Immunological function of Bombyx Toll9-2 in the silkworm (Bombyx mori) larval midgut: Activation by Escherichia coli/lipopolysaccharide and regulation of growth.


Journal

Archives of insect biochemistry and physiology
ISSN: 1520-6327
Titre abrégé: Arch Insect Biochem Physiol
Pays: United States
ID NLM: 8501752

Informations de publication

Date de publication:
Aug 2024
Historique:
revised: 18 06 2024
received: 28 03 2024
accepted: 29 06 2024
medline: 9 8 2024
pubmed: 9 8 2024
entrez: 9 8 2024
Statut: ppublish

Résumé

Toll receptors are important regulators of insects' innate immune system which, upon binding of pathogen molecules, activate a conserved signal transduction cascade known as the Toll pathway. RNA interference (RNAi) is a powerful tool to study the function of genes via reverse genetics. However, due to the reported refractory of RNAi efficiency in lepidopteran insects, successful reports of silencing of Toll receptors in the silkworm Bombyx mori have not been reported yet. In this study, a Toll receptor of the silkworm Bombyx Toll9-2 (BmToll9-2) was cloned and its expression and function were analyzed. The results showed that BmToll9-2 contains an ectodomain (ECD) with a signal peptide and nine leucine-rich repeats, a transmembrane helix, and a cytoplasmic region with a Toll/interleukin-1 domain. Phylogenetic analysis indicates that BmToll9-2 clusters with other insect Toll9 receptors and mammalian Toll-like receptor 4. Oral infection of exogenous pathogens showed that the Gram-negative bacterium Escherichia coli and its main cell wall component lipopolysaccharide (LPS), as well as the Gram-positive bacterium Staphylococcus aureus and its main cell wall component peptidoglycan, significantly induce BmToll9-2 expression in vivo. LPS also induced the expression of BmToll9-2 in BmN4 cells in vitro. These observations indicate its role as a sensor in the innate immunity to exogenous pathogens and as a pathogen-associated receptor that is responsive to LPS. RNAi of BmToll9-2 was effective in the midgut and epidermis. RNAi-mediated knock-down of BmToll9-2 reduced the weight and growth of the silkworm. Bacterial challenge following RNAi upregulated the expression of BmToll9-2 and rescued the weight differences of the silkworm, which may be related to its participation in the immune response and the regulation of the microbiota in the midgut lumen of the silkworm larvae.

Identifiants

pubmed: 39118437
doi: 10.1002/arch.22130
doi:

Substances chimiques

Insect Proteins 0
Lipopolysaccharides 0
Toll-Like Receptors 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e22130

Subventions

Organisme : Science and Technology Program of Guangzhou
ID : 202102010465
Organisme : National Natural Science Foundation of China
ID : 31501898
Organisme : Featured Innovation Project of Universities in Guangdong Province
ID : 2019KTSCX133
Organisme : Natural Science Foundation of Guangdong Province
ID : 2017A030313152
Organisme : Pearl River S&T Nova Program of Guangzhou
ID : 201710010094

Informations de copyright

© 2024 Wiley Periodicals LLC.

