Molecular Control of Bacterial Death and Lysis

Rice, Kelly C.; Bayles, Kenneth W.

doi:10.1128/mmbr.00030-07

Cited by 320 publications

(335 citation statements)

References 287 publications

(413 reference statements)

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“…(6) Both proteins were shown to permeabilize liposomes in a reconstituted in vitro system (Smith et al 1998;Saito et al 2000;Kuwana et al 2002). (7) Both are inhibited by closely related endogenous proteins: Bcl-xL and anti-holin, respectively (Wang et al 2000;Rice and Bayles 2008). It is worth noting, however, that Bax/Bak showed at least one difference from a typical holin.…”

Section: Active Bax and Bak As Functional Holins Mechanistically Linmentioning

confidence: 99%

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Active Bax and Bak are functional holins

Pang¹,

Moussa²,

Targy³

et al. 2011

Genes Dev.

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The mechanism of Bax/Bak-dependent mitochondrial outer membrane permeabilization (MOMP), a central apoptotic event primarily controlled by the Bcl-2 family proteins, remains not well understood. Here, we express active Bax/Bak in bacteria, the putative origin of mitochondria, and examine their functional similarities to the l bacteriophage (l) holin. As critical effectors for bacterial lysis, holin oligomers form membrane lesions, through which endolysin, a muralytic enzyme, escapes the cytoplasm to attack the cell wall at the end of the infection cycle. We found that active Bax/Bak, but not any other Bcl-2 family protein, displays holin behavior, causing bacterial lysis by releasing endolysin in an oligomerization-dependent manner. Strikingly, replacing the holin gene with active alleles of Bax/Bak results in plaque-forming phages. Furthermore, we provide evidence that active Bax produces large membrane holes, the size of which is controlled by structural elements of Bax. Notably, lysis by active Bax is inhibited by Bcl-xL, and the lysis activity of the wild-type Bax is stimulated by a BH3-only protein.Together, these results mechanistically link MOMP to holin-mediated hole formation in the bacterial plasma membrane.

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Section: Active Bax and Bak As Functional Holins Mechanistically Linmentioning

confidence: 99%

“…oligomers, and produces membrane holes large enough for the nonspecific passage of endolysin (Wang et al 2000;Bayles 2007;Rice and Bayles 2008). Once across the cell membrane, the endolysin degrades the cell wall, causing an explosive disruption of the cell due to osmotic forces (Grundling et al 2001).…”

mentioning

confidence: 99%

Active Bax and Bak are functional holins

Pang¹,

Moussa²,

Targy³

et al. 2011

Genes Dev.

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“…To demonstrate the potential of using orthogonal riboregulators to rapidly kill bacterial cells through AND gate logic, we used the λ-phage lysis genes: λR, λR Z , and λS (44). λR, an endolysin, and λR Z , an endopeptidase, degrade peptidoglycan (PG) but cannot access the PG layer without the holin λS permeabilizing the inner membrane (45).…”

Section: Resultsmentioning

confidence: 99%

Tracking, tuning, and terminating microbial physiology using synthetic riboregulators

Callura

Dwyer

Isaacs

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

173

162

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The development of biomolecular devices that interface with biological systems to reveal new insights and produce novel functions is one of the defining goals of synthetic biology. Our lab previously described a synthetic, riboregulator system that affords for modular, tunable, and tight control of gene expression in vivo. Here we highlight several experimental advantages unique to this RNA-based system, including physiologically relevant protein production, component modularity, leakage minimization, rapid response time, tunable gene expression, and independent regulation of multiple genes. We demonstrate this utility in four sets of in vivo experiments with various microbial systems. Specifically, we show that the synthetic riboregulator is well suited for GFP fusion protein tracking in wildtype cells, tight regulation of toxic protein expression, and sensitive perturbation of stress response networks. We also show that the system can be used for logic-based computing of multiple, orthogonal inputs, resulting in the development of a programmable kill switch for bacteria. This work establishes a broad, easy-to-use synthetic biology platform for microbiology experiments and biotechnology applications. S ynthetic biology seeks to reprogram organisms to alter natural biological behavior or perform novel functions, using engineered gene circuits, pathways, and whole genomes (1-8). Engineered gene circuits, in this regard, are typically constructed by assembling well-characterized biological components into unique architectures to achieve these unnatural capabilities, which are commonly used in biotechnology applications. A need also exists for synthetic biomolecular devices that interface with endogenous systems to track, probe, and influence, rather than reprogram, cellular physiology. Synthetic gene expression platforms that could accomplish this task would be well suited for use in a wide variety of phenotypic and genetic analyses aimed at expanding our knowledge of natural biomolecular components and networks, as well as enhancing our understanding of network dynamics under an array of conditions.In this work, we showcase an engineered riboregulator system that controls gene expression posttranscriptionally through highly specific RNA-RNA interactions (9). RNA molecules are useful components in synthetic biomolecular devices (10, 11) due to their large sequence space, the number of unique structures that can be adopted, the predictability of structure stability, and the range of functions enabled by these structures. Together, these features make RNA molecules ideal for interfacing with biological systems given that they can be used to control gene expression, sense biomolecules, and serve as foundational devices that can perform complex cellular behavior. As such, the engineered, RNA-based device space is remarkably diverse. Other successful examples include independent transcription-translation networks based on orthogonal mRNA-ribosome pairs (12), riboswitches in which RNA aptamers directly control translati...

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“…2 of biofilms in various organisms. [22] Regulated bacterial cell death and lysis in S. aureus is favoured by an enzyme murein hydrolase. [22] This enzyme targets cleavage of cell wall peptidoglycans and has shown to take part in cell growth, cell division, separation of daughter cells, peptidoglycan recycling and regulated cell lysis.…”

Section: Holin-like Protein (Cidabc) Operonmentioning

confidence: 99%

“…[22] Regulated bacterial cell death and lysis in S. aureus is favoured by an enzyme murein hydrolase. [22] This enzyme targets cleavage of cell wall peptidoglycans and has shown to take part in cell growth, cell division, separation of daughter cells, peptidoglycan recycling and regulated cell lysis. [22] The regulation of murein hydrolase activity is favoured by cid operon which acts as an effector by encoding holin-like proteins.…”

Section: Holin-like Protein (Cidabc) Operonmentioning

confidence: 99%

Revamping the role of biofilm regulating operons in device-associated Staphylococci and Pseudomonas aeruginosa

Halebeedu

Kumar

Gopal

2014

Indian Journal of Medical Microbiology

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Extensive use of indwelling devices in modern medicine has revoked higher incidence of device associated infections and most of these devices provide an ideal surface for microbial attachment to form strong biofilms. These obnoxious biofilms are responsible for persistent infections, longer hospitalization and high mortality rate. Gene regulations in bacteria play a significant role in survival, colonization and pathogenesis. Operons being a part of gene regulatory network favour cell colonization and biofilm formation in various pathogens. This review explains the functional role of various operons in biofilm expression and regulation observed in device-associated pathogens such as Staphylococcus aureus, Staphylococcus epidermidis and Pseudomonas aeruginosa.

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Molecular Control of Bacterial Death and Lysis

Cited by 320 publications

References 287 publications

Active Bax and Bak are functional holins

Active Bax and Bak are functional holins

Tracking, tuning, and terminating microbial physiology using synthetic riboregulators

Revamping the role of biofilm regulating operons in device-associated Staphylococci and Pseudomonas aeruginosa

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