Steroidogenic acute regulatory protein in the rat brain: cellular distribution, developmental regulation and overexpression after injury
Abstract
The central nervous system synthesizes steroids which regulate the development and function of neurons and glia and have neuroprotective properties. The first step in this process involves the delivery of free cholesterol to the inner mitochondrial membrane where it can be converted into pregnenolone. This delivery is mediated by steroidogenic acute regulatory protein (StAR). Here, we present a detailed analysis of the distribution of StAR expression in neurons and glia, in the developing, adult and aged male rat brain. Immunohistochemical analysis revealed that StAR is widely distributed throughout the brain, although in each brain area it is restricted to very specific neuronal and astroglial populations. In most regions expressing StAR, immunoreactivity appeared at P10 and the levels of expression then either increased or remained constant until adulthood. In 2‐year‐old rat brains, StAR immunoreactivity was increased compared to young adults. StAR was expressed in the subventricular zone of the adult brain, in proliferating cells which incorporate BrdU as well as in germinal layers in the developing brain. These findings indicate that StAR expression is developmentally regulated and that StAR may play some function in regulating cell proliferation in the brain. Furthermore, StAR mRNA and protein levels were acutely and transiently increased in the hippocampus following excitotoxic brain injury induced by the administration of kainic acid. This raises the possibility that the up‐regulation of StAR expression and the subsequent modifications in steroidogenesis may be part of the mechanisms used by the brain to cope with neurodegeneration.
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Tissue injury and inflammation with subsequent healing is associated with a specific physiological process that involves local production of estrogen from its precursors.
“Animal experiments with chemotoxic and mechanic stress to astroglia [20, 52, 53] and urinary bladder tissue as well as studies with isolated connective tissue such as fibroblasts and cartilage [54–56] have revealed that tissue injury and inflammation with subsequent healing is associated with a specific physiological process that involves the local production of estrogen from its precursors.”
From The pathophysiology of endometriosis and adenomyosis, tissue injury and repair (2009) · cites this paper as [52]
Interleukin-1-induced activation of COX-2 results in production of PGE2, which in turn activates STAR and P450 aromatase.
“Interleukin-1-induced activation of the cyclooxygenase-2 enzyme (COX-2) results in the production of prostaglandin E2 (PGE2), which in turn activates STAR (steroidogenic acute regulatory protein) and the P450 aromatase.”
From The pathophysiology of endometriosis and adenomyosis, tissue injury and repair (2009) · cites this paper as [52]
Cites
Real time quantitative PCR.Preprint
Heid, C., Stevens, J., Livak, K. J., & Williams, P. (1996) · Genome Research · doi:10.1101/gr.6.10.986 · Cited by 6,180 · see citing works
NeuN, a neuronal specific nuclear protein in vertebratesxs
Mullen, R. J., Buck, C. R., & Smith, A. M. (1992) · Development · doi:10.1242/dev.116.1.201 · Cited by 2,351 · see citing works
Luskin, M. B. (1993) · Neuron · doi:10.1016/0896-6273(93)90281-u · Cited by 1,803 · see citing works
Clark, B. J., Wells, J., King, S. R., & Stocco, D. M. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)46930-x · Cited by 1,168 · see citing works
Tanapat, P., Hastings, N. B., Reeves, A. J., & Gould, E. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-14-05792.1999 · Cited by 978 · see citing works
Oxysterols: Modulators of Cholesterol Metabolism and Other Processes
Schroepfer, G. J. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.1.361 · Cited by 972 · see citing works
García‐Segura, L. M., Azcoitia, Í., & DonCarlos, L. L. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00025-3 · Cited by 938 · see citing works
(1997) · PubMed · Cited by 643 · see citing works
Drug Transporters in the Central Nervous System: Brain Barriers and Brain Parenchyma Considerations
