Abstract
Antioxidant system is crucial for protecting against environmental oxidative stress in fish life cycle. Although the effects of starvation on the antioxidant defenses in several adult fish have been defined, no relevant researches have been reported in the larval stage, particularly during the transition from endogenous to exogenous feeding. To clarify the molecular response of antioxidant system that occurs during the mouth-opening stage under starvation stress and explore its association with energy metabolism, we employed RNA-seq to analyze the gene expression profiles in zebrafish larvae that received a delayed first feeding for 3 days. Our data showed that delayed feeding resulted in downregulation of 7078 genes and upregulation of 497 genes. These differentially expressed genes are mainly involved in growth regulation (i.e., DNA replication and cell cycle), energy metabolism (i.e., glycolysis/gluconeogenesis and fatty acid metabolism), and antioxidant defenses. We demonstrated that the starved larvae are in an extremely malnourished state in the absence of exogenous nutrition, and the consequence is that numerous antioxidant genes are downregulated. Meanwhile, the antioxidant defenses also respond negatively to oxidative stress. After nutritional supply, the expression of these inhibited antioxidant genes was restored. These results suggest that the establishment of antioxidant defenses during the mouth-opening stage depends highly on exogenous nutrition. Our findings would contribute to comprehending the nutritional stress and metabolic switches during the mouth-opening stage and are essential for reducing high mortality in commercial fish farming.
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The data and materials that support the findings of this study are available from the corresponding author upon reasonable request.
References
Antonopoulou E, Kentepozidou E, Feidantsis K, Roufidou C, Despoti S, Chatzifotis S (2013) Starvation and re-feeding affect Hsp expression, MAPK activation and antioxidant enzymes activity of European sea bass (Dicentrarchus labrax). Comp Biochem Physiol A Mol Integr Physiol 165:79–88. https://doi.org/10.1016/j.cbpa.2013.02.019
Bayir A, Sirkecioglu AN, Bayir M, Haliloglu HI, Kocaman EM, Aras NM (2011) Metabolic responses to prolonged starvation, food restriction, and refeeding in the brown trout, Salmo trutta: oxidative stress and antioxidant defenses. Comp Biochem Physiol B Biochem Mol Biol 159:191–196. https://doi.org/10.1016/j.cbpb.2011.04.008
Berggren MI, Husbeck B, Samulitis B, Baker AF, Gallegos A, Powis G (2001) Thioredoxin peroxidase-1 (peroxiredoxin-1) is increased in thioredoxin-1 transfected cells and results in enhanced protection against apoptosis caused by hydrogen peroxide but not by other agents including dexamethasone, etoposide, and doxorubicin. Arch Biochem Biophys 392:103–109. https://doi.org/10.1006/abbi.2001.2435
Bhutta ZA, Berkley JA, Bandsma RHJ, Kerac M, Trehan I, Briend A (2017) Severe childhood malnutrition. Nat Rev Dis Primers 3:17067. https://doi.org/10.1038/nrdp.2017.67
China V, Holzman R (2014) Hydrodynamic starvation in first-feeding larval fishes. Proc Natl Acad Sci U S A 111:8083–8088. https://doi.org/10.1073/pnas.1323205111
Clarkston WK, Pantano MM, Morley JE, Horowitz M, Littlefield JM, Burton FR (1997) Evidence for the anorexia of aging: gastrointestinal transit and hunger in healthy elderly vs. young adults. Am J Physiol 272:R243–R248. https://doi.org/10.1152/ajpregu.1997.272.1.R243
De Caprio C, Alfano A, Senatore I, Zarrella L, Pasanisi F, Contaldo F (2006) Severe acute liver damage in anorexia nervosa: two case reports. Nutrition 22:572–575. https://doi.org/10.1016/j.nut.2006.01.003
