Abstract
This study focuses on the relationship between myostatin (MyoS), myogenin (MyoG), and the growth hormone/insulin-like growth factor-1 (GH/IGF-1) axis for muscle growth and histopathological changes in muscle after an Aeromonas hydrophila infection. A total number of 90 Nile tilapia (55.85 g) were randomly allocated into two equal groups of three replicates each. The first group was an uninfected control group that was injected intraperitoneally (ip) with 0.2 ml phosphate buffer saline (PBS), while the second group was injected ip with 0.2 ml (1.3 × 108 CFU/ml) Aeromonas hydrophila culture suspension. Sections of white muscle and liver tissues were taken from each group 24 h, 48 h, 72 h, and 1 week after infection for molecular analysis and histopathological examination. The results revealed that with time progression, the severity of muscle lesions increased from edema between bundles and mononuclear inflammatory cell infiltration 24 h post-challenge to severe atrophy of muscle bundles with irregular and curved fibers with hyalinosis of the fibers 1 week postinfection. The molecular analysis showed that bacterial infection was able to induce the muscle expression levels of GH with reduced ILGF-1, MyoS, and MyoG at 24 h postinfection. However, time progression postinfection reversed these findings through elevated muscle expression levels of MyoS with regressed expression levels of muscle GH, ILGF-1, and MyoG. There have been no previous reports on the molecular expression analysis of the aforementioned genes and muscle histopathological changes in Nile tilapia following acute Aeromonas hydrophila infection. Our findings, collectively, revealed that the up-and down-regulation of the myostatin signaling is likely to be involved in the postinfection-induced muscle wasting through the negative regulation of genes involved in muscle growth, such as GH, ILGF-1, and myogenin, in response to acute Aeromonas hydrophila infection in Nile tilapia, Oreochromis niloticus.
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All data generated or analyzed during this study are included in this published article (tables and figures).
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All data generated or analyzed during this study are included in this published article (tables and figures).
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References
Abdelhamed H, Ibrahim I, Baumgartner W, Lawrence ML, Karsi A (2017) Characterization of histopathological and ultrastructural changes in channel catfish experimentally infected with virulent Aeromonas hydrophila. Front Microbiol 8:1–15
Abo-Raya MH, Alshehri KM, Abdelhameed RFA, Elbialy ZI, Elhady SS, Mohamed RA (2021) Assessment of growth related parameters and immune-biochemical profile of Nile tilapia (oreochromis niloticus) fed dietary ulva fasciata extract. Aquac Res 1–14. https://doi.org/10.1111/are.15169
Aedo JE, Reyes AE, Avendaño-Herrera R, Molina A, Valdés JA (2015) Bacterial lipopolysaccharide induces rainbow trout myotube atrophy via Akt/FoxO1/Atrogin-1 signaling pathway. Acta Biochim Biophys Sin 47:932–937
Aluru N, Vijayan MM (2009) Stress transcriptomics in fish: a role for genomic cortisol signaling. Gen Comp Endocrinol 164:142–150
AlYahya SA, Ameen F, Al-Niaeem KS, Al-Sa’adi BA, Hadi S, Mostafa AA (2018) Histopathological studies of experimental Aeromonas hydrophila infection in blue tilapia, Oreochromis aureus. Saudi J Biol Sci 25(1):182–185. https://doi.org/10.1016/j.sjbs.2017.10.019
