Effects of Paclitaxel and Eribulin in Mouse Sciatic Nerve: A Microtubule-Based Rationale for the Differential Induction of Chemotherapy-Induced Peripheral Neuropathy

Neurotox Res. 2016 Feb;29(2):299-313. doi: 10.1007/s12640-015-9580-6. Epub 2015 Dec 11.

Abstract

Microtubule targeting agents (MTAs) often lead to treatment limiting and life threatening side effects, including chemotherapy-induced peripheral neuropathy (CIPN). The frequency of severe CIPN varies among different MTAs. Since the microtubule binding interactions and mechanisms of action also vary among MTAs, we hypothesized that these distinct mechanisms may underlie the variability in frequency of severe CIPN. Using a two-week, maximum tolerated dose model, we morphologically and biochemically analyzed sciatic nerves from mice treated with either paclitaxel or eribulin. These drugs differ in their manner of microtubule binding and mechanisms of action and reports indicate paclitaxel also induces a higher frequency of severe CIPN than does eribulin. Morphologically, paclitaxel increased the frequency of observed signs of axon degeneration more significantly than did eribulin. Alternatively, eribulin but not paclitaxel induced occasional myelin "halo" structures. Biochemically, paclitaxel, and eribulin both induced α-tubulin expression (~1.9- and ~2.5-fold, respectively) and tubulin acetylation, a marker for microtubule stability, (~5- and ~11.7-fold, respectively). Eribulin but not paclitaxel-induced EB1 expression ~2.2-fold while paclitaxel but not eribulin mildly suppressed EB3 expression. Both EB proteins are associated with microtubule growth. Eribulin's combination of relatively mild deleterious morphological effects coupled with more potent biochemical changes promoting microtubule stability and growth in mice correlate with lower frequencies of severe CIPN in humans. We suggest that these eribulin-induced effects create a relatively stable microtubule network that compensates, in part, for the toxic anti-cancer effects of the drug, leading to fewer reported incidences of CIPN than for paclitaxel.

Keywords: Chemotherapy-induced peripheral neuropathy; Eribulin; Microtubules; Paclitaxel; Sciatic nerve.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acetylation / drug effects
  • Animals
  • Axons / drug effects
  • Axons / pathology
  • Female
  • Furans / toxicity*
  • Ketones / toxicity*
  • Mice
  • Mice, Inbred BALB C
  • Microtubule-Associated Proteins / metabolism
  • Microtubules / drug effects*
  • Microtubules / metabolism*
  • Myelin Sheath / drug effects
  • Myelin Sheath / pathology
  • Paclitaxel / toxicity*
  • Peripheral Nervous System Diseases / chemically induced
  • Peripheral Nervous System Diseases / metabolism*
  • Peripheral Nervous System Diseases / pathology*
  • Sciatic Nerve / drug effects*
  • Sciatic Nerve / pathology*
  • Sciatic Neuropathy / chemically induced
  • Sciatic Neuropathy / metabolism
  • Sciatic Neuropathy / pathology
  • Tubulin / metabolism

Substances

  • Furans
  • Ketones
  • Mapre1 protein, rat
  • Microtubule-Associated Proteins
  • Tubulin
  • eribulin
  • Paclitaxel