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Progress of Research on Spatzle and Toll Signaling Pathway in Insects

Received: 3 December 2015    Accepted:     Published: 3 December 2015
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Abstract

Insects are the most diverse group of animals on Earth. Contrary to the vertebrates, insects have no acquired immunity, and to resist the invasion of external microbes, they can only rely on their own innate immunity. Innate immunity is the first line of defense in organisms. When microbia invade, a group of germline-encoded pattern recognition receptors (PRR) can recognize and bind to conserved pathogen-associated molecular pattern (PAMP) , and then the host activates multiple signaling pathways to induce the expression of antimicrobial peptides (AMP). Toll signaling pathway is the most actively studied signaling pathway. Toll and its ligand Spatzle play an important role in Toll pathway of the immune response. The structure and function of spatzle in Drosophila, Manduca sexta, Bombyx mori and other insects have been reviewed in this article. The results suggested that spatzle from different insects have conserved structure and similar activation mechanism and plays an important role in the initiation of Toll signaling pathway. This provides a theoretical basis for research on spatzle and Toll signaling pathway in other insects.

Published in American Journal of Bioscience and Bioengineering (Volume 3, Issue 5)
DOI 10.11648/j.bio.20150305.28
Page(s) 134-141
Creative Commons

This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.

Copyright

Copyright © The Author(s), 2024. Published by Science Publishing Group

Keywords

Insects, Innate Immunity, Humoral Immunity, Spatzle, Toll Pathway

References
[1] 吕鸿声.昆虫免疫学原理[M].上海:上海科学技术出版社,2008.12:20。
[2] 张明明,初源,赵章武,安春菊.昆虫天然免疫反应分子机制研究进展[J].昆虫学报,2012,55(10):1221—1229。
[3] Marcia P, Belvin, Kathryn V Anderson. A conserved signaling pathway: The Drosophila Toll-Dorsal Pathway[J]. Cell Dev Biol, 1996, 12:393–416.
[4] Medzhitov R, Janeway C Jr. Innate immune recognition: mechanisms and pathways[J]. Immunol Rev, 2000, 173, 89-97.
[5] Janeway CA Jr. Approaching the asymptote Evolution and revolution in immunology[J]. Cold Spring Harb Symp Quant Biol, 1989. 54: 1-13.
[6] James S. Parker, Kenji Mizuguchi, and Nicholas J. Gay. A Family of Proteins Related to Spatzle, the Toll Receptor Ligand, Are Encoded in the Drosophila Genome [J]. PROTEINS: Structure, Function, and Genetics, 2001, 45: 71-80.
[7] Ming M, Obata F, Kuranaga E, Miura M. Persephone/Spätzle pathogen sensors mediate the activation of Toll receptor signaling in response to endogenous danger signals in apoptosis-deficient Drosophila [J]. J Biol Chem. 2014. 289(11): 7558-68.
[8] Hoffmann A, Funkner A, Neumann P et al. Biophysical characterization of refolded Drosophila Spatzle, a Cystine Knot Protein,Reveals Distinct Properties of Three Isoforms[J]. J Biol Chem, 2008, Nov 21; 283(47): 32598-609.
[9] Christopher J. Arnot, Nicholas J. Gay, and Monique Gangloff. Molecular Mechanism That Induces Activation of Spatzle, the Ligand for the Drosophila Toll Receptor[J]. THE JOURNAL OF BIOLOGICAL CHEMISTRY, 2010, 25, 19502-19509.
[10] Weber AN, Tauszig-Delamasure S, Hoffmann JA et al. Binding of the Drosophila cytokine Spätzle to Toll is direct and establishes signaling[J]. Nat Immunol, 2003, 4(8): 794-800.
[11] LeMosy EK, Tan YQ, Hashimoto C. Activation of a protease cascade involved inpatterning the Drosophila embryo[J]. Proc Natl Acad Sci USA, 2001, 98: 5055–5060.
