Dual RNA-seq unveils noncoding RNA functions in host-pathogen interactions

Nature

Volumn 529, Issue 7587, 2016, Pages 496-501

  Westermann, Alexander J ^a   Förstner, Konrad U ^a   Amman, Fabian ^b,c   Barquist, Lars ^a   Chao, Yanjie ^a   Schulte, Leon N ^a   Müller, Lydia ^b   Reinhardt, Richard ^d   Stadler, Peter F ^b,c,e,f   Vogel, Jörg ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c UNIVERSITY OF VIENNA   (Austria)

^d MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^e MAX PLANCK INSTITUTE FOR MATHEMATICS IN THE SCIENCES   (Germany)

^f SANTA FE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

UNTRANSLATED RNA;

BACTERIUM; GENETIC ANALYSIS; HOST-PATHOGEN INTERACTION; PHENOTYPE; RNA; VIRULENCE;

ARTICLE; BACTERIAL GENE; CELL SURVIVAL; HOST PATHOGEN INTERACTION; INFECTION; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA SEQUENCE; SALMONELLA; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM;

BACTERIA (MICROORGANISMS); SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 84964262313     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature16547     Document Type: Article

References (84)

1. Caldelari, I., Chao, Y., Romby, P. & Vogel, J. RNA-mediated regulation in pathogenic bacteria. Cold Spring Harb. Perspect. Med. 3, http://dx.doi.org/10.1101/cshperspect.a010298 (2013).
2. Gottesman, S. & Storz, G. Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harbor Perspect. Biol. 3, http://dx.doi.org/10.1101/cshperspect.a003798 (2011).
3. Wagner, E. G. H. & Romby, P. Small RNAs in Bacteria and Archaea: who they are, what they do, and how they do it. Adv. Genet. 90, 133-208 (2015).
4. Kroger, C. et al. An infection-relevant transcriptomic compendium for Salmonella enterica serovar Typhimurium. Cell Host Microbe 14, 683-695 (2013).
5. Chao, Y., Papenfort, K., Reinhardt, R., Sharma, C. M. & Vogel, J. An atlas of Hfq-bound transcripts reveals 3′ UTRs as a genomic reservoir of regulatory small RNAs. EMBO J. 31, 4005-4019 (2012).
6. Ortega, A. D., Gonzalo-Asensio, J. & Garcia-del Portillo, F. Dynamics of Salmonella small RNA expression in non-growing bacteria located inside eukaryotic cells. RNA Biol. 9, 469-488 (2012).
7. Padalon-Brauch, G. et al. Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence. Nucleic Acids Res. 36, 1913-1927 (2008).
8. Pfeiffer, V. et al. A small non-coding RNA of the invasion gene island (SPI-1) represses outer membrane protein synthesis from the Salmonella core genome. Mol. Microbiol. 66, 1174-1191 (2007).
9. Gong, H. et al. A Salmonella small non-coding RNA facilitates bacterial invasion and intracellular replication by modulating the expression of virulence factors. PLoS Pathog. 7, e1002120 (2011).
10. Papenfort, K., Podkaminski, D., Hinton, J. C. & Vogel, J. The ancestral SgrS RNA discriminates horizontally acquired Salmonella mRNAs through a single G-U wobble pair. Proc. Natl Acad. Sci. USA 109, E757-E764 (2012).
11. Sittka, A., Pfeiffer, V., Tedin, K. & Vogel, J. The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol. Microbiol. 63, 193-217 (2007).
12. Santiviago, C. A. et al. Analysis of pools of targeted Salmonella deletion mutants identifies novel genes affecting fitness during competitive infection in mice. PLoS Pathog. 5, e1000477 (2009).
13. Chaudhuri, R. R. et al. Comprehensive assignment of roles for Salmonella Typhimurium genes in intestinal colonization of food-producing animals. PloS Genetics 9, e1003456 (2013).
14. Barquist, L. & Vogel, J. Accelerating discovery and functional analysis of small RNAs with new technologies. Annu. Rev. Genet. 49, 367-394 (2015).
