Estrogen Resistance Caused by a Mutation in the Estrogen-Receptor Gene in a Man
Open accessAbstract
BACKGROUND AND METHODS: Mutations in the estrogen-receptor gene have been thought to be lethal. A 28-year-old man whose estrogen resistance was caused by a disruptive mutation in the estrogen-receptor gene underwent studies of pituitary-gonadal function and bone density and received transdermal estrogen for six months. Estrogen-receptor DNA, extracted from lymphocytes, was evaluated by analysis of single-strand-conformation polymorphisms and by direct sequencing. RESULTS: The patient was tall (204 cm [80.3 in.]) and had incomplete epiphyseal closure, with a history of continued linear growth into adulthood despite otherwise normal pubertal development. He was normally masculinized and had bilateral axillary acanthosis nigricans. Serum estradiol and estrone concentrations were elevated, and serum testosterone concentrations were normal. Serum follicle-stimulating hormone and luteinizing hormone concentrations were increased. Glucose tolerance was impaired, and hyperinsulinemia was present. The bone mineral density of the lumbar spine was 0.745 g per square centimeter, 3.1 SD below the mean for age-matched normal women; there was biochemical evidence of increased bone turnover. The patient had no detectable response to estrogen administration, despite a 10-fold increase in the serum free estradiol concentration. Conformation analysis of his estrogen-receptor gene revealed a variant banding pattern in exon 2. Direct sequencing of exon 2 revealed a cytosine-to-thymine transition at codon 157 of both alleles, resulting in a premature stop codon. The patient's parents were heterozygous carriers of this mutation, and pedigree analysis revealed consanguinity. CONCLUSIONS: Disruption of the estrogen receptor in humans need not be lethal. Estrogen is important for bone maturation and mineralization in men as well as women.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
One patient with a mutation in ESR1 had a BMI in the obese range of 30 kg/m2 and clinical evidence of insulin resistance, although fat mass was not reported.
“One patient had a BMI in the obese range of 30 kg/m2 and clinical evidence of insulin resistance, 196 although fat mass was not reported.”
From The role of the androgen receptor in the pathogenesis of obesity and its utility as a target for obesity treatments (2022) · cites this paper as [196]
Cites
RADIOGRAPHIC ATLAS OF SKELETAL DEVELOPMENT OF THE HAND AND WRIST
GREULICH, W. W., & Pyle, S. I. (1959) · The American Journal of the Medical Sciences · doi:10.1097/00000441-195909000-00030 · Cited by 5,598 · see citing works
Orita, M., Suzuki, Y., Sekiya, T., & Hayashi, K. (1989) · Genomics · doi:10.1016/0888-7543(89)90129-8 · Cited by 3,433 · see citing works
Lubahn, D. B., Moyer, J. S., GOLDING, T. S., Couse, J. F., Korach, K. S., & Smithies, O. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.23.11162 · Cited by 1,901 · see citing works
Self-citationHanson, D. A., Weis, M. A., Bollen, A., Maslan, S., Singer, F. R., & Eyre, D. W. (1992) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650071119 · Cited by 653 · see citing works
Genomic organization of the human oestrogen receptor gene.
