Gene expression analysis of common carp (Cyprinus carpio L.) lines during Cyprinid herpesvirus 3 infection yields insights into differential immune responses

Developmental and Comparative Immunology

Volumn 37, Issue 1, 2012, Pages 65-76

  Rakus, Krzysztof L ^a,c   Irnazarow, Ilgiz ^a   Adamek, Mikołaj ^b   Palmeira, Leonor ^c   Kawana, Yuriko ^d   Hirono, Ikuo ^d   Kondo, Hidehiro ^d   Matras, Marek ^e   Steinhagen, Dieter ^b   Flasz, Barbara ^a   Brogden, Graham ^b   Vanderplasschen, Alain ^c   Aoki, Takashi ^d  

^a Polish Academy of Sciences   (Poland)

^b UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^c UNIVERSITY OF LIÈGE   (Belgium)

^d TOKYO UNIVERSITY OF MARINE SCIENCE AND TECHNOLOGY   (Japan)

^e NATIONAL VETERINARY RESEARCH INSTITUTE   (Poland)

Author keywords

Antiviral response; Common carp; CyHV 3; Cyprinid herpesvirus 3; Cytokines; Immune response; KHV; T cell marker

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARP; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYPRINID HERPESVIRUS 3; DISEASE MARKER; DOWN REGULATION; GENE EXPRESSION; GENE FUNCTION; GENETIC LINE; HERPES VIRUS; HERPES VIRUS INFECTION; IMMUNE RESPONSE; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SURVIVAL RATE; T LYMPHOCYTE ACTIVATION; UNINDEXED SEQUENCE; UPREGULATION; VIRUS LOAD;

COPROSMA KAUENSIS; CYPRINIDAE; CYPRINUS CARPIO; KOI HERPESVIRUS;

EID: 84859820156     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2011.12.006     Document Type: Article

References (86)

