Skip to main content

Advertisement

SpringerLink
Log in

The immunoadjuvant effects of interleukin-8 on Aeromonas veronii inactivated vaccine in largemouth bass (Micropterus salmoides)

  • Research
  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

Largemouth bass (Micropterus salmoides) is an economically important fish, yet it is plagued by frequent diseases caused by Aeromonas veronii infection in its aquaculture. Vaccination is a pivotal strategy in the prevention and management of infectious diseases, and adjuvants play a crucial role in augmenting the effectiveness of vaccines. Interleukin-8 (IL-8), one of the CXC chemokines, has been identified as having adjuvant potential in various species, although its efficacy in largemouth bass remains uncertain. In the present study, recombinant largemouth bass IL-8 (rLbIL-8) was prepared to explore its adjuvant potential in the A. veronii inactivated vaccine. Challenge experiment results revealed that the relative percent survival (RPS) of largemouth bass in the inactivated A. veronii + rLbIL-8 vaccinated group was calculated to be 70% following challenges with live A. veronii, higher than that of the inactivated A. veronii vaccinated group (56.67%). Furthermore, co-inoculation of rLbIL-8 and inactivated A. veronii markedly elevated serum SOD levels and lysozyme activities in largemouth bass. Indirect ELISA analysis found that rLbIL-8 enhanced the inactivated A. veronii vaccine’s ability to induce serum-specific antibodies against A. veronii. qRT-PCR analysis showed that rLbIL-8 enhanced the upregulation of IL-1β, TNF-α, CD4, MHC II, and IgM expression induced by inactivated A. veronii, with peak expression occurring on days 1 and 5 post-vaccination, respectively. Collectively, these findings attest to the potential of rLbIL-8 as a vaccine adjuvant for largemouth bass, advancing the progress and implementation of vaccines in aquaculture.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

Data will be made available from the corresponding author upon reasonable request.

References

  • Bekele Y, Sui YJ, Berzofsky JA (2021) IL-7 in SARS-CoV-2 infection and as a potential vaccine adjuvant. Front Immunol 12:737406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao YS, Zhang QY, Xu LM et al (2017) Effects of different cytokines on immune responses of rainbow trout in a virus DNA vaccination model. Oncotarget 8:112222–112235

    Article  PubMed  PubMed Central  Google Scholar 

  • Che MX, Lu ZY, Liu L et al (2023) Dietary lysophospholipids improves growth performance and hepatic lipid metabolism of largemouth bass (Micropterus salmoides). Anim Nutr 13:426–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chi YY, Jiao HY, Ran JY et al (2023) Construction and efficacy of Aeromonas veronii mutant Ahcp as a live attenuated vaccine for the largemouth bass (Micropterus salmoides). Fish Shellfish Immunol 136:108694

    Article  CAS  PubMed  Google Scholar 

  • de Oliveira S, Reyes-Aldasoro CC, Candel S et al (2013) Cxcl8 (IL-8) mediates neutrophil recruitment and behavior in the Zebrafish inflammatory response. J Immunol 190:4349–4359

    Article  PubMed  Google Scholar 

  • de Souza-Silva GA, Sulczewski FB, Boscardin SB (2023) Recombinant antigen delivery to dendritic cells as a way to improve vaccine design. Exp Biol Med 248:1616–1623

    Article  Google Scholar 

  • Dong Y, Yang Y, Liu J et al (2018) Inhibition of Aeromonas hydrophila-induced intestinal inflammation and mucosal barrier function damage in crucian carp by oral administration of Lactococcus lactis. Fish Shellfish Immunol 83:359–367

    Article  CAS  PubMed  Google Scholar 

  • Easterhoff D, Pollara J, Luo K et al (2020) Boosting with AIDSVAX B/E enhances env constant region 1 and 2 antibody-dependent cellular cytotoxicity breadth and potency. J Virol 94:e01120-e1219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fei H, Cheng Y, Zhang HM et al (2022) Effect of autolyzed Yarrowia lipolytica on the growth performance, antioxidant capacity, intestinal histology, microbiota, and transcriptome profile of juvenile largemouth bass (Micropterus salmoides). Int J Mol Sci 23:10780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo M, Li CH (2021) An overview of cytokine used as adjuvants in fish: current state and future trends. Rev Aquacult 13:996–1014