15. Westermann, A. J., Gorski, S. A. & Vogel, J. Dual RNA-seq of pathogen and host. Nature Rev. Microbiol. 10, 618-630 (2012).
16. Sorek, R. & Cossart, P. Prokaryotic transcriptomics: a new view on regulation, physiology and pathogenicity. Nature Rev. Genet. 11, 9-16, (2010).
17. Humphrys, M. S. et al. Simultaneous transcriptional profiling of bacteria and their host cells. PloS ONE 8, e80597 (2013).
18. Malik-Kale, P. et al. Salmonella - at home in the host cell. Front. Microbiol. 2, 125 (2011).
19. Wyllie, D. H. et al. Evidence for an accessory protein function for Toll-like receptor 1 in anti-bacterial responses. J. Immunol. 165, 7125-7132 (2000).
20. Bumann, D. Examination of Salmonella gene expression in an infected mammalian host using the green fluorescent protein and two-colour flow cytometry. Mol. Microbiol. 43, 1269-1283 (2002).
21. Sharma, C. M. et al. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464, 250-255 (2010).
22. Hautefort, I. et al. During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell Microbiol. 10, 958-984 (2008).
23. Hannemann, S., Gao, B. & Galan, J. E. Salmonella modulation of host cell gene expression promotes its intracellular growth. PLoS Pathog. 9, e1003668 (2013).
24. Masse, E., Vanderpool, C. K. & Gottesman, S. Effect of RyhB small RNA on global iron use in Escherichia coli. J. Bacteriol. 187, 6962-6971 (2005).
25. Guo, M. S. et al. MicL, a new σE-dependent sRNA, combats envelope stress by repressing synthesis of Lpp, the major outer membrane lipoprotein. Genes Dev. 28, 1620-1634 (2014).
26. Guillier, M. & Gottesman, S. The 5′ end of two redundant sRNAs is involved in the regulation of multiple targets, including their own regulator. Nucleic Acids Res. 36, 6781-6794 (2008).
27. Moon, K., Six, D. A., Lee, H. J., Raetz, C. R. & Gottesman, S. Complex transcriptional and post-transcriptional regulation of an enzyme for lipopolysaccharide modification. Mol. Microbiol. 89, 52-64 (2013).
28. Löber, S., Jackel, D., Kaiser, N. & Hensel, M. Regulation of Salmonella pathogenicity island 2 genes by independent environmental signals. Int. J. Med. Microbiol. 296, 435-447 (2006).
29. Sittka, A. et al. Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet. 4, e1000163 (2008).
30. Prost, L. R., Daley, M. E., Bader, M. W., Klevit, R. E. & Miller, S. I. The PhoQ histidine kinases of Salmonella and Pseudomonas spp. are structurally and functionally different: evidence that pH and antimicrobial peptide sensing contribute to mammalian pathogenesis. Mol. Microbiol. 69, 503-519 (2008).
31. Groisman, E. A. The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol. 183, 1835-1842 (2001).
32. Vogel, J. & Luisi, B. F. Hfq and its constellation of RNA. Nature Rev. Microbiol. 9, 578-589 (2011).
33. Bruno, V. M. et al. Salmonella Typhimurium type III secretion effectors stimulate innate immune responses in cultured epithelial cells. PLoS Pathog. 5, e1000538 (2009).
34. Vonaesch, P. et al. The Salmonella Typhimurium effector protein SopE transiently localizes to the early SCV and contributes to intracellular replication. Cell. Microbiol. 16, 1723-1735 (2014).
35. Bjur, E., Eriksson-Ygberg, S., Aslund, F. & Rhen, M. Thioredoxin 1 promotes intracellular replication and virulence of Salmonella enterica serovar Typhimurium. Infect. Immun. 74, 5140-5151 (2006).
36. Chen, Z. W. et al. Mutations in the Salmonella enterica serovar Choleraesuis cAMP-receptor protein gene lead to functional defects in the SPI-1 type III secretion system. Vet. Res. 41, 05 (2010).