Lee, G. S., Dallas, S., Hong, M., & Bendayan, R. (2001) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01513-8 · Cited by 540 · see citing works
Neurotrophic and Neuroprotective Actions of Estrogens and Their Therapeutic Implications
Lee, S. H., & McEwen, B. S. (2001) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.41.1.569 · Cited by 533 · see citing works
Neuroprotective effects of estrogens: potential mechanisms of action
Green, P. S., & Simpkins, J. W. (2000) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(00)00017-4 · Cited by 523 · see citing works
Neurosteroidogenesis in Astrocytes, Oligodendrocytes, and Neurons of Cerebral Cortex of Rat Brain
Zwain, I. H., & Yen, S. S. C. (1999) · Endocrinology · doi:10.1210/endo.140.8.6907 · Cited by 473 · see citing works
Cholesterol Modulates α-Secretase Cleavage of Amyloid Precursor Protein
Bodovitz, S., & Klein, W. L. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.8.4436 · Cited by 447 · see citing works
Kimonides, V. G., Khatibi, N. H., Svendsen, C. N., Sofroniew, M. V., & Herbert, J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.4.1852 · Cited by 438 · see citing works
Neurosteroids: Cytochrome P-450 scc in Rat Brain
Goascogne, C. L., Röbel, P., Gouézou, M., Sananès, N., Baulieu, É.-É., & Waterman, M. R. (1987) · Science · doi:10.1126/science.3306919 · Cited by 363 · see citing works
Thorsten Diemer, A., Allen, J., Hales, K. H., & Hales, D. B. (2003) · Endocrinology · doi:10.1210/en.2002-0090 · Cited by 356 · see citing works
Self-citationPoirier, J., Baccichet, A., Dea, D., & Gauthier, S. G. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90456-p · Cited by 329 · see citing works
Karishma, K. K., & Herbert, J. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02099.x · Cited by 297 · see citing works
Hale, K. K., Trollinger, D. B., Rihanek, M., & Manthey, C. L. (1999) · PubMed · Cited by 282 · see citing works
Friedman, B., Hockfield, S. J., Black, J. A., Woodruff, K., & Waxman, S. G. (1989) · Glia · doi:10.1002/glia.440020510 · Cited by 248 · see citing works
Hale, K. K., Trollinger, D. B., Rihanek, M., & Manthey, C. L. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.7.4246 · Cited by 245 · see citing works
Estrogen-Receptor-Dependent Regulation of Neural Stem Cell Proliferation and Differentiation
Brännvall, K. (2002) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2002.1194 · Cited by 240 · see citing works
Furukawa, A., Miyatake, A., Ohnishi, T., & Ichikawa, Y. (1998) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1998.71062231.x · Cited by 231 · see citing works
Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus
Banasr, M., Héry, M., Brezun, J. M., & Daszuta, A. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01763.x · Cited by 226 · see citing works
Kuhlmann, A. C., & Guilarte, T. R. (2000) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2000.0741694.x · Cited by 215 · see citing works
Sugawara, T., Lin, D., Holt, J. A., MARTIN, K. O., Javitt, N. B., Miller, W. L., & Strauss, J. F. (1995) · Biochemistry · doi:10.1021/bi00039a004 · Cited by 211 · see citing works
King, S. R., Manna, P. R., Ishii, T., Syapin, P. J., Ginsberg, S. D., Wilson, K. L., Walsh, L. P., Parker, K. L., Stocco, D. M., Smith, R. G., et al. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-24-10613.2002 · Cited by 209 · see citing works
Wise, P. M., Dubal, D. B., Wilson, M. E., Rau, S. W., Bottner, M. B., & Rosewell, K. L. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00136-9 · Cited by 207 · see citing works
Dehydroepiandrosterone: Biosynthesis and Metabolism in the Brain
Zwain, I. H., & Yen, S. S. C. (1999) · Endocrinology · doi:10.1210/endo.140.2.6528 · Cited by 193 · see citing works
Tracking the Role of a StAR in the Sky of the New Millennium
Stocco, D. M. (2001) · Molecular Endocrinology · doi:10.1210/mend.15.8.0697 · Cited by 193 · see citing works
Fuhrmann, T. R., Timberg, R., King, S. R., Hales, K. H., Hales, D. B., Stocco, D. M., & Orly, J. (1998) · Endocrinology · doi:10.1210/endo.139.1.5694 · Cited by 181 · see citing works
Self-citationCardounel, A. J., Regelson, W., & Kalimi, M. (1999) · Proceedings of The Society for Experimental Biology and Medicine · doi:10.1046/j.1525-1373.1999.d01-124.x · Cited by 177 · see citing works
