Cytokines in Carp in Response to Important Diseases

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1		Ali Asghar Baloch	+ 3432 word(s)	3432	2021-12-30 04:38:13

This entry is adapted from the peer-reviewed paper 10.3390/fishes7010003

Cytokines belong to the most widely studied group of intracellular molecules involved in the function of the immune system. Their secretion is induced by various infectious stimuli. Cytokine release by host cells has been extensively used as a powerful tool for studying immune reactions in the early stages of viral and bacterial infections. Recently, research attention has shifted to the investigation of cytokine responses using mRNA expression, an essential mechanism related to pathogenic and nonpathogenic-immune stimulants in fish.

common carp immune response koi herpesvirus (CyHV-3) carp edema virus (CEV) Aeromonas hydrophila

1. Cytokine Studied in Response to Cyprinid Herpesvirus 3 Infection

Cyprinid herpesvirus 3 (CyHV-3), also known as koi herpes virus (KHV), is the causative agent of koi herpesvirus disease (KHVD). This DNA virus belongs to the family Alloherpesviridae ^[1]. The disease affects both common carp (C. carpio) and its ornamental variety, koi (Cyprinus rubrofuscus). External clinical signs include lethargy and anorexia followed by excessive mucous production on the gills and skin and necrosis of gill tissue. Petechial bleeding spots can also be seen in the final stages of infection on the trunk, vent, and around the mouth ^[2]^[3]. KHV is categorized as an emerging disease that causes massive mortality resulting in substantial economic losses to the aquaculture industry (FAO, 2010).

The coevolution of fish herpesviruses and their hosts is believed to have occurred about 400 to 450 million years ago ^[4]^[5]. Over time, hosts have adapted a more developed and divergent immune system to safeguard themselves in the face of viral or other pathogenic infections. In different vertebrates, including humans, it has been proven that the non-specific immune reaction against herpesviruses generally incorporates an activation of (NK) cells and the production of interferons and different types of interleukins ^[6].

Interferon (IFN) plays a crucial role in innate immunity to guard the body against viral invasion. This cytokine significantly contributes to the early containment of herpesvirus infections because of its immunoreactive properties. Several type 1 IFN reactions, including interferon regulatory genes (ISGs), are characterized during viral infections ^[7]^[8]. Multiple studies have also shown that recombinant interferon or the stimulation of type I IFN production has a protective effect against numerous fish viruses, whether performed in vitro or in vivo. The magnitude of type I IFN responses are essential for increased resistance to virus-induced mortality in fish infected with viruses with more complex genomes, like alloherpesviruses. However, in the case of CyHV-3 infection, skin is considered a major entry organ and the primary site for infection in carp ^[9]^[10]. Fish skin serves as a good protection barrier from different types of pathogens ^[11]. Few studies have been carried out to gain insight into the type I IFN response during CyHV-3 infection exclusively. For instance, a relationship between the upregulation of type 1 IFN response and CyHV-3 infection was observed in the skin of infected common carp ^[7]. However, the localized intervention of IFN-1 on the skin interprets the absence of interferon type 1 response during in-vitro testing on C. carpio brain (CCB) cells infected with CyHV-3 ^[12]. Moreover, lack of type 1 interferon response on other sites could be extrapolated as antiviral capabilities adopted by koi herpesvirus against IFN-1.

During infection with herpesviruses, activation of adaptive immune response occurs in the later stages. The response is carried out by stimulation of the natural killer T cells and B lymphocytes to induce interleukins, in addition to TNF-β and IFN-γ, to initiate and prolong the responses by enhancing the production of antibodies ^[13]. However, the role of these specific cytokines is not fully elucidated in CyHV-3 infection. Rather, infected carp produce specific immunoglobulins (Ig) and mount cell-mediated immune responses ^[14]. Fish that survive a CyHV-3 infection acquire resistance, leading to a remarkable reduction in mortality ^[15]^[16]. Despite that, the capacity to build up a long-lasting latent infection is the hallmark of all known herpesviruses, including fish herpesviruses. Those latent infections are either controlled through the virus mimicking host immunoreactions or by encoding their own antiviral-like proteins such as IL-10 ^[17]^[18]^[19].

