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Article ; Online: Expression patterns of sex steroid receptors in developing mesonephros of the male mouse: three-dimensional analysis.

Omotehara, Takuya / Hess, Rex A / Nakata, Hiroki / Birch, Lynn A / Prins, Gail S / Itoh, Masahiro

2023 Volume 393, Issue 3, Page(s) 577–593

Abstract: The androgen pathway via androgen receptor (AR) has received the most attention for development of male reproductive tracts. The estrogen pathway through estrogen receptor (ESR1) is also a major contributor to rete testis and efferent duct formation, but ...

Abstract	The androgen pathway via androgen receptor (AR) has received the most attention for development of male reproductive tracts. The estrogen pathway through estrogen receptor (ESR1) is also a major contributor to rete testis and efferent duct formation, but the role of progesterone via progesterone receptor (PGR) has largely been overlooked. Expression patterns of these receptors in the mesonephric tubules (MTs) and Wolffian duct (WD), which differentiate into the efferent ductules and epididymis, respectively, remain unclear because of the difficulty in distinguishing each region of the tracts. This study investigated AR, ESR1, and PGR expressions in the murine mesonephros using three-dimensional (3-D) reconstruction. The receptors were localized in serial paraffin sections of the mouse testis and mesonephros by immunohistochemistry on embryonic days (E) 12.5, 15.5, and 18.5. Specific regions of the developing MTs and WD were determined by 3-D reconstruction using Amira software. AR was found first in the specific portion of the MTs near the MT-rete junction at E12.5, and the epithelial expression showed increasing strength from cranial to the caudal regions. Epithelial expression of ESR1 was found in the cranial WD and MTs near the WD first at E15.5. PGR was weakly positive only in the MTs and cranial WD starting on E15.5. This 3-D analysis suggests that gonadal androgen acts first on the MTs near the MT-rete junction but that estrogen is the first to influence MTs near the WD, while potential PGR activity is delayed and limited to the epithelium.
MeSH term(s)	Male ; Animals ; Mice ; Mesonephros ; Androgens ; Epididymis ; Receptors, Estrogen ; Receptors, Androgen ; Gonadal Steroid Hormones ; Estrogens
Chemical Substances	Androgens ; Receptors, Estrogen ; Receptors, Androgen ; Gonadal Steroid Hormones ; Estrogens
Language	English
Publishing date	2023-06-19
Publishing country	Germany
Document type	Journal Article
ZDB-ID	125067-x
ISSN	1432-0878 ; 0302-766X
ISSN (online)	1432-0878
ISSN	0302-766X
DOI	10.1007/s00441-023-03796-0
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Ub I Zs.94: Show issues

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Article: Disruption of estrogen receptor signaling and similar pathways in the efferent ductules and initial segment of the epididymis.

Hess, Rex A

Spermatogenesis

2014 Volume 4, Issue 2, Page(s) e979103

Abstract: Seminiferous tubular atrophy may involve indirectly the disruption of estrogen receptor-α (ESR1) function in efferent ductules of the testis. ESR1 helps to maintain fluid resorption by the ductal epithelium and the inhibition or stimulation of this ... ...

Abstract	Seminiferous tubular atrophy may involve indirectly the disruption of estrogen receptor-α (ESR1) function in efferent ductules of the testis. ESR1 helps to maintain fluid resorption by the ductal epithelium and the inhibition or stimulation of this activity in rodent species will lead to fluid accumulation in the lumen. If not resolved, the abnormal buildup of fluid in the head of the epididymis and efferent ductules becomes a serious problem for the testis, as it leads to an increase in testis weight, tubular dilation and seminiferous epithelial degeneration, as well as testicular atrophy. The same sequence of pathogenesis occurs if the efferent ductule lumen becomes occluded. This review provides an introduction to the role of estrogen in the male reproductive tract but focuses on the various overlapping mechanisms that could induce efferent ductule dysfunction and fluid backpressure histopathology. Although efferent ductules are difficult to find, their inclusion in routine histological evaluations is recommended, as morphological images of these delicate tubules may be essential for understanding the mechanism of testicular injury, especially if dilations are observed in the rete testis and/or seminiferous tubules.
Language	English
Publishing date	2014-12-31
Publishing country	United States
Document type	Review ; Journal Article
ZDB-ID	2629571-4
ISSN	2156-5562 ; 2156-5554
ISSN (online)	2156-5562
ISSN	2156-5554
DOI	10.4161/21565562.2014.979103
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Article ; Online: Estrogen in the male: a historical perspective.