Bologa, L., Sharma, J., & Roberts, E. R. (1987) · Journal of Neuroscience Research · doi:10.1002/jnr.490170305 · Cited by 166 · see citing works
Ormerod, B. K., & Galea, L. A. M. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00474-7 · Cited by 163 · see citing works
Garcı́a‐Estrada, J., Luquı́n, S., Fernandez, A. M., & García‐Segura, L. M. (1999) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(98)00065-3 · Cited by 150 · see citing works
START domain proteins and the intracellular trafficking of cholesterol in steroidogenic cells
Strauss, J. F., Kishida, T., Christenson, L. K., Fujimoto, T., & Hiroi, H. (2003) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(03)00063-7 · Cited by 150 · see citing works
Localization of the Steroidogenic Acute Regulatory Protein in Human Tissues1
Pollack, S. E., Furth, E. E., Kallen, C. B., Arakane, F., Kiriakidou, M., Kozarsky, K., & Strauss, J. F. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.12.4445 · Cited by 140 · see citing works
Pregnenolone binds to microtubule-associated protein 2 and stimulates microtubule assembly
Murakami, K., Fellous, A., Baulieu, É.-É., & Röbel, P. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.7.3579 · Cited by 133 · see citing works
Progesterone and the oligodendroglial lineage: Stage‐dependent biosynthesis and metabolism
Gago, N., Akwa, Y., Sananès, N., Guennoun, R., Baulieu, E. E., El‐Etr, M., & Schumacher, M. (2001) · Glia · doi:10.1002/glia.1117 · Cited by 127 · see citing works
Mitochondrial specificity of the early steps in steroidogenesis
Miller, W. L. (1995) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/0960-0760(95)00212-x · Cited by 111 · see citing works
Localization of the Steroidogenic Acute Regulatory Protein in Human Tissues
Pollack, S. E. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.82.12.4243 · Cited by 111 · see citing works
Neuroprotective activities of estrogen: An update
Behl, C., & Manthey, D. (2000) · Journal of Neurocytology · doi:10.1023/a:1007109222673 · Cited by 107 · see citing works
Rao, V. L. R., Rao, A. M., Dog⫧an, A., Bowen, K. K., Hatcher, J. F., Rothstein, J. D., & Dempsey, R. J. (2000) · Neurochemistry International · doi:10.1016/s0197-0186(99)00153-9 · Cited by 100 · see citing works
Hales, K. H., Thorsten Diemer, A., Ginde, S., Shankar, B. K., Roberts, M. E., Bosmann, H. B., & Hales, D. B. (2000) · Endocrinology · doi:10.1210/endo.141.11.7780 · Cited by 82 · see citing works
Self-citationLapchak, P. A., & Araujo, D. M. (2001) · International review of neurobiology · doi:10.1016/s0074-7742(01)46069-7 · Cited by 76 · see citing works
Altar, C. A., & Baudry, M. (1990) · Experimental Neurology · doi:10.1016/s0014-4886(05)80024-x · Cited by 71 · see citing works
Dehydroepiandrosterone (DHEA) reduces neuronal injury in a rat model of global cerebral ischemia.
Li, H., Klein, G., Sun, P., & Buchan, A. M. (2001) · Brain Research · doi:10.1016/s0006-8993(00)03077-8 · Cited by 70 · see citing works
Jung‐Testas, I., Schumacher, M., Röbel, P., & Baulieu, E. E. (1996) · Cellular and Molecular Neurobiology · doi:10.1007/bf02088110 · Cited by 62 · see citing works
Increased neurosteroids synthesis after brain and spinal cord injury in rats
di Michele, F., Lekieffre, D., Pasini, A., Bernardi, G., Bénavidès, J., & Romeo, E. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)00965-4 · Cited by 59 · see citing works
Zilz, A., Li, H., Castello, R., Papadopoulos, V., & Widmaier, E. P. (1999) · Endocrinology · doi:10.1210/endo.140.2.6475 · Cited by 58 · see citing works
Mayo, W., Moal, M. L., & Abrous, D. N. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2001.1677 · Cited by 41 · see citing works
Peripheral benzodiazepine receptor: structure and function in health and disease.
Papadopoulos, V. D. (2003) · PubMed · Cited by 39 · see citing works
Changes of steroidogenic acute regulatory protein mRNA expression in postnatal rat development
Kim, H. J., Park, C., Roh, G. S., Kang, S. S., Cho, G. J., & Choi, W. S. (2002) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00576-x · Cited by 24 · see citing works
Immunofluorescent localization of the StAR protein in mitochondria of mouse Leydig cells in vitro.
