RNA-Seq analysis of European sea bass (Dicentrarchus labrax L.) infected with nodavirus reveals powerful modulation of the stress response

FAO (2005–2019) Cultured aquatic species information programme: Dicentrarchus labrax. FAO fisheries and aquaculture Department Munday BL, Kwang J, Moody N (2002) Betanodavirus infections of teleost fish: a review. J Fish Dis 25:127–142 Nishizawa T, Furuhashi M, Nagai T, Nakai T, Muroga K (1997) Genomic classification of fish nodaviruses by molecular phylogenetic analysis of the coat protein gene. Appl Environ Microbiol 63:1633–1636 Doan QK, Vandeputte M, Chatain B, Morin T, Allal F (2017) Viral encephalopathy and retinopathy in aquaculture: a review. J Fish Dis 40:717–742 Lu MW, Ngou FH, Chao YM, Lai YS, Chen NY, Lee FY, Chiou PP (2012) Transcriptome characterization and gene expression of Epinephelus spp in endoplasmic reticulum stress-related pathway during betanodavirus infection in vitro. Genomics 13:651 Liu P, Wang L, Kwang J, Yue GH, Wong SM (2016) Transcriptome analysis of genes responding to NNV infection in Asian seabass epithelial cells. Fish Shellfish Immunol 54:342–352 Chaves-Pozo E, Valero Y, Esteve-Codina A, Gómez-Garrido J, Dabad M, Alioto T, Meseguer J, Esteban MA, Cuesta A (2017) Innate cell-mediated cytotoxic activity of European sea bass leucocytes against nodavirus-infected cells: a functional and RNA-seq study. Sci Rep 7:15396 Chen W, Yi L, Feng S, Liu X, Asim M, Zhou Y, Lan J, Jiang S, Tu J, Lin L (2017) Transcriptomic profiles of striped snakehead fish cells (SSN-1) infected with red-spotted grouper nervous necrosis virus (RGNNV) with an emphasis on apoptosis pathway. Fish Shellfish Immunol 60:346–354 Chaves-Pozo E, Bandín I, Olveira JG, Esteve-Codina A, Gómez-Garrido J, Dabad M, Alioto T, Esteban MÁ, Cuesta A (2019) European sea bass brain DLB-1 cell line is susceptible to nodavirus: a transcriptomic study. Fish Shellfish Immunol 1:14–24 Kim JO, Kim JO, Kim WS, Oh MJ (2017) Characterization of the transcriptome and gene expression of brain tissue in Sevenband gouper (Hyporthodus septemfasciatus) in response to NNV infection. Genes 8:E31 Labella AM, Garcia-Rosado E, Bandín I, Dopazo CP, Castro D, Alonso MC, Borrego JJ (2018) Transcriptomic profiles of Senegalese sole infected with nervous necrosis virus reassortants presenting different degree of virulence. Front Immunol 9:1626 Tso CH, Lu MW (2018) Transcriptome profiling analysis of grouper during nervous necrosis virus persistent infection. Fish Shellfish Immunol 76:224–232 Wang L, Tian Y, Cheng M, Li Z, Li S, Wu Y, Zhang J, Ma W, Li W, Pang Z, Zhai J (2019) Transcriptome comparative analysis of immune tissues from asymptomatic and diseased Epinephelus moara naturally infected with nervous necrosis virus. Fish Shellfish Immunol 93:99–107 Poisa-Beiro L, Dios S, Montes A, Aranguren R, Figueras A, Novoa B (2008) Nodavirus increases the expression of Mx and inflammatory cytokines in fish brain. Mol Immunol 45:218–225 Poisa-Beiro L, Dios S, Ahmed H, Vasta GR, Martínez-López A, Estepa A, Alonso-Gutiérrez J, Figueras A, Novoa B (2009) Nodavirus infection of sea bass (Dicentrarchus labrax) induces up-regulation of galectin-1 expression with potential anti-inflammatory activity. J Immunol 183:6600–6611 Sarropoulou E, Sepulcre P, Poisa-Beiro L, Mulero V, Meseguer J, Figueras A, Novoa B, Terzoglou V, Reinhardt R, Magoulas A, Kotoulas G (2009) Profiling of infection specific mRNA transcripts of the European seabass Dicentrarchus labrax. BMC Genomics 10:157 Scapigliati G, Buonocore F, Randelli E, Casani D, Meloni S, Zarletti G, Tiberi M, Pietretti D, Boschi I, Manchado M, Martin-Antonio B, Jimenez-Cantizano R, Bovo G, Borghesan F, Lorenzen N, Einer-Jensen K, Adams S, Thompson K, Alonso C, Bejar J, Cano I, Borrego JJ, Alvarez MC (2010) Cellular and molecular immune responses of the sea bass (Dicentrarchus labrax) experimentally infected with betanodavirus. Fish Shellfish Immunol 28:303 Chaves-Pozo E, Guardiola FA, Meseguer J, Esteban MA, Cuesta A (2012) Nodavirus infection induces a great innate cell-mediated cytotoxic activity in resistant, gilthead seabream, and susceptible, European sea bass, teleost fish. Fish Shellfish Immunol 33:1159–1166 