SecA2 Associates with Translating Ribosomes and Contributes to the Secretion of Potent IFN-β Inducing RNAs
Abstract
:1. Introduction
2. Results
2.1. Production of Tagged and Functional SecA2 in ∆secA2 Deletion Mutant
2.2. Affinity-Based Purification of Tagged SecA2
2.3. SecA2 Co-Sediments with Ribosomes
2.4. SecA2 Interacts with Translating Ribosomes
2.5. Identification of SecA2 Co-Eluted Proteins
2.6. Association of RNA with SecA2
2.7. SecA2-Associated RNAs Are Potent Inducers of IFN-β
2.8. Detection of Small Non-Coding RNAs in SecA2-Associated RNAs
2.9. Deletion of Enolase Affects the Sec-RNA Amount and Composition in the Sec-RNA Fraction
3. Discussion
4. Materials and Methods
4.1. Bacterial Strains and Growth Conditions
4.2. Construction of Deletion Mutants
4.3. Construction of Affinity-Tagged SecA2 Expression Plasmid
4.4. Protein Purification
4.5. Matrix-Assisted Laser-Desorption Ionization Time-Of-Flight Mass Spectrometry (MALDI-TOF-MS)
4.6. Ribosome Purification
4.7. Co-Sedimentation Experiments
4.8. Western Blotting
4.9. Polysome Profiling Using Sucrose Gradient Centrifugation
4.10. Isolation of Cytosolic RNA
4.11. Isolation of Sec-RNA and SecA2/SecA1-Associated RNAs
4.12. cDNA Synthesis and RNA-Sequencing
4.13. Cell Culture and Transfection Assay
4.14. Quantitative Real-Time PCR
4.15. Statistical Analysis
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Lmo Nr. | Gene Name | Protein Name | Function (COGs) * | emPAI * | mol % * |
---|---|---|---|---|---|
lmo0583 | secA2 | Protein translocase subunit SecA 2 | Intracellular trafficking and secretion | 5.81 | 6.75 |
lmo2632 | rplC | 50S ribosomal protein L3 | Translation | 4.75 | 4.69 |
lmo1934 | hup | DNA-binding protein HU | Replication. recombination and repair | 3.54 | 4.69 |
lmo2629 | rplB | 50S ribosomal protein L2 | Translation | 3.20 | 3.87 |
lmo2653 * | tuf | Elongation factor Tu | Translation | 2.78 | 3.69 |
lmo1830 | Short-chain dehydrogenase | Lipid transport and metabolism; Secondary metabolites biosynthesis. transport and catabolism; General function prediction only; | 1.73 | 2.41 | |
lmo1783 | rplT | 50S ribosomal protein L20 | Translation | 2.08 | 2.26 |
lmo1072 | pycA | Pyruvate carboxylase | Energy production and conversion | 2.08 | 2.20 |
lmo1356 | Acetyl-CoA carboxylase biotin carboxyl carrier protein | Lipid transport and metabolism | 1.70 | 2.16 | |
lmo1330 | rpsO | 30S ribosomal protein S15 | Translation | 2.32 | 2.15 |
lmo2624 | rpmC | 50S ribosomal protein L29 | Translation | 1.60 | 2.09 |
lmo2016 | cspB | Cold shock-like protein CspLB | Transcription | 1.51 | 1.98 |
lmo1473 * | dnaK | Chaperone protein DnaK | Posttranslational modification. protein turnover. chaperones | 1.72 | 1.96 |
lmo2631 | rplD | 50S ribosomal protein L4 | Translation | 1.53 | 1.78 |
lmo2459 | gap | Glyceraldehyde-3-phosphate dehydrogenase | Carbohydrate transport and metabolism | 1.25 | 1.60 |
lmo1596 | rpsD | 30S ribosomal protein S4 | Translation | 1.47 | 1.37 |
lmo1055 | PdhD | Dihydrolipoamide dehydrogenase | Energy production and conversion | 0.91 | 1.33 |
lmo2625 | rplP | 50S ribosomal protein L16 | Translation | 1.00 | 1.29 |
lmo1542 | rplU | 50S ribosomal protein L21 | Translation | 0.93 | 1.13 |
lmo2455 * | eno | Enolase | Carbohydrate transport and metabolism | 0.77 | 1.10 |
lmo1658 | rpsB | 30S ribosomal protein S2 | Translation | 0.94 | 1.09 |
lmo0972 | dltC | D-alanine--poly(phosphoribitol) ligase subunit 2 | Cell wall/membrane biogenesis | 0.98 | 1.02 |