1. Aoki T., Hirono I., Kurokawa K., Fukuda H., Nahary R., Eldar A., et al. Genome sequences of three koi herpesvirus isolates representing the expanding distribution of an emerging disease threatening koi and common carp worldwide. Journal of Virology 2007, 81:5058-5065.
2. Baerwald M.R., Welsh A.B., Hedrick R.P., May B. Discovery of genes implicated in whirling disease infection and resistance in rainbow trout using genome-wide expression profiling. BMC Genomics 2008, 9:1-11.
3. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B 1995, 57:289-300.
4. Bianchet M.A., Odom E.W., Vasta G.R., Amzel L.M. A novel fucose recognition fold involved in innate immunity. Nature Structural Biology 2002, 9:628-634.
5. Bilodeau-Bourgeois L., Bosworth B.G., Peterson B.C. Differences in mortality, growth, lysozyme, and toll-like receptor gene expression among genetic groups of catfish exposed to virulent Edwardsiella ictaluri. Fish & Shellfish Immunology 2008, 24:82-89.
6. Bode J.G., Ludwig S., Ehrhardt C., Erhardt A., Albrecht U., Schaper F., et al. IFN-α antagonistic activity of HCV core protein involves induction of suppressor of cytokine signaling-3. The FASEB Journal 2003, 17:488-490.
7. Bolstad B.M., Irizarry R.A., Astrand M., Speed T.P. A comparison of normalization methods for high density oligonucleotide array data based on bias and variance. Bioinformatics 2003, 19:185-193.
8. Brazma A., Hingamp P., Quackenbush J., Sherlock G., Spellman P., Stoeckert C., et al. Minimum information about a microarray experiment (MIAME) - toward standards for microarray data. Nature Genetics 2001, 29:365-371.
9. Bretzinger A., Fischer-Scheri T., Oumouna M., Hoffman R., Truyen U. Mass mortalities in koi carp, Cyprinus carpio, associated with gill and skin disease. Bulletin of European Association of Fish Pathology 1999, 19:182-185.
10. Chan T., Barra N.G., Lee A.J., Ashkar A.A. Innate and adaptive immunity against herpes simplex virus type 2 in the genital mucosa. Journal of Reproductive Immunology 2011, 88:210-218.
11. Collet B., Bain N., Prevost S., Besinque G., McBeath A., Snow M., et al. Isolation of an Atlantic salmon (Salmo salar) signal transducer and activator of transcription STAT1 gene: Kinetics of expression upon ISAV or IPNV infection. Fish & Shellfish Immunology 2008, 25:861-867.
12. Costes B., Stalin Raj V., Michel B., Fournier G., Thirion M., Gillet L., et al. The major portal of entry of Koi Herpesvirus in Cyprinus carpio is the skin. Journal of Virology 2009, 83:2819-2830.
13. Coyle P., Philcox J.C., Carey L.C., Rofe A.M. Metallothionein: the multipurpose protein. Cellular and Molecular Life Sciences 2002, 59:627-647.
14. Davison A.J., Eberle R., Ehlers B., Hayward G.S., McGeoch D.J., Minson A.C., et al. The order Herpesvirales. Archives of Virology 2009, 154:171-177.
15. D'Cunha J., Knight E., Haas A.L., Truitt R.L., Borden E.C. Immunoregulatory properties of ISG15, an interferon-induced cytokine. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:211-215.
16. Devine L., Kieffer L.J., Aitken V., Kavathas P.B. Human CD8 beta, but not mouse CD8 beta, can be expressed in the absence of CD8 alpha as a beta beta homodimer. Journal of Immunology 2000, 164:833-838.
17. Dixon P.F., Joiner C.L., Way K., Reese R.A., Jeney G., Jeney Z. Comparison of the resistance of selected families of common carp, Cyprinus carpio L., to koi herpesvirus: preliminary study. Journal of Fish Diseases 2009, 32:1035-1039.
18. Fenner J.E., Starr R., Cornish A.L., Zhang J.-G., Metcalf D., Schreiber R.D., et al. Suppressor of cytokine signaling 1 regulates the immune response to infection by a unique inhibition of type I interferon activity. Nature Immunology 2006, 7:33-39.
19. Fischer U., Utke K., Somamoto T., Köllner B., Ototake M., Nakanishi T. Cytotoxic activities of fish leucocytes. Fish & Shellfish Immunology 2006, 20:209-226.
20. Forlenza, M., 2009. Immune response of carp. A molecular and cellular approach to infections. PhD Thesis, Wageningen University, Wageningen, The Netherlands.
21. Forlenza M., de Carvalho Dias J.D.A., Vesely T., Pokorova D., Savelkoul H.F.J., Wiegertjes G.F. Transcription of signal-3 cytokines, IL-12 and IFNαβ, coincides with the timing of CD8αβ up-regulation during viral infection of common carp (Cyprinus carpio L.). Molecular Immunology 2008, 45:1531-1547.
