Characterization of virus/double-stranded RNA-dependent induction of antimicrobial peptide hepcidin in trout macrophages

Developmental and Comparative Immunology

Volumn 31, Issue 12, 2007, Pages 1297-1309

  Chiou, Pinwen Peter ^a   Lin, Chun Mean ^a   Bols, Niels C ^b   Chen, Thomas T ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Hepcidin; Infectious hematopoietic necrosis virus; Interferon; Macrophage; Poly I:C; RTS11; Toll like receptor

Indexed keywords

DOUBLE STRANDED RNA; HEPCIDIN; INTERFERON; MESSENGER RNA; POLYINOSINIC POLYCYTIDYLIC ACID; POLYPEPTIDE ANTIBIOTIC AGENT; TOLL LIKE RECEPTOR 3; VIRUS RNA;

ANIMAL CELL; ARTICLE; LIVER CELL; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN SYNTHESIS; RAINBOW TROUT; VIRUS CHARACTERIZATION;

BACTERIA (MICROORGANISMS); INFECTIOUS HEMATOPOIETIC NECROSIS VIRUS; ONCORHYNCHUS MYKISS; SALMONIDAE;

EID: 35648961324     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2007.03.009     Document Type: Article

References (43)

1. Krause A., Neitz S., Magert H.J., Schulz A., Forssmann W.G., Schulz-Knappe P., et al. LEAP-1, a novel highly disulfide-bonded human peptide, exhibits antimicrobial activity. FEBS Lett 480 (2000) 147-150
2. Park C.H., Valore E.V., Waring A.J., and Ganz T. Hepcidin, a urinary antimicrobial peptide synthesized in the liver. J Biol Chem 276 (2001) 7806-7810
3. Shi J., and Camus A.C. Hepcidins in amphibians and fishes: antimicrobial peptides or iron-regulatory hormones?. Dev Comp Immunol 30 (2006) 746-755
4. Verga Falzacappa M.V., and Muckenthaler M.U. Hepcidin: iron-hormone and anti-microbial peptide. Gene 364 (2005) 37-44
5. Nemeth E., Valore E.V., Territo M., Schiller G., Lichtenstein A., and Ganz T. Hepcidin, a putative mediator of anemia of inflammation, is a type II acute-phase protein. Blood 101 (2003) 2461-2463
6. Nemeth E., Tuttle M.S., Powelson J., Vaughn M.B., Donovan A., Ward D.M., et al. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306 (2004) 2090-2093
7. Lauth X., Babon J.J., Stannard J.A., Singh S., Nizet V., Carlberg J.M., et al. Bass hepcidin synthesis, solution structure, antimicrobial activities and synergism, and in vivo hepatic response to bacterial infections. J Biol Chem 280 (2005) 9272-9282
8. Shike H., Lauth X., Westerman M.E., Ostland V.E., Carlberg J.M., Van Olst J.C., et al. Bass hepcidin is a novel antimicrobial peptide induced by bacterial challenge. Eur J Biochem 269 (2002) 2232-2237
9. Rodrigues P.N., Vazquez-Dorado S., Neves J.V., and Wilson J.M. Dual function of fish hepcidin: response to experimental iron overload and bacterial infection in sea bass (Dicentrarchus labrax). Dev Comp Immunol 30 (2006) 1156-1167
10. Douglas S.E., Gallant J.W., Liebscher R.S., Dacanay A., and Tsoi S.C. Identification and expression analysis of hepcidin-like antimicrobial peptides in bony fish. Dev Comp Immunol 27 (2003) 589-601
11. Hirono I., Hwang J.Y., Ono Y., Kurobe T., Ohira T., Nozaki R., et al. Two different types of hepcidins from the Japanese flounder Paralichthys olivaceus. FEBS J 272 (2005) 5257-5264
12. Fraenkel P.G., Traver D., Donovan A., Zahrieh D., and Zon L.I. Ferroportin 1 is required for normal iron cycling in zebrafish. J Clin Invest 115 (2005) 1532-1541
13. Gracey A.Y., Troll J.V., and Somero G.N. Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis. Proc Natl Acad Sci USA 98 (2001) 1993-1998
14. Shike H., Shimizu C., Lauth X., and Burns J.C. Organization and expression analysis of the zebrafish hepcidin gene, an antimicrobial peptide gene conserved among vertebrates. Dev Comp Immunol 28 (2004) 747-754
15. Nicolas G., Bennoun M., Porteu A., Mativet S., Beaumont C., Grandchamp B., et al. Severe iron deficiency anemia in transgenic mice expressing liver hepcidin. Proc Natl Acad Sci USA 99 (2002) 4596-4601
16. Pigeon C., Ilyin G., Courselaud B., Leroyer P., Turlin B., Brissot P., et al. A new mouse liver-specific gene, encoding a protein homologous to human antimicrobial peptide hepcidin, is overexpressed during iron overload. J Biol Chem 276 (2001) 7811-7819
17. Zheng W., Liu G., Ao J., and Chen X. Expression analysis of immune-relevant genes in the spleen of large yellow croaker (Pseudosciaena crocea) stimulated with poly I:C. Fish Shellfish Immunol 21 (2006) 414-430
18. Huang P.H., Chen J.Y., and Kuo C.M. Three different hepcidins from tilapia, Oreochromis mossambicus: analysis of their expressions and biological functions. Mol Immunol 44 (2007) 1932-1944
