Genome-wide whole blood microRNAome and transcriptome analyses reveal miRNA-mRNA regulated host response to foodborne pathogen Salmonella infection in swine

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Bao, Hua ^a   Kommadath, Arun ^a   Liang, Guanxiang ^a   Sun, Xu ^a   Arantes, Adriano S ^a   Tuggle, Christopher K ^b   Bearson, Shawn M D ^c   Plastow, Graham S ^a   Stothard, Paul ^a   Guan, Le Luo ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b IOWA STATE UNIVERSITY   (United States)

^c NATIONAL ANIMAL DISEASE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATION TRANSPORT PROTEIN; MESSENGER RNA; MICRORNA; NATURAL RESISTANCE-ASSOCIATED MACROPHAGE PROTEIN 1;

ANIMAL; ANIMAL SALMONELLOSIS; BLOOD; FOOD POISONING; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MICROBIOLOGY; PIG; REPRODUCIBILITY;

ANIMALS; CATION TRANSPORT PROTEINS; FOODBORNE DISEASES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME-WIDE ASSOCIATION STUDY; HOST-PATHOGEN INTERACTIONS; MICRORNAS; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; SALMONELLA INFECTIONS, ANIMAL; SUS SCROFA;

EID: 84938299328     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep12620     Document Type: Article

References (59)

