Transcriptional regulation of antimicrobial peptides in mucosal tissues of Atlantic cod Gadus morhua L. in response to different stimuli

Aquaculture Research

Volumn 45, Issue 12, 2014, Pages 1893-1905

  Ruangsri, Jareeporn ^a   Lokesh, Jep ^a   Fernandes, Jorge M O ^a   Kiron, Viswanath ^a  

^a NORD UNIVERSITY   (Norway)

Author keywords

AMP; Antimicrobial peptides; Atlantic cod; Gadus morhua; Innate immunity

Indexed keywords

GADUS MORHUA;

EID: 84911958063     PISSN: 1355557X     EISSN: 13652109     Source Type: Journal    
DOI: 10.1111/are.12136     Document Type: Article

References (60)

1. Aberg K.M., Radek K.A., Choi E.H., Kim D.K., Demerjian M., Hupe M., Kerbleski J., Gallo R.L., Ganz T., Mauro T., Feingold K.R. & Elias P.M. (2007) Psychological stress downregulates epidermal antimicrobial peptide expression and increases severity of cutaneous infections in mice. The Journal of Clinical Investigation 117, 3339-3349.
2. Barbosa Pelegrini P., Del Sarto R.P., Silva O.N., Franco O.L. & Grossi-De-Sa M.F. (2011) Antibacterial peptides from plants: what they are and how they probably work. Biochemistry Research International 2011, 250349.
3. Bridle A., Nosworthy E., Polinski M. & Nowak B. (2011) Evidence of an antimicrobial-immunomodulatory role of Atlantic salmon cathelicidins during infection with Yersinia ruckeri. PLoS ONE 6, e23417.
4. Broekman D.C., Frei D.M., Gylfason G.A., Steinarsson A., Jornvall H., Agerberth B., Gudmundsson G.H. & Maier V.H. (2011) Cod cathelicidin: isolation of the mature peptide, cleavage site characterisation and developmental expression. Developmental and Comparative Immunology 35, 296-303.
5. Broekman D.C., Zenz A., Gudmundsdottir B.K., Lohner K., Maier V.H. & Gudmundsson G.H. (2011) Functional characterization of codCath, the mature cathelicidin antimicrobial peptide from Atlantic cod (Gadus morhua). Peptides 32, 2044-2051.
6. Caipang C.M.A., Brinchmann M.F., Berg I., Iversen M., Eliassen R. & Kiron V. (2008) Changes in selected stress and immune related genes in Atlantic cod, Gadus morhua, following overcrowding. Aquaculture Research 39, 1533-1540.
7. Caipang C.M.A., Berg I., Brinchmann M.F. & Kiron V. (2009) Short-term crowding stress in Atlantic cod, Gadus morhua L. modulates the humoral immune response. Aquaculture 295, 110-115.
8. Caipang C.M., Lazado C.C., Brinchmann M.F. & Kiron V. (2010) Infection-induced changes in expression of antibacterial and cytokine genes in the gill epithelial cells of Atlantic cod, Gadus morhua during incubation with bacterial pathogens. Comparative Biochemistry and Physiology Part B 156, 319-325.
9. Campagna S., Saint N., Molle G. & Aumelas A. (2007) Structure and mechanism of action of the antimicrobial peptide piscidin. Biochemistry 46, 1771-1778.
10. Casadei E., Wang T., Zou J., Gonzalez Vecino J.L., Wadsworth S. & Secombes C.J. (2009) Characterization of three novel beta-defensin antimicrobial peptides in rainbow trout (Oncorhynchus mykiss). Molecular Immunology 46, 3358-3366.
11. Chen J., Shen H., Chen C., Wang W., Yu S., Zhao M. & Li M. (2009) The effect of psychological stress on iron absorption in rats. BMC Gastroenterology 9, 83.
12. Chia T.J., Wu Y.C., Chen J.Y. & Chi S.C. (2010) Antimicrobial peptides (AMP) with antiviral activity against fish nodavirus. Fish and Shellfish Immunology 28, 434-439.