AsghariHanjani N, Vafa M (2019) The role of IGF-1 in obesity, cardiovascular disease, and cancer. Med J Islam Repub Iran 33:56
Ashley PJ (2007) Fish welfare: current issues in aquaculture. Appl Anim Behav Sci 104:199–235
Avnimelech Y (2009) Biofloc technology. A practical guide book. The World Aquaculture Society, Baton Rouge, p 182
Bancroft JD, Layton C (2013) The hematoxylin and eosin. In: Suvarna SK, Layton C, Bancroft JD (eds) theory practice of histological techniques, 7th edn. Philadelphia, PA, USA, Churchill Livingstone of ElSevier, pp 179–220
Baskin KK, Winders BR, Olson EN (2015) Muscle as a “mediator” of systemic metabolism. Cell Metab 21:237–248
Beaz-Hidalgo R, Figueras MJ (2013) Aeromonas spp. whole genomes and virulence factors implicated in fish disease. J Fish Dis 36:371–388
Biga PR, Cain KD, Hardy RW, Schelling GT, Overturf K, Roberts SB, Goetz FW, Ott TL (2004) Growth hormone differentially regulates muscle myostatin1 and -2 and increases circulating cortisol in rainbow trout (Oncorhynchus mykiss. Gen Comp Endocrinol 138:32–41
Björnsson BTh, Johansson V, Benedet S, Einarsdottir IE, Hildahl J, Agustsson T, Jönsson E (2002) Growth hormone endocrinology of salmonids: regulatory mechanisms and mode of action. Fish Physiol Biochem 27:227–242
Bodine CS, Furlow JD (2015) Glucocorticoids in skeletal muscle. In: Wang, J.-C., Harris, C. (Eds.), Glucocorticoid Signaling. 872 Advances in Experimental Medicine and Biology. https://doi.org/10.1007/978-1-4939-2895-8_7
Bonaldo P, Sandri M (2013) Cellular and molecular mechanisms of muscle atrophy. Dis Model Mech 6(1):25–39. https://doi.org/10.1242/dmm.010389
Bower NI, Johnston IA (2010) Transcriptional regulation of the IGF signaling pathway by amino acids and insulin-like growth factors during myogenesis in Atlantic salmon. PLoS One 5(6):e11100. https://doi.org/10.1371/journal.pone.0011100
Braun TP, Marks DL (2015) The regulation of muscle mass by endogenous glucocorticoids. Front Physiol 6:12. https://doi.org/10.3389/fphys.2015.00012
Buhl M, Bosnjak E, Vendelbo MH, Gjedsted J, Nielsen RR, Hafstrøm TK, Vestergaard ET, Jessen N, Tonnesen E, Moller AB et al (2013) Direct effects of locally administered lipopolysaccharide on glucose, lipid, and protein metabolism in the placebo-controlled, bilaterally infused human leg. J Clin Endocrinol Metab 98:2090–2099
Butler AA, Le Roith D (2001) Control of growth by the somatropic axis: growth hormone and the insulin-like growth factors have related and independent roles. Annu Rev Physiol 63:141–164
Carnevali O, de Vivo L, Sulpizio R, Silvi GS, Cresci A (2006) Growth improvement by probiotic in European sea bass juveniles (Dicentrarchus labrax, L.) with particular attention to IGF-1, myostatin, and cortisol gene expression. Aquaculture 258:430–438
Carrizo V, Valenzuela CA, Aros C, Dettleff P, Valenzuela-Muñoz V, Gallardo-Escarate C, Altamirano C, Molina A, Valdés JA (2021) Transcriptomic analysis reveals a Piscirickettsia salmonis-induced early inflammatory response in rainbow trout skeletal muscle. Comp Biochem Physiol Part D Genom Proteom 39:100859
Carrizo V, Valenzuela CA, Zuloaga R, Aros C, Altamirano C, Valdés JA, Molina A (2021) Effect of cortisol on the immune-like response of rainbow trout (Oncorhynchus mykiss) myotubes challenged with Piscirickettsia salmonis. Vet Immunol Immunopathol 237:110240
Carrizo V, Valenzuela CA, Zuloaga R, Aros C, Altamirano C, Valdés JA, Molina A (2021) Effect of cortisol on the immune-like response of rainbow trout (Oncorhynchus mykiss) myotubes challenged with Piscirickettsia salmonis. Vet Immunol Immunopathol 237:110240
