Keywords
temperature
rainbow trout
fry
ISGs
real-time PCR
mortality
IPNV
temperatura
trucha arcoíris
alevines
ISGs
PCR tiempo- real
mortalidad
How to Cite
Abstract
The infectious pancreatic necrosis (IPNV) is the causative agent of an acute illness well characterized in salmonids worldwide. Clinical signs and mortality rates are dependent on several factors such as the viral dose, the age of the fish, the water temperature, among others. An experimental study was conducted to measure the effect of temperature on the gene expression profile of IFN-1(α), STAT-1 and Mx-1 in rainbow trout fry, exposed to IPNV. Fry (n=198) were exposed at 8, 12 and 16°C, and samples were taken for 21 days to determine the virus titer and gene expression. In the first 11 days the greatest viral titer was recorded at 8°C compared with the values obtained at 12 and 16°C. At 8°C, there was a significant increase on day 4 of mRNA Mx-1 (t-test, p<0.05), time in which the viral titer began to decrease. Furthermore, as the viral titer increased, STAT-1 and Mx-1 (r=0.91) and (r=0.96) increased, respectively. The animals were able to recover from day 4 from some of the symptoms of IPN. Clinical disease was developed only in fish exposed to 12°C and all died between days 6 and 14, despite the highly significant increase shown in the average expression level of Mx-1, compared with the values recorded at 8°C and 16°C (Tukey, p<0.0001). Additionally, the expression profiles of IFN-1(α) and STAT-1 decreased completely (~0.016) and (~0.020 times) on day 7. The highest expression level of IFN-1(α), occurred at 16°C (Tukey, p<0.0005). Fry exposed at 16°C were normal during the experiment. IFN-1(α) possibly generated a protector effect from day 2 when they showed a significant expression increase compared with the results at 8°C and 12°C (t-student, p<0.0001); however, STAT-1 was not significantly affected by temperature, although the highest average expression value was recorded at 16°C. Our research supports the expression of relevant anti-viral response genes as IFN-1(α), STAT-1 and Mx-1 are physiologically modulated by the water temperature, directly influencing the development of the IPN disease in rainbow trout.References
Battersby, B. J., & Moyes, C. D. (1998). Influence of acclimation temperature on mitochondrial DNA, RNA, and enzymes in skeletal muscle. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 275, 905-912.
Collet, B., Boudinot, P., Benmansour, A., & Secombes, C. J. (2004). An Mx1 promoter–reporter system to study interferon pathways in rainbow trout. Developmental & Comparative Immunology, 28, 793-801.
Dios, S., Romero, A., Chamorro, R., Figueras, A., & Novoa, B. (2010). Effect of the temperature during antiviral immune response ontogeny in teleosts. Fish & Shellfish Immunology, 29, 1019-1027.
Dobos, P. (1995). The molecular biology of infectious pancreatic necrosis virus (IPNV). Annual Review of Fish Diseases, 5, 25-54.
Eaton, W. D. (1990). Anti-viral activity in four species of salmonids following exposure to poly inosinic: cytidylic acid. Diseases of Aquatic Organisms, 9, 193-198.
Feng, H., Liu, H., Kong, R., Wang, L., Wang, Y., Hu, W., & Guo, Q. (2011). Expression profiles of carp IRF-3/-7 correlate with the up-regulation of RIG-I/MAVS/TRAF3/TBK1, four pivotal molecules in RIG-I signaling pathway. Fish & Shellfish Immunology, 30, 1159-1169.
García, I., Galiana, A., Falcó, A., Estepa, A., & Perez, L. (2011). Characterization of an infectious pancreatic necrosis (IPN) virus carrier cell culture with resistance to superinfection with heterologous viruses. Veterinary Microbiology, 149, 48-55.
Gravell, M., & Malsberger, R. G. (1965). A permanent cell line from the fathead minnow (Pimephales promelas). Annals of the New York Academy of Sciences, 126, 555-565.
Guderley, H. (2004). Metabolic responses to low temperature in fish muscle. Biological Reviews, 79, 409-427.
Haverinen, J., & Vornanen, M. (2007). Temperature acclimation modifies sinoatrial pacemaker mechanism of the rainbow trout heart. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 292, 1023-1032.
Herbomel, P., Thisse, B., & Thisse, C. (2001). Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through an M-CSF receptor-dependent invasive process. Developmental Biology, 238, 274-288.
