Cytotoxic responses in BC3H1 myoblast cell lines exposed to 1-desulfoyessotoxin

Toxicology in Vitro

Volumn 27, Issue 6, 2013, Pages 1962-1969

  Korsnes, Mónica Suárez ^a   Espenes, Arild ^a   Hermansen, Lene C ^a   Loader, Jared I ^c,d   Miles, Christopher O ^b,c  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b NORWEGIAN VETERINARY INSTITUTE   (Norway)

^c RUAKURA RESEARCH CENTRE   (New Zealand)

^d CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

1 Desulfoyessotoxin; Cytoplasmic vacuolation; DNA fragmentation; Endoplasmic reticulum; Hsp70; Intracellular signalling; Mitochondria; P38; Paraptosis; Yessotoxin

Indexed keywords

1 DESULFOYESSOTOXIN; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; YESSOTOXIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL STRUCTURE; CELL VACUOLE; CELL VIABILITY; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; ELECTRON MICROSCOPY; FLUORESCENCE MICROSCOPY; MOLECULAR DYNAMICS; MOUSE; MYOBLAST; NONHUMAN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

1-DESULFOYESSOTOXIN; CYTOPLASMIC VACUOLATION; DNA FRAGMENTATION; ENDOPLASMIC RETICULUM; HSP70; INTRACELLULAR SIGNALLING; MITOCHONDRIA; P38; PARAPTOSIS; YESSOTOXIN;

ANIMALS; APOPTOSIS; CELL LINE; CELL SURVIVAL; DNA FRAGMENTATION; ETHERS, CYCLIC; HSP70 HEAT-SHOCK PROTEINS; MICE; MOLLUSK VENOMS; MYOBLASTS; OXOCINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES;

EID: 84880999838     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2013.06.012     Document Type: Article

References (71)

