Roles of interleukins in antibacterial immune defense of the brood pouch in the lined seahorse <italic style="font-style: italic">Hippocampus erectus</italic>

Han JIANG; Chunyan LI; Bo ZHANG; Yongli WU; Qiang LIN

doi:10.1007/s00343-021-0310-z

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Roles of interleukins in antibacterial immune defense of the brood pouch in the lined seahorse Hippocampus erectus

Biology | Updated：2023-04-27

- Roles of interleukins in antibacterial immune defense of the brood pouch in the lined seahorse Hippocampus erectus
- Journal of Oceanology and Limnology Vol. 40, Issue 1, Pages: 235-244(2022)
- Affiliations：
  
  1.CAS Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
  2.Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
  3.University of Chinese Academy of Sciences, Beijing 100049, China
- Author bio：
  
  Chunyan LI, E-mail: cyli@scsio.ac.cn
  Qiang LIN, E-mail: linqiang@scsio.ac.cn
- Funds：
- DOI：10.1007/s00343-021-0310-z
  CLC：
- Received：19 August 2020，
  
  Accepted：25 September 2020，
  
  Online First：19 January 2021，
  
  Published：2022-01
- Accepted：
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Han JIANG, Chunyan LI, Bo ZHANG, et al. Roles of interleukins in antibacterial immune defense of the brood pouch in the lined seahorse Hippocampus erectus[J]. Journal of Oceanology and Limnology, 2022, 40(1): 235-244.
DOI：

Han JIANG, Chunyan LI, Bo ZHANG, et al. Roles of interleukins in antibacterial immune defense of the brood pouch in the lined seahorse Hippocampus erectus[J]. Journal of Oceanology and Limnology, 2022, 40(1): 235-244. DOI： 10.1007/s00343-021-0310-z.

摘要

Abstract

Seahorse embryos are brooded in the enclosed nutrient-rich environment of the male brood pouch

which may be prone to bacterial infection. The immune responses of interleukin (IL) genes in the brood pouch have not been well studied. We identified 13 interleukins in the lined seahorse

Hippocampus erectus

. Tissue-specific expression analysis revealed increased mRNA expression levels of

il-1β

il-18

and

il-8

in the brood pouch. When challenged with lipopolysaccharide or

Vibrio parahaemolyticus

il-1β

and

il-18

were active as part of the acute and chronic inflammatory responses

respectively. Importantly

il-8

may be involved in powerful antibacterial immune responses and may be induced by

il-1β

and

il-18

via a process involving the nuclear factor-κB signaling pathway. These results suggest that

il-1β

il-18

and

il-8

may play key roles in the antibacterial immune defense of the brood pouch in male seahorses.

关键词

Keywords

references

S Akira . The role of IL-18 in innate immunity . Current Opinion in Immunology , 2000 . 12 ( 1 ): 59 - 63 . DOI: 10.1016/s0952-7915(99)00051-5 http://doi.org/10.1016/s0952-7915(99)00051-5 .

F Biet , C Locht , L Kremer . Immunoregulatory functions of interleukin 18 and its role in defense against bacterial pathogens . Journal of Molecular Medicine , 2002 . 80 ( 3 ): 147 - 162 . DOI: 10.1007/s00109-001-0307-1 http://doi.org/10.1007/s00109-001-0307-1 .

S Bird , J Zou , T H Wang , B Munday , C Cunningham , C J Secombes . Evolution of interleukin-1β . Cytokine & Growth Factor Reviews , 2002 . 13 ( 6 ): 483 - 502 . DOI: 10.1016/s1359-6101(02)00028-x http://doi.org/10.1016/s1359-6101(02)00028-x .

Y X Bo , X H Song , K Wu , B Hu , B Y Sun , Z J Liu , J G Fu . Characterization of interleukin-1β as a proinflammatory cytokine in grass carp ( Ctenopharyngodon idella ) . Fish & Shellfish Immunology , 2015 . 46 ( 2 ): 584 - 595 . DOI: 10.1016/j.fsi.2015.07.024 http://doi.org/10.1016/j.fsi.2015.07.024 .

S A Bustin , V Benes , J A Garson , J Hellemans , J Huggett , M Kubista , R Mueller , T Nolan , M W Pfaffl , G L Shipley , J Vandesompele , C T Wittwer . The MIQE guidelines: M inimum I nformation for publication of Quantitative real-time PCR Experiments . Clinical Chemistry , 2009 . 55 ( 4 ): 611 - 622 . DOI: 10.1373/clinchem.2008.112797 http://doi.org/10.1373/clinchem.2008.112797 .

