A Comprehensive Review on Porcine Reproductive and Respiratory Syndrome Virus with Emphasis on Immunity
Abstract
:1. The Porcine Reproductive and Respiratory Syndrome—History and Relevance
1.1. History
1.2. Economic and Scientific Relevance
2. Taxonomy, Viral Structure and Genetic Diversity
2.1. Taxonomy
2.2. Genome and Viral Structure
2.3. Genetic Diversity and Phylogeny
3. Pathogenesis
3.1. Cell Tropism, Viral Entry and Replication
3.2. Stages of Infection, Disease Mechanisms and Clinical Signs
3.2.1. Acute and Persistent Infections
3.2.2. Induction of Apoptosis
3.2.3. Modulation of Immune Response and Secondary Infections
3.2.4. Clinical Signs
3.3. Transmission, Risk Factors and Biosecurity
4. Modulation of the Innate Immune Response
4.1. Innate Immune Cells and Their Interaction with PRRSV
4.1.1. Macrophages
4.1.2. Dendritic Cells
- The first subset contains the conventional DCs (cDCs), which play a major role as APCs.
- The second subset consists of the plasmacytoid DCs (pDCs), which play a role in the regulation of the immune response, by production of both anti-viral cytokines (mainly IFN-α) and proinflammatory cytokines and chemokines, including IL-6, IL-12, CXC-chemokine ligand 8 (CXCL8), CXCL10, CC-chemokine ligand 3 (CCL3) and CCL4.
4.1.3. Natural Killer Cells
4.2. Pathogen Recognition and Type I Interferon Response
4.3. PRRSV Modulation of the Type I Interferon Response
- Liu et al. (2019) described the downregulation of IRF7 by the PRRSV NSP7 in infected PAMs [205].
- A further modulation of the type I interferon response is achieved by the PRRSV NSP1α. This non-structural protein contributes to the degradation of the cyclic AMP responsive element-binding protein (CBP). Since CBP is an important coactivator for many transcription factors, including the IRFs, its degradation indirectly inhibits the type I interferon response [208,209].
- Liu et al. (2020) described the immunosuppressive function of Sn, which was shown to suppress type I interferon responses by targeting the NF-κB pathway [210]. Further inhibition of the NF-κB pathway has been described for NSP4, which cleaves an essential mediator of the NF-κB pathway, and for NSP1α, NSP2 and NSP11, which interfere with the translocation of NF-κB to the nucleus [211,212,213,214].
- Finally, PRRSV can further modulate the innate immune response by influencing the expression of microRNA (miRNA) [215,216,217,218]. The miRNAs are small non-coding RNAs, typically 19 to 25 nucleotides in length, that play a role during the post-transcriptional gene expression. They can bind to certain target mRNAs, which results in gene silencing [219]. Hicks et al. (2013) performed deep sequencing of in vitro PRRSV-2-infected PAMs at 48 h post-infection and compared the miRNAome of these infected PAMs with the miRNAome of mock-infected PAMs [216]. A significantly different expression of 40 cellular miRNAs was observed in the PRRSV-2 infected PAMs. Furthermore, analysis of the target genes of these differentially expressed miRNAs revealed that most of them targeted genes involved in immune regulation, including the production of cytokines. The upregulation of miR-24-3p [220], miR-30c [221], miR-373 [222] and miR-382-5p [223] has been described during PRRSV infection. These miRNA silence genes are responsible for the type I interferon response. Therefore, the upregulation of these miRNAs by PRRSV inhibits type I interferon production and further facilitates immune escape and replication. Additionally, Zhang et al. (2021) reported the downregulation of miR-218 by PRRSV [224]. This miRNA silences an inhibitor of the type I interferon response, and thus, downregulation of miR-218 results in further inhibition of the interferon response.
5. Modulation of the Adaptive Immune Response
5.1. T Cells and Cell-Mediated Immunity
Role of T Cells during PRRSV Infection
5.2. B Cells and Humoral Response
- IgM is associated with the primary immune response. The monomeric IgMs have a lower affinity compared to the other Ig isotypes. However, they will typically form a pentameric complex, consisting of five IgM molecules linked via disulfide bonds. Due to this, the pentameric IgM complex can have multiple interactions with a certain antigen, resulting in a high avidity. The main function of IgM is the coating of the antigen (opsonization), which targets the antigen for destruction [256].
- IgAs are mainly found at mucosal surfaces and secretions, where they are mainly present in the forms of dimers, termed secretory IgA (sIgA). Additionally, they can be present in serum, although at lower concentrations and in the form of monomers. The main function of IgA is the protection of the mucosal surfaces, both by the direct neutralization of pathogens and by the prevention of binding of pathogens to the mucosal surfaces [256].
- IgGs are the dominant isotype, they have the longest serum half-life and play a critical role in the immune response [256]. They can eliminate pathogens, either directly, by neutralization, or indirectly, by activation of the complement cascade [256,257,258]. In pigs, six IgG subclasses were originally reported, based on the cDNA sequencing of the immunoglobulin heavy chain constant region (IGHG) gene [253]. However genomic analyses revealed that the porcine IGHG genes can be classified into nine subclasses, which are variably present in different pig breeds [259]. Therefore, depending on the breed of the pig and the genetic analysis that is used to determine the IGHG genes, a different amount of IgG subclasses can be defined [259].
- IgE plays a minor role in viral infections but is known as a highly potent Ig, typically associated with hypersensitivity and allergy reactions [256].
- Finally, the role of IgD is still under investigation [260]. It was first considered as a vestigial isotype in most mammals, without a role in the antibody-mediated immune response but with a function during the development and activation of B cells [253]. More recent findings indicate that, at least in humans and mice, sIgD could recognize antigens from aerodigestive commensal microbiota, food and pathogens and play a role in the maintenance of mucosal homeostasis in cooperation with IgA and IgG [261,262].
Role of B Cells and the Humoral Response during PRRSV Infection
- Second, the induction of antibodies directed against the major neutralizing epitope of PRRSV, the GP5 protein, is not sufficient to clear the virus [287].
6. Research Gaps
7. Methodology
8. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
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Fiers, J.; Cay, A.B.; Maes, D.; Tignon, M. A Comprehensive Review on Porcine Reproductive and Respiratory Syndrome Virus with Emphasis on Immunity. Vaccines 2024, 12, 942. https://doi.org/10.3390/vaccines12080942
Fiers J, Cay AB, Maes D, Tignon M. A Comprehensive Review on Porcine Reproductive and Respiratory Syndrome Virus with Emphasis on Immunity. Vaccines. 2024; 12(8):942. https://doi.org/10.3390/vaccines12080942
Chicago/Turabian StyleFiers, Jorian, Ann Brigitte Cay, Dominiek Maes, and Marylène Tignon. 2024. "A Comprehensive Review on Porcine Reproductive and Respiratory Syndrome Virus with Emphasis on Immunity" Vaccines 12, no. 8: 942. https://doi.org/10.3390/vaccines12080942