Mechanisms of Chemotherapy-Induced Peripheral Neuropathy

Renata Zajączkowska, Magdalena Kocot-Kępska, Wojciech Leppert, Anna Wrzosek, Joanna Mika, Jerzy Wordliczek, Renata Zajączkowska, Magdalena Kocot-Kępska, Wojciech Leppert, Anna Wrzosek, Joanna Mika, Jerzy Wordliczek

Abstract

Chemotherapy-induced peripheral neuropathy (CIPN) is one of the most frequent side effects caused by antineoplastic agents, with a prevalence from 19% to over 85%. Clinically, CIPN is a mostly sensory neuropathy that may be accompanied by motor and autonomic changes of varying intensity and duration. Due to its high prevalence among cancer patients, CIPN constitutes a major problem for both cancer patients and survivors as well as for their health care providers, especially because, at the moment, there is no single effective method of preventing CIPN; moreover, the possibilities of treating this syndrome are very limited. There are six main substance groups that cause damage to peripheral sensory, motor and autonomic neurons, which result in the development of CIPN: platinum-based antineoplastic agents, vinca alkaloids, epothilones (ixabepilone), taxanes, proteasome inhibitors (bortezomib) and immunomodulatory drugs (thalidomide). Among them, the most neurotoxic are platinum-based agents, taxanes, ixabepilone and thalidomide; other less neurotoxic but also commonlyused drugs are bortezomib and vinca alkaloids. This paper reviews the clinical picture of CIPN and the neurotoxicity mechanisms of the most common antineoplastic agents. A better understanding of the risk factors and underlying mechanisms of CIPN is needed to develop effective preventive and therapeutic strategies.

Keywords: anticancer drugs; cancer pain; chemotherapy-induced neuropathy; drug neurotoxicity; pathophysiological mechanisms.

Conflict of interest statement

The authors declare no conflicts of interest.

Figures

Figure 1
Figure 1
The mechanisms of chemotherapy-induced peripheral neuropathy (CIPN) induced by platinum-based drugs: Platinum-based drugs induce the activation of glia cells, which leads to the activation of the attraction and activation of immune cells and to the release and elevation of pro-inflammatory cytokines (interleukins and chemokines), which results in nociceptor sensitization and hyperexcitability of peripheral neurons, and (together with ROS) damage the blood–brain barrier. These processes lead to the development of neuroinflammation. Mitochondrial damage caused by platinum-based drugs leads to an increased production of reactive oxygen species (ROS), which leads to enzyme, protein and lipid damage within neurons as well as the dysregulation of calcium homeostasis, which induces apoptotic changes in peripheral nerves and in DRG cells. Platinum-based drugs also alter the activity Na+, K+ and TRP ion channels, resulting in the hyperexcitability of peripheral neurons. All of the above-described processes have the potential to alter the excitability of peripheral neurons.
Figure 2
Figure 2
The mechanisms of CIPN induced by thalidomide: Thalidomide downregulates TNF-α and inhibits NF-κB, which leads to the dysregulation of neurotrophins and their receptors and, in consequence, accelerates neuronal cell death. Moreover, the antiangiogenic effect induced by thalidomide causes secondary ischemia and hypoxia of nerve fibres and, subsequently, irreversible damage of sensory neurons. The activation of the dihydroxy metabolite of thalidomide causes the extensive release and activation of ROS and activates DNA cleavage, though further preclinical and clinical trials are needed to confirm the presence of such a mechanism in thalidomide-induced peripheral neuropathy.
Figure 3
Figure 3
The mechanisms of CIPN induced by taxanes: Taxanes cause microtubule disruption, which impairs axonal transport and leads to Wallerian degeneration, altered activity of ion channels and hyperexcitability of peripheral neurons. Taxanes also modify the expression and function of Na+, K+ and TRP ion channels, which results in the hyperexcitability of peripheral neurons. Taxane-induced mitochondrial damage contributes to the increased production of reactive oxygen species (ROS), which leads to enzyme, protein and lipid damage as well as the dysregulation of calcium homeostasis within neurons, which induces apoptotic changes and the demyelination of peripheral nerves. These processes alter the excitability of peripheral neurons. The activation of microglia and astrocytes by taxanes also leads to the activation of attraction and activation of immune cells and to the release and elevation of pro-inflammatory cytokines (interleukins and chemokines), which results in the nociceptor sensitization and hyperexcitability of peripheral neurons. These processes lead to nociceptor sensitization and the development of neuroinflammation.
Figure 4
Figure 4
The mechanisms of CIPN induced by epothilones: Epothilones cause microtubule disruption, which impairs axonal transport and leads to Wallerian degeneration, the altered activity of ion channels and the hyperexcitability of peripheral neurons. Furthermore, the damage to mitochondria by epothilones leads to an increased production of reactive oxygen species (ROS), resulting in enzyme, protein and lipid damage within neurons as well as apoptotic changes to peripheral nerve. These processes lead to altered excitability of peripheral neurons. ROS release and the attraction and activation of T-lymphocytes and monocytes also induces the release and elevation of pro-inflammatory cytokines (interleukins and chemokines), the activation of immune cells and the development of neuroinflammation.
Figure 5
Figure 5
The mechanisms of CIPN induced by vinca alkaloids: Vinca alkaloids cause changes to large axons and DRG neurons, which leads to Wallerian degeneration, the altered activity of ion channels and the hyperexcitability of peripheral neurons. Moreover, the inhibition of polymerization into microtubules inhibits axonal transport, which leads to distal axonopathy. These processes alter the excitability of peripheral neurons, whereas the attraction and activation of immune cells by vinca alkaloids causes the release and elevation of pro-inflammatory cytokines (interleukins and chemokines), which results in neuroinflammation.
Figure 6
Figure 6
The mechanisms of CIPN induced by protease inhibitors: Protease inhibitors increase the metabolism of sphingolipids in astrocytes, which leads to the formation of ceramide, sphingosine-1 phosphate (S1P) and dihydrosphingosine-1-phosphate (DH-S1P), which by binding to astrocyte receptors, increase the release of presynaptic glutamate at the level of the dorsal horn, which leads to the development of neuropathic pain. Moreover, bortezomib-induced mitochondrial damage increases the production of reactive oxygen species (ROS), which results in enzyme, protein and lipid damage within the neurons as well as induces apoptotic changes in peripheral nerves. These processes alter the excitability of peripheral neurons, whereas the attraction and activation of T-lymphocytes and monocytes, as well as the increases in the production of reactive oxygen species (ROS) induce the release and elevation of pro-inflammatory cytokines (interleukins and chemokines). These processes lead to nociceptor sensitization, the hyperexcitability of peripheral neurons and the development of neuroinflammation.

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