In order to replicate more effectively, several viruses encode their own viral IL-10 homolog (vIL-10), which exert an immunosuppressive effect in the host at the beginning of the infection ^[17]^[18]. CyHV-3 vIL-10 was initially described in common carp and the European eel ^[19]. Later on, Sunarto et al. ^[20] also reported that CyHV-3 captures an IL-10 gene from the host and modulates its features to tackle the host immune response. However, an in-vitro study conducted by Ouyang et al. ^[21] demonstrated that CyHV-3 ORF134 (the gene encoding an IL-10 homolog) was neither essential for viral replication nor virulence in common carp.

Nevertheless, CyHV-3 appears to manipulate host antiviral mechanisms more prominently via interaction with the TNF-α pathway. A study conducted by Rakus et al. ^[22] revealed a significant connection between CyHV-3 infection and the development of inflammatory responses controlled by TNF-α. Based on the findings of the study, infected carp demonstrated a delay in fever manifestation, which is an essential infection phase that promotes viral replication. This modulation in disease development was associated with viral CyHV-3 ORF12 encoding the TNF-α soluble decoy receptor, which is known to block cytokine activity ^[22].

The research of gene expression in carp has yielded an insightful perception of the CyHV-3 pathogenesis associated with cytokine secretion. Specific groups of cytokines including IFNγ-1, IFNγ-2, IL-12, IL-10, IL-1β, TNF-α1, and genes of major histocompatibility complex (MHC-II), are found to be over- or under-expressed, respectively, to the ongoing infection stage ^[23]. For instance, fish tested during acute phases of infection show a higher expression rate in all interleukin and interferon genes, while class II MHC and TNF-α1 genes are downregulated ^[23]. Furthermore, a survey conducted by Rakus et al. ^[24] on two carp lines (R3 and K) following CyHV-3 infection has revealed a disparity in the kinetics of cytokine genes expression on different days post-infection. The R3 line exhibited significant upregulation of IL-1β, IL-10, IL-12, and MHC class I genes and more disease resistance compared to the K line, whereas no significant differences in IFN expression were detected in both lines during the infection. It can be speculated that differential expression of those cytokine genes in carp lines could be due to host-related genetic factors incorporating the progress of the infection phase and shifting to adaptive immunity.

The use of cytokine or cytokine inducing cells (i.e., macrophages, B cells, and dendritic cells) as an adjuvant to improve the immunogenicity of DNA vaccines in fish is another growing research interest ^[25]^[26]. A potential protective effect of IL-β in combination with the CyHV-3 ORF25 DNA vaccine has been observed in common carp ^[27]. Likewise, the mammalian granulocyte–macrophage colony-stimulating factor, which in mammals is described as a regulator cytokine of immune cells proliferation, differentiation, and maturation ^[28], has also improved the immunogenicity of DNA and subunit vaccines in fish ^[29]. Moreover, the effect of the CyHV-3 ORF25 DNA vaccine on IL-β, cxca, cxcb1 chemokines, and interferon-stimulated genes (Mx1, vip2, pkr3, and isg15) have been examined in muscles of common carp by Embregts et al. ^[30]. In their study, they used ORF25-based DNA vaccine in different vaccination routes, i.e., intramuscular injection (i.m.) or oral gavage, in one or multiple doses. A strong immunostimulant effect was observed through the repeated i.m. injection, which resulted in cytokine expression and interferon-stimulated genes.

2. Cytokine Studied in Response to Spring Viremia of Carp Infections

Spring viremia of carp (SVC) is a highly contagious viral disease affecting carp (C. carpio) and other cyprinid species. The disease is caused by the Carp sprivivirus (originally SVC virus), a single-stranded RNA virus belonging to the family Rhabdovividae ^[31]^[32]. The condition is associated with edematous symptoms such as exophthalmia, edema of the underlying tissues, and abdominal distention ^[31]. Gross signs include petechial hemorrhages on the eyes, skin, gills, and internal organs, specifically on the swim bladder ^[33].

The SVCV genome encodes five different viral proteins, including matrix protein (M), nucleoprotein (N), glycoprotein (G), phosphoprotein (P), and viral RNA-dependent polymerase, important for viral transcription and replication, endocytosis, and infectivity ^[34]. The accessibility of the entire genomic information of SVCV, and its homology to mammalian rhabdoviruses, has allowed us to understand the function of these proteins more accurately ^[31]^[35].