R C Edgar . MUSCLE: multiple sequence alignment with high accuracy and high throughput . Nucleic Acids Research , 2004 . 32 ( 5 ): 1 792 - 1 797 . DOI: 10.1093/nar/gkh340 http://doi.org/10.1093/nar/gkh340 .

R Geisert , A Fazleabas , M Lucy , D Mathew . Interaction of the conceptus and endometrium to establish pregnancy in mammals: role of interleukin 1β . Cell and Tissue Research , 2012 . 349 ( 3 ): 825 - 838 . DOI: 10.1007/s00441-012-1356-1 http://doi.org/10.1007/s00441-012-1356-1 .

S Ghosh , M S Hayden . New regulators of NF-κB in inflammation . Nature Reviews Immunology , 2008 . 8 ( 11 ): 837 - 848 . DOI: 10.1038/nri2423 http://doi.org/10.1038/nri2423 .

M S Hayden , S Ghosh . NF-κB in immunobiology . Cell Research , 2011 . 21 ( 2 ): 223 - 244 . DOI: 10.1038/cr.2011.13 http://doi.org/10.1038/cr.2011.13 .

J Heled , A J Drummond . Bayesian inference of species trees from multilocus data . Molecular Biology and Evolution , 2010 . 27 ( 3 ): 570 - 580 . DOI: 10.1093/molbev/msp274 http://doi.org/10.1093/molbev/msp274 .

H M L P B Herath , D A S Elvitigala , G I Godahewa , N Umasuthan , I Whang , J K Noh , J Lee . Molecular characterization and comparative expression analysis of two teleostean pro-inflammatory cytokines, IL-1β and IL-8 , from Sebastes schlegeli . Gene , 2016 . 575 ( 2 ): 732 - 742 . DOI: 10.1016/j.gene.2015.09.082 http://doi.org/10.1016/j.gene.2015.09.082 .

P Y Ho , O Byadgi , P C Wang , M A Tsai , L L Liaw , S C Chen . Identification, molecular cloning of IL-1β and its expression profile during Nocardia seriolae infection in largemouth bass, Micropterus salmoides . International Journal of Molecular Sciences , 2016 . 17 ( 10 ): 1 670 DOI: 10.3390/ijms17101670 http://doi.org/10.3390/ijms17101670 .

P Kaiser , L Rothwell , S Avery , S Balu . Evolution of the interleukins . Developmental & Comparative Immunology , 2004 . 28 ( 5 ): 375 - 394 . DOI: 10.1016/j.dci.2003.09.004 http://doi.org/10.1016/j.dci.2003.09.004 .

M Kawaguchi , R Okubo , A Harada , K Miyasaka , K Takada , J Hiroi , S Yasumasu . Morphology of brood pouch formation in the pot-bellied seahorse Hippocampus abdominalis . Zoological Letters , 2017 . 3 ( 1 ): 19 DOI: 10.1186/s40851-017-0080-9 http://doi.org/10.1186/s40851-017-0080-9 .

P Laksanawimol , P Damrongphol , M Kruatrachue . Alteration of the brood pouch morphology during gestation of male seahorses, Hippocampus kuda . Marine and Freshwater Research , 2006 . 57 ( 5 ): 497 - 502 . DOI: 10.1071/MF05112 http://doi.org/10.1071/MF05112 .

C Li , C L Yao . Molecular and expression characterizations of interleukin-8 gene in large yellow croaker ( Larimichthys crocea ) . Fish & Shellfish Immunology , 2013 . 34 ( 3 ): 799 - 809 . DOI: 10.1016/j.fsi.2012.12.019 http://doi.org/10.1016/j.fsi.2012.12.019 .

C L Liao , G R Zhang , D M Zhu , W Ji , Z C Shi , R Jiang , Q X Fan , K J Wei . Molecular cloning and expression analysis of interleukin-1β and interleukin-1 receptor type I genes in yellow catfish ( Pelteobagrus fulvidraco ): responses to challenge of Edwardsiella ictaluri . Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology , 2018 . 223 1 - 15 . DOI: 10.1016/j.cbpb.2018.05.001 http://doi.org/10.1016/j.cbpb.2018.05.001 .

Q Lin , S H Fan , Y H Zhang , M Xu , H X Zhang , Y L Yang , A P Lee , J M Woltering , V Ravi , H M Gunter , W Luo , Z X Gao , Z W Lim , G Qin , R F Schneider , X Wang , P W Xiong , G Li , K Wang , J M Min , C Zhang , Y Qiu , J Bai , C He W M Bian , X H Zhang , D Shan , H Y Qu , Y Sun , Q Gao , L M Huang , Q Shi , A Meyer , B Venkatesh . The seahorse genome and the evolution of its specialized morphology . Nature , 2016 . 540 ( 7633 ): 395 - 399 . DOI: 10.1038/nature20595 http://doi.org/10.1038/nature20595 .