Kotula, M., Kozieł, E., Sadowska, J., Gancarczyk, M., & Bilińska, B. (2001) · PubMed · Cited by 5 · see citing works
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The pathophysiology of endometriosis and adenomyosis, tissue injury and repair
Leyendecker, G., Wildt, L., & Mall, G. (2009) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-009-1191-0 · Cited by 418 · see citing works
“Animal experiments with chemotoxic and mechanic stress to astroglia [20, 52 , 53] and urinary bladder tissue as well as studies with isolated connective tissue such as Wbroblasts and cartilage [54–56] have revealed that tissue injury and inXammation with subsequent healing is associated with a speciWc physiological pr…”
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Sierra, A., Gottfried‐Blackmore, A., Milner, T. A., McEwen, B. S., & Bulloch, K. (2008) · Glia · doi:10.1002/glia.20644 · Cited by 405 · see citing works
Self-citationdo Rego, J. L., Seong, J. Y., Burel, D., Leprince, J., Luu-The, V., Tsutsui, K., Tonon, M., Pelletier, G., & Vaudry, H. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.006 · Cited by 356 · see citing works
Neuroactive steroids: State of the art and new perspectives
Melcangi, R. C., García‐Segura, L. M., & Mensah‐Nyagan, A. G. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-7403-5 · Cited by 232 · see citing works
Glia-neuron crosstalk in the neuroprotective mechanisms of sex steroid hormones
García‐Ovejero, D., Azcoitia, Í., DonCarlos, L. L., Melcangi, R. C., & García‐Segura, L. M. (2005) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.12.018 · Cited by 220 · see citing works
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García‐Segura, L. M., & Melcangi, R. C. (2006) · Glia · doi:10.1002/glia.20404 · Cited by 198 · see citing works
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Santos‐Galindo, M., Acaz‐Fonseca, E., Bellini, M. J., & García‐Segura, L. M. (2011) · Biology of Sex Differences · doi:10.1186/2042-6410-2-7 · Cited by 190 · see citing works
Aromatase: a neuroprotective enzyme
García‐Segura, L. M., Veiga, S. J., Sierra, A., Melcangi, R. C., & Azcoitia, Í. (2003) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2003.09.005 · Cited by 182 · see citing works
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Saldanha, C. J., Duncan, K. A., & Walters, B. J. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.04.016 · Cited by 167 · see citing works
Schumacher, M., Guennoun, R., Ghoumari, A. M., Massaad, C., Robert, F., El‐Etr, M., Akwa, Y., Rajkowski, K. M., & Baulieu, É.-É. (2007) · Endocrine Reviews · doi:10.1210/er.2006-0050 · Cited by 165 · see citing works
A new concept of endometriosis and adenomyosis, tissue injury and repair (TIAR)
Leyendecker, G., & Wildt, L. (2011) · hmbci · doi:10.1515/hmbci.2011.002 · Cited by 147 · see citing works
Oestrogens and Progestagens: Synthesis and Action in the Brain
Rossetti, M. F., Cambiasso, M. J., Holschbach, M., & Cabrera, R. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12402 · Cited by 129 · see citing works
Regulation of astroglia by gonadal steroid hormones under physiological and pathological conditions
Acaz‐Fonseca, E., Ávila-Rodriguez, M., García‐Segura, L. M., & Barreto, G. E. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.06.002 · Cited by 126 · see citing works
Meffre, D., Pianos, A., Lière, P., Eychenne, B., Cambourg, A., Schumacher, M., Stein, D. G., & Guennoun, R. (2007) · Endocrinology · doi:10.1210/en.2006-1678 · Cited by 126 · see citing works
Labombarda, F., Pianos, A., Lière, P., Eychenne, B., González, S. L., Cambourg, A., Nicola, A. F. D., Schumacher, M., & Guennoun, R. (2006) · Endocrinology · doi:10.1210/en.2005-0955 · Cited by 94 · see citing works
Neurosteroids: The StAR Protein in the Brain
Sierra, A. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2004.01226.x · Cited by 93 · see citing works
Self-citationSteroidogenic acute regulatory protein in the brain
Lavaque, E., Sierra, A., Azcoitia, I., & Garcia-Segura, L. M. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.05.060 · Cited by 81 · see citing works
