Brevetoxin-induced phosphorylation of Pyk2 and Src in murine neocortical neurons involves distinct signaling pathways

Brain Research

Volumn 1184, Issue 1, 2007, Pages 17-27

  Cao, Zhengyu ^a   George, Joju ^a   Baden, Daniel G ^b   Murray, Thomas F ^a  

^a CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

Author keywords

Brevetoxin; mGluR; Neocortical neuron; PKC; Pyk2; Src

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; BREVETOXIN; CALCIUM; FOCAL ADHESION KINASE 2; GUANINE NUCLEOTIDE BINDING PROTEIN; METABOTROPIC RECEPTOR 5; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE C INHIBITOR; PROTEIN TYROSINE KINASE; RO 318425; ROTTLERIN; TYROSINE; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ARTICLE; BRAIN CELL; CALCIUM TRANSPORT; CONTROLLED STUDY; DRUG EFFECT; DRUG INHIBITION; ENZYME ACTIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANALYSIS OF VARIANCE; ANIMALS; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EMBRYO, MAMMALIAN; ENZYME ACTIVATION; ENZYME INHIBITORS; FOCAL ADHESION KINASE 2; MARINE TOXINS; MICE; NEOCORTEX; NEURONS; NEUROTOXINS; OXOCINS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

DINOPHYCEAE; KARENIA BREVIS; MURINAE;

EID: 36348956805     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.09.065     Document Type: Article

References (54)