Rhabdovirus infections, in fish, are controlled through the responses of group I and II IFNs. The recombinant IFNs group I appears to inhibit virus replication at any of the replicative stages ^[36]^[37]^[38]^[39]. The mechanism of rhabdovirus containment by group II IFNs varies intrinsically ^[39]. Recombinant IFNs-II was found to induce a protective effect against SVCV infection in zebrafish through upregulation of interferon regulatory genes such as myxovirus resistance protein (Mx) and viperin. On the contrary, group 1 IFNs upregulate both ISGs and pro-inflammatory cytokines (IL-10β and TNF-α) more persistently ^[40]. Conclusions from in-vitro and in-vivo research in carp indicate alternative responses of IFNs-I during SVCV and CyHV-3 infections. For instance, in a study on CCB cells infected with either SVCV or CyHV-3, a higher IFN-I upregulating response was detected through SVCV compared to CyHV-3, which oppositely diminished IFN-I production ^[12]. A similar trend of IFN response was noticed when different common carp strains (Amur wild carp, Amur sasan, AS; Ropsha scaly carp, Rop; Prerov scaly carp, PS; and koi) were challenged with the same viruses ^[41]. Rop was found to be more resistant to SVCV infection than the PS strain. During CyHV-3 infection, both Rop and AS displayed an increased survival rate compared with the PS strain. Interestingly, these observations were associated with increased activity of IFN-I among the SVCV resistant carp more than that in the CyHV-3 resistant group. The contribution of type 1 interferon to prevent SVCV, but not CyHV-3, infection appears to be a host–pathogen-specific interaction with the SVC virus.

Type 1 interferon, in addition to IL-12, are collectively known as signal-3 cytokines, which have been shown to activate clusters of differentiation 8 (CD8) T cells ^[42]. The cluster comprises CD8a and CD8b; both are dimeric co-receptors recognizing peptides presented by MHC class I molecules. They have a crucial role in immune defenses against various pathogens, including viruses. Both type 1 IFN and IL-12 were found to support the expansion and differentiation of CD8 T cells in vitro ^[43]^[44]. CD8 T cells also display an equivalent gene expression profile in the presence of either type 1 interferon or IL-12 and also upon in vitro stimulation. A survey conducted by Forlenza et al. ^[14] evaluated transcription of signal-3 cytokines, evident a concomitant of IL-12 and type 1 interferon, with CD8ab during SVCV infection in common carp. Precisely, signal-3 cytokines coincided with CD8ab upregulation at day 4 post SVCV infection. Initiation of CD8ab via signal-3 cytokines during SVCV infection indicates that these pro-inflammatory molecules play a regulatory and reciprocal role via the MHC-I pathway, which involves activating antigen-directed adaptive immunity.

Earlier research revealed the presence of active IFNs in sera of fish infected with viral hemorrhagic septicemia virus (VHSV), infectious hematopoietic necrosis virus (IHNV), and SVCV ^[45]. More recent follow-up research has confirmed the presence of these similar interferons via transcriptional upregulation of genes after experimental infection with the viruses mentioned above ^[40]^[46].

IFN-γ, in fish, generally evokes an immune response that features overriding virus-replicative activity. For instance, recombinant IFN-γ upregulates some interferon regulatory genes, including ISG12, ISG15, and Mx ^[47], and shows antiviral effects, such as the inhibition of viral structural proteins synthesis and the reduction of virus titer in different cell lines of Atlantic salmon ^[48]. In cyprinids, i.e., zebrafish, the biological activities of IFN-γ, in addition to groups 1 and 11 of IFNs that are classified as type I interferons in fish, have been evaluated in vivo during SVCV infection. Strikingly, and unlike groups 1 and 11 IFN-I, zebrafish interferon (zfIFNγ) failed to produce pro-inflammatory genes and antiviral effects when administered ^[40].

As previously mentioned, IFNs have a significant role in establishing an antiviral response against Carp sprivivirus involving initialization of the adaptive immunity. Despite that, Carp sprivivirus was reported to have the ability to evade host immune response ^[49]. Studies conducted by Li et al. ^[50] and Lu et al. ^[51] demonstrated that the overexpression of SVCV phosphoprotein N and glycoprotein G inhibits IFN synthesis in carp and zebrafish by reducing IFN transcription in host cells.

Interferons are not the only cytokines involved in the immune response during Carp sprivivirus infection. Some studies also observed an interleukin activity in response to this pathogen. For instance, carp IL-10 paralogues IL-10a and IL-10b possess similar protein sequences and phagocytes-provoking bioactivity were tested on carp head kidney cells. IL-10b had a low tissue constitutive expression in the liver, gut, gills, spleen, thymus, peripheral blood leucocytes, head, and trunk kidney when assessed in the absence of pathogens. However, it was upregulated during SVCV infection in the head and trunk kidney, followed by other tissues. Contrary to this, IL-10a gene expression did not change throughout the infection period despite its tissue constitutive expression being higher in healthy tissue ^[52].