Self-citationSakamoto, H., Ukena, K., Takemori, H., Okamoto, M., Kawata, M., & Tsutsui, K. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.04.003 · Cited by 80 · see citing works
Veiga, S. J., Melcangi, R. C., DonCarlos, L. L., García‐Segura, L. M., & Azcoitia, Í. (2004) · Experimental Gerontology · doi:10.1016/j.exger.2004.05.008 · Cited by 75 · see citing works
Soma, K. K., Sinchak, K., Lakhter, A. J., Schlinger, B. A., & Micevych, P. E. (2005) · Endocrinology · doi:10.1210/en.2005-0569 · Cited by 75 · see citing works
Bryan, K. J., Mudd, J. C., Richardson, S. L., Chang, J., Lee, H., Zhu, X., Smith, M. A., & Casadesús, G. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06502.x · Cited by 70 · see citing works
Estrogen actions in the nervous system
Cersosimo, M. G., & Benarroch, E. E. (2015) · Neurology · doi:10.1212/wnl.0000000000001776 · Cited by 68 · see citing works
Lavaque, E., Mayen, A., Azcoitia, Í., Tena‐Sempere, M., & García‐Segura, L. M. (2005) · Journal of Neurobiology · doi:10.1002/neu.20221 · Cited by 67 · see citing works
Self-citationNeurosteroidogenesis and progesterone anti‐inflammatory/neuroprotective effects
Nicola, A. F. D., Garay, L. I., Meyer, M., Guennoun, R., Sitruk-Ware, R. L., Schumacher, M., & Deniselle, M. C. G. (2017) · Journal of Neuroendocrinology · doi:10.1111/jne.12502 · Cited by 65 · see citing works
Villeneuve, D. L., Wang, R., Bencic, D. C., Biales, A. D., Martinović‐Weigelt, D., Lazorchak, J. M., Toth, G. P., & Ankley, G. T. (2009) · Environmental Toxicology and Chemistry · doi:10.1897/08-653.1 · Cited by 54 · see citing works
Phenotypic Features Associated with Mutations in Steroidogenic Acute Regulatory Protein
Bhangoo, A., Gu, W.-X., Pavlakis, S. G., Anhalt, H., Heier, L., Ten, S., & Jameson, J. L. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-0434 · Cited by 52 · see citing works
George, O., Vallée, M., Moal, M. L., & Mayo, W. (2006) · Psychopharmacology · doi:10.1007/s00213-005-0254-6 · Cited by 52 · see citing works
Meethal, S. V., Liu, T., Chan, H. W., Ginsburg, E., Wilson, A. C., Gray, D. N., Bowen, R. L., Vonderhaar, B. K., & Atwood, C. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06192.x · Cited by 51 · see citing works
Lopez-Rodriguez, A., Acaz‐Fonseca, E., Giatti, S., Caruso, D., Viveros, M.-P., Melcangi, R., & Garcia-Segura, L. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.02.018 · Cited by 52 · see citing works
Injury-Induced Regulation of Steroidogenic Gene Expression in the Cerebellum
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Cisternas, C. D., Tome, K., Caeiro, X. E., Dadam, F., García‐Segura, L. M., & Cambiasso, M. J. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.07.027 · Cited by 44 · see citing works
Nunez, B. S., & Evans, A. N. (2006) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2006.11.011 · Cited by 41 · see citing works
Munetomo, A., Hojo, Y., Higo, S., Kato, A., Yoshida, K., Shirasawa, T., Shimizu, T., Barron, A. M., Kimoto, T., & Kawato, S. (2015) · The Journal of Physiological Sciences · doi:10.1007/s12576-015-0363-x · Cited by 41 · see citing works
Veiga, S. J., Azcoitia, Í., & García‐Segura, L. M. (2005) · Neuroreport · doi:10.1097/01.wnr.0000179081.39659.7d · Cited by 41 · see citing works
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Wirbisky, S. E., Sepúlveda, M. S., Weber, G. J., Jannasch, A. S. H., Horzmann, K. A., & Freeman, J. L. (2016) · Toxicological Sciences · doi:10.1093/toxsci/kfw115 · Cited by 38 · see citing works
Profiling Neuroactive Steroid Levels After Traumatic Brain Injury in Male Mice
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The steroidogenic acute regulatory protein is expressed in steroidogenic cells of the day-old brain
King, S. R., Ginsberg, S. D., Ishii, T., Smith, R. G., Parker, K. L., & Lamb, D. J. (2004) · Endocrinology · doi:10.1210/en.2003-1740 · Cited by 34 · see citing works
Powrie, Y. S. L., & Smith, C. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1324-0 · Cited by 35 · see citing works
Emerging Roles for Neurosteroids in Sexual Behavior and Function
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Cholesterol signaling in single cells: lessons from STAR and sm-FISH
