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Sanguinarine caused larval lethality and growth inhibition by suppressing energy metabolism in silkworms, Bombyx mori

Sanguinarine (Sang) is a natural alkaloid and distributed in several plants of Papaveraceae. The antitumor, antioxidant, antimicrobial and anti-inflammatory effects of Sang were extensively reported, but its speciality and mechanism against Lepidoptera insects were still unknown. In this study, deta...

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Published in:Pesticide biochemistry and physiology 2019-10, Vol.160, p.154-162
Main Authors: Li, Ping, Hu, Jing-wei, Wen, Chao-wei, Hang, Yang, Zhou, Zhuo-hua, Xie, Min, Lv, Jia-cheng, Wang, Chun-meng, Huang, Ying-Hao, Xu, Jia-ping, Deng, Ming-jie
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cited_by cdi_FETCH-LOGICAL-c362t-4810675c51436b7f24c770f32b351a4a30ecddf3998125ef8b17899e536ca6c03
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container_title Pesticide biochemistry and physiology
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creator Li, Ping
Hu, Jing-wei
Wen, Chao-wei
Hang, Yang
Zhou, Zhuo-hua
Xie, Min
Lv, Jia-cheng
Wang, Chun-meng
Huang, Ying-Hao
Xu, Jia-ping
Deng, Ming-jie
description Sanguinarine (Sang) is a natural alkaloid and distributed in several plants of Papaveraceae. The antitumor, antioxidant, antimicrobial and anti-inflammatory effects of Sang were extensively reported, but its speciality and mechanism against Lepidoptera insects were still unknown. In this study, detailed toxicological parameters of Sang against silkworms, Bombyx mori (B. mori), were determined by a toxicological test. Then, a nuclear magnetic resonance-based (NMR) metabolomics method was adopted to analyze the changes in hemolymph metabolites of silkworms after feeding Sang. The growth of fourth-instar larvae was significantly ceased by the oral administration of 0.05–0.3% Sang and vast deaths appeared in 0.3% Sang group on Day 4 and Day 5. The quantitative analysis of metabolites indicated that trehalose and citrate levels in hemolymph were increased after 24 h of feeding 0.3% Sang, whereas the concentrations of pyruvate, succinate, malate and fumarate were decreased. In addition, the enzymatic determination and reverse transcription quantitative PCR (RT-qPCR) showed that the trehalase (THL) activity and the transcriptional level of one gene coding THL were uniformly weakened by 0.3% Sang. One of the important mechanisms of Sang against silkworms might be interpreted as follows. Sang impaired trehalose hydrolysis, reduced THL activity and transcription, and led to the inhibition of energy metabolism, consequent antigrowth and high lethality in larvae of B. mori. Our findings offered new insights into the insecticidal effect of Sang from the perspective of energy metabolism and provided the basis for the application of Sang in the control of Lepidoptera pests. [Display omitted] •The defensive roles of sanguinarine against the Lepidoptera insect were still unknown.•Sanguinarine significantly inhibited the growth of fourth-instar Bombyx mori larvae.•Sanguinarine targeted on trehalase and induced the systemic inhibition of energy metabolism in silkworms.•This study provided the basis for the application of Sang in the control of Lepidoptera pests.
