Integrative Transcriptomic and Small RNA Sequencing Reveals Immune-Related miRNA–mRNA Regulation Network for Soybean Meal-Induced Enteritis in Hybrid Grouper, Epinephelus fuscoguttatus♀ × Epinephelus lanceolatus

A 10-week feeding experiment was conducted to reveal the immune mechanism for soybean meal-induced enteritis (SBMIE) in hybrid grouper, Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂. Four isonitrogenous and isolipidic diets were formulated by replacing 0, 10, 30, and 50% fish meal protein...

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Published inFrontiers in immunology Vol. 11; p. 1502
Main Authors He, Yuanfa, Ye, Guanlin, Chi, Shuyan, Tan, Beiping, Dong, Xiaohui, Yang, Qihui, Liu, Hongyu, Zhang, Shuang
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 06.08.2020
Subjects
Animals
Cytotoxicity, Immunologic
Enteritis - immunology
Fish Diseases - immunology
Fishes - physiology
Gene Expression Profiling
Gene Expression Regulation
Gene Regulatory Networks
hybrid grouper
immune response
Immunity - genetics
Immunoglobulin A - biosynthesis
Immunology
inflammation
Integrative Medicine
intestinal health
MicroRNAs - genetics
MicroRNAs - immunology
Phagocytosis
RNA, Messenger - genetics
RNA-seq
Sequence Analysis, RNA
intestinal health
RNA-seq
immune response
inflammation
hybrid grouper
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Abstract A 10-week feeding experiment was conducted to reveal the immune mechanism for soybean meal-induced enteritis (SBMIE) in hybrid grouper, Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂. Four isonitrogenous and isolipidic diets were formulated by replacing 0, 10, 30, and 50% fish meal protein with soybean meal (namely FM, SBM10, SBM30, and SBM50, respectively). The weight gain rate of the SBM50 group was significantly lower than those of the other groups. Plica height, muscular layer thickness, and goblet cells of the distal intestine in the SBM50 group were much lower than those in the FM group. The intestinal transcriptomic data, including the transcriptome and miRNAome, showed that a total of 6,390 differentially expressed genes (DEGs) and 92 DEmiRNAs were identified in the SBM50 and FM groups. DEmiRNAs (10 known and 1 novel miRNAs) and their DE target genes were involved in immune-related phagosome, natural killer cell-mediated cytotoxicity, Fc gamma R-mediated phagocytosis, and the intestinal immune network for IgA production pathways. Our study is the first to offer transcriptomic and small RNA profiling for SBMIE in hybrid grouper. Our findings offer important insights for the understanding of the RNA profile and further elucidation of the underlying molecular immune mechanism for SBMIE in carnivorous fish.
AbstractList A 10-week feeding experiment was conducted to reveal the immune mechanism for soybean meal-induced enteritis (SBMIE) in hybrid grouper, Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂. Four isonitrogenous and isolipidic diets were formulated by replacing 0, 10, 30, and 50% fish meal protein with soybean meal (namely FM, SBM10, SBM30, and SBM50, respectively). The weight gain rate of the SBM50 group was significantly lower than those of the other groups. Plica height, muscular layer thickness, and goblet cells of the distal intestine in the SBM50 group were much lower than those in the FM group. The intestinal transcriptomic data, including the transcriptome and miRNAome, showed that a total of 6,390 differentially expressed genes (DEGs) and 92 DEmiRNAs were identified in the SBM50 and FM groups. DEmiRNAs (10 known and 1 novel miRNAs) and their DE target genes were involved in immune-related phagosome, natural killer cell-mediated cytotoxicity, Fc gamma R-mediated phagocytosis, and the intestinal immune network for IgA production pathways. Our study is the first to offer transcriptomic and small RNA profiling for SBMIE in hybrid grouper. Our findings offer important insights for the understanding of the RNA profile and further elucidation of the underlying molecular immune mechanism for SBMIE in carnivorous fish.
