IonoBiology: The functional dynamics of the intracellular metallome, with lessons from bacteria

Galera-Laporta, Leticia; Comerci, Colin J.; García-Ojalvo, Jordi; Süel, Gürol M.

doi:10.1016/j.cels.2021.04.011

Cited by 24 publications

(18 citation statements)

References 118 publications

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“…In principle, the transcription, translation, and post-translational gating of these ion channel and junction proteins are amenable to external modulation and future therapeutic strategies [ 3 , 12 , 13 , 15 , 45 , 56 , 62 , 63 , 64 , 65 , 66 , 67 , 68 , 69 , 70 , 71 ]. Consequently, the bioelectrical patterns and their encoded information could be externally regulated by acting on multicellular mean field phenomena such as electrical potential, potassium, and calcium waves [ 3 , 4 , 5 , 9 , 72 , 73 ] as a complementary procedure to addressing individual cell characteristics. In this context, the intercellular gap junctions can offer future opportunities [ 10 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 74 , 75 ].…”

Section: Discussionmentioning

confidence: 99%

Cell Systems Bioelectricity: How Different Intercellular Gap Junctions Could Regionalize a Multicellular Aggregate

Riol

Cervera

Levin

et al. 2021

Cancers

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Electric potential distributions can act as instructive pre-patterns for development, regeneration, and tumorigenesis in cell systems. The biophysical states influence transcription, proliferation, cell shape, migration, and differentiation through biochemical and biomechanical downstream transduction processes. A major knowledge gap is the origin of spatial patterns in vivo, and their relationship to the ion channels and the electrical synapses known as gap junctions. Understanding this is critical for basic evolutionary developmental biology as well as for regenerative medicine. We computationally show that cells may express connexin proteins with different voltage-gated gap junction conductances as a way to maintain multicellular regions at distinct membrane potentials. We show that increasing the multicellular connectivity via enhanced junction function does not always contribute to the bioelectrical normalization of abnormally depolarized multicellular patches. From a purely electrical junction view, this result suggests that the reduction rather than the increase of specific connexin levels can also be a suitable bioelectrical approach in some cases and time stages. We offer a minimum model that incorporates effective conductances ultimately related to specific ion channel and junction proteins that are amenable to external regulation. We suggest that the bioelectrical patterns and their encoded instructive information can be externally modulated by acting on the mean fields of cell systems, a complementary approach to that of acting on the molecular characteristics of individual cells. We believe that despite the limitations of a biophysically focused model, our approach can offer useful qualitative insights into the collective dynamics of cell system bioelectricity.

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Section: Discussionmentioning

confidence: 99%

Cell Systems Bioelectricity: How Different Intercellular Gap Junctions Could Regionalize a Multicellular Aggregate

Riol

Cervera

Levin

et al. 2021

Cancers

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“…Then, e n ∼ e∆n (1) rms C ≈ 3.5 V, with ∆n In the second, we estimate e n from fluctuations in the intracellular ion concentrations. We assume that the ions are distributed uniformly inside (and outside) the cell and that only K + , Na + , and Cl − ions contribute to the steady-state value of V mem .…”

Section: Estimation Of the Membrane Potential Noisementioning

confidence: 99%

“…where R is the universal gas constant, T is the temperature, F is Faraday's constant; p X is the relative membrane permeability, and [X] i and [X] o are the uniform intracellular and extracellular concentrations of the ion. The rms fluctuations in intracellular ion concentration for each ion is estimated to be of order, ∆[X] i ∼ ∆n (1) rms V b ∼ 10 24 m −3 , for a cell with volume V b ∼ 10 −18 m 3 [12]. The extracellular ion concentrations are assumed to remain constant.…”

Section: Estimation Of the Membrane Potential Noisementioning

confidence: 99%

“…Bacteria create and maintain transmembrane concentration gradients of small metal ions, such as potassium and sodium [1,2]. These ionic concentration gradients are the main source of the electrical and electrochemical potentials that are present across the cell membrane and facilitate a number of crucial cellular processes [3][4][5][6][7][8][9].…”