22. Forlenza M., Walker P.D., de Vries B.J., Bonga S.E.W., 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 Immunology 2008, 25:76-83.
23. 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 and Comparative Immunology 2003, 27:127-136.
24. Gentleman R.C., Carey V.J., Bates D.M., Bolstad B., Dettling M., Dudoit S., et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biology 2004, 5:R80.
25. Gilad O., Yun S., Zagmutt-Vergara F.J., Leutenegger C.M., Bercovier H., Hedrick R.P. Concentrations of a koi herpesvirus (KHV) in tissues of experimentally infected Cyprinus carpio koi as assessed by real-time TaqMan PCR. Diseases of Aquatic Organisms 2004, 60:179-187.
26. 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 Immunology 2007, 22:641-650.
27. Harty R.N., Pitha P.M., Okumura A. Antiviral activity of innate immune protein ISG15. Journal of Innate Immunity 2009, 1:397-404.
28. Hedrick R.P., Gilad O., Yun S., Spangenberg J.V., Marty G.D., Nordhausen R.W., et al. A herpesvirus associated with mass mortality of juvenile and adult koi, a strain of common carp. Journal of Aquatic Animals and Health 2000, 12:44-57.
29. Honda S., Kashiwagi M., Miyamoto K., Takei Y., Hirose S. Multiplicity, Structures, and Endocrine and Exocrine Natures of Eel Fucose-binding Lectins. Journal of Biological Chemistry 2000, 275:33151-33157.
30. Huising M.O., van Schijndel J.E., Kruiswijk C.P., Nabuurs S.B., Savelkoul H.F.J., 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.
31. Ingerslev H.C., Rønneseth A., Pettersen E.F., Wergeland H.I. Differential expression of immune genes in Atlantic salmon (Salmo salar L.) challenged intraperitoneally or by cohabitation with IPNV. Scand. Journal of Immunology 2009, 69:90-98.
32. Irnazarow I. Genetic variability of Polish and Hungarian carp lines. Aquaculture 1995, 129:215-219.
33. Katze M.G., He Y., Gale M. Viruses and interferon: a fight for supremacy. Nature Reviews Immunology 2002, 2:675-687.
34. Kerscher O., Felberbaum R., Hochstrasser M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annual Review of Cell and Developmental Biology 2006, 22:159-180.
35. Kunkel E.J., Campbell J.J., Haraldsen G., Pan J., Boisvert J., Roberts A.I., et al. Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. Journal of Experimental Medicine 2000, 192:761-768.
36. Liu M., Reimschuessel R., Hassel B.A. Molecular cloning of the fish interferon stimulated gene, 15 kDa (ISG15) orthologue: a ubiquitin-like gene induced by nephrotoxic damage. Gene 2002, 298:129-139.
37. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 2001, 25:402-408.
38. Lovoll M., Fischer U., Mathisen G.S., Bogwald J., Ototake M., Dalmo R.A. The C3 subtypes are differentially regulated after immunostimulation in rainbow trout, but head kidney macrophages do not contribute to C3 transcription. Veterinary Immunology and Immunopathology 2007, 117:284-295.
39. Meurens F., Berri M., Whale J., Dybvig T., Strom S., Thompson D., et al. Expression of TECK/CCL25 and MEC/CCL28 chemokines and their respective receptors CCR9 and CCR10 in porcine mucosal tissues. Veterinary Immunology and Immunopathology 2006, 113:313-327.
40. Meurens F., Whale J., Brownlie R., Dybvig T., Thompson D.R., Gerdts V. Expression of mucosal chemokines TECK/CCL25 and MEC/CCL28 during fetal development of the ovine mucosal immune system. Immunology 2007, 120:544-555.
41. Michel B., Fournier G., Lieffrig F., Costes B., Vanderplasschen A. Cyprinid herpesvirus 3. Emerging Infectious Diseases 2010, 16:1835-1843.
42. Mocchegiani E., Costarelli L., Giacconi R., Cipriano C., Muti E., Malavolta M. Zinc-binding proteins (metallothionein and α-2 macroglobulin) and immunosenescence. Experimental Gerontology 2006, 41:1094-1107.
43. Mohanty B.R., Sahoo P.K. Immune responses and expression profiles of some immune-related genes in Indian major carp, Labeo rohita to Edwardsiella tarda infection. Fish & Shellfish Immunology 2010, 28:613-621.
44. Mossman K.L., Ashkar A.A. Herpesviruses and the innate immune response. Viral Immunology 2005, 18:267-281.
45. Nakanishi T., Fischer U., Dijkstra J.M., Hasegawa S., Somamoto T., Okamoto N., et al. Cytotoxic T cell function in fish. Developmental and Comparative Immunology 2002, 26:131-139.
