Academic Journal
LincRNA_XR209691.3 could promote Bombyx mori nucleopolyhedrovirus replication by interacting with BmHSP70.
| Title: | LincRNA_XR209691.3 could promote Bombyx mori nucleopolyhedrovirus replication by interacting with BmHSP70. |
|---|---|
| Authors: | Lin S; School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China., Yin HT; School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China., Zhao ZM; School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China., Chen ZK; School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China., Zhou XM; School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China., Zhang ZD; School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China., Guo XJ; 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 Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, China., Zhao WG; 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 Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, China., Wu P; 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 Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, China. |
| Source: | Insect molecular biology [Insect Mol Biol] 2023 Apr; Vol. 32 (2), pp. 160-172. Date of Electronic Publication: 2022 Dec 16. |
| Publication Type: | Journal Article; Research Support, Non-U.S. Gov't |
| Language: | English |
| Journal Info: | Publisher: Blackwell Scientific For The Royal Entomological Society Country of Publication: England NLM ID: 9303579 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-2583 (Electronic) Linking ISSN: 09621075 NLM ISO Abbreviation: Insect Mol Biol Subsets: MEDLINE |
| Imprint Name(s): | Publication: Oxford : Blackwell Scientific For The Royal Entomological Society Original Publication: Oxford : Published for the Royal Entomological Society by Blackwell Scientific Publications, c1992- |
| MeSH Terms: | Nucleopolyhedroviruses*/physiology , Bombyx*/genetics , RNA, Long Noncoding*, Insect Proteins/metabolism ; Actins/metabolism ; Animals |
| Abstract: | Long non-coding RNAs (lncRNAs), a class of transcripts exceeding 200 nucleotides and lacking protein coding potential, have been proven to play important roles in viral infection and host immunity. Bombyx mori nucleopolyhedrovirus (BmNPV) is an important pathogen, which causes the silkworm disease and leads to a huge challenge to the sericultural industry. At present, research on the roles of insect lncRNAs in host-virus interaction are relatively few. In this study, we explored the function of lincRNA_XR209691.3 that was significantly up-regulated in the silkworm fat body upon BmNPV infection. Firstly, the subcellular localization experiment confirmed that lincRNA_XR209691.3 was present in both the nucleus and cytoplasm. Enhancing the expression of lincRNA_XR209691.3 in BmN cells could promote the proliferation of BmNPV, while inhibition of lincRNA_XR209691.3 by RNA interference suppresses the proliferation of BmNPV. Combining RNA pull-down and mass spectrometry, we identified the host and BmNPV proteins that could interact with lincRNA_XR209691.3. Next, by using truncation experiment and RNA immunoprecipitation (RIP) assay, it was found that lincRNA_XR209691.3 could bind to the Actin domain of BmHSP70. Subsequently, overexpression of lncRNA_XR209691.3 in BmN cells promoted the expression of BmHSP70, while knockdown of BmHsp70 suppressed the replication of BmNPV. Based on the above results, it is speculated that lincRNA_XR209691.3 could promote the proliferation of BmNPV through interaction with BmHSP70, possibly by improving the stability of BmHSP70 and thereby enhancing the expression of BmHSP70. Our results shed light on the lncRNA function in insect-pathogen interactions and provide a new clue to elucidate the molecular mechanism of BmNPV infection. (© 2022 Royal Entomological Society.) |