Ponglikitmongkol, M., Green, S., & Chambon, P. (1988) · The EMBO Journal · doi:10.1002/j.1460-2075.1988.tb03211.x · Cited by 485 · see citing works
Osteopenia in Men with a History of Delayed Puberty
Finkelstein, J. S., Neer, R. M., Biller, B. M. K., Crawford, J. D., & Klibanski, A. (1992) · New England Journal of Medicine · doi:10.1056/nejm199202273260904 · Cited by 436 · see citing works
Osteoporosis in Men with Idiopathic Hypogonadotropic Hypogonadism
Finkelstein, J. S., KLIBANSKI, A., NEER, R. M., GREENSPAN, S. L., ROSENTHAL, D. I., & CROWLEY, W. F. (1987) · Annals of Internal Medicine · doi:10.7326/0003-4819-106-3- · Cited by 407 · see citing works
Conte, F. A., Grumbach, M. M., Ito, Y., Fisher, C. R., & Simpson, E. R. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.78.6.8200927 · Cited by 379 · see citing works
Vitamin-D-Dependent Rickets Type II
Brooks, M. H., Bell, N. H., Love, L., Stern, P. H., Orfei, E., Queener, S. F., Hamstra, A. J., & DeLuca, H. F. (1978) · New England Journal of Medicine · doi:10.1056/nejm197805042981804 · Cited by 346 · see citing works
Origin of Estrogen in Normal Men and in Women with Testicular Feminization*
MacDonald, P. C., Madden, J. D., Brenner, P. F., Wilson, J. D., & Siiteri, P. K. (1979) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-49-6-905 · Cited by 320 · see citing works
Barbieri, R. L., & Ryan, K. J. (1983) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(83)90091-1 · Cited by 295 · see citing works
A New Cause of Female Pseudohermaphroditism: Placental Aromatase Deficiency
Shozu, M., Akasofu, K., HARADA, T., & Kubota, Y. (1991) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-72-3-560 · Cited by 287 · see citing works
Syndromes of Glucocorticoid Resistance
Chrousos, G. P., Detera-Wadleigh, S. D., & Karl, M. (1993) · Annals of Internal Medicine · doi:10.7326/0003-4819-119-11-199312010-00009 · Cited by 235 · see citing works
Ito, Y., Fisher, C. R., Conte, F. A., Grumbach, M. M., & Simpson, E. R. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.24.11673 · Cited by 218 · see citing works
Seibel, M. J., Robins, S. P., & Bilezikian, J. P. (1992) · Trends in Endocrinology and Metabolism · doi:10.1016/1043-2760(92)90129-o · Cited by 175 · see citing works
ZACHMANN, M., Prader, A., Sobel, E. H., Crigler, J. F., Ritzén, E. M., Atares, M., & Ferrandez, A. (1986) · The Journal of Pediatrics · doi:10.1016/s0022-3476(86)81043-5 · Cited by 141 · see citing works
Brown, T. R., Lubahn, D. B., Wilson, E., French, F. S., Migeon, C. J., & Corden, J. L. (1990) · Molecular Endocrinology · doi:10.1210/mend-4-12-1759 · Cited by 125 · see citing works
Self-citationTreatment of Familial Male Precocious Puberty with Spironolactone and Testolactone
Laue, L., Kenigsberg, D., Pescovitz, O. H., HENCH, K. D., Barnes, K. M., Loriaux, D. L., & Cutler, G. B. (1989) · New England Journal of Medicine · doi:10.1056/nejm198902233200805 · Cited by 119 · see citing works
Osteoporosis and Decline of Gonadal Function in the Elderly Male
Foresta, C., Ruzza, G., Mioni, R., Guarner, G., Gribaldo, R., Meneghello, A., & Mastrogiacomo, I. (1984) · Hormone Research · doi:10.1159/000179855 · Cited by 100 · see citing works
Sex Determination and Differentiation
Swain, A., & Lovell-Badge, R. H. (2002) · Elsevier eBooks · doi:10.1016/b978-012597951-1/50021-4 · Cited by 99 · see citing works
CLINICAL REVIEW 14 Pathophysiology and Treatment of Sexual Precocity
Kaplan, S. L., & GRUMBACH, M. M. (1990) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-71-4-785 · Cited by 98 · see citing works
Inhibition of estrogen biosynthesis and its consequences on gonadotrophin secretion in the male
Bhatnagar, A. S., Müller, P., Schenkel, L., et al. (1992) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/0960-0760(92)90369-t · Cited by 55 · see citing works
Analysis of oncogene alterations in human endometrial carcinoma: Prevalence of ras mutations
Boyd, J. A., & Risinger, J. I. (1991) · Molecular Carcinogenesis · doi:10.1002/mc.2940040305 · Cited by 53 · see citing works
Self-citationLeiter, E. H., Beamer, W. G., Coleman, D. L., & Longcope, C. (1987) · Metabolism · doi:10.1016/0026-0495(87)90095-3 · Cited by 50 · see citing works
Thyroid hormone resistance syndromes
McDermott, M. T., & Ridgway, E. C. (1993) · The American Journal of Medicine · doi:10.1016/0002-9343(93)90155-i · Cited by 49 · see citing works
Anabolic steroids and osteoporosis
Dequeker, J., & Geusens, P. P. M. M. (1985) · European Journal of Endocrinology · doi:10.1530/acta.0.109s0045 · Cited by 37 · see citing works
Male Hypogonadism and Bone Fracture
Swartz, C. M., & Young, M. A. (1988) · New England Journal of Medicine · doi:10.1056/nejm198804143181517 · Cited by 26 · see citing works
Carlström, K., Collste, L., Eriksson, A., et al. (1989) · The Prostate · doi:10.1002/pros.2990140210 · Cited by 22 · see citing works
Valenta, L. J., Elias, A. N., & Domurat, E. S. (1992) · PubMed Central · Cited by 17 · see citing works
Prochazka, M., Premdas, F. H., Leiter, E. H., et al. (1986) · Diabetes · doi:10.2337/diabetes.35.6.725 · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Sex and Gender Differences in Risk, Pathophysiology and Complications of Type 2 Diabetes Mellitus
Kautzky-Willer, A., Harreiter, J., & Pacini, G. (2016) · Endocrine Reviews · doi:10.1210/er.2015-1137 · Cited by 2,043 · see citing works
Estrogen Receptor Null Mice: What Have We Learned and Where Will They Lead Us?
