Palytoxin induces cell lysis by priming a two-step process in MCF-7 cells

Chemical Research in Toxicology

Volumn 24, Issue 8, 2011, Pages 1283-1296

  Prandi, Simone ^a   Sala, Gian Luca ^a   Bellocci, Mirella ^a   Alessandrini, Andrea ^a,b   Facci, Paolo ^b   Bigiani, Albertino ^a   Rossini, Gian Paolo ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); PALYTOXIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; CELL MEMBRANE; CELL STRAIN MCF 7; CELL STRUCTURE; CONTROLLED STUDY; CYTOLYSIS; CYTOSKELETON; DRUG MECHANISM; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; PATCH CLAMP;

ACRYLAMIDES; APOPTOSIS; CELL LINE, TUMOR; HUMANS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, FLUORESCENCE; OSMOLAR CONCENTRATION; PATCH-CLAMP TECHNIQUES; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 80051748586     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx2001866     Document Type: Article

References (69)

1. Moore, R. E. and Scheuer, P. J. (1971) Palytoxin: a new marine toxin from a coelenterate Science 172, 495-498
2. Kimura, S., Hashimoto, Y., and Yamazato, K. (1972) Toxicity of the zoanthid Palythoa tuberculosa Toxicon 10, 611-617
3. Onuma, Y., Satake, M., Ukena, T., Roux, J., Chanteau, S., Rasolofonirina, N., Ratsimaloto, M., Naoki, H., and Yasumoto, T. (1999) Identification of putative palytoxin as the cause of clupeotoxism Toxicon 37, 55-65 (Pubitemid 28512988)
4. Lenoir, S., Ten-Hage, L., Turquet, J., Quod, J. P., Bernard, C., and Hennion, M. C. (2004) First evidence of palytoxin analogues from an Ostreopsis mascarenensis (Dinophyceae) benthic bloom in Southwestern Indian Ocean J. Phycol. 40, 1042-1051 (Pubitemid 40025128)
5. Ciminiello, P., DellAversano, C., Fattorusso, E., Forino, M., Magno, S., Tartaglione, L., Grillo, C., and Melchiore, N. (2006) The Genoa 2005 outbreak. Determination of palytoxin in Mediterranean Ostreopsis ovata by a new liquid chromatography tandem mass spectrometry method Anal. Chem. 78, 6153-6159 (Pubitemid 44360128)
6. Ciminiello, P., DellAversano, C., Fattorusso, E., Forino, M., Tartaglione, L., Grillo, C., and Melchiorre, N. (2008) Putative palytoxin and its new analogue, ovatoxin-a, in Ostreopsis ovata collected along the Ligurian coasts during the 2006 toxic outbreak J. Am. Soc. Mass Spectrom. 19, 111-120
7. Moore, R. E. and Bartolini, G. (1981) Structure of palytoxin J. Am. Chem. Soc. 103, 2491-2494 (Pubitemid 11039021)
8. Uemura, D., Ueda, K., Hirata, Y., Naoki, H., and Iwashita, T. (1981) Further studies on palytoxin.1 Tetrahedron Lett. 22, 1909-1912
9. Uemura, D., Ueda, K., Hirata, Y., Naoki, H., and Iwashita, T. (1981) Further studies on palytoxin. 2. Structure of palytoxin Tetrahedron Lett. 22, 2781-2784
10. Deeds, J. R. and Schwartz, M. D. (2010) Human risk associated with palytoxin exposure Toxicon 56, 150-162
11. Tubaro, A., Durando, P., Del Favero, G., Ansaldi, F., Icardi, G., Deeds, J. R., and Sosa, S. (2011) Case definitions for human poisonings postulated to palytoxins exposure Toxicon 57, 478-495
12. Rossini, G. P. and Hess, P. (2009) Phycotoxins: Chemistry, Mechanisms of Action and Shellfish Poisoning, in Molecular, Clinical and Environmental Toxicology (Luch, A., Ed.), pp 65-122, Birkhåuser-Verlag AG, Basel, Switzerland.
