Comparative effects of the marine algal toxins azaspiracid-1, -2, and -3 on jurkat T lymphocyte cells

Chemical Research in Toxicology

Volumn 25, Issue 3, 2012, Pages 747-754

  Twiner, Michael J ^a   El Ladki, Racha ^a   Kilcoyne, Jane ^b   Doucette, Gregory J ^c  

^a UNIVERSITY OF MICHIGAN DEARBORN   (United States)

^b MARINE INSTITUTE   (Ireland)

^c CENTER FOR COASTAL ENVIRONMENTAL HEALTH AND BIOMOLECULAR RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; AZASPIRACID; AZASPIRACID 1; AZASPIRACID 2; AZASPIRACID 3; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; CYTOTOXICITY; FLUORESCENCE IMAGING; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKEMIA CELL LINE; NONHUMAN; T LYMPHOCYTE;

ACTINS; ANIMALS; CELL SURVIVAL; DINOFLAGELLIDA; FURANS; HUMANS; JURKAT CELLS; MARINE TOXINS; MYTILUS EDULIS; PSEUDOPODIA; PYRANS; SPIRO COMPOUNDS; T-LYMPHOCYTES;

ALGAE; DINOPHYCEAE;

EID: 84858694033     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx200553p     Document Type: Article

References (50)

