The hormonal-control of sexual development

Wilson, Jean D.; George, Fredrick W.; Griffin, James E.

doi:10.1126/science.7010602

Cited by 451Sexual Differentiation and DisordersGenetic and Clinical Aspects of Sex Determination and Chromosomal AbnormalitiesUrological Disorders and Treatments

The hormonal-control of sexual development

Wilson, Jean D., George, Fredrick W., Griffin, James E.·1981·Science

DOI 10.1126/science.7010602

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Abstract

Male and female human embryos develop identically during the first phase of gestation. The indifferent gonads then differentiate into ovaries or testes and soon begin to secrete their characteristic hormones. If ovaries (or no gonads) are present the final phenotype is female; thus no gonadal hormones are required for female development during embryogenesis. Two hormones of the fetal testis—Müllerian regression hormone and testosterone—are responsible for the formation of the male phenotype. Analysis of fibroblasts from the skin of patients with abnormalities of sexual development due to single gene defects shows that testosterone is responsible for virilization of the male internal genital tract, that its derivative dihydrotestosterone causes development of the male external genitalia, and that both hormones act in the embryo by the same receptor mechanisms operative in postnatal life.

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Masculinization of the external genitalia in humans depends on formation of 5α-dihydrotestosterone (DHT) through both the canonical androgenic pathway and an alternative (backdoor) pathway.
“Masculinization of the external genitalia in humans is dependent on formation of 5α-dihydrotestosterone (DHT) through both the canonical androgenic pathway and an alternative (backdoor) pathway.”
From Alternative (backdoor) androgen production and masculinization in the human fetus (2019) · cites this paper as [10]
Conversion of testosterone to DHT at the target organ leads to masculinization of the external genitalia.
“However, it is conversion of testosterone to the more potent 5α-dihydrotestosterone (DHT) at the target organ that leads to masculinization of the external genitalia [10].”
From Alternative (backdoor) androgen production and masculinization in the human fetus (2019) · cites this paper as [10]

