Antibody screening identifies 78 putative host proteins involved in Cyprinid herpesvirus 3 infection or propagation in common carp, Cyprinus carpio L

Journal of Fish Diseases

Volumn 36, Issue 8, 2013, Pages 721-733

  Gotesman, M ^a   Soliman, H ^a   El Matbouli, M ^a  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

Electrospray ionization mass spectrometry; Immunochemistry; Koi herpesvirus; Polyacrylamide gel electrophoresis; Protein purification

Indexed keywords

COPROSMA KAUENSIS; CYPRINIDAE; CYPRINUS CARPIO; HERPESVIRIDAE; KOI HERPESVIRUS;

EID: 84880277711     PISSN: 01407775     EISSN: 13652761     Source Type: Journal    
DOI: 10.1111/jfd.12073     Document Type: Article

References (83)

1. Adkinson M., Oren G. & Hendrick R.P. (2005) An enzyme linked immunosorbent assay (ELISA) for detection of antibodies to the koi herpesvirus (KHV) in the serum of koi Cyprinus carpio. Fish Pathology 40, 53-62.
2. Aoki T., Hirono I., Kurokawa K., Fukuda H., Nahary R., Eldar A., Davison A.J., Waltzek T.B., Bercovie H. & Hedrick R.P. (2007) Genome sequences of three koi herpesvirus isolates representing the expanding distribution of an emerging disease threatening koi and common carp worldwide. Journal of Virology 81, 5058-5065.
3. Aoki T., Takano T., Unajak S., Takagi M., Kim Y.R., Park S.B., Kondo H., Hirono I., Saito-Taki T., Hikima J. & Jung T.S. (2011) Generation of monoclonal antibodies specific for ORF68 of koi herpesvirus. Comparative Immunology, Microbiology & Infectious Diseases 34, 209-216.
4. Belcourt D.R., Okawara Y., Fryer J.N. & Bennett H.P. (1995) Immunocytochemical localization of granulin-1 to mononuclear phagocytic cells of the teleost fish Cyprinus carpio and Carassius auratus. Journal of Leukocyte Biology 57, 94-100.
5. Bercovier H., Fishman Y., Nahary R., Sinai S., Zlotkin A., Eyngor M., Gilad O., Eldar A. & Hedrick R.P. (2005) Cloning of the koi herpesvirus (KHV) gene encoding thymidine kinase and its use for a highly sensitive PCR-based diagnosis. BMC Microbiology 5, 13-22.
6. Bergmann S.M. & Kempter J. (2011) Detection of koi herpesvirus (KHV) after re-activation in persistently infected common carp (Cyprinus carpio L.) using non-lethal sampling methods. Bulletin of the European Association of Fish Pathologists 30, 74.
7. Bergmann S.M., Kempter J., Sadowski J. & Fichtner D. (2006) First detection, confirmation and isolation of koi herpesvirus (KHV) in cultured common carp (Cyprinus carpio L.) in Poland. Bulletin of the European Association of Fish Pathologists 26, 97-104.
8. Bergmann S.M., Schütze H., Fischer U., Fichtner D., Riechardt M., Meyer K., Schrudde D. & Kempter J. (2009) Detection of koi herpes virus (KHV) genome in apparently healthy fish. Bulletin of the European Association of Fish Pathologists 31, 92-100.
9. Bergmann S.M., Riechart M., Fichtner D., Leeb P. & Kempter J. (2010) Investigation on the diagnostic sensitivity of molecular tools used for detection of koi herpesvirus. Journal of Virological Methods 163, 229-233.
10. Bernhagen J., Calandra T., Mitchell R.A., Martin S.B., Tracey K.J., Voelter W., Manogue K.R., Cerami A. & Bucala R. (1993) MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature 365, 756-759.
11. Blondot M.L., Dubosclard V., Fix J., Lassoued S., Aumont-Nicaise M., Bontems F., Eléouët J.F. & Sizun C. (2012) Structure and functional analysis of the rna- and viral phosphoprotein-binding domain of respiratory syncytial virus M2-1 protein. PLoS Pathogen 8, e1002734.
12. Bondad-Reantaso M.G., Sunarto A. & Subasinghe R.P. (2007) Managing the koi herpesvirus disease outbreak in Indonesia and the lessons learned. Developments in Biologicals 129, 21-28.