A 10-week feeding experiment was conducted to reveal the immune mechanism for soybean meal-induced enteritis (SBMIE) in hybrid grouper, Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂. Four isonitrogenous and isolipidic diets were formulated by replacing 0, 10, 30, and 50% fish meal protein with soybean meal (namely FM, SBM10, SBM30, and SBM50, respectively). The weight gain rate of the SBM50 group was significantly lower than those of the other groups. Plica height, muscular layer thickness, and goblet cells of the distal intestine in the SBM50 group were much lower than those in the FM group. The intestinal transcriptomic data, including the transcriptome and miRNAome, showed that a total of 6,390 differentially expressed genes (DEGs) and 92 DEmiRNAs were identified in the SBM50 and FM groups. DEmiRNAs (10 known and 1 novel miRNAs) and their DE target genes were involved in immune-related phagosome, natural killer cell-mediated cytotoxicity, Fc gamma R-mediated phagocytosis, and the intestinal immune network for IgA production pathways. Our study is the first to offer transcriptomic and small RNA profiling for SBMIE in hybrid grouper. Our findings offer important insights for the understanding of the RNA profile and further elucidation of the underlying molecular immune mechanism for SBMIE in carnivorous fish.A 10-week feeding experiment was conducted to reveal the immune mechanism for soybean meal-induced enteritis (SBMIE) in hybrid grouper, Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂. Four isonitrogenous and isolipidic diets were formulated by replacing 0, 10, 30, and 50% fish meal protein with soybean meal (namely FM, SBM10, SBM30, and SBM50, respectively). The weight gain rate of the SBM50 group was significantly lower than those of the other groups. Plica height, muscular layer thickness, and goblet cells of the distal intestine in the SBM50 group were much lower than those in the FM group. The intestinal transcriptomic data, including the transcriptome and miRNAome, showed that a total of 6,390 differentially expressed genes (DEGs) and 92 DEmiRNAs were identified in the SBM50 and FM groups. DEmiRNAs (10 known and 1 novel miRNAs) and their DE target genes were involved in immune-related phagosome, natural killer cell-mediated cytotoxicity, Fc gamma R-mediated phagocytosis, and the intestinal immune network for IgA production pathways. Our study is the first to offer transcriptomic and small RNA profiling for SBMIE in hybrid grouper. Our findings offer important insights for the understanding of the RNA profile and further elucidation of the underlying molecular immune mechanism for SBMIE in carnivorous fish.
Author Zhang, Shuang
He, Yuanfa
Yang, Qihui
Ye, Guanlin
Tan, Beiping
Liu, Hongyu
Chi, Shuyan
Dong, Xiaohui
AuthorAffiliation 2 Aquatic Animals Precision Nutrition and High-Efficiency Feed Engineering Research Center of Guangdong Province , Zhanjiang , China
1 Laboratory of Aquatic Animal Nutrition and Feed, Fisheries College, Guangdong Ocean University , Zhanjiang , China
3 Key Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture , Zhanjiang , China
4 Southern Marine Science and Engineering Guangdong Laboratory, Guangdong Ocean University , Zhanjiang , China
AuthorAffiliation_xml – name: 4 Southern Marine Science and Engineering Guangdong Laboratory, Guangdong Ocean University , Zhanjiang , China
– name: 1 Laboratory of Aquatic Animal Nutrition and Feed, Fisheries College, Guangdong Ocean University , Zhanjiang , China
– name: 3 Key Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture , Zhanjiang , China
– name: 2 Aquatic Animals Precision Nutrition and High-Efficiency Feed Engineering Research Center of Guangdong Province , Zhanjiang , China
