Oxidative burst and nitric oxide responses in carp macrophages induced by zymosan, MacroGard® and selective dectin-1 agonists suggest recognition by multiple pattern recognition receptors

Fish and Shellfish Immunology

Volumn 35, Issue 3, 2013, Pages 847-857

  Pietretti, D ^a   Vera Jimenez, N I ^b   Hoole, D ^c   Wiegertjes, G F ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c KEELE UNIVERSITY   (United Kingdom)

Author keywords

Carp; Fish; Nitric oxide; Respiratory burst; Glucan receptors

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); BASIDIOMYCOTA; CYPRINIDAE; FUNGI; MAMMALIA; SACCHAROMYCES CEREVISIAE;

CYTOKINE; DECTIN 1; GLUCAN; LECTIN; NITRIC OXIDE; NITROGEN; REACTIVE OXYGEN METABOLITE; TLR2 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 2; ZYMOSAN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CARP; CELL STRAIN HEK293; CHEMISTRY; CYTOLOGY; DIET SUPPLEMENTATION; DRUG EFFECT; DRUG POTENTIATION; FISH; GENE EXPRESSION REGULATION; GENETICS; HEAD KIDNEY; HUMAN; MACROPHAGE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; RESPIRATORY BURST; SPECIES DIFFERENCE; Β-GLUCAN RECEPTORS;

CARP; FISH; NITRIC OXIDE; RESPIRATORY BURST; Β-GLUCAN RECEPTORS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CYTOKINES; DIETARY SUPPLEMENTS; GENE EXPRESSION REGULATION; GLUCANS; HEAD KIDNEY; HEK293 CELLS; HUMANS; LECTINS, C-TYPE; MACROPHAGES; MOLECULAR SEQUENCE DATA; NITRIC OXIDE; NITROGEN; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST; SPECIES SPECIFICITY; TOLL-LIKE RECEPTOR 2; ZYMOSAN;

EID: 84882862308     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2013.06.022     Document Type: Article

References (71)

