Ontogeny and modulation after PAMPs stimulation of β-defensin, hepcidin, and piscidin antimicrobial peptides in meagre (Argyrosomus regius)

Fish and Shellfish Immunology

Volumn 69, Issue , 2017, Pages 200-210

  Campoverde, Cindy ^a   Milne, Douglas J ^b   Estévez, Alicia ^a   Duncan, Neil ^a   Secombes, Christopher J ^b   Andree, Karl B ^a  

^a IRTA   (Spain)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Antimicrobial peptides; Argyrosomus regius; Immune response; Meagre; Ontogeny; PAMP

Indexed keywords

BETA DEFENSIN; BETA GLUCAN; HEPCIDIN; MESSENGER RNA; PISCIDIN; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; FISH PROTEIN; PATHOGEN ASSOCIATED MOLECULAR PATTERN;

ANIMAL CELL; ANIMAL TISSUE; ARGYROSOMUS REGIUS; ARTEMIA; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; EUROPEAN SEA BASS; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GILL; HATCHING; IMMUNOPHARMACOLOGY; INNATE IMMUNITY; INTESTINE TISSUE; JUVENILE; KIDNEY CELL; KIDNEY TISSUE; LARVA; LARVAL DEVELOPMENT; LIMIT OF QUANTITATION; MALE; MOLECULAR CLONING; NONHUMAN; ONTOGENY; OPEN READING FRAME; OPTIMAL DRUG DOSE; PHYLOGENETIC TREE; PREY; SCIAENIDAE; SPLEEN TISSUE; UPREGULATION; ANIMAL; GENETICS; IMMUNOLOGY; PERCIFORMES; PHYLOGENY; VETERINARY;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BETA-DEFENSINS; FISH PROTEINS; GENE EXPRESSION PROFILING; HEPCIDINS; PATHOGEN-ASSOCIATED MOLECULAR PATTERN MOLECULES; PERCIFORMES; PHYLOGENY;

EID: 85028070384     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2017.08.026     Document Type: Article

References (64)

