Electrotaxis

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Electrotaxis, also known as galvanotaxis, is the directed motion of biological cells or organisms guided by an electric field or current. [1] The directed motion of electrotaxis can take many forms, such as; growth, development, active swimming, and passive migration. [1] [2] A wide variety of biological cells can naturally sense and follow DC electric fields. Such electric fields arise naturally in biological tissues during development and healing. [3] [4] These and other observations have led to research into how applied electric fields can impact wound healing [5] [6] [7] An increase in wound healing rate is regularly observed and this is thought to be due to the cell migration and other signaling pathways that are activated by the electric field. [8] Additional research has been conducted into how applied electric fields impact cancer metastasis, morphogenesis, neuron guidance, motility of pathogenic bacteria, biofilm formation, and many other biological phenomena. [2] [9] [10] [11]

Contents

History

In 1889, German physiologist Max Verworn applied a low-level direct current to a mixture of bacterial species and observed that some moved toward the anode and others moved to the cathode. [12] Two years later, in 1891, Belgian microscopist E. Dineur made the first known report of vertebrate cells migrating directionally in a direct current, a phenomenon which he coined galvanotaxis. [13] Dineur used a zinc–copper cell to apply a constant current to the abdominal cavity of a frog via a pair of platinum electrodes. He found that inflammatory leukocytes aggregated at the negative electrode. Since these pioneering studies, a variety of different cell types and organisms have been shown to respond to electric fields. [10]

Mechanism

Understanding of the underlying mechanisms that cause electrotaxis to occur is limited. The diversity of biological cells and environmental conditions make it likely that there are many different mechanisms that allow for cells to migrate due to electric fields. Some studies have indicated that certain organisms move passively without any specific sensing mechanisms applied to alter active motility. [14] [15]

Bacteria

In a sufficiently strong electric field, small cells may move as uniformly charged particles [16] or dipoles. [17] Other research reports suggest that bacteria cells might perceive local electric fields via chemotaxis. [18] [19] [20] This is done by sensing redox molecules that have formed a gradient relative to the poised electrical surface in the local environment.

Mammalian cells

The method of detection of a field in mammalian cells is under active investigation and might involve several mechanisms. For now, it is thought that redistribution of membrane-bound sensors dragged by Coulombic forces and electro-osmosis at the membrane would cause the cell to polarize, then migrate. [21] Mathematical modeling suggests that a 6-10% change in sensor concentration across the cell is detectable. [22] Experiments that repeatedly changed orientation of a field applied to several cell lines suggest that sensor polarization occurs on a relatively rapid timescale, perhaps several seconds, compared to the cell migration response, which is observed after 5-10 minutes. [23] This allows cells to time-average changes in the direction of the electric field before migrating. [23]

Evidence for a mechanism

There has been no discovery of a single mechanism or process by which all cells undergo electrotaxis. [24] However, multiple explanations have been investigated, resulting in a considerable body of evidence and a limited understanding of how cells migrate using electric fields. Electrotaxis is thought to operate based on changes in Ca2+ concentration produced by direct-current electric fields (dcEFs) due to the fact that exposure to dcEFs can cause concentration changes in excess of 1 millimolar. Additionally, calcium channel inhibition using Co2+ or D600 was observed to prevent electotaxis in most cases. [25] Cells that exhibit electrotaxis undergo an influx of Ca2+ ions on the anodal side of the cell, and simultaneous decrease in concentration on that cathodal side. This rearrangement is thought to create "push-pull" forces that induce net movement in the cathodal direction. However, this process would be more complicated in cells with intercellular calcium stores or voltage-gated calcium channels. In addition, voltage-gated sodium channels, protein kinases, growth factors, surface charge, and protein electrophoresis have been observed to have a role in electrotaxis. [25] However, there is no knowledge of a sensor molecule used specifically for electrotaxis. [26] The exact role and function of these and other cellular components in electrotaxis is not fully understood and is the basis of ongoing research. [25]

