Interleukin gene expression is strongly modulated at the local level in a fish-parasite model

Fish and Shellfish Immunology

Volumn 37, Issue 2, 2014, Pages 201-208

  Pérez Cordón, Gregorio ^a   Estensoro, Itziar ^a   Benedito Palos, Laura ^a   Calduch Giner, Josep Alvar ^a   Sitjà Bobadilla, Ariadna ^a   Pérez Sánchez, Jaume ^a  

^a CSIC Instituto de Acuicultura de Torre de la Sal IATS   (Spain)

Author keywords

Cytokines; Enteromyxum leei; Intestine; Myxozoa; Sparus aurata

Indexed keywords

FISH PROTEIN; INTERLEUKIN DERIVATIVE;

ANIMAL; ANIMAL PARASITOSIS; ANTIBODY SPECIFICITY; DNA SEQUENCE; FISH DISEASE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; MYXOZOA; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SEA BREAM; VETERINARY;

ANIMALS; FISH DISEASES; FISH PROTEINS; GENE EXPRESSION REGULATION; INTERLEUKINS; MOLECULAR SEQUENCE DATA; MYXOZOA; ORGAN SPECIFICITY; PARASITIC DISEASES, ANIMAL; REAL-TIME POLYMERASE CHAIN REACTION; SEA BREAM; SEQUENCE ANALYSIS, DNA;

EID: 84894676355     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2014.01.022     Document Type: Article

References (82)