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Cites_doi 10.1016/j.fsi.2019.10.075
10.1016/j.fsi.2019.10.025
10.1093/nar/gkl243
10.1016/j.fsi.2019.11.002
10.1038/ni.1994
10.1186/s12864-018-5132-9
10.1016/j.fsi.2018.07.038
10.1186/1746-6148-8-101
10.1093/bioinformatics/btp612
10.1093/nar/gkr688
10.1002/JLB.MR0718-269R
10.1016/j.aquaculture.2018.08.021
10.1016/j.ajpath.2019.05.018
10.1038/cr.2008.81
10.1017/S0007114518001022
10.3389/fimmu.2019.00610
10.1111/anu.12375
10.1016/j.cbd.2015.04.001
10.1038/nbt.1883
10.1074/jbc.M109.057141
10.1016/j.fsi.2019.11.072
10.1038/s41598-017-18430-7
10.1186/s12864-016-2473-0
10.1016/j.aqrep.2016.12.005
10.1016/j.dci.2017.02.024
10.1093/bioinformatics/btg034
10.1186/gb-2010-11-10-r106
10.1007/s00424-017-1958-2
10.1016/j.fsi.2017.08.048
10.1016/j.fsi.2014.11.018
10.1016/j.dci.2016.02.019
10.1016/j.fsi.2019.09.034
10.3390/ijms18061161
10.3390/ijms17040566
10.1016/j.fsi.2018.04.004
10.1371/journal.pone.0015224
10.3389/fphys.2018.01154
10.1155/2019/7149296
10.1016/S0044-8486(00)00382-3
10.1016/j.aquaculture.2019.734337
10.1186/gb-2009-10-3-r25
10.1371/journal.pone.0167515
10.2217/fvl-2016-0010
10.1016/j.fsi.2015.08.006
10.1053/j.gastro.2013.07.001
10.1371/journal.pbio.0030264
10.1007/s10126-019-09903-z
10.1021/jf3016943
10.1053/j.gastro.2010.07.040
10.1016/j.fsi.2015.11.011
10.1016/j.fsi.2012.11.031
10.1007/s00109-006-0097-6
10.1016/j.cell.2016.11.040
10.1016/j.fsi.2019.05.030
10.1038/ni0311-195
10.1016/j.fsi.2019.02.064
10.1016/j.fsi.2017.09.042
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Keywords intestinal health
RNA-seq
immune response
inflammation
hybrid grouper
Language English
License Copyright © 2020 He, Ye, Chi, Tan, Dong, Yang, Liu and Zhang.
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This article was submitted to Nutritional Immunology, a section of the journal Frontiers in Immunology
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References Goto (B21) 2011; 12
Refstie (B4) 2000; 190
Grainger (B52) 2017; 469
Liu (B10) 2018; 497
Li (B42) 2018; 19
Liu (B46) 2017; 23
Zhang (B54) 2015; 43
Tan (B11) 2019; 91
Miao (B24) 2017; 18
Prager (B55) 2019; 105
Wu (B27) 2018; 120
Tafalla (B15) 2016; 64
Kortner (B49) 2012; 8
Schefe (B44) 2006; 84
Gao (B23) 2019; 21
Yin (B30) 2018; 81
Anders (B35) 2011; 11
Zhou (B38) 2010; 5
Yang (B58) 2019; 2019
Wang (B9) 2017; 5
Liu (B6) 2019; 88
Martin (B14) 2017; 75
Wu (B3) 2018; 9
Nowarski (B8) 2017; 168
Wu (B5) 2015; 46
Langmead (B36) 2009; 10
John (B41) 2004; 3
Feijoo (B13) 2019; 10
Wulff (B17) 2012; 60
McKenna (B19) 2010; 139
Miao (B45) 2018; 8
Wang (B25) 2019; 98
Pertea (B33) 2003; 19
Zhao (B43) 2016; 17
Koukos (B50) 2013; 145
Gu (B48) 2018; 77
Biton (B20) 2011; 12
Parashar (B57) 2016; 11
Jan (B40) 2006; 34
An (B26) 2019; 96
Krol (B1) 2016; 17
Nguyen (B18) 2010; 285
De (B16) 2015; 15
Hu (B2) 2016; 11
Soroosh (B51) 2019; 189
Qin (B56) 2017; 70
Rasmussen (B39) 2007
Sahlmann (B47) 2013; 34
Wang (B53) 2016; 48
Gu (B7) 2017; 70
Sun (B28) 2019; 98
Wang (B34) 2010; 26
Friedländer (B37) 2012; 40
Grabherr (B32) 2011; 29
Fehrmann-Cartes (B12) 2019; 95
Tan (B29) 2019; 98
Zhang (B31) 2019; 512
Monzo (B22) 2008; 18
References_xml – volume: 95
  start-page: 564
  year: 2019
  ident: B12
  article-title: Anti-inflammatory effects of aloe vera on soy meal-induced intestinal inflammation in zebrafish
  publication-title: Fish ShellFish Immunol.
  doi: 10.1016/j.fsi.2019.10.075
– volume: 98
  start-page: 619
  year: 2019
  ident: B25
  article-title: The effect of partial replacement of fish meal by soy protein concentrate on growth performance, immune responses, gut morphology and intestinal inflammation for juvenile hybrid grouper (Epinephelus fuscoguttatus female symbol x Epinephelus lanceolatus male symbol)
  publication-title: Fish ShellFish Immunol.