Jefcoate, C. R. E., & Lee, J. (2018) · Journal of Molecular Endocrinology · doi:10.1530/jme-17-0281 · Cited by 33 · see citing works
Sakamoto, H., Ukena, K., Kawata, M., & Tsutsui, K. (2008) · The Cerebellum · doi:10.1007/s12311-008-0007-2 · Cited by 28 · see citing works
Canis, M. J., Bourdel, N., Houlle, C., Grémeau, A.-S., Botchorishvili, R., & Matsuzaki, S. (2017) · Journal of Gynecology Obstetrics and Human Reproduction · doi:10.1016/j.jogoh.2016.12.008 · Cited by 27 · see citing works
Steroidogenic Acute Regulatory Protein Expression in the Central Nervous System
King, S. R., & Stocco, D. M. (2011) · Frontiers in Endocrinology · doi:10.3389/fendo.2011.00072 · Cited by 28 · see citing works
Progesterone: Synthesis, Metabolism, Mechanism of Action, and Effects in the Nervous System
Schumacher, M., Zhu, X., & Guennoun, R. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00054-7 · Cited by 28 · see citing works
Hormonal and genetic factors interact to control aromatase expression in the developing brain
Cisternas, C. D., García‐Segura, L. M., & Cambiasso, M. J. (2017) · Journal of Neuroendocrinology · doi:10.1111/jne.12535 · Cited by 24 · see citing works
Bian, C., Zhu, H.-T., Zhao, Y.-G., Cai, W., & Zhang, J.-Q. (2014) · Journal of Molecular Neuroscience · doi:10.1007/s12031-014-0285-8 · Cited by 25 · see citing works
Changes in neurosteroidogenesis during demyelination and remyelination in cuprizone‐treated mice
Leicaj, M. L., Pasquini, L. A., Lima, A. E., Deniselle, M. C. G., Pasquini, J. M., Nicola, A. F. D., & Garay, L. I. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12649 · Cited by 24 · see citing works
Neurosteroids and the Nervous System
King, S. R. (2012) · SpringerBriefs in neuroscience · doi:10.1007/978-1-4614-5559-2 · Cited by 22 · see citing works
Karri, S., Dertien, J. S., Stocco, D. M., & Syapin, P. J. (2007) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2007.01600.x · Cited by 23 · see citing works
Migliara, G., Mueller, M., Piermattei, A., Brodie, C., Paidas, M. J., Barnea, E. R., & Ria, F. (2017) · Oncotarget · doi:10.18632/oncotarget.15662 · Cited by 21 · see citing works
Immunohistochemical detection of StarD6 in the rat nervous system
Chang, I. Y., Kim, J. H., Hwang, G., Song, P. I., Song, R. J., Kim, J. W., & Yoon, S. P. (2007) · Neuroreport · doi:10.1097/wnr.0b013e3282f0402f · Cited by 19 · see citing works
Garay, L. I., Paula, G. G., Guennoun, R., Schumacher, M., Deniselle, M. C. G., & Nicola, A. F. D. (2016) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2016.09.001 · Cited by 18 · see citing works
Brain steroidogenesis: emerging therapeutic strategies to prevent neurodegeneration
Azcoitia, Í., Sierra, A., Veiga, S. J., & García‐Segura, L. M. (2004) · Journal of Neural Transmission · doi:10.1007/s00702-004-0179-y · Cited by 17 · see citing works
Self-citationGnRH-Mediated DAN Production Regulates the Transcription of the GnRH Receptor in Gonadotrope Cells
de Maturana, R. L., Martin, B., Millar, R. P., Brown, P., Davidson, L., Pawson, A. J., Nicol, M. R., Mason, J. I., Barran, P. E., Naor, Z., et al. (2007) · NeuroMolecular Medicine · doi:10.1007/s12017-007-8004-z · Cited by 17 · see citing works
Acaz‐Fonseca, E., Castelló‐Ruiz, M., Burguete, M. C., Aliena‐Valero, A., Salom, J. B., Torregrosa, G., & García‐Segura, L. M. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14731 · Cited by 17 · see citing works
Chang, I. Y., Ohn, T., Ko, G. S., Yoon, Y., Kim, J. W., & Yoon, S. P. (2011) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2011.10.003 · Cited by 16 · see citing works
The changed immunoreactivity of StarD6 after pilocarpine-induced epilepsy
Chang, I. Y., Kim, J. K., Lee, S. M., Kim, J. N., Soh, J., Kim, J. W., & Yoon, S. P. (2009) · Neuroreport · doi:10.1097/wnr.0b013e32832ca264 · Cited by 16 · see citing works
Steroidogenic acute regulatory protein: its presence and function in brain neurosteroidogenesis
Kim, H. J., Kang, S. S., Cho, G. J., & Choi, W. S. (2004) · Archivum histologicum japonicum · doi:10.1679/aohc.67.383 · Cited by 16 · see citing works
Does the StarD6 mark the same as the StAR in the nervous system?
