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Teleost Fish as an Experimental Model for Vaccine Development

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Vaccine Design

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2411))

Abstract

Advances in vaccine development depend on animal models to test innovative therapies. Recent studies have reported the successful introduction of teleost fish as a new vertebrate model in scientific research, with emphasis on the species Danio rerio (zebrafish). This chapter aims to give an overview of important aspects related to the immune system of fish, as well as the current progress of the successful use of these animals in studies for the development of vaccines, assisting in the determination of efficacy and clinical safety. Among the advantages of using fish for the development of vaccines and immunomodulatory drugs, it is worth highlighting the reproductive capacity of these animals resulting in a high number of individuals belonging to the same spawning, transparent embryos, low cost of breeding and high genetic similarity that favor translational responses to vertebrate organisms like humans.

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References

  1. Rauta PR, Nayak B, Das S (2012) Immune system and immune responses in fish and their role in comparative immunity study: a model for higher organisms. Immunol Lett 148:23–33

    CAS  PubMed  Google Scholar 

  2. Uribe C, Folch H, Enríquez R et al (2011) Innate and adaptive immunity in teleost fish: a review. Vet Med 56:486–503

    CAS  Google Scholar 

  3. Buchmann K (2014) Evolution of innate immunity: clues from invertebrates via fish to mammals. Front Immunol 5:459

    PubMed  PubMed Central  Google Scholar 

  4. Zhu LY, Nie L, Zhu G et al (2013) Advances in research of fish immune-relevant genes: a comparative overview of innate and adaptive immunity in teleosts. Dev Comp Immunol 39:39–62

    CAS  PubMed  Google Scholar 

  5. Charlie-Silva I, Klein A, Gomes JM et al (2019) Acute-phase proteins during inflammatory reaction by bacterial infection: fish-model. Sci Rep 9. https://doi.org/10.1038/s41598-019-41312-z

  6. Belo MAA, Schalch SHC, Moraes FR et al (2005) Effect of dietary supplementation with vitamin E and stocking density on macrophage recruitment and giant cell formation in the teleost fish, Piaractus mesopotamicus. J Comp Pathol 133:146–154

    CAS  PubMed  Google Scholar 

  7. Kondera E (2019) Haematopoiesis and haematopoietic organs in fish. Rocz Nauk Pol Tow Zootech 15:9–16

    Google Scholar 

  8. Mustafa ES, AL-Taee SK (2020) Innate and adaptive immunity in fish: a review. Al-Anbar J Vet Sci 13:1–16

    Google Scholar 

  9. Zapata A, Diez B, Cejalvo T et al (2006) Ontogeny of the immune system of fish. Fish Shellfish Immunol 20:126–136

    CAS  PubMed  Google Scholar 

  10. Xu J, Du L, Wen Z (2012) Myelopoiesis during zebrafish early development. J Genet Genomics 39:435–442

    CAS  PubMed  Google Scholar 

  11. Kernen L, Rieder J, Duus A et al (2020) Thymus development in the zebrafish (Danio rerio) from an ecoimmunology perspective. J Exp Zool A Ecol Integr Physiol 333:805–819

    CAS  PubMed  Google Scholar 

  12. Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625

    CAS  PubMed  Google Scholar 

  13. Fernandes DC, Eto SF, Moraes AC (2019) Phagolysosomal activity of macrophages in Nile tilapia (Oreochromis niloticus) infected in vitro by Aeromonas hydrophila: infection and immunotherapy. Fish Shellfish Immunol 87:51–61

    CAS  PubMed  Google Scholar 

  14. Rodrigues-Soares JP, Jesus GF, Goncalves EL et al (2018) Induced aerocystitis and hemato-immunological parameters in Nile tilapia fed supplemented diet with essential oil of Lippia alba. Braz J Vet Res Anim Sci 55:1–12

    Google Scholar 

  15. Magnadóttir B (2006) Innate immunity of fish (overview). Fish Shellfish Immunol 20:137–151

    PubMed  Google Scholar 

  16. Eto SF, Fernandes DC, Moraes AC et al (2020) Meningitis caused by Streptococcus agalactiae in Nile Tilapia (Oreochromis niloticus): infection and inflammatory response. Animals 10:2166

    PubMed Central  Google Scholar 

  17. Belo MAA, Moraes FR, Yoshida L et al (2014) Deleterious effects of low level of vitamin E and high stocking density on the hematology response of pacus, during chronic inflammatory reaction. Aquaculture 422:124–128

    Google Scholar 

  18. Claudiano GS, Petrillo TR, Manrique WG (2013) Acute aerocystitis in Piaractus mesopotamicus: participation of eicosanoids and pro-inflammatory cytokines. Fish Shellfish Immunol 34:1057–1062

