Central role for RNase YbeY in Hfq-dependent and Hfq-independent small-RNA regulation in bacteria
Background: Conceptual parallels exist between bacterial and eukaryotic small-RNA (sRNA) pathways, yet relatively little is known about which protein may recognize and recruit bacterial sRNAs to interact with targets. In eukaryotes, Argonaute (AGO) proteins discharge such functions. The highly cons...
| Main Authors: | , , , , , |
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| Other Authors: | |
| Format: | Article |
| Language: | English |
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BioMed Central Ltd
2014
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| Online Access: | http://hdl.handle.net/1721.1/85993 https://orcid.org/0000-0001-7243-8261 |
| _version_ | 1826203790097776640 |
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| author | Pandey, Shree P. Winkler, Jonathan A. Li, Hu Camacho, Diogo M. Collins, James J. Walker, Graham C. |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Pandey, Shree P. Winkler, Jonathan A. Li, Hu Camacho, Diogo M. Collins, James J. Walker, Graham C. |
| author_sort | Pandey, Shree P. |
| collection | MIT |
| description | Background:
Conceptual parallels exist between bacterial and eukaryotic small-RNA (sRNA) pathways, yet relatively little is known about which protein may recognize and recruit bacterial sRNAs to interact with targets. In eukaryotes, Argonaute (AGO) proteins discharge such functions. The highly conserved bacterial YbeY RNase has structural similarities to the MID domain of AGOs. A limited study had indicated that in Sinorhizobium meliloti the YbeY ortholog regulates the accumulation of sRNAs as well as the target mRNAs, raising the possibility that YbeY may play a previously unrecognized role in bacterial sRNA regulation.
Results:
We have applied a multipronged approach of loss-of-function studies, genome-wide mRNA and sRNA expression profiling, pathway analysis, target prediction, literature mining and network analysis to unravel YbeY-dependent molecular responses of E. coli exposed to hydroxyurea (HU). Loss of ybeY function, which results in a marked resistance to HU, had global affects on sRNA-mediated gene expression. Of 54 detectable E. coli sRNAs in our microarray analysis, 30 sRNAs showed a differential expression upon HU stress, of which 28 sRNAs displayed a YbeY-dependent change in expression. These included 12 Hfq-dependent and 16 Hfq-independent sRNAs. We successfully identified at least 57 experimentally inferred sRNA-mRNA relationships. Further applying a 'context likelihood of relatedness' algorithm, we reverse engineered the YbeY-dependent Hfq-dependent sRNA-mRNA network as well as YbeY-dependent Hfq-independent sRNA-mRNA network.
Conclusion:
YbeY extensively modulates Hfq-dependent and independent sRNA-mRNA interactions. YbeY-dependent sRNAs have central roles in modulating cellular response to HU stress. |
| first_indexed | 2024-09-23T12:43:04Z |
| format | Article |
| id | mit-1721.1/85993 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2024-09-23T12:43:04Z |
| publishDate | 2014 |
| publisher | BioMed Central Ltd |
| record_format | dspace |
| spelling | mit-1721.1/859932022-10-01T10:40:33Z Central role for RNase YbeY in Hfq-dependent and Hfq-independent small-RNA regulation in bacteria Pandey, Shree P. Winkler, Jonathan A. Li, Hu Camacho, Diogo M. Collins, James J. Walker, Graham C. Massachusetts Institute of Technology. Department of Biology Walker, Graham C. Background: Conceptual parallels exist between bacterial and eukaryotic small-RNA (sRNA) pathways, yet relatively little is known about which protein may recognize and recruit bacterial sRNAs to interact with targets. In eukaryotes, Argonaute (AGO) proteins discharge such functions. The highly conserved bacterial YbeY RNase has structural similarities to the MID domain of AGOs. A limited study had indicated that in Sinorhizobium meliloti the YbeY ortholog regulates the accumulation of sRNAs as well as the target mRNAs, raising the possibility that YbeY may play a previously unrecognized role in bacterial sRNA regulation. Results: We have applied a multipronged approach of loss-of-function studies, genome-wide mRNA and sRNA expression profiling, pathway analysis, target prediction, literature mining and network analysis to unravel YbeY-dependent molecular responses of E. coli exposed to hydroxyurea (HU). Loss of ybeY function, which results in a marked resistance to HU, had global affects on sRNA-mediated gene expression. Of 54 detectable E. coli sRNAs in our microarray analysis, 30 sRNAs showed a differential expression upon HU stress, of which 28 sRNAs displayed a YbeY-dependent change in expression. These included 12 Hfq-dependent and 16 Hfq-independent sRNAs. We successfully identified at least 57 experimentally inferred sRNA-mRNA relationships. Further applying a 'context likelihood of relatedness' algorithm, we reverse engineered the YbeY-dependent Hfq-dependent sRNA-mRNA network as well as YbeY-dependent Hfq-independent sRNA-mRNA network. Conclusion: YbeY extensively modulates Hfq-dependent and independent sRNA-mRNA interactions. YbeY-dependent sRNAs have central roles in modulating cellular response to HU stress. National Institutes of Health (U.S.) (Grant R01 CA021615) National Institutes of Health (U.S.) (Grant GM31010) National Institutes of Health (U.S.) (Grant P30 ES002019) Howard Hughes Medical Institute 2014-04-03T16:09:02Z 2014-04-03T16:09:02Z 2014-02 2014-01 2014-04-02T15:36:33Z Article http://purl.org/eprint/type/JournalArticle 1471-2164 http://hdl.handle.net/1721.1/85993 Pandey, Shree P et al. “Central Role for RNase YbeY in Hfq-Dependent and Hfq-Independent Small-RNA Regulation in Bacteria.” BMC Genomics 15.1 (2014): 121. https://orcid.org/0000-0001-7243-8261 en http://dx.doi.org/10.1186/1471-2164-15-121 BMC Genomics Creative Commons Attribution http://creativecommons.org/licenses/by/2.0 Shree P Pandey et al.; licensee BioMed Central Ltd. application/pdf BioMed Central Ltd BioMed Central Ltd |
| spellingShingle | Pandey, Shree P. Winkler, Jonathan A. Li, Hu Camacho, Diogo M. Collins, James J. Walker, Graham C. Central role for RNase YbeY in Hfq-dependent and Hfq-independent small-RNA regulation in bacteria |
| title | Central role for RNase YbeY in Hfq-dependent and Hfq-independent small-RNA regulation in bacteria |
| title_full | Central role for RNase YbeY in Hfq-dependent and Hfq-independent small-RNA regulation in bacteria |
| title_fullStr | Central role for RNase YbeY in Hfq-dependent and Hfq-independent small-RNA regulation in bacteria |
| title_full_unstemmed | Central role for RNase YbeY in Hfq-dependent and Hfq-independent small-RNA regulation in bacteria |
| title_short | Central role for RNase YbeY in Hfq-dependent and Hfq-independent small-RNA regulation in bacteria |
| title_sort | central role for rnase ybey in hfq dependent and hfq independent small rna regulation in bacteria |
| url | http://hdl.handle.net/1721.1/85993 https://orcid.org/0000-0001-7243-8261 |
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