Hess, Rex A / Cooke, Paul S

Biology of reproduction

2018 Volume 99, Issue 1, Page(s) 27–44

Abstract: Estrogens have traditionally been considered female hormones. Nevertheless, the presence of estrogen in males has been known for over 90 years. Initial studies suggested that estrogen was deleterious to male reproduction because exogenous treatments ... ...

Abstract	Estrogens have traditionally been considered female hormones. Nevertheless, the presence of estrogen in males has been known for over 90 years. Initial studies suggested that estrogen was deleterious to male reproduction because exogenous treatments induced developmental abnormalities. However, demonstrations of estrogen synthesis in the testis and high concentrations of 17β-estradiol in rete testis fluid suggested that the female hormone might have a function in normal male reproduction. Identification of estrogen receptors and development of biological radioisotope methods to assess estradiol binding revealed that the male reproductive tract expresses estrogen receptor extensively from the neonatal period to adulthood. This indicated a role for estrogens in normal development, especially in efferent ductules, whose epithelium is the first in the male reproductive tract to express estrogen receptor during development and a site of exceedingly high expression. In the 1990s, a paradigm shift occurred in our understanding of estrogen function in the male, ushered in by knockout mouse models where estrogen production or expression of its receptors was not present. These knockout animals revealed that estrogen's main receptor (estrogen receptor 1 [ESR1]) is essential for male fertility and development of efferent ductules, epididymis, and prostate, and that loss of only the membrane fraction of ESR1 was sufficient to induce extensive male reproductive abnormalities and infertility. This review provides perspectives on the major discoveries and developments that led to our current knowledge of estrogen's importance in the male reproductive tract and shaped our evolving concept of estrogen's physiological role in the male.
MeSH term(s)	Animals ; Estrogens/metabolism ; Humans ; Male ; Receptors, Estrogen/metabolism ; Reproduction/physiology ; Signal Transduction/physiology ; Testis/metabolism
Chemical Substances	Estrogens ; Receptors, Estrogen
Language	English
Publishing date	2018-02-14
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	1118-6
ISSN	1529-7268 ; 0006-3363
ISSN (online)	1529-7268
ISSN	0006-3363
DOI	10.1093/biolre/ioy043
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Zs.A 551: Show issues

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Article ; Online: Estrogens and development of the rete testis, efferent ductules, epididymis and vas deferens.

Hess, Rex A / Sharpe, Richard M / Hinton, Barry T

Differentiation; research in biological diversity

2020 Volume 118, Page(s) 41–71

Abstract: Estrogen has always been considered the female hormone and testosterone the male hormone. However, estrogen's presence in the testis and deleterious effects of estrogen treatment during development have been known for nearly 90 years, long before ... ...