    CAS  Google Scholar 

  19. Castro MP, Claudiano GS, Petrillo TR et al (2014) Acute aerocystitis in Nile tilapia bred in net cages and supplemented with chromium carbochelate and Saccharomyces cerevisiae. Fish Shellfish Immunol 36:284–290

    CAS  PubMed  Google Scholar 

  20. Prado EJR, Belo MAA, Moraes AC et al (2018) Insulin favors acute inflammatory reaction in alloxan-diabetic tilapia during infectious aerocystitis. Pesq Vet Bras 38:2190–2193

    Google Scholar 

  21. Charlie-Silva I, Conde G, Gomes JMM et al (2020) Cyclophosphamide modulated the foreign body inflammatory reaction in tilapia (Oreochromis niloticus). Fish Shellfish Immunol 107:230–237

    CAS  PubMed  Google Scholar 

  22. Manrique WG, Claudiano GS, Castro MP (2015) Expression of cellular components in granulomatous inflammatory response in Piaractus mesopotamicus model. PLoS One 10:e0121625

    PubMed  PubMed Central  Google Scholar 

  23. Manrique WG, Figueiredo MA, Belo MAA et al (2017) Chronic granulomatous inflammation in teleost fish Piaractus mesopotamicus: histopathology model study. Revista MVZ Córdoba 22:5738–5746

    Google Scholar 

  24. Page DM, Wittamer V, Bertrand JY et al (2013) An evolutionarily conserved program of B-cell development and activation in zebrafish. Blood 122:e1–e11

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Danilova N, Steiner LA (2002) B cells develop in the zebrafish pancreas. Proc Natl Acad Sci U S A 99:13711–13716

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Li J, Barreda DR, Zhang YA et al (2006) B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat Immunol 7:1116–1124

    CAS  PubMed  Google Scholar 

  27. Cannon JP, Haire RN, Rast JP et al (2004) The phylogenetic origins of the antigen-binding receptors and somatic diversification mechanisms. Immunol Rev 200:12–22

    CAS  PubMed  Google Scholar 

  28. Danilova N, Bussmann J, Jekosch K et al (2005) The immunoglobulin heavy-chain locus in zebrafish: identification and expression of a previously unknown isotype, immunoglobulin Z. Nat Immunol 6:295–302

    CAS  PubMed  Google Scholar 

  29. Zimmerman AM, Moustafa FM, Romanowski KE et al (2011) Zebrafish immunoglobulin IgD: unusual exon usage and quantitative expression profiles with IgM and IgZ/T heavy chain isotypes. Mol Immunol 48:2220–2223

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Hansen JD, Landis ED, Phillips RB (2005) Discovery of a unique Ig heavy-chain isotype (IgT) in rainbow trout: implications for a distinctive B cell developmental pathway in teleost fish. Proc Natl Acad Sci U S A 102:6919–6924

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Hu YL, Xiang LX, Shao JZ (2010) Identification and characterization of a novel immunoglobulin Z isotype in zebrafish: implications for a distinct B cell receptor in lower vertebrates. Mol Immunol 47:738–746

    CAS  PubMed  Google Scholar 

  32. Ji JF, Hu CB, Shao T et al (2021) Differential immune responses of immunoglobulin Z subclass members in antibacterial immunity in a zebrafish model. Immunology 162:105–120

    CAS  PubMed  Google Scholar 

  33. Wang H, Ji D, Shao J et al (2012) Maternal transfer and protective role of antibodies in zebrafish Danio rerio. Mol Immunol 51:332–336

    CAS  PubMed  Google Scholar 

  34. Van Loon JJA, Van Oosterom R, Van Muiswinkel WB (1981) Development of the immune system in carp (Cyprinus carpio). In: Aspects of developmental and comparative immunology. Pergamon, pp 469–470

    Google Scholar 

  35. Bly JE, Grimm AS, Morris IG (1986) Transfer of passive immunity from mother to young in a teleost fish: haemagglutinating activity in the serum and eggs of plaice, Pleuronectes platessa L. Comp Biochem Physiol A Comp Physiol 84:309–313

    CAS  PubMed  Google Scholar 

  36. Zapata AG, Torroba M, Varas A et al (1997) Immunity in fish larvae. Dev Bio Stand 90:23–32

    CAS  Google Scholar 

  37. Wang Z, Zhang S, Tong Z et al (2009) Maternal transfer and protective role of the alternative complement components in zebrafish Danio rerio. PLoS One 4:e4498

    PubMed  PubMed Central  Google Scholar 

  38. Wang Z, Zhang S (2010) The role of lysozyme and complement in the antibacterial activity of zebrafish (Danio rerio) egg cytosol. Fish Shellfish Immunol 29:773–777

    CAS  PubMed  Google Scholar 

  39. De la Paz JF, Anguita-Salinas C, Díaz-Celis C et al (2020) The zebrafish perivitelline fluid provides maternally-inherited defensive immunity. Biomol Ther 10:1274

