Transcriptome analysis provided a new insight into the gene expression profiles of muscle after exercise training of juvenile Schizothorax wangchiachii
Springer Science and Business Media LLC - Trang 1-20 - 2024
Tóm tắt
The hatchery-raised juveniles of Schizothorax wangchiachii, a species widely distributed in the Jinsha River and its tributaries in China, have shown improved swimming performance through exercise training. Understanding the underlying biological processes and molecular mechanisms responsible for this enhanced swimming ability is crucial. In this research, the transcriptome of muscle tissue was sequenced for juvenile S. wangchiachii subjected to exercise training. After thorough data processing, a total of 113,814 unigenes were obtained, with 57,500 of them annotated using various datasets including Pfam, GO, COG, Swiss-Prot, NR, and KEGG. The study identified 889 differentially expressed genes (DEGs) between the experimental and control groups after 30 days of exercise training, of which 439 were upregulated and 450 downregulated. Enrichment analysis highlighted that these DEGs were predominantly involved in molecular processes such as protein metabolism and breakdown, neurodevelopment, immunity, and growth and development. The expression patterns of the DEGs were validated through real-time PCR, corroborating the findings derived from transcriptome analysis. Further experimental investigation led to the recognition of MYLPF as a potential functional candidate gene for swimming ability in S. wangchiachii. The results provide novel insights into how S. wangchiachii adapts to exercise training, contributing to a deeper comprehension of the mechanisms that underlie exercise-induced improvements in fish swimming performance.
Tài liệu tham khảo
Berkman SJ, Roscoe EM, Bourret JC (2019) Comparing self-directed methods for training staff to create graphs using Graphpad Prism. J Appl Behav Anal 52:188–204. https://doi.org/10.1002/jaba.522
Berna-Erro A, Jardin I, Salido GM, Rosado JA (2017) Role of STIM2 in cell function and physiopathology. J Physiol-London 595:3111–3128. https://doi.org/10.1113/jp273889
Boutilier JK, Taylor RL, Ram R, McNamara E, Nguyen Q, Goullee H, Chandler D, Mehta M, Balmer L, Laing NG, Morahan G, Nowak KJ (2017) Variable cardiac alpha-actin (Actc1) expression in early adult skeletal muscle correlates with promoter methylation. Biochim Biophys Acta-Gene Regul Mech 1860:1025–1036. https://doi.org/10.1016/j.bbagrm.2017.08.004
Camps J, Erdos MR, Ried T (2015) The role of lamin B1 for the maintenance of nuclear structure and function. Nucleus 6:8–14. https://doi.org/10.1080/19491034.2014.1003510
Castro V, Grisdale-Helland B, Helland SJ, Kristensen T, Jorgensen SM, Helgerud J, Claireaux G, Farrell AP, Krasnov A, Takle H (2011) Aerobic training stimulates growth and promotes disease resistance in Atlantic salmon (Salmo salar). Comp Biochem Physiol A-Mol Integr Physiol 160:278–290. https://doi.org/10.1016/j.cbpa.2011.06.013
Chang TJ, Wang WC, Hsiung CA, He CT, Lin MW, Sheu WHH, Chang YC, Quertermous T, Chen YDI, Rotter JI, Chuang LM, Grp SAS (2018) Genetic variation of SORBS1 gene is associated with glucose homeostasis and age at onset of diabetes: A SAPPHIRe Cohort Study. Sci Rep 8. https://doi.org/10.1038/s41598-018-28891-z
