Oxaliplatin induces hyperexcitability at motor and autonomic neuromuscular junctions through effects on voltage-gated sodium channels

British Journal of Pharmacology

Volumn 146, Issue 7, 2005, Pages 1027-1039

  Webster, Richard G ^a   Brain, Keith L ^b   Wilson, Richard H ^c   Grem, Jean L ^c   Vincent, Angela ^a  

^a JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

pompilidotoxin; Carbamazepine; Hyperexcitability; Neuromuscular junction; Neuromyotonia; Neurotoxicity; Oxaliplatin; Voltage activated Na + channels

Indexed keywords

4 AMINOPYRIDINE; APAMIN; BETA POMPILIDOTOXIN; CALCIUM ION; CARBAMAZEPINE; OXALIPLATIN; TETRODOTOXIN; TOXIN; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM; CONTROLLED STUDY; ENDPLATE POTENTIAL; HEMIDIAPHRAGM; MINIATURE ENDPLATE POTENTIAL; MOTOR NERVE; MOUSE; NERVE CONDUCTION; NERVE ENDING; NERVE EXCITABILITY; NERVE STIMULATION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; REPOLARIZATION; SYNAPSE; VAS DEFERENS;

ACTION POTENTIALS; ANIMALS; ANTINEOPLASTIC AGENTS; AUTONOMIC NERVOUS SYSTEM; CALCIUM; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEUROMUSCULAR JUNCTION; ORGANOPLATINUM COMPOUNDS; POTASSIUM CHANNELS; SODIUM CHANNELS; SYNAPTIC TRANSMISSION; VAS DEFERENS;

EID: 28444444891     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1038/sj.bjp.0706407     Document Type: Article

References (46)

