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Translocator protein (TSPO) inhibits Nosema bombycis proliferation in silkworm, Bombyx mori

Published online by Cambridge University Press:  11 September 2024

Mengjin Liu ,
Lang Wen ,
Ben Deng ,
Yaping Su ,
Zhenghao Han ,
Yiling Zhang ,
Feng Zhu ,
Qingsheng Qu ,
Mingze Li  and
Yujia Fang
...Show all authors
Mengjin Liu
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China Jiangyin Senior High School of Jiangsu Province, Jiangyin 214400, China
Lang Wen
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China
Ben Deng
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China
Yaping Su
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China
Zhenghao Han
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China
Yiling Zhang
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang 212100, China
Feng Zhu
Affiliation:
Zaozhuang University, Zaozhuang 277160, Shandong Province, China
Qingsheng Qu
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China
Mingze Li
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China
Yujia Fang
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China
Ping Qian
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang 212100, China
Xudong Tang*
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang 212100, China
*
Corresponding author: Xudong Tang; Email: [email protected]
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Abstract

Pebrine disease, caused by Nosema bombycis (Nb) infection in silkworms, is a severe and long-standing disease that threatens sericulture. As parasitic pathogens, a complex relationship exists between microsporidia and their hosts at the mitochondrial level. Previous studies have found that the translocator protein (TSPO) is involved in various biological functions, such as membrane potential regulation, mitochondrial autophagy, immune responses, calcium ion channel regulation, and cell apoptosis. In the present study, we found that TSPO expression in silkworms (BmTSPO) was upregulated following Nb infection, leading to an increase in cytoplasmic calcium, adenosine triphosphate, and reactive oxygen species levels. Knockdown and overexpression of BmTSPO resulted in the promotion and inhibition of Nb proliferation, respectively. We also demonstrated that the overexpression of BmTSPO promotes host cell apoptosis and significantly increases the expression of genes involved in the immune deficiency and Janus kinase-signal transducer and the activator of the transcription pathways. These findings suggest that BmTSPO activates the innate immune signalling pathway in silkworms to regulate Nb proliferation. Targeting TSPO represents a promising approach for the development of new treatments for microsporidian infections.

Keywords

Bombyx moriIMD pathwayJAK-STAT pathwayNosema bombycisTSPO
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 114 , Issue 4 , August 2024 , pp. 551 - 562
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Copyright © The Author(s), 2024. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this work and share first authorship.

References

Bessette, E and Williams, B (2022) Protists in the insect rearing industry: benign passengers or potential risk? Insects 13, 482. https://doi.org/10.3390/insects13050482CrossRefGoogle ScholarPubMed
Betlazar, C, Middleton, RJ, Banati, R and Liu, GJ (2020) The translocator protein (TSPO) in mitochondrial bioenergetics and immune processes. Cells 9, 512. https://doi.org/10.3390/cells9020512CrossRefGoogle ScholarPubMed
