Transcriptome profiling analysis reveals the role of latrophilin in controlling development, reproduction and insecticide susceptibility in Tribolium castaneum

Transcriptome profiling analysis reveals the role of latrophilin in controlling development,... Latrophilin of Tribolium castaneum (Tclph) has been reported to play crucial roles in growth, development and reproduction. However, the regulatory mechanism of Tclph associated with these physiology processes is unknown. Thus, the global transcriptome profiles between RNAi treated (ds-Tclph) and control larvae of T. castaneum were analyzed by RNA-sequencing. Totally, 274 differentially expressed genes (DEGs) were identified between the ds-Tclph and control samples. These DEGs were classified into 42 GO functional groups, including developmental process, reproduction and stress response. The results indicated that knockdown of Tclph disturbed the antioxidant activity process, and partially inhibited the serine protease (SP) and lipase signaling pathways to regulate the development and reproduction as well as the decreasing of the stress response in T. castaneum. Additionally, knockdown of Tclph suppressed IMD immunity pathways which likely modulated the effects of Tclph on stress response. Interestingly, CSPs, ESTs, CYPs, AOXs and BGs were significantly down-regulated in ds-Tclph larvae, implying that they cooperated with Tclph to reduce the activity of cellular metabolism system. FMOs was up-regulated in ds-Tclph insects suggested it may be involved in detoxifying alkaloid of insect metabolism system. These results implied that Tclph participated in phase 0, I and II cellular detoxification. Furthermore, RNAi against Tclph increased larval susceptibility to carbamates and organophosphates insecticides, supporting that Tclph was indeed involved into the insecticide susceptibility in T. castaneum. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Genetica Springer Journals

Transcriptome profiling analysis reveals the role of latrophilin in controlling development, reproduction and insecticide susceptibility in Tribolium castaneum

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Publisher
Springer International Publishing
Copyright
Copyright © 2018 by Springer International Publishing AG, part of Springer Nature
Subject
Life Sciences; Animal Genetics and Genomics; Plant Genetics and Genomics; Evolutionary Biology; Human Genetics; Microbial Genetics and Genomics
ISSN
0016-6707
eISSN
1573-6857
D.O.I.
10.1007/s10709-018-0020-4
Publisher site
See Article on Publisher Site

Abstract

Latrophilin of Tribolium castaneum (Tclph) has been reported to play crucial roles in growth, development and reproduction. However, the regulatory mechanism of Tclph associated with these physiology processes is unknown. Thus, the global transcriptome profiles between RNAi treated (ds-Tclph) and control larvae of T. castaneum were analyzed by RNA-sequencing. Totally, 274 differentially expressed genes (DEGs) were identified between the ds-Tclph and control samples. These DEGs were classified into 42 GO functional groups, including developmental process, reproduction and stress response. The results indicated that knockdown of Tclph disturbed the antioxidant activity process, and partially inhibited the serine protease (SP) and lipase signaling pathways to regulate the development and reproduction as well as the decreasing of the stress response in T. castaneum. Additionally, knockdown of Tclph suppressed IMD immunity pathways which likely modulated the effects of Tclph on stress response. Interestingly, CSPs, ESTs, CYPs, AOXs and BGs were significantly down-regulated in ds-Tclph larvae, implying that they cooperated with Tclph to reduce the activity of cellular metabolism system. FMOs was up-regulated in ds-Tclph insects suggested it may be involved in detoxifying alkaloid of insect metabolism system. These results implied that Tclph participated in phase 0, I and II cellular detoxification. Furthermore, RNAi against Tclph increased larval susceptibility to carbamates and organophosphates insecticides, supporting that Tclph was indeed involved into the insecticide susceptibility in T. castaneum.