1. Couso N., Castro R., Magariños B., Obach A., Lamas J. Effect of oral administration of glucans on the resistance of gilthead seabream to pasteurellosis. Aquaculture 2003, 219:99-109.
2. Siwicki A.K., Zake ś Z., Terech-Majewska E., Kowalska A., Małaczewska J. Supplementing the feed of pikeperch [Sander lucioperca (L.)] juveniles with MacroGard and its influence on nonspecific cellular and humoral defense mechanisms. Aquaculture Research 2008, 40:405-411.
3. Currie G.A. Activated macrophages kill tumour cells by releasing arginase. Nature 1978, 273:758-759.
4. Young S.H., Ye J., Frazer D.G., Shi X., Castranova V. Molecular mechanism of tumor necrosis factor-α production in 1→3-β-glucan (zymosan)-activated macrophages. Journal of Biological Chemistry 2001, 276:20781-20787.
5. Thompson I.J., Oyston P.C.F., Williamson D.E. Potential of the β-glucans to enhance innate resistance to biological agents. Expert Review of Anti-infective Therapy 2010, 8:339-352.
6. Volman J.J., Ramakers J.D., Plat J. Dietary modulation of immune function by β-glucans. Physiology & Behavior 2008, 94:276-284.
7. Betz B.E., Azad A.K., Morris J.D., Rajaram M.V.S., Schlesinger L.S. β-Glucans inhibit intracellular growth of Mycobacterium bovis BCG but not virulent Mycobacterium tuberculosis in human macrophages. Microbial Pathogenesis 2011, 51:233-242.
8. Selvaraj V., Sampath K., Sekar V. Administration of yeast glucan enhances survival and some non-specific and specific immune parameters in carp (Cyprinus carpio) infected with Aeromonas hydrophila. Fish & Shellfish Immunology 2005, 19:293-306.
9. Ai Q., Mai K., Zhang L., Tan B., Zhang W., Xu W., et al. Effects of dietary β-1,3 glucan on innate immune response of large yellow croaker, Pseudosciaena crocea. Fish & Shellfish Immunology 2007, 22:394-402.
10. Brown G.D., Gordon S. Immune recognition: a new receptor for [beta]-glucans. Nature 2001, 413:36-37.
11. Willment J.A., Gordon S., Brown G.D. Characterization of the human β-glucan receptor and its alternatively spliced isoforms. Journal of Biological Chemistry 2001, 276:43818-43823.
12. Taylor P.R., Tsoni S.V., Willment J.A., Dennehy K.M., Rosas M., Findon H., et al. Dectin-1 is required for [beta]-glucan recognition and control of fungal infection. Nature Immunology 2007, 8:31-38.
13. Netea M.G., Van der Graaf C., Van der Meer J.W., Kullberg B.J. Recognition of fungal pathogens by Toll-like receptors. European Journal of Clinical Microbiology & Infectious Diseases: Official Publication of the European Society of Clinical Microbiology 2004, 23:672-676.
14. Palma A.S., Feizi T., Zhang Y., Stoll M.S., Lawson A.M., Díaz-Rodríguez E., et al. Ligands for the β-glucan receptor, dectin-1, assigned using "designer" microarrays of oligosaccharide probes (neoglycolipids) generated from glucan polysaccharides. Journal of Biological Chemistry 2006, 281:5771-5779.
15. Brown G.D., Taylor P.R., Reid D.M., Willment J.A., Williams D.L., Martinez-Pomares L., et al. Dectin-1 is a major β-glucan receptor on macrophages. The Journal of Experimental Medicine 2002, 196:407-412.
16. Godfrey C., Wing C., Daniel S. The effects of β-glucan on human immune and cancer cells. Journal of Hematology & Oncology 2009, 2.
17. Sattler S., Ghadially H., Hofer E. Evolution of the C-type lectin-like receptor genes of the DECTIN-1 cluster in the NK gene complex. The Scientific World Journal 2012, 2012.
18. Irnazarow I. Genetic variability of Polish and Hungarian carp lines. Aquaculture 1995, 129:215-219.
19. Kemenade B., Groeneveld A., Rens B., Rombout J. Characterization of macrophages and neutrophilic granulocytes from the pronephros of carp (Cyprinus carpio). Journal of Experimental Biology 1994, 187:143-158.