Signaling pathways used in electrotaxis

In the absence of a complete explanation of the mechanism behind electrotaxis, certain signaling pathways have been found to have an involvement in electrotaxis. In both neutrophils and keratinocytes, Zhau et. al. experimentally determined that physiological strength EFs induce phosphorlyation of extracellular-signal-regulated kinase (ERK), p38 mitogen-activated Kinase (MAPK), Src, and Akt on ser 473. In chemotaxis, Src and Akt are polarized by phosphatidylinositol-3-OH kinase-γ (PI(3)Kγ) activation and inhibition of phosphate tensin homolog (PTEN). [27] In the experiment, phosphorylated Src polarized in the direction of migration when influnenced by physiological strength EFs, as is also seen in chemotaxis. Phosphatidylinositol-3,4,5-triphosphate (PtdIns(3,4,5)P3), another molecule used in signaling, polarized to the leading edge of HL60 cells when subjected to an EF. Upon reversal of the EF, polarization PtdIns(3,4,5)P3 rapidly reversed to the new direction of migration. Treatment with lantruculin did not prevent this from occurring, indicating that polarization is not actin-dependent. Cells in which the gene encoding PI(3)Kγ, Pik3cg, was disrupted exhibited reduced electrotaxic responses. Pharmocological inhibition of PI(3)K in keratinocytes produced the same results. Similarly, genetic disruption of PTEN resulted in increased phosphorylation of ERK and Akt and a greater electrotaxic response. [27] Consideration of these results suggests that PI(3)Kγ and PTEN are involved in the signaling pathway used in electrotaxis.

Role in wound healing

A transepithelial potential (TEP) is created by a difference in ion concentrations across a tissue barrier in the body. In humans, a gradient exists between the outermost and innermost layers of skin across the entire body. This gradient can range from 10mV to 60mV, depending on which part of the body is measured. The potential is created by epithelial cells, which pump Cl- ions out of the skin through the apical membrane and transport Na+ ions to the basal side of the epithelium. [26] This is supported by an experiment in which Na+ and Cl- transport was increased by addition of AgNO3, and a corresponding increase in membrane potential was observed. Furosemide, a Cl- efflux inhibitor, also decreased the strength of the field in corneal cells. [27] These potentials are maintained elsewhere on the body, such as in the GI, urinary, and respiratory ducts, as well as the corneal epithelium. [26] [28] When the epithelium is pierced by some kind of wound, the barrier which establishes the electric potential has been removed, and so the TEP cannot be maintained. This creates a lateral EF, running from intact epithelium toward the edges of the wound. [26] [29] These wound EFs last as long as the wound takes to heal, and are involved in guiding various types of cells toward the injury in order to facilitate recovery [26] [30] These lateral fields arise instantaneously upon disruption of the epithelium and gradually increase to their maximum strength. The current strength then declines but is maintained throughout the healing process. The strength and direction of these fields are the same regardless of the size of a wound. [27]

Healing of skin wounds is a complex process involving the cooperation of various elements of the body, such as platelets, immune cells, epithelial cells, and fibroblasts. This process is coordinated largely by chemical signals, but there is evidence that electrotaxis plays an additional role in directing specific cell types toward the site of an injury. [26] During the proliferation phase of recovery, keratinocytes move toward the cathodal side of the EFs occurring around and injury, bringing them toward the edge of the wound. In fact, in vitro experimentation found that application of physiological strength EFs could override other signals and guide cells to migrate towards or even away from a wound depending on the direction of the field, regardless of chemical factors. [27] EFs have also experimentally been found to influence cell migration in human umbilical vein cells, dermal fibroblasts, and myofibroblasts. [26]

Role in cancer metastasis

Cancer metastasis is the process by which a tumor spreads from its place of origin in the body to distant tissues. Cancer cells and tumors have been known to produce and respond to electrical currents within the body. Cancer cells isolated from brain, prostate, and lung tumors have all been observed to have electrotaxis responses, and it there is evidence suggesting that electrotaxis may play a role in cancer cell metastasis. [31]

Related Research Articles

<span class="mw-page-title-main">Chemotaxis</span> Movement of an organism or entity in response to a chemical stimulus

Chemotaxis is the movement of an organism or entity in response to a chemical stimulus. Somatic cells, bacteria, and other single-cell or multicellular organisms direct their movements according to certain chemicals in their environment. This is important for bacteria to find food by swimming toward the highest concentration of food molecules, or to flee from poisons. In multicellular organisms, chemotaxis is critical to early development and development as well as in normal function and health. In addition, it has been recognized that mechanisms that allow chemotaxis in animals can be subverted during cancer metastasis, and the aberrant change of the overall property of these networks, which control chemotaxis, can lead to carcinogenesis. The aberrant chemotaxis of leukocytes and lymphocytes also contribute to inflammatory diseases such as atherosclerosis, asthma, and arthritis. Sub-cellular components, such as the polarity patch generated by mating yeast, may also display chemotactic behavior.

