Phospholipase A2 activity of β-bungarotoxin is essential for induction of cytotoxicity on cerebellar granule neurons

Journal of Neurobiology

Volumn 64, Issue 2, 2005, Pages 213-223

  Chen, Yu Jen ^a  

^a YUANPEI UNIVERSITY   (Taiwan)

Author keywords

bungarotoxin; Cerebellar granule neuron; Cytotoxicity; Phospholipase A2

Indexed keywords

ANTIOXIDANT; ARISTOLOCHIC ACID; BETA BUNGAROTOXIN; CALCIUM CHELATING AGENT; CARDIOTOXIN; CASPASE 3; GLYCYRRHIZIC ACID; MELITTIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NITRIC OXIDE SYNTHASE INHIBITOR; PHOSPHOLIPASE A2; PHOSPHOLIPASE A2 INHIBITOR; POTASSIUM CHANNEL BLOCKING AGENT; POTASSIUM CHANNEL STIMULATING AGENT; SNAKE VENOM;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL MEMBRANE; CELL SPECIFICITY; CEREBELLUM; CONTROLLED STUDY; CYTOTOXICITY; DOSE TIME EFFECT RELATION; ENZYME ACTIVITY; GRANULE CELL; MOLECULAR INTERACTION; NERVE CELL; NEUROBLASTOMA; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; STRAIN DIFFERENCE;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BUNGAROTOXINS; CASPASE 3; CASPASES; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; CEREBELLUM; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENZYME INHIBITORS; FREE RADICALS; NEURONS; NEUROTOXINS; PHOSPHOLIPASES A; QUINACRINE; RATS; RATS, WISTAR; TIME FACTORS;

EID: 22144457076     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.20137     Document Type: Article

References (56)

