Temporal and spatial distribution of corticosteroidogenic enzymes immunoreactivity in developing human adrenal
Abstract
Steroid hormones secreted by fetal adrenocortical cells are considered to be a requirement for a fetus to maintain intrauterine life, but, to date, the regulation of steroid hormone secretion has not been studied in detail in the human fetal adrenal gland. In this study, we examined the immunolocalization of steroidogenic enzymes and their local regulation, including adrenal 4-binding protein (Ad4BP or NR5A1), steroidogenic acute regulatory protein (StAR), P450 cholesterol side-chain cleavage (P450scc or CYP11A1), P450 17alpha-hydroxylase/17,20-lyase (P450c17 or CYP17), 3beta-hydroxysteroid dehydrogenase/isomerase (3beta-HSD), P450 21 hydroxylase (P450c21 or CYP21), dehydroepiandrosterone sulfotransferase (DHEA-ST), P450 oxidoreductase and cytochrome b5, in the human fetal adrenal gland (n=31) obtained from fetuses ranging in ages from 14 to 40 weeks of gestation. Ad4BP immunoreactivity was detected in all adrenocortical zones throughout gestation, suggesting that this nuclear protein is likely to be essential in the development of the human adrenal. Immunoreactivity for StAR, P450scc, P450c21, P450 oxidoreductase and cytochrome b5 was detected only in fetal and transitional zone between 14 and 22 weeks of gestation, but was detected in all three zones after 23 gestational weeks. 3beta-HSD immunoreactivity was not detected in any of the three cortical zones prior to 22 weeks of gestation, but became discernible in the transitional zone and definitive zone after 23 weeks. Immunoreactivity for P450c17 and DHEA-ST was detected in the transitional and fetal zones throughout gestation, but not in the definitive zone. These results suggest that the human adrenal cortex may produce dehydroepiandrosterone (DHEA) in the transitional and fetal zones throughout gestation, and cortisol in the transitional zone after the 23rd week of gestation.
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The p.Val281Leu (V281L) mutation is by far the most common allele detected in patients with NC CAH and is highly prevalent in Ashkenazi Jews.
“The p.Val281Leu (V281L) mutation is by far the most common allele detected in patients with NC CAH and is highly prevalent in Ashkenazi Jews (155).”
From Congenital Adrenal Hyperplasia—Current Insights in Pathophysiology, Diagnostics, and Management (2022) · cites this paper as [155]
Cites
Molecular biology of steroid hormone synthesis
MILLER, W. L. (1988) · Endocrine Reviews · doi:10.1210/edrv-9-3-295 · Cited by 1,397 · 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
Regulation of the acute production of steroids in steroidogenic cells
STOCCO, D. M., & CLARK, B. J. (1996) · Endocrine Reviews · doi:10.1210/edrv-17-3-221 · Cited by 1,057 · see citing works
Steroidogenic factor 1: a key determinant of endocrine development and function
Parker, K. L., & Schimmer, B. P. (1997) · Endocrine Reviews · doi:10.1210/edrv.18.3.0301 · Cited by 764 · see citing works
Lala, D. S. (1992) · Molecular Endocrinology · doi:10.1210/me.6.8.1249 · Cited by 678 · see citing works
Developmental and Functional Biology of the Primate Fetal Adrenal Cortex*
Mesiano, S. A., & Jaffe, R. B. (1997) · Endocrine Reviews · doi:10.1210/edrv.18.3.0304 · Cited by 676 · see citing works
Regulation of the acute production of steroids in steroidogenic cells
Stocco, D. M. (1996) · Endocrine Reviews · doi:10.1210/er.17.3.221 · Cited by 635 · see citing works
A common trans-acting factor, Ad4-binding protein, to the promoters of steroidogenic P-450s.
Morohashi, K.-I., Honda, S., Inomata, Y., Handa, H., & Omura, T. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)37129-7 · Cited by 537 · see citing works
The Mechanism of Initiation of Parturition in the Ewe
Liggins, G. C., Fairclough, R. J., Grieves, S. A., Kendall, J. Z., & Knox, B. S. (1973) · Elsevier eBooks · doi:10.1016/b978-0-12-571129-6.50007-5 · Cited by 509 · see citing works
Stone, D. A., & Hechter, O. (1954) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(54)90501-9 · Cited by 445 · see citing works
Ad4BP regulating steroidogenic P-450 gene is a member of steroid hormone receptor superfamily.