<span class="mw-page-title-main">Keratinocyte</span> Primary type of cell found in the epidermis

Keratinocytes are the primary type of cell found in the epidermis, the outermost layer of the skin. In humans, they constitute 90% of epidermal skin cells. Basal cells in the basal layer of the skin are sometimes referred to as basal keratinocytes. Keratinocytes form a barrier against environmental damage by heat, UV radiation, water loss, pathogenic bacteria, fungi, parasites, and viruses. A number of structural proteins, enzymes, lipids, and antimicrobial peptides contribute to maintain the important barrier function of the skin. Keratinocytes differentiate from epidermal stem cells in the lower part of the epidermis and migrate towards the surface, finally becoming corneocytes and eventually being shed, which happens every 40 to 56 days in humans.

A taxis is the movement of an organism in response to a stimulus such as light or the presence of food. Taxes are innate behavioural responses. A taxis differs from a tropism in that in the case of taxis, the organism has motility and demonstrates guided movement towards or away from the stimulus source. It is sometimes distinguished from a kinesis, a non-directional change in activity in response to a stimulus.

<span class="mw-page-title-main">Wound healing</span> Series of events that restore integrity to damaged tissue after an injury

Wound healing refers to a living organism's replacement of destroyed or damaged tissue by newly produced tissue.

In cellular biology, haptotaxis is the directional motility or outgrowth of cells, e.g. in the case of axonal outgrowth, usually up a gradient of cellular adhesion sites or substrate-bound chemoattractants. These gradients are naturally present in the extracellular matrix (ECM) of the body during processes such as angiogenesis, or artificially present in biomaterials where gradients are established by altering the concentration of adhesion sites on a polymer substrate.

Mechanotaxis refers to the directed movement of cell motility via mechanical cues. In response to fluidic shear stress, for example, cells have been shown to migrate in the direction of the fluid flow. Mechanotaxis is critical in many normal biological processes in animals, such as gastrulation, inflammation, and repair in response to a wound, as well as in mechanisms of diseases such as tumor metastasis.

<span class="mw-page-title-main">Hyaluronic acid</span> Anionic, nonsulfated glycosaminoglycan

Hyaluronic acid, also called hyaluronan, is an anionic, nonsulfated glycosaminoglycan distributed widely throughout connective, epithelial, and neural tissues. It is unique among glycosaminoglycans as it is non-sulfated, forms in the plasma membrane instead of the Golgi apparatus, and can be very large: human synovial HA averages about 7 MDa per molecule, or about 20,000 disaccharide monomers, while other sources mention 3–4 MDa.

Cell migration is a central process in the development and maintenance of multicellular organisms. Tissue formation during embryonic development, wound healing and immune responses all require the orchestrated movement of cells in particular directions to specific locations. Cells often migrate in response to specific external signals, including chemical signals and mechanical signals. Errors during this process have serious consequences, including intellectual disability, vascular disease, tumor formation and metastasis. An understanding of the mechanism by which cells migrate may lead to the development of novel therapeutic strategies for controlling, for example, invasive tumour cells.

<i>PTEN</i> (gene) Tumor suppressor gene

Phosphatase and tensin homolog (PTEN) is a phosphatase in humans and is encoded by the PTEN gene. Mutations of this gene are a step in the development of many cancers, specifically glioblastoma, lung cancer, breast cancer, and prostate cancer. Genes corresponding to PTEN (orthologs) have been identified in most mammals for which complete genome data are available.

The lamellipodium is a cytoskeletal protein actin projection on the leading edge of the cell. It contains a quasi-two-dimensional actin mesh; the whole structure propels the cell across a substrate. Within the lamellipodia are ribs of actin called microspikes, which, when they spread beyond the lamellipodium frontier, are called filopodia. The lamellipodium is born of actin nucleation in the plasma membrane of the cell and is the primary area of actin incorporation or microfilament formation of the cell.