13. Bretzinger A., Fischer-Scherl T., Oumouna M., Hoffmann R. & Truyen U. (1999) Mass mortality in koi carp, Cyprinus carpio, associated with gill and skin disease. Bulletin of the European Association of Fish Pathologists 19, 182-185.
14. Bright L.J., Kambesis N., Nelson S.B., Jeong B. & Turkewitz A.P. (2010) Comprehensive analysis reveals dynamic and evolutionary plasticity of Rab GTPases and membrane traffic in Tetrahymena thermophila. PLoS Genetics 6, e1001155.
15. Cameron L.C. (2012) Mass spectrometry imaging: facts and perspectives from a non-mass spectrometrist point of view. Methods 57, 417-422.
16. Costes B., Raj V.S., Michel B., Fournier G., Thirion M., Gillet L., Mast J., Lieffrig F., Bremont M. & Vanderplasschen A. (2009) The major portal of entry of koi herpesvirus in Cyprinus carpio is the skin. Journal of Virology 83, 2819-2830.
17. De La Cruz E.M. (2009) How cofilin severs an actin filament. Biophysical Reviews 1, 51-59.
18. Dishon A., Davidovich M., Ilouze M. & Kotler M. (2007) Persistence of cyprinid herpesvirus 3 in infected cultured carp cells. Journal of Virology 9, 4828-4836.
19. Dong C., Weng S., Li W., Li X., Yi Y., Liang Q. & He J. (2011) Characterization of a new cell line from caudal fin of koi, Cyprinus carpio koi, and first isolation of cyprinid herpesvirus 3 in China. Virus Research 161, 140-149.
20. Eidea K., Miller-Morgana T., Heidela J.R., Kent M.L., Bildfella R.J., LaPatra S., Watson G. & Jin L. (2011) Investigation of koi herpesvirus latency in koi. Journal of Virology 85, 4954-4962.
21. El-Matbouli M., Rucker U. & Soliman H. (2007) Detection of Cyprinid herpesvirus-3 (CyHV-3) DNA in infected fish tissues by nested polymerase chain reaction. Diseases of Aquatic Organisms 78, 23-28.
22. FAO. (2010) The State of World Fisheries and Aquaculture 2010. FAO, Rome, p. 197.
23. Fenn J.B., Mann M., Meng C.K., Wong S.F. & Whitehouse C.M. (1989) Electrospray ionization for mass spectrometry of large biomolecules. Science 246, 64-71.
24. Fournier G., Boutier M., Raj V.S., Mast J., Parmentier E., Vanderwalle P., Peeters D., Lieffrig F., Farnir F., Gillet L. & Vanderplasschen A. (2012) Feeding Cyprinus carpio with infectious materials mediates cyprinid herpesvirus 3 entry through infection of pharyngeal periodontal mucosa. Veterinary Research 43, 6.
25. Fuchs W., Fichtner D., Bergmann S.M. & Mettenleiter T.C. (2011) Generation and characterization of koi herpesvirus recombinants lacking viral enzymes of nucleotide metabolism. Archives of Virology 156, 1059-1063.
26. Fujiki K., Shin D.H., Nakao M. & Yano T. (1999) Molecular cloning of carp (Cyprinus carpio) CC chemokine, CXC chemokine receptors, allograft inflammatory factor-1, and natural killer cell enhancing factor by use of suppression subtractive hybridization. Immunogenetics 49, 909-914.
27. Gavin R.H. (1997) Microtubule-microfilament synergy in the cytoskeleton. International Review of Cytology. 173, 207-242.
28. Gilad O., Yun S., Andree K.B., Adkison M.A., Zlotkin A., Bercovier H., Eldar A. & Hedrick R.P. (2002) Initial characteristics of koi herpesvirus and development of a polymerase chain reaction assay to detect the virus in koi, Cyprinus carpio koi. Diseases of Aquatic Organisms 48, 101-108.
29. Gilad O., Yun S., Andree K.B., Adkison M.A., Way K., Willits N.H., Bercovier H. & Hedrick R.P. (2003) Molecular comparison of isolates of an emerging fish pathogen, the koi herpesvirus, and the effect of water temperature on mortality of experimentally infected koi. Journal of General Virology 84, 1-8.
30. Gilad O., Yun S., Zagmutt-Vergara F.J., Leutenegger C.M., Bercovier H.V. & Hedrick R.P. (2004) Concentrations of a koi herpesvirus (KHV) tissues of experimentally infected Cyprinus carpio koi as assessed by real-time TaqMan PCR. Diseases of Aquatic Organisms 60, 179-187.