20. Joerink M., Ribeiro C.M.S., Stet R.J.M., Hermsen T., Savelkoul H.F.J., Wiegertjes G.F. Head kidney-derived macrophages of common carp (Cyprinus carpio L.) show plasticity and functional polarization upon differential stimulation. The Journal of Immunology 2006, 177:61-69.
21. Neumann N.F., Barreda D., Belosevic M. Production of a macrophage growth factor (s) by a goldfish macrophage cell line and macrophages derived from goldfish kidney leukocytes. Developmental & Comparative Immunology 1998, 22:417-432.
22. Vera-Jiménez N.I., Pietretti D., Wiegertjes G.F., Nielsen M.E. Comparative study of β-glucan induced respiratory burst measured by nitroblue tetrazolium assay and real-time luminol-enhanced chemiluminescence assay in common carp (Cyprinus carpio L.). Fish & Shellfish Immunology 2013, 34:1216-1222.
23. Allen R.C., Stjernholm R.L., Steele R.H. Evidence for the generation of an electronic excitation state(s) in human polymorphonuclear leukocytes and its participation in bactericidal activity. Biochemical and Biophysical Research Communications 1972, 47:679-684.
24. Verho S., Järvinen S., Nikoskelainen S., Lilius E.-M. Biological effect of vaccination can be assessed directly from diluted whole blood of rainbow trout using homologous blood phagocytes as immunosensors. Fish & Shellfish Immunology 2005, 19:175-183.
25. Saeij J., Van Muiswinkel W., Groeneveld A., Wiegertjes G. Immune modulation by fish kinetoplastid parasites: a role for nitric oxide. Parasitology 2002, 124:77-86.
26. Forlenza M., Kaiser T., Savelkoul H., Wiegertjes G.F. The use of real-time quantitative PCR for the analysis of cytokine mRNA levels. Methods in Molecular Biology (Clifton, NJ) 2012, 820:7.
27. Varela M., Dios S., Novoa B., Figueras A. Characterisation, expression and ontogeny of interleukin-6 and its receptors in zebrafish (Danio rerio). Developmental & Comparative Immunology 2012, 37:97-106.
28. Henkel C.V., Dirks R.P., Jansen H.J., Forlenza M., Wiegertjes G.F., Howe K., et al. Comparison of the exomes of common carp (Cyprinus carpio) and zebrafish (Danio rerio). Zebrafish 2012, 9:59-67.
29. Nielsen H., Engelbrecht J., Brunak S., Von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Engineering 1997, 10:1-6.
30. Bryson K., McGuffin L.J., Marsden R.L., Ward J.J., Sodhi J.S., Jones D.T. Protein structure prediction servers at University College London. Nucleic Acids Research 2005, 33:W36-W38.
31. Fujiki K., Nakao M., Dixon B. Molecular cloning and characterisation of a carp (Cyprinus carpio) cytokine-like cDNA that shares sequence similarity with IL-6 subfamily cytokines CNTF, OSM and LIF. Developmental & Comparative Immunology 2003, 27:127-136.
32. Hanington P.C., Belosevic M. Interleukin-6 family cytokine M17 induces differentiation and nitric oxide response of goldfish (Carassius auratus L.) macrophages. Developmental & Comparative Immunology 2007, 31:817-829.
33. Hwang J.Y., Santos M.D., Kondo H., Hirono I., Aoki T. Identification, characterization and expression of a novel cytokine M17 homologue (MSH) in fish. Fish & Shellfish Immunology 2007, 23:1256-1265.
34. Abdelkhalek N.K., Komiya A., Kato-Unoki Y., Somamoto T., Nakao M. Molecular evidence for the existence of two distinct IL-8 lineages of teleost CXC-chemokines. Fish & Shellfish Immunology 2009, 27:763-767.
35. Huising M.O., van Schijndel J.E., Kruiswijk C.P., Nabuurs S.B., Savelkoul H.F., Flik G., et al. The presence of multiple and differentially regulated interleukin-12p40 genes in bony fishes signifies an expansion of the vertebrate heterodimeric cytokine family. Molecular Immunology 2006, 43:1519-1533.
36. Saeij J.P., Stet R.J., de Vries B.J., van Muiswinkel W.B., Wiegertjes G.F. Molecular and functional characterization of carp TNF: a link between TNF polymorphism and trypanotolerance?. Developmental & Comparative Immunology 2003, 27:29-41.