Couse, J. F., & Korach, K. S. (1999) · Endocrine Reviews · doi:10.1210/edrv.20.3.0370 · Cited by 2,045 · see citing works
Self-citationSex Steroids and the Construction and Conservation of the Adult Skeleton
Riggs, B. L., Khosla, S., & Melton, L. J. (2002) · Endocrine Reviews · doi:10.1210/edrv.23.3.0465 · Cited by 1,846 · see citing works
The role of estrogens in control of energy balance and glucose homeostasis
Mauvais-Jarvis, F., Clegg, D. J., & Hevener, A. L. (2013) · Endocrine Reviews · doi:10.1210/er.2012-1055 · Cited by 1,329 · see citing works
Increased adipose tissue in male and female estrogen receptor-α knockout mice
Heine, P. A., Taylor, J. A., Iwamoto, G. A., Lubahn, D. B., & Cooke, P. S. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.23.12729 · Cited by 1,282 · see citing works
Self-citationAge-Associated Increased Interleukin-6 Gene Expression, Late-Life Diseases, and Frailty
Ershler, W. B., & Keller, E. T. (2000) · Annual Review of Medicine · doi:10.1146/annurev.med.51.1.245 · Cited by 1,282 · see citing works
Effect of testosterone and estradiol in a man with aromatase deficiency
Carani, C., Qin, K., Simoni, M., Faustini-Fustini, M., Serpente, S., Boyd, J., Korach, K. S., & Simpson, E. R. (1997) · New England Journal of Medicine · doi:10.1056/nejm199707103370204 · Cited by 1,151 · see citing works
Self-citationEstrogen Prevents Bone Loss via Estrogen Receptor α and Induction of Fas Ligand in Osteoclasts
Nakamura, T., Imai, Y., Matsumoto, T., Sato, S., Takeuchi, K., Igarashi, K., Harada, Y., Azuma, Y., Krust, A., Yamamoto, Y., et al. (2007) · Cell · doi:10.1016/j.cell.2007.07.025 · Cited by 1,013 · see citing works
Couse, J. F., Lindzey, J., Grandien, K., Gustafsson, J.-A., & Korach, K. S. (1997) · Endocrinology · doi:10.1210/endo.138.11.5496 · Cited by 978 · see citing works
Self-citationSources of estrogen and their importance
Simpson, E. R. (2003) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(03)00360-1 · Cited by 936 · see citing works
The G-protein-coupled estrogen receptor GPER in health and disease
Prossnitz, E. R., & Barton, M. (2011) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2011.122 · Cited by 925 · see citing works
“in men lead to osteopenia, enhanced bone remodeling through increased bone resorption and osteoclast activity and suppression of bone growth-plate closure”
BackgroundGender differences in insulin resistance, body composition, and energy balance
Geer, E. B., & Shen, W. (2009) · Gender Medicine · doi:10.1016/j.genm.2009.02.002 · Cited by 913 · see citing works
Pathogenesis of bone fragility in women and men
Seeman, E. (2002) · The Lancet · doi:10.1016/s0140-6736(02)08706-8 · Cited by 909 · see citing works
Estrogens and androgens in skeletal physiology and pathophysiology
Almeida, M., Laurent, M. R., Dubois, V., Claessens, F., O'Brien, C. A., Bouillon, R., Vanderschueren, D., & Manolagas, S. C. (2017) · Physiological Reviews · doi:10.1152/physrev.00033.2015 · Cited by 860 · see citing works
Estrogen production and action
Nelson, L. R., & Bulun, S. E. (2001) · Journal of the American Academy of Dermatology · doi:10.1067/mjd.2001.117432 · Cited by 834 · see citing works
Simpson, E. R., Clyne, C., Rubin, G., Boon, W. C., Robertson, K., Britt, K., Speed, C., & Jones, M. (2002) · Annual Review of Physiology · doi:10.1146/annurev.physiol.64.081601.142703 · Cited by 773 · see citing works
Falahati-Nini, A., Riggs, B. L., Atkinson, E. J., O’Fallon, W. M., Eastell, R., & Khosla, S. (2000) · Journal of Clinical Investigation · doi:10.1172/jci10942 · Cited by 757 · see citing works
Vanderschueren, D., Vandenput, L., Boonen, S., Lindberg, M. K., Bouillon, R., & Ohlsson, C. (2004) · Endocrine Reviews · doi:10.1210/er.2003-0003 · Cited by 717 · see citing works
Role of RANK ligand in mediating increased bone resorption in early postmenopausal women
