Tonsil conventional dendritic cells are not infected by porcine reproductive and respiratory syndrome virus

Puebla-Clark, Lucinda; Parra-Sánchez, Héctor; Reséndiz, Mónica; Valenzuela, Olivia; Hernández, Jesús

doi:10.1016/j.virol.2019.01.012

Cited by 8 publications

(16 citation statements)

References 32 publications

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“…The two main PRRSV cellular receptors are CD169/Sialoadhesin that allows the binding of the virus and CD163 which is essential for the release of the viral genome in the cytosol [for review see (16)]. PRRSV cellular targets are cells from the monocytic lineage, among them so far, only alveolar macrophages (MΦ) (17–19), pulmonary intravascular MΦ (20, 21) and CD163-positive tonsil macrophages (22) have been shown to be actually infected in vivo . We and others recently showed that in vivo , primary dendritic cells from lung (23) and tonsil (22) were not infected by the virus.…”

Section: Introductionmentioning

confidence: 99%

Macrophage-B Cell Interactions in the Inverted Porcine Lymph Node and Their Response to Porcine Reproductive and Respiratory Syndrome Virus

et al. 2019

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Swine lymph nodes (LN) present an inverted structure compared to mouse and human, with the afferent lymph diffusing from the center to the periphery. This structure, also observed in close and distant species such as dolphins, hippopotamus, rhinoceros, and elephants, is poorly described, nor are the LN macrophage populations and their relationship with B cell follicles. B cell maturation occurs mainly in LN B cell follicles with the help of LN macrophage populations endowed with different antigen delivery capacities. We identified three macrophage populations that we localized in the inverted LN spatial organization. This allowed us to ascribe porcine LN MΦ to their murine counterparts: subcapsular sinus MΦ, medullary cord MΦ and medullary sinus MΦ. We identified the different intra and extrafollicular stages of LN B cells maturation and explored the interaction of MΦ, drained antigen and follicular B cells. The porcine reproductive and respiratory syndrome virus (PRRSV) is a major porcine pathogen that infects tissue macrophages (MΦ). PRRSV is persistent in the secondary lymphoid tissues and induces a delay in neutralizing antibodies appearance. We observed PRRSV interaction with two LN MΦ populations, of which one interacts closely with centroblasts. We observed BCL6 up-regulation in centroblast upon PRRSV infection, leading to new hypothesis on PRRSV inhibition of B cell maturation. This seminal study of porcine LN will permit fruitful comparison with murine and human LN for a better understanding of normal and inverted LN development and functioning.

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Section: Introductionmentioning

confidence: 99%

Macrophage-B Cell Interactions in the Inverted Porcine Lymph Node and Their Response to Porcine Reproductive and Respiratory Syndrome Virus

et al. 2019

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“…However, the expression of CD80/86 and MHCII is affected by PRRSV infection, and the expression of interleukin-10 (IL-10) is increased [11]. Finally, in vivo, cDCs from PRRSV-experimentally infected pigs are not susceptible to the virus [12,13], while moDCs or bmDCs are susceptible [11]. These discrepancies show that moDCs and bmDCs, despite being an excellent study model, show limitations in understanding the interaction between PRRSV and DCs.…”

Section: Introductionmentioning

confidence: 99%

“…It is known that PRRSV infects monocytes, macrophages [11,14] and moDCs or bmDCs [14]. Nevertheless, lung, trachea and tonsil cDCs are refractory to PRRSV infection [12,13,15]. In the trachea, subtypes of cDCs have a variable response to PRRSV, as cDC1 expresses IFNα, and cDC2 expresses IL-10 [15].…”

Section: Introductionmentioning

confidence: 99%

Analysis of Swine Conventional Dendritic Cells, DEC205+CD172a+/−CADM1+, from Blood and Spleen in Response to PRRSV and PEDV