Novel P, Fernandez-Trujillo MA, Gallardo-Galvez JB, Cano I, Manchado M, Buonocore F, Randelli E, Scapigliati G, Alvarez MC, Bejar J (2013) Two Mx genes identified in European sea bass (Dicentrarchus labrax) respond differently to VNNV infection. Vet Immunol Immunopathol 153:240–248 Valero Y, Morcillo P, Meseguer J, Buonocore F, Esteban MA, Chaves-Pozo E, Cuesta A (2015) Characterization of the interferon pathway in the teleost fish gonad against the vertically transmitted nervous necrosis virus. J Gen Virol 96:2176–2187 Buonocore F, Randelli E, Tranfa P, Scapigliati G (2012) A CD83-like molecule in sea bass (Dicentrarchus labrax): molecular characterization and modulation by viral and bacterial infection. Fish Shellfish Immunol 32:1179–1184 Buonocore F, Stocchi V, Nunez-Ortiz N, Randelli E, Gerdol M, Pallavicini A, Facchiano A, Bernini C, Guerra L, Scapigliati G, Picchietti S (2017) Immunoglobulin T from sea bass (Dicentrarchus labrax L.): molecular characterization, tissue localization and expression after nodavirus infection. BMC Mol Biol 18:8 Tort L (2011) Stress and immune modulation in fish. Dev Comp Immunol 35:1366–1375 Bovo G, Nishizawa T, Maltese C, Borghesan F, Mutinelli F, Montesi F, De Mas S (1999) Viral encephalopathy and retinopathy of farmed marine fish species in Italy. Virus Res 63:143–146 Reed LJ, Müench H (1938) A simple method of estimating fifty per cent end-points. Am J Hyg 27:493–497 Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007 Kuo HC, Wang TY, Chen PP, Chen YM, Chuang HC, Chen TY (2011) Real-time quantitative PCR assay for monitoring of nervous necrosis virus infection in grouper aquaculture. J Clin Microbiol 49:1090–1096 Morgan JD, Iwama GK (1996) Cortisol-induced changes in oxygen consumption and ionic regulation in coastal cutthroat trout (Oncorhynchus clarki clarki) parr. Fish Physiol Biochem 15:385–394 Dong XX, Wang Y, Qin ZH (2009) Molecular mechanisms of excitotoxicity and their relevance to pathogenesis of neurodegenerative diseases. Acta Pharmacol Sin 30:379–387 Mennerich D, Kelokumpu S, Kietzmann T (2019) Hypoxia and reactive oxygen species as modulators of endoplasmic reticulum and Golgy homeostasis. Antioxid Redox Signal 30:113–137 Forrester JV, McMenamin PG, Dando SJ (2018) CNS infection and immune privilege. Nat Rev Neurosci 19:655–671 Khansari AR, Parra D, Reyes-López FE, Tort L (2017) Modulatory in vitro effect of stress hormones on the cytokine response of rainbow trout and gilthead sea bream head kidney stimulated with Vibrio anguillarum bacterin. Fish Shellfish Immunol 70:736–749 Benhar I, London A, Schwartz M (2012) The privileged immunity of immune privileged organs: the case of the eye. Front Immunol 3:296 Dios S, Poisa-Beiro L, Figueras A, Novoa B (2007) Suppression subtraction hybridization (SSH) and macroarray techniques reveal differential gene expression profiles in brain of sea bream infected with nodavirus. Mol Immunol 44:2195–2204 Gorissen M, Flik G (2016) The endocrinology of the stress response in fish: an adaptation-physiological view. In: Schreck CB, Tort L, Farrell AP, Brauner CJ (eds) Biology of stress in fish-fish physiology, vol 35. Academic Press, London Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Ann Rev Fish Dis 1:13–26 Heisler LK, Pronchuk N, Nonogaki K, Zhou L, Raber J, Tung L, Yeo GS, O’Rahilly S, Colmers WF, Elmquist JK, Tecott LH (2007) Serotonin activates the hypothalamic-pituitary-adrenal axis via serotonin 2C receptor stimulation. J Neurosci 27:6956–6964 Levy BH, Tasker JG (2012) Synaptic regulation of the hypothalamic–pituitary–adrenal axis and its modulation by glucocorticoids and stress. Front Cell Neurosci 6:24 Liu X, Khansari A, Teles M, Martínez-Rodríguez G, Zhang Y, Mancera JM, Reyes-López FE, Tort L (2019) Brain and pituitary response to vaccination in gilthead seabream (Sparus aurata L.). Front Physiol 10:717 Schreck CB, Tort L (2016) The concept of stress in fish. In: Schreck CB, Tort L, Farrell AP, Brauner CJ (eds) Biology of stress in fish-fish physiology, vol 35. Academic Press, London Yada T, Nakanishi T (2002) Interaction between endocrine and immune systems in fish. Int Rev Cytol 220:35–92 Pijanowski L, Jurecka P, Irnazarow I, Kepka