Eghbali-Fatourechi, G., Khosla, S., Sanyal, A., Boyle, W. J., Lacey, D. L., & Riggs, B. L. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17215 · Cited by 825 · see citing works
Wang, C., Cunningham, G., Dobs, A., Iranmanesh, A., Matsumoto, A. M., Snyder, P. J., Weber, T., Berman, N., Hull, L., & Swerdloff, R. S. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-032006 · Cited by 656 · see citing works
Osteoporosis in Men: An Endocrine Society Clinical Practice Guideline
Watts, N. B., Adler, R. A., Bilezikian, J. P., Drake, M. T., Eastell, R., Orwoll, E. S., & Finkelstein, J. S. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-3045 · Cited by 611 · see citing works
Distinct Hypothalamic Neurons Mediate Estrogenic Effects on Energy Homeostasis and Reproduction
Xu, Y., Nedungadi, T. P., Zhu, L., Sobhani, N., Irani, B. G., Davis, K. E., Zhang, X., Zou, F., Gent, L. M., Hahner, L. D., et al. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.08.009 · Cited by 597 · see citing works
International Union of Pharmacology. LXIV. Estrogen Receptors
Dahlman-Wright, K., Cavailles, V., Fuqua, S. A., Jordan, V. C., Katzenellenbogen, J. A., Korach, K. S., Maggi, A., Muramatsu, M., Parker, M. G., & Gustafsson, J.-Å. (2006) · Pharmacological Reviews · doi:10.1124/pr.58.4.8 · Cited by 583 · see citing works
Self-citationAbbott, D. H., Barnett, D. K., Bruns, C. M., & Dumesic, D. A. (2005) · Human Reproduction Update · doi:10.1093/humupd/dmi013 · Cited by 555 · see citing works
Long-term effect of testosterone therapy on bone mineral density in hypogonadal men
Behre, H. M., Kliesch, S., Leifke, E., Link, T. M., & Nieschlag, E. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.8.4163 · Cited by 559 · see citing works
Andropause: clinical implications of the decline in serum testosterone levels with aging in men
Matsumoto, A. M. (2002) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/57.2.m76 · Cited by 490 · see citing works
Amory, J. K., Watts, N. B., Easley, K. A., Sutton, P. R., Anawalt, B. D., Matsumoto, A. M., Bremner, W. J., & Tenover, J. L. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031110 · Cited by 475 · see citing works
Obesity and androgens: facts and perspectives
Pasquali, R. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.10.054 · Cited by 469 · see citing works
Estrogen Receptors and the Metabolic Network
Barros, R. P. A., & Gustafsson, J.-Å. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.08.005 · Cited by 458 · see citing works
Epigenetic Transgenerational Actions of Endocrine Disruptors
Anway, M. D., & Skinner, M. K. (2006) · Endocrinology · doi:10.1210/en.2005-1058 · Cited by 455 · see citing works
Slemenda, C. W., Longcope, C., Zhou, L., Hui, S. L., Peacock, M., & Johnston, C. C. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119701 · Cited by 455 · see citing works
Endocrine Control of Body Composition in Infancy, Childhood, and Puberty
Veldhuis, J. D., Roemmich, J. N., Richmond, E. J., Rogol, A. D., Lovejoy, J. C., Sheffield-Moore, M., Mauras, N., & Bowers, C. Y. (2005) · Endocrine Reviews · doi:10.1210/er.2003-0038 · Cited by 452 · see citing works
Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice
Riant, E., Waget, A., Cogo, H., Arnal, J.-F., Burcelin, R., & Gourdy, P. (2009) · Endocrinology · doi:10.1210/en.2008-0971 · Cited by 421 · see citing works
The role of estradiol in male reproductive function
Ramasamy, R., Schulster, M., & Bernie, A. (2016) · Asian Journal of Andrology · doi:10.4103/1008-682x.173932 · Cited by 411 · see citing works
Mechanisms of sex steroid effects on bone
Syed, F., & Khosla, S. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.11.097 · Cited by 380 · see citing works
