Cortisol modulates the induction of inflammatory gene expression in a rainbow trout macrophage cell line

Fish and Shellfish Immunology

Volumn 30, Issue 1, 2011, Pages 215-223

  Castro, Rosario ^a,b   Zou, Jun ^a   Secombes, Christopher J ^a   Martin, Samuel A M ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b INRA Institut National de la Recherche Agronomique   (France)

Author keywords

Cortisol; Cytokines; Inflammatory genes; Macrophages

Indexed keywords

ONCORHYNCHUS MYKISS; SALMONIDAE;

EID: 78650687492     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2010.10.010     Document Type: Article

References (90)

1. Rogatsky I., Ivashkiv L.B. Glucocorticoid modulation of cytokine signalling. Tissue Antigens 2006, 68:1-12.
2. Refojo D., Liberman A.C., Holsboer F., Arzt E. Transcription factor-mediated molecular mechanisms involved in the functional cross-talk between cytokines and glucocorticoids. Immunol Cell Biol 2001, 79:385-394.
3. Calcagni E., Elenkov I. Stress system activity, innate and T helper cytokines, and susceptibility to immune-related diseases. Ann NY Acad Sci 2006, 1069:62-76.
4. Elenkov I.J. Glucocorticoids and the Th1/Th2 balance. Ann NY Acad Sci 2004, 1024:138-146.
5. Elenkov I.J., Chrousos G.P. Stress hormones, Th1/Th2 patterns, pro/anti-inflammatory cytokines and susceptibility to disease. Trends Endocrinol Metab 1999, 10:359-368.
6. Calduch-Giner J.A., Sitja-Bobadilla A., Alvarez-Pellitero P., Perez-Sanchez J. Growth hormone as an in vitro phagocyte-activating factor in the gilthead sea bream (Sparus aurata). Cell Tiss Res 1997, 287:535-540.
7. Harris J., Bird D.J. Modulation of the fish immune system by hormones. Vet Immunol Immunopathol 2000, 77:163-176.
8. Weyts F.A., Cohen N., Flik G., Verburg-van Kemenade B.M. Interactions between the immune and endocrine system and the hypothalamo-pituitary-interrenal axis in fish. Fish Shellfish Immunol 1999, 9:1-20.
9. Yada T., Muto K., Azuma T., Hyodo S., Schreck C.B. Cortisol stimulates growth hormone gene expression in rainbow trout leucocytes in vitro. Gen Comp Endocrinol 2005, 142:248-255.
10. Yada T., Nakanishi T. Interaction between endocrine and immune systems in fish. Int Rev Cytol 2002, 220:35-92.
11. 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. J Mol Endocrinol 2003, 31:141-156.
12. Aluru N., Vijayan M.M. Stress transcriptomics in fish: a role for genomic cortisol signalling. Gen Comp Endocrinol 2009, 164:142-150.
13. Jiang J.Q., Young G., Kobayashi T., Nagahama Y. Eel (Anguilla japonica) testis 11 beta-hydrolase gene is expressed in interrenal tissue and its product lacks aldosterone synthesizing activity. Mol Cell Endocrinol 1998, 146:207-211.
14. Laing K.J., Holland J., Bonilla S., Cunningham C., Secombes C.J. Cloning and sequencing of caspase 6 in rainbow trout, Oncorhynchus mykiss, and analysis of its expression under conditions known to induce apoptosis. Dev Comp Immunol 2001, 25:303-312.
15. Saha N.R., Usami T., Suzuki Y. A double staining flow cytometric assay for the detection of steroid induced apoptotic leucocytes in common carp (Cyprinus carpio). Dev Comp Immunol 2003, 27:351-363.