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Mullerian Inhibiting Substance Activity in Bovine Fetal, Newborn and Prepubertal Testes1
Donahoe, P. K., Ito, Y., Price, J. M., & Hendren, W. H. (1977) · Biology of Reproduction · doi:10.1095/biolreprod16.2.238 · Cited by 85 · see citing works
Estrogen Formation by the Ovary of the Rabbit Embryo
Milewich, L., George, F. W., & Wilson, J. D. (1977) · Endocrinology · doi:10.1210/endo-100-1-187 · Cited by 83 · see citing works
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Gonadal dysgenesis in individuals with apparently normal chromosomal complements: tabulation of cases and compilation of genetic data.
Simpson, J. L., Christakos, A. C., Horwith, M., & Silverman, F. S. (1971) · PubMed · Cited by 82 · see citing works
Mechanisms of Gonadal Differentiation
Haseltine, F. P., & Ohno, S. (1981) · Science · doi:10.1126/science.7010601 · Cited by 81 · see citing works
In vitro analysis of the hormonal basis for the sexual dimorphism in the embryonic development of the mouse mammary gland
Kratochwil, K. (1971) · Development · doi:10.1242/dev.25.1.141 · Cited by 81 · see citing works
H-Y Antigen: Behavior and Function
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Mullerian Inhibiting Substance: An Update
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Congenital malformations in twins: epidemiologic survey.
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The androgen insensitive mouse: Absence of intranuclear androgen retention in the kidney
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Correlation of early cytodifferentiation of the human fetal prostate and leydig cells
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Two XY Siblings with Gonadal Dysgenesis and a Female Phenotype
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Biosynthesis of labelled anti-müllerian hormone by fetal testes: Evidence for the glycoprotein nature of the hormone and for its disulfide-bonded structure
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Estrogen inhibition of mullerian inhibiting substance in the chick embryo
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Studies on the Regulation of Testosterone Synthesis in the Fetal Rabbit Testis*
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EFFECTS OF OESTRADIOL-17β, OESTRADIOL BENZOATE AND THE SYNTHETIC OESTROGEN RU 2858 ON SEXUAL DIFFERENTIATION IN THE NEONATAL FEMALE RAT
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Developmental Pattern of Testosterone Synthesis in the Fetal Gonad of the Rabbit
Wilson, J. D., & Siiteri, P. K. (1973) · Endocrinology · doi:10.1210/endo-92-4-1182 · Cited by 69 · see citing works
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Genetic aspects of H-Y antigen
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Gonadotropin and Testosterone Measurements after Estrogen Administration to Adult Men, Prepubertal and Pubertal Boys, and Men with Hypogonadotropism: Evidence for Maturation of Positive Feedback in the Male
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Testosterone Synthesis by the Fetal Rabbit Gonad
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Clinical and Endocrinologic Characterization of a Patient with the Syndrome of Incomplete Testicular Feminization
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Mammalian Gonadal Determination and Gametogenesis
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Familial XY gonadal dysgenesis.
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Biological Activities of a New Steroidal Inhibitor of 4-5 -Reductase
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On the Role of Sex Hormones in Sex Differentiation in the Opossum (Didelphys virginiana)
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Sex differentiation during the early pouch stages of the opossum (Didelphys virginiana) and a comparison of the anatomical changes induced by male and female sex hormones
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Aromatase Activity in the Developing Rabbit Brain*
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Human Chorionic Gonadotropin Binding to Human Fetal Testes as a Function of Gestational Age*
MOLSBERRY, R. L., Carr, B. R., Mendelson, C. R., & SIMPSON, E. B. (1982) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-55-4-791 · Cited by 53 · see citing works
MULTIPLE ACTIVITIES OF ANDROGENIC COMPOUNDS
Deanesly, R., & Parkes, A. S. (1937) · Quarterly journal of experimental physiology · doi:10.1113/expphysiol.1937.sp000730 · Cited by 52 · see citing works
Studies on the Regulation of the Onset of Steroid Hormone Biosynthesis in Fetal Rabbit Gonads*
George, F. W., Simpson, E. R., Milewich, L., & Wilson, J. D. (1979) · Endocrinology · doi:10.1210/endo-105-5-1100 · Cited by 51 · see citing works
Self-citation
The HLA-dependent expression of testis-organizing H-Y antigen by human male cells
Beutler, B., Nagai, Y., Ohno, S., Klein, G., & Shapiro, I. M. (1978) · Cell · doi:10.1016/0092-8674(78)90324-0 · Cited by 50 · see citing works
Role of testosterone binding to the androgen receptor in male sexual differentiation of patients with 5α-reductase deficiency
Maes, M., Sultan, C., Zerhouni, N., Rothwell, S. W., & Migeon, C. J. (1979) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(79)90110-9 · Cited by 49 · see citing works
Role of oestrogen receptor in androgen-induced sexual differentiation of the brain
Westley, B. R., & SALAMAN, D. F. (1976) · Nature · doi:10.1038/262407a0 · Cited by 49 · see citing works
Increased estrogen formation and aromatase activity in fibroblasts cultured from the skin of chickens with the Henny feathering trait.
Leshin, M., Baron, J., George, F. W., & Wilson, J. D. (1981) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)69439-1 · Cited by 47 · see citing works
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Genetic regulation of thermostability of mouse submaxillary gland renin.
Wilson, C. M., & Taylor, B. A. (1982) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)68348-1 · Cited by 45 · see citing works