31. Gotesman M., Hosein R.E. & Gavin R.H. (2010) A FERM domain in a class XIV myosin interacts with actin and tubulin and localizes to the cytoskeleton, phagosomes, and nucleus in Tetrahymena thermophila. Cytoskeleton 67, 90-101.
32. Gotesman M., Hosein R.E. & Gavin R.H. (2011) MyTH4, independent of its companion FERM domain, affects the organization of an intramacronuclear microtubule array and is involved in elongation of the macronucleus in Tetrahymena thermophila. Cytoskeleton 68, 220-236.
33. Griffiths W.J., Jonsson A.P., Liu S., Rai D.K. & Wang Y. (2001) Electrospray and tandem mass spectrometry in biochemistry. Biochemical Journal 355, 545-561.
34. Guo K.K., Tang Q.H., Zhang Y.M., Kang K. & He L. (2011) Identification of two internal signal peptide sequences: critical for classical swine fever virus non-structural protein 2 to trans-localize to the endoplasmic reticulum. Virology Journal 18, 236-242.
35. Harper J.W. & Schulman B.A. (2006) Structural complexity in ubiquitin recognition. Cell 124, 1133-1136.
36. Hedrick R.P., Gilad O., Yun S., Spangenberg J.V., Marty G.D., Nordhausen R.W., Kebus M.J., Bercovier H. & Eldar A. (2000) A herpesvirus associated with mass mortality of juvenile and adult koi, a strain of common carp. Journal of Aquatic Animal Health 12, 44-57.
37. Hedrick R.P., Gilad O., Yun S.C., Mcdowell T.S., Waltzek T.B., Kelley G.O. & Adkison M.A. (2005) Initial isolation and characterization of a herpes-like virus (KHV) from koi and common carp. Bulletin of Fisheries Research Agency 2, 1-7.
38. Ho C.S., Lam C.W., Chan M.H., Cheung R.C., Law L.K., Lit L.C., Ng K.F., Suen M.W. & Tai H.L. (2003) Electrospray ionisation mass spectrometry: principles and clinical applications. The Clinical Biochemist Reviews 24, 3-12.
39. Hosein R.E., Williams S.A., Haye K. & Gavin R.H. (2003) Expression of GFP-actin leads to failure of nuclear elongation and cytokinesis in Tetrahymena thermophila. Journal of Eukaryotic Microbiology 6, 403-408.
40. Huang R., Zhong S., Liu H., Kong R., Wang Y., Hu W. & Guo Q. (2010) Identification and characterization of common carp (Cyprinus carpio L.) granzyme A/K, a cytotoxic cell granule-associated serine protease. Fish and Shellfish Immunology 29, 388-398.
41. Hutoran M., Ronen A., Perelberg A., Ilouze M., Dishon A., Bejerano I., Chen N. & Kotler M. (2005) Description of an as yet unclassified DNA virus from diseased Cyprinus carpio species. Journal of Virology, 79, 1983-1991.
42. Ilouze M., Dishon A., Davidovich M., Perelberg A. & Kotler M. (2008) KHV, CNGV or CyHV-3, which is the koi/carp killer? Diseases in Asian Aquaculture, VI, 115-128.
43. Jenuwein T. & Allis C.D. (2001) Translating the histone code. Science 293, 1074-1080.
44. Joazeiro C.A. & Weissman A.M. (2000) RING finger proteins: mediators of ubiquitin ligase activity. Cell 102, 549-552.
45. Kálmán M. (1998) Astroglial architecture of the carp (Cyprinus carpio) brain as revealed by immunohistochemical staining against glial fibrillary acidic protein (GFAP). Anatomy and Embryology 198, 409-433.
46. Kato Y., Nakao M., Shimizu M., Wariishi H. & Yano T. (2004) Purification and functional assessment of C3a, C4a and C5a of the common carp (Cyprinus carpio) complement. Developmental & Comparative Immunology 28, 901-910.
47. Kuznetsov S.A., Langford G.M. & Weiss D.G. (1992) Actin-dependent organelle movement in squid axoplasm. Nature 356, 722-725.
48. Letunic I., Doerks T. & Bork P. (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acid Research 40, D302-D305. Epub 2011 Nov 3.