Snyder, P. J., Kopperdahl, D. L., Stephens-Shields, A. J., Ellenberg, S. S., Cauley, J. A., Ensrud, K. E., Lewis, C. E., Barrett-Connor, E., Schwartz, A. V., Lee, D. C., et al. (2017) · JAMA Internal Medicine · doi:10.1001/jamainternmed.2016.9539 · Cited by 363 · see citing works
Mauvais-Jarvis, F. (2011) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2010.10.002 · Cited by 335 · see citing works
Obesity and Disturbed Lipoprotein Profile in Estrogen Receptor-α-Deficient Male Mice
Ohlsson, C., Hellberg, N., Parini, P., Vidal, O., Bohlooly, M., Rudling, M., Lindberg, M. K., Warner, M., Angelin, B., & Gustafsson, J.-Å. (2000) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2000.3827 · Cited by 332 · see citing works
Sex Steroid Actions in Male Bone
Vanderschueren, D., Laurent, M. R., Claessens, F., Gielen, E., Lagerquist, M. K., Vandenput, L., Börjesson, A. E., & Ohlsson, C. (2014) · Endocrine Reviews · doi:10.1210/er.2014-1024 · Cited by 327 · see citing works
Androgens, insulin resistance and vascular disease in men
Kapoor, D., Malkin, C. J., Channer, K. S., & Jones, T. H. (2005) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2005.02299.x · Cited by 317 · see citing works
Ribas, V., Nguyen, M. T. A., Henstridge, D. C., Nguyen, A.-K., Beaven, S. W., Watt, M. J., & Hevener, A. L. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00504.2009 · Cited by 309 · see citing works
Estrogen and the Male Skeleton
Khosla, S., Melton, L. J., & Riggs, B. L. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.4.8417 · Cited by 308 · see citing works
Lundsgaard, A.-M., & Kiens, B. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00195 · Cited by 289 · see citing works
Kalervo Väänänen, H., & Härkönen, P. L. (1996) · Maturitas · doi:10.1016/0378-5122(96)01015-8 · Cited by 293 · see citing works
Differential Effects of Androgens and Estrogens on Bone Turnover in Normal Men
Leder, B. Z., LeBlanc, K. M., Schoenfeld, D. A., Eastell, R., & Finkelstein, J. S. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021036 · Cited by 283 · see citing works
Growth hormone therapy of Turner's syndrome: beneficial effect on adult height
Rosenfeld, R. G., Attie, K. M., Frane, J., Brasel, A., Burstein, S., Cara, J. F., Chernausek, S., Gotlin, R. W., Kuntze, J., Lippe, B. M., et al. (1998) · The Journal of Pediatrics · doi:10.1016/s0022-3476(98)70452-4 · Cited by 265 · see citing works
Estrogen—the Good, the Bad, and the Unexpected
Simpson, E. R., Misso, M., Hewitt, K. N., Hill, R. A., Boon, W. C., Jones, M. E., Kovacic, A., Zhou, J., & Clyne, C. D. (2005) · Endocrine Reviews · doi:10.1210/er.2004-0020 · Cited by 266 · see citing works
The role of local estrogen Biosynthesis in males and females
Simpson, E., Rubin, G., Clyne, C., Robertson, K., O’Donnell, L., Jones, M., & Davis, S. (2000) · Trends in Endocrinology & Metabolism · doi:10.1016/s1043-2760(00)00254-x · Cited by 249 · see citing works
Yialamas, M. A., Dwyer, A. A., Hanley, E., Lee, H., Pitteloud, N., & Hayes, F. J. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-0454 · Cited by 220 · see citing works
Estrogens Are Essential for Male Pubertal Periosteal Bone Expansion
Bouillon, R., Bex, M., Vanderschueren, D., & Boonen, S. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0602 · Cited by 200 · see citing works
Hero, M., Norjavaara, E., & Dunkel, L. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-1392 · Cited by 198 · see citing works
Gonadal steroid–dependent effects on bone turnover and bone mineral density in men
Finkelstein, J. S., Lee, H., Leder, B. Z., Burnett-Bowie, S.-A. M., Goldstein, D. W., Hahn, C. W., Hirsch, S. C., Linker, A., Perros, N., Servais, A. B., et al. (2016) · Journal of Clinical Investigation · doi:10.1172/jci84137 · Cited by 198 · see citing works
Of mice and men: the evolving phenotype of aromatase deficiency