Oestrogen content of the embryonic rabbit ovary
George, F. W., Milewich, L., & Wilson, J. D. (1978) · Nature · doi:10.1038/274172a0 · Cited by 43 · see citing works
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Estrogens and the Human Male
Marcus, R., & Korenman, S. G. (1976) · Annual Review of Medicine · doi:10.1146/annurev.me.27.020176.002041 · Cited by 43 · see citing works
Role of Testosterone and its Metabolites in the Differentiation of the Mammary Gland in Rats
Goldman, A. S., Shapiro, B. H., & Neumann, F. (1976) · Endocrinology · doi:10.1210/endo-99-6-1490 · Cited by 42 · see citing works
pathogenesis of the henny feathering trait in the Sebright bantam chicken. Increased conversion of androgen to estrogen in skin.
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A new structural variant of glucose-6-phosphate dehydrogenase with a high production rate (G6PD Hektoen).
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Does "Blastocyst Estrogen" Initiate Implantation?
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Evidence for a gonad-specific receptor for H-Y antigen: Binding of exogenous H-Y antigen to gonadal cells is independent of β2-microglobulin
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Steroid enhancement of mullerian duct regression
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INHIBITION, BY THE ANTI-OESTROGEN MER-25, OF DEFEMINIZATION INDUCED BY THE SYNTHETIC OESTROGEN RU 2858
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A light and electron microscopic study of Rathke's pouch in fetal rabbits
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The Role of H-Y Antigen in Primary Sex Determination
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A Monoclonal Antibody against Bovine Anti-Müllerian Hormone*
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Classification of hereditary disorders of sexual development.
Wilson, J. D., & Goldstein, J. L. (1975) · PubMed · Cited by 31 · see citing works
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A SENSITIVE RADIOIMMUNOASSAY FOR BOVINE ANTI-MŰML;LLERIAN HORMONE, ALLOWING ITS DETECTION IN MALE AND FREEMARTIN FETAL SERUM
Vigier, B., Legeai‐Mallet, L., Picard, J., & Josso, N. (1982) · Endocrinology · doi:10.1210/endo-111-4-1409 · Cited by 30 · see citing works
Anovulation in adult female rats after neonatal intracerebral implantation of oestrogen.
Döcke, F., & Dörner, G. (1975) · PubMed · Cited by 28 · see citing works
Prostatic function in the brush-tailed possum, Trichosurus vulpecula
Cook, B., McDonald, I. R., & Gibson, W. R. (1978) · Reproduction · doi:10.1530/jrf.0.0530369 · Cited by 27 · see citing works
Hereditary Male Pseudohermaphroditism
Griffin, J. E., & Wilson, J. D. (1978) · Clinics in Obstetrics and Gynaecology · doi:10.1016/s0306-3356(21)00437-4 · Cited by 27 · see citing works
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Inhibition of masculine differentiation in male offspring of rabbits actively immunised against testosterone before pregnancy
BIDLINGMAIER, F., Knorr, D., & Neumann, F. (1977) · Nature · doi:10.1038/266647a0 · Cited by 26 · see citing works
THE ENDOCRINE SECRETION OF HEN-FEATHERED FOWLS
Morgan, T. H. (1920) · Endocrinology · doi:10.1210/endo-4-3-381 · Cited by 25 · see citing works
Female Feathering in Sebright Cocks Is Due to Conversion of Testosterone to Estradiol in Skin
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Developmental changes of the hypogastric ganglion associated with the differentiation of the reproductive tracts in the mouse
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The secretion of mullerian inhibiting substance by cultured isolated sertoli cells of the neonatal calf
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Endocrine differentiation of the fetal rabbit ovary in culture
George, F. W., & Wilson, J. D. (1980) · Nature · doi:10.1038/283861a0 · Cited by 24 · see citing works
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Sex Hormones and Sexual Behavior
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Androgens and Erythropoiesis
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Inhibition of steroid 5α-reductase from human skin fibroblasts by 17β-N, N-diethylcarbamoyl-4-methyl-4-aza-5α-androstan-3-one
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THE ANDROGENS IN THE GUINEA-PIG FOETUS THROUGHOUT THE EMBRYONIC DEVELOPMENT
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Production of Hypospadias in the Rat by Selective Inhibition of Fetal Testicular 17α-Hydroxylase and C 17-20 -lyase
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Developmental Pattern of Increased Aromatase Activity in the Sebright Bantam Chicken*
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Chromosomes and Human Disease
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DAS EMBRYONALE UND POSTNATALE VERHALTEN DER MÄNNLICHEN BRUSTDRÜSE BEIM MENSCHEN. II.
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Testosterone Metabolism in Skin
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Effect of 5α-Dihydrotestosterone on Differentiation of Masculine Pattern of the Brain in the Rat
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AN EXPERIMENT ON THE COMPLETE TRANSFORMATION OF THE SCROTUM INTO A MARSUPIAL POUCH IN TRICHOSURUS VULPECULA
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The genetics of sex determination in man
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Increased estrogen synthesis in the Sebright bantam is due to a mutation that causes increased aromatase activity.
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Relation of the Follicular Hormone to Feather Form and Pattern in the Fowl.
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Demonstration of the effects of castration on Seabright cockerels
Morgan, T. H. (1917) · Experimental Biology and Medicine · doi:10.3181/00379727-15-107 · Cited by 7 · see citing works
Testicular Hormones and Sebright Plumage.
Danforth, C. H. (1935) · Experimental Biology and Medicine · doi:10.3181/00379727-32-8141c · Cited by 5 · see citing works