1. APROMAR La Acuicultura Marina en España 2012, http://www.apromar.es/informes.asp.
2. Segner H., Sundh H., Buchmann K., Douxfils J., Sundell K., Mathieu C., et al. Health of farmed fish: its relation to fish welfare and its utility as welfare indicator. Fish Physiol Biochem 2012, 38:85-105.
3. Pulkkinen K., Suomalainen L.R., Read A.F., Ebert D., Rintamaki P., Valtonen E.T. Intensive fish farming and the evolution of pathogen virulence: the case of columnaris disease in Finland. Proc R Soc B 2010, 277:593-600.
4. Golomazou E., Karagouni E., Athanassopoulou F. The most important myxosporean parasite species affecting cultured Mediterranean fish. JHell Vet Med Soc 2004, 55:342-352.
5. Palenzuela O. Myxozoan infections in Mediterranean mariculture. Parassitologia 2006, 48:27-29.
6. Sitjà-Bobadilla A., Palenzuela O. Enteromyxum species. Fish parasites: pathology and protection 2009, 163-176. CAB International, Oxfordshire, UK. P.T.K. Woo, K. Buchmann (Eds.).
7. Chabalgoity J.A., Baz A., Rial A., Grille S. The relevance of cytokines for development of protective immunity and rational design of vaccines. Cytokine Growth Factor Rev 2007, 18:195-207.
8. Gery I., Gershon R.K., Waksman B.H. Potentiation of T-lymphocyte response to mitogens 1. The responding cell. JExp Med 1972, 136:128-142.
9. Mulero V., García Ayala A., Meseguer J. What can we learn from fish? An evolutionary perspective of pro-inflammatory cytokines. Inmunología 2005, 24:17-22.
10. Castro R., Bernard D., Lefranc M.P., Six A., Benmansour A., Boudinot R. Tcell diversity and TcR repertoires in teleost fish. Fish Shellfish Immunol 2011, 31:644-654.
11. Wang T., Secombes C.J. The cytokine networks of adaptive immunity in fish. Fish Shellfish Immunol 2013, 35:1703-1718.
12. Secombes C.J., Wang T., Bird S. The interleukins of fish. Dev Comp Immunol 2011, 35:1336-1345.
13. Kono T., Takayama H., Nagamine R., Korenaga H., Sakai M. Establishment of a multiplex RT-PCR assay for the rapid detection of fish cytokines. Vet Immunol Immunopathol 2013, 151:90-101.
14. Pereiro P., Balseiro P., Romero A., Dios S., Forn-Cuni G., Fuste B., et al. High-throughput sequence analysis of turbot (Scophthalmus maximus) transcriptome using 454-pyrosequencing for the discovery of antiviral immune genes. PLoS One 2012, 7.
15. Wang T.H., Kono T., Monte M.M., Kuse H., Costa M.M., Korenaga H., et al. Identification of IL-34 in teleost fish: differential expression of rainbow trout IL-34, MCSF1 and MCSF2, ligands of the MCSF receptor. Mol Immunol 2013, 53:398-409.
16. Estensoro I., Redondo M.J., Álvarez-Pellitero P., Sitjà-Bobadilla A. Novel horizontal transmission route for Enteromyxum leei (Myxozoa) by anal intubation of gilthead sea bream Sparus aurata. Dis Aquat Org 2010, 92:51-58.
17. Álvarez-Pellitero P., Palenzuela O., Sitjà-Bobadilla A. Histopathology and cellular response in Enteromyxum leei (Myxozoa) infections of Diplodus puntazzo (Teleostei). Parasitol Int 2008, 57:110-120.
18. -δδCT method. Methods 2001, 25:402-408.
19. Sitjà-Bobadilla A. Can Myxosporean parasites compromise fish and amphibian reproduction?. Proc R Soc B 2009, 276:2861-2870.
20. Rigos G., Katharios P. Pathological obstacles of newly-introduced fish species in Mediterranean mariculture: a review. Rev Fish Biol Fish 2010, 20:47-70.
21. Sitjà-Bobadilla A. Fish immune response to Myxozoan parasites. Parasite 2008, 15:420-425.
22. Downs C.J., Brown J.L., Wone B., Donovan E.R., Hunter K., Hayes J.P. Selection for increased mass-independent maximal metabolic rate suppresses innate but not adaptive immune function. Proc R Soc B 2013, 280. 10.1098/rspb.2012.2636.
23. Scharsack J.P., Koch K., Hammerschmidt K. Who is in control of the stickleback immune system: interactions between Schistocephalus solidus and its specific vertebrate host. Proc R Soc B 2007, 274:3151-3158.
24. Best A., Long G., White A., Boots M. The implications of immunopathology for parasite evolution. Proc R Soc B 2012, 279:3234-3240.