Fernandes MN, Perna-Martins SA (2001) Epithelial gill cells in the armored catfish, Hypostomus cf. plecostomus (Loricariidae). Braz J Biol 61:69–78. https://doi.org/10.1590/s0034-71082001000100010
FurnÉ M, GarcÍA-Gallego M, Hidalgo MC, Morales AE, Domezain A, Domezain J, Sanz A (2009) Oxidative stress parameters during starvation and refeeding periods in Adriatic sturgeon (Acipenser naccarii) and rainbow trout (Oncorhynchus mykiss). Aquac Nutr 15:587–595. https://doi.org/10.1111/j.1365-2095.2008.00626.x
Gaál T, Mézes M, Miskucza O, Ribiczey-szabó P (1993) Effect of fasting on blood lipid peroxidation parameters of sheep. Res Vet Sci 55:104–107. https://doi.org/10.1016/0034-5288(93)90042-e
Gobi N, Vaseeharan B, Rekha R, Vijayakumar S, Faggio C (2018) Bioaccumulation, cytotoxicity and oxidative stress of the acute exposure selenium in Oreochromis mossambicus. Ecotoxicol Environ Saf 162:147–159. https://doi.org/10.1016/j.ecoenv.2018.06.070
Hidalgo MC, Morales AE, Arizcun M, Abellan E, Cardenete G (2017) Regional asymmetry of metabolic and antioxidant profile in the sciaenid fish shi drum (Umbrina cirrosa) white muscle. Response to starvation and refeeding. Redox Biol 11:682–687. https://doi.org/10.1016/j.redox.2017.01.022
Huang W, Cao L, Ye Z, Yin X, Dou S (2010) Antioxidative responses and bioaccumulation in Japanese flounder larvae and juveniles under chronic mercury exposure. Comp Biochem Physiol C Toxicol Pharmacol 152:99–106. https://doi.org/10.1016/j.cbpc.2010.03.005
Joyner-Matos J, Abele D, Medina JPV, Zenteno-Savin T (2016) Oxidative stress in aquatic ecosystems: selected papers from the Second International Conference. Comp Biochem Physiol A Mol Integr Physiol 200:1–2. https://doi.org/10.1016/j.cbpa.2016.06.010
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36. https://doi.org/10.1186/gb-2013-14-4-r36
Kim DH, Jung IH, Kim DH, Park SW (2019) Knockout of longevity gene Sirt1 in zebrafish leads to oxidative injury, chronic inflammation, and reduced life span. PLoS ONE 14:e0220581. https://doi.org/10.1371/journal.pone.0220581
Kobayashi M, Itoh K, Suzuki T, Osanai H, Nishikawa K, Katoh Y, Takagi Y, Yamamoto M (2002) Identification of the interactive interface and phylogenic conservation of the Nrf2-Keap1 system. Genes Cells 7:807–820. https://doi.org/10.1046/j.1365-2443.2002.00561.x
Lisse TS, King BL, Rieger S (2016) Comparative transcriptomic profiling of hydrogen peroxide signaling networks in zebrafish and human keratinocytes: implications toward conservation, migration and wound healing. Sci Rep 6:20328. https://doi.org/10.1038/srep20328
Ma J, Li M, Kalavagunta PK, Li J, He Q, Zhang Y, Ahmad O, Yin H, Wang T, Shang J (2018) Protective effects of cichoric acid on H2O2-induced oxidative injury in hepatocytes and larval zebrafish models. Biomed Pharmacother 104:679–685. https://doi.org/10.1016/j.biopha.2018.05.081
Madeira D, Narciso L, Cabral HN, Vinagre C, Diniz MS (2013) Influence of temperature in thermal and oxidative stress responses in estuarine fish. Comp Biochem Physiol A Mol Integr Physiol 166:237–243. https://doi.org/10.1016/j.cbpa.2013.06.008
Martínez-Álvarez RM, Morales AE, Sanz A (2005) Antioxidant defenses in fish: biotic and abiotic factors. Rev Fish Biol Fish 15:75–88. https://doi.org/10.1007/s11160-005-7846-4
Maures TJ (2002) Structure, developmental expression, and physiological regulation of zebrafish IGF binding protein-1. Endocrinology 143:2722–2731. https://doi.org/10.1210/endo.143.7.8905
Mazurais D, Darias M, Zambonino-Infante JL, Cahu CL (2011) Transcriptomics for understanding marine fish larval development. Can J Zool 89:599–611. https://doi.org/10.1139/z11-036
Mennigen JA, Skiba-Cassy S, Panserat S (2013) Ontogenetic expression of metabolic genes and microRNAs in rainbow trout alevins during the transition from the endogenous to the exogenous feeding period. J Exp Biol 216:1597–1608. https://doi.org/10.1242/jeb.082248
