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Zinc alters behavioral phenotypes, neurotransmitter signatures, and immune homeostasis in male zebrafish (Danio rerio)
Anthropogenic activities discharge zinc into aquatic ecosystems, and the effects of long-term and low-concentration zinc exposure on fish behavior are unclear. We evaluated the behavior and physiology of male zebrafish (Danio rerio) after a 6-week exposure to 1.0 or 1.5 ppm (mg/L) zinc chloride. The...
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Published in: | The Science of the total environment 2022-07, Vol.828, p.154099-154099, Article 154099 |
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creator | Yu, Fan Hou, Zhi-Shuai Luo, Hong-Rui Cui, Xue-Fan Xiao, Jun Kim, Young-Bum Li, Jian-Lin Feng, Wen-Rong Tang, Yong-Kai Li, Hong-Xia Su, Sheng-Yan Song, Chang-You Wang, Mei-Yao Xu, Pao |
description | Anthropogenic activities discharge zinc into aquatic ecosystems, and the effects of long-term and low-concentration zinc exposure on fish behavior are unclear. We evaluated the behavior and physiology of male zebrafish (Danio rerio) after a 6-week exposure to 1.0 or 1.5 ppm (mg/L) zinc chloride. The exposure caused anxiety-like behaviors and altered the social preferences in both exposure groups. Analysis of transcriptional changes suggested that in the brain, zinc exerted heterogenetic effects on immune and neurotransmitter functions. Exposure to 1.0 ppm zinc chloride resulted in constitutive immune dyshomeostasis, while exposure to 1.5 ppm zinc chloride impaired the neurotransmitter glutamate. In the intestine, zinc dysregulated self-renewal of intestinal cells, a potential loss of defense function. Moreover, exposure to 1.5 ppm zinc chloride suppressed intestinal immune functions and dysregulated tyrosine metabolism. These behavioral alterations suggested that the underlying mechanisms were distinct and concentration-specific. Overall, environmental levels of zinc can alter male zebrafish behaviors by dysregulating neurotransmitter and immunomodulation signatures.
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•Environmental levels of zinc can alter zebrafish behaviors.•Zinc can exhibit dose-dependent effects on immunomodulation.•Zinc exposure dysregulates neurotransmitter signatures of brain and intestine.•Effects of zinc on aquatic organisms are underestimated and warrant future research. |
doi_str_mv | 10.1016/j.scitotenv.2022.154099 |
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•Environmental levels of zinc can alter zebrafish behaviors.•Zinc can exhibit dose-dependent effects on immunomodulation.•Zinc exposure dysregulates neurotransmitter signatures of brain and intestine.•Effects of zinc on aquatic organisms are underestimated and warrant future research.</description><identifier>ISSN: 0048-9697</identifier><identifier>EISSN: 1879-1026</identifier><identifier>DOI: 10.1016/j.scitotenv.2022.154099</identifier><identifier>PMID: 35240190</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Animals ; Behavior ; Behavior, Animal ; Danio rerio ; Ecosystem ; Homeostasis ; Immunomodulation ; Male ; Neurotransmitter ; Neurotransmitter Agents - metabolism ; Phenotype ; Physiology ; Water Pollutants, Chemical - metabolism ; Zebrafish - physiology ; Zinc - metabolism ; Zinc exposure</subject><ispartof>The Science of the total environment, 2022-07, Vol.828, p.154099-154099, Article 154099</ispartof><rights>2022 Elsevier B.V.</rights><rights>Copyright © 2022 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c371t-e0e0fbbfcdcff09253295cf7da6a7e553668bf8c7a1b758dcb74b635d572f3a83</citedby><cites>FETCH-LOGICAL-c371t-e0e0fbbfcdcff09253295cf7da6a7e553668bf8c7a1b758dcb74b635d572f3a83</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27923,27924</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35240190$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yu, Fan</creatorcontrib><creatorcontrib>Hou, Zhi-Shuai</creatorcontrib><creatorcontrib>Luo, Hong-Rui</creatorcontrib><creatorcontrib>Cui, Xue-Fan</creatorcontrib><creatorcontrib>Xiao, Jun</creatorcontrib><creatorcontrib>Kim, Young-Bum</creatorcontrib><creatorcontrib>Li, Jian-Lin</creatorcontrib><creatorcontrib>Feng, Wen-Rong</creatorcontrib><creatorcontrib>Tang, Yong-Kai</creatorcontrib><creatorcontrib>Li, Hong-Xia</creatorcontrib><creatorcontrib>Su, Sheng-Yan</creatorcontrib><creatorcontrib>Song, Chang-You</creatorcontrib><creatorcontrib>Wang, Mei-Yao</creatorcontrib><creatorcontrib>Xu, Pao</creatorcontrib><title>Zinc alters behavioral phenotypes, neurotransmitter signatures, and immune homeostasis in male zebrafish (Danio rerio)</title><title>The Science of the total environment</title><addtitle>Sci Total Environ</addtitle><description>Anthropogenic activities discharge zinc into aquatic ecosystems, and the effects of long-term and low-concentration zinc exposure on fish behavior are unclear. We evaluated the behavior and physiology of male zebrafish (Danio rerio) after a 6-week exposure to 1.0 or 1.5 ppm (mg/L) zinc chloride. The exposure caused anxiety-like behaviors and altered the social preferences in both exposure groups. Analysis of transcriptional changes suggested that in the brain, zinc exerted heterogenetic effects on immune and neurotransmitter functions. Exposure to 1.0 ppm zinc chloride resulted in constitutive immune dyshomeostasis, while exposure to 1.5 ppm zinc chloride impaired the neurotransmitter glutamate. In the intestine, zinc dysregulated self-renewal of intestinal cells, a potential loss of defense function. Moreover, exposure to 1.5 ppm zinc chloride suppressed intestinal immune functions and dysregulated tyrosine metabolism. These behavioral alterations suggested that the underlying mechanisms were distinct and concentration-specific. Overall, environmental levels of zinc can alter male zebrafish behaviors by dysregulating neurotransmitter and immunomodulation signatures.