    Google Scholar 

  40. Ni S, Zhou Y, Song L et al (2021) ELAVL1a is an immunocompetent protein that protects zebrafish embryos from bacterial infection. Commun Biol 4:1–13

    Google Scholar 

  41. Wang X, Ren Y, Li J et al (2021) Identification of the 14-3-3 β/α-a protein as a novel maternal peptidoglycan-binding protein that protects embryos of zebrafish against bacterial infections. Dev Comp Immunol 114:103867

    CAS  PubMed  Google Scholar 

  42. Parra D, Korytář T, Takizawa F et al (2016) B cells and their role in the teleost gut. Dev Comp Immunol 64:150–166

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Lazado CC, Caipang CMA (2014) Mucosal immunity and probiotics in fish. Fish Shellfish Immunol 39:78–89

    CAS  PubMed  Google Scholar 

  44. Yu Y, Wang Q, Huang Z et al (2020) Immunoglobulins, mucosal immunity and vaccination in teleost fish. Front Immunol 11:2597

    Google Scholar 

  45. Salinas I (2015) The mucosal immune system of teleost fish. Biology 4:525–539

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Xu Z, Takizawa F, Casadei E et al (2020) Specialization of mucosal immunoglobulins in pathogen control and microbiota homeostasis occurred early in vertebrate evolution. Sci Immunol 5:44

    Google Scholar 

  47. Somamoto T, Nakanishi T (2020) Mucosal delivery of fish vaccines: local and systemic immunity following mucosal immunisations. Fish Shellfish Immunol 99:199–207

    CAS  PubMed  Google Scholar 

  48. WHO (2016) Human challenge trials for vaccine development: regulatory considerations. Expert Committee on Biological Standardisation, Geneva. https://www.who.int/biologicals/expert_committee/Human_challenge_Trials_IK_final.pdf. Accessed 17 Apr 2021

    Google Scholar 

  49. Oksanen KE, Halfpenny NJ, Sherwood E et al (2013) An adult zebrafish model for preclinical tuberculosis vaccine development. Vaccine 31:5202–5209

    CAS  PubMed  Google Scholar 

  50. Fernandes BHV, Feitosa NM, Barbosa AP et al (2020) Zebrafish studies on the vaccine candidate to COVID-19, the spike protein: production of antibody and adverse reaction. https://doi.org/10.1101/2020.10.20.346262

  51. Myllymäki H, Niskanen M, Oksanen K et al (2018) Immunization of adult zebrafish for the preclinical screening of DNA-based vaccines. JoVE 140:e58453

    Google Scholar 

  52. López V, Risalde MA, Contreras M et al (2018) Heat-inactivated Mycobacterium bovis protects zebrafish against mycobacteriosis. J Fish Dis 41:1515–1528

    PubMed  Google Scholar 

  53. Pumchan A, Krobthong S, Roytrakul S et al (2020) Novel chimeric multiepitope vaccine for Streptococcosis disease in Nile tilapia (Oreochromis niloticus Linn.). Sci Rep 10:603. https://doi.org/10.1038/s41598-019-57283-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Howlader DR, Sinha R, Nag D et al (2016) Zebrafish as a novel model for non-typhoidal Salmonella pathogenesis, transmission and vaccine efficacy. Vaccine 34:5099–5106

    PubMed  Google Scholar 

  55. Brudal E, Lampe EO, Reubsaet L et al (2015) Vaccination with outer membrane vesicles from Francisella noatunensis reduces development of francisellosis in a zebrafish model. Fish Shellfish Immunol 42:50–57

    CAS  PubMed  Google Scholar 

  56. Flanagan KL, Fink AL, Plebanski M et al (2017) Sex and gender differences in the outcomes of vaccination over the life course. Annu Rev Cell Dev Biol 33:577–599

    CAS  PubMed  Google Scholar 

  57. Oh JZ, Ravindran R, Chassaing B et al (2014) TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination. Immunity 41:478–492

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Charlie-Silva I, Melo NFS, Gomes JM et al (2018) Nanoparticle mucoadhesive system as a new tool for fish immune system modulation. Fish Shellfish Immunol 80:651–654

    CAS  PubMed  Google Scholar 

  59. Kapadia CH, Perry JL, Tian S et al (2015) Nanoparticulate immunotherapy for cancer. J Control Release 219:167–180

    CAS  PubMed  Google Scholar 

  60. Talevi A, Duran N, Castro GR (2021) Lipid nanoparticles as a novel strategy to deliver bioactive molecules. Front Chem 9:69. https://doi.org/10.3389/fchem.2021.655480

    Article  Google Scholar 

  61. Weng Y, Li C, Yang T et al (2020) The challenge and prospect of mRNA therapeutics landscape. Biotechnol Adv 40:107534

