A Novel Hemocyte-Derived Peptide and Its Possible Roles in Immune Response of <i>Ciona intestinalis</i> Type A
A wide variety of bioactive peptides have been identified in the central nervous system and several peripheral tissues in the ascidian <i>Ciona intestinalis</i> type A (<i>Ciona robusta</i>). However, hemocyte endocrine peptides have yet to be explored. Here, we report a nove...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2024-02-01
|
| Series: | International Journal of Molecular Sciences |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1422-0067/25/4/1979 |
| _version_ | 1797298082189148160 |
|---|---|
| author | Shin Matsubara Rin Iguchi Michio Ogasawara Hiroya Nakamura Tatsuki R. Kataoka Akira Shiraishi Tomohiro Osugi Tsuyoshi Kawada Honoo Satake |
| author_facet | Shin Matsubara Rin Iguchi Michio Ogasawara Hiroya Nakamura Tatsuki R. Kataoka Akira Shiraishi Tomohiro Osugi Tsuyoshi Kawada Honoo Satake |
| author_sort | Shin Matsubara |
| collection | DOAJ |
| description | A wide variety of bioactive peptides have been identified in the central nervous system and several peripheral tissues in the ascidian <i>Ciona intestinalis</i> type A (<i>Ciona robusta</i>). However, hemocyte endocrine peptides have yet to be explored. Here, we report a novel 14-amino-acid peptide, CiEMa, that is predominant in the granular hemocytes and unilocular refractile granulocytes of <i>Ciona</i>. RNA-seq and qRT-PCR revealed the high <i>CiEma</i> expression in the adult pharynx and stomach. Immunohistochemistry further revealed the highly concentrated CiEMa in the hemolymph of the pharynx and epithelial cells of the stomach, suggesting biological roles in the immune response. Notably, bacterial lipopolysaccharide stimulation of isolated hemocytes for 1–4 h resulted in 1.9- to 2.4-fold increased CiEMa secretion. Furthermore, CiEMa-stimulated pharynx exhibited mRNA upregulation of the growth factor (<i>Fgf3/7/10/22</i>), vanadium binding proteins (<i>CiVanabin1</i> and <i>CiVanabin3</i>), and forkhead and homeobox transcription factors (<i>Foxl2</i>, <i>Hox3</i>, and <i>Dbx</i>) but not antimicrobial peptides (<i>CrPap-a</i> and <i>CrMam-a</i>) or immune-related genes (<i>Tgfbtun3</i>, <i>Tnfa</i>, and <i>Il17-2</i>). Collectively, these results suggest that CiEMa plays roles in signal transduction involving tissue development or repair in the immune response, rather than in the direct regulation of immune response genes. The present study identified a novel <i>Ciona</i> hemocyte peptide, CiEMa, which paves the way for research on the biological roles of hemocyte peptides in chordates. |
| first_indexed | 2024-03-07T22:29:43Z |
| format | Article |
| id | doaj.art-7281d8b524d340c988e683a13be571ae |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-07T22:29:43Z |
| publishDate | 2024-02-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-7281d8b524d340c988e683a13be571ae2024-02-23T15:19:17ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672024-02-01254197910.3390/ijms25041979A Novel Hemocyte-Derived Peptide and Its Possible Roles in Immune Response of <i>Ciona intestinalis</i> Type AShin Matsubara0Rin Iguchi1Michio Ogasawara2Hiroya Nakamura3Tatsuki R. Kataoka4Akira Shiraishi5Tomohiro Osugi6Tsuyoshi Kawada7Honoo Satake8Bioorganic Research Institute, Suntory Foundation for Life Sciences, 8-1-1 Seikadai, Seika-cho, Soraku-gun 619-0284, Kyoto, JapanDepartment of Biology, Graduate School of Science, Chiba University, 1-33 Yayoi-cho, Inage-ku 263-8522, Chiba, JapanDepartment of Biology, Graduate School of Science, Chiba University, 1-33 Yayoi-cho, Inage-ku 263-8522, Chiba, JapanDepartment of Pathology, Iwate Medical University, 2-1-1 Idaidori, Yahaba-cho, Shiwa-gun 028-3695, Iwate, JapanDepartment of Pathology, Iwate Medical University, 2-1-1 Idaidori, Yahaba-cho, Shiwa-gun 028-3695, Iwate, JapanBioorganic Research Institute, Suntory Foundation for Life Sciences, 8-1-1 Seikadai, Seika-cho, Soraku-gun 619-0284, Kyoto, JapanBioorganic Research Institute, Suntory Foundation for Life Sciences, 8-1-1 Seikadai, Seika-cho, Soraku-gun 619-0284, Kyoto, JapanBioorganic Research Institute, Suntory Foundation for Life Sciences, 8-1-1 Seikadai, Seika-cho, Soraku-gun 619-0284, Kyoto, JapanBioorganic Research Institute, Suntory Foundation for Life Sciences, 8-1-1 Seikadai, Seika-cho, Soraku-gun 619-0284, Kyoto, JapanA