

FOLLOWUS
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
Liangyi XUE, E-mail: xueliangyi@nbu.edu.cn
Received:23 July 2020,
Accepted:28 September 2020,
Online First:11 November 2020,
Published:2021-09
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Yu ZHANG, Weiliang SHEN, Juan LI, et al. Effect of fasting on protein metabolism in muscle tissue of
Yu ZHANG, Weiliang SHEN, Juan LI, et al. Effect of fasting on protein metabolism in muscle tissue of
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.
A Aranda , F J Sánchez-Vázquez , J A Madrid . Effect of short-term fasting on macronutrient self-selection in sea bass . Physiology & Behavior , 2001 . 73 ( 1-2 ): 105 - 109 . http://www.onacademic.com/detail/journal_1000035473684610_5d26.html http://www.onacademic.com/detail/journal_1000035473684610_5d26.html , .
M Bach , M Larance , D E James , G Ramm . The serine/threonine kinase ULK1 is a target of multiple phosphorylation events . Biochemical Journal , 2011 . 440 ( 2 ): 283 - 291 . DOI: 10.1042/BJ20101894 http://doi.org/10.1042/BJ20101894 .
D Black , R M Love . The sequential mobilisation and restoration of energy reserves in tissues of Atlantic cod during starvation and refeeding . Journal of Comparative Physiology B , 1986 . 156 ( 4 ): 469 - 479 . DOI: 10.1007/BF00691032 http://doi.org/10.1007/BF00691032 .
A A Cassidy , R J Saulnier , S G Lamarre . Adjustments of protein metabolism in fasting Arctic charr, Salvelinus alpinus . PLoS One , 2016 . 11 ( 4 ): e0153364 DOI: 10.1371/journal.pone.0153364 http://doi.org/10.1371/journal.pone.0153364 .
A Ciechanover , D Finley , A Varshavsky . The ubiquitin-mediated proteolytic pathway and mechanisms of energy-dependent intracellular protein degradation . Journal of Cellular Biochemistry , 1984 . 24 ( 1 ): 27 - 53 . DOI: 10.1002/jcb.240240104 http://doi.org/10.1002/jcb.240240104 .
M Codina , Y H Bian , J Gutiérrez , S J Du . Cloning and characterization of myogenin from seabream ( Sparus aurata ) and analysis of promoter muscle specificity . Comparative Biochemistry and Physiology Part D: Genomics and Proteomics , 2008 . 3 ( 1 ): 128 - 139 . DOI: 10.1016/j.cbd.2007.12.001 http://doi.org/10.1016/j.cbd.2007.12.001 .
A R Cukras , D R Southworth , J L Brunelle , G M Culver , R Green . Ribosomal proteins S12 and S13 function as control elements for translocation of the mRNA: tRNA complex . Molecular Cell , 2003 . 12 ( 2 ): 321 - 328 . DOI: 10.1016/S1097-2765(03)00275-2 http://doi.org/10.1016/S1097-2765(03)00275-2 .
R N da Silva-Gomes , M L G Kuniyoshi , B O da Silva Duran , B T T Zanella , P P Freire , T G de Paula , B E de Almeida Fantinatt , R A S Salomão , R F Carvalho , L D Santos , M Dal-Pai-Silva . Prolonged fasting followed by refeeding modifies proteome profile and parvalbumin expression in the fast-twitch muscle of pacu ( Piaractus mesopotamicus ) . PLoS One , 2019 . 14 ( 12 ): e0225864 DOI: 10.1371/journal.pone.0225864 http://doi.org/10.1371/journal.pone.0225864 .
P F Finn , J F Dice . Proteolytic and lipolytic responses to starvation . Nutrition , 2006 . 22 ( 7-8 ): 830 - 844 . DOI: 10.1016/j.nut.2006.04.008 http://doi.org/10.1016/j.nut.2006.04.008 .
K P P Fraser , A D Rogers . Protein metabolism in marine animals: the underlying mechanism of growth . Advances in Marine Biology , 2007 . 52 267 - 362 . http://www.onacademic.com/detail/journal_1000035600763310_98e6.html http://www.onacademic.com/detail/journal_1000035600763310_98e6.html , .
I G Ganley , D H Lam , J R Wang , X J Ding , S Chen , X J Jiang . ULK1·ATG13·FIP200 complex mediates mTOR signaling and is essential for autophagy . The Journal of Biological Chemistry , 2009 . 284 ( 18 ): 12 297 - 12 305 . DOI: 10.1074/jbc.M900573200 http://doi.org/10.1074/jbc.M900573200 .