Abstract	Estrogen has always been considered the female hormone and testosterone the male hormone. However, estrogen's presence in the testis and deleterious effects of estrogen treatment during development have been known for nearly 90 years, long before estrogen receptors (ESRs) were discovered. Eventually it was learned that testes actually synthesize high levels of estradiol (E2) and sequester high concentrations in the reproductive tract lumen, which seems contradictory to the overwhelming number of studies showing reproductive pathology following exogenous estrogen exposures. For too long, the developmental pathology of estrogen has dominated our thinking, even resulting in the "estrogen hypothesis" as related to the testicular dysgenesis syndrome. However, these early studies and the development of an Esr1 knockout mouse led to a deluge of research into estrogen's potential role in and disruption of development and function of the male reproductive system. What is new is that estrogen action in the male cannot be divorced from that of androgen. This paper presents what is known about components of the estrogen pathway, including its synthesis and target receptors, and the need to achieve a balance between androgen- and estrogen-action in male reproductive tract differentiation and adult functions. The review focuses on what is known regarding development of the male reproductive tract, from the rete testis to the vas deferens, and examines the expression of estrogen receptors and presence of aromatase in the male reproductive system, traces the evidence provided by estrogen-associated knockout and transgenic animal models and discusses the effects of fetal and postnatal exposures to estrogens. Hopefully, there will be enough here to stimulate discussions and new investigations of the androgen:estrogen balance that seems to be essential for development of the male reproductive tract.
MeSH term(s)	Androgens/genetics ; Androgens/metabolism ; Animals ; Embryo, Mammalian ; Embryonic Development/genetics ; Epididymis/growth & development ; Epididymis/metabolism ; Estradiol/metabolism ; Estrogen Receptor alpha/genetics ; Estrogens/genetics ; Estrogens/metabolism ; Female ; Genitalia, Male ; Male ; Mice ; Mice, Knockout/genetics ; Rete Testis/growth & development ; Rete Testis/metabolism ; Testosterone/genetics ; Testosterone/metabolism
Chemical Substances	Androgens ; Esr1 protein, mouse ; Estrogen Receptor alpha ; Estrogens ; Testosterone (3XMK78S47O) ; Estradiol (4TI98Z838E)
Language	English
Publishing date	2020-12-13
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	184540-8
ISSN	1432-0436 ; 0301-4681
ISSN (online)	1432-0436
ISSN	0301-4681
DOI	10.1016/j.diff.2020.11.004
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Article ; Online: Role for Nongenomic Estrogen Signaling in Male Fertility.

Graceli, Jones B / Zomer, Helena D / Medrano, Theresa I / Hess, Rex A / Korach, Kenneth S / Cooke, Paul S

Endocrinology

2023 Volume 165, Issue 3

Abstract: Estrogen actions are mediated by both nuclear (n) and membrane (m) localized estrogen receptor 1 (ESR1). Male Esr1 knockout (Esr1KO) mice lacking functional Esr1 are infertile, with reproductive tract abnormalities. Male mice expressing nESR1 but lacking ...

Abstract	Estrogen actions are mediated by both nuclear (n) and membrane (m) localized estrogen receptor 1 (ESR1). Male Esr1 knockout (Esr1KO) mice lacking functional Esr1 are infertile, with reproductive tract abnormalities. Male mice expressing nESR1 but lacking mESR1 (nuclear-only estrogen receptor 1 mice) are progressively infertile due to testicular, rete testis, and efferent ductule abnormalities similar to Esr1KO males, indicating a role for mESR1 in male reproduction. The H2NES mouse expresses only mESR1 but lacks nESR1. The goal of this study was to identify the functions of mESR1 alone in mice where nESR1 was absent. Breeding trials showed that H2NES males are fertile, with decreased litter numbers but normal pup numbers/litter. In contrast to Esr1KO mice, H2NES testicular, and epididymal weights were not reduced, and seminiferous tubule abnormalities were less pronounced. However, Esr1KO and H2NES males both had decreased sperm motility and a high incidence of abnormal sperm morphology. Seminiferous tubule and rete testis dilation and decreased efferent ductule epithelial height characteristic of Esr1KO males were reduced in H2NES. Consistent with this, expression of genes involved in fluid transport and ion movement that were reduced in Esr1KO (Aqp1, Car2, Car14, Cftr) were partially or fully restored to wild-type levels in H2NES. In summary, in contrast to Esr1KO males, H2NES males are fertile and have reduced phenotypic and functional abnormalities in the testis and efferent ductules. Thus, mESR1 alone, in the absence of nESR1, can partially regulate male reproductive tract structure and function, emphasizing its importance for overall estrogen action.
MeSH term(s)	Male ; Mice ; Animals ; Estrogen Receptor alpha/genetics ; Estrogen Receptor alpha/metabolism ; Sperm Motility/genetics ; Semen/metabolism ; Estrogens ; Mice, Knockout ; Fertility/genetics
Chemical Substances	Estrogen Receptor alpha ; Estrogens
Language	English
Publishing date	2023-12-08
Publishing country	United States
Document type	Journal Article
ZDB-ID	427856-2
ISSN	1945-7170 ; 0013-7227
ISSN (online)	1945-7170
ISSN	0013-7227
DOI	10.1210/endocr/bqad180
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Article ; Online: CEP164 is essential for efferent duct multiciliogenesis and male fertility.