16. Engelsma M.Y., Huising M.O., Van Muiswinkel W., Flik G., Kwang J., Savelkoul H.F., et al. Neuroendocrine-immune interactions in fish: a role for interleukin-1. Vet Immunol Immunopathol 2002, 87:467-479.
17. Kassel O., Herrlich P. Crosstalk between the glucocorticoid receptor and other transcription factors: molecular aspects. Mol Cell Endocrinol 2007, 275:13-29.
18. Schoneveld O.J., Gaemers I.C., Lamers W.H. Mechanisms of glucocorticoid signalling. Biochim Biophys Acta 2004, 1680:114-128.
19. Barnes P.J. Corticosteroid effects on cell signalling. Eur Respir J 2006, 27:413-426.
20. Bury N.R., Sturm A. Evolution of the corticosteroid receptor signalling pathway in fish. Gen Comp Endocrinol 2007, 153:47-56.
21. Greenwood A.K., Butler P.C., White R.B., DeMarco U., Pearce D., Fernald R.D. Multiple corticosteroid receptors in a teleost fish: distinct sequences, expression patterns, and transcriptional activities. Endocrinology 2003, 144:4226-4236.
22. Stolte E.H., Nabuurs S.B., Bury N.R., Sturm A., Flik G., Savelkoul H.F.J., et al. Stress and innate immunity in carp: corticosteroid receptors and pro-inflammatory cytokines. Mol Immunol 2008, 46:70-79.
23. Stolte E.H., van Kemenade B.M., Savelkoul H.F., Flik G. Evolution of glucocorticoid receptors with different glucocorticoid sensitivity. J Endocrinol 2006, 190:17-28.
24. Amsterdam A., Tajima K., Sasson R. Cell-specific regulation of apoptosis by glucocorticoids: implication to their anti-inflammatory action. Biochem Pharmacol 2002, 64:843-850.
25. Ehrchen J., Steinmüller L., Barczyk K., Tenbrock K., Nacken W., Eisenacher M., et al. Glucocorticoids induce differentiation of a specifically activated, anti-inflammatory subtype of human monocytes. Blood 2007, 109:1265-1274.
26. Yona S., Gordon S. Glucocorticoids turn the monocyte switch. Immunol Cell Biol 2007, 85:81-82.
27. Anderson C.F., Mosser D.M. A novel phenotype for an activated macrophage: the type 2 activated macrophage. J Leukoc Biol 2002, 72:101-106.
28. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003, 3:23-35.
29. Mosser D.M. The many faces of macrophage activation. J Leukoc Biol 2003, 73:209-212.
30. Hu X., Chakravarty S.D., Ivashkiv L.B. Regulation of interferon and toll-like receptor signalling during macrophage activation by opposing feedforward and feedback inhibition mechanisms. Immunological Rev 2008, 226:41-56.
31. Ganassin R.C., Bols N.C. Development of a monocyte/macrophage-like cell line, RTS11, from rainbow trout spleen. Fish Shellfish Immunol 1998, 8:457-476.
32. Martin S.A.M., Zou J., Houlihan D.F., Secombes C.J. Directional responses following recombinant cytokine stimulation of rainbow trout (Oncorhynchus mykiss) RTS-11 macrophage cells as revealed by transcriptome profiling. BMC Genomics 2007, 8:150.
33. Skinner L.A., LaPatra S.E., Adams A., Thompson K.D., Balfry S.K., McKinley R.S., et al. Supra-physiological levels of cortisol suppress lysozyme but not the antibody response in Atlantic salmon, Salmo salar L., following vaccine injection. Aquaculture 2010, 300:223-230.
34. Zou J., Grabowski P.S., Cunningham C., Secombes C.J. Molecular cloning of interleukin 1beta from rainbow trout Oncorhynchus mykiss reveals no evidence of an ice cut site. Cytokine 1999, 11:552-560.
