Hostname: page-component-5cf477f64f-h6p2m Total loading time: 0 Render date: 2025-03-29T05:15:50.691Z Has data issue: false hasContentIssue false

BmWARS inhibits BmNPV infection via the PI3K-Akt pathway

Published online by Cambridge University Press:  24 March 2025

Jinyang Wang
Affiliation:
Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China
Xiangrui Ding
Affiliation:
Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China
Kaifang Jia
Affiliation:
Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China
Haiyu Chen
Affiliation:
Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China
Guorong An
Affiliation:
Yancheng Agricultural College, Yancheng College of Agricultural Science and Technology Vocational, Yancheng, China
Qiaoling Zhao
Affiliation:
Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China
Dongxu Shen
Affiliation:
Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China
Zhiyong Qiu
Affiliation:
Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China
Xuelian Zhang
Affiliation:
Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China
Heying Qian
Affiliation:
Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China
Dingguo Xia*
Affiliation:
Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China
*
Corresponding author: Dingguo Xia; Email: [email protected]

Abstract

Bombyx mori Tryptophanyl-tRNA synthetase (BmWARS) belongs to the family of Ic-like aminoacyl-tRNA synthetases (aaRSs), whose specific recognition of the substrate Trp, tRNA, maintains the fidelity of protein synthesis. In this study, BmWARS was cloned and characterized from the midgut of the silkworm, Bombyx mori, resulting in an open reading frame (ORF) with a full length of 1,149 bp, which can encode 382 Aa. BmWARS is localized in the cytoplasm, and is expressed in all tissues of the silkworm, with higher expression in the testis, ovary, silk gland and malpighian tubule. The expression of BmWARS was significantly up-regulated in the midgut and silk gland after infection with Bombyx mori nuclear polyhedrosis virus (BmNPV). In addition, overexpression of BmWARS inhibited BmNPV infection and replication extremely significantly, while interference with BmWARS expression promoted BmNPV infection and replication. Analysis of the immune pathways in which BmWARS may be involved revealed that the expression of the key genes of the PI3K-Akt pathway, BmPI3K, BmAkt, BmPDK1, BmeIF4E, BmS6, and p-Akt protein was significantly reduced, whereas the expression of BmPTEN, BmFoxO, and BmCaspase9 was significantly increased in the cells that overexpressed BmWARS and were infected with BmNPV. Meanwhile, the results of the study interfering with the expression of BmWARS were completely opposite to those of the study overexpressing BmWARS. This is the first report that BmWARS has antiviral effects in Bombyx mori. Moreover, BmWARS inhibits BmNPV infection and replication in Bombyx mori cells by promoting apoptosis and inhibiting cell proliferation.

Type
Research Paper
Copyright
© The Author(s), 2025. Published by Cambridge University Press.

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahn, YH, Park, S, Choi, JJ, Park, B-K, Rhee, KH, Kang, E, Ahn, S, Lee, C-H, Lee, JS, Inn, K-S, Cho, M-L, Park, S-H, Park, K, Park, HJ, Lee, J-H, Park, J-W, Kwon, NH, Shim, H, Han, BW, Kim, P, Lee, J-Y, Jeon, Y, Huh, JW, Jin, M and Kim, S (2016) Secreted tryptophanyl-tRNA synthetase as a primary defence system against infection. Nature Microbiology 2, 16191. doi:10.1038/nmicrobiol.2016.191CrossRefGoogle ScholarPubMed