[12] Cho, Y. S., L. M. Stevens, and D. Stein. Pipe-dependent ventral processing of Easter by Snake is the defining step in Drosophila embryo DV axis formation[J]. Curr. Biol. 2010. 20: 1133–1137.
[13] David Stein, Iphigenie Charatsi, Yong Suk Cho, Zhenyu Zhang, Jesse Nguyen, Robert DeLotto, Stefan Luschnig, and Bernard Moussian. Localization and Activation of the Drosophila Protease Easter Require the ER-Resident Saposin-like Protein Seele [J]. Current Biology, 2010, 20, 1953-1958.
[14] Gobert V, Gottar M, Matskevich A. Dual activation of the Drosophila toll pathway by two pattern recognition receptors[J]. Science, 2003, 302(5653): 2126-2130.
[15] El Chamy, L., V. Leclerc, I. Caldelari, and J. M. Reichhart. Sensing of‘danger signals’ and pathogen-associated molecular patterns defines binary signaling pathways ‘upstream’ of Toll [J]. Nat. Immunol. 2008. 9: 1165–1170.
[16] Kambris, Z., S. Brun, I. H. Jang, H. J. Nam, Y. Romeo, K. Takahashi, W. J. Lee,R. Ueda, and B. Lemaitre. Drosophila immunity: a large-scale in vivo RNAi screen identifies five serine proteases required for Toll activation[J]. Curr. Biol. 2006.16:808–813.
[17] Buchon, N., M. Poidevin, H. M. Kwon, A. Guillou, V. Sottas, B. L. Lee, and B. Lemaitre. A single modular serine protease integrates signals from pattern-recognition receptors upstream of the Drosophila Toll pathway[J]. Proc. Natl.Acad. Sci. USA .2009.106: 12442–12447.
[18] Gottar, M., V. Gobert, A. A. Matskevich, J. M. Reichhart, C. Wang, T. M. Butt, M. Belvin, J. A. Hoffmann, and D. Ferrandon. Dual detection of fungal infections in Drosophila via recognition of glucans and sensing of virulence factors[J].Cell. 2006. 127: 1425–1437.
[19] Nadège Peltea, Andrew S. Robertsonb, Zhen Zouc, Didier Belorgeyb, Timothy R. Daffornd, Haobo Jiangc, David Lomase, Jean-Marc Reichharta, and David Gubbf. Immune challenge induces N-terminal cleavage of the Drosophila serpin Necrotic [J]. Insect Biochem Mol Biol, 2006 ,36(1): 37-46.
[20] Yamamoto-Hino M, Muraoka M, Kondo S, Ueda R, Okano H, Goto S. Dynamic regulation of innate immune responses in Drosophila by Senju-mediated glycosylation [J]. Proc Natl Acad Sci U S A. 2015. 112(18): 5809-14.
[21] Susanna Valanne, Jing-Huan Wang and Mika Rämet. The Drosophila Toll Signaling Pathway[J]. Immunol 2011.186: 649-656.
[22] An C, Jiang H, Kanost MR. Proteolytic activation and function of the cytokine Spatzle in the innate immune response of a lepidopteran insect, Manduca sexta[J]. FEBS, 2010, 277(1): 148-162.
[23] Chunju An, Jun Ishibashi, Emily J. Ragan, Haobo Jiang, and Michael R. Kanost. Functions of Manduca sexta Hemolymph Proteinases HP6 and HP8 in Two Innate Immune Pathways[J]. THE JOURNAL OF BIOLOGICAL CHEMISTRY, 2009, 29, 19716-19726.
[24] Taniai K, Ishii T, Sugiyama M. Nucleotide sequence of 5’-upstream region and expression of a silkworm gene encoding a new member of the attacin family[J]. Biochem Biophys Res Commun, 1996, 220(3): 594-599.
[25] Wang Y, Cheng T, Rayaprolu S et al. Proteolytic activation of pro-spatzle is required for the induced transcription of antimicrobial peptide genes in lepidopteran insects[J]. Dev Comp Immunol, 2007, 31(10): 1002-1012.
[26] 徐颖.家蚕新的免疫基因Spatzle克隆与功能及假单胞菌致病性研究[D]. 镇江:江苏科技大学硕士学位论文,2012。
[27] Lu ping Zheng, Lin Hou, Miao Yu, Xiang Li, Xiang-yang Zou. Cloning and the expression pattern of Spatzle gene during embryonic development and bacterial challenge in Artemia sinica[J]. Mol Biol Rep, 2012, 39: 6035-6042.
[28] Sang Woon Shin, Guowu Bian, and Alexander S. Raikhel. A Toll Receptor and a Cytokine, Toll5A and Spz1C, Are Involved in Toll Antifungal Immune Signaling in the Mosquito Aedes aegypti[J]. THE JOURNAL OF BIOLOGICAL CHEMISTRY. 2006, 51, 39388-39395.