Honda, S., Morohashi, K.-I., Nomura, M., Takeya, H., Kitajima, M., & Omura, T. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53202-6 · Cited by 403 · see citing works
Ikeda, Y., Lala, D. S., Luo, X., Kim, E., Moisan, M., & Parker, K. L. (1993) · Molecular Endocrinology · doi:10.1210/mend.7.7.8413309 · Cited by 400 · see citing works
Hormonal and developmental regulation of the steroidogenic acute regulatory protein
Clark, B. J., Soo, S. C., Caron, K. M., Ikeda, Y., Parker, K. L., & Stocco, D. M. (1995) · Molecular Endocrinology · doi:10.1210/mend.9.10.8544843 · Cited by 303 · see citing works
Adrenocortical-related maturational events in the fetus
Liggins, G. C. (1976) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(76)90680-3 · Cited by 291 · see citing works
Cholesterol side-chain cleavage, cytochrome P450, and the control of steroidogenesis
Simpson, E. R. (1979) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(79)90082-0 · Cited by 291 · see citing works
On the Mechanism of Action of ACTH
Garren, L. D., Gill, G. N., Masui, H., & Walton, G. M. (1971) · Elsevier eBooks · doi:10.1016/b978-0-12-571127-2.50035-3 · Cited by 260 · see citing works
Maturation and Activation of Hypothalamic-Pituitary Adrenal Function in Fetal Sheep*
Challis, J. R. G., & Brooks, A. N. (1989) · Endocrine Reviews · doi:10.1210/edrv-10-2-182 · Cited by 260 · see citing works
Karaboyas, G. C., & Koritz, S. B. (1965) · Biochemistry · doi:10.1021/bi00879a014 · Cited by 247 · see citing works
The regulation of 17,20 lyase activity
Miller, W. L., Auchus, R. J., & Geller, D. H. (1997) · Steroids · doi:10.1016/s0039-128x(96)00172-9 · Cited by 227 · see citing works
Regulation of the Primate Fetal Adrenal Cortex*
Pepe, G. J., & Albrecht, E. D. (1990) · Endocrine Reviews · doi:10.1210/edrv-11-1-151 · Cited by 209 · see citing works
VOUTILAINEN, R., & MILLER, W. L. (1986) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-63-5-1145 · Cited by 185 · see citing works
Lin, D., Black, S. M., Nagahama, Y., & Miller, W. L. (1993) · Endocrinology · doi:10.1210/endo.132.6.8504753 · Cited by 174 · see citing works
Yanagibashi, K., & Hall, P. F. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)83930-3 · Cited by 171 · see citing works
Farkash, Y., Timberg, R., & Orly, J. (1986) · Endocrinology · doi:10.1210/endo-118-4-1353 · Cited by 148 · 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
Mesiano, S. A., Coulter, C. L., & Jaffe, R. B. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.77.5.8077311 · Cited by 133 · see citing works
Cloning and expression of human liver dehydroepiandrosterone sulphotransferase
Comer, K. A., Falany, J. L., & Falany, C. N. (1993) · Biochemical Journal · doi:10.1042/bj2890233 · Cited by 120 · see citing works
Churchill, P. F., & Kimura, T. (1979) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)86728-5 · Cited by 117 · see citing works
Mitani, F., Shimizu, T., Ryouji, U. E. N. O., Ishimura, Y., Izumi, S., Komatsu, N., & Watanabe, K. (1982) · Journal of Histochemistry & Cytochemistry · doi:10.1177/30.10.6813370 · 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
Clark, B. J., Combs, R., Hales, K. H., Hales, D. B., & Stocco, D. M. (1997) · Endocrinology · doi:10.1210/endo.138.11.5535 · Cited by 105 · see citing works
Yamano, S., Aoyama, T., McBride, O. W., Hardwick, J. P., Gelboin, H. V., & Gonzalez, F. J. (1989) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)09090-x · Cited by 95 · see citing works
Mapes, S., Corbin, C. J., Tarantal, A., & Conley, A. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.9.6105 · Cited by 86 · see citing works
Yago, N., & ICHII, S. (1969) · PubMed · Cited by 85 · see citing works
Immunohistochemical study of cytochrome P-45017α in human adrenocortical disorders
Sasano, H., Mason, J. I., & Sasano, N. (1989) · Human Pathology · doi:10.1016/0046-8177(89)90174-3 · Cited by 68 · see citing works
Shinzawa, K., Kominami, S., & Takemori, S. (1985) · PubMed · Cited by 63 · see citing works
Coulter, C. L., & Jaffe, R. B. (1998) · Endocrinology · doi:10.1210/endo.139.12.6333 · Cited by 62 · see citing works
Immunolocalization of 3β-hydroxysteroid dehydrogenase in human adrenal cortex and in its disorders
Sasano, H., Mason, J. L., Sasano, N., & Nagura, H. (1990) · Endocrine Pathology · doi:10.1007/bf02915624 · Cited by 61 · see citing works
