Ozone treatment prevents the toxicity of an environmental mixture of estrogens on rat fetal testicular development

Lassonde, Guylaine; Nasuhoglu, Deniz; Pan, Jun Feng; Gaye, Bintou; Yargeau, Viviane; Delbès, Géraldine

doi:10.1016/j.reprotox.2015.09.001

Cited by 13 publications

(4 citation statements)

References 31 publications

(49 reference statements)

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“…However, the mechanisms involved have not been elucidated yet. We have used the organ culture of rat fetal testes to study the impact of various ED on gametogenesis and steroidogenesis during perinatal life [20, 25, 26]. It was proved to be a robust model to reproduce the kinetics of development of the rat fetal testis [24].…”

Section: Discussionmentioning

confidence: 99%

“…In particular, the maintenance of testicular development can only be achieved for a few days. Nonetheless, we and others have used this approach as a toxicological test to evaluate the direct effects of various ED on gametogenesis and steroidogenesis in rodent and human testes [20, 25, 26]. But, it is still unknown whether the epigenetic reprogramming that occurs in male germ cells at that time is faithfully reproduced in vitro.…”

Section: Introductionmentioning

confidence: 99%

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Fetal testis organ culture reproduces the dynamics of epigenetic reprogramming in rat gonocytes

Rwigemera

Joao

Delbès

2017

Epigenetics & Chromatin

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BackgroundEpigenetic reprogramming is a critical step in male germ cell development that occurs during perinatal life. It is characterized by the remodeling of different epigenetic marks such as DNA methylation (5mC) and methylation of histone H3. It has been suggested that endocrine disruptors can affect the male germline epigenome by altering epigenetic reprogramming, but the mechanisms involved are still unknown. We have previously used an organ culture system that maintains the development of the different fetal testis cell types, to evaluate the effects of various endocrine disruptors on gametogenesis and steroidogenesis in the rat. We hypothesize that this culture model can reproduce the epigenetic reprogramming in gonocytes. Our aim was to establish the kinetics of three epigenetic marks throughout perinatal development in rats in vivo and compare them after different culture times.ResultsUsing immunofluorescence, we showed that H3K4me2 transiently increased in gonocytes at 18.5 days post-coitum (dpc), while H3K4me3 displayed a stable increase in gonocytes from 18.5 dpc until after birth. 5mC progressively increased from 20.5 dpc until after birth. Using GFP-positive gonocytes purified from GCS-EGFP rats, we established the chronology of re-methylation of H19 and Snrpn in rat gonocytes. Most importantly, using testis explanted at 16.5 or 18.5 dpc and cultured for 2–4 days, we demonstrated that the kinetics of changes in H3K4me2, H3K4me3, global DNA methylation and on parental imprints can generally be reproduced ex vivo with the model of organ culture without the addition of serum.ConclusionsThis study reveals the chronology of three epigenetic marks (H3K4me2, H3K4me3 and 5mC) and the patterns of methylation of H19 and Snrpn differentially methylated regions in rat gonocytes during perinatal development. Most importantly, our results suggest that the organ culture can reproduce the process of epigenetic reprogramming and can be used to study the impact of environmental chemicals on the establishment of the male germ cell epigenome.Electronic supplementary materialThe online version of this article (doi:10.1186/s13072-017-0127-3) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Fetal testis organ culture reproduces the dynamics of epigenetic reprogramming in rat gonocytes

Rwigemera

Joao

Delbès

2017

Epigenetics & Chromatin

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“…Organ cultures were done as previously described [45]. Briefly, each testis was placed on hydrophilic PTFE cell culture inserts with a pore size of 0.4 µm (Millipore, #PICM01250).…”

Section: Methodsmentioning

confidence: 99%

Reproductive toxicity of emerging plasticizers, flame retardants, and bisphenols, using culture of the rat fetal testis

