The immune response differentially regulates Hsp70 and glucocorticoid receptor expression in vitro and in vivo in common carp (Cyprinus carpio L.)

Fish and Shellfish Immunology

Volumn 27, Issue 1, 2009, Pages 9-16

  Stolte, Ellen H ^a,b   Chadzinska, Magdalena ^a,c   Przybylska, Dominika ^a,c   Flik, Gert ^b   Savelkoul, Huub F J ^a   Verburg van Kemenade, B M Lidy ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^c JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

Common carp; Glucocorticoid receptor; Heat shock protein; Immune modulation; Teleost

Indexed keywords

CYPRINIDAE; CYPRINUS CARPIO; TELEOSTEI;

EID: 67349217388     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2008.11.003     Document Type: Article

References (45)

1. Elenkov I.J., and Chrousos G.P. Stress system - organization, physiology and immunoregulation. Neuroimmunomodulation 13 5-6 (2006) 257-267
2. Webster J.I., and Sternberg E.M. Role of the hypothalamic-pituitary-adrenal axis, glucocorticoids and glucocorticoid receptors in toxic sequelae of exposure to bacterial and viral products. Journal of Endocrinology 181 2 (2004) 207-221
3. Pratt W.B., and Toft D.O. Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Experimental Biology and Medicine (Maywood) 228 2 (2003) 111-133
4. Rhen T., and Cidlowski J.A. Antiinflammatory action of glucocorticoids - new mechanisms for old drugs. New England Journal of Medicine 353 16 (2005) 1711-1723
5. Ritossa F. New puffing pattern induced by temperature shock and Dnp in Drosophila. Experientia 18 12 (1962) 571-573
6. Young J.C., Barral J.M., and Hartl F.U. More than folding: localized functions of cytosolic chaperones. Trends in Biochemical Sciences 28 10 (2003) 541-547
7. Liberek K., Lewandowska A., and Zietkiewicz S. Chaperones in control of protein disaggregation. EMBO Journal 27 2 (2008) 328-335
8. Eisenberg E., and Greene L.E. Multiple roles of auxilin and Hsc70 in clathrin-mediated endocytosis. Traffic 8 6 (2007) 640-646
9. Suganuma T., Irie K., Fujii E., Yoshioka T., and Muraki T. Effect of heat stress on lipopolysaccharide-induced vascular permeability change in mice. Journal of Pharmacology and Experimental Therapeutics 303 2 (2002) 656-663
10. Shi Y., Tu Z., Tang D., Zhang H., Liu M., Wang K., et al. The inhibition of LPS-induced production of inflammatory cytokines by HSP70 involves inactivation of the NF-kappaB pathway but not the MAPK pathways. Shock 26 3 (2006) 277-284
11. Wang Y., Li C.L., Wang X.Y., Zhang J.S., and Zhang Z.L. Heat shock response down-regulates IL-18 expression in the murine macrophage cell line, RAW264.7. Chinese Science Bulletin 48 8 (2003) 780-785
12. Chen D.C., Pan J.Q., Du B., and Sun D.X. Induction of the heat shock response in vivo inhibits NF-kappa B activity and protects murine liver from endotoxemia-induced injury. Journal of Clinical Immunology 25 5 (2005) 452-461
13. Wang X., Zou Y., Wang Y., Li C., and Chang Z. Differential regulation of interleukin-12 and interleukin-10 by heat shock response in murine peritoneal macrophages. Biochemical and Biophysical Research Communications 287 5 (2001) 1041-1044
14. Calderwood S.K., Mambula S.S., Gray P.J., and Therlault J.R. Extracellular heat shock proteins in cell signaling. FEBS Letters 581 19 (2007) 3689-3694
15. Chase M.A., Wheeler D.S., Lierl K.M., Hughes V.S., Wong H.R., and Page K. Hsp72 induces inflammation and regulates cytokine production in airway epithelium through a TLR4- and NF-kappa B-dependent mechanism. Journal of Immunology 179 9 (2007) 6318-6324
16. Doz E., Noulin N., Boichbt E., Guénon I., Fick L., Le Bert M., et al. Cigarette smoke-induced pulmonary inflammation is TLR4/MyD88 and IL-1R1/MyD88 signaling dependent. Journal of Immunology 180 2 (2008) 1169-1178
17. Satoh M., Shimoda Y., Maesawa C., Akatsu T., Ishikawa Y., Minami Y., et al. Activated toll-like receptor 4 in monocytes is associated with heart failure after acute myocardial infarction. International Journal of Cardiology 109 2 (2006) 226-234
18. Vega V.L., Rodriguez-Silva M., Frey T., Gehrmann M., Diaz J.C., Steinem C., et al. Hsp70 translocates into the plasma membrane after stress and is released into the extracellular environment in a membrane-associated form that activates macrophages. Journal of Immunology 180 6 (2008) 4299-4307
19. Elsner L., Muppala V., Gehrmann M., Lozano J., Malzahn D., Bickeböller H., et al. The heat shock protein HSP70 promotes mouse NK cell activity against tumors that express inducible NKG2D ligands. Journal of Immunology 179 8 (2007) 5523-5533
20. Stolte E.H., van Kemenade B.M., Savelkoul H.F., and Flik G. Evolution of glucocorticoid receptors with different glucocorticoid sensitivity. Journal of Endocrinology 190 1 (2006) 17-28
21. Basu N., Kennedy C.J., and Iwama G.K. The effects of stress on the association between hsp70 and the glucocorticoid receptor in rainbow trout. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 134 3 (2003) 655-663
22. Stolte E.H., de Mazon A.F., Leon-Koosterziel K.M., Jesiak M., Bury N.R., Sturm A., et al. Corticosteroid receptors involved in stress regulation in common carp, Cyprinus carpio. Journal of Endocrinology 198 2 (2008) 403-417
