Gene expression networks and functionally enriched pathways involved in the response of domestic chicken to acute heat stress

Heat stress in poultry houses, especially in warm areas, is one of the main environmental factors that restrict the growth of broilers or laying performance of layers, suppresses the immune system, and deteriorates egg quality and feed conversion ratio. The molecular mechanisms underlying the response of chicken to acute heat stress (AHS) have not been comprehensively elucidated. Therefore, the main object of the current work was to investigate the liver gene expression profile of chickens under AHS in comparison with their corresponding control groups, using four RNA-seq datasets. The meta-analysis, GO and KEGG pathway enrichment, WGCNA, machine-learning, and eGWAS analyses were performed. The results revealed 77 meta-genes that were mainly related to protein biosynthesis, protein folding, and protein transport between cellular organelles. In other words, under AHS, the expression of genes involving in the structure of rough reticulum membrane and in the process of protein folding was adversely influenced. In addition, genes related to biological processes such as “response to unfolded proteins,” “response to reticulum stress” and “ERAD pathway” were differentially regulated. We introduce here a couple of genes such as HSPA5, SSR1, SDF2L1, and SEC23B, as the most significantly differentiated under AHS, which could be used as bio-signatures of AHS. Besides the mentioned genes, the main findings of the current work may shed light to the identification of the effects of AHS on gene expression profiling of domestic chicken as well as the adaptive response of chicken to environmental stresses.

[1]  S. Dridi,et al.  A review of heat stress in chickens. Part I: Insights into physiology and gut health , 2022, Frontiers in Physiology.

[2]  M. Mazzoni,et al.  Effect of chronic heat stress on gastrointestinal histology and expression of feed intake-regulatory hormones in broiler chickens. , 2022, Animal : an international journal of animal bioscience.

[3]  K. Aonuma,et al.  Identification of potential dilated cardiomyopathy-related targets by meta-analysis and co-expression analysis of human RNA-sequencing datasets. , 2022, Life sciences.

[4]  Lili Zhang,et al.  SERP1 reduces inchoate acute hepatic injury through regulation of endoplasmic reticulum stress via the GSK3β/β-catenin/TCF/LEF signaling pathway , 2022, Molecular medicine reports.

[5]  Min Wang,et al.  Clinical role of serum histone deacetylase 4 measurement in acute ischemic stroke: Relation to disease risk, severity, and prognosis , 2022, Journal of clinical laboratory analysis.

[6]  Mamadou Thiam,et al.  Liver Transcriptome Response to Heat Stress in Beijing You Chickens and Guang Ming Broilers , 2022, Genes.

[7]  Ye Tian,et al.  FYN and CD247: key Genes for Septic Shock Based on Bioinformatics and Meta-Analysis. , 2021, Combinatorial chemistry & high throughput screening.

[8]  Hyeran Kim,et al.  Transcriptomic Response under Heat Stress in Chickens Revealed the Regulation of Genes and Alteration of Metabolism to Maintain Homeostasis , 2021, Animals : an open access journal from MDPI.

[9]  M. Rothschild,et al.  Transcriptome Response of Liver and Muscle in Heat-Stressed Laying Hens , 2021, Genes.

[10]  S. Lamont,et al.  Liver Transcriptome Responses to Heat Stress and Newcastle Disease Virus Infection in Genetically Distinct Chicken Inbred Lines , 2020, Genes.

[11]  Shuhong Zhao,et al.  rMVP: A Memory-efficient, Visualization-enhanced, and Parallel-accelerated Tool for Genome-wide Association Study , 2020, bioRxiv.

[12]  A. Burlingame,et al.  An ER translocon for multi-pass membrane protein biogenesis , 2020, eLife.

[13]  L. Radwan,et al.  Genetic improvement of egg laying traits in Fayoumi chickens bred under conditions of heat stress through selection and gene expression studies. , 2020, Journal of thermal biology.

[14]  Ian H. Guldner,et al.  Cell surface GRP78 promotes stemness in normal and neoplastic cells , 2020, Scientific Reports.

