Splenic microRNA expression profiles and integration analyses involved in host responses to Salmonella enteritidis infection in chickens

Li, P.; Fan, W.; Li, Q.; Wang, J.; Liu, R.; Everaert, Nadia; Liu, Jian; Zhang, Y.; Zheng, M.; Cui, H.; Zhao, Guoying; Wen, J.

doi:10.3389/fcimb.2017.00377

Article (Scientific journals)

Splenic microRNA expression profiles and integration analyses involved in host responses to Salmonella enteritidis infection in chickens

Li, P.; Fan, W.; Li, Q. et al.

2017 • In Frontiers in Cellular and Infection Microbiology, 7 (AUG)

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/235273

DOI
10.3389/fcimb.2017.00377

PubMed
28884089

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Keywords :

Chicken; Clinical symptoms; MicroRNA; MiRNA-target genes; Next generation sequencing; Salmonella enteritidis; Spleen; Salmonella enteritidis vaccine; IRF4 protein, Gallus gallus; LRRC59 protein, human; Article; Leghorn chicken; RNA extraction; Salmonella enterica serovar Enteritidis; Adaptive Immunity; Animals; Apoptosis; Avian Proteins; Cell Line; Chickens; Host-Pathogen Interactions; Humans; Interferon Regulatory Factors; Membrane Proteins; MicroRNAs; NLR Proteins; Poultry Diseases; RNA, Messenger; Salmonella Infections, Animal; Transcriptome

Abstract :

[en] To understand the role of miRNAs in regulating genes involved in the host response to Salmonella enteritidis (SE) infection, next generation sequencing was applied to explore the altered splenic expression of microRNAs (miRNAs) and deregulated genes in specific-pathogen-free chickens. Birds were either infected or not (controls, C) and those challenged with SE were evaluated 24 h later and separated into two groups on the basis of the severity of clinical symptoms and blood load of SE: resistant (R, SE challenged-slight clinical symptoms and <10 5 cfu / 10 μL), and susceptible (S, SE challenged-severe clinical symptoms and >10 7 cfu/10 μL). Thirty-two differentially expressed (DE) miRNAs were identified in spleen, including 16 miRNAs between S and C, 13 between R and C, and 13 between S and R. Through integration analysis of DE miRNAs and mRNA, a total of 273 miRNA-target genes were identified. Functional annotation analysis showed that Apoptosis and NOD-like receptor signaling pathway and adaptive immune response were significantly enriched (P < 0.05). Interestingly, apoptosis pathway was significantly enriched in S vs. C, while NOD-like receptor pathway was enriched in R vs. C (P < 0.05). Two miRNAs, gga-miR-101-3p and gga-miR-155, in the hub positions of the miRNA-mRNA regulatory network, were identified as candidates potentially associated with SE infection. These 2 miRNAs directly repressed luciferase reporter gene activity via binding to 3'-untranslated regions of immune-related genes IRF4 and LRRC59; over-expressed gga-miR-155 and interference gga-miR-101-3p in chicken HD11 macrophage cells significantly altered expression of their target genes and decreased the production of pro-inflammatory cytokines. These findings facilitate better understanding of the mechanisms of host resistance and susceptibility to SE infection in chickens. © 2017 Li, Fan, Li, Wang, Liu, Everaert, Liu, Zhang, Zheng, Cui, Zhao and Wen.

Disciplines :

Animal production & animal husbandry

Author, co-author :

Li, P.; Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China, Precision Livestock and Nutrition Unit, Gembloux Agro-Bio Tech, University of Liège, Gembloux, Belgium, State Key Laboratory of Animal Nutrition, Beijing, China

Fan, W.; Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China

Li, Q.; Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China

Wang, J.; Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China, State Key Laboratory of Animal Nutrition, Beijing, China

Liu, R.; Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China

Everaert, Nadia ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Ingénierie des productions animales et nutrition

Liu, Jian

Zhang, Y.; College of Animal Science, Jilin University, Changchun, China

Zheng, M.; Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China

Cui, H.; Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China

Zhao, Guoying ; Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, C

Wen, J.; Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China, State Key Laboratory of Animal Nutrition, Beijing, China

Language :

English

Title :

Splenic microRNA expression profiles and integration analyses involved in host responses to Salmonella enteritidis infection in chickens

Publication date :

2017

Journal title :

Frontiers in Cellular and Infection Microbiology

eISSN :

2235-2988

Publisher :

Frontiers Media S.A.

