Mefloquine neurotoxicity is mediated by non-receptor tyrosine kinase

NeuroToxicology

Volumn 32, Issue 5, 2011, Pages 578-585

  Milatovic, Dejan ^a   Jenkins, Jerry W ^b   Hood, Jonathan E ^c   Yu, Yingchun ^a   Rongzhu, Lu ^d   Aschner, Michael ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b HUDSONALPHA INSTITUTE FOR BIOTECHNOLOGY   (United States)

^c CFD RESEARCH CORPORATION   (United States)

^d JIANGSU UNIVERSITY   (China)

Author keywords

Apoptosis; Mefloquine; Neuronal viability; Oxidative stress; Pyk2

Indexed keywords

FOCAL ADHESION KINASE 2; GLUTATHIONE; MEFLOQUINE; SMALL INTERFERING RNA;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; GENE SILENCING; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; MEFLOQUINE; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; TYK2 KINASE;

PLASMODIUM FALCIPARUM; RATTUS;

EID: 82455192351     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2011.01.001     Document Type: Article

References (49)

1. Avraham H., Park S.Y., Schinkmann K., Avraham S. RAFTK/Pyk2-mediated cellular signaling. Cell Signal 2000, 12:123-133.
2. Chellaiah M.A., Kuppuswamy D., Lasky L., Linder S. Phosphorylation of a Wiscott-Aldrich syndrome protein-associated signal complex is critical in osteoclast bone resorption. J Biol Chem 2007, 282:10104-10116.
3. Corvol J.C., Valjent E., Toutant M., Enslen H., Irinopoulou T., Lev S., et al. Depolarization activates ERK and proline-rich tyrosine kinase 2 (PYK2) independently in different cellular compartments in hippocampal slices. J Biol Chem 2005, 280:660-668.
4. Dikic I., Tokiwa G., Lev S., Courtneidge S.A., Schlessinger J. A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation. Nature 1996, 383:547-550.
5. Dow G., Bauman R., Caridha D., Cabezas M., Du F., Gomez-Lobo R., et al. Mefloquine induces dose-related neurological effects in a rat model. Antimicrob Agents Chemother 2006, 50:1045-1053.
6. Dow G.S., Caridha D., Goldberg M., Wolf L., Koenig M.L., Yourick D.L., et al. Transcriptional profiling of mefloquine-induced disruption of calcium homeostasis in neurons in vitro. Genomics 2005, 86:539-550.
7. Dow G.S., Hudson T.H., Vahey M., Koenig M.L. The acute neurotoxicity of mefloquine may be mediated through a disruption of calcium homeostasis and ER function in vitro. Malar J 2003, 2:14.
8. Dow G.S., Koenig M.L., Wolf L., Gerena l., Lopez-Sanchez M., Hudson T.H., et al. The Antimalarial potential of 4-quinolinecarbinolamines may be limited due to neurotoxicity and cross-resistance in mefloquine-resistant Plasmodium falciparum strains. Antimicrob Agents Chemother 2004, 48:2624-2632.
9. Faure C., Corvol J.C., Toutant M., Valjent E., Hvalby O., Jensen V., et al. Calcineurin is essential for depolarization-induced nuclear translocation and tyrosine phosphorylation of PYK2 in neurons. J Cell Sci 2007, 120:3034-3044.
10. Ghosh A., Ginty D.D., Bading H., Greenberg M.E. Calcium regulation of gene expression in neuronal cells. J Neurobiol 1994, 25:294-303.
11. Ginnan R., Singer H.A. CaM kinase II-dependent activation of tyrosine kinases and ERK1/2 in vascular smooth muscle. Am J Physiol: Cell Physiol 2002, 282:C754-C761.
12. Girault J.A., Costa A., Derkinderen P., Studler J.M., Toutant M. FAK and PYK2/CAKbeta in the nervous system: a link between neuronal activity, plasticity and survival?. Trends Neurosci 1999, 22:257-263.
13. Gribble F.M., Davis T.M., Higham C.E., Clark A., Ashcroft F.M. The antimalarial agent mefloquine inhibits ATP-sensitive K-channels. Br J Pharmacol 2000, 131:756-760.
