Journal of fish pathology (한국어병학회지)

The Korean Society of Fish Pathology (한국어병학회)
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Characterization of immune gene expression in rock bream (Oplegnathus fasciatus) kidney infected with rock bream iridovirus (RBIV) using microarray

  • Myung-Hwa Jung (Department of MarineBio and Medical Sciences, Hanseo University) ;
  • Sung-Ju Jung (Department of Aqualife Medicine, Chonnam National University)
  • Received : 2023.10.19
  • Accepted : 2023.11.16
  • Published : 2023.12.31
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Abstract

Rock bream iridovirus (RBIV) causes high mortality and economic losses in rock bream (Oplegnathus fasciatus) aquaculture industry in Korea. Although, the immune responses of rock bream under RBIV infection have been studied, there is not much information at the different stages of infection (initial, middle and recovery). Gene expression profiling of rock bream under different RBIV infection stages was investigated using a microarray approaches. In total, 5699 and 6557 genes were significantly up- or down-regulated over 2-fold, respectively, upon RBIV infection. These genes were grouped into categories such as innate immune responses, adaptive immune responses, complements, lectin, antibacterial molecule, stress responses, DNA/RNA binding, energy metabolism, transport and cell cycle. Interestingly, hemoglobins (α and β) appears to be important during pathogenesis; it is highly up-regulated at the initial stage and is gradually decreased when the pathogen most likely multiplying and fish begin to die at the middle or later stage. Expression levels were re-elevated at the recovery stage of infection. Among up-regulated genes, interferon-related genes were found to be responsive in most stages of RBIV infection. Moreover, X-linked inhibitor of apoptosis (XIAP)-associated factor 1 (XAF1) expression was high, whereas expression of apoptosis-relate genes were low. In addition, stress responses were highly induced in the virus infection. The cDNA microarray data were validated using quantative real-time PCR. Our results provide novel inslights into the broad immune responses triggered by RBIV at different infection stages.

Keywords

Acknowledgement

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT & Future Planning (RS-2023-00242225).

References

  1. Kurita, J. and Nakajima, K.: Megalocytiviruses. Viruses, 4: 521-538, 2012. https://doi.org/10.3390/v4040521
  2. Jung, S.J. and Oh, M.J.: Iridovirus-like infection associated with high mortalities of striped beak perch, Oplegnathus fasciatus (Temminck et Schlegel), in southern coastal areas of the Korea peninsula. J Fish Dis, 23: 223-236, 2000. https://doi.org/10.1046/j.1365-2761.2000.00212.x
  3. Jung, M.H., Jung, S.J., Vinay, T.N., Nikapitiya, C., Kim, J.O., Lee, J.H., Lee, J. and Oh, M.J.: Effects of water temperature on mortality in Megalocytivirus-infected rock bream Oplegnathus fasciatus (Temminck et Schlegel) and development of protective immunity. J Fish Dis, 38: 729-737, 2015. https://doi.org/10.1111/jfd.12286