C Gelfi , A Viganò , M Ripamonti , A Pontoglio , S Begum , M A Pellegrino , B Grassi , R Bottinelli , R Wait , P Cerretelli . The human muscle proteome in aging . Journal of Proteome Research , 2006 . 5 ( 6 ): 1 344 - 1 353 . DOI: 10.1021/pr050414x http://doi.org/10.1021/pr050414x .
D E Goll , V F Thompson , H Q Li , W Wei , J Y Cong . The calpain system . Physiological Reviews , 2003 . 83 ( 3 ): 731 - 801 . DOI: 10.1152/physrev.00029.2002 http://doi.org/10.1152/physrev.00029.2002 .
D E Goll , V F Thompson , R G Taylor , J A Christiansen . Role of the calpain system in muscle growth . Biochimie , 1992 . 74 ( 3 ): 225 - 237 . DOI: 10.1016/0300-9084(92)90121-T http://doi.org/10.1016/0300-9084(92)90121-T .
Y H Guo , J J Bai , O Q Chang , H H Lao , X Ye , J R Luo . Molecular structure of the largemouth bass ( Micropterus salmoides ) Myf5 gene and its effect on skeletal muscle growth . Molecular Biology Reports , 2009 . 36 ( 6 ): 1 497 - 1 504 . DOI: 10.1007/s11033-008-9341-1 http://doi.org/10.1007/s11033-008-9341-1 .
E B Harvald , R R Sprenger , K B Dall , C S Ejsing , R Nielsen , S Mandrup , A B Murillo , M Larance , A Gartner , A I Lamond , N J Færgeman . Multi-omics analyses of starvation responses reveal a central role for lipoprotein metabolism in acute starvation survival in C . elegans . Cell Systems , 2017 . 5 ( 1 ): 38 - 52.e34 . DOI: 10.1016/j.cels.2017.06.004 http://doi.org/10.1016/j.cels.2017.06.004 .
A Hershko , A Ciechanover . Mechanisms of intracellular protein breakdown . Annual Review of Biochemistry , 1982 . 51 335 - 364 . DOI: 10.1146/annurev.bi.51.070182.002003 http://doi.org/10.1146/annurev.bi.51.070182.002003 .
A Hershko , H Heller . Occurrence of a polyubiquitin structure in ubiquitin-protein conjugates . Biochemical and Biophysical Research Communications , 1985 . 128 ( 3 ): 1079 - 1086 . DOI: 10.1016/0006-291X(85)91050-2 http://doi.org/10.1016/0006-291X(85)91050-2 .
L L Hu , S J Ren , Q Shen , J C Chen , X Q Ye , J G Ling . Proteomic study of the effect of different cooking methods on protein oxidation in fish fillets . RSC Advances , 2017 . 7 ( 44 ): 27 496 - 27 505 . DOI: 10.1039/C7RA03408C http://doi.org/10.1039/C7RA03408C .
D W Huang , B T Sherman , R A Lempicki . Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources . Nature Protocols , 2008 . 4 ( 1 ): 44 - 57 . http://www.ff.ul.pt/FCT/PTDC/SAU-GMG/104781/30.pdf http://www.ff.ul.pt/FCT/PTDC/SAU-GMG/104781/30.pdf , .
D W Huang , B T Sherman , R A Lempicki . Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists . Nucleic Acids Research , 2009 . 37 ( 1 ): 1 - 13 . DOI: 10.1093/nar/gkn923 http://doi.org/10.1093/nar/gkn923 .
M A Ilian , N E Forsberg . Gene expression of calpains and their specific endogenous inhibitor, calpastatin, in skeletal muscle of fed and fasted rabbits . Biochemical Journal , 1992 . 287 ( Pt 1 ): 163 - 171 . http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1133139/pdf/biochemj00126-0164.pdf http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1133139/pdf/biochemj00126-0164.pdf , .
I A Johnston , N I Bower , D J Macqueen . Growth and the regulation of myotomal muscle mass in teleost fish . Journal of Experimental Biology , 2011 . 214 ( Pt 10 ): 1 617 - 1 628 . http://jeb.biologists.org/cgi/reprint/214/10/1617 http://jeb.biologists.org/cgi/reprint/214/10/1617 , .
