Cited by 109Adrenal Hormones and DisordersHormonal Regulation and HypertensionSexual Differentiation and Disorders

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Temporal and spatial distribution of Corticosteroidogenic Enzymes Immunoreactivity in developing human adrenal

Narasaka, Toshiaki, Suzuki, Takashi, Moriya, Takuya, Sasano, Hironobu·2001·Molecular and Cellular Endocrinology

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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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Molecular biology of steroid hormone synthesis
MILLER, W. L. (1988) · Endocrine Reviews · doi:10.1210/edrv-9-3-295 · Cited by 1,397
The purification, cloning and expression of a novel luteinizing hormone-induced mitochondrial protein in MA-10 mouse Leydig tumor cells. Characterization of the steroidogenic acute regulatory protein (StAR)
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
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
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
Steroidogenic factor I, a key regulator of steroidogenic enzyme expression, is the mouse homolog of fushi tarazu-factor I
Lala, D. S. (1992) · Molecular Endocrinology · doi:10.1210/me.6.8.1249 · Cited by 678
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
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
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
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
Studies on ACTH action in perfused bovine adrenals: The site of action of ACTH in corticosteroidogenesis
Stone, D. A., & Hechter, O. (1954) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(54)90501-9 · Cited by 443

Show all 51 references

Research works printed but not linked: 3

Mapes, 1999, J. Clin. Endocrinol. Metab., 84, 3382
McNutt, 1970, Observations on the ultrastructure of cytodifferntiation in the human fetal adrenal cortex, Lab. Invest., 11, 513
Mesiano, 1993, J. Clin. Endocrinol. Metab., 77, 1184

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Aus der Medizinischen Klinik und Poliklinik I der
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Bouvattier, C. M. (2012)

Authors: Narasaka, T., Suzuki, T., Moriya, T., & Sasano, H.
Affiliations: Tohoku University (JP)
Corresponding author: Narasaka, Toshiaki
ORCID: Suzuki, Takashi
Moriya, Takuya
Sasano, Hironobu
Venue: Molecular and Cellular Endocrinology
Publisher: Elsevier BV
Published: 2001-03
Volume: 174
Issue: 1-2
Pages: 111-120
ISSN: 0303-7207 (ISSN-L)
DOI: 10.1016/s0303-7207(00)00445-7
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
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
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
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › 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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Temporal and spatial distribution of Corticosteroidogenic Enzymes Immunoreactivity in developing human adrenal

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