    Article  Google Scholar 

  • Guo M, Tang XQ, Sheng XZ et al (2018a) Comparative study of the adjuvant potential of four Th0 cytokines of flounder (Paralichthys olivaceus) on an E-tarda subunit vaccine. Dev Comp Immunol 86:147–155

    Article  CAS  PubMed  Google Scholar 

  • Guo M, Tang XQ, Sheng XZ et al (2018b) The effects of IL-1β, IL-8, G-CSF and TNF-α as molecular adjuvant on the immune response to an E. tarda subunit vaccine in flounder (Paralichthys olivaceus). Fish Shellfish Immunol 77:374–384

    Article  CAS  PubMed  Google Scholar 

  • Hoai TD, Trang TT, Tuyen NV et al (2019) Aeromonas veronii caused disease and mortality in channel catfish in Vietnam. Aquaculture 513:734425

    Article  CAS  Google Scholar 

  • Hoseinifar SH, Shakouri M, Van Doan H et al (2020) Dietary supplementation of lemon verbena (Aloysia citrodora) improved immunity, immune-related genes expression and antioxidant enzymes in rainbow trout (Oncorrhyncus mykiss). Fish Shellfish Immunol 99:379–385

    Article  CAS  PubMed  Google Scholar 

  • Irshath AA, Rajan AP, Vimal S et al (2023) Bacterial pathogenesis in various fish diseases: recent advances and specific challenges in vaccine development. Vaccines 11:470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaiser R, Leunig A, Pekayvaz K et al (2021) Self-sustaining IL-8 loops drive a prothrombotic neutrophil phenotype in severe COVID-19. JCI Insight 6:e150862

    Article  PubMed  PubMed Central  Google Scholar 

  • Karatas S, Turgay E, Yardimci RE et al (2023) Aeromonas veronii biovar veronii infection in cultured European seabass (Dicentrarchus labrax) in Turkiye. Ksu Tarim Doga Derg 26:1397–1404

    Google Scholar 

  • Kim JJ, Yang J, Dentchev T et al (2000) Chemokine gene adjuvants can modulate immune responses induced by DNA vaccines. J Interferon Cytokine Res 20:487–498

    Article  CAS  PubMed  Google Scholar 

  • Kobari S, Kusakabe T, Momota M et al (2020) IL-33 is essential for adjuvant effect of hydroxypropyl-β-cyclodexrin on the protective intranasal influenza vaccination. Front Immunol 11:360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong YD, Kang YH, Tian JX et al (2019) Oral immunization with recombinant Lactobacillus casei expressing flaB confers protection against Aeromonas veronii challenge in common carp, Cyprinus carpio. Fish Shellfish Immunol 87:627–637

    Article  CAS  PubMed  Google Scholar 

  • Krzystek-Korpacka M, Mierzchala-Pasierb M, Zawadzki M et al (2021) Serum and erythrocyte antioxidant defense in colorectal cancer patients during early postoperative period: potential modifiers and impact on clinical outcomes. Antioxidants 10:999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee M, Young D, Mine Y et al (2009) Reduction of interlukin-8 by peptides from digestive enzyme hydrolysis of hen egg lysozyme. Food Sci Biotechnol 18:706–711

    CAS  Google Scholar 

  • Liang XM, Wang F, Li KB et al (2020) Effects of norfloxacin nicotinate on the early life stage of zebrafish (Danio rerio): developmental toxicity, oxidative stress and immunotoxicity. Fish Shell Immunol 96:262–269

    Article  CAS  Google Scholar 

  • Lin YH, Sun BN, Jin Z et al (2023) Enhanced immune responses to mucosa by functionalized chitosan-based composite nanoparticles as a vaccine adjuvant for intranasal delivery. ACS Appl Mater Interfaces 14:52691–52701

    Article  Google Scholar 

  • Ling ZR, Yin WJ, Li H et al (2017) Chromosome-mediated mcr-3 variants in Aeromonas veronii from chicken meat. Antimicrob Agents Ch 61:e01272-e1317