35. Zou J., Carrington A., Collet B., Dijkstra J.M., Yoshiura Y., Bols N., et al. Identification and bioactivities of IFN-γ in rainbow trout Oncorhynchus mykiss: the first Th1-type cytokine characterized functionally in fish. J Immunol 2005, 175:2484-2494.
36. Zou J., Tafalla C., Truckle J., Secombes C.J. Identification of a second group of type I IFNs in fish sheds light on IFN evolution in vertebrates. J Immunol 2007, 179:3859-3871.
37. Hong S., Zou J., Crampe M., Peddie S., Scapigliati G., Bols N., et al. The production and bioactivity of rainbow trout (Oncorhynchus mykiss) recombinant IL-1 beta. Vet Immunol Immunopathol 2001, 81:1-14.
38. Iliev D.B., Liarte C.Q., MacKenzie S., Goetz F.W. Activation of rainbow trout (Oncorhynchus mykiss) mononuclear phagocytes by different pathogen associated molecular patterns (PAMP) bearing agents. Mol Immunol 2005, 42:1215-1223.
39. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45.
40. Brodsky I.E., Medzhitov R. Targeting of immune signaling networks by bacterial pathogens. Nat Cell Biol 2009, 11:521-526.
41. Dinarello C.A. Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol 2009, 27:519-550.
42. Bird S., Zou J., Wang T., Munday B., Cunningham C., Secombes C.J. Evolution of interleukin-1beta. Cytokine Growth Factor Rev 2002, 13:483-502.
43. Baud V., Karin M. Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol 2001, 11:372-377.
44. Feldmann M., Maini R.N., Bondeson J., Taylor P., Foxwell B.M., Brennan F.M. Cytokine blockade in rheumatoid arthritis. Adv Exp Med Biol 2001, 490:119-127.
45. Vane J.R., Bakle Y.S., Botting R.M. Cyclooxygenases 1 and 2. Annu Rev Pharmacol 1998, 38:97-120.
46. Secombes C.J., Wang T., Hong S., Peddie S., Crampe M., Laing K.J., et al. Cytokines and innate immunity of fish. Dev Comp Immunol 2001, 25:713-723.
47. Kamimura D., Ishihara K., Hirano T. IL-6 signal transduction and its physiological roles: the signal orchestration model. Rev Physiol Biochem Pharmacol 2003, 149:1-38.
48. Kaplanski G., Marin V., Montero-Julian F., Mantovani A., Farnarier C. IL-6: a regulator of the transition from neutrophil to monocyte recruitment during inflammation. Trends Immunol 2003, 24:25-29.
49. Bird S., Zou J., Savan R., Kono T., Sakai M., Woo J., et al. Characterization and expression analysis of an interleukin 6 homologue in the Japanese pufferfish, Fugu rubripes. Dev Comp Immunol 2005, 29:775-789.
50. Iliev D.B., Castellana B., Mackenzie S., Planas J.V., Goetz F.W. Cloning and expression analysis of an IL-6 homolog in rainbow trout (Oncorhynchus mykiss). Mol Immunol 2007, 44:1803-1807.
51. Harum N.O., Zou J., Zhang Y.A., Nie P., Secombes C.J. The biological effects of rainbow trout (Oncorhynchus mykiss) recombinant interleukin-8. Dev Comp Immunol 2008, 32:673-681.
52. Montero J., Coll J., Sevilla N., Cuesta A., Bols N.C., Tafalla C. Interleukin 8 and CK-6 chemokines specifically attract rainbow trout (Oncorhynchus mykiss) RTS11 monocyte-macrophage cells and have variable effects on their immune functions. Dev Comp Immunol 2008, 32:1374-1384.
53. Wells C.A., Ravasi T., Hume D.A. Inflammation suppressor genes: please switch out all the lights. J Leukoc Biol 2005, 78:9-13.
54. Letterio J.J., Roberts A.B. Transforming growth factor-betaI-deficient mice: identification of isoform-specific activities in vivo. J Leuk Biol 1996, 59:769-774.
