铅和钙的串扰诱导了顶体损伤和精子的超极化:信号和超结构证据。

IF 4.3 2区 生物学 Q1 BIOLOGY
Rajkumar Singh Yadav, Bhawna Kushawaha, Rahul Dhariya, Dilip Kumar Swain, Brijesh Yadav, Mukul Anand, Priyambada Kumari, Pradeep Kumar Rai, Dipty Singh, Sarvajeet Yadav, Satish Kumar Garg
{"title":"铅和钙的串扰诱导了顶体损伤和精子的超极化:信号和超结构证据。","authors":"Rajkumar Singh Yadav, Bhawna Kushawaha, Rahul Dhariya, Dilip Kumar Swain, Brijesh Yadav, Mukul Anand, Priyambada Kumari, Pradeep Kumar Rai, Dipty Singh, Sarvajeet Yadav, Satish Kumar Garg","doi":"10.1186/s40659-024-00517-x","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Exposure of humans and animals to heavy metals is increasing day-by-day; thus, lead even today remains of significant public health concern. According to CDC, blood lead reference value (BLRV) ranges from 3.5 µg/dl to 5 μg/dl in adults. Recently, almost 2.6% decline in male fertility per year has been reported but the cause is not well established. Lead (Pb<sup>2+</sup>) affects the size of testis, semen quality, and secretory functions of prostate. But the molecular mechanism(s) of lead toxicity in sperm cells is not clear. Thus, present study was undertaken to evaluate the adverse effects of lead acetate at environmentally relevant exposure levels (0.5, 5, 10 and 20 ppm) on functional and molecular dynamics of spermatozoa of bucks following in vitro exposure for 15 min and 3 h.</p><p><strong>Results: </strong>Lead significantly decreased motility, viable count, and motion kinematic patterns of spermatozoa like curvilinear velocity, straight-line velocity, average path velocity, beat cross frequency and maximum amplitude of head lateral displacement even at 5 ppm concentration. Pb<sup>2+</sup> modulated intracellular cAMP and Ca<sup>2+</sup> levels in sperm cells through L-type calcium channels and induced spontaneous or premature acrosome reaction (AR) by increasing tyrosine phosphorylation of sperm proteins and downregulated mitochondrial transmembrane potential. Lead significantly increased DNA damage and apoptosis as well. Electron microscopy studies revealed Pb<sup>2+</sup> -induced deleterious effects on plasma membrane of head and acrosome including collapsed cristae in mitochondria.</p><p><strong>Conclusions: </strong>Pb<sup>2+</sup> not only mimics Ca<sup>2+</sup> but also affects cellular targets involved in generation of cAMP, mitochondrial transmembrane potential, and ionic exchange. Lead seems to interact with Ca<sup>2+</sup> channels because of charge similarity and probably enters the sperm cell through these channels and results in hyperpolarization. Our findings also indicate lead-induced TP and intracellular Ca<sup>2+</sup> release in spermatozoa which in turn may be responsible for premature acrosome exocytosis which is essential feature of capacitation for fertilization. Thus, lead seems to reduce the fertilizing capacity of spermatozoa even at 0.5 ppm concentrations.</p>","PeriodicalId":9084,"journal":{"name":"Biological Research","volume":null,"pages":null},"PeriodicalIF":4.3000,"publicationDate":"2024-07-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11225213/pdf/","citationCount":"0","resultStr":"{\"title\":\"Lead and calcium crosstalk tempted acrosome damage and hyperpolarization of spermatozoa: signaling and ultra-structural evidences.\",\"authors\":\"Rajkumar Singh Yadav, Bhawna Kushawaha, Rahul Dhariya, Dilip Kumar Swain, Brijesh Yadav, Mukul Anand, Priyambada Kumari, Pradeep Kumar Rai, Dipty Singh, Sarvajeet Yadav, Satish Kumar Garg\",\"doi\":\"10.1186/s40659-024-00517-x\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><strong>Background: </strong>Exposure of humans and animals to heavy metals is increasing day-by-day; thus, lead even today remains of significant public health concern. According to CDC, blood lead reference value (BLRV) ranges from 3.5 µg/dl to 5 μg/dl in adults. Recently, almost 2.6% decline in male fertility per year has been reported but the cause is not well established. Lead (Pb<sup>2+</sup>) affects the size of testis, semen quality, and secretory functions of prostate. But the molecular mechanism(s) of lead toxicity in sperm cells is not clear. Thus, present study was undertaken to evaluate the adverse effects of lead acetate at environmentally relevant exposure levels (0.5, 5, 10 and 20 ppm) on functional and molecular dynamics of spermatozoa of bucks following in vitro exposure for 15 min and 3 h.</p><p><strong>Results: </strong>Lead significantly decreased motility, viable count, and motion kinematic patterns of spermatozoa like curvilinear velocity, straight-line velocity, average path velocity, beat cross frequency and maximum amplitude of head lateral displacement even at 5 ppm concentration. Pb<sup>2+</sup> modulated intracellular cAMP and Ca<sup>2+</sup> levels in sperm cells through L-type calcium channels and induced spontaneous or premature acrosome reaction (AR) by increasing tyrosine phosphorylation of sperm proteins and downregulated mitochondrial transmembrane potential. Lead significantly increased DNA damage and apoptosis as well. Electron microscopy studies revealed Pb<sup>2+</sup> -induced deleterious effects on plasma membrane of head and acrosome including collapsed cristae in mitochondria.</p><p><strong>Conclusions: </strong>Pb<sup>2+</sup> not only mimics Ca<sup>2+</sup> but also affects cellular targets involved in generation of cAMP, mitochondrial transmembrane potential, and ionic exchange. Lead seems to interact with Ca<sup>2+</sup> channels because of charge similarity and probably enters the sperm cell through these channels and results in hyperpolarization. Our findings also indicate lead-induced TP and intracellular Ca<sup>2+</sup> release in spermatozoa which in turn may be responsible for premature acrosome exocytosis which is essential feature of capacitation for fertilization. Thus, lead seems to reduce the fertilizing capacity of spermatozoa even at 0.5 ppm concentrations.</p>\",\"PeriodicalId\":9084,\"journal\":{\"name\":\"Biological Research\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":4.3000,\"publicationDate\":\"2024-07-05\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11225213/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Biological Research\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1186/s40659-024-00517-x\",\"RegionNum\":2,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Biological Research","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1186/s40659-024-00517-x","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOLOGY","Score":null,"Total":0}
引用次数: 0