    Article  CAS  Google Scholar 

  • Liu F, Yuwono C, Tay ACY et al (2022) Analysis of global Aeromonas veronii genomes provides novel information on source of infection and virulence in human gastrointestinal diseases. BMC Genomics 23:166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Min W, Lillehoj HS, Burnside J et al (2001) Adjuvant effects of IL-1β, IL-2, IL-8, IL-15, IFN-α, IFN-γ, TGF-β4 and lymphotactin on DNA vaccination against Eimeria acervulina. Vaccine 20:267–274

    Article  CAS  PubMed  Google Scholar 

  • Nie MF, Wu SY, Chen YY et al (2023) Micronanoparticled risedronate exhibits potent vaccine adjuvant effects. J Control Release 365:369–383

    Article  PubMed  Google Scholar 

  • Patel B, Kumar P, Banerjee R et al (2016) Lactobacillus acidophilus attenuates Aeromonas hydrophila induced cytotoxicity in catla thymus macrophages by modulating oxidative stress and inflammation. Mol Immunol 75:69–83

    Article  CAS  PubMed  Google Scholar 

  • Pei C, Song HL, Zhu L et al (2021) Identification of Aeromonas veronii isolated from largemouth bass Micropterus salmoides and histopathological analysis. Aquaculture 540:736707

    Article  CAS  Google Scholar 

  • Raj NS, Swaminathan TR, Dharmaratnam A et al (2019) Aeromonas veronii caused bilateral exophthalmia and mass mortality in cultured Nile tilapia, Oreochromis niloticus (L.) in India. Aquaculture 512:734278

    Article  Google Scholar 

  • Song MF, Kang YH, Zhang DX et al (2018) Immunogenicity of extracellular products from an inactivated vaccine against Aeromonas veronii TH0426 in koi, Cyprinus carpio. Fish Shellfish Immunol 81:176–181

    Article  CAS  PubMed  Google Scholar 

  • Wang EL, Long B, Wang KY et al (2016a) Interleukin-8 holds promise to serve as a molecular adjuvant in DNA vaccination model against Streptococcus iniae infection in fish. Oncotarget 7:83938–83950

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang EL, Wang J, Long B et al (2016b) Molecular cloning, expression and the adjuvant effects of interleukin-8 of channel catfish (Ictalurus Punctatus) against Streptococcus iniae. Sci Rep 6:29310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang YD, Gong JS, Guan YC et al (2023) Hcp1 regulates flagella of Aeromonas veronii TH0426 to reduce virulence. Aquaculture 576:739899

    Article  CAS  Google Scholar 

  • Wu RH, Chi YY, Yu JQ et al (2021) Enhanced immersion vaccination through hyperosmotic treatment in the largemouth bass (Micropterus salmoides). Aquaculture 535:736371

    Article  CAS  Google Scholar 

  • Xiong XY, Peng YH, Chen RF et al (2023) Efficacy and transcriptome analysis of golden pompano (Trachinotus ovatus) immunized with a formalin-inactived vaccine against Streptococcus iniae. Fish Shellfish Immunol 134:108489

    Article  CAS  PubMed  Google Scholar 

  • Yan YM, Hu Y, Wang XR et al (2021) The predictive prognostic values of serum interleukin-2, interleukin-6, interleukin-8, tumor necrosis factor-α, and procalcitonin in surgical intensive care unit patients. Ann Transl Med 9:56

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang S, Chen WQ, He FF et al (2020) Comparison of the roles of IgM in systemic and mucosal immunity via tissue distribution analysis in largemouth bass (Micropterus salmoides). Aquaculture 527:735488

    Article  CAS  Google Scholar 

  • Yang S, Mkingule I, Liu L et al (2022) Protective efficacy evaluation of immunogenic protein AHA_3793 of Aeromonas hydrophila as vaccine candidate for largemouth bass Micropterus salmoides. J Oceanol Limnol 41:392–400

    Article  PubMed  PubMed Central  Google Scholar 

  • Yao JT, Hang Y, Hua XM et al (2022) Hepatopancreas-intestinal health in grass carp (Ctenopharyngodon idella) fed with hydrolyzable tannin or rapeseed meal. Aquacult Nutr 2022:6746201