Journal

Genetica – Springer Journals

Published: May 24, 2018

References

  • Beetle immunity: identification of immune-inducible genes from the model insect Tribolium castaneum
    Altincicek, B; Knorr, E; Vilcinskas, A
  • The role of reactive oxygen species in Anopheles aquasalis response to Plasmodium vivax infection
    Bahia, AC; Oliveira, JH; Kubota, MS; Araujo, HR; Lima, JB; Rios-Velasquez, CM; Lacerda, MV; Oliveira, PL; Traub-Cseko, YM; Pimenta, PF
  • Identification of G protein-coupled receptors required for vitellogenin uptake into the oocytes of the red flour beetle, Tribolium castaneum
    Bai, H; Palli, SR
  • Large-scale RNAi screen of G protein-coupled receptors involved in larval growth, molting and metamorphosis in the red flour beetle
    Bai, H; Zhu, F; Shah, K; Palli, SR
  • RNA interference of dual oxidase in the plant nematode Meloidogyne incognita
    Bakhetia, M; Charlton, W; Atkinson, HJ; Mcpherson, MJ
  • Evidence for trade-offs in detoxification and chemosensation gene signatures in Plutella xylostella
    Bautista, MA; Bhandary, B; Wijeratne, AJ; Michel, AP; Hoy, CW; Mittapalli, O
  • Genotype–phenotype relationship in three cases with overlapping 19p13.12 microdeletions
    Bonaglia, MC; Marelli, S; Novara, F; Commodaro, S; Borgatti, R; Minardo, G; Memo, L; Mangold, E; Beri, S; Zucca, C
  • Microarray analysis of differentially expressed genes in rat frontal cortex under chronic risperidone treatment
    Chen, M-L; Chen, C-H
  • Comparative RNA-sequencing profiling reveals novel Delta-class glutathione S-transferases relative genes expression patterns in Tribolium castaneum
    Chen, X; Xiong, W; Li, C; Gao, S; Song, X; Wei, W; Li, B
  • Mosquito cathepsin B-like protease involved in embryonic degradation of vitellin is produced as a latent extraovarian precursor
    Cho, W-L; Tsao, S-M; Hays, AR; Walter, R; Chen, J-S; Snigirevskaya, ES; Raikhel, AS
  • Oxidation of ranitidine by isozymes of flavin-containing monooxygenase and cytochrome P450
    Chung, WG; Park, CS; Roh, HK; Lee, WK; Cha, YN
  • Molecular characterization of the amplified aldehyde oxidase from insecticide resistant Culex quinquefasciatus
    Coleman, M; Vontas, JG; Hemingway, J
  • Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research
    Conesa, A; Gotz, S; Garcia-Gomez, JM; Terol, J; Talon, M; Robles, M
  • Tribolium castaneum immune defense genes are differentially expressed in response to Bacillus thuringiensis toxins sharing common receptor molecules and exhibiting disparate toxicity
    Contreras, E; Benito-Jardon, M; Lopez-Galiano, MJ; Real, MD; Rausell, C
  • Integrated disinfection by-products (DBP) mixtures research: gene expression alterations in primary rat hepatocyte cultures exposed to DBP mixtures formed by chlorination and ozonation/postchlorination
    Crosby, LM; Simmons, JE; Ward, WO; Moore, TM; Morgan, KT; DeAngelo, AB
  • Immune and stress response ‘cross-talk’ in the Drosophila Malpighian tubule
    Davies, SA; Overend, G; Sebastian, S; Cundall, M; Cabrero, P; Dow, JA; Terhzaz, S
  • Isolation and biochemical characterization of a Ca2+-independent α-latrotoxin-binding protein
    Davletov, BA; Shamotienko, OG; Lelianova, VG; Grishin, EV; Ushkaryov, YA
  • Short-term high fat-feeding results in morphological and metabolic adaptations in the skeletal muscle of C57BL/6J mice
    Wilde, J; Mohren, R; Berg, S; Boekschoten, M; Dijk, KW; De, GP; Müller, M; Mariman, E; Smit, E
  • Gene expression in the liver of rats fed alcohol by means of intragastric infusion
    Deaciuc, IV; Arteel, GE; Peng, X; Hill, DB; Mcclain, CJ
  • Influence of catalase gene silencing on the survivability of Sitobion avenae
    Deng, F; Zhao, Z
  • Suppressing a peroxidase gene reduces survival in the wheat aphid Sitobion avenae
    Deng, F; He, Q; Zhao, Z
  • iBeetle-Base: a database for RNAi phenotypes in the red flour beetle Tribolium castaneum
