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Combinatorial Chemistry & High Throughput Screening

Editor-in-Chief

ISSN (Print): 1386-2073
ISSN (Online): 1875-5402

Review Article

Mechanistic Involvement of Inflammation in Bortezomib-induced Peripheral Neuropathy

Author(s): Lavisha Goel, Pooja Gupta* and Monika Pahuja

Volume 25, Issue 10, 2022

Published on: 22 July, 2022

Page: [1595 - 1600] Pages: 6

DOI: 10.2174/1386207325666220524144147

Price: $65

Abstract

Aim: The aim of the study was to establish the role of inflammation in bortezomibinduced peripheral neuropathy (BIPN).

Background: Peripheral neuropathy is the dose-limiting toxicity of bortezomib that can lead to discontinuation of the treatment. There are multiple mechanisms involved in the disposition of BIPN. However, the role of inflammatory mediators is still under investigation. A complete understanding of inflammatory markers in relation to BIPN can lead to the development of effective therapy for prophylaxis and treatment of peripheral neuropathy.

Objective: Based on the available data, the role of inflammatory mediators in the development of peripheral neuropathy due to bortezomib has been postulated.

Methods: The “Pubmed” and “Google Scholar” were used as the search engines with terms like “peripheral neuropathy”, “bortezomib-induced peripheral neuropathy” and “inflammation”. Original research, case reports and review articles were considered.

Results: Bortezomib use is associated with the development of peripheral neuropathy. This effect is due to the damage to Schwann cells and dorsal root ganglion neurons, mitochondrial damage, increased ion channel susceptibility, and higher infiltration of macrophages in the spinal cord. All these factors collectively increase the secretion of inflammatory mediators and lead to the development of neuropathic pain.

Conclusion: Targeting inflammatory mediators may be helpful in the treatment of bortezomibinduced peripheral neuropathy.

Keywords: Bortezomib, peripheral neuropathy, inflammatory mediators, Schwann cells, tumor necrosis factor-alpha, myeloma.