Boutros, M, Agaisse, H and Perrimon, N (2002) Sequential activation of signaling pathways during innate immune responses in Drosophila. Developmental Cell 3, 711–722. https://doi.org/10.1016/s1534-5807(02)00325-8CrossRefGoogle ScholarPubMed
Bouyer, G, Cueff, A, Egée, S, Kmiecik, J, Maksimova, Y, Glogowska, E, Gallagher, PG and Thomas, SL (2011) Erythrocyte peripheral type benzodiazepine receptor/voltage-dependent anion channels are upregulated by Plasmodium falciparum. Blood 118, 2305–2312. https://doi.org/10.1182/blood-2011-01-329300CrossRefGoogle ScholarPubMed
Caballero, B, Veenman, L and Gavish, M (2013) Role of mitochondrial translocator protein (18 kDa) on mitochondrial-related cell death processes. Recent Patents. on Endocrine, Metabolic & Immune Drug Discovery 7, 86–101. https://doi.org/10.2174/1872214811307020002CrossRefGoogle ScholarPubMed
Chen, C, Eldein, S, Zhou, X, Sun, Y, Gao, J, Sun, Y, Liu, C and Wang, L (2018) Immune function of a Rab-related protein by modulating the JAK-STAT signaling pathway in the silkworm, Bombyx mori. Archives of Insect Biochemistry and Physiology 97, 21434. https://doi.org/10.1002/arch.21434CrossRefGoogle ScholarPubMed
Cho, JH, Park, JH, Chung, CG, Shim, HJ, Jeon, KH, Yu, SW and Lee, SB (2015) Parkin-mediated responses against infection and wound involve TSPO-VDAC complex in Drosophila. Biochemical and Biophysical Research Communications 463, 1–6. https://doi.org/10.1016/j.bbrc.2015.05.006CrossRefGoogle ScholarPubMed
del Aguila, C, Izquierdo, F, Granja, AG, Hurtado, C, Fenoy, S, Fresno, M and Revilla, Y (2006) Encephalitozoon microsporidia modulates p53-mediated apoptosis in infected cells. International Journal for Parasitology 36, 869–876. https://doi.org/10.1016/j.ijpara.2006.04.002CrossRefGoogle ScholarPubMed
Didier, ES, Sokolova, YY, Alvarez, X and Bowers, LC (2009) Encephalitozoon cuniculi (Microsporidia) suppresses apoptosis in human macrophages (133.12). The Journal of Immunology 182(suppl. 1), 133.112. https://doi.org/10.4049/jimmunol.182.Supp.133.12CrossRefGoogle Scholar
Dolgikh, VV, Semenov, PS and Grigor'ev, MV (2002) [Peculiarities of metabolism of the microsporidia Nosema grylli during the intracellular development]. Parazitologiia 36, 493–501.Google ScholarPubMed
Dostert, C, Jouanguy, E, Irving, P, Troxler, L, Galiana-Arnoux, D, Hetru, C, Hoffmann, JA and Imler, JL (2005) The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of drosophila. Nature Immunology 6, 946–953. https://doi.org/10.1038/ni1237CrossRefGoogle Scholar
El Chemali, L, Akwa, Y and Massaad-Massade, L (2022) The mitochondrial translocator protein (TSPO): a key multifunctional molecule in the nervous system. Biochemical Journal 479, 1455–1466. https://doi.org/10.1042/BCJ20220050CrossRefGoogle ScholarPubMed
Everett, H, Barry, M, Sun, X, Lee, SF, Frantz, C, Berthiaume, LG, McFadden, G and Bleackley, RC (2002) The myxoma poxvirus protein, M11L, prevents apoptosis by direct interaction with the mitochondrial permeability transition pore. Journal of Experimental Medicine 196, 1127–1139. https://doi.org/10.1084/jem.20011247CrossRefGoogle ScholarPubMed
Franzen, C, Nassonova, ES, Schölmerich, J and Issi, IV (2006) Transfer of the members of the genus Brachiola (microsporidia) to the genus Anncaliia based on ultrastructural and molecular data. Journal of Eukaryotic Microbiology 53, 26–35. https://doi.org/10.1111/j.1550-7408.2005.00066.xCrossRefGoogle Scholar
Freeman, MA, Bell, AS and Sommerville, C (2003) A hyperparasitic microsporidian infecting the salmon louse, Lepeophtheirus salmonis: an rDNA-based molecular phylogenetic study. Journal of Fish Diseases 26, 667–676. https://doi.org/10.1046/j.1365-2761.2003.00498.xCrossRefGoogle ScholarPubMed