1. Alier K.A., and Morris B.J. Divergent regulation of Pyk2/CAKbeta phosphorylation by Ca2+ and cAMP in the hippocampus. Biochim. Biophys. Acta 1745 (2005) 342-349
2. Amos S., Martin P.M., Polar G.A., Parsons S.J., and Hussaini I.M. Phorbol 12-myristate 13-acetate induces epidermal growth factor receptor transactivation via protein kinase Cdelta/c-Src pathways in glioblastoma cells. J. Biol. Chem. 280 (2005) 7729-7738
3. Andreev J., Galisteo M.L., Kranenburg O., Logan S.K., Chiu E.S., Okigaki M., Cary L.A., Moolenaar W.H., and Schlessinger J. Src and Pyk2 mediate G-protein-coupled receptor activation of epidermal growth factor receptor (EGFR) but are not required for coupling to the mitogen-activated protein (MAP) kinase signaling cascade. J. Biol. Chem. 276 (2001) 20130-20135
4. Attucci S., Carla V., Mannaioni G., and Moroni F. Activation of type 5 metabotropic glutamate receptors enhances NMDA responses in mice cortical wedges. Br. J. Pharmacol. 132 (2001) 799-806
5. Baden D.G. Brevetoxins: unique polyether dinoflagellate toxins. FASEB J. 3 (1989) 1807-1817
6. Baden D.G., and Mende T.J. Toxicity of two toxins from the Florida red tide marine dinoflagellate, Ptychodiscus brevis. Toxicon 20 (1982) 457-461
7. Bayer A.L., Heidkamp M.C., Howes A.L., Heller Brown J., Byron K.L., and Samarel A.M. Protein kinase C epsilon-dependent activation of proline-rich tyrosine kinase 2 in neonatal rat ventricular myocytes. J. Mol. Cell. Cardiol. 35 (2003) 1121-1133
8. Benson J.M., Tischler D.L., and Baden D.G. Uptake, tissue distribution, and excretion of brevetoxin 3 administered to rats by intratracheal instillation. J. Toxicol. Environ. Health, Part A 57 (1999) 345-355
9. Berman F.W., and Murray T.F. Brevetoxins cause acute excitotoxicity in primary cultures of rat cerebellar granule neurons. J. Pharmacol. Exp. Ther. 290 (1999) 439-444
10. Berman F.W., and Murray T.F. Brevetoxin-induced autocrine excitotoxicity is associated with manifold routes of Ca2+ influx. J. Neurochem. 74 (2000) 1443-1451
11. Bossart G.D., Baden D.G., Ewing R.Y., Roberts B., and Wright S.D. Brevetoxicosis in manatees (Trichechus manatus latirostris) from the 1996 epizootic: gross, histologic, and immunohistochemical features. Toxicol. Pathol. 26 (1998) 276-282
12. Butler B., and Blystone S.D. Tyrosine phosphorylation of beta3 integrin provides a binding site for Pyk2. J. Biol. Chem. 280 (2005) 14556-14562
13. Cataldi M., Taglialatela M., Guerriero S., Amoroso S., Lombardi G., di Renzo G., and Annunziato L. Protein-tyrosine kinases activate while protein-tyrosine phosphatases inhibit L-type calcium channel activity in pituitary GH3 cells. J. Biol. Chem. 271 (1996) 9441-9446
14. Cattet M., and Geraci J.R. Distribution and elimination of ingested brevetoxin (PbTx-3) in rats. Toxicon 31 (1993) 1483-1486
15. Cestele S., and Catterall W.A. Molecular mechanisms of neurotoxin action on voltage-gated sodium channels. Biochimie 82 (2000) 883-892
16. Corvol J.C., Valjent E., Toutant M., Enslen H., Irinopoulou T., Lev S., Herve D., and Girault J.A. Depolarization activates ERK and proline-rich tyrosine kinase 2 (PYK2) independently in different cellular compartments in hippocampal slices. J. Biol. Chem. 280 (2005) 660-668
17. Dikic I., Tokiwa G., Lev S., Courtneidge S.A., and Schlessinger J. A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation. Nature 383 (1996) 547-550
18. Dravid S.M., Baden D.G., and Murray T.F. Brevetoxin activation of voltage-gated sodium channels regulates Ca dynamics and ERK1/2 phosphorylation in murine neocortical neurons. J. Neurochem. 89 (2004) 739-749
19. Dravid S.M., Baden D.G., and Murray T.F. Brevetoxin augments NMDA receptor signaling in murine neocortical neurons. Brain Res. 1031 (2005) 30-38
20. Ellis S. Brevetoxins: chemistry and pharmacology of 'red tide' toxins from Ptychodiscus brevis (formerly Gymnodinium breve). Toxicon 23 (1985) 469-472
21. Fadool D.A., Holmes T.C., Berman K., Dagan D., and Levitan I.B. Tyrosine phosphorylation modulates current amplitude and kinetics of a neuronal voltage-gated potassium channel. J. Neurophysiol. 78 (1997) 1563-1573
22. Girault J.A., Costa A., Derkinderen P., Studler J.M., and Toutant M. FAK and PYK2/CAKbeta in the nervous system: a link between neuronal activity, plasticity and survival?. Trends Neurosci. 22 (1999) 257-263
23. Grishin A.A., Benquet P., and Gerber U. Muscarinic receptor stimulation reduces NMDA responses in CA3 hippocampal pyramidal cells via Ca2+-dependent activation of tyrosine phosphatase. Neuropharmacology 49 (2005) 328-337
24. Heidinger V., Manzerra P., Wang X.Q., Strasser U., Yu S.P., Choi D.W., and Behrens M.M. Metabotropic glutamate receptor 1-induced upregulation of NMDA receptor current: mediation through the Pyk2/Src-family kinase pathway in cortical neurons. J. Neurosci. 22 (2002) 5452-5461
25. Heidkamp M.C., Scully B.T., Vijayan K., Engman S.J., Szotek E.L., and Samarel A.M. PYK2 regulates SERCA2 gene expression in neonatal rat ventricular myocytes. Am. J. Physiol., Cell Physiol. 289 (2005) C471-C482