Jones, M. E. E., Chin Boon, W., Proietto, J., & Simpson, E. R. (2006) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2006.01.004 · Cited by 193 · see citing works
Khosla, S., Atkinson, E. J., Dunstan, C. R., & O’Fallon, W. M. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.4.8397 · Cited by 191 · see citing works
Takeda, K., Toda, K., Saibara, T., Nakagawa, M., Saika, K., Onishi, T., Sugiura, T., & Shizuta, Y. (2003) · Journal of Endocrinology · doi:10.1677/joe.0.1760237 · Cited by 182 · see citing works
Estrogens in adipose tissue physiology and obesity-related dysfunction
Kuryłowicz, A. (2023) · Biomedicines · doi:10.3390/biomedicines11030690 · Cited by 178 · see citing works
The role of androgens in male gender role behavior
Wilson, J. D. (1999) · Endocrine Reviews · doi:10.1210/edrv.20.5.0377 · Cited by 172 · see citing works
Quigley, C. A., Crowe, B. J., Anglin, D. G., & Chipman, J. J. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.5.8477 · Cited by 159 · see citing works
Participation of ERα and ERβ in glucose homeostasis in skeletal muscle and white adipose tissue
Barros, R. P. A., Gabbi, C., Morani, A., Warner, M., & Gustafsson, J.-Å. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00189.2009 · Cited by 155 · see citing works
Shirtcliff, E. A., Granger, D. A., Schwartz, E. B., Curran, M. J., Booth, A., & Overman, W. H. (2000) · Hormones and Behavior · doi:10.1006/hbeh.2000.1614 · Cited by 149 · see citing works
Burnett-Bowie, S.-A. M., McKay, E. A., Lee, H., & Leder, B. Z. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-0739 · Cited by 146 · see citing works
Estrogen receptor-α in osteocytes is important for trabecular bone formation in male mice
Windahl, S. H., Börjesson, A. E., Farman, H. H., Engdahl, C., Movérare-Skrtic, S., Sjögren, K., Lagerquist, M. K., Kindblom, J. M., Koskela, A., Tuukkanen, J., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220811110 · Cited by 136 · see citing works
Hormone Replacement Therapy and Physical Function in Healthy Older Men. Time to Talk Hormones?
Giannoulis, M. G., Martin, F. C., Nair, K. S., Umpleby, A. M., & Sonksen, P. (2012) · Endocrine Reviews · doi:10.1210/er.2012-1002 · Cited by 132 · see citing works
Expression of oestrogen receptor-alpha and -beta in ovarian endometriomata
Fujimoto, J. (1999) · Molecular Human Reproduction · doi:10.1093/molehr/5.8.742 · Cited by 123 · see citing works
Gorres, B. K., Bomhoff, G. L., Morris, J. K., & Geiger, P. C. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2010.199018 · Cited by 116 · see citing works
Obesity in men: The hypogonadal–estrogen receptor relationship and its effect on glucose homeostasis
Cohen, P. G. (2008) · Medical Hypotheses · doi:10.1016/j.mehy.2007.05.020 · Cited by 115 · see citing works
Cross-sex pattern of bone mineral density in early onset gender identity disorder
Haraldsen, I. R., Haug, E., Falch, J., Egeland, T., & Opjordsmoen, S. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.05.012 · Cited by 113 · see citing works
Kim, J. H., Cho, H. T., & Kim, Y. J. (2014) · Endocrine Journal · doi:10.1507/endocrj.ej14-0262 · Cited by 111 · see citing works
Effect of estrogen deficiency in the male: the ArKO mouse model
Murata, Y., Robertson, K. M., Jones, M. E. E., & Simpson, E. R. (2002) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(02)00090-4 · Cited by 111 · see citing works
Movérare‐Skrtic, S., Venken, K., Andersson, N., Lindberg, M. K., Svensson, J., Swanson, C., Vanderschueren, D., Oscarsson, J., Gustafsson, J., & Ohlsson, C. (2006) · Obesity · doi:10.1038/oby.2006.75 · Cited by 111 · see citing works
Steroid Hormone Biosynthesis and Actions in the Materno Fetoplacental Unit
Miller, W. L. (1998) · Clinics in Perinatology · doi:10.1016/s0095-5108(18)30084-8 · Cited by 98 · see citing works
Osteopenia as a feature of the androgen insensitivity syndrome.
