Cite this paper:
Yu ZHANG, Weiliang SHEN, Juan LI, Baoxiao ZHENG, Zhengjia LOU, Mohammad Aslam HOSAIN, Baoying QIAN, Liangyi XUE. Effect of fasting on protein metabolism in muscle tissue of Larimichthys crocea revealed by transcriptome and proteome[J]. Journal of Oceanology and Limnology, 2021, 39(5): 1972-1984

Effect of fasting on protein metabolism in muscle tissue of Larimichthys crocea revealed by transcriptome and proteome

Yu ZHANG1, Weiliang SHEN1,2, Juan LI1, Baoxiao ZHENG1, Zhengjia LOU1, Mohammad Aslam HOSAIN1, Baoying QIAN1,3, Liangyi XUE1
1 College of Marine Sciences, Ningbo University, Ningbo 315832, China;
2 Ningbo Institute of Marine and Fisheries, Ningbo 315103, China;
3 School of Life Science, Taizhou University, Taizhou 318000, China
Abstract:
The large yellow croaker (Larimichthys crocea) is an important mariculture fish in China. Farmed large yellow croaker undergo periods of fasting to adapt to the environment or to improve meat quality. To better understand the physiological responses of their muscle tissues to fasting stresses, we analyzed the transcriptomes and proteomes of both normally-fed and fasting fish groups and identified 7 578 differentially expressed genes (DEGs) and 297 differentially expressed proteins (DEPs) among them. Gene ontology and KEGG analysis showed that the enriched biological pathways were mainly involved in various synthetic and catabolic pathways, especially the protein metabolism. Based on the omics data, nine DEGs related to muscle composition (CAN3, MYL3, and TNNC2), growth (MSTN and MYF5), autophagy (TSC2 and ULK1), and the ubiquitin proteasome pathway (PRS6B and UCHL3) were examined using qPCR. In response to fasting stress, MYL3 and TNNC2 were significantly downregulated, while genes associated with autophagy and the ubiquitin proteasome pathway were significantly upregulated. In response to fasting stress, MYL3, TNNC2, and MYF5 positively correlated with muscle growth were significantly downregulated, while inhibiting growth MSTN and genes associated with autophagy and the ubiquitin proteasome pathways were significantly upregulated. These results clarify the effects of fasting on metabolic changes in their muscle components and growth at the molecular level.
Key words:    Larimichthys crocea|fasting|transcriptome|proteome|muscle   
Received: 2020-07-23   Revised: 2020-09-28
Tools
PDF (2048 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by Yu ZHANG
Articles by Weiliang SHEN
Articles by Juan LI
Articles by Baoxiao ZHENG
Articles by Zhengjia LOU
Articles by Mohammad Aslam HOSAIN
Articles by Baoying QIAN
Articles by Liangyi XUE
References:
Aranda A, Sánchez-Vázquez F J, Madrid J A. 2001. Effect of short-term fasting on macronutrient self-selection in sea bass. Physiology & Behavior, 73(1-2):105-109, https://doi.org/10.1016/S0031-9384(01)00464-4.
Bach M, Larance M, James D E, Ramm G. 2011. The serine/threonine kinase ULK1 is a target of multiple phosphorylation events. Biochemical Journal, 440(2):283-291, https://doi.org/10.1042/BJ20101894.
Black D, Love R M. 1986. The sequential mobilisation and restoration of energy reserves in tissues of Atlantic cod during starvation and refeeding. Journal of Comparative Physiology B, 156(4):469-479, https://doi.org/10.1007/BF00691032.
Cassidy A A, Saulnier R J, Lamarre S G. 2016. Adjustments of protein metabolism in fasting Arctic charr, Salvelinus alpinus. PLoS One, 11(4):e0153364, https://doi.org/10.1371/journal.pone.0153364.
Ciechanover A, Finley D, Varshavsky A. 1984. The ubiquitinmediated proteolytic pathway and mechanisms of energydependent intracellular protein degradation. Journal of Cellular Biochemistry, 24(1):27-53, https://doi.org/10.1002/jcb.240240104.