26. Huang Y., Lu W., Ali D.W., Pelkey K.A., Pitcher G.M., Lu Y.M., Aoto H., Roder J.C., Sasaki T., Salter M.W., and MacDonald J.F. CAKbeta/Pyk2 kinase is a signaling link for induction of long-term potentiation in CA1 hippocampus. Neuron 29 (2001) 485-496
27. Huo J.Z., Dykstra C.M., and Gurd J.W. Increase in tyrosine phosphorylation of the NMDA receptor following the induction of status epilepticus. Neurosci. Lett. 401 (2006) 266-270
28. Ishida H., Nozawa A., Nukaya H., Tsuji K., Kaspar H., Berkett N., and Kosuge T. Isolation and structure determination of a new marine neurotoxin from the New Zealand shellfish, Austrovenus stutchburyi. Toxicon 32 (1994) 1672-1674
29. Jeglitsch G., Rein K., Baden D.G., and Adams D.J. Brevetoxin-3 (PbTx-3) and its derivatives modulate single tetrodotoxin-sensitive sodium channels in rat sensory neurons. J. Pharmacol. Exp. Ther. 284 (1998) 516-525
30. Kalia L.V., Gingrich J.R., and Salter M.W. Src in synaptic transmission and plasticity. Oncogene 23 (2004) 8007-8016
31. Kato K., and Murota S.I. NMDA receptor stimulation in the absence of extracellular Ca2+ potentiates Ca2+ influx-dependent cell death system. Brain Res. 1035 (2005) 177-187
32. Kohling R. Voltage-gated sodium channels in epilepsy. Epilepsia 43 (2002) 1278-1295
33. Lev S., Moreno H., Martinez R., Canoll P., Peles E., Musacchio J.M., Plowman G.D., Rudy B., and Schlessinger J. Protein tyrosine kinase PYK2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions. Nature 376 (1995) 737-745
34. Lu Y.M., Jia Z., Janus C., Henderson J.T., Gerlai R., Wojtowicz J.M., and Roder J.C. Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP. J. Neurosci. 17 (1997) 5196-5205
35. Lu W.Y., Xiong Z.G., Lei S., Orser B.A., Dudek E., Browning M.D., and MacDonald J.F. G-protein-coupled receptors act via protein kinase C and Src to regulate NMDA receptors. Nat. Neurosci. 2 (1999) 331-338
36. Mannaioni G., Marino M.J., Valenti O., Traynelis S.F., and Conn P.J. Metabotropic glutamate receptors 1 and 5 differentially regulate CA1 pyramidal cell function. J. Neurosci. 21 (2001) 5925-5934
37. McFarren E.F., Silva F.J., Tanabe H., Wilson W.B., Campbell J.E., and Lewis K.H. The occurrence of a ciguatera-like poison in oysters, clams, and Gymnodinium breve cultures. Toxicon 3 (1965) 111-123
38. Moss S.J., Gorrie G.H., Amato A., and Smart T.G. Modulation of GABAA receptors by tyrosine phosphorylation. Nature 377 (1995) 344-348
39. Moyers J.S., Bouton A.H., and Parsons S.J. The sites of phosphorylation by protein kinase C and an intact SH2 domain are required for the enhanced response to beta-adrenergic agonists in cells overexpressing c-src. Mol. Cell. Biol. 13 (1993) 2391-2400
40. O'Shea T.J., Rathbun G.B., Buergelt C.D., and Odell D.K. An epizootic of Florida manatees associated with a dinoflagellate bloom. Mar. Mamm. Sci. 7 (1991) 165-179
41. Park S.Y., Avraham H.K., and Avraham S. RAFTK/Pyk2 activation is mediated by trans-acting autophosphorylation in a Src-independent manner. J. Biol. Chem. 279 (2004) 33315-33322
42. Pierce R.H. Red tide (Ptychodiscus brevis) toxin aerosols: a review. Toxicon 24 (1986) 955-965
43. Poli, M.A., Mende, T.J., Baden, D.G., 1986. Brevetoxins, unique activators of voltage-sensitive sodium channels, bind to specific sites in rat brain synaptosomes, Mol Pharmacol, 30, 129-135.
44. Sorokin A., Kozlowski P., Graves L., and Philip A. Protein-tyrosine kinase Pyk2 mediates endothelin-induced p38 MAPK activation in glomerular mesangial cells. J. Biol. Chem. 276 (2001) 21521-21528
45. Templeton C.B., Poli M.A., and Solow R. Prophylactic and therapeutic use of an anti-brevetoxin (PbTx-2) antibody in conscious rats. Toxicon 27 (1989) 1389-1395
46. Vondriska T.M., Zhang J., Song C., Tang X.L., Cao X., Baines C.P., Pass J.M., Wang S., Bolli R., and Ping P. Protein kinase C epsilon-Src modules direct signal transduction in nitric oxide-induced cardioprotection: complex formation as a means for cardioprotective signaling. Circ. Res. 88 (2001) 1306-1313
47. Wan Q., Man H.Y., Braunton J., Wang W., Salter M.W., Becker L., and Wang Y.T. Modulation of GABAA receptor function by tyrosine phosphorylation of beta subunits. J. Neurosci. 17 (1997) 5062-5069
48. Wang Y.T., and Salter M.W. Regulation of NMDA receptors by tyrosine kinases and phosphatases. Nature 369 (1994) 233-235
49. Wang K., Hackett J.T., Cox M.E., Van Hoek M., Lindstrom J.M., and Parsons S.J. Regulation of the neuronal nicotinic acetylcholine receptor by SRC family tyrosine kinases. J. Biol. Chem. 279 (2004) 8779-8786
50. Wayman G.A., Impey S., Marks D., Saneyoshi T., Grant W.F., Derkach V., and Soderling T.R. Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 50 (2006) 897-909
51. Wilkinson S.E., Parker P.J., and Nixon J.S. Isoenzyme specificity of bisindolylmaleimides, selective inhibitors of protein kinase C. Biochem. J. 294 Pt 2 (1993) 335-337
52. Yu X.M. The role of intracellular sodium in the regulation of NMDA-receptor-mediated channel activity and toxicity. Mol. Neurobiol. 33 (2006) 63-80
53. Yu X.M., and Salter M.W. Gain control of NMDA-receptor currents by intracellular sodium. Nature 396 (1998) 469-474
54. Yu X.M., Askalan R., Keil G.J., and Salter M.W. NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science 275 (1997) 674-678