49. Lv J., Huang R., Li H., Luo D., Liao L., Zhu Z. & Wang Y. (2012) Cloning and characterization of the grass carp (Ctenopharyngodon idella) Toll-like receptor 22 gene, a fish-specific gene. Fish and Shellfish Immunology 32, 1022-1031.
50. McColl K., Sunarto A., Williams L.M. & Crane M.S.T.J. (2007) Koi herpes virus: dreaded pathogen or white knight? Aquaculture Health International 9, 4-6.
51. Michel B., Leroy B., Stalin Raj V., Lieffrig F., Mast J., Wattiez R., Vanderplasschen A.F. & Costes B. (2010) The genome of cyprinid herpesvirus 3 encodes 40 proteins incorporated in mature virions. Journal of General Virology 91, 452-462.
52. Miyazaki T., Kuzuya Y., Yasumoto S., Yasuda M. & Kobayashi T. (2008) Histopathological and ultrastructural features of koi herpesvirus (KHV)-infected carp Cyprinus carpio, and the morphology and morphogenesis of KHV. Diseases of Aquatic Organisms 80, 1-11.
53. Moen R.J., Johnsrud D.O., Thomas D.D. & Titus M.A. (2011) Characterization of a myosin VII MyTH/FERM domain. Journal of Molecular Biology 413, 17-23.
54. Nakao M., Mutsuro J., Obo R., Fujiki K., Nonaka M. & Yano T. (2000) Molecular cloning and protein analysis of divergent forms of the complement component C3 from a bony fish, the common carp (Cyprinus carpio): presence of variants lacking the catalytic histidine. European Journal of Immunology 30, 858-866.
55. Pikarsky E., Ronen A., Abramowitz J., Levavi-Sivan B., Hutoran M., Shapira Y., Steinitz M., Perelberg A., Soffer D. & Kotler M. (2004) The pathogenesis of the acute viral disease in fish induced by the carp interstitial nephritis and gill necrosis virus. Journal of Virology 78, 9544-9551.
56. Pokorova D., Vesely T., Piackova V., Reschova S. & Hulova J. (2005) Current knowledge on koi herpesvirus (KHV): a review. Veterinary Medicine. - Czech, 50, 139-147.
57. Raj V.S., Fournier G., Rakus K., Ronsmans M., Ouyang P., Michel B., Delforges C., Costes B., Farnir F., Leroy B., Wattiez R., Melard C., Mast J., Lieffrig F. & Vanderplasschen A. (2011) Skin mucus of Cyprinus carpio inhibits cyprinid herpesvirus 3 binding to epidermal cells. Veterinary Research 42, 92-100.
58. Rakus K., Irnazarow I., Adamek M., Palmeira L., Kawana Y., Hirono I., Kondo H., Matras M., Steinhagen D., Flasz B., Brogden G., Vanderplasschen A. & Aoki T. (2012) 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 37, 65-76.
59. Rathore G., Kumar G., Swain P. & Lakra W.S. (2009) Development of new PCR primers for detection of koi herpes virus (KHV). Indian Journal of Comparative Microbiology, Immunology and Infectious Diseases 30, 52-53.
60. Ronen A., Perelberg A., Abramowitz J., Hutoran M., Tinman S., Bejerano Y., Steinitz M. & Kotler M. (2003) Efficient vaccine against the virus causing a lethal disease in cultured Cyprinus carpio. Vaccine 21, 4677-4684.
61. Rosenkranz D., Klupp B.G., Teifke J.P., Granzow H., Fichtner D., Mettenleiter T.C. & Fuchs W. (2008) Identification of envelope protein pORF81 of koi herpesvirus. Journal of General Virology 89, 896-900.
62. Sambrook J. & Russell D. (2001) Molecular Cloning, A Laboratory Manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
63. Savan R., Aman A. & Sakai M. (2003) Molecular cloning of G type lysozyme cDNA in common carp (Cyprinus carpio L.). Fish and Shellfish Immunology 15, 263-268.
64. Shiozaki N., Nakano K., Takaine M., Abe H. & Numata O. (2009) Usual and unusual biochemical properties of ADF/cofilin-like protein Adf73p in ciliate Tetrahymena thermophila. Biochemical and Biophysical Research Communications 390, 54-59.
65. Sigrist C.J.A., Cerutti L., de Castro E., Langendijk-Genevaux P.S., Bulliard V., Bairoch A. & Hulo N. (2010) PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Research 38, 161-166.