Codina M, Bian Y H, Gutiérrez J, Du S J. 2008. Cloning and characterization of myogenin from seabream (Sparus aurata) and analysis of promoter muscle specificity. Comparative Biochemistry and Physiology Part D:Genomics and Proteomics, 3(1):128-139, https://doi.org/10.1016/j.cbd.2007.12.001.
Cukras A R, Southworth D R, Brunelle J L, Culver G M, Green R. 2003. Ribosomal proteins S12 and S13 function as control elements for translocation of the mRNA:tRNA complex. Molecular Cell, 12(2):321-328, https://doi.org/10.1016/S1097-2765(03)00275-2.
da Silva-Gomes R N, Kuniyoshi M L G, da Silva Duran B O, Zanella B T T, Freire P P, de Paula T G, de Almeida Fantinatt B E, Salomão R A S, Carvalho R F, Santos L D, Dal-Pai-Silva M. 2019. Prolonged fasting followed by refeeding modifies proteome profile and parvalbumin expression in the fast-twitch muscle of pacu (Piaractus mesopotamicus). PLoS One, 14(12):e0225864, https://doi.org/10.1371/journal.pone.0225864.
Finn P F, Dice J F. 2006. Proteolytic and lipolytic responses to starvation. Nutrition, 22(7-8):830-844, https://doi.org/10.1016/j.nut.2006.04.008.
Fraser K P P, Rogers A D. 2007. Protein metabolism in marine animals:the underlying mechanism of growth. Advances in Marine Biology, 52:267-362, https://doi.org/10.1016/S0065-2881(06)52003-6.
Ganley I G, Lam D H, Wang J R, Ding X J, Chen S, Jiang X J. 2009. ULK1·ATG13·FIP200 complex mediates mTOR signaling and is essential for autophagy. The Journal of Biological Chemistry, 284(18):12 297-12 305, https://doi.org/10.1074/jbc.M900573200.
Gelfi C, Viganò A, Ripamonti M, Pontoglio A, Begum S, Pellegrino M A, Grassi B, Bottinelli R, Wait R, Cerretelli P. 2006. The human muscle proteome in aging. Journal of Proteome Research, 5(6):1 344-1 353, https://doi.org/10.1021/pr050414x.
Goll D E, Thompson V F, Li H Q, Wei W, Cong J Y. 2003. The calpain system. Physiological Reviews, 83(3):731-801, https://doi.org/10.1152/physrev.00029.2002.
Goll D E, Thompson V F, Taylor R G, Christiansen J A. 1992. Role of the calpain system in muscle growth. Biochimie, 74(3):225-237, https://doi.org/10.1016/0300-9084(92)90121-T.
Guo Y H, Bai J J, Chang O Q, Lao H H, Ye X, Luo J R. 2009. Molecular structure of the largemouth bass (Micropterus salmoides) Myf5 gene and its effect on skeletal muscle growth. Molecular Biology Reports, 36(6):1 497-1 504, https://doi.org/10.1007/s11033-008-9341-1.
Harvald E B, Sprenger R R, Dall K B, Ejsing C S, Nielsen R, Mandrup S, Murillo A B, Larance M, Gartner A, Lamond A I, Færgeman N J. 2017. Multi-omics analyses of starvation responses reveal a central role for lipoprotein metabolism in acute starvation survival in C. elegans. Cell Systems, 5(1):38-52.e34, https://doi.org/10.1016/j.cels.2017.06.004.
Hershko A, Ciechanover A. 1982. Mechanisms of intracellular protein breakdown. Annual Review of Biochemistry, 51:335-364, https://doi.org/10.1146/annurev.bi.51.070182. 002003.
Hershko A, Heller H. 1985. Occurrence of a polyubiquitin structure in ubiquitin-protein conjugates. Biochemical and Biophysical Research Communications, 128(3):1 079-1 086, https://doi.org/10.1016/0006-291X(85)91050-2.