Gatliff, J, East, DA, Singh, A, Alvarez, MS, Frison, M, Matic, I, Ferraina, C, Sampson, N, Turkheimer, F and Campanella, M (2017) A role for TSPO in mitochondrial Ca(2+) homeostasis and redox stress signaling. Cell Death & Disease 8, e2896. https://doi.org/10.1038/cddis.2017.186CrossRefGoogle ScholarPubMed
Guedes, CES, Dias, BRS, Petersen, A, Cruz, KP, Almeida, NJ, Andrade, DR, Menezes, JPB, Borges, VM and Veras, PST (2018) In vitro evaluation of the anti-leishmanial activity and toxicity of PK11195. Memorias do Instituto Oswaldo Cruz 113, e170345. https://doi.org/10.1590/0074-02760170345CrossRefGoogle ScholarPubMed
Hacker, C, Howell, M, Bhella, D and Lucocq, J (2014) Strategies for maximizing ATP supply in the microsporidian Encephalitozoon cuniculi: direct binding of mitochondria to the parasitophorous vacuole and clustering of the mitochondrial porin VDAC. Cellular Microbiology 16, 565–579. https://doi.org/10.1111/cmi.12240CrossRefGoogle Scholar
Hacker, C, Sendra, K, Keisham, P, Filipescu, T, Lucocq, J, Salimi, F, Ferguson, S, Bhella, D, MacNeill, SA, Embley, M and Lucocq, J (2024) Biogenesis, inheritance, and 3D ultrastructure of the microsporidian mitosome. Life Science Alliance 7, e202201635. https://doi.org/10.26508/lsa.202201635CrossRefGoogle ScholarPubMed
Halliwell, B (2011) Free radicals and antioxidants – quo vadis? Trends in Pharmacological Sciences 32, 125–130. https://doi.org/10.1016/j.tips.2010.12.002CrossRefGoogle ScholarPubMed
Han, B and Weiss, LM (2017) Microsporidia: obligate intracellular pathogens within the fungal kingdom. Microbiology Spectrum 5, 10. https://doi.org/10.1128/microbiolspec.FUNK-0018-2016CrossRefGoogle ScholarPubMed
Han, B, Ma, Y, Tu, V, Tomita, T, Mayoral, J, Williams, T, Horta, A, Huang, H and Weiss, LM (2019) Microsporidia interact with host cell mitochondria via voltage-dependent anion channels using sporoplasm surface protein 1. mBio 10, e01944-19. https://doi.org/10.1128/mBio.01944-19CrossRefGoogle ScholarPubMed
He, X, Fu, Z, Li, M, Liu, H, Cai, S, Man, N and Lu, X (2015) Nosema bombycis (Microsporidia) suppresses apoptosis in BmN cells (Bombyx mori). Acta Biochimica et Biophysica Sinica (Shanghai) 47, 696–702. https://doi.org/10.1093/abbs/gmv062CrossRefGoogle ScholarPubMed
Heussler, VT, Kuenzi, P and Rottenberg, S (2001) Inhibition of apoptosis by intracellular protozoan parasites. International Journal for Parasitology 31, 1166–1176. https://doi.org/10.1016/s0020-7519(01)00271-5CrossRefGoogle ScholarPubMed
Hiser, C, Montgomery, BL and Ferguson-Miller, S (2021) TSPO protein binding partners in bacteria, animals, and plants. Journal of Bioenergetics and Biomembranes 53, 463–487. https://doi.org/10.1007/s10863-021-09905-4CrossRefGoogle ScholarPubMed
Huang, L, Cheng, T, Xu, P, Cheng, D, Fang, T and Xia, Q (2009) A genome-wide survey for host response of silkworm, Bombyx mori during pathogen Bacillus bombyseptieus infection. PLoS ONE 4, e8098. https://doi.org/10.1371/journal.pone.0008098CrossRefGoogle ScholarPubMed
Kurze, C, Le Conte, Y, Dussaubat, C, Erler, S, Kryger, P, Lewkowski, O, Müller, T, Widder, M and Moritz, RF (2015) Nosema tolerant honeybees (Apis mellifera) escape parasitic manipulation of apoptosis. PLoS ONE 10, e0140174. https://doi.org/10.1371/journal.pone.0140174CrossRefGoogle ScholarPubMed
Kusumawidjaja, G, Kayed, H, Giese, N, Bauer, A, Erkan, M, Giese, T, Hoheise, JD, Friess, H and Kleeff, J (2007) Basic transcription factor 3 (BTF3) regulates transcription of tumor-associated genes in pancreatic cancer cells. Cancer Biology & Therapy 6, 367–376. https://doi.org/10.4161/cbt.6.3.3704CrossRefGoogle ScholarPubMed