  doi: 10.1016/j.fsi.2019.10.025
– volume: 34
  start-page: W451
  year: 2006
  ident: B40
  article-title: RNAhybrid: microRNA target prediction easy, fast and flexible
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkl243
– volume: 98
  start-page: 681
  year: 2019
  ident: B28
  article-title: Effects of dietary Senecio scandens buch-ham extracts on growth performance, plasma biochemical, histology and the expression of immune-related genes in hybrid grouper (Epinephelus lanceolatusmale symbol x Epinephelus fuscoguttatus female symbol)
  publication-title: Fish ShellFish Immunol.
  doi: 10.1016/j.fsi.2019.11.002
– volume: 12
  start-page: 239
  year: 2011
  ident: B20
  article-title: Epithelial microRNAs regulate gut mucosal immunity via epithelium–T cell crosstalk
  publication-title: Nat Immunol.
  doi: 10.1038/ni.1994
– volume: 19
  start-page: 1
  year: 2018
  ident: B42
  article-title: High throughput small RNA and transcriptome sequencing reveal capacitation-related microRNAs and mRNA in boar sperm
  publication-title: BMC Genomics.
  doi: 10.1186/s12864-018-5132-9
– volume: 81
  start-page: 318
  year: 2018
  ident: B30
  article-title: Cottonseed protein concentrate (CPC) suppresses immune function in different intestinal segments of hybrid grouper female symbol Epinephelus fuscoguttatus x male symbol Epinephelus lanceolatu via TLR-2/MyD88 signaling pathways
  publication-title: Fish ShellFish Immunol.
  doi: 10.1016/j.fsi.2018.07.038
– volume: 8
  start-page: 101
  year: 2012
  ident: B49
  article-title: Dietary soyasaponin supplementation to pea protein concentrate reveals nutrigenomic interactions underlying enteropathy in Atlantic salmon (Salmo salar)
  publication-title: BMC Vet Res.
  doi: 10.1186/1746-6148-8-101
– volume: 26
  start-page: 136
  year: 2010
  ident: B34
  article-title: DEGseq: an R package for identifying differentially expressed genes from RNA-seq data
  doi: 10.1093/bioinformatics/btp612
– volume: 40
  start-page: 37
  year: 2012
  ident: B37
  article-title: miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkr688
– volume: 105
  start-page: 1319
  year: 2019
  ident: B55
  article-title: Mechanisms of natural killer cell-mediated cellular cytotoxicity
  publication-title: J Leukocyte Biol.
  doi: 10.1002/JLB.MR0718-269R
– volume: 497
  start-page: 510
  year: 2018
  ident: B10
  article-title: The protective role of glutamine on enteropathy induced by high dose of soybean meal in turbot, Scophthalmus maximus L
  publication-title: Aquaculture.
  doi: 10.1016/j.aquaculture.2018.08.021
– volume: 189
  start-page: 1763
  year: 2019
  ident: B51
  article-title: miR-24 is elevated in ulcerative colitis patients and regulates intestinal epithelial barrier function
  publication-title: Am J Pathol.
  doi: 10.1016/j.ajpath.2019.05.018
– volume: 18
  start-page: 823
  year: 2008
  ident: B22
  article-title: Overlapping expression of microRNAs in human embryonic colon and colorectal cancer
  publication-title: Cell Res.
  doi: 10.1038/cr.2008.81
– volume: 120
  start-page: 269
  year: 2018
  ident: B27
  article-title: Dietary arginine affects growth, gut morphology, oxidation resistance and immunity of hybrid grouper (Epinephelus fuscoguttatus female symbolxEpinephelus lanceolatus male symbol) juveniles
  publication-title: Br J Nutr.
  doi: 10.1017/S0007114518001022
– volume: 10
  start-page: 610
  year: 2019
  ident: B13
  article-title: Soybean meal-induced intestinal inflammation in Zebrafish is T cell-dependent and has a Th17 cytokine profile
  publication-title: Front Immunol.
  doi: 10.3389/fimmu.2019.00610
– volume: 23
  start-page: 129
  year: 2017
  ident: B46
  article-title: Effect of substitution of dietary fish meal by soybean meal on different sizes of gibel carp (Carassius auratus gibelio): digestive enzyme gene expressions and activities, and intestinal and hepatic histology
  publication-title: Aquacult Nutr.
