Azaspiracid-1 inhibits endocytosis of plasma membrane proteins in epithelial cells

Toxicological Sciences

Volumn 117, Issue 1, 2010, Pages 109-121

  Bellocci, Mirella ^a   Sala, Gian Luca ^a   Callegari, Federica ^a   Rossini, Gian Paolo ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

Azaspiracid; Cytoskeleton; E cadherin; Endocytosis; Na+ K+ ATPase; Prolactin receptor; Yessotoxin

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); AZASPIRACID 1; BIOLOGICAL MARKER; CHLOROQUINE; LATRUNCULIN A; MARINE TOXIN; MEMBRANE PROTEIN; PROLACTIN RECEPTOR; PROTEINASE K; TRYPSIN; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; ARTICLE; BIOTINYLATION; CELL MEMBRANE; CELL STRAIN CACO 2; CELL STRAIN MCF 7; CELL SURFACE; COMPETITIVE INHIBITION; CONTROLLED STUDY; DOG; ENDOCYTOSIS; EPITHELIUM CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOREACTIVITY; KIDNEY EPITHELIUM; MEMBRANE STRUCTURE; MOLECULAR MIMICRY; NONHUMAN; PROTEIN DEGRADATION; PROTEIN LOCALIZATION;

BICYCLO COMPOUNDS, HETEROCYCLIC; CADHERINS; CELL LINE, TUMOR; CHLOROQUINE; ENDOCYTOSIS; EPITHELIAL CELLS; HUMANS; MARINE TOXINS; MEMBRANE PROTEINS; SPIRO COMPOUNDS; SUBCELLULAR FRACTIONS; THIAZOLIDINES;

EID: 77955874348     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq172     Document Type: Article

References (53)