Andjelković, M, Alessi, DR, Meier, R, Fernandez, A, Lamb, NJ, Frech, M, Cron, P, Cohen, P, Lucocq, JM and Hemmings, BA (1997) Role of translocation in the activation and function of protein kinase B. Journal of Biological Chemistry 272, 3151531524. doi:10.1074/jbc.272.50.31515Google ScholarPubMed
Asati, V, Mahapatra, DK and Bharti, SK (2016) PI3K/Akt/mTOR and Ras/Raf/MEK/ERK signaling pathways inhibitors as anticancer agents: Structural and pharmacological perspectives. European Journal of Medicinal Chemistry 109, 314341. doi:10.1016/j.ejmech.2016.01.012Google ScholarPubMed
Boasso, A, Herbeuval, J-P, Hardy, AW, Winkler, C and Shearer, GM (2005) Regulation of indoleamine 2,3-dioxygenase and tryptophanyl-tRNA-synthetase by CTLA-4-Fc in human CD4+ T cells. Blood 105, 15741581. doi:10.1182/blood-2004-06-2089CrossRefGoogle ScholarPubMed
Brunet, A, Datta, SR and Greenberg, ME (2001) Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Current Opinion in Neurobiology 11, 297305. doi:10.1016/s0959-4388(00)00211-7CrossRefGoogle ScholarPubMed
Chen, S, Hou, C, Bi, H, Wang, Y, Xu, J, Li, M, James, AA, Huang, Y and Tan, A (2017) Transgenic clustered regularly interspaced short palindromic repeat/cas9-mediated viral gene targeting for antiviral therapy of Bombyx mori nucleopolyhedrovirus. Journal of Virology 91, e0246516. doi:10.1128/JVI.02465-16CrossRefGoogle ScholarPubMed
Cheng, D, Zhang, L, Yang, G, Zhao, L, Peng, F, Tian, Y, Xiao, X, Chung, RT and Gong, G (2015) Hepatitis C virus NS5A drives a PTEN-PI3K/Akt feedback loop to support cell survival. Liver International 35, 16821691. doi:10.1111/liv.12733CrossRefGoogle ScholarPubMed
Chung, T-W, Lee, Y-C, Ko, J-H and Kim, C-H (2003) Hepatitis B Virus X protein modulates the expression of PTEN by inhibiting the function of p53, a transcriptional activator in liver cells. Cancer Research 63, 34533458.Google ScholarPubMed
Cooray, S (2004) The pivotal role of phosphatidylinositol 3-kinase-Akt signal transduction in virus survival. Journal of General Virology 85, 10651076. doi:10.1099/vir.0.19771-0Google ScholarPubMed
Diehl, N and Schaal, H (2013) Make yourself at home: Viral hijacking of the PI3K/Akt signaling pathway. Viruses 5, 31923212. doi:10.3390/v5123192Google ScholarPubMed
Dong, Z, Dong, F, Yu, X, Huang, L, Jiang, Y, Hu, Z, Chen, P, Lu, C and Pan, M (2018) Excision of Nucleopolyhedrovirus Form Transgenic Silkworm Using the CRISPR/Cas9 System. Frontiers in Microbiology 9, 209. doi:10.3389/fmicb.2018.00209Google ScholarPubMed
Fresno Vara, JA, Casado, E, de Castro, J, Cejas, P, Belda-Iniesta, C and González-Barón, M (2004) PI3K/Akt signalling pathway and cancer. Cancer Treatment Reviews 30, 193204. doi:10.1016/j.ctrv.2003.07.007CrossRefGoogle ScholarPubMed
Fuchs, SA, Schene, IF, Kok, G, Jansen, JM, Nikkels, PGJ, van Gassen, KLI, Terheggen-Lagro, SWJ, van der Crabben, SN, Hoeks, SE, Niers, LEM, Wolf, NI, de Vries, MC, Koolen, DA, Houwen, RHJ, Mulder, MF and van Hasselt, PM (2019) Aminoacyl-tRNA synthetase deficiencies in search of common themes. Genetics in Medicine 21, 319330. doi:10.1038/s41436-018-0048-yGoogle ScholarPubMed
