دورية أكاديمية
أعرض في EDS

Composition and abundance of midgut plasma membrane proteins in two major hemipteran vectors of plant viruses, Bemisia tabaci and Myzus persicae.

التفاصيل البيبلوغرافية
العنوان: Composition and abundance of midgut plasma membrane proteins in two major hemipteran vectors of plant viruses, Bemisia tabaci and Myzus persicae.
المؤلفون: Jiménez J; Department of Entomology and Nematology, University of Florida, Gainesville, Florida, USA., Mishra R; Department of Entomology and Nematology, University of Florida, Gainesville, Florida, USA., Wang X; Department of Entomology and Nematology, University of Florida, Gainesville, Florida, USA., Magee CM; Department of Entomology and Nematology, University of Florida, Gainesville, Florida, USA., Bonning BC; Department of Entomology and Nematology, University of Florida, Gainesville, Florida, USA.
المصدر: Archives of insect biochemistry and physiology [Arch Insect Biochem Physiol] 2024 Jul; Vol. 116 (3), pp. e22133.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Wiley Country of Publication: United States NLM ID: 8501752 Publication Model: Print Cited Medium: Internet ISSN: 1520-6327 (Electronic) Linking ISSN: 07394462 NLM ISO Abbreviation: Arch Insect Biochem Physiol Subsets: MEDLINE
أسماء مطبوعة: Publication: New York, NY : Wiley
Original Publication: New York : Alan R. Liss, c1983-
مواضيع طبية MeSH: Insect Proteins*/metabolism , Insect Vectors*/virology , Insect Vectors*/metabolism , Aphids*/virology , Aphids*/metabolism , Plant Viruses* , Gastrointestinal Tract*/virology , Gastrointestinal Tract*/metabolism, Animals ; Membrane Proteins/metabolism ; Hemiptera/virology ; Hemiptera/metabolism ; Proteome ; Cell Membrane/metabolism
مستخلص: Multiple species within the order Hemiptera cause severe agricultural losses on a global scale. Aphids and whiteflies are of particular importance due to their role as vectors for hundreds of plant viruses, many of which enter the insect via the gut. To facilitate the identification of novel targets for disruption of plant virus transmission, we compared the relative abundance and composition of the gut plasma membrane proteomes of adult Bemisia tabaci (Hemiptera: Aleyrodidae) and Myzus persicae (Hemiptera: Aphididae), representing the first study comparing the gut plasma membrane proteomes of two different insect species. Brush border membrane vesicles were prepared from dissected guts, and proteins extracted, identified and quantified from triplicate samples via timsTOF mass spectrometry. A total of 1699 B. tabaci and 1175 M. persicae proteins were identified. Following bioinformatics analysis and manual curation, 151 B. tabaci and 115 M. persicae proteins were predicted to localize to the plasma membrane of the gut microvilli. These proteins were further categorized based on molecular function and biological process according to Gene Ontology terms. The most abundant gut plasma membrane proteins were identified. The ten plasma membrane proteins that differed in abundance between the two insect species were associated with the terms "protein binding" and "viral processes." In addition to providing insight into the gut physiology of hemipteran insects, these gut plasma membrane proteomes provide context for appropriate identification of plant virus receptors based on a combination of bioinformatic prediction and protein localization on the surface of the insect gut.
(© 2024 The Author(s). Archives of Insect Biochemistry and Physiology published by Wiley Periodicals LLC.)
References: Almagro Armenteros, J.J., Sønderby, C.K., Sønderby, S.K., Nielsen, H. & Winther, O. (2017) DeepLoc: prediction of protein subcellular localization using deep learning. Bioinformatics, 33, 3387–3395.
Bairoch, A. (2004) The universal protein resource (UniProt). Nucleic Acids Research, 33, D154–D159.
Bateman, A., Martin, M.J., Orchard, S., Magrane, M., Ahmad, S., Alpi, E. et al.The UniProt Consortium. (2023) UniProt: the universal protein knowledgebase in 2023. Nucleic Acids Research, 51, D523–D531. Available from: https://doi.org/10.1093/nar/gkac1052.