| References: | Anderson, D.M., Anderson, K.M., Chang, C.L., Makarewich, C.A., Nelson, B.R., McAnally, J.R. et al. (2015) A micropeptide encoded by a putative long noncoding RNA regulates muscle performance. Cell, 160, 595-606. Aviner, R. & Frydman, J. (2020) Proteostasis in viral infection: unfolding the complex virus-chaperone interplay. Cold Spring Harbor Perspectives in Biology, 12, a034090. Beckmann, R.P., Mizzen, L.E. & Welch, W.J. (1990) Interaction of Hsp 70 with newly synthesized proteins: implications for protein folding and assembly. Science, 248, 850-854. Bhat, S.A., Ahmad, S.M., Mumtaz, P.T., Malik, A.A., Dar, M.A., Urwat, U. et al. (2016) Long non-coding RNAs: mechanism of action and functional utility. Noncoding RNA Research, 1, 43-50. Bridges, M.C., Daulagala, A.C. & Kourtidis, A. (2021) LNCcation: lncRNA localization and function. The Journal of Cell Biology, 220, e202009045. Carrieri, C., Cimatti, L., Biagioli, M., Beugnet, A., Zucchelli, S., Fedele, S. et al. (2012) Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature, 491, 454-457. Chai, W., Li, J., Shangguan, Q., Liu, Q., Li, X., Qi, D. et al. (2018) Lnc-ISG20 inhibits influenza a virus replication by enhancing ISG20 expression. Journal of Virology, 92, e00539-e00518. Chen, D., Chen, H., Du, Y., Zhou, D., Geng, S., Wang, H. et al. (2019) Genome-wide identification of Long non-coding RNAs and their regulatory networks involved in Apis mellifera ligustica response to Nosema ceranae infection. Insects, 10, 245. Chen, N., Chen, G., Kong, X. & Wu, X. (2022) Actin contributes to the hyperexpression of Baculovirus Polyhedrin (polh) and p10 as a component of transcription initiation complex (TIC). Viruses, 14, 153. Cudmore, S., Reckmann, I. & Way, M. (1997) Viral manipulations of the Actin cytoskeleton. Trends in Microbiology, 5, 142-148. Derrien, T., Johnson, R., Bussotti, G., Tanzer, A., Djebali, S., Tilgner, H. et al. (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Research, 22, 1775-1789. Elton, D., Simpson-Holley, M., Archer, K., Medcalf, L., Hallam, R., McCauley, J. et al. (2001) Interaction of the influenza virus nucleoprotein with the cellular CRM1-mediated nuclear export pathway. Journal of Virology, 75, 408-419. Engreitz, J.M., Haines, J.E., Perez, E.M., Munson, G., Chen, J., Kane, M. et al. (2016) Local regulation of gene expression by lncRNA promoters, transcription and splicing. Nature, 539, 452-455. Etebari, K., Asad, S., Zhang, G. & Asgari, S. (2016) Identification of Aedes aegypti Long intergenic non-coding RNAs and their association with Wolbachia and dengue virus infection. PLoS Neglected Tropical Diseases, 10, e0005069. Etebari, K., Furlong, M.J. & Asgari, S. (2015) Genome wide discovery of long intergenic non-coding RNAs in diamondback moth (Plutella xylostella) and their expression in insecticide resistant strains. Scientific Reports, 5, 14642. Gao, J., Xiao, S., Liu, X., Wang, L., Ji, Q., Mo, D. et al. (2014) Inhibition of HSP70 reduces porcine reproductive and respiratory syndrome virus replication in vitro. BMC Microbiology, 14, 64. Hou, Z., Xu, X., Fu, X., Tao, S., Zhou, J., Liu, S. et al. (2017) HBx-related long non-coding RNA MALAT1 promotes cell metastasis via up-regulating LTBP3 in hepatocellular carcinoma. American Journal of Cancer Research, 7, 845-856. Huang, J.Z., Chen, M., Chen, D., Gao, X.C., Zhu, S., Huang, H. et al. (2017) A peptide encoded by a putative lncRNA HOXB-AS3 suppresses colon cancer growth. Molecular Cell, 68, 171-184.e6. Iwanaga, M., Shibano, Y., Ohsawa, T., Fujita, T., Katsuma, S. & Kawasaki, H. (2014) Involvement of HSC70-4 and other inducible HSPs in Bombyx mori nucleopolyhedrovirus infection. Virus Research, 179, 