55. Lotz M., Seth P. TGF beta and HIV infection. Ann NY Acad Sci 1993, 685:501-511.
56. Cools N., Ponsaerts P., Van Tendeloo V.F., Berneman Z.N. Regulatory T cells and human disease. Clin Dev Immunol 2007, 89195.
57. Moore K.W., de Waal Makefyt R., Coffman R.L., O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001, 19:683-765.
58. Bird S., Zou J., Secombes C.J. Advances in fish cytokine biology give clues to the evolution of a complex network. Curr Pharm Des 2006, 12:3051-3069.
59. Pinto R.D., Nascimento D.S., Reis M.I., do Vale A., Dos Santos N.M. Molecular characterization, 3D modelling and expression analysis of sea bass (Dicentrarchus labrax L.) interleukin-10. Mol Immunol 2007, 44:2056-2065.
60. Seppola M., Larsen A.N., Steiro K., Robertsen B., Jensen I. Characterisation and expression analysis of the interleukin genes, IL-1beta, IL-8 and IL-10 in Atlantic cod (Gadus morhua L). Mol Immunol 2008, 45:887-897.
61. Haque S.J., Harbor P.C., Williams B.R. Identification of critical residues required for suppressor of cytokine signalling-specific regulation of interleukin-4 signalling. J Biol Chem 2000, 275:26500-26506.
62. Murray P.J. The JAK-STAT signalling pathway: input and output integration. J Immunol 2007, 178:2623-2629.
63. Wang T., Secombes C.J. Rainbow trout suppressor of cytokine signalling (SOCS)-1, 2 and 3: molecular identification, expression and modulation. Mol Immunol 2008, 45:1449-1457.
64. Castillo J., Teles M., Mackenzie S., Tort L. Stress-related hormones modulate cytokine expression in the head kidney of gilthead seabream (Sparus aurata). Fish Shellfish Imm 2009, 27:493-499.
65. Pagniello K.B., Bols N.C., Lee L.E. Effect of corticosteroids on viability and proliferation of the rainbow trout monocyte/macrophage cell line, RTS11. Fish Shellfish Immunol 2002, 13:199-214.
66. Ellsaesser C.F., Clem L.W. Cortical-induced hematologic and immunologic changes in channel catfish (Ictalurus punctatus). Comp Biochem Physiol 1987, 87A:405-408.
67. Huising M.O., Guichelaar T., Hoek C., Verburg-van Kemenade B.M., Flik G., Savelkoul H.F., et al. Increased efficacy of immersion vaccination in fish with hyperosmotic pretreatment. Vaccine 2003, 21:4178-4193.
68. Weyts F.A., Flik G., Verburg-van Kemenade B.M. Cortisol inhibits apoptosis in carp neutrophilic granulocytes. Dev Comp Immunol 1998, 22:563-572.
69. Weyts F.A., Flik G., Rombout J.H., Verburg-van Kemenade B.M. Cortisol induces apoptosis in activated B cells, not in other lymphoid cells of the common carp, Cyprinus carpio L. Dev Comp Immunol 1998, 22:551-562.
70. Yada T., Misumi I., Muto K., Azuma T., Schreck C.B. Effects of prolactin and growth hormone on proliferation and survival of cultured trout leucocytes. Gen Comp Endocrinol 2004, 136:298-306.
71. Peterson C.L., Laniel M.A. Histones and histone modifications. Curr Biol 2004, 14:R546-R551.
72. Ito K., Barnes P.J., Adcock I.M. Glucocorticoid receptor recruitment of histone deacetylase 2 inhibits IL-1β-induced histone H4 acetylation on lysines 8 and 12. Mol Cell Biol 2000, 20:6891-6903.
73. Mozo L., Suarez A., Gutierrez C. Glucocorticoids up-regulate constitutive interleukin-10 production by human monocytes. Clin Exp Allergy 2004, 34:406-412.