66. Sims R.J. 3rd & Reinberg D. (2008) Is there a code embedded in proteins that is based on post-translational modifications? Nature Reviews Molecular Cell Biology 9, 815-820.
67. Soliman H. & El-Matbouli M. (2005) An inexpensive and rapid diagnostic method of koi herpesvirus (KHV) infection by loop-mediated isothermal amplification. Virology Journal 2, 83.
68. Soliman H. & El-Matbouli M. (2009) Immunocapture and direct binding loop mediated isothermal amplification simplify molecular diagnosis of Cyprinid herpesvirus-3. Journal of Virological Methods. 162, 91-95.
69. Soliman H. & El-Matbouli M. (2010) Loop mediated isothermal amplification combined with nucleic acid lateral flow strip for diagnosis of cyprinid herpes virus-3. Molecular and Cellular Probes 1, 38-43.
70. de Souza M.G., Grossi A.L., Pereira E.L., da Cruz C.O., Mendes F.M., Cameron L.C. & Paiva C.L. (2008) Actin immobilization on chitin for purifying myosin II: a laboratory exercise that integrates concepts of molecular cell biology and protein chemistry. Biochemistry and Molecular Biology Education. 36, 55-60.
71. St-Hilaire S., Beevers N., Way K., Le Deuff R.M., Martin P. & Joiner C. (2005) Reactivation of koi herpesvirus infections in common carp Cyprinus carpio. Diseases of Aquatic Organisms, 67, 15-23.
72. St-Hilaire S., Beevers N., Joiner C., Hedrick R.P. & Way K. (2009) Antibody response of two populations of common carp, Cyprinus carpio L., exposed to koi herpesvirus. Journal of Fish Diseases 32, 311-320.
73. Sunarto A., McColl K.A., Crane M.S.T.J., Sumiati T., Hyatt A.D., Barnes A.C. & Walker P.J. (2007) Isolation and characterization of koi herpesvirus (KHV) from Indonesia: identification of a new genetic lineage. Journal of Fish Diseases 34, 87-101.
74. Tsai P.L., Chen C.H., Huang C.J., Chou C.M. & Chang G.D. (2004) Purification and cloning of an endogenous protein inhibitor of carp nephrosin, an astacin metalloproteinase. The Journal of Biological Chemistry 279, 11146-11155.
75. Tuxworth R.I., Stephens S., Ryan Z.C. & Titus M.A. (2005) Identification of a myosin VII-talin complex. The Journal of Biological Chemistry 28, 26557-26564.
76. Watson James D. (2003) DNA: The Secrets of Life. Knopf. Print, New York City, NY, pp. 220-222, 226-228.
77. Wei S., Huang Y., Cai J., Huang X., Fu J. & Qin Q. (2012) Molecular cloning and characterization of c-type lysozyme gene in orange-spotted grouper, Epinephelus coioides. Fish and Shellfish Immunology 33, 186-196.
78. Williams N.E. (2000) Immunoprecipitation procedures. In: Methods in Cell Biology: Tetrahymena thermophila, Vol. 62 (ed. by D.J. Asai & J.D. Forney ), pp. 449-453. Academic Press, New York, NY.
79. Williams S.A. & Schwarzbauer J.E. (2009) A shared mechanism of adhesion modulation for tenascin-C and fibulin-1. Molecular Biology of the Cell. 20, 1141-1149.
80. Williams N.E., Tsao C.C., Bowen J., Hehman G.L., Williams R.J. & Frankel J. (2006) The actin gene ACT1 is required for phagocytosis, motility, and cell separation of Tetrahymena thermophila. Eukaryotic Cell. 5, 555-567.
81. Wu C.L., Lin T.H., Chang T.L., Sun H.W., Hui C.F. & Wu J.L. (2011) Zebrafish HSC70 promoter to express carp muscle-specific creatine kinase for acclimation under cold condition. Transgenic Research 20, 1217-1226.
82. Ye X., Zhang L., Tian Y., Tan A., Bai J. & Li S. (2010) Identification and expression analysis of the g-type and c-type lysozymes in grass carp Ctenopharyngodon idellus. Developmental and Comparative Immunology 34, 501-509.
83. Zhang S., Han J., Sells M.A., Chernoff J., Knaus U.G., Ulevitch R.J. & Bokoch G.M. (1995) Rho family GTPases regulate p38 mitogen-activated protein kinase through the downstream mediator Pak1. The Journal of Biological Chemistry 270, 23934-23936.