113-118. Jayakodi, M., Jung, J.W., Park, D., Ahn, Y.J., Lee, S.C., Shin, S.Y. et al. (2015) Genome-wide characterization of long intergenic non-coding RNAs (lincRNAs) provides new insight into viral diseases in honey bees Apis cerana and Apis mellifera. BMC Genomics, 16, 680. Kim, Y.K., Furic, L., Desgroseillers, L. & Maquat, L.E. (2005) Mammalian Staufen1 recruits Upf1 to specific mRNA 3'UTRs so as to elicit mRNA decay. Cell, 120, 195-208. Kondo, T., Hashimoto, Y., Kato, K., Inagaki, S., Hayashi, S. & Kageyama, Y. (2007) Small peptide regulators of Actin-based cell morphogenesis encoded by a polycistronic mRNA. Nature Cell Biology, 9, 660-665. Lahaye, X., Vidy, A., Fouquet, B. & Blondel, D. (2012) Hsp70 protein positively regulates rabies virus infection. Journal of Virology, 86, 4743-4751. Lee, S., Kopp, F., Chang, T.C., Sataluri, A., Chen, B., Sivakumar, S. et al. (2016) Noncoding RNA NORAD regulates genomic stability by sequestering PUMILIO proteins. Cell, 164, 69-80. Lim, S.O., Park, S.G., Yoo, J.H., Park, Y.M., Kim, H.J., Jang, K.T. et al. (2005) Expression of heat shock proteins (HSP27, HSP60, HSP70, HSP90, GRP78, GRP94) in hepatitis B virus-related hepatocellular carcinomas and dysplastic nodules. World Journal of Gastroenterology, 11, 2072-2079. Lin, A., Li, C., Xing, Z., Hu, Q., Liang, K., Han, L. et al. (2016) The LINK-A lncRNA activates normoxic HIF1α signalling in triple-negative breast cancer. Nature Cell Biology, 18, 213-224. Lin, S., Zhang, S.L., Yin, H.T., Zhao, Z.M., Chen, Z.K., Shen, M.M. et al. (2022) Cellular Lnc_209997 suppresses Bombyx mori nucleopolyhedrovirus replication by targeting miR-275-5p in B. mori. Insect Molecular Biology, 31, 308-316. Ma, L., Bajic, V.B. & Zhang, Z. (2013) On the classification of long non-coding RNAs. RNA Biology, 10, 925-933. Magny, E.G., Pueyo, J.I., Pearl, F.M., Cespedes, M.A., Niven, J.E., Bishop, S.A. et al. (2013) Conserved regulation of cardiac calcium uptake by peptides encoded in small open reading frames. Science, 341, 1116-1120. Mayer, M.P. (2005) Recruitment of Hsp70 chaperones: a crucial part of viral survival strategies. Reviews of Physiology, Biochemistry and Pharmacology, 153, 1-46. Moure, U.A.E., Tan, T., Sha, L., Lu, X., Shao, Z., Yang, G. et al. (2022) Advances in the immune regulatory role of non-coding RNAs (miRNAs and lncRNAs) in insect-pathogen interactions. Frontiers in Immunology, 13, 856457. Nam, J.W., Choi, S.W. & You, B.H. (2016) Incredible RNA: dual functions of coding and noncoding. Molecules and Cells, 39, 367-374. Okamoto, T., Nishimura, Y., Ichimura, T., Suzuki, K., Miyamura, T., Suzuki, T. et al. (2006) Hepatitis C virus RNA replication is regulated by FKBP8 and Hsp90. The EMBO Journal, 25, 5015-5025. Ouyang, J., Zhu, X., Chen, Y., Wei, H., Chen, Q., Chi, X. et al. (2014) NRAV, a long noncoding RNA, modulates antiviral responses through suppression of interferon-stimulated gene transcription. Cell Host & Microbe, 16, 616-626. Prasanth, K.V. & Spector, D.L. (2007) Eukaryotic regulatory RNAs: an answer to the 'genome complexity' conundrum. Genes & Development, 21, 11-42. Ray, M., Acharya, S., Shambhavi, S. & Lakhotia, S.C. (2019) Over-expression of Hsp83 in grossly depleted hsrω lncRNA background causes synthetic lethality and l(2)gl phenocopy in drosophila. Journal of Biosciences, 44, 36. Satyavathi, V., Ghosh, R. & Subramanian, S. (2017) Long non-coding RNAs regulating immunity in insects. Noncoding RNA, 3, 14. Shang, Q., Wu, P., Huang, H.L., Zhang, S.L., Tang, X.D. & Guo, X.J. (2020) Inhibition of heat shock protein 90 suppresses Bombyx mori nucleopolyhedrovirus replication in B. mori. Insect Molecular Biology, 29, 205-213. Valanne, S., Salminen, T.S., Järvelä-Stölting, M., Vesala, L. & Rämet, M. (2019) Immune-inducible non-coding RNA molecule