37. Yoon, H. J., McDermott, J. E., Porwollik, S., McClelland, M. & Heffron, F. Coordinated regulation of virulence during systemic infection of Salmonella enterica serovar Typhimurium. PloS Pathogens 5, e1000306 (2009).
38. Choi, J. & Groisman, E. A. The lipopolysaccharide modification regulator PmrA limits Salmonella virulence by repressing the type three-secretion system Spi/Ssa. Proc. Natl Acad. Sci. USA 110, 9499-9504 (2013).
39. Li, Y., de Haar, C., Peppelenbosch, M. P. & van der Woude, C. J. SOCS3 in immune regulation of inflammatory bowel disease and inflammatory bowel disease-related cancer. Cytokine Growth Factor Rev. 23, 127-138 (2012).
40. Browning, D. D., Diehl, W. C., Hsu, M. H., Schraufstatter, I. U. & Ye, R. D. Autocrine regulation of interleukin-8 production in human monocytes. Am. J. Physiol. Lung Cell. Mol. Physiol. 279, L1129-L1136 (2000).
41. Uchiya, K. & Nikai, T. Salmonella pathogenicity island 2-dependent expression of suppressor of cytokine signaling 3 in macrophages. Infect. Immun. 73, 5587-5594 (2005).
42. Bhavsar, A. P. et al. The Salmonella type III effector SspH2 specifically exploits the NLR co-chaperone activity of SGT1 to subvert immunity. PLoS Pathog. 9, e1003518 (2013).
43. Winter, S. E. et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467, 426-429 (2010).
44. Stecher, B. et al. Salmonella enterica serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 5, e244 (2007).
45. Gewirtz, A. T., Siber, A. M., Madara, J. L. & McCormick, B. A. Orchestration of neutrophil movement by intestinal epithelial cells in response to Salmonella typhimurium can be uncoupled from bacterial internalization. Infect. Immun. 67, 608-617 (1999).
46. Holmqvist, E. et al. Two antisense RNAs target the transcriptional regulator CsgD to inhibit curli synthesis. EMBO J. 29, 1840-1850 (2010).
47. Chen, X. et al. An RNA degradation machine sculpted by Ro autoantigen and noncoding RNA. Cell 153, 166-177 (2013).
48. Mazurkiewicz, P., Tang, C. M., Boone, C. & Holden, D. W. Signature-tagged mutagenesis: barcoding mutants for genome-wide screens. Nature Rev. Genet. 7, 929-939 (2006).
49. Becker, D. et al. Robust Salmonella metabolism limits possibilities for new antimicrobials. Nature 440, 303-307 (2006).
50. Myers, M. G. Moonlighting in mitochondria. Science 323, 723-724 (2009).
51. Papenfort, K. et al. Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol. Microbiol. 74, 139-158 (2009).
52. Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA 97, 6640-6645 (2000).
53. Sternberg, N. L. & Maurer, R. Bacteriophage-mediated generalized transduction in Escherichia coli and Salmonella typhimurium. Methods Enzymol. 204, 18-43 (1991).
54. Berschneider, H. M. Development of normal cultured small intestinal epithelial cell lines which transport Na and Cl. Gastroenterology 96:A41 (1989).
55. Weingartl, H. M., Sabara, M., Pasick, J., van Moorlehem, E. & Babiuk, L. Continuous porcine cell lines developed from alveolar macrophages: partial characterization and virus susceptibility. J. Virol. Methods 104, 203-216 (2002).
56. 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. EMBO J. 30, 1977-1989 (2011).
57. Eriksson, S., Lucchini, S., Thompson, A., Rhen, M. & Hinton, J. C. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 47, 103-118 (2003).
58. Hamatani, K. et al. Improved RT-PCR amplification for molecular analyses with long-term preserved formalin-fixed, paraffin-embedded tissue specimens. J. Histochem. Cytochem. 54, 773-780 (2006).