1. Herikstad, H., Motarjemi, Y. & Tauxe, R. V. Salmonella surveillance: a global survey of public health serotyping. Epidemiology and infection 129, 1-8 (2002).
2. Hohmann, E. L. Nontyphoidal salmonellosis. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America 32, 263-269, doi: 10.1086/318457 (2001).
3. Korsak, N. et al. Salmonella contamination of pigs and pork in an integrated pig production system. Journal of food protection 66, 1126-1133 (2003).
4. Boyen, F. et al. Non-typhoidal Salmonella infections in pigs: a closer look at epidemiology, pathogenesis and control. Veterinary microbiology 130, 1-19, doi: 10.1016/j.vetmic.2007.12.017 (2008).
5. He, L. & Hannon, G. J. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5, 522-531, doi: 10.1038/nrg1379 (2004).
6. Filipowicz, W., Bhattacharyya, S. N. & Sonenberg, N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9, 102-114, doi: 10.1038/nrg2290 (2008).
7. Bao, H. et al. Expansion of ruminant-specific microRNAs shapes target gene expression divergence between ruminant and nonruminant species. BMC genomics 14, 609, doi: 10.1186/1471-2164-14-609 (2013).
8. Ambros, V. The functions of animal microRNAs. Nature 431, 350-355, doi: 10.1038/nature02871 (2004).
9. Kloosterman, W. P. & Plasterk, R. H. The diverse functions of microRNAs in animal development and disease. Developmental cell 11, 441-450, doi: 10.1016/j.devcel.2006.09.009 (2006).
10. Bao, H. et al. MicroRNA buffering and altered variance of gene expression in response to Salmonella infection. PloS one 9, e94352, doi: 10.1371/journal.pone.0094352 (2014).
11. Eulalio, A., Schulte, L. & Vogel, J. The mammalian microRNA response to bacterial infections. RNA biology 9, 742-750, doi: 10.4161/rna.20018 (2012).
12. Staedel, C. & Darfeuille, F. MicroRNAs and bacterial infection. Cellular microbiology 15, 1496-1507, doi: 10.1111/cmi.12159 (2013).
13. Lindsay, M. A. microRNAs and the immune response. Trends in immunology 29, 343-351, doi: 10.1016/j.it.2008.04.004 (2008).
14. Ma, F. et al. The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-gamma. Nature immunology 12, 861-869, doi: 10.1038/ni.2073 (2011).
15. Schulte, L. N., Eulalio, A., Mollenkopf, H. J., Reinhardt, R. & Vogel, J. Analysis of the host microRNA response to Salmonella uncovers the control of major cytokines by the let-7 family. The EMBO journal 30, 1977-1989, doi: 10.1038/emboj.2011.94 (2011).
16. Kluiver, J. et al. BIC and miR-155 are highly expressed in Hodgkin, primary mediastinal and diffuse large B cell lymphomas. The Journal of pathology 207, 243-249, doi: 10.1002/path.1825 (2005).
17. Baumjohann, D. & Ansel, K. M. MicroRNA-mediated regulation of T helper cell differentiation and plasticity. Nature reviews. Immunology 13, 666-678, doi: 10.1038/nri3494 (2013).
18. Martinez-Nunez, R. T., Louafi, F., Friedmann, P. S. & Sanchez-Elsner, T. MicroRNA-155 modulates the pathogen binding ability of dendritic cells (DCs) by down-regulation of DC-specific intercellular adhesion molecule-3 grabbing non-integrin (DC-SIGN). The Journal of biological chemistry 284, 16334-16342, doi: 10.1074/jbc.M109.011601 (2009).
19. Worm, J. et al. Silencing of microRNA-155 in mice during acute inflammatory response leads to derepression of c/ebp Beta and down-regulation of G-CSF. Nucleic Acids Res 37, 5784-5792, doi: 10.1093/nar/gkp577 (2009).
20. Hoeke, L. et al. Intestinal Salmonella typhimurium infection leads to miR-29a induced caveolin 2 regulation. PloS one 8, e67300, doi: 10.1371/journal.pone.0067300 (2013).
21. Huang, T. H. et al. Distinct peripheral blood RNA responses to Salmonella in pigs differing in Salmonella shedding levels: intersection of IFNG, TLR and miRNA pathways. PloS one 6, e28768, doi: 10.1371/journal.pone.0028768 (2011).
22. Mitchell, P. S. et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 105, 10513-10518, doi: 10.1073/pnas.0804549105 (2008).
23. Uthe, J. J. et al. Correlating blood immune parameters and a CCT7 genetic variant with the shedding of Salmonella enterica serovar Typhimurium in swine. Veterinary microbiology 135, 384-388, doi: 10.1016/j.vetmic.2008.09.074 (2009).
24. Knetter, S. M. et al. Salmonella enterica serovar Typhimurium-infected pigs with different shedding levels exhibit distinct clinical, peripheral cytokine and transcriptomic immune response phenotypes. Innate immunity 21, 227-241, doi: 10.1177/1753425914525812 (2015).
25. Kommadath, A. et al. Gene co-expression network analysis identifies porcine genes associated with variation in Salmonella shedding. BMC Genomics 15, 452, doi: 10.1186/1471-2164-15-452 (2014).
26. Friedlander, M. R., Mackowiak, S. D., Li, N., Chen, W. & Rajewsky, N. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res 40, 37-52, doi: 10.1093/nar/gkr688 (2012).
27. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10, R25, doi: 10.1186/gb-2009-10-3-r25 (2009).
28. Groenen, M. A. et al. Analyses of pig genomes provide insight into porcine demography and evolution. Nature 491, 393-398, doi: 10.1038/nature11622 (2012).
29. Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111, doi: 10.1093/bioinformatics/btp120 (2009).
30. Anders, S., Pyl, P. T. & Huber, W. HTSeq-A Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166-169, doi: 10.1093/bioinformatics/btu638 (2015).
31. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140, doi: 10.1093/bioinformatics/btp616 (2010).