1. Tillmann, U., Elbrächter, M., Krock, B., John, U., and Cembella, A. (2009) Azadinium spinosum gen. et sp. nov. (Dinophyceae) identified as a primary producer of azaspiracid toxins. Eur. J. Phycol. 44, 63-79.
2. Furey, A., O'Doherty, S., O'Callaghan, K., Lehane, M., and James, K. J. (2010) Azaspiracid poisoning (AZP) toxins in shellfish: Toxicological and health considerations. Toxicon 56, 173-190.
3. Klontz, K. C., Abraham, A., Plakas, S. M., and Dickey, R. W. (2009) Mussel-associated azaspiracid intoxication in the United States. Ann. Intern. Med. 150, 361.
4. Taleb, H., Vale, P., Amanhir, R., Benhadouch, A., Sagou, R., and Chafik, A. (2006) First detection of azaspiracids in mussels in north west Africa. J. Shellfish Res. 25, 1067-1070. (Pubitemid 46025294)
5. Álvarez, G., Uribe, E., Ávalos, P., Mariño, C., and Blanco, J. (2010) First identification of azaspiracid and spirolides in Mesodesma donacium and Mulinia edulis from Northern Chile. Toxicon 55, 638-641.
6. Ueoka, R., Ito, A., Izumikawa, M., Maeda, S., Takagi, M., Shin-ya, K., Yoshida, M., van Soest, R. W. M., and Matsunaga, S. (2009) Isolation of azaspiracid-2 from a marine sponge Echinoclathria sp. as a potent cytotoxin. Toxicon 53, 680-684.
7. Twiner, M. J., Rehmann, N., Hess, P., and Doucette, G. J. (2008) Azaspiracid shellfish poisoning: A review on the chemistry, ecology, and toxicology with an emphasis on human health impacts. Mar. Drugs 6, 39-72. (Pubitemid 351919074)
8. Rehmann, N., Hess, P., and Quilliam, M. (2008) Discovery of new analogs of the marine biotoxin azaspiracid in blue mussels (Mytilus edulis) by ultra-performance liquid chromatography/tandem mass spectrometry. Rapid Commun. Mass Spectrom. 22, 549-558. (Pubitemid 351300590)
9. James, K. J., Sierra, M. D., Lehane, M., Braña Magdalena, A., and Furey, A. (2003) Detection of five new hydroxyl analogues of azaspiracids in shellfish using multiple tandem mass spectrometry. Toxicon 41, 277-283. (Pubitemid 36144165)
10. Rundberget, T., Sandvik, M., Hovgaard, P., Nguyen, L., Aasen, J. A. B., Castberg, T., Gustad, E., and Miles, C. O. (2006) Use of SPATT Disks in Norway: Detection of AZAs & DTXs and Comparison with Algal Cell Counts and Toxin Profiles in Shellfish, in Marine Biotoxin Science Workshop No 23, pp 35-38, NZFSA, Wellington, New Zealand.
11. Krock, B., Tillmann, U., John, U., and Cembella, A. D. (2009) Characterization of azaspiracids in plankton size-fractions and isolation of an azaspiracid-producing dinoflagellate from the North Sea. Harmful Algae 8, 254-263.
12. Tillmann, U., Elbrächter, M., John, U., Krock, B., and Cembella, A. (2010) Azadinium obesum (Dinophyceae), a new nontoxic species in the genus that can produce azaspiracid toxins. Phycologia 49, 169-182.
13. James, K. J., Fidalgo Saez, M. J., Furey, A., and Lehane, M. (2004) Azaspiracid poisoning, the food-borne illness associated with shellfish consumption. Food Addit. Contam. 21, 879-892. (Pubitemid 39490008)
14. James, K. J., Furey, A., Satake, M., and Yasumoto, T. (2001) Azaspiracid Poisoning (AZP): A New Shellfish Toxic Syndrome in Europe, in Harmful Algal Blooms 2000 (Hallegraeff, G. M., Blackburn, S. I., Bolch, C. J., and Lewis, R. J., Eds.) pp 250-253, Intergovernmental Oceanographic Commission of UNESCO, Paris, France.
15. Nzoughet, J. K., Hamilton, J. T. G., Botting, C. H., Douglas, A., Devine, L., Nelson, J., and Elliott, C. T. (2009) Proteomics identification of azaspiracid toxin biomarkers in blue mussels, Mytilus edulis. Mol. Cell. Proteomics 8.8, 1811-1822.
16. Nzoughet, K. J., Hamilton, J. T. G., Floyd, S. D., Douglas, A., Nelson, J., Devine, L., and Elliott, C. T. (2008) Azaspiracid: First evidence of protein binding in shellfish. Toxicon 51, 1255-1263.
17. Ito, E., Satake, M., Ofuji, K., Higashi, M., Harigaya, K., McMahon, T., and Yasumoto, T. (2002) Chronic effects in mice caused by oral administration of sublethal doses of azaspiracid, a new marine toxin isolated from mussels. Toxicon 40, 193-203. (Pubitemid 33016549)