Hill, B. J., & Way, K. (1995). Serological classification of infectious pancreatic necrosis (IPN) virus and other aquatic birnaviruses. Annual Review of Fish Diseases, 5, 55-77.
Imajoh, M., Hirayama, T., & Oshima, S. I. (2005). Frequent occurrence of apoptosis is not associated with pathogenic infectious pancreatic necrosis virus (IPNV) during persistent infection. Fish & Shellfish Immunology, 18, 163-177.
Jørgensen, J. B., Johansen, A., Hegseth, M. N., Zou, J., Robertsen, B., Collet, B., & Secombes, C. J. (2007). A recombinant CHSE-214 cell line expressing an Mx1 promoter–reporter system responds to both interferon type I and type II from salmonids and represents a versatile tool to study the IFN-system in teleost fish. Fish & Shellfish Immunology, 23, 1294-1303.
Kinkelin, P., & Dorson, M. (1973). Interferon production in rainbow trout (Salmo gairdneri) experimentally infected with Egtved virus. Journal of General Virology, 19, 125-127.
Kochs, G., Reichelt, M., Danino, D., Hinshaw, J. E., & Haller, O. (2005). Assay and Functional Analysis of Dynamin‐Like Mx Proteins. Methods in Enzymology, 404, 632-643.
Kodama, H., Matsuoka, Y., Tanaka, Y., Liu, Y., Iwasaki, T., & Watarai, S. (2004). Changes of C-reactive protein levels in rainbow trout (Oncorhynchus mykiss) sera after exposure to anti-ectoparasitic chemicals used in aquaculture. Fish & Shellfish Immunology, 16, 589-597.
Kraffe, E., Marty, Y., & Guderley, H. (2007). Changes in mitochondrial oxidative capacities during thermal acclimation of rainbow trout Oncorhynchus mykiss: roles of membrane proteins, phospholipids and their fatty acid compositions. Journal of Experimental Biology, 210, 149-165.
Larsen, R., Røkenes, T. P., & Robertsen, B. (2004). Inhibition of infectious pancreatic necrosis virus replication by Atlantic salmon Mx1 protein. Journal of Virology, 78, 7938-7944.
Levy, D. E., & Garcı́a, A. (2001). The virus battles: IFN induction of the antiviral state and mechanisms of viral evasion. Cytokine & Growth Factor Reviews, 12, 143-156.
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method. Methods, 25, 402-408.
Matsuo, A., Oshiumi, H., Tsujita, T., Mitani, H., Kasai, H., Yoshimizu, M., & Seya, T. (2008). Teleost TLR22 recognizes RNA duplex to induce IFN and protect cells from birnaviruses. The Journal of Immunology, 181, 3474-3485.
M'gonigle, R. H. (1941). Acute catarrhal enteritis of salmonid fingerlings. Transactions of the American Fisheries Society, 70, 297-303.
Moss, L. H., & Gravell, M. (1969). Ultrastructure and sequential development of infectious pancreatic necrosis virus. Journal of Virology, 3, 52-58.
Nikoskelainen, S., Bylund, G., & Lilius, E. M. (2004). Effect of environmental temperature on rainbow trout (Oncorhynchus mykiss) innate immunity. Developmental & Comparative Immunology, 28, 581-592.
OIE. (2006). Manual of diagnostic test for aquatic animals. Paris, France: World Organization for Animal Health.
Ortega, C., & Enríquez, R. (2007). Factores asociados a la infección celular por el virus de la necrosis pancreática infecciosa (IPNV). Archivos de Medicina Veterinaria, 39, 7-18.
Ortega, C., Montes de Oca, R. M., Groman, D., Yason, C., Nicholson, B., & Blake, S. (2002). Case report: viral infectious pancreatic necrosis in farmed rainbow trout from Mexico. Journal of Aquatic Animal Health, 14, 305-310.
Padron, D., Bizeau, M. E., & Hazel, J. R. (2000). Is fluid-phase endocytosis conserved in hepatocytes of species acclimated and adapted to different temperatures? American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 278, 529-536.
Pérez-Prieto, S. I. (2003). Infectious pancreatic necrosis virus: biology, pathogenesis, and diagnostic methods. Advances in Virus Research, 62, 113-135.
Platanias, L. C. (2005). Mechanisms of type-I-and type-II-interferon-mediated signalling. Nature Reviews Immunology, 5, 375-386.
Raida, M. K., & Buchmann, K. (2007). Temperature-dependent expression of immune-relevant genes in rainbow trout following Yersinia ruckeri vaccination. Diseases of Aquatic Organisms, 77, 41-52.