  4. Jung, M.H., Lee, J. and Jung, S.J.: Low pathogenicity of FLIV (flounder iridovirus) and the absence of cross-protection between FLIV and RBIV (rock bream iridovirus). J Fish Dis, 39:1325-1333, 2016. https://doi.org/10.1111/jfd.12459
  5. Jung, M.H., Nikapitiya, C., Vinay, T.N., Lee, J. and Jung, S.J.: Rock bream iridovirus (RBIV) replication in rock bream (Oplegnathus fasciatus) exposed for different time periods to susceptible water temper-atures. Fish Shellfish Immunol, 70:731-735, 2017a. https://doi.org/10.1016/j.fsi.2017.09.038
  6. Jung, M.H., Lee, J., Ortega-Villaizan, M., Perez, L. and Jung, S.J.: Protective immunity against Megalocyti-virus infection in rock bream (Oplegnathus fasciatus) following CpG ODN administration. Vaccine, 35: 3691-3699, 2017b. https://doi.org/10.1016/j.vaccine.2017.05.073
  7. Jung, M.H. and Jung, S.J.: Protective immunity against rock bream iridovirus (RBIV) infection and TLR3-mediated type I interferon signaling pathway in rock bream (Oplegnathus fasciatus) following poly (I:C) administration. Fish. Shellfish Immunol, 67: 293-301, 2017a. https://doi.org/10.1016/j.fsi.2017.06.026
  8. Jung, M.H., Nikapitiya, C. and Jung, S.J.: DNA vaccine encoding myristoylated membrane protein (MMP) of rock bream iridovirus (RBIV) induces protective immunity in rock bream (Oplegnathus fasciatus). Vaccine, 36: 802-810, 2018. https://doi.org/10.1016/j.vaccine.2017.12.077
  9. Jung, M.H., Nikapitiya, C., Song, J.Y., Lee, J.H., Lee, J., Oh, M.J. and Jung, S.J.: Gene expression of proand anti-apoptotic proteins in rock bream (Oplegnathus fasciatus) infected with Megalocytivirus (family Iridoviridae). Fish. Shellfish Immunol, 37: 122-130, 2014. https://doi.org/10.1016/j.fsi.2014.01.012
  10. Nikapitiya, C., Jung, S.J., Jung, M.H., Song, J.Y., Lee, J., Lee, J.H. and Oh, M.J.: Identification and Molecular Characterization of Z/ZE Lineage MHC Class I Heavy Chain Homologue and β2-micro-globulin from Rock Bream Oplegnathus fasciatus. Fish. Pathol, 49: 93-112, 2014. https://doi.org/10.3147/jsfp.49.93
  11. Hong, S., Jin, J.W., Park, J.H.; Kim, J.K. and Jeong, D.H.: Analysis of proinflammatory gene expression by RBIV infection in rock bream, Oplegnathus faciatus. Fish. Shellfish Immunol, 50: 317-326, 2016. https://doi.org/10.1016/j.fsi.2015.09.002
  12. Jung, M.H. and Jung, S.J.: CpG ODN 1668 induce in-nate and adaptive immune responses in rock bream (Oplegnathus fasciatus) against rock bream iridovirus (RBIV) infection. Fish. Shellfish Immunol, 69:247-257, 2017b. https://doi.org/10.1016/j.fsi.2017.08.030
  13. Jung, M.H. and Jung, S.J.: Gene expression regulation of the TLR9 and MyD88-dependent pathway in rock bream against rock bream iridovirus (RBIV) infection. Fish. Shellfish Immunol, 70: 507-514, 2017c. https://doi.org/10.1016/j.fsi.2017.09.036
  14. Jung, M.H. and Jung, S.J.: Innate immune responses against rock bream iridovirus (RBIV) infection in rock bream (Oplegnathus fasciatus) following poly (I:C) administration. Fish. Shellfish Immunol, 71: 171-176, 2017d. https://doi.org/10.1016/j.fsi.2017.10.002