doi_str_mv 10.1016/j.pestbp.2019.08.004
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The antitumor, antioxidant, antimicrobial and anti-inflammatory effects of Sang were extensively reported, but its speciality and mechanism against Lepidoptera insects were still unknown. In this study, detailed toxicological parameters of Sang against silkworms, Bombyx mori (B. mori), were determined by a toxicological test. Then, a nuclear magnetic resonance-based (NMR) metabolomics method was adopted to analyze the changes in hemolymph metabolites of silkworms after feeding Sang. The growth of fourth-instar larvae was significantly ceased by the oral administration of 0.05–0.3% Sang and vast deaths appeared in 0.3% Sang group on Day 4 and Day 5. The quantitative analysis of metabolites indicated that trehalose and citrate levels in hemolymph were increased after 24 h of feeding 0.3% Sang, whereas the concentrations of pyruvate, succinate, malate and fumarate were decreased. In addition, the enzymatic determination and reverse transcription quantitative PCR (RT-qPCR) showed that the trehalase (THL) activity and the transcriptional level of one gene coding THL were uniformly weakened by 0.3% Sang. One of the important mechanisms of Sang against silkworms might be interpreted as follows. Sang impaired trehalose hydrolysis, reduced THL activity and transcription, and led to the inhibition of energy metabolism, consequent antigrowth and high lethality in larvae of B. mori. Our findings offered new insights into the insecticidal effect of Sang from the perspective of energy metabolism and provided the basis for the application of Sang in the control of Lepidoptera pests. [Display omitted] •The defensive roles of sanguinarine against the Lepidoptera insect were still unknown.•Sanguinarine significantly inhibited the growth of fourth-instar Bombyx mori larvae.•Sanguinarine targeted on trehalase and induced the systemic inhibition of energy metabolism in silkworms.•This study provided the basis for the application of Sang in the control of Lepidoptera pests.</description><identifier>ISSN: 0048-3575</identifier><identifier>EISSN: 1095-9939</identifier><identifier>DOI: 10.1016/j.pestbp.2019.08.004</identifier><identifier>PMID: 31519250</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Benzophenanthridines - toxicity ; Bombyx - drug effects ; Bombyx - growth &amp; development ; Energy metabolism ; Energy Metabolism - drug effects ; Hemolymph - metabolism ; Insecticides - pharmacology ; Isoquinolines - toxicity ; Larva - drug effects ; Metabolomics ; NMR ; Sanguinarine ; Silkworm ; Trehalose</subject><ispartof>Pesticide biochemistry and physiology, 2019-10, Vol.160, p.154-162</ispartof><rights>2019 Elsevier Inc.</rights><rights>Copyright © 2019 Elsevier Inc. 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In addition, the enzymatic determination and reverse transcription quantitative PCR (RT-qPCR) showed that the trehalase (THL) activity and the transcriptional level of one gene coding THL were uniformly weakened by 0.3% Sang. One of the important mechanisms of Sang against silkworms might be interpreted as follows. Sang impaired trehalose hydrolysis, reduced THL activity and transcription, and led to the inhibition of energy metabolism, consequent antigrowth and high lethality in larvae of B. mori. Our findings offered new insights into the insecticidal effect of Sang from the perspective of energy metabolism and provided the basis for the application of Sang in the control of Lepidoptera pests. [Display omitted] •The defensive roles of sanguinarine against the Lepidoptera insect were still unknown.•Sanguinarine significantly inhibited the growth of fourth-instar Bombyx mori larvae.•Sanguinarine targeted on trehalase and induced the systemic inhibition of energy metabolism in silkworms.•This study provided the basis for the application of Sang in the control of Lepidoptera pests.