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Endocrinology, Vol 137, 4796-4805, Copyright © 1996 by Endocrine Society

ARTICLES

Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility

EM Eddy, TF Washburn, DO Bunch, EH Goulding, BC Gladen, DB Lubahn and KS Korach
Gamete Biology Section, National Institute of Environmental Health Sciences, National Institutes of Health, Research Triangle Park, North Carolina 27709-2233, USA. eddy@niehs.nih.gov

The reproductive system of male mice homozygous for a mutation in the estrogen receptor (ER) gene (ER knock-out; ERKO) appears normal at the anatomical level. However, these males are infertile, indicating an essential role for ER-mediated processes in the regulation of male reproduction. Adult ERKO male mice have significantly fewer epididymal sperm than heterozygous or wild-type males. Although spermatogenesis is occurring in some seminiferous tubules of 3- to 5-month-old ERKO males, other tubules either have a dilated lumen and a disorganized seminiferous epithelium with few spermatogenic cells or lack a lumen and contain mainly Sertoli cells. There are no obvious differences in seminiferous tubules at 10 days of age between wild-type and ERKO mice, but the lumen in ERKO males is dilated in all seminiferous tubules by 20 days. However, spermatogenesis progresses and similar numbers of sperm are present in the cauda epididymis of ERKO and wild-type males until 10 weeks of age. Disruption of spermatogenesis and degeneration of the seminiferous tubules become apparent after 10 weeks in the caudal pole of the testis and progresses in a wave to the cranial pole by 6 months. However, the seminal vesicles, coagulating glands, prostate, and epididymis do not appear to be altered morphologically in ERKO mice. Serum testosterone levels are somewhat elevated, but LH and FSH levels are not significantly different from those in wild-type males. Sperm from 8- to 16-week-old mice have reduced motility and are ineffective at fertilizing eggs in vitro. In addition, ERKO males housed overnight with hormone-primed wild-type females produce significantly fewer copulatory plugs than do heterozygous or wild-type males. These results suggest that estrogen action is required for fertility in male mice and that the mutation of the ER in ERKO males leads to reduced mating frequency, low sperm numbers, and defective sperm function.


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Signal Transduction in the Ductuli Efferentes Testis of the Rat: Inhibition of Fluid Reabsorption by Cyclic Adenosine 3', 5'-Monophosphate
Biol Reprod, November 1, 2003; 69(5): 1714 - 1718.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
S. Aquila, D. Sisci, M. Gentile, A. Carpino, E. Middea, S. Catalano, V. Rago, and S. Ando
Towards a physiological role for cytochrome P450 aromatase in ejaculated human sperm
Hum. Reprod., August 1, 2003; 18(8): 1650 - 1659.
[Abstract] [Full Text] [PDF]

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 J AndrolHome page
M. R. Maduro, K. C. Lo, W. W. Chuang, and D. J. Lamb
Genes and Male Infertility: What Can Go Wrong?
J Androl, July 1, 2003; 24(4): 485 - 493.
[Full Text] [PDF]

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 Biol. Reprod.Home page
H.O. Goyal, A. Robateau, T.D. Braden, C.S. Williams, K.K. Srivastava, and K. Ali
Neonatal Estrogen Exposure of Male Rats Alters Reproductive Functions at Adulthood
Biol Reprod, June 1, 2003; 68(6): 2081 - 2091.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
S. Catalano, V. Pezzi, A. Chimento, C. Giordano, A. Carpino, M. Young, M. J. McPhaul, and S. Ando
Triiodothyronine Decreases the Activity of the Proximal Promoter (PII) of the Aromatase Gene in the Mouse Sertoli Cell Line, TM4
Mol. Endocrinol., May 1, 2003; 17(5): 923 - 934.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
J. M. Dufour, M.-N. Vo, N. Bhattacharya, J. Okita, R. Okita, and K. H. Kim
Peroxisome Proliferators Disrupt Retinoic Acid Receptor Alpha Signaling in the Testis
Biol Reprod, April 1, 2003; 68(4): 1215 - 1224.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
R. Thuillier, Y. Wang, and M. Culty
Prenatal Exposure to Estrogenic Compounds Alters the Expression Pattern of Platelet-Derived Growth Factor Receptors {alpha} and {beta} in Neonatal Rat Testis: Identification of Gonocytes as Targets of Estrogen Exposure
Biol Reprod, March 1, 2003; 68(3): 867 - 880.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
T. H. Thin, L. Wang, E. Kim, L. L. Collins, R. Basavappa, and C. Chang
Isolation and Characterization of Androgen Receptor Mutant, AR(M749L), with Hypersensitivity to 17-beta Estradiol Treatment
J. Biol. Chem., February 21, 2003; 278(9): 7699 - 7708.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
B. T. Akingbemi, R. Ge, C. S. Rosenfeld, L. G. Newton, D. O. Hardy, J. F. Catterall, D. B. Lubahn, K. S. Korach, and M. P. Hardy
Estrogen Receptor-{alpha} Gene Deficiency Enhances Androgen Biosynthesis in the Mouse Leydig Cell
Endocrinology, January 1, 2003; 144(1): 84 - 93.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
A. Rivas, J. S. Fisher, C. McKinnell, N. Atanassova, and R. M. Sharpe
Induction of Reproductive Tract Developmental Abnormalities in the Male Rat by Lowering Androgen Production or Action in Combination with a Low Dose of Diethylstilbestrol: Evidence for Importance of the Androgen-Estrogen Balance
Endocrinology, December 1, 2002; 143(12): 4797 - 4808.
[Abstract] [Full Text] [PDF]