Immunohistochemical localization of NADPH-cytochrome P450 reductase in human tissues
Pauline, D. M. H., Stupans, L., Burgess, W. M., Birkett, D., & McManus, M. E. (1989) · Carcinogenesis · doi:10.1093/carcin/10.3.521 · Cited by 59 · see citing works
YANASE, T., SASANO, H., YUBISUI, T., SAKAI, Y., TAKAYANAGI, R., & NAWATA, H. (1998) · Endocrine Journal · doi:10.1507/endocrj.45.89 · Cited by 54 · see citing works
Self-citationKyoko, S., Shiro, K., & Takemori, S. (1985) · Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism · doi:10.1016/0005-2760(85)90263-2 · Cited by 52 · see citing works
Hu, M.-C., & Chung, B.-C. (1990) · Molecular Endocrinology · doi:10.1210/mend-4-6-893 · Cited by 43 · see citing works
Sasano, H., Sato, F., Shizawa, S., Nagura, H., & Coughtrie, M. W. H. (1995) · PubMed · Cited by 40 · see citing works
Sasano, H., Sasano, N., & Okamoto, M. (1989) · Pathology - Research and Practice · doi:10.1016/s0344-0338(89)80096-2 · Cited by 39 · see citing works
Luo, X., Ikeda, Y., Lala, D. S., Rice, D. A., Wong, M., & Parker, K. L. (1999) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(98)00146-0 · Cited by 34 · see citing works
Peptide Regulation of Pituitary and Target Tissue Function and Growth in the Primate Fetus
Jaffe, R. B., MULCHAHEY, J. J., Blasio, A. M. D., Martin, M. C., Blumenfeld, Z., & Dumesic, D. A. (1988) · Elsevier eBooks · doi:10.1016/b978-0-12-571144-9.50017-x · Cited by 26 · see citing works
The regulation of steroidogenesis by 17.ALPHA.-hydroxylase/17,20-lyase (P450c17).
Katagiri, M., & Kagawa, N. (1998) · Folia Pharmacologica Japonica · doi:10.1254/fpj.112.43 · Cited by 7 · see citing works
Expression of P450 oxidoreductase in the human arenal gland
Freije, W. A., ZHANG, Y., CARR, B., & Rainey, W. E. (1998) · Journal of the Society for Gynecologic Investigation · doi:10.1016/s1071-5576(97)86298-3 · Cited by 2 · see citing works
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3 of the 51 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones
Payne, A. H., & Hales, D. B. (2004) · Endocrine Reviews · doi:10.1210/er.2003-0030 · Cited by 1,766 · see citing works
Congenital Adrenal Hyperplasia—Current Insights in Pathophysiology, Diagnostics, and Management
Claahsen - van der Grinten, H. L., Speiser, P. W., Ahmed, S. F., Arlt, W., Auchus, R. J., Falhammar, H., Flück, C. E., Guasti, L., Huebner, A., Kortmann, B. B. M., et al. (2022) · Endocrine Reviews · doi:10.1210/endrev/bnab016 · Cited by 556 · see citing works
Ishimoto, H., & Jaffe, R. B. (2011) · Endocrine Reviews · doi:10.1210/er.2010-0001 · Cited by 379 · see citing works
Acute and chronic regulation of aldosterone production
Hattangady, N. G., Olala, L. O., Bollag, W. B., & Rainey, W. E. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.07.034 · Cited by 347 · see citing works
Cortisol and DHEA in development and psychopathology
Kamin, H. S., & Kertes, D. A. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.11.018 · Cited by 311 · see citing works
Adrenarche—physiology, biochemistry and human disease
Auchus, R. J., & Rainey, W. E. (2004) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2003.01858.x · Cited by 296 · see citing works
In humans, early cortisol biosynthesis provides a mechanism to safeguard female sexual development
Goto, M. (2006) · Journal of Clinical Investigation · doi:10.1172/jci25091 · Cited by 284 · see citing works
Dissecting human adrenal androgen production
Rainey, W. E., Carr, B. R., Sasano, H., Suzuki, T., & Mason, J. I. (2002) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(02)00609-4 · Cited by 270 · see citing works
Regulation of the adrenal androgen biosynthesis
Rainey, W. E., & Nakamura, Y. (2007) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2007.09.015 · Cited by 171 · see citing works
Miki, Y., Nakata, T., Suzuki, T., Darnel, A. D., Moriya, T., Kaneko, C., Hidaka, K., Shiotsu, Y., Kusaka, H., & Sasano, H. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020670 · Cited by 171 · see citing works
Developmental origins of the human hypothalamic-pituitary-adrenal axis
Howland, M. A., Sandman, C. A., & Glynn, L. M. (2017) · Expert Review of Endocrinology & Metabolism · doi:10.1080/17446651.2017.1356222 · Cited by 171 · see citing works
Stowasser, M., & Gordon, R. D. (2016) · Physiological Reviews · doi:10.1152/physrev.00026.2015 · Cited by 159 · see citing works