1. Ayscough, KR(2005). Coupling actin dynamics to the endocytotic process in Saccharomyces cerevisiae. Protoplasma 226, 81-88.
2. Birchmeier, W., and Behrens, J. (1994). Cadherin expression in carcinomas: role in the formation of cell junctions and the prevention of invasiveness. Biochim. Biophys. Acta 1198, 11-26.
3. Callegari, F., and Rossini, G. P. (2008). Yessotoxin inhibits the complete degradation of E-cadherin. Toxicology 244, 133-144.
4. Cao, Z., Lepage, KT., Frederick, M. O., Nicolaou, KC., and Murray, T. F. (2010). Involvement of caspase activation in azaspiracid-induced neurotoxicity in neocortical neurons. Toxicol. Sci. 114, 323-334.
5. Clevenger, C. V., Gadd, S. L., and Zheng, J. (2009). New mechanisms for PRLr action in breast canceRTrends Endocrinol. Metab. 20, 223-229.
6. Ebeling, W., Hennrich, N., Klockow, M., Metz, H., Orth, H. D., and Lang, H. (1974). Proteinase K from Tritirachium album LimbeREuRJ. Biochem. 47, 91-97.
7. Elia, G. (2008). Biotinylation reagents for the study of cell surface proteins. Proteomics 8, 4012-4024.
8. European Food Safety Authority. (2008). Marine biotoxins in shellfish- azaspiracid group. Scientific Opinion of the Panel on Contaminants in the Food chain. EFSA J. 723, 1-52.
9. Fogh, J., Fogh, J. M., and Orfeo, T. (1977). One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice. J. Natl. Cancer Inst. 59, 221-226.
10. Fu, D., and Roufogalis, B. D. (2007). Actin disruption inhibits endosomal traffic of P-glycoprotein-EGFP and resistance to daunorubicin accumulation. Am. J. Cell Physiol. 292, C1543-C1552.
11. Gaush, C. R., Hard, W. L., and Smith, T. F. (1966). Characterization of an established line of canine kidney cells (MDCK). Proc. Soc. Exp. Biol. Med. 122, 931-935.
12. Goldstein, J. L., and Brown, M. S. (2009). The LDL receptoRArterioscleRThromb. Vasc. Biol. 29, 431-438.
13. Gumbiner, B. M. (2000). Regulation of cadherin adhesive activity. J. Cell Biol. 148, 399-403.
14. Hirano, S., Nose, A., Hatta, K., Kawatami, A., and Takeichi, M. (1987). Calcium-dependent cell-cell adhesion molecules (cadherins): subclass specificities and possible involvement of actin bundles. J. Cell Biol. 105, 2501-2510.
15. Hoe, H. S., and Rebeck, G. W. (2005). Regulation of ApoE receptor proteolysis by ligand binding. Brain Res. Mol. Brain Res. 137, 31-39.
16. Hyafil, F., Babinet, C., and Jacob, F. (1981). Cell-cell interactions in early embryogenesis: a molecular approach to the role of calcium. Cell 26, 447-454.
17. Ito, E., Frederick, M. O., Koftis, T. V., Tang, W., Petrovic, G., Ling, T., and Nicolaou, KC. (2006). Structure toxicity relationships of synthetic azaspiracid-1 and analogs in mice. Harmful Algae 5, 586-591.
18. 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.
19. 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.
20. Kaushal, G. P., Kaushal, V., Jerzog, C., and Yang, C. (2008). Autophagy delays apoptosis in renal tubular epithelial cells in cisplatin cytotoxicity. Autophagy 4, 710-712.
21. Kellman, R., Schaffner, C. A. M., Grønset, T. A., Satake, M., Ziegler, M., and Fladmark, KE. (2009). Proteomic response of human neuroblastoma cells to azaspiracid-1. J. Proteomics 72, 695-707.
22. Kühlbrandt, W. (2004). Biology, structure and mechanism of P-type ATPases. Nat. Rev. Mol. Cell Biol. 5, 282-295.
23. Kulagina, N. 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.
24. Laemmli, U. K(1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
25. Lamaze, C., Fujimoto, L. M., Yin, H. L., and Schmid, S. L. (1997). The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J. Biol. Chem. 272, 20332-20335.
26. McMahon, T., and Silke, J. (1996). Winter toxicity of unknown aetiology in mussels. Harmful Algae News 14, 2.
27. Nicolaou, KC., Chen, D. Y.-K., Li, Y., Qian, W., Ling, T., Vyskocil, S., Koftis, T. V., Govindasamy, M., and Uesaka, N. (2003b). Total synthesis of the proposed azaspiracid-1 structure, part 2: coupling of the C1-C20, C21- C27, and C28-C40 fragments and completion of the synthesis. Angew. Chem. Intl. Ed. 42, 3649-3653.
28. Nicolaou, KC., Li, Y., Uesaka, N., Koftis, T. V., Vyskocil, S., Ling, T., Govindasamy, M., Qian, W., Bernal, F., and Chen, D. Y. K(2003a). Total synthesis of the proposed azaspiracid-1 structure, part 1: construction of the enantiomerically pure C1-C20, C21-C27, and C28-C40 fragments. Angew. Chem. Intl. Ed. 42, 3643-3648.