[29] Christophides, G. K., Zdobnov, E., Barillas-Mury, C., Birney, E., Blandin, S., Blass, C., Brey, P. T., Collins, F. H., Danielli, A., Dimopoulos, G., Hetru, C., Hoa, N. T., Hoffmann, J. A., Kanzok, S. M., Letunic, I., Levashina, E. A., Loukeris, T. G., Lycett, G., Meister, S., Michel, K., Moita, L. F., Muller, H. M., Osta, M. A., Paskewitz, S. M., Reichhart, J. M., Rzhetsky, A., Troxler, L., Vernick, K. D., Vlachou, D., Volz, J., von Mering, C., Xu, J., Zheng, L., Bork, P., and Kafatos, F. C. Immunity-related genes and gene families in Anopheles gambiae[J]. Science. 2002, 298, 159-165.
[30] 黎群英, 张涛, 张传博.昆虫Toll受体及其研究进展[J].贵州农业科学.2008,36(6):67-69。
[31] Kimbrell D.A, Beutler B. The evolution and genetics of innate immunity[J]. Nat Rev Genet, 2001, 2: 256-267.
[32] Halfon M.S, Hashimoto C, Keshishian H. The Drosophila toll gene functions zygotically and is necessary for proper motoneuron and muscle development[J]. Dev Biol, 1995, 169: 151-167.
[33] Lemaitre B, Nicolas E, Michaut L et al. The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults[J]. Cell, 1996, 86: 973-983.
[34] Wu C, Chen C, Dai J, Zhang F, Chen Y, Li W, Pastor-Pareja JC, Xue L.Toll pathway modulates TNF-induced JNK-dependent cell death in Drosophila [J]. Open Biol. 2015. 5(7): 140171.
[35] Andy J. Chang and Donald Morisato. Regulation of Easter activity is required for shaping the Dorsal gradient in the Drosophila embryo[J]. Development, 2002, 129, 5635-5645.
[36] Ferreira ÁG, Naylor H, Esteves SS, Pais IS, Martins NE, Teixeira L. The Toll-dorsal pathway is required for resistance to viral oral infection in Drosophila [J]. PLoS Pathog. 2014. 10(12): e1004507.
[37] De Gregorio E, Spellman PT, Tzou P. The Toll and Imd pathways are the major regulators of the immune response in Drosophila[J]. EMBO, 2002, 21: 2568–2579.
[38] Mizuguchi K, Parker JS, Blundell TL. Getting knotted: a model forthe structure and activation of Spatzle[J]. Trends Biochem Sci, 1998, 23: 239–242.
[39] Arnot CJ, Gay NJ, Gangloff M. Molecular mechanism that induces activation of Spatzle, the ligand for the Drosophila toll receptor[J]. Biol Chem, 2010, 285: 19502-19509.
[40] Xue Zhong, Xiao-Xia Xu. A Toll-Spätzle pathway in the tobacco hornworm, Manduca sexta[J]. Insect Biochemistry and Molecular Biology, 2012, 42: 514-524.
[41] Valanne S, Wang JH, Ramet M. The Drosophila Toll signaling pathway[J]. Immunol, 2011, 186: 649-656.
[42] Miranda Lewisa, Christopher J. Arnota, Helen Beestonb, Airlie McCoyc, Alison E. Ashcroftb, Nicholas J. Gaya, and Monique Gangloffa. Cytokine Spätzle binds to the Drosophila immunoreceptor Toll with a neurotrophin-like specificity and couples receptor activation[J]. Proc Natl Acad Sci U S A. 2013, 17,110(51): 20461-20466.
[43] Parthier C, Stelter M, Ursel C, Fandrich U, Lilie H, Breithaupt C, Stubbs MT. Structure of the Toll-Spatzle complex, a molecular hub in Drosophila development and innate immunity [J]. Proc Natl Acad Sci U S A. 2014. 111(17): 6281-6.
[44] Hu X, Yagi Y, Tanji T et al. Multimerization and interaction of Toll and Spatzle in Drosophila[J]. Proc. Natl Acad Sci USA, 2004, 101: 9369-9374.
[45] Moncrieffe MC, Grossmann JG, Gay NJ. Assembly of oligomeric death domain complexes during Toll receptor signaling[J]. Biol Chem, 2008, 283: 33447-33454.
[46] Kanost MR, Jiang H, Yu XQ. Innate immune responses of a lepidopteran insect, Manduca sexta[J]. Immunol Rev, 2004, 198: 97-105.
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    Ji Liu, Jinmei Wu. (2015). Progress of Research on Spatzle and Toll Signaling Pathway in Insects. American Journal of Bioscience and Bioengineering, 3(5), 134-141. https://doi.org/10.11648/j.bio.20150305.28