Hoque, Mohammed / Chen, Danny / Hess, Rex A / Li, Feng-Qian / Takemaru, Ken-Ichi

Reproduction (Cambridge, England)

2021 Volume 162, Issue 2, Page(s) 129–139

Abstract: Cilia are evolutionarily conserved microtubule-based structures that perform diverse biological functions. Cilia are assembled on basal bodies and anchored to the plasma membrane via distal appendages. In the male reproductive tract, multicilia in ... ...

Abstract	Cilia are evolutionarily conserved microtubule-based structures that perform diverse biological functions. Cilia are assembled on basal bodies and anchored to the plasma membrane via distal appendages. In the male reproductive tract, multicilia in efferent ducts (EDs) move in a whip-like motion to prevent sperm agglutination. Previously, we demonstrated that the distal appendage protein CEP164 recruits Chibby1 (Cby1) to basal bodies to facilitate basal body docking and ciliogenesis. Mice lacking CEP164 in multiciliated cells (MCCs) (FoxJ1-Cre;CEP164fl/fl) show a significant loss of multicilia in the trachea, oviduct, and ependyma. In addition, we observed male sterility; however, the precise role of CEP164 in male fertility remained unknown. Here, we report that the seminiferous tubules and rete testis of FoxJ1-Cre;CEP164fl/fl mice exhibit substantial dilation, indicative of dysfunctional multicilia in the EDs. We found that multicilia were hardly detectable in the EDs of FoxJ1-Cre;CEP164fl/fl mice although FoxJ1-positive immature cells were present. Sperm aggregation and agglutination were commonly noticeable in the lumen of the seminiferous tubules and EDs of FoxJ1-Cre;CEP164fl/fl mice. In FoxJ1-Cre;CEP164fl/fl mice, the apical localization of Cby1 and the transition zone marker NPHP1 was severely diminished, suggesting basal body docking defects. TEM analysis of EDs further confirmed basal body accumulation in the cytoplasm of MCCs. Collectively, we conclude that male infertility in FoxJ1-Cre;CEP164fl/fl mice is caused by sperm agglutination and obstruction of EDs due to loss of multicilia. Our study, therefore, unravels an essential role of the distal appendage protein CEP164 in male fertility.
MeSH term(s)	Animals ; Cell Differentiation ; Cilia/metabolism ; Cilia/pathology ; Epididymis/metabolism ; Epididymis/pathology ; Epithelial Cells/metabolism ; Epithelial Cells/pathology ; Infertility, Male/etiology ; Infertility, Male/pathology ; Male ; Mice ; Mice, Knockout ; Microtubule Proteins/physiology ; Seminiferous Tubules/metabolism ; Seminiferous Tubules/pathology
Chemical Substances	Cep164 protein, mouse ; Microtubule Proteins
Language	English
Publishing date	2021-07-08
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2034501-X
ISSN	1741-7899 ; 1470-1626 ; 1476-3990
ISSN (online)	1741-7899
ISSN	1470-1626 ; 1476-3990
DOI	10.1530/REP-21-0042
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Article ; Online: In Memoriam: Duane L. Garner, PhD.

Lorton, Steven P / Amann, Rupert / DeJarnette, Mel / Johnson, Larry / Hess, Rex A

Andrology

2020 Volume 8, Issue 5, Page(s) 968–969

Language	English
Publishing date	2020-08-14
Publishing country	England
Document type	Journal Article
ZDB-ID	2696108-8
ISSN	2047-2927 ; 2047-2919
ISSN (online)	2047-2927
ISSN	2047-2919
DOI	10.1111/andr.12888
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Article ; Online: Single neonatal estrogen implant sterilizes female animals by decreasing hypothalamic KISS1 expression.