1. Jenssen, H., Hamill, P., Hancock, R.E., Peptide antimicrobial agents. Clin. Microbiol. Rev. 19 (2006), 491–511, 10.1128/CMR.00056-05.
2. Smith, V.J., Desbois, A.P., Dyrynda, E.A., Conventional and unconventional antimicrobials from fish, marine invertebrates and micro-algae. Mar. Drugs 8 (2010), 1213–1262, 10.3390/md8041213.
3. Rajanbabu, V., Chen, J.-Y., Applications of antimicrobial peptides from fish and perspectives for the future. Peptides 32 (2011), 415–420, 10.1016/j.peptides.2010.11.005.
4. Casadei, E., Wang, T., Zou, J., González Vecino, J.L., Wadsworth, S., Secombes, C.J., Characterization of three novel β-defensin antimicrobial peptides in rainbow trout (Oncorhynchus mykiss). Mol. Immunol. 46 (2009), 3358–3366, 10.1016/j.molimm.2009.07.018.
5. Silphaduang, U., Noga, E.J., Antimicrobials: peptide antibiotics in mast cells of fish. Nature 414 (2001), 268–269, 10.1016/j.peptides.2010.11.005.
6. Murray, H.M., Gallant, J.W., Douglas, S.E., Cellular localization of pleurocidin gene expression and synthesis in winter flounder gill using immunohistochemistry and in situ hybridization. Cell Tissue Res. 312 (2003), 197–202, 10.1007/s00441-003-0723-3.
7. Salerno, G., Parrinello, N., Roch, P., Cammarata, M., cDNA sequence and tissue expression of an antimicrobial peptide, dicentracin; a new component of the moronecidin family isolated from head kidney leukocytes of sea bass, Dicentrarchus labrax. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 146 (2007), 521–529, 10.1016/j.cbpb.2006.12.007.
8. Masso-Silva, A.J., Diamond, G., Antimicrobial peptides from fish. Pharmaceuticals, 7, 2014, 10.3390/ph7030265.
9. Katzenback, B.A., Antimicrobial peptides as mediators of innate immunity in teleosts. Biol. (Basel) 4 (2015), 607–639, 10.3390/biology4040607.
10. Nam, B.-H., Moon, J.-Y., Kim, Y.-O., Kong, H.J., Kim, W.-J., Lee, S.-J., Kim, K.-K., Multiple β-defensin isoforms identified in early developmental stages of the teleost Paralichthys olivaceus. Fish. Shellfish Immunol. 28 (2010), 267–274, 10.1016/j.fsi.2009.11.004.
11. Tang, Y.Q., Yuan, J., Osapay, G., Osapay, K., Tran, D., Miller, C.J., Ouellette, A.J., Selsted, M.E., A cyclic antimicrobial peptide produced in primate leukocytes by the ligation of two truncated alpha-defensins. Science 286 (1999), 498–502, 10.1126/science.286.5439.498.
12. Zou, J., Mercier, C., Koussounadis, A., Secombes, C., Discovery of multiple beta-defensin like homologues in teleost fish. Mol. Immunol. 44 (2007), 638–647, 10.1016/j.molimm.2006.01.012.
13. Cuesta, A., Meseguer, J., Esteban, M.Á., Molecular and functional characterization of the gilthead seabream β-defensin demonstrate its chemotactic and antimicrobial activity. Mol. Immunol. 48 (2011), 1432–1438, 10.1016/j.molimm.2011.03.022.
14. Falco, A., Chico, V., Marroqui, L., Perez, L., Coll, J.M., Estepa, A., Expression and antiviral activity of a β-defensin-like peptide identified in the rainbow trout (Oncorhynchus mykiss) EST sequences. Mol. Immunol. 45 (2008), 757–765, 10.1016/j.molimm.2007.06.358.
15. Jin, J.-Y., Zhou, L., Wang, Y., Li, Z., Zhao, J.-G., Zhang, Q.-Y., Gui, J.-F., Antibacterial and antiviral roles of a fish β-defensin expressed both in pituitary and testis. PLoS One, 5, 2010, 10.1371/journal.pone.0012883 e12883.
16. Krause, A., Neitz, S., Mägert, H.-J., Schulz, A., Forssmann, W.-G., Schulz-Knappe, P., Adermann, K., LEAP-1, a novel highly disulfide-bonded human peptide, exhibits antimicrobial activity. FEBS Lett. 480 (2000), 147–150, 10.1016/S0014-5793(00)01920-7.
17. Douglas, S.E., Gallant, J.W., Liebscher, R.S., Dacanay, A., Tsoi, S.C.M., Identification and expression analysis of hepcidin-like antimicrobial peptides in bony fish. Dev. Comp. Immunol. 27 (2003), 589–601, 10.1016/S0145-305X(03)00036-3.