46. Negenborn, J., 2009. Klinisch-chemische parameter im blut und urin von karpfen unter infection mit dem koi-herpesvirus. PhD Thesis, University of Veterinary Medicine in Hannover, Hannover, Germany.
47. Neukirch M., Böttcher R., Bunnajirakul S. Isolation of a virus from koi with altered gills. Bulletin of European Association of Fish Pathology 1999, 19:221-223.
48. Niu D., Peatman E., Liu H., Lu J., Kucuktas H., Liu S., et al. Microfibrillar-associated protein 4 (MFAP4) genes in catfish play a novel role in innate immune responses. Developmental and Comparative Immunology 2011, 35:568-579.
49. Ødegård J., Olesen I., Dixon P., Jeney Z., Nielsen H.-M., Way K., et al. Genetic analysis of common carp (Cyprinus carpio) strains. II: Resistance to koi herpesvirus and Aeromonas hydrophila and their relationship with pond survival. Aquaculture 2010, 304:7-13.
50. Oshansky C.M., Krunkosky T.M., Barber J., Jones L.P., Tripp R.A. Respiratory syncytial virus proteins modulate suppressors of cytokine signaling 1 and 3 and the type I interferon response to infection by a toll-like receptor pathway. Viral Immunology 2009, 22:147-161.
51. Perelberg A., Ilouze M., Kotler M., Steinitz M. Antibody response and resistance of Cyprinus carpio immunized with cyprinid herpes virus 3 (CyHV-3). Vaccine 2008, 26:3750-3756.
52. Pokorova D., Vesely T., Piackova V., Reschova S., Hulova J. Current knowledge on koi herpesvirus (KHV): a review. Veterinary Medicine (Czech) 2005, 50:139-147.
53. Pothlichet J., Chignard M., Si-Tahar M. Cutting edge: innate immune response triggered by influenza a virus is negatively regulated by SOCS1 and SOCS3 through a RIG-I/IFNARI-dependent pathway. Journal of Immunology 2008, 180:2034-2038.
54. Purcell M.K., Kurath G., Garver K.A., Herwig R.P., Winton J.R. Quantitative expression profiling of immune response genes in rainbow trout following infectious haematopoletic necrosis virus (IHNV) infection or DNA vaccination. Fish & Shellfish Immunology 2004, 17:447-462.
55. R Development Core Team, 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. http://www.R-project.org.
56. Raida M.K., Buchmann K. Development of adaptive immunity in rainbow trout, Oncorhynchus mykiss (Walbaum) surviving an infection with Yersinia ruckeri. Fish & Shellfish Immunology 2008, 25:533-541.
57. Raida M.K., Buchmann K. Bath vaccination of rainbow trout (Oncorhynchus mykiss Walbaum) against Yersinia ruckeri: effects of temperature on protection and gene expression. Vaccine 2008, 26:1050-1062.
58. Raj S.V., Fournier G., Rakus K., Ronsmans M., Ouyang P., Michel B., et al. Skin mucus of Cyprinus carpio inhibits cyprinid herpesvirus 3 binding to epidermal cells. Vet. Res. 2011, 42:92.
59. Rakus K.Ł., Wiegertjes G.F., Adamek M., Siwicki A.K., Lepa A., Irnazarow I. Resistance of common carp (Cyprinus carpio L.) to Cyprinid herpesvirus-3 is influenced by major histocompatibility (MH) class II B gene polymorphism. Fish & Shellfish Immunology 2009, 26:737-743.
60. Reed L.J., Meunch H.A. A simple method of estimating fifty percent endpoints. American Journal of Hygiene 1938, 24:493-497.
61. Ritchie M.E., Silver J., Oshlack A., Silver J., Holmes M., Diyagama D., et al. A comparison of background correction methods for two-colour microarrays. Bioinformatics 2007, 23:2700-2707.
62. Robertsen B. The interferon system of teleost fish. Fish & Shellfish Immunology 2006, 20:172-191.
63. Rombout J.H.W.M., Huttenhuis H.B.T., Picchietti S., Scapigliati G. Phylogeny and ontogeny of fish leucocytes. Fish & Shellfish Immunology 2005, 16:441-455.
64. Rossi D., Zlotnik A. The biology of chemokines and their receptors. Annual Review of Immunology 2000, 18:217-242.
65. Saeij J.P.J., de Vries B.J., Wiegertjes G.F. The immune response of carp to Trypanoplasma borreli: kinetics of immune gene expression and polyclonal lymphocyte activation. Developmental and Comparative Immunology 2003, 27:859-874.
66. Saito T., Hatada M., Iwanaga S., Kawabata S.I. A Newly Identified Horseshoe Crab Lectin with Binding Specificity to O-antigen of Bacterial Lipopolysaccharides. Journal of Biological Chemistry 1997, 272:30703-30708.
67. Shapira Y., Magen Y., Zak T., Kotler M., Hulata G., Levavi-Sivan B. Differential resistance to koi herpes virus (KHV)/carp interstitial nephritis and gill necrosis virus (CNGV) among common carp (Cyprinus carpio L.) strains and crossbreds. Aquaculture 2005, 245:1-11.