3. Cytokine Studied in Response to Carp Edema Virus Infection

Carp edema virus disease (CEVD) or sleepy koi disease (KSD) is a rising threat to koi and carp aquaculture. The disease was first reported in koi carp farms in Japan in 1974, where it caused substantial mortalities ^[53]^[54]^[55] and economic losses. The nomenclature of sleepy koi disease is attributed to the behavioral abnormalities showed by affected carp, including lethargy and unresponsiveness. Consequently, the disease is called sleepy koi, and fish can be seen lying in the bottom of tanks for extended periods ^[56]. Gross lesions incorporating spreading hemorrhagic skin lesions with edema, particularly in the abdomen, pale gills, sunken eyes, and ulcerative inflammation on the anus may also be seen ^[57]^[58]^[59]. Overproduction of mucus on the skin and gills is also observed ^[60]^[61].

Carp edema virus (CEV), belonging to the Poxviridae family, consists of double-stranded DNA about 250–280 nm in diameter, with a mulberry-like structure ^[58]. Gills seem to be the primary site for the infection. In diseased fish, poxvirus-like structures were confirmed by electron microscopy in morphologically altered gill tissue ^[55]^[56]^[62]. Three different genogroups of CEV have been so far characterized: I, IIa, and IIb ^[63]^[64]. Genogroup I, which has been detected in most European waters, is mainly infective to common carp. Genogroup IIa is almost entirely, but not exclusively, reported in koi, while genogroup IIb has been detected in both carp and koi samples.

Poxviruses are contained through innate immunity undertaken by the inflammatory and NK cells ^[65]. These responses control viral replication and mount an antigenic adaptive response ^[66]. Similar to other viral infections, interferons (α, β, and γ) play an important role during poxvirus infections. Interferons produced by NK cells, fibroblasts, lymphocytes, and leucocytes conclusively control poxvirus replication. Nevertheless, poxviruses also modulate the host immune responses to guarantee their survival ^[67]. The implicated mechanism incorporates interruption of ISGs synthesis resulting in IFN inhibition. Furthermore, poxviruses possess immunomodulating genes able to competitively antagonize the IFN-α via encoding a homolog of the ligand-binding receptors chain for this interferon ^[68].

However, during CEV infection in carp, the host–virus interaction is reciprocally impacted by host genetic competitiveness and virus genomic characteristics. In other words, the carp edema virus, although it still remains unclassified, can probably vary in its genotype, as several emerging genogroups have so far been identified among carp populations worldwide. On the other hand, these genogroups are seemingly selective mutations targeted towards the numerous variants within the common carp species. It is reported that the underlying strains of carp highly influence the expression profile of cytokines during infections, specifically the IFN and ISGs ^[69].

The only study based on IFN and ISGs concerning CEVD was conducted by Adamek et al. ^[70]. In their study, different carp strains, including AS, PS, Rop, and koi carp, were exposed to CEV, genogroups I and II, to investigate their susceptibility to infection. Their analysis comprised the expression of type I interferon, ISGs encoding IFNa2 in gills. Amur wild carp was found to be more resistant to the infections than the other three strains/species. The significant finding of this study was the downregulation of IFNa2 and ISGs in response to CEV infection in AS, known to be a highly resistant species compared to other strains/species. Such an effect indicates an activation of the adaptive immunity at the proposed time of infection marked by suppression of cellular immunity through a shutdown of interferon expression. Potential development of humoral immunity and antibody production might have been the reason for resistance to CEV infection displayed by the AS compared to the other strains/species. Likewise, a lack or delay in initiating an antigenic-based adaptive immunity in susceptible strains could be responsible for the high mortalities. A similar cytokine cellular immune-responsiveness trend is reported in association with CyHV-3 and SVCV. Previous transcriptomic analysis of differentially expressed immune genes during CyHV-3 infection elucidated a rapid upregulation of IFNs and ISGs in susceptible strains versus resistant ones ^[69]. These observations were supported by other findings reporting an influence of carp strain on the interferon expression rate in fish infected with CyHV-3 or SVCV ^[41]. In contrast to CyHV-3 and SVCV infections, where the mechanism of IFN response has been studied quite thoroughly, there remains a paucity of research on IFN response during CEV infection in common carp. Overall, the response of IFNs in different carp strains/species to CEV infections is consistent with previous studies ^[69]^[41]. However, more research is required to support the IFNs response to CEV infection in carp strains.