  doi: 10.1111/anu.12375
– volume: 15
  start-page: 1
  year: 2015
  ident: B16
  article-title: Nutrigenomic profiling of transcriptional processes affected in liver and distal intestine in response to a soybean meal-induced nutritional stress in Atlantic salmon (Salmo salar)
  publication-title: Comp Biochem Phys D.
  doi: 10.1016/j.cbd.2015.04.001
– volume: 29
  start-page: 644
  year: 2011
  ident: B32
  article-title: Full-length transcriptome assembly from RNA-Seq data without a reference genome
  publication-title: Nat Biotechnol.
  doi: 10.1038/nbt.1883
– volume: 285
  start-page: 1479
  year: 2010
  ident: B18
  article-title: MicroRNA-7 modulates CD98 expression during intestinal epithelial cell differentiation
  publication-title: J Biol Chem.
  doi: 10.1074/jbc.M109.057141
– volume: 96
  start-page: 86
  year: 2019
  ident: B26
  article-title: Effects of dietary n-3 highly unsaturated fatty acids on growth, non-specific immunity, expression of some immune-related genes and resistance to Vibrio harveyi in hybrid grouper (female symbol Epinephelus fuscoguttatus x male symbol Epinephelus lanceolatu)
  publication-title: Fish ShellFish Immunol.
  doi: 10.1016/j.fsi.2019.11.072
– volume: 8
  start-page: 113
  year: 2018
  ident: B45
  article-title: Dietary soybean meal affects intestinal homoeostasis by altering the microbiota, morphology and inflammatory cytokine gene expression in northern snakehead
  publication-title: Sci Rep.
  doi: 10.1038/s41598-017-18430-7
– volume: 17
  start-page: 156
  year: 2016
  ident: B1
  article-title: Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon
  publication-title: BMC Genomics.
  doi: 10.1186/s12864-016-2473-0
– volume: 5
  start-page: 52
  year: 2017
  ident: B9
  article-title: Effects of substituting fish meal with soybean meal on growth performance and intestinal morphology in orange-spotted grouper (Epinephelus coioides)
  publication-title: Aquacult Rep.
  doi: 10.1016/j.aqrep.2016.12.005
– volume: 75
  start-page: 86
  year: 2017
  ident: B14
  article-title: Nutrigenomics and immune function in fish: new insights from omics technologies
  publication-title: Dev Comp Immunol.
  doi: 10.1016/j.dci.2017.02.024
– volume: 19
  start-page: 651
  year: 2003
  ident: B33
  article-title: TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets
  publication-title: Bioinformatics.
  doi: 10.1093/bioinformatics/btg034
– volume: 11
  start-page: R106
  year: 2011
  ident: B35
  article-title: Differential expression analysis for sequence count data
  publication-title: Genome Biol.
  doi: 10.1186/gb-2010-11-10-r106
– volume: 469
  start-page: 527
  year: 2017
  ident: B52
  article-title: Macrophages in gastrointestinal homeostasis and inflammation
  publication-title: Pflug Arch Eur J Phy.
  doi: 10.1007/s00424-017-1958-2
– volume: 70
  start-page: 95
  year: 2017
  ident: B7
  article-title: Protective effect of glutamine and arginine against soybean meal-induced enteritis in the juvenile turbot (Scophthalmus maximus)
  publication-title: Fish Shellfish Immunol.
  doi: 10.1016/j.fsi.2017.08.048
– volume: 43
  start-page: 209
  year: 2015
  ident: B54
  article-title: Transcriptome analysis revealed changes of multiple genes involved in immunity in Cynoglossus semilaevis during Vibrio anguillarum infection
  publication-title: Fish Shellfish Immunol.
  doi: 10.1016/j.fsi.2014.11.018
– volume: 64
  start-page: 167
  year: 2016
  ident: B15
  article-title: T cell immunity in the teleost digestive tract
  publication-title: Dev Comp Immunol.
  doi: 10.1016/j.dci.2016.02.019
– volume: 98
  start-page: 611
  year: 2019
  ident: B29
  article-title: Dietary Ginkgo biloba leaf extracts supplementation improved immunity and intestinal morphology, antioxidant ability and tight junction proteins mRNA expression of hybrid groupers (Epinephelus lanceolatus male symbol x Epinephelus fuscoguttatus female symbol) fed high lipid diets
  publication-title: Fish ShellFish Immunol.