25. Kim D.H., Austin B. Cytokine expression in leucocytes and gut cells of rainbow trout, Oncorhynchus mykiss Walbaum, induced by probiotics. Vet Immunol Immunopathol 2006, 114:297-304.
26. Patel N., Kreider T., Urban, Gause W.C. Characterisation of effector mechanisms at the host: parasite interface during the immune response to tissue-dwelling intestinal nematode parasites. Int J Parasitol 2009, 39:13-21.
27. Montero D., Mathlouthi F., Tort L., Afonso J.M., Torrecillas S., Fernández-Vaquero A., et al. Replacement of dietary fish oil by vegetable oils affects humoral immunity and expression of pro-inflammatory cytokines genes in gilthead sea bream Sparus aurata. Fish Shellfish Immunol 2010, 29:1073-1081.
28. Domínguez B., Pardo B.G., Noia M., Millan A., Gómez-Tato A., Martínez P., et al. Microarray analysis of the inflammatory and immune responses in head kidney turbot leucocytes treated with resveratrol. Int Immunopharmacol 2013, 15:588-596.
29. Uran P.A., Goncalves A.A., Taverne-Thiele J.J., Schrama J.W., Verreth J.A.J., Rombout J.H.W.M. Soybean meal induces intestinal inflammation in common carp (Cyprinus carpio L.). Fish Shellfish Immunol 2008, 25:751-760.
30. Sepulcre M.P., Saffopoulou E., Kotoulas G., Meseguer J., Mulero V. Vibrio anguillarum evades the immune response of the bony fish sea bass (Dicentrarchus labrax L.) through the inhibition of leukocyte respiratory burst and down-regulation of apoptotic caspases. Mol Immunol 2007, 44:3751-3757.
31. Chettri J.K., Kuhn J.A., Jaafar R.M., Kania P.W., Møller O.S., Buchmann K. Epidermal response of rainbow trout to Ichthyobodo necator: immunohistochemical and gene expression studies indicate a Th1-/Th2-like switch. JFish Dis 2013, 10.1111/jfd.12169.
32. Pellizzari C., Krasnov A., Afanasyev S., Vitulo N., Franch R., Pegolo S., et al. High mortality of juvenile gilthead sea bream (Sparus aurata) from photobacteriosis is associated with alternative macrophage activation and anti-inflammatory response: results of gene expression profiling of early responses in the head kidney. Fish Shellfish Immunol 2013, 34:1269-1278.
33. Becknell B., Caligiuri M.A. Interleukin-2, interleukin-15, and their roles in human natural killer cells. Advances in immunology 2005, vol. 86:209-239. Elsevier Academic Press Inc., San Diego.
34. Paul S.R., Bennett F., Calvetti J.A., Kelleher K., Wood C.R., Ohara R.M., et al. Molecular-cloning of a cDNA-encoding interleukin-11, a stromal cell-derived lymphopoietic and hematopoietic cytokine. Proc Natl Acad Sci U S A 1990, 87:7512-7516.
35. Blaschitz C., Raffatellu M. Th17 cytokines and the gut mucosal barrier. JClin Immunol 2010, 30:196-203.
36. Lindenstrom T., Buchmann K., Secombes C.J. Gyrodactylus derjavini infection elicits IL-1 beta expression in rainbow trout skin. Fish Shellfish Immunol 2003, 15:107-115.
37. Gonzalez S.F., Buchmann K., Nielsen M.E. Real-time gene expression analysis in carp (Cyprinus carpio L.) skin: inflammatory responses caused by the ectoparasite Ichthyophthirius multifiliis. Fish Shellfish Immunol 2007, 22:641-650.
38. Morrison R.N., Zou J., Secombes C.J., Scapigliati G., Adams M.B., Nowak B.F. Molecular cloning and expression analysis of tumour necrosis factor-α in amoebic gill disease (AGD)-affected Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol 2007, 23:1015-1031.
39. Forlenza M., Walker P.D., de Vries B.J., Wendelaar Bonga S.E., Wiegertjes G.F. Transcriptional analysis of the common carp (Cyprinus carpio L.) immune response to the fish louse Argulus japonicus Thiele (Crustacea: Branchiura). Fish Shellfish Immunol 2008, 25:76-83.
40. Olsen M.M., Kania P.W., Heinecke R.D., Skjoedt K., Rasmussen K.J., Buchmann K. Cellular and humoral factors involved in the response of rainbow trout gills to Ichthyophthirius multifiliis infections: molecular and immunohistochemical studies. Fish Shellfish Immunol 2011, 30:859-869.
41. Khoo C.K., Abdul-Murad A.M., Kua B.C., Mohd-Adnan A. Cryptocaryon irritans infection induces the acute phase response in Lates calcarifer: a transcriptomic perspective. Fish Shellfish Immunol 2012, 33:788-794.