Chisada S-I, Okamoto H, Taniguchi Y, Kimori Y, Toyoda A, Sakaki Y, Takeda S, Yoshiura Y (2011) Myostatin-deficient medaka exhibit a double-muscling phenotype with hyperplasia and hypertrophy, which occur sequentially during post-hatch development. Dev Biol 359:82–94
Costa LS, Rosa PV, Fortes-Silva R, Sánchez-Vázquez FJ, López –Olmeda JF (2015) Daily rhythms of the expression of genes from the somatotropic axis: the influence on tilapia (Oreochromisniloticus) of feeding and growth hormone administration at different times. Comp Biochem Physiol C. https://doi.org/10.1016/j.cbpc.2015.12.008
De Santis C, Jerry DR (2011) Differential tissue-regulation of myostatin genes in the teleost fish Lates calcarifer in response to fasting. Evidence for functional differentiation. Mol Cell Endocrinol 335(2):158–165. https://doi.org/10.1016/j.mce.2011.01.011
Dehkhoda F, Lee CMM, Medina J, Brooks AJ (2018) The growth hormone receptor: mechanism of receptor activation, cell signaling, and physiological aspects. Front Endocrinol 9(35):1–23. https://doi.org/10.3389/fendo.2018.00035
Dong HT, Techatanakitarnan C, Jindakittikul P, Thaiprayoon A, Taengphu S, Charoensapsri W, Khunrae P, Rattanarojpong T, Senapin S (2017) Aeromonas jandaei and Aeromonas veronii caused disease and mortality in Nile tilapia, Oreochromis niloticus (L.). J Fish Dis 40(10):1395–1403. https://doi.org/10.1111/jfd.12617
Duran BOS, Zanella BTT, Perez ES, Mareco EA, Blasco J, Dal-Pai-Silva M, Garcia de la serrana D (2022) Amino acids and IGF1 regulation of fish muscle growth revealed by transcriptome and microRNAome integrative analyses of Pacu (Piaractus mesopotamicus) myotubes. Int J Mol Sci 23:1180. https://doi.org/10.3390/ijms23031180
Elbialy ZI, Salah AS, Elsheshtawy A, Rizk M, Abualreesh MH, Abdel-Daim MM, Salem SMR, Askary AE, Assar DH (2021) Exploring the multimodal role of Yucca schidigera extract in protection against chronic ammonia exposure targeting: growth, metabolic, stress and inflammatory responses in Nile tilapia (Oreochromis niloticus L.). Animals 11:2072. https://doi.org/10.3390/ani11072072
Elkatatny NA, Elbialy ZI, El-Nahas AF, Mahmoud S (2016) Characterization of Myostatin gene in Nile tilapia (Oreochromisniloticus), the possible association of BsmI-exon 2 polymorphism with its growth. Am J Life Sci 4(3):82–86
FAO (2020) Sustainability in action. State of World Fisheries and Aquaculture. Rome. https://doi.org/10.4060/ca9229en
Galt NJ, McCormick SD, Froehlich JM, Biga PR (2016) A comparative examination of cortisol effects on muscle myostatin and HSP90 gene expression in salmonids. Gen Comp Endocrinol 237:19–26. https://doi.org/10.1016/j.ygcen.2016.07.019
Gao J, Xi B, Chen K, Song R, Qin T, Xie J, Pan L (2018) The stress hormone norepinephrine increases the growth and virulence of Aeromonas hydrophila. Microbiology Open 8:e664. https://doi.org/10.1002/mbo3.664
Ghatak S, Blom J, Das S, Sanjukta R, Puro K, Mawlong M, Shakuntala I, Sen A et al (2016) Pan-genome analysis of Aeromonas hydrophila, Aeromonas veronii and Aeromonas caviae indicates phylogenomic diversity and greater pathogenic potential for Aeromonas hydrophila. Anton Leeuw 109:945–956
Gilson H, Schakman O, Combaret L, Lause P, Grobet L, Attaix D, Ketelslegers JM, Thissen JP (2007) Myostatin gene deletion prevents glucocorticoid-induced muscle atrophy. Endocrinology 148:452–460
Granado M, Martin AI, Lopez-Menduina M, Lopez-Calderon A, Villanua MA (2008) GH-releasing peptide-2 administration prevents liver inflammatory response in endotoxemia. Am J Physiol Endocrinol Metab 294:E131–E141