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 J AndrolHome page
Q. Zhou, R. Nie, G. S. Prins, P. T. K. Saunders, B. S. Katzenellenbogen, and R. A. Hess
Localization of Androgen and Estrogen Receptors in Adult Male Mouse Reproductive Tract
J Androl, November 1, 2002; 23(6): 870 - 881.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
T. R. Pak, G. R. Lynch, and P.-S. Tsai
Differential Alteration of the Reproductive Axis by Testosterone and Estrogen in Peripubertal and Adult Male Siberian Hamsters (Phodopus sungorus)
Biol Reprod, September 1, 2002; 67(3): 706 - 711.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
M. R. Fielden, R. G. Halgren, C. J. Fong, C. Staub, L. Johnson, K. Chou, and T. R. Zacharewski
Gestational and Lactational Exposure of Male Mice to Diethylstilbestrol Causes Long-Term Effects on the Testis, Sperm Fertilizing Ability in Vitro, and Testicular Gene Expression
Endocrinology, August 1, 2002; 143(8): 3044 - 3059.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
M. H. Tong and W.-C. Song
Estrogen Sulfotransferase: Discrete and Androgen-Dependent Expression in the Male Reproductive Tract and Demonstration of an in Vivo Function in the Mouse Epididymis
Endocrinology, August 1, 2002; 143(8): 3144 - 3151.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
S. Aquila, D. Sisci, M. Gentile, E. Middea, L. Siciliano, and S. Ando
Human Ejaculated Spermatozoa Contain Active P450 Aromatase
J. Clin. Endocrinol. Metab., July 1, 2002; 87(7): 3385 - 3390.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
C. A. Oliveira, Q. Zhou, K. Carnes, R. Nie, D. E. Kuehl, G. L. Jackson, L. R. Franca, M. Nakai, and R. A. Hess
ER Function in the Adult Male Rat: Short- and Long-Term Effects of the Antiestrogen ICI 182,780 on the Testis and Efferent Ductules, without Changes in Testosterone
Endocrinology, June 1, 2002; 143(6): 2399 - 2409.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
G. Pare, A. Krust, R. H. Karas, S. Dupont, M. Aronovitz, P. Chambon, and M. E. Mendelsohn
Estrogen Receptor-{alpha} Mediates the Protective Effects of Estrogen Against Vascular Injury
Circ. Res., May 31, 2002; 90(10): 1087 - 1092.
[Abstract] [Full Text] [PDF]