Chrifi I, Hermkens D, Brandt MM, van Dijk CGM, Bürgisser PE, Haasdijk R, Pei JY, van de Kamp EHM, Zhu CB, Blonden L, Kros JM, Duncker DJ, Duckers HJ, Cheng C (2017) Cgnl1, an endothelial junction complex protein, regulates GTPase mediated angiogenesis. Cardiovasc Res 113:1776–1788. https://doi.org/10.1093/cvr/cvx175
Darbellay B, Arnaudeau S, Ceroni D, Bader CR, Konig S, Bernheim L (2010) Human Muscle economy myoblast differentiation and excitation-contraction coupling use the same molecular partners, STIM1 and STIM2. J Biol Chem 285:22437–22447. https://doi.org/10.1074/jbc.M110.118984
DePasquale C, Leri J (2018) The influence of exercise on anxiety-like behavior in zebrafish (Danio rerio). Behav Proc 157:638–644. https://doi.org/10.1016/j.beproc.2018.04.006
Ecimovic P, Murray D, Doran P, McDonald J, Lambert DG, Buggy DJ (2011) Direct effect of morphine on breast cancer cell function in vitro: role of the NET1 gene. BJA: Br J Anaesth 107:916–923. https://doi.org/10.1093/bja/aer259
Fu LM, Niu BF, Zhu ZW, Wu ST, Li WZ (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28:3150–3152. https://doi.org/10.1093/bioinformatics/bts565
Gadadhar S, Bodakuntla S, Natarajan K, Janke C (2017) The tubulin code at a glance. J Cell Sci 130:1347–1353. https://doi.org/10.1242/jcs.199471
Gao XH, Xia JS, Munoz FM, Manners MT, Pan R, Meucci O, Dai Y, Hu HJ (2016) STIMs and Orai1 regulate cytokine production in spinal astrocytes. J Neuroinflamm 13. https://doi.org/10.1186/s12974-016-0594-7
Garred P, Honoré C, Ma YJ, Munthe-Fog L, Hummelshoj T (2009) MBL2, FCN1, FCN2 and FCN3-The genes behind the initiation of the lectin pathway of complement. Mol Immunol 46:2737–2744. https://doi.org/10.1016/j.molimm.2009.05.005
Goll DE, Neti G, Mares SW, Thompson VF (2008) The calpains, proteasome, and myofibrillar protein turnover. J Anim Sci 85:445–446. https://doi.org/10.2527/jas.2007-0395
Grabherr MG et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644-U130. https://doi.org/10.1038/nbt.1883
Guo ST, Gao WX, Zeng MS, Liu FL, Yang QZM, Chen L, Wang ZS, Jin YJ, Xiang P, Chen HX, Wen ZY, Shi Q, Song ZB (2023a) Characterization of TLR1 and expression profiling of TLR signaling pathway related genes in response to Aeromonas hydrophila challenge in hybrid yellow catfish (Pelteobagrus fulvidraco ♀ x P. vachelli ♂). Front Immunol 14. https://doi.org/10.3389/fimmu.2023.1163781
Guo ST, Zeng MS, Gao WX, Li F, Wei XY, Shi Q, Wen ZY, Song ZB (2023b) Toll-like receptor 3 in the hybrid yellow catfish (Pelteobagrus fulvidraco ♀ x P. vachelli ♂): Protein structure, evolution and immune response to exogenous Aeromonas hydrophila and poly (I:C) stimuli. Animals 13. https://doi.org/10.3390/ani13020288
Haas BJ et al (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512. https://doi.org/10.1038/nprot.2013.084
Hou Y, Yang Z, An R, Cai L, Chen X, Zhao X, Zou X (2019) Water flow and substrate preferences of Schizothorax wangchiachii (Fang, 1936). Ecol Eng 138:1–7. https://doi.org/10.1016/j.ecoleng.2019.07.008
Ishfaq M, Bashir N, Riaz SK, Manzoor S, Khan JS, Bibi Y, Sami R, Aljahani AH, Alharthy SA, Shahid R (2022) Expression of HK2, PKM2,and PFKM is associated with metastasis and late disease onset in breast cancer patients. Genes 13. https://doi.org/10.3390/genes13030549