K J Livak , T D Schmittgen . Analysis of relative gene expression data using real-time quantitative PCR and the 2 -ΔΔ C t method . Methods , 2001 . 25 ( 4 ): 402 - 408 . DOI: 10.1006/meth.2001.1262 http://doi.org/10.1006/meth.2001.1262 .

W Luo , X Wang , H Y Qu , G Qin , H X Zhang , Q Lin . Genomic structure and expression pattern of MHC IIα and IIβ genes reveal an unusual immune trait in lined seahorse Hippocampus erectus . Fish & Shellfish Immunology , 2016 . 58 521 - 529 . DOI: 10.1016/j.fsi.2016.09.057 http://doi.org/10.1016/j.fsi.2016.09.057 .

P Melamed , Y Xue , J F Poon , Q Wu , H Xie , J Yeo , T W Foo , H K Chua . The male seahorse synthesizes and secretes a novel C-type lectin into the brood pouch during early pregnancy . The FEBS Journal , 2005 . 272 ( 5 ): 1 221 - 1 235 . DOI: 10.1111/j.1742-4658.2005.04556.x http://doi.org/10.1111/j.1742-4658.2005.04556.x .

R Nichols . Gene trees and species trees are not the same . Trends in Ecology & Evolution , 2001 . 16 ( 7 ): 358 - 364 . DOI: 10.1016/s0169-5347(01)02203-0 http://doi.org/10.1016/s0169-5347(01)02203-0 .

M Oh , S D N K Bathige , Y Kim , S Lee , H Yang , M J Kim , J Lee . A CXCL ortholog from Hippocampus abdominalis : Molecular features and functional delineation as a pro-inflammatory chemokine . Fish & Shellfish Immunology , 2017 . 67 218 - 227 . DOI: 10.1016/j.fsi.2017.05.050 http://doi.org/10.1016/j.fsi.2017.05.050 .

G Qin , Y H Zhang , X Wang , Q Lin . Effects of anesthetic disposal on the physiological and behavioral responses of the lined seahorses, Hippocampus erectus . Journal of the World Aquaculture Society , 2016 . 47 ( 3 ): 387 - 395 . DOI: 10.1111/jwas.12282 http://doi.org/10.1111/jwas.12282 .

G Rosenqvist , A Berglund . Sexual signals and mating patterns in Syngnathidae . Journal of Fish Biology , 2011 . 78 ( 6 ): 1 647 - 1 661 . DOI: 10.1111/j.1095-8649.2011.02972.x http://doi.org/10.1111/j.1095-8649.2011.02972.x .

O Roth , M H Solbakken , O K Tørresen , T Bayer , M Matschiner , H T Baalsrud , S N K Hoff , M S O Brieuc , D Haase , R Hanel , T B H Reusch , S Jentoft . Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes . Proceedings of the National Academy of Sciences of the United States of America , 2020 . 117 ( 17 ): 9 431 - 9 439 . DOI: 10.1073/pnas.1916251117 http://doi.org/10.1073/pnas.1916251117 .

C J Secombes , T Wang , S Bird . The interleukins of fish . Developmental & Comparative Immunology , 2011 . 35 ( 12 ): 1 336 - 1 345 . DOI: 10.1016/j.dci.2011.05.001 http://doi.org/10.1016/j.dci.2011.05.001 .

A Shimoyama , A Saeki , N Tanimura , H Tsutsui , K Miyake , Y Suda , Y Fujimoto , K Fukase . Chemical synthesis of Helicobacter pylori lipopolysaccharide partial structures and their selective proinflammatory responses . Chemistry-A European Journal , 2011 . 17 ( 51 ): 14 464 - 14 474 . DOI: 10.1002/chem.201003581 http://doi.org/10.1002/chem.201003581 .

M Sugimoto , T Ohno , D Y Graham , Y Yamaoka . Gastric mucosal interleukin-17 and -18 mRNA expression in Helicobacter pylori-induced Mongolian gerbils . Cancer Science , 2009 . 100 ( 11 ): 2 152 - 2 159 . DOI: 10.1111/j.1349-7006.2009.01291.x http://doi.org/10.1111/j.1349-7006.2009.01291.x .

M D N Tharuka , S D N K Bathige , M Oh , S Lee , M J Kim , T T Priyathilaka , J Lee . Molecular characterization and expression analysis of big-belly seahorse ( Hippocampus abdominalis ) interleukin-10 and analysis of its potent anti-inflammatory properties in LPS-induced murine macrophage RAW 264.7 cells . Gene , 2019 . 685 1 - 11 . DOI: 10.1016/j.gene.2018.10.053 http://doi.org/10.1016/j.gene.2018.10.053 .