Section: Introductionmentioning

confidence: 99%

“…It has been suggested that these charge fluctuations are purposeful, but little is known about their downstream effects. Thus, bacterial ion homeostasis is expected to be highly dynamic [1] and dominated by strong charge noise. At the present time, quantitative measurements of electrical fluctuations and noise models of single bacterial cells are missing from the biophysics literature, partly due to a lack of sensitive tools on the size scale of a bacterium [14].…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Measurement of the Low-Frequency Charge Noise of Bacteria

Yang,

Gress,

Ekinci

2022

Preprint

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Bacteria meticulously regulate their intracellular ion concentrations and create ionic concentration gradients across the bacterial membrane. These ionic concentration gradients provide free energy for many cellular processes and are maintained by transmembrane transport. Given the physical dimensions of a bacterium and the stochasticity in transmembrane transport, intracellular ion concentrations and hence the charge state of a bacterium are bound to fluctuate. Here, we investigate the charge noise of 100s of non-motile bacteria by combining electrical measurement techniques from condensed matter physics with microfluidics. In our experiments, bacteria in a microchannel generate charge density fluctuations in the embedding electrolyte due to random influx and efflux of ions. Detected as electrical resistance noise, these charge density fluctuations display a power spectral density proportional to 1/f 2 for frequencies 0.05 Hz ≤ f ≤ 1 Hz. Fits to a simple noise model suggest that the steady-state charge of a bacterium fluctuates by ±1.30 × 10 6 e (e ≈ 1.60 × 10 −19 C), indicating that bacterial ion homeostasis is highly dynamic and dominated by strong charge noise. The rms charge noise can then be used to estimate the fluctuations in the membrane potential; however, the estimates are unreliable due to our limited understanding of the intracellular concentration gradients.

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Membrane Targeted Azobenzene Drives Optical Modulation of Bacterial Membrane Potential

Bondelli

Grobas²,

Donini

et al. 2023

Advanced Science

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Recent studies have shown that bacterial membrane potential is dynamic and plays signaling roles. Yet, little is still known about the mechanisms of membrane potential dynamics regulation-owing to a scarcity of appropriate research tools. Optical modulation of bacterial membrane potential could fill this gap and provide a new approach for studying and controlling bacterial physiology and electrical signaling. Here, the authors show that a membrane-targeted azobenzene (Ziapin2) can be used to photo-modulate the membrane potential in cells of the Gram-positive bacterium Bacillus subtilis. It is found that upon exposure to blue-green light (𝝀 = 470 nm), isomerization of Ziapin2 in the bacteria membrane induces hyperpolarization of the potential. To investigate the origin of this phenomenon, ion-channel-deletion strains and ion channel blockers are examined. The authors found that in presence of the chloride channel blocker idanyloxyacetic acid-94 (IAA-94) or in absence of KtrAB potassium transporter, the hyperpolarization response is attenuated. These results reveal that the Ziapin2 isomerization can induce ion channel opening in the bacterial membrane and suggest that Ziapin2 can be used for studying and controlling bacterial electrical signaling. This new optical tool could contribute to better understand various microbial phenomena, such as biofilm electric signaling and antimicrobial resistance.

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IonoBiology: The functional dynamics of the intracellular metallome, with lessons from bacteria

Cited by 24 publications

References 118 publications

Cell Systems Bioelectricity: How Different Intercellular Gap Junctions Could Regionalize a Multicellular Aggregate

Cell Systems Bioelectricity: How Different Intercellular Gap Junctions Could Regionalize a Multicellular Aggregate

Measurement of the Low-Frequency Charge Noise of Bacteria

Membrane Targeted Azobenzene Drives Optical Modulation of Bacterial Membrane Potential

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