18. Hirono I, A.T., Hwang, J., Ono, Y., Kurobe, T., Ohira, T., Nozaki, R., Two different types of hepcidins from the Japanese flounder Paralichthys olivaceus. FEBS J. 272 (2005), 5257–5264, 10.1111/j.1742-4658.2005.04922.x.
19. Shike, H., Shimizu, C., Lauth, X., 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, 10.1016/j.dci.2003.11.009.
20. Wang, K.-J., Cai, J.-J., Cai, L., Qu, H.-D., Yang, M., Zhang, M., Cloning and expression of a hepcidin gene from a marine fish (Pseudosciaena crocea) and the antimicrobial activity of its synthetic peptide. Peptides 30 (2009), 638–646, 10.1016/j.peptides.2008.12.014.
21. Cho, Y.S., Lee, S.Y., Kim, K.H., Kim, S.K., Kim, D.S., Nam, Y.K., Gene structure and differential modulation of multiple rockbream (Oplegnathus fasciatus) hepcidin isoforms resulting from different biological stimulations. Dev. Comp. Immunol. 33 (2009), 46–58, 10.1016/j.dci.2008.07.009.
22. Martin-Antonio, B., Jiménez-Cantizano, R.M., Salas-Leiton, E., Infante, C., Manchado, M., Genomic characterization and gene expression analysis of four hepcidin genes in the redbanded seabream (Pagrus auriga). Fish. Shellfish Immunol. 26 (2009), 483–491, 10.1016/j.fsi.2009.01.012.
23. Padhi, A., Verghese, B., Evidence for positive Darwinian selection on the hepcidin gene of Perciform and Pleuronectiform fishes. Mol. Divers 11 (2007), 119–130, 10.1007/s11030-007-9066-4.
24. Salger, S.A., Cassady, K.R., Reading, B.J., Noga, E.J., A diverse family of host-defense peptides (piscidins) exhibit specialized anti-bacterial and Anti-Protozoal activities in fishes. PLoS One, 11, 2016, 10.1371/journal.pone.0159423 e0159423.
25. Cole, A.M., Weis, P., Diamond, G., Isolation and characterization of pleurocidin, an antimicrobial peptide in the skin secretions of winter flounder. J. Biol. Chem. 272 (1997), 12008–12013.
26. Niu, S.-F., Jin, Y., Xu, X., Qiao, Y., Wu, Y., Mao, Y., Su, Y.-Q., Wang, J., Characterization of a novel piscidin-like antimicrobial peptide from Pseudosciaena crocea and its immune response to Cryptocaryon irritans. Fish. Shellfish Immunol. 35 (2013), 513–524, 10.1016/j.fsi.2013.05.007.
27. Lin, W.-C., Chang, H.-Y., Chen, J.-Y., Electrotransfer of the tilapia piscidin 3 and tilapia piscidin 4 genes into skeletal muscle enhances the antibacterial and immunomodulatory functions of Oreochromis niloticus. Fish. Shellfish Immunol. 50 (2016), 200–209, 10.1016/j.fsi.2016.01.034.
28. Jing, Y., Xin-Jiang, L.U., Fang-Chao, C., Jiong, C., Molecular characterization and functional analysis of a piscidin gene in large yellow croaker (Larimichthys crocea). Zool Res. 37 (2016), 347–355.
29. Pan, C.-Y., Huang, T.-C., Wang, Y.-D., Yeh, Y.-C., Hui, C.-F., Chen, J.-Y., Oral administration of recombinant epinecidin-1 protected grouper (Epinephelus coioides) and zebrafish (Danio rerio) from Vibrio vulnificus infection and enhanced immune-related gene expressions. Fish. Shellfish Immunol. 32 (2012), 947–957, 10.1016/j.fsi.2012.01.023.
30. Pan, C.-Y., Wu, J.-L., Hui, C.-F., Lin, C.-H., Chen, J.-Y., Insights into the antibacterial and immunomodulatory functions of the antimicrobial peptide, epinecidin-1, against Vibrio vulnificus infection in zebrafish. Fish. Shellfish Immunol. 31 (2011), 1019–1025, 10.1016/j.fsi.2011.09.001.
31. Lin, S.-B., Fan, T.-W., Wu, J.-L., Hui, C.-F., Chen, J.-Y., Immune response and inhibition of bacterial growth by electrotransfer of plasmid DNA containing the antimicrobial peptide, epinecidin-1, into zebrafish muscle. Fish. Shellfish Immunol. 26 (2009), 451–458, 10.1016/j.fsi.2009.01.008.
32. Shoemaker, C.A., Evans, J.J., Klesius, P.H., Density and dose: factors affecting mortality of Streptococcus iniae infected tilapia (Oreochromis niloticus). Aquaculture 188 (2000), 229–235, 10.1016/S0044-8486(00)00346-X.
