Oxidative stress in the development, maintenance and resolution of paclitaxel-induced painful neuropathy

Natalie Amy Duggett, Lisa Anne Griffiths, Olivia E McKenna, Vittorio de Santis, Nutcha Yongsanguanchai, Esther B Mokori, Sarah Jane Louise Flatters

Research output: Contribution to journalArticlepeer-review

140 Citations (Scopus)
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Abstract

Paclitaxel is a first-line chemotherapeutic with the major dose-limiting side effect of painful neuropathy. Previous preclinical studies indicate mitochondrial dysfunction and oxidative stress are associated with this disorder; however no direct assessment of ROS levels and antioxidant enzyme activity in sensory neurons following paclitaxel has been undertaken. As expected, repeated low doses of systemic paclitaxel in rats induced long-lasting pain behaviour with a delayed onset, akin to the clinical scenario. To elucidate the role of ROS in development and maintenance of paclitaxel-induced painful neuropathy, we have assessed ROS and antioxidant enzyme activity levels in the nociceptive system in vivo at three key behavioural time-points; prior to pain onset (day 7), peak pain severity and pain resolution. In isolated dorsal root ganglion (DRG) neurons, ROS levels were unchanged following paclitaxel-exposure in vitro or in vivo. ROS levels were further assessed in DRG and spinal cord in vivo following intrathecal MitoTracker®RedCM-H2XRos administration in paclitaxel-/vehicle-treated rats. ROS levels were increased at day 7, specifically in non-peptidergic DRG neurons. In the spinal cord, neuronally-derived ROS was increased at day 7, yet ROS levels in microglia and astrocytes was unaltered. In DRG, CuZnSOD and GPx activity were increased at day 7 and peak pain time-points, respectively. In peripheral sensory nerves, CuZnSOD activity was increased at day 7, and at peak pain, MnSOD, CuZnSOD and GPx activity were increased. Catalase activity was unaltered in DRG and saphenous nerves. These data suggest that neuronally-derived mitochondrial ROS, accompanied with an inadequate endogenous antioxidant enzyme response, are contributory factors in paclitaxel-induced painful neuropathy
Original languageEnglish
Pages (from-to)13-26
Number of pages14
JournalNeuroscience
Volume333
Early online date5 Jul 2016
DOIs
Publication statusPublished - 1 Oct 2016

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