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Structure and mechanism of a molecular rheostat, an RNA thermometer that modulates immune evasion by Neisseria meningitidis.

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Barnwal RP, Loh E, Godin KS, Yip J, Lavender H, Tang CM, Varani G
OpenAccess logo Nucleic Acids Res 44 9426-9437 (2016)
Related entries: 2n6s, 2n6w, 2n6x

Cited: 30 times
EuropePMC logo PMID: 27369378

Abstract

Neisseria meningitidis causes bacterial meningitis and septicemia. It evades the host complement system by upregulating expression of immune evasion factors in response to changes in temperature. RNA thermometers within mRNAs control expression of bacterial immune evasion factors, including CssA, in the 5'-untranslated region of the operon for capsule biosynthesis. We dissect the molecular mechanisms of thermoregulation and report the structure of the CssA thermometer. We show that the RNA thermometer acts as a rheostat, whose stability is optimized to respond in a small temperature range around 37°C as occur within the upper airways during infection. Small increases in temperature gradually open up the structure to allow progressively increased access to the ribosome binding site. Even small changes in stability induced by mutations of imperfect base pairs, as in naturally occurring polymorphisms, shift the thermometer response outside of the desired temperature range, suggesting that its activity could be modulated by pharmacological intervention.

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  1. Applications of NMR to structure determination of RNAs large and small. Barnwal RP, Yang F, Varani G. Arch Biochem Biophys 628 42-56 (2017)
  2. Probing RNA structure in vivo. Mitchell D, Assmann SM, Bevilacqua PC. Curr Opin Struct Biol 59 151-158 (2019)
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  5. Extending the Applicability of Exact Nuclear Overhauser Enhancements to Large Proteins and RNA. Nichols PJ, Born A, Henen MA, Strotz D, Celestine CN, Güntert P, Vögeli B. Chembiochem (2018)
  6. Isotope-Labeled RNA Building Blocks for NMR Structure and Dynamics Studies. Olenginski LT, Taiwo KM, LeBlanc RM, Dayie TK. Molecules 26 5581 (2021)
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  8. Microbial Mechanisms of Heat Sensing. Samtani H, Unni G, Khurana P. Indian J Microbiol 62 175-186 (2022)

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  2. Glyoxals as in vivo RNA structural probes of guanine base-pairing. Mitchell D, Ritchey LE, Park H, Babitzke P, Assmann SM, Bevilacqua PC. RNA 24 114-124 (2018)
  3. In vivo RNA structural probing of uracil and guanine base-pairing by 1-ethyl-3-(3-dimethylaminopropyl)carbodiimide (EDC). Mitchell D, Renda AJ, Douds CA, Babitzke P, Assmann SM, Bevilacqua PC. RNA 25 147-157 (2019)
  4. An NMR-based approach reveals the core structure of the functional domain of SINEUP lncRNAs. Ohyama T, Takahashi H, Sharma H, Yamazaki T, Gustincich S, Ishii Y, Carninci P. Nucleic Acids Res 48 9346-9360 (2020)
  5. An unconventional RNA-based thermosensor within the 5' UTR of Staphylococcus aureus cidA. Hussein H, Fris ME, Salem AH, Wiemels RE, Bastock RA, Righetti F, Burke CA, Narberhaus F, Carroll RK, Hassan NS, Mohamed SA, Fahmy AS, Murphy ER. PLoS One 14 e0214521 (2019)
  6. Structure of the RNA Specialized Translation Initiation Element that Recruits eIF3 to the 5'-UTR of c-Jun. Walker MJ, Shortridge MD, Albin DD, Cominsky LY, Varani G. J Mol Biol 432 1841-1855 (2020)
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  8. Neisseria cinerea Expresses a Functional Factor H Binding Protein Which Is Recognized by Immune Responses Elicited by Meningococcal Vaccines. Lavender H, Poncin K, Tang CM. Infect Immun 85 e00305-17 (2017)
  9. SHAPE analysis of the htrA RNA thermometer from Salmonella enterica. Choi EK, Ulanowicz KA, Nguyen YAH, Frandsen JK, Mitton-Fry RM. RNA 23 1569-1581 (2017)
  10. Characterizing the Structure-Function Relationship of a Naturally Occurring RNA Thermometer. Meyer S, Carlson PD, Lucks JB. Biochemistry 56 6629-6638 (2017)
  11. An integrative NMR-SAXS approach for structural determination of large RNAs defines the substrate-free state of a trans-cleaving Neurospora Varkud Satellite ribozyme. Dagenais P, Desjardins G, Legault P. Nucleic Acids Res 49 11959-11973 (2021)
  12. The gatekeeper of Yersinia type III secretion is under RNA thermometer control. Pienkoß S, Javadi S, Chaoprasid P, Nolte T, Twittenhoff C, Dersch P, Narberhaus F. PLoS Pathog 17 e1009650 (2021)
  13. RNA thermosensors facilitate Streptococcus pneumoniae and Haemophilus influenzae immune evasion. Eichner H, Karlsson J, Spelmink L, Pathak A, Sham LT, Henriques-Normark B, Loh E. PLoS Pathog 17 e1009513 (2021)
  14. Structure of the dengue virus RNA promoter. Sun YT, Varani G. RNA 28 1210-1223 (2022)
  15. Multilayer Regulation of Neisseria meningitidis NHBA at Physiologically Relevant Temperatures. Borghi S, Antunes A, Haag AF, Spinsanti M, Brignoli T, Ndoni E, Scarlato V, Delany I. Microorganisms 10 834 (2022)
  16. Neisseria genes required for persistence identified via in vivo screening of a transposon mutant library. Rhodes KA, Ma MC, Rendón MA, So M. PLoS Pathog 18 e1010497 (2022)
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