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Structure-Activity Relationship of Selected Meta- and Para-Hydroxylated Non–Dioxin Like Polychlorinated Biphenyls: From Single RyR1 Channels to Muscle Dysfunction
Journal article   Open access   Peer reviewed

Structure-Activity Relationship of Selected Meta- and Para-Hydroxylated Non–Dioxin Like Polychlorinated Biphenyls: From Single RyR1 Channels to Muscle Dysfunction

Yassaman Niknam, Wei Feng, Gennady Cherednichenko, Yao Dong, Sudhir N Joshi, Sandhya M Vyas, Hans-Joachim Lehmler and Isaac N Pessah
Toxicological sciences, Vol.136(2), pp.500-513
12/2013
DOI: 10.1093/toxsci/kft202
PMCID: PMC3858193
PMID: 24014653
url
https://doi.org/10.1093/toxsci/kft202View
Published (Version of record) Open Access

Abstract

Non–dioxin like polychlorinated biphenyls (NDL-PCBs) are legacy environmental contaminants with contemporary unintentional sources. NDL-PCBs interact with ryanodine receptors (RyRs), Ca 2+ channels of sarcoplasmic/endoplasmic reticulum (SR/ER) that regulate excitation-contraction coupling (ECC) and Ca 2+ -dependent cell signaling in muscle. Activities of 4 chiral congeners PCB91, 95, 132, and 149 and their respective 4- and 5-hydroxy (-OH) derivatives toward rabbit skeletal muscle ryanodine receptor (RyR1) are investigated using [ 3 H]ryanodine binding and SR Ca 2+ flux analyses. Although 5-OH metabolites have comparable activity to their respective parent in both assays, 4-OH derivatives are unable to trigger Ca 2+ release from SR microsomes in the presence of Ca 2+ -ATPase activity. PCB95 and derivatives are investigated using single channel voltage-clamp and primary murine embryonic muscle cells (myotubes). Like PCB95, 5-OH-PCB95 quickly and persistently increases channel open probability ( p o > .9) by stabilizing the full-open channel state, whereas 4-OH-PCB95 transiently enhances p o . Ca 2+ imaging of myotubes loaded with Fluo-4 show that acute exposure to PCB95 (5µM) potentiates ECC and caffeine responses and partially depletes SR Ca 2+ stores. Exposure to 5-OH-PCB95 (5 µM) increases cytoplasmic Ca 2+ , leading to rapid ECC failure in 50% of myotubes with the remainder retaining negligible responses. 4-OH-PCB95 neither increases baseline Ca 2+ nor causes ECC failure but depresses ECC and caffeine responses by 50%. With longer (3h) exposure to 300nM PCB95, 5-OH-PCB95, or 4-OH-PCB95 decreases the number of ECC responsive myotubes by 22%, 81%, and 51% compared with control by depleting SR Ca 2+ and/or uncoupling ECC. NDL-PCBs and their 5-OH and 4-OH metabolites differentially influence RyR1 channel activity and ECC in embryonic skeletal muscle.
hydroxylated metabolites polychlorinated biphenyls ryanodine receptor muscle dysfunction calcium signaling

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