Park, Chan Jin / Minabe, Shiori / Hess, Rex A / Lin, Po-Ching Patrick / Zhou, Sherry / Bashir, Shah Tauseef / Barakat, Radwa / Gal, Arnon / Ko, CheMyong Jay

Scientific reports

2023 Volume 13, Issue 1, Page(s) 9627

Abstract: Reproductive sterilization by surgical gonadectomy is strongly advocated to help manage animal populations, especially domesticated pets, and to prevent reproductive behaviors and diseases. This study explored the use of a single-injection method to ... ...

Abstract	Reproductive sterilization by surgical gonadectomy is strongly advocated to help manage animal populations, especially domesticated pets, and to prevent reproductive behaviors and diseases. This study explored the use of a single-injection method to induce sterility in female animals as an alternative to surgical ovariohysterectomy. The idea was based on our recent finding that repetitive daily injection of estrogen into neonatal rats disrupted hypothalamic expression of Kisspeptin (KISS1), the neuropeptide that triggers and regulates pulsatile secretion of GnRH. Neonatal female rats were dosed with estradiol benzoate (EB) either by daily injections for 11 days or by subcutaneous implantation of an EB-containing silicone capsule designed to release EB over 2-3 weeks. Rats treated by either method did not exhibit estrous cyclicity, were anovulatory, and became infertile. The EB-treated rats had fewer hypothalamic Kisspeptin neurons, but the GnRH-LH axis remained responsive to Kisspeptin stimulation. Because it would be desirable to use a biodegradable carrier that is also easier to handle, an injectable EB carrier was developed from PLGA microspheres to provide pharmacokinetics comparable to the EB-containing silicone capsule. A single neonatal injection of EB-microspheres at an equivalent dosage resulted in sterility in the female rat. In neonatal female Beagle dogs, implantation of an EB-containing silicone capsule also reduced ovarian follicle development and significantly inhibited KISS1 expression in the hypothalamus. None of the treatments produced any concerning health effects, other than infertility. Therefore, further development of this technology for sterilization in domestic female animals, such as dogs and cats is worthy of investigation.
MeSH term(s)	Female ; Animals ; Cats ; Dogs ; Rats ; Kisspeptins/pharmacology ; Cat Diseases ; Dog Diseases ; Hypothalamus ; Gonadotropin-Releasing Hormone ; Animals, Domestic ; Sterilization ; Infertility ; Estrogens/pharmacology
Chemical Substances	Kisspeptins ; Gonadotropin-Releasing Hormone (33515-09-2) ; Estrogens
Language	English
Publishing date	2023-06-14
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-023-36727-8
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Article ; Online: MIWI N-terminal RG motif promotes efficient pachytene piRNA production and spermatogenesis independent of LINE1 transposon silencing.

Wei, Chao / Jing, Jiongjie / Yan, Xiaoyuan / Mann, Jeffrey M / Geng, Ruirong / Xie, Huirong / Demireva, Elena Y / Hess, Rex A / Ding, Deqiang / Chen, Chen

PLoS genetics

2023 Volume 19, Issue 11, Page(s) e1011031

Abstract: PIWI proteins and their associated piRNAs act to silence transposons and promote gametogenesis. Murine PIWI proteins MIWI, MILI, and MIWI2 have multiple arginine and glycine (RG)-rich motifs at their N-terminal domains. Despite being known as docking ... ...