14. Heidinger V., Manzerra P., Wang X.Q., Strasser U., Yu S.P., Choi D.W., et al. Metabotropic glutamate receptor 1-induced upregulation of NMDA receptor current: mediation through the Pyk2/Src-family kinase pathway in cortical neurons. J Neurosci 2002, 22:5452-5461.
15. Hood J.E., Jenkins J.W., Milatovic D., Rongzhu L., Aschner M. Mefloquine induces oxidative stress and neurodegeneration in primary rat cortical neurons. Neurotoxicology 2010, 31:518-523.
16. Huang Y., Lu W., Ali D.W., Pelkey K.A., Pitcher G.M., Lu Y.M., et al. CAKbeta/Pyk2 kinase is a signaling link for induction of long-term potentiation in CA1 hippocampus. Neuron 2001, 29:485-496.
17. Jenkins J. Biological pathway-centric approach to integrative analysis of array data as applied to mefloquine neurotoxicity. J Biomol Tech 2007, 18(83).
18. Jenkins J.W., Hood J.E., Soni A.S., Sundaram S., Aschner M., Jiang C.T. Biological pathway-centric approach to integrative analysis of array data as applied to mefloquine neurotoxicity. The 2007 Annual Meeting Salt Lake City - UT. 657-Genomic Approaches to System Biology 2007.
19. Lev S., Moreno H., Martinez R., Canoll P., Peles E., Musacchio J.M., et al. Protein tyrosine kinase PYK2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions. Nature 1995, 376:737-745.
20. Lim L.Y., Go M.L. The anticholinesterase activity of mefloquine. Clin Exp Pharmacol Physiol 1985, 12:527-531.
21. Maertens C., Wei L., Droogmans G., Nilius B. Inhibition of volume-regulated and calcium-activated chloride channels by the antimalarial mefloquine. J Pharmacol Exp Ther 2000, 295:29-36.
22. McArdle J.J., Sellin L.C., Coakley K.M., Potian J.G., Quinones-Lopez M.C., Rosenfeld C.A., et al. Mefloquine inhibits cholinesterases at the mouse neuromuscular junction. Neuropharmacology 2005, 49:1132-1139.
23. McLaughlin B.A., Nelson D., Silver I.A., Erecinska M., Chesselet M.F. Methylmalonate toxicity in primary neuronal cultures. Neuroscience 1998, 86:279-290.
24. Melendez J., Turner C., Avraham H., Steinberg S.F., Schaefer E., Sussman M.A. Cardiomyocyte apoptosis triggered by RAFTK/pyk2 via Src kinase is antagonized by paxillin. J Biol Chem 2004, 279:53516-53523.
25. Milatovic D., Ascher M. Measurement of isoprostanes as markers of oxidative stress in neuronal tissue. Curr Protoc Toxicol 2009, 39(Unit12.14):1-12.
26. Milatovic D., Zaja-Milatovic S., Montine K.S., Horner P.J., Montine T.J. Pharmacologic suppression of neuronal oxidative damage and dendritic degeneration following direct activation of glial innate immunity in mouse cerebrum. J Neurochem 2003, 87:1518-1526.
27. Milatovic D., Zaja-Milatovic S., Montine K.S., Shie F.S., Montine T.J. Neuronal oxidative damage and dendritic degeneration following activation of CD14-dependent innate immune response in vivo. J Neuroinflammation 2004, 1:20.
28. Morrow J.D., Roberts L.J. Quantification of noncyclooxygenase derived prostanoids as a marker of oxidative stress. Free Radic Biol Med 1991, 10:195-200.
29. Neely M.D., Boutte A., Milatovic D., Montine T.J. Mechanisms of 4-hydroxynonenal-induced neuronal microtubule dysfunction. Brain Res 2005, 1037:90-98.
30. Nevin R.L., Pietrusiack P.P., Caci J.B. Prevalence of contraindications to mefloquine use among USA military personnel deployed to Avganistan. Malar J 2008, 7:1-5.
31. Nicodemo A.A., Pampillo M., Ferreira L.T., Dale L.B., Cregan T., Ribeiro F.M., et al. Pyk2 uncouples metabotropic glutamate receptor G protein signaling but facilitates ERK1/2 activation. Mol Brain 2010, 3:4.