lmo2613 | rplO | 50S ribosomal protein L15 | Translation | 0.75 | 0.90 |
lmo2785 | kat | Catalase | Inorganic ion transport and metabolism | 0.65 | 0.90 |
lmo1657 | tsf | Elongation factor Ts | Translation | 0.70 | 0.88 |
lmo2654 | fus | Elongation factor G | Translation | 0.71 | 0.78 |
lmo2630 | rplW | 50S ribosomal protein L23 | Translation | 0.62 | 0.77 |
lmo2969 | groES | 10 kDa chaperonin | not in COGs | 0.46 | 0.75 |
lmo2483 | hprK | Phosphocarrier protein HPr | Signal transduction mechanisms | 0.70 | 0.73 |
lmo1920 | Copper chaperone CopZ | Function unknown | 0.52 | 0.64 | |
lmo1364 | cspL | Cold shock protein CspA | Transcription | 0.47 | 0.61 |
lmo0044 | rpsF | 30S ribosomal protein S6 | Translation | 0.47 | 0.61 |
lmo2608 | rpsM | 30S ribosomal protein S13 | Translation | 0.39 | 0.51 |
lmo2068 * | groEL | 60 kDa chaperonin | Posttranslational modification. protein turnover. chaperones | 0.40 | 0.50 |
lmo2703 | similar to B. subtilis YaaK protein | Function unknown | 0.39 | 0.48 | |
lmo2182 | Iron ABC transporter ATP-binding protein | Inorganic ion transport and metabolism; Coenzyme transport and metabolism; | 0.37 | 0.46 | |
lmo1797 | rpsP | 30S ribosomal protein S16 | Translation | 0.39 | 0.44 |
lmo0866 | cshA | DEAD-box ATP-dependent RNA helicase CshA | Replication. recombination and repair; Transcription; Translation; | 0.32 | 0.41 |
lmo2219 | prsA2 | Foldase protein PrsA 2 | Posttranslational modification. protein turnover. chaperones | 0.30 | 0.34 |
lmo1398 | recA | Protein RecA | Replication. recombination and repair | 0.30 | 0.34 |
lmo0249 | rplA | Ribosomal protein (Fragment) | Translation | 0.26 | 0.34 |
lmo2511 | hpf | Ribosome hibernation promoting factor | Translation | 0.26 | 0.32 |
lmo1373 | 2-oxoisovalerate dehydrogenase | Energy production and conversion | 0.30 | 0.31 | |
lmo1388 * | tcsA | CD4+ T-cell-stimulating antigen | General function prediction only | 0.25 | 0.30 |
lmo0237 | gltX | Glutamate--tRNA ligase | Translation | 0.20 | 0.29 |
lmo1785 | infC | Initiation factor IF-3 | Translation | 0.28 | 0.29 |
lmo1267 | tig | Trigger factor | Posttranslational modification. protein turnover. chaperones | 0.19 | 0.28 |
lmo1054 * | pdhC | Pyruvate dehydrogenase E2 component (Dihydrolipoamide acetyltransferase) | Energy production and conversion | 0.20 | 0.26 |
lmo2615 | rpsE | 30S ribosomal protein S5 | Translation | 0.19 | 0.25 |
lmo0135 | Putative oligopeptide ABC transporter. OppA | Amino acid transport and metabolism | 0.21 | 0.24 | |
lmo2457 | tpiA | Triosephosphate isomerase | Carbohydrate transport and metabolism | 0.21 | 0.24 |
lmo1579 | Alanine dehydrogenase | Amino acid transport and metabolism | 0.16 | 0.21 | |
lmo1331 | pnpA | Polyribonucleotide nucleotidyltransferase | Translation | 0.19 | 0.21 |
lmo2799 | GTP-binding protein YchF | Carbohydrate transport and metabolism | 0.23 | 0.21 | |
lmo1664 | metK | S-adenosylmethionine synthase | Coenzyme transport and metabolism | 0.20 | 0.20 |
lmo1439 * | sodA | Superoxide dismutase | Inorganic ion transport and metabolism | 0.13 | 0.20 |
lmo2597 | rplM | 50S ribosomal protein L13 | Translation | 0.17 | 0.20 |
lmo2510 | secA | Protein translocase subunit SecA 1 | Intracellular trafficking and secretion | 0.21 | 0.19 |
lmo2618 | rpsH | 30S ribosomal protein S8 | Translation | 0.16 | 0.19 |
lmo0539 | Tagatose 1.6-diphosphate aldolase | Carbohydrate transport and metabolism | 0.13 | 0.18 | |
lmo2637 * | FMN-binding domain protein | Function unknown | 0.13 | 0.16 | |