13. Choi H.J., Seo C.H., Park S.H., Yang H., Do K.H., Kim J., Kim H.K., Chung D.H., Ahn J.H. & Moon Y. (2011) Involvement of epidermal growth factor receptor-linked signaling responses in Pseudomonas fluorescens-infected alveolar epithelial cells. Infection and Immunity 79, 1998-2005.
14. Corrales J., Gordon W. & Noga E. (2009) Development of an ELISA for quantification of the antimicrobial peptide piscidin 4 and its application to assess stress in fish. Fish and Shellfish Immunology 27, 154-163.
15. Cuesta A., Meseguer J. & Esteban M.Á. (2011) Molecular and functional characterization of the gilthead seabream [beta]-defensin demonstrate its chemotactic and antimicrobial activity. Molecular Immunology 48, 1432-1438.
16. Dann S.M. & Eckmann L. (2007) Innate immune defenses in the intestinal tract: defensins. Current Opinion in Gastroenterology 23, 115-120.
17. Dhanasiri A.K.S., Brunvold L., Brinchmann M.F., Korsnes K., Bergh Ø. & Kiron V. (2011) Changes in the intestinal microbiota of wild Atlantic cod Gadus morhua L. upon captive rearing. Microbial Ecology 61, 20-30.
18. Douglas S.E., Gallant J.W., Liebscher R.S., Dacanay A. & Tsoi S.C. (2003) Identification and expression analysis of hepcidin-like antimicrobial peptides in bony fish. Developmental and Comparative Immunology 27, 589-601.
19. Falco A., Chico V., Marroquí L., Perez L., Coll J.M. & Estepa A. (2008) Expression and antiviral activity of a β-defensin-like peptide identified in the rainbow trout (Oncorhynchus mykiss) EST sequences. Molecular Immunology 45, 757-765.
20. Fernandes J.M., Mackenzie M.G., Wright P.A., Steele S.L., Suzuki Y., Kinghorn J.R. & Johnston I.A. (2006) Myogenin in model pufferfish species: comparative genomic analysis and thermal plasticity of expression during early development. Comparative Biochemistry and Physiology Part D 1, 35-45.
21. Fernandes J.M.O., Ruangsri J. & Kiron V. (2010) Atlantic cod piscidin and its diversification through positive selection. PLoS ONE 5, e9501.
22. Fogarty M., Incze L., Hayhoe K., Mountain D. & Manning J. (2008) Potential climate change impacts on Atlantic cod (Gadus morhua) off the northeastern USA. Mitigation and Adaptation Strategies for Global Change 13, 453-466.
23. Inami M., Taverne-Thiele A.J., Schrøder M.B., Kiron V. & Rombout J.H.W.M. (2009) Immunological differences in intestine and rectum of Atlantic cod (Gadus morhua L.). Fish and Shellfish Immunology 26, 751-759.
24. Jin J.Y., Zhou L., Wang Y., Li Z., Zhao J.-G., Zhang Q.-Y. & Gui J.-F. (2010) Antibacterial and antiviral roles of a fish β-defensin expressed both in pituitary and testis. PLoS ONE 5, e12883.
25. Kiron V. (2012) Fish immune system and its nutritional modulation for preventive health care. Animal Feed Science and Technology 173, 111-133.
26. Lai Y. & Gallo R.L. (2009) AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends in Immunology 30, 131-141.
27. Lazado C.C., Caipang C.M., Gallage S., Brinchmann M.F. & Kiron V. (2010) Expression profiles of genes associated with immune response and oxidative stress in Atlantic cod, Gadus morhua head kidney leukocytes modulated by live and heat-inactivated intestinal bacteria. Comparative Biochemistry and Physiology Part B 155, 249-255.
28. Lazado C.C., Caipang C.M.A., Rajan B., Brinchmann M.F. & Kiron V. (2010) Characterisation of GP21 and GP12: two potential probiotic bacteria isolated from the gastrointestinal tract of Atlantic cod. Probiotics and Antimicrobial Proteins 2, 126-134.
29. Lazado C.C., Caipang C.M.A. & Kiron V. (2012) Enzymes from the gut bacteria of Atlantic cod, Gadus morhua and their influence on intestinal enzyme activity. Aquaculture Nutrition 18, 423-431.