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•Environmental levels of zinc can alter zebrafish behaviors.•Zinc can exhibit dose-dependent effects on immunomodulation.•Zinc exposure dysregulates neurotransmitter signatures of brain and intestine.•Effects of zinc on aquatic organisms are underestimated and warrant future research.</description><subject>Animals</subject><subject>Behavior</subject><subject>Behavior, Animal</subject><subject>Danio rerio</subject><subject>Ecosystem</subject><subject>Homeostasis</subject><subject>Immunomodulation</subject><subject>Male</subject><subject>Neurotransmitter</subject><subject>Neurotransmitter Agents - metabolism</subject><subject>Phenotype</subject><subject>Physiology</subject><subject>Water Pollutants, Chemical - metabolism</subject><subject>Zebrafish - physiology</subject><subject>Zinc - metabolism</subject><subject>Zinc exposure</subject><issn>0048-9697</issn><issn>1879-1026</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNqFkMFO3DAQhq0KVBbaVwAfqUS2thPbyRFRaCsh9VIuXCzbGbNeJfZiOyvB0zfRAtfOZQ7z_TOaD6ELStaUUPF9u87Wl1gg7NeMMLamvCFd9wmtaCu7ihImjtCKkKatOtHJE3Sa85bMJVv6GZ3UnDWEdmSF9o8-WKyHAiljAxu99zHpAe82EGJ52UG-wgGmFEvSIY--zCDO_inoMqVlqEOP_ThOAfAmjhBz0dln7AMe9QD4FUzSzucNvvyhg484QfLx2xd07PSQ4etbP0MPd7d_b35V939-_r65vq9sLWmpgABxxjjbW-dIx3jNOm6d7LXQEjivhWiNa63U1Eje9tbIxoia91wyV-u2PkOXh727FJ8nyEWNPlsYBh0gTlkxUQvasJYvqDygNsWcEzi1S37U6UVRohbpaqs-pKtFujpIn5Pnb0cmM0L_kXu3PAPXBwDmV_ce0rIIgoXeJ7BF9dH_98g_ZRGa_Q</recordid><startdate>20220701</startdate><enddate>20220701</enddate><creator>Yu, Fan</creator><creator>Hou, Zhi-Shuai</creator><creator>Luo, Hong-Rui</creator><creator>Cui, Xue-Fan</creator><creator>Xiao, Jun</creator><creator>Kim, Young-Bum</creator><creator>Li, Jian-Lin</creator><creator>Feng, Wen-Rong</creator><creator>Tang, Yong-Kai</creator><creator>Li, Hong-Xia</creator><creator>Su, Sheng-Yan</creator><creator>Song, Chang-You</creator><creator>Wang, Mei-Yao</creator><creator>Xu, Pao</creator><general>Elsevier B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20220701</creationdate><title>Zinc alters behavioral phenotypes, neurotransmitter signatures, and immune homeostasis in male zebrafish (Danio rerio)</title><author>Yu, Fan ; Hou, Zhi-Shuai ; Luo, Hong-Rui ; Cui, Xue-Fan ; Xiao, Jun ; Kim, Young-Bum ; Li, Jian-Lin ; Feng, Wen-Rong ; Tang, Yong-Kai ; Li, Hong-Xia ; Su, Sheng-Yan ; Song, Chang-You ; Wang, Mei-Yao ; Xu, Pao</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c371t-e0e0fbbfcdcff09253295cf7da6a7e553668bf8c7a1b758dcb74b635d572f3a83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Animals</topic><topic>Behavior</topic><topic>Behavior, Animal</topic><topic>Danio rerio</topic><topic>Ecosystem</topic><topic>Homeostasis</topic><topic>Immunomodulation</topic><topic>Male</topic><topic>Neurotransmitter</topic><topic>Neurotransmitter Agents - metabolism</topic><topic>Phenotype</topic><topic>Physiology</topic><topic>Water Pollutants, Chemical - metabolism</topic><topic>Zebrafish - physiology</topic><topic>Zinc - metabolism</topic><topic>Zinc