1. Abe T, Alema S, Miledi R. 1977. Isolation and characterization of presynaptically acting neurotoxins from the venom of Bungarus snakes. Eur J Biochem 80:1-12.
2. Altman J. 1972. Postnatal development of the cerebellar cortex in the rat. 3. Maturation of the components of the granular layer. J Comp Neurol 145:465-513.
3. Amruthesh SC, Boerschel MF, McKinney JS, Willoughby KA, Ellis EF. 1993. Metabolism of arachidonic acid to epoxyeicosatrienoic acids, hydroxyeicosatetraenoic acids, and prostaglandins in cultured rat hippocampal astrocytes. J Neurochem 61:150-159.
4. Anderson DC, Parsons SM. 1986. Uncoupling of cholinergic synaptic vesicles by the presynaptic toxin beta-bungarotoxin. J Neurochem 47:1305-1311.
5. Balazs R, Jorgensen OS, Hack N. 1988. N-methyl-D-aspartate promotes the survival of cerebellar granule cells in culture. Neuroscience 27:437-451.
6. Bodis B, Karadi O, Szabo I, Nemeth P, Belagyi J, Mozsik G. 2000. Evidence for the involvement of oxygen free radicals in the ethanol-induced late cellular injury in mouse myeloma cells. J Physiol Paris 94:67-70.
7. Burgoyne RD, Graham ME, Cambray-Deakin M. 1993. Neurotrophic effects of NMDA receptor activation on developing cerebellar granule cells. J Neurocytol 22: 689-695.
8. Camoratto AM, Grandison L. 1985. Evidence supporting a correlation between arachidonic acid release and prolactin secretion from GH3 cells. Endocrinology 116: 1506-1513.
9. Carmignoto G. 2000. Reciprocal communication systems between astrocytes and neurones. Prog Neurobiol 62:561-581.
10. Chang LS, Yang CC. 1993. Separation and characterization of the A chain and B chain in beta 1-bungarotoxin from Bungarus multicinctus (Taiwan banded krait) venom. J Protein Chem 12:469-475.
11. Chao KF, Lin-Shiau SY. 1995. Enhancement of a slow potassium current component by uranyl nitrate and its relation to the antagonism on beta-bungarotoxin in the mouse motor nerve terminal. Neuropharmacology 34: 165-173.
12. Choi DW. 1992. Excitotoxic cell death. J Neurobiol 23: 1261-1276.
13. Dell'Angelica EC, Mullins C, Bonifacino JS. 1999. AP-4, a novel protein complex related to clathrin adaptors. J Biol Chem 274:7278-7285.
14. Dessi F, Charriaut-Marlangue C, Ben-Ari Y. 1994. Glutamate-induced neuronal death in cerebellar culture is mediated by two distinct components: a sodium-chloride component and a calcium component. Brain Res 650: 49-55.
15. Di Iorio P, Kleywegt S, Ciccarelli R, Traversa U, Andrew CM, Crocker CE, Werstiuk ES, Rathbone MP. 2002. Mechanisms of apoptosis induced by purine nucleosides in astrocytes. Glia 38:179-190.
16. Donato NJ, Martin CA, Ferez M, Newman RA, Vidal JC, Etcheverry M. 1996. Regulation of epidermal growth factor receptor activity by crotoxin, a snake venom phospholipase A2 toxin. A novel growth inhibitory mechanism. Biochem Pharmacol 51:1535-1543.
17. Donovan FM, Pike CJ, Cotman CW, Cunningham DD. 1997. Thrombin induces apoptosis in cultured neurons and astrocytes via a pathway requiring tyrosine kinase and RhoA activities. J Neurosci 17:5316-5326.
18. Dufton MJ. 1985. Proteinase inhibitors and dendrotoxins. Sequence classification, structural prediction and structure/activity. Eur J Biochem 153:647-654.
19. Fabisiak JP, Kagan VE, Tyurina YY, Tyurin VA, Lazo JS. 1998. Paraquat-induced phosphatidylserine oxidation and apoptosis are independent of activation of PLA2. Am J Physiol 274:L793-802.
20. Fasanmade AA, Owuor ED, Ee RP, Qato D, Heller M, Kong AN. 2001. Quinacrine induces cytochrome c-dependent apoptotic signaling in human cervical carcinoma cells. Arch Pharm Res 24:126-135.
21. Fletcher JE, Rapuano BE, Condrea E, Yang CC, Ryan M, Rosenberg P. 1980. Comparison of a relatively toxic phospholipase A2 from Naja nigricollis snake venom with that of a relatively non-toxic phospholipase A2 from Hemachatus haemachatus snake venom-II. Pharmacological properties in relationship to enzymatic activity. Biochem Pharmacol 29:1565-1574.
22. Gallo V, Kingsbury A, Balazs R, Jorgensen OS. 1987. The role of depolarization in the survival and differentiation of cerebellar granule cells in culture. J Neurosci 7: 2203-2213.
23. Haas J, Erdo SL. 1991. Quisqualate-induced excitotoxic death of glial cells: transient vulnerability of cultured astrocytes. Glia 4:111-114.
24. Halliwell JV, Dolly JO. 1982. Preferential action of beta-bungarotoxin at nerve terminal regions in the hippocampus. Neurosci Lett 30:321-327.
25. Herkert M, Shakhman O, Schweins E, Becker CM. 2001. Beta-bungarotoxin is a potent inducer of apoptosis in cultured rat neurons by receptor-mediated internalization. Eur J Neurosci 14:821-828.
26. Ho CL, Lee CY. 1983. Mode of neuromuscular blocking action of ceruleotoxin. Toxicon 21:301-307.
27. Ito M. 1984. Granule cells. In: Ito M, editor. The cerebellum and Neural Control. New York: Raven Press, p 74-85.
28. Kini RM, Evans HJ. 1987. Structure-function relationships of phospholipases. The anticoagulant region of phospholipases A2. J Biol Chem 262:14402-14407.
29. Koh JY, Palmer E, Lin A, Cotman CW. 1991. A metabotropic glutamate receptor agonist does not mediate neuronal degeneration in cortical culture. Brain Res 561: 338-343.