Hamid NH, Hassan MD, Sabri MYM, Hasliza AH, Hamdan RH, Afifah MNF, Raina MS, Nadia ABS, Fuad MM (2017) Studies on pathogenicity effect of Aeromonas hydrophila infection in juvenile red hybrid tilapia Oreochromis sp. In: Proceedings of International Seminar on Livestock Production and Veterinary Technology, 532–539
Handfield M, Simard P, Couillard M, Letarte R (1996) Aeromonas hydrophila isolated from food and drinking water: hemagglutination, hemolysis, and cytotoxicity for a human intestinal cell line (HT-29). Appl Environ Microbiol 62:3459–3461
Hargreaves JA (2013) Biofloc production systems for aquaculture (Vol. 4503). Southern Regional Aquaculture Center Stoneville, MS, p 11
Helterline DL, Garikipati D, Stenkamp DL, Rodgers BD (2007) Embryonic and tissue-specific regulation of myostatin-1 and -2 gene expression in zebrafish. Gen Comp Endocrinol 151:90–97
Hennebry A, Oldham J, Shavlakadze T, Grounds MD, Sheard P, Fiorotto ML, Falconer S, Smith HK, Berry C, Jeanplong F et al (2017) IGF1 stimulates greater muscle hypertrophy in the absence of myostatin in male mice. J Endocrinol 234:187–200
Hossain MJ, Sun DW, McGarey DJ, Wrenn S, Alexander LM, Martino ME, Liles MR (2014) An asian origin of virulent Aeromonas hydrophila responsible for disease epidemics in united states-farmed catfish. Mbio 5:e00848-e914. https://doi.org/10.1128/mBio.00848-14
Iturriaga M, Espinoza MB, Poblete-Morales M, Feijoo CG, Reyes AE, Molina A, Avendaño-Herrera R, Valdés JA (2017) Cytotoxic activity of Flavobacterium psychrophilum in skeletal muscle cells of rainbow trout (Oncorhynchus mykiss). Vet Microbiol 210:101–106
Jeschke MG, Herndon DN (2004) Effect of growth factors as therapeutic drugs on hepatic metabolism during the systemic inflammatory response syndrome. Curr Drug Metab 5:399–413
Johansen KA, Overturf K (2006) Alterations in expression of genes associated with muscle metabolism and growth during nutritional restriction and refeeding in rainbow trout. Comp Biochem Physiol B Biochem Mol Biol 144(1):119–127. https://doi.org/10.1016/j.cbpb.2006.02.001
Johnston IA (2001) Genetic and environmental determinants of muscle growth patterns. In Muscle Development and Growth; Johnston, I.A., Ed.; Academic Press: Cambridge, MA, USA, 2001; pp. 141–186. 2
Johnston IA (2006) Environment and plasticity of myogenesis in teleost fish. J Exp Biol 209:2249–2264
Johnston IA, Bower NI, Macqueen DJ (2011) Growth and the regulation of myotomal muscle mass in teleost fish. J Exp Biol 214(Pt 10):1617–1628. https://doi.org/10.1242/jeb.038620
Kishimoto K, Washio Y, Yoshiura Y, Toyoda A, Ueno T, Fukuyama H et al (2018) Production of a breed of red sea bream Pagrus major with an increase of skeletal muscle mass and reduced body length by genome editing with CRISPR/Cas9. Aquaculture 495:415–427. https://doi.org/10.1016/j.aquaculture.2018.05.055
Kumar R, Pande V, Singh L, Sharma L, Saxena N, Thakuria D, Singh AK, Sahoo PK (2016) Pathological findings of experimental Aeromonas hydrophila infection in golden mahseer (Tor putitora). Fish Aquac J 7:1. https://doi.org/10.4172/2150-3508.1000160
Lang CH, Silvis C, Nystrom G, Frost RA (2001) Regulation of myostatin by glucocorticoids after thermal injury. FASEB J 15:1807–1809
Lee SB, Kim YS, Oh MY, Jeong IH, Seong KB, Jin HJ (2010) Improving rainbow trout (Oncorhynchus mykiss) growth by treatment with a fish (Paralichthys olivaceus) myostatin prodomain expressed in soluble forms in E. coli. Aquaculture 302:270–278