Bayyareddy, K., Zhu, X., Orlando, R. & Adang, M.J. (2012) Proteome analysis of Cry4Ba toxin‐interacting Aedes aegypti lipid rafts using geLC–MS/MS. Journal of Proteome Research, 11, 5843–5855.
Bhella, D. (2015) The role of cellular adhesion molecules in virus attachment and entry. Philosophical Transactions of the Royal Society, B: Biological Sciences, 370, 20140035. Available from: https://doi.org/10.1098/rstb.2014.0035.
Binns, D., Dimmer, E., Huntley, R., Barrell, D., O'Donovan, C. & Apweiler, R. (2009) QuickGO: a web‐based tool for gene ontology searching. Bioinformatics, 25, 3045–3046.
Blackman, R.L. & Eastop, V.F. (2000) Aphids on the world's crops: an identification and information guide, 2nd edition. Hoboken: Wiley.
Bonning, B.C. (2025) Pathogen binding and entry: molecular interactions with the insect gut. Annual Review of Entomology. Forthcoming.
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein‐dye binding. Analytical Biochemistry, 72, 248–254.
Butt, A.H., Rasool, N. & Khan, Y.D. (2017) A treatise to computational approaches towards prediction of membrane protein and its subtypes. The Journal of Membrane Biology, 250, 55–76.
Caccia, S., Casartelli, M. & Tettamanti, G. (2019) The amazing complexity of insect midgut cells: types, peculiarities, and functions. Cell and Tissue Research, 377, 505–525.
Cantalapiedra, C.P., Hernández‐Plaza, A., Letunic, I., Bork, P. & Huerta‐Cepas, J. (2021) eggNOG‐mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Molecular Biology and Evolution, 38, 5825–5829.
Charif, D. & Lobry, J.R. (2007) SeqinR 1.0‐2: a contributed package to the R project for statistical computing devoted to biological sequences retrieval and analysis. In: Bastolla, U., Porto, M., Roman, H.E. & Vendruscolo, M., (Eds.) Structural approaches to sequence evolution: molecules, networks, populations. Berlin, Heidelberg: Springer. pp. 207–232 in: https://doi.org/10.1007/978-3-540-35306-5_10.
Collins, M.P. & Forgac, M. (2020) Regulation and function of V‐ATPases in physiology and disease. Biochimica et Biophysica Acta (BBA) ‐ Biomembranes, 1862, 183341. Available from: https://doi.org/10.1016/j.bbamem.2020.183341.
Czosnek, H., Hariton‐Shalev, A., Sobol, I., Gorovits, R. & Ghanim, M. (2017) The incredible journey of begomoviruses in their whitefly vector. Viruses, 9, 273.
DeBlasio, S.L., Wilson, J.R., Tamborindeguy, C., Johnson, R.S., Pinheiro, P.V., MacCoss, M.J. et al. (2021) Affinity purification–mass spectrometry identifies a novel interaction between a polerovirus and a conserved innate immunity aphid protein that regulates transmission efficiency. Journal of Proteome Research, 20, 3365–3387. Available from: https://doi.org/10.1021/acs.jproteome.1c00313.
Delang, L., Paeshuyse, J. & Neyts, J. (2012) The role of phosphatidylinositol 4‐kinases and phosphatidylinositol 4‐phosphate during viral replication. Biochemical Pharmacology, 84, 1400–1408. Available from: https://doi.org/10.1016/j.bcp.2012.07.034.
Doellinger, J., Schneider, A., Hoeller, M. & Lasch, P. (2020) Sample preparation by easy extraction and digestion (SPEED)‐a universal, rapid, and detergent‐free protocol for proteomics based on acid extraction. Molecular & Cellular Proteomics, 19, 209–222.
Drysdale, R., FlyBase Consortium. (2008) FlyBase: a database for the Drosophila research community. Methods in Molecular Biology, 420, 45–59. Available from: https://doi.org/10.1007/978-1-59745-583-1_3.
Fan, Y.‐Y., Chi, Y., Chen, N., Cuellar, W.J. & Wang, X.‐W. (2024) Role of aminopeptidase N‐like in the acquisition of begomoviruses by Bemisia tabaci, the whitefly vector. Insect Science, 31(3), 707–719. https://doi.org/10.1111/1744-7917.13336.
