Interactions between ABC-transport proteins and the secondary Fusarium metabolites enniatin and beauvericin

Molecular Nutrition and Food Research

Volumn 53, Issue 7, 2009, Pages 904-920

  Dornetshuber, Rita ^a,b   Heffeter, Petra ^b   Sulyok, Michael ^c   Schumacher, Rainer ^c   Chiba, Peter ^d   Kopp, Stephan ^d   Koellensperger, Gunda ^c   Micksche, Michael ^b   Lemmens Gruber, Rosa ^a   Berger, Walter ^b  

^a UNIVERSITY OF VIENNA   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

ABC transport proteins; Beauvericin; Enniatin; Multidrug resistance; Mycotoxins

Indexed keywords

ABC TRANSPORTER; ABCB1 PROTEIN, HUMAN; ABCG2 PROTEIN, HUMAN; BEAUVERICIN; CALCIUM; DEPSIPEPTIDE; ENNIATINS; GLYCOPROTEIN P; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE-ASSOCIATED PROTEIN 1; MYCOTOXIN; TUMOR PROTEIN;

ARTICLE; DRUG RESISTANCE; FUSARIUM; HUMAN; METABOLISM; PATHOGENICITY; PHYSIOLOGY; TUMOR CELL LINE;

ATP-BINDING CASSETTE TRANSPORTERS; CALCIUM; CELL LINE, TUMOR; DEPSIPEPTIDES; DRUG RESISTANCE, NEOPLASM; FUSARIUM; HUMANS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MYCOTOXINS; NEOPLASM PROTEINS; P-GLYCOPROTEIN;

FUSARIUM;

EID: 68149124662     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.200800384     Document Type: Article

References (56)