M L G Kuniyoshi , R N Da Silva-Gomes , J C S Vieira , M C Hessel , E A Mareco , V B D Santos , R F Carvalho , P De Magalhães Padilha , M Dal-Pai-Silva . 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 , 2019 . 30 321 - 332 . DOI: 10.1016/j.cbd.2019.04.005 http://doi.org/10.1016/j.cbd.2019.04.005 .
B Langmead , C Trapnell , M Pop , S L Salzberg . Ultrafast and memory-efficient alignment of short DNA sequences to the human genome . Genome Biology , 2009 . 10 ( 3 ): R25 DOI: 10.1186/gb-2009-10-3-r25 http://doi.org/10.1186/gb-2009-10-3-r25 .
F Lavajoo , M Perelló-Amorós , E J Vélez , A Sánchez-Moya , S Balbuena-Pecino , N Riera-Heredia , J Fernández-Borràs , J Blasco , I Navarro , E Capilla , J Gutiérrez . Regulatory mechanisms involved in muscle and bone remodeling during refeeding in gilthead sea bream . Scientific Reports , 2020 . 10 ( 1 ): 184 - 184 . DOI: 10.1038/s41598-019-57013-6 http://doi.org/10.1038/s41598-019-57013-6 .
S H Lecker , A L Goldberg , W E Mitch . Protein degradation by the ubiquitin-proteasome pathway in normal and disease states . Journal of the American Society of Nephrology , 2006 . 17 ( 7 ): 1 807 - 1 819 . DOI: 10.1681/ASN.2006010083 http://doi.org/10.1681/ASN.2006010083 .
M Long , J Zhao , T T Li , C Tafalla , Q Q Zhang , X H Wang , X N Gong , Z X Shen , A H Li . Transcriptomic and proteomic analyses of splenic immune mechanisms of rainbow trout ( Oncorhynchus mykiss ) infected by Aeromonas salmonicida subsp . salmonicida. Journal of Proteomics , 2015 . 122 41 - 54 . DOI: 10.1016/j.jprot.2015.03.031 http://doi.org/10.1016/j.jprot.2015.03.031 .
Q Ma , X F Liu , W R Feng , S F Liu , Z M Zhuang . 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 , 2018 . 136 40 - 53 . DOI: 10.1016/j.pbiomolbio.2018.02.003 http://doi.org/10.1016/j.pbiomolbio.2018.02.003 .
D M Maddock , M P M Burton . Some effects of starvation on the lipid and skeletal muscle layers of the winter flounder, Pleuronectes americanus . Canadian Journal of Zoology , 1994 . 72 ( 9 ): 1 672 - 1 679 . DOI: 10.1139/z94-223 http://doi.org/10.1139/z94-223 .
S Martin , S Blaney , A Bowman , D Houlihan . Ubiquitin-proteasome-dependent proteolysis in rainbow trout ( Oncorhynchus mykiss ): effect of food deprivation . Pflügers Archiv , 2002 . 445 ( 2 ): 257 - 266 . DOI: 10.1007/s00424-002-0916-8 http://doi.org/10.1007/s00424-002-0916-8 .
T Mélèse , Z X Xue . The nucleolus: an organelle formed by the act of building a ribosome . Current Opinion in Cell Biology , 1995 . 7 ( 3 ): 319 - 324 . DOI: 10.1016/0955-0674(95)80085-9 http://doi.org/10.1016/0955-0674(95)80085-9 .
N Mizushima , A Yamamoto , M Matsui , T Yoshimori , Y Ohsumi . In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker . Molecular Biology of the Cell , 2004 . 15 ( 3 ): 1 101 - 1 111 . DOI: 10.1091/mbc.e03-09-0704 http://doi.org/10.1091/mbc.e03-09-0704 .
T P Mommsen . Salmon spawning migration and muscle protein metabolism: the August Krogh principle at work . Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology , 2004 . 139 ( 3 ): 383 - 400 . DOI: 10.1016/j.cbpc.2004.09.018 http://doi.org/10.1016/j.cbpc.2004.09.018 .
M A Moses , D Wiederschain , I Wu , C A Fernandez , V Ghazizadeh , W S Lane , E Flynn , A Sytkowski , T Tao , R Langer . Troponin I is present in human cartilage and inhibits angiogenesis . Proceedings of the National Academy of Sciences of the United States of America , 1999 . 96 ( 6 ): 2 645 - 2 650 . DOI: 10.1073/pnas.96.6.2645 http://doi.org/10.1073/pnas.96.6.2645 .