Farhan, H. & Hsu, V.W. (2016) Cdc42 and cellular polarity: emerging roles at the Golgi. Trends in Cell Biology, 26, 241–248. Available from: https://doi.org/10.1016/j.tcb.2015.11.003.
Fereres, A. & Raccah, B. (2015) Plant virus transmission by insects, Encyclopedia of Life Sciences. John Wiley & Sons, Ltd. pp. 1–12. https://doi.org/10.1002/9780470015902.a0000760.pub3.
Gao, H., Shi, W. & Freund, L.B. (2005) Mechanics of receptor‐mediated endocytosis. Proceedings of the National Academy of Sciences of the United States of America, 102, 9469–9474. Available from: https://doi.org/10.1073/pnas.0503879102.
Ghosh, S., Bello, V.H. & Ghanim, M. (2021) Transmission parameters of pepper whitefly‐borne vein yellows virus (PeWBVYV) by Bemisia tabaci and identification of an insect protein with a putative role in polerovirus transmission. Virology, 560, 54–65.
Ghosh, S. & Ghanim, M. (2021) Factors determining transmission of persistent viruses by Bemisia tabaci and emergence of new virus–vector relationships. Viruses, 13, 1808.
Gíslason, M.H., Nielsen, H., Almagro Armenteros, J.J. & Johansen, A.R. (2021) Prediction of GPI‐anchored proteins with pointer neural networks. Current Research in Biotechnology, 3, 6–13.
Gray, S. & Gildow, F.E. (2003) Luteovirus‐aphid interactions. Annual Review of Phytopathology, 41, 539–566. Available from: https://doi.org/10.1146/annurev.phyto.41.012203.105815.
Hogenhout, S.A., Ammar, E.‐D., Whitfield, A.E. & Redinbaugh, M.G. (2008) Insect vector interactions with persistently transmitted viruses. Annual Review of Phytopathology, 46, 327–359. Available from: https://doi.org/10.1146/annurev.phyto.022508.092135.
Holtof, M., Lenaerts, C., Cullen, D. & Vanden Broeck, J. (2019) Extracellular nutrient digestion and absorption in the insect gut. Cell and Tissue Research, 377, 397–414.
Huang, D.W., Sherman, B.T. & Lempicki, R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols, 4, 44–57.
Huerta‐Cepas, J., Szklarczyk, D., Heller, D., Hernández‐Plaza, A., Forslund, S.K., Cook, H. et al. (2019) eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Research, 47, D309–D314.
Javed, M.A., Coutu, C., Theilmann, D.A., Erlandson, M.A. & Hegedus, D.D. (2019) Proteomics analysis of Trichoplusia ni midgut epithelial cell brush border membrane vesicles. Insect science, 26, 424–440.
Johnson, S.A.S., Mandavia, N., Wang, H.‐D. & Johnson, D.L. (2000) Transcriptional regulation of the TATA‐binding protein by ras cellular signaling. Molecular and Cellular Biology, 20, 5000–5009. Available from: https://doi.org/10.1128/MCB.20.14.5000-5009.2000.
Jones, B.D., Paterson, H.F., Hall, A. & Falkow, S. (1993) Salmonella typhimurium induces membrane ruffling by a growth factor‐receptor‐independent mechanism. Proceedings of the National Academy of Sciences of the United States of America, 90, 10390–10394. Available from: https://doi.org/10.1073/pnas.90.21.10390.
Jones, T., Naslavsky, N. & Caplan, S. (2020) Eps15 homology domain protein 4 (EHD4) is required for Eps15 homology domain protein 1 (EHD1)‐mediated endosomal recruitment and fission. PLoS One, 15, e0239657. Available from: https://doi.org/10.1371/journal.pone.0239657.
Jurat‐Fuentes, J.L., Heckel, D.G. & Ferré, J. (2021) Mechanisms of resistance to insecticidal proteins from Bacillus thuringiensis. Annual Review of Entomology, 66, 121–140. Available from: https://doi.org/10.1146/annurev-ento-052620-073348.