1. Alfonso A., de la Rosa L., Vieytes M.R., Yasumoto T., Botana L.M. Yessotoxin, a novel phycotoxin, activates phosphodiesterase activity: effect of yessotoxin on cAMP levels in human lymphocytes. Biochem. Pharmacol. 2003, 65:193-208.
2. Aune T., Sørby R., Yasumoto T., Ramstad H., Landsverk T. Comparison of oral and intraperitoneal toxicity of yessotoxin towards mice. Toxicon 2002, 40:77-82.
3. Barker R.N., Erwig L., Pearce W.P., Devine A., Rees A.J. Differential effects of necrotic or apoptotic cell uptake on antigen presentation by macrophages. Pathobiology 1999, 67:302-305.
4. Bhanot H., Young A.M., Overmeyer J.H., Maltese W.A. Induction of nonapoptotic cell death by activated ras requires inverse regulation of Rac1 and Arf6. Mol. Cancer Res. 2010, 8:1358-1374.
5. Byun J.Y., Yoon C.H., An S., Park I.C., Kang C.M., Kim M.J., Lee S.J. The rac1/mkk7/jnk pathway signals upregulation of atg5 and subsequent autophagic cell death in response to oncogenic ras. Carcinogenesis 2009, 30:1880-1888.
6. Callegari F., Rossini G.P. Yessotoxin inhibits the complete degradation of E-cadherin. Toxicology 2008, 244:133-144.
7. Chi S., Kitanaka C., Noguchi K., Mochizuki T., Nagashima Y., Shirouzu M., Fujita H., Yoshida M., Chen W., Asai A., Himeno M., Yokoyama S., Kuchino Y. Oncogenic ras triggers cell suicide through the activation of a caspase-independent cell death program in human cancer cells. Oncogene 1999, 18:2281-2290.
8. Choi J.A., Park M.T., Kang C.M., Um H.D., Bae S., Lee K.H., Kim T.H., Kim J.H., Cho C.K., Lee Y.S., Chung H.Y., Lee S.J. Opposite effects of Ha-Ras and Ki-Ras on radiation-induced apoptosis via differential activation of PI3K/Akt and Rac/p38 mitogen-activated protein kinase signaling pathways. Oncogene 2004, 23:9-20.
9. Ciminiello P., Dell'aversano C., Fattorusso E., Forino M., Magno S., Guerrini F., Pistocchi R., Boni L. Complex yessotoxins profile in Protoceratium reticulatum from north-western Adriatic Sea revealed by LC-MS analysis. Toxicon 2003, 42:7-14.
10. +2 channel blockers and kinases. Cell. Signal. 2001, 13:711-716.
11. Dell'Ovo V., Bandi E., Coslovich T., Florio C.M.S., Decorti G., Sosa S., Lorenzon P., Yasumoto T., Tubaro T. In vitro effects of yessotoxin on a primary culture of rat cardiomyocytes. Toxicol. Sci. 2008, 106:392-399.
12. Dominguez H.J., Paz B., Daranas A.H., Norte M., Franco J.M., Fernández J.J. Dinoflagellate polyether within the yessotoxin, pectenotoxin and okadaic acid toxin groups: characterization, analysis and human health implications. Toxicon 2010, 56:191-217.
13. Dunn W.A. Studies on the mechanisms of autophagy: maturation of the autophagic vacuole. J. Cell Biol. 1990, 110:1935-1945.
14. Dunn W.A. Autophagy and related mechanisms of lysosome-mediated protein degradation. Trends Cell Biol. 1994, 4:139-143.
15. Elgendy M., Sheridan C., Brumatti G., Martin S.J. Oncogenic Ras-induced expression of Noxa and Beclin-1 promotes autophagic cell death and limits clonogenic survival. Mol. Cell 2011, 42:23-35.
16. Espenes, A., Aasen, J., Hetland, D., Satake, M., Smith, A., Eraker, N., Aune, T., 2006. Toxicity of yessotoxin in mice after repeated oral exposure. In: Henshilwood, K., Deegan, B., McMahon, T., Cusack, C., Keaveney, S., Silke, J., O'Cinneide, M., Lyons, D., Hess, P. (Eds.), Molluscan Shellfish Safety. Proceedings 5th International Conference on Molluscan Shellfish Safety, Galway, Ireland, June 14th-18th, 2004, pp. 419-423.
17. Ferrari S., Ciminiello P., Dell'Aversano C., Forino M., Malaguti C., Tubaro A., Poletti R., Yasumoto T., Fattorusso E., Rossini G.P. Structure-activity relationships of yessotoxins in cultured cells. Chem. Res. Toxicol. 2004, 17:1251-1257.
18. Franchini A., Marchesini E., Poletti R., Ottaviani E. Lethal and sub-lethal yessotoxin dose-induced morpho-functional alterations in intraperitoneal injected Swiss CD1 mice. Toxicon 2004, 44:83-90.
19. Gallucci S., Matzinger P. Danger signals: SOS to the immune system. Curr. Opin. Immunol. 2001, 13:114-119.
20. Gallucci S., Lolkema M., Matzinger P. Natural adjuvants: endogenous activators of dendritic cells. Nat. Med. 1999, 5:1249-1255.
21. Galluzzi L., Vitale I., Abrams J.M., Alnemri E.S., Baehrecke E.H., Blagosklonny M.V., Dawson T.M., Dawson V.L., El-Deiry W.S., Fulda S., et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell. Death Differ. 2012, 1:107-120.
22. Gordon P.B., Seglen P.O. Prelysosomal convergence of autophagic and endocytic pathways. Biochem. Biophys. Res. Commun. 1988, 151:40-47.
23. Gozuacik D., Kimchi A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 2004, 23:2891-2906.