wide variety of bioactive peptides have been identified in the central nervous system and several peripheral tissues in the ascidian <i>Ciona intestinalis</i> type A (<i>Ciona robusta</i>). However, hemocyte endocrine peptides have yet to be explored. Here, we report a novel 14-amino-acid peptide, CiEMa, that is predominant in the granular hemocytes and unilocular refractile granulocytes of <i>Ciona</i>. RNA-seq and qRT-PCR revealed the high <i>CiEma</i> expression in the adult pharynx and stomach. Immunohistochemistry further revealed the highly concentrated CiEMa in the hemolymph of the pharynx and epithelial cells of the stomach, suggesting biological roles in the immune response. Notably, bacterial lipopolysaccharide stimulation of isolated hemocytes for 1–4 h resulted in 1.9- to 2.4-fold increased CiEMa secretion. Furthermore, CiEMa-stimulated pharynx exhibited mRNA upregulation of the growth factor (<i>Fgf3/7/10/22</i>), vanadium binding proteins (<i>CiVanabin1</i> and <i>CiVanabin3</i>), and forkhead and homeobox transcription factors (<i>Foxl2</i>, <i>Hox3</i>, and <i>Dbx</i>) but not antimicrobial peptides (<i>CrPap-a</i> and <i>CrMam-a</i>) or immune-related genes (<i>Tgfbtun3</i>, <i>Tnfa</i>, and <i>Il17-2</i>). Collectively, these results suggest that CiEMa plays roles in signal transduction involving tissue development or repair in the immune response, rather than in the direct regulation of immune response genes. The present study identified a novel <i>Ciona</i> hemocyte peptide, CiEMa, which paves the way for research on the biological roles of hemocyte peptides in chordates.https://www.mdpi.com/1422-0067/25/4/1979ascidian<i>Ciona</i>hemocytestomachpharynxpeptide |
| spellingShingle | Shin Matsubara Rin Iguchi Michio Ogasawara Hiroya Nakamura Tatsuki R. Kataoka Akira Shiraishi Tomohiro Osugi Tsuyoshi Kawada Honoo Satake A Novel Hemocyte-Derived Peptide and Its Possible Roles in Immune Response of <i>Ciona intestinalis</i> Type A International Journal of Molecular Sciences ascidian <i>Ciona</i> hemocyte stomach pharynx peptide |
| title | A Novel Hemocyte-Derived Peptide and Its Possible Roles in Immune Response of <i>Ciona intestinalis</i> Type A |
| title_full | A Novel Hemocyte-Derived Peptide and Its Possible Roles in Immune Response of <i>Ciona intestinalis</i> Type A |
| title_fullStr | A Novel Hemocyte-Derived Peptide and Its Possible Roles in Immune Response of <i>Ciona intestinalis</i> Type A |
| title_full_unstemmed | A Novel Hemocyte-Derived Peptide and Its Possible Roles in Immune Response of <i>Ciona intestinalis</i> Type A |
| title_short | A Novel Hemocyte-Derived Peptide and Its Possible Roles in Immune Response of <i>Ciona intestinalis</i> Type A |
| title_sort | novel hemocyte derived peptide and its possible roles in immune response of i ciona intestinalis i type a |
| topic | ascidian <i>Ciona</i> hemocyte stomach pharynx peptide |
| url | https://www.mdpi.com/1422-0067/25/4/1979 |
| work_keys_str_mv | AT shinmatsubara anovelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT riniguchi anovelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT michioogasawara anovelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT hiroyanakamura anovelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT tatsukirkataoka anovelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT akirashiraishi anovelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT tomohiroosugi anovelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT tsuyoshikawada anovelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT honoosatake anovelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT shinmatsubara novelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT riniguchi novelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT michioogasawara novelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT hiroyanakamura novelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT tatsukirkataoka novelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT akirashiraishi novelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT tomohiroosugi novelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT tsuyoshikawada novelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea AT honoosatake novelhemocytederivedpeptideanditspossiblerolesinimmuneresponseoficionaintestinalisitypea |