Goldsmith, MR, Shimada, T and Abe, H (2005) The genetics and genomics of the silkworm, Bombyx mori. Annual Review of Entomology 50, 71100. doi:10.1146/annurev.ento.50.071803.130456CrossRefGoogle ScholarPubMed
Guo, M and Schimmel, P (2013) Essential nontranslational functions of tRNA synthetases. Nature Chemical Biology 9, 145153. doi:10.1038/nchembio.1158CrossRefGoogle ScholarPubMed
Hu, Z-G, Dong, Z-Q, Dong, -F-F, Zhu, Y, Chen, P, Lu, C and Pan, M-H (2020) Identification of a PP2A gene in Bombyx mori with antiviral function against B. mori nucleopolyhedrovirus. Insect Science 27, 687696. doi:10.1111/1744-7917.12678Google ScholarPubMed
Isobe, R, Kojima, K, Matsuyama, T, Quan, GX, Kanda, T, Tamura, T, Sahara, K, Asano, SI and Bando, H (2004) Use of RNAi technology to confer enhanced resistance to BmNPV on transgenic silkworms. Archives of Virology 149, 19311940. doi:10.1007/s00705-004-0349-0Google ScholarPubMed
Jia, K, Wang, J, Jiang, D, Zhao, Q, Shen, D, Zhang, X, Qiu, Z, Wang, Y, Lu, C and Xia, D (2024) Bombyx mori triose-phosphate transporter protein inhibits Bombyx mori nucleopolyhedrovirus infection by reducing the cell glycolysis pathway. International Journal of Biological Macromolecules 266, 131197. doi:10.1016/j.ijbiomac.2024.131197CrossRefGoogle ScholarPubMed
Jiang, L, Cheng, T, Zhao, P, Yang, Q, Wang, G, Jin, S, Lin, P, Xiao, Y and Xia, Q (2012) Resistance to BmNPV via overexpression of an exogenous gene controlled by an inducible promoter and enhancer in transgenic silkworm, Bombyx mori. Public Library of Science 7, e41838. doi:10.1371/journal.pone.0041838Google Scholar
Jiang, L, Liu, W, Guo, H, Dang, Y, Cheng, T, Yang, W, Sun, Q, Wang, B, Wang, Y, Xie, E, and Xia, Q (2019) Distinct Functions of Bombyx mori Peptidoglycan Recognition Protein 2 in Immune Responses to Bacteria and Viruses. Frontiers in Immunology 10, 776. doi:10.3389/fimmu.2019.00776CrossRefGoogle ScholarPubMed
Jiang, L and Xia, Q (2014) The progress and future of enhancing antiviral capacity by transgenic technology in the silkworm Bombyx mori.. Insect Biochemistry and Molecular Biology 48, 17. doi:10.1016/j.ibmb.2014.02.003Google ScholarPubMed
Jiang, L, Zhao, P, Cheng, T, Sun, Q, Peng, Z, Dang, Y, Wu, X, Wang, G, Jin, S, Lin, P and Xia, Q (2013) A transgenic animal with antiviral properties that might inhibit multiple stages of infection. Antiviral Research 98, 171173. doi:10.1016/j.antiviral.2013.02.015Google ScholarPubMed
Kang, X, Wang, Y, Liang, W, Tang, X, Zhang, Y, Wang, L, Zhao, P and Lu, Z (2021) Bombyx mori nucleopolyhedrovirus downregulates transcription factor BmFoxO to elevate virus infection. Developmental & Comparative Immunology 116, 103904. doi:10.1016/j.dci.2020.103904Google ScholarPubMed
Kaplan, DR, Whitman, M, Schaffhausen, B, Pallas, DC, White, M, Cantley, L and Roberts, TM (1987) Common elements in growth factor stimulation and oncogenic transformation: 85 kd phosphoprotein and phosphatidylinositol kinase activity. Cell 50, 10211029. doi:10.1016/0092-8674(87)90168-1Google ScholarPubMed
Kim, S, You, S and Hwang, D (2011) Aminoacyl-tRNA synthetases and tumorigenesis: More than housekeeping. Nature Reviews Cancer 11, 708718. doi:10.1038/nrc3124Google ScholarPubMed
Kise, Y, Lee, SW, Park, SG, Fukai, S, Sengoku, T, Ishii, R, Yokoyama, S, Kim, S and Nureki, O (2004) A short peptide insertion crucial for angiostatic activity of human tryptophanyl-tRNA synthetase. Nature Structural and Molecular Biology 11, 149156. doi:10.1038/nsmb722Google Scholar