  doi: 10.1016/j.fsi.2019.09.034
– volume: 18
  start-page: E1161
  year: 2017
  ident: B24
  article-title: Identification of Differentially expressed micrornas associate with glucose metabolism in different organs of blunt snout bream (Megalobrama amblycephala)
  publication-title: Int J Mol Sci.
  doi: 10.3390/ijms18061161
– volume: 17
  start-page: 566
  year: 2016
  ident: B43
  article-title: Profilings of microRNAs in the liver of common carp (Cyprinus carpio) infected with Flavobacterium columnare
  publication-title: Int J Mol Sci.
  doi: 10.3390/ijms17040566
– volume: 77
  start-page: 264
  year: 2018
  ident: B48
  article-title: Soya-saponins induce intestinal inflammation and barrier dysfunction in juvenile turbot (Scophthalmus maximus)
  publication-title: Fish Shellfish Immunol.
  doi: 10.1016/j.fsi.2018.04.004
– volume: 5
  start-page: e15224
  year: 2010
  ident: B38
  article-title: Integrated profiling of microRNAs and mRNAs: microRNAs located on Xq27
  publication-title: PLoS ONE.
  doi: 10.1371/journal.pone.0015224
– volume: 9
  start-page: 1154
  year: 2018
  ident: B3
  article-title: Integrative transcriptomic and microRNAomic profiling reveals immune mechanism for the resilience to soybean meal stress in fish gut and liver
  publication-title: Front Physiol.
  doi: 10.3389/fphys.2018.01154
– volume: 2019
  start-page: 1
  year: 2019
  ident: B58
  article-title: miRNA and mRNA integration network construction reveals novel key regulators in left-sided and right-sided colon adenocarcinoma
  publication-title: BioMed Res Int.
  doi: 10.1155/2019/7149296
– volume: 190
  start-page: 49
  year: 2000
  ident: B4
  article-title: Differing nutritional responses to dietary soybean meal in rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar)
  publication-title: Aquaculture.
  doi: 10.1016/S0044-8486(00)00382-3
– volume: 512
  start-page: 734337
  year: 2019
  ident: B31
  article-title: Identification of potential biomarkers for soybean meal-induced enteritis in juvenile pearl gentian grouper, Epinephelus lanceolatus♂ × Epinephelus fuscoguttatus♀
  publication-title: Aquaculture.
  doi: 10.1016/j.aquaculture.2019.734337
– volume: 10
  start-page: R25
  year: 2009
  ident: B36
  article-title: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome
  publication-title: Genome Biol.
  doi: 10.1186/gb-2009-10-3-r25
– volume: 11
  start-page: e0167515
  year: 2016
  ident: B2
  article-title: Intestinal fluid permeability in Atlantic Salmon (Salmo salar L.) is affected by dietary protein source
  publication-title: PLoS ONE.
  doi: 10.1371/journal.pone.0167515
– volume: 11
  start-page: 321
  year: 2016
  ident: B57
  article-title: RNAi agents as chikungunya virus therapeutics
  publication-title: Future Virol.
  doi: 10.2217/fvl-2016-0010
– volume: 46
  start-page: 765
  year: 2015
  ident: B5
  article-title: Investigating the potential immune role of fish NCAMs: molecular cloning and expression analysis in mandarin fish
  publication-title: Fish Shellfish Immunol.
  doi: 10.1016/j.fsi.2015.08.006
– volume-title: Encyclopedia of Measurement and Statistics
  year: 2007
  ident: B39
– volume: 145
  start-page: 842
  year: 2013
  ident: B50
  article-title: MicroRNA-124 regulates STAT3 expression and is down-regulated in colon tissues of pediatric patients with ulcerative colitis
  publication-title: Gastroenterology.
  doi: 10.1053/j.gastro.2013.07.001
– volume: 3
  start-page: e264
  year: 2004
  ident: B41
  article-title: Correction: human microRNA targets
  publication-title: PLoS Biol.
  doi: 10.1371/journal.pbio.0030264
– volume: 21
  start-page: 550
  year: 2019
  ident: B23
  article-title: Dynamics of miRNA transcriptome in turbot (Scophthalmus maximus L.) intestine following Vibrio anguillarum infection
  publication-title: Mar Biotechnol (NY).
