The interferon system of non-mammalian vertebrates
Introduction
Although interferon (IFN) was discovered in 1957 during experimental work with embryonated chicken eggs [1], the molecular analysis of IFNs from avian and other non-mammalian vertebrate species began only in 1994 [2] after most types of mammalian IFNs had already been characterized in great detail. Isolation of non-mammalian IFN genes proved very difficult mainly because the homology to their mammalian counterparts is low, thus severely aggravating the design of primer pairs suitable for RT-PCR. Interest in IFNs of birds and fish has recently sparked from increasing problems with viral diseases in the poultry industry and in aquaculture farming. In this review we will focus on recent progress towards a more detailed understanding of the biology of the avian and fish IFN systems.
Section snippets
IFNs of mammals: a brief overview
IFNs constitute a large group of cytokines that are best known for their ability to induce cellular resistance to viral pathogens [3], [4], [5]. They also play a critical role in the response to microbial infections by modulating the innate and adaptive immune system [6]. Furthermore, they are potent regulators of cell growth and can have inflammatory as well as anti-inflammatory effects [7], [8]. Two major types of IFN are known. IFN-γ, also called type II or immune IFN, is encoded by a single
IFNs of birds
Avian cytokine research started nearly half a century ago with the discovery of a virus-induced factor in embryonated eggs that interfered with influenza virus replication in chorioallantoic membranes of chicken embryos, hence the name IFN [1]. Early work in chickens focused on the purification of virus-induced IFN from embryonated eggs and chicken embryo cells [28], [29], [30]. It was described as a glycosylated polypeptide of 20–30 kDa with antiviral activity that was resistant to acid and
IFNs of fish
It has been known for many years that trout (Salmo gairdneri) can produce an IFN-like activity following virus challenge [56]. More recently, it has been demonstrated that leukocytes from the anterior kidney of trout are able to produce an antiviral response when stimulated with either poly I:C or infectious hematopoietic necrosis virus [57]. Leukocytes from rainbow trout stimulated with mitogen secreted a MAF activity into the supernatant that rendered a trout epithelial cell line resistant to
Interferon-like activities in reptiles and amphibians
An IFN-like activity in reptiles was demonstrated in primary turtle kidney cells (Testudo graeca). This factor, which was produced in response to virus infection, rendered normal turtle cells resistant to virus challenge [76]. It had a molecular weight of about 33 kDa, was acid-stable and heat-resistant. When peritoneal leukocytes from turtles were stimulated with Newcastle disease virus, poly I:C and endotoxin, antiviral mediators of higher molecular weight were secreted [76]. Antiviral
Conclusions and perspectives
From the available data summarized above, a picture emerges which shows that IFN is used by most, if not all, vertebrates. Over the last decade, IFN of birds was characterized at the molecular level and its biological activity was documented. At present, the potential beneficial effect of IFN is being evaluated in the poultry industry. Administration of IFN to birds might improve the efficacy of vaccines and enhance microbial resistance. Since a first gene for ZfIFN has recently been cloned,
Acknowledgements
This work was supported by a grant from the Deutsche Forschungsgemeinschaft (Schu1152/1-1).
References (78)
- et al.
The virus battles: IFN induction of the antiviral state and mechanisms of viral evasion
Cytokine Growth Factor Rev
(2001) - et al.
The interferon-alpha/beta system in antiviral responses: a multimodal machinery of gene regulation by the IRF family of transcription factors
Curr Opin Immunol
(2002) New insights into the mechanisms of interferon alfa: an immunoregulatory and anti-inflammatory cytokine
Gastroenterology
(1997)- et al.
Structural relationship of human interferon alpha genes and pseudogenes
J Mol Biol
(1985) - et al.
Bovine interferon alpha genes. Structure and expression
J Biol Chem
(1985) - et al.
A comparison of vertebrate interferon gene families detected by hybridization with human interferon DNA
J Mol Biol
(1983) - et al.
A novel and atypical type one interferon gene expressed by trophoblast during early pregnancy
J Biol Chem
(1993) - et al.
Induction of high titer chicken interferon
Methods Enzymol
(1986) - et al.
Chicken macrophage activation by interferon: do birds lack the molecular homologue of mammalian interferon-gamma?
Vet Immunol Immunopathol
(1990) - et al.
A family of genes coding for two serologically distinct chicken interferons
J Biol Chem
(1996)
The chicken Mx promoter contains an ISRE motif and confers interferon inducibility to a reporter gene in chick and monkey cells
Virology
Promoter structures and differential responses to viral and nonviral inducers of chicken type I interferon genes
J Biol Chem
Recombinant duck interferon: a new reagent for studying the mode of interferon action against hepatitis B virus
Virology
Structural and functional homology between duck and chicken interferon-gamma
Dev Comp Immunol
Structure of the chicken interferon-gamma gene, and comparison to mammalian homologues
Gene
Turkey and chicken interferon-gamma, which share high sequence identity, are biologically cross-reactive
Dev Comp Immunol
Production of lymphokine (macrophage activating factor) by salmon (Salmo salar) leucocytes stimulated with outer membrane protein antigens of Aeromonas salmonicida
Fish Shellfish Immunol
Cytokine-mediated antimicrobial immune response of catfish, Clarias gariepinus, as a defence against Aeromonas hydrophila
Fish Shellfish Immunol
Functional characterization of macrophage-activating factor produced by leucocytes of gilthead seabream (Sparus aurata L.)
Fish Shellfish Immunol
Requirements for nitric oxide production by turbot (Scophthalmus maximus) head kidney macrophages
Dev Comp Immunol
Viral haemorrhagic septicaemia virus induces vig-2, a new interferon-responsive gene in rainbow trout
Fish Shellfish Immunol
Cloning and expression analysis of rainbow trout Oncorhynchus mykiss interferon regulatory factor 1 and 2 (IRF-1 and IRF-2)
Dev Comp Immunol
Molecular cloning of the fish interferon stimulated gene, 15 kDa (ISG15) orthologue: a ubiquitin-like gene induced by nephrotoxic damage
Gene
Cloning and expression of flatfish (Paralichthys olivaceus) interferon cDNA
Biochim Biophys Acta
Evolution of effectors and receptors of innate immunity
Dev Comp Immunol
Induction and characterization of tortoise interferon
Methods Enzymol
An interferon regulatory factor-related gene (xIRF-6) is expressed in the posterior mesoderm during the early development of Xenopus laevis
Gene
Virus interference. I. The Interferon
Proc R Soc Lond
Chicken interferon gene: cloning, expression, and analysis
J Interferon Res
Antiviral actions of interferons
Clin Microbiol Rev
Interferons and other cytokines
How does interferon exert its cell growth inhibitory effect?
Eur J Haematol
Synergistic effects of IL-4 and IL-18 on IL-12-dependent IFN-gamma production by dendritic cells
J Immunol
Interleukin 12-dependent interferon gamma production by CD8alpha+ lymphoid dendritic cells
J Exp Med
IL-12 up-regulates IL-18 receptor expression on T cells, Th1 cells, and B cells: synergism with IL-18 for IFN-gamma production
J Immunol
Novel interferons
Nat Immunol
Structure and expression of cloned murine IFN-alpha genes
Nucleic Acids Res
Interferons and other cytokines
A novel class of human type I interferons
Nucleic Acids Res
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