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Receptor-mediated and lectin-like activities of carp (Cyprinus carpio) TNF-alpha.
J Immunol. 2009 Oct 15; 183(8):5319-32.JI

Abstract

Functional characterization of TNF-alpha in species other than mammalian vertebrates is limited, and TNF-alpha has been studied in a limited number of fish species, primarily in vitro using recombinant proteins. Studies on TNF-alpha from different fish species so far pointed to several inconsistencies, in particular with respect to some receptor-mediated activities of fish TNF-alpha, such as the ability to directly activate phagocytes. In the present study a comprehensive analysis of in vitro as well as in vivo biological activities of two isoforms of carp TNF-alpha was performed. Our results show that carp TNF-alpha directly primes carp phagocytes and indirectly promotes typical receptor-mediated activities such as phagocyte activation by acting via endothelial cells. Additionally, for the first time in nonmammalian vertebrate species, the lectin-like activity of fish TNF-alpha homologs was investigated. Our results show an evolutionary conservation of function of this receptor-independent activity of TNF-alpha not only in cyprinid fish, but also in perciform and salmonid fish. The role of TNF-alpha in vivo, during infections of carp with the blood parasite Trypanoplasma borreli, was examined using three fundamentally different but complementary approaches: (1) inhibition of TNF-alpha expression, (2) overexpression of TNF-alpha, and (3) inhibition of shedding of membrane-bound TNF-alpha. Our results show that, also in fish, a tight regulation of TNF-alpha expression is important, since depletion or excess of TNF-alpha can make an important difference to survival of infection. Finally, we demonstrate a crucial protective role for membrane-bound TNF-alpha, which has a yet unexploited function in fish.

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Authors+Show Affiliations

Forlenza M
Cell Biology and Immunology Group, Wageningen Institute of Animal Sciences, Wageningen University, Wageningen, The Netherlands.
Magez S
No affiliation info available
Scharsack JP
No affiliation info available
Westphal A
No affiliation info available
Savelkoul HF
No affiliation info available
Wiegertjes GF
No affiliation info available

MeSH

Amino Acid SequenceAnimalsCarpsCell MovementEndothelial CellsFish DiseasesGene ExpressionLectinsMolecular Sequence DataPentoxifyllinePhagocytesPhagocytosisPhosphodiesterase InhibitorsRecombinant ProteinsSequence AlignmentTrypanosomiasisTumor Necrosis Factor-alphaUp-Regulation

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

19786556

Citation

Forlenza, Maria, et al. "Receptor-mediated and Lectin-like Activities of Carp (Cyprinus Carpio) TNF-alpha." Journal of Immunology (Baltimore, Md. : 1950), vol. 183, no. 8, 2009, pp. 5319-32.
Forlenza M, Magez S, Scharsack JP, et al. Receptor-mediated and lectin-like activities of carp (Cyprinus carpio) TNF-alpha. J Immunol. 2009;183(8):5319-32.
Forlenza, M., Magez, S., Scharsack, J. P., Westphal, A., Savelkoul, H. F., & Wiegertjes, G. F. (2009). Receptor-mediated and lectin-like activities of carp (Cyprinus carpio) TNF-alpha. Journal of Immunology (Baltimore, Md. : 1950), 183(8), 5319-32. https://doi.org/10.4049/jimmunol.0901780
Forlenza M, et al. Receptor-mediated and Lectin-like Activities of Carp (Cyprinus Carpio) TNF-alpha. J Immunol. 2009 Oct 15;183(8):5319-32. PubMed PMID: 19786556.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Receptor-mediated and lectin-like activities of carp (Cyprinus carpio) TNF-alpha. AU - Forlenza,Maria, AU - Magez,Stefan, AU - Scharsack,Jörn P, AU - Westphal,Adrie, AU - Savelkoul,Huub F J, AU - Wiegertjes,Geert F, Y1 - 2009/09/28/ PY - 2009/9/30/entrez PY - 2009/9/30/pubmed PY - 2009/11/11/medline SP - 5319 EP - 32 JF - Journal of immunology (Baltimore, Md. : 1950) JO - J Immunol VL - 183 IS - 8 N2 - Functional characterization of TNF-alpha in species other than mammalian vertebrates is limited, and TNF-alpha has been studied in a limited number of fish species, primarily in vitro using recombinant proteins. Studies on TNF-alpha from different fish species so far pointed to several inconsistencies, in particular with respect to some receptor-mediated activities of fish TNF-alpha, such as the ability to directly activate phagocytes. In the present study a comprehensive analysis of in vitro as well as in vivo biological activities of two isoforms of carp TNF-alpha was performed. Our results show that carp TNF-alpha directly primes carp phagocytes and indirectly promotes typical receptor-mediated activities such as phagocyte activation by acting via endothelial cells. Additionally, for the first time in nonmammalian vertebrate species, the lectin-like activity of fish TNF-alpha homologs was investigated. Our results show an evolutionary conservation of function of this receptor-independent activity of TNF-alpha not only in cyprinid fish, but also in perciform and salmonid fish. The role of TNF-alpha in vivo, during infections of carp with the blood parasite Trypanoplasma borreli, was examined using three fundamentally different but complementary approaches: (1) inhibition of TNF-alpha expression, (2) overexpression of TNF-alpha, and (3) inhibition of shedding of membrane-bound TNF-alpha. Our results show that, also in fish, a tight regulation of TNF-alpha expression is important, since depletion or excess of TNF-alpha can make an important difference to survival of infection. Finally, we demonstrate a crucial protective role for membrane-bound TNF-alpha, which has a yet unexploited function in fish. SN - 1550-6606 UR - https://www.unboundmedicine.com/medline/citation/19786556/Receptor_mediated_and_lectin_like_activities_of_carp__Cyprinus_carpio__TNF_alpha_ L2 - http://www.jimmunol.org/cgi/pmidlookup?view=long&pmid=19786556 DB - PRIME DP - Unbound Medicine ER -