    Article  Google Scholar 

  • Youssef HA, Ayoub HF, Soror EI et al (2022) Virulence genes contributing to Aeromonas veronii pathogenicity in Nile tilapia (Oreochromis niloticus): approaching the development of live and inactivated vaccines. Aquacult Int 31:1253–1267

    Article  Google Scholar 

  • Yuan XY, Zhang XT, Xia YT et al (2021) Transcriptome and 16S rRNA analyses revealed differences in the responses of largemouth bass (Micropterus salmoides) to early Aeromonas hydrophila infection and immunization. Aquaculture 541:736759

    Article  CAS  Google Scholar 

  • Zhang AP, Xiong YL, Xu FH et al (2020a) IL-1B enhances human placenta-derived mesenchymal stromal cells ability to mediate Th1/Th2 and Th1/CD4+IL-10+ T cell balance and regulates its adhesion, proliferation and migration via PD-L1. Cell Immunol 352:104113

    Article  CAS  PubMed  Google Scholar 

  • Zhang HP, Chen MY, Xu YX et al (2020b) An effective live attenuated vaccine against Aeromonas veronii infection in the loach (Misgumus anguillicaudatus). Fish Shellfish Immunol 104:269–278

    Article  CAS  PubMed  Google Scholar 

  • Zhao MH, Liu YZ, Gao YJ et al (2021) Insights into the functional role of grass carp IL-8 in head kidney leukocytes: pro-inflammatory effects and signalling mechanisms. J Fish Biol 100:192–202

    Article  PubMed  Google Scholar 

  • Zhu XH, Qian QQ, Wu CC et al (2022) Pathogenicity of Aeromonas veronii causing mass mortality of largemouth bass (Micropterus salmoides) and its induced host immune response. Microorganisms 10:2198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study was supported by the National Natural Science Foundation of China (No. 32102824).

Author information

Author notes

  1. Shun Yang and Qian-Rong Liang contributed equally to this study.

Authors and Affiliations

  1. College of Animal Science and Technology, Northeast Agricultural University, Harbin, 150030, People’s Republic of China

    Shun Yang & Yu-Hong Yang

  2. College of Life Sciences and Medicine, Zhejiang Sci-Tech University, Hangzhou, 310018, China

    Shun Yang, Ze-Sheng Zhang & Hui Fei

  3. Zhejiang Fisheries Test and Aquatic Disease Prevention Center, Zhejiang Fisheries Technical Extension Center, Hangzhou, 310023, China

    Qian-Rong Liang

  4. Zhejiang Huadi Pharmaceutical Group Co., Ltd, Hangzhou, 313300, China

    Xiao-Fei Yao

  5. Huanggang Modern Agriculture Exhibition and Information Center, Huanggang, 438021, China

    Dao-Le Liu

Authors
  1. Shun Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qian-Rong Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dao-Le Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ze-Sheng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yu-Hong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiao-Fei Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hui Fei
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study’s conception and design. Material preparation, data collection, and analysis were performed by Shun Yang, Qian-Rong Liang, and Ze-Sheng Zhang. Shun Yang, Yu-Hong Yang, and Hui Fei contributed reagents/materials/analysis tools. Conceptualization, formal analysis, methodology, project administration, resources, supervision, visualization, and writing—original draft and editing by Shun Yang, Qian-Rong Liang, Dao-Le Liu, and Xiao-Fei Yao. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Yu-Hong Yang, Xiao-Fei Yao or Hui Fei.

Ethics declarations

Ethics approval

The animal experiments in the present study were in strict accordance with the relevant provisions of the welfare ethics and protection of experimental animals in the state and Zhejiang Province. The animal-related experiments were approved and supervised by the Committee of Ethics on Animal Care and Experiments at the Zhejiang Sci-Tech University.

Competing interests

The authors declare no competing interests.

Additional information

Handling Editor: Brian Austin

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, S., Liang, QR., Liu, DL. et al. The immunoadjuvant effects of interleukin-8 on Aeromonas veronii inactivated vaccine in largemouth bass (Micropterus salmoides). Aquacult Int (2024). https://doi.org/10.1007/s10499-024-01453-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10499-024-01453-z

Keywords

Search

Navigation