32. Overbosch D., Schilthuis H., Bienzle U., Behrens R.H., Kain K.C., Clarke P.D., et al. Atovaquone-proguanil versus mefloquine for malaria prophylaxis in nonimmune travelers: results from arandomized, double-blind study. Clin Infect Dis 2001, 33:1015-1021.
33. Pussard E., Merzouk M., Barennes H. Increased uptake of quinine into the brain by inhibition of P-glycoprotein. Eur J Pharm Sci 2007, 32:123-127.
34. Rendi-Wagner P., Noedl H., Wernsdorfer W.H., Wiedermann G., Mikolasek A., Kollaritsch H. Unexpected frequency, duration and spectrum of adverse events after therapeutiv dose of mefloquine in healthy adults. Acta Trop 2002, 81:167-173.
35. Rice G.C., Bump E.A., Shrieve D.C., Lee W., Kovacs M. Quantitative analysis of cellular glutathione by flow cytometry utilizing monochlorobimane: some applications to radiation and drug resistance in vitro and in vivo. Cancer Res 1986, 46:6105-6110.
36. Roberts L.J., Morrow J.D. Isoprostanes. Novel markers of endogenous lipid peroxidation and potential mediators of oxidant injury. Ann N Y Acad Sci 1994, 744:237-242.
37. Siciliano J.C., Toutant M., Derkinderen P., Sasaki T., Girault J.A. Differential regulation of proline-rich tyrosine kinase 2/cell adhesion kinase β (PYK2/CAKβ) and pp125FAK by glutamate and depolarization in rat hippocampus. J Biol Chem 1996, 271:28942-28946.
38. Simpson J., Price A., terKuile R., Teja-Isavatharm F., Nosten P., Chongsuphajaisiddhi F., et al. Population pharmacokinetics of mefloquine in patients with acute falciparum malaria. Clin Pharmacol Ther 1999, 66:472-484.
39. Siegel G.J., Agranoff B.W., Albers R.W., Fisher S.K., Uhler M.D. Basic Neurochemistry 1999, Lippincott, Williams & Wilkins, Philadelphia, PA.
40. Strappazzon F., Torch S., Trioulier Y., Blot B., Sadoul R., Verna J.M. Survival response-linked Pyk2 activation during potassium depletion-induced apoptosis of cerebellar granule neurons. Mol Cell Neurosci 2007, 34:3355-3365.
41. Tokiwa G., Dikic I., Lev S., Schlessinger J. Activation of Pyk2 by stress signals and coupling with JNK signaling pathway. Science 1996, 273:792-794.
42. Toovey S. Mefloquine neurotoxicity: a literature review. Travel Med Infect Dis 2009, 7:2-6.
43. Weiss S.M., Benwell K., Cliffe I.A., Gillespie R.J., Knight A.R., Lerpiniere J., et al. Discovery of nonxanthine adenosine A2A receptor antagonists for the treatment of Parkinson's disease. Neurology 2003, 61:S101-S106.
44. World Health and Organization WHO Expert Committee on Malaria. World Malaria Report 2009 2009, World Health Organization, Geneva.
45. Xi C.X., Xiong F., Zhou Z., Mei L., Xiong W.C. PYK2 interacts with MyD88 and regulates MyD88-mediated NF-κB activation in macrophages. J Leukoc Biol 2010, 87:415-423.
46. Xiong W., Parsons J.T. Induction of apoptosis after expression of PYK2, a tyrosine kinase structurally related to focal adhesion kinase. J Cell Biol 1997, 139:529-539.
47. Xiong W.C., Mei L. Roles of FAK family kinases in nervous system. Front Biosci 2003, 8:s676-s682.
48. Zhou C., Xiao C., McArdle J.J., Ye J.H. Mefloquine enhances nigral gamma-aminobutyric acid release via inhibition of cholinesterase. J Pharmacol Exp Ther 2006, 317:1155-1160.
49. Zwick E., Wallasch C., Daub H., Ullrich A. Distinct calcium-dependent pathways of epidermal growth factor receptor transactivation and PYK2 tyrosine phosphorylation in PC12 cells. J Biol Chem 1999, 274:20989-20996.