13. Mangialajo, L., Ganzin, N., Accoroni, S., Asnaghi, V., Blanfunè, A., Cabrini, M., Cattaneo-Vietti, R., Chavanon, F., Chiantore, M., Cohu, S., Costa, E., Fornasaro, D., Grossel, H., Marco-Miralles, F., Masò, M., Reñè, A., Rossi, A. M., Sala, M. M., Thibaut, T., Totti, C., Vila, M., and Lemèe, R. (2011) Trends in Ostreopsis proliferation along the Northern Mediterranean coasts Toxicon 57, 408-420
14. Gallitelli, M., Ungaro, N., Addante, L. M., Gentiloni, N., and Sabbà, C. (2005) Respiratory illness as a reaction to tropical algal blooms occurring in a temperate climate JAMA 293, 2599-2600 (Pubitemid 40741197)
15. Habermann, E. and Chhatwal, G. S. (1982) Ouabain inhibits the increase due to palytoxin of cationic permeability of erythrocytes Naunyn-Schmeidebergs Arch. Pharmacol. 319, 101-107 (Pubitemid 12091327)
16. Gadsby, D. C., Takeuchi, A., Artigas, P., and Reyes, N. (2009) Peering into an ATPase ion pump with single channel recordings Phil. Trans. R. Soc. B 364, 229-238
17. Wu, C. H. (2009) Palytoxin: Membrane mechanism of action Toxicon 54, 1183-1189
18. +-ATPase and the disruption of ion equilibria in biological systems Toxicon 57, 429-439
19. +-ATPase Toxicon 27, 1171-1187
20. Bellocci, M., Sala, G. L., and Prandi, S. (2011) The cytolytic and cytotoxic activities of palytoxin Toxicon 57, 449-459
21. Habermann, E., Ahnert-Hilger, G., Chhatwal, G. S., and Beress, L. (1981) Delayed haemolytic action of palytoxin general characteristics Biochim. Biophys. Acta 649, 481-486 (Pubitemid 12223646)
22. Bignami, G. S. (1993) A rapid and sensitive hemolysis neutralization assay for palytoxins Toxicon 31, 817-820
23. Bellocci, M., Ronzitti, G., Milandri, A., Melchiorre, N., Grillo, C., Poletti, R., Yasumoto, T., and Rossini, G. P. (2008) A cytolytic assay for the measurement of palytoxin based on a cultured monolayer cell line Anal. Biochem. 374, 48-55
24. An addendum has appeared in 2008, 380, 178.
25. Cañete, E. and Diogène, J. (2008) Comparative study of the use of neuroblastoma cells (Neuro-2a) and neuroblastoma × glioma hybrid cells (NG108-15) for the toxic effect quantification of marine toxins Toxicon 52, 541-550
26. Riobò, P., Paz, B., Franco, J. M., Vàzquez, J., and Murado, M. A. (2008) Proposal for a simple and sensitive haemolytic assay for palytoxin. Toxicological dynamics, kinetics, ouabain inhibition and thermal stability Harmful Algae 7, 415-429 (Pubitemid 351626720)
27. Ledreux, A., Krys, S., and Bernard, C. (2009) Suitability of the Neuro-2a cell line for the detection of palytoxin and analogues (neurotoxic phycotoxins) Toxicon 53, 300-308
28. Malaguti, C. and Rossini, G. P. (2002) Recovery of cellular E-cadherin precedes replenishment of estrogen receptor and estrogen-dependent proliferation of breast cancer cells rescued from a death stimulus J. Cell. Physiol. 192, 171-181 (Pubitemid 34747785)
29. Wròblewski, F. and LaDue, J. S. (1956) Serum glutamic pyruvic transaminase in cardiac and hepatic disease Proc. Soc. Exp. Biol. Med. 91, 569-571
30. Butt, H. J. and Jaschke, M. (1995) Calculation of thermal noise in atomic force microscopy Nanotechnology 6, 1-7
31. Alessandrini, A. and Facci, P. (2005) AFM: a versatile tool in biophysics Measurement Sci. Technol. 16, R65-R92