Kisselev, L, Frolova, L and Haenni, AL (1993) Interferon inducibility of mammalian tryptophanyl-tRNA synthetase: New perspectives. Trends in Biochemical Sciences 18, 263267. doi:10.1016/0968-0004(93)90178-pCrossRefGoogle ScholarPubMed
Laplante, M and Sabatini, DM (2012) mTOR signaling in growth control and disease. Cell 149, 274293. doi:10.1016/j.cell.2012.03.017Google ScholarPubMed
Lee, H-C, Lee, E-S, Uddin, MB, Kim, T-H, Kim, J-H, Chathuranga, K, Chathuranga, WAG, Jin, M, Kim, S, Kim, C-J and Lee, J-S (2019) Released Tryptophanyl-tRNA Synthetase Stimulates Innate Immune Responses against Viral Infection. Journal Virology 93, e0129118. doi:10.1128/JVI.01291-18Google ScholarPubMed
Lee, SW, Cho, BH, Park, SG and Kim, S (2004) Aminoacyl-tRNA synthetase complexes: Beyond translation. Journal of Cell Science 117, 37253734. doi:10.1242/jcs.01342CrossRefGoogle ScholarPubMed
Lei, J, Hu, D, Xue, S, Mao, F, Obeng, E, Quan, Y and Yu, W (2019) HN1L is essential for cell growth and survival during nucleopolyhedrovirus infection in silkworm, Bombyx mori. Public Library of Science 14, e0216719. doi:10.1371/journal.pone.0216719Google ScholarPubMed
Li, F, Liu, L, Yu, X, Rensing, C and Wang, D (2022) The PI3K/AKT Pathway and PTEN Gene Are Involved in “Tree-Top Disease” of Lymantria dispar. Genes (Basel) 13, 247. doi:10.3390/genes13020247Google ScholarPubMed
Liu, M, Xie, W, Wan, X and Deng, T (2020) Clostridium butyricum protects intestinal barrier function via upregulation of tight junction proteins and activation of the Akt/mTOR signaling pathway in a mouse model of dextran sodium sulfate-induced colitis. Experimental and Therapeutic Medicine 20, 10. doi:10.3892/etm.2020.9138Google Scholar
Liu, T-H, Dong, X-L, Pan, C-X, Du, G-Y, Wu, Y-F, Yang, J-G, Chen, P, Lu, C and Pan, M-H (2016) A newly discovered member of the Atlastin family, BmAtlastin-n, has an antiviral effect against BmNPV in Bombyx mori. Scientific Reports 6, 28946. doi:10.1038/srep28946CrossRefGoogle ScholarPubMed
, P, Pan, Y, Yang, Y, Zhu, F, Li, C, Guo, Z, Yao, Q and Chen, K (2018) Discovery of anti-viral molecules and their vital functions in Bombyx mori. Journal of Invertebrate Pathology 154, 1218. doi:10.1016/j.jip.2018.02.012Google ScholarPubMed
Manning, BD and Toker, A (2017) AKT/PKB Signaling: Navigating the Network. Cell 169, 381405. doi:10.1016/j.cell.2017.04.001Google ScholarPubMed
Mei, X, Li, C, Peng, P, Wang, J, He, E, Qiu, Z, Xia, D, Zhao, Q and Shen, D (2022) Bombyx mori C-Type Lectin (BmIML-2) Inhibits the Proliferation of B. mori Nucleopolyhedrovirus (BmNPV) through Involvement in Apoptosis. International Journal of Molecular Sciences 23, 8369. doi:10.3390/ijms23158369Google ScholarPubMed
Obenauer, JC, Cantley, LC and Yaffe, MB (2003) Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Research 31, 36353641. doi:10.1093/nar/gkg584Google ScholarPubMed
Polcicova, K, Badurova, L and Tomaskova, J (2020) Metabolic reprogramming as a feast for virus replication. Acta virologica 64, 201215. doi:10.4149/av_2020_210CrossRefGoogle ScholarPubMed
Porta, C, Paglino, C and Mosca, A (2014) Targeting PI3K/Akt/mTOR Signaling in Cancer. Frontiers in Oncology 4, 64. doi:10.3389/fonc.2014.00064CrossRefGoogle ScholarPubMed