[15]  C. Schwarzinger,et al.  Ginseng Extract Ameliorates the Negative Physiological Effects of Heat Stress by Supporting Heat Shock Response and Improving Intestinal Barrier Integrity: Evidence from Studies with Heat-Stressed Caco-2 Cells, C. elegans and Growing Broilers , 2020, Molecules.

[16]  H. Freetly,et al.  Genes associated with body weight gain and feed intake identified by meta-analysis of the mesenteric fat from crossbred beef steers , 2020, PloS one.

[17]  M. Rothschild,et al.  Effects of acute and chronic heat stress on the performance, egg quality, body temperature, and blood gas parameters of laying hens , 2019, Poultry science.

[18]  I. Wada,et al.  SDF2-like protein 1 (SDF2L1) regulates the endoplasmic reticulum localization and chaperone activity of ERdj3 protein , 2019, The Journal of Biological Chemistry.

[19]  M. T. te Pas,et al.  Cardiac and Skeletal Muscle Transcriptome Response to Heat Stress in Kenyan Chicken Ecotypes Adapted to Low and High Altitudes Reveal Differences in Thermal Tolerance and Stress Response , 2019, Front. Genet..

[20]  Q. Nie,et al.  The Low Expression of DUSP1 and HSPA5 Inhibits Chicken Immune Response and Causes Decreased Immunity under Heat Stress , 2019 .

[21]  Steven L Salzberg,et al.  Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype , 2019, Nature Biotechnology.

[22]  I. Zulkifli,et al.  Effects of heat stress on growth performance, selected physiological and immunological parameters, caecal microflora, and meat quality in two broiler strains , 2019, Asian-Australasian journal of animal sciences.

[23]  J. Armengaud,et al.  Co-expression network analysis identifies gonad- and embryo-associated protein modules in the sentinel species Gammarus fossarum , 2019, Scientific Reports.

[24]  F. Martinelli,et al.  Identification of key genes and its chromosome regions linked to drought responses in leaves across different crops through meta-analysis of RNA-Seq data , 2019, BMC Plant Biology.

[25]  Chao-Jung Chen,et al.  Acute Heat Stress Changes Protein Expression in the Testes of a Broiler-Type Strain of Taiwan Country Chickens , 2019, Animal biotechnology.

[26]  L. Radwan,et al.  Genetic selection for growth performance and thermal tolerance under high ambient temperature after two generations using heat shock protein 90 expression as an index , 2019, Animal Production Science.

[27]  M. T. te Pas,et al.  Comparative transcriptome analysis of Ethiopian indigenous chickens from low and high altitudes under heat stress condition reveals differential immune response , 2018, Animal genetics.

[28]  M. Sirard,et al.  Follicle capacitation: a meta-analysis to investigate the transcriptome dynamics following follicle-stimulating hormone decline in bovine granulosa cells† , 2018, Biology of Reproduction.

[29]  J. Keele,et al.  RNA-Seq Meta-analysis identifies genes in skeletal muscle associated with gain and intake across a multi-season study of crossbred beef steers , 2018, BMC Genomics.

[30]  S. High,et al.  Chaperone-Mediated Sec61 Channel Gating during ER Import of Small Precursor Proteins Overcomes Sec61 Inhibitor-Reinforced Energy Barrier , 2018, Cell reports.

[31]  A. Schäffer,et al.  Plasma cell deficiency in human subjects with heterozygous mutations in Sec61 translocon alpha 1 subunit (SEC61A1) , 2017, The Journal of allergy and clinical immunology.

[32]  E. Ebrahimie,et al.  Transcriptome signature of the lactation process, identified by meta-analysis of microarray and RNA-Seq data , 2018 .

[33]  Chao-Jung Chen,et al.  Functional genomics study of acute heat stress response in the small yellow follicles of layer-type chickens , 2018, Scientific Reports.

[34]  K. Wimmers,et al.  Integrative approach using liver and duodenum RNA-Seq data identifies candidate genes and pathways associated with feed efficiency in pigs , 2018, Scientific Reports.