18. Ito, E., Satake, M., Ofuji, K., Kurita, N., McMahon, T., James, K., and Yasumoto, T. (2000) Multiple organ damage caused by a new toxin azaspiracid, isolated from mussels produced in Ireland. Toxicon 38, 917-930. (Pubitemid 30084733)
19. Ito, E., Terao, K., McMahon, T., Silke, J., and Yasumoto, T. (1998) Acute Pathological Changes in Mice Caused by Crude Extracts of Novel Toxins Isolated from Irish Mussels, in Harmful Algae (Reguera, B., Blanco, J., Fernandez, M. L., and Wyatt, T., Eds.) pp 588-589, Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO, Santiago de Compostela, Spain.
20. Satake, M., Ofuji, K., James, K. J., Furey, A., and Yasumoto, T. (1998) New Toxic Event Caused by Irish Mussels, in Harmful Algae (Reguera, B., Blanco, J., Fernandez, M. L., and Wyatt, T., Eds.) pp 468-469, Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO, Santiago de Compostela, Spain.
21. Ofuji, K., Satake, M., McMahon, T., Silke, J., James, K. J., Naoki, H., Oshima, Y., and Yasumoto, T. (1999) Two analogs of azaspiracid isolated from mussels, Mytilus edulis, involved in human intoxication in Ireland. Nat. Toxins 7, 99-102.
22. Ofuji, K., Satake, M., McMahon, T., James, K. J., Naoki, H., Oshima, Y., and Yasumoto, T. (2001) Structures of azaspiracid analogs, azaspiracid-4 and azaspiracid-5, causative toxins of azaspiracid poisoning in Europe. Biosci. Biotechnol. Biochem. 65, 740-742. (Pubitemid 33615955)
23. EFSA (2008) Marine biotoxins in shellfish - Azaspiracid group: scientific opinion of the Panel on Contaminants in the Food chain. EFSA J. 723, 1-52.
24. Twiner, M. J., Hess, P., Bottein Dechraoui, M.-Y., McMahon, T., Samons, M. S., Satake, M., Yasumoto, T., Ramsdell, J. S., and Doucette, G. J. (2005) Cytotoxic and cytoskeletal effects of azaspiracid-1 on mammalian cell lines. Toxicon 45, 891-900. (Pubitemid 40719792)
25. Vale, C., Nicolaou, K. C., Frederick, M. O., Gomez-Limia, B., Alfonso, A., Vieytes, M. R., and Botana, L. M. (2007) Effects of azaspiracid-1, a potent cytotoxic agent, on primary neuronal cultures. A structure-activity relationship study. J. Med. Chem. 50, 356-363. (Pubitemid 46147715)
26. Vilariño, N. (2008) Marine toxins and the cytoskeleton: azaspiracids. FEBS J. 275, 6075-6081.
27. Vilariño, N., Nicolaou, K. C., Frederick, M. O., Cagide, E., Ares, I. R., Louzao, M. C., Vieytes, M. R., and Botana, L. M. (2006) Cell growth inhibition and actin cytoskeleton disorganization induced by azaspiracid-1 structure-activity studies. Chem. Res. Toxicol. 19, 1459-1466. (Pubitemid 44863488)
28. 2+entry by stored operated channels in human T lymphocytes. Biochem. Pharmacol. 69, 1627-1636.
29. 2+], and pH. Chem. Res. Toxicol. 17, 1338-1349.
30. Kellmann, R., Schaffner, C. A. M., Grønset, T. A., Satake, M., Ziegler, M., and Fladmark, K. E. (2009) Proteomic response of human neuroblastoma cells to azaspiracid-1. J. Proteomics 72, 695-707.
31. Cao, Z., LePage, K. T., Frederick, M. O., Nicolaou, K. C., and Murray, T. F. (2010) Involvement of caspase activation in azaspiracid-induced neurotoxicity in neocortical neurons. Toxicol. Sci. 114, 323-334.
32. Kulagina, K. V., Twiner, M. J., Hess, P., McMahon, T., Satake, M., Yasumoto, T., Ramsdell, J. S., Doucette, G. J., Ma, W., and O'Shaughnessy, T. J. (2006) Azaspiracid-1 inhibits bioelectrical activity of spinal cord neuronal networks. Toxicon 47, 766-773. (Pubitemid 43766829)
33. Vale, C., Gomez-Limia, B., Nicolaou, K. C., Frederick, M. O., Vieytes, M. R., and Botana, L. M. (2007) The c-Jun-N-terminal kinase is involved in the neurotoxic effect of azaspiracid-1. Cell Physiol. Biochem. 20, 957-966. (Pubitemid 350059738)
34. Vale, C., Nicolaou, K. C., Frederick, M. O., Vieytes, M. R., and Botana, L. M. (2010) Cell volume decrease as a link between azaspiracid-induced cytotoxicity and c-Jun-N-terminal kinase activation in cultured neurons. Toxicol. Sci. 113, 158-168.
35. 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.