Qian, H, Guo, H, Zhang, X, Liu, M, Zhao, G, Xu, A and Li, G (2022) Metabolic characterization of hemolymph in Bombyx mori varieties after Bombyx mori nucleopolyhedrovirus infection by GC-MS-based metabolite profiling. Archives of Virology 167, 16371648. doi:10.1007/s00705-022-05463-1Google ScholarPubMed
Rubio Gomez, MA and Ibba, M (2020) Aminoacyl-tRNA synthetases. RNA 26, 910936. doi:10.1261/rna.071720.119Google ScholarPubMed
Sajish, M, Zhou, Q, Kishi, S, Valdez, DM, Kapoor, M, Guo, M, Lee, S, Kim, S, Yang, X-L and Schimmel, P (2012) Trp-tRNA synthetase bridges DNA-PKcs to PARP-1 to link IFN-γ and p53 signaling. Nature Chemical Biology 8, 547554. doi:10.1038/nchembio.937CrossRefGoogle ScholarPubMed
Scheid, MP, Parsons, M and Woodgett, JR (2005) Phosphoinositide-dependent phosphorylation of PDK1 regulates nuclear translocation. Molecular and Cellular Biology 25, 23472363. doi:10.1128/MCB.25.6.2347-2363.2005CrossRefGoogle ScholarPubMed
Seshaiah, P and Andrew, DJ (1999) WRS-85D: A tryptophanyl-tRNA synthetase expressed to high levels in the developing Drosophila salivary gland. Molecular Biology of the Cell 10, 15951608. doi:10.1091/mbc.10.5.1595Google ScholarPubMed
Shen, N, Zhou, M, Yang, B, Yu, Y, Dong, X and Ding, J (2008) Catalytic mechanism of the tryptophan activation reaction revealed by crystal structures of human tryptophanyl-tRNA synthetase in different enzymatic states. Nucleic Acids Research 36, 12881299. doi:10.1093/nar/gkm1153CrossRefGoogle ScholarPubMed
Stitt, TN, Drujan, D, Clarke, BA, Panaro, F, Timofeyva, Y, Kline, WO, Gonzalez, M, Yancopoulos, GD and Glass, DJ (2004) The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Molecular Cell 14, 395403. doi:10.1016/s1097-2765(04)00211-4Google ScholarPubMed
Thai, M, Graham, NA, Braas, D, Nehil, M, Komisopoulou, E, Kurdistani, SK, McCormick, F, Graeber, TG and Christofk, HR (2014) Adenovirus E4ORF1-Induced MYC Activation Promotes Host Cell Anabolic Glucose Metabolism and Virus Replication. Cell Metabolism 19, 694701. doi:10.1016/j.cmet.2014.03.009Google ScholarPubMed
Thaker, SK, Ch’ng, J and Christofk, HR (2019) Viral hijacking of cellular metabolism. BMC Biology 17, 59. doi:10.1186/s12915-019-0678-9Google ScholarPubMed
Ueki, K, Yamamoto-Honda, R, Kaburagi, Y, Yamauchi, T, Tobe, K, Burgering, BM, Coffer, PJ, Komuro, I, Akanuma, Y, Yazaki, Y and Kadowaki, T (1998) Potential role of protein kinase B in insulin-induced glucose transport, glycogen synthesis, and protein synthesis. Ournal of Biological Chemistry 273, 53155322. doi:10.1074/jbc.273.9.5315Google ScholarPubMed
Vanhaesebroeck, B, Guillermet-Guibert, J, Graupera, M and Bilanges, B (2010) The emerging mechanisms of isoform-specific PI3K signalling. Nature Reviews Molecular Cell Biology 11, 329341. doi:10.1038/nrm2882CrossRefGoogle ScholarPubMed
Wakasugi, K (2007) Human tryptophanyl-tRNA synthetase binds with heme to enhance its aminoacylation activity. Biochemistry 46, 1129111298. doi:10.1021/bi7012068Google ScholarPubMed
Wang, L, Harris, TE and Lawrence, JC (2008) Regulation of proline-rich Akt substrate of 40 kDa (PRAS40) function by mammalian target of rapamycin complex 1 (mTORC1)-mediated phosphorylation. Ournal of Biological Chemistry 283, 1561915627. doi:10.1074/jbc.M800723200Google ScholarPubMed
Whitman, M, Kaplan, DR, Schaffhausen, B, Cantley, L and Roberts, TM (1985) Association of phosphatidylinositol kinase activity with polyoma middle-T competent for transformation. Nature 315, 239242. doi:10.1038/315239a0CrossRefGoogle ScholarPubMed