19. Ganassin R.C., and Bols N.C. Development of a monocyte/macrophage-like cell line, RTS11, from rainbow trout spleen. Fish Shellfish Immunol 8 (1998) 457-476
20. Chen M.J., Chiou P.P., Yang B.Y., Lo H.C., Son J.K., Hendricks J., et al. Development of rainbow trout hepatoma cell lines: effect of pro-IGF-I Ea4-peptide on morphological changes and anchorage-independent growth. In Vitro Cell Dev Biol Anim 40 (2004) 118-128
21. Liu X.B., Nguyen N.B., Marquess K.D., Yang F., and Haile D.J. Regulation of hepcidin and ferroportin expression by lipopolysaccharide in splenic macrophages. Blood Cells Mol Dis 35 (2005) 47-56
22. Bayne C.J., Gerwick L., Fujiki K., Nakao M., and Yano T. Immune-relevant (including acute phase) genes identified in the livers of rainbow trout, Oncorhynchus mykiss, by means of suppression subtractive hybridization. Dev Comp Immunol 25 (2001) 205-217
23. Platanias L.C. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 5 (2005) 375-386
24. Blair J.B., Miller M.R., Pack D., Barnes R., Teh S.J., and Hinton D.E. Isolated trout liver cells: establishing short-term primary cultures exhibiting cell-to-cell interactions. In Vitro Cell Dev Biol 26 (1990) 237-249
25. Kawai T., and Akira S. TLR signaling. Cell Death Differ 13 (2006) 816-825
26. Brubacher J.L., Secombes C.J., Zou J., and Bols N.C. Constitutive and LPS-induced gene expression in a macrophage-like cell line from the rainbow trout (Oncorhynchus mykiss). Dev Comp Immunol 24 (2000) 565-574
27. Chiou P.P., Khoo J., Bols N.C., Douglas S., and Chen T.T. Effects of linear cationic alpha-helical antimicrobial peptides on immune-relevant genes in trout macrophages. Dev Comp Immunol 30 (2006) 797-806
28. Peyssonnaux C., Zinkernagel A.S., Datta V., Lauth X., Johnson R.S., and Nizet V. TLR4-dependent hepcidin expression by myeloid cells in response to bacterial pathogens. Blood 107 (2006) 3727-3732
29. Dewitte-Orr S.J., Zorzitto J.R., Sutton L.P., and Bols N.C. Preferential induction of apoptosis in the rainbow trout macrophage cell line, RTS11, by actinomycin D, cycloheximide and double stranded RNA. Fish Shellfish Immunol 18 (2005) 279-295
30. Wrighting D.M., and Andrews N.C. Interleukin-6 induces hepcidin expression through STAT3. Blood 108 (2006) 3204-3209
31. Jacobs B.L., and Langland J.O. When two strands are better than one: the mediators and modulators of the cellular responses to double-stranded RNA. Virology 219 (1996) 339-349
32. Bayne C.J., and Gerwick L. The acute phase response and innate immunity of fish. Dev Comp Immunol 25 (2001) 725-743
33. Gerwick L., Corley-Smith G., and Bayne C.J. Gene transcript changes in individual rainbow trout livers following an inflammatory stimulus. Fish Shellfish Immunol 22 (2007) 157-171
34. Ong S.T., Ho J.Z., Ho B., and Ding J.L. Iron-withholding strategy in innate immunity. Immunobiology 211 (2006) 295-314
35. Ahmed M., and Lyles D.S. Effect of vesicular stomatitis virus matrix protein on transcription directed by host RNA polymerases I, II, and III. J Virol 72 (1998) 8413-8419
36. Chiou P.P., Kim C.H., Ormonde P., and Leong J.A. Infectious hematopoietic necrosis virus matrix protein inhibits host-directed gene expression and induces morphological changes of apoptosis in cell cultures. J Virol 74 (2000) 7619-7627
37. Babitt J.L., Huang F.W., Wrighting D.M., Xia Y., Sidis Y., Samad T.A., et al. Bone morphogenetic protein signaling by hemojuvelin regulates hepcidin expression. Nat Genet 38 (2006) 531-539
38. Wang R.H., Li C., Xu X., Zheng Y., Xiao C., Zerfas P., et al. A role of SMAD4 in iron metabolism through the positive regulation of hepcidin expression. Cell Metab 2 (2005) 399-409
39. Kawai T., and Akira S. Innate immune recognition of viral infection. Nat Immunol 7 (2006) 131-137
40. Sen G.C., and Sarkar S.N. Transcriptional signaling by double-stranded RNA: role of TLR3. Cytokine Growth Factor Rev 16 (2005) 1-14
41. Werts C., Girardin S.E., and Philpott D.J. TIR, CARD and PYRIN: three domains for an antimicrobial triad. Cell Death Differ 13 (2006) 798-815
42. Gohda J., Matsumura T., and Inoue J. Cutting edge: TNFR-associated factor (TRAF) 6 is essential for MyD88-dependent pathway but not toll/IL-1 receptor domain-containing adaptor-inducing IFN-beta (TRIF)-dependent pathway in TLR signaling. J Immunol 173 (2004) 2913-2917
43. Ren H.L., Wang K.J., Zhou H.L., and Yang M. Cloning and organisation analysis of a hepcidin-like gene and cDNA from Japan sea bass, Lateolabrax japonicus. Fish Shellfish Immunol 21 (2006) 221-227