Abstract	PIWI proteins and their associated piRNAs act to silence transposons and promote gametogenesis. Murine PIWI proteins MIWI, MILI, and MIWI2 have multiple arginine and glycine (RG)-rich motifs at their N-terminal domains. Despite being known as docking sites for the TDRD family proteins, the in vivo regulatory roles for these RG motifs in directing PIWI in piRNA biogenesis and spermatogenesis remain elusive. To investigate the functional significance of RG motifs in mammalian PIWI proteins in vivo, we genetically engineered an arginine to lysine (RK) point mutation of a conserved N-terminal RG motif in MIWI in mice. We show that this tiny MIWI RG motif is indispensable for piRNA biogenesis and male fertility. The RK mutation in the RG motif disrupts MIWI-TDRKH interaction and impairs enrichment of MIWI to the intermitochondrial cement (IMC) for efficient piRNA production. Despite significant overall piRNA level reduction, piRNA trimming and maturation are not affected by the RK mutation. Consequently, MiwiRK mutant mice show chromatoid body malformation, spermatogenic arrest, and male sterility. Surprisingly, LINE1 transposons are effectively silenced in MiwiRK mutant mice, indicating a LINE1-independent cause of germ cell arrest distinctive from Miwi knockout mice. These findings reveal a crucial function of the RG motif in directing PIWI proteins to engage in efficient piRNA production critical for germ cell progression and highlight the functional importance of the PIWI N-terminal motifs in regulating male fertility.
MeSH term(s)	Male ; Mice ; Animals ; Piwi-Interacting RNA ; Testis/metabolism ; RNA, Small Interfering/metabolism ; Spermatogenesis/genetics ; Proteins/metabolism ; Mice, Knockout ; Arginine/metabolism ; Argonaute Proteins/genetics ; Argonaute Proteins/metabolism ; Mammals/genetics
Chemical Substances	Piwi-Interacting RNA ; RNA, Small Interfering ; Proteins ; Arginine (94ZLA3W45F) ; Argonaute Proteins
Language	English
Publishing date	2023-11-13
Publishing country	United States
Document type	Journal Article
ZDB-ID	2186725-2
ISSN	1553-7404 ; 1553-7390
ISSN (online)	1553-7404
ISSN	1553-7390
DOI	10.1371/journal.pgen.1011031
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Article ; Online: SYPL1 defines a vesicular pathway essential for sperm cytoplasmic droplet formation and male fertility.

Liu, Jiali / Hermo, Louis / Ding, Deqiang / Wei, Chao / Mann, Jeffrey M / Yan, Xiaoyuan / Melnick, Ashley F / Wu, Yingjie / Withrow, Alicia / Cibelli, Jose / Hess, Rex A / Chen, Chen

Nature communications

2023 Volume 14, Issue 1, Page(s) 5113

Abstract: The cytoplasmic droplet is a conserved dilated area of cytoplasm situated at the neck of the sperm flagellum. Viewed as residual cytoplasm inherited from late spermatids, the cytoplasmic droplet contains numerous saccular elements as its key content. ... ...

Abstract	The cytoplasmic droplet is a conserved dilated area of cytoplasm situated at the neck of the sperm flagellum. Viewed as residual cytoplasm inherited from late spermatids, the cytoplasmic droplet contains numerous saccular elements as its key content. However, the origin of these saccules and the function of the cytoplasmic droplet have long been speculative. Here, we identify the molecular origin of these cytoplasmic droplet components by uncovering a vesicle pathway essential for formation and sequestration of saccules within the cytoplasmic droplet. This process is governed by a transmembrane protein SYPL1 and its interaction with VAMP3. Genetic ablation of SYPL1 in mice reveals that SYPL1 dictates the formation and accumulation of saccular elements in the forming cytoplasmic droplet. Derived from the Golgi, SYPL1 vesicles are critical for segregation of key metabolic enzymes within the forming cytoplasmic droplet of late spermatids and epididymal sperm, which are required for sperm development and male fertility. Our results uncover a mechanism to actively form and segregate saccules within the cytoplasmic droplet to promote sperm fertility.
MeSH term(s)	Animals ; Male ; Mice ; Blister ; Cytoplasm ; Cytosol ; Fertility ; Semen ; Spermatozoa
Chemical Substances	Sypl protein, mouse
Language	English
Publishing date	2023-08-22
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-40862-1
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