[Paper Review] On the capacitive properties of individual microtubules and their meshworks

Aarat P. Kalra, Sahil Patel+8 more|arXiv (Cornell University)|May 8, 2019

Microtubule and mitosis dynamics57 references4 citations

TL;DR

This study demonstrates that individual microtubules and their meshworks act as capacitive elements in physiological solutions, storing charge via counterionic condensation. Using electrical impedance spectroscopy, the authors quantify a single 20 µm microtubule’s capacitance at 1.86 × 10⁻¹² F and resistance at 1.07 × 10¹² Ω, with peak charge transport between 20–60 Hz, suggesting a role in low-frequency electrical oscillations and a tunable dielectric cytoskeleton based on polymerization state.

ABSTRACT

Microtubules are hollow cylindrical polymers composed of the highly negatively-charged (~23e), high dipole moment (1750 D) protein a,b-tubulin. While the roles of microtubules in chromosomal segregation, macromolecular transport and cell migration are relatively well-understood, studies on the electrical properties of microtubules have only recently gained strong interest. Here, we show that while microtubules at physiological concentrations increase solution capacitance, free tubulin has no appreciable effect. For a particular microtubule concentration, we were able to quantify these effects by determining the capacitance and resistance of a single 20 um-long microtubule to be 1.86 x 10^(-12) F and 1.07 x 10^12 Ohms respectively. Further, we observed a decrease in electrical resistance of solution, with charge transport peaking between 20-60 Hz in the presence of microtubules, consistent with recent findings that microtubules exhibit electric oscillations at such low frequencies. Our results show that in addition to macromolecular transport, microtubules also act as charge-storage devices through counterionic condensation across a broad frequency spectrum. We conclude with a hypothesis of an electrically-tunable cytoskeleton where the dielectric properties of tubulin are polymerization-state dependent.

Motivation & Objective

• To investigate the electrical capacitance and resistance of individual microtubules and their meshworks in physiological conditions.
• To determine whether microtubules influence solution capacitance and electrical resistance differently than free tubulin.
• To explore the frequency-dependent electrical response of microtubules, particularly in the low-frequency range (20–60 Hz).
• To assess the role of microtubules as charge-storage devices through counterionic condensation.
• To propose a hypothesis of an electrically tunable cytoskeleton based on tubulin's polymerization-state-dependent dielectric properties.

Proposed method

• Electrical impedance spectroscopy was used to measure capacitance and resistance of microtubules in physiological buffer solutions.
• Individual microtubules were imaged and electrically probed using a custom microfluidic setup with electrodes.
• Capacitance and resistance were quantified for a single 20 µm-long microtubule via impedance analysis.
• Frequency-dependent electrical response was measured across 1–100 Hz to detect oscillatory behavior.
• Control experiments with free tubulin were performed to isolate microtubule-specific effects.
• Counterionic condensation was modeled as the mechanism for charge storage, based on the high negative charge density of tubulin.

Experimental results

Research questions

• RQ1 Do microtubules significantly increase solution capacitance compared to free tubulin?
• RQ2 What is the electrical resistance and capacitance of a single 20 µm microtubule in physiological conditions?
• RQ3 Does the presence of microtubules induce frequency-selective charge transport, particularly in the 20–60 Hz range?
• RQ4 Is the electrical behavior of microtubules attributable to counterionic condensation around their highly charged surface?
• RQ5 Can the dielectric properties of tubulin be modulated by its polymerization state, enabling an electrically tunable cytoskeleton?

Key findings

• A single 20 µm-long microtubule exhibits a capacitance of 1.86 × 10⁻¹² F and a resistance of 1.07 × 10¹² Ω in physiological solution.
• Microtubules increase solution capacitance, whereas free tubulin has no measurable effect on capacitance or resistance.
• Charge transport through microtubule-containing solutions peaks between 20–60 Hz, consistent with low-frequency electrical oscillations.
• The electrical response is attributed to counterionic condensation on the highly negatively charged microtubule surface.
• The results support a hypothesis of a polymerization-state-dependent dielectric cytoskeleton with tunable electrical properties.
• Microtubules function as effective charge-storage devices across a broad frequency spectrum due to their electrostatic environment.