  15. Hori, T.S., Gamperl, A.K., Booman, M., Nash, G.W. and Rise, M.L.: A moderate increase in ambient temperature modulates the Atlantic cod (Gadus morhua) spleen transcriptome response to intraperitoneal viral mimic injection. BMC genomics, 13: 431, 2012. https://doi.org/10.1186/1471-2164-13-431
  16. Burnside, J., Neiman, P., Tang, J., Basom, R., Talbot, R., Aronszajn, M., Burt, D. and Delrow, J.: Development of a cDNA array for chicken gene expression analysis. BMC genomics, 6:13, 2005. https://doi.org/10.1186/1471-2164-6-13
  17. Fagutao, F.F., Maningas, M.B.B., Kondo, H., Aoki, T. and Hirono, I.: Transglutaminase regulates immunerelated genes in shrimp, Fish. Shellfish Immunol, 32: 711-715, 2012. https://doi.org/10.1016/j.fsi.2012.01.018
  18. Lua, D.T., Yasuike, M., Hirono, I. and Aoki, T.: Transcription program of red sea bream iridovirus as revealed by DNA microarrays, J. Virol, 79, 15151-64, 2005. https://doi.org/10.1128/jvi.79.24.15151-15164.2005
  19. Thanasaksiri, K., Hirono, I. and Kondo, H.: Temperature-dependent regulation of gene expression in poly (I:C)-treated Japanese flounder, Paralichthys olivaceus, Fish. Shellfish Immunol, 45: 835-840, 2015. https://doi.org/10.1016/j.fsi.2015.05.036
  20. Cho, H.K., Kim, J., Moon, J.Y., Nam, B.H., Kim, Y.O., Kim, W.J., Park, J.Y., An, C.M., Cheong, J. and Kong, H.J.: Microarray analysis of gene expression in olive flounder liver infected with viral haemorrhagic septicaemia virus (VHSV), Fish. Shellfish Immunol, 49: 66-78, 2016. https://doi.org/10.1016/j.fsi.2015.11.031
  21. Romero, A., Forn-Cuni, G., Moreira, R., Milan, M., Bargelloni, L., Figueras, A. and Novoa, B,: An immune-enriched oligo-microarray analysis of gene expression in Manila clam (Venerupis philippinarum) haemocytes after a Perkinsus olseni challenge, Fish. Shellfish Immunol, 43: 275-286, 2015. https://doi.org/10.1016/j.fsi.2014.12.029
  22. Xu, D., Wei, J., Cui, H., Gong, J., Yan, Y., Lai, R. and Qin, Q.: Differential profiles of gene expression in grouper Epinephelus coioides, infected with Singa-pore grouper iridovirus, revealed by suppression subtractive hybridization and DNA microarray, J. Fish. Biol, 77: 341-360, 2010. https://doi.org/10.1111/j.1095-8649.2010.02676.x
  23. Jung, M.H., Song, J.Y. and Jung, S.J.: Transcriptional profiles of rock bream iridovirus (RBIV) using microarray approaches. Fish. Pathol, 35(2): 141-155, 2022. https://doi.org/10.7847/jfp.2022.35.2.141
  24. Kwon, M.G., Kim, J.W., Park, M., Hwang, J.Y., Choi, H.S., Kim, M.C., Park, D.W., Jung, J.M. and Park, C.I.: Microarray analysis of gene expression in peripheral blood leucocytes from rock bream (Oplegnathus fasciatus) after stimulation by LPS, ConA/PMA, and poly I:C. Genes. Genomics, 35: 343-353, 2013. https://doi.org/10.1007/s13258-012-0001-4
  25. Livak, K.J. and Schmittgen, T.D.: Analysis of relative gene expression data using real time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 25: 402-408, 2001. https://doi.org/10.1006/meth.2001.1262
  26. Medzhitov, R. Toll-like receptors and innate immunity. Nat. Rev. Immunol, 1: 135, 2001. https://doi.org/10.1038/35100529
  27. Takeda, K., Kaisho, T. and Akira, S.: Toll-like receptors. Ann. Rev. Immunol, 21: 335-376, 2003. https://doi.org/10.1146/annurev.immunol.21.120601.141126
