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Hydrophobic-cationic peptides modulate RNA polymerase ribozyme activity by accretion

Author

Listed:
  • Peiying Li

    (RIKEN Center for Biosystems Dynamics Research)

  • Philipp Holliger

    (MRC Laboratory of Molecular Biology, Francis Crick Avenue, Cambridge Biomedical Campus)

  • Shunsuke Tagami

    (RIKEN Center for Biosystems Dynamics Research
    MRC Laboratory of Molecular Biology, Francis Crick Avenue, Cambridge Biomedical Campus)

Abstract

Accretion and the resulting increase in local concentration is a widespread mechanism in biology to enhance biomolecular functions (for example, in liquid-liquid demixing phases). Such macromolecular aggregation phases (e.g., coacervates, amyloids) may also have played a role in the origin of life. Here, we report that a hydrophobic-cationic RNA binding peptide selected by phage display (P43: AKKVWIIMGGS) forms insoluble amyloid-containing aggregates, which reversibly accrete RNA on their surfaces in an RNA-length and Mg2+-concentration dependent manner. The aggregates formed by P43 or its sequence-simplified version (K2V6: KKVVVVVV) inhibited RNA polymerase ribozyme (RPR) activity at 25 mM MgCl2, while enhancing it significantly at 400 mM MgCl2. Our work shows that such hydrophobic-cationic peptide aggregates can reversibly concentrate RNA and enhance the RPR activity, and suggests that they could have aided the emergence and evolution of longer and functional RNAs in the fluctuating environments of the prebiotic earth.

Suggested Citation

  • Peiying Li & Philipp Holliger & Shunsuke Tagami, 2022. "Hydrophobic-cationic peptides modulate RNA polymerase ribozyme activity by accretion," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30590-3
    DOI: 10.1038/s41467-022-30590-3
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    1. Moran Frenkel-Pinter & Jay W. Haynes & Ahmad M. Mohyeldin & Martin C & Alyssa B. Sargon & Anton S. Petrov & Ramanarayanan Krishnamurthy & Nicholas V. Hud & Loren Dean Williams & Luke J. Leman, 2020. "Mutually stabilizing interactions between proto-peptides and RNA," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    2. Pierre Canavelli & Saidul Islam & Matthew W. Powner, 2019. "Peptide ligation by chemoselective aminonitrile coupling in water," Nature, Nature, vol. 571(7766), pages 546-549, July.
    3. Raghav R. Poudyal & Rebecca M. Guth-Metzler & Andrew J. Veenis & Erica A. Frankel & Christine D. Keating & Philip C. Bevilacqua, 2019. "Template-directed RNA polymerization and enhanced ribozyme catalysis inside membraneless compartments formed by coacervates," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    4. Saroj K. Rout & Michael P. Friedmann & Roland Riek & Jason Greenwald, 2018. "A prebiotic template-directed peptide synthesis based on amyloids," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    5. James Attwater & Aniela Wochner & Vitor B. Pinheiro & Alan Coulson & Philipp Holliger, 2010. "Ice as a protocellular medium for RNA replication," Nature Communications, Nature, vol. 1(1), pages 1-9, December.
    6. Björn Drobot & Juan M. Iglesias-Artola & Kristian Vay & Viktoria Mayr & Mrityunjoy Kar & Moritz Kreysing & Hannes Mutschler & T-Y Dora Tang, 2018. "Compartmentalised RNA catalysis in membrane-free coacervate protocells," Nature Communications, Nature, vol. 9(1), pages 1-9, December.
    7. Marc Rodriguez-Garcia & Andrew J. Surman & Geoffrey J.T. Cooper & Irene Suárez-Marina & Zied Hosni & Michael P. Lee & Leroy Cronin, 2015. "Formation of oligopeptides in high yield under simple programmable conditions," Nature Communications, Nature, vol. 6(1), pages 1-7, December.
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