Premature adrenarche: Etiology, clinical findings, and consequences
Voutilainen, R., & Jääskeläinen, J. (2014) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2014.06.004 · Cited by 141 · see citing works
Mechanisms of Glucocorticoid Action During Development
Busada, J. T., & Cidlowski, J. A. (2017) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2016.12.004 · Cited by 141 · see citing works
Premature Birth and Developmental Programming: Mechanisms of Resilience and Vulnerability
Lammertink, F., Vinkers, C. H., Tataranno, M. L., & Benders, M. J. N. L. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.531571 · Cited by 132 · see citing works
The Orphan Nuclear Receptor NGFIB Regulates Transcription of 3β-Hydroxysteroid Dehydrogenase
Bassett, M. H., Suzuki, T., Sasano, H., de Vries, C. J. M., Jimenez, P. T., Carr, B. R., & Rainey, W. E. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405431200 · Cited by 126 · see citing works
Evolution of steroids during pregnancy: Maternal, placental and fetal synthesis
Morel, Y., Roucher, F., Plotton, I., Goursaud, C., Tardy, V., & Mallet, D. (2016) · Annales d'Endocrinologie · doi:10.1016/j.ando.2016.04.023 · Cited by 119 · see citing works
The Human Fetal Adrenal: Making Adrenal Androgens for Placental Estrogens
Rainey, W. E., Rehman, K. S., & Carr, B. R. (2004) · Seminars in Reproductive Medicine · doi:10.1055/s-2004-861549 · Cited by 114 · see citing works
Tardy-Guidollet, V., Menassa, R., Costa, J.-M., David, M., Bouvattier-Morel, C., Baumann, C., Houang, M., Lorenzini, F., Philip, N., Odent, S., et al. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-2895 · Cited by 96 · see citing works
Sirianni, R., Rehman, K. S., Carr, B. R., Parker, C. R., & Rainey, W. E. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0865 · Cited by 98 · see citing works
Adrenal gland development and defects
Kempná, P., & Flück, C. E. (2008) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2007.07.008 · Cited by 97 · see citing works
Colocalization of P450c17 and Cytochrome b5 in Androgen-Synthesizing Tissues of the Human1
Dharia, S. P., Slane, A., Jian, M., Conner, M. G., Conley, A. J., & Parker, C. R. (2004) · Biology of Reproduction · doi:10.1095/biolreprod.103.026732 · Cited by 96 · see citing works
The Biology of Normal Zona Glomerulosa And Aldosterone-Producing Adenoma: Pathological Implications
Seccia, T. M., Caroccia, B., Gómez-Sánchez, E. P., Gómez-Sánchez, C. E., & Rossi, G. P. (2018) · Endocrine Reviews · doi:10.1210/er.2018-00060 · Cited by 94 · see citing works
Adrenal Androgens in Humans and Nonhuman Primates: Production, Zonation and Regulation
Nguyen, A. D., & Conley, A. J. (2008) · KARGER eBooks · doi:10.1159/000134765 · Cited by 91 · see citing works
Maternal melatonin selectively inhibits cortisol production in the primate fetal adrenal gland
Torres‐Farfan, C., Richter, H. G., Germain, A. M., Valenzuela, G. J., Campino, C., Rojas‐García, P., Forcelledo, M. L., Torrealba, F., & Serón‐Ferré, M. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2003.056465 · Cited by 85 · see citing works
Adrenal changes associated with adrenarche
Nakamura, Y., Gang, H. X., Suzuki, T., Sasano, H., & Rainey, W. E. (2009) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-008-9092-2 · Cited by 84 · see citing works
Steroid metabolome in fetal and maternal body fluids in human late pregnancy
Hill, M., Pařı́zek, A., Cibula, D., Kancheva, R. L., Jirasek, J. E., Jirkovská, M., Velíková, M., Kubátová, J., Klímková, M., Pašková, A., et al. (2010) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2010.05.007 · Cited by 75 · see citing works
Molecular mechanisms of stem/progenitor cell maintenance in the adrenal cortex
Lerario, A. M., Finco, I., LaPensee, C., & Hammer, G. D. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00052 · Cited by 68 · see citing works
Circulating 11-oxygenated androgens across species
Rege, J., Garber, S., Conley, A. J., Elsey, R. M., Turcu, A. F., Auchus, R. J., & Rainey, W. E. (2019) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2019.04.005 · Cited by 68 · see citing works
The human fetal adrenal cortex and the window of sexual differentiation
Hanley, N. A., & Arlt, W. (2006) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2006.10.001 · Cited by 65 · see citing works