Tardif

Rwigemera

Letourneau

et al. 2023

Biology of Reproduction

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The use of bis (2-ethylhexyl) phthalate (DEHP), 2,2′4,4′-tetrabromodiphenyl ether (BDE-47) and bisphenol A (BPA), as plasticizers, flame-retardant and epoxy resins, respectively, has been regulated due to their endocrine disrupting chemical (EDC) activities. Replacements for these chemicals are found in the environment and human matrices, yet the EDC activity of these emerging contaminants is poorly characterized. We compared the effects of legacy chemicals with those of their replacements using fetal rat testis organ culture. Fetal testes sampled at gestation day 15 were grown ex vivo and the impact was evaluated after a 3-day exposure to 10 μM of each legacy chemical, two BPA analogs (BPM and BPTMC), three replacements for DEHP/MEHP (TXIB, DINP, DIDA) or two replacements for BDE-47 (TBEP, IPPP). Using culture media, we showed that only BPA and MEHP significantly decrease basal testosterone secretions after 24 h of treatment while BPM and BPTMC have the opposite effect. LH-stimulated testosterone was reduced by BPA and MEHP but increased by BPTMC. After exposure, testes were used for immunofluorescent staining of germ cells, Sertoli cells and Leydig cells. Interestingly, the effect of BPM and BPTMC on testosterone secretion was associated with a significant increase in Leydig cell density and surface area. A decrease in germ cell density was observed only after treatment with MEHP or BDE-47. MEHP significantly decreased Sertoli cell proliferation. These studies show that some replacement chemicals can affect testicular function while others appear to show little toxicity in this model. These findings provide essential information regarding the need for their regulation.

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“…Exposure to estrogen-like molecules found in the environment, such as wastewater, can negatively affect testicular fetal development, partly by inhibiting spermatogenesis, especially during gestation, when testicular cells are more sensitive to estrogens (Ullah et al, 2018). Ozone can degrade steroids and in particular estradiol (Mills et al, 2015), thus one study (Lassonde et al, 2015) used organ cultures of rat fetal testis as a bioassay to monitor the toxicity of mixture of estrogens: 17B-estradiol (E2), 17 alpha-ethinylestradiol (EE2), estrone (E1) and estriol (E3), at concentrations found in wastewater. The aim of the study was to determine whether OT could remove these compounds and alleviate their potential toxicity.…”

Section: Effect Of Ozone On Estrogen-induced Testicular Toxicitymentioning

confidence: 99%

Ozone Therapy: Overview of its Potential Utility in Male Reproduction

Merhi¹,

Bazzi²,

Moseley-LaRue³

et al. 2018

American Journal of Immunology

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Ozone (O3), a highly water-soluble inorganic molecule, is a gas made of three atoms of oxygen (O) with a cyclic structure. Ozone can be produced by medical generators from pure oxygen after passing through a high voltage gradient. Ozone therapy (OT) can be given in medical practice via several routes that include transdermal, intramuscular, rectal, nasal, oral, vaginal, intravenous, intra-arterial, intraperitoneal, intra-pleural, topical, dental, intra-discal and by autohemotherapy. Because ozone, a highly reactive molecule, is a potent oxidant and anti-inflammatory agent, it has strong bactericidal, antiviral, anti-fungal and anti-protozoal actions as well as therapeutic effects on the immune system. With its multifaceted route of administration, OThas been used to treat several pathologies that involve the immune system such as cancers, sepsis, abscesses and chronic wounds, skin problems (such as eczema and psoriasis), HIV infection, asthma, arthritis, urologic problems, osteomyelitis and many others. The purpose of this review article is to evaluate the role of OT in the male reproductive system. We performed a review of all available basic science, experimental animal studies and clinical peer-reviewed articles published in PubMed and Google Scholar until November 2018. The literature so far retrieved shows that most studies pertaining to the effect of OT on male reproduction were performed in animals. Results to date show that OT, via improving the immune system, significantly protects testicular function in the setting of testicular torsion/ischemia, protects against the effect of gonadotoxic agents and treats bacterial infections in the semen. This article calls for a need for at least pilot studies in humans using OT in its safest route of administration, which is probably the transdermal one. This would be significant especially considering that male factor infertility constitutes up to one third of couple infertility and it is very common that poor semen parameters are irreversible with medical or surgical treatment, such as varicocele repair or vasectomy reversal.

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Ozone treatment prevents the toxicity of an environmental mixture of estrogens on rat fetal testicular development

Cited by 13 publications

References 31 publications

Fetal testis organ culture reproduces the dynamics of epigenetic reprogramming in rat gonocytes

Fetal testis organ culture reproduces the dynamics of epigenetic reprogramming in rat gonocytes

Reproductive toxicity of emerging plasticizers, flame retardants, and bisphenols, using culture of the rat fetal testis

Ozone Therapy: Overview of its Potential Utility in Male Reproduction

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