    CAS  PubMed  Google Scholar 

  62. Ji J, Torrealba D, Ruyra À et al (2015) Nanodelivery systems as new tools for immunostimulant or vaccine administration: targeting the fish immune system. Biology 4:664–696

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Kavaliauskis A, Arnemo M, Speth M et al (2016) Protective effect of a recombinant VHSV-G vaccine using poly (I: C) loaded nanoparticles as an adjuvant in zebrafish (Danio rerio) infection model. Dev Comp Immunol 61:248–257

    CAS  PubMed  Google Scholar 

  64. Charlie-Silva I, Feitosa NM, Gomes JMM et al (2020) Potential of mucoadhesive nanocapsules in drug release and toxicology in zebrafish. PLoS One 15:e0238823

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Charlie-Silva I, Melo NFS, Gomes JM et al (2019) Novel nanostructure obtained from pacamã, Lophiosilurus alexandri, skin mucus presents potential as a bioactive carrier in fish. Aquaculture 512:734294

    Google Scholar 

  66. Charlie-Silva I, Fraceto LF, Melo NFS (2018) Progress in nano-drug delivery of artemisinin and its derivatives: towards to use in immunomodulatory approaches. Art Cells Nanomed Biotechnol 46:S611–S620

    CAS  Google Scholar 

  67. Ferreira AL, Charlie-Silva I, Favero GC et al (2020) Chitosan-coated zein nanoparticles containing eugenol potentiates anesthesia in Nile tilapia. Aquaculture 529:735659

    CAS  Google Scholar 

  68. Cavalcante CH, Fernandes RS, Oliveira Silva J et al (2021) Doxorubicin-loaded pH-sensitive micelles: a promising alternative to enhance antitumor activity and reduce toxicity. Biomed Pharmacother 134:111076

    CAS  PubMed  Google Scholar 

  69. Guimarães ATB, Charlie-Silva I, Malafaia G (2021) Toxic effects of naturally-aged microplastics on zebrafish juveniles: a more realistic approach to plastic pollution in freshwater ecosystems. J Hazard Mater 407:124833

    PubMed  Google Scholar 

  70. Chagas TQ, Freitas ÍN, Montalvão MF et al (2021) Multiple ENDPOINTS of polylactic acid biomicroplastic toxicity in adult zebrafish (Danio rerio). Chemosphere 130279

    Google Scholar 

  71. Charlie-Silva I, Feitosa NM, Fukushima HCS et al (2021) Effects of nanocapsules of poly-ε-caprolactone containing artemisinin on zebrafish early-life stages and adults. Sci Tot Environ 756:143851

    CAS  Google Scholar 

  72. Crecente-Campo J, Guerra-Varela J, Peleteiro M et al (2019) The size and composition of polymeric nanocapsules dictate their interaction with macrophages and biodistribution in zebrafish. J Control Release 308:98–108

    CAS  PubMed  Google Scholar 

  73. Løvmo SD, Speth MT, Repnik U et al (2017) Translocation of nanoparticles and Mycobacterium marinum across the intestinal epithelium in zebrafish and the role of the mucosal immune system. Dev Comp Immunol 67:508–518

    PubMed  Google Scholar 

  74. McAroe CL, Craig CM, Holland RA (2017) Shoaling promotes place over response learning but does not facilitate individual learning of that strategy in zebrafish (Danio rerio). BMC Zool. https://doi.org/10.1186/s40850-017-0019-9

  75. Berghmans S, Jette C, Langenau D et al (2005) Making waves in cancer research: new models in the zebrafish. BioTechniques 39:227–237

    CAS  PubMed  Google Scholar 

  76. Hoo JY, Kumari Y, Shaikh MF et al (2016) Zebrafish: a versatile animal model for fertility research. Biomed Res Int 2016:9732780. https://doi.org/10.1155/2016/9732780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Fishman MC, Stainier DY, Breitbart RE et al (1997) Zebrafish: genetic and embryological methods in a transparent vertebrate embryo. Methods Cell Biol 52:67–82

    CAS  PubMed  Google Scholar 

  78. Howe K, Clark MD, Torroja CF et al (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496(7446):498–503

    CAS  PubMed  PubMed Central  Google Scholar 

  79. MacRae CA, Peterson RT (2015) Zebrafish as tools for drug discovery. Nat Rev Drug Disc 14:721–731

    CAS  Google Scholar 

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de Andrade Belo, M.A., Charlie-Silva, I. (2022). Teleost Fish as an Experimental Model for Vaccine Development. In: Thomas, S. (eds) Vaccine Design. Methods in Molecular Biology, vol 2411. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-1888-2_10

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  • DOI: https://doi.org/10.1007/978-1-0716-1888-2_10

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