  doi: 10.1007/s10126-019-09903-z
– volume: 60
  start-page: 8457
  year: 2012
  ident: B17
  article-title: Proteome analysis of pyloric ceca: a methodology for fish feed development?
  publication-title: J Agric Food Chem.
  doi: 10.1021/jf3016943
– volume: 139
  start-page: 1654
  year: 2010
  ident: B19
  article-title: MicroRNAs control intestinal epithelial differentiation, architecture, and barrier function
  publication-title: Gastroenterology.
  doi: 10.1053/j.gastro.2010.07.040
– volume: 48
  start-page: 1
  year: 2016
  ident: B53
  article-title: Transcriptome analysis of the Larimichthys crocea liver in response to Cryptocaryon irritans
  publication-title: Fish Shellfish Immunol.
  doi: 10.1016/j.fsi.2015.11.011
– volume: 34
  start-page: 599
  year: 2013
  ident: B47
  article-title: Early response of gene expression in the distal intestine of Atlantic salmon (Salmo salar L.) during the development of soybean meal induced enteritis
  publication-title: Fish Shellfish Immunol.
  doi: 10.1016/j.fsi.2012.11.031
– volume: 84
  start-page: 901
  year: 2006
  ident: B44
  article-title: Quantitative real-time RT-PCR data analysis: current concepts and the novel “gene expression's CT difference” formula
  publication-title: J Mol Med.
  doi: 10.1007/s00109-006-0097-6
– volume: 168
  start-page: 362
  year: 2017
  ident: B8
  article-title: The stromal intervention: regulation of immunity and inflammation at the epithelial-mesenchymal barrier
  publication-title: Cell.
  doi: 10.1016/j.cell.2016.11.040
– volume: 91
  start-page: 130
  year: 2019
  ident: B11
  article-title: Resveratrol attenuates oxidative stress and inflammatory response in turbot fed with soybean meal based diet
  publication-title: Fish Shellfish Immunol.
  doi: 10.1016/j.fsi.2019.05.030
– volume: 12
  start-page: 195
  year: 2011
  ident: B21
  article-title: Epithelial cell microRNAs in gut immunity
  publication-title: Nat Immunol.
  doi: 10.1038/ni0311-195
– volume: 88
  start-page: 65
  year: 2019
  ident: B6
  article-title: Sodium butyrate supplementation in high-soybean meal diets for turbot (Scophthalmus maximus L.): effects on inflammatory status, mucosal barriers and microbiota in the intestine
  publication-title: Fish Shellfish Immunol.
  doi: 10.1016/j.fsi.2019.02.064
– volume: 70
  start-page: 498
  year: 2017
  ident: B56
  article-title: Transcriptome analysis of the spleen of the darkbarbel catfish Pelteobagrus vachellii in response to Aeromonas hydrophila infection
  publication-title: Fish Shellfish Immunol.
  doi: 10.1016/j.fsi.2017.09.042
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Snippet A 10-week feeding experiment was conducted to reveal the immune mechanism for soybean meal-induced enteritis (SBMIE) in hybrid grouper, Epinephelus...
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SubjectTerms Animals
Cytotoxicity, Immunologic
Enteritis - immunology
Fish Diseases - immunology
Fishes - physiology
Gene Expression Profiling
Gene Expression Regulation
Gene Regulatory Networks
hybrid grouper
immune response
Immunity - genetics
Immunoglobulin A - biosynthesis
Immunology
inflammation
Integrative Medicine
intestinal health
MicroRNAs - genetics
MicroRNAs - immunology
Phagocytosis
RNA, Messenger - genetics
RNA-seq
Sequence Analysis, RNA
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Title Integrative Transcriptomic and Small RNA Sequencing Reveals Immune-Related miRNA–mRNA Regulation Network for Soybean Meal-Induced Enteritis in Hybrid Grouper, Epinephelus fuscoguttatus♀ × Epinephelus lanceolatus
URI https://www.ncbi.nlm.nih.gov/pubmed/32903657
https://www.proquest.com/docview/2441603810
https://pubmed.ncbi.nlm.nih.gov/PMC7438716
https://doaj.org/article/4ac66602b3a34e349fdee31caab42642
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