32. Hertz, H. (1882) Ueber die Berührung fester elasticher körper Reine Angew. Mathematik 92, 156-171
33. Radmacher, M., Fritz, M., Kacher, C. M., Cleveland, J. P., and Hansma, P. K. (1996) Measuring the viscoelastic properties of human platelets with the atomic force microscope Biophys. J. 70, 556-567 (Pubitemid 26021495)
34. Domke, J. and Radmacher, M. (1998) Measuring the elastic properties of thin polymer films with the atomic force microscope Langmuir 14, 3320-3325 (Pubitemid 128559765)
35. Plesnila, N., Müller, E., Guretzki, S., Ringel, F., Staub, F., and Baethmann, A. (2000) Effect of hypothermia on the volume of rat glial cells J. Physiol. 523, 155-162 (Pubitemid 30135829)
36. Sunyer, R., Trepat, X., Fredberg, J. J., Farrè, R., and Navajas, D. (2009) The temperature dependence of cell mechanics measured by atomic force microscopy Phys. Biol. 6, 25009
37. Hamill, O. P., Marty, A., Neher, E., Sakmann, B., and Sigworth, F. J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches Pflugers Arch. 391, 85-100 (Pubitemid 11012976)
38. + current that regulates progression through early G1 phase of the cell cycle in MCF-7 human breast cancer cells J. Membr. Biol. 171, 35-46 (Pubitemid 29430637)
39. + channels identification in human breast carcinoma cells: involvement in cell proliferation Biochem. Biophys. Res. Commun. 278, 272-277
40. Gillis, K. D. (1995) Techniques for Membrane Capacitance Measurements, in Single-Channel Recording (Sakmann, B. and Neher, E., Eds.) pp 155-197, Plenum Press, New York.
41. Hille, B. (2001) Ion Channels of Excitable Membranes, Sinauer Associates, Sunderland, MA.
42. Sala, G. L., Bellocci, M., and Rossini, G. P. (2009) The cytotoxicity pathway triggered by palytoxin involves a change in the cellular pool of stress response proteins Chem. Res. Toxicol. 22, 2009-2016
43. 3H transport in frog oocyte by extractive and radioautographic techniques J. Gen. Physiol. 51, 703-730
44. Rossini, G. P. and Malaguti, C. (1994) Nanomolar concentrations of untransformed glucocorticoid receptor in nuclei of intact cells J. Steroid Biochem. Mol. Biol. 51, 291-298
45. Nollet, F., Kools, P., and van Roy, F. (2000) Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members J. Mol. Biol. 299, 551-572
46. Bellocci, M., Sala, G. L., Callegari, F., and Rossini, G. P. (2010) Azaspiracid-1 inhibits endocytosis of plasma membrane proteins in epithelial cells Toxicol. Sci. 117, 109-121
47. Ares, I. R., Cagide, E., Louzao, M. C., Espina, B., Vieytes, M. R., Yasumoto, T., and Botana, L. M. (2009) Ostreocin-D impact on globular actin of intact cells Chem. Res. Toxicol. 22, 374-81
48. Löw, I., Dancker, P., and Wieland, T. (1975) Stabilization of F-actin by phalloidin. reversal of the destabilizing effect of cytochalasin B FEBS Lett. 54, 263-265
49. Schneider, S. W., Yano, Y., Sumpio, B. E., Jena, B. P., Geibel, J. P., Gekle, M., and Oberleithner, H. (1997) Rapid aldosterone-induced cell volume increase of endothelial cells measured by the atomic force microscope Cell Biol. Int. 21, 759-768 (Pubitemid 28454233)
50. Rotsch, C. and Radmacher, M. (2000) Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study Biophys. J. 78, 520-535 (Pubitemid 30207160)