30. Liu F., Li J.-L., Yue G.-H., Fu J.-J. & Zhou Z.-F. (2010) Molecular cloning and expression analysis of the liver-expressed antimicrobial peptide 2 (LEAP-2) gene in grass carp. Veterinary Immunology and Immunopathology 133, 133-143.
31. Lokesh J. (2011) Transcription Analysis of Selected Cytokine Genes in the Intestine of Atlantic Cod. Faculty of Biosciences and Aquaculture, University of Nordland, Bodø, Norway, 80pp.
32. Maier V.H., Dorn K.V., Gudmundsdottir B.K. & Gudmundsson G.H. (2008) Characterisation of cathelicidin gene family members in divergent fish species. Molecular Immunology 45, 3723-3730.
33. Mangoni M. (2011) Host-defense peptides: from biology to therapeutic strategies. Cellular and Molecular Life Sciences 68, 2157-2159.
34. Nam B.H., Moon J.O., Kim Y.O., Kong H.J., Kim W.J., Lee S.J. & Kim K.K. (2010) Multiple β-defensin isoforms identified in early developmental stages of the teleost Paralichthys olivaceus. Fish and Shellfish Immunology 28, 267-274.
35. Nicolas G., Chauvet C., Viatte L., Danan J.L., Bigard X., Devaux I., Beaumont C., Kahn A. & Vaulont S. (2002) The gene encoding the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation. The Journal of Clinical Investigation 110, 1037-1044.
36. Noga E.J., Ullal A.J., Corrales J. & Fernandes J.M.O. (2011) Application of antimicrobial polypeptide host defenses to aquaculture: exploitation of downregulation and upregulation responses. Comparative Biochemistry and Physiology Part D 6, 44-54.
37. Olsvik P.A., Softeland L. & Lie K.K. (2008) Selection of reference genes for qRT-PCR studies of wild populations of Atlantic cod Gadus morhua. BMC Research Notes 1, 47.
38. Ortuño J., Esteban M.A. & Meseguer J. (2001) Effects of short-term crowding stress on the gilthead seabream (Sparus aurata L.) innate immune response. Fish and Shellfish Immunology 11, 187-197.
39. Pérez-Casanova J.C., Rise M.L., Dixon B., Afonso L.O.B., Hall J.R., Johnson S.C. & Gamperl A.K. (2008) The immune and stress responses of Atlantic cod to long-term increases in water temperature. Fish and Shellfish Immunology 24, 600-609.
40. Pongsaton J. (2009) Synergy Between Antibiotics and Antimicrobial Peptides of Atlantic Cod. Faculty of Biosciences and Aquaculture, University of Nordland, Bodø, Norway 110pp.
41. Robinette D.W. & Noga E.J. (2001) Histone-like protein: a novel method for measuring stress in fish. Diseases of Aquatic Organisms 44, 97-107.
42. Rodrigues P.N.S., Vázquez-Dorado S., Neves J.V. & Wilson J.M. (2006) Dual function of fish hepcidin: response to experimental iron overload and bacterial infection in sea bass (Dicentrarchus labrax). Developmental and Comparative Immunology 30, 1156-1167.
43. Ruangsri J., Fernandes J.M.O., Brinchmann M. & Kiron V. (2010) Antimicrobial activity in the tissues of Atlantic cod (Gadus morhua L.). Fish and Shellfish Immunology 28, 879-886.
44. Ruangsri J., Fernandes J.M.O., Rombout J.H.W.M., Brinchmann M.F. & Kiron V. (2012) Ubiquitous presence of piscidin-1 in Atlantic cod as evidenced by immunolocalisation. BMC Veterinary Research 8, 46 in press.
45. Ruangsri J., Salger S.A., Caipang C.M.A., Kiron V. & Fernandes J.M.O. (2012) Differential expression and biological activity of two piscidin paralogues and a novel splice variant in Atlantic cod (Gadus morhua L.). Fish and Shellfish Immunology 32, 396-406.