Morales AE, Perez-Jimenez A, Hidalgo MC, Abellan E, Cardenete G (2004) Oxidative stress and antioxidant defenses after prolonged starvation in Dentex dentex liver. Comp Biochem Phys C 139:153–161. https://doi.org/10.1016/j.cca.2004.10.008
Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185. https://doi.org/10.1093/nar/gkm321
Mukaigasa K, Nguyen LT, Li L, Nakajima H, Yamamoto M, Kobayashi M (2012) Genetic evidence of an evolutionarily conserved role for Nrf2 in the protection against oxidative stress. Mol Cell Biol 32:4455–4461. https://doi.org/10.1128/MCB.00481-12
Mustafa SA, Al-Subiai SN, Davies SJ, Jha AN (2011) Hypoxia-induced oxidative DNA damage links with higher level biological effects including specific growth rate in common carp, Cyprinus carpio L. Ecotoxicology 20:1455–1466. https://doi.org/10.1007/s10646-011-0702-5
Nakajima H, Nakajima-Takagi Y, Tsujita T, Akiyama S, Wakasa T, Mukaigasa K, Kaneko H, Tamaru Y, Yamamoto M, Kobayashi M (2011) Tissue-restricted expression of Nrf2 and its target genes in zebrafish with gene-specific variations in the induction profiles. PLoS ONE 6:e26884. https://doi.org/10.1371/journal.pone.0026884
Neumann CA, Krause DS, Carman CV, Das S, Dubey DP, Abraham JL, Bronson RT, Fujiwara Y, Orkin SH, Van Etten RA (2003) Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature 424:561–565. https://doi.org/10.1038/nature01819
Nurdiani R, Zeng C (2007) Effects of temperature and salinity on the survival and development of mud crab, Scylla serrata (Forsskål), larvae. Aquac Res 38:1529–1538. https://doi.org/10.1111/j.1365-2109.2007.01810.x
Oliver PL, Finelli MJ, Edwards B, Bitoun E, Butts DL, Becker EB, Cheeseman MT, Davies B, Davies KE (2011) Oxr1 is essential for protection against oxidative stress-induced neurodegeneration. PLoS Genet 7:e1002338. https://doi.org/10.1371/journal.pgen.1002338
Pascual P, Pedrajas JR, Toribio F, López-Barea J, Peinado J (2003) Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata). Chem Biol Interact 145:191–199. https://doi.org/10.1016/s0009-2797(03)00002-4
Pérez-Jiménez A, Guedes MJ, Morales AE, Oliva-Teles A (2007) Metabolic responses to short starvation and refeeding in Dicentrarchus labrax Effect of dietary composition. Aquaculture 265:325–335. https://doi.org/10.1016/j.aquaculture.2007.01.021
Robinson MK, Rustum RR, Chambers EA, Rounds JD, Wilmore DW, Jacobs DO (1997) Starvation enhances hepatic free radical release following endotoxemia. J Surg Res 69:325–330. https://doi.org/10.1006/jsre.1997.5062
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. https://doi.org/10.1093/bioinformatics/btp616
Rousseau ME, Sant KE, Borden LR, Franks DG, Hahn ME, Timme-Laragy AR (2015) Regulation of Ahr signaling by Nrf2 during development: effects of Nrf2a deficiency on PCB126 embryotoxicity in zebrafish (Danio rerio). Aquat Toxicol 167:157–171. https://doi.org/10.1016/j.aquatox.2015.08.002
Rudneva II (1997) Blood antioxidant system of Black Sea elasmobranch and teleosts. Comp Biochem Phys C 118:255–260. https://doi.org/10.1016/s0742-8413(97)00111-4
Santos MA, Pacheco M, Ahmad I (2004) Anguilla anguilla L. antioxidants responses to in situ bleached kraft pulp mill effluent outlet exposure. Environ Int 30:301–308. https://doi.org/10.1016/s0160-4120(03)00178-8
Scott RC, Schuldiner O, Neufeld TP (2004) Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev Cell 7:167–178. https://doi.org/10.1016/j.devcel.2004.07.009
Shan X, Quan H, Dou S (2008) Effects of delayed first feeding on growth and survival of rock bream Oplegnathus fasciatus larvae. Aquaculture 277:14–23. https://doi.org/10.1016/j.aquaculture.2008.01.044