23. Irnazarow I. Genetic variabilityof Polish and Hungarian carp lines. Aquaculture 129 (1995) 215-219
24. Chadzinska M., Leon-Kloosterziel K.M., Plytycz B., and Lidy Verburg-van Kemenade B.M. In vivo kinetics of cytokine expression during peritonitis in carp: evidence for innate and alternative macrophage polarization. Developmental and Comparative Immunology 32 5 (2008) 509-518
25. Steinhagen D., Kruse P., and Korting W. The parasitemia of cloned Trypanoplasma borreli Laveran and Mesnil, 1901, in laboratory-infected common carp (Cyprinus carpio L. Journal of Parasitology 75 5 (1989) 685-689
26. Kemenade B., Groeneveld A., Rens B., and Rombout J. Characterization of macrophages and neutrophilic granulocytes from the pronephros of carp (Cyprinus carpio). Journal of Experimental Biology 187 1 (1994) 143-158
27. Stolte E.H., Nabuurs S.B., Bury N.R., Sturm A., Flik G., Savelkoul H.F., et al. Stress and innate immunity in carp: corticosteroid receptors and pro-inflammatory cytokines. Molecular Immunology 46 1 (2008) 70-79
28. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29 9 (2001) e45
29. Munck A., Guyre P.M., and Holbrook N.J. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocrine Reviews 5 1 (1984) 25-44
30. Bury N.R., Sturm A., Le Rouzic P., Lethimonier C., Ducouret B., Guiguen Y., et al. Evidence for two distinct functional glucocorticoid receptors in teleost fish. Journal of Molecular Endocrinology 31 1 (2003) 141-156
31. Barish G.D., Downes M., Alaynick W.A., Yu R.T., Ocampo C.B., Bookout A.L., et al. A nuclear receptor atlas: macrophage activation. Molecular Endocrinology 19 10 (2005) 2466-2477
32. Chadzinska M., Baginski P., Kolaczkowska E., Savelkoul H.F., and Lidy Verburg-van Kemenade B.M. Expression profiles of matrix metalloproteinase 9 in teleost fish provide evidence for its active role in initiation and resolution of inflammation. Immunology 125 4 (2008) 601-610
33. Gallo V.P., and Civinini A. Survey of the adrenal homolog in teleosts. International Review of Cytology 230 (2003) 89-187
34. Acerete L., Balasch J.C., Castellana B., Redruello B., Roher N., Canario A.V., et al. Cloning of the glucocorticoid receptor (GR) in gilthead seabream (Sparus aurata). Differential expression of GR and immune genes in gilthead seabream after an immune challenge. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 148 1 (2007) 32-43
35. Scislowska-Czarnecka A., Chadzinska M., Pierzchala-Koziec K., and Plytycz B. Long-lasting effects of social stress on peritoneal inflammation in some strains of mice. Folia Biologica-Krakow 52 1-2 (2004) 97-104
36. Basu N., Nakano T., Grau E.G., and Iwama G.K. The effects of cortisol on heat shock protein 70 levels in two fish species. General and Comparative Endocrinology 124 1 (2001) 97-105
37. Vijayan M.M., Pereira C., Forsyth R.B., Kennedy C.J., and Iwama G.K. Handling stress does not affect the expression of hepatic heat shock protein 70 and conjugation enzymes in rainbow trout treated with beta-naphthoflavone. Life Sciences 61 2 (1997) 117-127
38. Washburn B.S., Moreland J.J., Slaughter A.M., Werner I., Hinton D.E., and Sanders B.M. Effects of handling on heat shock protein expression in rainbow trout (Oncorhynchus mykiss). Environmental Toxicology and Chemistry 21 3 (2002) 557-560
39. Hosoya S., Johnson S.C., Iwama G.K., Gamperl A.K., and Afonso L.O.B. Changes in free and total plasma cortisol levels in juvenile haddock (Melanogrammus aeglefinus) exposed to long-term handling stress. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 146 1 (2007) 78-86
40. Vijayan M.M., Raptis S., and Sathiyaa R. Cortisol treatment affects glucocorticoid receptor and glucocorticoid-responsive genes in the liver of rainbow trout. General and Comparative Endocrinology 132 2 (2003) 256-263
41. Weyts F.A., Flik G., Rombout J.H., and Verburg-van Kemenade B.M. Cortisol induces apoptosis in activated B cells, not in other lymphoid cells of the common carp, Cyprinus carpio L. Developmental and Comparative Immunology 22 5-6 (1998) 551-562
42. Weyts F.A., Flik G., and Verburg-van Kemenade B.M. Cortisol inhibits apoptosis in carp neutrophilic granulocytes. Developmental and Comparative Immunology 22 5-6 (1998) 563-572
43. Joerink M., Forlenza M., Ribeiro C.M.S., de Vries B.J., Savelkoul H.F.J., and Wiegertjes G.F. Differential macrophage polarisation during parasitic infections in common carp (Cyprinus carpio L.). Fish & Shellfish Immunology 21 5 (2006) 561-571
44. Saeij J.P., de Vries B.J., and Wiegertjes G.F. The immune response of carp to Trypanoplasma borreli: kinetics of immune gene expression and polyclonal lymphocyte activation. Developmental and Comparative Immunology 27 10 (2003) 859-874
45. Forlenza M., Scharsack J.P., Kachamakova N.M., Taverne-Thiele A.J., Rombout J.H., and Wiegertjes G.F. Differential contribution of neutrophilic granulocytes and macrophages to nitrosative stress in a host-parasite animal model. Molecular Immunology 45 11 (2008) 3178-3189