Homma, K., Hasegawa, T., MASUMOTO, M., Takeshita, E., Watanabe, K., Chiba, H., Kurosawa, T., Takahashi, T., & Matsuo, N. (2003) · Endocrine Journal · doi:10.1507/endocrj.50.783 · Cited by 63 · see citing works
The cAMP pathway and the control of adrenocortical development and growth
de Joussineau, C., Sahut‐Barnola, I., Levy, I., Saloustros, E. S., Val, P., Stratakis, C. A., & Martinez, A. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.10.006 · Cited by 62 · see citing works
Samandari, E., Kempná, P., Nuoffer, J., Hofer, G., Mullis, P. E., & Flück, C. E. (2007) · Journal of Endocrinology · doi:10.1677/joe-07-0166 · Cited by 60 · see citing works
Steroid hormone synthesis in pregnancy
Kallen, C. B. (2004) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/j.ogc.2004.08.009 · Cited by 56 · see citing works
Miki, Y., Clyne, C. D., Suzuki, T., Moriya, T., Shibuya, R., Nakamura, Y., Ishida, T., Yabuki, N., Kitada, K., Hayashi, S., et al. (2006) · Cancer Letters · doi:10.1016/j.canlet.2005.11.038 · Cited by 55 · see citing works
Chamoux, E., Narcy, A., Lehoux, J., & Gallo‐Payet, N. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.4.8359 · Cited by 55 · see citing works
Ontogeny of adrenal steroid biosynthesis: why girls will be girls
White, P. C. (2006) · Journal of Clinical Investigation · doi:10.1172/jci28296 · Cited by 53 · see citing works
DAX1 and its network partners: exploring complexity in development
Clipsham, R. C., & McCabe, E. R. B. (2003) · Molecular Genetics and Metabolism · doi:10.1016/j.ymgme.2003.08.023 · Cited by 49 · see citing works
Johnston, Z. C., Bellingham, M., Filis, P., Soffientini, U., Hough, D., Bhattacharya, S., Simard, M., Hammond, G. L., King, P., O’Shaughnessy, P. J., et al. (2018) · BMC Medicine · doi:10.1186/s12916-018-1009-7 · Cited by 44 · see citing works
Cheng, K., Seita, Y., Moriwaki, T., Noshiro, K., Sakata, Y., Hwang, Y. S., Torigoe, T., Saitou, M., Tsuchiya, H., Iwatani, C., et al. (2022) · Science Advances · doi:10.1126/sciadv.abn8485 · Cited by 48 · see citing works
Characterization of human adrenal steroidogenesis during fetal development
Melau, C., Nielsen, J. E., Frederiksen, H., Kilcoyne, K., Perlman, S., Lundvall, L., Langhoff Thuesen, L., Juul Hare, K., Andersson, A.-M., Mitchell, R. T., et al. (2019) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-01759 · Cited by 47 · see citing works
Lu, L., Suzuki, T., Yoshikawa, Y., Murakami, O., Miki, Y., Moriya, T., Bassett, M. H., Rainey, W. E., Hayashi, Y., & Sasano, H. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0069 · Cited by 45 · see citing works
Moran, F. M., Ford, J. J., Corbin, C. J., Mapes, S. M., Njar, V. C. O., Brodie, A. M., & Conley, A. J. (2002) · Endocrinology · doi:10.1210/en.2002-220329 · Cited by 44 · see citing works
Nguyen, A. D., Mapes, S. M., Corbin, C. J., & Conley, A. J. (2008) · Journal of Endocrinology · doi:10.1677/joe-08-0337 · Cited by 38 · see citing works
Pattison, J. C., Wendy Saltzman, A., Abbott, D. H., Hogan, B. K., Nguyen, A. D., Husen, B., Einspanier, A., Conley, A. J., & Bird, I. M. (2007) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2006.12.023 · Cited by 38 · see citing works
Profiling the Steroidogenic Pathway in Human Fetal and Adult Adrenals
Rehman, K., Carr, B. R., & Rainey, W. E. (2003) · Journal of the Society for Gynecologic Investigation · doi:10.1016/s1071-5576(03)00118-7 · Cited by 35 · see citing works
Adrenocortical Cytochrome b5 Expression during Fetal Development of the Rhesus Macaque
Mapes, S. M., Tarantal, A. F., Parker, C. R., Moran, F. M., Bahr, J. M., Pyter, L. M., & Conley, A. J. (2002) · Endocrinology · doi:10.1210/endo.143.4.8718 · Cited by 35 · see citing works
Update on Biology and Genomics of Adrenocortical Carcinomas: Rationale for Emerging Therapies
Lerário, A. M., Mohan, D. R., & Hammer, G. D. (2022) · Endocrine Reviews · doi:10.1210/endrev/bnac012 · Cited by 34 · see citing works
Nguyen, A. D., Corbin, C. J., Pattison, J. C., Bird, I. M., & Conley, A. J. (2008) · Endocrinology · doi:10.1210/en.2008-1303 · Cited by 33 · see citing works
Pattison, J. C., Abbott, D. H., Wendy Saltzman, A., Nguyen, A. D., Henderson, G. L., Jing, H., Pryce, C. R., Allen, A. J., Conley, A. J., & Bird, I. M. (2004) · Endocrinology · doi:10.1210/en.2004-0689 · Cited by 32 · see citing works
Metastin Stimulates Aldosterone Synthesis in Human Adrenal Cells