  28. Akira, S. and Takeda, K.: Toll-like receptor signalling. Nat Rev Immunol, 4: 499-511, 2004. https://doi.org/10.1038/nri1391
  29. Oshiumi, H., Matsumoto, M., Funami, K., Akazawa, T. and Seya, T.: TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction, Nat. Immunol, 4: 161-167, 2003. https://doi.org/10.1038/ni886
  30. El-Omar, E.M., Carrington, M., Chow, W.H., McColl, K.E., Bream, J.H., Young, H.A., Herrera, J., Lissowska, J., Yuan, C.C., Rothmam, N., Lanyon, G., Martin, M., Fraumeni Jr, J.F. and Rabkin, C.S.: Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature, 404: 398, 2000. https://doi.org/10.1038/35006081
  31. Baggiolini, M., Dewald, B., Moser, B.: Human chemo-kines: an update. Annual review of immunology, 15(1): 675-705, 1997. https://doi.org/10.1146/annurev.immunol.15.1.675
  32. Zhang, Y.B. and Gui, J.F.: Molecular regulation of interferon antiviral response in fish. Dev Comp Immunol, 38: 193-202, 2012. https://doi.org/10.1016/j.dci.2012.06.003
  33. Schneider, W.M., Chevillotte, M.D. and Rice, C.M.: Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol, 32: 513-545, 2014. https://doi.org/10.1146/annurev-immunol-032713-120231
  34. Zou, J., Tafalla, C., Truckle, J. and Secombes, C.J.: Identification of a second group of type I IFNs in fish sheds light on IFN evolution in vertebrates. J. Immunol, 179: 3859-3871, 2007. https://doi.org/10.4049/jimmunol.179.6.3859
  35. Kitao, Y., Kono, T., Korenaga, H., Iizasa, T., Nakamura, K. and Savan, R.: Characterization and expression analysis of type I interferon in common carp Cyprinus carpio L. Molecular Immunol, 46: 2548-2556, 2009. https://doi.org/10.1016/j.molimm.2009.05.012
  36. Chen, Y.M., Su, Y.L., Lin, J.H.Y., Yang, H.L. and Chen, T.Y.: Cloning of an orange-spotted grouper (Epine-phelus coioides) Mx cDNA and characterisation of its expression in response to nodavirus. Fish. Shellfish Immunol, 20: 58-71, 2006. https://doi.org/10.1016/j.fsi.2005.04.001
  37. Larsen, R., Rokenes, T.P. and Robertsen, B.: Inhibition of infectious pancreatic necrosis virus replication by Atlantic salmon Mx1 protein. J. Virol, 78: 7938-7944, 2004. https://doi.org/10.1128/jvi.78.15.7938-7944.2004
  38. Lin, C.H., John, J.A.C., Lin, C.H. and Chang, C.Y.: Inhibition of nervous necrosis virus propagation by fish Mx proteins. Biochem. Bioph. Res. Co, 351: 534-539, 2006. https://doi.org/10.1016/j.bbrc.2006.10.063
  39. Caipang, C.M.A., Hirono, I. and Aoki, T.: In vitro in-hibition of fish rhabdoviruses by Japanese flounder, Paralichthys olivaceus Mx. Virology, 317: 373-382, 2003. https://doi.org/10.1016/j.virol.2003.08.040
  40. Avunje, S., Kim, W.S., Park, C.S., Oh, M.J. and Jung, S.J.: Toll-like receptors and interferon associated immune factors in viral haemorrhagic septicaemia virus-infected olive flounder (Paralichthys olivaceus). Fish. Shellfish Immunol, 31: 407-414, 2011. https://doi.org/10.1016/j.fsi.2011.06.009
  41. Zhang, J., Tang, X., Sheng, X., Xing, J. and Zhan, W.: The influence of temperature on viral replication and antiviral-related genes response in hirame rhabdovirus-infected flounder (Paralichthys olivaceus). Fish. Shellfish Immunol, 68: 260-265, 2017. https://doi.org/10.1016/j.fsi.2017.07.029