Volume :

Issue :

AUG

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 08 May 2019

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Bibliography

Ambros, V. (2004). The functions of animal microRNAs. Nature 431, 350-355. doi: 10.1038/nature02871
Bao, H., Kommadath, A., Liang, G., Sun, X., Arantes, A. S., Tuggle, C. K., et al. (2015). Genome-wide whole blood microRNAome and transcriptome analyses reveal miRNA-mRNA regulated host response to foodborne pathogen Salmonella infection in swine. Sci. Rep. 5:12620. doi: 10.1038/srep12620
Bao, H., Kommadath, A., Plastow, G. S., Tuggle, C. K., Guan, L. L., and Stothard, P. (2014). MicroRNA Buffering and altered variance of gene expression in response to Salmonella infection. PLoS ONE 9:e94352. doi: 10.1371/journal.pone.0094352
Barrow, P. A., Jones, M. A., Smith, A. L., and Wigley, P. (2012). The long view: Salmonella - the last forty years. Avian Pathol. 41, 413-420. doi: 10.1080/03079457.2012.718071
BIG Data Center Members (2017). The BIG Data Center: from deposition to integration to translation. Nucleic Acids Res. 45, D18-D24. doi: 10.1093/nar/gkw1060
Calenge, F., and Beaumont, C. (2012). Toward integrative genomics study of genetic resistance to Salmonella and Campylobacter intestinal colonization in fowl. Front. Genet. 3:261. doi: 10.3389/fgene.2012.00261
Calenge, F., Kaiser, P., Vignal, A., and Beaumont, C. (2010). Genetic control of resistance to salmonellosis and to Salmonella carrier-state in fowl: a review. Genet. Sel. Evol. 42:11. doi: 10.1186/1297-9686-42-11
Das, K., Garnica, O., and Dhandayuthapani, S. (2016). Modulation of Host miRNAs by Intracellular Bacterial Pathogens. Front. Cell. Infect. Microbiol. 6:79. doi: 10.3389/fcimb.2016.00079
Deng, S. X., Cheng, A. C., Wang, M. S., and Cao, P. (2008). Serovar-specific real-time quantitative detection of Salmonella enteritidis in the gastrointestinal tract of ducks after oral challenge. Avian Dis. 52, 88-93. doi: 10.1637/8102-090107-Reg
DuPont, H. L., and Steele, J. H. (1987). The human health implication of the use of antimicrobial agents in animal feeds. Vet. Q. 9, 309-320. doi: 10.1080/01652176.1987.9694119
EFSA and ECDC. (European Food Safety Authority and European Centre for Disease Prevention and Control) (2016). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2015. EFSA J. 14, 4634-4634. doi: 10.2903/j.efsa.2016.4634
Elton, T. S., Selemon, H., Elton, S. M., and Parinandi, N. L. (2013). Regulation of the MIR155 host gene in physiological and pathological processes. Gene 532, 1-12. doi: 10.1016/j.gene.2012.12.009
Eulalio, A., Schulte, L. N., and Vogel, J. (2012). The mammalian microRNA response to bacterial infections. RNA Biol. 9, 742-750. doi: 10.4161/rna.20018
Filipowicz, W., Bhattacharyya, S. N., and Sonenberg, N. (2008). Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet. 9, 102-114. doi: 10.1038/nrg2290
Goldman, E. (2004). Antibiotic abuse in animal agriculture: exacerbating drug resistance in human pathogens. Hum. Ecol. Risk Assess. 10, 121-134. doi: 10.1080/10807030490281016
Gou, Z., Liu, R., Zhao, G., Zheng, M., Li, P., Wang, H., et al. (2012). Epigenetic modification of TLRs in Leukocytes is associated with increased susceptibility to Salmonella enteritidis in chickens. PLoS ONE 7:e33627. doi: 10.1371/journal.pone.0033627
He, X., and Zhang, J. (2006). Why do hubs tend to be essential in protein networks? PLoS Genet. 2, 826-834. doi: 10.1371/journal.pgen.0020088