29. 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.
30. Paterson, A. D., Parton, RG., Ferguson, C., Stow, J. L., and Yap, A. S. (2003). Characterization of E-cadherin endocytosis in isolated MCF-7 and chinese hamster ovary cells: the initial fate of unbound E-cadherin. J. Biol. Chem. 278, 21050-21057.
31. Pierotti, S., Malaguti, C., Milandri, A., Poletti, R., and Rossini, G. P. (2003). Functional assay to measure yessotoxins in contaminated mussel samples. Anal. Biochem. 312, 208-216.
32. Ronzitti, G., Callegari, F., Malaguti, C., and Rossini, G. P. (2004). Selective disruption of the E-cadherin-catenin system by an algal toxin. BRJ. Cancer 90, 1100-1107.
33. 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.
34. Ronzitti, G., and Rossini, G. P. (2008). Yessotoxin induces the accumulation of altered E-cadherin dimers that are not part of adhesive structures in intact cells. Toxicology 244, 145-156.
35. Rossini, G. P., and Hess, P. (2010). Phycotoxins: chemistry, mechanisms of action and shellfish poisoning. In Molecular, Clinical and Environmental Toxicology (A. Luch, Ed.), pp. 65-122. Birkhåuser-Verlag AG, Basel, Switzerland.
36. Satake, M., Ofuji, K., Naoki, H., James, KJ., Furey, A., McMahon, T., Silke, J., and Yasumoto, T. (1998). Azaspiracid, a new marine toxin having a unique spiro ring assemblies, isolated from Irish mussels, Mytilus edulis. J. Am. Chem. Soc. 120, 9967-9968.
37. Scita, G., and Di Fiore, P. P. (2010). The endocytic matrix. Nature 463, 464-473.
38. Shimoyama, Y., Hirohashi, S., Hirano, S., Noguchi, M., Shimosato, Y., Takeichi, M., and Abe, O. (1989). Cadherin cell-adhesion molecules in human epithelial tissues and carcinomas. Cancer Res. 49, 2128-2133.
39. Shore, E. M., and Nelson, W. J. (1991). Biosynthesis of the cell adhesion molecule uvomorulin (E-cadherin) in Madin-Darby Canine Kidney epithelial cells. J. Biol. Chem. 266, 19672-19680.
40. Singh, R., Kaushik, S., Wang, Y., Xiang, Y., Novak, I., Komatsu, M., Tanaka, K., Cuervo, A. M., and Czaja, M. J. (2009). Autophagy regulates lipid metabolism. Nature 458, 1131-1135.
41. Smith, P. K., Krohn, RI., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J., and Klenk, D. C. (1985). Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85.
42. Sorkin, A., and von Zastrow, M. (2009). Endocytosis and signalling: intertwining molecular networks. Nat. Rev. Mol. Cell Biol. 10, 609-622.
43. Tillmann, U., Elbraumlchter, M., Krock, B., John, U., and Cembella, A. (2009). Azadinium spinosum gen. et sp. nov. (Dinophyceae) identified as a primary producer of azaspiracid toxins. EuRJ. Phycol. 44, 63-79.
44. 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.
45. Twiner, M. J., Rehmann, N., Hess, P., and Doucette, G. J. (2008a). Azaspiracid shellfish poisoning: a review on the ecology, chemistry, toxicology and human health impacts. Marine Drugs 6, 39-74.
46. Twiner, M. J., Ryan, J. C., Morey, J. S., Van Dolah, F. M., Hess, P., McMahon, T., and Doucette, G. J. (2008b). Transcriptional profiling and inhibition of cholesterol biosynthesis in human T lymphocyte cells by the marine toxin azaspiracid. Genomics 91, 289-300.
47. Vale, C., Nicolaou, KC., Frederick, M. O., Gómez-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.
48. Vale, C., Nicolaou, KC., 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.
49. van Tetering, G., van Diest, P., Verlaan, I., van der Wall, E., Kopan, R., and Vooijis, M. (2009). Metalloprotease ADAM10 is required for Notch1 site 2 cleavage. J. Biol. Chem. 284, 31018-31027.
50. Vestweber, D., and Kemler, R(1985). Identification of a putative cell adhesion domain of uvomorulin. EMBO J. 4, 3393-3398.
51. Vilariño, N., Nicolaou, KC., 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.
52. Vilariño, N., Nicolaou, KC., Frederick, M. O., Vieytes, M. R., and Botana, L. M. (2007). Irreversible cytoskeletal disarrangement is in- dependent of caspase activation during in vitro azaspiracid toxicity in human neuroblastoma cells. Biochem. Pharmacol. 74, 327-335.
53. Yang, F., Yang, Y. P., Mao, C. J., Cao, B. Y., Cai, Z. L., Shi, J. J., Huang, J. Z., Zhang, P., and Liu, C. F. (2009). Role of autophagy and proteasome degradation pathways in apoptosis of PC12 cells overexpressing human alpha-synuclein. Neurosci. Lett. 454, 203-208.