</description><subject>Animals</subject><subject>Benzophenanthridines - toxicity</subject><subject>Bombyx - drug effects</subject><subject>Bombyx - growth &amp; development</subject><subject>Energy metabolism</subject><subject>Energy Metabolism - drug effects</subject><subject>Hemolymph - metabolism</subject><subject>Insecticides - pharmacology</subject><subject>Isoquinolines - toxicity</subject><subject>Larva - drug effects</subject><subject>Metabolomics</subject><subject>NMR</subject><subject>Sanguinarine</subject><subject>Silkworm</subject><subject>Trehalose</subject><issn>0048-3575</issn><issn>1095-9939</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNp9kE1v1DAQhi1ERZfCP0DIRw4kjOM4iS9ItOJLqtRDy9myncmuF8cOdtKSf0-qLRw5jTR63nk1DyFvGJQMWPPhWE6YZzOVFTBZQlcC1M_IjoEUhZRcPie7bdMVXLTinLzM-QgAsgb5gpxzJpisBOzIcqvDfnFBJxeQWr1k7KnX6V576nE-aO_mlerQ032KD_OBunBwxs0uBmpWmpdpSpizC3uKAdN-pSPO2kTv8rixNDv_8yGmMb-nl3E06286xuRekbNB-4yvn-YF-fHl893Vt-L65uv3q0_XheVNNRd1x6BphRWs5o1ph6q2bQsDrwwXTNeaA9q-H7iUHasEDp1hbSclCt5Y3VjgF-Td6e6U4q9l06VGly16rwPGJauqktDVALzZ0PqE2hRzTjioKblRp1UxUI_C1VGdhKtH4Qo6tendYm-fGhYzYv8v9NfwBnw8Abj9ee8wqWwdBou9S2hn1Uf3_4Y_OIKVqA</recordid><startdate>201910</startdate><enddate>201910</enddate><creator>Li, Ping</creator><creator>Hu, Jing-wei</creator><creator>Wen, Chao-wei</creator><creator>Hang, Yang</creator><creator>Zhou, Zhuo-hua</creator><creator>Xie, Min</creator><creator>Lv, Jia-cheng</creator><creator>Wang, Chun-meng</creator><creator>Huang, Ying-Hao</creator><creator>Xu, Jia-ping</creator><creator>Deng, Ming-jie</creator><general>Elsevier Inc</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>201910</creationdate><title>Sanguinarine caused larval lethality and growth inhibition by suppressing energy metabolism in silkworms, Bombyx mori</title><author>Li, Ping ; 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The antitumor, antioxidant, antimicrobial and anti-inflammatory effects of Sang were extensively reported, but its speciality and mechanism against Lepidoptera insects were still unknown. In this study, detailed toxicological parameters of Sang against silkworms, Bombyx mori (B. mori), were determined by a toxicological test. Then, a nuclear magnetic resonance-based (NMR) metabolomics method was adopted to analyze the changes in hemolymph metabolites of silkworms after feeding Sang. The growth of fourth-instar larvae was significantly ceased by the oral administration of 0.05–0.3% Sang and vast deaths appeared in 0.3% Sang group on Day 4 and Day 5. The quantitative analysis of metabolites indicated that trehalose and citrate levels in hemolymph were increased after 24 h of feeding 0.3% Sang, whereas the concentrations of pyruvate, succinate, malate and fumarate were decreased. In addition, the enzymatic determination and reverse transcription quantitative PCR (RT-qPCR) showed that the trehalase (THL) activity and the transcriptional level of one gene coding THL were uniformly weakened by 0.3% Sang. One of the important mechanisms of Sang against silkworms might be interpreted as follows. Sang impaired trehalose hydrolysis, reduced THL activity and transcription, and led to the inhibition of energy metabolism, consequent antigrowth and high lethality in larvae of B. mori. Our findings offered new insights into the insecticidal effect of Sang from the perspective of energy metabolism and provided the basis for the application of Sang in the control of Lepidoptera pests. [Display omitted] •The defensive roles of sanguinarine against the Lepidoptera insect were still unknown.•Sanguinarine significantly inhibited the growth of fourth-instar Bombyx mori larvae.•Sanguinarine targeted on trehalase and induced the systemic inhibition of energy metabolism in silkworms.•This study provided the basis for the application of Sang in the control of Lepidoptera pests.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>31519250</pmid><doi>10.1016/j.pestbp.2019.08.004</doi><tpages>9</tpages></addata></record>
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source Elsevier
subjects Animals
Benzophenanthridines - toxicity
Bombyx - drug effects
Bombyx - growth & development
Energy metabolism
Energy Metabolism - drug effects
Hemolymph - metabolism
Insecticides - pharmacology
Isoquinolines - toxicity
Larva - drug effects
Metabolomics
NMR
Sanguinarine
Silkworm
Trehalose
title Sanguinarine caused larval lethality and growth inhibition by suppressing energy metabolism in silkworms, Bombyx mori
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