[35]  P. Ping,et al.  HSPA5 Gene encoding Hsp70 chaperone BiP in the endoplasmic reticulum. , 2017, Gene.

[36]  I. Misztal.  BREEDING AND GENETICS SYMPOSIUM: Resilience and lessons from studies in genetics of heat stress. , 2017, Journal of animal science.

[37]  M. Rothschild,et al.  Genomic Comparison of Indigenous African and Northern European Chickens Reveals Putative Mechanisms of Stress Tolerance Related to Environmental Selection Pressure , 2017, G3: Genes, Genomes, Genetics.

[38]  A. Vickers,et al.  Liver Effects of Clinical Drugs Differentiated in Human Liver Slices , 2017, International journal of molecular sciences.

[39]  S. Lamont,et al.  Liver transcriptome response to hyperthermic stress in three distinct chicken lines , 2016, BMC Genomics.

[40]  H. Khosravinia.  Mortality, production performance, water intake and organ weight of the heat stressed broiler chicken given savory (Satureja khuzistanica) essential oils through drinking water , 2016 .

[41]  M. Rothschild,et al.  Identification of quantitative trait loci for body temperature, body weight, breast yield, and digestibility in an advanced intercross line of chickens under heat stress , 2015, Genetics Selection Evolution.

[42]  Jingjing Xie,et al.  Effects of acute and chronic heat stress on plasma metabolites, hormones and oxidant status in restrictedly fed broiler breeders. , 2015, Poultry science.

[43]  San-Yuan Huang,et al.  Acute Heat Stress Induces Differential Gene Expressions in the Testes of a Broiler-Type Strain of Taiwan Country Chickens , 2015, PloS one.

[44]  Jiangxia Zheng,et al.  Transcriptome responses to heat stress in hypothalamus of a meat-type chicken , 2015, Journal of Animal Science and Biotechnology.

[45]  M. Rothschild,et al.  RNA-seq: primary cells, cell lines and heat stress , 2015, bioRxiv.

[46]  M. Goddard,et al.  The Genetic Architecture of Climatic Adaptation of Tropical Cattle , 2014, PloS one.

[47]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[48]  Paul Theodor Pyl,et al.  HTSeq—a Python framework to work with high-throughput sequencing data , 2014, bioRxiv.

[49]  Chao-Jung Chen,et al.  Changes in protein expression in testes of L2 strain Taiwan country chickens in response to acute heat stress. , 2014, Theriogenology.

[50]  A. Lawrence,et al.  Selection for 'environmentaI fit' from existing domesticated species. , 2014, Revue scientifique et technique.

[51]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[52]  P. Prunet,et al.  Transcriptional Assessment by Microarray Analysis and Large-Scale Meta-analysis of the Metabolic Capacity of Cardiac and Skeletal Muscle Tissues to Cope With Reduced Nutrient Availability in Gilthead Sea Bream (Sparus aurata L.) , 2014, Marine Biotechnology.

[53]  L. Rui,et al.  Energy metabolism in the liver. , 2014, Comprehensive Physiology.

[54]  M. Rothschild,et al.  RNA-seq analysis of broiler liver transcriptome reveals novel responses to high ambient temperature , 2014, BMC Genomics.

[55]  C. Berri,et al.  Thermal manipulation of the embryo modifies the physiology and body composition of broiler chickens reared in floor pens without affecting breast meat processing quality. , 2013, Journal of animal science.

[56]  Andrea Rau,et al.  Differential meta-analysis of RNA-seq data from multiple studies , 2013, BMC Bioinformatics.

[57]  L. A. Mack,et al.  Genetic variations alter production and behavioral responses following heat stress in 2 strains of laying hens. , 2013, Poultry science.

[58]  Teresa M. Przytycka,et al.  Chapter 5: Network Biology Approach to Complex Diseases , 2012, PLoS Comput. Biol..

[59]  M. Amaral,et al.  Regulation of ENaC biogenesis by the stress response protein SERP1 , 2012, Pflügers Archiv - European Journal of Physiology.