Suzuki T, Takagi Y, Osanai H, Li L, Takeuchi M, Katoh Y, Kobayashi M, Yamamoto M (2005) Pi class glutathione S-transferase genes are regulated by Nrf 2 through an evolutionarily conserved regulatory element in zebrafish. Biochem J 388:65–73. https://doi.org/10.1042/BJ20041860
Takagi Y, Kobayashi M, Li L, Suzuki T, Nishikawa K, Yamamoto M (2004) MafT, a new member of the small Maf protein family in zebrafish. Biochem Biophys Res Commun 320:62–69. https://doi.org/10.1016/j.bbrc.2004.05.131
Taylor JJ, Wilson SM, Sopinka NM, Hinch SG, Patterson DA, Cooke SJ, Willmore WG (2015) Are there intergenerational and population-specific effects of oxidative stress in sockeye salmon (Oncorhynchus nerka)? Comp Biochem Physiol A Mol Integr Physiol 184:97–104. https://doi.org/10.1016/j.cbpa.2015.01.022
Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578. https://doi.org/10.1038/nprot.2012.016
Wang Z, Fang B, Chen J, Zhang X, Luo Z, Huang L, Chen X, Li Y (2010) De novo assembly and characterization of root transcriptome using Illumina paired-end sequencing and development of cSSR markers in sweet potato (Ipomoea batatas). BMC Genomics 11:726. https://doi.org/10.1186/1471-2164-11-726
Xu H, Liu EX, Li Y, Li XJ, Ding CY (2017) Transcriptome analysis reveals increases in visceral lipogenesis and storage and activation of the antigen processing and presentation pathway during the mouth-opening stage in zebrafish larvae. Int J Mol Sci 18:1634. https://doi.org/10.3390/ijms18081634
Xu H, Jiang Y, Li S, Xie L, Tao YX, Li Y (2020) Zebrafish oxr1a knockout reveals its role in regulating antioxidant defenses and aging. Genes 11:1118. https://doi.org/10.3390/genes11101118
Yandi I, Altinok I (2018) Irreversible starvation using RNA/DNA on lab-grown larval anchovy, Engraulis encrasicolus, and evaluating starvation in the field-caught larval cohort. Fish Res 201:32–37. https://doi.org/10.1016/j.fishres.2018.01.005
Yang M, Lin X, Rowe A, Rognes T, Eide L, Bjoras M (2015) Transcriptome analysis of human OXR1 depleted cells reveals its role in regulating the p53 signaling pathway. Sci Rep 5:17409. https://doi.org/10.1038/srep17409
Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297. https://doi.org/10.1093/nar/gkl031
Funding
The research was supported by the Chongqing Natural Science Foundation (Postdoctoral Fund) (No. cstc2020jcyj-bsh0053) and the Ecological Fishery Technological System of Chongqing Municipal Agricultural and Rural Committee under Grant No. 40810017.
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Conceptualization, H.X. and Y.L.; methodology, H.X. and S.-Q.F.; software, H.X., G.W., and X.-M.M.; validation, H.X. and X.-M.M.; formal analysis, H.X., S.-Q.F., and X.-M.M.; investigation, H.X., X.-M.M., S.-Q.F., and G.W.; resources, Y.L.; data curation, H.X., S.-Q.F., and X.-M.M.; writing—original draft preparation, H.X.; writing—review & editing, H.X. and Y.L.; visualization, H.X.; supervision, Y.L.; project administration, H.X.; funding acquisition, Y.L. All authors have read and agreed to the published version of the manuscript.
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All animal experiments were performed in accordance with the Guiding Principles for the Care and Use of Laboratory Animals and were approved by the Committee for Laboratory Animal Experimentation at Southwest University, China (Approval ID: 2,018,092,308).
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Xu, H., Fan, SQ., Wang, G. et al. Transcriptome analysis reveals the importance of exogenous nutrition in regulating antioxidant defenses during the mouth-opening stage in oviparous fish. Fish Physiol Biochem 47, 1087–1103 (2021). https://doi.org/10.1007/s10695-021-00954-5
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DOI: https://doi.org/10.1007/s10695-021-00954-5