Ji JP, Li HB, Wang WJ, Yuan B, Shen TY (2022) ARPC1A is regulated by STAT3 to inhibit ferroptosis and promote prostate cancer progression. Hum Cell 35:1591–1601. https://doi.org/10.1007/s13577-022-00754-w
Jonsson N, Jonsson B, Hansen LP (2003) The marine survival and growth of wild and hatchery-reared Atlantic salmon. J Appl Ecol 40:900–911. https://doi.org/10.1046/j.1365-2664.2003.00851.x
Klopfenstein DV, Zhang LS, Pedersen BS, Ramirez F, Vesztrocy AW, Naldi A, Mungall CJ, Yunes JM, Botvinnik O, Weigel M, Dampier W, Dessimoz C, Flick P, Tang HB (2018): GOATOOLS: A Python library for Gene Ontology analyses. Sci Rep 8. https://doi.org/10.1038/s41598-018-28948-z
Kopp R, Koblitz L, Egg M, Pelster B (2011) HIF signaling and overall gene expression changes during hypoxia and prolonged exercise differ considerably. Physiol Genomics 43:506–516. https://doi.org/10.1152/physiolgenomics.00250.2010
Kwon Y, Choi Y, Kim M, Jeong MS, Jung HS, Jeoung D (2021) HDAC6 and CXCL13 mediate atopic dermatitis by regulating cellular interactions and expression level bv s of miR-9 and SIRT1. Front Pharmacol 12:2468. https://doi.org/10.3389/fphar.2021.691279
LeMoine CMR, Craig PM, Dhekney K, Kim JJ, McClelland GB (2010) Temporal and spatial patterns of gene expression in skeletal muscles in response to swim training in adult zebrafish (Danio rerio). J Comp Physiol B-Biochem Syst Environ Physiol 180:151–160. https://doi.org/10.1007/s00360-009-0398-5
Li SJ, Liu H, Bai JJ, Zhu XP (2017a) Transcriptome assembly and identification of genes and SNPs associated with growth traits in largemouth bass (Micropterus salmoides). Genetica 145:175–187. https://doi.org/10.1007/s10709-017-9956-z
Li XM, Pang X, Zheng H, Li XJ, Fu SJ, Zhang YG (2017b) Effects of prolonged exercise training and exhaustive chasing training on the swimming performance of an endangered bream Megalobrama pellegrini. Aquat Biol 26:125–135. https://doi.org/10.3354/ab00681
Liang X, Wan Y, Shen ZY, Liu YM, Li DP, Li L, Tang R, Zhang X (2021) Molecular Characterization of Hsp47 in Grass Carp (Ctenopharyngodon idella) and Its Correlation with Type I Collagen in Response to Fish Aerobic Exercise. Fishes 6. https://doi.org/10.3390/fishes6020017
Liu L, Dang YF (2020) Antimicrobial activity of mannose binding lectin in grass carp (Ctenopharyngodon idella) in vivo and in vitro. Fish Shellfish Immunol 98:25–33. https://doi.org/10.1016/j.fsi.2019.12.088
Liu GY, Wu YJ, Qin XH, Shi XT, Wang XL (2018) The effect of aerobic exercise training on growth performance, innate immune response and disease resistance in juvenile Schizothorax prenanti. Aquaculture 486:18–25. https://doi.org/10.1016/j.aquaculture.2017.12.006
Liu H, Guo S, He Y, Shi Q, Yang M, You X (2021) Toll protein family structure, evolution and response of the whiteleg shrimp (Litopenaeus vannamei) to exogenous iridescent virus. J Fish Dis 44:1131–1145. https://doi.org/10.1111/jfd.13374
Lu Y, Wu H, Deng L-j, Li T-c, Yang K, Fu S-j, Song Z-b (2020) Improved aerobic and anaerobic swimming performance after exercise training and detraining in Schizothorax wangchiachii: Implications for fisheries releases. Comp Biochem Physiol A: Mol Integr Physiol 245:110698. https://doi.org/10.1016/j.cbpa.2020.110698