Chang, I. Y., Jeon, Y. J., Jung, S. M., Jang, Y. H., Ahn, J. B., Park, K. S., & Yoon, S. P. (2010) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2010.06.006 · Cited by 15 · see citing works
Kudová, E., Mareš, P., Hill, M., Vondráková, K., Tsenov, G., Chodounská, H., Kubová, H., & Valeš, K. (2021) · Pharmaceuticals · doi:10.3390/ph15010049 · Cited by 14 · see citing works
Song, D., & Du, T. (2014) · Current Neuropharmacology · doi:10.2174/1570159x12666140828222115 · Cited by 14 · see citing works
Garcia, C. I., Paez, P. M., Soto, E. F., & Pasquini, J. M. (2007) · Developmental Neuroscience · doi:10.1159/000097317 · Cited by 11 · see citing works
Propiedades neuroprotectoras de los esteroides sexuales y los neuroesteroides
Veiga, S. J., García‐Segura, L. M., & Azcoitia, Í. (2004) · Revista de Neurología · doi:10.33588/rn.3911.2004555 · Cited by 10 · see citing works
The Effects of Neuroactive Steroids on Myelin in Health and Disease
Kalakh, S., & Mouihate, A. (2024) · Medical Principles and Practice · doi:10.1159/000537794 · Cited by 8 · see citing works
Manna, P. R. (2025) · Journal of Endocrinology · doi:10.1530/joe-24-0380 · Cited by 9 · see citing works
Jadhav, V., Stair, J. G., Eck, R. J., Smukowski, S. N., Currey, H. N., García‐Toscano, L., Hincks, J. C., Latimer, C. S., Valdmanis, P. N., Kraemer, B. C., et al. (2024) · Neurobiology of Disease · doi:10.1016/j.nbd.2024.106441 · Cited by 9 · see citing works
Inter-relations of brain neurosteroids and monoamines towards reproduction in fish
Kalarani, A., VINODHA, V., & Moses, I. R. (2021) · Reproduction and Breeding · doi:10.1016/j.repbre.2021.09.001 · Cited by 8 · see citing works
Neurosteroids and the Nervous System
King, S. R. (2012) · SpringerBriefs in neuroscience · doi:10.1007/978-1-4614-5559-2_1 · Cited by 7 · see citing works
Glia-Neuron Interactions: Neurosteroids and Epileptogenesis
Biagini, G., Marinelli, C., Panuccio, G., Puia, G., & Avoli, M. (2012) · IRIS UNIMORE (University of Modena and Reggio Emilia) · Cited by 7 · see citing works
Hormone Regulation of Adult Hippocampal Neurogenesis in the Mammalian Brain
Barha, C. K., Barker, J. M., Brummelte, S., Epp, J. R., & Galea, L. A. M. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00067-x · Cited by 7 · see citing works
Rosado-Olivieri, E. A., Ramos-Ortiz, G. A., Hernández‐Pasos, J., Díaz-Balzac, C. A., Vázquez‐Rosa, E., Valentín‐Tirado, G., Vega, I. E., & García‐Arrarás, J. E. (2017) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2017.08.004 · Cited by 7 · see citing works
Regulation and role of Acyl-CoA synthetase 4 in glial cells
Dattilo, M. A., Benzo, Y., Herrera, L. M., Prada, J. G., Lopez, P. F., Caruso, C. M., Lasaga, M., García, C. I., Paz, C., & Maloberti, P. M. (2020) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2020.105792 · Cited by 6 · see citing works
Chang, I. Y., Ohn, T., Jeon, Y. J., Lee, K. H., Kim, J. W., Kim, I. Y., & Yoon, S. P. (2013) · Acta Histochemica · doi:10.1016/j.acthis.2013.11.008 · Cited by 5 · see citing works
Steroidogenic enzymes in the hippocampus: Transcriptional regulation aspects
Rossetti, M. F., Varayoud, J., & Ramos, J. G. (2022) · Vitamins and hormones · doi:10.1016/bs.vh.2021.11.004 · Cited by 4 · see citing works
Uterine Peristalsis and the Development of Endometriosis and Adenomyosis
LEYENDECKER, G., & Wildt, L. (2011) · Wiley eBooks · doi:10.1002/9781444398519.ch20 · Cited by 4 · see citing works
Therapeutic implications of brain steroidogenesis
Azcoitia, Í., DonCarlos, L. L., Arévalo, M., & García‐Segura, L. M. (2009) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci.2010.003 · Cited by 2 · see citing works
Hormone Regulation of Neurogenesis Across the Lifespan
Duarte‐Guterman, P., Yagi, S., Epp, J. R., Brummelte, S., Wainwright, S. R., Barha, C. K., Chow, C., Barker, J. M., & Galea, L. A. M. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00108-5 · Cited by 2 · see citing works
Endometriosis and adenomyosis – a shared pathophysiology