24. Hoa N., Myers M., Douglass T., Zhang J., Delgado C., Driggers L., Callahan L., VanDeusen G., Pham J., Bhakta N., Ge L., Jadus M.R. Molecular mechanisms of paraptosis induction: implications for a non-genetically modified tumor vaccine. PLoS One 2009, 4:e4631.
25. Ireland H.E., Leoni F., Altaie O., Birch C.S., Coleman R.C., Hunter-Lavin C., Williams J.H. Measuring the secretion of heat shock proteins from cells. Methods 2007, 43:176-183.
26. Jadus M., Chen Y., Boldaji M., Delgado C., Sanchez R., Douglass T., Al-Atar U., Schulz W., Lloyd C., Wepsic H. Human U251MG glioma cells expressing the membrane form of macrophage colony-stimulating factor (mM-CSF) are killed by human monocytes in vitro and are rejected within immunodeficient mice via paraptosis that is associated with increased expression of three different heat shock proteins. Cancer. Gene. Ther. 2003, 10:411-420.
27. Kitanaka C., Kuchino Y. Caspase-independent programmed cell death with necrotic morphology. Cell. Death Differ. 1999, 6:508-515.
28. Korsnes M.S. Yessotoxin as a tool to study induction of multiple cell death pathways. Toxins 2012, 4:568-579.
29. Korsnes M.S., Espenes A. Yessotoxin as an apoptotic inducer. Toxicon 2011, 57:947-958.
30. Korsnes M.S., Hetland D.L., Espenes A., Aune T. Induction of apoptosis by YTX in myoblast cell lines via mitochondrial signalling transduction pathway. Toxicol. In Vitro 2006, 20:1419-1426.
31. Korsnes M.S., Hetland D.L., Espenes A., Tranulis M.A., Aune T. Apoptotic events induced by yessotoxin in myoblast cell lines from rat and mouse. Toxicol. In Vitro 2006, 20:1077-1087.
32. Korsnes M.S., Hetland D.L., Espenes A., Aune T. Cleavage of tensin during cytoskeleton disruption in YTX-induced apoptosis. Toxicol. In Vitro 2007, 21:9-15.
33. Korsnes M.S., Espenes A., Hetland D.L., Hermansen L.C. Paraptosis-like cell death induced by yessotoxin. Toxicol. In Vitro 2011, 25:1764-1770.
34. Kroemer G., Levine B. Autophagic cell death: the story of a misnomer. Nat. Rev. Mol. Cell. Biol. 2008, 9:1004-1010.
35. Lee J.S., Tangen K., Dahl E., Hovgaard P., Yasumoto T. Diarrhetic shellfish toxins in Norwegian mussels. Nippon Suisan Gakkaishi 1988, 54:1953-1957.
36. Loader J., Hawkes A., Beuzenberg V., Jensen D., Cooney J., Wilkins A., Fitzgerald J., Briggs L., Miles C. Convenient large-scale purification of yessotoxin from Protoceratium reticulatum culture and isolation of a novel furanoyessotoxin. J. Agric. Food Chem. 2007, 55:11093-11100.
37. López A.M., Rodríguez J.J.G., Mirón A.S., Camacho F.G., Grima E.M. Immunoregulatory potential of marine algal toxins yessotoxin and okadaic acid in mouse T lymphocyte cell line EL-4. Toxicol. Lett. 2011, 207:167-172.
38. Malagoli D., Marchesini E., Ottaviani E. Lysosomes as the target of yessotoxin in invertebrate and vertebrate cell lines. Toxicol. Lett. 2006, 167:75-83.
39. Martín-López A., Gallardo-Rodríguez J.J., Sánchez-Mirón A., García-Camacho F., Molina-Grima E. Cytotoxicity of yessotoxin and okadaic acid in mouse T lymphocyte cell line EL-4. Toxicon 2012, 60:1049-1056.
40. Mathew R., Karantza-Wadsworth V., White E. Role of autophagy in cancer. Nat. Rev. Cancer 2007, 7:961-967.
41. Mayer M.P., Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 2005, 62:670-684.
42. Melcher A., Todryk S., Hardwick N., Ford M., Jacobson M., Vile R. Tumor immunogenicity is determined by the mechanism of cell death via induction of heat shock protein expression. Nat. Med. 1998, 4:581-587.
43. Miles C.O., Samdal I.A., Aasen J.A.B., Jensen D.J., Quilliam M.A., Petersen D., Briggs L.M., Wilkins A.L., Rise F., Cooney J.M., MacKenzie A.L. Evidence of numerous analogs of yessotoxin in Protoceratium reticulatum. Harmful Algae 2005, 4:1075-1091.
44. Murata M., Kumagai M., Lee J.S., Yasumuto T. Isolation and structure of yessotoxin, a novel polyether compound implicated in diarrhetic shellfish poisining. Tetrahedron Lett. 1987, 28:5869-5872.
45. Njemini R., Abeele M.V., Demanet C., Lambert M., Vandebosch S., Mets T. Age-related decrease in the inducibility of heat-shock protein 70 in human peripheral blood mononuclear cells. J. Clin. Immunol. 2002, 22:195-205.
46. Ogino H., Kumagai M., Yasumoto T. Toxicologic evaluation of yessotoxin. Nat. Toxins 1997, 5:255-259.
47. Orsi C.F., Colombari B., Callegari F., Todaro A.M., Ardizzoni A., Rossini G.P., Blasi E., Peppoloni S. Yessotoxin inhibits phagocytic activity of macrophages. Toxicon 2010, 55:265-273.
48. Overmeyer J.H., Maltese W.A. Death pathways triggered by activated ras in cancer cells. Front. Biosci. 2011, 16:1693-1713.