Wu, M-S, Yen, H-R, Chang, C-W, Peng, T-Y, Hsieh, C-F, Chen, C-J, Lin, T-Y and Horng, J-T (2011) Mechanism of action of the suppression of influenza virus replication by Ko-Ken Tang through inhibition of the phosphatidylinositol 3-kinase/Akt signaling pathway and viral RNP nuclear export. Journal of Ethnopharmacology 134, 614623. doi:10.1016/j.jep.2011.01.005Google ScholarPubMed
Xia, D, Jiang, D, Yu, P, Jia, K, Wang, J, Shen, D, Zhao, Q and Lu, C (2024) Ras3 in Bombyx mori with antiviral function against B. mori nucleopolyhedrovirus. Developmental & Comparative Immunology 152, 105114. doi:10.1016/j.dci.2023.105114CrossRefGoogle ScholarPubMed
Xiao, W, Yang, Y, Weng, Q, Lin, T, Yuan, M, Yang, K and Pang, Y (2009) The role of the PI3K-Akt signal transduction pathway in Autographa californica multiple nucleopolyhedrovirus infection of Spodoptera frugiperda cells. Virology 391, 8389. doi:10.1016/j.virol.2009.06.007Google ScholarPubMed
Xiong, X, Tao, R, DePinho, RA and Dong, XC (2013) Deletion of hepatic FoxO1/3/4 genes in mice significantly impacts on glucose metabolism through downregulation of gluconeogenesis and upregulation of glycolysis. Public Library of Science 8, e74340. doi:10.1371/journal.pone.0074340Google ScholarPubMed
Xiong, Y, Lei, Q-Y, Zhao, S and Guan, K-L (2011) Regulation of glycolysis and gluconeogenesis by acetylation of PKM and PEPCK. Cold Spring Harbor Symposia on Quantitative Biology 76, 285289. doi:10.1101/sqb.2011.76.010942Google ScholarPubMed
Xu, ZJ, Love, ML, Ma, LY, Blum, M, Bronskill, PM, Bernstein, J, Grey, AA, Hofmann, T, Camerman, N and Wong, JT (1989) Tryptophanyl-tRNA synthetase from Bacillus subtilis. Characterization and role of hydrophobicity in substrate recognition. Ournal of Biological Chemistry 264, 43044311.Google ScholarPubMed
Yang, X-L, Guo, M, Kapoor, M, Ewalt, KL, Otero, FJ, Skene, RJ, McRee, DE and Schimmel, P (2007) Functional and crystal structure analysis of active site adaptations of a potent anti-angiogenic human tRNA synthetase. Structure 15, 793805. doi:10.1016/j.str.2007.05.009Google ScholarPubMed
Yao, P and Fox, PL (2013) Aminoacyl-tRNA synthetases in medicine and disease. EMBO Molecular Medicine 5, 332343. doi:10.1002/emmm.201100626Google Scholar
Zhang, C, Lin, X, Zhao, Q, Wang, Y, Jiang, F, Ji, C, Li, Y, Gao, J, Li, J and Shen, L (2020) YARS as an oncogenic protein that promotes gastric cancer progression through activating PI3K-Akt signaling. Journal of Cancer Research and Clinical Oncology 146, 329342. doi:10.1007/s00432-019-03115-7Google Scholar
Zhang, P, Wang, J, Lu, Y, Hu, Y, Xue, R, Cao, G and Gong, C (2014) Resistance of transgenic silkworm to BmNPV could be improved by silencing ie-1 and lef-1 genes. Gene Therapy 21, 8188. doi:10.1038/gt.2013.60CrossRefGoogle ScholarPubMed
Zhang, Q, Wu, Y-F, Chen, P, Liu, T-H, Dong, Z-Q, Lu, C and Pan, M-H (2021) Bombyx mori cell division cycle protein 37 promotes the proliferation of BmNPV. Pesticide Biochemistry and Physiology 178, 104923. doi:10.1016/j.pestbp.2021.104923CrossRefGoogle ScholarPubMed
Zhou, M, Dong, X, Shen, N, Zhong, C and Ding, J (2010) Crystal structures of Saccharomyces cerevisiae tryptophanyl-tRNA synthetase: New insights into the mechanism of tryptophan activation and implications for anti-fungal drug design. Nucleic Acids Research 38, 33993413. doi:10.1093/nar/gkp1254CrossRefGoogle ScholarPubMed