Alleviating 3-MCPD-induced male reproductive toxicity: Mechanistic insights and resveratrol intervention

3-Monochloropropane-1, 2-diol (3-MCPD), a food-borne contaminant, is widely regarded as the primary cause of male infertility. At present, identifying a method to improve/reduce the male reproductive toxicity caused by 3-MCPD is important. In our study, we explored the potential application of resve...

Full description

Bibliographic Details
Main Authors: Kai-Lee Wang, Yi-Fen Chiang, Ko-Chieh Huang, Hsin-Yuan Chen, Mohamed Ali, Shih-Min Hsia
Format: Article
Language:English
Published: Elsevier 2024-02-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0147651324000538
_version_ 1827361001698230272
author Kai-Lee Wang
Yi-Fen Chiang
Ko-Chieh Huang
Hsin-Yuan Chen
Mohamed Ali
Shih-Min Hsia
author_facet Kai-Lee Wang
Yi-Fen Chiang
Ko-Chieh Huang
Hsin-Yuan Chen
Mohamed Ali
Shih-Min Hsia
author_sort Kai-Lee Wang
collection DOAJ
description 3-Monochloropropane-1, 2-diol (3-MCPD), a food-borne contaminant, is widely regarded as the primary cause of male infertility. At present, identifying a method to improve/reduce the male reproductive toxicity caused by 3-MCPD is important. In our study, we explored the potential application of resveratrol (RSV) in mitigating the adverse effects of 3-MCPD. Using 7-week-old Sprague-Dawley (SD) rats as animal models, we investigated the impacts and underlying mechanisms of 3-MCPD and RSV on reproductive function. The administration of 3-MCPD led to significant reductions in testicular and epididymal weights, as well as disruptions in spermatogenesis and histological abnormalities. However, co-treatment with RSV and 3-MCPD mitigated these adverse effects. In vitro study, RSV exhibited the ability to reverse the decline in Leydig and Sertoli cell populations inflicted by 3-MCPD treatment. Mechanistically, RSV reduced endoplasmic reticulum stress (PARP), inflammasome activation (NLRP3), and autophagy-mediated lysosome dysfunction (p62 and LC3BII) induced by 3-MCPD. In addition, 3-MCPD treatment increased the expression level of steroidogenesis-related proteins, steroidogenic acute regulatory (StAR) and CYP11A1, but RSV normalized StAR expression. Moreover, 3-MCPD-induced pro-inflammatory responses were counteracted by RSV treatment, with the cytokine reduction and modulation of CD206 expression, a marker of macrophage activation. These findings indicate that RSV attenuates 3-MCPD-induced reproductive toxicity, highlighting its application potential as an adjuvant agent for male reproductive health.
first_indexed 2024-03-08T06:56:41Z
format Article
id doaj.art-3482d847ad5e4a96a947340ecfb9ac2c
institution Directory Open Access Journal
issn 0147-6513
language English
last_indexed 2024-03-08T06:56:41Z
publishDate 2024-02-01
publisher Elsevier
record_format Article
series Ecotoxicology and Environmental Safety
spelling doaj.art-3482d847ad5e4a96a947340ecfb9ac2c2024-02-03T06:34:31ZengElsevierEcotoxicology and Environmental Safety0147-65132024-02-01271115978Alleviating 3-MCPD-induced male reproductive toxicity: Mechanistic insights and resveratrol interventionKai-Lee Wang0Yi-Fen Chiang1Ko-Chieh Huang2Hsin-Yuan Chen3Mohamed Ali4Shih-Min Hsia5Department of Nursing, Deh Yu College of Nursing and Health, Keelung 203301, Taiwan; School of Nutrition and Health Sciences, College of Nutrition, Taipei Medical University, 11031 Taipei, TaiwanSchool of Nutrition and Health Sciences, College of Nutrition, Taipei Medical University, 11031 Taipei, TaiwanSchool of Nutrition and Health Sciences, College of Nutrition, Taipei Medical University, 11031 Taipei, TaiwanSchool of Nutrition and Health Sciences, College of Nutrition, Taipei Medical University, 11031 Taipei, TaiwanClinical Pharmacy Department, Faculty of Pharmacy, Ain Shams University, 11566 Cairo, Egypt; Department of Obstetrics and Gynecology, University of Chicago, Chicago, IL 60637, USASchool of Nutrition and Health Sciences, College of Nutrition, Taipei Medical University, 11031 