Li J, Zhang XL, Liu YJ, Lu CP (2011) Development of an Aeromonas hydrophila infection model using the protozoan Tetrahymena thermophila. FEMS Microbiol Lett 316:160–168. https://doi.org/10.1111/j.1574-6968.2010.02208.x
Lima ECS, Povh JA, Otonel RAA, Leonhardt JH, Alfieri AA, Headley SA et al (2017) Morphology and muscle gene expression in GIFT and supreme Nile tilapia varieties reared in two cultivation systems. Genet Mol Res 16:gmr16019407. https://doi.org/10.4238/gmr16019407
Lipina C, Kendall H, McPherron AC, Taylor PM, Hundal HS (2010) Mechanisms involved in the enhancement of mammalian target of rapamycin signalling and hypertrophy in skeletal muscle of myostatin-deficient mice. FEBS Lett 584:2403–2408
Ma K, Mallidis C, Artaza J, Taylor W, Gonzalez-Cadavid N, Bhasin S (2001) Characterization of 5′- regulatory region of human myostatin gene: regulation by dexamethasone in vitro. Am J Physiol 281:E1128-1136
Ma K, Mallidis C, Artaza J, Taylor W, Gonzalez-Cadavid N, Bhasin S (2001) Characterization of 5′- regulatory region of human myostatin gene: regulation by dexamethasone in vitro. Am J Physiol 281:E1128-1136
Ma K, Mallidis C, Bhasin S, Mahabadi V, Artaza J, Gonzalez-Cadavid N, Arias J, Salehian B (2003) Glucocorticoid-induced skeletal muscle atrophy is associated with upregulation of myostatin gene expression. Am J Physiol Endocrinol Metab 285(2):E363–E371. https://doi.org/10.1152/ajpendo.00487.2002
Maggio M, De Vita F, Lauretani F, Butto V, Bondi G, Cattabiani C, Nouvenne A, Meschi T, Dall’Aglio E, Ceda GP (2013) IGF-1, the cross road of the nutritional, inflammatory and hormonal pathways to frailty. Nutrients 5:4184–4205
Magnoni LJ, Roher N, Crespo D, Krasnov A, Planas JV (2015) In vivo molecular responses of fast and slow muscle fibers to lipopolysaccharide in a teleost fish, the rainbow trout (Oncorhynchus mykiss). Biology 4:67–87. https://doi.org/10.3390/biology4010067
Marino M, Scuderi F, Provenzano C, Bartoccioni E (2011) Skeletal muscle cells: from local inflammatory response to active immunity. Gene Ther 18:109–116
Martín AI, Priego T, Moreno-Ruperez Á, González-Hedström D, Granado M, López-Calderón A (2021) IGF-1 and IGFBP-3 in inflammatory cachexia. Int J Mol Sci 22:9469. https://doi.org/10.3390/ijms22179469
McFarlane C, Plummer E, Thomas M, Hennebry A, Ashby M, Ling N, Smith H, Sharma M, Kambadur R (2006) Myostatin induces cachexia by activating the ubiquitin proteolytic system through an NF-kappaB-independent, FoxO1-dependent mechanism. J Cell Physiol 209(2):501–514. https://doi.org/10.1002/jcp.20757
McPherron CA, Lawler MA, Lee SJ (1997) Regulation of skeletal muscle mass in mice by a new TGF-p superfamily member. Nature 387:83–90. https://doi.org/10.1038/387083a0
Morissette MR, Cook SA, Buranasombati C, Rosenberg MA, Rosenzweig A (2009) Myostatin inhibits IGF-I-induced myotube hypertrophy through Akt. Am J Physiol Cell Physiol 297:C1124–C1132
Moriyama S, Ayson GF, Kawauchi H (2000) Growth regulation by insulin-like growth factor-I in fish. Biosci Biotech Bioch 64:1553–1562. https://doi.org/10.1271/bbb.64.1553
Musaro A et al (2001) Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat Genet 27:195–200
Nebo C, Portella MC, Carani FR, de Almeida FLA, Padovani CR, Carvalho RF et al (2013) Short periods of fasting followed by refeeding change the expression of muscle growth-related genes in juvenile Nile tilapia (Oreochromis niloticus. Comp Biochem Physiol B Biochem Mol Biol 164:268–274. https://doi.org/10.1016/j.cbpb.2013.02.003