Kall, L., Krogh, A. & Sonnhammer, E.L.L. (2007) Advantages of combined transmembrane topology and signal peptide prediction—the Phobius web server. Nucleic Acids Research, 35, W429–W432.
Letunic, I., Khedkar, S. & Bork, P. (2021) SMART: recent updates, new developments and status in 2020. Nucleic Acids Research, 49, D458–D460. Available from: https://doi.org/10.1093/nar/gkaa937.
Linz, L.B., Liu, S., Chougule, N.P. & Bonning, B.C. (2015) In vitro evidence supports membrane alanyl aminopeptidase N as a receptor for a plant virus in the pea aphid vector. Journal of Virology, 89, 11203–11212. Available from: https://doi.org/10.1128/JVI.01479-15.
Liu, S., Sivakumar, S., Sparks, W.O., Miller, W.A. & Bonning, B.C. (2010) A peptide that binds the pea aphid gut impedes entry of pea enation mosaic virus into the aphid hemocoel. Virology, 401, 107–116. Available from: https://doi.org/10.1016/j.virol.2010.02.009.
Ma, W., Zhang, Z., Peng, C., Wang, X., Li, F. & Lin, Y. (2012) Exploring the midgut transcriptome and brush border membrane vesicle proteome of the rice stem borer, Chilo suppressalis (Walker). PLoS One, 7, e38151.
Mateo, M., Generous, A., Sinn, P.L. & Cattaneo, R. (2015) Connections matter − how viruses use cell–cell adhesion components. Journal of Cell Science, 128, 431–439. Available from: https://doi.org/10.1242/jcs.159400.
Meier, F., Beck, S., Grassl, N., Lubeck, M., Park, M.A., Raether, O. et al. (2015) Parallel accumulation–serial fragmentation (PASEF): multiplying sequencing speed and sensitivity by synchronized scans in a trapped ion mobility device. Journal of Proteome Research, 14, 5378–5387.
Meier, F., Brunner, A.‐D., Koch, S., Koch, H., Lubeck, M., Krause, M. et al. (2018) Online parallel accumulation–serial fragmentation (PASEF) with a novel trapped ion mobility mass spectrometer. Molecular & Cellular Proteomics, 17, 2534–2545.
Mohanta, T.K., Sharma, N., Arina, P. & Defilippi, P. (2020) Molecular insights into the MAPK cascade during viral infection: potential crosstalk between HCQ and HCQ analogues. BioMed Research International, 2020, 8827752.
Mulot, M., Monsion, B., Boissinot, S., Rastegar, M., Meyer, S., Bochet, N. et al. (2018) Transmission of turnip yellows virus by Myzus persicae is reduced by feeding aphids on double‐stranded RNA targeting the ephrin receptor protein. Frontiers in Microbiology, 9, 457. Available from: https://doi.org/10.3389/fmicb.2018.00457.
Nasuhidehnavi, A., Zhao, Y., Punetha, A., Hemphill, A., Li, H. & Bechtel, T.J. et al. (2022) A role for Basigin in Toxoplasma gondii infection. Infection & Immunity, 90(8), e00205‐22.
Navas‐Castillo, J., Fiallo‐Olivé, E. & Sánchez‐Campos, S. (2011) Emerging virus diseases transmitted by whiteflies. Annual Review of Phytopathology, 49, 219–248. Available from: https://doi.org/10.1146/annurev-phyto-072910-095235.
Nesvizhskii, A.I., Keller, A., Kolker, E. & Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Analytical Chemistry, 75, 4646–4658.
Ng, J.C.K. & Perry, K.L. (2004) Transmission of plant viruses by aphid vectors. Molecular Plant Pathology, 5, 505–511. Available from: https://doi.org/10.1111/j.1364-3703.2004.00240.x.
Ning, W., Jiang, P., Guo, Y., Wang, C., Tan, X., Zhang, W. et al. (2021) GPS‐Palm: a deep learning‐based graphic presentation system for the prediction of S‐palmitoylation sites in proteins. Briefings in Bioinformatics, 22, 1836–1847.
