Head Kidney-Derived Macrophages of Common Carp (<i>Cyprinus carpio</i> L.) Show Plasticity and Functional Polarization upon Differential Stimulation

Joerink, Maaike; Ribeiro, Carla M. S.; Stet, R.J.M.; Hermsen, Trudi; Savelkoul, H.F.J.; Wiegertjes, G.F.

doi:10.4049/jimmunol.177.1.61

Cited by 136 publications

(118 citation statements)

References 51 publications

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“…4B). Recently, functional heterogeneity was also reported in carp macrophages (44). These results indicate that fish monocytes are composed of many populations.…”

Section: Discussionmentioning

confidence: 64%

Teleost B7 Expressed on Monocytes Regulates T Cell Responses

Sugamata

Suetake

Kikuchi

et al. 2009

The Journal of Immunology

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In mammals, professional APCs induce adaptive immunity via the activation of T cells. During this process, B7 family molecules present upon APCs are known to play crucial roles in optimal T cell stimulation. In contrast, the confirmation of APCs in a nonmammalian vertebrate has yet to be achieved. To obtain further insights into the evolutionary origin of APCs, we have identified three members of the B7 family in the teleost Takifugu rubripes (fugu): B7-H1/DC, B7-H3, and B7-H4. The three fugu B7s were expressed on the surface of blood monocytes. The B7 ؉ monocytes, which are composed of at least two distinct populations, expressed the MHC class II component gene. The fugu B7 molecules bound to activated T cells, indicating that putative B7 receptors were expressed upon T cells. Fugu B7-H1/DC inhibited T cell proliferation concomitant with increasing levels of both IL-10 and IFN-␥ expression, whereas both B7-H3 and B7-H4 promoted T cell growth following IL-2 induction and the suppression of IL-10. These observations indicate that fugu B7s regulate T cell responses via receptors upon T cells. We suggest that fish B7 ؉ monocytes are APCs and that a costimulatory system has already developed in fish via the evolutionary process.

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“…4B). Recently, functional heterogeneity was also reported in carp macrophages (44). These results indicate that fish monocytes are composed of many populations.…”

Section: Discussionmentioning

confidence: 64%

Teleost B7 Expressed on Monocytes Regulates T Cell Responses

Sugamata

Suetake

Kikuchi

et al. 2009

The Journal of Immunology

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“…Peripheral blood leukocytes (PBL), mid-kidney leukocytes, head kidney leukocytes (HKL), and total thymocytes were isolated as described previously (14,15) and resuspended in the appropriate medium for the experiment as described below. Head kidney-derived mature macrophages (referred to as macrophages) were obtained upon 6 d culture of HKL as previously described (16).…”

Section: Cell Isolation and Culturementioning

confidence: 99%

Cyprinid Herpesvirus 3 Il10 Inhibits Inflammatory Activities of Carp Macrophages and Promotes Proliferation of Igm+ B Cells and Memory T Cells in a Manner Similar to Carp Il10

Piazzon

Wentzel

Tijhaar

et al. 2015

The Journal of Immunology

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Cyprinid herpesvirus 3 (CyHV-3) is the causative agent of a lethal disease of carp and encodes for an Il10 homolog (ORF134). Our previous studies with a recombinant ORF134-deleted strain and the derived revertant strain suggested that cyprinid herpesvirus 3 Il10 (CyHV-3 Il10 [cyhv3Il10]) is not essential for viral replication in vitro, or virulence in vivo. In apparent contrast, cyhv3Il10 is one of the most abundant proteins of the CyHV-3 secretome and is structurally very similar to carp Il10 and also human IL10. To date, studies addressing the biological activity of cyhv3Il10 on cells of its natural host have not been performed. To address the apparent contradiction between the presence of a structurally conserved Il10 homolog in the genome of CyHV-3 and the lack of a clear phenotype in vivo using recombinant cyhv3Il10-deleted viruses, we used an in vitro approach to investigate in detail whether cyhv3Il10 exerts any biological activity on carp cells. In this study, we provide direct evidence that cyhv3Il10 is biologically active and, similarly to carp Il10, signals via a conserved Stat3 pathway modulating immune cells of its natural host, carp. In vitro, cyhv3Il10 deactivates phagocytes with a prominent effect on macrophages, while also promoting proliferation of Igm+ B cells and memory T cells. Collectively, this study demonstrates a clear biological activity of cyhv3Il10 on cells of its natural host and indicates that cyhv3Il10 is a true viral ortholog of carp Il10. Furthermore, to our knowledge, this is the first report on biological activities of a nonmammalian viral Il10 homolog.

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“…Activated macrophages produce pro-and/or anti-inflammatory cytokines. Innate activation of carp macrophages is implied by activation of IL-1β, TNF-α and CXC chemokines genes [9]. In vivo and in vitro stimulation of carp head kidney phagocytes with LPS or peptidoglycan successfully induced IL-1β gene activation [7,12,13].…”

Section: Discussionmentioning

confidence: 99%

Protection against Atypical Aeromonas salmonicida Infection in Common Carp, Cyprinus carpio L., by Oral Administration of a Mixed Microbial Culture of Lactobacillus paracasei, Pichia membranifaciens and Saccharomyces cereviciae

Kodama

Nakamura

Kashima

et al. 2011

The Journal of Veterinary Medical Science

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ABSTRACT. A microbial culture was prepared by co-cultivation of Lactobacillus paracasei, Pichia membranifaciens and Saccharomyces cereviciae for 48 hr at 30C in rice bran extract medium, supplemented with dextrose. Oral administration of the resulting non-viable heat-inactivated microbial culture to common carp, Cyprinus carpio L., delivered in feed for four weeks, induced effective protection against experimental atypical Aeromonas salmonicida infection which causes "ulcer disease". After challenge of the carp by immersion, fish mortality and development of skin lesions such as hemorrhages and ulcers were significantly suppressed in carp treated with mixed microbial culture adsorbed on dry pellets relative to carp treated with medium or without extract. Atypical A. salmonicida was re-isolated from ulcerative lesions in parts of dead and surviving fish, but Aeromonas hydrophila and Flavobacterium sp. were also isolated from these fish, verifying microbial population changes during the progression of skin lesions. Among interleukin-1 (IL-1), tumor necrosis factor-, as well as CXC- and CXC- chemokines, gene expression of IL-1 was up regulated in the spleen and head kidney three weeks after administration of the mixed microbial culture. These results clearly show that this mixed microbial culture, delivered in feed, is effective in preventing A. salmonicida disease in carp.

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Head Kidney-Derived Macrophages of Common Carp (Cyprinus carpio L.) Show Plasticity and Functional Polarization upon Differential Stimulation

Cited by 136 publications

References 51 publications

Teleost B7 Expressed on Monocytes Regulates T Cell Responses

Teleost B7 Expressed on Monocytes Regulates T Cell Responses

Cyprinid Herpesvirus 3 Il10 Inhibits Inflammatory Activities of Carp Macrophages and Promotes Proliferation of Igm+ B Cells and Memory T Cells in a Manner Similar to Carp Il10

Protection against Atypical Aeromonas salmonicida Infection in Common Carp, Cyprinus carpio L., by Oral Administration of a Mixed Microbial Culture of Lactobacillus paracasei, Pichia membranifaciens and Saccharomyces cereviciae

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