Reed, L. J., & Muench, H. (1938). A simple method of estimating fifty per cent endpoints. American Journal of Epidemiology, 27, 493-497.
Roberts, R. J., & Pearson, M. D. (2005). Infectious pancreatic necrosis in Atlantic salmon, Salmo salar L. Journal of Fish Diseases, 28, 383-390.
Roberts, T. E., & Dobos, P. (1983). Studies on the mechanism of temperature sensitivity of infectious pancreatic necrosis virus replication. Journal of General Virology, 64, 331-339.
Robertsen, B. (2006). The interferon system of teleost fish. Fish & Shellfish Immunology, 20, 172-191.
Robertsen, B., Bergan, V., Røkenes, T., Larsen, R., & Albuquerque, A. (2003). Atlantic salmon interferon genes: cloning, sequence analysis, expression, and biological activity. Journal of Interferon & Cytokine Research, 23, 601-612.
Rubio-Godoy, M. (2010). Teleost fish immunology. Revista Mexicana de Ciencias Pecuarias, 1, 43-57.
Ruiz, F. A., & De Blas, I. (2003). Factors affecting the immune response in fish virus infections. AquaTIC, 19, 1-7.
Saint-Jean, S. R., Borrego, J. J., & Pérez-Prieto, S. I. (2003). Infectious Pancreatic Necrosis Virus: Biology, pathogenesis and diagnostic methods. Advances in Virus Research, 62,113-165.
Saint-Jean, S. R., & Pérez-Prieto, S. I. (2007). Effects of salmonid fish viruses on Mx gene expression and resistance to single or dual viral infections. Fish & Shellfish Immunology, 23, 390-400.
Santi, N., Vakharia, V. N., & Evensen, Ø. (2004). Identification of putative motifs involved in the virulence of infectious pancreatic necrosis virus. Virology, 322, 31-40.
Sen, G. C. (2001). Viruses and interferons. Annual Reviews in Microbiology, 55, 255-281.
Skjesol, A., Aamo, T., Hegseth, M. N., Robertsen, B., & Jørgensen, J. B. (2009). The interplay between infectious pancreatic necrosis virus (IPNV) and the IFN system: IFN signaling is inhibited by IPNV infection. Virus Research, 143, 53-60.
Smail, D. A., Bain. N., Bruno, D. W., King, J. A., Thompson, F., Pendrey, D. J., & Cunningham, C. O. (2006). Infectious pancreatic necrosis virus in Atlantic salmon (Salmo salar) post‐smolts in the Shetland Isles, Scotland: virus identification, histopathology, immunohistochemistry and genetic comparison with Scottish mainland isolates. Journal of Fish Diseases, 29, 31-41.
Suzuki, Y., Otaka, T., Sato, S., Hou, Y. Y., & Aida, K. (1997). Reproduction related immunoglobulin changes in rainbow trout. Fish Physiology and Biochemistry, 17, 415-421.
Verrier, E. R., Langevin, C., Benmansour, A., & Boudinot, P. (2011). Early antiviral response and virus-induced genes in fish. Developmental & Comparative Immunology, 3, 1204-1214.
Wolf, K. (1988). Fish viruses and fish viral diseases. US: Comstock Publishing Associates.
Wolf, K. (1966). Infectious pancreatic necrosis (IPN) of salmonid fishes. Fish, 1, 1-8.
Wolf, K., Snieszko, S. F., Dunbar, C. E., & Pyle, E. (1960). Virus nature of infectious pancreatic necrosis in trout. Experimental Biology and Medicine, 104, 105-108.
Wu, Y. C., Lu, Y. F., & Chi, S. C. (2010). Anti-viral mechanism of barramundi Mx against betanodavirus involves the inhibition of viral RNA synthesis through the interference of RdRp. Fish & Shellfish Immunology, 28, 467-475.
Xu, L. G., Wang, Y. Y., Han, K. J., Li, L. Y., Zhai, Z., & Shu, H. B. (2005). VISA is an adapter protein required for virus-triggered IFN-β signaling. Molecular Cell, 19, 727-740.
Zhou, Z., Hamming, O. J., Ank, N., Paludan, S. R., Nielsen, A. L., & Hartmann, R. (2007). Type III interferon (IFN) induces a type I IFN-like response in a restricted subset of cells through signaling pathways involving both the Jak-STAT pathway and the mitogen-activated protein kinases. Journal of Virology, 81, 7749-7758.
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