30. Kondo K, Narita K, Lee CY. 1978a. Amino acid sequences of the two polypeptide chains in beta1-bungarotoxin from the venom of Bungarus multicinctus. J Biochem (Tokyo) 83:101-115.
31. Kondo K, Toda H, Narita K. 1978b. Characterization of phospholipase A activity of beta1-bungarotoxin from Bungarus multicinctus venom. I. Its enzymatic properties and modification with p-bromophenacyl bromide. J Biochem (Tokyo) 84:1291-1300.
32. Kondo K, Toda H, Narita K, Lee CY. 1982. Amino acid sequence of beta 2-bungarotoxin from Bungarus multicinctus venom. The amino acid substitutions in the B chains. J Biochem (Tokyo) 91:1519-1530.
33. Levi G, Aloisi F, Ciotti MT, Gallo V. 1984. Autoradiographic localization and depolarization-induced release of acidic amino acids in differentiating cerebellar granule cell cultures. Brain Res 290:77-86.
34. Lin-Shiau SY, Fu WM. 1986. Antagonistic action of uranyl nitrate on presynaptic neurotoxins from snake venoms. Neuropharmacology 25:95-101.
35. Lin-Shiau SY, Lin MJ. 1999. Suramin inhibits the toxic effects of presynaptic neurotoxins at the mouse motor nerve terminals. Eur J Pharmacol 382:75-80.
36. Lysko PG, Cox JA, Vigano MA, Henneberry RC. 1989. Excitatory amino acid neurotoxicity at the N-methyl-D-aspartate receptor in cultured neurons: pharmacological characterization. Brain Res 499:258-266.
37. Nakanishi N, Axel R, Shneider NA. 1992. Alternative splicing generates functionally distinct N-methyl-D-aspartate receptors. Proc Natl Acad Sci USA 89:8552-8556.
38. Nishimura RN, Santos D, Fu ST, Dwyer BE. 2000. Induction of cell death by L-alpha-aminoadipic acid exposure in cultured rat astrocytes: relationship to protein synthesis. Neurotoxicology 21:313-320.
39. Okimasu E, Moromizato Y, Watanabe S, Sasaki J, Shiraishi N, Morimoto YM, Miyahara M, Utsumi K. 1983. Inhibition of phospholipase A2 and platelet aggregation by glycyrrhizin, an antiinflammation drug. Acta Med Okayama 37:385-391.
40. Rapuano BE, Yang CC, Rosenberg P. 1986. The relationship between high-affinity noncatalytic binding of snake venom phospholipases A2 to brain synaptic plasma membranes and their central lethal potencies. Biochim Biophys Acta 856:457-470.
41. Rosenberg P, Ghassemi A, Condrea E, Dhillon D, Yang CC. 1989. Do chemical modifications dissociate between the enzymatic and pharmacological activities of beta bungarotoxin and notexin? Toxicon 27:137-159.
42. Rowan EG, Harvey AL. 1988. Potassium channel blocking actions of beta-bungarotoxin and related toxins on mouse and frog motor nerve terminals. Br J Pharmacol 94:839-847.
43. Rowan EG, Pemberton KE, Harvey AL. 1990. On the blockade of acetylcholine release at mouse motor nerve terminals by beta-bungarotoxin and crotoxin. Br J Pharmacol 100:301-304.
44. Shimoyama Y, Sakamoto R, Akaboshi T, Tanaka M, Ohtsuki K. 2001. Characterization of secretory type IIA phospholipase A2 (sPLA2-IIA) as a glycyrrhizin (GL)-binding protein and the GL-induced inhibition of the CK-II-mediated stimulation of sPLA2-IIA activity in vitro. Biol Pharm Bull 24:1004-1008.
45. Strong PN, Heuser JE, Kelly RB. 1977. Selective enzymatic hydrolysis of nerve terminal phospholipids by beta-bungarotoxin: biochemical and morphological studies. Prog Clin Biol Res 15:227-249.
46. Tessier C, Hichami A, Khan NA. 2002. Implication of three isoforms of PLA(2) in human T-cell proliferation. FEBS Lett 520:111-116.
47. Tosaki A, Haseloff RF, Hellegouarch A, Schoenheit K, Martin VV, Das DK, Blasig IE. 1992. Does the antiarrhythmic effect of DMPO originate from its oxygen radical trapping property or the structure of the molecule itself? Basic Res Cardiol 87:536-547.
48. Tseng WP, Lin-Shiau SY. 2003a. Activation of NMDA receptor partly involved in beta-bungarotoxin-induced neurotoxicity in cultured primary neurons. Neurochem Int 42:333-344.
49. Tseng WP, Lin-Shiau SY. 2003b. Calcium-activated NO production plays a role in neuronal death induced by beta-bungarotoxin in primary cultures of cerebellar granular neurons. Naunyn Schmiedebergs Arch Pharmacol 367:451-461.
50. Tseng WP, Lin-Shiau SY. 2003c. Suramin inhibits beta-bungarotoxin-induced activation of N-methyl-D-aspartate receptors and cytotoxicity in primary neurons. Toxicol Appl Pharmacol 189:45-55.
51. Vernon LP, Bell JD. 1992. Membrane structure, toxins and phospholipase A2 activity. Pharmacol Ther 54: 269-295.
52. Wang JY, Chi SI, Hwang CP. 1996. Effects of various nitric oxide synthase inhibitors on NMDA-induced neuronal injury in rat cortical neurons. Chin J Physiol 39:227-233.
53. Wernicke JF, Vanker AD, Howard BD. 1975. The mechanism of action of beta-bungarotoxin. J Neurochem 25: 483-496.
54. Yamauchi M, Omote K, Ninomiya T. 1998. Direct evidence for the role of nitric oxide on the glutamate-induced neuronal death in cultured cortical neurons. Brain Res 780:253-259.
55. Yan GM, Ni B, Weller M, Wood KA, Paul SM. 1994. Depolarization or glutamate receptor activation blocks apoptotic cell death of cultured cerebellar granule neurons. Brain Res 656:43-51.
56. Yates SL, Burns M, Condrea E, Ghassemi A, Shina R, Rosenberg P. 1990. Phospholipid hydrolysis and loss of membrane integrity following treatment of rat brain synaptosomes with beta-bungarotoxin, notexin, and Naja naja atra and Naja nigricollis phospholipase A2. Toxicon 28:939-951.