Norbeck LA, Kittilson JD, Sheridan MA (2007) Resolving the growth-promoting and metabolic effects of growth hormone: differential regulation of GH–IGF-I system components. Gen Comp Endocrinol 151(3):332–341. https://doi.org/10.1016/j.ygcen.2007.01.039
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29(9):45–45
Pfalzgraff T, Lund I, Skov PV (2021) Cortisol affects feed utilization, digestion and performance in juvenile rainbow trout (Oncorhynchus mykiss). Aquaculture 536:736472. https://doi.org/10.1016/j.aquaculture.2021.73
Pooley NJ, Tacchi L, Secombes CJ, Martin SA (2013) Inflammatory responses in primary muscle cell cultures in Atlantic salmon (Salmo salar). BMC Genom 14:747
Priego T, Granado M, Ibanez de Caceres I, Martin AI, Villanua MA, Lopez-Calderon A (2003) Endotoxin at low doses stimulates pituitary GH whereas it decreases IGF-I and IGF-binding protein-3 in rats. J Endocrinol 2003(179):107–117
Priego T, Granado M, Castillero E, Martin AI, Villanua MA, Lopez-Calderon A (2006) Nitric oxide production by hepatocytes contributes to the inhibitory effect of endotoxin on insulin-like growth factor I gene expression. J Endocrinol 190:847–856
Puche JE, Castilla-Cortazar I (2012) Human conditions of insulin-like growth factor-I (IGF-I) deficiency. J Transl Med 10:224
Pujante IM, Martos-Sitcha JA, Moyano FJ, Ruiz-Jarabo I, Martínez-Rodríguez G, Mancera JM (2015) Starving/re-feeding processes induce metabolic modifications in thick-lipped grey mullet (Chelon labrosus, Risso 1827). Comp Biochem Physiol Part B Biochem Mol Biol 180:57–67. https://doi.org/10.1016/j.cbpb.2014.10.005
Qiang J, He J, Yang H, Wang H, Kpundeh MD, Xu P, Zhu ZX (2014) Temperature modulates hepatic carbohydrate metabolic enzyme activity and gene expression in juvenile GIFT tilapia (Oreochromisniloticus) fed a carbohydrateenriched diet. J Therm Biol 40:25–31. https://doi.org/10.1016/j.jtherbio.2013.12.003
Reed LJ, Muench H (1938) A simple method of estimating ffty percent endpoint. Am J Epidemiol 27:493–497
Reindl KM, Sheridan MA (2012) Peripheral regulation of the growth hormone insulin-like growth factor system in fish and other vertebrates. Comp Biochem Physiol A Mol Integr Physiol 163:231–245
Rodgers BD, Garikipati DK (2008) Clinical, agricultural, and evolutionary biology of myostatin: a comparative review. Endocrine Revs 29:513–534
Rodriguez J, Vernus B, Chelh I, Cassar-Malek I, Gabillard JC, Hadj Sassi A et al (2014) Myostatin and the skeletal muscle atrophy and hypertrophy signaling pathways. Cell Mol Life Sci 71:4361–4371. https://doi.org/10.1007/s00018-014-1689-x
Rozas-Serri M, Pena A, Maldonado L (2018) Transcriptomic profiles of post-smolt Atlantic salmon challenged with Piscirickettsia salmonis reveal a strategy to evade the adaptive immune response and modify cell-autonomous immunity. Dev Comp Immunol 81:348–362
Sadoul B, Geffroy B (2019) Measuring cortisol, the major stress hormone in fishes. J Fish Biol 94:540–555
Sarkar MJA, Rashid MM (2012) Pathogenicity of the bacterial isolate Aeromonas hydrophila to catfishes, carps and perch. J Bangladesh Agric Univ 10:157–161
Sartori R, Romanello V, Sandri M (2021) Mechanisms of muscle atrophy and hypertrophy: implications in health and disease. Nature Communications | (2021) 12:330 | https://doi.org/10.1038/s41467-020-20123-1 |
Sawatari E, Seki R, Adachi T, Hashimoto H, Uji S, Wakamatsu Y, Nakata T, Kinoshita M (2010) Overexpression of the dominant-negative form of myostatin results in doubling of muscle-fiber number in transgenic medaka (Oryzias latipes). Comp Biochem Physiol A 155:183–189