Luchiari AC, Chacon DMM (2013) Physical exercise improves learning in zebrafish, Danio rerio. Behav Proc 100:44–47. https://doi.org/10.1016/j.beproc.2013.07.020
Ma HN, Jin M, Zhu TT, Li CC, Lu Y, Yuan Y, Xiong J, Zhou QC (2018) Effect of dietary arachidonic acid levels on growth performance, fatty acid profiles and lipid metabolism of juvenile yellow catfish (Pelteobagrus fulvidraco). Aquaculture 486:31–41. https://doi.org/10.1016/j.aquaculture.2017.11.055
Martin-Perez M, Fernandez-Borras J, Ibarz A, Millan-Cubillo A, Felip O, de Oliveira E, Blasco J (2012) New insights into fish swimming: a proteomic and isotopic approach in gilthead sea bream. J Proteome Res 11:3533–3547. https://doi.org/10.1021/pr3002832
Mes D, Palstra AP, Henkel C, Mayer I, Vindas MA (2020) Swimming exercise enhances brain plasticity in fish. R Soc Open Sci 7. https://doi.org/10.1098/rsos.191640
Meskyte EM, Keskas S, Ciribilli Y (2020) MYC as a multifaceted regulator of tumor microenvironment leading to metastasis. Int J Mol Sci 21. https://doi.org/10.3390/ijms21207710
Miller LM, Close T, Kapuscinski AR (2004) Lower fitness of hatchery and hybrid rainbow trout compared to naturalized populations in Lake Superior tributaries. Mol Ecol 13:3379–3388. https://doi.org/10.1111/j.1365-294X.2004.02347.x
Nakamura M, Kumrungsee T, Sakuma T, Yamamoto T, Yanaka N (2017) TALEN-mediated targeted editing of the GDE5 gene suppresses fibroblastic cell proliferation. Biosci Biotechnol Biochem 81:2164–2167. https://doi.org/10.1080/09168451.2017.1373593
Noreen M, Arshad M (2015) Association of TLR1, TLR2, TLR4, TLR6, and TIRAP polymorphisms with disease susceptibility. Immunol Res 62:234–252. https://doi.org/10.1007/s12026-015-8640-6
Okazaki Y, Nakamura K, Takeda S, Yoshizawa I, Yoshida F, Ohshima N, Izumi T, Klein JD, Kumrungsee T, Sands JM, Yanaka N (2019) GDE5 inhibition accumulates intracellular glycerophosphocholine and suppresses adipogenesis at a mitotic clonal expansion stage. Am J Physiol Cell Physiol 316:C162–C174. https://doi.org/10.1152/ajpcell.00305.2018
Owa T, Taya S, Miyashita S, Yamashita M, Adachi T, Yamada K, Yokoyama M, Aida S, Nishioka T, Inoue YU, Goitsuka R, Nakamura T, Inoue T, Kaibuchi K, Hoshino M (2018) Meis1 coordinates cerebellar granule cell development by regulating Pax6 transcription, BMP signaling and Atoh1 degradation. J Neurosci 38:1277–1294. https://doi.org/10.1523/jneurosci.1545-17.2017
Palstra AP, Tudorache C, Rovira M, Brittijn SA, Burgerhout E, van den Thillart G, Spaink HP, Planas JV (2010) Establishing zebrafish as a novel exercise model: swimming economy, swimming-enhanced growth and muscle growth marker gene expression. Plos One 5. https://doi.org/10.1371/journal.pone.0014483
Palstra AP, Beltran S, Burgerhout E, Brittijn SA, Magnoni LJ, Henkel CV, Jansen HJ, van den Thillart G, Spaink HP, Planas JV (2013) Deep RNA sequencing of the skeletal muscle transcriptome in swimming fish. Plos One 8. https://doi.org/10.1371/journal.pone.0053171
Palstra AP, Roque A, Kruijt L, Jéhannet P, Pérez-Sánchez J, Dirks RP (2020) Physiological effects of water flow induced swimming exercise in seabream Sparus aurata. Front Physiol 11. https://doi.org/10.3389/fphys.2020.610049