Références

Anderson, K.V., Jürgens, G. & Nüsslein‐Volhard, C. (1985) Establishment of dorsal‐ventral polarity in the Drosophila embryo: Genetic studies on the role of the Toll gene product. Cell, 42, 779–789.
Bettencourt, R., Tanji, T., Yagi, Y. & Ip, Y.T. (2004) Toll and Toll‐9 in Drosophila innate immune response. Journal of Endotoxin Research, 10, 261–268.
Bilak, H., Tauszig‐Delamasure, S. & Imler, J.L. (2003) Toll and Toll‐like receptors in Drosophila. Biochemical Society Transactions, 31, 648–651.
Cao, X., He, Y., Hu, Y., Wang, Y., Chen, Y.R., Bryant, B. et al. (2015) The immune signaling pathways of Manduca sexta. Insect Biochemistry and Molecular Biology, 62, 64–74.
Cheng, T.C., Zhang, Y.L., Liu, C., Xu, P.Z., Gao, Z., Xia, Q.Y. et al. (2008) Identification and analysis of Toll‐related genes in the domesticated silkworm, Bombyx mori. Developmental & Comparative Immunology, 32, 464–475.
Chowdhury, M., Li, C.F., He, Z., Lu, Y., Liu, X.S., Wang, Y.F. et al. (2019) Toll family members bind multiple Spätzle proteins and activate antimicrobial peptide gene expression in Drosophila. Journal of Biological Chemistry, 294, 10172–10181.
Christophides, G.K., Zdobnov, E., Barillas‐Mury, C., Birney, E., Blandin, S., Blass, C. et al. (2002) Immunity‐related genes and gene families in Anopheles gambiae. Science, 298, 159–165.
Evans, J.D., Aronstein, K., Chen, Y.P., Hetru, C., Imler, J.L., Jiang, H. et al. (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Molecular Biology, 15, 645–656.
Gay, N.J. & Keith, F.J. (1991) Drosophila Toll and IL‐1 receptor. Nature, 351, 355–356.
Guo, B., Tang, J., Ding, G., Mashilingi, S.K., Huang, J. & An, J. (2023) Gut microbiota is a potential factor in shaping phenotypic variation in larvae and adults of female bumble bees. Frontiers in Microbiology, 14, 1117077.
Lemaitre, B. & Hoffmann, J. (2007) The host defense of Drosophila melanogaster. Annual Review of Immunology, 25, 697–743.
Liang, Y., Wang, T., Yang, W., Chen, Z., Li, Q., Swevers, L. et al. (2023) Silencing of the immune gene BmPGRP‐L4 in the midgut affects the growth of silkworm (Bombyx mori) larvae. Insect Molecular Biology, 32, 340–351.
Lima, L.F., Torres, A.Q., Jardim, R., Mesquita, R.D. & Schama, R. (2021) Evolution of Toll, Spatzle and MyD88 in insects: The problem of the Diptera bias. BMC Genomics, 22, 562.
Liu, J., Kolliopoulou, A., Smagghe, G. & Swevers, L. (2014) Modulation of the transcriptional response of innate immune and RNAi genes upon exposure to dsRNA and LPS in silkmoth‐derived Bm5 cells overexpressing BmToll9‐1 receptor. Journal of Insect Physiology, 66, 10–19.
Liu, J., Smagghe, G. & Swevers, L. (2013) Transcriptional response of BmToll9‐1 and RNAi machinery genes to exogenous dsRNA in the midgut of Bombyx mori. Journal of Insect Physiology, 59, 646–654.
Livak, K. J. & Schmittgen, T. D. (2001) Analysis of relative gene expression data using real‐time quantitative PCR and the 2–ΔΔCT method. Methods, 25(4), 402–408. https://doi.org/10.1006/meth.2001.1262
Luna, C., Wang, X., Huang, Y., Zhang, J. & Zheng, L. (2002) Characterization of four Toll related genes during development and immune responses in Anopheles gambiae. Insect Biochemistry and Molecular Biology, 32, 1171–1179.
Narbonne‐Reveau, K., Charroux, B. & Royet, J. (2011) Lack of an antibacterial response defect in Drosophila Toll‐9 mutant. PLoS One, 6, e17470.
Ooi, J.Y., Yagi, Y., Hu, X. & Ip, Y.T. (2002) The Drosophila Toll‐9 activates a constitutive antimicrobial defense. EMBO Reports, 3, 82–87.
Qiao, H., Keesey, I.W., Hansson, B.S. & Knaden, M. (2019) Gut microbiota affects development and olfactory behavior in Drosophila melanogaster. Journal of Experimental Biology, 222. https://doi.org/10.1242/jeb.192500
Sakakibara, Y., Yamashiro, R., Chikamatsu, S., Hirota, Y., Tsubokawa, Y., Nishijima, R. et al. (2023) Drosophila Toll‐9 is induced by aging and neurodegeneration to modulate stress signaling and its deficiency exacerbates tau‐mediated neurodegeneration. iScience, 26, 105968.
