Characterization of molecular interactions between <i>Escherichia coli </i><scp>RNA</scp> polymerase and topoisomerase I by molecular simulations

Tiwari, Purushottam; Chapagain, Prem P.; Banda, Srikanth; Darici, Yesim; Üren, Aykut; Tse‐Dinh, Yuk‐Ching

doi:10.1002/1873-3468.12321

Cited by 17 publications

(27 citation statements)

References 39 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Molecular simulations predicted that salt bridges and hydrogen bonds formed by basic residues positioned over a large molecular surface formed by the zinc ribbon motifs of E. coli TopoI are responsible for interactions with acidic residues in RNAP 16 . In contrast, a distinct mode of protein-protein interaction utilizing a short stretch of C-terminal tail is employed instead for the TopoI-RNAP interaction in bacteria that do not have Zn(II) binding TopoI-CTD.…”

Section: Discussionmentioning

confidence: 99%

“…It was previously reported that the E. coli RNA polymerase β′ subunit interacts directly with the zinc ribbon and zinc ribbon-like C-terminal domains (CTD) of topoisomerase I 15, 16 . In E. coli and most bacterial species, the CTD of topoisomerase I have multiple zinc ribbon domains, each with a Zn(II) ion coordinated by four cysteines 17–19 .…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Distinct Mechanism Evolved for Mycobacterial RNA Polymerase and Topoisomerase I Protein–Protein Interaction

Banda

Cao

Tse‐Dinh

2017

Journal of Molecular Biology

Self Cite

View full text Add to dashboard Cite

We report here a distinct mechanism of interaction between topoisomerase I and RNA polymerase in Mycobacterium tuberculosis and Mycobacterium smegmatis that has evolved independently from the previously characterized interaction between bacterial topoisomerase I and RNA polymerase. Bacterial DNA topoisomerase I is responsible for preventing the hyper-negative supercoiling of genomic DNA. The association of topoisomerase I with RNA polymerase during transcription elongation could efficiently relieve transcription-driven negative supercoiling. Our results demonstrate a direct physical interaction between the C-terminal domains of topoisomerase I (TopoI-CTD) and the β′ subunit of RNA polymerase of M. smegmatis in the absence of DNA. The TopoI-CTD in mycobacteria are evolutionarily unrelated in amino acid sequence and three-dimensional structure to the TopoI-CTD found in the majority of bacterial species outside Actinobacteria, including Escherichia coli. The functional interaction between topoisomerase I and RNA polymerase has evolved independently in mycobacteria and E. coli, with distinctively different structural elements of TopoI-CTD utilized for this protein-protein interaction. Zinc ribbon motifs in E. coli TopoI-CTD are involved in the interaction with RNA polymerase. For M. smegmatis TopoI-CTD, a 27 amino acid tail that is rich in basic residues at the C-terminal end is responsible for the interaction with RNA polymerase. Overexpression of recombinant TopoI-CTD in M. smegmatis competed with the endogenous topoisomerase I for protein-protein interactions with RNA polymerase. The TopoI-CTD overexpression resulted in decreased survival following treatment with antibiotics and hydrogen peroxide, supporting the importance of the protein-protein interaction between topoisomerase I and RNA polymerase during stress response of mycobacteria.

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Distinct Mechanism Evolved for Mycobacterial RNA Polymerase and Topoisomerase I Protein–Protein Interaction

Banda

Cao

Tse‐Dinh

2017

Journal of Molecular Biology

Self Cite

View full text Add to dashboard Cite

show abstract

“…ChIP-seq experiments have not yet been performed to map genome-wide topo I binding and cleavage sites on the chromosome of E. coli. Because topo I physically interacts with RNAP [40,41], these sites are expected to be largely determined by transcription. In fact, the full-length complete structure of topo I recently reported demonstrates how the C-terminal domain binds ssDNA to recognize the accumulation of negative supercoils and how this domain allows the rapid removal of transcription-induced negative supercoiling [42].…”

Section: Viability Of Single Topa Null Mutants and The Role Of Topo Imentioning

confidence: 99%

Supercoiling, R-Loops, Replication and the Functions of Bacterial Type 1A Topoisomerases

Brochu

Breton

Drolet

2020

Genes

View full text Add to dashboard Cite

Type 1A topoisomerases (topos) are the only topos that bind single-stranded DNA and the only ones found in all cells of the three domains of life. Two subfamilies, topo I and topo III, are present in bacteria. Topo I, found in all of them, relaxes negative supercoiling, while topo III acts as a decatenase in replication. However, recent results suggest that they can also act as back-up for each other. Because they are ubiquitous, type 1A enzymes are expected to be essential for cell viability. Single topA (topo I) and topB (topo III) null mutants of Escherichia coli are viable, but for topA only with compensatory mutations. Double topA topB null mutants were initially believed to be non-viable. However, in two independent studies, results of next generation sequencing (NGS) have recently shown that double topA topB null mutants of Bacillus subtilis and E. coli are viable when they carry parC parE gene amplifications. These genes encode the two subunits of topo IV, the main cellular decatenase. Here, we discuss the essential functions of bacterial type 1A topos in the context of this observation and new results showing their involvement in preventing unregulated replication from R-loops.

show abstract

“…It was previously reported that E. coli RNA polymerase beta' subunit interacts directly with the zinc ribbon and zinc ribbon-like C-terminal domains (CTD) of topoisomerase I (Cheng et al, 2003;Tiwari et al, 2016). In E. coli and most bacterial species, the CTD of topoisomerase I have multiple zinc ribbon domains, each with a Zn(II) ion coordinated by four cysteines (Tse-Dinh et al, 1988;Suerbaum et al, 1998;Grishin, 2000).…”

Section: Discussionmentioning

confidence: 99%

“…Resonance could be used for obtaining the kinetic parameters of the physical interaction between proteins (Pierce et al, 1999;Tiwari et al, 2016). However, these methods require large amounts of protein, and are expensive.…”

Section: Physical Interactions Between Rna Polymerase Beta' Subunit Amentioning

confidence: 99%

Protein-protein Interactions of Bacterial Topoisomerase I

Banda¹

Self Cite

View full text Add to dashboard Cite

show abstract

Characterization of molecular interactions between Escherichia coli RNA polymerase and topoisomerase I by molecular simulations

Cited by 17 publications

References 39 publications

Distinct Mechanism Evolved for Mycobacterial RNA Polymerase and Topoisomerase I Protein–Protein Interaction

Distinct Mechanism Evolved for Mycobacterial RNA Polymerase and Topoisomerase I Protein–Protein Interaction

Supercoiling, R-Loops, Replication and the Functions of Bacterial Type 1A Topoisomerases

Protein-protein Interactions of Bacterial Topoisomerase I

Contact Info

Product

Resources

About