Hu L L, Ren S J, Shen Q, Chen J C, Ye X Q, Ling J G. 2017. Proteomic study of the effect of different cooking methods on protein oxidation in fish fillets. RSC Advances, 7(44):27 496-27 505, https://doi.org/10.1039/C7RA03408C.
Huang D W, Sherman B T, Lempicki R A. 2008. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols, 4(1):44-57, https://doi.org/10.1038/nprot.2008.211.
Huang D W, Sherman B T, Lempicki R A. 2009. Bioinformatics enrichment tools:paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research, 37(1):1-13, https://doi.org/10.1093/nar/gkn923.
Ilian M A, Forsberg N E. 1992. Gene expression of calpains and their specific endogenous inhibitor, calpastatin, in skeletal muscle of fed and fasted rabbits. Biochemical Journal, 287(Pt 1):163-171, https://doi.org/10.1042/bj2870163.
Johnston I A, Bower N I, Macqueen D J. 2011. Growth and the regulation of myotomal muscle mass in teleost fish. Journal of Experimental Biology, 214(Pt 10):1 617-1 628, https://doi.org/10.1242/jeb.038620.
Kuniyoshi M L G, Da Silva-Gomes R N, Vieira J C S, Hessel M C, Mareco E A, Santos V B D, Carvalho R F, De Magalhães Padilha P, Dal-Pai-Silva M. 2019. Proteomic analysis of the fast-twitch muscle of pacu (Piaractus mesopotamicus) after prolonged fasting and compensatory growth. Comparative Biochemistry and Physiology Part D:Genomics and Proteomics, 30:321-332, https://doi.org/10.1016/j.cbd.2019.04.005.
Langmead B, Trapnell C, Pop M, Salzberg S L. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 10(3):R25, https://doi.org/10.1186/gb-2009-10-3-r25.
Lavajoo F, Perelló-Amorós M, Vélez E J, Sánchez-Moya A, Balbuena-Pecino S, Riera-Heredia N, Fernández-Borràs J, Blasco J, Navarro I, Capilla E, Gutiérrez J. 2020. Regulatory mechanisms involved in muscle and bone remodeling during refeeding in gilthead sea bream. Scientific Reports, 10(1):184-184, https://doi.org/10.1038/s41598-019-57013-6.
Lecker S H, Goldberg A L, Mitch W E. 2006. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. Journal of the American Society of Nephrology, 17(7):1 807-1 819, https://doi.org/10.1681/ASN.2006010083.
Long M, Zhao J, Li T T, Tafalla C, Zhang Q Q, Wang X H, Gong X N, Shen Z X, Li A H. 2015. Transcriptomic and proteomic analyses of splenic immune mechanisms of rainbow trout (Oncorhynchus mykiss) infected by Aeromonas salmonicida subsp. salmonicida. Journal of Proteomics, 122:41-54, https://doi.org/10.1016/j.jprot.2015.03.031.
Ma Q, Liu X F, Feng W R, Liu S F, Zhuang Z M. 2018. Analyses of the molecular mechanisms associated with salinity adaption of Trachidermus fasciatus through combined iTRAQ-based proteomics and RNA sequencing-based transcriptomics. Progress in Biophysics and Molecular Biology, 136:40-53, https://doi.org/10.1016/j.pbiomolbio.2018.02.003.
Maddock D M, Burton M P M. 1994. Some effects of starvation on the lipid and skeletal muscle layers of the winter flounder, Pleuronectes americanus. Canadian Journal of Zoology, 72(9):1 672-1 679, https://doi.org/10.1139/z94-223.
Martin S, Blaney S, Bowman A, Houlihan D. 2002. Ubiquitinproteasome-dependent proteolysis in rainbow trout(Oncorhynchus mykiss):effect of food deprivation. Pflügers Archiv, 445(2):257-266, https://doi.org/10.1007/s00424-002-0916-8.
Mélèse T, Xue Z X. 1995. The nucleolus:an organelle formed by the act of building a ribosome. Current Opinion in Cell Biology, 7(3):319-324, https://doi.org/10.1016/0955-0674(95)80085-9.
Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. 2004. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Molecular Biology of the Cell, 15(3):1 101-1 111, https://doi.org/10.1091/mbc.e03-09-0704.
Mommsen T P. 2004. Salmon spawning migration and muscle protein metabolism:the August Krogh principle at work. Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 139(3):383-400, https://doi.org/10.1016/j.cbpc.2004.09.018.
Moses M A, Wiederschain D, Wu I, Fernandez C A, Ghazizadeh V, Lane W S, Flynn E, Sytkowski A, Tao T, Langer R. 1999. Troponin I is present in human cartilage and inhibits angiogenesis. Proceedings of the National Academy of Sciences of the United States of America, 96(6):2 645-2 650, https://doi.org/10.1073/pnas.96.6.2645.
Neave M J, Streten-Joyce C, Nouwens A S, Glasby C J, McGuinness K A, Parry D L, Gibb K S. 2012. The transcriptome and proteome are altered in marine polychaetes (Annelida) exposed to elevated metal levels. Journal of Proteomics, 75(9):2 721-2 735, https://doi.org/10.1016/j.jprot.2012.03.031.
Piec I, Listrat A, Alliot J, Chambon C, Taylor R G, Bechet D. 2005. Differential proteome analysis of aging in rat skeletal muscle. FASEB Journal Official Publication of the Federation of American Societies for Experimental Biology, 19(9):1 143-1 145, https://doi.org/10.1096/fj.04-3084fje.
Purintrapiban J, Wang M C, Forsberg N E. 2003. Degradation of sarcomeric and cytoskeletal proteins in cultured skeletal muscle cells. Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 136(3):393-401, https://doi.org/10.1016/S1096-4959(03)00201-X.
Qian B Y, Xue L Y, Huang H L. 2016. Liver transcriptome analysis of the large yellow croaker (Larimichthys crocea) during fasting by using RNA-Seq. PLoS One, 11(3):e0150240, https://doi.org/10.1371/journal.pone.0150240.
Radhi O A, Davidson S, Scott F, Zeng R X, Jones D H, Tomkinson N C O, Yu J, Chan E Y W. 2019. Inhibition of the ULK1 protein complex suppresses Staphylococcusinduced autophagy and cell death. Journal of Biological Chemistry, 294(39):14 289-14 307, https://doi.org/10.1074/jbc.RA119.008923.
Rescan P Y, Montfort J, Rallière C, Cam A L, Esquerré D, Hugot K. 2007. Dynamic gene expression in fish muscle during recovery growth induced by a fasting-refeeding schedule. BMC Genomics, 8:438, https://doi.org/10.1186/1471-2164-8-438.
Salem M, Silverstein J, Rexroad III C E, Yao J B. 2007. Effect of starvation on global gene expression and proteolysis in rainbow trout (Oncorhynchus mykiss). BMC Genomics, 8:328, https://doi.org/10.1186/1471-2164-8-328.
Salmerón C, de la Serrana D G, Jiménez-Amilburu V, Fontanillas R, Navarro I, Johnston I A, Gutiérrez J, Capilla E. 2013. Characterisation and expression of calpain family members in relation to nutritional status, diet composition and flesh texture in gilthead sea bream(Sparus aurata). PLoS One, 8(9):e75349, https://doi.org/10.1371/journal.pone.0075349.
Seiliez I, Médale F, Aguirre P, Larquier M, Lanneretonne L, Alami-Durante H, Panserat S, Skiba-Cassy S. 2013. Postprandial regulation of growth-and metabolism-related factors in zebrafish. Zebrafish, 10(2):237-248, https://doi.org/10.1089/zeb.2012.0835.
Seiliez I, Panserat S, Skiba-Cassy S, Fricot A, Vachot C, Kaushik S, Tesseraud S. 2008. Feeding status regulates the polyubiquitination step of the ubiquitin-proteasomedependent proteolysis in rainbow trout (Oncorhynchus mykiss) muscle. Journal of Nutrition, 138(3):487-491, https://doi.org/10.1093/jn/138.3.487.