Palstra AP, Planas JV (2011) Fish under exercise. Fish Physiol Biochem 37:259–272. https://doi.org/10.1007/s10695-011-9505-0
Pasello M, Giudice AM, Scotlandi K (2020) The ABC subfamily A transporters: multifaceted players with incipient potentialities in cancer. Semin Cancer Biol 60:57–71. https://doi.org/10.1016/j.semcancer.2019.10.004
Pedersen BK (2011) Muscles and their myokines. J Exp Biol 214:337–346. https://doi.org/10.1242/jeb.048074
Pettersson AML, Stenson BM, Lorente-Cebrian S, Andersson DP, Mejhert N, Kratzel J, Astrom G, Dahlman I, Chibalin AV, Arner P, Laurencikiene J (2013) LXR is a negative regulator of glucose uptake in human adipocytes. Diabetologia 56:2044–2054. https://doi.org/10.1007/s00125-013-2954-5
Pizarro-Cerdá J, Chorev DS, Geiger B, Cossart P (2017) The diverse family of Arp2/3 complexes. Trends Cell Biol 27:93–100. https://doi.org/10.1016/j.tcb.2016.08.001
Qiu K, Xu DD, Wang LQ, Zhang X, Jiao N, Gong L, Yin JD (2020) Association analysis of single-cell RNA sequencing and proteomics reveals a vital role of Ca2+ signaling in the determination of skeletal muscle development potential. Cells 9. https://doi.org/10.3390/cells9041045
Rovira M, Arrey G, Planas JV (2017) Exercise-Induced hypertrophic and oxidative signaling pathways and myokine expression in fast muscle of adult zebrafish. Front Physiol 8. https://doi.org/10.3389/fphys.2017.01063
Rovira M, Borras DM, Marques IJ, Puig C, Planas JV (2018) Physiological responses to swimming-induced exercise in the adult zebrafish regenerating heart. Front Physiol 9. https://doi.org/10.3389/fphys.2018.01362
Schlaepfer IR, Joshi M (2020) CPT1A-mediated fat oxidation, mechanisms, and therapeutic potential. Endocrinol 161. https://doi.org/10.1210/endocr/bqz046
Shek PN, Shephard RJ (1998) Physical exercise as a human model of limited inflammatory response. Can J Physiol Pharmacol 76:589–597. https://doi.org/10.1139/cjpp-76-5-589
Sheng JJ, Jin JP (2016) TNNI1, TNNI2 and TNNI3: evolution, regulation, and protein structure-function relationships. Gene 576:385–394. https://doi.org/10.1016/j.gene.2015.10.052
Simao FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–3212. https://doi.org/10.1093/bioinformatics/btv351
Sinclair ELE, de Souza CRN, Ward AJW, Seebacher F (2014) Exercise changes behaviour. Funct Ecol 28:652–659. https://doi.org/10.1111/1365-2435.12198
Smith-Unna R, Boursnell C, Patro R, Hibberd JM, Kelly S (2016) TransRate: reference-free quality assessment of de novo transcriptome assemblies. Genome Res 26:1134–1144. https://doi.org/10.1101/gr.196469.115
Sun SY, Zhang H, Liu J, Popugaeva E, Xu NJ, Feske S, White CL, Bezprozvanny I (2014) Reduced synaptic STIM2 expression and impaired store-operated calcium entry cause destabilization of mature spines in mutant presenilin mice. Neuron 82:79–93. https://doi.org/10.1016/j.neuron.2014.02.019
Tawk M, Araya C, Lyons DA, Reugels AM, Girdler GC, Bayley PR, Hyde DR, Tada M, Clarke JDW (2007) A mirror-symmetric cell division that orchestrates neuroepithelial morphogenesis. Nature 446:797–800. https://doi.org/10.1038/nature05722
Taylor MD, Chick RC, Lorenzen K, Agnalt AL, Leber KM, Blankenship HL, Haegen GV, Loneragan NR (2017) Fisheries enhancement and restoration in a changing world. Fish Res 186:407–412. https://doi.org/10.1016/j.fishres.2016.10.004