lincRNA-IBIN connects immunity and metabolism in Drosophila melanogaster. PLoS Pathogens, 15, e1007504. Volkman, L.E. (2007) Baculovirus infectivity and the Actin cytoskeleton. Current Drug Targets, 8, 1075-1083. Wang, K.C. & Chang, H.Y. (2011) Molecular mechanisms of long noncoding RNAs. Molecular Cell, 43, 904-914. Wu, P., Shang, Q., Dweteh, O.A., Huang, H., Zhang, S., Zhong, J. et al. (2019) Over expression of bmo-miR-2819 suppresses BmNPV replication by regulating the BmNPV ie-1 gene in Bombyx mori. Molecular Immunology, 109, 134-139. Wu, Y., Cheng, T., Liu, C., Liu, D., Zhang, Q., Long, R. et al. (2016) Systematic identification and characterization of Long non-coding RNAs in the silkworm, Bombyx mori. PLoS One, 11, e0147147. Xiong, Y., Jia, M., Yuan, J., Zhang, C., Zhu, Y., Kuang, X. et al. (2015) STAT3-regulated long non-coding RNAs lnc-7SK and lnc-IGF2-AS promote hepatitis C virus replication. Molecular Medicine Reports, 12, 6738-6744. Yang, F., Deng, X., Ma, W., Berletch, J.B., Rabaia, N., Wei, G. et al. (2015) The lncRNA firre anchors the inactive X chromosome to the nucleolus by binding CTCF and maintains H3K27me3 methylation. Genome Biology, 16, 52. Yin, H., Zhang, S., Shen, M., Zhang, Z., Huang, H., Zhao, Z. et al. (2021) Integrative analysis of circRNA/miRNA/mRNA regulatory network reveals the potential immune function of circRNAs in the Bombyx mori fat body. Journal of Invertebrate Pathology, 179, 107537. Young, R.S., Marques, A.C., Tibbit, C., Haerty, W., Bassett, A.R., Liu, J.L. et al. (2012) Identification and properties of 1,119 candidate lincRNA loci in the Drosophila melanogaster genome. Genome Biology and Evolution, 4, 427-442. Zhang, J.H., Dong, Y., Wu, W., Yi, D.S., Wang, M., Wang, H.T. et al. (2020) Comprehensive identification and characterization of Long non-coding RNAs associated with Rice black-streaked dwarf virus infection in Laodelphax striatellus (Fallén) midgut. Frontiers in Physiology, 11, 1011. Zhang, L., Xu, W., Gao, X., Li, W., Qi, S., Guo, D. et al. (2020) lncRNA sensing of a viral suppressor of RNAi activates non-canonical innate immune signaling in drosophila. Cell Host & Microbe, 27, 115-128.e8. Zhang, S., Yin, H., Shen, M., Huang, H., Hou, Q., Zhang, Z. et al. (2020) Analysis of lncRNA-mediated gene regulatory network of Bombyx mori in response to BmNPV infection. Journal of Invertebrate Pathology, 170, 107323. Zhang, S.Z., Zhu, L.B., Yu, D., You, L.L., Wang, J., Cao, H.H. et al. (2020) Identification and functional analysis of BmNPV-interacting proteins from Bombyx mori (lepidoptera) larval midgut based on subcellular protein levels. Frontiers in Microbiology, 11, 1481. Zhang, Z., Zhao, Z., Lin, S., Wu, W., Tang, W., Dong, Y. et al. (2021) Identification of long noncoding RNAs in silkworm larvae infected with Bombyx mori cypovirus. Archives of Insect Biochemistry and Physiology, 106, 1-12. Zhou, H., Ni, J., Wu, S., Ma, F., Jin, P. & Li, S. (2021) lncRNA-CR46018 positively regulates the drosophila toll immune response by interacting with Dif/dorsal. Developmental and Comparative Immunology, 124, 104183. Zhou, J., Yang, L., Zhong, T., Mueller, M., Men, Y., Zhang, N. et al. (2015) H19 lncRNA alters DNA methylation genome wide by regulating S-adenosylhomocysteine hydrolase. Nature Communications, 6, 10221. |
| Contributed Indexing: | Keywords: BmNPV; HSP70; RNA-protein interaction; host-pathogen interaction; lncRNA |
| Substance Nomenclature: | 0 (RNA, Long Noncoding) 0 (Insect Proteins) 0 (Actins) |
| SCR Organism: | Bombyx mori nucleopolyhedrovirus |
| Entry Date(s): | Date Created: 20221209 Date Completed: 20230314 Latest Revision: 20230316 |
| Update Code: | 20260130 |
| DOI: | 10.1111/imb.12821 |
| PMID: | 36482511 |
| Database: | MEDLINE |
Be the first to leave a comment!