33. Zou, J., Bird, S., Minter, R., Horton, J., Cunningham, C., Secombes, C.J., Molecular cloning of the gene for interleukin-1β from Xenopus laevis and analysis of expression in vivo and in vitro. Immunogenetics 51 (2000), 332–338.
34. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S., MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28 (2011), 2731–2739, 10.1093/molbev/msr121.
35. Jukes, T.H., Cantor, C.R., Evolution of protein molecules. Mamm. Protein Metab., 3, 1969, 132.
36. Zhao, J.-G., Zhou, L., Jin, J.-Y., Zhao, Z., Lan, J., Zhang, Y.-B., Zhang, Q.-Y., Gui, J.-F., Antimicrobial activity-specific to Gram-negative bacteria and immune modulation-mediated NF-κB and Sp1 of a medaka β-defensin. Dev. Comp. Immunol. 33 (2009), 624–637, 10.1016/j.dci.2008.11.006.
37. Liang, T., Wang, D.-D., Zhang, G.-R., Wei, K.-J., Wang, W.-M., Zou, G.-W., Molecular cloning and expression analysis of two β-defensin genes in the blunt snout bream (Megalobrama amblycephala). Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 166 (2013), 91–98, 10.1016/j.cbpb.2013.07.006.
38. Ferraresso, S., Bonaldo, A., Parma, L., Buonocore, F., Scapigliati, G., Gatta, P.P., Bargelloni, L., Ontogenetic onset of immune-relevant genes in the common sole (Solea solea). Fish. Shellfish Immunol. 57 (2016), 278–292, 10.1016/j.fsi.2016.08.044.
39. Ostaff, M.J., Stange, E.F., Wehkamp, J., Antimicrobial peptides and gut microbiota in homeostasis and pathology. EMBO Mol. Med. 5 (2013), 1465–1483, 10.1002/emmm.201201773.
40. van der Marel, M., Adamek, M., Gonzalez, S.F., Frost, P., Rombout, J.H.W.M., Wiegertjes, G.F., Savelkoul, H.F.J., Steinhagen, D., Molecular cloning and expression of two β-defensin and two mucin genes in common carp (Cyprinus carpio L.) and their up-regulation after β-glucan feeding. Fish. Shellfish Immunol. 32 (2012), 494–501, 10.1016/j.fsi.2011.12.008.
41. Cerezuela, R., Guardiola, F.A., Meseguer, J., Esteban, M.A., Enrichment of gilthead seabream (Sparus aurata L.) diet with microalgae: effects on the immune system. Fish Physiol. Biochem. 38 (2012), 1729–1739, 10.1007/s10695-012-9670-9.
42. Huang, L., Yuan, Z., Liu, P., Zhou, T., Effects of promoter leakage on dynamics of gene expression. BMC Syst. Biol., 9, 2015, 16, 10.1186/s12918-015-0157-z.
43. Ruangsri, J., Kitani, Y., Kiron, V., Lokesh, J., Brinchmann, M.F., Karlsen, B.O., Fernandes, J.M.O., A novel beta-defensin antimicrobial peptide in Atlantic cod with stimulatory effect on phagocytic activity. PLoS One, 8, 2013, 10.1371/journal.pone.0062302 e62302.
44. Shi, J., Camus, A.C., Hepcidins in amphibians and fishes: antimicrobial peptides or iron-regulatory hormones?. Dev. Comp. Immunol. 30 (2006), 746–755, 10.1016/j.dci.2005.10.009.
45. Hilton, K.B., Lambert, L.A., Molecular evolution and characterization of hepcidin gene products in vertebrates. Gene 415 (2008), 40–48, 10.1016/j.gene.2008.02.016.
46. Seppola, M., Johnsen, H., Mennen, S., Myrnes, B., Tveiten, H., Maternal transfer and transcriptional onset of immune genes during ontogenesis in Atlantic cod. Dev. Comp. Immunol. 33 (2009), 1205–1211, 10.1016/j.dci.2009.06.013.
47. Wang, Y., Liu, X., Ma, L., Yu, Y., Yu, H., Mohammed, S., Chu, G., Mu, L., Zhang, Q., Identification and characterization of a hepcidin from half-smooth tongue sole Cynoglossus semilaevis. Fish. Shellfish Immunol. 33 (2012), 213–219, 10.1016/j.fsi.2012.04.011.
48. Das, A., Mohapatra, A., Sahoo, P.K., Cloning and characterization of antimicrobial peptide, hepcidin in medium carp, Puntius sarana. Int. J. Pept. Res. Ther. 21 (2015), 139–147, 10.1007/s10989-014-9438-4.
49. Neves, J.V., Caldas, C., Vieira, I., Ramos, M.F., Rodrigues, P.N.S., Multiple hepcidins in a teleost fish, Dicentrarchus labrax: different hepcidins for different roles. J. Immunol. 195 (2015), 2696–2709.