Nakamura, Y., Aoki, S., Xing, Y., Sasano, H., & Rainey, W. E. (2007) · Reproductive Sciences · doi:10.1177/1933719107307823 · Cited by 31 · see citing works
Early hypoadrenalism in premature infants at risk for bronchopulmonary dysplasia or death
Nykänen, P., Anttila, E., Heinonen, K., Hallman, M., & Voutilainen, R. (2007) · Acta Paediatrica · doi:10.1111/j.1651-2227.2007.00500.x · Cited by 30 · see citing works
Temporal and spatial distribution of mast cells and steroidogenic enzymes in the human fetal adrenal
Naccache, A., Louiset, E., Duparc, C., Laquerrière, A., Patrier, S., Renouf, S., Gómez-Sánchez, C. E., Mukai, K., Lefèbvre, H., & Castanet, M. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.06.015 · Cited by 30 · see citing works
CITED2 is expressed in human adrenocortical cells and regulated by basic fibroblast growth factor
Haase, M., Schott, M., Bornstein, S. R., Malendowicz, L. K., Scherbaum, W. A., & Willenberg, H. S. (2007) · Journal of Endocrinology · doi:10.1677/joe-06-0083 · Cited by 29 · see citing works
Conley, A. J., Moeller, B. C., Nguyen, A. D., Stanley, S. D., Plant, T. M., & Abbott, D. H. (2010) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2010.12.022 · Cited by 29 · see citing works
16α-Hydroxyprogesterone: Origin, biosynthesis and receptor interaction
Storbeck, K., Swart, P., Africander, D., Conradie, R., Toit, R. L.-D., & Swart, A. C. (2010) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2010.11.016 · Cited by 28 · see citing works
Fletcher, A. J. W., Hong, X., Wu, W. X., Nathanielsz, P. W., McGARRIGLE, H. H. G., Fowden, A. L., & Giussani, D. A. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00158.2003 · Cited by 28 · see citing works
FUNCTIONAL BIOLOGY OF THE PRIMATE FETAL ADRENAL GLAND: ADVANCES IN TECHNOLOGY PROVIDE NEW INSIGHT
Coulter, C. L. (2004) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2004.04031.x · Cited by 26 · see citing works
Barzon, L., Maffei, P., Sonino, N., Pilon, C., Baldazzi, L., Balsamo, A., Del Maschio, O., Masi, G., Trevisan, M., Pacenti, M., et al. (2007) · Journal of Endocrinological Investigation · doi:10.1007/bf03346358 · Cited by 24 · see citing works
Inhibition of Src tyrosine kinase stimulates adrenal androgen production
Sirianni, R., Carr, B., Andò, S., & Rainey, W. (2003) · Journal of Molecular Endocrinology · doi:10.1677/jme.0.0300287 · Cited by 23 · see citing works
Niwa, F., Kawai, M., Kanazawa, H., Iwanaga, K., Matsukura, T., Shibata, M., Hasegawa, T., & Heike, T. (2012) · Clinical Endocrinology · doi:10.1111/cen.12049 · Cited by 21 · see citing works
Nykänen, P., Heinonen, K., Riepe, F. G., Sippell, W. G., & Voutilainen, R. (2010) · Hormone Research in Paediatrics · doi:10.1159/000314970 · Cited by 21 · see citing works
Yang, M., & White, P. C. (2025) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgae535 · Cited by 20 · see citing works
New Insights in the Functional Zonation of the Canine Adrenal Cortex
Sanders, K., Mol, J. A., Kooistra, H. S., Slob, A., & Galac, S. (2016) · Journal of Veterinary Internal Medicine · doi:10.1111/jvim.13946 · Cited by 20 · see citing works
Nguyen, P., Young, I. R., Walker, D., & Hirst, J. J. (2004) · Journal of Endocrinology · doi:10.1677/joe.0.1820081 · Cited by 19 · see citing works
Adrenal androgen concentrations increase during infancy in male rhesus macaques (Macaca mulatta)
Conley, A. J., Plant, T. M., Abbott, D. H., Moeller, B. C., & Stanley, S. D. (2011) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00200.2011 · Cited by 18 · see citing works
STEROIDOGENIC ENZYME EXPRESSION WITHIN THE ADRENAL CORTEX DURING EARLY HUMAN GESTATION
Goto, M., Brickwood, S., Wilson, D. I., Wood, P. J., Mason, J. I., & Hanley, N. A. (2002) · Endocrine Research · doi:10.1081/erc-120016979 · Cited by 18 · see citing works
Coulter, C. L., McMillen, I. C., Bird, I. M., & Salkeld, M. D. (2002) · Biology of Reproduction · doi:10.1095/biolreprod67.2.584 · Cited by 17 · see citing works
Melau, C., Nielsen, J. E., Perlman, S., Lundvall, L., Langhoff Thuesen, L., Juul Hare, K., Schou Hammerum, M., Frederiksen, H., Mitchell, R. T., Juul, A., et al. (2021) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaa852 · Cited by 16 · see citing works
Glucocorticosteroids Effects on Brain Development in the Preterm Infant: A Role for Microglia?