Graphical Abstract
[1]
Richardson, P.G.; Sonneveld, P.; Schuster, M.W.; Irwin, D.; Stadtmauer, E.A.; Facon, T. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N. Engl. J. Med., 2005, 352(24), 2487-2498.
[2]
Richardson, P.G.; Sonneveld, P.; Schuster, M.; Irwin, D.; Stadtmauer, E.; Facon, T. Extended follow-up of a phase 3 trial in relapsed multiple myeloma: Final time-to-event results of the APEX trial. Blood, 2007, 110(10), 3557-3560.
[3]
Moreau, P.; Coiteux, V.; Hulin, C.; Leleu, X.; van de Velde, H.; Acharya, M. Prospective comparison of subcutaneous versus intravenous administration of bortezomib in patients with multiple myeloma. Haematologica, 2008, 93(12), 1908-1911.
[4]
Kristinsson, S.Y.; Anderson, W.F.; Landgren, O. Improved long-term survival in multiple myeloma up to the age of 80 years. Leukemia, 2014, 28(6), 1346-1348.
[5]
Richardson, P.G.; Barlogie, B.; Berenson, J.; Singhal, S.; Jagannath, S.; Irwin, D. A phase 2 study of bortezomib in relapsed, refractory myeloma. N. Engl. J. Med., 2003, 348(26), 2609-2617.
[6]
Cho, J.; Kang, D.; Lee, J.Y.; Kim, K.; Kim, S.J. Impact of dose modification on intravenous bortezomib-induced peripheral neuropathy in multiple myeloma patients. Support. Care Cancer, 2014, 22(10), 2669-2675.
[7]
Pragnya, C.; Linga, V.G.; Thota, N.K.; Gundeti, S.; Digumarti, R. Bortezomib in newly diagnosed patients with multiple myeloma: A retrospective analysis from a tertiary care center in India. Indian J. Cancer, 2015, 52(4), 537-540.
[8]
Ye, Z.; Chen, J.; Xuan, Z.; Yang, W.; Chen, J. Subcutaneous bortezomib might be standard of care for patients with multiple myeloma: A systematic review and meta-analysis. Drug Des. Devel. Ther., 2019, 13, 1707-1716.
[9]
Mohty, B.; El-Cheikh, J.; Yakoub-Agha, I.; Moreau, P.; Harousseau, J.L.; Mohty, M. Peripheral neuropathy and new treatments for multiple myeloma: Background and practical recommendations. Haematologica, 2010, 95(2), 311-319.
[10]
Laforgia, M.; Laface, C.; Calabro, C.; Ferraiuolo, S.; Ungaro, V.; Tricarico, D. Peripheral neuropathy under oncologic therapies: A literature review on pathogenetic mechanisms. Int. J. Mol. Sci., 2021, 22(4), 1980.
[11]
Carozzi, V.A.; Renn, C.L.; Bardini, M.; Fazio, G.; Chiorazzi, A.; Meregalli, C. Bortezomib-induced painful peripheral neuropathy: An electrophysiological, behavioral, morphological and mechanistic study in the mouse. PLoS One, 2013, 8(9), e72995.
[http://dx.doi.org/10.1371/journal.pone.0072995]
[12]
Ellis, A.; Bennett, D.L. Neuroinflammation and the generation of neuropathic pain. Br. J. Anaesth., 2013, 111(1), 26-37.
[13]
Yan, W.; Wu, Z.; Zhang, Y.; Hong, D.; Dong, X.; Liu, L. The molecular and cellular insight into the toxicology of bortezomib-induced peripheral neuropathy. Biomed. Pharmacother., 2021, 142, 112068.
[14]
Yamamoto, S.; Egashira, N. Pathological mechanisms of bortezomib-induced peripheral neuropathy. Int. J. Mol. Sci., 2021, 22(2), 888.
[15]
Zhang, Y.; Mei, H.; Cao, Y.; Yan, X.; Yan, J.; Gao, H. Recent advances and challenges of electrode materials for flexible supercapacitors. Coord. Chem. Rev., 2021, 438, 213910.
[16]
Zhang, Y. Synthesis and electrochemical performance of MnO2/BC composite as active materials for supercapacitors. J. Anal. Appl. Pyrolysis, 2015, 111, 233-237.
[17]
Argyriou, A.A.; Iconomou, G.; Kalofonos, H.P. Bortezomib-induced peripheral neuropathy in multiple myeloma: A comprehensive review of the literature. Blood, 2008, 112(5), 1593-1599.
[18]
Cavaletti, G.; Gilardini, A.; Canta, A.; Rigamonti, L.; Rodriguez-Menendez, V.; Ceresa, C.; Marmiroli, P.; Bossi, M.; Oggioni, N.; D’Incalci, M.; De Coster, R. Bortezomib-induced peripheral neurotoxicity: A neurophysiological and pathological study in the rat. Exp. Neurol., 2007, 204(1), 317-325.
[19]
Bilinska, M.; Usnarska-Zubkiewicz, L.; Pokryszko-Dragan, A. Bortezomib-induced painful neuropathy in patients with multiple myeloma. Contemp. Oncol. (Pozn.), 2013, 17(5), 421-426.
[20]