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    Ji Liu; Jinmei Wu. Progress of Research on Spatzle and Toll Signaling Pathway in Insects. Am. J. BioSci. Bioeng. 2015, 3(5), 134-141. doi: 10.11648/j.bio.20150305.28

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    AMA Style

    Ji Liu, Jinmei Wu. Progress of Research on Spatzle and Toll Signaling Pathway in Insects. Am J BioSci Bioeng. 2015;3(5):134-141. doi: 10.11648/j.bio.20150305.28

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  • @article{10.11648/j.bio.20150305.28,
      author = {Ji Liu and Jinmei Wu},
      title = {Progress of Research on Spatzle and Toll Signaling Pathway in Insects},
      journal = {American Journal of Bioscience and Bioengineering},
      volume = {3},
      number = {5},
      pages = {134-141},
      doi = {10.11648/j.bio.20150305.28},
      url = {https://doi.org/10.11648/j.bio.20150305.28},
      eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.bio.20150305.28},
      abstract = {Insects are the most diverse group of animals on Earth. Contrary to the vertebrates, insects have no acquired immunity, and to resist the invasion of external microbes, they can only rely on their own innate immunity. Innate immunity is the first line of defense in organisms. When microbia invade, a group of germline-encoded pattern recognition receptors (PRR) can recognize and bind to conserved pathogen-associated molecular pattern (PAMP) , and then the host activates multiple signaling pathways to induce the expression of antimicrobial peptides (AMP). Toll signaling pathway is the most actively studied signaling pathway. Toll and its ligand Spatzle play an important role in Toll pathway of the immune response. The structure and function of spatzle in Drosophila, Manduca sexta, Bombyx mori and other insects have been reviewed in this article. The results suggested that spatzle from different insects have conserved structure and similar activation mechanism and plays an important role in the initiation of Toll signaling pathway. This provides a theoretical basis for research on spatzle and Toll signaling pathway in other insects.},
     year = {2015}
    }
    

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  • TY  - JOUR
    T1  - Progress of Research on Spatzle and Toll Signaling Pathway in Insects
    AU  - Ji Liu
    AU  - Jinmei Wu
    Y1  - 2015/12/03
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    N1  - https://doi.org/10.11648/j.bio.20150305.28
    DO  - 10.11648/j.bio.20150305.28
    T2  - American Journal of Bioscience and Bioengineering
    JF  - American Journal of Bioscience and Bioengineering
    JO  - American Journal of Bioscience and Bioengineering
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    PB  - Science Publishing Group
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    UR  - https://doi.org/10.11648/j.bio.20150305.28
    AB  - Insects are the most diverse group of animals on Earth. Contrary to the vertebrates, insects have no acquired immunity, and to resist the invasion of external microbes, they can only rely on their own innate immunity. Innate immunity is the first line of defense in organisms. When microbia invade, a group of germline-encoded pattern recognition receptors (PRR) can recognize and bind to conserved pathogen-associated molecular pattern (PAMP) , and then the host activates multiple signaling pathways to induce the expression of antimicrobial peptides (AMP). Toll signaling pathway is the most actively studied signaling pathway. Toll and its ligand Spatzle play an important role in Toll pathway of the immune response. The structure and function of spatzle in Drosophila, Manduca sexta, Bombyx mori and other insects have been reviewed in this article. The results suggested that spatzle from different insects have conserved structure and similar activation mechanism and plays an important role in the initiation of Toll signaling pathway. This provides a theoretical basis for research on spatzle and Toll signaling pathway in other insects.
    VL  - 3
    IS  - 5
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Author Information
  • College of Biotechnology, Jiangsu Universitiy of Scence and Technology, Zhenjiang, China

  • College of Biotechnology, Jiangsu Universitiy of Scence and Technology, Zhenjiang, China; The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, China

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