O'Leary, N.A., Wright, M.W., Brister, J.R., Ciufo, S., Haddad, D., Mcveigh, R. et al. (2016) Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Research, 44, D733–D745.
Okada, A.K., Teranishi, K., Ambroso, M.R., Isas, J.M., Vazquez‐Sarandeses, E., Lee, J.‐Y. et al. (2021) Lysine acetylation regulates the interaction between proteins and membranes. Nature Communications, 12, 6466. Available from: https://doi.org/10.1038/s41467-021-26657-2.
Pauchet, Y., Muck, A., Svatoš, A. & Heckel, D.G. (2009) Chromatographic and electrophoretic resolution of proteins and protein complexes from the larval midgut microvilli of Manduca sexta. Insect Biochemistry and Molecular Biology, 39, 467–474.
Pierleoni, A., Martelli, P.L. & Casadio, R. (2008) PredGPI: a GPI‐anchor predictor. BMC Bioinformatics, 9, 392.
Polston, J.E. & Anderson, P.K. (1997) The emergence of whitefly‐transmitted geminiviruses in tomato in the western hemisphere. Plant Disease, 81, 1358–1369. Available from: https://doi.org/10.1094/PDIS.1997.81.12.1358.
Popova‐Butler, A. & Dean, D.H. (2009) Proteomic analysis of the mosquito Aedes aegypti midgut brush border membrane vesicles. Journal of Insect Physiology, 55, 264–272.
Qin, F., Liu, W., Wu, N., Zhang, L., Zhang, Z., Zhou, X. et al. (2018) Invasion of midgut epithelial cells by a persistently transmitted virus is mediated by sugar transporter 6 in its insect vector. PLoS Pathogens, 14, e1007201.
Savojardo, C., Martelli, P.L., Fariselli, P., Profiti, G. & Casadio, R. (2018) BUSCA: an integrative web server to predict subcellular localization of proteins. Nucleic Acids Research, 46, W459–W466.
Sayers, E.W., Bolton, E.E., Brister, J.R., Canese, K., Chan, J., Comeau, D.C. et al. (2021) Database resources of The National Center for Biotechnology Information. Nucleic Acids Research, 50, D20–D26. Available from: https://doi.org/10.1093/nar/gkab1112.
Sherman, B.T., Hao, M., Qiu, J., Jiao, X., Baseler, M.W., Lane, H.C. et al. (2022) DAVID: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update). Nucleic Acids Research, 50, W216–W221.
Stelzer, G., Rosen, N., Plaschkes, I., Zimmerman, S., Twik, M. & Fishilevich, S. et al. (2016) The GeneCards suite: from gene data mining to disease genome sequence analyses. Current Protocols in Bioinformatics, 54, 1.30.1–1.30.33.
Szklarczyk, D., Kirsch, R., Koutrouli, M., Nastou, K., Mehryary, F., Hachilif, R. et al. (2023) The STRING database in 2023: protein‐protein association networks and functional enrichment analyses for any sequenced genome of interest. Nucleic Acids Research, 51, D638–D646. Available from: https://doi.org/10.1093/nar/gkac1000.
Tavares, C.S., Mishra, R., Ghobrial, P.N. & Bonning, B.C. (2022) Composition and abundance of midgut surface proteins in the Asian citrus psyllid, Diaphorina citri. Journal of Proteomics, 261, 104580.
Thurmond, J., Goodman, J.L., Strelets, V.B., Attrill, H., Gramates, L.S., Marygold, S.J. et al. (2019) FlyBase 2.0: the next generation. Nucleic Acids Research, 47, D759–D765.
Valero‐Rello, A., Baeza‐Delgado, C., Andreu‐Moreno, I. & Sanjuán, R. (2024) Cellular receptors for mammalian viruses. PLoS Pathogens, 20, e1012021. Available from: https://doi.org/10.1371/journal.ppat.1012021.
Varma, A. & Malathi, V.G. (2003) Emerging geminivirus problems: a serious threat to crop production. Annals of Applied Biology, 142, 145–164. Available from: https://doi.org/10.1111/j.1744-7348.2003.tb00240.x.