Tariman, J.D.; Love, G.; McCullagh, E.; Sandifer, S. Peripheral neuropathy associated with novel therapies in patients with multiple myeloma: Consensus statement of the IMF Nurse Leadership Board. Clin. J. Oncol. Nurs., 2008, 12(3)(Suppl.), 29-36.
[21]
Kopito, R.R. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol., 2000, 10(12), 524-530.
[22]
Strohm, L.; Behrends, C. Glia-specific autophagy dysfunction in ALS. Semin. Cell Dev. Biol., 2020, 99, 172-182.
[23]
Badros, A.; Goloubeva, O.; Dalal, J.S.; Can, I.; Thompson, J.; Rapoport, A.P. Neurotoxicity of bortezomib therapy in multiple myeloma: A single-center experience and review of the literature. Cancer, 2007, 110(5), 1042-1049.
[24]
Filosto, M.; Rossi, G.; Pelizzari, A.M.; Buzio, S.; Tentorio, M.; Broglio, L. A high-dose bortezomib neuropathy with sensory ataxia and myelin involvement. J. Neurol. Sci., 2007, 263(1-2), 40-43.
[25]
Bruna, J.; Udina, E.; Ale, A.; Vilches, J.J.; Vynckier, A.; Monbaliu, J. Neurophysiological, histological and immunohistochemical characterization of bortezomib-induced neuropathy in mice. Exp. Neurol., 2010, 223(2), 599-608.
[26]
Koksal, A.R.; Verne, G.N.; Zhou, Q. Endoplasmic reticulum stress in biological processing and disease. J. Investig. Med., 2021, 69(2), 309-315.
[27]
Qu, J.; Zou, T.; Lin, Z. The roles of the ubiquitin-proteasome system in the endoplasmic reticulum stress pathway. Int. J. Mol. Sci., 2021, 22(4), 1526.
[28]
Shin, Y.K.; Jang, S.Y.; Lee, H.K.; Jung, J.; Suh, D.J.; Seo, S.Y.; Park, H.T. Pathological adaptive responses of Schwann cells to endoplasmic reticulum stress in bortezomib-induced peripheral neuropathy. Glia, 2010, 58(16), 1961-1976.
[29]
Raasakka, A.; Ruskamo, S.; Kowal, J.; Han, H.; Baumann, A.; Myllykoski, M. Molecular structure and function of myelin protein P0 in membrane stacking. Sci. Rep., 2019, 9(1), 642.
[30]
Robinson, C.R.; Zhang, H.; Dougherty, P.M. Astrocytes, but not microglia, are activated in oxaliplatin and bortezomib-induced peripheral neuropathy in the rat. Neuroscience, 2014, 274, 308-317.
[31]
Palanca, A.; Casafont, I.; Berciano, M.T.; Lafarga, M. Proteasome inhibition induces DNA damage and reorganizes nuclear architecture and protein synthesis machinery in sensory ganglion neurons. Cell. Mol. Life Sci., 2014, 71(10), 1961-1975.
[32]
Tomita, S.; Sekiguchi, F.; Deguchi, T.; Miyazaki, T.; Ikeda, Y.; Tsubota, M. Critical role of Cav3.2 T-type calcium channels in the peripheral neuropathy induced by bortezomib, a proteasome-inhibiting chemotherapeutic agent, in mice. Toxicology, 2019, 413, 33-39.
[33]
Candelas, M.; Reynders, A.; Arango-Lievano, M.; Neumayer, C.; Fruquiere, A.; Demes, E. Cav3.2 T-type calcium channels shape electrical firing in mouse Lamina II neurons. Sci. Rep., 2019, 9(1), 3112.
[34]
Trevisan, G.; Materazzi, S.; Fusi, C.; Altomare, A.; Aldini, G.; Lodovici, M. Novel therapeutic strategy to prevent chemotherapy-induced persistent sensory neuropathy by TRPA1 blockade. Cancer Res., 2013, 73(10), 3120-3131.
[35]
Xie, J.D.; Chen, S.R.; Chen, H.; Pan, H.L. Bortezomib induces neuropathic pain through protein kinase C-mediated activation of presynaptic NMDA receptors in the spinal cord. Neuropharmacology, 2017, 123, 477-487.
[36]
Maharjan, S.; Oku, M.; Tsuda, M.; Hoseki, J.; Sakai, Y. Mitochondrial impairment triggers cytosolic oxidative stress and cell death following proteasome inhibition. Sci. Rep., 2014, 4, 5896.
[37]
Areti, A.; Yerra, V.G.; Naidu, V.; Kumar, A. Oxidative stress and nerve damage: Role in chemotherapy induced peripheral neuropathy. Redox Biol., 2014, 2, 289-295.
[38]
Napoli, I.; Noon, L.A.; Ribeiro, S.; Kerai, A.P.; Parrinello, S.; Rosenberg, L.H. A central role for the ERK-signaling pathway in controlling Schwann cell plasticity and peripheral nerve regeneration in vivo. Neuron, 2012, 73(4), 729-742.
[39]
Perkins, N.M.; Tracey, D.J. Hyperalgesia due to nerve injury: Role of neutrophils. Neuroscience, 2000, 101(3), 745-757.
[40]
Kumar, V.; Sharma, A. Neutrophils: Cinderella of innate immune system. Int. Immunopharmacol., 2010, 10(11), 1325-1334.
[41]