Sphingosine-1-phosphate (S1P) is a signaling sphingolipid, also known as lysosphingolipid. It is also referred to as a bioactive lipid mediator. Sphingolipids at large form a class of lipids characterized by a particular aliphatic aminoalcohol, which is sphingosine.

<span class="mw-page-title-main">Heparin-binding EGF-like growth factor</span> Protein-coding gene in the species Homo sapiens

Heparin-binding EGF-like growth factor (HB-EGF) is a member of the EGF family of proteins that in humans is encoded by the HBEGF gene.

<span class="mw-page-title-main">CHUK</span> Protein-coding gene in humans

Inhibitor of nuclear factor kappa-B kinase subunit alpha (IKK-α) also known as IKK1 or conserved helix-loop-helix ubiquitous kinase (CHUK) is a protein kinase that in humans is encoded by the CHUK gene. IKK-α is part of the IκB kinase complex that plays an important role in regulating the NF-κB transcription factor. However, IKK-α has many additional cellular targets, and is thought to function independently of the NF-κB pathway to regulate epidermal differentiation.

The Akt signaling pathway or PI3K-Akt signaling pathway is a signal transduction pathway that promotes survival and growth in response to extracellular signals. Key proteins involved are PI3K and Akt.

<span class="mw-page-title-main">PI3K/AKT/mTOR pathway</span> Cell cycle regulation pathway

The PI3K/AKT/mTOR pathway is an intracellular signaling pathway important in regulating the cell cycle. Therefore, it is directly related to cellular quiescence, proliferation, cancer, and longevity. PI3K activation phosphorylates and activates AKT, localizing it in the plasma membrane. AKT can have a number of downstream effects such as activating CREB, inhibiting p27, localizing FOXO in the cytoplasm, activating PtdIns-3ps, and activating mTOR which can affect transcription of p70 or 4EBP1. There are many known factors that enhance the PI3K/AKT pathway including EGF, shh, IGF-1, insulin, and calmodulin. Both leptin and insulin recruit PI3K signalling for metabolic regulation. The pathway is antagonized by various factors including PTEN, GSK3B, and HB9.

β-Neoendorphin Chemical compound

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<span class="mw-page-title-main">Wound healing assay</span>

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Collective cell migration describes the movements of group of cells and the emergence of collective behavior from cell-environment interactions and cell-cell communication. Collective cell migration is an essential process in the lives of multicellular organisms, e.g. embryonic development, wound healing and cancer spreading (metastasis). Cells can migrate as a cohesive group or have transient cell-cell adhesion sites. They can also migrate in different modes like sheets, strands, tubes, and clusters. While single-cell migration has been extensively studied, collective cell migration is a relatively new field with applications in preventing birth defects or dysfunction of embryos. It may improve cancer treatment by enabling doctors to prevent tumors from spreading and forming new tumors.

<span class="mw-page-title-main">Developmental bioelectricity</span> Electric current produced in living cells

Developmental bioelectricity is the regulation of cell, tissue, and organ-level patterning and behavior by electrical signals during the development of embryonic animals and plants. The charge carrier in developmental bioelectricity is the ion rather than the electron, and an electric current and field is generated whenever a net ion flux occurs. Cells and tissues of all types use flows of ions to communicate electrically. Endogenous electric currents and fields, ion fluxes, and differences in resting potential across tissues comprise a signalling system. It functions along with biochemical factors, transcriptional networks, and other physical forces to regulate cell behaviour and large-scale patterning in processes such as embryogenesis, regeneration, and cancer suppression.

Scanning vibrating electrode technique (SVET), also known as vibrating probe within the field of biology, is a scanning probe microscopy (SPM) technique which visualizes electrochemical processes at a sample. It was originally introduced in 1974 by Jaffe and Nuccitelli to investigate the electrical current densities near living cells. Starting in the 1980s Hugh Isaacs began to apply SVET to a number of different corrosion studies. SVET measures local current density distributions in the solution above the sample of interest, to map electrochemical processes in situ as they occur. It utilizes a probe, vibrating perpendicular to the sample of interest, to enhance the measured signal. It is related to scanning ion-selective electrode technique (SIET), which can be used with SVET in corrosion studies, and scanning reference electrode technique (SRET), which is a precursor to SVET.

References

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