51. Smith, B. A., Tolloczko, B., Martin, J. G., and Grütter, P. (2005) Probing the viscoelastic behavior of cultured airway smooth muscle cells with atomic force microscopy: stiffening induced by cantractile agonist Biophys. J. 88, 2994-3007 (Pubitemid 40976162)
52. Hillebrand, U., Hausberg, M., Lang, D., Stock, C., Riethmüller, C., Callies, C., and Büssemaker, E. (2008) How steroid hormones act on the endothelium: insights by atomic force microscopy Pflugers Arch. 456, 51-60
53. Pelling, A. E., Dawson, D. W., Carreon, D. M., Christiansen, J. J., Shen, R. R., Teitell, M. A., and Gimzewski, J. K. (2007) Distinct contributions of microtubule subtypes to cell membrane shape and stability Nanomedicine 3, 43-52 (Pubitemid 46428186)
54. Oberleithner, H., Callies, C., Kusche-Vihrog, K., Schillers, H., Shahin, V., Riethmüller, C., Macgregor, G. A., and de Wardener, H. E. (2009) Potassium softens vascular endothelium and increases nitric oxide release Proc. Natl. Acad. Sci. U.S.A. 106, 2829-2834
55. Li, Q. S., Lee, G. Y. H., Ong, C. N., and Lim, C. T. (2008) AFM indentation study of breast cancer cells Biochem. Biophys. Res. Commun. 374, 609-613
56. Hoffmann, E. K., Lambert, I. H., and Pedersen, S. F. (2009) Physiology of cell volume regulation in vertebrates Physiol. Rev. 89, 193-277
57. +-ATPase Naunyn-Schmiedebergs Arch. Pharmacol. 323, 261-268 (Pubitemid 13025788)
58. Muramatsu, I., Uemura, D., Fujiwara, M., and Narahashi, T. (1984) Characteristics of palytoxin-induced depolarization in squid axons J. Pharmacol. Exp. Ther. 231, 488-494 (Pubitemid 15178956)
59. Muramatsu, I., Nishio, M., Kigoshi, S., and Uemura, D. (1988) Single ionic channels induced by palytoxin in guinea-pig ventricular myocytes Br. J. Pharmacol. 93, 811-816 (Pubitemid 18093387)
60. Ikeda, M., Mitani, K., and Ito, K. (1988) Palytoxin induces a nonselective cation channel in single ventricular cells of rat Naunyn-Schmeidebergs Arch. Pharmacol. 337, 591-593
61. + efflux from yeast cells expressing the mammalian sodium pump Mol. Pharmacol. 45, 1132-1136 (Pubitemid 24195570)
62. + influx into yeast cells expressing the mammalian sodium pump is due to the formation of a channel within the enzyme Mol. Pharmacol. 49, 49-57 (Pubitemid 26036783)
63. Hirsh, J. K. and Wu, C. H. (1997) Palytoxin-induced single-channel currents from the sodium pump synthesized by in vitro expression Toxicon 35, 169-176 (Pubitemid 27102282)
64. +-ATPase Toxicol. Appl. Pharmacol. 151, 377-384 (Pubitemid 128421801)
65. Li, S. and Wattenberg, E. V. (1999) Cell-type-specific activation of p38 protein kinase cascades by the novel tumor promoter palytoxin Toxicol. Appl. Pharmacol. 160, 109-119 (Pubitemid 29498394)
66. Louzao, M. C., Ares, I. R., Cagide, E., Espiña, B., Vilariño, N., Alfonso, A., Vieytes, M. R., and Botana, L. M. (2011) Palytoxins and cytoskeleton: an overview Toxicon 57, 460-469
67. Tilly, B. C., Gaestel, M., Engel, K., Edixhoven, M. J., and de Jonge, H. R. (1996) Hypo-osmotic cell swelling activates the p38 MAP kinase signalling cascade FEBS Lett. 395, 133-136 (Pubitemid 26356170)
68. Zhang, Z. and Cohen, D. M. (1996) NaCl but not urea activates p38 and jun kinase in mIMCD3 murine inner medullary cells Am. J. Phisiol. 271, F1234-F1238
69. Mounier, N. and Arrigo, A.-P. (2002) Actin cytoskeleton and small heat shock proteins: how do they interact? Cell Stress Chaperones 7, 167-176 (Pubitemid 36133467)