42. Fast M.D., Muise D.M., Easy R.E., Ross N.W., Johnson S.C. The effects of Lepeophtheirus salmonis infections on the stress response and immunological status of Atlantic salmon (Salmo salar). Fish Shellfish Immunol 2006, 21:228-241.
43. Rombout J.H.W.M., Abelli L., Picchietti S., Scapigliati G., Kiron V. Teleost intestinal immunology. Fish Shellfish Immunol 2011, 31:616-626.
44. Salinas I., Zhang Y.-A., Sunyer J.O. Mucosal immunoglobulins and B cells of teleost fish. Dev Comp Immunol 2011, 35:1346-1365.
45. Mulder I.E., Wadsworth S., Secombes C.J. Cytokine expression in the intestine of rainbow trout (Oncorhynchus mykiss) during infection with Aeromonas salmonicida. Fish Shellfish Immunol 2007, 23:747-759.
46. Inami M., Taverne-Thiele A.J., Schroder M.B., Kiron V., Rombout J.H.W.M. Immunological differences in intestine and rectum of Atlantic cod (Gadus morhua L.). Fish Shellfish Immunol 2009, 26:751-759.
47. Vignali D.A., Kuchroo V.K. IL-12 family cytokines: immunological playmakers. Nat Immunol 2012, 13:722-728.
48. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 2003, 3:133-146.
49. Nascimento D.S., do Vale A., Tomas A.M., Zou J., Secombes C.J., dos Santos N.M.S. Cloning, promoter analysis and expression in response to bacterial exposure of sea bass (Dicentrarchus labrax L.) interleukin-12 p40 and p35 subunits. Mol Immunol 2007, 44:2277-2291.
50. Forlenza M., de Carvalho Dias J.D., Vesely T., Pokorova D., Savelkoul H.F., Wiegertjes G.F. Transcription of signal-3 cytokines, IL-12 and IFN, coincides with the timing of CD8 up-regulation during viral infection of common carp (Cyprinus carpio L.). Mol Immunol 2008, 45:1531-1547.
51. Grayfer L., Hanington P.C., Belosevic M. Macrophage colony-stimulating factor (CSF-1) induces pro-inflammatory gene expression and enhances antimicrobial responses of goldfish (Carassius auratus L.) macrophages. Fish Shellfish Immunol 2009, 26:406-413.
52. Ristow S., Evans D.L., Jaso-Friedmann L. Analyzing nonspecific cytotoxic cells in fish. Methods in molecular biology: natural killer cell protocols 2000, vol. 121:347-357. Humana Press, Clifton, NJ.
53. Cuesta A., Salinas I., Rodríguez A., Muñoz P., Sitjà-Bobadilla A., Álvarez-Pellitero P., et al. Cell-mediated cytotoxicity is the main innate immune mechanism involved in the cellular defence of gilthead seabream (Teleostei: Sparidae) against Enteromyxum leei (Myxozoa). Parasite Immunol 2006, 28:657-665.
54. Sitjà-Bobadilla A., Redondo M.J., Bermúdez R., Palenzuela O., Ferreiro I., Riaza A., et al. Innate and adaptive immune responses of turbot, Scophthalmus maximus (L.), following experimental infection with Enteromyxum scophthalmi (Myxosporea: Myxozoa). Fish Shellfish Immunol 2006, 21:485-500.
55. Huising M.O., Stolte E., Flik G., Savelkoul H.F.J., Verburg-van Kemenade B.M.L. CXC chemokines and leukocyte chemotaxis in common carp (Cyprinus carpio L.). Dev Comp Immunol 2003, 27:875-888.
56. Harun 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.
57. Fleurance R., Sauvegrain C., Marques A., Le Breton A., Guereaud C., Cherel Y., et al. Histopathological changes caused by Enteromyxum leei infection in farmed sea bream Sparus aurata. Dis Aquat Org 2008, 79:219-228.
58. Álvarez-Pellitero P. Fish immunity and parasite infections: from innate immunity to immunoprophylactic prospects. Vet Immunol Immunopathol 2008, 126:171-198.
59. Körner H., McMorran B., Schluter D., Fromm P. The role of TNF in parasitic diseases: still more questions than answers. Int J Parasitol 2010, 40:879-888.
60. Roca F.J., Mulero I., López-Muñoz A., Sepulcre M.P., Renshaw S.A., Meseguer J., et al. Evolution of the inflammatory response in vertebrates: fish TNF-α is a powerful activator of endothelial cells but hardly activates phagocytes. JImmunol 2008, 181:5071-5081.