    Dönitz, J; Schmitt-Engel, C; Grossmann, D; Gerischer, L; Tech, M; Schoppmeier, M; Klingler, M; Bucher, G
  • Latrophilin-2 is a novel component of the epithelial-mesenchymal transition within the atrioventricular canal of the embryonic chicken heart
    Doyle, SE; Scholz, MJ; Greer, KA; Hubbard, AD; Darnell, DK; Antin, PB; Klewer, SE; Runyan, RB
  • Dynamics of immune system gene expression upon bacterial challenge and wounding in a social insect (Bombus terrestris)
    Erler, S; Popp, M; Lattorff, HM
  • Downregulation of the Musca domestica peptidoglycan recognition protein SC (PGRP-SC) leads to overexpression of antimicrobial peptides and tardy pupation
    Gao, Y; Tang, T; Gu, J; Sun, L; Gao, X; Ma, X; Wang, X; Liu, F; Wang, J
  • Identification and evolution of latrophilin receptor gene involved in Tribolium castaneum development and female fecundity
    Gao, S; Liu, X; Liu, J; Xiong, W; Song, X; Wei, W; Wei, L; Li, B
  • Characterization of glutathione-S-transferases in zebrafish (Danio rerio)
    Glisic, B; Mihaljevic, I; Popovic, M; Zaja, R; Loncar, J; Fent, K; Kovacevic, R; Smital, T
  • Sp22D: a multidomain serine protease with a putative role in insect immunity
    Gorman, MJ; Andreeva, OV; Paskewitz, SM
  • Tiger moths and woolly bears. Behaviour, ecology, and evolution of the Arctiidae
    Hartmann, T
  • Viperin interaction with mitochondrial antiviral signaling protein (MAVS) limits viperin-mediated inhibition of the interferon response in macrophages
    Hee, JS; Cresswell, P
  • Changes in cysteine protease activity and localization during midgut metamorphosis in the crucifer root maggot (Delia radicum)
    Hegedus, D; O’Grady, M; Chamankhah, M; Baldwin, D; Gleddie, S; Braun, L; Erlandson, M
  • Aberrant epigenetic modifications of LPHN2 function as a potential cisplatin-specific biomarker for human gastrointestinal cancer
    Jeon, MS; Song, SH; Yun, J; Kang, JY; Kim, HP; Han, SW; Kim, TY
  • Modeling cognitive endophenotypes of schizophrenia in mice
    Kellendonk, C; Simpson, EH; Kandel, ER
  • Role of DUOX in gut inflammation: lessons from Drosophila model of gut-microbiota interactions
    Kim, SH; Lee, WJ
  • The ADHD-susceptibility gene lphn3.1 modulates dopaminergic neuron formation and locomotor activity during zebrafish development
    Lange, M; Norton, W; Coolen, M; Chaminade, M; Merker, S; Proft, F; Schmitt, A; Vernier, P; Lesch, KP; Bally-Cuif, L
  • Latrophilin signaling links anterior–posterior tissue polarity and oriented cell divisions in the C. elegans embryo
    Langenhan, T; Prömel, S; Mestek, L; Esmaeili, B; Waller-Evans, H; Hennig, C; Kohara, Y; Avery, L; Vakonakis, I; Schnabel, R; Russ, AP
  • Identification and functional characterization of viperin of amphioxus Branchiostoma japonicum: Implications for ancient origin of viperin-mediated antiviral response
    Lei, M; Liu, H; Liu, S; Zhang, Y; Zhang, S
  • Activation of alpha-latrotoxin receptors in neuromuscular synapses leads to a prolonged splash acetylcholine release
    Lelyanova, VG; Thomson, D; Ribchester, RR; Tonevitsky, EA; Ushkaryov, YA
  • Comparative RNA-sequencing analysis of mthl1 functions and signal transductions in Tribolium castaneum
    Li, C; Wu, W; Sang, M; Liu, X; Hu, X; Yun, X; Li, B
  • Methuselah-like genes affect development, stress resistance, lifespan and reproduction in Tribolium castaneum
    Li, C; Zhang, Y; Yun, X; Wang, Y; Sang, M; Liu, X; Hu, X; Li, B
  • Molecular characterization and expression pattern of four chemosensory proteins from diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae)
    Liu, X; Luo, Q; Zhong, G; Rizwan-Ul-Haq, M; Hu, M
  • Biotype expression and insecticide response of Bemisia tabaci chemosensory protein-1
    Liu, GX; Xuan, N; Chu, D; Xie, HY; Fan, ZX; Bi, YP; Picimbon, JF; Qin, YC; Zhong, ST; Li, YF; Gao, ZL; Pan, WL; Wang, GY; Rajashekar, B
  • Cholinergic and non-cholinergic functions of two acetylcholinesterase genes revealed by gene-silencing in Tribolium castaneum
