Serine Protease Networks Mediate Immune Responses in Extra-Embryonic Tissues of Eggs in the Tobacco Hornworm, Manduca sexta
The melanization and Toll pathways, regulated by a network of serine proteases and noncatalytic serine protease homologs (SPHs), have been investigated mostly in adult and larval insects. However, how these innate immune reactions are regulated in insect eggs remains unclear. Here we present evidenc...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Karger Publishers
2022-12-01
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| Series: | Journal of Innate Immunity |
| Subjects: | |
| Online Access: | https://www.karger.com/Article/FullText/527974 |
| _version_ | 1797955223325507584 |
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| author | Tisheng Shan Yang Wang Neal T. Dittmer Michael R. Kanost Haobo Jiang |
| author_facet | Tisheng Shan Yang Wang Neal T. Dittmer Michael R. Kanost Haobo Jiang |
| author_sort | Tisheng Shan |
| collection | DOAJ |
| description | The melanization and Toll pathways, regulated by a network of serine proteases and noncatalytic serine protease homologs (SPHs), have been investigated mostly in adult and larval insects. However, how these innate immune reactions are regulated in insect eggs remains unclear. Here we present evidence from transcriptome and proteome analyses that extra-embryonic tissues (yolk and serosa) of early-stage Manduca sexta eggs are immune competent, with expression of immune effector genes including prophenoloxidase and antimicrobial peptides. We identified gene products of the melanization and Toll pathways in M. sexta eggs. Through in vitro reconstitution experiments, we demonstrated that constitutive and infection-induced serine protease cascade modules that stimulate immune responses exist in the extra-embryonic tissues of M. sexta eggs. The constitutive module (HP14b-SP144-GP6) may promote rapid early immune signaling by forming a cascade activating the cytokine Spätzle and regulating melanization by activating prophenoloxidase (proPO). The inducible module (HP14a-HP21-HP5) may trigger enhanced activation of Spätzle and proPO at a later phase of infection. Crosstalk between the two modules may occur in transition from the constitutive to the induced response in eggs inoculated with bacteria. Examination of data from two other well-studied insect species, Tribolium castaneum and Drosophila melanogaster, supports a role for a serosa-dependent constitutive protease cascade in protecting early embryos against invading pathogens. |
| first_indexed | 2024-04-10T23:29:56Z |
| format | Article |
| id | doaj.art-9664e0274e404f758922dcd07e3f22b7 |
| institution | Directory Open Access Journal |
| issn | 1662-811X 1662-8128 |
| language | English |
| last_indexed | 2024-04-10T23:29:56Z |
| publishDate | 2022-12-01 |
| publisher | Karger Publishers |
| record_format | Article |
| series | Journal of Innate Immunity |
| spelling | doaj.art-9664e0274e404f758922dcd07e3f22b72023-01-12T07:42:25ZengKarger PublishersJournal of Innate Immunity1662-811X1662-81282022-12-0111510.1159/000527974527974Serine Protease Networks Mediate Immune Responses in Extra-Embryonic Tissues of Eggs in the Tobacco Hornworm, Manduca sextaTisheng Shan0https://orcid.org/0000-0003-3310-0676Yang Wang1Neal T. Dittmer2Michael R. Kanost3https://orcid.org/0000-0002-6827-0061Haobo Jiang4Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK, USADepartment of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK, USADepartment of Biochemistry and Molecular Biophysics, Kansas State University, Manhattan, KS, USADepartment of Biochemistry and Molecular Biophysics, Kansas State University, Manhattan, KS, USADepartment of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK, USAThe melanization and Toll pathways, regulated by a network of serine proteases and noncatalytic serine protease homologs (SPHs), have been investigated mostly in adult and larval insects. However, how these innate immune reactions are regulated in insect eggs remains unclear. Here we present evidence from transcriptome and proteome analyses that extra-embryonic tissues (yolk and serosa) of early-stage Manduca sexta eggs are immune competent, with expression of immune effector genes including prophenoloxidase and antimicrobial peptides. We identified gene products of the melanization and Toll pathways in M. sexta eggs. Through in vitro reconstitution experiments, we demonstrated that constitutive and infection-induced serine protease cascade modules that stimulate immune responses exist in the extra-embryonic tissues of M. sexta eggs. The constitutive module (HP14b-SP144-GP6) may promote rapid early immune signaling by forming a cascade activating the cytokine Spätzle and regulating melanization by activating prophenoloxidase (proPO). The inducible module (HP14a-HP21-HP5) may trigger enhanced activation of Spätzle and proPO at a later phase of infection. Crosstalk between the two modules may occur in transition from the constitutive to the induced response in eggs inoculated with bacteria. Examination of data from two other well-studied insect species, Tribolium castaneum and Drosophila melanogaster, supports a role for a serosa-dependent constitutive protease cascade in protecting early embryos against invading pathogens.https://www.karger.com/Article/FullText/527974innate immunityinsect immunityserine protease cascadezymogen activationserosa |
| spellingShingle | Tisheng Shan Yang Wang Neal T. Dittmer Michael R. Kanost Haobo Jiang Serine Protease Networks Mediate Immune Responses in Extra-Embryonic Tissues of Eggs in the Tobacco Hornworm, Manduca sexta Journal of Innate Immunity innate immunity insect immunity serine protease cascade zymogen activation serosa |
| title | Serine Protease Networks Mediate Immune Responses in Extra-Embryonic Tissues of Eggs in the Tobacco Hornworm, Manduca sexta |
| title_full | Serine Protease Networks Mediate Immune Responses in Extra-Embryonic Tissues of Eggs in the Tobacco Hornworm, Manduca sexta |
| title_fullStr | Serine Protease Networks Mediate Immune Responses in Extra-Embryonic Tissues of Eggs in the Tobacco Hornworm, Manduca sexta |
| title_full_unstemmed | Serine Protease Networks Mediate Immune Responses in Extra-Embryonic Tissues of Eggs in the Tobacco Hornworm, Manduca sexta |
| title_short | Serine Protease Networks Mediate Immune Responses in Extra-Embryonic Tissues of Eggs in the Tobacco Hornworm, Manduca sexta |
| title_sort | serine protease networks mediate immune responses in extra embryonic tissues of eggs in the tobacco hornworm manduca sexta |
| topic | innate immunity insect immunity serine protease cascade zymogen activation serosa |
| url | https://www.karger.com/Article/FullText/527974 |
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