Tidball JG (2017) Regulation of muscle growth and regeneration by the immune system. Nat Rev Immunol 17:165–178. https://doi.org/10.1038/nri.2016.150
Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74. https://doi.org/10.1093/nar/gkm306
Vaeth M, Eckstein M, Shaw PJ, Kozhaya L, Yang J, Berberich-Siebelt F, Clancy R, Unutmaz D, Feske S (2016) Store-operated Ca2+ entry in follicular T cells controls humoral immune responses and autoimmunity. Immunity 44:1350–1364. https://doi.org/10.1016/j.immuni.2016.04.013
van der Meulen T, Schipper H, van den Boogaart JGM, Huising MO, Kranenbarg S, van Leeuwen JL (2006) Endurance exercise differentially stimulates heart and axial muscle development in zebrafish (Danio rerio). Am J Physiol-Regul Integ Comp Physiol 291:R1040–R1048. https://doi.org/10.1152/ajpregu.00116.2006
Vasilev VV, Radanova M, Lazarov VJ, Dragon-Durey MA, Fremeaux-Bacchi V, Roumenina LT (2019) Autoantibodies against C3b-functional consequences and disease relevance. Front Immunol 10. https://doi.org/10.3389/fimmu.2019.00064
Velez EJ, Azizi S, Millan-Cubillo A, Fernandez-Borras J, Blasco J, Chan SJ, Calduch-Giner JA, Perez-Sanchez J, Navarro I, Capilla E, Gutierrez J (2016) Effects of sustained exercise on GH-IGFs axis in gilthead sea bream (Sparus aurata). Am J Physiol-Regul Integr Comp Physiol 310:R313–R322. https://doi.org/10.1152/ajpregu.00230.2015
Wang YC, Szczesna-Cordary D, Craig R, Diaz-Perez Z, Guzman G, Miller T, Potter JD (2007) Fast skeletal muscle regulatory light chain is required for fast and slow skeletal muscle development. FASEB J 21:2205–2214. https://doi.org/10.1096/fj.06-7538com
Wiendl H, Hohlfeld R, Kieseier BC (2005) Immunobiology of muscle: advances in understanding an immunological microenvironment. Trends Immunol 26:373–380. https://doi.org/10.1016/j.it.2005.05.003
Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li C-Y, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39:W316–W322. https://doi.org/10.1093/nar/gkr483
Xu Z (2009) The influence of differential expression proteome of right ventricular muscle of rat under the eight weeks aerobic exercise. Dissertation, Hunan Normal University
Yang K, Li S, Liu XS, Gan WX, Deng LJ, Tang YZ, Song ZB (2017) Mass marking of juvenile Schizothorax wangchiachii (Fang) with alizarin red S and evaluation of stock enhancement in the Jinping area of the Yalong River. Peerj 5. https://doi.org/10.7717/peerj.4142
Young PS, Cech JJ (1993) Improved growth, swimming performance, and muscular development in exercise-conditioned young-of-the-year striped bass (Morone-Saxatilis). Can J Fish Aquat Sci 50:703–707. https://doi.org/10.1139/f93-080
Zhang C, Zhang X, Han Z, Zhu H, Wan T (2020) Silence of cytoskeleton-associated protein 2 represses cell proliferation and migration and promotes apoptosis in liver cancer cell lines. Zhong Nan Da Xue Xue Bao Yi Xue Ban 45:365–371. https://doi.org/10.11817/j.issn.1672-7347.2020.180798
Zhang X, Wang X, Li Q, Chen Y, Zhang X, Wang P, Yuan M, Pei H (2022) Role of PNPT1 in cardiomyocyte apoptosis induced by oxygen-glucose deprivation. Nan Fang Yi Ke Da Xue Xue Bao 42:584–590. https://doi.org/10.12122/j.issn.1673-4254.2022.04.15