Schakman O, Gilson H, Thissen JP (2008) Mechanisms of glucocorticoid-induced myopathy. J Endocrinol 197(1):1–10. https://doi.org/10.1677/JOE-07-0606
Segev-Hadar A, Alupo G, Tal K, Nitzan T, Biran J (2020) Identification and characterization of a non-muscular myostatin in the Nile tilapia. Front Endocrinol 11:94. https://doi.org/10.3389/fendo.2020.00094
Silva VV, Salomão RAS, Mareco ES, Pai MD, Santos VB (2021) Probiotic additive affects muscle growth of Nile tilapia (Oreochromis niloticus). Aquac Res 52:2061–2069
Soto L, Martin AI, Millan S, Vara E, Lopez-Calderon A (1998) Effects of endotoxin lipopolysaccharide administration on the somatotropic axis. J Endocrinol 159:239–246
Stana F, Vujovic M, Mayaki D, Leduc-Gaudet JP, Leblanc P, Huck L, Hussain SNA (2017) Differential regulation of the autophagy and proteasome pathways in skeletal muscles in sepsis. Crit Care Med 45:e971–e979
Stratev D, Stoev S, Vashin I, Daskalov H (2015) Some varieties of pathological changes in eximentalper infection of carps (Cyprinus carpio) with Aeromonas hydrophila. J Aquacult Eng Fish Res 1:191–202
Straub RH (2014) Interaction of the endocrine system with inflammation: a function of energy and volume regulation. Arthritis Res 16:203
Sun L, Trausch-Azar JS, Muglia LJ, Schwartz AL (2008) Glucocorticoids differentially regulate degradation of MyoD and Id1 by N-terminal ubiquitination to promote muscle protein catabolism. Proc Natl Acad Sci USA 105(9):3339–3344
Tacchi L, Bron JE, Taggart JB, Secombes CJ, Bickerdike R, Adler MA, Takle H, Martin SA (2011) Multiple tissue transcriptomic responses to Piscirickettsia salmonis in Atlantic salmon (Salmo salar). Physiol Genom 43:1241–1254
Thissen JP, Verniers J (1997) Inhibition by interleukin-1 beta and tumor necrosis factor-alpha of the insulin-like growth factor I messenger ribonucleic acid response to growth hormone in rat hepatocyte primary culture. Endocrinology 138:1078–1084
Torres-Velardea J, Llera-Herreraa R, García-Gascab T, García-Gascaa A (2018) Mechanisms of stress-related muscle atrophy in fish: an ex vivo approach mechanisms of development 154:162–169
Tort L (2011) Stress and immune modulation in fish. Dev Comp Immunol 35:1366–1375
Trendelenburg AU, Meyer A, Rohner D, Boyle J, Hatakeyama S, Glass DJ (2009) Myostatin reduces Akt/TORC1/p70S6K signaling, inhibiting myoblast differentiation and myotube size. American J Cell Physiol 296(6):C1258–C1270
Uren Webster TM, Rodriguez-Barreto D, Consuegra S, de Leaniz CG (2020) Cortisol-related signatures of stress in the fish microbiome. Front Microbiol 11:1621. https://doi.org/10.3389/fmicb.2020.01621
Valenzuela CA, Zuloaga R, Poblete-Morales M, Vera-Tobar T, Mercado L, Avendaño-Herrera R, Valdés JA, Molina A (2017) Fish skeletal muscle tissue is an important focus of immune reactions during pathogen infection. Dev Comp Immunol 73:1–9
Valenzuela CA, Ponce C, Zuloaga R, González P, Avendaño-Herrera R, Valdés JA, Molina A (2020) Effects of crowding on the three main proteolytic mechanism of skeletal muscle in rainbow trout (Oncorhynchus mykiss. BMC Vet Res 16:294
Verburg-Van Kemenade BML, Ribeiro CMS, Chadzinska M (2011) Neuroendocrine-immune interaction in fish: differential regulation of phagocyte activity by neuroendocrine factors. Gen Comp Endocrinol 172(1):31–38. https://doi.org/10.1016/j.ygcen.2011.01.004
Vianello S, Brazzoduro L, Dalla Valle L, Belvedere P, Colombo L (2003) Myostatin expression during development and chronic stress in zebrafish (Danio rerio). J Endocrinol 176:47–59
Wang M, Lu M (2016) Tilapia polyculture: a global review. Aquac Res 47(8):2363–2374