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 J AndrolHome page
H. H. Badran and L. S. Hermo
Expression and Regulation of Aquaporins 1, 8, and 9 in the Testis, Efferent Ducts, and Epididymis of Adult Rats and During Postnatal Development
J Androl, May 1, 2002; 23(3): 358 - 373.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
C.-R. Shyr, Y.-C. Hu, E. Kim, and C. Chang
Modulation of Estrogen Receptor-mediated Transactivation by Orphan Receptor TR4 in MCF-7 Cells
J. Biol. Chem., April 19, 2002; 277(17): 14622 - 14628.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
R. Nie, Q. Zhou, E. Jassim, P. T.K. Saunders, and R. A. Hess
Differential Expression of Estrogen Receptors {alpha} and {beta} in the Reproductive Tractsof Adult Male Dogs and Cats
Biol Reprod, April 1, 2002; 66(4): 1161 - 1168.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
X. Meng, H. Akutsu, K. Schoene, C. Reifsteck, E. P. Fox, S. Olson, H. Sariola, R. Yanagimachi, and M. Baetscher
Transgene Insertion Induced Dominant Male Sterility and Rescue of Male Fertility Using Round Spermatid Injection
Biol Reprod, March 1, 2002; 66(3): 726 - 734.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
D. G. de Rooij, H. J.G. van de Kant, R. Dol, G. Wagemaker, P. P.W. van Buul, A. van Duijn-Goedhart, F. H. de Jong, and J. J. Broerse
Long-Term Effects of Irradiation Before Adulthood on Reproductive Function in the Male Rhesus Monkey
Biol Reprod, February 1, 2002; 66(2): 486 - 494.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
C. L. Smith, D. G. DeVera, D. J. Lamb, Z. Nawaz, Y.-H. Jiang, A. L. Beaudet, and B. W. O'Malley
Genetic Ablation of the Steroid Receptor Coactivator-Ubiquitin Ligase, E6-AP, Results in Tissue-Selective Steroid Hormone Resistance and Defects in Reproduction
Mol. Cell. Biol., January 15, 2002; 22(2): 525 - 535.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
G. Cobellis, R. Meccariello, G. Fienga, R. Pierantoni, and S. Fasano
Cytoplasmic and Nuclear Fos Protein Forms Regulate Resumption of Spermatogenesis in the Frog, Rana esculenta
Endocrinology, January 1, 2002; 143(1): 163 - 170.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
S. Tsukahara and K. Yamanouchi
Sex Difference in Septal Neurons Projecting Axons to Midbrain Central Gray in Rats: A Combined Double Retrograde Tracing and ER-Immunohistochemical Study
Endocrinology, January 1, 2002; 143(1): 285 - 294.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
Y. M. Qian, X. J. Sun, M. H. Tong, X. P. Li, J. Richa, and W.-C. Song
Targeted Disruption of the Mouse Estrogen Sulfotransferase Gene Reveals a Role of Estrogen Metabolism in Intracrine and Paracrine Estrogen Regulation
Endocrinology, December 1, 2001; 142(12): 5342 - 5350.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
E. R. Simpson and S. R. Davis
Minireview: Aromatase and the Regulation of Estrogen Biosynthesis--Some New Perspectives
Endocrinology, November 1, 2001; 142(11): 4589 - 4594.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
K.-H. Lee, C. Finnigan-Bunick, J. Bahr, and D. Bunick
Estrogen Regulation of Ion Transporter Messenger RNA Levels in Mouse Efferent Ductules Are Mediated Differentially Through Estrogen Receptor (ER) {alpha} and ER{beta}
Biol Reprod, November 1, 2001; 65(5): 1534 - 1541.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
Q. Zhou, L. Clarke, R. Nie, K. Carnes, L.-W. Lai, Y.-H. H. Lien, A. Verkman, D. Lubahn, J. S. Fisher, B. S. Katzenellenbogen, et al.
Estrogen action and male fertility: Roles of the sodium/hydrogen exchanger-3 and fluid reabsorption in reproductive tract function
PNAS, October 31, 2001; (2001) 241245898.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
E. R. Levin
Genome and Hormones: Gender Differences in Physiology: Invited Review: Cell localization, physiology, and nongenomic actions of estrogen receptors
J Appl Physiol, October 1, 2001; 91(4): 1860 - 1867.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
B. Jeffs, J. J. Meeks, M. Ito, F. A. Martinson, M. M. Matzuk, J. L. Jameson, and L. D. Russell
Blockage of the Rete Testis and Efferent Ductules by Ectopic Sertoli and Leydig Cells Causes Infertility in Dax1-Deficient Male Mice
Endocrinology, October 1, 2001; 142(10): 4486 - 4495.
[Abstract] [Full Text] [PDF]

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 Physiol. Rev.Home page
S. Nilsson, S. Makela, E. Treuter, M. Tujague, J. Thomsen, G. Andersson, E. Enmark, K. Pettersson, M. Warner, and J.-A. Gustafsson
Mechanisms of Estrogen Action
Physiol Rev, October 1, 2001; 81(4): 1535 - 1565.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
F. Larrea, R. Garcia-Becerra, A. E. Lemus, G. A. Garcia, G. Perez-Palacios, K. J. Jackson, K. M. Coleman, R. Dace, C. L. Smith, and A. J. Cooney
A-Ring Reduced Metabolites of 19-nor Synthetic Progestins as Subtype Selective Agonists for ER{alpha}
Endocrinology, September 1, 2001; 142(9): 3791 - 3799.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
C. A. Oliveira, K. Carnes, L. R. Franca, and R. A. Hess
Infertility and Testicular Atrophy in the Antiestrogen-Treated Adult Male Rat
Biol Reprod, September 1, 2001; 65(3): 913 - 920.
[Abstract] [Full Text] [PDF]


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