37. Stolte E.H., Savelkoul H.F., Wiegertjes G., Flik G., Lidy Verburg-van Kemenade B. Differential expression of two interferon-γ genes in common carp (Cyprinus carpio L.). Developmental & Comparative Immunology 2008, 32:1467-1481.
38. Dalmo R.A., Bogwald J. Beta-glucans as conductors of immune symphonies. Fish & Shellfish Immunology 2008, 25:384-396.
39. Jørgensen J.B., Robertsen B. Yeast β-glucan stimulates respiratory burst activity of Atlantic salmon (Salmo salar L.) macrophages. Developmental & Comparative Immunology 1995, 19:43-57.
40. Bridle A., Carter C., Morrison R., Nowak B. The effect of β-glucan administration on macrophage respiratory burst activity and Atlantic salmon, Salmo salar L., challenged with amoebic gill disease - evidence of inherent resistance. Journal of Fish Diseases 2005, 28:347-356.
41. Bagni M., Romano N., Finoia M.G., Abelli L., Scapigliati G., Tiscar P.G., et al. Short- and long-term effects of a dietary yeast β-glucan (MacroGard) and alginic acid (Ergosan) preparation on immune response in sea bass (Dicentrarchus labrax). Fish & Shellfish Immunology 2005, 18:311-325.
42. Chadzinska M., Leon-Kloosterziel K.M., Plytycz B., Lidy Verburg-van Kemenade B. Invivo kinetics of cytokine expression during peritonitis in carp: evidence for innate and alternative macrophage polarization. Developmental & Comparative Immunology 2008, 32:509-518.
43. Gopalakannan A., Arul V. Enhancement of the innate immune system and disease-resistant activity in Cyprinus carpio by oral administration of β-glucan and whole cell yeast. Aquaculture Research 2009, 41:884-892.
44. Rairakhwada D., Pal A., Bhathena Z., Sahu N., Jha A., Mukherjee S. Dietary microbial levan enhances cellular non-specific immunity and survival of common carp (Cyprinus carpio) juveniles. Fish & Shellfish Immunology 2007, 22:477-486.
45. Lin S., Pan Y., Luo L., Luo L. Effects of dietary β-1,3-glucan, chitosan or raffinose on the growth, innate immunity and resistance of koi (Cyprinus carpio koi). Fish & Shellfish Immunology 2011, 31:788-794.
46. Vera-Jimenez N., Nielsen M. Carp head kidney leukocytes display different patterns of oxygen radical production after stimulation with PAMPs and DAMPs. Molecular Immunology 2013, 55:231-236.
47. Przybylska D.A., Schmidt J.G., Vera-Jiménez N.I., Steinhagen D., Nielsen M.E. β-Glucan enriched bath directly stimulates the wound healing process incommon carp (Cyprinus carpio L.). Fish & Shellfish Immunology 2013, 35:998-1006. [available online 13 June 2013].
48. Brogden G., von Köckritz-Blickwede M., Adamek M., Reuner F., Jung-Schroers V., Naim H.Y., et al. β-Glucan protects neutrophil extracellular traps against degradation by Aeromonas hydrophila in carp (Cyprinus carpio). Fish & Shellfish Immunology 2012, 33:1060-1064.
49. Oyarbide U., Rainieri S., Pardo M. Zebrafish (Danio rerio) larvae as a system to test the efficacy of polysaccharides as immunostimulants. Zebrafish 2012, 9:74-84.
50. Falco A., Frost P., Miest J., Pionnier N., Irnazarow I., Hoole D. Reduced inflammatory response to Aeromonas salmonicida infection in common carp (Cyprinus carpio L.) fed with β-glucan supplements. Fish & Shellfish Immunology 2012, 32:1051-1057.
51. Kadowaki T., Yasui Y., Nishimiya O., Takahashi Y., Kohchi C., Soma G.-I., et al. Orally administered LPS enhance head kidney macrophage activation with down-regulation of IL-6 in common carp (Cyprinus carpio). Fish & Shellfish Immunology 2013, 34:1569-1575.
52. Huising M.O., Kruiswijk C.P., van Schijndel J.E., Savelkoul H.F., Flik G., Verburg-van Kemenade B.L. Multiple and highly divergent IL-11 genes in teleost fish. Immunogenetics 2005, 57:432-443.
53. Neben S., Turner K. The biology of interleukin 11. Stem Cells 1993, 11:156-162.