1. + channel kinetics on rat sensory neurons. Eur. J. Pharmacol., 406, 25-32.
2. ANDRE, T., BONI, C., MOUNEDJI-BOUDIAF, L., NAVARRO, M., TABERNERO, J., HICKISH, T., TOPHAM, C., ZANINELLI, M., CLINGAN, P., BRIDGEWATER, J., TABAH-FISCH, I. & DE GRAMONT, A. (2004). Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer. N. Engl. J. Med., 350, 2343-2351.
3. BOUHOURS, M., STERNBERG, D., DAVOINE, C.S., FERRER, X., WILLER, J.C., FONTAINE, B. & TABTI, N. (2004). Functional characterization and cold sensitivity of T1313A, a new mutation of the skeletal muscle sodium channel causing paramyotonia congenita in humans. J. Physiol., 554, 635-647.
4. BRAIN, K.L. & BENNETT, M.R. (1997). Calcium in sympathetic varicosities of mouse vas deferens during facilitation, augmentation and autoinhibition. J. Physiol., 502 (Part 3), 521-536.
5. BRAIN, K.L., TROUT, S.J., JACKSON, V.M., DASS, N. & CUNNANE, T.C. (2001). Nicotine induces calcium spikes in single nerve terminal varicosities: a role for intracellular calcium stores. Neuroscience, 106, 395-403.
6. BROCK, J.A. & CUNNANE, T.C. (1992). Impulse conduction in sympathetic nerve terminals in the guinea-pig vas deferens and the role of the pelvic ganglia. Neuroscience, 47, 185-196.
7. BURNSTOCK, G. (1976). Do some nerve cells release more than one transmitter? Neuroscience, 1, 239-248.
8. CANNON, S.C. (1997). From mutation to myotonia in sodium channel disorders. Neuromuscul. Disord., 7, 241-249.
9. CARIGNANI, C., RONCARATI, R., RIMINI, R. & TERSTAPPEN, G.C. (2002). Pharmacological and molecular characterisation of SK3 channels in the TE671 human medulloblastoma cell line. Brain Res., 939, 11-18.
10. CESTELE, S. & CATTERALL, W.A. (2000). Molecular mechanisms of neurotoxin action on voltage-gated sodium channels. Biochimie, 82, 883-892.
11. CVITKOVIC, E. & BEKRADDA, M. (1999). Oxaliplatin: a new therapeutic option in colorectal cancer. Semin. Oncol., 26, 647-662.
12. ELLIOTT, P. (1990). Action of antiepileptic and anaesthetic drugs on Na- and Ca-spikes in mammalian non-myelinated axons. Eur. J. Pharmacol., 175, 155-163.
13. EXTRA, J.M., MARTY, M., BRIENZA, S. & MISSET, J.L. (1998). Pharmacokinetics and safety profile of oxaliplatin. Semin. Oncol., 25, 13-22.
14. GAMELIN, L., BOISDRON-CELLE, M., DELVA, R., GUERIN-MEYER, V., IFRAH, N., MOREL, A. & GAMELIN, W. (2004). Prevention of oxaliplatin-related neurotoxicity by calcium and magnesium infusions: a retrospective study of 161 patients receiving oxaliplatin combined with 5-Fluorouracil and leucovorin for advanced colorectal cancer. Clin. Cancer Res., 10, 4055-4061.
15. GILLES, N., CHEN, H., WILSON, H., LE GALL, F., MONTOYA, G., MOLGO, J., SCHONHERR, R., NICHOLSON, G., HEINEMANN, S.H. & GORDON, D. (2000). Scorpion alpha and alpha-like toxins differentially interact with sodium channels in mammalian CNS and periphery. Eur. J. Neurosci., 12, 2823-2832.
16. GIOVANNINI, F., SHER, E., WEBSTER, R., BOOT, J. & LANG, B. (2002). Calcium channel subtypes contributing to acetylcholine release from normal, 4-aminopyridine-treated and myasthenic syndrome auto-antibodies-affected neuromuscular junctions. Br. J. Pharmacol., 136, 1135-1145.
17. GROLLEAU, F., GAMELIN, L., BOISDRON-CELLE, M., LAPIED, B., PELHATE, M. & GAMELIN, E. (2001). A possible explanation for a neurotoxic effect of the anticancer agent oxaliplatin on neuronal voltage-gated sodium channels. J. Neurophysiol., 85, 2293-2297.
18. GROVER, A.K. & KWAN, C.Y. (1984). ATP-dependent Ca-uptake by rat vas deferens smooth muscle micro somes: properties of oxalate stimulated and oxalate-independent Ca-uptake. Arch. Int. Pharmacodyn. Ther., 267, 4-12.
19. + channels are implicated in neuromyotonia. Ann. Neurol., 41, 238-246.
20. JACKSON, V.M., TROUT, S.J., BRAIN, K.L. & CUNNANE, T.C. (2001). Characterization of action potential-evoked calcium transients in mouse postganglionic sympathetic axon bundles. J. Physiol., 537, 3-16.
21. KATZ, B. & THESLEFF, S. (1957). On the factors which determine the amplitude of the miniature end-plate potential. J. Physiol., 137, 267-278.
22. KERN, W., BRAESS, J., BOTTGER, B., KAUFMANN, C.C., HIDDEMANN, W. & SCHLEYER, E. (1999). Oxaliplatin pharmacokinetics during a four-hour infusion. Clin. Cancer Res., 5, 761-765.
23. KINALI, M., JUNGBLUTH, H., EUNSON, L.H., SEWRY, C.A., MANZUR, A.Y., MERCURI, E., HANNA, M.G. & MUNTONI, F. (2004). Expanding the phenotype of potassium channelopathy: severe neuromyotonia and skeletal deformities without prominent Episodic Ataxia. Neuromuscul. Disord., 14, 689-693.