Sheldon, B.C. & Verhulst, S. (1996) Ecological immunology: Costly parasite defences and trade‐offs in evolutionary ecology. Trends in Ecology & Evolution, 11, 317–321.
Shmueli, A., Shalit, T., Okun, E. & Shohat‐Ophir, G. (2018) The Toll pathway in the central nervous system of flies and mammals. NeuroMolecular Medicine, 20, 419–436.
Siomi, H. & Siomi, M.C. (2009) On the road to reading the RNA‐interference code. Nature, 457, 396–404.
Stanley, D., Haas, E. & Kim, Y. (2023) Beyond cellular immunity: On the biological significance of insect hemocytes. Cells, 12, 599.
Takeda, K. & Akira, S. (2004) TLR signaling pathways. Seminars in Immunology, 16, 3–9.
Tanaka, H., Ishibashi, J., Fujita, K., Nakajima, Y., Sagisaka, A., Tomimoto, K. et al. (2008) A genome‐wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochemistry and Molecular Biology, 38, 1087–1110.
Terenius, O., Papanicolaou, A., Garbutt, J.S., Eleftherianos, I., Huvenne, H., Kanginakudru, S. et al. (2011) RNA interference in Lepidoptera: An overview of successful and unsuccessful studies and implications for experimental design. Journal of Insect Physiology, 57, 231–245.
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., & Speleman, F. (2002). Accurate normalization of real‐time quantitative RT‐PCR data by geometric averaging of multiple internal control genes. Genome Biology, 3(7). https://doi.org/10.1186/gb-2002-3-7-research0034
Wang, G.H., Xia, Q.Y., Cheng, D.J., Duan, J., Zhao, P., Chen, J. et al. (2008) Reference genes identified in the silkworm Bombyx mori during metamorphism based on oligonucleotide microarray and confirmed by qRT‐PCR. Insect Science, 15, 405–413.
Wang, X., Zhang, Y., Zhang, R. & Zhang, J. (2019) The diversity of pattern recognition receptors (PRRs) involved with insect defense against pathogens. Current Opinion in Insect Science, 33, 105–110.
Weiss, H.J. & O'Neill, L.A.J. (2022) Of flies and Men‐The Discovery of TLRs. Cells, 11, 3127.
Wu, S., Zhang, X., Chen, X., Cao, P., Beerntsen, B.T. & Ling, E. (2010) BmToll9, an Arthropod conservative Toll, is likely involved in the local gut immune response in the silkworm, Bombyx mori. Developmental & Comparative Immunology, 34, 93–96.
Xia, Q., Zhou, Z., Lu, C., Cheng, D., Dai, F., Li, B. et al. (2004) A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science, 306, 1937–1940.
Yu, B., Sang, Q., Pan, G., Li, C. & Zhou, Z. (2020) A Toll‐Spätzle pathway in the immune response of Bombyx mori. Insects, 11, 586.
Zhang, C., Yan, S.Q., Shen, B.B., Ali, S., Wang, X.M., Jin, F.L. et al. (2017) RNAi knock‐down of the Bemisia tabaci Toll gene (BtToll) increases mortality after challenge with destruxin A. Molecular Immunology, 88, 164–173.
Zhang, R.N., Li, X.F., Zhang, J., Li, Y.J., Wang, Y., Song, Y.H. et al. (2021) Toll9 from Bombyx mori functions as a pattern recognition receptor that shares features with Toll‐like receptor 4 from mammals. Proceedings of the National Academy of Sciences of the United States of America, 118. https://doi.org/10.1073/pnas.2103021118
Zou, Z., Evans, J.D., Lu, Z., Zhao, P., Williams, M., Sumathipala, N. et al. (2007) Comparative genomic analysis of the Tribolium immune system. Genome Biology, 8, R177.

Auteurs

Jisheng Liu (J)

School of Life Sciences, Guangzhou University, Guangzhou, China.

Weifeng Yang (W)

School of Life Sciences, Guangzhou University, Guangzhou, China.

Wenli Liao (W)

School of Life Sciences, Guangzhou University, Guangzhou, China.

Yanling Huang (Y)

School of Life Sciences, Guangzhou University, Guangzhou, China.

Weijian Chen (W)

School of Life Sciences, Guangzhou University, Guangzhou, China.

Xiaoling Bu (X)

School of Life Sciences, Guangzhou University, Guangzhou, China.

Shiyi Huang (S)

School of Life Sciences, Guangzhou University, Guangzhou, China.

Wanyi Jiang (W)

School of Life Sciences, Guangzhou University, Guangzhou, China.

Luc Swevers (L)

Institute of Biosciences and Applications, National Centre for Scientific Research Demokritos, Athens, Greece.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Classifications MeSH