Honma, K., Udono, H., Kohno, T., Yamamoto, K., Ogawa, A., Takemori, T., et al. (2005). Interferon regulatory factor 4 negatively regulates the production of proinflammatory cytokines by macrophages in response to LPS. Proc. Natl. Acad. Sci. U.S.A. 102, 16001-16006. doi: 10.1073/pnas.0504226102
Huang, D. W., Sherman, B. T., and Lempicki, R. A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57. doi: 10.1038/nprot.2008.211
Huang, H. Y., Liu, R. R., Zhao, G. P., Li, Q. H., Zheng, M. Q., Zhang, J. J., et al. (2015). Integrated analysis of microRNA and mRNA expression profiles in abdominal adipose tissues in chickens. Sci. Rep. 5, 16132-16132. doi: 10.1038/srep16132
Inns, T., Lane, C., Peters, T., Dallman, T., Chatt, C., McFarland, N., et al. (2015). A multi-country Salmonella enteritidis phage type 14b outbreak associated with eggs from a German producer: 'near real-time' application of whole genome sequencing and food chain investigations, United Kingdom, May to September 2014. Eurosurveillance 20, 15-22. doi: 10.2807/1560-7917.ES2015.20.16.21098
Jia, X., Nie, Q., Zhang, X., Nolan, L. K., and Lamont, S. J. (2017). Novel microRNA involved in host response to avian pathogenic Escherichia coli identified by deep sequencing and integration analysis. Infect. Immun. 85:e00688-16. doi: 10.1128/iai.00688-16
Kawai, T., and Akira, S. (2011). Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637-650. doi: 10.1016/j.immuni.2011.05.006
Keestra, A. M., de Zoete, M. R., Bouwman, L. I., Vaezirad, M. M., and van Putten, J. P. M. (2013). Unique features of chicken Toll-like receptors. Dev. Comp. Immunol. 41, 316-323. doi: 10.1016/j.dci.2013.04.009
Kozomara, A., and Griffiths-Jones, S. (2014). miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 42, D68-D73. doi: 10.1093/nar/gkt1181
Krol, J., Loedige, I., and Filipowicz, W. (2010). The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 11, 597-610. doi: 10.1038/nrg2843
Kuang, X., Hao, H., Dai, M., Wang, Y., Ahmad, I., Liu, Z., et al. (2015). Serotypes and antimicrobial susceptibility of Salmonella spp. isolated from farm animals in China. Front. Microbiol. 6:602. doi: 10.3389/fmicb.2015.00602
Li, P., Xia, P., Wen, J., Zheng, M., Chen, J., Zhao, J., et al. (2010). Up-regulation of the MyD88-dependent pathway of TLR signaling in spleen and caecum of young chickens infected with Salmonella serovar Pullorum. Vet. Microbiol. 143, 346-351. doi: 10.1016/j.vetmic.2009.12.008
Li, X., Shahid, M. Q., Wu, J., Wang, L., Liu, X., and Lu, Y. (2016). Comparative small RNA analysis of pollen development in autotetraploid and diploid rice. Int. J. Mol. Sci. 17:499. doi: 10.3390/IJMS17040499
Li, Y., and Shi, X. (2013). MicroRNAs in the regulation of TLR and RIG-I pathways. Cell. Mol. Immunol. 10, 65-71. doi: 10.1038/cmi.2012.55
Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
Maudet, C., Mano, M., and Eulalio, A. (2014). MicroRNAs in the interaction between host and bacterial pathogens. FEBS Lett. 588, 4140-4147. doi: 10.1016/j.febslet.2014.08.002
Murie, C., Barette, C., Lafanechere, L., and Nadon, R. (2014). Control-Plate Regression (CPR) Normalization for high-throughput screens with many active features. J. Biomol. Screen. 19, 661-671. doi: 10.1177/1087057113516003
Negishi, H., Ohba, Y., Yanai, H., Takaoka, A., Honma, K., Yui, K., et al. (2005). Negative regulation of Toll-like-receptor signaling by IRF-4. Proc. Natl. Acad. Sci. U.S.A. 102, 15989-15994. doi: 10.1073/pnas.0508327102
Olivieri, F., Rippo, M. R., Prattichizzo, F., Babini, L., Graciotti, L., Recchioni, R., et al. (2013). Toll like receptor signaling in "inflammaging": microRNA as new players. Immun. Ageing 10:11. doi: 10.1186/1742-4933-10-11