lmo2367 | pgi | Glucose-6-phosphate isomerase | Carbohydrate transport and metabolism | 0.11 | 0.16 |
lmo1571 | pfkA | ATP-dependent 6-phosphofructokinase | Carbohydrate transport and metabolism | 0.12 | 0.15 |
lmo0223 | cysK | Cysteine synthase | Amino acid transport and metabolism | 0.12 | 0.15 |
lmo2620 | rplE | 50S ribosomal protein L5 | Translation | 0.12 | 0.15 |
lmo0416 | Uncharacterized protein. DNA-binding. putative regulator | Transcription | 0.14 | 0.14 | |
lmo1052 | pdhA | Pyruvate dehydrogenase (Acetyl-transferring) E1 component. alpha subunit | Energy production and conversion | 0.10 | 0.13 |
lmo2458 | pgk | Phosphoglycerate kinase | Carbohydrate transport and metabolism | 0.09 | 0.13 |
lmo2206 | clpB | Chaperone protein ClpB | Posttranslational modification. protein turnover. chaperones | 0.12 | 0.13 |
lmo1357 | acetyl-CoA carboxylase biotin carboxylase subunit | Lipid transport and metabolism | 0.12 | 0.11 | |
lmo1217 | Putative aminopeptidase. M42 family | Carbohydrate transport and metabolism | 0.09 | 0.11 | |
lmo1928 | aroF | Chorismate synthase | Amino acid transport and metabolism | 0.08 | 0.10 |
lmo2559 | pyrG | CTP synthase | Nucleotide transport and metabolism | 0.09 | 0.09 |
lmo2456 | pgm | 2.3-bisphosphoglycerate-independent phosphoglycerate mutase | Carbohydrate transport and metabolism | 0.07 | 0.09 |
lmo1938 | rpsA | 30S ribosomal protein S1 homolog | Translation | 0.08 | 0.08 |
lmo1755 | gatA | Glutamyl-tRNA(Gln) amidotransferase subunit A | Translation | 0.07 | 0.08 |
lmo0727 | glmS | Glutamine--fructose-6-phosphate aminotransferase [isomerizing] | Cell wall/membrane biogenesis | 0.07 | 0.08 |
lmo1286 | parE | DNA topoisomerase 4 subunit B | Replication. recombination and repair | 0.06 | 0.07 |
lmo0258 * | rpoB | RNA polymerase beta subunit | Transcription | 0.05 | 0.06 |
lmo1003 | ptsI | Phosphoenolpyruvate-protein phosphotransferase | Carbohydrate transport and metabolism | 0.05 | 0.06 |
lmo1634 * | lap | Aldehyde-alcohol dehydrogenase | Energy production and conversion | 0.05 | 0.06 |
lmo0259 * | rpoC | DNA-directed RNA polymerase subunit beta’ | Transcription | 0.05 | 0.05 |
lmo1504 | alaS | Alanine—tRNA ligase | Translation | 0.04 | 0.05 |
lmo2019 | ileS | Isoleucine—tRNA ligase | Translation | 0.03 | 0.04 |
lmo0007 | gyrA | DNA gyrase subunit A | Replication. recombination and repair | 0.03 | 0.03 |
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Teubner, L.; Frantz, R.; La Pietra, L.; Hudel, M.; Bazant, J.; Lochnit, G.; Eismann, L.; Kramer, G.; Chakraborty, T.; Abu Mraheil, M. SecA2 Associates with Translating Ribosomes and Contributes to the Secretion of Potent IFN-β Inducing RNAs. Int. J. Mol. Sci. 2022, 23, 15021. https://doi.org/10.3390/ijms232315021
Teubner L, Frantz R, La Pietra L, Hudel M, Bazant J, Lochnit G, Eismann L, Kramer G, Chakraborty T, Abu Mraheil M. SecA2 Associates with Translating Ribosomes and Contributes to the Secretion of Potent IFN-β Inducing RNAs. International Journal of Molecular Sciences. 2022; 23(23):15021. https://doi.org/10.3390/ijms232315021
Chicago/Turabian StyleTeubner, Lisa, Renate Frantz, Luigi La Pietra, Martina Hudel, Jasmin Bazant, Günter Lochnit, Lena Eismann, Günter Kramer, Trinad Chakraborty, and Mobarak Abu Mraheil. 2022. "SecA2 Associates with Translating Ribosomes and Contributes to the Secretion of Potent IFN-β Inducing RNAs" International Journal of Molecular Sciences 23, no. 23: 15021. https://doi.org/10.3390/ijms232315021