32. Enright, A. J. et al. MicroRNA targets in Drosophila. Genome Biol 5, R1, doi: 10.1186/gb-2003-5-1-r1 (2003).
33. Zhang, Y. & Verbeek, F. J. Comparison and integration of target prediction algorithms for microRNA studies. Journal of integrative bioinformatics 7, doi: 10.2390/biecoll-jib-2010-127 (2010).
34. Le, T. D. et al. Inferring microRNA-mRNA causal regulatory relationships from expression data. Bioinformatics 29, 765-771, doi: 10.1093/bioinformatics/btt048 (2013).
35. Bona, M. Causality: models, reasoning, and inference. Choice: Current Reviews for Academic Libraries 47, 1304-1304 (2010).
36. Monteys, A. M. et al. Structure and activity of putative intronic miRNA promoters. RNA 16, 495-505, doi: 10.1261/rna.1731910 (2010).
37. Marsico, A. et al. PROmiRNA: a new miRNA promoter recognition method uncovers the complex regulation of intronic miRNAs. Genome Biol 14, R84, doi: 10.1186/gb-2013-14-8-r84 (2013).
38. He, C. et al. Young intragenic miRNAs are less coexpressed with host genes than old ones: implications of miRNA-host gene coevolution. Nucleic Acids Res 40, 4002-4012, doi: 10.1093/nar/gkr1312 (2012).
39. Sharbati, J. et al. Integrated microRNA-mRNA-Analysis of human monocyte derived macrophages upon Mycobacterium avium subsp. hominissuis infection. PloS one 6, e20258, doi: 10.1371/journal.pone.0020258 (2011).
40. Wang, Y. et al. Integrated analysis of microRNA expression and mRNA transcriptome in lungs of avian influenza virus infected broilers. BMC Genomics 13, 278, doi: 10.1186/1471-2164-13-278 (2012).
41. Peng, X. et al. Computational identification of hepatitis C virus associated microRNA-mRNA regulatory modules in human livers. BMC Genomics 10, 373, doi: 10.1186/1471-2164-10-373 (2009).
42. Durinck, S., Spellman, P. T., Birney, E. & Huber, W. Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt. Nat Protoc 4, 1184-1191, doi: 10.1038/nprot.2009.97 (2009).
43. Falcon, S. & Gentleman, R. Using GOstats to test gene lists for GO term association. Bioinformatics 23, 257-258, doi: 10.1093/bioinformatics/btl567 (2007).
44. Sun, Y. M., Lin, K. Y. & Chen, Y. Q. Diverse functions of miR-125 family in different cell contexts. Journal of hematology & oncology 6, 6, doi: 10.1186/1756-8722-6-6 (2013).
45. Gruenheid, S., Pinner, E., Desjardins, M. & Gros, P. Natural resistance to infection with intracellular pathogens: the Nramp1 protein is recruited to the membrane of the phagosome. The Journal of experimental medicine 185, 717-730 (1997).
46. Brown, D., Trowsdale, J. & Allen, R. The LILR family: modulators of innate and adaptive immune pathways in health and disease. Tissue antigens 64, 215-225, doi: 10.1111/j.0001-2815.2004.00290.x (2004).
47. Boettcher, J. P. et al. Tyrosine-phosphorylated caveolin-1 blocks bacterial uptake by inducing Vav2-RhoA-mediated cytoskeletal rearrangements. PLoS Biol 8, doi: 10.1371/journal.pbio.1000457 (2010).
48. He, X. & Zhang, J. Why do hubs tend to be essential in protein networks? PLoS Genet 2, e88, doi: 10.1371/journal.pgen.0020088 (2006).
49. Arpaia, N. et al. TLR signaling is required for Salmonella typhimurium virulence. Cell 144, 675-688, doi: 10.1016/j.cell.2011.01.031 (2011).
50. Turner, M. & Billadeau, D. D. VAV proteins as signal integrators for multi-subunit immune-recognition receptors. Nature reviews. Immunology 2, 476-486, doi: 10.1038/nri840 (2002).
51. Barton, C. H., Biggs, T. E., Baker, S. T., Bowen, H. & Atkinson, P. G. Nramp1: a link between intracellular iron transport and innate resistance to intracellular pathogens. Journal of leukocyte biology 66, 757-762 (1999).
52. Zhong, W., Lafuse, W. P. & Zwilling, B. S. Infection with Mycobacterium avium differentially regulates the expression of iron transport protein mRNA in murine peritoneal macrophages. Infection and immunity 69, 6618-6624, doi: 10.1128/IAI.69.11.6618-6624.2001 (2001).
53. Richer, E., Campion, C. G., Dabbas, B., White, J. H. & Cellier, M. F. Transcription factors Sp1 and C/EBP regulate NRAMP1 gene expression. The FEBS journal 275, 5074-5089, doi: 10.1111/j.1742-4658.2008.06640.x (2008).
54. Pilsbury, L. E., Allen, R. L. & Vordermeier, M. Modulation of Toll-like receptor activity by leukocyte Ig-like receptors and their effects during bacterial infection. Mediators of inflammation 2010, 536478, doi: 10.1155/2010/536478 (2010).
55. Anderson, K. J. & Allen, R. L. Regulation of T-cell immunity by leucocyte immunoglobulin-like receptors: innate immune receptors for self on antigen-presenting cells. Immunology 127, 8-17, doi: 10.1111/j.1365-2567.2009.03097.x (2009).
56. Liew, F. Y., Xu, D., Brint, E. K. & O'Neill, L. A. Negative regulation of toll-like receptor-mediated immune responses. Nature reviews. Immunology 5, 446-458, doi: 10.1038/nri1630 (2005).
57. Boquet, P. & Lemichez, E. Bacterial virulence factors targeting Rho GTPases: parasitism or symbiosis? Trends in cell biology 13, 238-246 (2003).
58. Abe, K. et al. Vav2 is an activator of Cdc42, Rac1, and RhoA. The Journal of biological chemistry 275, 10141-10149 (2000).
59. Krause-Gruszczynska, M. et al. The signaling pathway of Campylobacter jejuni-induced Cdc42 activation: Role of fibronectin, integrin beta1, tyrosine kinases and guanine exchange factor Vav2. Cell communication and signaling: CCS 9, 32, doi: 10.1186/1478-811X-9-32 (2011).