Solomon V, Goldberg A L. 1996. Importance of the ATPubiquitin-proteasome pathway in the degradation of soluble and myofibrillar proteins in rabbit muscle extracts. Journal of Biological Chemistry, 271(43):26 690-26 697, https://doi.org/10.1074/jbc.271.43.26690.
Sun P, Bao P B, Tang B J. 2017. Transcriptome analysis and discovery of genes involved in immune pathways in large yellow croaker (Larimichthys crocea) under high stocking density stress. Fish & Shellfish Immunology, 68:332-340, https://doi.org/10.1016/j.fsi.2017.07.013.
Taillandier D, Combaret L, Pouch M N, Samuels S E, Béchet D, Attaix D. 2004. The role of ubiquitin-proteasomedependent proteolysis in the remodelling of skeletal muscle. Proceedings of the Nutrition Society, 63(2):357-361, https://doi.org/10.1079/PAR2004358.
Takahashi L S, Biller J D, Criscuolo-Urbinati E, Urbinati E C. 2011. Feeding strategy with alternate fasting and refeeding:effects on farmed pacu production. Journal of Animal Physiology and Animal Nutrition, 95(2):259-266, https://doi.org/10.1111/j.1439-0396.2010.01050.x.
Tian X L, Fang J H, Dong S L. 2010. Effects of starvation and recovery on the growth, metabolism and energy budget of juvenile tongue sole (Cynoglossus semilaevis). Aquaculture, 310(1-2):122-129, https://doi.org/10.1016/j.aquaculture.2010.10.021.
Tse W K F, Sun J, Zhang H M, Law A Y S, Yeung B H Y, Chow S C, Qiu J W, Wong C K C. 2013. Transcriptomic and iTRAQ proteomic approaches reveal novel short-term hyperosmotic stress responsive proteins in the gill of the Japanese eel (Anguilla japonica). Journal of Proteomics, 89:81-94, https://doi.org/10.1016/j.jprot.2013.05.026.
Wagner G P, Kin K, Lynch V J. 2012. Measurement of mRNA abundance using RNA-seq data:RPKM measure is inconsistent among samples. Theory in Biosciences, 131(4):281-285, https://doi.org/10.1007/s12064-012-0162-3.
Wang P P, Wang J, Su Y Q, Mao Y, Zhang J S, Wu C W, Ke Q Z, Han K H, Zheng W Q, Xu N D. 2016. Transcriptome analysis of the Larimichthys crocea liver in response to Cryptocaryon irritans. Fish & Shellfish Immunology, 48:1-11, https://doi.org/10.1016/j.fsi.2015.11.011.
Wang L, Feng Z, Wang X et al. 2010. DEGseq:an R package for identifying differentially expressed genes from RNAseq data. Bioinformatics, 26(1):136-138, https://doi.org/10.1093/bioinformatics/btp612.
Xu C, Wu G, Zohar Y, Du S J. 2003. Analysis of myostatin gene structure, expression and function in zebrafish. Journal of Experimental Biology, 206(Pt 22):4 067-4 079, https://doi.org/10.1242/jeb.00635.
Yang Y, Zhou H Q, Hou L P, Xing K, Shu H. 2019. Transcriptional profiling of skeletal muscle reveals starvation response and compensatory growth in Spinibarbus hollandi. BMC Genomics, 20(1):938, https://doi.org/10.1186/s12864-019-6345-2.
Zhang X D, Zhu Y F, Cai L S, Wu T X. 2008. Effects of fasting on the meat quality and antioxidant defenses of marketsize farmed large yellow croaker (Pseudosciaena crocea). Aquaculture, 280(1-4):136-139, https://doi.org/10.1016/j.aquaculture.2008.05.010
Zhou R X, Huang B, Meng T, Chu W Y, Cheng J, Zhao F L, Chen D X, Bin S Y, Zhang J S. 2010. Cloning and ontogenetic expression analysis of the alkali myosin light chain gene in siniperca chuasti. Acta Hydrobiologica Sinica, 34(5):927-934, https://doi.org/10.3724/SP.J.1035.2010.00927. (in Chinese with English abstract)
Copyright © Haiyang Xuebao