  42. Uribe, C., Folch, H., Enriquez, R. and Moran, G.: Innate and adaptive immunity in teleost fish: A review. Vet. Med, 56: 486-503, 2011. DOI: 10.17221/3294-VETMED
  43. Klein, J.: Natural History of the Major Histocompatibility Complex, Wiley. New York, 60: 621, 1986. https://lccn.loc.gov/85029420
  44. Monac, J.J.: A molecular model of MHC class-I re-stricted antigen processing, Immunol Today, 13:173-179, 1992. https://doi.org/10.1016/0167-5699(92)90122-N
  45. Sun, E.W. and Shi, Y.F.: Apoptosis: the quiet death silences the immune system. Pharmacol Therapeut, 92: 135-145, 2001. https://doi.org/10.1016/S0163-7258(01)00164-4
  46. Hughes, F.M., Foster, B., Grewal, S. and Sokolova, I.M.: Apoptosis as a host defense mechanism in Crassostrea virginica and its modulation by Perkinsus marinus. Fish. Shellfish Immunol, 29: 247-257, 2010. https://doi.org/10.1016/j.fsi.2010.03.003
  47. Sunila, I. and LaBanca, J.: Apoptosis in the pathogenesis of infectious diseases of the eastern oyster Crassostrea virginica. Dis. Aquat. Org, 56: 163-170, 2003. https://doi:10.3354/dao056163
  48. Liston, P., Fong, W.G., Kelly, N.L., Toji, S., Miyazaki, T., Conte, D., Tamai, K., Craig, C.G., McBurney, M.W and Koneluk, R.G.: Identification of XAF1 as an antagonist of XIAP anti-Caspase activity. Nat. Cell. Biol, 3: 128, 2001. https://doi.org/10.1038/35055027
  49. Guo, C., Yan, Y., Cui, H., Huang, X. and Qin, Q.: miR-homoHSV of Singapore grouper iridovirus (SGIV) inhibits expression of the SGIV pro-apoptotic factor LITAF and attenuates cell death. PloS one, 8: e83027, 2013. https://doi.org/10.1371/journal.pone.0083027
  50. Anthea, M., Hopkins, J., McLaughlin, C.W., Johnson, S., Warner, M.Q. and LaHart, D.: Human Biology and Health, Prentice Hall, Englewood Cliffs, NJ, USA, 1993, https://www.worldcat.org/title/humanbiology-and-health/oclc/32308337.
  51. Nishi, H., Inagi, R., Kato, H., Tanemoto, M., Kojima, I., Son, D., Fujita, T. and Nangaku, M.: Hemoglobin is expressed by mesangial cells and reduces oxidant stress. J Am Soc Nephrol, 19: 1500-1508, 2008. https://doi: 10.1681/ASN.2007101085
  52. Liu, W., Baker, S.S., Baker, R.D., Nowak, N.J. and Zhu, L.: Upregulation of hemoglobin expression by oxidative stress in hepatocytes and its implication in nonalcoholic steatohepatitis. PLoS One, 6: e24363, 2011. https://doi.org/10.1371/journal.pone.0024363
  53. Li, X., Wu, Z., Wang, Y., Mei, Q., Fu, X. and Han, W.: Characterization of adult α-and β-globin elevated by hydrogen peroxide in cervical cancer cells that play a cyto-protective role against oxidative insults. PLoS One, 8: e54342, 2013. https://doi.org/10.1371/journal.pone.0054342
  54. Tezel, T.H., Geng, L., Lato, E.B., Schaal, S., Liu, Y., Dean, D., Klein, J.B. and Kaplan, H.J.: Synthesis and secretion of hemoglobin by retinal pigment epithelium. Invest Ophth Vis Sci, 50: 1911-1919, 2009. https://doi.org/10.1167/iovs.07-1372
  55. Grek, C., Newton, D., Spyropoulos, D. and Baatz, J.: Hypoxia up-regulates expression of hemoglobin in alveolar epithelial cells. Am J Resp Cell Mol, 44: 439-447, 2011. https://doi.org/10.1165/rcmb.2009-0307OC