Villegas‐Coronado, D., Guzman‐Partida, A.M., Aispuro‐Hernandez, E., Vazquez‐Moreno, L., Huerta‐Ocampo, J.Á., Sarabia‐Sainz, J.A. et al. (2022) Characterization and expression of prohibitin during the Mexican bean weevil (Zabrotes subfasciatus, Boheman, 1833) larvae development. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 262, 110770.
Wang, H., Wu, K., Liu, Y., Wu, Y. & Wang, X. (2015) Integrative proteomics to understand the transmission mechanism of barley yellow dwarf virus‐GPV by its insect vector Rhopalosiphum padi. Scientific Reports, 5, 10971. Available from: https://doi.org/10.1038/srep10971.
Watarai, M., Kamata, Y., Kozaki, S. & Sasakawa, C. (1997) rho, a small GTP‐Binding protein, is essential for shigella invasion of epithelial cells. The Journal of Experimental Medicine, 185, 281–292. Available from: https://doi.org/10.1084/jem.185.2.281.
Wickham, H., Averick, M., Bryan, J., Chang, W., McGowan, L., François, R. et al. (2019) Welcome to the Tidyverse. Journal of Open Source Software, 4, 1686. Available from: https://doi.org/10.21105/joss.01686.
Wolfersberger, M.G. (1993) Preparation and partial characterization of amino acid transporting brush border membrane vesicles from the larval midgut of the gypsy moth (Lymantria dispar). Archives of Insect Biochemistry and Physiology, 24, 139–147. Available from: https://doi.org/10.1002/arch.940240304.
Wu, C., Yang, C., Wang, Y., Wang, J. & Zhu, J. (2023) Molecular characterization and functional analysis of the dipeptidyl peptidase IV from venom of the ectoparasitoid Scleroderma guani. Toxins, 15, 311. Available from: https://doi.org/10.3390/toxins15050311.
Wu, C.H. (2006) The universal protein resource (UniProt): an expanding universe of protein information. Nucleic Acids Research, 34, D187–D191.
Yuan, C., Ding, X., Xia, L., Yin, J., Huang, S. & Huang, F. (2011) Proteomic analysis of BBMV in Helicoverpa armigera midgut with and without Cry1Ac toxin treatment. Biocontrol Science and Technology, 21, 139–151.
Zhang, Y., Wen, Z., Washburn, M.P. & Florens, L. (2010) Refinements to label free proteome quantitation: how to deal with peptides shared by multiple proteins. Analytical Chemistry, 82, 2272–2281. Available from: https://doi.org/10.1021/ac9023999.
Zhao, J., Chi, Y., Zhang, X.‐J., Wang, X.‐W. & Liu, S.‐S. (2019) Implication of whitefly vesicle associated membrane protein‐associated protein B in the transmission of tomato yellow leaf curl virus. Virology, 535, 210–217. Available from: https://doi.org/10.1016/j.virol.2019.07.007.
Zhao, J., Lei, T., Zhang, X.‐J., Yin, T.‐Y., Wang, X.‐W. & Liu, S.‐S. (2020) A vector whitefly endocytic receptor facilitates the entry of begomoviruses into its midgut cells via binding to virion capsid proteins. PLoS Pathogens, 16, e1009053. Available from: https://doi.org/10.1371/journal.ppat.1009053.
Zybailov, B., Mosley, A.L., Sardiu, M.E., Coleman, M.K., Florens, L. & Washburn, M.P. (2006) Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. Journal of Proteome Research, 5, 2339–2347. Available from: https://doi.org/10.1021/pr060161n.
معلومات مُعتمدة: 2310815 National Science Foundation; IIP-1821914 National Science Foundation
فهرسة مساهمة: Keywords: Hemiptera; gut receptors; insect gut; plant virus; proteome; whitefly
المشرفين على المادة: 0 (Insect Proteins)
0 (Membrane Proteins)
0 (Proteome)
تواريخ الأحداث: Date Created: 20240726 Date Completed: 20240726 Latest Revision: 20240726
رمز التحديث: 20240726
DOI: 10.1002/arch.22133
PMID: 39054788
قاعدة البيانات: MEDLINE
الوصف
تدمد:1520-6327
DOI:10.1002/arch.22133