Taipei, Taiwan; Graduate Institute of Metabolism and Obesity Sciences, College of Nutrition, Taipei Medical University, 11031 Taipei, Taiwan; School of Food and Safety, Taipei Medical University, 11031 Taipei, Taiwan; Nutrition Research Center, Taipei Medical University Hospital, 11031 Taipei, Taiwan; TMU Research Center for Digestive Medicine, Taipei Medical University, 11031 Taipei, Taiwan; Correspondence to: School of Nutrition and Health Sciences, Taipei Medical University, Taipei 110, Taiwan.3-Monochloropropane-1, 2-diol (3-MCPD), a food-borne contaminant, is widely regarded as the primary cause of male infertility. At present, identifying a method to improve/reduce the male reproductive toxicity caused by 3-MCPD is important. In our study, we explored the potential application of resveratrol (RSV) in mitigating the adverse effects of 3-MCPD. Using 7-week-old Sprague-Dawley (SD) rats as animal models, we investigated the impacts and underlying mechanisms of 3-MCPD and RSV on reproductive function. The administration of 3-MCPD led to significant reductions in testicular and epididymal weights, as well as disruptions in spermatogenesis and histological abnormalities. However, co-treatment with RSV and 3-MCPD mitigated these adverse effects. In vitro study, RSV exhibited the ability to reverse the decline in Leydig and Sertoli cell populations inflicted by 3-MCPD treatment. Mechanistically, RSV reduced endoplasmic reticulum stress (PARP), inflammasome activation (NLRP3), and autophagy-mediated lysosome dysfunction (p62 and LC3BII) induced by 3-MCPD. In addition, 3-MCPD treatment increased the expression level of steroidogenesis-related proteins, steroidogenic acute regulatory (StAR) and CYP11A1, but RSV normalized StAR expression. Moreover, 3-MCPD-induced pro-inflammatory responses were counteracted by RSV treatment, with the cytokine reduction and modulation of CD206 expression, a marker of macrophage activation. These findings indicate that RSV attenuates 3-MCPD-induced reproductive toxicity, highlighting its application potential as an adjuvant agent for male reproductive health.http://www.sciencedirect.com/science/article/pii/S0147651324000538TestosteroneLeydig cellsSteroidogenesis3-MCPD
spellingShingle Kai-Lee Wang
Yi-Fen Chiang
Ko-Chieh Huang
Hsin-Yuan Chen
Mohamed Ali
Shih-Min Hsia
Alleviating 3-MCPD-induced male reproductive toxicity: Mechanistic insights and resveratrol intervention
Ecotoxicology and Environmental Safety
Testosterone
Leydig cells
Steroidogenesis
3-MCPD
title Alleviating 3-MCPD-induced male reproductive toxicity: Mechanistic insights and resveratrol intervention
title_full Alleviating 3-MCPD-induced male reproductive toxicity: Mechanistic insights and resveratrol intervention
title_fullStr Alleviating 3-MCPD-induced male reproductive toxicity: Mechanistic insights and resveratrol intervention
title_full_unstemmed Alleviating 3-MCPD-induced male reproductive toxicity: Mechanistic insights and resveratrol intervention
title_short Alleviating 3-MCPD-induced male reproductive toxicity: Mechanistic insights and resveratrol intervention
title_sort alleviating 3 mcpd induced male reproductive toxicity mechanistic insights and resveratrol intervention
topic Testosterone
Leydig cells
Steroidogenesis
3-MCPD
url http://www.sciencedirect.com/science/article/pii/S0147651324000538
work_keys_str_mv AT kaileewang alleviating3mcpdinducedmalereproductivetoxicitymechanisticinsightsandresveratrolintervention
AT yifenchiang alleviating3mcpdinducedmalereproductivetoxicitymechanisticinsightsandresveratrolintervention
AT kochiehhuang alleviating3mcpdinducedmalereproductivetoxicitymechanisticinsightsandresveratrolintervention
AT hsinyuanchen alleviating3mcpdinducedmalereproductivetoxicitymechanisticinsightsandresveratrolintervention
AT mohamedali alleviating3mcpdinducedmalereproductivetoxicitymechanisticinsightsandresveratrolintervention
AT shihminhsia alleviating3mcpdinducedmalereproductivetoxicitymechanisticinsightsandresveratrolintervention