[60]  J. Tong,et al.  The probiotic Bacillus licheniformis ameliorates heat stress-induced impairment of egg production, gut morphology, and intestinal mucosal immunity in laying hens. , 2012, Poultry science.

[61]  G. Tseng,et al.  Comprehensive literature review and statistical considerations for microarray meta-analysis , 2012, Nucleic acids research.

[62]  Deborah J. Andrew,et al.  The CrebA/Creb3-like transcription factors are major and direct regulators of secretory capacity , 2010, The Journal of cell biology.

[63]  Shinichi Kondo,et al.  Regulation of endoplasmic reticulum stress response by a BBF2H7-mediated Sec23a pathway is essential for chondrogenesis , 2009, Nature Cell Biology.

[64]  M. Selsted,et al.  SDF2L1, a Component of the Endoplasmic Reticulum Chaperone Complex, Differentially Interacts with α-, β-, and θ-Defensin Propeptides* , 2009, Journal of Biological Chemistry.

[65]  Pornpimol Charoentong,et al.  ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks , 2009, Bioinform..

[66]  Steve Horvath,et al.  WGCNA: an R package for weighted correlation network analysis , 2008, BMC Bioinformatics.

[67]  Randy Schekman,et al.  Coordination of COPII vesicle trafficking by Sec23. , 2008, Trends in cell biology.

[68]  M. Toyomizu,et al.  Mitochondrial Oxidative Damage in Chicken Skeletal Muscle Induced by Acute Heat Stress , 2007 .

[69]  Manuel A. R. Ferreira,et al.  PLINK: a tool set for whole-genome association and population-based linkage analyses. , 2007, American journal of human genetics.

[70]  J. Buyse,et al.  Acute heat stress induces oxidative stress in broiler chickens. , 2006, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[71]  S. Horvath,et al.  Statistical Applications in Genetics and Molecular Biology , 2011 .

[72]  Amy S. Lee.  The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. , 2005, Methods.

[73]  H. Ploegh,et al.  A membrane protein required for dislocation of misfolded proteins from the ER , 2004, Nature.

[74]  W. Nastainczyk,et al.  Characterization of pancreatic ERj3p, ahomolog of yeast DnaJ-like protein Scj1p , 2004, Biological chemistry.

[75]  E. Koonin,et al.  Regeneration of Peroxiredoxins by p53-Regulated Sestrins, Homologs of Bacterial AhpD , 2004, Science.

[76]  F. Edens,et al.  Influence of selenium sources on age-related and mild heat stress-related changes of blood and liver glutathione redox cycle in broiler chickens (Gallus domesticus). , 2003, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[77]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[78]  G. B. Havenstein,et al.  Growth, livability, and feed conversion of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. , 2003, Poultry science.

[79]  Ö. Altan,et al.  Effect of heat stress on oxidative stress, lipid peroxidation and some stress parameters in broilers , 2003, British poultry science.

[80]  X. Puente,et al.  Human and mouse proteases: a comparative genomic approach , 2003, Nature Reviews Genetics.

[81]  Gary D. Schnitkey,et al.  ECONOMIC LOSSES FROM HEAT STRESS BY US LIVESTOCK INDUSTRIES , 2003 .

[82]  S. High,et al.  Different transmembrane domains associate with distinct endoplasmic reticulum components during membrane integration of a polytopic protein. , 2002, Molecular biology of the cell.

[83]  L. Hendershot,et al.  A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. , 2002, Molecular biology of the cell.

[84]  A. Chajut,et al.  Identification of a novel stress-responsive gene Hi95 involved in regulation of cell viability , 2002, Oncogene.

[85]  S. Burley,et al.  Universal conservation in translation initiation revealed by human and archaeal homologs of bacterial translation initiation factor IF2. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[86]  Leonard Buckbinder,et al.  PA26, a novel target of the p53 tumor suppressor and member of the GADD family of DNA damage and growth arrest inducible genes , 1999, Oncogene.