59. Kuramochi, H. et al. Vascular endothelial growth factor messenger RNA expression level is preserved in liver metastases compared with corresponding primary colorectal cancer. Clin. Cancer Res. 12, 29-33 (2006).
60. -ΔΔCT Method. Methods 25, 402-408 (2001).
61. E-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol. Microbiol. 62, 1674-1688 (2006).
62. Urban, J. H. & Vogel, J. Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res. 35, 1018-1037 (2007).
63. The 1000 Genomes Project Consortium An integrated map of genetic variation from 1,092 human genomes. Nature 491, 56-65 (2012).
64. Förstner K. U., Vogel J. & Sharma C. M. READemption - a tool for the computational analysis of deep-sequencing-based transcriptome data. Bioinformatics 30, 3421-3423 (2014).
65. Otto, C., Stadler, P. F. & Hoffmann, S. Lacking alignments? The next-generation sequencing mapper segemehl revisited. Bioinformatics 30, 1837-1843 (2014).
66. Hoffmann, S. et al. A multi-split mapping algorithm for circular RNA, splicing, trans-splicing, and fusion detection. Genome Biol. 15, R34 (2014).
67. Harrow, J. et al. GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res. 22, 1760-1774 (2012).
68. Xie, C. et al. NONCODEv4: exploring the world of long non-coding RNA genes. Nucleic Acids Res. 42, D98-D103 (2014).
69. Kozomara, A. & Griffiths-Jones, S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 42, D68-D73 (2014).
70. Kroger, C. et al. The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc. Natl Acad. Sci. USA 109, E1277-E1286 (2012).
71. 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 (2010).
72. Risso, D., Ngai, J., Speed, T. P. & Dudoit, S. Normalization of RNA-seq data using factor analysis of control genes or samples. Nature Biotechnol. 32, 896-902 (2014).
73. Nicol, J. W., Helt, G. A., Blanchard, S. G., Raja, A. & Loraine, A. E. The Integrated Genome Browser: free software for distribution and exploration of genome-scale datasets. Bioinformatics 25, 2730-2731 (2009).
74. Kanehisa, M. et al. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 42, D199-D205 (2014).
75. Luo, W. & Brouwer, C. Pathview: an R/Bioconductor package for pathway-based data integration and visualization. Bioinformatics 29, 1830-1831 (2013).
76. Rebhan, M., Chalifa-Caspi, V., Prilusky, J. & Lancet, D. GeneCards: integrating information about genes, proteins and diseases. Trends Genet. 13, 163 (1997).
77. Choi, Y. S. et al. Nuclear IL-33 is a transcriptional regulator of NF-κB p65 and induces endothelial cell activation. Biochem. Biophys. Res. Commun. 421, 305-311 (2012).
78. Oida, Y. et al. Inhibition of nuclear factor-κB augments antitumor activity of adenovirus-mediated melanoma differentiation-associated gene-7 against lung cancer cells via mitogen-activated protein kinase kinase kinase 1 activation. Mol. Cancer Ther. 6, 1440-1449 (2007).
79. Dauer, D. J. et al. Stat3 regulates genes common to both wound healing and cancer. Oncogene 24, 3397-3408 (2005).
80. Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnol. 28, 511-515 (2010).
81. Trapnell, C. et al. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nature Biotechnol. 31, 46-53 (2013).
82. Bauer, S., Grossmann, S., Vingron, M. & Robinson, P. N. Ontologizer 2.0-a multifunctional tool for GO term enrichment analysis and data exploration. Bioinformatics 24, 1650-1651 (2008).
83. Soncini, F. C., Vescovi, E. G. & Groisman, E. A. Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon. J. Bacteriol. 177, 4364-4371 (1995).
84. Rehmsmeier, M., Steffen, P., Hochsmann, M. & Giegerich, R. Fast and effective prediction of microRNA/target duplexes. RNA 10, 1507-1517 (2004).