  56. Russo, R., Zucchelli, S., Codrich, M., Marcuzzi, F., Verde, C. and Gustincich, S.: Hemoglobin is present as a canonical α 2 β 2 tetramer in dopaminergic neurons. BBA-Proteins Proteom, 1834: 1939-1943, 2013. https://doi.org/10.1016/j.bbapap.2013.05.005
  57. Zhou, W., Zhang, Y., Wen, Y., Ji, W., Zhou, Y., Ji, Y., Liu, X., Wang, W., Asim, W., Liang, X., Ai, T. and Lin, L.: Analysis of the transcriptomic profilings of Mandarin fish (Siniperca chuatsi) infected with Flavobacterium columnare with an emphasis on immune responses. Fish. Shellfish Immunol, 43: 111-119, 2015. https://doi.org/10.1016/j.fsi.2014.12.006
  58. Dettleff, P., Moen, T., Santi, N. and Martinez, V.: Transcriptomic analysis of spleen infected with infectious salmon anemia virus reveals distinct pattern of viral replication on resistant and susceptible Atlantic salmon (Salmo salar). Fish. Shellfish Immunol, 61: 187-193, 2017. https://doi.org/10.1016/j.fsi.2017.01.005
  59. Dunkelberger, J.R. and Song, W.C.: Complement and its role in innate and adaptive immune responses. Cell Research, 20: 34, 2010. https://doi.org/10.1038/cr.2009.139
  60. Molina, H., Holers, V.M., Li, B., Fung, Y., Mariathasan, S., Goellner, J., Strauss-Schoenberger, J., Karr, R.W. and Chaplin, D.D.: Markedly impaired humoral immune response in mice deficient in complement receptors 1 and 2. P Natl A Sci, 93: 3357-3361, 1996. https://doi.org/10.1073/pnas.93.8.3357
  61. Sunyer, J.O and Lambris, J.D.: Evolution and diversity of the complement system of poikilothermic verte-brates. Immunol Rev, 166: 39-57, 1998. https://doi.org/10.1111/j.1600-065X.1998.tb01251.x
  62. Beckmann, R.P., Mizzen, L.E. and Welch, W.I.: Interaction of Hsp 70 with newly synthesized proteins: implications for protein folding and assembly. Science, 248: 850-854, 1990. https://doi.org/10.1126/science.2188360
  63. Forsyth, R.B., Candido, E.P.M., Babich, S.L. and Iwama, G.K.: Stress protein expression in coho salmon with bacterial kidney disease. J Aquat Anim Health, 9: 18, 1997. https://doi.org/10.1577/1548-8667(1997)009<0018:SPEICS>2.3.CO;2
  64. Ackerman, P.A. and Iwama, G.K.: Physiological and cellular stress responses of juvenile rainbow trout to vibriosis. J Aquat Anim Health, 13: 173, 2001. https://doi.org/10.1577/1548-8667(2001)013<0173:PACSRO>2.0.CO;2
  65. Deane, E.E. and Woo, N.Y.S.: Evidence for disruption of Na+-K+-ATPase and hsp70 during vibriosis of sea bream, Sparus (= Rhabdosargus) sarba Forsskal. J Fish Dis, 28: 239-251, 2005. https://doi.org/10.1111/j.1365-2761.2005.00624.x
  66. Dong, C., Zhang, Y., Zhang, Q. and Gui, J.: Differential expression of three Paralichthys livaceus Hsp40 genes in responses to virus infection and heat shock. Fish. Shellfish Immunol, 21: 146-158, 2006. https://doi.org/10.1016/j.fsi.2005.11.002
  67. Yokoyama, Y., Hashimoto, H., Kubota, S., Kinoshita, M., Toyohara, H., Sakaguchi, M., Tanaka, M., Seikai, T. and Kanamori, M.: cDNA cloning of heat-inducible HSP70, a 70.6 kDa heat shock protein, in Japanese flounder Paralichtys olivaceus. Fish Sci, 64: 964-968, 1998. https://doi.org/10.2331/fishsci.64.964