Parra-Sánchez

Bustamante-Córdova

Reséndiz

et al. 2019

Viruses

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Conventional dendritic cells (cDCs) cannot be infected by porcine reproductive and respiratory syndrome virus (PRRSV) but respond to infection via cytokine production, indicating a possible role in initiation/regulation of the immune response against PRRSV. In this work, we evaluated the responses of splenic and blood cDCs, with DEC205+CADM1+CD172a+/− phenotype, as well as those of CD163+ cells against PRRSV and porcine epidemic diarrhea virus (PEDV). Both populations were incubated in the presence of PRRSV or PEDV with and without naïve CD3+ T cells, and cytokine responses were evaluated by qPCR and ELISA. Our results showed that cDCs, but not CD163+ cells, produced IL-12 in response to PRRSV. PEDV did not induce IL-12 production. Cocultures of cDCs and autologous naïve CD3+ cells resulted in decreased IL-12 production and low expression of IFN-γ transcripts in response to PRRSV. Interestingly, cDCs increased the proliferation of naïve T cells in the presence of PRRSV compared with that achieved with monocytes and peripheral blood mononuclear cells (PBMCs). Cocultures of CD163+ cells induced IL-10 and IL-4 expression in the presence of PRRSV and PEDV, respectively. In conclusion, cDCs can selectively produce IL-12 in response to PRRSV but poorly participate in the activation of naïve T cells.

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“…Porcine dendritic cell (DC) populations, i.e., conventional DC (cDC) and non-conventional DC, exhibit different PRRSV susceptibility. Several studies strongly indicated that PRRSV could not infect both cDC1 and cDC2 populations (54–56). It should be emphasized that this study utilized MoDC, a non-conventional DC, and that the observed PRRSV infectivity in porcine MoDC was consistent with the previous reports (10, 57).…”

Section: Discussionmentioning

confidence: 99%

Negative Immunomodulatory Effects of Type 2 Porcine Reproductive and Respiratory Syndrome Virus-Induced Interleukin-1 Receptor Antagonist on Porcine Innate and Adaptive Immune Functions

et al. 2019

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Impaired innate and adaptive immune responses are evidenced throughout the course of PRRSV infection. We previously reported that interleukin-1 receptor antagonist (IL-1Ra) was involved in PRRSV-induced immunosuppression during an early phase of infection. However, the exact mechanism associated with PRRSV-induced IL-1Ra immunomodulation remains unknown. To explore the immunomodulatory properties of PRRSV-induced IL-1Ra on porcine immune functions, monocyte-derived dendritic cells (MoDC) and leukocytes were cultured with type 2 PRRSV, and the immunological role of IL-1Ra was assessed by addition of anti-porcine IL-1Ra Ab. The results demonstrated that PRRSV - induced IL-1Ra reduced phagocytosis, surface expression of MHC II (SLA-DR) and CD86, as well as downregulation of IFNA and IL1 gene expression in the MoDC culture system. Interestingly, IL-1Ra secreted by the PRRSV-infected MoDC also inhibited T lymphocyte differentiation and proliferation, but not IFN-γ production. Although PRRSV-induced IL-1Ra was not directly linked to IL-10 production, it contributed to the differentiation of regulatory T lymphocytes (Treg) within the culture system. Taken together, our results demonstrated that PRRSV-induced IL-1Ra downregulates innate immune functions, T lymphocyte differentiation and proliferation, and influences collectively with IL-10 in the Treg induction. The immunomodulatory roles of IL-1Ra elucidated in this study increase our understanding of the immunobiology of PRRSV.

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Tonsil conventional dendritic cells are not infected by porcine reproductive and respiratory syndrome virus

Cited by 8 publications

References 32 publications

Macrophage-B Cell Interactions in the Inverted Porcine Lymph Node and Their Response to Porcine Reproductive and Respiratory Syndrome Virus

Macrophage-B Cell Interactions in the Inverted Porcine Lymph Node and Their Response to Porcine Reproductive and Respiratory Syndrome Virus

Analysis of Swine Conventional Dendritic Cells, DEC205+CD172a+/−CADM1+, from Blood and Spleen in Response to PRRSV and PEDV

Negative Immunomodulatory Effects of Type 2 Porcine Reproductive and Respiratory Syndrome Virus-Induced Interleukin-1 Receptor Antagonist on Porcine Innate and Adaptive Immune Functions

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