LEYENDECKER, G., Wildt, L., & Mall, G. (2010) · CNR Solar (Scientific Open-access Literature Archive and Repository) (Consiglio Nazionale delle Ricerche) · Cited by 2 · see citing works
Regulation of synaptic plasticity by hippocampus synthesized estradiol
Barron, A. M., Hojo, Y., Mukai, H., Higo, S., Ooishi, Y., Hatanaka, Y., Ogiue‐Ikeda, M., Murakami, G., Kimoto, T., & Kawato, S. (2011) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci.2011.118 · Cited by 2 · see citing works
LEYENDECKER, G., & Wildt, L. (2011) · Springer eBooks · doi:10.1007/978-3-642-15012-8_9 · Cited by 2 · see citing works
Biagini, G., Marinelli, C., Panuccio, G., Puia, G., & Avoli, M. (2012) · Oxford University Press eBooks · doi:10.1093/med/9780199746545.003.0049 · Cited by 7 · see citing works
Steroid Metabolism in Glial Cells
Melcangi, R. C., & García‐Segura, L. M. (2008) · Springer eBooks · doi:10.1007/978-1-4020-6854-6_2 · Cited by 1 · see citing works
Kawato, S., Hojo, Y., Ogiue‐Ikeda, M., Soma, M., Saito, M., Kim, J., Munetomo, A., Higo, S., Ishii, H., Kato, A., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.17.670749 · Cited by 1 · see citing works
Pil, S. (2011) · InTech eBooks · doi:10.5772/17294
Title : Novel perspectives for progesterone in HRT, with special reference to the nervous system
Schumacher, M., Guennoun, R., Ghoumari, A. M., Massaad, C., Robert, F., Akwa, Y., Rajkowski, K. M., & Baulieu, É.-É. (2007)
Gabor, A. (2012) · uO Research (University of Ottawa) · doi:10.20381/ruor-5818
Neurosteroids and Sexual Behavior and Reproduction
King, S. R. (2009) · Springer eBooks · doi:10.1007/978-0-387-88186-7_20
Chapter 2 Steroid Metabolism in Glial Cells
Melcangi, R. C., & García‐Segura, L. M. (2008)
Cook, N. L. (2010) · Adelaide Research & Scholarship (AR&S) (University of Adelaide)
Oι υποδοχείς οιστρογόνων ως ρυθμιστές της παθοφυσιολογίας του κυττάρου
Γοργογιέτας, Β. (2018) · doi:10.12681/eadd/43829
Sex differences and the protective influence of estrogen in a mouse model of demyelinating disease
Taylor, L. C. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/5t0s-5k20
Hewitson, E., & Bailey, C. D. C. (2021) · The FASEB Journal · doi:10.1096/fasebj.2021.35.s1.03869
Sidime, F., Bendaoud, M., Abdelgawad, M., & Idrissi, A. E. (2023) · Springer eBooks · doi:10.1007/978-3-031-42383-3_20
Hogan, M. F., Akter, R., Aplin, A. C., Templin, A. T., Esser, N., Meier, D. T., Fountaine, B. S., CASTILLO, J. J., El-Osta, A., Hull-Meichle, R. L., et al. (2026) · Diabetologia · doi:10.1007/s00125-026-06749-8
- Authors
- Sierra, A., Lavaque, E., Perez‐Martin, M., Azcoitia, I., Hales, D. B., & Garcia‐Segura, L. M.
- Affiliations
- Instituto Cajal (ES)
- University of Illinois Chicago (US)
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2003-09
- Volume
- 18
- Issue
- 6
- Pages
- 1458-1467
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W1994096100
- Cited by
- 98
- References
- 54
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 2 · 2023: 1 · 2022: 1 · 2021: 3 · 2020: 2 · 2019: 1 · 2018: 4 · 2017: 5 · 2016: 8 · 2015: 4 · 2014: 3 · 2013: 3 · 2012: 5
- FWCI
- 1.46
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- Funders
- Comunidad de Madrid
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pharmacological Receptor Mechanisms and Effects
- Keywords
- steroidogenic acute regulatory protein, stars, brain steroidogenesis, cholesterol transport, pregnenolone synthesis, neurosteroids, neuronal expression, astrocytes, subventricular zone, brain development, brain aging, excitotoxic brain injury, kainic acid, hippocampus, neurodegeneration, cell proliferation
- MeSH terms
- Steroidogenic Acute Regulatory Protein, Aging, Animals, Animals, Newborn, Brain Chemistry, Brain Injuries, Bromodeoxyuridine, Immunohistochemistry, Kainic Acid, Male, Neurons, Phosphoproteins, RNA, Messenger, Time Factors, Rats, Wistar, Gene Expression Regulation, Developmental, Excitatory Amino Acid Agonists, Reverse Transcriptase Polymerase Chain Reaction, Rats
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