Lin, R, Angelin, A, Da Settimo, F, Martini, C, Taliani, S, Zhu, S and Wallace, DC (2014) Genetic analysis of dTSPO, an outer mitochondrial membrane protein, reveals its functions in apoptosis, longevity, and Ab42-induced neurodegeneration. Aging Cell 13, 507–518. https://doi.org/10.1111/acel.12200CrossRefGoogle ScholarPubMed
Lin, R, Rittenhouse, D, Sweeney, K, Potluri, P and Wallace, DC (2015) TSPO, a mitochondrial outer membrane protein, controls ethanol-related behaviors in drosophila. PLoS Genetics 11, e1005366. https://doi.org/10.1371/journal.pgen.1005366CrossRefGoogle ScholarPubMed
Liu, W, Liu, J, Lu, Y, Gong, Y, Zhu, M, Chen, F, Liang, Z, Zhu, L, Kuang, S, Hu, X, Cao, G, Xue, R and Gong, C (2015) Immune signaling pathways activated in response to different pathogenic micro-organisms in Bombyx mori. Molecular Immunology 65, 391–397. https://doi.org/10.1016/j.molimm.2015.02.018CrossRefGoogle ScholarPubMed
Liu, X, Gu, H, Xu, Q, Jiang, Z, Li, B and Wei, J (2023) Determination of suitable reference genes for RT-qPCR normalisation in Bombyx mori (Lepidoptera: Bombycidae) infected by the parasitoid Exorista sorbillans (Diptera, Tachinidae). Bulletin of Entomological Research 113, 845–857. https://doi.org/10.1017/S0007485323000536CrossRefGoogle ScholarPubMed
Lyu, C, Chen, Y, Meng, Y, Yang, J, Ye, S, Niu, Z, Ei-Debs, I, Gupta, N and Shen, B (2023) The mitochondrial pyruvate carrier coupling glycolysis and the tricarboxylic acid cycle is required for the asexual reproduction of Toxoplasma gondii. Microbiology Spectrum 11, e0504322. https://doi.org/10.1128/spectrum.05043-22CrossRefGoogle ScholarPubMed
Ma, Z, Li, C, Pan, G, Li, Z, Han, B, Xu, J, Lan, X, Chen, J, Yang, D, Chen, Q, Sang, Q, Ji, X, Li, T, Long, M and Zhou, Z (2013) Genome-wide transcriptional response of silkworm (Bombyx mori) to infection by the microsporidian Nosema bombycis. PLoS ONE 8, e84137. https://doi.org/10.1371/journal.pone.0084137CrossRefGoogle ScholarPubMed
Marginedas-Freixa, I, Hattab, C, Bouyer, G, Halle, F, Chene, A, Lefevre, SD, Cambot, M, Cueff, A, Schmitt, M, Gamain, B, Lacapere, JJ, Egee, S, Bihel, F, Le Van Kim, C and Ostuni, MA (2016) TSPO ligands stimulate ZnPPIX transport and ROS accumulation leading to the inhibition of P. falciparum growth in human blood. Scientific Reports 6, 33516. https://doi.org/10.1038/srep33516CrossRefGoogle Scholar
Massoco, C and Palermo-Neto, J (2003) Effects of midazolam on equine innate immune response: a flow cytometric study. Veterinary Immunology and Immunopathology 95, 11–19. https://doi.org/10.1016/s0165-2427(03)00097-7CrossRefGoogle ScholarPubMed
McMenamin, AJ, Daughenbaugh, KF, Parekh, F, Pizzorno, MC and Flenniken, ML (2018) Honey bee and bumble bee antiviral defense. Viruses 10, 395. https://doi.org/10.3390/v10080395CrossRefGoogle ScholarPubMed
Morgulis, MS and Palermo-Neto, J (2002) Effects of in ovo and acute diazepam treatments on peripheral benzodiazepine receptors and cutaneous basophil hypersensitivity in chickens. Veterinary and Human Toxicology 44, 328–330.Google ScholarPubMed
Morrow, G and Tanguay, RM (2012) Small heat shock protein expression and functions during development. International Journal of Biochemistry & Cell Biology 44, 1613–1621. https://doi.org/10.1016/j.biocel.2012.03.009CrossRefGoogle ScholarPubMed
Mühling, J, Gonter, J, Nickolaus, KA, Matejec, R, Welters, ID, Wolff, M, Sablotzki, A, Engel, J, Krüll, M, Menges, T, Fuchs, M, Dehne, MG and Hempelmann, G (2005) Benzodiazepine receptor-dependent modulation of neutrophil (PMN) free amino- and alpha-keto acid profiles or immune functions. Amino Acids 28, 85–98. https://doi.org/10.1007/s00726-004-0136-yCrossRefGoogle ScholarPubMed