O'Neill, L. A., Sheedy, F. J., and McCoy, C. E. (2011). MicroRNAs: the fine-tuners of Toll-like receptor signalling. Nat. Rev. Immunol. 11, 163-175. doi: 10.1038/nri2957
Pallai, R., Bhaskar, A., Barnett-Bernodat, N., Gallo-Ebert, C., Pusey, M., Nickels, J. T. Jr., et al. (2015). Leucine-rich repeat-containing protein 59 mediates nuclear import of cancerous inhibitor of PP2A in prostate cancer cells. Tumor Biol. 36, 6383-6390. doi: 10.1007/s13277-015-3326-1
Quinn, S. R., and O'Neill, L. A. (2011). A trio of microRNAs that control Toll-like receptor signalling. Int. Immunol. 23, 421-425. doi: 10.1093/intimm/dxr034
Schulte, L. N., Eulalio, A., Mollenkopf, H.-J., Reinhardt, R., and Vogel, J. (2011). Analysis of the host microRNA response to Salmonella uncovers the control of major cytokines by the let-7 family. EMBO J. 30, 1977-1989. doi: 10.1038/emboj.2011.94
Skjerpen, C. S., Wesche, J., and Olsnes, S. (2002). Identification of ribosome-binding protein p34 as an intracellular protein that binds acidic fibroblast growth factor. J. Biol. Chem. 277, 23864-23871. doi: 10.1074/jbc.M112193200
Smith, K. G., and Hunt, J. L. (2004). On the use of spleen mass as a measure of avian immune system strength. Oecologia 138, 28-31. doi: 10.1007/s00442-003-1409-y
Sonkoly, E., Stahle, M., and Pivarcsi, A. (2008). MicroRNAs and immunity: novel players in the regulation of normal immune function and inflammation. Semin. Cancer Biol. 18, 131-140. doi: 10.1016/j.semcancer.2008.01.005
Staedel, C., and Darfeuille, F. (2013). MicroRNAs and bacterial infection. Cell. Microbiol. 15, 1496-1507. doi: 10.1111/cmi.12159
Tatematsu, M., Funami, K., Ishii, N., Seya, T., Obuse, C., and Matsumoto, M. (2015). LRRC59 regulates trafficking of nucleic acid-sensing TLRs from the endoplasmic reticulum via association with UNC93B1. J. Immunol. 195, 4933-4942. doi: 10.4049/jimmunol.1501305
Tiron, A., and Vasilescu, C. (2008). Spleen and immunity. Immune implications of splenectomy. Chirurgia (Bucur) 103, 255-263.
Trapnell, C., Pachter, L., and Salzberg, S. L. (2009). TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111. doi: 10.1093/bioinformatics/btp120
Trapnell, C., Williams, B. A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M. J., et al. (2010). Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, U511-U174. doi: 10.1038/nbt.1621
Wang, Y., Song, F., Zhu, J., Zhang, S., Yang, Y., Chen, T., et al. (2017). GSA: GENOME Sequence Archive. Genomics Proteomics Bioinform. 15, 14-18. doi: 10.1016/j.gpb.2017.01.001
Wu, G., Qi, Y., Liu, X., Yang, N., Xu, G., Liu, L., et al. (2017). Cecal microRNAome response to Salmonella enterica serovar enteritidis infection in white Leghorn Layer. BMC Genomics 18:77. doi: 10.1186/s12864-016-3413-8
Yao, M., Gao, W., Tao, H., Yang, J., Liu, G., and Huang, T. (2016a). Regulation signature of miR-143 and miR-26 in porcine Salmonella infection identified by binding site enrichment analysis. Mol. Genet. Genomics 291, 789-799. doi: 10.1007/s00438-015-1146-z
Yao, M., Gao, W., Yang, J., Liang, X., Luo, J., and Huang, T. (2016b). The regulation roles of miR-125b, miR-221 and miR-27b in porcine Salmonella infection signalling pathway. Biosci. Rep. 36:e00375. doi: 10.1042/bsr20160243
Yates, L. A., Norbury, C. J., and Gilbert, R. J. C. (2013). The long and short of MicroRNA. Cell 153, 516-519. doi: 10.1016/j.cell.2013.04.003
Ye, B., Wang, R., and Wang, J. (2016). Correlation analysis of the mRNA and miRNA expression profiles in the nascent synthetic allotetraploid Raphanobrassica. Sci. Rep. 6:37416. doi: 10.1038/srep37416