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Ion channel clustering enhances weak electric field detection by neutrophils: apparent roles of SKF96365-sensitive cation channels and myeloperoxidase trafficking in cellular responses

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Abstract

We have tested Galvanovskis and Sandblom’s prediction that ion channel clustering enhances weak electric field detection by cells as well as how the elicited signals couple to metabolic alterations. Electric field application was timed to coincide with certain known intracellular chemical oscillators (phase-matched conditions). Polarized, but not spherical, neutrophils labeled with anti-Kv1.3, FL-DHP, and anti-TRP1, but not anti-T-type Ca2+ channels, displayed clusters at the lamellipodium. Resonance energy transfer experiments showed that these channel pairs were in close proximity. Dose-field sensitivity studies of channel blockers suggested that K+ and Ca2+ channels participate in field detection, as judged by enhanced oscillatory NAD(P)H amplitudes. Further studies suggested that K+ channel blockers act by reducing the neutrophil’s membrane potential. Mibefradil and SKF93635, which block T-type Ca2+ channels and SOCs, respectively, affected field detection at appropriate doses. Microfluorometry and high-speed imaging of indo-1-labeled neutrophils was used to examine Ca2+ signaling. Electric fields enhanced Ca2+ spike amplitude and triggered formation of a second traveling Ca2+ wave. Mibefradil blocked Ca2+ spikes and waves. Although 10 μM SKF96365 mimicked mibefradil, 7 μM SKF96365 specifically inhibited electric field-induced Ca2+ signals, suggesting that one SKF96365-senstive site is influenced by electric fields. Although cells remained morphologically polarized, ion channel clusters at the lamellipodium and electric field sensitivity were inhibited by methyl-β-cyclodextrin. As a result of phase-matched electric field application in the presence of ion channel clusters, myeloperoxidase (MPO) was found to traffic to the cell surface. As MPO participates in high amplitude metabolic oscillations, this suggests a link between the signaling apparatus and metabolic changes. Furthermore, electric field effects could be blocked by MPO inhibition or removal while certain electric field effects were mimicked by the addition of MPO to untreated cells. Therefore, channel clustering plays an important role in electric field detection and downstream responses of morphologically polarized neutrophils. In addition to providing new mechanistic insights concerning electric field interactions with cells, our work suggests novel methods to remotely manipulate physiological pathways.

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Abbreviations

4-AP:

4-Aminopyridine

di-8-ANEPPS:

1-(3-Sulfonatopropyl)-4-[beta [2-(di-n-octylamino)-6-naphtyl]vinyl] pyridinium betaine

ELF:

Extremely-low frequency

FcγR:

Fcγ receptor

FITC:

Fluorescein isothiocyanate

FL-DHP:

DM-bodipy (−)-dihydropyridine

FMLP:

N-formyl-met-leu-phe

HBSS:

Hanks‘ buffered salt solution

pHBAH:

p-hydroxybenzoic acid hydrazide

HQ:

Hydroxyquinone

mβCD:

Methyl-β-cyclodextrin

MPO:

Myeloperoxidase

OTP:

Optical transmembrane potential

PMA:

Phorbol myristate acetate

PMT:

Photomultiplier tube

RET:

Resonance energy transfer

ROM:

Reactive oxygen metabolite

SHA:

Salicylhydroxamic acid

SOC:

Store-operated channel

TEA:

Tetraethylammonium chloride

TRITC:

Tetramethylisothiocyanate

TRP:

Transient receptor potential-like

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Acknowledgements

This work was supported by NIH Grant CA74120 (H.R.P.).

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Authors and Affiliations

  1. Department of Ophthalmology and Visual Sciences, The University of Michigan Medical School, 1000 Wall Street, Ann Arbor, MI, 48105, USA

    Andrei L. Kindzelskii & Howard R. Petty

  2. Department of Microbiology and Immunology, The University of Michigan Medical School, Ann Arbor, MI, 48105, USA

    Howard R. Petty

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  1. Andrei L. Kindzelskii
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  2. Howard R. Petty
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Correspondence to Howard R. Petty.

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Kindzelskii, A.L., Petty, H.R. Ion channel clustering enhances weak electric field detection by neutrophils: apparent roles of SKF96365-sensitive cation channels and myeloperoxidase trafficking in cellular responses. Eur Biophys J 35, 1–26 (2005). https://doi.org/10.1007/s00249-005-0001-2

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  • DOI: https://doi.org/10.1007/s00249-005-0001-2

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