Zinni, M., Pansiot, J., Billion, E., Baud, O., & Mairesse, J. (2021) · Current Neuropharmacology · doi:10.2174/1570159x19666210517112913 · Cited by 15 · see citing works
Masumoto, K., Tagawa, N., Kobayashi, Y., & Kusuda, S. (2018) · Pediatrics & Neonatology · doi:10.1016/j.pedneo.2018.12.001 · Cited by 14 · see citing works
Zone-specific reference ranges of fetal adrenal artery Doppler indices: a longitudinal study
Xu, R., Zhu, Z., Tang, W., Zhou, Q., & Zeng, S. (2020) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-020-03480-z · Cited by 12 · see citing works
Le développement de la surrénale humaine
Folligan, K., Bouvier, R., Targe, F., Morel, Y., & Trouillas, J. (2005) · Annales d Endocrinologie · doi:10.1016/s0003-4266(05)81789-5 · Cited by 11 · see citing works
Turning the spotlight on the C11-oxy androgens in human fetal development
du Toit, T., & Swart, A. C. (2021) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2021.105946 · Cited by 10 · see citing works
Malendowicz, L. K. (2011) · Folia Histochemica et Cytobiologica · doi:10.2478/v10042-010-0062-7 · Cited by 10 · see citing works
Fetal adrenal gland size in gestational diabetes mellitus
Hetkamp, T., Hammer, K., Möllers, M., Köster, H. A., Falkenberg, M. K., Kerschke, L., Braun, J., de Murcia, K. O., Klockenbusch, W., & Schmitz, R. (2019) · Journal of Perinatal Medicine · doi:10.1515/jpm-2019-0146 · Cited by 9 · see citing works
Nakamura, Y., Suzuki, T., & Sasano, H. (2007) · Endocrine Journal · doi:10.1507/endocrj.k07e-001 · Cited by 9 · see citing works
The invention of aldosterone, how the past resurfaces in pediatric endocrinology
Viengchareun, S., Pussard, E., Castanet, M., Sachs, L. M., Vu, T. A., Boileau, P., Lombès, M., & Martinerie, L. (2021) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2021.111375 · Cited by 7 · see citing works
ATP2A3 in Primary Aldosteronism: Machine Learning-Based Discovery and Functional Validation
Sun, Z., Kemter, E., Pang, Y., Bidlingmaier, M., Wolf, E., Reincke, M., & Williams, T. A. (2024) · Hypertension · doi:10.1161/hypertensionaha.124.23817 · Cited by 7 · see citing works
Michikata, K., Sameshima, H., Sumiyoshi, K., Kodama, Y., Kaneko, M., & Ikenoue, T. (2010) · Early Human Development · doi:10.1016/j.earlhumdev.2010.05.016 · Cited by 7 · see citing works
Lopez, A.-G., Duparc, C., Wils, J., Naccache, A., Castanet, M., Lefèbvre, H., & Louiset, E. (2021) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2021.111377 · Cited by 7 · see citing works
Fetal and Neonatal Adrenocortical Physiology
Watterberg, K. L. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4160-3479-7.10181-8 · Cited by 7 · see citing works
Étude histologique et moléculaire de la corticosurrénale fœtale humaine (12e-36e SD)
Folligan, K., Bouvier, R., Targe, F., Morel, Y., & Trouillas, J. (2005) · Annales d Endocrinologie · doi:10.1016/s0003-4266(05)82112-2 · Cited by 5 · see citing works
Life Course Impact of Glucocorticoids During Pregnancy on Muscle Development and Function
Liu, Y., Ding, Q., & Guo, W. (2021) · Frontiers in Animal Science · doi:10.3389/fanim.2021.788930 · Cited by 5 · see citing works
Fetal and Neonatal Adrenocortical Physiology
Watterberg, K. L., & Muglia, L. J. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-35214-7.00147-5 · Cited by 5 · see citing works
Prenatal corticosteroid use and offspring neurological outcomes
Yan, Y., Wang, J., & Lei, X. (2025) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2025.107564 · Cited by 3 · see citing works
Fetal adrenal gland size and umbilical artery Doppler in growth-restricted fetuses
Oelmeier, K., Möllers, M., Köster, H. A., Willy, D., Bormann, E., Braun, J., Klockenbusch, W., & Schmitz, R. (2022) · Journal of Perinatal Medicine · doi:10.1515/jpm-2022-0203 · Cited by 3 · see citing works
Regulation of Aldosterone Production
Rainey, W. E., Bollag, W. B., & Isales, C. M. (2009) · Elsevier eBooks · doi:10.1016/b978-0-12-373870-7.00024-7 · Cited by 3 · see citing works
Pituitary-Adrenal Axis During Human Development
Goto, M. (2007) · Clinical Pediatric Endocrinology · doi:10.1297/cpe.16.37 · Cited by 3 · see citing works
Expression of ghrelin in human fetal adrenal glands and paraadrenal nerve ganglions.