Soule, S. G., Conway, G., Prelevic, G. M., Prentice, M., Ginsburg, J., & Jacobs, H. S. (1995) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1995.tb00533.x · Cited by 99 · see citing works
Roselli, C. E., Klosterman, S., & Resko, J. A. (2001) · Journal of Comparative Neurology · doi:10.1002/cne.1343 · Cited by 91 · see citing works
Andropause: Symptom Management for Prostate Cancer Patients Treated With Hormonal Ablation
Thompson, C. A., Shanafelt, T. D., & Loprinzi, C. L. (2003) · The Oncologist · doi:10.1634/theoncologist.8-5-474 · Cited by 84 · see citing works
Smith, A. W., Bosch, M. A., Wagner, E. J., Rønnekleiv, O. K., & Kelly, M. J. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00281.2013 · Cited by 79 · see citing works
Juul, A. (2002) · Human Reproduction Update · doi:10.1093/humupd/8.5.423 · Cited by 80 · see citing works
Camporez, J. P., Lyu, K., Goldberg, E. L., Zhang, D., Cline, G. W., Jurczak, M. J., Dixit, V. D., Petersen, K. F., & Shulman, G. I. (2019) · The Journal of Physiology · doi:10.1113/jp277270 · Cited by 71 · see citing works
Oh, K. W., Rhee, E. J., Lee, W. Y., Kim, S. W., Baek, K. H., Kang, M. I., Yun, E. J., Park, C. Y., Ihm, S. H., Choi, M. G., et al. (2005) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2004.02179.x · Cited by 73 · see citing works
Comparative Assessment in Young and Elderly Men of the Gonadotropin Response to Aromatase Inhibition
T’Sjoen, G. G., Giagulli, V. A., Delva, H., Crabbe, P., De Bacquer, D., & Kaufman, J.-M. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-0982 · Cited by 73 · see citing works
Hofbauer, L., Hicok, K., Chen, D., & Khosla, S. (2002) · European Journal of Endocrinology · doi:10.1530/eje.0.1470269 · Cited by 72 · see citing works
Hevener, A. L., Zhou, Z., Moore, T. M., Drew, B. G., & Ribas, V. (2018) · Molecular Metabolism · doi:10.1016/j.molmet.2018.06.013 · Cited by 72 · see citing works
Wickman, S., Kajantie, E., & Dunkel, L. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021643 · Cited by 71 · see citing works
The Role of Sex Differences in Bone Health and Healing
Ortona, E., Pagano, M. T., Capossela, L., & Malorni, W. (2023) · Biology · doi:10.3390/biology12070993 · Cited by 68 · see citing works
Hero, M., Mäkitie, O., Kröger, H., Nousiainen, E., Toiviainen-Salo, S., & Dunkel, L. (2009) · Hormone Research in Paediatrics · doi:10.1159/000208803 · Cited by 60 · see citing works
Treatment of familial male-limited precocious puberty with bicalutamide and anastrozole
Kreher, N. C., Pescovitz, O. H., Delameter, P., Tiulpakov, A., & Hochberg, Z. (2006) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2006.04.027 · Cited by 59 · see citing works
Chwalisz, K., Surrey, E., & Stanczyk, F. Z. (2012) · Reproductive Sciences · doi:10.1177/1933719112438061 · Cited by 58 · see citing works
Ohlsson, C., Hammarstedt, A., Vandenput, L., Saarinen, N., Ryberg, H., Windahl, S. H., Farman, H. H., Jansson, J.-O., Movérare-Skrtic, S., Smith, U., et al. (2017) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00093.2017 · Cited by 55 · see citing works
Nuclear receptor superfamily: Principles of signaling
Germain, P., Altucci, L., Bourguet, W., Rochette-Egly, C., & Gronemeyer, H. (2003) · Pure and Applied Chemistry · doi:10.1351/pac200375111619 · Cited by 53 · see citing works
Teplyuk, N. M., Zhang, Y., Lou, Y., Hawse, J. R., Hassan, M. Q., Teplyuk, V. I., Pratap, J., Galindo, M., Stein, J. L., Stein, G. S., et al. (2009) · Molecular Endocrinology · doi:10.1210/me.2008-0270 · Cited by 52 · see citing works
Insulin-like growth factors and skeletal growth: possibilities for therapeutic interventions