54. Engelsma M.Y., Stet R.J., Saeij J.P., Lidy Verburg-van Kemenade B. Differential expression and haplotypic variation of two interleukin-1β genes in the common carp (Cyprinus carpio L.). Cytokine 2003, 22:21-32.
55. Zelensky A.N., Gready J.E. C-type lectin-like domains in Fugu rubripes. BMC Genomics 2004, 5:51.
56. Le Cabec V., Carréno S., Moisand A., Bordier C., Maridonneau-Parini I. Complement receptor 3 (CD11b/CD18) mediates type I and type II phagocytosis during nonopsonic and opsonic phagocytosis, respectively. The Journal of Immunology 2002, 169:2003-2009.
57. Takahara K., Tokieda S., Nagaoka K., Inaba K. Efficient capture of Candida albicans and zymosan by SIGNR1 augments TLR2-dependent TNF-α production. International Immunology 2012, 24:89-96.
58. Lin A.-F., Xiang L.-X., Wang Q.-L., Dong W.-R., Gong Y.-F., Shao J.-Z. The DC-SIGN of zebrafish: insights into the existence of a CD209 homologue in a lower vertebrate and its involvement in adaptive immunity. The Journal of Immunology 2009, 183:7398-7410.
59. Esteban M., Rodriguez A., Meseguer J. Glucan receptor but not mannose receptor is involved in the phagocytosis of Saccharomyces cerevisiae by seabream (Sparus aurata L.) blood leucocytes. Fish & Shellfish Immunology 2004, 16:447.
60. Nayak D.K., Tang A., Wilson M., Miller N.W., Bengtén E. Channel catfish soluble FcμR binds conserved linear epitopes present on Cμ3 and Cμ4. Molecular Immunology 2010, 47:1306-1316.
61. Rombout J., van der Tuin S., Yang G., Schopman N., Mroczek A., Hermsen T., et al. Expression of the polymeric immunoglobulin receptor (pIgR) in mucosal tissues of common carp (Cyprinus carpio L.). Fish & Shellfish Immunology 2008, 24:620-628.
62. Tadiso T.M., Sharma A., Hordvik I. Analysis of polymeric immunoglobulin receptor- and CD300-like molecules from Atlantic salmon. Molecular Immunology 2011, 49:462-473.
63. Nakao M., Fujiki K., Kondo M., Yano T. Detection of complement receptors on head kidney phagocytes of the common carp Cyprinus carpio. Fisheries Science 2003, 69:929-935.
64. Mikrou A., Marioli D., Papanastasiou A.D., Zarkadis I.K. CR3 complement receptor: cloning and characterization in rainbow trout. Fish & Shellfish Immunology 2009, 26:19-28.
65. Kerrigan A.M., Brown G.D. C-type lectins and phagocytosis. Immunobiology 2009, 214:562-575.
66. Amiel E., Alonso A., Uematsu S., Akira S., Poynter M.E., Berwin B. Pivotal advance: Toll-like receptor regulation of scavenger receptor-A-mediated phagocytosis. Journal of Leukocyte Biology 2009, 85:595-605.
67. Murphy J.E., Tedbury P.R., Homer-Vanniasinkam S., Walker J.H., Ponnambalam S. Biochemistry and cell biology of mammalian scavenger receptors. Atherosclerosis 2005, 182:1-15.
68. Krasnov A., Koskinen H., Rexroad C., Afanasyev S., Mölsä H., Oikari A. Transcriptome responses to carbon tetrachloride and pyrene in the kidney and liver of juvenile rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 2005, 74:70-81.
69. Meng Z., Zhang X.-y., Guo J., Xiang L.-x., Shao J.-z. Scavenger receptor in fish is a lipopolysaccharide recognition molecule involved in negative regulation of NF-κB activation by competing with TNF receptor-associated factor 2 recruitment into the TNF-α signaling pathway. The Journal of Immunology 2012, 189:4024-4039.
70. Erdman L.K., Cosio G., Helmers A.J., Gowda D.C., Grinstein S., Kain K.C. CD36 and TLR interactions in inflammation and phagocytosis: implications for malaria. The Journal of Immunology 2009, 183:6452-6459.
71. Means T.K., Mylonakis E., Tampakakis E., Colvin R.A., Seung E., Puckett L., et al. Evolutionarily conserved recognition and innate immunity to fungal pathogens by the scavenger receptors SCARF1 and CD36. The Journal of Experimental Medicine 2009, 206:637-653.