Orrenius, S, Gogvadze, V and Zhivotovsky, B (2015) Calcium and mitochondria in the regulation of cell death. Biochemical and Biophysical Research Communications 460, 72–81. https://doi.org/10.1016/j.bbrc.2015.01.137CrossRefGoogle ScholarPubMed
Pan, G, Bao, J, Ma, Z, Song, Y, Han, B, Ran, M, Li, C and Zhou, Z (2018) Invertebrate host responses to microsporidia infections. Developmental & Comparative Immunology 83, 104–113. https://doi.org/10.1016/j.dci.2018.02.004CrossRefGoogle ScholarPubMed
Pernas, L, Bean, C, Boothroyd, JC and Scorrano, L (2018) Mitochondria restrict growth of the intracellular parasite Toxoplasma gondii by limiting its uptake of fatty acids. Cell Metabolism 27, 886–897 e884. https://doi.org/10.1016/j.cmet.2018.02.018CrossRefGoogle ScholarPubMed
Redza-Dutordoir, M and Averill-Bates, DA (2016) Activation of apoptosis signalling pathways by reactive oxygen species. Biochimica et Biophysica Acta 1863, 2977–2992. https://doi.org/10.1016/j.bbamcr.2016.09.012CrossRefGoogle ScholarPubMed
Rupprecht, R, Rammes, G, Eser, D, Baghai, TC, Schüle, C, Nothdurfter, C, Troxler, T, Gentsch, C, Kalkman, HO, Chaperon, F, Uzunov, V, McAllister, KH, Bertaina-Anglade, V, La Rochelle, CD, Tuerck, D, Floesser, A, Kiese, B, Schumacher, M, Landgraf, R, Holsboer, F and Kucher, K (2009) Translocator protein (18 kD) as target for anxiolytics without benzodiazepine-like side effects. Science 325, 490–493. https://doi.org/10.1126/science.1175055CrossRefGoogle ScholarPubMed
Selvaraj, V, Stocco, DM and Tu, LN (2015) Minireview: translocator protein (TSPO) and steroidogenesis: a reappraisal. Molecular Endocrinology 29, 490–501. https://doi.org/10.1210/me.2015-1033CrossRefGoogle ScholarPubMed
Shah-Simpson, S, Lentini, G, Dumoulin, PC and Burleigh, BA (2017) Modulation of host central carbon metabolism and in situ glucose uptake by intracellular Trypanosoma cruzi amastigotes. PLoS Pathogens 13, e1006747. https://doi.org/10.1371/journal.ppat.1006747CrossRefGoogle ScholarPubMed
Smith, WA (1995) Regulation and consequences of cellular changes in the prothoracic glands of Manduca sexta during the last larval instar: a review. Archives of Insect Biochemistry and Physiology 30, 271–293. https://doi.org/10.1002/arch.940300214CrossRefGoogle ScholarPubMed
Snyder, MJ and Van Antwerpen, R (1998) Evidence for a diazepam-binding inhibitor (DBI) benzodiazepine receptor-like mechanism in ecdysteroidogenesis by the insect prothoracic gland. Cell and Tissue Research 294, 161–168. https://doi.org/10.1007/s004410051166CrossRefGoogle ScholarPubMed
Sonenshine, DE and Macaluso, KR (2017) Microbial invasion vs. tick immune regulation. Frontiers in Cellular and Infection Microbiology 7, 390. https://doi.org/10.3389/fcimb.2017.00390CrossRefGoogle ScholarPubMed
Souza-Neto, JA, Sim, S and Dimopoulos, G (2009) An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proceedings of the National Academy of Sciences of the USA 106, 17841–17846. https://doi.org/10.1073/pnas.0905006106CrossRefGoogle ScholarPubMed
Tang, X, Zhang, Y, Zhou, Y, Liu, R and Shen, Z (2020) Quantitative proteomic analysis of ovaries from Nosema bombycis-infected silkworm (Bombyx mori). Journal of Invertebrate Pathology 172, 107355. https://doi.org/10.1016/j.jip.2020.107355CrossRefGoogle ScholarPubMed
Tanimoto, Y, Onishi, Y, Sato, Y and Kizaki, H (1999) Benzodiazepine receptor agonists modulate thymocyte apoptosis through reduction of the mitochondrial transmembrane potential. Japanese Journal of Pharmacology 79, 177–183. https://doi.org/10.1254/jjp.79.177Google ScholarPubMed
Vávra, J and Lukeš, J (2013) Microsporidia and ‘the art of living together’. Advances in Parasitology 82, 253–319. https://doi.org/10.1016/b978-0-12-407706-5.00004-6CrossRefGoogle ScholarPubMed