E L Wang , J Wang , B Long , K Y Wang , Y He , Q Yang , D F Chen , Y Geng , X L Huang , P Ouyang , W M Lai . Molecular cloning, expression and the adjuvant effects of interleukin-8 of channel catfish ( Ictalurus Punctatus ) against Streptococcus iniae . Scientific Reports , 2016 . 6 29 310 DOI: 10.1038/srep29310 http://doi.org/10.1038/srep29310 .

K Wang , J A Lenstra , L Liu , Q J Hu , T Ma , Q Qiu , J Q Liu . Incomplete lineage sorting rather than hybridization explains the inconsistent phylogeny of the wisent . Communications Biology , 2018 . 1 169 DOI: 10.1038/s42003-018-0176-6 http://doi.org/10.1038/s42003-018-0176-6 .

T M Wang , J Liang , X W Xiang , J J Yuan , X Chen , X W Xiang , J W Yang . Functional identification and expressional responses of large yellow croaker ( Larimichthys crocea ) interleukin-8 and its receptor . Fish & Shellfish Immunology , 2019 . 87 470 - 477 . DOI: 10.1016/j.fsi.2019.01.035 http://doi.org/10.1016/j.fsi.2019.01.035 .

X Y Wang , P J Quinn . Lipopolysaccharide: biosynthetic pathway and structure modification . Progress in Lipid Research , 2010 . 49 ( 2 ): 97 - 107 . DOI: 10.1016/j.plipres.2009.06.002 http://doi.org/10.1016/j.plipres.2009.06.002 .

C M Whittington , C R Friesen . The evolution and physiology of male pregnancy in syngnathid fishes . Biological Reviews , 2020 . 95 ( 5 ): 1 252 - 1 272 . DOI: 10.1111/brv.12607 http://doi.org/10.1111/brv.12607 .

C M Whittington , O W Griffith , W H Qi , M B Thompson , A B Wilson . Seahorse brood pouch transcriptome reveals common genes associated with vertebrate pregnancy . Molecular Biology and Evolution , 2015 . 32 ( 12 ): 3 114 - 3 131 . DOI: 10.1093/molbev/msv177 http://doi.org/10.1093/molbev/msv177 .

A B Wilson , A Vincent , I Ahnesjö , A Meyer . Male pregnancy in seahorses and pipefishes (family Syngnathidae): rapid diversification of paternal brood pouch morphology inferred from a molecular phylogeny . Journal of Heredity , 2001 . 92 ( 2 ): 159 - 166 . DOI: 10.1093/jhered/92.2.159 http://doi.org/10.1093/jhered/92.2.159 .

Y Xiao , L Yu , G Gui , Y Gong , X Wen , W Xia , H Yang , L Zhang . Molecular cloning and expression analysis of interleukin-8 and -10 in yellow catfish and in response to bacterial pathogen infection . BioMed Research International , 2019 . 2019 9617659 DOI: 10.1155/2019/9617659 http://doi.org/10.1155/2019/9617659 .

Q Q Xu , P Xu , J W Zhou , T S Pan , R Tuo , K Ai , D Q Yang . Cloning and expression analysis of two proinflammatory cytokines, IL-1β and its receptor, IL-1R2, in the Asian swamp eel Monopterus albus . Molecular Biology , 2016 . 50 ( 5 ): 760 - 774 . DOI: 10.7868/s0026898416030125 http://doi.org/10.7868/s0026898416030125 .

Q Yang , Q Chu , X Y Zhao , T J Xu . Characterization of IL-1β and two types of IL-1 receptors in miiuy croaker and evolution analysis of IL-1 family . Fish & Shellfish Immunology , 2017 . 63 165 - 172 . DOI: 10.1016/j.fsi.2017.02.005 http://doi.org/10.1016/j.fsi.2017.02.005 .

J Zou , C J Secombes . The function of fish cytokines . Biology , 2016 . 5 ( 2 ): 23 DOI: 10.3390/biology5020023 http://doi.org/10.3390/biology5020023 .

J Zou , Y Yoshiura , J M Dijkstra , M Sakai , M Ototake , C Secombes . Identification of an interferon gamma homologue in Fugu, Takifugu rubripes . Fish & Shellfish Immunology , 2004 . 17 ( 4 ): 403 - 409 . DOI: 10.1016/j.fsi.2004.04.015 http://doi.org/10.1016/j.fsi.2004.04.015 .

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⁰

Roles of interleukins in antibacterial immune defense of the brood pouch in the lined seahorse Hippocampus erectus

DOI：10.1007/s00343-021-0310-z

摘要

Abstract

关键词

Keywords

references