1. Klyszejko, A., Kubus, Z., Zakowska, Z., Mycological analysis of cereal samples and screening of Fusarium strains' ability to form deoxynivalenole (DON) and zearalenone (ZEA) mycotoxins - A pilot study, Pol. J. Microbiol. 2005, 54 (Suppl.), 21-25.
2. Jestoi, M., Rokka, M., Yli-Mattila, T., Parikka, P., et al., Presence and concentrations of the Fusarium-related mycotoxins beauvericin, enniatins and moniliformin in finnish grain samples, Food Addit. Contam. 2004, 21, 794-802.
3. Wilson, J. P., Jurjevic, Z., Hanna, W. W., Wilson, D. M., et al., Host-specific variation in infection by toxigenic fungi and contamination by mycotoxins in pearl millet and corn, Mycopathologia 2006, 161, 101-107.
4. Tomoda, H., Huang, X. H., Cao, J., Nishida, H., et al., Inhibition of acyl-CoA: Cholesterol acyltransferase activity by cyclodepsipeptide antibiotics, J. Antibiot. (Tokyo) 1992, 45, 1626-1632.
5. Kamyar, M., Rawnduzi, P., Studenik, C. R., Kouri, K., Lemmens-Gruber, R., Investigation of the electrophysiological properties of enniatins, Arch. Biochem. Biophys. 2004, 429, 215-223.
6. Kouri, K., Kamyar, M. R., Lemmens-Gruber, R., Actions of the antibiotic mycotoxins beauvericin and enniatin on mammalian tissue, Forum Nutr. 2003, 56, 413-414.
7. Kamyar, M. R., Kouri, K., Rawnduzi, P., Studenik, C., Lemmens-Gruber, R., Effects of moniliformin in presence of cyclohexadepsipeptides on isolated mammalian tissue and cells, Toxicol. In Vitro 2006, 20, 1284-1291.
8. Calo, L., Fornelli, F., Ramires, R., Nenna, S., et al., Cytotoxic effects of the mycotoxin beauvericin to human cell lines of myeloid origin, Pharmacol. Res. 2004, 49, 73-77.
9. Calo, L., Fornelli, F., Nenna, S., Tursi, A., et al., Beauvericin cytotoxicity to the invertebrate cell line SF-9, J. Appl. Genet. 2003,44,515-520.
10. Jow, G. M., Chou, C. J., Chen, B. F., Tsai, J. H., Beauvericin induces cytotoxic effects in human acute lymphoblastic leukemia cells through cytochrome c release, caspase 3 activation: The causative role of calcium, Cancer Lett. 2004, 216, 165-173.
11. Zhan, J., Burns, A. M., Liu, M. X., Faeth, S. H., Gunatilaka, A. A., Search for cell motility and angiogenesis inhibitors with potential anticancer activity: Beauvericin and other constituents of two endophytic strains of Fusarium oxysporum, J. Nat. Prod. 2007, 70, 227-232.
12. Dornetshuber, R., Heffeter, P., Kamyar, M. R., Peterbauer, T., et al., Enniatin exerts p53-dependent cytostatic and p53-independent cytotoxic activities against human cancer cells, Chem. Res. Toxicol. 2007, 20, 465-473.
13. Tep, J., Videmann, B., Mazallon, M., Balleydier, S., et al., Transepithelial transport of fusariotoxin nivalenol: Mediation of secretion by ABC transporters, Toxicol. Lett. 2007, 170, 248-258.
14. Gottesman, M. M., Fojo, T., Bates, S. E., Multidrug resistance in cancer: Role of ATP-dependent transporters, Nat. Rev. Cancer 2002, 2, 48-58.
15. Shen, D. W., Cardarelli, C., Hwang, J., Cornwell, M., et al., Multiple drug-resistant human KB carcinoma cells independently selected for high-level resistance to colchicine, adriamycin, or vinblastine show changes in expression of specific proteins, J. Biol. Chem. 1986, 261, 7762-7770.
16. McGrath, T., Center, M. S., Mechanisms of multidrug resistance in HL60 cells: Evidence that a surface membrane protein distinct from P-glycoprotein contributes to reduced cellular accumulation of drug, Cancer Res. 1988, 48, 3959-3963.
17. Zijlstra, J. G., de Vries, E. G., Mulder, N. H., Multifactorial drug resistance in an adriamycin-resistant human small cell lung carcinoma cell line, Cancer Res. 1987, 47, 1780-1784.
18. Elbling, L., Berger, W., Weiss, R. M., Printz, D., et al., A novel bioassay for P-glycoprotein functionality using cytochalasin D, Cytometry 1998, 31, 187-198.