    Lu, Y; Park, Y; Gao, X; Zhang, X; Yao, J; Pang, YP; Jiang, H; Zhu, KY
  • From the black widow spider to human behavior: Latrophilins, a relatively unknown class of G protein-coupled receptors, are implicated in psychiatric disorders
    Martinez, AF; Muenke, M; Arcos-Burgos, M
  • An ultraconserved brain-specific enhancer within ADGRL3 (LPHN3) underpins attention-deficit/hyperactivity disorder susceptibility
    Martinez, AF; Yu, A; Hong, S; Molyneux, K; Yarnell, D; Löhr, H; Driever, W; Acosta, MT; Arcos-Burgos, M; Muenke, M
  • The latrophilin family: multiply spliced G protein-coupled receptors with differential tissue distribution
    Matsushita, H; Lelianova, VG; Ushkaryov, YA
  • Latrophilin is required for toxicity of black widow spider venom in Caenorhabditis elegans
    Mee, CJ; Tomlinson, SR; Perestenko, PV; Pomerai, D; Duce, IR; Usherwood, PN; Bell, DR
  • Latrophilins updated
    Mezaaguilar, DG; Boucard, AA
  • The classification of esterases: an important gene family involved in insecticide resistance—a review
    Montella, IR; Schama, R; Valle, D
  • Larval environmental stress alters Aedes aegypti competence for Sindbis virus
    Muturi, EJ; Kim, CH; Alto, BW; Berenbaum, MR; Schuler, MA
  • Gene expression changes induced in the testis by transplacental exposure to high and low doses of 17{alpha}-ethynyl estradiol, genistein, or bisphenol A
    Naciff, JM; Hess, KA; Overmann, GJ; Torontali, SM; Carr, GJ; Tiesman, JP; Foertsch, LM; Richardson, BD; Martinez, JE; Daston, GP
  • The emerging mutational landscape of G proteins and G-protein-coupled receptors in cancer
    O’Hayre, M; Vázquezprado, J; Kufareva, I; Stawiski, EW; Handel, TM; Seshagiri, S; Gutkind, JS
  • Microarray analysis reveals strategies of Tribolium castaneum larvae to compensate for cysteine and serine protease inhibitors
    Oppert, B; Elpidina, EN; Toutges, M; Mazumdar-Leighton, S
  • RNA interference and dietary inhibitors induce a similar compensation response in Tribolium castaneum larvae
    Perkin, LC; Elpidina, EN; Oppert, B
  • The neuroprotective action of the mood stabilizing drugs lithium chloride and sodium valproate is mediated through the up-regulation of the homeodomain protein Six1
    Plant, KE; Anderson, E; Simecek, N; Brown, R; Forster, S; Spinks, J; Toms, N; Gibson, GG; Lyon, J; Plant, N
  • Identification and evolution of two insulin receptor genes involved in Tribolium castaneum development and reproduction
    Sang, M; Li, C; Wu, W; Li, B
  • Rhodnius prolixus supergene families of enzymes potentially associated with insecticide resistance
    Schama, R; Pedrini, N; Juárez, MP; Nelson, DR; Torres, AQ; Valle, D; Mesquita, RD
  • The adhesion GPCR latrophilin/CIRL shapes mechanosensation
    Scholz, N; Gehring, J; Guan, C; Ljaschenko, D; Fischer, R; Lakshmanan, V; Kittel, RJ; Langenhan, T
  • Mechano-dependent signaling by Latrophilin/CIRL quenches cAMP in proprioceptive neurons
    Scholz, N; Guan, C; Nieberler, M; Grotemeyer, A; Maiellaro, I; Gao, S; Beck, S; Pawlak, M; Sauer, M; Asan, E
  • Mating activates the heme peroxidase HPX15 in the sperm storage organ to ensure fertility in Anopheles gambiae
    Shaw, WR; Teodori, E; Mitchell, SN; Baldini, F; Gabrieli, P; Rogers, DW; Catteruccia, F
  • The latrophilins, “split-personality” receptors
    Silva, JP; Ushkaryov, YA
  • Statistical significance for genomewide studies
    Storey, JD; Tibshirani, R
  • Expression of functional neuronal receptor latrophilin 1 in human acute myeloid leukaemia cells
    Sumbayev, VV; Gonçalves, SI; Blackburn, J; Gibbs, BF; Yasinska, IM; Garrett, MD; Tonevitsky, AG; Ushkaryov, YA
  • Molecular cloning of cDNA for the 29kDa proteinase participating in decomposition of the larval fat body during metamorphosis of Sarcophaga peregrina (flesh fly)
    Takahashi, N; Kurata, S; Natori, S
  • Genetically modifying the insect gut microbiota to control Chagas disease vectors through systemic RNAi
