Functional Analysis of a Multiple-Domain CTL15 in the Innate Immunity, Eclosion, and Reproduction of <i>Tribolium castaneum</i>

C-type lectin X (CTL-X) plays critical roles in immune defense, cell adhesion, and developmental regulation. Here, a transmembrane CTL-X of <i>Tribolium castaneum</i>, <i>TcCTL15,</i> with multiple domains was characterized. It was highly expressed in the early and late pupae...

Full description

Bibliographic Details
Main Authors: Suisui Wang, Huayi Ai, Yonglei Zhang, Jingxiu Bi, Han Gao, Peng Chen, Bin Li
Format: Article
Language:English
Published: MDPI AG 2023-02-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/12/4/608
_version_ 1797621819336818688
author Suisui Wang
Huayi Ai
Yonglei Zhang
Jingxiu Bi
Han Gao
Peng Chen
Bin Li
author_facet Suisui Wang
Huayi Ai
Yonglei Zhang
Jingxiu Bi
Han Gao
Peng Chen
Bin Li
author_sort Suisui Wang
collection DOAJ
description C-type lectin X (CTL-X) plays critical roles in immune defense, cell adhesion, and developmental regulation. Here, a transmembrane CTL-X of <i>Tribolium castaneum</i>, <i>TcCTL15,</i> with multiple domains was characterized. It was highly expressed in the early and late pupae and early adults and was distributed in all examined tissues. In addition, its expression levels were significantly induced after being challenged with pathogen-associated molecular patterns (PAMPs) and bacteria. In vitro, the recombinant TcCTL15 could recognize bacteria through binding PAMPs and exhibit agglutinating activity against a narrow range of bacteria in the presence of Ca<sup>2+</sup>. RNAi-mediated <i>TcCTL15</i>-knockdown-larvae infected with <i>Escherichia coli</i> and <i>Staphylococcus aureus</i> showed less survival, had activated immune signaling pathways, and induced the expression of antimicrobial peptide genes. Moreover, silencing <i>TcCTL15</i> caused eclosion defects by impairing ecdysone and crustacean cardioactive peptide receptors (CCAPRs). Suppression of <i>TcCTL15</i> in female adults led to defects in ovary development and fecundity, accompanied by concomitant reductions in the mRNA levels of vitellogenin (<i>TcVg)</i> and farnesol dehydrogenase (<i>TcFDH)</i>. These findings imply that TcCTL15 has extensive functions in developmental regulation and antibacterial immunity. Uncovering the function of TcCTL15 will enrich the understanding of CTL-X in invertebrates. Its multiple biological functions endow the potential to be an attractive target for pest control.
first_indexed 2024-03-11T09:01:24Z
format Article
id doaj.art-e456c0d0297b447c87a9be9e742196b2
institution Directory Open Access Journal
issn 2073-4409
language English
last_indexed 2024-03-11T09:01:24Z
publishDate 2023-02-01
publisher MDPI AG
record_format Article
series Cells
spelling doaj.art-e456c0d0297b447c87a9be9e742196b22023-11-16T19:44:44ZengMDPI AGCells2073-44092023-02-0112460810.3390/cells12040608Functional Analysis of a Multiple-Domain CTL15 in the Innate Immunity, Eclosion, and Reproduction of <i>Tribolium castaneum</i>Suisui Wang0Huayi Ai1Yonglei Zhang2Jingxiu Bi3Han Gao4Peng Chen5Bin Li6Jiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, ChinaJiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, ChinaJiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, ChinaJiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, ChinaJiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, ChinaJiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, ChinaJiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, ChinaC-type lectin X (CTL-X) plays critical roles in immune defense, cell adhesion, and developmental regulation. Here, a transmembrane CTL-X of <i>Tribolium castaneum</i>, <i>TcCTL15,</i> with multiple domains was characterized. It was highly expressed in the early and late pupae and early adults and was distributed in all examined tissues. In addition, its expression levels were significantly induced after being challenged with pathogen-associated molecular patterns (PAMPs) and bacteria. In vitro, the recombinant TcCTL15 could recognize bacteria through binding PAMPs and exhibit agglutinating activity against a narrow range of bacteria in the presence of Ca<sup>2+</sup>. RNAi-mediated <i>TcCTL15</i>-knockdown-larvae infected with <i>Escherichia coli</i> and <i>Staphylococcus aureus</i> showed less survival, had activated immune signaling pathways, and induced the expression of antimicrobial peptide genes. Moreover, silencing <i>TcCTL15</i> caused eclosion defects by impairing ecdysone and crustacean cardioactive peptide receptors (CCAPRs). Suppression of <i>TcCTL15</i> in female adults led to defects in ovary development and fecundity, accompanied by concomitant reductions in the mRNA levels of vitellogenin (<i>TcVg)</i> and farnesol dehydrogenase (<i>TcFDH)</i>. These findings imply that TcCTL15 has extensive functions in developmental regulation and antibacterial immunity. Uncovering the function of TcCTL15 will enrich the understanding of CTL-X in invertebrates. Its multiple biological functions endow the potential to be an attractive target for pest control.https://www.mdpi.com/2073-4409/12/4/608C-type lectin X<i>Tribolium castaneum</i>RNAiinnate immunityeclosionreproduction
spellingShingle Suisui Wang
Huayi Ai
Yonglei Zhang
Jingxiu Bi
Han Gao
Peng Chen
Bin Li
Functional Analysis of a Multiple-Domain CTL15 in the Innate Immunity, Eclosion, and Reproduction of <i>Tribolium castaneum</i>
Cells
C-type lectin X
<i>Tribolium castaneum</i>
RNAi
innate immunity
eclosion
reproduction
title Functional Analysis of a Multiple-Domain CTL15 in the Innate Immunity, Eclosion, and Reproduction of <i>Tribolium castaneum</i>
title_full Functional Analysis of a Multiple-Domain CTL15 in the Innate Immunity, Eclosion, and Reproduction of <i>Tribolium castaneum</i>
title_fullStr Functional Analysis of a Multiple-Domain CTL15 in the Innate Immunity, Eclosion, and Reproduction of <i>Tribolium castaneum</i>
title_full_unstemmed Functional Analysis of a Multiple-Domain CTL15 in the Innate Immunity, Eclosion, and Reproduction of <i>Tribolium castaneum</i>
title_short Functional Analysis of a Multiple-Domain CTL15 in the Innate Immunity, Eclosion, and Reproduction of <i>Tribolium castaneum</i>
title_sort functional analysis of a multiple domain ctl15 in the innate immunity eclosion and reproduction of i tribolium castaneum i
topic C-type lectin X
<i>Tribolium castaneum</i>
RNAi
innate immunity
eclosion
reproduction
url https://www.mdpi.com/2073-4409/12/4/608
work_keys_str_mv AT suisuiwang functionalanalysisofamultipledomainctl15intheinnateimmunityeclosionandreproductionofitriboliumcastaneumi
AT huayiai functionalanalysisofamultipledomainctl15intheinnateimmunityeclosionandreproductionofitriboliumcastaneumi
AT yongleizhang functionalanalysisofamultipledomainctl15intheinnateimmunityeclosionandreproductionofitriboliumcastaneumi
AT jingxiubi functionalanalysisofamultipledomainctl15intheinnateimmunityeclosionandreproductionofitriboliumcastaneumi
AT hangao functionalanalysisofamultipledomainctl15intheinnateimmunityeclosionandreproductionofitriboliumcastaneumi
AT pengchen functionalanalysisofamultipledomainctl15intheinnateimmunityeclosionandreproductionofitriboliumcastaneumi
AT binli functionalanalysisofamultipledomainctl15intheinnateimmunityeclosionandreproductionofitriboliumcastaneumi