Wang, C, Yu, L, Zhang, J, Zhou, Y, Sun, B, Xiao, Q, Zhang, M, Liu, H, Li, J, Li, J, Luo, Y, Xu, J, Lian, Z, Lin, J, Wang, X, Zhang, P, Guo, L, Ren, R and Deng, D (2023) Structural basis of the substrate recognition and inhibition mechanism of Plasmodium falciparum nucleoside transporter PfENT1. Nature Communications 14, 1727. https://doi.org/10.1038/s41467-023-37411-1CrossRefGoogle ScholarPubMed
Weiss, LM (2015) Microsporidia: Pathogens of Opportunity. Hoboken, NJ, USA: John Wiley & Sons Inc.Google Scholar
Winterbourn, CC (2015) Are free radicals involved in thiol-based redox signaling? Free Radical Biology & Medicine 80, 164–170. https://doi.org/10.1016/j.freeradbiomed.2014.08.017CrossRefGoogle ScholarPubMed
Wu, S, Zhang, X, He, Y, Shuai, J, Chen, X and Ling, E (2010) Expression of antimicrobial peptide genes in Bombyx mori gut modulated by oral bacterial infection and development. Developmental & Comparative Immunology 34, 1191–1198. https://doi.org/10.1016/j.dci.2010.06.013CrossRefGoogle ScholarPubMed
Xia, N, Ye, S, Liang, X, Chen, P, Zhou, Y, Fang, R, Zhao, J, Gupta, N, Yang, S, Yuan, J and Shen, B (2019) Pyruvate homeostasis as a determinant of parasite growth and metabolic plasticity in Toxoplasma gondii. mBio 10, e00898-19. https://doi.org/10.1128/mBio.00898-19CrossRefGoogle ScholarPubMed
Yasin, N, Veenman, L, Singh, S, Azrad, M, Bode, J, Vainshtein, A, Caballero, B, Marek, I and Gavish, M (2017) Classical and novel TSPO ligands for the mitochondrial TSPO can modulate nuclear gene expression: implications for mitochondrial retrograde signaling. International Journal of Molecular Sciences 18, 786. https://doi.org/10.3390/ijms18040786CrossRefGoogle ScholarPubMed
Yu, L, Ling, C, Li, Y, Guo, H, Xu, A, Qian, H and Li, G (2024) The Bombyx mori G protein beta subunit 1 (BmGNbeta1) gene inhibits BmNPV infection. Journal of Invertebrate Pathology 204, 108097. https://doi.org/10.1016/j.jip.2024.108097CrossRefGoogle ScholarPubMed
Yue, YJ, Tang, XD, Xu, L, Yan, W, Li, QL, Xiao, SY, Fu, XL, Wang, W, Li, N and Shen, ZY (2015) Early responses of silkworm midgut to microsporidium infection – a digital gene expression analysis. Journal of Invertebrate Pathology 124, 6–14. https://doi.org/10.1016/j.jip.2014.10.003CrossRefGoogle ScholarPubMed
Zeng, T, Jaffar, S, Xu, Y and Qi, Y (2022) The intestinal immune defense system in insects. International Journal of Molecular Sciences 23, 15132. https://doi.org/10.3390/ijms232315132CrossRefGoogle ScholarPubMed
Zhai, Z, Huang, X and Yin, Y (2018) Beyond immunity: the Imd pathway as a coordinator of host defense, organismal physiology and behavior. Developmental & Comparative Immunology 83, 51–59. https://doi.org/10.1016/j.dci.2017.11.008CrossRefGoogle ScholarPubMed
Zhang, Z, Yao, M, Zhu, G, Chen, Y, Chen, Y, Sun, F, Zhang, Y, Wang, Q and Shen, Z (2020) Identification and subcellular localization of splicing factor arginine/serine-rich 10 in the microsporidian Nosema bombycis. Journal of Invertebrate Pathology 174, 107441. https://doi.org/10.1016/j.jip.2020.107441CrossRefGoogle ScholarPubMed
Zhou, T, Dang, Y and Zheng, YH (2014) The mitochondrial translocator protein, TSPO, inhibits HIV-1 envelope glycoprotein biosynthesis via the endoplasmic reticulum-associated protein degradation pathway. Journal of Virology 88, 3474–3484. https://doi.org/10.1128/jvi.03286-13CrossRefGoogle ScholarPubMed
Zuzarte-Luís, V, Mello-Vieira, J, Marreiros, IM, Liehl, P, Chora, ÂF, Carret, CK, Carvalho, T and Mota, MM (2017) Dietary alterations modulate susceptibility to Plasmodium infection. Nature Microbiology 2, 1600–1607. https://doi.org/10.1038/s41564-017-0025-2CrossRefGoogle ScholarPubMed
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