36. Twiner, M. J., Ryan, J. C., Morey, J. S., Smith, K. J., Hammad, S. M., Van Dolah, F. M., Hess, P., McMahon, T., Satake, M., Yasumoto, T., and Doucette, G. J. (2008) Transcriptional profiling and inhibition of cholesterol biosynthesis in human lymphocyte T cells by the marine toxin azaspiracid. Genomics 91, 289-300.
37. Colman, J. R., Twiner, M. J., Hess, P., McMahon, T., Satake, M., Yasumoto, T., Doucette, G. J., and Ramsdell, J. S. (2005) Teratogenic effects of azaspiracid-1 identified by microinjection of Japanese medaka (Oryzias latipes) embryos. Toxicon 45, 881-890. (Pubitemid 40719791)
38. Roman, Y., Alfonso, A., Louzao, M. C., de la Rosa, L. A., Leira, F., Vieites, J. M., Vieytes, M. R., Ofuji, K., Satake, M., Yasumoto, T., and Botana, L. M. (2002) Azaspiracid-1, a potent, nonapoptotic new phycotoxin with several cell targets. Cell. Signalling 14, 703-716. (Pubitemid 34518624)
39. Vilariño, N., Nicolaou, K. C., Frederick, M. O., Vieytes, M. R., and Botana, L. M. (2007) Irreversible cytoskeletal disarrangement is independent of caspase activation during in vitro azaspiracid toxicity in human neuroblastoma cells. Biochem. Pharmacol. 74, 327-335. (Pubitemid 46890814)
40. Ito, E., Frederick, M. O., Koftis, T. V., Tang, W., Petrovic, G., Ling, T., and Nicolaou, K. C. (2006) Structure toxicity relationships of synthetic azaspiracid-1 and analogs in mice. Harmful Algae 5, 586-591. (Pubitemid 44311078)
41. Alfonso, A., Vieytes, M. R., Ofuji, K., Satake, M., Nicolaou, K. C., Frederick, M. O., and Botana, L. M. (2006) Azaspiracids modulate intracellular pH levels in human lymphocytes. Biochem. Biophys. Res. Commun. 346, 1091-1099.
42. Alfonso, C., Alfonso, A., Otero, P., Rodriguez, P., Vieytes, M. R., Elliott, C. T., Higgins, C., and Botana, L. M. (2008) Purification of five azaspiracids from mussel samples contaminated with DSP toxins and azaspiracids. J. Chromatogr., B 865, 133-140.
43. Nicolaou, K. C., Koftis, T. V., Vyskocil, S., Petrovic, G., Ling, T., Yamada, T. M. A., Tang, W., and Frederick, M. O. (2004) Structural revision and total synthesis of azaspiracid-1, Part 2: Definition of the ABCD domain and total synthesis. Angew. Chem. Int. Ed 43, 4318-4324. (Pubitemid 39257409)
44. Nicolaou, K. C., Koftis, T. V., Vyskocil, S., Petrovic, G., Tang, W., Frederick, M. O., Chen, D. Y. K., Yiwei, L., Ling, T., and Yamada, T. M. A. (2004) Total synthesis and structural elucidation of azaspiracid-1. Final assigment and total synthesis of the correct structure of azaspiracid-1. J. Am. Chem. Soc. 128, 2859-2872.
45. Perez, R., Rehmann, N., Crain, S., LeBlanc, P., Craft, C., MacKinnon, S., Reeves, K., Burton, I., Walter, J., Hess, P., Quilliam, M., and Melanson, J. (2010) The preparation of certified calibration solutions for azaspiracid-1, -2, and -3, potent marine biotoxins found in shellfish. Anal. Bioanal. Chem. 398, 2243-2252.
46. Kilcoyne, J., Keogh, A., Clancy, G., Le Blanc, P., Burton, I., Quilliam, M., Hess, P., and Miles, C. O. (2012) Improved isolation procedure for azaspiracids from shellfish, structural elucidation of azaspiracid-6 and stability studies. J. Agric. Food Chem., DOI 10.1021/jf2048788.
47. Satake, M., Ofuji, K., Naoki, H., James, K. J., Furey, A., McMahon, T., Silke, J., and Yasumoto, T. (1998) Azaspiracid, a new marine toxin having unique spiro ring assemlies, isolated from Irish mussels Mytilus edulis. J. Amer. Chem. Soc. 120, 9967-9968. (Pubitemid 28462514)
48. Ronzitti, G., Hess, P., Rehmann, N., and Rossini, G. P. (2007) Azaspiracid-1 alters the E-cadherin pool in epithelial cells. Toxicol. Sci. 95, 427-435. (Pubitemid 46152615)
49. Harris, E. S., Rouiller, I., Hanein, D., and Higgs, H. N. (2006) Mechanistic differences in actin bundling activity of two mammalian formins, FRL1 and mDia2. J. Biol. Chem. 281, 14383-14392. (Pubitemid 43848368)
50. Harris, E. S., Gauvin, T. J., Heimsath, E. G., and Higgs, H. N. (2010) Assembly of filopodia by the formin FRL2 (FMNL3). Cytoskeleton 67, 755-772.