74. Unterberger C., Staples K.J., Smallie T., Williams L., Foxwell B., Schaefer A., et al. Role of STAT3 in glucocorticoid-induced expression of the human IL-10 gene. Mol Immunol 2008, 45:3230-3237.
75. Wissing S., Van Heerde E.C., Van Der Burg B., Van Der Saag P.T. A dual mechanism mediates repression of NF-kappaB activity by glucocorticoids. Mol Endocrinol 1998, 12:355-363.
76. Clark A.R. MAP kinase phosphatase 1: a novel mediator of biological effects of glucocorticoids?. J Endocrinol 2003, 178:5-12.
77. Mittelstadt P.R., Ashwell J.D. Inhibition of AP-1 by the glucocorticoid-inducible protein GILZ. J Biol Chem 2001, 276:29603-29610.
78. Scheinman R.I., Cogswell P.C., Lofquist A.K., Baldwin A.S. Role of transcriptional activation of IkB in mediation of immunosuppression by glucocorticoids. Science 1995, 270:283-286.
79. Dean J.L., Sully G., Clark A.R., Saklatvala J. The involvement of AU-rich element-binding proteins in p38 mitogen-activated protein kinase pathway-mediated mRNA stabilization. Cell Signal 2004, 16:1113-1121.
80. Lasa M., Brook M., Saklatvala J., Clark A.R. Dexamethasone destabilizes cyclooxygenase 2 mRNA by inhibiting mitogen-activated protein kinase p38. Mol Cell Biol 2001, 21:771-780.
81. Pinto R.A., Arredondo S.M., Bono M.R., Gaggero A.A., Diaz P.V. T helper 1/T helper 2 cytokine imbalance in respiratory syncytial virus infection is associated with increased endogenous plasma cortisol. Pediatrics 2006, 117:878-886.
82. Hu X., Li W.P., Meng C., Ivashkiv L.B. Inhibition of IFN-gamma signalling by glucocorticoids. J Immunol 2003, 170:4833-4839.
83. Haffner M.C., Jurgeit A., Berlato C., Geley S., Parajuli N., Yoshimura A., et al. Interaction and functional interference of glucocorticoid receptor and SOCS1. J Biol Chem 2008, 283:22089-22096.
84. De Witte-Orr S.J., Leong J.A., Bols N.C. Induction of antiviral genes, Mx and vig-1, by dsRNA and Chum salmon reovirus in rainbow trout monocyte/macrophage and fibroblast cell lines. Fish Shellfish Immunol 2007, 23:670-682.
85. Goetz F.W., Iliev D.B., McCauley L.A., Liarte C.Q., Tort L.B., Planas J.V., et al. Analysis of genes isolated from lipopolysaccharide-stimulated rainbow trout (Oncorhynchus mykiss) macrophages. Mol Immunol 2004, 41:1199-1210.
86. Castellana B., Iliev D.B., Sepulcre M.P., MacKenzie S., Goetz F.W., Mulero V., et al. Molecular characterization of interleukin-6 in the gilthead seabream (Sparus aurata). Mol Immunol 2008, 45:3363-3370.
87. MacKenzie S., Iliev D., Liarte C., Koskinen H., Planas J.V., Goetz F.W., et al. Transcriptional analysis of LPS-stimulated activation of trout (Oncorhynchus mykiss) monocyte/macrophage cells in primary culture treated with cortisol. Mol Immunol 2006, 43:1340-1348.
88. Medzhitov R., Horng T. Transcriptional control of the inflammatory response. Nat Rev Immunol 2009, 9:692-703.
89. Varga G., Ehrchen J., Tsianakas A., Tenbrock K., Rattenholl A., Seeliger S., et al. Glucocorticoids induce an activated, anti-inflammatory monocyte subset in mice that resembles myeloid-derived suppressor cells. J Leukoc Biol 2008, 84:644-650.
90. Gabay C. Interleukin-6 and chronic inflammation. Arthritis Res Ther 2006, 8(Suppl. 2). S3.