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Testosterone and dominance in men
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Androgen Receptor Defects: Historical, Clinical, and Molecular Perspectives*
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Human behavioral sex differences: A role for gonadal hormones during early development?
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Factor Analysis Shows That Female Rat Behaviour Is Characterized Primarily by Activity, Male Rats Are Driven by Sex and Anxiety
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Prenatal endocrine influences on sexual orientation and on sexually differentiated childhood behavior
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A BIPHASIC MODEL FOR THE HORMONAL CONTROL OF TESTICULAR DESCENT
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Primary genetic control of somatic sexual differentiation in a mammal
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Testosterone during Pregnancy and Gender Role Behavior of Preschool Children: A Longitudinal, Population Study
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Histological and ultrastructural evidence for the role of gonadal steroid hormones in sex change in the protogynous wrasse Thalassoma duperrey
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Cancer Risk in Men Exposed In Utero to Diethylstilbestrol
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Sex steroid profiles of coho salmon (Oncorhynchus kisutch) during early development and sexual differentiation
Feist, G. W., Schreck, C. B., Fitzpatrick, M. S., & Redding, J. M. (1990) · General and Comparative Endocrinology · doi:10.1016/0016-6480(90)90174-k · Cited by 189 · see citing works
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Alternative (backdoor) androgen production and masculinization in the human fetus
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DIABETIC SEXUAL DYSFUNCTION
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Self-citation
Sex Differences Are Here to Stay: Relevance to Prenatal Care
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Authors: Wilson, J. D., George, F. W., & Griffin, J. E.
Affiliations: The University of Texas Southwestern Medical Center (US)
ORCID: Griffin, James E.
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 1981-03-20
Volume: 211
Issue: 4488
Pages: 1278-1284
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.7010602
OpenAlex: W2112600512
Cited by: 451
References: 167
Citations by year: 2026: 3 · 2025: 7 · 2024: 6 · 2023: 9 · 2022: 4 · 2021: 4 · 2020: 12 · 2019: 11 · 2018: 11 · 2017: 10 · 2016: 12 · 2015: 6 · 2014: 7 · 2013: 10 · 2012: 7
FWCI: 1.83
Type: journal article
Language: en
Open access: closed
Locations: Science (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
Health Sciences › Medicine › Urology › Urological Disorders and Treatments
Keywords: sexual development, gonadal differentiation, testosterone, dihydrotestosterone, sex determination, external genitalia development, masculinization, sex chromosome abnormalities, hormone receptors, embryonic development
MeSH terms: Animals, Estradiol, Female, Glycoproteins, Gonadotropins, Growth Inhibitors, Humans, Male, Morphogenesis, Mullerian Ducts, Ovary, Rabbits, Receptors, Androgen, Sex Differentiation, Testicular Hormones, Testis, Testosterone, Time Factors, Urogenital System, Wolffian Ducts, Anti-Mullerian Hormone

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The hormonal-control of sexual development

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