46. Shi J., Aono S., Lu W., Ouellette A.J., Hu X., Ji Y., Wang L., Lenz S., Van Ginkel F.W., Liles M., Dykstra C., Morrison E.E. & Elson C.O. (2007) A novel role for defensins in intestinal homeostasis: regulation of IL-1beta secretion. Journal of Immunology 179, 1245-1253.
47. Shike H., Lauth X., Westerman M.E., Ostland V.E., Carlberg J.M., Van Olst J.C., Shimizu C., Bulet P. & Burns J.C. (2002) Bass hepcidin is a novel antimicrobial peptide induced by bacterial challenge. European Journal of Biochemistry 269, 2232-2237.
48. Solstad T., Larsen A.N., Seppola M. & Jørgensen T.Ø. (2008) Identification, cloning and expression analysis of a hepcidin cDNA of the Atlantic cod (Gadus morhua L.). Fish and Shellfish Immunology 25, 298-310.
49. Star B., Nederbragt A.J., Jentoft S., Grimholt U., Malmstrom M., Gregers T.F., Rounge T.B., Paulsen J., Solbakken M.H., Sharma A., Wetten O.F., Lanzen A., Winer R., Knight J., Vogel J.H., Aken B., Andersen O., Lagesen K., Tooming-Klunderud A., Edvardsen R.B., Tina K.G., Espelund M., Nepal C., Previti C., Karlsen B.O., Moum T., Skage M., Berg P.R., Gjoen T., Kuhl H., Thorsen J., Malde K., Reinhardt R., Du L., Johansen S.D., Searle S., Lien S., Nilsen F., Jonassen I., Omholt S.W., Stenseth N.C. & Jakobsen K.S. (2011) The genome sequence of Atlantic cod reveals a unique immune system. Nature 477, 207-210.
50. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A. & Speleman F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, 1-11.
51. Vijayan M.M., Pereira C., Grau E.G. & Iwama G.K. (1997) Metabolic responses associated with confinement stress in tilapia: the role of cortisol. Comparative Biochemistry and Physiology Part C 116, 89-95.
52. Wang K.J., Cai J.J., Cai L., Qu H.D., Yang M. & Zhang M. (2009) Cloning and expression of a hepcidin gene from a marine fish (Pseudosciaena crocea) and the antimicrobial activity of its synthetic peptide. Peptides 30, 638-646.
53. Wehkamp K., Schwichtenberg L., Schroder J.-M.M. & Harder J. (2006) Pseudomonas aeruginosa- and IL-1 [beta]-mediated induction of human [beta] defensin-2 in keratinocytes is controlled by NF-[kappa] B and AP-1. The Journal of Investigative Dermatology 126, 121-127.
54. Weyts F.a.A., Cohen N., Flik G. & Verburg-Van Kemenade B.M.L. (1999) Interactions between the immune system and the hypothalamo-pituitary-interrenal axis in fish. Fish and Shellfish Immunology 9, 1-20.
55. Zakhartsev M., De Wachter B., Johansen T., Pörtner H.O. & Blust R. (2005) Hsp70 is not a sensitive indicator of thermal limitation in Gadus morhua. Journal of Fish Biology 67, 767-778.
56. Zanetti M. (2004) Cathelicidins, multifunctional peptides of the innate immunity. Journal of Leukocyte Biology 75, 39-48.
57. Zhang Y.-A., Zou J., Chang C.-I. & Secombes C.J. (2004) Discovery and characterization of two types of liver-expressed antimicrobial peptide 2 (LEAP-2) genes in rainbow trout. Veterinary Immunology and Immunopathology 101, 259-269.
58. Zhao J.G., Zhou L., Jin J.Y., Zhao Z., Lan J., Zhang Y.B., Zhang Q.Y. & Gui J.F. (2009) Antimicrobial activity-specific to Gram-negative bacteria and immune modulation-mediated NfκB and Sp1 of a medaka β-defensin. Developmental and Comparative Immunology 33, 624-637.
59. Zhao H.W., Zhou D. & Haddad G.G. (2011) Antimicrobial peptides increase tolerance to oxidant stress in Drosophila melanogaster. The Journal of Biological Chemistry 286, 6211-6218.
60. Zou J., Mercier C., Koussounadis A. & Secombes C. (2007) Discovery of multiple beta-defensin like homologues in teleost fish. Molecular Immunology 44, 638-647.