M J Neave , C Streten-Joyce , A S Nouwens , C J Glasby , K A McGuinness , D L Parry , K S Gibb . The transcriptome and proteome are altered in marine polychaetes (Annelida) exposed to elevated metal levels . Journal of Proteomics , 2012 . 75 ( 9 ): 2 721 - 2 735 . DOI: 10.1016/j.jprot.2012.03.031 http://doi.org/10.1016/j.jprot.2012.03.031 .
I Piec , A Listrat , J Alliot , C Chambon , R G Taylor , D Bechet . Differential proteome analysis of aging in rat skeletal muscle . FASEB Journal Official Publication of the Federation of American Societies for Experimental Biology , 2005 . 19 ( 9 ): 1 143 - 1 145 . DOI: 10.1096/fj.04-3084fje http://doi.org/10.1096/fj.04-3084fje .
J Purintrapiban , M C Wang , N E Forsberg . Degradation of sarcomeric and cytoskeletal proteins in cultured skeletal muscle cells . Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology , 2003 . 136 ( 3 ): 393 - 401 . DOI: 10.1016/S1096-4959(03)00201-X http://doi.org/10.1016/S1096-4959(03)00201-X .
B Y Qian , L Y Xue , H L Huang . Liver transcriptome analysis of the large yellow croaker ( Larimichthys crocea ) during fasting by using RNA-Seq . PLoS One , 2016 . 11 ( 3 ): e0150240 DOI: 10.1371/journal.pone.0150240 http://doi.org/10.1371/journal.pone.0150240 .
O A Radhi , S Davidson , F Scott , R X Zeng , D H Jones , N C O Tomkinson , J Yu , E Y W Chan . Inhibition of the ULK1 protein complex suppresses Staphylococcus -induced autophagy and cell death . Journal of Biological Chemistry , 2019 . 294 ( 39 ): 14 289 - 14 307 . DOI: 10.1074/jbc.RA119.008923 http://doi.org/10.1074/jbc.RA119.008923 .
P Y Rescan , J Montfort , C Rallière , A L Cam , D Esquerré , K Hugot . Dynamic gene expression in fish muscle during recovery growth induced by a fasting-refeeding schedule . BMC Genomics , 2007 . 8 438 DOI: 10.1186/1471-2164-8-438 http://doi.org/10.1186/1471-2164-8-438 .
M Salem , J Silverstein , C E Rexroad Ⅲ , J B Yao . Effect of starvation on global gene expression and proteolysis in rainbow trout ( Oncorhynchus mykiss ) . BMC Genomics , 2007 . 8 328 DOI: 10.1186/1471-2164-8-328 http://doi.org/10.1186/1471-2164-8-328 .
C Salmerón , D G de la Serrana , V Jiménez-Amilburu , R Fontanillas , I Navarro , I A Johnston , J Gutiérrez , E Capilla . 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 , 2013 . 8 ( 9 ): e75349 DOI: 10.1371/journal.pone.0075349 http://doi.org/10.1371/journal.pone.0075349 .
I Seiliez , F Médale , P Aguirre , M Larquier , L Lanneretonne , H Alami-Durante , S Panserat , S Skiba-Cassy . Postprandial regulation of growth- and metabolism-related factors in zebrafish . Zebrafish , 2013 . 10 ( 2 ): 237 - 248 . DOI: 10.1089/zeb.2012.0835 http://doi.org/10.1089/zeb.2012.0835 .
I Seiliez , S Panserat , S Skiba-Cassy , A Fricot , C Vachot , S Kaushik , S Tesseraud . Feeding status regulates the polyubiquitination step of the ubiquitin-proteasome-dependent proteolysis in rainbow trout ( Oncorhynchus mykiss ) muscle . Journal of Nutrition , 2008 . 138 ( 3 ): 487 - 491 . DOI: 10.1093/jn/138.3.487 http://doi.org/10.1093/jn/138.3.487 .
V Solomon , A L Goldberg . Importance of the ATP-ubiquitin-proteasome pathway in the degradation of soluble and myofibrillar proteins in rabbit muscle extracts . Journal of Biological Chemistry , 1996 . 271 ( 43 ): 26 690 - 26 697 . DOI: 10.1074/jbc.271.43.26690 http://doi.org/10.1074/jbc.271.43.26690 .
P Sun , P B Bao , B J Tang . Transcriptome analysis and discovery of genes involved in immune pathways in large yellow croaker ( Larimichthys crocea ) under high stocking density stress . Fish & Shellfish Immunology , 2017 . 68 332 - 340 . http://www.sciencedirect.com/science/article/pii/S1050464817304060 http://www.sciencedirect.com/science/article/pii/S1050464817304060 , .
