ORCID

https://orcid.org/0009-0000-5536-5929

Date of Award

Fall 2024

Language

English

Embargo Period

10-6-2025

Document Type

Dissertation

Degree Name

Doctor of Philosophy (PhD)

College/School/Department

Department of Chemistry

Program

Chemistry

First Advisor

Alexander Shekhtman

Committee Members

Li Niu, Jia Sheng, Alex M. Valm

Keywords

Ribosome, Glycolysis, In-cell NMR, Quinary structure, Cross-linking mass spectrometry, Metabolic flux analysis

Subject Categories

Biochemistry | Biophysics

Abstract

Quinary interactions arise due to the extreme macromolecular crowding inside live cells. Quinary interactions affect intracellular protein stability, activity, and homeostasis. Ribosomes, traditionally known for their role in protein synthesis, have been found to engage in quinary interactions with metabolic enzymes, modulating their activity and thereby revealing a potential regulatory role for ribosomes in cellular metabolism. This phenomenon, termed the Ribosome-Amplified MetaBOlism (RAMBO) effect, was investigated in this dissertation through a series of in vitro and in vivo studies using primarily Nuclear Magnetic Resonance (NMR) spectroscopy.

Firstly, an NMR-based direct enzyme assay compatible with ribosome was developed and validated using pyruvate kinase (PYK) from Bacillus stearothermophilus as a probe. A high-quality Escherichia coli 70S ribosomes preparation was developed. Highly purified ribosomes were used to ensure that the observed amplification in enzyme activity was solely attributable to ribosomal interactions. Ribosomes were shown to significantly enhance the PYK activity and chemical cross-linking mass spectrometry (XL-MS) was used to identify key ribosomal binding sites of PYK, supporting the RAMBO effect.

Next, a general mechanism for the RAMBO effect was proposed and elucidated, where the ribosome external electric field (EEF)-substrate dipole interaction energy stabilizes transition states, significantly increasing the activity of triosephosphate isomerase (TPI) from Gallus gallus. NMR spectroscopy was performed to examine the quinary interaction surface of TPI binding to the ribosomes, and to access the TPI kinetic assay. XL-MS coupled with molecular docking were used to determine the potential TPI-ribosome binding conformations, providing structural models for the electric fields and substrate dipoles calculations. Ribosomal protein L11 was identified as the primary binding partner of TPI, confirming the origin of the RAMBO effect.

Finally, the in vivo RAMBO effect was studied in the context of glycolysis in E. coli using real-time pulse chase (RTPC)-NMR. The activity of pyruvate kinase I (PYFK) from E. coli was significantly enhanced in the presence of ribosomes, but this ribosome-mediated amplification was disrupted by the addition of ribosomal antibiotics in vitro. Kinetic flux profiling (KFP) further demonstrated the RAMBO effect observed in vitro also occurs in live cells, thereby confirming the role of ribosomes metabolic regulation and validating the RAMBO hypothesis.

License

Creative Commons Attribution 4.0 International License
This work is licensed under a Creative Commons Attribution 4.0 International License.

Available for download on Monday, October 06, 2025

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