49. Overmeyer J.H., Kaul A., Johnson E.E., Maltese W.A. Active ras triggers death in glioblastoma cells through hyperstimulation of macropinocytosis. Mol. Cancer Res. 2008, 6:965-977.
50. Pandey K.B., Mishra N., Rizvi S.I. Protein oxidation biomarkers in plasma of type 2 diabetic patients. Clin. Biochem. 2010, 43:508-511.
51. Pang M., Wang Z.L., Gao C.L., Qu P., Li H.D. Characterization of apoptotic changes induced by yessotoxin in the Bel7402 human hepatoma cell line. Mol. Med. Rep. 2011, 4:547-552.
52. Paz B., Riobo P., Fernandez M.L., Fraga S., Franco J.M. Production and release of yessotoxins by the dinoflagellates Protoceratium reticulatum and Lingulodinium polyedrum in culture. Toxicon 2004, 44:251-258.
53. Paz B., Daranas A.H., Norte M., Riobó P., Franco J.M., Fernández J.J. Yessotoxins, a group of marine polyether toxins: an overview. Mar. Drugs 2008, 6:73-102.
54. Pérez-Gómez A., Ferrerro-Gutiérrez A., Novelli A., Franco J.M., Paz B., Fernández-Sánchez M.T. Potent neurotoxic action of the shellfish biotoxin yessotoxin on cultured cerebellar neurons. Toxicol. Sci. 2006, 90:168-177.
55. Racoosin E.L., Swanson J.A. M-CSF-induced macropinocytosis increases solute endocytosis but not receptor-mediated endocytosis in mouse macrophages. J. Cell Sci. 1992, 102(Pt 4):867-880.
56. Rhodes L., McNabb P., De Salas M., Briggs L., Beuzenberg V., Gladstone M. Yessotoxin production by Gonyaulax spinifera. Harmful Algae 2006, 5:148-155.
57. Roberts S.P., Feder M.E. Natural hyperthermia and expression of the heat shock protein Hsp70 affect developmental abnormalities in Drosophila melanogaster. Oecologia 1999, 121:323-329.
58. Sabehat A., Lurie S., Weiss D. Expression of small heat-shock proteins at low temperatures A possible role in protecting against chilling injuries. Plant Physiol. 1998, 117:651-658.
59. Samdal I.A., Naustvoll L.J., Olseng C.D., Briggs L.R., Miles C.O. Use of ELISA to identify Protoceratium reticulatum as a source of yessotoxin in Norway. Toxicon 2004, 44:75-82.
60. Satake M., MacKenzie L., Yasumoto T. Identification of Protoceratium reticulatum as the biogenetic origin of yessotoxin. Nat. Toxins 1997, 4:164-167.
61. Søti C., Nagy E., Giricz Z., Vigh L., Csermely P., Ferdinandy P. Heat shock proteins as emerging therapeutic targets. Br. J. Pharmacol. 2005, 146:769-780.
62. Sperandio S., de Belle I., Bredesen D.E. An alternative, nonapoptotic form of programmed cell death. Proc. Natl. Acad. Sci. USA. 2000, 97:14376-14381.
63. Sperandio S., Poksay K., de Belle I., Lafuente M.J., Liu B., Nasir J., Bredesen D.E. Paraptosis: mediation by MAP kinases and inhibition by AIP-1/Alix. Cell. Death Differ. 2004, 11:1066-1075.
64. Takahashi H., Kusumi T., Kan Y., Satake M., Yasumoto T. Determination of the absolute configuration of yessotoxin, a polyether compound implicated in diarrhetic shellfish poisoning, by NMR spectroscopic method using a chiral anisotropic reagent, methoxy-(2-naphthyl)acetic acid. Tetrahedron Lett. 1996, 37:7087-7090.
65. Terao K., Ito E., Oarada M., Murata M., Yasumoto T. Histopathological studies on experimental marine toxin poisoning - 5 the effects in mice of yessotoxin isolated from Patinopecten yessoensis and of a desulfated derivative. Toxicon 1990, 28:1095-1104.
66. Tobio A., Fernández-Araujo A., Alfonso A., Botana L.M. Role of yessotoxin in calcium and cAMP-crosstalks in primary and K-562 human lymphocytes: the effect is mediated by anchor kinase A mitochondrial proteins. J. Cell Biochem. 2012, 113:3752-3761.
67. Tubaro A., Sosa S., Carbonatto M., Altinier G., Vita F., Melato M., Satake M., Yasumoto T. Oral and intraperitoneal acute toxicity studies of yessotoxin and homoyessotoxins in mice. Toxicon 2003, 41:783-792.
68. Tubaro A., Giangaspero A., Ardizzone M., Soranzo M.R., Vita F., Yasumoto T., Maucher J.M., Ramsdell J.S., Sosa S. Ultrastructural damage to heart tissue from repeated oral exposure to yessotoxin resolves in three months. Toxicon 2008, 51:1225-1235.
69. Ujihara S., Oishi T., Mouri R., Tamate R., Konoki K., Matsumori N., Murata M., Oshima Y., Sugiyama N., Tomita M., Ishihama Y. Detection of Rap1A as a yessotoxin binding protein from blood cell membranes. Bioorg. Med. Chem. Lett. 2010, 20:6443-6446.
70. Wyllie A.H. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 1980, 284:555-556.
71. Young C., Truman P., Boucher M., Keyzers R., Northcote P., Jordan W.T. The algal metabolite yessotoxin affects heterogeneous nuclear ribonucleoproteins in HepG2 cells. Proteomics 2009, 9:2529-2542.