摘要

背景:人类和动物接触重金属的机会与日俱增,因此,即使在今天,铅仍然是公众健康的重大问题。根据美国疾病预防控制中心(CDC)的数据,成人血铅参考值(BLRV)为 3.5 µg/dl 至 5 μg/dl。最近有报道称,男性生育能力每年下降近 2.6%,但原因尚未明确。铅(Pb2+)会影响睾丸大小、精液质量和前列腺的分泌功能。但铅对精子细胞毒性的分子机制尚不清楚。因此,本研究评估了环境相关暴露水平(0.5、5、10 和 20 ppm)的醋酸铅在体外暴露 15 分钟和 3 小时后对雄鹿精子功能和分子动力学的不利影响:结果:铅明显降低了精子的运动能力、存活率和运动模式,如曲线速度、直线速度、平均路径速度、搏动交叉频率和头部横向位移的最大振幅,即使在百万分之 5 的浓度下也是如此。铅通过 L 型钙通道调节精子细胞内的 cAMP 和 Ca2+ 水平,并通过增加精子蛋白质的酪氨酸磷酸化和下调线粒体跨膜电位诱导自发或过早顶体反应(AR)。铅还会明显增加 DNA 损伤和细胞凋亡。电子显微镜研究显示,铅对精子头部和顶体的质膜产生有害影响,包括线粒体嵴的塌陷:结论:Pb2+不仅能模拟 Ca2+,还能影响细胞中参与产生 cAMP、线粒体跨膜电位和离子交换的靶点。由于电荷的相似性,铅似乎与 Ca2+ 通道相互作用,可能通过这些通道进入精子细胞并导致超极化。我们的研究结果还表明,铅诱导精子的 TP 和细胞内 Ca2+ 释放,这反过来又可能导致顶体过早外渗,而顶体外渗是获能受精的基本特征。因此,即使在 0.5 ppm 的浓度下,铅似乎也会降低精子的受精能力。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
Lead and calcium crosstalk tempted acrosome damage and hyperpolarization of spermatozoa: signaling and ultra-structural evidences.

Background: Exposure of humans and animals to heavy metals is increasing day-by-day; thus, lead even today remains of significant public health concern. According to CDC, blood lead reference value (BLRV) ranges from 3.5 µg/dl to 5 μg/dl in adults. Recently, almost 2.6% decline in male fertility per year has been reported but the cause is not well established. Lead (Pb2+) affects the size of testis, semen quality, and secretory functions of prostate. But the molecular mechanism(s) of lead toxicity in sperm cells is not clear. Thus, present study was undertaken to evaluate the adverse effects of lead acetate at environmentally relevant exposure levels (0.5, 5, 10 and 20 ppm) on functional and molecular dynamics of spermatozoa of bucks following in vitro exposure for 15 min and 3 h.

Results: Lead significantly decreased motility, viable count, and motion kinematic patterns of spermatozoa like curvilinear velocity, straight-line velocity, average path velocity, beat cross frequency and maximum amplitude of head lateral displacement even at 5 ppm concentration. Pb2+ modulated intracellular cAMP and Ca2+ levels in sperm cells through L-type calcium channels and induced spontaneous or premature acrosome reaction (AR) by increasing tyrosine phosphorylation of sperm proteins and downregulated mitochondrial transmembrane potential. Lead significantly increased DNA damage and apoptosis as well. Electron microscopy studies revealed Pb2+ -induced deleterious effects on plasma membrane of head and acrosome including collapsed cristae in mitochondria.

Conclusions: Pb2+ not only mimics Ca2+ but also affects cellular targets involved in generation of cAMP, mitochondrial transmembrane potential, and ionic exchange. Lead seems to interact with Ca2+ channels because of charge similarity and probably enters the sperm cell through these channels and results in hyperpolarization. Our findings also indicate lead-induced TP and intracellular Ca2+ release in spermatozoa which in turn may be responsible for premature acrosome exocytosis which is essential feature of capacitation for fertilization. Thus, lead seems to reduce the fertilizing capacity of spermatozoa even at 0.5 ppm concentrations.

求助全文
通过发布文献求助,成功后即可免费获取论文全文。 去求助
来源期刊
Biological Research
Biological Research 生物-生物学
CiteScore
10.10
自引率
0.00%
发文量
33
审稿时长
>12 weeks
期刊介绍: Biological Research is an open access, peer-reviewed journal that encompasses diverse fields of experimental biology, such as biochemistry, bioinformatics, biotechnology, cell biology, cancer, chemical biology, developmental biology, evolutionary biology, genetics, genomics, immunology, marine biology, microbiology, molecular biology, neuroscience, plant biology, physiology, stem cell research, structural biology and systems biology.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信