50. Kim, Y.-O., Park, E.-M., Nam, B.-H., Kong, H.J., Kim, W.-J., Lee, S.-J., Identification and molecular characterization of two hepcidin genes from black rockfish (Sebastes schlegelii). Mol. Cell. Biochem., 315, 2008, 131, 10.1007/s11010-008-9796-3.
51. Cuesta, A., Cerezuela, R., Esteban, M.Á., Meseguer, J., In vivo actions of melatonin on the innate immune parameters in the teleost fish gilthead seabream. J. Pineal Res. 45 (2008), 70–78, 10.1111/j.1600-079X.2008.00557.x.
52. Chiou, P.P., Lin, C.-M., Bols, N.C., Chen, T.T., Characterization of virus/double-stranded RNA-dependent induction of antimicrobial peptide hepcidin in trout macrophages. Dev. Comp. Immunol. 31 (2007), 1297–1309, 10.1016/j.dci.2007.03.009.
53. Chen, J.-Y., Lin, W.-J., Lin, T.-L., A fish antimicrobial peptide, tilapia hepcidin TH2-3, shows potent antitumor activity against human fibrosarcoma cells. Peptides 30 (2009), 1636–1642, 10.1016/j.peptides.2009.06.009.
54. Salger, S.A., Reading, B.J., Noga, E.J., Tissue localization of piscidin host-defense peptides during striped bass (Morone saxatilis) development. Fish. Shellfish Immunol. 61 (2017), 173–180, 10.1016/j.fsi.2016.12.034.
55. Dezfuli, B.S., Pironi, F., Giari, L., Noga, E.J., Immunocytochemical localization of piscidin in mast cells of infected seabass gill. Fish. Shellfish Immunol. 28 (2010), 476–482, 10.1016/j.fsi.2009.12.012.
56. Ruangsri, J., Salger, S.A., Caipang, C.M.A., Kiron, V., Fernandes, J.M.O., Differential expression and biological activity of two piscidin paralogues and a novel splice variant in Atlantic cod (Gadus morhua L.). Fish. Shellfish Immunol. 32 (2012), 396–406, 10.1016/j.fsi.2011.11.022.
57. Zhou, Q.-J., Su, Y.-Q., Niu, S.-F., Liu, M., Qiao, Y., Wang, J., Discovery and molecular cloning of piscidin-5-like gene from the large yellow croaker (Larimichthys crocea). Fish. Shellfish Immunol. 41 (2014), 417–420, 10.1016/j.fsi.2014.09.023.
58. Jing, Y., Xin-Jiang, L.U., Fang-Chao, C., Jiong, C., Molecular characterization and functional analysis of a piscidin gene in large yellow croaker (Larimichthys crocea). Zool. Res. 37 (2016), 347–355, 10.13918/j.issn.2095-8137.2016.6.347.
59. Silphaduang, U., Colorni, A., Noga, E.J., Evidence for widespread distribution of piscidin antimicrobial peptides in teleost fish. Dis. Aquat. Organ 72 (2006), 241–252, 10.3354/dao072241.
60. Noga, E.J., Silphaduang, U., Park, N.G., Seo, J.K., Stephenson, J., Kozlowicz, S., Piscidin 4, a novel member of the piscidin family of antimicrobial peptides. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 152 (2009), 299–305, 10.1016/j.peptides.2010.11.005.
61. Bae, J.-S., Shim, S.H., Hwang, S.D., Park, M.-A., Jee, B.-Y., An, C.-M., Kim, Y.-O., Kim, J.-W., Park, C.-I., Expression analysis and biological activity of moronecidin from rock bream, Oplegnathus fasciatus. Fish. Shellfish Immunol. 40 (2014), 345–353, 10.1016/j.fsi.2014.07.023.
62. Chinchar, V.G., Bryan, L., Silphadaung, U., Noga, E., Wade, D., Rollins-Smith, L., Inactivation of viruses infecting ectothermic animals by amphibian and piscine antimicrobial peptides. Virology 323 (2004), 268–275, 10.1016/j.virol.2004.02.029.
63. Sun, B.J., Xie, H.X., Song, Y., Nie, P., Gene structure of an antimicrobial peptide from mandarin fish, Siniperca chuatsi (Basilewsky), suggests that moronecidins and pleurocidins belong in one family: the piscidins. J. Fish. Dis. 30 (2007), 335–343, 10.1111/j.1365-2761.2007.00789.x.
64. Pan, C.-Y., Tsai, T.-Y., Su, B.-C., Hui, C.-F., Chen, J.-Y., Study of the antimicrobial activity of Tilapia piscidin 3 (TP3) and TP4 and their effects on immune functions in hybrid Tilapia (Oreochromis spp.). PLoS One, 12, 2017, 10.1371/journal.pone.0169678 e0169678.