4. Cytokine Studied in Response to Aeromonas hydrophila Infections

Aeromonas hydrophila is a rod-shaped Gram-negative bacterium and one of the most common bacterial pathogens infecting fish in freshwater ^[71]. Aeromonas hydrophila naturally inhabits the gastrointestinal tract of fish ^[72]. This bacterium predominantly affects teleosts that are highly susceptible to the infection, such as common carp, catfish, goldfish, and other tropical and ornamental fish ^[73]^[74]. Infected fish manifest different clinical signs, including swimming abnormalities, generalized edema, pale gills, and deep dermal ulcers ^[75]. In common carp, a distended abdomen and scale blisters on the skin are the prominent signs of this disease ^[76].

Eliminating bacterial pathogens in the host is carried out through an immediate and non-specific response. Upon the stimuli of the immune system with bacterial agents, the recruitment of several phagocytes involved in cytokine production like neutrophils, macrophages, and dendritic cells takes place ^[77]. During A. hydrophila infections, the secretion of cytokines such as ILs, IFNs, and TNFs hold great importance. Interleukins seem to be a focal point for immunological research interest, followed by tumor necrosis factors and interferons.

It is believed that the expression of IL1-β, IL-10, and IFN in carp during A. hydrophila invasion is triggered primarily by the toll-like receptor 18 (Tlr18), as indicated by a study on the epithelioma papulosum cyprini cell lines (EPC) ^[78]. This important pattern recognition molecule usually exists on macrophages and dendritic cells and has a fish-specific expansion that plays a crucial role in innate immunity against pathogens via cytokines activation.

In response to bacterial infections, IL-1β induces adhesion molecules (selectins, integrins, and cadherins), which assist in recruiting neutrophils to the site of inflammation ^[79]. Several studies have been conducted to evaluate the response of IL-1β during A. hydrophila infections. For instance, carp subjected to high temperature (30 °C) for 30 days and subsequently challenged with A. hydrophila had significantly elevated IL-1β and TNFα expression in the spleen and head kidney. Other immune or stress-related genes, such as inducible nitric oxide synthase (iNOS), glucocorticoid receptor (GR), and superoxide dismutase (SOD), were also suppressed ^[80].

The emergence of A. hydrophila in the carp population is common around the globe, but using antibiotics as a preventive measure has been questioned due to bacterial resistance and potential risk to consumer health ^[81]. Additionally, A. hydrophila has a significant strain diversity with plentiful pervasiveness in aquatic environments ^[82]. Therefore, developing an effective vaccine to control this pathogen remains an issue of interest. At present, various A. hydrophila vaccines have been developed, such as inoculations comprising killed whole bacteria, components of the pathogen macromolecules, biofilms, or non-replicated protein isolates ^[66]^[83]^[84]^[85]^[86]^[87]. Most of these vaccines, however, exhibit nonfunctional immunogenicity. Considering this fact, multiple research attempts have aimed to evaluate the efficiency of live, attenuated (XX1LA) or killed (by formalin) A. hydrophila to induce an early and adequate immune stimulation in carp. In both cases, upregulation of the IL-1β- and IL-10-related genes occurs in the spleen and liver specifically, as indicated in a study conducted by Jiang et al. ^[88]. Although other parameters, such as survival rate, antibody titer, and serum lysozyme were vaccine-dependent, it can be demonstrated that the IL-1β and IL-10 are major game changers in the innate immune defense against A. hydrophila with association to tissue-specific gene regulation.

Interleukin IL-17 is another nominated key pro-inflammatory cytokine involved in immunoreactions against bacterial infections in carp. In fact, IL-17 with pro-inflammatory characteristics plays an essential role against a wide range of viral, bacterial, and fungal infections ^[89]. Providing mucosal immunity at the first entry sites, i.e., gills and skin, against various pathogens is the hallmark of this cytokine, which exists abundantly in mucosal and immune tissues ^[90]. In mammals, interleukin comprises seven ligands, from IL-17A to IL-17F. IL-17A and IL-17F are pivotal cytokines that play a significant role in autoimmune disorders and immunological responses to pathogens ^[91].

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