, a peripheral benzodiazepine receptor ligand, reduces reactive gliosis and protects hippocampal hilar neurons from kainic acid excitotoxicity. J Neurosci Res 2005; 80: 129-137.
218. Cermenati G, Giatti S, Cavaletti G, Bianchi R, Maschi O, Pesaresi M, Abbiati F, Volonterio A, Saez E, Caruso D, Melcangi RC, Mitro N. Activation of the liver X receptor increases neuroactive steroid levels and protects from diabetes-induced peripheral neuropathy. J Neurosci 2010; 30: 11896-11901.
219. Caruso D, Scurati S, Maschi O, De Angelis L, Roglio I, Giatti S, Garcia-Segura LM, Melcangi RC. Evaluation of neuroactive steroid levels by liquid chromatography-tandem mass spectrometry in central and peripheral nervous system: effect of diabetes. Neurochem Int 2008; 52: 560-568.
220. Mensah-Nyagan AG, Saredi S, Schaeffer V, Kibaly C, Meyer L, Melcangi RC, Patte-Mensah C. Assessment of neuroactive steroid formation in diabetic rat spinal cord using high-performance liquid chromatography and continuous flow scintillation detection. Neurochem Int 2008; 52: 554-559.
221. Pesaresi M, Maschi O, Giatti S, Garcia-Segura LM, Caruso D, Melcangi RC. Sex differences in neuroactive steroid levels in the nervous system of diabetic and non-diabetic rats. Horm Behav 2010; 57: 46-55.
222. Roglio I, Giatti S, Pesaresi M, Bianchi R, Cavaletti G, Lauria G, Garcia-Segura LM, Melcangi RC. Neuroactive steroids and peripheral neuropathy. Brain Res Rev 2008; 57: 460-469.
223. Labombarda F, Pianos A, Liere P, Eychenne B, Gonzalez S, Cambourg A, De Nicola AF, Schumacher M, Guennoun R. Injury elicited increase in spinal cord neurosteroid content analyzed by gas chromatography mass spectrometry. Endocrinology 2006; 147: 1847-1859.
224. Meffre D, Pianos A, Liere P, Eychenne B, Cambourg A, Schumacher M, Stein DG, Guennoun R. Steroid profiling in brain and plasma of male and pseudopregnant female rats after traumatic brain injury: analysis by gas chromatography/mass spectrometry. Endocrinology 2007; 148: 2505-2517.
225. Caruso D, D'Intino G, Giatti S, Maschi O, Pesaresi M, Calabrese D, Garcia-Segura LM, Calza L, Melcangi RC. Sex-dimorphic changes in neuroactive steroid levels after chronic experimental autoimmune encephalomyelitis. J Neurochem 2010; 114: 921-932.
226. Giatti S, D'Intino G, Maschi O, Pesaresi M, Garcia-Segura LM, Calza L, Caruso D, Melcangi RC. Acute experimental autoimmune encephalomyelitis induces sex dimorphic changes in neuroactive steroid levels. Neurochem Int 2010; 56: 118-127.
227. Biamonte F, Assenza G, Marino R, D'Amelio M, Panteri R, Caruso D, Scurati S, Yague JG, Garcia-Segura LM, Cesa R, Strata P, Melcangi RC, Keller F. Interactions between neuroactive steroids and reelin haploinsufficiency in Purkinje cell survival. Neurobiol Dis 2009; 36: 103-115.
228. Melcangi RC, Caruso D, Levandis G, Abbiati F, Armentero MT, Blandini F. Modifications of neuroactive steroid levels in an experimental model of nigrostriatal degeneration: potential relevance to the pathophysiology of Parkinson's disease. J Mol Neurosci 2011; doi: 10.1007/512031-11-9570y.
229. Al Sweidi S, Sanchez MG, Bourque M, Morissette M, Dluzen D, Di Paolo T. Oestrogen receptors and signalling pathways: implications for neuroprotective effects of sex steroids in parkinson's disease. J Neuroendocrinol 2011; 24: 48-61.
230. Ahboucha S, Pomier-Layrargues G, Mamer O, Butterworth RF. Increased levels of pregnenolone and its neuroactive metabolite allopregnanolone in autopsied brain tissue from cirrhotic patients who died in hepatic coma. Neurochem Int 2006; 49: 372-378.
231. Luchetti S, Bossers K, Van de Bilt S, Agrapart V, Morales RR, Frajese GV, Swaab DF. Neurosteroid biosynthetic pathways changes in prefrontal cortex in Alzheimer's disease. Neurobiol Aging 2011; 32: 1964-1976.
232. Luchetti S, Bossers K, Frajese GV, Swaab DF. Neurosteroid biosynthetic pathway changes in substantia nigra and caudate nucleus in Parkinson's disease. Brain Pathol 2010; 20: 945-951.
233. Luchetti S, Huitinga I, Swaab DF. Neurosteroid and GABA-A receptor alterations in Alzheimer's disease, Parkinson's disease and multiple sclerosis. Neuroscience 2011; 191: 6-21.
234. Luchetti S, Bossers K, Van de Bilt S, Agrapart V, Morales RR, Frajese GV, Swaab DF. Neurosteroid biosynthetic pathways changes in prefrontal cortex in Alzheimer's disease. Neurobiol Aging 2011; 32: 1964-1976.
235. Weill-Engerer S, David JP, Sazdovitch V, Liere P, Eychenne B, Pianos A, Schumacher M, Delacourte A, Baulieu EE, Akwa Y. Neurosteroid quantification in human brain regions: comparison between Alzheimer's and nondemented patients. J Clin Endocrinol Metab 2002; 87: 5138-5143.
236. Melcangi RC, Garcia-Segura LM. Sex-specific therapeutic strategies based on neuroactive steroids: in search for innovative tools for neuroprotection. Horm Behav 2010; 57: 2-11.
237. Caruso D, Scurati S, Roglio I, Nobbio L, Schenone A, Melcangi RC. Neuroactive steroid levels in a transgenic rat model of CMT1A Neuropathy. J Mol Neurosci 2008; 34: 249-253.
238. di Michele F, Lekieffre D, Pasini A, Bernardi G, Benavides J, Romeo E. Increased neurosteroids synthesis after brain and spinal cord injury in rats. Neurosci Lett 2000; 284: 65-68.