D Taillandier , L Combaret , M N Pouch , S E Samuels , D Béchet , D Attaix . The role of ubiquitin-proteasome-dependent proteolysis in the remodelling of skeletal muscle . Proceedings of the Nutrition Society , 2004 . 63 ( 2 ): 357 - 361 . DOI: 10.1079/PAR2004358 http://doi.org/10.1079/PAR2004358 .
L S Takahashi , J D Biller , E Criscuolo-Urbinati , E C Urbinati . Feeding strategy with alternate fasting and refeeding: effects on farmed pacu production . Journal of Animal Physiology and Animal Nutrition , 2011 . 95 ( 2 ): 259 - 266 . DOI: 10.1111/j.1439-0396.2010.01050.x http://doi.org/10.1111/j.1439-0396.2010.01050.x .
X L Tian , J H Fang , S L Dong . Effects of starvation and recovery on the growth, metabolism and energy budget of juvenile tongue sole ( Cynoglossus semilaevis ) . Aquaculture , 2010 . 310 ( 1-2 ): 122 - 129 . DOI: 10.1016/j.aquaculture.2010.10.021 http://doi.org/10.1016/j.aquaculture.2010.10.021 .
W K F Tse , J Sun , H M Zhang , A Y S Law , B H Y Yeung , S C Chow , J W Qiu , C K C Wong . 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 , 2013 . 89 81 - 94 . DOI: 10.1016/j.jprot.2013.05.026 http://doi.org/10.1016/j.jprot.2013.05.026 .
G P Wagner , K Kin , V J Lynch . Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples . Theory in Biosciences , 2012 . 131 ( 4 ): 281 - 285 . DOI: 10.1007/s12064-012-0162-3 http://doi.org/10.1007/s12064-012-0162-3 .
P P Wang , J Wang , Y Q Su , Y Mao , J S Zhang , C W Wu , Q Z Ke , K H Han , W Q Zheng , N D Xu . Transcriptome analysis of the Larimichthys crocea liver in response to Cryptocaryon irritans . Fish & Shellfish Immunology , 2016 . 48 1 - 11 . http://www.onacademic.com/detail/journal_1000038403387710_d6e1.html http://www.onacademic.com/detail/journal_1000038403387710_d6e1.html , .
L Wang , Z Feng , X Wang , 等 . DEGseq: an R package for identifying differentially expressed genes from RNA-seq data . Bioinformatics , 2010 . 26 ( 1 ): 136 - 138 . DOI: 10.1093/bioinformatics/btp612 http://doi.org/10.1093/bioinformatics/btp612 .
C Xu , G Wu , Y Zohar , S J Du . Analysis of myostatin gene structure, expression and function in zebrafish . Journal of Experimental Biology , 2003 . 206 ( Pt 22 ): 4 067 - 4 079 . http://pdfs.semanticscholar.org/4eef/b084058d0cda9ae2e5c7e258b8b61c85dbfe.pdf http://pdfs.semanticscholar.org/4eef/b084058d0cda9ae2e5c7e258b8b61c85dbfe.pdf , .
Y Yang , H Q Zhou , L P Hou , K Xing , H Shu . Transcriptional profiling of skeletal muscle reveals starvation response and compensatory growth in Spinibarbus hollandi . BMC Genomics , 2019 . 20 ( 1 ): 938 DOI: 10.1186/s12864-019-6345-2 http://doi.org/10.1186/s12864-019-6345-2 .
X D Zhang , Y F Zhu , L S Cai , T X Wu . Effects of fasting on the meat quality and antioxidant defenses of market-size farmed large yellow croaker ( Pseudosciaena crocea ) . Aquaculture , 2008 . 280 ( 1-4 ): 136 - 139 . DOI: 10.1016/j.aquaculture.2008.05.010 http://doi.org/10.1016/j.aquaculture.2008.05.010 .
R X Zhou , B Huang , T Meng , W Y Chu , J Cheng , F L Zhao , D X Chen , S Y Bin , J S Zhang . Cloning and ontogenetic expression analysis of the alkali myosin light chain gene in siniperca chuasti . Acta Hydrobiologica Sinica , 2010 . 34 ( 5 ): 927 - 934 . DOI: 10.3724/SP.J.1035.2010.00927 http://doi.org/10.3724/SP.J.1035.2010.00927 .
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