68. Sigh J., Lindenstrom T., Buchmann K. Expression of pro-inflammatory cytokines in rainbow trout (Oncorhynchus mykiss) during an infection with Ichthyophthirius multifiliis. Fish & Shellfish Immunology 2004, 17:75-86.
69. Smyth, G.K., 2004. Linear models and empirical Bayes methods for assessing diffrential expression in microarray experiments. Statastiacl Application of Genetics and Molecular Biology 3, Article 3.
70. Starr R., Willson T.A., Viney E.M., Murray L.J.L., Rayner J.R., Jenkins B.J., et al. A family of cytokine-inducible inhibitors of signaling. Nature 1997, 387:917-921.
71. Sun B., Robertsen B., Wang Z., Liu B. Identification of an Atlantic salmon IFN multigene cluster encoding three IFN subtypes with very different expression properties. Developmental and Comparative Immunology 2009, 33:547-558.
72. Sun X.F., Shang N., Hu W., Wang Y.P., Guo Q.L. Molecular cloning and characterization of carp (Cyprinus carpio L.) CD8 beta and CD4-like genes. Fish & Shellfish Immunology 2007, 23:1242-1255.
73. Tafalla C., Coll J., Secombes C.J. Expression of genes related to the early immune response in rainbow trout (Oncorhynchus mykiss) after viral haemorrhagic septicemia virus (VHSV) infection. Developmental and Comparative Immunology 2005, 29:615-626.
74. Takano T., Iwahori A., Hirono I., Aoki T. Development of a DNA vaccine against hirame rhabdovirus and analysis of the expression of immune-related genes after vaccination. Fish & Shellfish Immunology 2004, 17:367-374.
75. Utke K., Bergmann S., Lorenzen N., Köllner B., Ototake M., Fischer U. Cell-mediated cytotoxicity in rainbow trout, Oncorhynchus mykiss, infected with viral haemorrhagic septicaemia virus. Fish & Shellfish Immunology 2007, 22:182-196.
76. Verrier E.R., Langevin C., Benmansour A., Boudinot P. Early antiviral response and virus-induced genes in fish. Developmental and Comparative Immunology 2011, 35:101-111.
77. Vicari A.P., Figueroa D.J., Hedrick J.A., Foster J.S., Singh K.P., Menon S., et al. TECK: A novel CC chemokine specifically expressed by thymic dendritic cells and potentially involved in T cell development. Immunity 1997, 7:291-301.
78. Waltzek T.B., Kelley G.O., Alfaro M.E., Kurobe T., Davison A.J., Hedrick R.P. Phylogenetic relationships in the family Alloherpesviridae. Diseases of Aquatic Organisms 2009, 84:179-194.
79. Wang T., Secombes C.J. Identification and expression analysis of two fish-specific IL-6 cytokine family members, the ciliary neurotrophic factor (CNTF)-like and M17 genes, in rainbow trout Oncorhynchus mykiss. Molecular Immunology 2009, 46:2290-2298.
80. Wills M.R., Carmichael A.J., Sinclair J., Sissons J.P. Immunobiology and host response. Human Herpesviruses: Biology, Therapy and Immunoprophylaxis 2007, Cambridge University Press, Cambridge, Chapter 43. A. Arvin, G. Campadelli-Fiume, E. Mocarski, P.S. Moore, B. Roizman, R. Whitley, K. Yamanishi (Eds.).
81. Witte T., Spoerl R., Chang H.C. The CD8 beta ectodomain contributes to the augmented coreceptor function of CD8 alpha beta heterodimers relative to CD8 alpha alpha homodimers. Cellular Immunology 1999, 191:90-96.
82. Yang, Y.H., Thorne, N.P. 2003. Normalization for two-color cDNA microarray data. In: Goldstein, D.R. (Ed.), Science and Statistics A Festschrift for Terry Speed IMS Lecture Notes - Monograph Series, pp. 403-418.
83. Yano, T. 1992. Assays of hemolytic complement activity. In: Stolen, J.S. Fletcher, T.C., Anderson, D.P., Kaatari, S.L., Rowley A.F. (Eds.), Techniques in Fish Immunology, vol. 2, pp. 131-141.
84. Yasuike M., Takano T., Kondo H., Hirono I., Aoki T. Differential gene expression profiles in Japanese flounder (Paralichthys olivaceus) with different susceptibilities to edwardsiellosis. Fish & Shellfish Immunology 2010, 29:747-752.
85. Zhang Y.B., Gui J.F. Identification of two novel interferon-stimulated genes from cultured CAB cells induced by UV-inactivated grass carp hemorrhage virus. Diseases of Aquatic Organisms 2004, 60:1-9.
86. Zhao D.C., Yan T., Li L., You S., Zhang C. Respiratory syncytial virus inhibits interferon-ainducible signaling in macrophage-like U937 cells. Journal of Infection 2007, 54:393-398.