61. Sitjà-Bobadilla A., Calduch-Giner J., Saera-Vila A., Palenzuela O., Álvarez-Pellitero P., Pérez-Sánchez J. Chronic exposure to the parasite Enteromyxum leei (Myxozoa: Myxosporea) modulates the immune response and the expression of growth, redox and immune relevant genes in gilthead sea bream, Sparus aurata L. Fish Shellfish Immunol 2008, 24:610-619.
62. Taga T., Kishimoto T. gp130 and the interleukin-6 family of cytokines. Annu Rev Immunol 1997, 15:797-819.
63. Eulenfeld R., Dittrich A., Khouri C., Mueller P.J., Muetze B., Wolf A., et al. Interleukin-6 signalling: more than Jaks and STATs. Eur J Cell Biol 2012, 91:486-495.
64. Xing Z., Gauldie J., Cox G., Baumann H., Jordana M., Lei X.F., et al. IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. JClin Invest 1998, 101:311-320.
65. Chen H.H., Lin H.T., Foung Y.F., Han-You Lin J. The bioactivity of teleost IL-6: IL-6 protein in orange-spotted grouper (Epinephelus coioides) induces Th2 cell differentiation pathway and antibody production. Dev Comp Immunol 2012, 38:285-294.
66. Kaneda M., Odaka T., Suetake H., Tahara D., Miyadai T. Teleost IL-6 promotes antibody production through STAT3 signaling via IL-6R and gp130. Dev Comp Immunol 2012, 38:224-231.
67. Malefyt R.D., Abrams J., Bennett B., Figdor C.G., Devries J.E. Interleukin-10 (IL-10) inhibits cytokine synthesis by human monocytes - an autoregulatory role of IL-10 produced by monocytes. JExp Med 1991, 174:1209-1220.
68. Taylor A., Akdis M., Joss A., Akkoc T., Wenig R., Colonna M., et al. IL-10 inhibits CD28 and ICOS costimulations of T cells via src homology 2 domain-containing protein tyrosine phosphatase 1. JAllergy Clin Immunol 2007, 120:76-83.
69. Inoue Y., Kamota S., Ito K., Yoshiura Y., Ototake M., Motitomo T., et al. Molecular cloning and expression analysis of rainbow trout (Oncorhynchus mykiss) interleukin-10 cDNAs. Fish Shellfish Immunol 2005, 18:335-344.
70. Zhang D.C., Shao Y.Q., Huang Y.Q., Jiang S.G. Cloning, characterization and expression analysis of interleukin-10 from the zebrarish (Danio rerio). JBiochem Mol Biol 2005, 38:571-576.
71. Kumari J., Bøgwald J., Dalmo R.A. Vaccination of Atlantic salmon, Salmo salar L., with Aeromonas salmonicida and infectious pancreatic necrosis virus (IPNV) showed a mixed Th1/Th2/Treg response. JFish Dis 2013, 36:881-886.
72. Seppola M., Larsen A.N., Steiro K., Robertsen B., Jensen I. Characterisation and expression analysis of the interleukin genes, IL-1 beta, IL-8 and IL-10, in Atlantic cod (Gadus morhua L.). Mol Immunol 2008, 45:887-897.
73. c family cytokines. Nat Rev Immunol 2009, 9:480-490.
74. Scheller J., Chalaris A., Schmidt-Arras D., Rose-John S. The pro- and anti-inflammatory properties of the cytokine interleukin-6. BBA - Mol Cell Res 2011, 1813:878-888.
75. Estensoro I., Calduch-Giner J.A., Kaushik S., Pérez-Sánchez J., Sitjà-Bobadilla A. Modulation of the IgM gene expression and the IgM immunoreactive cell distribution by the nutritional background in gilthead sea bream (Sparus aurata) challenged with Enteromyxum leei (Myxozoa). Fish Shellfish Immunol 2012, 33:401-410.
76. Zou J., Bird S., Truckle J., Bols N., Horne M., Secombes C. Identification and expression analysis of an IL-18 homologue and its alternatively spliced form in rainbow trout (Oncorhynchus mykiss). Eur J Biochem 2004, 271:1913-1923.
77. Smith D.E. The biological paths of IL-1 family members IL-18 and IL-33. JLeukoc Biol 2011, 89:383-392.
78. Akdis M., Burgler S., Crameri R., Eiwegger T., Fujita H., Gomez E., et al. Interleukins, from 1 to 37, and interferon-gamma: receptors, functions, and roles in diseases. JAllergy Clin Immunol 2011, 127:701-721. e1-70.
79. Boehm T. Evolution of vertebrate immunity. Curr Biol 2012, 22:R722-R732.
80. Zapata A., Diez B., Cejalvo T., Gutiérrez-de Frías C., Cortés A. Ontogeny of the immune system of fish. Fish Shellfish Immunol 2006, 20:126-136.
81. Lieschke G. Zebrafish - an emerging genetic model for the study of cytokines and hematopoiesis in the era of functional genomics. Int J Hematol 2001, 73:23-31.
82. Savan R., Sakai M. Genomics of fish cytokines. Comp Biochem Phys D 2006, 1:89-101.