Wang C, Chen Y-L, Bian W-P, Xie S-L, Qi G-L, Liu L et al (2018) Deletion of mstna and mstnb impairs the immune system and affects growth performance in zebrafish. Fish Shellfish Immunol 72:572–580. https://doi.org/10.1016/j.fsi.2017.11.040
Weber TE, Bosworth BG (2005) Effects of 28 day exposure to cold temperature or feed restriction on growth, body composition, and expression of genes related to muscle growth and metabolism in channel catfish. Aquaculture 246:483–492. https://doi.org/10.1016/j.aquaculture.2005.02.032
Wiendl H, Hohlfeld R, Kieseier BC (2005) Immunobiology of muscle: advances in understanding an immunological microenvironment. Trends Immunol 26:373–380
Wood AW, Duan C, Bern HA (2005) Insulin-like growth factor signaling in fish. Int Rev Cytol 243:215–285
Xu C, Wu G, Zohar Y, Du SJ (2003) Analysis of myostatin gene structure, expression and function in zebrafish. J Exp Biol 206:4067–4079
Xu L, Zhang W, Sun R, Liu J, Hong J, Li Q, Hu B, Gong F (2017) IGF-1 may predict the severity and outcome of patients with sepsis and be associated with microRNA-1 level changes. Exp Ther Med 14:797–804
Zhang DL, Guan RZ, Huang WS, Xiong J (2013) Isolation and characterization of a novel antibacterial peptide derived from hemoglobin alpha in the liver of Japanese eel, Anguilla japonica. Fish Shellfish Immunol 35:625–631. https://doi.org/10.1016/j.fsi.2012.08.022
Zhong Z, Niu P, Wang M, Huang G, Xu S, Sun Y et al (2016) Targeted disruption of sp7 and myostatin with CRISPR-Cas9 results in severe bone defects and more muscular cells in common carp. Sci Rep 6:22953. https://doi.org/10.1038/srep22953
Zuloaga R, Dettleff P, Bastias-Molina M, Meneses C, Altamirano C, Valdés JA, Molina A (2021) RNA-seq-based analysis of cortisol-induced differential gene expression associated with Piscirickettsia salmonis infection in rainbow trout (Oncorhynchus mykiss) myotubes. Animals 11:2399. https://doi.org/10.3390/ani11082399
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The authors would like to acknowledge the Biotechnology Lab., Faculty of Aquatic and Fisheries Sciences, Kafrelsheikh University, where the molecular analysis was performed.
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Z.I.E. is responsible for conceptualization, molecular analysis, reviewing and editing the final version, and publishing the paper. E.A. performed the experiment, sampling, and laboratory investigation. I.I.A. supervision and validation of the study. A.S.S. is responsible for data curation, statistical analysis, and software analysis of data. A.A.A. studies visualization and supervision. M.A.A. reviewed and edited the final version. D.H.A. methodology, including pathological examination and validation of the study, was a significant contributor to writing the manuscript. All authors read and approved the final manuscript.
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The current study’s methods and experimental protocols adhered to the relevant guidelines and regulations of Kafrelsheikh University’s ethical approval committee no. IAACUC-KSU-2020–21.
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ELbialy, Z.I., Atef, E., Al-Hawary, I.I. et al. Myostatin-mediated regulation of skeletal muscle damage post-acute Aeromonas hydrophila infection in Nile tilapia (Oreochromis niloticus L.). Fish Physiol Biochem 49, 1–17 (2023). https://doi.org/10.1007/s10695-022-01165-2
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DOI: https://doi.org/10.1007/s10695-022-01165-2