19. Doyle, L. A., Yang, W., Abruszzo, L. V., Krogmann, T., et al., A multidrug resistance transporter from human MCF-7 breast cancer cells, Proc. Natl. Acad. Sci. USA 1998, 95, 15665-15670.
20. Schmid, D., Ecker, G., Kopp, S., Hitzler, M., Chiba, P., Structure-activity relationship studies of propafenone analogs based on P-glycoprotein ATPase activity measurements, Biochem. Pharmacol. 1999, 58, 1447-1456.
21. Shi, Z., Peng, X. X., Kim, I. W., Shukla, S., et al., Erlotinib(Tarceva, OSI-774) antagonizes ATP-binding cassette subfamily B member 1 and ATP-binding cassette subfamily G member 2-mediated drug resistance, Cancer Res. 2007, 67, 11012-11020.
22. Sulyok, M., Berthiller, F., Krska, R., Schuhmacher, R., Development and validation of a liquid chromatography/tandem mass spectrometric method for the determination of 39 mycotoxins in wheat and maize, Rapid Commun. Mass Spectrom. 2006,20,2649-2659.
23. Heffeter, P., Pongratz, M., Steiner, E., Chiba, P., et al., Intrinsic and acquired forms of resistance against the anticancer ruthenium compound KP1019 [indazolium trans-[tetrachlorobis(1H-indazole)ruthenate (III)] (FFC14A), J. Pharmacol. Exp. Ther. 2005, 312, 281-289.
24. Hirohashi, T., Suzuki, H., Chu, X. Y., Tamai, I., et al., Function and expression of multidrug resistance-associated protein family in human colon adenocarcinoma cells (Caco-2), J. Pharmacol. Exp. Ther. 2000, 292, 265-270.
25. Steiner, E., Holzmann, K., Elbling, L., Micksche, M., Berger, W., Cellular functions of vaults and their involvement in multidrug resistance, Curr. Drug Targets 2006, 7, 923-934.
26. Fojo, T., Bates, S., Strategies for reversing drug resistance, Oncogene 2003, 22, 7512-7523.
27. Robey, R. W., Steadman, K., Polgar, O., Morisaki, K., et al., Pheophorbide a is a specific probe for ABCG2 function and inhibition, Cancer Res. 2004, 64, 1242-1246.
28. Heffeter, P., Jakupec, M. A., Korner, W., Chiba, P., et al., Multidrug-resistant cancer cells are preferential targets of the new antineoplastic lanthanum compound KP772 (FFC24), Biochem. Pharmacol. 2007, 73, 1873-1886.
29. Logrieco, A., Rizzo, A., Ferracane, R., Ritieni, A., Occurrence of beauvericin and enniatins in wheat affected by Fusarium avenaceum head blight, Appl. Environ. Microbiol. 2002, 68,82-85.
30. Uhlig, S., Jestoi, M., Parikka, P., Fusarium avenaceum The North European situation, Int. J. Food Microbiol. 2007, 119, 17-24.
31. Leitgeb, R., Lew, H., Khidr, R., Böhm, J., et al., Influence of Fusarium toxins on growth and carcass characteristics of turkeys, Die Bodenkultur 2000, 52, 171-178.
32. Leitgeb, R., Lew, H., Wetscherek, W., Böhm, J., Quinz, A., Influence of fusariotoxins on growing and slaughtering performance of broilers, Die Bodenkultur 1999, 50, 67-66.
33. McKee, T. C., Bokesch, H. R., McCormick, J. L., Rashid, M. A., et al., Isolation and characterization of new anti-HIVand cytotoxic leads from plants, marine, and microbial organisms, J. Nat. Prod. 1997, 60, 431-438.
34. Lin, H. I., Lee, Y. J., Chen, B. F., Tsai, M. C., et al., Involvement of Bcl-2 family, cytochrome c and caspase 3 in induction of apoptosis by beauvericin in human nonsmall cell lung cancer cells, Cancer Lett. 2005, 230, 248-259.
35. Fricker, G., Miller, D. S., Relevance of multidrug resistance proteins for intestinal drug absorption in vitro and in vivo, Pharmacol. Toxicol. 2002, 90, 5-13.
36. Litman, T., Druley, T. E., Stein, W. D., Bates, S. E., From MDR to MXR: New understanding of multidrug resistance systems, their properties and clinical significance, Cell Mol. Life Sci. 2001, 58, 931-959.
37. Kino, K., Taguchi, Y., Yamada, K., Komano, T., Ueda, K., Aureobasidin A, an antifungal cyclic depsipeptide antibiotic, is a substrate for both human MDR1 and MDR2/P-glycoproteins, FEBS Lett. 1996, 399, 29-32.