exposure</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yu, Fan</creatorcontrib><creatorcontrib>Hou, Zhi-Shuai</creatorcontrib><creatorcontrib>Luo, Hong-Rui</creatorcontrib><creatorcontrib>Cui, Xue-Fan</creatorcontrib><creatorcontrib>Xiao, Jun</creatorcontrib><creatorcontrib>Kim, Young-Bum</creatorcontrib><creatorcontrib>Li, Jian-Lin</creatorcontrib><creatorcontrib>Feng, Wen-Rong</creatorcontrib><creatorcontrib>Tang, Yong-Kai</creatorcontrib><creatorcontrib>Li, Hong-Xia</creatorcontrib><creatorcontrib>Su, Sheng-Yan</creatorcontrib><creatorcontrib>Song, Chang-You</creatorcontrib><creatorcontrib>Wang, Mei-Yao</creatorcontrib><creatorcontrib>Xu, Pao</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>The Science of the total environment</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yu, Fan</au><au>Hou, Zhi-Shuai</au><au>Luo, Hong-Rui</au><au>Cui, Xue-Fan</au><au>Xiao, Jun</au><au>Kim, Young-Bum</au><au>Li, Jian-Lin</au><au>Feng, Wen-Rong</au><au>Tang, Yong-Kai</au><au>Li, Hong-Xia</au><au>Su, Sheng-Yan</au><au>Song, Chang-You</au><au>Wang, Mei-Yao</au><au>Xu, Pao</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Zinc alters behavioral phenotypes, neurotransmitter signatures, and immune homeostasis in male zebrafish (Danio rerio)</atitle><jtitle>The Science of the total environment</jtitle><addtitle>Sci Total Environ</addtitle><date>2022-07-01</date><risdate>2022</risdate><volume>828</volume><spage>154099</spage><epage>154099</epage><pages>154099-154099</pages><artnum>154099</artnum><issn>0048-9697</issn><eissn>1879-1026</eissn><abstract>Anthropogenic activities discharge zinc into aquatic ecosystems, and the effects of long-term and low-concentration zinc exposure on fish behavior are unclear. We evaluated the behavior and physiology of male zebrafish (Danio rerio) after a 6-week exposure to 1.0 or 1.5 ppm (mg/L) zinc chloride. The exposure caused anxiety-like behaviors and altered the social preferences in both exposure groups. Analysis of transcriptional changes suggested that in the brain, zinc exerted heterogenetic effects on immune and neurotransmitter functions. Exposure to 1.0 ppm zinc chloride resulted in constitutive immune dyshomeostasis, while exposure to 1.5 ppm zinc chloride impaired the neurotransmitter glutamate. In the intestine, zinc dysregulated self-renewal of intestinal cells, a potential loss of defense function. Moreover, exposure to 1.5 ppm zinc chloride suppressed intestinal immune functions and dysregulated tyrosine metabolism. These behavioral alterations suggested that the underlying mechanisms were distinct and concentration-specific. Overall, environmental levels of zinc can alter male zebrafish behaviors by dysregulating neurotransmitter and immunomodulation signatures.
[Display omitted]
•Environmental levels of zinc can alter zebrafish behaviors.•Zinc can exhibit dose-dependent effects on immunomodulation.•Zinc exposure dysregulates neurotransmitter signatures of brain and intestine.•Effects of zinc on aquatic organisms are underestimated and warrant future research.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>35240190</pmid><doi>10.1016/j.scitotenv.2022.154099</doi><tpages>1</tpages></addata></record> |
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subjects | Animals Behavior Behavior, Animal Danio rerio Ecosystem Homeostasis Immunomodulation Male Neurotransmitter Neurotransmitter Agents - metabolism Phenotype Physiology Water Pollutants, Chemical - metabolism Zebrafish - physiology Zinc - metabolism Zinc exposure |
title | Zinc alters behavioral phenotypes, neurotransmitter signatures, and immune homeostasis in male zebrafish (Danio rerio) |
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