Obara-Moszyńska, M., Kędzia, A. W., & Chmielnicka-Kopaczyk, M. (2009) · Folia Histochemica et Cytobiologica · doi:10.2478/v10042-009-0023-1 · Cited by 3 · see citing works
Martinez-Arguelles, D. B., & Papadopoulos, V. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.66177-9 · Cited by 3 · see citing works
Glucocorticoid trajectories in preterm infants—born too soon, wired differently
Kuiri‐Hänninen, T., Flück, C. E., Silvennoinen, S., Groessl, M., & Sankilampi, U. (2026) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgag048 · Cited by 2 · see citing works
Sato, S., Watanabe, S., Saito, Y., Takanashi, A., Ikeda, H., Sakurai, Y., Koshinami, S., Kumagai, Y., Usuda, H., Hanita, T., et al. (2023) · Journal of the Endocrine Society · doi:10.1210/jendso/bvad100 · Cited by 2 · see citing works
Auchus, R. J. (2004) · The Endocrinologist · doi:10.1097/01.ten.0000146265.52916.23 · Cited by 1 · see citing works
Alonso, S., Cáceres, S., Vélez, D., Sanz, L. A. R., Silván, G., Illera, M. J., & Illera, J. C. (2021) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-021-03617-8 · Cited by 1 · see citing works
Regulation of Aldosterone Production
Monticone, S., Rainey, W. E., Bollag, W. B., & Isales, C. M. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-803247-3.00025-8 · Cited by 1 · see citing works
Tissue concentration of aldosterone in fetal adrenals of intrauterine death cases
Dwivedi, D., & Chander, B. (2022) · Journal of Pediatric Endocrinology and Metabolism · doi:10.1515/jpem-2022-0031 · Cited by 1 · see citing works
Tomita, Y., Umemura, S., Sasou, T., Hasegawa, H., Mitani, F., Shinohara, O., Ichikawa, I., & OSAMURA, R. Y. (2002) · ACTA HISTOCHEMICA ET CYTOCHEMICA · doi:10.1267/ahc.35.441
Aus der Medizinischen Klinik und Poliklinik I der
München, L.-M.-U., & Steinbeck, G. (2002)
Les androgènes : de la conception à la puberté féminine Androgens: from fetal life to puberty
Bouvattier, C. M. (2012)
- Authors
- Narasaka, T., Suzuki, T., Moriya, T., & Sasano, H.
- Affiliations
- Tohoku University (JP)
- Corresponding author
- Narasaka, Toshiaki
- Venue
- Molecular and Cellular Endocrinology
- Publisher
- Elsevier BV
- Published
- 2001-03
- Volume
- 174
- Issue
- 1-2
- Pages
- 111-120
- ISSN
- 0303-7207 (ISSN-L)
- OpenAlex
- W1980898029
- Cited by
- 109
- References
- 51
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 1 · 2023: 3 · 2022: 4 · 2021: 8 · 2020: 4 · 2019: 3 · 2018: 6 · 2017: 4 · 2016: 7 · 2014: 2 · 2012: 2
- FWCI
- 5.99
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular and Cellular Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministry of Education, Culture, Sports, Science and Technology (B-11470047)
- Naito Foundation
- Ministry of Health, Labour and Welfare (A-11137301)
- Suzuken Memorial Foundation
- Japan Society for the Promotion of Science
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal Regulation and Hypertension
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- Keywords
- fetal adrenal gland, adrenal cortex development, steroidogenic enzymes, immunoreactivity, gestational age, dehydroepiandrosterone, cortisol, steroidogenic acute regulatory protein, 3β-hydroxysteroid dehydrogenase, 17α-hydroxylase/17,20-lyase, 21-hydroxylase, cytochrome P450 oxidoreductase, cytochrome b5
- MeSH terms
- Steroidogenic Acute Regulatory Protein, Adrenal Cortex Hormones, Adrenal Glands, DNA-Binding Proteins, Enzymes, Female, Fetus, Humans, Immunohistochemistry, Male, Phosphoproteins, Pregnancy, Pregnancy Trimester, Second, Transcription Factors, Receptors, Cytoplasmic and Nuclear, Homeodomain Proteins, Fushi Tarazu Transcription Factors, Steroidogenic Factor 1
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