Award Date

12-15-2025

Degree Type

Dissertation

Degree Name

Doctor of Philosophy (PhD)

Department

Life Sciences

First Committee Member

Helen Wing

Second Committee Member

Boo Shan Tseng

Third Committee Member

Christy Strong

Fourth Committee Member

Rajeev Misra

Fifth Committee Member

Ronald Gary

Number of Pages

328

Abstract

Shigella species are the causative agents of bacillary dysentery and the second leading cause of diarrheal death worldwide. In Shigella, many of the virulence genes are encoded on a large virulence plasmid. Outside of the host, at 30 °C, the expression of virulence genes is silenced by the histone-like nucleoid structuring protein, H-NS. Upon host entry, a temperature shift to 37 °C triggers the production of VirB, a key virulence gene regulator that counteracts H-NS-mediated silencing through a process known as anti-silencing. Interestingly, VirB is not related to other transcriptional regulators; instead, it is an unusual member of the ParB superfamily. Recent work on members of the ParB superfamily found that several ParB proteins bind the nucleoside triphosphate ligand, CTP, and function as CTPases to properly segregate DNA prior to cell division. This posed the question of whether VirB, which serves a different cellular role, binds CTP or possibly another NTP ligand. Therefore, the goal of my dissertation was to determine if VirB binds CTP or another NTP and, if so, what role this NTP ligand plays in the mechanism of VirB-dependent anti-silencing.

In this work, I determined that VirB binds CTP preferentially and with specificity using ITC and DRaCALA. Further characterization of the importance of CTP binding for VirB function revealed that CTP is essential for the regulatory activities of VirB, including VirB-dependent anti-silencing. While we know that CTP binding by VirB is required for VirB-dependent anti-silencing, the role that CTP plays in the mechanism of VirBdependent anti-silencing remains unclear. Prior to the discovery of CTP, it was well- iv established that the mechanism of VirB-dependent anti-silencing relies on i) specific engagement with the VirB binding site, ii) the formation of large VirB-DNA complexes, and iii) the modulation of DNA supercoiling. Thus, I tested the requirement for CTP at each of these steps. My work demonstrates that CTP binding by VirB is not required for specific engagement with the VirB binding site; however, CTP is necessary for the formation of large VirB-DNA complexes and the modulation of DNA supercoiling. This would support a model where, following CTP binding and DNA binding site engagement, VirB undergoes a DNA sliding clamp conformation, in which the DNA falls into the lumen of the protein, much like beads on a string.

Based on these findings, we had an additional question about how VirB is removed from the DNA once it is in a closed DNA sliding clamp conformation. Because ParB proteins hydrolyze CTP to be recycled off the DNA, we wanted to determine if VirB also hydrolyzes CTP. My colleague and I demonstrate that VirB hydrolyzes CTP in a site-dependent manner but does so at rates approximately four times slower than Caulobacter vibrioides ParB. Using a suite of VirB mutant derivatives likely involved in CTP hydrolysis, we demonstrate that while VirB Q47A, Q54A, T92A, and Q127A all retain CTP and DNA binding activities, VirB Q54A, T92A, and Q127A all displayed defects in their ability to interfere with a constitutively active promoter, modulate DNA supercoiling, and anti-silence Shigella virulence genes; three activities that rely on VirB remaining associated with the DNA. VirB Q47A, however, retains wild-type levels in all three activities, with the exception that VirB Q47A displayed increased anti-silencing activity when the VirB binding site is repositioned 3600 bp further upstream. These findings start to suggest that CTP hydrolysis by VirB plays an important role in VirB- v dependent anti-silencing, where CTP hydrolysis rates may dictate the DNA residence time of VirB.

Lastly, I investigated whether VirB requires a DNA-binding partner to hydrolyze CTP more efficiently. My data identified two proteins, ProP and Protein X, as potential VirB binding partners. Subsequent in silico modelling of a potential interaction between VirB and each protein revealed that Protein X displayed a moderate interaction score suggestive of an interaction. In sum, my dissertation work significantly increases our understanding of the mechanism of VirB-dependent anti-silencing and provides insight into CTP as an important ligand for Shigella virulence.

Keywords

bacterial pathogen; DNA-supercoiling; ParB; Protein-DNA interactions; virulence gene regulation

Disciplines

Biochemistry | Microbiology | Molecular Biology

File Format

PDF

File Size

12600 KB

Degree Grantor

University of Nevada, Las Vegas

Language

English

Rights

IN COPYRIGHT. For more information about this rights statement, please visit http://rightsstatements.org/vocab/InC/1.0/

Available for download on Wednesday, December 15, 2032


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