38. Tiberghien, F., Kurome, T., Takesako, K., Didier, A., et al., Aureobasidins: Structure-activity relationships for the inhibition of the human MDR1 P-glycoprotein ABC-transporter, J. Med. Chem. 2000, 43, 2547-2556.
39. Hiraga, K., Yamamoto, S., Fukuda, H., Hamanaka, N., Oda, K., Enniatin has a new function as an inhibitor of Pdr5p, one of the ABC transporters in Saccharomyces cerevisiae, Biochem. Biophys. Res. Commun. 2005, 328, 1119-1125.
40. Jestoi, M., Emerging fusarium-mycotoxins fusaproliferin, beauvericin, enniatins, and moniliformin: A review, Crit. Rev. Food Sci. Nutr. 2008, 48, 21-49.
41. Kouri, K., Lemmens, M., Lemmens-Gruber, R., Beauvericininduced channels in ventricular myocytes and liposomes, Biochim. Biophys. Acta 2003, 1609, 203-210.
42. Prime-Chapman, H. M., Fearn, R. A., Cooper, A. E., Moore, V., Hirst, B. H., Differential multidrug resistance-associated protein 1 through 6 isoform expression and function in human intestinal epithelial Caco-2 cells, J. Pharmacol. Exp. Ther. 2004,311,476-484.
43. De Angelis, I., Frigge, G., Raimondi, F., Stammati, A., et al., Absorption of fumonisin B1 and aminopentol on an in vitro model of intestinal epithelium; the role of P-glycoprotein, Toxicon 2005, 45, 285-291.
44. Videmann, B., Tep, J., Cavret, S., Lecoeur, S., Epithelial transport of deoxynivalenol: Involvement of human P-glycoprotein (ABCB1) and multidrug resistance-associated protein 2 (ABCC2), Food Chem. Toxicol. 2007, 45, 1938-1947.
45. Ozvegy-Laczka, C., Cserepes, J., Elkind, N. B., Sarkadi, B., Tyrosine kinase inhibitor resistance in cancer: Role of ABC multidrug transporters, Drug Resist. Updat. 2005, 8, 15-26.
46. Klaric, M. S., Pepeljnjak, S., Domijan, A. M., Petrik, J., Lipid peroxidation and glutathione levels in porcine kidney PK15 cells after individual and combined treatment with fumonisin B(1), beauvericin and ochratoxin A, Basic Clin. Pharmacol. Toxicol. 2007, 100, 157-164.
47. Polgar, O., Robey, R. W., Bates, S. E., ABCG2: Structure, function and role in drug response, Expert Opin. Drug Metab. Toxicol. 2008, 4, 1-15.
48. Ivanov, V. T., Evstratov, A. V., Sumskaya, L. V., Melnik, E. I., et al., Sandwich complexes as a functional form of the enniatin ionophores, FEBS Lett. 1973, 36, 65-71.
49. Jestoi, M., Rokka, M., Peltonen, K., An integrated sample preparation to determine coccidiostats and emerging Fusarium-mycotoxins in various poultry tissues with LC-MS/MS, Mol. Nutr. Food Res. 2007, 51, 625-637.
50. Sharom, F. J., Lu, P., Liu, R., Yu, X., Linear and cyclic peptides as substrates and modulators of P-glycoprotein: Peptide binding and effects on drug transport and accumulation, Biochem. J. 1998, 333, 621-630.
51. Ozvegy, C., Litman, T., Szakacs, G., Nagy, Z., et al., Functional characterization of the human multidrug transporter, ABCG2, expressed in insect cells, Biochem. Biophys. Res. Commun. 2001, 285, 111-117.
52. Robey, R. W., Honjo, Y., van de Laar, A., Miyake, K., et al., A functional assay for detection of the mitoxantrone resistance protein, MXR (ABCG2), Biochim. Biophys. Acta 2001, 1512, 171-182.
53. Sarkadi, B., Ozvegy-Laczka, C., Nemet, K., Varadi, A., ABCG2 A transporter for all seasons, FEBS Lett. 2004, 567,116-120.
54. Kok, J. W., Veldman, R. J., Klappe, K., Koning, H., et al., Differential expression of sphingolipids in MRP1 overexpressing HT29 cells, Int. J. Cancer 2000, 87, 172-178.
55. Stewart, D. J., Mechanisms of resistance to cisplatin and carboplatin, Crit. Rev. Oncol. Hematol. 2007, 63, 12-31.
56. Berger, W., Elbling, L., Micksche, M., Expression of the major vault protein LRP in human nonsmall-cell lung cancer cells: Activation by short-term exposure to antineoplastic drugs, Int. J. Cancer 2000, 88, 293-300.