M, Szwejser E, Verburg-van Kemenade BML, Chadzinska M (2015) Activity of the hypothalamus-pituitary-interrenal axis (HPI axis) and immune response in carp lines with different susceptibility to disease. Fish Physiol Biochem 41:1261–1278 Grove S, Johansen R, Reitan LJ, Press CM, Dannevig BH (2006) Quantitative investigation of antigen and immune response in nervous and lymphoid tissues of Atlantic halibut (Hippoglossus hippoglossus) challenged with nodavirus. Fish Shellfish Immunol 21:525–539 López-Muñoz A, Sepulcre MP, García-Moreno D, Fuentes I, Béjar J, Manchado M, Álvarez MC, Meseguer J, Mulero V (2012) Viral nervous necrosis virus persistently replicates in the central nervous system of asymptomatic gilthead seabream and promotes a transient inflammatory response followed by the infiltration of IgM + B lymphocytes. Dev Comp Immunol 37:429–437 Piazzon MC, Galindo-Villegas J, Pereiro P, Estensoro I, Calduch-Giner JA, Gómez-Casado E, Novoa B, Mulero V, Sitjà-Bobadilla A, Pérez-Sánchez J (2016) Differential modulation of IgT and IgM upon parasitic, bacterial, viral, and dietary challenges in a perciform fish. Front Immunol 7:637 Parra D, Reyes-Lopez FE, Tort L (2015) Mucosal immunity and B cells in teleosts: effect of vaccination and stress. Front Immunol 6:354 Yada T, Nagae M, Moriyama S, Azuma T (1999) Effects of prolactin and growth hormone on plasma immunoglobulin M levels of hypophysectomized rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 115:46–52 Chen NC, Yoshimura M, Guan HH, Wang TY, Misumi Y, Lin CC, Chuankhayan P, Nakagawa A, Chan SI, Tsukihara T, Chen TY, Chen CJ (2015) Crystal structures of a piscine betanodavirus: mechanisms of capsid assembly and viral infection. PLoS Pathog 11:e1005203 Jang S, Oh D, Lee Y, Hosy E, Shin H, van Riesen C, Whitcomb D, Warburton JM, Jo J, Kim D, Kim SG, Um SM, Kwon SK, Kim MH, Roh JD, Woo J, Jun H, Lee D, Mah W, Kim H, Kaang BK, Cho K, Rhee JS, Choquet D, Kim E (2016) Synaptic adhesion molecule IgSF11 regulates synaptic transmission and plasticity. Nat Neurosci 19:84–93 Chen J, Kaul S, Simons SS Jr (2002) Structure/activity elements of the multifunctional protein, GMEB-1. Characterization of domains relevant for the modulation of glucocorticoid receptor transactivation properties. J Biol Chem 277:22053–22062 Plotsky PM, Otto S, Sutton S (1987) Neurotransmitter modulation of corticotropin releasing factor secretion into the hypophysial-portal circulation. Life Sci 41:1311–1317 Schulz JB, Matthews RT, Jenkins BG, Ferrante RJ, Siwek D, Henshaw DR, Cipolloni PB, Mecocci P, Kowall NW, Rosen BR (1995) Blockade of neuronal nitric oxide synthase protects against excitotoxicity in vivo. J Neurosci 15:8419–8429 Schonbrunn A, Koch BD (1987) Mechanisms by which somatostatin inhibits pituitary hormone release. In: Reichlin S (ed) somatostatin. Springer, Boston Costanza M, Binart N, Steinman L, Pedotti R (2015) Prolactin: a versatile regulator of inflammation and autoimmune pathology. Autoimmun Rev 14:223–230 Rivero-Segura NA, Flores-Soto E, García de la Cadena S, Coronado-Mares I, Gomez-Verjan JC, Ferreira DG, Cabrera-Reyes EA, Lopes LV, Massieu L, Cerbón M (2017) Prolactin-induced neuroprotection against glutamate excitotoxicity is mediated by the reduction of [Ca2 +]i overload and NF-κB activation. PLoS One 12:e0176910 Gonzalez C, Corbacho AM, Eiserich JP, Garcia C, Lopez-Barrera F, Morales-Tlalpan V, Barajas-Espinosa A, Diaz-Muñoz M, Rubio R, Lin SH, Martinez de la Escalera G, Clapp C (2004) 16K-Prolactin inhibits activation of endothelial nitric oxide synthase, intracellular calcium mobilization, and endothelium-dependent vasorelaxation. Endocrinology 145:5714–5722 Webster JI, Sternberg EM (2004) Role of the hypothalamic-pituitary-adrenal axis, glucocorticoids and glucocorticoid receptors in toxic sequelae of exposure to bacterial and viral products. J Endocrinol 181:207–221 Silverman MN, Pearce BD, Biron CA, Miller AH (2005) Immune modulation of the hypothalamic-pituitary-adrenal (HPA) axis during viral infection. Viral Immunol 18:41–78 Castric J, Thiéry R, Jeffroy J, de Kinkelin P, Raymond J (2001) Sea bream Sparus aurata, an asymptomatic contagious fish host for nodavirus. Dis Aquat Organ 47:33–38