Van Wyk, J. J., & Smith, E. P. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.12.6201 · Cited by 53 · see citing works
Self-citationThe Impact of Skeletal Muscle ERα on Mitochondrial Function and Metabolic Health
Hevener, A. L., Ribas, V., Moore, T. M., & Zhou, Z. (2020) · Endocrinology · doi:10.1210/endocr/bqz017 · Cited by 54 · see citing works
Arisaka, O., Hoshi, M., Kanazawa, S., Numata, M., Nakajima, D., Kanno, S., Negishi, M., Nishikura, K., Nitta, A., Imataka, M., et al. (2001) · Metabolism · doi:10.1053/meta.2001.21678 · Cited by 50 · see citing works
Szulc, P., Claustrat, B., Munoz, F., Marchand, F., & Delmas, P. D. (2004) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2004.02117.x · Cited by 48 · see citing works
Estrogens: Two nuclear receptors, multiple possibilities
Biason-Lauber, A., & Lang-Muritano, M. (2022) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2022.111710 · Cited by 49 · see citing works
Effect of aromatase inhibition on bone metabolism in elderly hypogonadal men
Leder, B. Z., & Finkelstein, J. S. (2005) · Osteoporosis International · doi:10.1007/s00198-005-1890-8 · Cited by 44 · see citing works
Shozu, M., Zhao, Y., & R. Simpson, E. (2000) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(99)00233-6 · Cited by 36 · see citing works
Veldhuis, J. D., & Iranmanesh, A. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0834 · Cited by 36 · see citing works
The androgen receptor is required for maintenance of bone mass in adult male mice
Wu, J., Henning, P., Sjögren, K., Koskela, A., Tuukkanen, J., Movérare-Skrtic, S., & Ohlsson, C. (2019) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2018.10.008 · Cited by 30 · see citing works
Estrogen Deficiency, Postmenopausal Osteoporosis, and Age-Related Bone Loss
Khosla, S., & Pacifici, R. (2013) · Osteoporosis · doi:10.1016/b978-0-12-415853-5.00046-7 · Cited by 31 · see citing works
Sacharidou, A., Chambliss, K., Peng, J., Barrera, J., Tanigaki, K., Luby-Phelps, K., Özdemir, İ., Khan, S., Sirsi, S. R., Kim, S. H., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-40562-w · Cited by 25 · see citing works
- Authors
- Smith, E. P., Boyd, J., Frank, G. R., Takahashi, H., Cohen, R. M., Specker, B., Williams, T. C., Lubahn, D. B., & Korach, K. S.
- Affiliations
- Cincinnati Children's Hospital Medical Center (US)
- National Institutes of Health (US)
- University of North Carolina at Chapel Hill (US)
- Venue
- New England Journal of Medicine
- Publisher
- Massachusetts Medical Society
- Published
- 1994-10-20
- Volume
- 331
- Issue
- 16
- Pages
- 1056-1061
- ISSN
- 0028-4793 (ISSN-L)
- 1533-4406
- OpenAlex
- W2321613759
- Cited by
- 2,471
- References
- 30
- Citations by year
- 2026: 18 · 2025: 26 · 2024: 22 · 2023: 32 · 2022: 36 · 2021: 42 · 2020: 49 · 2019: 55 · 2018: 59 · 2017: 60 · 2016: 60 · 2015: 70 · 2014: 76 · 2013: 72 · 2012: 67
- FWCI
- 35.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- New England Journal of Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Center for Research Resources (M01RR008084, MO1 RR 08084)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- 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
- Keywords
- estrogen resistance, estrogen receptor gene, estrogen receptor mutations, premature stop codon, pituitary-gonadal function, hyperinsulinemia, impaired glucose tolerance, bone mineral density, bone turnover, epiphyseal closure, consanguinity, transdermal estrogen, tall stature
- MeSH terms
- Adult, Base Sequence, Codon, Drug Resistance, Estrogens, Humans, Male, Molecular Sequence Data, Mutation, Osteoporosis, Pedigree, Receptors, Estrogen, Polymerase Chain Reaction
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