Moalem, G.; Xu, K.; Yu, L. T lymphocytes play a role in neuropathic pain following peripheral nerve injury in rats. Neuroscience, 2004, 129(3), 767-777.
[42]
Sorkin, L.S.; Xiao, W.H.; Wagner, R.; Myers, R.R. Tumour necrosis factor-alpha induces ectopic activity in nociceptive primary afferent fibres. Neuroscience, 1997, 81(1), 255-262.
[43]
Morenilla-Palao, C.; Planells-Cases, R.; García-Sanz, N.; Ferrer-Montiel, A. Regulated exocytosis contributes to protein kinase C potentiation of vanilloid receptor activity. J. Biol. Chem., 2004, 279(24), 25665-25672.
[44]
Binshtok, A.M.; Wang, H.; Zimmermann, K.; Amaya, F.; Vardeh, D.; Shi, L. Nociceptors are interleukin-1beta sensors. J. Neurosci., 2008, 28(52), 14062-14073.
[45]
Torii, H.; Hosoi, J.; Beissert, S.; Xu, S.; Fox, F.E.; Asahina, A. Regulation of cytokine expression in macrophages and the Langerhans cell-like line XS52 by calcitonin gene-related peptide. J. Leukoc. Biol., 1997, 61(2), 216-223.
[46]
Vellani, V.; Mapplebeck, S.; Moriondo, A.; Davis, J.B.; McNaughton, P.A. Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat and anandamide. J. Physiol., 2001, 534(Pt 3), 813-825.
[47]
Meregalli, C.; Marjanovic, I.; Scali, C.; Monza, L.; Spinoni, N.; Galliani, C. High-dose intravenous immunoglobulins reduce nerve macrophage infiltration and the severity of bortezomib-induced peripheral neurotoxicity in rats. J. Neuroinflammation, 2018, 15(1), 232.
[48]
Cata, J.P.; Weng, H.R.; Chen, J.H.; Dougherty, P.M. Altered discharges of spinal wide dynamic range neurons and down-regulation of glutamate transporter expression in rats with paclitaxel-induced hyperalgesia. Neuroscience, 2006, 138(1), 329-338.
[49]
Barton, M.J.; John, J.S.; Clarke, M.; Wright, A.; Ekberg, J. The Glia response after peripheral nerve injury: A comparison between schwann cells and olfactory ensheathing cells and their uses for neural regenerative therapies. Int. J. Mol. Sci., 2017, 18(2), 287.
[50]
Jha, M.K.; Jeon, S.; Suk, K. Glia as a link between neuroinflammation and neuropathic pain. Immune Netw., 2012, 12(2), 41-47.
[51]
Stockstill, K.; Doyle, T.M.; Yan, X.; Chen, Z.; Janes, K.; Little, J.W. Dysregulation of sphingolipid metabolism contributes to bortezomib-induced neuropathic pain. J. Exp. Med., 2018, 215(5), 1301-1313.
[52]
Watanabe, T.; Nagase, K.; Chosa, M.; Tobinai, K. Schwann cell autophagy induced by SAHA, 17-AAG, or clonazepam can reduce bortezomib-induced peripheral neuropathy. Br. J. Cancer, 2010, 103(10), 1580-1587.
[53]
Bang, Y.; Kang, B.Y.; Choi, H.J. Preconditioning stimulus of proteasome inhibitor enhances aggresome formation and autophagy in differentiated SH-SY5Y cells. Neurosci. Lett., 2014, 566, 263-268.
[54]
Meregalli, C.; Chiorazzi, A.; Carozzi, V.A.; Canta, A.; Sala, B.; Colombo, M. Evaluation of tubulin polymerization and chronic inhibition of proteasome as citotoxicity mechanisms in bortezomib-induced peripheral neuropathy. Cell Cycle, 2014, 13(4), 612-621.
[55]
Gomez-Sanchez, J.A.; Carty, L.; Iruarrizaga-Lejarreta, M.; Palomo-Irigoyen, M.; Varela-Rey, M.; Griffith, M. Schwann cell autophagy, myelinophagy, initiates myelin clearance from injured nerves. J. Cell Biol., 2015, 210(1), 153-168.
[56]
Li, R.; Li, D.; Wu, C.; Ye, L.; Wu, Y.; Yuan, Y. Nerve growth factor activates autophagy in Schwann cells to enhance myelin debris clearance and to expedite nerve regeneration. Theranostics, 2020, 10(4), 1649-1677.
[57]
Bouchenaki, H.; Danigo, A.; Sturtz, F.; Hajj, R.; Magy, L.; Demiot, C. An overview of ongoing clinical trials assessing pharmacological therapeutic strategies to manage chemotherapy-induced peripheral neuropathy, based on preclinical studies in rodent models. Fundam. Clin. Pharmacol., 2021, 35(3), 506-523.
[58]
Maschio, M.; Zarabla, A.; Maialetti, A.; Marchesi, F.; Giannarelli, D.; Gumenyuk, S.; Pisani, F.; Renzi, D.; Galiè, E.; Mengarelli, A. Prevention of bortezomib-related peripheral neuropathy with docosahexaenoic acid and α-lipoic acid in patients with multiple myeloma: Preliminary data. Integr. Cancer Ther., 2018, 17(4), 1115-1124.

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