    Taracena, ML; Oliveira, PL; Almendares, O; Umana, C; Lowenberger, C; Dotson, EM; Paiva-Silva, GO; Pennington, PM
  • Preoviposition activation of cathepsin-like proteinases in degenerating ovarian follicles of the mosquito Culex pipiens pallens
    Uchida, K; Ohmori, D; Ueno, T; Nishizuka, M; Eshita, Y; Fukunaga, A; Kominami, E
  • Beta-glucuronidase activity is a sensitive biomarker to assess low-level organophosphorus insecticide exposure
    Ueyama, J; Satoh, T; Kondo, T; Takagi, K; Shibata, E; Goto, M; Kimata, A; Saito, I; Hasegawa, T; Wakusawa, S
  • Deletion of the mitochondrial superoxide dismutase sod-2 extends lifespan in Caenorhabditis elegans
    Van, RJM; Siegfried, H
  • ADHD-associated dopamine transporter, latrophilin and neurofibromin share a dopamine-related locomotor signature in Drosophila
    Voet, MVD; Harich, B; Franke, B; Schenck, A
  • Age-related differences in the disposition of nicotine and metabolites in rat brain and plasma
    Vieira-Brock, PL; Andrenyak, DM; Nielsen, SM; Fleckenstein, AE; Wilkins, DG
  • Latrophilin, neurexin, and their signaling-deficient mutants facilitate alpha-latrotoxin insertion into membranes but are not involved in pore formation
    Volynski, KE; Meunier, FA; Lelianova, VG; Dudina, EE; Volkova, TM; Rahman, MA; Manser, C; Grishin, EV; Dolly, JO; Ashley, RH
  • Initial characterization of mice null for Lphn3, a gene implicated in ADHD and addiction
    Wallis, D; Hill, DS; Mendez, IA; Abbott, LC; Finnell, RH; Wellman, PJ; Setlow, B
  • Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission
    Wang, J; Wu, Y; Yang, G; Aksoy, S
  • DEGseq: an R package for identifying differentially expressed genes from RNA-seq data
    Wang, L; Feng, Z; Wang, X; Zhang, X
  • Tcmof regulates larval/pupal development and female fecundity in red flour beetle, Tribolium castaneum
    Wang, Y; Li, C; Sang, M; Li, B
  • Serine protease P-IIc is responsible for the digestion of yolk proteins at the late stage of silkworm embryogenesis
    Wang, D; Zhang, Y; Dong, Z; Guo, P; Ma, S; Guo, K; Xia, Q; Zhao, P
  • Comparative RNA-sequencing analysis of ER-based HSP90 functions and signal pathways in Tribolium castaneum
    Xiong, W; Zhai, M; Yu, X; Wei, L; Mao, J; Liu, J; Xie, J; Li, B
  • Cathepsin B-like proteinase is involved in the decomposition of the adult fat body of Helicoverpa armigera
    Yang, XM; Hou, LJ; Dong, DJ; Shao, HL; Wang, JX; Zhao, XF
  • Characterization and expression of cytoplasmic copper/zinc superoxide dismutase (CuZn SOD) gene under temperature and hydrogen peroxide (H2O2) in rotifer Brachionus calyciflorus
    Yang, J; Dong, S; Jiang, Q; Si, Q; Liu, X; Yang, J
  • WEGO: a web tool for plotting GO annotations
    Ye, J; Fang, L; Zheng, H; Zhang, Y; Chen, J; Zhang, Z; Wang, J; Li, S; Li, R; Bolund, L
  • Microarray data mining for potential selenium targets in chemoprevention of prostate cancer
    Zhang, H; Dong, Y; Zhao, H; Brooks, JD; Hawthorn, L; Nowak, N; Marshall, JR; Gao, AC; Clement, IP
  • Identification and characterization of novel ER-based hsp90 gene in the red flour beetle, Tribolium castaneum
    Zhang, Y; Gu, S; Li, C; Sang, M; Wu, W; Yun, X; Hu, X; Li, B
  • Expression of the Helicoverpa cathepsin B-like proteinase during embryonic development
    Zhao, XF; An, XM; Wang, JX; Dong, DJ; Du, XJ; Sueda, S; Kondo, H
  • Evidence of multiple/cross resistance to Bt and organophosphate insecticides in Puerto Rico population of the fall armyworm, Spodoptera frugiperda
    Zhu, YC; Blanco, CA; Portilla, M; Adamczyk, J; Luttrell, R; Huang, F
  • Characterization of an Apis cerana cerana cytochrome P450 gene (AccCYP336A1) and its roles in oxidative stresses responses
    Zhu, M; Zhang, W; Liu, F; Chen, X; Li, H; Xu, B
  • Comparative analysis of serine protease-related genes in the honey bee genome: possible involvement in embryonic development and innate immunity
    Zou, Z; Lopez, DL; Kanost, MR; Evans, JD; Jiang, H

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