24. KINOSHITA, E., MAEJIMA, H., YAMAOKA, K., KONNO, K., KAWAI, N., SHIMIZU, E., YOKOTE, S., NAKAYAMA, H. & SEYAMA, I. (2001). Novel wasp toxin discriminates between neuronal and cardiac sodium channels. Mol. Pharmacol., 59, 1457-1463.
25. LEHKY, T.J., LEONARD, G.D., WILSON, R.H., GREM, J.L. & FLOETER, M.K. (2004). Oxaliplatin-induced neurotoxicity: acute hyperexcitability and chronic neuropathy. Muscle Nerve, 29, 387-392.
26. LERSCH, C., SCHMELZ, R., ECKEL, F., ERDMANN, J., MAYR, M., SCHULTE-FROHLINDE, E., QUASTHOFF, S., GROSSKREUTZ, J. & ADELSBERGER, H. (2002). Prevention of oxaliplatin-induced peripheral sensory neuropathy by carbamazepine in patients with advanced colorectal cancer. Clin. Colorectal Cancer, 2, 54-58.
27. MEIJER, C., DE VRIES, E.G., MARMIROLI, P., TREDICI, G., FRATTOLA, L. & CAVALETTI, G. (1999). Cisplatin-induced DNA-platination in experimental dorsal root ganglia neuronopathy. Neurotoxicology, 20, 883-887.
28. MISSET, J.L., BLEIBERG, H., SUTHERLAND, W., BEKRADDA, M. & CVITKOVIC, E. (2000). Oxaliplatin clinical activity: a review. Crit. Rev. Oncol. Hematol., 35, 75-93.
29. MOLGO, J., COMELLA, J.X. & LEGRAND, A.M. (1990). Ciguatoxin enhances quantal transmitter release from frog motor nerve terminals. Br. J. Pharmacol., 99, 695-700.
30. NEWSOM-DAVIS, J. (2004). Neuromyotonia. Rev. Neurol. (Paris), 160, S85-S89.
31. O'CONNOR, S.C., BRAIN, K.L. & BENNETT, M.R. (1999). Individual sympathetic varicosities possess different sensitivities to alpha 2 and P2 receptor agonists and antagonists in mouse vas deferens. Br. J. Pharmacol., 128, 1739-1753.
32. OLIVEIRA, M.J., FONTANA, M.D., GIGLIO, J.R., SAMPAIO, S.V., CORRADO, A.P. & PRADO, W.A. (1989). Effects of the venom of the Brazilian scorpion Tityus serrulatus and two of its fractions on the isolated diaphragm of the rat. Gen. Pharmacol., 20, 205-210.
33. PENDYALA, L. & CREAVEN, P.J. (1993). In vitro cytotoxicity, protein binding, red blood cell partitioning, and biotransformation of oxaliplatin. Cancer Res., 53, 5970-5976.
34. PENDYALA, L., KIDANI, Y., PEREZ, R., WILKES, J., BERNACKI, R.J. & CREAVEN, P.J. (1995). Cytotoxicity, cellular accumulation and DNA binding of oxaliplatin isomers. Cancer Lett., 97, 177-184.
35. QUASTHOFF, S. & HARTUNG, H.P. (2002). Chemotherapy-induced peripheral neuropathy. J. Neurol., 249, 9-17.
36. RAYMOND, E., FAIVRE, S., WOYNAROWSKI, J.M. & CHANEY, S.G. (1998). Oxaliplatin: mechanism of action and antineoplastic activity. Semin. Oncol., 25, 4-12.
37. RONCARATI, R., DI CHIO, M., SAVA, A., TERSTAPPEN, G.C. & FUMAGALLI, G. (2001). Presynaptic localization of the small conductance calcium-activated potassium channel SK3 at the neuromuscular junction. Neuroscience, 104, 253-262.
38. SAHARA, Y., GOTOH, M., KONNO, K., MIWA, A., TSUBOKAWA, H., ROBINSON, H.P. & KAWAI, N. (2000). A new class of neurotoxin from wasp venom slows inactivation of sodium current. Eur. J. Neurosci., 12, 1961-1970.
39. TAIEB, S., TRILLET-LENOIR, V., RAMBAUD, L., DESCOS, L. & FREYER, G. (2002). Lhermitte sign and urinary retention: atypical presentation of oxaliplatin neurotoxicity in four patients. Cancer, 94, 2434-2440.
40. TAXI, J. (1965). Contribution a l'étude des connexions des neurones moteurs du système nerveux autonomie. Ann. Sci. Nat. Zool. Biol. Anim., 7, 413-674.
41. THOMSEN, R.H. & WILSON, D.F. (1983). Effects of 4-aminopyridine and 3,4-diaminopyridine on transmitter release at the neuromuscular junction. J. Pharmacol. Exp. Ther., 227, 260-265.
42. WALDRON, R.T., SHORT, A.D. & GILL, D.L. (1995). Thapsigargin- resistant intracellular calcium pumps. Role in calcium pool function and growth of thapsigargin-resistant cells. J. Biol. Chem., 270, 11955-11961.
43. + channels by the novel antiepileptic compound DCUKA: identification of the diphenyl-ureido moiety as an inactivation modifier. Exp. Neurol., 178, 129-138.
44. WILSON, R.H., LEHKY, T., THOMAS, R.R., QUINN, M.G., FLOETER, M.K. & GREM, J.L. (2002). Acute oxaliplatin-induced peripheral nerve hyperexcitability. J. Clin. Oncol., 20, 1767-1774.
45. WISEMAN, L.R., ADKINS, J.C., PLOSKER, G.L. & GOA, K.L. (1999). Oxaliplatin: a review of its use in the management of metastatic colorectal cancer. Drugs Aging, 14, 459-475.
46. + current by imipramine and related compounds: different binding kinetics as an inactivation stabilizer and as an open channel blocker. Mol. Pharmacol., 62, 1228-1237.